1887

Abstract

The binding of human immunodeficiency virus (HIV) to C-type lectin receptors may result in either enhanced -infection of T-cells or virus degradation. We have investigated the efficacy of HIV-1 utilization of DC-SIGN, a C-type lectin receptor, in the setting of intrauterine or intrapartum mother-to-child transmission (MTCT). Viruses isolated from HIV-1-infected mothers at delivery and from their vertically infected children both shortly after birth and later during the progression of the disease were analysed for their use of DC-SIGN, binding and ability to -infect. DC-SIGN use of a child’s earlier virus isolate tended to be reduced as compared with that of the corresponding maternal isolate. Furthermore, the children’s later isolate displayed enhanced DC-SIGN utilization compared with that of the corresponding earlier virus. These results were also supported in head-to-head competition assays and suggest that HIV-1 variants displaying efficient DC-SIGN use are not selected for during intrauterine or intrapartum MTCT. However, viruses with increased DC-SIGN use may evolve later in paediatric HIV-1 infections.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.043620-0
2013-04-01
2020-07-10
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/4/767.html?itemId=/content/journal/jgv/10.1099/vir.0.043620-0&mimeType=html&fmt=ahah

References

  1. Backé E., Jiménez E., Unger M., Schäfer A., Jauniaux E., Vogel M. 1992; Demonstration of HIV-1 infected cells in human placenta by in situ hybridisation and immunostaining. J Clin Pathol 45:871–874 [CrossRef][PubMed]
    [Google Scholar]
  2. Baribaud F., Pöhlmann S., Doms R. W. 2001; The role of DC-SIGN and DC-SIGNR in HIV and SIV attachment, infection, and transmission. Virology 286:1–6 [CrossRef][PubMed]
    [Google Scholar]
  3. Boily-Larouche G., Iscache A. L., Zijenah L. S., Humphrey J. H., Mouland A. J., Ward B. J., Roger M. 2009; Functional genetic variants in DC-SIGNR are associated with mother-to-child transmission of HIV-1. PLoS ONE 4:e7211 [CrossRef][PubMed]
    [Google Scholar]
  4. Boily-Larouche G., Milev M. P., Zijenah L. S., Labbé A. C., Zannou D. M., Humphrey J. H., Ward B. J., Poudrier J., Mouland A. J. other authors 2012; Naturally-occurring genetic variants in human DC-SIGN increase HIV-1 capture, cell-transfer and risk of mother-to-child transmission. PLoS ONE 7:e40706 [CrossRef][PubMed]
    [Google Scholar]
  5. Borggren M., Repits J., Kuylenstierna C., Sterjovski J., Churchill M. J., Purcell D. F., Karlsson A., Albert J., Gorry P. R., Jansson M. 2008; Evolution of DC-SIGN use revealed by fitness studies of R5 HIV-1 variants emerging during AIDS progression. Retrovirology 5:28 [CrossRef][PubMed]
    [Google Scholar]
  6. Cameron P. U., Freudenthal P. S., Barker J. M., Gezelter S., Inaba K., Steinman R. M. 1992; Dendritic cells exposed to human immunodeficiency virus type-1 transmit a vigorous cytopathic infection to CD4+ T cells. Science 257:383–387 [CrossRef][PubMed]
    [Google Scholar]
  7. Canque B., Bakri Y., Camus S., Yagello M., Benjouad A., Gluckman J. C. 1999; The susceptibility to X4 and R5 human immunodeficiency virus-1 strains of dendritic cells derived in vitro from CD34+ hematopoietic progenitor cells is primarily determined by their maturation stage. Blood 93:3866–3875[PubMed]
    [Google Scholar]
  8. Casper C., Navér L., Clevestig P., Belfrage E., Leitner T., Albert J., Lindgren S., Ottenblad C., Bohlin A. B. other authors 2002a; Coreceptor change appears after immune deficiency is established in children infected with different HIV-1 subtypes. AIDS Res Hum Retroviruses 18:343–352 [CrossRef][PubMed]
    [Google Scholar]
  9. Casper C. H., Clevestig P., Carlenor E., Leitner T., Anzén B., Lidman K., Belfrage E., Albert J., Bohlin A. B. other authors 2002b; Link between the X4 phenotype in human immunodeficiency virus type 1-infected mothers and their children, despite the early presence of R5 in the child. J Infect Dis 186:914–921 [CrossRef][PubMed]
    [Google Scholar]
  10. CDC 1994; Revised classification system for human immunodeficiency virus infection in children less than 13 years of age. MMWR Morb Mortal Wkly Rep 431–10
    [Google Scholar]
  11. Contag C. H., Ehrnst A., Duda J., Bohlin A. B., Lindgren S., Learn G. H., Mullins J. I. 1997; Mother-to-infant transmission of human immunodeficiency virus type 1 involving five envelope sequence subtypes. J Virol 71:1292–1300[PubMed]
    [Google Scholar]
  12. da Silva R. C., Segat L., Crovella S. 2011; Role of DC-SIGN and L-SIGN receptors in HIV-1 vertical transmission. Hum Immunol 72:305–311 [CrossRef][PubMed]
    [Google Scholar]
  13. Dictor M., Lindgren S., Bont J., Anzén B., Lidman K., Wallin K. L., Navér L., Bohlin A. B., Ehrnst A. Michael Dictor, Susanne Lindgren, J 2001; HIV-1 in placentas of untreated HIV-1-infected women in relation to viral transmission, infectious HIV-1 and RNA load in plasma. Scand J Infect Dis 33:27–32 [CrossRef][PubMed]
    [Google Scholar]
  14. Geijtenbeek T. B., Kwon D. S., Torensma R., van Vliet S. J., van Duijnhoven G. C., Middel J., Cornelissen I. L., Nottet H. S., KewalRamani V. N. other authors 2000; DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100:587–597 [CrossRef][PubMed]
    [Google Scholar]
  15. Groot F., Geijtenbeek T. B., Sanders R. W., Baldwin C. E., Sanchez-Hernandez M., Floris R., van Kooyk Y., de Jong E. C., Berkhout B. 2005; Lactoferrin prevents dendritic cell-mediated human immunodeficiency virus type 1 transmission by blocking the DC-SIGN–gp120 interaction. J Virol 79:3009–3015 [CrossRef][PubMed]
    [Google Scholar]
  16. Hong P., Ninonuevo M. R., Lee B., Lebrilla C., Bode L. 2009; Human milk oligosaccharides reduce HIV-1-gp120 binding to dendritic cell-specific ICAM3-grabbing non-integrin (DC-SIGN). Br J Nutr 101:482–486 [CrossRef][PubMed]
    [Google Scholar]
  17. Kwiek J. J., Arney L. A., Harawa V., Pedersen B., Mwapasa V., Rogerson S. J., Meshnick S. R. 2008; Maternal-fetal DNA admixture is associated with intrapartum mother-to-child transmission of HIV-1 in Blantyre, Malawi. J Infect Dis 197:1378–1381 [CrossRef][PubMed]
    [Google Scholar]
  18. Lancet 1991; Children born to women with HIV-1 infection: natural history and risk of transmission. European Collaborative Study. Lancet 337:253–260 [CrossRef][PubMed]
    [Google Scholar]
  19. Lehman D. A., Farquhar C. 2007; Biological mechanisms of vertical human immunodeficiency virus (HIV-1) transmission. Rev Med Virol 17:381–403 [CrossRef][PubMed]
    [Google Scholar]
  20. Martin A. W., Brady K., Smith S. I., DeCoste D., Page D. V., Malpica A., Wolf B., Neiman R. S. 1992; Immunohistochemical localization of human immunodeficiency virus p24 antigen in placental tissue. Hum Pathol 23:411–414 [CrossRef][PubMed]
    [Google Scholar]
  21. Martin M. P., Lederman M. M., Hutcheson H. B., Goedert J. J., Nelson G. W., van Kooyk Y., Detels R., Buchbinder S., Hoots K. other authors 2004; Association of DC-SIGN promoter polymorphism with increased risk for parenteral, but not mucosal, acquisition of human immunodeficiency virus type 1 infection. J Virol 78:14053–14056 [CrossRef][PubMed]
    [Google Scholar]
  22. Marzi A., Mitchell D. A., Chaipan C., Fisch T., Doms R. W., Carrington M., Desrosiers R. C., Pöhlmann S. 2007; Modulation of HIV and SIV neutralization sensitivity by DC-SIGN and mannose-binding lectin. Virology 368:322–330 [CrossRef][PubMed]
    [Google Scholar]
  23. Mild M., Esbjörnsson J., Fenyö E. M., Medstrand P. 2007; Frequent intrapatient recombination between human immunodeficiency virus type 1 R5 and X4 envelopes: implications for coreceptor switch. J Virol 81:3369–3376 [CrossRef][PubMed]
    [Google Scholar]
  24. Moussa M., Mognetti B., Dubanchet S., Menu E., Roques P., Gras G., Dormont D., Barre-Sinoussi F., Chaouat G. 1999; Vertical transmission of HIV: parameters which might affect infection of placental trophoblasts by HIV-1: a review. Am J Reprod Immunol 41:312–319 [CrossRef][PubMed]
    [Google Scholar]
  25. Naarding M. A., Ludwig I. S., Groot F., Berkhout B., Geijtenbeek T. B., Pollakis G., Paxton W. A. 2005; Lewis X component in human milk binds DC-SIGN and inhibits HIV-1 transfer to CD4+ T lymphocytes. J Clin Invest 115:3256–3264 [CrossRef][PubMed]
    [Google Scholar]
  26. Naarding M. A., Dirac A. M., Ludwig I. S., Speijer D., Lindquist S., Vestman E. L., Stax M. J., Geijtenbeek T. B., Pollakis G. other authors 2006; Bile salt-stimulated lipase from human milk binds DC-SIGN and inhibits human immunodeficiency virus type 1 transfer to CD4+ T cells. Antimicrob Agents Chemother 50:3367–3374 [CrossRef][PubMed]
    [Google Scholar]
  27. Nabatov A. A., van Montfort T., Geijtenbeek T. B., Pollakis G., Paxton W. A. 2006; Interaction of HIV-1 with dendritic cell-specific intercellular adhesion molecule-3-grabbing non-integrin-expressing cells is influenced by gp120 envelope modifications associated with disease progression. FEBS J 273:4944–4958 [CrossRef][PubMed]
    [Google Scholar]
  28. Navér L., Ehrnst A., Belfrage E., Sönnerborg A., Lidin-Janson G., Christensson B., Ljung R., Bohlin A. B. 1999; Long-term pattern of HIV-1 RNA load in perinatally infected children. Scand J Infect Dis 31:337–343 [CrossRef][PubMed]
    [Google Scholar]
  29. Patterson S., Knight S. C. 1987; Susceptibility of human peripheral blood dendritic cells to infection by human immunodeficiency virus. J Gen Virol 68:1177–1181 [CrossRef][PubMed]
    [Google Scholar]
  30. Pöhlmann S., Baribaud F., Lee B., Leslie G. J., Sanchez M. D., Hiebenthal-Millow K., Münch J., Kirchhoff F., Doms R. W. 2001a; DC-SIGN interactions with human immunodeficiency virus type 1 and 2 and simian immunodeficiency virus. J Virol 75:4664–4672 [CrossRef][PubMed]
    [Google Scholar]
  31. Pöhlmann S., Soilleux E. J., Baribaud F., Leslie G. J., Morris L. S., Trowsdale J., Lee B., Coleman N., Doms R. W. 2001b; DC-SIGNR, a DC-SIGN homologue expressed in endothelial cells, binds to human and simian immunodeficiency viruses and activates infection in trans . Proc Natl Acad Sci U S A 98:2670–2675 [CrossRef][PubMed]
    [Google Scholar]
  32. Rappersberger K., Gartner S., Schenk P., Stingl G., Groh V., Tschachler E., Mann D. L., Wolff K., Konrad K., Popovic M. 1988; Langerhans’ cells are an actual site of HIV-1 replication. Intervirology 29:185–194[PubMed]
    [Google Scholar]
  33. Requena M., Bouhlal H., Nasreddine N., Saidi H., Gody J. C., Aubry S., Grésenguet G., Kazatchkine M. D., Sekaly R. P. other authors 2008; Inhibition of HIV-1 transmission in trans from dendritic cells to CD4+ T lymphocytes by natural antibodies to the CRD domain of DC-SIGN purified from breast milk and intravenous immunoglobulins. Immunology 123:508–518 [CrossRef][PubMed]
    [Google Scholar]
  34. Saeland E., de Jong M. A., Nabatov A. A., Kalay H., Geijtenbeek T. B., van Kooyk Y. 2009; MUC1 in human milk blocks transmission of human immunodeficiency virus from dendritic cells to T cells. Mol Immunol 46:2309–2316 [CrossRef][PubMed]
    [Google Scholar]
  35. 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]
  36. Sheikh A. U., Polliotti B. M., Miller R. K. 2000; Human immunodeficiency virus infection: in situ polymerase chain reaction localization in human placentas after in utero and in vitro infection. Am J Obstet Gynecol 182:207–213 [CrossRef][PubMed]
    [Google Scholar]
  37. Shen R., Smythies L. E., Clements R. H., Novak L., Smith P. D. 2010; Dendritic cells transmit HIV-1 through human small intestinal mucosa. J Leukoc Biol 87:663–670 [CrossRef][PubMed]
    [Google Scholar]
  38. Snyder G. A., Ford J., Torabi-Parizi P., Arthos J. A., Schuck P., Colonna M., Sun P. D. 2005; Characterization of DC-SIGN/R interaction with human immunodeficiency virus type 1 gp120 and ICAM molecules favors the receptor’s role as an antigen-capturing rather than an adhesion receptor. J Virol 79:4589–4598 [CrossRef][PubMed]
    [Google Scholar]
  39. Soilleux E. J., Coleman N. 2003; Transplacental transmission of HIV: a potential role for HIV binding lectins. Int J Biochem Cell Biol 35:283–287 [CrossRef][PubMed]
    [Google Scholar]
  40. Soilleux E. J., Morris L. S., Lee B., Pöhlmann S., Trowsdale J., Doms R. W., Coleman N. 2001; Placental expression of DC-SIGN may mediate intrauterine vertical transmission of HIV. J Pathol 195:586–592 [CrossRef][PubMed]
    [Google Scholar]
  41. Steinman R. M., Granelli-Piperno A., Pope M., Trumpfheller C., Ignatius R., Arrode G., Racz P., Tenner-Racz K. 2003; The interaction of immunodeficiency viruses with dendritic cells. Curr Top Microbiol Immunol 276:1–30[PubMed]
    [Google Scholar]
  42. Trouplin V., Salvatori F., Cappello F., Obry V., Brelot A., Heveker N., Alizon M., Scarlatti G., Clavel F., Mammano F. 2001; Determination of coreceptor usage of human immunodeficiency virus type 1 from patient plasma samples by using a recombinant phenotypic assay. J Virol 75:251–259 [CrossRef][PubMed]
    [Google Scholar]
  43. Tsegaye T. S., Pöhlmann S. 2010; The multiple facets of HIV attachment to dendritic cell lectins. Cell Microbiol 12:1553–1561 [CrossRef][PubMed]
    [Google Scholar]
  44. Turville S. G., Cameron P. U., Handley A., Lin G., Pöhlmann S., Doms R. W., Cunningham A. L. 2002; Diversity of receptors binding HIV on dendritic cell subsets. Nat Immunol 3:975–983 [CrossRef][PubMed]
    [Google Scholar]
  45. Turville S. G., Santos J. J., Frank I., Cameron P. U., Wilkinson J., Miranda-Saksena M., Dable J., Stössel H., Romani N. other authors 2004; Immunodeficiency virus uptake, turnover, and 2-phase transfer in human dendritic cells. Blood 103:2170–2179 [CrossRef][PubMed]
    [Google Scholar]
  46. van Montfort T., Nabatov A. A., Geijtenbeek T. B., Pollakis G., Paxton W. A. 2007; Efficient capture of antibody neutralized HIV-1 by cells expressing DC-SIGN and transfer to CD4+ T lymphocytes. J Immunol 178:3177–3185[PubMed] [CrossRef]
    [Google Scholar]
  47. 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]
  48. Wu L., KewalRamani V. N. 2006; Dendritic-cell interactions with HIV: infection and viral dissemination. Nat Rev Immunol 6:859–868 [CrossRef][PubMed]
    [Google Scholar]
  49. Wu L., Martin T. D., Carrington M., KewalRamani V. N. 2004; Raji B cells, misidentified as THP-1 cells, stimulate DC-SIGN-mediated HIV transmission. Virology 318:17–23 [CrossRef][PubMed]
    [Google Scholar]
  50. Yagi Y., Watanabe E., Watari E., Shinya E., Satomi M., Takeshita T., Takahashi H. 2010; Inhibition of DC-SIGN-mediated transmission of human immunodeficiency virus type 1 by Toll-like receptor 3 signalling in breast milk macrophages. Immunology 130:597–607 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.043620-0
Loading
/content/journal/jgv/10.1099/vir.0.043620-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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