Cytotoxic T cells swarm by homotypic chemokine signalling
Cytotoxic T lymphocytes (CTLs) are thought to arrive at target sites either via random search or following signals by other leukocytes. Here, we reveal independent emergent behaviour in CTL populations attacking tumour masses. Primary murine CTLs coordinate their migration in a process reminiscent o...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2020-10-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/56554 |
| _version_ | 1811202594379399168 |
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| author | Jorge Luis Galeano Niño Sophie V Pageon Szun S Tay Feyza Colakoglu Daryan Kempe Jack Hywood Jessica K Mazalo James Cremasco Matt A Govendir Laura F Dagley Kenneth Hsu Simone Rizzetto Jerzy Zieba Gregory Rice Victoria Prior Geraldine M O'Neill Richard J Williams David R Nisbet Belinda Kramer Andrew I Webb Fabio Luciani Mark N Read Maté Biro |
| author_facet | Jorge Luis Galeano Niño Sophie V Pageon Szun S Tay Feyza Colakoglu Daryan Kempe Jack Hywood Jessica K Mazalo James Cremasco Matt A Govendir Laura F Dagley Kenneth Hsu Simone Rizzetto Jerzy Zieba Gregory Rice Victoria Prior Geraldine M O'Neill Richard J Williams David R Nisbet Belinda Kramer Andrew I Webb Fabio Luciani Mark N Read Maté Biro |
| author_sort | Jorge Luis Galeano Niño |
| collection | DOAJ |
| description | Cytotoxic T lymphocytes (CTLs) are thought to arrive at target sites either via random search or following signals by other leukocytes. Here, we reveal independent emergent behaviour in CTL populations attacking tumour masses. Primary murine CTLs coordinate their migration in a process reminiscent of the swarming observed in neutrophils. CTLs engaging cognate targets accelerate the recruitment of distant T cells through long-range homotypic signalling, in part mediated via the diffusion of chemokines CCL3 and CCL4. Newly arriving CTLs augment the chemotactic signal, further accelerating mass recruitment in a positive feedback loop. Activated effector human T cells and chimeric antigen receptor (CAR) T cells similarly employ intra-population signalling to drive rapid convergence. Thus, CTLs recognising a cognate target can induce a localised mass response by amplifying the direct recruitment of additional T cells independently of other leukocytes. |
| first_indexed | 2024-04-12T02:41:22Z |
| format | Article |
| id | doaj.art-d671480f3ae34c5f99f6cf4e7a7c2792 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T02:41:22Z |
| publishDate | 2020-10-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-d671480f3ae34c5f99f6cf4e7a7c27922022-12-22T03:51:18ZengeLife Sciences Publications LtdeLife2050-084X2020-10-01910.7554/eLife.56554Cytotoxic T cells swarm by homotypic chemokine signallingJorge Luis Galeano Niño0Sophie V Pageon1https://orcid.org/0000-0003-1701-5551Szun S Tay2https://orcid.org/0000-0003-0186-8154Feyza Colakoglu3Daryan Kempe4Jack Hywood5Jessica K Mazalo6James Cremasco7Matt A Govendir8Laura F Dagley9https://orcid.org/0000-0003-4171-3712Kenneth Hsu10Simone Rizzetto11https://orcid.org/0000-0003-3881-8759Jerzy Zieba12Gregory Rice13Victoria Prior14https://orcid.org/0000-0002-2285-5398Geraldine M O'Neill15Richard J Williams16David R Nisbet17Belinda Kramer18Andrew I Webb19Fabio Luciani20Mark N Read21Maté Biro22https://orcid.org/0000-0001-5852-3726EMBL Australia, Single Molecule Science node, University of New South Wales, Sydney, Australia; School of Medical Sciences, Faculty of Medicine, University of New South Wales, Sydney, AustraliaEMBL Australia, Single Molecule Science node, University of New South Wales, Sydney, Australia; School of Medical Sciences, Faculty of Medicine, University of New South Wales, Sydney, AustraliaEMBL Australia, Single Molecule Science node, University of New South Wales, Sydney, Australia; School of Medical Sciences, Faculty of Medicine, University of New South Wales, Sydney, AustraliaEMBL Australia, Single Molecule Science node, University of New South Wales, Sydney, Australia; School of Medical Sciences, Faculty of Medicine, University of New South Wales, Sydney, AustraliaEMBL Australia, Single Molecule Science node, University of New South Wales, Sydney, Australia; School of Medical Sciences, Faculty of Medicine, University of New South Wales, Sydney, AustraliaSydney Medical School, The University of Sydney, Sydney, AustraliaEMBL Australia, Single Molecule Science node, University of New South Wales, Sydney, Australia; School of Medical Sciences, Faculty of Medicine, University of New South Wales, Sydney, AustraliaEMBL Australia, Single Molecule Science node, University of New South Wales, Sydney, Australia; School of Medical Sciences, Faculty of Medicine, University of New South Wales, Sydney, AustraliaEMBL Australia, Single Molecule Science node, University of New South Wales, Sydney, Australia; School of Medical Sciences, Faculty of Medicine, University of New South Wales, Sydney, AustraliaThe Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia; Department of Medical Biology, University of Melbourne, Melbourne, AustraliaChildren's Cancer Research Unit, The Children's Hospital at Westmead, Sydney, AustraliaSchool of Medical Sciences, Faculty of Medicine, University of New South Wales, Sydney, Australia; The Kirby Institute for Infection and Immunity in Society, UNSW, Sydney, AustraliaSchool of Medical Sciences, Faculty of Medicine, University of New South Wales, Sydney, Australia; Neuroscience Research Australia (NeuRA), Randwick, AustraliaDepartment of Statistics and Actuarial Science, University of Waterloo, Waterloo, CanadaChildren's Cancer Research Unit, The Children's Hospital at Westmead, Sydney, Australia; Discipline of Child and Adolescent Health, University of Sydney, Sydney, AustraliaChildren's Cancer Research Unit, The Children's Hospital at Westmead, Sydney, Australia; Discipline of Child and Adolescent Health, University of Sydney, Sydney, AustraliaBiofab3D, St. Vincent’s Hospital, Melbourne, Australia; Institute for Innovation in Mental and Physical Health and Clinical Translation (iMPACT), School of Medicine, Deakin University, Victoria, AustraliaBiofab3D, St. Vincent’s Hospital, Melbourne, Australia; Advanced Biomaterials Lab, Research School of Engineering, ANU, Canberra, AustraliaChildren's Cancer Research Unit, The Children's Hospital at Westmead, Sydney, AustraliaThe Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia; Department of Medical Biology, University of Melbourne, Melbourne, AustraliaSchool of Medical Sciences, Faculty of Medicine, University of New South Wales, Sydney, Australia; The Kirby Institute for Infection and Immunity in Society, UNSW, Sydney, AustraliaSchool of Computer Science, Westmead Initiative, and Charles Perkins Centre, University of Sydney, Sydney, AustraliaEMBL Australia, Single Molecule Science node, University of New South Wales, Sydney, Australia; School of Medical Sciences, Faculty of Medicine, University of New South Wales, Sydney, AustraliaCytotoxic T lymphocytes (CTLs) are thought to arrive at target sites either via random search or following signals by other leukocytes. Here, we reveal independent emergent behaviour in CTL populations attacking tumour masses. Primary murine CTLs coordinate their migration in a process reminiscent of the swarming observed in neutrophils. CTLs engaging cognate targets accelerate the recruitment of distant T cells through long-range homotypic signalling, in part mediated via the diffusion of chemokines CCL3 and CCL4. Newly arriving CTLs augment the chemotactic signal, further accelerating mass recruitment in a positive feedback loop. Activated effector human T cells and chimeric antigen receptor (CAR) T cells similarly employ intra-population signalling to drive rapid convergence. Thus, CTLs recognising a cognate target can induce a localised mass response by amplifying the direct recruitment of additional T cells independently of other leukocytes.https://elifesciences.org/articles/56554T cellsswarmingemergent behaviourchemotaxiscell migrationsimulations |
| spellingShingle | Jorge Luis Galeano Niño Sophie V Pageon Szun S Tay Feyza Colakoglu Daryan Kempe Jack Hywood Jessica K Mazalo James Cremasco Matt A Govendir Laura F Dagley Kenneth Hsu Simone Rizzetto Jerzy Zieba Gregory Rice Victoria Prior Geraldine M O'Neill Richard J Williams David R Nisbet Belinda Kramer Andrew I Webb Fabio Luciani Mark N Read Maté Biro Cytotoxic T cells swarm by homotypic chemokine signalling eLife T cells swarming emergent behaviour chemotaxis cell migration simulations |
| title | Cytotoxic T cells swarm by homotypic chemokine signalling |
| title_full | Cytotoxic T cells swarm by homotypic chemokine signalling |
| title_fullStr | Cytotoxic T cells swarm by homotypic chemokine signalling |
| title_full_unstemmed | Cytotoxic T cells swarm by homotypic chemokine signalling |
| title_short | Cytotoxic T cells swarm by homotypic chemokine signalling |
| title_sort | cytotoxic t cells swarm by homotypic chemokine signalling |
| topic | T cells swarming emergent behaviour chemotaxis cell migration simulations |
| url | https://elifesciences.org/articles/56554 |
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