Structural and mutational analyses of protein-protein interactions between transthyretin and retinol-binding protein

FEBS Journal

Volumn 275, Issue 23, 2008, Pages 5841-5854

  Zanotti, Giuseppe ^a,b   Folli, Claudia ^c   Cendron, Laura ^a,b   Alfieri, Beatrice ^c   Nishida, Sonia K ^d   Gliubich, Francesca ^a,e   Pasquato, Nicola ^a   Negro, Alessandro ^a   Berni, Rodolfo ^c  

^a UNIVERSITY OF PADOVA   (Italy)

^b VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^c UNIVERSITY OF PARMA   (Italy)

^d FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^e KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Fab; Mutational analysis; Protein protein interactions; Retinol binding protein; Transthyretin

Indexed keywords

HYDROXYL GROUP; IMMUNOGLOBULIN F(AB) FRAGMENT; ISOLEUCINE; PREALBUMIN; PROTEIN SUBUNIT; RETINOL BINDING PROTEIN; SERINE;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CRYSTAL STRUCTURE; HUMAN; HYDROPHILICITY; HYDROPHOBICITY; MOLECULAR RECOGNITION; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; STOICHIOMETRY;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; FLUORESCENCE POLARIZATION; HUMANS; HYDROGEN BONDING; HYDROPHOBICITY; IMMUNOGLOBULIN FAB FRAGMENTS; MICE; MODELS, MOLECULAR; PREALBUMIN; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RETINOL-BINDING PROTEINS, PLASMA; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

MURINAE; PISCES;

EID: 55949120463     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2008.06705.x     Document Type: Article

References (59)

1. Richardson SJ, Monk JA, Shepherdley CA, Ebbesson LO, Sin F, Power DM, Frappell PB, Kohrle J Renfree MB (2005) Developmentally regulated thyroid hormone distributor proteins in marsupials, a reptile, and fish. Am J Physiol Regul Integr Comp Physiol 288, R1264 R1272.
2. Ramazzina I, Folli C, Secchi A, Berni R Percudani R (2006) Completing the uric acid degradation pathway through phylogenetic comparison of whole genomes. Nat Chem Biol 2, 144 148.
3. Hennebry SC, Law RH, Richardson SJ, Buckle AM Whisstock JC (2006) The crystal structure of the transthyretin-like protein from Salmonella dublin, a prokaryote 5-hydroxyisourate hydrolase. J Mol Biol 359, 1389 1399.
4. Jung DK, Lee Y, Park SG, Park BC, Kim GH Rhee S (2006) Structural and functional analysis of PucM, a hydrolase in the ureide pathway and a member of the transthyretin-related protein family. Proc Natl Acad Sci USA 103, 9790 9795.
5. Zanotti G, Cendron L, Ramazzina I, Folli C, Percudani R Berni R (2006) Structure of zebra fish HIUase: Insights into evolution of an enzyme to a hormone transporter. J Mol Biol 363, 1 9.
6. Lundberg E, Backstrom S, Sauer UH Sauer-Eriksson AE (2006) The transthyretin-related protein: structural investigation of a novel protein family. J Struct Biol 155, 445 457.
7. Goodman DS 1984) Plasma retinol-binding protein. In The Retinoids (Sporn MB, Roberts AB Goodman DS, eds), pp. 41 88. Academic Press, New York, NY.
8. Zanotti G Berni R (2004) Plasma retinol-binding protein: structure and interactions with retinol, retinoids, and transthyretin. Vitam Horm 69, 271 295.
9. Kawaguchi R, Yu J, Honda J, Hu J, Whitelegge J, Ping P, Wiita P, Bok D Sun H (2007) A membrane receptor for retinol binding protein mediates cellular uptake of vitamin A. Science 315, 820 825.
10. Redondo C, Vouropoulou M, Evans J Findlay JB (2008) Identification of the retinol-binding protein (RBP) interaction site and functional state of RBPs for the membrane receptor. FASEB J 22, 1043 1054.
11. Goodman DS Raz A (1972) Extraction and recombination studies of the interaction of retinol with human plasma retinol-binding protein. J Lipid Res 13, 338 347.
12. Folli C, Viglione S, Busconi M Berni R (2005) Biochemical basis for retinol deficiency induced by the I41N and G75D mutations in human plasma retinol-binding protein. Biochem Biophys Res Commun 336, 1017 1022.
13. Episkopou V, Maeda S, Nishiguchi S, Shimada K, Gaitanaris GA, Gottesman ME Robertson EJ (1993) Disruption of the transthyretin gene results in mice with depressed levels of plasma retinol and thyroid hormone. Proc Natl Acad Sci USA 90, 2375 2379.
14. Quadro L, Blaner WS, Salchow DJ, Vogel S, Piantedosi R, Gouras P, Freeman S, Cosma MP, Colantuoni V Gottesman ME (1999) Impaired retinal function and vitamin A availability in mice lacking retinol-binding protein. EMBO J 18, 4633 4644.
15. van Bennekum AM, Wei S, Gamble MV, Vogel S, Piantedosi R, Gottesman M, Episkopou V Blaner WS (2001) Biochemical basis for depressed serum retinol levels in transthyretin-deficient mice. J Biol Chem 276, 1107 1113.
16. Fex G, Albertsson PA Hansson B (1979) Interaction between prealbumin and retinol-binding protein studied by affinity chromatography, gel filtration and two-phase partition. Eur J Biochem 99, 353 360.
17. Malpeli G, Folli C Berni R (1996) Retinoid binding to retinol-binding protein and the interference with the interaction with transthyretin. Biochim Biophys Acta 1294, 48 54.
18. Damas AM Saraiva MJ (2000) Review: TTR amyloidosis-structural features leading to protein aggregation and their implications on therapeutic strategies. J Struct Biol 130, 290 299.
19. Benson MD Kincaid JC (2007) The molecular biology and clinical features of amyloid neuropathy. Muscle Nerve 36, 411 423.
20. Buxbaum JN, Ye Z, Reixach N, Friske L, Levy C, Das P, Golde T, Masliah E, Roberts AR Bartfai T (2008) Transthyretin protects Alzheimer's mice from the behavioral and biochemical effects of Abeta toxicity. Proc Natl Acad Sci USA 105, 2681 2686.
21. Costa R, Goncalves A, Saraiva MJ Cardoso I (2008) Transthyretin binding to A-Beta peptide - impact on A-Beta fibrillogenesis and toxicity. FEBS Lett 582, 936 942.
22. Yang Q, Graham TE, Mody N, Preitner F, Peroni OD, Zabolotny JM, Kotani K, Quadro L Kahn BB (2005) Serum retinol binding protein 4 contributes to insulin resistance in obesity and type 2 diabetes. Nature 436, 356 362.
23. Blake CC, Geisow MJ, Oatley SJ, Rerat B Rerat C (1978) Structure of prealbumin: secondary, tertiary and quaternary interactions determined by Fourier refinement at 1.8 A. J Mol Biol 121, 339 356.
24. Wojtczak A (1997) Crystal structure of rat transthyretin at 2.5 A resolution: first report on a unique tetrameric structure. Acta Biochim Pol 44, 505 517.
25. Hornberg A, Eneqvist T, Olofsson A, Lundgren E Sauer-Eriksson AE (2000) A comparative analysis of 23 structures of the amyloidogenic protein transthyretin. J Mol Biol 302, 649 669.
26. Sunde M, Richardson SJ, Chang L, Pettersson TM, Schreiber G Blake CC (1996) The crystal structure of transthyretin from chicken. Eur J Biochem 236, 491 499.
27. Folli C, Pasquato N, Ramazzina I, Battistutta R, Zanotti G Berni R (2003) Distinctive binding and structural properties of piscine transthyretin. FEBS Lett 555, 279 284.
28. Eneqvist T, Lundberg E, Karlsson A, Huang S, Santos CR, Power DM Sauer-Eriksson AE (2004) High resolution crystal structures of piscine transthyretin reveal different binding modes for triiodothyronine and thyroxine. J Biol Chem 279, 26411 26416.
29. Cowan SW, Newcomer ME Jones TA (1990) Crystallographic refinement of human serum retinol binding protein at 2A resolution. Proteins 8, 44 61.
30. Zanotti G, Ottonello S, Berni R Monaco HL (1993) Crystal-structure of the trigonal form of human plasma retinol-binding protein at 2.5-angstrom resolution. J Mol Biol 230, 613 624.
31. Zanotti G, Berni R Monaco HL (1993) Crystal-structure of liganded and unliganded forms of bovine plasma retinol-binding protein. J Biol Chem 268, 10728 10738.
32. Zanotti G, Panzalorto M, Marcato A, Malpeli G, Folli C Berni R (1998) Structure of pig plasma retinol-binding protein at 1.65 angstrom resolution. Acta Crystallogr D Biol Crystallogr 54, 1049 1052.
33. Calderone V, Berni R Zanotti G (2003) High-resolution structures of retinol-binding protein in complex with retinol: pH-induced protein structural changes in the crystal state. J Mol Biol 329, 841 850.
34. Zanotti G, Calderone V, Beda M, Malpeli G, Folli C Berni R (2001) Structure of chicken plasma retinol-binding protein. Biochim Biophys Acta-Protein Struct Molec Enzym 1550, 64 69.
35. Monaco HL, Rizzi M Coda A (1995) Structure of a complex of two plasma proteins: transthyretin and retinol-binding protein. Science 268, 1039 1041.
36. Naylor HM Newcomer ME (1999) The structure of human retinol-binding protein (RBP) with its carrier protein transthyretin reveals an interaction with the carboxy terminus of RBP. Biochemistry 38, 2647 2653.
37. Berni R, Malpeli G, Folli C, Murrell JR, Liepnieks JJ Benson MD (1994) The Ile-84 - >Ser amino acid substitution in transthyretin interferes with the interaction with plasma retinol-binding protein. J Biol Chem 269, 23395 23398.
38. Waits RP, Yamada T, Uemichi T Benson MD (1995) Low plasma concentrations of retinol-binding protein in individuals with mutations affecting position 84 of the transthyretin molecule. Clin Chem 41, 1288 1291.
39. Pasquato N, Berni R, Folli C, Alfieri B, Cendron L Zanotti G (2007) Acidic pH-induced conformational changes in amyloidogenic mutant transthyretin. J Mol Biol 366, 711 719.
40. Kopelman M, Cogan U, Mokady S Shinitzky M (1976) The interaction between retinol-binding proteins and prealbumins studied by fluorescence polarization. Biochim Biophys Acta 439, 449 460.
41. Schwede T, Kopp J, Guex N Peitsch MC (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31, 3381 3385.
42. Berni R, Stoppini M Zapponi MC (1992) The piscine plasma retinol-binding protein. Purification, partial amino acid sequence and interaction with mammalian transthyretin of rainbow trout (Oncorhynchus mykiss) retinol-binding protein. Eur J Biochem 204, 99 106.
43. Berni R, Clerici M, Malpeli G, Cleris L Formelli F (1993) Retinoids: in vitro interaction with retinol-binding protein and influence on plasma retinol. FASEB J 7, 1179 1184.
44. Zanotti G, Marcello M, Malpeli G, Folli C, Sartori G Berni R (1994) Crystallographic studies on complexes between retinoids and plasma retinol-binding protein. J Biol Chem 269, 29613 29620.
45. Tragardh L, Anundi H, Rask L, Sege K Peterson PA (1980) On the stoichiometry of the interaction between prealbumin and retinol-binding protein. J Biol Chem 255, 9243 9248.
46. Shidoji Y Muto Y (1977) Vitamin A transport in plasma of the non-mammalian vertebrates: isolation and partial characterization of piscine retinol-binding protein. J Lipid Res 18, 679 691.
47. Pereira AB, Nishida SK, Vieira JG, Lombardi MT, Silva MS, Ajzen H Ramos OL (1993) Monoclonal antibody-based immunoenzymometric assays of retinol-binding protein. Clin Chem 39, 472 476.
48. Orlandi R, Gussow DH, Jones PT Winter G (1989) Cloning immunoglobulin variable domains for expression by the polymerase chain reaction. Proc Natl Acad Sci USA 86, 3833 3837.
49. Malpeli G, Zanotti G, Gliubich F, Rizzotto A, Nishida SK, Folli C Berni R (1999) Crystallization and preliminary X-ray data for the human transthyretin-retinol-binding protein (RBP) complex bound to an anti-REP Fab. Acta Crystallogr D Biol Crystallogr 55, 276 278.
50. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS et al. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54, 905 921.
51. Murshudov GN, Vagin AA Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53, 240 255.
52. Emsley P Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60, 2126 2132.
53. Laskowski RA, Macarthur MW, Moss DS Thornton JM (1993) Procheck - a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26, 283 291.
54. Collaborative Computational Project, Number 4. (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50, 760 763.
55. Hamilton JA, Steinrauf LK, Braden BC, Liepnieks J, Benson MD, Holmgren G, Sandgren O Steen L (1993) The x-ray crystal structure refinements of normal human transthyretin and the amyloidogenic Val-30 - >Met variant to 1.7-A resolution. J Biol Chem 268, 2416 2424.
56. Sebastiao MP, Saraiva MJ Damas AM (1998) The crystal structure of amyloidogenic Leu55 - > Pro transthyretin variant reveals a possible pathway for transthyretin polymerization into amyloid fibrils. J Biol Chem 273, 24715 24722.
57. Schormann N, Murrell JR Benson MD (1998) Tertiary structures of amyloidogenic and non-amyloidogenic transthyretin variants: new model for amyloid fibril formation. Amyloid 5, 175 187.
58. Thompson JD, Higgins DG Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673 4680.
59. Gouet P, Courcelle E, Stuart DI Metoz F (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15, 305 308.