Multiple sites in the N-terminal half of simian immunodeficiency virus capsid protein contribute to evasion from rhesus monkey TRIM5α-mediated restriction

Retrovirology

Volumn 7, Issue , 2010, Pages

  Kono, Ken ^a   Song, Haihan ^a   Yokoyama, Masaru ^b   Sato, Hironori ^b   Shioda, Tatsuo ^a   Nakayama, Emi E ^a  

^a OSAKA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; GLUTAMINE; PROLINE; TRIPARTITE MOTIF PROTEIN 5; PROTEIN; TRIM5(ALPHA) PROTEIN, RHESUS MONKEY; VIRULENCE FACTOR;

ALPHA HELIX; AMINO ACID COMPOSITION; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 2; MOLECULAR MODEL; NONHUMAN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RESTRICTION SITE; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; STRAIN DIFFERENCE; STRUCTURE ANALYSIS; VIRION; VIRUS EXAMINATION; VIRUS PARTICLE; VIRUS RESISTANCE; VIRUS STRAIN; ANIMAL; CELL LINE; CHEMICAL STRUCTURE; GENETIC RECOMBINATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNE EVASION; IMMUNOLOGY; MACACA; PROTEIN QUATERNARY STRUCTURE;

HUMAN IMMUNODEFICIENCY VIRUS 2; MACACA FASCICULARIS; MACACA MULATTA; MIRIDAE; SIMIAN IMMUNODEFICIENCY VIRUS;

ANIMALS; CAPSID PROTEINS; CELL LINE; HIV-2; HUMANS; IMMUNE EVASION; MACACA MULATTA; MODELS, MOLECULAR; PROTEIN STRUCTURE, QUATERNARY; PROTEINS; RECOMBINATION, GENETIC; SIMIAN IMMUNODEFICIENCY VIRUS; VIRULENCE FACTORS;

EID: 77956485026     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-7-72     Document Type: Article

References (74)

1. Gao F, Bailes E, Robertson DL, Chen Y, Rodenburg CM, Michael SF, Cummins LB, Arthur LO, Peeters M, Shaw GM, Sharp PM, Hahn BH. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 1999, 397:436-441. 10.1038/17130, 9989410.
2. Shibata R, Sakai H, Kawamura M, Tokunaga K, Adachi A. Early replication block of human immunodeficiency virus type 1 in monkey cells. J Gen Virol 1995, 76(Pt 11):2723-2730. 10.1099/0022-1317-76-11-2723, 7595379.
3. Himathongkham S, Luciw PA. Restriction of HIV-1 (subtype B) replication at the entry step in rhesus macaque cells. Virology 1996, 219:485-488. 10.1006/viro.1996.0276, 8638416.
4. Akari H, Mori K, Terao K, Otani I, Fukasawa M, Mukai R, Yoshikawa Y. In vitro immortalization of Old World monkey T lymphocytes with Herpesvirus saimiri: its susceptibility to infection with simian immunodeficiency viruses. Virology 1996, 218:382-388. 10.1006/viro.1996.0207, 8610465.
5. Akari H, Nam KH, Mori K, Otani I, Shibata H, Adachi A, Terao K, Yoshikawa Y. Effects of SIVmac infection on peripheral blood CD4+CD8+ T lymphocytes in cynomolgus macaques. Clin Immunol 1999, 91:321-329. 10.1006/clim.1999.4700, 10370378.
6. VandeWoude S, Apetrei C. Going wild: lessons from naturally occurring T-lymphotropic lentiviruses. Clin Microbiol Rev 2006, 19:728-762. 10.1128/CMR.00009-06, 1592692, 17041142.
7. Hahn BH, Shaw GM, De Cock KM, Sharp PM. AIDS as a zoonosis: scientific and public health implications. Science 2000, 287:607-614. 10.1126/science.287.5453.607, 10649986.
8. Castro BA, Nepomuceno M, Lerche NW, Eichberg JW, Levy JA. Persistent infection of baboons and rhesus monkeys with different strains of HIV-2. Virology 1991, 184:219-226. 10.1016/0042-6822(91)90838-3, 1678564.
9. Fujita M, Yoshida A, Sakurai A, Tatsuki J, Ueno F, Akari H, Adachi A. Susceptibility of HVS-immortalized lymphocytic HSC-F cells to various strains and mutants of HIV/SIV. Int J Mol Med 2003, 11:641-644.
10. Castro BA, Barnett SW, Evans LA, Moreau J, Odehouri K, Levy JA. Biologic heterogeneity of human immunodeficiency virus type 2 (HIV-2) strains. Virology 1990, 178:527-534. 10.1016/0042-6822(90)90350-Z, 2120848.
11. Locher CP, Witt SA, Herndier BG, Abbey NW, Tenner-Racz K, Racz P, Kiviat NB, Murthy KK, Brasky K, Leland M, Levy JA. Increased virus replication and virulence after serial passage of human immunodeficiency virus type 2 in baboons. J Virol 2003, 77:77-83. 10.1128/JVI.77.1.77-83.2003, 140565, 12477812.
12. Locher CP, Blackbourn DJ, Herndier BG, Reyes-Teran G, Barnett SW, Murthy KK, Levy JA. Transient virus infection and pathogenesis of a new HIV type 2 isolate, UC12, in baboons. AIDS Res Hum Retroviruses 1998, 14:79-82. 10.1089/aid.1998.14.79, 9453254.
13. Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 2004, 427:848-853. 10.1038/nature02343, 14985764.
14. Nakayama EE, Miyoshi H, Nagai Y, Shioda T. A specific region of 37 amino acid residues in the SPRY (B30.2) domain of African green monkey TRIM5alpha determines species-specific restriction of simian immunodeficiency virus SIVmac infection. J Virol 2005, 79:8870-8877. 10.1128/JVI.79.14.8870-8877.2005, 1168783, 15994780.
15. Hatziioannou T, Perez-Caballero D, Yang A, Cowan S, Bieniasz PD. Retrovirus resistance factors Ref1 and Lv1 are species-specific variants of TRIM5alpha. Proc Natl Acad Sci USA 2004, 101:10774-10779. 10.1073/pnas.0402361101, 490010, 15249685.
16. Keckesova Z, Ylinen LM, Towers GJ. The human and African green monkey TRIM5alpha genes encode Ref1 and Lv1 retroviral restriction factor activities. Proc Natl Acad Sci USA 2004, 101:10780-10785. 10.1073/pnas.0402474101, 490011, 15249687.
17. Perron MJ, Stremlau M, Song B, Ulm W, Mulligan RC, Sodroski J. TRIM5alpha mediates the postentry block to N-tropic murine leukemia viruses in human cells. Proc Natl Acad Sci USA 2004, 101:11827-11832. 10.1073/pnas.0403364101, 511059, 15280539.
18. Reymond A, Meroni G, Fantozzi A, Merla G, Cairo S, Luzi L, Riganelli D, Zanaria E, Messali S, Cainarca S, Guffanti A, Minucci S, Pelicci PG, Ballabio A. The tripartite motif family identifies cell compartments. Embo J 2001, 20:2140-2151. 10.1093/emboj/20.9.2140, 125245, 11331580.
19. Jackson PK, Eldridge AG, Freed E, Furstenthal L, Hsu JY, Kaiser BK, Reimann JD. The lore of the RINGs: substrate recognition and catalysis by ubiquitin ligases. Trends Cell Biol 2000, 10:429-439. 10.1016/S0962-8924(00)01834-1, 10998601.
20. Anderson JL, Campbell EM, Wu X, Vandegraaff N, Engelman A, Hope TJ. Proteasome inhibition reveals that a functional preintegration complex intermediate can be generated during restriction by diverse TRIM5 proteins. J Virol 2006, 80:9754-9760. 10.1128/JVI.01052-06, 1617233, 16973579.
21. Wu X, Anderson JL, Campbell EM, Joseph AM, Hope TJ. Proteasome inhibitors uncouple rhesus TRIM5alpha restriction of HIV-1 reverse transcription and infection. Proc Natl Acad Sci USA 2006, 103:7465-7470. 10.1073/pnas.0510483103, 1464362, 16648264.
22. Maegawa H, Miyamoto T, Sakuragi J, Shioda T, Nakayama EE. Contribution of RING domain to retrovirus restriction by TRIM5alpha depends on combination of host and virus. Virology 2010, 399:212-220. 10.1016/j.virol.2010.01.003, 20110098.
23. Javanbakht H, Diaz-Griffero F, Stremlau M, Si Z, Sodroski J. The contribution of RING and B-box 2 domains to retroviral restriction mediated by monkey TRIM5alpha. J Biol Chem 2005, 280:26933-26940. 10.1074/jbc.M502145200, 15897199.
24. Diaz-Griffero F, Kar A, Perron M, Xiang SH, Javanbakht H, Li X, Sodroski J. Modulation of retroviral restriction and proteasome inhibitor-resistant turnover by changes in the TRIM5alpha B-box 2 domain. J Virol 2007, 81:10362-10378. 10.1128/JVI.00703-07, 2045480, 17626085.
25. Kar AK, Diaz-Griffero F, Li Y, Li X, Sodroski J. Biochemical and biophysical characterization of a chimeric TRIM21-TRIM5alpha protein. J Virol 2008, 82:11669-11681. 10.1128/JVI.01559-08, 2583655, 18799572.
26. Langelier CR, Sandrin V, Eckert DM, Christensen DE, Chandrasekaran V, Alam SL, Aiken C, Olsen JC, Kar AK, Sodroski JG, Sundquist WI. Biochemical characterization of a recombinant TRIM5alpha protein that restricts human immunodeficiency virus type 1 replication. J Virol 2008, 82:11682-11694. 10.1128/JVI.01562-08, 2583683, 18799573.
27. Li X, Sodroski J. The TRIM5alpha B-box 2 domain promotes cooperative binding to the retroviral capsid by mediating higher-order self-association. J Virol 2008, 82:11495-11502. 10.1128/JVI.01548-08, 2583650, 18799578.
28. Diaz-Griffero F, Qin XR, Hayashi F, Kigawa T, Finzi A, Sarnak Z, Lienlaf M, Yokoyama S, Sodroski J. A B-box 2 Surface Patch Important for TRIM5{alpha} Self-Association, Capsid-binding Avidity and Retrovirus Restriction. J Virol 2009, 83:10737-51. 10.1128/JVI.01307-09, 2753111, 19656869.
29. Mische CC, Javanbakht H, Song B, Diaz-Griffero F, Stremlau M, Strack B, Si Z, Sodroski J. Retroviral restriction factor TRIM5alpha is a trimer. J Virol 2005, 79:14446-14450. 10.1128/JVI.79.22.14446-14450.2005, 1280198, 16254380.
30. Javanbakht H, Yuan W, Yeung DF, Song B, Diaz-Griffero F, Li Y, Li X, Stremlau M, Sodroski J. Characterization of TRIM5alpha trimerization and its contribution to human immunodeficiency virus capsid binding. Virology 2006, 353:234-246. 10.1016/j.virol.2006.05.017, 16808955.
31. Nakayama EE, Maegawa H, Shioda T. A dominant-negative effect of cynomolgus monkey tripartite motif protein TRIM5alpha on anti-simian immunodeficiency virus SIVmac activity of an African green monkey orthologue. Virology 2006, 350:158-163. 10.1016/j.virol.2006.03.035, 16647098.
32. Perez-Caballero D, Hatziioannou T, Yang A, Cowan S, Bieniasz PD. Human tripartite motif 5alpha domains responsible for retrovirus restriction activity and specificity. J Virol 2005, 79:8969-8978. 10.1128/JVI.79.14.8969-8978.2005, 1168745, 15994791.
33. Sawyer SL, Wu LI, Emerman M, Malik HS. Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc Natl Acad Sci USA 2005, 102:2832-2837. 10.1073/pnas.0409853102, 549489, 15689398.
34. Kono K, Song H, Shingai Y, Shioda T, Nakayama EE. Comparison of anti-viral activity of rhesus monkey and cynomolgus monkey TRIM5alphas against human immunodeficiency virus type 2 infection. Virology 2008, 373:447-456. 10.1016/j.virol.2007.12.022, 18201746.
35. Ohkura S, Yap MW, Sheldon T, Stoye JP. All three variable regions of the TRIM5alpha B30.2 domain can contribute to the specificity of retrovirus restriction. J Virol 2006, 80:8554-8565. 10.1128/JVI.00688-06, 1563890, 16912305.
36. Kono K, Bozek K, Domingues FS, Shioda T, Nakayama EE. Impact of a single amino acid in the variable region 2 of the Old World monkey TRIM5alpha SPRY (B30.2) domain on anti-human immunodeficiency virus type 2 activity. Virology 2009, 388:160-168. 10.1016/j.virol.2009.03.004, 19342071.
37. Perron MJ, Stremlau M, Sodroski J. Two surface-exposed elements of the B30.2/SPRY domain as potency determinants of N-tropic murine leukemia virus restriction by human TRIM5alpha. J Virol 2006, 80:5631-5636. 10.1128/JVI.00219-06, 1472168, 16699044.
38. Yap MW, Nisole S, Stoye JP. A single amino acid change in the SPRY domain of human Trim5alpha leads to HIV-1 restriction. Curr Biol 2005, 15:73-78. 10.1016/j.cub.2004.12.042, 15649369.
39. Stremlau M, Perron M, Welikala S, Sodroski J. Species-specific variation in the B30.2(SPRY) domain of TRIM5alpha determines the potency of human immunodeficiency virus restriction. J Virol 2005, 79:3139-3145. 10.1128/JVI.79.5.3139-3145.2005, 548447, 15709033.
40. Sebastian S, Luban J. TRIM5alpha selectively binds a restriction-sensitive retroviral capsid. Retrovirology 2005, 2:40. 10.1186/1742-4690-2-40, 1166576, 15967037.
41. Stremlau M, Perron M, Lee M, Li Y, Song B, Javanbakht H, Diaz-Griffero F, Anderson DJ, Sundquist WI, Sodroski J. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. Proc Natl Acad Sci USA 2006, 103:5514-5519. 10.1073/pnas.0509996103, 1459386, 16540544.
42. Ylinen LM, Keckesova Z, Wilson SJ, Ranasinghe S, Towers GJ. Differential restriction of human immunodeficiency virus type 2 and simian immunodeficiency virus SIVmac by TRIM5alpha alleles. J Virol 2005, 79:11580-11587. 10.1128/JVI.79.18.11580-11587.2005, 1212619, 16140735.
43. Shibata R, Miura T, Hayami M, Ogawa K, Sakai H, Kiyomasu T, Ishimoto A, Adachi A. Mutational analysis of the human immunodeficiency virus type 2 (HIV-2) genome in relation to HIV-1 and simian immunodeficiency virus SIV (AGM). J Virol 1990, 64:742-747. 249168, 2296082.
44. Song H, Nakayama EE, Yokoyama M, Sato H, Levy JA, Shioda T. A single amino acid of the human immunodeficiency virus type 2 capsid affects its replication in the presence of cynomolgus monkey and human TRIM5alphas. J Virol 2007, 81:7280-7285. 10.1128/JVI.00406-07, 1933286, 17475650.
45. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 1989, 77:51-59. 10.1016/0378-1119(89)90358-2, 2744487.
46. Gyuris A, Vajda G, Foldes I. Establishment of an MT4 cell line persistently producing infective HIV-1 particles. Acta Microbiol Hung 1992, 39:271-279.
47. Kuroishi A, Saito A, Shingai Y, Shioda T, Nomaguchi M, Adachi A, Akari H, Nakayama EE. Modification of a loop sequence between alpha-helices 6 and 7 of virus capsid (CA) protein in a human immunodeficiency virus type 1 (HIV-1) derivative that has simian immunodeficiency virus (SIVmac239) vif and CA alpha-helices 4 and 5 loop improves replication in cynomolgus monkey cells. Retrovirology 2009, 6:70. 10.1186/1742-4690-6-70, 2731049, 19650891.
48. Price AJ, Marzetta F, Lammers M, Ylinen LM, Schaller T, Wilson SJ, Towers GJ, James LC. Active site remodeling switches HIV specificity of antiretroviral TRIMCyp. Nat Struct Mol Biol 2009, 16:1036-1042. 10.1038/nsmb.1667, 19767750.
49. Gamble TR, Yoo S, Vajdos FF, von Schwedler UK, Worthylake DK, Wang H, McCutcheon JP, Sundquist WI, Hill CP. Structure of the carboxyl-terminal dimerization domain of the HIV-1 capsid protein. Science 1997, 278:849-853. 10.1126/science.278.5339.849, 9346481.
50. Pornillos O, Ganser-Pornillos BK, Kelly BN, Hua Y, Whitby FG, Stout CD, Sundquist WI, Hill CP, Yeager M. X-ray structures of the hexameric building block of the HIV capsid. Cell 2009, 137:1282-1292. 10.1016/j.cell.2009.04.063, 2840706, 19523676.
51. Deshpande N, Addess KJ, Bluhm WF, Merino-Ott JC, Townsend-Merino W, Zhang Q, Knezevich C, Xie L, Chen L, Feng Z, Green RK, Flippen-Anderson JL, Westbrook J, Berman HM, Bourne PE. The RCSB Protein Data Bank: a redesigned query system and relational database based on the mmCIF schema. Nucleic Acids Res 2005, 33:D233-237. 10.1093/nar/gki057, 540011, 15608185.
52. Shirakawa K, Takaori-Kondo A, Yokoyama M, Izumi T, Matsui M, Io K, Sato T, Sato H, Uchiyama T. Phosphorylation of APOBEC3G by protein kinase A regulates its interaction with HIV-1 Vif. Nat Struct Mol Biol 2008, 15:1184-1191. 10.1038/nsmb.1497, 18836454.
53. Labute P. The generalized Born/volume integral implicit solvent model: estimation of the free energy of hydration using London dispersion instead of atomic surface area. J Comput Chem 2008, 29:1693-1698. 10.1002/jcc.20933, 18307169.
54. Ponder JW, Case DA. Force fields for protein simulations. Adv Protein Chem 2003, 66:27-85. full_text, 14631816.
55. Onufriev A, Bashford D, Case DA. Modification of the generalized Born model suitable for macromolecules. Journal of Physical Chemistry B 2000, 104:3712-3720.
56. Onyangoa C, Leligdowicz A, Yokoyamac M, Sato H, Song H, Nakayama EE, Shioda T, Silva T, Townenda J, Jayea A, Whittle H, Rowland-Jones S, Cotten M. HIV-2 capsids distinguish high and low virus load patients in a West African community cohort. Vaccine 2010, 28S2:60-67.
57. Braaten D, Franke EK, Luban J. Cyclophilin A is required for the replication of group M human immunodeficiency virus type 1 (HIV-1) and simian immunodeficiency virus SIV(CPZ)GAB but not group O HIV-1 or other primate immunodeficiency viruses. J Virol 1996, 70:4220-4227. 190352, 8676442.
58. Besnier C, Takeuchi Y, Towers G. Restriction of lentivirus in monkeys. Proc Natl Acad Sci USA 2002, 99:11920-11925. 10.1073/pnas.172384599, 129369, 12154231.
59. Cowan S, Hatziioannou T, Cunningham T, Muesing MA, Gottlinger HG, Bieniasz PD. Cellular inhibitors with Fv1-like activity restrict human and simian immunodeficiency virus tropism. Proc Natl Acad Sci USA 2002, 99:11914-11919. 10.1073/pnas.162299499, 129368, 12154227.
60. Hatziioannou T, Cowan S, Goff SP, Bieniasz PD, Towers GJ. Restriction of multiple divergent retroviruses by Lv1 and Ref1. EMBO J 2003, 22:385-394. 10.1093/emboj/cdg042, 140727, 12554640.
61. Kootstra NA, Munk C, Tonnu N, Landau NR, Verma IM. Abrogation of postentry restriction of HIV-1-based lentiviral vector transduction in simian cells. Proc Natl Acad Sci USA 2003, 100:1298-1303. 10.1073/pnas.0337541100, 298767, 12547912.
62. Owens CM, Song B, Perron MJ, Yang PC, Stremlau M, Sodroski J. Binding and susceptibility to postentry restriction factors in monkey cells are specified by distinct regions of the human immunodeficiency virus type 1 capsid. J Virol 2004, 78:5423-5437. 10.1128/JVI.78.10.5423-5437.2004, 400345, 15113921.
63. Lin TY, Emerman M. Determinants of cyclophilin A-dependent TRIM5 alpha restriction against HIV-1. Virology 2008, 379:335-341. 10.1016/j.virol.2008.06.037, 2615586, 18678385.
64. Hatziioannou T, Princiotta M, Piatak M, Yuan F, Zhang F, Lifson JD, Bieniasz PD. Generation of simian-tropic HIV-1 by restriction factor evasion. Science 2006, 314:95. 10.1126/science.1130994, 17023652.
65. Berthoux L, Sebastian S, Sokolskaja E, Luban J. Cyclophilin A is required for TRIM5{alpha}-mediated resistance to HIV-1 in Old World monkey cells. Proc Natl Acad Sci USA 2005, 102:14849-14853. 10.1073/pnas.0505659102, 1239943, 16203999.
66. Keckesova Z, Ylinen LM, Towers GJ. Cyclophilin A renders human immunodeficiency virus type 1 sensitive to Old World monkey but not human TRIM5 alpha antiviral activity. J Virol 2006, 80:4683-4690. 10.1128/JVI.80.10.4683-4690.2006, 1472055, 16641261.
67. Sokolskaja E, Berthoux L, Luban J. Cyclophilin A and TRIM5alpha independently regulate human immunodeficiency virus type 1 infectivity in human cells. J Virol 2006, 80:2855-2862. 10.1128/JVI.80.6.2855-2862.2006, 1395419, 16501094.
68. Stremlau M, Song B, Javanbakht H, Perron M, Sodroski J. Cyclophilin A: an auxiliary but not necessary cofactor for TRIM5alpha restriction of HIV-1. Virology 2006, 351:112-120. 10.1016/j.virol.2006.03.015, 16643975.
69. Khorasanizadeh S, Campos-Olivas R, Clark CA, Summers MF. Sequence-specific 1H, 13C and 15N chemical shift assignment and secondary structure of the HTLV-I capsid protein. Journal of biomolecular NMR 1999, 14:199-200. 10.1023/A:1008307507462, 10427751.
70. Jin Z, Jin L, Peterson DL, Lawson CL. Model for lentivirus capsid core assembly based on crystal dimers of EIAV p26. J Mol Biol 1999, 286:83-93. 10.1006/jmbi.1998.2443, 9931251.
71. Mortuza GB, Dodding MP, Goldstone DC, Haire LF, Stoye JP, Taylor IA. Structure of B-MLV capsid amino-terminal domain reveals key features of viral tropism, gag assembly and core formation. J Mol Biol 2008, 376:1493-1508. 10.1016/j.jmb.2007.12.043, 18222469.
72. Mortuza GB, Goldstone DC, Pashley C, Haire LF, Palmarini M, Taylor WR, Stoye JP, Taylor IA. Structure of the capsid amino-terminal domain from the betaretrovirus, Jaagsiekte sheep retrovirus. J Mol Biol 2009, 386:1179-1192. 10.1016/j.jmb.2008.10.066, 19007792.
73. Kinomoto M, Appiah-Opong R, Brandful JA, Yokoyama M, Nii-Trebi N, Ugly-Kwame E, Sato H, Ofori-Adjei D, Kurata T, Barre-Sinoussi F, Sata T, Tokunaga K. HIV-1 proteases from drug-naive West African patients are differentially less susceptible to protease inhibitors. Clin Infect Dis 2005, 41:243-251. 10.1086/431197, 15983923.
74. Kinomoto M, Yokoyama M, Sato H, Kojima A, Kurata T, Ikuta K, Sata T, Tokunaga K. Amino acid 36 in the human immunodeficiency virus type 1 gp41 ectodomain controls fusogenic activity: implications for the molecular mechanism of viral escape from a fusion inhibitor. J Virol 2005, 79:5996-6004. 10.1128/JVI.79.10.5996-6004.2005, 1091722, 15857986.