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Frontiers of Medicine

, Volume 11, Issue 4, pp 480–489 | Cite as

Immunological and virological characteristics of human immunodeficiency virus type 1 superinfection: implications in vaccine design

  • Yang Gao
  • Wen Tian
  • Xiaoxu HanEmail author
  • Feng GaoEmail author
Review

Abstract

Superinfection is frequently detected among individuals infected by human immunodeficiency virus type I (HIV-1). Superinfection occurs at similar frequencies at acute and chronic infection stages but less frequently than primary infection. This observation indicates that the immune responses elicited by natural HIV-1 infection may play a role in curb of superinfection; however, these responses are not sufficiently strong to completely prevent superinfection. Thus, a successful HIV-1 vaccine likely needs to induce more potent and broader immune responses than those elicited by primary infection. On the other hand, potent and broad neutralization responses are more often detected after superinfection than during monoinfection. This suggests that broadly neutralizing antibodies are more likely induced by sequential immunization of multiple different immunogens than with only one form of envelope glycoprotein immunogens. Understanding why the protection from superinfection by immunity induced by primary infection is insufficient and if superinfection can lead to cross-reactive immune responses will be highly informative for HIV-1 vaccine design.

Keywords

human immunodeficiency virus type I superinfection incidence immune response 

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Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Nos. 31670162 and 81371787), Program for JLU Science and Technology Innovative Research Team (No. 2017TD-05), and a grant from NIAID of NIH (No. AI118571).

References

  1. 1.
    Allen TM, Altfeld M. HIV-1 superinfection. J Allergy Clin Immunol 2003; 112(5): 829–835, quiz 836CrossRefPubMedGoogle Scholar
  2. 2.
    Smith DM, Richman DD, Little SJ. HIV superinfection. J Infect Dis 2005; 192(3): 438–444CrossRefPubMedGoogle Scholar
  3. 3.
    Waters L, Smit E. HIV-1 superinfection. Curr Opin Infect Dis 2012; 25(1): 42–50CrossRefPubMedGoogle Scholar
  4. 4.
    Ramos A, Hu DJ, Nguyen L, Phan KO, Vanichseni S, Promadej N, Choopanya K, Callahan M, Young NL, McNicholl J, Mastro TD, Folks TM, Subbarao S. Intersubtype human immunodeficiency virus type 1 superinfection following seroconversion to primary infection in two injection drug users. J Virol 2002; 76(15): 7444–7452CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Manigart O, Courgnaud V, Sanou O, Valéa D, Nagot N, Meda N, Delaporte E, Peeters M, Van de Perre P. HIV-1 superinfections in a cohort of commercial sex workers in Burkina Faso as assessed by an autologous heteroduplex mobility procedure. AIDS 2004; 18(12): 1645–1651CrossRefPubMedGoogle Scholar
  6. 6.
    Hu DJ, Subbarao S, Vanichseni S, Mock PA, Ramos A, Nguyen L, Chaowanachan T, Griensven Fv, Choopanya K, Mastro TD, Tappero JW. Frequency of HIV-1 dual subtype infections, including intersubtype superinfections, among injection drug users in Bangkok, Thailand. AIDS 2005; 19(3): 303–308PubMedGoogle Scholar
  7. 7.
    Smith DM, Strain MC, Frost SD, Pillai SK, Wong JK, Wrin T, Liu Y, Petropolous CJ, Daar ES, Little SJ, Richman DD. Lack of neutralizing antibody response to HIV-1 predisposes to superinfection. Virology 2006; 355(1): 1–5CrossRefPubMedGoogle Scholar
  8. 8.
    Redd AD, Collinson-Streng A, Martens C, Ricklefs S, Mullis CE, Manucci J, Tobian AA, Selig EJ, Laeyendecker O, Sewankambo N, Gray RH, Serwadda D, Wawer MJ, Porcella SF, Quinn TC; Rakai Health Sciences Program. Identification of HIV superinfection in seroconcordant couples in Rakai, Uganda, by use of next-generation deep sequencing. J Clin Microbiol 2011; 49(8): 2859–2867CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Redd AD, Ssemwanga D, Vandepitte J, Wendel SK, Ndembi N, Bukenya J, Nakubulwa S, Grosskurth H, Parry CM, Martens C, Bruno D, Porcella SF, Quinn TC, Kaleebu P. Rates of HIV-1 superinfection and primary HIV-1 infection are similar in female sex workers in Uganda. AIDS 2014; 28(14): 2147–2152CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Redd AD, Mullis CE, Serwadda D, Kong X, Martens C, Ricklefs SM, Tobian AA, Xiao C, Grabowski MK, Nalugoda F, Kigozi G, Laeyendecker O, Kagaayi J, Sewankambo N, Gray RH, Porcella SF, Wawer MJ, Quinn TC. The rates of HIV superinfection and primary HIV incidence in a general population in Rakai, Uganda. J Infect Dis 2012; 206(2): 267–274CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    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 PJ, Brander C, Rosenberg ES, Walker BD. HIV-1 superinfection despite broad CD8+ T-cell responses containing replication of the primary virus. Nature 2002; 420(6914): 434–439CrossRefPubMedGoogle Scholar
  12. 12.
    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. HIV-1 subtype C superinfected individuals mount low autologous neutralizing antibody responses prior to intrasubtype superinfection. Retrovirology 2012; 9(1): 76CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Basu D, Xiao P, Ende Z, Bere A, Britt WJ, Mulenga J, Kilembe W, Allen SA, Derdeyn CA, Hunter E. Low antibody-dependent cellular cytotoxicity responses in Zambians prior to HIV-1 intrasubtype C superinfection. Virology 2014; 462–463: 295–298CrossRefPubMedGoogle Scholar
  14. 14.
    Blish CA, Dogan OC, Derby NR, Nguyen MA, Chohan B, Richardson BA, Overbaugh J. Human immunodeficiency virus type 1 superinfection occurs despite relatively robust neutralizing antibody responses. J Virol 2008; 82(24): 12094–12103CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Sun M, Zheng H, Xie Y, Li B, Long H, Guo G, Guo L, Wang J, Ning R, Li Y, Liu L. Functional effector memory T cells contribute to protection from superinfection with heterologous simian immunodeficiency virus or simian-human immunodeficiency virus isolates in Chinese rhesus macaques. Arch Virol 2017; 162(5): 1211–1221CrossRefPubMedGoogle Scholar
  16. 16.
    Cortez V, Wang B, Dingens A, Chen MM, Ronen K, Georgiev IS, McClelland RS, Overbaugh J. The broad neutralizing antibody responses after HIV-1 superinfection are not dominated by antibodies directed to epitopes common in single infection. PLoS Pathog 2015; 11(7): e1004973CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Powell RL, Kinge T, Nyambi PN. Infection by discordant strains of HIV-1 markedly enhances the neutralizing antibody response against heterologous virus. J Virol 2010; 84(18): 9415–9426CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Cortez V, Odem-Davis K, McClelland RS, Jaoko W, Overbaugh J. HIV-1 superinfection in women broadens and strengthens the neutralizing antibody response. PLoS Pathog 2012; 8(3): e1002611CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Jost S, Bernard MC, Kaiser L, Yerly S, Hirschel B, Samri A, Autran B, Goh LE, Perrin L. A patient with HIV-1 superinfection. N Engl J Med 2002; 347(10): 731–736CrossRefPubMedGoogle Scholar
  20. 20.
    van der Kuyl AC, Cornelissen M. Identifying HIV-1 dual infections. Retrovirology 2007; 4(1): 67CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Wagner GA, Pacold ME, Kosakovsky Pond SL, Caballero G, Chaillon A, Rudolph AE, Morris SR, Little SJ, Richman DD, Smith DM. Incidence and prevalence of intrasubtype HIV-1 dual infection in at-risk men in the United States. J Infect Dis 2014; 209(7): 1032–1038CrossRefPubMedGoogle Scholar
  22. 22.
    Smith DM, Wong JK, Hightower GK, Ignacio CC, Koelsch KK, Daar ES, Richman DD, Little SJ. Incidence of HIV superinfection following primary infection. JAMA 2004; 292(10): 1177–1178CrossRefPubMedGoogle Scholar
  23. 23.
    Bezemer D, van Sighem A, deWolf F, Cornelissen M, van der Kuyl AC, Jurriaans S, van der Hoek L, Prins M, Coutinho RA, Lukashov VV. Combination antiretroviral therapy failure and HIV superinfection. AIDS 2008; 22(2): 309–311CrossRefPubMedGoogle Scholar
  24. 24.
    Sidat MM, Mijch AM, Lewin SR, Hoy JF, Hocking J, Fairley CK. Incidence of putative HIV superinfection and sexual practices among HIV-infected men who have sex with men. Sex Health 2008; 5(1): 61–67CrossRefPubMedGoogle Scholar
  25. 25.
    Wagner GA, Pacold ME, Vigil E, Caballero G, Morris SR, Kosakovsky Pond SL, Little SJ, Richman DD, Gianella S, Smith DM. Using ultradeep pyrosequencing to study HIV-1 coreceptor usage in primary and dual infection. J Infect Dis 2013; 208(2): 271–274CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Promadej-Lanier N, Thielen C, Hu DJ, Chaowanachan T, Gvetadze R, Choopanya K, Vanichseni S, McNicholl JM. Cross-reactive T cell responses in HIV CRF01_AE and B′-infected intravenous drug users: implications for superinfection and vaccines. AIDS Res Hum Retroviruses 2009; 25(1): 73–81CrossRefPubMedGoogle Scholar
  27. 27.
    McCutchan FE, Hoelscher M, Tovanabutra S, Piyasirisilp S, Sanders-Buell E, Ramos G, Jagodzinski L, Polonis V, Maboko L, Mmbando D, Hoffmann O, Riedner G, von Sonnenburg F, Robb M, Birx DL. In-depth analysis of a heterosexually acquired human immunodeficiency virus type 1 superinfection: evolution, temporal fluctuation, and intercompartment dynamics from the seronegative window period through 30 months postinfection. J Virol 2005; 79(18): 11693–11704CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Redd AD, Mullis CE, Wendel SK, Sheward D, Martens C, Bruno D, Werner L, Garrett NJ, Abdool Karim Q, Williamson C, Porcella SF, Quinn TC, Abdool Karim SS. Limited HIV-1 superinfection in seroconverters from the CAPRISA 004 Microbicide Trial. J Clin Microbiol 2014; 52(3): 844–848CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Grobler J, Gray CM, Rademeyer C, Seoighe C, Ramjee G, Karim SA, Morris L, Williamson C. Incidence of HIV-1 dual infection and its association with increased viral load set point in a cohort of HIV- 1 subtype C-infected female sex workers. J Infect Dis 2004; 190(7): 1355–1359CrossRefPubMedGoogle Scholar
  30. 30.
    Redd AD, Wendel SK, Longosz AF, Fogel JM, Dadabhai S, Kumwenda N, Sun J, Walker MP, Bruno D, Martens C, Eshleman SH, Porcella SF, Quinn TC, Taha TE. Evaluation of postpartum HIV superinfection and mother-to-child transmission. AIDS 2015; 29(12): 1567–1573CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Chohan B, Lavreys L, Rainwater SM, Overbaugh J. Evidence for frequent reinfection with human immunodeficiency virus type 1 of a different subtype. J Virol 2005; 79(16): 10701–10708CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Redd AD, Quinn TC, Tobian AA. Frequency and implications of HIV superinfection. Lancet Infect Dis 2013; 13(7): 622–628CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Gottlieb GS, Nickle DC, Jensen MA, Wong KG, Grobler J, Li F, Liu SL, Rademeyer C, Learn GH, Karim SS, Williamson C, Corey L, Margolick JB, Mullins JI. Dual HIV-1 infection associated with rapid disease progression. Lancet 2004; 363(9409): 619–622CrossRefPubMedGoogle Scholar
  34. 34.
    Tsui R, Herring BL, Barbour JD, Grant RM, Bacchetti P, Kral A, Edlin BR, Delwart EL. Human immunodeficiency virus type 1 superinfection was not detected following 215 years of injection drug user exposure. J Virol 2004; 78(1): 94–103CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Rachinger A, Stolte IG, van de Ven TD, Burger JA, Prins M, Schuitemaker H, van’t Wout AB. Absence of HIV-1 superinfection 1 year after infection between 1985 and 1997 coincides with a reduction in sexual risk behavior in the seroincident Amsterdam cohort of homosexual men. Clin Infect Dis 2010; 50(9): 1309–1315CrossRefPubMedGoogle Scholar
  36. 36.
    Rachinger A, van de Ven TD, Burger JA, Schuitemaker H, van’t Wout AB. Evaluation of pre-screening methods for the identification of HIV-1 superinfection. J Virol Methods 2010; 165(2): 311–317CrossRefPubMedGoogle Scholar
  37. 37.
    Rachinger A, Manyenga P, Burger JA, Derks van de Ven TL, Stolte IG, Prins M, van’t Wout AB, Schuitemaker H. Low incidence of HIV-1 superinfection even after episodes of unsafe sexual behavior of homosexual men in the Amsterdam Cohort Studies on HIV Infection and AIDS. J Infect Dis 2011; 203(11): 1621–1628CrossRefPubMedGoogle Scholar
  38. 38.
    Templeton AR, Kramer MG, Jarvis J, Kowalski J, Gange S, Schneider MF, Shao Q, Zhang GW, Yeh MF, Tsai HL, Zhang H, Markham RB. Multiple-infection and recombination in HIV-1 within a longitudinal cohort of women. Retrovirology 2009; 6(1): 54CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Koelsch KK, Smith DM, Little SJ, Ignacio CC, Macaranas TR, Brown AJ, Petropoulos CJ, Richman DD, Wong JK. Clade B HIV-1 superinfection with wild-type virus after primary infection with drug-resistant clade B virus. AIDS 2003; 17(7): F11–F16CrossRefPubMedGoogle Scholar
  40. 40.
    Piantadosi A, Chohan B, Chohan V, McClelland RS, Overbaugh J. Chronic HIV-1 infection frequently fails to protect against superinfection. PLoS Pathog 2007; 3(11): e177CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Piantadosi A, Ngayo MO, Chohan B, Overbaugh J. Examination of a second region of the HIV type 1 genome reveals additional cases of superinfection. AIDS Res Hum Retroviruses 2008; 24(9): 1221–1224CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Kraft CS, Basu D, Hawkins PA, Hraber PT, Chomba E, Mulenga J, Kilembe W, Khu NH, Derdeyn CA, Allen SA, Manigart O, Hunter E. Timing and source of subtype-C HIV-1 superinfection in the newly infected partner of Zambian couples with disparate viruses. Retrovirology 2012; 9(1): 22CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Sheward DJ, Ntale R, Garrett NJ, Woodman ZL, Abdool Karim SS, Williamson C. HIV-1 superinfection resembles primary infection. J Infect Dis 2015; 212(6): 904–908CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Shapland EB, Holmes V, Reeves CD, Sorokin E, Durot M, Platt D, Allen C, Dean J, Serber Z, Newman J, Chandran S. Low-cost, highthroughput sequencing of DNA assemblies using a highly multiplexed nextera process. ACS Synth Biol 2015; 4(7): 860–866CrossRefPubMedGoogle Scholar
  45. 45.
    Mild M, Hedskog C, Jernberg J, Albert J. Performance of ultra-deep pyrosequencing in analysis of HIV-1 pol gene variation. PLoS One 2011; 6(7): e22741CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Kijak GH, Sanders-Buell E, Harbolick EA, Pham P, Chenine AL, Eller LA, Rono K, Robb ML, Michael NL, Kim JH, Tovanabutra S. Targeted deep sequencing of HIV-1 using the IonTorrentPGM platform. J Virol Methods 2014; 205: 7–16CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Ronen K, McCoy CO, Matsen FA, Boyd DF, Emery S, Odem-Davis K, Jaoko W, Mandaliya K, McClelland RS, Richardson BA, Overbaugh J. HIV-1 superinfection occurs less frequently than initial infection in a cohort of high-risk Kenyan women. PLoS Pathog 2013; 9(8): e1003593CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Luan H, Han X, Yu X, An M, Zhang H, Zhao B, Xu J, Chu Z, Shang H. Dual infection contributes to rapid disease progression in men who have sex with men in China. J Acquir Immune Defic Syndr 2017; 75(4): 480–487CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Soares de Oliveira AC, Pessôa de Farias R, da Costa AC, Sauer MM, Bassichetto KC, Oliveira SM, Costa PR, Tomiyama C, Tomiyama HT, Sabino EC, Kallas EG, Sanabani SS. Frequency of subtype B and F1 dual infection in HIV-1 positive, Brazilian men who have sex with men. Virol J 2012; 9(1): 223CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Chohan BH, Piantadosi A, Overbaugh J. HIV-1 superinfection and its implications for vaccine design. Curr HIV Res 2010; 8(8): 596–601CrossRefPubMedGoogle Scholar
  51. 51.
    Yerly S, Jost S, Monnat M, Telenti A, Cavassini M, Chave JP, Kaiser L, Burgisser P, Perrin L; Swiss HIV Cohort Study. HIV-1 co/super-infection in intravenous drug users. AIDS 2004; 18(10): 1413–1421CrossRefPubMedGoogle Scholar
  52. 52.
    Courtney CR, Mayr L, Nanfack AJ, Banin AN, Tuen M, Pan R, Jiang X, Kong XP, Kirkpatrick AR, Bruno D, Martens CA, Sykora L, Porcella SF, Redd AD, Quinn TC, Nyambi PN, Dürr R. Contrasting antibody responses to intrasubtype superinfection with CRF02_AG. PLoS One 2017; 12(3): e0173705CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Ritchie AJ, Cai F, Smith NM, Chen S, Song H, Brackenridge S, Abdool Karim SS, Korber BT, McMichael AJ, Gao F, Goonetelleke N. Recombination-mediated escape from primary CD8+ T cells in acute HIV-1 infection. Retrovirology 2014; 11: 69CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Streeck H, Li B, Poon AF, Schneidewind A, Gladden AD, Power KA, Daskalakis D, Bazner S, Zuniga R, Brander C, Rosenberg ES, Frost SD, Altfeld M, Allen TM. Immune-driven recombination and loss of control after HIV superinfection. J Exp Med 2008; 205(8): 1789–1796CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Doria-Rose NA, Schramm CA, Gorman J, Moore PL, Bhiman JN, DeKosky BJ, Ernandes MJ, Georgiev IS, Kim HJ, Pancera M, Staupe RP, Altae-Tran HR, Bailer RT, Crooks ET, Cupo A, Druz A, Garrett NJ, Hoi KH, Kong R, Louder MK, Longo NS, McKee K, Nonyane M, O’Dell S, Roark RS, Rudicell RS, Schmidt SD, Sheward DJ, Soto C, Wibmer CK, Yang Y, Zhang Z; NISC Comparative Sequencing Program, Mullikin JC, Binley JM, Sanders RW, Wilson IA, Moore JP, Ward AB, Georgiou G, Williamson C, Abdool Karim SS, Morris L, Kwong PD, Shapiro L, Mascola JR. Developmental pathway for potent V1V2-directed HIV-neutralizing antibodies. Nature 2014; 509(7498): 55–62CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Diaz RS, Pardini R, Catroxo M, Operskalski EA, Mosley JW, Busch MP. HIV-1 superinfection is not a common event. J Clin Virol 2005; 33(4): 328–330CrossRefPubMedGoogle Scholar
  57. 57.
    Chakraborty B, Valer L, De Mendoza C, Soriano V, Quiñones-Mateu ME. Failure to detect human immunodeficiency virus type 1 superinfection in 28 HIV-seroconcordant individuals with high risk of reexposure to the virus. AIDS Res Hum Retroviruses 2004; 20(9): 1026–1031CrossRefPubMedGoogle Scholar
  58. 58.
    Gonzales MJ, Delwart E, Rhee SY, Tsui R, Zolopa AR, Taylor J, Shafer RW. Lack of detectable human immunodeficiency virus type 1 superinfection during 1072 person-years of observation. J Infect Dis 2003; 188(3): 397–405CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Martin F, Lee J, Thomson E, Tarrant N, Hale A, Lacey CJ. Two cases of possible transmitted drug-resistant HIV: likely HIV superinfection and unmasking of pre-existing resistance. Int J STD AIDS 2016; 27(1): 66–69CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Cowan SA, Gerstoft J, Haff J, Christiansen AH, Nielsen J, Obel N. Stable incidence of HIV diagnoses among Danish MSM despite increased engagement in unsafe sex. J Acquir Immune Defic Syndr 2012; 61(1): 106–111CrossRefPubMedGoogle Scholar
  61. 61.
    Trkola A, Kuster H, Rusert P, Joos B, Fischer M, Leemann C, Manrique A, Huber M, Rehr M, Oxenius A, Weber R, Stiegler G, Vcelar B, Katinger H, Aceto L, Günthard HF. Delay of HIV-1 rebound after cessation of antiretroviral therapy through passive transfer of human neutralizing antibodies. Nat Med 2005; 11(6): 615–622CrossRefPubMedGoogle Scholar
  62. 62.
    Mehandru S, Vcelar B, Wrin T, Stiegler G, Joos B, Mohri H, Boden D, Galovich J, Tenner-Racz K, Racz P, Carrington M, Petropoulos C, Katinger H, Markowitz M. Adjunctive passive immunotherapy in human immunodeficiency virus type 1-infected individuals treated with antiviral therapy during acute and early infection. J Virol 2007; 81(20): 11016–11031CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Barouch DH, Whitney JB, Moldt B, Klein F, Oliveira TY, Liu J, Stephenson KE, Chang HW, Shekhar K, Gupta S, Nkolola JP, Seaman MS, Smith KM, Borducchi EN, Cabral C, Smith JY, Blackmore S, Sanisetty S, Perry JR, Beck M, Lewis MG, Rinaldi W, Chakraborty AK, Poignard P, Nussenzweig MC, Burton DR. Therapeutic efficacy of potent neutralizing HIV-1-specific monoclonal antibodies in SHIV-infected rhesus monkeys. Nature 2013; 503(7475): 224–228CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Wagner GA, Landais E, Caballero G, Phung P, Kosakovsky Pond SL, Poignard P, Richman DD, Little SJ, Smith DM. Intrasubtype B HIV-1 superinfection correlates with delayed neutralizing antibody response. J Virol 2017; 91(17): e00475–17CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Mikell I, Sather DN, Kalams SA, Altfeld M, Alter G, Stamatatos L. Characteristics of the earliest cross-neutralizing antibody response to HIV-1. PLoS Pathog 2011; 7(1): e1001251CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Moore PL, Gray ES, Sheward D, Madiga M, Ranchobe N, Lai Z, Honnen WJ, Nonyane M, Tumba N, Hermanus T, Sibeko S, Mlisana K, Abdool Karim SS, Williamson C, Pinter A, Morris L; CAPRISA 002 Study. Potent and broad neutralization of HIV-1 subtype C by plasma antibodies targeting a quaternary epitope including residues in the V2 loop. J Virol 2011; 85(7): 3128–3141CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Liao HX, Lynch R, Zhou T, Gao F, Alam SM, Boyd SD, Fire AZ, Roskin KM, Schramm CA, Zhang Z, Zhu J, Shapiro L; NISC Comparative Sequencing Program, Mullikin JC, Gnanakaran S, Hraber P, Wiehe K, Kelsoe G, Yang G, Xia SM, Montefiori DC, Parks R, Lloyd KE, Scearce RM, Soderberg KA, Cohen M, Kamanga G, Louder MK, Tran LM, Chen Y, Cai F, Chen S, Moquin S, Du X, Joyce MG, Srivatsan S, Zhang B, Zheng A, Shaw GM, Hahn BH, Kepler TB, Korber BT, Kwong PD, Mascola JR, Haynes BF. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 2013; 496(7446): 469–476CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Weinfurter JT, May GE, Soma T, Hessell AJ, León EJ, Macnair CE, Piaskowski SM, Weisgrau K, Furlott J, Maness NJ, Reed J, Wilson NA, Rakasz EG, Burton DR, Friedrich TC. Macaque long-term nonprogressors resist superinfection with multiple CD8 + T cell escape variants of simian immunodeficiency virus. J Virol 2011; 85(1): 530–541CrossRefPubMedGoogle Scholar
  69. 69.
    Blish CA, Dogan OC, Jaoko W, McClelland RS, Mandaliya K, Odem-Davis KS, Richardsonb BA, Overbaugh J. Cellular immune responses and susceptibility to HIV-1 superinfection: a case-control study. AIDS 2012; 26(5): 643–646CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Forthal DN, Landucci G, Chohan B, Richardson BA, McClelland RS, Jaoko W, Blish C, Overbaugh J. Antibody-dependent cellmediated virus inhibition antibody activity does not correlate with risk of HIV-1 superinfection. J Acquir Immune Defic Syndr 2013; 63(1): 31–33CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Blish CA, Dogan OC, Jaoko W, McClelland RS, Mandaliya K, Odem-Davis K, Richardson BA, Overbaugh J. Association between cellular immune activation, target cell frequency, and risk of human immunodeficiency virus type 1 superinfection. J Virol 2014; 88(10): 5894–5899CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Ronen K, Dingens AS, Graham SM, Jaoko W, Mandaliya K, McClelland RS, Overbaugh J. Comprehensive characterization of humoral correlates of human immunodeficiency virus 1 superinfection acquisition in high-risk Kenyan women. EBioMedicine 2017; 18: 216–224CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Vesa J, Chaillon A, Wagner GA, Anderson CM, Richman DD, Smith DM, Little SJ. Increased HIV-1 superinfection risk in carriers of specific human leukocyte antigen alleles. AIDS 2017; 31(8): 1149–1158CrossRefPubMedGoogle Scholar
  74. 74.
    Campbell MS, Gottlieb GS, Hawes SE, Nickle DC, Wong KG, Deng W, Lampinen TM, Kiviat NB, Mullins JI. HIV-1 superinfection in the antiretroviral therapy era: are seroconcordant sexual partners at risk? PLoS One 2009; 4(5): e5690CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Haynes BF, Kelsoe G, Harrison SC, Kepler TB. B-cell-lineage immunogen design in vaccine development with HIV-1 as a case study. Nat Biotechnol 2012; 30(5):423–433CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Haynes BF, Shaw GM, Korber B, Kelsoe G, Sodroski J, Hahn BH, Borrow P, McMichael AJ. HIV-host interactions: implications for vaccine design. Cell Host Microbe 2016; 19:292–303CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Gao F. Broad neutralization as a byproduct of antibody maturation during HIV-1 infection: a personal perspective. Infect Dis Transl Med 2016; 2:60–68Google Scholar
  78. 78.
    Piantadosi A, Panteleeff D, Blish CA, Baeten JM, Jaoko W, McClelland RS, Overbaugh J. 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 2009; 83(19): 10269–10274CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Euler Z, van den Kerkhof TL, van Gils MJ, Burger JA, Edo-Matas D, Phung P, Wrin T, Schuitemaker H. Longitudinal analysis of early HIV-1-specific neutralizing activity in an elite neutralizer and in five patients who developed cross-reactive neutralizing activity. J Virol 2012; 86(4): 2045–2055CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Pernas M, Casado C, Arcones C, Llano A, Sánchez-Merino V, Mothe B, Vicario JL, Grau E, Ruiz L, Sánchez J, Telenti A, Yuste E, Brander C, Galíndez CL. Low-replicating viruses and strong antiviral immune response associated with prolonged disease control in a superinfected HIV-1 LTNP elite controller. PLoS One 2012; 7(2): e31928CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Higher Education Press and Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Key Laboratory of AIDS Immunology of National Health and Family Planning Commission, Department of Laboratory Medicine, The First Affiliated HospitalChina Medical UniversityShenyangChina
  2. 2.National Engineering Laboratory for AIDS Vaccine, School of Life SciencesJilin UniversityChangchunChina
  3. 3.Department of MedicineDuke University Medical CenterDurhamUSA

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