Inflammatory Resolution Triggers a Prolonged Phase of Immune Suppression through COX-1/mPGES-1-Derived Prostaglandin E2

Cell Reports

Volumn 20, Issue 13, 2017, Pages 3162-3175

  Newson, Justine ^a   Motwani, Madhur P ^a   Kendall, Alexandra C ^b   Nicolaou, Anna ^b   Muccioli, Giulio G ^c   Alhouayek, Mireille ^c   Bennett, Melanie ^a   Van De Merwe, Rachel ^a   James, Sarah ^a   De Maeyer, Roel P H ^a   Gilroy, Derek W ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

adaptive homeostasis; autoimmunity; eicosanoid; immune scarring; macrophage

Indexed keywords

CYCLOOXYGENASE 1; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; PROSTAGLANDIN E RECEPTOR 1; PROSTAGLANDIN E SYNTHASE 1; PROSTAGLANDIN E2; MEMBRANE PROTEIN; PROSTAGLANDIN E SYNTHASE; PTGS1 PROTEIN, MOUSE;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; IMMUNOLOGICAL TOLERANCE; INFLAMMATION; INTERFERON PRODUCTION; MACROPHAGE; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PNEUMOCOCCAL INFECTION; PRIORITY JOURNAL; SECONDARY INFECTION; T LYMPHOCYTE; ZYMOSAN-INDUCED PERITONITIS; ANIMAL; C57BL MOUSE; ENZYMOLOGY; IMMUNOLOGY;

ANIMALS; CYCLOOXYGENASE 1; DINOPROSTONE; INFLAMMATION; INTERFERON-GAMMA; MACROPHAGES; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; PROSTAGLANDIN-E SYNTHASES;

EID: 85029865764     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2017.08.098     Document Type: Article

References (56)

1. Abramson, S.B., Weissmann, G., The mechanisms of action of nonsteroidal antiinflammatory drugs. Arthritis Rheum. 32 (1989), 1–9.
2. Abramson, S., Korchak, H., Ludewig, R., Edelson, H., Haines, K., Levin, R.I., Herman, R., Rider, L., Kimmel, S., Weissmann, G., Modes of action of aspirin-like drugs. Proc. Natl. Acad. Sci. USA 82 (1985), 7227–7231.
3. Aronoff, D.M., Canetti, C., Peters-Golden, M., Prostaglandin E2 inhibits alveolar macrophage phagocytosis through an E-prostanoid 2 receptor-mediated increase in intracellular cyclic AMP. J. Immunol. 173 (2004), 559–565.
4. Aronoff, D.M., Lewis, C., Serezani, C.H., Eaton, K.A., Goel, D., Phipps, J.C., Peters-Golden, M., Mancuso, P., E-prostanoid 3 receptor deletion improves pulmonary host defense and protects mice from death in severe Streptococcus pneumoniae infection. J. Immunol. 183 (2009), 2642–2649.
5. Baker, P.E., Fahey, J.V., Munck, A., Prostaglandin inhibition of T-cell proliferation is mediated at two levels. Cell. Immunol. 61 (1981), 52–61.
6. Betz, M., Fox, B.S., Prostaglandin E2 inhibits production of Th1 lymphokines but not of Th2 lymphokines. J. Immunol. 146 (1991), 108–113.
7. Boasso, A., Hardy, A.W., Anderson, S.A., Dolan, M.J., Shearer, G.M., HIV-induced type I interferon and tryptophan catabolism drive T cell dysfunction despite phenotypic activation. PLoS ONE, 3, 2008, e2961.
8. Dinauer, M.C., The respiratory burst oxidase and the molecular genetics of chronic granulomatous disease. Crit. Rev. Clin. Lab. Sci. 30 (1993), 329–369.
9. Ferber, I.A., Brocke, S., Taylor-Edwards, C., Ridgway, W., Dinisco, C., Steinman, L., Dalton, D., Fathman, C.G., Mice with a disrupted IFN-gamma gene are susceptible to the induction of experimental autoimmune encephalomyelitis (EAE). J. Immunol. 156 (1996), 5–7.
10. Ferreira, S.H., Moncada, S., Vane, J.R., Indomethacin and aspirin abolish prostaglandin release from the spleen. Nat. New Biol. 231 (1971), 237–239.
11. Flower, R., Gryglewski, R., Herbaczyńska-Cedro, K., Vane, J.R., Effects of anti-inflammatory drugs on prostaglandin biosynthesis. Nat. New Biol. 238 (1972), 104–106.
12. Fonseca, D.M., Hand, T.W., Han, S.J., Gerner, M.Y., Glatman Zaretsky, A., Byrd, A.L., Harrison, O.J., Ortiz, A.M., Quinones, M., Trinchieri, G., et al. Microbiota-dependent sequelae of acute infection compromise tissue-specific immunity. Cell 163 (2015), 354–366.
13. Fujinami, R.S., Oldstone, M.B., Wroblewska, Z., Frankel, M.E., Koprowski, H., Molecular mimicry in virus infection: crossreaction of measles virus phosphoprotein or of herpes simplex virus protein with human intermediate filaments. Proc. Natl. Acad. Sci. USA 80 (1983), 2346–2350.
14. Fujinami, R.S., von Herrath, M.G., Christen, U., Whitton, J.L., Molecular mimicry, bystander activation, or viral persistence: infections and autoimmune disease. Clin. Microbiol. Rev. 19 (2006), 80–94.
15. González-Navajas, J.M., Lee, J., David, M., Raz, E., Immunomodulatory functions of type I interferons. Nat. Rev. Immunol. 12 (2012), 125–135.
16. Guedez, Y.B., Whittington, K.B., Clayton, J.L., Joosten, L.A., van de Loo, F.A., van den Berg, W.B., Rosloniec, E.F., Genetic ablation of interferon-gamma up-regulates interleukin-1beta expression and enables the elicitation of collagen-induced arthritis in a nonsusceptible mouse strain. Arthritis Rheum. 44 (2001), 2413–2424.
17. Jamieson, T., Cook, D.N., Nibbs, R.J., Rot, A., Nixon, C., McLean, P., Alcami, A., Lira, S.A., Wiekowski, M., Graham, G.J., The chemokine receptor D6 limits the inflammatory response in vivo. Nat. Immunol. 6 (2005), 403–411.
18. Kalinski, P., Regulation of immune responses by prostaglandin E2. J. Immunol. 188 (2012), 21–28.
19. Kawabata, A., Prostaglandin E2 and pain–an update. Biol. Pharm. Bull. 34 (2011), 1170–1173.
20. Kuperman, D.A., Huang, X., Koth, L.L., Chang, G.H., Dolganov, G.M., Zhu, Z., Elias, J.A., Sheppard, D., Erle, D.J., Direct effects of interleukin-13 on epithelial cells cause airway hyperreactivity and mucus overproduction in asthma. Nat. Med. 8 (2002), 885–889.
21. Lawrence, T., Willoughby, D.A., Gilroy, D.W., Anti-inflammatory lipid mediators and insights into the resolution of inflammation. Nat. Rev. Immunol. 2 (2002), 787–795.
22. León, B., López-Bravo, M., Ardavín, C., Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity 26 (2007), 519–531.
23. Lykens, J.E., Terrell, C.E., Zoller, E.E., Divanovic, S., Trompette, A., Karp, C.L., Aliberti, J., Flick, M.J., Jordan, M.B., Mice with a selective impairment of IFN-gamma signaling in macrophage lineage cells demonstrate the critical role of IFN-gamma-activated macrophages for the control of protozoan parasitic infections in vivo. J. Immunol. 184 (2010), 877–885.
24. Mao, Y., Sarhan, D., Steven, A., Seliger, B., Kiessling, R., Lundqvist, A., Inhibition of tumor-derived prostaglandin-e2 blocks the induction of myeloid-derived suppressor cells and recovers natural killer cell activity. Clin. Cancer Res. 20 (2014), 4096–4106.
25. Massey, K.A., Nicolaou, A., Lipidomics of oxidized polyunsaturated fatty acids. Free Radic. Biol. Med. 59 (2013), 45–55.
26. Medeiros, A.I., Serezani, C.H., Lee, S.P., Peters-Golden, M., Efferocytosis impairs pulmonary macrophage and lung antibacterial function via PGE2/EP2 signaling. J. Exp. Med. 206 (2009), 61–68.
27. Moncada, S., Vane, J.R., Pharmacology and endogenous roles of prostaglandin endoperoxides, thromboxane A2, and prostacyclin. Pharmacol. Rev. 30 (1978), 293–331.
28. Morgenstern, D.E., Gifford, M.A., Li, L.L., Doerschuk, C.M., Dinauer, M.C., Absence of respiratory burst in X-linked chronic granulomatous disease mice leads to abnormalities in both host defense and inflammatory response to Aspergillus fumigatus. J. Exp. Med. 185 (1997), 207–218.
29. Nakano, H., Lin, K.L., Yanagita, M., Charbonneau, C., Cook, D.N., Kakiuchi, T., Gunn, M.D., Blood-derived inflammatory dendritic cells in lymph nodes stimulate acute T helper type 1 immune responses. Nat. Immunol. 10 (2009), 394–402.
30. Nathan, C., Points of control in inflammation. Nature 420 (2002), 846–852.
31. Newson, J., Stables, M., Karra, E., Arce-Vargas, F., Quezada, S., Motwani, M., Mack, M., Yona, S., Audzevich, T., Gilroy, D.W., Resolution of acute inflammation bridges the gap between innate and adaptive immunity. Blood 124 (2014), 1748–1764.
32. O'Brien, A.J., Fullerton, J.N., Massey, K.A., Auld, G., Sewell, G., James, S., Newson, J., Karra, E., Winstanley, A., Alazawi, W., et al. Immunosuppression in acutely decompensated cirrhosis is mediated by prostaglandin E2. Nat. Med. 20 (2014), 518–523.
33. Obermajer, N., Kalinski, P., Generation of myeloid-derived suppressor cells using prostaglandin E2. Transplant. Res., 1, 2012, 15.
34. Obermajer, N., Muthuswamy, R., Lesnock, J., Edwards, R.P., Kalinski, P., Positive feedback between PGE2 and COX2 redirects the differentiation of human dendritic cells toward stable myeloid-derived suppressor cells. Blood 118 (2011), 5498–5505.
35. Rajakariar, R., Hilliard, M., Lawrence, T., Trivedi, S., Colville-Nash, P., Bellingan, G., Fitzgerald, D., Yaqoob, M.M., Gilroy, D.W., Hematopoietic prostaglandin D2 synthase controls the onset and resolution of acute inflammation through PGD2 and 15-deoxyDelta12 14 PGJ2. Proc. Natl. Acad. Sci. USA 104 (2007), 20979–20984.
36. Savill, J.S., Wyllie, A.H., Henson, J.E., Walport, M.J., Henson, P.M., Haslett, C., Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. J. Clin. Invest. 83 (1989), 865–875.
37. Schuh, C.D., Pierre, S., Weigert, A., Weichand, B., Altenrath, K., Schreiber, Y., Ferreiros, N., Zhang, D.D., Suo, J., Treutlein, E.M., et al. Prostacyclin mediates neuropathic pain through interleukin 1β-expressing resident macrophages. Pain 155 (2014), 545–555.
38. Segal, A.W., The NADPH oxidase and chronic granulomatous disease. Mol. Med. Today 2 (1996), 129–135.
39. Segal, A.W., Peters, T.J., Characterisation of the enzyme defect in chronic granulomatous disease. Lancet 1 (1976), 1363–1365.
40. Serezani, C.H., Aronoff, D.M., Jancar, S., Mancuso, P., Peters-Golden, M., Leukotrienes enhance the bactericidal activity of alveolar macrophages against Klebsiella pneumoniae through the activation of NADPH oxidase. Blood 106 (2005), 1067–1075.
41. Serezani, C.H., Chung, J., Ballinger, M.N., Moore, B.B., Aronoff, D.M., Peters-Golden, M., Prostaglandin E2 suppresses bacterial killing in alveolar macrophages by inhibiting NADPH oxidase. Am. J. Respir. Cell Mol. Biol. 37 (2007), 562–570.
42. Serhan, C.N., Brain, S.D., Buckley, C.D., Gilroy, D.W., Haslett, C., O'Neill, L.A., Perretti, M., Rossi, A.G., Wallace, J.L., Resolution of inflammation: state of the art, definitions and terms. FASEB J. 21 (2007), 325–332.
43. Simmons, D.L., Botting, R.M., Hla, T., Cyclooxygenase isozymes: the biology of prostaglandin synthesis and inhibition. Pharmacol. Rev. 56 (2004), 387–437.
44. Sinha, P., Clements, V.K., Fulton, A.M., Ostrand-Rosenberg, S., Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells. Cancer Res. 67 (2007), 4507–4513.
45. Stables, M.J., Newson, J., Ayoub, S.S., Brown, J., Hyams, C.J., Gilroy, D.W., Priming innate immune responses to infection by cyclooxygenase inhibition kills antibiotic-susceptible and -resistant bacteria. Blood 116 (2010), 2950–2959.
46. Stoecklin, G., Anderson, P., Posttranscriptional mechanisms regulating the inflammatory response. Adv. Immunol. 89 (2006), 1–37.
47. Taub, D.D., Lloyd, A.R., Conlon, K., Wang, J.M., Ortaldo, J.R., Harada, A., Matsushima, K., Kelvin, D.J., Oppenheim, J.J., Recombinant human interferon-inducible protein 10 is a chemoattractant for human monocytes and T lymphocytes and promotes T cell adhesion to endothelial cells. J. Exp. Med. 177 (1993), 1809–1814.
48. Teijaro, J.R., Ng, C., Lee, A.M., Sullivan, B.M., Sheehan, K.C., Welch, M., Schreiber, R.D., de la Torre, J.C., Oldstone, M.B., Persistent LCMV infection is controlled by blockade of type I interferon signaling. Science 340 (2013), 207–211.
49. Uderhardt, S., Herrmann, M., Oskolkova, O.V., Aschermann, S., Bicker, W., Ipseiz, N., Sarter, K., Frey, B., Rothe, T., Voll, R., et al. 12/15-lipoxygenase orchestrates the clearance of apoptotic cells and maintains immunologic tolerance. Immunity 36 (2012), 834–846.
50. Vane, J.R., Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs. Nat. New Biol. 231 (1971), 232–235.
51. Vermeire, K., Heremans, H., Vandeputte, M., Huang, S., Billiau, A., Matthys, P., Accelerated collagen-induced arthritis in IFN-gamma receptor-deficient mice. J. Immunol. 158 (1997), 5507–5513.
52. Wakim, L.M., Bevan, M.J., Cross-dressed dendritic cells drive memory CD8+ T-cell activation after viral infection. Nature 471 (2011), 629–632.
53. Wilson, E.B., Yamada, D.H., Elsaesser, H., Herskovitz, J., Deng, J., Cheng, G., Aronow, B.J., Karp, C.L., Brooks, D.G., Blockade of chronic type I interferon signaling to control persistent LCMV infection. Science 340 (2013), 202–207.
54. Woodland, D.L., Blackman, M.A., Retroviral super-antigens and T cells. Int. Rev. Immunol. 8 (1992), 311–325.
55. Wright, K.L., Weaver, S.A., Patel, K., Coopman, K., Feeney, M., Kolios, G., Robertson, D.A., Ward, S.G., Differential regulation of prostaglandin E biosynthesis by interferon-gamma in colonic epithelial cells. Br. J. Pharmacol. 141 (2004), 1091–1097.
56. Yona, S., Kim, K.W., Wolf, Y., Mildner, A., Varol, D., Breker, M., Strauss-Ayali, D., Viukov, S., Guilliams, M., Misharin, A., et al. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis. Immunity 38 (2013), 79–91.