Adult pancreatic acinar cells give rise to ducts but not endocrine cells in response to growth factor signaling

Development

Volumn 137, Issue 14, 2010, Pages 2289-2296

  Blaine, Stacy A ^a   Ray, Kevin C ^a   Anunobi, Reginald ^a   Gannon, Maureen A ^a,b   Washington, Mary K ^a   Means, Anna L ^a,b  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Beta cell neogenesis; Growth factor signaling; Mouse; Transdifferentiation

Indexed keywords

TRANSFORMING GROWTH FACTOR ALPHA;

ACINAR CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL STRUCTURE; ENDOCRINE CELL; EPITHELIUM; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PANCREAS DUCT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ADULT; ANIMALS; CELL DIFFERENTIATION; CHOLANGIOPANCREATOGRAPHY, ENDOSCOPIC RETROGRADE; ENDOCRINE CELLS; EPITHELIAL CELLS; EPITHELIUM; HUMANS; INSULIN; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; ISLETS OF LANGERHANS; MICE; MICE, TRANSGENIC; PANCREAS; PANCREAS, EXOCRINE; PANCREATIC NEOPLASMS; PANCREATITIS; SIGNAL TRANSDUCTION;

RODENTIA;

EID: 77954636626     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.048421     Document Type: Article

References (42)

1. Ackermann Misfeldt, A., Costa, R. H. and Gannon, M. (2008). Beta-cell proliferation, but not neogenesis, following 60% partial pancreatectomy is impaired in the absence of FoxM1. Diabetes 57, 3069-3077.
2. Baeyens, L., De Breuck, S., Lardon, J., Mfopou, J. K., Rooman, I. and Bouwens, L. (2005). In vitro generation of insulin-producing beta cells from adult exocrine pancreatic cells. Diabetologia 48, 49-57. (Pubitemid 40174656)
3. Bonner-Weir, S., Baxter, L. A., Schuppin, G. T. and Smith, F. E. (1993). A second pathway for regeneration of adult exocrine and endocrine pancreas. A possible recapitulation of embryonic development. Diabetes 42, 1715-1720. (Pubitemid 23346407)
4. Chen, J., Baithun, S. I., Pollock, D. J. and Berry, C. L. (1988). Argyrophilic and hormone immunoreactive cells in normal and hyperplastic pancreatic ducts and exocrine pancreatic carcinoma. Virchows Arch. A Pathol. Anat. Histopathol. 413, 399-405.
5. Desai, B. M., Oliver-Krasinski, J., De Leon, D. D., Farzad, C., Hong, N., Leach, S. D. and Stoffers, D. A. (2007). Preexisting pancreatic acinar cells contribute to acinar cell, but not islet beta cell, regeneration. J. Clin. Invest. 117, 971-977. (Pubitemid 46556753)
6. Dor, Y., Brown, J., Martinez, O. I. and Melton, D. A. (2004). Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 429, 41-46. (Pubitemid 38620543)
7. el Marjou, F., Janssen, K. P., Chang, B. H., Li, M., Hindie, V., Chan, L., Louvard, D., Chambon, P., Metzger, D. and Robine, S. (2004). Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis 39, 186-193.
8. Esposito, I., Seiler, C., Bergmann, F., Kleeff, J., Friess, H. and Schirmacher, P. (2007). Hypothetical progression model of pancreatic cancer with origin in the centroacinar-acinar compartment. Pancreas 35, 212-217. (Pubitemid 47482512)
9. Gannon, M. and Wright, C. V. (1999). Endodermal patterning and organogenesis. In Cell Lineage and Fate Determination (ed. S. A. Moody), pp. 583-616. San Diego, CA: Academic Press.
10. Gidekel Friedlander, S. Y., Chu, G. C., Snyder, E. L., Girnius, N., Dibelius, G., Crowley, D., Vasile, E., DePinho, R. A. and Jacks, T. (2009). Context-dependent transformation of adult pancreatic cells by oncogenic K-Ras. Cancer Cell 16, 379-389.
11. Gu, D. and Sarvetnick, N. (1993). Epithelial cell proliferation and islet neogenesis in IFN-g transgenic mice. Development 118, 33-46. (Pubitemid 23191608)
12. Inada, A., Nienaber, C., Katsuta, H., Fujitani, Y., Levine, J., Morita, R., Sharma, A. and Bonner-Weir, S. (2008). Carbonic anhydrase II-positive pancreatic cells are progenitors for both endocrine and exocrine pancreas after birth. Proc. Natl. Acad. Sci. USA 105, 19915-19919.
13. Kloppel, G. (1993). Pathology of nonendocrine pancreatic tumors. In The Pancreas: Biology, Pathobiology, and Disease (ed. V. L. W. Go), pp. 871-897. New York: Raven Press.
14. Kloppel, G. and Maillet, B. (1998). Pathology of chronic pancreatitis. In The Pancreas, vol. 1 (ed. H. G. Beger, A. L. Warshaw, M. W. Buchler, D. L. Carr-Locke, J. P. Neoptolemos, C. Russell and M. G. Sarr), pp. 720-723. London: Blackwell Science.
15. Korc, M., Chandrasekar, B., Yamanaka, Y., Friess, H., Buchier, M. and Beger, H. G. (1992). Overexpression of the epidermal growth factor receptor in human pancreatic cancer is associated with concomitant increases in the levels of epidermal growth factor and transforming growth factor alpha. J. Clin. Invest. 90, 1352-1360.
16. Kozawa, J., Tokui, Y., Moriwaki, M., Li, M., Ohmoto, H., Yuan, M., Zhang, J., Iwahashi, H., Imagawa, A., Yamagata, K. et al. (2005). Regenerative and therapeutic effects of heparin-binding epidermal growth factor-like growth factor on diabetes by gene transduction through retrograde pancreatic duct injection of adenovirus vector. Pancreas 31, 32-42.
17. Kruse, F., Rose, S. D., Swift, G. H., Hammer, R. E. and MacDonald, R. J. (1993). An endocrine-specific element is an integral component of an exocrine-specific pancreatic enhancer. Genes Dev. 7, 774-786.
18. Lee, C. S., De Leon, D. D., Kaestner, K. H. and Stoffers, D. A. (2006). Regeneration of pancreatic islets after partial pancreatectomy in mice does not involve the reactivation of neurogenin-3. Diabetes 55, 269-272.
19. Madden, M. E. and Sarras, M. P., Jr (1989). The pancreatic ductal system of the rat: cell diversity, ultrastructure, and innervation. Pancreas 4, 472-485.
20. Means, A. L., Meszoely, I. M., Suzuki, K., Miyamoto, Y., Rustgi, A. K., Coffey, R. J., Jr, Wright, C. V., Stoffers, D. A. and Leach, S. D. (2005). Pancreatic epithelial plasticity mediated by acinar cell transdifferentiation and generation of nestin-positive intermediates. Development 132, 3767-3776.
21. Minami, K., Okuno, M., Miyawaki, K., Okumachi, A., Ishizaki, K., Oyama, K., Kawaguchi, M., Ishizuka, N., Iwanaga, T. and Seino, S. (2005). Lineage tracing and characterization of insulin-secreting cells generated from adult pancreatic acinar cells. Proc. Natl. Acad. Sci. USA 102, 15116-15121.
22. Nir, T., Melton, D. A. and Dor, Y. (2007). Recovery from diabetes in mice by beta cell regeneration. J. Clin. Invest. 117, 2553-2561.
23. Phillips, J. M., O'Reilly, L., Bland, C., Foulis, A. K. and Cooke, A. (2007). Patients with chronic pancreatitis have islet progenitor cells in their ducts, but reversal of overt diabetes in NOD mice by anti-CD3 shows no evidence for islet regeneration. Diabetes 56, 634-640.
24. Postic, C., Shiota, M., Niswender, K. D., Jetton, T. L., Chen, Y., Moates, J. M., Shelton, K. D., Lindner, J., Cherrington, A. D. and Magnuson, M. A. (1999). Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic beta cell-specific gene knock-outs using Cre recombinase. J. Biol. Chem. 274, 305-315.
25. Ray, K. C., Blaine, S. A., Washington, M. K., Braun, A. H., Singh, A. B., Harris, R. C., Harding, P. A., Coffey, R. J. and Means, A. L. (2009). Transmembrane and soluble isoforms of heparin-binding epidermal growth factor-like growth factor regulate distinct processes in the pancreas. Gastroenterology 137, 1785-1794.
26. Rooman, I., Heremans, Y., Heimberg, H. and Bouwens, L. (2000). Modulation of rat pancreatic acinoductal transdifferentiation and expression of PDX-1 in vitro. Diabetologia 43, 907-914. (Pubitemid 30463171)
27. Sandgren, E. P., Luetteke, N. C., Palmiter, R. D., Brinster, R. L. and Lee, D. C. (1990). Overexpression of TGF alpha in transgenic mice: induction of epithelial hyperplasia, pancreatic metaplasia, and carcinoma of the breast. Cell 61, 1121-1135.
28. Sharma, A., Zangen, D. H., Reitz, P., Taneja, M., Lissauer, M. E., Miller, C. P., Weir, G. C., Habener, J. F. and Bonner-Weir, S. (1999). The homeodomain protein IDX-1 increases after an early burst of proliferation during pancreatic regeneration. Diabetes 48, 507-513.
29. Solar, M., Cardalda, C., Houbracken, I., Martin, M., Maestro, M. A., De Medts, N., Xu, X., Grau, V., Heimberg, H., Bouwens, L. et al. (2009). Pancreatic exocrine duct cells give rise to insulin-producing beta cells during embryogenesis but not after birth. Dev. Cell 17, 849-860.
30. Song, S. Y., Gannon, M., Washington, M. K., Scoggins, C. R., Meszoely, I. M., Goldenring, J. R., Marino, C. R., Sandgren, E. P., Coffey, R. J., Jr, Wright, C. V. et al. (1999). Expansion of Pdx1-expressing pancreatic epithelium and islet neogenesis in transgenic mice overexpressing transforming growth factor alpha. Gastroenterology 117, 1416-1426.
31. Soriano, P. (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71.
32. Srinivas, S., Watanabe, T., Lin, C. S., William, C. M., Tanabe, Y., Jessell, T. M. and Costantini, F. (2001). Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1, 4.
33. Strobel, O., Dor, Y., Alsina, J., Stirman, A., Lauwers, G., Trainor, A., Castillo, C. F., Warshaw, A. L. and Thayer, S. P. (2007). In vivo lineage tracing defines the role of acinar-to-ductal transdifferentiation in inflammatory ductal metaplasia. Gastroenterology 133, 1999-2009.
34. Suarez-Pinzon, W. L., Lakey, J. R., Brand, S. J. and Rabinovitch, A. (2005a). Combination therapy with epidermal growth factor and gastrin induces neogenesis of human islet {beta}-cells from pancreatic duct cells and an increase in functional {beta}-cell mass. J. Clin. Endocrinol. Metab. 90, 3401-3409.
35. Suarez-Pinzon, W. L., Yan, Y., Power, R., Brand, S. J. and Rabinovitch, A. (2005b). Combination therapy with epidermal growth factor and gastrin increases beta-cell mass and reverses hyperglycemia in diabetic NOD mice. Diabetes 54, 2596-2601. (Pubitemid 41233580)
36. Teta, M., Rankin, M. M., Long, S. Y., Stein, G. M. and Kushner, J. A. (2007). Growth and regeneration of adult beta cells does not involve specialized progenitors. Dev. Cell 12, 817-826. (Pubitemid 46667754)
37. Tokui, Y., Kozawa, J., Yamagata, K., Zhang, J., Ohmoto, H., Tochino, Y., Okita, K., Iwahashi, H., Namba, M., Shimomura, I. et al. (2006). Neogenesis and proliferation of beta-cells induced by human betacellulin gene transduction via retrograde pancreatic duct injection of an adenovirus vector. Biochem. Biophys. Res. Commun. 350, 987-993.
38. Wang, R. N., Kloppel, G. and Bouwens, L. (1995). Duct- to islet-cell differentiation and islet growth in the pancreas of duct-ligated adult rats. Diabetologia 38, 1405-1411.
39. Wang, S., Jensen, J. N., Seymour, P. A., Hsu, W., Dor, Y., Sander, M., Magnuson, M. A., Serup, P. and Gu, G. (2009). Sustained Neurog3 expression in hormone-expressing islet cells is required for endocrine maturation and function. Proc. Natl. Acad. Sci. USA 106, 9715-9720.
40. Xu, X., D'Hoker, J., Stange, G., Bonne, S., De Leu, N., Xiao, X., Van de Casteele, M., Mellitzer, G., Ling, Z., Pipeleers, D. et al. (2008). Beta cells can be generated from endogenous progenitors in injured adult mouse pancreas. Cell 132, 197-207.
41. Zhang, H., Fujitani, Y., Wright, C. V. and Gannon, M. (2005). Efficient recombination in pancreatic islets by a tamoxifen-inducible Cre-recombinase. Genesis 42, 210-217. (Pubitemid 41099681)
42. Zhou, Q., Brown, J., Kanarek, A., Rajagopal, J. and Melton, D. A. (2008). In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 455, 627-632.