Lineage tracing reveals the dynamic contribution of Hes1+ cells to the developing and adult pancreas

Development

Volumn 138, Issue 3, 2011, Pages 431-441

  Kopinke, Daniel ^a   Brailsford, Marisa ^a   Shea, Jill E ^a   Leavitt, Rebecca ^a   Scaife, Courtney L ^a   Murtaugh, L Charles ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Hes1; Mouse; Notch; Pancreas; Stem cell

Indexed keywords

NOTCH RECEPTOR;

ACINAR CELL; ADULT STEM CELL; ALLELE; ANIMAL EXPERIMENT; ARTICLE; CELL LINEAGE; CONTROLLED STUDY; DYNAMICS; EMBRYO; EMBRYO DEVELOPMENT; GENE; GENE EXPRESSION PROFILING; HES1 GENE; LARGE INTESTINE; MOUSE; NONHUMAN; ORGANOGENESIS; PANCREAS; PRIORITY JOURNAL; SMALL INTESTINE;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; HOMEODOMAIN PROTEINS; INSULIN-SECRETING CELLS; INTESTINES; LIVER; MICE; MICE, MUTANT STRAINS; MICROSCOPY, FLUORESCENCE; PANCREAS; STEM CELLS;

EID: 78751515624     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.053843     Document Type: Article

References (62)

1. Antoniou, A., Raynaud, P., Cordi, S., Zong, Y., Tronche, F., Stanger, B. Z., Jacquemin, P., Pierreux, C. E., Clotman, F. and Lemaigre, F. P. (2009). Intrahepatic bile ducts develop according to a new mode of tubulogenesis regulated by the transcription factor SOX9. Gastroenterology 136, 2325-2333.
2. Apelqvist, A., Li, H., Sommer, L., Beatus, P., Anderson, D. J., Honjo, T., Hrabe de Angelis, M., Lendahl, U. and Edlund, H. (1999). Notch signalling controls pancreatic cell differentiation. Nature 400, 877-881.
3. Barker, N., van Es, J. H., Kuipers, J., Kujala, P., van den Born, M., Cozijnsen, M., Haegebarth, A., Korving, J., Begthel, H., Peters, P. J. et al. (2007). Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449, 1003-1007.
4. Barker, N., Ridgway, R. A., van Es, J. H., van de Wetering, M., Begthel, H., van den Born, M., Danenberg, E., Clarke, A. R., Sansom, O. J. and Clevers, H. (2009). Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457, 608-611.
5. Chiba, S. (2006). Notch signaling in stem cell systems. Stem Cells 24, 2437-2447.
6. Crosnier, C., Stamataki, D. and Lewis, J. (2006). Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat. Rev. Genet. 7, 349-359.
7. De La O, J. P., Emerson, L. L., Goodman, J. L., Froebe, S. C., Illum, B. E., Curtis, A. B. and Murtaugh, L. C. (2008). Notch and Kras reprogram pancreatic acinar cells to ductal intraepithelial neoplasia. Proc. Natl. Acad. Sci. USA 105, 18907-18912.
8. 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.
9. 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.
10. Dovey, H. F., John, V., Anderson, J. P., Chen, L. Z., de Saint Andrieu, P., Fang, L. Y., Freedman, S. B., Folmer, B., Goldbach, E., Holsztynska, E. J. et al. (2001). Functional gamma-secretase inhibitors reduce beta-amyloid peptide levels in brain. J. Neurochem. 76, 173-181.
11. Esni, F., Ghosh, B., Biankin, A. V., Lin, J. W., Albert, M. A., Yu, X., MacDonald, R. J., Civin, C. I., Real, F. X., Pack, M. A. et al. (2004). Notch inhibits Ptf1 function and acinar cell differentiation in developing mouse and zebrafish pancreas. Development 131, 4213-4224.
12. Farley, F. W., Soriano, P., Steffen, L. S. and Dymecki, S. M. (2000). Widespread recombinase expression using FLPeR (flipper) mice. Genesis 28, 106-110.
13. Feil, R., Wagner, J., Metzger, D. and Chambon, P. (1997). Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochem. Biophys. Res. Commun. 237, 752-757.
14. Geisler, F., Nagl, F., Mazur, P. K., Lee, M., Zimber-Strobl, U., Strobl, L. J., Radtke, F., Schmid, R. M. and Siveke, J. T. (2008). Liver-specific inactivation of Notch2, but not Notch1, compromises intrahepatic bile duct development in mice. Hepatology 48, 607-616.
15. Gittes, G. K. (2009). Developmental biology of the pancreas: a comprehensive review. Dev. Biol. 326, 4-35.
16. Golson, M. L., Loomes, K. M., Oakey, R. and Kaestner, K. H. (2009). Ductal malformation and pancreatitis in mice caused by conditional Jag1 deletion. Gastroenterology 136, 1761-1771.
17. Gradwohl, G., Dierich, A., LeMeur, M. and Guillemot, F. (2000). neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas. Proc. Natl. Acad. Sci. USA 97, 1607-1611.
18. Greenwood, A. L., Li, S., Jones, K. and Melton, D. A. (2007). Notch signaling reveals developmental plasticity of Pax4(+) pancreatic endocrine progenitors and shunts them to a duct fate. Mech. Dev. 124, 97-107.
19. Gu, G., Dubauskaite, J. and 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.
20. Hald, J., Hjorth, J. P., German, M. S., Madsen, O. D., Serup, P. and Jensen, J. (2003). Activated Notch1 prevents differentiation of pancreatic acinar cells and attenuate endocrine development. Dev. Biol. 260, 426-437.
21. Harada, N., Tamai, Y., Ishikawa, T., Sauer, B., Takaku, K., Oshima, M. and Taketo, M. M. (1999). Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J. 18, 5931-5942.
22. Hayashi, K. Y., Tamaki, H., Handa, K., Takahashi, T., Kakita, A. and Yamashina, S. (2003). Differentiation and proliferation of endocrine cells in the regenerating rat pancreas after 90% pancreatectomy. Arch. Histol. Cytol. 66, 163-174.
23. Herrera, P. L., Huarte, J., Sanvito, F., Meda, P., Orci, L. and Vassalli, J. D. (1991). Embryogenesis of the murine endocrine pancreas; early expression of pancreatic polypeptide gene. Development 113, 1257-1265.
24. 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.
25. Ishibashi, M., Ang, S. L., Shiota, K., Nakanishi, S., Kageyama, R. and Guillemot, F. (1995). Targeted disruption of mammalian hairy and Enhancer of split homolog-1 (HES-1) leads to up-regulation of neural helix-loop-helix factors, premature neurogenesis, and severe neural tube defects. Genes Dev. 9, 3136-3148.
26. Jensen, J., Pedersen, E. E., Galante, P., Hald, J., Heller, R. S., Ishibashi, M., Kageyama, R., Guillemot, F., Serup, P. and Madsen, O. D. (2000). Control of endodermal endocrine development by Hes-1. Nat. Genet. 24, 36-44.
27. Kageyama, R., Ohtsuka, T. and Kobayashi, T. (2007). The Hes gene family: repressors and oscillators that orchestrate embryogenesis. Development 134, 1243-1251.
28. Kobayashi, H., Spilde, T. L., Li, Z., Marosky, J. K., Bhatia, A. M., Hembree, M. J., Prasadan, K., Preuett, B. L. and Gittes, G. K. (2002). Lectin as a marker for staining and purification of embryonic pancreatic epithelium. Biochem. Biophys. Res. Commun. 293, 691-697.
29. Kodama, Y., Hijikata, M., Kageyama, R., Shimotohno, K. and Chiba, T. (2004). The role of notch signaling in the development of intrahepatic bile ducts. Gastroenterology 127, 1775-1786.
30. Kopinke, D. and Murtaugh, L. C. (2010). Exocrine-to-endocrine differentiation is detectable only prior to birth in the uninjured mouse pancreas. BMC Dev. Biol. 10, 38.
31. Lai, E. C. (2004). Notch signaling: control of cell communication and cell fate. Development 131, 965-973.
32. Lammert, E., Brown, J. and Melton, D. A. (2000). Notch gene expression during pancreatic organogenesis. Mech. Dev. 94, 199-203.
33. Lee, J. C., Smith, S. B., Watada, H., Lin, J., Scheel, D., Wang, J., Mirmira, R. G. and German, M. S. (2001). Regulation of the pancreatic pro-endocrine gene neurogenin3. Diabetes 50, 928-936.
34. Liu, P., Jenkins, N. A. and Copeland, N. G. (2003). A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res. 13, 476-484.
35. Lozier, J., McCright, B. and Gridley, T. (2008). Notch signaling regulates bile duct morphogenesis in mice. PLoS ONE 3, e1851.
36. Miyamoto, Y., Maitra, A., Ghosh, B., Zechner, U., Argani, P., Iacobuzio-Donahue, C. A., Sriuranpong, V., Iso, T., Meszoely, I. M., Wolfe, M. S. et al. (2003). Notch mediates TGF alpha-induced changes in epithelial differentiation during pancreatic tumorigenesis. Cancer Cell 3, 565-576.
37. Murtaugh, L. C., Stanger, B. Z., Kwan, K. M. and Melton, D. A. (2003). Notch signaling controls multiple steps of pancreatic differentiation. Proc. Natl. Acad. Sci. USA 100, 14920-14925.
38. Murtaugh, L. C., Law, A. C., Dor, Y. and Melton, D. A. (2005). Beta-Catenin is essential for pancreatic acinar but not islet development. Development 132, 4663-4674.
39. Nagasao, J., Yoshioka, K., Amasaki, H. and Mutoh, K. (2003). Centroacinar and intercalated duct cells as potential precursors of pancreatic endocrine cells in rats treated with streptozotocin. Ann. Anat. 185, 211-216.
40. Nagy, A., Rossant, J., Nagy, R., Abramow-Newerly, W. and Roder, J. C. (1993). Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. USA 90, 8424-8428.
41. Nakhai, H., Siveke, J. T., Klein, B., Mendoza-Torres, L., Mazur, P. K., Algul, H., Radtke, F., Strobl, L., Zimber-Strobl, U. and Schmid, R. M. (2008). Conditional ablation of Notch signaling in pancreatic development. Development 135, 2757-2765.
42. Parsons, M. J., Pisharath, H., Yusuff, S., Moore, J. C., Siekmann, A. F., Lawson, N. and Leach, S. D. (2009). Notch-responsive cells initiate the secondary transition in larval zebrafish pancreas. Mech. Dev. 126, 898-912.
43. Pictet, R. and Rutter, W. J. (1972). Development of the embryonic endocrine pancreas. In Handbook of Physiology, Section 7, vol. 1 (ed. D. Steiner and N. Freinkel), pp. 25-66. Baltimore: Williams & Williams.
44. Rovira, M., Scott, S. G., Liss, A. S., Jensen, J., Thayer, S. P. and Leach, S. D. (2010). Isolation and characterization of centroacinar/terminal ductal progenitor cells in adult mouse pancreas. Proc. Natl. Acad. Sci. USA 107, 75-80.
45. Sangiorgi, E. and Capecchi, M. R. (2008). Bmi1 is expressed in vivo in intestinal stem cells. Nat. Genet. 40, 915-920.
46. Schroder, N. and Gossler, A. (2002). Expression of Notch pathway components in fetal and adult mouse small intestine. Gene Expr. Patterns 2, 247-250.
47. Scoggins, C. R., Meszoely, I. M., Wada, M., Means, A. L., Yang, L. and Leach, S. D. (2000). p53-dependent acinar cell apoptosis triggers epithelial proliferation in duct-ligated murine pancreas. Am. J. Physiol. Gastrointest. Liver Physiol. 279, G827-G836.
48. Seymour, P. A., Freude, K. K., Dubois, C. L., Shih, H. P., Patel, N. A. and Sander, M. (2008). A dosage-dependent requirement for Sox9 in pancreatic endocrine cell formation. Dev. Biol. 323, 19-30.
49. 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.
50. Soriano, P. (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71.
51. 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.
52. Stanger, B. Z., Stiles, B., Lauwers, G. Y., Bardeesy, N., Mendoza, M., Wang, Y., Greenwood, A., Cheng, K. H., McLaughlin, M., Brown, D. et al. (2005). Pten constrains centroacinar cell expansion and malignant transformation in the pancreas. Cancer Cell 8, 185-195.
53. Thorel, F., Nepote, V., Avril, I., Kohno, K., Desgraz, R., Chera, S. and Herrera, P. L. (2010). Conversion of adult pancreatic alpha-cells to beta-cells after extreme beta-cell loss. Nature 464, 1149-1154.
54. Vooijs, M., Ong, C. T., Hadland, B., Huppert, S., Liu, Z., Korving, J., van den Born, M., Stappenbeck, T., Wu, Y., Clevers, H. et al. (2007). Mapping the consequence of Notch1 proteolysis in vivo with NIP-CRE. Development 134, 535-544.
55. 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.
56. Watanabe, S., Abe, K., Anbo, Y. and 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.
57. 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.
58. Yee, N. S., Lorent, K. and Pack, M. (2005). Exocrine pancreas development in zebrafish. Dev. Biol. 284, 84-101.
59. Zecchin, E., Filippi, A., Biemar, F., Tiso, N., Pauls, S., Ellertsdottir, E., Gnugge, L., Bortolussi, M., Driever, W. and Argenton, F. (2006). Distinct delta and jagged genes control sequential segregation of pancreatic cell types from precursor pools in zebrafish. Dev. Biol. 301, 192-204.
60. Zhou, Q., Law, A. C., Rajagopal, J., Anderson, W. J., Gray, P. A. and Melton, D. A. (2007). A multipotent progenitor domain guides pancreatic organogenesis. Dev. Cell 13, 103-114.
61. Zhu, L., Gibson, P., Currle, D. S., Tong, Y., Richardson, R. J., Bayazitov, I. T., Poppleton, H., Zakharenko, S., Ellison, D. W. and Gilbertson, R. J. (2008). Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature 457, 603-607.
62. Zong, Y., Panikkar, A., Xu, J., Antoniou, A., Raynaud, P., Lemaigre, F. and Stanger, B. Z. (2009). Notch signaling controls liver development by regulating biliary differentiation. Development 136, 1727-1739.