Association between cellular immune activation, target cell frequency, and risk of human immunodeficiency virus type 1 superinfection

Journal of Virology

Volumn 88, Issue 10, 2014, Pages 5894-5899

  Blish, Catherine A ^a,b,e   Dogan, Ozge C ^a   Jaoko, Walter ^c   McClelland, R Scott ^b,c   Mandaliya, Kishorchandra ^d   Odem Davis, Katherine ^a   Richardson, Barbra A ^a,b   Overbaugh, Julie ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF NAIROBI   (Kenya)

^d Department of Obstetrics and Gynaecology   (Kenya)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CASE CONTROL STUDY; CD4 LYMPHOCYTE COUNT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNE RESPONSE; IMMUNOREACTIVITY; INFECTION RISK; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; RISK FACTOR; SUPERINFECTION; T LYMPHOCYTE ACTIVATION; VIRUS LOAD; VIRUS REPLICATION; VIRUS STRAIN;

CASE-CONTROL STUDIES; FEMALE; HIV INFECTIONS; HIV-1; HUMANS; SUPERINFECTION;

EID: 84899088732     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00187-14     Document Type: Article

References (45)

1. Giorgi JV, Hultin LE, McKeating JA, Johnson TD, Owens B, Jacobson LP, Shih R, Lewis J, Wiley DJ, Phair JP, Wolinsky SM, Detels R. 1999. Shorter survival in advanced human immunodeficiency virus type 1 infection is more closely associated with T lymphocyte activation than with plasma virus burden or virus chemokine coreceptor usage. J. Infect. Dis. 179:859-870. http://dx.doi.org/10.1086/314660.
2. Lawn SD, Butera ST, Folks TM. 2001. Contribution of immune activation to the pathogenesis and transmission of human immunodeficiency virus type 1 infection. Clin. Microbiol. Rev. 14:753-777. http://dx.doi.org/10.1128/CMR.14.4.753-777.2001.
3. Card CM, Ball TB, Fowke KR. 2013. Immune quiescence: a model of protection against HIV infection. Retrovirology 10:141. http://dx.doi.org/10.1186/1742-4690-10-141.
4. Salkowitz JR, Purvis SF, Meyerson H, Zimmerman P, O'Brien TR, Aledort L, Eyster ME, Hilgartner M, Kessler C, Konkle BA, White GC, II, Goedert JJ, Lederman MM. 2001. Characterization of high-risk HIV-1 seronegative hemophiliacs. Clin. Immunol. 98:200-211. http://dx.doi.org/10.1006/clim.2000.4969.
5. Bégaud E, Chartier L, Marechal V, Ipero J, Léal J, Versmisse P, Breton G, Fontanet A, Capoulade-Metay C, Fleury H, Barré-Sinoussi F, Scott- Algara D, Pancino G. 2006. Reduced CD4 T cell activation and in vitro susceptibility to HIV-1 infection in exposed uninfected Central Africans. Retrovirology 3:35. http://dx.doi.org/10.1186/1742-4690-3-35.
6. Koning FA, Otto SA, Hazenberg MD, Dekker L, Prins M, Miedema F, Schuitemaker H. 2005. Low-level CD4+ T cell activation is associated with low susceptibility to HIV-1 infection. J. Immunol. 175:6117- 6122.
7. Chege D, Chai Y, Huibner S, Kain T, Wachihi C, Kimani M, Barasa S, McKinnon LR, Muriuki FK, Kariri A, Jaoko W, Anzala O, Kimani J, Ball TB, Plummer FA, Kaul R. 2012. Blunted IL17/IL22 and proinflammatory cytokine responses in the genital tract and blood of HIVexposed, seronegative female sex workers in Kenya. PLoS One 7:e43670. http://dx.doi.org/10.1371/journal.pone.0043670.
8. Legrand FA, Nixon DF, Loo CP, Ono E, Chapman JM, Miyamoto M, Diaz RS, Santos AM, Succi RC, Abadi J, Rosenberg MG, De Moraes-Pinto MI, Kallas EG. 2006. Strong HIV-1-specific T cell responses in HIV-1-exposed uninfected infants and neonates revealed after regulatory T cell removal. PLoS One 1:e102. http://dx.doi.org/10.1371/journal.pone.0000102.
9. Card CM, McLaren PJ, Wachihi C, Kimani J, Plummer FA, Fowke KR. 2009. Decreased immune activation in resistance to HIV-1 infection is associated with an elevated frequency of CD4(+)CD25(+)FOXP3(+) regulatory T cells. J. Infect. Dis. 199:1318-1322. http://dx.doi.org/10.1086/597801.
10. Camara M, Dieye TN, Seydi M, Diallo AA, Fall M, Diaw PA, Sow PS, Mboup S, Kestens L, Jennes W. 2010. Low-level CD4+ T cell activation in HIV-exposed seronegative subjects: influence of gender and condom use. J. Infect. Dis. 201:835-842. http://dx.doi.org/10.1086/651000.
11. Lajoie J, Juno J, Burgener A, Rahman S, Mogk K, Wachihi C, Mwanjewe J, Plummer FA, Kimani J, Ball TB, Fowke KR. 2012. A distinct cytokine and chemokine profile at the genital mucosa is associated with HIV-1 protection among HIV-exposed seronegative commercial sex workers. Mucosal Immunol. 5:277-287. http://dx.doi.org/10.1038/mi.2012.7.
12. McLaren PJ, Ball TB, Wachihi C, Jaoko W, Kelvin DJ, Danesh A, Kimani J, Plummer FA, Fowke KR. 2010. HIV-exposed seronegative commercial sex workers show a quiescent phenotype in the CD4+ T cell compartment and reduced expression of HIV-dependent host factors. J. Infect. Dis. 202:S339-S344. http://dx.doi.org/10.1086/655968.
13. Naranbhai V, Abdool Karim SS, Altfeld M, Samsunder N, Durgiah R, Sibeko S, Abdool Karim Q, Carr WH, CAPRISA004 TRAPS team. 2012. Innate immune activation enhances HIV acquisition in women, diminishing the effectiveness of tenofovir microbicide gel. J. Infect. Dis. 206: 993-1001. http://dx.doi.org/10.1093/infdis/jis465.
14. Songok EM, Luo M, Liang B, McLaren P, Kaefer N, Apidi W, Boucher G, Kimani J, Wachihi C, Sekaly R, Fowke K, Ball BT, Plummer FA. 2012. Microarray analysis of HIV resistant female sex workers reveal a gene expression signature pattern reminiscent of a lowered immune activation state. PLoS One 7:e30048. http://dx.doi.org/10.1371/journal.pone.0030048.
15. Yao X-D, Omange RW, Henrick BM, Lester RT, Kimani J, Ball TB, Plummer FA, Rosenthal KL. 26 June 2013. Acting locally: innate mucosal immunity in resistance to HIV-1 infection in Kenyan commercial sex workers. Mucosal Immunol. http://dx.doi.org/10.1038/mi.2013.44.
16. Jennes W, Evertse D, Borget M-Y, Vuylsteke B, Maurice C, Nkengasong JN, Kestens L. 2006. Suppressed cellular alloimmune responses in HIVexposed seronegative female sex workers. Clin. Exp. Immunol. 143:435- 444. http://dx.doi.org/10.1111/j.1365-2249.2006.03017.x.
17. Tran HK, Chartier L, Troung LX, Nguyen NN, Fontanet A, Barré-Sinoussi FE, Pancino G, Scott-Algara D. 2006. Systemic immune activation in HIV-1-exposed uninfected Vietnamese intravascular drug users. AIDS Res. Hum. Retroviruses 22:255-261. http://dx.doi.org/10.1089/aid.2006.22.255.
18. Biasin M, Caputo SL, Speciale L, Colombo F, Racioppi L, Zagliani A, Blé C, Vichi F, Cianferoni L, Masci AM, Villa ML, Ferrante P, Mazzotta F, Clerici M. 2000. Mucosal and systemic immune activation is present in human immunodeficiency virus-exposed seronegative women. J. Infect. Dis. 182:1365-1374. http://dx.doi.org/10.1086/315873.
19. Restrepo C, Rallón NI, Carrillo J, Soriano V, Blanco J, Benito JM. 2011. Host factors involved in low susceptibility to HIV infection. AIDS Rev. 13:30-40.
20. Suy A, Castro P, Nomdedeu M, García F, López A, Fumero E, Gallart T, Lopalco L, Coll O, Gatell JM, Plana M. 2007. Immunological profile of heterosexual highly HIV-exposed uninfected individuals: predominant role of CD4 and CD8 T-cell activation. J. Infect. Dis. 196:1191-1201. http://dx.doi.org/10.1086/521193.
21. Rowland-Jones SL, Dong T, Fowke KR, Kimani J, Krausa P, Newell H, Blanchard T, Ariyoshi K, Oyugi J, Ngugi E, Bwayo J, Macdonald KS, Mcmichael AJ, Plummer FA. 1998. Cytotoxic T cell responses to multiple conserved HIV epitopes in HIV-resistant prostitutes in Nairobi. J. Clin. Invest. 102:1758-1765. http://dx.doi.org/10.1172/JCI4314.
22. Fowke KR, Kaul R, Rosenthal KL, Oyugi J, Kimani J, Rutherford WJ, Nagelkerke NJ, Ball TB, Bwayo JJ, Simonsen JN, Shearer GM, Plummer FA. 2000. HIV-1-specific cellular immune responses among HIV-1-resistant sex workers. Immunol. Cell Biol. 78:586-595. http://dx.doi.org/10.1046/j.1440-1711.2000.00944.x.
23. Lo Caputo S, Trabattoni D, Vichi F, Piconi S, Lopalco L, Villa ML, Mazzotta F, Clerici M. 2003. Mucosal and systemic HIV-1-specific immunity in HIV-1-exposed but uninfected heterosexual men. AIDS 17: 531-539. http://dx.doi.org/10.1097/00002030-200303070-00008.
24. Pattacini L, Murnane PM, Kahle EM, Bolton MJ, Delrow JJ, Lingappa JR, Katabira E, Donnell D, McElrath MJ, Baeten JM, Lund JM. 2013. Differential regulatory T cell activity in HIV type 1-exposed seronegative individuals. AIDS Res. Hum. Retroviruses 29:1321-1329. http://dx.doi.org/10.1089/aid.2013.0075.
25. Carrillo J, Restrepo C, Rallón NI, Massanella M, del Romero J, Rodríguez C, Soriano V, Clotet B, Benito JM, Blanco J. 2013. HIV exposed seronegative individuals show antibodies specifically recognizing native HIV envelope glycoprotein. AIDS 27:1375-1385. http://dx.doi.org/10.1097/QAD.0b013e32835fac08.
26. Restrepo C, Rallón NI, del Romero J, Rodríguez C, Hernando V, López M, Peris A, Lozano S, Sempere-Ortells JM, Soriano V, Benito JM. 2010. Low-level exposure to HIV induces virus-specific T cell responses and immune activation in exposed HIV-seronegative individuals. J. Immunol. 185:982-989. http://dx.doi.org/10.4049/jimmunol.1000221.
27. Buchbinder SP, Mehrotra DV, Duerr A, Fitzgerald DW, Mogg R, Li D, Gilbert PB, Lama JR, Marmor M, Rio CD, McElrath MJ, Casimiro DR, Gottesdiener KM, Chodakewitz JA, Corey L, Robertson MN. 2008. Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet 372:1881-1893. http://dx.doi.org/10.1016/S0140-6736(08)61591-3.
28. McElrath MJ, De Rosa SC, Moodie Z, Dubey S, Kierstead L, Janes H, Defawe OD, Carter DK, Hural J, Akondy R, Buchbinder SP, Robertson MN, Mehrotra DV, Self SG, Corey L, Shiver JW, Casimiro DR. 2008. HIV-1 vaccine-induced immunity in the test-of-concept Step Study: a case-cohort analysis. Lancet 372:1894-1905. http://dx.doi.org/10.1016/S0140-6736(08)61592-5.
29. Haynes BF, Gilbert PB, McElrath MJ, Zolla-Pazner S, Tomaras GD, Alam SM, Evans DT, Montefiori DC, Karnasuta C, Sutthent R, Liao H-X, DeVico AL, Lewis GK, Williams C, Pinter A, Fong Y, Janes H, Decamp A, Huang Y, Rao M, Billings E, Karasavvas N, Robb ML, Ngauy V, de Souza MS, Paris R, Ferrari G, Bailer RT, Soderberg KA, Andrews C, Berman PW, Frahm N, De Rosa SC, Alpert MD, Yates NL, Shen X, Koup RA, Pitisuttithum P, Kaewkungwal J, Nitayaphan S, Rerks-Ngarm S, Michael NL, Kim JH. 2012. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N. Engl. J. Med. 366:1275-1286. http://dx.doi.org/10.1056/NEJMoa1113425.
30. Chohan B, Lavreys L, Rainwater SMJ, Overbaugh J. 2005. Evidence for frequent reinfection with human immunodeficiency virus type 1 of a different subtype. J. Virol. 79:10701-10708. http://dx.doi.org/10.1128/JVI.79.16.10701-10708.2005.
31. Piantadosi A, Chohan B, Chohan V, Mcclelland RS, Overbaugh J. 2007. Chronic HIV-1 infection frequently fails to protect against superinfection. PLoS Pathog. 3:e177. http://dx.doi.org/10.1371/journal.ppat.0030177.
32. Piantadosi A, Ngayo MO, Chohan B, Overbaugh J. 2008. Examination of a second region of the HIV type 1 genome reveals additional cases of superinfection. AIDS Res. Hum. Retroviruses 24:1221. http://dx.doi.org/10.1089/aid.2008.0100.
33. Blish CA, Dogan OC, Derby NR, Nguyen M-A, Chohan B, Richardson BA, Overbaugh J. 2008. Human immunodeficiency virus type 1 superinfection occurs despite relatively robust neutralizing antibody responses. J. Virol. 82:12094-12103. http://dx.doi.org/10.1128/JVI.01730-08.
34. Blish CA, Dogan OC, Jaoko W, Mcclelland RS, Mandaliya KK, Odem-Davis KSK, Richardsonb BA, Overbaugh J. 2012. Cellular immune responses and susceptibility to HIV-1 superinfection: a case-control study. AIDS 26:643-646. http://dx.doi.org/10.1097/QAD.0b013e3283509a0b.
35. Forthal DN, Landucci G, Chohan B, Richardson BA, McClelland RS, Jaoko W, Blish C, Overbaugh J. 2013. Antibody-dependent cellmediated virus inhibition antibody activity does not correlate with risk of HIV-1 superinfection. J. Acquir. Immune Defic. Syndr. 63:31-33. http://dx.doi.org/10.1097/QAI.0b013e3182874d41.
36. Smith DM, Strain MC, Frost SDW, Pillai SK, Wong JK, Wrin T, Liu Y, Petropolous CJ, Daar ES, Little SJ, Richman DD. 2006. Lack of neutralizing antibody response to HIV-1 predisposes to superinfection. Virology 355:1-5. http://dx.doi.org/10.1016/j.virol.2006.08.009.
37. Chaillon A, Wagner GA, Hepler NL, Little SJ, Kosakovsky Pond SL, Caballero G, Pacold ME, Phung P, Wrin T, Richman DD, Wertheim JO, Smith DM. 2013. Dynamics of viral evolution and neutralizing antibody response after HIV-1 superinfection. J. Virol. 87:12737-12744. http://dx.doi.org/10.1128/JVI.02260-13.
38. Basu D, Kraft CS, Murphy MK, Campbell PJ, Yu T, Hraber PT, Irene C, Pinter A, Chomba E, Mulenga J, Kilembe W, Allen SA, Derdeyn CA, Hunter E. 2012. HIV-1 subtype C superinfected individuals mount low autologous neutralizing antibody responses prior to intrasubtype superinfection. Retrovirology 9:76. http://dx.doi.org/10.1186/1742-4690-9-76.
39. Altfeld M, Allen TM, Yu XG, Johnston MN, Agrawal D, Korber BT, Montefiori DC, O'Connor DH, Davis BT, Lee PK, Maier EL, Harlow J, Goulder PJR, Brander C, Rosenberg ES, Walker BD. 2002. HIV-1 superinfection despite broad CD8+ T-cell responses containing replication of the primary virus. Nature 420:434-439. http://dx.doi.org/10.1038/nature01200.
40. Appay V, Dunbar PR, Callan M, Klenerman P, Gillespie GMA, Papagno L, Ogg GS, King A, Lechner F, Spina CA, Little S, Havlir DV, Richman DD, Gruener N, Pape G, Waters A, Easterbrook P, Salio M, Cerundolo V, Mcmichael AJ, Rowland-Jones SL. 2002. Memory CD8+ T cells vary in differentiation phenotype in different persistent virus infections. Nat. Med. 8:379-385. http://dx.doi.org/10.1038/nm0402-379.
41. Deeks SG. 2004. Immune activation set point during early HIV infection predicts subsequent CD4+ T-cell changes independent of viral load. Blood 104:942-947. http://dx.doi.org/10.1182/blood-2003-09-3333.
42. Giorgi JV, Lyles RH, Matud JL, Yamashita TE, Mellors JW, Hultin LE, Jamieson BD, Margolick JB, Rinaldo CR, Phair JP, Detels R, Detels R, Multicenter AIDS Cohort Study. 2002. Predictive value of immunologic and virologic markers after long or short duration of HIV-1 infection. J. Acquir. Immune Defic. Syndr. 29:346-355.
43. Liu ZZ, Cumberland WGW, Hultin LEL, Kaplan AHA, Detels RR, Giorgi JVJ. 1998. CD8+ T-lymphocyte activation in HIV-1 disease reflects an aspect of pathogenesis distinct from viral burden and immunodeficiency. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 18:332-340. http://dx.doi.org/10.1097/00042560-199808010-00004.
44. Ronen K, McCoy CO, Matsen FA, Boyd DF, Emery S, Odem-Davis K, Jaoko W, Mandaliya K, Mcclelland RS, Richardson BA, Overbaugh J. 2013. HIV-1 superinfection occurs less frequently than initial infection in a cohort of high-risk Kenyan women. PLoS Pathog. 9:e1003593. http://dx.doi.org/10.1371/journal.ppat.1003593.
45. Redd AD, Quinn TC, Tobian AA. 2013. Frequency and implications of HIV superinfection. Lancet Infect. Dis. 13:622-628. http://dx.doi.org/10.1016/S1473-3099(13)70066-5.