IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-34698-4.html
   My bibliography  Save this article

Selective retention of virus-specific tissue-resident T cells in healed skin after recovery from herpes zoster

Author

Listed:
  • Kerry J. Laing

    (University of Washington)

  • Werner J. D. Ouwendijk

    (Erasmus Medical Center)

  • Victoria L. Campbell

    (University of Washington)

  • Christopher L. McClurkan

    (University of Washington)

  • Shahin Mortazavi

    (University of Washington)

  • Michael Elder Waters

    (University of Washington)

  • Maxwell P. Krist

    (University of Washington)

  • Richard Tu

    (University of Washington)

  • Nhi Nguyen

    (University of Washington)

  • Krithi Basu

    (University of Washington)

  • Congrong Miao

    (Division of Viral Diseases)

  • D. Scott Schmid

    (Division of Viral Diseases)

  • Christine Johnston

    (University of Washington
    Fred Hutchinson Cancer Center)

  • Georges M. G. M. Verjans

    (Erasmus Medical Center)

  • David M. Koelle

    (University of Washington
    Fred Hutchinson Cancer Center
    University of Washington
    University of Washington)

Abstract

Herpes zoster is a localized skin infection caused by reactivation of latent varicella-zoster virus. Tissue-resident T cells likely control skin infections. Zoster provides a unique opportunity to determine if focal reinfection of human skin boosts local or disseminated antigen-specific tissue-resident T cells. Here, we show virus-specific T cells are retained over one year in serial samples of rash site and contralateral unaffected skin of individuals recovered from zoster. Consistent with zoster resolution, viral DNA is largely undetectable on skin from day 90 and virus-specific B and T cells decline in blood. In skin, there is selective infiltration and long-term persistence of varicella-zoster virus-specific T cells in the rash site relative to the contralateral site. The skin T cell infiltrates express the canonical tissue-resident T cell markers CD69 and CD103. These findings show that zoster promotes spatially-restricted long-term retention of antigen-specific tissue-resident T cells in previously infected skin.

Suggested Citation

  • Kerry J. Laing & Werner J. D. Ouwendijk & Victoria L. Campbell & Christopher L. McClurkan & Shahin Mortazavi & Michael Elder Waters & Maxwell P. Krist & Richard Tu & Nhi Nguyen & Krithi Basu & Congron, 2022. "Selective retention of virus-specific tissue-resident T cells in healed skin after recovery from herpes zoster," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34698-4
    DOI: 10.1038/s41467-022-34698-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-34698-4
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-34698-4?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. Xiaodong Jiang & Rachael A. Clark & Luzheng Liu & Amy J. Wagers & Robert C. Fuhlbrigge & Thomas S. Kupper, 2012. "Skin infection generates non-migratory memory CD8+ TRM cells providing global skin immunity," Nature, Nature, vol. 483(7388), pages 227-231, March.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Mike B. Barnkob & Yale S. Michaels & Violaine André & Philip S. Macklin & Uzi Gileadi & Salvatore Valvo & Margarida Rei & Corinna Kulicke & Ji-Li Chen & Vitul Jain & Victoria K. Woodcock & Huw Colin-Y, 2024. "Semaphorin 3A causes immune suppression by inducing cytoskeletal paralysis in tumour-specific CD8+ T cells," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Song Li & Wenbin Yu & Fei Xie & Haitao Luo & Zhimin Liu & Weiwei Lv & Duanbo Shi & Dexin Yu & Peng Gao & Cheng Chen & Meng Wei & Wenhao Zhou & Jiaqian Wang & Zhikun Zhao & Xin Dai & Qian Xu & Xue Zhan, 2023. "Neoadjuvant therapy with immune checkpoint blockade, antiangiogenesis, and chemotherapy for locally advanced gastric cancer," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Thillai V. Sekar & Eslam A. Elghonaimy & Katy L. Swancutt & Sebastian Diegeler & Isaac Gonzalez & Cassandra Hamilton & Peter Q. Leung & Jens Meiler & Cristina E. Martina & Michael Whitney & Todd A. Ag, 2023. "Simultaneous selection of nanobodies for accessible epitopes on immune cells in the tumor microenvironment," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    4. Jeremy J. Ratiu & William E. Barclay & Elliot Lin & Qun Wang & Sebastian Wellford & Naren Mehta & Melissa J. Harnois & Devon DiPalma & Sumedha Roy & Alejandra V. Contreras & Mari L. Shinohara & David , 2022. "Loss of Zfp335 triggers cGAS/STING-dependent apoptosis of post-β selection thymocytes," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    5. Jani Huuhtanen & Dipabarna Bhattacharya & Tapio Lönnberg & Matti Kankainen & Cassandra Kerr & Jason Theodoropoulos & Hanna Rajala & Carmelo Gurnari & Tiina Kasanen & Till Braun & Antonella Teramo & Re, 2022. "Single-cell characterization of leukemic and non-leukemic immune repertoires in CD8+ T-cell large granular lymphocytic leukemia," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    6. Emmanuel C. Patin & Pablo Nenclares & Charleen Chan Wah Hak & Magnus T. Dillon & Anton Patrikeev & Martin McLaughlin & Lorna Grove & Shane Foo & Heba Soliman & Joao P. Barata & Joanna Marsden & Holly , 2024. "Sculpting the tumour microenvironment by combining radiotherapy and ATR inhibition for curative-intent adjuvant immunotherapy," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    7. Jani Huuhtanen & Liang Chen & Emmi Jokinen & Henna Kasanen & Tapio Lönnberg & Anna Kreutzman & Katriina Peltola & Micaela Hernberg & Chunlin Wang & Cassian Yee & Harri Lähdesmäki & Mark M. Davis & Sat, 2022. "Evolution and modulation of antigen-specific T cell responses in melanoma patients," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    8. Antonella Teramo & Andrea Binatti & Elena Ciabatti & Gianluca Schiavoni & Giulia Tarrini & Gregorio Barilà & Giulia Calabretto & Cristina Vicenzetto & Vanessa Rebecca Gasparini & Monica Facco & Iacopo, 2022. "Defining TCRγδ lymphoproliferative disorders by combined immunophenotypic and molecular evaluation," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    9. Michael D. Keller & Stefan A. Schattgen & Shanmuganathan Chandrakasan & E. Kaitlynn Allen & Mariah A. Jensen-Wachspress & Christopher A. Lazarski & Muna Qayed & Haili Lang & Patrick J. Hanley & Jay Ta, 2024. "Secondary bone marrow graft loss after third-party virus-specific T cell infusion: Case report of a rare complication," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    10. Yu Guo & Guangshun Zhang & Qi Yang & Xiaowei Xie & Yang Lu & Xuelian Cheng & Hui Wang & Jingxi Liang & Jielin Tang & Yuxin Gao & Hang Shang & Jun Dai & Yongxia Shi & Jiaxi Zhou & Jun Zhou & Hangtian G, 2023. "Discovery and characterization of potent pan-variant SARS-CoV-2 neutralizing antibodies from individuals with Omicron breakthrough infection," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    11. Hongbin Wang & Carol Hoffman & Xinghong Yang & Beata Clapp & David W Pascual, 2020. "Targeting resident memory T cell immunity culminates in pulmonary and systemic protection against Brucella infection," PLOS Pathogens, Public Library of Science, vol. 16(1), pages 1-31, January.
    12. Meng Xu & Taku Ito-Kureha & Hyun-Seo Kang & Aleksandar Chernev & Timsse Raj & Kai P. Hoefig & Christine Hohn & Florian Giesert & Yinhu Wang & Wenliang Pan & Natalia Ziętara & Tobias Straub & Regina Fe, 2024. "The thymocyte-specific RNA-binding protein Arpp21 provides TCR repertoire diversity by binding to the 3’-UTR and promoting Rag1 mRNA expression," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    13. Martin Lauss & Bengt Phung & Troels Holz Borch & Katja Harbst & Kamila Kaminska & Anna Ebbesson & Ingrid Hedenfalk & Joan Yuan & Kari Nielsen & Christian Ingvar & Ana Carneiro & Karolin Isaksson & Kri, 2024. "Molecular patterns of resistance to immune checkpoint blockade in melanoma," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    14. Vitaly V Ganusov & Jeremy Auerbach, 2014. "Mathematical Modeling Reveals Kinetics of Lymphocyte Recirculation in the Whole Organism," PLOS Computational Biology, Public Library of Science, vol. 10(5), pages 1-15, May.
    15. Juan Blanco-Heredia & Carla Anjos Souza & Juan L. Trincado & Maria Gonzalez-Cao & Samuel Gonçalves-Ribeiro & Sara Ruiz Gil & Dmytro Pravdyvets & Samandhy Cedeño & Maurizio Callari & Antonio Marra & An, 2024. "Converging and evolving immuno-genomic routes toward immune escape in breast cancer," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    16. Nicole Caduff & Lisa Rieble & Michelle Böni & Donal McHugh & Romin Roshan & Wendell Miley & Nazzarena Labo & Sumanta Barman & Matthew Trivett & Douwe M. T. Bosma & Julia Rühl & Norbert Goebels & Denis, 2024. "KSHV infection of B cells primes protective T cell responses in humanized mice," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    17. Zhongchao Li & Jing Liu & Bo Zhang & Jinbo Yue & Xuetao Shi & Kai Cui & Zhaogang Liu & Zhibin Chang & Zhicheng Sun & Mingming Li & Yue Yang & Zhao Ma & Lei Li & Chengsheng Zhang & Pengfei Sun & Jingta, 2024. "Neoadjuvant tislelizumab plus stereotactic body radiotherapy and adjuvant tislelizumab in early-stage resectable hepatocellular carcinoma: the Notable-HCC phase 1b trial," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    18. 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.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34698-4. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.