Vitamin E reduces the reactive oxygen species production in dominant follicle during the negative energy balance in cattle.
antioxidants
fatty acids
follicular fluid
oxidative stress
vitamin E
Journal
Reproduction in domestic animals = Zuchthygiene
ISSN: 1439-0531
Titre abrégé: Reprod Domest Anim
Pays: Germany
ID NLM: 9015668
Informations de publication
Date de publication:
Dec 2023
Dec 2023
Historique:
revised:
07
09
2023
received:
10
08
2023
accepted:
14
09
2023
pubmed:
25
9
2023
medline:
25
9
2023
entrez:
25
9
2023
Statut:
ppublish
Résumé
In the postpartum period, there is an increase in non-esterified fatty acids (NEFA) in both serum and follicular fluid (FF) of cattle. The increase in fatty acid concentration results in increased production of reactive oxygen species (ROS) that can compromise bovine fertility. The objectives of this study were to characterize the lipid profile found in the FF of cows experiencing induced negative energy balance (NEB) and to evaluate the effect of α-tocopherol in the prevention of oxidative stress in the serum and FF of cows. Twenty-nine beef cows were divided into groups: (1) control; (2) Fasting for 24 days; and (3) Fasting + VitE. Between D0 and D4 blood samples were taken to assess concentrations of NEFA, ROS production, total antioxidant capacity (FRAP), lipid peroxidation, and α-tocopherol (vitamin E). On D4, follicular aspiration was performed for analysis of FF from the dominant follicle. Our results demonstrate that fasting was effective in causing increased fat mobilization in animals. The increase in serum concentration of C18:1c9 was reflected in the FF of fasting cows. Serum α-tocopherol concentration was higher in the control and Fasting + VitE groups compared to the Fasting group. In FF, there was an increase of α-tocopherol in the Fasting + VitE group in comparison to Fasting cows. There was an increase in ROS production in the serum of fasting cows. ROS production in FF was higher in the Fasting compared to the Fasting + VitE group. Vitamin E has beneficial effects in reducing ROS production in the dominant follicle of cows in NEB.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1662-1671Subventions
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
Organisme : Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
Organisme : Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul
Organisme : Fundação de Amparo à Pesquisa e Inovação do Estado de Santa Catarina
Informations de copyright
© 2023 Wiley-VCH GmbH. Published by John Wiley & Sons Ltd.
Références
Aardema, H., Lolicato, F., van de Lest, C. H., Brouwers, J. F., Vaandrager, A. B., van Tol, H. T., Roelen, B. A., Vos, P. L., Helms, J. B., & Gadella, B. M. (2013). Bovine cumulus cells protect maturing oocytes from increased fatty acid levels by massive intracellular lipid storage. Biology of Reproduction, 88, 1-15. https://doi.org/10.1095/biolreprod.112.106062
Aardema, H., Vos, P. L. A. M., Lolicato, F., Roelen, B. A. J., Knijn, H. M., Vaandrager, A. B., Helms, J. B., & Gadella, B. M. (2011). Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence. Biology of Reproduction, 69, 62-69. https://doi.org/10.1095/biolreprod.110.088815
Abuelo, A., Hernández, J., Benedito, J. L., & 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. https://doi.org/10.1111/jpn.12273
Aréchiga, C. F., Vázquez-Flores, S., Ortiz, O., Hernández-Cerón, J., Porras, A., McDowell, L. R., & Hansen, P. J. (1998). Effect of injection of β-carotene or vitamin E and selenium on fertility of lactating dairy cows. Theriogenology, 50, 65-76. https://doi.org/10.1016/S0093-691X(98)00114-9
Baldi, A., Savoini, G., Pinotti, L., Monfardini, E., Cheli, F., & Orto, V. D. (2000). Effects of vitamin E and different energy sources on vitamin e status, milk quality and reproduction in transition cows. Journal of Veterinary Medicine, 47, 599-608. https://doi.org/10.1046/j.1439-0442.2000.00323.x
Beam, S. W., & Butler, W. R. (1997). Energy balance and ovarian follicle development prior to the first ovulation postpartum in dairy cows receiving three levels of dietary fat. Biology of Reproduction, 56, 133-142. https://doi.org/10.1095/biolreprod56.1.133
Bell, A. W. (1995). Regulation of organic nutrient metabolism during transition from late pregnancy to early lactation. Journal of Animal Science, 73, 2804-2819. https://doi.org/10.2527/1995.7392804x
Benedet, A., Manuelian, C. L., Zidi, A., Penasa, M., & Marchi, M. (2019). Invited review: β-hydroxybutyrate concentration in blood and milk and its associations with cow performance. Animal, 13, 1676-1689. https://doi.org/10.1017/S175173111900034X
Benzie, I. F., & Strain, J. J. (1996). The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: The FRAP assay. Analytical Biochemistry, 239, 70-76. https://doi.org/10.1006/abio.1996.0292
Bernabucci, U., Ronchi, B., Lacetera, N., & 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. https://doi.org/10.3168/jds.S0022-0302(05)72878-2
Bionaz, M., Trevisi, E., Calamari, L., Librandi, F., Ferrari, A., & Bertoni, G. (2007). Plasma paraoxonase, health, inflammatory conditions, and liver function in transition dairy cows. Journal of Dairy Science, 90, 1740-1750. https://doi.org/10.3168/jds.2006-445
Bouwstra, R. J., Goselink, R. M. A., Dobbelaar, P., Nielen, M., Newbold, J. R., & Van Werven, T. (2008). The relationship between oxidative damage and vitamin e concentration in blood, milk, and liver tissue from vitamin E supplemented and nonsupplemented periparturient heifers. Journal of Dairy Science, 91, 977-987. https://doi.org/10.3168/jds.2007-0596
Bouwstra, R. J., Nielen, M., Newbold, J. R., Jansen, E. H. J. M., Jelinek, H. F., & Van Werven, T. (2010). Vitamin E supplementation during the dry period in dairy cattle. Part II: Oxidative stress following vitamin E supplementation may increase clinical mastitis incidence postpartum. Journal of Dairy Science, 93, 5696-5706. https://doi.org/10.3168/jds.2010-3161
Campbell, M. H., & Miller, J. K. (1998). Effect of supplemental dietary vitamin E and zinc on reproductive performance of dairy cows and heifers fed excess iron. Journal of Dairy Science, 81, 2693-2699. https://doi.org/10.3168/jds.S0022-0302(98)75826-6
Charão, M. F., Moro, A. M., Brucker, N., Bulcão, R. P., Baierle, M., Freitas, F., Durgante, J., Nascimento, S., Bubols, G. B., Saldiva, P. H., Bohrer, D., & Garcia, S. C. (2012). Simultaneous quantification of lycopene, β-carotene, retinol and α -tocopherol in plasma after a simple extraction procedure: Stability study and application to human volunteers. Journal of the Brazilian Chemical Society, 23, 1441-1449. https://doi.org/10.1590/S0103-50532012005000001
Colitti, M., Stradaioli, G., & Stefanon, B. (2000). Effect of α-tocopherol deprivation on the involution of mammary gland in sheep. Journal of Dairy Science, 83, 345-350. https://doi.org/10.3168/jds.S0022-0302(00)74885-5
Cury-Boaventura, M. F., Gorjão, R., de Lima, T. M., Newsholme, P., & Curi, R. (2006). Comparative toxicity of oleic and linoleic acid on human lymphocytes. Life Sciences, 78, 1448-1456. https://doi.org/10.1016/j.lfs.2005.07.038
De Bie, J., Langbeen, A., Verlaet, A. A. J., Florizoone, F., Immig, I., Hermans, N., Fransen, E., Bols, P. E. J., & Leroy, J. L. M. R. (2016). The effect of a negative energy balance status on β-carotene availability in serum and follicular fluid of nonlactating dairy cows. Journal of Dairy Science, 99, 5808-5819. https://doi.org/10.3168/jds.2016-10870
Dupont, J., Scaramuzzi, R. J., & Reverchon, M. (2014). The effect of nutrition and metabolic status on the development of follicles, oocytes and embryos in ruminants. Animal, 8, 1031-1044. https://doi.org/10.1017/S1751731114000937
Ferst, J. G., Glanzner, W. G., Gutierrez, K., de Macedo, M. P., Ferreira, R., Gasperin, B. G., Duggavathi, R., Gonçalves, P. B., & Bordignon, V. (2021). Supplementation of oleic acid, stearic acid, palmitic acid and β-hydroxybutyrate increase H3K9me3 in endometrial epithelial cells of cattle cultured in vitro. Animal Reproduction Science, 233, 106851. https://doi.org/10.1016/j.anireprosci.2021.106851
Ferst, J. G., Missio, D., Bertolin, K., Gasperin, B. G., Leivas, F. G., Bordignon, V., Gonçalves, P. B., & Ferreira, R. (2020). Intrafollicular injection of nonesterified fatty acids impaired dominant follicle growth in cattle. Animal Reproduction Science, 219, 106536. https://doi.org/10.1016/j.anireprosci.2020.106536
Fiore, E., Lisuzzo, A., Laghi, L., Harvatine, K. J., Mazzotta, E., Alterisio, M. C., Ciaramella, P., Zhu, C., Contiero, B., Faillace, V., & Guccione, J. (2023). Serum metabolomics assessment of etiological processes predisposing ketosis in water buffalo during early lactation. Journal of Dairy Science, 106(5), 3465-3476. https://doi.org/10.3168/jds.2022-2220
Fiore, E., Tessari, R., Morgante, M., Gianesella, M., Badon, T., Bedin, S., Mazzotta, E., & Berlanda, M. (2020). Identification of plasma fatty acids in four lipid classes to understand energy metabolism at different levels of ketonemia in dairy cows using thin layer chromatography and gas chromatographic techniques (TLC-GC). Animals, 10(4), 571. https://doi.org/10.3390/ani10040571
Goff, J. P., Kimura, K., & Horst, R. L. (2002). Effect of mastectomy on milk fever, energy, and vitamins a, e, and β-carotene status at parturition. Journal of Dairy Science, 85, 1427-1436. https://doi.org/10.3168/jds.S0022-0302(02)74210-0
Han, L. D., Xia, J. F., Liang, Q. L., Wang, Y., Wang, Y. M., Hu, P., Li, P., & Luo, G. A. (2011). Plasma esterified and non-esterified fatty acids metabolic profiling using gas chromatography-mass spectrometry and its application in the study of diabetic mellitus and diabetic nephropathy. Analytica Chimica Acta, 689, 85-91. https://doi.org/10.1016/j.aca.2011.01.034
Herdt, T. H., & Smith, J. C. (1996). Blood-lipid and lactation-stage factors affecting serum vitamin e concentrations and vitamin E cholesterol ratios in dairy cattle. Journal of Veterinary Diagnostic Investigation, 8, 228-232. https://doi.org/10.1177/104063879600800213
Hogan, J. S., Weiss, W. P., & Smith, K. L. (1993). Role of vitamin E and selenium in host defense against mastitis. Journal of Dairy Science, 76, 2795-2803. https://doi.org/10.3168/jds.S0022-0302(93)77618-3
Ibrahim, W., Lee, U. S., Yeh, C. C., Szabo, J., Bruckner, G., & Chow, C. K. (1997). Oxidative stress and antioxidant status in mouse liver: Effects of dietary lipid, vitamin E and iron. The Journal of Nutrition, 127, 1401-1406. https://doi.org/10.1093/jn/127.7.1401
Jiang, Q., Wu, B. Y., & Chen, X. D. (2012). Effect of oleic acid on the proliferation and secretion of pro-inflammatory mediators of human normal fibroblasts and scar fibroblasts. Zhonghua Shao Shang Za Zhi = Zhonghua Shaoshang Zazhi = Chinese Journal of Burns, 28, 444-450.
Jorritsma, R., César, M. L., Hermans, J. T., Kruitwagen, C. L. J. J., Vos, P. L. A. M., & Kruip, T. A. M. (2004). Effects of non-esterified fatty acids on bovine granulosa cells and developmental potential of oocytes in vitro. Animal Reproduction Science, 81, 225-235. https://doi.org/10.1016/j.anireprosci.2003.10.005
LeBlanc, S. J., Herdt, T. H., Seymour, W. M., Duffield, T. F., & Leslie, K. E. (2004). Peripartum serum vitamin E, retinol, and beta-carotene in dairy cattle and their associations with disease. Journal of Dairy Science, 87, 609-619. https://doi.org/10.3168/jds.S0022-0302(04)73203-8
Leroy, J. L. M. R., Vanholder, T., Mateusen, B., Christophe, A., Opsomer, G., de Kruif, A., Genicot, G., & Van Soom, A. (2005). Non-esterified fatty acids in follicular fluid of dairy cows and their effect on developmental capacity of bovine oocytes in vitro. Reproduction, 130, 485-495. https://doi.org/10.1530/rep.1.00735
Lisuzzo, A., Bonelli, F., Sgorbini, M., Nocera, I., Cento, G., Mazzotta, E., Turini, L., Martini, M., Salari, F., Morgante, M., Badon, T., & Fiore, E. (2022). Differences of the plasma total lipid fraction from pre-foaling to post-foaling period in donkeys. Animals, 12(3), 304. https://doi.org/10.3390/ani12030304
Lisuzzo, A., Fiore, F., Harvatine, K., Mazzotta, E., Berlanda, M., Spissu, N., Badon, T., Contiero, B., Moscati, L., & Fiore, E. (2022). Changes in plasma fatty acids profile in hyperketonemic ewes during early lactation: A preliminary study. Scientific Reports, 12(1), 17017. https://doi.org/10.1038/s41598-022-21088-5
Lisuzzo, A., Laghi, L., Fiore, F., Harvatine, K., Mazzotta, E., Faillace, V., Spissu, N., Zhu, C., Moscati, L., & Fiore, E. (2022). Evaluation of the metabolomic profile through 1H-NMR spectroscopy in ewes affected by postpartum hyperketonemia. Scientific Reports, 12(1), 16463. https://doi.org/10.1038/s41598-022-20371-9
Loetchutinat, C., Kothan, S., Dechsupa, S., Meesungnoen, J., Jay-Gerin, J. P., & Mankhetkorn, S. (2005). Spectrofluorometric determination of intracellular levels of reactive oxygen species in drug-sensitive and drug-resistant cancer cells using the 2′,7′-dichlorofluorescein diacetate assay. Radiation Physics and Chemistry, 72, 323-331.
Miller, J. K., Brzezinska-Slebodzinska, E., & Madsen, F. C. (1993). Oxidative stress, antioxidants, and animal function. Journal of Dairy Science, 76, 2812-2823. https://doi.org/10.3168/jds.S0022-0302(93)77620-1
Mohamed, T., Oikawa, S., Iwasaki, Y., Mizunuma, Y., Takehana, K., Endoh, D., Kurosawa, T., & Sato, H. (2004). Metabolic profiles and bile acid extraction rate in the liver of cows with fasting-induced hepatic lipidosis. Journal of Veterinary Medicine, 51, 113-118. https://doi.org/10.1111/j.1439-0442.2004.00614.x
Ohkawa, H., Ohishi, N., & Yagi, K. (1979). Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry, 95, 351-358.
Ono, M., Ohtaki, T., Tanemura, K., Ishii, M., Watanabe, G., Taya, K., & Tsumagari, S. (2011). Effect of short-term fasting on hepatic steroid hormone metabolism in cows. Journal of Veterinary Medical Science, 73, 1145-1150. https://doi.org/10.1292/jvms.10-0578
Pontes, G. C. S., Monteiro, P. L. J., Prata, A. B., Guardieiro, M. M., Pinto, D. A. M., Fernandes, G. O., Wiltbank, M. C., Santos, J. E. P., & Sartori, R. (2015). Effect of injectable vitamin E on incidence of retained fetal membranes and reproductive performance of dairy cows. Journal of Dairy Science, 98, 2437-2449. https://doi.org/10.3168/jds.2014-8886
Rukkwamsuk, T., Geelen, M. J. H., Kruip, T. A. M., & Wensing, T. (2000). Interrelation of fatty acid composition in adipose tissue, serum, and liver of dairy cows during the development of fatty liver postpartum. Journal of Dairy Science, 83, 52-59. https://doi.org/10.3168/jds.S0022-0302(00)74854-5
Sharma, A., Baddela, V. S., Becker, F., Dannenberger, D., Viergutz, T., & Vanselow, J. (2019). Elevated free fatty acids affect bovine granulosa cell function: A molecular cue for compromised reproduction during negative energy balance. Endocrine Connections, 8, 493-505. https://doi.org/10.1530/EC-19-0011
Sordillo, L. M., & Raphael, W. (2013). Significance of metabolic stress, lipid mobilization, and inflammation on transition cow disorders. Veterinary Clinics: Food Animal Practice, 29, 267-278. https://doi.org/10.1016/j.cvfa.2013.03.002
Sutton-Mcdowall, M. L., Wu, L. L. Y., Purdey, M., Abell, A. D., Ewa, M., Macmillan, K. L., Thompson, J. G., & Robker, R. L. (2016). Nonesterified fatty acid-induced endoplasmic reticulum stress in cattle cumulus oocyte complexes alters cell metabolism and developmental competence. Biology of Reproduction, 94, 1-9. https://doi.org/10.1095/biolreprod.115.131862
Tessari, R., Mazzotta, E., Blasi, F., Morgante, M., Badon, T., Bedin, S., Fabbri, G., Lisuzzo, A., Contiero, B., Fiore, E., & Berlanda, M. (2021). Milk fatty acids as biomarkers of metabolic diseases in dairy cows identified through thin layer chromatography and gas chromatographic techniques (TLC-GC). Large Animal Review, 27(4), 187-193.
Turk, R., Podpečan, O., Mrkun, J., Kosec, M., Flegar-Meštrić, Z., Perkov, S., Starič, J., Robić, M., Belić, M., & Zrimšek, P. (2013). Lipid mobilization and oxidative stress as metabolic adaptation processes in dairy heifers during transition period. Animal Reproduction Science, 141, 109-115. https://doi.org/10.1016/j.anireprosci.2013.07.014
Van Hoeck, V., Leroy, J. L. M. R., Alvarez, M. A., Rizos, D., Gutierrez-Adan, A., Schnorbusch, K., Bols, P. E. J., Leese, H. J., & Sturmey, R. G. (2013). Oocyte developmental failure in response to elevated nonesterified fatty acid concentrations: Mechanistic insights. Reproduction, 145, 33-44. https://doi.org/10.1530/REP-12-0174
Van Hoeck, V., Sturmey, R. G., Bermejo-Alvarez, P., Rizos, D., Gutierrez-Adan, A., Leese, H. J., Bols, P. E. J., & Leroy, J. L. M. R. (2011). Elevated non-esterified fatty acid concentrations during bovine oocyte maturation compromise early embryo physiology. PLoS One, 6, e23183. https://doi.org/10.1371/journal.pone.0023183
Vanholder, T., Leroy, J. L. M. R., Van Soom, A., Opsomer, G., Maes, D., Coryn, M., & Kruif, A. (2005). Effect of non-esterified fatty acids on bovine granulosa cell steroidogenesis and proliferation in vitro. Animal Reproduction Science, 87, 33-44. https://doi.org/10.1016/j.anireprosci.2004.09.006
Wang, X., & Quinn, P. J. (1999). Vitamin E and its function in membranes. Progress in Lipid Research, 38, 309-336. https://doi.org/10.1016/s0163-7827(99)00008-9
Weiss, W. P., Hogan, J. S., Todhunter, D. A., & Smith, K. L. (1997). Effect of vitamin E supplementation in diets with a low concentration of selenium on mammary gland health of dairy cows. Journal of Dairy Science, 80, 1728-1737. https://doi.org/10.3168/jds.S0022-0302(97)76105
Yenuganti, V. R., Viergutz, T., & Vanselow, J. (2016). Oleic acid induces specific alterations in the morphology, gene expression and steroid hormone production of cultured bovine granulosa cells. General and Comparative Endocrinology, 232, 134-144. https://doi.org/10.1016/j.ygcen.2016.04