Pancreatic Stem Cells: From Possible to Probable

Stem Cell Reviews and Reports

Volumn 8, Issue 3, 2012, Pages 647-657

  Jiang, Fang Xu ^a   Morahan, Grant ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Clonogenesis; Differentiation; Pancreatic stem cells; Regeneration; Self renewal

Indexed keywords

ANIMAL; EPITHELIUM; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS; PANCREAS DUCT; PANCREAS ISLET BETA CELL; PATHOLOGY; PHYSIOLOGY; PRENATAL DEVELOPMENT; REGENERATION; REGENERATIVE MEDICINE; REVIEW; STEM CELL; STEM CELL TRANSPLANTATION;

ANIMALS; DIABETES MELLITUS, TYPE 1; EPITHELIUM; HUMANS; INSULIN-SECRETING CELLS; PANCREAS; PANCREATIC DUCTS; REGENERATION; REGENERATIVE MEDICINE; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 84865558353     PISSN: 15508943     EISSN: 15586804     Source Type: Journal    
DOI: 10.1007/s12015-011-9333-8     Document Type: Review

References (95)

1. Lock, L. T., & Tzanakakis, E. S. (2007). Stem/progenitor cell sources of insulin-producing cells for the treatment of diabetes. Tissue Engineering, 13, 1399-1412.
2. Ramalho-Santos, M., & Willenbring, H. (2007). On the origin of the term stem cell". Cell Stem Cell, 1, 35-38.
3. Evans, M. J., & Kaufman, M. H. (1981). Establishment in culture of pluripotential cells from mouse embryos. Nature, 292, 154-156.
4. Martin, G. R. (1981). Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proceedings of the National Academy of Sciences of the United States of America, 78, 7634-7638.
5. Tesar, P. J., Chenoweth, J. G., Brook, F. A., et al. (2007). New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature, 448, 196-199.
6. Brons, I. G., Smithers, L. E., Trotter, M. W., et al. (2007). Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature, 448, 191-195.
7. Shamblott, M. J., Axelman, J., Wang, S., et al. (1998). Derivation of pluripotent stem cells from cultured human primordial germ cells. Proceedings of the National Academy of Sciences of the United States of America, 95, 13726-13731.
8. Kanatsu-Shinohara, M., Inoue, K., Lee, J., et al. (2004). Generation of pluripotent stem cells from neonatal mouse testis. Cell, 119, 1001-1012.
9. Guan, K., Nayernia, K., Maier, L. S., et al. (2006). Pluripotency of spermatogonial stem cells from adult mouse testis. Nature, 440, 1199-1203.
10. Aoi, T., Yae, K., Nakagawa, M., et al. (2008). Generation of pluripotent stem cells from adult mouse liver and stomach cells. Science, 321, 699-702.
11. Hanna, J., Markoulaki, S., Schorderet, P., et al. (2008). Direct reprogramming of terminally differentiated mature B lymphocytes to pluripotency. Cell, 133, 250-264.
12. Park, I. H., Zhao, R., West, J. A., et al. (2008). Reprogramming of human somatic cells to pluripotency with defined factors. Nature, 451, 141-146.
13. Takahashi, K., & Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126, 663-676.
14. Ramiya, V. K., Maraist, M., Arfors, K. E., Schatz, D. A., Peck, A. B., & Cornelius, J. G. (2000). Reversal of insulin-dependent diabetes using islets generated in vitro from pancreatic stem cells. Nature Medicine, 6, 278-282.
15. Dor, Y., Brown, J., Martinez, O. I., & Melton, D. A. (2004). Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature, 429, 41-46.
16. Pictet, R. L., Clark, W. R., Williams, R. H., & Rutter, W. J. (1972). An ultrastructural analysis of the developing embryonic pancreas. Developmental Biology, 29, 436-467.
17. Pan, F. C., & Wright, C. (2011). Pancreas organogenesis: From bud to plexus to gland. Developmental Dynamics, 240, 530-565.
18. Seymour, P. A., & Sander, M. (2011). Historical perspective: Beginnings of the beta-cell: Current perspectives in beta-cell development. Diabetes, 60, 364-376.
19. Piper, K., Brickwood, S., Turnpenny, L. W., et al. (2004). Beta cell differentiation during early human pancreas development. Journal of Endocrinology, 181, 11-23.
20. Herrera, P. L., Huarte, J., Sanvito, F., Meda, P., Orci, L., & Vassalli, J. D. (1991). Embryogenesis of the murine endocrine pancreas; early expression of pancreatic polypeptide gene. Development, 113, 1257-1265.
21. Richardson, M. K., Hanken, J., Gooneratne, M. L., et al. (1997). There is no highly conserved embryonic stage in the vertebrates: Implications for current theories of evolution and development. Anatomy and Embryology (Berl), 196, 91-106.
22. Fougerousse, F., Bullen, P., Herasse, M., et al. (2000). Human-mouse differences in the embryonic expression patterns of developmental control genes and disease genes. Human Molecular Genetics, 9, 165-173.
23. De Krijger, R. R., Aanstoot, H. J., Kranenburg, G., Reinhard, M., Visser, W. J., & Bruining, G. J. (1992). The midgestational human fetal pancreas contains cells coexpressing islet hormones. Developmental Biology, 153, 368-375.
24. Lukinius, A., Ericsson, J. L., Grimelius, L., & Korsgren, O. (1992). Ultrastructural studies of the ontogeny of fetal human and porcine endocrine pancreas, with special reference to colocalization of the four major islet hormones. Developmental Biology, 153, 376-385.
25. Polak, M., Bouchareb-Banaei, L., Scharfmann, R., & Czernichow, P. (2000). Early pattern of differentiation in the human pancreas. Diabetes, 49, 225-232.
26. Gu, G., Dubauskaite, J., & Melton, D. A. (2002). Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development, 129, 2447-2457.
27. Ohneda, K., Mirmira, R. G., Wang, J., Johnson, J. D., & German, M. S. (2000). The homeodomain of PDX-1 mediates multiple protein-protein interactions in the formation of a transcriptional activation complex on the insulin promoter. Molecular and Cellular Biology, 20, 900-911.
28. Zhou, Q., Law, A. C., Rajagopal, J., Anderson, W. J., Gray, P. A., & Melton, D. A. (2007). A multipotent progenitor domain guides pancreatic organogenesis. Developmental Cell, 13, 103-114.
29. Seymour, P. A., Freude, K. K., Tran, M. N., et al. (2007). SOX9 is required for maintenance of the pancreatic progenitor cell pool. Proceedings of the National Academy of Sciences of the United States of America, 104, 1865-1870.
30. Lyttle, B. M., Li, J., Krishnamurthy, M., et al. (2008). Transcription factor expression in the developing human fetal endocrine pancreas. Diabetologia, 51, 1169-1180.
31. Jeon, J., Correa-Medina, M., Ricordi, C., Edlund, H., & Diez, J. A. (2009). Endocrine cell clustering during human pancreas development. Journal of Histochemistry and Cytochemistry, 57, 811-824.
32. Gradwohl, G., Dierich, A., LeMeur, M., & Guillemot, F. (2000). Neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas. Proceedings of the National Academy of Sciences of the United States of America, 97, 1607-1611.
33. Xu, X., D'Hoker, J., Stange, G., et al. (2008). Beta cells can be generated from endogenous progenitors in injured adult mouse pancreas. Cell, 132, 197-207.
34. Schwitzgebel, V. M., Scheel, D. W., Conners, J. R., et al. (2000). Expression of neurogenin3 reveals an islet cell precursor population in the pancreas. Development, 127, 3533-3542.
35. Jensen, J., Heller, R. S., Funder-Nielsen, T., et al. (2000). Independent development of pancreatic alpha- and beta-cells from neurogenin3-expressing precursors: A role for the notch pathway in repression of premature differentiation. Diabetes, 49, 163-176.
36. Oliver-Krasinski, J. M., Kasner, M. T., Yang, J., et al. (2009). The diabetes gene Pdx1 regulates the transcriptional network of pancreatic endocrine progenitor cells in mice. Journal of Clinical Investigation, 119, 1888-1898.
37. Desgraz, R., Herrera, P. L. (2009). Pancreatic neurogenin 3-expressing cells are unipotent islet precursors. Development.
38. Miyatsuka, T., Kosaka, Y., Kim, H., & German, M. S. (2011). Neurogenin3 inhibits proliferation in endocrine progenitors by inducing Cdkn1a. Proceedings of the National Academy of Sciences of the United States of America, 108, 185-190.
39. Bonner-Weir, S., & Sharma, A. (2002). Pancreatic stem cells. The Journal of Pathology, 197, 519-526.
40. Ryan, E. A., Lakey, J. R., Paty, B. W., et al. (2002). Successful islet transplantation: Continued insulin reserve provides long-term glycemic control. Diabetes, 51, 2148-2157.
41. Ryan, E. A., Paty, B. W., Senior, P. A., et al. (2005). Five-year follow-up after clinical islet transplantation. Diabetes, 54, 2060-2069.
42. Wagers, A. J., Sherwood, R. I., Christensen, J. L., & Weissman, I. L. (2002). Little evidence for developmental plasticity of adult hematopoietic stem cells. Science, 297, 2256-2259.
43. Bonner-Weir, S. (2000). Life and death of the pancreatic beta cells. Trends in Endocrinology and Metabolism, 11, 375-378.
44. Parsons, J. A., Brelje, T. C., & Sorenson, R. L. (1992). Adaptation of islets of Langerhans to pregnancy: Increased islet cell proliferation and insulin secretion correlates with the onset of placental lactogen secretion. Endocrinology, 130, 1459-1466.
45. Hellman, B. (1960). The islets of Langerhans in the rat during pregnancy and lactation, with special reference to the changes in the B/A cell ratio. Acta Obstetricia et Gynecologica Scandinavica, 39, 331-342.
46. van Assche, F. A. (1974). Quantitative morphologic and histoenzymatic study of the endocrine pancreas in nonpregnant and pregnant rats. American Journal of Obstetrics and Gynecology, 118, 39-41.
47. Karnik, S. K., Chen, H., McLean, G. W., et al. (2007). Menin controls growth of pancreatic beta-cells in pregnant mice and promotes gestational diabetes mellitus. Science, 318, 806-809.
48. van Assche, F. A., Aerts, L., & De Prins, F. (1978). A morphological study of the endocrine pancreas in human pregnancy. British Journal of Obstetrics and Gynaecology, 85, 818-820.
49. Nielsen, J. H., Svensson, C., Galsgaard, E. D., Moldrup, A., & Billestrup, N. (1999). Beta cell proliferation and growth factors. Journal of Molecular Medicine, 77, 62-66.
50. Rieck, S., & Kaestner, K. H. (2010). Expansion of beta-cell mass in response to pregnancy. Trends in Endocrinology and Metabolism, 21, 151-158.
51. Kim, H., Toyofuku, Y., Lynn, F. C., et al. (2010). Serotonin regulates pancreatic beta cell mass during pregnancy. Nature Medicine, 16, 804-808.
52. Butler, A. E., Janson, J., Bonner-Weir, S., Ritzel, R., Rizza, R. A., & Butler, P. C. (2003). Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes, 52, 102-110.
53. Butler, A. E., Janson, J., Soeller, W. C., & Butler, P. C. (2003). Increased beta-cell apoptosis prevents adaptive increase in beta-cell mass in mouse model of type 2 diabetes: Evidence for role of islet amyloid formation rather than direct action of amyloid. Diabetes, 52, 2304-2314.
54. Matveyenko, A. V., Veldhuis, J. D., & Butler, P. C. (2006). Mechanisms of impaired fasting glucose and glucose intolerance induced by an approximate 50% pancreatectomy. Diabetes, 55, 2347-2356.
55. Stagner, J. I., & Samols, E. (1991). Deterioration of islet beta-cell function after hemipancreatectomy in dogs. Diabetes, 40, 1472-1479.
56. Robertson, R. P., Lanz, K. J., Sutherland, D. E., & Seaquist, E. R. (2002). Relationship between diabetes and obesity 9 to 18 years after hemipancreatectomy and transplantation in donors and recipients. Transplantation, 73, 736-741.
57. Nir, T., Melton, D. A., & Dor, Y. (2007). Recovery from diabetes in mice by beta cell regeneration. Journal of Clinical Investigation, 117, 2553-2561.
58. Brennand, K., Huangfu, D., & Melton, D. (2007). All beta cells contribute equally to islet growth and maintenance. PLoS Biology, 5, e163.
59. Gupta, R. K., Gao, N., Gorski, R. K., et al. (2007). Expansion of adult beta-cell mass in response to increased metabolic demand is dependent on HNF-4alpha. Genes & Development, 21, 756-769.
60. Georgia, S., & Bhushan, A. (2004). Beta cell replication is the primary mechanism for maintaining postnatal beta cell mass. Journal of Clinical Investigation, 114, 963-968.
61. Teta, M., Rankin, M. M., Long, S. Y., Stein, G. M., & Kushner, J. A. (2007). Growth and regeneration of adult beta cells does not involve specialized progenitors. Developmental Cell, 12, 817-826.
62. Jiang, F. X., Mehta, M., & Morahan, G. (2010). Quantification of insulin gene expression during development of pancreatic islet cells. Pancreas, 39, 201-208.
63. Hara, M., Dizon, R. F., Glick, B. S., et al. (2006). Imaging pancreatic beta-cells in the intact pancreas. American Journal of Physiology, Endocrinology and Metabolism, 290, E1041-E1047.
64. Alpert, S., Hanahan, D., & Teitelman, G. (1988). Hybrid insulin genes reveal a developmental lineage for pancreatic endocrine cells and imply a relationship with neurons. Cell, 53, 295-308.
65. Cornelius, J. G., Tchernev, V., Kao, K. J., & Peck, A. B. (1997). In vitro-generation of islets in long-term cultures of pluripotent stem cells from adult mouse pancreas. Hormone and Metabolic Research, 29, 271-277.
66. Suzuki, A., Oyama, K., Fukao, K., Nakauchi, H., & Taniguchi, H. (2002). Establishment of clonal colony-forming assay system for pancreatic stem/progenitor cells. Cell Transplantation, 11, 451-453.
67. Zulewski, H., Abraham, E. J., Gerlach, M. J., et al. (2001). Multipotential nestin-positive stem cells isolated from adult pancreatic islets differentiate ex vivo into pancreatic endocrine, exocrine, and hepatic phenotypes. Diabetes, 50, 521-533.
68. Seaberg, R. M., Smukler, S. R., Kieffer, T. J., et al. (2004). Clonal identification of multipotent precursors from adult mouse pancreas that generate neural and pancreatic lineages. Nature Biotechnology, 22, 1115-1124.
69. Suzuki, A., Nakauchi, H., & Taniguchi, H. (2004). Prospective isolation of multipotent pancreatic progenitors using flow-cytometric cell sorting. Diabetes, 53, 2143-2152.
70. Jiang, F. X., Stanley, E. G., Gonez, L. J., & Harrison, L. C. (2002). Bone morphogenetic proteins promote development of fetal pancreas epithelial colonies containing insulin-positive cells. Journal of Cell Science, 115, 753-760.
71. Jiang, F. X., & Harrison, L. C. (2005). Convergence of bone morphogenetic protein and laminin-1 signaling pathways promotes proliferation and colony formation by fetal mouse pancreatic cells. Experimental Cell Research, 308, 114-122.
72. Jiang, F. X., & Harrison, L. C. (2005). Laminin-1 and epidermal growth factor family members co-stimulate fetal pancreas cell proliferation and colony formation. Differentiation, 73, 45-49.
73. Bonner-Weir, S., Taneja, M., Weir, G. C., et al. (2000). In vitro cultivation of human islets from expanded ductal tissue. Proceedings of the National Academy of Sciences of the United States of America, 97, 7999-8004.
74. Seeberger, K. L., Dufour, J. M., Shapiro, A. M., Lakey, J. R., Rajotte, R. V., & Korbutt, G. S. (2006). Expansion of mesenchymal stem cells from human pancreatic ductal epithelium. Laboratory Investigation, 86, 141-153.
75. Bonner-Weir, S., Inada, A., Yatoh, S., et al. (2008). Transdifferentiation of pancreatic ductal cells to endocrine beta-cells. Biochemical Society Transactions, 36, 353-356.
76. Inada, A., Nienaber, C., Katsuta, H., et al. (2008). Carbonic anhydrase II-positive pancreatic cells are progenitors for both endocrine and exocrine pancreas after birth. Proceedings of the National Academy of Sciences of the United States of America, 105, 19915-19919.
77. Solar, M., Cardalda, C., Houbracken, I., et al. (2009). Pancreatic exocrine duct cells give rise to insulin-producing beta cells during embryogenesis but not after birth. Developmental Cell, 17, 849-860.
78. Haumaitre, C., Barbacci, E., Jenny, M., Ott, M. O., Gradwohl, G., & Cereghini, S. (2005). Lack of TCF2/vHNF1 in mice leads to pancreas agenesis. Proceedings of the National Academy of Sciences of the United States of America, 102, 1490-1495.
79. Haumaitre, C., Fabre, M., Cormier, S., Baumann, C., Delezoide, A. L., & Cereghini, S. (2006). Severe pancreas hypoplasia and multicystic renal dysplasia in two human fetuses carrying novel HNF1beta/MODY5 mutations. Human Molecular Genetics, 15, 2363-2375.
80. Hao, E., Tyrberg, B., Itkin-Ansari, P., et al. (2006). Beta-cell differentiation from nonendocrine epithelial cells of the adult human pancreas. Nature Medicine, 12, 310-316.
81. Minami, K., Okuno, M., Miyawaki, K., et al. (2005). Lineage tracing and characterization of insulin-secreting cells generated from adult pancreatic acinar cells. Proceedings of the National Academy of Sciences of the United States of America, 102, 15116-15121.
82. Baeyens, L., De Breuck, S., Lardon, J., Mfopou, J. K., Rooman, I., & Bouwens, L. (2005). In vitro generation of insulin-producing beta cells from adult exocrine pancreatic cells. Diabetologia, 48, 49-57.
83. Minami, K., Okano, H., Okumachi, A., & Seino, S. (2008). Role of cadherin-mediated cell-cell adhesion in pancreatic exocrine-to-endocrine transdifferentiation. Journal of Biological Chemistry, 283, 13753-13761.
84. Zhou, Q., Brown, J., Kanarek, A., Rajagopal, J., & Melton, D. A. (2008). In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature, 455, 627-632.
85. Desai, B. M., Oliver-Krasinski, J., De Leon, D. D., et al. (2007). Preexisting pancreatic acinar cells contribute to acinar cell, but not islet beta cell, regeneration. Journal of Clinical Investigation, 117, 971-977.
86. Abraham, E. J., Leech, C. A., Lin, J. C., Zulewski, H., & Habener, J. F. (2002). Insulinotropic hormone glucagon-like peptide-1 differentiation of human pancreatic islet-derived progenitor cells into insulin-producing cells. Endocrinology, 143, 3152-3161.
87. Lardon, J., Rooman, I., & Bouwens, L. (2002). Nestin expression in pancreatic stellate cells and angiogenic endothelial cells. Histochemistry and Cell Biology, 117, 535-540.
88. Selander, L., & Edlund, H. (2002). Nestin is expressed in mesenchymal and not epithelial cells of the developing mouse pancreas. Mechanisms of Development, 113, 189-192.
89. Gershengorn, M. C., Hardikar, A. A., Wei, C., Geras-Raaka, E., Marcus-Samuels, B., & Raaka, B. M. (2004). Epithelial-to-mesenchymal transition generates proliferative human islet precursor cells. Science, 306, 2261-2264.
90. Chase, L. G., Ulloa-Montoya, F., Kidder, B. L., & Verfaillie, C. M. (2007). Islet-derived fibroblast-like cells are not derived via epithelial-mesenchymal transition from Pdx-1 or insulin-positive cells. Diabetes, 56, 3-7.
91. Russ, H. A., Bar, Y., Ravassard, P., & Efrat, S. (2008). In vitro proliferation of cells derived from adult human beta-cells revealed by cell-lineage tracing. Diabetes, 57, 1575-1583.
92. Smukler, S. R., Arntfield, M. E., Razavi, R., et al. (2011). The adult mouse and human pancreas contain rare multipotent stem cells that express insulin. Cell Stem Cell, 8, 281-293.
93. Daniel, C. P., Ponting, I. L., & Dexter, T. M. (1989). Growth and development of haemopoietic cells: A deterministic process? Hämatologie und Bluttransfusion, 32, 172-177.
94. Dexter, T. M. (1989). Regulation of hemopoietic cell growth and development: Experimental and clinical studies. Leukemia, 3, 469-474.
95. Gu, G., Wells, J. M., Dombkowski, D., Preffer, F., Aronow, B., & Melton, D. A. (2004). Global expression analysis of gene regulatory pathways during endocrine pancreatic development. Development, 131, 165-179.