Simian immunodeficiency virus (SIV) envelope quasispecies transmission and evolution in infant rhesus macaques after oral challenge with uncloned SIVmac251: increased diversity is associated with neutralizing antibodies and improved survival in previously immunized animals

Virology Journal

Marta L Marthas⁴  Bernard Moss²  Patricia Earl²  David Montefiori¹  Koen KA Van Rompay³  Jennifer L Greenier³ 

[1] Duke University Medical Center, Durham, NC 27710, USA;Laboratory of Viral Diseases, National Institutes of Health, Bethesda, MD 20892, USA;California National Primate Research Center, University of California, Davis, CA 95616, USA;Department of Pathology, Microbiology and Immunology, School of Veterinary Medicine, University of California, Davis, CA 95616, USA

关键词: HMA;    HIV;    vaccine;    pediatric;   

Others  :  1158208
DOI  :  10.1186/1743-422X-2-11

 received in 2004-12-24, accepted in 2005-02-14,  发布年份 2005

【 摘 要 】

Background

Oral infection of infant macaques with simian immunodeficiency virus (SIV) is a useful animal model to test interventions to reduce postnatal HIV transmission via breast-feeding. We previously demonstrated that immunization of infant rhesus macaques with either modified vaccinia virus Ankara (MVA) expressing SIV Gag, Pol and Env, or live-attenuated SIVmac1A11 resulted in lower viremia and longer survival compared to unimmunized controls after oral challenge with virulent SIVmac251 (Van Rompay et al., J. Virology 77:179–190, 2003). Here we evaluate the impact of these vaccines on oral transmission and evolution of SIV envelope variants.

Results

Limiting dilution analysis of SIV RNA followed by heteroduplex mobility assays of the V1–V2 envelope (env) region revealed two major env variants in the uncloned SIVmac251 inoculum. Plasma sampled from all infants 1 week after challenge contained heterogeneous SIV env populations including one or both of the most common env variants in the virus inoculum; no consistent differences in patterns of env variants were found between vaccinated and unvaccinated infants. However, SIV env variant populations diverged in most vaccinated monkeys 3 to 5 months after challenge, in association with the development of neutralizing antibodies.

Conclusions

These patterns of viral envelope diversity, immune responses and disease course in SIV-infected infant macaques are similar to observations in HIV-infected children, and underscore the relevance of this pediatric animal model. The results also support the concept that neonatal immunization with HIV vaccines might modulate disease progression in infants infected with HIV by breast-feeding.

【 授权许可】

   
2005 Greenier et al; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Kreiss J: Breastfeeding and vertical transmission of HIV-1. Acta Paediatr Suppl 1997, 421:113-117.
• [2]Leroy V, Newell ML, Dabis F, Peckham C, Van de Perre P, Bulterys M, Kind C, Simonds RJ, Wiktor S, Msellati P: International mulicentre pooled analysis of late postnatal mother-to-child transmission of HIV-1 infection. Ghent International Working Group on Mother-to-Child Transmission of HIV. Lancet 1998, 352:597-600.
• [3]Nduati R, John G, Mbori-Ngacha D, Richardson B, Overbaugh J, Mwatha A, Ndinya-Achola J, Bwayo J, Onyango FE, Hughes J, Kreiss J: Effect of breastfeeding and formula feeding on transmission of HIV-1. JAMA 2000, 283:1167-1174.
• [4]Bertolli J, St Louis ME, Simonds RJ, Nieburg P, Kamenga M, Brown C, Tarande M, Quinn T, Ou CY: Estimating the timing of mother-to-child transmission of human immunodeficiency virus in a breast-feeding population in Kinshasa, Zaire. J Infect Dis 1996, 174:722-726.
• [5]De Cock K, Fowler MG, Mercier E, de Vincenzi I, Saba J, Hoff E, Alnwick DJ, Rogers M, Shaffer N: Prevention of mother-to-child HIV transmission in resource-poor countries. Translating research into policy and practice. JAMA 2000, 283:1175-1182.
• [6]Dickover RE, Garratty EM, Plaeger S, Bryson YJ: Perinatal transmission of major, minor, and multiple maternal human immunodeficiency virus type 1 variants in utero and intrapartum. J Virol 2001, 75:2194-2203.
• [7]Essajee SM, Pollack H, Rochford G, Oransky I, Krasinski K, Borkowsky W: Early changes in quasispecies repertoire in HIV-infected infants: correlation with disease progression. AIDS Res Hum Retroviruses 2000, 16:1949-57.
• [8]Delwart EL, Pan H, Sheppard HW, Wolpert D, Neumann AU, Korber B, Mullins JI: Slower evolution of human immunodeficiency virus type 1 quasispecies during progression to AIDS. J Virol 1997, 71:7498-7508.
• [9]Shankarappa R, Margolick JB, Gange SJ, Rodrigo AG, Upchurch D, Farzadegan H, Gupta P, Rinaldo CR, Learn GH, He X, Huang XL, Mullins JI: Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J Virol 1999, 73:10489-502.
• [10]Wolinsky SM, Carla MW, Korber BTM, Hutto C, Parks WP, Rosenblum LL, Kunstman KJ, Furtado MR, Munoz JL: Selective transmission of human immunodeficiency virus type 1 variant from mothers to infants. Science 1992, 255:1134-1137.
• [11]Strunnikova N, Ray SC, Lancioni C, Nguyen M, Viscidi RP: Evolution of human immunodeficiency virus type 1 in relation to disease progression in children. J Hum Virol 1998, 1:224-39.
• [12]Strunnikova N, Ray S, Livingston R, Rubalcaba E, Viscidi R: Convergent evolution within the V3 loop domain of human immunodeficiency virus type 1 in association with disease progression. J Virol 1995, 69:7548-7558.
• [13]Hutto C, Zhou Y, He J, Geffin R, Hill M, Scott W, Wood C: Longitudinal studies of viral sequence, viral phenotype, and immunologic parameters of human immunodeficiency virus type 1 infection in perinatally infected twins with discordant diseases courses. J Virol 1996, 70:3589-3598.
• [14]Salvatori F, Masiero S, Giaquinto C, Wade CM, Leigh-Brown AJ, Chieco-Bianchi L, De Rossi A: Evolution of human immunodeficiency virus type 1 in perinatally infected infants with rapid and slow progression to disease. J Virol 1997, 71:4694-4706.
• [15]Ganeshan S, Dickover RE, Korber BTM, Bryson YJ, Wolinsky S: Human immunodeficiency virus type 1 genetic evolution in children with different rates of development of disease. J Virol 1997, 71:663-677.
• [16]Halapi E, Leitner T, Jansson M, Scarlatti G, Orlandi P, Plebani A, Romiti L, Albert J, Wigzell H, Rossi P: Correlation between HIV sequence evolution, specific immune response and clinical outcome in vertically infected infants. AIDS 1997, 11:1709-1717.
• [17]Geffin R, Hutto C, Andrew C, Scott GB: A longitudinal assessment of autologous neutralizing antibodies in children perinatally infected with human immunodeficiency virus type 1. Virology 2003, 310:207-215.
• [18]Marthas ML, Van Rompay KKA, Otsyula M, Miller CJ, Canfield D, Pedersen NC, McChesney MB: Viral factors determine progression to AIDS in simian immunodeficiency virus-infected newborn rhesus macaques. J Virol 1995, 69:4198-4205.
• [19]Van Rompay KKA, Berardi CJ, Dillard-Telm S, Tarara RP, Canfield DR, Valverde CR, Montefiori DC, Stefano Cole K, Montelaro RC, Miller CJ, Marthas ML: Passive immunization of newborn rhesus macaques prevents oral simian immunodeficiency virus infection. J Infect Dis 1998, 177:1247-1259.
• [20]Van Rompay KKA, McChesney MB, Aguirre NL, Schmidt KA, Bischofberger N, Marthas ML: Two low doses of tenofovir protect newborn macaques against oral simian immunodeficiency virus infection. J Infect Dis 2001, 184:429-438.
• [21]Van Rompay KKA, Greenier JL, Cole KS, Earl P, Moss B, Steckbeck JD, Pahar B, Rourke T, Montelaro RC, Canfield DR, Tarara RP, Miller CJ, McChesney MB, Marthas ML: Immunization of newborn rhesus macaques with simian immunodeficiency virus (SIV) vaccines prolongs survival after oral challenge with virulent SIVmac251. J Virol 2003, 77:179-190.
• [22]Greenier JL, Miller CJ, Lu D, Dailey PJ, Lü FX, Kunstman KJ, Wolinsky SM, Marthas ML: Route of simian immunodeficiency virus inoculation determines the complexity but not the identity of viral variant populations that infect rhesus macaques. J Virol 2001, 75:3753-3765.
• [23]Lamers SL, Sleasman JW, She JX, Barrie KA, Pomeroy SM, Barrett DJ, Goodenow MM: Persistence of multiple maternal genotypes of human immunodeficiency virus type I in infants infected by vertical transmission. J Clin Invest 1994, 93:380-390.
• [24]Briant L, Wade CM, Puel J, Leigh Brown AJ, Guyader M: Analysis of envelope sequence variants suggests multiple mechanisms of mother-to-child transmission of human immunodeficiency virus type 1. J Virol 1995, 69:3778-3788.
• [25]Wike CM, Korber BT, Daniels MR, Hutto C, Munoz J, Furtado M, Parks W, Saah A, Bulterys M, Kurawige JB, Wolinsky SM: HIV-1 sequence variation between isolates from mother-infant transmission pairs. AIDS Res Hum Retroviruses 1992, 8:1297-1300.
• [26]Kliks S, Contag CH, Corliss H, Learn G, Rodrigo A, Wara D, Mullins JI, Levy JA: Genetic analysis of viral variants selected in transmission of human immunodeficiency viruses in newborns. AIDS Res Hum Retroviruses 2000, 16:1223-1233.
• [27]Arroyo MA, Tien H, Pagán M, Swanstrom R, Hilyer GV, Cadilla CL, Meléndez-Guerrero LM: Virologic risk factors for vertical transmission of HIV type 1 in Puerto Rico. AIDS Res Hum Retroviruses 2002, 18:447-460.
• [28]Pasquier C, Cayrou C, Blancher A, Tourne-Petheil C, Berrebi A, Tricoire J, Puel J, Izopet J: Molecular evidence for mother-to-child transmission of multiple variants by analysis of RNA and DNA sequences of human immunodeficiency virus type 1. J Virol 1998, 72:8493-8501.
• [29]Sutthent R, Foongladda S, Chearskul S, Wanprapa N, Likanonskul S, Kositanont U, Riengrojpitak S, Sahaphong S, Wasi C: V3 sequence diversity of HIV-1 subtype E in infected mothers and their infants. J Acquir Immune Defic Syndr Hum Retrovirol 1998, 18:323-331.
• [30]Sutthent R, Foongladda S, Chearskul S, Wanaprapa N, Likanonskul S, Kositanont U, Riengrojpitak S, Sahapong S, Wasi C: Maternal and viral factors in vertical transmission of HIV-1 subtype E. Southeast Asian J Trop Med Public Health 1997, 28:689-98.
• [31]Renjifo B, Chung M, Gilbert P, Mwakagile D, Msamanga G, Fawzi W, Essex M: In-utero transmission of quasispecies among human immunodeficiency virus type 1 genotypes. Virology 2003, 307:278-282.
• [32]Ahmad N, Baroudy BM, Baker RC, Chappey C: Genetic analysis of human immunodeficiency virus type 1 envelope V3 region isolates from mothers and infants after perinatal transmission. J Virol 1995, 69:1001-1012.
• [33]Contag CH, Ehrnst A, Duda J, Bohlin AB, Lindgren S, Learn GH, Mullins JI: Mother-to-infant transmission of human immunodeficiency virus type 1 involving five envelope sequence subtypes. J Virol 1997, 71:1292-1300.
• [34]Mulder-Kampinga G, Kuiken C, Dekker J, Scherpbier H, Boer K, Goudsmit J: Genomic human immunodeficiency virus type 1 RNA variation in mother and child following intra-uterine virus transmission. J Gen Virol 1993, 74:1747-1756.
• [35]Matala E, Crandall KA, Baker RC, Ahmad N: Limited heterogeneity of HIV type 1 in infected mothers correlates with lack of vertical transmission. AIDS Res Hum Retroviruses 2000, 16:1481-1489.
• [36]Amedee AM, Lacour N, Martin LN, Clements JE, Bohm RB Jr, Davison B, Harrison R, Murphey-Corb M: Genotypic analysis of infant macaques infected transplacentally and orally. J Med Primatol 1996, 25:225-235.
• [37]Amedee AM, Lacour N, Ratterree M: Mother-to-infant transmission of SIV via breast-feeding in rhesus macaques. J Med Primatol 2003, 32:187-193.
• [38]Delwart E, Sheppard H, Walker B, Goudsmit J, Mullins J: Human immunodeficiency virus type 1 evolution in vivo tracked by DNA heteroduplex mobility assays. J Virol 1994, 68:6672-6683.
• [39]Lukashov VV, Kuiken CL, Goudsmit J: Intrahost human immunodeficiency virus type 1 evolution is related to length of the immunocompetent period. J Virol 1995, 69:6911-6916.
• [40]Mani I, Gilbert P, Sankalé J-L, Eisen G, Mboup S, Kanki PJ: Intrapatient diversity and its correlation with viral setpoint in human immunodeficiency virus type 1 CRF02_A/G-IbNG infection. J Virol 2002, 76:10745-10755.
• [41]Markham RB, Wang W-C, Weisstein AE, Wang Z, Munoz A, Templeton A, Margolick J, Vlahov D, Quinn T, Farzadegan H, Yu X-F: Patterns of HIV-1 evolution in individuals with differing rates of CD4 T cell decline. Proc Natl Acad Sci USA 1998, 95:12568-12573.
• [42]Wolinsky SM, Korber BTM, Neumann AU, Daniels M, Kunstman KJ, Whetsell AJ, Furtado MR, Cao Y, Ho DD, Safrit JT: Adaptive evolution of human immunodeficiency virus-type 1 during the natural course of infection. Science 1996, 272:537-542.
• [43]Wolfs TF, de Jong JJ, Van den Berg H, Tijnagel JM, Krone WJ, Goudsmit J: Evolution of sequences encoding the principal neutralization epitope of human immunodeficiency virus 1 is host dependent, rapid, and continuous. Proc Natl Acad Sci USA 1990, 87:9938-9942.
• [44]Liu SL, Schacker T, Musey L, Shriner D, McElrath MJ, Corey L, Mullins JI: Divergent patterns of progression to AIDS after infection from the same source: human immunodeficiency virus type 1 evolution and antiviral responses. J Virol 1997, 71:4284-4295.
• [45]Rybarczyk BJ, Montefiori D, Johnson PR, West A, Johnston RE, Swanstrom R: Correlation between env V1/V2 region diversification and neutralizing antibodies during primary infection by simian immunodeficiency virus sm in rhesus macaques. J Virol 2004, 78:3561-3571.
• [46]Van Rompay KKA, Abel K, Lawson JR, Singh RP, Schmidt KA, Evans T, Earl P, Harvey D, Franchini G, Tartaglia J, Montefiori D, Hattangadi S, Moss B, Marthas ML: Attenuated poxvirus-based SIV vaccines given in infancy partially protect infant and juvenile macaques against repeated oral challenge with virulent SIV. J Acquir Immune Defic Syndr 2005, 38:124-134.
• [47]National Research Council: Guide for the care and use of laboratory animals. Washington, D. C.: National Academy Press; 1996.
• [48]Delwart E, Shaper E, McCutchan F, Louwagie J, Grez M, Rubsamen-Waigmann H, Mullins J: Genetic relationships determined by a heteroduplex mobility assay: analysis of HIV env genes. Science 1993, 262:1257-1261.
• [49]Delwart EL, Herring B, Rodrigo AG, Mullins JI: Genetic subtyping of human immunodeficiency virus using a heteroduplex mobility assay. PCR Methods Appl 1995, 4:S202-S216.
• [50]Evans DT, Knapp LA, Jing P, Mitchen JL, Dykhuizen M, Montefiori DC, Pauza CD, Watkins DI: Rapid and slow progressors differ by a single MHC class I haplotype in a family of MHC-defined rhesus macques infected with SIV. Immunol Lett 1999, 66:53-59.
• [51]Knapp LA, Lehmann E, Piekarczyk MS, Urvater JA, Watkins DI: A high frequency of Mamu-1*01 in the rhesus macaque detected by polymerase chain reaction with sequence-specific primers and direct sequencing. Tissue Antigens 1997, 50:657-661.
• [52]Montefiori DC, Baba TW, Li A, Bilska M, Ruprecht RM: Neutralizing and infection-enhancing antibody responses do not correlate with the differential pathogenicity of SIVmac239Δ3 in adult and infant rhesus monkeys. J Immunol 1996, 157:5528-5535.