Skip to main content
Log in

Cold acclimation or grapeseed oil feeding affects phospholipid composition and mitochondrial function in duckling skeletal muscle

  • Published:
Lipids

Abstract

The phospholipid fatty acid (FA) composition and functional properties of skeletal muscle and liver mitochondria were examined in cold-acclimated (CA, 4°C) ducklings. Phospholipid FA of isolated muscle mitochondria from CA birds were longer and more unsaturated than those from thermoneutral (TN, 25°C) reared ducklings. The rise in long-chain and polyunsaturated FA (PUFA, mainly 20∶4n-6) was associated with a higher State 4 respiration rate and a lower respiratory control ratio (RCR). Hepatic mitochondria, by contrast, were much less affected by cold acclimation. The cold-induced changes in phospholipid FA profile and functional properties of muscle mitochondria were reproduced by giving TN ducklings a diet enriched in grapeseed oil (GO, rich in n-6 FA), suggesting a causal relationship between the membrane structure and mitochondrial functional parameters. However, hepatic mitochondria from ducklings fed the GO diet also showed an enrichment in long-chain PUFA but opposite changes in their biochemical characteristics (lower State 4, higher RCR). It is suggested that the differential modulation of mitochondrial functional properties by membrane lipid composition between skeletal muscle and liver may depend on muscle-specific factors possibly interacting with long-chain PUFA and affecting the proton leakiness of mitochondrial membranes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

ANOVA:

analysis of variance

BAT:

brown adipose tissue

CA:

cold acclimated

FA:

fatty acid

FOG:

fast-oxidative glycolytic

GO:

grapeseed oil

MUFA:

monounsaturated fatty acid

NST:

nonshivering thermogenesis

PUFA:

polyunsaturated fatty acid

RCR:

respiratory control ratio

SFA:

saturated fatty acid

TN:

thermoneutral control duckling

U.A.R.:

Usine d'Alimentation Rationnelle

References

  1. Jansky, L. (1971) Participation of Body Organs During Nonshivering Heat Production, Biol. Rev. 48, 85–132.

    Google Scholar 

  2. ElHalawani, M.E., Wilson, W.D., and Burger, R.E. (1971) Cold Acclimation and the Role of Catecholamines in Body Temperature Regulation in Male Leghorns, Poult. Sci. 49, 621–632.

    Google Scholar 

  3. Barré, H., Nedergaard, J., and Cannon, B. (1986) Increased Respiration in Skeletal Muscle Mitochondria from Cold-Acclimated Ducklings: Uncoupling Effects of Free Fatty Acids, Comp. Biochem. Physiol., B 85, 343–348.

    Article  PubMed  Google Scholar 

  4. Duchamp, C., Barré, H., Delage, D., Rouanet, J.L., Cohen-Adad, F., and Minaire, Y. (1989) Nonshivering Thermogenesis and Adaptation to Fasting in King Penguin Chicks, Am. J. Physiol. 257, R744-R751.

    PubMed  CAS  Google Scholar 

  5. Duchamp, C., Marmonier, F., Denjean, F., Lachuer, J., Eldershaw, T.P., Rouanet, J.L., Morales, A., Meister, R., Benistant, C., Roussel, D., and Barré, H. (1999) Regulatory, Cellular and Molecular Aspects of Avian Muscle Nonshivering Thermogenesis, Ornis Fennica 76, 151–165.

    Google Scholar 

  6. Barré, H., Cohen-Adad, F., Duchamp, C., and Rouanet, J.L. (1986) Multilocular Adipocytes from Muscovy Ducklings Differentiated in Response to Cold Acclimation, J. Physiol. (Lond.) 375, 27–38.

    Google Scholar 

  7. Saarela, S., Hissa, R., Pyörnilä, A., Harjula, R., Ojanen, M., and Orell, M. (1989) Do Birds Possess Brown Adipose Tissues? Comp. Biochem. Physiol., A 92A, 219–228.

    Article  Google Scholar 

  8. Denjean, F., Lachuer, J., Cohen-Adad, F., Barré, H., and Duchamp, C. (1999) Are the Mammalian-Like Uncoupling Proteins 1 and 2 Expressed in Cold-Acclimated Muscovy Ducklings? Ornis Fennica 76, 167–175.

    Google Scholar 

  9. Duchamp, C., and Barré, H. (1993) Skeletal Muscle as the Major Site of Nonshivering Thermogenesis in Cold-Acclimated Ducklings, Am. J. Physiol. 265, R1076-R1083.

    PubMed  CAS  Google Scholar 

  10. Barré, H., Berne, G., Brebion, P., Cohen-Adad, F., and Rouanet, J.L. (1989) Loose-Coupled Mitochondria in Chronic Glucagon-Treated Hyperthermic Ducklings, Am. J. Physiol. 256, R1192-R1199.

    PubMed  Google Scholar 

  11. Roussel, D., rouanet, J.L., Duchamp, C., and Barré, H. (1998) Effects of Cold Acclimation and Palmitate on Energy Coupling in Duckling Skeletal Muscle Mitochondria, FEBS Lett. 439, 258–262.

    Article  PubMed  CAS  Google Scholar 

  12. Skulachev, V.P., and Maslov, S.P. (1960) The Role of Nonphosphorylating Oxidation in Temperature Regulation, Biochemistry (Moscow) 25, 1058–1064.

    Google Scholar 

  13. Levachev, M.M., Mishukova, E.A., Sivkova, V.G., and Skulachev, V.P. (1965) Energy Metabolism in the Pigeon During Self-Warming After Hypothermia, Biokhimiia 30, 864–874.

    PubMed  CAS  Google Scholar 

  14. Garlid, K.D., Beavis, A.D., and Ratkje, S.K. (1989) On the Nature of Ion Leaks in Energy-Transducing Membranes, Biochim. Biophys. Acta 976, 109–120.

    PubMed  CAS  Google Scholar 

  15. Brown, G.C., and Brand, M.D. (1991) On the Nature of the Mitochondrial Proton Leak, Biochim. Biophys. Acta 1059, 55–62.

    Article  PubMed  CAS  Google Scholar 

  16. Porter R.K., Hulbert, A.J., and Brand, M.D. (1996) Allometry of Mitochondrial Proton Leak: Influence of Membrane Surface Area and Fatty Acid Composition, Am. J. Physiol. 271, R1550-R1560.

    PubMed  CAS  Google Scholar 

  17. Brookes, P.S., Buckingham, J.A., Tenreiro, A.M., Hulbert, A.J., and Brand, M.D. (1998) The Proton Permeability of the Inner Membrane of Liver Mitochondria from Ectothermic and Endothermic Vertebrates and from Obese Rats: Correlations with Standard Metabolic Rate and Phospholipid Fatty Acid Composition. Comp. Biochem. Physiol. 119B, 325–334.

    CAS  Google Scholar 

  18. Brand, M.D., Couture, P., Else, P.L., Withers, K.W., and Hulbert, A.J. (1991) Evolution of Energy Metabolism. Proton Permeability of the Inner Membrane of Liver Mitochondria Is Greater in a Mammal Than in a Reptile, Biochem. J. 275, 81–86.

    PubMed  CAS  Google Scholar 

  19. Senault, C., Yazbeck, J., Goubern, M., Portet, R., Vincent, M., and Gallay, J. (1990) Relation Between Membrane Phospholipid Composition, Fluidity and Function in Mitochondria of Rat Brown Adipose Tissue. Effect of Thermal Adaptation and Essential Fatty Acid Deficiency, Biochim. Biophys. Acta 1023, 283–289.

    Article  PubMed  CAS  Google Scholar 

  20. Early, R.J., and Spielman, S.P. (1995) Muscle Respiration in Rats Is Influenced by the Type and Level of Dietary Fat, J. Nutr. 125, 1546–1553.

    PubMed  CAS  Google Scholar 

  21. Ayre, K.J., and Hulbert, A.J. (1996) Dietary Fatty Acid Profile Influences the Composition of Skeletal Muscle Phospholipids in Rats, J. Nutr. 126, 653–662.

    PubMed  CAS  Google Scholar 

  22. Duchamp, C., Cohen-Adad, F., Rouanet, J.L., and Barré, H. (1992) Histochemical Arguments for Muscular Nonshivering Thermogenesis in Muscovy Ducklings, J. Physiol. (Lond.) 457, 27–45.

    CAS  Google Scholar 

  23. Folch, J., Lees, M., and Sloane Stanley, G.H. (1957) A Simple Method for the Isolation and Purification of Total Lipides from Animal Tissues, J. Biol. Chem. 226, 497–509.

    PubMed  CAS  Google Scholar 

  24. Slover, H.J., and Lanza, E. (1979) Quantitative Analysis of Food Fatty Acids by Capillary Gas Chromatography, J. Am. Oil Chem. Soc. 56, 953–962.

    Google Scholar 

  25. Lepage, G., and Roy, C.C. (1986) Direct Transesterification of All Classes of Lipids in a One-Step Reaction, J. Lipid Res. 27, 114–120.

    PubMed  CAS  Google Scholar 

  26. Wibom, R., Lundin, A., and Hultman, E. (1990) A Sensitive Method for Measuring ATP-Formation in Rat Muscle Mitochondria, Scand. J. Clin. Lab. Invest. 50, 143–152.

    PubMed  CAS  Google Scholar 

  27. Hulbert, A.J., and Else, P.L. (1999) Membranes as Possible Pacemakers of Metabolism, J. Theor. Biol. 199, 257–274.

    Article  PubMed  CAS  Google Scholar 

  28. Steffen, D.G., and Platner, W.S. (1976) Subcellular Membrane Fatty Acids of Rat Heart After Cold Acclimation or Thyroxine, Am. J. Physiol. 231, 650–654.

    PubMed  CAS  Google Scholar 

  29. Mak, I.T., Shrago, E., and Elson, C.E. (1983) Modification of Liver Mitochondrial Lipids and of Adenine Nucleotide Translocase and Oxidative Phosphorylation by Cold Adaptation, Biochim. Biophys. Acta 722, 302–309.

    Article  PubMed  CAS  Google Scholar 

  30. Field, C.J., and Clandinin, M.T. (1984) Modulation of Adipose Tissue Fat Composition by Diet: A Review, Nutr. Res. 4, 743–755.

    Article  CAS  Google Scholar 

  31. Daum, G. (1985) Lipids of Mitochondria, Biochim. Biophys. Acta 822, 1–42.

    PubMed  CAS  Google Scholar 

  32. Yeagle, P.L. (1989) Lipid Regulation of Cell Membrane Structure and Function, FASEB J. 3, 1833–1842.

    PubMed  CAS  Google Scholar 

  33. Merrill, A.H., Jr., and Schroeder, J.J. (1993) Lipid Modulation of Cell Function, Annu. Rev. Nutr. 13, 539–559.

    Article  PubMed  CAS  Google Scholar 

  34. Gibson, R.A., McMurchie, E.J., Charnock, J.S., and Kneebone, G.M. (1984) Homeostatic Control of Membrane Fatty Acid Composition in the Rat After Dietary Lipid Treatment, Lipids 19, 942–951.

    PubMed  CAS  Google Scholar 

  35. Benistant, C., Duchamp, C., Cohen-Adad, F., Rouanet, J.L., and Barré, H. (1998) Increased in vitro Fatty Acid Supply and Cellular Transport Capacities in Cold-Acclimated Ducklings (Cairina moschata), Am. J. Physiol. 275, R683-R690.

    PubMed  CAS  Google Scholar 

  36. Gompertz, D., and Greenbaum, A.L. (1966) The Effects of Thyroxine on the Pattern of Fatty Acid Synthesis in Rat Liver, Biochim. Biophys. Acta 116, 441–459.

    PubMed  CAS  Google Scholar 

  37. Faas, F.H., Carter, W.J., and Wynn, J. (1972) Effect of Thyroxine on Fatty Acid Synthesis in vitro, Endocrinology 91, 1481–1492.

    Article  PubMed  CAS  Google Scholar 

  38. Clejan, S., Collipp, P.J., and Maddaiah, V.T. (1980) Hormones and Liver Mitochondria: Influence of Growth Hormone, Thyroxine, Testosterone, and Insulin on Thermotropic Effects of Respiration and Fatty Acid Composition of Membranes, Arch. Biochem. Biophys. 203, 744–752.

    Article  PubMed  CAS  Google Scholar 

  39. Vidal-Puig, A., Solanes, G., Grujic, D., Flier, J.S., and Lowell, B.B. (1997) UCP3: An Uncoupling Protein Homologue Expressed Preferentially and Abundantly in Skeletal Muscle and Brown Adipose Tissue, Biochem. Biophys. Res. Commun. 235, 79–82.

    Article  PubMed  CAS  Google Scholar 

  40. Boss, O., Samec, S., Paoloni-Giacobino, A., Rossier, C., Dulloo, A., Seydoux, J., Muzzin, P., and Giacobino, J.P. (1997) Uncoupling Protein-3: a New Member of the Mitochondrial Carrier Family with Tissue-Specific Expression, FEBS Lett. 408, 39–42.

    Article  PubMed  CAS  Google Scholar 

  41. Brookes, P.S., Hulbert, A.J., and Brand, M.D. (1997) The Proton Permeability of Liposomes Made from Mitochondrial Inner Membrane Phospholipids: No Effect of Fatty Acid Composition, Biochim. Biophys. Acta 1330, 157–164.

    Article  PubMed  CAS  Google Scholar 

  42. Bruni, A., van Dijck, P.W., and de Gier, J. (1975) The Role of Phospholipid Acyl Chains in the Activation of Mitochondrial ATPase Complex, Biochim. Biophys. Acta 406, 315–328.

    Article  PubMed  CAS  Google Scholar 

  43. Jumelle-Laclau, M., Rigoulet, M., Averet, N., Leverve, X., Dubourg, L., Carbonneau, A., Clerc, M., and Guerin, B. (1993) Relationships Between Age-Dependent Changes in the Effect of Almitrine on H(+)-ATPase/ATPsynthase and the Pattern of Membrane Fatty Acid Composition, Biochim. Biophys. Acta 1141, 90–94.

    Article  PubMed  CAS  Google Scholar 

  44. Estabrook, R.W. (1967) Mitochondrial Respiratory Control and the Polarographic Measurement of ADP:O Ratios, Methods Enzymol. 10, 41–47.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Roger Meister.

About this article

Cite this article

Chaînier, F., Roussel, D., Georges, B. et al. Cold acclimation or grapeseed oil feeding affects phospholipid composition and mitochondrial function in duckling skeletal muscle. Lipids 35, 1099–1106 (2000). https://doi.org/10.1007/s11745-000-0625-8

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11745-000-0625-8

Keywords

Navigation