Generation of rhesus macaque-tropic HIV-1 clones that are resistant to major anti-HIV-1 restriction factors

Journal of Virology

Volumn 87, Issue 21, 2013, Pages 11447-11461

  Nomaguchi, Masako ^a   Yokoyama, Masaru ^b   Kono, Ken ^c   Nakayama, Emi E ^c   Shioda, Tatsuo ^c   Doi, Naoya ^a,d   Fujiwara, Sachi ^a   Saito, Akatsuki ^d,e   Akari, Hirofumi ^e   Miyakawa, Kei ^d,f   Ryo, Akihide ^f   Ode, Hirotaka ^d,g   Iwatani, Yasumasa ^g   Miura, Tomoyuki ^h   Igarashi, Tatsuhiko ^h   Sato, Hironori ^a,b   Adachi, Akio ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d The Japan Foundation   (Japan)

^e KYOTO UNIVERSITY   (Japan)

^f YOKOHAMA CITY UNIVERSITY   (Japan)

^g NATIONAL HOSPITAL ORGANIZATION NAGOYA MEDICAL CENTER   (Japan)

^h KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; GAG PROTEIN; TRIPARTITE MOTIF PROTEIN 5; VPU PROTEIN;

ALLELE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CELL LINE; CLONE; CONTROLLED STUDY; CORRELATION ANALYSIS; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN STRUCTURE; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; VIROGENESIS; VIRUS CAPSID; VIRUS REPLICATION;

ANIMALS; CELLS, CULTURED; GENE PRODUCTS, GAG; HIV-1; HUMAN IMMUNODEFICIENCY VIRUS PROTEINS; HUMANS; LEUKOCYTES, MONONUCLEAR; MACACA MULATTA; MUTANT PROTEINS; VIRAL REGULATORY AND ACCESSORY PROTEINS; VIRAL TROPISM; VIRUS REPLICATION;

EID: 84886900821     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01549-13     Document Type: Article

References (73)

1. KirchhoffF. 2010. Immune evasion and counteraction of restriction factors by HIV-1 and other primate lentiviruses. Cell Host Microbe 8:55-67.
2. Sharp PM, Hahn BH. 2011. Origins of HIV and the AIDS pandemic. Cold Spring Harb. Perspect. Med. 1:a006841.
3. Shibata R, Sakai H, Kawamura M, Tokunaga K, Adachi A. 1995. Early replication block of human immunodeficiency virus type 1 in monkey cells. J. Gen. Virol. 76:2723-2730.
4. Blanco-Melo D, Venkatesh S, Bieniasz PD. 2012. Intrinsic cellular defenses against human immunodeficiency viruses. Immunity 37:399-411.
5. Harris RS, Hultquist JF, Evans DT. 2012. The restriction factors of human immunodeficiency virus. J. Biol. Chem. 287:40875-40883.
6. Malim MH, Bieniasz PD. 2012. HIV restriction factors and mechanisms of evasion. Cold Spring Harb. Perspect. Med. 2:a006940. doi:10.1101/cshperspect.a006940.
7. Hatziioannou T, Evans DT. 2012. Animal models for HIV/AIDS research. Nat. Rev. Microbiol. 10:852-867.
8. Nomaguchi M, Doi N, Fujiwara S, Adachi A. 2011. Macaque-tropic HIV-1 derivatives: a novel experimental approach to understand viral replication and evolution in vivo, p 325-348. In Chang T.Y.-L. (ed), HIVhost interactions. InTech, Rijeka, Croatia. http://www.intechopen.com/books/hiv-host-interactions/macaque-tropic-hiv-1-derivatives-a-novel-experimental-approach-to-understand-viral-replication-and-e.
9. Shedlock DJ, Silvestri G, Weiner DB. 2009. Monkeying around with HIV vaccines: using rhesus macaques to define 'gatekeepers' for clinical trials. Nat. Rev. Immunol. 9:717-728.
10. Nomaguchi M, Doi N, Matsumoto Y, Sakai Y, Fujiwara S, Adachi A. 2012. Species tropism of HIV-1 modulated by viral accessory proteins. Front. Microbiol. 3:267. doi:10.3389/fmicb.2012.00267.
11. Holmes RK, Malim MH, Bishop KN. 2007. APOBEC-mediated viral restriction: not simply editing? Trends Biochem. Sci. 32:118-128.
12. Malim MH, Emerman M. 2008. HIV-1 accessory proteins- ensuring viral survival in a hostile environment. Cell Host Microbe 3:388-398.
13. Grütter MG, Luban J. 2012. TRIM5 structure, HIV-1 capsid recognition, and innate immune signaling. Curr. Opin. Virol. 2:142-150.
14. Nakayama EE, Shioda T. 2010. Anti-retroviral activity of TRIM5 alpha. Rev. Med. Virol. 20:77-92.
15. Douglas JL, Gustin JK, Viswanathan K, Mansouri M, Moses AV, Früh K. 2010. The great escape: viral strategies to counter BST-2/tetherin. PLoS Pathog. 6:e1000913. doi:10.1371/journal.ppat.1000913.
16. Hatziioannou T, Ambrose Z, Chung NP, Piatak M, Jr, Yuan F, Trubey CM, Coalter V, Kiser R, Schneider D, Smedley J, Pung R, Gathuka M, Estes JD, Veazey RS, KewalRamani VN, Lifson JD, Bieniasz PD. 2009. A macaque model of HIV-1 infection. Proc. Natl. Acad. Sci. U. S. A. 106: 4425-4429.
17. Hatziioannou T, Princiotta M, Piatak M, Jr, Yuan F, Zhang F, Lifson JD, Bieniasz PD. 2006. Generation of simian-tropic HIV-1 by restriction factor evasion. Science 314:95. doi:10.1126/science.1130994.
18. Kamada K, Igarashi T, Martin MA, Khamsri B, Hatcho K, Yamashita T, Fujita M, Uchiyama T, Adachi A. 2006. Generation of HIV-1 derivatives that productively infect macaque monkey lymphoid cells. Proc. Natl. Acad. Sci. U. S. A. 103:16959-16964.
19. Nomaguchi M, Yokoyama M, Kono K, Nakayama EE, Shioda T, Saito A, Akari H, Yasutomi Y, Matano T, Sato H, Adachi A. 2013. Gag-CA Q110D mutation elicits TRIM5-independent enhancement of HIV-1mt replication in macaque cells. Microbes Infect. 15:56-65.
20. Saito A, Nomaguchi M, Iijima S, Kuroishi A, Yoshida T, Lee YJ, Hayakawa T, Kono K, Nakayama EE, Shioda T, Yasutomi Y, Adachi A, Matano T, Akari H. 2011. Improved capacity of a monkey-tropic HIV-1 derivative to replicate in cynomolgus monkeys with minimal modifications. Microbes Infect. 13:58-64.
21. Thippeshappa R, Polacino P, Yu Kimata MT, Siwak EB, Anderson D, Wang W, Sherwood L, Arora R, Wen M, Zhou P, Hu SL, Kimata JT. 2011. Vif substitution enables persistent infection of pig-tailed macaques by human immunodeficiency virus type 1. J. Virol. 85:3767-3779.
22. Shingai M, Yoshida T, Martin MA, Strebel K. 2011. Some human immunodeficiency virus type 1 Vpu proteins are able to antagonize macaque BST-2 in vitro and in vivo: Vpu-negative simian-human immunodeficiency viruses are attenuated in vivo. J. Virol. 85:9708-9715.
23. Bitzegeio J, Sampias M, Bieniasz PD, Hatziioannou T. 2013. Adaptation to the interferon-induced antiviral state by human and simian immunodeficiency viruses. J. Virol. 87:3549-3560.
24. Saito A, Nomaguchi M, Kono K, Iwatani Y, Yokoyama M, Yasutomi Y, Sato H, Shioda T, Sugiura W, Matano T, Adachi A, Nakayama E, Akari H. 2013. TRIM5 genotypes in cynomolgus monkeys primarily influence inter-individual diversity in susceptibility to monkey-tropic human immunodeficiency virus type 1. J. Gen. Virol. 94:1318-1324.
25. Doi N, Fujiwara S, Adachi A, Nomaguchi M. 2011. Rhesus M1.3S cells suitable for biological evaluation of macaque-tropic HIV/SIV clones. Front. Microbiol. 2:115. doi:10.3389/fmicb.2011.00115.
26. Sauter D, Schindler M, Specht A, Landford WN, Münch J, Kim KA, Votteler J, Schubert U, Bibollet-Ruche F, Keele BF, Takehisa J, Ogando Y, Ochsenbauer C, Kappes JC, Ayouba A, Peeters M, Learn GH, Shaw G, Sharp PM, Bieniasz P, Hahn BH, Hatziioannou T, KirchhoffF. 2009. Tetherin-driven adaptation of Vpu and Nef function and the evolution of pandemic and nonpandemic HIV-1 strains. Cell Host Microbe 6:409-421.
27. Lebkowski JS, Clancy S, Calos MP. 1985. Simian virus 40 replication in adenovirus-transformed human cells antagonizes gene expression. Nature 317:169-171.
28. Kimpton J, Emerman M. 1992. Detection of replication-competent and pseudotyped human immunodeficiency virus with a sensitive cell line on the basis of activation of an integrated beta-galactosidase gene. J. Virol. 66:2232-2239.
29. Nomaguchi M, Doi N, Fujiwara S, Fujita M, Adachi A. 2010. Site-directed mutagenesis of HIV-1 vpu gene demonstrates two clusters of replication-defective mutants with distinct ability to down-modulate cell surface CD4 and tetherin. Front. Microbiol. 1:116. doi:10.3389/fmicb.2010.00116.
30. McNatt MW, Zang T, Hatziioannou T, Bartlett M, Fofana IB, Johnson WE, Neil SJ, Bieniasz PD. 2009. Species-specific activity of HIV-1 Vpu and positive selection of tetherin transmembrane domain variants. PLoS Pathog. 5:e1000300. doi:10.1371/journal.ppat.1000300.
31. Yoshida T, Kao S, Strebel K. 2011. Identification of residues in the BST-2TM domain important for antagonism by HIV-1 Vpu using a gain-of-function approach. Front. Microbiol. 2:35. doi:10.3389/fmicb.2011.00035.
32. Adachi A, Gendelman HE, Koenig S, Folks T, Willey R, Rabson A, Martin MA. 1986. Production of acquired immunodeficiency syndromeassociated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59:284-291.
33. Willey RL, Smith DH, Lasky LA, Theodore TS, Earl PL, Moss B, Capon DJ, Martin MA. 1988. In vitro mutagenesis identifies a region within the envelope gene of the human immunodeficiency virus that is critical for infectivity. J. Virol. 62:139-147.
34. O'Doherty U, Swiggard WJ, Malim MH. 2000. Human immunodeficiency virus type 1 spinoculation enhances infection through virus binding. J. Virol. 74:10074-10080.
35. Wilson SJ, Webb BL, Ylinen LM, Verschoor E, Heeney JL, Towers GJ. 2008. Independent evolution of an antiviral TRIMCyp in rhesus macaques. Proc. Natl. Acad. Sci. U. S. A. 105:3557-3562.
36. Kono K, Song H, Yokoyama M, Sato H, Shioda T, Nakayama EE. 2010. Multiple sites in the N-terminal half of simian immunodeficiency virus capsid protein contribute to evasion from rhesus monkey TRIM5α-mediated restriction. Retrovirology 7:72. doi:10.1186/1742-4690-7-72.
37. Howard BR, Vajdos FF, Li S, Sundquist WI, Hill CP. 2003. Structural insights into the catalytic mechanism of cyclophilin A. Nat. Struct. Biol. 10:475-481.
38. Park SH, Mrse AA, Nevzorov AA, Mesleh MF, Oblatt-Montal M, Montal M, Opella SJ. 2003. Three-dimensional structure of the channelforming trans-membrane domain of virus protein "u" (Vpu) from HIV-1. J. Mol. Biol. 333:409-424.
39. Leaver-Fay A, Tyka M, Lewis SM, Lange OF, Thompson J, Jacak R, Kaufman K, Renfrew PD, Smith CA, Sheffler W, Davis IW, Cooper S, Treuille A, Mandell DJ, Richter F, Ban YE, Fleishman SJ, Corn JE, Kim DE, Lyskov S, Berrondo M, Mentzer S, Popović Z, Havranek JJ, Karanicolas J, Das R, Meiler J, Kortemme T, Gray JJ, Kuhlman B, Baker D, Bradley P. 2011. ROSETTA3: an object-oriented software suite for the simulation and design of macromolecules. Methods Enzymol. 487:545-574.
40. Kirmaier A, Wu F, Newman RM, Hall LR, Morgan JS, O'Connor S, Marx PA, Meythaler M, Goldstein S, Buckler-White A, Kaur A, Hirsch VM, Johnson WE. 2010. TRIM5 suppresses cross-species transmission of a primate immunodeficiency virus and selects for emergence of resistant variants in the new species. PLoS Biol. 8:e1000462. doi:10.1371/journal.pbio.1000462.
41. Newman RM, Hall L, Connole M, Chen GL, Sato S, Yuste E, Diehl W, Hunter E, Kaur A, Miller GM, Johnson WE. 2006. Balancing selection and the evolution of functional polymorphism in Old World monkey TRIM5alpha. Proc. Natl. Acad. Sci. U. S. A. 103:19134-19139.
42. Price AJ, Marzetta F, Lammers M, Ylinen LM, Schaller T, Wilson SJ, Towers GJ, James LC. 2009. Active site remodeling switches HIV specificity of antiretroviral TRIMCyp. Nat. Struct. Mol. Biol. 16:1036-1042.
43. Ylinen LM, Price AJ, Rasaiyaah J, Hué S, Rose NJ, Marzetta F, James LC, Towers GJ. 2010. Conformational adaptation of Asian macaque TRIMCyp directs lineage specific antiviral activity. PLoS Pathog. 6:e1001062. doi:10.1371/journal.ppat.1001062.
44. Fassati A. 2012. Multiple roles of the capsid protein in the early steps of HIV-1 infection. Virus Res. 170:15-24.
45. Ganser-Pornillos BK, Yeager M, Sundquist WI. 2008. The structural biology of HIV assembly. Curr. Opin. Struct. Biol. 18:203-217.
46. Miyamoto T, Yokoyama M, Kono K, Shioda T, Sato H, Nakayama EE. 2011. A single amino acid of human immunodeficiency virus type 2 capsid protein affects conformation of two external loops and viral sensitivity to TRIM5α. PLoS One 6:e22779. doi:10.1371/journal.pone.0022779.
47. Nomaguchi M, Doi N, Fujiwara S, Saito A, Akari H, Nakayama EE, Shioda T, Yokoyama M, Sato H, Adachi A. 2013. Systemic biological analysis of the mutations in two distinct HIV-1mt genomes occurred during replication in macaque cells. Microbes Infect. 15:319-328.
48. Hatziioannou T, Cowan S, Von Schwedler UK, Sundquist WI, Bieniasz PD. 2004. Species-specific tropism determinants in the human immunodeficiency virus type 1 capsid. J. Virol. 78:6005-6012.
49. Owens CM, Song B, Perron MJ, Yang PC, Stremlau M, Sodroski J. 2004. 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. 78:5423-5437.
50. von Schwedler UK, Stray KM, Garrus JE, Sundquist WI. 2003. Functional surfaces of the human immunodeficiency virus type 1 capsid protein. J. Virol. 77:5439-5450.
51. Lim SY, Rogers T, Chan T, Whitney JB, Kim J, Sodroski J, Letvin NL. 2010. TRIM5alpha modulates immunodeficiency virus control in rhesus monkeys. PLoS Pathog. 6:e1000738. doi:10.1371/journal.ppat.1000738.
52. Jia B, Serra-Moreno R, Neidermyer W, Rahmberg A, Mackey J, Fofana IB, Johnson WE, Westmoreland S, Evans DT. 2009. Species-specific activity of SIV Nef and HIV-1 Vpu in overcoming restriction by tetherin/BST2. PLoS Pathog. 5:e1000429. doi:10.1371/journal.ppat.1000429.
53. Zhang F, Wilson SJ, Landford WC, Virgen B, Gregory D, Johnson MC, Munch J, KirchhoffF, Bieniasz PD, Hatziioannou T. 2009. Nef proteins from simian immunodeficiency viruses are tetherin antagonists. Cell Host Microbe 6:54-67.
54. Vigan R, Neil SJ. 2010. Determinants of tetherin antagonism in the transmembrane domain of the human immunodeficiency virus type 1 Vpu protein. J. Virol. 84:12958-12970.
55. McCarthy KR, Schmidt AG, Kirmaier A, Wyand AL, Newman RM, Johnson WE. 2013. Gain-of-sensitivity mutations in a Trim5-resistant primary isolate of pathogenic SIV identify two independent conserved determinants of Trim5α specificity. PLoS Pathog. 9:e1003352. doi:10.1371/journal.ppat.1003352.
56. Kuroishi A, Saito A, Shingai Y, Shioda T, Nomaguchi M, Adachi A, Akari H, Nakayama EE. 2009. 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 6:70. doi:10.1186/1742-4690-6-70.
57. Ohkura S, Goldstone DC, Yap MW, Holden-Dye K, Taylor IA, Stoye JP. 2011. Novel escape mutants suggest an extensive TRIM5α binding site spanning the entire outer surface of the murine leukemia virus capsid protein. PLoS Pathog. 7:e1002011. doi:10.1371/journal.ppat.1002011.
58. Homann S, Smith D, Little S, Richman D, Guatelli J. 2011. Upregulation of BST-2/tetherin by HIV infection in vivo. J. Virol. 85:10659-10668.
59. Liberatore RA, Bieniasz PD. 2011. Tetherin is a key effector of the antiretroviral activity of type I interferon in vitro and in vivo. Proc. Natl. Acad. Sci. U. S. A. 108:18097-18101.
60. Pillai SK, Abdel-Mohsen M, Guatelli J, Skasko M, Monto A, Fujimoto K, Yukl S, Greene WC, Kovari H, Rauch A, Fellay J, Battegay M, Hirschel B, Witteck A, Bernasconi E, Ledergerber B, Günthard HF, Wong JK, Swiss HIV Cohort Study. 2012. Role of retroviral restriction factors in the interferon-α-mediated suppression of HIV-1 in vivo. Proc. Natl. Acad. Sci. U. S. A. 109:3035-3040.
61. Serra-Moreno R, Jia B, Breed M, Alvarez X, Evans DT. 2011. Compensatory changes in the cytoplasmic tail of gp41 confer resistance to tetherin/BST-2 in a pathogenic nef-deleted SIV. Cell Host Microbe 9:46-57.
62. Goldstein S, Brown CR, Dehghani H, Lifson JD, Hirsch VM. 2000. Intrinsic susceptibility of rhesus macaque peripheral CD4(+) T cells to simian immunodeficiency virus in vitro is predictive of in vivo viral replication. J. Virol. 74:9388-9395.
63. Lifson JD, Nowak MA, Goldstein S, Rossio JL, Kinter A, Vasquez G, Wiltrout TA, Brown C, Schneider D, Wahl L, Lloyd AL, Williams J, Elkins WR, Fauci AS, Hirsch VM. 1997. The extent of early viral replication is a critical determinant of the natural history of simian immunodeficiency virus infection. J. Virol. 71:9508-9514.
64. Igarashi T, Iyengar R, Byrum RA, Buckler-White A, Dewar RL, Buckler CE, Lane HC, Kamada K, Adachi A, Martin MA. 2007. Human immunodeficiency virus type 1 derivative with 7% simian immunodeficiency virus genetic content is able to establish infections in pig-tailed macaques. J. Virol. 81:11549-11552.
65. Lifson JD, Haigwood NL. 2012. Lessons in nonhuman primate models for AIDS vaccine research: from minefields to milestones. Cold Spring Harb. Perspect. Med. 2:a007310. doi:10.1101/cshperspect.a007310.
66. Shaw GM, Hunter E. 2012. HIV transmission. Cold Spring Harb. Perspect. Med. 2:a006965. doi:10.1101/cshperspect.a006965.
67. Swanstrom R, Coffin J. 2012. HIV-1 pathogenesis: the virus. Cold Spring Harb. Perspect. Med. 2:a007443. doi:10.1101/cshperspect.a007443.
68. Nishimura Y, Shingai M, Willey R, Sadjadpour R, Lee WR, Brown CR, Brenchley JM, Buckler-White A, Petros R, Eckhaus M, Hoffman V, Igarashi T, Martin MA. 2010. Generation of the pathogenic R5-tropic simian/human immunodeficiency virus SHIVAD8 by serial passaging in rhesus macaques. J. Virol. 84:4769-4781.
69. Ren W, Mumbauer A, Gettie A, Seaman MS, Russell-Lodrigue K, Blanchard J, Westmoreland S, Cheng-Mayer C. 2013. Generation of lineage-related, mucosally transmissible subtype C R5 simian-human immunodeficiency viruses capable of AIDS development, induction of neurological disease, and coreceptor switching in rhesus macaques. J. Virol. 87:6137-6149.
70. Shingai M, Donau OK, Schmidt SD, Gautam R, Plishka RJ, Buckler-White A, Sadjadpour R, Lee WR, LaBranche CC, Montefiori DC, Mascola JR, Nishimura Y, Martin MA. 2012. Most rhesus macaques infected with the CCR5-tropic SHIVAD8 generate cross-reactive antibodies that neutralize multiple HIV-1 strains. Proc. Natl. Acad. Sci. U. S. A. 109:19769-19774.
71. Shibata R, Kawamura M, Sakai H, Hayami M, Ishimoto A, Adachi A. 1991. Generation of a chimeric human and simian immunodeficiency virus infectious to monkey peripheral blood mononuclear cells. J. Virol. 65:3514-3520.
72. Kawamura M, Sakai H, Adachi A. 1994. Human immunodeficiency virus Vpx is required for the early phase of replication in peripheral blood mononuclear cells. Microbiol. Immunol. 38:871-878.
73. Gamble TR, Vajdos FF, Yoo S, Worthylake DK, Houseweart M, Sundquist WI, Hill CP. 1996. Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell 87:1285-1294.