Acyl-CoA thioesterase-2 facilitates mitochondrial fatty acid oxidation in the liver

Journal of Lipid Research

Volumn 55, Issue 12, 2015, Pages 2458-2470

  Moffat, Cynthia ^a   Bhatia, Lavesh ^a   Nguyen, Teresa ^a   Lynch, Peter ^a   Wang, Miao ^b   Wang, Dongning ^c   Ilkayeva, Olga R ^c   Han, Xianlin ^b   Hirschey, Matthew D ^c   Claypool, Steven M ^d   Seifert, Erin L ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b BURNHAM INSTITUTE   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Acyl coenzyme A; Cardiolipin; Mitochondria; Mitochondrial proton leak; Mitochondrial thioesterase; Mouse; oxidation

Indexed keywords

ACYL COENZYME A THIOESTERASE 2; FATTY ACID; KETONE; PALMITOYL COENZYME A HYDROLASE; UNCLASSIFIED DRUG; ACYL COENZYME A; KETONE BODY; MITOCHONDRIAL ACYL-COA THIOESTERASE I, MOUSE; MITOCHONDRIAL PROTEIN; RECOMBINANT PROTEIN; THIOL ESTER HYDROLASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; ENZYME ACTIVITY; FATTY ACID METABOLISM; FATTY ACID OXIDATION; FATTY LIVER; LIVER MITOCHONDRION; MALE; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PROTEIN EXPRESSION; ANIMAL; BLOOD; C57BL MOUSE; CELL CULTURE; CIRCADIAN RHYTHM; COMPARATIVE STUDY; CYTOLOGY; ENERGY METABOLISM; ENZYMOLOGY; GENETICS; KINETICS; LIPID METABOLISM; LIVER; METABOLISM; OXIDATION REDUCTION REACTION; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ACYL COENZYME A; ANIMALS; CARBOHYDRATE METABOLISM; CELLS, CULTURED; CIRCADIAN RHYTHM; ENERGY METABOLISM; FATTY ACIDS, NONESTERIFIED; KETONE BODIES; KINETICS; LIPID METABOLISM; LIVER; MALE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA, LIVER; MITOCHONDRIAL PROTEINS; OXIDATION-REDUCTION; OXIDATIVE PHOSPHORYLATION; PALMITOYL-COA HYDROLASE; RECOMBINANT PROTEINS; THIOLESTER HYDROLASES;

EID: 84919742518     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M046961     Document Type: Article

References (39)

1. Koves, T. R., J. R. Ussher, R. C. Noland, D. Slentz, M. Mosedale, O. Ilkayeva, J. Bain, R. Stevens, J. R. Dyck, C. B. Newgard, et al. 2008. Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab. 7: 45-56.
2. Muoio, D. M., and P. D. Neufer. 2012. Lipid-induced mitochondrial stress and insulin action in muscle. Cell Metab. 15: 595-605.
3. Muoio, D. M., R. C. Noland, J. P. Kovalik, S. E. Seiler, M. N. Davies, K. L. DeBalsi, O. R. Ilkayeva, R. D. Stevens, I. Kheterpal, J. Zhang, et al. 2012. Muscle-specifi c deletion of carnitine acetyltransferase compromises glucose tolerance and metabolic fl exibility. Cell Metab. 15: 764-777.
4. van Eunen, K., S. M. Simons, A. Gerding, A. Bleeker, G. den Besten, C. M. Touw, S. M. Houten, B. K. Groen, K. Krab, D. J. Reijngoud, et al. 2013. Biochemical competition makes fatty-acid beta-oxidation vulnerable to substrate overload. PLOS Comput. Biol. 9: e1003186.
5. Shug, A., E. Lerner, C. Elson, and E. Shrago. 1971. The inhibition of adenine nucleotide translocase activity by oleoyl CoA and its reversal in rat liver mitochondria. Biochem. Biophys. Res. Commun. 43: 557-563.
6. Woldegiorgis, G., S. Y. Yousufzai, and E. Shrago. 1982. Studies on the interaction of palmitoyl coenzyme A with the adenine nucleotide translocase. J. Biol. Chem. 257: 14783-14787.
7. Hunt, M. C., K. Solaas, B. F. Kase, and S. E. Alexson. 2002. Characterization of an acyl-coA thioesterase that functions as a major regulator of peroxisomal lipid metabolism. J. Biol. Chem. 277: 1128-1138.
8. Tillander, V., E. Arvidsson Nordström, J. Reilly, M. Strozyk, P. P. Van Veldhoven, M. C. Hunt, and S. E. Alexson. 2014. Acyl-CoA thioesterase 9 (ACOT9) in mouse may provide a novel link between fatty acid and amino acid metabolism in mitochondria. Cell. Mol. Life Sci. 71: 933-948.
9. Zhuravleva, E., H. Gut, D. Hynx, D. Marcellin, C. K. Bleck, C. Genoud, P. Cron, J. J. Keusch, B. Dummler, M. D. Esposti, et al. 2012. Acyl coenzyme A thioesterase Them5/Acot15 is involved in cardiolipin remodeling and fatty liver development. Mol. Cell. Biol. 32: 2685-2697.
10. Zhang, Y., Y. Li, M. W. Niepel, Y. Kawano, S. Han, S. Liu, A. Marsili, P. R. Larsen, C. H. Lee, and D. E. Cohen. 2012. Targeted deletion of thioesterase superfamily member 1 promotes energy expenditure and protects against obesity and insulin resistance. Proc. Natl. Acad. Sci. USA. 109: 5417-5422.
11. Wei, J., H. W. Kang, and D. E. Cohen. 2009. Thioesterase superfamily member 2 (Them2)/acyl-CoA thioesterase 13 (Acot13): a homotetrameric hotdog fold thioesterase with selectivity for longchain fatty acyl-CoAs. Biochem. J. 421: 311-322.
12. Claypool, S. M., and C. M. Koehler. 2012. The complexity of cardiolipin in health and disease. Trends Biochem. Sci. 37: 32-41.
13. King, K. L., M. E. Young, J. Kerner, H. Huang, K. M. O'Shea, S. E. Alexson, C. L. Hoppel, and W. C. Stanley. 2007. Diabetes or peroxisome proliferator-activated receptor alpha agonist increases mitochondrial thioesterase I activity in heart. J. Lipid Res. 48: 1511-1517.
14. Stavinoha, M. A., J. W. RaySpellicy, M. F. Essop, C. Graveleau, E. D. Abel, M. L. Hart-Sailors, H. J. Mersmann, M. S. Bray, and M. E. Young. 2004. Evidence for mitochondrial thioesterase 1 as a peroxisome proliferator-activated receptor-alpha-regulated gene in cardiac and skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 287: E888-E895.
15. Hunt, M. C., S. E. Nousiainen, M. K. Huttunen, K. E. Orii, L. T. Svensson, and S. E. Alexson. 1999. Peroxisome proliferatorinduced long chain acyl-CoA thioesterases comprise a highly conserved novel multi-gene family involved in lipid metabolism. J. Biol. Chem. 274: 34317-34326.
16. Hunt, M. C., Y. Z. Yang, G. Eggertsen, C. M. Carneheim, M. Gafvels, C. Einarsson, and S. E. Alexson. 2000. The peroxisome prolifera-tor-activated receptor alpha (PPARalpha) regulates bile acid biosynthesis. J. Biol. Chem. 275: 28947-28953.
17. Seifert, E. L., V. Bezaire, C. Estey, and M. E. Harper. 2008. Essential role for uncoupling protein-3 in mitochondrial adaptation to fasting but not in fatty acid oxidation or fatty acid anion export. J. Biol. Chem. 283: 25124-25131.
18. Svensson, L. T., S. E. Alexson, and J. K. Hiltunen. 1995. Very long chain and long chain acyl-CoA thioesterases in rat liver mitochondria. Identification, purification, characterization, and induction by peroxisome proliferators. J. Biol. Chem. 270: 12177-12183.
19. Duarte, A., A. F. Castillo, R. Castilla, P. Maloberti, C. Paz, E. J. Podesta, and F. Cornejo Maciel. 2007. An arachidonic acid generation/export system involved in the regulation of cholesterol transport in mitochondria of steroidogenic cells. FEBS Lett. 581: 4023-4028.
20. Maloberti, P., R. Castilla, F. Castillo, F. Cornejo Maciel, C. F. Mendez, C. Paz, and E. J. Podesta. 2005. Silencing the expression of mitochondrial acyl-CoA thioesterase I and acyl-CoA synthetase 4 inhibits hormone-induced steroidogenesis. FEBS J. 272: 1804-1814.
21. Seifert, E. L., C. Estey, J. Y. Xuan, and M. E. Harper. 2010. Electron transport chain-dependent and -independent mechanisms of mitochondrial H2O2 emission during long-chain fatty acid oxidation. J. Biol. Chem. 285: 5748-5758.
22. Rogers, G. W., M. D. Brand, S. Petrosyan, D. Ashok, A. A. Elorza, D. A. Ferrick, and A. N. Murphy. 2011. High throughput microplate respiratory measurements using minimal quantities of isolated mitochondria. PLoS ONE. 6: e21746.
23. Christie, W. W., and X. Han. 2010. Lipid Analysis: Isolation, Separation, Identifi cation and Lipidomic Analysis. Oily Press, Bridgwater, UK.
24. Han, X., K. Yang, and R. W. Gross. 2008. Microfl uidics-based electrospray ionization enhances the intrasource separation of lipid classes and extends identifi cation of individual molecular species through multi-dimensional mass spectrometry: development of an automated high-throughput platform for shotgun lipidomics. Rapid Commun. Mass Spectrom. 22: 2115-2124.
25. Yang, K., H. Cheng, R. W. Gross, and X. Han. 2009. Automated lipid identifi cation and quantifi cation by multidimensional mass spectrometry-based shotgun lipidomics. Anal. Chem. 81: 4356-4368.
26. Yang, K., and X. Han. 2011. Accurate quantifi cation of lipid species by electrospray ionization mass spectrometry-Meet a key challenge in lipidomics. Metabolites. 1: 21-40.
27. Claypool, S. M., Y. Oktay, P. Boontheung, J. A. Loo, and C. M. Koehler. 2008. Cardiolipin defi nes the interactome of the major ADP/ATP carrier protein of the mitochondrial inner membrane. J. Cell Biol. 182: 937-950.
28. Claypool, S. M., J. M. McCaffery, and C. M. Koehler. 2006. Mitochondrial mislocalization and altered assembly of a cluster of Barth syndrome mutant tafazzins. J. Cell Biol. 174: 379-390.
29. Rouser, G., S. Fkeischer, and A. Yamamoto. 1970. Two dimensional then layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids. 5: 494-496.
30. Das, S., N. Hajnoczky, A. N. Antony, G. Csordas, L. D. Gaspers, D. L. Clemens, J. B. Hoek, and G. Hajnoczky. 2012. Mitochondrial morphology and dynamics in hepatocytes from normal and ethanol-fed rats. Pflugers Arch. 464: 101-109.
31. Guan, H. P., J. L. Goldstein, M. S. Brown, and G. Liang. 2009. Accelerated fatty acid oxidation in muscle averts fasting-induced hepatic steatosis in SJL/J mice. J. Biol. Chem. 284: 24644-24652.
32. Chicco, A. J., and G. C. Sparagna. 2007. Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am. J. Physiol. Cell Physiol. 292: C33-C44.
33. Himms-Hagen, J., and M. E. Harper. 2001. Physiological role of UCP3 may be export of fatty acids from mitochondria when fatty acid oxidation predominates: an hypothesis. Exp. Biol. Med. (Maywood). 226: 78-84.
34. Schönfeld, P., L. Schild, and W. Kunz. 1989. Long-chain fatty acids act as protonophoric uncouplers of oxidative phosphorylation in rat liver mitochondria. Biochim. Biophys. Acta. 977: 266-272.
35. Violante, S., L. Ijlst, H. van Lenthe, I. T. de Almeida, R. J. Wanders, and F. V. Ventura. 2010. Carnitine palmitoyltransferase 2: new insights on the substrate specifi city and implications for acylcarnitine profi ling. Biochim. Biophys. Acta. 1802: 728-732.
36. Johnson, T. M., W. R. Mann, C. J. Dragland, R. C. Anderson, G. M. Nemecek, and P. A. Bell. 1995. Over-expression and characterization of active recombinant rat liver carnitine palmitoyltransferase II using baculovirus. Biochem. J. 309: 689-693.
37. Gomes, L. C., G. Di Benedetto, and L. Scorrano. 2011. During autophagy mitochondria elongate, are spared from degradation and sustain cell viability. Nat. Cell Biol. 13: 589-598.
38. Jheng, H. F., P. J. Tsai, S. M. Guo, L. H. Kuo, C. S. Chang, I. J. Su, C. R. Chang, and Y. S. Tsai. 2012. Mitochondrial fi ssion contributes to mitochondrial dysfunction and insulin resistance in skeletal muscle. Mol. Cell. Biol. 32: 309-319.
39. Acehan, D., F. Vaz, R. H. Houtkooper, J. James, V. Moore, C. Tokunaga, W. Kulik, J. Wansapura, M. J. Toth, A. Strauss, et al. 2011. Cardiac and skeletal muscle defects in a mouse model of human Barth syndrome. J. Biol. Chem. 286: 899-908.