Association equilibrium of the HIV-1 capsid protein in a crowded medium reveals that hexamerization during capsid assembly requires a functional C-domain dimerization interface

Biophysical Journal

Volumn 104, Issue 4, 2013, Pages 884-893

  Bocanegra, Rebeca ^a,c   Alfonso, Carlos ^b   Rodríguez Huete, Alicia ^a   Fuertes, Miguel Ángel ^a   Jiménez, Mercedes ^b   Rivas, Germán ^b   Mateu, Mauricio G ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^c CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; HUMAN IMMUNODEFICIENCY VIRUS 1; KINETICS; MOLECULAR GENETICS; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; CAPSID PROTEINS; HIV-1; KINETICS; MOLECULAR SEQUENCE DATA; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY;

EID: 84874129551     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.12.035     Document Type: Article

References (51)

1. B.K. Ganser-Pornillos, M. Yeager, and W.I. Sundquist The structural biology of HIV assembly Curr. Opin. Struct. Biol. 18 2008 203 217
2. B.K. Ganser-Pornillos, M. Yeager, and O. Pornillos Assembly and architecture of HIV Adv. Exp. Med. Biol. 726 2012 441 465
3. J.A. Briggs, and H.G. Kräusslich The molecular architecture of HIV J. Mol. Biol. 410 2011 491 500
4. W.I. Sundquist, and H.G. Kräusslich HIV-1 assembly, budding, and maturation Cold Spring Harb. Perspect. Med 2 2012 a006924
5. S. Li, and C.P. Hill J.T. Finch Image reconstructions of helical assemblies of the HIV-1 CA protein Nature 407 2000 409 413
6. J.A. Briggs, and T. Wilk S.D. Fuller Structural organization of authentic, mature HIV-1 virions and cores EMBO J. 22 2003 1707 1715
7. M.G. Mateu The capsid protein of human immunodeficiency virus: intersubunit interactions during virus assembly FEBS J. 276 2009 6098 6109
8. I.J. Byeon, and X. Meng A.M. Gronenborn Structural convergence between Cryo-EM and NMR reveals intersubunit interactions critical for HIV-1 capsid function Cell 139 2009 780 790
9. P.E. Prevelige Jr. New approaches for antiviral targeting of HIV assembly J. Mol. Biol. 410 2011 634 640
10. A.A. Waheed, and E.O. Freed HIV type 1 Gag as a target for antiviral therapy AIDS Res. Hum. Retroviruses 28 2012 54 75
11. R. Bocanegra, and A. Rodríguez-Huete M.G. Mateu Molecular recognition in the human immunodeficiency virus capsid and antiviral design Virus Res. 169 2012 388 410
12. C. Momany, and L.C. Kovari M.G. Rossmann Crystal structure of dimeric HIV-1 capsid protein Nat. Struct. Biol. 3 1996 763 770
13. R.K. Gitti, and B.M. Lee W.I. Sundquist Structure of the amino-terminal core domain of the HIV-1 capsid protein Science 273 1996 231 235
14. T.R. Gamble, and S. Yoo C.P. Hill Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein Science 278 1997 849 853
15. B.K. Ganser-Pornillos, A. Cheng, and M. Yeager Structure of full-length HIV-1 CA: a model for the mature capsid lattice Cell 131 2007 70 79
16. 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
17. R. Bocanegra, and M. Nevot M.G. Mateu Rationally designed interfacial peptides are efficient in vitro inhibitors of HIV-1 capsid assembly with antiviral activity PLoS ONE 6 2011 e23877
18. H. Zhang, and F. Curreli A.K. Debnath Antiviral activity of α-helical stapled peptides designed from the HIV-1 capsid dimerization domain Retrovirology 8 2011 1 18
19. J. Lanman, and J. Sexton P.E. Prevelige Jr. Kinetic analysis of the role of intersubunit interactions in human immunodeficiency virus type 1 capsid protein assembly in vitro J. Virol. 76 2002 6900 6908
20. J. Lanman, and T.T. Lam P.E. Prevelige Jr. Identification of novel interactions in human immunodeficiency virus type 1 capsid protein assembly in vitro J. Mol. Biol. 325 2003 759 772
21. O. Pornillos, and B.K. Ganser-Pornillos M. Yeager X-ray structures of the hexameric building block of the HIV capsid Cell 137 2009 1282 1292
22. O. Pornillos, and B.K. Ganser-Pornillos M. Yeager Disulfide bond stabilization of the hexameric capsomer of human immunodeficiency virus J. Mol. Biol. 401 2010 985 995
23. O. Pornillos, B.K. Ganser-Pornillos, and M. Yeager Atomic-level modeling of the HIV capsid Nature 469 2011 424 427
24. G.B. Mortuza, and L.F. Haire I.A. Taylor High-resolution structure of a retroviral capsid hexameric amino-terminal domain Nature 431 2004 481 485
25. L.A. Carlson, and J.A. Briggs H.G. Kräusslich Three-dimensional analysis of budding sites and released virus suggests a revised model for HIV-1 morphogenesis Cell Host Microbe 4 2008 592 599
26. A.P. Minton The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media J. Biol. Chem. 276 2001 10577 10580
27. R.J. Ellis Macromolecular crowding: obvious but underappreciated Trends Biochem. Sci. 26 2001 597 604
28. H.-X. Zhou, G. Rivas, and A.P. Minton Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences Annu. Rev. Biophys 37 2008 375 397
29. 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
30. V. Rincón, and R. Bocanegra M.G. Mateu Effects of macromolecular crowding on the inhibition of virus assembly and virus-cell receptor recognition Biophys. J. 100 2011 738 746
31. S. Campbell, and V.M. Vogt Self-assembly in vitro of purified CA-NC proteins from Rous sarcoma virus and human immunodeficiency virus type 1 J. Virol. 69 1995 6487 6497
32. I. Gross, H. Hohenberg, and H.-G. Kräusslich In vitro assembly properties of purified bacterially expressed capsid proteins of human immunodeficiency virus Eur. J. Biochem. 249 1997 592 600
33. B.K. Ganser, and S. Li W.I. Sundquist Assembly and analysis of conical models for the HIV-1 core Science 283 1999 80 83
34. M. del Alamo, and M.G. Mateu Electrostatic repulsion, compensatory mutations, and long-range non-additive effects at the dimerization interface of the HIV capsid protein J. Mol. Biol. 345 2005 893 906
35. C.C. Douglas, and D. Thomas P.E. Prevelige Jr. Investigation of N-terminal domain charged residues on the assembly and stability of HIV-1 CA Biochemistry 43 2004 10435 10441
36. S. Erickson-Viitanen, and J. Manfredi R. Swanstrom Cleavage of HIV-1 Gag polyprotein synthesized in vitro: sequential cleavage by the viral protease AIDS Res. Hum. Retroviruses 5 1989 577 591
37. S.C. Gill, and P.H. von Hippel Calculation of protein extinction coefficients from amino acid sequence data Anal. Biochem. 182 1989 319 326
38. P. Schuck Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling Biophys. J. 78 2000 1606 1619
39. P. Schuck, and M.A. Perugini D. Schubert Size-distribution analysis of proteins by analytical ultracentrifugation: strategies and application to model systems Biophys. J. 82 2002 1096 1111
40. A.P. Minton Modern Analytical Ultracentrifugation T.H. Schuster, T.H. Lave, 1994 Birkhauser Boston, MA 81 93
41. J.L. Cole Analysis of heterogeneous interactions Methods Enzymol. 384 2004 212 232
42. G. Rivas, J.A. Fernandez, and A.P. Minton Direct observation of the self-association of dilute proteins in the presence of inert macromolecules at high concentration via tracer sedimentation equilibrium: theory, experiment, and biological significance Biochemistry 38 1999 9379 9388
43. S. Zorrilla, and M. Jiménez A.P. Minton Sedimentation equilibrium in a solution containing an arbitrary number of solute species at arbitrary concentrations: theory and application to concentrated solutions of ribonuclease Biophys. Chem. 108 2004 89 100
44. G. Rivas, and A.P. Minton Beyond the second virial coefficient: sedimentation equilibrium in highly non-ideal solutions Methods 54 2011 167 174
45. S. Darawshe, G. Rivas, and A.P. Minton Rapid and accurate microfractionation of the contents of small centrifuge tubes: application in the measurement of molecular weight of proteins via sedimentation equilibrium Anal. Biochem. 209 1993 130 135
46. A.A. Fodeke, and A.P. Minton Quantitative characterization of polymer-polymer, protein-protein, and polymer-protein interaction via tracer sedimentation equilibrium J. Phys. Chem. B 114 2010 10876 10880
47. U.K. von Schwedler, and K.M. Stray W.I. Sundquist Functional surfaces of the human immunodeficiency virus type 1 capsid protein J. Virol. 77 2003 5439 5450
48. X. Yu, and Q. Wang J. Zheng Mutational analysis and allosteric effects in the HIV-1 capsid protein carboxyl-terminal dimerization domain Biomacromolecules 10 2009 390 399
49. 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
50. L.A. Alcaraz, and M. del Alamo J.L. Neira Flexibility in HIV-1 assembly subunits: solution structure of the monomeric C-terminal domain of the capsid protein Biophys. J. 93 2007 1264 1276
51. De Lano, W. L. 2002. The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA. http://www.pymol.org.