Abstract
Atrial fibrillation (AF) is the most common type of cardiac rhythm disturbance. At the cellular level, excessive ROS generation during AF is associated with ER stress, which induces an inflammatory response by activating the unfolded protein response (UPR) pathway and the nuclear factor-kappa B (NF-kB) signaling pathway. Activation of the NLR family pyrin domain containing 3 (NLRP3) inflammasome has been linked to the pathogenesis of AF through NF-kB activation and inflammatory cytokine secretion. It has been shown that NLRP3 inflammasome activation by endoplasmic reticulum (ER) stress is dependent on NF-kB activation. The anti-inflammatory role of resolvin D1 (RvD1), a pro-resolving mediator derived from omega-3 fatty acids, has demonstrated that the NF-κB/NLRP3 inflammasome pathway in different tissues is attenuated after treatment with RvD1. However, the mechanism of the anti-inflammatory activity of RvD1 in AF has not been clarified. This review suggests that RvD1 may inhibit ER stress-induced NLRP3 inflammasome through suppressing NF-κB in cardiac tissue and, thus ameliorate AF.
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Abbreviations
- ASC:
-
Apoptosis-associated speck-like protein
- AF:
-
Atrial fibrillation
- ATF6:
-
Activating transcription factor 6
- CAS1:
-
Caspase 1
- CD68:
-
Cluster of differentiation 68
- CHOP:
-
C/EBP homologous protein
- DHA:
-
Docosahexaenoic acid
- eIF2α:
-
Eukaryotic translation initiation factor 2 alpha
- ER:
-
Endoplasmic reticulum
- EPA:
-
Eicosapentaenoic acid
- ESRD:
-
End-stage renal disease
- FPR2:
-
Formyl peptide receptor 2
- GPCRs:
-
Specific G protein-coupled receptors
- GPR32:
-
G protein-coupled receptor 32
- GRP78:
-
78 KDa glucose-regulated protein
- hHcys:
-
Hyperhomocysteinemia
- HFD:
-
High-fat diet
- Icam1 :
-
Intercellular adhesion molecule 1
- IκB:
-
Inhibitors of NF-κB
- IKK:
-
IκB kinase
- IL:
-
Interleukin
- I/R injury:
-
Ischemia/reperfusion injury
- IRE1α:
-
Inositol requiring enzyme 1 alpha
- NF-κB:
-
Nuclear factor-kappa B
- NLRP3:
-
NLR family pyrin domain containing 3
- PERK:
-
Protein kinase RNA (PKR)-like kinase
- ROS:
-
Reactive oxygen species
- RvD1:
-
Resolvin D1
- Rvs:
-
Resolvins
- SAH:
-
Subarachnoid hemorrhage
- SPMs:
-
Specialized pro-resolving mediators
- Socs3:
-
Suppressor of cytokine signaling 3
- TAK1:
-
TGF-β-activated kinase 1
- TLRs:
-
Toll-like receptors
- TNF-α:
-
Tumor necrosis factor-alpha
- TRAF2:
-
Tumor necrosis factor receptor-associated factor 2
- UPR:
-
Unfolded protein response
- XBP1:
-
X-box-binding protein 1
- ω-3PUFAs:
-
The omega-3 polyunsaturated fatty acids
References
Abdolmaleki F, Kovanen PT, Mardani R et al (2020) Resolvins: emerging players in autoimmune and inflammatory diseases. Clin Rev Allergy Immunol 58:82–91. https://doi.org/10.1007/s12016-019-08754-9
Almanza A, Carlesso A, Chintha C et al (2019) Endoplasmic reticulum stress signalling–from basic mechanisms to clinical applications. FEBS J 286:241–278. https://doi.org/10.1111/febs.14608
Antonetti DA, Barber AJ, Bronson SK et al (2006) Diabetic retinopathy: seeing beyond glucose-induced microvascular disease. Diabetes 55:2401–2411
Barangi S, Hayes AW, Karimi G (2018) The more effective treatment of atrial fibrillation applying the natural compounds; as NADPH oxidase and ion channel inhibitors. Crit Rev Food Sci Nutr 58:1230–1241. https://doi.org/10.1080/10408398.2017.1379000
Bruchard M, Rebé C, Derangère V et al (2015) The receptor NLRP3 is a transcriptional regulator of TH 2 differentiation. Nat Immunol 16:859–870. https://doi.org/10.1038/ni.3202
Cao D, Pi J, Shan Y et al (2018) Anti-inflammatory effect of Resolvin D1 on LPS-treated MG-63 cells. Exp Ther Med 16:4283–4288. https://doi.org/10.3892/etm.2018.6721
Chen JJ, Chen J, Jiang ZX, et al (2020) Resolvin D1 alleviates cerebral ischemia/reperfusion injury in rats by inhibiting NLRP3 signaling pathway. J Biol Regul Homeost Agents 34:. https://doi.org/10.23812/20-392-A
Chen X, Zhuo S, Zhu T et al (2019) Fpr2 deficiency alleviates diet-induced insulin resistance through reducing body weight gain and inhibiting inflammation mediated by macrophage chemotaxis and M1 polarization. Diabetes 68:1130–1142. https://doi.org/10.2337/db18-0469
Dartt DA, Hodges RR, Serhan CN (2019) Immunoresolvent resolvin D1 maintains the health of the ocular surface. Adv Exp Med Biol 1161:13–25. https://doi.org/10.1007/978-3-030-21735-8_3
Freundt JK, Frommeyer G, Wötzel F et al (2018) The transcription factor ATF4 promotes expression of cell stress genes and cardiomyocyte death in a cellular model of atrial fibrillation. Biomed Res Int 2018:3694362. https://doi.org/10.1155/2018/3694362
Giacomello M, Pyakurel A, Glytsou C, Scorrano L (2020) The cell biology of mitochondrial membrane dynamics. Nat Rev Mol Cell Biol 21:204–224. https://doi.org/10.1038/s41580-020-0210-7
Gilbert K, Bernier J, Bourque-Riel V et al (2015) Resolvin D1 reduces infarct size through a phosphoinositide 3-kinase/protein kinase B mechanism. J Cardiovasc Pharmacol 66:72–79
Hamatani Y, Ogawa H, Takabayashi K et al (2016) Left atrial enlargement is an independent predictor of stroke and systemic embolism in patients with non-valvular atrial fibrillation. Sci Rep 6:1–8. https://doi.org/10.1038/srep31042
Harada M, Van Wagoner DR, Nattel S (2015) Role of inflammation in atrial fibrillation pathophysiology and management. Circ J 79:495–502. https://doi.org/10.1253/circj.CJ-15-0138
Hiram R, Xiong F, Naud P et al (2020) The inflammation-resolution promoting molecule resolvin-D1 prevents atrial proarrhythmic remodeling in experimental right heart disease. Cardiovasc Res. https://doi.org/10.1093/cvr/cvaa186
Hsiao H-M, Thatcher TH, Levy EP et al (2014) Resolvin D1 attenuates polyinosinic-polycytidylic acid–induced inflammatory signaling in human airway epithelial cells via TAK1. J Immunol 193:4980–4987
Huang H, Zhao N, Xu X et al (2011) Dose-specific effects of tumor necrosis factor alpha on osteogenic differentiation of mesenchymal stem cells. Cell Prolif 44:420–427
Jeganathan J, Saraf R, Mahmood F et al (2017) Mitochondrial dysfunction in atrial tissue of patients developing postoperative atrial fibrillation. Ann Thorac Surg 104:1547–1555. https://doi.org/10.1016/j.athoracsur.2017.04.060
Kain V, Jadapalli JK, Tourki B, Halade GV (2019) Inhibition of FPR2 impaired leukocytes recruitment and elicited non-resolving inflammation in acute heart failure. Pharmacol Res 146:104295. https://doi.org/10.1016/j.phrs.2019.104295
Karam BS, Chavez-Moreno A, Koh W et al (2017) Oxidative stress and inflammation as central mediators of atrial fibrillation in obesity and diabetes. Cardiovasc Diabetol 16:1–9. https://doi.org/10.1186/s12933-017-0604-9
Kelley N, Jeltema D, Duan Y, He Y (2019) The NLRP3 inflammasome: an overview of mechanisms of activation and regulation. Int J Mol Sci 20:3328. https://doi.org/10.3390/ijms20133328
Li C, Wu X, Liu S et al (2020a) Role of resolvins in the inflammatory resolution of neurological diseases. Front Pharmacol 11:612
Li G, Chen Z, Bhat OM et al (2017) NLRP3 inflammasome as a novel target for docosahexaenoic acid metabolites to abrogate glomerular injury. J Lipid Res 58:1080–1090. https://doi.org/10.1194/jlr.M072587
Li N, Brundel BJJM (2020) Inflammasomes and proteostasis novel molecular mechanisms associated with atrial fibrillation. Circ Res 127:73–90
Li W, Cao T, Luo C et al (2020b) Crosstalk between ER stress, NLRP3 inflammasome, and inflammation. Appl Microbiol Biotechnol 104:6129–6140. https://doi.org/10.1007/s00253-020-10614-y
Liu R, Li Z, Wang Q (2019) Resolvin D1 attenuates myocardial infarction in a rodent model with the participation of the HMGB1 pathway. Cardiovasc Drugs Ther 33:399–406
Macdonald RL, Schweizer TA (2017) Spontaneous subarachnoid haemorrhage. Lancet 389:655–666
Martella BM, Veiga GRL, Alves BCA et al (2018) The importance of homocysteine levels in the prognosis of patients with chronic renal disease and in hemodialysis patients. J Bras Patol e Med Lab 54:170–176
Mason FE, Pronto JRD, Alhussini K et al (2020) Cellular and mitochondrial mechanisms of atrial fibrillation. Basic Res Cardiol 115:1–16. https://doi.org/10.1007/s00395-020-00827-7
Nso N, Bookani KR, Metzl M, Radparvar F (2021) Role of inflammation in atrial fibrillation: a comprehensive review of current knowledge. J Arrhythmia 37:1–10. https://doi.org/10.1002/joa3.12473
Ren J, Bi Y, Sowers JR, et al (2021) Endoplasmic reticulum stress and unfolded protein response in cardiovascular diseases. Nat Rev Cardiol 1–23https://doi.org/10.1038/s41569-021-00511-w
Scott LJ, Fender AC, Saljic A et al (2021) NLRP3 inflammasome is a key driver of obesity-induced atrial arrhythmias. Cardiovasc Res 117:1746–1759. https://doi.org/10.1093/cvr/cvab024
Sugimoto MA, Vago JP, Perretti M, Teixeira MM (2019) Mediators of the resolution of the inflammatory response. Trends Immunol 40:212–227. https://doi.org/10.1016/j.it.2019.01.007
Sullivan GP, O’Connor H, Henry CM et al (2020) TRAIL receptors serve as stress-associated molecular patterns to promote ER-stress-induced inflammation. Dev Cell 52:714-730.e5. https://doi.org/10.1016/j.devcel.2020.01.031
Sun Y-P, Oh SF, Uddin J et al (2007) Resolvin D1 and its aspirin-triggered 17R epimer: stereochemical assignments, anti-inflammatory properties, and enzymatic inactivation. J Biol Chem 282:9323–9334
Swanson KV, Deng M, Ting JPY (2019) The NLRP3 inflammasome: molecular activation and regulation to therapeutics. Nat Rev Immunol 19:477–489. https://doi.org/10.1038/s41577-019-0165-0
Trojan E, Bryniarska N, Leśkiewicz M et al (2020) The contribution of formyl peptide receptor dysfunction to the course of neuroinflammation: a potential role in the brain pathology. Curr Neuropharmacol 18:229–249
Wei C, Guo S, Liu W et al (2020) Resolvin D1 ameliorates inflammation-mediated blood-brain barrier disruption after subarachnoid hemorrhage in rats by modulating A20 and NLRP3 inflammasome. Front Pharmacol 11:610734. https://doi.org/10.3389/fphar.2020.610734
Wiersma M, Meijering RAM, Qi X-Y et al (2017) Endoplasmic reticulum stress is associated with autophagy and cardiomyocyte remodeling in experimental and human atrial fibrillation. J Am Heart Assoc 6(10):e006458. https://doi.org/10.1161/JAHA.117.006458
Yao C, Veleva T, Scott L Jr et al (2018) Enhanced cardiomyocyte NLRP3 inflammasome signaling promotes atrial fibrillation. Circulation 138:2227–2242. https://doi.org/10.1161/CIRCULATIONAHA.118.035202
Yarmohammadi F, Rezaee R, Haye AW, Karimi G (2021) Endoplasmic reticulum stress in doxorubicin-induced cardiotoxicity may be therapeutically targeted by natural and chemical compounds: a review. Pharmacol Res 164:105383. https://doi.org/10.1016/j.phrs.2020.105383
Yin Y, Chen F, Wang W et al (2017) Resolvin D1 inhibits inflammatory response in STZ-induced diabetic retinopathy rats: possible involvement of NLRP3 inflammasome and NF-κB signaling pathway. Mol vis 23:242–250
Yuan M, Gong M, Zhang Z et al (2020) Hyperglycemia induces endoplasmic reticulum stress in atrial cardiomyocytes, and mitofusin-2 downregulation prevents mitochondrial dysfunction and subsequent cell death. Oxid Med Cell Longev 2020:6569728. https://doi.org/10.1155/2020/6569728
Zhang X, Jing W (2018) Upregulation of miR-122 is associated with cardiomyocyte apoptosis in atrial fibrillation. Mol Med Rep 18:1745–1751. https://doi.org/10.3892/mmr.2018.9124
Zhang Y, Yang S, Fu J et al (2020) Inhibition of endoplasmic reticulum stress prevents high-fat diet mediated atrial fibrosis and fibrillation. J Cell Mol Med 24:13660–13668
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The authors are thankful to Mashhad University of Medical Sciences for financial support.
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GhK conceived and designed research; GhK and AWH revised and edited the manuscript; FY wrote the manuscript; All authors read and approved the final version of the manuscript. The authors declare that all data were generated in-house and that no paper mill was used.
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Yarmohammadi, F., Hayes, A.W. & Karimi, G. Possible protective effect of resolvin D1 on inflammation in atrial fibrillation: involvement of ER stress mediated the NLRP3 inflammasome pathway. Naunyn-Schmiedeberg's Arch Pharmacol 394, 1613–1619 (2021). https://doi.org/10.1007/s00210-021-02115-0
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DOI: https://doi.org/10.1007/s00210-021-02115-0