Recent progress in studies of factors that elicit pancreatic β-cell expansion

Qiu Li, Zhi-Chun Lai

PDF(156 KB)
PDF(156 KB)
Protein Cell ›› 2015, Vol. 6 ›› Issue (2) : 81-87. DOI: 10.1007/s13238-014-0123-3
MINI-REVIEW
MINI-REVIEW

Recent progress in studies of factors that elicit pancreatic β-cell expansion

Author information +
History +

Abstract

The loss of or decreased functional pancreatic β-cell is a major cause of type 1 and type 2 diabetes. Previous studies have shown that adult β-cells can maintain their ability for a low level of turnover through replication and neogenesis. Thus, a strategy to prevent and treat diabetes would be to enhance the ability of β-cells to increase the mass of functional β-cells. Consequently, much effort has been devoted to identify factors that can effectively induce β-cell expansion. This review focuses on recent reports on small molecules and protein factors that have been shown to promote β-cell expansion.

Keywords

pancreatic islet / β-cell / cell proliferation/ replication/expansion / cell signaling

Cite this article

Download citation ▾
Qiu Li, Zhi-Chun Lai. Recent progress in studies of factors that elicit pancreatic β-cell expansion. Protein Cell, 2015, 6(2): 81‒87 https://doi.org/10.1007/s13238-014-0123-3

References

[1]
Adeghate E, Ponery AS (2002) GABA in the endocrine pancreas: Cellular localization and function in normal and diabetic rats. Tissue Cell34: 1-6
CrossRef Google scholar
[2]
Aguayo-Mazzucato C, Zavacki AM, Marinelarena A, Hollister-Lock J, El Khattabi I, Marsili A, Weir GC, Sharma A, Larsen PR, Bonner-Weir S (2013) Thyroid hormone promotes postnatal rat pancreatic β -cell development and glucose-responsive insulin secretion through MAFA. Diabetes62: 1569-1580
CrossRef Google scholar
[3]
Annes JP, Ryu JH, Lam K, Carolan PJ, Utz K, Hollister-Lock J, Arvanites AC, Rubin LL, Weir G, Melton DA (2012) Adenosine kinase inhibition selectively promotes rodent and porcine islet β - cell replication. Proc Natl Acad Sci USA109: 3915-3920
CrossRef Google scholar
[4]
Ansarullah, Lu Y, Holstein M, DeRuyter B, Rabinovitch A, Guo Z (2013) Stimulating β -cell regeneration by combining a GPR119 agonist with a DPP-IV inhibitor. PLoS One8: e53345
CrossRef Google scholar
[5]
Bernal-Mizrachi E, Kulkarni RN, Scott DK, Mauvais-Jarvis F, Stewart AF, Garcia-Ocaña A (2014) Human β -cell proliferation and intracellular signaling part 2: still driving in the dark without a road map. Diabetes63: 819-831
CrossRef Google scholar
[6]
Bock T, Pakkenberg B, Buschard K (2003) Increased islet volume but unchanged islet number in ob/ob mice. Diabetes52: 1716-1722
CrossRef Google scholar
[7]
Boström P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo JC, Rasbach KA, Boström EA, Choi JH, Long JZ, Kajimura S, Zingaretti MC, Vind BF, Tu H, Cinti S, Højlund K, Gygi SP, Spiegelman BM (2012) A PGC1-α -dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature481: 463-468
CrossRef Google scholar
[8]
Braun M, Ramracheya R, Bengtsson M, Clark A, Walker JN, Johnson PR, Rorsman P (2010) GABA is an autocrine excitatory transmitter in human pancreatic beta-cells. Diabetes59: 1694-1701
CrossRef Google scholar
[9]
Cavelti-Weder C, Shtessel M, Reuss JE, Jermendy A, Yamada T, Caballero F, Bonner-Weir S, Weir GC (2013) Pancreatic duct ligation after almost complete β -cell loss: exocrine regeneration but no evidence of β -cell regeneration. Endocrinology154: 4493-4502
CrossRef Google scholar
[10]
Centers for Disease Control and Prevention (2014) National diabetes statistics report: estimates of diabetes and its burden in the United States, 2014. U.S. Department of Health and Human Services, Atlanta
[11]
Dor Y, Brown J, Martinez OI, Melton DA (2004) Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature429: 41 -46
CrossRef Google scholar
[12]
Fenalti G, Law RH, Buckle AM, Langendorf C, Tuck K, Rosado CJ, Faux NG, Mahmood K, Hampe CS, Banga JP, Wilce M, Schmidberger J, Rossjohn J, El-Kabbani O, Pike RN, Smith AI, Mackay IR, Rowley MJ, Whisstock JC (2007) GABA production by glutamic aciddecarboxylase is regulated by a dynamic catalytic loop. Nat Struct Mol Biol14: 280-286
CrossRef Google scholar
[13]
Ferron M, Hinoi E, Karsenty G, Ducy P (2008) Osteocalcin differentially regulates β cell and adipocyte gene expression and affects the development of metabolic diseases in wild-type mice. Proc Natl Acad Sci USA105: 5266-5270
CrossRef Google scholar
[14]
Furuya F, Shimura H, Asami K, Ichijo S, Takahashi K, Kaneshige M, Oikawa Y, Aida K, Endo T, Kobayashi T (2013) Ligand-bound thyroid hormone receptor contributes to reprogramming of pancreatic acinar cells into insulin-producing cells. J Biol Chem288: 16155-16166
CrossRef Google scholar
[15]
Futamura M, Yao J, Li X, Bergeron R, Tran JL, Zycband E, Woods J, Zhu Y, Shao Q, Maruki-Uchida H, Goto-Shimazaki H, Langdon RB, Erion MD, Eiki J, Zhou YP (2012) Chronic treatment with a glucokinase activator delays the onset of hyperglycaemia and preserves beta cell mass in the Zucker diabetic fatty rat. Diabetologia55: 1071-1080
CrossRef Google scholar
[16]
Gao J, Tian L, Weng G, Bhagroo NV, Sorenson RL, O’Brien TD, Luo J, Guo Z (2011) Stimulating beta cell replication and improving islet graft function by GPR119 agonists. Transpl Int24: 1124-1134
CrossRef Google scholar
[17]
Guardado-Mendoza R, Jimenez-Ceja L, Majluf-Cruz A, Kamath S, Fiorentino TV, Casiraghi F, Velazquez AO, DeFronzo RA, Dick E, Davalli A, Folli F (2012) Impact of obesity severity and duration on pancreatic β -cell and α -cell dynamics in normoglycemic nonhuman primates. Int J Obes37: 1071 -1078
CrossRef Google scholar
[18]
Gunasekaran U, Hudgens CW, Wright BT, Maulis MF, Gannon M (2012) Differential regulation of embryonic and adult β cell replication. Cell Cycle11: 2431-2442
CrossRef Google scholar
[19]
Gusarova V, Alexa CA, Na E, Stevis PE, Xin Y, Bonner-Weir S, Cohen JC, Hobbs HH, Murphy AJ, Yancopoulos GD, Gromada J (2014) ANGPTL8/Betatrophin does not control pancreatic beta cell expansion. Cell159: 691-696
CrossRef Google scholar
[20]
Hanley SC, Austin E, Assouline-Thomas B, Kapeluto J, Blaichman J, Moosavi M, Petropavlovskaia M, Rosenberg L (2010) Beta-cell mass dynamics and islet cell plasticity in human type 2 diabetes. Endocrinology151: 1462-1472
CrossRef Google scholar
[21]
Hartoft-Nielsen ML, Rasmussen AK, Bock T, Feldt-Rasmussen U, Kaas A, Buschard K (2009) Iodine and tri-iodo-thyronine reduce the incidence of type 1 diabetes mellitus in the autoimmune prone BB rats. Autoimmunity42: 131-138
CrossRef Google scholar
[22]
Heit JJ, Karnik SK, Kim SK (2006) Intrinsic regulators of pancreatic beta-cell proliferation. Annu Rev Cell Dev Biol22: 311 -338
CrossRef Google scholar
[23]
Hull RL, Kodama K, Utzschneider KM, Carr DB, Prigeon RL, Kahn SE (2005) Dietary-fat-induced obesity in mice results in beta cell hyperplasia but not increased insulin release: evidence for specificity of impaired beta cell adaptation. Diabetologia48: 1350-1358
CrossRef Google scholar
[24]
Jackerott M, Lee YC, Møllgård K, Kofod H, Jensen J, Rohleder S, Neubauer N, Gaarn LW, Lykke J, Dodge R, Dalgaard LT, Søstrup B, Jensen DB, Thim L, Nexø E, Thams P, Bisgaard HC, Nielsen JH (2006) Trefoil factors are expressed in human and rat endocrine pancreas: differential regulation by growth hormone. Endocrinology147: 5752-5759
CrossRef Google scholar
[25]
Jörns A, Rath KJ, Terbish T, Arndt T, Meyer Zu, Vilsendorf A, Wedekind D, Hedrich HJ, Lenzen S (2010) Diabetes prevention by immunomodulatory FTY720 treatment in the LEW.1AR1-iddm rat despite immune cell activation. Endocrinology151: 3555-3565
CrossRef Google scholar
[26]
Jörns A, Akin M, Arndt T, Terbish T, Zu Vilsendorf AM, Wedekind D, Hedrich HJ, Lenzen S (2014) Anti-TCR therapy combined with fingolimod for reversal of diabetic hyperglycemia by β cell regeneration in the LEW.1AR1-iddm rat model of type 1 diabetes. J Mol Med92: 743-755
[27]
Kaneto H, Miyatsuka T, Kawamori D, Yamamoto K, Kato K, Shiraiwa T, Katakami N, Yamasaki Y, Matsuhisa M, Matsuoka TA (2008) PDX-1 and MafA play a crucial role in pancreatic beta-cell differentiation and maintenance of mature beta-cell function. Endocr J55: 235-252
CrossRef Google scholar
[28]
Kaneto H, Matsuoka TA, Katakami N, Matsuhisa M (2009) Combination of MafA, PDX-1 and NeuroD is a useful tool to efficiently induce insulin-producing surrogate beta-cells. Curr Med Chem16: 3144-3151
CrossRef Google scholar
[29]
Kim TK, Lee JS, Jung HS, Ha TK, Kim SM, Han N, Lee EJ, Kim TN, Kwon MJ, Lee SH, Kim MK, Rhee BD, Park JH (2014) Triiodothyronine induces proliferation of pancreatic β –cells through the MAPK/ERK pathway. Exp Clin Endocrinol Diabetes122: 240-245
CrossRef Google scholar
[30]
Klöppel G, Löhr M, Habich K, Oberholzer M, Heitz PU (1985) Islet pathology and the pathogenesis of type 1 and type 2 diabetes mellitus revisited. Surv Synth Pathol Res4: 110-125
[31]
Kulkarni RN, Mizrachi EB, Ocana AG, Stewart AF (2012) Human β - cell proliferation and intracellular signaling: driving in the dark without a road map. Diabetes61: 2205-2213
CrossRef Google scholar
[32]
Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD, Confavreux C, Dacquin R, Mee PJ, McKee MD, Jung DY, Zhang Z, Kim JK, MauvaisJarvis F, Ducy P, Karsenty G (2007) Endocrine regulation of energy metabolism by the skeleton. Cell130: 456-469
CrossRef Google scholar
[33]
Lenzen S, Bailey CJ (1984) Thyroid hormones, gonadal and adrenocortical steroids and the function of the islets of Langerhans. Endocr Rev5: 411-434
CrossRef Google scholar
[34]
Ligon B, Ligon B, Yang J, Morin SB, Ruberti MF, Steer ML (2007) Regulation of pancreatic islet cell survival and replication by gamma-aminobutyric acid. Diabetologia50: 764-773
CrossRef Google scholar
[35]
López-Acosta JF, Moreno-Amador JL, Jiménez-Palomares M, DíazMarrero AR, Cueto M, Perdomo G, Cózar-Castellano I (2013) Epoxypukalide induces proliferation and protects against cytokine-mediated apoptosis in primary cultures of pancreatic β -cells. PLoS One8: e52862
CrossRef Google scholar
[36]
Madsbad S, Laurberg P, Weeke J, Orskov H, Faber OK, Binder C, Krarup T, Regeur L (1981) Very early changes in circulating T3 and rT3 during development of metabolic derangement in diabetic patients. Acta Med Scand209: 385-387
CrossRef Google scholar
[37]
Meier JJ, Lin JC, Butler AE, Galasso R, Martinez DS, Butler PC (2006) Direct evidence of attempted beta cell regeneration in an 89-year-old patient with recent-onset type 1 diabetes. Diabetologia49: 1838-1844
CrossRef Google scholar
[38]
Mizokami A, Yasutake Y, Gao J, Matsuda M, Takahashi I, Takeuchi H, Hirata M (2013) Osteocalcin induces release of glucagon-like peptide-1 and thereby stimulates insulin secretion in mice. PloS One8: e57375
CrossRef Google scholar
[39]
Moon H, Chon J, Joo J, Kim D, In J, Lee H, Park J, Choi J (2013) FTY720 preserved islet β -cell mass by inhibiting apoptosis and increasing survival of β -cells in db/db mice. Diabetes Metab Res Rev29: 19-24
CrossRef Google scholar
[40]
Nir T, Melton DA, Dor Y (2007) Recovery from diabetes in mice by beta cell regeneration. J Clin Invest117: 2553-2561
CrossRef Google scholar
[41]
Oh YS, Lee YJ, Park K, Choi HH, Yoo S, Jun HS (2014) Treatment with glucokinase activator, YH-GKA, increases cell proliferation and decreases glucotoxic apoptosis in INS-1 cells. Eur J Pharm Sci51: 137-145
CrossRef Google scholar
[42]
Orime K, Shirakawa J, Togashi Y, Tajima K, Inoue H, Ito Y, Sato K, Nakamura A, Aoki K, Goshima Y, Terauchi Y (2013) Trefoil factor 2 promotes cell proliferation in pancreatic β -cells through CXCR-4-mediated ERK1/2 phosphorylation. Endocrinology154: 54-64
CrossRef Google scholar
[43]
Overton HA, Babbs AJ, Doel SM, Fyfe MC, Gardner LS, Griffin G, Jackson HC, Procter MJ, Rasamison CM, Tang-Christensen M, Widdowson PS, Williams GM, Reynet C (2006) Deorphanization of a G protein-coupled receptor for oleoylethanolamide and its use in the discovery of small-molecule hypophagic agents. Cell Metab3: 167-175
CrossRef Google scholar
[44]
Park K (2012) Identification of YH-GKA, a novel benzamideglucokinase activator as therapeutic candidate for type 2 diabetes mellitus. Arch Pharm Res35: 2029-2033
CrossRef Google scholar
[45]
Peshavaria M, Larmie BL, Lausier J, Satish B, Habibovic A, Roskens V, Larock K, Everill B, Leahy JL, Jetton TL (2006) Regulation of pancreatic beta-cell regeneration in the normoglycemic 60 % partial-pancreatectomy mouse. Diabetes55: 3289-3298
CrossRef Google scholar
[46]
Rahier J, Guiot Y, Goebbels RM, Sempoux C, Henquin JC (2008) Pancreatic beta-cell mass in European subjects with type 2 diabetes. Diabetes Obes Metab10(Suppl 4): 32-42
CrossRef Google scholar
[47]
Saisho Y, Butler AE, Manesso E, Elashoff D, Rizza RA, Butler PC (2013) β -Cell mass and turnover in humans: effects of obesity and aging. Diabetes Care36: e112
CrossRef Google scholar
[48]
Salpeter SJ, Klein AM, Huangfu D, Grimsby J, Dor Y (2010) Glucose and aging control the quiescence period that follows pancreatic beta cell replication. Development137: 3205-3213
CrossRef Google scholar
[49]
Samson MH, Vestergaard EM, Milman N, Poulsen SS, Nexo E (2008) Circulating serum trefoil factors increase dramatically during pregnancy. Scand J Clin Lab Invest68: 369-374
CrossRef Google scholar
[50]
Samson MH, Poulsen SS, Obeid R, Herrmann W, Nexo E (2011) Trefoil factor family peptides in the human foetus and at birth. Eur J Clin Invest41: 785-792
CrossRef Google scholar
[51]
Sanchis-Gomar F, Perez-Quilis C (2014) The p38-PGC-1 α -irisinbetatrophin axis: exploring new pathways in insulin resistance. Adipocyte3: 67-68
CrossRef Google scholar
[52]
Sherry NA, Kushner JA, Glandt M, Kitamura T, Brillantes AM, Herold KC (2006) Effects of autoimmunity and immune therapy on betacell turnover in type 1 diabetes. Diabetes55: 3238-3245
CrossRef Google scholar
[53]
Shirakawa J, Okuyama T, Yoshida E, Shimizu M, Horigome Y, Tuno T, Hayasaka M, Abe S, Fuse M, Togashi Y, Terauchi Y (2014) Effects of the antitumor drug OSI-906, a dual inhibitor of IGF-1 receptor and insulin receptor, on the glycemic control, β –cell functions, and β -cell proliferation in male mice. Endocrinology155: 2102-2111
CrossRef Google scholar
[54]
Soltani N, Qiu H, Aleksic M, Glinka Y, Zhao F, Liu R, Li Y, Zhang N, Chakrabarti R, Ng T, Jin T, Zhang H, Lu WY, Feng ZP, Prud’homme GJ, Wang Q (2011) GABA exerts protective and regenerative effects on islet beta cells and reverses diabetes. Proc Natl Acad Sci USA108: 11692-11697
CrossRef Google scholar
[55]
Song M, Park HJ (2014) Anti-inflammatory effect of Phellinuslinteus grown on germinated brown rice on dextran sodium sulfateinduced acute colitis in mice and LPS-activated macrophages. J Ethnopharmacol154: 311 -318
CrossRef Google scholar
[56]
Sorenson RL, Brelje TC (1997) Adaptation of islets of Langerhans to pregnancy: beta-cell growth, enhanced insulin secretion and the role of lactogenic hormones. Horm Metab Res29: 301 -307
CrossRef Google scholar
[57]
Stolovich-Rain M, Hija A, Grimsby J, Glaser B, Dor Y (2012) Pancreatic beta cells in very old mice retain capacity for compensatory proliferation. J Biol Chem287: 27407-27414
CrossRef Google scholar
[58]
Tian J, Dang H, Chen Z, Guan A, Jin Y, Atkinson MA, Kaufman DL (2013) γ -Aminobutyric acid regulates both the survival and replication of human β -cells. Diabetes62: 3760-3765
CrossRef Google scholar
[59]
Toselli C, Hyslop CM, Hughes M, Natale DR, Santamaria P, Huang CT (2014) Contribution of a non-β -cell source to β -cell mass during pregnancy. PLoS One9: e100398
CrossRef Google scholar
[60]
Truong W, Emamaullee JA, Merani S, Anderson CC, James Shapiro AM (2007) Human islet function is not impaired by the sphingosine-1-phosphate receptor modulator FTY720. Am J Transpl7: 2031 -2038
CrossRef Google scholar
[61]
Vetere A, Choudhary A, Burns SM, Wagner BK (2014) Targeting the pancreatic β -cell to treat diabetes. Nat Rev Drug Discov13: 278-289
CrossRef Google scholar
[62]
Wang Y, Liu Y, Wang H, Li C, Qi P, Bao J (2012) Agaricusbisporuslectins mediates islet β -cell proliferation through regulation of cell cycle proteins. Exp Biol Med237: 287-296
CrossRef Google scholar
[63]
Wei P, Shi M, Barnum S, Cho H, Carlson T, Fraser JD (2009) Effects of glucokinase activators GKA50 and LY2121260 on proliferation and apoptosis in pancreatic INS-1 beta cells. Diabetologia52: 2142-2150
CrossRef Google scholar
[64]
Wei J, Hanna T, Suda N, Karsenty G, Ducy P (2014) Osteocalcin promotes β -cell proliferation during development and adulthood through Gprc6a. Diabetes63: 1021 -1031
CrossRef Google scholar
[65]
Xiao X, Chen Z, Shiota C, Prasadan K, Guo P, El-Gohary Y, Paredes J, Welsh C, Wiersch J, Gittes GK (2013a) No evidence for β cell neogenesis in murine adult pancreas. J Clin Invest123: 2207-2217
CrossRef Google scholar
[66]
Xiao X, Wiersch J, El-Gohary Y, Guo P, Prasadan K, Paredes J, Welsh C, Shiota C, Gittes GK (2013b) TGFβ receptor signaling is essential for inflammation-induced but not β -cell workloadinduced β -cell proliferation. Diabetes62: 1217-1226
CrossRef Google scholar
[67]
Ximenes HM, Lortz S, Jörns A, Lenzen S (2007) Triiodothyronine (T3)-mediated toxicity and induction of apoptosis in insulinproducing INS-1 cells. Life Sci80: 2045-2050
CrossRef Google scholar
[68]
Xu Y, Wang L, He J, Bi Y, Li M, Wang T, Wang L, Jiang Y, Dai M, Lu J, Xu M, Li Y, Hu N, Li J, Mi S, Chen CS, Li G, Mu Y, Zhao J, Kong L, Chen J, Lai S, Wang W, Zhao W, Ning G, 2010China noncommunicable disease surveillance group (2013) Prevalence and control of diabetes in Chinese adults. JAMA310: 948-959
CrossRef Google scholar
[69]
Yi P, Park JS, Melton DA (2013) Betatrophin: a hormone that controls pancreatic β cell proliferation. Cell153: 747-758
CrossRef Google scholar
[70]
Yi P, Park JS, Melton DA (2014) Perspectives on the activities of ANGPTL8/Betatrophin. Cell159: 467-468
CrossRef Google scholar
[71]
Yu LG, Fernig DG, Smith JA, Milton JD, Rhodes JM (1993) Reversible inhibition of proliferation of epithelial cell lines by Agaricus bisporus (edible mushroom) lectin. Cancer Res53: 4627-4632
[72]
Yu LG, Fernig DG, White MR, Spiller DG, Appleton P, Evans RC, Grierson I, Smith JA, Davies H, Gerasimenko OV, Petersen OH, Milton JD, Rhodes JM (1999) Edible mushroom (Agaricus bisporus) lectin, which reversibly inhibits epithelial cell proliferation, blocks nuclear localization sequence-dependent nuclear protein import. J Biol Chem274: 4890-4899
CrossRef Google scholar
[73]
Zhang Y, Li R, Meng Y, Li S, Donelan W, Zhao Y, Qi L, Zhang M, Wang X, Cui T, Yang LJ, Tang D (2014) Irisin stimulates browning of white adipocytes through mitogen-activated protein kinase p38 MAP kinase and ERK MAP kinase signaling. Diabetes63: 514-525
CrossRef Google scholar
[74]
Zhao Z, Choi J, Zhao C, Ma ZA (2012) FTY720 normalizes hyperglycemia by stimulating β -cell in vivo regeneration in db/ db mice through regulation of cyclin D3 and p57 (KIP2). J Biol Chem287: 5562-5573
CrossRef Google scholar

RIGHTS & PERMISSIONS

2014 This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
AI Summary AI Mindmap
PDF(156 KB)

Accesses

Citations

Detail

Sections
Recommended

/