β-Cell differentiation and regeneration in type 1 diabetes

Diabetes, Obesity and Metabolism

Volumn 15, Issue S3, 2013, Pages 98-104

  Ding, L ^a   Gysemans, C ^a   Mathieu, C ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Regeneration; Replication; Reprogramming; Type 1 diabetes; cells

Indexed keywords

GROWTH FACTOR; INCRETIN; TRANSCRIPTION FACTOR;

ACINAR CELL; APOPTOSIS; CELL DEATH; CELL DIFFERENTIATION; CELL DIVISION; CELL FUNCTION; CELL REGENERATION; CELL RENEWAL; CELL TYPE; IMMUNOLOGICAL TOLERANCE; INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS ISLET; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; PROTEIN EXPRESSION; REVIEW;

REGENERATION; REPLICATION; REPROGRAMMING; TYPE 1 DIABETES; Β-CELLS;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL TRANSDIFFERENTIATION; DIABETES MELLITUS, TYPE 1; HUMANS; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; REGENERATION;

EID: 84883510524     PISSN: 14628902     EISSN: 14631326     Source Type: Journal    
DOI: 10.1111/dom.12164     Document Type: Review

References (75)

1. van Belle TL, Coppieters KT, von Herrath MG. Type 1 diabetes: etiology, immunology, and therapeutic strategies. Physiol Rev 2011; 91: 79-118.
2. Sherry NA, Kushner JA, Glandt M, Kitamura T, Brillantes AM, Herold KC. Effects of autoimmunity and immune therapy on beta-cell turnover in type 1 diabetes. Diabetes 2006; 55: 3238-3245.
3. Nir T, Melton DA, Dor Y. Recovery from diabetes in mice by beta cell regeneration. J Clin Invest 2007; 117: 2553-2561.
4. Meier JJ, Bhushan A, Butler AE, Rizza RA, Butler PC. Sustained beta cell apoptosis in patients with long-standing type 1 diabetes: indirect evidence for islet regeneration? Diabetologia 2005; 48: 2221-2228.
5. Paris M, Tourrel-Cuzin C, Plachot C, Ktorza A. Review: pancreatic beta-cell neogenesis revisited. Exp Diabesity Res 2004; 5: 111-121.
6. 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.
7. Meier JJ, Butler AE, Saisho Y et al. Beta-cell replication is the primary mechanism subserving the postnatal expansion of beta-cell mass in humans. Diabetes 2008; 57: 1584-1594.
8. Cnop M, Igoillo-Esteve M, Hughes SJ, Walker JN, Cnop I, Clark A. Longevity of human islet alpha- and beta-cells. Diabetes Obes Metab 2011; 13(Suppl. 1): 39-46.
9. 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: 249-256.
10. Cnop M, Hughes SJ, Igoillo-Esteve M et al. The long lifespan and low turnover of human islet beta cells estimated by mathematical modelling of lipofuscin accumulation. Diabetologia 2009; 53: 321-330.
11. Perl S, Kushner JA, Buchholz BA 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: E234-239.
12. 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: 301-307.
13. Peshavaria M, Larmie BL, Lausier J et al. Regulation of pancreatic beta-cell regeneration in the normoglycemic 60% partial-pancreatectomy mouse. Diabetes 2006; 55: 3289-3298.
14. Heit JJ, Karnik SK, Kim SK. Intrinsic regulators of pancreatic beta-cell proliferation. Annu Rev Cell Dev Biol 2006; 22: 311-338.
15. Alonso LC, Yokoe T, Zhang P et al. Glucose infusion in mice: a new model to induce beta-cell replication. Diabetes 2007; 56: 1792-1801.
16. Georgia S, Bhushan A. Beta cell replication is the primary mechanism for maintaining postnatal beta cell mass. J Clin Invest 2004; 114: 963-968.
17. Levitt HE, Cyphert TJ, Pascoe JL et al. Glucose stimulates human beta cell replication in vivo in islets transplanted into NOD-severe combined immunodeficiency (SCID) mice. Diabetologia 2011; 54: 572-582.
18. Parsons JA, Brelje TC, Sorenson RL. Adaptation of islets of Langerhans to pregnancy: increased islet cell proliferation and insulin secretion correlates with the onset of placental lactogen secretion. Endocrinology 1992; 130: 1459-1466.
19. In't Veld P, Lievens D, De Grijse J et al. Screening for insulitis in adult autoantibody-positive organ donors. Diabetes 2007; 56: 2400-2404.
20. Meier JJ, Lin JC, Butler AE, Galasso R, Martinez DS, Butler PC. Direct evidence of attempted beta cell regeneration in an 89-year-old patient with recent-onset type 1 diabetes. Diabetologia 2006; 49: 1838-1844.
21. Aly H, Gottlieb P. The honeymoon phase: intersection of metabolism and immunology. Curr Opin Endocrinol Diabetes Obes 2009; 16: 286-292.
22. Xu X, D'Hoker J, Stange G et al. Beta cells can be generated from endogenous progenitors in injured adult mouse pancreas. Cell 2008; 132: 197-207.
23. Thorel F, Nepote V, Avril I et al. Conversion of adult pancreatic alpha-cells to beta-cells after extreme beta-cell loss. Nature 2010; 464: 1149-1154.
24. Basta G, Racanicchi L, Mancuso F et al. Transdifferentiation molecular pathways of neonatal pig pancreatic duct cells into endocrine cell phenotypes. Transplant Proc 2004; 36: 2857-2863.
25. Bonner-Weir S, Taneja M, Weir GC et al. In vitro cultivation of human islets from expanded ductal tissue. Proc Natl Acad Sci USA 2000; 97: 7999-8004.
26. Liu T, Wang CY, Yu F et al. In vitro pancreas duodenal homeobox-1 enhances the differentiation of pancreatic ductal epithelial cells into insulin-producing cells. World J Gastroenterol 2007; 13: 5232-5237.
27. Anastasi E, Ponte E, Gradini R et al. Expression of Reg and cytokeratin 20 during ductal cell differentiation and proliferation in a mouse model of autoimmune diabetes. Eur J Endocrinol 1999; 141: 644-652.
28. Higuchi Y, Herrera P, Muniesa P et al. Expression of a tumor necrosis factor alpha transgene in murine pancreatic beta cells results in severe and permanent insulitis without evolution towards diabetes. J Exp Med 1992; 176: 1719-1731.
29. Gu D, Arnush M, Sawyer SP, Sarvetnick N. Transgenic mice expressing IFN-gamma in pancreatic beta-cells are resistant to streptozotocin-induced diabetes. Am J Physiol 1995; 269: E1089-1094.
30. Kritzik MR, Jones E, Chen Z et al. PDX-1 and Msx-2 expression in the regenerating and developing pancreas. J Endocrinol 1999; 163: 523-530.
31. Rankin MM, Wilbur CJ, Rak K, Shields EJ, Granger A, Kushner JA. Beta-cells are not generated in pancreatic duct ligation-induced injury in adult mice. Diabetes 2013; 62: 1634-1645.
32. Gu G, Dubauskaite J, Melton DA. Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 2002; 129: 2447-2457.
33. Bonner-Weir S, Inada A, Yatoh S et al. Transdifferentiation of pancreatic ductal cells to endocrine beta-cells. Biochem Soc Trans 2008; 36: 353-356.
34. Solar M, Cardalda C, Houbracken I et al. Pancreatic exocrine duct cells give rise to insulin-producing beta cells during embryogenesis but not after birth. Dev Cell 2009; 17: 849-860.
35. Tanaka S, Kobayashi T, Nakanishi K et al. Evidence of primary beta-cell destruction by T-cells and beta-cell differentiation from pancreatic ductal cells in diabetes associated with active autoimmune chronic pancreatitis. Diabetes Care 2001; 24: 1661-1667.
36. Martin-Pagola A, Sisino G, Allende G et al. Insulin protein and proliferation in ductal cells in the transplanted pancreas of patients with type 1 diabetes and recurrence of autoimmunity. Diabetologia 2008; 51: 1803-1813.
37. Bogdani M, Lefebvre V, Buelens N et al. Formation of insulin-positive cells in implants of human pancreatic duct cell preparations from young donors. Diabetologia 2003; 46: 830-838.
38. Okuno M, Minami K, Okumachi A et al. Generation of insulin-secreting cells from pancreatic acinar cells of animal models of type 1 diabetes. Am J Physiol Endocrinol Metab 2007; 292: E158-165.
39. Minami K, Okuno M, Miyawaki K et al. Lineage tracing and characterization of insulin-secreting cells generated from adult pancreatic acinar cells. Proc Natl Acad Sci USA 2005; 102: 15116-15121.
40. Lardon J, Huyens N, Rooman I, Bouwens L. Exocrine cell transdifferentiation in dexamethasone-treated rat pancreas. Virchows Arch 2004; 444: 61-65.
41. Topp BG, McArthur MD, Finegood DT. Metabolic adaptations to chronic glucose infusion in rats. Diabetologia 2004; 47: 1602-1610.
42. Lipsett M, Finegood DT. Beta-cell neogenesis during prolonged hyperglycemia in rats. Diabetes 2002; 51: 1834-1841.
43. Desai BM, Oliver-Krasinski J, De Leon DD et al. Preexisting pancreatic acinar cells contribute to acinar cell, but not islet beta cell, regeneration. J Clin Invest 2007; 117: 971-977.
44. Zhou Q, Brown J, Kanarek A, Rajagopal J, Melton DA. In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 2008; 455: 627-632.
45. Gosmain Y, Marthinet E, Cheyssac C et al. Pax6 controls the expression of critical genes involved in pancreatic α cell differentiation and function. J Biol Chem 2010; 285: 33381-33393.
46. Fomina-Yadlin D, Kubicek S, Vetere A, He KH, Schreiber SL, Wagner BK. GW8510 increases insulin expression in pancreatic alpha cells through activation of p53 transcriptional activity. PLoS One 2012; 7: e28808.
47. Collombat P, Xu X, Ravassard P et al. The ectopic expression of Pax4 in the mouse pancreas converts progenitor cells into alpha and subsequently beta cells. Cell 2009; 138: 449-462.
48. Yang YP, Thorel F, Boyer DF, Herrera PL, Wright CV. Context-specific alpha- to-beta-cell reprogramming by forced Pdx1 expression. Genes Dev 2011; 25: 1680-1685.
49. 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: 1630-1638.
50. Chung CH, Levine F. Adult pancreatic alpha-cells: a new source of cells for beta-cell regeneration. Rev Diabet Stud 2010; 7: 124-131.
51. Friedrichsen BN, Neubauer N, Lee YC et al. Stimulation of pancreatic beta-cell replication by incretins involves transcriptional induction of cyclin D1 via multiple signalling pathways. J Endocrinol 2006; 188: 481-492.
52. Kwon DY, Kim YS, Ahn IS et al. Exendin-4 potentiates insulinotropic action partly via increasing beta-cell proliferation and neogenesis and decreasing apoptosis in association with the attenuation of endoplasmic reticulum stress in islets of diabetic rats. J Pharmacol Sci 2009; 111: 361-371.
53. Bulotta A, Hui H, Anastasi E et al. Cultured pancreatic ductal cells undergo cell cycle re-distribution and beta-cell-like differentiation in response to glucagon-like peptide-1. J Mol Endocrinol 2002; 29: 347-360.
54. Ogawa N, List JF, Habener JF, Maki T. Cure of overt diabetes in NOD mice by transient treatment with anti-lymphocyte serum and exendin-4. Diabetes 2004; 53: 1700-1705.
55. Sherry NA, Chen W, Kushner JA et al. Exendin-4 improves reversal of diabetes in NOD mice treated with anti-CD3 monoclonal antibody by enhancing recovery of beta-cells. Endocrinology 2007; 148: 5136-5144.
56. 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: 2270-2276.
57. Tian L, Gao J, Hao J et al. Reversal of new-onset diabetes through modulating inflammation and stimulating beta-cell replication in nonobese diabetic mice by a dipeptidyl peptidase IV inhibitor. Endocrinology 2010; 151: 3049-3060.
58. Rolin B, Larsen MO, Gotfredsen CF et al. The long-acting GLP-1 derivative NN2211 ameliorates glycemia and increases beta-cell mass in diabetic mice. Am J Physiol Endocrinol Metab 2002; 283: E745-752.
59. Suarez-Pinzon WL, Lakey JR, Rabinovitch A. Combination therapy with glucagon-like peptide-1 and gastrin induces beta-cell neogenesis from pancreatic duct cells in human islets transplanted in immunodeficient diabetic mice. Cell Transplant 2008; 17: 631-640.
60. Dupre J, Behme MT, McDonald TJ. Exendin-4 normalized postcibal glycemic excursions in type 1 diabetes. J Clin Endocrinol Metab 2004; 89: 3469-3473.
61. Raman VS, Mason KJ, Rodriguez LM et al. The role of adjunctive exenatide therapy in pediatric type 1 diabetes. Diabetes Care 2010; 33: 1294-1296.
62. Rother KI, Spain LM, Wesley RA et al. Effects of exenatide alone and in combination with daclizumab on beta-cell function in long-standing type 1 diabetes. Diabetes Care 2009; 32: 2251-2257.
63. Hari Kumar KV, Shaikh A, Prusty P. Addition of exenatide or sitagliptin to insulin in new onset type 1 diabetes: a randomized, open label study. Diabetes Res Clin Pract 2013; 100: e55-58.
64. Varanasi A, Bellini N, Rawal D et al. Liraglutide as additional treatment for type 1 diabetes. Eur J Endocrinol 2011; 165: 77-84.
65. Uzan B, Figeac F, Portha B, Movassat J. Mechanisms of KGF mediated signaling in pancreatic duct cell proliferation and differentiation. PLoS One 2009; 4: e4734.
66. Suarez-Pinzon WL, Lakey JR, Brand SJ, Rabinovitch A. Combination therapy with epidermal growth factor and gastrin induces neogenesis of human islet β-cells from pancreatic duct cells and an increase in functional β-cell mass. J Clin Endocrinol Metab 2005; 90: 3401-3409.
67. Wang M, Racine JJ, Song X et al. Mixed chimerism and growth factors augment beta cell regeneration and reverse late-stage type 1 diabetes. Sci Transl Med 2012; 4: 133ra59.
68. Oh YS, Shin S, Lee YJ, Kim EH, Jun HS. Betacellulin-induced beta cell proliferation and regeneration is mediated by activation of ErbB-1 and ErbB-2 receptors. PLoS One 2011; 6: e23894.
69. Mashima H, Ohnishi H, Wakabayashi K et al. Betacellulin and activin A coordinately convert amylase-secreting pancreatic AR42J cells into insulin-secreting cells. J Clin Invest 1996; 97: 1647-1654.
70. Gahr S, Merger M, Bollheimer LC, Hammerschmied CG, Scholmerich J, Hugl SR. Hepatocyte growth factor stimulates proliferation of pancreatic beta-cells particularly in the presence of subphysiological glucose concentrations. J Mol Endocrinol 2002; 28: 99-110.
71. Mashima H, Shibata H, Mine T, Kojima I. Formation of insulin-producing cells from pancreatic acinar AR42J cells by hepatocyte growth factor. Endocrinology 1996; 137: 3969-3976.
72. You YH, Ham DS, Park HS, Rhee M, Kim JW, Yoon KH. Adenoviruses expressing PDX-1, BETA2/NeuroD and MafA induces the transdifferentiation of porcine neonatal pancreas cell clusters and adult pig pancreatic cells into beta-cells. Diabetes Metab J 2011; 35: 119-129.
73. Noguchi H, Kaneto H, Weir GC, Bonner-Weir S. PDX-1 protein containing its own antennapedia-like protein transduction domain can transduce pancreatic duct and islet cells. Diabetes 2003; 52: 1732-1737.
74. Koya V, Lu S, Sun YP et al. Reversal of streptozotocin-induced diabetes in mice by cellular transduction with recombinant pancreatic transcription factor pancreatic duodenal homeobox-1: a novel protein transduction domain-based therapy. Diabetes 2008; 57: 757-769.
75. Chen S, Shimoda M, Wang MY et al. Regeneration of pancreatic islets in vivo by ultrasound-targeted gene therapy. Gene Ther 2010; 17: 1411-1420.