Structural studies of HIV-1 Gag p6ct and Its interaction with Vpr determined by solution nuclear magnetic resonance

Biochemistry

Volumn 48, Issue 11, 2009, Pages 2355-2367

  Salgado, Gilmar F ^a,b,c,d,e   Marquant, Rodrigue ^a,b,c,d   Vogel, Alexander ^a,b,c   Alves, Isabel D ^a,b,c,f   Feller, Scott E ^a,b,c   Morellet, Nelly ^a,b,c,d   Bouaziz, Serge ^a,b,c,d  

^a Centre National de la Recherche Scientifique   (France)

^b WABASH COLLEGE   (United States)

^c SORBONNE UNIVERSITÉ   (France)

^d CNRS UMR8151   (France)

^e ECOLE NORMALE SUPÉRIEURE   (France)

^f Centre National de la Recherche Scientifique   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BI LAYERS; C TERMINUS; C-TERMINAL REGIONS; ESCAPE MECHANISMS; HUMAN CELLS; HUMAN IMMUNODEFICIENCY VIRUS TYPE-1; MATRIXES; MICELLE SURFACES; MOLECULAR-DYNAMICS SIMULATIONS; MULTIVESICULAR BODIES; N TERMINALS; NEW RESULTS; PLASMON WAVEGUIDE RESONANCES; PROTEIN CORES; SORTING PROCESS; STRUCTURAL STUDIES; THREE-DIMENSIONAL STRUCTURES; VIRAL PROTEINS;

AMINES; AMINO ACIDS; CYTOLOGY; DIFFERENTIAL SCANNING CALORIMETRY; DYNAMICS; MICELLES; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; ORGANIC ACIDS; PRESSURIZED WATER REACTORS; RESONANCE; THREE DIMENSIONAL;

CELL MEMBRANES;

GAG PROTEIN; PHENYLALANINE; TYROSINE; VPR PROTEIN;

ADSORPTION; ALPHA HELIX; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; HUMAN IMMUNODEFICIENCY VIRUS 1; MICELLE; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIMULATION; VIRION; VIRUS ASSEMBLY; VIRUS INFECTIVITY; VIRUS MUTATION;

AMINO ACID SEQUENCE; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; VPR GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 64849112013     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801794v     Document Type: Article

References (52)

1. Gottlinger, H. G., Dorfman, T., Sodroski, J. G., and Haseltine, W. A. (1991) Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release. Proc. Natl. Acad. Sci. U.S.A. 88, 3195-3199.
2. Huang, M., Orenstein, J. M., Martin, M. A., and Freed, E. O. (1995) p6Gag is required for particle production from full-length human immunodeficiency virus type 1 molecular clones expressing protease. J. Virol. 69, 6810-6818.
3. Freed, E. O. (2002) Viral late domains. J. Virol. 76, 4679-4687.
4. Wilkinson, T. A., Tellinghuisen, T. L., Kuhn, R. J., and Post, C. B. (2005) Association of sindbis virus capsid protein with phospholipid membranes and the E2 glycoprotein: Implications for alphavirus assembly. Biochemistry 44, 2800-2810.
5. Usami, Y., Popov, S., and Göttlinger, H. G. (2007) Potent rescue of human immunodeficiency virus type 1 late domain mutants by ALIX/AIP1 depends on its CHMP4 binding site. J. Virol. 81, 6614- 6622.
6. Martin-Serrano, J., and Bieniasz, P. D. (2003) A bipartite latebudding domain in human immunodeficiency virus type 1. J. Virol. 77, 12373-12377.
7. Zhu, H., Jian, H., and Zhao, L. J. (2004) Identification of the 15FRFG domain in HIV-1 Gag p6 essential for Vpr packaging into the virion. Retrovirology 21, 1:26.
8. Barbara, M., Tilo, P., and Hans-Georg, K. (2002) The Late-Domain- Containing Protein p6 Is the Predominant Phosphoprotein of Human Immunodeficiency Virus Type 1 Particles. J. Virol. 76, 1015-1020.
9. Ott, D. E., Chertova, E. N., Busch, L. K., Coren, L. V., Gagliardi, T. D., and Johnson, D. G. (1999) Mutational Analysis of the Hydrophobic Tail of the Human Immunodeficiency Virus Type 1 p6Gag Protein Produces a Mutant That Fails To Package Its Envelope Protein. J. Virol. 73, 19-24.
10. Siddhartha, A. K., Zhao, Z., Clark, P. K., Tarasov, S., Alexandratos, J. N., Campbell, S. J., Kvaratskhelia, M., Lebowitz, J., and Rein, A. (2007) Interactions between HIV-1 Gag molecules in solution: An inositol phosphate-mediated switch. J. Mol. Biol. 365, 799- 811.
11. Strack, B., Calistri, A., Craig, S., Popova, E., and Göttlinger, H. G. (2003) AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 114, 689-699.
12. Rouzic, E. L., and Benichou, S. (2005) The Vpr protein from HIV- 1: Distinct roles along the viral life cycle. Retrovirology 22, 2-11.
13. Freed, E. O. (2001) HIV-1 replication. Somatic Cell Mol. Genet. 26, 13-33.
14. Mairea, M., Champeila, P., and Møller, J. V. (2000) Interaction of membrane proteins and lipids with solubilizing detergents. Biochim. Biophys. Acta 1508, 86-111.
15. Schievano, E., Calisti, T., Menegazzo, I., Battistutta, R., Peggion, E., Mammi, S., Palú, G., and Loregian, A. (2004) pH-Dependent conformational changes and topology of a herpesvirus translocating peptide in a membrane-mimetic environment. Biochemistry 43, 9343-9351.
16. Ruan, K. H., Li, D., Ji, J., Lin, Y. Z., and Gao, X. (1998) Structural characterization and topology of the second potential membrane anchor region in the thromboxane A2 synthase amino-terminal domain. Biochemistry 37, 822-830.
17. Li, Y., Han, X., Bushweller, J. H., Cafiso, D. S., and Tamm, L. K. (2005) Membrane structures of the hemifusion-inducing fusion peptide mutant G1S and the fusion-blocking mutant G1V of influenza virus hemagglutinin suggest a mechanism for pore opening in membrane fusion. J. Virol. 79, 12065-12076.
18. Hwang, P. M., Choy, W. Y., Lo, E. I., Chen, L., Forman-Kay, J. D., Raetz, C. R., Prive', G. G., Bishop, R. E., and Kay, L. E. (2002) Solution structure and dynamics of the outer membrane enzyme PagP by NMR. Proc. Natl. Acad. Sci. U.S.A. 99, 13560- 13565.
19. Wagner, G., Kumar, A., and Wuthrich, K. (1981) Systematic application of two-dimensional 1H nuclear-magnetic-resonance techniques for studies of proteins. 2. Combined use of correlated spectroscopy and nuclear Overhauser spectroscopy for sequential assignments of backbone resonances and elucidation of polypeptide secondary structures. Eur. J. Biochem. 114, 375-384.
20. Wuthrich, K., Wider, G., Wagner, G., and Braun, W. (1982) Sequential resonance assignments as a basis for determination of spatial protein structures by high resolution proton nuclear magnetic resonance. J. Mol. Biol. 155, 311-319.
21. Wagner, G., and Wüthrich, K. (1982) Sequential resonance assignments in protein 1H nuclear magnetic resonance spectra. Basic pancreatic trypsin inhibitor. J. Mol. Biol. 155, 347-366.
22. Wuthrich, K. (1986) NMR of Proteins and Nucleic Acids, Wiley, New York.
23. Piotto, M., Daudek, V., and Sklenar, V. (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR 2, 661-665.
24. Braunschweiler, L., and Ernst, R. R. (1983) Coherence Transfer by Isotropic Mixing: Application to Proton Correlation Spectroscopy. J. Magn. Reson. 53, 521-528.
25. Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., and Pedersen, L. G. (1995) A smooth particle mesh Ewald method. J. Chem. Phys. 103, 8577-8593.
26. Cheng, Y., LeGall, T., Oldfield, C. J., Mueller, J. P., Van, Y. Y., Romero, P., Cortese, M. S., Uversky, V. N., and Dunker, A. K. (2006) Rational drug design via intrinsically disordered protein. Trends Biotechnol. 24, 435-442.
27. Dunker, A. K., Lawson, J. D., Brown, C. J., Williams, R. M., Romero, P., Oh, J. S., Oldfield, C. J., Campen, A. M., Ratliff, C. M., Hipps, K. W., Ausio, J., Nissen, M. S., Reeves, R., Kang, C., Kissinger, C. R., Bailey, R. W., Griswold, M. D., Chiu, W., Garner, E. C., and Obradovic, Z. (2001) Intrinsically disordered protein. J. Mol. Graphics Modell. 19, 26-59.
28. Seelig, J. (2004) Thermodynamics of lipid-peptide interactions. Biochim. Biophys. Acta 1666, 40-50.
29. Klajnert, B., Janiszewska, J., Urbanczyk-Lipkowska, J., Bryszewska, Z., and Epand, R. M. (2006) DSC studies on interactions between low molecular mass peptide dendrimers and model lipid membranes. Int. J. Pharm. 327, 145-152.
30. Goddard, T. D., and Kneller, D. G. (2003) Sparky, University of California, San Francisco.
31. Fogh, R., Ionides, J., Ulrich, E., Boucher, W., Vranken, W., Linge, J. P., Habeck, M., Rieping, W., Bhat, T. N., Westbrook, J., Henrick, K., Gilliland, G., Berman, H., Thornton, J., Nilges, M., Markley, J., and Laue, E. (2002) The CCPN project: An interim report on a data model for the NMR community. Nat. Struct. Biol. 9, 416- 418.
32. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486.
33. Clore, G. M., and Gronenborn, A. M. (1994) Multidimensional heteronuclear nuclear magnetic resonance of proteins. Methods Enzymol. 239, 349-363.
34. Brooks, B. R., Bruccoleri, R. E., Olafson, B. D., States, D. J., Swaminathan, S., and Karplus, M. (1983) CHARMM: A program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4, 187-217.
35. Gumbart, J., Wang, Y., Aksimentiev, A., Tajkhorshid, E., and Schulten, K. (2005) Molecular dynamics simulations of proteins in lipid bilayers. Curr. Opin. Struct. Biol. 15, 423-431.
36. Fossen, T., Wray, V., Bruns, K., Rachmat, J., Henklein, P., Tessmer, U., Maczurek, A., Klinger, P., and Schubert, U. (2005) Solution structure of the human immunodeficiency virus type 1 p6 protein. J. Biol. Chem. 280, 42515-42527.
37. Dyson, H. J., and Wright, P. E. (2001) Nuclear magnetic resonance methods for elucidation of structure and dynamics in disordered states. Methods Enzymol. 339, 258-270.
38. Lu, Y. L., Bennett, R. P., Wills, J. W., Gorelick, R., and Ratner, L. (1995) A leucine triplet repeat sequence (LXX)4 in p6gag is important for Vpr incorporation into human immunodeficiency virus type 1 particles. J. Virol. 69, 6873-6879.
39. Munshi, U. M., Kim, J., Nagashima, K., Hurley, J. H., and Freed, E. O. (2007) An Alix fragment potently inhibits HIV-1 budding: Characterization of binding to retroviral YPXL late domains. J. Biol. Chem. 282, 3847-3855.
40. Linge, J. P., Habeck, M., Rieping, W., and Nilges, M. (2003) ARIA: Automated NOE assignment and NMR structure calculation. Bioinformatics 19, 315-316.
41. Klauda, J. B., Brooks, B. R., MacKerell, A. D., Venable, R. M., and Pastor, R. W. (2005) An ab Initio Study on the Torsional Surface of Alkanes and Its Effect on Molecular Simulations of Alkanes and a DPPC Bilayer. J. Phys. Chem. B 109, 5300-5531.
42. Gunasekaran, K., Tsai, C., Kumar, S., Zanuy, D., and Nussinov, R. (2003) Extended disordered proteins: Targeting function with less scaffold. Trends Biochem. Sci. 28, 81-85.
43. Roccatano, D., Colombo, G., Fioroni, M., and Mark, A. E. (2002) Mechanism by which 2,2,2-trifluoroethanol/water mixtures stabilize secondary-structure formation in peptides: A molecular dynamics study. Proc. Natl. Acad. Sci. U.S.A. 99, 12179-12184.
44. Lee, S., Joshi, A., Nagashima, K., Freed, E. O., and Hurley, J. H. (2007) Structural basis for viral late-domain binding to Alix. Nat. Struct. Mol. Biol. 14, 194-199.
45. Votteler, J., Studtrucker, N., Sörgel, S., Münch, J., Rücker, E., Kirchhoff, F., Schick, B., Henklein, P., Fossen, T., Bruns, K., Sharma, A., Wray, V., and Schubert, U. (2007) Proline 35 of Human Immunodeficiency Virus Type 1 (HIV-1) Vpr Regulates the Integrity of the N-Terminal Helix and the Incorporation of Vpr into Virus Particles and Supports the Replication of R5-Tropic HIV-1 in Human Lymphoid Tissue Ex Vivo. J. Virol. 81 (17), 9572-9576.
46. Engler, A., Stangler, T., and Willbold, D. (2003) Solution structure of human immunodeficiency virus type 1 Vpr(13-33) peptide in micelles. Eur. J. Biochem. 268, 389-395.
47. Schüler, W., Wecker, K., Rocquigny, H., Baudat, Y., Sire, J., and Roques, B. P. (1999) NMR structure of the (52-96) C-terminal domain of the HIV-1 regulatory protein Vpr: Molecular insights into its biological functions. J. Mol. Biol. 285, 2105-2117.
48. Ebbets-Reed, D., Scarlata, S., and Carter, C. A. (1996) The major homology region of the HIV-1 gag precursor influences membrane affinity. Biochemistry 35, 14268-14275.
49. Bouamr, F., Scarlata, S., and Carter, C. A. (2003) Role of myristylation in HIV-1 Gag assembly. Biochemistry 42, 6408-6417.
50. Ott, D. E. (2008) Cellular proteins detected in HIV-1. Rev. Med. Virol. 18, 159-175.
51. Stys, D., Blaha, I., and Strop, P. (1993) Structural and functional studies on the p6 protein from HIV-1 gag open reading frame. Biochim. Biophys. Acta 1182, 157-161.
52. Morellet, N., Bouaziz, S., Petitjean, P., and Roques, B. P. (2003) NMR structure of the HIV-1 regulatory protein VPR. J. Mol. Biol. 327, 215-227.