Prostaglandin E2 inhibits NLRP3 inflammasome activation through EP4 receptor and intracellular cyclic AMP in human macrophages

Journal of Immunology

Volumn 194, Issue 11, 2015, Pages 5472-5487

  Sokolowska, Milena ^a   Chen, Li Yuan ^a   Liu, Yueqin ^a   Martinez Anton, Asuncion ^a   Qi, Hai Yan ^a   Logun, Carolea ^a   Alsaaty, Sara ^a   Park, Yong Hwan ^b   Kastner, Daniel L ^b   Chae, Jae Jin ^b   Shelhamer, James H ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; ADENYLATE CYCLASE INHIBITOR; ANTIPORTER; CRYOPYRIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLOOXYGENASE 2; CYTOSOLIC PHOSPHOLIPASE A2; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; PHOSPHODIESTERASE INHIBITOR; PROSTAGLANDIN E RECEPTOR 4; PROSTAGLANDIN E2; PROSTAGLANDIN RECEPTOR BLOCKING AGENT; SMALL INTERFERING RNA; CARRIER PROTEIN; CYCLOOXYGENASE 2 INHIBITOR; IL1B PROTEIN, HUMAN; LIPOPOLYSACCHARIDE; NLRP3 PROTEIN, HUMAN; PHOSPHOLIPASE A2 GROUP IV; PLA2G4A PROTEIN, HUMAN; PROSTAGLANDIN E RECEPTOR 2;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL INFILTRATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; HUMAN CELL; IMMUNOREGULATION; INTRACELLULAR MEMBRANE; MACROPHAGE; OLIGOMERIZATION; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; TIME SERIES ANALYSIS; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL LINE; CINCA SYNDROME; GENETICS; IMMUNOLOGY; INFLAMMATION; METABOLISM; MONONUCLEAR CELL; PHYSIOLOGY; PRIMARY CELL CULTURE; RNA INTERFERENCE; SECRETION (PROCESS);

ADENYLYL CYCLASE INHIBITORS; ADENYLYL CYCLASES; CARRIER PROTEINS; CELL LINE; CRYOPYRIN-ASSOCIATED PERIODIC SYNDROMES; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITORS; DINOPROSTONE; ENZYME ACTIVATION; GROUP IV PHOSPHOLIPASES A2; HUMANS; INFLAMMASOMES; INFLAMMATION; INTERLEUKIN-1BETA; LEUKOCYTES, MONONUCLEAR; LIPOPOLYSACCHARIDES; MACROPHAGES; PHOSPHODIESTERASE INHIBITORS; PRIMARY CELL CULTURE; RECEPTORS, PROSTAGLANDIN E, EP2 SUBTYPE; RECEPTORS, PROSTAGLANDIN E, EP4 SUBTYPE; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 84929643541     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401343     Document Type: Article

References (71)

1. Martinon, F., K. Burns, and J. Tschopp. 2002. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proILb. Mol. Cell 10: 417-426.
2. Latz, E., T. S. Xiao, and A. Stutz. 2013. Activation and regulation of the inflammasomes. Nat. Rev. Immunol. 13: 397-411.
3. De Nardo, D., C. M. De Nardo, and E. Latz. 2014. New insights into mechanisms controlling the NLRP3 inflammasome and its role in lung disease. Am. J. Pathol. 184: 42-54.
4. Davis, B. K., H. Wen, and J. P. Ting. 2011. The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu. Rev. Immunol. 29: 707-735.
5. Allen, I. C., E. M. TeKippe, R. M. Woodford, J. M. Uronis, E. K. Holl, A. B. Rogers, H. H. Herfarth, C. Jobin, and J. P. Ting. 2010. The NLRP3 inflammasome functions as a negative regulator of tumorigenesis during colitisassociated cancer. J. Exp. Med. 207: 1045-1056.
6. Wen, H., D. Gris, Y. Lei, S. Jha, L. Zhang, M. T. Huang, W. J. Brickey, and J. P. Ting. 2011. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat. Immunol. 12: 408-415.
7. Martinon, F., V. Pétrilli, A. Mayor, A. Tardivel, and J. Tschopp. 2006. Goutassociated uric acid crystals activate the NALP3 inflammasome. Nature 440: 237-241.
8. Duewell, P., H. Kono, K. J. Rayner, C. M. Sirois, G. Vladimer, F. G. Bauernfeind, G. S. Abela, L. Franchi, G. Nuñez, M. Schnurr, et al. 2010. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 464: 1357-1361.
9. Heneka, M. T., M. P. Kummer, A. Stutz, A. Delekate, S. Schwartz, A. Vieira-Saecker, A. Griep, D. Axt, A. Remus, T. C. Tzeng, et al. 2013. NLRP3 is activated in Alzheimer's disease and contributes to pathology in APP/PS1 mice. Nature 493: 674-678.
10. Hoffman, H. M., J. L. Mueller, D. H. Broide, A. A. Wanderer, and R. D. Kolodner. 2001. Mutation of a new gene encoding a putative pyrin-like protein causes familial cold autoinflammatory syndrome and Muckle-Wells syndrome. Nat. Genet. 29: 301-305.
11. Masters, S. L., A. Simon, I. Aksentijevich, and D. L. Kastner. 2009. Horror autoinflammaticus: the molecular pathophysiology of autoinflammatory disease. Annu. Rev. Immunol. 27: 621-668.
12. Goldbach-Mansky, R., and D. L. Kastner. 2009. Autoinflammation: the prominent role of IL-1 in monogenic autoinflammatory diseases and implications for common illnesses. J. Allergy Clin. Immunol. 124: 1141-1149. doi:10.1016/j. jaci.2009.11.016
13. Shi, C. S., K. Shenderov, N. N. Huang, J. Kabat, M. Abu-Asab, K. A. Fitzgerald, A. Sher, and J. H. Kehrl. 2012. Activation of autophagy by inflammatory signals limits IL-1b production by targeting ubiquitinated inflammasomes for destruction. Nat. Immunol. 13: 255-263.
14. Guarda, G., M. Braun, F. Staehli, A. Tardivel, C. Mattmann, I. Förster, M. Farlik, T. Decker, R. A. Du Pasquier, P. Romero, and J. Tschopp. 2011. Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity 34: 213-223.
15. Bauernfeind, F. G., G. Horvath, A. Stutz, E. S. Alnemri, K. MacDonald, D. Speert, T. Fernandes-Alnemri, J. Wu, B. G. Monks, K. A. Fitzgerald, et al. 2009. Cutting edge: NF-kB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J. Immunol. 183: 787-791.
16. Yan, Y., W. Jiang, T. Spinetti, A. Tardivel, R. Castillo, C. Bourquin, G. Guarda, Z. Tian, J. Tschopp, and R. Zhou. 2013. Omega-3 fatty acids prevent inflammation and metabolic disorder through inhibition of NLRP3 inflammasome activation. Immunity 38: 1154-1163.
17. Hernandez-Cuellar, E., K. Tsuchiya, H. Hara, R. Fang, S. Sakai, I. Kawamura, S. Akira, and M. Mitsuyama. 2012. Cutting edge: nitric oxide inhibits the NLRP3 inflammasome. J. Immunol. 189: 5113-5117.
18. Lee, G. S., N. Subramanian, A. I. Kim, I. Aksentijevich, R. Goldbach-Mansky, D. B. Sacks, R. N. Germain, D. L. Kastner, and J. J. Chae. 2012. The calciumsensing receptor regulates the NLRP3 inflammasome through Ca2+ and cAMP. Nature 492: 123-127.
19. Kalinski, P. 2012. Regulation of immune responses by prostaglandin E2. J. Immunol. 188: 21-28.
20. Desouza, I. A., C. F. Franco-Penteado, E. A. Camargo, C. S. Lima, S. A. Teixeira, M. N. Muscará, G. De Nucci, and E. Antunes. 2005. Inflammatory mechanisms underlying the rat pulmonary neutrophil influx induced by airway exposure to staphylococcal enterotoxin type A. Br. J. Pharmacol. 146: 781-791.
21. Tajima, T., T. Murata, K. Aritake, Y. Urade, H. Hirai, M. Nakamura, H. Ozaki, and M. Hori. 2008. Lipopolysaccharide induces macrophage migration via prostaglandin D2 and prostaglandin E2. J. Pharmacol. Exp. Ther. 326: 493-501.
22. Weller, C. L., S. J. Collington, A. Hartnell, D. M. Conroy, T. Kaise, J. E. Barker, M. S. Wilson, G. W. Taylor, P. J. Jose, and T. J. Williams. 2007. Chemotactic action of prostaglandin E2 on mouse mast cells acting via the PGE2 receptor 3. Proc. Natl. Acad. Sci. USA 104: 11712-11717.
23. Natura, G., K. J. Bär, A. Eitner, M. K. Boettger, F. Richter, S. Hensellek, A. Ebersberger, J. Leuchtweis, T. Maruyama, G. O. Hofmann, et al. 2013. Neuronal prostaglandin E2 receptor subtype EP3 mediates antinociception during inflammation. Proc. Natl. Acad. Sci. USA 110: 13648-13653.
24. Hellmann, J., M. J. Zhang, Y. Tang, M. Rane, A. Bhatnagar, and M. Spite. 2013. Increased saturated fatty acids in obesity alter resolution of inflammation in part by stimulating prostaglandin production. J. Immunol. 191: 1383-1392.
25. Kvirkvelia, N., M. McMenamin, K. Chaudhary, M. Bartoli, and M. P. Madaio. 2013. Prostaglandin E2 promotes cellular recovery from established nephrotoxic serum nephritis in mice, prosurvival, and regenerative effects on glomerular cells. Am. J. Physiol. Renal Physiol. 304: F463-F470.
26. MacKenzie, K. F., K. Clark, S. Naqvi, V. A. McGuire, G. Nöehren, Y. Kristariyanto, M. van den Bosch, M. Mudaliar, P. C. McCarthy, M. J. Pattison, et al. 2013. PGE2 induces macrophage IL-10 production and a regulatory-like phenotype via a protein kinase A-SIK-CRTC3 pathway. J. Immunol. 190: 565-577.
27. Nakanishi, M., and D. W. Rosenberg. 2013. Multifaceted roles of PGE2 in inflammation and cancer. Semin. Immunopathol. 35: 123-137.
28. Hirata, T., and S. Narumiya. 2012. Prostanoids as regulators of innate and adaptive immunity. Adv. Immunol. 116: 143-174.
29. Dennis, E. A., J. Cao, Y. H. Hsu, V. Magrioti, and G. Kokotos. 2011. Phospholipase A2 enzymes: physical structure, biological function, disease implication, chemical inhibition, and therapeutic intervention. Chem. Rev. 111: 6130-6185.
30. Murakami, M., Y. Taketomi, Y. Miki, H. Sato, T. Hirabayashi, and K. Yamamoto. 2011. Recent progress in phospholipase A2 research: from cells to animals to humans. Prog. Lipid Res. 50: 152-192.
31. Hirata, T., and S. Narumiya. 2011. Prostanoid receptors. Chem. Rev. 111: 6209-6230.
32. Katoh, H., A. Watabe, Y. Sugimoto, A. Ichikawa, and M. Negishi. 1995. Characterization of the signal transduction of prostaglandin E receptor EP1 subtype in cDNA-transfected Chinese hamster ovary cells. Biochim. Biophys. Acta 1244: 41-48.
33. Fujino, H., S. Salvi, and J. W. Regan. 2005. Differential regulation of phosphorylation of the cAMP response element-binding protein after activation of EP2 and EP4 prostanoid receptors by prostaglandin E2. Mol. Pharmacol. 68: 251-259.
34. Yokoyama, U., K. Iwatsubo, M. Umemura, T. Fujita, and Y. Ishikawa. 2013. The prostanoid EP4 receptor and its signaling pathway. Pharmacol. Rev. 65: 1010-1052.
35. Lefkimmiatis, K., and M. Zaccolo. 2014. cAMP signaling in subcellular compartments. Pharmacol. Ther. 143: 295-304.
36. Sugimoto, Y., T. Namba, A. Honda, Y. Hayashi, M. Negishi, A. Ichikawa, and S. Narumiya. 1992. Cloning and expression of a cDNA for mouse prostaglandin E receptor EP3 subtype. J. Biol. Chem. 267: 6463-6466.
37. Qi, H. Y., and J. H. Shelhamer. 2005. Toll-like receptor 4 signaling regulates cytosolic phospholipase A2 activation and lipid generation in lipopolysaccharide-stimulated macrophages. J. Biol. Chem. 280: 38969-38975.
38. Buczynski, M. W., D. L. Stephens, R. C. Bowers-Gentry, A. Grkovich, R. A. Deems, and E. A. Dennis. 2007. TLR-4 and sustained calcium agonists synergistically produce eicosanoids independent of protein synthesis in RAW264.7 cells. J. Biol. Chem. 282: 22834-22847.
39. Kuroda, E., K. J. Ishii, S. Uematsu, K. Ohata, C. Coban, S. Akira, K. Aritake, Y. Urade, and Y. Morimoto. 2011. Silica crystals and aluminum salts regulate the production of prostaglandin in macrophages via NALP3 inflammasomeindependent mechanisms. Immunity 34: 514-526.
40. Sokolowska, M., L. Y. Chen, M. Eberlein, A. Martinez-Anton, Y. Liu, S. Alsaaty, H. Y. Qi, C. Logun, M. Horton, and J. H. Shelhamer. 2014. Low molecular weight hyaluronan activates cytosolic phospholipase A2a and eicosanoid production in monocytes and macrophages. J. Biol. Chem. 289: 4470-4488.
41. Barberà-Cremades, M., A. Baroja-Mazo, A. I. Gomez, F. Machado, F. Di Virgilio, and P. Pelegrín. 2012. P2X7 receptor-stimulation causes fever via PGE2 and IL-1b release. FASEB J. 26: 2951-2962.
42. von Moltke, J., N. J. Trinidad, M. Moayeri, A. F. Kintzer, S. B. Wang, N. van Rooijen, C. R. Brown, B. A. Krantz, S. H. Leppla, K. Gronert, and R. E. Vance. 2012. Rapid induction of inflammatory lipid mediators by the inflammasome in vivo. Nature 490: 107-111.
43. Mariathasan, S., D. S. Weiss, K. Newton, J. McBride, K. O'Rourke, M. Roose-Girma,W. P. Lee, Y. Weinrauch, D. M. Monack, and V. M. Dixit. 2006. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440: 228-232.
44. Hornung, V., F. Bauernfeind, A. Halle, E. O. Samstad, H. Kono, K. L. Rock, K. A. Fitzgerald, and E. Latz. 2008. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 9: 847-856.
45. Koga, K., G. Takaesu, R. Yoshida, M. Nakaya, T. Kobayashi, I. Kinjyo, and A. Yoshimura. 2009. Cyclic adenosine monophosphate suppresses the transcription of proinflammatory cytokines via the phosphorylated c-Fos protein. Immunity 30: 372-383.
46. Ma, W., and R. Quirion. 2005. Up-regulation of interleukin-6 induced by prostaglandin E from invading macrophages following nerve injury: an in vivo and in vitro study. J. Neurochem. 93: 664-673.
47. Ratcliffe, M. J., A. Walding, P. A. Shelton, A. Flaherty, and I. G. Dougall. 2007. Activation of E-prostanoid4 and E-prostanoid2 receptors inhibits TNF-a release from human alveolar macrophages. Eur. Respir. J. 29: 986-994.
48. Bender, A. T., and J. A. Beavo. 2006. Cyclic nucleotide phosphodiesterases: molecular regulation to clinical use. Pharmacol. Rev. 58: 488-520.
49. Kumar, S., S. Kostin, J. P. Flacke, H. P. Reusch, and Y. Ladilov. 2009. Soluble adenylyl cyclase controls mitochondria-dependent apoptosis in coronary endothelial cells. J. Biol. Chem. 284: 14760-14768.
50. Iwatsubo, K., T. Tsunematsu, and Y. Ishikawa. 2003. Isoform-specific regulation of adenylyl cyclase: a potential target in future pharmacotherapy. Expert Opin. Ther. Targets 7: 441-451.
51. Fawcett, L., R. Baxendale, P. Stacey, C. McGrouther, I. Harrow, S. Soderling, J. Hetman, J. A. Beavo, and S. C. Phillips. 2000. Molecular cloning and characterization of a distinct human phosphodiesterase gene family: PDE11A. Proc. Natl. Acad. Sci. USA 97: 3702-3707.
52. Frei, R., R. Ferstl, P. Konieczna, M. Ziegler, T. Simon, T. M. Rugeles, S. Mailand, T. Watanabe, R. Lauener, C. A. Akdis, and L. O'Mahony. 2013. Histamine receptor 2 modifies dendritic cell responses to microbial ligands. J. Allergy Clin. Immunol. 132: 194-204.
53. Aronoff, D. M., C. Canetti, C. H. Serezani, M. Luo, and M. Peters-Golden. 2005. Cutting edge: macrophage inhibition by cyclic AMP (cAMP): differential roles of protein kinase A and exchange protein directly activated by cAMP-1. J. Immunol. 174: 595-599.
54. Gattorno, M., S. Tassi, S. Carta, L. Delfino, F. Ferlito, M. A. Pelagatti, A. D'Osualdo, A. Buoncompagni, M. G. Alpigiani, M. Alessio, et al. 2007. Pattern of interleukin-1b secretion in response to lipopolysaccharide and ATP before and after interleukin-1 blockade in patients with CIAS1 mutations. Arthritis Rheum. 56: 3138-3148.
55. Piccini, A., S. Carta, S. Tassi, D. Lasiglié, G. Fossati, and A. Rubartelli. 2008. ATP is released by monocytes stimulated with pathogen-sensing receptor ligands and induces IL-1beta and IL-18 secretion in an autocrine way. Proc. Natl. Acad. Sci. USA 105: 8067-8072.
56. Rossol, M., M. Pierer, N. Raulien, D. Quandt, U. Meusch, K. Rothe, K. Schubert, T. Schöneberg, M. Schaefer, U. Krügel, et al. 2012. Extracellular Ca2+ is a danger signal activating the NLRP3 inflammasome through G protein-coupled calcium sensing receptors. Nat. Commun. 3: 1329.
57. Park, J. Y., M. H. Pillinger, and S. B. Abramson. 2006. Prostaglandin E2 synthesis and secretion: the role of PGE2 synthases. Clin. Immunol. 119: 229-240.
58. Almeida, M. Q., K. M. Tsang, C. Cheadle, T. Watkins, J. C. Grivel, M. Nesterova, R. Goldbach-Mansky, and C. A. Stratakis. 2011. Protein kinase A regulates caspase- 1 via Ets-1 in bone stromal cell-derived lesions: a link between cyclic AMP and proinflammatory pathways in osteoblast progenitors. Hum. Mol. Genet. 20: 165-175.
59. Liu, Y., L. Y. Chen, M. Sokolowska, M. Eberlein, S. Alsaaty, A. Martinez-Anton, C. Logun, H. Y. Qi, and J. H. Shelhamer. 2014. The fish oil ingredient, docosahexaenoic acid, activates cytosolic phospholipase A2 via GPR120 receptor to produce prostaglandin E2 and plays an anti-inflammatory role in macrophages. Immunology 143: 81-95.
60. Brandwein, S. R. 1986. Regulation of interleukin 1 production by mouse peritoneal macrophages. Effects of arachidonic acid metabolites, cyclic nucleotides, and interferons. J. Biol. Chem. 261: 8624-8632.
61. Shirahama, M., H. Ishibashi, Y. Tsuchiya, S. Kurokawa, K. Hayashida, Y. Okumura, and Y. Niho. 1988. Kupffer cells may autoregulate interleukin 1 production by producing interleukin 1 inhibitor and prostaglandin E2. Scand. J. Immunol. 28: 719-725.
62. Goss, J. A., M. J. Mangino, and M. W. Flye. 1992. Kupffer cell autoregulation of IL-1 production by PGE2 during hepatic regeneration. J. Surg. Res. 52: 422-428.
63. Knudsen, P. J., C. A. Dinarello, and T. B. Strom. 1986. Prostaglandins posttranscriptionally inhibit monocyte expression of interleukin 1 activity by increasing intracellular cyclic adenosine monophosphate. J. Immunol. 137: 3189-3194.
64. Hart, P. H., G. A. Whitty, D. S. Piccoli, and J. A. Hamilton. 1989. Control by IFN-gamma and PGE2 of TNF alpha and IL-1 production by human monocytes. Immunology 66: 376-383.
65. Sung, S. S., and J. A. Walters. 1991. Increased cyclic AMP levels enhance IL-1 alpha and IL-1 beta mRNA expression and protein production in human myelomonocytic cell lines and monocytes. J. Clin. Invest. 88: 1915-1923.
66. Ohmori, Y., G. Strassman, and T. A. Hamilton. 1990. cAMP differentially regulates expression of mRNA encoding IL-1 alpha and IL-1 beta in murine peritoneal macrophages. J. Immunol. 145: 3333-3339.
67. Oshima, H., K. Hioki, B. K. Popivanova, K. Oguma, N. Van Rooijen, T. O. Ishikawa, and M. Oshima. 2011. Prostaglandin E2 signaling and bacterial infection recruit tumor-promoting macrophages to mouse gastric tumors. Gastroenterology 140: 596-607.e7. doi:10.1053/j.gastro.2010.11.007
68. Chandra, G., J. P. Cogswell, L. R. Miller, M. M. Godlevski, S. W. Stinnett, S. L. Noel, S. H. Kadwell, T. A. Kost, and J. G. Gray. 1995. Cyclic AMP signaling pathways are important in IL-1 beta transcriptional regulation. J. Immunol. 155: 4535-4543.
69. Otterness, I. G., M. L. Bliven, J. D. Eskra, M. Reinke, and D. C. Hanson. 1988. The pharmacologic regulation of interleukin-1 production: the role of prostaglandins. Cell. Immunol. 114: 385-397.
70. Andrei, C., P. Margiocco, A. Poggi, L. V. Lotti, M. R. Torrisi, and A. Rubartelli. 2004. Phospholipases C and A2 control lysosome-mediated IL- 1b secretion: implications for inflammatory processes. Proc. Natl. Acad. Sci. USA 101: 9745-9750.
71. Hua, K. F., J. C. Chou, S. M. Ka, Y. L. Tasi, A. Chen, S. H. Wu, H. W. Chiu, W. T. Wong, Y. F. Wang, C. L. Tsai, et al. 2015. Cyclooxygenase-2 regulates NLRP3 inflammasome-derived IL-1b production. J. Cell. Physiol. 230: 863-874.