A second-site suppressor significantly improves the defective phenotype imposed by mutation of an aromatic residue in the N-terminal domain of the HIV-1 capsid protein

Virology

Volumn 359, Issue 1, 2007, Pages 105-115

  Tang, Shixing ^a,b   Ablan, Sherimay ^c   Dueck, Megan ^a   Ayala López, Wilfredo ^a   Soto, Brenda ^a   Caplan, Margaret ^a   Nagashima, Kunio ^d   Hewlett, Indira K ^b   Freed, Eric O ^c   Levin, Judith G ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d SAIC FREDERICK INC   (United States)

Author keywords

Dominant negative inhibition; HIV 1 assembly; HIV 1 capsid protein; HIV 1 viral cores; Reverse transcriptase; Second site suppressors; Structural models; Transmission electron microscopy

Indexed keywords

VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROPHOBICITY; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN STRUCTURE, FUNCTION AND VARIABILITY; VIRION; VIRUS CAPSID; VIRUS PARTICLE; VIRUS REPLICATION; WILD TYPE;

CAPSID PROTEINS; CELL LINE; HIV-1; HUMANS; MICROBIAL VIABILITY; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, MOLECULAR; MUTATION; PHENOTYPE; PROTEIN STRUCTURE, TERTIARY; RNA-DIRECTED DNA POLYMERASE; SUPPRESSION, GENETIC; VIRION; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1; MIRIDAE;

EID: 33846847729     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2006.09.027     Document Type: Article

References (68)

1. Aberham C., Weber S., and Phares W. Spontaneous mutations in the human immunodeficiency virus type 1 gag gene that affect viral replication in the presence of cyclosporins. J. Virol. 70 (1996) 3536-3544
2. Adachi A., Gendelman H.E., Koenig S., Folks T., Willey R., Rabson A., and Martin M.A. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59 (1986) 284-291
3. Ako-Adjei D., Johnson M.C., and Vogt V.M. The retroviral capsid domain dictates virion size, morphology, and coassembly of Gag into virus-like particles. J. Virol. 79 (2005) 13463-13472
4. Auerbach M.R., Shu C., Kaplan A., and Singh I.R. Functional characterization of a portion of the Moloney murine leukemia virus gag gene by genetic footprinting. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 11678-11683
5. Auerbach M.R., Brown K.R., Kaplan A., de Las Nueces D., and Singh I.R. A small loop in the capsid protein of Moloney murine leukemia virus controls assembly of spherical cores. J. Virol. 80 (2006) 2884-2893
6. Benjamin J., Ganser-Pornillos B.K., Tivol W.F., Sundquist W.I., and Jensen G.J. Three-dimensional structure of HIV-1 virus-like particles by electron cryotomography. J. Mol. Biol. 346 (2005) 577-588
7. Bowzard J.B., Wills J.W., and Craven R.C. Second-site suppressors of Rous sarcoma virus CA mutations: evidence for interdomain interactions. J. Virol. 75 (2001) 6850-6856
8. Briggs J.A.G., Wilk T., Welker R., Kräusslich H.-G., and Fuller S.D. Structural organization of authentic, mature HIV-1 virions and cores. EMBO J. 22 (2003) 1707-1715
9. Briggs J.A.G., Simon M.N., Gross I., Kräusslich H.-G., Fuller S.D., Vogt V.M., and Johnson M.C. The stoichiometry of Gag protein in HIV-1. Nat. Struct. Mol. Biol. 11 (2004) 672-675
10. Briggs J.A.G., Grünewald K., Glass B., Förster F., Kräusslich H.-G., and Fuller S.D. The mechanism of HIV-1 core assembly: insights from three-dimensional reconstructions of authentic virions. Structure 14 (2006) 15-20
11. Cairns T.M., and Craven R.C. Viral DNA synthesis defects in assembly-competent Rous sarcoma virus CA mutants. J. Virol. 75 (2001) 242-250
12. 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
13. Cheng H., Tarnok J., and Parks W.P. Human immunodeficiency virus type 1 genome activation induced by human T-cell leukemia virus type 1 Tax protein is through cooperation of NF-κB and Tat. J. Virol. 72 (1998) 6911-6916
14. Derdeyn C.A., Decker J.M., Sfakianos J.N., Wu X., O'Brien W.A., Ratner L., Kappes J.C., Shaw G.M., and Hunter E. Sensitivity of human immunodeficiency virus type 1 to the fusion inhibitor T-20 is modulated by coreceptor specificity defined by the V3 loop of gp120. J. Virol. 74 (2000) 8358-8367
15. Dorfman T., Bukovsky A., Öhagen Å., Höglund S., and Göttlinger H.G. Functional domains of the capsid protein of human immunodeficiency virus type 1. J. Virol. 68 (1994) 8180-8187
16. Ehrlich L.S., Agresta B.E., and Carter C.A. Assembly of recombinant human immunodeficiency virus type 1 capsid protein in vitro. J. Virol. 66 (1992) 4874-4883
17. Fitzon T., Leschonsky B., Bieler K., Paulus C., Schröder J., Wolf H., and Wagner R. Proline residues in the HIV-1 NH2-terminal capsid domain: structure determinants for proper core assembly and subsequent steps of early replication. Virology 268 (2000) 294-307
18. Forshey B.M., and Aiken C. Disassembly of human immunodeficiency virus type 1 cores in vitro reveals association of Nef with the subviral ribonucleoprotein complex. J. Virol. 77 (2003) 4409-4414
19. Forshey B.M., von Schwedler U., Sundquist W.I., and Aiken C. Formation of a human immunodeficiency virus type 1 core of optimal stability is crucial for viral replication. J. Virol. 76 (2002) 5667-5677
20. Freed E.O. HIV-1 Gag proteins: diverse functions in the virus life cycle. Virology 251 (1998) 1-15
21. Freed E.O., and Martin M.A. Evidence for a functional interaction between the V1/V2 and C4 domains of human immunodeficiency virus type 1 envelope glycoprotein gp120. J. Virol. 68 (1994) 2503-2512
22. Freed E.O., Englund G., and Martin M.A. Role of the basic domain of human immunodeficiency virus type 1 matrix in macrophage infection. J. Virol. 69 (1995) 3949-3954
23. Furuta R.A., Shimano R., Ogasawara T., Inubushi R., Amano K., Akari H., Hatanaka M., Kawamura M., and Adachi A. HIV-1 capsid mutants inhibit the replication of wild-type virus at both early and late infection phases. FEBS Lett. 415 (1997) 231-234
24. 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
25. Ganser B.K., Li S., Klishko V.Y., Finch J.T., and Sundquist W.I. Assembly and analysis of conical models for the HIV-1 core. Science 283 (1999) 80-83
26. Ganser B.K., Cheng A., Sundquist W.I., and Yeager M. Three-dimensional structure of the M-MuLV CA protein on a lipid monolayer: a general model for retroviral capsid assembly. EMBO J. 22 (2003) 2886-2892
27. Ganser-Pornillos B.K., von Schwedler U.K., Stray K.M., Aiken C., and Sundquist W.I. Assembly properties of the human immunodeficiency virus type 1 CA protein. J. Virol. 78 (2004) 2545-2552
28. Gitti R.K., Lee B.M., Walker J., Summers M.F., Yoo S., and Sundquist W.I. Structure of the amino-terminal core domain of the HIV-1 capsid protein. Science 273 (1996) 231-235
29. Gross I., Hohenburg H., and Kräusslich H.-G. In vitro assembly properties of purified bacterially expressed capsid proteins of human immunodeficiency virus. Eur. J. Biochem. 249 (1997) 592-600
30. Gross I., Hohenberg H., Huckhagel C., and Kräusslich H.-G. N-terminal extension of human immunodeficiency virus capsid protein converts the in vitro assembly phenotype from tubular to spherical particles. J. Virol. 72 (1998) 4798-4810
31. Gross I., Hohenberg H., Wilk T., Wiegers K., Grättinger M., Müller B., Fuller S., and Kräusslich H.-G. A conformational switch controlling HIV-1 morphogenesis. EMBO J. 19 (2000) 103-113
32. Guo X., Roy B.B., Hu J., Roldan A., Wainberg M.A., and Liang C. The R362A mutation at the C-terminus of CA inhibits packaging of human immunodeficiency virus type 1 RNA. Virology 343 (2005) 190-200
33. Huseby D., Barklis R.L., Alfadhli A., and Barklis E. Assembly of human immunodeficiency virus precursor Gag proteins. J. Biol. Chem. 280 (2005) 17664-17670
34. Khan M.A., Aberham C., Kao S., Akari H., Gorelick R., Bour S., and Strebel K. Human immunodeficiency virus type 1 Vif protein is packaged into the nucleoprotein complex through an interaction with viral genomic RNA. J. Virol. 75 (2001) 7252-7265
35. Klutch M., Woerner A.M., Marcus-Sekura C.J., and Levin J.G. Generation of HIV-1/HIV-2 cross-reactive peptide antisera by small sequence changes in HIV-1 reverse transcriptase and integrase immunizing peptides. J. Biomed. Sci. 5 (1998) 192-202
36. Lanman J., and Prevelige Jr. P.E. Kinetic and mass spectrometry-based investigation of human immunodeficiency virus type 1 assembly and maturation. Adv. Virus Res. 64 (2005) 285-309
37. Lanman J., Lam T.T., Barnes S., Sakalian M., Emmett M.R., Marshall A.G., and Prevelige Jr. P.E. Identification of novel interactions in HIV-1 capsid protein assembly by high-resolution mass spectrometry. J. Mol. Biol. 325 (2003) 759-772
38. Lanman J., Lam T.T., Emmett M.R., Marshall A.G., Sakalian M., and Prevelige Jr. P.E. Key interactions in HIV-1 maturation identified by hydrogen-deuterium exchange. Nat. Struct. Mol. Biol. 11 (2004) 676-677
39. Li S., Hill C.P., Sundquist W.I., and Finch J.T. Image reconstructions of helical assemblies of the HIV-1 CA protein. Nature 407 (2000) 409-413
40. Liang C., Hu J., Russell R.S., Roldan A., Kleiman L., and Wainberg M.A. Characterization of a putative α-helix across the capsid-SP1 boundary that is critical for the multimerization of human immunodeficiency virus type 1 gag. J. Virol. 76 (2002) 11729-11737
41. Liang C., Hu J., Whitney J.B., Kleiman L., and Wainberg M.A. A structurally disordered region at the C terminus of capsid plays essential roles in multimerization and membrane binding of the Gag protein of human immunodeficiency virus type 1. J. Virol. 77 (2003) 1772-1783
42. Mammano F., Öhagen Å., Höglund S., and Göttlinger H.G. Role of the major homology region of human immunodeficiency virus type 1 in virion morphogenesis. J. Virol. 68 (1994) 4927-4936
43. Mayo K., Huseby D., McDermott J., Arvidson B., Finlay L., and Barklis E. Retrovirus capsid protein assembly arrangements. J. Mol. Biol. 325 (2003) 225-237
44. Melamed D., Mark-Danieli M., Kenan-Eichler M., Kraus O., Castiel A., Laham N., Pupko T., Glaser F., Ben-Tal N., and Bacharach E. The conserved carboxy terminus of the capsid domain of human immunodeficiency virus type 1 Gag protein is important for virion assembly and release. J. Virol. 78 (2004) 9675-9688
45. Momany C., Kovari L.C., Prongay A.J., Keller W., Gitti R.K., Lee B.M., Gorbalenya A.E., Tong L., McClure J., Ehrlich L.S., Summers M.F., Carter C., and Rossmann M.G. Crystal structure of dimeric HIV-1 capsid protein. Nat. Struct. Biol. 3 (1996) 763-770
46. Mortuza G.B., Haire L.F., Stevens A., Smerdon S.J., Stoye J.P., and Taylor I.A. High-resolution structure of a retroviral capsid hexameric amino-terminal domain. Nature 431 (2004) 481-485
47. Murakami T., and Freed E.O. The long cytoplasmic tail of gp41 is required in a cell type-dependent manner for HIV-1 envelope glycoprotein incorporation into virions. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 343-348
48. Platt E.J., Wehrly K., Duhmann S.E., Chesebro B., and Kabat D. Effects of CCR5 and CD4 cell surface concentrations on infections by macrophage tropic isolates of human immunodeficiency virus type 1. J. Virol. 72 (1998) 2855-2864
49. Reicin A.S., Ohagen A., Yin L., Hoglund S., and Goff S.P. The role of Gag in human immunodeficiency virus type 1 virion morphogenesis and early steps of the viral life cycle. J. Virol. 70 (1996) 8645-8652
50. Roos J.W., Maughan M.F., Liao Z., Hildreth J.E.K., and Clements J.E. LuSIV cells: a reporter cell line for the detection and quantitation of a single cycle of HIV and SIV replication. Virology 273 (2000) 307-315
51. Rulli Jr. S.J., Muriaux D., Nagashima K., Mirro J., Oshima M., Baumann J.G., and Rein A. Mutant murine leukemia virus Gag proteins lacking proline at the N-terminus of the capsid domain block infectivity in virions containing wild-type Gag. Virology 347 (2006) 364-371
52. Scholz I., Arvidson B., Huseby D., and Barklis E. Virus particle core defects caused by mutations in the human immunodeficiency virus capsid N-terminal domain. J. Virol. 79 (2005) 1470-1479
53. Shimano R., Iida S., Fukumori T., Yamamoto Y., Kawamura M., Furuta R.A., and Adachi A. Inhibition of HIV replication by capsid mutant C6b. Biochem. Biophys. Res. Commun. 242 (1998) 313-316
54. Swanstrom R., and Wills J.W. Synthesis, assembly, and processing of viral proteins. In: Coffin J.M., Hughes S.H., and Varmus H.E. (Eds). Retroviruses (1997), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 263-334
55. Tang S., Collier A.J., and Elliott R.M. Alterations to both the primary and predicted secondary structure of stem-loop IIIc of the hepatitis C virus 1b 5′ untranslated region (5′ UTR) lead to mutants severely defective in translation which cannot be complemented in trans by the wild-type 5′UTR sequence. J. Virol. 73 (1999) 2359-2364
56. Tang S., Murakami T., Agresta B.E., Campbell S., Freed E.O., and Levin J.G. 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 (2001) 9357-9366
57. 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
58. Tang C., Loeliger E., Kinde I., Kyere S., Mayo K., Barklis E., Sun Y., Huang M., and Summers M.F. Antiviral inhibition of the HIV-1 capsid protein. J. Mol. Biol. 327 (2003) 1013-1020
59. Tang S., Murakami T., Cheng N., Steven A.C., Freed E.O., and Levin J.G. Human immunodeficiency virus type 1 N-terminal capsid mutants containing cores with abnormally high levels of capsid protein and virtually no reverse transcriptase. J. Virol. 77 (2003) 12592-12602
60. Trono D., Feinberg M.B., and Baltimore D. HIV-1 Gag mutants can dominantly interfere with the replication of the wild-type virus. Cell 59 (1989) 113-120
61. Vogt V.M. Retroviral virions and genomes. In: Coffin J.M., Hughes S.H., and Varmus H.E. (Eds). Retroviruses (1997), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 27-69
62. Vogt V.M., and Simon M.N. Mass determination of Rous sarcoma virus virions by scanning transmission electron microscopy. J. Virol. 73 (1999) 7050-7055
63. von Schwedler U., Stemmler T.L., Klishko V.Y., Li S., Albertine K.H., Davis D.R., and Sundquist W.I. Proteolytic refolding of the HIV-1 capsid protein amino-terminus facilitates viral core assembly. EMBO J. 17 (1998) 1555-1568
64. von Schwedler U.K., Stray K.M., Garrus J.E., and Sundquist W.I. Functional surfaces of the human immunodeficiency virus type 1 capsid protein. J. Virol. 77 (2003) 5439-5450
65. Wei X., Decker J.M., Liu H., Zhang Z., Arani R.B., Kilby J.M., Saag M.S., Wu X., Shaw G.M., and Kappes J.C. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob. Agents Chemother. 46 (2002) 1896-1905
66. Wiegers K., Rutter G., Kottler H., Tessmer U., Hohenberg H., and Kräusslich H.-G. Sequential steps in human immunodeficiency virus particle maturation revealed by alterations of individual Gag polyprotein cleavage sites. J. Virol. 72 (1998) 2846-2854
67. Wills J.W., and Craven R.C. Form, function, and use of retroviral Gag proteins. AIDS 5 (1991) 639-654
68. Zack J.A., Cann A.J., Lugo J.P., and Chen I.S. HIV-1 production from infected peripheral blood T cells after HTLV-1 induced mitogenic stimulation. Science 240 (1988) 1026-1029