An extensive thermodynamic characterization of the dimerization domain of the HIV-1 capsid protein

Protein Science

Volumn 14, Issue 9, 2005, Pages 2387-2404

  Lidón Moya, María C ^a   Barrera, Francisco N ^a   Bueno, Marta ^b   Pérez Jiménez, Raúl ^c   Sancho, Javier ^b   Mateu, Mauricio G ^d   Neira, José L ^a,b  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^b UNIVERSITY OF ZARAGOZA   (Spain)

^c UNIVERSITY OF GRANADA   (Spain)

^d UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

Chemical denaturation; Circular dichroism; Fluorescence; NMR; Protein stability; Thermal denaturation

Indexed keywords

CAPSID PROTEIN; DIMER; MONOMER;

ABSORPTION; ACIDITY; ANISOTROPY; ARTICLE; BINDING AFFINITY; CIRCULAR DICHROISM; COMPRESSION; DENATURATION; DIMERIZATION; DISSOCIATION; FLUORESCENCE; GEL PERMEATION CHROMATOGRAPHY; HUMAN IMMUNODEFICIENCY VIRUS 1; INFRARED SPECTROSCOPY; NUCLEAR MAGNETIC RESONANCE; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; THERMODYNAMICS; TRANSITION TEMPERATURE; ULTRAVIOLET RADIATION;

ANILINO NAPHTHALENESULFONATES; ANISOTROPY; CAPSID PROTEINS; CHROMATOGRAPHY, LIQUID; CIRCULAR DICHROISM; DIMERIZATION; FLUORESCENCE; HIV-1; HYDROGEN-ION CONCENTRATION; MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; THERMODYNAMICS; TRYPTOPHAN; TYROSINE;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MIRIDAE;

EID: 24344469405     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.041324305     Document Type: Article

References (62)

1. Anderson, D.E., Becktel, W.J., and Dahlquist, F.W. 1990. pH-induced denaturation of proteins: A single salt bridge contributes 3-5 kcal/mol to the free energy of folding of T4 lysozyme. Biochemistry 29: 2403-2408.
2. Backmann, J., Schäfer, G., Wyns, L., and Bönisch, H. 1998. Thermodynamics and kinetics of unfolding of the thermostable trimeric adenylate kinase from the archeon Sulfolobus acidocaldarius. J. Mol. Biol. 284: 817-833.
3. Borsetti, A., Öhagen, Å., and Göttlinger, H.G. 1998. The C-terminal half of the human immunodeficiency virus type 1 Gag precursor is sufficient for efficient particle assembly. J. Virol. 72: 9313-9317.
4. Campos, L.A., Bueno, M., López-Llano, J., Jiménez, M.A., and Sancho, J. 2004. Structure of stable protein folding intermediates by equilibrium φ-analysis: The apoflavodoxin thermal intermediate. J. Mol. Biol. 344: 239-255.
5. Cantor, C.R. and Schimmel, P.R. 1980. Biophysical chemistry. W.H. Freeman, New York.
6. a of a glutamate on the ligand binding surface. Biochemistry 39: 6814-6824.
7. Clarke, J. and Fersht, A.R. 1993. Engineered disulfide bonds as probes of the folding pathway of barnase: Increasing the stability of proteins against the rate of denaturation. Biochemistry 32: 4322-4329.
8. del Álamo, M. and Mateu, M.G. 2005. Electrostatic repulsion, compensatory mutations, and long-range non-additive effects at the dimerization interface of the HIV capsid protein. J. Mol. Biol. 345: 893-906.
9. del Álamo, M., Neira, J.L., and Mateu, M.G. 2003. Thermodynamic dissection of a low-affinity protein-protein interface involved in human immunodeficiency virus assembly. J. Biol. Chem. 278: 27923-27929.
10. Ding, K., Louis, J.M., and Gronenborg, A.M. 2004. Insights into conformation and dynamics of protein GB1 during folding and unfolding by NMR. J. Mol. Biol. 335: 1299-1307.
11. Dorfman, T., Bukovsky, A., Öhagen, Å., Hoglund, S., and Göttlinger, H.G. 1994. Functional domains of the capsid protein of human immunodeficiency virus. J. Virol. 68: 8180-8187.
12. Ehrlich, L.S., Liu, T., Scarlata, S., Chu, B., and Carter, C.A. 2001. HIV-1 capsid proteins forms spherical (immature-like) and tubular (mature-like) particles in vitro: Structure switching by pH-induced conformational changes. Biophys. J. 81: 586-594.
13. Forshey, B.M., von Schwedler, U.K., Sundquist, W.I., and Aiken, C. 2002. Formation of a human immunodeficiency virus type 1 core of optimal stability is crucial for viral replication. J. Virol. 76: 5667-5677.
14. a values in the ovomucoid third domain to charge replacement at a neighboring residue. Biochemistry 39: 8067-8072.
15. Fuller, T.W., Wilk, T., Gowen, B.E., Kräuslich, H.G., and Vogt, V.M. 1997. Cryo-electron microscopy reveals ordered domains in the immature HIV-1 particle. Curr. Biol. 7: 729-738.
16. Gamble, T.R., Vajdos, F.F., Yoo, S., Worthylake, D.K., Houseweart, M., Sundquist, W.I., and Hill, C.P. 1996. Crystal structure of human cyclophylin A bound to the amino terminal domain of HIV-1 capsid. Cell 87: 1285-1294.
17. Gamble, T.R., Yoo, S., Vajdos, F.F., von Schwedler, U.K., Worthylake, D.K., Wang, H., McCutcheon, J.P., Sundquist, W.I., and Hill, C.P. 1997. Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein. Science 278: 849-853.
18. Ganser, B.K., Li, S., Kliskho, V.Y., Finch, J.T., and Sundquist, W.I. 1999. Assembly and analysis of conical models for the HIV-1 core. Science 283: 80-83.
19. Gelderblom, H.R. 1991. Assembly and morphology of HIV: Potential effect of structure on viral function. AIDS 5: 617-638.
20. Gitti, R.K., Lee, B.M., Walker, J., Summers, M.F., Yoo, S., and Sundquist, W.I. 1996. Structure of the amino-terminal core domain of the HIV-1 capsid protein. Science 273: 231-235.
21. Groß, I., Hohenberg, H., and Kräulisch, H.G. 1997. In vitro assembly properties of purified bacterially expressed capsid proteins of human immunodeficiency virus. Eur. J. Biochem. 249: 592-600.
22. Groß, I., Hohenberg, H., Huckangel, C., and Kräulisch, H.G. 1998. N-terminal extension of human immunodeficiency virus capsid protein converts the in vitro assembly phenotype from tubular to spherical particles. J. Virol. 72: 4798-4810.
23. Groß, I., Hohenberg, H., Wilk, T., Wiegers, K., Grättinger, M., Müller, B., Fuller, S., and Kräulisch, H.G. 2000. A conformational switch controlling HIV-1 morphogenesis. EMBO J. 19: 103-113.
24. Hinkle, A., Goranson, A., Butters, C.A., and Tobacman, L.S. 1999. Roles for the troponin tail domain in thin filament assembly and regulation. A deletional study of cardiac troponin T. J. Biol. Chem. 274: 7157-7164.
25. Honig, B. and Yang, A.S. 1995. Free energy balance in protein folding. Adv. Protein Chem. 46: 27-58.
26. Irún, M.P., García-Mira, M.M., Sánchez-Ruiz, J.M., and Sancho, J. 2001. Native hydrogen bonds in a molten globule: The apoflavodoxin thermal intermediate. J. Mol. Biol. 306: 877-888.
27. Jaenicke, R. and Lillie, H. 2000. Folding and association of oligomeric and multimeric proteins. Adv. Protein Chem. 53: 329-401.
28. Johnson, J.E. 1996. Functional implications of protein-protein interaction in icosahedral viruses. Proc. Natl. Acad. Sci. 93: 27-33.
29. Kelly, S.M. and Price, N.C. 2000. The use of circular dichroism in the investigation of protein structure and function. Curr. Protein Pept. Sci. 1: 349-384.
30. Lakowicz, J.R. 1999. Principles of fluorescence spectroscopy, 2nd ed. Plenum Press, New York.
31. Lanman, J., Sexton, J., Sakalian, M., and Prevelige Jr., P.E. 2002. Kinetic analysis of the role of intersubunit interactions in human immunodeficiency virus type 1 capsid protein assembly in vitro. J. Virol. 76: 6900-6908.
32. Li, S., Hill, C.P., Sundquist, W.I., and Finch, J.T. 2000. Image reconstructions of helical assemblies of the HIV-1 CA protein. Nature 407: 409-413.
33. Luo, J., Iwakura, M., and Matthews, C.R. 1995. Detection of an intermediate in the thermal unfolding of a cysteine-free form of dihydrofolate from Escherichia coli. Biochemistry 34: 10669-10675.
34. Luo, Y., Kay, M., and Baldwin, R.L. 1997. Co-operativity of folding of apomyoglobin pH 4 intermediate studied by glycine and proline mutations. Nat. Struct. Biol. 4: 925-930.
35. Mach, H., Volkin, D.B., Burke, C.J., and Middaugh, C.R. 1995. Ultraviolet absorption spectroscopy. In Protein stability and folding (Methods in molecular biology, Vol. 40) (ed. B.A. Shirley), pp. 91-114. Humana Press, Towota, NJ.
36. Maldonado, S., Jiménez, M.A., Langdon, G.M., and Sancho, J. 1998. Cooperative stabilization of a molten-globule apoflavodoxin fragment. Biochemistry 37: 10589-10596.
37. Mann, C.J. and Matthews, C.R. 1993. Structure and stability of an early folding intermediate of Escherichia coli trp aporepressor measured by far-UV stopped-flow circular dichroism and 8-anilino-1-naphthalene sulfonate binding. Biochemistry 32: 5282-5290.
38. Marky, L.A. and Breslauer, K.J. 1987. Calculating thermodynamic data for transitions of any molecularity from equilibrium melting curves. Biopolymers 26: 1601-1620.
39. Mateu, M.G. 2002. Conformational stability of dimeric and monomeric forms of the C-terminal domain of human immunodeficiency virus. J. Mol. Biol. 318: 519-531.
40. Misselwitz, R., Hausdorf, G., Welfe, K., Höhne, W.E., and Welfe, H. 1995. Conformation and stability of recombinant HIV-1 capsid protein p24 (rp24). Biochem. Biophys. Acta 1250: 9-18.
41. Momany, C., Kovari, L.C., Prongay, A.J., Keller, W., Gitti, R.K., Lee, B.M., Gorbalenya, A.E., Tong, L., McClure, J., Ehrlich, L.S., et al. 1996. Crystal structure of the dimeric HIV-1 cpasid protein. Nat. Struct. Biol. 3: 763-770.
42. Neet, K.E. and Timm, D.E. 1994. Conformational stability of dimeric proteins: Quantitative studies by equilibrium denaturation. Protein Sci. 3: 2167-2174.
43. Pace, C.N. and Laurents, D.V. 1989. A new method for determining the heat capacity change for protein folding. Biochemistry 28: 2520-2525.
44. Pace, C.N. and Scholtz, J.M. 1997. Measuring the conformational stability of a protein. In Protein structure (ed. T.E. Creighton), 2nd ed., pp. 253-259. Oxford University Press, Oxford.
45. Piotto, M., Saudek, V., and Sklenar, V. 1992. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR 2: 661-665.
46. Ptitsyn, O.B. 1995. Molten globule and protein folding. Adv. Protein Chem. 47: 83-229.
47. Robertson, A.D. and Murphy, K.P. 1997. Protein structure and the energetics of protein stability. Chem. Rev. 97: 1251-1267.
48. Rosé, S., Hensley, P., O'Shanessy, D.J., Culp, J., Debouck, C., and Chaiken, I. 1992. Characterization of HIV-1 p24 self-association using analytical chromatography. Proteins 13: 112-119.
49. Royer, C.A. 1995. Fluorescence spectroscopy. In Protein stability and folding (Methods in molecular biology Vol. 40) (ed. B.A. Shirley), pp. 65-89. Humana Press, Towota, NJ.
50. Semisotnov, G.V., Rodionova, N.A., Razgulyaev, O.I., Uversky, V.N., Gripas, A.F., and Gimanshin, R.I. 1991. Study of the "molten globule" intermediate state in protein folding by a hydrophobic fluorescent probe. Biopolymers 31: 119-128.
51. Steif, C., Weber, P., Hinz, H.J., Flossdorf, J., Cesareni, G., and Kokkinidis, M. 1993. Subunit interactions provide a significant contribution to the stability of the dimeric four-α-helical bundle protein ROP. Biochemistry 32: 3867-3876.
52. Stryer, L. 1965. The interaction of a naphthalene sulfonate dye with apomyoglobin and apohemoglobin: A fluorescent probe of non-polar binding site. J. Mol. Biol. 13: 482-495.
53. Tang, K.S., Guralnick, B.J., Wong, W.K., Fersht, A.R., and Itzhaki, L.S. 1999. Stability and folding of the tumor suppressor protein p16. J. Mol. Biol. 285: 1869-1886.
54. Tang, S., Murakami, T., Agresta, B.E., Campbell, S., Freed, E.O., and Levin, J.G. 2001. Human immunodeficiency virus type 1 N-terminal capsid mutants that exhibit aberrant core morphology are blocked in initiation of reverse transcription in infected cells. J. Virol. 75: 9357-9366.
55. von Schwedler, U.K., Stemmler, T.L., Kliskho, V.Y., Li, S., Albertine, K.H., Davis, D.R., and Sundquist, W.I. 1998. Proteolytic refolding of the HIV-1 capsid protein amino-terminus facilitates viral core assembly. EMBO J. 17: 1555-1568.
56. Wang, C.T. and Barklis, E. 1993. Assembly, processing and infectivity of human immunodeficiency virus type 1 Gag mutants. J. Virol. 67: 4264-4273.
57. Welker, R., Hohenberg, H., Tessmer, U., Huckhagel, C., and Kräuslich, H.G. 2000. Biochemical and structural analysis of isolated matured cores of human immunodeficiency virus type I. J. Virol. 74: 1168-1177.
58. Wills, J.W. and Craven, C. 1991. Form, function and use of retroviral gag proteins. AIDS 5: 639-654.
59. Woody, R.W. 1995. Circular dichroism. Methods Enzymol. 246: 34-71.
60. Worthylake, D.K., Wang, H., Yoo, S., Sundquist, W.I., and Hill, C.P. 1999. Structures of the HIV-1 capsid protein dimerization domain at 2.6 Å resolution. Acta Crystallogr. D Acta Crystallogr. 55: 85-92.
61. Wüthrich, K. 1986. NMR of proteins and nucleic acids. John Wiley & Sons, New York.
62. Zweifel, M.E. and Barrick, D. 2002. Relationships between the temperature dependence of solvent denaturation and the denaturant dependence of protein stability curves. Biophys. Chem. 101-102: 221-237.