The Contribution of Formyl Peptide Receptor Dysfunction to the Course of Neuroinflammation: A Potential Role in the Brain Pathology

Author(s): Ewa Trojan, Natalia Bryniarska, Monika Leśkiewicz, Magdalena Regulska, Katarzyna Chamera, Magdalena Szuster-Głuszczak, Marcello Leopoldo, Enza Lacivita, Agnieszka Basta-Kaim*

Journal Name: Current Neuropharmacology

Volume 18 , Issue 3 , 2020

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Chronic inflammatory processes within the central nervous system (CNS) are in part responsible for the development of neurodegenerative and psychiatric diseases. These processes are associated with, among other things, the increased and disturbed activation of microglia and the elevated production of proinflammatory factors. Recent studies indicated that the disruption of the process of resolution of inflammation (RoI) may be the cause of CNS disorders. It is shown that the RoI is regulated by endogenous molecules called specialized pro-resolving mediators (SPMs), which interact with specific membrane receptors. Some SPMs activate formyl peptide receptors (FPRs), which belong to the family of seven-transmembrane G protein-coupled receptors. These receptors take part not only in the proinflammatory response but also in the resolution of the inflammation process. Therefore, the activation of FPRs might have complex consequences.

This review discusses the potential role of FPRs, and in particular the role of FPR2 subtype, in the brain under physiological and pathological conditions and their involvement in processes underlying neurodegenerative and psychiatric disorders as well as ischemia, the pathogenesis of which involves the dysfunction of inflammatory processes.

Keywords: Neuroinflammation, glial cells, resolution of inflammation, formyl peptide receptors, new pro-resolving agonists, Alzheimer's disease, depression, ischemia.

[1]
Takeuchi, O.; Akira, S. Pattern recognition receptors and inflammation. Cell, 2010, 140(6), 805-820.
[http://dx.doi.org/10.1016/j.cell.2010.01.022] [PMID: 20303872]
[2]
Gallin, J.I.; Goldstein, I.M.; Snyderman, R., Eds.; Inflammation: Basic principles and clinical correlates; Raven Press: New York, 1992.
[3]
Ortega-Gómez, A.; Perretti, M.; Soehnlein, O. Resolution of inflammation: an integrated view. EMBO Mol. Med., 2013, 5(5), 661-674.
[http://dx.doi.org/10.1002/emmm.201202382] [PMID: 23592557]
[4]
Serhan, C.N. Discovery of specialized pro-resolving mediators marks the dawn of resolution physiology and pharmacology. Mol. Aspects Med., 2017, 58, 1-11.
[http://dx.doi.org/10.1016/j.mam.2017.03.001] [PMID: 28263773]
[5]
Nathan, C.; Ding, A. Nonresolving inflammation. Cell, 2010, 140(6), 871-882.
[http://dx.doi.org/10.1016/j.cell.2010.02.029] [PMID: 20303877]
[6]
Murakami, M.; Hirano, T. The molecular mechanisms of chronic inflammation development. Front. Immunol., 2012, 3, 323.
[http://dx.doi.org/10.3389/fimmu.2012.00323] [PMID: 23162547]
[7]
Jones, H.R.; Robb, C.T.; Perretti, M.; Rossi, A.G. The role of neutrophils in inflammation resolution. Semin. Immunol., 2016, 28(2), 137-145.
[http://dx.doi.org/10.1016/j.smim.2016.03.007] [PMID: 27021499]
[8]
Fox, S.; Leitch, A.E.; Duffin, R.; Haslett, C.; Rossi, A.G. Neutrophil apoptosis: relevance to the innate immune response and inflammatory disease. J. Innate Immun., 2010, 2(3), 216-227.
[http://dx.doi.org/10.1159/000284367] [PMID: 20375550]
[9]
Feghali, C.A.; Wright, T.M. Cytokines in acute and chronic inflammation. Front. Biosci., 1997, 2, d12-d26.
[http://dx.doi.org/10.2741/A171] [PMID: 9159205]
[10]
Lintermans, L.L.; Stegeman, C.A.; Heeringa, P.; Abdulahad, W.H. T cells in vascular inflammatory diseases. Front. Immunol., 2014, 5, 504.
[http://dx.doi.org/10.3389/fimmu.2014.00504] [PMID: 25352848]
[11]
Medzhitov, R. Origin and physiological roles of inflammation. Nature, 2008, 454(7203), 428-435.
[http://dx.doi.org/10.1038/nature07201] [PMID: 18650913]
[12]
Ashley, N.T.; Weil, Z.M.; Nelson, R. J. Inflammation: Mechanisms, Costs, and Natural Variation. Annu. Rev. Ecol. Evol. Syst., 2012, 43, 385-406.
[http://dx.doi.org/10.1146/annurev-ecolsys-040212-092530]
[13]
Schett, G.; Neurath, M.F. Resolution of chronic inflammatory disease: universal and tissue-specific concepts. Nat. Commun., 2018, 9(1), 3261.
[http://dx.doi.org/10.1038/s41467-018-05800-6] [PMID: 30111884]
[14]
Leszek, J.; Barreto, G.E.; Gąsiorowski, K.; Koutsouraki, E.; Ávila-Rodrigues, M.; Aliev, G. Inflammatory mechanisms and oxidative stress as key factors responsible for progression of neurodegeneration: Role of brain innate immune system. CNS Neurol. Disord. Drug Targets, 2016, 15(3), 329-336.
[http://dx.doi.org/10.2174/1871527315666160202125914] [PMID: 26831258]
[15]
Graeber, M.B. Neuroinflammation: no rose by any other name. Brain Pathol., 2014, 24(6), 620-622.
[http://dx.doi.org/10.1111/bpa.12192] [PMID: 25345892]
[16]
Abushouk, A.I.; Negida, A.; Ahmed, H.; Abdel-Daim, M.M. Neuroprotective mechanisms of plant extracts against MPTP induced neurotoxicity: Future applications in Parkinson’s disease. Biomed. Pharmacother., 2017, 85, 635-645.
[http://dx.doi.org/10.1016/j.biopha.2016.11.074] [PMID: 27890431]
[17]
Yang, Q.Q.; Zhou, J.W. Neuroinflammation in the central nervous system: Symphony of glial cells. Glia, 2019, 67(6), 1017-1035.
[http://dx.doi.org/10.1002/glia.23571] [PMID: 30548343]
[18]
Mariani, M.M.; Kielian, T. Microglia in infectious diseases of the central nervous system. J. Neuroimmune Pharmacol., 2009, 4(4), 448-461.
[http://dx.doi.org/10.1007/s11481-009-9170-6] [PMID: 19728102]
[19]
Michell-Robinson, M.A.; Touil, H.; Healy, L.M.; Owen, D.R.; Durafourt, B.A.; Bar-Or, A.; Antel, J.P.; Moore, C.S. Roles of microglia in brain development, tissue maintenance and repair. Brain, 2015, 138(Pt 5), 1138-1159.
[http://dx.doi.org/10.1093/brain/awv066] [PMID: 25823474]
[20]
Kierdorf, K.; Prinz, M. Factors regulating microglia activation. Front. Cell. Neurosci., 2013, 7, 44.
[http://dx.doi.org/10.3389/fncel.2013.00044] [PMID: 23630462]
[21]
Bylicky, M.A.; Mueller, G.P.; Day, R.M. Mechanisms of endogenous neuroprotective effects of astrocytes in brain injury. Oxid. Med. Cell. Longev., 2018, 2018 6501031
[http://dx.doi.org/10.1155/2018/6501031] [PMID: 29805731]
[22]
Liu, W.; Tang, Y.; Feng, J. Cross talk between activation of microglia and astrocytes in pathological conditions in the central nervous system. Life Sci., 2011, 89(5-6), 141-146.
[http://dx.doi.org/10.1016/j.lfs.2011.05.011] [PMID: 21684291]
[23]
Hu, S.; Sheng, W.S.; Ehrlich, L.C.; Peterson, P.K.; Chao, C.C. Cytokine effects on glutamate uptake by human astrocytes. Neuroimmunomodulation, 2000, 7(3), 153-159.
[http://dx.doi.org/10.1159/000026433] [PMID: 10754403]
[24]
Thornton, P.; Pinteaux, E.; Gibson, R.M.; Allan, S.M.; Rothwell, N.J. Interleukin-1-induced neurotoxicity is mediated by glia and requires caspase activation and free radical release. J. Neurochem., 2006, 98(1), 258-266.
[http://dx.doi.org/10.1111/j.1471-4159.2006.03872.x] [PMID: 16805812]
[25]
Boutin, H.; LeFeuvre, R.A.; Horai, R.; Asano, M.; Iwakura, Y.; Rothwell, N.J. Role of IL-1alpha and IL-1beta in ischemic brain damage. J. Neurosci., 2001, 21(15), 5528-5534.
[http://dx.doi.org/10.1523/JNEUROSCI.21-15-05528.2001] [PMID: 11466424]
[26]
da Cunha, A.; Jefferson, J.A.; Jackson, R.W.; Vitković, L. Glial cell-specific mechanisms of TGF-beta 1 induction by IL-1 in cerebral cortex. J. Neuroimmunol., 1993, 42(1), 71-85.
[http://dx.doi.org/10.1016/0165-5728(93)90214-J] [PMID: 8423208]
[27]
Abbott, N.J.; Rönnbäck, L.; Hansson, E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci., 2006, 7(1), 41-53.
[http://dx.doi.org/10.1038/nrn1824] [PMID: 16371949]
[28]
Uddin, M.S.; Stachowiak, A.; Mamun, A.A.; Tzvetkov, N.T.; Takeda, S.; Atanasov, A.G.; Bergantin, L.B.; Abdel-Daim, M.M.; Stankiewicz, A.M. Autophagy and Alzheimer's Disease: From Molecular Mechanisms to Therapeutic Implications. Front Aging Neurosci., 2018, 30, 10-04.
[http://dx.doi.org/10.3389/fnagi.2018.00004] [PMID: 29441009]
[29]
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]
[30]
Corminboeuf, O.; Leroy, X. FPR2/ALXR agonists and the resolution of inflammation. J. Med. Chem., 2015, 58(2), 537-559.
[http://dx.doi.org/10.1021/jm501051x] [PMID: 25365541]
[31]
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., 2007, 21(2), 325-332.
[http://dx.doi.org/10.1096/fj.06-7227rev] [PMID: 17267386]
[32]
Stables, M.J.; Gilroy, D.W. Old and new generation lipid mediators in acute inflammation and resolution. Prog. Lipid Res., 2011, 50(1), 35-51.
[http://dx.doi.org/10.1016/j.plipres.2010.07.005] [PMID: 20655950]
[33]
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]
[34]
Serhan, C.N. Pro-resolving lipid mediators are leads for resolution physiology. Nature, 2014, 510(7503), 92-101.
[http://dx.doi.org/10.1038/nature13479] [PMID: 24899309]
[35]
Perretti, M.; Leroy, X.; Bland, E.J.; Montero-Melendez, T. Resolution pharmacology: Opportunities for therapeutic innovation in inflammation. Trends Pharmacol. Sci., 2015, 36(11), 737-755.
[http://dx.doi.org/10.1016/j.tips.2015.07.007] [PMID: 26478210]
[36]
Headland, S.E.; Norling, L.V. The resolution of inflammation: Principles and challenges. Semin. Immunol., 2015, 27(3), 149-160.
[http://dx.doi.org/10.1016/j.smim.2015.03.014] [PMID: 25911383]
[37]
Fiorucci, S.; Distrutti, E.; Mencarelli, A.; Rizzo, G.; Lorenzo, A.R.; Baldoni, M.; Del Soldato, P.; Morelli, A.; Wallace, J.L. Cooperation between aspirin-triggered lipoxin and nitric oxide (NO) mediates antiadhesive properties of 2-(Acetyloxy)benzoic acid 3-(nitrooxymethyl)phenyl ester (NCX-4016) (NO-aspirin) on neutrophil-endothelial cell adherence. J. Pharmacol. Exp. Ther., 2004, 309(3), 1174-1182.
[http://dx.doi.org/10.1124/jpet.103.063651] [PMID: 14762100]
[38]
Petasis, N.A.; Akritopoulou-Zanze, I.; Fokin, V.V.; Bernasconi, G.; Keledjian, R.; Yang, R.; Uddin, J.; Nagulapalli, K.C.; Serhan, C.N. Design, synthesis and bioactions of novel stable mimetics of lipoxins and aspirin-triggered lipoxins. Prostaglandins Leukot. Essent. Fatty Acids, 2005, 73(3-4), 301-321.
[http://dx.doi.org/10.1016/j.plefa.2005.05.020] [PMID: 16098719]
[39]
Mitchell, S.; Thomas, G.; Harvey, K.; Cottell, D.; Reville, K.; Berlasconi, G.; Petasis, N.A.; Erwig, L.; Rees, A.J.; Savill, J.; Brady, H.R.; Godson, C. Lipoxins, aspirin-triggered epi-lipoxins, lipoxin stable analogues, and the resolution of inflammation: stimulation of macrophage phagocytosis of apoptotic neutrophils in vivo. J. Am. Soc. Nephrol., 2002, 13(10), 2497-2507.
[http://dx.doi.org/10.1097/01.ASN.0000032417.73640.72] [PMID: 12239238]
[40]
Nigam, S.K. Subcellular distribution of small GTP binding proteins in pancreas: identification of small GTP binding proteins in the rough endoplasmic reticulum. Proc. Natl. Acad. Sci. USA, 1990, 87(4), 1296-1299.
[http://dx.doi.org/10.1073/pnas.87.4.1296] [PMID: 2106133]
[41]
Fiore, S.; Ryeom, S.W.; Weller, P.F.; Serhan, C.N. Lipoxin recognition sites. Specific binding of labeled lipoxin A4 with human neutrophils. J. Biol. Chem., 1992, 267(23), 16168-16176.
[PMID: 1322894]
[42]
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]
[43]
Bäck, M.; Powell, W.S.; Dahlén, S.E.; Drazen, J.M.; Evans, J.F.; Serhan, C.N.; Shimizu, T.; Yokomizo, T.; Rovati, G.E. Update on leukotriene, lipoxin and oxoeicosanoid receptors: IUPHAR Review 7. Br. J. Pharmacol., 2014, 171(15), 3551-3574.
[http://dx.doi.org/10.1111/bph.12665] [PMID: 24588652]
[44]
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]
[45]
Forsman, H.; Dahlgren, C. Lipoxin A(4) metabolites/analogues from two commercial sources have no effects on TNF-alpha-mediated priming or activation through the neutrophil formyl peptide receptors. Scand. J. Immunol., 2009, 70(4), 396-402.
[http://dx.doi.org/10.1111/j.1365-3083.2009.02311.x] [PMID: 19751275]
[46]
Forsman, H.; Önnheim, K.; Andreasson, E.; Dahlgren, C. What formyl peptide receptors, if any, are triggered by compound 43 and lipoxin A4? Scand. J. Immunol., 2011, 74(3), 227-234.
[http://dx.doi.org/10.1111/j.1365-3083.2011.02570.x] [PMID: 21535079]
[47]
Hanson, J.; Ferreirós, N.; Pirotte, B.; Geisslinger, G.; Offermanns, S. Heterologously expressed formyl peptide receptor 2 (FPR2/ALX) does not respond to lipoxin A4. Biochem. Pharmacol., 2013, 85(12), 1795-1802.
[http://dx.doi.org/10.1016/j.bcp.2013.04.019] [PMID: 23643932]
[48]
Planagumà, A.; Domenech, T.; Jover, I.; Ramos, I.; Sentellas, S.; Malhotra, R.; Miralpeix, M. Lack of activity of 15-epi-lipoxin A4 on FPR2/ALX and CysLT1 receptors in interleukin-8-driven human neutrophil function. Clin. Exp. Immunol., 2013, 173(2), 298-309.
[http://dx.doi.org/10.1111/cei.12110] [PMID: 23607720]
[49]
Bianchi, M.E. DAMPs, PAMPs and alarmins: all we need to know about danger. J. Leukoc. Biol., 2007, 81(1), 1-5.
[http://dx.doi.org/10.1189/jlb.0306164] [PMID: 17032697]
[50]
Carp, H. Mitochondrial N-formylmethionyl proteins as chemoattractants for neutrophils. J. Exp. Med., 1982, 155(1), 264-275.
[http://dx.doi.org/10.1084/jem.155.1.264] [PMID: 6274994]
[51]
Zhang, Q.; Raoof, M.; Chen, Y.; Sumi, Y.; Sursal, T.; Junger, W.; Brohi, K.; Itagaki, K.; Hauser, C.J. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature, 2010, 464(7285), 104-107.
[http://dx.doi.org/10.1038/nature08780] [PMID: 20203610]
[52]
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]
[53]
Cattaneo, F.; Guerra, G.; Ammendola, R. Expression and signaling of formyl-peptide receptors in the brain. Neurochem. Res., 2010, 35(12), 2018-2026.
[http://dx.doi.org/10.1007/s11064-010-0301-5] [PMID: 21042851]
[54]
Lacy, M.; Jones, J.; Whittemore, S.R.; Haviland, D.L.; Wetsel, R.A.; Barnum, S.R. Expression of the receptors for the C5a anaphylatoxin, interleukin-8 and FMLP by human astrocytes and microglia. J. Neuroimmunol., 1995, 61(1), 71-78.
[http://dx.doi.org/10.1016/0165-5728(95)00075-D] [PMID: 7560015]
[55]
Müller-Ladner, U.; Jones, J.L.; Wetsel, R.A.; Gay, S.; Raine, C.S.; Barnum, S.R. Enhanced expression of chemotactic receptors in multiple sclerosis lesions. J. Neurol. Sci., 1996, 144(1-2), 135-141.
[http://dx.doi.org/10.1016/S0022-510X(96)00217-1] [PMID: 8994115]
[56]
Yao, J.; Harvath, L.; Gilbert, D.L.; Colton, C.A. Chemotaxis by a CNS macrophage, the microglia. J. Neurosci. Res., 1990, 27(1), 36-42.
[http://dx.doi.org/10.1002/jnr.490270106] [PMID: 2254955]
[57]
Cui, Y.H.; Le, Y.; Gong, W.; Proost, P.; Van Damme, J.; Murphy, W.J.; Wang, J.M. Bacterial lipopolysaccharide selectively up-regulates the function of the chemotactic peptide receptor formyl peptide receptor 2 in murine microglial cells. J. Immunol., 2002, 168(1), 434-442.
[http://dx.doi.org/10.4049/jimmunol.168.1.434] [PMID: 11751990]
[58]
Hilger, D.; Masureel, M.; Kobilka, B.K. Structure and dynamics of GPCR signaling complexes. Nat. Struct. Mol. Biol., 2018, 25(1), 4-12.
[http://dx.doi.org/10.1038/s41594-017-0011-7] [PMID: 29323277]
[59]
Fredriksson, R.; Lagerström, M.C.; Lundin, L.G.; Schiöth, H.B. The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol. Pharmacol., 2003, 63(6), 1256-1272.
[http://dx.doi.org/10.1124/mol.63.6.1256] [PMID: 12761335]
[60]
Perez, D.M. The evolutionarily triumphant G-protein-coupled receptor. Mol. Pharmacol., 2003, 63(6), 1202-1205.
[http://dx.doi.org/10.1124/mol.63.6.1202] [PMID: 12761327]
[61]
Venkatakrishnan, A.J.; Deupi, X.; Lebon, G.; Tate, C.G.; Schertler, G.F.; Babu, M.M. Molecular signatures of G-protein-coupled receptors. Nature, 2013, 494(7436), 185-194.
[http://dx.doi.org/10.1038/nature11896] [PMID: 23407534]
[62]
Sensoy, O.; Weinstein, H. A mechanistic role of Helix 8 in GPCRs: Computational modeling of the dopamine D2 receptor interaction with the GIPC1-PDZ-domain. Biochim. Biophys. Acta, 2015, 1848(4), 976-983.
[http://dx.doi.org/10.1016/j.bbamem.2014.12.002] [PMID: 25592838]
[63]
Katritch, V.; Cherezov, V.; Stevens, R.C. Diversity and modularity of G protein-coupled receptor structures. Trends Pharmacol. Sci., 2012, 33(1), 17-27.
[http://dx.doi.org/10.1016/j.tips.2011.09.003] [PMID: 22032986]
[64]
He, R.; Browning, D.D.; Ye, R.D. Differential roles of the NPXXY motif in formyl peptide receptor signaling. J. Immunol., 2001, 166(6), 4099-4105.
[http://dx.doi.org/10.4049/jimmunol.166.6.4099] [PMID: 11238659]
[65]
Bennett, T.A.; Maestas, D.C.; Prossnitz, E.R. Arrestin binding to the G protein-coupled N-formyl peptide receptor is regulated by the conserved “DRY” sequence. J. Biol. Chem., 2000, 275(32), 24590-24594.
[http://dx.doi.org/10.1074/jbc.C000314200] [PMID: 10823817]
[66]
Boulay, F.; Tardif, M.; Brouchon, L.; Vignais, P. Synthesis and use of a novel N-formyl peptide derivative to isolate a human N-formyl peptide receptor cDNA. Biochem. Biophys. Res. Commun., 1990, 168(3), 1103-1109.
[http://dx.doi.org/10.1016/0006-291X(90)91143-G] [PMID: 2161213]
[67]
Boulay, F.; Tardif, M.; Brouchon, L.; Vignais, P. The human N-formylpeptide receptor. Characterization of two cDNA isolates and evidence for a new subfamily of G-protein-coupled receptors. Biochemistry, 1990, 29(50), 11123-11133.
[http://dx.doi.org/10.1021/bi00502a016] [PMID: 2176894]
[68]
Ye, R.D.; Cavanagh, S.L.; Quehenberger, O.; Prossnitz, E.R.; Cochrane, C.G. Isolation of a cDNA that encodes a novel granulocyte N-formyl peptide receptor. Biochem. Biophys. Res. Commun., 1992, 184(2), 582-589.
[http://dx.doi.org/10.1016/0006-291X(92)90629-Y] [PMID: 1374236]
[69]
Murphy, P.M.; Ozçelik, T.; Kenney, R.T.; Tiffany, H.L.; McDermott, D.; Francke, U. A structural homologue of the N-formyl peptide receptor. Characterization and chromosome mapping of a peptide chemoattractant receptor family. J. Biol. Chem., 1992, 267(11), 7637-7643.
[PMID: 1373134]
[70]
Bao, L.; Gerard, N.P.; Eddy, R.L., Jr; Shows, T.B.; Gerard, C. Mapping of genes for the human C5a receptor (C5AR), human FMLP receptor (FPR), and two FMLP receptor homologue orphan receptors (FPRH1, FPRH2) to chromosome 19. Genomics, 1992, 13(2), 437-440.
[http://dx.doi.org/10.1016/0888-7543(92)90265-T] [PMID: 1612600]
[71]
Muto, Y.; Guindon, S.; Umemura, T.; Kőhidai, L.; Ueda, H. Adaptive evolution of formyl peptide receptors in mammals. J. Mol. Evol., 2015, 80(2), 130-141.
[http://dx.doi.org/10.1007/s00239-015-9666-z] [PMID: 25627928]
[72]
Rabiet, M.J.; Macari, L.; Dahlgren, C.; Boulay, F. N-formyl peptide receptor 3 (FPR3) departs from the homologous FPR2/ALX receptor with regard to the major processes governing chemoattractant receptor regulation, expression at the cell surface, and phosphorylation. J. Biol. Chem., 2011, 286(30), 26718-26731.
[http://dx.doi.org/10.1074/jbc.M111.244590] [PMID: 21543323]
[73]
Alvarez, V.; Coto, E.; Setién, F.; González-Roces, S.; López-Larrea, C. Molecular evolution of the N-formyl peptide and C5a receptors in non-human primates. Immunogenetics, 1996, 44(6), 446-452.
[http://dx.doi.org/10.1007/BF02602806] [PMID: 8824156]
[74]
Migeotte, I.; Communi, D.; Parmentier, M. Formyl peptide receptors: a promiscuous subfamily of G protein-coupled receptors controlling immune responses. Cytokine Growth Factor Rev., 2006, 17(6), 501-519.
[http://dx.doi.org/10.1016/j.cytogfr.2006.09.009] [PMID: 17084101]
[75]
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]
[76]
Le, Y.; Hu, J.; Gong, W.; Shen, W.; Li, B.; Dunlop, N.M.; Halverson, D.O.; Blair, D.G.; Wang, J.M. Expression of functional formyl peptide receptors by human astrocytoma cell lines. J. Neuroimmunol., 2000, 111(1-2), 102-108.
[http://dx.doi.org/10.1016/S0165-5728(00)00373-8] [PMID: 11063827]
[77]
Gao, J.L.; Lee, E.J.; Murphy, P.M. Impaired antibacterial host defense in mice lacking the N-formylpeptide receptor. J. Exp. Med., 1999, 189(4), 657-662.
[http://dx.doi.org/10.1084/jem.189.4.657] [PMID: 9989980]
[78]
Liu, M.; Chen, K.; Yoshimura, T.; Liu, Y.; Gong, W.; Wang, A.; Gao, J.L.; Murphy, P.M.; Wang, J.M. Formylpeptide receptors are critical for rapid neutrophil mobilization in host defense against Listeria monocytogenes. Sci. Rep., 2012, 2, 786.
[http://dx.doi.org/10.1038/srep00786] [PMID: 23139859]
[79]
Hartt, J.K.; Barish, G.; Murphy, P.M.; Gao, J.L. N-formylpeptides induce two distinct concentration optima for mouse neutrophil chemotaxis by differential interaction with two N-formylpeptide receptor (FPR) subtypes. Molecular characterization of FPR2, a second mouse neutrophil FPR. J. Exp. Med., 1999, 190(5), 741-747.
[http://dx.doi.org/10.1084/jem.190.5.741] [PMID: 10477558]
[80]
He, H.Q.; Liao, D.; Wang, Z.G.; Wang, Z.L.; Zhou, H.C.; Wang, M.W.; Ye, R.D. Functional characterization of three mouse formyl peptide receptors. Mol. Pharmacol., 2013, 83(2), 389-398.
[http://dx.doi.org/10.1124/mol.112.081315] [PMID: 23160941]
[81]
Liang, T.S.; Wang, J.M.; Murphy, P.M.; Gao, J.L. Serum amyloid A is a chemotactic agonist at FPR2, a low-affinity N-formylpeptide receptor on mouse neutrophils. Biochem. Biophys. Res. Commun., 2000, 270(2), 331-335.
[http://dx.doi.org/10.1006/bbrc.2000.2416] [PMID: 10753626]
[82]
Tiffany, H.L.; Lavigne, M.C.; Cui, Y.H.; Wang, J.M.; Leto, T.L.; Gao, J.L.; Murphy, P.M. Amyloid-beta induces chemotaxis and oxidant stress by acting at formylpeptide receptor 2, a G protein-coupled receptor expressed in phagocytes and brain. J. Biol. Chem., 2001, 276(26), 23645-23652.
[http://dx.doi.org/10.1074/jbc.M101031200] [PMID: 11316806]
[83]
Gao, J.L.; Guillabert, A.; Hu, J.; Le, Y.; Urizar, E.; Seligman, E.; Fang, K.J.; Yuan, X.; Imbault, V.; Communi, D.; Wang, J.M.; Parmentier, M.; Murphy, P.M.; Migeotte, I. F2L, a peptide derived from heme-binding protein, chemoattracts mouse neutrophils by specifically activating Fpr2, the low-affinity N-formylpeptide receptor. J. Immunol., 2007, 178(3), 1450-1456.
[http://dx.doi.org/10.4049/jimmunol.178.3.1450] [PMID: 17237393]
[84]
Migeotte, I.; Riboldi, E.; Franssen, J.D.; Grégoire, F.; Loison, C.; Wittamer, V.; Detheux, M.; Robberecht, P.; Costagliola, S.; Vassart, G.; Sozzani, S.; Parmentier, M.; Communi, D. Identification and characterization of an endogenous chemotactic ligand specific for FPRL2. J. Exp. Med., 2005, 201(1), 83-93.
[http://dx.doi.org/10.1084/jem.20041277] [PMID: 15623572]
[85]
Tiffany, H.L.; Gao, J.L.; Roffe, E.; Sechler, J.M.; Murphy, P.M. Characterization of Fpr-rs8, an atypical member of the mouse formyl peptide receptor gene family. J. Innate Immun., 2011, 3(5), 519-529.
[http://dx.doi.org/10.1159/000327718] [PMID: 21691049]
[86]
Takano, T.; Fiore, S.; Maddox, J.F.; Brady, H.R.; Petasis, N.A.; Serhan, C.N. Aspirin-triggered 15-epi-lipoxin A4 (LXA4) and LXA4 stable analogues are potent inhibitors of acute inflammation: evidence for anti-inflammatory receptors. J. Exp. Med., 1997, 185(9), 1693-1704.
[http://dx.doi.org/10.1084/jem.185.9.1693] [PMID: 9151906]
[87]
Wang, Z.G.; Ye, R.D. Characterization of two new members of the formyl peptide receptor gene family from 129S6 mice. Gene, 2002, 299(1-2), 57-63.
[http://dx.doi.org/10.1016/S0378-1119(02)01012-0] [PMID: 12459252]
[88]
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]
[89]
Xu, Z.Q.; Zhang, X.; Scott, L. Regulation of G protein-coupled receptor trafficking. Acta Physiol. (Oxf.), 2007, 190(1), 39-45.
[http://dx.doi.org/10.1111/j.1365-201X.2007.01695.x] [PMID: 17428231]
[90]
Maaty, W.S.; Lord, C.I.; Gripentrog, J.M.; Riesselman, M.; Keren-Aviram, G.; Liu, T.; Dratz, E.A.; Bothner, B.; Jesaitis, A.J. Identification of C-terminal phosphorylation sites of N-formyl peptide receptor-1 (FPR1) in human blood neutrophils. J. Biol. Chem., 2013, 288(38), 27042-27058.
[http://dx.doi.org/10.1074/jbc.M113.484113] [PMID: 23873933]
[91]
Filep, J.G. Biasing the lipoxin A4/formyl peptide receptor 2 pushes inflammatory resolution. Proc. Natl. Acad. Sci. USA, 2013, 110(45), 18033-18034.
[http://dx.doi.org/10.1073/pnas.1317798110] [PMID: 24154723]
[92]
Brandenburg, L.O.; Konrad, M.; Wruck, C.J.; Koch, T.; Lucius, R.; Pufe, T. Functional and physical interactions between formyl-peptide-receptors and scavenger receptor MARCO and their involvement in amyloid beta 1-42-induced signal transduction in glial cells. J. Neurochem., 2010, 113(3), 749-760.
[http://dx.doi.org/10.1111/j.1471-4159.2010.06637.x] [PMID: 20141570]
[93]
Raabe, C.A.; Gröper, J.; Rescher, U. Biased perspectives on formyl peptide receptors. Biochim. Biophys. Acta Mol. Cell Res., 2019, 1866(2), 305-316.
[http://dx.doi.org/10.1016/j.bbamcr.2018.11.015] [PMID: 30521870]
[94]
Chiang, N.; Fierro, I.M.; Gronert, K.; Serhan, C.N. Activation of lipoxin A(4) receptors by aspirin-triggered lipoxins and select peptides evokes ligand-specific responses in inflammation. J. Exp. Med., 2000, 191(7), 1197-1208.
[http://dx.doi.org/10.1084/jem.191.7.1197] [PMID: 10748237]
[95]
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]
[96]
Schepetkin, I.A.; Khlebnikov, A.I.; Giovannoni, M.P.; Kirpotina, L.N.; Cilibrizzi, A.; Quinn, M.T. Development of small molecule non-peptide formyl peptide receptor (FPR) ligands and molecular modeling of their recognition. Curr. Med. Chem., 2014, 21(13), 1478-1504.
[http://dx.doi.org/10.2174/0929867321666131218095521] [PMID: 24350845]
[97]
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]
[98]
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]
[99]
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]propanamides 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]
[100]
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]
[101]
Clish, C.B.; Levy, B.D.; Chiang, N.; Tai, H.H.; Serhan, C.N. Oxidoreductases in lipoxin A4 metabolic inactivation: a novel role for 15-onoprostaglandin 13-reductase/leukotriene B4 12-hydroxydehydrogenase in inflammation. J. Biol. Chem., 2000, 275(33), 25372-25380.
[http://dx.doi.org/10.1074/jbc.M002863200] [PMID: 10837478]
[102]
Alzheimer, A.; Stelzmann, R.A.; Schnitzlein, H.N.; Murtagh, F.R. An English translation of Alzheimer’s 1907 paper, “Uber eine eigenartige Erkankung der Hirnrinde. Clin. Anat., 1995, 8(6), 429-431.
[http://dx.doi.org/10.1002/ca.980080612] [PMID: 8713166]
[103]
Doody, R.S.; Farlow, M.; Aisen, P.S. Phase 3 trials of solanezumab and bapineuzumab for Alzheimer’s disease. N. Engl. J. Med., 2014, 370(15), 1460.
[PMID: 24716687]
[104]
Akama, K.T.; Van Eldik, L.J. Beta-amyloid stimulation of inducible nitric-oxide synthase in astrocytes is interleukin-1beta- and tumor necrosis factor-alpha (TNFalpha)-dependent, and involves a TNFalpha receptor-associated factor- and NFkappaB-inducing kinase-dependent signaling mechanism. J. Biol. Chem., 2000, 275(11), 7918-7924.
[http://dx.doi.org/10.1074/jbc.275.11.7918] [PMID: 10713108]
[105]
Akiyama, H.; Barger, S.; Barnum, S.; Bradt, B.; Bauer, J.; Cole, G.M.; Cooper, N.R.; Eikelenboom, P.; Emmerling, M.; Fiebich, B.L.; Finch, C.E.; Frautschy, S.; Griffin, W.S.; Hampel, H.; Hull, M.; Landreth, G.; Lue, L.; Mrak, R.; Mackenzie, I.R.; McGeer, P.L.; O’Banion, M.K.; Pachter, J.; Pasinetti, G.; Plata-Salaman, C.; Rogers, J.; Rydel, R.; Shen, Y.; Streit, W.; Strohmeyer, R.; Tooyoma, I.; Van Muiswinkel, F.L.; Veerhuis, R.; Walker, D.; Webster, S.; Wegrzyniak, B.; Wenk, G.; Wyss-Coray, T. Inflammation and Alzheimer’s disease. Neurobiol. Aging, 2000, 21(3), 383-421.
[http://dx.doi.org/10.1016/S0197-4580(00)00124-X] [PMID: 10858586]
[106]
Combs, C.K.; Johnson, D.E.; Karlo, J.C.; Cannady, S.B.; Landreth, G.E. Inflammatory mechanisms in Alzheimer’s disease: inhibition of beta-amyloid-stimulated proinflammatory responses and neurotoxicity by PPARgamma agonists. J. Neurosci., 2000, 20(2), 558-567.
[http://dx.doi.org/10.1523/JNEUROSCI.20-02-00558.2000] [PMID: 10632585]
[107]
Griffin, W.S.; Stanley, L.C.; Ling, C.; White, L.; MacLeod, V.; Perrot, L.J.; White, C.L., III; Araoz, C. Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease. Proc. Natl. Acad. Sci. USA, 1989, 86(19), 7611-7615.
[http://dx.doi.org/10.1073/pnas.86.19.7611] [PMID: 2529544]
[108]
Griffin, W.S.T.; Sheng, J.G.; Roberts, G.W.; Mrak, R.E. Interleukin-1 expression in different plaque types in Alzheimer’s disease: significance in plaque evolution. J. Neuropathol. Exp. Neurol., 1995, 54(2), 276-281.
[http://dx.doi.org/10.1097/00005072-199503000-00014] [PMID: 7876895]
[109]
McGeer, P.L.; Akiyama, H.; Itagaki, S.; McGeer, E.G. Immune system response in Alzheimer’s disease. Can. J. Neurol. Sci., 1989, 16(4)(Suppl.), 516-527.
[http://dx.doi.org/10.1017/S0317167100029863] [PMID: 2804814]
[110]
McGeer, P.L.; McGeer, E.G. The inflammatory response system of brain: implications for therapy of Alzheimer and other neurodegenerative diseases. Brain Res. Brain Res. Rev., 1995, 21(2), 195-218.
[http://dx.doi.org/10.1016/0165-0173(95)00011-9] [PMID: 8866675]
[111]
Mrak, R.E.; Griffin, W.S.T. Common inflammatory mechanisms in Lewy body disease and Alzheimer disease. J. Neuropathol. Exp. Neurol., 2007, 66(8), 683-686.
[http://dx.doi.org/10.1097/nen.0b013e31812503e1] [PMID: 17882012]
[112]
Mrak, R.E.; Sheng, J.G.; Griffin, W.S.T. Glial cytokines in Alzheimer’s disease: review and pathogenic implications. Hum. Pathol., 1995, 26(8), 816-823.
[http://dx.doi.org/10.1016/0046-8177(95)90001-2] [PMID: 7635444]
[113]
Tuppo, E.E.; Arias, H.R. The role of inflammation in Alzheimer’s disease. Int. J. Biochem. Cell Biol., 2005, 37(2), 289-305.
[http://dx.doi.org/10.1016/j.biocel.2004.07.009] [PMID: 15474976]
[114]
Walters, A.; Phillips, E.; Zheng, R.; Biju, M.; Kuruvilla, T. Evidence for neuroinflammation in Alzheimer’s disease. Prog. Neurol. Psychiatry, 2016, 20, 25-31.
[http://dx.doi.org/10.1002/pnp.444]
[115]
Beard, C.M.; Waring, S.C.; O’Brien, P.C.; Kurland, L.T.; Kokmen, E. Nonsteroidal anti-inflammatory drug use and Alzheimer’s disease: a case-control study in Rochester, Minnesota, 1980 through 1984. Mayo Clin. Proc., 1998, 73(10), 951-955.
[http://dx.doi.org/10.4065/73.10.951] [PMID: 9787743]
[116]
Breitner, J.C.; Gau, B.A.; Welsh, K.A.; Plassman, B.L.; McDonald, W.M.; Helms, M.J.; Anthony, J.C. Inverse association of anti-inflammatory treatments and Alzheimer’s disease: initial results of a co-twin control study. Neurology, 1994, 44(2), 227-232.
[http://dx.doi.org/10.1212/WNL.44.2.227] [PMID: 8309563]
[117]
Rich, J.B.; Rasmusson, D.X.; Folstein, M.F.; Carson, K.A.; Kawas, C.; Brandt, J. Nonsteroidal anti-inflammatory drugs in Alzheimer’s disease. Neurology, 1995, 45(1), 51-55.
[http://dx.doi.org/10.1212/WNL.45.1.51] [PMID: 7824134]
[118]
Goldgaber, D.; Harris, H.W.; Hla, T.; Maciag, T.; Donnelly, R.J.; Jacobsen, J.S.; Vitek, M.P.; Gajdusek, D.C. Interleukin 1 regulates synthesis of amyloid beta-protein precursor mRNA in human endothelial cells. Proc. Natl. Acad. Sci. USA, 1989, 86(19), 7606-7610.
[http://dx.doi.org/10.1073/pnas.86.19.7606] [PMID: 2508093]
[119]
Plassman, B.L.; Havlik, R.J.; Steffens, D.C.; Helms, M.J.; Newman, T.N.; Drosdick, D.; Phillips, C.; Gau, B.A.; Welsh-Bohmer, K.A.; Burke, J.R.; Guralnik, J.M.; Breitner, J.C. Documented head injury in early adulthood and risk of Alzheimer’s disease and other dementias. Neurology, 2000, 55(8), 1158-1166.
[http://dx.doi.org/10.1212/WNL.55.8.1158] [PMID: 11071494]
[120]
Quintanilla, R.A.; Orellana, D.I.; González-Billault, C.; Maccioni, R.B. Interleukin-6 induces Alzheimer-type phosphorylation of tau protein by deregulating the cdk5/p35 pathway. Exp. Cell Res., 2004, 295(1), 245-257.
[http://dx.doi.org/10.1016/j.yexcr.2004.01.002] [PMID: 15051507]
[121]
Cagnin, A.; Brooks, D.J.; Kennedy, A.M.; Gunn, R.N.; Myers, R.; Turkheimer, F.E.; Jones, T.; Banati, R.B. In-vivo measurement of activated microglia in dementia. Lancet, 2001, 358(9280), 461-467.
[http://dx.doi.org/10.1016/S0140-6736(01)05625-2] [PMID: 11513911]
[122]
Fan, Z.; Brooks, D.J.; Okello, A.; Edison, P. An early and late peak in microglial activation in Alzheimer’s disease trajectory. Brain, 2017, 140(3), 792-803.
[http://dx.doi.org/10.1093/brain/aww349] [PMID: 28122877]
[123]
Parbo, P.; Ismail, R.; Hansen, K.V.; Amidi, A.; Mårup, F.H.; Gottrup, H.; Brændgaard, H.; Eriksson, B.O.; Eskildsen, S.F.; Lund, T.E.; Tietze, A.; Edison, P.; Pavese, N.; Stokholm, M.G.; Borghammer, P.; Hinz, R.; Aanerud, J.; Brooks, D.J. Brain inflammation accompanies amyloid in the majority of mild cognitive impairment cases due to Alzheimer’s disease. Brain, 2017, 140(7), 2002-2011.
[http://dx.doi.org/10.1093/brain/awx120] [PMID: 28575151]
[124]
Swardfager, W.; Lanctôt, K.; Rothenburg, L.; Wong, A.; Cappell, J.; Herrmann, N. A meta-analysis of cytokines in Alzheimer’s disease. Biol. Psychiatry, 2010, 68(10), 930-941.
[http://dx.doi.org/10.1016/j.biopsych.2010.06.012] [PMID: 20692646]
[125]
Bishnoi, R.J.; Palmer, R.F.; Royall, D.R. Serum interleukin (IL)-15 as a biomarker of Alzheimer’s disease. PLoS One, 2015, 10(2)e0117282
[http://dx.doi.org/10.1371/journal.pone.0117282] [PMID: 25710473]
[126]
Lai, K.S.P.; Liu, C.S.; Rau, A.; Lanctôt, K.L.; Köhler, C.A.; Pakosh, M.; Carvalho, A.F.; Herrmann, N. Peripheral inflammatory markers in Alzheimer’s disease: a systematic review and meta-analysis of 175 studies. J. Neurol. Neurosurg. Psychiatry, 2017, 88(10), 876-882.
[http://dx.doi.org/10.1136/jnnp-2017-316201] [PMID: 28794151]
[127]
Walker, D.G.; Dalsing-Hernandez, J.E.; Campbell, N.A.; Lue, L.F. Decreased expression of CD200 and CD200 receptor in Alzheimer’s disease: a potential mechanism leading to chronic inflammation. Exp. Neurol., 2009, 215(1), 5-19.
[http://dx.doi.org/10.1016/j.expneurol.2008.09.003] [PMID: 18938162]
[128]
Sawikr, Y.; Yarla, N.S.; Peluso, I.; Kamal, M.A.; Aliev, G.; Bishayee, A. Neuroinflammation in alzheimer’s disease: The preventive and therapeutic potential of polyphenolic nutraceuticals. Adv. Protein Chem. Struct. Biol., 2017, 108, 33-57.
[http://dx.doi.org/10.1016/bs.apcsb.2017.02.001] [PMID: 28427563]
[129]
Wilkins, H.M.; Swerdlow, R.H. Relationships between mitochondria and neuroinflammation: Implications for alzheimer’s disease. Curr. Top. Med. Chem., 2016, 16(8), 849-857.
[http://dx.doi.org/10.2174/1568026615666150827095102] [PMID: 26311426]
[130]
Dahlgren, C.; Gabl, M.; Holdfeldt, A.; Winther, M.; Forsman, H. Basic characteristics of the neutrophil receptors that recognize formylated peptides, a danger-associated molecular pattern generated by bacteria and mitochondria. Biochem. Pharmacol., 2016, 114, 22-39.
[http://dx.doi.org/10.1016/j.bcp.2016.04.014] [PMID: 27131862]
[131]
Raoof, M.; Zhang, Q.; Itagaki, K.; Hauser, C.J. Mitochondrial peptides are potent immune activators that activate human neutrophils via FPR-1. J. Trauma, 2010, 68(6), 1328-1332.
[http://dx.doi.org/10.1097/TA.0b013e3181dcd28d] [PMID: 20539176]
[132]
Arnardottir, H.H.; Dalli, J.; Colas, R.A.; Shinohara, M.; Serhan, C.N. Aging delays resolution of acute inflammation in mice: reprogramming the host response with novel nano-proresolving medicines. J. Immunol., 2014, 193(8), 4235-4244.
[http://dx.doi.org/10.4049/jimmunol.1401313] [PMID: 25217168]
[133]
Wang, X.; Puerta, E.; Cedazo-Minguez, A.; Hjorth, E.; Schultzberg, M. Insufficient resolution response in the hippocampus of a senescence-accelerated mouse model--SAMP8. J. Mol. Neurosci., 2015, 55(2), 396-405.
[http://dx.doi.org/10.1007/s12031-014-0346-z] [PMID: 24913689]
[134]
Pallas, M.; Camins, A.; Smith, M.A.; Perry, G.; Lee, H.G.; Casadesus, G. From aging to Alzheimer’s disease: unveiling “the switch” with the senescence-accelerated mouse model (SAMP8). J. Alzheimers Dis., 2008, 15(4), 615-624.
[http://dx.doi.org/10.3233/JAD-2008-15408] [PMID: 19096160]
[135]
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]
[136]
Dunn, H.C.; Ager, R.R.; Baglietto-Vargas, D.; Cheng, D.; Kitazawa, M.; Cribbs, D.H.; Medeiros, R. Restoration of lipoxin A4 signaling reduces Alzheimer’s disease-like pathology in the 3xTg-AD mouse model. J. Alzheimers Dis., 2015, 43(3), 893-903.
[http://dx.doi.org/10.3233/JAD-141335] [PMID: 25125468]
[137]
Zhu, M.; Wang, X.; Schultzberg, M.; Hjorth, E. Differential regulation of resolution in inflammation induced by amyloid-β42 and lipopolysaccharides in human microglia. J. Alzheimers Dis., 2015, 43(4), 1237-1250.
[http://dx.doi.org/10.3233/JAD-141233] [PMID: 25147114]
[138]
Gangemi, S.; Pescara, L.; D’Urbano, E.; Basile, G.; Nicita-Mauro, V.; Davì, G.; Romano, M. Aging is characterized by a profound reduction in anti-inflammatory lipoxin A4 levels. Exp. Gerontol., 2005, 40(7), 612-614.
[http://dx.doi.org/10.1016/j.exger.2005.04.004] [PMID: 15935589]
[139]
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, 40-50.
[http://dx.doi.org/10.1016/j.jalz.2013.12.024] [PMID: 24530025]
[140]
de Waal Malefyt, R.; Abrams, J.; Bennett, B.; Figdor, C.G.; de Vries, J.E. Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med., 1991, 174(5), 1209-1220.
[http://dx.doi.org/10.1084/jem.174.5.1209] [PMID: 1940799]
[141]
Moore, K.W.; de Waal Malefyt, R.; Coffman, R.L.; O’Garra, A. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol., 2001, 19, 683-765.
[http://dx.doi.org/10.1146/annurev.immunol.19.1.683] [PMID: 11244051]
[142]
Zhu, M.; Wang, X.; Hjorth, E.; Colas, R.A.; Schroeder, L.; Granholm, A.C.; Serhan, C.N.; Schultzberg, M. Pro-Resolving Lipid Mediators Improve Neuronal Survival and Increase Aβ42 Phagocytosis. Mol. Neurobiol., 2016, 53(4), 2733-2749.
[http://dx.doi.org/10.1007/s12035-015-9544-0] [PMID: 26650044]
[143]
Ashraf, G.M.; Tarasov, V.V.; Makhmutova, A.; Chubarev, V.N.; Avila-Rodriguez, M.; Bachurin, S.O.; Aliev, G. The Possibility of an Infectious Etiology of Alzheimer Disease. Mol. Neurobiol., 2019, 56(6), 4479-4491.
[http://dx.doi.org/10.1007/s12035-018-1388-y] [PMID: 30338482]
[144]
Schloer, S.; Hübel, N.; Masemann, D.; Pajonczyk, D.; Brunotte, L.; Ehrhardt, C.; Brandenburg, L.O.; Ludwig, S.; Gerke, V.; Rescher, U. The annexin A1/FPR2 signaling axis expands alveolar macrophages, limits viral replication, and attenuates pathogenesis in the murine influenza A virus infection model. FASEB J., 2019. fj201901265R
[http://dx.doi.org/10.1096/fj.201901265R] [PMID: 31398292]
[145]
Tarasov, V.V.; Kudryashov, N.V.; Chubarev, V.N.; Kalinina, T.S.; Barreto, G.E.; Ashraf, G.M.; Aliev, G. Pharmacological Aspects of Neuro-Immune Interactions. Curr. Pharm. Des., 2018, 24(1), 15-21.
[http://dx.doi.org/10.2174/1381612823666170829135115] [PMID: 28875850]
[146]
Aguilar-Valles, A.; Kim, J.; Jung, S.; Woodside, B.; Luheshi, G.N. Role of brain transmigrating neutrophils in depression-like behavior during systemic infection. Mol. Psychiatry, 2014, 19(5), 599-606.
[http://dx.doi.org/10.1038/mp.2013.137] [PMID: 24126927]
[147]
Wohleb, E.S.; Franklin, T.; Iwata, M.; Duman, R.S. Integrating neuroimmune systems in the neurobiology of depression. Nat. Rev. Neurosci., 2016, 17(8), 497-511.
[http://dx.doi.org/10.1038/nrn.2016.69] [PMID: 27277867]
[148]
Maes, M. Evidence for an immune response in major depression: a review and hypothesis. Prog. Neuropsychopharmacol. Biol. Psychiatry, 1995, 19(1), 11-38.
[http://dx.doi.org/10.1016/0278-5846(94)00101-M] [PMID: 7708925]
[149]
Maes, M.; Yirmyia, R.; Noraberg, J.; Brene, S.; Hibbeln, J.; Perini, G.; Kubera, M.; Bob, P.; Lerer, B.; Maj, M. The inflammatory & neurodegenerative (I&ND) hypothesis of depression: leads for future research and new drug developments in depression. Metab. Brain Dis., 2009, 24(1), 27-53.
[http://dx.doi.org/10.1007/s11011-008-9118-1] [PMID: 19085093]
[150]
Zorrilla, E.P.; Luborsky, L.; McKay, J.R.; Rosenthal, R.; Houldin, A.; Tax, A.; McCorkle, R.; Seligman, D.A.; Schmidt, K. The relationship of depression and stressors to immunological assays: a meta-analytic review. Brain Behav. Immun., 2001, 15(3), 199-226.
[http://dx.doi.org/10.1006/brbi.2000.0597] [PMID: 11566046]
[151]
Dowlati, Y.; Herrmann, N.; Swardfager, W.; Liu, H.; Sham, L.; Reim, E.K.; Lanctôt, K.L. A meta-analysis of cytokines in major depression. Biol. Psychiatry, 2010, 67(5), 446-457.
[http://dx.doi.org/10.1016/j.biopsych.2009.09.033] [PMID: 20015486]
[152]
Maes, M. Major depression and activation of the inflammatory response system. Adv. Exp. Med. Biol., 1999, 461, 25-46.
[http://dx.doi.org/10.1007/978-0-585-37970-8_2] [PMID: 10442165]
[153]
Raison, C.L.; Capuron, L.; Miller, A.H. Cytokines sing the blues: inflammation and the pathogenesis of depression. Trends Immunol., 2006, 27(1), 24-31.
[http://dx.doi.org/10.1016/j.it.2005.11.006] [PMID: 16316783]
[154]
Sutcigil, L.; Oktenli, C.; Musabak, U.; Bozkurt, A.; Cansever, A.; Uzun, O.; Sanisoglu, S.Y.; Yesilova, Z.; Ozmenler, N.; Ozsahin, A.; Sengul, A. Pro- and anti-inflammatory cytokine balance in major depression: effect of sertraline therapy. Clin. Dev. Immunol., 2007, 2007, 76396.
[http://dx.doi.org/10.1155/2007/76396] [PMID: 18317531]
[155]
Hernández, M.E.; Mendieta, D.; Martínez-Fong, D.; Loría, F.; Moreno, J.; Estrada, I.; Bojalil, R.; Pavón, L. Variations in circulating cytokine levels during 52 week course of treatment with SSRI for major depressive disorder. Eur. Neuropsychopharmacol., 2008, 18(12), 917-924.
[http://dx.doi.org/10.1016/j.euroneuro.2008.08.001] [PMID: 18805677]
[156]
Kubera, M.; Curzytek, K.; Duda, W.; Leskiewicz, M.; Basta-Kaim, A.; Budziszewska, B.; Roman, A.; Zajicova, A.; Holan, V.; Szczesny, E.; Lason, W.; Maes, M. A new animal model of (chronic) depression induced by repeated and intermittent lipopolysaccharide administration for 4 months. Brain Behav. Immun., 2013, 31, 96-104.
[http://dx.doi.org/10.1016/j.bbi.2013.01.001] [PMID: 23313516]
[157]
Diz-Chaves, Y.; Astiz, M.; Bellini, M.J.; Garcia-Segura, L.M. Prenatal stress increases the expression of proinflammatory cytokines and exacerbates the inflammatory response to LPS in the hippocampal formation of adult male mice. Brain Behav. Immun., 2013, 28, 196-206.
[http://dx.doi.org/10.1016/j.bbi.2012.11.013] [PMID: 23207108]
[158]
Xiu, L.J.; Lin, H.M.; Wei, P.K. The effect of chronic mild stress on tumor-bearing rats’ behavior and its mechanism. Neurosci. Lett., 2010, 473(1), 1-4.
[http://dx.doi.org/10.1016/j.neulet.2009.06.031] [PMID: 19539710]
[159]
Ślusarczyk, J.; Trojan, E.; Głombik, K.; Budziszewska, B.; Kubera, M.; Lasoń, W.; Popiołek-Barczyk, K.; Mika, J.; Wędzony, K.; Basta-Kaim, A. Prenatal stress is a vulnerability factor for altered morphology and biological activity of microglia cells. Front. Cell. Neurosci., 2015, 9, 82.
[http://dx.doi.org/10.3389/fncel.2015.00082] [PMID: 25814933]
[160]
Ślusarczyk, J.; Trojan, E.; Wydra, K.; Głombik, K.; Chamera, K.; Kucharczyk, M.; Budziszewska, B.; Kubera, M.; Lasoń, W.; Filip, M.; Basta-Kaim, A. Beneficial impact of intracerebroventricular fractalkine administration on behavioral and biochemical changes induced by prenatal stress in adult rats: Possible role of NLRP3 inflammasome pathway. Biochem. Pharmacol., 2016, 113, 45-56.
[http://dx.doi.org/10.1016/j.bcp.2016.05.008] [PMID: 27206338]
[161]
Gao, J.L.; Schneider, E.H.; Dimitrov, E.L.; Haun, F.; Pham, T.M.; Mohammed, A.H.; Usdin, T.B.; Murphy, P.M. Reduced fear memory and anxiety-like behavior in mice lacking formylpeptide receptor 1. Behav. Genet., 2011, 41(5), 724-733.
[http://dx.doi.org/10.1007/s10519-011-9467-0] [PMID: 21484271]
[162]
Gallo, I.; Rattazzi, L.; Piras, G.; Gobbetti, T.; Panza, E.; Perretti, M.; Dalley, J.W.; D’Acquisto, F. Formyl peptide receptor as a novel therapeutic target for anxiety-related disorders. PLoS One, 2014, 9(12) e114626
[http://dx.doi.org/10.1371/journal.pone.0114626] [PMID: 25517119]
[163]
Ishikawa, Y.; Deyama, S.; Shimoda, K.; Yoshikawa, K.; Ide, S.; Satoh, M.; Minami, M. Rapid and sustained antidepressant effects of resolvin D1 and D2 in a chronic unpredictable stress model. Behav. Brain Res., 2017, 332, 233-236.
[http://dx.doi.org/10.1016/j.bbr.2017.06.010] [PMID: 28610917]
[164]
Deyama, S.; Ishikawa, Y.; Yoshikawa, K.; Shimoda, K.; Ide, S.; Satoh, M.; Minami, M. Resolvin D1 and D2 Reverse Lipopolysaccharide-Induced Depression-Like Behaviors Through the mTORC1 Signaling Pathway. Int. J. Neuropsychopharmacol., 2017, 20(7), 575-584.
[http://dx.doi.org/10.1093/ijnp/pyx023] [PMID: 28419244]
[165]
Rey, C.; Nadjar, A.; Buaud, B.; Vaysse, C.; Aubert, A.; Pallet, V.; Layé, S.; Joffre, C. Resolvin D1 and E1 promote resolution of inflammation in microglial cells in vitro. Brain Behav. Immun., 2016, 55, 249-259.
[http://dx.doi.org/10.1016/j.bbi.2015.12.013] [PMID: 26718448]
[166]
Layé, S.; Nadjar, A.; Joffre, C.; Bazinet, R.P. Anti-inflammatory effects of omega-3 fatty acids in the brain: Physiological mechanisms and relevance to pharmacology. Pharmacol. Rev., 2018, 70(1), 12-38.
[http://dx.doi.org/10.1124/pr.117.014092] [PMID: 29217656]
[167]
Durukan, A.; Tatlisumak, T. Acute ischemic stroke: overview of major experimental rodent models, pathophysiology, and therapy of focal cerebral ischemia. Pharmacol. Biochem. Behav., 2007, 87(1), 179-197.
[http://dx.doi.org/10.1016/j.pbb.2007.04.015] [PMID: 17521716]
[168]
Markus, H. Stroke: causes and clinical features. Medicine (Baltimore), 2008, 36, 586-591.
[http://dx.doi.org/10.1016/j.mpmed.2008.08.009]
[169]
Doyle, K.P.; Simon, R.P.; Stenzel-Poore, M.P. Mechanisms of ischemic brain damage. Neuropharmacology, 2008, 55(3), 310-318.
[http://dx.doi.org/10.1016/j.neuropharm.2008.01.005] [PMID: 18308346]
[170]
Sommer, C.J. Ischemic stroke: experimental models and reality. Acta Neuropathol., 2017, 133(2), 245-261.
[http://dx.doi.org/10.1007/s00401-017-1667-0] [PMID: 28064357]
[171]
Lo, E.H.; Dalkara, T.; Moskowitz, M.A. Mechanisms, challenges and opportunities in stroke. Nat. Rev. Neurosci., 2003, 4(5), 399-415.
[http://dx.doi.org/10.1038/nrn1106] [PMID: 12728267]
[172]
Kalogeris, T.; Baines, C.P.; Krenz, M.; Korthuis, R.J. Ischemia/Reperfusion. Compr. Physiol., 2016, 7(1), 113-170.
[http://dx.doi.org/10.1002/cphy.c160006] [PMID: 28135002]
[173]
Jin, R.; Yang, G.; Li, G. Inflammatory mechanisms in ischemic stroke: role of inflammatory cells. J. Leukoc. Biol., 2010, 87(5), 779-789.
[http://dx.doi.org/10.1189/jlb.1109766] [PMID: 20130219]
[174]
Fang, M.; Zhong, L.; Jin, X.; Cui, R.; Yang, W.; Gao, S.; Lv, J.
Li, B.; Liu, T. Effect of inflammation on the process of stroke rehabilitation and poststroke depression. Front. Psychiatry, 2019, 10, 184.
[http://dx.doi.org/10.3389/fpsyt.2019.00184] [PMID: 31031649]
[175]
Ansari, J.; Kaur, G.; Gavins, F.N.E. Therapeutic potential of annexin A1 in ischemia reperfusion injury. Int. J. Mol. Sci., 2018, 19(4) E1211
[http://dx.doi.org/10.3390/ijms19041211] [PMID: 29659553]
[176]
Perretti, M. The annexin 1 receptor(s): is the plot unravelling? Trends Pharmacol. Sci., 2003, 24(11), 574-579.
[http://dx.doi.org/10.1016/j.tips.2003.09.010] [PMID: 14607080]
[177]
Gavins, F.N. Are formyl peptide receptors novel targets for therapeutic intervention in ischaemia-reperfusion injury? Trends Pharmacol. Sci., 2010, 31(6), 266-276.
[http://dx.doi.org/10.1016/j.tips.2010.04.001] [PMID: 20483490]
[178]
Solito, E.; McArthur, S.; Christian, H.; Gavins, F.; Buckingham, J.C.; Gillies, G.E. Annexin A1 in the brain--undiscovered roles? Trends Pharmacol. Sci., 2008, 29(3), 135-142.
[http://dx.doi.org/10.1016/j.tips.2007.12.003] [PMID: 18262660]
[179]
Vital, S.A.; Becker, F.; Holloway, P.M.; Russell, J.; Perretti, M.; Granger, D.N.; Gavins, F.N. Formyl-peptide receptor 2/3/lipoxin A4 receptor regulates neutrophil-platelet aggregation and attenuates cerebral inflammation: Impact for therapy in cardiovascular disease. Circulation, 2016, 133(22), 2169-2179.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.115.020633] [PMID: 27154726]
[180]
Gussenhoven, R.; Klein, L.; Ophelders, D.R.M.G.; Habets, D.H.J.; Giebel, B.; Kramer, B.W.; Schurgers, L.J.; Reutelingsperger, C.P.M.; Wolfs, T.G.A.M. Annexin A1 as neuroprotective determinant for blood-brain barrier integrity in neonatal hypoxic-ischemic encephalopathy. J. Clin. Med., 2019, 8(2) E137
[http://dx.doi.org/10.3390/jcm8020137] [PMID: 30682787]
[181]
Gavins, F.N.; Sawmynaden, P.; Chatterjee, B.E.; Perretti, M. A twist in anti-inflammation: annexin 1 acts via the lipoxin A4 receptor. Prostaglandins Leukot. Essent. Fatty Acids, 2005, 73(3-4), 211-219.
[http://dx.doi.org/10.1016/j.plefa.2005.05.008] [PMID: 15982865]
[182]
Smith, H.K.; Gil, C.D.; Oliani, S.M.; Gavins, F.N.E. Targeting formyl peptide receptor 2 reduces leukocyte-endothelial interactions in a murine model of stroke. FASEB J., 2015, 29(5), 2161-2171.
[http://dx.doi.org/10.1096/fj.14-263160] [PMID: 25690650]
[183]
Filep, J.G.; Sekheri, M.; El Kebir, D. Targeting formyl peptide receptors to facilitate the resolution of inflammation. Eur. J. Pharmacol., 2018, 833, 339-348.
[http://dx.doi.org/10.1016/j.ejphar.2018.06.025] [PMID: 29935171]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 18
ISSUE: 3
Year: 2020
Page: [229 - 249]
Pages: 21
DOI: 10.2174/1570159X17666191019170244
Price: $65

Article Metrics

PDF: 26
HTML: 2