Tax-inducible production of CC chemokine ligand 22 by human T cell leukemia virus type 1 (HTLV-1)-infected T cells promotes preferential transmission of HTLV-1 to CCR4-expressing CD4+ T cells

J Immunol. 2008 Jan 15;180(2):931-9. doi: 10.4049/jimmunol.180.2.931.

Abstract

Adult T cell leukemia is a mature CD4+ T cell malignancy which predominantly expresses CCR4 and is etiologically associated with human T cell leukemia virus type 1 (HTLV-1). Because HTLV-1 transmission depends on close cell-cell contacts, HTLV-1-infected T cells may preferentially interact with CCR4+CD4+ T cells for efficient viral transmission. In terms of gene expression and protein secretion, we found a strong correlation between HTLV-1 Tax oncoprotein and CCL22, a CCR4 ligand, in HTLV-1-infected T cells. Transient Tax expression in an HTLV-1-negative T cell line activated the CCL22 promoter and induced CCL22. Additionally, tax gene knockdown by small interference RNA reduced CCL22 expression in the infected T cells. These findings indicate that CCL22 is a cellular target gene of Tax. In chemotaxis assays, the culture supernatants of HTLV-1-infected T cells selectively attracted CCR4+CD4+ T cells in PBMCs. This was blocked by pretreating the supernatants with anti-CCL22 Ab or PBMCs with a synthetic CCR4 antagonist. In coculture experiments, primary CCR4+CD4+ T cells significantly adhered to Tax-expressing cells. This adhesion was blocked by the CCR4 antagonist or pertussis toxin. Interestingly, CCR4 was redistributed to the contact region, and in some cases, this was accompanied by a polarized microtubule-organizing center, which is an indicator of virological synapse formation, in the infected T cells. Finally, anti-CCL22 Ab treatment also blocked HTLV-1 transmission to primary CD4+ T cells in coculture experiments with HTLV-1 producer cells. Thus, HTLV-1-infected T cells produce CCL22 through Tax and selectively interact with CCR4+CD4+ T cells, resulting in preferential transmission of HTLV-1 to CCR4+CD4+ T cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • CD4-Positive T-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / virology*
  • Cell Adhesion / drug effects
  • Cell Adhesion / genetics
  • Cell Line
  • Chemokine CCL22 / antagonists & inhibitors
  • Chemokine CCL22 / genetics*
  • Chemokine CCL22 / metabolism
  • Gene Expression Regulation, Viral*
  • Gene Products, tax / antagonists & inhibitors
  • Gene Products, tax / genetics
  • Gene Products, tax / metabolism*
  • Human T-lymphotropic virus 1 / genetics
  • Human T-lymphotropic virus 1 / metabolism
  • Human T-lymphotropic virus 1 / physiology*
  • Humans
  • Pertussis Toxin / pharmacology
  • RNA, Messenger / metabolism
  • RNA, Small Interfering / pharmacology
  • Receptors, CCR4 / antagonists & inhibitors
  • Receptors, CCR4 / metabolism
  • T-Lymphocytes / immunology
  • T-Lymphocytes / virology
  • Virus Internalization*

Substances

  • CCL22 protein, human
  • CCR4 protein, human
  • Chemokine CCL22
  • Gene Products, tax
  • RNA, Messenger
  • RNA, Small Interfering
  • Receptors, CCR4
  • Pertussis Toxin