Development of a novel rhesus macaque model with an infectious R5 simian–human immunodeficiency virus encoding HIV-1 CRF08_BC env
Li Huang
Research Group of HIV Molecular Epidemiology and Virology, Center for Emerging Infectious Diseases, The State Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, China
Search for more papers by this authorShigeru Kusagawa
Laboratory of Virology and Diagnosis, AIDS Research Center, National Institute of Infectious Disease, Toyama, Tokyo, Japan
Search for more papers by this authorHaiyan Zeng
Research Group of HIV Molecular Epidemiology and Virology, Center for Emerging Infectious Diseases, The State Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, China
Search for more papers by this authorGuibo Yang
National Center for AIDS/STD Control and Prevention, China Center for Disease Prevention and Control, Beijing, China
Search for more papers by this authorBinlian Sun
Research Group of HIV Molecular Epidemiology and Virology, Center for Emerging Infectious Diseases, The State Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, China
Search for more papers by this authorTomoyuki Miura
Laboratory of Primate Model, Experimental Research Center for Infectious Diseases, Institute for Virus Research, Kyoto University, Kyoto, Japan
Search for more papers by this authorCorresponding Author
Rongge Yang
Research Group of HIV Molecular Epidemiology and Virology, Center for Emerging Infectious Diseases, The State Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, China
Correspondence
Rongge Yang, Research Group of HIV Molecular Epidemiology and Virology, Center for Emerging Infectious Diseases, The State Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Xiaohongshan 44, Wuhan 430071, China.
Tel.: +86 27 87198736;
fax: +86 27 87198736;
e-mail: [email protected]
Search for more papers by this authorLi Huang
Research Group of HIV Molecular Epidemiology and Virology, Center for Emerging Infectious Diseases, The State Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, China
Search for more papers by this authorShigeru Kusagawa
Laboratory of Virology and Diagnosis, AIDS Research Center, National Institute of Infectious Disease, Toyama, Tokyo, Japan
Search for more papers by this authorHaiyan Zeng
Research Group of HIV Molecular Epidemiology and Virology, Center for Emerging Infectious Diseases, The State Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, China
Search for more papers by this authorGuibo Yang
National Center for AIDS/STD Control and Prevention, China Center for Disease Prevention and Control, Beijing, China
Search for more papers by this authorBinlian Sun
Research Group of HIV Molecular Epidemiology and Virology, Center for Emerging Infectious Diseases, The State Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, China
Search for more papers by this authorTomoyuki Miura
Laboratory of Primate Model, Experimental Research Center for Infectious Diseases, Institute for Virus Research, Kyoto University, Kyoto, Japan
Search for more papers by this authorCorresponding Author
Rongge Yang
Research Group of HIV Molecular Epidemiology and Virology, Center for Emerging Infectious Diseases, The State Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, China
Correspondence
Rongge Yang, Research Group of HIV Molecular Epidemiology and Virology, Center for Emerging Infectious Diseases, The State Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Xiaohongshan 44, Wuhan 430071, China.
Tel.: +86 27 87198736;
fax: +86 27 87198736;
e-mail: [email protected]
Search for more papers by this authorAbstract
Background
The CRF08_BC strain is one of the most predominant circulating Human immunodeficiency virus type 1 (HIV-1) strains in the Chinese pandemic. A simian–human immunodeficiency virus (SHIV) encoding HIV-1 CRF08_BC env is highly desirable to evaluate candidate AIDS vaccines in non-human primates.
Methods
SHIV-KBQJ-12, which carries the envelope glycoprotein from QJ001, an infectious molecular clone of HIV-1 CRF08_BC, was generated. The replication capacity of SHIV-KBQJ-12 was determined both in human and rhesus macaque (Macaca mulatta) peripheral blood mononuclear cells (PBMCs) and in Chinese rhesus macaques.
Results
SHIV-KBQJ-12 replicated efficiently in human and macaque PBMCs and displayed a preference for CCR5 as an entry coreceptor. Productive infection of two macaques by intravenous inoculation with SHIV-KBQJ-12 was confirmed.
Conclusions
SHIV-KBQJ-12 is an R5-tropic chimeric virus that can establish productive infection both in vitro and in vivo in Chinese rhesus macaques and will be useful to assess candidate HIV-1 CRF08_BC vaccines in China.
References
- 1Rosenfield A: AIDS in South and Southeast Asia. Introduction and greeting. Presented at the observance of World AIDS Day, November 30, 2000 at the United Nations. AIDS Patient Care STDS 2001; 15: 425–6.
- 2Zhong P, Pan Q, Ning Z, Xue Y, Gong J, Zhen X, Zhou L, Sheng F, Zhang W, Gai J, Cheng H, Yue Q, Xing H, Zhuang M, Lu W, Shao Y, Kang L: Genetic diversity and drug resistance of human immunodeficiency virus type 1 (HIV-1) strains circulating in Shanghai. AIDS Res Hum Retroviruses 2007; 23: 847–56.
- 3Excler JL, Pitisuttithum P, Rerks-Ngarm S, Shao Y, Zhang L, Tamashiro H, Osmanov S: Expanding research capacity and accelerating AIDS vaccine development in Asia. Southeast Asian J Trop Med Public Health 2008; 39: 766–84.
- 4Vasan S, Schlesinger SJ, Chen Z, Hurley A, Lombardo A, Than S, Adesanya P, Bunce C, Boaz M, Boyle R, Sayeed E, Clark L, Dugin D, Boente-Carrera M, Schmidt C, Fang Q, Lei B, Huang Y, Zaharatos GJ, Gardiner DF, Caskey M, Seamons L, Ho M, Dally L, Smith C, Cox J, Gill D, Gilmour J, Keefer MC, Fast P, Ho DD: Phase 1 safety and immunogenicity evaluation of ADMVA, a multigenic, modified vaccinia Ankara-HIV-1 B’/C candidate vaccine. PLoS ONE 2010; 5: e8816.
- 5Akiyama H, Ishimatsu M, Miura T, Hayami M, Ido E: Construction and infection of a new simian/human immunodeficiency chimeric virus (SHIV) containing the integrase gene of the human immunodeficiency virus type 1 genome and analysis of its adaptation to monkey cells. Microbes Infect 2008; 10: 531–9.
- 6Barnett SW, Srivastava IK, Kan E, Zhou F, Goodsell A, Cristillo AD, Ferrai MG, Weiss DE, Letvin NL, Montefiori D, Pal R, Vajdy M: Protection of macaques against vaginal SHIV challenge by systemic or mucosal and systemic vaccinations with HIV-envelope. AIDS 2008; 22: 339–48.
- 7Chen Z, Huang Y, Zhao X, Skulsky E, Lin D, Ip J, Gettie A, Ho DD: Enhanced infectivity of an R5-tropic simian/human immunodeficiency virus carrying human immunodeficiency virus type 1 subtype C envelope after serial passages in pig-tailed macaques (Macaca nemestrina). J Virol 2000; 74: 6501–10.
- 8Cohen J: AIDS research. Vaccine studies stymied by shortage of animals. Science 2000; 287: 959–60.
- 9Feinberg MB, Moore JP: AIDS vaccine models: challenging challenge viruses. Nat Med 2002; 8: 207–10.
- 10Hsu M, Ho SH, Balfe P, Gettie A, Harouse J, Blanchard J, Cheng-Mayer C: A CCR5-tropic simian-HIV molecular clone capable of inducing AIDS in rhesus macaques. J Acquir Immune Defic Syndr 2005; 40: 383–7.
- 11Song RJ, Chenine AL, Rasmussen RA, Ruprecht CR, Mirshahidi S, Grisson RD, Xu W, Whitney JB, Goins LM, Ong H, Li PL, Shai-Kobiler E, Wang T, McCann CM, Zhang H, Wood C, Kankasa C, Secor WE, McClure HM, Strobert E, Else JG, Ruprecht RM: Molecularly cloned SHIV-1157ipd3N4: a highly replication- competent, mucosally transmissible R5 simian-human immunodeficiency virus encoding HIV clade C Env. J Virol 2006; 80: 8729–38.
- 12Joag SV, Li Z, Foresman L, Stephens EB, Zhao LJ, Adany I, Pinson DM, McClure HM, Narayan O: Chimeric simian/human immunodeficiency virus that causes progressive loss of CD4 + T cells and AIDS in pig-tailed macaques. J Virol 1996; 70: 3189–97.
- 13Li J, Lord CI, Haseltine W, Letvin NL, Sodroski J: Infection of cynomolgus monkeys with a chimeric HIV-1/SIVmac virus that expresses the HIV-1 envelope glycoproteins. J Acquir Immune Defic Syndr 1992; 5: 639–46.
- 14Luciw PA, Pratt-Lowe E, Shaw KE, Levy JA, Cheng-Mayer C: Persistent infection of rhesus macaques with T-cell-line-tropic and macrophage-tropic clones of simian/human immunodeficiency viruses (SHIV). Proc Natl Acad Sci USA 1995; 92: 7490–4.
- 15Reimann KA, Li JT, Voss G, Lekutis C, Tenner-Racz K, Racz P, Lin W, Montefiori DC, Lee-Parritz DE, Lu Y, Collman RG, Sodroski J, Letvin NL: An env gene derived from a primary human immunodeficiency virus type 1 isolate confers high in vivo replicative capacity to a chimeric simian/human immunodeficiency virus in rhesus monkeys. J Virol 1996; 70: 3198–206.
- 16Schell J, Rose NF, Fazo N, Marx PA, Hunter M, Ramsburg E, Montefiori D, Earl P, Moss B, Rose JK: Long-term vaccine protection from AIDS and clearance of viral DNA following SHIV89.6P challenge. Vaccine 2009; 27: 979–86.
- 17Shibata R, Kawamura M, Sakai H, Hayami M, Ishimoto A, Adachi A: Generation of a chimeric human and simian immunodeficiency virus infectious to monkey peripheral blood mononuclear cells. J Virol 1991; 65: 3514–20.
- 18Humbert M, Rasmussen RA, Song R, Ong H, Sharma P, Chenine AL, Kramer VG, Siddappa NB, Xu W, Else JG, Novembre FJ, Strobert E, O'Neil SP, Ruprecht RM: SHIV-1157i and passaged progeny viruses encoding R5 HIV-1 clade C env cause AIDS in rhesus monkeys. Retrovirology 2008; 5: 94.
- 19Lu Y, Pauza CD, Lu X, Montefiori DC, Miller CJ: Rhesus macaques that become systemically infected with pathogenic SHIV 89.6-PD after intravenous, rectal, or vaginal inoculation and fail to make an antiviral antibody response rapidly develop AIDS. J Acquir Immune Defic Syndr Hum Retrovirol 1998; 19: 6–18.
- 20Cayabyab M, Rohne D, Pollakis G, Mische C, Messele T, Abebe A, Etemad-Moghadam B, Yang P, Henson S, Axthelm M, Goudsmit J, Letvin NL, Sodroski J: Rapid CD4 + T-lymphocyte depletion in rhesus monkeys infected with a simian-human immunodeficiency virus expressing the envelope glycoproteins of a primary dual-tropic Ethiopian Clade C HIV type 1 isolate. AIDS Res Hum Retroviruses 2004; 20: 27–40.
- 21Li Y, Yang GB, Chen QM, Liu Q, Meng ZF, Geng YQ, Qiao WT, Shao YM: Construction and characterization of a new simian/human immunodeficiency viruses clone carrying an env gene derived from a CRF07_BC strain. Chin Med J (Engl) 2009; 122: 2874–9.
- 22Liu Q, Li Y, Yang G, Dai J, Ruprecht RM, Shao Y: Molecularly cloned SHIV-CN97001: a replication-competent, R5 simian/human immunodeficiency virus containing env of a primary Chinese HIV-1 clade C isolate. J Med Primatol 2011; 40: 427–36.
- 23Ndung'u T, Lu Y, Renjifo B, Touzjian N, Kushner N, Pena-Cruz V, Novitsky VA, Lee TH, Essex M: Infectious simian/human immunodeficiency virus with human immunodeficiency virus type 1 subtype C from an African isolate: rhesus macaque model. J Virol 2001; 75: 11417–25.
- 24Wu Y, Hong K, Chenine AL, Whitney JB, Xu W, Chen Q, Geng Y, Ruprecht RM, Shao Y: Molecular cloning and in vitro evaluation of an infectious simian-human immunodeficiency virus containing env of a primary Chinese HIV-1 subtype C isolate. J Med Primatol 2005; 34: 101–7.
- 25Karlsson GB, Halloran M, Schenten D, Lee J, Racz P, Tenner-Racz K, Manola J, Gelman R, Etemad-Moghadam B, Desjardins E, Wyatt R, Gerard NP, Marcon L, Margolin D, Fanton J, Axthelm MK, Letvin NL, Sodroski J: The envelope glycoprotein ectodomains determine the efficiency of CD4 + T lymphocyte depletion in simian-human immunodeficiency virus-infected macaques. J Exp Med 1998; 188: 1159–71.
- 26Reimann KA, Li JT, Veazey R, Halloran M, Park IW, Karlsson GB, Sodroski J, Letvin NL: A chimeric simian/human immunodeficiency virus expressing a primary patient human immunodeficiency virus type 1 isolate env causes an AIDS-like disease after in vivo passage in rhesus monkeys. J Virol 1996; 70: 6922–8.
- 27Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011; 28: 2731–9.
- 28Karlsson GB, Halloran M, Li J, Park IW, Gomila R, Reimann KA, Axthelm MK, Iliff SA, Letvin NL, Sodroski J: Characterization of molecularly cloned simian-human immunodeficiency viruses causing rapid CD4 + lymphocyte depletion in rhesus monkeys. J Virol 1997; 71: 4218–25.
- 29Smith JM, Dauner A, Li B, Srinivasan P, Mitchell J, Hendry M, Ellenberger D, Butera S, Otten RA: Generation of a dual RT Env SHIV that is infectious in rhesus macaques. J Med Primatol 2010; 39: 213–23.
- 30Hu J, Pope M, Brown C, O'Doherty U, Miller CJ: Immunophenotypic characterization of simian immunodeficiency virus-infected dendritic cells in cervix, vagina, and draining lymph nodes of rhesus monkeys. Lab Invest 1998; 78: 435–51.
