β2-Integrin Adhesive Bond Tension under Shear Stress Modulates Cytosolic Calcium Flux and Neutrophil Inflammatory Response
On arrested neutrophils a focal adhesive cluster of ~200 high affinity (HA) β2-integrin bonds under tension is sufficient to trigger Ca2+ flux that signals an increase in activation in direct proportion to increments in shear stress. We reasoned that a threshold tension acting on individual β2-integ...
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Published in | Cells (Basel, Switzerland) Vol. 11; no. 18; p. 2822 |
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Main Authors | , , , , , , |
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Language | English |
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Abstract | On arrested neutrophils a focal adhesive cluster of ~200 high affinity (HA) β2-integrin bonds under tension is sufficient to trigger Ca2+ flux that signals an increase in activation in direct proportion to increments in shear stress. We reasoned that a threshold tension acting on individual β2-integrin bonds provides a mechanical means of transducing the magnitude of fluid drag force into signals that enhance the efficiency of neutrophil recruitment and effector function. Tension gauge tethers (TGT) are a duplex of DNA nucleotides that rupture at a precise shear force, which increases with the extent of nucleotide overlap, ranging from a tolerance of 54pN to 12pN. TGT annealed to a substrate captures neutrophils via allosteric antibodies that stabilize LFA-1 in a high- or low-affinity conformation. Neutrophils sheared on TGT substrates were recorded in real time to form HA β2-integrin bonds and flux cytosolic Ca2+, which elicited shape change and downstream production of reactive oxygen species. A threshold force of 33pN triggered consolidation of HA β2-integrin bonds and triggered membrane influx of Ca2+, whereas an optimum tension of 54pN efficiently transduced activation at a level equivalent to chemotactic stimulation on ICAM-1. We conclude that neutrophils sense the level of fluid drag transduced through individual β2-integrin bonds, providing an intrinsic means to modulate inflammatory response in the microcirculation. |
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AbstractList | On arrested neutrophils a focal adhesive cluster of ~200 high affinity (HA) β
2
-integrin bonds under tension is sufficient to trigger Ca
2+
flux that signals an increase in activation in direct proportion to increments in shear stress. We reasoned that a threshold tension acting on individual β
2
-integrin bonds provides a mechanical means of transducing the magnitude of fluid drag force into signals that enhance the efficiency of neutrophil recruitment and effector function. Tension gauge tethers (TGT) are a duplex of DNA nucleotides that rupture at a precise shear force, which increases with the extent of nucleotide overlap, ranging from a tolerance of 54pN to 12pN. TGT annealed to a substrate captures neutrophils via allosteric antibodies that stabilize LFA-1 in a high- or low-affinity conformation. Neutrophils sheared on TGT substrates were recorded in real time to form HA β
2
-integrin bonds and flux cytosolic Ca
2+
, which elicited shape change and downstream production of reactive oxygen species. A threshold force of 33pN triggered consolidation of HA β
2
-integrin bonds and triggered membrane influx of Ca
2+
, whereas an optimum tension of 54pN efficiently transduced activation at a level equivalent to chemotactic stimulation on ICAM-1. We conclude that neutrophils sense the level of fluid drag transduced through individual β
2
-integrin bonds, providing an intrinsic means to modulate inflammatory response in the microcirculation. On arrested neutrophils a focal adhesive cluster of ~200 high affinity (HA) β2-integrin bonds under tension is sufficient to trigger Ca2+ flux that signals an increase in activation in direct proportion to increments in shear stress. We reasoned that a threshold tension acting on individual β2-integrin bonds provides a mechanical means of transducing the magnitude of fluid drag force into signals that enhance the efficiency of neutrophil recruitment and effector function. Tension gauge tethers (TGT) are a duplex of DNA nucleotides that rupture at a precise shear force, which increases with the extent of nucleotide overlap, ranging from a tolerance of 54pN to 12pN. TGT annealed to a substrate captures neutrophils via allosteric antibodies that stabilize LFA-1 in a high- or low-affinity conformation. Neutrophils sheared on TGT substrates were recorded in real time to form HA β2-integrin bonds and flux cytosolic Ca2+, which elicited shape change and downstream production of reactive oxygen species. A threshold force of 33pN triggered consolidation of HA β2-integrin bonds and triggered membrane influx of Ca2+, whereas an optimum tension of 54pN efficiently transduced activation at a level equivalent to chemotactic stimulation on ICAM-1. We conclude that neutrophils sense the level of fluid drag transduced through individual β2-integrin bonds, providing an intrinsic means to modulate inflammatory response in the microcirculation. |
Author | Ha, Taekjip Madigan, Julianna Werba, Lisette Caroline Jo, Myung Hyun Chen, Szu Jung Morikis, Vasilios Aris Simon, Scott Irwin |
AuthorAffiliation | 2 Department of Biophysics & Biophysical Chemistry, Baltimore, MD 21218, USA 1 Department of Biomedical Engineering, University of California-Davis, Davis, CA 95616, USA 3 Biomedical Engineering, Johns Hopkins University, Baltimore, MD 21218, USA |
AuthorAffiliation_xml | – name: 2 Department of Biophysics & Biophysical Chemistry, Baltimore, MD 21218, USA – name: 3 Biomedical Engineering, Johns Hopkins University, Baltimore, MD 21218, USA – name: 1 Department of Biomedical Engineering, University of California-Davis, Davis, CA 95616, USA |
Author_xml | – sequence: 1 givenname: Vasilios Aris surname: Morikis fullname: Morikis, Vasilios Aris – sequence: 2 givenname: Szu Jung surname: Chen fullname: Chen, Szu Jung – sequence: 3 givenname: Julianna surname: Madigan fullname: Madigan, Julianna – sequence: 4 givenname: Myung Hyun orcidid: 0000-0003-2745-2843 surname: Jo fullname: Jo, Myung Hyun – sequence: 5 givenname: Lisette Caroline surname: Werba fullname: Werba, Lisette Caroline – sequence: 6 givenname: Taekjip surname: Ha fullname: Ha, Taekjip – sequence: 7 givenname: Scott Irwin orcidid: 0000-0003-1186-6611 surname: Simon fullname: Simon, Scott Irwin |
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Snippet | On arrested neutrophils a focal adhesive cluster of ~200 high affinity (HA) β2-integrin bonds under tension is sufficient to trigger Ca2+ flux that signals an... On arrested neutrophils a focal adhesive cluster of ~200 high affinity (HA) β 2 -integrin bonds under tension is sufficient to trigger Ca 2+ flux that signals... |
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StartPage | 2822 |
SubjectTerms | Affinity Allosteric properties Antibodies Calcium influx Calcium signalling Conformation Cooperation Glass substrates Immunological tolerance Inflammation Intercellular adhesion molecule 1 Leukocytes (neutrophilic) LFA-1 antigen Mechanical stimuli Neutrophils Nucleotides Proteins Reactive oxygen species Shear stress T cell receptors tension gauge tethers β2-integrin |
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Title | β2-Integrin Adhesive Bond Tension under Shear Stress Modulates Cytosolic Calcium Flux and Neutrophil Inflammatory Response |
URI | https://www.proquest.com/docview/2716512568 https://search.proquest.com/docview/2717682954 https://pubmed.ncbi.nlm.nih.gov/PMC9497066 https://doaj.org/article/1dacf4bafe904297ad311c81964bada6 |
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