Reduced ribosomal protein gene dosage and p53 activation in low-risk myelodysplastic syndrome

Blood

Volumn 118, Issue 13, 2011, Pages 3622-3633

  McGowan, Kelly A ^a   Pang, Wendy W ^b   Bhardwaj, Rashmi ^c   Perez, Marcelina G ^a   Pluvinage, John V ^b   Glader, Bertil E ^a   Malek, Reem ^d   Mendrysa, Susan M ^d   Weissman, Irving L ^b   Park, Christopher Y ^b,c   Barsh, Gregory S ^a,e,f  

^a STANFORD UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d PURDUE UNIVERSITY   (United States)

^e HUDSONALPHA INSTITUTE FOR BIOTECHNOLOGY   (United States)

^f STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLUOROURACIL; PROTEIN MDM2; PROTEIN P53; PROTEIN S6; PROTEIN TRP53; RIBOSOME PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD CELL; BLOOD CELL COUNT; BLOOD DISEASE; CELL MATURATION; CHROMOSOME 5Q; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG EFFECT; ERYTHROID HYPOPLASIA; GENE CONTROL; GENE DOSAGE; HEMATOPOIESIS; HEMIZYGOSITY; HUMAN; HUMAN CELL; MACROCYTIC ANEMIA; MEGAKARYOCYTIC DYSPLASIA; MOUSE; MUTATIONAL ANALYSIS; MYELODYSPLASTIC SYNDROME; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; RISK ASSESSMENT; THROMBOCYTOSIS;

EID: 80053358313     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-11-318584     Document Type: Article

References (46)

1. Olney HJ, Le Beau MM. The cytogenetics of myelodysplastic syndromes. Best Pract Res Clin Haematol. 2001;14(3):479-495. (Pubitemid 33019747)
2. 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.
3. Pellagatti A, Cazzola M, Giagounidis A, et al. Deregulated gene expression pathways in myelodysplastic syndrome hematopoietic stem cells. Leukemia. 2010;24(4):756-764.
4. 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)
5. Lipton JM, Ellis SR. Diamond Blackfan anemia 2008-2009: broadening the scope of ribosome biogenesis disorders. Curr Opin Pediatr. 2010;22(1):12-19.
6. Starczynowski DT, Kuchenbauer F, Argiropoulos B, et al. Identification of miR-145 and miR-146a as mediators of the 5q- syndrome phenotype. Nat Med. 2010;16(1):49-58.
7. 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.
8. Lambertsson A. The minute genes in Drosophila and their molecular functions. Adv Genet. 1998;38:69-134.
9. Léger-Silvestre I, Caffrey JM, Dawaliby R, et al. Specific role for yeast homologs of the Diamond Blackfan anemia-associated Rps19 protein in ribosome synthesis. J Biol Chem. 2005;280(46):38177-38185. (Pubitemid 43853712)
10. Matsson H, Davey EJ, Draptchinskaia N, et al. Targeted disruption of the ribosomal protein S19 gene is lethal prior to implantation. Mol Cell Biol. 2004;24(9):4032-4037. (Pubitemid 38496179)
11. 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. (Pubitemid 39232151)
12. Volarevic S, Stewart MJ, Ledermann B, et al. Proliferation, but not growth, blocked by conditional deletion of 40S ribosomal protein S6. Science. 2000;288(5473):2045-2047. (Pubitemid 30397685)
13. Weijers D, Franke-van Dijk M, Vencken RJ, Quint A, Hooykaas P, Offringa R. An Arabidopsis Minute-like phenotype caused by a semi-dominant mutation in a ribosomal protein S5 gene. Development. 2001;128(21):4289-4299. (Pubitemid 33077039)
14. Morata G, Ripoll P. Minutes: mutants of drosophila autonomously affecting cell division rate. Dev Biol. 1975;42(2):211-221.
15. Fitch KR, McGowan KA, van Raamsdonk CD, et al. Genetics of dark skin in mice. Genes Dev. 2003;17(2):214-228. (Pubitemid 36105894)
16. 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.
17. Ramirez A, Page A, Gandarillas A, et al. A keratin K5Cre transgenic line appropriate for tissue-specific or generalized Cre-mediated recombination. Genesis. 2004;39(1):52-57. (Pubitemid 38738016)
18. Jacks T, Remington L, Williams BO, et al. Tumor spectrum analysis in p53-mutant mice. Curr Biol. 1994;4(1):1-7.
19. Hrabé de Angelis MH, Flaswinkel H, Fuchs H, et al. Genome-wide, large-scale production of mutant mice by ENU mutagenesis. Nat Genet. 2000;25(4):444-447. (Pubitemid 32983440)
20. Glader BE, Backer K, Diamond LK. Elevated erythrocyte adenosine deaminase activity in congenital hypoplastic anemia. N Engl J Med. 1983;309(24):1486- 1490. (Pubitemid 14208425)
21. Pronk CJ, Rossi DJ, Mansson R, et al. Elucidation of the phenotypic, functional, and molecular topography of a myeloerythroid progenitor cell hierarchy. Cell Stem Cell. 2007;1(4):428-442. (Pubitemid 47506534)
22. Socolovsky M, Nam H, Fleming MD, Haase VH, Brugnara C, Lodish HF. Ineffective erythropoiesis in Stat5a(-/-)5b(-/-) mice due to decreased survival of early erythroblasts. Blood. 2001;98(12):3261-3273.
23. Karlsson G, Blank U, Moody JL, et al. Smad4 is critical for self-renewal of hematopoietic stem cells. J Exp Med. 2007;204(3):467-474. (Pubitemid 46457070)
24. Chuang SS, Jung YC, Li CY. von Willebrand factor is the most reliable immunohistochemical marker for megakaryocytes of myelodysplastic syndrome and chronic myeloproliferative disorders. Am J Clin Pathol. 2000;113(4):506-511.
25. Vardiman JW, Harris NL, Brunning RD. The World Health Organization (WHO) classification of the myeloid neoplasms. Blood. 2002;100(7):2292-2302.
26. Mendrysa SM, McElwee MK, Michalowski J, O'Leary KA, Young KM, Perry ME. mdm2 Is critical for inhibition of p53 during lymphopoiesis and the response to ionizing irradiation. Mol Cell Biol. 2003;23(2):462-472.
27. Bunz F, Hwang PM, Torrance C, et al. Disruption of p53 in human cancer cells alters the responses to therapeutic agents. J Clin Invest. 1999;104(3):263-269.
28. Agosti V, Karur V, Sathyanarayana P, Besmer P, Wojchowski DM. A KIT juxtamembrane PY567-directed pathway provides nonredundant signals for erythroid progenitor cell development and stress erythropoiesis. Exp Hematol. 2009;37(2):159-171.
29. Majeti R, Park CY, Weissman IL. Identification of a hierarchy of multipotent hematopoietic progenitors in human cord blood. Cell Stem Cell. 2007;1(6):635-645. (Pubitemid 350215330)
30. Greenberg P, Cox C, LeBeau MM, et al. International scoring system for evaluating prognosis in myelodysplastic syndromes. Blood. 1997;89(6):2079-2088. (Pubitemid 27132124)
31. 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. 2009;16(1):59-66.
32. Panić L, Tamarut S, Sticker-Jantscheff M, et al. Ribosomal protein S6 gene haploinsufficiency is associated with activation of a p53-dependent checkpoint during gastrulation. Mol Cell Biol. 2006;26(23):8880-8891. (Pubitemid 44851946)
33. Dutt S, Narla A, Lin K, et al. Haploinsufficiency for ribosomal protein genes causes selective activation of p53 in human erythroid progenitor cells. Blood. 2011;117(9):2567-2576.
34. Fiskum G, Rosenthal RE, Vereczki V, et al. Protection against ischemic brain injury by inhibition of mitochondrial oxidative stress. J Bioenerg Biomembr. 2004;36(4):347-352. (Pubitemid 39619839)
35. Matsusaka H, Ide T, Matsushima S, et al. Targeted deletion of p53 prevents cardiac rupture after myocardial infarction in mice. Cardiovasc Res. 2006;70(3):457-465.
36. Jones NC, Lynn ML, Gaudenz K, et al. Prevention of the neurocristopathy Treacher Collins syndrome through inhibition of p53 function. Nat Med. 2008;14(2):125-133. (Pubitemid 351214559)
37. Liu TX, Howlett NG, Deng M, et al. Knockdown of zebrafish Fancd2 causes developmental abnormalities via p53-dependent apoptosis. Dev Cell. 2003;5(6):903-914. (Pubitemid 37527690)
38. Vousden KH, Lane DP. p53 in health and disease. Nat Rev Mol Cell Biol. 2007;8(4):275-283. (Pubitemid 46474662)
39. Gazda HT, Kho AT, Sanoudou D, et al. Defective ribosomal protein gene expression alters transcription, translation, apoptosis, and oncogenic pathways in Diamond-Blackfan anemia. Stem Cells. 2006;24(9):2034-2044. (Pubitemid 44477128)
40. Miyake K, Utsugisawa T, Flygare J, et al. Ribosomal protein S19 deficiency leads to reduced proliferation and increased apoptosis but does not affect terminal erythroid differentiation in a cell line model of Diamond-Blackfan anemia. Stem Cells. 2008;26(2):323-329. (Pubitemid 351413591)
41. Passegué E, Wagers AJ, Giuriato S, Anderson WC, Weissman IL. Global analysis of proliferation and cell cycle gene expression in the regulation of hematopoietic stem and progenitor cell fates. J Exp Med. 2005;202(11):1599-1611. (Pubitemid 41746605)
42. Adolfsson J, Mansson R, Buza-Vidas N, et al. Identification of Flt3+ lympho-myeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell. 2005;121(2):295-306. (Pubitemid 40546396)
43. Pellagatti A, Hellstrom-Lindberg E, Giagounidis A, et al. Haploinsufficiency of RPS14 in 5q- syndrome is associated with deregulation of ribosomal- and translation-related genes. Br J Haematol. 2008;142(1):57-64. (Pubitemid 351783162)
44. Sridhar K, Ross DT, Tibshirani R, Butte AJ, Greenberg PL. Relationship of differential gene expression profiles in CD34+ myelodysplastic syndrome marrow cells to disease subtype and progression. Blood. 2009;114(23):4847-4858.
45. Boultwood J, Pellagatti A, Cattan H, et al. Gene expression profiling of CD34+ cells in patients with the 5q- syndrome. Br J Haematol. 2007; 139(4):578-589. (Pubitemid 350043812)
46. Zaghloul NA, Katsanis N. Mechanistic insights into Bardet-Biedl syndrome, a model ciliopathy. J Clin Invest. 2009;119(3):428-437.