Specialized Proresolving Lipid Mediators: A Potential Therapeutic Target for Atherosclerosis

. 2022 Mar 15 ; 23 (6) : . [epub] 20220315

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid35328553

Grantová podpora
CC-0437-10-21-09-10 Consejo de Desarrollo Científico, Humanístico y Tecnológico (CONDES), University of Zulia

Cardiovascular disease (CVD) is a global public health issue due to its high morbidity, mortality, and economic impact. The implementation of innovative therapeutic alternatives for CVD is urgently required. Specialized proresolving lipid mediators (SPMs) are bioactive compounds derived from ω-3 and ω-6 fatty acids, integrated into four families: Lipoxins, Resolvins, Protectins, and Maresins. SPMs have generated interest in recent years due to their ability to promote the resolution of inflammation associated with the pathogeneses of numerous illnesses, particularly CVD. Several preclinical studies in animal models have evidenced their ability to decrease the progression of atherosclerosis, intimal hyperplasia, and reperfusion injury via diverse mechanisms. Large-scale clinical trials are required to determine the effects of SPMs in humans. This review integrates the currently available knowledge of the therapeutic impact of SPMs in CVD from preclinical and clinical studies, along with the implicated molecular pathways. In vitro results have been promising, and as such, SPMs could soon represent a new therapeutic alternative for CVD.

Zobrazit více v PubMed

Capó X., Martorell M., Busquets-Cortés C., Tejada S., Tur J.A., Pons A., Sureda A. Resolvins as proresolving inflammatory mediators in cardiovascular disease. Eur. J. Med. Chem. 2018;153:123–130. doi: 10.1016/j.ejmech.2017.07.018. PubMed DOI

World Health Organization Cardiovascular Diseases (CVDs) [(accessed on 18 August 2021)]. Available online: https://www.who.int/news-room/fact-sheets/detail/cardiovascular-diseases-(cvds)

Morales Aguilar R., Lastre-Amell G., Pardo Vásquez A. Estilos de vida relacionados con factores de riesgo cardiovascular. AVFT Arch. Venez. Farm. Ter. 2018;37:50–62.

Recchiuti A., Serhan C.N. Pro-Resolving Lipid Mediators (SPMs) and Their Actions in Regulating miRNA in Novel Resolution Circuits in Inflammation. Front. Immunol. 2012;3:298. doi: 10.3389/fimmu.2012.00298. PubMed DOI PMC

Sugimoto M.A., Sousa L.P., Pinho V., Perretti M., Teixeira M.M. Resolution of Inflammation: What Controls Its Onset? Front. Immunol. 2016;7:160. doi: 10.3389/fimmu.2016.00160. PubMed DOI PMC

Nathan C., Ding A. Nonresolving Inflammation. Cell. 2010;140:871–882. doi: 10.1016/j.cell.2010.02.029. PubMed DOI

Headland S.E., Norling L.V. The resolution of inflammation: Principles and challenges. Semin. Immunol. 2015;27:149–160. doi: 10.1016/j.smim.2015.03.014. PubMed DOI

Serhan C.N., Chiang N., Van Dyke T.E. Resolving inflammation: Dual anti-inflammatory and pro-resolution lipid mediators. Nat. Rev. Immunol. 2008;8:349–361. doi: 10.1038/nri2294. PubMed DOI PMC

Buckley C.D., Gilroy D.W., Serhan C.N. Pro-Resolving lipid mediators and Mechanisms in the resolution of acute inflammation. Immunity. 2014;40:315–327. doi: 10.1016/j.immuni.2014.02.009. PubMed DOI PMC

Basil M.C., Levy B.D. Specialized pro-resolving mediators: Endogenous regulators of infection and inflammation. Nat. Rev. Immunol. 2016;16:51–67. doi: 10.1038/nri.2015.4. PubMed DOI PMC

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;3:88–106. doi: 10.1021/acsptsci.9b00075. PubMed DOI PMC

Doran A.C. Inflammation Resolution: Implications for Atherosclerosis. Circ. Res. 2022;130:130–148. doi: 10.1161/CIRCRESAHA.121.319822. PubMed DOI PMC

de Gaetano M., McEvoy C., Andrews D., Cacace A., Hunter J., Brennan E., Godson C. Specialized Pro-resolving Lipid Mediators: Modulation of Diabetes-Associated Cardio-, Reno-, and Retino-Vascular Complications. Front. Pharmacol. 2018;9:1488. doi: 10.3389/fphar.2018.01488. PubMed DOI PMC

Doyle R., Sadlier D.M., Godson C. Pro-resolving lipid mediators: Agents of anti-ageing? Semin. Immunol. 2018;40:36–48. doi: 10.1016/j.smim.2018.09.002. PubMed DOI

Viola J.R., Lemnitzer P., Jansen Y., Csaba G., Winter C., Neideck C., Silvestre-Roig C., Dittmar G., Döring Y., Drechsler M., et al. Resolving Lipid Mediators Maresin 1 and Resolvin D2 Prevent Atheroprogression in Mice. Circ. Res. 2016;119:1030–1038. doi: 10.1161/CIRCRESAHA.116.309492. PubMed DOI

Fredman G., Spite M. Specialized pro-resolving mediators in cardiovascular diseases. Mol. Asp. Med. 2017;58:65–71. doi: 10.1016/j.mam.2017.02.003. PubMed DOI PMC

Kasikara C., Doran A.C., Cai B., Tabas I. The role of non-resolving inflammation in atherosclerosis. J. Clin. Investig. 2018;128:2713–2723. doi: 10.1172/JCI97950. PubMed DOI PMC

Satish M., Agrawal D.K. Pro-resolving lipid mediators in the resolution of neointimal hyperplasia pathogenesis in atherosclerotic diseases. Expert Rev. Cardiovasc. Ther. 2019;17:177–184. doi: 10.1080/14779072.2019.1563483. PubMed DOI PMC

Halade G.V., Black L.M., Verma M. Paradigm shift—Metabolic transformation of docosahexaenoic and eicosapentaenoic acids to bioactives exemplify the promise of fatty acid drug discovery. Biotechnol. Adv. 2018;36:935–953. doi: 10.1016/j.biotechadv.2018.02.014. PubMed DOI PMC

Halade G.V., Kain V., Ingle K.A., Prabhu S.D. Interaction of 12/15-lipoxygenase with fatty acids alters the leukocyte kinetics leading to improved postmyocardial infarction healing. Am. J. Physiol. Heart Circ. Physiol. 2017;313:H89–H102. doi: 10.1152/ajpheart.00040.2017. PubMed DOI PMC

Halade G.V., Kain V., Tourki B., Jadapalli J.K. Lipoxygenase drives lipidomic and metabolic reprogramming in ischemic heart failure. Metabolism. 2019;96:22–32. doi: 10.1016/j.metabol.2019.04.011. PubMed DOI

Chiang N., Serhan C.N. Structural elucidation and physiologic functions of specialized pro-resolving mediators and their receptors. Mol. Asp. Med. 2017;58:114–129. doi: 10.1016/j.mam.2017.03.005. PubMed DOI PMC

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. Investig. 2018;128:3568–3582. doi: 10.1172/JCI99888. PubMed DOI PMC

Dalli J., Serhan C.N. Identification and structure elucidation of the pro-resolving mediators provides novel leads for resolution pharmacology. Br. J. Pharmacol. 2019;176:1024–1037. doi: 10.1111/bph.14336. PubMed DOI PMC

Han Y.-H., Lee K., Saha A., Han J., Choi H., Noh M., Lee Y.-H., Lee M.-O. Specialized Proresolving Mediators for Therapeutic Interventions Targeting Metabolic and Inflammatory Disorders. Biomol. Ther. 2021;29:455–464. doi: 10.4062/biomolther.2021.094. PubMed DOI PMC

Kang G.J., Kim E.J., Lee C.H. Therapeutic Effects of Specialized Pro-Resolving Lipids Mediators on Cardiac Fibrosis via NRF2 Activation. Antioxidants. 2020;9:1259. doi: 10.3390/antiox9121259. PubMed DOI PMC

Recchiuti A. Resolvin D1 and its GPCRs in resolution circuits of inflammation. Prostaglandins Other Lipid Mediat. 2013;107:64–76. doi: 10.1016/j.prostaglandins.2013.02.004. PubMed DOI

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., et al. Protective effects of GPR37 via regulation of inflammation and multiple cell death pathways after ischemic stroke in mice. FASEB J. 2019;33:10680–10691. doi: 10.1096/fj.201900070R. PubMed DOI PMC

Dalli J., Serhan C.N. Pro-Resolving Mediators in Regulating and Conferring Macrophage Function. Front. Immunol. 2017;8:1400. doi: 10.3389/fimmu.2017.01400. PubMed DOI PMC

Yokomizo T. Two distinct leukotriene B4 receptors, BLT1 and BLT2. J. Biochem. 2015;157:65–71. doi: 10.1093/jb/mvu078. PubMed DOI

Colas R.A., Dalli J., Chiang N., Vlasakov I., Sanger J.M., Riley I.R., Serhan C.N. Identification and Actions of the Maresin 1 Metabolome in Infectious Inflammation. J. Immunol. 2016;197:4444–4452. doi: 10.4049/jimmunol.1600837. PubMed DOI PMC

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. Investig. 2019;129:5294–5311. doi: 10.1172/JCI129448. PubMed DOI PMC

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. Investig. 2020;130:359–373. doi: 10.1172/JCI131609. PubMed DOI PMC

Chattopadhyay R., Mani A.M., Singh N.K., Rao G.N. Resolvin D1 blocks H2O2-mediated inhibitory crosstalk between SHP2 and PP2A and suppresses endothelial-monocyte interactions. Free Radic. Biol. Med. 2018;117:119–131. doi: 10.1016/j.freeradbiomed.2018.01.034. PubMed DOI PMC

Chattopadhyay R., Raghavan S., Rao G.N. Resolvin D1 via prevention of ROS-mediated SHP2 inactivation protects endothelial adherens junction integrity and barrier function. Redox Biol. 2017;12:438–455. doi: 10.1016/j.redox.2017.02.023. PubMed DOI PMC

Carracedo M., Artiach G., Arnardottir H., Bäck M. The resolution of inflammation through omega-3 fatty acids in atherosclerosis, intimal hyperplasia, and vascular calcification. Semin. Immunopathol. 2019;41:757–766. doi: 10.1007/s00281-019-00767-y. PubMed DOI PMC

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;107:1660–1665. doi: 10.1073/pnas.0907342107. PubMed DOI PMC

So J., Wu D., Lichtenstein A.H., Tai A.K., Matthan N.R., Maddipati K.R., Lamon-Fava S. EPA and DHA differentially modulate monocyte inflammatory response in subjects with chronic inflammation in part via plasma specialized pro-resolving lipid mediators: A randomized, double-blind, crossover study. Atherosclerosis. 2020;316:90–98. doi: 10.1016/j.atherosclerosis.2020.11.018. PubMed DOI

Lopez E.F., Kabarowski J.H., Ingle K.A., Kain V., Barnes S., Crossman D., Lindsey M., Halade G.V. Obesity superimposed on aging magnifies inflammation and delays the resolving response after myocardial infarction. Am. J. Physiol. Circ. Physiol. 2015;308:H269–H280. doi: 10.1152/ajpheart.00604.2014. PubMed DOI PMC

Halade G.V., Kain V., Black L.M., Prabhu S.D., Ingle K.A. Aging dysregulates D- and E-series resolvins to modulate cardiosplenic and cardiorenal network following myocardial infarction. Aging. 2016;8:2611–2634. doi: 10.18632/aging.101077. PubMed DOI PMC

Jadapalli J.K., Wright G.W., Kain V., Sherwani M.A., Sonkar R., Yusuf N., Halade G.V. Doxorubicin triggers splenic contraction and irreversible dysregulation of COX and LOX that alters the inflammation-resolution program in the myocardium. Am. J. Physiol. Circ. Physiol. 2018;315:H1091–H1100. doi: 10.1152/ajpheart.00290.2018. PubMed DOI PMC

Halade G.V., Kain V., Wright G.M., Jadapalli J.K. Subacute treatment of carprofen facilitate splenocardiac resolution deficit in cardiac injury. J. Leukoc. Biol. 2018;104:1173–1186. doi: 10.1002/JLB.3A0618-223R. PubMed DOI PMC

Kain V., Jadapalli J.K., Tourki B., Halade G.V. Inhibition of FPR2 impaired leukocytes recruitment and elicited non-resolving inflammation in acute heart failure. Pharmacol. Res. 2019;146:104295. doi: 10.1016/j.phrs.2019.104295. PubMed DOI PMC

Brennan E., Kantharidis P., Cooper M.E., Godson C. Pro-resolving lipid mediators: Regulators of inflammation, metabolism and kidney function. Nat. Rev. Nephrol. 2021;17:725–739. doi: 10.1038/s41581-021-00454-y. PubMed DOI PMC

Jadapalli J.K., Halade G.V. Unified nexus of macrophages and maresins in cardiac reparative mechanisms. FASEB J. 2018;32:5227–5237. doi: 10.1096/fj.201800254R. PubMed DOI PMC

Chandrasekharan J.A., Sharma-Walia N. Lipoxins: Nature’s way to resolve inflammation. J. Inflamm. Res. 2015;8:181–192. PubMed PMC

Ho K.J., Spite M., Owens C.D., Lancero H., Kroemer A.H., Pande R., Creager M.A., Serhan C.N., Conte M.S. Aspirin-Triggered Lipoxin and Resolvin E1 Modulate Vascular Smooth Muscle Phenotype and Correlate with Peripheral Atherosclerosis. Am. J. Pathol. 2010;177:2116–2123. doi: 10.2353/ajpath.2010.091082. PubMed DOI PMC

Rafieian-Kopaei M., Setorki M., Doudi M., Baradaran A., Nasri H. Atherosclerosis: Process, Indicators, Risk Factors and New Hopes. Int. J. Prev. Med. 2014;5:927–946. PubMed PMC

Verónica Mora D.E., Morr C., Paciotti S., Prospert O.P., Quiroz J. Células inflamatorias en lesiones ateroescleróticas de las arterias coronarias humanas. Gac. Médica Caracas. 2020;124:298–307.

Fredman G., Tabas I. Boosting Inflammation Resolution in Atherosclerosis: The Next Frontier for Therapy. Am. J. Pathol. 2017;187:1211–1221. doi: 10.1016/j.ajpath.2017.01.018. PubMed DOI PMC

Rojas J., Salazar J., Martínez M.S., Palmar J., Bautista J., Chávez-Castillo M., Gómez A., Bermudez V. Macrophage Heterogeneity and Plasticity: Impact of Macrophage Biomarkers on Atherosclerosis. Scientifica. 2015;2015:1–17. doi: 10.1155/2015/851252. PubMed DOI PMC

Viola J., Soehnlein O. Atherosclerosis—A matter of unresolved inflammation. Semin. Immunol. 2015;27:184–193. doi: 10.1016/j.smim.2015.03.013. PubMed DOI

Sansbury B.E., Spite M. Resolution of Acute Inflammation and the Role of Resolvins in Immunity, Thrombosis, and Vascular Biology. Circ. Res. 2016;119:113–130. doi: 10.1161/CIRCRESAHA.116.307308. PubMed DOI PMC

Kain V., Van Der Pol W., Mariappan N., Ahmad A., Eipers P., Morrow C., Gibson D.L., Gladine C., Vigor C., Durand T., et al. Obesogenic diet in aging mice disrupts gut microbe composition and alters neutrophil:lymphocyte ratio leading to inflamed milieu in acute heart failure. FASEB J. 2019;33:6456–6469. doi: 10.1096/fj.201802477R. PubMed DOI PMC

Chatterjee A., Sharma A., Chen M., Toy R., Mottola G., Conte M.S. The Pro-Resolving Lipid Mediator Maresin 1 (MaR1) Attenuates Inflammatory Signaling Pathways in Vascular Smooth Muscle and Endothelial Cells. PLoS ONE. 2014;9:e113480. doi: 10.1371/journal.pone.0113480. PubMed DOI PMC

Cherpokova D., Jouvene C.C., Libreros S., DeRoo E.P., Chu L., De La Rosa X., Norris P.C., Wagner D.D., Serhan C.N. Resolvin D4 attenuates the severity of pathological thrombosis in mice. Blood. 2019;134:1458–1468. doi: 10.1182/blood.2018886317. PubMed DOI PMC

Miyahara T., Runge S., Chatterjee A., Chen M., Mottola G., Fitzgerald J.M., Serhan C.N., Conte M.S. D-series resolvin attenuates vascular smooth muscle cell activation and neointimal hyperplasia following vascular injury. FASEB J. 2013;27:2220–2232. doi: 10.1096/fj.12-225615. PubMed DOI PMC

Dalli J., Serhan C.N. Specific lipid mediator signatures of human phagocytes: Microparticles stimulate macrophage efferocytosis and pro-resolving mediators. Blood. 2012;120:e60–e72. doi: 10.1182/blood-2012-04-423525. PubMed DOI PMC

Mitchell S., Thomas G., Harvey K., Cottell D., Reville K., Berlasconi G., Petasis N., Erwig L., Rees A.J., Savill J., et al. 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;13:2497–2507. doi: 10.1097/01.ASN.0000032417.73640.72. PubMed DOI

Petri M.H., Laguna-Fernández A., Gonzalez-Diez M., Paulsson-Berne G., Hansson G.K., Bäck M. The role of the FPR2/ALX receptor in atherosclerosis development and plaque stability. Cardiovasc. Res. 2015;105:65–74. doi: 10.1093/cvr/cvu224. PubMed DOI PMC

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. Arter. Thromb. Vasc. Biol. 2012;32:1970–1978. doi: 10.1161/ATVBAHA.112.249508. PubMed DOI PMC

Spite M., Norling L.V., Summers L., Yang R., Cooper D., Petasis N.A., Flower R.J., Perretti M., Serhan C.N. Resolvin D2 is a potent regulator of leukocytes and controls microbial sepsis. Nature. 2009;461:1287–1291. doi: 10.1038/nature08541. PubMed DOI PMC

Roig C.S., Daemen M., Lutgens E., Soehnlein O., Hartwig H. Neutrophils in atherosclerosis. A brief overview. Hamostaseologie. 2015;35:121–127. doi: 10.5482/HAMO-14-09-0040. PubMed DOI

Zhang P., Yin Y., Wang T., Li W., Li C., Zeng X., Yang W., Zhang R., Tang Y., Shi L., et al. Maresin 1 mitigates concanavalin A-induced acute liver injury in mice by inhibiting ROS-mediated activation of NF-κB signaling. Free Radic. Biol. Med. 2020;147:23–36. doi: 10.1016/j.freeradbiomed.2019.11.033. PubMed DOI

Zhuang Y., Liu H., Zhou X.E., Verma R.K., De Waal P.W., Jang W., Xu T.-H., Wang L., Meng X., Zhao G., et al. Structure of formylpeptide receptor 2-Gi complex reveals insights into ligand recognition and signaling. Nat. Commun. 2020;11:885. doi: 10.1038/s41467-020-14728-9. PubMed DOI PMC

Romano M., Cianci E., Simiele F., Recchiuti A. Lipoxins and aspirin-triggered lipoxins in resolution of inflammation. Eur. J. Pharmacol. 2015;760:49–63. doi: 10.1016/j.ejphar.2015.03.083. PubMed DOI

Elajami T.K., Colas R.A., Dalli J., Chiang N., Serhan C.N., Welty F.K. Specialized proresolving lipid mediators in patients with coronary artery disease and their potential for clot remodeling. FASEB J. 2016;30:2792–2801. doi: 10.1096/fj.201500155R. PubMed DOI PMC

Mottola G., Chatterjee A., Wu B., Chen M., Conte M.S. Aspirin-triggered resolvin D1 attenuates PDGF-induced vascular smooth muscle cell migration via the cyclic adenosine monophosphate/protein kinase A (cAMP/PKA) pathway. PLoS ONE. 2017;12:e0174936. doi: 10.1371/journal.pone.0174936. PubMed DOI PMC

Bennett M.R., Sinha S., Owens G.K. Vascular Smooth Muscle Cells in Atherosclerosis. Circ. Res. 2016;118:692–702. doi: 10.1161/CIRCRESAHA.115.306361. PubMed DOI PMC

Nakayama A., Albarrán-Juárez J., Liang G., Roquid K.A., Iring A., Tonack S., Chen M., Müller O.J., Weinstein L.S., Offermanns S. Disturbed flow–induced Gs-mediated signaling protects against endothelial inflammation and atherosclerosis. JCI Insight. 2020;5:140485. doi: 10.1172/jci.insight.140485. PubMed DOI PMC

Fredman G., Hellmann J., Proto J.D., Kuriakose G., Colas R.A., Dorweiler B., Connolly E.S., Solomon R., Jones D.M., Heyer E.J., et al. An imbalance between specialized pro-resolving lipid mediators and pro-inflammatory leukotrienes promotes instability of atherosclerotic plaques. Nat. Commun. 2016;7:12859. doi: 10.1038/ncomms12859. PubMed DOI PMC

Lee H.-N., Surh Y.-J. Resolvin D1-mediated NOX2 inactivation rescues macrophages undertaking efferocytosis from oxidative stress-induced apoptosis. Biochem. Pharmacol. 2013;86:759–769. doi: 10.1016/j.bcp.2013.07.002. PubMed DOI

Fredman G., Ozcan L., Spolitu S., Hellmann J., Spite M., Backs J., Tabas I. Resolvin D1 limits 5-lipoxygenase nuclear localization and leukotriene B4 synthesis by inhibiting a calcium-activated kinase pathway. Proc. Natl. Acad. Sci. USA. 2014;111:14530–14535. doi: 10.1073/pnas.1410851111. PubMed DOI PMC

Doran A.C., Yurdagul A., Tabas I. Efferocytosis in health and disease. Nat. Rev. Immunol. 2019;20:254–267. doi: 10.1038/s41577-019-0240-6. PubMed DOI PMC

Cai B., Thorp E.B., Doran A.C., Subramanian M., Sansbury B.E., Lin C.-S., Spite M., Fredman G., Tabas I. MerTK cleavage limits proresolving mediator biosynthesis and exacerbates tissue inflammation. Proc. Natl. Acad. Sci. USA. 2016;113:6526–6531. doi: 10.1073/pnas.1524292113. PubMed DOI PMC

Rymut N., Heinz J., Sadhu S., Hosseini Z., Riley C.O., Marinello M., Maloney J., MacNamara K.C., Spite M., Fredman G. Resolvin D1 promotes efferocytosis in aging by limiting senescent cell-induced MerTK cleavage. FASEB J. 2019;34:597–609. doi: 10.1096/fj.201902126R. PubMed DOI PMC

Hosseini Z., Marinello M., Decker C., Sansbury B.E., Sadhu S., Gerlach B.D., Ramos R.B., Adam A.P., Spite M., Fredman G. Resolvin D1 Enhances Necroptotic Cell Clearance Through Promoting Macrophage Fatty Acid Oxidation and Oxidative Phosphorylation. Arter. Thromb. Vasc. Biol. 2021;41:1062–1075. doi: 10.1161/ATVBAHA.120.315758. PubMed DOI PMC

Schif-Zuck S., Gross N., Assi S., Rostoker R., Serhan C.N., Ariel A. Saturated-efferocytosis generates pro-resolving CD11b low macrophages: Modulation by resolvins and glucocorticoids. Eur. J. Immunol. 2011;41:366–379. doi: 10.1002/eji.201040801. PubMed DOI PMC

Dalli J., Winkler J.W., Colas R.A., Arnardottir H., Cheng C.-Y.C., Chiang N., Petasis N.A., Serhan C.N. Resolvin D3 and Aspirin-Triggered Resolvin D3 Are Potent Immunoresolvents. Chem. Biol. 2013;20:188–201. doi: 10.1016/j.chembiol.2012.11.010. PubMed DOI PMC

Welty F.K., Schulte F., Alfaddagh A., Elajami T.K., Bistrian B.R., Hardt M. Regression of human coronary artery plaque is associated with a high ratio of (18-hydroxy-eicosapentaenoic acid + resolvin E1) to leukotriene B 4. FASEB J. 2021;35:e21448. doi: 10.1096/fj.202002471R. PubMed DOI PMC

Wu B., Mottola G., Schaller M., Upchurch G.R., Conte M.S. Resolution of vascular injury: Specialized lipid mediators and their evolving therapeutic implications. Mol. Asp. Med. 2017;58:72–82. doi: 10.1016/j.mam.2017.07.005. PubMed DOI PMC

Efremova O.A., Starodubov O.D., Kamyshnikova L.A., Bolkhovitina O.A., Obolonkova N.I. Clinical-functional changes of myocardium after percutaneous coronary interventions in patients with chronic heart failure. Lat. Hipertens. 2019;14:256–261.

Espinoza R., Arab G., Wiliam Z., Carrasquero L., Subero L., Colina R., Ana T., Jorge P., José T., Antonio V., et al. Evaluación de la incidencia de trombosis coronaria post Stent, posterior a la comercialización de segundas marcas de Clopidogrel. Hospital Miguel Pérez Carreño. Caracas. Venezuela. AVFT Arch. Venez. Farm. Ter. 2015;33:7–12.

Shah P.K. Inflammation, Neointimal Hyperplasia, and Restenosis. Circulation. 2003;107:2175–2177. doi: 10.1161/01.CIR.0000069943.41206.BD. PubMed DOI

Newby A.C., Zaltsman A.B. Molecular mechanisms in intimal hyperplasia. J. Pathol. 2000;190:300–309. doi: 10.1002/(SICI)1096-9896(200002)190:3<300::AID-PATH596>3.0.CO;2-I. PubMed DOI

Conte M.S., Desai T.A., Wu B., Schaller M., Werlin E. Pro-resolving lipid mediators in vascular disease. J. Clin. Investig. 2018;128:3727–3735. doi: 10.1172/JCI97947. PubMed DOI PMC

Liu G., Gong Y., Zhang R., Piao L., Li X., Liu Q., Yan S., Shen Y., Guo S., Zhu M., et al. Resolvin E1 attenuates injury-induced vascular neointimal formation by inhibition of inflammatory responses and vascular smooth muscle cell migration. FASEB J. 2018;32:5413–5425. doi: 10.1096/fj.201800173R. PubMed DOI

Petri M.H., Laguna-Fernandez A., Tseng C.-N., Hedin U., Perretti M., Bäck M. Aspirin-triggered 15-epi-lipoxin A4 signals through FPR2/ALX in vascular smooth muscle cells and protects against intimal hyperplasia after carotid ligation. Int. J. Cardiol. 2015;179:370–372. doi: 10.1016/j.ijcard.2014.11.010. PubMed DOI PMC

Akagi D., Chen M., Toy R., Chatterjee A., Conte M.S. Systemic delivery of proresolving lipid mediators resolvin D 2 and maresin 1 attenuates intimal hyperplasia in mice. FASEB J. 2015;29:2504–2513. doi: 10.1096/fj.14-265363. PubMed DOI PMC

Wu B., Mottola G., Chatterjee A., Lance K.D., Chen M., Siguenza I.O., Desai T.A., Conte M.S. Perivascular delivery of resolvin D1 inhibits neointimal hyperplasia in a rat model of arterial injury. J. Vasc. Surg. 2016;65:207–217.e3. doi: 10.1016/j.jvs.2016.01.030. PubMed DOI PMC

Yang M., Chen Q., Mei L., Wen G., An W., Zhou X., Niu K., Liu C., Ren M., Sun K., et al. Neutrophil elastase promotes neointimal hyperplasia by targeting toll-like receptor 4 (TLR4)-NF-κB signalling. Br. J. Pharmacol. 2021;178:4048–4068. doi: 10.1111/bph.15583. PubMed DOI

Li Y., Wang N., Ma Z., Wang Y., Yuan Y., Zhong Z., Hong Y., Zhao M. Lipoxin A4 protects against paraquat-induced acute lung injury by inhibiting the TLR4/MyD88-mediated activation of the NF-κB and PI3K/AKT pathways. Int. J. Mol. Med. 2021;47:86. doi: 10.3892/ijmm.2021.4919. PubMed DOI PMC

Liu Z., Qu M., Yang Q., Chang Y. Lipoxin A4 ameliorates renal ischaemia–reperfusion-induced acute lung injury in rats. Clin. Exp. Pharmacol. Physiol. 2019;46:65–74. doi: 10.1111/1440-1681.13023. PubMed DOI

Liu R., Li Z., Wang Q. Resolvin D1 Attenuates Myocardial Infarction in a Rodent Model with the Participation of the HMGB1 Pathway. Cardiovasc. Drugs Ther. 2019;33:399–406. doi: 10.1007/s10557-019-06884-y. PubMed DOI

Pan H., Xue C., Auerbach B.J., Fan J., Bashore A.C., Cui J., Yang D.Y., Trignano S.B., Liu W., Shi J., et al. Single-Cell Genomics Reveals a Novel Cell State During Smooth Muscle Cell Phenotypic Switching and Potential Therapeutic Targets for Atherosclerosis in Mouse and Human. Circulation. 2020;142:2060–2075. doi: 10.1161/CIRCULATIONAHA.120.048378. PubMed DOI PMC

Feil S., Fehrenbacher B., Lukowski R., Essmann F., Schulze-Osthoff K., Schaller M., Feil R. Transdifferentiation of Vascular Smooth Muscle Cells to Macrophage-Like Cells During Atherogenesis. Circ. Res. 2014;115:662–667. doi: 10.1161/CIRCRESAHA.115.304634. PubMed DOI

Yang J., Li M., Hu X., Lu J., Wang Q., Lu S., Gao F., Jin S., Zheng S. Protectin DX promotes epithelial injury repair and inhibits fibroproliferation partly via ALX/PI3K signalling pathway. J. Cell. Mol. Med. 2020;24:14001–14012. doi: 10.1111/jcmm.16011. PubMed DOI PMC

Zheng S., Wang Q., D’Souza V., Bartis D., Dancer R., Parekh D., Gao F., Lian Q., Jin S., Thickett D.R. ResolvinD1 stimulates epithelial wound repair and inhibits TGF-β-induced EMT whilst reducing fibroproliferation and collagen production. Lab. Investig. 2018;98:130–140. doi: 10.1038/labinvest.2017.114. PubMed DOI PMC

Zheng S., D’Souza V.K., Bartis D., Dancer R.C., Parekh D., Naidu B., Gao-Smith F., Wang Q., Jin S., Lian Q., et al. Lipoxin A4promotes lung epithelial repair whilst inhibiting fibroblast proliferation. ERJ Open Res. 2016;2:00079–02015. doi: 10.1183/23120541.00079-2015. PubMed DOI PMC

Frank A., Bonney M., Bonney S., Weitzel L., Koeppen M., Eckle T. Myocardial ischemia reperfusion injury: From basic science to clinical bedside. Semin. Cardiothorac. Vasc. Anesth. 2012;16:123–132. doi: 10.1177/1089253211436350. PubMed DOI PMC

Bermúdez Arias D.F. La recuperación del miocardio hibernado mejora el pronóstico de la cardiopatía isquémica metabólica. Gac. Médica Caracas. 2020;113:19–41.

Wu M.-Y., Yiang G.-T., Liao W.-T., Tsai A.P.Y., Cheng Y.-L., Cheng P.-W., Li C.-Y., Li C.J. Current Mechanistic Concepts in Ischemia and Reperfusion Injury. Cell. Physiol. Biochem. 2018;46:1650–1667. doi: 10.1159/000489241. PubMed DOI

Chen Z., Wu Z., Huang C., Zhao Y., Zhou Y., Zhou X., Lu X., Mao L., Li S. Effect of Lipoxin A4 on Myocardial Ischemia Reperfusion Injury Following Cardiac Arrest in a Rabbit Model. Inflammation. 2013;36:468–475. doi: 10.1007/s10753-012-9567-x. PubMed DOI

Chen X.-Q., Wu S.-H., Zhou Y., Tang Y.-R. Involvement of K+ channel-dependant pathways in lipoxin A4-induced protective effects on hypoxia/reoxygenation injury of cardiomyocytes. Prostaglandins Leukot. Essent. Fat. Acids. 2013;88:391–397. doi: 10.1016/j.plefa.2013.03.007. PubMed DOI

Zheng J., Chen P., Zhong J., Cheng Y., Chen H., He Y., Chen C. HIF-1α in myocardial ischemia-reperfusion injury. Mol. Med. Rep. 2021;23:352. doi: 10.3892/mmr.2021.11991. PubMed DOI PMC

Zhao Q., Shao L., Hu X., Wu G., Du J., Xia J., Qiu H. Lipoxin A4Preconditioning and Postconditioning Protect Myocardial Ischemia/Reperfusion Injury in Rats. Mediat. Inflamm. 2013;2013:e231351. doi: 10.1155/2013/231351. PubMed DOI PMC

Cheng Y., Rong J. Pro-resolving lipid mediators as therapeutic leads for cardiovascular diseases. Expert Opin. Ther. Targets. 2019;23:423–436. doi: 10.1080/14728222.2019.1599360. PubMed DOI

Halade G.V., Norris P.C., Kain V., Serhan C.N., Ingle K.A. Splenic leukocytes define the resolution of inflammation in heart failure. Sci. Signal. 2018;11:eaao1818. doi: 10.1126/scisignal.aao1818. PubMed DOI PMC

Halade G.V., Kain V., Dillion C., Beasley M., Dudenbostel T., Oparil S., Limdi N.A. Race-based and sex-based differences in bioactive lipid mediators after myocardial infarction. ESC Heart Fail. 2020;7:1700–1710. doi: 10.1002/ehf2.12730. PubMed DOI PMC

Tourki B., Kain V., Pullen A.B., Norris P.C., Patel N., Arora P., Leroy X., Serhan C.N., Halade G.V. Lack of resolution sensor drives age-related cardiometabolic and cardiorenal defects and impedes inflammation-resolution in heart failure. Mol. Metab. 2020;31:138–149. doi: 10.1016/j.molmet.2019.10.008. PubMed DOI PMC

Keyes K.T., Ye Y., Lin Y., Zhang C., Perez-Polo J.R., Gjorstrup P., Birnbaum Y. Resolvin E1 protects the rat heart against reperfusion injury. Am. J. Physiol. Circ. Physiol. 2010;299:H153–H164. doi: 10.1152/ajpheart.01057.2009. PubMed DOI

Gilbert K., Bernier J., Godbout R., Rousseau G. Resolvin D1, a Metabolite of Omega-3 Polyunsaturated Fatty Acid, Decreases Post-Myocardial Infarct Depression. Mar. Drugs. 2014;12:5396–5407. doi: 10.3390/md12115396. PubMed DOI PMC

Gilbert K., Bernier J., Bourque-Riel V., Malick M., Rousseau G. Resolvin D1 Reduces Infarct Size Through a Phosphoinositide 3-Kinase/Protein Kinase B Mechanism. J. Cardiovasc. Pharmacol. 2015;66:72–79. doi: 10.1097/FJC.0000000000000245. PubMed DOI

Kain V., Ingle K.A., Colas R.A., Dalli J., Prabhu S.D., Serhan C.N., Joshi M.D., Halade G.V. Resolvin D1 activates the inflammation resolving response at splenic and ventricular site following myocardial infarction leading to improved ventricular function. J. Mol. Cell. Cardiol. 2015;84:24–35. doi: 10.1016/j.yjmcc.2015.04.003. PubMed DOI PMC

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. Cell. Mol. Physiol. 2015;308:L904–L911. doi: 10.1152/ajplung.00370.2014. PubMed DOI PMC

Pirault J., Bäck M. Lipoxin and Resolvin Receptors Transducing the Resolution of Inflammation in Cardiovascular Disease. Front. Pharmacol. 2018;9:1273. doi: 10.3389/fphar.2018.01273. PubMed DOI PMC

Sánchez-Hernández C.D., Torres-Alarcón L.A., González-Cortés A., Peón A.N. Ischemia/Reperfusion Injury: Pathophysiology, Current Clinical Management, and Potential Preventive Approaches. Mediat. Inflamm. 2020;2020:e8405370. doi: 10.1155/2020/8405370. PubMed DOI PMC

Heinz J., Marinello M., Fredman G. Pro-resolution therapeutics for cardiovascular diseases. Prostaglandins Other Lipid Mediat. 2017;132:12–16. doi: 10.1016/j.prostaglandins.2017.03.004. PubMed DOI

Ayala J., López C., Hong A., Oberto C., Paiva A., Lares M. Efecto de los ácidos grasos poliinsaturados (omega 3) sobre la agregación plaquetaria. Lat. Hipertens. 2009;4:71–78.

Hasturk H., Abdallah R., Kantarci A., Nguyen D., Giordano N., Hamilton J., Van Dyke T.E. Resolvin E1 (RvE1) Attenuates Atherosclerotic Plaque Formation in Diet and Inflammation-Induced Atherogenesis. Arter. Thromb. Vasc. Biol. 2015;35:1123–1133. doi: 10.1161/ATVBAHA.115.305324. PubMed DOI PMC

Salic K., Morrison M.C., Verschuren L., Wielinga P.Y., Wu L., Kleemann R., Gjorstrup P., Kooistra T. Resolvin E1 attenuates atherosclerosis in absence of cholesterol-lowering effects and on top of atorvastatin. Atherosclerosis. 2016;250:158–165. doi: 10.1016/j.atherosclerosis.2016.05.001. PubMed DOI

Petri M.H., Laguna-Fernandez A., Arnardottir H., Wheelock C.E., Perretti M., Hansson G.K., Bäck M. Aspirin-triggered lipoxin A4 inhibits atherosclerosis progression in apolipoprotein E-/- mice. Br. J. Pharmacol. 2017;174:4043–4054. doi: 10.1111/bph.13707. PubMed DOI PMC

Makino Y., Miyahara T., Nitta J., Miyahara K., Seo A., Kimura M., Suhara M., Akai A., Akagi D., Yamamoto K., et al. Proresolving Lipid Mediators Resolvin D1 and Protectin D1 Isomer Attenuate Neointimal Hyperplasia in the Rat Carotid Artery Balloon Injury Model. J. Surg. Res. 2019;233:104–110. doi: 10.1016/j.jss.2018.07.049. PubMed DOI

Thul S., Labat C., Temmar M., Benetos A., Bäck M. Low salivary resolvin D1 to leukotriene B4 ratio predicts carotid intima media thickness: A novel biomarker of non-resolving vascular inflammation. Eur. J. Prev. Cardiol. 2017;24:903–906. doi: 10.1177/2047487317694464. PubMed DOI

Bhatt D.L., Steg P.G., Miller M., Brinton E.A., Jacobson T.A., Ketchum S.B., Doyle R.T., Jr., Juliano R.A., Jiao L., Granowitz C., et al. Cardiovascular Risk Reduction with Icosapent Ethyl for Hypertriglyceridemia. N. Engl. J. Med. 2019;380:11–22. doi: 10.1056/NEJMoa1812792. PubMed DOI

Gromovsky A.D., Schugar R.C., Brown A.L., Helsley R.N., Burrows A.C., Ferguson D., Zhang R., Sansbury B.E., Lee R.G., Morton R.E., et al. Δ-5 Fatty Acid Desaturase FADS1 Impacts Metabolic Disease by Balancing Proinflammatory and Proresolving Lipid Mediators. Arter. Thromb. Vasc. Biol. 2018;38:218–231. doi: 10.1161/ATVBAHA.117.309660. PubMed DOI PMC

Skarke C., Alamuddin N., Lawson J.A., Li X., Ferguson J.F., Reilly M.P., FitzGerald G.A. Bioactive products formed in humans from fish oils. J. Lipid Res. 2015;56:1808–1820. doi: 10.1194/jlr.M060392. PubMed DOI PMC

Bäck M., Yurdagul A., Jr., Tabas I., Öörni K., Kovanen P.T. Inflammation and its resolution in atherosclerosis: Mediators and therapeutic opportunities. Nat. Rev. Cardiol. 2019;16:389–406. doi: 10.1038/s41569-019-0169-2. PubMed DOI PMC

Zhou X., Cai J., Liu W., Wu X., Gao C. Cysteinyl leukotriene receptor type 1 (CysLT1R) antagonist zafirlukast protects against TNF-α-induced endothelial inflammation. Biomed. Pharmacother. 2019;111:452–459. doi: 10.1016/j.biopha.2018.12.064. PubMed DOI

Medina-Leyte D., Zepeda-García O., Domínguez-Pérez M., González-Garrido A., Villarreal-Molina T., Jacobo-Albavera L. Endothelial Dysfunction, Inflammation and Coronary Artery Disease: Potential Biomarkers and Promising Therapeutical Approaches. Int. J. Mol. Sci. 2021;22:3850. doi: 10.3390/ijms22083850. PubMed DOI PMC

Ridker P.M., Everett B.M., Thuren T., MacFadyen J.G., Chang W.H., Ballantyne C., Fonseca F., Nicolau J., Koenig W., Anker S.D., et al. Antiinflammatory Therapy with Canakinumab for Atherosclerotic Disease. N. Engl. J. Med. 2017;377:1119–1131. doi: 10.1056/NEJMoa1707914. PubMed DOI

Ridker P.M., Everett B.M., Pradhan A., MacFadyen J.G., Solomon D.H., Zaharris E., Mam V., Hasan A., Rosenberg Y., Iturriaga E., et al. Low-Dose Methotrexate for the Prevention of Atherosclerotic Events. N. Engl. J. Med. 2019;380:752–762. doi: 10.1056/NEJMoa1809798. PubMed DOI PMC

Chávez-Castillo M., Ortega A., Cudris-Torres L., Duran P., Rojas M., Manzano A., Garrido B., Salazar J., Silva A., Rojas-Gomez D.M., et al. Specialized Pro-Resolving Lipid Mediators: The Future of Chronic Pain Therapy? Int. J. Mol. Sci. 2021;22:10370. doi: 10.3390/ijms221910370. PubMed DOI PMC

Gila-Diaz A., Carrillo G., Singh P., Ramiro-Cortijo D. Specialized Pro-Resolving Lipid Mediators in Neonatal Cardiovascular Physiology and Diseases. Antioxidants. 2021;10:933. doi: 10.3390/antiox10060933. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...