HIV-1 Gag extension: Conformational changes require simultaneous interaction with membrane and nucleic acid

Journal of Molecular Biology

Volumn 406, Issue 2, 2011, Pages 205-214

  Datta, Siddhartha A K ^a   Heinrich, Frank ^b   Raghunandan, Sindhu ^c   Krueger, Susan ^c   Curtis, Joseph E ^c   Rein, Alan ^a   Nanda, Hirsh ^c  

^a NATIONAL CANCER INSTITUTE   (United States)

^b CARNEGIE MELLON UNIVERSITY   (United States)

^c NATIONAL INSTITUTE OF STANDARDS AND TECHNOLOGY   (United States)

Author keywords

disordered proteins; neutron reflectivity; retroviral assembly; SANS; tethered membranes

Indexed keywords

GAG PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CRYOELECTRON MICROSCOPY; HUMAN IMMUNODEFICIENCY VIRUS 1; INTERACTIONS WITH NUCLEIC ACID; MOLECULAR INTERACTION; MOLECULAR MODEL; NEUTRON SCATTERING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; SMALL ANGLE SCATTERING; VIRION; VIRUS ASSEMBLY; VIRUS PARTICLE;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 79251596756     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.11.051     Document Type: Article

References (35)

1. Swanstrom R., and Wills J.W. Synthesis, assembly, and processing of viral proteins J.M. Coffin, S.H. Hughes, H.E. Varmus, Retroviruses 1997 Cold Spring Harbor Laboratory Press Plainview, NY 263 334
2. Ganser-Pornillos B.K., Yeager M., and Sundquist W.I. The structural biology of HIV assembly Curr. Opin. Struct. Biol. 18 2008 203 217
3. Zhou W.J., Parent L.J., Wills J.W., and Resh M.D. Identification of a membrane binding domain within the amino-terminal region of human immunodeficiency virus type 1 Gag protein which interacts with acidic phospholipids J. Virol. 68 1994 2556 2569
4. Fuller S.D., Wilk T., Gowen B.E., Kräusslich H.G., and Vogt V.M. Cryo-electron microscopy reveals ordered domains in the immature HIV-1 particle Curr. Biol. 7 1997 729 738
5. Campbell S., and Rein A. In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain J. Virol. 73 1999 2270 2279
6. Datta S.A.K., Zhao Z., Clark P.K., Tarasov S., Alexandratos J.N., and Campbell S.J. Interactions between HIV-1 Gag molecules in solution: an inositol phosphate-mediated switch J. Mol. Biol. 365 2007 799 811
7. Datta S.A.K., Curtis J., Ratcliff W., Clark P., Crist R., and Lebowitz J. Conformation of the HIV-1 Gag protein in solution J. Mol. Biol. 365 2007 812 824
8. Byeon I.J., Meng X., Jung J., Zhao G., Yang R., and Ahn J. Structural convergence between cryo-EM and NMR reveals intersubunit interactions critical for HIV-1 capsid function Cell 139 2009 780 790
9. Campbell S., Fisher R.J., Towler E.M., Fox S., Issaq H.J., and Wolfe T. Modulation of HIV-like particle assembly in vitro by inositol phosphates Proc. Natl Acad. Sci. USA 98 2001 10875 10979
10. Tang C., Ndassa Y., and Summers M.F. Structure of the N-terminal 283-residue fragment of the immature HIV-1 Gag polyprotein Nat. Struct. Biol. 9 2002 537 543
11. Gamble T.R., Yoo S.H., Vajdos F.F., von Schwedler U.K., Worthylake D.K., and Wang H. Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein Science 278 1997 849 853
12. De Guzman R.N., Wu Z.R., Stalling C.C., Pappalardo L., Borer P.N., and Summers M.F. Structure of the HIV-1 nucleocapsid protein bound to the SL3 Psi-RNA recognition element Science 279 1998 384 388
13. Lee B.M., De Guzman R.N., Turner B.G., Tjandra N., and Summers M.F. Dynamical behavior of the HIV-1 nucleocapsid protein J. Mol. Biol. 279 1998 633 649
14. Newman J.L., Butcher E.W., Patel D.T., Mikhaylenko Y., and Summers M.F. Flexibility in the P2 domain of the HIV-1 Gag polyprotein Protein Sci. 13 2004 2101 2107
15. Stys D., Blaha I., and Strop P. Structural and functional studies in vitro on the p6 protein from the HIV-1 gag open reading frame Biochim. Biophys. Acta 1182 1993 157 161
16. Curtis J.E., Raghunandan S., Nanda H., and Krueger S. SASSIE: A program to study intrinsically disordered biological molecules and macromolecular ensembles using experimental scattering restraints 2010 http://www.smallangles. net/sassie/SASSIE/SASSIE-HOME.html
17. Campbell S., and Vogt V.M. In vitro assembly of virus-like particles with Rous sarcoma virus Gag deletion mutants: identification of the p10 domain as a morphological determinant in the formation of spherical particles J. Virol. 71 1997 4425 4435
18. Yu F., Joshi S.M., Ma Y.M., Kingston R.L., Simon M.N., and Vogt V.M. Characterization of Rous sarcoma virus Gag particles assembled in vitro J. Virol. 75 2001 2753 2764
19. Fisher R.J., Fivash M.J., Stephen A.G., Hagan N.A., Shenoy S.R., and Medaglia M.V. Complex interactions of HIV-1 nucleocapsid protein with oligonucleotides Nucleic Acids Res. 34 2006 472 484
20. McGillivray D.J., Valincius G., Vanderah D.J., FeboAyala W., Woodward J.T., and Heinrich F. Molecular-scale structural and functional characterization of sparsely tethered bilayer lipid membranes Biointerphases 2 2007 21 33
21. Cornell B.A., Braach-Maksvytis V.L.B., King L.G., Osman P.D.J., Raguse B., Wieczorek L., and Pace R.J. A biosensor that uses ion-channel switches Nature 387 1997 580 583
22. Shenoy S., Moldovan R., Fitzpatrick J., Vanderah D.J., Deserno M., and Loesche M. In-plane homogeneity and lipid dynamics in tethered bilayer lipid membranes (tBLMs) Soft Matter 6 2010 1263 1274
23. Parratt L.G. Surface studies of solids by total reflection of x-rays Phys. Rev. 95 1954 359 369
24. Heinrich F., Ng T., Vanderah D.J., Shekhar P., Mihailescu M., Nanda H., and Lösche M. A new lipid anchor for sparsely-tethered bilayer lipid membranes Langmuir 25 2009 4219 4229
25. Kienzle, P. A., Doucet, M., McGillivray, D. J., O'Donovan, K. V., Berk, N. F. & Majkrzak, C. F. (2000). ga-refl, a program for simultaneous fitting of X ray and neutron polarized reflectometry data; http://www.ncnr.nist.gov/ reflpak.
26. Brügger B., Glass B., Haberkant P., Leibrecht I., Wieland F.T., and Kräusslich H.G. The HIV lipidome: a raft with an unusual composition Proc. Natl Acad. Sci. USA 103 2006 2641 2646
27. Nanda H., Datta S.A.K., Heinrich F., Lösche M., Rein A., Krueger S., and Curtis J.E. Electrostatic interactions and binding orientation of HIV-1 matrix, studied by neutron reflectivity Biophys. J. 99 2010 2516 2524
28. Purohit P., Dupont S., Stevenson M., and Green M.R. Sequence-specific interaction between HIV-1 matrix protein and viral genomic RNA revealed by in vitro genetic selection RNA 7 2001 576 584
29. Hearps A., Wagstaff K.M., Piller S.C., and Jans D. The N-terminal basic domain of the HIV-1 matrix protein does not contain a conventional nuclear localization sequence but is required for DNA binding and protein self-association Biochemistry 47 2008 2199 2210
30. Shkriabai N., Datta S.A.K., Zhao Z.J., Hess S., Rein A., and Kvaratskhelia M. Interactions of HIV-1 Gag with assembly cofactors Biochemistry 45 2006 4077 4083
31. Alfadhli A., Still A., and Barklis E. Analysis of human immunodeficiency virus type 1 matrix binding to membranes and nucleic acids J. Virol. 83 2009 12196 12203
32. Lochrie M.A., Waugh S., Pratt D.G., Clever J., Parslow T.G., and Polisky B. In vitro selection of RNAs that bind to the human immunodeficiency virus type-1 gag polyprotein Nucleic Acids Res. 25 1997 2902 2910
33. Chukkapalli V., Oh S.J., and Ono A. Opposing mechanisms involving RNA and lipids regulate HIV-1 Gag membrane binding through the highly basic region of the matrix domain Proc. Natl Acad. Sci. USA 107 2010 1600 1605
34. Jones C.P., Datta S.A.K., Rein A., Rouzina I., and Musier-Forsyth K. Matrix domain modulates HIV-1 Gag's nucleic acid chaperone activity via inositol phosphate binding J. Virol. 2010 In press. doi:10.1128/JVI.01809-10
35. Jouvenet N., Simon S.M., and Bieniasz P.D. Imaging the interaction of HIV-1 genomes and Gag during assembly of individual viral particles Proc. Natl Acad. Sci. USA 106 2009 19114 19119