Stem cell-based approaches to solving the problem of tissue supply for islet transplantation in type 1 diabetes

International Journal of Biochemistry and Cell Biology

Volumn 36, Issue 4, 2004, Pages 667-683

  Street, Cale N ^a   Sipione, Simonetta ^a   Helms, Lisa ^a   Binette, Tanya ^a   Rajotte, Ray V ^a   Bleackley, R Chris ^a   Korbutt, Gregory S ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Differentiation; Islet transplantation; Stem cells; Type 1 diabetes; Xenotransplantation

Indexed keywords

INSULIN;

ANIMAL EMBRYO; CELL DIFFERENTIATION; CELL ISOLATION; CELL MATURATION; CELL TYPE; INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET CELL; PANCREAS ISLET TRANSPLANTATION; REVIEW; STEM CELL; SWINE;

ANIMALS; DIABETES MELLITUS, TYPE 1; EMBRYO; HUMANS; ISLETS OF LANGERHANS; ISLETS OF LANGERHANS TRANSPLANTATION; PANCREAS; STEM CELL TRANSPLANTATION; STEM CELLS; SWINE; TRANSPLANTS;

SUIDAE;

EID: 1542328921     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2003.09.005     Document Type: Review

References (134)

1. Abe K., Niwa H., Iwase K., Takiguchi M., Mori M., Abe S.I., Yamamura K.I. Endoderm-specific gene expression in embryonic stem cells differentiated to embryoid bodies. Experimental Cell Research. 229:1996;27-34.
2. Abraham E.G., Leech C.A., Lin J., Zulewski H., Habener J.F. Insulinotropic hormone glucagons-like peptide 1 differentiation of human pancreatic islet derived progenitor cells into insulin-producing cells. Endocrinology. 143:2002;3152-3161.
3. Alison M.R., Poulsom R., Forbes S., Wright N.A. An introduction to stem cells. Journal of Pathology. 197:2002;419-423.
4. Assady S., Maor G., Amit M., Itskovitz-Eldor J., Skorecki K.L., Tzukerman M. Insulin production by human embryonic stem cells. Diabetes. 50:2001;1691-1697.
5. Ballinger W.F., Lacy P.E. Transplantation of intact pancreatic islets in rats. Surgery. 72:1972;175-186.
6. Benoit B.O., Savarese T., Joly M., Engstrom C.N., Pang L., Reilly J., Recht L.D., Ross A.H., Quesenberry P.H. Neurotrophin channeling of neural progenitor cell differentiation. Journal of Neurobiology. 46(4):2001;265-280.
7. Bertelli E., Regoli M., Orazioli D., Bendayan M. Association between islets of Langerhans and pancreatic ductal system in adult rat. Where endocrine and exocrine meet together? Diabetologia. 44:2001;575-584.
8. Blyszczuk P., Czyz J., Kania G., Wagner M., Roll U., St-Onge L., Wobus A.M. Expression of Pax4 in embryonic stem cells promotes differentiation of nestin-positive progenitor and insulin-producing cells. Proceedings of the National Academy of Sciences of the United States of America. 100:2003;998-1003.
9. Bonner-Weir S., Deery D., Leahy J.L., Weir G.C. Compensatory growth of pancreatic β-cells in adult rats after short term glucose infusion. Diabetes. 38:1989;49-53.
10. Bonner-Weir S., Smith F.E. Islet cell growth and the growth factors involved. Trends in Endocrinology and Metabolism. 5:1994;60-64.
11. Bonner-Weir S., Taneja M., Weir G.C., Tatarkiewicz K., Song K., Sharma A., O'Neil J.J. In vitro cultivation of human islets from expanded ductal tissue. Proceedings of the National Academy of Sciences of the United States of America. 97(14):2000;7999-8004.
12. Bouwens L., DeBlay E. Islet morphogenesis and stem cell markers in rat pancreas. Journal of Histochemistry and Cytochemistry. 44:1996;947-951.
13. Bouwens L., Lu W.G., Dekrijger R. Proliferation and differentiation in the human fetal endocrine pancreas. Diabetologia. 40:1997;398-404.
14. Bouwens L., Pipeleers D.G. Extra insular beta cells associated with ductules are frequent in adult human pancreas. Diabetologia. 41:1998;629-633.
15. Bouwens L., Wang R.N., DeBlay E., Pipeleers D.G., Kloppel G. Cytokeratins as markers of ductal cell differentiation and islet neogenesis in the neonatal rat pancreas. Diabetes. 43:1994;1279-1283.
16. Bretzel, R. G., Brendel, M. D., Hering, B. J. (2001). International islet transplant registry report (p. 8). Justis Liebis University of Giessen.
17. Brustle O., Jones K.N., Learish R.D., Karram K., Choudhary K., Wiestler O.D., Duncan I.D., McKay R.D. Embryonic stem cell-derived glial precursors: A source of myelinating transplants. Science. 285:1999;754-756.
18. Cassiman D., Denef C., Desmet V.J., Roskams T. Human and rat hepatic stellate cells express neurotrophins and neurotrophin receptors. Hepatology. 33(1):2001;148-158.
19. Dani C., Smith A.G., Dessolin S., Leroy P., Staccini L., Villageois P., Darimont C., Ailhaud G. Differentiation of embryonic stem cells into adipocytes in vitro. Journal of Cell Science. 110(Part 11):1997;1279-1285.
20. De Lisle R.C., Logsdon C.D. Pancreatic acinar cells in culture: Expression of acinar and ductal antigens in a growth-related manner. European Journal of Cell Biology. 51:1990;64-75.
21. Diabetes Control and Complications Trial Research Group (1993). The effect of intensive treatment of diabetes on the development and progression of long term complications in insulin dependent diabetes mellitus. New England Journal of Medicine, 329, 977-986.
22. Dudek R.W., Lawrence I.E., Hill R.S., Johnson R.C. Induction of islet cytodifferentiation by fetal mesenchyme in adult pancreatic ductal epithelium. Diabetes. 40:1991;1041-1048.
23. Duvillie B., Currie C., Chrones T., Buchini D., Jami J., Joshi R.L., Hill D.J. Increased islet cell proliferation, decreased apoptosis, and greater vascularization leading to β-cell hyperplasia in mutant mice lacking insulin. Endocrinology. 143:2002;1530-1537.
24. Edenfeld G., Pielage J., Klambt C. Cell lineage specification in the nervous system. Current Opinion in Genetics and Development. 12:2002;473-477.
25. Edlund H. Transcribing pancreas. Diabetes. 47:1998;1817-1823.
26. Edlund H. Developmental biology of the pancreas. Diabetes. 50(Suppl. 1):2001;S5-S9.
27. Eguchi G., Kodama R. Transdifferentiation. Current Opinion in Cell Biology. 5:1993;1023-1028.
28. Evans M.J., Kaufman M.H. Establishment in culture of pluripotential cells from mouse embryos. Nature. 292:1981;154-156.
29. Faich G.A., Fishbein H.A., Ellis S.E. The epidemiology of diabetic acidosis: A population based study. American Journal of Epidemiology. 117:1983;551-558.
30. Field L.L., Tobias R., Magnus T. A locus on chromosome 15q26 (IDDM3) produces susceptibility to insulin dependent diabetes mellitus. Nature Genetics. 8:1994;189-194.
31. Finegood D.T., Scaglia L., Bonner-Weir S. Dynamics of β-cell mass in the growing rat pancreas. Estimation with a simple mathematical model. Diabetes. 44:1995;249-256.
32. Gardner D.F., Arakaki R.F., Podet E.J., Nell L.J., Thomas J.W., Field J.B. The pharmacokinetics of subcutaneous regular insulin in type 1 diabetic patients: Assessment using a glucose clamp technique. Journal of Clinical Endocrinology and Metabolism. 63:1986;689-694.
33. Gmyr V., Kerr-Conte J., Belaich S., Vandewalle B., Leteurtre E., Vantyghem M.C., Lecomte-Houcke M., Proye C., Lefefbvre J., Pattou F. Adult human cytokeratin 19 positive cells re-express insulin promoter factor 1 in vitro. Diabetes. 49:2000;1671-1680.
34. Gmyr V., Kerr-Conte J., Vandewalle B., Proye C., Lefebvre J., Pattou F. Human pancreatic ductal cells: Large scale isolation and expansion. Cell Transplantation. 10:2001;109-121.
35. Guz Y., Nasir J., Teitelman G. Regeneration of pancreatic beta-cells from intra-islet precursor cells in an experimental model of diabetes. Endocrinology. 142(11):2001;4956-4968.
36. Hakelien A.M., Landsverk H.B., Robl J.M., Skalhegg B.S., Collas P. Reprogramming fibroblasts to express T-cell functions using cell extracts. Nature Biotechnology. 20:2002;460-466.
37. Hall P.A., Lemoine N.R. Rapid acinar to ductal transdifferentiation in cultured human exocrine pancreas. Journal of Pathology. 166:1992;97-103.
38. Hanley N.A. Beta cell differentiation during human development does not rely on nestin positive precursors: Implications for stem cell derived replacement therapy (letter). Diabetologia. 45:2002;1045-1047.
39. Heimberg H., Bouwens L., Heremans Y., Van den Casteele M., Lefebvre V., Pipeleers D. Adult human pancreatic duct and islet cells exhibit similarities in expression and differences in phosphorylation and complex formation of the homeodomain protein IPF-1. Diabetes. 49:2000;571-579.
40. Heremans Y., Van den Casteele M., Veld P., Gradwohl G., Serup P., Madsen O., Pipeleers D., Heimberg H. Recapitulation of embryonic neuroendocrine differentiation in adult human pancreatic duct cells expressing neurogenin 3. Journal of Cell Biology. 159(2):2002;303-311.
41. Higashikawa K., Yokozaki H., Ue T., Taniyama K., Ishikawa T., Tarin D., Tahara E. Evaluation of CD44 transcription variants in human digestive tract carcinomas and normal tissues. International Journal of Cancer. 66:1996;11-17.
42. Hollands P. Differentiation and grafting of hematopoietic stem cells from early post-implantation mouse embryos. Development. 99:1987;69-76.
43. Horb M.E., Shen C.N., Tosh D., Slack J.M. Experimental conversion of liver to pancreas. Current Biology. 13:2003;105-115.
44. Hori Y., Rulifson I.C., Tsai B.C., Heit J.J., Cahoy J.D., Kim S.K. Growth inhibitors promote differentiation of insulin-producing tissue from embryonic stem cells. Proceedings of the National Academy of Sciences of the United States of America. 99:2002;16105-16110.
45. Houard N., Rousseau G.G., Lemaigre F.P. HNF-6-independent differentiation of mouse embryonic stem cells into insulin-producing cells. Diabetologia. 46:2003;378-385.
46. Hubner K., Fuhrmann G., Christenson L.K., Kehler J., Reinbold R., De La Fuente R., Wood J., Strauss J.F., Boiani M., Scholer H.R. Derivation of oocytes from mouse embryonic stem cells. Science. 300:2003;1251-1256.
47. Hunziker E., Stein M. Nestin-expressing cells in the pancreatic islets of Langerhans. Biochemical and Biophysical Research Communications. 271:2000;116-119.
48. Ianus A., Holz G.G., Theise N.D., Hussain M.A. In vivo derivation of glucose-competent pancreatic endocrine cells from bone marrow without evidence of cell fusion. Journal of Clinical Investigations. 111:2003;843-850.
49. Jiang Y., Jahagirdar B.N., Reinhardt R.L., Schwartz R.E., Keene C.D., Ortiz-Gonzalez X.R., Reyes M., Lenvik T., Lund T., Blackstad M., Du J., Aldrich S., Lisberg A., Low W.C., Largaespada D.A., Verfaillie C.M. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature. 418:2002a;41-49.
50. Jiang Y., Vaessen B., Lenvik T., Blackstad M., Reyes M., Verfaillie C.M. Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle, and brain. Experimental Hematology. 30:2002b;896-904.
51. Jones E.A., Tosh D., Wilson D.I., Lindsay S., Forrester L.M. Hepatic differentiation of murine embryonic stem cells. Experimental Cell Research. 272:2002;15-22.
52. Kikyo N., Wolffe A.P. Reprogramming nuclei: Insights from cloning, nuclear transfer and heterokaryons. Journal of Cell Science. 113(Part 1):2000;11-20.
53. Klug M.G., Soonpaa M.H., Koh G.Y., Field L.J. Genetically selected cardiomyocytes from differentiating embronic stem cells form stable intracardiac grafts. Journal of Clinical Investigations. 98:1996;216-224.
54. Kojima H., Fujimiya M., Matsumura K., Younan P., Imaeda H., Maeda M., Chan L. NeuroD-betacellulin gene therapy induces islet neogenesis in the liver and reverses diabetes in mice. Nature Medicines. 9:2003;596-603.
55. Korbutt G.S., Elliott J.F., Ao Z., Smith D.K., Warnock G.L., Rajotte R.V. Large scale isolation, growth, and function of porcine neonatal islet cells. Journal of Clinical Investigations. 97:1996;2119-2129.
56. Korbutt G.S., Warnock G.L., Rajotte R.V. Islet transplantation. Physiology and Pathophysiology of the Islets of Langerhans. 53:1997;397-410.
57. Korsgren O., Jansson L., Eizirik D., Andersson A. Functional and morphological differentiation of fetal porcine islet-like clusters after transplantation into nude mice. Diabetologia. 34:1991;379-386.
58. Landsverk H.B., Hakelien A.M., Kuntziger T., Robl J.M., Skalhegg B.S., Collas P. Reprogrammed gene expression in a somatic cell-free extract. EMBO Report. 3:2002;384-389.
59. Lardon J., Rooman I., Bouwens L. Nestin expression in pancreatic stellate cells and angiogenic endothelial cells. Histochemistry and Cell Biology. 117:2002;535-540.
60. Lendahl U., Zimmerman L.B., McKay R.D. CNS stem cells express a new class of intermediate filament protein. Cell. 60:1990;585-595.
61. Li L., Seno M., Yamada H., Kojima I. Promotion of β-cell regeneration by betacellulin in ninety-percent pancreatectomized rats. Endocrinology. 142:2001;5379-5385.
62. Lipsett M., Finegood D.T. β-Cell neogenesis during prolonged hyperglycemia in rats. Diabetes. 51:2002;1834-1841.
63. Liu S., Qu Y., Stewart T.J., Howard M.J., Chakrabortty S., Holekamp T.F., McDonald J.W. Embryonic stem cells differentiate into oligodendrocytes and myelinate in culture and after spinal cord transplantation. Proceedings of the National Academy of Sciences of the United States of America. 97:2000;6126-6131.
64. Liu Y., Rao M.S. Transdifferentiation - Fact or artifact. Journal of Cellular Biochemistry. 88:2003;29-40.
65. Lumelsky N., Blondel O., Laeng P., Velasco I., Ravin R., McKay R. Differentiation of embryonic stem cells to insulin-secreting structures similar to pancreatic islets. Science. 292:2001;1389-1394.
66. Maclaren N., Atkinson M. Is insulin dependent diabetes mellitus environmentally induced? New England Journal of Medicine. 327:1992;348-349.
67. Maedler K., Fontana A., Ris F., Sergeev P., Toso C., Oberholzer J., Lehmann R., Bachmann F., Tasinato A., Spinas G.A., Halban P.A., Donath M.A. FLIP switches Fas-mediated glucose signaling in human pancreatic β-cells from apoptosis to cell replication. Proceedings of the National Academy of Sciences of the United States of America. 99(12):2002;8236-8241.
68. Martin G.R., Evans M.J. Differentiation of clonal lines of teratocarcinoma cells: Formation of embryoid bodies in vitro. Proceedings of the National Academy of Sciences of the United States of America. 72:1975;1441-1445.
69. Martin G.R., Wiley L.M., Damjanov I. The development of cystic embryoid bodies in vitro from clonal teratocarcinoma stem cells. Developmental Biology. 61:1977;230-244.
70. Medvinsky A., Smith A. Stem cells: Fusion brings down barriers. Nature. 422:2003;823-825.
71. Messam C.A., Hou J., Major E.O. Coexpression of nestin in neural and glial cells in the developing human CNS defined by a human specific anti nestin antibody. Experimental Neurology. 161:2000;585-596.
72. Miralles F., Czernichow P., Scharfmann R. Pancreatic acinar AR42J cells express functional nerve growth factor receptors. Journal of Endocrinology. 160(3):1999;433-442.
73. Miralles F., Phillipe P., Czernichow P., Scharfmann R. Expression of nerve growth factor and its high affinity receptor Trk-A in the rat pancreas during embryonic and fetal life. Journal of Endocrinology. 156(3):1998;431-439.
74. Moritoh Y., Yamato E., Yasui Y., Miyazaki S., Miyazaki J. Analysis of insulin-producing cells during in vitro differentiation from feeder-free embryonic stem cells. Diabetes. 52:2003;1163-1168.
75. Nakano T. In vitro development of hematopoietic system from mouse embryonic stem cells: A new approach for embryonic hematopoiesis. International Journal of Hematology. 65:1996;1-8.
76. Nishikawa S. Embryonic stem cells as a source of hematopoietic and vascular endothelial cells in vitro. Journal of Allergy and Clinical Immunology. 100:1997;S102-S104.
77. Offield M.F., Jetton T.L., Labosky P.A., Ray M., Stein R., Magnuson M.A., Hogan B.L., Wright C.V. PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development. 122:1996;983-995.
78. Okabe S., Forsberg-Nilsson K., Spiro A.C., Segal M., McKay R.D. Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. Mechanism of Development. 59:1996;89-102.
79. Owerbach D., Gabbay K.H. The HOXD8 locus (2q31) is linked to type 1 diabetes mellitus: Interaction with chromosomes 6 and 11 disease susceptibility genes. Diabetes. 44:1995;132-136.
80. Perez-Villamil B., Schwartz P.T., Vallejo M. The pancreatic homeodomain transcription factor IDX1/IPF1 is expressed in neural cells during brain development. Endocrinology. 140:1999;3857-3860.
81. Peshavaria M., Stein R. PDX-1: An activator of genes involved in pancreatic development and islet gene expression. Pancreatic Growth an Regeneration Karger Landes Systems (Basel). 4:1997;96-107.
82. Petropavlovskaia M., Rosenberg L. Identification and characterization of small cells in the adult pancreas: Potential progenitor cells? Cell Tissue Research. 310:2002;51-58.
83. Poulsom R., Alison M.R., Forbes S.J., Wright N.A. Adult stem cell plasticity. Journal of Pathology. 197:2002;441-456.
84. Rajagopal J., Anderson W.J., Kume S., Martinez O.I., Melton D.A. Insulin staining of ES cell progeny from insulin uptake. Science. 299:2003;363.
85. Rayat G.R., Rajotte R.V., Ao Z., Korbutt G.S. Microencapsulation of neonatal porcine islets: Protection from human antibody/complement-mediated cytolysis in vitro and long-term reversal of diabetes in nude mice. Transplantation. 69:2000;1084-1090.
86. Rayat G.R., Rajotte R.V., Hering B.J., Binette T.M., Korbutt G.S. In vitro and in vivo expression of Galα-(1,3)Gal on porcine islet cells is age dependent. Journal of Endocrinology. 177:2003;127-135.
87. Reckard C., Barker C. Transplantation of isolated pancreatic islets across strong and weak histocompatibility barriers. Transplantation Proceedings. 5:1973;761-763.
88. Reynolds B.A., Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science. 255:1992;1707-1710.
89. Reynolds B.A., Weiss S. Clonal and population analysis demonstrate that an EGF responsive mammalian embryonic CNS precursor is a stem cell. Developmental Biology. 175:1996;1-13.
90. Robertson, E. (1987). Embryo-derived stem cell lines. In E. Robertson (Ed.), Teratocarcinomas and embryonic stem cells: A practical approach (pp. 71-112). Oxford, UK: IRL Press.
91. Rohwedel J., Maltsev V., Bober E., Arnold H.H., Hescheler J., Wobus A.M. Muscle cell differentiation of embryonic stem cells reflects myogenesis in vivo: Developmentally regulated expression of myogenic determination genes and functional expression of ionic currents. Developmental Biology. 164:1994;87-101.
92. Rooman L., Heremans Y., Heimberg H., Bouwens L. Modulation of rat pancreatic acinoductal transdifferentiation and expression of PDX-1 in vitro. Diabetologia. 43:2000;907-914.
93. Rooman I., Lardon J., Bouwens L. Gastrin stimulates β-cell neogenesis and increases islet mass from transdifferentiated but not from normal exocrine pancreas tissue. Diabetes. 51:2002;686-690.
94. Rosenbaum T., Vidaltamayo R., Sanchez-Soto M.C., Zentella A., Hiriart M. Pancreatic beta-cells synthesize and secrete nerve growth factor. Proceedings of the National Academy of Sciences of the United States of America. 95(13):1998;7784-7788.
95. Roy N.S., Wang S., Jiang L., Kang J., Benraiss A., Harrison-Restelli C., Fraser R.A., Couldwell W.T., Kawaguchi A., Okano H., Nedergaard M., Goldman S.A. In vitro neurogenesis by progenitor cells isolated from the adult human hippocampus. Nature Medicine. 6(3):2000;271-277.
96. Ryan E.A., Lakey J.R.T., Paty B., Imes S., Korbutt G.S., Kneteman N.M., Bigam D., Rajotte R.V., Shapiro A.M.J. Successful islet transplantation: Continued insulin reserve provides long term glycemic control. Diabetes. 51:2002;2148-2157.
97. Ryan E.A., Lakey J.R.T., Rajotte R.V., Korbutt G.S., Kin T., Imes S., Rabinovitch A., Elliot J.F., Bigam D., Kneteman N.M., Warnock G.L., Larsen I., Shapiro A.M.J. Clinical outcomes and insulin secretion after islet transplantation with the Edmonton Protocol. Diabetes. 50:2001;710-719.
98. Sahlgren C.M., Mikhailov A., Hellman J., Chou Y., Lendahl U., Goldman R.D., Eriksson J.E. Mitotic reorganization of the intermediate filament protein nestin involves phosphorylation by cdc2 kinase. Journal of Biological Chemistry. 276(19):2001;16456-16463.
99. Sander M., German M. The beta-cell transcription factors and development of the pancreas. Journal Molecular Medicine. 75:1997;327-340.
100. Satoh K., Shimosegawa T., Koizumi M., Toyota T. Expression of CD44 in duct cell carcinomas and intraductal neoplasms of the pancreas. Anticancer Research. 17:1997;215-220.
101. Scharp D.W., Downing R., Merrel R.C. Isolating the elusive islet. Diabetes. 29:1980;19-30.
102. Seelentag W.K., Komminoth P., Saremaslani P., Heitz P.U., Roth J. CD44 isoform expression in the diffuse neuroendocrine system. I. Normal cells and hyperplasia. Histochemical and Cellular Biology. 106:1996;543-550.
103. Selander L., Edlund H. Nestin is expressed in mesenchymal and not epithelial cells of the developing mouse pancreas. Mechanism of Development. 113:2002;189-192.
104. Shapiro A.M.J., Lakey J.R.T., Ryan E.A., Korbutt G.S., Toth E., Warnock G.L., Kneteman N.M., Rajotte R.V. Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid free immunosuppressive regimen. New England Journal of Medicine. 343(4):2000;230-238.
105. Sharma A., Zangen D.H., Reitz P., Taneja M., Lissauer M.E., Miller C.P., Weir G.C., Habener J.F., Bonner-Weir S. The homeodomain protein IDX-1 increases after an early burst of proliferation during pancreatic regeneration. Diabetes. 48:1999;507-513.
106. Sharma A., Zangen D.H., Reitz P., Taneja M., Lissauer M.E., Miller C.P., Weir G.C., Habner J.F., Bonner-Weir S. The homeodomain protein IDX-1 increases after an early burst of proliferation during pancreatic regeneration. Diabetes. 48:1999;507-513.
107. Shiroi A., Yoshikawa M., Yokota H., Fukui H., Ishizaka S., Tatsumi K., Takahashi Y. Identification of insulin-producing cells derived from embryonic stem cells by zinc-chelating dithizone. Stem Cells. 20:2002;284-292.
108. Soria B., Roche E., Berna G., Leon-Quinto T., Reig J.A., Martin F. Insulin-secreting cells derived from embryonic stem cells normalize glycemia in streptozotocin-induced diabetic mice. Diabetes. 49:2000;157-162.
109. Sosa-Pineda B., Chowdhury K., Torres M., Oliver G., Gruss P. The Pax4 gene is essential for differentiation of insulin-producing beta cells in the mammalian pancreas. Nature. 386:1997;399-402.
110. Steinert P.M., Chou Y., Prahlad V., Parry D.A., Marekov L.N., Wu K.C., Jang S., Goldman R.D. A high molecular weight intermediate filament associated protein in BHK-21 cells is nestin, a type VI intermediate filament protein. Journal of Biological Chemistry. 274(14):1999;9881-9890.
111. Svendsen C.N., Smith A.G. New prospects for human stem-cell therapy in the nervous system. Trends in Neuroscience. 22:1999;357-364.
112. Swenne I. Effects of aging on the regenerative capacity of the pancreatic β-cell of the rat. Diabetes. 32:1983;14-19.
113. Taniguchi H., Yamato E., Tashiro F., Ikegami H., Ogihara T., Miyazaki J. β-Cell neogenesis induced by adenovirus mediated gene delivery of transcription factor PDX-1 into mouse pancreas. Gene Therapy. 10:2003;15-23.
114. Teitelman G., Guz Y., Ivkovic S., Erholich M. Islet injury induces neurotrophin expression in pancreatic cells and reactive gliosis of peri-islet Schwann cells. Journal of Neurobiology. 34(4):1998;304-318.
115. Tosh D., Slack J.M. How cells change their phenotype. Nature Reviews. Molecular Cell Biology. 3:2002;187-194.
116. Tourrel C., Bailbe D., Meile M., Kergoat M., Portha B. Glucagon-like-peptide-1 and exendin-4 stimulate β-cell neogenesis in streptozotocin treated newborn rats resulting in persistently improved glucose homeostasis at adult age. Diabetes. 50:2001;1562-1570.
117. Trivedi N., Hollister-Lock J., Lopez-Avalos M.D., O'Neil J.J., Keegan M., Bonner-Weir S., Weir G.C. Increase in β-cell mass in transplanted porcine neonatal pancreatic cell clusters is due to proliferation of β-cells and differentiation of duct cells. Endocrinology. 142:2001;2115-2122.
118. Vassilopoulos G., Wang P.R., Russell D.W. Transplanted bone marrow regenerates liver by cell fusion. Nature. 422:2003;901-904.
119. Verfaillie C.M. Adult stem cells: Assessing the case for pluripotency. Trends in Cell Biology. 12:2002;502-508.
120. Wang R.N., Kloppel G., Bouwens L. Duct to islet cell differentiation and islet growth in the pancreas of duct ligated adult rats. Diabetologia. 38:1995;1405-1411.
121. Wang X., Willenbring H., Akkari Y., Torimaru Y., Foster M., Al Dhalimy M., Lagasse E., Finegold M., Olson S., Grompe M. Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature. 422:2003;897-901.
122. Western P.S., Surani M.A. Nuclear reprogramming - Alchemy or analysis? Nature Biotechnology. 20:2002;445-446.
123. Wiles M.V., Keller G. Multiple hematopoietic lineages develop from embryonic stem (ES) cells in culture. Development. 111:1991;259-267.
124. 2+ channel blockers. Differentiation. 48:1991;173-182.
125. Yamamoto K., Miyagawa J., Waguri M., Sasada R., Igarashi K., Li M., Nammo T., Moriwaki M., Imagawa A., Yamagata K., Nakajima H., Namba M., Tochino Y., Hanafusa T., Matsuzawa Y. Recombinant human betacellulin promotes the neogenesis of β-cells and ameliorates glucose intolerance in mice with diabetes induced by selective alloxan perfusion. Diabetes. 49:2000;2021-2027.
126. Ying Q.L., Nichols J., Evans E.P., Smith A.G. Changing potency by spontaneous fusion. Nature. 416:2002;545-548.
127. Yang L., Li S., Hatch H., Ahrens K., Cornelius J.G., Petersen B.E., Peck A.B. In vitro trans-differentiation of adult hepatic stem cells into pancreatic endocrine hormone-producing cells. Proceedings of the National Academy of Sciences of the United States of America. 99:2002;8078-8083.
128. Ying Q.L., Nichols J., Evans E.P., Smith A.G. Changing potency by spontaneous fusion. Nature. 416:2002;545-548.
129. Yoon K., Quickel R.R., Tatarkiewicz K., Ulrich T.R., Hollister-Lock J., Trivedi N., Bonner-Weir S., Weir G.C. Differentiation and expansion of beta cell mass in porcine neonatal pancreatic cell clusters transplanted into nude mice. Cell Transplantation. 8:1999;673-689.
130. Young-Song S., Gannon M., Washington M.K., Scoggins C.R., Meszoely I.M., Goldenring J.R., Marino C.R., Sandgren E.P., Coffey R.J., Wright C.V., Leach S. Expansion of PDX-1 expressing pancreatic epithelium and islet neogenesis in transgenic mice overexpressing transforming growth factor-alpha. Gastroenterology. 117:1999;1416-1426.
131. Yuan S., Duguid W.P., Agapitos D., Wyllie B., Rosenberg L. Phenotypic modulation of hamster acinar cells by culture in collagen matrix. Experimental Cell Research. 237:1997;247-258.
132. Zalzman, M., Gupta, S., Giri, R. K., Berkovich, I., Sappal, B. S., Karnieli, O., Zern, M. A., Fleischer, N., Efrat, S. (2003). Reversal of hyperglycemia in mice by using human expandable insulin-producing cells differentiated from fetal liver progenitor cells. Proceedings of the National Academy of Sciences of the United States of America.
133. Zammit P., Beauchamp J. The skeletal muscle satellite cell: Stem cell or son of a stem cell? Differentiation. 68(4-5):2001;193-204.
134. Zulewski H., Abraham E.J., Gerlach M.J., Daniel P.B., Moritz W., Muller B., Vallejo M., Thomas M.K., Habener J.F. Multipotential nestin-positive stem cells isolated from adult pancreatic islets differentiate ex vivo into pancreatic endocrine, exocrine, and hepatic phenotypes. Diabetes. 50:2001;521-533.