Crystal structure of dimeric HIV-1 capsid protein

Nature Structural Biology

Volumn 3, Issue 9, 1996, Pages 763-770

  Momany, Cory ^a   Kovari, Ladislau C ^a   Prongay, Andrew J ^a,b   Keller, Walter ^a,c   Gitti, Rossitza K ^d   Lee, Brian M ^d   Gorbalenya, Alexander E ^a,e   Tong, Liang ^a,f   McClure, Jan ^g   Ehrlich, Lorna S ^h   Summers, Michael F ^d   Carter, Carol ^h   Rossmann, Michael G ^a  

^a PURDUE UNIVERSITY   (United States)

^b MERCK RESEARCH LABORATORIES   (United States)

^c UNIVERSITY OF GRAZ   (Austria)

^d UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

^e CHUMAKOV INSTITUTE OF POLIOMYELITIS AND VIRAL ENCEPHALITIDES   (Russian Federation)

^f BOEHRINGER INGELHEIM PHARMACEUTICALS INC   (United States)

^g BRISTOL MYERS SQUIBB   (United States)

^h STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; DIMER; VIRUS PROTEIN;

ARTICLE; CRYSTAL STRUCTURE; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; X RAY DIFFRACTION;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; BINDING SITES, ANTIBODY; CAPSID; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; HIV ANTIBODIES; HIV-1; HUMANS; MICE; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY;

EID: 16044367113     PISSN: 10728368     EISSN: None     Source Type: Journal    
DOI: 10.1038/nsb0996-763     Document Type: Article

References (69)

1. Nermut, M.V. & Thomas, D. Fullerene-like organization of HIV gag-protein shell in virus-like particles produced by recombinant baculovirus. Virology 198, 288-296 (1994).
2. Gelderblom, H.R., Hausmann, E.H.S., Özel, M., Pauli, G. & Koch, M.A. Fine structure of human immunodeficiency virus (HIV) and immunolocalization of structural proteins. Virology 156, 171-176 (1987).
3. Kaplan, A.H. & Swanstrom, R. Human immunodeficiency virus type 1 gag proteins are processed into two cellular compartments. Proc. Natl. Acad. Sci. USA 88, 4528-4532 (1991).
4. Pal, R. et al. Myristoylation of gag proteins of HIV-1 plays an important role in virus assembly. AIDS Res. Hum. Retroviruses 6, 721-730 (1990).
5. Bryant, M. & Ratner, L Myristoylation-dependent replication and assembly of human immunodeficiency virus 1. Proc. Natl. Acad. Sci. USA 87, 523-527 (1990).
6. Chazal, N, Carrière, C, Gay, B. & Boulanger, P. Phenotypic characterization of insertion mutants of the human immunodeficiency virus type 1 gag precursor expressed in recombinant baculovirus-infected cells. J. Virol. 68, 111-122 (1994).
7. Carrière, C, Gay, B., Chazal, N., Morin, N. & Boulanger, P. Sequence requirements for encapsidation of deletion mutants and chimeras of human immunodeficiency virus type 1 gag precursor into retrovirus-like particles. J. Virol. 69, 2366-2377 (1995).
8. Dorfman, T., Bukovsky, A, Öhagen, Å., Höglund, S. & Göttlinger, H.G. Functional domains of the capsid protein of human immunodeficiency virus type 1. J. Virol. 68, 8180-8187 (1994).
9. Hong, S.S. & Boulanger, P. Assembly-defective point mutants of the human immunodeficiency virus type 1 gag precursor phenotypically expressed in recombinant baculovirus-infected cells. J. Virol. 67, 2787-2798 (1993).
10. Srinivasakuman, N., Hammarskjöld, M.-L. & Rekosh, D. Characterization of deletion mutations in the capsid region of human immunodeficiency virus type 1 that affect particle formation and gag-pol precursor incorporation. J. Virol. 69, 6106-6114 (1995).
11. gag-polyprotein essential for HIV-1 particle formation. Virology 193, 981-985 (1993).
12. Zhao, Y, Jones, I.M, Hockley, D.J., Nermut M.V. & Roy, P. Complementation of human immunodeficiency virus (HIV-1) gag particle formation. Virology 199, 403-408 (1994).
13. Zhang, W.-H., Hockley, D.J., Nermut, M.V., Morikawa, Y. & Jones, I.M. Gag-Gag interactions in the C-terminal domain of human immunodeficiency virus type 1 p24 capsid antigen are essential for Gag particle assembly. J. Gen. Virol. 77, 743-751 (1996).
14. Patarca, R. & Haseltine, W.A. A major retroviral core protein related to EPA and TIMP. Nature 318, 390 (1985).
15. Ratner, L et al. Complete nucleotide sequence of the AIDS virus, HTLV-III. Nature 313, 277-283 (1985).
16. Wang, C-T. & Barklis, E. Assembly, processing and infectivity of human immunodeficiency virus type 1 gag mutants. J. Virol. 67, 4264-4273 (1993).
17. Reicin, A.S. et al. Linker insertion mutations in the human immunodeficiency virus type 1 gag gene: effects on virion particle assembly, release and infectivity. J. Virol. 69, 642-650 (1995).
18. Luban, J., Bossolt, K.L., Franke, E.K., Kalpana, G.V. & Goff, S.P. Human immunodeficiency virus type 1 gag protein binds to cyclophilins A and B. Cell 73, 1067-1078 (1993).
19. Franke, E.K. et al. Cyclophilin binding to the human immunodeficiency virus type 1 gag polyprotein is mimicked by an anti-cyclosporine antibody. J. Virol. 69, 5821-5823 (1995).
20. Thali, M. et al. Functional association of cydophilin A with HIV-1 virions. Nature 372, 363-365 (1994).
21. Billich, A. et al. Mode of action of SDZ NIM 811,a nonimmunosuppressive cyclosporin A analog with activity against human immunodeficiency virus (HIV) type 1: interference with HIV protein-cyclophilin A interactions. J. Virol. 69, 2451-2461 (1995).
22. Klasse, P.J, Schultz, T.F. & Willison, K.R. Cyclophilins unfold the gag? Nature 365, 395-396 (1993).
23. Rossmann, M.G. Antiviral agents targeted to interact with viral capsid proteins and a possible application to human immunodeficiency virus. Proc. Natl. Acad. Sci. USA 85, 4625-4627 (1988).
24. Argos, P. A possible homology between immunodeficiency virus p24 core protein and picornaviral VP2 coat protein: prediction of HIV p24 antigenic sites. EMBO J. 8, 779-785 (1989).
25. Langedijk, J.P.M, Schalken, J.J, Tersmette, M, Huisman, J.G. & Meloen, R.H. Location of epitopes on the major core protein p24 of human immunodeficiency virus. J. Gen. Virol. 71, 2609-2614 (1990).
26. Robert-Hebmann, V. et al. Clonal analysis of murine B cell response to the human immunodeficiency virus type 1 (HIV1)-gag p17 and p25 antigens. Mol. Immunol. 29, 729-738 (1992).
27. Coates, A.R.M, Cookson, J., Barton, G.J., Zvelebil, M.J. & Sternberg, M.J.E. AIDS vaccine predictions. Nature 326, 549-550 (1987).
28. Ehrlich, L.S., Agresta, B.E., Gelfand, C.A., Jentoft, J. & Carter, C.A. Spectral analysis and tryptic susceptibility as probes of HIV-1 capsid protein structure. Virology 204, 515-525 (1994).
29. Misselwitz, R, Hausdorf, G., Welfle, K., Hohne, W.E. & Welfle, H. Conformation and stability of recombinant HIV-1 capsid protein p24 (rp24). Biochim. Biophys. Acta 1250, 9-18 (1995).
30. Burns, N.R. et al. Purification and secondary structure determination of simian immunodeficiency virus p27. J. Mol. Biol. 216, 207-211 (1990).
31. Burnette, W.N., Holladay, LA & Mitchell, W.M. Physical and chemical properties of Moloney murine leukemia virus p30 protein: a major core structural component exhibiting high helicity and self-association. J. Mol. Biol. 107,131-143 (1976).
32. Prongay, A.J. et al. Preparation and crystallization of a human immunodeficiency virus p24-Fab complex. Proc. Natl. Acad. Sci. USA 87, 9980-9984 (1990).
33. Air, G.M, Webster, R.G., Colman, P.M. & Laver, W.G. Distribution of sequence differences in influenza N9 neuraminidase of tern and whale viruses and crystallization of the whale neuraminidase complexed with antibodies. Virology 160, 346-354 (1987).
34. Stammers, D.K. et al. Structural studies on human immunodeficiency virus reverse transcriptase in Use of X-ray Crystallography in the Design of Antiviral Agents, (eds. Laver, W.G. & G.M. Air) 309-319. (Academic Press, Inc., San Diego, 1990).
35. Jacobo-Molina, A. et al. Crystals of a ternary complex of human immunodeficiency virus type 1 reverse transcriptase with a monoclonal antibody Fab fragment and double-stranded DNA diffract X-rays to 3.5 Å resolution. Proc. Natl. Acad. Sci. USA 88, 10895-10899 (1991).
36. v fragment-mediated crystallization of the membrane protein bacterial cytochrome c oxidase. Nature Struct Biology 2, 842-845 (1995).
37. Gitti, R.K. et al. Structure of the N-terminal core domain of the HIV-1 capsid protein. Science 273, 231-235 (1996).
38. Grimes, J., Basak, A.K., Roy, P. & Stuart, D. The crystal structure of bluetongue virus VP7. Nature 373, 167-170 (1995).
39. Munshi, S. et al. Membrane translocation of viral RNA: deductions from the 2.8 Å structure of a T=4 virus. J. Mol. Biol. In the press (1996).
40. Cheng, R.H. et al. Functional implications of quasi-equivalence in a T= 3 icosahedral animal virus established by cryo-electron microscopy and X-ray crystallography. Structure 2, 271-282 (1994).
41. Rao, Z. et al. Crystal structure of SIV matrix antigen and implications for virus assembly. Nature 378, 743-747 (1995).
42. Hill, C.P., Worthylake, D., Bancroft D.P., Christensen, A.M. & Sundquist, W.I. Crystal structures of the trimeric human immunodeficiency virus type 1 matrix protein: implications for membrane association and assembly. Proc. Natl. Acad. Sci. USA 93, 3099-3104 (1996).
43. Matthews, S. et al. Structural similarity between the p17 matrix protein of HIV-1 and interferon-γ. Nature 370, 666-668 (1994).
44. Massiah, M.A. et al. Three-dimensional structure of the human immunodeficiency virus type 1 matrix protein. J. Mol. Biol. 244, 198-223 (1994).
45. O'Shea, E.K., Klemm, J.D., Kim, P.S. & Alber, T. X-ray structure of the GCN4 leucine zipper, a two-stranded, parallel coiled coil. Science 254, 539-544 (1991).
46. Crick, F.H.C The packing of α-helices: simple coiled-coils. Acta Crystallogr. 6, 689-697 (1953).
47. Crick, F.H.C The Fourier transform of a coiled-coil. Acta Crystallogr. 6, 685-689 (1953).
48. Harbury, P.B., Zhang, T., Kim, P.S. & Alber, T. A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants. Science 262, 1401-1407 (1993).
49. Cohen, C & Parry, D.A.D. α-helical coiled coils and bundles: how to design an α-helical protein. Proteins 7, 1-15 (1990).
50. Harbury, P.B., Kim, P.S. & Alber, T. Crystal structure of an isoleucine-zipper trimer. Nature 371, 80-83 (1994).
51. Higgins, D.G., Bleasby, A.J. & Fuchs, R. CLUSTAL V: improved software for multiple sequence alignment. Comp. Appl. Biosci. 8, 189-191 (1992).
52. Rost B. & Sander, C Prediction of protein secondary structure at better than 70% accuracy. J. Mol. Biol. 232, 584-599 (1993).
53. McClure, MA Evolution of retroposons by acquisition or deletion of retrovirus-like genes. Mol. Biol. Evol. 8, 835-856 (1991).
54. Partin, K., Kräusslich, H.-G., Ehrlich, L, Wimmer, E. & Carter, C. Mutational studies of a native substrate of the human immunodeficiency virus type 1 proteinase. J. Virol. 64, 3938-3947 (1990).
55. Rossmann, M.G. Viral cell recognition and entry. Prot. Sci. 3, 1712-1725 (1994).
56. Rosé, S. et al. Characterization of HIV-1 p24 self-association using analytical affinity chromatography. Proteins 13, 112-119 (1992).
57. Wikoff, W.R. et al. The structure of a neutralized virus: canine parvovirus complexed with neutralizing antibody fragment. Structure 2, 595-607 (1994).
58. Kallen, J. & Walkinshaw, M.D. The X-ray structure of a tetrapeptide bound to the active site of human cyclophilin A. FEBS Letters 300, 286-290 (1992).
59. Franke, E.K., Yuan, H.E.H. & Luban, J. Specific incorporation of cydophilin A into HIV-1 virions. Nature 372, 359-362 (1994).
60. Ehrlich, L.S., Kräusslich, H.-G., Wimmer, E. & Carter, C.A. Expression in Eschericia coli and purification of human immunodeficiency virus type 1 capsid protein (p24). AIDS Res. Hum. Retroviruses 6, 1169-1175 (1990).
61. Kovari, L.C., Momany, C & Rossmann, M.G. The use of antibody fragments for crystallization and structure determinations. Structure 3, 1291-1293 (1995).
62. Larrick, J.W. et al. Rapid cloning of rearranged immunoglobulin genes from human hybridoma cells using mixed primers and the polymerase chain reaction. Biochem. Biophys. Res. Comm. 160, 1250-1256 (1989).
63. Otwinowski, Z. DENZO in Data Collection and Processing, (eds. Sawyer, L., N. Isaacs & S. Bailey) 56-62 (SERC Daresbury Laboratory, Warrington, UK, 1993).
64. Collaborative Computational Project Number 4 The CCP4 Suite: programs for protein crystallography. Acta Crystallogr. D50, 760-763 (1994).
65. Cowtan, K.D. & Main, P. Improvement of macromolecular electron-denisty maps by the simultaneous application of real and reciprocal space constraints. Acta Crystallogr. D49, 148-157 (1993).
66. Brünger, A.T. X-PLOR, Version 3.1 Manual: A System for X-ray Crystallography and NMR (New Haven:Yale University Press, 1993).
67. Jones, TA, Zou, J.-Y., Cowan, S.W. & Kjeldgaard, M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A47, 110-119 (1991).
68. Cullis, A.F., Muirhead, H, Perutz, M.F., Rossmann, M.G. & North, A.C.T. The structure of haemoglobin. IX. A three-dimensional Fourier synthesis at 5.5 Å resolution: description of the structure. Proc Roy. Soc. Lond. A265, 161-187 (1962).
69. Kraulis, P. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950 (1991).