C1q/TNF-Related Protein 9 (CTRP9) attenuates hepatic steatosis via the autophagy-mediated inhibition of endoplasmic reticulum stress

Molecular and Cellular Endocrinology

Volumn 417, Issue , 2015, Pages 131-140

  Jung, Tae Woo ^a   Hong, Ho Cheol ^a   Hwang, Hwan Jin ^a   Yoo, Hye Jin ^a   Baik, Sei Hyun ^a   Choi, Kyung Mook ^a  

^a Korea University College of Medicine   (South Korea)

Author keywords

AMP activated protein kinase; Apoptosis; Autophagy; C1q TNF Related Protein 9; Endoplasmic reticulum stress; Non alcoholic fatty liver

Indexed keywords

3 METHYLADENINE; ADENYLATE KINASE; ADIPONECTIN; BECLIN 1; CASPASE 3; CHAPERONE; CHLOROQUINE; FAS LIGAND; MESSENGER RNA; PROTEIN P62; RECOMBINANT COMPLEMENT COMPONENT C1Q TUMOR NECROSIS FACTOR RELATED PROTEIN; STEROL REGULATORY ELEMENT BINDING PROTEIN; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; C1QTNF9B PROTEIN, HUMAN; CTRP9 PROTEIN, MOUSE; GLYCOPROTEIN; PALMITIC ACID; TUNICAMYCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL VIABILITY; CHROMATIN CONDENSATION; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; DRUG RESPONSE; ENDOPLASMIC RETICULUM STRESS; FATTY ACID OXIDATION; FATTY LIVER; GLUCOSE TOLERANCE; HUMAN; HUMAN CELL; IN VITRO STUDY; INSULIN SENSITIVITY; INTRACELLULAR TRANSPORT; LIPID DIET; LIPID METABOLISM; LIPOGENESIS; LIVER CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PHOSPHORYLATION; WEIGHT GAIN; ANIMAL; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION REGULATION; HEP-G2 CELL LINE; METABOLISM; NONALCOHOLIC FATTY LIVER;

ADIPONECTIN; ANIMALS; AUTOPHAGY; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION; GLYCOPROTEINS; HEP G2 CELLS; HUMANS; LIPID METABOLISM; MICE; NON-ALCOHOLIC FATTY LIVER DISEASE; PALMITIC ACID; TUNICAMYCIN;

EID: 84960260263     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2015.09.027     Document Type: Article

References (47)

1. Argo C.K., Caldwell S.H. Epidemiology and natural history of non-alcoholic steatohepatitis. Clin. Liver Dis. 2009, 13:511-531.
2. Bachar-Wikstrom E., Wikstrom J.D., Ariav Y., Tirosh B., Kaiser N., Cerasi E., Leibowitz G. Stimulation of autophagy improves endoplasmic reticulum stress-induced diabetes. Diabetes 2013, 62:1227-1237.
3. Browning J.D., Szczepaniak L.S., Dobbins R., Nuremberg P., Horton J.D., Cohen J.C., Grundy S.M., Hobbs H.H. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 2004, 40:1387-1395.
4. Cai G., Cole S.A., Freeland-Graves J.H., MacCluer J.W., Blangero J., Comuzzie A.G. Genome-wide scans reveal quantitative trait Loci on 8p and 13q related to insulin action and glucose metabolism: the San Antonio family heart Study. Diabetes 2004, 53:1369-1374.
5. Cao J., Dai D.L., Yao L., Yu H.H., Ning B., Zhang Q., Chen J., Cheng W.H., Shen W., Yang Z.X. Saturated fatty acid induction of endoplasmic reticulum stress and apoptosis in human liver cells via the PERK/ATF4/CHOP signaling pathway. Mol. Cell Biochem. 2012, 364:115-129.
6. Das S.K., Chu W.S., Mondal A.K., Sharma N.K., Kern P.A., Rasouli N., Elbein S.C. Effect of pioglitazone treatment on endoplasmic reticulum stress response in human adipose and in palmitate-induced stress in human liver and adipose cell lines. Am. J. Physiol. Endocrinol. Metab. 2008, 295:E393-E400.
7. Gonzalez-Rodriguez A., Mayoral R., Agra N., Valdecantos M.P., Pardo V., Miquilena-Colina M.E., Vargas-Castrillon J., Lo Iacono O., Corazzari M., Fimia G.M., Piacentini M., Muntane J., Bosca L., Garcia-Monzon C., Martin-Sanz P., Valverde A.M. Impaired autophagic flux is associated with increased endoplasmic reticulum stress during the development of NAFLD. Cell Death Dis. 2014, 5:e1179.
8. Gu Y., Sun X.X., Ye J.M., He L., Yan S.S., Zhang H.H., Hu L.H., Yuan J.Y., Yu Q. Arctigenin alleviates ER stress via activating AMPK. Acta Pharmacol. Sin. 2012, 33:941-952.
9. Hardie D.G. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat. Rev. Mol. Cell Biol. 2007, 8:774-785.
10. Herrero-Martin G., Hoyer-Hansen M., Garcia-Garcia C., Fumarola C., Farkas T., Lopez-Rivas A., Jaattela M. TAK1 activates AMPK-dependent cytoprotective autophagy in TRAIL-treated epithelial cells. EMBO J. 2009, 28:677-685.
11. Horton J.D. Sterol regulatory element-binding proteins: transcriptional activators of lipid synthesis. Biochem. Soc. Trans. 2002, 30:1091-1095.
12. Hwang Y.C., Woo Oh S., Park S.W., Park C.Y. Association of serum C1q/TNF-related Protein-9 (CTRP9) concentration with visceral adiposity and metabolic syndrome in humans. Int. J. Obes. Lond. 2013, 38(9):1207-1212.
13. Kambara T., Ohashi K., Shibata R., Ogura Y., Maruyama S., Enomoto T., Uemura Y., Shimizu Y., Yuasa D., Matsuo K., Miyabe M., Kataoka Y., Murohara T., Ouchi N. CTRP9 protein protects against myocardial injury following ischemia-reperfusion through AMP-activated protein kinase (AMPK)-dependent mechanism. J. Biol. Chem. 2012, 287:18965-18973.
14. Kim J., Kundu M., Viollet B., Guan K.L. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 2011, 13:132-141.
15. Kim K.H., Lee M.S. Autophagy-a key player in cellular and body metabolism. Nat. Rev. Endocrinol. 2014, 10:322-337.
16. Klionsky D.J. The molecular machinery of autophagy: unanswered questions. J. Cell Sci. 2005, 118:7-18.
17. Klionsky D.J., Abdalla F.C., Abeliovich H., Abraham R.T., Acevedo-Arozena A., Adeli K., Agholme L., Agnello M., Agostinis P., Aguirre-Ghiso J.A., Ahn H.J., Ait-Mohamed O., Ait-Si-Ali S., Akematsu T., Akira S., Al-Younes H.M., Al-Zeer M.A., Albert M.L., Albin R.L., Alegre-Abarrategui J., Aleo M.F., Alirezaei M., Almasan A., Almonte-Becerril M., Amano A., Amaravadi R., Amarnath S., Amer A.O., Andrieu-Abadie N., Anantharam V., Ann D.K., Anoopkumar-Dukie S., Aoki H., Apostolova N., Arancia G., Aris J.P., Asanuma K., Asare N.Y., Ashida H., Askanas V., Askew D.S., Auberger P., Baba M., Backues S.K., Baehrecke E.H., Bahr B.A., Bai X.Y., Bailly Y., Baiocchi R., Baldini G., Balduini W., Ballabio A., Bamber B.A., Bampton E.T., Banhegyi G., Bartholomew C.R., Bassham D.C., Bast R.C., Batoko H., Bay B.H., Beau I., Bechet D.M., Begley T.J., Behl C., Behrends C., Bekri S., Bellaire B., Bendall L.J., Benetti L., Berliocchi L., Bernardi H., Bernassola F., Besteiro S., Bhatia-Kissova I., Bi X., Biard-Piechaczyk M., Blum J.S., Boise L.H., Bonaldo P., Boone D.L., Bornhauser B.C., Bortoluci K.R., Bossis I., Bost F., Bourquin J.P., Boya P., Boyer-Guittaut M., Bozhkov P.V., Brady N.R., Brancolini C., Brech A., Brenman J.E., Brennand A., Bresnick E.H., Brest P., Bridges D., Bristol M.L., Brookes P.S., Brown E.J., Brumell J.H., et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012, 8:445-544.
18. Li L., Huang J.L., Liu Q.C., Wu P.H., Liu R.Y., Zeng Y.X., Huang W.L. Endostatin gene therapy for liver cancer by a recombinant adenovirus delivery. World J. Gastroenterol. 2004, 10:1867-1871.
19. Matsui Y., Takagi H., Qu X., Abdellatif M., Sakoda H., Asano T., Levine B., Sadoshima J. Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ. Res. 2007, 100:914-922.
20. Mei S., Ni H.M., Manley S., Bockus A., Kassel K.M., Luyendyk J.P., Copple B.L., Ding W.X. Differential roles of unsaturated and saturated fatty acids on autophagy and apoptosis in hepatocytes. J. Pharmacol. Exp. Ther. 2011, 339:487-498.
21. Meley D., Bauvy C., Houben-Weerts J.H., Dubbelhuis P.F., Helmond M.T., Codogno P., Meijer A.J. AMP-activated protein kinase and the regulation of autophagic proteolysis. J. Biol. Chem. 2006, 281:34870-34879.
22. Ni M., Lee A.S. ER chaperones in mammalian development and human diseases. FEBS Lett. 2007, 581:3641-3651.
23. Ogata M., Hino S., Saito A., Morikawa K., Kondo S., Kanemoto S., Murakami T., Taniguchi M., Tanii I., Yoshinaga K., Shiosaka S., Hammarback J.A., Urano F., Imaizumi K. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol. Cell Biol. 2006, 26:9220-9231.
24. Otabe S., Yuan X., Fukutani T., Wada N., Hashinaga T., Nakayama H., Hirota N., Kojima M., Yamada K. Overexpression of human adiponectin in transgenic mice results in suppression of fat accumulation and prevention of premature death by high-calorie diet. Am. J. Physiol. Endocrinol. Metab. 2007, 293:E210-E218.
25. Ozcan U., Cao Q., Yilmaz E., Lee A.H., Iwakoshi N.N., Ozdelen E., Tuncman G., Gorgun C., Glimcher L.H., Hotamisligil G.S. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 2004, 306:457-461.
26. Ozcan U., Yilmaz E., Ozcan L., Furuhashi M., Vaillancourt E., Smith R.O., Gorgun C.Z., Hotamisligil G.S. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006, 313:1137-1140.
27. Papackova Z., Dankova H., Palenickova E., Kazdova L., Cahova M. Effect of short- and long-term high-fat feeding on autophagy flux and lysosomal activity in rat liver. Physiol. Res. 2012, 61(Suppl. 2):S67-S76.
28. Peterson J.M., Wei Z., Seldin M.M., Byerly M.S., Aja S., Wong G.W. CTRP9 transgenic mice are protected from diet-induced obesity and metabolic dysfunction. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2013, 305:R522-R533.
29. Pfaffenbach K.T., Gentile C.L., Nivala A.M., Wang D., Wei Y., Pagliassotti M.J. Linking endoplasmic reticulum stress to cell death in hepatocytes: roles of C/EBP homologous protein and chemical chaperones in palmitate-mediated cell death. Am. J. Physiol. Endocrinol. Metab. 2010, 298:E1027-E1035.
30. Saimura M., Nagai E., Mizumoto K., Maehara N., Okino H., Katano M., Matsumoto K., Nakamura T., Narumi K., Nukiwa T., Tanaka M. Intraperitoneal injection of adenovirus-mediated NK4 gene suppresses peritoneal dissemination of pancreatic cancer cell line AsPC-1 in nude mice. Cancer Gene Ther. 2002, 9:799-806.
31. Salvado L., Coll T., Gomez-Foix A.M., Salmeron E., Barroso E., Palomer X., Vazquez-Carrera M. Oleate prevents saturated-fatty-acid-induced ER stress, inflammation and insulin resistance in skeletal muscle cells through an AMPK-dependent mechanism. Diabetologia 2013, 56:1372-1382.
32. Satoh H., Nguyen M.T., Trujillo M., Imamura T., Usui I., Scherer P.E., Olefsky J.M. Adenovirus-mediated adiponectin expression augments skeletal muscle insulin sensitivity in male Wistar rats. Diabetes 2005, 54:1304-1313.
33. Schroder M., Kaufman R.J. The mammalian unfolded protein response. Annu. Rev. Biochem. 2005, 74:739-789.
34. Seldin M.M., Tan S.Y., Wong G.W. Metabolic function of the CTRP family of hormones. Rev. Endocr. Metab. Disord. 2013, 15(2):111-123.
35. Seo J., Fortuno E.S., Suh J.M., Stenesen D., Tang W., Parks E.J., Adams C.M., Townes T., Graff J.M. Atf4 regulates obesity, glucose homeostasis, and energy expenditure. Diabetes 2009, 58:2565-2573.
36. Sha H., He Y., Chen H., Wang C., Zenno A., Shi H., Yang X., Zhang X., Qi L. The IRE1alpha-XBP1 pathway of the unfolded protein response is required for adipogenesis. Cell Metab. 2009, 9:556-564.
37. Shi W.Y., Xiao D., Wang L., Dong L.H., Yan Z.X., Shen Z.X., Chen S.J., Chen Y., Zhao W.L. Therapeutic metformin/AMPK activation blocked lymphoma cell growth via inhibition of mTOR pathway and induction of autophagy. Cell Death Dis. 2012, 3:e275.
38. Tonjes A., Bluher M., Stumvoll M. Retinol-binding protein 4 and new adipocytokines in nonalcoholic fatty liver disease. Curr. Pharm. Des. 2010, 16:1921-1928.
39. Vingtdeux V., Giliberto L., Zhao H., Chandakkar P., Wu Q., Simon J.E., Janle E.M., Lobo J., Ferruzzi M.G., Davies P., Marambaud P. AMP-activated protein kinase signaling activation by resveratrol modulates amyloid-beta peptide metabolism. J. Biol. Chem. 2010, 285:9100-9113.
40. Wang G.L., Fu Y.C., Xu W.C., Feng Y.Q., Fang S.R., Zhou X.H. Resveratrol inhibits the expression of SREBP1 in cell model of steatosis via Sirt1-FOXO1 signaling pathway. Biochem. Biophys. Res. Commun. 2009, 380:644-649.
41. Wang Y., Wu Z., Li D., Wang D., Wang X., Feng X., Xia M. Involvement of oxygen-regulated protein 150 in AMP-activated protein kinase-mediated alleviation of lipid-induced endoplasmic reticulum stress. J. Biol. Chem. 2011, 286:11119-11131.
42. Wei Z., Lei X., Petersen P.S., Aja S., Wong G.W. Targeted deletion of C1q/TNF-related protein 9 increases food intake, decreases insulin sensitivity, and promotes hepatic steatosis in mice. Am. J. Physiol. Endocrinol. Metab. 2014, 306:E779-E790.
43. Werstuck G.H., Lentz S.R., Dayal S., Hossain G.S., Sood S.K., Shi Y.Y., Zhou J., Maeda N., Krisans S.K., Malinow M.R., Austin R.C. Homocysteine-induced endoplasmic reticulum stress causes dysregulation of the cholesterol and triglyceride biosynthetic pathways. J. Clin. Invest. 2001, 107:1263-1273.
44. Wong G.W., Krawczyk S.A., Kitidis-Mitrokostas C., Ge G., Spooner E., Hug C., Gimeno R., Lodish H.F. Identification and characterization of CTRP9, a novel secreted glycoprotein, from adipose tissue that reduces serum glucose in mice and forms heterotrimers with adiponectin. FASEB J. 2009, 23:241-258.
45. Wong G.W., Wang J., Hug C., Tsao T.S., Lodish H.F. A family of Acrp30/adiponectin structural and functional paralogs. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:10302-10307.
46. Wu Y., Li X., Zhu J.X., Xie W., Le W., Fan Z., Jankovic J., Pan T. Resveratrol-activated AMPK/SIRT1/autophagy in cellular models of Parkinson's disease. Neurosignals 2011, 19:163-174.
47. Yang L., Li P., Fu S., Calay E.S., Hotamisligil G.S. Defective hepatic autophagy in obesity promotes ER stress and causes insulin resistance. Cell Metab. 2010, 11:467-478.