Exchange protein activated by cAMP 1 (Epac1)-deficient mice develop β-cell dysfunction and metabolic syndrome

FASEB Journal

Volumn 27, Issue 10, 2013, Pages 4122-4135

  Kai, Alan K L ^a   Lam, Amy K M ^a   Chen, Yingxian ^a   Tai, Andrew C P ^a   Zhang, Xinmei ^b   Lai, Angela K W ^a   Yeung, Patrick K K ^a   Tam, Sidney ^b   Wang, Jian ^c   Lam, Karen S ^a,b   Vanhoutte, Paul M ^a,b   Bos, Johannes L ^d   Chung, Stephen S M ^e   Xu, Aimin ^a,b   Chung, Sookja K ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^d UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^e BNU HKBU UNITED INTERNATIONAL COLLEGE   (China)

Author keywords

Glucose transporter type 2; Glucose stimulated insulin secretion; High fat diet induced obesity; Hyperglycemia; Multiple lowdose streptozotocin induced diabetes

Indexed keywords

ANTIPORTER; CYCLIC AMP; EPAC 1 PROTEIN; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; GLUCOSE TRANSPORTER 2; INSULIN; MESSENGER RNA; PROTEIN; STREPTOZOCIN; TRANSCRIPTION FACTOR PDX 1; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; EPAC PROTEIN, MOUSE; FAT INTAKE; GLUCOSE BLOOD LEVEL; GUANINE NUCLEOTIDE EXCHANGE FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOARCHITECTURE; EMBRYO; EMBRYONIC STEM CELL; GENE DELETION; GLUCOSE TOLERANCE; HYPERGLYCEMIA; IN VITRO STUDY; IN VIVO STUDY; INSULIN RELEASE; INSULITIS; LUNG GAS EXCHANGE; MALE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL; TRIACYLGLYCEROL BLOOD LEVEL; ANIMAL; EXPERIMENTAL DIABETES MELLITUS; FAT INTAKE; GENETICS; GLUCOSE BLOOD LEVEL; KNOCKOUT MOUSE; METABOLIC SYNDROME X; METABOLISM; OBESITY;

MUS;

ANIMALS; BLOOD GLUCOSE; DIABETES MELLITUS, EXPERIMENTAL; DIETARY FATS; EMBRYONIC STEM CELLS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; INSULIN-SECRETING CELLS; METABOLIC SYNDROME X; MICE; MICE, KNOCKOUT; OBESITY;

EID: 84885160578     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-230433     Document Type: Article

References (45)

1. Pilkis, S. J., Claus, T. H., and El-Maghrabi, M. R. (1988) The role of cyclic AMP in rapid and long-term regulation of gluconeogenesis and glycolysis. Adv. Second Messenger Phosphoprotein Res. 22, 175-191
2. Overton, H. A., Fyfe, M. C, and Reynet, C. (2008) GPR 119, a novel G protein-coupled receptor target for the treatment of type 2 diabetes and obesity. Brit. J. Pharmacol. 153(Suppl. 1), S76-S81
3. Holz, G. G, and Habener, J. F. (1992) Signal transduction crosstalk in the endocrine system: pancreatic beta-cells and the glucose competence concept. Trends Biochem. Sci. 17, 388-393
4. McKnight, G. S., Cummings, D. E., Amieux, P. S., Sikorski, M. A., Planas, J. V., Motamed, K., and Idzerda, R. L. (1998) Cyclic AMP, PKA, and the physiological regulation of adiposity. Recent Progr. Hormone Res. 53, 139-159; discussion 160-131
5. Collins, S., and Surwit, R. S. (2001) The -adrenergic receptors and the control of adipose tissue metabolism and thermogenesis. Recent Progr. Hormone Res. 56, 309-328
6. De Rooij, J., Zwartkruis, F. J., Verheijen, M. H., Cool, R. H., Wittinghofer, A., and Bos, J. L. (1998) Epac is a Rap1 guanine-nucleotide- exchange factor directly activated by cyclic AMP. Nature 396, 474-477
7. Ueno, H., Shibasaki, T., Iwanaga, T., Takahashi, K., Liu, L. M., Yokoi, N., Ozaki, N., Matsukura, S., Yano, H., and Seino, S. (2001) Characterization of the gene EPAC2: structure, chromosomal localization, tissue expression, and identification of the liver-specific isoform. Genomics 78, 91-98
8. Leech, C. A., Holz, G. G, Chepurny, O., and Habener, J. F. (2000) Expression of cAMP-regulated guanine nucleotide exchange factors in pancreatic beta-cells. Biochem. Biophys. Res. Commun. 278, 44-47
9. Bos, J. L. (2006) Epac proteins: multi-purpose cAMP targets. Trends Biochem. Sci. 31, 680-686
10. Kang, G., Joseph, J. W., Chepurny, O. G., Monaco, M., Bos, J. L., Schwede, F., Genieser, H. G, and Holz, G. G (2003) Epac-selective cAMP analog 8-pCPT-2'-O-Me-cAMP as a stimulus for Ca +-induced Ca + release and exocytosis in pancreatic beta-cells. J. Biol. Chem. 278, 8279-8285
11. Liu, M. J., Han, J., Lee, Y. S., Park, M. S., and Jun, H. S. (2010) Amelioration of hyperglycemia by intestinal overexpression of glucagon-like peptide-1 in mice. J. Mol. Med. 88, 351-358
12. Movassat, J., Beattie, G. M., Lopez, A. D., and Hayek, A. (2002) Exendin 4 up-regulates expression of PDX 1 and hastens differentiation and maturation of human fetal pancreatic cells. J. Clin. Endocrinol. Metab. 87, 4775-4781
13. Li, H., Lam, A., Xu, A. M., Lam, K. S., and Chung, S. K. (2010) High dosage of Exendin-4 increased early insulin secretion in differentiated beta cells from mouse embryonic stem cells. Acta Pharmacol. Sin. 31, 570-577
14. Ho, H. T., Chung, S. K., Law, J. W., Ko, B. C, Tam, S. C, Brooks, H. L., and Chung, S. S. (2000) Aldose reductase-deficient mice develop nephrogenic diabetes insipidus. Mol. Cell. Biol. 20, 5840-5846
15. Mortensen, R. M., Conner, D. A., Chao, S., Geisterfer-Lowrance, A. A., and Seidman, J. G. (1992) Production of homozygous mutant ES cells with a single targeting construct. Mol. Cell. Biol. 12, 2391-2395
16. Harrity, T., Farrelly, D., Tieman, A., Chu, C, Kunselman, L., Ponticiello, R, Cap, M., Qu, F., Shao, C, Wang, W., Zhang, H., Fenderson, W., Chen, S., Devasthale, P., Jeon, Y, Seethala, R, Yang, W. P., Ren, J., Zhou, M., Ryono, D., Biller, S., Mookhtiar, K. A., Wetterau, J., Gregg, R, Cheng, P. T., and Hariharan, N. (2006) Muraglitazar, a novel dual (alpha/gamma) peroxisome proliferator-activated receptor activator, improves diabetes and other metabolic abnormalities and preserves beta-cell function in db/db mice. Diabetes 55, 240-248
17. Kawasaki, H., Springett, G. M., Mochizuki, N., Toki, S., Matsuda, M., Housman, D. E., and Graybiel, A. M. (1998) A family of cAMP-binding proteins that directly activate Rap1. Science 282, 2275-2279
18. Li, D. S., Yuan, Y. H., Tu, H. J., Liang, Q. L., and Dai, L. J. (2009) A protocol for islet isolation from mouse pancreas. Nat. Protoc. 4, 1649-1652
19. Schroeder, I. S., Rolletschek, A., Blyszczuk, P., Kania, G., and Wobus, A. M. (2006) Differentiation of mouse embryonic stem cells to insulin-producing cells. Nat. Protoc. 1, 495-507
20. Bock, T., Pakkenberg, B., and Buschard, K. (2003) Increased islet volume but unchanged islet number in ob/ob mice. Diabetes 52, 1716-1722
21. Morioka, T., Asilmaz, E., Hu, J., Dishinger, J. F., Elias, C. F., Li, H., Elmquist, J. K., Kennedy, R. T., and Kulkarni, R. N. (2007) Disruption of leptin receptor expression in the pancreas directly affects beta cell growth and function in mice. J. Clin. Invest. 117, 2860-2868
22. Li, Y., Hansotia, T., Yusta, B., Ris, F., and Drucker, D. J. (2003) Glucagon-like peptide-1 receptor signaling modulates beta cell apoptosis. J. Biol. Chem. 278, 471-478
23. Green, E. A., Eynon, E. E., and Flavell, R. A. (1998) Local expression of TNF-a in neonatal NOD mice promotes diabetes by enhancing presentation of islet antigens. Immunity 9, 733-743
24. Bergman, R. N., and Ader, M. (2000) Free fatty acids and pathogenesis of type 2 diabetes mellitus. Trends Endocrinol. Metab. 11, 351-356
25. O'Brien, B. A., Harmon, B. V., Cameron, D. P., and Allan, D. J. (1996) (3-cell apoptosis is responsible for the development of IDDM in the multiple low-dose streptozotocin model. J. Pathol. 178, 176-181
26. Deng, S., Vatamaniuk, M., Huang, X., Doliba, N., Frank, A., Velidedeoglu, E., Desai, N. M., Koeberlein, B., Wolf, B., Barker, C. F., Naji, A., Matschinsky, F. M., and Markmann, J. F. (2004) Structural and functional abnormalities in the islets isolated from type 2 diabetic subjects. Diabetes 53, 624-632
27. Price, L. S., Hajdo-Milasinovic, A., Zhao, J., Zwartkruis, F. J., and Bos, J. L. (2004) Rap1 regulates E-cadherinmediated cell-cell adhesion. J. Biol. Chem. 279, 35127-35132
28. Esni, F., Taljedal, I. B., Perl, A. K., Cremer, H., and Semb, H. (1999) Neural cell adhesion molecule (N-CAM) is required for cell type segregation and normal ultrastructure in pancreatic islets. J. Cell. Biol. 144, 325-337
29. Guillam, M. T., Hummler, E., Schaerer, E., Yeh, J. I., Beermann, F., Schmidt, A., Deriaz, N., and Thorens, B. (1997) Early diabetes and abnormal postnatal pancreatic islet development in mice lacking Glut-2. Nat. Genet. 17, 327-330
30. Jorns, A., Tiedge, M., Sickel, E., and Lenzen, S. (1996) Loss of GLUT2 glucose transporter expression in pancreatic beta cells from diabetic Chinese hamsters. Virchows Arch. 428, 177-185
31. Reimer, M. K., and Ahren, B. (2002) Altered β-cell distribution of pdx-1 and GLUT-2 after a short-term challenge with a high-fat diet in C57BL/6J mice. Diabetes 51(Suppl. 1), S138-S143
32. Doyle, M. E., and Egan, J. M. (2007) Mechanisms of action of glucagon-like peptide 1 in the pancreas. Pharmacol. Ther. 113, 546-593
33. Xu, G., Stoffers, D. A., Habener, J. F., and Bonner-Weir, S. (1999) Exendin-4 stimulates both β-cell replication and neogenesis, resulting in increased β-cell mass and improved glucose tolerance in diabetic rats. Diabetes 48, 2270-2276
34. Thorens, B., Porret, A., Buhler, L., Deng, S. P., and Widmann, C. (1993) Cloning and functional expression of the human islet GLP-1 receptor. Demonstration that exendin-4 is an agonist and exendin-(9-39) an antagonist of the receptor. Diabetes 42, 1678-1682
35. Zhao, A. Z. (2005) Control of food intake through regulation of cAMP. Curr. Topics Dev. Biol. 67, 207-224
36. Yan, J., Mei, F. C., Cheng, H., Lao, D. H., Wei, J., Patrikeev, I., Hao, D., Stutz, S. J., Dineley, K. T., Motamedi, M., Hommel, J. D., Cunningham, K. A., Chen, J., and Cheng, X. (2013) Enhanced leptin sensitivity, reduced adiposity, and improved glucose homeostasis in mice lacking exchange protein directly activated by cyclic AMP isoform 1. Mol. Cell. Biol. 33, 918-926
37. Conarello, S. L., Li, Z., Ronan, J., Roy, R. S., Jiang, G., Liu, F., Woods, J., Zycband, E., Moller, D. E., Thornberry, N. A., and Zhang, B. B. (2003) Mice lacking dipeptidyl peptidase IV are protected against obesity and insulin resistance. Proc. Natl. Acad. Sci. U. S. A. 100, 6825-6830
38. Okada, T., Liew, C. W., Hu, J., Hinault, C., Krtzfeldt, J., Yin, C, Holzenberger, M., Stoffel, M., and Kulkarni, R. N. (2007) Insulin receptors in β-cells are critical for islet compensatory growth response to insulin resistance. Proc. Natl. Acad. Sci. U. S. A. 104, 8977-8982
39. Von Herrath, M., Sanda, S., and Herold, K. (2007) Type 1 diabetes as a relapsing-remitting disease? Nat. Rev. Immunol. 7, 988-994
40. Kahn, S. E., Hull, R. L., and Utzschneider, K. M. (2006) Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 444, 840-846
41. Pick, A., Clark, J., Kubstrup, C, Levisetti, M., Pugh, W., and Polonsky, K. S. (1998) Role of apoptosis in failure of β-cell mass compensation for insulin resistance and beta-cell defects in the male Zucker diabetic fatty rat. Diabetes 47, 358-364
42. Butler, A. E., Janson, J., Bonner-Weir, S., Ritzel, R., and Butler, P. C. (2003) β-cell deficit and increased β-cell apoptosis in humans with type 2 diabetes. Diabetes 52, 102-110
43. Koh, G., Suh, K. S., Chon, S., Oh, S., Kim, S. W., Kim, J. W., and Kim, Y. S. (2005) Elevated cAMP level attenuates 2-deoxy-d-ribose-induced oxidative damage in pancreatic betacells. Arch. Biochem. Biophys. 438, 70-79
44. Kwon, G., Pappan, K. L., Marshall, C. A., Schaffer, J. E., and McDaniel, M. L. (2004) cAMP Dose-dependently prevents palmitate-induced apoptosis by both protein kinase A-and cAMP-guanine nucleotide exchange factor-dependent pathways in beta-cells. J. Biol. Chem. 279, 8938-8945
45. Aston-Mourney, K., Proietto, J., Morahan, G., and Andrikopoulos, S. (2008) Too much of a good thing: why it is bad to stimulate the beta cell to secrete insulin. Diabetologia 51, 540-545