Skip to main content
SpringerLink
Log in

Docosahexaenoic acid-and eicosapentaenoic acid-enriched cardiolipin in the manila clam Ruditapes philippinarum

  • Articles
  • Published:
Lipids

Abstract

The FA composition of cardiolipin (CL) from the Manila clam Ruditapes philippinarum was investigated in whole body and individual organs. CL was isolated by HPLC and its chemical structure characterized using NMR spectroscopy. Two prominent FA, EPA and DHA, were found in approximately equal proportions, contributing together up to 73 mol% of the total FA. The FA composition of CL is presumed to reflect a specific synthesis pathway independent of diet and of total glycerophospholipid FA composition. To the best of our knowledge, this is the first time that a CL dominated by the two PUFA 22∶6n−3 and 20∶5n−3 has been characterized and described. This EPA+DHA specificity of the CL in the Manila clam is though to reflect a functional and structural modification of mitochondrial membranes of this bivalve species compared with scallops, oysters, and mussels that possess a CL dominated by DHA. The FA composition and levels of CL differed little between separated organs, and the large pool of DHA and EPA was found fairly equally distributed in gills, mantle, foot, siphon, and muscle. However, whereas DHA and PUFA levels were most stable between organs, EPA and arachidonic acid were significantly more variable and seemed to be interrelated.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

CL:

cardiolipin, common name of diphosphatidylglycerol

DQF-COSY:

double-quantum filter correlated spectroscopy

GPL:

glycerophospholipid(s)

HMBC:

heteronuclear multiple bond coherence

HMQC:

heteronuclear multiple quantum coherence

NL:

neural lipids

NMI:

non-methylene interrupted

References

  1. Robinson, N.C., Zborowski, J., and Talbert, L.H. (1990) Cardiolipin-Depleted Bovine Heart Cytochrome c Oxidase: Binding Stoichiometry and Affinity for Cardiolipin Derivatives, Biochemistry 29, 8962–8969.

    Article  PubMed  CAS  Google Scholar 

  2. Berger, A., German, J.B., and Gershwin, M.E. (1993) Biochemistry of CL: Sensitivity to Dietary Fatty Acids, in Advances in Food and Nutrition Research (Kissela, J.E., ed.), pp. 259–338, Academic Press, San Diego.

    Google Scholar 

  3. McAuley, K.E., Fyfe, P.K., Ridge, J.P., Isaacs N.W., Cogdell, R.J., and Jones, M.R. (1999) Structural Details of an Interaction Between Cardiolipin and an Integral Membrane Protein, Proc. Natl. Acad. Sci. USA 96, 14706–14711.

    Article  PubMed  CAS  Google Scholar 

  4. Schlame, M., Rua, D., and Greenberg, M.L. (2000) The Biosynthesis and Functional Role of Cardiolipim, Prog. Lipid Res. 39, 257–288.

    Article  PubMed  CAS  Google Scholar 

  5. Zhang, M., Mileykovskaya, E., and Dowhan, W. (2002) Gluing the Respiratory Chain Together: Cardiolipin Is Required for Supercomplex Formation in the Inner Mitochondrial Membrane, J. Biol. Chem. 277, 43553–43556.

    Article  PubMed  CAS  Google Scholar 

  6. Ma, B.J., Taylor, W.A., Dolinsky, V.W., and Hatch, G.M. (1999) Acylation of Monolysocardiolipin in Rat Heart, J. Lipid Res. 40, 1837–1845.

    PubMed  CAS  Google Scholar 

  7. Clandinin, M.T., Field, C.J., Hargraves, K., Morson, L., and Zsigmond, E. (1985) Role of Diet Fat in Subcellular Structure and Function, Can. J. Physiol. Pharmacol. 63, 546–556.

    PubMed  CAS  Google Scholar 

  8. Yamaoka, S., Urade, R., and Kito, M. (1988) Mitochondrial Function in Rats Is Affected by Modification of Membrane Phospholipids with Dietary Sardine Oil, J. Nutr. 118, 290–296.

    PubMed  CAS  Google Scholar 

  9. Watkins, S.M., Lin, T.Y., Davis, R.M., Ching, J.R., Depeters, E.J., Halpern, G.M., Walzem, R.L., and German, J.B. (2001) Unique Phospholipid Metabolism in Mouse Heart in Response to Dietary Docosahexaenoic or α-Linoleic Acids, Lipids 36, 247–254.

    Article  PubMed  CAS  Google Scholar 

  10. Hostetler, K. (1982) Polyglycerophospholipids: Phosphatidylglycerol, Diphosphatidyl Glycerol, and Bis (Monoacylglycero)Phosphate, Elsevier Biomedical Press, Amsterdam.

    Google Scholar 

  11. Schlame, M., Shanske, S., Doty, S., König, T., Sculco, T., Dimauro, S., and Blanck, T.J.J. (1999) Microanalysis of Cardiolipin in Small Biopsies Including Skeletal Muscle from Patients with Mitochondrial Disease, J. Lipid Res. 40, 1585–1592.

    PubMed  CAS  Google Scholar 

  12. Wolff, R.L., Combe, N.A., and Entressangles, B. (1985) Positional Distribution of Fatty Acids in Cardiolipin of Mitochondria from 21-Day-Old Rats, Lipids 20, 908–914.

    PubMed  CAS  Google Scholar 

  13. Berger, A., and German, J.B. (1990) Phospholipid Fatty Acid Composition of Various Mouse Tissues After Feeding α-Linolenate (18∶3n−3) or Eicosatrienoate (20∶3n−3), Lipids 25, 473–480.

    PubMed  CAS  Google Scholar 

  14. Kraffe, E., Soudant, P., Marty, Y., Kervarec, N., and Jehan, P. (2002) Evidence of a Tetradocosahexaenoic Cardiolipin in Some Marine Bivalves, Lipids 37, 507–514.

    Article  PubMed  CAS  Google Scholar 

  15. Bell, M.V., and Sargent, J.R. (1985) Fatty Acid Analyses of Phosphoglycerides from Tissues of the Clam Chlamys islandica (Muller) and the Starfish Ctenodiscus crispatus (Retzius) from Balsfjorden, Northern Norway, J. Exp. Mar. Biol. Ecol. 87, 31–40.

    Article  CAS  Google Scholar 

  16. Soudant, P., Moal, J., Marty, Y., and Samain, J.F. (1996) Impact of the Quality of Dietary Fatty Acids on Metabolism and the Composition of Polar Lipid Classes in Female Gonads of Pectenmaximus (L.), J. Exp. Mar. Biol. Ecol. 205, 149–163.

    Article  CAS  Google Scholar 

  17. Soudant, P., Moal, J., Marty, Y., and Samain, J.F. (1997) Composition of Polar Lipid Classes in Male Gonads of Pecten maximus (L.). Effect of Nutrition, J. Exp. Mar. Biol. Ecol. 215 103–114.

    Article  CAS  Google Scholar 

  18. Soudant, P., Van Ryckeghem, K., Marty, Y., Moal, J., Samain, J.F., and Sorgeloos, P. (1999) Comparison of the Lipid Class and Fatty Acid Composition Between a Reproductive Cycle in Nature and a Standard Hatchery Conditioning of the Pacific Oyster Crassostrea gigas, Comp. Biochem. Phys. 123, 209–222.

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  20. Nelson, G.J. (1993) Isolation and Purification of Lipids from Biological Matrices, in Analysis of Fats. Oils and Derivatives (Perkins, E.G., ed.), pp. 20–89, AOCS Press, Champaign.

    Google Scholar 

  21. Marty, Y., Delaunay, F., Moal, J., and Samain, J.F. (1992) Changes in the Fatty Acid Composition of the Scallop Pecten maximus (L.) During Larval Development, J. Exp. Mar. Biol. Ecol. 163, 221–234.

    Article  CAS  Google Scholar 

  22. Soudant, P., Marty, Y., Moal, J., Masski, H., and Samain, J.F. (1998) Fatty Acid Composition of Polar Lipid Classes During Larval Development of Scallop Pecten maximus (L.), Comp. Biochem. Physiol. A 121, 279–288.

    Google Scholar 

  23. Vlahov, G. (1999) Application of NMR to the Study of Olive Oils, Prog. Nucl. Magn. Reson. Spectrosc. 35, 341–357.

    Article  CAS  Google Scholar 

  24. Adosraku, R.K., Smith, J.D., Nicolaou, A., and Gibbons, W.A. (1996) Tetrahymena thermophila: Analysis of Phospholipids and Phosphonolipids by High-Field 1H-NMR, Biochim. Biophys. Acta 1299, 167–174.

    PubMed  Google Scholar 

  25. Schlame, M., Beyer, K., Hayer-Hartl, M., and Klingenberg, M. (1991) Molecular Species of Cardiolipin in Relation to Other Mitochondrial Phospholipids. Is There an Acyl Specificity of the Interaction Between Cardiolipin and the ADP/ATP Carrier? Eur. J. Biochem. 199, 459–466.

    Article  PubMed  CAS  Google Scholar 

  26. Ackman, R.G. (1983) Fatty Acid Metabolism of Bivalves, Proc. 2nd Int. Conf. Aquac. Nutr. Spec. Publ. 2, 358–375.

    Google Scholar 

  27. Paradies, G., and Ruggiero, F.M. (1990) Age-Related Changes in the Activity of the Pyruvate Carrier and in Lipid Composition in Rat-Heart Mitochondria, Biochim. Biophys. Acta 1016, 207–212.

    Article  PubMed  CAS  Google Scholar 

  28. Paradies, G., Ruggiero, F.M., Petrosillo, G., and Quagliariello, E. (1994) Enhanced Cytochrome Oxidase Activity and Modification of Lipids in Heart Mitochondria from Hyperthyroid Rats, Biochim. Biophys. Acta 1225, 165–170.

    PubMed  CAS  Google Scholar 

  29. Alasnier, C., and Gandemer, G. (1998) Fatty Acid and Aldehyde Composition of Individual Phospholipid Classes of Rabbit Skeletal Muscles Is Related to the Metabolic Type of the Fibre, Meat Sci. 48, 225–235.

    Article  CAS  Google Scholar 

  30. Tschischka, K., Abele, D., and Portner, H.O. (2000) Mitochondrial Oxyconformity and Cold Adaptation in the Polychaete Nereis pelagica and the Bivalve Arctica islandica from the Baltic and White Seas, J. Exp. Biol. 203, 3355–3368.

    PubMed  CAS  Google Scholar 

  31. Abele, D., Heise, K., Portner, H.O., and Puntarulo, S. (2002) Temperature-Dependence of Mitochondrial Function and Production of Reactive Oxygen Species in the Intertidal Mud Clam Mya arenaria, J. Exp. Biol. 205, 1831–1841.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Unité mixte CNRS 6539, Institut Universitaire Européen de la Mer (IUEM), Université de Bretagne Occidentale, 29280, Plouzane, France

    Philippe Soudant

  2. Laboratoire de Résonance Magnétique Nucléaire (RMN), Université de Bretagne Occidentale, 29285, Brest cedex, France

    Nelly Kervarec

  3. Unité mixte CNRS 6521, Université de Bretagne Occidentale, C.S. 29238, Brest cedex, France

    Edouard Kraffe & Yanic Marty

Authors
  1. Edouard Kraffe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Philippe Soudant
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yanic Marty
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nelly Kervarec
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yanic Marty.

About this article

Cite this article

Kraffe, E., Soudant, P., Marty, Y. et al. Docosahexaenoic acid-and eicosapentaenoic acid-enriched cardiolipin in the manila clam Ruditapes philippinarum . Lipids 40, 619–625 (2005). https://doi.org/10.1007/s11745-005-1423-z

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11745-005-1423-z

Keywords

Search

Navigation