Skip to main content
Journal of Virology logoLink to Journal of Virology
. 1994 May;68(5):2898–2905. doi: 10.1128/jvi.68.5.2898-2905.1994

Role of the cytoskeleton in cell-to-cell transmission of human immunodeficiency virus.

R Pearce-Pratt 1, D Malamud 1, D M Phillips 1
PMCID: PMC236778  PMID: 8151760

Abstract

We previously observed that when human immunodeficiency virus (HIV)-infected T lymphocytes are added to epithelial cells, they adhere, polarize, and secrete virions unidirectionally onto the epithelium. Epithelial cells subsequently take up virus and become productively infected. We report here that colchicine treatment of T-lymphocyte suspensions induced lymphocyte polarization, redistribution of F-actin into a pseudopod, and secretion of HIV from the pseudopod. Immobilization of T lymphocytes on negatively charged plastic also caused redistribution of F-actin and unidirectional secretion of HIV onto the plastic. As neither colchicine nor adhesion caused an increase in HIV secretion, they apparently act by focusing secretion to the tip of the pseudopod. We speculate that adhesion-induced polar secretion of HIV, from activated mononuclear cells onto epithelia, is a cytoskeleton-mediated process which may be involved in HIV transmission in vivo.

Full text

PDF
2898

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson D. J., O'Brien T. R., Politch J. A., Martinez A., Seage G. R., 3rd, Padian N., Horsburgh C. R., Jr, Mayer K. H. Effects of disease stage and zidovudine therapy on the detection of human immunodeficiency virus type 1 in semen. JAMA. 1992 May 27;267(20):2769–2774. [PubMed] [Google Scholar]
  2. Barnett S. W., Barboza A., Wilcox C. M., Forsmark C. E., Levy J. A. Characterization of human immunodeficiency virus type 1 strains recovered from the bowel of infected individuals. Virology. 1991 Jun;182(2):802–809. doi: 10.1016/0042-6822(91)90621-h. [DOI] [PubMed] [Google Scholar]
  3. Barré-Sinoussi F., Chermann J. C., Rey F., Nugeyre M. T., Chamaret S., Gruest J., Dauguet C., Axler-Blin C., Vézinet-Brun F., Rouzioux C. Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science. 1983 May 20;220(4599):868–871. doi: 10.1126/science.6189183. [DOI] [PubMed] [Google Scholar]
  4. Bourinbaiar A. S., Phillips D. M. Transmission of human immunodeficiency virus from monocytes to epithelia. J Acquir Immune Defic Syndr. 1991;4(1):56–63. [PubMed] [Google Scholar]
  5. Carpén O., Virtanen I., Lehto V. P., Saksela E. Polarization of NK cell cytoskeleton upon conjugation with sensitive target cells. J Immunol. 1983 Dec;131(6):2695–2698. [PubMed] [Google Scholar]
  6. Coates T. D., Watts R. G., Hartman R., Howard T. H. Relationship of F-actin distribution to development of polar shape in human polymorphonuclear neutrophils. J Cell Biol. 1992 May;117(4):765–774. doi: 10.1083/jcb.117.4.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dougherty G. J., Murdoch S., Hogg N. The function of human intercellular adhesion molecule-1 (ICAM-1) in the generation of an immune response. Eur J Immunol. 1988 Jan;18(1):35–39. doi: 10.1002/eji.1830180107. [DOI] [PubMed] [Google Scholar]
  8. Dustin M. L., Carpen O., Springer T. A. Regulation of locomotion and cell-cell contact area by the LFA-1 and ICAM-1 adhesion receptors. J Immunol. 1992 May 1;148(9):2654–2663. [PubMed] [Google Scholar]
  9. Fantini J., Baghdiguian S., Yahi N., Chermann J. C. Selected human immunodeficiency virus replicates preferentially through the basolateral surface of differentiated human colon epithelial cells. Virology. 1991 Dec;185(2):904–907. doi: 10.1016/0042-6822(91)90570-2. [DOI] [PubMed] [Google Scholar]
  10. Gallo R. C., Salahuddin S. Z., Popovic M., Shearer G. M., Kaplan M., Haynes B. F., Palker T. J., Redfield R., Oleske J., Safai B. Frequent detection and isolation of cytopathic retroviruses (HTLV-III) from patients with AIDS and at risk for AIDS. Science. 1984 May 4;224(4648):500–503. doi: 10.1126/science.6200936. [DOI] [PubMed] [Google Scholar]
  11. Heise C., Dandekar S., Kumar P., Duplantier R., Donovan R. M., Halsted C. H. Human immunodeficiency virus infection of enterocytes and mononuclear cells in human jejunal mucosa. Gastroenterology. 1991 Jun;100(6):1521–1527. doi: 10.1016/0016-5085(91)90648-5. [DOI] [PubMed] [Google Scholar]
  12. Ho D. D., Schooley R. T., Rota T. R., Kaplan J. C., Flynn T., Salahuddin S. Z., Gonda M. A., Hirsch M. S. HTLV-III in the semen and blood of a healthy homosexual man. Science. 1984 Oct 26;226(4673):451–453. doi: 10.1126/science.6208608. [DOI] [PubMed] [Google Scholar]
  13. Howard T. H., Oresajo C. O. The kinetics of chemotactic peptide-induced change in F-actin content, F-actin distribution, and the shape of neutrophils. J Cell Biol. 1985 Sep;101(3):1078–1085. doi: 10.1083/jcb.101.3.1078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Levy J. A., Hoffman A. D., Kramer S. M., Landis J. A., Shimabukuro J. M., Oshiro L. S. Isolation of lymphocytopathic retroviruses from San Francisco patients with AIDS. Science. 1984 Aug 24;225(4664):840–842. doi: 10.1126/science.6206563. [DOI] [PubMed] [Google Scholar]
  15. Levy J. A., Margaretten W., Nelson J. Detection of HIV in enterochromaffin cells in the rectal mucosa of an AIDS patient. Am J Gastroenterol. 1989 Jul;84(7):787–789. [PubMed] [Google Scholar]
  16. Levy J. A. The transmission of AIDS: the case of the infected cell. JAMA. 1988 May 27;259(20):3037–3038. [PubMed] [Google Scholar]
  17. Mathijs J. M., Hing M., Grierson J., Dwyer D. E., Goldschmidt C., Cooper D. A., Cunningham A. L. HIV infection of rectal mucosa. Lancet. 1988 May 14;1(8594):1111–1111. doi: 10.1016/s0140-6736(88)91932-0. [DOI] [PubMed] [Google Scholar]
  18. Nelson J. A., Wiley C. A., Reynolds-Kohler C., Reese C. E., Margaretten W., Levy J. A. Human immunodeficiency virus detected in bowel epithelium from patients with gastrointestinal symptoms. Lancet. 1988 Feb 6;1(8580):259–262. doi: 10.1016/s0140-6736(88)90348-0. [DOI] [PubMed] [Google Scholar]
  19. Parrott D. M., Wilkinson P. C. Lymphocyte locomotion and migration. Prog Allergy. 1981;28:193–284. [PubMed] [Google Scholar]
  20. Pearce-Pratt R., Phillips D. M. Studies of adhesion of lymphocytic cells: implications for sexual transmission of human immunodeficiency virus. Biol Reprod. 1993 Mar;48(3):431–445. doi: 10.1095/biolreprod48.3.431. [DOI] [PubMed] [Google Scholar]
  21. Phillips D. M., Bourinbaiar A. S. Mechanism of HIV spread from lymphocytes to epithelia. Virology. 1992 Jan;186(1):261–273. doi: 10.1016/0042-6822(92)90080-9. [DOI] [PubMed] [Google Scholar]
  22. Phillips D. M., Pearce-Pratt R., Tan X., Zacharopoulos V. R. Association of mycoplasma with HIV-1 and HTLV-I in human T lymphocytes. AIDS Res Hum Retroviruses. 1992 Nov;8(11):1863–1868. doi: 10.1089/aid.1992.8.1863. [DOI] [PubMed] [Google Scholar]
  23. Rothstein T. L., Mage M., Jones G., McHugh L. L. Cytotoxic T lymphocyte sequential killing of immobilized allogeneic tumor target cells measured by time-lapse microcinematography. J Immunol. 1978 Nov;121(5):1652–1656. [PubMed] [Google Scholar]
  24. Ryser J. E., Rungger-Brändle E., Chaponnier C., Gabbiani G., Vassalli P. The area of attachment of cytotoxic T lymphocytes to their target cells shows high motility and polarization of actin, but not myosin. J Immunol. 1982 Mar;128(3):1159–1162. [PubMed] [Google Scholar]
  25. Tan X., Pearce-Pratt R., Phillips D. M. Productive infection of a cervical epithelial cell line with human immunodeficiency virus: implications for sexual transmission. J Virol. 1993 Nov;67(11):6447–6452. doi: 10.1128/jvi.67.11.6447-6452.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Vogt M. W., Witt D. J., Craven D. E., Byington R., Crawford D. F., Schooley R. T., Hirsch M. S. Isolation of HTLV-III/LAV from cervical secretions of women at risk for AIDS. Lancet. 1986 Mar 8;1(8480):525–527. doi: 10.1016/s0140-6736(86)90884-6. [DOI] [PubMed] [Google Scholar]
  27. Wallace P. J., Wersto R. P., Packman C. H., Lichtman M. A. Chemotactic peptide-induced changes in neutrophil actin conformation. J Cell Biol. 1984 Sep;99(3):1060–1065. doi: 10.1083/jcb.99.3.1060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wilkinson P. C., Higgins A. OKT3-activated locomotion of human blood lymphocytes: a phenomenon requiring contact of T cells with Fc receptor-bearing cells. Immunology. 1987 Mar;60(3):445–451. [PMC free article] [PubMed] [Google Scholar]
  29. Wofsy C. B., Cohen J. B., Hauer L. B., Padian N. S., Michaelis B. A., Evans L. A., Levy J. A. Isolation of AIDS-associated retrovirus from genital secretions of women with antibodies to the virus. Lancet. 1986 Mar 8;1(8480):527–529. doi: 10.1016/s0140-6736(86)90885-8. [DOI] [PubMed] [Google Scholar]
  30. Yahi N., Baghdiguian S., Bolmont C., Fantini J. Replication and apical budding of HIV-1 in mucous-secreting colonic epithelial cells. J Acquir Immune Defic Syndr. 1992 Oct;5(10):993–1000. [PubMed] [Google Scholar]
  31. Zagury D., Bernard J., Leibowitch J., Safai B., Groopman J. E., Feldman M., Sarngadharan M. G., Gallo R. C. HTLV-III in cells cultured from semen of two patients with AIDS. Science. 1984 Oct 26;226(4673):449–451. doi: 10.1126/science.6208607. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES