Structural dynamics and folding of β-lactoglobulin probed by heteronuclear NMR

Biochimica et Biophysica Acta - General Subjects

Volumn 1790, Issue 6, 2009, Pages 527-537

  Sakurai, Kazumasa ^a   Konuma, Tsuyoshi ^a   Yagi, Masanori ^a   Goto, Yuji ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Lactoglobulin; Conformational dynamics; Heteronuclear NMR; Ligand binding; Protein folding; Tanford transition

Indexed keywords

BETA LACTOGLOBULIN; DISULFIDE; LIPOCALIN; THIOL;

DENATURATION; HETERONUCLEAR NUCLEAR MAGNETIC RESONANCE; LIGAND BINDING; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MOLECULAR SIZE; NONHUMAN; PH; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; REVIEW; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ANIMALS; CATTLE; DIMERIZATION; LACTOGLOBULINS; LIGANDS; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; RECOMBINANT PROTEINS;

BOVINAE;

EID: 67349093283     PISSN: 03044165     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbagen.2009.04.003     Document Type: Review

References (122)

1. Pervaiz S., and Brew K. Homology of β-lactoglobulin, serum retinol-binding protein, and protein HC. Science 228 (1985) 335-337
2. Godovac-Zimmermann J. The structural motif of β-lactoglobulin and retinol-binding protein: a basic framework for binding and transport of small hydrophobic molecules?. Trends Biochem. Sci. 13 (1988) 64-66
3. Hambling S.G., MacAlpine A.S., and Sawyer L. β-lactoglobulin. In: Fox P.F. (Ed). Advanced Dairy Chemistry 1 (1992), Proteins, Elsevier, Amsterdam 141-190
4. Sawyer L., and Kontopidis G. The core lipocalin, bovine β-lactoglobulin. Biochim. Biophys. Acta 1482 (2000) 136-148
5. Cerbulis J., and Farrell Jr. H.M. Composition of milks of dairy cattle. I. Protein, lactose, and fat contents and distribution of protein fraction. J. Dairy Sci. 58 (1975) 817-827
6. Brunori M. Structural dynamics of myoglobin. Biophys. Chem. 86 (2000) 221-230
7. Schlichting I., and Chu K. Trapping intermediates in the crystal: ligand binding to myoglobin. Curr. Opin. Struct. Biol. 10 (2000) 744-752
8. Baldwin R.L. On-pathway versus off-pathway folding intermediates. Fold. Des. 1 (1996) R1-8
9. Fukamizo T. Chitinolytic enzymes: catalysis, substrate binding, and their application. Curr. Protein Pept. Sci. 1 (2000) 105-124
10. Adams M.J., Ford G.C., Koekoek R., Lentz P.J., McPherson Jr. A., Rossmann M.G., Smiley I.E., Schevitz R.W., and Wonacott A.J. Structure of lactate dehydrogenase at 2-8 Å resolution. Nature 227 (1970) 1098-1103
11. Clarke A.R., Atkinson T., and Holbrook J.J. From analysis to synthesis: new ligand binding sites on the lactate dehydrogenase framework. Part II. Trends Biochem. Sci. 14 (1989) 145-148
12. Tanford C., and Nozaki Y. Physico-chemical comparison of β-lactoglobulins A and B. J. Biol. Chem. 234 (1959) 2874-2877
13. Fugate R.D., and Song P.S. Spectroscopic characterization of β-lactoglobulin-retinol complex. Biochim. Biophys. Acta 625 (1980) 28-42
14. Sawyer L., Brownlow S., Polikarpov I., and Wu S.Y. β-Lactoglobulin: structural studies, biological clues. Int. Dairy J. 8 (1998) 65-72
15. Kinsella J.E., and Whitehead D.M. Proteins in whey: chemical, physical, and functional properties. Adv. Food Nutr. Res. 33 (1989) 343-438
16. Kontopidis G., Holt C., and Sawyer L. Invited review: β-lactoglobulin: binding properties, structure, and function. J. Dairy Sci. 87 (2004) 785-796
17. Sawyer L. β-lactoglobulin. In: Fox P.F., and McSweeney P. (Eds). Advanced Dairy Chemistry I. 3rd ed (2003), Kluwer, Amsterdam and New York 319-386
18. Papiz M.Z., Sawyer L., Eliopoulos E.E., North A.C., Findlay J.B., Sivaprasadarao R., Jones T.A., Newcomer M.E., and Kraulis P.J. The structure of β-lactoglobulin and its similarity to plasma retinol-binding protein. Nature 324 (1986) 383-385
19. Brownlow S., Morais Cabral J.H., Cooper R., Flower D.R., Yewdall S.J., Polikarpov I., North A.C., and Sawyer L. Bovine β-lactoglobulin at 1.8 Å resolution-still an enigmatic lipocalin. Structure 5 (1997) 481-495
20. Qin B.Y., Bewley M.C., Creamer L.K., Baker H.M., Baker E.N., and Jameson G.B. Structural basis of the Tanford transition of bovine β-lactoglobulin. Biochemistry 37 (1998) 14014-14023
21. Qin B.Y., Creamer L.K., Baker E.N., and Jameson G.B. 12-Bromododecanoic acid binds inside the calyx of bovine β-lactoglobulin. FEBS Lett. 438 (1998) 272-278
22. Cupo J.F., and Pace C.N. Conformational stability of mixed disulfide derivatives of β-lactoglobulin B. Biochemistry 22 (1983) 2654-2658
23. Alting A.C., de Jongh H.H., Visschers R.W., and Simons J.W. Physical and chemical interactions in cold gelation of food proteins. J. Agric. Food Chem. 50 (2002) 4682-4689
24. Mercade-Prieto R., Falconer R.J., Paterson W.R., and Wilson D.I. Effect of gel structure on the dissolution of heat-induced β-lactoglobulin gels in alkali. J. Agric. Food Chem. 54 (2006) 5437-5444
25. Cho Y., Batt C.A., and Sawyer L. Probing the retinol-binding site of bovine β-lactoglobulin. J. Biol. Chem. 269 (1994) 11102-11107
26. Cho Y., Gu W., Watkins S., Lee S.P., Kim T.R., Brady J.W., and Batt C.A. Thermostable variants of bovine β-lactoglobulin. Protein Eng. 7 (1994) 263-270
27. Kim T.R., Goto Y., Hirota N., Kuwata K., Denton H., Wu S.Y., Sawyer L., and Batt C.A. High-level expression of bovine β-lactoglobulin in Pichia pastoris and characterization of its physical properties. Protein Eng. 10 (1997) 1339-1345
28. Kuwata K., Hoshino M., Era S., Batt C.A., and Goto Y. α → β transition of β-lactoglobulin as evidenced by heteronuclear NMR. J. Mol. Biol. 283 (1998) 731-739
29. Kuwata K., Hoshino M., Forge V., Era S., Batt C.A., and Goto Y. Solution structure and dynamics of bovine β-lactoglobulin A. Protein Sci. 8 (1999) 2541-2545
30. Uhrínová S., Smith M.H., Jameson G.B., Uhrín D., Sawyer L., and Barlow P.N. Structural changes accompanying pH-induced dissociation of the β-lactoglobulin dimer. Biochemistry 39 (2000) 3565-3574
31. Kuwata K., Shastry R., Cheng H., Hoshino M., Batt C.A., Goto Y., and Roder H. Structural and kinetic characterization of early folding events in β-lactoglobulin. Nat. Struct. Biol. 8 (2001) 151-155
32. Sakurai K., and Goto Y. Manipulating monomer-dimer equilibrium of bovine β-lactoglobulin by amino acid substitution. J. Biol. Chem. 277 (2002) 25735-25740
33. Yagi M., Sakurai K., Kalidas C., Batt C.A., and Goto Y. Reversible unfolding of bovine β-lactoglobulin mutants without a free thiol group. J. Biol. Chem. 278 (2003) 47009-47015
34. Dill K.A., and Chan H.S. From Levinthal to pathways to funnels. Nat. Struct. Biol. 4 (1997) 10-19
35. Socci N.D., Onuchic J.N., and Wolynes P.G. Protein folding mechanisms and the multidimensional folding funnel. Proteins 32 (1998) 136-158
36. Wolynes P.G. Energy landscapes and solved protein-folding problems. Philos. Trans. A Math. Phys. Eng. Sci. 363 (2005) 453-464 discussion 464-457
37. Nishimura C., Dyson H.J., and Wright P.E. Identification of native and non-native structure in kinetic folding intermediates of apomyoglobin. J. Mol. Biol. 355 (2006) 139-156
38. Nishimura C., Dyson H.J., and Wright P.E. Enhanced picture of protein-folding intermediates using organic solvents in H/D exchange and quench-flow experiments. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 4765-4770
39. Dobson C.M. Protein folding and misfolding. Nature 426 (2003) 884-890
40. Fogolari F., Ragona L., Zetta L., Romagnoli S., De Kruif K.G., and Molinari H. Monomeric bovine β-lactoglobulin adopts a β-barrel fold at pH 2. FEBS Lett. 436 (1998) 149-154
41. 15N chemical shifts for bovine β-lactoglobulin: secondary structure and topology of the native state is retained in a partially unfolded form. J. Biomol. NMR 12 (1998) 89-107
42. Joss L.A., and Ralston G.B. β-Lactoglobulin B: a proposed standard for the study of reversible self-association reactions in the analytical ultracentrifuge?. Anal. Biochem. 236 (1996) 20-26
43. Sakurai K., Oobatake M., and Goto Y. Salt-dependent monomer-dimer equilibrium of bovine β-lactoglobulin at pH 3. Protein Sci. 10 (2001) 2325-2335
44. Apenten R.K. Protein stability function relations: β-lactoglobulin-A sulphydryl group reactivity and its relationship to protein unfolding stability. Int. J. Biol. Macromol. 23 (1998) 19-25
45. Sakai K., Sakurai K., Sakai M., Hoshino M., and Goto Y. Conformation and stability of thiol-modified bovine β-lactoglobulin. Protein Sci. 9 (2000) 1719-1729
46. Yamasaki R., Hoshino M., Wazawa T., Ishii Y., Yanagida T., Kawata Y., Higurashi T., Sakai K., Nagai J., and Goto Y. Single molecular observation of the interaction of GroEL with substrate proteins. J. Mol. Biol. 292 (1999) 965-972
47. Burova T.V., Choiset Y., Tran V., and Haertlé T. Role of free Cys121 in stabilization of bovine β-lactoglobulin B. Protein Eng. 11 (1998) 1065-1073
48. Narayan M., and Berliner L.J. Mapping fatty acid binding to β-lactoglobulin: ligand binding is restricted by modification of Cys 121. Protein Sci. 7 (1998) 150-157
49. Flower D.R. The lipocalin protein family: structure and function. Biochem. J. 318 Pt 1 (1996) 1-14
50. Breustedt D.A., Korndörfer I.P., Redl B., and Skerra A. The 1.8-Å crystal structure of human tear lipocalin reveals an extended branched cavity with capacity for multiple ligands. J. Biol. Chem. 280 (2005) 484-493
51. Sacchettini J.C., Gordon J.I., and Banaszak L.J. Crystal structure of rat intestinal fatty-acid-binding protein. Refinement and analysis of the Escherichia coli-derived protein with bound palmitate. J. Mol. Biol. 208 (1989) 327-339
52. Urade Y., Fujimoto N., and Hayaishi O. Purification and characterization of rat brain prostaglandin D synthetase. J. Biol. Chem. 260 (1985) 12410-12415
53. Seppälä M., Taylor R.N., Koistinen H., Koistinen R., and Milgrom E. Glycodelin: a major lipocalin protein of the reproductive axis with diverse actions in cell recognition and differentiation. Endocr. Rev. 23 (2002) 401-430
54. Taulier N., and Chalikian T.V. Characterization of pH-induced transitions of β-lactoglobulin: ultrasonic, densimetric, and spectroscopic studies. J. Mol. Biol. 314 (2001) 873-889
55. Tanford C., Bunville L.G., and Nozaki Y. The reversible transformation of β-lactoglobulin at pH 7.5. J. Am. Chem. Soc. 81 (1959) 4032-4036
56. Vijayalakshmi L., Krishna R., Sankaranarayanan R., and Vijayan M. An asymmetric dimer of β-lactoglobulin in a low humidity crystal form-structural changes that accompany partial dehydration and protein action. Proteins 71 (2008) 241-249
57. Sakurai K., and Goto Y. Dynamics and mechanism of the Tanford transition of bovine β-lactoglobulin studied using heteronuclear NMR spectroscopy. J. Mol. Biol. 356 (2006) 483-496
58. Tanford C. Protein denaturation. C. Theoretical models for the mechanism of denaturation. Adv. Protein Chem. 24 (1970) 1-95
59. Barrick D., and Baldwin R.L. Three-state analysis of sperm whale apomyoglobin folding. Biochemistry 32 (1993) 3790-3796
60. Fogolari F., Moroni E., Wojciechowski M., Baginski M., Ragona L., and Molinari H. MM/PBSA analysis of molecular dynamics simulations of bovine β-lactoglobulin: free energy gradients in conformational transitions?. Proteins 59 (2005) 91-103
61. Ragona L., Fogolari F., Zetta L., Peréz D.M., Puyol P., De Kruif K., Löhr F., Rüterjans H., and Molinari H. Bovine β-lactoglobulin: interaction studies with palmitic acid. Protein Sci. 9 (2000) 1347-1356
62. Sakurai K., and Goto Y. Principal component analysis of the pH-dependent conformational transitions of bovine β-lactoglobulin monitored by heteronuclear NMR. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 15346-15351
63. Lipari G., and Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. J. Am. Chem. Soc. 104 (1982) 4546-4559
64. Dosset P., Hus J.C., Blackledge M., and Marion D. Efficient analysis of macromolecular rotational diffusion from heteronuclear relaxation data. J. Biomol. NMR 16 (2000) 23-28
65. 1H exchange. Biochemistry 36 (1997) 2278-2290
66. Shimamoto S., Yoshida T., Inui T., Gohda K., Kobayashi Y., Fujimori K., Tsurumura T., Aritake K., Urade Y., and Ohkubo T. NMR solution structure of lipocalin-type prostaglandin D synthase: evidence for partial overlapping of catalytic pocket and retinoic acid-binding pocket within the central cavity. J. Biol. Chem. 282 (2007) 31373-31379
67. Kushibiki S., Hodate K., Kurisaki J., Shingu H., Ueda Y., Watanabe A., and Shinoda M. Effect of β-lactoglobulin on plasma retinol and triglyceride concentrations, and fatty acid composition in calves. J. Dairy Res. 68 (2001) 579-586
68. Yang M.C., Chen N.C., Chen C.J., Wu C.Y., and Mao S.J. Evidence for β-lactoglobulin involvement in vitamin D transport in vivo-role of the γ-turn (Leu-Pro-Met) of β-lactoglobulin in vitamin D binding. FEBS J. 276 (2009) 2251-2265
69. McMeekin T.L., Polis B.D., Della-Monica E.S., and Custer J.H. A crystalline compound of β-lactoglobulin with dodecyl sulphate. J. Am. Chem. Soc. 71 (1949) 3606-3609
70. Kontopidis G., Holt C., and Sawyer L. The ligand-binding site of bovine β-lactoglobulin: evidence for a function?. J. Mol. Biol. 318 (2002) 1043-1055
71. Wu S.Y., Pérez M.D., Puyol P., and Sawyer L. β-Lactoglobulin binds palmitate within its central cavity. J. Biol. Chem. 274 (1999) 170-174
72. 3 binding site of milk β-lactoglobulin. Proteins 71 (2008) 1197-1210
73. Konuma T., Sakurai K., and Goto Y. Promiscuous binding of ligands by β-lactoglobulin involves hydrophobic interactions and plasticity. J. Mol. Biol. 368 (2007) 209-218
74. Stevens S.Y., Sanker S., Kent C., and Zuiderweg E.R. Delineation of the allosteric mechanism of a cytidylyltransferase exhibiting negative cooperativity. Nat. Struct. Biol. 8 (2001) 947-952
75. Zuiderweg E.R. Mapping protein-protein interactions in solution by NMR spectroscopy. Biochemistry 41 (2002) 1-7
76. Goh C.S., Milburn D., and Gerstein M. Conformational changes associated with protein-protein interactions. Curr. Opin. Struct. Biol. 14 (2004) 104-109
77. Zídek L., Novotny M.V., and Stone M.J. Increased protein backbone conformational entropy upon hydrophobic ligand binding. Nat. Struct. Biol. 6 (1999) 1118-1121
78. Jameson G.B., Adams J.J., and Creamer L.K. Flexibility, functionality and hydrophobicity of bovine β-lactoglobulin. Int. Dairy J. 12 (2002) 319-329
79. Braig K., Otwinowski Z., Hegde R., Boisvert D.C., Joachimiak A., Horwich A.L., and Sigler P.B. The crystal structure of the bacterial chaperonin GroEL at 2.8 Å. Nature 371 (1994) 578-586
80. Chatellier J., Buckle A.M., and Fersht A.R. GroEL recognises sequential and non-sequential linear structural motifs compatible with extended β-strands and α-helices. J. Mol. Biol. 292 (1999) 163-172
81. Gómez-Puertas P., Martín-Benito J., Carrascosa J.L., Willison K.R., and Valpuesta J.M. The substrate recognition mechanisms in chaperonins. J. Mol. Recognit. 17 (2004) 85-94
82. Wright P.E., and Dyson H.J. Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J. Mol. Biol. 293 (1999) 321-331
83. Fink A.L. Natively unfolded proteins. Curr. Opin. Struct. Biol. 15 (2005) 35-41
84. Tompa P., Szász C., and Buday L. Structural disorder throws new light on moonlighting. Trends Biochem. Sci. 30 (2005) 484-489
85. Hamada D., Segawa S., and Goto Y. Non-native α-helical intermediate in the refolding of β-lactoglobulin, a predominantly β-sheet protein. Nat. Struct. Biol. 3 (1996) 868-873
86. Forge V., Hoshino M., Kuwata K., Arai M., Kuwajima K., Batt C.A., and Goto Y. Is folding of β-lactoglobulin non-hierarchic? Intermediate with native-like β-sheet and non-native α-helix. J. Mol. Biol. 296 (2000) 1039-1051
87. Cohen F.E. Protein misfolding and prion diseases. J. Mol. Biol. 293 (1999) 313-320
88. Uversky V.N., and Fink A.L. Conformational constraints for amyloid fibrillation: the importance of being unfolded. Biochim. Biophys. Acta 1698 (2004) 131-153
89. Hamada D., Tanaka T., Tartaglia G.G., Pawar A., Vendruscolo M., Kawamura M., Tamura A., Tanaka N., and Dobson C.M. Competition between folding, native-state dimerisation and amyloid aggregation in β-lactoglobulin. J. Mol. Biol. 386 (2009) 878-890
90. Hamada D., Kuroda Y., Tanaka T., and Goto Y. High helical propensity of the peptide fragments derived from β-lactoglobulin, a predominantly β-sheet protein. J. Mol. Biol. 254 (1995) 737-746
91. Kuroda Y., Hamada D., Tanaka T., and Goto Y. High helicity of peptide fragments corresponding to β-strand regions of β-lactoglobulin observed by 2D-NMR spectroscopy. Fold. Des. 1 (1996) 255-263
92. Hamada D., and Goto Y. The equilibrium intermediate of β-lactoglobulin with non-native α-helical structure. J. Mol. Biol. 269 (1997) 479-487
93. Roder H., Elöve G.A., and Englander S.W. Structural characterization of folding intermediates in cytochrome c by H-exchange labelling and proton NMR. Nature 335 (1988) 700-704
94. Ragona L., Fogolari F., Romagnoli S., Zetta L., Maubois J.L., and Molinari H. Unfolding and refolding of bovine β-lactoglobulin monitored by hydrogen exchange measurements. J. Mol. Biol. 293 (1999) 953-969
95. Fujiwara K., Arai M., Shimizu A., Ikeguchi M., Kuwajima K., and Sugai S. Folding-unfolding equilibrium and kinetics of equine β-lactoglobulin: equivalence between the equilibrium molten globule state and a burst-phase folding intermediate. Biochemistry 38 (1999) 4455-4463
96. D'Alfonso L., Collini M., Ragona L., Ugolini R., Baldini G., and Molinari H. Porcine β-lactoglobulin chemical unfolding: identification of a non-native α-helical intermediate. Proteins 58 (2005) 70-79
97. Ikeguchi M., Kato S., Shimizu A., and Sugai S. Molten globule state of equine β-lactoglobulin. Proteins 27 (1997) 567-575
98. Kobayashi T., Ikeguchi M., and Sugai S. Molten globule structure of equine β-lactoglobulin probed by hydrogen exchange. J. Mol. Biol. 299 (2000) 757-770
99. Greene L.H., Wijesinha-Bettoni R., and Redfield C. Characterization of the molten globule of human serum retinol-binding protein using NMR spectroscopy. Biochemistry 45 (2006) 9475-9484
100. Yagi M., Kameda A., Sakurai K., Nishimura C., and Goto Y. Disulfide-linked bovine β-lactoglobulin dimers fold slowly, navigating a glassy folding landscape. Biochemistry 47 (2008) 5996-6006
101. Hoyer W., Ramm K., and Plückthun A. A kinetic trap is an intrinsic feature in the folding pathway of single-chain Fv fragments. Biophys. Chem. 96 (2002) 273-284
102. Tsunenaga M., Goto Y., Kawata Y., and Hamaguchi K. Unfolding and refolding of a type κ immunoglobulin light chain and its variable and constant fragments. Biochemistry 26 (1987) 6044-6051
103. Fenton W.A., and Horwich A.L. GroEL-mediated protein folding. Protein Sci. 6 (1997) 743-760
104. Horst R., Bertelsen E.B., Fiaux J., Wider G., Horwich A.L., and Wüthrich K. Direct NMR observation of a substrate protein bound to the chaperonin GroEL. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 12748-12753
105. Horst R., Fenton W.A., Englander S.W., Wüthrich K., and Horwich A.L. Folding trajectories of human dihydrofolate reductase inside the GroEL GroES chaperonin cavity and free in solution. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 20788-20792
106. Nishimura C., Dyson H.J., and Wright P.E. The apomyoglobin folding pathway revisited: structural heterogeneity in the kinetic burst phase intermediate. J. Mol. Biol. 322 (2002) 483-489
107. Nishimura C., Wright P.E., and Dyson H.J. Role of the B helix in early folding events in apomyoglobin: evidence from site-directed mutagenesis for native-like long range interactions. J. Mol. Biol. 334 (2003) 293-307
108. Go N. The consistency principle in protein structure and pathways of folding. Adv. Biophys. 18 (1984) 149-164
109. Onuchic J.N., and Wolynes P.G. Theory of protein folding. Curr. Opin. Struct. Biol. 14 (2004) 70-75
110. Sutto L., Lätzer J., Hegler J.A., Ferreiro D.U., and Wolynes P.G. Consequences of localized frustration for the folding mechanism of the IM7 protein. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 19825-19830
111. Ferreiro D.U., Hegler J.A., Komives E.A., and Wolynes P.G. Localizing frustration in native proteins and protein assemblies. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 19819-19824
112. Deléage G., and Roux B. An algorithm for protein secondary structure prediction based on class prediction. Protein Eng. 1 (1987) 289-294
113. King R.D., and Sternberg M.J. Identification and application of the concepts important for accurate and reliable protein secondary structure prediction. Protein Sci. 5 (1996) 2298-2310
114. Garnier J., Osguthorpe D.J., and Robson B. Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J. Mol. Biol. 120 (1978) 97-120
115. Gibrat J.F., Garnier J., and Robson B. Further developments of protein secondary structure prediction using information theory. New parameters and consideration of residue pairs. J. Mol. Biol. 198 (1987) 425-443
116. Y. Guermeur, Combinaison de classifieurs statistiques, Application a la prediction de structure secondaire des proteines., vol. Ph. D, Universite' Paris, France, 1997.
117. Guermeur Y., Geourjon C., Gallinari P., and Deléage G. Improved performance in protein secondary structure prediction by inhomogeneous score combination. Bioinformatics 15 (1999) 413-421
118. Rost B., and Sander C. Prediction of protein secondary structure at better than 70% accuracy. J. Mol. Biol. 232 (1993) 584-599
119. Frishman D., and Argos P. Incorporation of non-local interactions in protein secondary structure prediction from the amino acid sequence. Protein Eng. 9 (1996) 133-142
120. Geourjon C., and Deléage G. SOPM: a self-optimized method for protein secondary structure prediction. Protein Eng. 7 (1994) 157-164
121. Deléage G., Combet C., Blanchet C., and Geourjon C. ANTHEPROT: an integrated protein sequence analysis software with client/server capabilities. Comput. Biol. Med. 31 (2001) 259-267
122. Flower D.R., North A.C., and Sansom C.E. The lipocalin protein family: structural and sequence overview. Biochim. Biophys. Acta 1482 (2000) 9-24