Extensive intrasubtype recombination in South African human immunodeficiency virus type 1 subtype C infections

Journal of Virology

Volumn 81, Issue 9, 2007, Pages 4492-4500

  Rousseau, Christine M ^a   Learn, Gerald H ^a   Bhattacharya, Tanmoy ^b   Nickle, David C ^a   Heckerman, David ^c   Chetty, Senica ^d   Brander, Christian ^e   Goulder, Philip J R ^e,f   Walker, Bruce D ^e,g   Kiepiela, Photini ^d   Korber, Bette T ^b   Mullins, James I ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b LOS ALAMOS NATIONAL LABORATORY   (United States)

^c MICROSOFT RESEARCH   (United States)

^d UNIVERSITY OF KWAZULU NATAL   (South Africa)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

^f UNIVERSITY OF OXFORD   (United Kingdom)

^g HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; EVOLUTION; EVOLUTIONARY RATE; GENETIC VARIABILITY; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SOUTH AFRICA; VIRAL GENETICS; VIRUS GENOME; VIRUS RECOMBINANT; VIRUS RECOMBINATION; VIRUS STRAIN;

COMPUTATIONAL BIOLOGY; EVOLUTION, MOLECULAR; GENETICS, POPULATION; GENOME, VIRAL; HIV INFECTIONS; HIV-1; HUMANS; LIKELIHOOD FUNCTIONS; MODELS, GENETIC; PHYLOGENY; RECOMBINATION, GENETIC; SOUTH AFRICA;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 34247647904     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02050-06     Document Type: Article

References (63)

1. Becker-Pergola, G., J. L. Mellquist, L. Guay, F. Mmiro, C. Ndugwa, P. Kataaha, J. B. Jackson, and S. H. Eshleman. 2000. Identification of diverse HIV type 1 subtypes and dual HIV type 1 infection in pregnant Ugandan women. AIDS Res. Hum. Retrovir. 16:1099-1104.
2. Benjamini, Y., and Y. Hochberg. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 57:289-300.
3. Bhattacharya, T., M. Daniels, D. Heckerman, B. Foley, N. Frahm, C. Kadie, J. Carlson, K. Yusim, B. McMahon, B. Gaschen, S. Mallal, J. I. Mullins, D. C. Nickle, J. Herbeck, C. Rousseau, G. H. Learn, T. Miura, C. Brander, B. Walker, and B. Korber. Founder effects in the assessment of HIV polymorphisms and HLA allele associations. Science, in press.
4. Brenner, B., J. P. Routy, Y. Quan, D. Moisi, M. Oliveira, D. Turner, and M. A. Wainberg. 2004. Persistence of multidrug-resistant HIV-1 in primary infection leading to superinfection. AIDS 18:1653-1660.
5. Chohan, B., L. Lavreys, S. M. Rainwater, and J. Overbaugh. 2005. Evidence for frequent reinfection with human immunodeficiency virus type 1 of a different subtype. J. Virol. 79:10701-10708.
6. Curlin, M. E., G. S. Gottlieb, S. E. Hawes, P. S. Sow, I. Ndoye, C. W. Critchlow, N. B. Kiviat, and J. I. Mullins. 2004. No evidence for recombination between HIV type 1 and HIV type 2 within the envelope region in dually seropositive individuals from Senegal. AIDS Res. Hum. Retrovir. 20:958-963.
7. de Oliveira, T., K. Deforche, S. Cassol, M. Salminen, D. Paraskevis, C. Seebregts, J. Snoeck, E. J. van Rensburg, A. M. Wensing, D. A. van de Vijver, C. A. Boucher, R. Camacho, and A. M. Vandamme. 2005. An automated genotyping system for analysis of HIV-1 and other microbial sequences. Bioinformatics 21:3797-3800.
8. Fang, G., B. Weiser, C. Kuiken, S. M. Philpott, S. Rowland-Jones, F. Plummer, J. Rimani, B. Shi, R. Kaul, J. Bwayo, O. Anzala, and H. Burger. 2004. Recombination following superinfection by HIV-1. AIDS 18:153-159.
9. Gascuel, O. 1997. BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol. Biol. Evol. 14:685-695.
10. Gerhardt, M., D. Mloka, S. Tovanabutra, E. Sanders-Buell, O. Hoffmann, L. Maboko, D. Mmbando, D. L. Birx, F. E. McCutchan, and M. Hoelscher. 2005. In-depth, longitudinal analysis of viral quasispecies from an individual triply infected with late-stage human immunodeficiency virus type 1, using a multiple PCR primer approach. J. Virol. 79:8249-8261.
11. Gordon, M., T. De Oliveira, K. Bishop, H. M. Coovadia, L. Madurai, S. Engelbrecht, E. Janse van Rensburg, A. Mosam, A. Smith, and S. Cassol. 2003. Molecular characteristics of human immunodeficiency virus type 1 subtype C viruses from KwaZulu-Natal, South Africa: implications for vaccine and antiretroviral control strategies. J. Virol. 77:2587-2599.
12. 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.
13. Gottlieb, G. S., P. S. Sow, S. E. Hawes, I. Ndoye, A. M. Coll-Seck, M. E. Curlin, C. W. Critchlow, N. B. Kiviat, and J. I. Mullins. 2003. Molecular epidemiology of dual HIV-1/HIV-2 seropositive adults from Senegal, West Africa. AIDS Res. Hum. Retrovir. 19:575-584.
14. Grobler, J., C. M. Gray, C. Rademeyer, C. Seoighe, G. Ramjee, S. Abdool 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 HlV-1 subtype C-infected female sex workers. J. Infect. Dis. 190:1355-1359.
15. Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
16. Harris, M. E., S. Maayan, B. Kim, M. Zeira, G. Ferrari, D. L. Birx, and F. E. McCutchan. 2003. A cluster of HIV type 1 subtype C sequences from Ethiopia, observed in full genome analysis, is not sustained in subgenomic regions. AIDS Res. Hum. Retrovir. 19:1125-1133.
17. Herbinger, K. H., M. Gerhardt, S. Piyasirisilp, D. Mloka, M. A. Arroyo, O. Hoffmann, L. Maboko, D. L. Birx, D. Mmbando, F. E. McCutchan, and M. Hoelscher. 2006. Frequency of HIV type 1 dual infection and HIV diversity: analysis of low- and high-risk populations in Mbeya Region, Tanzania. AIDS Res. Hum. Retrovir. 22:599-606.
18. Hu, D. J., S. Subbarao, S. Vanichseni, P. A. Mock, A. Ramos, L. Nguyen, T. Chaowanachan, F. Griensven, K. Choopanya, T. D. Mastro, and J. W. Tappero. 2005. Frequency of HIV-1 dual subtype infections, including intersubtype superinfections, among injection drug users in Bangkok, Thailand. AIDS 19:303-308.
19. Iversen, A. K., G. H. Learn, L. Fugger, J. Gerstoft, J. I. Mullins, and P. Skinhoj. 1999. Presence of multiple HIV subtypes and a high frequency of subtype chimeric viruses in heterosexually infected women. J. Acquir. Immune Defic. Syndr. 22:325-332.
20. Jetzt, A. E., H. Yu, G. J. Klarmann, Y. Ron, B. D. Preston, and J. P. Dougherty. 2000. High rate of recombination throughout the human immunodeficiency virus type 1 genome. J. Virol. 74:1234-1240.
21. Jung, A., R. Maier, J.-P. Vartanian, G. Bocharov, V. Jung, U. Fischer, E. Meese, S. Wain-Hobson, and A. Meyerhans. 2002. Multiply infected spleen cells in HIV patients. Nature 418:144.
22. Kiepiela, P., A. J. Leslie, I. Honeyborne, D. Ramduth, C. Thobakgale, S. Chetty, P. Rathnavalu, C. Moore, K. J. Pfafferott, L. Hilton, P. Zimbwa, S. Moore, T. Allen, C. Brander, M. M. Addo, M. Altfeld, I. James, S. Mallal, M. Bunce, L. D. Barber, J. Szinger, C. Day, P. Klenerman, J. Mullins, B. Korber, H. M. Coovadia, B. D. Walker, and P. J. Goulder. 2004. Dominant influence of HLA-B in mediating the potential co-evolution of HIV and HLA. Nature 432:769-775.
23. 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.
24. Korber, B., M. Muldoon, J. Theiler, F. Gao, R. Gupta, A. Lapedes, B. H. Hahn, S. Wolinsky, and T. Bhattacharya. 2000. Timing the ancestor of the HIV-1 pandemic strains. Science 288:1789-1796.
25. Kuhner, M. K., J. Yamato, and J. Felsenstein. 2000. Maximum likelihood estimation of recombination rates from population data. Genetics 156:1393-1401.
26. Liu, Y., D. C. Nickle, D. Shriner, M. A. Jensen, G. H. Learn, Jr., J. E. Mittler, and J. I. Mullins. 2004. Molecular clock-like evolution of human immunodeficiency virus type 1. Virology 329:101-108.
27. Loie, K. S., R. C. Bollinger, R. S. Paranjape, D. Gadkari, S. S. Kulkarni, N. G. Novak, R. Ingersoll, H. W. Sheppard, and S. C. Ray. 1999. Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J. Virol. 73:152-160.
28. Maddison, W. P., and D. R. Maddison. 2001. MacClade: analysis of phylogcny and character evolution, version 4.08. Sinauer Associates, Inc., Sunderland, MA.
29. Mansky, L. M. 1996. Forward mutation rate of human immunodeficiency virus type I in a T lymphoid cell line. AIDS Res. Hum. Retrovir. 12:307-314.
30. Maynard Smith, J. 1992. Analyzing the mosaic structure of genes. J. Mol. Evol. 34:126-129.
31. McCormack, G. P., J. R. Glynn, A. C. Crampin, F. Sibande, D. Mulawa, L. Bliss, P. Broadbent, K. Abarca, J. M. Ponnighaus, P. E. Fine, and J. P. Clewley. 2002. Early evolution of the human immunodeficiency virus type 1 subtype C epidemic in rural Malawi. J. Virol. 76:12890-12899.
32. 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.
33. Moore, C. B., M. John, I. R. James, F. T. Christiansen, C. S. Witt, and S. A. Mallal. 2002. Evidence of HIV-1 adaptation to HLA-restricted immune responses at a population level. Science 296:1439-1443.
34. Novitsky, V., U. R. Smith, P. Gilbert, M. F. McLane, P. Chigwedere, C. Williamson, T. Ndung'u, I. Klein, S. Y. Chang, T. Peter, I. Thior, B. T. Foley, S. Gaolekwe, N. Rybak, S. Gaseitsiwe, F. Vannberg, R. Marlink, T. H. Lee, and M. Essex. 2002. Human immunodeficiency virus type 1 subtype C molecular phylogeny: consensus sequence for an AIDS vaccine design? J. Virol. 76:5435-5451.
35. Novitsky, V. A., M. A. Montano, M. F. McLane, B. Renjifo, F. Vannberg, B. T. Foley, T. P. Ndung'u, M. Rahman, M. J. Makhema, R. Marlink, and M. Essex. 1999. Molecular cloning and phylogenetic analysis of human immunodeficiency virus type 1 subtype C: a set of 23 full-length clones from Botswana. J. Virol. 73:4427-4432.
36. 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.
37. Philpott, S., H. Burger, C. Tsoukas, B. Foley, K. Anastos, C. Kitchen, and B. Weiser. 2005. Human immunodeficiency virus type 1 genomic RNA sequences in the female genital tract and blood: compartmentalization and intrapatient recombination. J. Virol. 79:353-363.
38. Pollakis, G., A. Abebe, A. Kliphuis, T. F. De Wit, B. Fisseha, B. Tegbaru, G. Tesfaye, H. Negassa, Y. Mengistu, A. L. Fontanet, M. Cornelissen, and J. Goudsmit. 2003. Recombination of HIV type 1C (C′/C″) in Ethiopia: possible link of EthHIV-1C′ to subtype C sequences from the high-prevalence epidemics in India and Southern Africa. AIDS Res. Hum. Retrovir. 19:999-1008.
39. Posada, D., and K. A. Crandall. 2001. Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc. Natl. Acad. Sci. USA 98:13757-13762.
40. Robertson, D. L., B. H. Hahn, and P. M. Sharp. 1995. Recombination in AIDS viruses. J. Mol. Evol. 40:249-259.
41. Rodenburg, C. M., Y. Li, S. A. Trask, Y. Chen, J. Decker, D. L. Robertson, M. L. Kalish, G. M. Shaw, S. Allen, B. H. Hahn, and F. Gao. 2001. Near full-length clones and reference sequences for subtype C isolates of HIV type 1 from three different continents. AIDS Res. Hum. Retrovir. 17:161-168.
42. Rose, P. P., and B. T. Korber. 2000. Detecting hypermutations in viral sequences with an emphasis on G → A hypermutation. Bioinformatics 16:400-401.
43. Rousseau, C., B. A. Birditt, A. R. McKay, J. N. Stoddard, T. C. Lee, S. McLaughlin, S. W. Moore, N. Shindo, G. H. Learn, B. T. Korber, C. Brander, P. J. Goulder, P. Kiepiela, B. D. Walker, and J. I. Mullins. 2006. Large-scale amplification, cloning and sequencing of near full-length HIV-1 subtype C genomes. J. Virol. Methods 136:118-125.
44. Sanabani, S., W. K. Neto, D. J. de Sa Filho, R. S. Diaz, P. Munerato, L. M. Janini, and E. C. Sabino. 2006. Full-length genome analysis of human immunodeficiency virus type 1 subtype C in Brazil. AIDS Res. Hum. Retrovir. 22:171-176.
45. Schierup, M. H., and J. Hein. 2000. Consequences of recombination on traditional phylogenetic analysis. Genetics 156:879-891.
46. Shankarappa, R., R. Chatterjee, G. H. Learn, D. Neogi, M. Ding, P. Roy, A. Ghosh, L. Kingsley, L. Harrison, J. I. Mullins, and P. Gupta. 2001. Human immunodeficiency virus type 1 Env sequences from Calcutta in eastern India: identification of features that distinguish subtype C sequences in India from other subtype C sequences. J. Virol. 75:10479-10487.
47. Shimodaira, H., and M. Hasegawa. 1999. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 16:1114-1116.
48. Shriner, D., A. G. Rodrigo, D. C. Nickle, and J. I. Mullins. 2004. Pervasive genomic recombination of HIV-1 in vivo. Genetics 167:1573- 1583.
49. Slatkin, M., and W. P. Maddison. 1989. A cladistic measure of gene flow inferred from the phylogenies of alleles. Genetics 123:603-613.
50. 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.
51. Reference deleted.
52. Soares, M. A., T. De Oliveira, R. M. Brindeiro, R. S. Diaz, E. C. Sabino, L. Brigido, I. L. Pires, M. G. Morgado, M. C. Dantas, D. Barreira, P. R. Teixeira, S. Cassol, and A. Tanuri. 2003. A specific subtype C of human immunodeficiency virus type 1 circulates in Brazil. AIDS 17:11-21.
53. Storey, J. D., and R. Tibshirani. 2003. Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. USA 100:9440-9445.
54. Swofford, D. L. 1999. PAUP* 4.0: phylogenetic analysis using parsimony (* and other methods), version 4.0b10. Sinauer Associates, Inc., Sunderland, MA.
55. Taylor, J. E., and B. T. Korber. 2005. HIV-1 intra-subtype superinfection rates: estimates using a structured coalescent with recombination. Infect. Genet. Evol. 5:85-95.
56. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
57. Travers, S. A., J. P. Clewley, J. R. Glynn, P. E. Fine, A. C. Crampin, F. Sibande, D. Mulawa, J. O. Mclnerney, and G. P. McCormack. 2004. Timing and reconstruction of the most recent common ancestor of the subtype C clade of human immunodeficiency virus type 1. J. Virol. 78:10501-10506.
58. van Harmelen, J., C. Williamson, B. Kim, L. Morris, J. Carr, S. S. Karim, and F. McCutchan. 2001. Characterization of full-length HIV type 1 subtype C sequences from South Africa. AIDS Res. Hum. Retrovir. 17:1527-1531.
59. Van Harmelen, J. H., E. Van der Ryst, A. S. Loubser, D. York, S. Madurai, S. Lyons, R. Wood, and C. Williamson. 1999. A predominantly HIV type 1 subtype C-restricted epidemic in South African urban populations. AIDS Res. Hum. Retrovir. 15:395-398.
60. van Rij, R. P., M. Worobey, J. A. Visser, and H. Schuitemaker. 2003. Evolution of R5 and X4 human immunodeficiency virus type 1 gag sequences in vivo: evidence for recombination. Virology 314:451-459.
61. 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.
62. Zhuang, J., A. E. Jetzt, G. Sun, H. Yu, G. Klarmann, Y. Ron, B. D. Preston, and J. P. Dougherty. 2002. Human immunodeficiency virus type 1 recombination: rate, fidelity, and putative hot spots. J. Virol. 76:11273-11282.
63. zur Megede, J., S. Engelbrecht, T. de Oliveira, S. Cassol, T. J. Scriba, E. J. van Rensburg, and S. W. Barnett. 2002. Novel evolutionary analyses of full-length HIV type 1 subtype C molecular clones from Cape Town, South Africa. AIDS Res. Hum. Retrovir. 18:1327-1332.