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Invariant γδTCR natural killer-like effector T cells in the naked mole-rat

Author

Listed:
  • Guillem Sanchez Sanchez

    (Université Libre de Bruxelles (ULB)
    Université Libre de Bruxelles (ULB)
    Université Libre de Bruxelles (ULB)
    WEL Research Institute)

  • Stephan Emmrich

    (University of Rochester)

  • Maria Georga

    (Université de Montpellier (UM))

  • Ariadni Papadaki

    (Université de Montpellier (UM))

  • Sofia Kossida

    (Université de Montpellier (UM))

  • Andrei Seluanov

    (University of Rochester
    University of Rochester)

  • Vera Gorbunova

    (University of Rochester
    University of Rochester)

  • David Vermijlen

    (Université Libre de Bruxelles (ULB)
    Université Libre de Bruxelles (ULB)
    Université Libre de Bruxelles (ULB)
    WEL Research Institute)

Abstract

The naked mole-rat (Heterocephalus glaber) is a long-lived rodent species showing resistance to the development of cancer. Although naked mole-rats have been reported to lack natural killer (NK) cells, γδ T cell-based immunity has been suggested in this species, which could represent an important arm of the immune system for antitumor responses. Here, we investigate the biology of these unconventional T cells in peripheral tissues (blood, spleen) and thymus of the naked mole-rat at different ages by TCR repertoire profiling and single-cell gene expression analysis. Using our own TCR annotation in the naked mole-rat genome, we report that the γδ TCR repertoire is dominated by a public invariant Vγ4-2/Vδ1-4 TCR, containing the complementary-determining-region-3 (CDR3)γ CTYWDSNYAKKLF / CDR3δ CALWELRTGGITAQLVF that are likely generated by short-homology-repeat-driven DNA rearrangements. This invariant TCR is specifically found in γδ T cells expressing genes associated with NK cytotoxicity and is generated in both the thoracic and cervical thymus of the naked mole-rat until adult life. Our results indicate that invariant Vγ4-2/Vδ1-4 NK-like effector T cells in the naked mole-rat can contribute to tumor immunosurveillance by γδ TCR-mediated recognition of a common molecular signal.

Suggested Citation

  • Guillem Sanchez Sanchez & Stephan Emmrich & Maria Georga & Ariadni Papadaki & Sofia Kossida & Andrei Seluanov & Vera Gorbunova & David Vermijlen, 2024. "Invariant γδTCR natural killer-like effector T cells in the naked mole-rat," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48652-z
    DOI: 10.1038/s41467-024-48652-z
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    References listed on IDEAS

    as
    1. Guillem Sanchez Sanchez & Maria Papadopoulou & Abdulkader Azouz & Yohannes Tafesse & Archita Mishra & Jerry K. Y. Chan & Yiping Fan & Isoline Verdebout & Silvana Porco & Frédérick Libert & Florent Gin, 2022. "Identification of distinct functional thymic programming of fetal and pediatric human γδ thymocytes via single-cell analysis," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    2. Fazal Hadi & Yavuz Kulaberoglu & Kyren A. Lazarus & Karsten Bach & Rosemary Ugur & Paul Beattie & Ewan St John Smith & Walid T. Khaled, 2020. "Transformation of naked mole-rat cells," Nature, Nature, vol. 583(7814), pages 1-7, July.
    3. Mikhail Shugay & Dmitriy V Bagaev & Maria A Turchaninova & Dmitriy A Bolotin & Olga V Britanova & Ekaterina V Putintseva & Mikhail V Pogorelyy & Vadim I Nazarov & Ivan V Zvyagin & Vitalina I Kirgizova, 2015. "VDJtools: Unifying Post-analysis of T Cell Receptor Repertoires," PLOS Computational Biology, Public Library of Science, vol. 11(11), pages 1-16, November.
    4. Masayuki Hirano & Peng Guo & Nathanael McCurley & Michael Schorpp & Sabyasachi Das & Thomas Boehm & Max D. Cooper, 2013. "Evolutionary implications of a third lymphocyte lineage in lampreys," Nature, Nature, vol. 501(7467), pages 435-438, September.
    5. Xiao Tian & Jorge Azpurua & Christopher Hine & Amita Vaidya & Max Myakishev-Rempel & Julia Ablaeva & Zhiyong Mao & Eviatar Nevo & Vera Gorbunova & Andrei Seluanov, 2013. "High-molecular-mass hyaluronan mediates the cancer resistance of the naked mole rat," Nature, Nature, vol. 499(7458), pages 346-349, July.
    6. Anett Jandke & Daisy Melandri & Leticia Monin & Dmitry S. Ushakov & Adam G. Laing & Pierre Vantourout & Philip East & Takeshi Nitta & Tomoya Narita & Hiroshi Takayanagi & Regina Feederle & Adrian Hayd, 2020. "Butyrophilin-like proteins display combinatorial diversity in selecting and maintaining signature intraepithelial γδ T cell compartments," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
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