Concise review: Pluripotent stem cell-based regenerative applications for failing β-cell function

Stem Cells Translational Medicine

Volumn 3, Issue 5, 2014, Pages 653-661

  Holditch, Sara J ^a   Terzic, Andre ^a,b   Ikeda, Yasuhiro ^a  

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

Diabetes mellitus; Regenerative medicine; Stem cells; Translation; Transplantation

Indexed keywords

4 [4 (1, 3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL] BENZAMIDE; ACTIVIN A; BONE MORPHOGENETIC PROTEIN 4; C PEPTIDE; CHEMOKINE RECEPTOR CXCR4; CYCLOPAMINE; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 10; FIBROBLAST GROWTH FACTOR 2; GLUCAGON LIKE PEPTIDE 1; HEPATOCYTE NUCLEAR FACTOR 3BETA; INDOLACTAM V; INSULIN; NEUROGENIN 3; NICOTINAMIDE; NOGGIN; PROTEIN KINASE C; RETINOIC ACID; SELENIUM; SOMATOMEDIN; TRANSCRIPTION FACTOR MAFA; TRANSCRIPTION FACTOR NKX6.1; TRANSCRIPTION FACTOR PDX 1; TRANSCRIPTION FACTOR SOX17; TRANSFERRIN; TRANSFORMING GROWTH FACTOR; UNCLASSIFIED DRUG; UNINDEXED DRUG; UROCORTIN III; VASCULOTROPIN;

ADULT STEM CELL; ARTICLE; BIOSAFETY; CELL DIFFERENTIATION; CELL FUNCTION; CELL LOSS; CELL POPULATION; CELL REGENERATION; CELL RENEWAL; CLONAL VARIATION; DIABETES MELLITUS; DNA MODIFICATION; EMBRYONIC STEM CELL; ENDODERM; EPIGENETICS; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; HUMAN; IMMUNOGENICITY; IMMUNOSUPPRESSIVE TREATMENT; INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; NUCLEAR REPROGRAMMING; PANCREAS ISLET BETA CELL; PATHOGENESIS; PLURIPOTENT STEM CELL; RECURRENT DISEASE; REGENERATIVE MEDICINE; SOMATIC CELL; STEM CELL TRANSPLANTATION; TERATOMA;

DIABETES MELLITUS; REGENERATIVE MEDICINE; STEM CELLS; TRANSLATION; TRANSPLANTATION;

ANIMALS; DIABETES MELLITUS; EMBRYONIC STEM CELLS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; INSULIN-SECRETING CELLS; REGENERATIVE MEDICINE; STEM CELL TRANSPLANTATION;

EID: 84899683694     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2013-0184     Document Type: Article

References (107)

1. Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract 2010;87:4-14.
2. Terzic A, Waldman S. Chronic diseases: The emerging pandemic. Clin Transl Sci 2011; 4:225-226.
3. Butler AE, Galasso R, Meier JJ et al. Modestly increased beta cell apoptosis but no increased beta cell replication in recent-onset type 1 diabetic patients who died of diabetic ketoacidosis. Diabetologia 2007;50:2323-2331.
4. Xiao X, Chen Z, Shiota C et al. No evidence for b cell neogenesis in murine adult pancreas. J Clin Invest 2013;123:2207-2217.
5. Kushner JA. The role of aging upon b cell turnover. J Clin Invest 2013;123:990-995.
6. Butler AE, Janson J, Bonner-Weir S et al. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 2003;52:102-110.
7. Drucker DJ, Nauck MA. The incretin system: Glucagon-like peptide-1 receptor agonists and dipeptidyl peptidase-4 inhibitors in type 2 diabetes. Lancet 2006;368:1696-1705.
8. Ricordi C, Inverardi L, Domínguez-Bendala J. From cellular therapies to tissue reprogramming and regenerative strategies in the treatment of diabetes. Regen Med 2012;7:41-48.
9. Shapiro AM, Ricordi C, Hering BJ et al. International trial of the Edmonton protocol for islet transplantation. N Engl J Med 2006;355: 1318-1330.
10. Ryan EA, Paty BW, Senior PA et al. Fiveyear follow-up after clinical islet transplantation. Diabetes 2005;54:2060-2069.
11. Barton FB, Rickels MR, Alejandro R et al. Improvement in outcomes of clinical islet transplantation: 1999-2010. Diabetes Care 2012;35: 1436-1445.
12. Bellin MD, Kandaswamy R, Parkey J et al. Prolonged insulin independence after islet allotransplants in recipients with type 1 diabetes. Am J Transplant 2008;8:2463-2470.
13. BellinMD, Barton FB, HeitmanA et al. Potent induction immunotherapy promotes longterm insulin independence after islet transplantation in type 1 diabetes. Am J Transplant 2012; 12:1576-1583.
14. Johnson PR, Jones KE. Pancreatic islet transplantation. Semin Pediatr Surg 2012;21: 272-280.
15. Ludwig B, Reichel A, SteffenAet al. Transplantation ofhumanislets withoutimmunosuppression. Proc Natl Acad Sci USA 2013;110: 19054-19058.
16. Smink AM, Faas MM, de Vos P. Toward engineering a novel transplantation site for human pancreatic islets. Diabetes 2013;62:1357-1364.
17. Sutherland DE, Radosevich DM, Bellin MD et al. Total pancreatectomy and islet autotransplantation for chronic pancreatitis. J Am Coll Surg 2012;214:409-424; discussion 424-426.
18. Matsumoto S, Okitsu T, Iwanaga Y et al. Insulin independence after living-donor distal pancreatectomy and islet allotransplantation. Lancet 2005;365:1642-1644.
19. Hering BJ, Wijkstrom M, Graham ML et al. Prolonged diabetes reversal after intraportal xenotransplantation of wild-type porcine islets in immunosuppressed nonhuman primates. Nat Med 2006;12:301-303.
20. Chhabra P, Brayman KL. Stem cell therapy to cure type 1 diabetes: From hype to hope. STEM CELLS TRANSLATIONAL MEDICINE 2013;2: 328-336.
21. Domínguez-Bendala J, Lanzoni G, Inverardi L et al. Concise review: Mesenchymal stem cells for diabetes. STEM CELLS TRANSLATIONALMEDICINE 2012;1:59-63.
22. Aguayo-Mazzucato C, Bonner-Weir S. Stem cell therapy for type 1 diabetes mellitus. Nat Rev Endocrinol 2010;6:139-148.
23. Abdi R, Fiorina P, Adra CN et al. Immunomodulation by mesenchymal stem cells: A potential therapeutic strategy for type 1 diabetes. Diabetes 2008;57:1759-1767.
24. Staeva TP, Chatenoud L, Insel R et al. Recent lessons learned from prevention and recent-onset type 1 diabetes immunotherapy trials. Diabetes 2013;62:9-17.
25. Hematti P, Kim J, Stein AP et al. Potential role of mesenchymal stromal cells in pancreatic islet transplantation. Transplant Rev (Orlando) 2013;27:21-29.
26. Lanzoni G, Oikawa T, Wang Y et al. Concise review: Clinical programs of stem cell therapies for liver and pancreas. STEM CELLS 2013;31: 2047-2060.
27. Lysy PA, Weir GC, Bonner-Weir S. Concise review: Pancreas regeneration: Recent advances and perspectives. STEM CELLS TRANSLATIONAL MEDICINE 2012;1:150-159.
28. Soria B, Roche E, Berná G et al. Insulinsecreting cells derived fromembryonic stemcells normalize glycemia in streptozotocin-induced diabetic mice. Diabetes 2000;49:157-162.
29. León-Quinto T, Jones J, Skoudy A et al. In vitro directed differentiation of mouse embryonic stem cells into insulin-producing cells. Diabetologia 2004;47:1442-1451.
30. Lumelsky N, Blondel O, Laeng P et al. Differentiation of embryonic stem cells to insulinsecreting structures similar to pancreatic islets. Science 2001;292:1389-1394.
31. Rajagopal J, Anderson WJ, Kume S et al. Insulin staining of ES cell progeny from insulin uptake. Science 2003;299:363.
32. Schroeder IS, Rolletschek A, Blyszczuk P et al. Differentiation of mouse embryonic stem cells to insulin-producing cells. Nat Protoc 2006; 1:495-507.
33. 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.
34. Borowiak M, Maehr R, Chen S et al. Small molecules efficiently direct endodermal differentiation of mouse and human embryonic stem cells. Cell Stem Cell 2009;4:348-358.
35. McLean AB, D'Amour KA, Jones KL et al. Activin A efficiently specifies definitive endoderm from human embryonic stem cells only when phosphatidylinositol 3-kinase signaling is suppressed. STEM CELLS 2007;25:29-38.
36. Kubo A, Shinozaki K, Shannon JM et al. Development of definitive endoderm from embryonic stem cells in culture. Development 2004;131:1651-1662.
37. D'Amour KA, Agulnick AD, Eliazer S et al. Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat Biotechnol 2005;23:1534-1541.
38. Yasunaga M, Tada S, Torikai-Nishikawa S et al. Induction and monitoring of definitive and visceral endoderm differentiation of mouse ES cells. Nat Biotechnol 2005;23:1542-1550.
39. D'Amour KA, Bang AG, Eliazer S et al. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat Biotechnol 2006;24:1392-1401.
40. Ameri J, Stahlberg A, Pedersen J et al. FGF2 specifies hESC-derived definitive endoderm into foregut/midgut cell lineages in a concentration-dependent manner. STEM CELLS 2010;28:45-56.
41. Jiang J, Au M, Lu K et al. Generation of insulin-producing islet-like clusters fromhuman embryonic stem cells. STEM CELLS 2007;25: 1940-1953.
42. Jiang W, Shi Y, Zhao D et al. In vitro derivation of functional insulin-producing cells from human embryonic stem cells. Cell Res 2007;17:333-344.
43. Mfopou JK, Chen B, Mateizel I et al. Noggin, retinoids, and fibroblast growth factor regulate hepatic or pancreatic fate of human embryonic stem cells. Gastroenterology 2010; 138:2233-2245, 2245. e1-14.
44. Nostro MC, Sarangi F, Ogawa S et al. Stage-specific signaling through TGFb family members and WNT regulates patterning and pancreatic specification of human pluripotent stem cells. Development 2011;138:861-871.
45. Rezania A, Riedel MJ, Wideman RD et al. Production of functional glucagon-secreting a-cells from human embryonic stem cells. Diabetes 2011;60:239-247.
46. Rezania A, Bruin JE, Riedel MJ 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.
47. Xu X, Browning VL, Odorico JS. Activin, BMP and FGF pathways cooperate to promote endoderm and pancreatic lineage cell differentiation fromhumanembryonic stem cells. Mech Dev 2011;128:412-427.
48. Gadue P, Huber TL, Paddison PJ et al. Wnt and TGF-beta signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells. Proc Natl Acad Sci USA 2006;103:16806-16811.
49. Micallef SJ, Li X, Schiesser JV et al. INS (GFP/w) human embryonic stem cells facilitate isolation of in vitro derived insulin-producing cells. Diabetologia 2012;55:694-706.
50. Basford CL, Prentice KJ, Hardy AB et al. The functional and molecular characterisation of humanembryonic stemcell-derived insulin-positive cells compared with adult pancreatic beta cells. Diabetologia 2012;55:358-371.
51. Xie R, Everett LJ, Lim HW et al. Dynamic chromatin remodeling mediated by polycomb proteins orchestrates pancreatic differentiation of human embryonic stem cells. Cell Stem Cell 2013;12:224-237.
52. Chen S, Borowiak M, Fox JL et al. A small molecule that directs differentiation of human ESCs into the pancreatic lineage. Nat Chem Biol 2009;5:258-265.
53. Tachibana M, Amato P, SparmanMet al. Human embryonic stem cells derived by somatic cell nuclear transfer. Cell 2013;153:1228-1238.
54. Takahashi K, Yamanaka S. Induced pluripotent stem cells in medicine and biology. Development 2013;140:2457-2461.
55. Robinton DA, Daley GQ. The promise of induced pluripotent stem cells in research and therapy. Nature 2012;481:295-305.
56. Takahashi K, Tanabe K, OhnukiMet al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131:861-872.
57. Yu J, Hu K, Smuga-Otto K et al. Human induced pluripotent stem cells free of vector and transgene sequences. Science 2009;324: 797-801.
58. Ohmine S, Dietz AB, Deeds MC et al. Induced pluripotent stem cells from GMP-grade hematopoietic progenitor cells and mononuclear myeloid cells. Stem Cell Res Ther 2011; 2:46.
59. Thatava T, Armstrong AS, De Lamo JG et al. Successful disease-specific induced pluripotent stem cell generation from patients with kidney transplantation. Stem Cell Res Ther 2011;2:48.
60. Terzic A, Nelson TJ. Regenerative medicine primer. Mayo Clin Proc 2013;88:766-775.
61. Park IH, Arora N, Huo H et al. Diseasespecific induced pluripotent stem cells. Cell 2008;134:877-886.
62. Ebert AD, Yu J, Rose FF Jr et al. Induced pluripotentstem cells from a spinal muscular atrophy patient. Nature 2009;457:277-280.
63. Lee TH, Song SH, Kim KL et al. Functional recapitulation of smooth muscle cells via induced pluripotent stem cells from human aortic smooth muscle cells. Circ Res 2010;106: 120-128.
64. Carvajal-Vergara X, Sevilla A, D'Souza SL et al. Patient-specific induced pluripotent stemcell-derived models of LEOPARD syndrome. Nature 2010;465:808-812.
65. Ohmine S, Squillace KA, Hartjes KA et al. Reprogrammedkeratinocytes from elderly type 2 diabetes patients suppress senescence genes to acquire induced pluripotency. Aging (Albany NY) 2012;4:60-73.
66. Thatava T, Nelson TJ, Edukulla R et al. Indolactam V/GLP-1-mediated differentiation of human iPS cells into glucose-responsive insulin-secreting progeny. Gene Ther 2011;18: 289-293.
67. Kudva YC, Ohmine S, Greder LV et al. Transgene-free disease-specific induced pluripotent stem cells from patients with type 1 and type 2 diabetes. STEM CELLS TRANSLATIONAL MEDICINE 2012;1:451-461.
68. Maehr R, Chen S, SnitowM et al. Generation of pluripotent stem cells from patients with type 1 diabetes. Proc Natl Acad Sci USA 2009;106:15768-15773.
69. Thatava T, Kudva YC, Edukulla R et al. Intrapatient variations in type 1 diabetesspecific iPS cell differentiation into insulinproducing cells. Mol Ther 2013;21:228-239.
70. Hua H, Shang L, Martinez H et al. iPSCderived b cells model diabetes due to glucokinase deficiency. J Clin Invest 2013;123: 3146-3153.
71. Hussein SM, Batada NN, Vuoristo S et al. Copy number variation and selection during reprogramming to pluripotency. Nature 2011; 471:58-62.
72. Gore A, Li Z, Fung HL et al. Somatic coding mutations in human induced pluripotent stem cells. Nature 2011;471:63-67.
73. Lister R, Pelizzola M, Dowen RH et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009;462:315-322.
74. Mayshar Y, Ben-David U, Lavon N et al. Identification and classification of chromosomal aberrations in human induced pluripotent stem cells. Cell Stem Cell 2010;7:521-531.
75. Zhao T, Zhang ZN, Rong Z et al. Immunogenicity of induced pluripotent stem cells. Nature 2011;474:212-215.
76. Araki R, UdaM, Hoki Y et al. Negligible immunogenicity of terminally differentiated cells derived from induced pluripotent or embryonic stem cells. Nature 2013;494:100-104.
77. Hattori F, Chen H, YamashitaHet al. Nongenetic method for purifying stem cell-derived cardiomyocytes. Nat Methods 2010;7:61-66.
78. Darabi R, Gehlbach K, Bachoo RM et al. Functional skeletal muscle regeneration from differentiating embryonic stem cells. Nat Med 2008;14:134-143.
79. Sakuma T, Barry MA, Ikeda Y. Lentiviral vectors: Basic to translational. Biochem J 2012;443:603-618.
80. Okita K, Ichisaka T, Yamanaka S. Generation of germline-competent induced pluripotent stem cells. Nature 2007;448:313-317.
81. Osafune K, Caron L, Borowiak M et al. Marked differences in differentiation propensity among human embryonic stem cell lines. Nat Biotechnol 2008;26:313-315.
82. Bock C, Kiskinis E, VerstappenGet al. Reference maps of human ES and iPS cell variation enable high-throughput characterization of pluripotent cell lines. Cell 2011;144:439-452.
83. Tateishi K, He J, Taranova O et al. Generation of insulin-secreting islet-like clusters from human skin fibroblasts. J Biol Chem 2008;283: 31601-31607.
84. Thatava T, Nelson TJ, Edukulla R et al. Indolactam V/GLP-1-mediated differentiation of human iPS cells into glucose-responsive insulinsecreting progeny. Gene Ther 2011;18:283-293.
85. Rezania A, Bruin JE, Xu J et al. Enrichment of human embryonic stem cell-derived NKX6.1-expressing pancreatic progenitor cells accelerates the maturation of insulin-secreting cells in vivo. STEM CELLS 2013;31:2432-2442.
86. Kroon E, Martinson LA, Kadoya K et al. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo. Nat Biotechnol 2008;26:443-452.
87. Sibley RK, Sutherland DE, Goetz F et al. Recurrent diabetes mellitus in the pancreas iso-and allograft: A light and electron microscopic and immunohistochemical analysis of four cases. Lab Invest 1985;53:132-144.
88. Sibley RK, Sutherland DE. Pancreas transplantation: An immunohistologic and histopathologic examination of 100 grafts. Am J Pathol 1987;128:151-170.
89. Huurman VA, Hilbrands R, Pinkse GG et al. Cellular islet autoimmunity associates with clinical outcome of islet cell transplantation. PLoS One 2008;3:e2435.
90. Seki T, Yuasa S, Fukuda K. Generation of induced pluripotent stem cells from a small amountofhumanperipheral blood using a combination of activated T cells and Sendai virus. Nat Protoc 2012;7:718-728.
91. Stadtfeld M, Nagaya M, Utikal J et al. Induced pluripotent stem cells generated without viral integration. Science 2008;322:945-949.
92. Warren L, Manos PD, Ahfeldt T et al. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 2010;7: 618-630.
93. Anokye-Danso F, Trivedi CM, Juhr D et al. Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 2011;8:376-388.
94. Aasen T, Raya A, Barrero MJ et al. Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes. Nat Biotechnol 2008;26:1276-1284.
95. Loh YH, Agarwal S, Park IH et al. Generation of induced pluripotent stem cells from human blood. Blood 2009;113:5476-5479.
96. Hanna J, Markoulaki S, Schorderet P et al. Direct reprogramming of terminally differentiated mature B lymphocytes to pluripotency. Cell 2008;133:250-264.
97. Miura K, Okada Y, Aoi T et al. Variation in the safety of induced pluripotent stem cell lines. Nat Biotechnol 2009;27:743-745.
98. Cahan P, Daley GQ. Origins and implications of pluripotent stem cell variability and heterogeneity. Nat Rev Mol Cell Biol 2013;14:357-368.
99. Li C, Chen P, Vaughan J et al. Urocortin 3 regulates glucose-stimulated insulin secretion and energy homeostasis. Proc Natl Acad Sci USA 2007;104:4206-4211.
100. BlumB, Hrvatin SS, SchuetzCet al. Functional beta-cell maturation is marked by an increased glucose threshold and by expression of urocortin 3. Nat Biotechnol 2012;30: 261-264.
101. Hawdon JM, Aynsley-Green A, Alberti KG et al. The role of pancreatic insulin secretion in neonatal glucoregulation. I. Healthy term and preterm infants. Arch Dis Child 1993;68(3 Spec No):274-279.
102. Tuch BE, Jones A, Turtle JR. Maturation of the response of human fetal pancreatic explants to glucose. Diabetologia 1985;28: 28-31.
103. Espinosa de los M, Driscoll SG, Steinke J. Insulin release from isolated human fetal pancreatic islets. Science 1970;168:1111-1112.
104. Aguayo-Mazzucato C, Zavacki AM, Marinelarena A et al. Thyroid hormone promotes postnatal rat pancreatic b-cell development and glucose-responsive insulin secretion through MAFA. Diabetes 2013;62: 1569-1580.
105. Banga A, Akinci E, Greder LV et al. In vivo reprogramming of Sox9+ cells in the liver to insulin-secreting ducts. Proc Natl Acad Sci USA 2012;109:15336-15341.
106. Zhou Q, Brown J, Kanarek A et al. In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 2008;455:627-632.
107. Wang AY, Ehrhardt A, Xu H et al. Adenovirus transduction is required for the correction of diabetes using Pdx-1 or Neurogenin-3 in the liver. Mol Ther 2007;15:255-263.