Id3 upregulates BrdU incorporation associated with a DNA damage response, not replication, in human pancreatic β-cells

Islets

Volumn 3, Issue 6, 2011, Pages 358-366

  Lee, Seung Hee ^a   Hao, Ergeng ^a,b   Levine, Fred ^a   Itkin Ansari, Pamela ^b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c BURNHAM INSTITUTE   (United States)

Author keywords

DNA damage; Regeneration; Replication

Indexed keywords

BROXURIDINE; CYCLIN DEPENDENT KINASE INHIBITOR 1C; HISTONE H2AX; HYDROXYUREA; INHIBITOR OF DIFFERENTIATION 3; KI 67 ANTIGEN;

ADENOVIRUS INFECTION; ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; DNA SYNTHESIS; GENE OVEREXPRESSION; GENE REPRESSION; GENE SILENCING; GENETIC ASSOCIATION; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; UPREGULATION;

ANIMALS; BROMODEOXYURIDINE; CELL CYCLE; CELL GROWTH PROCESSES; CYCLIN-DEPENDENT KINASE INHIBITOR P57; DNA DAMAGE; GENE EXPRESSION REGULATION; HISTONES; HUMANS; IMMUNOHISTOCHEMISTRY; INHIBITOR OF DIFFERENTIATION PROTEINS; INSULIN-SECRETING CELLS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KI-67 ANTIGEN; MALE; MICE; MICE, INBRED ICR; TRANSFECTION; UP-REGULATION;

EID: 80455143204     PISSN: 19382014     EISSN: 19382022     Source Type: Journal    
DOI: 10.4161/isl.3.6.17923     Document Type: Article

References (81)

1. 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; 52:102-10; PMID:12502499; DOI:10.2337/diabetes.52.1. 102.
2. Ritzel RA, Butler AE, Rizza RA, Veldhuis JD, Butler PC. Relationship between beta-cell mass and fasting blood glucose concentration in humans. Diabetes Care 2006; 29:717-8; PMID:16505537; DOI:10.2337/diacare.29.03.06.dc05- 1538.
3. Levine F, Itkin-Ansari P. Beta-cell regeneration: neogenesis, replication or both? J Mol Med 2008; 86:247-58; PMID:17922102; DOI:10.1007/s00109-007-0259- 1.
4. Demeterco C, Hao E, Lee SH, Itkin-Ansari P, Levine F. Adult human beta-cell neogenesis? Diabetes Obes Metab 2009; 11:46-53; PMID:19817788; DOI:10.1111/j.1463-326.2009.01105.x.
5. Hao E, Tyrberg B, Itkin-Ansari P, Lakey JR, Geron I, Monosov EZ, et al. Beta-cell differentiation from nonendocrine epithelial cells of the adult human pancreas. Nat Med 2006; 12:310-6; PMID:16491084; DOI:10.1038/nm1367.
6. Thorel F, Nepote V, Avril I, Kohno K, Desgraz R, Chera S, et al. Conversion of adult pancreatic alphacells to beta-cells after extreme beta-cell loss. Nature 2010; 464:1149-54; PMID:20364121; DOI:10.1038/nature08894.
7. Chung CH, Hao E, Piran R, Keinan E, Levine F. Pancreatic beta-cell neogenesis by direct conversion from mature alpha-cells. Stem Cells 2010; 28:1630-8; PMID:20653050; DOI:10.1002/stem.482.
8. Dor Y, Brown J, Martinez OI, Melton DA. Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 2004; 429:41-6; PMID:15129273; DOI:10.1038/nature02520.
9. Teta M, Long SY, Wartschow LM, Rankin MM, Kushner JA. Very slow turnover of beta-cells in aged adult mice. Diabetes 2005; 54:2557-67; PMID:16123343; DOI:10.2337/diabetes.54.9.2557.
10. 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; 12:817-26; PMID:17488631; DOI:10.1016/j.devcel.2007.04.011.
11. Brennand K, Huangfu D, Melton D. All beta cells contribute equally to islet growth and maintenance. PLoS Biol 2007; 5:163; PMID:17535113; DOI:10.1371/journal.pbio.0050163.
12. Meier JJ, Butler AE, Saisho Y, Monchamp T, Galasso R, Bhushan A, et al. Beta-cell replication is the primary mechanism subserving the postnatal expansion of beta-cell mass in humans. Diabetes 2008; 57:1584-94; PMID:18334605; DOI:10.2337/db07-1369.
13. Georgia S, Bhushan A. Beta cell replication is the primary mechanism for maintaining postnatal beta cell mass. J Clin Invest 2004; 114:963-8; PMID:15467835.
14. Xu X, D'Hoker J, Stange G, Bonne S, De Leu N, Xiao X, et al. Beta cells can be generated from endogenous progenitors in injured adult mouse pancreas. Cell 2008; 132:197-207; PMID:18243096; DOI:10.1016/j.cell.2007.12.015.
15. Lee SH, Hao E, Savinov AY, Geron I, Strongin AY, Itkin-Ansari P. Human beta-cell precursors mature into functional insulin-producing cells in an immunoisolation device: implications for diabetes cell therapies. Transplantation 2009; 87:983-91; PMID:19352116; DOI:10.1097/TP.0b013e31819c86ea.
16. Meier JJ, Butler AE, Galasso R, Rizza RA, Butler PC. Increased islet beta cell replication adjacent to intrapancreatic gastrinomas in humans. Diabetologia 2006; 49:2689-96; PMID:17016695; DOI:10.1007/s00125-006-0410-5.
17. Tyrberg B, Anachkov KA, Dib SA, Wang-Rodriguez J, Yoon KH, Levine F. Islet expression of the DNA repair enzyme 8-oxoguanosine DNA glycosylase (Ogg1) in human type 2 diabetes. BMC Endocr Disord 2002; 2:2; PMID:12003641; DOI:10.1186/1472-6823-2-2.
18. Menge BA, Tannapfel A, Belyaev O, Drescher R, Muller C, Uhl W, et al. Partial pancreatectomy in adult humans does not provoke beta-cell regeneration. Diabetes 2008; 57:142-9; PMID:17959931; DOI:10.2337/db07-1294.
19. Cnop M, Hughes SJ, Igoillo-Esteve M, Hoppa MB, Sayyed F, van de Laar L, et al. The long lifespan and low turnover of human islet beta cells estimated by mathematical modelling of lipofuscin accumulation. Diabetologia 2010; 53:321-30; PMID:19855953; DOI:10.1007/s00125-009-1562-x.
20. Perl S, Kushner JA, Buchholz BA, Meeker AK, Stein GM, Hsieh M, et al. Significant human beta-cell turnover is limited to the first three decades of life as determined by in vivo thymidine analog incorporation and radiocarbon dating. J Clin Endocrinol Metab 2010; 95:234-9; PMID:20660050; DOI:10.1210/jc.2010-0932.
21. Rankin MM, Kushner JA. Adaptive beta-cell proliferation is severely restricted with advanced age. Diabetes 2009; 58:1365-72; PMID:19265026; DOI:10.2337/db08-1198.
22. Genevay M, Pontes H, Meda P. Beta cell adaptation in pregnancy: a major difference between humans and rodents? Diabetologia 2010; 53:2089-92; PMID:20623217; DOI:10.1007/s00125-010-1848-z.
23. Butler AE, Cao-Minh L, Galasso R, Rizza RA, Corradin A, Cobelli C, et al. Adaptive changes in pancreatic beta cell fractional area and beta cell turnover in human pregnancy. Diabetologia 2010; 53:2167-76; PMID:20523966; DOI:10.1007/s00125-010-1809-6.
24. Rieck S, Kaestner KH. Expansion of beta-cell mass in response to pregnancy. Trends Endocrinol Metab 2010; 21:151-8; PMID:20015659; DOI:10.1016/j.tem.2009.11.001.
25. Parnaud G, Bosco D, Berney T, Pattou F, Kerr-Conte J, Donath MY, et al. Proliferation of sorted human and rat beta cells. Diabetologia 2008; 51:91-100; PMID:17994216; DOI:10.1007/s00125-007-0855-1.
26. Nielsen JH, Galsgaard ED, Moldrup A, Friedrichsen BN, Billestrup N, Hansen JA, et al. Regulation of betacell mass by hormones and growth factors. Diabetes 2001; 50:25-9; PMID:11272193; DOI:10.2337/diabetes.50.2007.S25.
27. Kassem SA, Ariel I, Thornton PS, Hussain K, Smith V, Lindley KJ, et al. p57(KIP2) expression in normal islet cells and in hyperinsulinism of infancy. Diabetes 2001; 50:2763-9; PMID:11723059; DOI:10.2337/diabetes.50.12.2763.
28. Itkin-Ansari P, Bain G, Beattie GM, Murre C, Hayek A, Levine F. E2A gene products are not required for insulin gene expression. Endocrinology 1996; 137:3540-3; PMID:8754784; DOI:10.1210/en.137.8.3540.
29. Itkin-Ansari P, Marcora E, Geron I, Tyrberg B, Demeterco C, Hao E, et al. NeuroD1 in the endocrine pancreas: localization and dual function as an activator and repressor. Dev Dyn 2005; 233:946-53; PMID:15906379; DOI:10.1002/dvdy.20443.
30. Ball AJ, Abrahamsson AE, Tyrberg B, Itkin-Ansari P, Levine F. HES6 reverses nuclear reprogramming of insulin-producing cells following cell fusion. Biochem Biophys Res Commun 2007; 355:331-7; PMID:17300753; DOI:10.1016/j.bbrc. 2007.01.153.
31. Demeterco C, Itkin-Ansari P, Tyrberg B, Ford LP, Jarvis RA, Levine F. c-Myc controls proliferation versus differentiation in human pancreatic endocrine cells. J Clin Endocrinol Metab 2002; 87:3475-85; PMID:12107268; DOI:10.1210/jc.87.7.3475.
32. Gradwohl G, Dierich A, LeMeur M, Guillemot F. neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas. Proc Natl Acad Sci USA 2000; 97:1607-11; PMID:10677506; DOI:10.1073/pnas.97.4.1607.
33. Wang S, Yan J, Anderson DA, Xu Y, Kanal MC, Cao Z, et al. Neurog3 gene dosage regulates allocation of endocrine and exocrine cell fates in the developing mouse pancreas. Dev Biol 2010; 339:26-37; PMID:20025861; DOI:10.1016/j.ydbio.2009.12.009.
34. Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 1990; 61:49-59; PMID:2156629; DOI:10.1016/0092-8674(90)90214-Y.
35. Fiaschi-Taesch N, Bigatel TA, Sicari B, Takane KK, Salim F, Velazquez-Garcia S, et al. Survey of the human pancreatic beta-cell G1/S proteome reveals a potential therapeutic role for cdk-6 and cyclin D1 in enhancing human beta-cell replication and function in vivo. Diabetes 2009; 58:882-93; PMID:19136653; DOI:10.2337/db08-0631.
36. Hua H, Zhang YQ, Dabernat S, Kritzik M, Dietz D, Sterling L, et al. BMP4 regulates pancreatic progenitor cell expansion through Id2. J Biol Chem 2006; 281:13574-80; PMID:16547003; DOI:10.1074/jbc.M600526200.
37. Cordle SR, Whelan J, Henderson E, Masuoka H, Weil PA, Stein R. Insulin gene expression in nonexpressing cells appears to be regulated by multiple distinct negative-acting control elements. Mol Cell Biol 1991; 11:2881-6; PMID:2017182.
38. Wice BM, Bernal-Mizrachi E, Permutt MA. Glucose and other insulin secretagogues induce, rather than inhibit, expression of Id-1 and Id-3 in pancreatic islet beta cells. Diabetologia 2001; 44:453-63; PMID:11357476; DOI:10.1007/s001250051643.
39. Lee SH, Hao E, Kiselyuk A, Shapiro J, Shields DJ, Lowy A, et al. The Id3/E47 axis mediates cell-cycle control in human pancreatic ducts and adenocarcinoma. Mol Cancer Res 2011; 9:782-90; PMID:21498546; DOI:10.1158/1541-7786.MCR-10-0535.
40. Kiselyuk A, Farber-Katz S, Cohen T, Lee SH, Geron I, Azimi B, et al. Phenothiazine neuroleptics signal to the human insulin promoter as revealed by a novel highthroughput screen. J Biomol Screen 2010; 15:663-70; PMID:20547533; DOI:10.1177/1087057110372257.
41. Kip2 to regulate cell cycle in neural cells. Mol Cell Biol 2006; 26:4351-61; PMID:16705184; DOI:10.1128/MCB.01743-05.
42. Jung HS, Ahn YR, Oh SH, Kim YS, No H, Lee MK, et al. Enhancement of beta-cell regeneration by islet transplantation after partial pancreatectomy in mice. Transplantation 2009; 88:354-9; PMID:19667937; DOI:10.1097/TP. 0b013e3181b07a02.
43. Brelje TC, Parsons JA, Sorenson RL. Regulation of islet beta-cell proliferation by prolactin in rat islets. Diabetes 1994; 43:263-73; PMID:7904577; DOI:10.2337/diabetes.43.2.263.
44. Xu G, Stoffers DA, Habener JF, Bonner-Weir S. Exendin-4 stimulates both beta-cell replication and neogenesis, resulting in increased beta-cell mass and improved glucose tolerance in diabetic rats. Diabetes 1999; 48:2270-6; PMID:10580413; DOI:10.2337/diabetes.48.12.2270.
45. Movassat J, Beattie GM, Lopez AD, Hayek A. Exendin 4 up-regulates expression of PDX 1 and hastens differentiation and maturation of human fetal pancreatic cells. J Clin Endocrinol Metab 2002; 87:4775-81; PMID:12364473; DOI:10.1210/jc.2002-020137.
46. Cortez D. Caffeine inhibits checkpoint responses without inhibiting the ataxia-telangiectasia-mutated (ATM) and ATM- and Rad3-related (ATR) protein kinases. J Biol Chem 2003; 278:37139-45; PMID:12847089; DOI:10.1074/jbc. M307088200.
47. Taupin P. BrdU immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations and validation. Brain Res Rev 2007; 53:198-214; PMID:17020783; DOI:10.1016/j.brainresrev.2006.08.002.
48. Nagai S, Dubrana K, Tsai-Pflugfelder M, Davidson MB, Roberts TM, Brown GW, et al. Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 2008; 322:597-602; PMID:18948542; DOI:10.1126/science.1162790.
49. Francis AA, Blevins RD, Carrier WL, Smith DP, Regan JD. Inhibition of DNA repair in ultraviolet-irradiated human cells by hydroxyurea. Biochim Biophys Acta 1979; 563:385-92; PMID:465496.
50. Ward IM, Chen J. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J Biol Chem 2001; 276:47759-62; PMID:11673449.
51. Liu JS, Kuo SR, Melendy T. Comparison of checkpoint responses triggered by DNA polymerase inhibition versus DNA damaging agents. Mutat Res 2003; 532:215-26; PMID:14643438; DOI:10.1016/j.mrfmmm.2003.08.018.
52. Anderson L, Henderson C, Adachi Y. Phosphorylation and rapid relocalization of 53BP1 to nuclear foci upon DNA damage. Mol Cell Biol 2001; 21:1719-29; PMID:11238909; DOI:10.1128/MCB.21.5.1719-29.2001.
53. Zebedee Z, Hara E. Id proteins in cell cycle control and cellular senescence. Oncogene 2001; 20:8317-25; PMID:11840324; DOI:10.1038/sj.onc. 1205092.
54. Sikder HA, Devlin MK, Dunlap S, Ryu B, Alani RM. Id proteins in cell growth and tumorigenesis. Cancer Cell 2003; 3:525-30; PMID:12842081; DOI:10.1016/S1535-6108(03)00141-7.
55. Fong S, Debs RJ, Desprez PY. Id genes and proteins as promising targets in cancer therapy. Trends Mol Med 2004; 10:387-92; PMID:15310459; DOI:10.1016/j.molmed.2004.06.008.
56. Yokota Y, Mori S. Role of Id family proteins in growth control. J Cell Physiol 2002; 190:21-8; PMID:11807807; DOI:10.1002/jcp.10042.
57. Prabhu S, Ignatova A, Park ST, Sun XH. Regulation of the expression of cyclin-dependent kinase inhibitor p21 by E2A and Id proteins. Mol Cell Biol 1997; 17:5888-96; PMID:9315646.
58. Pagliuca A, Gallo P, De Luca P, Lania L. Class A helix-loop-helix proteins are positive regulators of several cyclin-dependent kinase inhibitors' promoter activity and negatively affect cell growth. Cancer Res 2000; 60:1376-82; PMID:10728702.
59. Lyden D, Young AZ, Zagzag D, Yan W, Gerald W, O'Reilly R, et al. Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 1999; 401:670-7; PMID:10537105; DOI:10.1038/44334.
60. Mori S, Nishikawa SI, Yokota Y. Lactation defect in mice lacking the helix-loop-helix inhibitor Id2. EMBO J 2000; 19:5772-81; PMID:11060028; DOI:10.1093/emboj/19.21.5772.
61. INK4a expression during cellular senescence. Nature 2001; 409:1067-70; PMID:11234019; DOI:10.1038/35059131.
62. Ouyang XS, Wang X, Ling MT, Wong HL, Tsao SW, Wong YC. Id-1 stimulates serum independent prostate cancer cell proliferation through inactivation of p16(INK4a)/pRB pathway. Carcinogenesis 2002; 23:721-5; PMID:12016143; DOI:10.1093/carcin/23.5.721.
63. 1 phase and is required for cell-cycle progression. Oncogene 2007; 26:5772-83; PMID:17404577; DOI:10.1038/sj.onc.1210386.
64. INK4a induces an age-dependent decline in islet regenerative potential. Nature 2006; 443:453-7; PMID:16957737; DOI:10.1038/nature05092.
65. Buck SB, Bradford J, Gee KR, Agnew BJ, Clarke ST, Salic A. Detection of S-phase cell cycle progression using 5-ethynyl-2′-deoxyuridine incorporation with click chemistry, an alternative to using 5-bromo-2′- deoxyuridine antibodies. Biotechniques 2008; 44:927-9; PMID:18533904; DOI:10.2144/000112812.
66. Köhler CU, Kreuter A, Rozynkowski MC, Rahmel T, Uhl W, Tannapfel A, et al. Validation of different replication markers for the detection of beta-cell proliferation in human pancreatic tissue. Regul Pept 2010; 162:115-21; PMID:20079379; DOI:10.1016/j.regpep.2009.12.021.
67. Kurki P, Vanderlaan M, Dolbeare F, Gray J, Tan EM. Expression of proliferating cell nuclear antigen (PCNA)/cyclin during the cell cycle. Exp Cell Res 1986; 166:209-19; PMID:2874992; DOI:10.1016/0014-4827(86)90520-3.
68. Bruno S, Crissman HA, Bauer KD, Darzynkiewicz Z. Changes in cell nuclei during S phase: progressive chromatin condensation and altered expression of the proliferation-associated nuclear proteins Ki-67, cyclin (PCNA), p105 and p34. Exp Cell Res 1991; 196:99-106; PMID:1831764; DOI:10.1016/0014-4827(91)90460-C.
69. Tsurusawa M, Ito M, Zha Z, Kawai S, Takasaki Y, Fujimoto T. Cell-cycle-associated expressions of proliferating cell nuclear antigen and Ki-67 reactive antigen of bone marrow blast cells in childhood acute leukemia. Leukemia 1992; 6:669-74; PMID:1352561.
70. Perfetti R, Zhou J, Doyle ME, Egan JM. Glucagon-like peptide-1 induces cell proliferation and pancreatic-duodenum homeobox-1 expression and increases endocrine cell mass in the pancreas of old, glucose-intolerant rats. Endocrinology 2000; 141:4600-5; PMID:11108273; DOI:10.1210/en.141.12.4600.
71. Essers J, Theil AF, Baldeyron C, van Cappellen WA, Houtsmuller AB, Kanaar R, et al. Nuclear dynamics of PCNA in DNA replication and repair. Mol Cell Biol 2005; 25:9350-9; PMID:16227586; DOI:10.1128/MCB.25.21.9350-9.2005.
72. Ward IM, Wu X, Chen J. Threonine 68 of Chk2 is phosphorylated at sites of DNA strand breaks. J Biol Chem 2001; 276:47755-8; PMID:11668173.
73. Pictet RL, Clark WR, Williams RH, Rutter WJ. An ultrastructural analysis of the developing embryonic pancreas. Dev Biol 1972; 29:436-67; PMID:4570759; DOI:10.1016/0012-1606(72)90083-8.
74. Lee SH, Itkin-Ansari P, Levine F. CENP-A, a protein required for chromosome segregation in mitosis, declines with age in islet but not exocrine cells. Aging 2010; 2:785-90; PMID:21068465.
75. cip is not essential for maintaining beta-cell cycle arrest or beta-cell function in vivo. Diabetes 2006; 55:3271-8; PMID:17130470; DOI:10.2337/db06-0627.
76. Rane SG, Dubus P, Mettus RV, Galbreath EJ, Boden G, Reddy EP, et al. Loss of Cdk4 expression causes insulin-deficient diabetes and Cdk4 activation results in beta-islet cell hyperplasia. Nat Genet 1999; 22:44-52; PMID:10319860; DOI:10.1038/8751.
77. Martín J, Hunt SL, Dubus P, Sotillo R, Nehme-Pelluard F, Magnuson MA, et al. Genetic rescue of Cdk4 null mice restores pancreatic beta-cell proliferation but not homeostatic cell number. Oncogene 2003; 22:5261-9; PMID:12917627; DOI:10.1038/sj.onc.1206506.
78. Marzo N, Mora C, Fabregat ME, Martin J, Usac EF, Franco C, et al. Pancreatic islets from cyclin-dependent kinase 4/R24C (Cdk4) knockin mice have significantly increased beta cell mass and are physiologically functional, indicating that Cdk4 is a potential target for pancreatic beta cell mass regeneration in Type 1 diabetes. Diabetologia 2004; 47:686-94; PMID:15298346; DOI:10.1007/s00125-004-1372-0.
79. Kushner JA, Ciemerych MA, Sicinska E, Wartschow LM, Teta M, Long SY, et al. Cyclins D2 and D1 are essential for postnatal pancreatic beta-cell growth. Mol Cell Biol 2005; 25:3752-62; PMID:15831479; DOI:10.1128/MCB.25.9.3752-62. 2005.
80. 1/S regulatory molecule, cdk6. Diabetes 2010; 59:1926-36; PMID:20668294; DOI:10.2337/db09-1776.
81. Matsumura ME, Li F, Berthoux L, Wei B, Lobe DR, Jeon C, et al. Vascular injury induces posttranscriptional regulation of the Id3 gene: cloning of a novel Id3 isoform expressed during vascular lesion formation in rat and human atherosclerosis. Arterioscler Thromb Vasc Biol 2001; 21:752-8; PMID:11348870; DOI:10.1161/01.ATV.21.5.752.