Purinergic signaling: A fundamental mechanism in neutrophil activation

Science Signaling

Volumn 3, Issue 125, 2010, Pages

  Chen, Yu ^a   Yao, Yongli ^a   Sumi, Yuka ^a   Li, Andrew ^a   Kim To, Uyen ^a   Elkhal, Abdallah ^a   Inoue, Yoshiaki ^a   Woehrle, Tobias ^a   Zhang, Qin ^a   Hauser, Carl ^a   Junger, Wolfgang G ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b LUDWIG BOLTZMANN INSTITUTE FOR EXPERIMENTAL AND CLINICAL TRAUMATOLOGY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; COMPLEMENT COMPONENT C5A; FORMYLPEPTIDE RECEPTOR; INTERLEUKIN 8; LEUKOTRIENE B4 RECEPTOR; PURINERGIC P2Y2 RECEPTOR;

ARTICLE; BACTERIAL INFECTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HUMAN; HUMAN CELL; INNATE IMMUNITY; LEUKOCYTE ACTIVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; HUMANS; NEUTROPHIL ACTIVATION; RECEPTORS, PURINERGIC; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS);

EID: 77953853994     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2000549     Document Type: Article

References (43)

1. A. K. Nussler, U. A. Wittel, N. C. Nussler, H. G. Beger, Leukocytes, the Janus cells in inflammatory disease. Langenbecks Arch. Surg. 384, 222-232 (1999).
2. M. J. Rabiet, E. Huet, F. Boulay, The N-formyl peptide receptors and the anaphylatoxin C5a receptors: An overview. Biochimie 89, 1089-1106 (2007).
3. D. J. Waugh, C. Wilson, The interleukin-8 pathway in cancer. Clin. Cancer Res. 14, 6735-6741 (2008).
4. V. Capra, Molecular and functional aspects of human cysteinyl leukotriene receptors. Pharmacol. Res. 50, 1-11 (2004).
5. S. J. Fuller, L. Stokes, K. K. Skarratt, B. J. Gu, J. S. Wiley, Genetics of the P2X7 receptor and human disease. Purinergic Signal. 5, 257-262 (2009).
6. F. Di Virgilio, S. Ceruti, P. Bramanti, M. P. Abbracchio, Purinergic signalling in inflammation of the central nervous system. Trends Neurosci. 32, 79-87 (2009).
7. Y. Qu, L. Ramachandra, S. Mohr, L. Franchi, C. V. Harding, G. Nunez, G. R. Dubyak, P2X7 receptor-stimulated secretion of MHC class II-containing exosomes requires the ASC/NLRP3 inflammasome but is independent of caspase-1. J. Immunol. 182, 5052-5062 (2009).
8. G. Haskó, J. Linden, B. Crostein, P. Pacher, Adenosine receptors: Therapeutic aspects for inflammatory and immune diseases. Nat. Rev. Drug Discov. 7, 759-770 (2008).
9. B. B. Fredholm, Adenosine, an endogenous distress signal, modulates tissue damage and repair. Cell Death Differ. 14, 1315-1323 (2007).
10. G. Burnstock, G. E. Knight, Cellular distribution and functions of P2 receptor subtypes in different systems. Int. Rev. Cytol. 240, 31-304 (2004).
11. B. B. Fredholm, A. P. IJzerman, K. A. Jacobson, K. N. Klotz, J. Linden, International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol. Rev. 53, 527-552 (2001).
12. Y. Chen, R. Corriden, Y. Inoue, L. Yip, N. Hashiguchi, A. Zinkernagel, V. Nizet, P. A. Insel, W. G. Junger, ATP release guides neutrophil chemotaxis via P2Y2 and A3 receptors. Science 314, 1792-1795 (2006).
13. E. M. Schwiebert, ATP release mechanisms, ATP receptors and purinergic signalling along the nephron. Clin. Exp. Pharmacol. Physiol. 28, 340-350 (2001).
14. H. K. Eltzschig, T. Eckle, A. Mager, N. Kuper, C. Karcher, T. Weissmuller, K. Boengler, R. Schulz, S. C. Robson, S. P. Colgan, ATP release from activated neutrophils occurs via connexin 43 and modulates adenosine-dependent endothelial cell function. Circ. Res. 99, 1100-1108 (2006).
15. M. Suzuki, A. Mizuno, A novel human Cl- channel family related to Drosophila flightless locus. J. Biol. Chem. 279, 22461-22468 (2004).
16. U. Schenk, A. M. Westendorf, E. Radaelli, A. Casati, M. Ferro, M. Fumagalli, C. Verderio, J. Buer, E. Scanziani, F. Grassi, Purinergic control of T cell activation by ATP released through pannexin-1 hemichannels. Sci. Signal. 1, ra6 (2008).
17. R. Z. Sabirov, Y. Okada, ATP release via anion channels. Purinergic Signal. 1, 311-328 (2005).
18. W. Ma, H. Hui, P. Pelegrin, A. Surprenant, Pharmacological characterization of pannexin-1 currents expressed in mammalian cells. J. Pharmacol. Exp. Ther. 328, 409-418 (2009).
19. M. S. Leite, R. Thomaz, J. H. Oliveira, P. L. Oliveira, J. R. Meyer-Fernandes, Trypanosoma brucei brucei: Effects of ferrous iron and heme on ecto-nucleoside triphosphate diphosphohydrolase activity. Exp. Parasitol. 121, 137-143 (2009).
20. Y. Chen, N. Hashiguchi, L. Yip, W. G. Junger, Hypertonic saline enhances neutrophil elastase release through activation of P2 and A3 receptors. Am. J. Physiol. Cell Physiol. 290, C1051-C1059 (2006).
21. P. Pelegrin, A. Surprenant, Pannexin-1 mediates large pore formation and interleukin-1b release by the ATP-gated P2X7 receptor. EMBO J. 25, 5071-5082 (2006).
22. R. Corriden, Y. Chen, Y. Inoue, G. Beldi, S. C. Robson, P. A. Insel, W.G. Junger, Ectonucleoside triphosphate diphosphohydrolase 1 (E-NTPDase1/CD39) regulates neutrophil chemotaxis by hydrolyzing released ATP to adenosine. J. Biol. Chem. 283, 28480-28486 (2008).
23. R. J. Thompson, M. F. Jackson, M. E. Olah, R. L. Rungta, D. J. Hines, M. A. Beazely, J. F. MacDonald, B. A. MacVicar, Activation of pannexin-1 hemichannels augments aberrant bursting in the hippocampus. Science 322, 1555-1559 (2008).
24. Y. Inoue, Y. Chen, M. I. Hirsh, L. Yip, W. G. Junger, A3 and P2Y2 receptors control the recruitment of neutrophils to the lungs in a mouse model of sepsis. Shock 30, 173-177 (2008).
25. S. J. Weiss, Tissue destruction by neutrophils. N. Engl. J. Med. 320, 365-376 (1989).
26. P. Bodin, G. Burnstock, Purinergic signalling: ATP release. Neurochem. Res. 26, 959-969 (2001).
27. L. Bao, S. Locovei, G. Dahl, Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett. 572, 65-68 (2004).
28. J. Kang, N. Kang, D. Lovatt, A. Torres, Z. Zhao, J. Lin, M. Nedergaard, Connexin 43 hemichannels are permeable to ATP. J. Neurosci. 28, 4702-4711 (2008).
29. P. D. Bell, J.-Y. Lapointe, R. Sabirov, S. Hayashi, J. Peti-Peterdi, K. Manabe, G. Kovacs, Y. Okada, Macula densa cell signaling involves ATP release through a maxi anion channel. Proc. Natl. Acad. Sci. U.S.A. 100, 4322-4327 (2003).
30. A. K. Dutta, R. Z. Sabirov, H. Uramoto, Y. Okada, Role of ATP-conductive anion channel in ATP release from neonatal rat cardiomyocytes in ischaemic or hypoxic conditions. J. Physiol. 559, 799-812 (2004).
31. A. K. Dutta, Y. E. Korchev, A. I. Shevchuk, S. Hayashi, Y. Okada, R. Z. Sabirov, Spatial distribution of maxi-anion channel on cardiomyocytes detected by smart-patch technique. Biophys. J. 94, 1646-1655 (2008).
32. R. Z. Sabirov, A. K. Dutta, Y. Okada, Volume-dependent ATP-conductive large-conductance anion channel as a pathway for swelling-induced ATP release. J. Gen. Physiol. 118, 251-266 (2001).
33. H. T. Liu, B. A. Tashmukhamedov, H. Inoue, Y. Okada, R. Z. Sabirov, Roles of two types of anion channels in glutamate release from mouse astrocytes under ischemic or osmotic stress. Glia 54, 343-357 (2006).
34. A. Ram, S. K. Singh, V. P. Singh, S. Kumar, B. Ghosh, Inhaled carbenoxolone prevents allergic airway inflammation and airway hyperreactivity in a mouse model of asthma. Int. Arch. Allergy Immunol. 149, 38-46 (2009).
35. M. Bai, Dimerization of G-protein-coupled receptors: Roles in signal transduction. Cell. Signal. 16, 175-186 (2004).
36. R. Franco, V. Casadó, A. Cortés, J. Mallol, F. Ciruela, S. Ferré, C. Lluis, E. I. Canela, G-protein-coupled receptor heteromers: Function and ligand pharmacology. Br. J. Pharmacol. 153 (Suppl. 1), S90-S98 (2008).
37. R. Franco, S. Ferré, L. Agnati, M. Torvinen, S. Ginés, J. Hillion, V. Casadó, P. Lledó, M. Zoli, C. Lluis, K. Fuxe, Evidence for adenosine/dopamine receptor interactions: Indications for heteromerization. Neuropsychopharmacology 23, S50-S59 (2000).
38. K. Yoshioka, O. Saitoh, H. Nakata, Heteromeric association creates a P2Y-like adenosine receptor. Proc. Natl. Acad. Sci. U.S.A. 98, 7617-7622 (2001).
39. G. G. Yegutkin, Nucleotide- and nucleoside-converting ectoenzymes: Important modulators of purinergic signalling cascade. Biochim. Biophys. Acta 1783, 673-694 (2008).
40. M. R. Elliott, F. B. Chekeni, P. C. Trampont, E. R. Lazarowski, A. Kadl, S. F. Walk, D. Park, R. I. Woodson, M. Ostankovich, P. Sharma, J. J. Lysiak, T. K. Harden, N. Leitinger, K. S. Ravichandran, Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 461, 282-286 (2009).
41. L. J. Relvas, C. Bouffioux, B. Marcet, D. Communi, M. Makhoul, M. Horckmans, C. Blero, D. Bruyns, L. Caspers, J. M. Boeynaems, F. Willermain, Extracellular nucleotides and interleukin-8 production by ARPE cells: Potential role of danger signals in blood-retinal barrier activation. Invest. Ophthalmol. Vis. Sci. 50, 1241-1246 (2009).
42. W. G. Junger, D. B. Hoyt, R. E. Davis, C. Herdon-Remelius, S. Namiki, H. Junger, W. Loomis, A. Altman, Hypertonicity regulates the function of human neutrophils by modulating chemoattractant receptor signaling and activating mitogen-activated protein kinase p38. J. Clin. Invest. 101, 2768-2779 (1998).
43. Acknowledgments: We thank H. Sitte and C. Nanoff (Medical University of Vienna, Vienna, Austria) for providing the pECFP-P2Y2 receptor construct. Funding: This study was supported in part by a Shock Society/Nova Nordisk research grant for Early Career Investigators (Y.C.) and by NIH grants GM-51477, GM-60475, AI-072287, and AI-080582 and Congressionally Directed Medical Research Programs grant PR043034 (W.G.J.). Author contributions: Y.C. performed most of the experiments and prepared the manuscript and figures; Y.Y. and U.K.T. provided technical and logistical assistance; Y.S., T.W., Y.I., and A.E. performed the animal experiments; A.L. and Q.Z. performed calcium measurements; C.H. helped with the discussion and interpretation of results; and W.G.J. was responsible for the design and coordination of the study and finalized the manuscript. Competing interests: The authors have no conflicts of interest to declare. Use of the expression plasmids described in this study requires a materials transfer agreement.