Erratum: The in vitro effects of n-3 fatty acids on immune response regulation of bovine ex vivo endometrial explants

Authors

DOI:

https://doi.org/10.11606/issn.1678-4456.bjvras.2023.214210

Keywords:

Cytokines, Fatty acids, Reproduction, Uterus

Abstract

Fatty acids are considered metabolic intermediaries, although new facts indicate they also work as signaling molecules with different roles in the immune response. Based on that, in this study, we investigated the anti-inflammatory effects of n-3 polyunsaturated fatty acids (PUFAs) as eicosapentaenoic acid (EPA), docosahexaenoic acid (DHA), and α-linolenic acid (LNA) in ex vivo bovine endometrial explants. For this, two groups were formed: (1) LPS-challenged and (2) control, both to evaluate the accumulation of proinflammatory cytokines as interleukin 1β (IL1B) and interleukin 6 (IL6). To develop the study, bovine female reproductive tracts from non-pregnant Angus heifers without evidence of reproductive diseases were selected. Endometrial explants were processed and treated for 24 h with EPA, DHA, and LNA in five different concentrations (0μM, 50μM, 100 μM, 200μM and 400 μM) and then, challenged with LPS for 24 h. Supernatants were collected to evaluate the concentration of IL1B and IL6 by ELISA. Explants treated with EPA from control groups reduced the concentrations of ILB (200μM) and IL6 (400 μM), and IL6 (50 μM; 100 μM) from the LPS-challenged group. DHA decreased the accumulation of IL1B and IL6 at 200 μM on explants from the LPS-challenged group, and 200 μM reduced IL6 from the control group. In contrast, explants treated with LNA only reduced the accumulation of IL1B to 400μM (from both groups). In conclusion, the EPA acid is the best anti-inflammatory option to decrease the concentration of both pro-inflammatory cytokines (IL1B and IL6) from LPS-challenged and control groups in bovine endometrial explants; while LNA evidence to be the last option to promote an anti-inflammatory response.

Downloads

Download data is not yet available.

References

Albiger B, Dahlberg S, Normark S. Role of the innate immune system in host defence against bacterial infections : focus on the Toll-like receptors. J Intern Med. 2007;261(6):511- 28. http://dx.doi.org/10.1111/j.1365-2796.2007.01821.x. PMid:17547708.

Bionaz M, Vargas-Bello-Pérez E, Busato S. Advances in fatty acids nutrition in dairy cows: from gut to cells and effects on performance. J Anim Sci Biotechnol. 2020;11(1):110. http://dx.doi.org/10.1186/s40104-020-00512-8. PMid:33292523.

Borges ÁM, Healey GD, Sheldon IM. Explants of intact endometrium to model bovine innate immunity and inflammation ex vivo. Am J Reprod Immunol. 2012;67(6):526- 39. http://dx.doi.org/10.1111/j.1600-0897.2012.01106.x. PMid:22324889.

Calder PC. Polyunsaturated fatty acids and inflammation. Prostaglandins Leukot Essent Fatty Acids. 2006;75(3):197-202. http://dx.doi.org/10.1016/j.plefa.2006.05.012. PMid:16828270.

Caughey GE, Mantzioris E, Gibson RA, Cleland LG, James MJ. The effect on human tumor necrosis factor α and interleukin 1β production of diets enriched in n-3 fatty acids from vegetable oil or fish oil. Am J Clin Nutr. 1996;63(1):116-22. http://dx.doi.org/10.1093/ajcn/63.1.116. PMid:8604658.

Chapwanya A, Meade KG, Doherty ML, Callanan JJ, Mee JF, Farrelly CO. Histopathological and molecular evaluation of Holstein-Friesian cows postpartum: toward an improved understanding of uterine innate immunity. Theriogenology. 2009;71(9):1396-407. http://dx.doi.org/10.1016/j.theriogenology.2009.01.006. PMid:19233457.

Chen C, Guan W, Xie Q, Chen G, He X, Zhang H, Guo W, Chen F, Tan Y, Pan Q. n-3 essential fatty acids in Nile tilapia, Oreochromis niloticus: bioconverting LNA to DHA is relatively efficient and the LC-PUFA biosynthetic pathway is substrate limited in juvenile fish. Aquaculture. 2018;495:513- 22. http://dx.doi.org/10.1016/j.aquaculture.2018.06.023.

Collins T, Read MA, Neish AS, Whitley MZ, Thanos D, Maniatis T. Transcriptional regulation of endothelial cell adhesion molecules: NF‐κB and cytokine‐inducible enhancers. FASEB J. 1995;9(10):899-909. http://dx.doi.org/10.1096/fasebj.9.10.7542214. PMid:7542214.

Dirandeh E, Ghaffari J. Effects of feeding a source of omega-3 fatty acid during the early postpartum period on the endocannabinoid system in the bovine endometrium. Theriogenology. 2018;121:141-6. http://dx.doi.org/10.1016/j.theriogenology.2018.07.043. PMid:30145543.

Fritsche KL. Too much linoleic acid promotes inflammationdoesn’t it? Prostaglandins Leukot Essent Fatty Acids. 2008;79(3– 5):173-5. http://dx.doi.org/10.1016/j.plefa.2008.09.019. PMid:18990555.

Gorjão R, Verlengia R, de Lima TM, Soriano FG, Boaventura MFC, Kanunfre CC, Peres CM, Sampaio SC, Otton R, Folador A, Martins EF, Curi TCP, Portiolli ÉP, Newsholme P, Curi R. Effect of docosahexaenoic acid-rich fish oil supplementation on human leukocyte function. Clin Nutr. 2006;25(6):923-38. http://dx.doi.org/10.1016/j.clnu.2006.03.004. PMid:16697494.

Haag M. Essential fatty acids and the brain. Can J Psychiatry. 2003;48(3):195-203. http://dx.doi.org/10.1177/070674370304800308. PMid:12728744.

He X, Liu W, Shi M, Yang Z, Zhang X, Gong P. Docosahexaenoic acid attenuates LPS-stimulated inflammatory response by regulating the PPARγ/NF-κB pathways in primary bovine mammary epithelial cells. Res Vet Sci. 2017;112:7-12. http://dx.doi.org/10.1016/j.rvsc.2016.12.011. PMid:28095338.

Ireland JJ, Coulson PB, Murphree RL. Follicular development during four stages of the estrous cycle of beef cattle. J Anim Sci. 1979;49(5):1261-9. http://dx.doi.org/10.2527/jas1979.4951261x. PMid:575533.

Kelley DS, Taylor PC, Nelson GJ, Schmidt PC, Ferretti A, Erickson KL, Ranjit K, Mackey BE. Docosahexaenoic acid ingestion inhibits natural killer cell activity and production of inflammatory mediators in young healthy men. Lipids. 1999;34(4):317-24. http://dx.doi.org/10.1007/s11745-999-0369-5. PMid:10443964.

Koh A, Silva APB, Bansal AK, Bansal M, Sun C, Lee H, Glogauer M, Sodek J, Zohar R. Role of osteopontin in neutrophil function. Immunology. 2007;122(4):466-75. http://dx.doi.org/10.1111/j.1365-2567.2007.02682.x. PMid:17680800.

Lackey DE, Olefsky JM. Regulation of metabolism by the innate immune system. Nat Rev Endocrinol. 2016;12(1):15-28. http://dx.doi.org/10.1038/nrendo.2015.189. PMid:26553134.

Lee JY, Zhao L, Youn HS, Weatherill AR, Tapping R, Feng L, Lee WH, Fitzgerald KA, Hwang DH. Saturated fatty acid activates but polyunsaturated fatty acid inhibits toll-like receptor 2 dimerized with toll-like receptor 6 or 1. J Biol Chem. 2004;279(17):16971-9. http://dx.doi.org/10.1074/jbc.M312990200. PMid:14966134.

Mattos R, Guzeloglu A, Badinga L, Staples CR, Thatcher WW. Polyunsaturated fatty acids and bovine interferon-tau modify phorbol ester-induced secretion of prostaglandin F2 alpha and expression of prostaglandin endoperoxide synthase-2 and phospholipase-A2 in bovine endometrial cells. Biol Reprod. 2003;69(3):780-7. http://dx.doi.org/10.1095/biolreprod.102.015057. PMid:12724278.

Mickleborough TD, Tecklenburg SL, Montgomery GS, Lindley MR. Eicosapentaenoic acid is more effective than docosahexaenoic acid in inhibiting proinflammatory mediator production and transcription from LPS-induced human asthmatic alveolar macrophage cells. Clin Nutr. 2009;28(1):71-7. http://dx.doi.org/10.1016/j.clnu.2008.10.012. PMid:19054597.

Moallem U. Invited review : roles of dietary n-3 fatty acids in performance, milk fat composition, and reproductive and immune systems in dairy cattle. J Dairy Sci. 2018;101(10):8641- 61. http://dx.doi.org/10.3168/jds.2018-14772. PMid:30100509.

Moallem U, Lehrer H, Livshits L, Zachut M. The effects of omega-3 α-linolenic acid from flaxseed oil supplemented to high-yielding dairy cows on production, health, and fertility. Livest Sci. 2020;242:104302. http://dx.doi.org/10.1016/j.livsci.2020.104302.

Oh DY, Talukdar S, Bae EJ, Imamura T, Morinaga H, Fan WQ, Li P, Lu WJ, Watkins SM, Olefsky JM. GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell. 2010;142(5):687-98. http://dx.doi.org/10.1016/j.cell.2010.07.041. PMid:20813258.

Olmo I, Teuber S, Larrazabal C, Alarcon P, Raipane F, Burgos RA, Hidalgo MA. Docosahexaenoic acid and TUG-891 activate free fatty acid-4 receptor in bovine neutrophils. Vet Immunol Immunopathol. 2019;209:53-60. http://dx.doi.org/10.1016/j.vetimm.2019.02.008. PMid:30885306.

Parshyna I, Lehmann S, Grahl K, Pahlke C, Frenzel A, Weidlich H, Morawietz H. Impact of omega-3 fatty acids on expression of angiogenic cytokines and angiogenesis by adipose-derived stem cells. Atheroscler Suppl. 2017;30:303-10. http://dx.doi.org/10.1016/j.atherosclerosissup.2017.05.040. PMid:29096855.

Penrod LV, Allen RE, Turner JL, Limesand SW, Arns MJ. Effects of oxytocin, lipopolysaccharide (LPS), and polyunsaturated fatty acids on prostaglandin secretion and gene expression in equine endometrial explant cultures. Domest Anim Endocrinol. 2013;44(1):46-55. http://dx.doi.org/10.1016/j.domaniend.2012.09.002. PMid:23063410.

Pisani LF, Lecchi C, Invernizzi G, Sartorelli P, Savoini G, Ceciliani F. In vitro modulatory effect of ω-3 polyunsaturated fatty acid (EPA and DHA) on phagocytosis and ROS production of goat neutrophils. Vet Immunol Immunopathol. 2009;131(1- 2):79-85. http://dx.doi.org/10.1016/j.vetimm.2009.03.018. PMid:19395090.

Plewes MR, Burns PD, Hyslop RM, George Barisas B. Influence of omega-3 fatty acids on bovine luteal cell plasma membrane dynamics. Biochim Biophys Acta Biomembr. 2017;1859(12):2413-9. http://dx.doi.org/10.1016/j.bbamem.2017.09.012. PMid:28912100.

Roberts RM, Chen Y, Ezashi T, Walker AM. Interferons and the maternal-conceptus dialog in mammals. Semin Cell Dev Biol. 2008;19(2):170-7. http://dx.doi.org/10.1016/j.semcdb.2007.10.007. PMid:18032074.

Thien FC, Hallsworth MP, Soh H, Lee TH. Effects of exogenous eicosapentaenoic acid on generation of leukotriene C4 and leukotriene C5 by calcium ionophore-activated human eosinophils in vitro. J Immunol. 1993;150(8 Pt 1):3546-52. http://dx.doi.org/10.4049/jimmunol.150.8.3546. PMid:8468488.

Tortosa-Caparrós E, Navas-Carrillo D, Marín F, OrenesPiñero E. Anti-inflammatory effects of omega 3 and omega 6 polyunsaturated fatty acids in cardiovascular disease and metabolic syndrome. Crit Rev Food Sci Nutr. 2017;57(16):3421-9. http://dx.doi.org/10.1080/10408398.2015.1126549. PMid:26745681.

Williams-Bey Y, Boularan C, Vural A, Huang NN, Hwang IY, Shan-Shi C, Kehrl JH. Omega-3 free fatty acids suppress macrophage inflammasome activation by inhibiting NF-κB activation and enhancing autophagy. PLoS One. 2014;9(6): e97957. http://dx.doi.org/10.1371/journal.pone.0097957. PMid:24911523.

Xie D, Liu X, Wang S, You C, Li Y. Effects of dietary LNA/ LA ratios on growth performance, fatty acid composition and expression levels of elovl5, Δ4 fad and Δ6/Δ5 fad in the marine teleost Siganus canaliculatus. Aquaculture. 2017;2018(484):309-16.

Yan Y, Jiang W, Spinetti T, Tardivel A, Castillo R, Bourquin C, Guarda G, Tian Z, Tschopp J, Zhou R. Omega-3 fatty acids prevent inflammation and metabolic disorder through inhibition of NLRP3 inflammasome activation. Immunity. 2013;38(6):1154-63. http://dx.doi.org/10.1016/j.immuni.2013.05.015. PMid:23809162.

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- 82. http://dx.doi.org/10.1016/j.pharmthera.2013.10.010. PMid:24201219.

Downloads

Published

2023-08-03

Issue

Section

ERRATUM

How to Cite

1.
Carneiro LC, Saut JPE, Almeida M de O, Barbosa SPF, Williams EJ, Cerqueira HDB de, et al. Erratum: The in vitro effects of n-3 fatty acids on immune response regulation of bovine ex vivo endometrial explants. Braz. J. Vet. Res. Anim. Sci. [Internet]. 2023 Aug. 3 [cited 2024 Jul. 16];60:e214210. Available from: https://www.revistas.usp.br/bjvras/article/view/214210