Dietary macronutrients modulate the fatty acyl composition of rat liver mitochondrial cardiolipins

Journal of Lipid Research

Volumn 54, Issue 10, 2013, Pages 2623-2635

  Stavrovskaya, Irina G ^a   Bird, Susan S ^a   Marur, Vasant R ^a   Sniatynski, Matthew J ^a   Baranov, Sergei V ^a,b   Greenberg, Heather K ^a   Porter, Caryn L ^a   Kristal, Bruce S ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b PRESBYTERIAN UNIVERSITY HOSPITAL   (United States)

Author keywords

Glycemic index; Lipidomics; Mitochondria; Monounsaturated fatty acids; Polyunsaturated fatty acids; Saturated fatty acids; Trans fatty acids; Ubiquinones

Indexed keywords

CARDIOLIPIN; FATTY ACID; GLYCEROPHOSPHOLIPID; MONOLYSOCARDIOLIPIN; PHOSPHORYLCHOLINE; UBIQUINONE; UBIQUINONE Q9; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARBOHYDRATE INTAKE; CONTROLLED STUDY; DIETARY INTAKE; FAT INTAKE; GROWTH RATE; LIPID COMPOSITION; LIVER MITOCHONDRION; MACRONUTRIENT; MALE; METABOLIC REGULATION; MITOCHONDRIAL RESPIRATION; NONHUMAN; PHOSPHOLIPID SYNTHESIS; PRIORITY JOURNAL; RAT;

GLYCEMIC INDEX; LIPIDOMICS; MITOCHONDRIA; MONOUNSATURATED FATTY ACIDS; POLYUNSATURATED FATTY ACIDS; SATURATED FATTY ACIDS; TRANS FATTY ACIDS; UBIQUINONES;

ANIMALS; CARDIOLIPINS; CELL RESPIRATION; DIET; FATTY ACIDS, OMEGA-3; FATTY ACIDS, OMEGA-6; GLYCEMIC INDEX; LIVER; MALE; MITOCHONDRIA, LIVER; OXIDATIVE STRESS; OXYGEN CONSUMPTION; RATS; UBIQUINONE;

EID: 84884131036     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M036285     Document Type: Article

References (71)

1. Ioannou, P. V., and B. T. Golding. 1979. Cardiolipins: their chemistry and biochemistry. Prog. Lipid Res. 17: 279-318.
2. Hoch, F. L. 1992. Cardiolipins and biomembrane function. Biochim. Biophys. Acta. 1113: 71-133.
3. Schlame, M., D. Rua, and M. L. Greenberg. 2000. The biosynthesis and functional role of cardiolipin. Prog. Lipid Res. 39: 257-288.
4. Schlame, M., and D. Otten. 1991. Analysis of cardiolipin molecular species by high-performance liquid chromatography of its derivative 1,3-bisphosphatidyl-2-benzoyl-sn-glycerol dimethyl ester. Anal. Biochem. 195: 290-295.
5. Schlame, M., M. Ren, Y. Xu, M. L. Greenberg, and I. Haller. 2005. Molecular symmetry in mitochondrial cardiolipins. Chem. Phys. Lipids. 138: 38-49.
6. Robinson, N. C. 1993. Functional binding of cardiolipin to cytochrome c oxidase. J. Bioenerg. Biomembr. 25: 153-163.
7. Schlame, M., and W. Rustow. 1990. Lysocardiolipin formation and reacylation in isolated rat liver mitochondria. Biochem. J. 272: 589-595.
8. 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.
9. Schlame, M., and M. Ren. 2009. The role of cardiolipin in the structural organization of mitochondrial membranes. Biochim. Biophys. Acta. 1788: 2080-2083.
10. Claypool, S. M., and C. M. Koehler. 2012. The complexity of cardiolipin in health and disease. Trends Biochem. Sci. 37: 32-41.
11. Fry, M., and D. E. Green. 1980. Cardiolipin requirement by cytochrome oxidase and the catalytic role of phospholipid. Biochem. Biophys. Res. Commun. 93: 1238-1246.
12. Fry, M., and D. E. Green. 1981. Cardiolipin requirement for electron transfer in complex I and III of mitochondrial respiratory chain. J. Biol. Chem. 256: 1874-1880.
13. Eble, K. S., W. B. Coleman, R. R. Hantgan, and C. C. Cunningham. 1990. Tightly associated cardiolipin in the bovine heart mitochondrial ATP synthase as analyzed by 31P nuclear magnetic resonance spectroscopy. J. Biol. Chem. 265: 19434-19440.
14. Hoch, F. L. 1998. Cardiolipins and mitochondrial proton-selective leakage. J. Bioenerg. Biomembr. 30: 511-532.
15. Claypool, S. M. 2009. Cardiolipin, a critical determinant of mitochondrial carrier protein assembly and function. Biochim. Biophys. Acta. 1788: 2059-2068.
16. Zhang, M., E. Mileykovskaya, and W. Dowhan. 2002. Gluing the respiratory chain together. Cardiolipin is required for supercomplexes formation in the inner mitochondrial membrane. J. Biol. Chem. 277: 43553-43556.
17. Pfeiffer, K., V. Gohil, R. A. Stuart, C. Hunte, U. Brandt, M. L. Greenberg, and H. Schagger. 2003. Cardiolipin stabilizes respiratory chain supracomplexes. J. Biol. Chem. 278: 52873-52880.
18. Klingenberg, M. 2009. Cardiolipin and mitochondrial carriers. Biochim. Biophys. Acta. 1788: 2048-2058.
19. Acehan, D., A. Malhotra, Y. Xu, M. Ren, D. L. Stokes, and M. Schlame. 2011. Cardiolipin affects the supramolecular organization of ATP synthase in mitochondria. Biophys. J. 100: 2184-2192.
20. Schlame, M., and K. Y. Hostetler. 1991. Solubilization, purification, and characterization of cardiolipin synthase from rat liver mitochondria. Demonstration of its phospholipid requirement. J. Biol. Chem. 266: 22398-22403.
21. Beyer, K., and B. Nuscher. 1996. Specific cardiolipin binding interferes with labeling of sulfhydryl residues in the adenosine diphosphate/adenosine triphosphate carrier protein from beef heart mitochondria. Biochemistry. 35: 15784-15790.
22. Kadenbach, B., P. Mende, H. V. Kolbe, I. Stipani, and F. Palmieri. 1982. The mitochondrial phosphate carrier has an essential requirement for cardiolipin. FEBS Lett. 139: 109-112.
23. Nałecz, K. A., R. Bolli, L. Wojtczak, and A. Azzi. 1986. The monocarboxylate carrier from bovine heart mitochondria: partial purifi- cation and its substrate-transporting properties in a reconstituted system. Biochim. Biophys. Acta. 851: 29-37.
24. Noël, H., and S. V. Pande. 1986. An essential requirement of cardiolipin for mitochondrial carnitine acylcarnitine translocase activity. Lipid requirement of carnitine acylcarnitine translocase. Eur. J. Biochem. 155: 99-102.
25. Müller, M., D. Cheneval, and E. Carafoli. 1986. The mitochondrial creatine phosphokinase is associated with inner mitochondrial membrane cardiolipin. Adv. Exp. Med. Biol. 194: 151-156.
26. Ott, M., J. D. Robertson, V. Gogvadze, B. Zhivotovsky, and S. Orrenius. 2002. Cytochrome c release from mitochondria proceeds by a two-step process. Proc. Natl. Acad. Sci. USA. 99: 1259-1263.
27. Koshkin, V., and M. L. Greenberg. 2002. Cardiolipin prevents ratedependent uncoupling and provides osmotic stability in yeast mitochondria. Biochem. J. 364: 317-322.
28. Hauff, K. D., and G. M. Hatch. 2006. Cardiolipin metabolism and Barth syndrome. Prog. Lipid Res. 45: 91-101.
29. Schlame, M., and M. Ren. 2006. Barth syndrome, a human disorder of cardiolipin metabolism. FEBS Lett. 580: 5450-5455.
30. Lesnefsky, E. J., P. Minkler, and C. L. Hoppel. 2009. Enhanced modification of cardiolipin during ischemia in the aged heart. J. Mol. Cell. Cardiol. 46: 1008-1015.
31. Ji, J ., A. E. Kline, A. Amoscato, A. K. Samhan-Arias, L. J. Sparvero, V. A. Tyurin, Y. Y. Tyurina, B. Fink, M. D. Manole, A. M. Puccio, et al. 2012. Lipidomics identifies cardiolipin as a mitochondrial target for redox therapy of brain injury. Nat. Neurosci. 15: 1407-1413.
32. Sparagna, G. C., A. J. Chicco, R. C. Murphy, M. R. Bristow, C. A. Johnson, M. L. Rees, M. L. Maxey, S. A. McCune, and R. L. Moore. 2007. Loss of cardiac tetralinoleoyl cardiolipin in human and experimental heart failure. J. Lipid Res. 48: 1559-1570.
33. Moreira, P. I., M. S. Santos, A. M. Moreno, T. Proenca, R. Seica, and C. R. Oliveira. 2004. Effect of streptozotocin-induced diabetes on rat brain mitochondria. J. Neuroendocrinol. 16: 32-38.
34. Han, X., J. Yang, H. Cheng, K. Yang, D. R. Abendschein, and R. W. Gross. 2007. Alterations in myocardial cardiolipin content and composition occur at the very earliest stages of diabetes: a shotgun lipidomics study. Biochemistry. 46: 6417-6428.
35. Pepe, S., N. Tsuchiya, E. G. Lakatta, and R. G. Hansford. 1999. PUFA and aging modulate cardiac membrane mitochondrial composition and Ca2+ activation of PDH. Am. J. Physiol. 276: H149 - H158.
36. Lee, H. J., J. Mayette, S. I. Rapoport, and R. P. Bazinet. 2006. Selective remodeling of cardiolipin fatty acids in the aged rat heart. Lipids Health Dis. 5: 2.
37. Lesnefsky, E. J., and C. H. Hoppel. 2008. Cardiolipin as an oxidative target in cardiac mitochondria in the aged rat. Biochim. Biophys. Acta. 1777: 1020-1027.
38. Sparagna, G. C., and E. J. Lesnefsky. 2009. Cardiolipin remodeling in the heart. J. Cardiovasc. Pharmacol. 53: 290-301.
39. Blomstrand, R., and L. Svensson. 1983. The effect of partially hydrogenated marine oils on the mitochondrial function and membrane phospholipid fatty acids in rat heart. Lipids. 18: 151-170.
40. Berger, A., and J. B. German. 1990. Phospholipid fatty acid composition of various mouse tissues after feeding -linoleate or eicosatrienoate. Lipids. 25: 473-480.
41. Høy, C-E., and G. Holmer. 1990. Influence of dietary linoleic acid and trans fatty acids on the fatty acid profile of cardiolipins in rats. Lipids. 25: 455-459.
42. Berger, A., J. B. German, and M. E. Gershwin. 1992. Effect of various dietary fats on cardiolipin acyl composition during ontogeny of mice. Lipids. 27: 605-612.
43. Yamaoka, S., R. Urade, and M. Kito. 1988. Mitochondrial function in rats is affected by modification of membrane phospholipids with dietary sardine oil. J. Nutr. 118: 290-296.
44. Yamaoka, S., R. Urade, and M. Kito. 1990. Cardiolipin molecular species in rat heart mitochondria are sensitive to essential fatty acid-deficient dietary lipids. J. Nutr. 120: 415-421.
45. Yamaoka-Koseki, S., R. Urade, and M. Kito. 1991. Cardiolipins from rats fed different dietary lipids affect bovine heart cytochrome c oxidase activity. J. Nutr. 121: 956-958.
46. Valianpour, F., R. J. Wanders, H. Overmars, F. M. Vaz, P. G. Barth, and A. H. van Gennip. 2003. Linoleic acid supplementation of Barth syndrome fibroblasts restores cardiolipin levels: implication for treatment. J. Lipid Res. 44: 560-566.
47. Bird, S. S., V. R. Marur, M. J. Sniatynski, H. K. Greenberg, and B. S. Kristal. 2011. Lipidomics profiling by high-resolution LC-MS and high-energy collisional dissociation fragmentation: focus on characterization of mitochondrial cardiolipins and monolysocardiolipins. Anal. Chem. 83: 940-949.
48. Bird, S. S., V. R. Marur, I. G. Stavrovskaya, and B. S. Kristal. 2013. Qualitative characterization of the rat liver mitochondrial lipidome using LC-MS profiling and high energy collisional dissociation (HCD) all ion fragmentation. Metabolomics. 9 (1 Suppl.): 67-83.
49. Bird, S. S., V. R. Marur, I. G. Stavrovskaya, and B. S. Kristal. 2012. Separation of cis-trans phospholipid isomers using reverse phase LC with high resolution MC detection. Anal. Chem. 84: 5509-5517.
50. Kilkenny, C., W. Browne, I. C. Cuthill, M. Emerson, and D. G. Altman. 2010. Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br. J. Pharmacol. 160: 1577-1579.
51. Stavrovskaya, I. G., M. V. Narayanan, W. Zhang, B. F. Krasnikov, J. Heemskerk, S. S. Young, J. P. Blass, A. Brown, M. F. Beal, R. M. Friedlander, et al. 2004. Clinically-approved heterocyclics act on a mitochondrial target and reduce stroke-induced pathology. J. Exp. Med. 200: 211-222.
52. Krasnikov, B. F., D. B. Zorov, Y. N. Antonenko, A. A. Zaspa, I. V. Kulikov, B. S. Kristal, A. J. L. Cooper, and A. M. Brown. 2005. Comparative kinetic analysis reveals that inducer-specific ion release precedes the mitochondrial permeability transition. Biochim. Biophys. Acta. 1708: 375-392.
53. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37: 911-917.
54. Cequier-Sánchez, E., C. Rodríguez, A. G. Ravelo, and R. Zárate. 2008. Dichloromethane as a solvent for lipid extraction and assessment of lipid classes and fatty acids from samples of different natures. J. Agric. Food Chem. 56: 4297-4303.
55. Preacher, K. J. 2001. Calculation for the chi-square test: An interactive calculation tool for chi-square tests of goodness of fit and independence [Computer software]. Available from http://quantpsy. org.
56. Turunen, M., J. Olsson, and G. Dallner. 2004. Metabolism and function of coenzyme Q. Biochim. Biophys. Acta. 1660: 171-199.
57. Chatgilialoglu, C., D. Crich, M. Komatsu, and I. Ryu. 1999. Chemistry of acyl radicals. Chem. Rev. 99: 1991-2070.
58. Ma, B. J., W. A. Taylor, V. W. Dolinsky, and G. M. Hatch. 1999. Acylation of monolysocardiolipin in rat heart. J. Lipid Res. 40: 1837-1845.
59. Xu, Y., R. I. Kelley, J. J. Blanck, and M. Schlame. 2003. Remodeling of cardiolipin by phospholipid transacylation. J. Biol. Chem. 278: 51380-51385.
60. Wolff, L., and B. Entressangles. 1991. Compositional changes of fatty acids in the 1(1'')- and 2(2'')-positions of cardiolipin from liver, heart, and kidney mitochondria of rats fed low-fat diet. Biochim. Biophys. Acta. 1082: 136-142.
61. Lenaz, G. 2001. A critical appraisal for the mitochondrial coenzyme Q pool. FEBS Lett. 509: 151-155.
62. Aoun, M., G. Fouret, F. Michel, B. Bonafos, J. Ramos, J-P. Cristol, M-A. Carbonneau, C. Coudray, and C. Feillet-Coudray. 2012. Dietary fatty acids modulate liver mitochondrial cardiolipin content and its fatty acid composition in rats with non alcoholic fatty liver disease. J. Bioenerg. Biomembr. 44: 439-452.
63. Connerth, M., T. Tatsuta, M. Haag, T. Klecker, B. Westermann, and T. Langer. 2012. Intramitochondrial transport of phosphatidic acid in yeast by a lipid transfer protein. Science. 338: 815-818.
64. Malhotra, A., Y. Xu, M. Ren, and M. Schlame. 2009. Formation of molecular species of mitochondrial cardiolipin. 1. A novel transacylation mechanism to shuttle fatty acids between sn-1 and sn-2 positions of multiple phospholipid species. Biochim. Biophys. Acta. 1791: 321-325.
65. Xu, Y., A. Malhorta, M. Ren, and M. Schlame. 2006. The enzymatic function of tafazzin. J. Biol. Chem. 281: 39217-39224.
66. Taylor, W. A., and G. M. Hatch. 2009. Identification of the human mitochondrial linoleoyl-coenzyme A monolysocardiolipin acyltransferase (MLCL AT-1). J. Biol. Chem. 284: 30360-30371.
67. Kiebish, M. A., K. Yang, H. F. Sims, C. M. Jenkins, X. Liu, D. J. Mancuso, Z. Zhao, S. Guan, D. R. Abendschein, X. Han, et al. 2012. Myocardial regulation of lipidomic flux by cardiolipin synthase: setting the beat for bioenergetic efficiency. J. Biol. Chem. 287: 25086-25097.
68. Li, J., X. Liu, H. Wang, W. Zhang, D. C. Chan, and Y. Shi. 2012. Lysocardiolipin acyltransferase 1 (ALCAT1) controls mitochondrial DNA fidelity and biogenesis through modulation of MFN2 expression. Proc. Natl. Acad. Sci. USA. 109: 6975-6980.
69. Schlame, M. 2009. Formation of molecular species of mitochondrial cardiolipin 2. A mathematical model of pattern formation by phospholipid transacylation. Biochim. Biophys. Acta. 1791: 321-325.
70. Sparagna, G. C., C. A. Johnson, S. A. McCune, R. L. Moore, and R. C. Murphy. 2005. Quantitation of cardiolipin molecular species in spontaneously hypertensive heart failure rats using electrospray ionization mass spectrometry. J. Lipid Res. 46: 1196-1204.
71. Zhang, L., R. J. Bell, M. A. Kiebish, T. N. Seyfried, X. Han, R. W. Gross, and J. H. Chuang. 2011. A mathematical model for the determination of steady-state cardiolipin remodeling mechanisms using lipidomic data. PLoS ONE. 6: e21170.