1887

Abstract

Understanding the properties of viruses preferentially establishing infection during perinatal transmission of human immunodeficiency virus type 1 (HIV-1) is critical for the development of effective measures to prevent transmission. A previous study demonstrated that the newly transmitted viruses (in infants) of chronically infected mother–infant pairs (MIPs) were fitter in terms of growth, which was imparted by their envelope (Env) glycoprotein V1–V5 regions, than those in the corresponding chronically infected mothers. In order to investigate whether the higher fitness of transmitted viruses was conferred by their higher entry efficiency directed by the V1–V5 regions during perinatal transmission, the fusogenicity of Env containing V1–V5 regions derived from transmitted and non-tranmsmitted viruses of five chronically infected MIPs and two acutely infected MIPs was analysed using two different cell–cell fusion assays. The results showed that, in one chronically infected MIP, a higher fusion efficiency was induced by the infant Env V1–V5 compared with that of the corresponding mother. Moreover, the V4–V5 regions played an important role in discriminating the transmitted and non-transmitted viruses in this pair. However, neither a consistent pattern nor significant differences in fusogenicity mediated by the V1–V5 regions between maternal and infant variants was observed in the other MIPs. This study suggests that there is no consistent and significant correlation between viral fitness selection and entry efficiency directed by the V1–V5 regions during perinatal transmission. Other factors such as the route and timing of transmission may also be involved.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.046771-0
2012-12-01
2020-01-27
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/12/2635.html?itemId=/content/journal/jgv/10.1099/vir.0.046771-0&mimeType=html&fmt=ahah

References

  1. Abrahamyan L. G., Markosyan R. M., Moore J. P., Cohen F. S., Melikyan G. B.. ( 2003;). Human immunodeficiency virus type 1 Env with an intersubunit disulfide bond engages coreceptors but requires bond reduction after engagement to induce fusion. . J Virol 77:, 5829–5836. [CrossRef][PubMed]
    [Google Scholar]
  2. Ahmad N.. ( 2005;). The vertical transmission of human immunodeficiency virus type 1: molecular and biological properties of the virus. . Crit Rev Clin Lab Sci 42:, 1–34. [CrossRef][PubMed]
    [Google Scholar]
  3. Alcântara K. C., Lins J. B., Albuquerque M., Aires L. M., Cardoso L. P., Minuzzi A. L., Stefani M. M.. ( 2012;). HIV-1 mother-to-child transmission and drug resistance among Brazilian pregnant women with high access to diagnosis and prophylactic measures. . J Clin Virol 54:, 15–20. [CrossRef][PubMed]
    [Google Scholar]
  4. Barin F., Jourdain G., Brunet S., Ngo-Giang-Huong N., Weerawatgoompa S., Karnchanamayul W., Ariyadej S., Hansudewechakul R., Achalapong J.. & other authors ( 2006;). Revisiting the role of neutralizing antibodies in mother-to-child transmission of HIV-1. . J Infect Dis 193:, 1504–1511. [CrossRef][PubMed]
    [Google Scholar]
  5. Briant L., Wade C. M., Puel J., Brown A. J., Guyader M.. ( 1995;). Analysis of envelope sequence variants suggests multiple mechanisms of mother-to-child transmission of human immunodeficiency virus type 1. . J Virol 69:, 3778–3788.[PubMed]
    [Google Scholar]
  6. Bültmann A., Muranyi W., Seed B., Haas J.. ( 2001;). Identification of two sequences in the cytoplasmic tail of the human immunodeficiency virus type 1 envelope glycoprotein that inhibit cell surface expression. . J Virol 75:, 5263–5276. [CrossRef][PubMed]
    [Google Scholar]
  7. Checkley M. A., Luttge B. G., Freed E. O.. ( 2011;). HIV-1 envelope glycoprotein biosynthesis, trafficking, and incorporation. . J Mol Biol 410:, 582–608. [CrossRef][PubMed]
    [Google Scholar]
  8. Chen B., Vogan E. M., Gong H., Skehel J. J., Wiley D. C., Harrison S. C.. ( 2005;). Structure of an unliganded simian immunodeficiency virus gp120 core. . Nature 433:, 834–841. [CrossRef][PubMed]
    [Google Scholar]
  9. Cohen F. S., Melikyan G. B.. ( 1998;). Methodologies in the study of cell–cell fusion. . Methods 16:, 215–226. [CrossRef][PubMed]
    [Google Scholar]
  10. Dash B., McIntosh A., Barrett W., Daniels R.. ( 1994;). Deletion of a single N-linked glycosylation site from the transmembrane envelope protein of human immunodeficiency virus type 1 stops cleavage and transport of gp160 preventing env-mediated fusion. . J Gen Virol 75:, 1389–1397. [CrossRef][PubMed]
    [Google Scholar]
  11. Deng H., Liu R., Ellmeier W., Choe S., Unutmaz D., Burkhart M., Di Marzio P., Marmon S., Sutton R. E.. & other authors ( 1996;). Identification of a major co-receptor for primary isolates of HIV-1. . Nature 381:, 661–666. [CrossRef][PubMed]
    [Google Scholar]
  12. Derdeyn C. A., Decker J. M., Bibollet-Ruche F., Mokili J. L., Muldoon M., Denham S. A., Heil M. L., Kasolo F., Musonda R.. & other authors ( 2004;). Envelope-constrained neutralization-sensitive HIV-1 after heterosexual transmission. . Science 303:, 2019–2022. [CrossRef][PubMed]
    [Google Scholar]
  13. Dickover R. E., Garratty E. M., Plaeger S., Bryson Y. J.. ( 2001;). Perinatal transmission of major, minor, and multiple maternal human immunodeficiency virus type 1 variants in utero and intrapartum. . J Virol 75:, 2194–2203. [CrossRef][PubMed]
    [Google Scholar]
  14. Dickover R., Garratty E., Yusim K., Miller C., Korber B., Bryson Y.. ( 2006;). Role of maternal autologous neutralizing antibody in selective perinatal transmission of human immunodeficiency virus type 1 escape variants. . J Virol 80:, 6525–6533. [CrossRef][PubMed]
    [Google Scholar]
  15. Fenouillet E., Jones I. M.. ( 1995;). The glycosylation of human immunodeficiency virus type 1 transmembrane glycoprotein (gp41) is important for the efficient intracellular transport of the envelope precursor gp160. . J Gen Virol 76:, 1509–1514. [CrossRef][PubMed]
    [Google Scholar]
  16. Furuta R. A., Nishikawa M., Fujisawa J.. ( 2006;). Real-time analysis of human immunodeficiency virus type 1 Env-mediated membrane fusion by fluorescence resonance energy transfer. . Microbes Infect 8:, 520–532. [CrossRef][PubMed]
    [Google Scholar]
  17. Gray L., Sterjovski J., Ramsland P. A., Churchill M. J., Gorry P. R.. ( 2011;). Conformational alterations in the CD4 binding cavity of HIV-1 gp120 influencing gp120–CD4 interactions and fusogenicity of HIV-1 envelopes derived from brain and other tissues. . Retrovirology 8:, 42. [CrossRef][PubMed]
    [Google Scholar]
  18. Guo H. G., Veronese F. M., Tschachler E., Pal R., Kalyanaraman V. S., Gallo R. C., Reitz M. S. Jr. ( 1990;). Characterization of an HIV-1 point mutant blocked in envelope glycoprotein cleavage. . Virology 174:, 217–224. [CrossRef][PubMed]
    [Google Scholar]
  19. Hoffmann F. G., He X., West J. T., Lemey P., Kankasa C., Wood C.. ( 2008;). Genetic variation in mother-child acute seroconverter pairs from Zambia. . AIDS 22:, 817–824. [CrossRef][PubMed]
    [Google Scholar]
  20. Keele B. F., Giorgi E. E., Salazar-Gonzalez J. F., Decker J. M., Pham K. T., Salazar M. G., Sun C., Grayson T., Wang S.. & other authors ( 2008;). Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. . Proc Natl Acad Sci U S A 105:, 7552–7557. [CrossRef][PubMed]
    [Google Scholar]
  21. Kishko M., Somasundaran M., Brewster F., Sullivan J. L., Clapham P. R., Luzuriaga K.. ( 2011;). Genotypic and functional properties of early infant HIV-1 envelopes. . Retrovirology 8:, 67. [CrossRef][PubMed]
    [Google Scholar]
  22. Kong X., West J. T., Zhang H., Shea D. M., M’soka T. J., Wood C.. ( 2008;). The human immunodeficiency virus type 1 envelope confers higher rates of replicative fitness to perinatally transmitted viruses than to nontransmitted viruses. . J Virol 82:, 11609–11618. [CrossRef][PubMed]
    [Google Scholar]
  23. Kwiek J. J., Russell E. S., Dang K. K., Burch C. L., Mwapasa V., Meshnick S. R., Swanstrom R.. ( 2008;). The molecular epidemiology of HIV-1 envelope diversity during HIV-1 subtype C vertical transmission in Malawian mother–infant pairs. . AIDS 22:, 863–871. [CrossRef][PubMed]
    [Google Scholar]
  24. Lassen K. G., Lobritz M. A., Bailey J. R., Johnston S., Nguyen S., Lee B., Chou T., Siliciano R. F., Markowitz M., Arts E. J.. ( 2009;). Elite suppressor-derived HIV-1 envelope glycoproteins exhibit reduced entry efficiency and kinetics. . PLoS Pathog 5:, e1000377. [CrossRef][PubMed]
    [Google Scholar]
  25. Luzuriaga K.. ( 2007;). Mother-to-child transmission of HIV: a global perspective. . Curr Infect Dis Rep 9:, 511–517. [CrossRef][PubMed]
    [Google Scholar]
  26. Mantina H., Kankasa C., Klaskala W., Brayfield B., Campbell J., Du Q., Bhat G., Kasolo F., Mitchell C., Wood C.. ( 2001;). Vertical transmission of Kaposi’s sarcoma-associated herpesvirus. . Int J Cancer 94:, 749–752. [CrossRef][PubMed]
    [Google Scholar]
  27. Marozsan A. J., Moore D. M., Lobritz M. A., Fraundorf E., Abraha A., Reeves J. D., Arts E. J.. ( 2005;). Differences in the fitness of two diverse wild-type human immunodeficiency virus type 1 isolates are related to the efficiency of cell binding and entry. . J Virol 79:, 7121–7134. [CrossRef][PubMed]
    [Google Scholar]
  28. Martinez-Picado J., Prado J. G., Fry E. E., Pfafferott K., Leslie A., Chetty S., Thobakgale C., Honeyborne I., Crawford H.. & other authors ( 2006;). Fitness cost of escape mutations in p24 Gag in association with control of human immunodeficiency virus type 1. . J Virol 80:, 3617–3623. [CrossRef][PubMed]
    [Google Scholar]
  29. Muñoz-Barroso I., Durell S., Sakaguchi K., Appella E., Blumenthal R.. ( 1998;). Dilation of the human immunodeficiency virus-1 envelope glycoprotein fusion pore revealed by the inhibitory action of a synthetic peptide from gp41. . J Cell Biol 140:, 315–323. [CrossRef][PubMed]
    [Google Scholar]
  30. Pancera M., Majeed S., Ban Y. E., Chen L., Huang C.-C., Kong L., Kwon Y. D., Stuckey J., Zhou T.. & other authors ( 2010;). Structure of HIV-1 gp120 with gp41-interactive region reveals layered envelope architecture and basis of conformational mobility. . Proc Natl Acad Sci U S A 107:, 1166–1171. [CrossRef][PubMed]
    [Google Scholar]
  31. Rossi F., Querido B., Nimmagadda M., Cocklin S., Navas-Martín S., Martín-García J.. ( 2008;). The V1–V3 region of a brain-derived HIV-1 envelope glycoprotein determines macrophage tropism, low CD4 dependence, increased fusogenicity and altered sensitivity to entry inhibitors. . Retrovirology 5:, 89. [CrossRef][PubMed]
    [Google Scholar]
  32. Scarlatti G., Leitner T., Halapi E., Wahlberg J., Marchisio P., Clerici-Schoeller M. A., Wigzell H., Fenyö E. M., Albert J.. & other authors ( 1993;). Comparison of variable region 3 sequences of human immunodeficiency virus type 1 from infected children with the RNA and DNA sequences of the virus populations of their mothers. . Proc Natl Acad Sci U S A 90:, 1721–1725. [CrossRef][PubMed]
    [Google Scholar]
  33. Steain M. C., Wang B., Saksena N. K.. ( 2006;). Analysis of HIV-1 sequences vertically transmitted to infants in Kisumu, Kenya. . J Clin Virol 36:, 298–302. [CrossRef][PubMed]
    [Google Scholar]
  34. Sterjovski J., Churchill M. J., Ellett A., Gray L. R., Roche M. J., Dunfee R. L., Purcell D. F., Saksena N., Wang B.. & other authors ( 2007;). Asn 362 in gp120 contributes to enhanced fusogenicity by CCR5-restricted HIV-1 envelope glycoprotein variants from patients with AIDS. . Retrovirology 4:, 89. [CrossRef][PubMed]
    [Google Scholar]
  35. Sterjovski J., Churchill M. J., Roche M., Ellett A., Farrugia W., Wesselingh S. L., Cunningham A. L., Ramsland P. A., Gorry P. R.. ( 2011;). CD4-binding site alterations in CCR5-using HIV-1 envelopes influencing gp120-CD4 interactions and fusogenicity. . Virology 410:, 418–428. [CrossRef][PubMed]
    [Google Scholar]
  36. Verhofstede C., Demecheleer E., De Cabooter N., Gaillard P., Mwanyumba F., Claeys P., Chohan V., Mandaliya K., Temmerman M., Plum J.. ( 2003;). Diversity of the human immunodeficiency virus type 1 (HIV-1) env sequence after vertical transmission in mother–child pairs infected with HIV-1 subtype A. . J Virol 77:, 3050–3057. [CrossRef][PubMed]
    [Google Scholar]
  37. Wei X., Decker J. M., Wang S., Hui H., Kappes J. C., Wu X., Salazar-Gonzalez J. F., Salazar M. G., Kilby J. M.. & other authors ( 2003;). Antibody neutralization and escape by HIV-1. . Nature 422:, 307–312. [CrossRef][PubMed]
    [Google Scholar]
  38. Willey R. L., Klimkait T., Frucht D. M., Bonifacinot J. S., Martin M. A.. ( 1991;). Mutations within the human immunodeficiency virus type 1 gp160 envelope glycoprotein alter its intracellular transport and processing. . Virology 184:, 319–329. [CrossRef][PubMed]
    [Google Scholar]
  39. 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.. ( 1992;). Selective transmission of human immunodeficiency virus type-1 variants from mothers to infants. . Science 255:, 1134–1137. [CrossRef][PubMed]
    [Google Scholar]
  40. Wyatt R., Kwong P. D., Desjardins E., Sweet R. W., Robinson J., Hendrickson W. A., Sodroski J. G.. ( 1998;). The antigenic structure of the HIV gp120 envelope glycoprotein. . Nature 393:, 705–711. [CrossRef][PubMed]
    [Google Scholar]
  41. Zhang H., Hoffmann F., He J., He X., Kankasa C., West J. T., Mitchell C. D., Ruprecht R. M., Orti G., Wood C.. ( 2006;). Characterization of HIV-1 subtype C envelope glycoproteins from perinatally infected children with different courses of disease. . Retrovirology 3:, 73. [CrossRef][PubMed]
    [Google Scholar]
  42. Zhang H., Rola M., West J. T., Tully D. C., Kubis P., He J., Kankasa C., Wood C.. ( 2010a;). Functional properties of the HIV-1 subtype C envelope glycoprotein associated with mother-to-child transmission. . Virology 400:, 164–174. [CrossRef][PubMed]
    [Google Scholar]
  43. Zhang H., Tully D. C., Hoffmann F. G., He J., Kankasa C., Wood C.. ( 2010b;). Restricted genetic diversity of HIV-1 subtype C envelope glycoprotein from perinatally infected Zambian infants. . PLoS ONE 5:, e9294. [CrossRef][PubMed]
    [Google Scholar]
  44. Zhu T., Mo H., Wang N., Nam D. S., Cao Y., Koup R. A., Ho D. D.. ( 1993;). Genotypic and phenotypic characterization of HIV-1 patients with primary infection. . Science 261:, 1179–1181. [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.046771-0
Loading
/content/journal/jgv/10.1099/vir.0.046771-0
Loading

Data & Media loading...

Supplements

Supplementary table 

PDF

Most cited articles

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error