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Chemokines enhance immunity by guiding naive CD8+ T cells to sites of CD4+ T cell–dendritic cell interaction

Author

Listed:
  • Flora Castellino

    (National Institutes of Health
    Chiron Vaccines)

  • Alex Y. Huang

    (National Institutes of Health)

  • Grégoire Altan-Bonnet

    (National Institutes of Health
    cBio, Memorial Sloan-Kettering Cancer Center)

  • Sabine Stoll

    (National Institutes of Health
    University of Mainz)

  • Clemens Scheinecker

    (National Institutes of Health
    Medical University of Vienna, General Hospital of Vienna)

  • Ronald N. Germain

    (National Institutes of Health)

Abstract

CD8+ T cells have a crucial role in resistance to pathogens and can kill malignant cells; however, some critical functions of these lymphocytes depend on helper activity provided by a distinct population of CD4+ T cells. Cooperation between these lymphocyte subsets involves recognition of antigens co-presented by the same dendritic cell, but the frequencies of such antigen-bearing cells early in an infection and of the relevant naive T cells are both low. This suggests that an active mechanism facilitates the necessary cell–cell associations. Here we demonstrate that after immunization but before antigen recognition, naive CD8+ T cells in immunogen-draining lymph nodes upregulate the chemokine receptor CCR5, permitting these cells to be attracted to sites of antigen-specific dendritic cell–CD4+ T cell interaction where the cognate chemokines CCL3 and CCL4 (also known as MIP-1α and MIP-1β) are produced. Interference with this actively guided recruitment markedly reduces the ability of CD4+ T cells to promote memory CD8+ T-cell generation, indicating that an orchestrated series of differentiation events drives nonrandom cell–cell interactions within lymph nodes, optimizing CD8+ T-cell immune responses involving the few antigen-specific precursors present in the naive repertoire.

Suggested Citation

  • Flora Castellino & Alex Y. Huang & Grégoire Altan-Bonnet & Sabine Stoll & Clemens Scheinecker & Ronald N. Germain, 2006. "Chemokines enhance immunity by guiding naive CD8+ T cells to sites of CD4+ T cell–dendritic cell interaction," Nature, Nature, vol. 440(7086), pages 890-895, April.
  • Handle: RePEc:nat:nature:v:440:y:2006:i:7086:d:10.1038_nature04651
    DOI: 10.1038/nature04651
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    Citations

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    Cited by:

    1. Renske M A Vroomans & Athanasius F M Marée & Rob J de Boer & Joost B Beltman, 2012. "Chemotactic Migration of T Cells towards Dendritic Cells Promotes the Detection of Rare Antigens," PLOS Computational Biology, Public Library of Science, vol. 8(11), pages 1-13, November.
    2. Edward J Banigan & Tajie H Harris & David A Christian & Christopher A Hunter & Andrea J Liu, 2015. "Heterogeneous CD8+ T Cell Migration in the Lymph Node in the Absence of Inflammation Revealed by Quantitative Migration Analysis," PLOS Computational Biology, Public Library of Science, vol. 11(2), pages 1-20, February.
    3. Bartosz Wiernicki & Sophia Maschalidi & Jonathan Pinney & Sandy Adjemian & Tom Vanden Berghe & Kodi S. Ravichandran & Peter Vandenabeele, 2022. "Cancer cells dying from ferroptosis impede dendritic cell-mediated anti-tumor immunity," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    4. Chirag Krishna & Joshua Chiou & Saori Sakaue & Joyce B. Kang & Stephen M. Christensen & Isac Lee & Melis Atalar Aksit & Hye In Kim & David Schack & Soumya Raychaudhuri & Daniel Ziemek & Xinli Hu, 2024. "The influence of HLA genetic variation on plasma protein expression," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    5. Jing Wang & Ramon Ocadiz-Ruiz & Matthew S. Hall & Grace G. Bushnell & Sophia M. Orbach & Joseph T. Decker & Ravi M. Raghani & Yining Zhang & Aaron H. Morris & Jacqueline S. Jeruss & Lonnie D. Shea, 2023. "A synthetic metastatic niche reveals antitumor neutrophils drive breast cancer metastatic dormancy in the lungs," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    6. Chaim A. Schramm & Damee Moon & Lowrey Peyton & Noemia S. Lima & Christian Wake & Kristin L. Boswell & Amy R. Henry & Farida Laboune & David Ambrozak & Samuel W. Darko & I-Ting Teng & Kathryn E. Fould, 2023. "Interaction dynamics between innate and adaptive immune cells responding to SARS-CoV-2 vaccination in non-human primates," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    7. Shuang Shang & Chen Yang & Fei Chen & Ren-shen Xiang & Huan Zhang & Shu-yuan Dai & Jing Liu & Xiao-xi Lv & Cheng Zhang & Xiao-tong Liu & Qi Zhang & Shuai-bing Lu & Jia-wei Song & Jiao-jiao Yu & Ji-cha, 2023. "ID1 expressing macrophages support cancer cell stemness and limit CD8+ T cell infiltration in colorectal cancer," Nature Communications, Nature, vol. 14(1), pages 1-19, December.

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