Pancreatic development and maturation of the islet B cell: Studies of pluripotent islet cultures

European Journal of Biochemistry

Volumn 242, Issue 3, 1996, Pages 435-445

  Madsen, Ole Dragsbæk ^a   Jensen, Jan ^a   Blume, Niels ^a   Petersen, Helle V ^a   Lund, Kaare ^a   Karlsen, Christina ^a   Andersen, Frank G ^a   Jensen, Per B ^a   Larsson, Lars Inge ^b   Serup, Palle ^a  

^a HAGEDORN RESEARCH INSTITUTE   (Denmark)

^b STATENS SERUM INSTITUT   (Denmark)

Author keywords

B cell; Insulin; Insulin promoter factor 1; Islet; Pancreas

Indexed keywords

GLUCOSE TRANSPORTER; INSULIN; TRANSCRIPTION FACTOR;

CELL DIFFERENTIATION; ENDODERM; GENE ACTIVATION; GENE EXPRESSION REGULATION; GLUCAGONOMA; HUMAN; INSULINOMA; MATURATION; NERVE CELL DIFFERENTIATION; NONHUMAN; ORGANOGENESIS; PANCREAS; PANCREAS ISLET CELL; PRIORITY JOURNAL; REVIEW;

AMYLOID; ANIMALS; B-LYMPHOCYTES; CELL DIFFERENTIATION; CELLS, CULTURED; GENE EXPRESSION REGULATION; GLUCOSE TRANSPORTER TYPE 2; HOMEODOMAIN PROTEINS; HUMANS; INSULIN; ISLETS OF LANGERHANS; MICE; MONOSACCHARIDE TRANSPORT PROTEINS; PANCREAS; RATS; TRANS-ACTIVATORS;

EID: 0030432477     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1996.435rr.x     Document Type: Review

References (126)

1. Ahlgren, U., Jonsson, J. & Edlund, H. (1996) The morphogenesis of the pancreatic mesenchyme is uncoupled from that of the pancreatic epithelium in IPF1/PDX1-deficient mice, Development (Camb.) 122, 1409-1416.
2. Aiken, K. D., Kisslinger, J. A. & Roth, K. A. (1994) Immunohistochemical studies indicate multiple enteroendocrine cell differentiation pathways in the mouse proximal small intestine, Dev. Dyn. 201, 63-70.
3. 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.
4. Andersson, A. & Hellerström, C. (1972) Metabolic characteristics of isolated pancreatic islets in tissue culture, Diabetes 21 (Suppl. 2), 546-554.
5. Aronheim, A., Ohlsson, H., Park, C. W., Edlund, T. & Walker, M. D. (1991) Distribution and characterisation of helix-loop-helix enhancer binding proteins from pancreatic beta-cells and lymphocytes, Nucleic Acids Res. 19, 3893-3899.
6. Beck, T. C. & Madsen, O. D. (1989) Monoclonal antibodies as probes to the differentiated exocrine pancreas react to monoclonal islet tumor tissue, Exp. Clin. Endocrinol. 93, 255-260.
7. Bell, G. I., Gerhard, D. S., Fong, N. M., Sanchez-Pescador, R. & Rail, L. B. (1985) Isolation of the human insulin-like growth factor genes: insulin-like growth factor II and insulin genes are contiguous, Proc. Natl Acad. Sci. USA 82, 6450-6454.
8. Blume, N., Petersen, J. S., Andersen, L. C., Kofod, H., Dyrberg, T., Michelsen, B. K., Serup, P. & Madsen, O. D. (1992) Immature transformed islet β-cells differentially express C-peptides derived from genes coding for insulin I and II as well as a transfected human insulin gene, Mol. Endocrinol. 6, 299-307.
9. Blume, N., Skouv, J., Larsson, L.-I., Holst, J. J. & Madsen, O. D. (1995) Potent inhibitory effects of transplantable rat glucagonomas and insulinomas on the respective endogenous islet cells are associated with pancreatic apoptosis, J. Clin. Invest. 96, 2227-2235.
10. Bonner-Weir, S. & Orci, L. (1982) New perspectives on the microvasculature of the islet of Langerhans in the rat, Diabetes 31, 883-889.
11. Bonner-Weir, S., Baxter, L. A., Schuppin, G. T. & Smith, F. E. (1993) A 2nd for regeneration of adult exocrine and endocrine pancreas - a possible recapitulation of embryonic-development, Diabetes 42, 1715-1720.
12. Bordi, C. & Bussolati, G. (1974) Immunofluorescence, histochemical and ultrastructural studies for the detection of multiple endocrine polypeptide tumours of the pancreas, Virchows Arch. Cell Pathol. 17, 13-27.
13. Bouwens, L., Wang, R. N., Deblay, E., Pipeleers, D. G. & Klöppel, G. (1994) Cytokeratins as markers of ductal cell-differentiation and islet neogenesis in the neonatal rat pancreas, Diabetes 43, 1279-1283.
14. Bouwens, L., Braet, F. & Heimberg, H. (1995) Identification of rat pancreatic duct cells by their expression of cytokeratin-7, cytokeratin-19, and cytokeratin-20 in-vivo and after isolation and culture, J. Histochem. Cytochem. 43, 245-253.
15. Bretherton-Watt, D., Ghatei, M. A., Jamal, H., Gilbey, S. G., Jones, P. M. & Bloom, S. R. (1992) The physiology of calcitonin gene-related peptide in the islet compared with that of sielt amyloid polypeptide (amylin), Ann. N.Y. Acad. Sci. 657, 299-312.
16. Brubaker, P. L., Lee, Y. C. & Drucker, D. J. (1992) Alterations in proglucagon processing and inhibition of proglucagon gene expression in transgenic mice which contain a chimeric proglucagon-SV40 T antigen gene. J. Biol. Chem. 267, 20 728-20 733.
17. Bucchini, D., Ripoche, M.-A., Stinnakre, M.-G., Desbois, P., Lores, P., Monthioux, E., Absil, J., Lepesant, J.-A., Pictet, R. & Jami, J. (1986) Pancreatic expression of human insulin gene in transgenic mice, Proc. Natl Acad. Sci. USA 83, 2511-2515.
18. Bucchini, D., Madsen, O., Desbois, P., Pictet, R. & Jami, J. (1989) B islet cells of pancreas are the site of expression of the human insulin gene in transgenic mice, Exp. Cell Res. 180, 467-474.
19. Chick, W. L., Warren, S., Chute, R. N., Like, A. A., Lauris, V. & Kitchen, K. C. (1977) A transplantable insulinoma in the rat, Proc. Natl Acad. Sci. USA 74, 628-632.
20. Contreas, G., Jørgensen, J. & Madsen, O. D. (1990) Novel islet, duct and acinar cell markers defined by monoclonal autoantibodies from prediabetic BB-rats, Pancreas 5, 540-547.
21. DeKrijger, 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, Dev. Biol. 153, 368-375.
22. Deltour, L., Leduque, P., Paldi, A., Ripoche, M. A., Dubois, P. & Jami, J. (1991) Polyclonal origin of pancreatic islets in aggregation mouse chimaeras, Development (Camb.) 112, 1115-1121.
23. Deltour, L., Leduque, P., Blume, N., Madsen, O., Dubois, P., Jami, J. & Bucchini, D. (1993) Differential expression of the two nonallelic proinsulin genes in the developing mouse embryo, Proc. Natl Acad. Sci. USA 90, 527-531.
24. Devos, A., Heimberg, H., Quartier, E., Huypens, P., Bouwens, L., Pipeleers, D. & Schuit, F. (1995) Human and rat beta-cells differ in glucose-transporter but not in glucokinase gene-expression, J. Clin. Invest. 96, 2489-2495.
25. Docherty, K. & Clark, A. R. (1994) Nutrient regulation of insulin gene expression, FASEB J. 8, 20-27.
26. Douarin, N. M. L. (1988) On the origin of pancreatic endocrine cells, Cell 153, 169-171.
27. Drucker, D. J., Jin, T., Asa. S. L.. Young, T. A. & Brubaker, P. L. (1994) Activation of proglucagon gene transcription by protein kinase-A in a novel mouse enteroendocrine cell line, Mol. Endocrinol. 8, 1646-1655.
28. Dudek, R. W., Lawrence, I. E., Hill, R. S. & Johnson, R. C. (1991) Induction of islet cytodifferentiation by fetal mesenchyme in adult pancreatic ductal epithelium, Diabetes 40, 1041-1048.
29. Ebiou, J. C., Bulant, M., Nicolas, P. & Aratan-Spire, S. (1992) Pattern of thyrotropinreleasing hormone secretion from the adult and neonatal rat pancreas: comparison with insulin secretion, Endocrinology 130, 1371-1379.
30. Edlund, T., Walker, M. D., Barr, P. J. & Rutter, W. J. (1985) Cell-specific expression of the rat I insulin gene: evidence for role of two distinct 5′ flanking elements, Science 230, 912-916.
31. Efrat, S., Linde, S., Kofod, H., Spector, D., Delannoy, M., Grant, S., Baekkeskov, S. & Hanahan, D. (1988a) Beta-cell lines derived from transgenic mice expressing a hybrid insulin-oncogene, Proc. Natl Acad. Sci. USA 85, 9037-9041.
32. Efrat, S., Teitelman, G., Anwar, M., Ruggiero, D. & Hanahan, D. (1988b) Glucagon gene regulatory region directs oncoprotein expression to neurons and pancreatic α-cells, Neuron I, 605-613.
33. Fromont-Racine, M., Bucchini, D., Madsen, O., Desbois, P., Linde, S., Nielsen, J. H., Saulnier, C., Ripoche, M.-A., Jami, J. & Pectet, R. (1990) Effect of 5′-flanking sequence deletions on expression of the human insulin gene in transgenic mice, Mol. Endocrinol. 4, 669-677.
34. Gamer, L. W. & Wright, C. V. E. (1995) Autonomous endodermal determination in Xenopus: regulation of expression of the pancreatic gene XlHbox 8, Dev. Biol. 171, 240-251.
35. Gazdar, A. F., Chick, W. L., Oie, H. K., Sims, H. L., King, D. L., Weir, G. C. & Lauris, V. (1980) Continous, clonal, insulin- and somatostatin secreting cell lines established from a transplantable rat islet cell tumor, Proc. Natl Acad. Sci. USA 77, 3519-3523.
36. German, M. S., Blanar, M. A., Nelson, C., Moss, L. G. & Rutter, W. J. (1991) Two related helix-loop-helix proteins participate in separate cell-specific complexes that bind the insulin enhancer, Mol. Endocrinol. 5, 292-299.
37. German, M., Ashcroft, S., Docherty, K., Edlund, H., Edlund, T., Goodison, S., Imura, H., Kennedy, G., Madsen, O., Melloul, D., Moss, L., Olson, K., Permutt, A., Philippe, J., Robertson, R. P., Rutter, W. J., Serup, P., Stein, R., Steiner, D., Tsai, M.-J. & Walker, M. (1995) The insulin gene promoter: a simplified nomenclature, Diabetes 44, 1002-1004.
38. Gittes, G. K. & Rutter, W. J. (1992) Onset of cell-specific gene expression in the developing mouse pancreas, Proc. Natl Acad. Sci. USA 89, 1128-1132.
39. Gittes, G. K., Galante, P. E., Hanahan, D., Rutter, W. J. & Debas, H. T. (1996) Lineage-specific morphogenesis in the developing pancreas: role of mesenchymal factors, Development (Camb.) 122 439-447.
40. Gordon, J. I. (1989) Intestinal epithelial differentiation: new insights from chimeric and transgenic mice, J. Cell Biol. 108, 1187-1194.
41. Gu, D. & Sarvetnick, N. (1993) Epithelial cell proliferation and islet neogenesis in IFNγ transgenic mice, Development (Camb.) 118, 33-46.
42. Gu, D., Lee, M. S., Krahl, T. & Sarvetnick, N. (1994) Transitional cells in the regenerating pancreas, Development (Camb.) 120, 1873-1881.
43. Guz, Y., Montminy, M. R., Stein, R., Leonard, J., Gamer, L. W., Wright, C. V. E. & Teitelman, G. (1995) Expression of Stf-1, a putative insulin gene transcription factor, in b-cells of pancreas, duodenal epithelium and pancreatic exocrine and endocrine progenitors during ontogeny, Development (Camb.) 121, 11-18.
44. Hanahan, D. (1985) Heritable formation of pancreatic β-cell tumors in transgenic mice expression recombinant insulin/simial virus 40 oncogenes, Nature 315, 115-122.
45. Hashimoto, T., Kawano, H., Daikoku, S., Shima, K., Taniguchi, H. & Baba, S. (1988) Transient coappearance of glucagon and insulin in the progenitor cells of the rat pancreatic islets, Anat. Embryol. 178, 489-497.
46. Heimberg, H., Devos, A., Pipeleers, D., Thorens, B. & Schuit, F. (1995) Differences in glucose-transporter gene-expression between rat pancreatic alpha-cells and beta-cells are correlated to differences in glucose-transport but not in glucose-utilization, J. Biol. Chem. 270, 8971-8975.
47. Herrera, P.-L., Huarte, J., Sanvito, F., Meda, P., Orci, L. & Vassali, J.-D. (1991) Embryogenesis of the murine endocrine pancreas; early expression of the pancreatic polypeptide gene, Develoment (Camb.) 113, 1257-1265.
48. Jackerott, M., Øster, A. & Larsson, L.-I. (1996) PYY in developing murine islet cells: Comparisons to development of islet hormones NPY, and BrdU incorporation, J. Histochem. Cytochem. 44, 809-817.
49. Jensen, J., Serup, P., Karlsen, C., Funder, T. F. & Madsen, O. D. (1996) mRNA profiling of rat islet tumors reveals Nkx 6.1 as a β-cell specific homeodomain transcription factor, J. Biol. Chem. 271, 18 749-18 758.
50. Jessop, N. W. & Hay, R. J. (1980) Characteristics of two rat pancreatic exocrine cell lines derived from transplantable tumors, In Vitro (Rockville) 16, 212-216.
51. Jonsson, J., Carlsson, L., Edlund, T. & Edlund, H. (1994) Insulin-promoter-factor 1 is required for pancreas development in mice, Nature 371, 606-609.
52. Kanaka-Gantenbein, C., Dicou, E., Czernichow, P. & Scharfmann, R. (1995a) Presence of nerve growth factor and its receptors in an in vitro model of islet cell development: implication in normal islet morphogenesis, Endocrinology 136, 3154-3162.
53. Kanaka-Gantenbein, C., Tazi, A., Czemichow, P. & Scharfmann, R. (1995b) In vivo presence of the high-affinity NGF receptor TRK-A in the rat pancreas: differential localization during pancreatic development, Endocrinology 136, 761-769.
54. Larsson, L.-I., Grimelius, L., Häkanson, R., Rehfeld, J. F., Stadil, F., Holst, J., Angervall, L. & Sundler, F. (1975) Mixed endocrine pancreatic tumors producing several peptide hormones, Am. J. Pathol. 79, 271-284.
55. Larsson, L.-I., Rehfeld, J. F., Sundler, F. & Hdkanson, R. (1976) Pancreatic gastrin in neonatal rats, Nature 262, 609-610.
56. Larsson, L.-I. (1978) Endocrine pancreatic tumors, Hum. Pathol. 9, 401-416.
57. Larsson, L.-I. & Jorgensen, L. M. (1978) Ultrastructural and cytochemical studies on the cytodifferentiation of duodenal endocrine cells, Cell & Tissue Res. 194, 79-102.
58. Larsson, L.-I. & Hougaard, D. M. (1994) Coexpression of islet hormones and messenger RNA's in the human foetal pancreas, Endocrine 2, 759-765.
59. Larsson, L.-I., Tingstedt, J.-E., Madsen, O. D., Serup, P. & Hougaard, D. (1995) The LIM-homeodomain protein Isl-1 segregates with somatostatin but not with gastrin expression during differentiation of somatostatin/gastrin precursor cells, Endocrine 3, 519-524.
60. Lee, J. E., Hollenberg, S. M., Snider, L., Turner, D. L., Lipnick, N. & Weintraub, H. (1995) Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein, Science 268, 836-844.
61. Lee, Y. C., Brubaker, P. L. & Drucker, D. J. (1990) Developmental and tissue-specific regulation of proglucagon gene expression, Endocrinology 127, 2217-2222.
62. Leonard, J., Peers, B., Johnson, T., Fefferi, K., Lee, S. & Montminy, M. R. (1993) Characterization of somatostatin transactivating factor-1, a novel homeobox factor that stimulates somatostatin expression in pancreatic islet cells, Mol. Endocrinol. 7, 1275-1283.
63. MacFarlane, W. M., Read, M. L., Gilligan, M., Bujalska, I. & Docherty, K. (1994) Glucose modulates the binding activity of the β-cell transcription factor 1UFL in a phosphorylation-dependent manner, Biochem. J. 303, 625-631.
64. Madsen, O. D., Larsson, L.-I., Rehfeld, J. F., Schwartz, T., Lemmark, A., Labrecque, A. & Steiner, D. F. (1986) Cloned cell lines from a transplantable insulinoma are heterogeneous and express cholecystokinin in addition to islet hormones, J. Cell Biol. 103, 2025-2034.
65. Madsen, O. D., Andersen, L. C., Michelsen, B., Owerbach, D., Larsson, L.-I., Lemmark, A. & Steiner, D. F. (1988) Tissue-specific expression of transfected human insulin genes in pluripotent clonal rat insulinoma lines induced during passage in vivo. Proc. Natl Acad. Sci. USA 85, 6652-6656.
66. Madsen, O. D., Andersen, L. C., Serup, P. & Michelsen, B. (1989) Control of insulin gene expression in pluripotent rat islet tumor cells, in Genes and gene products in the development of diabetes mellitus (Nerup, J., Mandrup-Poulsen, T. & Hökfelt, B., eds) pp. 141-153, Elsevier Science Publishers, Amsterdam.
67. Madsen, O. D., Nielsen, J. H., Michelsen, B., Westermark, P., Betsholtz, C., Nishi, M. & Steiner, D. F. (1991) Islet amyloid polypeptide and insulin expression are controlled differently in primary and transformed islet cells, Mol. Endocrinol. 5, 143-148.
68. Madsen, O. D., Karlsen, C., Nielsen, E. & Holst, J. J. (1993a) Proglucagon processing in transplantable glucagonomas associated with severe anorexia, Digestion 54, 361-363.
69. Madsen, O. D., Karlsen, C., Nielsen, E., Lund, K., Kofod, H., Welinder, B., Rehfeld, J. F., Larsson, L.-I., Steiner, D. F., Holst, J. J. & Michelsen, B. K. (1993b) The dissociation of tumor-induced weight loss from hypoglycemia in a transplantable pluripotent rat islet tumor results in the segregation of stable α- and β-cell tumor phenotypes, Endocrinology 133, 2022-2030.
70. Madsen, O., Karlsen, C., Blume, N., Jensen, H., Larsson, L.-I. & Holst, J. (1994) Transplantable glucagonomas derived from pluripotent rat islet tumor tissue cause severe anorexia and adipsia, Scand. J. Clin. Lab. Invest. 55 (Suppl. 220), 27-36.
71. Melloul, D., Ben-Neriah, Y. & Cerasi, E. (1993) Glucose modulates the binding of an islet-specific factor to a conserved sequence within the rat I and the human insulin gene promoters, Proc. Natl Acad. Sci. USA 90, 3865-3869.
72. Miller, C. P., McGehee, R. E. & Habener, J. F. (1994) 1DX-1: a new homeodomain transcription factor expressed in rat pancreatic islets and duodenum that transactivates the somatostatin gene, EMBO J. 13, 1145-1156.
73. Møller, C. J., Christgau, S., Williamson, M. R., Madsen, O. D., ZhanPo, N., Bock, E. & Baekkeskov, S. (1992) Differential expression of neural cell adhesion molecule and cadherins in pancreatic islets, glucagonomas, and insulinomas, Mol. Endocrinol. 6, 1332-1342.
74. Naya, F. J., Stellrecht, C. M. & Tsai, M. J. (1995) Tissue-specific regulation of the insulin gene by a novel basic helix-loop-helix transcription factor, Genes & Dev. 9, 1009-1019.
75. Nielsen, E., Welinder, B. S. & Madsen, O. D. (1991) Chromoganin-B, a putative precursor of eight novel rat glucagonoma peptides through processing at mono-, di-, or tribasic residues, Endcrinology 129, 3147-3156.
76. Nielsen, J. H., Linde, S., Welinder, B. S., Billestrup, N. & Madsen, O. D. (1989) Growth hormone is a growth factor for the differentiated pancreatic β-cell, Mol. Endocrinol. 13, 165-173.
77. O'Malley, K. L. & Rotwein, P. (1988) Human tyrosine hydroxylase and insulin genes are contiguous on chromosome 11, Nucleic Acids Res. 16, 4437-4446.
78. Offield, M. F., Jetton, T. L., Labosky, P. A., Stein, R., Magnuson, M. A., Hogan, B. L. M. & Wright, C. V. E. (1996) Pdx-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum, Development (Camb.) 112, 983-995.
79. Ohlsson, H., Thor, S. & Edlund, T. (1991) Novel insulin promoter- and enhancer-binding proteins that discriminate between pancreatic α-and β-cells, Mol. Endocrinol. 5, 897-904.
80. Ohlsson, H., Karlsson, K. & Edlund, T. (1993) IPF1, a homeodomain-containing transactivator of the insulin gene, EMBO J. 12, 4251-4259.
81. Oie, H. K., Gazdar, A. F., Minna, J. D., Weir, G. & Baylin, S. B. (1983) Clonal analysis of insulin and somatostatin secretion and L-dopa decarboxylase expression by a rat islet cell tumor, Endocrinology 112, 1070-1075.
82. Okada, Y. & Ando, T. (1980) Properties of hamster insulinoma cell (In111-R), J. Physiol. Soc. Jpn 42, 358.
83. Otonkoski, T., Cirulli, V., Beattie, G. M., Mally, M. I., Soto, G., Rubin, J. S. & Hayek, A. (1996) A role for hepatocyte growth factor/scatter factor in fetal mesenchyme-induced pancreatic β-cell growth, Development (Camb.) 137, 3131-3139.
84. Pang, K., Mukonoweshuro, C. & Wong, G. G. (1994) Beta cells arise from glucose transporter type 2 (Glut2)-expressing epithelial cells of the developing rat pancreas, Proc. Natl Acad. Sci. USA 91, 9559-9563.
85. Park, C. W. & Walker, M. D. (1992) Subunit structure of cell-specific E-box binding proteins analysed by quantitation of electrophoretic mobility shift, J. Biol. Chem. 267, 15 642-15 649.
86. Patel, Y. C. (1992) General aspects of the biology and function of somatostatin, in Somatostatin (Weil, C., Muller, E. E. & Thomer, M. O., eds) pp. 1-16, Springer-Verlag, Berlin.
87. Pearse, A. G. E. (1982) Islet cell precursors are neurons, Nature 295, 96-97.
88. Peers, B., Leonard, J., Sharrna, S., Teitelman, G. & Montminy, M. R. (1994) Insulin expression in pancreatic islet cells relies in cooperative interactions between the helix-loop-helix factor E47 and the homeobox factor STF-1, Mol Endocrinol. 8, 1798-1806.
89. Petersen, H. V., Serup, P., Leonard, J., Michelsen, B. K. & Madsen, O. D. (1994) Transcriptional regulation of the human insulin gene is dependent on the homeodomain protein STF1/IPF1 acting through the CT boxes, Proc. Natl Acad. Sci. USA 91, 10 465-10 469.
90. Philippe, J., Chick, W. L. & Habener, J. F. (1987) Multipotential phenotypic expression of genes encoding peptide hormones in clonal rat insulinoma cell lines, J. Clin. Invest. 79, 351-358.
91. Philippe, J. (1991) Structure and pancreatic expression of the insulin and glucagon genes, Endocr. Rev. 12, 252-271.
92. Philippe, J. (1994) Pancreatic expression of the insulin and glucagon genes: update 1994, Endocr. Rev. 2, 21-27.
93. Pictet, R. L. & Runer, W. J. (1972) Development of the embryonic endocrine pancreas, Handb. Physiol. 1, 25-66.
94. Pictet, L. P., Rall, L. B., Phelps, P. & Rutter, W. J. (1976) The neural crest and the origin of the insulin-producing and other gastrointestinal hormone-producing cells, Science 191, 191-192.
95. Ponder, B. A. J., Schmidt, G. H., Wilkinson, M. M., Wood, M. J., Monk, M. & Reid, A. (1985) Derivation of mouse intestinal crypts from single progenitor cells, Nature 313, 689-691.
96. Rao, M. S., Yeldandi, A. V. & Reddy, J. K. (1990) Stem cell potential of ductular and periductular cells in the adult rat pancreas, Cell Differ. Dev. 29, 155-163.
97. Robinson, G. L. W. G., Peshavaria, M., Henderson, E., Shieh, S.-Y., Tsai, M. J., Teitelman, G. & Stein, R. (1994) Expression of the transactive factors that stimulate insulin control element-mediated activity appear to precede insulin gene transcription, J. Biol. Chem. 269, 2452-2460.
98. Rosenberg, L. & Vinik, A. I. (1992) Trophic stimulation of the ductularislet cell axis: a new approach to the treatment of diabetes, Adv. Exp. Med. Biol. 321, 95-104.
99. Rosewicz, S., Vogt, D., Harth, N., Grund, C., Franke, W. W., Ruppert, S., Schweitzer, R., Riecken, E.-O. & Wiedenmann, B. (1992) An amphicrine pancreatic cell line: AR42J cells combine exocrine and neuroendocrine properties, Eur. J. Cell Biol. 59, 80-91.
100. Roth, K. A., Hertz, J. M. & Gordon, J. I. (1990) Mapping enteroendocrine cell populations in transgenic mice reveals an unexpected degree of complexity in cellular differentiation within the gastrointestinal tract, J. Cell Biol. 110, 1791-1801.
101. Roth, K. A., Kim, S. & Gordon, J. I. (1992) Immununocytochemical studies suggest two pathways for enteroendocrine cell differentiation in the colon, Am. J. Physiol. 263, G174-G180.
102. Rudnick, A., Ling, T. Y., Odagiri, H., Rutter, W. J. & German, M. S. (1994) Pancreatic beta cells express a diverse set of homeobox genes, Proc Natl Acad. Sci. USA 91, 12 203-12 207.
103. Samols, E., Stagner, J. I., Ewart, R. B. L. & Marks, V. (1988) The order of islet microvascular cellular perfusion is B to A to D in the perfused rat pancreas, J. Clin. Invest. 82, 350-353.
104. Samols, E. & Stagner, J. I. (1990) Islet somatostalin - microvascular, paracrine and pulsatile regulation, Metabolism 39 (Suppl. 2), 55-60.
105. Santerre, R. F., Cook, R. A., Crisel, R. M. D., Sharp, J. D., Schmidt, R. J., Williams, D. C. & Wilson, C. P. (1981) Insulin synthesis in a clonal cell line of simian virus 40-transformed hamster pancreatic beta cells, Proc. Natl Acad. Sci. USA 78, 4339-4343.
106. Selden, R. F., Skoskiewicz, M. J., Howie, K. B., Russel, P. S. & Goodman, H. M. (1986) Regulation of human insulin gene expression in transgenic mice, Nature 321, 525-528.
107. Serup, P., Andersen, F. G., Petersen, E. E. & Madsen, O. D. (1992) Generation of a somatostatinoma cell line derived from a pluripotent transformed islet culture, Diabetologia 35 (Suppl. 1), A118.
108. Serup, P., Petersen, H. V., Petersen, E. E., Edlund, H., Leonard, J., Petersen, J. S., Larsson, L.-I. & Madsen, O. D. (1995) The homeodomain protein IPF1/STF1 is expressed in a subset of islet cells and promotes rat insulin 1 gene expression dependent on an intact E1 helix-loop-helix factor binding site, Biochem. J. 310, 997-1003.
109. Serup, P., Jensen, J., Andersen, F. G., Jørgensen, M. C., Blume, N., Holst, J. J. & Madsen, O. D. (1996) Induction of insulin and IAPP production in pancreatic islet glucagononia cells by insulin promoter factor 1, Proc. Natl Acad. Sci. USA 93, 9015-9020.
110. Slack, J. M. W. (1995) Developmental biology of the pancreas, Development (Camb.) 121, 1569-1580.
111. Soares, M. B., Schon, E., Henderson, A., Karathanasis, S. K., Cate, R., Zeitlin, S., Chirgwin, J. & Efstratiadis, A. (1985) RNA-mediated gene duplication: the rat preproinsulin gene is a functional retroposon, Mol. Cell. Biol. 5, 2090-2103.
112. Stein, R. (1993) Regulation of insulin gene transcription, Trends Endocrinol. Metab. 4, 96-101.
113. Steiner, D. F., Chan, S. J., Welsh, J. M. & Kwok, S. C. M. (1985) Structure and evolution of the insulin gene, Annu. Rev. Genet. 19, 463-484.
114. Takaki, R., Ono, J., Nakamura, M., Tokogawa, Y., Kumae, S., Hiraoko, T., Yamaguchi, K., Hamaguchi, K. & Uchida, S. (1986) Isolation of glucagon-secreting cell lines by cloning insulinoma cells, In Vitro (Rockville) 22, 120-126.
115. Takaki, R. (1989) Culture of pancreatic islet cells and islet producing cell lines: 'morphological and functional integrity in culture', In Vitro (Rockville) 25, 763-769.
116. Teitelman, G. (1990) Phenotypic plasticity of pancreatic islet cells, in Frontiers in diabetes research, Lessons from animal diabetes III (Shafrir, E., ed.) pp. 520-522, Smith-Gordon, London.
117. Teitelman, G. (1991) Cellular and molecular analysis of pancreatic islet cell lineage and differentiation, in Recent progress in hormone research (Bardin, C. W., ed.) pp. 259-294, Academic Press, Inc., San Diego.
118. Teitelman, G. (1993) On the origin of pancreatic endocrine cells, proliferation and neoplastic transformation, Tumor Biol. 14, 167-173.
119. Teitelman, G., Alpert, S., Polak, J. M., Martinez, A. & Hanahan, D. (1993) Precursor cells of mouse endocrine pancreas coexpress insulin, glucagon and the neuronal proteins tyrosine hydroxylase and neuropeptide Y, but not pancreatic polypeptide, Development (Camb.) 118, 1031-1039.
120. Uchida, S., Watanabe, S., Aizawa, T., Furuno, A. & Muto, T. (1979) Polyoncogenicity and insulinoma-induced ability of BK virus, a human papovavirus, in Syrian golden hamsters, J. Natl Cancer Inst. 63, 119-126.
121. Upchurch, B. H., Aponte, G. W. & Leiter, A. B. (1994) Expression of peptide YY in all four islet cell types in the developing mouse pancreas suggests a common peptide YY-producing progenitor, Development (Camb.) 120, 245-252.
122. Upchurch, B. H., Fung, B. P., Rindi, G., Ronco, A. & Leiter, A. B. (1996) Peptide YY expression is an early event in colonic endocrine cell differentiation: evidence from normal and transgenic mice, Development (Camb.) 22, 1157-1163.
123. Walker, M. D., Edlund, T., Boulet, A. M. & Rutter, W. J. (1983) Cell-specific expression controlled by the 5′ flanking regions of the insulin and chymotrypsin genes, Nature 306, 557-561.
124. Wang, R. N., Klöppel, G. & Bouwens, L. (1995) Duct-cell to islet-cell differentiation and islet growth in the pancreas of duct-ligated adult rats, Diabetologia 38, 1404-1411.
125. Watanabe, S., Abe, K., Anbo, Y. & Katoh, H. (1995) Changes in the mouse exocrine pancreas after pancreatic duct ligation: a qualitative and quantitative histological study, Arch. Histol. Cytol. 58, 365-374.
126. Wright, C. V. E., Schnegelsberg, P. & De Robertis, E. M. (1988) XIHbox 8: a novel Xenopus homeoprotein restricted to a narrow band of endoderm, Development (Camb.) 104, 787-794.