Pathogenicity and mucosal transmissibility of the R5-Tropic simian/human immunodeficiency virus SHIVAD8 in Rhesus Macaques: Implications for USE in vaccine studies

Journal of Virology

Volumn 86, Issue 16, 2012, Pages 8516-8526

  Gautam, Rajeev ^a   Nishimura, Yoshiaki ^a   Lee, Wendy R ^a   Donau, Olivia ^a   Buckler White, Alicia ^a   Shingai, Masashi ^a   Sadjadpour, Reza ^a   Schmidt, Stephen D ^b   LaBranche, Celia C ^d   Keele, Brandon F ^c   Montefiori, David ^d   Mascola, John R ^b   Martin, Malcolm A ^a  

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

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c SAIC FREDERICK INC   (United States)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNE RESPONSE; IN VIVO STUDY; LYMPHOCYTE DEPLETION; MEMORY T LYMPHOCYTE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPPORTUNISTIC INFECTION; PRIORITY JOURNAL; RHESUS MONKEY; SEQUENCE ALIGNMENT; T LYMPHOCYTE SUBPOPULATION; VIREMIA; VIRUS REPLICATION; VIRUS STRAIN; VIRUS TRANSMISSION; VIRUS VIRULENCE;

AIDS VACCINES; ANIMALS; ANTIBODIES, NEUTRALIZING; CD4 LYMPHOCYTE COUNT; DISEASE MODELS, ANIMAL; HIV ANTIBODIES; HIV-1; HUMANS; MACACA MULATTA; MUCOUS MEMBRANE; RECOMBINATION, GENETIC; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 84865096278     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00644-12     Document Type: Article

References (53)

1. Amara RR, et al. 2001. Control of a mucosal challenge and prevention of AIDS by a multiprotein DNA/MVA vaccine. Science 292:69-74.
2. Barouch DH, et al. 2000. Control of viremia and prevention of clinical AIDS in rhesus monkeys by cytokine-augmented DNA vaccination. Science 290:486-492.
3. Brown CR, et al. 2007. Unique pathology in simian immunodeficiency virus-infected rapid progressor macaques is consistent with a pathogenesis distinct from that of classical AIDS. J. Virol. 81:5594-5606.
4. Burton DR, et al. 1994. Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science 266: 1024-1027.
5. Chen Z, et al. 2002. CD4+ lymphocytopenia in acute infection of Asian macaques by a vaginally transmissible subtype-C, CCR5-tropic simian/ human immunodeficiency virus (SHIV). J. Acquir. Immune Defic. Syndr. 30:133-145.
6. Dewar RL, et al. 1994. Application of branched DNA signal amplification to monitor human immunodeficiency virus type 1 burden in human plasma. J. Infect. Dis. 170:1172-1179.
7. Dreja H, et al. 2010. Neutralization activity in a geographically diverse East London cohort of human immunodeficiency virus type 1-infected patients: clade C infection results in a stronger and broader humoral immune response than clade B infection. J. Gen. Virol. 91:2794-2803.
8. Endo Y, et al. 2000. Short- and long-term clinical outcomes in rhesus monkeys inoculated with a highly pathogenic chimeric simian/human immunodeficiency virus. J. Virol. 74:6935-6945.
9. Fauci AS, et al. 2008. HIV vaccine research: the way forward. Science 321:530-532.
10. Feinberg MB, Moore JP. 2002. AIDS vaccine models: challenging challenge viruses. Nat. Med. 8:207-210.
11. Fenizia C, et al. 2011. TRIM5alpha does not affect simian immunodeficiency virus SIV(mac251) replication in vaccinated or unvaccinated Indian rhesus macaques following intrarectal challenge exposure. J. Virol. 85:12399-12409.
12. Gautam R, et al. 2009. Simian immunodeficiency virus SIVrcm, a unique CCR2-tropic virus, selectively depletes memory CD4+T cells in pigtailed macaques through expanded coreceptor usage in vivo. J. Virol. 83:7894-7908.
13. Harouse JM, Gettie A, Tan RC, Blanchard J, Cheng-Mayer C. 1999. Distinct pathogenic sequela in rhesus macaques infected with CCR5 or CXCR4 utilizing SHIVs. Science 284:816-819.
14. Ho SH, et al. 2007. Coreceptor switch in R5-tropic simian/human immunodeficiency virus-infected macaques. J. Virol. 81:8621-8633.
15. Ho SH, Trunova N, Gettie A, Blanchard J, Cheng-Mayer C. 2008. Different mutational pathways to CXCR4 coreceptor switch of CCR5-using simian-human immunodeficiency virus. J. Virol. 82:5653-5656.
16. Hsu M, et al. 2003. Increased mucosal transmission but not enhanced pathogenicity of the CCR5-tropic, simian AIDS-inducing simian/human immunodeficiency virus SHIV(SF162P3) maps to envelope gp120. J. Virol. 77:989-998.
17. Humbert M, et al. 2008. SHIV-1157i and passaged progeny viruses encoding R5 HIV-1 clade C env cause AIDS in rhesus monkeys. Retrovirology 5:94.
18. Igarashi T, et al. 2003. Macrophage-tropic simian/human immunodeficiency virus chimeras use CXCR4, not CCR5, for infections of rhesus macaque peripheral blood mononuclear cells and alveolar macrophages. J. Virol. 77:13042-13052.
19. Igarashi T, et al. 1999. Emergence of a highly pathogenic simian/human immunodeficiency virus in a rhesus macaque treated with anti-CD8 mAb during a primary infection with a nonpathogenic virus. Proc. Natl. Acad. Sci. U. S. A. 96:14049-14054.
20. Joag SV, et al. 1996. Chimeric simian/human immunodeficiency virus that causes progressive loss of CD4+ T cells and AIDS in pig-tailed macaques. J. Virol. 70:3189-3197.
21. Johnson WE, et al. 2003. Assorted mutations in the envelope gene of simian immunodeficiency virus lead to loss of neutralization resistance against antibodies representing a broad spectrum of specificities. J. Virol. 77:9993-10003.
22. Keele BF, et al. 2009. Low-dose rectal inoculation of rhesus macaques by SIVsmE660 or SIVmac251 recapitulates human mucosal infection by HIV-1. J. Exp. Med. 206:1117-1134.
23. Khoury G, Rajasuriar R, Cameron PU, Lewin SR. 2011. The role of naive T-cells in HIV-1 pathogenesis: an emerging key player. Clin. Immunol. 141:253-267.
24. Kraft Z, et al. 2007. Macaques infected with a CCR5-tropic simian/ human immunodeficiency virus (SHIV) develop broadly reactive anti-HIV neutralizing antibodies. J. Virol. 81:6402-6411.
25. Kuwata T, et al. 2009. Association of progressive CD4(+) T cell decline in SIV infection with the induction of autoreactive antibodies. PLoS Pathog. 5:e1000372. doi:10.1371/journal.ppat.1000372.
26. Laird ME, Igarashi T, Martin MA, Desrosiers RC. 2008. Importance of the V1/V2 loop region of simian-human immunodeficiency virus envelope glycoprotein gp120 in determining the strain specificity of the neutralizing antibody response. J. Virol. 82:11054-11065.
27. Li M, et al. 2005. Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. J. Virol. 79:10108-10125.
28. Liu J, et al. 2010. Low-dose mucosal simian immunodeficiency virus infection restricts early replication kinetics and transmitted virus variants in rhesus monkeys. J. Virol. 84:10406-10412.
29. Luciw PA, Pratt-Lowe E, Shaw KE, Levy JA, Cheng-Mayer C. 1995. Persistent infection of rhesus macaques with T-cell-line-tropic and macrophage-tropic clones of simian/human immunodeficiency viruses (SHIV). Proc. Natl. Acad. Sci. U. S. A. 92:7490-7494.
30. National Institutes of Health. 1985. Guide for the care and use of laboratory animals. Department of Health and Human Services publication no. NIH 85-23. National Institutes of Health, Bethesda, MD.
31. Nishimura Y, et al. 2005. Resting naive CD4+ T cells are massively infected and eliminated by X4-tropic simian-human immunodeficiency viruses in macaques. Proc. Natl. Acad. Sci. U. S. A. 102:8000-8005.
32. Nishimura Y, et al. 2007. Loss of naive cells accompanies memory CD4+ T-cell depletion during long-term progression to AIDS in simian immunodeficiency virus-infected macaques. J. Virol. 81:893-902.
33. Nishimura Y, et al. 2011. Recombination-mediated changes in coreceptor usage confer an augmented pathogenic phenotype in a nonhuman primate model of HIV-1-induced AIDS. J. Virol. 85:10617-10626.
34. Nishimura Y, et al. 2010. Generation of the pathogenic R5-tropic simian/ human immunodeficiency virus SHIVAD8 by serial passaging in rhesus macaques. J. Virol. 84:4769-4781.
35. Pahar B, Wang X, Dufour J, Lackner AA, Veazey RS. 2007. Virusspecific T cell responses in macaques acutely infected with SHIV(sf162p3). Virology 363:36-47.
36. Pal R, et al. 2003. Characterization of a simian human immunodeficiency virus encoding the envelope gene from the CCR5-tropic HIV-1 Ba-L. J. Acquir. Immune Defic. Syndr. 33:300-307.
37. 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.
38. Pejchal R, et al. 2011. A potent and broad neutralizing antibody recognizes and penetrates the HIV glycan shield. Science 334:1097-1103.
39. Picker LJ, et al. 2004. Insufficient production and tissue delivery of CD4+ memory T cells in rapidly progressive simian immunodeficiency virus infection. J. Exp. Med. 200:1299-1314.
40. Reed LJ, Muench H. 1938. A simple method of estimating fifty per cent endpoints. J. Am. Hyg. 27:493-497.
41. Reimann KA, et al. 1996. 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. 70:6922-6928.
42. Rickabaugh TM, et al. 2011. The dual impact of HIV-1 infection and aging on naive CD4 T-cells: additive and distinct patterns of impairment. PLoS One 6:e16459. doi:10.1371/journal.pone.0016459.
43. Rose NF, et al. 2001. An effective AIDS vaccine based on live attenuated vesicular stomatitis virus recombinants. Cell 106:539-549.
44. Seaman MS, et al. 2010. Tiered categorization of a diverse panel of HIV-1 Env pseudoviruses for assessment of neutralizing antibodies. J. Virol. 84: 1439-1452.
45. Shu Y, et al. 2007. Efficient protein boosting after plasmid DNA or recombinant adenovirus immunization with HIV-1 vaccine constructs. Vaccine 25:1398-1408.
46. Stone M, et al. 2010. A limited number of simian immunodeficiency virus (SIV) env variants are transmitted to rhesus macaques vaginally inoculated with SIVmac251. J. Virol. 84:7083-7095.
47. Tasca S, Ho SH, Cheng-Mayer C. 2008. R5X4 viruses are evolutionary, functional, and antigenic intermediates in the pathway of a simian-human immunodeficiency virus coreceptor switch. J. Virol. 82:7089-7099.
48. Trkola A, et al. 1996. Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J. Virol. 70:1100-1108.
49. Walker LM, et al. 2011. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477:466-470.
50. Walker LM, et al. 2011. Rapid development of glycan-specific, broad, and potent anti-HIV-1 gp120 neutralizing antibodies in an R5 SIV/HIV chimeric virus infected macaque. Proc. Natl. Acad. Sci. U. S. A. 108:20125-20129.
51. Willey RL, et al. 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.
52. Wu X, et al. 2010. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329:856-861.
53. Wu X, et al. 2011. Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing. Science 333:1593-1602.