HIV-1 infection ex vivo accelerates measles virus infection by upregulating signaling lymphocytic activation molecule (SLAM) in CD4+ T Cells

Yu Ya Mitsuki, Kazutaka Terahara, Kentaro Shibusawa, Takuya Yamamoto, Takatsugu Tsuchiya, Fuminori Mizukoshi, Masayuki Ishige, Seiji Okada, Kazuo Kobayashi, Yuko Morikawa, Tetsuo Nakayama, Makoto Takeda, Yusuke Yanagi, Yasuko Tsunetsugu-Yokota

Research output: Contribution to journalArticle

Abstract

Measles virus (MV) infection in children harboring human immunodeficiency virus type 1 (HIV-1) is often fatal, even in the presence of neutralizing antibodies; however, the underlying mechanisms are unclear. Therefore, the aim of the present study was to examine the interaction between HIV-1 and wild-type MV (MVwt) or an MV vaccine strain (MVvac) during dual infection. The results showed that the frequencies of MVwt- and MVvac-infected CD4+ T cells within the resting peripheral blood mononuclear cells (PBMCs) were increased 3- to 4-fold after HIV-1 infection, and this was associated with a marked upregulation of signaling lymphocytic activation molecule (SLAM) expression on CD4+ T cells but not on CD8+ T cells. SLAM upregulation was induced by infection with a replication-competent HIV-1 isolate comprising both the X4 and R5 types and to a lesser extent by a pseudotyped HIV-1 infection. Notably, SLAM upregulation was observed in HIV-infected as well as -uninfected CD4+ T cells and was abrogated by the removal of HLA-DR+ cells from the PBMC culture. Furthermore, SLAM upregulation did not occur in uninfected PBMCs cultured together with HIV-infected PBMCs in compartments separated by a permeable membrane, indicating that no soluble factors were involved. Rather, CD4+ T cell activation mediated through direct contact with dendritic cells via leukocyte function-associated molecule 1 (LFA-1)/intercellular adhesion molecule 1 (ICAM-1) and LFA-3/CD2 was critical. Thus, HIV-1 infection induces a high level of SLAM expression on CD4+ T cells, which may enhance their susceptibility to MV and exacerbate measles in coinfected individuals.

Original languageEnglish
Pages (from-to)7227-7234
Number of pages8
JournalJournal of virology
Volume86
Issue number13
DOIs
Publication statusPublished - Jul 1 2012

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Measles virus
Virus Diseases
Human immunodeficiency virus 1
HIV-1
T-lymphocytes
mononuclear leukocytes
T-Lymphocytes
Blood Cells
Up-Regulation
infection
CD58 Antigens
HIV
vaccines
Measles Vaccine
Measles
HLA-DR Antigens
Intercellular Adhesion Molecule-1
dendritic cells
direct contact
Infection

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Immunology
  • Insect Science
  • Virology

Cite this

Mitsuki, Y. Y., Terahara, K., Shibusawa, K., Yamamoto, T., Tsuchiya, T., Mizukoshi, F., ... Tsunetsugu-Yokota, Y. (2012). HIV-1 infection ex vivo accelerates measles virus infection by upregulating signaling lymphocytic activation molecule (SLAM) in CD4+ T Cells. Journal of virology, 86(13), 7227-7234. https://doi.org/10.1128/JVI.06681-11

HIV-1 infection ex vivo accelerates measles virus infection by upregulating signaling lymphocytic activation molecule (SLAM) in CD4+ T Cells. / Mitsuki, Yu Ya; Terahara, Kazutaka; Shibusawa, Kentaro; Yamamoto, Takuya; Tsuchiya, Takatsugu; Mizukoshi, Fuminori; Ishige, Masayuki; Okada, Seiji; Kobayashi, Kazuo; Morikawa, Yuko; Nakayama, Tetsuo; Takeda, Makoto; Yanagi, Yusuke; Tsunetsugu-Yokota, Yasuko.

In: Journal of virology, Vol. 86, No. 13, 01.07.2012, p. 7227-7234.

Research output: Contribution to journalArticle

Mitsuki, YY, Terahara, K, Shibusawa, K, Yamamoto, T, Tsuchiya, T, Mizukoshi, F, Ishige, M, Okada, S, Kobayashi, K, Morikawa, Y, Nakayama, T, Takeda, M, Yanagi, Y & Tsunetsugu-Yokota, Y 2012, 'HIV-1 infection ex vivo accelerates measles virus infection by upregulating signaling lymphocytic activation molecule (SLAM) in CD4+ T Cells', Journal of virology, vol. 86, no. 13, pp. 7227-7234. https://doi.org/10.1128/JVI.06681-11
Mitsuki, Yu Ya ; Terahara, Kazutaka ; Shibusawa, Kentaro ; Yamamoto, Takuya ; Tsuchiya, Takatsugu ; Mizukoshi, Fuminori ; Ishige, Masayuki ; Okada, Seiji ; Kobayashi, Kazuo ; Morikawa, Yuko ; Nakayama, Tetsuo ; Takeda, Makoto ; Yanagi, Yusuke ; Tsunetsugu-Yokota, Yasuko. / HIV-1 infection ex vivo accelerates measles virus infection by upregulating signaling lymphocytic activation molecule (SLAM) in CD4+ T Cells. In: Journal of virology. 2012 ; Vol. 86, No. 13. pp. 7227-7234.
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abstract = "Measles virus (MV) infection in children harboring human immunodeficiency virus type 1 (HIV-1) is often fatal, even in the presence of neutralizing antibodies; however, the underlying mechanisms are unclear. Therefore, the aim of the present study was to examine the interaction between HIV-1 and wild-type MV (MVwt) or an MV vaccine strain (MVvac) during dual infection. The results showed that the frequencies of MVwt- and MVvac-infected CD4+ T cells within the resting peripheral blood mononuclear cells (PBMCs) were increased 3- to 4-fold after HIV-1 infection, and this was associated with a marked upregulation of signaling lymphocytic activation molecule (SLAM) expression on CD4+ T cells but not on CD8+ T cells. SLAM upregulation was induced by infection with a replication-competent HIV-1 isolate comprising both the X4 and R5 types and to a lesser extent by a pseudotyped HIV-1 infection. Notably, SLAM upregulation was observed in HIV-infected as well as -uninfected CD4+ T cells and was abrogated by the removal of HLA-DR+ cells from the PBMC culture. Furthermore, SLAM upregulation did not occur in uninfected PBMCs cultured together with HIV-infected PBMCs in compartments separated by a permeable membrane, indicating that no soluble factors were involved. Rather, CD4+ T cell activation mediated through direct contact with dendritic cells via leukocyte function-associated molecule 1 (LFA-1)/intercellular adhesion molecule 1 (ICAM-1) and LFA-3/CD2 was critical. Thus, HIV-1 infection induces a high level of SLAM expression on CD4+ T cells, which may enhance their susceptibility to MV and exacerbate measles in coinfected individuals.",
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