Resveratrol ameliorates the maturation process of β-cell-like cells obtained from an optimized differentiation protocol of human embryonic stem cells

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Pezzolla, Daniela ^a,c   López Beas, Javier ^a,c   Lachaud, Christian C ^a   Domínguez Rodríguez, Alejandro ^b   Smani, Tarik ^b   Hmadcha, Abdelkrim ^a,c   Soria, Bernat ^a,c  

^a CABIMER Andalusian Center for Molecular Biology and Regenerative Medicine CSIC University of Seville UPO   (Spain)

^b Instituto de Biomedicina de Sevilla   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN A; CELL PROTEIN; CYCLOPAMINE; GCG PROTEIN; HEPATOCYTE NUCLEAR FACTOR 3BETA; INS PROTEIN; ISL1 PROTEIN; NEUROGENIN 3; NOGGIN; POLYPHENOL; RESVERATROL; RETINOIC ACID; SST PROTEIN; TRANSCRIPTION FACTOR PDX 1; TRANSCRIPTION FACTOR SOX17; UNCLASSIFIED DRUG; STILBENE DERIVATIVE;

ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; DRUG MECHANISM; EMBRYO; EMBRYONIC STEM CELL; ENDODERM; HUMAN; HUMAN CELL; IN VIVO STUDY; INSULIN RELEASE; MALE; MOUSE; NONHUMAN; ORGANOGENESIS; PANCREAS ISLET BETA CELL; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; ANIMAL; CELL LINE; DIABETES MELLITUS, EXPERIMENTAL; DRUG EFFECTS; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE; TRANSPLANTATION; XENOGRAFT;

MUS; RICE STRIPE VIRUS;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; DIABETES MELLITUS, EXPERIMENTAL; EMBRYONIC STEM CELLS; HETEROGRAFTS; HUMANS; INSULIN-SECRETING CELLS; MICE; MICE, INBRED NOD; MICE, SCID; STILBENES;

EID: 84925018214     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0119904     Document Type: Article

References (67)

1. Hmadcha A, Dominguez-Bendala J, Wakeman J, Arredouani M, Soria B. The immune boundaries for stem cell based therapies: problems and prospective solutions. J Cell Mol Med. 2009;13:1464-1475. doi: 10.1111/j.1582-4934.2009.00837.x PMID: 19583810
2. Soria B, Roche E, Berna G, Leon-Quinto T, Reig JA, Martin F. Insulin-secreting cells derived from embryonic stem cells normalize glycemia in streptozotocin-induced diabetic mice. Diabetes. 2000;49:157-162. PMID: 10868930
3. Segev H, Fishman B, Ziskind A, Shulman M, Itskovitz-Eldor J. Differentiation of human embryonic stem cells into insulin-producing clusters. Stem Cells. 2004;22:265-274. PMID: 15153604
4. Rajagopal J, Anderson WJ, Kume S, Martinez OI, Melton DA. Insulin staining of ES cell progeny from insulin uptake. Science. 2003;299:363. PMID: 12532008
5. Leon-Quinto T, Jones J, Skoudy A, Burcin M, Soria B. In vitro directed differentiation of mouse embryonic stem cells into insulin-producing cells. Diabetologia. 2004;47:1442-1451. PMID: 15309294
6. Vaca P, Martin F, Vegara-Meseguer JM, Rovira JM, Berna G, Soria B. Induction of differentiation of embryonic stem cells into insulin-secreting cells by fetal soluble factors. Stem Cells. 2006;24:258-265. PMID: 16109755
7. Soria B. In-vitro differentiation of pancreatic beta-cells. Differentiation. 2001;68:205-219. PMID: 11776473
8. Bonal C, Herrera PL. Genes controlling pancreas ontogeny. Int J Dev Biol. 2008;52:823-835. doi: 10. 1387/ijdb.072444cb PMID: 18956314
9. Cano DA, Soria B, Martin F, Rojas A. Transcriptional control of mammalian pancreas organogenesis. Cell Mol Life Sci. 2014;71:2383-2402. doi: 10.1007/s00018-013-1510-2 PMID: 24221136
10. Champeris Tsaniras S, Jones PM. Generating pancreatic beta-cells from embryonic stem cells by manipulating signaling pathways. J Endocrinol. 2010;206:13-26. doi: 10.1677/JOE-10-0073 PMID: 20385725
11. Soria B, Pezzolla D, López J, Rojas A, Hmadcha A. Generation of Pancreatic Islets from Stem Cells. In: Lanza R, Langer R, Vacanti JP, editors. Principles of Tissue Engineering Fourth Edition. Elsevier B. V.; 2014. p. 837-847.
12. Rezania A, Bruin JE, Arora P, Rubin A, Batushansky I, Asadi A et al. Reversal of diabetes with insulinproducing cells derived in vitro from human pluripotent stem cells. Nat Biotechnol. 2014;32:1121-1133. doi: 10.1038/nbt.3033 PMID: 25211370
13. Pagliuca FW, Millman JR, Gurtler M, Segel M, Van Dervort A, Ryu JH, et al. Generation of Functional Human Pancreatic beta Cells In Vitro. Cell. 2014;159:428-439. doi: 10.1016/j.cell.2014.09.040 PMID: 25303535
14. Kroon E, Martinson LA, Kadoya K, Bang AG, Kelly OG, Eliazer S, et al. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol. 2008;26:443-452. doi: 10.1038/nbt1393 PMID: 18288110
15. Rezania A, Bruin JE, Riedel MJ, Mojibian M, Asadi A, Xu J, et al. Maturation of human embryonic stem cell-derived pancreatic progenitors into functional islets capable of treating pre-existing diabetes in mice. Diabetes. 2012;61:2016-2029. doi: 10.2337/db11-1711 PMID: 22740171
16. Rezania A, Bruin JE, Xu J, Narayan K, Fox JK, O'Neil JJ, et al. Enrichment of human embryonic stem cell-derived NKX6.1-expressing pancreatic progenitor cells accelerates the maturation of insulinsecreting cells in vivo. Stem Cells. 2013;31:2432-2442. doi: 10.1002/stem.1489 PMID: 23897760
17. Champeris Tsaniras S. Generating mature beta-cells from embryonic stem cells: strategies for latestage differentiation. Vitam Horm. 2011;87:79-92. doi: 10.1016/B978-0-12-386015-6.00025-1 PMID: 22127238
18. Nostro MC, Keller G. Generation of beta cells from human pluripotent stem cells: Potential for regenerative medicine. Semin Cell Dev Biol. 2012;23:701-710. doi: 10.1016/j.semcdb.2012.06.010 PMID: 22750147
19. Baetge EE. Production of beta-cells from human embryonic stem cells. Diabetes Obes Metab. 2008; (10 Suppl 4):186-194. doi: 10.1111/j.1463-1326.2008.00956.x PMID: 18834446
20. Schiesser JV, Wells JM. Generation of beta cells from human pluripotent stem cells: are we there yet? Ann N Y Acad Sci. 2014;1311:124-137. doi: 10.1111/nyas.12369 PMID: 24611778
21. Shiroi A, Yoshikawa M, Yokota H, Fukui H, Ishizaka S, Tatsumi K, et al. Identification of insulinproducing cells derived from embryonic stem cells by zinc-chelating dithizone. Stem Cells. 2002;20:284-292. PMID: 12110697
22. Basford CL, Prentice KJ, Hardy AB, Sarangi F, Micallef SJ, Li X, et al. The functional and molecular characterisation of human embryonic stem cell-derived insulin-positive cells compared with adult pancreatic beta cells. Diabetologia. 2012;55:358-371. doi: 10.1007/s00125-011-2335-x PMID: 22075915
23. Hrvatin S, O'Donnell CW, Deng F, Millman JR, Pagliuca FW, Dilorio P, et al. Differentiated human stem cells resemble fetal, not adult, beta cells. Proc Natl Acad Sci U S A. 2014;111:3038-3043. doi: 10. 1073/pnas.1400709111 PMID: 24516164
24. Bruin JE, Erener S, Vela J, Hu X, Johnson JD, Kurata HT, et al. Characterization of polyhormonal insulinproducing cells derived in vitro from human embryonic stem cells. Stem Cell Res. 2014;12:194-208. doi: 10.1016/j.scr.2013.10.003 PMID: 24257076
25. Vetterli L, Brun T, Giovannoni L, Bosco D, Maechler P. Resveratrol potentiates glucose-stimulated insulin secretion in INS-1E beta-cells and human islets through a SIRT1-dependent mechanism. J Biol Chem. 2011;286:6049-6060. doi: 10.1074/jbc. M110.176842 PMID: 21163946
26. Howitz KT, Bitterman KJ, Cohen HY, Lamming DW, Lavu S, Wood JG, et al. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature. 2003;425:191-196. PMID: 12939617
27. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, et al. Resveratrol improves health and survival of mice on a high-calorie diet. Nature. 2006;444:337-342. PMID: 17086191
28. Calvanese V, Lara E, Suarez-Alvarez B, Abu Dawud R, Vazquez-Chantada M, Martinez-Chantar ML, et al. Sirtuin 1 regulation of developmental genes during differentiation of stem cells. Proc Natl Acad Sci U S A. 2010;107:13736-13741. doi: 10.1073/pnas.1001399107 PMID: 20631301
29. Zhang Y, Jayaprakasam B, Seeram NP, Olson LK, De Witt D, Nair MG. Insulin secretion and cyclooxygenase enzyme inhibition by cabernet sauvignon grape skin compounds. J Agric Food Chem. 2004;52:228-233. PMID: 14733500
30. Bordone L, Motta MC, Picard F, Robinson A, Jhala US, Apfeld J, et al. Sirt1 regulates insulin secretion by repressing UCP2 in pancreatic beta cells. PLoS Biol. 2006;4:e31. PMID: 16366736
31. Affourtit C, Brand MD. Uncoupling protein-2 contributes significantly to high mitochondrial proton leak in INS-1E insulinoma cells and attenuates glucose-stimulated insulin secretion. Biochem J. 2008;409:199-204. PMID: 17824844
32. Moynihan KA, Grimm AA, Plueger MM, Bernal-Mizrachi E, Ford E, Cras-Meneur C, et al. Increased dosage of mammalian Sir2 in pancreatic beta cells enhances glucose-stimulated insulin secretion in mice. Cell Metab. 2005;2:105-117. PMID: 16098828
33. Fiori JL, Shin YK, Kim W, Krzysik-Walker SM, Gonzalez-Mariscal I, Carlson OD, et al. Resveratrol prevents beta-cell dedifferentiation in nonhuman primates given a high-fat/high-sugar diet. Diabetes. 2013;62:3500-3513. doi: 10.2337/db13-0266 PMID: 23884882
34. Xie S, Sinha RA, Singh BK, Li GD, Han W, Yen PM. Resveratrol induces insulin gene expression in mouse pancreatic alpha-cells. Cell Biosci. 2013;3:47. doi: 10.1186/2045-3701-3-47 PMID: 24330680
35. D'Amour KA, Bang AG, Eliazer S, Kelly OG, Agulnick AD, Smart NG, et al. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat Biotechnol. 2006;24:1392-1401. PMID: 17053790
36. Shim JH, Kim SE, Woo DH, Kim SK, Oh CH, McKay R, et al. Directed differentiation of human embryonic stem cells towards a pancreatic cell fate. Diabetologia. 2007;50:1228-1238. PMID: 17457565
37. Jiang W, Shi Y, Zhao D, Chen S, Yong J, Zhang J, et al. In vitro derivation of functional insulinproducing cells from human embryonic stem cells. Cell Res. 2007;17:333-344. PMID: 17426693
38. Jiang J, Au M, Lu K, Eshpeter A, Korbutt G, Fisk G, et al. Generation of insulin-producing islet-like clusters from human embryonic stem cells. Stem Cells. 2007;25:1940-1953. PMID: 17510217
39. Zhang D, Jiang W, Liu M, Sui X, Yin X, Chen S, et al. Highly efficient differentiation of human ES cells and iPS cells into mature pancreatic insulin-producing cells. Cell Res. 2009;19:429-438. doi: 10.1038/cr.2009.28 PMID: 19255591
40. Borriello A, Cucciolla V, Della Ragione F, Galletti P. Dietary polyphenols: focus on resveratrol, a promising agent in the prevention of cardiovascular diseases and control of glucose homeostasis. Nutr Metab Cardiovasc Dis. 2010;20:618-625. doi: 10.1016/j.numecd.2010.07.004 PMID: 20850033
41. Szkudelski T, Szkudelska K. Anti-diabetic effects of resveratrol. Ann N Y Acad Sci. 2011;1215:34-39. doi: 10.1111/j.1749-6632.2010.05844.x PMID: 21261639
42. Chen WP, Chi TC, Chuang LM, Su MJ. Resveratrol enhances insulin secretion by blocking K (ATP) and K (V) channels of beta cells. Eur J Pharmacol. 2007;568:269-277. PMID: 17573071
43. Affourtit C, Brand MD. On the role of uncoupling protein-2 in pancreatic beta cells. Biochim Biophys Acta. 2008;1777:973-979. doi: 10.1016/j.bbabio.2008.03.022 PMID: 18433713
44. Azzu V, Affourtit C, Breen EP, Parker N, Brand MD. Dynamic regulation of uncoupling protein 2 content in INS-1E insulinoma cells. Biochim Biophys Acta. 2008;1777:1378-1383. doi: 10.1016/j.bbabio.2008. 07.001 PMID: 18692019
45. Brand MD, Parker N, Affourtit C, Mookerjee SA, Azzu V. Mitochondrial uncoupling protein 2 in pancreatic beta-cells. Diabetes Obes Metab. 2010; (12 Suppl 2):134-140. doi: 10.1111/j.1463-1326.2010. 01264.x PMID: 21029310
46. Hay DC, Fletcher J, Payne C, Terrace JD, Gallagher RC, Snoeys J, et al. Highly efficient differentiation of hESCs to functional hepatic endoderm requires ActivinA and Wnt3a signaling. Proc Natl Acad Sci U S A. 2008;105:12301-12306. doi: 10.1073/pnas.0806522105 PMID: 18719101
47. Sulzbacher S, Schroeder IS, Truong TT, Wobus AM. Activin A-induced differentiation of embryonic stem cells into endoderm and pancreatic progenitors-the influence of differentiation factors and culture conditions. Stem Cell Rev. 2009;5:159-173. doi: 10.1007/s12015-009-9061-5 PMID: 19263252
48. Loh KM, Ang LT, Zhang J, Kumar V, Ang J, Auyeong JQ, et al. Efficient endoderm induction from human pluripotent stem cells by logically directing signals controlling lineage bifurcations. Cell Stem Cell. 2014;14:237-252. doi: 10.1016/j.stem.2013.12.007 PMID: 24412311
49. Guo S, Mao X, He F, Liu H, Ming L. Activin A supplement in the hESCs culture enhances the endoderm differentiation efficiency. Cell Biol Int. 2014;38:849-856. doi: 10.1002/cbin. 10274 PMID: 24604611
50. D'Amour KA, Agulnick AD, Eliazer S, Kelly OG, Kroon E, Baetge EE. Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat Biotechnol. 2005;23:1534-1541. PMID: 16258519
51. Johannesson M, Stahlberg A, Ameri J, Sand FW, Norrman K, Semb H. FGF4 and retinoic acid direct differentiation of hESCs into PDX1-expressing foregut endoderm in a time- and concentrationdependent manner. PLoS One. 2009;4:e4794. doi: 10.1371/journal.pone.0004794 PMID: 19277121
52. Ameri J, Stahlberg A, Pedersen J, Johansson JK, Johannesson MM, Artner I, et al. FGF2 specifies hESC-derived definitive endoderm into foregut/midgut cell lineages in a concentration-dependent manner. Stem Cells. 2010;28:45-56. doi: 10.1002/stem.249 PMID: 19890880
53. Kim SK, Melton DA. Pancreas development is promoted by cyclopamine, a hedgehog signaling inhibitor. Proc Natl Acad Sci U S A. 1998;95:13036-13041. PMID: 9789036
54. Schulz TC, Young HY, Agulnick AD, Babin MJ, Baetge EE, Bang AG, et al. A scalable system for production of functional pancreatic progenitors from human embryonic stem cells. PLoS One. 2012;7:e37004. doi: 10.1371/journal.pone.0037004 PMID: 22623968
55. Hou X, Xu S, Maitland-Toolan KA, Sato K, Jiang B, Ido Y, et al. SIRT1 regulates hepatocyte lipid metabolism through activating AMP-activated protein kinase. J Biol Chem. 2008;283:20015-20026. doi: 10. 1074/jbc. M802187200 PMID: 18482975
56. Dasgupta B, Milbrandt J. Resveratrol stimulates AMP kinase activity in neurons. Proc Natl Acad Sci U S A. 2007;104:7217-7222. PMID: 17438283
57. Crandall JP, Barzilai N. Exploring the promise of resveratrol: where do we go from here? Diabetes. 2013;62:1022-1023. doi: 10.2337/db12-1788 PMID: 23520278
58. Price NL, Gomes AP, Ling AJ, Duarte FV, Martin-Montalvo A, North BJ, et al. SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab. 2012;15:675-690. doi: 10.1016/j.cmet.2012.04.003 PMID: 22560220
59. Elrick LJ, Docherty K. Phosphorylation-dependent nucleocytoplasmic shuttling of pancreatic duodenal homeobox-1. Diabetes. 2001;50:2244-2252. PMID: 11574405
60. Watanabe H, Saito H, Nishimura H, Ueda J, Evers BM. Activation of phosphatidylinositol-3 kinase regulates pancreatic duodenal homeobox-1 in duct cells during pancreatic regeneration. Pancreas. 2008;36:153-159. doi: 10.1097/MPA.0b013e318157753e PMID: 18376306
61. Patel KR, Scott E, Brown VA, Gescher AJ, Steward WP, Brown K. Clinical trials of resveratrol. Ann N Y Acad Sci. 2011;1215:161-169. doi: 10.1111/j.1749-6632.2010.05853.x PMID: 21261655
62. Brasnyo P, Molnar GA, Mohas M, Marko L, Laczy B, Cseh J, et al. Resveratrol improves insulin sensitivity, reduces oxidative stress and activates the Akt pathway in type 2 diabetic patients. Br J Nutr. 2011;106:383-389. doi: 10.1017/S0007114511000316 PMID: 21385509
63. Crandall JP, Oram V, Trandafirescu G, Reid M, Kishore P, Hawkins M, et al. Pilot study of resveratrol in older adults with impaired glucose tolerance. J Gerontol A Biol Sci Med Sci. 2012;67:1307-1312. doi: 10.1093/gerona/glr235 PMID: 22219517
64. Bashmakov YK, Assaad-Khalil SH, Abou Seif M, Udumyan R, Megallaa M, Rohoma KH, et al. Resveratrol promotes foot ulcer size reduction in type 2 diabetes patients. ISRN Endocrinol. 2014;2014:816307. doi: 10.1155/2014/816307 PMID: 24701359
65. Hovatta O, Mikkola M, Gertow K, Stromberg AM, Inzunza J, Hreinsson J, et al. A culture system using human foreskin fibroblasts as feeder cells allows production of human embryonic stem cells. Hum Reprod. 2003;18:1404-1409. PMID: 12832363
66. Merglen A, Theander S, Rubi B, Chaffard G, Wollheim CB, Maechler P. Glucose sensitivity and metabolism-secretion coupling studied during two-year continuous culture in INS-1E insulinoma cells. Endocrinology. 2004;145:667-678. PMID: 14592952
67. Lachaud CC, Pezzolla D, Dominguez-Rodriguez A, Smani T, Soria B, Hmadcha A. Functional vascular smooth muscle-like cells derived from adult mouse uterine mesothelial cells. PLoS One. 2013;8:e55181. doi: 10.1371/journal.pone.0055181 PMID: 23405120