Investigation of N-terminal domain charged residues on the assembly and stability of HIV-1 CA

Biochemistry

Volumn 43, Issue 32, 2004, Pages 10435-10441

  Douglas, Chanel C ^a   Thomas, Dennis ^a,b   Lanman, Jason ^a,c   Prevelige Jr , Peter E ^a  

^a University of Alabama at Birmingham   (United States)

^b BRANDEIS UNIVERSITY   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOLOGY; MONOMERS; PROTEINS; VIRUSES;

CAPSID PROTEINS (CA); MUTATIONS;

BIOCHEMISTRY;

CAPSID PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CIRCULAR DICHROISM; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; VIRION; VIRUS INFECTIVITY; VIRUS MUTANT; WILD TYPE;

CAPSID PROTEINS; DIMERIZATION; ELECTROSTATICS; HIV-1; HUMANS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; VIRUS ASSEMBLY;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; RNA VIRUSES;

EID: 4043142786     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049359g     Document Type: Article

References (45)

1. Freed, E. O. (1998) HIV-1 gag proteins: diverse functions in the virus life cycle, Virology 251, 1-15.
2. Hunter, E. (1994) Macromolecular interactions in the assembly of HIV and other retroviruses, Semin. Virol. 5, 71-83.
3. Mervis, R. J., Ahmad, N., Lillehoj, E. P., Raum, M. G., Salazar, F. H., Chan, H. W., and Venkatesan, S. (1988) The gag gene products of Human Immunodeficiency Virus type 1 : alignment within the gag open reading frame, identification of posttranslational modifications, and evidence for alternative gag precursors, J. Virol. 62, 3993-4002.
4. Turner, B. G., and Summers, M. F. (1999) Structural biology of HIV1, J. Mol. Biol. 285, 1-32.
5. Nermut, M. V., and Hockley, D. J. (1996) Comparative morphology and structural classification of retroviruses, Curr. Topics Microbiol. Immunol. 214, 1-24.
6. Jacks, T., Power, M. D., Masiarz, F. R., Luciw, P. A., Barr, P. J., and Varmus, H. E. (1988) Characterization of ribosomal frame-shifting in HIV-1 gag-pol expression, Nature 331, 280-283.
7. Fuller, S. D., Wilk, T., Gowen, B. E., Krausslich, H. G., and Vogt, V. M. (1997) Cryoelectron microscopy reveals ordered domains in the immature HIV-1 particle, Curr. Biol. 7, 729-738.
8. Wilk, T., Gross, I., Gowen, B. E., Rutten, T., de Haas, F., Welker, R., Krausslich, H. G., Boulanger, P., and Fuller, S. D. (2001) Organization of immature human immunodeficiency virus type 1, J. Virol. 75, 759-771.
9. Dorfman, T., Bukovsky, A., Ohagen, A., Hoglund, S., and Gottlinger, H. (1994) Functional domains of the capsid protein of human immunodeficiency virus type 1, J. Virol. 68, 8180-8187.
10. Fitzon, T., Leschonsky, B., Bieler, K., Paulus, C., Schroder, J., Wolf, H., and Wagner, R. (2000) Proline Residues in the HIV-1 NH2-Terminal Capsid Domain: Structure Determinants for Proper Core Assembly and Subsequent Steps of Early Replication, Virology 268, 294-307.
11. Reicin, A., Paik, S., Berkowitz, R., Luban, J., Lowy, I., and Goff, S. (1995) 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.
12. Reicin, A., Ohagen, A., Yin, L., Hoglund, S., and Goff, S. (1996) The role of Gag in human immunodeficiency virus type 1 virion morphogenesis and early steps of the viral life cycle, J. Virol. 70, 8645-8652.
13. 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 and Are Blocked in Initiation of Reverse Transcription in Infected Cells, J. Virol. 75, 9357-9366.
14. von Schwedler, U. K., Stemmler, T. L., Klishko, 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.
15. Wang, C., and Barklis, E. (1993) Assembly, processing, and infectivity of human immunodeficiency virus type 1 gag mutants, J. Virol. 67, 4264-4273.
16. Forshey, B. M., von Schwedler, U., 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.
17. McDonald, D., Vodicka, M. A., Lucero, G., Svitkina, T. M., Borisy, G. G., Emerman, M., and Hope, T. J. (2002) Visualization of the intracellular behavior of HIV in living cells, J. Cell Biol. 159, 441-452.
18. Sodeik, B. (2002) Unchain my heart, baby let me go-the entry and intracellular transport of HIV, J. Cell Biol. 159, 393-395.
19. Campbell, S., and Vogt, V. (1995) Self-assembly in vitro of purified CA-NC proteins from Rous sarcoma virus and human immunodeficiency virus type 1, J. Virol. 69, 6487-6497.
20. Ehrlich, L., Agresta, B., and Carter, C. (1992) Assembly of recombinant human immunodeficiency virus type 1 capsid protein in vitro, J. Virol. 66, 4874-4883.
21. Gross, I., Hohenberg, H., and Krausslich, H. (1997) In vitro assembly properties of purified bacterially expressed capsid proteins of human immunodeficiency virus, Eur. J. Biochem. 249, 592-600.
22. Ganser, B. K., Li, S., Klishko, 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.
23. 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.
24. 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 cyclophilin A bound to the amino-terminal domain of HIV-1 capsid, Cell 87, 1285-1294.
25. 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.
26. 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.
27. 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. D55 (Pt 1), 85-92.
28. Tang, C., Ndassa, Y., and Summers, M. F. (2002) Structure of the N-terminal 283-residue fragment of the immature HIV-1 Gag polyprotein, Nat. Struct. Biol. 9, 537-543.
29. von Schwedler, U. K., Stray, K. M., Garrus, J. E., and Sundquist, W. I. (2003) Functional surfaces of the human immunodeficiency virus type 1 capsid protein, J. Virol. 77, 5439-5450.
30. Lanman, J., Lam, T. T., Barnes, S., Sakalian, M., Emmett, M. R., Marshall, A. G., and Prevelige, P. E., Jr. (2003) Identification of novel interactions in HIV-1 capsid protein assembly by high-resolution mass spectrometry, J. Mol. Biol. 325, 759-772.
31. Ganser-Pornillos, B. K., von Schwedler, U. K., Stray, K. M., Aiken, C., and Sundquist, W. I. (2004) Assembly properties of the human immunodeficiency virus type 1 CA protein, J. Virol. 78, 2545-2552.
32. Lanman, J., Sexton, J., Sakalian, M., and Prevelige, P. E., 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.
33. Laue, T. M., Shah, B. D., Ridgeway, T. M., and Pelletier, S. L. (1992) in Analytical ultracentrifugation in biochemistry and polymer science (Al, S. E. H., Ed.) pp 90-125, The Royal Society of Chemistry, Cambridge, UK.
34. Johnson, M. L., Correia, J. J., Yphantis, D. A., and Halvorson, H. R. (1981) Analysis of data from the analytical ultracentrifuge by nonlinear least-squares techniques, Biophys. J. 36, 575-588.
35. Schreiber, G., and Fersht, A. R. (1996) Rapid, electrostatically assisted association of proteins, Nat. Struct. Biol. 3, 427-431.
36. Andreu, J. M., and Timasheff, S. N. (1986) The measurement of cooperative protein self-assembly by turbidity and other techniques, Methods Enzymol. 130, 47-59.
37. Harper, J. D., and Lansbury, P. T. (1997) Models of Amyloid Seeding in Alzheimer's Disease and Scrapie: Mechanistic Truths and Physiological Consequences of the Time-Dependent Solubility of Amyloid Proteins, Ann. Rev. Biochem. 66, 385-407.
38. Prevelige, P. E., Jr., Thomas, D., and King, J. (1993) Nucleation and growth phases in the polymerization of coat and scaffolding subunits into icosahedral procapsid shells, Biophys. J. 64, 824-835.
39. Oosawa, F., and Kasai, M. (1962) A theory of Linear and Helical Aggregations of Macromolecules, J. Mol. Biol. 4, 10-21.
40. del Alamo, 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.
41. Briggs, J. A., Wilk, T., Welker, R., Krausslich, H. G., and Fuller, S. D. (2003) Structural organization of authentic, mature HIV-1 virions and cores, EMBO. J. 22, 1707-1715.
42. Coffin, J. M., Hughes, S. H., and Varmus, H. E. (1997) Retroviruses, Cold Spring Harbor Laboratory Press, Plainview, NY.
43. Tang, C., Loeliger, E., Luncsford, P., Kinde, I., Beckett, D., and Summers, M. F. (2004) Entropic switch regulates myristate exposure in the HIV-1 matrix protein, Proc. Natl. Acad. Sci. U.S.A. 101, 517-522.
44. Morikawa, Y., Zhang, W. H., Hockley, D. J., Nermut, M. V., and Jones, I. M. (1998) Detection of a trimeric human immunodeficiency virus type 1 gag intermediate is dependent on sequences in the matrix protein, p17, J. Virol. 72, 7659-7663.
45. Hill, C. P., Worthylake, D., Bancroft, D. P., Christensen, A. M., and Sundquist, W. I. (1996) Crystal structures of the trimeric human immunodeficiency virus type 1 matrix protein: Implications for membrane association and assembly, PNAS 93, 3099-3104.