Nucleotide signalling during inflammation

Nature

Volumn 509, Issue 7500, 2014, Pages 310-317

  Idzko, Marco ^a   Ferrari, Davide ^b   Eltzschig, Holger K ^c  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FERRARA   (Italy)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; PURINERGIC P2X RECEPTOR; PURINERGIC P2X7 RECEPTOR; PURINERGIC P2Y RECEPTOR; PURINERGIC P2Y12 RECEPTOR; PURINERGIC P2Y2 RECEPTOR; PURINERGIC P2Y6 RECEPTOR;

BIOCHEMISTRY; CYTOLOGY; DEFENSE MECHANISM; DISEASE INCIDENCE; DISEASE TREATMENT; INFECTIOUS DISEASE; MEDICINE; NUCLEIC ACID; PHYSIOLOGY; SIGNALING; TUMOR;

ADAPTIVE IMMUNITY; CHEMICAL STRUCTURE; CHRONIC INFLAMMATION; CHRONIC LUNG DISEASE; HOST RESISTANCE; INFLAMMATION; INFLAMMATORY BOWEL DISEASE; INNATE IMMUNITY; ISCHEMIA; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; SIGNAL TRANSDUCTION;

ADENOSINE TRIPHOSPHATE; ANIMALS; HUMANS; INFECTION; INFLAMMATION; ION CHANNELS; NEOPLASMS; PURINERGIC P2 RECEPTOR ANTAGONISTS; RECEPTORS, PURINERGIC P2; SIGNAL TRANSDUCTION;

EID: 84900530332     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature13085     Document Type: Review

References (116)

1. Khakh, B. S. & Burnstock, G. The double life of ATP. Sci. Am. 301, 84-92 (2009).
2. Junger, W. G. Immune cell regulation by autocrine purinergic signalling. Nature Rev. Immunol. 11, 201-212 (2011).
3. Fredholm, B. & Verkhratsky, A. Purines-80 years and very much alive. Acta Physiol. 199, 91-92 (2010).
4. Burnstock, G. Purinergic signalling and disorders of the central nervous system. Nature Rev. Drug. Discov. 7, 575-590 (2008).
5. Eltzschig, H. K., Sitkovsky, M. V. & Robson, S. C. Purinergic signaling during inflammation. N. Engl. J. Med. 367, 2322-2333 (2012).
6. Eltzschig, H. K., Macmanus, C. F. & Colgan, S. P. Neutrophils as sources of extracellular nucleotides: functional consequences at the vascular interface. Trends Cardiovasc. Med. 18, 103-107 (2008).
7. Eltzschig, H. K. et al. ATP release from activated neutrophils occurs via connexin 43 and modulates adenosine-dependent endothelial cell function. Circ. Res. 99, 1100-1108 (2006).
8. Chekeni, F. B. et al. Pannexin 1 channels mediate 'find-me' signal release and membrane permeability during apoptosis. Nature 467, 863-867 (2010).
9. Faigle, M., Seessle, J., Zug, S., El Kasmi, K. C. & Eltzschig, H. K. ATP release from vascular endothelia occurs across Cx43 hemichannels and is attenuated during hypoxia. PLoS ONE 3, e2801 (2008).
10. Lazarowski, E. R. Vesicular and conductive mechanisms of nucleotide release. Purinergic Signal. 8, 359-373 (2012).
11. Abbracchio, M. P. et al. International Union of Pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol. Rev. 58, 281-341 (2006).
12. Jacobson, K. A., Balasubramanian, R., Deflorian, F.& Gao, Z. G. G protein-coupled adenosine (P1) and P2Y receptors: ligand design and receptor interactions. Purinergic Signal. 8, 419-436 (2012).
13. Soulet, C. et al. Gi-dependent and-independentmechanisms downstreamof the P2Y12 ADP-receptor. J. Thromb. Haemost. 2, 135-146 (2004).
14. Hardy, A. R. et al. P2Y1 and P2Y12 receptors for ADP desensitize by distinct kinase-dependent mechanisms. Blood 105, 3552-3560 (2005).
15. von Kugelgen, I. Pharmacological profiles of cloned mammalian P2Y-receptor subtypes. Pharmacol. Ther. 110, 415-432 (2006).
16. Harden, T. K., Sesma, J. I., Fricks, I. P. & Lazarowski, E. R. Signalling and pharmacological properties of the P2Y receptor. Acta Physiol. 199, 149-160 (2010).
17. Hawking, F. Suramin: with special reference to onchocerciasis. Adv. Pharmacol. Chemother. 15, 289-322 (1978).
18. Voogd, T. E., Vansterkenburg, E. L., Wilting, J. & Janssen, L. H. Recent research on the biological activity of suramin. Pharmacol. Rev. 45, 177-203 (1993).
19. Ratjen, F. et al. Long term effects of denufosol tetrasodiumin patients with cystic fibrosis. J. Cyst. Fibros. 11, 539-549 (2012).
20. Rieg, T. et al. Mice lacking P2Y2 receptors have salt-resistant hypertension and facilitated renal Na1 and water reabsorption. FASEB J. 21, 3717-3726 (2007).
21. Horckmans, M. et al.Gene deletion ofP2Y4 receptor lowers exercise capacity and reduces myocardial hypertrophy with swimming exercise. Am. J. Physiol. Heart. Circ. Physiol. 303, H835-H843 (2012).
22. Knowles, M. R., Clarke, L. L. & Boucher, R. C. Activation by extracellular nucleotides of chloride secretion in the airway epithelia of patients with cystic fibrosis. N. Engl. J. Med. 325, 533-538 (1991).
23. Parr, C. E. et al. Cloning and expression of a human P2U nucleotide receptor, a target for cystic fibrosis pharmacotherapy. Proc. Natl Acad. Sci. USA 91, 3275-3279 (1994).
24. Davis, S. D. & Ferkol, T. Identifying the origins of cystic fibrosis lung disease. N. Engl. J. Med. 368, 2026-2028 (2013).
25. Burnstock, G., Brouns, I., Adriaensen, D.&Timmermans, J. P.Purinergic signaling in the airways. Pharmacol. Rev. 64, 834-868 (2012).
26. Kellerman, D. et al. Denufosol: a review of studies with inhaled P2Y2 agonists that led to Phase 3. Pulm. Pharmacol. Ther. 21, 600-607 (2008).
27. Deterding, R. R. et al. Phase 2 randomized safety and efficacy trial of nebulized denufosol tetrasodium in cystic fibrosis. Am. J. Respir. Crit. Care Med. 176, 362-369 (2007).
28. Gendaszewska-Darmach, E. & Kucharska, M. Nucleotide receptors as targets in the pharmacological enhancement of dermal wound healing. Purinergic Signal. 7, 193-206 (2011).
29. 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).
30. Chen, Y. et al. Purinergic signaling: a fundamental mechanism in neutrophil activation. Sci. Signal 3, ra45 (2010).
31. Chen, Y. et al. ATP release guides neutrophil chemotaxis via P2Y2 and A3 receptors. Science 314, 1792-1795 (2006).
32. Myrtek, D.& Idzko, M. Chemotactic activity of extracellular nucleotideson human immune cells. Purinergic Signal. 3, 5-11 (2007).
33. Ferrari, D. et al. Activation of human eosinophils via P2 receptors: novel findings and future perspectives. J. Leukoc. Biol. 79, 7-15 (2006).
34. Kronlage, M. et al. Autocrine purinergic receptor signaling is essential for macrophage chemotaxis. Sci. Signal 3, ra55 (2010).
35. Ben Yebdri, F., Kukulski, F., Tremblay, A. & Sevigny, J. Concomitant activation of P2Y2 and P2Y6 receptors on monocytes is required for TLR1/2-induced neutrophil migration by regulating IL-8 secretion. Eur. J. Immunol. 39, 2885-2894 (2009).
36. Kobayashi, T., Kouzaki, H. & Kita, H. Human eosinophils recognize endogenous danger signal crystalline uric acid and produce proinflammatory cytokines mediated by autocrine ATP. J. Immunol. 184, 6350-6358 (2010).
37. Geary, C. et al. Increased susceptibility of purinergic receptor-deficient mice to lung infection with Pseudomonas aeruginosa.Am. J. Physiol. Lung Cell Mol. Physiol. 289, L890-L895 (2005).
38. Inoue, Y., Chen, Y., Hirsh, M. I., Yip, L. & Junger, W. G. A3 and P2Y2 receptors control the recruitment of neutrophils to the lungs in a mouse model of sepsis. Shock 30, 173-177 (2008).
39. Ayata, C. K. et al. Purinergic P2Y2 receptors promote neutrophil infiltration and hepatocyte death in mice with acute liver injury. Gastroenterology 143, 1620-1629 (2012).
40. Lommatzsch, M. et al. Extracellular adenosine triphosphate and chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 181, 928-934 (2010).
41. Cicko, S. et al. Purinergic receptor inhibition prevents the development ofsmokeinduced lung injury and emphysema. J. Immunol. 185, 688-697 (2010).
42. Idzko, M. et al. Extracellular ATP triggers and maintains asthmatic airway inflammation by activating dendritic cells. Nature Med. 13, 913-919 (2007).
43. Muller, T. et al. The purinergic receptor P2Y2 receptor mediates chemotaxis of dendritic cells and eosinophils in allergic lung inflammation. Allergy 65, 1545-1553 (2010).
44. Weber, F. C. et al. Lack of the purinergic receptor P2X7 results in resistance to contact hypersensitivity. J. Exp. Med. 207, 2609-2619 (2010).
45. Idzko, M. et al. Stimulation of P2 purinergic receptors induces the release of eosinophil cationic protein and interleukin-8 from human eosinophils. Br. J. Pharmacol. 138, 1244-1250 (2003).
46. Kouzaki, H., Iijima, K., Kobayashi, T., O'Grady, S. M. & Kita, H. The danger signal, extracellular ATP, is a sensor for an airborne allergen and triggers IL-33 release and innate Th2-type responses. J. Immunol. 186, 4375-4387 (2011).
47. Kunzli, B. M. et al. Upregulation of CD39/NTPDases and P2 receptors in human pancreatic disease. Am. J. Physiol. Gastrointest. Liver Physiol. 292, G223-G230 (2007).
48. Vieira, R. P. et al. Purinergic receptor type 6 contributes to airway inflammation and remodeling in experimental allergic airway inflammation. Am. J. Respir. Crit. Care Med. 184, 215-223 (2011).
49. Grbic, D. M., Degagne, E., Langlois, C., Dupuis, A. A. & Gendron, F. P. Intestinal inflammation increases the expression of the P2Y6 receptor on epithelial cells and the release ofCXCchemokine ligand8 byUDP. J.Immunol. 180, 2659-2668 (2008).
50. Riegel, A. K. et al. Selective induction of endothelial P2Y6 nucleotide receptor promotes vascular inflammation. Blood 117, 2548-2555 (2011).
51. Zhang, Z. et al. P2Y6 agonist uridine 59-diphosphate promotes host defense against bacterial infection via monocyte chemoattractant protein-1-mediated monocytes/macrophages recruitment. J. Immunol. 186, 5376-5387 (2011).
52. Idzko, M. et al. Characterization of the biological activities of uridine diphosphate in human dendritic cells: influence on chemotaxis and CXCL8 release. J. Cell. Physiol. 201, 286-293 (2004).
53. Ferrari, D. et al. P2 purinergic receptors of human eosinophils: characterization and coupling to oxygen radical production. FEBS Lett. 486, 217-224 (2000).
54. Koizumi, S. et al. UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature 446, 1091-1095 (2007).
55. Grbic, D. M. et al. P2Y6 receptor contributes to neutrophil recruitment to inflamed intestinalmucosa by increasing CXC chemokine ligand 8 expression in an AP-1-dependent manner in epithelial cells. Inflamm. Bowel Dis. 18, 1456-1469 (2012).
56. Guns, P. J., Hendrickx, J., Van Assche, T., Fransen, P. & Bult, H. P2Y receptors and atherosclerosis in apolipoprotein E-deficient mice. Br. J. Pharmacol. 159, 326-336 (2010).
57. Semple, J. W., Italiano, J. E., Jr. & Freedman, J. Platelets and the immune continuum. Nature Rev. Immunol. 11, 264-274 (2011).
58. Muhlestein, J. B. Effect of antiplatelet therapy on inflammatory markers in atherothrombotic patients. Thromb. Haemost. 103, 71-82 (2010).
59. Li, D. et al. Roles of purinergic receptor P2Y, G protein-coupled 12 in the development of atherosclerosis in apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 32, e81-e89 (2012).
60. Yashiro, K. et al. Involvement of platelet activation by P2Y12 receptor in the development of transplant arteriosclerosis in mice. Transplantation 87, 660-667 (2009).
61. Paruchuri, S. et al. Leukotriene E4-inducedpulmonary inflammation ismediated by the P2Y12 receptor. J. Exp. Med. 206, 2543-2555 (2009).
62. Neves, J. S., Radke, A. L. & Weller, P. F. Cysteinyl leukotrienes acting via granule membrane-expressed receptors elicit secretion from within cell-free human eosinophil granules. J. Allergy Clin. Immunol. 125, 477-482 (2010).
63. Ben Addi, A., Cammarata, D., Conley, P. B., Boeynaems, J. M. & Robaye, B. Role of the P2Y12 receptor in the modulation of murine dendritic cell function by ADP. J. Immunol. 185, 5900-5906 (2010).
64. Bunyavanich, S., Boyce, J. A., Raby, B. A. & Weiss, S. T. Gene-by-environment effect of house dust mite on purinergic receptor P2Y12 (P2RY12) and lung function in children with asthma. Clin. Exp. Allergy 42, 229-237 (2012).
65. Surprenant, A. & North, R. A. Signaling at purinergic P2X receptors. Annu. Rev. Physiol. 71, 333-359 (2009).
66. Khakh, B. S. & North, R. A. Neuromodulation by extracellular ATP and P2X receptors in the CNS. Neuron 76, 51-69 (2012).
67. Khakh, B. S. & North, R. A. P2X receptors as cell-surface ATP sensors in health and disease. Nature 442, 527-532 (2006).
68. Kawate, T., Michel, J. C., Birdsong, W. T. & Gouaux, E. Crystal structure of the ATP-gated P2X4 ion channel in the closed state. Nature 460, 592-598 (2009).
69. Alberto, A. V. et al. Is pannexin the pore associated with the P2X7 receptor? Naunyn Schmiedebergs Arch. Pharmacol. 386, 775-787 (2013).
70. Surprenant, A., Rassendren, F., Kawashima, E., North, R. A. & Buell, G. The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7). Science 272, 735-738 (1996).
71. Schwarz, N. et al. Alternative splicing of the N-terminal cytosolic and transmembrane domains of P2X7 controls gating of the ion channel by ADP-ribosylation. PLoS One 7, e41269 (2012).
72. North, R. A. & Jarvis, M. F. P2X receptors as drug targets. Mol. Pharmacol. 83, 759-769 (2013).
73. Mulryan, K. et al. Reduced vas deferens contraction and male infertility in mice lacking P2X1 receptors. Nature 403, 86-89 (2000).
74. Yan, D. et al. Mutation of the ATP-gated P2X2 receptor leads to progressive hearing loss and increased susceptibility to noise. Proc. Natl Acad. Sci. USA 110, 2228-2233 (2013).
75. Cockayne, D. A. et al. Urinary bladder hyporeflexia and reduced pain-related behaviour in P2X3-deficient mice. Nature 407, 1011-1015 (2000).
76. Coutinho-Silva, R., Knight, G. E. & Burnstock, G. Impairment of the splenic immune system in P2X2/P2X3 knockout mice. Immunobiology 209, 661-668 (2005).
77. Falzoni, S. et al. The purinergic P2Z receptor of human macrophage cells. Characterization and possible physiological role. J. Clin. Invest. 95, 1207-1216 (1995).
78. Coutinho-Silva, R.& Ojcius, D. M. Role of extracellular nucleotides in the immune response against intracellular bacteria and protozoan parasites. Microbes Infect. 14, 1271-1277 (2012).
79. Stagg, J. & Smyth, M. J. Extracellular adenosine triphosphate and adenosine in cancer. Oncogene 29, 5346-5358 (2010).
80. Ghiringhelli, F. et al. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1b-dependent adaptive immunity against tumors. Nature Med. 15, 1170-1178 (2009).
81. Muller, T. et al. A potential role for P2X7R in allergic airway inflammation in mice and humans. Am. J. Respir. Cell Mol. Biol. 44, 456-464 (2011).
82. Wilhelm, K. et al. Graft-versus-host disease is enhanced by extracellular ATP activating P2X7R. Nature Med. 16, 1434-1438 (2010).
83. Killeen, M. E., Ferris, L., Kupetsky, E. A., Falo, L., Jr. & Mathers, A. R. Signaling through purinergic receptors for ATP induces human cutaneous innate and adaptive Th17 responses: implications in the pathogenesis of psoriasis. J. Immunol. 190, 4324-4336 (2013).
84. Manthei, D. M. et al. Protection from asthma in a high-risk birth cohort by attenuated P2X7 function. J. Allergy Clin. Immunol. 130, 496-502 (2012).
85. Atarashi, K. et al. ATP drives lamina propria TH17 cell differentiation. Nature 455, 808-812 (2008).
86. Gulbransen, B. D. et al. Activation of neuronal P2X7 receptor-pannexin-1 mediates death of enteric neurons during colitis. Nature Med. 18, 600-604 (2012).
87. Kurashima, Y. et al. Extracellular ATP mediates mast cell-dependent intestinal inflammation through P2X7 purinoceptors. Nature Commun. 3, 1034 (2012).
88. Lucattelli, M. et al. P2X7 receptor signalling in the pathogenesis of smoke-induced lung inflammation and emphysema. Am. J. Respir. Cell Mol. Biol. 44, 423-429 (2010).
89. Zimmermann, H., Zebisch, M. & Strater, N. Cellular function and molecular structure of ecto-nucleotidases. Purinergic Signal. 8, 437-502 (2012).
90. Kohler, D. et al. CD39/ectonucleoside triphosphate diphosphohydrolase 1 provides myocardial protection during cardiac ischemia/reperfusion injury. Circulation 116, 1784-1794 (2007).
91. Pinsky, D. J. et al. Elucidation of the thromboregulatory role ofCD39/ectoapyrase in the ischemic brain. J. Clin. Invest. 109, 1031-1040 (2002).
92. Flogel, U. et al. Selective activation of adenosine A2A receptors on immune cells by a CD73-dependent prodrug suppresses joint inflammation in experimental rheumatoid arthritis. Sci. Transl. Med. 4, 146ra108 (2012).
93. Ohta, A. & Sitkovsky, M. Role of G-protein-coupled adenosine receptors in downregulation of inflammation and protection from tissue damage. Nature 414, 916-920 (2001).
94. Sitkovsky, M. V. et al. Physiological control of immune response and inflammatory tissue damage by hypoxia-inducible factors and adenosine A2A receptors. Annu. Rev. Immunol. 22, 657-682 (2004).
95. Colgan, S. P. & Eltzschig, H. K. Adenosine and hypoxia-inducible factor signaling in intestinal injury and recovery. Annu. Rev. Physiol. 74, 153-175 (2012).
96. Friedman, D. J. et al. CD39 deletion exacerbates experimental murine colitis and human polymorphisms increase susceptibility to inflammatory bowel disease. Proc. Natl Acad. Sci. USA 106, 16788-16793 (2009).
97. Eckle, T. et al. Identification of ectonucleotidases CD39 and CD73 in innate protection during acute lung injury. J. Immunol. 178, 8127-8137 (2007).
98. Chevalier, M. F. & Weiss, L. The split personality of regulatory T cells in HIV infection. Blood 121, 29-37 (2013).
99. Deaglio, S. et al. Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J. Exp. Med. 204, 1257-1265 (2007).
100. Ehrentraut, H. et al. CD731 regulatory T cells contribute to adenosine-mediated resolution of acute lung injury. FASEB J. 27, 2207-2219 (2013).
101. Nikolova, M. et al. CD39/adenosine pathway is involved in AIDS progression. PLoS Pathog. 7, e1002110 (2011).
102. Beldi, G. et al. Natural killer T cell dysfunction in CD39-null mice protects against concanavalin A-induced hepatitis. Hepatology 48, 841-852 (2008).
103. Sansom, F. M. et al. A bacterial ecto-triphosphate diphosphohydrolase similar to human CD39 is essential for intracellular multiplication of Legionella pneumophila. Cell Microbiol. 9, 1922-1935 (2007).
104. Eltzschig, H. K. & Eckle, T. Ischemia and reperfusion-from mechanism to translation. Nature Med. 17, 1391-1401 (2011).
105. Eltzschig, H. K. et al. Endothelial catabolism of extracellular adenosine during hypoxia: the role of surface adenosine deaminase and CD26. Blood 108, 1602-1610 (2006).
106. Morote-Garcia, J. C., Rosenberger, P., Kuhlicke, J. & Eltzschig, H. K. HIF-1-dependent repression of adenosine kinase attenuates hypoxia-induced vascular leak. Blood 111, 5571-5580 (2008).
107. Schingnitz, U. et al. Signaling through the A2B adenosine receptor dampens endotoxin-induced acute lung injury. J. Immunol. 184, 5271-5279 (2010).
108. Eltzschig, H. K., Bonney, S. K. & Eckle, T. Attenuating myocardial ischemia by targeting A2B adenosine receptors. Trends Mol. Med. 19, 345-354 (2013).
109. Eckle, T. et al. Adora2b-elicited Per2 stabilization promotes a HIF-dependent metabolic switch crucial for myocardial adaptation to ischemia. Nature Med. 18, 774-782 (2012).
110. Eckle, T. et al. Crosstalk between the equilibrative nucleoside transporter ENT2 and alveolar Adora2b adenosine receptors dampens acute lung injury. FASEB J. 27, 3078-3089 (2013).
111. Morote-Garcia, J. C., Rosenberger, P., Nivillac, N. M., Coe, I. R. & Eltzschig, H. K. Hypoxia-inducible factor-dependent repression of equilibrative nucleoside transporter 2 attenuates mucosal inflammation during intestinal hypoxia. Gastroenterology 136, 607-618 (2009).
112. Frick, J. S. et al. Contribution of adenosine A2B receptors to inflammatory parameters of experimental colitis. J. Immunol. 182, 4957-4964 (2009).
113. Csoka, B. et al. A2B adenosine receptors protect against sepsis-induced mortality by dampening excessive inflammation. J. Immunol. 185, 542-550 (2010).
114. Belikoff, B. G. et al. A2B adenosine receptor blockade enhances macrophagemediated bacterial phagocytosis and improves polymicrobial sepsis survival in mice. J. Immunol. 186, 2444-2453 (2011).
115. Zhang, K. et al. Structure of the human P2Y12 receptor in complex with an antithrombotic drug. Nature http://dx.doi.org/10.1038/nature13083 (23 March, 2014).
116. Zhang, J. et al. Agonist-bound structure of the human P2Y12 receptor. Nature (in the press).