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Similar mechanisms of fatty acid transfer from human anal rodent fatty acid-binding proteins to membranes: Liver, intestine, heart muscle, and adipose tissue FABPs

  • Judith Storch
  • Jacques H. Veerkamp
  • Kuo-Tung Hsu
Part of the Developments in Molecular and Cellular Biochemistry book series (DMCB, volume 38)

Abstract

The mammalian fatty acid-binding proteins (FABPs) are thought to be important for the transport and metabolism of fatty acids in numerous cell types. The transfer of FA from different members of the FABP family to membranes has been shown to occur by two distinct mechanisms, an aqueous diffusion-based mechanism and a collisional mechanism, wherein the FABP interacts directly with membrane acceptors. Much of the work that underlies this concept comes from efforts using rodent FABPs. Given the increasing awareness of links between FABPs and several chronic diseases in humans, it was important to establish the mechanisms of FA transfer for human FABPs. In the present studies, we examined the rate and mechanism of fatty acid transfer from four pairs of human and rodent (rat or mouse, as specified) FABPs: hLFABP and rLFABP, hIFABP and rIFABP, hHFABP and rHFABP, and hAFABP and mAFABP. In the case of human IFABP, both the Ala54and Thr54 forms were examined. The results show clearly that for all FABPs examined, the mechanisms of ligand transfer observed for rodent proteins hold true for their human counterparts. Moreover, it appears that the Ala to Thr substitution at residue 54 of the human IFABP does not alter the fundamental mechanism of ligand transfer to membranes, but nevertheless causes a consistent decrease in the rate of transfer. (Mol Cell Biochem 239: 25–33, 2002)

Key words

fatty acid-binding protein fatty acid lipid transport phospholipid membranes gene polymorphism 

Abbreviations

FA

fatty acid

FABP

fatty acid-binding protein

LFABP

liver FABP

IFABP

intestinal FABP

AFABP

adipose tissue FABP

HFABP

heart muscle FABP

rFABP

rat FABP

mFABP

mouse FABP

hFABP

human FABP

AOFA

anthroyloxy-labeled FA

12AO

12-(9-anthroyloxy)-oleic acid

2AP

2-(9-anthroyloxy)-palmitric acid

SUV

small unilamellar vesicles

EPC

egg phosphatidylcholine

PS

brain phosphatidylserine

CL

bovine heart cardiolipin

NBC-PC

1-palmitoyl-2(lautryl-N-(7-nitro2,1,3-benzoxadiazol-4-yl))-phosphatidylcholine

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References

  1. 1.
    Storch J. Thumser AEA: The fatty acid transport function of fatty acid-binding proteins. Biochim Biophys Acta 1486: 28–44, 2000PubMedCrossRefGoogle Scholar
  2. 2.
    Glatz JFC, van der Vusse G: Cellular fatty acid-binding proteins: Their function and physiological significance. Prog Lipid Res 35: 243–282, 1996PubMedCrossRefGoogle Scholar
  3. 3.
    Kim HK, Storch J: 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, 1992PubMedGoogle Scholar
  4. 4.
    Hsu KT, Storch J: Fatty acid transfer from liver and intestinal fatty acid binding-proteins to membranes occurs by different mechanisms. J Biol Chem 271: 13317–13323, 1996PubMedCrossRefGoogle Scholar
  5. 5.
    Storch J, Bass NM: Transfer of fluorescent fatty acids from liver and heart fatty acid-binding proteins to model membranes. J Biol Chem 265: 7827–7831, 1990PubMedGoogle Scholar
  6. 6.
    Wootan MG, Bernlohr DA, Storch J: Mechanism of fluorescent fatty acid transfer from adipocyte fatty acid binding protein to membrane. Biochemistry 32: 8622–8627, 1993PubMedCrossRefGoogle Scholar
  7. 7.
    Wootan MG, Storch J: 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: 10517–10523, 1994PubMedGoogle Scholar
  8. 8.
    Kim HK, Storch J: 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: 20051–20056, 1992PubMedGoogle Scholar
  9. 9.
    Liou H, Storch J: The helical cap domain is important for fatty acid transfer from adipocyte and heart fatty acid-binding proteins to membranes. FASEB J 12: A514–000, 1998Google Scholar
  10. 10.
    Corsico B, Cistola DP, Frieden C, Storch J: The helical domain of intestinal fatty acid binding protein is critical for collisional transfer of fatty acids to phospholipid membranes. Proc Natl Acad Sci USA 95: 12174–12178, 1998PubMedCrossRefGoogle Scholar
  11. 11.
    Liou H-L, Storch J: Role of surface lysine residues of adipocyte fatty acid-binding protein in fatty acid transfer to phospholipid vesicles. Biochemistry 40: 6475–6485, 2001PubMedCrossRefGoogle Scholar
  12. 12.
    Richieri GV, Low PJ, Ogata RT, Kleinfeld AM: Thermodynamics of fatty acid binding to engineered mutants of the adipocyte and intestinal fatty acid-binding proteins. J Biol Chem 273: 7397–7405, 1998PubMedCrossRefGoogle Scholar
  13. 13.
    Baier LJ, Sacchettini JC, Knowler WC, Eads J, Paolisso G, Tataranni PA, Mochizuki H, Bennett PH, Bogardus C, Prochazka M: An amino acid substitution in the human intestinal fatty acid binding protein is associated with increased fatty acid binding, increased fat oxidation, and insulin resistance. J Clin Invest 95: 1281–1287, 1995PubMedCrossRefGoogle Scholar
  14. 14.
    Herr FM, Matarese V, Bernlohr DA, Storch J: Surface lysine residues modulate the collisional transfer of fatly acid from adipocyte fatty acid binding protein to membranes. Biochemistry 34: 11840–11845, 1995PubMedCrossRefGoogle Scholar
  15. 15.
    Zimmerman AW, van Moerkerk HTB, Veerkamp JH: Ligand specificity and conformational stability of human fatty acid-binding proteins. Int J Biochcm Cell Biol 33: 865–876, 2001CrossRefGoogle Scholar
  16. 16.
    Veerkamp JH, van Moerkerk HTB, Prinsen CFM, van Kuppevelt TH: Structural and functional studies on different human FABP types. Mol Cell Biochem 192: 137–142, 1999PubMedCrossRefGoogle Scholar
  17. 17.
    Smith ER, Storch J: The adipocyte fatty acid-binding protein binds to membranes by electrostatic interactions. J Biol Chem 274: 35325–35330, 1999PubMedCrossRefGoogle Scholar
  18. 18.
    Ames BN: Assay of inorganic phosphate, total phosphate and phosphatases. Meth Enzymol 8: 115–118, 1966CrossRefGoogle Scholar
  19. 19.
    Herr FM, Aronson J, Storch J: Role of portal region lysine residues in electrostatic interactions between heart fatty acid binding protein and phospholipid membranes. Biochemistry 35: 1296–1303, 1996PubMedCrossRefGoogle Scholar
  20. 20.
    Richieri GV, Ogata RT, Kleinfeld AM: Equilibrium constants for the binding of fatty acids with fatty acid-binding proteins from adipocyte. intestine, heart, and liver measured with the fluorescent probe ADIFAB. J Biol Chem 269: 23918–23930, 1994PubMedGoogle Scholar
  21. 21.
    Charlton SC, Smith LC: Kinetics of transfer of pyrene and rac-1-oleyl-2-[4-(3-pyrenyl)butanoyl]glyccrol between human plasma lipoproteins. Biochemistry 21: 4023–4030, 1982PubMedCrossRefGoogle Scholar
  22. 22.
    Zucker SD: Kinetic model of protein-mediated ligand transport: Influence of soluble binding proteins on the intermembrane diffusion of a fluorescent fatty acid. Biochemistry 40: 977–986, 2001PubMedCrossRefGoogle Scholar
  23. 23.
    Weisiger RW, Zucker SD: Transfer of fatty acids between intracellular membranes: Roles of soluble binding proteins, distance, and time. Am J Physiol 282: G105–G115, 2002Google Scholar
  24. 24.
    Pratley RE, Baier L, Pan DA, Salbe AD, Storlien L, Ravussin E, Bogardus C: Effects of an Ala54Thr polymorphism in the intestinal fatty acid-binding protein on responses to dietary fat in humans. J Lipid Res 41: 2002–2008, 2000PubMedGoogle Scholar
  25. 25.
    Agren JJ, Vidgren HM, Valve RS, Laakso M, Uusitupa MI: Postprandial responses of individual fatty acids in subjects homozygous for the threonine-or alanine-encoding allelc in codon 54 of the intestinal fatty acid binding protein 2 gene. Am J Clin Nutr 73: 31–35, 2001PubMedGoogle Scholar
  26. 26.
    Georgopoulos A, Aras O, Tsai MY: Codon-54 polymorphism of the fatty acid-binding protein 2 gene is associated with elevation of fasting and postprandial triglyceride in type 2 diabetes. J Clin Endocrinol Metab 85: 3155–3160, 2000PubMedCrossRefGoogle Scholar
  27. 27.
    Lei HH, Coresh J, Shuldiner AR, Boerwinkle E, Brancati FL: Variants of the insulin receptor substrate-1 and fatty acid binding protein 2 genes and the risk of type 2 diabetes, obesity, and hyperinsulmemia in african-americans: The atherosclerosis risk in communities study. Diabetes 48: 1868–1872, 1999PubMedCrossRefGoogle Scholar
  28. 28.
    Tahvanaincn L, Molin M, Vainio S, Tiret L. Nicaud V, Farinaro E, Masana L, Ehnholm C: Intestinal fatty acid binding protein polymorphism at codon 54 is not associated with postprandial responses to fat and glucose tolerance tests in healthy young europeans. Results from EARS IT participants. Atherosclerosis 152: 317–325, 2000CrossRefGoogle Scholar
  29. 29.
    Levy E, Menard D, Delvin E, Stan S, Mitchell G, Lambert M, Ziv E, Feoli-Fonseca JC, Seidman E: The polymorphism at codon 54 of the FABP2 gene increases fat absorption in human intestinal explants. J Biol Chem 276: 39679–39684, 2001PubMedCrossRefGoogle Scholar
  30. 30.
    Vassileva G, Huwyler L, Poirier K, Agellon LBTM.I: The intestinal fatty acid binding protein is not essential for dietary fat absorption in mice. FASEB J 14: 2040–2046, 2000PubMedCrossRefGoogle Scholar
  31. 31.
    Baier LJ, Bogardus C, Sacchettini JC: A polymorphism in the human intestinal fatty acid binding protein alters fatty acid transport across Caco-2 cells. J Biol Chem 271: 10892–10896, 1996PubMedCrossRefGoogle Scholar
  32. 32.
    Darimont C, Gradoux N, Persohn E, Cumin F, De Pover A: Effects of intestinal fatty acid-binding protein overexpression on fatty acid metabolism in Caco-2 cells. J Lipid Res 41: 84–92, 2000PubMedGoogle Scholar
  33. 33.
    Binas B, Danncbcrg H, McWhir J, Mullins L, Clark AJ: Requirement for the heart-type fatty acid binding protein in cardiac fatty acid utilization. FASEB J 13: 805–812, 1999PubMedGoogle Scholar
  34. 34.
    Scheja L, Makowski L, Uysal KT, Wiesbrock SM, Shimshek DR, Meyers DS, Morgan M, Parker RA, Hotamisligil GS: Altered insulin secretion associated with reduced lipolytic efficiency in aP2 mice. Diabetes 48: 1987–1993, 1999PubMedCrossRefGoogle Scholar
  35. 35.
    Uysal KT, Scheja L. Wiesbrock SM, Bonner-Weir S, Hotamisligil GS: Improved glucose and lipid metabolism in genetically obese mice lacking aP2. Endocrinology 141: 3388–3396, 2000PubMedCrossRefGoogle Scholar
  36. 36.
    Shaughnessy S, Smith ER, Kodukula S, Storch J, Fried SK: Adipoeyte metabolism in adipocyte fatty acid binding protein knockout (aP2 ) mice after short-term high-fat feeding. Diabetes 49: 904–911, 2000PubMedCrossRefGoogle Scholar
  37. 37.
    Hotamisligil GS, Johnson RS, Distel RJ, Ellis R, Papaioannou VE, Spicgelman BM: Uncoupling of obesity from insulin resistance through a targeted mutation in aP2, the adipocyte fatty acid binding protein. Science 274: 1377–1379, 1996PubMedCrossRefGoogle Scholar
  38. 38.
    Coe NR, Simpson MA, Bcrnlohr D: Targeted disruption of the adipocyte lipid-binding protein (aP2 protein) gene impairs fat cell lipolysis and increases cellular fatty acid levels. J Lipid Res 40: 967–972, 1999PubMedGoogle Scholar
  39. 39.
    Pcrrella MA, Pcllacani A, Laync MD, Patel A, Zhao D, Schreiber BM, Storch J, Feinberg MW, Hsieh CM, Haber E, Lee ME: Absence of adipocyte fatty acid binding protein prevents the development of accelerated atherosclerosis in hypercholcsterolemic mice. FASEB J. 15: 1774–1776, 2001Google Scholar
  40. 40.
    Laync MD, Patel A, Chen YH, Rebel VI, Carvajal IM, Pellaeani A, Ith B, Zhao D, Schreiber BM, Yet SF, Lee ME, Storch J. Perrella MA: Role of macrophage-expressed adipocyte fatty acid-binding protein in the development of accelerated atherolselerosis in hypercholesterolcmic mice. FASLB J 15: 2733–3735, 2001Google Scholar
  41. 41.
    Makowski L, Boord JB, Maeda K, Babaev VR, Uysal KT, Morgan MA, Parker RA, Sultles J, Fazio S, Hotamisligil GS, Linton MF: Lack of macrophage fatty-acid-binding protein aP2 protects mice deficient in apolipoprotein L against atherosclerosis. Nature Med 7: 699–705, 2001PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2002

Authors and Affiliations

  • Judith Storch
    • 1
    • 3
  • Jacques H. Veerkamp
    • 2
  • Kuo-Tung Hsu
    • 1
  1. 1.Department of Nutritional SciencesRutgers UniversityNew BrunswickUSA
  2. 2.Department of BiochemistryUniversity of NijmegenNijmegenThe Netherlands
  3. 3.Department of Nutritional SciencesRutgers UniversityNew BrunswickUSA

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