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Mini-Reviews in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1389-5575
ISSN (Online): 1875-5607

Review Article

G-Protein Coupled Receptors Involved in the Resolution of Inflammation: Ligands and Therapeutic Perspectives

Author(s): Margherita Mastromarino, Enza Lacivita*, Nicola A. Colabufo and Marcello Leopoldo

Volume 20, Issue 20, 2020

Page: [2090 - 2103] Pages: 14

DOI: 10.2174/1389557520666200719014433

Price: $65

Abstract

Dysregulated inflammation is a central pathological process in diverse disease states, including neurodegenerative disorders. The recent concept of “resolution of inflammation” is offering a conceptual change for the diagnosis and the development of new therapeutic approaches for chronic inflammatory diseases. Resolution of inflammation terminates the inflammatory response promoting the return to tissue homeostasis through the action of several classes of mediators, termed specialized pro-resolving lipid mediators (SPMs), that include lipoxins, resolvins, protectins, and maresins. SPMs provide “stop signals” that reduce the number of immune cells at the site of insult and increase the clearance of apoptotic cells through phagocytosis. SPMs elicit their effects through the interaction with specific G-protein coupled receptors (GPCRs). The elucidation of the pathways downstream of the GPCRs involved in the resolution of chronic inflammation is opening novel opportunities to generate novel anti-inflammatory agents. This review focuses on the SPMs and the receptors through which their effects are mediated. The medicinal chemistry of the modulators of the GPCRs involved in the resolution of inflammation will be illustrated, by highlighting the potential for developing new antiinflammatory drugs.

Keywords: Resolution of inflammation, pro-resolving specialized mediators, GPCRs, FPR2, GPR32, ChemR23, GPR18.

Graphical Abstract

[1]
Cotran, R.S.; Kumar, V.; Collins, T. Robbins Pathologic Basis of Disease, 6th ed; W. B. Saunders: Philadelphia, 1999.
[2]
Medzhitov, R. Inflammation 2010: New adventures of an old flame. Cell, 2010, 140(6), 771-776.
[http://dx.doi.org/10.1016/j.cell.2010.03.006] [PMID: 20303867]
[3]
Serhan, C.N.; Brain, S.D.; Buckley, C.D.; Gilroy, D.W.; Haslett, C.; O’Neill, L.A.J.; Perretti, M.; Rossi, A.G.; Wallace, J.L. Resolution of inflammation: State of the art, definitions and terms. FASEB J., 2007, 21(2), 325-332.
[http://dx.doi.org/10.1096/fj.06-7227rev] [PMID: 17267386]
[4]
Fullerton, J.N.; Gilroy, D.W. Resolution of inflammation: A new therapeutic frontier. Nat. Rev. Drug Discov., 2016, 15(8), 551-567.
[http://dx.doi.org/10.1038/nrd.2016.39] [PMID: 27020098]
[5]
Serhan, C.N. Novel pro-resolving lipid mediators in inflammation are leads for resolution physiology. Nature, 2014, 510(7503), 92-101.
[http://dx.doi.org/10.1038/nature13479] [PMID: 24899309]
[6]
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., 2001, 2(7), 612-619.
[http://dx.doi.org/10.1038/89759] [PMID: 11429545]
[7]
Serhan, C.N.; Chiang, N.; Van Dyke, T.E. Resolving inflammation: Dual anti-inflammatory and pro-resolution lipid mediators. Nat. Rev. Immunol., 2008, 8(5), 349-361.
[http://dx.doi.org/10.1038/nri2294] [PMID: 18437155]
[8]
Chiurchiù, V.; Leuti, A.; Maccarrone, M. Bioactive lipidis and chronic inflammation: Managing the fire. Front. Immunol., 2018, 9, 38.
[http://dx.doi.org/10.3389/fimmu.2018.00038] [PMID: 29434586]
[9]
Dalli, J.; Serhan, C.N. Identification and structure elucidation of the pro-resolving mediators provides novel leads for resolution pharmacology. Br. J. Pharmacol., 2019, 176(8), 1024-1037.
[http://dx.doi.org/10.1111/bph.14336] [PMID: 29679485]
[10]
Alessandri, A.L.; Sousa, L.P.; Lucas, C.D.; Rossi, A.G.; Pinho, V.; Teixeira, M.M. Resolution of inflammation: Mechanisms and opportunity for drug development. Pharmacol. Ther., 2013, 139(2), 189-212.
[http://dx.doi.org/10.1016/j.pharmthera.2013.04.006 ] [PMID: 23583354]
[11]
Buckley, C.D.; Gilroy, D.W.; Serhan, C.N. Proresolving lipid mediators and mechanisms in the resolution of acute inflammation. Immunity, 2014, 40(3), 315-327.
[http://dx.doi.org/10.1016/j.immuni.2014.02.009] [PMID: 24656045]
[12]
Leuti, A.; Maccarrone, M.; Chiurchiù, V. Preresolving lipid mediators: Endogenous modulators of oxidative stress. Oxid. Med. Cell. Longev., 2019.20198107265
[PMID: 31316721]
[13]
Serhan, C.N.; Krishnamoorthy, S.; Recchiuti, A.; Chiang, N. Novel anti-inflammatory--pro-resolving mediators and their receptors. Curr. Top. Med. Chem., 2011, 11(6), 629-647.
[http://dx.doi.org/10.2174/1568026611109060629] [PMID: 21261595]
[14]
Chiang, N.; Serhan, C.N. Structural elucidation and physiologic functions of specialized pro-resolving mediators and their receptors. Mol. Aspects Med., 2017, 58, 114-129.
[http://dx.doi.org/10.1016/j.mam.2017.03.005] [PMID: 28336292]
[15]
Gilroy, D.W.; Lawrence, T.; Perretti, M.; Rossi, A.G. Inflammatory resolution: New opportunities for drug discovery. Nat. Rev. Drug Discov., 2004, 3(5), 401-416.
[http://dx.doi.org/10.1038/nrd1383] [PMID: 15136788]
[16]
Serhan, C.N.; Chiang, N. Endogenous pro-resolving and anti-inflammatory lipid mediators: A new pharmacologic genus. Br. J. Pharmacol., 2008, 153(Suppl. 1), S200-S215.
[http://dx.doi.org/10.1038/sj.bjp.0707489] [PMID: 17965751]
[17]
Sansbury, B.E.; Spite, M. Resolution of acute inflammation and the role of resolvins in immunity, thrombosis, and vascular biology. Circ. Res., 2016, 119(1), 113-130.
[http://dx.doi.org/10.1161/CIRCRESAHA.116.307308 ] [PMID: 27340271]
[18]
Lee, C.H. Epithelial-mesenchymal transition: Initiation by cues from chronic inflammatory tumor microenvironment and termination by anti-inflammatory compounds and specialized pro-resolving lipids. Biochem. Pharmacol., 2018, 158, 261-273.
[http://dx.doi.org/10.1016/j.bcp.2018.10.031] [PMID: 30389404]
[19]
Fu, H.; Karlsson, J.; Bylund, J.; Movitz, C.; Karlsson, A.; Dahlgren, C. Ligand recognition and activation of formyl peptide receptors in neutrophils. J. Leukoc. Biol., 2006, 79(2), 247-256.
[http://dx.doi.org/10.1189/jlb.0905498] [PMID: 16365159]
[20]
Becker, E.L.; Forouhar, F.A.; Grunnet, M.L.; Boulay, F.; Tardif, M.; Bormann, B.J.; Sodja, D.; Ye, R.D.; Woska, J.R., Jr; Murphy, P.M. Broad immunocytochemical localization of the formylpeptide receptor in human organs, tissues, and cells. Cell Tissue Res., 1998, 292(1), 129-135.
[http://dx.doi.org/10.1007/s004410051042] [PMID: 9506920]
[21]
Ye, R.D.; Boulay, F.; Wang, J.M.; Dahlgren, C.; Gerard, C.; Parmentier, M.; Serhan, C.N.; Murphy, P.M. International union of basic and clinical pharmacology. LXXIII. Nomenclature for the Formyl Peptide Receptor (FPR) family. Pharmacol. Rev., 2009, 61(2), 119-161.
[http://dx.doi.org/10.1124/pr.109.001578] [PMID: 19498085]
[22]
Selvatici, R.; Falzarano, S.; Mollica, A.; Spisani, S. Signal transduction pathways triggered by selective formylpeptide analogues in human neutrophils. Eur. J. Pharmacol., 2006, 534(1-3), 1-11.
[http://dx.doi.org/10.1016/j.ejphar.2006.01.034] [PMID: 16516193]
[23]
Fiore, S.; Maddox, J.F.; Perez, H.D.; Serhan, C.N. Identification of a human cDNA encoding a functional high affinity lipoxin A4 receptor. J. Exp. Med., 1994, 180(1), 253-260.
[http://dx.doi.org/10.1084/jem.180.1.253] [PMID: 8006586]
[24]
Krishnamoorthy, S.; Recchiuti, A.; Chiang, N.; Fredman, G.; Serhan, C.N. Resolvin D1 receptor stereoselectivity and regulation of inflammation and proresolving microRNAs. Am. J. Pathol., 2012, 180(5), 2018-2027.
[http://dx.doi.org/10.1016/j.ajpath.2012.01.028] [PMID: 22449948]
[25]
Arnardottir, H.H.; Dalli, J.; Norling, L.V.; Colas, R.A.; Perretti, M.; Serhan, C.N. Resolvin D3 is dysregulated in arthritis and reduces arthritic inflammation. J. Immunol., 2016, 197(6), 2362-2368.
[http://dx.doi.org/10.4049/jimmunol.1502268] [PMID: 27534559]
[26]
Bena, S.; Brancaleone, V.; Wang, J.M.; Perretti, M.; Flower, R.J. Annexin A1 interaction with the FPR2/ALX receptor: Identification of distinct domains and downstream associated signaling. J. Biol. Chem., 2012, 287(29), 24690-24697.
[http://dx.doi.org/10.1074/jbc.M112.377101] [PMID: 22610094]
[27]
Cooray, S.N.; Gobbetti, T.; Montero-Melendez, T.; McArthur, S.; Thompson, D.; Clark, A.J.; Flower, R.J.; Perretti, M. Ligand-specific conformational change of the G-protein-coupled receptor ALX/FPR2 determines proresolving functional responses. Proc. Natl. Acad. Sci. USA, 2013, 110(45), 18232-18237.
[http://dx.doi.org/10.1073/pnas.1308253110] [PMID: 24108355]
[28]
Fredman, G.; Ozcan, L.; Spolitu, S.; Hellmann, J.; Spite, M.; Backs, J.; Tabas, I. Resolvin D1 limits 5-lipoxygenase nuclear localization and leukotriene B4 synthesis by inhibiting a calcium-activated kinase pathway. Proc. Natl. Acad. Sci. USA, 2014, 111(40), 14530-14535.
[http://dx.doi.org/10.1073/pnas.1410851111] [PMID: 25246560]
[29]
Petri, M.H.; Silke, T.; Andonova, T.; Lindquist-Liljeqvist, M.; Jin, H. Skenteris, M-Arnardottir, H.; Maegdefessel, L.;Caidahl, K.; Perretti, M.; Roy, J.; Back, M. Lipoxin and ALX/FPR2 receptor pathway protects against abdominal aortic aneurysms. JACC Basic Transl. Sci., 2018, 3(6), 719-727.
[http://dx.doi.org/10.1016/j.jacbts.2018.08.005] [PMID: 30623131]
[30]
Devchand, P.R.; Arita, M.; Hong, S.; Bannenberg, G.; Moussignac, R.L.; Gronert, K.; Serhan, C.N. Human ALX receptor regulates neutrophil recruitment in transgenic mice: Roles in inflammation and host defense. FASEB J., 2003, 17(6), 652-659.
[http://dx.doi.org/10.1096/fj.02-0770com] [PMID: 12665478]
[31]
Dufton, N.; Hannon, R.; Brancaleone, V.; Dalli, J.; Patel, H.B.; Gray, M.; D’Acquisto, F.; Buckingham, J.C.; Perretti, M.; Flower, R.J. Anti-inflammatory role of the murine formyl-peptide receptor 2: ligand-specific effects on leukocyte responses and experimental inflammation. J. Immunol., 2010, 184(5), 2611-2619.
[http://dx.doi.org/10.4049/jimmunol.0903526] [PMID: 20107188]
[32]
Serhan, C.N.; Maddox, J.F.; Petasis, N.A.; Akritopoulou-Zanze, I.; Papayianni, A.; Brady, H.R.; Colgan, S.P.; Madara, J.L. Design of lipoxin A4 stable analogs that block transmigration and adhesion of human neutrophils. Biochemistry, 1995, 34(44), 14609-14615.
[http://dx.doi.org/10.1021/bi00044a041] [PMID: 7578068]
[33]
Serhan, C.N.; Fiore, S.; Brezinski, D.A.; Lynch, S. Lipoxin A4 metabolism by differentiated HL-60 cells and human monocytes: Conversion to novel 15-oxo and dihydro products. Biochemistry, 1993, 32(25), 6313-6319.
[http://dx.doi.org/10.1021/bi00076a002] [PMID: 8518275]
[34]
Bozinovski, S.; Anthony, D.; Anderson, G.P.; Irving, L.B.; Levy, B.D.; Vlahos, R. Treating neutrophilic inflammation in COPD by targeting ALX/FPR2 resolution pathways. Pharmacol. Ther., 2013, 140(3), 280-289.
[http://dx.doi.org/10.1016/j.pharmthera.2013.07.007 ] [PMID: 23880288]
[35]
Philippe, R.; Urbach, V. Specialized pro-resolving lipid mediators in cystic fibrosis. Int. J. Mol. Sci., 2018, 19(10), 2865.
[http://dx.doi.org/10.3390/ijms19102865] [PMID: 30241412]
[36]
Pirault, J.; Bäck, M. Lipoxin and resolvin receptors transducing the resolution of inflammation in cardiovascular disease. Front. Pharmacol., 2018, 9, 1273.
[http://dx.doi.org/10.3389/fphar.2018.01273] [PMID: 30487747]
[37]
Svensson, C.I.; Zattoni, M.; Serhan, C.N. Lipoxins and aspirin-triggered lipoxin inhibit inflammatory pain processing. J. Exp. Med., 2007, 204(2), 245-252.
[http://dx.doi.org/10.1084/jem.20061826] [PMID: 17242163]
[38]
Medeiros, R.; Kitazawa, M.; Passos, G.F.; Baglietto-Vargas, D.; Cheng, D.; Cribbs, D.H.; LaFerla, F.M. Aspirin-triggered lipoxin A4 stimulates alternative activation of microglia and reduces Alzheimer disease-like pathology in mice. Am. J. Pathol., 2013, 182(5), 1780-1789.
[http://dx.doi.org/10.1016/j.ajpath.2013.01.051] [PMID: 23506847]
[39]
Serhan, C.N.; Gotlinger, K.; Hong, S.; Arita, M. Resolvins, docosatrienes, and neuroprotectins, novel omega-3-derived mediators, and their aspirin-triggered endogenous epimers: An overview of their protective roles in catabasis. Prostaglandins Other Lipid Mediat., 2004, 73(3-4), 155-172.
[http://dx.doi.org/10.1016/j.prostaglandins.2004.03.005 ] [PMID: 15290791]
[40]
Prieto, P.; Rosales-Mendoza, C.E.; Terrón, V.; Toledano, V.; Cuadrado, A.; López-Collazo, E.; Bannenberg, G.; Martín-Sanz, P.; Fernández-Velasco, M.; Boscá, L. Activation of autophagy in macrophages by pro-resolving lipid mediators. Autophagy, 2015, 11(10), 1729-1744.
[http://dx.doi.org/10.1080/15548627.2015.1078958 ] [PMID: 26506892]
[41]
Eickmeier, O.; Seki, H.; Haworth, O.; Hilberath, J.N.; Gao, F.; Uddin, M.; Croze, R.H.; Carlo, T.; Pfeffer, M.A.; Levy, B.D. Aspirin-triggered resolvin D1 reduces mucosal inflammation and promotes resolution in a murine model of acute lung injury. Mucosal Immunol., 2013, 6(2), 256-266.
[http://dx.doi.org/10.1038/mi.2012.66] [PMID: 22785226]
[42]
Chiurchiù, V.; Leuti, A.; Dalli, J.; Jacobsson, A.; Battistini, L.; Maccarrone, M.; Serhan, C.N. Proresolving lipid mediators resolvin D1, Resolvin D2, and Maresin 1 are critical in modulating T cell responses. Sci. Transl. Med., 2016, 8(353), 353.
[43]
Bisicchia, E.; Sasso, V.; Catanzaro, G.; Leuti, A.; Besharat, Z.M.; Chiacchiarini, M.; Molinari, M.; Ferretti, E.; Viscomi, M.T.; Chiurchiù, V. Resolvin D1 halts remote neuroinflammation and improves functional recovery after focal brain damage via ALX/FPR2 receptor-regulated MicroRNAs. Mol. Neurobiol., 2018, 55(8), 6894-6905.
[http://dx.doi.org/10.1007/s12035-018-0889-z] [PMID: 29357041]
[44]
Krashia, P.; Cordella, A.; Nobili, A.; La Barbera, L.; Federici, M.; Leuti, A.; Campanelli, F.; Natale, G.; Marino, G.; Calabrese, V.; Vedele, F.; Ghiglieri, V.; Picconi, B.; Di Lazzaro, G.; Schirinzi, T.; Sancesario, G.; Casadei, N.; Riess, O.; Bernardini, S.; Pisani, A.; Calabresi, P.; Viscomi, M.T.; Serhan, C.N.; Chiurchiù, V.; D’Amelio, M.; Mercuri, N.B. Blunting neuroinflammation with resolvin D1 prevents early pathology in a rat model of Parkinson’s disease. Nat. Commun., 2019, 10(1), 3945.
[http://dx.doi.org/10.1038/s41467-019-11928-w] [PMID: 31477726]
[45]
Sun, Y.P.; Oh, S.F.; Uddin, J.; Yang, R.; Gotlinger, K.; Campbell, E.; Colgan, S.P.; Petasis, N.A.; Serhan, C.N. Resolvin D1 and its aspirin-triggered 17R epimer. Stereochemical assignments, anti-inflammatory properties, and enzymatic inactivation. J. Biol. Chem., 2007, 282(13), 9323-9334.
[http://dx.doi.org/10.1074/jbc.M609212200] [PMID: 17244615]
[46]
O’Sullivan, T.P.; Vallin, K.S.A.; Shah, S.T.; Fakhry, J.; Maderna, P.; Scannell, M.; Sampaio, A.L.F.; Perretti, M.; Godson, C.; Guiry, P.J. Aromatic lipoxin A4 and lipoxin B4 analogues display potent biological activities. J. Med. Chem., 2007, 50(24), 5894-5902.
[http://dx.doi.org/10.1021/jm060270d] [PMID: 17960922]
[47]
Börgeson, E.; Docherty, N.G.; Murphy, M.; Rodgers, K.; Ryan, A.; O’Sullivan, T.P.; Guiry, P.J.; Goldschmeding, R.; Higgins, D.F.; Godson, C. Lipoxin A4 and benzo-lipoxin A4 attenuate experimental renal fibrosis. FASEB J., 2011, 25(9), 2967-2979.
[http://dx.doi.org/10.1096/fj.11-185017] [PMID: 21628447]
[48]
Duffy, C.D.; Maderna, P.; McCarthy, C.; Loscher, C.E.; Godson, C.; Guiry, P.J. Synthesis and biological evaluation of pyridine-containing lipoxin A4 analogues. ChemMedChem, 2010, 5(4), 517-522.
[http://dx.doi.org/10.1002/cmdc.200900533] [PMID: 20127785]
[49]
de Gaetano, M.; Butler, E.; Gahan, K.; Zanetti, A.; Marai, M.; Chen, J.; Cacace, A.; Hams, E.; Maingot, C.; McLoughlin, A.; Brennan, E.; Leroy, X.; Loscher, C.E.; Fallon, P.; Perretti, M.; Godson, C.; Guiry, P.J. Asymmetric synthesis and biological evaluation of imidazole- and oxazole-containing synthetic lipoxin A4 mimetics (sLXms). Eur. J. Med. Chem., 2019, 162, 80-108.
[http://dx.doi.org/10.1016/j.ejmech.2018.10.049] [PMID: 30419493]
[50]
He, M.; Cheng, N.; Gao, W.W.; Zhang, M.; Zhang, Y.Y.; Ye, R.D.; Wang, M.W. Characterization of Quin-C1 for its anti-inflammatory property in a mouse model of bleomycin-induced lung injury. Acta Pharmacol. Sin., 2011, 32(5), 601-610.
[http://dx.doi.org/10.1038/aps.2011.4] [PMID: 21499285]
[51]
Bürli, R.W.; Xu, H.; Zou, X.; Muller, K.; Golden, J.; Frohn, M.; Adlam, M.; Plant, M.H.; Wong, M.; McElvain, M.; Regal, K.; Viswanadhan, V.N.; Tagari, P.; Hungate, R. Potent hFPRL1 (ALXR) agonists as potential anti-inflammatory agents. Bioorg. Med. Chem. Lett., 2006, 16(14), 3713-3718.
[http://dx.doi.org/10.1016/j.bmcl.2006.04.068] [PMID: 16697190]
[52]
Beard, R. L.; Duong, T. T.; Donello, J. E.; Viswanath, V.; Garst, M. E. Preparation of amide derivatives of N-urea substituted amino acids and dipeptides as N-formyl peptide receptor like-1 (FPRL-1) modulators. WO2013062947A1, 2013.
[53]
Abdel-Magid, A.F. FPRL-1 receptor modulators may provide treatment for inflammation. ACS Med. Chem. Lett., 2013, 4(7), 574-575.
[http://dx.doi.org/10.1021/ml400179m] [PMID: 24900712]
[54]
Bur, D.; Corminboeuf, O.; Cren, S.; Fretz, H.; Grisostomi, C.; Leroy, X.; Pothier, J.; Richard-Bildstein, S. Preparation of aminopyrazole derivatives as ALXR receptor agonists. WO2009077954A1, 2009.
[55]
Bur, D.; Corminboeuf, O.; Cren, S.; Grisostomi, C.; Leroy, X.; Richard-Bildstein, S. Fluorinated aminotriazole derivatives as ALX receptor agonists and their preparation, pharmaceutical compositions and use in the treatment of diseases. WO2010143116A1, 2010.
[56]
Stalder, A.K.; Lott, D.; Strasser, D.S.; Cruz, H.G.; Krause, A.; Groenen, P.M.A.; Dingemanse, J. Biomarker-guided clinical development of the first-in-class anti-inflammatory FPR2/ALX agonist ACT-389949. Br. J. Clin. Pharmacol., 2017, 83(3), 476-486.
[http://dx.doi.org/10.1111/bcp.13149] [PMID: 27730665]
[57]
Qin, C.X.; May, L.T.; Li, R.; Cao, N.; Rosli, S.; Deo, M.; Alexander, A.E.; Horlock, D.; Bourke, J.E.; Yang, Y.H.; Stewart, A.G.; Kaye, D.M.; Du, X-J.; Sexton, P.M.; Christopoulos, A.; Gao, X-M.; Ritchie, R.H. Small-molecule-biased formyl peptide receptor agonist compound 17b protects against myocardial ischaemia-reperfusion injury in mice. Nat. Commun., 2017, 8, 14232.
[http://dx.doi.org/10.1038/ncomms14232] [PMID: 28169296]
[58]
Deora, G.S.; Qin, C.X.; Vecchio, E.A.; Debono, A.J.; Priebbenow, D.L.; Brady, R.M.; Beveridge, J.; Teguh, S.C.; Deo, M.; May, L.T.; Krippner, G.; Ritchie, R.H.; Baell, J.B. Substituted pyridazin-3(2H)-ones as highly potent and biased formyl peptide receptor agonists. J. Med. Chem., 2019, 62(10), 5242-5248.
[http://dx.doi.org/10.1021/acs.jmedchem.8b01912] [PMID: 31038950]
[59]
Schepetkin, I.A.; Kirpotina, L.N.; Khlebnikov, A.I.; Jutila, M.A.; Quinn, M.T. Gastrin-releasing peptide/neuromedin B receptor antagonists PD176252, PD168368, and related analogs are potent agonists of human formyl-peptide receptors. Mol. Pharmacol., 2011, 79(1), 77-90.
[http://dx.doi.org/10.1124/mol.110.068288] [PMID: 20943772]
[60]
Schepetkin, I.A.; Kirpotina, L.N.; Khlebnikov, A.I.; Leopoldo, M.; Lucente, E.; Lacivita, E.; De Giorgio, P.; Quinn, M.T. 3-(1H-indol-3-yl)-2-[3-(4-nitrophenyl)ureido]propanamide enantiomers with human formyl-peptide receptor agonist activity: Molecular modeling of chiral recognition by FPR2. Biochem. Pharmacol., 2013, 85(3), 404-416.
[http://dx.doi.org/10.1016/j.bcp.2012.11.015] [PMID: 23219934]
[61]
Lacivita, E.; Schepetkin, I.A.; Stama, M.L.; Kirpotina, L.N.; Colabufo, N.A.; Perrone, R.; Khlebnikov, A.I.; Quinn, M.T.; Leopoldo, M. Novel 3-(1H-indol-3-yl)-2-[3-(4-methoxyphenyl)ureido]propana-mides as selective agonists of human formyl-peptide receptor 2. Bioorg. Med. Chem., 2015, 23(14), 3913-3924.
[http://dx.doi.org/10.1016/j.bmc.2014.12.007] [PMID: 25549897]
[62]
Lacivita, E.; Stama, M.L.; Maeda, J.; Fujinaga, M.; Hatori, A.; Zhang, M.R.; Colabufo, N.A.; Perrone, R.; Higuchi, M.; Suhara, T.; Leopoldo, M. Radiosynthesis and in vivo Evaluation of Carbon-11 (2S)-3-(1H-Indol-3-yl)-2-[(4-methoxyphenyl)carbamoyl]amino-N-[1-(5-methoxypyridin-2-yl)cyclohexyl]methylpropanamide: An attempt to visualize brain formyl peptide receptors in mouse Models of neuroinflammation. Chem. Biodivers., 2016, 13(7), 875-883.
[http://dx.doi.org/10.1002/cbdv.201500281] [PMID: 27251949]
[63]
Stama, M.L.; Ślusarczyk, J.; Lacivita, E.; Kirpotina, L.N.; Schepetkin, I.A.; Chamera, K.; Riganti, C.; Perrone, R.; Quinn, M.T.; Basta-Kaim, A.; Leopoldo, M. Novel ureidopropanamide based N-formyl peptide receptor 2 (FPR2) agonists with potential application for central nervous system disorders characterized by neuroinflammation. Eur. J. Med. Chem., 2017, 141, 703-720.
[http://dx.doi.org/10.1016/j.ejmech.2017.09.023] [PMID: 29102463]
[64]
Krishnamoorthy, S.; Recchiuti, A.; Chiang, N.; Yacoubian, S.; Lee, C.H.; Yang, R.; Petasis, N.A.; Serhan, C.N. Resolvin D1 binds human phagocytes with evidence for proresolving receptors. Proc. Natl. Acad. Sci. USA, 2010, 107(4), 1660-1665.
[http://dx.doi.org/10.1073/pnas.0907342107] [PMID: 20080636]
[65]
Serhan, C.N.; Chiang, N.; Dalli, J. New pro-resolving n-3 mediators bridge resolution of infectious inflammation to tissue regeneration. Mol. Aspects Med., 2018, 64, 1-17.
[http://dx.doi.org/10.1016/j.mam.2017.08.002] [PMID: 28802833]
[66]
Chiang, N.; Fredman, G.; Bäckhed, F.; Oh, S.F.; Vickery, T.; Schmidt, B.A.; Serhan, C.N. Infection regulates pro-resolving mediators that lower antibiotic requirements. Nature, 2012, 484(7395), 524-528.
[http://dx.doi.org/10.1038/nature11042] [PMID: 22538616]
[67]
Schmid, M.; Gemperle, C.; Rimann, N.; Hersberger, M. Resolvin D1 Polarizes Primary Human Macrophages toward a proresolution phenotype through GPR32. J. Immunol., 2016, 196(8), 3429-3437.
[http://dx.doi.org/10.4049/jimmunol.1501701] [PMID: 26969756]
[68]
Mizwicki, M.T.; Liu, G.; Fiala, M.; Magpantay, L.; Sayre, J.; Siani, A.; Mahanian, M.; Weitzman, R.; Hayden, E.Y.; Rosenthal, M.J.; Nemere, I.; Ringman, J.; Teplow, D.B. 1α,25-dihydroxyvitamin D3 and resolvin D1 retune the balance between amyloid-β phagocytosis and inflammation in Alzheimer’s disease patients. J. Alzheimers Dis., 2013, 34(1), 155-170.
[http://dx.doi.org/10.3233/JAD-121735] [PMID: 23186989]
[69]
Norling, L.V.; Dalli, J.; Flower, R.J.; Serhan, C.N.; Perretti, M. Resolvin D1 limits polymorphonuclear leukocyte recruitment to inflammatory loci: Receptor-dependent actions. Arterioscler. Thromb. Vasc. Biol., 2012, 32(8), 1970-1978.
[http://dx.doi.org/10.1161/ATVBAHA.112.249508 ] [PMID: 22499990]
[70]
Orr, S.K.; Colas, R.A.; Dalli, J.; Chiang, N.; Serhan, C.N. Proresolving actions of a new resolvin D1 analog mimetic qualifies as an immunoresolvent. Am. J. Physiol. Lung Cell. Mol. Physiol., 2015, 308(9), L904-L911.
[http://dx.doi.org/10.1152/ajplung.00370.2014] [PMID: 25770181]
[71]
Chiang, N.; Barnaeva, E.; Hu, X.; Marugan, J.; Southall, N.; Ferrer, M.; Serhan, C. Identification of chemotype agonists for human Resolvin D1 receptor DRV1 with pro-resolving functions. Cell Chem. Biol., 2019, 2126(2), 244-254.
[http://dx.doi.org/10.1016/j.chembiol.2018.10.023]
[72]
Arita, M.; Bianchini, F.; Aliberti, J.; Sher, A.; Chiang, N.; Hong, S.; Yang, R.; Petasis, N.A.; Serhan, C.N. Stereochemical assignment, antiinflammatory properties, and receptor for the omega-3 lipid mediator resolvin E1. J. Exp. Med., 2005, 201(5), 713-722.
[http://dx.doi.org/10.1084/jem.20042031] [PMID: 15753205]
[73]
Methner, A.; Hermey, G.; Schinke, B.; Hermans-Borgmeyer, I. A novel G protein-coupled receptor with homology to neuropeptide and chemoattractant receptors expressed during bone development. Biochem. Biophys. Res. Commun., 1997, 233(2), 336-342.
[http://dx.doi.org/10.1006/bbrc.1997.6455] [PMID: 9144535]
[74]
Herová, M.; Schmid, M.; Gemperle, C.; Hersberger, M. ChemR23, the receptor for chemerin and resolvin E1, is expressed and functional on M1 but not on M2 macrophages. J. Immunol., 2015, 194(5), 2330-2337.
[http://dx.doi.org/10.4049/jimmunol.1402166] [PMID: 25637017]
[75]
Ohira, T.; Arita, M.; Omori, K.; Recchiuti, A.; Van Dyke, T.E.; Serhan, C.N. Resolvin E1 receptor activation signals phosphorylation and phagocytosis. J. Biol. Chem., 2010, 285(5), 3451-3461.
[http://dx.doi.org/10.1074/jbc.M109.044131] [PMID: 19906641]
[76]
Vermi, W.; Riboldi, E.; Wittamer, V.; Gentili, F.; Luini, W.; Marrelli, S.; Vecchi, A.; Franssen, J.D.; Communi, D.; Massardi, L.; Sironi, M.; Mantovani, A.; Parmentier, M.; Facchetti, F.; Sozzani, S. Role of ChemR23 in directing the migration of myeloid and plasmacytoid dendritic cells to lymphoid organs and inflamed skin. J. Exp. Med., 2005, 201(4), 509-515.
[http://dx.doi.org/10.1084/jem.20041310] [PMID: 15728234]
[77]
Gisondi, P.; Lora, V.; Bonauguri, C.; Russo, A.; Lippi, G.; Girolomoni, G. Serum chemerin is increased in patients with chronic plaque psoriasis and normalizes following treatment with infliximab. Br. J. Dermatol., 2013, 168(4), 749-755.
[http://dx.doi.org/10.1111/bjd.12118] [PMID: 23110708]
[78]
Haworth, O.; Cernadas, M.; Levy, B.D. NK cells are effectors for resolvin E1 in the timely resolution of allergic airway inflammation. J. Immunol., 2011, 186(11), 6129-6135.
[http://dx.doi.org/10.4049/jimmunol.1004007] [PMID: 21515793]
[79]
Freire, M.O.; Dalli, J.; Serhan, C.N.; Van Dyke, T.E. Neutrophil resolvin E1 receptor expression and function in type 2 diabetes. J. Immunol., 2017, 198(2), 718-728.
[http://dx.doi.org/10.4049/jimmunol.1601543] [PMID: 27994073]
[80]
Deyama, S.; Shimoda, K.; Suzuki, H.; Ishikawa, Y.; Ishimura, K.; Fukuda, H.; Hitora-Imamura, N.; Ide, S.; Satoh, M.; Kaneda, K.; Shuto, S.; Minami, M. Resolvin E1/E2 ameliorate lipopolysaccharide-induced depression-like behaviors via ChemR23. Psychopharmacology (Berl.), 2018, 235(1), 329-336.
[http://dx.doi.org/10.1007/s00213-017-4774-7] [PMID: 29090333]
[81]
Cholkar, K.; Gilger, B.C.; Mitra, A.K. Topical delivery of aqueous micellar resolvin E1 analog (RX-10045). Int. J. Pharm., 2016, 498(1-2), 326-334.
[http://dx.doi.org/10.1016/j.ijpharm.2015.12.037] [PMID: 26706439]
[82]
Imaizumi, T.; Kobayashi, A.; Otsubo, S.; Komai, M.; Magara, M.; Otsubo, N. The discovery and optimization of a series of 2-aminobenzoxazole derivatives as ChemR23 inhibitors. Bioorg. Med. Chem., 2019, 27(21)115091
[http://dx.doi.org/10.1016/j.bmc.2019.115091] [PMID: 31521459]
[83]
McHugh, D. GPR18 in microglia: Implications for the CNS and endocannabinoid system signalling. Br. J. Pharmacol., 2012, 167(8), 1575-1582.
[http://dx.doi.org/10.1111/j.1476-5381.2012.02019.x ] [PMID: 22563843]
[84]
Kohno, M.; Hasegawa, H.; Inoue, A.; Muraoka, M.; Miyazaki, T.; Oka, K.; Yasukawa, M. Identification of N-arachidonylglycine as the endogenous ligand for orphan G-protein-coupled receptor GPR18. Biochem. Biophys. Res. Commun., 2006, 347(3), 827-832.
[http://dx.doi.org/10.1016/j.bbrc.2006.06.175] [PMID: 16844083]
[85]
Qin, Y.; Verdegaal, E.M.E.; Siderius, M.; Bebelman, J.P.; Smit, M.J.; Leurs, R.; Willemze, R.; Tensen, C.P.; Osanto, S. Quantitative expression profiling of G-Protein-Coupled Receptors (GPCRs) in metastatic melanoma: The constitutively active orphan GPCR GPR18 as novel drug target. Pigment Cell Melanoma Res., 2011, 24(1), 207-218.
[http://dx.doi.org/10.1111/j.1755-148X.2010.00781.x ] [PMID: 20880198]
[86]
Finlay, D.B.; Joseph, W.R.; Grimsey, N.L.; Glass, M. GPR18 undergoes a high degree of constitutive trafficking but is unresponsive to N-Arachidonoyl Glycine. PeerJ, 2016, 4e1835
[http://dx.doi.org/10.7717/peerj.1835] [PMID: 27018161]
[87]
Chiang, N.; Dalli, J.; Colas, R.A.; Serhan, C.N. Identification of resolvin D2 receptor mediating resolution of infections and organ protection. J. Exp. Med., 2015, 212(8), 1203-1217.
[http://dx.doi.org/10.1084/jem.20150225] [PMID: 26195725]
[88]
Wang, X.; Zhu, M.; Hjorth, E.; Cortés-Toro, V.; Eyjolfsdottir, H.; Graff, C.; Nennesmo, I.; Palmblad, J.; Eriksdotter, M.; Sambamurti, K.; Fitzgerald, J.M.; Serhan, C.N.; Granholm, A.C.; Schultzberg, M. Resolution of inflammation is altered in Alzheimer’s disease. Alzheimers Dement., 2015, 11(1), 40-50.
[http://dx.doi.org/10.1016/j.jalz.2013.12.024] [PMID: 24530025]
[89]
Hashimoto, M.; Katakura, M.; Tanabe, Y.; Al Mamun, A.; Inoue, T.; Hossain, S.; Arita, M.; Shido, O. n-3 fatty acids effectively improve the reference memory-related learning ability associated with increased brain docosahexaenoic acid-derived docosanoids in aged rats. Biochim. Biophys. Acta, 2015, 1851(2), 203-209.
[http://dx.doi.org/10.1016/j.bbalip.2014.10.009] [PMID: 25450447]
[90]
Homann, J.; Suo, J.; Schmidt, M.; de Bruin, N.; Scholich, K.; Geisslinger, G.; Ferreirós, N. In Vivo availability of pro-resolving lipid mediators in oxazolone induced dermal inflammation in the mouse. PLoS One, 2015, 10(11)e0143141
[http://dx.doi.org/10.1371/journal.pone.0143141 ] [PMID: 26599340]
[91]
McHugh, D.; Hu, S.S.; Rimmerman, N.; Juknat, A.; Vogel, Z.; Walker, J.M.; Bradshaw, H.B. N-arachidonoyl glycine, an abundant endogenous lipid, potently drives directed cellular migration through GPR18, the putative abnormal cannabidiol receptor. BMC Neurosci., 2010, 11, 44.
[http://dx.doi.org/10.1186/1471-2202-11-44] [PMID: 20346144]
[92]
Schmuhl, E.; Ramer, R.; Salamon, A.; Peters, K.; Hinz, B. Increase of mesenchymal stem cell migration by cannabidiol via activation of p42/44 MAPK. Biochem. Pharmacol., 2014, 87(3), 489-501.
[http://dx.doi.org/10.1016/j.bcp.2013.11.016] [PMID: 24304686]
[93]
Nazir, M.; Harms, H.; Loef, I.; Kehraus, S.; El Maddah, F.; Arslan, I.; Rempel, V.; Müller, C.E.; König, G.M. GPR18 Inhibiting amauromine and the novel triterpene glycoside auxarthonoside from the sponge-derived fungus auxarthron reticulatum. Planta Med., 2015, 81(12-13), 1141-1145.
[http://dx.doi.org/10.1055/s-0035-1545979] [PMID: 26287693]
[94]
Rempel, V.; Atzler, K.; Behrenswerth, A.; Karcz, T.; Schoeder, C.; Hinz, S.; Kaleta, M.; Thimm, D.; Kiec-Kononowicz, K.; Müller, C.E. Bicyclic imidazole-4-one de- rivatives: A new class of antagonists for the orphan G protein-coupled receptors GPR18 and GPR55. MedChemComm, 2014, 5, 632-649.
[http://dx.doi.org/10.1039/C3MD00394A]
[95]
Schoeder, C.T.; Kaleta, M.; Mahardhika, A.B.; Olejarz-Maciej, A.; Łażewska, D.; Kieć-Kononowicz, K.; Müller, C.E. Structure-activity relationships of imidazothiazinones and analogs as antagonists of the cannabinoid-activated orphan G protein-coupled receptor GPR18. Eur. J. Med. Chem., 2018, 155, 381-397.
[http://dx.doi.org/10.1016/j.ejmech.2018.05.050 ] [PMID: 29902723]

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