Absence of p53-dependent apoptosis combined with nonhomologous end-joining deficiency leads to a severe diabetic phenotype in mice

Diabetes

Volumn 59, Issue 1, 2010, Pages 135-142

  Tavana, Omid ^a,b   Puebla Osorio, Nahum ^a   Sang, Mei ^a   Zhu, Chengming ^a,b  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P21; PROTEIN P53; DNA BINDING PROTEIN; INSULIN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE (ATP); XRCC4 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL AGING; CELL PROLIFERATION; CONTROLLED STUDY; DIABETES MELLITUS; DIABETOGENESIS; DISEASE SEVERITY; DNA DAMAGE; DNA REPAIR; GLUCOSE INTOLERANCE; INNATE IMMUNITY; INSULIN RELEASE; MOUSE; NONHOMOLOGOUS END JOINING; NONHUMAN; PANCREAS ISLET CELL FUNCTION; PHENOTYPE; PRIORITY JOURNAL; ANIMAL; BLOOD; C57BL MOUSE; EXPERIMENTAL DIABETES MELLITUS; GENETICS; GLUCOSE BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; METABOLISM; MOUSE STRAIN; PANCREAS; PANCREAS ISLET; PATHOLOGY; SECRETION;

ANIMALS; BLOOD GLUCOSE; CELL AGING; DIABETES MELLITUS, EXPERIMENTAL; DNA DAMAGE; DNA LIGASES; DNA-BINDING PROTEINS; GLUCOSE INTOLERANCE; IMMUNITY, INNATE; IMMUNOHISTOCHEMISTRY; INSULIN; ISLETS OF LANGERHANS; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; PANCREAS; PHENOTYPE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 77449137837     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db09-0792     Document Type: Article

References (43)

1. Mahaney BL, Meek K, Lees-Miller SP. Repair of ionizing radiation-induced DNA double-strand breaks by non-homologous end-joining. Biochem J 2009;417:639-650
2. Huang Y, Giblin W, Kubec M, Westfield G, St Charles J, Chadde L, Kraftson S, Sekiguchi J. Impact of a hypomorphic Artemis disease allele on lymphocyte development, DNA end processing, and genome stability. J Exp Med 2009;206:893-908
3. Mills KD, Ferguson DO, Essers J, Eckersdorff M, Kanaar R, Alt FW. Rad54 and DNA Ligase IV cooperate to maintain mammalian chromatid stability. Genes Dev 2004;18:1283-1292
4. Li G, Alt FW, Cheng HL, Brush JW, Goff PH, Murphy MM, Franco S, Zhang Y, Zha S. Lymphocyte-specific compensation for XLF/cernunnos end-joining functions in V(D)J recombination. Mol Cell 2008;31:631-640
5. Puebla-Osorio N, Zhu C. DNA damage and repair during lymphoid development: antigen receptor diversity, genomic integrity and lymphomagenesis. Immunol Res 2008;41:103-122
6. Frank KM, Sharpless NE, Gao Y, Sekiguchi JM, Ferguson DO, Zhu C, Manis JP, Horner J, DePinho RA, Alt FW. DNA ligase IV deficiency in mice leads to defective neurogenesis and embryonic lethality via the p53 pathway. Mol Cell 2000;5:993-1002
7. Gao Y, Sun Y, Frank KM, Dikkes P, Fujiwara Y, Seidl KJ, Sekiguchi JM, Rathbun GA, Swat W, Wang J, Bronson RT, Malynn BA, Bryans M, Zhu C, Chaudhuri J, Davidson L, Ferrini R, Stamato T, Orkin SH, Greenberg ME, Alt FW. A critical role for DNA end-joining proteins in both lymphogenesis and neurogenesis. Cell 1998;95:891-902
8. Frank KM, Sekiguchi JM, Seidl KJ, Swat W, Rathbun GA, Cheng HL, Davidson L, Kangaloo L, Alt FW. Late embryonic lethality and impaired V(D)J recombination in mice lacking DNA ligase IV. Nature 1998;396:173-177
9. Gao Y, Ferguson DO, Xie W, Manis JP, Sekiguchi J, Frank KM, Chaudhuri J, Horner J, DePinho RA, Alt FW. Interplay of p53 and DNA-repair protein XRCC4 in tumorigenesis, genomic stability and development. Nature 2000;404:897-900
10. Zhu C, Mills KD, Ferguson DO, Lee C, Manis J, Fleming J, Gao Y, Morton CC, Alt FW. Unrepaired DNA breaks in p53-deficient cells lead to oncogenic gene amplification subsequent to translocations. Cell 2002;109:811-821
11. Liu G, Parant JM, Lang G, Chau P, Chavez-Reyes A, El-Naggar AK, Multani A, Chang S, Lozano G. Chromosome stability, in the absence of apoptosis, is critical for suppression of tumorigenesis in Trp53 mutant mice. Nat Genet 2004;36:63-68
12. Van Nguyen T, Puebla-Osorio N, Pang H, Dujka ME, Zhu C. DNA damage-induced cellular senescence is sufficient to suppress tumorigenesis: a mouse model. J Exp Med 2007;204:1453-1461
13. d'Adda di Fagagna F. Living on a break: cellular senescence as a DNAdamage response. Nat Rev Cancer 2008;8:512-522
14. Ackermann AM, Gannon M. Molecular regulation of pancreatic beta-cell mass development, maintenance, and expansion. J Mol Endocrinol 2007; 38:193-206
15. Lee YC, Nielsen JH. Regulation of beta cell replication. Mol Cell Endocrinol 2009;297:18-27
16. Meijer AJ, Codogno P. Autophagy: a sweet process in diabetes. Cell Metab 2008;8:275-276
17. Dor Y, Brown J, Martinez OI, Melton DA. Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 2004;429:41-46
18. Georgia S, Bhushan A. Beta cell replication is the primary mechanism for maintaining postnatal beta cell mass. J Clin Invest 2004;114:963-968
19. Yesil P, Lammert E. Islet dynamics: a glimpse at beta cell proliferation. Histol Histopathol 2008;23:883-895
20. Teta M, Rankin MM, Long SY, Stein GM, Kushner JA. Growth and regeneration of adult beta cells does not involve specialized progenitors. Dev Cell 2007;12:817-826
21. Halvorsen TL, Beattie GM, Lopez AD, Hayek A, Levine F. Accelerated telomere shortening and senescence in human pancreatic islet cells stimulated to divide in vitro. J Endocrinol 2000;166:103-109
22. Sone H, Kagawa Y. Pancreatic beta cell senescence contributes to the pathogenesis of type 2 diabetes in high-fat diet-induced diabetic mice. Diabetologia 2005;48:58-67
23. Kukreja A, Maclaren NK. Autoimmunity and diabetes. J Clin Endocrinol Metab 1999;84:4371-4378
24. DeFronzo RA. Insulin resistance: a multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidaemia and atherosclerosis. Neth J Med 1997;50:191-197
25. Karaca M, Magnan C, Kargar C. Functional pancreatic beta-cell mass: involvement in type 2 diabetes and therapeutic intervention. Diabete Metab 2009;35:77-84
26. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 2003;52:102-110
27. Scaglia L, Cahill CJ, Finegood DT, Bonner-Weir S. Apoptosis participates in the remodeling of the endocrine pancreas in the neonatal rat. Endocrinology 1997;138:1736-1741
28. Nam SY, Lee MK, Sabapathy K. The tumour-suppressor p53 is not required for pancreatic beta cell death during diabetes and upon irradiation. J Physiol 2008;586:407-417
29. Lenzen S. Oxidative stress: the vulnerable beta-cell. Biochem Soc Trans 2008;36:343-347
30. Wei YF, Robins P, Carter K, Caldecott K, Pappin DJ, Yu GL, Wang RP, Shell BK, Nash RA, Schär P. Molecular cloning and expression of human cDNAs encoding a novel DNA ligase IV and DNA ligase III, an enzyme active in DNA repair and recombination. Mol Cell Biol 1995;15:3206-3216
31. Masiello P. Animal models of type 2 diabetes with reduced pancreatic beta-cell mass. Int J Biochem Cell Biol 2006;38:873-893
32. Rane SG, Dubus P, Mettus RV, Galbreath EJ, Boden G, Reddy EP, Barbacid M. Loss of Cdk4 expression causes insulin-deficient diabetes and Cdk4 activation results in beta-islet cell hyperplasia. Nat Genet 1999;22:44-52
33. Tsutsui T, Hesabi B, Moons DS, Pandolfi PP, Hansel KS, Koff A, Kiyokawa H. Targeted disruption of CDK4 delays cell cycle entry with enhanced p27(Kip1) activity. Mol Cell Biol 1999;19:7011-7019
34. Kushner JA, Ciemerych MA, Sicinska E, Wartschow LM, Teta M, Long SY, Sicinski P, White MF. Cyclins D2 and D1 are essential for postnatal pancreatic beta-cell growth. Mol Cell Biol 2005;25:3752-3762
35. Zhang X, Gaspard JP, Mizukami Y, Li J, Graeme-Cook F, Chung DC. Overexpression of cyclin D1 in pancreatic beta-cells in vivo results in islet hyperplasia without hypoglycemia. Diabetes 2005;54:712-719
36. Krishnamurthy J, Ramsey MR, Ligon KL, Torrice C, Koh A, Bonner-Weir S, Sharpless NE. p16INK4a induces an age-dependent decline in islet regenerative potential. Nature 2006;443:453-457
37. Uchida T, Nakamura T, Hashimoto N, Matsuda T, Kotani K, Sakaue H, Kido Y, Hayashi Y, Nakayama KI, White MF, Kasuga M. Deletion of Cdkn1b ameliorates hyperglycemia by maintaining compensatory hyperinsulinemia in diabetic mice. Nat Med 2005;11:175-182
38. Rachdi L, Balcazar N, Elghazi L, Barker DJ, Krits I, Kiyokawa H, Bernal-Mizrachi E. Differential effects of p27 in regulation of beta-cell mass during development, neonatal period, and adult life. Diabetes 2006;55:3520-3528
39. Cozar-Castellano I, Weinstock M, Haught M, Velázquez-Garcia S, Sipula D, Stewart AF. Evaluation of beta-cell replication in mice transgenic for hepatocyte growth factor and placental lactogen: comprehensive characterization of the G1/S regulatory proteins reveals unique involvement of p21cip. Diabetes 2006;55:70-77
40. Cozar-Castellano I, Haught M, Stewart AF. The cell cycle inhibitory protein p21cip is not essential for maintaining beta-cell cycle arrest or beta-cell function in vivo. Diabetes 2006;55:3271-3278
41. Difilippantonio MJ, Petersen S, Chen HT, Johnson R, Jasin M, Kanaar R, Ried T, Nussenzweig A. Evidence for replicative repair of DNA double-strand breaks leading to oncogenic translocation and gene amplification. J Exp Med 2002;196:469-480
42. Chesnokova V, Wong C, Zonis S, Gruszka A, Wawrowsky K, Ren SG, Benshlomo A, Yu R. Diminished pancreatic beta-cell mass in securin-null mice is caused by beta-cell apoptosis and senescence. Endocrinology 2009;150:2603-2610
43. Campisi J, Vijg J. Does damage to DNA and other macromolecules play a role in aging? If so, how? J Gerontol A Biol Sci Med Sci 2009;64:175-178