Distinctions between islet neogenesis and β-cell replication: Implications for reversal of Type 1 and 2 diabetes

Journal of Diabetes

Volumn 2, Issue 2, 2010, Pages 76-84

  Levetan, Claresa ^a  

^a Delaware Valley Nephrology and Hypertension   (United States)

Author keywords

cell replication; Islet neogenesis; Reversal therapy

Indexed keywords

ANTIDIABETIC AGENT; GLUCOSE; NEUROGENIC DIFFERENTIATION FACTOR; NEUROGENIN 3; PLACEBO; PROTEIN REG; PROTEIN REG3A; TRANSCRIPTION FACTOR MAFA; TRANSCRIPTION FACTOR NKX2.2; TRANSCRIPTION FACTOR PAX4; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR PDX 1; UNCLASSIFIED DRUG;

APOPTOSIS; CELL DIVISION; DISEASE COURSE; DRUG SCREENING; FETUS DEVELOPMENT; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GESTATION PERIOD; GLUCOSE TOLERANCE; HUMAN; HYPOGLYCEMIA; IMMUNOLOGICAL TOLERANCE; INSULIN DEPENDENT DIABETES MELLITUS; LIFESTYLE MODIFICATION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; REVIEW; STEM CELL; TISSUE REGENERATION;

ADULT; BLOOD GLUCOSE; CELL DIVISION; CHILD; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; GENE EXPRESSION REGULATION; GHRELIN; HOMEOSTASIS; HUMANS; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; LITHOSTATHINE; PANCREAS; PANCREATIC DUCTS; REFERENCE VALUES; REGENERATION; TRANSCRIPTION FACTORS;

EID: 77953372197     PISSN: 17530393     EISSN: 17530407     Source Type: Journal    
DOI: 10.1111/j.1753-0407.2010.00074.x     Document Type: Review

References (89)

1. Andralojc KM, Mercalli A, Nowak KW et al. Ghrelin-producing epsilon cells in the developing and adult human pancreas. Diabetologia. 2009 52 : 486 493.
2. Holdstock C, Ludvigsson J, Karlsson FA. Abnormal ghrelin secretion in new onset childhood Type 1 diabetes. Diabetologia. 2004 47 : 150 151.
3. Togliatto G, Trombetta A, Dentelli P et al. Unacylated ghrelin rescues endothelial progenitor cell function in individuals with Type 2 diabetes. Diabetes. 2010 59 : 1016 1025.
4. Granata R, Settanni F, Biancone L et al. Acylated and unacylated ghrelin promote proliferation and inhibit apoptosis of pancreatic beta-cells and human islets: involvement of 3′,5′-cyclic adenosine monophosphate/protein kinase A, extracellular signal-regulated kinase 1/2, and phosphatidyl inositol 3-Kinase/Akt signaling. Endocrinology. 2007 148 : 512 529.
5. Hellman B, Salehi A, Gylfe E et al. Glucose generates coincident insulin and somatostatin pulses andantisynchronous glucagon pulses from human pancreatic islets. Endocrinology. 2009 150 : 5334 5340.
6. Stefan Y, Grasso S, Perrelet A, Orci L. A quantitative immunofluorescent study of the endocrine cell populations in the developing human pancreas. Diabetes. 1983 32 : 293 301.
7. De Krijgar RR, Aanstoot HJ, Kranenburg G et al. The midgestational human fetal pancreas contains cells coexpressing islet hormones. Dev Biol. 1992 153 : 368 375.
8. Fowden AL, Hill DJ. Intra-uterine programming of the endocrine pancreas. Br Med Bull. 2001 60 : 123 142.
9. Defronzo RA. Banting Lecture. From the triumvirate to the ominous octet: a new paradigm for the treatment of Type 2 diabetes mellitus. Diabetes. 2009 58 : 773 795.
10. Doniach I, Morgan AG. Islets of Langerhans in juvenile diabetes mellitus. Clin Endocrinol. 1973 2 : 233 248.
11. Deng S, Vatamaniuk M, Huang X et al. Structural and functional abnormalities in the islets isolated from Type 2 diabetic subjects. Diabetes. 2004 53 : 624 632.
12. Barron M. The relation of the islets of Langerhans to diabetes with special reference to cases of pancreatic lithiasis. Surg Gynecol Obstet. 1920 19 : 437 448.
13. Banting FG, Best CH. Pancreatic extracts. J Lab Clin Med. 1922 7 : 464 472.
14. DeTakats G. Ligation of the tail of the pancreas in juvenile diabetes. Endocrinology. 1930 14 : 255 264.
15. Gymr V, Kerr-Conte J, Belaich S et al. Newly updated Laguesse's theory of balance: neogenesis of pancreatic beta cells via acinar transdifferentiation in adult human. Pancreatology. 2001 1 : 144 (Abstract).
16. Laguesse E. Pancreas's structure and development from recent works. J Anat Phys. 1894 30 : 591 731.
17. 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.
18. 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.
19. Nir T, Melton DA, Dor Y. Recovery from diabetes in mice by beta cell regeneration. J Clin Invest. 2007 117 : 2553 2561.
20. Bonner-Weir S. Islet growth and development in the adult. J Mol Endocrinol. 2000 24 : 297 302.
21. Bonner-Weir S, Toschi E, Inada A et al. The pancreatic ductal epithelium serves as a potential pool of progenitor cells. Pediatr Diabetes. 2004 5 : 16 22.
22. Davani BL, Ikonomou L, Raaka BM et al. Human islet-derived precursor cells are mesenchymal stromal cells that differentiate and mature to hormone-expression cells in vivo. Stem Cells. 2007 25 : 3215 3222.
23. D'Alessandro JS, Lu K, Fung BP et al. Rapid and efficient in vitro generation of pancreatic islet progenitor cells from nonendocrine epithelial cells in the adult human pancreas. Stem Cells Dev. 2007 16 : 75 89.
24. Parenteau NJ, Rosenberg L, Hardin-Young J. The engineering of tissues using progenitor cells. Curr Top Dev Biol. 2004 64 : 101 137.
25. Baertschiger RM, Bosco D, Morel P et al. Mesenchymal stem cells derived from human exocrine pancreas express transcription factors implicated in beta-cell development. Pancreas. 2008 37 : 75 84.
26. Dusetti NJ, Frigerio JM, Fox MF et al. Molecular cloning, genomic organization, and chromosomal localization of the human pancreatitis-associated protein (PAP) gene. Genomics. 1994 19 : 108 114.
27. Orelle B, Keim V, Masciotra L et al. Human pancreatitis-associated protein. Messenger RNA cloning and expression in pancreatic diseases. J Clin Invest. 1992 90 : 2284 2291.
28. Graf R, Schiesser M, Reding T et al. Exocrine meets endocrine: pancreatic stone protein and regenerating protein: two sides of the same coin. J Surg Res. 2006 133 : 113 120.
29. Bonner-Weir S, Baxter LA, Schuppin GT, Smith FE. A second pathway for regeneration of adult exocrine and endocrine pancreas. A possible recapitulation of embryonic development. Diabetes. 1993 42 : 1715 1720.
30. Fernandes A, King LC, Guz Y et al. Differentiation of new insulin-producing cells is induced by injury in adult pancreatic islets. Endocrinology. 1997 138 : 1750 1762.
31. Xu X, D'Hoker J, Stangé G et al. Beta cells can be generated from endogenous progenitors in injured adult mouse pancreas. Cell. 2008 132 : 197 207.
32. Hardikar AA, Karandikar MS, Bhonde RR. Effect of partial pancreatectomy on diabetic status in BALB/c mice. J Endocrinol. 1999 162 : 189 195.
33. Rosenberg L, Vinik AI, Pittenger GL et al. Islet-cell regeneration in the diabetic hamster pancreas with restoration of normoglycaemia can be induced by a local growth factor(s). Diabetologia. 1996 39 : 256 262.
34. Johansson M, Mattsson G, Andersson A et al. Islet endothelial cells and pancreatic beta-cell proliferation: Studies in vitro and during pregnancy in adult rats. Endocrinology. 2006 147 : 2315 2324.
35. Percival AC, Slack JM. Analysis of pancreatic development using a cell lineage label. Exp Cell Res. 1999 247 : 123 132.
36. Inada A, Nienaber C, Katsuta H et al. Carbonic anhydrase II-positive pancreatic cells are progenitors for both endocrine and exocrine pancreas after birth. Proc Natl Acad Sci USA. 2008 105 : 19915 19919.
37. 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.
38. White P, May CL, Lamounier RN et al. Defining pancreatic endocrine precursors and their descendants. Diabetes. 2008 57 : 654 668.
39. Wilson ME, Scheel D, German MS. Gene expression cascades in pancreatic development. Mech Dev. 2003 120 : 65 80.
40. Habener JF, Kemp DM, Thomas MK. Minireview: transcriptional regulation in pancreatic development. Endocrinology. 2005 146 : 1025 1034.
41. Kaneto H, Matsuoka TA, Miyatsuka T et al. PDX-1 functions as a master factor in the pancreas. Front Biosci. 2008 13 : 6406 6420.
42. Habener JF, Stoffers DA. A newly discovered role of transcription factors involved in pancreas development and the pathogenesis of diabetes mellitus. Proc Assoc Am Physicians. 1998 110 : 12 21.
43. Stoffers DA, Thomas MK, Habener JF. Homeodomain protein IDX-1: a master regulator of pancreas development and insulin gene expression. Trends Endocrinol Metab. 1997 8 : 145 151.
44. Abe M, Nata K, Akiyama T et al. Identification of a novel Reg family gene, Reg III delta, and mapping of all three types of Reg family gene in a 75 kilobase mouse genomic region. Gene. 2000 246 : 111 122.
45. Zenilman ME, Perfetti R, Swinson K et al. Pancreatic regeneration (reg) gene expression in a rat model of islet hyperplasia. Surgery. 1996 119 : 576 584.
46. Castellarin ML, Petropavlovskaia M, Lipsett MA, Rosenberg L. The identification and sequence analysis of a new Reg3gamma and Reg2 in the Syrian golden hamster. Biochim Biophys Acta. 2007 1769 : 579 585.
47. Nata K, Liu Y, Xu L et al. Molecular cloning, expression and chromosomal localization of a novel human REG family gene, REG III. Gene. 2004 340 : 161 170.
48. Hamblet NS, Shi W, Vinik AI, Taylor-Fishwick DA The Reg family member INGAP is a marker of endocrine patterning in the embryonic pancreas. Pancreas. 2008 36 : 1 9.
49. Liu JL, Cui W, Li B, Lu Y. Possible roles of reg family proteins in pancreatic islet cell growth. Endocr Metab Immune Disord Drug Targets. 2008 8 : 1 10.
50. Mouse Genomics Informatics Mus musculus 11 Days Pregnant Adult Female Ovary and Uterus cDNA, RIKEN Full-Length Enriched Library, Clone: 5033401N17, Product: Regenerating Islet-Derived 1, Full Insert Sequence. Available from: http://www.ebi.ac.uk/cgi-bin/emblfetch?AK133506 (accessed 17 December 2007).
51. Taylor-Fishwick DA, Shi W, Hughes L, Vinik A. Pdx-1 regulation of the INGAP promoter involves sequestration of NeuroD into a non-DNA-binding complex. Pancreas. 2010 39 : 64 70.
52. Anderson KR, White P, Kaestner KH, Lori Sussel L. Identification of known and novel pancreas genes expressed downstream of Nkx2.2 during development. BMC Dev Biol. 2009 9 : 65.
53. Francini F, Del Zotto H, Massa ML, Gagliardino JJ. Selective effect of INGAP-PP upon mouse embryonic stem cell differentiation toward islet cells. Regul Pept. 2009 153 : 43 8.
54. 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.
55. Kaneto H, Matsuoka TA, Katakami N, Matsuhisa M. Combination of MafA, PDX-1 and NeuroD is a useful tool to efficiently induce insulin-producing surrogate beta-cells. Curr Med Chem. 2009 16 : 3144 3151.
56. Terazono K, Yamamoto H, Takasawa S et al. A novel gene activated in regenerating islets. J Biol Chem. 1988 263 : 2111 2114.
57. Vukkadapu SS, Belli JM, Ishii K et al. Dynamic interaction between T cell-mediated β-cell damage and β-cell repair in the run up to autoimmune diabetes of the NOD mouse. Physiol Genomics. 2005 21 : 201 211.
58. Sanchez D, Baeza N, Blouin R et al. Overexpression of the reg gene in non-obese diabetic mouse pancreas during active diabetogenesis is restricted to exocrine tissue. J Histochem Cytochem. 2000 48 : 1401 1410.
59. Baeza N, Sanchez D, Christa L et al. Pancreatitis-associated protein (HIP/PAP) gene expression is upregulated in NOD mice pancreas and localized in exocrine tissue during diabetes. Digestion. 2001 64 : 233 239.
60. Planas R, Alba A, Carrillo J et al. Reg (regenerating) gene overexpression in islets from non-obese diabetic mice with accelerated diabetes: role of IFNbeta. Diabetologia. 2006 49 : 2379 2387.
61. Smith FE, Bonner-Weir S, Leahy JL et al. Pancreattic Reg/pancreatic stone protein (PSP) gene expression does not correlate with beta-cell growth and regeneration in rats. Diabetologia. 1994 37 : 994 999.
62. Gurr W, Yavari R, Wen L et al. A Reg family protein is overexpressed in islets from a patient with new-onset Type 1 diabetes and acts as T-cell autoantigen in NOD mice. Diabetes. 2002 51 : 339 346.
63. Viterbo D, Callender GE, DiMaio T et al. Administration of anti-Reg antibodies worsens pancreatitis. JOP. 2009 10 : 15 23.
64. Watanabe T, Yonekura H, Terazono K et al. Complete nucleotide sequence of human reg gene and its expression in normal and tumoral tissues. The reg protein, pancreatic stone protein, and pancreatic thread protein are one and the same product of the gene. J Biol Chem. 1990 265 : 7432 7439.
65. Zenilman ME, Chen J, Magnuson TH. Effect of reg protein on rat pancreatic ductal cells. Pancreas. 1998 17 : 256 261.
66. Rosenberg L, Lipsett M, Yoon JW et al. A pentadecapeptide fragment of islet neogenesis-associated protein increases beta-cell mass and reverses diabetes in C57BL/6J mice. Ann Surg. 2004 240 : 875 884.
67. Rosenberg L, Duguid WP, Healy M et al. Reversal of diabetes by the induction of islet cell neogenesis. Transplant Proc. 1992 24 : 1027 1028.
68. Levetan CS, Upham LV, Deng S et al. Discovery of a human peptide sequence signaling islet neogenesis. Endocr Pract. 2008 14 : 1075 1083.
69. Guillemain G, Filhoulaud G, Da Silva-Xavier G et al. Glucose is necessary for embryonic pancreatic endocrine cell differentiation. J Biol Chem. 2007 282 : 15228 15237.
70. Jorns A, Klempnauer J, Tiedge M, Lenzen S. Recovery of pancreatic beta cells in response to long-term normoglycemia after pancreas or islet transplantation in severely streptozotocin diabetic adult rats. Pancreas. 2001 23 : 186 196.
71. Ryu S, Shohta K, Kazuko R et al. Reversal of established autoimmune diabetes by restoration of endogenous β cell function. J Clin Invest. 2001 108 : 63 72.
72. Miyaura C, Chen L, Appel M et al. Expression of reg/PSP, a pancreatic exocrine gene: relationship to changes in islet beta-cell mass. Mol Endocrinol. 1991 5 : 226 234.
73. Jovanovic L, Knopp RH, Brown Z et al. National Institute of Child Health and Human Development. Diabetes in Early Pregnancy Study Group. Declining insulin requirement in the late first trimester of diabetic pregnancy. Diabetes Care. 2001 24 : 1130 1136.
74. Ilic S, Jovanovic L, Wollitzer AO. Is the paradoxical first trimester drop in insulin requirement due to an increase in C-peptide concentration in pregnant Type I diabetic women? Diabetologia. 2000 43 : 1329 1330.
75. Rigg L, Cousins L, Hollingsworth D et al. Effects of exogenous insulin on excursions and diurnal rhythm of plasma glucose in pregnant diabetic patients with and without residual beta-cell function. Am J Obstet Gynecol. 1980 136 : 537 544.
76. Lewis SB, Wallin JD, Kuzuya H et al. Circadian variation of serum glucose, C-peptide immunoreactivity and free insulin normal and insulin-treated diabetic pregnant subjects. Diabetologia. 1976 12 : 343 350.
77. Teta M, Rankin MM, Long SY et al. Growth and regeneration of adult beta cells does not involve specialized progenitors. Dev Cell. 2007 12 : 817 826.
78. Diamyd Medical. Press Release: diamyd Announces Completion of Type 1 Diabetes Vaccine Trial With Long Term Efficacy Demonstrated at 30 Months. 2008. Available from http://www.diamyd.com/docs/pressClip.aspx?section= investor&clipid=420 (accessed 14 January 2010).
79. Herold KC, Gitelman S, Greenbaum C et al. Treatment of patients with new onset Type 1 diabetes with a single course of anti-CD3 mAb Teplizumab preserves insulin production for up to 5 years. Clin Immunol. 2009 132 : 166 173.
80. Keymeulen B, Walter M, Mathieu C et al. Four-year metabolic outcome of a randomised controlled CD3-antibody trial in recent-onset Type 1 diabetic patients depends on their age and baseline residual beta cell mass. Diabetologia. 2010 53 : 614 623.
81. Knowler WC, Barrett-Connor E, Fowler SE et al. Diabetes Prevention Program Research Group. Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N Engl J Med. 2002 346 : 393 403.
82. Tuomilehto J. Nonpharmacologic therapy and exercise in the prevention of Type 2 diabetes. Diabetes Care. 2009 32 (Suppl. 2 S189 93.
83. Pan XR, Li GW, Hu YH et al. Effects of diet and exercise in preventing NIDDM in people with impaired glucose tolerance. The Da Qing IGT and Diabetes Study. Diabetes Care. 1997 20 : 537 544.
84. Elias D, Avron A, Tamir M, Raz I. DiaPep277 preserves endogenous insulin production by immunomodulation in Type 1 diabetes. Ann N Y Acad Sci. 2006 1079 : 340 344.
85. Ludvigsson J, Faresjö M, Hjorth M et al. GAD treatment and insulin secretion in recent-onset Type 1 diabetes. N Engl J Med. 2008 359 : 1909 1920.
86. Zerhouni P, Casas R. GAD treatment and insulin secretion in recent-onset Type 1 diabetes. N Engl J Med. 2008 359 : 1909 1920.
87. Raz I, Elias D, Avron A et al. Beta-cell function in new-onset Type 1 diabetes and immunomodulation with a heat-shock protein peptide (DiaPep277): a randomised, double-blind, phase II trial. Lancet. 2001 358 : 1749 1753.
88. Eisenbarth GS, Srikanta S, Jackson R et al. Anti-thymocyte globulin and prednisone immunotherapy of recent onset Type 1 diabetes mellitus. Diabetes Res. 1985 2 : 271 276.
89. Morgan NG. Fatty acids and beta-cell toxicity. Curr Opin Clin Nutr Metab Care. 2009 12 : 117 122.