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T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases

Author

Listed:
  • Thorsten R. Mempel

    (Harvard Medical School)

  • Sarah E. Henrickson

    (Harvard Medical School)

  • Ulrich H. von Andrian

    (Harvard Medical School)

Abstract

Primary T-cell responses in lymph nodes (LNs) require contact-dependent information exchange between T cells and dendritic cells (DCs). Because lymphocytes continually enter and leave normal LNs, the resident lymphocyte pool is composed of non-synchronized cells with different dwell times that display heterogeneous behaviour in mouse LNs in vitro1,2,3. Here we employ two-photon microscopy in vivo to study antigen-presenting DCs and naive T cells whose dwell time in LNs was synchronized. During the first 8 h after entering from the blood, T cells underwent multiple short encounters with DCs, progressively decreased their motility, and upregulated activation markers. During the subsequent 12 h T cells formed long-lasting stable conjugates with DCs and began to secrete interleukin-2 and interferon-γ. On the second day, coinciding with the onset of proliferation, T cells resumed their rapid migration and short DC contacts. Thus, T-cell priming by DCs occurs in three successive stages: transient serial encounters during the first activation phase are followed by a second phase of stable contacts culminating in cytokine production, which makes a transition into a third phase of high motility and rapid proliferation.

Suggested Citation

  • Thorsten R. Mempel & Sarah E. Henrickson & Ulrich H. von Andrian, 2004. "T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases," Nature, Nature, vol. 427(6970), pages 154-159, January.
  • Handle: RePEc:nat:nature:v:427:y:2004:i:6970:d:10.1038_nature02238
    DOI: 10.1038/nature02238
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    1. Hong Sheng Quah & Elaine Yiqun Cao & Lisda Suteja & Constance H. Li & Hui Sun Leong & Fui Teen Chong & Shilpi Gupta & Camille Arcinas & John F. Ouyang & Vivian Ang & Teja Celhar & Yunqian Zhao & Hui C, 2023. "Single cell analysis in head and neck cancer reveals potential immune evasion mechanisms during early metastasis," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    2. Brian J Schmidt & Jason A Papin & Michael B Lawrence, 2009. "Nano-motion Dynamics are Determined by Surface-Tethered Selectin Mechanokinetics and Bond Formation," PLOS Computational Biology, Public Library of Science, vol. 5(12), pages 1-19, December.
    3. Frederic Geissmann & Thomas O Cameron & Stephane Sidobre & Natasha Manlongat & Mitchell Kronenberg & Michael J Briskin & Michael L Dustin & Dan R Littman, 2005. "Intravascular Immune Surveillance by CXCR6+ NKT Cells Patrolling Liver Sinusoids," PLOS Biology, Public Library of Science, vol. 3(4), pages 1-1, April.
    4. 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.
    5. G Matthew Fricke & Kenneth A Letendre & Melanie E Moses & Judy L Cannon, 2016. "Persistence and Adaptation in Immunity: T Cells Balance the Extent and Thoroughness of Search," PLOS Computational Biology, Public Library of Science, vol. 12(3), pages 1-23, March.
    6. 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.
    7. Fan Xia & Cheng-Rui Qian & Zhou Xun & Yannick Hamon & Anne-Marie Sartre & Anthony Formisano & Sébastien Mailfert & Marie-Claire Phelipot & Cyrille Billaudeau & Sébastien Jaeger & Jacques Nunès & Xiao-, 2018. "TCR and CD28 Concomitant Stimulation Elicits a Distinctive Calcium Response in Naive T Cells," Post-Print hal-02084941, HAL.
    8. Frederik Graw & Roland R Regoes, 2009. "Investigating CTL Mediated Killing with a 3D Cellular Automaton," PLOS Computational Biology, Public Library of Science, vol. 5(8), pages 1-12, August.
    9. Elisabeth H. Vollmann & Kristin Rattay & Olga Barreiro & Aude Thiriot & Rebecca A. Fuhlbrigge & Vladimir Vrbanac & Ki-Wook Kim & Steffen Jung & Andrew M. Tager & Ulrich H. von Andrian, 2021. "Specialized transendothelial dendritic cells mediate thymic T-cell selection against blood-borne macromolecules," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    10. Colleen M Witt & Subhadip Raychaudhuri & Brian Schaefer & Arup K Chakraborty & Ellen A Robey, 2005. "Directed Migration of Positively Selected Thymocytes Visualized in Real Time," PLOS Biology, Public Library of Science, vol. 3(6), pages 1-1, May.
    11. Kenneth Letendre & Emmanuel Donnadieu & Melanie E Moses & Judy L Cannon, 2015. "Bringing Statistics Up to Speed with Data in Analysis of Lymphocyte Motility," PLOS ONE, Public Library of Science, vol. 10(5), pages 1-18, May.

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