Sequential evolution and escape from neutralization of simian immunodeficiency virus SIVsmE660 Clones in Rhesus Macaques

Journal of Virology

Volumn 86, Issue 16, 2012, Pages 8835-8847

  Wu, Fan ^a   Ourmanov, Ilnour ^a   Kuwata, Takeo ^b   Goeken, Robert ^a   Brown, Charles R ^a   Buckler White, Alicia ^a   Iyengar, Ranjini ^a   Plishka, Ronald ^a   Aoki, Scott T ^c   Hirsch, Vanessa M ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b KUMAMOTO UNIVERSITY   (Japan)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENVELOPE PROTEIN; NEUTRALIZING ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; GENETIC POLYMORPHISM; IN VIVO STUDY; INDEL MUTATION; INFECTION CONTROL; LUNG LAVAGE; LYMPHOCYTE COUNT; MACACA; MEMORY T LYMPHOCYTE; MOLECULAR CLONING; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; RHESUS MACAQUES; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; VIREMIA; VIRUS IMMUNITY; VIRUS ISOLATION; VIRUS NEUTRALIZATION; VIRUS PATHOGENESIS; VIRUS REPLICATION;

AMINO ACID SUBSTITUTION; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CD4 LYMPHOCYTE COUNT; DISEASE MODELS, ANIMAL; EVOLUTION, MOLECULAR; IMMUNE EVASION; MACACA MULATTA; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; MUTATION; POINT MUTATION; POLYMORPHISM, GENETIC; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; SEQUENCE DELETION; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 84865076975     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00923-12     Document Type: Article

References (69)

1. Baba TW, et al. 2000. Human neutralizing monoclonal antibodies of the IgG1 subtype protect against mucosal simian-human immunodeficiency virus infection. Nat. Med. 6:200-206.
2. Barouch DH, et al. 2012. Vaccine protection against acquisition of neutralization-resistant SIV challenges in rhesus monkeys. Nature 482: 89-93.
3. Binley JM, et al. 2008. Profiling the specificity of neutralizing antibodies in a large panel of plasmas from patients chronically infected with human immunodeficiency virus type 1 subtypes B and C. J. Virol. 82:11651-11668.
4. Bottiger D, Putkonen P, Oberg B. 1992. Prevention of HIV-2 and SIV infections in cynomolgus macaques by prophylactic treatment with 3=-fluorothymidine. AIDS Res. Hum. Retroviruses 8:1235-1238.
5. Bunnik EM, et al. 2010. Adaptation of HIV-1 envelope gp120 to humoral immunity at a population level. Nat. Med. 16:995-997.
6. Bunnik EM, Lobbrecht MS, van Nuenen AC, Schuitemaker H. 2010. Escape from autologous humoral immunity of HIV-1 is not associated with a decrease in replicative capacity. Virology 397:224-230.
7. Bunnik EM, et al. 2010. Emergence of monoclonal antibody b12-resistant human immunodeficiency virus type 1 variants during natural infection in the absence of humoral or cellular immune pressure. J. Gen. Virol. 91:1354-1364.
8. Bunnik EM, et al. 2009. Changing sensitivity to broadly neutralizing antibodies b12, 2G12, 2F5, and 4E10 of primary subtype B human immunodeficiency virus type 1 variants in the natural course of infection. Virology 390:348-355.
9. Burns DP, Collignon C, Desrosiers RC. 1993. Simian immunodeficiency virus mutants resistant to serum neutralization arise during persistent infection of rhesus monkeys. J. Virol. 67:4104-4113.
10. Burns DP, Desrosiers RC. 1991. Selection of genetic variants of simian immunodeficiency virus in persistently infected rhesus monkeys. J. Virol. 65:1843-1854.
11. Cao Y, Qin L, Zhang L, Safrit J, Ho DD. 1996. Characterization of long-term survivors of human immunodeficiency virus type 1 infection. Immunol. Lett. 51:7-13.
12. Deeks SG, et al. 2006. Neutralizing antibody responses against autologous and heterologous viruses in acute versus chronic human immunodeficiency virus (HIV) infection: evidence for a constraint on the ability of HIV to completely evade neutralizing antibody responses. J. Virol. 80: 6155-6164.
13. de Silva TI, et al. 2012. Potent autologous and heterologous neutralizing antibody responses occur in HIV-2 infection across a broad range of infection outcomes. J. Virol. 86:930-946.
14. Dickover R, et al. 2006. Role of maternal autologous neutralizing antibody in selective perinatal transmission of human immunodeficiency virus type 1 escape variants. J. Virol. 80:6525-6533.
15. Doria-Rose NA, et al. 2009. Frequency and phenotype of human immunodeficiency virus envelope-specific B cells from patients with broadly cross-neutralizing antibodies. J. Virol. 83:188-199.
16. Emini EA, et al. 1992. Prevention of HIV-1 infection in chimpanzees by gp120 V3 domain-specific monoclonal antibody. Nature 355:728-730.
17. Euler Z, et al. 2010. Cross-reactive neutralizing humoral immunity does not protect from HIV type 1 disease progression. J. Infect. Dis. 201:1045-1053.
18. Goldstein S, et al. 1994. Immunization with whole inactivated vaccine protects from infection by SIV grown in human but not macaque cells. J. Med. Primatol. 23:75-82.
19. Gray ES, et al. 2007. Neutralizing antibody responses in acute human immunodeficiency virus type 1 subtype C infection. J. Virol. 81:6187-6196.
20. Haynes BF, et al. 2012. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N. Engl. J. Med. 366:1275-1286.
21. Hirsch V, et al. 1997. A molecularly cloned, pathogenic, neutralizationresistant simian immunodeficiency virus, SIVsmE543-3. J. Virol. 71: 1608-1620.
22. Hirsch VM, et al. 1996. Patterns of viral replication correlate with outcome in simian immunodeficiency virus (SIV)-infected macaques: effect of prior immunization with a trivalent SIV vaccine in modified vaccinia virus Ankara. J. Virol. 70:3741-3752.
23. Hirsch VM, Zack PM, Johnson PR. 1990. Molecular characterization of SIV in tissues from experimentally infected macaques. J. Med. Primatol. 19:287-294.
24. Huang KH, et al. 2010. B-cell depletion reveals a role for antibodies in the control of chronic HIV-1 infection. Nat. Commun. 1:102.
25. Kirmaier A, et al. 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.
26. Kong R, et al. 2012. Broad and potent neutralizing antibody responses elicited in natural HIV-2 infection. J. Virol. 86:947-960.
27. Kuiken C, et al (ed). 2011. HIV sequence compendium. Los Alamos National Laboratory, Theoretical Biology and Biophysics, Los Alamos, NM.
28. Kuwata T, et al. 2007. A rapid progressor-specific variant clone of simian immunodeficiency virus replicates efficiently in vivo only in the absence of immune responses. J. Virol. 81:8891-8904.
29. Kuwata T, et al. 2006. Infectious molecular clones from a simian immunodeficiency virus-infected rapid-progressor (RP) macaque: evidence of differential selection of RP-specific envelope mutations in vitro and in vivo. J. Virol. 80:1463-1475.
30. Lai L, et al. 2011. Prevention of infection by a granulocytemacrophage colony-stimulating factor co-expressing DNA/modified vaccinia Ankara simian immunodeficiency virus vaccine. J. Infect. Dis. 204:164-173.
31. Lifson JD, Haigwood NL. 2011. 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.
32. Mahalanabis M, et al. 2009. Continuous viral escape and selection by autologous neutralizing antibodies in drug-naive human immunodeficiency virus controllers. J. Virol. 83:662-672.
33. Mascola JR, et al. 1996. Immunization with envelope subunit vaccine products elicits neutralizing antibodies against laboratory-adapted but not primary isolates of human immunodeficiency virus type 1. J. Infect. Dis. 173:340-348.
34. Mascola JR, et al. 2000. Protection of macaques against vaginal transmission of a pathogenic HIV-1/SIV chimeric virus by passive infusion of neutralizing antibodies. Nat. Med. 6:207-210.
35. Miller CJ, et al. 2007. Antiviral antibodies are necessary for control of simian immunodeficiency virus replication. J. Virol. 81:5024-5035.
36. Montefiori DC, et al. 1996. Neutralizing and infection-enhancing antibody responses to human immunodeficiency virus type 1 in long-term nonprogressors. J. Infect. Dis. 173:60-67.
37. Moore PL, et al. 2011. Potent and broad neutralization of HIV-1 subtype C by plasma antibodies targeting a quaternary epitope including residues in the V2 loop. J. Virol. 85:3128-3141.
38. Moore PL, et al. 2009. Limited neutralizing antibody specificities drive neutralization escape in early HIV-1 subtype C infection. PLoS Pathog. 5:e1000598. doi:10.1371/journal.ppat.1000598.
39. Ourmanov I, Bilska M, Hirsch VM, Montefiori DC. 2000. Recombinant modified vaccinia virus Ankara expressing the surface gp120 of simian immunodeficiency virus (SIV) primes for a rapid neutralizing antibody response to SIV infection in macaques. J. Virol. 74:2960-2965.
40. Ourmanov I, et al. 2009. Improved survival in rhesus macaques immunized with modified vaccinia virus Ankara recombinants expressing simian immunodeficiency virus envelope correlates with reduction in memory CD4_ T-cell loss and higher titers of neutralizing antibody. J. Virol. 83:5388-5400.
41. Overbaugh J, Morris L. 2012. The antibody response against HIV-1. Cold Spring Harb. Perspect. Med. 2:a007039. doi:10.1101/cshperspect.a007039.
42. Overbaugh J, Rudensey LM. 1992. Alterations in potential sites for glycosylation predominate during evolution of the simian immunodeficiency virus envelope gene in macaques. J. Virol. 66:5937-5948.
43. Overbaugh J, Rudensey LM, Papenhausen MD, Benveniste RE, Morton WR. 1991. Variation in simian immunodeficiency virus env is confined to V1 and V4 during progression to simian AIDS. J. Virol. 65:7025-7031.
44. Parren PW, et al. 2001. Antibody protects macaques against vaginal challenge with a pathogenic R5 simian/human immunodeficiency virus at serum levels giving complete neutralization in vitro. J. Virol. 75:8340-8347.
45. Pereyra F, et al. 2008. Genetic and immunologic heterogeneity among persons who control HIV infection in the absence of therapy. J. Infect. Dis. 197:563-571.
46. Piantadosi A, et al. 2009. Breadth of neutralizing antibody response to human immunodeficiency virus type 1 is affected by factors early in infection but does not influence disease progression. J. Virol. 83: 10269-10274.
47. Pilgrim AK, et al. 1997. Neutralizing antibody responses to human immunodeficiency virus type 1 in primary infection and long-termnonprogressive infection. J. Infect. Dis. 176:924-932.
48. Prince AM, et al. 1991. Prevention of HIV infection by passive immunization with HIV immunoglobulin. AIDS Res. Hum. Retroviruses 7:971-973.
49. Reed LJ, Muench H. 1938. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 27:493-497.
50. Reynolds MR, et al. 2011. The TRIM5_ genotype of rhesus macaques affects acquisition of simian immunodeficiency virus SIVsmE660 infection after repeated limiting-dose intrarectal challenge. J. Virol. 85:9637-9640.
51. Richman DD, Wrin T, Little SJ, Petropoulos CJ. 2003. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc. Natl. Acad. Sci. U. S. A. 100:4144-4149.
52. Rong R, et al. 2009. Escape from autologous neutralizing antibodies in acute/early subtype C HIV-1 infection requires multiple pathways. PLoS Pathog. 5:e1000594. doi:10.1371/journal.ppat.1000594.
53. Rudensey LM, Kimata JT, Long EM, Chackerian B, Overbaugh J. 1998. Changes in the extracellular envelope glycoprotein of variants that evolve during the course of simian immunodeficiency virus SIVMne infection affect neutralizing antibody recognition, syncytium formation, and macrophage tropism but not replication, cytopathicity, or CCR-5 coreceptor recognition. J. Virol. 72:209-217.
54. Sather DN, et al. 2009. Factors associated with the development of crossreactive neutralizing antibodies during human immunodeficiency virus type 1 infection. J. Virol. 83:757-769.
55. Sato S, et al. 2008. Potent antibody-mediated neutralization and evolution of antigenic escape variants of simian immunodeficiency virus strain SIVmac239 in vivo. J. Virol. 82:9739-9752.
56. Scarlatti G, et al. 1993. Mother-to-child transmission of human immunodeficiency virus type 1: correlation with neutralizing antibodies against primary isolates. J. Infect. Dis. 168:207-210.
57. Schmitz JE, et al. 2003. Effect of humoral immune responses on controlling viremia during primary infection of rhesus monkeys with simian immunodeficiency virus. J. Virol. 77:2165-2173.
58. Shibata R, et al. 1999. Neutralizing antibody directed against the HIV-1 envelope glycoprotein can completely block HIV-1/SIV chimeric virus infections of macaque monkeys. Nat. Med. 5:204-210.
59. Simek MD, et al. 2009. Human immunodeficiency virus type 1 elite neutralizers: individuals with broad and potent neutralizing activity identified by using a high-throughput neutralization assay together with an analytical selection algorithm. J. Virol. 83:7337-7348.
60. van Gils MJ, et al. 2010. Rapid escape from preserved cross-reactive neutralizing humoral immunity without loss of viral fitness in HIV-1-infected progressors and long-term nonprogressors. J. Virol. 84:3576-3585.
61. Wang C, et al. 2009. Ecosystem services assessment of two watersheds of Lancang River in Yunnan, China with a decision tree approach. Ambio 38:47-54.
62. Wei X, et al. 2002. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob. Agents Chemother. 46:1896-1905.
63. Wei X, et al. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312.
64. Wrin T, Nunberg JH. 1994. HIV-1MN recombinant gp120 vaccine se-rum, which fails to neutralize primary isolates of HIV-1, does not antagonize neutralization by antibodies from infected individuals. AIDS 8:1622-1623.
65. Wu X, et al. 2012. Selection pressure on HIV-1 envelope by broadly neutralizing antibodies to the conserved CD4-binding site. J. Virol. 86: 5844-5856.
66. Yeh WW, et al. 2010. Autologous neutralizing antibodies to the transmitted/ founder viruses emerge late after simian immunodeficiency virus SIVmac251 infection of rhesus monkeys. J. Virol. 84:6018-6032.
67. Yeh WW, et al. 2011. The TRIM5 gene modulates penile mucosal acquisition of simian immunodeficiency virus in rhesus monkeys. J. Virol. 85: 10389-10398.
68. Zhang M, et al. 2004. Tracking global patterns of N-linked glycosylation site variation in highly variable viral glycoproteins: HIV, SIV, and HCV envelopes and influenza hemagglutinin. Glycobiology 14:1229-1246.
69. Zinkernagel RM. 2003. On natural and artificial vaccinations. Annu. Rev. Immunol. 21:515-546.