Dietary fatty acid composition and the homeostatic regulation of mitochondrial phospholipid classes in red muscle of rainbow trout (Oncorhynchus mykiss)

Journal of Experimental Zoology Part A: Ecological Genetics and Physiology

Volumn 323, Issue 1, 2015, Pages 60-71

  Martin, Nicolas ^a,b,e   Kraffe, Edouard ^b,f   Le Grand, Fabienne ^b   Marty, Yanic ^c   Bureau, Dominique P ^d   Guderley, Helga ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b INSTITUT UNIVERSITAIRE EUROPÉEN DE LA MER   (France)

^c UNIVERSITÉ DE BRETAGNE OCCIDENTALE   (France)

^d UNIVERSITY OF GUELPH   (Canada)

^e UNIVERSITY OF WOLLONGONG   (Australia)

^f CENTRO DE INVESTIGACIONES BIOLÓGICAS DEL NOROESTE   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

ONCORHYNCHUS MYKISS; SALMONIDAE;

FATTY ACID; PHOSPHOLIPID;

ANIMAL; DIET; HOMEOSTASIS; METABOLISM; MITOCHONDRIAL MEMBRANE; MUSCLE; MUSCLE MITOCHONDRION; RAINBOW TROUT; SLOW MUSCLE FIBER; TEMPERATURE;

ANIMALS; DIET; FATTY ACIDS; HOMEOSTASIS; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL MEMBRANES; MUSCLE FIBERS, SLOW-TWITCH; MUSCLES; ONCORHYNCHUS MYKISS; PHOSPHOLIPIDS; TEMPERATURE;

EID: 84916908772     PISSN: 19325223     EISSN: 19325231     Source Type: Journal    
DOI: 10.1002/jez.1896     Document Type: Article

References (64)

1. Abbott SK, Else PL, Hulbert AJ. 2010. Membrane fatty acid composition of rat skeletal muscle is most responsive to the balance of dietary n-3 and n-6 PUFA. Br J Nutr 103:522-529.
2. Abbott SK, Else PL, Atkins TA, Hulbert AJ. 2012. Fatty acid composition of membrane bilayers: importance of diet polyunsaturated fat balance. Biochim Biophys Acta 1818:1309-1317.
3. Astorg PO, Chevalier J. 1991. Phospholipid fatty acid composition and respiratory properties of heart and liver mitochondria from rats fed with or deprived of linolenic acid. Nutr Res 11:71-77.
4. Beyer K, Nuscher B. 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.
5. Daum G. 1985. Lipids of mitochondria. Biochim Biophys Acta 822:1-42.
6. Demaison L, Sergiel JP, Moreau D, Grynberg A. 1994. Influence of the phospholipid n-6/n-3 polyunsaturated fatty acid ratio on the mitochondrial oxidative metabolism before and after myocardial ischemia. Biochim Biophys Acta 1227:53-59.
7. Drose S, Zwicker K, Brandt U. 2002. Full recovery of the NADH:ubiquinone activity of complex I NADH: ubiquinone oxidoreductase from Yarrowia lipolytica by the addition of phospholipids. Biochim Biophys Acta 1556:65-72.
8. Eble KS, Coleman WB, Hantgan RR, Cunningham CC. 1990. Tightly associated cardiolipin in the bovine heart mitochondrial ATP synthase as analyzed by p31 nuclear magnetic resonance spectroscopy. J Biol Chem 265:19434-19440.
9. 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.
10. Frick NT, Bystriansky JS, Ip YK, Chew SF, Ballantyne JS. 2010. Cytochrome c oxidase is regulated by modulations in protein expression and mitochondrial membrane phospholipid composition in estivating African lungfish. Am J Physiol 298:R608-R616.
11. Fry M, Blondin GA, Green DE. 1980. The localization of tightly bound cardiolipin in cytochrome oxidase. J Biol Chem 255:9967-9970.
12. Gillis TE, Ballantyne JS. 1999. Influences of subzero thermal acclimation on mitochondrial membrane composition of temperate zone marine bivalve mollusks. Lipids 34:59-66.
13. Glémet HC, Gerrits MF, Ballantyne JS. 1997. Membrane lipids of red muscle mitochondria from land-locked and sea-run Arctic char, Salvelinus alpinus. Mar Biol 129:673-679.
14. Gohil VM, Hayes P, Matsuyama S, et al. 2004. Cardiolipin biosynthesis and mitochondrial respiratory chain function are interdependent. J Biol Chem 279:42612-42618.
15. Gomez BJr, Robinson NC. 1999. Phospholipase digestion of bound cardiolipin reversibly inactivates bovine cytochrome bc1. Biochemistry 38:9031-9038.
16. Guderley H. 2004. Metabolic response to low temperature in fish muscle. Biol Rev 79:409-427.
17. Guderley H, Kraffe E, Bureau W, Bureau DP. 2008. Dietary fatty acid composition changes mitochondrial phospholipids and oxidative capacities in rainbow trout red muscle. J Comp Physiol B 178:385-399.
18. Hagopian K, Weber KL, Hwee DT, et al. 2010. Complex I associated hydrogen peroxide production is decreased and electron transport chain enzyme activities are altered in n-3 enriched fat-1 mice. PLoS ONE 59:e12696. doi: 10.1371/journal.pone.
19. Haines TH, Dencher NA. 2002. Cardiolipin: a proton trap for oxidative phosphorylation. FEBS Letters 528:35-39.
20. Hazel JR. 1995. Thermal adaptation in biological membranes is homeoviscous adaptation the explanation. Annu Rev Physiol 57:19-42.
21. Hazel JR, Carpenter R. 1985. Rapid changes in the phospholipid composition of gill membranes during thermal acclimation of the rainbow trout, Salmo gairdneri. J Comp Physiol B 155:597-602.
22. Hazel JR, Landrey SR. 1988a. Time course of thermal adaptation in plasma membranes of trout kidney I: headgroup composition. Am J Physiol 255:R622-R627.
23. Hazel JR, Landrey SR. 1988b. Time course of thermal adaptation in plasma membranes of trout kidney II: molecular species composition. Am J Physiol 255:R628-R634.
24. Horvath SE, Daum G. 2013. Lipids of mitochondria. Prog Lipid Res 52:590-614.
25. Hulbert AJ. 2010. Metabolism and longevity: is there a role for membrane fatty acids. Integr Comp Biol 50:808-817.
26. Hulbert AJ, Else PL. 1999. Membranes as possible pacemakers of metabolism. J Theor Biol 199:257-274.
27. Hulbert AJ, Turner N, Storlien LH, Else P. 2005. Dietary fats and membrane function: implications for metabolism and disease. Biol Rev 80:155-169.
28. Innis SM, Clandinin MT. 1981. Dynamic modulation of mitochondrial membrane physical properties and ATPase activity by diet lipid. Biochem J 198:167-175.
29. Javouhey A, Rocquelin G, Rochette L, Juanèla P. 1990. Comparative effects of equivalent intakes of 18:3n-3 and of marine n-3 fatty acids on rat cardiac phospholipid contents and fatty acid compositions. Nutr Res 10:291-301.
30. Khairallah RJ, Kim J, O'Shea KM, et al. 2012. Improved mitochondrial function with diet-induced increase in either docosahexaenoic acid or arachidonic acid in membrane phospholipids. PLoS ONE 7:e34402. doi: 10.1371/journal.pone.0034402.
31. Klingenberg M. 2009. Cardiolipin and mitochondrial carriers. Biochim Biophys Acta 1788:2048-2058.
32. Kraffe E, Marty Y, Guderley H. 2007. Changes in mitochondrial oxidative capacities during thermal acclimation of rainbow trout Oncorhynchus mykiss: roles of membrane proteins, phospholipids and their fatty acid compositions. J Exp Biol 210:149-165.
33. Kraffe E, Tremblay R, Belvin S, LeCoz JR, Marty Y, Guderley H. 2008. Effect of reproduction on escape responses, metabolic rates and muscle mitochondrial properties in the scallop Placopecten magellanicus. Mar Biol 156:25-38.
34. Krämer R, Klingenberg M. 1980. Modulation of the reconstituted adenine nucleotide exchange by membrane potential. Biochemistry 193:556-560.
35. 1 ATPase. J Biol Chem 261:4851-4856.
36. Lange C, Nett JH, Trumpower BL, Hunte C. 2001. Specific roles of protein phospholipid interactions in the yeast cytochrome bc1 complex structure. EMBO J 20:6591-6600.
37. Le Grand F, Soudant P, Marty Y, Le Goìc N, Kraffe E. 2013. Altered membrane lipid composition and functional parameters of circulating cells in cockles (Cerastoderma edule) affected by disseminated neoplasia. Chem Phys Lipids 168:9-20.
38. Lemieux H, Blier PU, Tardif JC. 2008. Does membrane fatty acid composition modulate mitochondrial functions and their thermal sensitivities. Comp Biochem Physiol A 149:20-29.
39. Logue JA, De Vries AL, Fodor E, Cossins AR. 2000. Lipid compositional correlates of temperature adaptive interspecific differences in membrane physical structure. J Exp Biol 203:2105-2115.
40. Mak IT, Shrago E, Elson CE. 1983. Effect of thyroidectomy on the kinetics of ADP ATP translocation in liver mitochondria. Arch Biochem Biophys 2261:317-323.
41. Malis CD, Weber PC, Leaf A, Bonventre JV. 1990. Incorporation of marine lipids into mitochondrial membranes increases susceptibility to damage by calcium and reactive oxygen species: evidence for enhanced activation of phospholipase A2 in mitochondria enriched with n-3 fatty acids. Proc Nati Acad Sci USA 87:8845-8849.
42. Martin N, Bureau DP, Marty Y, Kraffe E, Guderley H. 2013. Dietary lipid quality and mitochondrial membrane composition in trout: responses of membrane enzymes and oxidative capacities. J Comp Physiol B 1833:393-408.
43. Marty Y, Delaunay F, Moal J, Samain JF. 1992. Changes in the fatty acid composition of Pecten maximus during larval development. J Exp Mar Biol Ecol 163:221-234.
44. McMillin JB, Bick RJ, Benedict CR. 1992. Influence of dietary fish oil on mitochondrial function and response to ischemia. Am J Physiol 263:H1479-H1485.
45. McMurchie EJ, Abeywardena MY, Charnock JS, Gibson RA. 1983. Differential modulation of rat heart mitochondrial membrane associated enzymes by dietary lipid. Biochim Biophys Acta 760:13-24.
46. Milke LM, Bricelj VM, Parrish CC. 2006. Comparison of early life history stages of the bay scallop, Argopecten irradians: effects of microalgal diets on growth and biochemical composition. Aquaculture 260:272-289.
47. Morash AJ, Bureau DP, McClelland GB. 2009. Effects of dietary fatty acid composition on the regulation of carnitine palmitoyltransferase CPT I in rainbow trout Oncorhynchus mykiss. Comp Biochem Physiol B 152:85-93.
48. Paradies G, Ruggiero FM, Petrosillo G, Quagliariello E. 1994. Enhanced cytochrome oxidase activity and modification of lipids in heart mitochondria from hyperthyroid rats. Biochim Biophys Acta 1225:165-170.
49. Paradies G, Petrosillo G, Pistolese M, Ruggiero FM. 2002. Reactive oxygen species affect mitochondrial electron transport complex I activity through oxidative cardiolipin damage. Gene 286:135-141.
50. Paradies G, Petrosillo G, Paradies V, Ruggiero FM. 2011. Mitochondrial dysfunction in brain aging: role of oxidative stress and cardiolipin. Neurochem Int 58:447-457.
51. Phillips R, Ursell T, Wiggins P, Sens P. 2009. Emerging roles for lipids in shaping membrane protein function. Nature 459:379-385.
52. Robinson NC, Zborowski J, Talbert LH. 1990. Cardiolipin depleted bovine heart cytochrome c oxidase: binding stoichiometry and affinity for cardiolipin derivatives. Biochem 29:8962-8969.
53. Rohrbach S. 2009. Effects of dietary polyunsaturated fatty acids on mitochondria. Curr Pharm Des 15:4103-4116.
54. Schlame M, Hostetler KY. 1992. Mammalian cardiolipin biosynthesis. Meth Enzymol 209:330-337.
55. Sedlák E, Robinson NC. 1999. Phospholipase A2 digestion of cardiolipin bound to bovine cytochrome c oxidase alters both activity and quaternary structure. Biochemistry 38:14966-14972.
56. Sharpley MS, Shannon RJ, Draghi F, Hirst J. 2006. Interactions between phospholipids and NADH: ubiquinone oxidoreductase complex I from bovine mitochondria. Biochemistry 45:241-248.
57. Shinzawa-Itoh K, Aoyama H, Muramoto K, et al. 2007. Structures and physiological roles of 13 integral lipids of bovine heart cytochrome c oxidase. EMBO J 26:1713-1725.
58. Stillwell W, Jenski LJ, Crump FT, Ehringer W. 1997. Effect of docosahexanoic acid on mouse mitochondrial membrane properties. Lipids 32:497-506.
59. Stuart JA, Gillis TE, Ballantyne JS. 1998. Compositional correlates of metabolic depression in the mitochondrial membranes of estivating snails. Am J Physiol 275:1977-1982.
60. Tocher DR, Carr J, Sargent JR. 1989. Polyunsaturated fatty acid metabolism in fish cells: differential metabolism of n-3 and n-6 series acids by cultured cells originating from a fresh water teleost fish and from marine teleost fish. Comp Biochem Physiol B 94:367-374.
61. Wu BJ, Hulbert AJ, Storlien LH, Else PL. 2004. Membrane lipids and sodium pumps of cattle and crocodiles: an experimental test of the membrane pacemaker theory of metabolism. Am J Physiol 287:R633-R641.
62. Wodtke E. 1981. Temperature adaptation of biological membranes: the effects of acclimation temperature on the unsaturation of the main neutral and charged phospholipids in mitochondrial membranes of the carp Cyprinus carpio. Biochim Biophys Acta 640:698-709.
63. Yamaoka S, Urade R, Makoto K. 1988. Mitochondrial function in rats is affected by modification of membrane phospholipids with dietary sardine oil. J Nutr 118:290-296.
64. Zhou M, Morgner N, Barrera NP, et al. 2011. Mass spectrometry of intact V type ATPases reveals bound lipids and the effects of nucleotide binding. Science 334:380-385.