Stem cells for the cell and molecular therapy of type 1 diabetes mellitus (T1D): The gap between dream and reality

American Journal of Stem Cells

Volumn 4, Issue 1, 2015, Pages 22-31

  Calafiore, Riccardo ^a   Basta, Giuseppe ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

Author keywords

Blood glucose; Complications; Insulin; Reversal

Indexed keywords

ADIPOCYTOKINE; NEUROGENIC DIFFERENTIATION FACTOR; NEUROGENIN 3; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ARX; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR PAX4; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR PDX 1; UNCLASSIFIED DRUG;

ADIPOSE TISSUE; ADULT STEM CELL; ALLOGRAFT; CELL DIFFERENTIATION; CELL REGENERATION; CELL SURVIVAL; CELL TRANSPLANTATION; CLINICAL TRIAL (TOPIC); EMBRYONIC STEM CELL; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; HEMATOPOIETIC STEM CELL; HORMONE SUBSTITUTION; HUMAN; IMMUNITY; IMMUNOGENICITY; IMMUNOSUPPRESSIVE TREATMENT; INSULIN DEPENDENT DIABETES MELLITUS; MESENCHYMAL STEM CELL; MICROENCAPSULATION; MOLECULAR THERAPY; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS TRANSPLANTATION; PLURIPOTENT STEM CELL; QUALITY OF LIFE; REVIEW; STEM CELL;

EID: 85015139014     PISSN: None     EISSN: 21604150     Source Type: Journal    
DOI: None     Document Type: Review

References (80)

1. Bluestone JA, Herold K and Eisenbarth G. Genetics, pathogenesis and clinical interventions in type 1 diabetes. Nature 2010; 464: 1293-1300.
2. Ashcroft FM and Rorsman P. Diabetes mellitus and the β cell: the last ten years. Cell 2012; 148: 1160-1171.
3. Jensen RA, Agardh E, Lernmark A, Gudbjörnsdottir S, Smith NL, Siscovick DS, Törn C and DISS Group. HLA genes, islet auto antibodies and residual C-peptide at the clinical onset of type 1 diabetes mellitus and the risk of retinopathy 15 years later. PLoS One 2011; 6: e17569.
4. Cefalu WT. American diabetes association-European association for the study of diabetes position statement: due diligence was conducted. Diabetes Care 2012; 35: 1201-1203.
5. CITR Research Group. 2007 Update on allogeneic islet transplantation from the Collaborative Islet Transplant Registry (CITR). Cell Transplant 2009; 18: 753-767.
6. Balamurugan AN, Naziruddin B, Lockridge A, Tiwari M, Loganathan G, Takita M, Matsumoto S, Papas K, Trieger M, Rainis H, Kin T, Kay TW, Wease S, Messinger S, Ricordi C, Alejandro R, Markmann J, Kerr-Conti J, Rickels MR, Liu C, Zhang X, Witkowski P, Posselt A, Maffi P, Secchi A, Berney T, O’Connell PJ, Hering BJ and Barton FB. Islet product characteristics and factors related to successful human islet transplantation from the Collaborative Islet Transplant Registry (CITR) 1999-2010. Am J Transplant 2014; 14: 2595-2606.
7. Nilsson B, Ekdahl KN and Korsgren O. Control of instant blood-mediated inflammatory reaction to improve islets of Langerhans engraftment. Curr Opin Organ Transplant 2011; 16: 620-626.
8. Murua A, Portero A, Orive G, Hernández RM, de Castro M and Pedraz JL. Cell microencapsulation technology: towards clinical application. J Control Release 2008; 132: 76-83.
9. Elliott RB, Escobar L, Tan PL, Muzina M, Zwain S and Buchanan C. Live encapsulated porcine islets from a type 1 diabetic patient 9.5 yr after xenotransplantation. Xenotransplantation 2007; 14: 157-161.
10. Dufrane D and Gianello P. Pig islet xenotransplantation into non-human primate model. Transplantation 2008; 86: 753-760.
11. Calafiore R, Basta G, Luca G, Lemmi A, Montanucci MP, Calabrese G, Racanicchi L, Mancuso F and Brunetti P. Microencapsulated pancreatic islet allografts into nonimmunosuppressed patients with type 1 diabetes: first two cases. Diabetes Care 2006; 29: 137-138.
12. Basta G, Montanucci P, Luca G, Boselli C, Noya G, Barbaro B, Qi M, Kinzer KP, Oberholzer J and Calafiore R. Long-term metabolic and immunological follow-up of nonimmunosuppressed patients with type 1 diabetes treated with microencapsulated islet allografts: four cases. Diabetes Care 2011; 34: 2406-2409.
13. Puri S and Hebrok M. Cellular plasticity within the pancreas--lessons learned from development. Dev Cell 2010; 18: 342-356.
14. Shao S, Fang Z, Yu X and Zhang M. Transcription factors involved in glucose-stimulated insulin secretion of pancreatic beta cells. Biochem Biophys Res Commun 2009; 384: 401-404.
15. Burlison JS, Long Q, Fujitani Y, Wright CV and Magnuson MA. Pdx-1 and Ptf1a concurrently determine the fate specification of pancreatic multipotent progenitor cells. Dev Biol 2008; 316: 74-86.
16. Kawaguchi Y, Cooper B, Gannon M, Ray M, MacDonald RJ and Wright CV. The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat Genet 2002; 32: 128-134.
17. Sellick GS, Barker KT, Stolte-Dijkstra I, Fleischmann C, Coleman RJ, Garrett C, Gloyn AL, Edghill EL, Hattersley AT, Wellauer PK, Goodwin G and Houlston RS. Mutations in PTF1A cause pancreatic and cerebellar agenesis. Nat Genet 2004; 36: 1301-1305.
18. Gradwohl G, Dierich A, LeMeur M and Guillemot F. Neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas. Proc Natl Acad Sci U S A 2000; 97: 1607-1611.
19. Sussel L, Kalamaras J, Hartingan-O’Connor DJ, Meneses JJ, Pedersen RA, Rubenstein JL and German MS. Mice lacking the homeodomain transcription factor Nkx2.2 have diabetes due to arrested differentiation of pancreatic beta cells. Development 1998; 125: 2213-2221.
20. Servitja JM and Ferrer J. Transcriptional networks controlling pancreatic development and beta cell function. Diabetologia 2004; 47: 597-613.
21. Soria B, Roche E, Berná G, León-Quinto T, Reig JA and Martín F. Insulin secreting cells derived from embryonic stem cells normalize glycemia in streptozotocin-induced diabetic mice. Diabetes 2000; 49: 157-162.
22. Lumelsky N, Blondel O, Laeng P, Velasco I, Ravin R and McKay R. Differentiation of embryonic stem cells to insulin secreting structures similar to pancreatic islets. Science 2001; 292: 1389-1394.
23. Sipione S, Eshpeter A, Lyon JG, Korbutt GS and Blackely RC. Insulin expressing cells from differentiated embryonic stem cells are not beta cells. Diabetologia 2004; 47: 499-508.
24. Rolletscheck A, Kania G and Wobus AM. Generation of pancreatic insulin-producing cells from embryonic stem cells-‘proof of principle’, but questions still unanswered. Diabetologia 2006; 49: 2541-2545.
25. Blum B and Benvenisty N. The tumorigenicity of diploid and aneuploid human pluripotent stem cells. Cell Cycle 2009; 8: 3822-3830.
26. Knoepfler PS. Deconstructing stem cell tumorigenicity: a roadmap to safe regenerative medicine. Stem Cells 2009; 27: 1050-1056.
27. Kooreman NG and Wu JC. Tumorigenicity of pluripotent stem cells: biological insights from molecular imaging. J R Soc Interface 2010; 7 Suppl 6: S753-S763.
28. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K and Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131: 861-872.
29. Aoi T, Yae K, Nakagawa M, Ichisaka T, Okita K, Takahashi K, Chiba T and Yamanaka S. Generation of pluripotent stem cells from adult mouse liver and stomach cells. Science 2008; 321: 699-702.
30. Hanna J, Markoulaki S, Schorderet P, Carey BW, Beard C, Wernig M, Creyghton MP, Steine EJ, Cassady JP, Foreman R, Lengner CJ, Dausman JA and Jaenisch R. Direct reprogramming of terminally differentiated mature B lymphocytes to pluripotency. Cell 2008; 133: 250-264.
31. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II and Thomson JA. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007; 318: 1917-1920.
32. Maehr R, Chen S, Snitow M, Ludwig T, Yagasaki L, Goland R, Leibel RL and Melton DA. Generation of pluripotent stem cells from patients with type 1 diabetes. Proc Natl Acad Sci U S A 2009; 106: 15768-15773.
33. Zhang D, Jiang W, Liu M, Sui X, Yin X, Chen S, Shi Y and Deng H. Highly efficient differentiation of human ES cells and iPS cells into mature pancreatic insulin-producing cells. Cell Res 2009; 19: 429-438.
34. D’Amour KA, Bang AG, Eliazer S, Kelly OG, Agulnick AD, Smart NG, Moorman MA, Kroon E, Carpenter MK and Baetge EE. Production of pancreatic hormone expressing endocrine cells from human embryonic stem cells. Nat Biotechnol 2006; 24: 1392-1401.
35. Hua H, Shang L, Martinez H, Freeby M, Gallagher MP, Ludwig T, Deng L, Greenberg E, Leduc C, Chung WK, Goland R, Leibel RL and Egli D. iPSC-derived β cells model diabetes due to glucokinase deficiency. J Clin Invest 2013; 123: 3146-3153.
36. Thatava T, Kudva YC, Edukulla R, Squillace K, De Lamo JG, Khan YK, Sakuma T, Ohmine S, Terzic A and Ikeda Y. Intrapatient variations in type 1 diabetes specific iPS cell differentiation into insulin-producing cells. Mol Ther 2013; 21: 228-239.
37. Tateishi K, He J, Taranova O, Liang G, D’Alessio AC and Zhang Y. Generation of insulin-secreting islet-like clusters from human skin fibroblasts. J Biol Chem 2008; 283: 31601-31607.
38. Thatava T, Nelson TJ, Edukulla R, Sakuma T, Ohmine S, Tonne JM, Yamada S, Kudva Y, Terzic A and Ikeda Y. Indolactam V/GLP-1-mediated differentiation of human iPS cells into glucose-responsive insulin-secreting progeny. Gene Ther 2011; 18: 283-293.
39. Nostro MC, Sarangi F, Ogawa S, Holtzinger A, Corneo B, Li X, Micallef SJ, Park IH, Basford C, Wheeler MB, Daley GQ, Elefanty AG, Stanley EG and Keller G. Stage-specific signaling through TGFb family members and WNT regulates patterning and pancreatic specification of human pluripotent stem cells. Development 2011; 138: 861-871.
40. Liew CG, Shah NN, Briston SJ, Shepherd RM, Khoo CP, Dunne MJ, Moore HD, Cosgrove KE, Andrews PW. PAX4 enhances beta-cell differentiation of human embryonic stem cells. PLoS One 2008; 3: e1783.
41. Teo AK, Wagers AJ and Kulkarni RN. New opportunities: harnessing induced pluripotency for discovery in diabetes and metabolism. Cell Metab 2013; 18: 775-791.
42. Jiang J, Au M, Lu K, Eshpeter A, Korbutt G, Fisk G and Majumdar AS. Generation of insulin-producing islet-like clusters from human embryonic stem cells. Stem Cells 2007; 25: 1940-1953.
43. Kroon E, Martinson LA, Kadoya K, Bang AG, Kelly OG, Eliazer S, Young H, Richardson M, Smart NG, Cunningham J, Agulnick AD, D’Amour KA, Carpenter MK and Baetge EE. Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin secreting cells in vivo. Nature Biotechnol 2008; 26: 443-452.
44. Shim JH, Kim SE, Woo DH, Kim SK, Oh CH, McKay R and Kim JH. Directed differentiation of human embryonic stem cells towards a pancreatic cell fate. Diabetologia 2007; 50: 1228-1238.
45. Mfopou JK, Chen B, Mateizel I, Sermon K and Bouwens L. Noggin, retinoids, and fibroblast growth factor regulate hepatic or pancreatic fate of human embryonic stem cells. Gastroenterology 2010; 138: 2233-2245, e1-14.
46. Kelly OG, Chan MY, Martinson LA, Kadoya K, Ostertag TM, Ross KG, Richardson M, Carpenter MK, D’Amour KA, Kroon E, Moorman M, Baetge EE and Bang AG. Cell-surface markers for the isolation of pancreatic cell types derived from human embryonic stem cells. Nat Biotechnol 2011; 29: 750-756.
47. Xu X, Browning VL and Odorico JS. Activin, BMP and FGF pathways cooperate to promote endoderm and pancreatic lineage cell differentiation from human embryonic stem cells. Mech Dev 2011; 128: 412-427.
48. Alipio Z, Liao W, Roemer EJ, Waner M, Fink LM, Ward DC and Ma Y. Reversal of hyperglycemia in diabetic mouse models using induced-pluripotent stem (iPS)-derived pancreatic beta-like cells. Proc Natl Acad Sci U S A 2010; 107: 13426-13431.
49. Zhu FF, Zhang PB, Zhang DH, Sui X, Yin M, Xiang TT, Shi Y, Ding MX and Deng H. Generation of pancreatic insulin-producing cells from rhesus monkey induced pluripotent stem cells. Diabetologia 2011; 54: 2325-2336.
50. Jeon K, Lim H, Kim JH, Thuan NV, Park SH, Lim YM, Choi HY, Lee ER, Kim JH, Lee MS and Cho SG. Differentiation and transplantation of functional pancreatic beta cells generated from induced pluripotent stem cells derived from a type 1 diabetes mouse model. Stem Cells Dev 2012; 21: 2642-2655.
51. Okita K, Ichisaka T and Yamanaka S. Generation of germline-competent induced pluripotent stem cells. Nature 2007; 448: 313-317.
52. Stadtfeld M, Nagaya M, Utikal J, Weir G and Hochedlinger K. Induced pluripotent stem cells generated without viral integration. Science 2008; 322: 945-949.
53. Okita K, Nakagawa M, Hyenjong H, Ichisaka T and Yamanaka S. Generation of mouse induced pluripotent stem cells without viral vectors. Science 2008; 322: 949-953.
54. Yamanaka S. Strategies and new developments in the generation of patient-specific pluripotent stem cells. Cell Stem Cell 2007; 1: 39-49.
55. Knoepfler PS. Why myc? An unexpected ingredient in the stem cell cocktail. Cell Stem Cell 2008; 2: 18-21.
56. Nakagawa M, Koyanagi M, Tanabe K, Takahashi K, Ichisaka T, Aoi T, Okita K, Mochiduki Y, Takizawa N and Yamanaka S. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol 2008; 26: 101-106.
57. Wernig M, Meissner A, Cassady JP and Jaenisch R. c-Myc is dispensable for direct reprogramming of mouse fibroblasts. Cell Stem Cell 2008; 2: 10-12.
58. Kern S, Eichler H, Stoeve J, Klüter H and Bieback K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 2006; 24: 1294-1301.
59. Oswald J, Boxberger S, Jørgensen B, Feldmann S, Ehninger G, Bornhäuser M and Werner C. Stem Cells 2004; 22: 377-384.
60. Pittenger MF and Martin BJ. Mesenchymal stem cells and their potential as cardiac therapeutics. Circ Res 2004; 95: 9-20.
61. Hung SC, Chen NJ, Hsieh SL, Ma HL and Lo WH. Isolation and characterization of size-sieved stem cells from human bone marrow. Stem Cells 2002; 20: 249-258.
62. Delorme B, Ringe J, Gallay N, Le Vern Y, Kerboeuf D, Jorgensen C, Rosset P, Sensebé L, Layrolle P, Häupl T and Charbord P. Specific plasma membrane protein phenotype of culture amplified and native human bone marrow mesenchymal stem cells. Blood 2008; 111: 2631-2635.
63. Reger RL, Tucker AH and Wolfe MR. Differentiation and characterization of human MSCs. Methods Mol Biol 2008; 449: 93-107.
64. Turnovcova K, Ruzickova K, Vanecek V, Sykova E and Jendelova P. Properties and growth of human bone marrow mesenchymal stromal cells cultivated in different media. Cytotherapy 2009; 11: 874-885.
65. Weiss ML, Medicetty S, Bledsoe AR, Rachakatla RS, Choi M, Merchav S, Luo Y, Rao MS, Velagaleti G and Troyer D. Human umbilical cord matrix stem cells: preliminary characterization and effect of transplantation in a rodent model of Parkinson’s disease. Stem Cells 2006; 24: 781-792.
66. Baksh D, Yao R and Tuan RS. Comparison of proliferative and multilineage differentiation potential of human mesenchymal stem cells derived from umbilical cord and bone marrow. Stem Cells 2007; 25: 1384-1392.
67. Oh SH, Muzzonigro TM, Bae SH, LaPlante JM, Hatch HM and Petersen BE. Adult bone marrow-derivedcells trans-differentiating into insulin-producing cells for treatment of type I diabetes. Lab Invest 2004; 84: 607-617.
68. Xie QP, Huang H, Xu B, Dong X, Gao SL, Zhang B and Wu YL. Human bone marrow mesenchymal stem cells differentiate into insulin-producing cells upon microenvironmental manipulation in vitro. Differentiation 2009; 77: 483-491.
69. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P and Hedrick MH. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002; 13: 4279-4295.
70. Schäffler A and Büchler C. Concise review: Adipose tissue-derived stromal cells-basic and clinical implications for novel cell-based therapies. Stem Cells 2007; 25: 818-827.
71. Kojima H, Fujimiya M, Matsumura K, Nakahara T, Hara M and Chan L. Extrapancreatic insulin-producing cells in multiple organs in diabetes. Proc Natl Acad Sci U S A 2004; 101: 2458-2563.
72. Timper K, Seboek D, Eberhardt M, Linscheid P, Christ-Crain M, Keller U, Müller B and Zulewski H. Human adipose tissue derived mesenchymal stem cells differentiate into insulin, somatostatin, and glucagon expressing cells. Biochem Biophys Res Commun 2006; 341: 1135-1140.
73. Chandra V, GS, Phadnis S, Nair PD and Bhonde RR. Generation of pancreatic hormone-expressing islet-like cell aggregates from murine adipose tissue-derived stem cells. Stem Cells 2009; 27: 1941-1953.
74. Romanov YA, Svintsitskaya VA and Smirnov VN. Searching for alternative sources of postnatal human mesenchymal stem cells: candidate MSC-like from umbilical cord. Stem Cells 2003; 21: 105-110.
75. La Rocca G, Anzalone R, Corrao S, Magno F, Loria T, Lo Iacono M, Di Stefano A, Giannuzzi P, Marasà L, Cappello F, Zummo G and Farina F. Isolation and characterization of Oct-4+/HLA-G+ mesenchymal stem cells from human umbilical cord matrix: differentiation potential and detection of new markers. Histochem Cell Biol 2009; 131: 267-282.
76. Montanucci P, Basta G, Pescara T, Pennoni I, Di Giovanni F and Calafiore R. New simple and rapid method for purification of mesenchymal stem cells from the human umbilical cord Wharton jelly. Tissue Eng Part A 2011; 17: 2651-2661.
77. Weiss ML, Anderson C, Medicetty S, Seshareddy KB, Weiss RJ, VanderWerff I, Troyer D and McIntosh KR. Immune properties of human umbilical cord Wharton’s jelly-derived cells. Stem Cells 2008; 26: 2865-2874.
78. Deuse T, Stubbendorff M, Tang-Quan K, Phillips N, Kay MA, Eiermann T, Phan TT, Volk HD, Reichenspurner H, Robbins RC and Schrepfer S. Immunogenicity and immunomodulatory properties of umbilical cord lining mesenchymal stem cells. Cell Transplant 2011; 20: 655-667.
79. Ricordi C, Inverardi L and Domínguez-Bendala J. From cellular therapies to tissue reprogramming and regenerative strategies in the treatment of diabetes. Regen Med 2012; 7: 41-48.
80. Hu J, Yu X, Wang Z, Wang F, Wang L, Gao H, Chen Y, Zhao W, Jia Z, Yan S and Wang Y. Long term effects of the implantation of Wharton’s jelly-derived mesenchymal stem cells from the umbilical cord for newly-onset type 1 diabetes mellitus. Endocr J 2013; 60: 347-357.