Manganese enhances the expression of the manganese superoxide dismutase in cultured primary chick embryonic myocardial cells

doi:10.1016/S2095-3119(16)61527-7

摘要/Abstract

Abstract: In the present study, the effect of manganese (Mn) on antioxidant status and the expression of the manganese superoxide dismutase (MnSOD) gene in cultured primary myocardial cells collected from the chick embryos was investigated. The hypothesis that Mn supplementation would enhance the expression of MnSOD in cultured primary myocardial cells of chick embryos was tested. Eggs collected from Mn-depleted Arbor Acres laying breeder hens were incubated for 10 days and then myocardial cells were isolated and cultivated for 8 days. The embryonic myocardial cells on day 6 were treated with Mn in the cell culture medium at different time points when the proportion of cells showing spontaneous contraction was over 95% after the 3-day primary culture. A completely randomized design involving a 3 Mn levels (0, 0.5 and 1.0 mmol L^–1)×3 incubation time points (12, 24 and 48 h) factorial arrangement of treatments (n=6) was used in the current experiment. The results showed that MnSOD activity and mRNA expression level were induced by Mn and increased with incubation time, which supported the hypothesis that Mn would enhance the expression of the MnSOD gene, and thus might protect myocardial cells from oxidative stress during the chick embryonic development.

Key words: manganese , MnSOD , expressions , cultured primary myocardial cells , chick embryos

. [J]. Journal of Integrative Agriculture, 2017, 16(09): 2038-2046.

QIN Shi-zhen, LIAO Xiu-dong, LU Lin, ZHANG Li-yang, XI Lin, GUO Yan-li, LUO Xu-gang. Manganese enhances the expression of the manganese superoxide dismutase in cultured primary chick embryonic myocardial cells[J]. Journal of Integrative Agriculture, 2017, 16(09): 2038-2046.

参考文献

Akashi M, Hachiya M, Paquette R L, Osawa Y, Shimizu S, Suzuki G. 1995. Irradiation increases manganese superoxide dismutase mRNA levels in human fibroblasts. Possible mechanisms for its accumulation. Journal of Biological Chemistry, 270, 15864–15869.

AOAC (Association of Official Analytical Chemists). 1990. Official Methods of Analysis. 9th ed. Association of Offiial Analytical Chemists, Arlington, Virginia, USA.

Arechiga C F, Ealy A D, Hansen P J. 1995. Evidence that glutathione is involved in thermotolerance of preimplantation murine embryos. Biology of Reproduction, 52, 1296–1301.

Bao E, Sultan K R, Nowak B, Hartung J. 2008. Expression and distribution of heat shock proteins in the heart of transported pigs. Cell Stress Chaperones, 13, 459–466.

Bianchi A, Becuwe P, Franck P, Dauca M. 2002. Induction of Mnsod gene by arachidonic acid is mediated by reactive oxygen species and p38 MAPK signaling pathway in human HepG2 hepatoma cells. Free Radical Biology and Medicine, 32, 1132–1142.

Brumell J H, Burkhardt A L, Bolen J B, Grinstein S. 1996. Endogenous reactive oxygen intermediates activate tyrosine kinases in human neutrophils. Journal of Biological Chemistry, 271, 1455–1461.

Buyukokuroglu M E, Taysi S, Buyukavci M, Bakan E. 2004. Prevention of acute adriamycin cardiotoxicity by dantrolene in rats. Human & Experimental Toxicology, 23, 251–256.

Cederberg J, Siman C M, Eriksson U J. 2001. Combined treatment with vitamin E and vitamin C decreases oxidative stress and improves fetal outcome in experimental diabetic pregnancy. Pediatric Research, 49, 755–762.

Cyrne L, Martins L, Fernandes L, Marinho H S. 2003. Regulation of antioxidant enzymes gene expression in the yeast Saccharomyces cerevisiae during stationary phase. Free Radical Biology and Medicine, 34, 385–393.

Davis C D, Greger J L. 1992. Longitudinal changes of manganese-dependent superoxide dismutase and other indexes of manganese and iron status in women. The American Journal of Clinical Nutrition, 55, 747–752.

Eastgate J, Moreb J, Nick H S, Suzuki K, Taniguchi N, Zucali J R. 1993. A role for manganese superoxide dismutase in radioprotection of hematopoietic stem cells by interleukin-1. Blood, 81, 639–646.

Fridovich I. 1978. Superoxide dismutases: defence against endogenous superoxide radical. Oxygen Free Radicals and Tissue Damage, 65, 77–93.

Fridovich I. 1995. Superoxide radical and superoxide dismutases. Annual Review of Biochemistry, 64, 97–112.

Fujii J, Taniguchi N. 1991. Phorbol ester induces manganese-superoxide dismutase in tumor necrosis factor-resistant cells. Journal of Biological Chemistry, 266, 23142–23146.

Gallup W D, Norris C. 1939. The effect of a deficiency of manganese in the diet of the hen. Poultry Science, 18, 83–88.

Gao T Q, Wang F N, Li S F, Luo X G, Zhang K. 2011. Manganese regulates manganese-containing superoxide dismutase (MnSOD) expression in the primary broiler myocardial cells. Biological Trace Element Research, 144, 695–704.

Georgopoulos C, Welch W. 1993. Role of the major heat shock proteins as molecular chaperones. Annual Review of Cell Biology, 9, 601–634.

Ishiyama H, Ogino K, Hobara T. 1995. Role of Kupffer cells in rat liver injury induced by diethyldithiocarbamate. European Journal of Pharmacology: Environmental Toxicology and Pharmacology, 292, 135–141.

Iwamoto S, Takeda K. 1990. Possible cytotoxic mechanisms of TNF in vitro. Human Cell, 3, 107–112.

Jadhav J T, Kengar S. 2016. Influence of hydrogen peroxide induced oxidative stress on survival rate of early chick embryo development. International Journal of Bioassays, 5, 4603–4606.

Kasten T P, Settle S L, Misko T P, Riley D P, Weiss R H, Currie M G, Nickols G A. 1995. Potentiation of nitric oxide-mediated vascular relaxation by SC52608, a superoxide dismutase mimic. Experimental Biology and Medicine, 208, 170–177.

Li S F, Lu L, Hao S F, Wang Y P, Zhang L Y, Liu S B, Liu B, Li K, Luo X G. 2011. Dietary manganese modulates expression of the manganese-containing superoxide dismutase gene in chickens. The Journal of Nutrition, 141, 189–194.

Li S F, Lu L, Liao X D, Gao T Q, Wang F N, Zhang L Y, Xi L, Liu S B, Luo X G. 2016. Manganese elevates manganese superoxide dismutase protein level through protein kinase C and protein tyrosine kinase. Biometals, 29, 265–274.

Li S F, Luo X G, Liu B, Crenshaw T D, Kuang X, Shao G Z, Yu S X. 2004. Use of chemical characteristics to predict the relative bioavailability of supplemental organic manganese sources for broilers. Journal of Animal Science, 82, 2352–2363.

Li S F, Luo X G, Lu L, Crenshaw T D, Bu Y Q, Liu B, Kuang X, Shao G Z, Yu S X. 2005. Bioavailability of organic manganese sources in broilers fed high dietary calcium. Animal Feed Science and Technolog, 124, 703–715.

Li S F, Luo X G, Lu L, Liu B, Kuang X, Shao G Z, Yu S X. 2008. Effect of intravenously injected manganese on the gene expression of manganese-containing superoxide dismutase in broilers. Poultry Science, 87, 2259–2265.

Lin Y H, Chiu J H, Tung H H, Tsou M T, Lui W Y, Wu C W. 2001. Preconditioning somatothermal stimulation on right seventh intercostal nerve territory increases hepatic heat shock protein 70 and protects the liver from ischemia-reperfusion injury in rats. Journal of Surgical Research, 99, 328–334.

Lindau-Shepard B, Shaffer J B, Del Vecchio P J. 1994. Overexpression of manganous superoxide dismutase (MnSOD) in pulmonary endothelial cells confers resistance to hyperoxia. Journal of Cellular Physiolog, 161, 237–242.

Luo X G, Li S F, Lu L, Liu B, Kuang X, Shao G Z, Yu S X. 2007. Gene expression of manganese-containing superoxide dismutase as a biomarker of manganese bioavailability for manganese sources in broilers. Poultry Science, 86, 888–894.

Luo X G, Su Q, Huang J C, Liu J X. 1991. A study on the optimal manganese (Mn) level in a practical diet of broiler chicks. Chinese Journal of Animal and Veterinary Sciences, 22, 313–317.

Luo X G, Su Q, Huang J C, Liu J X. 1992. Effects of manganese (Mn) deficiency on tissue, Mn-containing superoxide dismutase activity and its mitochondrial ultrastructures of broiler chicks fed a practical diet. Chinese Journal of Animal and Veterinary Sciences, 23, 97–101.

Marklund S. 1980. Distribution of CuZn superoxide dismutase and Mn superoxide dismutase in human tissues and extracellular fluids. Acta Physiologica Scandinavica (Suppl.), 492, 19–23.

McCord J M, Keele Jr B B, Fridovich I. 1971. An enzyme-based theory of obligate anaerobiosis: The physiological function of superoxide dismutase. Proceedings of the National Academy of Sciences of the United States of America, 68, 1024–1027.

Mitchell M A, Sandercock D A. 1995. Creatine kinase isoenzyme profiles in the plasma of the domestic fowl (Gallus domesticus): Effects of acute heat stress. Research in Veterinary Science, 59, 30–34.

NRC (National Research Council). 1994. Nutrient Requirements of Poultry. 9th ed. The National Academies Press, Washington, D.C. p. 40.

Oberley L W, Buettner G R. 1979. Role of superoxide dismutase in cancer: A review. Cancer Research, 39, 1141–1149.

Qadri I, Iwahashi M, Capasso J M, Hopken M W, Flores S, Schaack J, Simon F R. 2004. Induced oxidative stress and activated expression of manganese superoxide dismutase during hepatitis C virus replication: role of JNK, p38 MAPK and AP-1. Biochemical Journal, 378, 919–928.

Roberfroid M B, Calderon P B. 1995. Free Radicals and Oxidation Phenomena in Biological Systems. M. Dekker, New York.

Rogers R J, Monnier J M, Nick H S. 2001. Tumor necrosis factor-alpha selectively induces MnSOD expression via mitochondria-to-nucleus signaling, whereas interleukin-1 beta utilizes an alternative pathway. Journal of Biological Chemistry, 276, 20419–20427.

Saravanan G, Ponmurugan P, Sathiyavathi M, Vadivukkarasi S, Sengottuvelu S. 2013. Cardioprotective activity of Amaranthus viridis Linn: Effect on serum marker enzymes, cardiac troponin and antioxidant system in experimental myocardial infarcted rats. International Journal of Cardiology, 165, 494–498.

Savage J E. 1968. Trace minerals and avian reproduction. Federation Proceedings, 27, 927–931.

Starck J M. 1998. Avian Growth and Development: Evolution Within the Altricial-Precocial Spectrum (No.8). Oxford University, London.

Stephanz G B, Gwinner W, Cannon J K, Tisher C C, Nick H S. 1996. Heat-aggregated IgG and interleukin-1-beta stimulate manganese superoxide dismutase in mesangial cells. Experimental Nephrology, 4, 151–158.

Surai P, McDevitt R, Speake B, Noble R, Sparks N. 1998. Vitamin E transfer from the feed into the egg yolk: Effect of dietary supplementation. Proceedings of the Nutrition Society, 58, 29A.

Surai P F. 1999a. Tissue-specific changes in the activities of antioxidant enzymes during the development of the chicken embryo. British Poultry Science, 40, 397–405.

Surai P F. 1999b. Vitamin E in avian reproduction. Poultry and Avian Biology Reviews, 10, 1.

Surai P F. 2000. Effect of selenium and vitamin E content of the maternal diet on the antioxidant system of the yolk and the developing chick. British Poultry Science, 41, 235–243.

Thongphasuk J, Oberley L W, Oberley T D. 1999. Induction of superoxide dismutase and cytotoxicity by manganese in human breast cancer cells. Archives of Biochemistry and Biophysics, 365, 317–327.

Umaoka Y, Noda Y, Narimoto K, Mori T. 1992. Effects of oxygen toxicity on early development of mouse embryos. Molecular Reproduction and Development, 31, 28–33.

Valentine J F, Nick H S. 1992. Acute-phase induction of manganese superoxide dismutase in intestinal epithelial cell lines. Gastroenterology, 103, 905–912.

Visner G A, Block E R, Burr I M, Nick H S. 1991. Regulation of manganese superoxide dismutase in porcine pulmonary artery endothelial cells. American Journal of Physiology-Lung Cellular and Molecular Physiology, 260, L444–L449.

Visner G A, Chesrown S E, Monnier J, Ryan U S, Nick H S. 1992. Regulation of manganese superoxide dismutase: IL-1 and TNF induction in pulmonary artery and microvascular endothelial cells. Biochemical and Biophysical Research Communications, 188, 453–462.

Wada K, Fujibayashi Y, Yokoyama A. 1994. Copper(II)[2,3-butanedionebis(N4-methylthiosemicarbazone)], a stable superoxide dismutase-like copper complex with high membrane penetrability. Archives of Biochemistry and Biophysics, 310, 1–5.

Whitsett J A, Clark J C, Wispe J R, Pryhuber G S. 1992. Effects of TNF-alpha and phorbol ester on human surfactant protein and MnSOD gene transcription in vitro. American Journal of Physiology (Lung Cellular and Molecular Physiology), 262, L688–L693.

Winyard P G, Moody C J, Jacob C. 2005. Oxidative activation of antioxidant defence. Trends in Biochemical Sciences, 30, 453–461.

Wong G H W. 1995. Protective roles of cytokines against radiation - induction of mitochondrial mnsod. Biochimica et Biophysica Acta (BBA, Molecular Basis of Disease), 1271, 205–209.

Wong G H, Elwell J H, Oberley L W, Goeddel D V. 1989. Manganous superoxide dismutase is essential for cellular resistance to cytotoxicity of tumor necrosis factor. Cell, 58, 923–931.

Wu L M, Xi Z F, Guo R, Liu S R, Yang S J, Liu D Y, Dong S Q, Guo D Z. 2013. Exogenous ARC down-regulates caspase-3 expression and inhibits apoptosis of broiler chicken cardiomyocytes exposed to hydrogen peroxide. Avian Pathology, 42, 32–37.

Xie J J, Tang L, Lu L, Zhang LY, Xi L, Liu H C, Odle J, Luo X G. 2014. Differential expression of heat shock transcription factors and heat shock proteins after acute and chronic heat stress in laying chickens (Gallus gallus). PLoS ONE, 9, e102204.

Zhang M, Yue Z H, Liu Z J, Islam A, Rehana B, Tang S, Bao E D, Hartung J. 2012. Hsp70 and HSF-1 expression is altered in the tissues of pigs transported for various periods of times. Journal of Veterinary Science, 13, 253–259.

Zhong W X, Oberley L W, Oberley T D, Yan T, Domann F E, StClair D K. 1996. Inhibition of cell growth and sensitization to oxidative damage by overexpression of manganese superoxide dismutase in rat glioma cells. Cell Growth and Differentiation (Publication American Association for Cancer Research), 7, 1175–1186.

Zhu Y W, Lu L, Li W X, Zhang L Y, Ji C, Lin X, Liu H C, Odle J, Luo X G. 2015a. Effect of dietary manganese on antioxidant status and expression levels of heat-shock proteins and factors in tissues of laying broiler breeders under normal and high environmental temperatures. British Journal of Nutrition, 114, 1965–1974.

Zhu Y W, Lu L, Li W X, Zhang L Y, Ji C, Lin X, Liu H C, Odle J, Luo X G. 2015b. Effects of maternal dietary manganese and incubation temperature on hatchability, antioxidant status, and expression of heat shock proteins in chick embryos. Journal of Animal Science, 93, 5725–5734