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Cited by 64T-cell and Retrovirus StudiesExtracellular vesicles in diseaseViral-associated cancers and disorders

HTLV-1 Extracellular Vesicles Promote Cell-to-Cell Contact

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Pinto, Daniel O., DeMarino, Catherine, Pleet, Michelle L., Cowen, Maria, Branscome, Heather, Al Sharif, Sarah, Jones, Jennifer, Dutartre, Helene +4 more·2019·Frontiers in Microbiology
DOI 10.3389/fmicb.2019.02147PMC PMC6759572
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Abstract

Human T-cell leukemia virus-1 (HTLV-1) is a neglected and incurable retrovirus estimated to infect 5 to 10 million worldwide. Specific indigenous Australian populations report infection rates of more than 40%, suggesting a potential evolution of the virus with global implications. HTLV-1 causes adult T-cell leukemia/lymphoma (ATLL), and a neurological disease named HTLV-1 associated myelopathy/tropical spastic paraparesis (HAM/TSP). Even though HTLV-1 transmission primarily occurs from cell-to-cell, there is still a gap of knowledge regarding the mechanisms of viral spread and disease progression. We have recently shown that Extracellular Vesicles (EVs) ubiquitously produced by cells may be used by HTLV-1 to transport viral proteins and RNA, and elicit adverse effects on recipient uninfected cells. The viral proteins Tax and HBZ are involved in disease progression and impairment of autophagy in infected cells. Here, we show that activation of HTLV-1 via ionizing radiation (IR) causes a significant increase of intracellular Tax, but not EV-associated Tax. Also, lower density EVs from HTLV-1-infected cells, separated by an Iodixanol density gradient, are positive for gp61+++/Tax+++/HBZ+ proteins (HTLV-1 EVs). We found that HTLV-1 EVs are not infectious when tested in multiple cell lines. However, these EVs promote cell-to-cell contact of uninfected cells, a phenotype which was enhanced with IR, potentially promoting viral spread. We treated humanized NOG mice with HTLV-1 EVs prior to infection and observed an increase in viral RNA synthesis in mice compared to control (EVs from uninfected cells). Proviral DNA levels were also quantified in blood, lung, spleen, liver, and brain post-treatment with HTLV-1 EVs, and we observed a consistent increase in viral DNA levels across all tissues, especially the brain. Finally, we show direct implications of EVs in viral spread and disease progression and suggest a two-step model of infection including the release of EVs from donor cells and recruitment of recipient cells as well as an increase in recipient cell-to-cell contact promoting viral spread.

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  • Exosomes from HTLV-1-infected HUT102 cells containing Tax increase intercellular contacts and enhance viral transmission in vitro; pretreatment of humanized mice with such exosomes increases HTLV-1 infection of organs/tissues in vivo.

    “In in vitro experiments, exosomes secreted by HTLV-1-infected HUT102 cells and containing the viral protein Tax, increased the number of intercellular contacts, which led to enhanced viral transmission. In in vivo experiments, pretreatment of humanized mice with such exosomes increased the infection of different organs and tissues by HTLV-1 [122].”

    From HIV-1 and HTLV-1 Transmission Modes: Mechanisms and Importance for Virus Spread (2022) · cites this paper as [122]

    The Results section, “Increased Cell-to-Cell Contact Promotes Potential Increase in Viral Spread” (page unavailable), reports greater cell contact and viral RNA in recipient cells treated with HUT102-derived EVs. The in vivo Results and Discussion report higher viral levels across tissues in EV-pretreated mice. The claim overstates the in vitro mechanism: the paper says increased contact could potentially facilitate viral spread, not that it was shown to cause enhanced transmission. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Animal models can provide information about HTLV-1 replication and virus-associated disease progression.

    “Some mechanisms of HTLV-1 replication and virus-associated disease progression can be learnt from animal models [44,122,136,137].”

    From HIV-1 and HTLV-1 Transmission Modes: Mechanisms and Importance for Virus Spread (2022) · cites this paper as [122]

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Cited by

Sorted by citations

Authors
Pinto, D. O., DeMarino, C., Pleet, M. L., Cowen, M., Branscome, H., Al Sharif, S., Jones, J., Dutartre, H., Lepene, B., Liotta, L. A., Mahieux, R., & Kashanchi, F.
Affiliations
  • George Mason University (US)
  • National Institutes of Health (US)
  • Ceres Nanosciences (US)
  • Lyon 1 Université (FR)
Corresponding author
Kashanchi, Fatah
ORCID
Venue
Frontiers in Microbiology
Publisher
Frontiers Media SA
Published
2019-09-18
Volume
10
Pages
2147-2147
ISSN
1664-302X (ISSN-L)
DOI
10.3389/fmicb.2019.02147
PMC
PMC6759572
OpenAlex
W2971078149
Cited by
64
References
2
Citations by year
2026: 2 · 2025: 5 · 2024: 11 · 2023: 11 · 2022: 14 · 2021: 8 · 2020: 13
FWCI
3.50
Type
journal article
Language
en
Open access
Licence
Locations
  • Frontiers in Microbiology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Institutes of Health (AI078859, AI074410, AI127351-01, AI043894, NS0099029)
  • Ligue Contre le Cancer
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › T-cell and Retrovirus Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
  • Health Sciences › Medicine › Oncology › Viral-associated cancers and disorders
Keywords
HTLV-1, extracellular vesicles, cell-cell contact, viral spread, taxation, HBZ, ionizing radiation, proviral DNA, viral RNA synthesis, adult T-cell leukemia/lymphoma, HAM/TSP, virus transmission, autophagy

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