Differential regulation of embryonic and adult β cell replication

Cell Cycle

Volumn 11, Issue 13, 2012, Pages 2431-2442

  Gunasekaran, Uma ^a   Hudgens, Courtney W ^a   Wright, Brian T ^a   Maulis, Matthew F ^a   Gannon, Maureen ^a,b,c  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Connective tissue growth factor; Diabetes; Embryogenesis; Pancreatic cell; Replication

Indexed keywords

CONNECTIVE TISSUE GROWTH FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CELL DIVISION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW;

EID: 84863798318     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.20545     Document Type: Review

References (79)

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; http://dx.doi.org/10.2337/ diabetes.52.1.102.
2. Diseases NIoDaDaK. National Diabetes Fact Sheet 2011.
3. Crawford LA, Guney MA, Oh YA, Deyoung RA, Valenzuela DM, Murphy AJ, et al. Connective tissue growth factor (CTGF) inactivation leads to defects in islet cell lineage allocation and beta-cell proliferation during embryogenesis. Mol Endocrinol 2009; 23:324-36; PMID:19131512; http://dx.doi.org/10.1210/me. 2008-0045.
4. Guney MA, Petersen CP, Boustani A, Duncan MR, Gunasekaran U, Menon R, et al. Connective tissue growth factor acts within both endothelial cells and beta cells to promote proliferation of developing beta cells. Proc Natl Acad Sci USA 2011; 108:15242-7; PMID:21876171; http://dx.doi.org/10.1073/pnas.1100072108.
5. Milo-Landesman D, Surana M, Berkovich I, Compagni A, Christofori G, Fleischer N, et al. Correction of hyperglycemia in diabetic mice transplanted with reversibly immortalized pancreatic beta cells controlled by the tet-on regulatory system. Cell Transplant 2001; 10:645-50; PMID:11714200.
6. Offield MF, Jetton TL, Labosky PA, Ray M, Stein RW, Magnuson MA, et al. PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 1996; 122:983-95; PMID:8631275.
7. Kawaguchi Y, Cooper B, Gannon M, Ray M, MacDonald RJ, Wright CV. The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat Genet 2002; 32:128-34; PMID:12185368; http://dx.doi.org/10. 1038/ng959.
8. 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; http://dx.doi.org/10.1073/pnas.97. 4.1607.
9. Jacquemin P, Durviaux SM, Jensen J, Godfraind C, Gradwohl G, Guillemot F, et al. Transcription factor hepatocyte nuclear factor 6 regulates pancreatic endocrine cell differentiation and controls expression of the proendocrine gene ngn3. Mol Cell Biol 2000; 20:4445-54; PMID:10825208; http://dx.doi.org/10.1128/ MCB.20.12.4445-54.2000.
10. Seymour PA, Freude KK, Dubois CL, Shih HP, Patel NA, Sander M. A dosage-dependent requirement for Sox9 in pancreatic endocrine cell formation. Dev Biol 2008; 323:19-30; PMID:18723011; http://dx.doi.org/10.1016/j.ydbio.2008. 07.034.
11. Oliver-Krasinski JM, Kasner MT, Yang J, Crutchlow MF, Rustgi AK, Kaestner KH, et al. The diabetes gene Pdx1 regulates the transcriptional network of pancreatic endocrine progenitor cells in mice. J Clin Invest 2009; 119:1888-98; PMID:19487809; http://dx.doi.org/10.1172/JCI37028.
12. Sander M, Sussel L, Conners J, Scheel D, Kalamaras J, Dela Cruz F, et al. Homeobox gene Nkx6.1 lies downstream of Nkx2.2 in the major pathway of beta-cell formation in the pancreas. Development 2000; 127:5533-40; PMID:11076772.
13. Kim SK, MacDonald RJ. Signaling and transcriptional control of pancreatic organogenesis. Curr Opin Genet Dev 2002; 12:540-7; PMID:12200159; http://dx.doi.org/10.1016/S0959-437X(02)00338-6.
14. Jensen J. Gene regulatory factors in pancreatic development. Dev Dyn 2004; 229:176-200; PMID:14699589; http://dx.doi.org/10.1002/dvdy.10460.
15. Pan FC, Wright C. Pancreas organogenesis: from bud to plexus to gland. Dev Dyn 2011; 240:530-65; PMID:21337462; http://dx.doi.org/10.1002/dvdy.22584.
16. Zhang W, Feng D, Li Y, Iida K, McGrath B, Cavener DR. PERK EIF2AK3 control of pancreatic beta cell differentiation and proliferation is required for postnatal glucose homeostasis. Cell Metab 2006; 4:491-7; PMID:17141632; http://dx.doi.org/10.1016/j.cmet.2006.11.002.
17. Ford SP, Zhang L, Zhu M, Miller MM, Smith DT, Hess BW, et al. Maternal obesity accelerates fetal pancreatic beta-cell but not alpha-cell development in sheep: prenatal consequences. Am J Physiol Regul Integr Comp Physiol 2009; 297:835-43; PMID:19605766; http://dx.doi.org/10.1152/ajpregu.00072.2009.
18. Georgia S, Bhushan A. p27 Regulates the transition of beta-cells from quiescence to proliferation. Diabetes 2006; 55:2950-6; PMID:17065330; http://dx.doi.org/10.2337/db06-0249.
19. Guz Y, Montminy MR, Stein R, Leonard J, Gamer LW, Wright CV, et al. Expression of murine STF-1, a putative insulin gene transcription factor, in beta cells of pancreas, duodenal epithelium and pancreatic exocrine and endocrine progenitors during ontogeny. Development 1995; 121:11-8; PMID:7867492.
20. Holland AM, Hale MA, Kagami H, Hammer RE, MacDonald RJ. Experimental control of pancreatic development and maintenance. Proc Natl Acad Sci USA 2002; 99:12236-41; PMID:12221286; http://dx.doi.org/10.1073/pnas.192255099.
21. Gannon M, Ables ET, Crawford L, Lowe D, Offield MF, Magnuson MA, et al. pdx-1 function is specifically required in embryonic beta cells to generate appropriate numbers of endocrine cell types and maintain glucose homeostasis. Dev Biol 2008; 314:406-17; PMID:18155690; http://dx.doi.org/10.1016/j.ydbio. 2007.10.038.
22. Artner I, Blanchi B, Raum JC, Guo M, Kaneko T, Cordes S, et al. MafB is required for islet beta cell maturation. Proc Natl Acad Sci USA 2007; 104:3853-8; PMID:17360442; http://dx.doi.org/10.1073/pnas.0700013104.
23. Moussad EE, Brigstock DR. Connective tissue growth factor: what's in a name? Mol Genet Metab 2000; 71:276-92; PMID:11001822; http://dx.doi.org/10.1006/ mgme.2000.3059.
24. Zhang C, Moriguchi T, Kajihara M, Esaki R, Harada A, Shimohata H, et al. MafA is a key regulator of glucose-stimulated insulin secretion. Mol Cell Biol 2005; 25:4969-76; PMID:15923615; http://dx.doi.org/10.1128/MCB.25.12.4969-76. 2005.
25. Finegood DT, Scaglia L, Bonner-Weir S. Dynamics of beta-cell mass in the growing rat pancreas. Estimation with a simple mathematical model. Diabetes 1995; 44:249-56; PMID:7883109; http://dx.doi.org/10.2337/diabetes.44.3.249.
26. 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; http://dx.doi.org/10.1038/nature02520.
27. Ahlgren U, Jonsson J, Jonsson L, Simu K, Edlund H. Beta-cell-specific inactivation of the mouse Ipf1/Pdx1 gene results in loss of the beta-cell phenotype and maturity onset diabetes. Genes Dev 1998; 12:1763-8; PMID:9637677; http://dx.doi.org/10.1101/gad.12.12.1763.
28. 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.
29. Martín J, Hunt SL, Dubus P, Sotillo R, Néhmé- Pélluard 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; http://dx.doi.org/10.1038/sj.onc.1206506.
30. INK4a induces an age-dependent decline in islet regenerative potential. Nature 2006; 443:453-7; PMID:16957737; http://dx.doi.org/10.1038/ nature05092.
31. Dhawan S, Tschen SI, Bhushan A. Bmi-1 regulates the Ink4a/Arf locus to control pancreatic beta-cell proliferation. Genes Dev 2009; 23:906-11; PMID:19390085; http://dx.doi.org/10.1101/gad.1742609.
32. Chen H, Gu X, Su IH, Bottino R, Contreras JL, Tarakhovsky A, et al. Polycomb protein Ezh2 regulates pancreatic beta-cell Ink4a/Arf expression and regeneration in diabetes mellitus. Genes Dev 2009; 23:975-85; PMID:19390090; http://dx.doi.org/10.1101/gad.1742509.
33. Chen H, Gu X, Liu Y, Wang J, Wirt SE, Bottino R, et al. PDGF signalling controls age-dependent proliferation in pancreatic β-cells. Nature 2011; 478:349-55; PMID:21993628; http://dx.doi.org/10.1038/nature10502.
34. Wang IC, Chen YJ, Hughes D, Petrovic V, Major ML, Park HJ, et al. Forkhead box M1 regulates the transcriptional network of genes essential for mitotic progression and genes encoding the SCF (Skp2-Cks1) ubiquitin ligase. Mol Cell Biol 2005; 25:10875-94; PMID:16314512; http://dx.doi.org/10.1128/MCB.25. 24.10875-94.2005.
35. Laoukili J, Kooistra MR, Brás A, Kauw J, Kerkhoven RM, Morrison A, et al. FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat Cell Biol 2005; 7:126-36; PMID:15654331; http://dx.doi.org/10. 1038/ncb1217.
36. Zhang H, Zhang J, Pope CF, Crawford LA, Vasavada RC, Jagasia SM, et al. Gestational diabetes mellitus resulting from impaired beta-cell compensation in the absence of FoxM1, a novel downstream effector of placental lactogen. Diabetes 2010; 59:143-52; PMID:19833884; http://dx.doi.org/10.2337/db09-0050.
37. Ackermann Misfeldt A, Costa RH, Gannon M. Beta-cell proliferation, but not neogenesis, following 60% partial pancreatectomy is impaired in the absence of FoxM1. Diabetes 2008; 57:3069-77; PMID:18728229; http://dx.doi.org/10.2337/ db08-0878.
38. Zhang H, Ackermann AM, Gusarova GA, Lowe D, Feng X, Kopsombut UG, et al. The FoxM1 transcription factor is required to maintain pancreatic beta-cell mass. Mol Endocrinol 2006; 20:1853-66; PMID:16556734; http://dx.doi.org/10.1210/ me.2006-0056.
39. Gunasekaran U, Gannon M. Type 2 diabetes and the aging pancreatic beta cell. Aging 2011; 3:565-75; PMID:21765202.
40. Kushner JA. Beta-cell growth: an unusual paradigm of organogenesis that is cyclin D2/Cdk4 dependent. Cell Cycle 2006; 5:234-7; PMID:16410729; http://dx.doi.org/10.4161/cc.5.3.2399.
41. Dhawan S, Georgia S, Bhushan A. Formation and regeneration of the endocrine pancreas. Curr Opin Cell Biol 2007; 19:634-45; PMID:18061427; http://dx.doi.org/10.1016/j.ceb.2007.09.015.
42. Cozar-Castellano I, Fiaschi-Taesch N, Bigatel TA, Takane KK, Garcia-Ocaña A, Vasavada R, et al. Molecular control of cell cycle progression in the pancreatic beta-cell. Endocr Rev 2006; 27:356-70; PMID:16638909; http://dx.doi.org/10.1210/er.2006-0004.
43. Pick A, Clark J, Kubstrup C, Levisetti M, Pugh W, Bonner-Weir S, et al. Role of apoptosis in failure of beta-cell mass compensation for insulin resistance and beta-cell defects in the male Zucker diabetic fatty rat. Diabetes 1998; 47:358-64; PMID:9519740; http://dx.doi.org/10.2337/diabetes.47.3.358.
44. Sorenson RL, Brelje TC. Adaptation of islets of Langerhans to pregnancy: beta-cell growth, enhanced insulin secretion and the role of lactogenic hormones. Horm Metab Res 1997; 29:301-7; PMID:9230352; http://dx.doi.org/10. 1055/s-2007-979040.
45. Bonner-Weir S, Deery D, Leahy JL, Weir GC. Compensatory growth of pancreatic beta-cells in adult rats after short-term glucose infusion. Diabetes 1989; 38:49-53; PMID:2642434; http://dx.doi.org/10.2337/diabetes.38.1.49.
46. Topp BG, McArthur MD, Finegood DT. Metabolic adaptations to chronic glucose infusion in rats. Diabetologia 2004; 47:1602-10; PMID:15349726; http://dx.doi.org/10.1007/s00125-004-1493-5.
47. Paris M, Bernard-Kargar C, Berthault MF, Bouwens L, Ktorza A. Specific and combined effects of insulin and glucose on functional pancreatic beta-cell mass in vivo in adult rats. Endocrinology 2003; 144:2717-27; PMID:12746336; http://dx.doi.org/10.1210/en.2002-221112.
48. Kozma SC, Thomas G. Regulation of cell size in growth, development and human disease: PI3K, PKB and S6K. Bioessays 2002; 24:65-71; PMID:11782951; http://dx.doi.org/10.1002/bies.10031.
49. Gu Y, Lindner J, Kumar A, Yuan W, Magnuson MA. Rictor/mTORC2 is essential for maintaining a balance between beta-cell proliferation and cell size. Diabetes 2011; 60:827-37; PMID:21266327; http://dx.doi.org/10.2337/db10-1194.
50. Kitamura T, Nakae J, Kitamura Y, Kido Y, Biggs WH, 3rd, Wright CV, et al. The forkhead transcription factor Foxo1 links insulin signaling to Pdx1 regulation of pancreatic beta cell growth. J Clin Invest 2002; 110:1839-47; PMID:12488434.
51. Kulkarni RN, Jhala US, Winnay JN, Krajewski S, Montminy M, Kahn CR. PDX-1 haploinsufficiency limits the compensatory islet hyperplasia that occurs in response to insulin resistance. J Clin Invest 2004; 114:828-36; PMID:15372107.
52. Heit JJ, Apelqvist AA, Gu X, Winslow MM, Neilson JR, Crabtree GR, et al. Calcineurin/NFAT signalling regulates pancreatic beta-cell growth and function. Nature 2006; 443:345-9; PMID:16988714; http://dx.doi.org/10.1038/nature05097.
53. Lawrence MC, Bhatt HS, Easom RA. NFAT regulates insulin gene promoter activity in response to synergistic pathways induced by glucose and glucagon-like peptide-1. Diabetes 2002; 51:691-8; PMID:11872668; http://dx.doi.org/10.2337/diabetes.51.3.691.
54. Liu J, Farmer JD Jr, Lane WS, Friedman J, Weissman I, Schreiber SL. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 1991; 66:807-15; PMID:1715244; http://dx.doi.org/10.1016/0092- 8674(91)90124-H.
55. Buchanan TA, Metzger BE, Freinkel N, Bergman RN. Insulin sensitivity and B-cell responsiveness to glucose during late pregnancy in lean and moderately obese women with normal glucose tolerance or mild gestational diabetes. Am J Obstet Gynecol 1990; 162:1008-14; PMID:2183610.
56. Vasavada RC, Garcia-Ocaña A, Zawalich WS, Sorenson RL, Dann P, Syed M, et al. Targeted expression of placental lactogen in the beta cells of transgenic mice results in beta cell proliferation, islet mass augmentation and hypoglycemia. J Biol Chem 2000; 275:15399-406; PMID:10809775; http://dx.doi.org/10.1074/jbc.275.20.15399.
57. Kim H, Toyofuku Y, Lynn FC, Chak E, Uchida T, Mizukami H, et al. Serotonin regulates pancreatic beta cell mass during pregnancy. Nat Med 2010; 16:804-8; PMID:20581837; http://dx.doi.org/10.1038/nm.2173.
58. Otonkoski T, Beattie GM, Rubin JS, Lopez AD, Baird A, Hayek A. Hepatocyte growth factor/scatter factor has insulinotropic activity in human fetal pancreatic cells. Diabetes 1994; 43:947-53; PMID:8013761; http://dx.doi.org/10. 2337/diabetes.43.7.947.
59. 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; http://dx.doi.org/10.2337/diabetes.48.12.2270.
60. Hügl SR, White MF, Rhodes CJ. Insulin-like growth factor I (IGF-I)-stimulated pancreatic beta-cell growth is glucose-dependent. Synergistic activation of insulin receptor substrate-mediated signal transduction pathways by glucose and IGF-I in INS-1 cells. J Biol Chem 1998; 273:17771-9; PMID:9651378; http://dx.doi.org/10.1074/jbc.273.28.17771.
61. Zhou Y, Capuco AV, Jiang H. Involvement of connective tissue growth factor (CTGF) in insulinlike growth factor-I (IGF1) stimulation of proliferation of a bovine mammary epithelial cell line. Domest Anim Endocrinol 2008; 35:180-9; PMID:18586434; http://dx.doi.org/10.1016/j.domaniend.2008.05.003.
62. Rankin MM, Kushner JA. Adaptive beta-cell proliferation is severely restricted with advanced age. Diabetes 2009; 58:1365-72; PMID:19265026; http://dx.doi.org/10.2337/db08-1198.
63. Artner I, Hang Y, Mazur M, Yamamoto T, Guo M, Lindner J, et al. MafA and MafB regulate genes critical to beta-cells in a unique temporal manner. Diabetes 2010; 59:2530-9; PMID:20627934; http://dx.doi.org/10.2337/db10-0190.
64. di Mola FF, Friess H, Martignoni ME, Di Sebastiano P, Zimmermann A, Innocenti P, et al. Connective tissue growth factor is a regulator for fibrosis in human chronic pancreatitis. Ann Surg 1999; 230:63-71; PMID:10400038; http://dx.doi.org/10.1097/00000658-199907000-00010.
65. Hartel M, Di Mola FF, Gardini A, Zimmermann A, Di Sebastiano P, Guweidhi A, et al. Desmoplastic reaction influences pancreatic cancer growth behavior. World J Surg 2004; 28:818-25; PMID:15457365; http://dx.doi.org/10.1007/s00268- 004-7147-4.
66. Brigstock DR. Regulation of angiogenesis and endothelial cell function by connective tissue growth factor (CTGF) and cysteine-rich 61 (CYR61). Angiogenesis 2002; 5:153-65; PMID:12831056; http://dx.doi.org/10.1023/A: 1023823803510.
67. Yang H, Huang Y, Chen X, Liu J, Lu Y, Bu L, et al. The role of CTGF in the diabetic rat retina and its relationship with VEGF and TGFbeta, elucidated by treatment with CTGFsiRNA. Acta Ophthalmol 2009.
68. Kroon E, Martinson LA, Kadoya K, Bang AG, Kelly OG, Eliazer S, et al. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol 2008; 26:443-52; PMID:18288110; http://dx.doi.org/10.1038/nbt1393.
69. Dutta S, Bonner-Weir S, Montminy M, Wright C. Regulatory factor linked to late-onset diabetes? Nature 1998; 392:560; PMID:9560151; http://dx.doi.org/10. 1038/33311.
70. Rose SD, Swift GH, Peyton MJ, Hammer RE, MacDonald RJ. The role of PTF1-P48 in pancreatic acinar gene expression. J Biol Chem 2001; 276:44018-26; PMID:11562365; http://dx.doi.org/10.1074/jbc.M106264200.
71. Wang S, Jensen JN, Seymour PA, Hsu W, Dor Y, Sander M, et al. Sustained Neurog3 expression in hormone-expressing islet cells is required for endocrine maturation and function. Proc Natl Acad Sci USA 2009; 106:9715-20; PMID:19487660; http://dx.doi.org/10.1073/pnas.0904247106.
72. Dubois CL, Shih HP, Seymour PA, Patel NA, Behrmann JM, Ngo V, et al. Sox9-haploinsufficiency causes glucose intolerance in mice. PLoS ONE 2011; 6:23131; PMID:21829703; http://dx.doi.org/10.1371/journal.pone.0023131.
73. Zhang H, Ables ET, Pope CF, Washington MK, Hipkens S, Means AL, et al. Multiple, temporal-specific roles for HNF6 in pancreatic endocrine and ductal differentiation. Mech Dev 2009; 126:958-73; PMID:19766716; http://dx.doi.org/10. 1016/j.mod.2009.09.006.
74. Artner I, Le Lay J, Hang Y, Elghazi L, Schisler JC, Henderson E, et al. MafB: an activator of the glucagon gene expressed in developing islet alpha- and beta-cells. Diabetes 2006; 55:297-304; PMID:16443760; http://dx.doi.org/10. 2337/diabetes.55.02.06.db05-0946.
75. Buteau J, Accili D. Regulation of pancreatic beta-cell function by the forkhead protein FoxO1. Diabetes Obes Metab 2007; 9:140-6; PMID:17919188; http://dx.doi.org/10.1111/j.1463-326.2007.00782.x.
76. Garcia-Ocaña A, Takane KK, Syed MA, Philbrick WM, Vasavada RC, Stewart AF. Hepatocyte growth factor overexpression in the islet of transgenic mice increases beta cell proliferation, enhances islet mass and induces mild hypoglycemia. J Biol Chem 2000; 275:1226-32; PMID:10625667; http://dx.doi.org/ 10.1074/jbc.275.2.1226.
77. Cozar-Castellano I, Takane KK, Bottino R, Balamurugan AN, Stewart AF. Induction of beta-cell proliferation and retinoblastoma protein phosphorylation in rat and human islets using adenovirus-mediated transfer of cyclin-dependent kinase-4 and cyclin D1. Diabetes 2004; 53:149-59; PMID:14693709; http://dx.doi.org/10.2337/diabetes.53.1.149.
78. Westmoreland JJ, Wang Q, Bouzaffour M, Baker SJ, Sosa-Pineda B. Pdk1 activity controls proliferation, survival and growth of developing pancreatic cells. Dev Biol 2009; 334:285-98; PMID:19635472; http://dx.doi.org/10.1016/j. ydbio.2009.07.030.
79. Zehri A. Differential effects of pulsatile vs. chronic hyperglycemia on fetal pancreatic beta cell population. Physiology. Tuscon: University of Arizona 2011; 22.