Lenalidomide promotes p53 degradation by inhibiting MDM2 auto-ubiquitination in myelodysplastic syndrome with chromosome 5q deletion

Oncogene

Volumn 32, Issue 9, 2013, Pages 1110-1120

  Wei, S ^a   Chen, X ^a   McGraw, K ^a   Zhang, L ^a   Komrokji, R ^a   Clark, J ^a   Caceres, G ^a   Billingsley, D ^a   Sokol, L ^a   Lancet, J ^a   Fortenbery, N ^a   Zhou, J ^a   Eksioglu, E A ^a   Sallman, D ^a   Wang, H ^a   Epling Burnette, P K ^a   Djeu, J ^a   Sekeres, M ^b   Maciejewski, J P ^b   List, A ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^b TAUSSIG CANCER INSTITUTE   (United States)

Author keywords

drug resistance; MDM2; myelodysplastic syndrome

Indexed keywords

LENALIDOMIDE; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN MDM2; PROTEIN P53;

5Q- SYNDROME; ALPHA CHAIN; ARTICLE; AUTOUBIQUITINATION; BIOGENESIS; ENZYME INHIBITION; ERYTHROID PRECURSOR CELL; GENE ACTIVATION; GENE DISRUPTION; GENE OVEREXPRESSION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN STABILITY; UBIQUITINATION; UPREGULATION;

ANIMALS; CHROMOSOME DELETION; CHROMOSOMES, HUMAN, PAIR 5; HUMANS; MICE; MYELODYSPLASTIC SYNDROMES; PROTO-ONCOGENE PROTEINS C-MDM2; THALIDOMIDE; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITINATION;

EID: 84874743166     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.139     Document Type: Article

References (48)

1. Nimer SD. Myelodysplastic syndromes. Blood 2008; 111: 4841-4851.
2. Look AT. Molecular Pathogenesis of MDS. Hematology Am Soc Hematol Educ Program 2005 156-160.
3. List A. Lenalidomide-a transforming therapeutic agent in myelodysplastic syndromes. Clin Lymphoma Myeloma 2009; 9(Suppl 3): S302-S304.
4. Ebert BL. Deletion 5q in myelodysplastic syndrome: a paradigm for the study of hemizygous deletions in cancer. Leukemia 2009; 23: 1252-1256.
5. Ebert BL, Pretz J, Bosco J, Chang CY, Tamayo P, Galili N et al. Identification of RPS14 as a 5q- syndrome gene by RNA interference screen. Nature 2008; 451: 335-339.
6. Lehmann S, O'Kelly J, Raynaud S, Funk SE, Sage EH, Koeffler HP. Common deleted genes in the 5q- syndrome: thrombocytopenia and reduced erythroid colony formation in SPARC null mice. Leukemia 2007; 21: 1931-1936.
7. Joslin JM, Fernald AA, Tennant TR, Davis EM, Kogan SC, Anastasi J et al. Haploinsufficiency of EGR1, a candidate gene in the del(5q), leads to the development of myeloid disorders. Blood 2007; 110: 719-726.
8. Starczynowski DT, Kuchenbauer F, Argiropoulos B, Sung S, Morin R, Muranyi A et al. Identification of miR-145 and miR-146a as mediators of the 5q- syndrome phenotype. Nat Med 2010; 16: 49-58.
9. Lohrum MA, Ludwig RL, Kubbutat MH, Hanlon M, Vousden KH. Regulation of HDM2 activity by the ribosomal protein L11. Cancer Cell 2003; 3: 577-587.
10. Zhang Y, Lu H. Signaling to p53: ribosomal proteins find their way. Cancer Cell 2009; 16: 369-377.
11. Fumagalli S, Di Cara A, Neb-Gulati A, Natt F, Schwemberger S, Hall J et al. Absence of nucleolar disruption after impairment of 40S ribosome biogenesis reveals an rpL11-translation-dependent mechanism of p53 induction. Nat Cell Biol 2009; 11: 501-508.
12. Dutt S, Narla A, Lin K, Mullally A, Abayasekara N, Megerdichian C et al. Haploinsufficiency for ribosomal protein genes causes selective activation of p53 in human erythroid progenitor cells. Blood 2011; 117: 2567-2576.
13. 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: 5228-5237.
14. Jones NC, Lynn ML, Gaudenz K, Sakai D, Aoto K, Rey JP et al. Prevention of the neurocristopathy Treacher Collins syndrome through inhibition of p53 function. Nat Med 2008; 14: 125-133.
15. McGowan KA, Li JZ, Park CY, Beaudry V, Tabor HK, Sabnis AJ et al. Ribosomal mutations cause p53-mediated dark skin and pleiotropic effects. Nat Genet 2008; 40: 963-970.
16. Barlow JL, Drynan LF, Hewett DR, Holmes LR, Lorenzo-Abalde S, Lane AL et al. A p53-dependent mechanism underlies macrocytic anemia in a mouse model of human 5q- syndrome. Nat Med 2010; 16: 59-66.
17. List A, Dewald G, Bennett J, Giagounidis A, Raza A, Feldman E et al. Lenalidomide in the myelodysplastic syndrome with chromosome 5q deletion. N Engl J Med 2006; 355: 1456-1465.
18. List A, Kurtin S, Roe DJ, Buresh A, Mahadevan D, Fuchs D et al. Efficacy of lenalidomide in myelodysplastic syndromes. N Engl J Med 2005; 352: 549-557.
19. Wei S, Chen X, Rocha K, Epling-Burnette PK, Djeu JY, Liu Q et al. A critical role for phosphatase haplodeficiency in the selective suppression of deletion 5q MDS by lenalidomide. Proc Natl Acad Sci USA 2009; 106: 12974-12979.
20. Ebert BL. Molecular dissection of the 5q deletion in myelodysplastic syndrome. Semin Oncol 2011; 38: 621-626.
21. Liu G, Terzian T, Xiong S, Van Pelt CS, Audiffred A, Box NF et al. The p53-Mdm2 network in progenitor cell expansion during mouse postnatal development J Pathol 2007; 213: 360-368.
22. Gandhi AK, Kang J, Naziruddin S, Parton A, Schafer PH, Stirling DI. Lenalidomide inhibits proliferation of Namalwa CSN.70 cells and interferes with Gab1 phosphorylation and adaptor protein complex assembly. Leuk Res 2006; 30: 849-858.
23. Kruse JP, Gu W. Modes of p53 regulation. Cell 2009; 137: 609-622.
24. Harris SL, Levine AJ. The p53 pathway: positive and negative feedback loops. Oncogene 2005; 24: 2899-2908.
25. Westermarck J, Hahn WC. Multiple pathways regulated by the tumor suppressor PP2A in transformation. Trends Mol Med 2008; 14: 152-160.
26. Mi J, Bolesta E, Brautigan DL, Larner JM. PP2A regulates ionizing radiation-induced apoptosis through Ser46 phosphorylation of p53. Mol Cancer Ther 2009; 8: 135-140.
27. Meek DW, Hupp TR. The regulation of MDM2 by multisite phosphorylation- opportunities for molecular-based intervention to target tumours? Semin Cancer Biol 2009; 20: 19-28.
28. Okamoto K, Li H, Jensen MR, Zhang T, Taya Y, Thorgeirsson SS et al. Cyclin G recruits PP2A to dephosphorylate Mdm2. Mol Cell 2002; 9: 761-771.
29. Zhou BP, Liao Y, Xia W, Zou Y, Spohn B, Hung MC. HER-2/neu induces p53 ubiquitination via Akt-mediated MDM2 phosphorylation. Nat Cell Biol 2001; 3: 973-982.
30. Meek DW, Knippschild U. Posttranslational modification of MDM2. Mol Cancer Res 2003; 1: 1017-1026.
31. Fang S, Jensen JP, Ludwig RL, Vousden KH, Weissman AM. Mdm2 is a RING fingerdependent ubiquitin protein ligase for itself and p53. J Biol Chem 2000; 275: 8945-8951.
32. Honda R, Yasuda H. Activity of MDM2, a ubiquitin ligase, toward p53 or itself is dependent on the RING finger domain of the ligase. Oncogene 2000; 19: 1473-1476.
33. O'Connor PM, Jackman J, Jondle D, Bhatia K, Magrath I, Kohn KW. Role of the p53 tumor suppressor gene in cell cycle arrest and radiosensitivity of Burkitt's lymphoma cell lines. Cancer Res 1993; 53: 4776-4780.
34. Ginzinger DG, Godfrey TE, Nigro J, Moore 2nd DH, Suzuki S, Pallavicini MG et al. Measurement of DNA copy number at microsatellite loci using quantitative PCR analysis. Cancer Res 2000; 60: 5405-5409.
35. Dai MS, Shi D, Jin Y, Sun XX, Zhang Y, Grossman SR et al. Regulation of the MDM2- p53 pathway by ribosomal protein L11 involves a post-ubiquitination mechanism. J Biol Chem 2006; 281: 24304-24313.
36. Quarello P, Garelli E, Carando A, Brusco A, Calabrese R, Dufour C et al. Diamond- Blackfan anemia: genotype-phenotype correlations in Italian patients with RPL5 and RPL11 mutations. Haematologica 2010; 95: 206-213.
37. Ogawara Y, Kishishita S, Obata T, Isazawa Y, Suzuki T, Tanaka K et al. Akt enhances Mdm2-mediated ubiquitination and degradation of p53. J Biol Chem 2002; 277: 21843-21850.
38. Zhou BB, Elledge SJ. The DNA damage response: putting checkpoints in perspective. Nature 2000; 408: 433-439.
39. Li HH, Li AG, Sheppard HM, Liu X. Phosphorylation on Thr-55 by TAF1 mediates degradation of p53: a role for TAF1 in cell G1 progression. Mol Cell 2004; 13: 867-878.
40. Oda K, Arakawa H, Tanaka T, Matsuda K, Tanikawa C, Mori T et al. p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46- phosphorylated p53. Cell 2000; 102: 849-862.
41. Wade M, Wang YV, Wahl GM. The p53 orchestra: Mdm2 and Mdmx set the tone. Trends Cell Biol 2010; 20: 299-309.
42. Volonte D, Caveolin-1 Galbiati F. cellular senescence and pulmonary emphysema. Aging (Albany NY) 2009; 1: 831-835.
43. Li L, Ren CH, Tahir SA, Ren C, Thompson TC. Caveolin-1 maintains activated Akt in prostate cancer cells through scaffolding domain binding site interactions with and inhibition of serine/threonine protein phosphatases PP1 and PP2A. Mol Cell Biol 2003; 23: 9389-9404.
44. Fresno Vara JA, Casado E, de Castro J, Cejas P, Belda-Iniesta C, Gonzalez-Baron M. PI3K/Akt signalling pathway and cancer. Cancer Treat Rev 2004; 30: 193-204.
45. Jadersten M, Saft L, Smith A, Kulasekararaj A, Pomplun S, Gohring G et al. TP53 mutations in low-risk myelodysplastic syndromes with del(5q) predict disease progression. J Clin Oncol 2011; 29: 1971-1979.
46. Ito T, Ando H, Suzuki T, Ogura T, Hotta K, Imamura Y et al. Identification of a primary target of thalidomide teratogenicity. Science 2010; 327: 1345-1350.
47. Whelan JA, Russell NB, Whelan MA. A method for the absolute quantification of cDNA using real-time PCR. J Immunol Methods 2003; 278: 261-269.
48. Yokobori T, Mimori K, Iwatsuki M, Ishii H, Onoyama I, Fukagawa T et al. p53- Altered FBXW7 expression determines poor prognosis in gastric cancer cases. Cancer Res 2009; 69: 3788-3794.