Loss of p53 Ser18 and Atm results in embryonic lethality without cooperation in tumorigenesis

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Armata, Heather L ^a   Shroff, Punita ^a   Garlick, David E ^a   Penta, Krista ^a   Tapper, Andrew R ^a   Sluss, Hayla K ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; MUTANT PROTEIN; PHOSPHOTRANSFERASE; SERINE; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; PROTEIN P53; PROTEIN SERINE THREONINE KINASE; TUMOR SUPPRESSOR PROTEIN;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATAXIA TELANGIECTASIA MUTATED GENE; CANCER INHIBITION; CANCER SURVIVAL; CARCINOGENESIS; CONTROLLED STUDY; EMBRYO DEATH; GENE; GENE INTERACTION; GENE LOSS; GENE MUTATION; HOMOZYGOTE; IN VIVO STUDY; LIFESPAN; MOTOR COORDINATION; MOUSE; NONHUMAN; OBSERVATIONAL STUDY; P53SER18 GENE; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; TUMOR SUPPRESSOR GENE; ANIMAL; BIOLOGICAL MODEL; CELL PROLIFERATION; CYTOLOGY; FEMALE; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MALE; MUTATION; PHOSPHORYLATION; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALIA; ATAXIA TELANGIECTASIA; MURINAE; MUS;

ANIMALS; CELL CYCLE PROTEINS; CELL PROLIFERATION; DNA-BINDING PROTEINS; FEMALE; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; GERM-LINE MUTATION; HUMANS; MALE; MICE; MICE, TRANSGENIC; MODELS, GENETIC; MUTATION; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 80053178281     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024813     Document Type: Article

References (40)

1. Taylor AM, Byrd PJ, (2005) Molecular pathology of ataxia telangiectasia. J Clin Pathol 58: 1009-1015.
2. Taylor AM, Metcalfe JA, Thick J, Mak YF, (1996) Leukemia and lymphoma in ataxia telangiectasia. Blood 87: 423-443 428.
3. Vorechovsky I, Luo L, Dyer MJ, Catovsky D, Amlot PL, et al. (1997) Clustering of missense mutations in the ataxia-telangiectasia gene in a sporadic T-cell leukaemia. Nat Genet 17: 96-99.
4. Stilgenbauer S, Schaffner C, Litterst A, Liebisch P, Gilad S, et al. (1997) Biallelic mutations in the ATM gene in T-prolymphocytic leukemia. Nat Med 3: 1155-1159.
5. Stoppa-Lyonnet D, Soulier J, Lauge A, Dastot H, Garand R, et al. (1998) Inactivation of the ATM gene in T-cell prolymphocytic leukemias. Blood 91: 3920-3926.
6. Stankovic T, Stewart GS, Byrd P, Fegan C, Moss PA, et al. (2002) ATM mutations in sporadic lymphoid tumours. Leuk Lymphoma 43: 1563-1571.
7. Bullrich F, Rasio D, Kitada S, Starostik P, Kipps T, et al. (1999) ATM mutations in B-cell chronic lymphocytic leukemia. Cancer Res 59: 24-27.
8. Schaffner C, Stilgenbauer S, Rappold GA, Dohner H, Lichter P, (1999) Somatic ATM mutations indicate a pathogenic role of ATM in B-cell chronic lymphocytic leukemia. Blood 94: 748-753.
9. Schaffner C, Idler I, Stilgenbauer S, Dohner H, Lichter P, (2000) Mantle cell lymphoma is characterized by inactivation of the ATM gene. Proc Natl Acad Sci U S A 97: 2773-2778.
10. Stankovic T, Kidd AM, Sutcliffe A, McGuire GM, Robinson P, et al. (1998) ATM mutations and phenotypes in ataxia-telangiectasia families in the British Isles: expression of mutant ATM and the risk of leukemia, lymphoma, and breast cancer. Am J Hum Genet 62: 334-345.
11. Swift M, Reitnauer PJ, Morrell D, Chase CL, (1987) Breast and other cancers in families with ataxia-telangiectasia. N Engl J Med 316: 1289-1294.
12. Xu Y, Baltimore D, (1996) Dual roles of ATM in the cellular response to radiation and in cell growth control. Genes Dev 10: 2401-2410.
13. Xu Y, Ashley T, Brainerd EE, Bronson RT, Meyn MS, et al. (1996) Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev 10: 2411-2422.
14. Elson A, Wang Y, Daugherty CJ, Morton CC, Zhou F, et al. (1996) Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc Natl Acad Sci U S A 93: 13084-13089.
15. Barlow C, Hirotsune S, Paylor R, Liyanage M, Eckhaus M, et al. (1996) Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86: 159-171.
16. Kuljis RO, Xu Y, Aguila MC, Baltimore D, (1997) Degeneration of neurons, synapses, and neuropil and glial activation in a murine Atm knockout model of ataxia-telangiectasia. Proc Natl Acad Sci U S A 94: 12688-12693.
17. Borghesani PR, Alt FW, Bottaro A, Davidson L, Aksoy S, et al. (2000) Abnormal development of Purkinje cells and lymphocytes in Atm mutant mice. Proc Natl Acad Sci U S A 97: 3336-3341.
18. Wong KK, Maser RS, Bachoo RM, Menon J, Carrasco DR, et al. (2003) Telomere dysfunction and Atm deficiency compromises organ homeostasis and accelerates ageing. Nature 421: 643-648.
19. Spring K, Cross S, Li C, Watters D, Ben-Senior L, et al. (2001) Atm knock-in mice harboring an in-frame deletion corresponding to the human ATM 7636del9 common mutation exhibit a variant phenotype. Cancer Res 61: 4561-4568.
20. O'Driscoll M, Jeggo PA, (2006) The role of double-strand break repair- insights from human genetics. Nat Rev Genet 7: 45-54.
21. Lombard DB, Chua KF, Mostoslavsky R, Franco S, Gostissa M, et al. (2005) DNA repair, genome stability, and aging. Cell 120: 497-512.
22. Harper JW, Elledge SJ, (2007) The DNA damage response: ten years after. Mol Cell 28: 739-745.
23. Appella E, Anderson CW, (2001) Post-translational modifications and activation of p53 by genotoxic stresses. Eur J Biochem 268: 2764-2772.
24. Giaccia AJ, Kastan MB, (1998) The complexity of p53 modulation: emerging patterns from divergent signals. Genes Dev 12: 2973-2983.
25. Sluss HK, Armata H, Gallant J, Jones SN, (2004) Phosphorylation of serine 18 regulates distinct p53 functions in mice. Mol Cell Biol 24: 976-984.
26. Armata HL, Garlick DS, Jones SN, Sluss HK, (2007) The ataxia telangiectasia-mutated target site Ser18 is required for p53-mediated tumor suppression. Cancer Res 67: 11696-11703.
27. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CA Jr, et al. (1992) Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356: 215-221.
28. Xu Y, Yang EM, Brugarolas J, Jacks T, Baltimore D, (1998) Involvement of p53 and p21 in cellular defects and tumorigenesis in Atm-/- mice. Mol Cell Biol 18: 4385-4390.
29. Jacks T, Remington L, Williams BO, Schmitt EM, Halachmi S, et al. (1994) Tumor spectrum analysis in p53-mutant mice. Curr Biol 4: 1-7.
30. Reliene R, Schiestl RH, (2007) Antioxidants suppress lymphoma and increase longevity in Atm-deficient mice. J Nutr 137: 229S-232S.
31. Chao C, Hergenhahn M, Kaeser MD, Wu Z, Saito S, et al. (2003) Cell type- and promoter-specific roles of Ser18 phosphorylation in regulating p53 responses. J Biological Chem in press.
32. Bailey SL, Gurley KE, Hoon-Kim K, Kelly-Spratt KS, Kemp CJ, (2008) Tumor suppression by p53 in the absence of Atm. Mol Cancer Res 6: 1185-1192.
33. Armata HL, Golebiowski D, Jung DY, Ko HJ, Kim JK, et al. (2010) Requirement of the ATM/p53 tumor suppressor pathway for glucose homeostasis. Mol Cell Biol 30: 5787-5794.
34. Sluss HK, Gannon H, Coles AH, Shen Q, Eischen CM, et al. (2010) Phosphorylation of p53 serine 18 upregulates apoptosis to suppress Myc-induced tumorigenesis. Mol Cancer Res 8: 216-222.
35. Spring K, Ahangari F, Scott SP, Waring P, Purdie DM, et al. (2002) Mice heterozygous for mutation in Atm, the gene involved in ataxia-telangiectasia, have heightened susceptibility to cancer. nature genetics 32: 185-190.
36. Barlow C, Eckhaus M, Schaffer A, Wynshaw-Boris A, (1999) Atm haploinsufficiency results in inreased sensitivity to sublethal doses of ionizing radiation in mice. Nature 4: 359-360.
37. Smilenov LB, Brenner DJ, Hall EJ, (2001) Modest increased sensitivity to radiation oncogenesis in ATM heterozygous versus wild-type mammalian cells. Cancer Res 61: 5710-5713.
38. Worgul BV, Smilenov L, Brenner DJ, Junk A, Zhou W, et al. (2002) Atm heterozygous mice are more sensitive to radiation-induced cataracts than are their wild-type counterparts. Proc Natl Acad Sci U S A 99: 9836-9839.
39. Mao JH, Wu D, DelRosario R, Castellanos A, Balmain A, et al. (2008) Atm heterozygosity does not increase tumor susceptibility to ionizing radiation alone or in a p53 heterozygous background. Oncogene 27: 6596-6600.
40. Thompson D, Duedal S, Kirner J, McGuffog L, Last J, et al. (2005) Cancer risks and mortality in heterozygous ATM mutation carriers. J Natl Cancer Inst 97: 813-822.