Extracellular ATP protects against sepsis through macrophage P2X7 purinergic receptors by enhancing intracellular bacterial killing

FASEB Journal

Volumn 29, Issue 9, 2015, Pages 3626-3637

  Csóka, Balázs ^a,b   Németh, Zoltan H ^a,c   Töro, Gabor ^a,b   Idzko, Marco ^d   Zech, Andreas ^d   Koscsó, Balázs ^a   Spolarics, Zoltan ^a,b   Antonioli, Luca ^e   Cseri, Karolina ^f   Erdélyi, Katalin ^g   Pacher, Pal ^g   Haskó, György ^a,b  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b Rutgers The State University of New Jersey   (United States)

^c MORRISTOWN MEDICAL CENTER   (United States)

^d UNIVERSITY OF FREIBURG   (Germany)

^e UNIVERSITY OF PISA   (Italy)

^f UNIVERSITY OF DEBRECEN   (Hungary)

^g NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

Author keywords

Connexin; Inflammasome; Inflammation; Pannexin; Phagocytosis

Indexed keywords

ADENOSINE TRIPHOSPHATE; ADENOSINE TRIPHOSPHATE MAGNESIUM; ALANINE AMINOTRANSFERASE; INFLAMMASOME; MYELOPEROXIDASE; PROTEIN INHIBITOR; PURINERGIC P2X7 RECEPTOR; UREA;

ADOPTIVE TRANSFER; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL LOAD; BACTERICIDAL ACTIVITY; BONE MARROW; CELLULAR IMMUNITY; CHEMOTAXIS ASSAY; CHIMERA; COLONY FORMING UNIT; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EC50; ENZYME ACTIVITY; EXTRACELLULAR SPACE; IC50; IMMUNOREGULATION; INTRACELLULAR SPACE; MALE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PHAGOCYTOSIS; PRIORITY JOURNAL; REGULATORY MECHANISM; SEPSIS; SIGNAL TRANSDUCTION; SURVIVAL; UREA NITROGEN BLOOD LEVEL; ANALOGS AND DERIVATIVES; ANIMAL; BACTERIUM; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; MACROPHAGE; MICROBIOLOGY; PATHOLOGY;

ADENOSINE TRIPHOSPHATE; ADOPTIVE TRANSFER; ANIMALS; BACTERIA; INFLAMMASOMES; MACROPHAGES; MICE; MICE, KNOCKOUT; RECEPTORS, PURINERGIC P2X7; SEPSIS; SIGNAL TRANSDUCTION;

EID: 84943181140     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-272450     Document Type: Article

References (47)

1. Stearns-Kurosawa, D. J., Osuchowski, M. F., Valentine, C., Kurosawa, S., and Remick, D. G. (2011) The pathogenesis of sepsis. Annu. Rev. Pathol. 6, 19-48
2. Riedemann, N. C., and Guo, R. F., and Ward, P. A. (2003) The enigma of sepsis. J. Clin. Invest. 112, 460-467
3. Van der Poll, T., and Opal, S. M. (2008) Host-pathogen interactions in sepsis. Lancet Infect. Dis. 8, 32-43
4. Angus, D. C., Linde-Zwirble, W. T., Lidicker, J., Clermont, G., Carcillo, J., and Pinsky, M. R. (2001) Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit. Care Med. 29, 1303-1310
5. Benjamim, C. F., and Hogaboam, C. M., and Kunkel, S. L. (2004) The chronic consequences of severe sepsis. J. Leukoc. Biol. 75, 408-412
6. Oberholzer, A., Oberholzer, C., and Moldawer, L. L. (2001) Sepsis syndromes: understanding the role of innate and acquired immunity. Shock 16, 83-96
7. King, E. G., Bauzá, G. J., Mella, J. R., and Remick, D. G. (2014) Pathophysiologic mechanisms in septic shock. Lab. Invest. 94, 4-12
8. La Sala, A., Ferrari, D., Di Virgilio, F., Idzko, M., Norgauer, J., and Girolomoni, G. (2003) Alerting and tuning the immune response by extracellular nucleotides. J. Leukoc. Biol. 73, 339-343
9. Idzko, M., Ferrari, D., and Eltzschig, H. K. (2014) Nucleotide signalling during inflammation. Nature 509, 310-317
10. Lohman, A. W., and Isakson, B. E. (2014) Differentiating connexin hemichannels and pannexin channels in cellular ATP release. FEBS Lett. 588, 1379-1388
11. Eugenin, E. A. (2014) Role of connexin/pannexin containing channels in infectious diseases. FEBS Lett. 588, 1389-1395
12. Gu, B.J., Zhang, W. Y., Bendall, L.J., Chessell, I.P., Buell, G.N., and Wiley, J. S. (2000) Expression of P2X(7) purinoceptors on human lymphocytes and monocytes: evidence for nonfunctional P2X(7) receptors. Am. J. Physiol. Cell Physiol. 279, C1189-C1197
13. Martel-Gallegos, G., Rosales-Saavedra, M. T., Reyes, J. P., Casas-Pruneda, G., Toro-Castillo, C., Pérez-Cornejo, P., and Arreola, J. (2010) Human neutrophils do not express purinergic P2X7 receptors. Purinergic Signal. 6, 297-306
14. Christenson, K., Björkman, L., Tängemo, C., and Bylund, J. (2008) Serum amyloid A inhibits apoptosis of human neutrophils via a P2X7-sensitive pathway independent of formyl peptide receptorlike 1. J. Leukoc. Biol. 83, 139-148
15. Bartlett, R., Stokes, L., and Sluyter, R. (2014) The P2X7 receptor channel: recent developments and the use of P2X7 antagonists in models of disease. Pharmacol. Rev. 66, 638-675
16. Dubyak, G. R. (2012) P2X7 receptor regulation of non-classical secretion from immune effector cells. Cell. Microbiol. 14, 1697-1706
17. Bours, M. J., and Swennen, E. L., Di Virgilio, F., Cronstein, B. N., and Dagnelie, P. C. (2006) Adenosine 59-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol. Ther. 112, 358-404
18. Wiley, J.S., Sluyter, R., Gu, B.J., Stokes, L., and Fuller, S.J.(2011) The human P2X7 receptorandits role in innate immunity. Tissue Antigens 78, 321-332
19. Lammas, D.A., Stober, C., Harvey, C.J., Kendrick, N., Panchalingam, S., and Kumararatne, D. S. (1997) ATP-induced killing of mycobacteria by human macrophages is mediated by purinergic P2Z(P2X7) receptors. Immunity 7, 433-444
20. Morandini, A.C., Savio, L.E., and Coutinho-Silva, R.(2014) The role of P2X7 receptor in infectious inflammatory diseases and the influence of ectonucleotidases. Biomed. J. 37, 169-177
21. Chen, Q., Jin, Y., Zhang, K., Li, H., Chen, W., Meng, G., and Fang, X. (2014) Alarmin HNP-1 promotes pyroptosis and IL-1β release through different roles of NLRP3 inflammasome via P2X7 in LPS-primed macrophages. Innate Immun. 20, 290-300
22. Miao, E. A., and Leaf, I. A., Treuting, P. M., Mao, D. P., Dors, M., Sarkar, A., Warren, S. E., Wewers, M. D., and Aderem, A. (2010) Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat. Immunol. 11, 1136-1142
23. Skarnes, W. C., Rosen, B., West, A. P., Koutsourakis, M., Bushell, W., Iyer, V., Mujica, A. O., Thomas, M., Harrow, J., Cox, T., Jackson, D., Severin, J., Biggs, P., Fu, J., Nefedov, M., de Jong, P. J., Stewart, A. F., and Bradley, A. (2011) A conditional knockout resource for the genome-wide study of mouse gene function. Nature 474, 337-342
24. Csóka, B., Németh, Z. H., Mukhopadhyay, P., Spolarics, Z., Rajesh, M., Federici, S., Deitch, E. A., Bátkai, S., Pacher, P., and Haskó, G. (2009) CB2 cannabinoid receptors contribute to bacterial invasion and mortality in polymicrobial sepsis. PLoS ONE 4, e6409
25. Haskó, G., Csóka, B., Koscsó, B., Chandra, R., Pacher, P., Thompson, L. F., Deitch, E. A., Spolarics, Z., Virág, L., Gergely, P., Rolandelli, R. H., and Németh, Z. H. (2011) Ecto-59-nucleotidase (CD73) decreases mortality and organ injury in sepsis. J. Immunol. 187, 4256-4267
26. Grenz, A., Zhang, H., Hermes, M., Eckle, T., Klingel, K., Huang, D. Y., Müller, C. E., Robson, S. C., Osswald, H., and Eltzschig, H. K. (2007) Contribution of E-NTPDase1 (CD39) to renal protection from ischemia-reperfusion injury. FASEB J. 21, 2863-2873
27. Csóka, B., Németh, Z.H., Rosenberger, P., Eltzschig, H.K., Spolarics, Z., Pacher, P., Selmeczy, Z., Koscsó, B., Himer, L., Vizi, E. S., Blackburn, M. R., Deitch, E. A., and Haskó, G.(2010) A2B adenosine receptors protect against sepsis-induced mortality by dampening excessive inflammation. J. Immunol. 185, 542-550
28. Csóka, B., Németh, Z. H., Virág, L., Gergely, P., and Leibovich, S. J., Pacher, P., Sun, C. X., Blackburn, M. R., Vizi, E. S., Deitch, E. A., and Haskó, G. (2007) A2A adenosine receptors and C/EBPbeta are crucially required for IL-10 production by macrophages exposed to Escherichia coli. Blood 110, 2685-2695
29. Németh, Z. H., Csóka, B., Wilmanski, J., Xu, D., Lu, Q., Ledent, C, Deitch, E. A, Pacher, P., Spolarics, Z., and Haskó, G. (2006) Adenosine A2A receptor inactivation increases survival in polymicrobial sepsis. J. Immunol. 176, 5616-5626
30. Van Gils, J. M., Derby, M. C., Fernandes, L. R., Ramkhelawon, B., Ray, T. D., Rayner, K J., Parathath, S., Distel, E., Feig, J. L., Alvarez-Leite, J. I., Rayner, A. J., McDonald, T. O., O'Brien, K D., Stuart, L. M., Fisher, E. A., Lacy-Hulbert, A, and Moore, K.J. (2012) The neuroimmune guidance cue netrin-1 promotes atherosclerosis by inhibiting the emigration of macrophages from plaques. Nat Immunol. 13, 136-143
31. Remick, D. G., and Newcomb, D. E., Bolgos, G. L., and Call, D. R (2000) Comparison of the mortality and inflammatory response of two models of sepsis: lipopolysaccharide vs. cecal ligation and puncture. Shock 13, 110-116
32. Gallardo-Soler, A., Gómez-Nieto, C., Campo, M. L., Marathe, C., Tontonoz, P., Castrillo, A, and Corraliza, I. (2008) Arginase I induction by modified lipoproteins in macrophages: a peroxisome proliferator-activated receptor-gamma/delta-mediated effect that links lipid metabolism and immunity. Mol. Endocrinol. 22,1394-1402
33. Senthil, M., Watkins, A., Barlos, D., Xu, D. Z., Lu, Q., Abungu, B., Caputo, F., Feinman, R, and Deitch, E. A (2007) Intravenous injection of trauma-hemorrhagic shock mesenteric lymph causes lung injury that is dependent upon activation of the inducible nitric oxide synthase pathway. Ann. Surg. 246, 822-830
34. Bone, R. C., Balk, R.A, Cerra, F. B., Dellinger, R P., Fein, A M., Knaus, W. A, Schein, R M., and Sibbald, W. J.; ACCP/SCCM Consensus Conference Committee. (2009) Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. The ACCP/SCCM Consensus Conference Committee. American College of Chest Physicians/Society of Critical Care Medicine. 1992. Chest 136(5, Suppl)e28
35. Ulloa, L., and Tracey, K J. (2005) The "cytokine profile": a code for sepsis. Trends Mol. Med. 11, 56-63
36. Ulloa, L., Brunner, M., Ramos, L., and Deitch, E. A (2009) Scientific and clinical challenges in sepsis. Curr. Pharm. Des. 15, 1918-1935
37. Xiao, W., and Mindrinos, M. N., Seok, J., Cuschieri, J., Cuenca, A. G., Gao, H., Hayden, D. L., Hennessy, L., Moore, E. E., Minei, J. P., Bankey, P. E., Johnson, J. L., Sperry, J., Nathens, A. B., Billiar, T. R, West, M. A., Brownstein, B. H., Mason, P. H., Baker, H. V., Finnerty, C. C. Jeschke, M. G., Lopez, M. C., Klein, M. B., Gamelli, R L., Gibran, N. S., Arnoldo, B., Xu, W., Zhang, Y., Calvano, S. E., McDonald-Smith, G. P., Schoenfeld, D. A., Storey, J. D., Cobb, J. P., Warren, H. S., Moldawer, L. L., Herndon, D. N., Lowry, S. F., Maier, R. V., Davis, R. W., and Tompkins, R. G.; Inflammation and Host Response to Injury Large-Scale Collaborative Research Program. (2011) A genomic storm in critically injured humans. J. Exp. Med. 208, 2581-2590
38. Antonioli, L., Pacher, P., Vizi, E. S., and Haskó, G. (2013) CD39 and CD73 in immunity and inflammation. Trends Mol. Med. 19, 355-367
39. Csóka, B., Németh, Z. H., Töro, G., Koscsó, B., Kó kai, E., Robson, S. C., Enjyoji, K., Rolandelli, R. H., Erdélyi, K., Pacher, P., and Haskó, G. (2015) CD39 improves survival in microbial sepsis by attenuating systemic inflammation. FASEB J. 29, 25-36
40. Ali, S. R., and Timmer, A. M., Bilgrami, S., Park, E. J., Eckmann, L., Nizet, V., and Karin, M. (2011) Anthrax toxin induces macrophage death by p38 MAPK inhibition but leads to inflammasome activation via ATP leakage. Immunity 35, 34-44
41. Eltzschig, H. K., Eckle, T., Mager, A., Küper, N., Karcher, C., Weissmüller, T., Boengler, K., Schulz, R., Robson, S. C., and Colgan, S. P. (2006) ATP release from activated neutrophils occurs via connexin 43 and modulates adenosine-dependent endothelial cell function. Circ. Res. 99, 1100-1108
42. Bao, Y., Chen, Y., Ledderose, C., Li, L., and Junger, W. G. (2013) Pannexin 1 channels link chemoattractant receptor signaling to local excitation and global inhibition responses at the front and back of polarized neutrophils. J. Biol. Chem. 288, 22650-22657
43. Schenk, U., and Westendorf, A. M., Radaelli, E., Casati, A., Ferro, M., Fumagalli, M., Verderio, C., Buer, J., Scanziani, E., and Grassi, F. (2008) Purinergic control of T cell activation by ATP released through pannexin-1 hemichannels. Sci. Signal. 1, ra6
44. Gu, B. J., and Baird, P. N., Vessey, K. A., Skarratt, K. K., Fletcher, E. L., Fuller, S.J., Richardson, A. J., Guymer, R. H., and Wiley, J.S.(2013) A rare functional haplotype of the P2RX4 and P2RX7 genes leads to loss of innate phagocytosis and confers increased risk of age-related macular degeneration. FASEB J. 27, 1479-1487
45. Lees, M. P., and Fuller, S. J., McLeod, R., Boulter, N. R., Miller, C. M., Zakrzewski, A. M., Mui, E. J., Witola, W. H., Coyne, J. J., Hargrave, A. C., Jamieson, S. E., Blackwell, J. M., Wiley, J. S., and Smith, N. C. (2010) P2X7 receptor-mediated killing of an intracellular parasite, Toxoplasma gondii, by human and murine macrophages. J. Immunol. 184, 7040-7046
46. Chaves, M. M., Marques-da-Silva, C., Monteiro, A.P., Canetti, C., and Coutinho-Silva, R.(2014) Leukotriene B4 modulates P2X7 receptor-mediated Leishmania amazonensis elimination in murine macrophages. J. Immunol. 192, 4765-4773
47. Santana, P. T., and Benjamim, C. F., Martinez, C. G., Kurtenbach, E., Takiya, C. M., and Coutinho-Silva, R. (2015) The P2X7 Receptor contributes to the development of the exacerbated inflammatory response associated with sepsis [E-pub ahead of print]. J. Innate Immun. DOI:10.1159/000371388.