Characterization of the molten globule of human serum retinol-binding protein using NMR spectroscopy

Biochemistry

Volumn 45, Issue 31, 2006, Pages 9475-9484

  Greene, Lesley H ^a,b   Wijesinha Bettoni, Ramani ^a   Redfield, Christina ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CELLS; CONFORMATIONS; FLUORESCENCE; NAPHTHALENE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; ORGANIC ACIDS;

AMYLOID FIBRIL FORMATION; HUMAN SERUM RETINOL-BINDING PROTEIN; MOLTEN GLOBULE; STOPPED-FLOW FLUORESCENCE SPECTROSCOPY;

PROTEINS;

8 ANILINO 1 NAPHTHALENESULFONIC ACID; ALPHA LACTALBUMIN; LIGAND; RETINOL BINDING PROTEIN;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; CONTROLLED STUDY; FLUORESCENCE SPECTROSCOPY; MOLTEN GLOBULE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN STABILITY; SEQUENCE ANALYSIS; SERUM; STOPPED FLOW FLUORESCENCE SPECTROSCOPY;

AMINO ACID SEQUENCE; ANILINO NAPHTHALENESULFONATES; BLOOD PROTEINS; CIRCULAR DICHROISM; CONSERVED SEQUENCE; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; RETINOL-BINDING PROTEINS;

EID: 33747119345     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060229c     Document Type: Article

References (60)

1. Dolgikh, D. A., Gilmanshin, R. I., Brazhnikov, E. V., Bychkova, V. E., Semisotnov, G. V., Venyaminov, S. Y., and Ptitsyn, O. B. (1981) Alpha-lactalbumin: compact state with fluctuating tertiary structure, FEBS Lett. 136, 311-315.
2. Ohgushi, M., and Wada, A. (1983) Molten-globule state - a compact form of globular-proteins with mobile side-chains, FEBS Lett. 164, 21-24.
3. Ptitsyn, O. B., Pain, R. H., Semisotnov, G. V., Zerovnik, E., and Razgulyaev, O. I. (1990) Evidence for a molten globule state as a general intermediate in protein folding, FEBS Lett. 262, 20-24.
4. Jennings, P. A., and Wright, P. E. (1993) Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin, Science 262, 892-896.
5. Yao, J., Chung, J., Eliezer, D., Wright, P. E., and Dyson, H. J. (2001) NMR structural and dynamic characterization of the acid-unfolded state of apomyoglobin provides insights into the early events in protein folding, Biochemistry 40, 3561-3571.
6. Sandberg, A., Leckner, J., and Karlsson, B. G. (2004) Apo-azurin folds via an intermediate that resembles the molten-globule, Protein Sci. 13, 2628-2638.
7. Bose, H. S., Whittal, R. M., Baldwin, M. A., and Miller, W. L. (1999) The active form of the steroidogenic acute regulatory protein, StAR, appears to be a molten globule, Proc. Natl. Acad. Sci. U.S.A. 96, 7250-7255.
8. Twigg, P. D., Parthasarathy, G., Guerrero, L., Logon, T. M., and Caspar, D. L. D. (2001) Disordered to ordered folding in the regulation of diphtheria toxin repressor activity, Proc. Natl. Acad. Sci. U.S.A. 98, 11259-11264.
9. Vandergoot, F. G., Gonzalezmanas, J. M., Lakey, J. H., and Pattus, F. (1991) A molten-globule membrane-insertion intermediate of the pore-forming domain of colicin-A, Nature 354, 408-410.
10. Dunker, A. K., Ensign, L. D., Arnold, G. E., and Roberts, L. M. (1991) Proposed molten globule intermediates in Fd phage penetration and assembly, FEBS Lett. 292, 275-278.
11. Kirkitadze, M. D., Barlow, P. N., Price, N. C., Kelly, S. M., Boutell, C. J., Rixon, F. J., and McClelland, D. A. (1998) The herpes simplex virus triplex protein, VP23, exists as a molten globule. Journal of Virology 72, 10066-10072.
12. Safar, J., Roller, P. P., Gajdusek, D. C., and Gibbs, C. J. (1994) Scrapie amyloid (prion) protein has the conformational characteristics of an aggregated molten globule folding intermediate, Biochemistry 33, 8375-8383.
13. Dumoulin, M., Canet, D., Last, A. M., Pardon, E., Archer, D. B., Muyldermans, S., Wyns, L., Matagne, A., Robinson, C. V., Redfield, C., and Dobson, C. M. (2005) Reduced global copperativity is a common feature underlying the amyloidogenicity of pathogenic lysozyme mutations, J. Mol. Biol. 346, 773-788.
14. Redfield, C. (2004) Using nuclear magnetic resonance spectroscopy to study molten globule states of proteins, Methods 34, 121-132.
15. Schulman, B. A., Kim, P. S., Dobson, C. M., and Redfield, C. (1997) A residue-specific NMR view of the non-cooperative unfolding of a molten globule, Nat. Struct. Biol. 4, 630-634.
16. Redfield, C., Schulman, B. A., Milhollen, M. A., Kim, P. S., and Dobson, C. M. (1999) alpha-lactalbumin forms a compact molten globule in the absence of disulfide bonds, Nat. Struct. Biol. 6, 948-952.
17. Baum, J., Dobson, C. M., Evans, P. A., and Hanley, C. (1989) Characterization of a partly folded protein by NMR methods: studies on the molten globule state of guinea-pig alpha-lactalbumin, Biochemistry 28, 7-13.
18. Hughson, F. M., Wright, P. E., and Baldwin, R. L. (1990) Structural characterization of a partly folded apomyoglobin intermediate, Science 249, 1544-1548.
19. Eliezer, D., Yao, J., Dyson, H. J., and Wright, P. E. (1998) Structural and dynamic characterization of partially folded states of apomyoglobin and implications for protein folding, Nat. Struct. Biol. 5, 148-155.
20. Eliezer, D., Chung, J., Dyson, H. J., and Wright, P. E. (2000) Native and non-native secondary structure and dynamics in the pH 4 intermediate of apomyoglobin, Biochemistry 39, 2894-2901.
21. Ramboarina, S., and Redfield, C. (2003) Structural characterisation of the human alpha-lactalbumin molten globule at high temperature, J. Mol. Biol. 330, 1177-1188.
22. Demarest, S. J., Fairman, R., and Raleigh, D. P. (1998) Peptide models of local and long-range interactions in the molten globule state of human alpha-lactalbumin, J. Mol. Biol. 283, 279-291.
23. Chowdhury, F. A., and Raleigh, D. P. (2005) A comparative study of the alpha-subdomains of bovine and human alpha-lactalbumin reveals key differences that correlate with molten globule stability, Protein Sci. 14, 89-96.
24. Wang, Y., and Shortle, D. (1996) A dynamic bundle of four adjacent hydrophobic segments in the denatured state of staphylococcal nuclease, Protein Sci. 5, 1898-1906.
25. Mok, K. H., Nagashima, T., Day, L. J., Hore, P. J., and Dobson, C. M. (2005) Multiple subsets of side-chain packing in partially folded states of alpha-lactalbumins, Proc. Natl. Acad. Sci. U.S.A. 102, 8899-8904.
26. Pervaiz, S., and Brew, K. (1985) Homology of beta-lactoglobulin, serum retinol-binding protein, and protein Hc, Science 228, 335-337.
27. Holm, L., and Sander, C. (1998) Dictionary of recurrent domains in protein structures, Proteins: Struct., Funct., Bioinf. 33, 88-96.
28. Greene, L. H., Hamada, D., Eyles, S. J., and Brew, K. (2003) Conserved signature proposed for folding in the lipocalin superfamily, FEBS Lett. 553, 39-44.
29. Naylor, H. M., and Newcomer, M. E. (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.
30. McCammon, M. G., Scott, D. J., Keetch, C. A., Greene, L. H., Purkey, H. E., Petrassi, H. M., Kelly, J. W., and Robinson, C. V. (2002) Screening transthyretin amyloid fibril inhibitors: Characterization of novel multiprotein, multiligand complexes by mass spectrometry, Structure 10, 851-863.
31. Sundaram, M., van Aalten, D. M. F., Findlay, J. B. C., and Sivaprasadarao, A. (2002) The transfer of transthyretin and receptor-binding properties from the plasma retinol-binding protein to the epididymal retinoic acid-binding protein, Biochem. J. 362, 265-271.
32. Ptitsyn, O. B., Zanotti, G., Denesyuk, A. L., and Bychkova, V. E. (1993) Mechanism of Ph-induced release of retinol from retinol-binding protein, FEBS Lett. 317, 181-184.
33. Bychkova, V. E., Dujsekina, A. E., Fantuzzi, A., Ptitsyn, O. B., and Rossi, G. L. (1998) Release of retinol and denaturation of its plasma carrier, retinol-binding protein, Folding Des. 3, 285-291.
34. Paci, E., Greene, L. H., Jones, R. M., and Smith, L. J. (2005) Characterization of the molten globule state of retinol-binding protein using a molecular dynamics simulation approach, FEBS Journal 272, 4826-4838.
35. Greene, L. H., Chrysina, E. D., Irons, L. I., Papageorgiou, A. C., Acharya, K. R., and Brew, K. (2001) Role of conserved residues in structure and stability: Tryptophans of human serum retinol-binding protein, a model for the lipocalin superfamily, Protein Sci. 10, 2301-2316.
36. Braun, D., Wider, G., and Wuthrich, K. (1994) Sequence-corrected N-15 random coil chemical-shifts, J. Am. Chem. Soc. 116, 8466-8469.
37. Marion, D., Driscoll, P. C., Kay, L. E., Wingfield, P. T., Bax, A., Gronenborn, A. M., and Clore, G. M. (1989) Overcoming the overlap problem in the assignment of H-1-NMR spectra of larger proteins by use of 3-dimensional heteronuclear H-1-N-15 Hartmann-Hahn multiple quantum coherence and nuclear Overhauser multiple quantum coherence spectroscopy: application to interleukin-1-beta, Biochemistry 28, 6150-6156.
38. Kay, L. E., Keifer, P., and Saarinen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity, J. Am. Chem. Soc. 114, 10663-10665.
39. Frenkiel, T., Bauer, C., Carr, M. D., Birdsall, B., and Feeney, J. (1990) Hmqc-Noesy-Hmqc, a 3-dimensional NMR experiment which allows detection of nuclear Overhauser effects between protons with overlapping signals, J. Magn. Reson. 90, 420-425.
40. Bychkova, V. E., Berni, R., Rossi, G. L., Kutyshenko, V. P., and Ptitsyn, O. B. (1992) Retinol-binding protein is in the molten globule state at low pH, Biochemistry 31, 7566-7571.
41. Jones, J. A., Wilkins, D. K., Smith, L. J., and Dobson, C. M. (1997) Characterisation of protein unfolding by NMR diffusion measurements, J. Biomol. NMR 10, 199-203.
42. Bodenhausen, G., and Ruben, D. J. (1980) Natural abundance N-15 NMR by enhanced heteronuclear spectroscopy, Chem. Phys. Lett. 69, 185-189.
43. Semisotnov, G. V., Rodionova, N. A., Razgulyaev, O. I., Uversky, V. N., Gripas, A. F., and Gilmanshin, R. I. (1991) Study of the molten globule intermediate state in protein folding by a hydrophobic fluorescent-probe, Biopolymers 31, 119-128.
44. Engelhard, M., and Evans, P. A. (1995) Kinetics of interaction of partially-folded proteins with a hydrophobic fluorescent dye: evidence that molten globule character is maximal in early folding intermediates, Protein Sci. 4, 1553-1562.
45. Maki, K., Cheng, H., Dolgikh, D. A., Ramachandran, S. M. C. and Roder, H. (2004) Early events during folding of wild-type staphylococcal nuclease and a single-tryptophan variant studied by ultrarapid mixing, J. Mol. Biol. 338, 383-400.
46. Chapeaurouge, A., Johansson, J. S., and Ferreira, S. T. (2002) Folding of a de novo designed nativelike four-helix bundle protein, J. Biol. Chem. 277, 16478-16483.
47. Clark, P. L., Liu, Z. P., Rizo, J., and Gierasch, L. M. (1997) Cavity formation before stable hydrogen bonding in the folding of a beta-clam protein, Nat. Struct. Biol. 4, 883-886.
48. Kuwata, K., Shastry, R., Cheng, H., Hoshino, M., Batt, C. A., Goto, Y., and Roder, H. (2001) Structural and kinetic characterization of early folding events in beta-lactoglobulin, Nat. Struct. Biol. 8, 151-155.
49. Ragona, L., Catalano, M., Zetta, L., Longhi, R., Fogolari, F., and Molinari, H. (2002) Peptide models of folding initiation sites of bovine beta-lactoglobulin: Identification of nativelike hydrophobic interactions involving G and H strands, Biochemistry 41, 2786-2796.
50. Kobayashi, T., Ikeguchi, M., and Sugai, S. (2000) Molten globule structure of equine beta-lactoglobulin probed by hydrogen exchange, J. Mol. Biol. 299, 757-770.
51. Schulman, B. A., and Kim, P. S. (1996) Proline scanning mutagenesis of a molten globule reveals noncooperative formation of a protein's overall topology, Nat. Struct. Biol. 3, 682-687.
52. Quezada, C. M., Schulman, B. A., Froggatt, J. J., Dobson, C. M., and Redfield, C. (2004) Local and global cooperativity in the human alpha-lactalbumin molten globule, J. Mol. Biol. 338, 149-158.
53. Calderone, V., Berni, R., and 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.
54. Ragona, L., Fogolari, F., Catalano, M., Ugolini, R., Zetta, L., and Molinari, H. (2003) EF loop conformational change triggers ligand binding in beta-lactoglobulins, J. Biol. Chem. 278, 38840-38846.
55. Gasymov, O. K., Abduragimov, A. R., Yusifov, T. N., and Glasgow, B. J. (2004) Interstrand loops CD and EF act as pH-dependent gates to regulate fatty acid ligand binding in tear lipocalin, Biochemistry 43, 12894-12904.
56. Flower, D. R. (1996) The lipocalin protein family: Structure and function, Biochem. J. 318, 1-14.
57. Gasymov, O. K., Abduragimov, A. R., Gasimov, E. O., Yusifov, T. N., Dooley, A. N., and Glasgow, B. J. (2004) Tear lipocalin: potential for selective delivery of rifampin, Biochim. Biophys. Acta-Molecular Basis of Disease 1688, 102-111.
58. Gasymov, O. K., Abduragimov, A. R., Yusifov, T. N., and Glasgow, B. J. (1998) Structural changes in human tear lipocalins associated with lipid binding, Biochim. Biophys. Acta-Protein Structure and Molecular Enzymology 1386, 145-156.
59. Schlehuber, S., and Skerra, A. (2002) Tuning ligand affinity, specificity, and folding stability of an engineered lipocalin variant - a so-called 'anticalin' -using a molecular random approach, Biophys. Chem. 96, 213-228.
60. Beste, G., Schmidt, F. S., Stibora, T., and Skerra, A. (1999) Small antibody-like proteins with prescribed ligand specificities derived from the lipocalin fold, Proc. Natl. Acad. Sci. U.S.A. 96, 1898-1903.