Increased hepatic mitochondrial FA oxidation reduces plasma and liver TG levels and is associated with regulation of UCPs and APOC-III in rats

Journal of Lipid Research

Volumn 58, Issue 7, 2017, Pages 1362-1373

  Lindquist, Carine ^a,b   Bjørndal, Bodil ^a   Rossmann, Christine Renate ^c   Tusubira, Deusdedit ^a   Svardal, Asbjørn ^a   Røsland, Gro Vatne ^a   Tronstad, Karl Johan ^a   Hallström, Seth ^c   Berge, Rolf Kristian ^a,b  

^a UNIVERSITY OF BERGEN   (Norway)

^b HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^c MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

2 (tridec 12 yn 1 ylthio)acetic acid; Apolipoprotein C III; Fatty acid; Fatty acid metabolism; Lipids; Lipids oxidation; Lipoproteins; Metabolic syndrome; Mitochondria; Nonalcoholic fatty liver disease; Triglyceride; Uncoupling protein

Indexed keywords

2 (TRIDEC 12 YN 1 YLTHIO)ACETIC ACID; ACETIC ACID DERIVATIVE; ADENOSINE DIPHOSPHATE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; APOLIPOPROTEIN C3; BIOLOGICAL MARKER; CITRATE SYNTHASE; CYTOCHROME C; KETONE BODY; LIPOPROTEIN LIPASE; MITOCHONDRIAL DNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN; UNCOUPLING PROTEIN 2; UNCOUPLING PROTEIN 3; VERY LOW DENSITY LIPOPROTEIN RECEPTOR; ACETIC ACID; ACETYLCARNITINE; CARNITINE; FATTY ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET THERAPY; DOWN REGULATION; ENZYME ACTIVITY; FATTY ACID OXIDATION; GENE EXPRESSION; LIVER MITOCHONDRION; MALE; MITOCHONDRIAL BIOGENESIS; NONHUMAN; PRIORITY JOURNAL; RAT; TISSUE LEVEL; TRIACYLGLYCEROL BLOOD LEVEL; TRIGLYCERIDE TISSUE LEVEL; UPREGULATION; ANIMAL; BLOOD; CHEMISTRY; DRUG EFFECTS; ENERGY METABOLISM; LIVER; METABOLISM; OXIDATION REDUCTION REACTION; WISTAR RAT;

ACETIC ACID; ACETYLCARNITINE; ANIMALS; APOLIPOPROTEIN C-III; CARNITINE; ENERGY METABOLISM; FATTY ACIDS; LIVER; MALE; MITOCHONDRIA, LIVER; MITOCHONDRIAL UNCOUPLING PROTEINS; OXIDATION-REDUCTION; RATS; RATS, WISTAR; TRIGLYCERIDES;

EID: 85021733192     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M074849     Document Type: Article

References (58)

1. Nichols, M., N. Townsend, R. Luengo-Fernandez, J. Leal, A. Gray, P. Scarborough, and M. Rayner. 2012. European Cardiovascular Disease Statistics. European Heart Network, Brussels, Belgium.
2. World Health Organization. 2016. Cardiovascular diseases (CVDs). Accessed December 4, 2016, at http://www.who.int/mediacentre/factsheets/fs317/en/.
3. Galassi, A., K. Reynolds, and J. He. 2006. Metabolic syndrome and risk of cardiovascular disease: a meta-analysis. Am. J. Med. 119: 812–819.
4. Mottillo, S., K. B. Filion, J. Genest, L. Joseph, L. Pilote, P. Poirier, S. Rinfret, E. L. Schiffrin, and M. J. Eisenberg. 2010. The metabolic syndrome and cardiovascular risk a systematic review and meta-analysis. J. Am. Coll. Cardiol. 56: 1113–1132.
5. Egeland, G. M., J. Igland, G. Sulo, O. Nygard, M. Ebbing, and G. S. Tell. 2015. Non-fasting triglycerides predict incident acute myocardial infarction among those with favourable HDL-cholesterol: Cohort Norway. Eur. J. Prev. Cardiol. 22: 872–881.
6. Brunzell, J. D., and J. E. Hokanson. 1999. Low-density and high-density lipoprotein subspecies and risk for premature coronary artery disease. Am. J. Med. 107: 16S–18S.
7. Wadhera, R. K., D. L. Steen, I. Khan, R. P. Giugliano, and J. M. Foody. 2016. A review of low-density lipoprotein cholesterol, treatment strategies, and its impact on cardiovascular disease morbidity and mortality. J. Clin. Lipidol. 10: 472–489.
8. Huang, P. L. 2009. A comprehensive definition for metabolic syndrome. Dis. Model. Mech. 2: 231–237.
9. Jong, M. C., M. H. Hofker, and L. M. Havekes. 1999. Role of ApoCs in lipoprotein metabolism: functional differences between ApoC1, ApoC2, and ApoC3. Arterioscler. Thromb. Vasc. Biol. 19: 472–484.
10. Ito, Y., N. Azrolan, A. O’Connell, A. Walsh, and J. L. Breslow. 1990. Hypertriglyceridemia as a result of human apo CIII gene expression in transgenic mice. Science. 249: 790–793.
11. Cohn, J. S., M. Tremblay, R. Batal, H. Jacques, C. Rodriguez, G. Steiner, O. Mamer, and J. Davignon. 2004. Increased apoC-III production is a characteristic feature of patients with hypertriglyceridemia. Atherosclerosis. 177: 137–145.
12. Maeda, N., H. Li, D. Lee, P. Oliver, S. H. Quarfordt, and J. Osada. 1994. Targeted disruption of the apolipoprotein C-III gene in mice results in hypotriglyceridemia and protection from postprandial hypertriglyceridemia. J. Biol. Chem. 269: 23610–23616.
13. Sacks, F. M., P. Alaupovic, L. A. Moye, T. G. Cole, B. Sussex, M. J. Stampfer, M. A. Pfeffer, and E. Braunwald. 2000. VLDL, apolipo-proteins B, CIII, and E, and risk of recurrent coronary events in the Cholesterol and Recurrent Events (CARE) trial. Circulation. 102: 1886–1892.
14. Bedogni, G., and S. Bellentani. 2004. Fatty liver: how frequent is it and why? Ann. Hepatol. 3: 63–65.
15. Paschos, P., and K. Paletas. 2009. Non alcoholic fatty liver disease and metabolic syndrome. Hippokratia. 13: 9–19.
16. Wei, Y., R. S. Rector, J. P. Thyfault, and J. A. Ibdah. 2008. Nonalcoholic fatty liver disease and mitochondrial dysfunction. World J. Gastroenterol. 14: 193–199.
17. Tronstad, K. J., M. Nooteboom, L. I. Nilsson, J. Nikolaisen, M. Sokolewicz, S. Grefte, I. K. Pettersen, S. Dyrstad, F. Hoel, P. H. Willems, et al. 2014. Regulation and quantification of cellular mitochondrial morphology and content. Curr. Pharm. Des. 20: 5634–5652.
18. Paradies, G., V. Paradies, F. M. Ruggiero, and G. Petrosillo. 2014. Oxidative stress, cardiolipin and mitochondrial dysfunction in nonalcoholic fatty liver disease. World J. Gastroenterol. 20: 14205–14218.
19. Grav, H. J., K. J. Tronstad, O. A. Gudbrandsen, K. Berge, K. E. Fladmark, T. C. Martinsen, H. Waldum, H. Wergedahl, and R. K. Berge. 2003. Changed energy state and increased mitochondrial beta-oxidation rate in liver of rats associated with lowered proton electrochemical potential and stimulated uncoupling protein 2 (UCP-2) expression: evidence for peroxisome proliferator-activated receptor-alpha independent induction of UCP-2 expression. J. Biol. Chem. 278: 30525–30533.
20. Raspé, E., L. Madsen, A. M. Lefebvre, I. Leitersdorf, L. Gelman, J. Peinado-Onsurbe, J. Dallongeville, J. C. Fruchart, R. Berge, and B. Staels. 1999. Modulation of rat liver apolipoprotein gene expression and serum lipid levels by tetradecylthioacetic acid (TTA) via PPARalpha activation. J. Lipid Res. 40: 2099–2110.
21. Urbaniak, G. C., and S. Plous. 2013. Research Randomizer. Accessed March 9, 2015, at https://www.randomizer.org/.
22. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37: 911–917.
23. Vernez, L., M. Wenk, and S. Krahenbuhl. 2004. Determination of carnitine and acylcarnitines in plasma by high-performance liquid chromatography/electrospray ionization ion trap tandem mass spectrometry. Rapid Commun. Mass Spectrom. 18: 1233–1238.
24. Vigerust, N. F., P. Bohov, B. Bjorndal, R. Seifert, O. Nygard, A. Svardal, D. Glintborg, R. K. Berge, and M. Gaster. 2012. Free carnitine and acylcarnitines in obese patients with polycystic ovary syndrome and effects of pioglitazone treatment. Fertil. Steril. 98: 1620–1626.e1.
25. Fürst, W., and S. Hallström. 1992. Simultaneous determination of myocardial nucleotides, nucleosides, purine bases and creatine phosphate by ion-pair high-performance liquid chromatography. J. Chromatogr. 578: 39–44.
26. Hallström, S., H. Gasser, C. Neumayer, A. Fügl, J. Nanobashvili, A. Jakubowski, I. Huk, G. Schlag, and T. Malinski. 2002. S-nitroso human serum albumin treatment reduces ischemia/reperfusion injury in skeletal muscle via nitric oxide release. Circulation. 105: 3032–3038.
27. Pelzmann, B., S. Hallstrom, P. Schaffer, P. Lang, K. Nadlinger, G. D. Birkmayer, K. Vrecko, G. Reibnegger, and B. Koidl. 2003. NADH supplementation decreases pinacidil-primed I K ATP in ventricular cardiomyocytes by increasing intracellular ATP. Br. J. Pharmacol. 139: 749–754.
28. Berge, R. K., T. Flatmark, and H. Osmundsen. 1984. Enhancement of long-chain acyl-CoA hydrolase activity in peroxisomes and mitochondria of rat liver by peroxisomal proliferators. Eur. J. Biochem. 141: 637–644.
29. Willumsen, N., S. Hexeberg, J. Skorve, M. Lundquist, and R. K. Berge. 1993. Docosahexaenoic acid shows no triglyceride-lowering effects but increases the peroxisomal fatty acid oxidation in liver of rats. J. Lipid Res. 34: 13–22.
30. Bremer, J. 1981. The effect of fasting on the activity of liver carnitine palmitoyltransferase and its inhibition by malonyl-CoA. Biochim. Biophys. Acta. 665: 628–631.
31. Clinkenbeard, K. D., W. D. Reed, R. A. Mooney, and M. D. Lane. 1975. Intracellular localization of the 3-hydroxy-3-methylglutaryl co-enzme A cycle enzymes in liver. Separate cytoplasmic and mitochondrial 3-hydroxy-3-methylglutaryl coenzyme A generating systems for cholesterogenesis and ketogenesis. J. Biol. Chem. 250: 3108–3116.
32. Stadlmann, S., K. Renner, J. Pollheimer, P. L. Moser, A. G. Zeimet, F. A. Offner, and E. Gnaiger. 2006. Preserved coupling of oxidative phosphorylation but decreased mitochondrial respiratory capacity in IL-1beta-treated human peritoneal mesothelial cells. Cell Biochem. Biophys. 44: 179–186.
33. Srere, P. A., L. Gonen, and H. Brazil. 1963. The citrate condensing enzyme of pigeon breast muscle and moth flight muscle. Acta Chem. Scand. 17: S129–S134.
34. Roncari, D. A. 1981. Fatty acid synthase from human liver. Methods Enzymol. 71: 73–79.
35. Tanabe, T., S. Nakanishi, T. Hashimoto, H. Ogiwara, J. Nikawa, and S. Numa. 1981. Acetyl-CoA carboxylase from rat liver. Methods Enzymol. 71: 5–16.
36. Kim, Y. S., and P. E. Kolattukudy. 1978. Malonyl-CoA decarboxylase from the uropygial gland of waterfowl: purification, properties, immunological comparison, and role in regulating the synthesis of mul-timethyl-branched fatty acids. Arch. Biochem. Biophys. 190: 585–597.
37. Raaka, B. M., and J. M. Lowenstein. 1979. Inhibition of fatty acid oxidation by 2-bromooctanoate. Evidence for the enzymatic formation of 2-bromo-3-ketooctanoyl coenzyme A and the inhibition of 3-ketothiolase. J. Biol. Chem. 254: 6755–6762.
38. Stern, J. R., M. J. Coon, A. Del Campillo, and M. C. Schneider. 1956. Enzymes of fatty acid metabolism. IV. Preparation and properties of coenzyme A transferase. J. Biol. Chem. 221: 15–31.
39. Williamson, D. H., M. W. Bates, M. A. Page, and H. A. Krebs. 1971. Activities of enzymes involved in acetoacetate utilization in adult mammalian tissues. Biochem. J. 121: 41–47.
40. Hagland, H. R., L. I. Nilsson, L. Burri, J. Nikolaisen, R. K. Berge, and K. J. Tronstad. 2013. Induction of mitochondrial biogenesis and respiration is associated with mTOR regulation in hepatocytes of rats treated with the pan-PPAR activator tetradecylthioacetic acid (TTA). Biochem. Biophys. Res. Commun. 430: 573–578.
41. He, L., P. F. Chinnery, S. E. Durham, E. L. Blakely, T. M. Wardell, G. M. Borthwick, R. W. Taylor, and D. M. Turnbull. 2002. Detection and quantification of mitochondrial DNA deletions in individual cells by real-time PCR. Nucleic Acids Res. 30: e68.
42. Hodneland Nilsson, L. I., I. K. Nitschke Pettersen, J. Nikolaisen, D. Micklem, H. Avsnes Dale, G. Vatne Rosland, J. Lorens, and K. J. Tronstad. 2015. A new live-cell reporter strategy to simultaneously monitor mitochondrial biogenesis and morphology. Sci. Rep. 5: 17217.
43. Zhao, W. S., S. L. Hu, K. Yu, H. Wang, W. Wang, J. Loor, and J. Luo. 2014. Lipoprotein lipase, tissue expression and effects on genes related to fatty acid synthesis in goat mammary epithelial cells. Int. J. Mol. Sci. 15: 22757–22771.
44. Hussain, M. M., N. Nijstad, and L. Franceschini. 2011. Regulation of microsomal triglyceride transfer protein. Clin. Lipidol. 6: 293–303.
45. Pan, X., and M. M. Hussain. 2007. Diurnal regulation of microsomal triglyceride transfer protein and plasma lipid levels. J. Biol. Chem. 282: 24707–24719.
46. Tyagi, S., P. Gupta, A. S. Saini, C. Kaushal, and S. Sharma. 2011. The peroxisome proliferator-activated receptor: a family of nuclear receptors role in various diseases. J. Adv. Pharm. Technol. Res. 2: 236–240.
47. Burri, L., G. H. Thoresen, and R. K. Berge. 2010. The role of PPARalpha activation in liver and muscle. PPAR Res. 2010: 542359.
48. Burri, L., B. Bjorndal, H. Wergedahl, K. Berge, P. Bohov, A. Svardal, and R. K. Berge. 2011. Tetradecylthioacetic acid increases hepatic mitochondrial beta-oxidation and alters fatty acid composition in a mouse model of chronic inflammation. Lipids. 46: 679–689.
49. Makowski, L., R. C. Noland, T. R. Koves, W. Xing, O. R. Ilkayeva, M. J. Muehlbauer, R. D. Stevens, and D. M. Muoio. 2009. Metabolic profiling of PPARalpha-/- mice reveals defects in carnitine and amino acid homeostasis that are partially reversed by oral carnitine supplementation. FASEB J. 23: 586–604.
50. Berge, R. K., K. J. Tronstad, K. Berge, T. H. Rost, H. Wergedahl, O. A. Gudbrandsen, and J. Skorve. 2005. The metabolic syndrome and the hepatic fatty acid drainage hypothesis. Biochimie. 87: 15–20.
51. Stone, S. J., H. M. Myers, S. M. Watkins, B. E. Brown, K. R. Feingold, P. M. Elias, and R. V. Farese, Jr. 2004. Lipopenia and skin barrier abnormalities in DGAT2-deficient mice. J. Biol. Chem. 279: 11767–11776.
52. Stone, S. J., M. C. Levin, P. Zhou, J. Han, T. C. Walther, and R. V. Farese, Jr. 2009. The endoplasmic reticulum enzyme DGAT2 is found in mitochondria-associated membranes and has a mitochondrial targeting signal that promotes its association with mitochondria. J. Biol. Chem. 284: 5352–5361.
53. Kuerschner, L., C. Moessinger, and C. Thiele. 2008. Imaging of lipid biosynthesis: how a neutral lipid enters lipid droplets. Traffic. 9: 338–352.
54. Dominy, J. E., and P. Puigserver. 2013. Mitochondrial biogenesis through activation of nuclear signaling proteins. Cold Spring Harb. Perspect. Biol. 5: a015008.
55. Taanman, J. W. 1999. The mitochondrial genome: structure, transcription, translation and replication. Biochim. Biophys. Acta. 1410: 103–123.
56. Garstka, H. L., W. E. Schmitt, J. Schultz, B. Sogl, B. Silakowski, A. Perez-Martos, J. Montoya, and R. J. Wiesner. 2003. Import of mitochondrial transcription factor A (TFAM) into rat liver mitochondria stimulates transcription of mitochondrial DNA. Nucleic Acids Res. 31: 5039–5047.
57. Mrácek, T., Z. Drahota, and J. Houštek. 2013. The function and the role of the mitochondrial glycerol-3-phosphate dehydrogenase in mammalian tissues. Biochim. Biophys. Acta. 1827: 401–410.
58. Hardie, D. G. 2014. AMPK–sensing energy while talking to other signaling pathways. Cell Metab. 20: 939–952.