Mammalian aquaglyceroporin function in metabolism

Biochimica et Biophysica Acta - Biomembranes

Volumn 1858, Issue 1, 2016, Pages 1-11

  Laforenza, Umberto ^a   Bottino, Cinzia ^a   Gastaldi, Giulia ^a  

^a UNIVERSITY OF PAVIA   (Italy)

Author keywords

Adipose tissue; Glycerol facilitators; Metabolic syndrome; Obesity; Plasma glycerol concentration

Indexed keywords

AQUAGLYCEROPORIN; AQUAGLYCEROPORIN 10; AQUAGLYCEROPORIN 3; AQUAGLYCEROPORIN 7; AQUAGLYCEROPORIN 9; AQUAPORIN; AQUAPORIN 1; AQUAPORIN 10; AQUAPORIN 11; AQUAPORIN 2; AQUAPORIN 3; AQUAPORIN 4; AQUAPORIN 6; AQUAPORIN 7; AQUAPORIN 8; HEPATOCYTE NUCLEAR FACTOR 3BETA; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; GLYCEROL; WATER;

ADIPOSE TISSUE; CAPILLARY ENDOTHELIUM; CELL MEMBRANE; HEART; HUMAN; INSULIN RELEASE; KIDNEY; LIPOLYSIS; LIVER; LIVER CELL; MICROVASCULATURE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PANCREAS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN SYNTHESIS; PROTEIN TARGETING; PROTEIN TRANSPORT; REGULATORY MECHANISM; REVIEW; SKELETAL MUSCLE; SMALL INTESTINE; ACTIVE TRANSPORT; ANIMAL; ANTIBODY SPECIFICITY; CARDIAC MUSCLE; METABOLISM; PATHOLOGY;

ADIPOSE TISSUE; ANIMALS; AQUAGLYCEROPORINS; BIOLOGICAL TRANSPORT, ACTIVE; DIABETES MELLITUS, TYPE 2; GLYCEROL; HUMANS; INTESTINE, SMALL; KIDNEY; LIVER; MICROVESSELS; MUSCLE, SKELETAL; MYOCARDIUM; OBESITY; ORGAN SPECIFICITY; PANCREAS; WATER;

EID: 84945156171     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2015.10.004     Document Type: Review

References (166)

1. E.C. Lin Glycerol utilization and its regulation in mammals Annu. Rev. Biochem. 46 1977 765 795
2. A. Rodríguez, V. Catalán, J. Gómez-Ambrosi, and G. Frühbeck Aquaglyceroporins serve as metabolic gateways in adiposity and insulin resistance control Cell Cycle 10 2011 1548 1556
3. R.W. Hanson, and L. Reshef Glyceroneogenesis revisited Biochimie 85 2003 1199 1205
4. L. Reshef, Y. Olswang, H. Cassuto, B. Blum, C.M. Croniger, S.C. Kalhan, S.M. Tilghman, and R.W. Hanson Glyceroneogenesis and the triglyceride/fatty acid cycle J. Biol. Chem. 278 2003 30413 30416
5. G. Frühbeck Obesity: aquaporin enters the picture Nature 438 2005 436 437
6. E. Sohara, T. Rai, S. Sasaki, and S. Uchida Physiological roles of AQP7 in the kidney: lessons from AQP7 knockout mice Biochim. Biophys. Acta 1758 2006 1106 1110
7. W.M. Bortz, P. Paul, A.C. Haff, and W.L. Holmes Glycerol turnover and oxidation in man J. Clin. Invest. 51 1972 1537 1546
8. H. Baba, X.J. Zhang, and R.R. Wolfe Glycerol gluconeogenesis in fasting humans Nutr. 11 1995 149 153
9. L. Rui Energy metabolism in the liver Comp. Physiol. 4 2014 177 197
10. V.E. Chaves, D. Frasson, and N.H. Kawashita Several agents and pathways regulate lipolysis in adipocytes Biochimie 93 2011 1631 1640
11. L.S. King, D. Kozono, and P. Agre From structure to disease: the evolving tale of aquaporin biology Nat. Rev. Mol. Cell Biol. 5 2004 687 698
12. K. Ishibashi, S. Kondo, S. Hara, and Y. Morishita The evolutionary aspects of aquaporin family Am. J. Physiol. Regul. Integr. Comp. Physiol. 300 2011 R566 R576
13. A.S. Verkman Aquaporins at a glance J. Cell Sci. 124 2011 2107 2112
14. G. Benga Foreword to the special issue on water channel proteins (aquaporins and relatives) in health and disease: 25 years after the discovery of the first water channel protein, later called aquaporin 1 Mol. Asp. Med. 33 2012 511 513
15. A. Rojek, J. Praetorius, J. Frøkiaer, S. Nielsen, and R. Fenton A current view of the mammalian aquaglyceroporins Annu. Rev. Physiol. 70 2008 301 327
16. G. Benga On the definition, nomenclature and classification of water channel proteins (aquaporins and relatives) Mol. Asp. Med. 33 2012 514 517
17. G. Benga, O. Popescu, V.I. Pop, and R.P. Holmes p-(chloromercuri)benzenesulfonate binding by membrane proteins and the inhibition of water transport in human erythrocytes Biochem. 25 1986 1535 1538
18. R. Zhang, A.N. van Hoek, J. Biwersi, and A.S. Verkman A point mutation at cysteine 189 blocks the water permeability of rat kidney water channel CHIP28k Biochem. 32 1993 2938 2941
19. G.M. Preston, J.S. Jung, W.B. Guggino, and P. Agre The mercury-sensitive residue at cysteine 189 in the CHIP28 water channel J. Biol. Chem. 268 1993 17 20
20. C.M. Niemietz, and S.D. Tyerman New potent inhibitors of aquaporins: silver and gold compounds inhibit aquaporins of plant and human origin FEBS Lett. 531 2002 443 447
21. J.S. Hub, and B.L. de Groot Mechanism of selectivity in aquaporins and aquaglyceroporins Proc. Natl. Acad. Sci. U. S. A. 105 2008 1198 1203
22. D. Fu, A. Libson, L.J. Miercke, C. Weitzman, P. Nollert, J. Krucinski, and R.M. Stroud Structure of a glycerol-conducting channel and the basis for its selectivity Sci. 290 2000 481 486
23. H. Sui, B.G. Han, J.K. Lee, P. Walian, and B.K. Jap Structural basis of water-specific transport through the AQP1 water channel Nature 414 2001 872 878
24. A. Almasalmeh, D. Krenc, B. Wu, and E. Beitz Structural determinants of the hydrogen peroxide permeability of aquaporins FEBS J. 281 2014 647 656
25. E. Beitz, B. Wu, L.M. Holm, J.E. Schultz, and T. Zeuthen Point mutations in the aromatic/arginine region in aquaporin 1 allow passage of urea, glycerol, ammonia, and protons Proc. Natl. Acad. Sci. U. S. A. 103 2006 269 274
26. D. Kozono, M. Yasui, L.S. King, and P. Agre Aquaporin water channels: atomic structure molecular dynamics meet clinical medicine J. Clin. Invest. 109 2002 1395 1399
27. R.R. Geyer, R. Musa-Aziz, X. Qin, and W.F. Boron Relative CO(2)/NH(3) selectivities of mammalian aquaporins 0-9 Am. J. Physiol. Cell Physiol. 304 2013 C985 C994
28. G. Tsiavaliaris, F. Itel, K. Hedfalk, S. Al-Samir, W. Meier, G. Gros, and V. Endeward Low CO2 permeability of cholesterol-containing liposomes detected by stopped-flow fluorescence spectroscopy FASEB J. 29 2015 1780 1793
29. B.L. de Groot, and J.S. Hub A decade of debate: significance of CO2 permeation through membrane channels still controversial ChemPhysChem 12 2011 1021 1022
30. L.R. Soria, J. Marrone, G. Calamita, and R.A. Marinelli Ammonia detoxification via ureagenesis in rat hepatocytes involves mitochondrial aquaporin-8 channels Hepatology 57 2013 2061 2071
31. T. Finkel Signal transduction by reactive oxygen species J. Cell Biol. 194 2011 7 15
32. Z. Liu, J. Shen, J.M. Carbrey, R. Mukhopadhyay, P. Agre, and B.P. Rosen Arsenite transport by mammalian aquaglyceroporins AQP7 and AQP9 Proc. Natl. Acad. Sci. U. S. A. 99 2002 6053 6058
33. Z. Liu, J.M. Carbrey, P. Agre, and B.P. Rosen Arsenic trioxide uptake by human and rat aquaglyceroporins Biochem. Biophys. Res. Commun. 316 2004 1178 1185
34. R. Mukhopadhyay, H. Bhattacharjee, and B.P. Rosen Aquaglyceroporins: generalized metalloid channels Biochim. Biophys. Acta 1840 2014 1583 1591
35. J.M. Carbrey, L. Song, Y. Zhou, M. Yoshinaga, A. Rojek, Y. Wang, Y. Liu, H.L. Lujan, S.E. DiCarlo, S. Nielsen, B.P. Rosen, P. Agre, and R. Mukhopadhyay Reduced arsenic clearance and increased toxicity in aquaglyceroporin-9-null mice Proc. Natl. Acad. Sci. U. S. A. 106 2009 15956 15960
36. H. Tsukaguchi, S. Weremowicz, C.C. Morton, and M.A. Hediger Functional and molecular characterization of the human neutral solute channel aquaporin-9 Am. J. Physiol. 277 1999 F685 F696
37. G.Q. Chen, J. Zhu, X.G. Shi, J.H. Ni, H.J. Zhong, G.Y. Si, X.L. Jin, W. Tang, X.S. Li, S.M. Xong, Z.X. Shen, G.L. Sun, J. Ma, P. Zhang, T.D. Zhang, C. Gazin, T. Naoe, S.J. Chen, Z.Y. Wang, and Z. Chen In vitro studies on cellular and molecular mechanisms of arsenic trioxide (As2O3) in the treatment of acute promyelocytic leukemia: As2O3 induces NB4 cell apoptosis with downregulation of Bcl-2 expression and modulation of PML-RAR alpha/PML proteins Blood 88 1996 1052 1061
38. K.H. Antman, Introduction: the history of arsenic trioxide in cancer therapy, Oncologist 6 Suppl. 2 (2001) 1-2.
39. K. Liu, D. Kozono, Y. Kato, P. Agre, A. Hazama, and M. Yasui Conversion of aquaporin 6 from an anion channel to a water-selective channel by a single amino acid substitution Proc. Natl. Acad. Sci. U. S. A. 102 2005 2192 2197
40. M. Yasui, A. Hazama, T.H. Kwon, S. Nielsen, W.B. Guggino, and P. Agre Rapid gating and anion permeability of an intracellular aquaporin Nature 402 1999 184 187
41. M. Herrera, and J.L. Garvin Aquaporins as gas channels Pflugers Arch. 462 2011 623 630
42. K. Ishibashi, K. Yamauchi, Y. Kageyama, F. Saito-Ohara, T. Ikeuchi, F. Marumo, and S. Sasaki Molecular characterization of human aquaporin-7 gene and its chromosomal mapping Biochim. Biophys. Acta 1399 1998 62 66
43. H. Kuriyama, S. Kawamoto, N. Ishida, I. Ohno, S. Mita, Y. Matsuzawa, K. Matsubara, and K. Okubo Molecular cloning and expression of a novel human aquaporin from adipose tissue with glycerol permeability Biochem. Biophys. Res. Commun. 241 1997 53 58
44. A. Rodríguez, V. Catalán, J. Gómez-Ambrosi, S. García-Navarro, F. Rotellar, V. Valentí, C. Silva, M.J. Gil, J. Salvador, M.A. Burrell, G. Calamita, M.M. Malagón, and G. Frühbeck Insulin- and leptin-mediated control of aquaglyceroporins in human adipocytes and hepatocytes is mediated via the PI3K/Akt/mTOR signaling cascade J. Clin. Endocrinol. Metab. 96 2011 E586 E597
45. U. Laforenza, M.F. Scaffino, and G. Gastaldi Aquaporin-10 represents an alternative pathway for glycerol efflux from human adipocytes PLoS One 8 2013 e54474
46. A. Madeira, S. Fernández-Veledo, M. Camps, A. Zorzano, T.F. Moura, V. Ceperuelo-Mallafré, J. Vendrell, and G. Soveral Human aquaporin-11 is a water and glycerol channel and localizes in the vicinity of lipid droplets in human adipocytes Obesity (Silver Spring) 2014
47. T. Morinaga, M. Nakakoshi, A. Hirao, M. Imai, and K. Ishibashi Mouse aquaporin 10 gene (AQP10) is a pseudogene Biochem. Biophys. Res. Commun. 294 2002 630 634
48. Y. Tanaka, Y. Morishita, and K. Ishibashi Aquaporin10 is a pseudogene in cattle and their relatives Biochem. Biophys. Rep. 2015 16 21
49. K. Kishida, H. Kuriyama, T. Funahashi, I. Shimomura, S. Kihara, N. Ouchi, M. Nishida, H. Nishizawa, M. Matsuda, M. Takahashi, K. Hotta, T. Nakamura, S. Yamashita, Y. Tochino, and Y. Matsuzawa Aquaporin adipose, a putative glycerol channel in adipocytes J. Biol. Chem. 275 2000 20896 20902
50. K. Kishida, 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 Genomic structure and insulin-mediated repression of the aquaporin adipose (AQPap), adipose-specific glycerol channel J. Biol. Chem. 276 2001 36251 36260
51. M. Miranda, X. Escoté, V. Ceperuelo-Mallafré, M.J. Alcaide, I. Simón, N. Vilarrasa, M. Wabitsch, and J. Vendrell Paired subcutaneous and visceral adipose tissue aquaporin-7 expression in human obesity and type 2 diabetes: differences and similarities between depots J. Clin. Endocrinol. Metab. 95 2010 3470 3479
52. M. Skowronski, J. Lebeck, A. Rojek, J. Praetorius, E. Füchtbauer, J. Frøkiaer, and S. Nielsen AQP7 is localized in capillaries of adipose tissue, cardiac and striated muscle: implications in glycerol metabolism Am. J. Physiol. Renal. Physiol. 292 2007 F956 F965
53. J. Lebeck, T. Stergård, A. Rojek, E.M. Füchtbauer, S. Lund, S. Nielsen, and J. Praetorius Gender-specific effect of physical training on AQP7 protein expression in human adipose tissue Acta Diabetol. 49 Suppl. 1 2012 S215 S226
54. T. Miyauchi, H. Yamamoto, Y. Abe, G.J. Yoshida, A. Rojek, E. Sohara, S. Uchida, S. Nielsen, and M. Yasui Dynamic subcellular localization of aquaporin-7 in white adipocytes FEBS Lett. 589 2015 608 614
55. N. Maeda, T. Funahashi, T. Hibuse, A. Nagasawa, K. Kishida, H. Kuriyama, T. Nakamura, S. Kihara, I. Shimomura, and Y. Matsuzawa Adaptation to fasting by glycerol transport through aquaporin 7 in adipose tissue Proc. Natl. Acad. Sci. U. S. A. 101 2004 17801 17806
56. H. Kuriyama, I. Shimomura, K. Kishida, H. Kondo, N. Furuyama, H. Nishizawa, N. Maeda, M. Matsuda, H. Nagaretani, S. Kihara, T. Nakamura, Y. Tochino, T. Funahashi, and Y. Matsuzawa Coordinated regulation of fat-specific and liver-specific glycerol channels, aquaporin adipose and aquaporin 9 Diabetes 51 2002 2915 2921
57. D.H. Lee, D.B. Park, Y.K. Lee, C.S. An, Y.S. Oh, J.S. Kang, S.H. Kang, and M.Y. Chung The effects of thiazolidinedione treatment on the regulations of aquaglyceroporins and glycerol kinase in OLETF rats Metabolism 54 2005 1282 1289
58. M. Fasshauer, J. Klein, U. Lossner, M. Klier, S. Kralisch, and R. Paschke Suppression of aquaporin adipose gene expression by isoproterenol, TNFalpha, and dexamethasone Horm. Metab. Res. 35 2003 222 227
59. A. Rodríguez, J. Gómez-Ambrosi, V. Catalán, M.J. Gil, S. Becerril, N. Sáinz, C. Silva, J. Salvador, I. Colina, and G. Frühbeck Acylated and desacyl ghrelin stimulate lipid accumulation in human visceral adipocytes Int. J. Obes. 33 2009 541 552
60. M. Hara-Chikuma, E. Sohara, T. Rai, M. Ikawa, M. Okabe, S. Sasaki, S. Uchida, and A. Verkman Progressive adipocyte hypertrophy in aquaporin-7-deficient mice: adipocyte glycerol permeability as a novel regulator of fat accumulation J. Biol. Chem. 280 2005 15493 15496
61. T. Hibuse, 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 Aquaporin 7 deficiency is associated with development of obesity through activation of adipose glycerol kinase Proc. Natl. Acad. Sci. U. S. A. 102 2005 10993 10998
62. K. Matsumura, B. Chang, M. Fujimiya, W. Chen, R. Kulkarni, Y. Eguchi, H. Kimura, H. Kojima, and L. Chan Aquaporin 7 is a beta-cell protein and regulator of intraislet glycerol content and glycerol kinase activity, beta-cell mass, and insulin production and secretion Mol. Cell. Biol. 27 2007 6026 6037
63. H. Kondo, 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 Human aquaporin adipose (AQPap) gene. Genomic structure, promoter analysis and functional mutation Eur. J. Biochem. 269 2002 1814 1826
64. V. Ceperuelo-Mallafré, M. Miranda, M. Chacón, N. Vilarrasa, A. Megia, C. Gutiérrez, J. Fernández-Real, J. Gómez, E. Caubet, G. Frühbeck, and J. Vendrell 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 2007 3640 3645
65. C. Goubau, J. Jaeken, E.N. Levtchenko, C. Thys, M. Di Michele, G.A. Martens, E. Gerlo, R. De Vos, G.M. Buyse, N. Goemans, C. Van Geet, and K. Freson Homozygosity for aquaporin 7 G264V in three unrelated children with hyperglyceroluria and a mild platelet secretion defect Genet. Med. 15 2013 55 63
66. M. Marrades, F. Milagro, J. Martínez, and M. Moreno-Aliaga Differential expression of aquaporin 7 in adipose tissue of lean and obese high fat consumers Biochem. Biophys. Res. Commun. 339 2006 785 789
67. S. Prudente, 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 A functional variant of the adipocyte glycerol channel aquaporin 7 gene is associated with obesity and related metabolic abnormalities Diabetes 56 2007 1468 1474
68. V. Catalán, J. Gómez-Ambrosi, C. Pastor, F. Rotellar, C. Silva, A. Rodríguez, M.J. Gil, J.A. Cienfuegos, J. Salvador, J. Vendrell, and G. Frühbeck Influence of morbid obesity and insulin resistance on gene expression levels of AQP7 in visceral adipose tissue and AQP9 in liver Obes. Surg. 18 2008 695 701
69. M. Miranda, V. Ceperuelo-Mallafré, A. Lecube, C. Hernandez, M.R. Chacon, J.M. Fort, L. Gallart, J.A. Baena-Fustegueras, R. Simó, and J. Vendrell Gene expression of paired abdominal adipose AQP7 and liver AQP9 in patients with morbid obesity: relationship with glucose abnormalities Metabolism 58 2009 1762 1768
70. S. Nielsen, Z. Guo, C.M. Johnson, D.D. Hensrud, and M.D. Jensen Splanchnic lipolysis in human obesity J. Clin. Invest. 113 2004 1582 1588
71. M.D. Jensen, M.G. Sarr, D.A. Dumesic, P.A. Southorn, and J.A. Levine Regional uptake of meal fatty acids in humans Am. J. Physiol. Endocrinol. Metab. 285 2003 E1282 E1288
72. R. Nørregaard, B. Jensen, C. Li, W. Wang, M. Knepper, S. Nielsen, and J. Frøkiaer COX-2 inhibition prevents downregulation of key renal water and sodium transport proteins in response to bilateral ureteral obstruction Am. J. Physiol. Renal. Physiol. 289 2005 F322 F333
73. S.B. Votruba, R.S. Mattison, D.A. Dumesic, C. Koutsari, and M.D. Jensen Meal fatty acid uptake in visceral fat in women Diabetes 56 2007 2589 2597
74. S.E. Taksali, S. Caprio, J. Dziura, S. Dufour, A.M. Calí, T.R. Goodman, X. Papademetris, T.S. Burgert, B.M. Pierpont, M. Savoye, M. Shaw, A.A. Seyal, and R. Weiss High visceral and low abdominal subcutaneous fat stores in the obese adolescent: a determinant of an adverse metabolic phenotype Diabetes 57 2008 367 371
75. P. Portincasa, and G. Calamita Water channel proteins in bile formation and flow in health and disease: when immiscible becomes miscible Mol. Asp. Med. 33 2012 651 664
76. A.M. Lakner, T.L. Walling, I.H. McKillop, and L.W. Schrum Altered aquaporin expression and role in apoptosis during hepatic stellate cell activation Liver Int. 31 2011 42 51
77. T. Matsuzaki, Y. Tajika, A. Ablimit, T. Aoki, H. Hagiwara, and K. Takata Aquaporins in the digestive system Med. Electron Microsc. 37 2004 71 80
78. K. Ishibashi, S. Sasaki, F. Saito, T. Ikeuchi, and F. Marumo Structure and chromosomal localization of a human water channel (AQP3) gene Genomics 27 1995 352 354
79. L.M. Holm, T.P. Jahn, A.L. Møller, J.K. Schjoerring, D. Ferri, D.A. Klaerke, and T. Zeuthen NH3 and NH4 + permeability in aquaporin-expressing xenopus oocytes Pflugers Arch. 450 2005 415 428
80. A.M. Rojek, M.T. Skowronski, E.M. Füchtbauer, A.C. Füchtbauer, R.A. Fenton, P. Agre, J. Frøkiaer, and S. Nielsen Defective glycerol metabolism in aquaporin 9 (AQP9) knockout mice Proc. Natl. Acad. Sci. U. S. A. 104 2007 3609 3614
81. G. Calamita, P. Gena, D. Ferri, A. Rosito, A. Rojek, S. Nielsen, R.A. Marinelli, G. Frühbeck, and M. Svelto Biophysical assessment of aquaporin-9 as principal facilitative pathway in mouse liver import of glucogenetic glycerol Biol. Cell. 104 2012 342 351
82. S. Jelen, P. Gena, J. Lebeck, A. Rojek, J. Praetorius, J. Frøkiaer, R.A. Fenton, S. Nielsen, G. Calamita, and M. Rützler Aquaporin-9 and urea transporter-a gene deletions affect urea transmembrane passage in murine hepatocytes Am. J. Physiol. Gastrointest. Liver Physiol. 303 2012 G1279 G1287
83. J.M. Carbrey, D.A. Gorelick-Feldman, D. Kozono, J. Praetorius, S. Nielsen, and P. Agre Aquaglyceroporin AQP9: solute permeation and metabolic control of expression in liver Proc. Natl. Acad. Sci. U. S. A. 100 2003 2945 2950
84. J. Lebeck, P. Gena, H. O'Neill, M.T. Skowronski, S. Lund, G. Calamita, and J. Praetorius Estrogen prevents increased hepatic aquaporin-9 expression and glycerol uptake during starvation Am. J. Physiol. Gastrointest. Liver. Physiol. 302 2012 G365 G374
85. I. Goldstein, K. Yizhak, S. Madar, N. Goldfinger, E. Ruppin, and V. Rotter p53 promotes the expression of gluconeogenesis-related genes and enhances hepatic glucose production Cancer. Metab. 1 2013 9
86. Y. Yokoyama, K. Iguchi, S. Usui, and K. Hirano AMP-activated protein kinase modulates the gene expression of aquaporin 9 via forkhead box a2 Arch. Biochem. Biophys. 515 2011 80 88
87. C. Wolfrum, E. Asilmaz, E. Luca, J.M. Friedman, and M. Stoffel Foxa2 regulates lipid metabolism and ketogenesis in the liver during fasting and in diabetes Nature 432 2004 1027 1032
88. D. Patsouris, M. Müller, and S. Kersten Peroxisome proliferator activated receptor ligands for the treatment of insulin resistance Curr. Opin. Investig. Drugs 5 2004 1045 1050
89. S. Kersten, J. Seydoux, J.M. Peters, F.J. Gonzalez, B. Desvergne, and W. Wahli Peroxisome proliferator-activated receptor alpha mediates the adaptive response to fasting J. Clin. Invest. 103 1999 1489 1498
90. C. Wang, Z.L. Lv, Y.J. Kang, T.X. Xiang, P.L. Wang, and Z. Jiang Aquaporin-9 downregulation prevents steatosis in oleic acid-induced non-alcoholic fatty liver disease cell models Int. J. Mol. Med. 32 2013 1159 1165
91. L.Y. Gu, L.W. Qiu, X.F. Chen, L. Lv, and Z.C. Mei Expression of aquaporin 3 and aquaporin 9 is regulated by oleic acid through the PI3K/Akt and p38 MAPK signaling pathways Zhonghua Gan Zang Bing Za Zhi 21 2013 753 758
92. A. Rodríguez, P. Gena, L. Méndez-Giménez, A. Rosito, V. Valentí, F. Rotellar, I. Sola, R. Moncada, C. Silva, M. Svelto, J. Salvador, G. Calamita, and G. Frühbeck Reduced hepatic aquaporin-9 and glycerol permeability are related to insulin resistance in non-alcoholic fatty liver disease Int. J. Obes. 38 2014 1213 1220
93. F.H. Mattson, and R.A. Volpenhein The digestion and absorption of triglycerides J. Biol. Chem. 239 1964 2772 2777
94. G.C. Buell, and R. Reiser Glyceride-glycerol precursors in the intestinal mucosa J. Biol. Chem. 234 1959 217 219
95. K. Ishibashi, S. Sasaki, K. Fushimi, S. Uchida, M. Kuwahara, H. Saito, T. Furukawa, K. Nakajima, Y. Yamaguchi, and T. Gojobori 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. U. S. A. 91 1994 6269 6273
96. U. Laforenza Water channel proteins in the gastrointestinal tract Mol. Asp. Med. 33 2012 642 650
97. K.Y. Ohta, K. Inoue, Y. Hayashi, and H. Yuasa Carrier-mediated transport of glycerol in the perfused rat small intestine Biol. Pharm. Bull. 29 2006 785 789
98. M. Ishii, K. Ohta, T. Katano, K. Urano, J. Watanabe, A. Miyamoto, K. Inoue, and H. Yuasa Dual functional characteristic of human aquaporin 10 for solute transport Cell. Physiol. Biochem. 27 2011 749 756
99. Y. Ohgusu, K.Y. Ohta, M. Ishii, T. Katano, K. Urano, J. Watanabe, K. Inoue, and H. Yuasa Functional characterization of human aquaporin 9 as a facilitative glycerol carrier Drug Metab. Pharmacokinet. 23 2008 279 284
100. N. Ikarashi, R. Kon, T. Iizasa, N. Suzuki, R. Hiruma, K. Suenaga, T. Toda, M. Ishii, M. Hoshino, W. Ochiai, and K. Sugiyama Inhibition of aquaporin-3 water channel in the colon induces diarrhea Biol. Pharm. Bull. 35 2012 957 962
101. U. Laforenza, E. Miceli, G. Gastaldi, M.F. Scaffino, U. Ventura, J.M. Fontana, M.N. Orsenigo, and G.R. Corazza Solute transporters and aquaporins are impaired in celiac disease Biol. Cell. 102 2010 457 467
102. J. Hardin, L. Wallace, J. Wong, E. O'Loughlin, S. Urbanski, D. Gall, W. MacNaughton, and P. Beck Aquaporin expression is downregulated in a murine model of colitis and in patients with ulcerative colitis, Crohn's disease and infectious colitis Cell Tissue Res. 318 2004 313 323
103. T. Ma, Y. Song, B. Yang, A. Gillespie, E.J. Carlson, C.J. Epstein, and A.S. Verkman Nephrogenic diabetes insipidus in mice lacking aquaporin-3 water channels Proc. Natl. Acad. Sci. U. S. A. 97 2000 4386 4391
104. M. Asai, S. Higuchi, M. Kubota, K. Iguchi, S. Usui, and K. Hirano Regulators for blood glucose level affect gene expression of aquaporin 3 Biol. Pharm. Bull. 29 2006 991 996
105. P. Kruhoffer, and O.I. Nissen Handling of glycerol in the kidney Acta Physiol. Scand. 59 1963 284 294
106. D. Gaudet, S. Arsenault, L. Pérusse, M.C. Vohl, J. St-Pierre, J. Bergeron, J.P. Després, K. Dewar, M.J. Daly, T. Hudson, and J.D. Rioux Glycerol as a correlate of impaired glucose tolerance: dissection of a complex system by use of a simple genetic trait Am. J. Hum. Genet. 66 2000 1558 1568
107. E.N. Bergman Glycerol turnover in the nonpregnant and ketotic pregnant sheep Am. J. Physiol. 215 1968 865 873
108. S. Laurell, and G. Tibbling The use of blood glycerol determination in the diagnosis of hyperthyroidism Clin. Chim. Acta 21 1968 127 132
109. R.E. Swanson, and R.B. Thompson Renal tubular handling of glycerol and ethylene glycol in the dog Am. J. Physiol. 217 1969 553 562
110. J.A. Larsen Elimination of glycerol as a measure of hepatic blood flow in the cat Acta Physiol. Scand. 1963 224 234
111. M. Stumvoll, G. Perriello, C. Meyer, and J. Gerich Role of glutamine in human carbohydrate metabolism in kidney and other tissues Kidney Int. 55 1999 778 792
112. K. Kida, S. Nakajo, F. Kamiya, Y. Toyama, T. Nishio, and H. Nakagawa Renal net glucose release in vivo and its contribution to blood glucose in rats J. Clin. Invest. 62 1978 721 726
113. S. Nielsen, J. Frøkiaer, D. Marples, T.H. Kwon, P. Agre, and M.A. Knepper Aquaporins in the kidney: from molecules to medicine Physiol. Rev. 82 2002 205 244
114. A.S. Verkman Dissecting the roles of aquaporins in renal pathophysiology using transgenic mice Semin. Nephrol. 28 2008 217 226
115. E. Sohara, T. Rai, J. Miyazaki, A.S. Verkman, S. Sasaki, and S. Uchida Defective water and glycerol transport in the proximal tubules of AQP7 knockout mice Am. J. Physiol. Renal. Physiol. 289 2005 F1195 F1200
116. H. Li, J. Kamiie, Y. Morishita, Y. Yoshida, E. Yaoita, K. Ishibashi, and T. Yamamoto Expression and localization of two isoforms of AQP10 in human small intestine Biol. Cell. 97 2005 823 829
117. T. Aizawa, M. Komatsu, N. Asanuma, Y. Sato, and G.W. Sharp Glucose action 'beyond ionic events' in the pancreatic beta cell Trends Pharmacol. Sci. 19 1998 496 499
118. C. Delporte Aquaporins in salivary glands and pancreas Biochim. Biophys. Acta 1840 2014 1524 1532
119. R.J. Noel, P.A. Antinozzi, J.D. McGarry, and C.B. Newgard 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 1997 18621 18627
120. R.H. Skelly, B. Wicksteed, P.A. Antinozzi, and C.J. Rhodes Glycerol-stimulated proinsulin biosynthesis in isolated pancreatic rat islets via adenoviral-induced expression of glycerol kinase is mediated via mitochondrial metabolism Diabetes 50 2001 1791 1798
121. K. Louchami, L. Best, P. Brown, M. Virreira, E. Hupkens, J. Perret, O. Devuyst, S. Uchida, C. Delporte, W.J. Malaisse, R. Beauwens, and A. Sener A new role for aquaporin 7 in insulin secretion Cell. Physiol. Biochem. 29 2012 65 74
122. L. Best, P.D. Brown, A. Sener, and W.J. Malaisse Electrical activity in pancreatic islet cells: the VRAC hypothesis Islets 2 2010 59 64
123. L. Best, P.D. Brown, A.P. Yates, J. Perret, M. Virreira, R. Beauwens, W.J. Malaisse, A. Sener, and C. Delporte Contrasting effects of glycerol and urea transport on rat pancreatic beta-cell function Cell. Physiol. Biochem. 23 2009 255 264
124. A. Rutkovskiy, G. Valen, and J. Vaage Cardiac aquaporins Basic Res. Cardiol. 108 2013 393
125. T.L. Butler, C.G. Au, B. Yang, J.R. Egan, Y.M. Tan, E.C. Hardeman, K.N. North, A.S. Verkman, and D.S. Winlaw Cardiac aquaporin expression in humans, rats, and mice Am. J. Physiol. Heart Circ. Physiol. 291 2006 H705 H713
126. T. Hibuse, N. Maeda, H. Nakatsuji, Y. Tochino, K. Fujita, S. Kihara, T. Funahashi, and I. Shimomura The heart requires glycerol as an energy substrate through aquaporin 7, a glycerol facilitator Cardiovasc. Res. 83 2009 34 41
127. A. Mobasheri, S. Wray, and D. Marples Distribution of AQP2 and AQP3 water channels in human tissue microarrays J. Mol. Histol. 36 2005 1 14
128. F. Thuny, J. Textoris, A.B. Amara, A.E. Filali, C. Capo, G. Habib, D. Raoult, and J.L. Mege The gene expression analysis of blood reveals S100A11 and AQP9 as potential biomarkers of infective endocarditis PLoS One 7 2012 e31490
129. L.N. Nejsum, M. Elkjaer, H. Hager, J. Frokiaer, T.H. Kwon, and S. Nielsen Localization of aquaporin-7 in rat and mouse kidney using RT-PCR, immunoblotting, and immunocytochemistry Biochem. Biophys. Res. Commun. 277 2000 164 170
130. F. Umenishi, A.S. Verkman, and M.A. Gropper Quantitative analysis of aquaporin mRNA expression in rat tissues by RNase protection assay DNA Cell Biol. 15 1996 475 480
131. Y. Wakayama, T. Jimi, M. Inoue, H. Kojima, S. Shibuya, M. Murahashi, H. Hara, and H. Oniki Expression of aquaporin 3 and its localization in normal skeletal myofibres Histochem. J. 34 2002 331 337
132. S. Shibuya, Y. Wakayama, M. Inoue, H. Kojima, and H. Oniki The relationship between intramembranous particles and aquaporin molecules in the plasma membranes of normal rat skeletal muscles: a fracture-label study J. Electron Microsc. 55 2006 63 68
133. Y. Wakayama, M. Inoue, H. Kojima, T. Jimi, S. Shibuya, H. Hara, and H. Oniki Expression and localization of aquaporin 7 in normal skeletal myofiber Cell Tissue Res. 316 2004 123 129
134. B. Yang, J.M. Verbavatz, Y. Song, L. Vetrivel, G. Manley, W.M. Kao, T. Ma, and A.S. Verkman Skeletal muscle function and water permeability in aquaporin-4 deficient mice Am. J. Physiol. Cell Physiol. 278 2000 C1108 C1115
135. X. Chen, Q.Q. Yu, Y.H. Zhu, Y. Bi, W.P. Sun, H. Liang, M.Y. Cai, X.Y. He, and J.P. Weng Insulin therapy stimulates lipid synthesis and improves endocrine functions of adipocytes in dietary obese C57BL/6 mice Acta Pharmacol. Sin. 31 2010 341 346
136. K. Kishida, I. Shimomura, H. Nishizawa, N. Maeda, H. Kuriyama, H. Kondo, M. Matsuda, H. Nagaretani, N. Ouchi, K. Hotta, S. Kihara, T. Kadowaki, T. Funahashi, and Y. Matsuzawa Enhancement of the aquaporin adipose gene expression by a peroxisome proliferator-activated receptor gamma J. Biol. Chem. 276 2001 48572 48579
137. M. Guo, F. Chen, T. Lin, Y. Peng, W. Li, X. Zhu, L. Lin, and Y. Chen Apelin-13 decreases lipid storage in hypertrophic adipocytes in vitro through the upregulation of AQP7 expression by the PI3K signaling pathway Med. Sci. Monit. 20 2014 1345 1352
138. S. Jelen, S. Wacker, C. Aponte-Santamaría, M. Skott, A. Rojek, U. Johanson, P. Kjellbom, S. Nielsen, B.L. de Groot, and M. Rützler Aquaporin-9 protein is the primary route of hepatocyte glycerol uptake for glycerol gluconeogenesis in mice J. Biol. Chem. 286 2011 44319 44325
139. M. Hara-Chikuma, and A.S. Verkman Roles of aquaporin-3 in the epidermis J. Invest. Dermatol. 128 2008 2145 2151
140. J.M. Jungersted, J. Bomholt, N. Bajraktari, J.S. Hansen, D.A. Klærke, P.A. Pedersen, K. Hedfalk, K.H. Nielsen, T. Agner, and C. Hélix-Nielsen In vivo studies of aquaporins 3 and 10 in human stratum corneum Arch. Dermatol. Res. 305 2013 699 704
141. C. Moon, R. Rousseau, J.C. Soria, M.O. Hoque, J. Lee, S.J. Jang, B. Trink, D. Sidransky, and L. Mao Aquaporin expression in human lymphocytes and dendritic cells Am. J. Hematol. 75 2004 128 133
142. M. Hara-Chikuma, S. Chikuma, Y. Sugiyama, K. Kabashima, A.S. Verkman, S. Inoue, and Y. Miyachi Chemokine-dependent T cell migration requires aquaporin-3-mediated hydrogen peroxide uptake J. Exp. Med. 209 2012 1743 1752
143. P.D. Kingsley, E. Greenfest-Allen, J.M. Frame, T.P. Bushnell, J. Malik, K.E. McGrath, C.J. Stoeckert, and J. Palis Ontogeny of erythroid gene expression Blood 121 2013 e5 e13
144. N. Roudier, J.M. Verbavatz, C. Maurel, P. Ripoche, and F. Tacnet Evidence for the presence of aquaporin-3 in human red blood cells J. Biol. Chem. 273 1998 8407 8412
145. D. Zhang, Y.J. Tan, F. Qu, J.Z. Sheng, and H.F. Huang Functions of water channels in male and female reproductive systems Mol. Asp. Med. 33 2012 676 690
146. K.L. Schey, Z. Wang, J.L. Wenke, and Y. Qi Aquaporins in the eye: expression, function, and roles in ocular disease Biochim. Biophys. Acta 1840 2014 1513 1523
147. Y.L. Liu, T. Matsuzaki, T. Nakazawa, S. Murata, N. Nakamura, T. Kondo, M. Iwashina, K. Mochizuki, T. Yamane, K. Takata, and R. Katoh Expression of aquaporin 3 (AQP3) in normal and neoplastic lung tissues Hum. Pathol. 38 2007 171 178
148. T. Matsuzaki, N. Machida, Y. Tajika, A. Ablimit, T. Suzuki, T. Aoki, H. Hagiwara, and K. Takata Expression and immunolocalization of water-channel aquaporins in the rat and mouse mammary gland Histochem. Cell Biol. 123 2005 501 512
149. A. Mobasheri, and R. Barrett-Jolley Aquaporin water channels in the mammary gland: from physiology to pathophysiology and neoplasia J. Mammary Gland Biol. Neoplasia 19 2014 91 102
150. A. Mobasheri, E. Trujillo, S. Bell, S.D. Carter, P.D. Clegg, P. Martín-Vasallo, and D. Marples Aquaporin water channels AQP1 and AQP3, are expressed in equine articular chondrocytes Vet. J. 168 2004 143 150
151. M. Takumida, H. Takumida, A. Kakigi, N. Egami, R. Nishioka, and M. Anniko Localization of aquaporins in the mouse vestibular end organs Acta Otolaryngol. 133 2013 804 813
152. F.M. Gu, H.L. Han, and L.S. Zhang Effects of vasopressin on gene expression in rat inner ear Hear. Res. 222 2006 70 78
153. A. Eckhard, C. Gleiser, H. Arnold, H. Rask-Andersen, H. Kumagami, M. Müller, B. Hirt, and H. Löwenheim Water channel proteins in the inner ear and their link to hearing impairment and deafness Mol. Asp. Med. 33 2012 612 637
154. H. Peng, Y. Zhang, L. Lei, Q. Chen, J. Yue, Y. Tan, and E. Duan Aquaporin 7 expression in postimplantation mouse uteri: a potential role for glycerol transport in uterine decidualization Fertil. Steril. 95 2011 1514 1517 e1511-1513.
155. T.L. Tran, T. Bek, L. Holm, M. la Cour, S. Nielsen, J.U. Prause, A. Rojek, S. Hamann, and S. Heegaard Aquaporins 6-12 in the human eye Acta Ophthalmol. (Copenh) 91 2013 557 563
156. S. Okada, T. Misaka, I. Matsumoto, H. Watanabe, and K. Abe Aquaporin-9 is expressed in a mucus-secreting goblet cell subset in the small intestine FEBS Lett. 540 2003 157 162
157. M.T. Skowronski, T.H. Kwon, and S. Nielsen Immunolocalization of aquaporin 1, 5, and 9 in the female pig reproductive system J. Histochem. Cytochem. 57 2009 61 67
158. R. Aharon, and Z. Bar-Shavit Involvement of aquaporin 9 in osteoclast differentiation J. Biol. Chem. 281 2006 19305 19309
159. Y. Liu, L. Song, Y. Wang, A. Rojek, S. Nielsen, P. Agre, and J.M. Carbrey Osteoclast differentiation and function in aquaglyceroporin AQP9-null mice Biol. Cell. 101 2009 133 140
160. G. Bu, F. Shuang, Y. Wu, D. Ren, and S. Hou AQP9: a novel target for bone loss induced by microgravity Biochem. Biophys. Res. Commun. 419 2012 774 778
161. Y. Liu, D. Promeneur, A. Rojek, N. Kumar, J. Frøkiaer, S. Nielsen, L.S. King, P. Agre, and J.M. Carbrey 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 2007 12560 12564
162. K. Ishibashi, M. Kuwahara, Y. Gu, Y. Tanaka, F. Marumo, and S. Sasaki 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 1998 268 274
163. V.M. Loitto, T. Forslund, T. Sundqvist, K.E. Magnusson, and M. Gustafsson Neutrophil leukocyte motility requires directed water influx J. Leukoc. Biol. 71 2002 212 222
164. T. Karlsson, M. Glogauer, R.P. Ellen, V.M. Loitto, K.E. Magnusson, and M.A. Magalhães Aquaporin 9 phosphorylation mediates membrane localization and neutrophil polarization J. Leukoc. Biol. 90 2011 963 973
165. J. Badaut, A.M. Fukuda, A. Jullienne, and K.G. Petry Aquaporin and brain diseases Biochim. Biophys. Acta 1840 2014 1554 1565
166. L. Hermo, D. Krzeczunowicz, and R. Ruz Cell specificity of aquaporins 0, 3, and 10 expressed in the testis, efferent ducts, and epididymis of adult rats J. Androl. 25 2004 494 505