Is Resolution the End of Inflammation?

Trends in Molecular Medicine - Tập 25 - Trang 198-214 - 2019
Karen T. Feehan1, Derek W. Gilroy1
1Centre for Clinical Pharmacology and Therapeutics, Division of Medicine, 5 University Street, University College London, London WC1E 6JF, UK

Tài liệu tham khảo

Takeuchi, 2010, Pattern recognition receptors and inflammation, Cell, 140, 805, 10.1016/j.cell.2010.01.022 Ala, 2003, Role of cell adhesion molecules in leukocyte recruitment in the liver and gut, Int. J. Exp. Pathol., 84, 1, 10.1046/j.1365-2613.2003.00235.x Kolaczkowska, 2013, Neutrophil recruitment and function in health and inflammation, Nat. Rev. Immunol., 13, 159, 10.1038/nri3399 Smolen, 2003, Therapeutic strategies for rheumatoid arthritis, Nat. Rev. Drug Discov., 2, 473, 10.1038/nrd1109 Shao, 2011, Disturbances of apoptotic cell clearance in systemic lupus erythematosus, Arthritis Res. Ther., 13, 202, 10.1186/ar3206 Dinauer, 1993, The respiratory burst oxidase and the molecular genetics of chronic granulomatous disease, Crit. Rev. Clin. Lab. Sci., 30, 329, 10.3109/10408369309082591 Morgenstern, 1997, 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, 207, 10.1084/jem.185.2.207 Buckley, 2014, Proresolving lipid mediators and mechanisms in the resolution of acute inflammation, Immunity, 40, 315, 10.1016/j.immuni.2014.02.009 Buckley, 2013, The resolution of inflammation, Nat. Rev. Immunol., 13, 59, 10.1038/nri3362 Serhan, 2007, Resolution of inflammation: state of the art, definitions and terms, FASEB J., 21, 325, 10.1096/fj.06-7227rev Winkelstein, 2000, Chronic granulomatous disease. Report on a national registry of 368 patients, Medicine, 79, 155, 10.1097/00005792-200005000-00003 Armstrong, 1971, Response of cultured macrophages to Mycobacterium tuberculosis, with observations on fusion of lysosomes with phagosomes, J. Exp. Med., 134, 713, 10.1084/jem.134.3.713 Sturgill-Koszycki, 1994, Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase, Science, 263, 678, 10.1126/science.8303277 Matsumura, 2010, Identification of BCAP-L as a negative regulator of the TLR signaling-induced production of IL-6 and IL-10 in macrophages by tyrosine phosphoproteomics, Biochem. Biophys. Res. Commun., 400, 265, 10.1016/j.bbrc.2010.08.055 Chandel, 2000, Role of oxidants in NF-κB activation and TNF-α gene transcription induced by hypoxia and endotoxin, J. Immunol., 165, 1013, 10.4049/jimmunol.165.2.1013 Seymour, 2001, Anti-TNF agents for rheumatoid arthritis, Br. J. Clin. Pharmacol., 51, 201, 10.1046/j.1365-2125.2001.00321.x Akira, 2004, Toll-like receptor signalling, Nat. Rev. Immunol., 4, 499, 10.1038/nri1391 Liu, 2013, Identification and characterization of a unique leucine-rich repeat protein (LRRC33) that inhibits Toll-like receptor-mediated NF-κB activation, Biochem. Biophys. Res. Commun., 434, 28, 10.1016/j.bbrc.2013.03.071 Gilroy, 2015, New insights into the resolution of inflammation, Semin. Immunol., 27, 161, 10.1016/j.smim.2015.05.003 Perretti, 1996, Mobilizing lipocortin 1 in adherent human leukocytes downregulates their transmigration, Nat. Med., 2, 1259, 10.1038/nm1196-1259 Ryan, 1977, Acute inflammation. A review, Am. J. Pathol., 86, 183 Henson, 1987, Tissue injury in inflammation Oxidants, proteinases, and cationic proteins, J. Clin. Investig., 79, 669, 10.1172/JCI112869 Weiss, 1989, Tissue destruction by neutrophils, N. Engl. J. Med., 320, 365, 10.1056/NEJM198902093200606 Dean, 2008, Macrophage-specific metalloelastase (MMP-12) truncates and inactivates ELR+ CXC chemokines and generates CCL2,-7,-8, and-13 antagonists: potential role of the macrophage in terminating polymorphonuclear leukocyte influx, Blood, 112, 3455, 10.1182/blood-2007-12-129080 Charo, 2006, The many roles of chemokines and chemokine receptors in inflammation, N. Engl. J. Med., 354, 610, 10.1056/NEJMra052723 Nibbs, 2001, The β-chemokine receptor D6 is expressed by lymphatic endothelium and a subset of vascular tumors, Am. J. Pathol., 158, 867, 10.1016/S0002-9440(10)64035-7 Di Liberto, 2008, Role of the chemokine decoy receptor D6 in balancing inflammation: immune activation, and antimicrobial resistance in Mycobacterium tuberculosis infection, J. Exp. Med., 205, 2075, 10.1084/jem.20070608 Murphy, 2000, International union of pharmacology. XXII. Nomenclature for chemokine receptors, Pharmacol. Rev., 52, 145 Jamieson, 2005, The chemokine receptor D6 limits the inflammatory response in vivo, Nat. Immunol., 6, 403, 10.1038/ni1182 Henson, 2003, The final step in programmed cell death: phagocytes carry apoptotic cells to the grave, Essays Biochem., 39, 105, 10.1042/bse0390105 Da Silva, 2009, Cell death during sepsis: integration of disintegration in the inflammatory response to overwhelming infection, Apoptosis, 14, 509, 10.1007/s10495-009-0320-3 Savill, 1997, Apoptosis in resolution of inflammation, J. Leukoc. Biol., 61, 375, 10.1002/jlb.61.4.375 Lauber, 2004, Clearance of apoptotic cells: getting rid of the corpses, Mol. Cell, 14, 277, 10.1016/S1097-2765(04)00237-0 Fadok, 2001, Phagocyte receptors for apoptotic cells: recognition, uptake, and consequences, J. Clin. Investig., 108, 957, 10.1172/JCI200114122 Mandal, 2005, Fas-, caspase 8-, and caspase 3-dependent signaling regulates the activity of the aminophospholipid translocase and phosphatidylserine externalization in human erythrocytes, J. Biol. Chem., 280, 39460, 10.1074/jbc.M506928200 Bratton, 2008, Apoptotic cell recognition: will the real phosphatidylserine receptor (s) please stand up?, Curr. Biol., 18, R76, 10.1016/j.cub.2007.11.024 Miyanishi, 2007, Identification of Tim4 as a phosphatidylserine receptor, Nature, 450, 435, 10.1038/nature06307 Kobayashi, 2007, TIM-1 and TIM-4 glycoproteins bind phosphatidylserine and mediate uptake of apoptotic cells, Immunity, 27, 927, 10.1016/j.immuni.2007.11.011 Kuchroo, 2008, New roles for TIM family members in immune regulation, Nat. Rev. Immunol., 8, 577, 10.1038/nri2366 Bystrom, 2008, Resolution-phase macrophages possess a unique inflammatory phenotype that is controlled by cAMP, Blood, 112, 4117, 10.1182/blood-2007-12-129767 Ariel, 2012, New lives given by cell death: macrophage differentiation following their encounter with apoptotic leukocytes during the resolution of inflammation, Front. Immunol., 3, 4, 10.3389/fimmu.2012.00004 Fadok, 1998, Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF, J. Clin. Investig., 101, 890, 10.1172/JCI1112 Schwab, 2007, Resolvin E1 and protectin D1 activate inflammation-resolution programmes, Nature, 447, 869, 10.1038/nature05877 Serhan, 2012, Macrophage proresolving mediator maresin 1 stimulates tissue regeneration and controls pain, FASEB J., 26, 1755, 10.1096/fj.11-201442 Munoz, 2008, Apoptosis in the pathogenesis of systemic lupus erythematosus, Lupus, 17, 371, 10.1177/0961203308089990 Grabiec, 2016, The role of airway macrophages in apoptotic cell clearance following acute and chronic lung inflammation, Semin. Immunopathol., 38, 409, 10.1007/s00281-016-0555-3 Grabiec, 2017, Diminished airway macrophage expression of the Axl receptor tyrosine kinase is associated with defective efferocytosis in asthma, J. Allergy Clin. Immunol., 140, 1144, 10.1016/j.jaci.2017.03.024 Firestein, 1995, Apoptosis in rheumatoid arthritis synovium, J. Clin. Investig., 96, 1631, 10.1172/JCI118202 Ariel, 2006, Apoptotic neutrophils and T cells sequester chemokines during immune response resolution through modulation of CCR5 expression, Nat. Immunol., 7, 1209, 10.1038/ni1392 Botto, 1998, Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies, Nat. Genet., 19, 56, 10.1038/ng0598-56 Tager, 2003, BLT1 and BLT2: the leukotriene B4 receptors, Prostaglandins Leukot Essent Fatty Acids, 69, 123, 10.1016/S0952-3278(03)00073-5 Crooks, 1998, Leukotriene B4, Int. J. Biochem. Cell Biol., 30, 173, 10.1016/S1357-2725(97)00123-4 Cannetti, 2003, IL-18 enhances collagen-induced arthritis by recruiting neutrophils via TNF-α and leukotriene B4, J. Immunol., 171, 1009, 10.4049/jimmunol.171.2.1009 Arita, 2007, Resolvin E1 selectively interacts with leukotriene B4 receptor BLT1 and ChemR23 to regulate inflammation, J. Immunol., 178, 3912, 10.4049/jimmunol.178.6.3912 Krishnamoorthy, 2010, Resolvin D1 binds human phagocytes with evidence for proresolving receptors, Proc. Natl. Acad. Sci. U. S. A., 107, 1660, 10.1073/pnas.0907342107 Fullerton, 2016, Resolution of inflammation: a new therapeutic frontier, Nat. Rev. Drug Discov., 15, 551, 10.1038/nrd.2016.39 Arita, 2005, Stereochemical assignment, antiinflammatory properties, and receptor for the omega-3 lipid mediator resolvin E1, J. Exp. Med., 201, 713, 10.1084/jem.20042031 Ohira, 2010, Resolvin E1 receptor activation signals phosphorylation and phagocytosis, J. Biol. Chem., 285, 3451, 10.1074/jbc.M109.044131 Schett, 2018, Resolution of chronic inflammatory disease: universal and tissue-specific concepts, Nat. Commun., 9, 3261, 10.1038/s41467-018-05800-6 Newson, 2014, Resolution of acute inflammation bridges the gap between innate and adaptive immunity, Blood, 124, 1748, 10.1182/blood-2014-03-562710 Newson, 2017, Inflammatory resolution triggers a prolonged phase of immune suppression through COX-1/mPGES-1-derived prostaglandin E, Cell Rep., 20, 3162, 10.1016/j.celrep.2017.08.098 da Fonseca, 2015, Microbiota-dependent sequelae of acute infection compromise tissue-specific immunity, Cell, 163, 354, 10.1016/j.cell.2015.08.030 Collins, 2017, Sustained accumulation of antigen-presenting cells after infection promotes local T-cell immunity, Immunol. Cell Biol., 95, 878, 10.1038/icb.2017.60 Yona, 2013, Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis, Immunity, 38, 79, 10.1016/j.immuni.2012.12.001 Turnbull, 2006, Cutting edge: TREM-2 attenuates macrophage activation, J. Immunol., 177, 3520, 10.4049/jimmunol.177.6.3520 Wu, 2015, TREM-2 promotes macrophage survival and lung disease after respiratory viral infection, J. Exp. Med., 212, 681, 10.1084/jem.20141732 Avraham-Davidi, 2013, On-site education of VEGF-recruited monocytes improves their performance as angiogenic and arteriogenic accessory cells, J. Exp. Med., 210, 2611, 10.1084/jem.20120690 Motwani, 2016, Novel translational model of resolving inflammation triggered by UV-killed E. coli, J. Pathol.: Clin. Res., 2, 154 Motwani, 2017, Prolonged immune alteration following resolution of acute inflammation in humans, PLoS One, 12, 10.1371/journal.pone.0186964 Serhan, 2005, Resolution of inflammation: the beginning programs the end, Nat. Immunol., 6, 1191, 10.1038/ni1276 Cope, 1997, Chronic tumor necrosis factor alters T cell responses by attenuating T cell receptor signaling, J. Exp. Med., 185, 1573, 10.1084/jem.185.9.1573 Smith, 1992, Prostanoid biosynthesis and mechanisms of action, Am. J. Physiol. Renal Physiol., 263, F181, 10.1152/ajprenal.1992.263.2.F181 Vane, 1971, Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs, Nat. New Biol., 231, 232, 10.1038/newbio231232a0 Silverstein, 2000, Gastrointestinal toxicity with celecoxib vs nonsteroidal anti-inflammatory drugs for osteoarthritis and rheumatoid arthritis: the CLASS study: a randomized controlled trial, JAMA, 284, 1247, 10.1001/jama.284.10.1247 Baker, 1981, Prostaglandin inhibition of T-cell proliferation is mediated at two levels, Cell. Immunol., 61, 52, 10.1016/0008-8749(81)90353-1 Betz, 1991, Prostaglandin E2 inhibits production of Th1 lymphokines but not of Th2 lymphokines, J. Immunol., 146, 108, 10.4049/jimmunol.146.1.108 Mao, 2014, Inhibition of tumor-derived prostaglandin-e2 blocks the induction of myeloid-derived suppressor cells and recovers natural killer cell activity, Clin. Cancer Res., 20, 4096, 10.1158/1078-0432.CCR-14-0635 Obermajer, 2012, Generation of myeloid-derived suppressor cells using prostaglandin E 2, Transplant. Res., 1, 15, 10.1186/2047-1440-1-15 Obermajer, 2011, Positive feedback between PGE2 and COX2 redirects the differentiation of human dendritic cells towards stable myeloid-derived suppressor cells, Blood, 118, 5498, 10.1182/blood-2011-07-365825 Obermajer, 2011, PGE2-dependent CXCL12 production and CXCR4 expression control the accumulation of human MDSCs in ovarian cancer environment, Cancer Res., 71, 7463, 10.1158/0008-5472.CAN-11-2449 Stokes Peebles, 2002, Selective cyclooxygenase-1 and-2 inhibitors each increase allergic inflammation and airway hyperresponsiveness in mice, Am. J. Respir. Crit. Care Med., 165, 1154, 10.1164/ajrccm.165.8.2106025 Lundequist, 2010, Prostaglandin E2 exerts homeostatic regulation of pulmonary vascular remodeling in allergic airway inflammation, J. Immunol., 184, 433, 10.4049/jimmunol.0902835 Kunikata, 2005, Suppression of allergic inflammation by the prostaglandin E receptor subtype EP3, Nat. Immunol., 6, 524, 10.1038/ni1188 Shiraishi, 2008, Prostaglandin E2 is a major soluble factor produced by stromal cells for preventing inflammatory cytokine production from dendritic cells, Int. Immunol., 20, 1219, 10.1093/intimm/dxn078 Koga, 2009, Cyclic adenosine monophosphate suppresses the transcription of proinflammatory cytokines via the phosphorylated c-Fos protein, Immunity, 30, 372, 10.1016/j.immuni.2008.12.021 Zamuner, 2005, Predisposition to colorectal cancer in rats with resolved colitis: role of cyclooxygenase-2-derived prostaglandin d2, Am. J. Pathol., 167, 1293, 10.1016/S0002-9440(10)61216-3 Bell, 1995, Disruption of colonic electrolyte transport in experimental colitis, Am. J. Physiol. Gastrointest. Liver Physiol., 268, G622, 10.1152/ajpgi.1995.268.4.G622 Kachur, 1995, Colitis reduces short-circuit current response to inflammatory mediators in rat colonic mucosa, Inflammation, 19, 245, 10.1007/BF01534465 Didierlaurent, 2008, Sustained desensitization to bacterial Toll-like receptor ligands after resolutionof respiratory influenza infection, J. Exp. Med., 205, 323, 10.1084/jem.20070891 Snelgrove, 2008, A critical function for CD200 in lung immune homeostasis and the severity of influenza infection, Nat. Immunol., 9, 1074, 10.1038/ni.1637 Kaur, 2015, Macrophage adaptation in airway inflammatory resolution, Eur. Respir. Rev., 24, 510, 10.1183/16000617.0030-2015 Goulding, 2011, Lowering the threshold of lung innate immune cell activation alters susceptibility to secondary bacterial superinfection, J. Infect. Dis., 204, 1086, 10.1093/infdis/jir467 Fujinami, 1983, Molecular mimicry in virus infection: crossreaction of measles virus phosphoprotein or of herpes simplex virus protein with human intermediate filaments, Proc. Natl. Acad. Sci. U. S. A., 80, 2346, 10.1073/pnas.80.8.2346 Fujinami, 2006, Molecular mimicry, bystander activation, or viral persistence: infections and autoimmune disease, Clin. Microbiol. Rev., 19, 80, 10.1128/CMR.19.1.80-94.2006 Woodland, 1992, Retroviral super-antigens and T cells, Int. Rev. Immunol., 8, 311, 10.3109/08830189209053515 Teijaro, 2013, Persistent LCMV infection is controlled by blockade of type I interferon signaling, Science, 340, 207, 10.1126/science.1235214 Wilson, 2013, Blockade of chronic type I interferon signaling to control persistent virus infection (P6048), J. Immunol., 190, 10.4049/jimmunol.190.Supp.49.7 O’Connor, 2006, Emerging infectious determinants of chronic diseases, Emerg. Infect. Dis., 12, 1051, 10.3201/eid1207.060037 Lucey, 2005, Mesenteric lymph nodes seen at imaging: causes and significance, Radiographics, 25, 351, 10.1148/rg.252045108 Huppert, 2004, Diagnosis of cavitating mesenteric lymph node syndrome in celiac disease using MRI, Am. J. Roentgenol., 183, 1375, 10.2214/ajr.183.5.1831375 Rivas, 2011, Deep resequencing of GWAS loci identifies independent rare variants associated with inflammatory bowel disease, Nat. Genet., 43, 1066, 10.1038/ng.952 Belkaid, 2014, Role of the microbiota in immunity and inflammation, Cell, 157, 121, 10.1016/j.cell.2014.03.011 Walter, 2002, Viral induction of a chronic asthma phenotype and genetic segregation from the acute response, J. Clin. Investig., 110, 165, 10.1172/JCI0214345 Crapster-Pregont, 2012, Dendritic cells and alveolar macrophages mediate IL-13-induced airway inflammation and chemokine production, J. Allergy Clin. Immunol., 129, 1621, 10.1016/j.jaci.2012.01.052 Kuperman, 2002, Direct effects of interleukin-13 on epithelial cells cause airway hyperreactivity and mucus overproduction in asthma, Nat. Med., 8, 885, 10.1038/nm734 Chinen, 2011, Prostaglandin E2 and SOCS1 have a role in intestinal immune tolerance, Nat. Commun., 2, 190, 10.1038/ncomms1181 De Heer, 2004, Essential role of lung plasmacytoid dendritic cells in preventing asthmatic reactions to harmless inhaled antigen, J. Exp. Med., 200, 89, 10.1084/jem.20040035 Machado, 2008, Role of lipoxin in the modulation of immune response during infection, Int. Immunopharmacol., 8, 1316, 10.1016/j.intimp.2008.01.001 Serhan, 2008, Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators, Nat. Rev. Immunol., 8, 349, 10.1038/nri2294 Recchiuti, 2013, Resolvin D1 and its GPCRs in resolution circuits of inflammation, Prostaglandins Other Lipid Mediat., 107, 64, 10.1016/j.prostaglandins.2013.02.004 Chen, 2014, Annexin 1: a glucocorticoid-inducible protein that modulates inflammatory pain, Eur. J. Pain, 18, 338, 10.1002/j.1532-2149.2013.00373.x Scannell, 2007, Annexin-1 and peptide derivatives are released by apoptotic cells and stimulate phagocytosis of apoptotic neutrophils by macrophages, J. Immunol., 178, 4595, 10.4049/jimmunol.178.7.4595 Kourtzelis, 2018, DEL-1 promotes macrophage efferocytosis and clearance of inflammation, Nat. Immunol., 20, 40, 10.1038/s41590-018-0249-1 Lawrence, 2010, The resolution of inflammation: anti-inflammatory roles for NF-κB, Int. J. Biochem. Cell Biol., 42, 519, 10.1016/j.biocel.2009.12.016 Ariel, 2006, Apoptotic neutrophils and T cells sequester chemokines during immune response resolution through modulation of CCR5 expression, Nat. Immunol., 7, 1209, 10.1038/ni1392 Fong, 2008, An antiinflammatory role for IKKβ through the inhibition of “classical” macrophage activation, J. Exp. Med., 205, 1269, 10.1084/jem.20080124 Sousa, 2009, Cyclic AMP enhances resolution of allergic pleurisy by promoting inflammatory cell apoptosis via inhibition of PI3K/Akt and NF-κB, Biochem. Pharmacol., 78, 396, 10.1016/j.bcp.2009.04.030 Rodrigues, 2010, Absence of PI3Kγ leads to increased leukocyte apoptosis and diminished severity of experimental autoimmune encephalomyelitis, J. Neuroimmunol., 222, 90, 10.1016/j.jneuroim.2010.02.016 Sousa, 2010, PDE4 inhibition drives resolution of neutrophilic inflammation by inducing apoptosis in a PKA-PI3K/Akt-dependent and NF-κB-independent manner, J. Leukoc. Biol., 87, 895, 10.1189/jlb.0809540 Sawatzky, 2006, The involvement of the apoptosis-modulating proteins ERK 1/2, Bcl-xL and Bax in the resolution of acute inflammation in vivo, Am. J. Pathol., 168, 33, 10.2353/ajpath.2006.050058 Rossi, 1998, Regulation of macrophage phagocytosis of apoptotic cells by cAMP, J. Immunol., 160, 3562, 10.4049/jimmunol.160.7.3562 Divanovic, 2005, Negative regulation of Toll-like receptor 4 signaling by the Toll-like receptor homolog RP105, Nat. Immunol., 6, 571, 10.1038/ni1198 Taganov, 2006, NF-κB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses, Proc. Natl. Acad. Sci. U. S. A., 103, 12481, 10.1073/pnas.0605298103 Sheedy, 2010, Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21, Nat. Immunol., 11, 141, 10.1038/ni.1828 Huber, 1991, Regulation of transendothelial neutrophil migration by endogenous interleukin-8, Science, 254, 99, 10.1126/science.1718038 Paccaud, 1990, NAP-1IL-8 induces up-regulation of CR1 receptors in human neutrophil leukocytes, Biochem. Biophys. Res. Commun., 166, 187, 10.1016/0006-291X(90)91929-M Schenk, 2002, Platelet-derived chemokines CXC chemokine ligand (CXCL) 7, connective tissue-activating peptide III, and CXCL4 differentially affect and cross-regulate neutrophil adhesion and transendothelial migration, J. Immunol., 169, 2602, 10.4049/jimmunol.169.5.2602 Farber, 1993, HuMig: a new human member of the chemokine family of cytokines, Biochem. Biophys. Res. Commun., 192, 223, 10.1006/bbrc.1993.1403 Luster, 1985, γ-Interferon transcriptionally regulates an early-response gene containing homology to platelet proteins, Nature, 315, 672, 10.1038/315672a0 Jiang, 1990, Post-translational modification of a monocyte-specific chemoattractant synthesized by glioma, osteosarcoma, and vascular smooth muscle cells, J. Biol. Chem., 265, 18318, 10.1016/S0021-9258(17)44754-5 Deshmane, 2009, Monocyte chemoattractant protein-1 (MCP-1): an overview, J. Interferon Cytokine Res., 29, 313, 10.1089/jir.2008.0027 Taguchi, 1998, Patterns for RANTES secretion and intercellular adhesion molecule 1 expression mediate transepithelial T cell traffic based on analyses in vitro and in vivo, J. Exp. Med., 187, 1927, 10.1084/jem.187.12.1927 Opdenakker, 1993, Human monocyte chemotactic protein-3 (MCP-3): molecular cloning of the cDNA and comparison with other chemokines, Biochem. Biophys. Res. Commun., 191, 535, 10.1006/bbrc.1993.1251 Van Damme, 1992, Structural and functional identification of two human, tumor-derived monocyte chemotactic proteins (MCP-2 and MCP-3) belonging to the chemokine family, J. Exp. Med., 176, 59, 10.1084/jem.176.1.59 Garcia-Zepeda, 1996, Human monocyte chemoattractant protein (MCP)-4 is a novel CC chemokine with activities on monocytes, eosinophils, and basophils induced in allergic and nonallergic inflammation that signals through the CC chemokine receptors (CCR)-2 and-3, J. Immunol., 157, 5613, 10.4049/jimmunol.157.12.5613 Uguccioni, 1996, Monocyte chemotactic protein 4 (MCP-4), a novel structural and functional analogue of MCP-3 and eotaxin, J. Exp. Med., 183, 2379, 10.1084/jem.183.5.2379 Bazan, 1997, A new class of membrane-bound chemokine with a CX3C motif, Nature, 385, 640, 10.1038/385640a0 Chiang, 2015, Identification of resolvin D2 receptor mediating resolution of infections and organ protection, J. Exp. Med., 212, 1203, 10.1084/jem.20150225 Serhan, 2009, Maresins: novel macrophage mediators with potent antiinflammatory and proresolving actions, J. Exp. Med., 206, 15, 10.1084/jem.20081880 Gilroy, 1999, Inducible cyclooxygenase may have anti-inflammatory properties, Nat. Med., 5, 698, 10.1038/9550 Rajakariar, 2007, Hematopoietic prostaglandin D2 synthase controls the onset and resolution of acute inflammation through PGD2 and 15-deoxyΔ12–14 PGJ2, Proc. Natl. Acad. Sci. U. S. A., 104, 20979, 10.1073/pnas.0707394104 Pettipher, 2008, Antagonists of the prostaglandin D2 receptor CRTH2, Drug News Perspect, 21, 317, 10.1358/dnp.2008.21.6.1246831