Acute mucosal pathogenesis of feline immunodeficiency virus is independent of viral dose in vaginally infected cats

Retrovirology

Volumn 7, Issue , 2010, Pages

  Howard, Kristina E ^a   Reckling, Stacie K ^a   Egan, Erin A ^a,b   Dean, Gregg A ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b Immunobio   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CAT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FELINE IMMUNODEFICIENCY VIRUS; FEMALE; IMMUNOPATHOLOGY; INNATE IMMUNITY; MUCOSAL IMMUNITY; NATURAL KILLER CELL; NONHUMAN; VAGINITIS; VIREMIA; VIRUS LOAD; VIRUS REPLICATION; ANIMAL; ANIMAL DISEASE; CAT DISEASE; IMMUNOLOGY; INTESTINE MUCOSA; LENTIVIRUS INFECTION; PATHOGENICITY; PATHOLOGY; SECRETION; VAGINA; VIROLOGY;

ANIMALIA; FELINE IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

CYTOKINE;

ANIMALS; CAT DISEASES; CATS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; FEMALE; IMMUNODEFICIENCY VIRUS, FELINE; INTESTINAL MUCOSA; KILLER CELLS, NATURAL; LENTIVIRUS INFECTIONS; VAGINA; VIRAL LOAD; VIREMIA;

EID: 77649300653     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-7-2     Document Type: Article

References (90)

1. HIV vaccine failure prompts Merck to halt trial. Nature 2007, 449:390.
2. Vaccine trial discontinued. AIDS Patient Care STDS 2007, 21:778-779.
3. Cohen J. AIDS research. Promising AIDS vaccine's failure leaves field reeling. Science 2007, 318:28-29. 10.1126/science.318.5847.28, 17916696.
4. Priddy FH, Brown D, Kublin J, Monahan K, Wright DP, Lalezari J, Santiago S, Marmor M, Lally M, Novak RM, Brown SJ, Kulkarni P, Dubey SA, Kierstead LS, Casimiro DR, Mogg R, DiNubile MJ, Shiver JW, Leavitt RY, Robertson MN, Mehrotra DV, Quirk E, . Merck V520-016 Study Group Safety and immunogenicity of a replication-incompetent adenovirus type 5 HIV-1 clade B gag/pol/nef vaccine in healthy adults. Clin Infect Dis 2008, 46:1769-1781. 10.1086/587993, 18433307, Merck V520-016 Study Group.
5. Buchbinder SP, Mehrotra DV, Duerr A, Fitzgerald DW, Mogg R, Li D, Gilbert PB, Lama JR, Marmor M, Del Rio C, McElrath MJ, Casimiro DR, Gottesdiener KM, Chodakewitz JA, Corey L, Robertson MN, . Step Study Protocol Team Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet 2008, 372:1881-1893. 10.1016/S0140-6736(08)61591-3, 2721012, 19012954, Step Study Protocol Team.
6. Heeney JL, Plotkin SA. Immunological correlates of protection from HIV infection and disease. Nat Immunol 2006, 7:1281-1284. 10.1038/ni1206-1281, 17110946.
7. Betts MR, Nason MC, West SM, De Rosa SC, Migueles SA, Abraham J, Lederman MM, Benito JM, Goepfert PA, Connors M, Roederer M, Koup RA. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 2006, 107:4781-4789. 10.1182/blood-2005-12-4818, 1895811, 16467198.
8. Kaul R, Rowland-Jones SL, Kimani J, Fowke K, Dong T, Kiama P, Rutherford J, Njagi E, Mwangi F, Rostron T, Onyango J, Oyugi J, MacDonald KS, Bwayo JJ, Plummer FA. New insights into HIV-1 specific cytotoxic T-lymphocyte responses in exposed, persistently seronegative Kenyan sex workers. Immunol Lett 2001, 79:3-13. 10.1016/S0165-2478(01)00260-7, 11595284.
9. Addo MM, Draenert R, Rathod A, Verrill CL, Davis BT, Gandhi RT, Robbins GK, Basgoz NO, Stone DR, Cohen DE, Johnston MN, Flynn T, Wurcel AG, Rosenberg ES, Altfeld M, Walker BD. Fully differentiated HIV-1 specific CD8+ T effector cells are more frequently detectable in controlled than in progressive HIV-1 infection. PLoS ONE 2007, 2:e321. 10.1371/journal.pone.0000321, 1824710, 17389912.
10. Gea-Banacloche JC, Migueles SA, Martino L, Shupert WL, McNeil AC, Sabbaghian MS, Ehler L, Prussin C, Stevens R, Lambert L, Altman J, Hallahan CW, de Quiros JC, Connors M. Maintenance of large numbers of virus-specific CD8+ T cells in HIV-infected progressors and long-term nonprogressors. J Immunol 2000, 165:1082-1092.
11. Lamine A, Caumont-Sarcos A, Chaix ML, Saez-Cirion A, Rouzioux C, Delfraissy JF, Pancino G, Lambotte O. Replication-competent HIV strains infect HIV controllers despite undetectable viremia (ANRS EP36 study). Aids 2007, 21:1043-1045. 10.1097/QAD.0b013e3280d5a7ac, 17457100.
12. Saez-Cirion A, Lacabaratz C, Lambotte O, Versmisse P, Urrutia A, Boufassa F, Barre-Sinoussi F, Delfraissy JF, Sinet M, Pancino G, Venet A. HIV controllers exhibit potent CD8 T cell capacity to suppress HIV infection ex vivo and peculiar cytotoxic T lymphocyte activation phenotype. Proc Natl Acad Sci USA 2007, 104:6776-6781. 10.1073/pnas.0611244104, 1851664,1851664, 17428922.
13. Hladik F, Desbien A, Lang J, Wang L, Ding Y, Holte S, Wilson A, Xu Y, Moerbe M, Schmechel S, McElrath MJ. Most highly exposed seronegative men lack HIV-1-specific, IFN-gamma-secreting T cells. J Immunol 2003, 171:2671-2683.
14. Mansfield K, Lang SM, Gauduin MC, Sanford HB, Lifson JD, Johnson RP, Desrosiers RC. Vaccine protection by live, attenuated simian immunodeficiency virus in the absence of high-titer antibody responses and high-frequency cellular immune responses measurable in the periphery. J Virol 2008, 82:4135-4148. 10.1128/JVI.00015-08, 2292994, 18272584.
15. Nguyen M, Pean P, Lopalco L, Nouhin J, Phoung V, Ly N, Vermisse P, Henin Y, Barre-Sinoussi F, Burastero SE, Reynes JM, Carcelain G, Pancino G. HIV-specific antibodies but not t-cell responses are associated with protection in seronegative partners of HIV-1-infected individuals in Cambodia. J Acquir Immune Defic Syndr 2006, 42:412-419. 10.1097/01.qai.0000222289.97825.35, 16837821.
16. Schmechel SC, Russell N, Hladik F, Lang J, Wilson A, Ha R, Desbien A, McElrath MJ. Immune defence against HIV-1 infection in HIV-1-exposed seronegative persons. Immunol Lett 2001, 79:21-27. 10.1016/S0165-2478(01)00262-0, 11595286.
17. Sadoff JC, Wittes J. Correlates, surrogates, and vaccines. J Infect Dis 2007, 196:1279-1281. 10.1086/522432, 17922389.
18. Qin L, Gilbert PB, Corey L, McElrath MJ, Self SG. A framework for assessing immunological correlates of protection in vaccine trials. J Infect Dis 2007, 196:1304-1312. 10.1086/522428, 17922394.
19. Casimiro DR, Wang F, Schleif WA, Liang X, Zhang ZQ, Tobery TW, Davies ME, McDermott AB, O'Connor DH, Fridman A, Bagchi A, Tussey LG, Bett AJ, Finnefrock AC, Fu TM, Tang A, Wilson KA, Chen M, Perry HC, Heidecker GJ, Freed DC, Carella A, Punt KS, Sykes KJ, Huang L, Ausensi VI, Bachinsky M, Sadasivan-Nair U, Watkins DI, Emini EA, Shiver JW. Attenuation of simian immunodeficiency virus SIVmac239 infection by prophylactic immunization with dna and recombinant adenoviral vaccine vectors expressing Gag. J Virol 2005, 79:15547-15555. 10.1128/JVI.79.24.15547-15555.2005, 1315991, 16306625.
20. Wilson NA, Reed J, Napoe GS, Piaskowski S, Szymanski A, Furlott J, Gonzalez EJ, Yant LJ, Maness NJ, May GE, Soma T, Reynolds MR, Rakasz E, Rudersdorf R, McDermott AB, O'Connor DH, Friedrich TC, Allison DB, Patki A, Picker LJ, Burton DR, Lin J, Huang L, Patel D, Heindecker G, Fan J, Citron M, Horton M, Wang F, Liang X, Shiver JW, Casimiro DR, Watkins DI. Vaccine-induced cellular immune responses reduce plasma viral concentrations after repeated low-dose challenge with pathogenic simian immunodeficiency virus SIVmac239. J Virol 2006, 80:5875-5885. 10.1128/JVI.00171-06, 1472612, 16731926.
21. Mattapallil JJ, Douek DC, Buckler-White A, Montefiori D, Letvin NL, Nabel GJ, Roederer M. Vaccination preserves CD4 memory T cells during acute simian immunodeficiency virus challenge. J Exp Med 2006, 203:1533-1541. 10.1084/jem.20060657, 2118314, 16735692.
22. Buge SL, Murty L, Arora K, Kalyanaraman VS, Markham PD, Richardson ES, Aldrich K, Patterson LJ, Miller CJ, Cheng SM, Robert-Guroff M. Factors associated with slow disease progression in macaques immunized with an adenovirus-simian immunodeficiency virus (SIV) envelope priming- gp120 boosting regimen and challenged vaginally with SIVmac251. J Virol 1999, 73:7430-7440. 104270, 10438833.
23. Shiver JW, Fu TM, Chen L, Casimiro DR, Davies ME, Evans RK, Zhang ZQ, Simon AJ, Trigona WL, Dubey SA, Huang L, Harris VA, Long RS, Liang X, Handt L, Schleif WA, Zhu L, Freed DC, Persaud NV, Guan L, Punt KS, Tang A, Chen M, Wilson KA, Collins KB, Heidecker GJ, Fernandez VR, Perry HC, Joyce JG, Grimm KM, Cook JC, Keller PM, Kresock DS, Mach H, Troutman RD, Isopi LA, Williams DM, Xu Z, Bohannon KE, Volkin DB, Montefiori DC, Miura A, Krivulka GR, Lifton MA, Kuroda MJ, Schmitz JE, Letvin NL, Caulfield MJ, Bett AJ, Youil R, Kaslow DC, Emini EA. Replication-incompetent adenoviral vaccine vector elicits effective anti-immunodeficiency-virus immunity. Nature 2002, 415:331-335. 10.1038/415331a, 11797011.
24. Regoes RR, Longini IM, Feinberg MB, Staprans SI. Preclinical assessment of HIV vaccines and microbicides by repeated low-dose virus challenges. PLoS Med 2005, 2:e249. 10.1371/journal.pmed.0020249, 1176242,1176242, 16018721.
25. AIDS Epidemic Update:December 2008. WHO/UNAIDS Joint United Nations Programme on HIV/AIDS 2008,
26. Wilson DP, Law MG, Grulich AE, Cooper DA, Kaldor JM. Relation between HIV viral load and infectiousness: a model-based analysis. Lancet 2008, 372:314-320. 10.1016/S0140-6736(08)61115-0, 18657710.
27. Kaizu M, Weiler AM, Weisgrau KL, Vielhuber KA, May G, Piaskowski SM, Furlott J, Maness NJ, Friedrich TC, Loffredo JT, Usborne A, Rakasz EG. Repeated intravaginal inoculation with cell-associated simian immunodeficiency virus results in persistent infection of nonhuman primates. J Infect Dis 2006, 194:912-916. 10.1086/507308, 16960778.
28. Ma ZM, Abel K, Rourke T, Wang Y, Miller CJ. A period of transient viremia and occult infection precedes persistent viremia and antiviral immune responses during multiple low-dose intravaginal simian immunodeficiency virus inoculations. J Virol 2004, 78:14048-14052. 10.1128/JVI.78.24.14048-14052.2004, 533914, 15564513.
29. McDermott AB, Mitchen J, Piaskowski S, De Souza I, Yant LJ, Stephany J, Furlott J, Watkins DI. Repeated low-dose mucosal simian immunodeficiency virus SIVmac239 challenge results in the same viral and immunological kinetics as high-dose challenge: a model for the evaluation of vaccine efficacy in nonhuman primates. J Virol 2004, 78:3140-3144. 10.1128/JVI.78.6.3140-3144.2004, 353751, 14990733.
30. Assogba BD, Leavell S, Porter K, Burkhard MJ. Mucosal administration of low-dose cell-associated feline immunodeficiency virus promotes viral latency. J Infect Dis 2007, 195:1184-1188. 10.1086/512861, 17357056.
31. McChesney MB, Collins JR, Lu D, Lu X, Torten J, Ashley RL, Cloyd MW, Miller CJ. Occult systemic infection and persistent simian immunodeficiency virus (SIV)-specific CD4(+)-T-cell proliferative responses in rhesus macaques that were transiently viremic after intravaginal inoculation of SIV. J Virol 1998, 72:10029-10035. 110525, 9811741.
32. Zhu T, Corey L, Hwangbo Y, Lee JM, Learn GH, Mullins JI, McElrath MJ. Persistence of extraordinarily low levels of genetically homogeneous human immunodeficiency virus type 1 in exposed seronegative individuals. J Virol 2003, 77:6108-6116. 10.1128/JVI.77.11.6108-6116.2003, 154986, 12743268.
33. Nicastri E, Ercoli L, Sarmati L, d'Ettorre G, Iudicone P, Massetti P, Vullo V, Andreoni M. Human immunodeficiency virus-1 specific and natural cellular immunity in HIV seronegative subjects with multiple sexual exposures to virus. J Med Virol 2001, 64:232-237. 10.1002/jmv.1041, 11424109.
34. Pereyra F, Addo MM, Kaufmann DE, Liu Y, Miura T, Rathod A, Baker B, Trocha A, Rosenberg R, Mackey E, Ueda P, Lu Z, Cohen D, Wrin T, Petropoulos CJ, Rosenberg ES, Walker BD. Genetic and immunologic heterogeneity among persons who control HIV infection in the absence of therapy. J Infect Dis 2008, 197:563-571. 10.1086/526786, 18275276.
35. Tompkins MB, Nelson PD, English RV, Novotney C. Early events in the immunopathogenesis of feline retrovirus infections. J Am Vet Med Assoc 1991, 199:1311-1315.
36. English RV, Nelson P, Johnson CM, Nasisse M, Tompkins WA, Tompkins MB. Development of clinical disease in cats experimentally infected with feline immunodeficiency virus. J Infect Dis 1994, 170:543-552.
37. Sparkes AH, Hopper CD, Millard WG, Gruffydd-Jones TJ, Harbour DA. Feline immunodeficiency virus infection. Clinicopathologic findings in 90 naturally occurring cases. J Vet Intern Med 1993, 7:85-90.
38. Obert LA, Hoover EA. Feline immunodeficiency virus clade C mucosal transmission and disease courses. AIDS Res Hum Retroviruses 2000, 16:677-688. 10.1089/088922200308909, 10791878.
39. Allison RW, Hoover EA. Covert vertical transmission of feline immunodeficiency virus. AIDS Res Hum Retroviruses 2003, 19:421-434. 10.1089/088922203765551764, 12804000.
40. Dean GA, LaVoy A, Burkhard MJ. Peptide mapping of feline immunodeficiency virus by IFN-gamma ELISPOT. Vet Immunol Immunopathol 2004, 100:49M-59.
41. Krieger JN, Coombs RW, Collier AC, Ross SO, Chaloupka K, Cummings DK, Murphy VL, Corey L. Recovery of human immunodeficiency virus type 1 from semen: minimal impact of stage of infection and current antiviral chemotherapy. Infect Dis J 1991, 163:386-388.
42. Plummer FA, Simonsen JN, Cameron DW, Ndinya-Achola JO, Kreiss JK, Gakinya MN, Waiyaki P, Cheang M, Piot P, Ronald AR, et al. Cofactors in male-female sexual transmission of human immunodeficiency virus type 1. J Infect Dis 1991, 163:233-239.
43. Spinillo A, Zara F, De Santolo A, Brerra R, Maserati R, Romero E, Filice G. Quantitative assessment of cell-associated and cell-free virus in cervicovaginal samples of HIV-1-infected women. Clin Microbiol Infect 1999, 5:605-611. 10.1111/j.1469-0691.1999.tb00416.x, 11851690.
44. Politch JA, Wolff H, Hill JA, Anderson DJ. Comparison of methods to enumerate white blood cells in semen. Fertil Steril 1993, 60:372-375.
45. Wolff H, Anderson DJ. Male genital tract inflammation associated with increased numbers of potential human immunodeficiency virus host cells in semen. Andrologia 1988, 20:404-410.
46. Wolff H, Anderson DJ. Immunohistologic characterization and quantitation of leukocyte subpopulations in human semen. Fertil Steril 1988, 49:497-504.
47. Shacklett BL. Understanding the "lucky few": the conundrum of HIV-exposed, seronegative individuals. Curr HIV/AIDS Rep 2006, 3:26-31. 10.1007/s11904-006-0005-2, 16522256.
48. Dandekar S, Beebe AM, Barlough J, Phillips T, Elder J, Torten M, Pedersen N. Detection of feline immunodeficiency virus (FIV) nucleic acids in FIV- seronegative cats. J Virol 1992, 66:4040-4049. 241206, 1318395.
49. Sandy JR, Robinson WF, Bredhauer B, Kyaw-Tanner M, Howlett CR. Productive infection of the bone marrow cells in feline immunodeficiency virus infected cats. Arch Virol 2002, 147:1053-1059. 10.1007/s00705-001-0790-2, 12021873.
50. Rojko JL, Hoover EA, Quackenbush SL, Olsen RG. Reactivation of latent feline leukaemia virus infection. Nature 1982, 298:385-388. 10.1038/298385a0, 6283387.
51. Siebelink KH, Chu IH, Rimmelzwaan GF, Weijer K, Osterhaus AD, Bosch ML. Isolation and partial characterization of infectious molecular clones of feline immunodeficiency virus obtained directly from bone marrow DNA of a naturally infected cat. J Virol 1992, 66:1091-1097. 240813, 1309891.
52. Stevens R, Howard KE, Nordone S, Burkhard M, Dean GA. Oral immunization with recombinant listeria monocytogenes controls virus load after vaginal challenge with feline immunodeficiency virus. J Virol 2004, 78:8210-8218. 10.1128/JVI.78.15.8210-8218.2004, 446143, 15254192.
53. Sahu GK, Chen JJ, Huang JC, Ramsey KM, Cloyd MW. Transient or occult HIV-1 infection in high-risk adults. Aids 2001, 15:1175-1177. 10.1097/00002030-200106150-00013, 11416720.
54. Sahu GK, McNearney T, Evans A, Turner A, Weaver S, Huang JC, Baron S, Paar D, Cloyd MW. Transient or occult HIV infections may occur more frequently than progressive infections: changing the paradigm about HIV persistence. Arch Virol Suppl 2005, 131-145.
55. Tenenbaum SA, Morris CA, Alexander SS, McFerrin HE, Garry RF, Leissinger CA. Evidence of HIV exposure and transient seroreactivity in archived HIV-negative severe hemophiliac sera. Virol J 2005, 2:65. 10.1186/1743-422X-2-65, 1232868, 16107217.
56. Uberla K. HIV vaccine development in the aftermath of the STEP study: re-focus on occult HIV infection?. PLoS Pathog 2008, 4:e1000114. 10.1371/journal.ppat.1000114, 2517652, 18769723.
57. Fortis C, Poli G. Dendritic cells and natural killer cells in the pathogenesis of HIV infection. Immunol Res 2005, 33:1-21. 10.1385/IR:33:1:001, 16120969.
58. Alter G, Altfeld M. NK cells in HIV-1 infection: evidence for their role in the control of HIV-1 infection. J Intern Med 2009, 265:29-42. 10.1111/j.1365-2796.2008.02045.x, 19093958.
59. Scott-Algara D, Truong LX, Versmisse P, David A, Luong TT, Nguyen NV, Theodorou I, Barre-Sinoussi F, Pancino G. Cutting edge: increased NK cell activity in HIV-1-exposed but uninfected Vietnamese intravascular drug users. J Immunol 2003, 171:5663-5667.
60. O'Connell KA, Han Y, Williams TM, Siliciano RF, Blankson JN. Role of natural killer cells in a cohort of elite suppressors: low frequency of the protective KIR3DS1 allele and limited inhibition of human immunodeficiency virus type 1 replication in vitro. J Virol 2009, 83:5028-5034. 10.1128/JVI.02551-08, 2682110, 19211742.
61. Emu B, Sinclair E, Favre D, Moretto WJ, Hsue P, Hoh R, Martin JN, Nixon DF, McCune JM, Deeks SG. Phenotypic, functional, and kinetic parameters associated with apparent T-cell control of human immunodeficiency virus replication in individuals with and without antiretroviral treatment. J Virol 2005, 79:14169-14178. 10.1128/JVI.79.22.14169-14178.2005, 1280210, 16254352.
62. Daucher M, Price DA, Brenchley JM, Lamoreaux L, Metcalf JA, Rehm C, Nies-Kraske E, Urban E, Yoder C, Rock D, Gumkowski J, Betts MR, Dybul MR, Douek DC. Virological Outcome After Structured Interruption of Antiretroviral Therapy For HIV Infection is Associated with the Functional Profile of Virus-Specific CD8+ T-Cells. J Virol 2008, 82:4102-4114. 10.1128/JVI.02212-07, 2292997, 18234797.
63. Pahar B, Lackner AA, Piatak M, Lifson JD, Wang X, Das A, Ling B, Montefiori DC, Veazey RS. Control of viremia and maintenance of intestinal CD4(+) memory T cells in SHIV(162P3) infected macaques after pathogenic SIV(MAC251) challenge. Virology 2009, 387:273-284. 10.1016/j.virol.2009.02.014, 19298994.
64. Barry AP, Silvestri G, Safrit JT, Sumpter B, Kozyr N, McClure HM, Staprans SI, Feinberg MB. Depletion of CD8+ cells in sooty mangabey monkeys naturally infected with simian immunodeficiency virus reveals limited role for immune control of virus replication in a natural host species. J Immunol 2007, 178:8002-8012.
65. Schellens IM, Borghans JA, Jansen CA, De Cuyper IM, Geskus RB, van Baarle D, Miedema F. Abundance of early functional HIV-specific CD8+ T cells does not predict AIDS-free survival time. PLoS One 2008, 3:e2745. 10.1371/journal.pone.0002745, 2447878, 18648514.
66. Jiao Y, Xie J, Li T, Han Y, Qiu Z, Zuo L, Wang A. Correlation between gag-specific CD8 T-cell responses, viral load, and CD4 count in HIV-1 infection is dependent on disease status. J Acquir Immune Defic Syndr 2006, 42:263-268. 10.1097/01.qai.0000221692.00091.a2, 16763520.
67. Smith SM, Holland B, Russo C, Dailey PJ, Marx PA, Connor RI. Retrospective analysis of viral load and SIV antibody responses in rhesus macaques infected with pathogenic SIV: predictive value for disease progression. AIDS Res Hum Retroviruses 1999, 15:1691-1701. 10.1089/088922299309739, 10606092.
68. Beer BE, Brown CR, Whitted S, Goldstein S, Goeken R, Plishka R, Buckler-White A, Hirsch VM. Immunodeficiency in the absence of high viral load in pig-tailed macaques infected with Simian immunodeficiency virus SIVsun or SIVlhoest. J Virol 2005, 79:14044-14056. 10.1128/JVI.79.22.14044-14056.2005, 1280237, 16254339.
69. Staprans SI, Barry AP, Silvestri G, Safrit JT, Kozyr N, Sumpter B, Nguyen H, McClure H, Montefiori D, Cohen JI, Feinberg MB. Enhanced SIV replication and accelerated progression to AIDS in macaques primed to mount a CD4 T cell response to the SIV envelope protein. Proc Natl Acad Sci USA 2004, 101:13026-13031. 10.1073/pnas.0404739101, 516468, 15326293.
70. Bruck C, Thiriart C, Fabry L, Francotte M, Pala P, Van Opstal O, Culp J, Rosenberg M, De Wilde M, Heidt P, Heeney J. HIV-1 envelope-elicited neutralizing antibody titres correlate with protection and virus load in chimpanzees. Vaccine 1994, 12:1141-1148. 10.1016/0264-410X(94)90185-6, 7998425.
71. Cao Y, Qin L, Zhang L, Safrit J, Ho DD. Virologic and immunologic characterization of long-term survivors of human immunodeficiency virus type 1 infection. N Engl J Med 1995, 332:201-208. 10.1056/NEJM199501263320401, 7808485.
72. Harrer T, Harrer E, Kalams SA, Elbeik T, Staprans SI, Feinberg MB, Cao Y, Ho DD, Yilma T, Caliendo AM, Johnson RP, Buchbinder SP, Walker BD. Strong cytotoxic T cell and weak neutralizing antibody responses in a subset of persons with stable nonprogressing HIV type 1 infection. AIDS Res Hum Retroviruses 1996, 12:585-592. 10.1089/aid.1996.12.585, 8743084.
73. Montefiori DC, Pantaleo G, Fink LM, Zhou JT, Zhou JY, Bilska M, Miralles GD, Fauci AS. Neutralizing and infection-enhancing antibody responses to human immunodeficiency virus type 1 in long-term nonprogressors. J Infect Dis 1996, 173:60-67.
74. Bailey JR, Lassen KG, Yang HC, Quinn TC, Ray SC, Blankson JN, Siliciano RF. Neutralizing antibodies do not mediate suppression of human immunodeficiency virus type 1 in elite suppressors or selection of plasma virus variants in patients on highly active antiretroviral therapy. J Virol 2006, 80:4758-4770. 10.1128/JVI.80.10.4758-4770.2006, 1472047, 16641269.
75. Brenchley JM, Schacker TW, Ruff LE, Price DA, Taylor JH, Beilman GJ, Nguyen PL, Khoruts A, Larson M, Haase AT, Douek DC. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 2004, 200:749-759. 10.1084/jem.20040874, 2211962, 15365096.
76. Mattapallil JJ, Douek DC, Hill B, Nishimura Y, Martin M, Roederer M. Massive infection and loss of memory CD4+ T cells in multiple tissues during acute SIV infection. Nature 2005, 434:1093-1097. 10.1038/nature03501, 15793563.
77. Mehandru S, Poles MA, Tenner-Racz K, Horowitz A, Hurley A, Hogan C, Boden D, Racz P, Markowitz M. Primary HIV-1 infection is associated with preferential depletion of CD4+ T lymphocytes from effector sites in the gastrointestinal tract. J Exp Med 2004, 200:761-770. 10.1084/jem.20041196, 2211967, 15365095.
78. Veazey RS, DeMaria M, Chalifoux LV, Shvetz DE, Pauley DR, Knight HL, Rosenzweig M, Johnson RP, Desrosiers RC, Lackner AA. Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science 1998, 280:427-431. 10.1126/science.280.5362.427, 9545219.
79. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, Kazzaz Z, Bornstein E, Lambotte O, Altmann D, Blazar BR, Rodriguez B, Teixeira-Johnson L, Landay A, Martin JN, Hecht FM, Picker LJ, Lederman MM, Deeks SG, Douek DC. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006, 12:1365-1371. 10.1038/nm1511, 17115046.
80. Sankaran S, George MD, Reay E, Guadalupe M, Flamm J, Prindiville T, Dandekar S. Rapid onset of intestinal epithelial barrier dysfunction in primary human immunodeficiency virus infection is driven by an imbalance between immune response and mucosal repair and regeneration. J Virol 2008, 82:538-545. 10.1128/JVI.01449-07, 2224350, 17959677.
81. Howard KE, Burkhard MJ. Mucosal challenge with cell-associated or cell-free feline immunodeficiency virus induces rapid and distinctly different patterns of phenotypic change in the mucosal and systemic immune systems. Immunology 2007, 122:571-583. 10.1111/j.1365-2567.2007.02673.x, 2266040, 17635613.
82. Pandrea IV, Gautam R, Ribeiro RM, Brenchley JM, Butler IF, Pattison M, Rasmussen T, Marx PA, Silvestri G, Lackner AA, Perelson AS, Douek DC, Veazey RS, Apetrei C. Acute loss of intestinal CD4+ T cells is not predictive of simian immunodeficiency virus virulence. J Immunol 2007, 179:3035-3046. 2367134, 17709518.
83. Burkhard MJ, Mathiason CK, Bowdre T, Hoover EA. Feline immunodeficiency virus Gag- and Env-specific immune responses after vaginal versus intravenous infection. AIDS Res Hum Retroviruses 2001, 17:1767-1778. 10.1089/08892220152741469, 11788028.
84. Howard KE, Fisher IL, Dean GA, Burkhard MJ. Methodology for isolation and phenotypic characterization of feline small intestinal leukocytes. J Immunol Methods 2005, 302:36-53. 10.1016/j.jim.2005.04.019, 16023664.
85. Ignacio G, Nordone S, Howard KE, Dean GA. Toll-like receptor expression in feline lymphoid tissues. Vet Immunol Immunopathol 2005, 106:229-237. 10.1016/j.vetimm.2005.02.022, 15963821.
86. Burkhard MJ, Valenski L, Leavell S, Dean GA, Tompkins WA. Evaluation of FIV protein-expressing VEE-replicon vaccine vectors in cats. Vaccine 2002, 21:258-268. 10.1016/S0264-410X(02)00455-3, 12450701.
87. Pedersen NC, Leutenegger CM, Woo J, Higgins J. Virulence differences between two field isolates of feline immunodeficiency virus (FIV-APetaluma and FIV-CPGammar) in young adult specific pathogen free cats. Vet Immunol Immunopathol 2001, 79:53-67. 10.1016/S0165-2427(01)00252-5, 11356250.
88. Reid G, Rigby MA, McDonald M, Hosie MJ, Neil JC, Jarrett O. Immunodiagnosis of feline immunodeficiency virus infection using recombinant viral p17 and p24. Aids 1991, 5:1477-1483. 10.1097/00002030-199112000-00010, 1667575.
89. Staats HF, Nichols WG, Palker TJ. Mucosal immunity to HIV-1: systemic and vaginal antibody responses after intranasal immunization with the HIV-1 C4/V3 peptide T1SP10 MN(A). J Immunol 1996, 157:462-472.
90. de Parseval A, Elder JH. Binding of recombinant feline immunodeficiency virus surface glycoprotein to feline cells: role of CXCR4, cell-surface heparans, and an unidentified non-CXCR4 receptor. J Virol 2001, 75:4528-4539. 10.1128/JVI.75.10.4528-4539.2001, 114206, 11312323.