FIV Gag: Virus assembly and host-cell interactions

Veterinary Immunology and Immunopathology

Volumn 134, Issue 1-2, 2010, Pages 3-13

  Luttge, Benjamin G ^a   Freed, Eric O ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

ESCRT; FIV; Gag; HIV 1; Viral late domains; Virus cell interactions

Indexed keywords

GAG PROTEIN; RNA DIRECTED DNA POLYMERASE; TRIPARTITE MOTIF PROTEIN 5; VIRUS ENVELOPE PROTEIN;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; CYTOSKELETON; FELINE IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MEMBRANE BINDING; MOLECULAR MECHANICS; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REVIEW; STRUCTURAL HOMOLOGY; UBIQUITINATION; VIRAL GENE THERAPY; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS INFECTIVITY; VIRUS MORPHOLOGY; VIRUS NUCLEOCAPSID; VIRUS REPLICATION;

ANIMALS; CATS; FELINE ACQUIRED IMMUNODEFICIENCY SYNDROME; GENE PRODUCTS, GAG; HOST-PATHOGEN INTERACTIONS; IMMUNODEFICIENCY VIRUS, FELINE; VIRUS ASSEMBLY; VIRUS RELEASE;

FELINE IMMUNODEFICIENCY VIRUS; FELIS CATUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MIRIDAE; PRIMATES;

EID: 75749094701     PISSN: 01652427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetimm.2009.10.003     Document Type: Review

References (143)

1. Adamson C.S., and Freed E.O. Human immunodeficiency virus type 1 assembly, release, and maturation. Adv. Pharmacol. 55 (2007) 347-387
2. Adamson C.S., Salzwedel K., and Freed E.O. Inhibiting viral maturation as a novel HIV-1 therapeutic target. Expert Opin. Ther. Targets 13 8 (2009) 895-908
3. Amodeo P., Castiglione Morelli M.A., Ostuni A., Battistuzzi G., and Bavoso A. Structural features in EIAV NCp11: a lentivirus nucleocapsid protein with a short linker. Biochemistry 45 (2006) 5517-5526
4. Bieniasz P.D. Late budding domains and host proteins in enveloped virus release. Virology 344 (2006) 55-63
5. Brennan G., Kozyrev Y., and Hu S.L. TRIMCyp expression in Old World primates Macaca nemestrina and Macaca fascicularis. Proc. Natl. Acad. Sci. U.S.A. 105 9 (2008) 3569-3574
6. Bukrinskaya A.G., Brichacek B., Mann A., and Stevenson M. Establishment of a functional human immunodeficiency virus type 1 (HIV-1) reverse transcription complex involves the cytoskeleton. J. Exp. Med. 188 (1998) 2113-2125
7. Burkala E., and Poss M. Evolution of feline immunodeficiency virus Gag proteins. Virus Genes 35 (2007) 251-264
8. Burkhard M.J., and Dean G.A. Transmission and immunopathogenesis of FIV in cats as a model for HIV. Curr. HIV Res. 1 (2003) 15-29
9. Calistri A., Del Vecchio C., Salata C., Celestino M., Celegato M., Gottlinger H., Palu G., and Parolin C. Role of the feline immunodeficiency virus L-domain in the presence or absence of Gag processing: involvement of ubiquitin and Nedd4-2s ligase in viral egress. J. Cell. Physiol. 218 (2009) 175-182
10. 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
11. Campbell S., and Vogt V.M. Self-assembly in vitro of purified CA-NC proteins from Rous sarcoma virus and human immunodeficiency virus type 1. J. Virol. 69 (1995) 6487-6497
12. Celma C.C., Paladino M.G., González S.A., and Affranchino J.L. Importance of the short cytoplasmic domain of the feline immunodeficiency virus transmembrane glycoprotein for fusion activity and envelope glycoprotein incorporation into virions. Virology 366 (2007) 405-414
13. Chukkapalli V., Hogue I.B., Boyko V., Hu W.S., and Ono A. Interaction between the human immunodeficiency virus type 1 Gag matrix domain and phosphatidylinositol-(4,5)-bisphosphate is essential for efficient gag membrane binding. J. Virol. 82 (2008) 2405-2417
14. Chung H.Y., Morita E., von Schwedler U., Müller B., Krausslich H.G., and Sundquist W.I. NEDD4L overexpression rescues the release and infectivity of human immunodeficiency virus type 1 constructs lacking PTAP and YPXL late domains. J. Virol. 82 (2008) 4884-4897
15. Coats K.S. The feline immunodeficiency virus-infected cat: a model for lentivirus-induced placental immunopathology and reproductive failure (mini-review). Am. J. Reprod. Immunol. 54 (2005) 169-185
16. Coleman J.K., Pu R., Martin M., Sato E., and Yamamoto J.K. HIV-1 p24 vaccine protects cats against feline immunodeficiency virus infection. AIDS 19 (2005) 1457-1466
17. Dalton A.K., Ako-Adjei D., Murray P.S., Murray D., and Vogt V.M. Electrostatic interactions drive membrane association of the human immunodeficiency virus type 1 Gag MA domain. J. Virol. 81 (2007) 6434-6445
18. Davis M.R., Jiang J., Zhou J., Freed E.O., and Aiken C. A mutation in the human immunodeficiency virus type 1 Gag protein destabilizes the interaction of the envelope protein subunits gp120 and gp41. J. Virol. 80 (2006) 2405-2417
19. 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
20. Demirov D.G., and Freed E.O. Retrovirus budding. Virus Res. 106 (2004) 87-102
21. Demirov D.G., Ono A., Orenstein J.M., and Freed E.O. Overexpression of the N-terminal domain of TSG101 inhibits HIV-1 budding by blocking late domain function. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 955-960
22. Deneka M., Pelchen-Matthews A., Byland R., Ruiz-Mateos E., and Marsh M. In macrophages, HIV-1 assembles into an intracellular plasma membrane domain containing the tetraspanins CD81, CD9, and CD53. J. Cell Biol. 177 (2007) 329-341
23. Diaz-Griffero F., Kar A., Lee M., Stremlau M., Poeschla E.M., and Sodroski J. Comparative requirements for the restriction of retrovirus infection by TRIM5alpha and TRIMCyp. Virology 369 (2007) 400-410
24. Egberink H.F., Ederveen J., Montelaro R.C., Pedersen N.C., Horzinek M.C., and Koolen M.J. Intracellular proteins of feline immunodeficiency virus and their antigenic relationship with equine infectious anaemia virus proteins. J. Gen. Virol. 71 Pt 3 (1990) 739-743
25. Egberink H.F., Lutz H., and Horzinek M.C. Use of western blot and radioimmunoprecipitation for diagnosis of feline leukemia and feline immunodeficiency virus infections. J. Am. Vet. Med. Assoc. 199 (1991) 1339-1342
26. Elder J.H., Schnolzer M., Hasselkus-Light C.S., Henson M., Lerner D.A., Phillips T.R., Wagaman P.C., and Kent S.B. Identification of proteolytic processing sites within the Gag and Pol polyproteins of feline immunodeficiency virus. J. Virol. 67 (1993) 1869-1876
27. Elder J.H., Sundstrom M., de Rozieres S., de Parseval A., Grant C.K., and Lin Y.C. Molecular mechanisms of FIV infection. Vet. Immunol. Immunopathol. 123 (2008) 3-13
28. Fackler O.T., and Krausslich H.G. Interactions of human retroviruses with the host cell cytoskeleton. Curr. Opin. Microbiol. 9 (2006) 409-415
29. Franke E.K., Yuan H.E., and Luban J. Specific incorporation of cyclophilin A into HIV-1 virions. Nature 372 (1994) 359-362
30. Freed E.O. HIV-1 gag proteins: diverse functions in the virus life cycle. Virology 251 (1998) 1-15
31. Freed E.O., and Martin M.A. The role of human immunodeficiency virus type 1 envelope glycoproteins in virus infection. J. Biol. Chem. 270 (1995) 23883-23886
32. Freed E.O., and Martin M.A. Domains of the human immunodeficiency virus type 1 matrix and gp41 cytoplasmic tail required for envelope incorporation into virions. J. Virol. 70 (1996) 341-351
33. Freed E.O., Orenstein J.M., Buckler-White A.J., and Martin M.A. Single amino acid changes in the human immunodeficiency virus type 1 matrix protein block virus particle production. J. Virol. 68 (1994) 5311-5320
34. Fu W., Dang Q., Nagashima K., Freed E.O., Pathak V.K., and Hu W.S. Effects of Gag mutation and processing on retroviral dimeric RNA maturation. J. Virol. 80 (2006) 1242-1249
35. Fujii K., Hurley J., and Freed E.O. Beyond Tsg101: the role of Alix in 'ESCRTing' HIV-1. Nat. Rev. Microbiol. 5 (2007) 912-916
36. Gamble T.R., Vajdos F.F., Yoo S., Worthylake D.K., Houseweart M., Sundquist W.I., and Hill C.P. Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell 87 (1996) 1285-1294
37. 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. Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein. Science 278 (1997) 849-853
38. Ganser-Pornillos B.K., Cheng A., and Yeager M. Structure of full-length HIV-1 CA: a model for the mature capsid lattice. Cell 131 (2007) 70-79
39. Ganser-Pornillos B.K., Yeager M., and Sundquist W.I. The structural biology of HIV assembly. Curr. Opin. Struct. Biol. 18 (2008) 203-217
40. Garrus J.E., von Schwedler U.K., Pornillos O.W., Morham S.G., Zavitz K.H., Wang H.E., Wettstein D.A., Stray K.M., Côté M., Rich R.L., Myszka D.G., and Sundquist W.I. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107 (2001) 55-65
41. Goila-Gaur R., Demirov D.G., Orenstein J.M., Ono A., and Freed E.O. Defects in human immunodeficiency virus budding and endosomal sorting induced by TSG101 overexpression. J. Virol. 77 (2003) 6507-6519
42. Goila-Gaur R., and Strebel K. HIV-1 Vif, APOBEC, and intrinsic immunity. Retrovirology 5 (2008) 51
43. González S.A., Affranchino J.L., Gelderblom H.R., and Burny A. Assembly of the matrix protein of simian immunodeficiency virus into virus-like particles. Virology 194 (1993) 548-556
44. Groot F., Welsch S., and Sattentau Q.J. Efficient HIV-1 transmission from macrophages to T cells across transient virological synapses. Blood 111 (2008) 4660-4663
45. Haedicke J., de Los Santos K., Goff S.P., and Naghavi M.H. The Ezrin-radixin-moesin family member ezrin regulates stable microtubule formation and retroviral infection. J. Virol. 82 (2008) 4665-4670
46. Hatziioannou T., Cowan S., Goff S.P., Bieniasz P.D., and Towers G.J. Restriction of multiple divergent retroviruses by Lv1 and Ref1. EMBO J. 22 (2003) 385-394
47. Hatziioannou T., Perez-Caballero D., Yang A., Cowan S., and Bieniasz P.D. Retrovirus resistance factors Ref1 and Lv1 are species-specific variants of TRIM5alpha. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 10774-10779
48. Heaslet H., Lin Y.C., Tam K., Torbett B.E., Elder J.H., and Stout C.D. Crystal structure of an FIV/HIV chimeric protease complexed with the broad-based inhibitor, TL-3. Retrovirology 4 (2007) 1
49. Hicke L., and Dunn R. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19 (2003) 141-172
50. Hill C.P., Worthylake D., Bancroft D.P., Christensen A.M., and 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. U.S.A. 93 (1996) 3099-3104
51. Ho M.S., Ou C., Chan Y.R., Chien C.T., and Pi H. The utility F-box for protein destruction. Cell. Mol. Life Sci. 65 (2008) 1977-2000
52. Hohdatsu T., Okada S., Motokawa K., Aizawa C., Yamamoto J.K., and Koyama H. Effect of dual-subtype vaccine against feline immunodeficiency virus infection. Vet. Microbiol. 58 (1997) 155-165
53. Huang M., Orenstein J.M., Martin M.A., and Freed E.O. p6Gag is required for particle production from full-length human immunodeficiency virus type 1 molecular clones expressing protease. J. Virol. 69 (1995) 6810-6818
54. Hurley J.H., and Emr S.D. The ESCRT complexes: structure and mechanism of a membrane-trafficking network. Annu. Rev. Biophys. Biomol. Struct. 35 (2006) 277-298
55. Hurley J.H., Lee S., and Prag G. Ubiquitin-binding domains. Biochem. J. 399 (2006) 361-372
56. Javanbakht H., Diaz-Griffero F., Yuan W., Yeung D.F., Li X., Song B., and Sodroski J. The ability of multimerized cyclophilin A to restrict retrovirus infection. Virology 367 (2007) 19-29
57. Jin Z., Jin L., Peterson D.L., and Lawson C.L. Model for lentivirus capsid core assembly based on crystal dimers of EIAV p26. J. Mol. Biol. 286 (1999) 83-93
58. Johnson M.C., Spidel J.L., Ako-Adjei D., Wills J.W., and Vogt V.M. The C-terminal half of TSG101 blocks Rous sarcoma virus budding and sequesters Gag into unique nonendosomal structures. J. Virol. 79 (2005) 3775-3786
59. Johnston J.C., Gasmi M., Lim L.E., Elder J.H., Yee J.K., Jolly D.J., Campbell K.P., Davidson B.L., and Sauter S.L. Minimum requirements for efficient transduction of dividing and nondividing cells by feline immunodeficiency virus vectors. J. Virol. 73 (1999) 4991-5000
60. Joshi A., and Freed E. HIV-1 Gag trafficking. Future HIV Ther. 1 (2007) 427-438
61. Joshi A., Munshi U., Ablan S.D., Nagashima K., and Freed E.O. Functional replacement of a retroviral late domain by ubiquitin fusion. Traffic 9 (2008) 1972-1983
62. Jouvenet N., Neil S.J., Zhadina M., Zang T., Kratovac Z., Lee Y., McNatt M., Hatziioannou T., and Bieniasz P.D. Broad-spectrum inhibition of retroviral and filoviral particle release by tetherin. J. Virol. 83 (2009) 1837-1844
63. Karpas A., Lowdell M., Jacobson S.K., and Hill F. Inhibition of human immunodeficiency virus and growth of infected T cells by the immunosuppressive drugs cyclosporin A and FK 506. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 8351-8355
64. Katzourakis A., Tristem M., Pybus O.G., and Gifford R.J. Discovery and analysis of the first endogenous lentivirus. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 6261-6265
65. Keckesova Z., Ylinen L.M., and Towers G.J. The human and African green monkey TRIM5alpha genes encode Ref1 and Lv1 retroviral restriction factor activities. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 10780-10785
66. Kemler I., Barraza R.A., and Poeschla E.M. Mapping the encapsidation determinants of feline immunodeficiency virus. J. Virol. 76 (2002) 11889-11903
67. Kikonyogo A., Bouamr F., Vana M.L., Xiang Y., Aiyar A., Carter C., and Leis J. Proteins related to the Nedd4 family of ubiquitin protein ligases interact with the L domain of Rous sarcoma virus and are required for gag budding from cells. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 11199-11204
68. Kratovac Z., Virgen C.A., Bibollet-Ruche F., Hahn B.H., Bieniasz P.D., and Hatziioannou T. Primate lentivirus capsid sensitivity to TRIM5 proteins. J. Virol. 82 (2008) 6772-6777
69. Lambelé M., Labrosse B., Roch E., Moreau A., Verrier B., Barin F., Roingeard P., Mammano F., and Brand D. Impact of natural polymorphism within the gp41 cytoplasmic tail of human immunodeficiency virus type 1 on the intracellular distribution of envelope glycoproteins and viral assembly. J. Virol. 81 (2007) 125-140
70. Lee S., Joshi A., Nagashima K., Freed E.O., and Hurley J.H. Structural basis for viral late-domain binding to Alix. Nat. Struct. Mol. Biol. 14 (2007) 194-199
71. Lin T.Y., and Emerman M. Cyclophilin A interacts with diverse lentiviral capsids. Retrovirology 3 (2006) 70
72. Lin Y.C., Brik A., de Parseval A., Tam K., Torbett B.E., Wong C.H., and Elder J.H. Altered gag polyprotein cleavage specificity of feline immunodeficiency virus/human immunodeficiency virus mutant proteases as demonstrated in a cell-based expression system. J. Virol. 80 (2006) 7832-7843
73. Lopez-Vergès S., Camus G., Blot G., Beauvoir R., Benarous R., and Berlioz-Torrent C. Tail-interacting protein TIP47 is a connector between Gag and Env and is required for Env incorporation into HIV-1 virions. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 14947-14952
74. Luban J. Cyclophilin A, TRIM5, and resistance to human immunodeficiency virus type 1 infection. J. Virol. 81 (2007) 1054-1061
75. Luttge B.G., Shehu-Xhilaga M., Demirov D.G., Adamson C.S., Soheilian F., Nagashima K., Stephen A.G., Fisher R.J., and Freed E.O. Molecular characterization of feline immunodeficiency virus budding. J. Virol. 82 (2008) 2106-2119
76. Manrique M.L., González S.A., and Affranchino J.L. Functional relationship between the matrix proteins of feline and simian immunodeficiency viruses. Virology 329 (2004) 157-167
77. Manrique M.L., Rauddi M.L., González S.A., and Affranchino J.L. Functional domains in the feline immunodeficiency virus nucleocapsid protein. Virology 327 (2004) 83-92
78. Martin-Serrano J. The role of ubiquitin in retroviral egress. Traffic 8 (2007) 1297-1303
79. Martin-Serrano J., Yarovoy A., Perez-Caballero D., Bieniasz P.D., and Yaravoy A. Divergent retroviral late-budding domains recruit vacuolar protein sorting factors by using alternative adaptor proteins. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 12414-12419
80. Martin-Serrano J., Zang T., and Bieniasz P.D. HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nat. Med. 7 (2001) 1313-1319
81. Martinez N.W., Xue X., Berro R.G., Kreitzer G., and Resh M.D. Kinesin KIF4 regulates intracellular trafficking and stability of the human immunodeficiency virus type 1 Gag polyprotein. J. Virol. 82 (2008) 9937-9950
82. Martins A.N., Medeiros S.O., Simonetti J.P., Schatzmayr H.G., Tanuri A., and Brindeiro R.M. Phylogenetic and genetic analysis of feline immunodeficiency virus gag, pol, and env genes from domestic cats undergoing nucleoside reverse transcriptase inhibitor treatment or treatment-naïve cats in Rio de Janeiro, Brazil. J. Virol. 82 (2008) 7863-7874
83. Morita E., and Sundquist W.I. Retrovirus budding. Annu. Rev. Cell Dev. Biol. 20 (2004) 395-425
84. Mortola E., Endo Y., Ohno K., Watari T., Tsujimoto H., and Hasegawa A. The use of two immunosuppressive drugs, cyclosporin A and tacrolimus, to inhibit virus replication and apoptosis in cells infected with feline immunodeficiency virus. Vet. Res. Commun. 22 (1998) 553-563
85. Moscardini M., Pistello M., Bendinelli M., Ficheux D., Miller J.T., Gabus C., Le Grice S.F., Surewicz W.K., and Darlix J.L. Functional interactions of nucleocapsid protein of feline immunodeficiency virus and cellular prion protein with the viral RNA. J. Mol. Biol. 318 (2002) 149-159
86. Münk C., Beck T., Zielonka J., Hotz-Wagenblatt A., Chareza S., Battenberg M., Thielebein J., Cichutek K., Bravo I., O'Brien S.J., Löchelt M., and Yuhki N. Functions, structure, and read-through alternative splicing of feline APOBEC3 genes. Genome Biol. 9 (2008) R48
87. Münk C., Zielonka J., Constabel H., Kloke B.P., Rengstl B., Battenberg M., Bonci F., Pistello M., Löchelt M., and Cichutek K. Multiple restrictions of human immunodeficiency virus type 1 in feline cells. J. Virol. 81 (2007) 7048-7060
88. Munshi U.M., Kim J., Nagashima K., Hurley J.H., and Freed E.O. An Alix fragment potently inhibits HIV-1 budding: characterization of binding to retroviral YPXL late domains. J. Biol. Chem. 282 (2007) 3847-3855
89. Murakami T., and Freed E.O. Genetic evidence for an interaction between human immunodeficiency virus type 1 matrix and alpha-helix 2 of the gp41 cytoplasmic tail. J. Virol. 74 (2000) 3548-3554
90. Muriaux D., Mirro J., Harvin D., and Rein A. RNA is a structural element in retrovirus particles. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 5246-5251
91. Mustafa F., Jayanth P., Phillip P.S., Ghazawi A., Schmidt R.D., Lew K.A., and Rizvi T.A. Relative activity of the feline immunodeficiency virus promoter in feline and primate cell lines. Microbes Infect. 7 (2005) 233-239
92. Naghavi M.H., and Goff S.P. Retroviral proteins that interact with the host cell cytoskeleton. Curr. Opin. Immunol. 19 (2007) 402-407
93. Naghavi M.H., Valente S., Hatziioannou T., de Los Santos K., Wen Y., Mott C., Gundersen G.G., and Goff S.P. Moesin regulates stable microtubule formation and limits retroviral infection in cultured cells. EMBO J. 26 (2007) 41-52
94. Nath M.D., and Peterson D.L. In vitro assembly of feline immunodeficiency virus capsid protein: biological role of conserved cysteines. Arch. Biochem. Biophys. 392 (2001) 287-294
95. Neil S.J., Zang T., and Bieniasz P.D. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451 (2008) 425-430
96. Newman R.M., Hall L., Kirmaier A., Pozzi L.A., Pery E., Farzan M., O'Neil S.P., and Johnson W. Evolution of a TRIM5-CypA splice isoform in old world monkeys. PLoS Pathog. 4 (2008) e1000003
97. Nisole S., Lynch C., Stoye J.P., and Yap M.W. A Trim5-cyclophilin A fusion protein found in owl monkey kidney cells can restrict HIV-1. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 13324-13328
98. Norelli S., El Daker S., D'Ostilio D., Mele F., Mancini F., Taglia F., Ruggieri A., Ciccozzi M., Cauda R., Ciervo A., Barreca M.L., Pistello M., Bendinelli M., and Savarino A. Response of feline immunodeficiency virus (FIV) to tipranavir may provide new clues for development of broad-based inhibitors of retroviral proteases acting on drug-resistant HIV-1. Curr. HIV Res. 6 (2008) 306-317
99. Olmsted R.A., Hirsch V.M., Purcell R.H., and Johnson P.R. Nucleotide sequence analysis of feline immunodeficiency virus: genome organization and relationship to other lentiviruses. Proc. Natl. Acad. Sci. U.S.A. 86 (1989) 8088-8092
100. Ono A., Ablan S.D., Lockett S.J., Nagashima K., and Freed E.O. Phosphatidylinositol (4,5) bisphosphate regulates HIV-1 Gag targeting to the plasma membrane. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 14889-14894
101. Ono A., Demirov D.G., and Freed E.O. Relationship between human immunodeficiency virus type 1 Gag multimerization and membrane binding. J. Virol. 74 (2000) 5142-5150
102. Ono A., Waheed A.A., Joshi A., and Freed E.O. Association of human immunodeficiency virus type 1 gag with membrane does not require highly basic sequences in the nucleocapsid: use of a novel Gag multimerization assay. J. Virol. 79 (2005) 14131-14140
103. Ott D.E., Coren L.V., Johnson D.G., Kane B.P., Sowder II R.C., Kim Y.D., Fisher R.J., Zhou X.Z., Lu K.P., and Henderson L.E. Actin-binding cellular proteins inside human immunodeficiency virus type 1. Virology 266 (2000) 42-51
104. Ott D.E., Coren L.V., Kane B.P., Busch L.K., Johnson D.G., Sowder II R.C., Chertova E.N., Arthur L.O., and Henderson L.E. Cytoskeletal proteins inside human immunodeficiency virus type 1 virions. J. Virol. 70 (1996) 7734-7743
105. Ozato K., Shin D.M., Chang T.H., and Morse H.C. TRIM family proteins and their emerging roles in innate immunity. Nat. Rev. Immunol. 8 (2008) 849-860
106. Pecon-Slattery J., Troyer J.L., Johnson W.E., and O'Brien S.J. Evolution of feline immunodeficiency virus in Felidae: implications for human health and wildlife ecology. Vet. Immunol. Immunopathol. 123 (2008) 32-44
107. Pedersen N.C., Ho E.W., Brown M.L., and Yamamoto J.K. Isolation of a T-lymphotropic virus from domestic cats with an immunodeficiency-like syndrome. Science 235 (1987) 790-793
108. Peng C., Ho B.K., Chang T.W., and Chang N.T. Role of human immunodeficiency virus type 1-specific protease in core protein maturation and viral infectivity. J. Virol. 63 (1989) 2550-2556
109. Pu R., Tellier M.C., and Yamamoto J.K. Mechanism(s) of FIV vaccine protection. Leukemia 11 Suppl. 3 (1997) 98-101
110. Rey O., Canon J., and Krogstad P. HIV-1 Gag protein associates with F-actin present in microfilaments. Virology 220 (1996) 530-534
111. Ribeiro I.P., Menezes A.N., Moreira M.A., Bonvicino C.R., Seuanez H.N., and Soares M.A. Evolution of cyclophilin A and TRIMCyp retrotransposition in New World primates. J. Virol. 79 (2005) 14998-15003
112. Rold C.J., and Aiken C. Proteasomal degradation of TRIM5alpha during retrovirus restriction. PLoS Pathog. 4 (2008) e1000074
113. Rulli S.J., Hibbert C.S., Mirro J., Pederson T., Biswal S., and Rein A. Selective and nonselective packaging of cellular RNAs in retrovirus particles. J. Virol. 81 (2007) 6623-6631
114. Saad J.S., Ablan S.D., Ghanam R.H., Kim A., Andrews K., Nagashima K., Soheilian F., Freed E.O., and Summers M.F. Structure of the myristylated human immunodeficiency virus type 2 matrix protein and the role of phosphatidylinositol-(4,5)-bisphosphate in membrane targeting. J. Mol. Biol. 382 (2008) 434-447
115. Saad J.S., Miller J., Tai J., Kim A., Ghanam R.H., and Summers M.F. Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 11364-11369
116. Saenz D.T., Teo W., Olsen J.C., and Poeschla E.M. Restriction of feline immunodeficiency virus by Ref1, Lv1, and primate TRIM5alpha proteins. J. Virol. 79 (2005) 15175-15188
117. Salzwedel K., Martin D.E., and Sakalian M. Maturation inhibitors: a new therapeutic class targets the virus structure. AIDS Rev. 9 (2007) 162-172
118. Sasaki H., Nakamura M., Ohno T., Matsuda Y., Yuda Y., and Nonomura Y. Myosin-actin interaction plays an important role in human immunodeficiency virus type 1 release from host cells. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 2026-2030
119. Sattentau Q. Avoiding the void: cell-to-cell spread of human viruses. Nat. Rev. Microbiol. 6 (2008) 815-826
120. Savarino A., Pistello M., D'Ostilio D., Zabogli E., Taglia F., Mancini F., Ferro S., Matteucci D., De Luca L., Barreca M.L., Ciervo A., Chimirri A., Ciccozzi M., and Bendinelli M. Human immunodeficiency virus integrase inhibitors efficiently suppress feline immunodeficiency virus replication in vitro and provide a rationale to redesign antiretroviral treatment for feline AIDS. Retrovirology 4 (2007) 79
121. Sayah D.M., Sokolskaja E., Berthoux L., and Luban J. Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 430 (2004) 569-573
122. Shehu-Xhilaga M., Ablan S.D., Demirov D.G., Chen C., Montelaro R.C., and Freed E.O. Late domain-dependent inhibition of equine infectious anemia virus budding. J. Virol. 78 (2004) 724-732
123. Sokolskaja E., Berthoux L., and Luban J. Cyclophilin A and TRIM5alpha independently regulate human immunodeficiency virus type 1 infectivity in human cells. J. Virol. 80 (2006) 2855-2862
124. Strack B., Calistri A., Craig S., Popova E., and Göttlinger H.G. AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 114 (2003) 689-699
125. Stremlau M., Owens C.M., Perron M.J., Kiessling M., Autissier P., and Sodroski J. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 427 (2004) 848-853
126. Stremlau M., Perron M., Lee M., Li Y., Song B., Javanbakht H., Diaz-Griffero F., Anderson D.J., Sundquist W.I., and Sodroski J. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 5514-5519
127. Stuffers S., Brech A., and Stenmark H. ESCRT proteins in physiology and disease. Exp. Cell Res. 315 (2009) 1619-1626
128. Sundstrom M., Chatterji U., Schaffer L., de Rozières S., and Elder J.H. Feline immunodeficiency virus OrfA alters gene expression of splicing factors and proteasome-ubiquitination proteins. Virology 371 (2008) 394-404
129. Tang Y., Winkler U., Freed E.O., Torrey T.A., Kim W., Li H., Goff S.P., and Morse H.C. Cellular motor protein KIF-4 associates with retroviral Gag. J. Virol. 73 (1999) 10508-10513
130. Tomonaga K., Itagaki S.I., Kashiwase H., Kawaguchi Y., Inoshima Y., Ikeda Y., and Mikami T. Characterization of an integrase mutant of feline immunodeficiency virus. Arch. Virol. 143 (1998) 1-14
131. Towers G.J. The control of viral infection by tripartite motif proteins and cyclophilin A. Retrovirology 4 (2007) 40
132. Troyer J.L., Pecon-Slattery J., Roelke M.E., Johnson W., VandeWoude S., Vazquez-Salat N., Brown M., Frank L., Woodroffe R., Winterbach C., Winterbach H., Hemson G., Bush M., Alexander K.A., Revilla E., and O'Brien S.J. Seroprevalence and genomic divergence of circulating strains of feline immunodeficiency virus among Felidae and Hyaenidae species. J. Virol. 79 (2005) 8282-8294
133. Van Damme N., Goff D., Katsura C., Jorgenson R.L., Mitchell R., Johnson M.C., Stephens E.B., and Guatelli J.C. The interferon-induced protein BST-2 restricts HIV-1 release and is downregulated from the cell surface by the viral Vpu protein. Cell Host Microbe 3 (2008) 245-252
134. VerPlank L., Bouamr F., LaGrassa T.J., Agresta B., Kikonyogo A., Leis J., and Carter C.A. Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55(Gag). Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 7724-7729
135. Virgen C.A., Kratovac Z., Bieniasz P.D., and Hatziioannou T. Independent genesis of chimeric TRIM5-cyclophilin proteins in two primate species. Proc. Natl. Acad. Sci. U.S.A. 105 (2008) 3563-3568
136. Willett B.J., Flynn J.N., and Hosie M.J. FIV infection of the domestic cat: an animal model for AIDS. Immunol. Today 18 (1997) 182-189
137. Williams R.L., and Urbe S. The emerging shape of the ESCRT machinery. Nat. Rev. Mol. Cell Biol. 8 (2007) 355-368
138. Wilson S.J., Webb B.L., Ylinen L.M., Verschoor E., Heeney J.L., and Towers G.J. Independent evolution of an antiviral TRIMCyp in rhesus macaques. Proc. Natl. Acad. Sci. U.S.A. 105 (2008) 3557-3562
139. Winkler I.G., Löchelt M., and Flower R.L. Epidemiology of feline foamy virus and feline immunodeficiency virus infections in domestic and feral cats: a seroepidemiological study. J. Clin. Microbiol. 37 (1999) 2848-2851
140. Wolf D., and Goff S.P. Host restriction factors blocking retroviral replication. Annu. Rev. Genet. 42 (2008) 143-163
141. Yuan X., Yu X., Lee T.H., and Essex M. Mutations in the N-terminal region of human immunodeficiency virus type 1 matrix protein block intracellular transport of the Gag precursor. J. Virol. 67 (1993) 6387-6394
142. Zhadina M., McClure M.O., Johnson M.C., and Bieniasz P.D. Ubiquitin-dependent virus particle budding without viral protein ubiquitination. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 20031-20036
143. Zhou W., 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