The cysteine residues of HIV-1 capsid regulate oligomerization and cyclophilin A-induced changes

Biophysical Journal

Volumn 88, Issue 3, 2005, Pages 2078-2088

  Homme, Marjorie Bon ^a   Carter, Carol ^a   Scarlata, Suzanne ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHILIN A; CYSTEINE; GAG PROTEIN; CAPSID PROTEIN; MULTIPROTEIN COMPLEX; RECOMBINANT PROTEIN;

ARTICLE; BINDING KINETICS; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; DISSOCIATION CONSTANT; ENZYME ACTIVITY; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROSTATIC PRESSURE; NONHUMAN; OLIGOMERIZATION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; REGULATORY MECHANISM; VIRION; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS MORPHOLOGY; VIRUS PATHOGENESIS; AMINO ACID SUBSTITUTION; BINDING SITE; CHEMISTRY; COMPARATIVE STUDY; DIMERIZATION; KINETICS; METABOLISM; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; MIRIDAE;

AMINO ACID SUBSTITUTION; BINDING SITES; CAPSID PROTEINS; CYCLOPHILIN A; CYSTEINE; DIMERIZATION; HIV-1; KINETICS; MULTIPROTEIN COMPLEXES; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; RECOMBINANT PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; VIRUS ASSEMBLY;

EID: 21244446315     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.053298     Document Type: Article

References (37)

1. Ackerson, B., O. Rey, J. Canon, and P. Krogstad. 1998. Cells with high cyclophilin A content support replication of human immunodeficiency virus type 1 Gag mutants with decreased ability to incorporate cyclophilin A. J. Virol. 72:303-308.
2. Agarwal, P. K. 2004. Cis/trans isomerization of HIV-1 capsid protein catalyzed by cyclophilin A: insights from computational and theoretical studies. Proteins. 56:449-463.
3. Berthet-Colominas, C., S. Monaco, A. Novelli, G. Sibai, F. Mallet, and S. Cusack. 1999. Head-to-tail dimers and interdomain flexibility revealed by the crystal structure of HIV-1 capsid protein (p24) complexed with a monoclonal antibody Fab. EMBO J. 18:1124-1136.
4. BonHomme, M., S. Wong, C. Carter, and S. Scarlata. 2003. The pH dependence of HIV-1 capsid assembly and its interaction with cyclophilin A. Biophys. Chem. 105:67-77.
5. Bosco, D., E. Eisenmesser, S. Pochapsky, W. Sundquist, and D. Kern. 2002. Catalysis of cis/trans isomerization in native HIV-1 capsid by human cyclophilin A. Proc. Natl. Acad. Sci. USA. 99:5247-5252.
6. Bosco, D., and D. Kern. 2004. Catalysis and binding of cyclophilin A with different HIV-1 capsid constructs. Biochemistry. 43:6110-6119.
7. Braaten, D., E. Franke, and J. Luban. 1996. Cyclophilin A is required for an early step in the life cycle of human immunodeficiency virus type 1 before the initiation of reverse transcription. J. Virol. 70:3551-3560.
8. Bukinsky, M., and A. Adzhubei. 1999. Viral protein R of HIV-1. Rev. Med. Virol. 8:39-49.
9. Bukovsky, A. A., A. Weimann, M. A. Accola, and H. G. Gottlinger. 1997. Transfer of the HIV-1 cyclophilin-binding site to simian immunodeficiency virus from Macaca mulatta can confer both cyclosporin sensitivity and cyclosporin dependence. Proc. Natl. Acad. Sci. USA. 94:10943-10948.
10. Campbell, S., and A. Rein. 1999. In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain. J. Virol. 73:2270-2278.
11. Colgan, J., H. E. Yuan, E. K. Franke, and J. Luban. 1996. Binding of the human immunodeficiency virus type 1 Gag polyprotein to cyclophilin A is mediated by the central region of capsid and requires Gag dimerization. J. Virol. 70:4299-4310.
12. Dietrich, L., L. Ehrlich, T. LaGrassa, D. Ebbets-Reed, and C. Carter. 2001. Structural consequences of cyclophilin A binding on maturational refolding in human immunodfeiciency virus type 1 capsid protein. J. Virol. 75:4721-4733.
13. Dorfman, T., A. Weimann, A. Borsetti, C. T. Walsh, and H. G. Gottlinger. 1997. Active-site residues of cyclophilin A are crucial for its incorporation into human immunodeficiency virus type 1 virions. J. Virol. 71:7110-7113.
14. Ehrlich, L. S., T. Liu, S. Scarlata, B. Chu, and C. A. Carter. 2001. HIV-1 capsid protein forms spherical (immature-like) and tubular (mature-like) particles in vitro: structure switching by pH-induced conformational changes. Biophys. J. 81:586-594.
15. Endrich, M., P. Gehrig, and H. Gehring. 1996. Maturation-induced conformational changes of HIV-1 capsid protein and identification of two high affinity sites for cyclophilin in the C-terminal domain. J. Biol. Chem. 274:5326-5332.
16. Franke, E. K., H. E. Yuan, and J. Luban. 1994. Specific incorporation of cyclophilin A into HIV-1 virions. Nature. 372:359-362.
17. Gamble, T. R., F. F. Vajdos, S. Yoo, D. K. Worthylake, M. Houseweart, W. I. Sundquist, and C. P. Hill. 1996. Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell. 87: 1285-1294.
18. Gitti, R., B. Lee, J. Walker, M. K. Summers, S. Yoo, and W. Sundquist. 1996. Structure of the N-terminal core domain of the HIV-1 capsid protein. Science. 273:231-235.
19. Gross, I., H. Hohenberg, C. Huckhagel, and H.-G. Krausslich. 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.
20. Henklein, P., K. Bruns, M. P. Sherman, U. Tessmer, K. Licha, J. Kopp, C. M. de Noronha, W. C. Greene, V. Wray, and U. Schubert. 2000. Functional and structural characterization of synthetic HIV-1 vpr that transduces cells, localizes to the nucleus, and induces G2 cell cycle arrest. J. Biol. Chem. 275:32016-32026.
21. Heremans, K. A. H. 1992. High pressure effects upon proteins and other biomolecules. Annu. Rev. Biophys. Bioeng. 11:1-21.
22. Howard, B. R., F. F. Vajdos, S. Li, W. I. Sundquist, and C. P. Hill. 2003. Structural insights into the catalytic mechanism of cyclophilin A. Nat. Struct. Biol. 475-481.
23. Kattendbeck, B., A. von Poblotzki, A. Rohrhofer, H. Wolf, and S. Modrow. 1997. Inhibition of human immunodeficiency virus type 1 particle formation by alteration of defined amino acids within the C-terminus of capsid. J. Genet. Virol. 78:2489-2496.
24. Lanman, J., J. Sexton, M. Sakalian, and P. E. Prevelige Jr. 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.
25. Liang, C., J. Hu, J. B. Whitney, L. Kleiman, and M. A. Wainberg. 2003. A structurally disordered region at the C terminus of capsid plays essential roles in multimerization and membrane binding of the Gag protein of human immunodeficiency virus type 1. J. Virol. 77:1772-1783.
26. Mammano, F., A. Ohagen, S. Hoglund, and H. Gottlinger. 1994. Role of the major homology region of human immunodeficiency virus type 1 in virion morphogenesis. J. Virol. 68:4927-4936.
27. McDermott, G., L. Farrell, R. Ross, and E. Barklise. 1996. Structural analysis of human immunodeficiency virus type 1 Gag protein interactions using cysteine-specific reagents. J. Virol. 70:5106-5114.
28. Recin, A. S., S. R. Paik, R. D. Berkowitz, J. Luban, I. Lowy, and S. P. Goff. 1995. Linker insertion mutation in the human immunodeficeincy virus type 1 gag gene: effects on virion particle assembly, release and mfectivity. J. Virol. 69:642-650.
29. Saphire, A., M. Bobardt, and P. Gallay. 1999. Host cyclophilin A mediates HIV-I attachment to target cells via heparans. EMBO J. 18:6771-6785.
30. Scarlata, S., and C. Carter. 2003. Role of HIV-1 gag domains in viral assembly. Biochim. Biophys. Acta. 1614:62-72.
31. Sherry, B., G. Zybarth, M. Alfano, L. Dubrobsky, R. Mitchell, D. Rich, P. Ulrich, R. Bucala, A. Cerami, and M. Bukrinsky. 1998. Role of cyclophilin A in the uptake of HIV-1 by macrophages and T lymphocytes. Proc. Natl. Acad. Sci. USA. 95:1758-1763.
32. Steinkasserer, A., R. Harrison, A. Billich, F. Hammerschmid, G. Werner, B. Wolff, P. Peichl, G. Palfi, W. Schnitzel, E. Mlynar, and others. 1995. Mode of action of SDZ NIM 811, a nonimmunosuppressive cyclosporin A analog with activity against human immunodeficiency virus type 1 (HIV-1): interference with early and late events in HIV-1 replication. J. Virol. 69:814-824.
33. Towers, G. J., T. Hatziioannou, S. Cowan, S. P. Goff, J. Luban, and P. D. Bieniasz. 2003. Cyclophilin A modulates the sensitivity of HIV-1 to host restriction factors. Nat. Med. 9:1138-1143.
34. von Poblotzki, A., R. Wagner, M. Niedrig, G. Wanner, H. Wolf, and S. Modrow. 1993. Identification of a region of Pr55gag-polyprotein essential for HIV-1 particle formation. Virology. 193:981-985.
35. von Schwedler, U., T. Stemmler, V. Klishko, S. Li, K. Albertine, D. Davis, and W. Sundquist. 1998. Proteolytic refolding of the HIV-1 capsid protein amino -terminus facilitates viral core assembly. EMBO J. 17: 1555-1568.
36. Zander, K., M. P. Sherman, U. Tessmer, K. Bruns, V. Wray, A. T. Prechtel, E. Schubert, P. Henklein, J. Luban, J. Neidleman, W. C. Greene, and U. Schubert. 2003. Cyclophilin A interacts with HIV-1 Vpr and is required for its functional expression. J. Biol. Chem. 278:43202-43213.
37. Zydowsky, L., F. Etzkorn, H. Y. Change, S. B. Ferguson, L. A. Stolz, S. I. Ho, and C. T. Walsh. 1992. Active site mutants of human cyclophilin A separate peptidyl-prolyl isomerase activity from cyclosporin A binding and calcineurin inhibition. Protein Sci. 1:1092-1099.