Aquaporin 7 Is a β-Cell Protein and Regulator of Intraislet Glycerol Content and Glycerol Kinase Activity, β-Cell Mass, and Insulin Production and Secretion

REFERENCES

• Alcazar, O., E. Gine, Z. Qiu-Yue, and J. Tamarit-Rodriguez. 1995. The stimulation of insulin secretion by d-glyceraldehyde correlates with its rate of oxidation in islet cells. Biochem. J. 310:215–220.
   PubMedGoogle Scholar
• Ashcroft, S. J., L. C. Weerasinghe, and P. J. Randle. 1973. Interrelationship of islet metabolism, adenosine triphosphate content and insulin release. Biochem. J. 132:223–231.
   PubMed Web of Science ®Google Scholar
• Borgnia, M., S. Nielsen, A. Engel, and P. Agre. 1999. Cellular and molecular biology of the aquaporin water channels. Annu. Rev. Biochem. 68:425–458.
   PubMed Web of Science ®Google Scholar
• Calvo, E. L., N. J. Dusetti, M. B. Cadenas, J. C. Dagorn, and J. L. Iovanna. 1991. Changes in gene expression during pancreatic regeneration: activation of c-myc and H-ras oncogenes in the rat pancreas. Pancreas 6:150–156.
   PubMed Web of Science ®Google Scholar
• Carbrey, J. M., D. A. Gorelick-Feldman, D. Kozono, J. Praetorius, S. Nielsen, and P. Agre. 2003. Aquaglyceroporin AQP9: solute permeation and metabolic control of expression in liver. Proc. Natl. Acad. Sci. USA 100:2945–2950.
   PubMed Web of Science ®Google Scholar
• Chang, B. H., W. Liao, L. Li, M. Nakamuta, D. Mack, and L. Chan. 1999. Liver-specific inactivation of the abetalipoproteinemia gene completely abrogates very low density lipoprotein/low density lipoprotein production in a viable conditional knockout mouse. J. Biol. Chem. 274:6051–6055.
   PubMed Web of Science ®Google Scholar
• Demeterco, C., P. Itkin-Ansari, B. Tyrberg, L. P. Ford, R. A. Jarvis, and F. Levine. 2002. c-Myc controls proliferation versus differentiation in human pancreatic endocrine cells. J. Clin. Endocrinol. Metab. 87:3475–3485.
   PubMed Web of Science ®Google Scholar
• Deng, S., M. Vatamaniuk, X. Huang, N. Doliba, M. M. Lian, A. Frank, E. Velidedeoglu, N. M. Desai, B. Koeberlein, B. Wolf, C. F. Barker, A. Naji, F. M. Matschinsky, and J. F. Markmann. 2004. Structural and functional abnormalities in the islets isolated from type 2 diabetic subjects. Diabetes 53:624–632.
   PubMed Web of Science ®Google Scholar
• Echevarria, M., E. E. Windhager, S. S. Tate, and G. Frindt. 1994. Cloning and expression of AQP3, a water channel from the medullary collecting duct of rat kidney. Proc. Natl. Acad. Sci. USA 91:10997–11001.
   PubMed Web of Science ®Google Scholar
• Efrat, S., S. Linde, H. Kofod, D. Spector, M. Delannoy, S. Grant, D. Hanahan, and S. Baekkeskov. 1988. Beta-cell lines derived from transgenic mice expressing a hybrid insulin gene-oncogene. Proc. Natl. Acad. Sci. USA 85:9037–9041.
   PubMedGoogle Scholar
• Engel, A., Y. Fujiyoshi, and P. Agre. 2000. The importance of aquaporin water channel protein structures. EMBO J. 19:800–806.
   PubMed Web of Science ®Google Scholar
• Guan, H. P., Y. Li, M. V. Jensen, C. B. Newgard, C. M. Steppan, and M. A. Lazar. 2002. A futile metabolic cycle activated in adipocytes by antidiabetic agents. Nat. Med. 8:1122–1128.
   PubMed Web of Science ®Google Scholar
• Hara-Chikuma, M., E. Sohara, T. Rai, M. Ikawa, M. Okabe, S. Sasaki, S. Uchida, and A. S. Verkman. 2005. Progressive adipocyte hypertrophy in aquaporin-7-deficient mice: adipocyte glycerol permeability as a novel regulator of fat accumulation. J. Biol. Chem. 280:15493–15496.
   PubMed Web of Science ®Google Scholar
• Hashimoto, H., H. Ishikawa, and M. Kusakabe. 1999. Preparation of whole mounts and thick sections for confocal microscopy. Methods Enzymol. 307:84–107.
   PubMedGoogle Scholar
• Hibuse, T., N. Maeda, T. Funahashi, K. Yamamoto, A. Nagasawa, W. Mizunoya, K. Kishida, K. Inoue, H. Kuriyama, T. Nakamura, T. Fushiki, S. Kihara, and I. Shimomura. 2005. Aquaporin 7 deficiency is associated with development of obesity through activation of adipose glycerol kinase. Proc. Natl. Acad. Sci. USA 102:10993–10998.
   PubMed Web of Science ®Google Scholar
• Ishibashi, K., M. Kuwahara, Y. Gu, Y. Kageyama, A. Tohsaka, F. Suzuki, F. Marumo, and S. Sasaki. 1997. Cloning and functional expression of a new water channel abundantly expressed in the testis permeable to water, glycerol, and urea. J. Biol. Chem. 272:20782–20786.
   PubMed Web of Science ®Google Scholar
• Ishibashi, K., T. Morinaga, M. Kuwahara, S. Sasaki, and M. Imai. 2002. Cloning and identification of a new member of water channel (AQP10) as an aquaglyceroporin. Biochim. Biophys. Acta 1576:335–340.
   PubMedGoogle Scholar
• Ishibashi, K., S. Sasaki, K. Fushimi, S. Uchida, M. Kuwahara, H. Saito, T. Furukawa, K. Nakajima, Y. Yamaguchi, and T. Gojobori. 1994. Molecular cloning and expression of a member of the aquaporin family with permeability to glycerol and urea in addition to water expressed at the basolateral membrane of kidney collecting duct cells. Proc. Natl. Acad. Sci. USA 91:6269–6273.
   PubMed Web of Science ®Google Scholar
• Johnson, J. D., N. T. Ahmed, D. S. Luciani, Z. Han, H. Tran, J. Fujita, S. Misler, H. Edlund, and K. S. Polonsky. 2003. Increased islet apoptosis in Pdx1+/− mice. J. Clin. Investig. 111:1147–1160.
   PubMed Web of Science ®Google Scholar
• Jonas, J. C., A. Sharma, W. Hasenkamp, H. Ilkova, G. Patane, R. Laybutt, S. Bonner-Weir, and G. C. Weir. 1999. Chronic hyperglycemia triggers loss of pancreatic beta cell differentiation in an animal model of diabetes. J. Biol. Chem. 274:14112–14121.
   PubMed Web of Science ®Google Scholar
• Kahn, S. E., D. K. McCulloh, and D. J. Porte. 1997. Insulin secretion in the normal and diabetic human, p. 337–353. In K. G. M. M. Alberti, P. Zimmet, R. A. DeFronzo, and H. Keen (ed.), International textbook of diabetes mellitus. John Wiley & Sons, New York, NY.
   Google Scholar
• Kahn, S. E. 2003. The relative contributions of insulin resistance and beta-cell dysfunction to the pathophysiology of type 2 diabetes. Diabetologia 46:3–19.
   PubMed Web of Science ®Google Scholar
• Kaneto, H., A. Sharma, K. Suzuma, D. R. Laybutt, G. Xu, S. Bonner-Weir, and G. C. Weir. 2002. Induction of c-Myc expression suppresses insulin gene transcription by inhibiting NeuroD/BETA2-mediated transcriptional activation. J. Biol. Chem. 277:12998–13006.
   PubMed Web of Science ®Google Scholar
• Kaneto, H., K. Suzuma, A. Sharma, S. Bonner-Weir, G. L. King, and G. C. Weir. 2002. Involvement of protein kinase C beta 2 in c-myc induction by high glucose in pancreatic beta-cells. J. Biol. Chem. 277:3680–3685.
   PubMedGoogle Scholar
• Kishida, K., I. Shimomura, H. Kondo, H. Kuriyama, Y. Makino, H. Nishizawa, N. Maeda, M. Matsuda, N. Ouchi, S. Kihara, Y. Kurachi, T. Funahashi, and Y. Matsuzawa. 2001. Genomic structure and insulin-mediated repression of the aquaporin adipose (AQPap), adipose-specific glycerol channel. J. Biol. Chem. 276:36251–36260.
   PubMed Web of Science ®Google Scholar
• Ko, S. B., S. Naruse, M. Kitagawa, H. Ishiguro, S. Furuya, N. Mizuno, Y. Wang, T. Yoshikawa, A. Suzuki, S. Shimano, and T. Hayakawa. 2002. Aquaporins in rat pancreatic interlobular ducts. Am. J. Physiol. Gastrointest. Liver Physiol. 282:G324–G331.
   PubMedGoogle Scholar
• Kojima, H., M. Fujimiya, K. Matsumura, T. Nakahara, M. Hara, and L. Chan. 2004. Extrapancreatic insulin-producing cells in multiple organs in diabetes. Proc. Natl. Acad. Sci. USA 101:2458–2463.
   PubMed Web of Science ®Google Scholar
• Kondo, H., I. Shimomura, K. Kishida, H. Kuriyama, Y. Makino, H. Nishizawa, M. Matsuda, N. Maeda, H. Nagaretani, S. Kihara, Y. Kurachi, T. Nakamura, T. Funahashi, and Y. Matsuzawa. 2002. Human aquaporin adipose (AQPap) gene. Genomic structure, promoter analysis and functional mutation. Eur. J. Biochem. 269:1814–1826.
   PubMedGoogle Scholar
• Kulkarni, R. N., J. N. Winnay, M. Daniels, J. C. Bruning, S. N. Flier, D. Hanahan, and C. R. Kahn. 1999. Altered function of insulin receptor substrate-1-deficient mouse islets and cultured beta-cell lines. J. Clin. Investig. 104:R69–R75.
   PubMed Web of Science ®Google Scholar
• Laybutt, D. R., G. C. Weir, H. Kaneto, J. Lebet, R. D. Palmiter, A. Sharma, and S. Bonner-Weir. 2002. Overexpression of c-Myc in beta-cells of transgenic mice causes proliferation and apoptosis, downregulation of insulin gene expression, and diabetes. Diabetes 51:1793–1804.
   PubMed Web of Science ®Google Scholar
• Liu, Z., J. Shen, J. M. Carbrey, R. Mukhopadhyay, P. Agre, and B. P. Rosen. 2002. Arsenite transport by mammalian aquaglyceroporins AQP7 and AQP9. Proc. Natl. Acad. Sci. USA 99:6053–6058.
   PubMed Web of Science ®Google Scholar
• MacDonald, M. J. 2002. Differences between mouse and rat pancreatic islets: succinate responsiveness, malic enzyme, and anaplerosis. Am. J. Physiol. Endocrinol. Metab. 283:E302–E310.
   PubMedGoogle Scholar
• Maeda, N., T. Funahashi, T. Hibuse, A. Nagasawa, K. Kishida, H. Kuriyama, T. Nakamura, S. Kihara, I. Shimomura, and Y. Matsuzawa. 2004. Adaptation to fasting by glycerol transport through aquaporin 7 in adipose tissue. Proc. Natl. Acad. Sci. USA 101:17801–17806.
   PubMed Web of Science ®Google Scholar
• Mobasheri, A., M. Shakibaei, and D. Marples. 2004. Immunohistochemical localization of aquaporin 10 in the apical membranes of the human ileum: a potential pathway for luminal water and small solute absorption. Histochem. Cell Biol. 121:463–471.
   PubMedGoogle Scholar
• Morinaga, T., M. Nakakoshi, A. Hirao, M. Imai, and K. Ishibashi. 2002. Mouse aquaporin 10 gene (AQP10) is a pseudogene. Biochem. Biophys. Res. Commun. 294:630–634.
   PubMedGoogle Scholar
• Nagy, A., E. Gocza, E. M. Diaz, V. R. Prideaux, E. Ivanyi, M. Markkula, and J. Rossant. 1990. Embryonic stem cells alone are able to support fetal development in the mouse. Development 110:815–821.
   PubMed Web of Science ®Google Scholar
• NIH. 1985. Principles of laboratory animal care. Publication no. 85023. NIH, Bethesda, MD.
   Google Scholar
• Noel, R. J., P. A. Antinozzi, J. D. McGarry, and C. B. Newgard. 1997. Engineering of glycerol-stimulated insulin secretion in islet beta cells. Differential metabolic fates of glucose and glycerol provide insight into mechanisms of stimulus-secretion coupling. J. Biol. Chem. 272:18621–18627.
   PubMedGoogle Scholar
• Prudente, S., E. Flex, E. Morini, F. Turchi, D. Capponi, S. De Cosmo, V. Tassi, V. Guida, A. Avogaro, F. Folli, F. Maiani, L. Frittitta, B. Dallapiccola, and V. Trischitta. 2007. A functional variant of the adipocyte glycerol channel aquaporin 7 gene is associated with obesity and related metabolic abnormalities. Diabetes 56:1468–1474.
   PubMed Web of Science ®Google Scholar
• Skelly, R. H., B. Wicksteed, P. A. Antinozzi, and C. J. Rhodes. 2001. Glycerol-stimulated proinsulin biosynthesis in isolated pancreatic rat islets via adenoviral-induced expression of glycerol kinase is mediated via mitochondrial metabolism. Diabetes 50:1791–1798.
   PubMed Web of Science ®Google Scholar
• Skowronski, M. T., J. Lebeck, A. Rojek, J. Praetorius, E. M. Fuchtbauer, J. Frokiaer, and S. Nielsen. 2007. AQP7 is localized in capillaries of adipose tissue, cardiac and striated muscle: implications in glycerol metabolism. Am. J. Physiol. Renal Physiol. 292:F956–F965.
   PubMed Web of Science ®Google Scholar
• Tsukaguchi, H., C. Shayakul, U. V. Berger, B. Mackenzie, S. Devidas, W. B. Guggino, A. N. van Hoek, and M. A. Hediger. 1998. Molecular characterization of a broad selectivity neutral solute channel. J. Biol. Chem. 273:24737–24743.
   PubMed Web of Science ®Google Scholar
• Weir, G. C., D. R. Laybutt, H. Kaneto, S. Bonner-Weir, and A. Sharma. 2001. Beta-cell adaptation and decompensation during the progression of diabetes. Diabetes 50(Suppl. 1):S154–S159.
   PubMedGoogle Scholar
• Zawalich, W. S., K. C. Zawalich, G. J. Tesz, J. A. Sterpka, and W. M. Philbrick. 2001. Insulin secretion and IP levels in two distant lineages of the genus Mus: comparisons with rat islets. Am. J. Physiol. Endocrinol. Metab. 280:E720–E728.
   PubMedGoogle Scholar