P2X1 Ion Channels Promote Neutrophil Chemotaxis through Rho Kinase Activation

[en] This study shows that activation of P2X1 ion channels by ATP promotes neutrophil chemotaxis, a process involving Rho kinase-dependent actomyosin-mediated contraction at the cell rear. These ion channels may therefore play a significant role in host defense and inflammation.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Lecut, Christelle ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > GIGA-R : Génétique générale et humaine

Frederix, Kim ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > GIGA-R : Génétique générale et humaine

Johnson, Daniel M; Universiteit Maastricht > Cardiology > CARIM

Deroanne, Christophe ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Laboratoire des tissus conjonctifs

Thiry, Marc ; Université de Liège - ULiège > Département des sciences de la vie > Biologie cellulaire

Faccinetto, Céline ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > GIGA-R : Génétique générale et humaine

Marée, Raphaël ; Université de Liège - ULiège > GIGA-Management : Plateforme bioinformatique

Evans, Richard J; University of Leicester > Cell Physiology and Pharmacology

Volders, Paul GA; Universiteit Maastricht > Cardiology > CARIM

Bours, Vincent ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > GIGA-R : Génétique générale et humaine

Oury, Cécile ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > GIGA-R : Génétique générale et humaine

Language :

English

Title :

P2X1 Ion Channels Promote Neutrophil Chemotaxis through Rho Kinase Activation

Publication date :

2009

Journal title :

Journal of Immunology

ISSN :

0022-1767

eISSN :

1550-6606

Publisher :

American Association of Immunologists, Baltimore, United States - Maryland

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 14 September 2009

Statistics

Number of views

155 (21 by ULiège)

Number of downloads

202 (7 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Alves-Filho, J. C., A. de Freitas, F. Spiller, F. O. Souto, and F. Q. Cunha. 2008. The role of neutrophils in severe sepsis. Shock 30(Suppl. 1): 3-9.
Buffon, A., L. M. Biasucci, G. Liuzzo, G. D'Onofrio, F. Crea, and A. Maseri. 2002. Widespread coronary inflammation in unstable angina. N. Engl. J. Med. 347: 5-12.
Wipke, B. T., and P. M. Allen. 2001. Essential role of neutrophils in the initiation and progression of a murine model of rheumatoid arthritis. J. Immunol. 167: 1601-1608.
Stephens, L., L. Milne, and P. Hawkins. 2008. Moving towards a better understanding of chemotaxis. Curr. Biol. 18: R485-R494.
Xu, J., F. Wang, A. Van Keymeulen, P. Herzmark, A. Straight, K. Kelly, Y. Takuwa, N. Sugimoto, T. Mitchison, and H. R. Bourne. 2003. Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell 114: 201-214.
Chen, Y., R. Corriden, Y. Inoue, L. Yip, N. Hashiguchi, A. Zinkernagel, V. Nizet, P. A. Insel, and W. G. Junger. 2006. ATP release guides neutrophil chemotaxis via P2Y2 and A3 receptors. Science 314: 1792-1795.
Lazarowski, E. R., R. C. Boucher, and T. K. Harden. 2003. Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules. Mol. Pharmacol. 64: 785-795.
Ralevic, V., and G. Burnstock. 1998. Receptors for purines and pyrimidines. Pharmacol. Rev. 50: 413-492.
Burnstock, G. 2007. Purine and pyrimidine receptors. Cell Mol. Life Sci. 64: 1471-1483.
North, R. A. 2002. Molecular physiology of P2X receptors. Physiol. Rev. 82: 1013-1067.
Khakh, B. S., and R. A. North. 2006. P2X receptors as cell-surface ATP sensors in health and disease. Nature 442: 527-532.
Gu, B. J., W. Y. Zhang, L. J. Bendall, I. P. Chessell, G. N. Buell, and J. S. Wiley. 2000. Expression of P2X7 purinoceptors on human lymphocytes and monocytes: evidence for nonfunctional P2X7 receptors. Am. J. Physiol. 279: C1189-C1197.
Mohanty, J. G., D. G. Raible, L. J. McDermott, A. Pelleg, and E. S. Schulman. 2001. Effects of purine and pyrimidine nucleotides on intracellular Ca2+ in human eosinophils: activation of purinergic P2Y receptors. J. Allergy Clin. Immunol. 107: 849-855.
Suh, B. C., J. S. Kim, U. Namgung, H. Ha, and K. T. Kim. 2001. P2X7 nucleotide receptor mediation of membrane pore formation and superoxide generation in human promyelocytes and neutrophils. J. Immunol. 166: 6754-6763.
Surprenant, A., and R. A. North. 2009. Signaling at purinergic P2X receptors. Annu. Rev. Physiol. 71: 333-359.
Ferrari, D., C. Pizzirani, E. Adinolfi, R. M. Lemoli, A. Curti, M. Idzko, E. Panther, and F. Di Virgilio. 2006. The P2X7 receptor: a key player in IL-1 processing and release. J. Immunol. 176: 3877-3883. (Pubitemid 44264361)
Bours, M. J., E. L. Swennen, F. Di Virgilio, B. N. Cronstein, and P. C. Dagnelie. 2006. Adenosine 5′-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol. Ther. 112: 358-404.
Taylor, S. R., M. Gonzalez-Begne, S. Dewhurst, G. Chimini, C. F. Higgins, J. E. Melvin, and J. I. Elliott. 2008. Sequential shrinkage and swelling underlie P2X7-stimulated lymphocyte phosphatidylserine exposure and death. J. Immunol. 180: 300-308.
Labasi, J. M., N. Petrushova, C. Donovan, S. McCurdy, P. Lira, M. M. Payette, W. Brissette, J. R. Wicks, L. Audoly, and C. A. Gabel. 2002. Absence of the P2X7 receptor alters leukocyte function and attenuates an inflammatory response. J. Immunol. 168: 6436-6445.
Heiss, K., N. Janner, B. Mahnss, V. Schumacher, F. Koch-Nolte, F. Haag, and H. W. Mittrucker. 2008. High sensitivity of intestinal CD8+ T cells to nucleotides indicates P2X7 as a regulator for intestinal T cell responses. J. Immunol. 181: 3861-3869.
Oury, C., E. Toth-Zsamboki, C. Van Geet, C. Thys, L. Wei, B. Nilius, J. Vermylen, and M. F. Hoylaerts. 2000. A natural dominant negative P2X1 receptor due to deletion of a single amino acid residue. J. Biol. Chem. 275: 22611-22614.
Mulryan, K., D. P. Gitterman, C. J. Lewis, C. Vial, B. J. Leckie, A. L. Cobb, J. E. Brown, E. C. Conley, G. Buell, C. A. Pritchard, and R. J. Evans. 2000. Reduced vas deferens contraction and male infertility in mice lacking P2X1 receptors. Nature 403: 86-89.
Corhay, J. L., L. Hemelaers, M. Henket, J. Sele, and R. Louis. 2007. Granulocyte chemotactic activity in exhaled breath condensate of healthy subjects and patients with COPD. Chest 131: 1672-1677.
Oury, C., M. J. Kuijpers, E. Toth-Zsamboki, A. Bonnefoy, S. Danloy, I. Vreys, M. A. Feijge, R. De Vos, J. Vermylen, J. W. Heemskerk, and M. F. Hoylaerts. 2003. Overexpression of the platelet P2X1 ion channel in transgenic mice generates a novel prothrombotic phenotype. Blood 101: 3969-3976.
Ho, T. T., S. D. Merajver, C. M. Lapiere, B. V. Nusgens, and C. F. Deroanne. 2008. RhoA-GDP regulates RhoB protein stability: potential involvement of RhoGDIα. J. Biol. Chem. 283: 21588-21598.
Toth-Zsamboki, E., C. Oury, H. Cornelissen, R. De Vos, J. Vermylen, and M. F. Hoylaerts. 2003. P2X1-mediated ERK2 activation amplifies the collageni-nduced platelet secretion by enhancing myosin light chain kinase activation. J. Biol. Chem. 278: 46661-46667.
Clifford, E. E., K. Parker, B. D. Humphreys, S. B. Kertesy, and G. R. Dubyak. 1998. The P2X1 receptor, an adenosine triphosphate-gated cation channel, is expressed in human platelets but not in human blood leukocytes. Blood 91: 3172-3181.
Gever, J. R., D. A. Cockayne, M. P. Dillon, G. Burnstock, and A. P. Ford. 2006. Pharmacology of P2X channels. Pflugers Arch. 452: 513-537.
Evans, R. J. 1996. Single channel properties of ATP-gated cation channels (P2X receptors) heterologously expressed in Chinese hamster ovary cells. Neurosci. Lett. 212: 212-214.
Boyden, S. 1962. The chemotactic effect of mixtures of antibody and antigen on polymorphonuclear leukocytes. J. Exp. Med. 115: 453-466.
Ferguson, G. J., L. Milne, S. Kulkarni, T. Sasaki, S. Walker, S. Andrews, T. Crabbe, P. Finan, G. Jones, S. Jackson, et al. 2007. PI3Kγ has an important context-dependent role in neutrophil chemokinesis. Nat. Cell Biol. 9: 86-91.
Pomel, V., J. Klicic, D. Covini, D. D. Church, J. P. Shaw, K. Roulin, F. Burgat-Charvillon, D. Valognes, M. Camps, C. Chabert, et al. 2006. Furan-2-yl methylene thiazolidinediones as novel, potent, and selective inhibitors of phosphoinositide 3-kinase γ. J. Med. Chem. 49: 3857-3871.
Hechler, B., N. Lenain, P. Marchese, C. Vial, V. Heim, M. Freund, J. P. Cazenave, M. Cattaneo, Z. M. Ruggeri, R. Evans, and C. Gachet. 2003. A role of the fast ATP-gated P2X1 cation channel in thrombosis of small arteries in vivo. J. Exp. Med. 198: 661-667.
Gachet, C. 2008. P2 receptors, platelet function and pharmacological implications. Thromb. Haemostasis 99: 466-472.
Longhurst, P. A., T. Schwegel, K. Folander, and R. Swanson. 1996. The human P2x1 receptor: molecular cloning, tissue distribution, and localization to chromosome 17. Biochim. Biophys. Acta 1308: 185-188.
Buell, G., A. D. Michel, C. Lewis, G. Collo, P. P. Humphrey, and A. Surprenant. 1996. P2X1 receptor activation in HL60 cells. Blood 87: 2659-2664.
Sim, J. A., C. K. Park, S. B. Oh, R. J. Evans, and R. A. North. 2007. P2X1 and P2X4 receptor currents in mouse macrophages. Br. J. Pharmacol. 152: 1283-1290.
Verghese, M. W., T. B. Kneisler, and J. A. Boucheron. 1996. P2U agonists induce chemotaxis and actin polymerization in human neutrophils and differentiated HL60 cells. J. Biol. Chem. 271: 15597-15601.
Vial, C., A. B. Tobin, and R. J. Evans. 2004. G-protein-coupled receptor regulation of P2X1 receptors does not involve direct channel phosphorylation. Biochem. J. 382: 101-110.
Nishio, M., K. Watanabe, J. Sasaki, C. Taya, S. Takasuga, R. Iizuka, T. Balla, M. Yamazaki, H. Watanabe, R. Itoh, et al. 2007. Control of cell polarity and motility by the PtdIns(3,4,5)P3 phosphatase SHIP1. Nat. Cell Biol. 9: 36-44.
Herzmark, P., K. Campbell, F. Wang, K. Wong, H. El-Samad, A. Groisman, and H. R. Bourne. 2007. Bound attractant at the leading vs. the trailing edge determines chemotactic prowess. Proc. Natl. Acad. Sci. USA 104: 13349-13354.
Condliffe, A. M., K. Davidson, K. E. Anderson, C. D. Ellson, T. Crabbe, K. Okkenhaug, B. Vanhaesebroeck, M. Turner, L. Webb, M. P. Wymann, et al. 2005. Sequential activation of class IB and class IA PI3K is important for the primed respiratory burst of human but not murine neutrophils. Blood 106: 1432-1440.
Wong, K., O. Pertz, K. Hahn, and H. Bourne. 2006. Neutrophil polarization: spatiotemporal dynamics of RhoA activity support a self-organizing mechanism. Proc. Natl. Acad. Sci. USA 103: 3639-3644.
Van Keymeulen, A., K. Wong, Z. A. Knight, C. Govaerts, K. M. Hahn, K. M. Shokat, and H. R. Bourne. 2006. To stabilize neutrophil polarity, PIP3 and Cdc42 augment RhoA activity at the back as well as signals at the front. J. Cell Biol. 174: 437-445.
Sanchez-Madrid, F., and J. M. Serrador. 2009. Bringing up the rear: defining the roles of the uropod. Nat. Rev. Mol. Cell Biol. 10: 353-359.
Smith, L. A., H. Aranda-Espinoza, J. B. Haun, M. Dembo, and D. A. Hammer. 2007. Neutrophil traction stresses are concentrated in the uropod during migration. Biophys. J. 92: L58-L60.
Laudanna, C., J. J. Campbell, and E. C. Butcher. 1996. Role of Rho in chemoattractant-activated leukocyte adhesion through integrins. Science 271: 981-983. (Pubitemid 26066394)
Alblas, J., L. Ulfman, P. Hordijk, and L. Koenderman. 2001. Activation of Rhoa and ROCK are essential for detachment of migrating leukocytes. Mol. Biol. Cell 12: 2137-2145. (Pubitemid 33049705)
Vogt, S., R. Grosse, G. Schultz, and S. Offermanns. 2003. Receptor-dependent RhoA activation in G12/G13-deficient cells: genetic evidence for an involvement of Gq/G11. J. Biol. Chem. 278: 28743-28749.
Rossman, K. L., C. J. Der, and J. Sondek. 2005. GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol. 6: 167-180.
Francis, S. A., X. Shen, J. B. Young, P. Kaul, and D. J. Lerner. 2006. Rho GEF Lsc is required for normal polarization, migration, and adhesion of formyl-peptide-stimulated neutrophils. Blood 107: 1627-1635.
Saneyoshi, T., G. Wayman, D. Fortin, M. Davare, N. Hoshi, N. Nozaki, T. Natsume, and T. R. Soderling. 2008. Activity-dependent synaptogenesis: regulation by a CaM-kinase kinase/CaM-kinase I/βPIX signaling complex. Neuron 57: 94-107.
Wang, L., L. Karlsson, S. Moses, A. Hultgardh-Nilsson, M. Andersson, C. Borna, T. Gudbjartsson, S. Jern, and D. Erlinge. 2002. P2 receptor expression profiles in human vascular smooth muscle and endothelial cells. J. Cardiovasc. Pharmacol. 40: 841-853.
Lewis, C. J., and R. J. Evans. 2000. Comparison of P2X receptors in rat mesenteric, basilar and septal (coronary) arteries. J. Auton. Nerv. Syst. 81: 69-74.
Xiang, Z., and G. Burnstock. 2005. Expression of P2X receptors on rat microglial cells during early development. Glia 52: 119-126. (Pubitemid 41652916)