Ribosomal proteins and human diseases: Pathogenesis, molecular mechanisms, and therapeutic implications

Medicinal Research Reviews

Volumn 35, Issue 2, 2015, Pages 225-285

  Wang, Wei ^a   Nag, Subhasree ^a   Zhang, Xu ^a   Wang, Ming Hai ^a   Wang, Hui ^b   Zhou, Jianwei ^c   Zhang, Ruiwen ^a  

^a TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b Chinese Academy of Sciences   (China)

^c NANJING MEDICAL UNIVERSITY   (China)

Author keywords

Cancer; Drug discovery; Ribosomal protein; Ribosomopathy; RP MDM2 p53 pathway

Indexed keywords

BIOLOGICAL MARKER; PROTEIN MDM2; PROTEIN P53; RIBOSOME PROTEIN; RIBOSOME RNA;

ANGIOGENESIS; APOPTOSIS; ARTICLE; BIOGENESIS; CARDIOVASCULAR DISEASE; CELL CYCLE REGULATION; CELL INVASION; CELL MIGRATION; CELL STRESS; CELL TRANSFORMATION; DNA REPAIR; GENE EXPRESSION REGULATION; HEMATOLOGIC DISEASE; HUMAN; METABOLIC DISORDER; MOLECULAR PATHOLOGY; NEOPLASM; NONHUMAN; NUCLEOLUS; PROTEIN DEFECT; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; REGULATORY MECHANISM; RNA PROCESSING; RNA SYNTHESIS; DISEASES; METABOLISM; MITOCHONDRION; PHYSIOLOGICAL STRESS; RIBOSOME;

CELL NUCLEOLUS; DISEASE; HUMANS; MITOCHONDRIA; RIBOSOMAL PROTEINS; RIBOSOMES; STRESS, PHYSIOLOGICAL;

EID: 84922812674     PISSN: 01986325     EISSN: 10981128     Source Type: Journal    
DOI: 10.1002/med.21327     Document Type: Article

References (378)

1. Lafontaine DL, Tollervey D. The function and synthesis of ribosomes. Nat Rev Mol Cell Biol 2001;2(7):514-520.
2. Ruggero D, Pandolfi PP. Does the ribosome translate cancer? Nat Rev Cancer 2003;3(3):179-192.
3. Boulon S, Westman BJ, Hutten S, Boisvert FM, Lamond AI. The nucleolus under stress. Mol Cell 2010;40(2):216-227.
4. Lohrum MA, Ludwig RL, Kubbutat MH, Hanlon M, Vousden KH. Regulation of HDM2 activity by the ribosomal protein L11. Cancer Cell 2003;3(6):577-587.
5. Wool IG. Extraribosomal functions of ribosomal proteins. Trends Biochem Sci 1996;21(5):164-165.
6. Warner JR, McIntosh KB. How common are extraribosomal functions of ribosomal proteins? Mol Cell 2009;34(1):3-11.
7. Lindstrom MS, Zhang Y. Ribosomal protein S9 is a novel B23/NPM-binding protein required for normal cell proliferation. J Biol Chem 2008;283(23):15568-15576.
8. Kim JH, You KR, Kim IH, Cho BH, Kim CY, Kim DG. Over-expression of the ribosomal protein L36a gene is associated with cellular proliferation in hepatocellular carcinoma. Hepatology 2004;39(1):129-138.
9. Volarevic S, Stewart MJ, Ledermann B, Zilberman F, Terracciano L, Montini E, Grompe M, Kozma SC, Thomas G. Proliferation, but not growth, blocked by conditional deletion of 40S ribosomal protein S6. Science 2000;288(5473):2045-2047.
10. He H, Sun Y. Ribosomal protein S27L is a direct p53 target that regulates apoptosis. Oncogene 2007;26(19):2707-2716.
11. Jang CY, Lee JY, Kim J. RpS3, a DNA repair endonuclease and ribosomal protein, is involved in apoptosis. FEBS Lett 2004;560(1-3):81-85.
12. Hegde V, Wang M, Deutsch WA. Human ribosomal protein S3 interacts with DNA base excision repair proteins hAPE/Ref-1 and hOGG1. Biochemistry 2004;43(44):14211-14217.
13. Kim J, Chubatsu LS, Admon A, Stahl J, Fellous R, Linn S. Implication of mammalian ribosomal protein S3 in the processing of DNA damage. J Biol Chem 1995;270(23):13620-13629.
14. Flygare J, Kiefer T, Miyake K, Utsugisawa T, Hamaguchi I, Da Costa L, Richter J, Davey EJ, Matsson H, Dahl N, Wiznerowicz M, Trono D, Karlsson S. Deficiency of ribosomal protein S19 in CD34+ cells generated by siRNA blocks erythroid development and mimics defects seen in Diamond-Blackfan anemia. Blood 2005;105(12):4627-4634.
15. Anderson SJ, Lauritsen JP, Hartman MG, Foushee AM, Lefebvre JM, Shinton SA, Gerhardt B, Hardy RR, Oravecz T, Wiest DL. Ablation of ribosomal protein L22 selectively impairs alphabeta T cell development by activation of a p53-dependent checkpoint. Immunity 2007;26(6):759-772.
16. Da Costa L, Narla G, Willig TN, Peters LL, Parra M, Fixler J, Tchernia G, Mohandas N. Ribosomal protein S19 expression during erythroid differentiation. Blood 2003;101(1):318-324.
17. Zhan Y, Melian NY, Pantoja M, Haines N, Ruohola-Baker H, Bourque CW, Rao Y, Carbonetto S. Dystroglycan and mitochondrial ribosomal protein L34 regulate differentiation in the Drosophila eye. Plos One 2010;5(5):e10488.
18. Zhang Y, Lu H. Signaling to p53: Ribosomal proteins find their way. Cancer Cell 2009;16(5):369-377.
19. Zhou X, Liao JM, Liao WJ, Lu H. Scission of the p53-MDM2 loop by ribosomal proteins. Genes Cancer 2012;3(3-4):298-310.
20. Pestov DG, Strezoska Z, Lau LF. Evidence of p53-dependent cross-talk between ribosome biogenesis and the cell cycle: Effects of nucleolar protein Bop1 on G(1)/S transition. Mol Cell Biol 2001;21(13):4246-4255.
21. Fumagalli S, Di Cara A, Neb-Gulati A, Natt F, Schwemberger S, Hall J, Babcock GF, Bernardi R, Pandolfi PP, Thomas G. Absence of nucleolar disruption after impairment of 40S ribosome biogenesis reveals an rpL11-translation-dependent mechanism of p53 induction. Nat Cell Biol 2009;11(4):501-508.
22. Sun XX, Wang YG, Xirodimas DP, Dai MS. Perturbation of 60 S ribosomal biogenesis results in ribosomal protein L5- and L11-dependent p53 activation. J Biol Chem 2010;285(33):25812-25821.
23. Narla A, Ebert BL. Ribosomopathies: Human disorders of ribosome dysfunction. Blood 2010;115(16):3196-3205.
24. Draptchinskaia N, Gustavsson P, Andersson B, Pettersson M, Willig TN, Dianzani I, Ball S, Tchernia G, Klar J, Matsson H, Tentler D, Mohandas N, Carlsson B, Dahl N. The gene encoding ribosomal protein S19 is mutated in Diamond-Blackfan anaemia. Nat Genet 1999;21(2):169-175.
25. Ebert BL, Pretz J, Bosco J, Chang CY, Tamayo P, Galili N, Raza A, Root DE, Attar E, Ellis SR, Golub TR. Identification of RPS14 as a 5q- syndrome gene by RNA interference screen. Nature 2008;451(7176):335-339.
26. Gilkes DM, Chen L, Chen J. MDMX regulation of p53 response to ribosomal stress. EMBO J 2006;25(23):5614-5625.
27. Sundqvist A, Liu G, Mirsaliotis A, Xirodimas DP. Regulation of nucleolar signalling to p53 through NEDDylation of L11. EMBO Rep 2009;10(10):1132-1139.
28. Xue S, Barna M. Specialized ribosomes: A new frontier in gene regulation and organismal biology. Nat Rev Mol Cell Biol 2012;13(6):355-369.
29. Shenoy N, Kessel R, Bhagat TD, Bhattacharyya S, Yu Y, McMahon C, Verma A. Alterations in the ribosomal machinery in cancer and hematologic disorders. J Hematol Oncol 2012;5:32.
30. Deisenroth C, Zhang Y. Ribosome biogenesis surveillance: Probing the ribosomal protein-Mdm2-p53 pathway. Oncogene 2010;29(30):4253-4260.
31. Miliani de Marval PL, Zhang Y. The RP-Mdm2-p53 pathway and tumorigenesis. Oncotarget 2011;2(3):234-238.
32. Shcherbik N, Pestov DG. Ubiquitin and ubiquitin-like proteins in the nucleolus: Multitasking tools for a ribosome factory. Genes Cancer 2010;1(7):681-689.
33. Chakraborty A, Uechi T, Kenmochi N. Guarding the 'translation apparatus': Defective ribosome biogenesis and the p53 signaling pathway. Wiley Interdiscip Rev RNA 2011;2(4):507-522.
34. Thomson E, Ferreira-Cerca S, Hurt E. Eukaryotic ribosome biogenesis at a glance. J Cell Sci 2013;126(Pt 21):4815-4821.
35. Wilson DN, Doudna Cate JH. The structure and function of the eukaryotic ribosome. Cold Spring Harb Perspect Biol 2012;4(5): a011536.
36. Klinge S, Voigts-Hoffmann F, Leibundgut M, Arpagaus S, Ban N. Crystal structure of the eukaryotic 60S ribosomal subunit in complex with initiation factor 6. Science 2011;334(6058):941-948.
37. Ben-Shem A, Garreau de Loubresse N, Melnikov S, Jenner L, Yusupova G, Yusupov M. The structure of the eukaryotic ribosome at 3.0 A resolution. Science 2011;334(6062):1524-1529.
38. Doudna JA, Rath VL. Structure and function of the eukaryotic ribosome: The next frontier. Cell 2002;109(2):153-156.
39. Fatica A, Tollervey D. Making ribosomes. Curr Opin Cell Biol 2002;14(3):313-318.
40. Ciganda M, Williams N. Eukaryotic 5S rRNA biogenesis. Wiley Interdiscip Rev RNA 2011;2(4):523-533.
41. Lo KY, Li Z, Bussiere C, Bresson S, Marcotte EM, Johnson AW. Defining the pathway of cytoplasmic maturation of the 60S ribosomal subunit. Mol Cell 2010;39(2):196-208.
42. Rouquette J, Choesmel V, Gleizes PE. Nuclear export and cytoplasmic processing of precursors to the 40S ribosomal subunits in mammalian cells. EMBO J 2005;24(16):2862-2872.
43. Choesmel V, Fribourg S, Aguissa-Toure AH, Pinaud N, Legrand P, Gazda HT, Gleizes PE. Mutation of ribosomal protein RPS24 in Diamond-Blackfan anemia results in a ribosome biogenesis disorder. Hum Mol Genet 2008;17(9):1253-1263.
44. Flygare J, Aspesi A, Bailey JC, Miyake K, Caffrey JM, Karlsson S, Ellis SR. Human RPS19, the gene mutated in Diamond-Blackfan anemia, encodes a ribosomal protein required for the maturation of 40S ribosomal subunits. Blood 2007;109(3):980-986.
45. Idol RA, Robledo S, Du HY, Crimmins DL, Wilson DB, Ladenson JH, Ladenson JH, Bessler M, Mason PJ. Cells depleted for RPS19, a protein associated with Diamond Blackfan Anemia, show defects in 18S ribosomal RNA synthesis and small ribosomal subunit production. Blood Cells Mol Dis 2007;39(1):35-43.
46. O'Donohue MF, Choesmel V, Faubladier M, Fichant G, Gleizes PE. Functional dichotomy of ribosomal proteins during the synthesis of mammalian 40S ribosomal subunits. J Cell Biol 2010;190(5):853-866.
47. Panse VG, Johnson AW. Maturation of eukaryotic ribosomes: Acquisition of functionality. Trends Biochem Sci 2010;35(5):260-266.
48. Gould HJ, Martini OH, King HS. 80S ribosomal proteins. Biochem J 1972;129(3):31P-32P.
49. Korobeinikova AV, Garber MB, Gongadze GM. Ribosomal proteins: Structure, function, and evolution. Biochemistry (Mosc) 2012;77(6):562-574.
50. Nissen P, Hansen J, Ban N, Moore PB, Steitz TA. The structural basis of ribosome activity in peptide bond synthesis. Science 2000;289(5481):920-930.
51. Barth-Baus D, Stratton CA, Parrott L, Myerson H, Meyuhas O, Templeton DJ, Landreth GE, Hensold JO. S6 phosphorylation-independent pathways regulate translation of 5'-terminal oligopyrimidine tract-containing mRNAs in differentiating hematopoietic cells. Nucleic Acids Res 2002;30(9):1919-1928.
52. Schwartz EI, Intine RV, Maraia RJ. CK2 is responsible for phosphorylation of human La protein serine-366 and can modulate rpL37 5'-terminal oligopyrimidine mRNA metabolism. Mol Cell Biol 2004;24(21):9580-9591.
53. Brenet F, Socci ND, Sonenberg N, Holland EC. Akt phosphorylation of La regulates specific mRNA translation in glial progenitors. Oncogene 2009;28(1):128-139.
54. Caldarola S, De Stefano MC, Amaldi F, Loreni F. Synthesis and function of ribosomal proteins-Fading models and new perspectives. FEBS J 2009;276(12):3199-3210.
55. Wolin SL, Cedervall T. The La protein. Ann Rev Biochem 2002;71:375-403.
56. Orom UA, Nielsen FC, Lund AH. MicroRNA-10a binds the 5'UTR of ribosomal protein mRNAs and enhances their translation. Mol Cell 2008;30(4):460-471.
57. Vogt PK. PI 3-kinase, mTOR, protein synthesis and cancer. Trends Mol Med 2001;7(11):482-484.
58. Ruvinsky I, Sharon N, Lerer T, Cohen H, Stolovich-Rain M, Nir T, Dor Y, Zisman P, Meyuhas O. Ribosomal protein S6 phosphorylation is a determinant of cell size and glucose homeostasis. Genes Dev 2005;19(18):2199-2211.
59. Hasler P, Brot N, Weissbach H, Parnassa AP, Elkon KB. Ribosomal proteins P0, P1, and P2 are phosphorylated by casein kinase II at their conserved carboxyl termini. J Biol Chem 1991;266(21):13815-13820.
60. Lam YW, Lamond AI, Mann M, Andersen JS. Analysis of nucleolar protein dynamics reveals the nuclear degradation of ribosomal proteins. Curr Biol 2007;17(9):749-760.
61. Spence J, Gali RR, Dittmar G, Sherman F, Karin M, Finley D. Cell cycle-regulated modification of the ribosome by a variant multiubiquitin chain. Cell 2000;102(1):67-76.
62. Kraft C, Deplazes A, Sohrmann M, Peter M. Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat Cell Biol 2008;10(5):602-610.
63. Blobel G, Potter VR. Studies on free and membrane-bound ribosomes in rat liver. I. Distribution as related to total cellular RNA. J Mol Biol 1967;26(2):279-292.
64. Andrews TM, Tata JR. Protein synthesis by membrane-bound and free ribosomes of secretory and non-secretory tissues. Biochem J 1971;121(4):683-694.
65. Lerner RS, Seiser RM, Zheng T, Lager PJ, Reedy MC, Keene JD, Nicchitta CV. Partitioning and translation of mRNAs encoding soluble proteins on membrane-bound ribosomes. RNA 2003;9(9):1123-1137.
66. Walter P, Johnson AE. Signal sequence recognition and protein targeting to the endoplasmic reticulum membrane. Annu Rev Cell Biol 1994;10:87-119.
67. Stephens SB, Dodd RD, Brewer JW, Lager PJ, Keene JD, Nicchitta CV. Stable ribosome binding to the endoplasmic reticulum enables compartment-specific regulation of mRNA translation. Mol Biol Cell 2005;16(12):5819-5831.
68. Bolze A, Mahlaoui N, Byun M, Turner B, Trede N, Ellis SR, Abhyankar A, Itan Y, Patin E, Brebner S, Sackstein P, Puel A, Picard C, Abel L, Quintana-Murci L, Faust SN, Williams AP, Baretto R, Duddridge M, Kini U, Pollard AJ, Gaud C, Frange P, Orbach D, Emile JF, Stephan JL, Sorensen R, Plebani A, Hammarstrom L, Conley ME, Selleri L, Casanova JL. Ribosomal protein SA haploinsufficiency in humans with isolated congenital asplenia. Science 2013;340(6135):976-978.
69. Choi S, Jung CR, Kim JY, Im DS. PRMT3 inhibits ubiquitination of ribosomal protein S2 and together forms an active enzyme complex. Biochim Biophys Acta 2008;1780(9):1062-1069.
70. Lee SB, Kwon IS, Park J, Lee KH, Ahn Y, Lee C, Kim J, Choi SY, Cho SW, Ahn JY. Ribosomal protein S3, a new substrate of Akt, serves as a signal mediator between neuronal apoptosis and DNA repair. J Biol Chem 2010;285(38):29457-29468.
71. Hegde V, Yadavilli S, Deutsch WA. Knockdown of ribosomal protein S3 protects human cells from genotoxic stress. DNA Repair (Amst) 2007;6(1):94-99.
72. Hegde V, Wang M, Deutsch WA. Characterization of human ribosomal protein S3 binding to 7, 8-dihydro-8-oxoguanine and abasic sites by surface plasmon resonance. DNA Repair (Amst) 2004;3(2):121-126.
73. Wan F, Anderson DE, Barnitz RA, Snow A, Bidere N, Zheng L, Hegde V, Lam LT, Staudt LM, Levens D, Deutsch WA, Lenardo MJ. Ribosomal protein S3: A KH domain subunit in NF-kappaB complexes that mediates selective gene regulation. Cell 2007;131(5):927-939.
74. Yadavilli S, Mayo LD, Higgins M, Lain S, Hegde V, Deutsch WA. Ribosomal protein S3: A multi-functional protein that interacts with both p53 and MDM2 through its KH domain. DNA Repair (Amst) 2009;8(10):1215-1224.
75. Wan F, Weaver A, Gao X, Bern M, Hardwidge PR, Lenardo MJ. IKKbeta phosphorylation regulates RPS3 nuclear translocation and NF-kappaB function during infection with Escherichia coli strain O157:H7. Nat Immunol 2011;12(4):335-343.
76. Yang HJ, Youn H, Seong KM, Jin YW, Kim J, Youn B. Phosphorylation of ribosomal protein S3 and antiapoptotic TRAF2 protein mediates radioresistance in non-small cell lung cancer cells. J Biol Chem 2013;288(5):2965-2975.
77. Jang CY, Kim HD, Kim J. Ribosomal protein S3 interacts with TRADD to induce apoptosis through caspase dependent JNK activation. Biochem Biophys Res Commun 2012;421(3):474-478.
78. Naora H, Takai I, Adachi M, Naora H. Altered cellular responses by varying expression of a ribosomal protein gene: sequential coordination of enhancement and suppression of ribosomal protein S3a gene expression induces apoptosis. J Cell Biol 1998;141(3):741-753.
79. Cui K, Coutts M, Stahl J, Sytkowski AJ. Novel interaction between the transcription factor CHOP (GADD153) and the ribosomal protein FTE/S3a modulates erythropoiesis. J Biol Chem 2000;275(11):7591-7596.
80. Hu ZB, Minden MD, McCulloch EA, Stahl J. Regulation of drug sensitivity by ribosomal protein S3a. Blood 2000;95(3):1047-1055.
81. Yadaiah M, Sudhamalla B, Rao PN, Roy KR, Ramakrishna D, Hussain Syed G, Ramaiah KV, Bhuyan AK. Arrested cell proliferation through cysteine protease activity of eukaryotic ribosomal protein S4. FASEB J 2013;27(2):803-810.
82. Matragkou CN, Papachristou ET, Tezias SS, Tsiftsoglou AS, Choli-Papadopoulou T, Vizirianakis IS. The potential role of ribosomal protein S5 on cell cycle arrest and initiation of murine erythroleukemia cell differentiation. J Cell Biochem 2008;104(4):1477-1490.
83. Panic L, Tamarut S, Sticker-Jantscheff M, Barkic M, Solter D, Uzelac M, Grabusić K, Volarević S. Ribosomal protein S6 gene haploinsufficiency is associated with activation of a p53-dependent checkpoint during gastrulation. Mol Cell Biol 2006;26(23):8880-8891.
84. Jeon YJ, Kim IK, Hong SH, Nan H, Kim HJ, Lee HJ, Masuda ES, Meyuhas O, Oh BH, Jung YK. Ribosomal protein S6 is a selective mediator of TRAIL-apoptotic signaling. Oncogene 2008;27(31):4344-4352.
85. Chen D, Zhang Z, Li M, Wang W, Li Y, Rayburn ER, Hill DL, Wang H, Zhang R. Ribosomal protein S7 as a novel modulator of p53-MDM2 interaction: Binding to MDM2, stabilization of p53 protein, and activation of p53 function. Oncogene 2007;26(35):5029-5037.
86. Zhu Y, Poyurovsky MV, Li Y, Biderman L, Stahl J, Jacq X, Prives C. Ribosomal protein S7 is both a regulator and a substrate of MDM2. Mol Cell 2009;35(3):316-326.
87. Gao M, Li X, Dong W, Jin R, Ma H, Yang P, Hu M, Li Y, Hao Y, Yuan S, Huang J, Song L. Ribosomal protein S7 regulates arsenite-induced GADD45alpha expression by attenuating MDM2-mediated GADD45alpha ubiquitination and degradation. Nucleic Acids Res 2013;41(10):5210-5222.
88. Watkins-Chow DE, Cooke J, Pidsley R, Edwards A, Slotkin R, Leeds KE, Mullen R, Baxter LL, Campbell TG, Salzer MC, Biondini L, Gibney G, Phan Dinh Tuy F, Chelly J, Morris HD, Riegler J, Lythgoe MF, Arkell RM, Loreni F, Flint J, Pavan WJ, Keays DA. Mutation of the diamond-blackfan anemia gene Rps7 in mouse results in morphological and neuroanatomical phenotypes. PLoS Genet 2013;9(1):e1003094.
89. Hao Y, Kong X, Ruan Y, Gan H, Chen H, Zhang C, Ren S, Gu J. CDK11p46 and RPS8 associate with each other and suppress translation in a synergistic manner. Biochem Biophys Res Commun 2011;407(1):169-174.
90. Lindstrom MS, Nister M. Silencing of ribosomal protein S9 elicits a multitude of cellular responses inhibiting the growth of cancer cells subsequent to p53 activation. PLoS One 2010;5(3):e9578.
91. Guo X, Shi Y, Gou Y, Li J, Han S, Zhang Y, Huo J, Ning X, Sun L, Chen Y, Sun S, Fan D. Human ribosomal protein S13 promotes gastric cancer growth through down-regulating p27(Kip1). J Cell Mol Med 2011;15(2):296-306.
92. Zhou X, Hao Q, Liao JM, Liao P, Lu H. Ribosomal protein S14 negatively regulates c-Myc activity. J Biol Chem 2013;288(30):21793-21801.
93. Zhou X, Hao Q, Liao J, Zhang Q, Lu H. Ribosomal protein S14 unties the MDM2-p53 loop upon ribosomal stress. Oncogene 2013;32(3):388-396.
94. Zhang J, Bai D, Ma X, Guan J, Zheng X. hCINAP is a novel regulator of ribosomal protein-HDM2-p53 pathway by controlling NEDDylation of ribosomal protein S14. Oncogene 2014;33(2):246-254.
95. Barlow JL, Drynan LF, Hewett DR, Holmes LR, Lorenzo-Abalde S, Lane AL, Jolin HE, Pannell R, Middleton AJ, Wong SH, Warren AJ, Wainscoat JS, Boultwood J, McKenzie AN. A p53-dependent mechanism underlies macrocytic anemia in a mouse model of human 5q- syndrome. Nat Med 2010;16(1):59-66.
96. Daftuar L, Zhu Y, Jacq X, Prives C. Ribosoal proteins RPL37, RPS15 and RPS20 regulate the Mdm2-p53-MdmX network. PLoS One 2013;8(7):e68667.
97. Cmejla R, Cmejlova J, Handrkova H, Petrak J, Pospisilova D. Ribosomal protein S17 gene (RPS17) is mutated in Diamond-Blackfan anemia. Hum Mutat 2007;28(12):1178-1182.
98. Farrar JE, Vlachos A, Atsidaftos E, Carlson-Donohoe H, Markello TC, Arceci RJ, Ellis SR, Lipton JM, Bodine DM. Ribosomal protein gene deletions in Diamond-Blackfan anemia. Blood 2011;118(26):6943-6951.
99. Song MJ, Yoo EH, Lee KO, Kim GN, Kim HJ, Kim SY, Kim SH. A novel initiation codon mutation in the ribosomal protein S17 gene (RPS17) in a patient with Diamond-Blackfan anemia. Pediatr Blood Cancer 2010;54(4):629-631.
100. Moniz H, Gastou M, Leblanc T, Hurtaud C, Cretien A, Lecluse Y, Raslova H, Larghero J, Croisille L, Faubladier M, Bluteau O, Lordier L, Tchernia G, Vainchenker W, Mohandas N, Da Costa L; DBA Group of Société d'Hématologie et d'Immunologie Pédiatrique-SHIP. Primary hematopoietic cells from DBA patients with mutations in RPL11 and RPS19 genes exhibit distinct erythroid phenotype in vitro. Cell Death Dis 2012;3:e356.
101. Jaako P, Flygare J, Olsson K, Quere R, Ehinger M, Henson A, Ellis S, Schambach A, Baum C, Richter J, Larsson J, Bryder D, Karlsson S. Mice with ribosomal protein S19 deficiency develop bone marrow failure and symptoms like patients with Diamond-Blackfan anemia. Blood 2011;118(23):6087-6096.
102. Dutt S, Narla A, Lin K, Mullally A, Abayasekara N, Megerdichian C, Wilson FH, Currie T, Khanna-Gupta A, Berliner N, Kutok JL, Ebert BL. Haploinsufficiency for ribosomal protein genes causes selective activation of p53 in human erythroid progenitor cells. Blood 2011;117(9):2567-2576.
103. McGowan KA, Li JZ, Park CY, Beaudry V, Tabor HK, Sabnis AJ, Zhang W, Fuchs H, de Angelis MH, Myers RM, Attardi LD, Barsh GS. Ribosomal mutations cause p53-mediated dark skin and pleiotropic effects. Nat Genet 2008;40(8):963-970.
104. Filip AM, Klug J, Cayli S, Frohlich S, Henke T, Lacher P, Eickhoff R, Bulau P, Linder M, Carlsson-Skwirut C, Leng L, Bucala R, Kraemer S, Bernhagen J, Meinhardt A. Ribosomal protein S19 interacts with macrophage migration inhibitory factor and attenuates its pro-inflammatory function. J Biol Chem 2009;284(12):7977-7985.
105. Matsson H, Davey EJ, Draptchinskaia N, Hamaguchi I, Ooka A, Leeven P, Forsberg E, Karlsson S, Dahl N. Targeted disruption of the ribosomal protein S19 gene is lethal prior to implantation. Mol Cell Biol 2004;24(9):4032-4037.
106. Zhang X, Wang W, Wang H, Wang MH, Xu W, Zhang R. Identification of ribosomal protein S25 (RPS25)-MDM2-p53 regulatory feedback loop. Oncogene 2013;32(22):2782-2791.
107. Adilakshmi T, Laine RO. Ribosomal protein S25 mRNA partners with MTF-1 and La to provide a p53-mediated mechanism for survival or death. J Biol Chem 2002;277(6):4147-4151.
108. Cui D, Li L, Lou H, Sun H, Ngai SM, Shao G, Tang J. The ribosomal protein S26 regulates p53 activity in response to DNA damage. Oncogene 2013;33(17):2225-2235.
109. Xiong X, Zhao Y, He H, Sun Y. Ribosomal protein S27-like and S27 interplay with p53-MDM2 axis as a target, a substrate and a regulator. Oncogene 2011;30(15):1798-1811.
110. Yang ZY, Qu Y, Zhang Q, Wei M, Liu CX, Chen XH, Yan M, Zhu ZG, Liu BY, Chen GQ, Wu YL, Gu QL. Knockdown of metallopanstimulin-1 inhibits NF-kappaB signaling at different levels: The role of apoptosis induction of gastric cancer cells. Int J Cancer 2012;130(12):2761-2770.
111. Yang ZY, Jiang H, Qu Y, Wei M, Yan M, Zhu ZG, Liu BY, Chen GQ, Wu YL, Gu QL. Metallopanstimulin-1 regulates invasion and migration of gastric cancer cells partially through integrin beta4. Carcinogenesis 2013;34(12):2851-2860.
112. Sun XX, DeVine T, Challagundla KB, Dai MS. Interplay between ribosomal protein S27a and MDM2 protein in p53 activation in response to ribosomal stress. J Biol Chem 2011;286(26):22730-22741.
113. Khanna N, Sen S, Sharma H, Singh N. S29 ribosomal protein induces apoptosis in H520 cells and sensitizes them to chemotherapy. Biochem Biophys Res Commun 2003;304(1):26-35.
114. Khanna N, Reddy VG, Tuteja N, Singh N. Differential gene expression in apoptosis: Identification of ribosomal protein S29 as an apoptotic inducer. Biochem Biophys Res Commun 2000;277(2):476-486.
115. Russo A, Esposito D, Catillo M, Pietropaolo C, Crescenzi E, Russo G. Human rpL3 induces G(1)/S arrest or apoptosis by modulating p21 (waf1/cip1) levels in a p53-independent manner. Cell Cycle 2013;12(1):76-87.
116. Provost E, Wehner KA, Zhong X, Ashar F, Nguyen E, Green R, Parsons MJ, Leach SD. Ribosomal biogenesis genes play an essential and p53-independent role in zebrafish pancreas development. Development 2012;139(17):3232-3241.
117. Dai MS, Lu H. Inhibition of MDM2-mediated p53 ubiquitination and degradation by ribosomal protein L5. J Biol Chem 2004;279(43):44475-44482.
118. Horn HF, Vousden KH. Cooperation between the ribosomal proteins L5 and L11 in the p53 pathway. Oncogene 2008;27(44):5774-5784.
119. Wu Q, Gou Y, Wang Q, Jin H, Cui L, Zhang Y, He L, Wang J, Nie Y, Shi Y, Fan D. Downregulation of RPL6 by siRNA inhibits proliferation and cell cycle progression of human gastric cancer cell lines. PLoS One 2011;6(10):e26401.
120. Gou Y, Shi Y, Zhang Y, Nie Y, Wang J, Song J, Jin H, He L, Gao L, Qiao L, Wu K, Fan D. Ribosomal protein L6 promotes growth and cell cycle progression through upregulating cyclin E in gastric cancer cells. Biochem Biophys Res Commun 2010;393(4):788-793.
121. Du J, Shi Y, Pan Y, Jin X, Liu C, Liu N, Han Q, Lu Y, Qiao T, Fan D. Regulation of multidrug resistance by ribosomal protein l6 in gastric cancer cells. Cancer Biol Ther 2005;4(2):242-247.
122. Bai D, Zhang J, Xiao W, Zheng X. Regulation of the HDM2-p53 pathway by ribosomal protein L6 in response to ribosomal stress. Nucleic Acids Res 2014;42(3):1799-1811.
123. Provost E, Weier CA, Leach SD. Multiple ribosomal proteins are expressed at high levels in developing zebrafish endoderm and are required for normal exocrine pancreas development. Zebrafish 2013;10(2):161-169.
124. Neumann F, Krawinkel U. Constitutive expression of human ribosomal protein L7 arrests the cell cycle in G1 and induces apoptosis in Jurkat T-lymphoma cells. Exp Cell Res 1997;230(2):252-261.
125. Li H, Pan L, Gou K. Depletion of ribosomal protein L8 impairs Drosophila development and is associated with apoptosis. Sci China Life Sci 2010;53(9):1092-1097.
126. Swoboda RK, Somasundaram R, Caputo L, Ochoa EM, Gimotty PA, Marincola FM, Van Belle P, Barth S, Elder D, Guerry D, Czerniecki B, Schuchter L, Vonderheide RH, Herlyn D. Shared MHC class II-dependent melanoma ribosomal protein L8 identified by phage display. Cancer Res 2007;67(8):3555-3559.
127. Zhang Y, Wolf GW, Bhat K, Jin A, Allio T, Burkhart WA, Xiong Y. Ribosomal protein L11 negatively regulates oncoprotein MDM2 and mediates a p53-dependent ribosomal-stress checkpoint pathway. Mol Cell Biol 2003;23(23):8902-8912.
128. Bhat KP, Itahana K, Jin A, Zhang Y. Essential role of ribosomal protein L11 in mediating growth inhibition-induced p53 activation. EMBO J 2004;23(12):2402-2412.
129. Dai MS, Shi D, Jin Y, Sun XX, Zhang Y, Grossman SR, Lu H. Regulation of the MDM2-p53 pathway by ribosomal protein L11 involves a post-ubiquitination mechanism. J Biol Chem 2006;281(34):24304-24313.
130. Dai MS, Arnold H, Sun XX, Sears R, Lu H. Inhibition of c-Myc activity by ribosomal protein L11. EMBO J 2007;26(14):3332-3345.
131. Mazumder B, Sampath P, Seshadri V, Maitra RK, DiCorleto PE, Fox PL. Regulated release of L13a from the 60S ribosomal subunit as a mechanism of transcript-specific translational control. Cell 2003;115(2):187-198.
132. Mukhopadhyay R, Ray PS, Arif A, Brady AK, Kinter M, Fox PL. DAPK-ZIPK-L13a axis constitutes a negative-feedback module regulating inflammatory gene expression. Mol Cell 2008;32(3):371-382.
133. Poddar D, Basu A, Baldwin WM, 3rd, Kondratov RV, Barik S, Mazumder B. An extraribosomal function of ribosomal protein L13a in macrophages resolves inflammation. J Immunol 2013;190(7):3600-3612.
134. Hsu YA, Lin HJ, Sheu JJ, Shieh FK, Chen SY, Lai CH, Tsai FJ, Wan L, Chen BH. A novel interaction between interferon-inducible protein p56 and ribosomal protein L15 in gastric cancer cells. DNA Cell Biol 2011;30(9):671-679.
135. Smolock EM, Korshunov VA, Glazko G, Qiu X, Gerloff J, Berk BC. Ribosomal protein L17, RpL17, is an inhibitor of vascular smooth muscle growth and carotid intima formation. Circulation 2012;126(20):2418-2427.
136. Rao S, Lee SY, Gutierrez A, Perrigoue J, Thapa RJ, Tu Z, Jeffers JR, Rhodes M, Anderson S, Oravecz T, Hunger SP, Timakhov RA, Zhang R, Balachandran S, Zambetti GP, Testa JR, Look AT, Wiest DL. Inactivation of ribosomal protein L22 promotes transformation by induction of the stemness factor, Lin28B. Blood 2012;120(18):3764-3773.
137. Dai MS, Zeng SX, Jin Y, Sun XX, David L, Lu H. Ribosomal protein L23 activates p53 by inhibiting MDM2 function in response to ribosomal perturbation but not to translation inhibition. Mol Cell Biol 2004;24(17):7654-7668.
138. Jin A, Itahana K, O'Keefe K, Zhang Y. Inhibition of HDM2 and activation of p53 by ribosomal protein L23. Mol Cell Biol 2004;24(17):7669-7680.
139. Wanzel M, Russ AC, Kleine-Kohlbrecher D, Colombo E, Pelicci PG, Eilers M. A ribosomal protein L23-nucleophosmin circuit coordinates Mizl function with cell growth. Nat Cell Biol 2008;10(9):1051-1061.
140. Takagi M, Absalon MJ, McLure KG, Kastan MB. Regulation of p53 translation and induction after DNA damage by ribosomal protein L26 and nucleolin. Cell 2005;123(1):49-63.
141. Ofir-Rosenfeld Y, Boggs K, Michael D, Kastan MB, Oren M. Mdm2 regulates p53 mRNA translation through inhibitory interactions with ribosomal protein L26. Mol Cell 2008;32(2):180-189.
142. Jones DT, Lechertier T, Reynolds LE, Mitter R, Robinson SD, Kirn-Safran CB, Hodivala-Dilke KM. Endogenous ribosomal protein L29 (RPL29): A newly identified regulator of angiogenesis in mice. Dis Model Mech 2013;6(1):115-124.
143. Oristian DS, Sloofman LG, Zhou X, Wang L, Farach-Carson MC, Kirn-Safran CB. Ribosomal protein L29/HIP deficiency delays osteogenesis and increases fragility of adult bone in mice. J Orthop Res 2009;27(1):28-35.
144. Li C, Ge M, Yin Y, Luo M, Chen D. Silencing expression of ribosomal protein L26 and L29 by RNA interfering inhibits proliferation of human pancreatic cancer PANC-1 cells. Mol Cell Biochem 2012;370(1-2):127-139.
145. Sun B, Hou YL, Hou WR, Zhang SN, Ding X, Su XL. cDNA cloning, overexpression, purification and pharmacologic evaluation for anticancer activity of ribosomal protein L23A gene (RPL23A) from the giant panda. Int J Mol Sci 2012;13(2):2133-2147.
146. Su XL, Hou YL, Yan XH, Ding X, Hou WR, Sun B, Zhang SN. Expression, purification, and evaluation for anticancer activity of ribosomal protein L31 gene (RPL31) from the giant panda (Ailuropoda melanoleuca). Mol Biol Rep 2012;39(9):8945-8954.
147. Lopez CD, Martinovsky G, Naumovski L. Inhibition of cell death by ribosomal protein L35a. Cancer Lett 2002;180(2):195-202.
148. Farrar JE, Nater M, Caywood E, McDevitt MA, Kowalski J, Takemoto CM, Talbot CC, Jr., Meltzer P, Esposito D, Beggs AH, Schneider HE, Grabowska A, Ball SE, Niewiadomska E, Sieff CA, Vlachos A, Atsidaftos E, Ellis SR, Lipton JM, Gazda HT, Arceci RJ. Abnormalities of the large ribosomal subunit protein, Rpl35a, in Diamond-Blackfan anemia. Blood 2008;112(5):1582-1592.
149. Llanos S, Serrano M. Depletion of ribosomal protein L37 occurs in response to DNA damage and activates p53 through the L11/MDM2 pathway. Cell Cycle 2010;9(19):4005-4012.
150. Wang S, Huang J, He J, Wang A, Xu S, Huang SF, Xiao S. RPL41, a small ribosomal peptide deregulated in tumors, is essential for mitosis and centrosome integrity. Neoplasia 2010;12(3):284-293.
151. Wang A, Xu S, Zhang X, He J, Yan D, Yang Z, Xiao S. Ribosomal protein RPL41 induces rapid degradation of ATF4, a transcription factor critical for tumour cell survival in stress. J Pathol 2011;225(2):285-292.
152. Artero-Castro A, Kondoh H, Fernandez-Marcos PJ, Serrano M, Ramon Y, Cajal S, Lleonart ME. Rplp1 bypasses replicative senescence and contributes to transformation. Exp Cell Res 2009;315(8):1372-1383.
153. Berghofer-Hochheimer Y, Zurek C, Wolfl S, Hemmerich P, Munder T. L7 protein is a coregulator of vitamin D receptor retinoid X receptor-mediated transactivation. J Cell Biochem 1998;69(1):1-12.
154. Gray JP, Davis JW, 2nd, Gopinathan L, Leas TL, Nugent CA, Vanden Heuvel JP. The ribosomal protein rpL11 associates with and inhibits the transcriptional activity of peroxisome proliferator-activated receptor-alpha. Toxicol Sci 2006;89(2):535-546.
155. Kim HD, Kim TS, Joo YJ, Shin HS, Kim SH, Jang CY, Lee CE, Kim J. RpS3 translation is repressed by interaction with its own mRNA. J Cell Biochem 2010;110(2):294-303.
156. Lindström MS. Emerging functions of ribosomal proteins in gene-specific transcription and translation. Biochem Biophys Res Commun 2009;6;379(2):167-170.
157. Neumann F, Krawinkel U. Constitutive expression of human ribosomal protein L7 arrests the cell cycle in G(1) and induces apoptosis in Jurkat T-lymphoma cells. Exp Cell Res 1997;230(2):252-261.
158. Wang H, Zhao LN, Li KZ, Ling R, Li XJ, Wang L. Overexpression of ribosomal protein L15 is associated with cell proliferation in gastric cancer. BMC Cancer 2006;6:91.
159. Jang CY, Kim HD, Zhang X, Chang JS, Kim J. Ribosomal protein S3 localizes on the mitotic spindle and functions as a microtubule associated protein in mitosis. Biochem Biophys Res Commun 2012;429(1-2):57-62.
160. Yadavilli S, Hegde V, Deutsch WA. Translocation of human ribosomal protein S3 to sites of DNA damage is dependant on ERK-mediated phosphorylation following genotoxic stress. DNA Repair (Amst) 2007;6(10):1453-1462.
161. Duan J, Ba Q, Wang ZL, Hao M, Li XG, Hu PT, Zhang D, Zhang R, Wang H. Knockdown of ribosomal protein S7 causes developmental abnormalities via p53 dependent and independent pathways in zebrafish. Int J Biochem Cell Biol 2011;43(8):1218-1227.
162. Uechi T, Nakajima Y, Nakao A, Torihara H, Chakraborty A, Inoue K, Kenmochi N. Ribosomal protein gene knockdown causes developmental defects in zebrafish. PLoS One 2006;1:e37.
163. Anderson SJ, Lauritsen JPH, Hartman MG, Foushee AMD, Lefebvre JM, Shinton SA, Gerhardt B, Hardy RR, Oravecz T, Wiest DL. Ablation of ribosomal protein L22 selectively impairs alpha beta T cell development by activation of a p53-dependent checkpoint. Immunity 2007;26(6):759-772.
164. Stadanlick JE, Zhang Z, Lee SY, Hemann M, Biery M, Carleton MO, Zambetti GP, Anderson SJ, Oravecz T, Wiest DL. Developmental arrest of T cells in Rpl22-deficient mice is dependent upon multiple p53 effectors. J Immunol 2011;187(2):664-675.
165. Bevort M, Leffers H. Down regulation of ribosomal protein mRNAs during neuronal differentiation of human NTERA2 cells. Differentiation 2000;66(2-3):81-92.
166. Liu JJ, Huang BH, Zhang JQ, Carson DD, Hooi SC. Repression of HIP/RPL29 expression induces differentiation in colon cancer cells. J Cell Physiol 2006;207(2):287-292.
167. Kreunin P, Yoo C, Urquidi V, Lubman DM, Goodison S. Differential expression of ribosomal proteins in a human metastasis model identified by coupling 2-D liquid chromatography and mass spectrometry. Cancer Genomics Proteomics 2007;4(5):329-339.
168. Liu F, Li Y, Yu Y, Fu S, Li P. Cloning of novel tumor metastasis-related genes from the highly metastatic human lung adenocarcinoma cell line Anip973. J Genet Genomics 2007;34(3):189-195.
169. McDonald JM, Pelloski CE, Ledoux A, Sun M, Raso G, Komaki R, Wistuba II, Bekele BN, Aldape K. Elevated phospho-S6 expression is associated with metastasis in adenocarcinoma of the lung. Clin Cancer Res 2008;14(23):7832-7837.
170. Rubbi CP, Milner J. Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J 2003;22(22):6068-6077.
171. Boyd MT, Vlatkovic N, Rubbi CP. The nucleolus directly regulates p53 export and degradation. J Cell Biol 2011;194(5):689-703.
172. Nag S, Qin JJ, Srivenugopal K, Wang MH, Zhang R. The MDM2-p53 pathway revisited. J Biomed Res 2013; 27(4):254-271
173. Strezoska Z, Pestov DG, Lau LF. Bop1 is a mouse WD40 repeat nucleolar protein involved in 28S and 5. 8S RRNA processing and 60S ribosome biogenesis. Mol Cell Biol 2000;20(15):5516-5528.
174. McMahon M, Ayllon V, Panov KI, O'Connor R. Ribosomal 18 S RNA processing by the IGF-I-responsive WDR3 protein is integrated with p53 function in cancer cell proliferation. J Biol Chem 2010;285(24):18309-18318.
175. Holzel M, Orban M, Hochstatter J, Rohrmoser M, Harasim T, Malamoussi A, Kremmer E, Längst G, Eick D. Defects in 18 S or 28 S rRNA processing activate the p53 pathway. J Biol Chem 2010;285(9):6364-6370.
176. Zhang F, Hamanaka RB, Bobrovnikova-Marjon E, Gordan JD, Dai MS, Lu H, Simon MC, Diehl JA. Ribosomal stress couples the unfolded protein response to p53-dependent cell cycle arrest. J Biol Chem 2006;281(40):30036-30045.
177. Donati G, Bertoni S, Brighenti E, Vici M, Trere D, Volarevic S, Montanaro L, Derenzini M. The balance between rRNA and ribosomal protein synthesis up- and downregulates the tumour suppressor p53 in mammalian cells. Oncogene 2011;30(29):3274-3288.
178. Schnapp A, Pfleiderer C, Rosenbauer H, Grummt I. A growth-dependent transcription initiation factor (TIF-IA) interacting with RNA polymerase I regulates mouse ribosomal RNA synthesis. EMBO J 1990;9(9):2857-2863.
179. Yuan XJ, Zhou YG, Casanova E, Chai MQ, Kiss E, Grone HJ, Schütz G, Grummt I. Genetic inactivation of the transcription factor TIF-IA leads to nucleolar disruption, cell cycle arrest, and p53-mediated apoptosis. Mol Cell 2005;19(1):77-87.
180. Burger K, Muhl B, Harasim T, Rohrmoser M, Malamoussi A, Orban M, Kellner M, Gruber-Eber A, Kremmer E, Hölzel M, Eick D. Chemotherapeutic drugs inhibit ribosome biogenesis at various levels. J Biol Chem 2010;285(16):12416-12425.
181. Sun XX, Dai MS, Lu H. 5-Fluorouracil activation of p53 involves an MDM2-ribosomal protein interaction. J Biol Chem 2007;282(11):8052-8059.
182. Sun XX, Dai MS, Lu H. Mycophenolic acid activation of p53 requires ribosomal proteins L5 and L11. J Biol Chem 2008;283(18):12387-12392.
183. Dai MS, Sun XX, Lu H. Aberrant expression of nucleostemin activates p53 and induces cell cycle arrest via inhibition of MDM2. Mol Cell Biol 2008;28(13):4365-4376.
184. Lo D, Dai MS, Sun XX, Zeng SX, Lu H. Ubiquitin- and MDM2 E3 ligase-independent proteasomal turnover of nucleostemin in response to GTP depletion. J Biol Chem 2012;287(13):10013-10020.
185. Yu WS, Qiu ZW, Gao N, Wang LR, Cui HX, Qian Y, Jiang L, Luo J, Yi Z, Lu H, Li D, Liu M. PAK1IP1, a ribosomal stress-induced nucleolar protein, regulates cell proliferation via the p53-MDM2 loop. Nucleic Acids Res 2011;39(6):2234-2248.
186. Itahana K, Bhat KP, Jin AW, Itahana Y, Hawke D, Kobayashi R, Zhang Y. Tumor suppressor ARF degrades B23, a nucleolar protein involved in ribosome biogenesis and cell proliferation. Mol Cell 2003;12(5):1151-1164.
187. Lessard F, Morin F, Ivanchuk S, Langlois F, Stefanovsky V, Rutka J, Moss T. The ARF tumor suppressor controls ribosome biogenesis by regulating the RNA polymerase I transcription factor TTF-I. Mol Cell 2010;38(4):539-550.
188. Lessard F, Stefanovsky V, Tremblay MG, Moss T. The cellular abundance of the essential transcription termination factor TTF-I regulates ribosome biogenesis and is determined by MDM2 ubiquitinylation. Nucleic Acids Res 2012;40(12):5357-5367.
189. Ayrault O, Andrique L, Fauvin D, Eymin B, Gazzeri S, Seite P. Human tumor suppressor p14(ARF) negatively regulates rRNA transcription and inhibits UBF1 transcription factor phosphorylation. Oncogene 2006;25(58):7577-7586.
190. Sun XX, Wang YG, Xirodimas DP, Dai MS. Perturbation of 60 S ribosomal biogenesis results in ribosomal protein L5-and L11-dependent p53 activation. J Biol Chem 2010;285(33):25812-25821.
191. Uechi T, Nakajima Y, Chakraborty A, Torihara H, Higa S, Kenmochi N. Deficiency of ribosomal protein S19 during early embryogenesis leads to reduction of erythrocytes in a zebrafish model of Diamond-Blackfan anemia. Hum Mol Genet 2008;17(20):3204-3211.
192. Chakraborty A, Uechi T, Higa S, Torihara H, Kenmochi N. Loss of ribosomal protein L11 affects zebrafish embryonic development through a p53-dependent apoptotic response. PLoS One 2009;4(1):e4152.
193. Danilova N, Sakamoto KM, Lin S. Ribosomal protein L11 mutation in zebrafish leads to haematopoietic and metabolic defects. Br J Haematol 2011;152(2):217-228.
194. Sulic S, Panic L, Barkic M, Mercep M, Uzelac M, Volarevic S. Inactivation of S6 ribosomal protein gene in T lymphocytes activates a p53-dependent checkpoint response. Genes Dev 2005;19(24):3070-3082.
195. McGowan KA, Pang WW, Bhardwaj R, Perez MG, Pluvinage JV, Glader BE, Malek R, Mendrysa SM, Weissman IL, Park CY, Barsh GS. Reduced ribosomal protein gene dosage and p53 activation in low-risk myelodysplastic syndrome. Blood 2011;118(13):3622-3633.
196. Golomb L, Bublik DR, Wilder S, Nevo R, Kiss V, Grabusic K, Volarevic S, Oren M. Importin 7 and exportin 1 link c-Myc and p53 to regulation of ribosomal biogenesis. Mol Cell 2012;45(2):222-232.
197. Vousden KH, Lane DP. p53 in health and disease. Nat Rev Mol Cell Biol 2007;8(4):275-283.
198. Vousden KH, Prives C. Blinded by the light: The growing complexity of p53. Cell 2009;137(3):413-431.
199. Levine AJ, Oren M. The first 30 years of p53: Growing ever more complex. Nat Rev Cancer 2009;9(10):749-758.
200. Toledo F, Wahl GM. Regulating the p53 pathway: In vitro hypotheses, in vivo veritas. Nat Rev Cancer 2006;6(12):909-923.
201. Juven T, Barak Y, Zauberman A, George DL, Oren M. Wild type p53 can mediate sequence-specific transactivation of an internal promoter within the mdm2 gene. Oncogene 1993;8(12):3411-3416.
202. Wu X, Bayle JH, Olson D, Levine AJ. The p53-mdm-2 autoregulatory feedback loop. Genes Dev 1993;7(7A):1126-1132.
203. Barak Y, Juven T, Haffner R, Oren M. mdm2 expression is induced by wild type p53 activity. EMBO J 1993;12(2):461-468.
204. Oliner JD, Pietenpol JA, Thiagalingam S, Gyuris J, Kinzler KW, Vogelstein B. Oncoprotein MDM2 conceals the activation domain of tumour suppressor p53. Nature 1993;362(6423):857-860.
205. Haupt Y, Maya R, Kazaz A, Oren M. Mdm2 promotes the rapid degradation of p53. Nature 1997;387(6630):296-299.
206. Kubbutat MH, Jones SN, Vousden KH. Regulation of p53 stability by Mdm2. Nature 1997;387(6630):299-303.
207. Maya R, Balass M, Kim ST, Shkedy D, Leal JF, Shifman O, Moas M, Buschmann T, Ronai Z, Shiloh Y, Kastan MB, Katzir E, Oren M. ATM-dependent phosphorylation of Mdm2 on serine 395: Role in p53 activation by DNA damage. Genes Dev 2001;15(9):1067-1077.
208. Inuzuka H, Tseng A, Gao D, Zhai B, Zhang Q, Shaik S, Wan L, Ang XL, Mock C, Yin H, Stommel JM, Gygi S, Lahav G, Asara J, Xiao ZX, Kaelin WG, Jr., Harper JW, Wei W. Phosphorylation by casein kinase I promotes the turnover of the Mdm2 oncoprotein via the SCF(beta-TRCP) ubiquitin ligase. Cancer Cell 2010;18(2):147-159.
209. Li M, Luo J, Brooks CL, Gu W. Acetylation of p53 inhibits its ubiquitination by Mdm2. J Biol Chem 2002;277(52):50607-50611.
210. Zhang Y, Xiong Y, Yarbrough WG. ARF promotes MDM2 degradation and stabilizes p53: ARF-INK4a locus deletion impairs both the Rb and p53 tumor suppression pathways. Cell 1998;92(6):725-734.
211. Weber JD, Taylor LJ, Roussel MF, Sherr CJ, Bar-Sagi D. Nucleolar Arf sequesters Mdm2 and activates p53. Nat Cell Biol 1999;1(1):20-26.
212. Moll UM, Petrenko O. The MDM2-p53 interaction. Mol Cancer Res. 2003;1(14):1001-1008.
213. Shangary S, Wang S. Targeting the MDM2-p53 interaction for cancer therapy. Clin Cancer Res. 2008;14(17):5318-5324.
214. Marechal V, Elenbaas B, Piette J, Nicolas JC, Levine AJ. The ribosomal L5 protein is associated with mdm-2 and mdm-2-p53 complexes. Mol Cell Biol 1994;14(11):7414-7420.
215. Donati G, Peddigari S, Mercer CA, Thomas G. 5S ribosomal RNA is an essential component of a nascent ribosomal precursor complex that regulates the Hdm2-p53 checkpoint. Cell Rep 2013;4(1):87-98.
216. Bursac S, Brdovcak MC, Pfannkuchen M, Orsolic I, Golomb L, Zhu Y, Katz C, Daftuar L, Grabušić K, Vukelić I, Filić V, Oren M, Prives C, Volarevic S. Mutual protection of ribosomal proteins L5 and L11 from degradation is essential for p53 activation upon ribosomal biogenesis stress. Proc Natl Acad Sci USA 2012;109(50):20467-20472.
217. Zhang Y, Wang J, Yuan Y, Zhang W, Guan W, Wu Z, Jin C, Chen H, Zhang L, Yang X, He F. Negative regulation of HDM2 to attenuate p53 degradation by ribosomal protein L26. Nucleic Acids Res 2010;38(19):6544-6554.
218. Kawai H, Wiederschain D, Yuan ZM. Critical contribution of the MDM2 acidic domain to p53 ubiquitination. Mol Cell Biol 2003;23(14):4939-4947.
219. Zhang Q, Xiao H, Chai SC, Hoang QQ, Lu H. Hydrophilic residues are crucial for ribosomal protein L11 (RPL11) interaction with zinc finger domain of MDM2 and p53 protein activation. J Biol Chem 2011;286(44):38264-38274.
220. Li M, Gu W. A critical role for noncoding 5S rRNA in regulating Mdmx stability. Mol Cell 2011;43(6):1023-1032.
221. Yim JH, Kim YJ, Ko JH, Cho YE, Kim SM, Kim JY, Lee S, Park JH. The putative tumor suppressor gene GLTSCR2 induces PTEN-modulated cell death. Cell Death Differ 2007;14(11):1872-1879.
222. Kim YJ, Cho YE, Kim YW, Kim JY, Lee S, Park JH. Suppression of putative tumour suppressor gene GLTSCR2 expression in human glioblastomas. J Pathol 2008;216(2):218-224.
223. Sasaki M, Kawahara K, Nishio M, Mimori K, Kogo R, Hamada K, Itoh B, Wang J, Komatsu Y, Yang YR, Hikasa H, Horie Y, Yamashita T, Kamijo T, Zhang Y, Zhu Y, Prives C, Nakano T, Mak TW, Sasaki T, Maehama T, Mori M, Suzuki A. Regulation of the MDM2-P53 pathway and tumor growth by PICT1 via nucleolar RPL11. Nat Med 2011;17(8):944-951.
224. Lee S, Kim JY, Kim YJ, Seok KO, Kim JH, Chang YJ, Kang HY, Park JH. Nucleolar protein GLTSCR2 stabilizes p53 in response to ribosomal stresses. Cell Death Differ 2012;19(10):1613-1622.
225. Lo D, Lu H. Nucleostemin: Another nucleolar "Twister" of the p53-MDM2 loop. Cell Cycle 2010;9(16):3227-3232.
226. Tang Y, Zhao W, Chen Y, Zhao Y, Gu W. Acetylation is indispensable for p53 activation. Cell 2008;133(4):612-626.
227. Owen HR, Elser M, Cheung E, Gersbach M, Kraus WL, Hottiger MO. MYBBP1a is a novel repressor of NF-kappaB. J Mol Biol 2007;366(3):725-736.
228. Yamauchi T, Keough RA, Gonda TJ, Ishii S. Ribosomal stress induces processing of Mybbp1a and its translocation from the nucleolus to the nucleoplasm. Genes Cells 2008;13(1):27-39.
229. Drakou CE, Malekkou A, Hayes JM, Lederer CW, Leonidas DD, Oikonomakos NG, Lamond AI, Santama N, Zographos SE. hCINAP is an atypical mammalian nuclear adenylate kinase with an ATPase motif: Structural and functional studies. Proteins 2012;80(1):206-220.
230. Malekkou A, Lederer CW, Lamond AI, Santama N. The nuclear ATPase/adenylate kinase hCINAP is recruited to perinucleolar caps generated upon RNA pol.II inhibition. FEBS Lett 2010;584(22):4559-4564.
231. Castro ME, Leal JF, Lleonart ME, Ramon YCS, Carnero A. Loss-of-function genetic screening identifies a cluster of ribosomal proteins regulating p53 function. Carcinogenesis 2008;29(7):1343-1350.
232. MacInnes AW, Amsterdam A, Whittaker CA, Hopkins N, Lees JA. Loss of p53 synthesis in zebrafish tumors with ribosomal protein gene mutations. Proc Natl Acad Sci USA 2008;105(30):10408-10413.
233. Budde A, Grummt I. p53 represses ribosomal gene transcription. Oncogene 1999;18(4):1119-1124.
234. Zhai W, Comai L. Repression of RNA polymerase I transcription by the tumor suppressor p53. Mol Cell Biol 2000;20(16):5930-5938.
235. Li J, Tan J, Zhuang L, Banerjee B, Yang X, Chau JF, Lee PL, Hande MP, Li B, Yu Q. Ribosomal protein S27-like, a p53-inducible modulator of cell fate in response to genotoxic stress. Cancer Res 2007;67(23):11317-11326.
236. Loging WT, Reisman D. Elevated expression of ribosomal protein genes L37, RPP-1, and S2 in the presence of mutant p53. Cancer Epidemiol Biomarkers Prev 1999;8(11):1011-1016.
237. Donati G, Montanaro L, Derenzini M. Ribosome biogenesis and control of cell proliferation: p53 is not alone. Cancer Res 2012;72(7):1602-1607.
238. Dai MS, Lu H. Crosstalk between c-Myc and ribosome in ribosomal biogenesis and cancer. J Cell Biochem 2008;105(3):670-677.
239. Dai MS, Sears R, Lu H. Feedback regulation of c-Myc by ribosomal protein L11. Cell Cycle 2007;6(22):2735-2741.
240. Dai MS, Sun XX, Lu H. Ribosomal protein L11 associates with c-Myc at 5 S rRNA and tRNA genes and regulates their expression. J Biol Chem 2010;285(17):12587-12594.
241. Challagundla KB, Sun XX, Zhang X, DeVine T, Zhang Q, Sears RC, Dai MS. Ribosomal protein L11 recruits miR-24/miRISC to repress c-Myc expression in response to ribosomal stress. Mol Cell Biol 2011;31(19):4007-4021.
242. Van Riggelen J, Yetil A, Felsher DW. MYC as a regulator of ribosome biogenesis and protein synthesis. Nat Rev Cancer 2010;10(4):301-309.
243. Iadevaia V, Caldarola S, Biondini L, Gismondi A, Karlsson S, Dianzani I, Loreni F. PIM1 kinase is destabilized by ribosomal stress causing inhibition of cell cycle progression. Oncogene 2010;29(40):5490-5469.
244. Donati G, Brighenti E, Vici M, Mazzini G, Trere D, Montanaro L, Derenzini M. Selective inhibition of rRNA transcription downregulates E2F-1: A new p53-independent mechanism linking cell growth to cell proliferation. J Cell Sci 2011;124(17):3017-3028.
245. Wanzel M, Russ AC, Kleine-Kohlbrecher D, Colombo E, Pelicci PG, Eilers M. A ribosomal protein L23-nucleophosmin circuit coordinates Miz1 function with cell growth. Nat Cell Biol 2008;10(9):1051-1061.
246. Russo A, Esposito D, Catillo M, Pietropaolo C, Crescenzi E, Russo G. Human rpL3 induces G(1)/S arrest or apoptosis by modulating p21(waf1/cip1) levels in a p53-independent manner. Cell Cycle 2013;12(1):76-87.
247. Wang YW, Qu Y, Li JF, Chen XH, Liu BY, Gu QL, Zhu ZG. In vitro and in vivo evidence of metallopanstimulin-1 in gastric cancer progression and tumorigenicity. Clin Cancer Res 2006;12(16):4965-4973.
248. Kerscher O, Felberbaum R, Hochstrasser M. Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 2006;22:159-180.
249. Xirodimas DP, Saville MK, Bourdon JC, Hay RT, Lane DP. Mdm2-mediated NEDD8 conjugation of p53 inhibits its transcriptional activity. Cell 2004;118(1):83-97.
250. Xirodimas DP, Sundqvist A, Nakamura A, Shen L, Botting C, Hay RT. Ribosomal proteins are targets for the NEDD8 pathway. EMBO Rep 2008;9(3):280-286.
251. Mahata B, Sundqvist A, Xirodimas DP. Recruitment of RPL11 at promoter sites of p53-regulated genes upon nucleolar stress through NEDD8 and in an Mdm2-dependent manner. Oncogene 2012;31(25):3060-3071.
252. Kim SH, Lee JY, Kim J. Characterization of a wide range base-damage-endonuclease activity of mammalian rpS3. Biochem Biophys Res Commun 2005;328(4):962-967.
253. Kim TS, Kim HD, Kim J. PKCdelta-dependent functional switch of rpS3 between translation and DNA repair. Biochim Biophys Acta 2009;1793(2):395-405.
254. Kim TS, Kim HD, Shin HS, Kim J. Phosphorylation status of nuclear ribosomal protein S3 is reciprocally regulated by protein kinase C{delta} and protein phosphatase 2A. J Biol Chem 2009;284(32):21201-21208.
255. Kim HD, Lee JY, Kim J. Erk phosphorylates threonine 42 residue of ribosomal protein S3. Biochem Biophys Res Commun 2005;333(1):110-115.
256. Krieg J, Hofsteenge J, Thomas G. Identification of the 40 S ribosomal protein S6 phosphorylation sites induced by cycloheximide. J Biol Chem 1988;263(23):11473-11477.
257. Hutchinson JA, Shanware NP, Chang H, Tibbetts RS. Regulation of ribosomal protein S6 phosphorylation by casein kinase 1 and protein phosphatase 1. J Biol Chem 2011;286(10):8688-8696.
258. Meyuhas O. Physiological roles of ribosomal protein S6: One of its kind. Int Rev Cell Mol Biol 2008;268:1-37.
259. Ruvinsky I, Meyuhas O. Ribosomal protein S6 phosphorylation: From protein synthesis to cell size. Trends Biochem Sci 2006;31(6):342-348.
260. Ruvinsky I, Katz M, Dreazen A, Gielchinsky Y, Saada A, Freedman N, Mishani E, Zimmerman G, Kasir J, Meyuhas O. Mice deficient in ribosomal protein S6 phosphorylation suffer from muscle weakness that reflects a growth defect and energy deficit. PLoS One 2009;4(5):e5618.
261. Khalaileh A, Dreazen A, Khatib A, Apel R, Swisa A, Kidess-Bassir N, Maitra A, Meyuhas O, Dor Y, Zamir G. Phosphorylation of ribosomal protein S6 attenuates DNA damage and tumor suppression during development of pancreatic cancer. Cancer Res 2013;73(6):1811-1820.
262. Hay RT. SUMO: A history of modification. Mol Cell 2005;18(1):1-12.
263. Haindl M, Harasim T, Eick D, Muller S. The nucleolar SUMO-specific protease SENP3 reverses SUMO modification of nucleophosmin and is required for rRNA processing. EMBO Rep. 2008; 9(3): 273-279.
264. Jang CY, Shin HS, Kim HD, Kim JW, Choi SY, Kim J. Ribosomal protein S3 is stabilized by sumoylation. Biochem Biophys Res Commun 2011;414(3):523-527.
265. Janas MM, Wang E, Love T, Harris AS, Stevenson K, Semmelmann K, Shaffer JM, Chen PH, Doench JG, Yerramilli SV, Neuberg DS, Iliopoulos D, Housman DE, Burge CB, Novina CD. Reduced expression of ribosomal proteins relieves microRNA-mediated repression. Mol Cell 2012;46(2):171-186.
266. Frum RA, Zhang YP. The RP-p53-Mdm2 pathway: A new link to genetic integrity? Cell Cycle 2010;9(22):4427-4432.
267. Dai MS, Challagundla KB, Sun XX, Palam LR, Zeng SX, Wek RC, Lu H. Physical and functional interaction between ribosomal protein L11 and the tumor suppressor ARF. J Biol Chem 2012;287(21):17120-17129.
268. Oliver ER, Saunders TL, Tarle SA, Glaser T. Ribosomal protein L24 defect in belly spot and tail (Bst), a mouse Minute. Development 2004;131(16):3907-3920.
269. Barkic M, Crnomarkovic S, Grabusic K, Bogetic I, Panic L, Tamarut S, Cokaric M, Jeric I, Vidak S, Volarevic S. The p53 tumor suppressor causes congenital malformations in Rpl24-deficient mice and promotes their survival. Mol Cell Biol 2009;29(10):2489-2504.
270. Terzian T, Dumble M, Arbab F, Thaller C, Donehower LA, Lozano G, Justice MJ, Roop DR, Box NF. Rpl27a mutation in the sooty foot ataxia mouse phenocopies high p53 mouse models. J Pathol 2011;224(4):540-552.
271. Kirn-Safran CB, Oristian DS, Focht RJ, Parker SG, Vivian JL, Carson DD. Global growth deficiencies in mice lacking the ribosomal protein HIP/RPL29. Dev Dyn 2007;236(2):447-460.
272. Saeboe-Larssen S, Lyamouri M, Merriam J, Oksvold MP, Lambertsson A. Ribosomal protein insufficiency and the minute syndrome in Drosophila: A dose-response relationship. Genetics 1998;148(3):1215-1224.
273. Amsterdam A, Nissen RM, Sun Z, Swindell EC, Farrington S, Hopkins N. Identification of 315 genes essential for early zebrafish development. Proc Natl Acad Sci USA 2004;101(35):12792-12797.
274. Ishijima J, Yasui H, Morishima M, Shiroishi T. Dominant lethality of the mouse skeletal mutation Tail-short (Ts) is determined by the Ts allele from mating partners. Genomics 1998; 49(3): 341-350.
275. Terzian T, Dumble M, Arbab F, Thaller C, Donehower LA, Lozano G, Justice MJ, Roop DR, Box NF. Rpl27a mutation in the sooty foot ataxia mouse phenocopies high p53 mouse models. J Pathol 2011;224(4):540-552.
276. Kondrashov N, Pusic A, Stumpf CR, Shimizu K, Hsieh AC, Xue S, Ishijima J, Shiroishi T, Barna M. Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning. Cell 2011;145(3):383-397.
277. Chiocchetti A, Pakalapati G, Duketis E, Wiemann S, Poustka A, Poustka F, Klauck SM. Mutation and expression analyses of the ribosomal protein gene RPL10 in an extended German sample of patients with autism spectrum disorder. Am J Med Genet A 2011;155A(6):1472-1475.
278. Gong X, Delorme R, Fauchereau F, Durand CM, Chaste P, Betancur C, Goubran-Botros H, Nygren G, Anckarsäter H, Rastam M, Gillberg IC, Kopp S, Mouren-Simeoni MC, Gillberg C, Leboyer M, Bourgeron T. An investigation of ribosomal protein L10 gene in autism spectrum disorders. BMC Med Genet 2009;10:7.
279. Klauck SM, Felder B, Kolb-Kokocinski A, Schuster C, Chiocchetti A, Schupp I, Wellenreuther R, Schmötzer G, Poustka F, Breitenbach-Koller L, Poustka A. Mutations in the ribosomal protein gene RPL10 suggest a novel modulating disease mechanism for autism. Mol Psychiatry 2006;11(12):1073-1084.
280. Terzian T, Box N. Genetics of ribosomal proteins: "Curiouser and curiouser". PLoS Genet 2013;9(1):e1003300.
281. Alexander SJ, Woodling NS, Yedvobnick B. Insertional inactivation of the L13a ribosomal protein gene of Drosophila melanogaster identifies a new Minute locus. Gene 2006;368:46-52.
282. Van Beest M, Mortin M, Clevers H. Drosophila RpS3a, a novel Minute gene situated between the segment polarity genescubitus interruptus and dTCF. Nucleic Acids Res 1998;26(19):4471-4475.
283. Casad ME, Abraham D, Kim IM, Frangakis S, Dong B, Lin N, Wolf MJ, Rockman HA. Cardiomyopathy is associated with ribosomal protein gene haplo-insufficiency in Drosophila melanogaster. Genetics 2011;189(3):861-870.
284. Hay N, Sonenberg N. Upstream and downstream of mTOR. Genes Dev 2004;18(16):1926-1945.
285. Di R, Wu X, Chang Z, Zhao X, Feng Q, Lu S, Luan Q, Hemmings BA, Li X, Yang Z. S6K inhibition renders cardiac protection against myocardial infarction through PDK1 phosphorylation of Akt. Biochem J 2012;441(1):199-207.
286. Treins C, Alliouachene S, Hassouna R, Xie Y, Birnbaum MJ, Pende M. The combined deletion of S6K1 and Akt2 deteriorates glycemic control in a high-fat diet. Mol Cell Biol 2012;32(19):4001-4011.
287. Li S, Ogawa W, Emi A, Hayashi K, Senga Y, Nomura K, Hara K, Yu D, Kasuga M. Role of S6K1 in regulation of SREBP1c expression in the liver. Biochem Biophys Res Commun 2011;412(2):197-202.
288. Um SH, Frigerio F, Watanabe M, Picard F, Joaquin M, Sticker M, Fumagalli S, Allegrini PR, Kozma SC, Auwerx J, Thomas G. Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 2004;431(7005):200-205.
289. Michel CI, Holley CL, Scruggs BS, Sidhu R, Brookheart RT, Listenberger LL, Behlke MA, Ory DS, Schaffer JE. Small nucleolar RNAs U32a, U33, and U35a are critical mediators of metabolic stress. Cell Metab 2011;14(1):33-44.
290. Chaudhuri S, Vyas K, Kapasi P, Komar AA, Dinman JD, Barik S, Mazumder B. Human ribosomal protein L13a is dispensable for canonical ribosome function but indispensable for efficient rRNA methylation. RNA 2007;13(12):2224-2237.
291. Flygare J, Karlsson S. Diamond-Blackfan anemia: Erythropoiesis lost in translation. Blood 2007;109(8):3152-3154.
292. Gazda HT, Grabowska A, Merida-Long LB, Latawiec E, Schneider HE, Lipton JM, Vlachos A, Atsidaftos E, Ball SE, Orfali KA, Niewiadomska E, Da Costa L, Tchernia G, Niemeyer C, Meerpohl JJ, Stahl J, Schratt G, Glader B, Backer K, Wong C, Nathan DG, Beggs AH, Sieff CA. Ribosomal protein S24 gene is mutated in Diamond-Blackfan anemia. Am J Hum Genet 2006;79(6):1110-1118.
293. Cmejla R, Cmejlova J, Handrkova H, Petrak J, Petrtylova K, Mihal V, Stary J, Cerna Z, Jabali Y, Pospisilova D. Identification of mutations in the ribosomal protein L5 (RPL5) and ribosomal protein L11 (RPL11) genes in Czech patients with Diamond-Blackfan anemia. Hum Mutat 2009;30(3):321-327.
294. Gazda HT, Sheen MR, Vlachos A, Choesmel V, O'Donohue MF, Schneider H, Darras N, Hasman C, Sieff CA, Newburger PE, Ball SE, Niewiadomska E, Matysiak M, Zaucha JM, Glader B, Niemeyer C, Meerpohl JJ, Atsidaftos E, Lipton JM, Gleizes PE, Beggs AH. Ribosomal protein L5 and L11 mutations are associated with cleft palate and abnormal thumbs in Diamond-Blackfan anemia patients. Am J Hum Genet 2008;83(6):769-780.
295. Gazda HT, Preti M, Sheen MR, O'Donohue MF, Vlachos A, Davies SM, Kattamis A, Doherty L, Landowski M, Buros C, Ghazvinian R, Sieff CA, Newburger PE, Niewiadomska E, Matysiak M, Glader B, Atsidaftos E, Lipton JM, Gleizes PE, Beggs AH. Frameshift mutation in p53 regulator RPL26 is associated with multiple physical abnormalities and a specific pre-ribosomal RNA processing defect in diamond-blackfan anemia. Hum Mutat 2012;33(7):1037-1044.
296. Doherty L, Sheen MR, Vlachos A, Choesmel V, O'Donohue MF, Clinton C, Schneider HE, Sieff CA, Newburger PE, Ball SE, Niewiadomska E, Matysiak M, Glader B, Arceci RJ, Farrar JE, Atsidaftos E, Lipton JM, Gleizes PE, Gazda HT. Ribosomal protein genes RPS10 and RPS26 are commonly mutated in Diamond-Blackfan anemia. Am J Hum Genet 2010;86(2):222-228.
297. Landowski M, O'Donohue MF, Buros C, Ghazvinian R, Montel-Lehry N, Vlachos A, Sieff CA, Newburger PE, Niewiadomska E, Matysiak M, Glader B, Atsidaftos E, Lipton JM, Beggs AH, Gleizes PE, Gazda HT. Novel deletion of RPL15 identified by array-comparative genomic hybridization in Diamond-Blackfan anemia. Hum Genet 2013;132(11):1265-1274.
298. Choesmel V, Bacqueville D, Rouquette J, Noaillac-Depeyre J, Fribourg S, Cretien A, Leblanc T, Tchernia G, Da Costa L, Gleizes PE. Impaired ribosome biogenesis in Diamond-Blackfan anemia. Blood 2007;109(3):1275-1283.
299. Danilova N, Sakamoto KM, Lin S. Ribosomal protein S19 deficiency in zebrafish leads to developmental abnormalities and defective erythropoiesis through activation of p53 protein family. Blood 2008;112(13):5228-5237.
300. Barlow JL, Drynan LF, Trim NL, Erber WN, Warren AJ, McKenzie AN. New insights into 5q- syndrome as a ribosomopathy. Cell Cycle 2010;9(21):4286-4293.
301. Starczynowski DT, Kuchenbauer F, Argiropoulos B, Sung S, Morin R, Muranyi A, Hirst M, Hogge D, Marra M, Wells RA, Buckstein R, Lam W, Humphries RK, Karsan A. Identification of miR-145 and miR-146a as mediators of the 5q- syndrome phenotype. Nat Med 2010;16(1):49-58.
302. Pellagatti A, Marafioti T, Paterson JC, Barlow JL, Drynan LF, Giagounidis A, Pileri SA, Cazzola M, McKenzie AN, Wainscoat JS, Boultwood J. Induction of p53 and up-regulation of the p53 pathway in the human 5q- syndrome. Blood 2010;115(13):2721-2723.
303. Sakai D, Trainor PA. Treacher Collins syndrome: Unmasking the role of Tcof1/treacle. Int J Biochem Cell Biol 2009;41(6):1229-1232.
304. Freed EF, Bleichert F, Dutca LM, Baserga SJ. When ribosomes go bad: Diseases of ribosome biogenesis. Mol Biosyst 2010;6(3):481-493.
305. Jones NC, Lynn ML, Gaudenz K, Sakai D, Aoto K, Rey JP, Glynn EF, Ellington L, Du C, Dixon J, Dixon MJ, Trainor PA. Prevention of the neurocristopathy Treacher Collins syndrome through inhibition of p53 function. Nat Med 2008;14(2):125-133.
306. Ganapathi KA, Shimamura A. Ribosomal dysfunction and inherited marrow failure. Br J Haematol 2008;141(3):376-387.
307. Burroughs L, Woolfrey A, Shimamura A. Shwachman-Diamond syndrome: A review of the clinical presentation, molecular pathogenesis, diagnosis, and treatment. Hematol Oncol Clin North Am 2009;23(2):233-248.
308. Boocock GR, Morrison JA, Popovic M, Richards N, Ellis L, Durie PR, Rommens JM. Mutations in SBDS are associated with Shwachman-Diamond syndrome. Nat Genet 2003;33(1):97-101.
309. Ganapathi KA, Austin KM, Lee CS, Dias A, Malsch MM, Reed R, Shimamura A. The human Shwachman-Diamond syndrome protein, SBDS, associates with ribosomal RNA. Blood 2007;110(5):1458-1465.
310. Rujkijyanont P, Adams SL, Beyene J, Dror Y. Bone marrow cells from patients with Shwachman-Diamond syndrome abnormally express genes involved in ribosome biogenesis and RNA processing. Br J Haematol 2009;145(6):806-815.
311. Liu JM, Ellis SR. Ribosomes and marrow failure: coincidental association or molecular paradigm? Blood 2006;107(12):4583-4588.
312. Dhanraj S, Manji A, Pinto D, Scherer SW, Favre H, Loh ML, Chetty R, Wei AC, Dror Y. Molecular characteristics of a pancreatic adenocarcinoma associated with Shwachman-Diamond syndrome. Pediatr Blood Cancer 2013;60(5):754-760.
313. Boon K, Caron HN, van Asperen R, Valentijn L, Hermus MC, van Sluis P, Roobeek I, Weis I, Voute PA, Schwab M, Versteeg R. N-myc enhances the expression of a large set of genes functioning in ribosome biogenesis and protein synthesis. EMBO J 2001;20(6):1383-1393.
314. Ruggero D. The role of Myc-induced protein synthesis in cancer. Cancer Res 2009;69(23):8839-8843.
315. Arabi A, Wu S, Ridderstrale K, Bierhoff H, Shiue C, Fatyol K, Fahlén S, Hydbring P, Söderberg O, Grummt I, Larsson LG, Wright AP. c-Myc associates with ribosomal DNA and activates RNA polymerase I transcription. Nat Cell Biol 2005;7(3):303-310.
316. Schlosser I, Holzel M, Murnseer M, Burtscher H, Weidle UH, Eick D. A role for c-Myc in the regulation of ribosomal RNA processing. Nucleic Acids Res 2003;31(21):6148-6156.
317. Barna M, Pusic A, Zollo O, Costa M, Kondrashov N, Rego E, Rao PH, Ruggero D. Suppression of Myc oncogenic activity by ribosomal protein haploinsufficiency. Nature 2008;456(7224):971-975.
318. Felton-Edkins ZA, Kenneth NS, Brown TR, Daly NL, Gomez-Roman N, Grandori C, Eisenman RN, White RJ. Direct regulation of RNA polymerase III transcription by RB, p53 and c-Myc. Cell Cycle 2003;2(3):181-184.
319. Amsterdam A, Sadler KC, Lai K, Farrington S, Bronson RT, Lees JA, Hopkins N. Many ribosomal protein genes are cancer genes in zebrafish. PLoS Biol 2004;2(5):E139.
320. Viswanathan SR, Powers JT, Einhorn W, Hoshida Y, Ng TL, Toffanin S, O'Sullivan M, Lu J, Phillips LA, Lockhart VL, Shah SP, Tanwar PS, Mermel CH, Beroukhim R, Azam M, Teixeira J, Meyerson M, Hughes TP, Llovet JM, Radich J, Mullighan CG, Golub TR, Sorensen PH, Daley GQ. Lin28 promotes transformation and is associated with advanced human malignancies. Nat Genet 2009;41(7):843-848.
321. King CE, Wang L, Winograd R, Madison BB, Mongroo PS, Johnstone CN, Rustgi AK. LIN28B fosters colon cancer migration, invasion and transformation through let-7-dependent and -independent mechanisms. Oncogene 2011;30(40):4185-4193.
322. Lindstrom MS, Jin A, Deisenroth C, White Wolf G, Zhang Y. Cancer-associated mutations in the MDM2 zinc finger domain disrupt ribosomal protein interaction and attenuate MDM2-induced p53 degradation. Mol Cell Biol 2007;27(3):1056-1068.
323. Macias E, Jin A, Deisenroth C, Bhat K, Mao H, Lindstrom MS, Zhang Y. An ARF-independent c-MYC-activated tumor suppression pathway mediated by ribosomal protein-Mdm2 Interaction. Cancer Cell 2010;18(3):231-243.
324. Shi Y, Zhai H, Wang X, Han Z, Liu C, Lan M, Du J, Guo C, Zhang Y, Wu K, Fan D. RPsS13 and L23 promote multidrug resistance in gastric cancer cells by suppressing drug-induced apoptosis. Exp Cell Res 2004;296(2):337-346.
325. Kondoh N, Shuda M, Tanaka K, Wakatsuki T, Hada A, Yamamoto M. Enhanced expression of S8, L12, L23a, L27 and L30 ribosomal protein mRNAs in human hepatocellular carcinoma. Anticancer Res 2001;21(4A):2429-2433.
326. Song MJ, Jung CK, Park CH, Hur W, Choi JE, Bae SH, Choi JY, Choi SW, Han NI, Yoon SK. RPL36 as a prognostic marker in hepatocellular carcinoma. Pathol Int 2011;61(11):638-644.
327. Kobayashi T, Sasaki Y, Oshima Y, Yamamoto H, Mita H, Suzuki H, Toyota M, Tokino T, Itoh F, Imai K, Shinomura Y. Activation of the ribosomal protein L13 gene in human gastrointestinal cancer. Int J Mol Med 2006;18(1):161-170.
328. Lai MD, Xu J. Ribosomal proteins and colorectal cancer. Curr Genomics 2007;8(1):43-49.
329. Pogue-Geile K, Geiser JR, Shu M, Miller C, Wool IG, Meisler AI, Pipas JM. Ribosomal protein genes are overexpressed in colorectal cancer: Isolation of a cDNA clone encoding the human S3 ribosomal protein. Mol Cell Biol 1991;11(8):3842-3849.
330. Kasai H, Nadano D, Hidaka E, Higuchi K, Kawakubo M, Sato TA, Nakayama J. Differential expression of ribosomal proteins in human normal and neoplastic colorectum. J Histochem Cytochem 2003;51(5):567-574.
331. Huang CJ, Chien CC, Yang SH, Chang CC, Sun HL, Cheng YC, Liu CC, Lin SC, Lin CM. Faecal ribosomal protein L19 is a genetic prognostic factor for survival in colorectal cancer. J Cell Mol Med 2008;12(5B):1936-1943.
332. Ojala P, Sundstrom J, Gronroos JM, Virtanen E, Talvinen K, Nevalainen TJ. mRNA differential display of gene expression in colonic carcinoma. Electrophoresis 2002;23(11):1667-1676.
333. Huang CJ, Yang SH, Lee CL, Cheng YC, Tai SY, Chien CC. Ribosomal protein s27-like in colorectal cancer: a candidate for predicting prognoses. PLoS One 2013;8(6):e67043.
334. Bee A, Ke Y, Forootan S, Lin K, Beesley C, Forrest SE, Foster CS. Ribosomal protein l19 is a prognostic marker for human prostate cancer. Clin Cancer Res 2006;12(7 Pt 1):2061-2065.
335. Bee A, Brewer D, Beesley C, Dodson A, Forootan S, Dickinson T, Gerard P, Lane B, Yao S, Cooper CS, Djamgoz MB, Gosden CM, Ke Y, Foster CS. siRNA knockdown of ribosomal protein gene RPL19 abrogates the aggressive phenotype of human prostate cancer. PLoS One 2011;6(7):e22672.
336. Ohkia A, Hu Y, Wang M, Garcia FU, Stearns ME. Evidence for prostate cancer-associated diagnostic marker-1: Immunohistochemistry and in situ hybridization studies. Clin Cancer Res 2004;10(7):2452-2458.
337. Wang M, Hu YJ, Stearns ME. RPS2: a novel therapeutic target in prostate cancer. J Exp Clin Cancer Res 2009;28:6.
338. Huang XP, Zhao CX, Li QJ, Cai Y, Liu FX, Hu H, Xu X, Han YL, Wu M, Zhan QM, Wang MR. Alteration of RPL14 in squamous cell carcinomas and preneoplastic lesions of the esophagus. Gene 2006;366(1):161-168.
339. Wang Q, Yang C, Zhou J, Wang X, Wu M, Liu Z. Cloning and characterization of full-length human ribosomal protein L15 cDNA which was overexpressed in esophageal cancer. Gene 2001;263(1-2):205-209.
340. Kim SH, Jang YH, Chau GC, Pyo S, Um SH. Prognostic significance and function of phosphorylated ribosomal protein S6 in esophageal squamous cell carcinoma. Mod Pathol 2013;26(3):327-335.
341. Yang M, Sun H, Wang H, Zhang S, Yu X, Zhang L. Down-regulation of ribosomal protein L22 in non-small cell lung cancer. Med Oncol 2013;30(3):646.
342. Zheng SE, Yao Y, Dong Y, Lin F, Zhao H, Shen Z, Sun YJ, Tang LN. Down-regulation of ribosomal protein L7A in human osteosarcoma. J Cancer Res Clin Oncol 2009;135(8):1025-1031.
343. Hagner PR, Mazan-Mamczarz K, Dai B, Balzer EM, Corl S, Martin SS, Zhao XF, Gartenhaus RB. Ribosomal protein S6 is highly expressed in non-Hodgkin lymphoma and associates with mRNA containing a 5′ terminal oligopyrimidine tract. Oncogene 2011;30(13):1531-1541.
344. Wu LY, Li X, Xu F, Chang CK, He Q, Zhang Z, Zhng Y. Over-expression of RPL23 in myelodysplastic syndromes is associated with apoptosis resistance of CD34(+) cells and predicts poor prognosis and distinct response to CHG chemotherapy or decitabine. Ann Hematol 2012;91(10):1547-1554.
345. Tsofack SP, Meunier L, Sanchez L, Madore J, Provencher D, Mes-Masson AM, Lebbel M. Low expression of the X-linked ribosomal protein S4 in human serous epithelial ovarian cancer is associated with a poor prognosis. BMC cancer 2013;13:303.
346. Flygare J, Olsson K, Richter J, Karlsson S. Gene therapy of Diamond-Blackfan anemia CD34(+) cells leads to improved erythroid development and engraftment following transplantation. Exp Hematol 2008;36(11):1428-1435.
347. Wei S, Chen X, McGraw K, Zhang L, Komrokji R, Clark J, Caceres G, Billingsley D, Sokol L, Lancet J, Fortenbery N, Zhou J, Eksioglu EA, Sallman D, Wang H, Epling-Burnette PK, Djeu J, Sekeres M, Maciejewski JP, List A. Lenalidomide promotes p53 degradation by inhibiting MDM2 auto-ubiquitination in myelodysplastic syndrome with chromosome 5q deletion. Oncogene 2013;32(9):1110-1120.
348. Olausson KH, Nistér M, Lindström MS. p53-Dependent and -independent nucleolar stress responses. Cells 2012;1:774-798.
349. Hwang IK, Yoo KY, Kim DW, Kim SY, Park JH, Ryoo ZY, Kim J, Choi SY, Won MH. Ischemia-induced ribosomal protein S3 expressional changes and the neuroprotective effect against experimental cerebral ischemic damage. J Neurosci Res 2008;86(8):1823-1835.
350. Ahn EH, Kim DW, Shin MJ, Kim YN, Kim HR, Woo SJ, Kim SM, Kim DS, Kim J, Park J, Eum WS, Hwang HS, Choi SY. PEP-1-ribosomal protein S3 protects dopaminergic neurons in an MPTP-induced Parkinson's disease mouse model. Free Radic Biol Med 2013;55:36-45.
351. Lv J, Huang XR, Klug J, Frohlich S, Lacher P, Xu A, Meinhardt A, Lan HY. Ribosomal protein S19 is a novel therapeutic agent in inflammatory kidney disease. Clin Sci (Lond) 2013;124(10):627-637.
352. Bywater MJ, Poortinga G, Sanij E, Hein N, Peck A, Cullinane C, Wall M, Cluse L, Drygin D, Anderes K, Huser N, Proffitt C, Bliesath J, Haddach M, Schwaebe MK, Ryckman DM, Rice WG, Schmitt C, Lowe SW, Johnstone RW, Pearson RB, McArthur GA, Hannan RD. Inhibition of RNA polymerase I as a therapeutic strategy to promote cancer-specific activation of p53. Cancer Cell 2012;22(1):51-65.
353. Drygin D, Lin A, Bliesath J, Ho CB, O'Brien SE, Proffitt C, Omori M, Haddach M, Schwaebe MK, Siddiqui-Jain A, Streiner N, Quin JE, Sanij E, Bywater MJ, Hannan RD, Ryckman D, Anderes K, Rice WG. Targeting RNA polymerase I with an oral small molecule CX-5461 inhibits ribosomal RNA synthesis and solid tumor growth. Cancer Res 2011;71(4):1418-1430.
354. Drygin D, Siddiqui-Jain A, O'Brien S, Schwaebe M, Lin A, Bliesath J, Ho CB, Proffitt C, Trent K, Whitten JP, Lim JK, Von Hoff D, Anderes K, Rice WG. Anticancer activity of CX-3543: A direct inhibitor of rRNA biogenesis. Cancer Res 2009;69(19):7653-7661.
355. Wu CT, Lin TY, Hsu HY, Sheu F, Ho CM, Chen EIT. Ling Zhi-8 mediates p53-dependent growth arrest of lung cancer cells proliferation via the ribosomal protein S7-MDM2-p53 pathway. Carcinogenesis 2011;32(12):1890-1896.
356. Zhang YF, Shi YQ, Li XH, Du WQ, Luo GH, Gou YW, Wang X, Guo X, Liu J, Ding J, Wu K, Fan D. Inhibition of the p53-MDM2 interaction by adenovirus delivery of ribosomal protein L23 stabilizes p53 and induces cell cycle arrest and apoptosis in gastric cancer. J Gene Med 2010;12(2):147-156.
357. Pel HJ, Grivell LA. Protein synthesis in mitochondria. Mol Biol Rep 1994;19(3):183-194.
358. O'Brien TW. Properties of human mitochondrial ribosomes. IUBMB Life 2003;55(9):505-513.
359. Suzuki T, Terasaki M, Takemoto-Hori C, Hanada T, Ueda T, Wada A, Watanabe K. Proteomic analysis of the mammalian mitochondrial ribosome. Identification of protein components in the 28 S small subunit. J Biol Chem 2001;276(35):33181-33195.
360. Kissil JL, Cohen O, Raveh T, Kimchi A. Structure-function analysis of an evolutionary conserved protein, DAP3, which mediates TNF-alpha- and Fas-induced cell death. EMBO J 1999;18(2):353-362.
361. Carim L, Sumoy L, Nadal M, Estivill X, Escarceller M. Cloning, expression, and mapping of PDCD9, the human homolog of Gallus gallus pro-apoptotic protein p52. Cytogenet Cell Genet 1999;87(1-2):85-88.
362. Cavdar Koc E, Ranasinghe A, Burkhart W, Blackburn K, Koc H, Moseley A, Spremulli LL. A new face on apoptosis: death-associated protein 3 and PDCD9 are mitochondrial ribosomal proteins. FEBS Lett 2001;492(1-2):166-170.
363. Levshenkova EV, Ukraintsev KE, Orlova VV, Alibaeva RA, Kovriga IE, Zhugdernamzhilyn O, Frolova EI. [The structure and specific features of the cDNA expression of the human gene MRPL37]. Bioorg khim 2004;30(5):499-506.
364. Chintharlapalli SR, Jasti M, Malladi S, Parsa KV, Ballestero RP, Gonzalez-Garcia M. BMRP is a Bcl-2 binding protein that induces apoptosis. J Cell Biochem 2005;94(3):611-626.
365. Yoo YA, Kim MJ, Park JK, Chung YM, Lee JH, Chi SG, Kim JS, Yoo YD. Mitochondrial ribosomal protein L41 suppresses cell growth in association with p53 and p27Kip1. Mol Cell Biol 2005;25(15):6603-6616.
366. Kim MJ, Yoo YA, Kim HJ, Kang S, Kim YG, Kim JS, Yoo YD. Mitochondrial ribosomal protein L41 mediates serum starvation-induced cell-cycle arrest through an increase of p21(WAF1/CIP1). Biochem Biophys Res Comm 2005;338(2):1179-1184.
367. Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, Finetti P, Hur MH, Diebel ME, Monville F, Dutcher J, Brown M, Viens P, Xerri L, Bertucci F, Stassi G, Dontu G, Birnbaum D, Wicha MS. Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res 2009;69(4):1302-1313.
368. Chen YC, Chang MY, Shiau AL, Yo YT, Wu CL. Mitochondrial ribosomal protein S36 delays cell cycle progression in association with p53 modification and p21(WAF1/CIP1) expression. J Cell Biochem 2007;100(4):981-990.
369. Kashuba E, Pavan Yenamandra S, Darekar SD, Yurchenko M, Kashuba V, Klein G, Szekely L. MRPS18-2 protein immortalizes primary rat embryonic fibroblasts and endows them with stem cell-like properties. Proc Natl Acad Sci 2009;106(47):19866-19871.
370. Chung HK, Yi YW, Jung NC, Kim D, Suh JM, Kim H, Park KC, Song JH, Kim DW, Hwang ES, Yoon SH, Bae YS, Kim JM, Bae I, Shong M. CR6-interacting factor 1 interacts with Gadd45 family proteins and modulates the cell cycle. J Biol Chem. 2003;278(30):28079-28088.
371. Handa Y, Hikawa Y, Tochio N, Kogure H, Inoue M, Koshiba S, Güntert P, Inoue Y, Kigawa T, Yokoyama S, Nameki N. Solution structure of the catalytic domain of the mitochondrial protein ICT1 that is essential for cell vitality. J Mol Biol 2010;404(2):260-273.
372. Chen D, Zhang R, Shen W, Fu H, Liu S, Sun K, Sun X. RPS12-specific shRNA inhibits the proliferation, migration of BGC823 gastric cancer cells with S100A4 as a downstream effector. Int J Oncol 2013;42(5):1763-1769.
373. Li H, Beeghly-Fadiel A, Wen W, Lu W, Gao YT, Xiang YB, Cai Q, Long J, Shi J, Chen K, Zheng Y, Shu XO, Zheng W. Gene-environment interactions for breast cancer risk among Chinese women: A report from the Shanghai Breast Cancer Genetics Study. Am J Epidemiol 2013;177(2):161-170.
374. O'Brien KM, Cole SR, Poole C, Bensen JT, Herring AH, Engel LS, Millikan RC. Replication of breast cancer susceptibility loci in whites and African Americans using a Bayesian approach. Am J Epidemiol 2014;179(3):382-394.
375. Bursac S, Brdovcak MC, Donati G, Volarevic S. Activation of the tumor suppressor p53 upon impairment of ribosome biogenesis. Biochim Biophys Acta 2014;1842(6):817-830.
376. Quin JE, Devlin JR, Cameron D, Hannan KM, Pearson RB, Hannan RD. Targeting the nucleolus for cancer intervention. Biochim Biophys Acta 2014;1842(6):802-816.
377. Kapoor NR, Ahuja R, Shukla SK, Kumar V. The HBx protein of hepatitis B virus confers resistance against nucleolar stress and anti-cancer drug-induced p53 expression. FEBS Lett 2013; 587(9):1287-1292.
378. Wade M, Wahl GM. Targeting Mdm2 and Mdmx in cancer therapy: better living through medicinal chemistry? Mol Cancer Res 2009;7(1):1-11.