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Solution structure of human intestinal fatty acid binding protein: implications for ligand entry and exit.

Zhang F, Lücke C, Baier LJ, Sacchettini JC, Hamilton JA
J Biomol NMR 9 213-28 (1997)
Cited: 43 times
EuropePMC logo PMID: 9204553

Abstract

The human intestinal fatty acid binding protein (I-FABP) is a small (131 amino acids) protein which binds dietary long-chain fatty acids in the cytosol of enterocytes. Recently, an alanine to threonine substitution at position 54 in I-FABP has been identified which affects fatty acid binding and transport, and is associated with the development of insulin resistance in several populations including Mexican-Americans and Pima Indians. To investigate the molecular basis of the binding properties of I-FABP, the 3D solution structure of the more common form of human I-FABP (Ala54) was studied by multidimensional NMR spectroscopy. Recombinant I-FABP was expressed from E. coli in the presence and absence of 15N-enriched media. The sequential assignments for non-delipidated I-FABP were completed by using 2D homonuclear spectra (COSY, TOCSY and NOESY) and 3D heteronuclear spectra (NOESY-HMQC and TOCSY-HMQC). The tertiary structure of human I-FABP was calculated by using the distance geometry program DIANA based on 2519 distance constraints obtained from the NMR data. Subsequent energy minimization was carried out by using the program SYBYL in the presence of distance constraints. The conformation of human I-FABP consists of 10 antiparallel beta-strands which form two nearly orthogonal beta-sheets of five strands each, and two short alpha-helices that connect the beta-strands A and B. The interior of the protein consists of a water-filled cavity between the two beta-sheets. The NMR solution structure of human I-FABP is similar to the crystal structure of rat I-FABP. The NMR results show significant conformational variability of certain backbone segments around the postulated portal region for the entry and exit of fatty acid ligand.

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  1. Predicting the accuracy of protein-ligand docking on homology models. Bordogna A, Pandini A, Bonati L. J Comput Chem 32 81-98 (2011)
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  1. Insights into binding of fatty acids by fatty acid binding proteins. Hanhoff T, Lücke C, Spener F. Mol Cell Biochem 239 45-54 (2002)
  2. Intracellular lipid binding proteins of the small intestine. Agellon LB, Toth MJ, Thomson AB. Mol Cell Biochem 239 79-82 (2002)
  3. How fatty acids bind to proteins: the inside story from protein structures. Hamilton JA. Prostaglandins Leukot Essent Fatty Acids 67 65-72 (2002)
  4. Survey of binding properties of fatty acid-binding proteins. Chromatographic methods. Massolini G, Calleri E. J Chromatogr B Analyt Technol Biomed Life Sci 797 255-268 (2003)
  5. Genetic predictors of plasma lipid response to diet intervention. Ordovas JM, Galluzzi JR. Curr Atheroscler Rep 1 196-203 (1999)

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  2. Solution structure and backbone dynamics of human epidermal-type fatty acid-binding protein (E-FABP). Gutiérrez-González LH, Ludwig C, Hohoff C, Rademacher M, Hanhoff T, Rüterjans H, Spener F, Lücke C. Biochem J 364 725-737 (2002)
  3. Solution structure and backbone dynamics of human liver fatty acid binding protein: fatty acid binding revisited. Cai J, Lücke C, Chen Z, Qiao Y, Klimtchuk E, Hamilton JA. Biophys J 102 2585-2594 (2012)
  4. Interactions between fatty acids and alpha-synuclein. Lücke C, Gantz DL, Klimtchuk E, Hamilton JA. J Lipid Res 47 1714-1724 (2006)
  5. Insights into the bile acid transportation system: the human ileal lipid-binding protein-cholyltaurine complex and its comparison with homologous structures. Kurz M, Brachvogel V, Matter H, Stengelin S, Thüring H, Kramer W. Proteins 50 312-328 (2003)
  6. Solution structure of ileal lipid binding protein in complex with glycocholate. Lücke C, Zhang F, Hamilton JA, Sacchettini JC, Rüterjans H. Eur J Biochem 267 2929-2938 (2000)
  7. The structure and dynamics of rat apo-cellular retinol-binding protein II in solution: comparison with the X-ray structure. Lu J, Lin CL, Tang C, Ponder JW, Kao JL, Cistola DP, Li E. J Mol Biol 286 1179-1195 (1999)
  8. Applications of NMR in drug discovery. Roberts GC. Drug Discov Today 5 230-240 (2000)
  9. Crystallographic study of FABP5 as an intracellular endocannabinoid transporter. Sanson B, Wang T, Sun J, Wang L, Kaczocha M, Ojima I, Deutsch D, Li H. Acta Crystallogr D Biol Crystallogr 70 290-298 (2014)
  10. Turn scanning by site-directed mutagenesis: application to the protein folding problem using the intestinal fatty acid binding protein. Kim K, Frieden C. Protein Sci 7 1821-1828 (1998)
  11. Characterization of the binding of drugs to human intestinal fatty acid binding protein (IFABP): potential role of IFABP as an alternative to albumin for in vitro-in vivo extrapolation of drug kinetic parameters. Rowland A, Knights KM, Mackenzie PI, Miners JO. Drug Metab Dispos 37 1395-1403 (2009)
  12. A comparative study of the backbone dynamics of two closely related lipid binding proteins: bovine heart fatty acid binding protein and porcine ileal lipid binding protein. Lücke C, Fushman D, Ludwig C, Hamilton JA, Sacchettini JC, Rüterjans H. Mol Cell Biochem 192 109-121 (1999)
  13. Fatty acid binding proteins: same structure but different binding mechanisms? Molecular dynamics simulations of intestinal fatty acid binding protein. Friedman R, Nachliel E, Gutman M. Biophys J 90 1535-1545 (2006)
  14. Spin-system heterogeneities indicate a selected-fit mechanism in fatty acid binding to heart-type fatty acid-binding protein (H-FABP). Lücke C, Rademacher M, Zimmerman AW, van Moerkerk HT, Veerkamp JH, Rüterjans H. Biochem J 354 259-266 (2001)
  15. Examination of the role of intestinal fatty acid-binding protein in drug absorption using a parallel artificial membrane permeability assay. Velkov T, Horne J, Laguerre A, Jones E, Scanlon MJ, Porter CJ. Chem Biol 14 453-465 (2007)
  16. Intestinal-fatty acid binding protein and lipid transport in human intestinal epithelial cells. Montoudis A, Delvin E, Menard D, Beaulieu JF, Jean D, Tremblay E, Bendayan M, Levy E. Biochem Biophys Res Commun 339 248-254 (2006)
  17. Peptides corresponding to the N- and C-terminal parts of PEBP are well-structured in solution: new insights into their possible interaction with partners in vivo. Vallée BS, Coadou G, Labbé H, Sy D, Vovelle F, Schoentgen F. J Pept Res 61 47-57 (2003)
  18. Measurement of methyl 13C-1H cross-correlation in uniformly 13C-, 15N-, labeled proteins. Liu W, Zheng Y, Cistola DP, Yang D. J Biomol NMR 27 351-364 (2003)
  19. Differences between apo and three holo forms of the intestinal fatty acid binding protein seen by molecular dynamics computer calculations. Woolf TB, Grossfield A, Tychko M. Biophys J 78 608-625 (2000)
  20. Letter Solution structure of chicken liver basic fatty acid binding protein. Vasile F, Ragona L, Catalano M, Zetta L, Perduca M, Monaco H, Molinari H. J Biomol NMR 25 157-160 (2003)
  21. Solution structure of fatty acid-binding protein from human brain. Rademacher M, Zimmerman AW, Rüterjans H, Veerkamp JH, Lücke C. Mol Cell Biochem 239 61-68 (2002)
  22. Measurement of dipolar cross-correlation in methylene groups in uniformly 13C-, 15N-labeled proteins. Zheng Y, Yang D. J Biomol NMR 28 103-116 (2004)
  23. Genetic variation of the intestinal fatty acid-binding protein 2 gene in carotid atherosclerosis. Wanby P, Palmquist P, Brudin L, Carlsson M. Vasc Med 10 103-108 (2005)
  24. Identification of structural transitions in bacterial fatty acid binding proteins that permit ligand entry and exit at membranes. Gullett JM, Cuypers MG, Grace CR, Pant S, Subramanian C, Tajkhorshid E, Rock CO, White SW. J Biol Chem 298 101676 (2022)
  25. Polymorphism of the FABP2 gene: a population frequency analysis and an association study with cardiovascular risk markers in Argentina. Gomez LC, Real SM, Ojeda MS, Gimenez S, Mayorga LS, Roqué M. BMC Med Genet 8 39 (2007)
  26. Evidence of chemical exchange in recombinant Major Urinary Protein and quenching thereof upon pheromone binding. Perazzolo C, Verde M, Homans SW, Bodenhausen G. J Biomol NMR 38 3-9 (2007)
  27. Identification and expression analysis of fabp2 gene from common carp Cyprinus carpio. Chen XW, Jiang S, Shi ZY. J Fish Biol 80 679-691 (2012)
  28. Increased plasma levels of asymmetric dimethylarginine in patients with carotid stenosis: no evidence for the role of the common FABP2 A54T gene polymorphism. Wanby P, Nilsson I, Brudin L, Nyhammar I, Gustafsson I, Carlsson M. Acta Neurol Scand 115 90-96 (2007)
  29. The FABP2 gene polymorphism in cerebrovascular disease. Wanby P, Palmquist P, Rydén I, Brattström L, Carlsson M. Acta Neurol Scand 110 355-360 (2004)
  30. 1H, 15N and 13C resonance assignments and secondary structure of apo liver fatty acid-binding protein. Wang H, He Y, Hsu KT, Magliocca JF, Storch J, Stark RE. J Biomol NMR 12 197-199 (1998)
  31. Gene expression profiles of FABP genes in protochordates, Ciona intestinalis and Branchiostoma belcheri. Orito W, Ohhira F, Ogasawara M. Cell Tissue Res 362 331-345 (2015)
  32. Effects of ligand binding on dynamics of fatty acid binding protein and interactions with membranes. Lu Y, Yang GZ, Yang D. Biophys J 121 4024-4032 (2022)
  33. Model of β-Sheet of Muscle Fatty Acid Binding Protein of Locusta migratoria Displays Characteristic Topology. Kizilbash NA, Hai A, Alruwaili J. Bioinformation 9 1003-1009 (2013)


Related citations provided by authors (3)

  1. A Polymorphism in the Human Intestinal Fatty Acid Binding Protein Alters Fatty Acid Transport Across Caco-2 Cells. Baier LJ, Bogardus C, Sacchettini JC J. Biol. Chem. 271 10892- (1996)
  2. 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. Baier LJ, Sacchettini JC, Knowler WC, Eads J, Paolisso G, Tataranni PA, Mochizuki H, Bennet PH, Bogardus C, Prochazka M J. Clin. Invest. 95 1281- (1995)
  3. Refinement of the Structure of Recombinant Rat Intestinal Fatty Acid-Binding Apoprotein at 1.2-Angstroms Resolution. Scapin G, Gordon JI, Sacchettini JC J. Biol. Chem. 267 4253- (1992)

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