The isolated major homology region of the HIV capsid protein is mainly unfolded in solution and binds to the intact protein

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1814, Issue 10, 2011, Pages 1269-1278

  Doménech, Rosa ^a   Bocanegra, Rebeca ^b   Velázquez Campoy, Adrián ^c,d   Neira, José L ^a,c  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c UNIVERSITY OF ZARAGOZA   (Spain)

^d FUNDACIÓN ARAID   (Spain)

Author keywords

Binding; Fluorescence; Folding; ITC; Peptide; Structure

Indexed keywords

ALANINE; ASPARTIC ACID; CAPSID PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN UNFOLDING; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STRUCTURE ANALYSIS; VIRUS ASSEMBLY;

AMINO ACID SEQUENCE; CAPSID PROTEINS; CRYSTALLOGRAPHY, X-RAY; HIV-1; HUMANS; MODELS, MOLECULAR; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SOLUTIONS; VIRUS ASSEMBLY;

HUMAN IMMUNODEFICIENCY VIRUS 1; MIRIDAE; RICHES;

EID: 79960487669     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2011.06.011     Document Type: Article

References (60)

1. B.K. Ganser-Pornillos, M. Yeager, and W. Sundquist The structural biology of HIV assembly Curr. Opin. Struct. Biol. 18 2008 203 217
2. M.G. Mateu The capsid protein of human immunodeficiency virus: intersubunit interactions during virus assembly FEBS J. 276 2009 6098 6109
3. J.L. Neira The capsid protein of human immunodeficiency virus: designing inhibitors of capsid assembly FEBS J. 276 2009 6110 6117
4. J.L. Neira Biophysical and structural studies on the capsid protein of the human immunodeficiency virus type 1: a new drug target? Scientific World Journal 9 2009 409 419
5. E. Barklis, A. Afadhili, C. McQuaw, S. Yalamuri, A. Still, R.L. Barklis, B. Kukull, and C.S. López Characterization of the in vitro HIV-1 capsid assembly pathway J. Mol. Biol. 387 2009 376 389
6. T.R. Gamble, F.F. Vajdos, S. Yoo, D.K. Worthylake, M. Houseweart, W.I. Sundquist, and C.P. Hill Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid Cell 87 1996 1285 1294 (Pubitemid 27010111)
7. T.R. Gamble, S. Yoo, F.F. Vajdos, U.K. von Schwedler, D.K. Worthylake, H. Wang, J.P. McCutcheon, W.I. Sundquist, and C.P. Hill Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein Science 278 1997 849 853 (Pubitemid 27467920)
8. C. Momany, L.C. Kovari, A.J. Prongay, W. Keller, R.K. Gitti, B.M. Lee, A.E. Gorbalenya, L. Tong, J. McClure, L.S. Ehrlich, M.F. Summers, C. Carter, and M.G. Rossmann Crystal structure of dimeric HIV-1 capsid protein Nat. Struct. Biol. 3 1996 763 770 (Pubitemid 26303402)
9. R.K. Gitti, B.M. Lee, J. Walker, M.F. Summers, S. Yoo, and W.I. Sundquist Structure of the amino-terminal core domain of the HIV-1 capsid protein Science 273 1996 231 235 (Pubitemid 26285888)
10. D.K. Worthylake, H. Wang, S. Yoo, W.I. Sundquist, and C.P. Hill Structures of the HIV-1 capsid protein dimerization domain at 2.6 Å resolution Acta Crystallog. D 55 1999 85 92 (Pubitemid 29053804)
11. R.C. Craven, A.E. Leuredupree, R.A. Weldon, and J.W. Wills Genetic-analysis of the major homology region of the Rous sarcoma virus Gag protein J. Virol. 69 1995 4213 4227
12. M.L. Pardue, S. Rashkova, E. Casacubierta, P.G. DeBaryshe, J.A. George, and K.L. Traverse Two retrotransposons minatian telomeres in Drosophila Chromosome Res. 13 2005 443 453 (Pubitemid 41205628)
13. A. Zlotnick, S.J. Stahl, P.T. Wingfield, J.F. Conway, N. Cheng, and A.C. Steven Shared motifs of the capsid proteins of hepadnaviruses and retroviruses suggest a common evolutionary origin FEBS Lett. 431 1998 301 304 (Pubitemid 28352378)
14. T.M. Cairns, and R.C. Craven Viral DNA synthesis defects in assembly-competent Rous sarcoma virus CA mutants J. Virol. 75 2001 242 250
15. F.A. Mammano, A. Ohagen, S. Hoglund, and H.G. Gottlinger Role of the major homology region of human immunodeficiency virus type 1 in virion morphogenesis J. Virol. 68 1994 4927 4936 (Pubitemid 24226558)
16. C. Strambio-de-Castillia, and E. Hunter Mutational analysis of the major homology region of the Mason-Pfizer monkey virus by use of saturation mutagenesis J. Virol. 66 1992 7021 7032
17. J.G. Purdy, J.M. Flanagan, I.J. Ropson, K.E. Rennoll-Bankert, and R.C. Craven Critical role of conserved hydrophobic residues within the major homology region in mature retroviral capsid assembly J. Virol. 82 2008 5951 5961 (Pubitemid 351822268)
18. P.M. Lokhandwala, T.L.N. Nguyen, J.B. Bowzard, and R.C. Craven Cooperative role of the MHR and the CA dimerization helix in the maturation of the functional retrovirus capsid Virology 376 2008 191 198
19. X. Yu, Q. Wang, J.-C. Yang, I. Buch, C.-J. Tsai, B. Ma, S.Z.D. Cheng, R. Nussinov, and J. Zheng Mutational analysis and allosteric effects in the HIV-1 capsid protein carboxyl-terminal dimerization domain Biomacromolecules 10 2009 390 399
20. J.A.G. Briggs, J.D. Riches, B. Glass, V. Baratonova, G. Zanetti, and H.-G. Kräusslich Structure and assembly of immature HIV Proc. Natl. Acad. Sci. U.S.A. 106 2009 11090 11095
21. M.G. Mateu Conformational stability of dimeric and monomeric forms of the C-terminal domain of human immunodeficiency virus-1 capsid protein J. Mol. Biol. 318 2002 519 531 (Pubitemid 34734844)
22. M. del Alamo, J.L. Neira, and M.G. Mateu Thermodynamic dissection of a low-affinity protein-protein interface involved in human immunodeficiency virus assembly J. Biol. Chem. 278 2003 27923 27929 (Pubitemid 36899986)
23. L.A. Alcaraz, M. del Alamo, F.N. Barrera, M.G. Mateu, and J.L. Neira Flexibility in HIV-1 assembly subunits: solution structure of the monomeric C-terminal domain of the capsid protein Biophys. J. 2007 1264 1276 (Pubitemid 47330906)
24. M. del Alamo, G. Rivas, and M.G. Mateu Effect of macromolecular crowding agents on human immunodeficiency virus type 1 capsid protein assembly in vitro J. Virol. 79 2005 14271 14281 (Pubitemid 41552725)
25. S.C. Gill, and P.H. von Hippel Calculation of protein extinction coefficients from amino acid sequence data Anal. Biochem. 182 1989 319 326 (Pubitemid 19277112)
26. M.T. Garzón, M.C. Lidón-Moya, F.N. Barrera, A. Prieto, J. Gómez, M.G. Mateu, and J.L. Neira The dimerization domain of the HIV-1 capsid protein binds a capsid protein-derived peptide: a biophysical characterization Protein Sci. 13 2004 1512 1523 (Pubitemid 38669239)
27. C. Royer Fluorescence spectroscopy B.A. Shirley, Methods in Molecular Biology (vol. 40). Protein Stability and Folding: Theory and Practice 1995 Humana Press Totowa, NJ 65 89
28. J. Sancho, J.L. Neira, and A.R. Fersht An N-terminal fragment of barnase has residual helical structure similar to that of the refolding intermediate J. Mol. Biol. 224 1992 749 758
29. 15N chemical shift referencing in biomolecular NMR J. Biomol. NMR 6 1995 135 141
30. H.C. Wong, R. Shin, and N.R. Krishna Solution structure of a double mutant of the carboxy-terminal dimerization domain of the HIV-1 capsid protein Biochemistry 47 2008 2289 2297 (Pubitemid 351304535)
31. G. Bodenhausen, and D. Ruben Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy Chem. Phys. Lett. 69 1980 185 189
32. M. Piotto, V. Saudek, and V. Sklenar Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions J. Biomol. NMR 2 1992 661 665
33. L.A. Alcaraz, M. del Alamo, M.G. Mateu, and J.L. Neira Structural mobility of the monomeric C terminal domain of the HIV-1 capsid protein FEBS J. 275 2007 3299 3311
34. I.J. Byeon, X. Meng, J. Jung, G. Zhao, R. Yang, J. Ahn, J. Shi, J. Concel, C. Aiken, P. Zhang, and A.M. Gronenborn Structural convergence between cryo-EM and NMR reveals intersubunit interactions critical for HIV-1 capsid function Cell 139 2009 780 790
35. J. Sticht, M. Humbert, S. Findlow, J. Bodem, B. Müller, U. Dietrich, J. Werner, and H.-G. Kräusslich A peptide inhibitor of HIV-1 assembly in vitro Nat. Struct. Mol. Biol. 12 2005 671 677 (Pubitemid 43086272)
36. S. Bhattacharya, H. Zhang, A.K. Debnath, and D. Cowburn Solution structure of a hydrocarbon staple peptide inhibitor in complex with monomeric C-terminal domain of HIV-1 capsid J. Biol. Chem. 283 2008 16274 16278
37. R. Doménech, O. Abian, R. Bocanegra, J. Correa, A. Sousa-Herves, R. Riguera, M.G. Mateu, E. Fernandez-Megia, A. Velázquez-Campoy, and J.L. Neira Dendrimers as inhibitors of the dimerization of the capsid protein of HIV-1 Biomacromolecules 11 2010 2069 2078
38. C.R. Bodner, A.S. Maltsev, C.M. Dobson, and A. Bax Differential phospholipids binding of α-synuclein variants implicated in Parkinson's disease revealed by solution NMR spectroscopy Biochemistry 49 2010 862 871
39. S. Mokhtarzada, C. Yu, A. Brickeden, and W.-Y. Choy Structural characterization of partially disordered human chibby: insights into its function in the Wnt-signalling pathway Biochemistry 50 2011 715 726
40. V. Sklenar, and A. Bax Spin echo water suppression for the generation of pure-phase two-dimensional NMR spectra J. Magn. Reson. 74 1987 469 479
41. J. Anglister, S. Grzesiek, H. Ren, C.B. Klee, and A. Bax Isotope-edited multidimensional NMR of calcineurin B in the presence of the non-deuterated detergent CHAPS J. Biomol. NMR 3 1993 121 126
42. K. Wüthrich NMR of Nucleic Acids and Proteins 1986 Wiley & Sons NY
43. E. Hurtado-Gómez, M. Caprini, A. Prieto, and J.L. Neira The helical structure propensity in the first helix of the histidine phosphocarrier protein of Steptomyces coelicolor Protein Pept. Sci. 14 2007 281 290 (Pubitemid 46376861)
44. G. Prat-Gay Association of complementary fragments and the elucidation of protein folding pathways Prot. Eng. 9 1996 843 847 (Pubitemid 26366509)
45. S. Schwarzinger, G.J.A. Kroon, T.R. Foss, J. Chung, P.E. Wright, and H.J. Dyson Sequence-dependent correction of random coil NMR chemical shifts J. Am. Chem. Soc. 123 2001 2970 2978 (Pubitemid 32879567)
46. 1H chemical shifts in proteins J. Biomol. NMR 9 1997 359 369 (Pubitemid 127505398)
47. M.W. Pantoliano, E.C. Petrella, J.D. Kwanoski, V.S. Lobanov, J. Myslik, E. Graf, T. Carver, E. Asel, A.R. Springer, P. Lane, and F.R. Salemme High-density miniaturized thermal shift assays as a general strategy for drug discovery J. Biomol. Screen. 6 2001 429 440 (Pubitemid 34052847)
48. T.T. Waldron, and K.P. Murphy Stabilization of proteins by ligand binding: Application to drug screening and determination of unfolding energetics Biochemistry 42 2003 5058 5064 (Pubitemid 36532060)
49. J. Lapham, J.P. Rife, P.B. Moore, and D.M. Crothers Measurement of diffusion constants for nucleic acids by NMR J. Biomol. NMR 10 1997 255 262 (Pubitemid 127504671)
50. M. Lin, and C.K. Larive Detection of insulin aggregates with pulse field gradient nuclear magnetic resonance spectroscopy Anal. Biochem. 229 1995 214 220
51. P.W. Atkins, and J. de Paula Physical Chemistry 8th ed. 2006 Oxford University Press Oxford
52. L.S. Ehrlich, B.E. Agresta, and C.A. Carter Assembly of recombinant human immunodeficiency virus type capsid protein in vitro J. Virol. 66 1992 4874 4883
53. I. Gross, H. Hohenberg, and H.-G. Kräusslich In vitro assembly properties of purified bacterially expressed capsid protein of human immunodeficiciency virus Eur. J. Biochem. 249 1997 592 600 (Pubitemid 27455804)
54. J. Lanman, J. Sexton, M. Sakalian, and P. Prevelige Kinetic analysis of the role of intersubunit interactions in human immunodeficiency virus type 1 capsid assembly protein in vitro J. Virol. 76 2002 6900 6908 (Pubitemid 41246205)
55. R.L. Baldwin, and G.D. Rose Is protein folding hierarchic? Local structure and peptide folding Trends Biochem. Sci. 24 1999 77 83
56. D. Ivanov, O.V. Tsodikov, J. Kasanov, T. Ellenberger, G. Wagner, and T. Collins Domain-swapped dimerization of the HIV-1 capsid C-terminal domain Proc. Natl. Acad. Sci. U.S.A 104 2007 4353 4358 (Pubitemid 47186230)
57. E.R. Wright, J.B. Schooler, H.J. Ding, C. Kieffer, C. Fillmore, W.I. Sundquist, and G.J. Jensen Electron cryo-tomography of immature HIV-1 virions reveals the structure of the CA and SP1 Gag shells EMBO J. 26 2007 2218 2226 (Pubitemid 46625799)
58. B.J. Kovalevski, R. Kennedy, A. Khorchid, K. Kleiman, H. Matsuo, and K. Musier-Forsyth Critical roles of helix 4 of HIV-1 capsid C-terminal domain in interactions with human lysyl-tRNA synthetase J. Biol. Chem. 282 2007 32274 32279 (Pubitemid 350106427)
59. A. Velazquez-Campoy, S.A. Leavitt, and E. Freire Characterization of protein-protein interactions by isothermal titration calorimetry Methods Mol. Biol. 261 2004 35 54
60. W.L. DeLano The PyMOL Molecular Graphics System 2002 DeLano Scientific LLC San Carlos, CA, USA PyMOL molecular graphics system on World Wide Web URL http://www.pymol.org