Haploinsufficiency for ribosomal protein genes causes selective activation of p53 in human erythroid progenitor cells

Blood

Volumn 117, Issue 9, 2011, Pages 2567-2576

  Dutt, Shilpee ^a   Narla, Anupama ^a,b,c   Lin, Katherine ^a   Mullally, Ann ^a   Abayasekara, Nirmalee ^a   Megerdichian, Christine ^a   Wilson, Frederick H ^a   Currie, Treeve ^a   Khanna Gupta, Arati ^a   Berliner, Nancy ^a   Kutok, Jeffery L ^a   Ebert, Benjamin L ^a,b,d  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEAR PROTEIN; NUTLIN 3; PIFITHRIN ALPHA; PROTEIN MDM2; PROTEIN P21; PROTEIN P53; RIBOSOME PROEIN S14; RIBOSOME PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

5Q- SYNDROME; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLACKFAN DIAMOND ANEMIA; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL LINEAGE; CONTROLLED STUDY; DRUG INHIBITION; ERYTHROID PRECURSOR CELL; ERYTHROPOIESIS; GENE ACTIVATION; GENE DELETION; GENE EXPRESSION; GENE MUTATION; HAPLOTYPE; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION;

EID: 79953117045     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-07-295238     Document Type: Article

References (42)

1. Draptchinskaia N, Gustavsson P, Andersson B, et al. The gene encoding ribosomal protein S19 is mutated in Diamond-Blackfan anaemia. Nat Genet. 1999;21(2):169-175. (Pubitemid 29070361)
2. Lipton JM, Ellis SR. Diamond-Blackfan anemia: diagnosis, treatment, and molecular pathogenesis. Hematol Oncol Clin North Am. 2009;23(2): 261-282.
3. Narla A, Ebert BL. Ribosomopathies: human disorders of ribosome dysfunction. Blood. 2010; 115(16):3196-3205.
4. Ebert BL. Deletion 5q in myelodysplastic syndrome: a paradigm for the study of hemizygous deletions in cancer. Leukemia. 2009;23(7):1252-1256.
5. Ebert BL, Pretz J, Bosco J, et al. Identification of RPS14 as a 5q- syndrome gene by RNA interference screen. Nature. 2008;451(7176):335-339.
6. Vardiman JW, Harris NL, Brunning RD. The World Health Organization (WHO) classification of the myeloid neoplasms. Blood. 2002;100(7): 2292-2302.
7. Lipton JM, Ellis SR. Diamond Blackfan anemia 2008-2009: broadening the scope of ribosome biogenesis disorders. Curr Opin Pediatr. 2010; 22(1):12-19.
8. Zhang Y, Lu H. Signaling to p53: ribosomal proteins find their way. Cancer Cell. 2009;16(5):369-377.
9. 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.
10. McGowan KA, Li JZ, Park CY, et al. Ribosomal mutations cause p53-mediated dark skin and pleiotropic effects. Nat Genet. 2008;40(8):963-970.
11. Barlow JL, Drynan LF, Hewett DR, et al. A p53-dependent mechanism underlies macrocytic anemia in a mouse model of human 5q- syndrome. Nat Med. 2010;16(1):59-66.
12. Moffat J, Grueneberg DA, Yang X, et al. A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell. 2006;124(6):1283-1298.
13. Subramanian A, Tamayo P, Mootha VK, et al. Gene set enrichment analysis: a knowledgebased approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005;102(43):15545-15550. (Pubitemid 41528093)
14. Reich M, Liefeld T, Gould J, Lerner J, Tamayo P, Mesirov JP. GenePattern 2.0. Nat Genet. 2006; 38(5):500-501.
15. Sieff CA, Yang J, Merida-Long LB, Lodish HF. Pathogenesis of the erythroid failure in Diamond Blackfan anaemia. Br J Haematol. 2010;148(4): 611-622.
16. Kannan K, Amariglio N, Rechavi G, et al. DNA microarrays identification of primary and secondary target genes regulated by p53. Oncogene. 2001;20(18):2225-2234. (Pubitemid 32531280)
17. Giagounidis AA, Germing U, Aul C. Biological and prognostic significance of chromosome 5q deletions in myeloid malignancies. Clin Cancer Res. 2006;12(1):5-10. (Pubitemid 43166169)
18. Diamond LK, Wang WC, Alter BP. Congenital hypoplastic anemia. Adv Pediatr. 1976;22:349-378.
19. 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. (Pubitemid 37463250)
20. 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. (Pubitemid 36808652)
21. Fumagalli S, Di Cara A, Neb-Gulati A, 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(4):501-508.
22. Zhang Y, Wolf GW, Bhat K, et al. Ribosomal protein L11 negatively regulates oncoprotein MDM2 and mediates a p53-dependent ribosomal-stress checkpoint pathway. Mol Cell Biol. 2003;23(23): 8902-8912. (Pubitemid 37433388)
23. Gilkes DM, Chen J. Distinct roles of MDMX in the regulation of p53 response to ribosomal stress. Cell Cycle. 2007;6(2):151-155. (Pubitemid 46232494)
24. Lindstrom MS, Deisenroth C, Zhang Y. Putting a finger on growth surveillance: insight into MDM2 zinc finger-ribosomal protein interactions. Cell Cycle. 2007;6(4):434-437. (Pubitemid 46393446)
25. Shangary S, Wang S. Small-molecule inhibitors of the MDM2-p53 protein-protein interaction to reactivate p53 function: a novel approach for cancer therapy. Annu Rev Pharmacol Toxicol. 2009; 49:223-241.
26. Lau LM, Nugent JK, Zhao X, Irwin MS. HDM2 antagonist Nutlin-3 disrupts p73-HDM2 binding and enhances p73 function. Oncogene. 2008; 27(7):997-1003.
27. Komarov PG, Komarova EA, Kondratov RV, et al. A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science. 1999;285(5434):1733-1737. (Pubitemid 29428873)
28. Komarova EA, Neznanov N, Komarov PG, Chernov MV, Wang K, Gudkov AV. p53 inhibitor pifithrin alpha can suppress heat shock and glucocorticoid signaling pathways. J Biol Chem. 2003;278(18):15465-15468. (Pubitemid 36799652)
29. Davidson W, Ren Q, Kari G, Kashi O, Dicker AP, Rodeck U. Inhibition of p73 function by Pifithrinalpha as revealed by studies in zebrafish embryos. Cell Cycle. 2008;7(9):1224-1230. (Pubitemid 351749276)
30. Ganapathi KA, Shimamura A. Ribosomal dysfunction and inherited marrow failure. Br J Haematol. 2008;141(3):376-387. (Pubitemid 351521153)
31. Liu JM, Ellis SR. Ribosomes and marrow failure: coincidental association or molecular paradigm? Blood. 2006;107(12):4583-4588.
32. Pellagatti A, Marafioti T, Paterson JC, et al. Induction of p53 and up-regulation of the p53 pathway in the human 5q- syndrome. Blood. 2010; 115(13):2721-2723.
33. Diamond LK, Allen DM, Magill FB. Congenital (erythroid) hypoplastic anemia: a 25-year study. Am J Dis Child. 1961;102:403-415.
34. Peller S, Frenkel J, Lapidot T, et al. The onset of p53-dependent apoptosis plays a role in terminal differentiation of human normoblasts. Oncogene. 2003;22(30):4648-4655. (Pubitemid 36976439)
35. Lajtha LG, Oliver R. A kinetic model of the erythron. Proc R Soc Med. 1961;54:369-371.
36. 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. (Pubitemid 41798121)
37. Kasyan A, Medeiros LJ, Zuo Z, et al. Acute erythroid leukemia as defined in the World Health Organization classification is a rare and pathogenetically heterogeneous disease. Mod Pathol. 2010;134:1261-1270.
38. Hasserjian RP, Zuo Z, Garcia C, et al. Acute erythroid leukemia: a reassessment using criteria refined in the 2008 WHO classification. Blood. 2010;115(10):1985-1992.
39. Meek DW. Tumour suppression by p53: a role for the DNA damage response? Nat Rev Cancer. 2009;9(10):714-723.
40. Negrini S, Gorgoulis VG, Halazonetis TD. Genomic instability: an evolving hallmark of cancer. Nat Rev Mol Cell Biol. 2010;11(3):220-228.
41. Bellodi C, Kopmar N, Ruggero D. Deregulation of oncogene-induced senescence and p53 translational control in X-linked dyskeratosis congenita. EMBO J. 2010;29(11):1865-1876.
42. Kennedy RD, D'Andrea AD. The Fanconi Anemia/ BRCA pathway: new faces in the crowd. Genes Dev. 2005;19(24):2925-2940. (Pubitemid 41798109)