Protection of bovine mammary epithelial cells from hydrogen peroxide-induced oxidative cell damage by selenium

https://doi.org/10.17221/76/2017-CJASCitation:Guo Y.M., Gong J., Zheng Y.G., Shi B.L., Guo X.Y., Yan S.M. (2018): Protection of bovine mammary epithelial cells from hydrogen peroxide-induced oxidative cell damage by selenium. Czech J. Anim. Sci., 63: 94-102.
download PDF

The uncontrolled release of arachidonic acid (ARA) and its metabolism by lipoxygenase (LOX) pathway can induce and aggravate cellular oxidative stress. Selenium (Se) is an integral part of some antioxidative selenoproteins and may protect cells from oxidative damage by modulating ARA release and metabolism. The present study aimed to investigate the protective response of Se against hydrogen peroxide (H2O2)-induced oxidative damage in bovine mammary epithelial cells (BMECs). The BMECs were incubated for 24 h in serum-free medium and then divided into four groups randomly. The cells in groups 1 and 2 were subsequently incubated for 30 h in serum-free medium containing 0 (control) and 50 nM Se (Se treatment group). The cells in groups 3 and 4 were incubated for 24 h in serum-free medium containing 0 and 50 nM Se, and then treated with 600 μM H2O2 for 6 h (H2O2 damage group and Se prevention group). The results showed that Se attenuated the H2O2-induced production of reactive oxygen species and the decrease of antioxidative enzymes as glutathione peroxidase (GPX), thioredoxin reductase (TrxR), selenoprotein P (SelP), superoxide dismutase, and catalase in BMECs. The preventive effects of Se on the decrease of selenoprotein activity were demonstrated further by the increase of mRNA expression for GPX1, TrxR1, and SelP, and protein expression for GPX1 and TrxR1. Pretreatment of cells with Se inhibited the H2O2-induced increase of mRNA expressions and activities for cytosolic phospholipase A2 and 5-lipoxygenase, ARA release, and 15-hydroperoxyeicosatetraenoic acid production. Se also blocked the H2O2-induced activation of p38 mitogen-activated protein kinase (MAPK) and c-Jun N-terminal kinase but not that of extracellular signal-regulated kinase. These results suggested that Se may protect BMECs against H2O2-induced oxidative damage by increasing selenoproteins synthesis, inhibiting MAPK pathway, and then decreasing ARA release and its metabolism by LOX pathway.

References:
Aitken S.L., Karcher E.L., Rezamand P., Gandy J.C., VandeHaar M.J., Capuco A.V., Sordillo L.M. (2009): Evaluation of antioxidant and proinflammatory gene expression in bovine mammary tissue during the periparturient period. Journal of Dairy Science, 92, 589-598  https://doi.org/10.3168/jds.2008-1551
 
Bi Chong-Liang, Wang Heng, Wang Yin-Jie, Sun Jun, Dong Jun-Sheng, Meng Xia, Li Jian-Ji (2016): Selenium inhibits Staphylococcus aureus -induced inflammation by suppressing the activation of the NF-κB and MAPK signalling pathways in RAW264.7 macrophages. European Journal of Pharmacology, 780, 159-165  https://doi.org/10.1016/j.ejphar.2016.03.044
 
Bruzelius K., Hoac T., Sundler R., Önning G., Åkesson B. (2007): Occurrence of Selenoprotein Enzyme Activities and mRNA in Bovine Mammary Tissue. Journal of Dairy Science, 90, 918-927  https://doi.org/10.3168/jds.S0022-0302(07)71575-8
 
CAMPS MONTSERRAT, NICHOLS ANTON, ARKINSTALL STEVE (2000): Dual specificity phosphatases: a gene family for control of MAP kinase function. The FASEB Journal, 14, 6-16  https://doi.org/10.1096/fasebj.14.1.6
 
Chen Yiyan, Chen Chonghong (2011): Corilagin prevents tert-butyl hydroperoxide-induced oxidative stress injury in cultured N9 murine microglia cells. Neurochemistry International, 59, 290-296  https://doi.org/10.1016/j.neuint.2011.05.020
 
Cyrus C (): 12/15-Lipoxygenase, Oxidative Modification of LDL and Atherogenesis. Trends in Cardiovascular Medicine, 11, 116-124  https://doi.org/10.1016/S1050-1738(01)00096-2
 
HARA Shuntaro, SHOJI Yasuko, SAKURAI Atsuko, YUASA Kouji, HIMENO Seiichiro, IMURA Nobumasa (): Effects of Selenium Deficiency on Expression of Selenoproteins in Bovine Arterial Endothelial Cells.. Biological & Pharmaceutical Bulletin, 24, 754-759  https://doi.org/10.1248/bpb.24.754
 
Hill K.E., Xia Y., Akesson B., Boeglin M.E., Burk R.F. (1996): Selenoprotein P concentration in plasma is an index of selenium status in selenium-deficient and selenium-supplemented Chinese subjects. Journal of Nutrition, 126, 138–145.
 
Hill Kristina E., McCollum Gary W., Burk Raymond F. (1997): Determination of Thioredoxin Reductase Activity in Rat Liver Supernatant. Analytical Biochemistry, 253, 123-125  https://doi.org/10.1006/abio.1997.2373
 
Jagnandan Davin, Church Jarrod E., Banfi Botond, Stuehr Dennis J., Marrero Mario B., Fulton David J. R. (2007): Novel Mechanism of Activation of NADPH Oxidase 5. Journal of Biological Chemistry, 282, 6494-6507  https://doi.org/10.1074/jbc.M608966200
 
Jin Xiaolu, Wang Kai, Liu Hongyun, Hu Fuliang, Zhao Fengqi, Liu Jianxin (2016): Protection of Bovine Mammary Epithelial Cells from Hydrogen Peroxide-Induced Oxidative Cell Damage by Resveratrol. Oxidative Medicine and Cellular Longevity, 2016, 1-15  https://doi.org/10.1155/2016/2572175
 
Kim Sang Hyun, Johnson Victor J, Sharma Raghubir P (2002): Mercury inhibits nitric oxide production but activates proinflammatory cytokine expression in murine macrophage: differential modulation of NF-κB and p38 MAPK signaling pathways. Nitric Oxide, 7, 67-74  https://doi.org/10.1016/S1089-8603(02)00008-3
 
Kim Sang Hyun, Johnson Victor J., Shin Tae-Yong, Sharma Raghubir P. (2016): Selenium Attenuates Lipopolysaccharide-Induced Oxidative Stress Responses Through Modulation of p38 MAPK and NF-κB Signaling Pathways. Experimental Biology and Medicine, 229, 203-213  https://doi.org/10.1177/153537020422900209
 
Korbecki J., Baranowska-Bosiacka I., Gutowska I., Chlubek D. (2013): The effect of reactive oxygen species on the synthesis of prostanoids from arachidonic acid. Journal of Basic and Clinical Physiology and Pharmacology, 64, 409–421.
 
Kurosawa Takeshi, Nakamura Hiroyuki, Yamaura Erika, Fujino Hiromichi, Matsuzawa Yasuo, Kawashima Tatsuo, Murayama Toshihiko (2009): Cytotoxicity induced by inhibition of thioredoxin reductases via multiple signaling pathways: Role of cytosolic phospholipase A 2 α-dependent and -independent release of arachidonic acid. Journal of Cellular Physiology, 219, 606-616  https://doi.org/10.1002/jcp.21703
 
Maccarrone Mauro, Ranalli Marco, Bellincampi Lorenza, Salucci Maria Luisa, Sabatini Stefania, Melino Gerry, Finazzi-Agrò Alessandro (2000): Activation of Different Lipoxygenase Isozymes Induces Apoptosis in Human Erythroleukemia and Neuroblastoma Cells. Biochemical and Biophysical Research Communications, 272, 345-350  https://doi.org/10.1006/bbrc.2000.2597
 
MILLER Sue, WALKER Simon W., ARTHUR John R., NICOL Fergus, PICKARD Karen, LEWIN Michelle H., HOWIE A. Forbes, BECKETT Geoffrey J. (2001): Selenite protects human endothelial cells from oxidative damage and induces thioredoxin reductase. Clinical Science, 100, 543-550  https://doi.org/10.1042/cs1000543
 
Miranda S.G., Wang Y.J., Purdie N.G., Osborne V.R., Coomber B.L., Cant J.P. (2009): Selenomethionine stimulates expression of glutathione peroxidase 1 and 3 and growth of bovine mammary epithelial cells in primary culture. Journal of Dairy Science, 92, 2670-2683  https://doi.org/10.3168/jds.2008-1901
 
Miranda S.G., Purdie N.G., Osborne V.R., Coomber B.L., Cant J.P. (2011): Selenomethionine increases proliferation and reduces apoptosis in bovine mammary epithelial cells under oxidative stress. Journal of Dairy Science, 94, 165-173  https://doi.org/10.3168/jds.2010-3366
 
Piotrowska-Tomala K.K., Siemieniuch M.J., Szóstek A.Z., Korzekwa A.J., Woclawek-Potocka I., Galváo A.M., Okuda K., Skarzynski D.J. (2012): Lipopolysaccharides, cytokines, and nitric oxide affect secretion of prostaglandins and leukotrienes by bovine mammary gland epithelial cells. Domestic Animal Endocrinology, 43, 278-288  https://doi.org/10.1016/j.domaniend.2012.04.005
 
Schönfeld Peter, Wojtczak Lech (2007): Fatty acids decrease mitochondrial generation of reactive oxygen species at the reverse electron transport but increase it at the forward transport. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1767, 1032-1040  https://doi.org/10.1016/j.bbabio.2007.04.005
 
Seguineau Catherine, Racotta Ilie S., Palacios Elena, Delaporte Maryse, Moal Jeanne, Soudant Philippe (2011): The influence of dietary supplementation of arachidonic acid on prostaglandin production and oxidative stress in the Pacific oyster Crassostrea gigas. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 160, 87-93  https://doi.org/10.1016/j.cbpa.2011.05.011
 
Sordillo Lorraine M. (2005): Factors affecting mammary gland immunity and mastitis susceptibility. Livestock Production Science, 98, 89-99  https://doi.org/10.1016/j.livprodsci.2005.10.017
 
Sordillo L.M., O’Boyle N., Gandy J.C., Corl C.M., Hamilton E. (2007): Shifts in Thioredoxin Reductase Activity and Oxidant Status in Mononuclear Cells Obtained from Transition Dairy Cattle. Journal of Dairy Science, 90, 1186-1192  https://doi.org/10.3168/jds.S0022-0302(07)71605-3
 
Sordillo Lorraine M., Streicher Katie L., Mullarky Isis K., Gandy Jeffery C., Trigona Wendy, Corl Chris M. (2008): Selenium inhibits 15-hydroperoxyoctadecadienoic acid-induced intracellular adhesion molecule expression in aortic endothelial cells. Free Radical Biology and Medicine, 44, 34-43  https://doi.org/10.1016/j.freeradbiomed.2007.09.002
 
STRAIF Dietlind, WERZ Oliver, KELLNER Roland, BAHR Ute, STEINHILBER Dieter (2000): Glutathione peroxidase-1 but not -4 is involved in the regulation of cellular 5-lipoxygenase activity in monocytic cells. Biochemical Journal, 349, 455-461  https://doi.org/10.1042/bj3490455
 
Weiss W.P., Hogan J.S., Smith K.L., Hoblet K.H. (1990): Relationships Among Selenium, Vitamin E, and Mammary Gland Health in Commercial Dairy Herds. Journal of Dairy Science, 73, 381-390  https://doi.org/10.3168/jds.S0022-0302(90)78684-5
 
Yang Feng, Li Xiao (2015): Role of antioxidant vitamins and trace elements in mastitis in dairy cows. Journal of Advanced Veterinary and Animal Research, 2, 1-  https://doi.org/10.5455/javar.2015.b48
 
Yang L., You Y., Lin Z., Lin Y. (2010): Protective effects of ganoderma lucidum polysaccharides peptide on human umbilical vein endothelial cells injury by reactive oxygen species. Chinese Pharmacological Bulletin, 26, 657–660.
 
Zhang Wen, Zhang Runxiang, Wang Tiancheng, Jiang Haichao, Guo Mengyao, Zhou Ershun, Sun Yong, Yang Zhengtao, Xu Shiwen, Cao Yongguo, Zhang Naisheng (2014): Selenium Inhibits LPS-Induced Pro-inflammatory Gene Expression by Modulating MAPK and NF-κB Signaling Pathways in Mouse Mammary Epithelial Cells in Primary Culture. Inflammation, 37, 478-485  https://doi.org/10.1007/s10753-013-9761-5
 
download PDF

© 2021 Czech Academy of Agricultural Sciences | Prohlášení o přístupnosti