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Collision-mediated transfer of long-chain fatty acids by neural tissue fatty acid-binding proteins (FABP)

Studies with fluorescent analogs

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Abstract

Mammalian fatty acid-binding proteins (FABP) are a family of intracellular proteins (approx 15 kDa) that bind long-chain fatty acids (FA) with high affinity. They are believed to serve as cytoplasmic transporters of FA and to target FA to specific cellular sites of utilization. Several different FABPs are expressed in neural tissue, including brain FABP (B-FABP), myelin FABP (M-FABP), and heart FABP (H-FABP). We have previously shown that H-FABP transfers FA via direct collisional interactions with acceptor model membranes. In the present studies, we use a fluorescence resonance energy transfer (FRET) assay to examine the rate and mechanism of transfer of a fluorescent long-chain fatty acid from B-FABP to phospholipid vesicles. The rate of transfer is shown to be independent of buffer ionic strength and dramatically enhanced by the presence of specific anionic phospholipids. These results are consistent with a mechanism by which FA are transferred from B-FABP to phospholipid membranes by a transient collision-based mechanism.

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References

  • Abumrad N. A., Harmon C. M., and Ibrahimi A. (1998) Membrane transport of long-chain fatty acids: evidence for a facilitated process. J. Lipid Res. 39, 2309–2318.

    PubMed  CAS  Google Scholar 

  • Arnold D., Feng L., Kim J., and Heintz N. (1994) A strategy for the analysis of gene expression during neural development. Proc. Natl. Acad. Sci. USA 91, 9970–9974.

    Article  PubMed  CAS  Google Scholar 

  • Banaszak L. J., Winter N., Xu Z., Bernlohr D. A., and Jones T. A. (1994) Lipid-binding proteins: A family of fatty acid and retinoid transport proteins. Adv. Prot. Chem. 145, 90–148.

    Google Scholar 

  • Bass N. M. (1985) Function and regulation of hepatic and intestinal fatty acid binding proteins. Chem. Phys. Lipids 38, 95–114.

    Article  PubMed  CAS  Google Scholar 

  • Bass N. M. (1993) Cellular binding proteins for fatty acids and retinoids: similar or specialized functions? Mol. Cell. Biochem. 123, 191–202.

    Article  PubMed  CAS  Google Scholar 

  • Bennett E., Stenvers K. L., Lund P. K., and Popko B. (1994) Cloning and characterization of a cDNA encoding a novel fatty acid binding protein from rat brain. J. Neurochem. 63, 1616–1624.

    Article  PubMed  CAS  Google Scholar 

  • Bradford M. (1976) A rapid and sensitive method for the quantitiation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254.

    Article  PubMed  CAS  Google Scholar 

  • Charlton S. C. and Smith L. C. (1982) Kinetics of transfer of pyrene and rac-1-oleyl-2-[4-(3-pyrenyl)butanoyl] glycerol between human plasma lipoproteins. Biochemistry 21, 4023–4030.

    Article  PubMed  CAS  Google Scholar 

  • Coe N. R. and Bernlohr D. A. (1998) Physiological properties and functions of intracellular fatty acid-binding proteins. Biochim. Biophys. Acta 1391, 287–306.

    PubMed  CAS  Google Scholar 

  • Feng L., Hatten M. E., and Heintz N. (1994) Brain lipid binding protein (BLBP): a novel signaling system in the developing mammalian CNS. Neuron 12, 895–908.

    Article  PubMed  CAS  Google Scholar 

  • Glatz J. F. and Van der vusse G. J. (1996) Cellular fatty acid-binding proteins: their function and physiological significance. Prog. Lipid Res. 35, 243–282.

    Article  PubMed  CAS  Google Scholar 

  • Glatz J. F. and Veerkamp J. H. (1983) A radiochemical procedure for the assay of fatty acid binding by proteins. Anal. Biochem. 132, 89–95.

    Article  PubMed  CAS  Google Scholar 

  • Gomori G. (1942) A modification of the colorimetric phosphorous determination for use with the photoelectric colorimeter. J. Lab. Clin. Med. 27, 955–960.

    CAS  Google Scholar 

  • Hamilton J. A. (1998) Fatty acid transport: difficult or easy? J. Lipid Res. 39, 467–481.

    PubMed  CAS  Google Scholar 

  • Herr F. M., Matarese V., Bernlohr D. A., and Storch J. (1995) Surface lysine residues modulate the collisional transfer of fatty acid from adipocyte fatty acid binding protein to membranes. Biochemistry 34, 11,840–11,845.

    Article  CAS  Google Scholar 

  • Herr F. M., Aronson J., and Storch J. (1996) Role of portal region lysine residues in electrostatic interactions between heart fatty acid binding protein and phospholipid membranes. Biochemistry 35, 1296–1303.

    Article  PubMed  CAS  Google Scholar 

  • Hsu K. T. and Storch J. (1996) Fatty acid transfer from liver and intestinal fatty acid-binding proteins to membranes occurs by different mechanisms. J. Biol. Chem. 271, 13,317–13,323.

    CAS  Google Scholar 

  • Huang C. and Thompson T. E. (1974) Preparation of homogeneous, single-walled phosphatidylcholine vesicles. Methods Enzymol. 32, 485–489.

    Article  PubMed  CAS  Google Scholar 

  • Kim H. K. and Storch J. (1992a) Mechanism of free fatty acid transfer from rat heart fatty acid-binding protein to phospholipid membranes. Evidence for a collisional process. J. Biol. Chem. 267, 20,051–20,056.

    CAS  Google Scholar 

  • Kim H. K. and Storch J. (1992b) Free fatty acid transfer from rat liver fatty acid-binding protein to phospholipid vesicles. Effect of ligand and solution properties. J. Biol. Chem. 267, 77–82.

    PubMed  CAS  Google Scholar 

  • Kurtz A., Zimmer A., Schnutgen F., Bruning G., Spener F., and Muller T. (1994) The expression pattern of a novel gene encoding brain fatty acid binding protein correlates with neural and glial cell development. Development 120, 2637–2649.

    PubMed  CAS  Google Scholar 

  • Laemmli U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.

    Article  PubMed  CAS  Google Scholar 

  • Lees M. B. and Brostoff S. W. (1984) Proteins of myelin, in Myelin (Morell, P. ed.), Plenum Press, New York, pp. 197–224.

    Google Scholar 

  • Maniatis T., Fritsch E. F., and Sambrook J. F. (1982) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.

    Google Scholar 

  • MyersPayne S. C., Hubbell T., Pu L. X., Schnutgen F., Borchers T., Wood W. G., Spener F., and Schroeder F. (1996) Isolation and characterization of two fatty acid binding proteins from mouse brain. J. Neurochem. 66, 1648–1656.

    Article  CAS  Google Scholar 

  • Narayanan V., Kaestner K. H., and Tennekoon G. (1991) Structure of the mouse myelin P2 protein gene. J. Neurochem. 57, 75–80.

    Article  PubMed  CAS  Google Scholar 

  • Owada Y., Yoshimoto T., and Kondo H. (1996) Spatiotemporally differential expression of genes for three members of fatty acid binding proteins in developing and mature rat brains. J. Chem. Neuroanat. 12, 113–122.

    Article  PubMed  CAS  Google Scholar 

  • Sacchettini J. C. and Gordon J. I. (1993) Rat intestinal fatty acid binding protein. A model system for analyzing the forces that can bind fatty acids to proteins. J. Biol. Chem. 268, 18,399–18,402.

    CAS  Google Scholar 

  • Schnutgen F., Borchers T., Muller T., and Spener F. (1996) Heterologous expression and characterisation of mouse brain fatty acid binding protein. Biol. Chem. Hoppe-Seyler 377, 211–215.

    PubMed  CAS  Google Scholar 

  • Sellner P. A., Chu W. J., Glatz J. F., and Berman N. E. J. (1995) Developmental role of fatty acid-binding proteins in mouse brain. Dev. Brain Res. 89, 33–46.

    Article  CAS  Google Scholar 

  • Smith E. R. and Storch J. (1999) The adipocyte fatty acid-binding protein binds to membranes by electrostatic interactions. J. Biol. Chem. 274, 35,325–35,330.

    CAS  Google Scholar 

  • Storch J., Herr F. M., Hsu K. T., Kim H. K., Liou H. L., and Smith E. R. (1996) The role of membranes and intracellular binding proteins in cytoplasmic transport of hydrophobic molecules: Fatty acid-binding proteins. Comp. Biochem. Physiol. 115, 333–339.

    Article  Google Scholar 

  • Storch J. and Bass N. M. (1990) Transfer of fluorescent fatty acids from liver and heart fatty acid-binding proteins to model membranes. J. Biol. Chem. 265, 7827–7831.

    PubMed  CAS  Google Scholar 

  • Storch J. and Kleinfeld A. M. (1986) Transfer of long-chain fluorescent free fatty acids between unilamellar vesicles. Biochemistry 25, 1717–1726.

    Article  PubMed  CAS  Google Scholar 

  • Storch J. and Thumser A. E. (2000) The fatty acid transport function of fatty acid binding proteins. Biochim. Biophys. Acta 1486, 28–44.

    PubMed  CAS  Google Scholar 

  • Thumser A. E. and Storch J. (2000) Liver and intestinal fatty acid-binding proteins obtain fatty acids from phospholipid membranes by different mechanisms. J. Lipid Res. 41, 647–656.

    PubMed  CAS  Google Scholar 

  • Trapp B. D., Dubois Dalcq M., and Quarles R. H. (1984) Ultrastructural localization of P2 protein in actively myelinating rat Schwann cells. J. Neurochem. 43, 944–948.

    Article  PubMed  CAS  Google Scholar 

  • Veerkamp J. H., Paulussen R. J. A., Peeters R. A., Maatman R. G. H. J., van Moerkerk H. T. B., and van Kuppevelt T. H. (1990) Detection, tissue distribution and (sub)cellular localization of fatty acid-binding protein types. Mol. Cell. Biochem. 98, 11–18.

    Article  PubMed  CAS  Google Scholar 

  • Veerkamp J. H. and Maatman R. G. H. J. (1995) Cytoplasmic fatty acid-binding proteins: their structure and genes. Prog. Lipid Res. 34, 17–52.

    Article  PubMed  CAS  Google Scholar 

  • Weise M. J. and Brostoff S. W. (1985) Research methods in studies with the P2 basic protein, in Research Methods in Neurochemistry (Marks, N. and Rodnight, R. ed.), Plenum Press, New York, pp. 263–302.

    Google Scholar 

  • Wootan M. G., Bernlohr D. A., and Storch J. (1993) Mechanism of fluorescent fatty acid transfer from adipocyte fatty acid binding protein to membranes. Biochemistry 32, 8622–8627.

    Article  PubMed  CAS  Google Scholar 

  • Wootan M. G. and Storch J. (1994) Regulation of fluorescent fatty acid transfer from adipocyte and heart fatty acid binding proteins by acceptor membrane lipid composition and structure. J. Biol. Chem. 269, 10,517–10,523.

    CAS  Google Scholar 

  • Xu L. Z., Sanchez R., Sali A., and Heintz N. (1996) Ligand specificity of brain lipid binding protein. J. Biol. Chem. 271, 24,711–24,719.

    CAS  Google Scholar 

  • Zhang F., Kamp F., and Hamilton J. A. (1996) Dissociation of long and very long chain fatty acids from phospholipid bilayers. Biochemistry 35, 16,055–16,060.

    CAS  Google Scholar 

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Author notes

  1. Alfred E. A. Thumser

    Present address: School of Biological Sciences, University of Surrey, GU2 7XH, Guildford, Surrey, UK

  2. Judy Tsai

    Present address: Department of Nutrition, Harvard School of Public Health, 02115, Boston, MA

Authors and Affiliations

  1. Department of Nutritional Sciences, Cook College, Rutgers University, 96 Lipman Drive, 08901-8525, New Brunswick, New Jersey

    Alfred E. A. Thumser, Judy Tsai & Judith Storch

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  1. Alfred E. A. Thumser
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  2. Judy Tsai
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Thumser, A.E.A., Tsai, J. & Storch, J. Collision-mediated transfer of long-chain fatty acids by neural tissue fatty acid-binding proteins (FABP). J Mol Neurosci 16, 143–150 (2001). https://doi.org/10.1385/JMN:16:2-3:143

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  • DOI: https://doi.org/10.1385/JMN:16:2-3:143

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