Replicative capacity of β-cells and type 1 diabetes

Journal of Autoimmunity

Volumn 71, Issue , 2016, Pages 59-68

  Saunders, Diane ^a   Powers, Alvin C ^a,b,c  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Autoimmune; Cell proliferation; Diabetes; Islet

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLIN DEPENDENT KINASE INHIBITOR 2C; FATTY ACID; GLYCOGEN SYNTHASE KINASE 3; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PEPTIDE HORMONE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RAF PROTEIN; RAS PROTEIN; SCATTER FACTOR; SEROTONIN; SODIUM GLUCOSE COTRANSPORTER 2 INHIBITOR; TRANSCRIPTION FACTOR PAX4; VASCULOTROPIN A;

AUTOIMMUNITY; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL PROLIFERATION; CELL REGENERATION; EXTRACELLULAR MATRIX; GLUCOSE METABOLISM; HIGH THROUGHPUT SCREENING; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RELEASE; INSULIN RESISTANCE; INTRACELLULAR SIGNALING; MACROPHAGE; MESENCHYMAL STEM CELL; MICROENVIRONMENT; NONHUMAN; PANCREAS DUCT LIGATION; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; REVIEW; VASCULAR ENDOTHELIUM; ANIMAL; DIABETES MELLITUS, TYPE 1; DRUG EFFECTS; ENERGY METABOLISM; IMMUNOLOGY; METABOLISM; MOLECULARLY TARGETED THERAPY; PANCREAS ISLET; REGENERATION; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

ANIMALS; AUTOIMMUNITY; CELL PROLIFERATION; CELLULAR MICROENVIRONMENT; DIABETES MELLITUS, TYPE 1; ENERGY METABOLISM; HUMANS; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MACROPHAGES; MOLECULAR TARGETED THERAPY; REGENERATION; SIGNAL TRANSDUCTION;

EID: 84964669338     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2016.03.014     Document Type: Review

References (73)

1. Dai C., Brissova M., Hang Y., Thompson C., Poffenberger G., Shostak A., et al. Islet-enriched gene expression and glucose-induced insulin secretion in human and mouse islets. Diabetologia 2012, 55:707-718. 10.1007/s00125-011-2369-0.
2. Gregg B.E., Moore P.C., Demozay D., Hall B.A., Li M., Husain A., et al. Formation of a human β-cell population within pancreatic islets is set early in life. J. Clin. Endocrinol. Metab. 2012, 97:3197-3206. 10.1210/jc.2012-1206.
3. Ernst S., Demirci C., Valle S., Velazquez-Garcia S., Garcia-Ocaña A. Mechanisms in the adaptation of maternal β-cells during pregnancy. Diabetes Manag. Lond. Engl. 2011, 1:239-248. 10.2217/dmt.10.24.
4. Huang C., Snider F., Cross J.C. Prolactin receptor is required for normal glucose homeostasis and modulation of β-Cell mass during pregnancy. Endocrinology 2009, 150:1618-1626. 10.1210/en.2008-1003.
5. Demirci C., Ernst S., Alvarez-Perez J.C., Rosa T., Valle S., Shridhar V., et al. Loss of HGF/c-Met signaling in pancreatic β-cells leads to incomplete maternal β-cell adaptation and gestational diabetes mellitus - PubMed - NCBI. Diabetes 2012, 61:1143-1152. 10.2337/db11-1154.
6. Johansson M., Mattsson G., Andersson A., Jansson L., Carlsson P.-O. Islet endothelial cells and pancreatic beta-cell proliferation: studies in vitro and during pregnancy in adult rats. Endocrinology 2006, 147:2315-2324. 10.1210/en.2005-0997.
7. El Ouaamari A., Dirice E., Gedeon N., Hu J., Zhou J.-Y., Shirakawa J., et al. SerpinB1 promotes pancreatic β cell proliferation. Cell Metab. 2016, 23:194-205. 10.1016/j.cmet.2015.12.001.
8. Robitaille K., Rourke J.L., McBane J.E., Fu A., Baird S., Du Q., et al. High-throughput functional genomics identifies regulators of primary human beta cell proliferation. J. Biol. Chem. 2016, 291:4614-4625. 10.1074/jbc.M115.683912.
9. Wang P., Alvarez-Perez J.C., Felsenfeld D.P., Liu H., Sivendran S., Bender A., et al. A high-throughput chemical screen reveals that harmine-mediated inhibition of DYRK1A increases human pancreatic beta cell replication. Nat. Med. 2015, 21:383-388. 10.1038/nm.3820.
10. Dirice E., Walpita D., Vetere A., Meier B.C., Kahraman S., Hu J., et al. Inhibition of DYRK1A stimulates human beta-cell proliferation. Diabetes 2016, db151127. 10.2337/db15-1127.
11. Walpita D., Hasaka T., Spoonamore J., Vetere A., Takane K.K., Fomina-Yadlin D., et al. A human islet cell culture system for high-throughput screening. J. Biomol. Screen. 2012, 17:509-518. 10.1177/1087057111430253.
12. Kulkarni R.N., Mizrachi E.-B., Ocana A.G., Stewart A.F. Human β-cell proliferation and intracellular signaling: driving in the dark without a road map. Diabetes 2012, 61:2205-2213. 10.2337/db12-0018.
13. Bernal-Mizrachi E., Kulkarni R.N., Scott D.K., Mauvais-Jarvis F., Stewart A.F., Garcia-Ocaña A. Human β-cell proliferation and intracellular signaling part 2: still driving in the dark without a road map. Diabetes 2014, 63:819-831. 10.2337/db13-1146.
14. Stewart A.F., Hussain M.A., Garcia-Ocaña A., Vasavada R.C., Bhushan A., Bernal-Mizrachi E., et al. Human β-cell proliferation and intracellular signaling: part 3. Diabetes 2015, 64:1872-1885. 10.2337/db14-1843.
15. Chen H., Kleinberger J.W., Takane K.K., Salim F., Fiaschi-Taesch N., Pappas K., et al. Augmented stat5 signaling bypasses multiple impediments to lactogen-mediated proliferation in human beta cells. Diabetes 2015, 64:db150083-3797. 10.2337/db15-0083.
16. Amaral M.E.C., Cunha D.A., Anhê G.F., Ueno M., Carneiro E.M., Velloso L.A., et al. Participation of prolactin receptors and phosphatidylinositol 3-kinase and MAP kinase pathways in the increase in pancreatic islet mass and sensitivity to glucose during pregnancy. J. Endocrinol. 2004, 183:469-476. 10.1677/joe.1.05547.
17. Dietrich M.G., Zuellig R.A., Spinas G.A., Lehmann R., Tschopp O., Niessen M. Specific and redundant roles of PKBα/AKT1 and PKBβ/AKT2 in human pancreatic islets. Exp. Cell Res. 2015, 338:82-88. 10.1016/j.yexcr.2015.08.008.
18. George N.M., Boerner B.P., Mir S.U.R., Guinn Z., Sarvetnick N.E. Exploiting expression of hippo effector, Yap, for expansion of functional islet mass. Mol. Endocrinol. 2015, 29:1594-1607. 10.1210/me.2014-1375.
19. Lakshmipathi J., Alvarez-Perez J.C., Rosselot C., Casinelli G.P., Stamateris R.E., Rausell-Palamos F., et al. PKC-ζ is essential for pancreatic beta cell replication during insulin resistance by regulating mTOR and cyclin-D2. Diabetes 2016, db151398. 10.2337/db15-1398.
20. Xiao X., Fischbach S., Song Z., Gaffar I., Zimmerman R., Wiersch J., et al. Transient suppression of transforming growth factor beta receptor signaling facilitates human islet transplantation. Endocrinology 2016, en20151986. 10.1210/en.2015-1986.
21. Leibiger B., Moede T., Paschen M., Yunn N.-O., Lim J.H., Ryu S.H., et al. PI3K-C2α knockdown results in rerouting of insulin signaling and pancreatic beta cell proliferation. Cell Rep. 2015, 13:15-22. 10.1016/j.celrep.2015.08.058.
22. Fiaschi-Taesch N.M., Kleinberger J.W., Salim F.G., Troxell R., Wills R., Tanwir M., et al. Human pancreatic β-cell G1/S molecule cell cycle atlas. Diabetes 2013, 62:2450-2459. 10.2337/db12-0777.
23. Fiaschi-Taesch N., Bigatel T.A., Sicari B., Takane K.K., Salim F., Velazquez-Garcia S., et al. Survey of the human pancreatic beta-cell G1/S proteome reveals a potential therapeutic role for cdk-6 and cyclin D1 in enhancing human beta-cell replication and function in vivo. Diabetes 2009, 58:882-893. 10.2337/db08-0631.
24. Fiaschi-Taesch N.M., Salim F., Kleinberger J., Troxell R., Cozar-Castellano I., Selk K., et al. Induction of human β-cell proliferation and engraftment using a single G1/S regulatory molecule, cdk6. Diabetes 2010, 59:1926-1936. 10.2337/db09-1776.
25. Draney C., Hobson A.E., Grover S.G., Jack B.O., Tessem J.S. Cdk5r1 overexpression induces primary β-cell proliferation. J. Diabetes Res. 2016, 2016:6375804-6375815. 10.1155/2016/6375804.
26. Pal A., Potjer T.P., Thomsen S.K., Ng H.J., Barrett A., Scharfmann R., et al. Loss-of-function mutations in the cell-cycle control gene CDKN2A impact on glucose homeostasis in humans. Diabetes 2016, 65:527-533. 10.2337/db15-0602.
27. Tiwari S., Roel C., Wills R., Casinelli G., Tanwir M., Takane K.K., et al. Early and late G1/S cyclins and Cdks act complementarily to enhance authentic human β-cell proliferation and expansion. Diabetes 2015, 64:3485-3498. 10.2337/db14-1885.
28. Karnik S.K., Hughes C.M., Gu X., Rozenblatt-Rosen O., McLean G.W., Xiong Y., et al. Menin regulates pancreatic islet growth by promoting histone methylation and expression of genes encoding p27Kip1 and p18INK4c. Pnas 2005, 102:14659-14664. 10.1073/pnas.0503484102.
29. Amisten S., Salehi A., Rorsman P., Jones P.M., Persaud S.J. An atlas and functional analysis of G-protein coupled receptors in human islets of Langerhans. Pharmacol. Ther. 2013, 139:359-391. 10.1016/j.pharmthera.2013.05.004.
30. Angueira A.R., Ludvik A.E., Reddy T.E., Wicksteed B., Lowe W.L., Layden B.T. New insights into gestational glucose metabolism: lessons learned from 21st century approaches. Diabetes 2015, 64:327-334. 10.2337/db14-0877.
31. Vasavada R.C., Wang L., Fujinaka Y., Takane K.K., Rosa T.C., Mellado-Gil J.M.D., et al. Protein kinase C-zeta activation markedly enhances beta-cell proliferation: an essential role in growth factor mediated beta-cell mitogenesis. Diabetes 2007, 56:2732-2743. 10.2337/db07-0461.
32. Guthalu Kondegowda N., Joshi-Gokhale S., Harb G., Williams K., Zhang X.Y., Takane K.K., et al. Parathyroid hormone-related protein enhances human ß-cell proliferation and function with associated induction of cyclin-dependent kinase 2 and cyclin E expression. Diabetes 2010, 59:3131-3138. 10.2337/db09-1796.
33. Arumugam R., Fleenor D., Freemark M. Knockdown of prolactin receptors in a pancreatic beta cell line: effects on DNA synthesis, apoptosis, and gene expression. Endocrine 2013, 46:568-576. 10.1007/s12020-013-0073-1.
34. Sorenson R.L., Brelje T.C., Roth C. Effects of steroid and lactogenic hormones on islets of Langerhans: a new hypothesis for the role of pregnancy steroids in the adaptation of islets - PubMed - NCBI. Endocrinology 1993, 133:2227-2234. 10.1210/endo.133.5.8404674.
35. Hyslop C.M., Tsai S., Shrivastava V., Santamaria P., Huang C. Prolactin as an adjunct for Type 1 diabetes immunotherapy. Endocrinology 2016, 157:150-165. 10.1210/en.2015-1549.
36. Kim H., Toyofuku Y., Lynn F.C., Chak E., Uchida T., Mizukami H.I., et al. Serotonin regulates pancreatic β-cell mass during pregnancy. Nat. Med. 2010, 16:804-808. 10.1038/nm.2173.
37. Wang G., Rajpurohit S.K., Delaspre F., Walker S.L. First quantitative high-throughput screen in zebrafish identifies novel pathways for increasing pancreatic β-cell mass. Elife 2015, 4:e08261. 10.7554/eLife.08261.001.
38. Liu Y., Tanabe K., Baronnier D., Patel S., Woodgett J., Cras-Méneur C., et al. Conditional ablation of Gsk-3β in islet beta cells results in expanded mass and resistance to fat feeding-induced diabetes in mice. Diabetologia 2010, 53:2600-2610. 10.1007/s00125-010-1882-x.
39. Porat S., Weinberg-Corem N., Tornovsky-Babaey S., Schyr-Ben-Haroush R., Hija A., Stolovich-Rain M., et al. Control of pancreatic β-cell regeneration by glucose metabolism. Cell Metab. 2011, 13:440-449. 10.1016/j.cmet.2011.02.012.
40. Shen W., Taylor B., Jin Q., Nguyen-Tran V., Meeusen S., Zhang Y.-Q., et al. Inhibition of DYRK1A and GSK3B induces human β-cell proliferation. Nat. Commun. 2015, 6:8372. 10.1038/ncomms9372.
41. Cheng S.T.W., Chen L., Li S.Y.T., Mayoux E., Leung P.S. The effects of empagliflozin, an SGLT2 inhibitor, on pancreatic β-cell mass and glucose homeostasis in type 1 diabetes. PLoS ONE 2016, 11:e0147391. 10.1371/journal.pone.0147391.
42. Lorenzo P.I., Fuente-Martín E., Brun T., Cobo-Vuilleumier N., Jimenez-Moreno C.M., G Herrera Gomez I., et al. PAX4 defines an expandable β-cell subpopulation in the adult pancreatic islet. Sci. Rep. 2015, 5:15672. 10.1038/srep15672.
43. Brun T., Franklin I., St-Onge L., Biason-Lauber A., Schoenle E.J., Wollheim C.B., et al. The diabetes-linked transcription factor PAX4 promotes (beta)-cell proliferation and survival in rat and human islets. J. Cell Biol. 2004, 167:1123-1135. 10.1083/jcb.200405148.
44. Liu J., Liu S., Chen Y., Zhao X., Lu Y., Cheng J. Functionalized self-assembling peptide improves INS-1 β-cell function and proliferation via the integrin/FAK/ERK/cyclin pathway. Int. J. Nanomedicine 2015, 10:3519-3531. 10.2147/IJN.S80502.
45. Brelje T.C., Bhagroo N.V., Stout L.E., Sorenson R.L. Beneficial effects of lipids and prolactin on insulin secretion and beta-cell proliferation: a role for lipids in the adaptation of islets to pregnancy. J. Endocrinol. 2008, 197:265-276. 10.1677/JOE-07-0657.
46. Maedler K., Oberholzer J., Bucher P., Spinas G.A., Donath M.Y. Monounsaturated fatty acids prevent the deleterious effects of palmitate and high glucose on human pancreatic beta-cell turnover and function. Diabetes 2003, 52:726-733.
47. Kigerl K.A., Gensel J.C., Ankeny D.P., Alexander J.K., Donnelly D.J., Popovich P.G. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J. Neurosci. 2009, 29:13435-13444. 10.1523/JNEUROSCI.3257-09.2009.
48. Arnold L., Henry A., Poron F., Baba-Amer Y., van Rooijen N., Plonquet A., et al. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J. Exp. Med. 2007, 204:1057-1069. 10.1084/jem.20070075.
49. He H., Xu J., Warren C.M., Duan D., Li X., Wu L., et al. Endothelial cells provide an instructive niche for the differentiation and functional polarization of M2-like macrophages. Blood 2012, 120:3152-3162. 10.1182/blood-2012-04-422758.
50. Cattin A.-L., Burden J.J., Van Emmenis L., Mackenzie F.E., Hoving J.J.A., Garcia Calavia N., et al. Macrophage-induced blood vessels guide Schwann cell-mediated regeneration of peripheral nerves. Cell. 2015, 162:1127-1139. 10.1016/j.cell.2015.07.021.
51. Sindrilaru A., Peters T., Wieschalka S., Baican C., Baican A., Peter H., et al. An unrestrained proinflammatory M1 macrophage population induced by iron impairs wound healing in humans and mice. J. Clin. Investig. 2011, 121:985-997. 10.1172/JCI44490.
52. Calderon B., Carrero J.A., Ferris S.T., Sojka D.K., Moore L., Epelman S., et al. The pancreas anatomy conditions the origin and properties of resident macrophages. J. Exp. Med. 2015, 212:1497-1512. 10.1084/jem.20150496.
53. Van Gassen N., Van Overmeire E., Leuckx G., Heremans Y., De Groef S., Cai Y., et al. Macrophage dynamics are regulated by local macrophage proliferation and monocyte recruitment in injured pancreas. Eur. J. Immunol. 2015, 45:1482-1493. 10.1002/eji.201445013.
54. Cucak H., Grunnet L.G., Rosendahl A. Accumulation of M1-like macrophages in type 2 diabetic islets is followed by a systemic shift in macrophage polarization. J. Leukoc. Biol. 2014, 95:149-160. 10.1189/jlb.0213075.
55. Lavin Y., Winter D., Blecher-Gonen R., David E., Keren-Shaul H., Merad M., et al. Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell. 2014, 159:1312-1326. 10.1016/j.cell.2014.11.018.
56. Criscimanna A., Coudriet G.M., Gittes G.K., Piganelli J.D., Esni F. Activated macrophages create lineage-specific microenvironments for pancreatic acinar- and β-cell regeneration in mice. Gastroenterology 2014, 147:1106-1118. e11. 10.1053/j.gastro.2014.08.008.
57. Pound L.D., Patrick C., Eberhard C.E., Mottawea W., Wang G.-S., Abujamel T., et al. Cathelicidin antimicrobial peptide: a novel regulator of islet function, islet regeneration, and selected gut bacteria. Diabetes 2015, 64:4135-4147. 10.2337/db15-0788.
58. Lee T.-S., Chau L.-Y. Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat. Med. 2002, 8:240-246. 10.1038/nm0302-240.
59. Nakamichi I., Habtezion A., Zhong B., Contag C.H., Butcher E.C., Omary M.B. Hemin-activated macrophages home to the pancreas and protect from acute pancreatitis via heme oxygenase-1 induction. J. Clin. Investig. 2005, 115:3007-3014. 10.1172/JCI24912.
60. Ndisang J.F., Mishra M. The heme oxygenase system selectively suppresses the proinflammatory macrophage m1 phenotype and potentiates insulin signaling in spontaneously hypertensive rats. Am. J. Hypertens. 2013, 26:1123-1131. 10.1093/ajh/hpt082.
61. Husseini M., Wang G.-S., Patrick C., Crookshank J.A., MacFarlane A.J., Noel J.A., et al. Heme oxygenase-1 induction prevents autoimmune diabetes in association with pancreatic recruitment of M2-like macrophages, mesenchymal cells, and fibrocytes. Endocrinology 2015, 156. en20151304-3949. 10.1210/en.2015-1304.
62. Nikolic I., Saksida T., Vujicic M., Stojanovic I., Stosic-Grujicic S. Anti-diabetic actions of carbon monoxide-releasing molecule (CORM)-A1: immunomodulation and regeneration of islet beta cells. Immunol. Lett. 2015, 165:39-46. 10.1016/j.imlet.2015.03.009.
63. Saavedra-Ávila N.A., Sengupta U., Sánchez B., Sala E., Haba L., Stratmann T., et al. Cyclin D3 promotes pancreatic β-cell fitness and viability in a cell cycle-independent manner and is targeted in autoimmune diabetes. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:E3405-E3414. 10.1073/pnas.1323236111.
64. Ding Y., Xu Y., Shuai X., Shi X., Chen X., Huang W., et al. Reg3α overexpression protects pancreatic beta-cells from cytokine-induced damage and improves islet transplant outcome. Mol. Med. 2014, 20:548-558. 10.2119/molmed.2014.00104.
65. Diaz-Ganete A., Baena-Nieto G., Lomas-Romero I.M., Lopez-Acosta J.F., Cozar-Castellano I., Medina F., et al. Ghrelin's effects on proinflammatory cytokine mediated apoptosis and their impact on β-cell functionality. Int. J. Endocrinol. 2015, 2015:1-11. 10.1155/2015/235727.
66. Song I., Patel O., Himpe E., Muller C.J.F., Bouwens L. Beta cell mass restoration in Alloxan-diabetic mice treated with EGF and gastrin. PLoS ONE 2015, 10:e0140148. 10.1371/journal.pone.0140148.
67. Brissova M., Aamodt K., Brahmachary P., Prasad N., Hong J.-Y., Dai C., et al. Islet microenvironment, modulated by vascular endothelial growth factor-A signaling, promotes β cell regeneration. Cell Metab. 2014, 19:498-511. 10.1016/j.cmet.2014.02.001.
68. Xiao X., Gaffar I., Guo P., Wiersch J., Fischbach S., Peirish L., et al. M2 macrophages promote beta-cell proliferation by up-regulation of SMAD7. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:E1211-E1220. 10.1073/pnas.1321347111.
69. Ino K., Masuya M., Tawara I., Miyata E., Oda K., Nakamori Y., et al. Monocytes infiltrate the pancreas via the MCP-1/CCR2 pathway and differentiate into stellate cells. PLoS ONE 2014, 9:e84889. 10.1371/journal.pone.0084889.
70. Bayan J.-A., Peng Z., Zeng N., He L., Chen J., Stiles B.L. Crosstalk between activated myofibroblasts and β cells in injured mouse pancreas. Pancreas 2015, 44:1111-1120. 10.1097/MPA.0000000000000431.
71. Chen P., Cescon M., Zuccolotto G., Nobbio L., Colombelli C., Filaferro M., et al. Collagen VI regulates peripheral nerve regeneration by modulating macrophage recruitment and polarization. Acta Neuropathol. 2015, 129:97-113. 10.1007/s00401-014-1369-9.
72. Cao X., Han Z.-B., Zhao H., Liu Q. Transplantation of mesenchymal stem cells recruits trophic macrophages to induce pancreatic beta cell regeneration in diabetic mice. Int. J. Biochem. Cell Biol. 2014, 53:372-379. 10.1016/j.biocel.2014.06.003.
73. Liou G.-Y., Döppler H., Necela B., Krishna M., Crawford H.C., Raimondo M., et al. Macrophage-secreted cytokines drive pancreatic acinar-to-ductal metaplasia through NF-κB and MMPs. J. Cell Biol. 2013, 202:563-577. 10.1083/jcb.201301001.