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Resolvins: Emerging Players in Autoimmune and Inflammatory Diseases

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Abstract

Resolvins, belonging to the group of specialized proresolving mediators (SPMs), are metabolic products of omega-3 polyunsaturated fatty acids (ω-3 PUFAs) and are synthesized during the initial phases of acute inflammatory responses to promote the resolution of inflammation. Resolvins are produced for termination of neutrophil infiltration, stimulation of the clearance of apoptotic cells by macrophages, and promotion of tissue remodeling and homeostasis. Metabolic dysregulation due to either uncontrolled activity of pro-inflammatory responses or to inefficient resolution of inflammation results in chronic inflammation and may also lead to atherosclerosis or other chronic autoimmune diseases such as rheumatoid arthritis, psoriasis, systemic lupus erythematosus, vasculitis, inflammatory bowel diseases, and type 1 diabetes mellitus. The pathogenesis of such diseases involves a complex interplay between the immune system and, environmental factors (non-infectious or infectious), and critically depends on individual susceptibility to such factors. In the present review, resolvins and their roles in the resolution of inflammation, as well as the role of these mediators as potential therapeutic agents to counteract specific chronic autoimmune and inflammatory diseases are discussed.

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References

  1. Kumar V, Abbas AK, Fausto N, Aster JC (2014) Robbins and Cotran pathologic basis of disease, professional edition e-book. elsevier health sciences

  2. Libby P, Ridker PM, Maseri A (2002) Inflammation and atherosclerosis. Circulation 105(9):1135–1143

    CAS  PubMed  Google Scholar 

  3. Hansson GK, Libby P (2006) The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol 6(7):508–519

    CAS  PubMed  Google Scholar 

  4. Serhan CN, Petasis NA (2011) Resolvins and protectins in inflammation resolution. Chem Rev 111(10):5922–5943. https://doi.org/10.1021/cr100396c

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Majno G, Joris I (2004) Cells, tissues, and disease: principles of general pathology. Oxford University Press

  6. Serhan CN, Brain SD, Buckley CD, Gilroy DW, Haslett C, O’Neill LA, Perretti M, Rossi AG, Wallace JL (2007) Resolution of inflammation: state of the art, definitions and terms. FASEB J 21(2):325–332

    CAS  PubMed  Google Scholar 

  7. Serhan CN (2004) A search for endogenous mechanisms of anti-inflammation uncovers novel chemical mediators: missing links to resolution. Histochem Cell Biol 122(4):305–321

    CAS  PubMed  Google Scholar 

  8. Serhan CN, Ward PA, Gilroy DW (2010) Fundamentals of inflammation. Cambridge University Press

  9. Schwab JM, Serhan CN (2006) Lipoxins and new lipid mediators in the resolution of inflammation. Curr Opin Pharmacol 6(4):414–420

    CAS  PubMed  Google Scholar 

  10. Crean D, Godson C (2015) Specialised lipid mediators and their targets. In: Seminars in immunology, vol 3. Elsevier, pp 169–176

  11. Samuelsson B, Dahlen S-E, Lindgren JA, Rouzer CA, Serhan CN (1987) Leukotrienes and lipoxins: structures, biosynthesis, and biological effects. Science 237(4819):1171–1176

    CAS  PubMed  Google Scholar 

  12. Manfredi AA, Ramirez GA, Rovere-Querini P, Maugeri N (2018) The neutrophil’s choice: phagocytose vs make neutrophil extracellular traps. Front Immunol 9:288

    PubMed  PubMed Central  Google Scholar 

  13. Branzk N, Lubojemska A, Hardison SE, Wang Q, Gutierrez MG, Brown GD, Papayannopoulos V (2014) Neutrophils sense microbe size and selectively release neutrophil extracellular traps in response to large pathogens. Nat Immunol 15(11):1017–1025

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Warnatsch A, Tsourouktsoglou T-D, Branzk N, Wang Q, Reincke S, Herbst S, Gutierrez M, Papayannopoulos V (2017) Reactive oxygen species localization programs inflammation to clear microbes of different size. Immunity 46(3):421–432

    CAS  PubMed  PubMed Central  Google Scholar 

  15. McDonald B, Urrutia R, Yipp BG, Jenne CN, Kubes P (2012) Intravascular neutrophil extracellular traps capture bacteria from the bloodstream during sepsis. Cell Host Microbe 12(3):324–333

    CAS  PubMed  Google Scholar 

  16. Kim S-J, Jenne CN (2016) Role of platelets in neutrophil extracellular trap (NET) production and tissue injury. In: Seminars in immunology, vol 6. Elsevier, pp 546–554

  17. Chiurchiù V, Leuti A, Dalli J, Jacobsson A, Battistini L, Maccarrone M, Serhan CN (2016) Proresolving lipid mediators resolvin D1, resolvin D2, and maresin 1 are critical in modulating T cell responses. Sci Transl Med 8(353):353ra111

    PubMed  PubMed Central  Google Scholar 

  18. Levy BD, Clish CB, Schmidt B, Gronert K, Serhan CN (2001) Lipid mediator class switching during acute inflammation: signals in resolution. Nat Immunol 2(7):612–619

    CAS  PubMed  Google Scholar 

  19. Arita M, Bianchini F, Aliberti J, Sher A, Chiang N, Hong S, Yang R, Petasis NA, Serhan CN (2005) Stereochemical assignment, antiinflammatory properties, and receptor for the omega-3 lipid mediator resolvin E1. J Exp Med 201(5):713–722. https://doi.org/10.1084/jem.20042031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Chiang N, Fredman G, Bäckhed F, Oh SF, Vickery T, Schmidt BA, Serhan CN (2012) Infection regulates pro-resolving mediators that lower antibiotic requirements. Nature 484(7395):524–528

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Han CZ, Ravichandran KS (2011) Metabolic connections during apoptotic cell engulfment. Cell 147(7):1442–1445

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Köröskényi K, Duró E, Pallai A, Sarang Z, Kloor D, Ucker DS, Beceiro S, Castrillo A, Chawla A, Ledent CA (2011) Involvement of adenosine A2A receptors in engulfment-dependent apoptotic cell suppression of inflammation. J Immunol 1002284

  23. Serhan CN, Chiang N (2013) Resolution phase lipid mediators of inflammation: agonists of resolution. Curr Opin Pharmacol 13(4):632–640

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Dalli J, Winkler JW, Colas RA, Arnardottir H, Cheng C-YC, Chiang N, Petasis NA, Serhan CN (2013) Resolvin D3 and aspirin-triggered resolvin D3 are potent immunoresolvents. Chem Biol 20(2):188–201

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Schwab JM, Chiang N, Arita M, Serhan CN (2007) Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 447(7146):869–874

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Spite M, Serhan CN (2010) Novel lipid mediators promote resolution of acute inflammation: impact of aspirin and statins. Circ Res 107(10):1170–1184

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Nathan C (2002) Points of control in inflammation. Nature 420(6917):846–852

    CAS  PubMed  Google Scholar 

  28. Back M, Yurdagul A Jr, Tabas I, Oorni K, Kovanen PT (2019) Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities. Nat Rev Cardiol 16:389–406. https://doi.org/10.1038/s41569-019-0169-2

    Article  PubMed  PubMed Central  Google Scholar 

  29. Serhan CN (2007) Resolution phase of inflammation: novel endogenous anti-inflammatory and proresolving lipid mediators and pathways. Annu Rev Immunol 25:101–137. https://doi.org/10.1146/annurev.immunol.25.022106.141647

    Article  CAS  PubMed  Google Scholar 

  30. Bannenberg G, Serhan CN (2010) Specialized pro-resolving lipid mediators in the inflammatory response: an update. Biochim Biophys Acta 1801(12):1260–1273. https://doi.org/10.1016/j.bbalip.2010.08.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Serhan CN (2010) Novel lipid mediators and resolution mechanisms in acute inflammation: to resolve or not? Am J Pathol 177(4):1576–1591. https://doi.org/10.2353/ajpath.2010.100322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Sun YP, Oh SF, Uddin J, Yang R, Gotlinger K, Campbell E, Colgan SP, Petasis NA, Serhan CN (2007) Resolvin D1 and its aspirin-triggered 17R epimer. Stereochemical assignments, anti-inflammatory properties, and enzymatic inactivation. J Biol Chem 282(13):9323–9334. https://doi.org/10.1074/jbc.M609212200

    Article  CAS  PubMed  Google Scholar 

  33. Spite M, Norling LV, Summers L, Yang R, Cooper D, Petasis NA, Flower RJ, Perretti M, Serhan CN (2009) Resolvin D2 is a potent regulator of leukocytes and controls microbial sepsis. Nature 461(7268):1287–1291. https://doi.org/10.1038/nature08541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Arita M, Yoshida M, Hong S, Tjonahen E, Glickman JN, Petasis NA, Blumberg RS, Serhan CN (2005) Resolvin E1, an endogenous lipid mediator derived from omega-3 eicosapentaenoic acid, protects against 2,4,6-trinitrobenzene sulfonic acid-induced colitis. Proc Natl Acad Sci U S A 102(21):7671–7676. https://doi.org/10.1073/pnas.0409271102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Serhan CN, Clish CB, Brannon J, Colgan SP, Chiang N, Gronert K (2000) Novel functional sets of lipid-derived mediators with antiinflammatory actions generated from omega-3 fatty acids via cyclooxygenase 2-nonsteroidal antiinflammatory drugs and transcellular processing. J Exp Med 192(8):1197–1204

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Fetterman JW Jr, Zdanowicz MM (2009) Therapeutic potential of n-3 polyunsaturated fatty acids in disease. Am J Health Syst Pharm 66(13):1169–1179. https://doi.org/10.2146/ajhp080411

    Article  CAS  PubMed  Google Scholar 

  37. Simopoulos AP (2002) Omega-3 fatty acids in inflammation and autoimmune diseases. J Am Coll Nutr 21(6):495–505

    CAS  PubMed  Google Scholar 

  38. Harper CR, Jacobson TA (2001) The fats of life: the role of omega-3 fatty acids in the prevention of coronary heart disease. Arch Intern Med 161(18):2185–2192

    CAS  PubMed  Google Scholar 

  39. Herrera BS, Hasturk H, Kantarci A, Freire MO, Nguyen O, Kansal S, Van Dyke TE (2015) Impact of resolvin E1 on murine neutrophil phagocytosis in type 2 diabetes. Infect Immun 83(2):792–801

    PubMed  PubMed Central  Google Scholar 

  40. Herová M, Schmid M, Gemperle C, Hersberger M (2015) ChemR23, the receptor for chemerin and resolvin E1, is expressed and functional on M1 but not on M2 macrophages. J Immunol 1402166

  41. Seki H, Fukunaga K, Arita M, Arai H, Nakanishi H, Taguchi R, Miyasho T, Takamiya R, Asano K, Ishizaka A (2010) The anti-inflammatory and proresolving mediator resolvin E1 protects mice from bacterial pneumonia and acute lung injury. J Immunol 184(2):836–843

    CAS  PubMed  Google Scholar 

  42. El Kebir D, Gjorstrup P, Filep JG (2012) Resolvin E1 promotes phagocytosis-induced neutrophil apoptosis and accelerates resolution of pulmonary inflammation. Proc Natl Acad Sci 201206641

  43. Hong S, Porter TF, Lu Y, Oh SF, Pillai PS, Serhan CN (2008) Resolvin E1 metabolome in local inactivation during inflammation-resolution. J Immunol 180(5):3512–3519

    CAS  PubMed  Google Scholar 

  44. Titos E, Rius B, González-Périz A, López-Vicario C, Morán-Salvador E, Martínez-Clemente M, Arroyo V, Clària J (2011) Resolvin D1 and its precursor docosahexaenoic acid promote resolution of adipose tissue inflammation by eliciting macrophage polarization toward an M2-like phenotype. J Immunol 1100225

  45. Serhan CN (2014) Pro-resolving lipid mediators are leads for resolution physiology. Nature 510(7503):92–101

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Kohli P, Levy BD (2009) Resolvins and protectins: mediating solutions to inflammation. Br J Pharmacol 158(4):960–971

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Mogensen TH (2009) Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev 22(2):240–273

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Akagi D, Chen M, Toy R, Chatterjee A, Conte MS (2015) Systemic delivery of proresolving lipid mediators resolvin D2 and maresin 1 attenuates intimal hyperplasia in mice. FASEB J 29(6):2504–2513

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Krishnamoorthy S, Recchiuti A, Chiang N, Yacoubian S, Lee C-H, Yang R, Petasis NA, Serhan CN (2010) Resolvin D1 binds human phagocytes with evidence for proresolving receptors. Proc Natl Acad Sci 107(4):1660–1665

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Krishnamoorthy S, Recchiuti A, Chiang N, Fredman G, Serhan CN (2012) Resolvin D1 receptor stereoselectivity and regulation of inflammation and proresolving microRNAs. Am J Pathol 180(5):2018–2027

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Park C-K, Xu Z-Z, Liu T, Lü N, Serhan CN, Ji R-R (2011) Resolvin D2 is a potent endogenous inhibitor for transient receptor potential subtype V1/A1, inflammatory pain, and spinal cord synaptic plasticity in mice: distinct roles of resolvin D1, D2, and E1. J Neurosci 31(50):18433–18438

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Wang B, Gong X, J-y W, Zhang L, Zhang Z, Li H-z, Min S (2011) Resolvin D1 protects mice from LPS-induced acute lung injury. Pulm Pharmacol Ther 24(4):434–441

    PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Wang L, Wang FS, Gershwin ME (2015) Human autoimmune diseases: a comprehensive update. J Intern Med 278(4):369–395

    CAS  PubMed  Google Scholar 

  55. Baccala R, Hoebe K, Kono DH, Beutler B, Theofilopoulos AN (2007) TLR-dependent and TLR-independent pathways of type I interferon induction in systemic autoimmunity. Nat Med 13(5):543–551

    CAS  PubMed  Google Scholar 

  56. Mitchell S, Thomas G, Harvey K, Cottell D, Reville K, Berlasconi G, Petasis NA, Erwig L, Rees AJ, Savill J (2002) 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 13(10):2497–2507

    CAS  PubMed  Google Scholar 

  57. Milligan G, Stoddart LA, Brown AJ (2006) G protein-coupled receptors for free fatty acids. Cell Signal 18(9):1360–1365. https://doi.org/10.1016/j.cellsig.2006.03.011

    Article  CAS  PubMed  Google Scholar 

  58. Eizirik DL, Colli ML, Ortis F (2009) The role of inflammation in insulitis and β-cell loss in type 1 diabetes. Nat Rev Endocrinol 5(4):219–226

    CAS  PubMed  Google Scholar 

  59. Serhan CN, Hong S, Gronert K, Colgan SP, Devchand PR, Mirick G, Moussignac R-L (2002) Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J Exp Med 196(8):1025–1037

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Chiang N, Arita M, Serhan CN (2005) Anti-inflammatory circuitry: lipoxin, aspirin-triggered lipoxins and their receptor ALX. Prostaglandins Leukot Essent Fat Acids 73(3–4):163–177

    CAS  Google Scholar 

  61. Oh DY, Talukdar S, Bae EJ, Imamura T, Morinaga H, Fan W, Li P, Lu WJ, Watkins SM, Olefsky JM (2010) GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell 142(5):687–698

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Das UN (2011) Lipoxins as biomarkers of lupus and other inflammatory conditions. Lipids Health Dis 10:76. https://doi.org/10.1186/1476-511x-10-76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Lattin JE, Schroder K, Su AI, Walker JR, Zhang J, Wiltshire T, Saijo K, Glass CK, Hume DA, Kellie S, Sweet MJ (2008) Expression analysis of G protein-coupled receptors in mouse macrophages. Immunome Res 4:5. https://doi.org/10.1186/1745-7580-4-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Weylandt KH, Kang JX, Wiedenmann B, Baumgart DC (2007) Lipoxins and resolvins in inflammatory bowel disease. Inflamm Bowel Dis 13(6):797–799. https://doi.org/10.1002/ibd.20109

    Article  PubMed  Google Scholar 

  65. Kelsall BL, Leon F (2005) Involvement of intestinal dendritic cells in oral tolerance, immunity to pathogens, and inflammatory bowel disease. Immunol Rev 206:132–148. https://doi.org/10.1111/j.0105-2896.2005.00292.x

    Article  CAS  PubMed  Google Scholar 

  66. Baumgart DC, Metzke D, Schmitz J, Scheffold A, Sturm A, Wiedenmann B, Dignass AU (2005) Patients with active inflammatory bowel disease lack immature peripheral blood plasmacytoid and myeloid dendritic cells. Gut 54(2):228–236. https://doi.org/10.1136/gut.2004.040360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Allen B (1991) Fish oil in combination with other therapies in the treatment of psoriasis. In: Health effects of omega 3 polyunsaturated fatty acids in seafoods, vol 66. Karger Publishers, pp 436–445

  68. Cleland L, James M (1997) Rheumatoid arthritis and the balance of dietary N-6 and N-3 essential fatty acids. Br J Rheumatol 36(5):513–514

    CAS  PubMed  Google Scholar 

  69. Kremer JM (2000) N-3 fatty acid supplements in rheumatoid arthritis. Am J Clin Nutr 71(1 Suppl):349s–351s. https://doi.org/10.1093/ajcn/71.1.349s

    Article  CAS  PubMed  Google Scholar 

  70. Bhatt DL, Steg PG, Miller M, Brinton EA, Jacobson TA, Ketchum SB, Doyle RT Jr, Juliano RA, Jiao L, Granowitz C (2019) Cardiovascular risk reduction with icosapent ethyl for hypertriglyceridemia. N Engl J Med 380(1):11–22

    CAS  PubMed  Google Scholar 

  71. Hughes RA, Cornblath DR (2005) Guillain-Barre syndrome. Lancet (London, England) 366(9497):1653–1666. https://doi.org/10.1016/s0140-6736(05)67665-9

    Article  CAS  Google Scholar 

  72. Soliven B (2012) Autoimmune neuropathies: insights from animal models. J Peripher Nerv Syst 17:28–33

    CAS  PubMed  Google Scholar 

  73. Yun JH, Henson PM, Tuder RM (2008) Phagocytic clearance of apoptotic cells: role in lung disease. Exp Rev Respir Med 2(6):753–765. https://doi.org/10.1586/17476348.2.6.753

    Article  Google Scholar 

  74. Annunziato F, Cosmi L, Liotta F, Maggi E, Romagnani S (2008) The phenotype of human Th17 cells and their precursors, the cytokines that mediate their differentiation and the role of Th17 cells in inflammation. Int Immunol 20(11):1361–1368. https://doi.org/10.1093/intimm/dxn106

    Article  CAS  PubMed  Google Scholar 

  75. Fadok VA, Bratton DL, Konowal A, Freed PW, Westcott JY, Henson PM (1998) Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J Clin Invest 101(4):890–898

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Kimura A, Naka T, Kishimoto T (2007) IL-6-dependent and -independent pathways in the development of interleukin 17-producing T helper cells. Proc Natl Acad Sci 104(29):12099–12104. https://doi.org/10.1073/pnas.0705268104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Luchting B, Rachinger-Adam B, Heyn J, Hinske LC, Kreth S, Azad SC (2015) Anti-inflammatory T-cell shift in neuropathic pain. J Neuroinflammation 12:12. https://doi.org/10.1186/s12974-014-0225-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Zhang Z, Zhang ZY, Schluesener HJ (2009) Compound A, a plant origin ligand of glucocorticoid receptors, increases regulatory T cells and M2 macrophages to attenuate experimental autoimmune neuritis with reduced side effects. J Immunol 183(5):3081–3091. https://doi.org/10.4049/jimmunol.0901088

    Article  CAS  PubMed  Google Scholar 

  79. Luo B, Han F, Xu K, Wang J, Liu Z, Shen Z, Li J, Liu Y, Jiang M, Zhang ZY, Zhang Z (2016) Resolvin D1 programs inflammation resolution by increasing TGF-beta expression induced by dying cell clearance in experimental autoimmune neuritis. J Neurosci 36(37):9590–9603. https://doi.org/10.1523/jneurosci.0020-16.2016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Dhopeshwarkar A, Mackie K (2014) CB2 cannabinoid receptors as a therapeutic target—what does the future hold? Mol Pharmacol 86(4):430–437

    PubMed  PubMed Central  Google Scholar 

  81. Rom S, Persidsky Y (2013) Cannabinoid receptor 2: potential role in immunomodulation and neuroinflammation. J NeuroImmune Pharmacol 8(3):608–620

    PubMed  PubMed Central  Google Scholar 

  82. Turcotte C, Blanchet M-R, Laviolette M, Flamand N (2016) The CB 2 receptor and its role as a regulator of inflammation. Cell Mol Life Sci 73(23):4449–4470

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Tepper MA, Zurier RB, Burstein SH (2014) Ultrapure ajulemic acid has improved CB2 selectivity with reduced CB1 activity. Bioorg Med Chem 22(13):3245–3251

    CAS  PubMed  Google Scholar 

  84. Motwani MP, Bennett F, Norris PC, Maini AA, George MJ, Newson J, Henderson A, Hobbs AJ, Tepper M, White B (2018) Potent anti-inflammatory and pro-resolving effects of anabasum in a human model of self-resolving acute inflammation. Clin Pharmacol Ther 104(4):675–686

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Zurier RB, Rossetti RG, Lane JH, Goldberg JM, Hunter SA, Burstein SH (1998) Dimethylheptyl-THC-11 OIC acid: a nonpsychoactive antiinflammatory agent with a cannabinoid template structure. Arthritis Rheum 41(1):163–170

    CAS  PubMed  Google Scholar 

  86. Zurier RB, Sun Y-P, George KL, Stebulis JA, Rossetti RG, Skulas A, Judge E, Serhan CN (2009) Ajulemic acid, a synthetic cannabinoid, increases formation of the endogenous proresolving and anti-inflammatory eicosanoid, lipoxin A4. FASEB J 23(5):1503–1509

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Gonzalez EG, Selvi E, Balistreri E, Akhmetshina A, Palumbo K, Lorenzini S, Lazzerini PE, Montilli C, Capecchi PL, Lucattelli M (2012) Synthetic cannabinoid ajulemic acid exerts potent antifibrotic effects in experimental models of systemic sclerosis. Ann Rheum Dis 71(9):1545–1551

    CAS  PubMed  Google Scholar 

  88. Lucattelli M, Fineschi S, Selvi E, Gonzalez EG, Bartalesi B, De Cunto G, Lorenzini S, Galeazzi M, Lungarella G (2016) Ajulemic acid exerts potent anti-fibrotic effect during the fibrogenic phase of bleomycin lung. Respir Res 17(1):49

    PubMed  PubMed Central  Google Scholar 

  89. Abdolmaleki F, Farahani N, Gheibi Hayat SM, Pirro M, Bianconi V, Barreto GE, Sahebkar A (2018) The role of efferocytosis in autoimmune diseases. Front Immunol 9:1645. https://doi.org/10.3389/fimmu.2018.01645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Gheibi Hayat SM, Bianconi V, Pirro M, Sahebkar A (2019) Efferocytosis: molecular mechanisms and pathophysiological perspectives. Immunol Cell Biol 97(2):124–133. https://doi.org/10.1111/imcb.12206

    Article  PubMed  Google Scholar 

  91. Tajbakhsh A, Gheibi Hayat SM, Butler AE, Sahebkar A (2019) Effect of soluble cleavage products of important receptors/ligands on efferocytosis: their role in inflammatory, autoimmune and cardiovascular disease. Ageing Res Rev 50:43–57. https://doi.org/10.1016/j.arr.2019.01.007

    Article  CAS  PubMed  Google Scholar 

  92. Tajbakhsh A, Rezaee M, Kovanen PT, Sahebkar A (2018) Efferocytosis in atherosclerotic lesions: malfunctioning regulatory pathways and control mechanisms. Pharmacol Ther 188:12–25. https://doi.org/10.1016/j.pharmthera.2018.02.003

    Article  CAS  PubMed  Google Scholar 

  93. Lauber K, Blumenthal SG, Waibel M, Wesselborg S (2004) Clearance of apoptotic cells: getting rid of the corpses. Mol Cell 14(3):277–287

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Cellular and Molecular Research Center, School of Paramedical Sciences, Qazvin University of Medical Sciences, Qazvin, Iran

    Fereshte Abdolmaleki

  2. Wihuri Research Institute, Helsinki, Finland

    Petri T. Kovanen

  3. Department of Biochemistry, Pasteur Institute of Iran, Tehran, Iran

    Rajab Mardani

  4. Department of Genetics, School of Medicine, Shahid Sadoughi University of Medical Sciences, Yazd, Iran

    Seyed Mohammad Gheibi-hayat

  5. Department of Medical Sciences, AOU Città della Salute e della Scienza di Torino, University of Turin, Torino, Italy

    Simona Bo

  6. Neurogenic Inflammation Research Center, Mashhad University of Medical Sciences, Mashhad, Iran

    Amirhossein Sahebkar

  7. Biotechnology Research Center, Pharmaceutical Technology Institute, Mashhad University of Medical Sciences, Mashhad, 9177948564, Iran

    Amirhossein Sahebkar

  8. School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran

    Amirhossein Sahebkar

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  1. Fereshte Abdolmaleki
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Abdolmaleki, F., Kovanen, P.T., Mardani, R. et al. Resolvins: Emerging Players in Autoimmune and Inflammatory Diseases. Clinic Rev Allerg Immunol 58, 82–91 (2020). https://doi.org/10.1007/s12016-019-08754-9

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