1887

Abstract

Acute measles virus (MV) infection results in a decrease in plasma human immunodeficiency virus type 1 (HIV-1) RNA levels in co-infected children. An peripheral blood mononuclear cell (PBMC) culture system was used to assess the mechanisms by which MV blocks HIV-1 replication. MV inhibited proliferation of CD4 T lymphocytes, the target cell for HIV-1 replication. In the presence of MV, cells did not progress to G and S phases, steps critical for the completion of HIV-1 reverse transcription and productive replication. This block in cell-cycle progression was characterized by an increased proportion of CD4 and HIV-1-infected cells retained in the parental generation in PBMCs co-cultured with MV and HIV-1, and decreased levels of cyclins and RNA synthesis. Early HIV-1 replication was also inhibited in the presence of MV, as measured by reduced expression of a luciferase reporter gene and lower levels of both early (LTR) and late (LTR–gag) DNA intermediates of HIV-1 reverse transcription in the presence of CCR5-tropic HIV-1. The effects of MV on lymphoproliferation and p24 antigen production were reproduced by -butyrate and hydroxyurea, drugs that block the cell cycle in G and G/S, respectively. It was concluded that MV inhibits HIV-1 productive replication in part by blocking the proliferation of CD4 T lymphocytes.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.83601-0
2008-04-01
2021-04-10
Loading full text...

Full text loading...

/deliver/fulltext/jgv/89/4/984.html?itemId=/content/journal/jgv/10.1099/vir.0.83601-0&mimeType=html&fmt=ahah

References

  1. Berger E. A., Murphy P. M., Farber J. M. 1999; Chemokine receptors as HIV-1 coreceptors: roles in viral entry, tropism, and disease. Annu Rev Immunol 17:657–700 [CrossRef]
    [Google Scholar]
  2. Bradford M. M. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254 [CrossRef]
    [Google Scholar]
  3. Clark E., Santiago F., Deng L., Chong S., de la Fuente C., Wang L., Fu P., Stein D., Denny T. other authors 2000; Loss of G1/S checkpoint in human immunodeficiency virus type 1-infected cells is associated with a lack of cyclin-dependent kinase inhibitor p21/Waf1. J Virol 74:5040–5052 [CrossRef]
    [Google Scholar]
  4. Darzynkiewicz Z., Sharpless T., Staiano-Coico L., Melamed M. R. 1980; Subcompartments of the G1 phase of cell cycle detected by flow cytometry. Proc Natl Acad Sci U S A 77:6696–6699 [CrossRef]
    [Google Scholar]
  5. Darzynkiewicz Z., Traganos F., Xue S. B., Melamed M. R. 1981; Effect of n-butyrate on cell cycle progression and in situ chromatin structure of L1210 cells. Exp Cell Res 136:279–293 [CrossRef]
    [Google Scholar]
  6. Derdeyn C. A., Decker J. M., Sfakianos J. N., Wu X., O'Brien W. A., Ratner L., Kappes J. C., Shaw G. M., Hunter E. 2000; Sensitivity of human immunodeficiency virus type 1 to the fusion inhibitor T-20 is modulated by coreceptor specificity defined by the V3 loop of gp120. J Virol 74:8358–8367 [CrossRef]
    [Google Scholar]
  7. Enders J. F., Peebles T. C. 1954; Propagation in tissue cultures of cytopathic agents from patients with measles. Proc Soc Exp Biol Med 86:277–286 [CrossRef]
    [Google Scholar]
  8. Engelking O., Fedorov L. M., Lilischkis R., ter Meulen V., Schneider-Schaulies S. 1999; Measles virus-induced immunosuppression in vitro is associated with deregulation of G1 cell cycle control proteins. J Gen Virol 80:1599–1608
    [Google Scholar]
  9. Furuya Y., Lundmo P., Short A. D., Gill D. L., Isaacs J. T. 1994; The role of calcium, pH, and cell proliferation in the programmed (apoptotic) death of androgen-independent prostatic cancer cells induced by thapsigargin. Cancer Res 54:6167–6175
    [Google Scholar]
  10. Garcia M., Yu X. F., Griffin D. E., Moss W. J. 2005; In vitro suppression of human immunodeficiency virus type 1 replication by measles virus. J Virol 79:9197–9205 [CrossRef]
    [Google Scholar]
  11. Grivel J. C., Garcia M., Moss W. J., Margolis L. B. 2005; Inhibition of HIV-1 replication in human lymphoid tissues ex vivo by measles virus. J Infect Dis 192:71–78 [CrossRef]
    [Google Scholar]
  12. Heaney J., Barrett T., Cosby S. L. 2002; Inhibition of in vitro leukocyte proliferation by morbilliviruses. J Virol 76:3579–3584 [CrossRef]
    [Google Scholar]
  13. Hirsch R. L., Griffin D. E., Johnson R. T., Cooper S. J., , Lindo de Soriano I., Roedenbeck S., Vaisberg A. 1984; Cellular immune responses during complicated and uncomplicated measles virus infections of man. Clin Immunol Immunopathol 31:1–12 [CrossRef]
    [Google Scholar]
  14. Kannangara S., DeSimone J. A., Pomerantz R. J. 2005; Attenuation of HIV-1 infection by other microbial agents. J Infect Dis 192:1003–1009 [CrossRef]
    [Google Scholar]
  15. Kashanchi F., Agbottah E. T., Pise-Masison C. A., Mahieux R., Duvall J., Kumar A., Brady J. N. 2000; Cell cycle-regulated transcription by the human immunodeficiency virus type 1 Tat transactivator. J Virol 74:652–660 [CrossRef]
    [Google Scholar]
  16. Kilby J. M. 2001; Human immunodeficiency virus pathogenesis: insights from studies of lymphoid cells and tissues. Clin Infect Dis 33:873–884 [CrossRef]
    [Google Scholar]
  17. Kootstra N. A., Zwart B. M., Schuitemaker H. 2000; Diminished human immunodeficiency virus type 1 reverse transcription and nuclear transport in primary macrophages arrested in early G1 phase of the cell cycle. J Virol 74:1712–1717 [CrossRef]
    [Google Scholar]
  18. Korin Y. D., Zack J. A. 1998; Progression to the G1b phase of the cell cycle is required for completion of human immunodeficiency virus type 1 reverse transcription in T cells. J Virol 72:3161–3168
    [Google Scholar]
  19. Korin Y. D., Zack J. A. 1999; Nonproductive human immunodeficiency virus type 1 infection in nucleoside-treated G0 lymphocytes. J Virol 73:6526–6532
    [Google Scholar]
  20. Laine D., Bourhis J. M., Longhi S., Flacher M., Cassard L., Canard B., Sautes-Fridman C., Rabourdin-Combe C., Valentin H. 2005; Measles virus nucleoprotein induces cell-proliferation arrest and apoptosis through NTAIL-NR and NCORE-Fc γ RIIB1 interactions, respectively. J Gen Virol 86:1771–1784 [CrossRef]
    [Google Scholar]
  21. Li Y., Hui H., Burgess C. J., Price R. W., Sharp P. M., Hahn B. H., Shaw G. M. 1992; Complete nucleotide sequence, genome organization, and biological properties of human immunodeficiency virus type 1 in vivo: evidence for limited defectiveness and complementation. J Virol 66:6587–6600
    [Google Scholar]
  22. Lori F., Lisziewicz J. 2000; Rationale for the use of hydroxyurea as an anti-human immunodeficiency virus drug. Clin Infect Dis 30:Suppl. 2S193–S197 [CrossRef]
    [Google Scholar]
  23. Lori F., Malykh A., Cara A., Sun D., Weinstein J. N., Lisziewicz J., Gallo R. C. 1994; Hydroxyurea as an inhibitor of human immunodeficiency virus-type 1 replication. Science 266:801–805 [CrossRef]
    [Google Scholar]
  24. Maurer-Schultze B., Siebert M., Bassukas I. D. 1988; An in vivo study on the synchronizing effect of hydroxyurea. Exp Cell Res 174:230–243 [CrossRef]
    [Google Scholar]
  25. Moss W. J., Ryon J. J., Monze M., Cutts F., Quinn T. C., Griffin D. E. 2002; Suppression of human immunodeficiency virus replication during acute measles. J Infect Dis 185:1035–1042 [CrossRef]
    [Google Scholar]
  26. Naniche D., Reed S. I., Oldstone M. B. 1999; Cell cycle arrest during measles virus infection: a G0-like block leads to suppression of retinoblastoma protein expression. J Virol 73:1894–1901
    [Google Scholar]
  27. Niewiesk S., Ohnimus H., Schnorr J. J., Gotzelmann M., Schneider-Schaulies S., Jassoy C., ter Meulen V. 1999; Measles virus-induced immunosuppression in cotton rats is associated with cell cycle retardation in uninfected lymphocytes. J Gen Virol 80:2023–2029
    [Google Scholar]
  28. Ruel T. D., Achan J., Gasasira A. F., Charlebois E. D., Rosenthal P. J., Dorsey G., Kamya M. R., Kekitiinwa A., Wong J., Havlir D., The CHAMP Team. 2007; Dramatic reductions in HIV RNA among HIV-infected children with acute measles in Uganda (abstract 707. In 14th Conference on Retroviruses and Opportunistic Infections (CROI) Los Angeles: 25–28 February 2007
    [Google Scholar]
  29. Stacey D. W. 2003; Cyclin D1 serves as a cell cycle regulatory switch in actively proliferating cells. Curr Opin Cell Biol 15:158–163 [CrossRef]
    [Google Scholar]
  30. Stevenson M., Stanwick T. L., Dempsey M. P., Lamonica C. A. 1990; HIV-1 replication is controlled at the level of T cell activation and proviral integration. EMBO J 9:1551–1560
    [Google Scholar]
  31. Suzuki Y., Misawa N., Sato C., Ebina H., Masuda T., Yamamoto N., Koyanagi Y. 2003; Quantitative analysis of human immunodeficiency virus type 1 DNA dynamics by real-time PCR: integration efficiency in stimulated and unstimulated peripheral blood mononuclear cells. Virus Genes 27:177–188 [CrossRef]
    [Google Scholar]
  32. Toba K., Winton E. F., Koike T., Shibata A. 1995; Simultaneous three-color analysis of the surface phenotype and DNA-RNA quantitation using 7-amino-actinomycin D and pyronin Y. J Immunol Methods 182:193–207 [CrossRef]
    [Google Scholar]
  33. Ward B. J., Johnson R. T., Vaisberg A., Jauregui E., Griffin D. E. 1991; Cytokine production in vitro and the lymphoproliferative defect of natural measles virus infection. Clin Immunol Immunopathol 61:236–248 [CrossRef]
    [Google Scholar]
  34. Watt G., Kantipong P., de Souza M., Chanbancherd P., Jongsakul K., Ruangweerayud R., Loomis-Price L. D., Polonis V., Myint K. S. other authors 2000; HIV-1 suppression during acute scrub-typhus infection. Lancet 356:475–479 [CrossRef]
    [Google Scholar]
  35. Watt G., Kantipong P., Jongsakul K. 2003; Decrease in human immunodeficiency virus type 1 load during acute dengue fever. Clin Infect Dis 36:1067–1069 [CrossRef]
    [Google Scholar]
  36. Weidmann A., Maisner A., Garten W., Seufert M., ter Meulen V., Schneider-Schaulies S. 2000; Proteolytic cleavage of the fusion protein but not membrane fusion is required for measles virus-induced immunosuppression in vitro. J Virol 74:1985–1993 [CrossRef]
    [Google Scholar]
  37. Williams C. F., Klinzman D., Yamashita T. E., Xiang J., Polgreen P. M., Rinaldo C., Liu C., Phair J., Margolick J. B. other authors 2004; Persistent GB virus C infection and survival in HIV-infected men. N Engl J Med 350:981–990 [CrossRef]
    [Google Scholar]
  38. World Health Organization 2001; Nomenclature for describing the genetic characteristics of wild-type measles viruses (update). Part I. Wkly Epidemiol Rec 76:242–247
    [Google Scholar]
  39. Yamanouchi K., Chino F., Kobune F., Kodama H., Tsuruhara T. 1973; Growth of measles virus in the lymphoid tissues of monkeys. J Infect Dis 128:795–799 [CrossRef]
    [Google Scholar]
  40. Yoshizuka N., Yoshizuka-Chadani Y., Krishnan V., Zeichner S. L. 2005; Human immunodeficiency virus type 1 Vpr-dependent cell cycle arrest through a mitogen-activated protein kinase signal transduction pathway. J Virol 79:11366–11381 [CrossRef]
    [Google Scholar]
  41. Zack J. A. 1995; The role of the cell cycle in HIV-1 infection. Adv Exp Med Biol 374:27–31
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.83601-0
Loading
/content/journal/jgv/10.1099/vir.0.83601-0
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