Dietary Fish Oil Increases the Number of CD11b⁺CD27⁻ NK Cells at the Inflammatory Site and Enhances Key Hallmarks of Resolution of Murine Antigen-Induced Peritonitis

References

• Headland SE, Norling LV. The resolution of inflammation: principles and challenges. Semin Immunol. 2015;27(3):149–160. doi:10.1016/j.smim.2015.03.014
   PubMed Web of Science ®Google Scholar
• Fullerton JN, Gilroy DW. Resolution of inflammation: a new therapeutic frontier. Nat Rev Drug Discov. 2016;15(8):551–567. doi:10.1038/nrd.2016.39
   PubMed Web of Science ®Google Scholar
• Sugimoto MA, Vago JP, Perretti M, Teixeira MM. Mediators of the resolution of the inflammatory response. Trends Immunol. 2019;40(3):212–227. doi:10.1016/j.it.2019.01.007
   PubMed Web of Science ®Google Scholar
• Serhan CN, Chiang N, Dalli J, Levy BD. Lipid mediators in the resolution of inflammation. Cold Spring Harb Perspect Biol. 2015;7(2):a016311. doi:10.1101/cshperspect.a016311
   Web of Science ®Google Scholar
• Chiurchiù V, Leuti A, Maccarrone M. Bioactive lipids and chronic inflammation: managing the fire within. Front Immunol. 2018;9(38). doi:10.3389/fimmu.2018.00038
   PubMed Web of Science ®Google Scholar
• Coghill AE, Schenk JM, Mahkoul Z, Orem J, Phipps W, Casper C. Omega-3 decreases IL-6 levels in HIV and human herpesvirus-8 coinfected patients in Uganda. AIDS. 2018;32(4):505–512. doi:10.1097/qad.0000000000001722
   PubMed Web of Science ®Google Scholar
• Yates CM, Calder PC, Ed Rainger G. Pharmacology and therapeutics of omega-3 polyunsaturated fatty acids in chronic inflammatory disease. Pharmacol Ther. 2014;141(3):272–282. doi:10.1016/j.pharmthera.2013.10.010
   PubMed Web of Science ®Google Scholar
• Thomson CA, McColl A, Graham GJ, Cavanagh J. Sustained exposure to systemic endotoxin triggers chemokine induction in the brain followed by a rapid influx of leukocytes. J Neuroinflammation. 2020;17(1). doi:10.1186/s12974-020-01759-8
   Web of Science ®Google Scholar
• Lawrence DW, King SB, Frazier WA, Koenig JM. Decreased CD47 expression during spontaneous apoptosis targets neutrophils for phagocytosis by monocyte-derived macrophages. Early Hum Dev. 2009;85(10):659–663. doi:10.1016/j.earlhumdev.2009.09.005
   PubMed Web of Science ®Google Scholar
• Barrera L, Montes-Servín E, Hernandez-Martinez J-M, et al. CD47 overexpression is associated with decreased neutrophil apoptosis/phagocytosis and poor prognosis in non-small-cell lung cancer patients. Br J Cancer. 2017;117(3):385–397. doi:10.1038/bjc.2017.173
   PubMed Web of Science ®Google Scholar
• Liu Y, Merlin D, Burst SL, Pochet M, Madara JL, Parkos CA. The role of CD47 in neutrophil transmigration. J Biol Chem. 2001;276(43):40156–40166. doi:10.1074/jbc.m104138200
   PubMed Web of Science ®Google Scholar
• Innes JK, Calder PC. Omega-6 fatty acids and inflammation. Prostaglandins Leukot Essent Fatty Acids. 2018;132:41–48. doi:10.1016/j.plefa.2018.03.004
   PubMed Web of Science ®Google Scholar
• Furman D, Campisi J, Verdin E, et al. Chronic inflammation in the etiology of disease across the life span. Nat Med. 2019;25(12):1822–1832. doi:10.1038/s41591-019-0675-0
   PubMed Web of Science ®Google Scholar
• Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol. 2008;9(5):503–510. doi:10.1038/ni1582
   PubMed Web of Science ®Google Scholar
• Chiossone L, Chaix J, Fuseri N, Roth C, Vivier E, Walzer T. Maturation of mouse NK cells is a 4-stage developmental program. Blood. 2009;113(22):5488–5496. doi:10.1182/blood-2008-10-187179
   PubMed Web of Science ®Google Scholar
• Abel AM, Yang C, Thakar MS, Malarkannan S. Natural killer cells: development, maturation, and clinical utilization. Front Immunol. 2018;9. doi:10.3389/fimmu.2018.01869
   Web of Science ®Google Scholar
• Kim S, Iizuka K, Kang H-SP, et al. In vivo developmental stages in murine natural killer cell maturation. Nat Immunol. 2002;3(6):523–528. doi:10.1038/ni796
   PubMed Web of Science ®Google Scholar
• Robertson MJ. Role of chemokines in the biology of natural killer cells. J Leukoc Biol. 2002;71:10. doi:10.1189/jlb.71.2.173
   Web of Science ®Google Scholar
• Zou Z, Zuo D, Yang J, Fan H. The ANXA1 released from intestinal epithelial cells alleviate DSS-induced colitis by improving NKG2A expression of natural killer cells. Biochem Biophys Res Commun. 2016;478(1):213–220. doi:10.1016/j.bbrc.2016.07.066
   PubMed Web of Science ®Google Scholar
• Haworth O, Cernadas M, Levy BD. NK cells are effectors for resolvin E1 in the timely resolution of allergic airway inflammation. J Immunol. 2011;186(11):6129–6135. doi:10.4049/jimmunol.1004007
   PubMed Web of Science ®Google Scholar
• Anuforo OUU, Bjarnarson SP, Jonasdottir HS, Giera M, Hardardottir I, Freysdottir J. Natural killer cells play an essential role in resolution of antigen-induced inflammation in mice. Mol Immunol. 2018;93:1–8. doi:10.1016/j.molimm.2017.10.019
   PubMed Web of Science ®Google Scholar
• Semeraro ML, Glenn LM, Morris MA. The four-way stop sign: viruses, 12-lipoxygenase, islets, and natural killer cells in type 1 diabetes progression. Front Endocrinol (Lausanne). 2017;8:246. doi:10.3389/fendo.2017.00246
   PubMed Web of Science ®Google Scholar
• Calder PC. Session 3: Joint Nutrition Society and Irish Nutrition and Dietetic Institute Symposium on ‘Nutrition and autoimmune disease’ PUFA, inflammatory processes and rheumatoid arthritis. Proc Nutr Soc. 2008;67(4):409–418. doi:10.1017/s0029665108008690
   PubMed Web of Science ®Google Scholar
• Calder PC. Polyunsaturated fatty acids, inflammatory processes and inflammatory bowel diseases. Mol Nutr Food Res. 2008;52(8):885–897. doi:10.1002/mnfr.200700289
   PubMed Web of Science ®Google Scholar
• Tomasdottir V, Vikingsson A, Freysdottir J, Hardardottir I. Dietary fish oil reduces the acute inflammatory response and enhances resolution of antigen-induced peritonitis. J Nutr Biochem. 2013;24(10):1758–1765. doi:10.1016/j.jnutbio.2013.03.005
   PubMed Web of Science ®Google Scholar
• Kong W, Yen J-H, Ganea D. Docosahexaenoic acid prevents dendritic cell maturation, inhibits antigen-specific Th1/Th17 differentiation and suppresses experimental autoimmune encephalomyelitis. Brain Behav Immun. 2011;25(5):872–882. doi:10.1016/j.bbi.2010.09.012
   PubMed Web of Science ®Google Scholar
• Jensen KN, Omarsdottir SY, Reinhardsdottir MS, Hardardottir I, Freysdottir J. docosahexaenoic acid modulates nk cell effects on neutrophils and their crosstalk. Front Immunol. 2020;11. doi:10.3389/fimmu.2020.570380
   Web of Science ®Google Scholar
• Arnardottir HH, Freysdottir J, Hardardottir I. Dietary fish oil decreases the proportion of classical monocytes in blood in healthy mice but increases their proportion upon induction of inflammation. J Nutr. 2012;142(4):803–808. doi:10.3945/jn.111.153221
   PubMed Web of Science ®Google Scholar
• Calder PC. Marine omega-3 fatty acids and inflammatory processes: effects, mechanisms and clinical relevance. Biochim Biophys Acta Mol Cell Biol Lipids. 2015;1851(4):469–484. doi:10.1016/j.bbalip.2014.08.010
   PubMed Web of Science ®Google Scholar
• Körner A, Zhou E, Müller C, et al. Inhibition of Δ24-dehydrocholesterol reductase activates pro-resolving lipid mediator biosynthesis and inflammation resolution. Proc Natl Acad Sci U S A. 2019;116(41):20623–20634. doi:10.1073/pnas.1911992116
   PubMed Web of Science ®Google Scholar
• Martín-Fontecha A, Thomsen LL, Brett S, et al. Induced recruitment of NK cells to lymph nodes provides IFN-γ for TH1 priming. Nat Immunol. 2004;5(12):1260–1265. doi:10.1038/ni1138
   PubMed Web of Science ®Google Scholar
• Alter G, Malenfant JM, Altfeld M. CD107a as a functional marker for the identification of natural killer cell activity. J Immunol Methods. 2004;294(1–2):15–22. doi:10.1016/j.jim.2004.08.008
   PubMed Web of Science ®Google Scholar
• Chin AC, Fournier B, Peatman EJ, Reaves TA, Lee WY, Parkos CA. CD47 and TLR-2 cross-talk regulates neutrophil transmigration. J Immunol. 2009;183(9):5957–5963. doi:10.4049/jimmunol.0900789
   PubMed Web of Science ®Google Scholar
• Navarathna DH, Stein EV, Lessey-Morillon EC, Nayak D, Martin-Manso G, Roberts DD. CD47 promotes protective innate and adaptive immunity in a mouse model of disseminated candidiasis. PLoS One. 2015;10(5):e0128220. doi:10.1371/journal.pone.0128220
   PubMed Web of Science ®Google Scholar
• Rajarathnam K, Schnoor M, Richardson RM, Rajagopal S. How do chemokines navigate neutrophils to the target site: dissecting the structural mechanisms and signaling pathways. Cell Signal. 2019;54:69–80. doi:10.1016/j.cellsig.2018.11.004
   PubMed Web of Science ®Google Scholar
• Sonica S, Sanjay C, Harsh M, Saroj S. Dietary supplementation with omega-3 polyunsaturated fatty acids ameliorates acute pneumonia induced by Klebsiella pneumoniae in BALB/c mice. Can J Microbiol. 2013;59(7):503–510. doi:10.1139/cjm-2012-0521
   PubMed Web of Science ®Google Scholar
• Novak TE, Babcock TA, Jho DH, Helton WS, Espat NJ. NF-kappa B inhibition by omega −3 fatty acids modulates LPS-stimulated macrophage TNF-alpha transcription. Am J Physiol Lung Cell Mol Physiol. 2003;284(1):L84–89. doi:10.1152/ajplung.00077.2002
   PubMed Web of Science ®Google Scholar
• Yao J, Lu Y, Zhi M, Hu P, Wu W, Gao X. Dietary n-3 polyunsaturated fatty acids ameliorate Crohn’s disease in rats by modulating the expression of PPAR-γ/NFAT. Mol Med Rep. 2017;16(6):8315–8322. doi:10.3892/mmr.2017.7673
   PubMed Web of Science ®Google Scholar
• Sears B, Saha AK. Dietary control of inflammation and resolution. Front Nutr. 2021;8:508. doi:10.3389/fnut.2021.709435
   Web of Science ®Google Scholar
• Salminen A, Hyttinen JMT, Kaarniranta K. AMP-activated protein kinase inhibits NF-κB signaling and inflammation: impact on healthspan and lifespan. J Mol Med. 2011;89(7):667–676. doi:10.1007/s00109-011-0748-0
   PubMed Web of Science ®Google Scholar
• Xue B, Yang Z, Wang X, Shi H, Xu H. Omega-3 polyunsaturated fatty acids antagonize macrophage inflammation via activation of AMPK/SIRT1 pathway. PLoS One. 2012;7(10):e45990. doi:10.1371/journal.pone.0045990
   PubMed Web of Science ®Google Scholar
• Rosa DD, Lourenço FC, da Fonseca AC, et al. Fish oil improves the lipid profile and reduces inflammatory cytokines in Wistar rats with precancerous colon lesions. Nutr Cancer. 2012;64(4):569–579. doi:10.1080/01635581.2012.665563
   PubMed Web of Science ®Google Scholar
• Zhang F, Wang H, Wang X, et al. TGF-β induces M2-like macrophage polarization via SNAIL-mediated suppression of a pro-inflammatory phenotype. Oncotarget. 2016;7(32):52294–52306. doi:10.18632/oncotarget.10561
   PubMedGoogle Scholar
• Barrett JP, Minogue AM, Falvey A, Lynch MA. Involvement of IGF-1 and Akt in M1/M2 activation state in bone marrow-derived macrophages. Exp Cell Res. 2015;335(2):258–268. doi:10.1016/j.yexcr.2015.05.015
   PubMed Web of Science ®Google Scholar
• Kourtzelis I, Hajishengallis G, Chavakis T. Phagocytosis of apoptotic cells in resolution of inflammation. Front Immunol. 2020;11. doi:10.3389/fimmu.2020.00553
   PubMed Web of Science ®Google Scholar
• Watts AD, Hunt NH, Madigan MC, Chaudhri G. Soluble TNF-α receptors bind and neutralize over-expressed transmembrane TNF-α on macrophages, but do not inhibit its processing. J Leukoc Biol. 1999;66(6):1005–1013. doi:10.1002/jlb.66.6.1005
   PubMed Web of Science ®Google Scholar
• Goffe B, Cather JC. Etanercept: an overview. J Am Acad Dermatol. 2003;49(2):105–111. doi:10.1016/mjd.2003.554
   PubMed Web of Science ®Google Scholar
• Djuric Z, Aslam MN, Simon BR, et al. Effects of fish oil supplementation on prostaglandins in normal and tumor colon tissue: modulation by the lipogenic phenotype of colon tumors. J Nutr Biochem. 2017;46:90–99. doi:10.1016/j.jnutbio.2017.04.013
   PubMed Web of Science ®Google Scholar
• Qin Y, Zhou Y, Chen S-H, et al. Fish oil supplements lower serum lipids and glucose in correlation with a reduction in plasma fibroblast growth factor 21 and prostaglandin E2 in nonalcoholic fatty liver disease associated with hyperlipidemia: a randomized clinical trial. PLoS One. 2015;10(7):e0133496. doi:10.1371/journal.pone.0133496
   PubMed Web of Science ®Google Scholar
• Dasilva G, Lois S, Méndez L, et al. Fish oil improves pathway-oriented profiling of lipid mediators for maintaining metabolic homeostasis in adipose tissue of prediabetic rats. Front Immunol. 2021;12. doi:10.3389/fimmu.2021.608875
   PubMed Web of Science ®Google Scholar
• Nagatake T, Shibata Y, Morimoto S, et al. 12-hydroxyeicosapentaenoic acid inhibits foam cell formation and ameliorates high-fat diet-induced pathology of atherosclerosis in mice. Sci Rep. 2021;11(1). doi:10.1038/s41598-021-89707-1
   PubMed Web of Science ®Google Scholar
• Krishnamurthy VR, Dougherty A, Haller CA, Chaikof EL. Total synthesis and bioactivity of 18(R)-hydroxyeicosapentaenoic acid. J Org Chem. 2011;76(13):5433–5437. doi:10.1021/jo2002243
   PubMed Web of Science ®Google Scholar
• Powell WS, Rokach J. Biosynthesis, biological effects, and receptors of hydroxyeicosatetraenoic acids (HETEs) and oxoeicosatetraenoic acids (oxo-ETEs) derived from arachidonic acid. Biochim Biophys Acta Mol Cell Biol Lipids. 2015;1851(4):340–355. doi:10.1016/j.bbalip.2014.10.008
   PubMed Web of Science ®Google Scholar