Aquaporins pp 233-249 | Cite as
Role of Aquaporin-7 and Aquaporin-9 in Glycerol Metabolism; Involvement in Obesity
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The discovery of aquaporin (AQP) has had a great impact on life sciences. So far, 13 AQPs have been identified in human. AQP3, 7, 9, and 10 are subcategorized as aquaglyceroporins which permeabilize glycerol as well as water. Many investigators have demonstrated that AQPs play a crucial role in maintaining water homeostasis, but the physiological significance of some AQPs as a glycerol channel has not been fully understood. Adipocyte is considered to be a major source of glycerol which is one of substrates for hepatic gluconeogenesis. This review focuses on recent studies of glycerol metabolism through AQP7 and AQP9, and discusses the importance of glycerol channel in adipose tissues and liver.
Keywords
Microsomal Triglyceride Transfer Protein Hormone Sensitive Lipase Glycerol Kinase Glycerol Metabolism Peroxisome Proliferator Response ElementPreview
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References
- Agre P, King LS, Yasui M, Guggino WB, Ottersen OP, Fujiyoshi Y, Engel A, Nielsen S (2002) Aquaporin water channels — from atomic structure to clinical medicine. J Physiol (London) 542:3–16CrossRefGoogle Scholar
- Badaut J, Regli L (2004) Distribution and possible roles of aquaporin 9 in the brain. Neuroscience 129:971–981PubMedCrossRefGoogle Scholar
- Badaut J, Hirt L, Granziera C, Bogousslavsky J, Magistretti PJ, Regli L (2001) Astrocyte-specific expression of aquaporin-9 in mouse brain is increased after transient focal cerebral ischemia. J Cereb Blood Flow Metab 21:477–482PubMedCrossRefGoogle Scholar
- Badaut J, Petit JM, Brunet JF, Magistretti PJ, Charriaut-Marlangue C, Regli L (2004) Distribution of Aquaporin 9 in the adult rat brain: preferential expression in catecholaminergic neurons and in glial cells. Neuroscience 128:27–38PubMedCrossRefGoogle Scholar
- Carbrey JM, Gorelick-Feldman DA, Kozono D, Praetorius J, Nielsen S, Agre P (2003) Aquaglyceroporin AQP9: solute permeation and metabolic control of expression in liver. Proc Natl Acad Sci U S A 100:2945–2950PubMedCrossRefGoogle Scholar
- Ceperuelo-Mallafré V, Miranda M, Chacón MR, Vilarrasa N, Megia A, Gutiérrez C, Fernández-Real JM, Gómez JM, Caubet E, Frühbeck G, Vendrell J (2007) Adipose tissue expression of the glycerol channel aquaporin-7 gene is altered in severe obesity but not in type 2 diabetes. J Clin Endocrinol Metab 92:3640–3645PubMedCrossRefGoogle Scholar
- Crosbie RH, Dovico SA, Flanagan JD, Chamberlain JS, Ownby CL, Campbell KP (2002) Characterization of aquaporin-4 in muscle and muscular dystrophy. FASEB J 16:943–949PubMedCrossRefGoogle Scholar
- Elkjaer M, Vajda Z, Nejsum LN, Kwon T, Jensen UB, Amiry-Moghaddam M, Frokiaer J, Nielsen S (2000) Immunolocalization of AQP9 in liver, epididymis, testis, spleen, and brain. Biochem Biophys Res Commun 276:1118–1128PubMedCrossRefGoogle Scholar
- Executive Summary of The Third Report of The National Cholesterol Education Program (NCEP) (2001) Expert Panel on Detection, Evaluation, And Treatment of High Blood Cholesterol In Adults (Adult Treatment Panel III). JAMA 285:2486–2497CrossRefGoogle Scholar
- Friedman JM (2004) Modern science versus the stigma of obesity. Nat Med 10:563–569PubMedCrossRefGoogle Scholar
- Frigeri A, Nicchia GP, Verbavatz JM, Valenti G, Svelto M (1998) Expression of aquaporin-4 in fast-twitch fibers of mammalian skeletal muscle. J Clin Invest 102:695–703PubMedCrossRefGoogle Scholar
- Frigeri A, Nicchia GP, Nico B, Quondamatteo F, Herken R, Roncali L, Svelto M (2001) Aquaporin-4 deficiency in skeletal muscle and brain of dystrophic mdx mice. FASEB J 15:90–98PubMedCrossRefGoogle Scholar
- Frigeri A, Nicchia GP, Repetto S, Bado M, Minetti C, Svelto M (2002) Altered aquaporin-4 expression in human muscular dystrophies: a common feature?. FASEB J 16:1120–1122PubMedGoogle Scholar
- Fujioka S, Matsuzawa Y, Tokunaga K, Tarui S (1987) Contribution of intra-abdominal fat accumulation to the impairment of glucose and lipid metabolism in human obesity. Metabolism 36:54–59PubMedCrossRefGoogle Scholar
- Funahashi T, Nakamura T, Shimomura I, Maeda K, Kuriyama H, Takahashi M, Arita Y, Kihara S, Matsuzawa Y (1999) Role of adipocytokines on the pathogenesis of atherosclerosis in visceral obesity. Intern Med 38:202–206PubMedCrossRefGoogle Scholar
- Guan HP, Li Y, Jensen MV, Newgard CB, Steppan CM, Lazar MA (2002) A futile metabolic cycle activated in adipocytes by antidiabetic agents. Nat Med 8:1122–1128PubMedCrossRefGoogle Scholar
- Hara-Chikuma M, Sohara E, Rai T, Ikawa M, Okabe M, Sasaki S, Uchida S, Verkman AS (2005) Progressive adipocyte hypertrophy in aquaporin-7-deficient mice: adipocyte glycerol permeability as a novel regulator of fat accumulation. J Biol Chem 280:15493–15496CrossRefGoogle Scholar
- Heymann JB, Engel A (2000) Structural clues in the sequences of the aquaporins. J Mol Biol 295:1039–1053PubMedCrossRefGoogle Scholar
- Hibuse T, Maeda N, Funahashi T, Yamamoto K, Nagasawa A, Mizunoya W, Kishida K, Inoue K, Kuriyama H, Nakamura T, Fushiki T, Kihara S, Shimomura I (2005) Aquaporin 7 deficiency is associated with development of obesity through activation of adipose glycerol kinase. Proc Natl Acad Sci U S A 102:10993–10998PubMedCrossRefGoogle Scholar
- Hibuse T, Maeda N, Nagasawa A, Funahashi T (2006) Aquaporins and glycerol metabolism. Biochim Biophys Acta 1758:1004–1011PubMedCrossRefGoogle Scholar
- Ibrahimi A, Sfeir Z, Magharaie H, Amri EZ, Grimaldi P, Abumrad NA (1996) Expression of the CD36 homolog (FAT) in fibroblast cells: effects on fatty acid transport. Proc Natl Acad Sci U S A 93:2646–2651PubMedCrossRefGoogle Scholar
- Ishibashi K, Kuwahara M, Gu Y, Kageyama Y, Tohsaka A, Suzuki F, Marumo F, Sasaki S (1997) Cloning and functional expression of a new water channel abundantly expressed in the testis permeable to water, glycerol, and urea. J Biol Chem 272:20782–20786PubMedCrossRefGoogle Scholar
- Ishibashi K, Kuwahara M, Gu Y, Tanaka Y, Marumo F, Sasaki S (1998) Cloning and functional expression of a new aquaporin (AQP9) abundantly expressed in the peripheral leukocytes permeable to water and urea, but not to glycerol. Biochem Biophys Res Commun 244:268–274PubMedCrossRefGoogle Scholar
- Jimi T, Wakayama Y, Matsuzaki Y, Hara H, Inoue M, Shibuya S (2004) Reduced expression of aquaporin 4 in human muscles with amyotrophic lateral sclerosis and other neurogenic atrophies. Pathol Res Pract 200:203–209PubMedCrossRefGoogle Scholar
- Kahn BB, Flier JS (2000) Obesity and insulin resistance. J Clin Invest 106:473–481PubMedCrossRefGoogle Scholar
- Kanai H, Matsuzawa Y, Kotani K, Keno Y, Kobatake T, Nagai Y, Fujioka S, Tokunaga K, Tarui S (1990) Close correlation of intra-abdominal fat accumulation to hypertension in obese women. Hypertension 16:484–490PubMedGoogle Scholar
- Kishida K, Kuriyama H, Funahashi T, Shimomura I, Kihara S, Ouchi N, Nishida M, Nishizawa H, Matsuda M, Takahashi M, Hotta K, Nakamura T, Yamashita S, Tochino Y, Matsuzawa Y (2000) Aquaporin adipose, a putative glycerol channel in adipocytes. J Biol Chem 275:20896–20902PubMedCrossRefGoogle Scholar
- Kishida K, Shimomura I, Kondo H, Kuriyama H, Makino Y, Nishizawa H, Maeda N, Matsuda M, Ouchi N, Kihara S, Kurachi Y, Funahashi T, Matsuzawa Y (2001a) Genomic structure and insulin-mediated repression of the aquaporin adipose (AQPap), adipose-specific glycerol channel. J Biol Chem 276:36251–36260CrossRefGoogle Scholar
- Kishida K, Shimomura I, Nishizawa H, Maeda N, Kuriyama H, Kondo H, Matsuda M, Nagaretani H, Ouchi N, Hotta K, Kihara S, Kadowaki T, Funahashi T, Matsuzawa Y (2001b) Enhancement of the aquaporin adipose gene expression by a peroxisome proliferator-activated receptor gamma. J Biol Chem 276:48572–48579Google Scholar
- Kondo H, Shimomura I, Kishida K, Kuriyama H, Makino Y, Nishizawa H, Matsuda M, Maeda N, Nagaretani H, Kihara S, Kurachi Y, Nakamura T, Funahashi T, Matsuzawa Y (2002) Human aquaporin adipose (AQPap) gene. Genomic structure, promoter analysis and functional mutation. Eur J Biochem 269:1814–1826PubMedCrossRefGoogle Scholar
- Ko SB, Uchida S, Naruse S, Kuwahara M, Ishibashi K, Marumo F, Hayakawa T, Sasaki S (1999) Cloning and functional expression of rAOP9L a new member of aquaporin family from rat liver. Biochem Mol Biol Int 47:309–318PubMedGoogle Scholar
- Kuriyama H, Kawamoto S, Ishida N, Ohno I, Mita S, Matsuzawa Y, Matsubara K, Okubo K (1997) Molecular cloning and expression of a novel human aquaporin from adipose tissue with glycerol permeability. Biochem Biophys Res Commun 241:53–58PubMedCrossRefGoogle Scholar
- Kuriyama H, Yamashita S, Shimomura I, Funahashi T, Ishigami M, Aragane K, Miyaoka K, Nakamura T, Takemura K, Man Z, Toide K, Nakayama N, Fukuda Y, Lin MC, Wetterau JR, Matsuzawa Y (1998) Enhanced expression of hepatic acyl-coenzyme A synthetase and microsomal triglyceride transfer protein messenger RNAs in the obese and hypertriglyceridemic rat with visceral fat accumulation. Hepatology 27:557–562PubMedCrossRefGoogle Scholar
- Kuriyama H, Shimomura I, Kishida K, Kondo H, Furuyama N, Nishizawa H, Maeda N, Matsuda M, Nagaretani H, Kihara S, Nakamura T, Tochino Y, Funahashi T, Matsuzawa Y (2002) Coordinated regulation of fat-specific and liver-specific glycerol channels, aquaporin adipose and aquaporin 9. Diabetes 51:2915–2921PubMedCrossRefGoogle Scholar
- Kuwahara M, Fushimi K, Terada Y, Bai L, Marumo F, Sasaki S (1995) cAMP-dependent phosphorylation stimulates water permeability of aquaporin-collecting duct water channel protein expressed in Xenopus oocytes. J Biol Chem 270:10384–10387PubMedCrossRefGoogle Scholar
- Liu JW, Wakayama Y, Inoue M, Shibuya S, Kojima H, Jimi T, Oniki H (1999) Immunocytochemical studies of aquaporin 4 in the skeletal muscle of mdx mouse. J Neurol Sci 164:24–28PubMedCrossRefGoogle Scholar
- Liu Z, Shen J, Carbrey JM, Mukhopadhyay R, Agre P, Rosen BP (2002) Arsenite transport by mammalian aquaglyceroporins AQP7 and AQP9. Proc Natl Acad Sci U S A 99:6053–6058PubMedCrossRefGoogle Scholar
- Liu Y, Promeneur D, Rojek A, Kumar N, Frøkiaer J, Nielsen S, King LS, Agre P, Carbrey JM (2007) Aquaporin 9 is the major pathway for glycerol uptake by mouse erythrocytes, with implications for malarial virulence. Proc Natl Acad Sci U S A 104:12560–12564PubMedCrossRefGoogle Scholar
- Londos C, Brasaemle DL, Schultz CJ, Adler-Wailes DC, Levin DM, Kimmel AR, Rondinone CM (1999) On the control of lipolysis in adipocytes. Ann N Y Acad Sci 892:155–168PubMedCrossRefGoogle Scholar
- Maeda K, Okubo K, Shimomura I, Mizuno K, Matsuzawa Y, Matsubara K (1997) Analysis of an expression profile of genes in the human adipose tissue. Gene 190:227–235PubMedCrossRefGoogle Scholar
- Maeda N, Funahashi T, Hibuse T, Nagasawa A, Kishida K, Kuriyama H, Nakamura T, Kihara S, Shimomura I, Matsuzawa Y (2004) Adaptation to fasting by glycerol transport through aquaporin 7 in adipose tissue. Proc Natl Acad Sci U S A 101:17801–17806PubMedCrossRefGoogle Scholar
- Mead JR, Irvine SA, Ramji DP (2002) Lipoprotein lipase: structure, function, regulation, and role in disease. J Mol Med 80:753–769PubMedCrossRefGoogle Scholar
- Motojima K, Passilly P, Peters JM, Gonzalez FJ, Latruffe N (1998) Expression of putative fatty acid transporter genes are regulated by peroxisome proliferator-activated receptor alpha and gamma activators in a tissue- and inducer-specific manner. J Biol Chem 273:16710–16714PubMedCrossRefGoogle Scholar
- Murata K, Mitsuoka K, Hirai T, Walz T, Agre P, Heymann JB, Engel A, Fujiyoshi Y (2000) Structural determinants of water permeation through aquaporin-1. Nature 407:599–605PubMedCrossRefGoogle Scholar
- Nakamura T, Tokunaga K, Shimomura I, Nishida M, Yoshida S, Kotani K, Islam AH, Keno Y, Kobatake T, Nagai Y et al. (1994) Contribution of visceral fat accumulation to the development of coronary artery disease in non-obese men. Atherosclerosis 107:239–246PubMedCrossRefGoogle Scholar
- Nicchia GP, Frigeri A, Nico B, Ribatti D, Svelto M (2001) Tissue distribution and membrane localization of aquaporin-9 water channel: evidence for sex-linked differences in liver. J Histochem Cytochem 49:1547–1556PubMedGoogle Scholar
- Nielsen S, Chou CL, Marples D, Christensen EI, Kishore BK, Knepper MA (1995) Vasopressin increases water permeability of kidney collecting duct by inducing translocation of aquaporin-CD water channels to plasma membrane. Proc Natl Acad Sci U S A 92:1013–1017PubMedCrossRefGoogle Scholar
- Prudente S, Flex E, Morini E, Turchi F, Capponi D, De Cosmo S, Tassi V, Guida V, Avogaro A, Folli F, Maiani F, Frittitta L, Dallapiccola B, Trischitta V (2007) A functional variant of the adipocyte glycerol channel aquaporin 7 gene is associated with obesity and related metabolic abnormalities. Diabetes 56:1468–1474PubMedCrossRefGoogle Scholar
- Ramsay TG (1996) Fat cells. Endocrinol Metab Clin North Am 25:847–870PubMedCrossRefGoogle Scholar
- Rojek AM, Skowronski MT, Füchtbauer EM, Füchtbauer AC, Fenton RA, Agre P, Frøkiaer J, Nielsen S (2007) Defective glycerol metabolism in aquaporin 9 (AQP9) knockout mice. Proc Natl Acad Sci U S A 104:3609–3614PubMedCrossRefGoogle Scholar
- Saito K, Kageyama Y, Okada Y, Kawakami S, Kihara K, Ishibashi K, Sasaki S (2004) Localization of aquaporin-7 in human testis and ejaculated sperm: possible involvement in maintenance of sperm quality. J Urol 172:2073–2076PubMedCrossRefGoogle Scholar
- Schaffer JE, Lodish HF (1994) Expression cloning and characterization of a novel adipocyte long chain fatty acid transport protein. Cell 79:427–436PubMedCrossRefGoogle Scholar
- Shepherd PR, Kahn BB (1999) Glucose transporters and insulin action-implications for insulin resistance and diabetes mellitus. N Engl J Med 341:248–257PubMedCrossRefGoogle Scholar
- Sohara E, Rai T, Miyazaki JI, Verkman AS, Sasaki S, Uchida S (2005) Defective water and glycerol transport in the proximal tubules of AQP7 knockout mice. Am J Physiol Renal Physiol 289:F1195–F1200PubMedCrossRefGoogle Scholar
- Spiegelman BM, Flier JS (2001) Obesity and the regulation of energy balance. Cell. 104:531–543PubMedCrossRefGoogle Scholar
- Stremmel W, Strohmeyer G, Borchard F, Kochwa S, Berk PD (1985) Isolation and partial characterization of a fatty acid binding protein in rat liver plasma membranes. Proc Natl Acad Sci U S A 82:4–8PubMedCrossRefGoogle Scholar
- Tsukaguchi H, Shayakul C, Berger UV, Mackenzie B, Devidas S, Guggino WB, van Hoek AN, Hediger MA (1998) Molecular characterization of a broad selectivity neutral solute channel. J Biol Chem 273:24737–24743PubMedCrossRefGoogle Scholar
- Wakayama Y, Jimi T, Inoue M, Kojima H, Murahashi M, Kumagai T, Yamashita S, Hara H, Shibuya S (2002) Reduced aquaporin 4 expression in the muscle plasma membrane of patients with Duchenne muscular dystrophy. Arch Neurol 59:431–437PubMedCrossRefGoogle Scholar
- Wakayama Y, Inoue M, Kojima H, Jimi T, Shibuya S, Hara H, Oniki H (2004) Expression and localization of aquaporin 7 in normal skeletal myofiber. Cell Tissue Res 316:123–129PubMedCrossRefGoogle Scholar
- Yamashita S, Nakamura T, Shimomura I, Nishida M, Yoshida S, Kotani K, Kameda-Takemuara K, Tokunaga K, Matsuzawa Y (1996) Insulin resistance and body fat distribution. Diabetes Care 19:287–291PubMedCrossRefGoogle Scholar
- Yeh JI, Charrier V, Paulo J, Hou L, Darbon E, Claiborne A, Hol WG, Deutscher J (2004) Structures of enterococcal glycerol kinase in the absence and presence of glycerol: correlation of conformation to substrate binding and a mechanism of activation by phosphorylation. Biochemistry 43:362–373PubMedCrossRefGoogle Scholar
- Zimmet P, Alberti KG, Shaw J (2001) Global and societal implications of the diabetes epidemic. Nature 414:782–787PubMedCrossRefGoogle Scholar