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The Tax-Inducible Actin-Bundling Protein Fascin Is Crucial for Release and Cell-to-Cell Transmission of Human T-Cell Leukemia Virus Type 1 (HTLV-1)

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Gross, Christine, Wiesmann, Veit, Millen, Sebastian, Kalmer, Martina, Wittenberg, Thomas, Gettemans, Jan, Thoma-Kress, Andrea K.·2016·PLOS Pathogens
DOI 10.1371/journal.ppat.1005916PMC PMC5077169
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Abstract

The delta-retrovirus Human T-cell leukemia virus type 1 (HTLV-1) preferentially infects CD4+ T-cells via cell-to-cell transmission. Viruses are transmitted by polarized budding and by transfer of viral biofilms at the virological synapse (VS). Formation of the VS requires the viral Tax protein and polarization of the host cytoskeleton, however, molecular mechanisms of HTLV-1 cell-to-cell transmission remain incompletely understood. Recently, we could show Tax-dependent upregulation of the actin-bundling protein Fascin (FSCN-1) in HTLV-1-infected T-cells. Here, we report that Fascin contributes to HTLV-1 transmission. Using single-cycle replication-dependent HTLV-1 reporter vectors, we found that repression of endogenous Fascin by short hairpin RNAs and by Fascin-specific nanobodies impaired gag p19 release and cell-to-cell transmission in 293T cells. In Jurkat T-cells, Tax-induced Fascin expression enhanced virus release and Fascin-dependently augmented cell-to-cell transmission to Raji/CD4+ B-cells. Repression of Fascin in HTLV-1-infected T-cells diminished virus release and gag p19 transfer to co-cultured T-cells. Spotting the mechanism, flow cytometry and automatic image analysis showed that Tax-induced T-cell conjugate formation occurred Fascin-independently. However, adhesion of HTLV-1-infected MT-2 cells in co-culture with Jurkat T-cells was reduced upon knockdown of Fascin, suggesting that Fascin contributes to dissemination of infected T-cells. Imaging of chronically infected MS-9 T-cells in co-culture with Jurkat T-cells revealed that Fascin's localization at tight cell-cell contacts is accompanied by gag polarization suggesting that Fascin directly affects the distribution of gag to budding sites, and therefore, indirectly viral transmission. In detail, we found gag clusters that are interspersed with Fascin clusters, suggesting that Fascin makes room for gag in viral biofilms. Moreover, we observed short, Fascin-containing membrane extensions surrounding gag clusters and clutching uninfected T-cells. Finally, we detected Fascin and gag in long-distance cellular protrusions. Taken together, we show for the first time that HTLV-1 usurps the host cell factor Fascin to foster virus release and cell-to-cell transmission.

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  • HTLV-1 concentrates and buds at contacts between conduits and cell bodies, named mini VS.

    “Gross et al. observed concentration and budding of HTLV-1 at such contacts, and named them “mini VS” [43] (Figure 4d).”

    From HIV-1 and HTLV-1 Transmission Modes: Mechanisms and Importance for Virus Spread (2022) · cites this paper as [43]

    The Results (Fig. 7) report gag at cell contacts and in protrusions connecting infected and uninfected T cells. But they describe budding at a putative “mini VS” as a possibility, not an observation, and say the structure had been proposed earlier. The Discussion likewise says whether viruses bud from these protrusions remains to be determined. (LLM, conf=0.90)

    Experimental — accuracy not yet measured

  • HTLV-1 Tax induces expression of actin-bundling protein fascin and secretion of leukotriene B4, which have been implicated in HTLV-1 transmission.

    “Tax also induces the expression of actin-bundling protein fascin [43], and secretion of leukotriene B4 [44], which have been implicated in HTLV-1 transmission.”

    From HIV-1 and HTLV-1 Transmission Modes: Mechanisms and Importance for Virus Spread (2022) · cites this paper as [43]

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Authors
Gross, C., Wiesmann, V., Millen, S., Kalmer, M., Wittenberg, T., Gettemans, J., & Thoma-Kress, A. K.
Affiliations
  • Fraunhofer Institute for Integrated Circuits (DE)
  • Friedrich-Alexander-Universität Erlangen-Nürnberg (DE)
  • Ghent University (BE)
ORCID
Venue
PLOS Pathogens
Publisher
Public Library of Science (PLoS)
Published
2016-10-24
Volume
12
Issue
10
Pages
e1005916
ISSN
  • 1553-7366 (ISSN-L)
  • 1553-7374
DOI
10.1371/journal.ppat.1005916
PMC
PMC5077169
OpenAlex
W2534662926
Cited by
35
References
3
Citations by year
2025: 1 · 2024: 4 · 2023: 1 · 2022: 4 · 2021: 4 · 2020: 7 · 2019: 7 · 2018: 3 · 2017: 4
FWCI
2.83
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS Pathogens (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Ghent University Academic Bibliography (Ghent University) (submittedVersion, cc-by)
  • OPUS FAU (Kooperativer Bibliotheksverbund Berlin-Brandenburg (KOBV), on behalf of the Universitätsbibliothek Erlangen-Nürnberg) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • Publikationsdatenbank der Fraunhofer-Gesellschaft (Fraunhofer-Gesellschaft) (submittedVersion, other-oa)
  • Fraunhofer-Publica (Fraunhofer-Gesellschaft) (submittedVersion)
Funders
  • Deutsche Forschungsgemeinschaft (DE) (SFB796, C6, SFB796, A4)
  • FWO-Flanders
  • BOF/GOA
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › T-cell and Retrovirus Studies
  • Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
  • Health Sciences › Medicine › Oncology › Viral-associated cancers and disorders
Keywords
HTLV-1, fascin, Tax protein, cell-to-cell transmission, virological synapse, actin cytoskeleton, viral budding, T-cell leukemia, viral dissemination, cell adhesion, nanobodies, shRNA knockdown, co-culture
MeSH terms
Carrier Proteins, Enzyme-Linked Immunosorbent Assay, Flow Cytometry, Fluorescent Antibody Technique, Humans, Microfilament Proteins, Transfection, Immunoblotting, Human T-lymphotropic virus 1, HTLV-I Infections, Polymerase Chain Reaction, Gene Products, tax, Microscopy, Confocal, Coculture Techniques, Jurkat Cells, Gene Knockdown Techniques, Virus Release, HEK293 Cells

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