RPLP1, a crucial ribosomal protein for embryonic development of the nervous system

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Perucho, Laura ^a   Artero Castro, Ana ^b   Guerrero, Sergi ^b   Ramón Y Cajal, Santiago ^b   LLeonart, Matilde E ^b   Wang, Zhao Qi ^a,c  

^a FRITZ LIPMANN INSTITUTE   (Germany)

^b HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLIN E; PROTEIN P53; PROTEIN RPLP1; RIBOSOME PROTEIN; UNCLASSIFIED DRUG; RPLP1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GENE; GENE DELETION; GENE INACTIVATION; HETEROZYGOSITY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RPLP1 GENE; SENESCENCE; ANIMAL; BODY SIZE; CELL CULTURE; CELL PROLIFERATION; CONGENITAL ABNORMALITIES; CYTOLOGY; EMBRYOLOGY; ESSENTIAL GENE; FIBROBLAST; GENETICS; LETHAL GENE; MALE; MALE INFERTILITY; METABOLISM; NERVOUS SYSTEM; NEWBORN; PATHOLOGY;

ANIMALS; ANIMALS, NEWBORN; BODY SIZE; CELL PROLIFERATION; CELLS, CULTURED; CONGENITAL ABNORMALITIES; FIBROBLASTS; GENE DELETION; GENE KNOCKOUT TECHNIQUES; GENES, ESSENTIAL; GENES, LETHAL; INFERTILITY, MALE; MALE; MICE; NERVOUS SYSTEM; RIBOSOMAL PROTEINS;

EID: 84903516698     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0099956     Document Type: Article

References (65)

1. Kondrashov N, Pusic A, Stumpf CR, Shimizu K, Hsieh AC, et al. (2011) Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning. Cell 145: 383-397.
2. Panic L, Tamarut S, Sticker-Jantscheff M, Barkic M, Solter D, et al. (2006) Ribosomal protein S6 gene haploinsufficiency is associated with activation of a p53-dependent checkpoint during gastrulation. Molecular and cellular biology 26: 8880-8891. (Pubitemid 44851946)
3. Kongsuwan K, Yu Q, Vincent A, Frisardi MC, Rosbash M, et al. (1985) A Drosophila Minute gene encodes a ribosomal protein. Nature 317: 555-558. (Pubitemid 16224168)
4. Lambertsson A (1998) The minute genes in Drosophila and their molecular functions. Adv Genet 38: 69-134.
5. Marygold SJ, Roote J, Reuter G, Lambertsson A, Ashburner M, et al. (2007) The ribosomal protein genes and Minute loci of Drosophila melanogaster. Genome biology 8: R216.
6. Yoshihama M, Uechi T, Asakawa S, Kawasaki K, Kato S, et al. (2002) The human ribosomal protein genes: sequencing and comparative analysis of 73 genes. Genome Res 12: 379-390. (Pubitemid 34233012)
7. Hustert E, Scherer G, Olowson M, Guenet JL, Balling R (1996) Rbt (Rabo torcido), a new mouse skeletal mutation involved in anteroposterior patterning of the axial skeleton, maps close to the Ts (tail-short) locus and distal to the Sox9 locus on chromosome 11. Mamm Genome 7: 881-885. (Pubitemid 126439169)
8. Morgan WC (1950) A new tail-short mutation in the mouse whose lethal effects are conditioned by the residual genotypes. J Hered 41: 208-215.
9. Oliver ER, Saunders TL, Tarle SA, Glaser T (2004) Ribosomal protein L24 defect in belly spot and tail (Bst), a mouse Minute. Development 131: 3907-3920. (Pubitemid 39232151)
10. Moazed D, Robertson JM, Noller HF (1988) Interaction of elongation factors EF-G and EF-Tu with a conserved loop in 23S RNA. Nature 334: 362-364.
11. Uchiumi T, Honma S, Nomura T, Dabbs ER, Hachimori A (2002) Translation elongation by a hybrid ribosome in which proteins at the GTPase center of the Escherichia coli ribosome are replaced with rat counterparts. J Biol Chem 277: 3857-3862. (Pubitemid 34968636)
12. Uchiumi T, Traut RR, Kominami R (1990) Monoclonal antibodies against acidic phosphoproteins P0, P1, and P2 of eukaryotic ribosomes as functional probes. J Biol Chem 265: 89-95.
13. Egebjerg J, Douthwaite SR, Liljas A, Garrett RA (1990) Characterization of the binding sites of protein L11 and the L10.(L12)4 pentameric complex in the GTPase domain of 23 S ribosomal RNA from Escherichia coli. J Mol Biol 213: 275-288. (Pubitemid 20176539)
14. Tsurugi K, Ogata K (1985) Evidence for the exchangeability of acidic ribosomal proteins on cytoplasmic ribosomes in regenerating rat liver. J Biochem 98: 1427-1431. (Pubitemid 16169178)
15. Zinker S, Warner JR (1976) The ribosomal proteins of Saccharomyces cerevisiae. Phosphorylated and exchangeable proteins. J Biol Chem 251: 1799-1807.
16. Martinez-Azorin F, Remacha M, Martinez-Salas E, Ballesta JP (2008) Internal translation initiation on the foot-and-mouth disease virus IRES is affected by ribosomal stalk conformation. FEBS Lett 582: 3029-3032.
17. Nusspaumer G, Remacha M, Ballesta JP (2000) Phosphorylation and N-terminal region of yeast ribosomal protein P1 mediate its degradation, which is prevented by protein P2. EMBO J 19: 6075-6084.
18. Zhang L, Zhou W, Velculescu VE, Kern SE, Hruban RH, et al. (1997) Gene expression profiles in normal and cancer cells. Science 276: 1268-1272. (Pubitemid 27227367)
19. Loging WT, Reisman D (1999) Elevated expression of ribosomal protein genes L37, RPP-1, and S2 in the presence of mutant p53. Cancer Epidemiol Biomarkers Prev 8: 1011-1016. (Pubitemid 29536095)
20. Artero-Castro A, Castellvi J, Garcia A, Hernandez J, Ramon y Cajal S, et al. (2011) Expression of the ribosomal proteins Rplp0, Rplp1, and Rplp2 in gynecologic tumors. Human pathology 42: 194-203.
21. Chen A, Kaganovsky E, Rahimipour S, Ben-Aroya N, Okon E, et al. (2002) Two forms of gonadotropin-releasing hormone (GnRH) are expressed in human breast tissue and overexpressed in breast cancer: a putative mechanism for the antiproliferative effect of GnRH by down-regulation of acidic ribosomal phosphoproteins P1 and P2. Cancer Res 62: 1036-1044. (Pubitemid 34160284)
22. Artero-Castro A, Kondoh H, Fernandez-Marcos PJ, Serrano M, Ramon y Cajal S, et al. (2009) Rplp1 bypasses replicative senescence and contributes to transformation. Exp Cell Res 315: 1372-1383.
23. Remacha M, Jimenez-Diaz A, Bermejo B, Rodriguez-Gabriel MA, Guarinos E, et al. (1995) Ribosomal acidic phosphoproteins P1 and P2 are not required for cell viability but regulate the pattern of protein expression in Saccharomyces cerevisiae. Molecular and cellular biology 15: 4754-4762.
24. Huang C, Mandava CS, Sanyal S (2010) The ribosomal stalk plays a key role in IF2-mediated association of the ribosomal subunits. J Mol Biol 399: 145-153.
25. Ishii K, Washio T, Uechi T, Yoshihama M, Kenmochi N, et al. (2006) Characteristics and clustering of human ribosomal protein genes. BMC Genomics 7: 37.
26. Colome N, Collado J, Bech-Serra JJ, Liiv I, Anton LC, et al. (2010) Increased apoptosis after autoimmune regulator expression in epithelial cells revealed by a combined quantitative proteomics approach. Journal of proteome research 9: 2600-2609.
27. Eymin B, Haugg M, Droin N, Sordet O, Dimanche-Boitrel MT, et al. (1999) p27Kip1 induces drug resistance by preventing apoptosis upstream of cytochrome c release and procaspase-3 activation in leukemic cells. Oncogene 18: 1411-1418. (Pubitemid 29103629)
28. Suzuki A, Tsutomi Y, Yamamoto N, Shibutani T, Akahane K (1999) Mitochondrial regulation of cell death: mitochondria are essential for procaspase 3-p21 complex formation to resist Fas-mediated cell death. Molecular and cellular biology 19: 3842-3847. (Pubitemid 29193843)
29. Feil R, Wagner J, Metzger D, Chambon P (1997) Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem Biophys Res Commun 237: 752-757. (Pubitemid 27434760)
30. Chen QM, Bartholomew JC, Campisi J, Acosta M, Reagan JD, et al. (1998) Molecular analysis of H2O2-induced senescent-like growth arrest in normal human fibroblasts: p53 and Rb control G1 arrest but not cell replication. The Biochemical journal 332 (Pt 1): 43-50. (Pubitemid 28239316)
31. Frippiat C, Chen QM, Remacle J, Toussaint O (2000) Cell cycle regulation in H(2)O(2)-induced premature senescence of human diploid fibroblasts and regulatory control exerted by the papilloma virus E6 and E7 proteins. Experimental gerontology 35: 733-745.
32. Nakayashiki T, Mori H (2013) Genome-wide screening with hydroxyurea reveals a link between nonessential ribosomal proteins and reactive oxygen species production. J Bacteriol 195: 1226-1235.
33. Bargis-Surgey P, Lavergne JP, Gonzalo P, Vard C, Filhol-Cochet O, et al. (1999) Interaction of elongation factor eEF-2 with ribosomal P proteins. Eur J Biochem 262: 606-611. (Pubitemid 29266076)
34. Gomez-Lorenzo MG, Spahn CM, Agrawal RK, Grassucci RA, Penczek P, et al. (2000) Three-dimensional cryo-electron microscopy localization of EF2 in the Saccharomyces cerevisiae 80S ribosome at 17.5 A resolution. EMBO J 19: 2710-2718. (Pubitemid 30323559)
35. Draptchinskaia N, Gustavsson P, Andersson B, Pettersson M, Willig TN, et al. (1999) The gene encoding ribosomal protein S19 is mutated in Diamond-Blackfan anaemia. Nat Genet 21: 169-175. (Pubitemid 29070361)
36. Kirn-Safran CB, Oristian DS, Focht RJ, Parker SG, Vivian JL, et al. (2007) Global growth deficiencies in mice lacking the ribosomal protein HIP/RPL29. Dev Dyn 236: 447-460. (Pubitemid 46233287)
37. Matsson H, Davey EJ, Draptchinskaia N, Hamaguchi I, Ooka A, et al. (2004) Targeted disruption of the ribosomal protein S19 gene is lethal prior to implantation. Molecular and cellular biology 24: 4032-4037. (Pubitemid 38496179)
38. Anderson SJ, Lauritsen JP, Hartman MG, Foushee AM, Lefebvre JM, et al. (2007) Ablation of ribosomal protein L22 selectively impairs alphabeta T cell development by activation of a p53-dependent checkpoint. Immunity 26: 759-772. (Pubitemid 46907667)
39. Chakraborty A, Uechi T, Higa S, Torihara H, Kenmochi N (2009) Loss of ribosomal protein L11 affects zebrafish embryonic development through a p53-dependent apoptotic response. PLoS One 4: e4152.
40. Danilova N, Sakamoto KM, Lin S (2008) Ribosomal protein S19 deficiency in zebrafish leads to developmental abnormalities and defective erythropoiesis through activation of p53 protein family. Blood 112: 5228-5237.
41. Jin A, Itahana K, O'Keefe K, Zhang Y (2004) Inhibition of HDM2 and activation of p53 by ribosomal protein L23. Mol Cell Biol 24: 7669-7680. (Pubitemid 39121492)
42. Lindstrom MS, Nister M (2010) Silencing of ribosomal protein S9 elicits a multitude of cellular responses inhibiting the growth of cancer cells subsequent to p53 activation. PloS one 5: e9578.
43. Sulic S, Panic L, Barkic M, Mercep M, Uzelac M, et al. (2005) Inactivation of S6 ribosomal protein gene in T lymphocytes activates a p53-dependent checkpoint response. Genes Dev 19: 3070-3082. (Pubitemid 41798121)
44. Marone M, Bonanno G, Rutella S, Leone G, Scambia G, et al. (2002) Survival and cell cycle control in early hematopoiesis: role of bcl-2, and the cyclin dependent kinase inhibitors P27 and P21. Leukemia & lymphoma 43: 51-57. (Pubitemid 34223970)
45. Nguyen L, Besson A, Heng JI, Schuurmans C, Teboul L, et al. (2006) p27kip1 independently promotes neuronal differentiation and migration in the cerebral cortex. Genes & development 20: 1511-1524. (Pubitemid 43830657)
46. McAllister SS, Becker-Hapak M, Pintucci G, Pagano M, Dowdy SF (2003) Novel p27(kip1) C-terminal scatter domain mediates Rac-dependent cell migration independent of cell cycle arrest functions. Molecular and cellular biology 23: 216-228. (Pubitemid 36008515)
47. Martinez-Azorin F, Remacha M, Ballesta JP (2008) Functional characterization of ribosomal P1/P2 proteins in human cells. The Biochemical journal 413: 527-534.
48. Mansergh FC, Daly CS, Hurley AL, Wride MA, Hunter SM, et al. (2009) Gene expression profiles during early differentiation of mouse embryonic stem cells. BMC Dev Biol 9: 5.
49. Santos C, Ballesta JP (1995) The highly conserved protein P0 carboxyl end is essential for ribosome activity only in the absence of proteins P1 and P2. J Biol Chem 270: 20608-20614.
50. Mitsui K, Nakagawa T, Tsurugi K (1988) On the size and the role of a free cytosolic pool of acidic ribosomal proteins in yeast Saccharomyces cerevisiae. J Biochem 104: 908-911.
51. van Agthoven A, Kriek J, Amons R, Moller W (1978) Isolation and characterization of the acidic phosphoproteins of 60-S ribosomes from Artemia salina and rat liver. Eur J Biochem 91: 553-565.
52. Saenz-Robles MT, Remacha M, Vilella MD, Zinker S, Ballesta JP (1990) The acidic ribosomal proteins as regulators of the eukaryotic ribosomal activity. Biochimica et biophysica acta 1050: 51-55. (Pubitemid 20285311)
53. Sun L, Xie P, Wada J, Kashihara N, Liu FY, et al. (2008) Rap1b GTPase ameliorates glucose-induced mitochondrial dysfunction. Journal of the American Society of Nephrology: JASN 19: 2293-2301.
54. Yoshida Y, Kawata M, Miura Y, Musha T, Sasaki T, et al. (1992) Microinjection of smg/rap1/Krev-1 p21 into Swiss 3T3 cells induces DNA synthesis and morphological changes. Molecular and cellular biology 12: 3407-3414.
55. Ribeiro-Neto F, Urbani J, Lemee N, Lou L, Altschuler DL (2002) On the mitogenic properties of Rap1b: cAMP-induced G(1)/S entry requires activated and phosphorylated Rap1b. Proceedings of the National Academy of Sciences of the United States of America 99: 5418-5423. (Pubitemid 34411563)
56. Sano R, Reed JC (2013) ER stress-induced cell death mechanisms. Biochimica et biophysica acta 1833: 3460-3470.
57. Robledo S, Idol RA, Crimmins DL, Ladenson JH, Mason PJ, et al. (2008) The role of human ribosomal proteins in the maturation of rRNA and ribosome production. RNA 14: 1918-1929.
58. Morgado-Palacin L, Llanos S, Serrano M (2012) Ribosomal stress induces L11- and p53-dependent apoptosis in mouse pluripotent stem cells. Cell Cycle 11: 503-510.
59. Iadevaia V, Caldarola S, Biondini L, Gismondi A, Karlsson S, et al. (2010) PIM1 kinase is destabilized by ribosomal stress causing inhibition of cell cycle progression. Oncogene 29: 5490-5499.
60. Challagundla KB, Sun XX, Zhang X, DeVine T, Zhang Q, et al. (2011) Ribosomal protein L11 recruits miR-24/miRISC to repress c-Myc expression in response to ribosomal stress. Molecular and cellular biology 31: 4007-4021.
61. de Las Heras-Rubio A, Perucho L, Paciucci R, Vilardell J, Lleonart ME (2013) Ribosomal proteins as novel players in tumorigenesis. Cancer metastasis reviews 10.1007/s10555-013-9460-6.
62. Denoyelle C, Abou-Rjaily G, Bezrookove V, Verhaegen M, Johnson TM, et al. (2006) Anti-oncogenic role of the endoplasmic reticulum differentially activated by mutations in the MAPK pathway. Nature cell biology 8: 1053-1063. (Pubitemid 44473600)
63. Furukawa T, Uchiumi T, Tokunaga R, Taketani S (1992) Ribosomal protein P2, a novel iron-binding protein. Arch Biochem Biophys 298: 182-186.
64. Lopez-Contreras AJ, Ruppen I, Nieto-Soler M, Murga M, Rodriguez-Acebes S, et al. (2013) A proteomic characterization of factors enriched at nascent DNA molecules. Cell Rep 3: 1105-1116.
65. Stoneley M, Willis AE (2004) Cellular internal ribosome entry segments: structures, trans-acting factors and regulation of gene expression. Oncogene 23: 3200-3207. (Pubitemid 38638831)