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. 1997 Jan;71(1):663–677. doi: 10.1128/jvi.71.1.663-677.1997

Human immunodeficiency virus type 1 genetic evolution in children with different rates of development of disease.

S Ganeshan 1, R E Dickover 1, B T Korber 1, Y J Bryson 1, S M Wolinsky 1
PMCID: PMC191099  PMID: 8985398

Abstract

The rate of development of disease varies considerably among human immunodeficiency virus type 1 (HIV-1)-infected children. The reasons for these observed differences are not clearly understood but most probably depend on the dynamic interplay between the HIV-1 quasispecies virus population and the immune constraints imposed by the host. To study the relationship between disease progression and genetic diversity, we analyzed the evolution of viral sequences within six perinatally infected children by examining proviral sequences spanning the C2 through V5 regions of the viral envelope gene by PCR of blood samples obtained at sequential visits. PCR product DNAs from four sample time points per child were cloned, and 10 to 13 clones from each sample were sequenced. Greater genetic distances relative to the time of infection were found for children with low virion-associated RNA burdens and slow progression to disease relative to those found for children with high virion-associated RNA burdens and rapid progression to disease. The greater branch lengths observed in the phylogenetic reconstructions correlated with a higher accumulation rate of nonsynonymous base substitutions per potential nonsynonymous site, consistent with positive selection for change rather than a difference in replication kinetics. Viral sequences from children with slow progression to disease also showed a tendency to form clusters that associated with different sampling times. These progressive shifts in the viral population were not found in viral sequences from children with rapid progression to disease. Therefore, despite the HIV-1 quasispecies being a diverse, rapidly evolving, and competing population of genetic variants, different rates of genetic evolution could be found under different selective constraints. These data suggest that the evolutionary dynamics exhibited by the HIV-1 quasispecies virus populations are compatible with a Darwinian system evolving under the constraints of natural selection.

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Selected References

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  1. Age-related standards for T lymphocyte subsets based on uninfected children born to human immunodeficiency virus 1-infected women. The European Collaborative Study. Pediatr Infect Dis J. 1992 Dec;11(12):1018–1026. [PubMed] [Google Scholar]
  2. Ahmad N., Baroudy B. M., Baker R. C., Chappey C. Genetic analysis of human immunodeficiency virus type 1 envelope V3 region isolates from mothers and infants after perinatal transmission. J Virol. 1995 Feb;69(2):1001–1012. doi: 10.1128/jvi.69.2.1001-1012.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aldhous M. C., Watret K. C., Mok J. Y., Bird A. G., Froebel K. S. Cytotoxic T lymphocyte activity and CD8 subpopulations in children at risk of HIV infection. Clin Exp Immunol. 1994 Jul;97(1):61–67. doi: 10.1111/j.1365-2249.1994.tb06580.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Alimenti A., Luzuriaga K., Stechenberg B., Sullivan J. L. Quantitation of human immunodeficiency virus in vertically infected infants and children. J Pediatr. 1991 Aug;119(2):225–229. doi: 10.1016/s0022-3476(05)80731-0. [DOI] [PubMed] [Google Scholar]
  5. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  6. Asjö B., Morfeldt-Månson L., Albert J., Biberfeld G., Karlsson A., Lidman K., Fenyö E. M. Replicative capacity of human immunodeficiency virus from patients with varying severity of HIV infection. Lancet. 1986 Sep 20;2(8508):660–662. [PubMed] [Google Scholar]
  7. Auger I., Thomas P., De Gruttola V., Morse D., Moore D., Williams R., Truman B., Lawrence C. E. Incubation periods for paediatric AIDS patients. Nature. 1988 Dec 8;336(6199):575–577. doi: 10.1038/336575a0. [DOI] [PubMed] [Google Scholar]
  8. Blanche S., Mayaux M. J., Rouzioux C., Teglas J. P., Firtion G., Monpoux F., Ciraru-Vigneron N., Meier F., Tricoire J., Courpotin C. Relation of the course of HIV infection in children to the severity of the disease in their mothers at delivery. N Engl J Med. 1994 Feb 3;330(5):308–312. doi: 10.1056/NEJM199402033300502. [DOI] [PubMed] [Google Scholar]
  9. Bryson Y. J., Luzuriaga K., Sullivan J. L., Wara D. W. Proposed definitions for in utero versus intrapartum transmission of HIV-1. N Engl J Med. 1992 Oct 22;327(17):1246–1247. doi: 10.1056/NEJM199210223271718. [DOI] [PubMed] [Google Scholar]
  10. Cao Y., Qin L., Zhang L., Safrit J., Ho D. D. Virologic and immunologic characterization of long-term survivors of human immunodeficiency virus type 1 infection. N Engl J Med. 1995 Jan 26;332(4):201–208. doi: 10.1056/NEJM199501263320401. [DOI] [PubMed] [Google Scholar]
  11. Carmichael A., Jin X., Sissons P., Borysiewicz L. Quantitative analysis of the human immunodeficiency virus type 1 (HIV-1)-specific cytotoxic T lymphocyte (CTL) response at different stages of HIV-1 infection: differential CTL responses to HIV-1 and Epstein-Barr virus in late disease. J Exp Med. 1993 Feb 1;177(2):249–256. doi: 10.1084/jem.177.2.249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chesebro B., Wehrly K., Nishio J., Perryman S. Macrophage-tropic human immunodeficiency virus isolates from different patients exhibit unusual V3 envelope sequence homogeneity in comparison with T-cell-tropic isolates: definition of critical amino acids involved in cell tropism. J Virol. 1992 Nov;66(11):6547–6554. doi: 10.1128/jvi.66.11.6547-6554.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cheynier R., Langlade-Demoyen P., Marescot M. R., Blanche S., Blondin G., Wain-Hobson S., Griscelli C., Vilmer E., Plata F. Cytotoxic T lymphocyte responses in the peripheral blood of children born to human immunodeficiency virus-1-infected mothers. Eur J Immunol. 1992 Sep;22(9):2211–2217. doi: 10.1002/eji.1830220905. [DOI] [PubMed] [Google Scholar]
  14. Coffin J. M. HIV population dynamics in vivo: implications for genetic variation, pathogenesis, and therapy. Science. 1995 Jan 27;267(5197):483–489. doi: 10.1126/science.7824947. [DOI] [PubMed] [Google Scholar]
  15. Connor R. I., Mohri H., Cao Y., Ho D. D. Increased viral burden and cytopathicity correlate temporally with CD4+ T-lymphocyte decline and clinical progression in human immunodeficiency virus type 1-infected individuals. J Virol. 1993 Apr;67(4):1772–1777. doi: 10.1128/jvi.67.4.1772-1777.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. De Rossi A., Giaquinto C., Ometto L., Mammano F., Zanotto C., Dunn D., Chieco-Bianchi L. Replication and tropism of human immunodeficiency virus type 1 as predictors of disease outcome in infants with vertically acquired infection. J Pediatr. 1993 Dec;123(6):929–936. doi: 10.1016/s0022-3476(05)80389-0. [DOI] [PubMed] [Google Scholar]
  17. Deacon N. J., Tsykin A., Solomon A., Smith K., Ludford-Menting M., Hooker D. J., McPhee D. A., Greenway A. L., Ellett A., Chatfield C. Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science. 1995 Nov 10;270(5238):988–991. doi: 10.1126/science.270.5238.988. [DOI] [PubMed] [Google Scholar]
  18. Delwart E. L., Sheppard H. W., Walker B. D., Goudsmit J., Mullins J. I. Human immunodeficiency virus type 1 evolution in vivo tracked by DNA heteroduplex mobility assays. J Virol. 1994 Oct;68(10):6672–6683. doi: 10.1128/jvi.68.10.6672-6683.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Dickover R. E., Dillon M., Gillette S. G., Deveikis A., Keller M., Plaeger-Marshall S., Chen I., Diagne A., Stiehm E. R., Bryson Y. Rapid increases in load of human immunodeficiency virus correlate with early disease progression and loss of CD4 cells in vertically infected infants. J Infect Dis. 1994 Nov;170(5):1279–1284. doi: 10.1093/infdis/170.5.1279. [DOI] [PubMed] [Google Scholar]
  20. Dickover R. E., Garratty E. M., Herman S. A., Sim M. S., Plaeger S., Boyer P. J., Keller M., Deveikis A., Stiehm E. R., Bryson Y. J. Identification of levels of maternal HIV-1 RNA associated with risk of perinatal transmission. Effect of maternal zidovudine treatment on viral load. JAMA. 1996 Feb 28;275(8):599–605. [PubMed] [Google Scholar]
  21. Duarte E. A., Novella I. S., Ledesma S., Clarke D. K., Moya A., Elena S. F., Domingo E., Holland J. J. Subclonal components of consensus fitness in an RNA virus clone. J Virol. 1994 Jul;68(7):4295–4301. doi: 10.1128/jvi.68.7.4295-4301.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Duliege A. M., Messiah A., Blanche S., Tardieu M., Griscelli C., Spira A. Natural history of human immunodeficiency virus type 1 infection in children: prognostic value of laboratory tests on the bimodal progression of the disease. Pediatr Infect Dis J. 1992 Aug;11(8):630–635. [PubMed] [Google Scholar]
  23. Faulkner D. V., Jurka J. Multiple aligned sequence editor (MASE). Trends Biochem Sci. 1988 Aug;13(8):321–322. doi: 10.1016/0968-0004(88)90129-6. [DOI] [PubMed] [Google Scholar]
  24. Felsenstein J. Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet. 1988;22:521–565. doi: 10.1146/annurev.ge.22.120188.002513. [DOI] [PubMed] [Google Scholar]
  25. Felsenstein J. The evolutionary advantage of recombination. Genetics. 1974 Oct;78(2):737–756. doi: 10.1093/genetics/78.2.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Fouchier R. A., Groenink M., Kootstra N. A., Tersmette M., Huisman H. G., Miedema F., Schuitemaker H. Phenotype-associated sequence variation in the third variable domain of the human immunodeficiency virus type 1 gp120 molecule. J Virol. 1992 May;66(5):3183–3187. doi: 10.1128/jvi.66.5.3183-3187.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Furtado M. R., Kingsley L. A., Wolinsky S. M. Changes in the viral mRNA expression pattern correlate with a rapid rate of CD4+ T-cell number decline in human immunodeficiency virus type 1-infected individuals. J Virol. 1995 Apr;69(4):2092–2100. doi: 10.1128/jvi.69.4.2092-2100.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Galli L., de Martino M., Tovo P. A., Gabiano C., Zappa M., Giaquinto C., Tulisso S., Vierucci A., Guerra M., Marchisio P. Onset of clinical signs in children with HIV-1 perinatal infection. Italian Register for HIV Infection in Children. AIDS. 1995 May;9(5):455–461. [PubMed] [Google Scholar]
  29. Greenough T. C., Somasundaran M., Brettler D. B., Hesselton R. M., Alimenti A., Kirchhoff F., Panicali D., Sullivan J. L. Normal immune function and inability to isolate virus in culture in an individual with long-term human immunodeficiency virus type 1 infection. AIDS Res Hum Retroviruses. 1994 Apr;10(4):395–403. doi: 10.1089/aid.1994.10.395. [DOI] [PubMed] [Google Scholar]
  30. Grubman S., Gross E., Lerner-Weiss N., Hernandez M., McSherry G. D., Hoyt L. G., Boland M., Oleske J. M. Older children and adolescents living with perinatally acquired human immunodeficiency virus infection. Pediatrics. 1995 May;95(5):657–663. [PubMed] [Google Scholar]
  31. Henrard D., Fauvel M., Samson J., Delage G., Boucher M., Hankins C., Stephens J., Lapointe N. Ontogeny of the humoral immune response to human immunodeficiency virus type 1 in infants. J Infect Dis. 1993 Aug;168(2):288–291. doi: 10.1093/infdis/168.2.288. [DOI] [PubMed] [Google Scholar]
  32. Holland J. J., De La Torre J. C., Steinhauer D. A. RNA virus populations as quasispecies. Curr Top Microbiol Immunol. 1992;176:1–20. doi: 10.1007/978-3-642-77011-1_1. [DOI] [PubMed] [Google Scholar]
  33. Holmes E. C., Zhang L. Q., Simmonds P., Ludlam C. A., Brown A. J. Convergent and divergent sequence evolution in the surface envelope glycoprotein of human immunodeficiency virus type 1 within a single infected patient. Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):4835–4839. doi: 10.1073/pnas.89.11.4835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Iversen A. K., Shpaer E. G., Rodrigo A. G., Hirsch M. S., Walker B. D., Sheppard H. W., Merigan T. C., Mullins J. I. Persistence of attenuated rev genes in a human immunodeficiency virus type 1-infected asymptomatic individual. J Virol. 1995 Sep;69(9):5743–5753. doi: 10.1128/jvi.69.9.5743-5753.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Kirchhoff F., Greenough T. C., Brettler D. B., Sullivan J. L., Desrosiers R. C. Brief report: absence of intact nef sequences in a long-term survivor with nonprogressive HIV-1 infection. N Engl J Med. 1995 Jan 26;332(4):228–232. doi: 10.1056/NEJM199501263320405. [DOI] [PubMed] [Google Scholar]
  36. Kitamura T. Summary of the epidemiology of HIV/AIDS in Japan. AIDS. 1994;8 (Suppl 2):S95–S97. [PubMed] [Google Scholar]
  37. Korber B. T., Farber R. M., Wolpert D. H., Lapedes A. S. Covariation of mutations in the V3 loop of human immunodeficiency virus type 1 envelope protein: an information theoretic analysis. Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7176–7180. doi: 10.1073/pnas.90.15.7176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Korber B. T., Learn G., Mullins J. I., Hahn B. H., Wolinsky S. Protecting HIV databases. Nature. 1995 Nov 16;378(6554):242–244. doi: 10.1038/378242a0. [DOI] [PubMed] [Google Scholar]
  39. Korber B., Wolinsky S., Haynes B., Kunstman K., Levy R., Furtado M., Otto P., Myers G. HIV-1 intrapatient sequence diversity in the immunogenic V3 region. AIDS Res Hum Retroviruses. 1992 Aug;8(8):1461–1465. doi: 10.1089/aid.1992.8.1461. [DOI] [PubMed] [Google Scholar]
  40. Kuiken C. L., de Jong J. J., Baan E., Keulen W., Tersmette M., Goudsmit J. Evolution of the V3 envelope domain in proviral sequences and isolates of human immunodeficiency virus type 1 during transition of the viral biological phenotype. J Virol. 1992 Jul;66(7):4622–4627. doi: 10.1128/jvi.66.7.4622-4627.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Kwok S., Higuchi R. Avoiding false positives with PCR. Nature. 1989 May 18;339(6221):237–238. doi: 10.1038/339237a0. [DOI] [PubMed] [Google Scholar]
  42. Lamers S. L., Sleasman J. W., She J. X., Barrie K. A., Pomeroy S. M., Barrett D. J., Goodenow M. M. Persistence of multiple maternal genotypes of human immunodeficiency virus type I in infants infected by vertical transmission. J Clin Invest. 1994 Jan;93(1):380–390. doi: 10.1172/JCI116970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Ljunggren K., Moschese V., Broliden P. A., Giaquinto C., Quinti I., Fenyö E. M., Wahren B., Rossi P., Jondal M. Antibodies mediating cellular cytotoxicity and neutralization correlate with a better clinical stage in children born to human immunodeficiency virus-infected mothers. J Infect Dis. 1990 Feb;161(2):198–202. doi: 10.1093/infdis/161.2.198. [DOI] [PubMed] [Google Scholar]
  44. Lukashov V. V., Kuiken C. L., Goudsmit J. Intrahost human immunodeficiency virus type 1 evolution is related to length of the immunocompetent period. J Virol. 1995 Nov;69(11):6911–6916. doi: 10.1128/jvi.69.11.6911-6916.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Luzuriaga K., Holmes D., Hereema A., Wong J., Panicali D. L., Sullivan J. L. HIV-1-specific cytotoxic T lymphocyte responses in the first year of life. J Immunol. 1995 Jan 1;154(1):433–443. [PubMed] [Google Scholar]
  46. Luzuriaga K., Koup R. A., Pikora C. A., Brettler D. B., Sullivan J. L. Deficient human immunodeficiency virus type 1-specific cytotoxic T cell responses in vertically infected children. J Pediatr. 1991 Aug;119(2):230–236. doi: 10.1016/s0022-3476(05)80732-2. [DOI] [PubMed] [Google Scholar]
  47. Mammano F., Salvatori F., Ometto L., Panozzo M., Chieco-Bianchi L., De Rossi A. Relationship between the V3 loop and the phenotypes of human immunodeficiency virus type 1 (HIV-1) isolates from children perinatally infected with HIV-1. J Virol. 1995 Jan;69(1):82–92. doi: 10.1128/jvi.69.1.82-92.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Marthas M. L., van Rompay K. K., Otsyula M., Miller C. J., Canfield D. R., Pedersen N. C., McChesney M. B. Viral factors determine progression to AIDS in simian immunodeficiency virus-infected newborn rhesus macaques. J Virol. 1995 Jul;69(7):4198–4205. doi: 10.1128/jvi.69.7.4198-4205.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. McFarland E. J., Curiel T. J., Schoen D. J., Rosandich M. E., Schooley R. T., Kuritzkes D. R. Cytotoxic T lymphocyte lines specific for human immunodeficiency virus type 1 Gag and reverse transcriptase derived from a vertically infected child. J Infect Dis. 1993 Mar;167(3):719–723. doi: 10.1093/infdis/167.3.719. [DOI] [PubMed] [Google Scholar]
  50. Michael N. L., Chang G., d'Arcy L. A., Tseng C. J., Birx D. L., Sheppard H. W. Functional characterization of human immunodeficiency virus type 1 nef genes in patients with divergent rates of disease progression. J Virol. 1995 Nov;69(11):6758–6769. doi: 10.1128/jvi.69.11.6758-6769.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Miedema F., Meyaard L., Koot M., Klein M. R., Roos M. T., Groenink M., Fouchier R. A., Van't Wout A. B., Tersmette M., Schellekens P. T. Changing virus-host interactions in the course of HIV-1 infection. Immunol Rev. 1994 Aug;140:35–72. doi: 10.1111/j.1600-065x.1994.tb00864.x. [DOI] [PubMed] [Google Scholar]
  52. Mulder-Kampinga G. A., Kuiken C., Dekker J., Scherpbier H. J., Boer K., Goudsmit J. Genomic human immunodeficiency virus type 1 RNA variation in mother and child following intra-uterine virus transmission. J Gen Virol. 1993 Sep;74(Pt 9):1747–1756. doi: 10.1099/0022-1317-74-9-1747. [DOI] [PubMed] [Google Scholar]
  53. Nei M., Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986 Sep;3(5):418–426. doi: 10.1093/oxfordjournals.molbev.a040410. [DOI] [PubMed] [Google Scholar]
  54. Nieburg P., Hu D. J., Moses S., Nagelkerke N. Contribution of breastfeeding to the reported variation in rates of mother-to-child HIV transmission. AIDS. 1995 Apr;9(4):396–397. [PubMed] [Google Scholar]
  55. Novella I. S., Elena S. F., Moya A., Domingo E., Holland J. J. Size of genetic bottlenecks leading to virus fitness loss is determined by mean initial population fitness. J Virol. 1995 May;69(5):2869–2872. doi: 10.1128/jvi.69.5.2869-2872.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Nowak M. A., Anderson R. M., McLean A. R., Wolfs T. F., Goudsmit J., May R. M. Antigenic diversity thresholds and the development of AIDS. Science. 1991 Nov 15;254(5034):963–969. doi: 10.1126/science.1683006. [DOI] [PubMed] [Google Scholar]
  57. Plaeger-Marshall S., Hultin P., Bertolli J., O'Rourke S., Kobayashi R., Kobayashi A. L., Giorgi J. V., Bryson Y., Stiehm E. R. Activation and differentiation antigens on T cells of healthy, at-risk, and HIV-infected children. J Acquir Immune Defic Syndr. 1993 Sep;6(9):984–993. [PubMed] [Google Scholar]
  58. Pollack H., Zhan M. X., Ilmet-Moore T., Ajuang-Simbiri K., Krasinski K., Borkowsky W. Ontogeny of anti-human immunodeficiency virus (HIV) antibody production in HIV-1-infected infants. Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2340–2344. doi: 10.1073/pnas.90.6.2340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Richman D. D., Bozzette S. A. The impact of the syncytium-inducing phenotype of human immunodeficiency virus on disease progression. J Infect Dis. 1994 May;169(5):968–974. doi: 10.1093/infdis/169.5.968. [DOI] [PubMed] [Google Scholar]
  60. Safrit J. T., Andrews C. A., Zhu T., Ho D. D., Koup R. A. Characterization of human immunodeficiency virus type 1-specific cytotoxic T lymphocyte clones isolated during acute seroconversion: recognition of autologous virus sequences within a conserved immunodominant epitope. J Exp Med. 1994 Feb 1;179(2):463–472. doi: 10.1084/jem.179.2.463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Schuitemaker H., Koot M., Kootstra N. A., Dercksen M. W., de Goede R. E., van Steenwijk R. P., Lange J. M., Schattenkerk J. K., Miedema F., Tersmette M. Biological phenotype of human immunodeficiency virus type 1 clones at different stages of infection: progression of disease is associated with a shift from monocytotropic to T-cell-tropic virus population. J Virol. 1992 Mar;66(3):1354–1360. doi: 10.1128/jvi.66.3.1354-1360.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Schuitemaker H., Kootstra N. A., de Goede R. E., de Wolf F., Miedema F., Tersmette M. Monocytotropic human immunodeficiency virus type 1 (HIV-1) variants detectable in all stages of HIV-1 infection lack T-cell line tropism and syncytium-inducing ability in primary T-cell culture. J Virol. 1991 Jan;65(1):356–363. doi: 10.1128/jvi.65.1.356-363.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Scott G. B., Buck B. E., Leterman J. G., Bloom F. L., Parks W. P. Acquired immunodeficiency syndrome in infants. N Engl J Med. 1984 Jan 12;310(2):76–81. doi: 10.1056/NEJM198401123100202. [DOI] [PubMed] [Google Scholar]
  64. Shioda T., Levy J. A., Cheng-Mayer C. Macrophage and T cell-line tropisms of HIV-1 are determined by specific regions of the envelope gp120 gene. Nature. 1991 Jan 10;349(6305):167–169. doi: 10.1038/349167a0. [DOI] [PubMed] [Google Scholar]
  65. Simmonds P., Balfe P., Ludlam C. A., Bishop J. O., Brown A. J. Analysis of sequence diversity in hypervariable regions of the external glycoprotein of human immunodeficiency virus type 1. J Virol. 1990 Dec;64(12):5840–5850. doi: 10.1128/jvi.64.12.5840-5850.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Smith R. F., Smith T. F. Automatic generation of primary sequence patterns from sets of related protein sequences. Proc Natl Acad Sci U S A. 1990 Jan;87(1):118–122. doi: 10.1073/pnas.87.1.118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Smith R. F., Smith T. F. Pattern-induced multi-sequence alignment (PIMA) algorithm employing secondary structure-dependent gap penalties for use in comparative protein modelling. Protein Eng. 1992 Jan;5(1):35–41. doi: 10.1093/protein/5.1.35. [DOI] [PubMed] [Google Scholar]
  68. Spencer L. T., Ogino M. T., Dankner W. M., Spector S. A. Clinical significance of human immunodeficiency virus type 1 phenotypes in infected children. J Infect Dis. 1994 Mar;169(3):491–495. doi: 10.1093/infdis/169.3.491. [DOI] [PubMed] [Google Scholar]
  69. Spira A. I., Ho D. D. Effect of different donor cells on human immunodeficiency virus type 1 replication and selection in vitro. J Virol. 1995 Jan;69(1):422–429. doi: 10.1128/jvi.69.1.422-429.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Strunnikova N., Ray S. C., Livingston R. A., Rubalcaba E., Viscidi R. P. Convergent evolution within the V3 loop domain of human immunodeficiency virus type 1 in association with disease progression. J Virol. 1995 Dec;69(12):7548–7558. doi: 10.1128/jvi.69.12.7548-7558.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Tersmette M., Gruters R. A., de Wolf F., de Goede R. E., Lange J. M., Schellekens P. T., Goudsmit J., Huisman H. G., Miedema F. Evidence for a role of virulent human immunodeficiency virus (HIV) variants in the pathogenesis of acquired immunodeficiency syndrome: studies on sequential HIV isolates. J Virol. 1989 May;63(5):2118–2125. doi: 10.1128/jvi.63.5.2118-2125.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Tersmette M., Lange J. M., de Goede R. E., de Wolf F., Eeftink-Schattenkerk J. K., Schellekens P. T., Coutinho R. A., Huisman J. G., Goudsmit J., Miedema F. Association between biological properties of human immunodeficiency virus variants and risk for AIDS and AIDS mortality. Lancet. 1989 May 6;1(8645):983–985. doi: 10.1016/s0140-6736(89)92628-7. [DOI] [PubMed] [Google Scholar]
  73. Tersmette M., de Goede R. E., Al B. J., Winkel I. N., Gruters R. A., Cuypers H. T., Huisman H. G., Miedema F. Differential syncytium-inducing capacity of human immunodeficiency virus isolates: frequent detection of syncytium-inducing isolates in patients with acquired immunodeficiency syndrome (AIDS) and AIDS-related complex. J Virol. 1988 Jun;62(6):2026–2032. doi: 10.1128/jvi.62.6.2026-2032.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Tovo P. A., de Martino M., Gabiano C., Cappello N., D'Elia R., Loy A., Plebani A., Zuccotti G. V., Dallacasa P., Ferraris G. Prognostic factors and survival in children with perinatal HIV-1 infection. The Italian Register for HIV Infections in Children. Lancet. 1992 May 23;339(8804):1249–1253. doi: 10.1016/0140-6736(92)91592-v. [DOI] [PubMed] [Google Scholar]
  75. Tovo P. A., de Martino M., Gabiano C., Galli L., Tibaldi C., Vierucci A., Veglia F. AIDS appearance in children is associated with the velocity of disease progression in their mothers. J Infect Dis. 1994 Oct;170(4):1000–1002. doi: 10.1093/infdis/170.4.1000. [DOI] [PubMed] [Google Scholar]
  76. Walker B. D., Chakrabarti S., Moss B., Paradis T. J., Flynn T., Durno A. G., Blumberg R. S., Kaplan J. C., Hirsch M. S., Schooley R. T. HIV-specific cytotoxic T lymphocytes in seropositive individuals. Nature. 1987 Jul 23;328(6128):345–348. doi: 10.1038/328345a0. [DOI] [PubMed] [Google Scholar]
  77. Willey R. L., Theodore T. S., Martin M. A. Amino acid substitutions in the human immunodeficiency virus type 1 gp120 V3 loop that change viral tropism also alter physical and functional properties of the virion envelope. J Virol. 1994 Jul;68(7):4409–4419. doi: 10.1128/jvi.68.7.4409-4419.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Wolfs T. F., de Jong J. J., Van den Berg H., Tijnagel J. M., Krone W. J., Goudsmit J. Evolution of sequences encoding the principal neutralization epitope of human immunodeficiency virus 1 is host dependent, rapid, and continuous. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9938–9942. doi: 10.1073/pnas.87.24.9938. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Wolinsky S. M., Korber B. T., Neumann A. U., Daniels M., Kunstman K. J., Whetsell A. J., Furtado M. R., Cao Y., Ho D. D., Safrit J. T. Adaptive evolution of human immunodeficiency virus-type 1 during the natural course of infection. Science. 1996 Apr 26;272(5261):537–542. doi: 10.1126/science.272.5261.537. [DOI] [PubMed] [Google Scholar]
  80. Wolinsky S. M., Wike C. M., Korber B. T., Hutto C., Parks W. P., Rosenblum L. L., Kunstman K. J., Furtado M. R., Muñoz J. L. Selective transmission of human immunodeficiency virus type-1 variants from mothers to infants. Science. 1992 Feb 28;255(5048):1134–1137. doi: 10.1126/science.1546316. [DOI] [PubMed] [Google Scholar]
  81. de la Torre J. C., Wimmer E., Holland J. J. Very high frequency of reversion to guanidine resistance in clonal pools of guanidine-dependent type 1 poliovirus. J Virol. 1990 Feb;64(2):664–671. doi: 10.1128/jvi.64.2.664-671.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]

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