Sequence and Structural Analysis of Cellular Retinoic Acid-Binding Proteins Reveals a Network of Conserved Hydrophobic Interactions

Proteins: Structure, Function and Genetics

Volumn 54, Issue 2, 2004, Pages 179-194

  Gunasekaran, Kannan ^a,b   Hagler, Arnold T ^a   Gierasch, Lila M ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

structure; Binary code; Cellular retinoic acid binding protein; Hydrophobic core; Intracellular lipid binding proteins; Pair wise correlations; Protein folding; Sequence conservation

Indexed keywords

CELLULAR RETINOIC ACID BINDING PROTEIN I; RETINOIC ACID BINDING PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; HUMAN; HYDROPHOBICITY; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN INTERACTION; PROTEIN STRUCTURE; RAT; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; CARRIER PROTEINS; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; FATTY ACID-BINDING PROTEINS; HYDROPHOBICITY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEOPLASM PROTEINS; ORGANIC ANION TRANSPORTERS, SODIUM-DEPENDENT; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, RETINOIC ACID; SEQUENCE ALIGNMENT; SYMPORTERS;

EID: 0347089152     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/prot.10520     Document Type: Article

References (67)

1. Anfinsen CB. Principles that govern the folding of protein chains. Science 1973;181:223-230.
2. Lattman EE, Rose GD. Protein folding - what's the question? Proc Natl Acad Sci USA 1993;90:439-441.
3. Cordes MHJ, Davidson AR, Sauer RT. Sequence space, folding and protein design. Curr Opin Struct Biol 1996;6:3-10.
4. Dalal S, Balasubramanian S, Regan L. Protein alchemy: changing β-sheet into α-helix. Nat Struct Biol 1997;4:548-552.
5. Yuan S-M, Clarke ND. A hybrid sequence approach to the paracelsus challenge. Proteins 1998;30:136-143.
6. Matthews BW. Structural and genetic analysis of protein stability. Annu Rev Biochem 1993;62:139-160.
7. Bowie JU, Reidhaar-Olson JF, Lim WA, Sauer RT. Deciphering the message in protein sequences: tolerance to amino acid substitutions. Science 1990;247:1306-1310.
8. Shakhnovich E, Abkevich V, Ptitsyn OB. Conserved residues and the mechanism of protein folding. Nature 1996;379:96-98.
9. Ptitsyn OB. Protein folding and protein evolution: common folding nucleus in different subfamilies of c-type cytochromes? J Mol Biol 1998;278:655-666.
10. Clarke J, Cota E, Fowler SB, Hamill SJ. Folding studies of immunoglobulin-like β-sandwich proteins suggest that they share a common folding pathway. Structure Fold Design 1999;7:1145-1153.
11. Kragelund BB, Osmark P, Neergaard TB, Schiødt J, Kristiansen K, Knudsen J, Poulsen FM, The formation of a native-like structure containing eight conserved hydrophobic residues is rate limiting in two-state protein folding of ACBP. Nat Struct Biol 1999;6:594-601.
12. Shindyalov IN, Kolchanov NA, Sander C. Can three-dimensional contacts in protein structures be predicted by analysis of correlated mutations? Protein Eng 1994;7:349-358.
13. Neher E. How frequent are correlated changes in families of protein sequences? Proc Natl Acad Sci USA 1994;91:98-102.
14. Oliveira L, Paiva AC, Vriend G. Correlated mutation analyses on very large sequence families. Chembiochem 2002;3:1010-1017.
15. Olmea O, Rost B, Valencia A. Effective use of sequence correlation and conservation in fold recognition. J Mol Biol 1999;293:1221-1239.
16. Mandel-Gutfreund Y, Zaremba SM, Gregoret LM. Contributions of residue pairing to β-sheet formation: conservation and co-variation of amino acid residue pairs on antiparallel β-strands. J Mol Biol 2001;305:1145-1159.
17. Kass I, Horovitz A. Mapping pathways of allosteric communication in GroEL by analysis of correlated mutations. Proteins 2002;48:611-617.
18. Rigden DJ. Use of covariance analysis for the prediction of structural domain boundaries from multiple protein sequence alignments. Protein Eng 2002;15:65-77.
19. Clark PL, Liu Z-P, Rizo J, Gierasch LM. Cavity formation before stable hydrogen bonding in the folding of a β-clam protein. Nat Struct Biol 1997;4:883-886.
20. Banaszak L, Winter N, Xu Z, Bernlohr DA, Cowan S, Jones TA. Lipid-binding proteins: a family of fatty acid and retinoid transport proteins. Adv Protein Chem 1994;45:89-151.
21. Bernlohr DA, Simpson MA, Hertzel AV, Banaszak LJ. Intracellular lipid-binding proteins and their genes. Annu Rev Nutr 1997;17:277-303.
22. Coe NR, Bernlohr DA. Physiological properties and functions of intracellular fatty acid-binding proteins. Biochim Biophys Acta 1998;1391:287-306.
23. Jones TA, Bergfors T, Sedzik J, Unge T. The three-dimensional structure of P2 myelin protein. EMBO J 1988;7:1597-1604.
24. Kleywegt GJ, Bergfors T, Senn H, Le Motte P, Gsell B, Shudo K, Jones TA. Crystal structures of cellular retinoic acid binding proteins I and II in complex with all-trans-retinoic acid and a synthetic retinoid. Structure 1994;2:1241-1258.
25. Thompson JR, Bratt JM, Banaszak LJ. Crystal structure of cellular retinoic acid binding protein I shows increased access to the binding cavity due to formation of an intermolecular β-sheet. J Mol Biol 1995;252:433-446.
26. Cowan SW, Newcomer ME, Jones TA. Crystallographic studies on a family of cellular lipophilic transport proteins. Refinement of P2 myelin protein and the structure determination and refinement of cellular retinol-binding protein in complex with all-trans-retinol. J Mol Biol 1993;230:1225-1246.
27. Xu Z, Bernlohr DA, Banaszak LJ. The adipocyte lipid-binding protein at 1.6Å resolution. Crystal structures of the apoprotein and with bound saturated and unsaturated fatty acids. J Biol Chem 1993;268:7874-7884.
28. Young AC, Scapin G, Kromminga A, Patel SB, Veerkamp JH, Sacchettini JC. Structural studies on human muscle fatty acid binding protein at 1.4Å resolution: binding interactions with three C18 fatty acids. Structure 1994;2:523-534.
29. Haunerland NH, Jacobson BL, Wesenberg G, Rayment I, Holden HM. Three-dimensional structure of the muscle fatty-acid-binding protein isolated from the desert locust Schistocerca gregaria. Biochemistry 1994;33:12378-12385.
30. Winter NS, Bratt JM, Banaszak LJ. Crystal structures of holo- and apo-cellular retinol-binding protein II. J Mol Biol 1993;230:1247-1259.
31. Sanchez R, Sali A. Advances in comparative protein-structure modeling. Curr Opin Struct Biol 1997;7:206-214.
32. Rost B, Eyrich VA. EVA: large-scale analysis of secondary structure prediction. Proteins 2001;Suppl 5:192-199.
33. Dobson CM. Protein folding and disease: a view from the first Horizon Symposium. Nat Rev Drug Discov 2003;2:154-160.
34. Sander C, Schneider R. Database of homology-derived protein structures and the structural meaning of sequence alignment. Proteins 1991;9:56-68.
35. Rost B. Twilight zone of protein sequence alignments. Protein Eng 1999;12:85-94.
36. Thompson JD, Plewniak F, Poch O. A comprehensive comparison of multiple sequence alignment programs. Nucleic Acids Res 1999;27:2682-2690.
37. Dayhoff MO, Schwartz RM, Orcutt BC. In: Dayhoff MO, editor. Atlas of protein sequence and structure Washington: NBRF; 1978;5 Suppl 3:345.
38. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994;22:4673-4680.
39. Dill KA. Polymer principles and protein folding. Protein Sci 1999;8:1166-1180.
40. Kamtekar S, Schiffer JM, Xiong H, Babik JM, Hecht MH. Protein design by binary patterning of polar and non-polar amino acids. Science 1993;262:1680-1685.
41. Sweet RM, Eisenberg D. Correlation of sequence hydrophobicities measures similarity in three-dimensional protein structure. J Mol Biol 1983;171:479-488.
42. Bashford D, Chothia C, Lesk AM. Determinants of a protein fold. Unique features of the globin amino acid sequences. J Mol Biol 1987;196:199-216.
43. Huang ES, Subbiah S, Levitt M. Recognizing native folds by the arrangement of hydrophobic and polar residues. J Mol Biol 1995;252:709-720.
44. Dougherty DA. Cation-π interactions in chemistry and biology: a new view of benzene, Phe, Tyr and Trp. Science 1996;271:163-168.
45. Steiner T, Koellner G. Hydrogen bonds with π-acceptors in proteins: frequencies and role in stabilizing local 3D structures. J Mol Biol 2001;305:535-557.
46. Kraulis PJ. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 1991;24:946-995.
47. Merritt EA, Bacon DJ. RASTER3D: photorealistic molecular graphics. Methods Enzymol 1997;277:505-524.
48. Sukumar M, Gierasch LM. Local interactions in a Schellman motif dictate interhelical arrangement in a protein fragment. Fold Design 1997;2:211-222.
49. Aurora R, Srinivasan R, Rose GD. Rules for α-helix termination by glycine. Science 1994;264:1126-1130.
50. Gunasekaran K, Nagarajaram HA, Ramakrishnan C, Balaram P. Stereochemical punctuation marks in protein structures: glycine and proline containing helix stop signals. J Mol Biol 1998;275:917-932.
51. 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 1996;35:1296-1303.
52. 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 1998;95:12174-12178.
53. Zhang J, Liu Z-P, Jones TA, Gierasch LM, Sambrook JF. Mutating the charged residues in the binding pocket of cellular retinoic acid-binding protein simultaneously reduces its binding affinity to retinoic acid and increases its thermostability. Proteins 1992;13:87-99.
54. Shaknovich E, Abkevich V, Ptitsyn OB. Conserved residues and the mechanism of protein folding. Nature 1996;379:96-98.
55. Nikiforovich GV, Frieden C. The search for local native-like nucleation centers in the unfolded state of β-sheet proteins. Proc Natl Acad Sci 2002;99:10388-10393.
56. Clark PL, Weston BF, Gierasch LM. Probing the folding pathway of a β-clam protein with single-tryptophan constructs. Fold Design 1998;3:401-412.
57. Clark PL, Liu ZP, Zhang J, Gierasch LM. Intrinsic tryptophans of CRABPI as probes of structure and folding. Protein Sci 1996;5:1108-1117.
58. Eyles SJ, Gierasch LM. Multiple roles of prolyl residues in structure and folding. J Mol Biol 2000;301:737-747.
59. Kim K, Ramanathan R, Frieden C. Intestinal fatty acid binding protein: a specific residue in one turn appears to stabilize the native structure and be responsible for slow refolding. Protein Sci 1997;6:364-372.
60. Grantcharova VP, Riddle DS, Santiago JV, Baker D. Important role of hydrogen bonds in the structurally polarized transition state for folding of the src SH3 domain. Nat Struct Biol 1998;5:714-720.
61. Guerois R, Serrano L. The SH3-fold family: experimental evidence and prediction of variations in the folding pathways. J Mol Biol 2000;304:967-982.
62. Kim K, Cistola DP, Frieden C. Intestinal fatty acid-binding protein: the structure and stability of a helix-less variant. Biochemistry 1996;35:7553-7558.
63. Dalessio PM, Ropson IJ. β-sheet proteins with nearly identical structures have different folding intermediates. Biochemistry 2000;39:860-871.
64. Gunasekaran K, Eyles SJ, Hagler AT, Gierasch LM. Keeping it in the family: folding studies of related proteins. Curr Opin Struct Biol 2001;11:83-93.
65. Gazit E. A possible role for pi-stacking in the self-assembly of amyloid fibrils. FASEB J 2002;16:77-83.
66. Fersht A. Structure and mechanism in protein science: a guide to enzyme catalysis and protein folding. New York: W.H. Freeman & Co; 1999. p 558-562.
67. Rotondi KS, Gierasch LM. Role of local sequence in the folding of cellular retinoic acid binding protein I: propensities of turns. Biochemistry 2003;42:7976-7985.