IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-51763-2.html
   My bibliography  Save this article

Discovery of an unconventional lamprey lymphocyte lineage highlights divergent features in vertebrate adaptive immune system evolution

Author

Listed:
  • Yingyi Huang

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Xiang Liu

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center
    BGI Research)

  • Shuo Li

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Chen Li

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Hong-Yan Wang

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Qun Liu

    (BGI Research
    BGI Research
    University of Copenhagen)

  • Jian-Yang Chen

    (BGI Research
    BGI Research)

  • Yingying Zhang

    (BGI Research
    BGI Research)

  • Yanan Li

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Xianghui Zhang

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Qian Wang

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Kaiqiang Liu

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Yu-Yan Liu

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

  • Yue Pang

    (Liaoning Normal University)

  • Shanshan Liu

    (BGI Research
    MGI Tech)

  • Guangyi Fan

    (BGI Research
    BGI Research
    BGI Research)

  • Changwei Shao

    (Chinese Academy of Fishery Sciences
    Qingdao Marine Science and Technology Center)

Abstract

Lymphocyte receptors independently evolved in both jawed and jawless vertebrates with similar adaptive immune responses. However, the diversity of functional subtypes and molecular architecture in jawless vertebrate lymphocytes, comparable to jawed species, is not well defined. Here, we profile the gills, intestines, and blood of the lamprey, Lampetra morii, with single-cell RNA sequencing, using a full-length transcriptome as a reference. Our findings reveal higher tissue-specific heterogeneity among T-like cells in contrast to B-like cells. Notably, we identify a unique T-like cell subtype expressing a homolog of the nonlymphoid hematopoietic growth factor receptor, MPL-like (MPL-L). These MPL-L+ T-like cells exhibit features distinct from T cells of jawed vertebrates, particularly in their elevated expression of hematopoietic genes. We further discovered that MPL-L+ VLRA+ T-like cells are widely present in the typhlosole, gill, liver, kidney, and skin of lamprey and they proliferate in response to both a T cell mitogen and recombinant human thrombopoietin. These findings provide new insights into the adaptive immune response in jawless vertebrates, shedding new light on the evolution of adaptive immunity.

Suggested Citation

  • Yingyi Huang & Xiang Liu & Shuo Li & Chen Li & Hong-Yan Wang & Qun Liu & Jian-Yang Chen & Yingying Zhang & Yanan Li & Xianghui Zhang & Qian Wang & Kaiqiang Liu & Yu-Yan Liu & Yue Pang & Shanshan Liu &, 2024. "Discovery of an unconventional lamprey lymphocyte lineage highlights divergent features in vertebrate adaptive immune system evolution," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51763-2
    DOI: 10.1038/s41467-024-51763-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-51763-2
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-51763-2?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. Peter A. Szabo & Hanna Mendes Levitin & Michelle Miron & Mark E. Snyder & Takashi Senda & Jinzhou Yuan & Yim Ling Cheng & Erin C. Bush & Pranay Dogra & Puspa Thapa & Donna L. Farber & Peter A. Sims, 2019. "Single-cell transcriptomics of human T cells reveals tissue and activation signatures in health and disease," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    2. Zeev Pancer & Chris T. Amemiya & Götz R. A. Ehrhardt & Jill Ceitlin & G. Larry Gartland & Max D. Cooper, 2004. "Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey," Nature, Nature, vol. 430(6996), pages 174-180, July.
    3. Baubak Bajoghli & Peng Guo & Narges Aghaallaei & Masayuki Hirano & Christine Strohmeier & Nathanael McCurley & Dale E. Bockman & Michael Schorpp & Max D. Cooper & Thomas Boehm, 2011. "A thymus candidate in lampreys," Nature, Nature, vol. 470(7332), pages 90-94, February.
    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. Alka Agrawal & Quinn M. Eastman & David G. Schatz, 1998. "Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system," Nature, Nature, vol. 394(6695), pages 744-751, August.
    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. Xiaojian Lu & Yanwei Luo & Xichen Nie & Bailing Zhang & Xiaoyan Wang & Ran Li & Guangmin Liu & Qianyin Zhou & Zhizhong Liu & Liqing Fan & James M. Hotaling & Zhe Zhang & Hao Bo & Jingtao Guo, 2023. "Single-cell multi-omics analysis of human testicular germ cell tumor reveals its molecular features and microenvironment," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Felix Drost & Yang An & Irene Bonafonte-Pardàs & Lisa M. Dratva & Rik G. H. Lindeboom & Muzlifah Haniffa & Sarah A. Teichmann & Fabian Theis & Mohammad Lotfollahi & Benjamin Schubert, 2024. "Multi-modal generative modeling for joint analysis of single-cell T cell receptor and gene expression data," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Jeff DeMartino & Michael T. Meister & Lindy L. Visser & Mariël Brok & Marian J. A. Groot Koerkamp & Amber K. L. Wezenaar & Laura S. Hiemcke-Jiwa & Terezinha Souza & Johannes H. M. Merks & Anne C. Rios, 2023. "Single-cell transcriptomics reveals immune suppression and cell states predictive of patient outcomes in rhabdomyosarcoma," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Augusto Faria Andrade & Alva Annett & Elham Karimi & Danai Georgia Topouza & Morteza Rezanejad & Yitong Liu & Michael McNicholas & Eduardo G. Gonzalez Santiago & Dhana Llivichuzhca-Loja & Arne Gehlhaa, 2024. "Immune landscape of oncohistone-mutant gliomas reveals diverse myeloid populations and tumor-promoting function," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    5. 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.
    6. Osama Al-Dalahmah & Michael G. Argenziano & Adithya Kannan & Aayushi Mahajan & Julia Furnari & Fahad Paryani & Deborah Boyett & Akshay Save & Nelson Humala & Fatima Khan & Juncheng Li & Hong Lu & Yu S, 2023. "Re-convolving the compositional landscape of primary and recurrent glioblastoma reveals prognostic and targetable tissue states," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    7. Nader Atlasy & Anna Bujko & Espen S. Bækkevold & Peter Brazda & Eva Janssen-Megens & Knut E. A. Lundin & Jørgen Jahnsen & Frode L. Jahnsen & Hendrik G. Stunnenberg, 2022. "Single cell transcriptomic analysis of the immune cell compartment in the human small intestine and in Celiac disease," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    8. Qi Zhang & Rober Abdo & Cristiana Iosef & Tomonori Kaneko & Matthew Cecchini & Victor K. Han & Shawn Shun-Cheng Li, 2022. "The spatial transcriptomic landscape of non-small cell lung cancer brain metastasis," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    9. Alexandra Argyriou & Marc H. Wadsworth & Adrian Lendvai & Stephen M. Christensen & Aase H. Hensvold & Christina Gerstner & Annika Vollenhoven & Kellie Kravarik & Aaron Winkler & Vivianne Malmström & K, 2022. "Single cell sequencing identifies clonally expanded synovial CD4+ TPH cells expressing GPR56 in rheumatoid arthritis," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    10. Anja Fischer & Thomas K. Albert & Natalia Moreno & Marta Interlandi & Jana Mormann & Selina Glaser & Paurnima Patil & Flavia W. Faria & Mathis Richter & Archana Verma & Sebastian T. Balbach & Rabea Wa, 2024. "Lack of SMARCB1 expression characterizes a subset of human and murine peripheral T-cell lymphomas," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    11. Kaitlyn A. Lagattuta & Hannah L. Park & Laurie Rumker & Kazuyoshi Ishigaki & Aparna Nathan & Soumya Raychaudhuri, 2024. "The genetic basis of autoimmunity seen through the lens of T cell functional traits," Nature Communications, Nature, vol. 15(1), pages 1-6, December.
    12. E. Koncina & M. Nurmik & V. I. Pozdeev & C. Gilson & M. Tsenkova & R. Begaj & S. Stang & A. Gaigneaux & C. Weindorfer & F. Rodriguez & M. Schmoetten & E. Klein & J. Karta & V. S. Atanasova & K. Grzyb , 2023. "IL1R1+ cancer-associated fibroblasts drive tumor development and immunosuppression in colorectal cancer," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    13. 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:15:y:2024:i:1:d:10.1038_s41467-024-51763-2. 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.