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Anti-inflammatory effects of conjugated linoleic acid isomers and essential fatty acids in bovine mammary epithelial cells

Published online by Cambridge University Press:  09 January 2018

D. Dipasquale ,
L. Basiricò ,
P. Morera ,
R. Primi ,
A. Tröscher  and
U. Bernabucci
D. Dipasquale
Affiliation:
Dipartimento di Scienze Agrarie e Forestali, Università degli Studi della Tuscia, via San Camillo De Lellis s.n.c., 01100 Viterbo, Italy
L. Basiricò
Affiliation:
Dipartimento di Scienze Agrarie e Forestali, Università degli Studi della Tuscia, via San Camillo De Lellis s.n.c., 01100 Viterbo, Italy
P. Morera
Affiliation:
Dipartimento di Scienze Agrarie e Forestali, Università degli Studi della Tuscia, via San Camillo De Lellis s.n.c., 01100 Viterbo, Italy
R. Primi
Affiliation:
Dipartimento di Scienze Agrarie e Forestali, Università degli Studi della Tuscia, via San Camillo De Lellis s.n.c., 01100 Viterbo, Italy
A. Tröscher
Affiliation:
Animal Nutrition, BASF SE, Chemiestrasse. 22, F 31, 68623 Lampertheim, Germany
U. Bernabucci*
Affiliation:
Dipartimento di Scienze Agrarie e Forestali, Università degli Studi della Tuscia, via San Camillo De Lellis s.n.c., 01100 Viterbo, Italy
*
†E-mail: bernab@unitus.it
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Abstract

Fatty acids are important modulators of inflammatory responses, in particular, n-3 and n-6 essential fatty acids and CLA have received particular attention for their ability to modulate inflammation. The objectives of this study were to compare the effects of CLA and essential fatty acids on the expression of pro and anti- inflammatory cytokines and their protective efficacy against inflammatory status in mammary gland by an in vitro model based on bovine mammary epithelial cells (BME-UV1). Bovine mammary epithelial cells were treated with complete medium containing either 50 µM of cis-9, trans-11 CLA (c9,t11 CLA) or trans-10, cis-12 CLA (t10,c12 CLA) or (α)-linolenic acid (aLnA) or (γ)-linolenic acid (gLnA) or linoleic acid (LA). After 48 h by fatty acids administration the cells were treated for 3 h with 20 µM of lipopolysaccharide (LPS) to induce inflammatory stimulus. Reactive oxygen species (ROS) production after treatments was assessed to verify and to compare the potential protection of different fatty acids against LPS-induced oxidative stress. The messenger RNA abundance of bovine pro and anti-inflammatory cytokines (tumor necrosis factor-α (TNF-α), interleukin-1β (IL-1β), interleukin-6 (IL-6) and interleukine-10 (IL-10)) and peroxisome proliferator receptor-α/γ (PPARγ/α) were determined in BME-UV1 by real-time PCR. The results showed that cells treated with fatty acids and LPS increased ROS production compared with control cells. Among treatments, cells treated with c9,t11 CLA and t10,c12 CLA isomers revealed significant lower levels of ROS production compared with other fatty acids. All fatty acids reduced the gene expression of pro- and anti-inflammatory cytokines. Among fatty acids, t10,c12 CLA, LA and gLnA showed an homogeneous reduction of the three pro-inflammatory cytokines and this may correspond to more balanced and efficient physiological activity and may trigger a better protective effect. The PPARγ gene expression was significantly greater in cells treated with t10,c12 CLA, aLnA and LA, whereas the PPARα gene expression levels were significantly lower in cells treated with all different fatty acids, compared with the control. These results suggest that fatty acids inhibited the transcription of pro-inflammatory cytokines by the upregulation of PPARγ expression.

Keywords

CLA cis-9trans-11CLA trans-10cis-12essential fatty acidsbovine mammary gland cellsinflammatory status
Type
Research Article
Information
animal , Volume 12 , Issue 10 , October 2018 , pp. 2108 - 2114
Copyright
© The Animal Consortium 2018 

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References

Abuelo, A, Hernández, J, Benedito, JL and Castillo, C 2015. The importance of the oxidative status of dairy cattle in the periparturient period: revisiting antioxidant supplementation. Journal of Animal Physiology and Animal Nutrition 99, 1003–1016.Google Scholar
Barbieri, E and Sestili, P 2012. Reactive oxygen species in skeletal muscle signaling. Journal of Signal Transduction 2012, 1–17.Google Scholar
Bernabucci, U, Ronchi, B, Lacetera, N and Nardone, A 2005. Influence of body condition score on relationships between metabolic status and oxidative stress in periparturient dairy cows. Journal of Dairy Science 88, 2017–2026.Google Scholar
Bertoni, G, Trevisi, E, Han, X and Bionaz, M 2008. Effects of inflammatory conditions on liver activity in puerperium period and consequences for performance in dairy cows. Journal of Dairy Science 91, 3300–3310.Google Scholar
Bionaz, M, Baumrucker, CR, Shirk, E, Vanden Heuvel, JP, Block, E and Varga, GA 2008. Characterization of Madin-Darby bovine kidney cell line for peroxisome proliferator-activated receptors: temporal response and sensitivity to fatty acids. Journal of Dairy Science 91, 2808–2813.Google Scholar
Boudjellab, N, Chan-Tang, HS and Zhao, X 2000. Bovine interleukin-1 expression by cultured mammary epithelial cells (MAC-T) and its involvement in the release of MAC-T derived interleukin-8. Comparative Biochemistry and Physiology – Part A: Molecular & Integrative Physiology 127, 191–199.Google Scholar
Cabrero, A, Alegret, M, Sanchez, RM, Adzet, T, Laguna, JC and Carrera, MV 2002. Increased reactive oxygen species production down-regulates peroxisome proliferator-activated alpha pathway in C2C12 skeletal muscle cells. Journal of Biological Chemistry 277, 10100–10107.Google Scholar
Cao, D, Luo, J, Zang, W, Chen, D, Xu, H, Shi, H and Jing, X 2016. Gamma-linolenic acid suppresses NF-κΒ signaling via CD36 in the lipopolysaccharide-induced inflammatory response in primary goat mammary gland epithelial cells. Inflammation 39, 1225–1237.Google Scholar
Changhua, L, Jindong, Y, Defa, L, Lidan, Z, Shiyan, Q and Jianjun, X 2005. Conjugated linoleic acid attenuates the production and gene expression of proinflammatory cytokines in weaned pigs challenged with lipopolysaccharide. Journal of Nutrition 135, 239–244.Google Scholar
de Heredia, FP, Gómez-Martínez, S and Marcos, A 2012. Obesity, inflammation and the immune system. Proceedings of the Nutrition Society 71, 332–338.Google Scholar
de Jong, AJ, Kloppenburg, M, Toes, REM and Ioan-Facsinay, A 2014. Fatty acids, lipid mediators, and T-cell function. Frontiers in Immunology 5, 1–7.Google Scholar
Erdinest, N, Shmueli, O, Grossman, Y, Ovadia, H and Solomon, A 2012. Anti-inflammatory effects of alpha linolenic acid on human corneal epithelial cells. Investigative Ophthalmology & Visual Science 53, 4396–4406.Google Scholar
Gonzalez, DD, Rimondi, A, Perez Aguirreburualde, MS, Mozgovoj, M, Bellido, D, Wigdorovitz, A and Dus Santos, MJ 2013. Quantitation of cytokine gene expression by real time PCR in bovine milk and colostrum cells from cows immunized with a bovine rotavirus VP6 experimental vaccine. Research in Veterinary Science 95, 703–708.Google Scholar
Hammond, S, Regna, N, Chafin, C and Reilly, C 2014. Conjugated linoleic acid reduces inflammation via PPARγ in murine autoimmune glomerulonephritis (THER6P.861). Journal of Immunology 192, 201–217.Google Scholar
Hontecillas, R, Wannemeulher, MJ, Zimmerman, DR, Hutto, DL, Wilson, JH, Ahn, DU and Bassaganya-Riera, J 2002. Nutritional regulation of porcine bacterial-induced colitis by conjugated linoleic acid 1,2. Journal of Nutrition 132, 2019–2027.Google Scholar
Lacetera, N, Scalia, D, Mashek, D, Bernabucci, U and Grummer, R 2007. Effects of intravenous triacylglycerol emulsions on lymphocyte responses to mitogens in fasted dairy cows undergoing intense lipomobilization. Journal of Dairy Research 74, 323–328.Google Scholar
Lawrence, T 2009. The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harbor Perspectives in Biology 1, 1–10.Google Scholar
Lin, S, Hou, J, Xiang, F, Zhang, X, Che, L, Lin, Y, Xu, S, Tian, G, Zeng, Q, Yu, B, Zhang, K, Chen, D, Wu, D and Fang, Z 2013. Mammary inflammation around parturition appeared to be attenuated by consumption of fish oil rich in n-3 polyunsaturated fatty acids. Lipids in Health and Disease 12, 1–13.Google Scholar
Liu, Y, Biarnés Costa, M and Gerhardinger, C 2012. IL-1β is upregulated in the diabetic retina and retinal vessels: cell-specific effect of high glucose and IL-1β autostimulation. PLoS One 7, e36949.Google Scholar
Mandard, S and Patsouris, D 2013. Nuclear control of the inflammatory response in mammals by peroxisome proliferator-activated receptors. PPAR Research 2013, 1–23.Google Scholar
McClenahan, DJ, Sotos, JP and Czuprynski, CJ 2005. Cytokine response of bovine mammary gland epithelial cells to Escherichia coli, coliform culture filtrate, or lipopolysaccharide. American Journal of Veterinary Research 66, 1590–1597.Google Scholar
Medina-Estrada, I, López-Meza, JE, Ochoa-Zarzosa, A and Ochoa-Zarzosa, A 2016. Anti-inflammatory and antimicrobial effects of estradiol in bovine mammary epithelial cells during Staphylococcus aureus internalization. Mediators of Inflammation 2016, 1–16.Google Scholar
Reynolds, CM and Roche, HM 2010. Conjugated linoleic acid and inflammatory cell signaling. Prostaglandins, Leukotrienes and Essential Fatty Acids (PLEFA) 82, 199–204.Google Scholar
Renner, L, Kersten, S, Duevel, A, Schuberth, HJ and Dänicke, S 2013. Effects of cis-9,trans-11 and trans-10, cis-12 conjugated linoleic acid, linoleic acid, phytanic acid and the combination of various fatty acids on proliferation and cytokine expression of bovine peripheral blood mononuclear cells. Nutrients 5, 2667–2683.Google Scholar
Scalia, D, Lacetera, N, Bernabucci, U, Demeyere, K, Duchateau, L, Burvenich, C, Aoki, T, Etoh, T, Hashimoto, T, Naruse, M, Sano, H, Utsumi, H and Nawata, H 2006. In vitro effects of nonesterified fatty acids on bovine neutrophils oxidative burst and viability. Journal of Dairy Science 89, 147–154.Google Scholar
Song, H-J, Grant, I, Rotondo, D, Mohede, I, Sattar, N, Heys, SD and Wahle, KWJ 2005. Effect of CLA supplementation on immune function in young healthy volunteers. European Journal of Clinical Nutrition 59, 508–517.Google Scholar
Sordillo, LM and Raphael, W 2013. Significance of metabolic stress, lipid mobilization, and inflammation on transition cow disorders. Veterinary Clinics of North America: Food Animal Practice 29, 267–278.Google Scholar
Tak, PP and Firestein, GS 2001. NF-κB: a key role in inflammatory diseases. Journal of Clinical Investigation 107, 7–11.Google Scholar
Tamayo, E, Fernández, A, Almansa, R, Carrasco, E, Heredia, M, Lajo, C, Goncalves, L, Gómez-Herreras, JI, de Lejarazu, RO and Bermejo-Martin, JF 2011. Pro- and anti-inflammatory responses are regulated simultaneously from the first moments of septic shock. European Cytokine Network 22, 82–87.Google Scholar
Teng, K-T, Chang, C-Y, Chang, LF and Nesaretnam, K 2014. Modulation of obesity-induced inflammation by dietary fats: mechanisms and clinical evidence. Nutrition Journal 13, 1–15.Google Scholar
Verlengia, R, Gorjão, R, Kanunfre, CC, Verlengia, SB, Gorjão, R, Kanunfre, CC, Bordin, S, de Lima, T M, Martins, EF, Newsholme, P and Curi, R 2004. Effects of EPA and DHA on proliferation, cytokine production, and gene expression in Raji cells. Lipids 39, 857–864.Google Scholar
Wallace, FA, Miles, EA, Evans, C, Stock, TE, Yaqoob, P and Calder, PC 2001. Dietary fatty acids influence the production of Th1- but Not Th2-type cytokines. Journal of Leukocyte Biology 69, 449–457.Google Scholar
Wojdasiewicz, P, Poniatowski, ŁA and Szukiewicz, D 2014. The Role of Inflammatory and Anti-Inflammatory Cytokines in the Pathogenesis of Osteoarthritis. Mediators of Inflammation 2014, 1–19.Google Scholar
Zhao, G, Etherton, TD, Martin, KR, Vanden Heuvel, JP, Gillies, PJ, West, SG and Kris-Etherton, PM. 2005. Anti-inflammatory effects of polyunsaturated fatty acids in THP-1 cells. Biochemical and Biophysical Research Communications 336, 909–917.Google Scholar