Hepatic Overexpression of CD36 Improves Glycogen Homeostasis and Attenuates High-Fat Diet-Induced Hepatic Steatosis and Insulin Resistance

REFERENCES

• Stefan N, Kantartzis K, Haring HU. 2008. Causes and metabolic consequences of fatty liver. Endocr Rev 29:939–960. http://dx.doi.org/10.1210/er.2008-0009.
   PubMed Web of Science ®Google Scholar
• Lu B, Bridges D, Yang Y, Fisher K, Cheng A, Chang L, Meng ZX, Lin JD, Downes M, Yu RT, Liddle C, Evans RM, Saltiel AR. 2014. Metabolic crosstalk: molecular links between glycogen and lipid metabolism in obesity. Diabetes 63:2935–2948. http://dx.doi.org/10.2337/db13-1531.
   PubMedGoogle Scholar
• Koonen DP, Jacobs RL, Febbraio M, Young ME, Soltys CL, Ong H, Vance DE, Dyck JR. 2007. Increased hepatic CD36 expression contributes to dyslipidemia associated with diet-induced obesity. Diabetes 56:2863–2871. http://dx.doi.org/10.2337/db07-0907.
   PubMed Web of Science ®Google Scholar
• Lee JH, Wada T, Febbraio M, He J, Matsubara T, Lee MJ, Gonzalez FJ, Xie W. 2010. A novel role for the dioxin receptor in fatty acid metabolism and hepatic steatosis. Gastroenterology 139:653–663. http://dx.doi.org/10.1053/j.gastro.2010.03.033.
   PubMed Web of Science ®Google Scholar
• Sheedfar F, Sung MM, Aparicio-Vergara M, Kloosterhuis NJ, Miquilena-Colina ME, Vargas-Castrillon J, Febbraio M, Jacobs RL, de Bruin A, Vinciguerra M, Garcia-Monzon C, Hofker MH, Dyck JR, Koonen DP. 2014. Increased hepatic CD36 expression with age is associated with enhanced susceptibility to nonalcoholic fatty liver disease. Aging 6:281–295. http://dx.doi.org/10.18632/aging.100652.
   PubMedGoogle Scholar
• Zhou J, Febbraio M, Wada T, Zhai Y, Kuruba R, He J, Lee JH, Khadem S, Ren S, Li S, Silverstein RL, Xie W. 2008. Hepatic fatty acid transporter Cd36 is a common target of LXR, PXR, and PPARgamma in promoting steatosis. Gastroenterology 134:556–567. http://dx.doi.org/10.1053/j.gastro.2007.11.037.
   PubMed Web of Science ®Google Scholar
• Buque X, Cano A, Miquilena-Colina ME, Garcia-Monzon C, Ochoa B, Aspichueta P. 2012. High insulin levels are required for FAT/CD36 plasma membrane translocation and enhanced fatty acid uptake in obese Zucker rat hepatocytes. Am J Physiol Endocrinol Metab 303:E504–E514. http://dx.doi.org/10.1152/ajpendo.00653.2011.
   PubMedGoogle Scholar
• Miquilena-Colina ME, Lima-Cabello E, Sanchez-Campos S, Garcia-Mediavilla MV, Fernandez-Bermejo M, Lozano-Rodriguez T, Vargas-Castrillon J, Buque X, Ochoa B, Aspichueta P, Gonzalez-Gallego J, Garcia-Monzon C. 2011. Hepatic fatty acid translocase CD36 upregulation is associated with insulin resistance, hyperinsulinaemia and increased steatosis in non-alcoholic steatohepatitis and chronic hepatitis C. Gut 60:1394–1402. http://dx.doi.org/10.1136/gut.2010.222844.
   PubMed Web of Science ®Google Scholar
• Zhang YL, Hernandez-Ono A, Siri P, Weisberg S, Conlon D, Graham MJ, Crooke RM, Huang LS, Ginsberg HN. 2006. Aberrant hepatic expression of PPARgamma2 stimulates hepatic lipogenesis in a mouse model of obesity, insulin resistance, dyslipidemia, and hepatic steatosis. J Biol Chem 281:37603–37615. http://dx.doi.org/10.1074/jbc.M604709200.
   PubMed Web of Science ®Google Scholar
• Nassir F, Adewole OL, Brunt EM, Abumrad NA. 2013. CD36 deletion reduces VLDL secretion, modulates liver prostaglandins, and exacerbates hepatic steatosis in ob/ob mice. J Lipid Res 54:2988–2997. http://dx.doi.org/10.1194/jlr.M037812.
   PubMedGoogle Scholar
• Deng B, Sullivan MA, Li J, Tan X, Zhu C, Schulz BL, Gilbert RG. 2015. Molecular structure of glycogen in diabetic liver. Glycoconj J 32:113–118. http://dx.doi.org/10.1007/s10719-015-9578-6.
   PubMedGoogle Scholar
• Ferrannini E, Lanfranchi A, Rohner-Jeanrenaud F, Manfredini G, Van de Werve G. 1990. Influence of long-term diabetes on liver glycogen metabolism in the rat. Metabolism 39:1082–1088. http://dx.doi.org/10.1016/0026-0495(90)90170-H.
   PubMed Web of Science ®Google Scholar
• Krssak M, Brehm A, Bernroider E, Anderwald C, Nowotny P, Dalla Man C, Cobelli C, Cline GW, Shulman GI, Waldhausl W, Roden M. 2004. Alterations in postprandial hepatic glycogen metabolism in type 2 diabetes. Diabetes 53:3048–3056. http://dx.doi.org/10.2337/diabetes.53.12.3048.
   PubMed Web of Science ®Google Scholar
• von Wilamowitz-Moellendorff A, Hunter RW, Garcia-Rocha M, Kang L, Lopez-Soldado I, Lantier L, Patel K, Peggie MW, Martinez-Pons C, Voss M, Calbo J, Cohen PT, Wasserman DH, Guinovart JJ, Sakamoto K. 2013. Glucose-6-phosphate-mediated activation of liver glycogen synthase plays a key role in hepatic glycogen synthesis. Diabetes 62:4070–4082. http://dx.doi.org/10.2337/db13-0880.
   PubMedGoogle Scholar
• Zhang Y, Xu D, Huang H, Chen S, Wang L, Zhu L, Jiang X, Ruan X, Luo X, Cao P, Liu W, Pan Y, Wang Z, Chen Y. 2014. Regulation of glucose homeostasis and lipid metabolism by PPP1R3G-mediated hepatic glycogenesis. Mol Endocrinol 28:116–126. http://dx.doi.org/10.1210/me.2013-1268.
   PubMedGoogle Scholar
• Puschel GP, Kirchner C, Schroder A, Jungermann K. 1993. Glycogenolytic and antiglycogenolytic prostaglandin E2 actions in rat hepatocytes are mediated via different signalling pathways. Eur J Biochem 218:1083–1089. http://dx.doi.org/10.1111/j.1432-1033.1993.tb18468.x.
   PubMedGoogle Scholar
• Julian MT, Alonso N, Ojanguren I, Pizarro E, Ballestar E, Puig-Domingo M. 2015. Hepatic glycogenosis: an underdiagnosed complication of diabetes mellitus? World J Diabetes 6:321–325. http://dx.doi.org/10.4239/wjd.v6.i2.321.
   PubMedGoogle Scholar
• Taylor AJ, Ye JM, Schmitz-Peiffer C. 2006. Inhibition of glycogen synthesis by increased lipid availability is associated with subcellular redistribution of glycogen synthase. J Endocrinol 188:11–23. http://dx.doi.org/10.1677/joe.1.06381.
   PubMedGoogle Scholar
• Lopez-Soldado I, Zafra D, Duran J, Adrover A, Calbo J, Guinovart JJ. 2015. Liver glycogen reduces food intake and attenuates obesity in a high-fat diet-fed mouse model. Diabetes 64:796–807. http://dx.doi.org/10.2337/db14-0728.
   PubMedGoogle Scholar
• O'Doherty RM, Jensen PB, Anderson P, Jones JG, Berman HK, Kearney D, Newgard CB. 2000. Activation of direct and indirect pathways of glycogen synthesis by hepatic overexpression of protein targeting to glycogen. J Clin Invest 105:479–488. http://dx.doi.org/10.1172/JCI8673.
   PubMedGoogle Scholar
• Zhou J, Zhai Y, Mu Y, Gong H, Uppal H, Toma D, Ren S, Evans RM, Xie W. 2006. A novel pregnane X receptor-mediated and sterol regulatory element-binding protein-independent lipogenic pathway. J Biol Chem 281:15013–15020. http://dx.doi.org/10.1074/jbc.M511116200.
   PubMed Web of Science ®Google Scholar
• Lu P, Yan J, Liu K, Garbacz WG, Wang P, Xu M, Ma X, Xie W. 2015. Activation of aryl hydrocarbon receptor dissociates fatty liver from insulin resistance by inducing fibroblast growth factor 21. Hepatology 61:1908–1919. http://dx.doi.org/10.1002/hep.27719.
   PubMed Web of Science ®Google Scholar
• Jiang M, He J, Kucera H, Gaikwad NW, Zhang B, Xu M, O'Doherty RM, Selcer KW, Xie W. 2014. Hepatic overexpression of steroid sulfatase ameliorates mouse models of obesity and type 2 diabetes through sex-specific mechanisms. J Biol Chem 289:8086–8097. http://dx.doi.org/10.1074/jbc.M113.535914.
   PubMed Web of Science ®Google Scholar
• Folch J, Lees M, Sloane Stanley GH. 1957. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509.
   PubMed Web of Science ®Google Scholar
• Poloyac SM, Zhang Y, Bies RR, Kochanek PM, Graham SH. 2006. Protective effect of the 20-HETE inhibitor HET0016 on brain damage after temporary focal ischemia. J Cereb Blood Flow Metab 26:1551–1561. http://dx.doi.org/10.1038/sj.jcbfm.9600309.
   PubMedGoogle Scholar
• Theken KN, Deng Y, Schuck RN, Oni-Orisan A, Miller TM, Kannon MA, Poloyac SM, Lee CR. 2012. Enalapril reverses high-fat diet-induced alterations in cytochrome P450-mediated eicosanoid metabolism. Am J Physiol Endocrinol Metab 302:E500–E509. http://dx.doi.org/10.1152/ajpendo.00370.2011.
   PubMed Web of Science ®Google Scholar
• Parniak MA, Kalant N. 1988. Enhancement of glycogen concentrations in primary cultures of rat hepatocytes exposed to glucose and fructose. Biochem J 251:795–802. http://dx.doi.org/10.1042/bj2510795.
   PubMedGoogle Scholar
• Lo S, Russell JC, Taylor AW. 1970. Determination of glycogen in small tissue samples. J Appl Physiol 28:234–236.
   PubMed Web of Science ®Google Scholar
• Mustonen AM, Kakela R, Halonen T, Karja V, Vartiainen E, Nieminen P. 2012. Fatty acid mobilization in voles: model species for rapid fasting response and fatty liver. Comp Biochem Physiol A Mol Integr Physiol 163:152–160. http://dx.doi.org/10.1016/j.cbpa.2012.05.196.
   PubMedGoogle Scholar
• Wapnir RA, Lifshitz F. 1977. Fasting-induced hypoglycemia in experimentally malnourished rats. J Nutr 107:383–390.
   PubMedGoogle Scholar
• Magnusson I, Rothman DL, Jucker B, Cline GW, Shulman RG, Shulman GI. 1994. Liver glycogen turnover in fed and fasted humans. Am J Physiol 266:E796–E803.
   PubMed Web of Science ®Google Scholar
• Cohen P, Nimmo HG, Proud CG. 1978. How does insulin stimulate glycogen synthesis? Biochem Soc Symp 43:69–95.
   Google Scholar
• Nuttall FQ, Gilboe DP, Gannon MC, Niewoehner CB, Tan AW. 1988. Regulation of glycogen synthesis in the liver. Am J Med 85:77–85. http://dx.doi.org/10.1016/0002-9343(88)90400-7.
   PubMedGoogle Scholar
• Viollet B, Horman S, Leclerc J, Lantier L, Foretz M, Billaud M, Giri S, Andreelli F. 2010. AMPK inhibition in health and disease. Crit Rev Biochem Mol Biol 45:276–295. http://dx.doi.org/10.3109/10409238.2010.488215.
   PubMed Web of Science ®Google Scholar
• Cohen PT. 2002. Protein phosphatase 1: targeted in many directions. J Cell Sci 115:241–256.
   PubMed Web of Science ®Google Scholar
• Korrodi-Gregorio L, Esteves SL, Fardilha M. 2014. Protein phosphatase 1 catalytic isoforms: specificity toward interacting proteins. Transl Res 164:366–391. http://dx.doi.org/10.1016/j.trsl.2014.07.001.
   PubMedGoogle Scholar
• Kuda O, Jenkins CM, Skinner JR, Moon SH, Su X, Gross RW, Abumrad NA. 2011. CD36 protein is involved in store-operated calcium flux, phospholipase A2 activation, and production of prostaglandin E2. J Biol Chem 286:17785–17795. http://dx.doi.org/10.1074/jbc.M111.232975.
   PubMedGoogle Scholar
• Nauli AM, Nassir F, Zheng S, Yang Q, Lo CM, Vonlehmden SB, Lee D, Jandacek RJ, Abumrad NA, Tso P. 2006. CD36 is important for chylomicron formation and secretion and may mediate cholesterol uptake in the proximal intestine. Gastroenterology 131:1197–1207. http://dx.doi.org/10.1053/j.gastro.2006.08.012.
   PubMedGoogle Scholar
• Lai G, Wu J, Liu X, Zhao Y. 2012. 20-HETE induces hyperglycemia through the cAMP/PKA-PhK-GP pathway. Mol Endocrinol 26:1907–1916. http://dx.doi.org/10.1210/me.2012-1139.
   PubMedGoogle Scholar
• Sacerdoti D, Balazy M, Angeli P, Gatta A, McGiff JC. 1997. Eicosanoid excretion in hepatic cirrhosis. Predominance of 20-HETE. J Clin Invest 100:1264–1270. http://dx.doi.org/10.1172/JCI119640.
   PubMed Web of Science ®Google Scholar
• Silverstein RL, Febbraio M. 2009. CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Sci Signal 2:re3. http://dx.doi.org/10.1126/scisignal.272re3.
   PubMed Web of Science ®Google Scholar
• Wilson CG, Tran JL, Erion DM, Vera NB, Febbraio M, Weiss EJ. 2016. Hepatocyte-specific disruption of CD36 attenuates fatty liver and improves insulin sensitivity in HFD-fed mice. Endocrinology 157:570–585. http://dx.doi.org/10.1210/en.2015-1866.
   PubMed Web of Science ®Google Scholar
• Macauley M, Smith FE, Thelwall PE, Hollingsworth KG, Taylor R. 2015. Diurnal variation in skeletal muscle and liver glycogen in humans with normal health and type 2 diabetes. Clin Sci 128:707–713. http://dx.doi.org/10.1042/CS20140681.
   PubMed Web of Science ®Google Scholar
• Ros S, Garcia-Rocha M, Calbo J, Guinovart JJ. 2011. Restoration of hepatic glycogen deposition reduces hyperglycaemia, hyperphagia and gluconeogenic enzymes in a streptozotocin-induced model of diabetes in rats. Diabetologia 54:2639–2648. http://dx.doi.org/10.1007/s00125-011-2238-x.
   PubMed Web of Science ®Google Scholar
• Rui L. 2014. Energy metabolism in the liver. Compr Physiol 4:177–197. http://dx.doi.org/10.1002/cphy.c130024.
   PubMed Web of Science ®Google Scholar
• Luo X, Zhang Y, Ruan X, Jiang X, Zhu L, Wang X, Ding Q, Liu W, Pan Y, Wang Z, Chen Y. 2011. Fasting-induced protein phosphatase 1 regulatory subunit contributes to postprandial blood glucose homeostasis via regulation of hepatic glycogenesis. Diabetes 60:1435–1445. http://dx.doi.org/10.2337/db10-1663.
   PubMed Web of Science ®Google Scholar
• Gomez-Foix AM, Rodriguez-Gil JE, Guinovart JJ, Bosch F. 1989. Prostaglandins E2 and F2 alpha affect glycogen synthase and phosphorylase in isolated hepatocytes. Biochem J 261:93–97. http://dx.doi.org/10.1042/bj2610093.
   PubMedGoogle Scholar
• de Souza HM, Borba-Murad GR, Ceddia RB, Curi R, Vardanega-Peicher M, Bazotte RB. 2001. Rat liver responsiveness to gluconeogenic substrates during insulin-induced hypoglycemia. Braz J Med Biol Res 34:771–777. http://dx.doi.org/10.1590/S0100-879X2001000600012.
   PubMedGoogle Scholar
• Newgard CB, Hirsch LJ, Foster DW, McGarry JD. 1983. Studies on the mechanism by which exogenous glucose is converted into liver glycogen in the rat. A direct or an indirect pathway? J Biol Chem 258:8046–8052.
   PubMed Web of Science ®Google Scholar
• Bjornsson OG, Sparks JD, Sparks CE, Gibbons GF. 1992. Prostaglandins suppress VLDL secretion in primary rat hepatocyte cultures: relationships to hepatic calcium metabolism. J Lipid Res 33:1017–1027.
   PubMedGoogle Scholar
• Okumura T, Kanemaki T, Kitade H. 1993. Stimulation of glucose incorporation into glycogen by E-series prostaglandins in cultured rat hepatocytes. Biochim Biophys Acta 1176:137–142.
   PubMedGoogle Scholar