Reduced hepatic aquaporin-9 and glycerol permeability are related to insulin resistance in non-alcoholic fatty liver disease

International Journal of Obesity

Volumn 38, Issue 9, 2014, Pages 1213-1220

  Rodriguez A ^a,b   Gena, P ^c   Mendez Gimenez L ^a   Rosito, A ^c   Valenti V ^a,b   Rotellar, F ^a,b   Sola, I ^a   Moncada, R ^a   Silva, C ^a   Svelto, M ^c,d   Salvador, J ^a   Calamita, G ^c,d   Fruhbeck G ^a,b  

^a UNIVERSITY CLINIC OF NAVARRA   (Spain)

^b Instituto de Salud Carlos III   (Spain)

^c UNIVERSITY OF BARI   (Italy)

^d Centro di Eccellenza di Genomica in campo Biomedico ed Agrario (CEGBA)   (Italy)

Author keywords

aquaporins; non alcoholic fatty liver disease; type 2 diabetes

Indexed keywords

AQUAGLYCEROPORIN; AQUAPORIN; AQUAPORIN 10; AQUAPORIN 3; AQUAPORIN 7; AQUAPORIN 9; C REACTIVE PROTEIN; GLYCEROL; INSULIN; UNCLASSIFIED DRUG; AQP9 PROTEIN, HUMAN; TRIACYLGLYCEROL;

ADULT; ARTICLE; BARIATRIC SURGERY; BASOLATERAL MEMBRANE; BODY MASS; CONTROLLED STUDY; ECHOGRAPHY; FATTY LIVER; FEMALE; GLUCOSE BLOOD LEVEL; GLYCEROL BLOOD LEVEL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMPAIRED GLUCOSE TOLERANCE; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIVER; LIVER BIOPSY; LIVER CELL; MAJOR CLINICAL STUDY; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONALCOHOLIC FATTY LIVER; OBESITY; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING; CROSS-SECTIONAL STUDY; DOWN REGULATION; GLUCOSE INTOLERANCE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PERMEABILITY;

ADULT; AQUAPORINS; BLOTTING, WESTERN; C-REACTIVE PROTEIN; CROSS-SECTIONAL STUDIES; DOWN-REGULATION; FATTY LIVER; FEMALE; GLUCOSE INTOLERANCE; GLYCEROL; HUMANS; INSULIN RESISTANCE; LIVER; MALE; NON-ALCOHOLIC FATTY LIVER DISEASE; PERMEABILITY; REAL-TIME POLYMERASE CHAIN REACTION; TRIGLYCERIDES;

EID: 84922158768     PISSN: 03070565     EISSN: 14765497     Source Type: Journal    
DOI: 10.1038/ijo.2013.234     Document Type: Article

References (44)

1. Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K et al. The diagnosis and management of non-alcoholic fatty liver disease: practice Guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology 2012; 55: 2005-2023.
2. Utzschneider KM, Kahn SE. Review: the role of insulin resistance in nonalcoholic fatty liver disease. J Clin Endocrinol Metab 2006; 91: 4753-4761.
3. Roden M. Mechanisms of disease: hepatic steatosis in type 2 diabetes-pathogenesis and clinical relevance. Nat Clin Pract Endocrinol Metab 2006; 2: 335-348.
4. Machado M, Marques-Vidal P, Cortez-Pinto H. Hepatic histology in obese patients undergoing bariatric surgery. J Hepatol 2006; 45: 600-606.
5. Boza C, Riquelme A, Ibanez L, Duarte I, Norero E, Viviani P et al. Predictors of nonalcoholic steatohepatitis (NASH) in obese patients undergoing gastric bypass. Obes Surg 2005; 15: 1148-1153.
6. Reshef L, Olswang Y, Cassuto H, Blum B, Croniger CM, Kalhan SC et al. Glyceroneogenesis and the triglyceride/fatty acid cycle. J Biol Chem 2003; 278: 30413-30416.
7. Fruhbeck G. Obesity: aquaporin enters the picture. Nature 2005; 438: 436-437.
8. Fruhbeck G, Catalan V, Gomez-Ambrosi J, Rodrguez A. Aquaporin-7 and glycerol permeability as novel obesity drug-target pathways. Trends Pharmacol Sci 2006; 27: 345-347.
9. Rodrguez A, Catalan V, Gomez-Ambrosi J, Fruhbeck G. Aquaglyceroporins serve as metabolic gateways in adiposity and insulin resistance control. Cell Cycle 2011; 10: 1548-1556.
10. Jelen S, Wacker S, Aponte-Santamaria C, Skott M, Rojek A, Johanson U et al. Aquaporin-9 protein is the primary route of hepatocyte glycerol uptake for glycerol gluconeogenesis in mice. J Biol Chem 2011; 286: 44319-44325.
11. Calamita G, Gena P, Ferri D, Rosito A, Rojek A, Nielsen S et al. Biophysical assessment of aquaporin-9 as principal facilitative pathway in mouse liver import of glucogenetic glycerol. Biol Cell 2012; 104: 342-351.
12. Gena P, Mastrodonato M, Portincasa P, Fanelli E, Mentino D, Rodrguez A et al. Liver glycerol permeability and aquaporin-9 are dysregulated in a murine model of non-alcoholic Fatty liver disease. PLoS One 2013; 8: e78139.
13. Rojek AM, Skowronski MT, Fuchtbauer EM, Fuchtbauer AC, Fenton RA, Agre P et al. Defective glycerol metabolism in aquaporin 9 (AQP9) knockout mice. Proc Natl Acad Sci USA 2007; 104: 3609-3614.
14. Kuriyama H, Shimomura I, Kishida K, Kondo H, Furuyama N, Nishizawa H et al. Coordinated regulation of fat-specific and liver-specific glycerol channels, aquaporin adipose and aquaporin 9. Diabetes 2002; 51: 2915-2921.
15. Carbrey JM, Gorelick-Feldman DA, Kozono D, Praetorius J, Nielsen S, Agre P. Aquaglyceroporin AQP9: solute permeation and metabolic control of expression in liver. Proc Natl Acad Sci USA 2003; 100: 2945-2950.
16. Rodrguez A, Catalan V, Gomez-Ambrosi J, Garca-Navarro S, Rotellar F, Valent V et al. 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 2011; 96: E586-E597.
17. Catalan V, Gomez-Ambrosi J, Pastor C, Rotellar F, Silva C, Rodrguez A et al. Influence of morbid obesity and insulin resistance on gene expression levels of AQP7 in visceral adipose tissue and AQP9 in liver. Obes Surg 2008; 18: 695-701.
18. Miranda M, Ceperuelo-Mallafre V, Lecube A, Hernandez C, Chacon MR, Fort JM et al. Gene expression of paired abdominal adipose AQP7 and liver AQP9 in patients with morbid obesity: relationship with glucose abnormalities. Metabolism 2009; 58: 1762-1768.
19. Genuth S, Alberti KG, Bennett P, Buse J, Defronzo R, Kahn R et al. Follow-up report on the diagnosis of diabetes mellitus. Diabetes Care 2003; 26: 3160-3167.
20. Brunt EM. Nonalcoholic steatohepatitis. Semin Liver Dis 2004; 24: 3-20.
21. Younossi ZM, Stepanova M, Rafiq N, Makhlouf H, Younoszai Z, Agrawal R et al. Pathologic criteria for nonalcoholic steatohepatitis: interprotocol agreement and ability to predict liver-related mortality. Hepatology 2011; 53: 1874-1882.
22. Bell LN, Wang J, Muralidharan S, Chalasani S, Fullenkamp AM, Wilson LA et al. Relationship between adipose tissue insulin resistance and liver histology in nonalcoholic steatohepatitis: a pioglitazone versus vitamin E versus placebo for the treatment of nondiabetic patients with nonalcoholic steatohepatitis trial follow-up study. Hepatology 2012; 56: 1311-1318.
23. Asai M, Higuchi S, Kubota M, Iguchi K, Usui S, Hirano K. Regulators for blood glucose level affect gene expression of aquaporin 3. Biol Pharm Bull 2006; 29: 991-996.
24. Tsukaguchi H, Weremowicz S, Morton CC, Hediger MA. Functional and molecular characterization of the human neutral solute channel aquaporin-9. Am J Physiol 1999; 277: F685-F696.
25. Rodrguez A, Catalan V, Gomez-Ambrosi J, Fruhbeck G. Role of aquaporin-7 in the pathophysiological control of fat accumulation in mice. FEBS Lett 2006; 580: 4771-4776.
26. Fru hbeck G, Gomez-Ambrosi J, Salvador J. Leptin-induced lipolysis opposes the tonic inhibition of endogenous adenosine in white adipocytes. FASEB J 2001; 15: 333-340.
27. Ishibashi K, Sasaki S, Saito F, Ikeuchi T, Marumo F. Structure and chromosomal localization of a human water channel (AQP3) gene. Genomics 1995; 27: 352-354.
28. Ishibashi K, Kuwahara M, Gu Y, Tanaka Y, Marumo F, Sasaki S. 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 1998; 244: 268-274.
29. Elkjaer M, Vajda Z, Nejsum LN, Kwon T, Jensen UB, Amiry-Moghaddam M et al. Immunolocalization of AQP9 in liver, epididymis, testis, spleen, and brain. Biochem Biophys Res Commun 2000; 276: 1118-1128.
30. Nicchia GP, Frigeri A, Nico B, Ribatti D, Svelto M. Tissue distribution and membrane localization of aquaporin-9 water channel: evidence for sex-linked differences in liver. J Histochem Cytochem 2001; 49: 1547-1556.
31. Rojek A, Fuchtbauer EM, Fuchtbauer A, Jelen S, Malmendal A, Fenton RA et al. Liver-specific aquaporin 11 knockout mice show rapid vacuolization of the rough endoplasmic reticulum in periportal hepatocytes after feeding amino acids. Am J Physiol Gastrointest Liver Physiol 2013; 304: G501-G515.
32. Lebeck J, Gena P, O'Neill H, Skowronski MT, Lund S, Calamita G et al. Estrogen prevents increased hepatic aquaporin-9 expression and glycerol uptake during starvation. Am J Physiol Gastrointest Liver Physiol 2011; 302: G365-G374.
33. Branes MC, Morales B, Rios M, Villalon MJ. Regulation of the immunoexpression of aquaporin 9 by ovarian hormones in the rat oviductal epithelium. Am J Physiol Cell Physiol 2005; 288: C1048-C1057.
34. Wellejus A, Jensen HE, Loft S, Jonassen TE. Expression of aquaporin 9 in rat liver and efferent ducts of the male reproductive system after neonatal diethylstilbestrol exposure. J Histochem Cytochem 2008; 56: 425-432.
35. Pastor-Soler NM, Fisher JS, Sharpe R, Hill E, Van Hoek A, Brown D et al. Aquaporin 9 expression in the developing rat epididymis is modulated by steroid hormones. Reproduction 2010; 139: 613-621.
36. Ji YF, Chen LY, Xu KH, Yao JF, Shi YF, Shanguan XJ. Reduced expression of aquaporin 9 in tubal ectopic pregnancy. J Mol Histol 2013; 44: 167-173.
37. Calamita G, Portincasa P. Present and future therapeutic strategies in non-alcoholic fatty liver disease. Expert Opin Ther Targets 2007; 11: 1231-1249.
38. Widhalm K, Ghods E. Nonalcoholic fatty liver disease: a challenge for pediatricians. Int J Obes (Lond) 2010; 34: 1451-1467.
39. Postic C, Girard J. The role of the lipogenic pathway in the development of hepatic steatosis. Diabetes Metab 2008; 34: 643-648.
40. Calamita G, Ferri D, Gena P, Carreras FI, Liquori GE, Portincasa P et al. Altered expression and distribution of aquaporin-9 in the liver of rat with obstructive extrahepatic cholestasis. Am J Physiol Gastrointest Liver Physiol 2008; 295: G682-G690.
41. Potter JJ, Koteish A, Hamilton J, Liu X, Liu K, Agre P et al. Effects of acetaldehyde on hepatocyte glycerol uptake and cell size: implication of aquaporin 9. Alcohol Clin Exp Res 2011; 35: 939-945.
42. Portincasa P, Calamita G. Water channel proteins in bile formation and flow in health and disease: when immiscible becomes miscible. Mol Aspects Med 2012; 33: 651-664.
43. Potter JJ, Koteish A, Hamilton J, Liu X, Liu K, Agre P et al. Effects of acetaldehyde on hepatocyte glycerol uptake and cell size: implication of aquaporin 9. Alcohol Clin Exp Res 2011; 35: 939-945.
44. Lehmann GL, Carreras FI, Soria LR, Gradilone SA, Marinelli RA. LPS induces the TNF-alpha-mediated downregulation of rat liver aquaporin-8: role in sepsis-associated cholestasis. Am J Physiol Gastrointest Liver Physiol 2008; 294: G567-G575.