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Research Article
C-type lectin-like receptor 2 (CLEC-2)-dependent dendritic cell migration is controlled by tetraspanin CD37
Charlotte M. de Winde, Alexandra L. Matthews, Sjoerd van Deventer, Alie van der Schaaf, Neil D. Tomlinson, Erik Jansen, Johannes A. Eble, Bernhard Nieswandt, Helen M. McGettrick, Carl G. Figdor, Michael G. Tomlinson, Sophie E. Acton, Annemiek B. van Spriel
J Cell Sci 2018 131: jcs214551 doi: 10.1242/jcs.214551 Published 2 October 2018
Charlotte M. de Winde
Radboud University Medical Center, Radboud Institute for Molecular Life Sciences, Department of Tumor Immunology, 6525 GA Nijmegen, The NetherlandsMRC Laboratory of Molecular Cell Biology, University College London, London WC1E 6BT, UK
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  • ORCID record for Charlotte M. de Winde
Alexandra L. Matthews
School of Biosciences, University of Birmingham, Birmingham B15 2TT, UK
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Sjoerd van Deventer
Radboud University Medical Center, Radboud Institute for Molecular Life Sciences, Department of Tumor Immunology, 6525 GA Nijmegen, The Netherlands
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Alie van der Schaaf
Radboud University Medical Center, Radboud Institute for Molecular Life Sciences, Department of Tumor Immunology, 6525 GA Nijmegen, The Netherlands
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Neil D. Tomlinson
Institute of Cardiovascular Sciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
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  • ORCID record for Neil D. Tomlinson
Erik Jansen
Radboud University Medical Center, Radboud Institute for Molecular Life Sciences, Department of Tumor Immunology, 6525 GA Nijmegen, The Netherlands
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Johannes A. Eble
Institute for Physiological Chemistry and Pathobiochemistry, D-48149 Münster, Germany
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Bernhard Nieswandt
University Clinic of Würzburg and Rudolf Virchow Center for Experimental Biomedicine, 97070 Würzburg, Germany
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Helen M. McGettrick
Institute of Inflammation and Ageing, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
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Carl G. Figdor
Radboud University Medical Center, Radboud Institute for Molecular Life Sciences, Department of Tumor Immunology, 6525 GA Nijmegen, The Netherlands
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Michael G. Tomlinson
School of Biosciences, University of Birmingham, Birmingham B15 2TT, UKCentre of Membrane Proteins and Receptors (COMPARE), Universities of Birmingham and Nottingham, Midlands, UK
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Sophie E. Acton
MRC Laboratory of Molecular Cell Biology, University College London, London WC1E 6BT, UK
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Annemiek B. van Spriel
Radboud University Medical Center, Radboud Institute for Molecular Life Sciences, Department of Tumor Immunology, 6525 GA Nijmegen, The Netherlands
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  • For correspondence: annemiek.vanspriel@radboudumc.nl
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ABSTRACT

Cell migration is central to evoking a potent immune response. Dendritic cell (DC) migration to lymph nodes is dependent on the interaction of C-type lectin-like receptor 2 (CLEC-2; encoded by the gene Clec1b), expressed by DCs, with podoplanin, expressed by lymph node stromal cells, although the underlying molecular mechanisms remain elusive. Here, we show that CLEC-2-dependent DC migration is controlled by tetraspanin CD37, a membrane-organizing protein. We identified a specific interaction between CLEC-2 and CD37, and myeloid cells lacking CD37 (Cd37−/−) expressed reduced surface CLEC-2. CLEC-2-expressing Cd37−/− DCs showed impaired adhesion, migration velocity and displacement on lymph node stromal cells. Moreover, Cd37−/− DCs failed to form actin protrusions in a 3D collagen matrix upon podoplanin-induced CLEC-2 stimulation, phenocopying CLEC-2-deficient DCs. Microcontact printing experiments revealed that CD37 is required for CLEC-2 recruitment in the membrane to its ligand podoplanin. Finally, Cd37−/− DCs failed to inhibit actomyosin contractility in lymph node stromal cells, thus phenocopying CLEC-2-deficient DCs. This study demonstrates that tetraspanin CD37 controls CLEC-2 membrane organization and provides new molecular insights into the mechanisms underlying CLEC-2-dependent DC migration.

This article has an associated First Person interview with the first author of the paper.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: C.M.d.W., S.v.D., M.G.T., S.E.A., A.B.v.S.; Methodology: C.M.d.W., M.G.T., S.E.A., A.B.v.S.; Validation: C.M.d.W., A.L.M.; Formal analysis: C.M.d.W., A.L.M.; Investigation: C.M.d.W., A.L.M., A.v.d.S., N.D.T., E.J., H.M.M., S.E.A.; Resources: J.A.E., B.N., H.M.M., S.E.A.; Writing - original draft: C.M.d.W.; Writing - review & editing: A.L.M., S.v.D., H.M.M., M.G.T., S.E.A., A.B.v.S.; Visualization: C.M.d.W., A.L.M.; Supervision: C.G.F., M.G.T., S.E.A., A.B.v.S.; Funding acquisition: C.M.d.W., A.L.M., H.M.M., C.G.F., M.G.T., S.E.A., A.B.v.S.

  • Funding

    This work was supported by Erasmus+ [Staff Mobility Grant to C.M.d.W.], Nederlandse Organisatie voor Wetenschappelijk Onderzoek [019.162LW.004 to C.M.d.W.; Scientific Research Spinoza Award to C.G.F.; 864.11.006 and ICI-024.002.009 to A.B.v.S.], the Biotechnology and Biological Sciences Research Council [PhD Studentship to A.L.M.], the Medical Research Council [PhD Studentship to N.D.T.; G0400247 to M.G.T.; MC_U12266B to S.E.A.], Deutsche Forschungsgemeinschaft [SFB1009 A09 to J.A.E.; SFB/TR 240 to B.N.], Arthritis Research UK [19899 to H.M.M.], the European Research Council [269019 to C.G.F.; 724281 to A.B.v.S.], KWF Kankerbestrijding [KUN2009-4402 to C.G.F.; KUN2014-6845 to A.B.v.S.], the British Heart Foundation [FS/08/062/25797 to M.G.T.] and Cancer Research UK [CRUK-A19763 to S.E.A.].

  • Supplementary information

    Supplementary information available online at http://jcs.biologists.org/lookup/doi/10.1242/jcs.214551.supplemental

  • Received January 2, 2018.
  • Accepted August 23, 2018.
  • © 2018. Published by The Company of Biologists Ltd
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Keywords

  • CLEC-2
  • Dendritic cell
  • Migration
  • Membrane organization
  • Tetraspanin

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Research Article
C-type lectin-like receptor 2 (CLEC-2)-dependent dendritic cell migration is controlled by tetraspanin CD37
Charlotte M. de Winde, Alexandra L. Matthews, Sjoerd van Deventer, Alie van der Schaaf, Neil D. Tomlinson, Erik Jansen, Johannes A. Eble, Bernhard Nieswandt, Helen M. McGettrick, Carl G. Figdor, Michael G. Tomlinson, Sophie E. Acton, Annemiek B. van Spriel
J Cell Sci 2018 131: jcs214551 doi: 10.1242/jcs.214551 Published 2 October 2018
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Research Article
C-type lectin-like receptor 2 (CLEC-2)-dependent dendritic cell migration is controlled by tetraspanin CD37
Charlotte M. de Winde, Alexandra L. Matthews, Sjoerd van Deventer, Alie van der Schaaf, Neil D. Tomlinson, Erik Jansen, Johannes A. Eble, Bernhard Nieswandt, Helen M. McGettrick, Carl G. Figdor, Michael G. Tomlinson, Sophie E. Acton, Annemiek B. van Spriel
J Cell Sci 2018 131: jcs214551 doi: 10.1242/jcs.214551 Published 2 October 2018

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