Pancreatic Exocrine Duct Cells Give Rise to Insulin-Producing β Cells during Embryogenesis but Not after Birth

Developmental Cell

Volumn 17, Issue 6, 2009, Pages 849-860

  Solar, Myriam ^a,b   Cardalda, Carina ^a,b   Houbracken, Isabelle ^c,d   Martín, Mercè ^a,b   Maestro, Miguel Angel ^a,b   De Medts, Nele ^c,d   Xu, Xiaobo ^c,d   Grau, Vanessa ^a,b   Heimberg, Harry ^c,d   Bouwens, Luc ^c,d   Ferrer, Jorge ^a,b,e  

^a ALBA SYNCHROTRON LIGHT SOURCE   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c DIABETES RESEARCH CENTER   (Belgium)

^d JDRF Center for Beta Cell Therapy in Diabetes   (Belgium)

^e HOSPITAL CLÍNIC   (Spain)

Author keywords

DEVBIO; HUMDISEASE; STEMCELL

Indexed keywords

ALLOXAN; EPIDERMAL GROWTH FACTOR; GASTRIN; HEPATOCYTE NUCLEAR FACTOR 1BETA; TAMOXIFEN;

ACINAR CELL; ANIMAL CELL; ARTICLE; BRANCHING MORPHOGENESIS; CELL DIFFERENTIATION; CELL FATE; CELL GROWTH; CELL LABELING; CELL LINEAGE; CELL REGENERATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENDOCRINE CELL; IMMUNOHISTOCHEMISTRY; MOUSE; NEWBORN; NONHUMAN; PANCREAS DUCT; PANCREAS DUCT LIGATION; PANCREAS ISLET BETA CELL; PERINATAL DEVELOPMENT; PRIORITY JOURNAL; TRANSGENIC MOUSE;

ANIMALS; FEMALE; HEPATOCYTE NUCLEAR FACTOR 1-BETA; INSULIN-SECRETING CELLS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PANCREAS; PANCREAS, EXOCRINE;

EID: 71649092364     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2009.11.003     Document Type: Article

References (47)

1. Baeyens L., Bonne S., Bos T., Rooman I., Peleman C., Lahoutte T., German M., Heimberg H., and Bouwens L. Notch signaling as gatekeeper of rat acinar-to-beta cell conversion in vitro. Gastroenterology 136 (2009) 1499-1502
2. Bensley R.R. Studies on the pancreas of the guinea pig. Am. J. Anat. 12 (1911) 297-388
3. Boj S.F., Parrizas M., Maestro M.A., and Ferrer J. A transcription factor regulatory circuit in differentiated pancreatic cells. Proc. Natl. Acad. Sci. USA 98 (2001) 14481-14486
4. Bonner-Weir S. Perspective: Postnatal pancreatic beta cell growth. Endocrinology 141 (2000) 1926-1929
5. Bonner-Weir S., Baxter L.A., Schuppin G.T., and Smith F.E. A second pathway for regeneration of adult exocrine and endocrine pancreas. A possible recapitulation of embryonic development. Diabetes 42 (1993) 1715-1720
6. Desai B.M., Oliver-Krasinski J., De Leon D.D., Farzad C., Hong N., Leach S.D., and Stoffers D.A. Preexisting pancreatic acinar cells contribute to acinar cell, but not islet beta cell, regeneration. J. Clin. Invest. 117 (2007) 971-977
7. Dor Y., Brown J., Martinez O.I., and Melton D.A. Adult pancreatic beta cells are formed by self-duplication rather than stem cell differentiation. Nature 429 (2004) 41-46
8. Gu D., and Sarvetnick N. Epithelial cell proliferation and islet neogenesis in IFN-g transgenic mice. Development 118 (1993) 33-46
9. Gu G., Dubauskaite J., and Melton D.A. Direct evidence for the pancreatic lineage: NGN3+ cells are islet progenitors and are distinct from duct progenitors. Development 129 (2002) 2447-2457
10. Hald J., Sprinkel A.E., Ray M., Serup P., Wright C., and Madsen O.D. Generation and characterization of Ptf1a antiserum and localization of Ptf1a in relation to Nkx6.1 and Pdx1 during the earliest stages of mouse pancreas development. J. Histochem. Cytochem. 56 (2008) 587-595
11. Haumaitre C., Barbacci E., Jenny M., Ott M.O., Gradwohl G., and Cereghini S. Lack of TCF2/vHNF1 in mice leads to pancreas agenesis. Proc. Natl. Acad. Sci. USA 102 (2005) 1490-1495
12. Haumaitre C., Fabre M., Cormier S., Baumann C., Delezoide A.L., and Cereghini S. Severe pancreas hypoplasia and multicystic renal dysplasia in two human fetuses carrying novel HNF1beta/MODY5 mutations. Hum. Mol. Genet. 15 (2006) 2363-2375
13. Hayashi S., and McMahon A.P. Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev. Biol. 244 (2002) 305-318
14. Herrera P.L. Adult insulin- and glucagon-producing cells differentiate from two independent cell lineages. Development 127 (2000) 2317-2322
15. Inada A., Nienaber C., Katsuta H., Fujitani Y., Levine J., Morita R., Sharma A., and Bonner-Weir S. Carbonic anhydrase II-positive pancreatic cells are progenitors for both endocrine and exocrine pancreas after birth. Proc. Natl. Acad. Sci. USA 105 (2008) 19915-19919
16. Jonsson J., Carlsson L., Edlund T., and Edlund H. Insulin-promoter-factor 1 is required for pancreas development in mice. Nature 371 (1994) 606-609
17. Kawaguchi Y., Cooper B., Gannon M., Ray M., MacDonald R.J., and Wright C.V. The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nat. Genet. 32 (2002) 128-134
18. Kellendonk C., Tronche F., Casanova E., Anlag K., Opherk C., and Schutz G. Inducible site-specific recombination in the brain. J. Mol. Biol. 285 (1999) 175-182
19. Laguesse E. Le pancréas. Revue Générale d'Histologie 2 (1906) 3
20. Liu P., Jenkins N.A., and Copeland N.G. A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res. 13 (2003) 476-484
21. Lynn F.C., Smith S.B., Wilson M.E., Yang K.Y., Nekrep N., and German M.S. Sox9 coordinates a transcriptional network in pancreatic progenitor cells. Proc. Natl. Acad. Sci. USA 104 (2007) 10500-10505
22. Maestro M.A., Boj S.F., Luco R.F., Pierreux C.E., Cabedo J., Servitja J.M., German M.S., Rousseau G.G., Lemaigre F.P., and Ferrer J. Hnf6 and Tcf2 (MODY5) are linked in a gene network operating in a precursor cell domain of the embryonic pancreas. Hum. Mol. Genet. 12 (2003) 3307-3314
23. Minami K., Okuno M., Miyawaki K., Okumachi A., Ishizaki K., Oyama K., Kawaguchi M., Ishizuka N., Iwanaga T., and Seino S. Lineage tracing and characterization of insulin-secreting cells generated from adult pancreatic acinar cells. Proc. Natl. Acad. Sci. USA 102 (2005) 15116-15121
24. Montanya E., Nacher V., Biarnes M., and Soler J. Linear correlation between beta cell mass and body weight throughout the lifespan in Lewis rats: role of beta cell hyperplasia and hypertrophy. Diabetes 49 (2000) 1341-1346
25. Nagasao J., Yoshioka K., Amasaki H., and Mutoh K. Centroacinar and intercalated duct cells as potential precursors of pancreatic endocrine cells in rats treated with streptozotocin. Ann. Anat. 185 (2003) 211-216
26. Nammo T., Yamagata K., Tanaka T., Kodama T., Sladek F.M., Fukui K., Katsube F., Sato Y., Miyagawa J., and Shimomura I. Expression of HNF-4alpha (MODY1), HNF-1beta (MODY5), and HNF-1alpha (MODY3) proteins in the developing mouse pancreas. Gene Expr. Patterns 8 (2008) 96-106
27. Nir T., Melton D.A., and Dor Y. Recovery from diabetes in mice by beta cell regeneration. J. Clin. Invest. 117 (2007) 2553-2561
28. Parrizas M., Maestro M.A., Boj S.F., Paniagua A., Casamitjana R., Gomis R., Rivera F., and Ferrer J. Hepatic nuclear factor 1-alpha directs nucleosomal hyperacetylation to its tissue-specific transcriptional targets. Mol. Cell. Biol. 21 (2001) 3234-3243
29. Phillips J.M., O'Reilly L., Bland C., Foulis A.K., and Cooke A. 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 (2007) 634-640
30. Pictet R.L., Clark W.R., Williams R.H., and Rutter W.J. An ultrastructural analysis of the developing embryonic pancreas. Dev. Biol. 29 (1972) 436-467
31. Pierreux C.E., Poll A.V., Kemp C.R., Clotman F., Maestro M.A., Cordi S., Ferrer J., Leyns L., Rousseau G.G., and Lemaigre F.P. The transcription factor hepatocyte nuclear factor-6 controls the development of pancreatic ducts in the mouse. Gastroenterology 130 (2006) 532-541
32. Rooman I., and Bouwens L. Combined gastrin and epidermal growth factor treatment induces islet regeneration and restores normoglycaemia in C57Bl6/J mice treated with alloxan. Diabetologia 47 (2004) 259-265
33. Rosenberg L. In vivo cell transformation: neogenesis of beta cells from pancreatic ductal cells. Cell Transplant. 4 (1995) 371-383
34. Rukstalis J.M., and Habener J.F. Snail2, a mediator of epithelial-mesenchymal transitions, expressed in progenitor cells of the developing endocrine pancreas. Gene Expr. Patterns 7 (2007) 471-479
35. Scaglia L., Cahill C.J., Finegood D.T., and Bonner-Weir S. Apoptosis participates in the remodeling of the endocrine pancreas in the neonatal rat. Endocrinology 138 (1997) 1736-1741
36. Seymour P.A., Freude K.K., Dubois C.L., Shih H.P., Patel N.A., and Sander M. A dosage-dependent requirement for Sox9 in pancreatic endocrine cell formation. Dev. Biol. 323 (2008) 19-30
37. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21 (1999) 70-71
38. Strobel O., Dor Y., Stirman A., Trainor A., Fernandez-del C.C., Warshaw A.L., and Thayer S.P. Beta cell transdifferentiation does not contribute to preneoplastic/metaplastic ductal lesions of the pancreas by genetic lineage tracing in vivo. Proc. Natl. Acad. Sci. USA 104 (2007) 4419-4424
39. Suarez-Pinzon W.L., Lakey J.R., Brand S.J., and Rabinovitch A. 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 (2005) 3401-3409
40. Suarez-Pinzon W.L., Yan Y., Power R., Brand S.J., and Rabinovitch A. Combination therapy with epidermal growth factor and gastrin increases beta cell mass and reverses hyperglycemia in diabetic NOD mice. Diabetes 54 (2005) 2596-2601
41. Teta M., Rankin M.M., Long S.Y., Stein G.M., and Kushner J.A. Growth and regeneration of adult beta cells does not involve specialized progenitors. Dev. Cell 12 (2007) 817-826
42. Walker N.I., Winterford C.M., and Kerr J.F. Ultrastructure of the rat pancreas after experimental duct ligation. II. Duct and stromal cell proliferation, differentiation, and deletion. Pancreas 7 (1992) 420-434
43. Wang R.N., Kloppel G., and Bouwens L. Duct- to islet cell differentiation and islet growth in the pancreas of duct-ligated adult rats. Diabetologia 38 (1995) 1405-1411
44. Wang R.N., Bouwens L., and Kloppel G. Beta cell growth in adolescent and adult rats treated with streptozotocin during the neonatal period. Diabetologia 39 (1996) 548-557
45. Xu X., D'Hoker J., Stange G., Bonne S., De Leu N., Xiao X., Van De C.M., Mellitzer G., Ling Z., Pipeleers D., et al. Beta cells can be generated from endogenous progenitors in injured adult mouse pancreas. Cell 132 (2008) 197-207
46. Zhou Q., Law A.C., Rajagopal J., Anderson W.J., Gray P.A., and Melton D.A. A multipotent progenitor domain guides pancreatic organogenesis. Dev. Cell 13 (2007) 103-114
47. Zhou Q., Brown J., Kanarek A., Rajagopal J., and Melton D.A. In vivo reprogramming of adult pancreatic exocrine cells to beta cells. Nature 455 (2008) 627-632