A mouse model for monitoring islet cell genesis and developing therapies for diabetes

DMM Disease Models and Mechanisms

Volumn 4, Issue 2, 2011, Pages 268-276

  Shimajiri, Yoshinori ^a,c   Kosaka, Yasuhiro ^a   Scheel, David W ^a   Lynn, Francis C ^a   Kishimoto, Nina ^a   Wang, Juehu ^a   Zhao, Shuhong ^a   German, Michael S ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c WAKAYAMA MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; BIOLOGICAL FACTOR; ENHANCED GREEN FLUORESCENT PROTEIN; GAMMA SECRETASE INHIBITOR; GROWTH DIFFERENTIATION FACTOR 11; NEUROGENIN 3; NOTCH RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL DIFFERENTIATION; CELL MATURATION; DIABETES MELLITUS; DISEASE MODEL; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; GENETIC CODE; HOMOLOGOUS RECOMBINATION; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; ISLET CELL GENESIS; MALE; MOUSE; NONHUMAN; PANCREAS DUCT; PANCREAS ISLET CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; RNA ISOLATION; SIGNAL TRANSDUCTION; STEM CELL; TRANSGENE; TRANSGENIC MOUSE;

ALKALINE PHOSPHATASE; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BONE MORPHOGENETIC PROTEINS; CELL LINEAGE; DIABETES MELLITUS; FETUS; GREEN FLUORESCENT PROTEINS; GROWTH DIFFERENTIATION FACTORS; HUMANS; ISLETS OF LANGERHANS; MICE; MICE, TRANSGENIC; MODELS, ANIMAL; NERVE TISSUE PROTEINS; ORGANOGENESIS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; TRANSGENES;

ANIMALIA; MUS; MUS MUSCULUS;

EID: 79952350477     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.002998     Document Type: Article

References (45)

1. Apelqvist, A., Li, H., Sommer, L., Beatus, P., Anderson, D. J., Honjo, T., Hrabe de Angelis, M., Lendahl, U. and Edlund, H. (1999). Notch signaling controls pancreatic cell differentiation. Nature 400, 877-881. (Pubitemid 29406724)
2. Baeyens, L., Bonne, S., German, M. S., Ravassard, P., Heimberg, H. and Bouwens, L. (2006). Ngn3 expression during postnatal in vitro beta cell neogenesis induced by the JAK/STAT pathway. Cell Death Differ. 13, 1892-1899. (Pubitemid 44542402)
3. Dichmann, D. S., Miller, C. P., Jensen, J., Scott Heller, R. and Serup, P. (2003). Expression and misexpression of members of the FGF and TGFbeta families of growth factors in the developing mouse pancreas. Dev. Dyn. 226, 663-674. (Pubitemid 36396875)
4. 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. (Pubitemid 32044380)
5. Dror, V., Nguyen, V., Walia, P., Kalynyak, T. B., Hill, J. A. and Johnson, J. D. (2007). Notch signalling suppresses apoptosis in adult human and mouse pancreatic islet cells. Diabetologia 50, 2504-2515.
6. Gasa, R., Mrejen, C., Leachman, N., Otten, M., Barnes, M., Wang, J., Chakrabarti, S., Mirmira, R. and German, M. (2004). Proendocrine genes coordinate the pancreatic islet differentiation program in vitro. Proc. Natl. Acad. Sci. USA 101, 13245-13250. (Pubitemid 39209650)
7. Giddings, S. J., Chirgwin, J. and Permutt, M. A. (1985). Evaluation of rat insulin messenger RNA in pancreatic and extra pancreatic tissues. Diabetologia 28, 343-347.
8. 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. (Pubitemid 30118489)
9. 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.
10. 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. (Pubitemid 36966084)
11. Harmon, E. B., Apelqvist, A. A., Smart, N. G., Gu, X., Osborne, D. H. and Kim, S. K. (2004). GDF11 modulates NGN3+ islet progenitor cell number and promotes beta-cell differentiation in pancreas development. Development 131, 6163-6174.
12. Heremans, Y., Van De Casteele, M., in't Veld, P., Gradwohl, G., Serup, P., Madsen, O., Pipeleers, D. and Heimberg, H. (2002). Recapitulation of embryonic neuroendocrine differentiation in adult human pancreatic duct cells expressing neurogenin 3. J. Cell Biol. 159, 303-312.
13. Hiramatsu, N., Kasai, A., Hayakawa, K., Nagai, K., Kubota, T., Yao, J. and Kitamura, M. (2006). Secreted protein-based reporter systems for monitoring inflammatory events: critical interference by endoplasmic reticulum stress. J. Immunol. Methods 315, 202-207. (Pubitemid 44414822)
14. Huang, H. P., Liu, M., El-Hodiri, H. M., Chu, K., Jamrich, M. and Tsai, M. J. (2000). Regulation of the pancreatic islet-specific gene BETA2 (neuroD) by neurogenin 3. Mol. Cell. Biol. 20, 3292-3307. (Pubitemid 30215041)
15. 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.
16. Jacquemin, P., Durviaux, S. M., Jensen, J., Godfraind, C., Gradwohl, G., Guillemot, F., Madsen, O. D., Carmeliet, P., Dewerchin, M., Collen, D. et al. (2000). Transcription factor hepatocyte nuclear factor 6 regulates pancreatic endocrine cell differentiation and controls expression of the proendocrine gene ngn3. Mol. Cell. Biol. 20, 4445-4454. (Pubitemid 30346639)
17. Jenny, M., Uhl, C., Roche, C., Duluc, I., Guillermin, V., Guillemot, F., Jensen, J., Kedinger, M. and Gradwohl, G. (2002). Neurogenin3 is differentially required for endocrine cell fate specification in the intestinal and gastric epithelium. EMBO J. 21, 6338-6347. (Pubitemid 35448412)
18. Jensen, J., Heller, R. S., Funder-Nielsen, T., Pedersen, E. E., Lindsell, C., Weinmaster, G., Madsen, O. D. and Serup, P. (2000a). 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. (Pubitemid 30070993)
19. Jensen, J., Pedersen, E. E., Galante, P., Hald, J., Heller, R. S., Ishibashi, M., Kageyama, R., Guillemot, F., Serup, P. and Madsen, O. D. (2000b). Control of endodermal endocrine development by Hes-1. Nat. Genet. 24, 36-44.
20. Johansson, K. A., Dursun, U., Jordan, N., Gu, G., Beermann, F., Gradwohl, G. and Grapin-Botton, A. (2007). Temporal control of neurogenin3 activity in pancreas progenitors reveals competence windows for the generation of different endocrine cell types. Dev. Cell 12, 457-465.
21. Kodama, S., Toyonaga, T., Kondo, T., Matsumoto, K., Tsuruzoe, K., Kawashima, J., Goto, H., Kume, K., Kume, S., Sakakida, M. et al. (2005). Enhanced expression of PDX-1 and Ngn3 by exendin-4 during beta cell regeneration in STZ-treated mice. Biochem. Biophys. Res. Commun. 327, 1170-1178. (Pubitemid 40137989)
22. Laybutt, D. R., Preston, A. M., Akerfeldt, M. C., Kench, J. G., Busch, A. K., Biankin, A. V. and Biden, T. J. (2007). Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes. Diabetologia 50, 752-763. (Pubitemid 46355827)
23. Lee, C. S., Perreault, N., Brestelli, J. E. and Kaestner, K. H. (2002). Neurogenin 3 is essential for the proper specification of gastric enteroendocrine cells and the maintenance of gastric epithelial cell identity. Genes Dev. 16, 1488-1497.
24. 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.
25. Lee, H. C., Bonner-Weir, S., Weir, G. C. and Leahy, J. L. (1989). Compensatory adaption to partial pancreatectomy in the rat. Endocrinology 124, 1571-1575.
26. 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. (Pubitemid 32374521)
27. Lynn, F. C., Smith, S. B., Wilson, M. E., Yang, K. Y., Nekrep, N. and German, M. S. (2007). Sox9 coordinates a transcriptional network in pancreatic progenitor cells. Proc. Natl. Acad. Sci. USA 104, 10500-10505. (Pubitemid 47185694)
28. 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. (2003). Hnf6 and Tcf2 (MODY5) are linked in a gene network operating in a precursor cell domain of the embryonic pancreas. Hum. Mol. Genet. 12, 3307-3314. (Pubitemid 37541076)
29. Mellitzer, G., Martin, M., Sidhoum-Jenny, M., Orvain, C., Barths, J., Seymour, P. A., Sander, M. and Gradwohl, G. (2004). Pancreatic islet progenitor cells in neurogenin 3-yellow fluorescent protein knock-add-on mice. Mol. Endocrinol. 18, 2765-2776. (Pubitemid 39482064)
30. Mellitzer, G., Bonne, S., Luco, R. F., Van De Casteele, M., Lenne-Samuel, N., Collombat, P., Mansouri, A., Lee, J., Lan, M., Pipeleers, D. et al. (2006). IA1 is NGN3-dependent and essential for differentiation of the endocrine pancreas. EMBO J. 25, 1344-1352.
31. 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.
32. Schwitzgebel, V. M., Scheel, D. W., Conners, J. R., Kalamaras, J., Lee, J. E., Anderson, D. J., Sussel, L., Johnson, J. D. and German, M. S. (2000). Expression of neurogenin3 reveals an islet cell precursor population in the pancreas. Development 127, 3533-3542.
33. Slack, J. M. (1995). Developmental biology of the pancreas. Development 121, 1569-1580.
34. Smith, S. B., Gasa, R., Watada, H., Wang, J., Griffen, S. C. and German, M. S. (2003). Neurogenin3 and hepatic nuclear factor 1 cooperate in activating pancreatic expression of Pax4. J. Biol. Chem. 278, 38254-38259. (Pubitemid 37221715)
35. Smith, S. B., Watada, H. and German, M. S. (2004). Neurogenin3 activates the islet differentiation program while repressing its own expression. Mol. Endocrinol. 18, 142-149. (Pubitemid 38073160)
36. Villasenor, A., Chong, D. C. and Cleaver, O. (2008). Biphasic Ngn3 expression in the developing pancreas. Dev. Dyn. 237, 3270-3279.
37. 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.
38. Wang, S., Hecksher-Sorensen, J., Xu, Y., Zhao, A., Dor, Y., Rosenberg, L., Serup, P. and Gu, G. (2008). Myt1 and Ngn3 form a feed-forward expression loop to promote endocrine islet cell differentiation. Dev. Biol. 317, 531-540.
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. Watada, H., Scheel, D. W., Leung, J. and German, M. S. (2003). Distinct gene expression programs function in progenitor and mature islet cells. J. Biol. Chem. 278, 17130-17140. (Pubitemid 36799591)
41. Wilson, M. E., Scheel, D. and German, M. S. (2003). Gene expression cascades in pancreatic development. Mech. Dev. 120, 65-80. (Pubitemid 35469131)
42. Wilson, M. E., Yang, K. Y., Kalousova, A., Lau, J., Kosaka, Y., Lynn, F. C., Wang, J., Mrejen, C., Episkopou, V., Clevers, H. C. et al. (2005). The HMG Box transcription factor Sox4 contributes to the development of the endocrine pancreas. Diabetes 54, 3402-3409. (Pubitemid 43334329)
43. 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. (Pubitemid 351181232)
44. Yamaoka, T., Idehara, C., Yano, M., Matsushita, T., Yamada, T., Ii, S., Moritani, M., Hata, J., Sugino, H., Noji, S. et al. (1998). Hypoplasia of pancreatic islets in transgenic mice expressing activin receptor mutants. J. Clin. Invest. 102, 294-301. (Pubitemid 28335188)
45. Yang, X. W., Model, P. and Heintz, N. (1997). Homologous recombination based modification in Escherichia coli and germline transmission in transgenic mice of a bacterial artificial chromosome. Nat. Biotechnol. 15, 859-865.