Human immunodeficiency virus type 1 superinfection occurs despite relatively robust neutralizing antibody responses

Journal of Virology

Volumn 82, Issue 24, 2008, Pages 12094-12103

  Blish, Catherine A ^a,b   Dogan, Ozge C ^a   Derby, Nina R ^a   Nguyen, Minh An ^a   Chohan, Bhavna ^a,c   Richardson, Barbra A ^c   Overbaugh, Julie ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUTRALIZING ANTIBODY;

ANTIBODY RESPONSE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REINFECTION; SUPERINFECTION; VACCINATION; VIRUS STRAIN;

ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; FEMALE; HIV ANTIBODIES; HIV INFECTIONS; HIV-1; HUMANS; MUTATION; PHYLOGENY; SUPERINFECTION; TIME FACTORS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 57349169315     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01730-08     Document Type: Article

References (57)

1. + T-cell responses containing replication of the primary virus. Nature 420:434-439.
2. Beirnaert, E., P. Nyambi, B. Willems, L. Heyndrickx, R. Colebunders, W. Janssens, and G. van der Groen. 2000. Identification and characterization of sera from HIV-infected individuals with broad cross-neutralizing activity against group M (Env clade A-H) and group O primary HIV-1 isolates. J. Med. Virol. 62:14-24.
3. Blish, C., R. Nedellec, K. Mandaliya, D. Mosier, and J. Overbaugh. 2007. HIV-1 subtype A envelope variants from early in infection have variable sensitivity to neutralization and to inhibitors of viral entry. AIDS 6:693-702.
4. Bocher, W. O., S. Herzog-Hauff, W. Herr, K. Heermann, G. Gerken, K. H. Meyer Zum Buschenfelde, and H. F. Lohr. 1996. Regulation of the neutralizing anti-hepatitis B surface (HBs) antibody response in vitro in HBs vaccine recipients and patients with acute or chronic hepatitis B virus (HBV) infection. Clin. Exp. Immunol. 105:52-58.
5. + T-cells: are they sufficient to prevent, contain or eradicate HIV-1 infection? Curr. Drug Targets Infect. Disord. 5:113-119.
6. Chakraborty, B., L. Valer, C. De Mendoza, V. Soriano, and M. E. Quinones-Mateu. 2004. Failure to detect human immunodeficiency virus type 1 super-infection in 28 HIV-seroconcordant individuals with high risk of reexposure to the virus. AIDS Res. Hum. Retrovir. 20:1026-1031.
7. Chohan, B., L. Lavreys, S. M. J. Rainwater, and J. Overbaugh. 2005. Evidence for frequent reinfection with human immunodeficiency virus type 1 of a different subtype. J. Virol. 79:10701-10708.
8. Dhillon, A. K., H. Donners, R. Pantophlet, W. E. Johnson, J. M. Decker, G. M. Shaw, F. H. Lee, D. D. Richman, R. W. Doms, G. Vanham, and D. R. Burton. 2007. Dissecting the neutralizing antibody specificities of broadly neutralizing sera from human immunodeficiency virus type 1-infected donors. J. Virol. 81:6548-6562.
9. Gonzales, M. J., E. Delwart, S. Y. Rhee, R. Tsui, A. R. Zolopa, J. Taylor, and R. W. Shafer. 2003. Lack of detectable human immunodeficiency virus type 1 superinfection during 1072 person-years of observation. J. Infect. Dis. 188:397-405.
10. Gottlieb, G. S., D. C. Nickle, M. A. Jensen, K. G. Wong, J. Grobler, F. Li, S. L. Liu, C. Rademeyer, G. H. Learn, S. S. Karim, C. Williamson, L. Corey, J. B. Margolick, and J. I. Mullins. 2004. Dual HIV-1 infection associated with rapid disease progression. Lancet 363:619-622.
11. Grobler, J., C. M. Gray, C. Rademeyer, C. Seoighe, G. Ramjee, S. A. Karim, L. Morris, and C. Williamson. 2004. 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. 190:1355-1359.
12. Harro, C. D., F. N. Judson, G. J. Gorse, K. H. Mayer, J. R. Kostman, S. J. Brown, B. Koblin, M. Marmor, B. N. Bartholow, and V. Popovic. 2004. Recruitment and baseline epidemiologic profile of participants in the first phase 3 HIV vaccine efficacy trial. J. Acquir. Immune Defic. Syndr. 37:1385-1392.
13. Jost, S., M. C. Bernard, L. Kaiser, S. Yerly, B. Hirschel, A. Samri, B. Autran, L. E. Goh, and L. Perrin. 2002. A patient with HIV-1 superinfection. N. Engl. J. Med. 347:731-736.
14. Koelsch, K. K., D. M. Smith, S. J. Little, C. C. Ignacio, T. R. Macaranas, A. J. Brown, C. J. Petropoulos, D. D. Richman, and J. K. Wong. 2003. Clade B HIV-1 superinfection with wild-type virus after primary infection with drug-resistant clade B virus. AIDS 17:F11-F16.
15. Lavreys, L., J. M. Baeten, V. Chohan, R. S. McClelland, W. M. Hassan, B. A. Richardson, K. Mandaliya, J. O. Ndinya-Achola, and J. Overbaugh. 2006. Higher set point plasma viral load and more-severe acute HIV type 1 (HIV-1) illness predict mortality among high-risk HIV-1-infected African women. Clin. Infect. Dis. 42:1333-1339.
16. Lavreys, L., J. M. Baeten, J. Overbaugh, D. D. Panteleeff, B. H. Chohan, B. A. Richardson, K. Mandaliya, J. O. Ndinya-Achola, and J. K. Kreiss. 2002. Virus load during primary human immunodeficiency virus (HIV) type 1 infection is related to the severity of acute HIV illness in Kenyan women. Clin. Infect. Dis. 35:77-81.
17. Li, M., F. Gao, J. R. Mascola, L. Stamatatos, V. R. Polonis, M. Koutsoukos, G. Voss, P. Goepfert, P. Gilbert, K. M. Greene, M. Bilska, D. L. Kothe, J. F. Salazar-Gonzalez, X. Wei, J. M. Decker, B. H. Hahn, and D. C. Montefiori. 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.
18. Li, M., J. F. Salazar-Gonzalez, C. A. Derdeyn, L. Morris, C. Williamson, J. E. Robinson, J. M. Decker, Y. Li, M. G. Salazar, V. R. Polonis, K. Mlisana, S. A. Karim, K. Hong, K. M. Greene, M. Bilska, J. Zhou, S. Allen, E. Chomba, J. Mulenga, C. Vwalika, F. Gao, M. Zhang, B. T. Korber, E. Hunter, B. H. Hahn, and D. C. Montefiori. 2006. Genetic and neutralization properties of subtype C human immunodeficiency virus type 1 molecular env clones from acute and early heterosexually acquired infections in Southern Africa. J. Virol. 80:11776-11790.
19. Li, Y., S. A. Migueles, B. Welcher, K. Svehla, A. Phogat, M. K. Louder, X. Wu, G. M. Shaw, M. Connors, R. T. Wyatt, and J. R. Mascola. 2007. Broad HIV-1 neutralization mediated by CD4-binding site antibodies. Nat. Med. 13:1032-1034.
20. Long, E. M., H. L. Martin, Jr., J. K. Kreiss, S. M. Rainwater, L. Lavreys, D. J. Jackson, J. Rakwar, K. Mandaliya, and J. Overbaugh. 2000. Gender differences in HIV-1 diversity at time of infection. Nat. Med. 6:71-75.
21. Long, E. M., S. M. J. Rainwater, L. Lavreys, K. Mandaliya, and J. Overbaugh. 2002. HIV type 1 variants transmitted to women in Kenya require the CCR5 coreceptor for entry, regardless of the genetic complexity of the infecting virus. AIDS Res. Hum. Retrovir. 18:567-576.
22. Maddison, D., and W. Maddison. 2005. MacClade 4: analysis of phylogeny and character evolution. Sinauer, Sunderland, MA.
23. Martin, H. L., D. J. Jackson, K. Mandaliya, J. Bwayo, J. P. Rakwar, P. Nyange, S. Moses, J. O. Ndinya-Achola, K. Holmes, F. Plummer, E. Ngugi, and J. Kreiss. 1994. Preparation for AIDS vaccine evaluation in Mombasa, Kenya: establishment of seronegative cohorts of commercial sex workers and trucking company employees. AIDS Res. Hum. Retrovir. 10:S235-S237.
24. Martin, H. L., P. M. Nyange, B. A. Richardson, L. Lavreys, K. Mandaliya, D. J. Jackson, J. O. Ndinya-Achola, and J. Kreiss. 1998. Hormonal contraception, sexually transmitted diseases, and the risk of heterosexual transmission of HIV-1. J. Infect. Dis. 178:1053-1059.
25. Martin, H. L., B. A. Richardson, P. M. Nyange, L. Lavreys, S. L. Hillier, B. Chohan, K. Mandaliya, J. O. Ndinya-Achola, J. Bwayo, and J. Kreiss. 1999. Vaginal lactobacilli, microbial flora, and risk of human immunodeficiency virus type 1 and sexually transmitted disease acquisition. J. Infect. Dis. 180:1863-1868.
26. Mascola, J. R., M. G. Lewis, G. Stiegler, D. Harris, T. C. VanCott, D. Hayes, M. K. Louder, C. R. Brown, C. V. Sapan, S. S. Frankel, Y. Lu, M. L. Robb, H. Katinger, and D. L. Birx. 1999. Protection of macaques against pathogenic simian/human immunodeficiency virus 89.6PD by passive transfer of neutralizing antibodies. J. Virol. 73:4009-4018.
27. Mascola, J. R., G. Stiegler, T. C. VanCott, H. Katinger, C. B. Carpenter, C. E. Hanson, H. Beary, D. Hayes, S. S. Frankel, D. L. Birx, and M. G. Lewis. 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.
28. McCutchan, F. E., M. Hoelscher, S. Tovanabutra, S. Piyasirisilp, E. Sanders-Buell, G. Ramos, L. Jagodzinski, V. Polonis, L. Maboko, D. Mmbando, O. Hoffmann, G. Riedner, F. von Sonnenburg, M. Robb, and D. L. Birx. 2005. 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. 79:11693-11704.
29. Montefiori, D. 2004. Evaluating neutralizing antibodies against HIV, SIV, and SHIV in luciferase reporter gene assays, p. 1-15. In J. E. Coligan, A. M. Kruisbeek, D. H. Margulies, E. M. Shevach, W. Strober, and R. Coico (ed.), Current protocols in immunology, vol. 12. John Wiley and Sons, New York, NY.
30. Montefiori, D. C., G. Pantaleo, L. M. Fink, J. T. Zhou, J. Y. Zhou, M. Bilska, G. D. Miralles, and A. S. Fauci. 1996. Neutralizing and infection-enhancing antibody responses to human immunodeficiency virus type 1 in long-term nonprogressors. J. Infect. Dis. 173:60-67.
31. Nishimura, Y., T. Igarashi, N. Haigwood, R. Sadjadpour, R. J. Plishka, A. Buckler-White, R. Shibata, and M. A. Martin. 2002. Determination of a statistically valid neutralization titer in plasma that confers protection against simian-human immunodeficiency virus challenge following passive transfer of high-titered neutralizing antibodies. J. Virol. 76:2123-2130.
32. Nyambi, P. N., J. Nkengasong, P. Lewi, K. Andries, W. Janssens, K. Fransen, L. Heyndrickx, P. Piot, and G. van-der-Groen. 1996. Multivariate analysis of human immunodeficiency virus type 1 neutralization data. J. Virol. 70:6235-6243.
33. Olsson, S. E., L. L. Villa, R. L. Costa, C. A. Petta, R. P. Andrade, C. Malm, O. E. Iversen, J. Hoye, M. Steinwall, G. Riis-Johannessen, A. Andersson-Ellstrom, K. Elfgren, G. von Krogh, M. Lehtinen, J. Paavonen, G. M. Tamms, K. Giacoletti, L. Lupinacci, M. T. Esser, S. C. Vuocolo, A. J. Saah, and E. Barr. 2007. Induction of immune memory following administration of a prophylactic quadrivalent human papillomavirus (HPV) types 6/11/16/18 L1 virus-like particle (VLP) vaccine. Vaccine 25:4931-4939.
34. Pal, R., V. S. Kalyanaraman, B. C. Nair, S. Whitney, T. Keen, L. Hocker, L. Hudacik, N. Rose, I. Mboudjeka, S. Shen, T. H. Wu-Chou, D. Montefiori, J. Mascola, P. Markham, and S. Lu. 2006. Immunization of rhesus macaques with a polyvalent DNA prime/protein boost human immunodeficiency virus type 1 vaccine elicits protective antibody response against simian human immunodeficiency virus of R5 phenotype. Virology 348:341-353.
35. Pantaleo, G., and R. A. Koup. 2004. Correlates of immune protection in HIV-1 infection: what we know, what we don't know, what we should know. Nat. Med. 10:806-810.
36. Parren, P. W., P. A. Marx, A. J. Hessell, A. Luckay, J. Harouse, C. Cheng-Mayer, J. P. Moore, and D. R. Burton. 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.
37. Pernas, M., C. Casado, R. Fuentes, M. J. Perez-Elias, and C. Lopez-Galindez. 2006. A dual superinfection and recombination within HIV-1 subtype B 12 years after primoinfection. J. Acquir. Immune Defic. Syndr. 42:12-18.
38. Piantadosi, A., B. Chohan, V. Chohan, R. S. McClelland, and J. Overbaugh. 2007. Chronic HIV-1 infection frequently fails to protect against superinfection. PLoS Pathog. 3:e177.
39. Pilgrim, A. K., G. Pantaleo, O. J. Cohen, L. M. Fink, J. Y. Zhou, J. T. Zhou, D. P. Bolognesi, A. S. Fauci, and D. C. Montefiori. 1997. Neutralizing antibody responses to human immunodeficiency virus type 1 in primary infection and long-term-nonprogressive infection. J. Infect. Dis. 176:924-932.
40. Plotkin, S. A. 2001. Immunologic correlates of protection induced by vaccination. Pediatr. Infect. Dis. J. 20:63-75.
41. Ramos, A., D. J. Hu, L. Nguyen, K. O. Phan, S. Vanichseni, N. Promadej, K. Choopanya, M. Callahan, N. L. Young, J. McNicholl, T. D. Mastro, T. M. Folks, and S. Subbarao. 2002. Intersubtype human immunodeficiency virus type 1 superinfection following seroconversion to primary infection in two injection drug users. J. Virol. 76:7444-7452.
42. Richman, D. D., T. Wrin, S. J. Little, and C. J. Petropoulos. 2003. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc. Natl. Acad. Sci. USA 100:4144-4149.
43. Smith, D. M., D. D. Richman, and S. J. Little. 2005. HIV superinfection. J. Infect. Dis. 192:438-444.
44. Smith, D. M., M. C. Strain, S. D. W. Frost, S. K. Pillai, J. K. Wong, T. Wrin, C. J. Petropolous, E. S. Daar, S. J. Little, and D. D. Richman. 2006. Lack of neutralizing antibody response to HIV-1 predisposes to superinfection. Virology 355:1-5.
45. Smith, D. M., J. K. Wong, G. K. Hightower, C. C. Ignacio, K. K. Koelsch, E. S. Daar, D. D. Richman, and S. J. Little. 2004. Incidence of HIV super-infection following primary infection. JAMA 292:1177-1178.
46. Srivastava, I. K., J. B. Ulmer, and S. W. Barnett. 2005. Role of neutralizing antibodies in protective immunity against HIV. Hum. Vaccine 1:45-60.
47. Streeck, H., B. Li, A. F. Poon, A. Schneidewind, A. D. Gladden, K. A. Power, D. Daskalakis, S. Bazner, R. Zuniga, C. Brander, E. S. Rosenberg, S. D. Frost, M. Altfeld, and T. M. Allen. 2008. Immune-driven recombination and loss of control after HIV superinfection. J. Exp. Med. 205:1789-1796.
48. Swofford, D. 1991. PAUP: phylogenetic analysis using parsimony, 3rd ed. Illinois Natural History Survey, University of Illinois, Champaign.
49. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
50. Tsui, R., B. L. Herring, J. D. Barbour, R. M. Grant, P. Bacchetti, A. Kral, B. R. Edlin, and E. L. Delwart. 2004. Human immunodeficiency virus type 1 superinfection was not detected following 215 years of injection drug user exposure. J. Virol. 78:94-103.
51. van der Kuyl, A. C., K. Kozaczynska, R. van den Burg, F. Zorgdrager, N. Back, S. Jurriaans, B. Berkhout, P. Reiss, and M. Cornelissen. 2005. Triple HIV-1 infection. N. Engl. J. Med. 352:2557-2559.
52. Villa, L. L., K. A. Ault, A. R. Giuliano, R. L. Costa, C. A. Petta, R. P. Andrade, D. R. Brown, A. Ferenczy, D. M. Harper, L. A. Koutsky, R. J. Kurman, M. Lehtinen, C. Malm, S. E. Olsson, B. M. Ronnett, F. E. Skjeldestad, M. Steinwall, M. H. Stoler, C. M. Wheeler, F. J. Taddeo, J. Yu, L. Lupinacci, R. Railkar, R. Marchese, M. T. Esser, J. Bryan, K. U. Jansen, H. L. Sings, G. M. Tamms, A. J. Saah, and E. Barr. 2006. Immunologic responses following administration of a vaccine targeting human papillomavirus types 6, 11, 16, and 18. Vaccine 24:5571-5583.
53. Voronin, Y., B. Chohan, M. Emerman, and J. Overbaugh. 2007. Primary isolates of human immunodeficiency virus type 1 are usually dominated by the major variants found in blood. J. Virol. 81:10232-10241.
54. Wu, X., A. B. Parast, B. A. Richardson, R. Nduati, G. John-Stewart, D. Mbori-Ngacha, S. M. Rainwater, and J. Overbaugh. 2006. Neutralization escape variants of human immunodeficiency virus type 1 are transmitted from mother to infant. J. Virol. 80:835-844.
55. Yang, O. O., E. S. Daar, B. D. Jamieson, A. Balamurugan, D. M. Smith, J. A. Pitt, C. J. Petropoulos, D. D. Richman, S. J. Little, and A. J. Brown. 2005. Human immunodeficiency virus type 1 clade B superinfection: evidence for differential immune containment of distinct clade B strains. J. Virol. 79:860-868.
56. Yerly, S., S. Jost, M. Monnat, A. Telenti, M. Cavassini, J. P. Chave, L. Kaiser, P. Burgisser, and L. Perrin. 2004. HIV-1 co/super-infection in intravenous drug users. AIDS 18:1413-1421.
57. Zhang, Y. J., C. Fracasso, J. R. Fiore, A. Bjorndal, G. Angarano, A. Gringeri, and E. M. Fenyo. 1997. Augmented serum neutralizing activity against primary human immunodeficiency virus type 1 (HIV-1) isolates in two groups of HIV-1-infected long-term nonprogressors. J. Infect. Dis. 176:1180-1187.