Interrelationship between cytoplasmic retroviral Gag concentration and Gag-membrane association

Journal of Molecular Biology

Volumn 426, Issue 7, 2014, Pages 1611-1624

  Fogarty, Keir H ^a,b,c   Berk, Serkan ^a,c   Grigsby, Iwen F ^a,b   Chen, Yan ^a,c   Mansky, Louis M ^a,b   Mueller, Joachim D ^a,c  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c University of Minnesota   (United States)

Author keywords

assembly; fluorescence; membrane; oligomerization; retrovirus

Indexed keywords

CYTOPLASM PROTEIN; GAG PROTEIN; MEMBRANE PROTEIN;

ARTICLE; CELL MEMBRANE; FLUORESCENCE; FLUORESCENCE SPECTROSCOPY; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN T CELL LEUKEMIA VIRUS 1; ILLUMINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RETROVIRUS; TOTAL INTERNAL REFLECTION FLUORESCENCE; VIRUS ASSEMBLY; VIRUS PARTICLE; CYTOPLASM; HUMAN T-LYMPHOTROPIC VIRUS 1; OLIGOMERIZATION; PROTEIN TARGETING;

HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN T-LYMPHOTROPIC VIRUS 1;

ASSEMBLY; FLUORESCENCE; MEMBRANE; OLIGOMERIZATION; RETROVIRUS;

CELL MEMBRANE; CYTOPLASM; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GENE PRODUCTS, GAG; HUMAN T-LYMPHOTROPIC VIRUS 1; RETROVIRIDAE;

EID: 84895925747     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.11.025     Document Type: Article

References (75)

1. R. Swanstrom, and J.W. Wills Synthesis, assembly, and processing of viral proteins J.M. Coffin, S.H. Hughes, H.E. Varmus, Retroviruses 1997 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY 263 334
2. J.W. Wills, and R.C. Craven Form, function, and use of retroviral Gag proteins AIDS 5 1991 639 654
3. D. Gheysen, E. Jacobs, F. Deforesta, C. Thiriart, M. Francotte, and D. Thines et al. Assembly and release of HIV-1 precursor Pr55gag virus-like particles from recombinant baculovirus infected insect cells Cell 59 1989 103 112
4. E. Hamard-Peron, and D. Muriaux Retroviral matrix and lipids, the intimate interaction Retrovirology 8 2011 15
5. A. Ono, D. Demirov, and E.O. Freed Relationship between human immunodeficiency virus type 1 Gag multimerization and membrane binding J Virol 74 2000 5142 5150
6. A. Ono, S.D. Ablan, S.J. Lockett, K. Nagashima, and E.O. Freed Phosphatidylinositol (4,5) bisphosphate regulates HIV-1 gag targeting to the plasma membrane Proc Natl Acad Sci USA 101 2004 14889 14894
7. J.S. Saad, J. Miller, J. Tai, A. Kim, R.H. Ghanam, and M.F. Summers Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly Proc Natl Acad Sci USA 103 2006 11364 11369
8. M. Bryant, and L. Ratner Myristoylation-dependent replication and assembly of human immunodeficiency virus 1 Proc Natl Acad Sci USA 87 1990 523 527
9. D. Ako-Adjei, M.C. Johnson, and V.M. Vogt The retroviral capsid domain dictates virion size, morphology, and coassembly of Gag into virus-like particles J Virol 79 2005 13463 13472
10. B.K. Ganser-Pornillos, M. Yeager, and W.I. Sundquist The structural biology of HIV assembly Curr Opin Struct Biol 18 2008 203 217
11. J.A.G. Briggs, J.D. Riches, B. Glass, V. Bartonova, G. Zanetti, and H.G. Krausslich Structure and assembly of immature HIV Proc Natl Acad Sci USA 106 2009 11090 11095
12. M.T. Burniston, A. Cimarelli, J. Colgan, S.P. Curtis, and J. Luban Human immunodeficiency virus type 1 Gag polyprotein multimerization requires the nucleocapsid domain and RNA and is promoted by the capsid-dimer interface and the basic region of matrix protein J Virol 73 1999 8527 8540
13. A. Cimarelli, S. Sandin, S. Hoglund, and J. Luban Basic residues in human immunodeficiency virus type 1 nucleocapsid promote virion assembly via interaction with RNA J Virol 74 2000 3046 3057
14. D. Muriaux, J. Mirro, D. Harvin, and A. Rein RNA is a structural element in retrovirus particles Proc Natl Acad Sci USA 98 2001 5246 5251
15. A.M. Christensen, M.A. Massiah, B.G. Turner, W.I. Sundquist, and M.F. Summers Three-dimensional structure of the HTLV-II matrix protein and comparative analysis of matrix proteins from the different classes of pathogenic human retroviruses J Mol Biol 264 1996 1117 1131
16. P.S. Murray, Z.H. Li, J.Y. Wang, C.L. Tang, B. Honig, and D. Murray Retroviral matrix domains share electrostatic homology: models for membrane binding function throughout the viral life cycle Structure 13 2005 1521 1531
17. O.W. Lindwasser, and M.D. Resh Multimerization of human immunodeficiency virus type 1 gag promotes its localization to barges, raft-like membrane microdomains J Virol 75 2001 7913 7924
18. S. Sandefur, V. Varthakavi, and P. Spearman The I domain is required for efficient plasma membrane binding of human immunodeficiency virus type 1 Pr55(Gag) J Virol 72 1998 2723 2732
19. D. Perez-Caballero, T. Hatziioannou, J. Martin-Serrano, and P.D. Bieniasz Human immunodeficiency virus type 1 matrix inhibits and confers cooperativity on Gag precursor-membrane interactions J Virol 78 2004 9560 9563
20. K.H. Fogarty, Y. Chen, I.F. Grigsby, P.J. Macdonald, E.M. Smith, and J.L. Johnson et al. Characterization of cytoplasmic Gag-Gag interactions by dual-color z-scan fluorescence fluctuation spectroscopy Biophys J 100 2011 1587 1595
21. S.B. Kutluay, and P.D. Bieniasz Analysis of the initiating events in HIV-1 particle assembly and genome packaging PLoS Pathog 6 2010 e1001200
22. W. Hubner, P. Chen, A. Del Portillo, Y. Liu, R.E. Gordon, and B.K. Chen Sequence of human immunodeficiency virus type 1 (HIV-1) gag localization and oligomerization monitored with live confocal imaging of a replication-competent, fluorescently tagged EIV-1 J Virol 81 2007 12596 12607
23. F. Rayne, F. Bouamr, J. Lalanne, and R.Z. Mamoun The NH2-terminal domain of the human T-cell leukemia virus type 1 capsid protein is involved in particle formation J Virol 75 2001 5277 5287
24. F. Rayne, A.V. Kajava, J. Lalanne, and R.Z. Mamoun In vivo homodimerisation of HTLV-1 Gag and MA gives clues to the retroviral capsid and TM envelope protein arrangement J Mol Biol 343 2004 903 916
25. J. Inlora, V. Chukkapalli, D. Derse, and A. Ono Gag localization and virus-like particle release mediated by the matrix domain of human T-lymphotropic virus type 1 Gag are less dependent on phosphatidylinositol-(4,5) -bisphosphate than those mediated by the matrix domain of HIV-1 Gag J Virol 85 2011 3802 3810
26. V. Chukkapalli, S.J. Oh, and A. Ono 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
27. A. Alfadhli, A. Still, and E. Barklis Analysis of human immunodeficiency virus type 1 matrix binding to membranes and nucleic acids J Virol 83 2009 12196 12203
28. A. Alfadhli, H. McNett, S. Tsagli, H.P. Bachinger, D.H. Peyton, and E. Barklis HIV-1 matrix protein binding to RNA J Mol Biol 410 2011 653 666
29. N. Jouvenet, S.J.D. Neil, C. Bess, M.C. Johnson, C.A. Virgen, and S.M. Simon et al. Plasma membrane is the site of productive HIV-1 particle assembly PLoS Biol 4 2006 2296 2310
30. N. Jouvenet, P.D. Bieniasz, and S.M. Simon Imaging the biogenesis of individual HIV-1 virions in live cells Nature 454 2008 236 240
31. N. Jouvenet, S.M. Simon, and P.D. Bieniasz Imaging the interaction of HIV-1 genomes and Gag during assembly of individual viral particles Proc Natl Acad Sci USA 106 2009 19114 19119
32. N. Jouvenet, M. Zhadina, P.D. Bieniasz, and S.M. Simon Dynamics of ESCRT protein recruitment during retroviral assembly Nat Cell Biol 13 2011 394 401
33. S. Ivanchenko, W.J. Godinez, M. Lampe, H.G. Krausslich, R. Eils, and K. Rohr et al. Dynamics of HIV-1 assembly and release PLoS Pathog 5 2009 e1000652
34. V. Baumgartel, S. Ivanchenko, A. Dupont, M. Sergeev, P.W. Wiseman, and H.-G. Krausslich et al. Live-cell visualization of dynamics of HIV budding site interactions with an ESCRT component Nat Cell Biol 13 2011 469 474
35. M.D. Resh Intracellular trafficking of HIV-1 Gag: how Gag interacts with cell membranes and makes viral particles AIDS Rev 7 2005 84 91
36. Y. Chen, J.D. Muller, Q.Q. Ruan, and E. Gratton Molecular brightness characterization of EGFP in vivo by fluorescence fluctuation spectroscopy Biophys J 82 2002 133 144
37. Y. Chen, L.N. Wei, and J.D. Muller Probing protein oligomerization in living cells with fluorescence fluctuation spectroscopy Proc Natl Acad Sci USA 100 2003 15492 15497
38. K.M. Berland, P.T.C. So, and E. Gratton Two-photon fluorescence correlation spectroscopy: method and application to the intracellular environment Biophys J 68 1995 694 701
39. A.K. Dalton, D. Ako-Adjei, P.S. Murray, D. Murray, and V.M. Vogt Electrostatic interactions drive membrane association of the human immunodeficiency virus type 1 Gag MA domain J Virol 81 2007 6434 6445
40. M.A. Massiah, M.R. Starich, C. Paschall, M.F. Summers, A.M. Christensen, and W.I. Sundquist Three-dimensional structure of the human immunodeficiency virus type 1 matrix protein J Mol Biol 244 1994 198 223
41. D. Mazurov, G. Heidecker, and D. Derse HTLV-1 Gag protein associates with CD82 tetraspanin microdomains at the plasma membrane Virology 346 2006 194 204
42. D. Mazurov, G. Heidecker, and D. Derse The inner loop of tetraspanins CD82 and CD81 mediates interactions with human T cell lymphotrophic virus type 1 Gag protein J Biol Chem 282 2007 3896 3903
43. S.A.K. Datta, Z. Zhao, P.K. Clark, S. Tarasov, J.N. Alexandratos, and S.J. Campbell et al. Interactions between HIV-1 Gag molecules in solution: an inositol phosphate-mediated switch J Mol Biol 365 2007 799 811
44. H.G. Gottlinger, J.G. Sodroski, and W.A. Haseltine Role of capsid precursor processing and myristoylation in morphogenesis and infectivity of human immunodeficiency virus type-1 Proc Natl Acad Sci USA 86 1989 5781 5785
45. I. Le Blanc, V. Blot, I. Bouchaert, J. Salamero, B. Goud, and A.R. Rosenberg et al. Intracellular distribution of human T-cell leukemia virus type 1 Gag proteins is independent of interaction with intracellular membranes J Virol 76 2002 905 911
46. D.R. Larson, M.C. Johnson, W.W. Webb, and V.M. Vogt Visualization of retrovirus budding with correlated light and electron microscopy Proc Natl Acad Sci USA 102 2005 15453 15458
47. O.W. Lindwasser, and M.D. Resh Human immunodeficiency virus type 1 Gag contains a dileucine-like motif that regulates association with multivesicular bodies J Virol 78 2004 6013 6023
48. Y. Morikawa, S. Hinata, H. Tomoda, T. Goto, M. Nakai, and C. Aizawa et al. Complete inhibition of human immunodeficiency virus gag myristoylation is necessary for inhibition of particle budding J Biol Chem 271 1996 2868 2873
49. J. Park, and C.D. Morrow The nonmyristylated Pr160gag-Pol polyprotein of human immunodeficiency virus type 1 interacts with Pr55gag and is incorporated into virus-like particles J Virol 66 1992 6304 6313
50. C. Tang, E. Loeliger, P. Luncsford, I. Kinde, D. Beckett, and M.F. Summers Entropic switch regulates myristate exposure in the HIV-1 matrix protein Proc Natl Acad Sci USA 101 2004 517 522
51. I.F. Grigsby, W. Zhang, J.L. Johnson, K.H. Fogarty, Y. Chen, and J.M. Rawson et al. Biophysical analysis of HTLV-1 particles reveals novel insights into particle morphology and Gag stoichiometry Retrovirology 7 2010 75
52. L.A. Carlson, J.A.G. Briggs, B. Glass, J.D. Riches, M.N. Simon, and M.C. Johnson et al. Three-dimensional analysis of budding sites and released virus suggests a revised model for HIV-1 morphogenesis Cell Host Microbe 4 2008 592 599
53. L.A. Carlson, A. de Marco, H. Oberwinkler, A. Habermann, J.A. Briggs, and H.G. Krausslich et al. Cryo electron tomography of native HIV-1 budding sites PLoS Pathog 6 2010 e1001173
54. A. Ono, and E.O. Freed Plasma membrane rafts play a critical role in HIV-1 assembly and release Proc Natl Acad Sci USA 98 2001 13925 13930
55. A. Ono, and E.O. Freed Role of lipid rafts in virus replication Virus structure and assembly 64 2005 Elsevier Academic Press Inc. San Diego, CA 311 358
56. A.A. Waheed, and E.O. Freed Lipids and membrane microdomains in HIV-1 replication Virus Res 143 2009 162 176
57. F. Bouamr, L. Garnier, F. Rayne, A. Verna, N. Rebeyrotte, and M. Cerutti et al. Differential budding efficiencies of human T-cell leukemia virus type I (HTLV-I) Gag and Gag-Pro polyproteins from insect and mammalian cells Virology 278 2000 597 609
58. D.F. Qualley, K.M. Stewart-Maynard, F. Wang, M. Mitra, R.J. Gorelick, and I. Rouzina et al. C-terminal domain modulates the nucleic acid chaperone activity of human T-cell leukemia virus type 1 nucleocapsid protein via an electrostatic mechanism J Biol Chem 285 2010 295 307
59. D.C. Johnson, and M.T. Huber Directed egress of animal viruses promotes cell-to-cell spread J Virol 76 2002 1 8
60. D.M. Phillips The role of cell-to-cell transmission in HIV-infection AIDS 8 1994 719 731
61. M. Yoshida Discovery of HTLV-1, the first human retrovirus, its unique regulatory mechanisms, and insights into pathogenesis Oncogene 24 2005 5931 5937
62. D. Mazurov, A. Ilinskaya, G. Heidecker, P. Lloyd, and D. Derse Quantitative comparison of HTLV-1 and HIV-1 cell-to-cell infection with new replication dependent vectors PLoS Pathog 6 2010 e1000788
63. C.Z. Giam, and K.T. Jeang HTLV-1 Tax and adult T-cell leukemia Front Biosci 12 2007 1496 1507
64. H.H. Baydoun, M. Bellon, and C. Nicot HTLV-1 yin and yang: Rex and p30 master regulators of viral mRNA trafficking AIDS Rev 10 2008 195 204
65. L.M. Mansky HIV mutagenesis and the evolution of antiretroviral drug resistance Drug Resist Updates 5 2002 219 223
66. R.X. Chen, M.E. Quinones-Mateu, and L.M. Mansky Drug resistance, virus fitness and HIV-1 mutagenesis Curr Pharm Des 10 2004 4065 4070
67. K.H. Fogarty, W. Zhang, I.F. Grigsby, J.L. Johnson, Y. Chen, and J.D. Mueller et al. New insights into HTLV-1 particle structure, assembly, and Gag-Gag interactions in living cells Viruses 3 2011 770 793
68. V. Chukkapalli, and A. Ono Molecular determinants that regulate plasma membrane association of HIV-1 Gag J Mol Biol 410 2011 512 524
69. W.T. Gao, A. Rzewski, H.J. Sun, P.D. Robbins, and A. Gambotto UpGene: application of a Web-based DNA codon optimization algorithm Biotechnol Prog 20 2004 443 448
70. M. Kozak Compilation and analysis of sequences upstream from the translational start site in eukaryotic messenger-RNAs Nucleic Acids Res 12 1984 857 872
71. M. Kozak An analysis of 5′-noncoding sequences from 699 vertebrate messenger-RNAs Nucleic Acids Res 15 1987 8125 8148
72. A. Derdowski, L.M. Ding, and P. Spearman A novel fluorescence resonance energy transfer assay demonstrates that the human immunodeficiency virus type 1 Pr55(Gag)I domain mediates Gag-Gag interactions J Virol 78 2004 1230 1242
73. Y. Chen, L.N. Wei, and J.D. Muller Unraveling protein-protein interactions in living cells with fluorescence fluctuation brightness analysis Biophys J 88 2005 4366 4377
74. P.J. Macdonald, Y. Chen, Y. Chen, X. Wang, and J.D. Mueller Brightness analysis by z-scan fluorescence fluctuation spectroscopy for the study of protein interactions within living cells Biophys J 99 2010 979 988
75. D. Axelrod, and D. Axelrod Total internal reflection fluorescence microscopy Biophysical Tools for Biologists, Vol 2 Biophysical Tools for Biologists 89 2008 Elsevier Academic Press Inc. San Diego, CA 169 221