Receptors of specialized pro-resolving mediators - a probable target of pharmacological restoration of homeostasis in allergic inflammation

Abstract

The action of most of the existing antiallergic methods and means is aimed at eliminating the cellular and molecular participants in allergic inflammation, in addition to the pro-allergic ones, performing various important homeostatic functions in the body. The few exceptions are 2. First, allergen-specific immunotherapy (ASIT), which switches the allergic response, designed to recognize low doses of an allergen entering the body in case of insufficiency of barrier tissues, to a different type of immune response, designed to recognize high doses of antigen (allergen), but without damage the participants in allergic inflammation themselves. Secondly, the replenishment of the impaired function of histohematic barriers, which also did not affect the participants in the pathogenesis of allergy, but excludes the need for the allergic response itself. In recent decades, attention has been paid to the study of the mechanisms of resolution of inflammation and its allergic form, in particular. The concept of resolution of inflammation as an active process has become recognized, in which various anti-inflammatory mediators and lipid mediators (specialized pro-resolving mediators, SPMs) specialized for resolution are involved. Violation of the mechanisms for resolving allergic inflammation leads to an aggravation of its course, transition to a chronic state, tissue remodeling and the development of secondary pathology. This justified extensive studies aimed at restoring the resolution mechanisms without affecting the morphofunctional elements important for homeostasis. A promising direction of these studies is the use of SPMs receptors as targets for effects that restore homeostatic functions. The paper considers the existing information on the types of SPMs receptors and justified ways of their targeted use for pharmacologically induced resolution of allergic inflammation. These studies will create a third, fundamentally new approach to controlling allergic inflammation without damaging the participants in maintaining homeostasis.

Keywords:allergy; allergic inflammation; homeostasis; resolution of inflammation; specialized pro-resolving mediators; receptors for specialized pro-resolving mediators; receptor pharmacology; review

For citation: Gushchin I.S. Receptors of specialized pro-resolving mediators - a probable target of pharmacological restoration of homeostasis in allergic inflammation. Immunologiya. 2021; 42 (3): 277-92. DOI: https://doi.org/10.33029/0206-4952-2021-42-3-277-292 (in Russian)

Funding. The study had no sponsor support.

Conflict of interests. The author declares no conflict of interests.

References

1. Гущин И.С. Об элементах биологической целесообразности аллергической реактивности. Патологическая физиология и экспериментальнаятабл терапия. 1979; (4): 3–11. [Gushchin I.S. On the elements of biological expediency of allergic reactivity. Patologicheskaya fiziologiya i eksperimental’naya terapiya. 1979; (4): 3–11. (in Russian)]

2. Гущин И.С. Аллергияпоздний продукт эволюции иммунной системы. Иммунология. 2019, 40 (2): 43–57. DOI: https://doi.org/10.24411/0206-4952-2019-12007 [Gushchin I.S. Allergy – late product of the immune system evolution. Immunologiya. 2019; 40 (2): 43–57. DOI: https://doi.org/10.24411/0206-4952-2019-12007 (in Russian)]

3. Pritchard D.I., Falcone F.H., Mitchell P.D. The evolution of IgE-mediated type I hypersensitivity and its immunological value. Allergy. 2021; 76 (4): 1024–40. DOI: https://doi.org/10.1111/all.14570

4. Гущин И.С. Эпидермальный барьер и аллергия. Российский аллергологический журнал. 2007; 4 (2): 3–16. [Gushchin I.S. Epidermal barrier and allergy. Rossiyskiy allergologicheskiy zhurnal. 2007; 4 (2): 3–16. (in Russian)]

5. Гущин И.С. IgE-опосредованная гиперчувствительность как ответ на нарушение барьерной функции тканей. Иммунология. 2015; 36 (1): 45–52. [Gushchin I.S. IgE-mediated hypersensitivity as a response to the barrier tissue disfunction. Immunologiya. 2015; 36 (1): 45–52. (in Russian)]

6. Гущин И.С. Самоограничение и разрешение аллергического процесса. Иммунология. 2020; 41 (6): 557–80. DOI: DOI: https://doi.org/10.33029/0206-4952-2020-41-6-557-580 [Gushchin I.S. Autorestriction and resolution of allergic process. Immunologiya. 2019; 41 (6): 557–80. DOI: DOI: https://doi.org/10.33029/0206-4952-2020-41-6-557-580 (in Russian)]

7. Samuelsson B., Dahlén S.E., Lindgren J.A., Rouzer C.A., Serhan C.N. Leukotrienes and lipoxins: structures, biosynthesis, and biological effects. Science. 1987; 237 (4819): 1171–6. DOI: https://doi.org/10.1126/science.2820055

8. Serhan C.N., Hamberg M., Samuelsson B. Lipoxins: novel series of biologically active compounds formed from arachidonic acid in human leukocytes. Proc. Natl Acad. Sci. USA. 1984; 81 (17): 5335–9. DOI: https://doi.org/10.1073/pnas.81.17.5335

9. Serhan C.N., Hamberg M., Samuelsson B. Trihydroxytetraenes: a novel series of compounds formed from arachidonic acid in human leukocytes. Biochem. Biophys. Res. Commun. 1984; 118 (3): 943–9. DOI: https://doi.org/10.1016/0006-291x(84)91486-4

10. Serhan C.N., Chiang N., Dalli J., Levy B.D. Lipid mediators in the resolution of inflammation. Cold Spring Harb. Perspect. Biol. 2014; 7 (2): a016311. DOI: https://doi.org/10.1101/cshperspect.a016311

11. Serhan C.N., Brain S.D., Buckley C.D., et al. Resolution of inflammation: state of the art, definitions and terms. FASEB J. 2007; 21 (2): 325–32. DOI: https://doi.org/10.1096/fj.06-7227rev

12. Serhan C.N. Pro-resolving lipid mediators are leads for resolution physiology. Nature. 2014; 510 (7503): 92–101. DOI: https://doi.org/10.1038/nature13479

13. Krishnamoorthy N., Abdulnour R.E., Walker K.H., Engstrom B.D., Levy B.D. Specialized proresolving mediators in innate and adaptive immune responses in airway diseases. Physiol. Rev. 2018; 98 (3): 1335–70. DOI: https://doi.org/10.1152/physrev.00026.2017

14. Chiang N., Serhan C.N. Specialized pro-resolving mediator network: an update on production and actions. Essays Biochem. 2020; 64 (3): 443–62. DOI: https://doi.org/10.1042/EBC20200018

15. Chiang N., Serhan C.N. Structural elucidation and physiologic functions of specialized pro-resolving mediators and their receptors. Mol. Aspects Med. 2017; 58: 114–29. DOI: https://doi.org/10.1016/j.mam.2017.03.005

16. Barnig C., Frossard N., Levy B.D. Towards targeting resolution pathways of airway inflammation in asthma. Pharmacol. Ther. 2018; 186: 98–113. DOI: https://doi.org/10.1016/j.pharmthera.2018.01.004

17. Barnig C., Bezema T., Calder P.C., Charloux A., Frossard N., Garssen J., Haworth O., Dilevskaya K., Levi-Schaffer F., Lonsdorfer E., Wauben M., Kraneveld A.D., Te Velde A.A. Activation of resolution pathways to prevent and fight chronic inflammation: lessons from asthma and inflammatory bowel disease. Front. Immunol. 2019; 10: 1699. DOI: https://doi.org/10.3389/fimmu.2019.01699

18. Park J., Langmead C.J., Riddy D.M. New advances in targeting the resolution of inflammation: implications for specialized pro-resolving mediator GPCR drug discovery. ACS Pharmacol. Transl. Sci. 2020; 3 (1): 88–106. DOI: https://doi.org/10.1021/acsptsci.9b00075

19. Lee C.H. Role of specialized pro-resolving lipid mediators and their receptors in virus infection: a promising therapeutic strategy for SARS-CoV-2 cytokine storm. Arch. Pharm. Res. 2021; Jan 4: 1–15. DOI: https://doi.org/10.1007/s12272-020-01299-y

20. Serhan C.N., Levy B.D. Resolvins in inflammation: emergence of the pro-resolving superfamily of mediators. J. Clin. Invest. 2018; 128 (7): 2657–69. DOI: https://doi.org/10.1172/JCI97943

21. Fullerton J.N., Gilroy D.W. Resolution of inflammation: a new therapeutic frontier. Nat. Rev. Drug Discov. 2016; 15 (8): 551–67. DOI: https://doi.org/10.1038/nrd.2016.39

22. Patel S.V., Khan D.A. Adverse reactions to biologic therapy. Immunol. Allergy Clin. North Am. 2017; 37 (2): 397–412. DOI: https://doi.org/10.1016/j.iac.2017.01.012

23. Fokkens W.J., Lund V., Bachert C., Mullol J., Bjermer L., Bousquet J., Canonica G.W., Deneyer L., Desrosiers M., Diamant Z., Han J., Heffler E., Hopkins C., Jankowski R., Joos G., Knill A., Lee J., Lee S.E., Mariën G., Pugin B., Senior B., Seys S.F., Hellings P.W. EUFOREA consensus on biologics for CRSwNP with or without asthma. Allergy. 2019; 74 (12): 2312–9. DOI: https://doi.org/10.1111/all.13875

24. McGregor M.C., Krings J.G., Nair P., Castro M. Role of Biologics in Asthma. Am. J. Respir. Cri. Care Med. 2019; 199 (4): 433–45. DOI: https://doi.org/10.1164/rccm.201810-1944CI

25. Just J., Deschildre A., Lejeune S., Amat F. New perspectives of childhood asthma treatment with biologics. Pediatr. Allergy Immunol. 2019; 30 (2): 159–71. DOI: https://doi.org/10.1111/pai.13007

26. Jung Y., Rothenberg M.E. Roles and regulation of gastrointestinal eosinophils in immunity and disease. J. Immunol. 2014; 193 (3): 999–1005. DOI: https://doi.org/10.4049/jimmunol.1400413

27. Simon H.U., Yousefi S., Germic N., et al. The cellular functions of eosinophils: Collegium Internationale Allergologicum (CIA) Update 2020. Int. Arch. Allergy Immunol. 2020; 181 (1): 11–23. DOI: https://doi.org/10.1159/000504847

28. Van der Stede T., Blancquaert L., Stassen F., Everaert I., Van Thienen R., Vervaet C., Gliemann L., Hellsten Y., Derave W. Histamine H1 and H2 receptors are essential transducers of the integrative exercise training response in humans. Sci. Adv. 2021; 7 (16): eabf2856. DOI: https://doi.org/10.1126/sciadv.abf2856 PMID: 33853781

29. Christopoulos A., Kenakin T. G protein-coupled receptor allosterism and complexing. Pharmacol. Rev. 2002; 54 (2): 323–74. DOI: https://doi.org/10.1124/pr.54.2.323

30. Бахтюков А.А., Шпаков А.О. Низкомолекулярные аллостерические регуляторы G-белок-сопряженных рецепторов полипептидных гормонов. Российский физиологический журнал имени И.М. Сеченова. 2019; 105 (3): 269–83. DOI: https://doi.org/10.1134/S0869813919030014 [Bakhtyukov A.A., Shpakov A.O. The low-molecular-weight allosteric regulators of g-proteincoupled receptors of the polypeptide hormones. Rossiyskiy fiziologicheskiy zhurnal imeni I.M. Sechenova. 2019; 105 (3): 269–83. DOI: https://doi.org/10.1134/S0869813919030014 (in Russian)]

31. Grover A.K. Use of allosteric targets in the discovery of safer drugs. Med. Princ. Pract. 2013; 22 (5): 418–26. DOI: https://doi.org/10.1159/000350417

32. Christopoulos A. Allosteric binding sites on cell-surface receptors: novel targets for drug discovery. Nat. Rev. Drug Discov. 2002; 1 (3): 198–210. DOI: https://doi.org/10.1038/nrd746

33. Conibear A.E., Kelly E. A biased view of μ-opioid receptors? Mol. Pharmacol. 2019; 96 (5): 542–9. DOI: https://doi.org/10.1124/mol.119.115956

34. Violin J.D., Crombie A.L., Soergel D.G., Lark M.W. Biased ligands at G-protein-coupled receptors: promise and progress. Trends Pharmacol. Sci. 2014; 35 (7): 308–16. DOI: https://doi.org/10.1016/j.tips.2014.04.007

35. Kenakin T. The effective application of biased signaling to new drug discovery. Mol. Pharmacol. 2015; 88 (6): 1055–61. DOI: https://doi.org/10.1124/mol.115.099770

36. Smith J.S., Lefkowitz R.J., Rajagopal S. Biased signalling: from simple switches to allosteric microprocessors. Nat. Rev. Drug Discov. 2018; 17 (4): 243–60. DOI: https://doi.org/10.1038/nrd.2017.229

37. Brink C., Dahlén S.E., Drazen J., Evans J.F., Hay D.W., Nicosia S., Serhan C.N., Shimizu T., Yokomizo T.; International Union of Pharmacology XXXVII. Nomenclature for leukotriene and lipoxin receptors. Pharmacol. Rev. 2003; 55 (1): 195–227. DOI: https://doi.org/10.1124/pr.55.1.8

38. Maderna P., Cottell D.C., Toivonen T., Dufton N., Dalli J., Perretti M., Godson C. FPR2/ALX receptor expression and internalization are critical for lipoxin A4 and annexin-derived peptide-stimulated phagocytosis. FASEB J. 2010; 24 (11): 4240–9. DOI: https://doi.org/10.1096/fj.10-159913

39. Barnig C., Cernadas M., Dutile S., Liu X., Perrella M.A., Kazani S., Wechsler M.E., Israel E., Levy B.D. Lipoxin A4 regulates natural killer cell and type 2 innate lymphoid cell activation in asthma. Sci. Transl. Med. 2013; 5 (174): 174ra26. DOI: https://doi.org/10.1126/scitranslmed.3004812

40. Chen K., Bao Z., Gong W., Tang P., Yoshimura T., Wang J.M. Regulation of inflammation by members of the formyl-peptide receptor family. J Autoimmun. 2017; 85: 64–77. DOI: https://doi.org/10.1016/j.jaut.2017.06.012

41. Devosse T., Guillabert A., D’Haene N., Berton A., De Nadai P., Noel S., Brait M., Franssen J.D., Sozzani S., Salmon I., Parmentier M. Formyl peptide receptor-like 2 is expressed and functional in plasmacytoid dendritic cells, tissue-specific macrophage subpopulations, and eosinophils. J. Immunol. 2009; 182 (8): 4974–84. DOI: https://doi.org/10.4049/jimmunol.0803128

42. 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): 16 168–76. PMID: 1322894.

43. Kim S.D., Kim J.M., Jo S.H., Lee H.Y., Lee S.Y., Shim J.W., Seo S.K., Yun J., Bae Y.S. Functional expression of formyl peptide receptor family in human NK cells. J. Immunol. 2009; 183 (9): 5511–7. DOI: https://doi.org/10.4049/jimmunol.0802986

44. Bonnans C., Fukunaga K., Levy M.A., Levy B.D. Lipoxin A(4) regulates bronchial epithelial cell responses to acid injury. Am. J. Pathol. 2006; 168 (4): 1064–72. DOI: https://doi.org/10.2353/ajpath.2006.051056

45. Ho C.F., Ismail N.B., Koh J.K., Gunaseelan S., Low Y.H., Ng Y.K., Chua J.J., Ong W.Y. Localisation of formyl-peptide receptor 2 in the rat central nervous system and its role in axonal and dendritic outgrowth. Neurochem. Res. 2018; 43 (8): 1587–98. DOI: https://doi.org/10.1007/s11064-018-2573-0

46. 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): 1970–8. DOI: https://doi.org/10.1161/ATVBAHA.112.249508

47. Chiang N., Takano T., Arita M., Watanabe S., Serhan C.N. A novel rat lipoxin A4 receptor that is conserved in structure and function. Br. J. Pharmacol. 2003; 139 (1): 89–98. DOI: https://doi.org/10.1038/sj.bjp.0705220

48. 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): 1693–704. DOI: https://doi.org/10.1084/jem.185.9.1693

49. 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): 18 232–7. DOI: https://doi.org/10.1073/pnas.1308253110

50. Filep J.G. Biasing the lipoxin A4/formyl peptide receptor 2 pushes inflammatory resolution. Proc. Natl Acad. Sci. USA. 2013; 110 (45): 18 033–4. DOI: https://doi.org/10.1073/pnas.1317798110

51. 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): 1660–5. DOI: https://doi.org/10.1073/pnas.0907342107

52. Lee H.N., Surh Y.J. Resolvin D1-mediated NOX2 inactivation rescues macrophages undertaking efferocytosis from oxidative stress-induced apoptosis. Biochem. Pharmacol. 2013; 86 (6): 759–69. DOI: https://doi.org/10.1016/j.bcp.2013.07.002

53. 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): 2018–27. DOI: https://doi.org/10.1016/j.ajpath.2012.01.028

54. Li Y., Dalli J., Chiang N., Baron R.M., Quintana C., Serhan C.N. Plasticity of leukocytic exudates in resolving acute inflammation is regulated by MicroRNA and proresolving mediators. Immunity. 2013; 39 (5): 885–98. DOI: https://doi.org/10.1016/j.immuni.2013.10.011

55. 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): 1970–8. DOI: https://doi.org/10.1161/ATVBAHA.112.249508

56. Alexander S.P., Christopoulos A., Davenport A.P., Kelly E., Marrion N.V., Peters J.A., Faccenda E., Harding S.D., Pawson A.J., Sharman J.L., Southan C., Davies J.A.; CGTP Collaborators. The concise guide to pharmacology 2017/18: G protein-coupled receptors. Br. J. Pharmacol. 2017; 174 (suppl 1): S17–129. DOI: https://doi.org/10.1111/bph.13878

57. 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): 24 690–7. DOI: https://doi.org/10.1074/jbc.M112.377101

58. Filep J.G., Sekheri M., El Kebir D. Targeting formyl peptide receptors to facilitate the resolution of inflammation. Eur. J. Pharmacol. 2018; 833: 339–48. DOI: https://doi.org/10.1016/j.ejphar.2018.06.025

59. 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): 1197–208. DOI: DOI: https://doi.org/10.1084/jem.191.7.1197

60. 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): 113–30. DOI: https://doi.org/10.1161/CIRCRESAHA.116.307308

61. 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): 1970–8. DOI: https://doi.org/10.1161/ATVBAHA.112.249508

62. 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): 3429–37. DOI: https://doi.org/10.4049/jimmunol.1501701

63. Dalli J., Winkler J.W., Colas R.A., Arnardottir H., Cheng C.Y., Chiang N., Petasis N.A., Serhan C.N. Resolvin D3 and aspirin-triggered resolvin D3 are potent immunoresolvents. Chem. Biol. 2013; 20 (2): 188–201. DOI: DOI: https://doi.org/10.1016/j.chembiol.2012.11.010

64. 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): 524–8. DOI: https://doi.org/10.1038/nature11042

65. 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): 1970–8. DOI: https://doi.org/10.1161/ATVBAHA.112.249508

66. Chiang N., Barnaeva E., Hu X., Marugan J., Southall N., Ferrer M., Serhan C.N. Identification of chemotype agonists for human resolvin D1 receptor DRV1 with pro-resolving functions. Cell Chem. Biol. 2019; 26 (2): 244–54.e4. DOI: https://doi.org/10.1016/j.chembiol.2018.10.023

67. Chiang N., de la Rosa X., Libreros S., Serhan C.N. Novel resolvin D2 receptor axis in infectious inflammation. J. Immunol. 2017; 198 (2): 842–51. DOI: https://doi.org/10.4049/jimmunol.1601650

68. 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): 827–32. DOI: https://doi.org/10.1016/j.bbrc.2006.06.175

69. Offertáler L., Mo F.M., Bátkai S., Liu J., Begg M., Razdan R.K., Martin B.R., Bukoski R.D., Kunos G. Selective ligands and cellular effectors of a G protein-coupled endothelial cannabinoid receptor. Mol. Pharmacol. 2003; 63 (3): 699–705. DOI: https://doi.org/10.1124/mol.63.3.699

70. McHugh D. GPR18 in microglia: implications for the CNS and endocannabinoid system signalling. Br. J. Pharmacol. 2012; 167 (8): 1575–82. DOI: https://doi.org/10.1111/j.1476-5381.2012.02019.x

71. Wang X., Sumida H., Cyster J.G. GPR18 is required for a normal CD8αα intestinal intraepithelial lymphocyte compartment. J. Exp. Med. 2014; 211 (12): 2351–9. DOI: https://doi.org/10.1084/jem.20140646 Epub 2014 Oct 27.

72. Zhang L., Qiu C., Yang L., Zhang Z., Zhang Q., Wang B., Wang X. GPR18 expression on PMNs as biomarker for outcome in patient with sepsis. Life Sci. 2019; 217: 49–56. DOI: https://doi.org/10.1016/j.lfs.2018.11.061

73. Pirault J., Bäck M. Lipoxin and resolvin receptors transducing the resolution of inflammation in cardiovascular disease. Front. Pharmacol. 2018; 9: 1273. DOI: https://doi.org/10.3389/fphar.2018.01273

74. Jablonski K.A., Amici S.A., Webb L.M., Ruiz-Rosado J. de D., Popovich P.G., Partida-Sanchez S., Guerau-de-Arellano M. Novel markers to delineate murine M1 and M2 macrophages. PLoS One. 2015; 10 (12): e0145342. DOI: https://doi.org/10.1371/journal.pone.0145342

75. Liu Y., Wang L., Lo K.W., Lui V.W.Y. Omics-wide quantitative B-cell infiltration analyses identify GPR18 for human cancer prognosis with superiority over CD20. Commun. Biol. 2020; 3 (1): 234. DOI: https://doi.org/10.1038/s42003-020-0964-7

76. Davenport A.P., Alexander S.P., Sharman J.L., Pawson A.J., Benson H.E., Monaghan A.E., Liew W.C., Mpamhanga C.P., Bonner T.I., Neubig R.R., Pin J.P., Spedding M., Harmar A.J. International Union of Basic and Clinical Pharmacology. LXXXVIII. G protein-coupled receptor list: recommendations for new pairings with cognate ligands. Pharmacol. Rev. 2013; 65 (3): 967-86. DOI: https://doi.org/10.1124/pr.112.007179

77. Alexander S.P.H., Christopoulos A., Davenport A.P., Kelly E., Mathie A., Peters J.A., Veale E.L., Armstrong J.F., Faccenda E., Harding S.D., Pawson A.J., Sharman J.L., Southan C., Davies J.A.; CGTP Collaborators. The concise guide to pharmacology 2019/20: G protein-coupled receptors. Br. J. Pharmacol. 2019; 176 (suppl 1): S21-141. DOI: https://doi.org/10.1111/bph.14748

78. Luangsay S., Wittamer V., Bondue B., De Henau O., Rouger L., Brait M., Franssen J.D., de Nadai P., Huaux F., Parmentier M. Mouse ChemR23 is expressed in dendritic cell subsets and macrophages, and mediates an anti-inflammatory activity of chemerin in a lung disease model. J. Immunol. 2009; 183 (10): 6489-99. DOI: https://doi.org/10.4049/jimmunol.0901037

79. Meder W., Wendland M., Busmann A., Kutzleb C., Spodsberg N., John H., Richter R., Schleuder D., Meyer M., Forssmann W.G. Characterization of human circulating TIG2 as a ligand for the orphan receptor ChemR23. FEBS Lett. 2003; 555 (3): 495-9. DOI: https://doi.org/10.1016/s0014-5793(03)01312-7

80. 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): 713-22. DOI: https://doi.org/10.1084/jem.20042031

81. Arita M., Ohira T., Sun Y.P., Elangovan S., Chiang N., Serhan C.N. Resolvin E1 selectively interacts with leukotriene B4 receptor BLT1 and ChemR23 to regulate inflammation. J. Immunol. 2007; 178 (6): 3912-7. DOI: https://doi.org/10.4049/jimmunol.178.6.3912

82. Wittamer V., Grégoire F., Robberecht P., Vassart G., Communi D., Parmentier M. The C-terminal nonapeptide of mature chemerin activates the chemerin receptor with low nanomolar potency. J. Biol. Chem. 2004; 279 (11): 9956-62. DOI: DOI: https://doi.org/10.1074/jbc.M313016200

83. 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): 349-61. DOI: https://doi.org/10.1038/nri2294

84. Herrera B.S., Hasturk H., Kantarci A., Freire M.O., Nguyen O., Kansal S., Van Dyke T.E. Impact of resolvin E1 on murine neutrophil phagocytosis in type 2 diabetes. Infect. Immun. 2015; 83 (2): 792-801. DOI: https://doi.org/10.1128/IAI.02444-14

85. Oh S.F., Pillai P.S., Recchiuti A., Yang R., Serhan C.N. Pro-resolving actions and stereoselective biosynthesis of 18S E-series resolvins in human leukocytes and murine inflammation. J. Clin. Invest. 2011; 121 (2): 569-81. DOI: https://doi.org/10.1172/JCI42545

86. Saeki K., Yokomizo T. Identification, signaling, and functions of LTB4 receptors. Semin. Immunol. 2017; 33: 30-6. DOI: https://doi.org/10.1016/j.smim.2017.07.010

87. Yokomizo T. Two distinct leukotriene B4 receptors, BLT1 and BLT2. J. Biochem. 2015; 157 (2): 65-71. DOI: https://doi.org/10.1093/jb/mvu078

88. Haworth O., Cernadas M., Yang R., Serhan C.N., Levy B.D. Resolvin E1 regulates interleukin 23, interferon-gamma and lipoxin A4 to promote the resolution of allergic airway inflammation. Nat. Immunol. 2008; 9 (8): 873-9. DOI: DOI: https://doi.org/10.1038/ni.1627

89. Oh S.F., Dona M., Fredman G., Krishnamoorthy S., Irimia D., Serhan C.N. Resolvin E2 formation and impact in inflammation resolution. J. Immunol. 2012; 188 (9): 4527-34. DOI: https://doi.org/10.4049/jimmunol.1103652

90. Unno Y., Sato Y., Fukuda H., Ishimura K., Ikeda H., Watanabe M., Tansho-Nagakawa S., Ubagai T., Shuto S., Ono Y. Resolvin E1, but not resolvins E2 and E3, promotes fMLF-induced ROS generation in human neutrophils. FEBS Lett. 2018; 592 (16): 2706-15. DOI: https://doi.org/10.1002/1873-3468.13215

91. Zhu M., Cortese G.P., Waites C.L. Parkinson's disease-linked Parkin mutations impair glutamatergic signaling in hippocampal neurons. BMC Biol. 2018; 16 (1): 100. DOI: https://doi.org/10.1186/s12915-018-0567-7

92. Smith N.J. Drug discovery opportunities at the endothelin B receptor-related orphan G protein-coupled receptors, GPR37 and GPR37L1. Front. Pharmacol. 2015; 6: 275. DOI: https://doi.org/10.3389/fphar.2015.00275

93. Yang H.J., Vainshtein A., Maik-Rachline G., Peles E. G protein-coupled receptor 37 is a negative regulator of oligodendrocyte differentiation and myelination. Nat. Commun. 2016; 7: 10884. DOI: https://doi.org/10.1038/ncomms10884

94. Marazziti D., Mandillo S., Di Pietro C., Golini E., Matteoni R., Tocchini-Valentini G.P. GPR37 associates with the dopamine transporter to modulate dopamine uptake and behavioral responses to dopaminergic drugs. Proc. Natl Acad. Sci. USA. 2007; 104 (23): 9846-51. DOI: https://doi.org/10.1073/pnas.0703368104

95. Fujita-Jimbo E., Yu Z.L., Li H., Yamagata T., Mori M., Momoi T., Momoi M.Y. Mutation in Parkinson disease-associated, G-protein-coupled receptor 37 (GPR37/PaelR) is related to autism spectrum disorder. PLoS One. 2012; 7 (12): e51155. DOI: https://doi.org/10.1371/journal.pone.0051155

96. Bang S., Xie Y.K., Zhang Z.J., Wang Z., Xu Z.Z., Ji R.R. GPR37 regulates macrophage phagocytosis and resolution of inflammatory pain. J. Clin. Invest. 2018; 128 (8): 3568-82. DOI: https://doi.org/10.1172/JCI99888

97. McCrary M.R., Jiang M.Q., Giddens M.M., Zhang J.Y., Owino S., Wei Z.Z., Zhong W., Gu X., Xin H., Hall R.A., Wei L., Yu S.P. Protective effects of GPR37 via regulation of inflammation and multiple cell death pathways after ischemic stroke in mice. FASEB J. 2019; 33 (10): 10 680-91. DOI: https://doi.org/10.1096/fj.201900070R

98. Snippert H.J., Haegebarth A., Kasper M., Jaks V., van Es J.H., Barker N., van de Wetering M., van den Born M., Begthel H., Vries R.G., Stange D.E., Toftgard R., Clevers H. Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science. 2010; 327 (5971): 1385-9. DOI: https://doi.org/10.1126/science.1184733

99. Chiang N., Libreros S., Norris P.C., de la Rosa X., Serhan C.N. Maresin 1 activates LGR6 receptor promoting phagocyte immunoresolvent functions. J. Clin. Invest. 2019; 129 (12): 5294-311. DOI: https://doi.org/10.1172/JCI129448

100. Flak M.B., Koenis D.S., Sobrino A., Smith J., Pistorius K., Palmas F., Dalli J. GPR101 mediates the pro-resolving actions of RvD5n-3 DPA in arthritis and infections. J. Clin. Invest. 2020; 130 (1): 359-73. DOI: https://doi.org/10.1172/JCI131609

101. Балан Г.М., Бубало Н.Н., Лепешкин И.В., Бубало В.А. Ядерные рецепторы - ключевые регуляторы биотрансформации ксенобиотиков. Часть 2. Ядерные ксено- и гормональные рецепторы: структура, номенклатура и роль в метаболизме и гомеостазе. Украинский журнал современных проблем токсикологии. 2016; 1: 24-42. [Balan G., Bubalo N., Lepeshkin I., Bubalo V. The nuclear receptors - a key regulator of biotransformation of xenobiotics. Part 2. The nuclear xeno- and hormonal receptors: structure, nomenclature and role in the metabolism and homeostasis. Ukrainskiy shurnal sovremennykh problem toksikologii. 2016; 1: 24-42 (in Russian)]

102. Zhao Y., Calon F., Julien C., Winkler J.W., Petasis N.A., Lukiw W.J., Bazan N.G. Docosahexaenoic acid-derived neuroprotectin D1 induces neuronal survival via secretase- and PPARγ-mediated mechanisms in Alzheimer’s disease models. PLoS One. 2011; 6 (1): e15816. DOI: https://doi.org/10.1371/journal.pone.0015816

103. Liao Z., Dong J., Wu W., Yang T., Wang T., Guo L., Chen L., Xu D., Wen F. Resolvin D1 attenuates inflammation in lipopolysaccharide-induced acute lung injury through a process involving the PPARγ/NF-κB pathway. Respir. Res. 2012; 13 (1): 110. DOI: https://doi.org/10.1186/1465-9921-13-110

104. Asha K., Balfe N., Sharma-Walia N. Concurrent control of the kaposi's sarcoma-associated herpesvirus life cycle through chromatin modulation and host hedgehog signaling: a new prospect for the therapeutic potential of lipoxin A4. J. Virol. 2020; 94 (9): e02177-19. DOI: https://doi.org/10.1128/JVI.02177-19.

105. Ghaedi M., Shen Z.Y., Orangi M., Martinez-Gonzalez I., Wei L., Lu X., Das A., Heravi-Moussavi A., Marra M.A., Bhandoola A., Takei F. Single-cell analysis of RORα tracer mouse lung reveals ILC progenitors and effector ILC2 subsets. J. Exp. Med. 2020; 217 (3): jem.20182293. DOI: https://doi.org/10.1084/jem.20182293

106. Dalli J., Chiang N., Serhan C.N. Elucidation of novel 13-series resolvins that increase with atorvastatin and clear infections. Nat. Med. 2015; 21 (9): 1071-5. DOI: https://doi.org/10.1038/nm.3911

107. Rodriguez A.R., Spur B.W. First total syntheses of the pro-resolving lipid mediators 7(S),13(R),20(S)-Resolvin T1 and 7(S),13(R)-Resolvin T4. Tetrahedron Lett. 2020; 61 (6): 151473. DOI: https://doi.org/10.1016/j.tetlet.2019.151473

108. Rodriguez A.R., Spur B.W. First total synthesis of the pro-resolving lipid mediator 7(S),12(R),13(S)-Resolvin T2 and its 13(R)-epimer. Tetrahedron Lett. 2020; 61 (20): 151857. DOI: https://doi.org/10.1016/j.tetlet.2020.151857

109. Körner A., Zhou E., Müller C., Mohammed Y., Herceg S., Bracher F., Rensen P.C.N., Wang Y., Mirakaj V., Giera M. Inhibition of Δ24-dehydrocholesterol reductase activates pro-resolving lipid mediator biosynthesis and inflammation resolution. Proc. Natl Acad. Sci. USA. 2019; 116 (41): 20 623-34. DOI: https://doi.org/10.1073/pnas.1911992116

110. Wootten D., Christopoulos A., Sexton P.M. Emerging paradigms in GPCR allostery: implications for drug discovery. Nat. Rev. Drug Discov. 2013; 12 (8): 630-44. DOI: https://doi.org/10.1038/nrd4052

111. Corminboeuf O., Leroy X. FPR2/ALXR agonists and the resolution of inflammation. J. Med. Chem. 2015; 58 (2): 537-59. DOI: https://doi.org/10.1021/jm501051x

112. 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): 1478-504. DOI: https://doi.org/10.2174/0929867321666131218095521

113. Sun Y.P., Tjonahen E., Keledjian R., Zhu M., Yang R., Recchiuti A., Pillai P.S., Petasis N.A., Serhan C.N. Anti-inflammatory and pro-resolving properties of benzo-lipoxin A(4) analogs. Prostaglandins Leukot. Essent Fatty Acids. 2009; 81 (5-6): 357-66. DOI: https://doi.org/10.1016/j.plefa.2009.09.004

114. Wu S.H., Chen X.Q., Liu B., Wu H.J., Dong L. Efficacy and safety of 15(R/S)-methyl-lipoxin A(4) in topical treatment of infantile eczema. Br. J. Dermatol. 2013; 168 (1): 172-8. DOI: https://doi.org/10.1111/j.1365-2133.2012.11177.x

115. Kong X., Wu S.H., Zhang L., Chen X.Q. Pilot application of lipoxin A4 analog and lipoxin A4 receptor agonist in asthmatic children with acute episodes. Exp. Ther. Med. 2017; 14 (3): 2284-90. DOI: https://doi.org/10.3892/etm.2017.4787

116. Stalder A.K., Lott D., Strasser D.S., Cruz H.G., Krause A., Groenen P.M., 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): 476-86. DOI: https://doi.org/10.1111/bcp.13149

117. Ferguson S.S., Downey W.E. 3rd, Colapietro A.M., Barak L.S., Ménard L., Caron M.G. Role of beta-arrestin in mediating agonist-promoted G protein-coupled receptor internalization. Science. 1996; 271 (5247): 363-6. DOI: https://doi.org/10.1126/science.271.5247.363

118. Lind S., Sundqvist M., Holmdahl R., Dahlgren C., Forsman H., Olofsson P. Functional and signaling characterization of the neutrophil FPR2 selective agonist Act-389949. Biochem. Pharmacol. 2019; 166: 163-73. DOI: https://doi.org/10.1016/j.bcp.2019.04.030

119. 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): L904-11. DOI: https://doi.org/10.1152/ajplung.00370.2014

120. Cortina M.S., Bazan H.E. Docosahexaenoic acid, protectins and dry eye. Curr. Opin. Clin. Nutr. Metab. Care. 2011; 14 (2): 132-7. DOI: https://doi.org/10.1097/MCO.0b013e328342bb1a

121. Chistyakov D.V., Astakhova A.A., Goriainov S.V., Sergeeva M.G. Comparison of PPAR ligands as modulators of resolution of inflammation, via their influence on cytokines and oxylipins release in astrocytes. Int. J. Mol. Sci. 2020; 21 (24): 9577. DOI: https://doi.org/10.3390/ijms21249577

122. Perretti M., Godson C. Formyl peptide receptor type 2 agonists to kick-start resolution pharmacology. Br. J. Pharmacol. 2020; 177 (20): 4595-600. DOI: https://doi.org/10.1111/bph.15212

123. Kenakin T., Miller L.J. Seven transmembrane receptors as shapeshifting proteins: the impact of allosteric modulation and functional selectivity on new drug discovery. Pharmacol. Rev. 2010; 62 (2): 265-304. DOI: https://doi.org/10.1124/pr.108.000992

124. Kenakin T. Functional selectivity and biased receptor signaling. J. Pharmacol. Exp. Ther. 2011; 336 (2): 296-302. DOI: https://doi.org/10.1124/jpet.110.173948

125. Суплатов Д.А., Швядас В.К. Изучение функциональных и аллостерических сайтов в суперсемействах белков. Acta Naturae. 2015; 7 (4): 39-52. [Suplatov D.A., Shvyadas V.K. Study of functional and allosteric sites in protein superfamilies. Acta Naturae. 2015; 7 (4): 39-52. (in Russian)]

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