β-cell growth and regeneration: Replication is only part of the story

Diabetes

Volumn 59, Issue 10, 2010, Pages 2340-2348

  Bonner Weir, Susan ^a   Li, Wan Chun ^a   Ouziel Yahalom, Limor ^a   Guo, Lili ^a   Weir, Gordon C ^a   Sharma, Arun ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLASE; CARBONATE DEHYDRATASE II; EXENDIN 4; GLUCAGON LIKE PEPTIDE 1; INSULIN; SOYBEAN TRYPSIN INHIBITOR; TRANSCRIPTION FACTOR PAX4; TRANSCRIPTION FACTOR PDX 1; TRANSFORMING GROWTH FACTOR ALPHA; UVOMORULIN;

APOPTOSIS; CELL DIVISION; CELL GROWTH; CELL PROLIFERATION; CELL REGENERATION; NEWBORN PERIOD; NONHUMAN; PANCREAS DUCT LIGATION; PANCREAS ISLET BETA CELL; PANCREAS RESECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

ADULT; ANIMALS; CELL DIVISION; CELL PROLIFERATION; HUMANS; INSULIN-SECRETING CELLS; MICE; PANCREAS; RATS; REGENERATION; SWINE;

EID: 77957606887     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db10-0084     Document Type: Review

References (96)

1. Granger A, Kushner JA. Cellular origins of beta-cell regeneration: a legacy view of historical controversies. J Intern Med 2009;266:325-338
2. Bonner-Weir S. Perspective: postnatal pancreatic beta cell growth. Endocrinology 2000;141:1926-1929
3. Bouwens L, Rooman I. Regulation of pancreatic beta-cell mass. Physiol Rev 2005;85:1255-1270
4. Bonner-Weir S. Regulation of pancreatic β-cell mass in vivo. Recent Prog Horm Res 1994;49:91-104
5. Finegood DT, Scaglia L, Bonner-Weir S. Dynamics of β-cell mass in the growing rat pancreas: estimation with a simple mathematical model. Diabetes 1995;44:249-256
6. Scaglia L, Cahill CJ, Finegood DT, Bonner-Weir S. Apoptosis participates in the remodeling of the endocrine pancreas in the neonatal rat. Endocrinol 1997;138:1736-1741
7. Montanya E, Nacher V, Biarnes M, Soler J. Linear correlation between beta cell mass and body weight throughout life in Lewis rats: role of β-cell hyperplasia and hypertrophy. Diabetes 2000;49:1341-1346
8. Xu G, Stoffers DA, Habener JF, Bonner-Weir S. Exendin-4 stimulates both β-cell replication and neogenesis, resulting in increased β-cell mass and improved glucose tolerance in diabetic rats. Diabetes 1999;48:2270-2276
9. Scaglia L, Smith FE, Bonner-Weir S. Apoptosis contributes to the involution of β cell mass in the post partum rat pancreas. Endocrinol 1995;136:5461-5468
10. Bonner-Weir S, Deery D, Leahy JL, Weir GC. Compensatory growth of pancreatic β-cells in adult rats after short-term glucose infusion. Diabetes 1989;38:49-53
11. 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
12. Parsons JA, Bartke A, Sorenson RL. Number and size of islets of langerhans in pregnant human growth hormone-expressing transgenic, and pituitary dwarf mice: effect of lactogenic hormones. Endocrinol 1995;136:2013-2021
13. Bock T, Pakkenberg B, Buschard K. Increased islet volume but unchanged islet number in ob/ob mice. Diabetes 2003;52:1716-1722
14. Larsen MO, Rolin B, Raun K, Bjerre Knudsen L, Gotfredsen CF, Bock T. Evaluation of beta-cell mass and function in the Gottingen minipig. Diabetes Obes Metab 2007;9(Suppl. 2):170-179
15. Butler AE, Cao-Minh L, Galasso R, Rizza RA, Corradin A, Cobelli C, Butler PC. Adaptive changes in pancreatic beta cell fractional area and beta cell turnover in human pregnancy. Diabetologia, 2010 [Epub ahead of print]
16. 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
17. Dor Y, Melton DA. Facultative endocrine progenitor cells in the adult pancreas. Cell 2008;132:183-184
18. Guo C, Yang W, Lobe CG. A Cre recombinase transgene with mosaic, widespread tamoxifen-inducible action. Genesis 2002;32:8-18
19. Xu X, D'Hoker J, Stange G, Bonne S, De Leu N, Xiao X, Van De Casteele M, Mellitzer G, Ling Z, Pipeleers D, Bouwens L, Scharfmann R, Gradwohl G, Heimberg H. Beta cells can be generated from endogenous progenitors in injured adult mouse pancreas. Cell 2008;132:197-207
20. Inada A, Nienaber C, Katsuta H, Fujitani Y, Levine J, Morita R, Sharma A, Bonner-Weir S. Carbonic anhydrase II-positive pancreatic cells are progenitors for both endocrine and exocrine pancreas after birth. Proc Natl Acad Sci U S A 2008;105:19915-19919
21. Bouwens L, Wang RN, De Blay E, Pipeleers DG, Kloppel G. Cytokeratins as markers of ductal cell differentiation and islet neogenesis in the neonatal rat pancreas. Diabetes 1994;43:1279-1283
22. Bonner-Weir S, Toschi E, Inada A, Reitz P, Fonseca SY, Aye T, Sharma A. The pancreatic ductal epithelium serves as a potential pool of progenitor cells. Ped Diabetes 2004;5:15-22
23. Inada A, Nienaber C, Fonseca S, Bonner-Weir S. Timing and expression pattern of carbonic anhydrase II in pancreas. Dev Dyn 2006;235:1571-1577
24. Solar M, Cardalda C, Houbracken I, Martin M, Maestro MA, De Medts N, Xu X, Grau V, Heimberg H, Bouwens L, Ferrer J. Pancreatic exocrine duct cells give rise to insulin-producing beta cells during embryogenesis but not after birth. Dev Cell 2009;17:849-860
25. Kopinke D, Murtaugh LC. Exocrine-to-endocrine differentiation is detectable only prior to birth in the uninjured mouse pancreas. BMC Dev Biol 2010;10:38
26. Peng SW, Zhu LY, Chen M, Zhang M, Li DZ, Fu YC, Chen SR, Wei CJ. Heterogeneity in mitotic activity and telomere length implies an important role of young islets in the maintenance of islet mass in the adult pancreas. Endocrinology 2009;150:3058-3066
27. Aye T, Toschi E, Sharma A, Sgroi D, Bonner-Weir S. Identification of markers for newly formed beta-cells in the perinatal period: a time of recognized beta-cell immaturity. J Histochem Cytochem 2010;58:369-376
28. Toschi EAT, Fuller A, Gaudet J, Sharma A, Weir GC, Sgroi D, Bonner-Weir S. Gene expression profiling of new b cells: evidence for differentiating β cells passing through a ductal phenotype. Diabetes 53, 2004
29. Yatoh S, Dodge R, Akashi T, Omer A, Sharma A, Weir GC, Bonner-Weir S. Differentiation of affinity-purified human pancreatic duct cells to β-cells. Diabetes 2007;56:1802-1809
30. Collombat P, Xu X, Ravassard P, Sosa-Pineda B, Dussaud S, Billestrup N, Madsen OD, Serup P, Heimberg H, Mansouri A. The ectopic expression of Pax4 in the mouse pancreas converts progenitor cells into alpha and subsequently beta cells. Cell 2009;138:449-462
31. Bonner-Weir S, Baxter LA, Schuppin GT, Smith FE. A second pathway for regeneration of the adult exocrine and endocrine pancreas: a possible recapitulation of embryonic development. Diabetes 1993;42:1715-1720
32. Wang RN, Kloppel G, Bouwens L. Duct- to islet-cell differentiation and islet growth in the pancreas of duct-ligated adult rats. Diabetologia 1995;38:1405-1411
33. Weaver CV, Sorenson RL, Kaung HC. Immunocytochemical localization of insulin-immunoreactive cells in the ducts of rats treated with trypsin inhibitor. Diabetologia 1985;28:781-785
34. Waguri M, Yamamoto K, Miyagawa Ji, Tochino Y, Yamamori K, Kajimoto Y, Nakajima H, Watada H, Yoshiuchi I, Itoh N, Imagawa A, Namba M, Kuwajima M, Yamasaki Y, Hanfusa T, Matsuzawa Y. Demonstration of two different processes of β-cell regeneration in a new diabetic mouse model induced by selective perfusion of alloxan. Diabetes 1997;46:1281-1290
35. Rosenberg L, Duguid WP, Vinik AI. The effect of cellophane wrapping of the pancreas in the Syrian golden hamster: autoradiographic observations. Pancreas 1989;4:31-37
36. Gu D, Sarvetnick N. Epithelial cell proliferation and islet neogenesis in IFN-γ transgenic mice. Development 1993;118:33-46
37. Wang TC, Bonner-Weir S, Oates PS, Chulak M, Simon B, Merlino GT, Schmidt EV, Brand SJ. Pancreatic gastrin stimulates islet differentiation of transforming growth factor alpha-induced ductular precursor cells. J Clin Invest 1993;92:1349-1356
38. Bonner-Weir S, Trent DF, Weir GC. Partial pancreatectomy in the rat and subsequent defect in glucose-induced insulin release. J Clin Invest 1983;71:1544-1553
39. Brockenbrough JS, Weir GC, Bonner-Weir S. Discordance of exocrine and endocrine growth after 90% pancreatectomy in rats. Diabetes 1988;37:232-236
40. Li WC, Rukstalis JM, Nishimura W, Tchipashvili V, Habener JF, Sharma A, Bonner-Weir S. Activation of pancreatic duct-derived progenitor cells during pancreatic regeneration in adult rats. J Cell Science 2010;123:2792-2802
41. Sharma A, Zangen GH, Reitz P, Taneja M, Lissauer ME, Miller CP, Weir GC, Habener JF, Bonner-Weir S. The homeodomain protein IDX-1 increases after an early burst of proliferation during pancreatic regeneration. Diabetes 1999;48:507-513
42. Bonner-Weir S, Stubbs M, Reitz P, Taneja M, Smith FE. Partial pancreatectomy as a model of pancreatic regeneration. In Pancreas regeneration. Sarvetnick N, Ed. Karger Landes Systems, 1997, p. 138-153
43. Bonner-Weir S, Leahy JL, Weir GC. Induced rat models of non-insulin-dependent diabetes mellitus. In Lessons From Animal Diabetes II. Shapiro E, Renold AE, Eds. London, John Libbey, 1988, p. 295-300
44. Jetton TL, Lausier J, LaRock K, Trotman WE, Larmie B, Habibovic A, Peshavaria M, Leahy JL. Mechanisms of compensatory β-cell growth in insulin-resistant rats: roles of Akt kinase. Diabetes 2005;54:2294-2304
45. Lee CS, De Leon DD, Kaestner KH, Stoffers DA. Regeneration of pancreatic islets after partial pancreatectomy in mice does not involve the reactivation of neurogenin-3. Diabetes 2006;55:269-272
46. Peshavaria M, Larmie BL, Lausier J, Satish B, Habibovic A, Roskens V, Larock K, Everill B, Leahy JL, Jetton TL. Regulation of pancreatic beta-cell regeneration in the normoglycemic 60% partial-pancreatectomy mouse. Diabetes 2006;55:3289-3298
47. Ackermann Misfeldt A, Costa RH, Gannon M. β-Cell proliferation, but not neogenesis, following 60% partial pancreatectomy is impaired in the absence of FoxM1. Diabetes 2008;57:3069-3077
48. Guo L, Li WC, Pittenger G, Fishwick-Taylor D, Vinik AI, Bonner-Weir S. Pancreatic regeneration after partial pancreatectomy (Px) in mice mirrors that in rats with both enhanced replication and neogenesis. Diabetes 2010;59(Suppl. 1):A676
49. Hultquist GT, Karlsson U, Hallner AC. The regenerative capacity of the pancreas in duct-ligated rats. Exp Pathol 1979;17:44-52
50. Edstrom C. Further quantitative structural studies of the pancreatic islet parenchyma in rats with duct ligation. Acta Soc Med Uppsala 1971;76:127-138
51. Lardon J, Huyens N, Rooman I, Bouwens L. Exocrine cell transdifferentiation in dexamethasone-treated rat pancreas. Virchows Arch 2004;444:61-65
52. Rooman I, Lardon J, Bouwens L. Gastrin stimulates β-cell neogenesis and increases islet mass from transdifferentiated but not from normal exocrine pancreas tissue. Diabetes 2002;51:686-690
53. Desai BM, Oliver-Krasinski J, De Leon DD, Farzad C, Hong N, Leach SD, Stoffers DA. Preexisting pancreatic acinar cells contribute to acinar cell, but not islet beta cell, regeneration. J Clin Invest 2007;117:971-977
54. Sarvetnick NE, Gu D. Regeneration of pancreatic endocrine cells in interferon-gamma transgenic mice. Adv Exp Med Biol 1992;321:85-89
55. Kritzik MR, Krahl T, Good A, Krakowski M, St-Onge L, Gruss P, Wright C, Sarvetnick N. Transcription factor expression during pancreatic islet regeneration. Mol Cell Endocrinol 2000;164:99-107 (Pubitemid 30665504)
56. Kritzik MR, Jones E, Chen Z, Krakowski M, Krahl T, Good A, Wright C, Fox H, Sarvetnick N. PDX-1 and Msx-2 expression in the regenerating and developing pancreas. J Endocrinol 1999;163:523-530
57. Jhappan C, Stahle C, Harkins RN, Fausto N, Smith GH, Merlino GT. TGFa overexpression in transgenic mice induces liver neoplasia and abnormal development of the mammary gland and pancreas. Cell 1990;61:1137-1146
58. Song SY, Gannon M, Washington MK, Scoggins CR, Meszoely IM, Goldenring JR, Marino CR, Sandgren EP, Coffey RJ Jr, Wright CV, Leach SD. Expansion of Pdx1-expressing pancreatic epithelium and islet neogenesis in transgenic mice overexpressing transforming growth factor alpha. Gastroenterology 1999;117:1416-1426
59. Bruning JC, Winnay J, Bonner-Weir S, Taylor SI, Accili D, Kahn CR. Development of a novel polygenic model of NIDDM in mice heterozygous for IR and IRS-1 null alleles. Cell 1999;88:561-572
60. Kloppel G, Lohr M, Habich K, Oberholzer M, Heitz PU. Islet pathology and the pathogenesis of type 1 and type 2 diabetes mellitus revisited. Surv Synth Pathol Res 1985;4:110-125
61. Rahier J, Guiot Y, Goebbels RM, Sempoux C, Henquin JC. Pancreatic beta-cell mass in European subjects with type 2 diabetes. Diabetes Obes Metab 2008;10(Suppl. 4):32-42
62. Meier JJ, Butler AE, Saisho Y, Monchamp T, Galasso R, Bhushan A, Rizza RA, Butler PC. β-Cell replication is the primary mechanism subserving the postnatal expansion of β-cell mass in humans. Diabetes 2008;57:1584-1594
63. Tyrberg B, Ustinov J, Otonkoski T, Andersson A. Stimulated endocrine cell proliferation and differentiation in transplanted human pancreatic islets: effects of the ob gene and compensatory growth of the implantation organ. Diabetes 2001;50:301-307
64. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. β-Cell deficit and increased β-cell apoptosis in humans with type 2 diabetes. Diabetes 2003;52:102-110
65. Reers C, Erbel S, Esposito I, Schmied B, Buchler MW, Nawroth PP, Ritzel RA. Impaired islet turnover in human donor pancreata with aging. Eur J Endocrinol 2009;160:185-191
66. 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
67. Wright WE, Shay JW. Historical claims and current interpretations of replicative aging. Nat Biotechnol 2002;20:682-688
68. Forsyth NR, Wright WE, Shay JW. Telomerase and differentiation in multicellular organisms: turn it off, turn it on, and turn it off again. Differentiation 2002;69:188-197
69. Blasco MA, Lee HW, Hande MP, Samper E, Lansdorp PM, DePinho RA, Greider CW. Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 1997;91:25-34
70. Seluanov A, Chen Z, Hine C, Sasahara TH, Ribeiro AA, Catania KC, Presgraves DC, Gorbunova V. Telomerase activity coevolves with body mass not lifespan. Aging Cell 2007;6:45-52
71. Seluanov A, Hine C, Bozzella M, Hall A, Sasahara TH, Ribeiro AA, Catania KC, Presgraves DC, Gorbunova V. Distinct tumor suppressor mechanisms evolve in rodent species that differ in size and lifespan. Aging Cell 2008;7:813-823
72. Hanley NA, Hanley KP, Miettinen PJ, Otonkoski T. Weighing up beta-cell mass in mice and humans: self-renewal, progenitors or stem cells? Mol Cell Endocrinol 2008;288:79-85
73. Gepts W. Pathological anatomy of the pancreas in juvenile diabetes mellitus. Diabetes 1965;14:619-633
74. Meier JJ, Butler AE, Galasso R, Butler PC. Hyperinsulinemic hypoglycemia after gastric bypass surgery is not accompanied by islet hyperplasia or increased β-cell turnover. Diabetes Care 2006;29:1554-1559
75. Meier JJ, Butler AE, Galasso R, Rizza RA, Butler PC. Increased islet beta cell replication adjacent to intrapancreatic gastrinomas in humans. Diabetologia 2006;49:2689-2696
76. Phillips JM, O'Reilly L, Bland C, Foulis AK, Cooke A. Patients with chronic pancreatitis have islet progenitor cells in their ducts, but reversal of overt diabetes in NOD mice by anti-CD3 shows no evidence for islet regeneration. Diabetes 2007;56:634-640
77. Menge BA, Tannapfel A, Belyaev O, Drescher R, Muller C, Uhl W, Schmidt WE, Meier JJ. Partial pancreatectomy in adult humans does not provoke beta-cell regeneration. Diabetes 2008;57:142-149
78. Martin-Pagola A, Sisino G, Allende G, Dominguez-Bendala J, Gianani R, Reijonen H, Nepom GT, Ricordi C, Ruiz P, Sageshima J, Ciancio G, Burke GW, Pugliese A. 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
79. Patti ME, McMahon G, Mun EC, Bitton A, Holst JJ, Goldsmith J, Hanto DW, Callery M, Arky R, Nose V, Bonner-Weir S, Goldfine AB. Severe hypoglycaemia post-gastric bypass requiring partial pancreatectomy: evidence for inappropriate insulin secretion and pancreatic islet hyperplasia. Diabetologia 2005;48:2236-2240
80. Bonner-Weir S, Taneja M, Weir GC, Tatarkiewicz K, Song KH, Sharma A, O'Neil JJ. In vitro cultivation of human islets from expanded ductal tissue. Proc Natl Acad Sci U S A 2000;97:7999-8004
81. Gao R, Ustinov J, Korsgren O, Otonkoski T. In vitro neogenesis of human islets reflects the plasticity of differentiated human pancreatic cells. Diabetologia 2005;48:2296-2304
82. Gao R, Ustinov J, Pulkkinen MA, Lundin K, Korsgren O, Otonkoski T. Characterization of endocrine progenitor cells and critical factors for their differentiation in human adult pancreatic cell culture. Diabetes 2003;52:2007-2015
83. Hao E, Tyrberg B, Itkin-Ansari P, Lakey JR, Geron I, Monosov EZ, Barcova M, Mercola M, Levine F. Beta-cell differentiation from nonendocrine epithelial cells of the adult human pancreas. Nat Med 2006;12:310-316
84. Suarez-Pinzon WL, Lakey JR, Brand SJ, Rabinovitch A. Combination therapy with epidermal growth factor and gastrin induces neogenesis of human islet b-cells from pancreatic duct cells and an increase in functional β-cell mass. J Clin Endocrinol Metab 2005;90:3401-3409
85. 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
86. Kushner JA, Weir GC, Bonner-Weir S. Ductal origin hypothesis of pancreatic regeneration under attack. Cell Metab 2010;11:2-3
87. Ouziel-Yahalom L, Li WC, Straussman S, Guo L, Sharma A, Weir GC, Bonner-Weir S. Ductal heterogeneity suggests a subpopulation serves as postnatal pancreatic progenitors. Diabetes 2010;59(Suppl. 1):A25
88. Rovira M, Scott SG, Liss AS, Jensen J, Thayer SP, Leach SD. Isolation and characterization of centroacinar/terminal ductal progenitor cells in adult mouse pancreas. Proc Natl Acad Sci U S A 2010;107:75-80
89. Wang RN, Bouwens L, Kloppel G. Beta-cell proliferation in normal and streptozotocin-treated newborn rats: site, dynamics and capacity. Diabetologia 1994;37:1088-1096
90. Cantenys D, Portha B, Dutrillaux MC, Hollande E, Roze C, Picon L. Histogenesis of the endocrine pancreas in newborn rats after destruction by streptozotocin an immunocytochemical study. Virchows ArchB 1981;35:109-122
91. Pick A, Clark J, Kubstrup C, Pugh W, Bonner-Weir S, Polonsky K. Role of apoptosis in failure of β cell mass compensation for insulin resistance and β cell defects in the male Zucker diabetic fatty (ZDF) rat. Diabetes 1998;47:358-364
92. Jetton TL, Everill B, Lausier J, Roskens V, Habibovic A, LaRock K, Gokin A, Peshavaria M, Leahy JL. Enhanced beta-cell mass without increased proliferation following chronic mild glucose infusion. Am J Physiol Endocrinol Metab 2008;294:E679-E687
93. Yamamoto K, Miyagawa J, Waguri M, Sasada R, Igarashi K, Li M, Nammo T, Moriwaki M, Imagawa A, Yamagata K, Nakajima H, Namba M, Tochino Y, Hanafusa T, Matsuzawa Y. Recombinant human betacellulin promotes the neogenesis of β-cells and ameliorates glucose intolerance in mice with diabetes induced by selective alloxan perfusion. Diabetes 2000;49:2021-2027
94. Tokui Y, Kozawa J, Yamagata K, Zhang J, Ohmoto H, Tochino Y, Okita K, Iwahashi H, Namba M, Shimomura I, Miyagawa J. Neogenesis and proliferation of beta-cells induced by human betacellulin gene transduction via retrograde pancreatic duct injection of an adenovirus vector. Biochem Biophys Res Commun 2006;350:987-993
95. Rooman I, Bouwens L. Combined gastrin and epidermal growth factor treatment induces islet regeneration and restores normoglycaemia in C57BL6/J mice treated with alloxan. Diabetologia 2004;47:259-265
96. Huang HP, Chu K, Nemoz-Gaillard E, Elberg D, Tsai MJ. Neogenesis of beta-cells in adult BETA2/NeuroD-deficient mice. Mol Endocrinol 2002;16:541-551