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Adhesion to laminin-1 and collagen IV induces the formation of Ca2+ microdomains that sensitize mouse T cells for activation

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Adhesion to laminin-1 and collagen IV induces the formation of Ca2+ microdomains that sensitize mouse T cells for activation. / Weiß, Mariella; Hernandez, Lola C; Gil Montoya, Diana C; Löhndorf, Anke; Krüger, Aileen; Kopdag, Miriam; Uebler, Liana; Landwehr, Marie; Nawrocki, Mikolaj; Huber, Samuel; Woelk, Lena-Marie; Werner, René; Failla, Antonio V; Flügel, Alexander; Dupont, Geneviève; Guse, Andreas H; Diercks, Björn-Philipp.

In: SCIENCE SIGNALING, Vol. 16, No. 790, 20.06.2023, p. eabn9405.

Research output: SCORING: Contribution to journal › SCORING: Journal article › Research › peer-review

Harvard

Weiß, M, Hernandez, LC, Gil Montoya, DC, Löhndorf, A, Krüger, A, Kopdag, M, Uebler, L, Landwehr, M, Nawrocki, M, Huber, S, Woelk, L-M, Werner, R, Failla, AV, Flügel, A, Dupont, G, Guse, AH & Diercks, B-P 2023, 'Adhesion to laminin-1 and collagen IV induces the formation of Ca2+ microdomains that sensitize mouse T cells for activation', SCIENCE SIGNALING, vol. 16, no. 790, pp. eabn9405. https://doi.org/10.1126/scisignal.abn9405

APA

Weiß, M., Hernandez, L. C., Gil Montoya, D. C., Löhndorf, A., Krüger, A., Kopdag, M., Uebler, L., Landwehr, M., Nawrocki, M., Huber, S., Woelk, L-M., Werner, R., Failla, A. V., Flügel, A., Dupont, G., Guse, A. H., & Diercks, B-P. (2023). Adhesion to laminin-1 and collagen IV induces the formation of Ca2+ microdomains that sensitize mouse T cells for activation. SCIENCE SIGNALING, 16(790), eabn9405. https://doi.org/10.1126/scisignal.abn9405

Vancouver

Weiß M, Hernandez LC, Gil Montoya DC, Löhndorf A, Krüger A, Kopdag M et al. Adhesion to laminin-1 and collagen IV induces the formation of Ca2+ microdomains that sensitize mouse T cells for activation. SCIENCE SIGNALING. 2023 Jun 20;16(790):eabn9405. https://doi.org/10.1126/scisignal.abn9405

Bibtex

@article{1602116faa444433a52a3b98da179214,
title = "Adhesion to laminin-1 and collagen IV induces the formation of Ca2+ microdomains that sensitize mouse T cells for activation",
abstract = "During an immune response, T cells migrate from blood vessel walls into inflamed tissues by migrating across the endothelium and through extracellular matrix (ECM). Integrins facilitate T cell binding to endothelial cells and ECM proteins. Here, we report that Ca2+ microdomains observed in the absence of T cell receptor (TCR)/CD3 stimulation are initial signaling events triggered by adhesion to ECM proteins that increase the sensitivity of primary murine T cells to activation. Adhesion to the ECM proteins collagen IV and laminin-1 increased the number of Ca2+ microdomains in a manner dependent on the kinase FAK, phospholipase C (PLC), and all three inositol 1,4,5-trisphosphate receptor (IP3R) subtypes and promoted the nuclear translocation of the transcription factor NFAT-1. Mathematical modeling predicted that the formation of adhesion-dependent Ca2+ microdomains required the concerted activity of two to six IP3Rs and ORAI1 channels to achieve the increase in the Ca2+ concentration in the ER-plasma membrane junction that was observed experimentally and that required SOCE. Further, adhesion-dependent Ca2+ microdomains were important for the magnitude of the TCR-induced activation of T cells on collagen IV as assessed by the global Ca2+ response and NFAT-1 nuclear translocation. Thus, adhesion to collagen IV and laminin-1 sensitizes T cells through a mechanism involving the formation of Ca2+ microdomains, and blocking this low-level sensitization decreases T cell activation upon TCR engagement.",
keywords = "Mice, Animals, Endothelial Cells, Extracellular Matrix Proteins/metabolism, T-Lymphocytes/metabolism, Receptors, Antigen, T-Cell/metabolism, Collagen/metabolism",
author = "Mariella Wei{\ss} and Hernandez, {Lola C} and {Gil Montoya}, {Diana C} and Anke L{\"o}hndorf and Aileen Kr{\"u}ger and Miriam Kopdag and Liana Uebler and Marie Landwehr and Mikolaj Nawrocki and Samuel Huber and Lena-Marie Woelk and Ren{\'e} Werner and Failla, {Antonio V} and Alexander Fl{\"u}gel and Genevi{\`e}ve Dupont and Guse, {Andreas H} and Bj{\"o}rn-Philipp Diercks",
year = "2023",
month = jun,
day = "20",
doi = "10.1126/scisignal.abn9405",
language = "English",
volume = "16",
pages = "eabn9405",
journal = "SCI SIGNAL",
issn = "1945-0877",
publisher = "American Association for the Advancement of Science",
number = "790",

}

RIS

TY - JOUR

T1 - Adhesion to laminin-1 and collagen IV induces the formation of Ca2+ microdomains that sensitize mouse T cells for activation

AU - Weiß, Mariella

AU - Hernandez, Lola C

AU - Gil Montoya, Diana C

AU - Löhndorf, Anke

AU - Krüger, Aileen

AU - Kopdag, Miriam

AU - Uebler, Liana

AU - Landwehr, Marie

AU - Nawrocki, Mikolaj

AU - Huber, Samuel

AU - Woelk, Lena-Marie

AU - Werner, René

AU - Failla, Antonio V

AU - Flügel, Alexander

AU - Dupont, Geneviève

AU - Guse, Andreas H

AU - Diercks, Björn-Philipp

PY - 2023/6/20

Y1 - 2023/6/20

N2 - During an immune response, T cells migrate from blood vessel walls into inflamed tissues by migrating across the endothelium and through extracellular matrix (ECM). Integrins facilitate T cell binding to endothelial cells and ECM proteins. Here, we report that Ca2+ microdomains observed in the absence of T cell receptor (TCR)/CD3 stimulation are initial signaling events triggered by adhesion to ECM proteins that increase the sensitivity of primary murine T cells to activation. Adhesion to the ECM proteins collagen IV and laminin-1 increased the number of Ca2+ microdomains in a manner dependent on the kinase FAK, phospholipase C (PLC), and all three inositol 1,4,5-trisphosphate receptor (IP3R) subtypes and promoted the nuclear translocation of the transcription factor NFAT-1. Mathematical modeling predicted that the formation of adhesion-dependent Ca2+ microdomains required the concerted activity of two to six IP3Rs and ORAI1 channels to achieve the increase in the Ca2+ concentration in the ER-plasma membrane junction that was observed experimentally and that required SOCE. Further, adhesion-dependent Ca2+ microdomains were important for the magnitude of the TCR-induced activation of T cells on collagen IV as assessed by the global Ca2+ response and NFAT-1 nuclear translocation. Thus, adhesion to collagen IV and laminin-1 sensitizes T cells through a mechanism involving the formation of Ca2+ microdomains, and blocking this low-level sensitization decreases T cell activation upon TCR engagement.

AB - During an immune response, T cells migrate from blood vessel walls into inflamed tissues by migrating across the endothelium and through extracellular matrix (ECM). Integrins facilitate T cell binding to endothelial cells and ECM proteins. Here, we report that Ca2+ microdomains observed in the absence of T cell receptor (TCR)/CD3 stimulation are initial signaling events triggered by adhesion to ECM proteins that increase the sensitivity of primary murine T cells to activation. Adhesion to the ECM proteins collagen IV and laminin-1 increased the number of Ca2+ microdomains in a manner dependent on the kinase FAK, phospholipase C (PLC), and all three inositol 1,4,5-trisphosphate receptor (IP3R) subtypes and promoted the nuclear translocation of the transcription factor NFAT-1. Mathematical modeling predicted that the formation of adhesion-dependent Ca2+ microdomains required the concerted activity of two to six IP3Rs and ORAI1 channels to achieve the increase in the Ca2+ concentration in the ER-plasma membrane junction that was observed experimentally and that required SOCE. Further, adhesion-dependent Ca2+ microdomains were important for the magnitude of the TCR-induced activation of T cells on collagen IV as assessed by the global Ca2+ response and NFAT-1 nuclear translocation. Thus, adhesion to collagen IV and laminin-1 sensitizes T cells through a mechanism involving the formation of Ca2+ microdomains, and blocking this low-level sensitization decreases T cell activation upon TCR engagement.

KW - Mice

KW - Animals

KW - Endothelial Cells

KW - Extracellular Matrix Proteins/metabolism

KW - T-Lymphocytes/metabolism

KW - Receptors, Antigen, T-Cell/metabolism

KW - Collagen/metabolism

U2 - 10.1126/scisignal.abn9405

DO - 10.1126/scisignal.abn9405

M3 - SCORING: Journal article

C2 - 37339181

VL - 16

SP - eabn9405

JO - SCI SIGNAL

JF - SCI SIGNAL

SN - 1945-0877

IS - 790

ER -