B cell zone reticular cell microenvironments shape CXCL13 gradient formation
Through the formation of concentration gradients, morphogens drive graded responses to extracellular signals, thereby fine-tuning cell behaviors in complex tissues. Here we show that the chemokine CXCL13 forms both soluble and immobilized gradients. Specifically, CXCL13 + follicular reticular cells...
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| Vydáno v: | Nature communications Ročník 11; číslo 1; s. 3677 - 15 |
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| Hlavní autoři: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
| Vydáno: |
London
Nature Publishing Group UK
22.07.2020
Nature Publishing Group Nature Portfolio |
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| ISSN: | 2041-1723, 2041-1723 |
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| Abstract | Through the formation of concentration gradients, morphogens drive graded responses to extracellular signals, thereby fine-tuning cell behaviors in complex tissues. Here we show that the chemokine CXCL13 forms both soluble and immobilized gradients. Specifically, CXCL13
+
follicular reticular cells form a small-world network of guidance structures, with computer simulations and optimization analysis predicting that immobilized gradients created by this network promote B cell trafficking. Consistent with this prediction, imaging analysis show that CXCL13 binds to extracellular matrix components in situ, constraining its diffusion. CXCL13 solubilization requires the protease cathepsin B that cleaves CXCL13 into a stable product. Mice lacking cathepsin B display aberrant follicular architecture, a phenotype associated with effective B cell homing to but not within lymph nodes. Our data thus suggest that reticular cells of the B cell zone generate microenvironments that shape both immobilized and soluble CXCL13 gradients.
Morphogens such as chemokines form gradients to direct graded responses and modulate cell behaviors. Here the authors show, using imaging and computer simulation, that the chemokine CXCL13 originated from follicular reticular cells in the lymph nodes forms both soluble and immobilized gradients to regulate B cell recruitment and migration. |
|---|---|
| AbstractList | Through the formation of concentration gradients, morphogens drive graded responses to extracellular signals, thereby fine-tuning cell behaviors in complex tissues. Here we show that the chemokine CXCL13 forms both soluble and immobilized gradients. Specifically, CXCL13+ follicular reticular cells form a small-world network of guidance structures, with computer simulations and optimization analysis predicting that immobilized gradients created by this network promote B cell trafficking. Consistent with this prediction, imaging analysis show that CXCL13 binds to extracellular matrix components in situ, constraining its diffusion. CXCL13 solubilization requires the protease cathepsin B that cleaves CXCL13 into a stable product. Mice lacking cathepsin B display aberrant follicular architecture, a phenotype associated with effective B cell homing to but not within lymph nodes. Our data thus suggest that reticular cells of the B cell zone generate microenvironments that shape both immobilized and soluble CXCL13 gradients. Morphogens such as chemokines form gradients to direct graded responses and modulate cell behaviors. Here the authors show, using imaging and computer simulation, that the chemokine CXCL13 originated from follicular reticular cells in the lymph nodes forms both soluble and immobilized gradients to regulate B cell recruitment and migration. Through the formation of concentration gradients, morphogens drive graded responses to extracellular signals, thereby fine-tuning cell behaviors in complex tissues. Here we show that the chemokine CXCL13 forms both soluble and immobilized gradients. Specifically, CXCL13 follicular reticular cells form a small-world network of guidance structures, with computer simulations and optimization analysis predicting that immobilized gradients created by this network promote B cell trafficking. Consistent with this prediction, imaging analysis show that CXCL13 binds to extracellular matrix components in situ, constraining its diffusion. CXCL13 solubilization requires the protease cathepsin B that cleaves CXCL13 into a stable product. Mice lacking cathepsin B display aberrant follicular architecture, a phenotype associated with effective B cell homing to but not within lymph nodes. Our data thus suggest that reticular cells of the B cell zone generate microenvironments that shape both immobilized and soluble CXCL13 gradients. Through the formation of concentration gradients, morphogens drive graded responses to extracellular signals, thereby fine-tuning cell behaviors in complex tissues. Here we show that the chemokine CXCL13 forms both soluble and immobilized gradients. Specifically, CXCL13+ follicular reticular cells form a small-world network of guidance structures, with computer simulations and optimization analysis predicting that immobilized gradients created by this network promote B cell trafficking. Consistent with this prediction, imaging analysis show that CXCL13 binds to extracellular matrix components in situ, constraining its diffusion. CXCL13 solubilization requires the protease cathepsin B that cleaves CXCL13 into a stable product. Mice lacking cathepsin B display aberrant follicular architecture, a phenotype associated with effective B cell homing to but not within lymph nodes. Our data thus suggest that reticular cells of the B cell zone generate microenvironments that shape both immobilized and soluble CXCL13 gradients.Through the formation of concentration gradients, morphogens drive graded responses to extracellular signals, thereby fine-tuning cell behaviors in complex tissues. Here we show that the chemokine CXCL13 forms both soluble and immobilized gradients. Specifically, CXCL13+ follicular reticular cells form a small-world network of guidance structures, with computer simulations and optimization analysis predicting that immobilized gradients created by this network promote B cell trafficking. Consistent with this prediction, imaging analysis show that CXCL13 binds to extracellular matrix components in situ, constraining its diffusion. CXCL13 solubilization requires the protease cathepsin B that cleaves CXCL13 into a stable product. Mice lacking cathepsin B display aberrant follicular architecture, a phenotype associated with effective B cell homing to but not within lymph nodes. Our data thus suggest that reticular cells of the B cell zone generate microenvironments that shape both immobilized and soluble CXCL13 gradients. Through the formation of concentration gradients, morphogens drive graded responses to extracellular signals, thereby fine-tuning cell behaviors in complex tissues. Here we show that the chemokine CXCL13 forms both soluble and immobilized gradients. Specifically, CXCL13 + follicular reticular cells form a small-world network of guidance structures, with computer simulations and optimization analysis predicting that immobilized gradients created by this network promote B cell trafficking. Consistent with this prediction, imaging analysis show that CXCL13 binds to extracellular matrix components in situ, constraining its diffusion. CXCL13 solubilization requires the protease cathepsin B that cleaves CXCL13 into a stable product. Mice lacking cathepsin B display aberrant follicular architecture, a phenotype associated with effective B cell homing to but not within lymph nodes. Our data thus suggest that reticular cells of the B cell zone generate microenvironments that shape both immobilized and soluble CXCL13 gradients. Through the formation of concentration gradients, morphogens drive graded responses to extracellular signals, thereby fine-tuning cell behaviors in complex tissues. Here we show that the chemokine CXCL13 forms both soluble and immobilized gradients. Specifically, CXCL13 + follicular reticular cells form a small-world network of guidance structures, with computer simulations and optimization analysis predicting that immobilized gradients created by this network promote B cell trafficking. Consistent with this prediction, imaging analysis show that CXCL13 binds to extracellular matrix components in situ, constraining its diffusion. CXCL13 solubilization requires the protease cathepsin B that cleaves CXCL13 into a stable product. Mice lacking cathepsin B display aberrant follicular architecture, a phenotype associated with effective B cell homing to but not within lymph nodes. Our data thus suggest that reticular cells of the B cell zone generate microenvironments that shape both immobilized and soluble CXCL13 gradients. Through the formation of concentration gradients, morphogens drive graded responses to extracellular signals, thereby fine-tuning cell behaviors in complex tissues. Here we show that the chemokine CXCL13 forms both soluble and immobilized gradients. Specifically, CXCL13 + follicular reticular cells form a small-world network of guidance structures, with computer simulations and optimization analysis predicting that immobilized gradients created by this network promote B cell trafficking. Consistent with this prediction, imaging analysis show that CXCL13 binds to extracellular matrix components in situ, constraining its diffusion. CXCL13 solubilization requires the protease cathepsin B that cleaves CXCL13 into a stable product. Mice lacking cathepsin B display aberrant follicular architecture, a phenotype associated with effective B cell homing to but not within lymph nodes. Our data thus suggest that reticular cells of the B cell zone generate microenvironments that shape both immobilized and soluble CXCL13 gradients. Morphogens such as chemokines form gradients to direct graded responses and modulate cell behaviors. Here the authors show, using imaging and computer simulation, that the chemokine CXCL13 originated from follicular reticular cells in the lymph nodes forms both soluble and immobilized gradients to regulate B cell recruitment and migration. Morphogens such as chemokines form gradients to direct graded responses and modulate cell behaviors. Here the authors show, using imaging and computer simulation, that the chemokine CXCL13 originated from follicular reticular cells in the lymph nodes forms both soluble and immobilized gradients to regulate B cell recruitment and migration. |
| ArticleNumber | 3677 |
| Author | Mörbe, Urs Pikor, Natalia B. O’Toole, Peter Venetz, Daniel Miller, Helen Stein, Jens V. Novkovic, Mario Taylor, Emily Uguccioni, Mariagrazia Jarrett, Simon Legler, Daniel F. Manoury, Bénedicte Ludewig, Burkhard Albrecht, Stefan Timmis, Jon Leake, Mark C. Zhou, Zhaoukun Cupedo, Tom Heller, Manfred Cupovic, Jovana Thuery, Anne Lacey, Charles J. Alden, Kieran Cosgrove, Jason Polak, Wojciech G. Coles, Mark C. Onder, Lucas Pinter, Rita Thelen, Marcus Coatesworth, Andrew Wolf, Marlene |
| Author_xml | – sequence: 1 givenname: Jason surname: Cosgrove fullname: Cosgrove, Jason organization: York Computational Immunology Lab, University of York, Centre for Immunology and Infection, Department of Biology and Hull York Medical School, University of York, Department of Electronic Engineering, University of York – sequence: 2 givenname: Mario orcidid: 0000-0001-7654-5777 surname: Novkovic fullname: Novkovic, Mario organization: Institute of Immunobiology, Kantonsspital St. Gallen – sequence: 3 givenname: Stefan surname: Albrecht fullname: Albrecht, Stefan organization: Theodor Kocher Institute, University of Bern – sequence: 4 givenname: Natalia B. surname: Pikor fullname: Pikor, Natalia B. organization: Institute of Immunobiology, Kantonsspital St. Gallen – sequence: 5 givenname: Zhaoukun surname: Zhou fullname: Zhou, Zhaoukun organization: Department of Biology, University of York, Biological Physical Sciences Institute (BPSI), University of York, Department of Physics, University of York – sequence: 6 givenname: Lucas surname: Onder fullname: Onder, Lucas organization: Institute of Immunobiology, Kantonsspital St. Gallen – sequence: 7 givenname: Urs surname: Mörbe fullname: Mörbe, Urs organization: Institute of Immunobiology, Kantonsspital St. Gallen – sequence: 8 givenname: Jovana surname: Cupovic fullname: Cupovic, Jovana organization: Institute of Immunobiology, Kantonsspital St. Gallen – sequence: 9 givenname: Helen orcidid: 0000-0001-7076-4151 surname: Miller fullname: Miller, Helen organization: Department of Biology, University of York, Biological Physical Sciences Institute (BPSI), University of York, Department of Physics, University of York – sequence: 10 givenname: Kieran surname: Alden fullname: Alden, Kieran organization: York Computational Immunology Lab, University of York, Department of Electronic Engineering, University of York – sequence: 11 givenname: Anne surname: Thuery fullname: Thuery, Anne organization: Centre for Immunology and Infection, Department of Biology and Hull York Medical School, University of York – sequence: 12 givenname: Peter surname: O’Toole fullname: O’Toole, Peter organization: Department of Biology, University of York – sequence: 13 givenname: Rita surname: Pinter fullname: Pinter, Rita organization: Kennedy Institute of Rheumatology at the University of Oxford – sequence: 14 givenname: Simon surname: Jarrett fullname: Jarrett, Simon organization: Kennedy Institute of Rheumatology at the University of Oxford – sequence: 15 givenname: Emily surname: Taylor fullname: Taylor, Emily organization: Centre for Immunology and Infection, Department of Biology and Hull York Medical School, University of York – sequence: 16 givenname: Daniel surname: Venetz fullname: Venetz, Daniel organization: Institute for Research in Biomedicine, Università della Svizzera italiana – sequence: 17 givenname: Manfred surname: Heller fullname: Heller, Manfred organization: Department of Clinical Research, University of Bern – sequence: 18 givenname: Mariagrazia surname: Uguccioni fullname: Uguccioni, Mariagrazia organization: Institute for Research in Biomedicine, Università della Svizzera italiana – sequence: 19 givenname: Daniel F. orcidid: 0000-0001-8610-4764 surname: Legler fullname: Legler, Daniel F. organization: Biotechnology Institute Thurgau (BITg) at the University of Konstanz – sequence: 20 givenname: Charles J. orcidid: 0000-0001-9250-2638 surname: Lacey fullname: Lacey, Charles J. organization: York Computational Immunology Lab, University of York – sequence: 21 givenname: Andrew surname: Coatesworth fullname: Coatesworth, Andrew organization: York Teaching Hospital NHS Foundation Trust – sequence: 22 givenname: Wojciech G. surname: Polak fullname: Polak, Wojciech G. organization: Department of Surgery, Erasmus University Medical Centre – sequence: 23 givenname: Tom surname: Cupedo fullname: Cupedo, Tom organization: Department of Hematology, Erasmus University Medical Centre – sequence: 24 givenname: Bénedicte surname: Manoury fullname: Manoury, Bénedicte organization: Institut Necker Enfants Malades, INSERM U1151- CNRS UMR 8253, 149 rue de Sèvres 75015 Paris, France Université René Descartes, Université Paris Descartes, Sorbonne Paris Cité – sequence: 25 givenname: Marcus surname: Thelen fullname: Thelen, Marcus organization: Institute for Research in Biomedicine, Università della Svizzera italiana – sequence: 26 givenname: Jens V. orcidid: 0000-0002-8199-9586 surname: Stein fullname: Stein, Jens V. organization: Department of Oncology, Microbiology and Immunology, University of Fribourg – sequence: 27 givenname: Marlene orcidid: 0000-0002-7283-4683 surname: Wolf fullname: Wolf, Marlene organization: Theodor Kocher Institute, University of Bern – sequence: 28 givenname: Mark C. orcidid: 0000-0002-1715-1249 surname: Leake fullname: Leake, Mark C. email: mark.leake@york.ac.uk organization: Department of Biology, University of York, Biological Physical Sciences Institute (BPSI), University of York, Department of Physics, University of York – sequence: 29 givenname: Jon surname: Timmis fullname: Timmis, Jon email: jon.timmis@sunderland.ac.uk organization: York Computational Immunology Lab, University of York, Department of Electronic Engineering, University of York – sequence: 30 givenname: Burkhard orcidid: 0000-0002-7685-573X surname: Ludewig fullname: Ludewig, Burkhard email: burkhard.ludewig@kssg.ch organization: Institute of Immunobiology, Kantonsspital St. Gallen – sequence: 31 givenname: Mark C. surname: Coles fullname: Coles, Mark C. email: mark.coles@kennedy.ox.ac.uk organization: York Computational Immunology Lab, University of York, Kennedy Institute of Rheumatology at the University of Oxford |
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| Title | B cell zone reticular cell microenvironments shape CXCL13 gradient formation |
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