Eicosanoid storm in infection and inflammation

Nature Reviews Immunology

Volumn 15, Issue 8, 2015, Pages 511-523

  Dennis, Edward A ^a   Norris, Paul C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ICOSANOID; PHOSPHOLIPASE A2; AUTACOID; CYTOCHROME P450; CYTOKINE; PHOSPHOLIPASE; PROSTAGLANDIN SYNTHASE;

BRONCHOCONSTRICTION; CELL ACTIVATION; CELL FUNCTION; DISEASE SEVERITY; ENDOPLASMIC RETICULUM; ENZYME INHIBITION; FATTY ACID METABOLISM; FATTY ACID SYNTHESIS; GENETIC VARIABILITY; HUMAN; ICOSANOID METABOLISM; INFECTION; INFLAMMATION; LIPIDOMICS; MACROPHAGE; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; STEADY STATE; SURVIVAL; ANIMAL; BACTERIAL INFECTION; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; LIPID METABOLISM; METABOLISM; MICROBIOLOGY; PATHOLOGY;

ANIMALS; BACTERIAL INFECTIONS; CYTOCHROME P-450 ENZYME SYSTEM; CYTOKINES; EICOSANOIDS; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; INFLAMMATION; INFLAMMATION MEDIATORS; LIPID METABOLISM; PHOSPHOLIPASES; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; SIGNAL TRANSDUCTION;

EID: 84937943929     PISSN: 14741733     EISSN: 14741741     Source Type: Journal    
DOI: 10.1038/nri3859     Document Type: Review

References (120)

1. Funk, C. D. Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294, 1871-1875 (2001).
2. Buczynski, M. W., Dumlao, D. S. & Dennis, E. A. Thematic review series: proteomics. An integrated omics analysis of eicosanoid biology. J. Lipid Res. 50, 1015-1038 (2009).
3. Gross, O., Thomas, C. J., Guarda, G. & Tschopp, J. The inflammasome: an integrated view. Immunol. Rev. 243, 136-151 (2011).
4. Latz, E., Xiao, T. S. & Stutz, A. Activation and regulation of the inflammasomes. Nat. Rev. Immunol. 13, 397-411 (2013).
5. Norris, P. C., Gosselin, D., Reichart, D., Glass, C. K. & Dennis, E. A. Phospholipase A2 regulates eicosanoid class switching during inflammasome activation. Proc. Natl Acad. Sci. USA 111, 12746-12751 (2014).
6. Harkewicz, R. & Dennis, E. A. Applications of mass spectrometry to lipids and membranes. Annu. Rev. Biochem. 80, 301-325 (2011).
7. Dumlao, D. S., Buczynski, M. W., Norris, P. C., Harkewicz, R. & Dennis, E. A. High-throughput lipidomic analysis of fatty acid derived eicosanoids and N-acylethanolamines. Biochim. Biophys. Acta 1811, 724-736 (2011).
8. Serhan, C. N. Pro-resolving lipid mediators are leads for resolution physiology. Nature 510, 92-101 (2014).
9. Quehenberger, O. & Dennis, E. A. The human plasma lipidome. New Engl. J. Med. 365, 1812-1823 (2011).
10. Wada, M. et al. Enzymes and receptors of prostaglandin pathways with arachidonic acid-derived versus eicosapentaenoic acid-derived substrates and products. J. Biol. Chem. 282, 22254-22266 (2007).
11. Nebert, D. W. & Dalton, T. P. The role of cytochrome P450 enzymes in endogenous signalling pathways and environmental carcinogenesis. Nat. Rev. Cancer 6, 947-960 (2006).
12. Brash, A. R. Lipoxygenases: occurrence, functions, catalysis, and acquisition of substrate. J. Biol. Chem. 274, 23679-23682 (1999).
13. Sala, A., Folco, G. & Murphy, R. C. Transcellular biosynthesis of eicosanoids. Pharmacol. Rep. 62, 503-510 (2010).
14. Ueno, N., Takegoshi, Y., Kamei, D., Kudo, I. & Murakami, M. Coupling between cyclooxygenases and terminal prostanoid synthases. Biochem. Biophys. Res. Commun. 338, 70-76 (2005).
15. Newcomer, M. E. & Gilbert, N. C. Location, location, location: compartmentalization of early events in leukotriene biosynthesis. J. Biol. Chem. 285, 25109-25114 (2010).
16. Dennis, E. A., Cao, J., Hsu, Y. H., Magrioti, V. & Kokotos, G. Phospholipase A2 enzymes: physical structure, biological function, disease implication, chemical inhibition, and therapeutic intervention. Chem. Rev. 111, 6130-6185 (2011).
17. Vane, J. R. Biomedicine. Back to an aspirin a day- Science 296, 474-475 (2002).
18. Rajakariar, R., Yaqoob, M. M. & Gilroy, D. W. COX-2 in inflammation and resolution. Mol. Interv. 6, 199-207 (2006).
19. Chen, C. COX-2's new role in inflammation. Nat. Chem. Biol. 6, 401-402 (2010).
20. Norris, P. C. & Dennis, E. A. Omega-3 fatty acids cause dramatic changes in TLR4 and purinergic eicosanoid signaling. Proc. Natl Acad. Sci. USA 109, 8517-8522 (2012).
21. Smith, W. L., DeWitt, D. L. & Garavito, R. M. Cyclooxygenases: structural, cellular, and molecular biology. Annu. Rev. Biochem. 69, 145-182 (2000).
22. Kühn, H. & O'Donnell, V. B. Inflammation and immune regulation by 12/15-lipoxygenases. Prog. Lipid Res. 45, 334-356 (2006).
23. Norris, P. C., Reichart, D., Dumlao, D. S., Glass, C. K. & Dennis, E. A. Specificity of eicosanoid production depends on the TLR-4-stimulated macrophage phenotype. J. Leukocyte Biol. 90, 563-574 (2011).
24. Lawrence, T., Willoughby, D. A. & Gilroy, D. W. Anti-inflammatory lipid mediators and insights into the resolution of inflammation. Nat. Rev. Immunol. 2, 787-795 (2002).
25. Shinomiya, S. et al. Regulation of TNF- and interleukin-10 production by prostaglandins I2 and E2: studies with prostaglandin receptor-deficient mice and prostaglandin E-receptor subtype-selective synthetic agonists. Biochem. Pharmacol. 61, 1153-1160 (2001).
26. Samuelsson, B. Leukotrienes: mediators of immediate hypersensitivity reactions and inflammation. Science 220, 568-575 (1983).
27. Lammermann, T. et al. Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo. Nature 498, 371-375 (2013).
28. Murakami, K., Ide, T., Suzuki, M., Mochizuki, T. & Kadowaki, T. Evidence for direct binding of fatty acids and eicosanoids to human peroxisome proliferators-activated receptor -. Biochem. Biophys. Res. Commun. 260, 609-613 (1999).
29. Huang, J. T. et al. Interleukin-4-dependent production of PPAR-- ligands in macrophages by 12/15-lipoxygenase. Nature 400, 378-382 (1999).
30. Roman, R. J. P-450 metabolites of arachidonic acid in the control of cardiovascular function. Physiol. Rev. 82, 131-185 (2002).
31. von Moltke, J. et al. Rapid induction of inflammatory lipid mediators by the inflammasome in vivo. Nature 490, 107-111 (2012).
32. Bitto, A. et al. Flavocoxid, a dual inhibitor of COX-2 and 5-LOX of natural origin, attenuates the inflammatory response and protects mice from sepsis. Crit. Care 16, R32 (2012).
33. Balsinde, J., Balboa, M. A. & Dennis, E. A. Antisense inhibition of group VI Ca2+-independent phospholipase A2 blocks phospholipid fatty acid remodeling in murine P388D1 macrophages. J. Biol. Chem. 272, 29317-29321 (1997).
34. Fitzpatrick, F. A. & Soberman, R. Regulated formation of eicosanoids. J. Clin. Invest. 107, 1347-1351 (2001).
35. Buczynski, M. W. et al. TLR-4 and sustained calcium agonists synergistically produce eicosanoids independent of protein synthesis in RAW264.7 cells. J. Biol. Chem. 282, 22834-22847 (2007).
36. Naraba, H. et al. Segregated coupling of phospholipases A2, cyclooxygenases, and terminal prostanoid synthases in different phases of prostanoid biosynthesis in rat peritoneal macrophages. J. Immunol. 160, 2974-2982 (1998).
37. Brock, T. G., McNish, R. W. & Peters-Golden, M. Arachidonic acid is preferentially metabolized by cyclooxygenase-2 to prostacyclin and prostaglandin E2. J. Biol. Chem. 274, 11660-11666 (1999).
38. Mandal, A. K. et al. The nuclear membrane organization of leukotriene synthesis. Proc. Natl Acad. Sci. USA 105, 20434-20439 (2008).
39. Kihara, Y. et al. Modeling of eicosanoid fluxes reveals functional coupling between cyclooxygenases and terminal synthases. Biophys. J. 106, 966-975 (2014).
40. Folco, G. & Murphy, R. C. Eicosanoid transcellular biosynthesis: from cell-cell interactions to in vivo tissue responses. Pharmacol. Rev. 58, 375-388 (2006).
41. Chiang, N., Arita, M. & Serhan, C. N. Anti-inflammatory circuitry: lipoxin, aspirin-triggered lipoxins and their receptor ALX. Prostaglandins Leukot. Essent. Fatty Acids 73, 163-177 (2005).
42. Claria, J. & Serhan, C. N. Aspirin triggers previously undescribed bioactive eicosanoids by human endothelial cell-leukocyte interactions. Proc. Natl Acad. Sci. USA 92, 9475-9479 (1995).
43. Morris, T. et al. Effects of low-dose aspirin on acute inflammatory responses in humans. J. Immunol. 183, 2089-2096 (2009).
44. Levy, B. D., Clish, C. B., Schmidt, B., Gronert, K. & Serhan, C. N. Lipid mediator class switching during acute inflammation: signals in resolution. Nat. Immunol. 2, 612-619 (2001).
45. Chan, M. M. & Moore, A. R. Resolution of inflammation in murine autoimmune arthritis is disrupted by cyclooxygenase-2 inhibition and restored by prostaglandin E2-mediated lipoxin A4 production. J. Immunol. 184, 6418-6426 (2010).
46. Gasser, O. & Schifferli, J. A. Activated polymorphonuclear neutrophils disseminate anti-inflammatory microparticles by ectocytosis. Blood 104, 2543-2548 (2004).
47. Dalli, J. & Serhan, C. N. Specific lipid mediator signatures of human phagocytes: microparticles stimulate macrophage efferocytosis and pro-resolving mediators. Blood 120, e60-e72 (2012).
48. Miki, Y. et al. Lymphoid tissue phospholipase A2 group IID resolves contact hypersensitivity by driving antiinflammatory lipid mediators. J. Exp. Med. 210, 1217-1234 (2013).
49. Dioszeghy, V. et al. 12/15-Lipoxygenase regulates the inflammatory response to bacterial products in vivo. J. Immunol. 181, 6514-6524 (2008).
50. Li, P. et al. NCoR repression of LXRs restricts macrophage biosynthesis of insulin-sensitizing omega 3 fatty acids. Cell 155, 200-214 (2013).
51. Harmon, G. S. et al. Pharmacological correction of a defect in PPAR-- signaling ameliorates disease severity in Cftr-deficient mice. Nat. Med. 16, 313-318 (2010).
52. Mayer-Barber, K. D. & Sher, A. Cytokine and lipid mediator networks in tuberculosis. Immunol. Rev. 264, 264-275 (2015).
53. Tobin, D. M. et al. The lta4h locus modulates susceptibility to mycobacterial infection in zebrafish and humans. Cell 140, 717-730 (2010).
54. Mayer-Barber, K. D. et al. Host-directed therapy of tuberculosis based on interleukin-1 and type I interferon crosstalk. Nature 511, 99-103 (2014).
55. Coulombe, F. et al. Targeted prostaglandin E2 inhibition enhances antiviral immunity through induction of type I interferon and apoptosis in macrophages. Immunity 40, 554-568 (2014).
56. Blaho, V. A., Buczynski, M. W., Brown, C. R. & Dennis, E. A. Lipidomic analysis of dynamic eicosanoid responses during the induction and resolution of Lyme arthritis. J. Biol. Chem. 284, 21599-21612 (2009).
57. Blaho, V. A., Zhang, Y., Hughes-Hanks, J. M. & Brown, C. R. 5-lipoxygenase-deficient mice infected with Borrelia burgdorferi develop persistent arthritis. J. Immunol. 186, 3076-3084 (2011).
58. Blaho, V. A., Mitchell, W. J. & Brown, C. R. Arthritis develops but fails to resolve during inhibition of cyclooxygenase 2 in a murine model of Lyme disease. Arthritis Rheumatism 58, 1485-1495 (2008).
59. Maier, N. K., Leppla, S. H. & Moayeri, M. The cyclopentenone prostaglandin 15d-PGJ2 inhibits the NLRP1 and NLRP3 inflammasomes. J. Immunol. 194, 2776-2785 (2015).
60. Chiang, N. et al. Infection regulates pro-resolving mediators that lower antibiotic requirements. Nature 484, 524-528 (2012).
61. Morita, M. et al. The lipid mediator protectin D1 inhibits influenza virus replication and improves severe influenza. Cell 153, 112-125 (2013).
62. Tam, V. C. et al. Lipidomic profiling of influenza infection identifies mediators that induce and resolve inflammation. Cell 154, 213-227 (2013).
63. Ramon, S. et al. The specialized proresolving mediator 17-HDHA enhances the antibody-mediated immune response against influenza virus: a new class of adjuvant- J. Immunol. 193, 6031-6040 (2014).
64. Aharony, D. Pharmacology of leukotriene receptor antagonists. Am. J. Respiratory Crit. Care Med. 157, S214-218; discussion S218-S219, S247-S248 (1998).
65. Wang, Y., Armando, A. M., Quehenberger, O., Yan, C. & Dennis, E. A. Comprehensive ultra-performance liquid chromatographic separation and mass spectrometric analysis of eicosanoid metabolites in human samples. Journal of Chromatogr. A. 1359, 60-69 (2014).
66. Kliewer, S. A. et al. Fatty acids and eicosanoids regulate gene expression through direct interactions with peroxisome proliferator-activated receptors - and -. Proc. Natl Acad. Sci. USA 94, 4318-4323 (1997).
67. Chou, W. L. et al. Identification of a novel prostaglandin reductase reveals the involvement of prostaglandin E2 catabolism in regulation of peroxisome proliferator-activated receptor - activation. J. Biol. Chem. 282, 18162-18172 (2007).
68. Baker, P. R. et al. Fatty acid transduction of nitric oxide signaling: multiple nitrated unsaturated fatty acid derivatives exist in human blood and urine and serve as endogenous peroxisome proliferator-activated receptor ligands. J. Biol. Chem. 280, 42464-42475 (2005).
69. Groeger, A. L. et al. Cyclooxygenase-2 generates anti-inflammatory mediators from omega-3 fatty acids. Nat. Chem. Biol. 6, 433-441 (2010).
70. Ricciotti, E. & FitzGerald, G. A. Prostaglandins and inflammation. Arterioscler. Thromb. Vascular Biol. 31, 986-1000 (2011).
71. Passarelli, M. K., Ewing, A. G. & Winograd, N. Single-cell lipidomics: characterizing and imaging lipids on the surface of individual Aplysia californica neurons with cluster secondary ion mass spectrometry. Anal. Chem. 85, 2231-2238 (2013).
72. Zemski Berry, K. A., Gordon, W. C., Murphy, R. C. & Bazan, N. G. Spatial organization of lipids in the human retina and optic nerve by MALDI imaging mass spectrometry. J. Lipid Res. 55, 504-515 (2014).
73. Fitzgerald, D. J. & Fitzgerald, G. A. Historical lessons in translational medicine: cyclooxygenase inhibition and P2Y12 antagonism. Circul. Res. 112, 174-194 (2013).
74. Patrono, C. & Baigent, C. Nonsteroidal anti-inflammatory drugs and the heart. Circulation 129, 907-916 (2014).
75. Serhan, C. N., Hamberg, M. & Samuelsson, B. Lipoxins: novel series of biologically active compounds formed from arachidonic acid in human leukocytes. Proc. Natl Acad. Sci. USA 81, 5335-5339 (1984).
76. Mukherjee, P. K., Marcheselli, V. L., Serhan, C. N. & Bazan, N. G. Neuroprotectin D1: a docosahexaenoic acid-derived docosatriene protects human retinal pigment epithelial cells from oxidative stress. Proc. Natl Acad. Sci. USA 101, 8491-8496 (2004).
77. Marcheselli, V. L. et al. Novel docosanoids inhibit brain ischemia-reperfusion-mediated leukocyte infiltration and pro-inflammatory gene expression. J. Biol. Chem. 278, 43807-43817 (2003).
78. Dalli, J., Chiang, N. & Serhan, C. N. Identification of 14-series sulfido-conjugated mediators that promote resolution of infection and organ protection. Proc. Natl Acad. Sci. USA 111, E4753-E4761 (2014).
79. Morimoto, K. et al. Prostaglandin E2-EP3 signaling induces inflammatory swelling by mast cell activation. J. Immunol. 192, 1130-1137 (2014).
80. Bray, M. A., Cunningham, F. M., Ford-Hutchinson, A. W. & Smith, M. J. Leukotriene B4: a mediator of vascular permeability. Br. J. Pharmacol. 72, 483-486 (1981).
81. Minami, T. et al. Characterization of EP receptor subtypes responsible for prostaglandin E2-induced pain responses by use of EP1 and EP3 receptor knockout mice. Br. J. Pharmacol. 133, 438-444 (2001).
82. Lin, C. R. et al. Prostaglandin E2 receptor EP4 contributes to inflammatory pain hypersensitivity. J. Pharmacol. Exp. Ther. 319, 1096-1103 (2006).
83. Moriyama, T. et al. Sensitization of TRPV1 by EP1 and IP reveals peripheral nociceptive mechanism of prostaglandins. Mol. Pain 1, 3 (2005).
84. Lazarus, M. et al. EP3 prostaglandin receptors in the median preoptic nucleus are critical for fever responses. Nat. Neurosci. 10, 1131-1133 (2007).
85. Treffkorn, L., Scheibe, R., Maruyama, T. & Dieter, P. PGE2 exerts its effect on the LPS-induced release of TNF-alpha, ET-1, IL-1alpha, IL-6 and IL-10 via the EP2 and EP4 receptor in rat liver macrophages. Prostaglandins Other Lipid Mediat. 74, 113-123 (2004).
86. Jakobsson, P. J., Thoren, S., Morgenstern, R. & Samuelsson, B. Identification of human prostaglandin E synthase: a microsomal, glutathione-dependent, inducible enzyme, constituting a potential novel drug target. Proc. Natl Acad. Sci. USA 96, 7220-7225 (1999).
87. Cheng, K. et al. Antagonism of the prostaglandin D2 receptor 1 suppresses nicotinic acid-induced vasodilation in mice and humans. Proc. Natl Acad. Sci. USA 103, 6682-6687 (2006).
88. Liang, X., Wu, L., Hand, T. & Andreasson, K. Prostaglandin D2 mediates neuronal protection via the DP1 receptor. J. Neurochem. 92, 477-486 (2005).
89. Taketomi, Y. et al. Mast cell maturation is driven via a group III phospholipase A2-prostaglandin D2-DP1 receptor paracrine axis. Nat. Immunol. 14, 554-563 (2013).
90. Spik, I. et al. Activation of the prostaglandin D2 receptor DP2/CRTH2 increases allergic inflammation in mouse. J. Immunol. 174, 3703-3708 (2005).
91. Schratl, P. et al. The role of the prostaglandin D2 receptor, DP, in eosinophil trafficking. J. Immunol. 179, 4792-4799 (2007).
92. Kliewer, S. A. et al. A prostaglandin J2 metabolite binds peroxisome proliferator-activated receptor gamma and promotes adipocyte differentiation. Cell 83, 813-819 (1995).
93. Forman, B. M. et al. 15-Deoxy--12,14-prostaglandin J2 is a ligand for the adipocyte determination factor PPAR-. Cell 83, 803-812 (1995).
94. Basu, S. Novel cyclooxygenase-catalyzed bioactive prostaglandin F2- from physiology to new principles in inflammation. Med. Res. Rev. 27, 435-468 (2007).
95. Woodward, D. F. et al. Prostaglandin F2 alpha effects on intraocular pressure negatively correlate with FP-receptor stimulation. Investigative Ophthalmol. Visual Sci. 30, 1838-1842 (1989).
96. Moncada, S., Herman, A. G., Higgs, E. A. & Vane, J. R. Differential formation of prostacyclin (PGX or PGI2) by layers of the arterial wall. An explanation for the anti-thrombotic properties of vascular endothelium. Thromb. Res. 11, 323-344 (1977).
97. Murata, T. et al. Altered pain perception and inflammatory response in mice lacking prostacyclin receptor. Nature 388, 678-682 (1997).
98. Weiss, H. J. & Turitto, V. T. Prostacyclin (prostaglandin I2, PGI2) inhibits platelet adhesion and thrombus formation on subendothelium. Blood 53, 244-250 (1979).
99. Lim, H. et al. Cyclo-oxygenase-2-derived prostacyclin mediates embryo implantation in the mouse via PPAR-. Genes Dev. 13, 1561-1574 (1999).
100. Gupta, R. A. et al. Prostacyclin-mediated activation of peroxisome proliferator-activated receptor - in colorectal cancer. Proc. Natl Acad. Sci. USA 97, 13275-13280 (2000).
101. Hartwig, J. H. et al. Thrombin receptor ligation and activated Rac uncap actin filament barbed ends through phosphoinositide synthesis in permeabilized human platelets. Cell 82, 643-653 (1995).
102. Auch-Schwelk, W., Katusic, Z. S. & Vanhoutte, P. M. Thromboxane A2 receptor antagonists inhibit endothelium-dependent contractions. Hypertension 15, 699-703 (1990).
103. Cogolludo, A., Moreno, L., Bosca, L., Tamargo, J. & Perez-Vizcaino, F. Thromboxane A2-induced inhibition of voltage-gated K+ channels and pulmonary vasoconstriction: role of protein kinase C-. Circul. Res. 93, 656-663 (2003).
104. Kabashima, K. et al. Thromboxane A2 modulates interaction of dendritic cells and T cells and regulates acquired immunity. Nat. Immunol. 4, 694-701 (2003).
105. Iizuka, Y. et al. Protective role of the leukotriene B4 receptor BLT2 in murine inflammatory colitis. FASEB J. 24, 4678-4690 (2010).
106. Narala, V. R. et al. Leukotriene B4 is a physiologically relevant endogenous peroxisome proliferator-activated receptor-- agonist. J. Biol. Chem. 285, 22067-22074 (2010).
107. Devchand, P. R. et al. The PPAR--leukotriene B4 pathway to inflammation control. Nature 384, 39-43 (1996).
108. Moos, M. P. et al. Cysteinyl leukotriene 2 receptor-mediated vascular permeability via transendothelial vesicle transport. FASEB J. 22, 4352-4362 (2008).
109. Hwang, S. W. et al. Direct activation of capsaicin receptors by products of lipoxygenases: endogenous capsaicin-like substances. Proc. Natl Acad. Sci. USA 97, 6155-6160 (2000).
110. Ng, V. Y. et al. Cytochrome P450 eicosanoids are activators of peroxisome proliferator-activated receptor -. Drug Metabolism Dispos. 35, 1126-1134 (2007).
111. Liu, Y. et al. The antiinflammatory effect of laminar flow: the role of PPAR-, epoxyeicosatrienoic acids, and soluble epoxide hydrolase. Proc. Natl Acad. Sci. USA 102, 16747-16752 (2005).
112. Inceoglu, B., Schmelzer, K. R., Morisseau, C., Jinks, S. L. & Hammock, B. D. Soluble epoxide hydrolase inhibition reveals novel biological functions of epoxyeicosatrienoic acids (EETs). Prostaglandins Other Lipid Mediat. 82, 42-49 (2007).
113. Gregus, A. M. et al. Spinal 12-lipoxygenase-derived hepoxilin A3 contributes to inflammatory hyperalgesia via activation of TRPV1 and TRPA1 receptors. Proc. Natl Acad. Sci. USA 109, 6721-6726 (2012).
114. Mrsny, R. J. et al. Identification of hepoxilin A3 in inflammatory events: a required role in neutrophil migration across intestinal epithelia. Proc. Natl Acad. Sci. USA 101, 7421-7426 (2004).
115. Hurley, B. P., Siccardi, D., Mrsny, R. J. & McCormick, B. A. Polymorphonuclear cell transmigration induced by Pseudomonas aeruginosa requires the eicosanoid hepoxilin A3. J. Immunol. 173, 5712-5720 (2004).
116. Nigam, S., Zafiriou, M. P., Deva, R., Ciccoli, R. & Roux-Van der Merwe, R. Structure, biochemistry and biology of hepoxilins: an update. FEBS J. 274, 3503-3512 (2007).
117. Hammond, V. J. & O'Donnell, V. B. Esterified eicosanoids: generation, characterization and function. Biochim. Biophys. Acta 1818, 2403-2412 (2012).
118. Brezinski, M. E. & Serhan, C. N. Selective incorporation of (15S)-hydroxyeicosatetraenoic acid in phosphatidylinositol of human neutrophils: agonist-induced deacylation and transformation of stored hydroxyeicosanoids. Proc. Natl Acad. Sci. USA 87, 6248-6252 (1990).
119. Rouzer, C. A. & Marnett, L. J. Non-redundant functions of cyclooxygenases: oxygenation of endocannabinoids. J. Biol. Chem. 283, 8065-8069 (2008).
120. Trostchansky, A. et al. Nitroarachidonic acid, a novel peroxidase inhibitor of prostaglandin endoperoxide H synthases 1 and 2. J. Biol. Chem. 286, 12891-12900 (2011).