Skip to main content
SpringerLink
Log in

Long-chain fatty acid uptake by skeletal muscle is impaired in homozygous, but not heterozygous, heart-type-FABP null mice

  • Articles
  • Published:
Lipids

Abstract

Previous studies with cardiac myocytes from homozygous heart-type fatty acid (FA)-binding protein (H-FABP)−/− mice have indicated that this intracellular: receptor protein for long-chain FA is involved in the cellular uptake of these substrates. Based on the knowledge that muscle FA uptake is a process highly sensitive to regulation by hormonal and mechanical stimuli, we studied whether H-FABP would play a role in this regulation. A suitable model system to answer this question is provided by H-FABP+/− mice, because in hindlimb muscles the content of H-FABP was measured to be 34% compared to wild-type mice. In these H-FABP+/− skeletal muscles, just as in H-FABP−/− muscles, contents of FA transporters, i.e., 43-kDa FABPpm and 88-kDa FAT/CD36, were similar compared to wild-type muscles, excluding possible compensatory mech-anisms at the sarcolemmal level. Palmitate uptake rates were measured in giant vesicles prepared from hindlimb muscles of H-FABP−/−, H-FABP+/− and H-FABP+/+ mice. For comparison, giant vesicles were isolated from liver, the tissue of which expresses a distinct type of FABP (i.e., L-FABP). Whereas in H-FABP−/− skeletal muscle FA uptake was reduced by 42–45%, FA uptake by H-FABP+/− skeletal muscle was not different from that in wild-type mice. In contrast, in liver from H-FABP−/− and from H-FABP+/− mice, FA uptake was not altered compared to wild-type animals, indicating that changes in FA uptake are restricted to H-FABP expressing tissues. It is concluded that H-FABP plays an important, yet merely permissive, role in FA uptake into muscle tissues.

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

ECL:

enhanced chemiluminescence

FA:

fatty acid

FABP:

fatty acid-binding protein

FABPpm:

plasma membrane FABP

FAT:

FA translocase

H-FABP:

heart-type FABP

L-FABP:

liver-type FABP

References

  1. Glatz, J.F.C., and van der Vusse, G.J. (1996) Cellular Fatty Acid Binding Proteins: Their Function and Physiological Significance, Prog. Lipid Res. 35, 243–282.

    Article  CAS  PubMed  Google Scholar 

  2. Schaap, F.G., Van Der Vusse, G.J., and Glatz, J.F.C. (1998) Fatty Acid-Binding Proteins in the Heart, Mol. Cell Biochem. 180, 43–51.

    Article  CAS  PubMed  Google Scholar 

  3. Storch, J., and Thumser, A.E. (2000) The Fatty Acid Transport Function of Fatty Acid-Binding Proteins, Biochim. Biophys. Acta 1486, 28–44.

    CAS  PubMed  Google Scholar 

  4. Peeters, R.A., and Veerkamp, J.H. (1989) Does Fatty Acid-Binding Protein Play a Role in Fatty Acid Transport?, Mol. Cell. Biochem. 88, 45–49.

    Article  CAS  PubMed  Google Scholar 

  5. Van der Vusse, G.J., Glatz, J.F.C., Stam, H.C., and Reneman, R.S. (1992) Fatty Acid Homeostasis in the Normoxic and Ischemic Heart, Physiol. Rev. 72, 881–940.

    PubMed  Google Scholar 

  6. Spitsberg, V.L., Matitashvili, E., and Gorewit, R.C. (1995) Association and Coexpression of Fatty-Acid-Binding Protein and Glycoprotein CD36 in the Bovine Mammary Gland, Eur. J. Biochem. 230, 872–878.

    Article  CAS  PubMed  Google Scholar 

  7. Prinsen, C.F., and Veerkamp, J.H. (1998) Transfection of L6 Myoblasts with Adipocyte Fatty Acid-Binding Protein cDNA Does Not Affect Fatty Acid Uptake but Disturbs Lipid Metabolism and Fusion, Biochem. J. 329, 265–273.

    CAS  PubMed  Google Scholar 

  8. Claffey, K.P., Crisman, T.S., Ruiz-Opazo, N., and Brecher, P. (1988) Expression of Rat Heart Fatty Acid Binding Protein cDNA in Rat L6 Myoblasts, FASEB J. 2, A1783.

    Google Scholar 

  9. Bühlmann, C., Börchers, T., Pollak, M., and Spener, F. (1999) Fatty Acid Metabolism in Human Breast Cancer Cells (MCF7) Transfected with Heart-Type Fatty Acid Binding Protein, Mol. Cell. Biochem. 199, 41–48.

    Article  PubMed  Google Scholar 

  10. Sha, R.S., Kane, C.D., Xu, Z., Banaszak, L.J., and Bernlohr, D.A. (1993) Modulation of Ligand Binding Affinity of the Adipocyte Lipid-Binding Protein by Selective Mutation. Analysis in vitro and in situ, J. Biol. Chem. 268, 7885–7892.

    CAS  PubMed  Google Scholar 

  11. Murphy, E.J., Prows, D.R., Jefferson, J.R., and Schroeder, F. (1996) Liver Fatty Acid-Binding Protein Expression in Transfected Fibroblasts Stimulates Fatty Acid Uptake and Metabolism, Biochim. Biophys. Acta 1301, 191–198.

    PubMed  Google Scholar 

  12. Binas, B., Danneberg, H., Mcwhir, J., Mullins, L., and Clark, A.J. (1999) Requirement for the Heart-Type Fatty Acid Binding Protein in Cardiac Fatty Acid Utilization, FASEB J. 13, 805–812.

    CAS  PubMed  Google Scholar 

  13. Schaap, F.G., Binas, B., Danneberg, H., Van Der Vusse, G.J., and Glatz, J.F.C. (1999) Impaired Long-Chain Fatty Acid Utilization by Cardiac Myocytes Isolated from Mice Lacking the Heart-Type Fatty Acid Binding Protein Gene, Circ. Res. 85, 329–337.

    CAS  PubMed  Google Scholar 

  14. Bonen, A., Luiken, J.J.F.P., Liu, S., Dyck, D.J., Kiens, B., Kristiansen, S., Turcotte, L.P., Van Der Vusse, G.J., and Glatz, J.F.C. (1998) Palmitate Transport and Fatty Acid Transporters in Red and White Muscles, Am. J. Physiol. 275, E471-E478.

    CAS  PubMed  Google Scholar 

  15. Luiken, J.J.F.P., Turcotte, L.P., and Bonen, A. (1999) Protein-Mediated Palmitate Uptake and Expression of Fatty Acid Transport Proteins in Heart Giant Vesicles, J. Lipid Res. 40, 1007–1016.

    CAS  PubMed  Google Scholar 

  16. Koonen, D.P.Y., Coumans, W.A., Arumugam, Y., Bonen, A., Glatz, J.F.C., and Luiken, J.J.F.P. (2002) Glant Membrane Vesicles as a Model to Study Cellular Substrate Uptake Dissected from Metabolism, Mol. Cell. Biochem. 239, 121–130.

    Article  CAS  PubMed  Google Scholar 

  17. Van Nieuwenhoven, F.A., Verstijnen, C.P.H.J., Van Eys, G.J.J.M., Van Breda, E., De Jong, Y.F., Van Der Vusse, G.J., and Glatz, J.F.C. (1994) Fatty Acid Transfer Across the Myocardial Capillary Wall: No Evidence of a Substantial Role for Cytoplasmic Fatty Acid-Binding Protein, J. Mol. Cell. Cardiol. 26, 1635–1647.

    Article  PubMed  Google Scholar 

  18. Luiken, J.J.F.P., Arumugam, Y., Dyck, D.J., Bell, R.C., Pelsers, M.M.L., Turcotte, L.P., Tandon, N.N., Glatz, J.F.C., and Bonen, A. (2001) Increased Rates of Fatty Acid Uptake and Plasmalemmal Fatty Acid Transporters in Obese Zucker Rats, J. Biol. Chem. 276, 40567–40573.

    Article  CAS  PubMed  Google Scholar 

  19. Vork, M.M., Glatz, J.F.C., Surtel, D.A., Knubben, H.J., and Van Der Vusse, G.J. (1991) A Sandwich Enzyme Linked Immuno-Sorbent Assay for the Determination of Rat Heart Fatty Acid-Binding Protein Using the Streptavidin-Biotin System. Application to Tissue and Effluent Samples from Normoxic Rat Heart Perfusion, Biochim. Biophys. Acta 1075, 199–205.

    CAS  PubMed  Google Scholar 

  20. Luiken, J.J.F.P., Arumugam, Y., Bell, R.C., Calles-Escandon, J., Tandon, N.N., Glatz, J.F.C., and Bonen, A. (2002) Changes in Fatty Acid Transport and Transporters Are Related to the Severity of Insulin Deficiency, Am. J. Physiol. Endocrinol. Metab. 283, E612-E621.

    CAS  PubMed  Google Scholar 

  21. Van Nieuwenhoven, F.A., Willemsen, P.H., Van Der Vusse, G.J., and Glatz, J.F.C. (1999) Co-Expression in Rat Heart and Skeletal Muscle of Four Genes Coding for Proteins Implicated in Long-Chain Fatty Acid Uptake, Int. J. Biochem. Cell Biol. 31, 489–498.

    Article  PubMed  Google Scholar 

  22. Richieri, G.V., Anel, A., and Kleinfeld, A.M. (1993) Interactions of Long-Chain Fatty Acids and Albumin: Determination of Free Fatty Acid Levels Using the Fluorescent Probe ADIFAB, Biochemistry 32, 7574–7580.

    Article  CAS  PubMed  Google Scholar 

  23. Vork, M.M., Glatz, J.F.C., and Van Der Vusse, G.J. (1993) On the Mechanism of Long-Chain Fatty Acid Transport in Cardiomycytes as Facilitated by Cytoplasmic Fatty Acid-Binding Protein, J. Theor. Biol. 160, 207–222.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Physiology, Cardiovascular Research Institute Maastricht (CARIM), Maastricht University, P.O. Box 616, NL-6200 MD, Maastricht, The Netherlands

    J. J. F. P. Luiken, D. P. Y. Koonen, W. A. Coumans, M. M. A. L. Pelsers & J. F. C. Glatz

  2. Department of Veterinary Pathobiology, College of Veterinary Medicine, Texas A&M University, College Station, Texas

    B. Binas

  3. Department of Kinesiology, University of Waterloo, Waterloo, Canada

    A. Bonen

Authors
  1. J. J. F. P. Luiken
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. P. Y. Koonen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. W. A. Coumans
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. M. A. L. Pelsers
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. B. Binas
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. Bonen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. F. C. Glatz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. J. F. P. Luiken.

About this article

Cite this article

Luiken, J.J.F.P., Koonen, D.P.Y., Coumans, W.A. et al. Long-chain fatty acid uptake by skeletal muscle is impaired in homozygous, but not heterozygous, heart-type-FABP null mice. Lipids 38, 491–496 (2003). https://doi.org/10.1007/s11745-003-1089-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11745-003-1089-6

Keywords

Search

Navigation