Piezo1 expression in neutrophils regulates shear-induced NETosis.
Neutrophils
/ metabolism
Ion Channels
/ metabolism
Humans
Extracellular Traps
/ metabolism
Stress, Mechanical
Calcium
/ metabolism
Mechanotransduction, Cellular
Adenosine Triphosphate
/ metabolism
Calpain
/ metabolism
Lipopolysaccharides
/ pharmacology
Cytoskeleton
/ metabolism
Neutrophil Infiltration
Inflammation
/ metabolism
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
22 Aug 2024
22 Aug 2024
Historique:
received:
13
07
2023
accepted:
31
07
2024
medline:
23
8
2024
pubmed:
23
8
2024
entrez:
22
8
2024
Statut:
epublish
Résumé
Neutrophil infiltration and subsequent extracellular trap formation (NETosis) is a contributing factor in sterile inflammation. Furthermore, neutrophil extracellular traps (NETs) are prothrombotic, as they provide a scaffold for platelets and red blood cells to attach to. In circulation, neutrophils are constantly exposed to hemodynamic forces such as shear stress, which in turn regulates many of their biological functions such as crawling and NETosis. However, the mechanisms that mediate mechanotransduction in neutrophils are not fully understood. In this study, we demonstrate that shear stress induces NETosis, dependent on the shear stress level, and increases the sensitivity of neutrophils to NETosis-inducing agents such as adenosine triphosphate and lipopolysaccharides. Furthermore, shear stress increases intracellular calcium levels in neutrophils and this process is mediated by the mechanosensitive ion channel Piezo1. Activation of Piezo1 in response to shear stress mediates calpain activity and cytoskeleton remodeling, which consequently induces NETosis. Thus, activation of Piezo1 in response to shear stress leads to a stepwise sequence of cellular events that mediates NETosis and thereby places neutrophils at the centre of localized inflammation and prothrombotic effects.
Identifiants
pubmed: 39174529
doi: 10.1038/s41467-024-51211-1
pii: 10.1038/s41467-024-51211-1
doi:
Substances chimiques
Ion Channels
0
PIEZO1 protein, human
0
Calcium
SY7Q814VUP
Adenosine Triphosphate
8L70Q75FXE
Calpain
EC 3.4.22.-
Lipopolysaccharides
0
Piezo1 protein, mouse
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
7023Subventions
Organisme : Department of Health | National Health and Medical Research Council (NHMRC)
ID : GNT2020197
Organisme : Department of Health | National Health and Medical Research Council (NHMRC)
ID : GNT1174098
Organisme : Department of Education and Training | Australian Research Council (ARC)
ID : LP190100728
Informations de copyright
© 2024. The Author(s).
Références
Mayadas, T. N., Cullere, X. & Lowell, C. A. The multifaceted functions of neutrophils. Annu. Rev. Pathol. 9, 181–218 (2014).
pubmed: 24050624
doi: 10.1146/annurev-pathol-020712-164023
Döring, Y., Soehnlein, O. & Weber, C. Neutrophils Cast NETs in Atherosclerosis. Circ. Res. 114, 931–934 (2014).
pubmed: 24625721
doi: 10.1161/CIRCRESAHA.114.303479
Castanheira, F. V. S. & Kubes, P. Neutrophils and NETs in modulating acute and chronic inflammation. Blood 133, 2178–2185 (2019).
pubmed: 30898862
doi: 10.1182/blood-2018-11-844530
Coughlin, M. F. & Schmid-Schönbein, G. W. Pseudopod projection and cell spreading of passive leukocytes in response to fluid shear stress. Biophys. J. 87, 2035–2042 (2004).
pubmed: 15345579
pmcid: 1304606
doi: 10.1529/biophysj.104.042192
Fukuda, S. et al. Mechanisms for regulation of fluid shear stress response in circulating leukocytes. Circ. Res 86, E13–E18 (2000).
pubmed: 10625314
doi: 10.1161/01.RES.86.1.e13
Mitchell, M. J., Lin, K. S. & King, M. R. Fluid shear stress increases neutrophil activation via platelet-activating factor. Biophys. J. 106, 2243–2253 (2014).
pubmed: 24853753
pmcid: 4052238
doi: 10.1016/j.bpj.2014.04.001
Papayannopoulos, V. Neutrophil extracellular traps in immunity and disease. Nat. Rev. Immunol. 18, 134–147 (2018).
pubmed: 28990587
doi: 10.1038/nri.2017.105
Noubouossie, D. F. et al. In vitro activation of coagulation by human neutrophil DNA and histone proteins but not neutrophil extracellular traps. Blood 129, 1021–1029 (2017).
pubmed: 27919911
pmcid: 5324715
doi: 10.1182/blood-2016-06-722298
Maugeri, N. et al. Activated platelets present high mobility group box 1 to neutrophils, inducing autophagy and promoting the extrusion of neutrophil extracellular traps. J. Thromb. Haemost. 12, 2074–2088 (2014).
pubmed: 25163512
doi: 10.1111/jth.12710
Mangold, A. et al. Coronary neutrophil extracellular trap burden and deoxyribonuclease activity in ST-elevation acute coronary syndrome are predictors of ST-segment resolution and infarct size. Circ. Res. 116, 1182–1192 (2015).
pubmed: 25547404
doi: 10.1161/CIRCRESAHA.116.304944
von Brühl, M. L. et al. Monocytes, neutrophils, and platelets cooperate to initiate and propagate venous thrombosis in mice in vivo. J. Exp. Med. 209, 819–835 (2012).
doi: 10.1084/jem.20112322
Stark, K. et al. Disulfide HMGB1 derived from platelets coordinates venous thrombosis in mice. Blood 128, 2435–2449 (2016).
pubmed: 27574188
pmcid: 5147023
doi: 10.1182/blood-2016-04-710632
Clark, S. R. et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat. Med. 13, 463–469 (2007).
pubmed: 17384648
doi: 10.1038/nm1565
Kessenbrock, K. et al. Netting neutrophils in autoimmune small-vessel vasculitis. Nat. Med. 15, 623–625 (2009).
pubmed: 19448636
pmcid: 2760083
doi: 10.1038/nm.1959
Yipp, B. G. & Kubes, P. NETosis: how vital is it? Blood 122, 2784–2794 (2013).
pubmed: 24009232
doi: 10.1182/blood-2013-04-457671
Yipp, B. G. et al. Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat. Med 18, 1386–1393 (2012).
pubmed: 22922410
pmcid: 4529131
doi: 10.1038/nm.2847
Douda, D. N. et al. SK3 channel and mitochondrial ROS mediate NADPH oxidase-independent NETosis induced by calcium influx. Proc. Natl Acad. Sci. USA 112, 2817–2822 (2015).
pubmed: 25730848
pmcid: 4352781
doi: 10.1073/pnas.1414055112
Vorobjeva, N. V. & Chernyak, B. V. NETosis: Molecular Mechanisms, Role in Physiology and Pathology. Biochem. 85, 1178–1190 (2020).
Yu, X., Tan, J. & Diamond, S. L. Hemodynamic force triggers rapid NETosis within sterile thrombotic occlusions. J. Thromb. Haemost. 16, 316–329 (2018).
pubmed: 29156107
pmcid: 5809303
doi: 10.1111/jth.13907
Abaricia, J. O., Shah, A. H. & Olivares-Navarrete, R. Substrate stiffness induces neutrophil extracellular trap (NET) formation through focal adhesion kinase activation. Biomaterials 271, 120715 (2021).
pubmed: 33677375
pmcid: 8044006
doi: 10.1016/j.biomaterials.2021.120715
Murthy, S. E., Dubin, A. E. & Patapoutian, A. Piezos thrive under pressure: mechanically activated ion channels in health and disease. Nat. Rev. Mol. Cell Biol. 18, 771–783 (2017).
pubmed: 28974772
doi: 10.1038/nrm.2017.92
Li, J. et al. Piezo1 integration of vascular architecture with physiological force. Nature 515, 279–282 (2014).
pubmed: 25119035
pmcid: 4230887
doi: 10.1038/nature13701
Rode, B. et al. Piezo1 channels sense whole body physical activity to reset cardiovascular homeostasis and enhance performance. Nat. Commun. 8, 350 (2017).
pubmed: 28839146
pmcid: 5571199
doi: 10.1038/s41467-017-00429-3
Lai, A. et al. Mechanosensing by Piezo1 and its implications for physiology and various pathologies. Biol. Rev. 97, 604–614 (2022).
pubmed: 34781417
doi: 10.1111/brv.12814
Wang, Y. et al. Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J. Cell Biol. 184, 205–213 (2009).
pubmed: 19153223
pmcid: 2654299
doi: 10.1083/jcb.200806072
Sharda, A., et al. Histone posttranslational modifications: Potential role in diagnosis, prognosis, and therapeutics of cancer. In Prognostic Epigenetics (ed. Sharma, S.) p. 351–373 (Academic Press, 2019)
Perdomo, J. et al. Neutrophil Activation and Netosis Are the Key Drivers of Thrombosis in Heparin-Induced Thrombocytopenia. Blood 132, 378–378 (2018).
doi: 10.1182/blood-2018-99-116421
Thålin, C. et al. Neutrophil Extracellular Traps. Arteriosclerosis, Thrombosis, Vasc. Biol. 39, 1724–1738 (2019).
doi: 10.1161/ATVBAHA.119.312463
Immler, R., Simon, S. I. & Sperandio, M. Calcium signalling and related ion channels in neutrophil recruitment and function. Eur. J. Clin. Investig. 48, e12964–e12964 (2018).
doi: 10.1111/eci.12964
Gottlieb, P. A. & Sachs, F. Piezo1: properties of a cation selective mechanical channel. Channels (Austin) 6, 214–219 (2012).
pubmed: 22790400
doi: 10.4161/chan.21050
Lai, A. et al. Analyzing the shear-induced sensitization of mechanosensitive ion channel Piezo-1 in human aortic endothelial cells. J. Cell. Physiol. 236, 2976–2987 (2021).
pubmed: 32959903
doi: 10.1002/jcp.30056
Baratchi, S. et al. Transcatheter Aortic Valve Implantation Represents an Anti-Inflammatory Therapy Via Reduction of Shear Stress–Induced, Piezo-1–Mediated Monocyte Activation. Circulation 142, 1092–1105 (2020).
pubmed: 32697107
doi: 10.1161/CIRCULATIONAHA.120.045536
Baratchi, S. et al. Shear stress mediates exocytosis of functional TRPV4 channels in endothelial cells. Cell. Mol. Life Sci. 73, 649–666 (2016).
pubmed: 26289129
doi: 10.1007/s00018-015-2018-8
Baratchi, S., et al. The TRPV4 Agonist GSK1016790A Regulates the Membrane Expression of TRPV4 Channels. Front. Pharmacol. 10, 6 (2019)
Gößwein, S. et al. Citrullination Licenses Calpain to Decondense Nuclei in Neutrophil Extracellular Trap Formation. Front Immunol. 10, 2481 (2019).
pubmed: 31695698
pmcid: 6817590
doi: 10.3389/fimmu.2019.02481
McCracken, J. M. & Allen, L. A. Regulation of human neutrophil apoptosis and lifespan in health and disease. J. Cell Death 7, 15–23 (2014).
pubmed: 25278783
pmcid: 4167320
doi: 10.4137/JCD.S11038
Solis, A. G. et al. Mechanosensation of cyclical force by PIEZO1 is essential for innate immunity. Nature 573, 69–74 (2019).
pubmed: 31435009
pmcid: 6939392
doi: 10.1038/s41586-019-1485-8
Collins, S. J., Gallo, R. C. & Gallagher, R. E. Continuous growth and differentiation of human myeloid leukaemic cells in suspension culture. Nature 270, 347–349 (1977).
pubmed: 271272
doi: 10.1038/270347a0
Neeli, I. et al. Regulation of extracellular chromatin release from neutrophils. J. Innate Immun. 1, 194–201 (2009).
pubmed: 20375577
pmcid: 6951038
doi: 10.1159/000206974
Sprenkeler, E. G. G. et al. Formation of neutrophil extracellular traps requires actin cytoskeleton rearrangements. Blood 139, 3166–3180 (2022).
pubmed: 35030250
doi: 10.1182/blood.2021013565
Palmer, L. J. et al. Hypochlorous acid regulates neutrophil extracellular trap release in humans. Clin. Exp. Immunol. 167, 261–268 (2012).
pubmed: 22236002
pmcid: 3278692
doi: 10.1111/j.1365-2249.2011.04518.x
Yoo, D. G. et al. Release of cystic fibrosis airway inflammatory markers from Pseudomonas aeruginosa-stimulated human neutrophils involves NADPH oxidase-dependent extracellular DNA trap formation. J. Immunol. 192, 4728–4738 (2014).
pubmed: 24740504
doi: 10.4049/jimmunol.1301589
Kaplan, M. J. & Radic, M. Neutrophil extracellular traps: double-edged swords of innate immunity. J. Immunol. 189, 2689–2695 (2012).
pubmed: 22956760
doi: 10.4049/jimmunol.1201719
Garcia-Romo, G. S. et al. Netting Neutrophils Are Major Inducers of Type I IFN Production in Pediatric Systemic Lupus Erythematosus. Sci. Transl. Med. 3, 73ra20–73ra20 (2011).
pubmed: 21389264
pmcid: 3143837
doi: 10.1126/scitranslmed.3001201
Lande, R., et al. Neutrophils Activate Plasmacytoid Dendritic Cells by Releasing Self-DNA–Peptide Complexes in Systemic Lupus Erythematosus. Sci. Transl. Med. 3, 73ra19-73ra19 (2011).
Brill, A. et al. Neutrophil extracellular traps promote deep vein thrombosis in mice. J. Thrombosis Haemost. 10, 136–144 (2012).
doi: 10.1111/j.1538-7836.2011.04544.x
Fuchs, T. A. et al. Extracellular DNA traps promote thrombosis. Proc. Natl Acad. Sci. 107, 15880–15885 (2010).
pubmed: 20798043
pmcid: 2936604
doi: 10.1073/pnas.1005743107
Martinac, B. Mechanosensitive ion channels: molecules of mechanotransduction. J. Cell Sci. 117, 2449–2460 (2004).
pubmed: 15159450
doi: 10.1242/jcs.01232
Dunn, J. & Grider, M. H. Physiology, Adenosine Triphosphate. In StatPearls (StatPearls Publishing, 2022).
Elliott, M. R. et al. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 461, 282–286 (2009).
pubmed: 19741708
pmcid: 2851546
doi: 10.1038/nature08296
la Sala, A. et al. Alerting and tuning the immune response by extracellular nucleotides. J. Leukoc. Biol. 73, 339–343 (2003).
pubmed: 12629147
doi: 10.1189/jlb.0802418
Carminita, E. et al. DNAse-dependent, NET-independent pathway of thrombus formation in vivo. Proc. Natl Acad. Sci. 118, e2100561118 (2021).
pubmed: 34260389
pmcid: 8285961
doi: 10.1073/pnas.2100561118
Pieterse, E. et al. Neutrophils Discriminate between Lipopolysaccharides of Different Bacterial Sources and Selectively Release Neutrophil Extracellular Traps. Front. Immunol. 7, 484 (2016).
pubmed: 27867387
pmcid: 5095130
doi: 10.3389/fimmu.2016.00484
Khan, M. A. et al. JNK Activation Turns on LPS- and Gram-Negative Bacteria-Induced NADPH Oxidase-Dependent Suicidal NETosis. Sci. Rep. 7, 3409 (2017).
pubmed: 28611461
pmcid: 5469795
doi: 10.1038/s41598-017-03257-z
Etulain, J. et al. P-selectin promotes neutrophil extracellular trap formation in mice. Blood 126, 242–246 (2015).
pubmed: 25979951
pmcid: 4497964
doi: 10.1182/blood-2015-01-624023
Moschonas, I. C. & Tselepis, A. D. The pathway of neutrophil extracellular traps towards atherosclerosis and thrombosis. Atherosclerosis 288, 9–16 (2019).
pubmed: 31280097
doi: 10.1016/j.atherosclerosis.2019.06.919
Ling, S. & Xu, J. W. NETosis as a Pathogenic Factor for Heart Failure. Oxid. Med. Cell Longev. 2021, 6687096 (2021).
pubmed: 33680285
pmcid: 7929675
doi: 10.1155/2021/6687096
Hann, J. et al. Calcium signaling and regulation of neutrophil functions: Still a long way to go. J. Leukoc. Biol. 107, 285–297 (2020).
pubmed: 31841231
doi: 10.1002/JLB.3RU0719-241R
Lecut, C. et al. P2X1 ion channels promote neutrophil chemotaxis through Rho kinase activation. J. Immunol. 183, 2801–2809 (2009).
pubmed: 19635923
doi: 10.4049/jimmunol.0804007
Lindemann, O. et al. TRPC1 regulates fMLP-stimulated migration and chemotaxis of neutrophil granulocytes. Biochim. Biophys. Acta 1853, 2122–2130 (2015).
pubmed: 25595528
doi: 10.1016/j.bbamcr.2014.12.037
Heiner, I. et al. Expression profile of the transient receptor potential (TRP) family in neutrophil granulocytes: evidence for currents through long TRP channel 2 induced by ADP-ribose and NAD. Biochem J. 371, 1045–1053 (2003).
pubmed: 12564954
pmcid: 1223343
doi: 10.1042/bj20021975
Di Virgilio, F. et al. The P2X7 Receptor in Infection and Inflammation. Immunity 47, 15–31 (2017).
pubmed: 28723547
doi: 10.1016/j.immuni.2017.06.020
Guo, Y. R. & MacKinnon, R. Structure-based membrane dome mechanism for Piezo mechanosensitivity. eLife 6, e33660 (2017).
pubmed: 29231809
pmcid: 5788504
doi: 10.7554/eLife.33660
Yang, X. et al. Structure deformation and curvature sensing of PIEZO1 in lipid membranes. Nature 604, 377–383 (2022).
pubmed: 35388220
doi: 10.1038/s41586-022-04574-8
Lin, Y.-C. et al. Force-induced conformational changes in PIEZO1. Nature 573, 230–234 (2019).
pubmed: 31435018
pmcid: 7258172
doi: 10.1038/s41586-019-1499-2
Haselwandter, C. A. & MacKinnon, R. Piezo’s membrane footprint and its contribution to mechanosensitivity. eLife 7, e41968 (2018).
pubmed: 30480546
pmcid: 6317911
doi: 10.7554/eLife.41968
Yang, S. et al. Membrane curvature governs the distribution of Piezo1 in live cells. Nat. Commun. 13, 7467 (2022).
pubmed: 36463216
pmcid: 9719557
doi: 10.1038/s41467-022-35034-6
Thiam, H. R. et al. NETosis proceeds by cytoskeleton and endomembrane disassembly and PAD4-mediated chromatin decondensation and nuclear envelope rupture. Proc. Natl Acad. Sci. 117, 7326–7337 (2020).
pubmed: 32170015
pmcid: 7132277
doi: 10.1073/pnas.1909546117
Cong, J. et al. The role of autolysis in activity of the Ca2+-dependent proteinases (mu-calpain and m-calpain). J. Biol. Chem. 264, 10096–10103 (1989).
pubmed: 2542320
doi: 10.1016/S0021-9258(18)81771-9
Metzler, K. D. et al. A myeloperoxidase-containing complex regulates neutrophil elastase release and actin dynamics during NETosis. Cell Rep. 8, 883–896 (2014).
pubmed: 25066128
pmcid: 4471680
doi: 10.1016/j.celrep.2014.06.044