Feedback regulation of c-Myc by ribosomal protein L11

Cell Cycle

Volumn 6, Issue 22, 2007, Pages 2735-2741

  Dai, Mu Shui ^a   Sears, Rosalie ^b   Lu, Hua ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

c Myc; Cell cycle; L11; Ribosomal protein; Transcription; TRRAP

Indexed keywords

GENE PRODUCT; HISTONE; MYC BOX II PROTEIN; MYC PROTEIN; PROTEIN P53; RIBOSOMAL PROTEIN L11; RIBOSOME PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ACETYLATION; BIOGENESIS; CELL CYCLE; CELL PROLIFERATION; FEEDBACK SYSTEM; GENE ACTIVITY; GENE CONTROL; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HUMAN; NONHUMAN; ONCOGENE; ONCOGENE C MYC; PROTEIN BINDING; REVIEW; TUMOR SUPPRESSOR GENE;

EID: 37249024568     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.6.22.4895     Document Type: Review

References (88)

1. Rotenberg MO, Moritz M, Woolford Jr JL. Depletion of Saccharomyces cerevisiae ribosomal protein L16 causes a decrease in 60S ribosomal subunits and formation of half-mer polyribosomes. Genes and development 1988; 2:160-72.
2. Lambertsson A. The minute genes in Drosophila and their molecular functions. Adv Genet 1998; 38:69-134.
3. 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; 148:1215-24.
4. 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; 21:169-75.
5. Oliver ER, Saunders TL, Tarle SA, Glaser T. Ribosomal protein L24 defect in belly spot and tail (Bst), a mouse Minute. Development 2004; 131:3907-20.
6. Matsson H, Davey EJ, Draptchinskaia N, Hamaguchi I, Ooka A, Leveen P, Forsberg E, Karlsson S, Dahl N. Targeted disruption of the ribosomal protein S19 gene is lethal prior to implantation. Molecular and Cellular Biology 2004; 24:4032-7.
7. 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; 288:2045-7.
8. 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 and Development 2005; 19:3070-82.
9. Panic L, Tamarut S, Sticker-Jantscheff M, Barkic M, Solter D, Uzelac M, Grabusic K, Volarevic S. Ribosomal protein S6 gene haploinsufficiency is associated with activation of a p53-dependent checkpoint during gastrulation. Mol Cell Biol 2006; 26:8880-91.
10. Panic L, Montagne J, Cokaric M, Volarevic S. S6-haploinsufficiency activates the p53 tumor suppressor. Cell Cycle 2007; 6:20-4.
11. 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; 236:447-60.
12. 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; 26:759-72.
13. Ruggero D, Pandolfi PP. Does the ribosome translate cancer? Nat Rev Cancer 2003; 3:179-92.
14. Naora H, Takai I, Adachi M. 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; 141:741-53.
15. De Benedetti A, Graff JR. eIF-4E expression and its role in malignancies and metastases. Oncogene 2004; 23:3189-99.
16. Ruggero D, Montanaro L, Ma L, Xu W, Londei P, Cordon-Cardo C, Pandolfi PP. The translation factor eIF-4E promotes tumor formation and cooperates with c-Myc in lymphomagenesis. Nat Med 2004; 10:484-6.
17. Zhang L, Pan X, Hershey JW. Individual overexpression of five subunits of human translation initiation factor eIF3 promotes malignant transformation of immortal fibroblast cells. The Journal of Biological Chemistry 2007; 282:5790-800.
18. 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; 21:2429-33.
19. Naora H. Involvement of ribosomal proteins in regulating cell growth and apoptosis: Translational modulation or recruitment for extraribosomal activity? Immunol Cell Biol 1999; 77:197-205.
20. Cairns CA, White RJ. p53 is a general repressor of RNA polymerase III transcription. The EMBO Journal 1998; 17:3112-23.
21. Chesnokov I, Chu WM, Botchan MR, Schmid CW. p53 inhibits RNA polymerase III-directed transcription in a promoter-dependent manner. Molecular and Cellular Biology 1996; 16:7084-8.
22. Chu WM, Wang Z, Roeder RG, Schmid CW. RNA polymerase III transcription repressed by Rb through its interactions with TFIIIB and TFIIIC2. The Journal of Biological Chemistry 1997; 272:14755-61.
23. Crighton D, Woiwode A, Zhang C, Mandavia N, Morton JP, Warnock LJ, Milner J, White RJ, Johnson DL. p53 represses RNA polymerase III transcription by targeting TBP and inhibiting promoter occupancy by TFIIIB. The EMBO Journal 2003; 22:2810-20.
24. 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; 2:181-4.
25. Larminie CG, Cairns CA, Mital R, Martin K, Kouzarides T, Jackson SP, White RJ. Mechanistic analysis of RNA polymerase III regulation by the retinoblastoma protein. The EMBO Journal 1997; 16:2061-71.
26. Sutcliffe JE, Brown TR, Allison SJ, Scott PH, White RJ. Retinoblastoma protein disrupts interactions required for RNA polymerase III transcription. Molecular and Cellular Biology 2000; 20:9192-202.
27. Sutcliffe JE, Cairns CA, McLees A, Allison SJ, Tosh K, White RJ. RNA polymerase III transcription factor IIIB is a target for repression by pocket proteins p107 and p130. Molecular and Cellular Biology 1999; 19:4255-61.
28. White RJ, Trouche D, Martin K, Jackson SP, Kouzarides T. Repression of RNA polymerase III transcription by the retinoblastoma protein. Nature 1996; 382:88-90.
29. Budde A, Grummt I. p53 represses ribosomal gene transcription. Oncogene 1999; 18:1119-24.
30. Cavanaugh AH, Hempel WM, Taylor LJ, Rogalsky V, Todorov G, Rothblum LI. Activity of RNA polymerase I transcription factor UBF blocked by Rb gene product. Nature 1995; 374:177-80.
31. Voit R, Schafer K, Grummt I. Mechanism of repression of RNA polymerase I transcription by the retinoblastoma protein. Molecular and Cellular Biology 1997; 17:4230-7.
32. Zhai W, Comai L. Repression of RNA polymerase I transcription by the tumor suppressor p53. Molecular and Cellular Biology 2000; 20:5930-8.
33. Zhang C, Comai L, Johnson DL. PTEN represses RNA Polymerase I transcription by disrupting the SL1 complex. Molecular and Cellular Biology 2005; 25:6899-911.
34. Itahana K, Bhat KP, Jin A, Itahana Y, Hawke D, Kobayashi R, Zhang Y. Tumor suppressor ARF degrades B23, a nucleolar protein involved in ribosome biogenesis and cell proliferation. Molecular Cell 2003; 12:1151-64.
35. Sugimoto M, Kuo ML, Roussel MF, Sherr CJ. Nucleolar Arf tumor suppressor inhibits ribosomal RNA processing. Mol Cell 2003; 11:415-24.
36. Ayrault O, Andrique L, Larsen CJ, Seite P. Human Arf tumor suppressor specifically interacts with chromatin containing the promoter of rRNA genes. Oncogene 2004; 23:8097-104.
37. Morton JP, Kantidakis T, White RJ. RNA polymerase III transcription is repressed in response to the tumour suppressor ARF. Nucleic Acids Research 2007; 35:3046-52.
38. Oskarsson T, Trumpp A. The Myc trilogy: Lord of RNA polymerases. Nat Cell Biol 2005; 7:215-7.
39. Adhikary S, Eilers M. Transcriptional regulation and transformation by Myc proteins. Nat Rev Mol Cell Biol 2005; 6:635-45.
40. Arabi A, Wu S, Ridderstrale K, Bierhoff H, Shiue C, Fatyol K, Fahlen S, Hydbring P, Soderberg O, Grummt I, Larsson LG, Wright AP. c-Myc associates with ribosomal DNA and activates RNA polymerase I transcription. Nature Cell Biology 2005; 7:303-10.
41. Grandori C, Gomez-Roman N, Felton-Edkins ZA, Ngouenet C, Galloway DA, Eisenman RN, White RJ. c-Myc binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I. Nature Cell Biology 2005; 7:311-8.
42. Grewal SS, Li L, Orian A, Eisenman RN, Edgar BA. Myc-dependent regulation of ribosomal RNA synthesis during Drosophila development. Nature Cell Biology 2005; 7:295-302.
43. Gomez-Roman N, Grandori C, Eisenman RN, White RJ. Direct activation of RNA polymerase III transcription by c-Myc. Nature 2003; 421:290-4.
44. Menssen A, Hermeking H. Characterization of the c-MYC-regulated transcriptome by SAGE: Identification and analysis of c-MYC target genes. Proc Natl Acad Sci USA 2002; 99:6274-9.
45. Coller HA, Grandori C, Tamayo P, Colbert T, Lander ES, Eisenman RN, Golub TR. Expression analysis with oligonucleotide microarrays reveals that MYC regulates genes involved in growth, cell cycle, signaling, and adhesion. Proc Natl Acad Sci USA 2000; 97:3260-5.
46. 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; 20:1383-93.
47. Guo QM, Malek RL, Kim S, Chiao C, He M, Ruffy M, Sanka K, Lee NH, Dang CV, Liu ET. Identification of c-myc responsive genes using rat cDNA microarray. Cancer Res 2000; 60:5922-8.
48. 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; 26:5029-37.
49. Dai MS, Lu H. Inhibition of MDM2-mediated p53 ubiquitination and degradation by ribosomal protein L5. The Journal of Biological Chemistry 2004; 279:44475-82.
50. 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. The Journal of Biological Chemistry 2006; 281:24304-13.
51. 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. Molecular and Cellular Biology 2004; 24:7654-68.
52. Jin A, Itahana K, O'Keefe K, Zhang Y. Inhibition of HDM2 and activation of p53 by ribosomal protein L23. Molecular and Cellular Biology 2004; 24:7669-80.
53. Lohrum MA, Ludwig RL, Kubbutat MH, Hanlon M, Vousden KH. Regulation of HDM2 activity by the ribosomal protein L11. Cancer Cell 2003; 3:577-87.
54. 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; 123:49-63.
55. 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. Molecular and Cellular Biology 2003; 23:8902-12.
56. Gilkes DM, Chen L, Chen J. MDMX regulation of p53 response to ribosomal stress. The EMBO Journal 2006; 25:5614-25.
57. Sun XX, Dai MS, Lu H. 5-fluorouracil activation of p53 involves an MDM2-ribosomal protein interaction. The Journal of Biological Chemistry 2007; 282:8052-9.
58. Bhat KP, Itahana K, Jin A, Zhang Y. Essential role of ribosomal protein L11 in mediating growth inhibition-induced p53 activation. Embo J 2004; 23:2402-12.
59. Yuan X, Zhou Y, Casanova E, Chai M, Kiss E, Grone HJ, Schutz G, Grummt I. Genetic inactivation of the transcription factor TIF-IA leads to nucleolar disruption, cell cycle arrest, and p53-mediated apoptosis. Molecular Cell 2005; 19:77-87.
60. 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 G1/S transition. Mol Cell Biol 2001; 21:4246-55.
61. Dai MS, Arnold H, Sun XX, Sears R, Lu H. Inhibition of c-Myc activity by ribosomal protein L11. The EMBO Journal 2007; 26:3332-45.
62. McMahon SB, Van Buskirk HA, Dugan KA, Copeland TD, Cole MD. The novel ATM-related protein TRRAP is an essential cofactor for the c-Myc and E2F oncoproteins. Cell 1998; 94:363-74.
63. Wood MA, McMahon SB, Cole MD. An ATPase/helicase complex is an essential cofactor for oncogenic transformation by c-Myc. Molecular Cell 2000; 5:321-30.
64. Kim SY, Herbst A, Tworkowski KA, Salghetti SE, Tansey WP. Skp2 regulates Myc protein stability and activity. Mol Cell 2003; 11:1177-88.
65. von der Lehr N, Johansson S, Wu S, Bahram F, Castell A, Cetinkaya C, Hydbring P, Weidung I, Nakayama K, Nakayama KI, Soderberg O, Kerppola TK, Larsson LG. The F-box protein Skp2 participates in c-Myc proteosomal degradation and acts as a cofactor for c-Myc-regulated transcription. Mol Cell 2003; 11:1189-200.
66. Vervoorts J, Luscher-Firzlaff JM, Rottmann S, Lilischkis R, Walsemann G, Dohmann K, Austen M, Luscher B. Stimulation of c-MYC transcriptional activity and acetylation by recruitment of the cofactor CBP. EMBO Rep 2003; 4:484-90.
67. Cohen DE, Prochownik EV. A functional hierarchy for c-Myc target genes? Lessons from MT-MC1. Cell Cycle 2006; 5:392-3.
68. Cowling VH, Cole MD. HATs off to capping: A new mechanism for Myc. Cell Cycle 2007; 6:907-9.
69. Davis AC, Wims M, Spotts GD, Hann SR, Bradley A. A null c-myc mutation causes lethality before 10.5 days of gestation in homozygotes and reduced fertility in heterozygous female mice. Genes and Development 1993; 7:671-82.
70. Pelengaris S, Khan M, Evan GI. Suppression of Myc-induced apoptosis in beta cells exposes multiple oncogenic properties of Myc and triggers carcinogenic progression. Cell 2002; 109:321-34.
71. Felsher DW, Bishop JM. Reversible tumorigenesis by MYC in hematopoietic lineages. Mol Cell 1999; 4:199-207.
72. Adams JM, Harris AW, Pinkert CA, Corcoran LM, Alexander WS, Cory S, Palmiter RD, Brinster RL. The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 1985; 318:533-8.
73. Dai MS, Jin Y, Gallegos JR, Lu H. Balance of Yin and Yang: Ubiquitylation-mediated regulation of p53 and c-Myc. Neoplasia 2006; 8:630-44.
74. Sears RC. The life cycle of C-myc: From synthesis to degradation. Cell Cycle 2004; 3:1133-7.
75. Zhang XY, DeSalle LM, McMahon SB. Identification of novel targets of MYC whose transcription requires the essential MbII domain. Cell Cycle 2006; 5:238-41.
76. Datta A, Nag A, Pan W, Hay N, Gartel AL, Colamonici O, Mori Y, Raychaudhuri P. Myc-ARF (alternate reading frame) interaction inhibits the functions of Myc. The Journal of Biological Chemistry 2004; 279:36698-707.
77. Gregory MA, Qi Y, Hann SR. The ARF tumor suppressor: Keeping Myc on a leash. Cell Cycle 2005; 4:249-52.
78. Qi Y, Gregory MA, Li Z, Brousal JP, West K, Hann SR. p19ARF directly and differentially controls the functions of c-Myc independently of p53. Nature 2004; 431:712-7.
79. Amente S, Gargano B, Varrone F, Ruggiero L, Dominguez-Sola D, Lania L, Majello B. p14ARF directly interacts with Myc through the Myc BoxII domain. Cancer Biol Ther 2006; 5:287-91.
80. Grignani F, Lombardi L, Inghirami G, Sternas L, Cechova K, Dalla-Favera R. Negative autoregulation of c-myc gene expression is inactivated in transformed cells. The EMBO Journal 1990; 9:3913-22.
81. Penn LJ, Brooks MW, Laufer EM, Land H. Negative autoregulation of c-myc transcription. The EMBO Journal 1990; 9:1113-21.
82. Zhang W, Wagner BJ, Ehrenman K, Schaefer AW, DeMaria CT, Crater D, DeHaven K, Long L, Brewer G. Purification, characterization, and cDNA cloning of an AU-rich element RNA-binding protein, AUF1. Molecular and Cellular Biology 1993; 13:7652-65.
83. Ma WJ, Cheng S, Campbell C, Wright A, Furneaux H. Cloning and characterization of HuR, a ubiquitously expressed Elav-like protein. The Journal of Biological Chemistry 1996; 271:8144-51.
84. Doyle GA, Betz NA, Leeds PF, Fleisig AJ, Prokipcak RD, Ross J. The c-myc coding region determinant-binding protein: A member of a family of KH domain RNA-binding proteins. Nucleic Acids Research 1998; 26:5036-44.
85. Lee CH, Leeds P, Ross J. Purification and characterization of a polysome-associated endoribonuclease that degrades c-myc mRNA in vitro. The Journal of Biological Chemistry 1998; 273:25261-71.
86. Yeilding NM, Lee WM. Coding elements in exons 2 and 3 target c-myc mRNA downregulation during myogenic differentiation. Molecular and Cellular Biology 1997; 17:2698-707.
87. Noubissi FK, Elcheva I, Bhatia N, Shakoori A, Ougolkov A, Liu J, Minamoto T, Ross J, Fuchs SY, Spiegelman VS. CRD-BP mediates stabilization of betaTrCP1 and c-myc mRNA in response to beta-catenin signalling. Nature 2006; 441:898-901.
88. Welcker M, Orian A, Grim JE, Eisenman RN, Clurman BE. A nucleolar isoform of the Fbw7 ubiquitin ligase regulates c-Myc and cell size. Curr Biol 2004; 14:1852-7.