α-硫辛酸抗氧化作用机制及其在动物生殖细胞和早期胚胎中抗氧化作用的研究进展
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摘要
活性氧(ROS)引起的氧化应激是动物生殖细胞和早期胚胎发生凋亡或永久性发育阻滞的主要原因之一。因此,在体外培养系统中添加抗氧化剂成为降低氧化应激对动物生殖细胞损伤和提高早期胚胎发育能力的方法之一。α-硫辛酸(LA)作为一种强抗氧化剂,可以通过直接清除自由基、螯合金属离子并促进其他抗氧化物质形成从而发挥抗氧化作用。在生殖细胞和早期胚胎中,LA可以通过降低ROS水平、促进抗氧化酶活性和线粒体活性来提高生殖细胞质量和早期胚胎发育能力。本文概述了LA抗氧化作用机制及其在动物生殖细胞和早期胚胎发育过程中抗氧化作用的研究进展,为进一步探究LA抗氧化作用的分子机制提供理论依据和研究思路。
It was reported that oxidative stress caused by the reactive oxygen species(ROS) was one of the factors of gametes and early embryo apoptosis or permanent developmental block. Hence, adding antioxidants to the in vitro culture system becomes one of the effective methods of decreasing the damages of oxidative stress and improving the developmental competence of early embryos. As a strong antioxidant, alpha lipoic acid(LA) plays an important role in antioxidation through scavenging free radicals directly, chelating metal ions and promoting the formation of other antioxidants etc. LA can improve the quality of gametes and the developmental capacity of early embryo through reducing the ROS level, increasing the activities of antioxidant enzymes and elevating the potential of mitochondria. In order to provide theoretical basis and research ideas for further study, the mechanisms of antioxidant activity of LA and its research progress on gametes and embryos were reviewed in this paper.
It was reported that oxidative stress caused by the reactive oxygen species(ROS) was one of the factors of gametes and early embryo apoptosis or permanent developmental block. Hence, adding antioxidants to the in vitro culture system becomes one of the effective methods of decreasing the damages of oxidative stress and improving the developmental competence of early embryos. As a strong antioxidant, alpha lipoic acid(LA) plays an important role in antioxidation through scavenging free radicals directly, chelating metal ions and promoting the formation of other antioxidants etc. LA can improve the quality of gametes and the developmental capacity of early embryo through reducing the ROS level, increasing the activities of antioxidant enzymes and elevating the potential of mitochondria. In order to provide theoretical basis and research ideas for further study, the mechanisms of antioxidant activity of LA and its research progress on gametes and embryos were reviewed in this paper.
引文
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[6]Li C Y, Zhao Y H, Hao H S, et al. Resveratrol significantlyimproves the fertilisation capacity of bovine sex-sorted semenby inhibiting apoptosis and lipid peroxidation[J]. Sci Rep, 2018,8(1):7603.
[7]Zhao X M, Wang N, Hao H S, et al. Melatonin improves thefertilization capacity and developmental ability of bovineoocytes by regulating:cytoplasmic maturation events[J]. JPineal Res, 2018, 64(1)12445.
[8]Haritoglou C, Gerss J, Hammes H P, et al. Alpha-lipoic acid forthe prevention of diabetic macular edema[J]. Ophthalmologica,2011, 226(3):127-137.
[9]Vasdev S, Gill V, Longerich L, et al. Salt-induced hyperten-sionin WKY rats:prevention by alpha-lipoic acid supplementation[J].Mol Cell Biochem, 2003, 254(1-2):319-326.
[10]Ibrahim S F, Osman K, Das S, et al. A study of the antioxidanteffect of alpha lipoic acids on sperm quality[J]. Clinics, 2008,63(4):545-550.
[11]Zhang H, Wu B, Liu H, et al. Improving development of clonedgoat embryos by supplementing alpha-lipoic acid to oocyte invitro maturation medium[J]. Theriogenology, 2013, 80(3):228-233.
[12]Vergely C, Maupoil W, Clermont G, et al. Identification andqantification of free radicals during myocardial ischemia andreperfusion using electron paramagnetic resonance spectroscopy[J].Arch Biochem Biophys, 2003, 420(2):209-216.
[13]de Lamirande E, Lamothe G. Reactive oxygen-induced reactiveoxygen formation during human sperm capacitation[J]. FreeRadic Biol Med, 2009, 46(4):502-510.
[14]Shi T Y, Chen G, Huang X, et al. Effects of reactive oxygenspecies from activated leucocytes on human sperm motility,viability and morphology[J]. Andrologia, 2012, 44(Suppl 1):696-703.
[15]Luczaj W, Skrzydlewska E. DNA damage caused by lipid per-oxidation products[J]. Cell Mol Biol Lett, 2003, 8(2):391-413.
[16]Agarwal A, Said T M, Bedaiwy M A, et al. Oxidative stressin an assisted reproductive techniques setting[J]. Fertil Steril,2006, 86(3):503-512.
[17]Sapanidou V, Taitzoglou I, Tsakmakidis I, et al. Antioxidant effectof crocin on bovine sperm quality and in vitro fertilization[J].Theriogenology, 2015, 84(8):1273-1282.
[18]Cummins J M, Jequier A M, Kan R. Molecular biology of humanmale infertility:links with aging, mitochondrial genetics, andoxidative stress?[J]. Mol Reprod Dev, 1994, 37(3):345-362.
[19]Alexiou M, Leese H J. Purine utilisation, de novo synthesisand degradation in mouse preimplantation embryos[J].Development, 1992, 114(1):185-192.
[20]Raha S, Robinson B H. Mitochondria, oxygen free radicals, andapoptosis[J]. Am J Med Genet, 2001, 106(1):62-70.
[21]Liu L, Keefe D L. Cytoplasm mediates both development andoxidation-induced apoptotic cell death in mouse zygotes[J].Biol Reprod, 2000, 62(6):1828-1834.
[22]Tripathi A, Shrivastav T G, Chaube S K. An increase of gran-ulosa cell apoptosis mediates aqueous neem(Azadirachtaindica)leaf extract-induced oocyte apoptosis in rat[J]. Int JAppl Basic Med Res, 2013, 3(1):27-36.
[23]Ishii T, Miyazawa M, Takanashi Y, et al. Genetically inducedoxidative stress in mice causes thrombocytosis, splenomegalyand placental angiodysplasia that leads to recurrent abortion[J].Redox Biology, 2014, 2:679-685.
[24]Kitagawa Y, Suzuki K, Yoneda A, et al. Effects of oxygen con-centration and antioxidants on the in vitro developmentalability, production of reactive oxygen species(ROS), and DNAfragmentation in porcine embryos[J]. Theriogenology, 2004,62(7):1186-1197.
[25]Favetta L A, St John E J, King W A, et al. High levels of p66(shc)and intracellular ROS in permanently arrested early embryos[J].Free Radic Biol Me, 2007, 42(8):1201-1210.
[26]Guerin P, El Mouatassim S, Menezo Y. Oxidative stress andprotection against reactive oxygen species in the pre-implantationembryo and its surroundings[J]. Hum Reprod Update, 2001, 7(2):175-189.
[27]Rinaudo P F, Giritharan G, Talbi S, et al. Effects of oxygentension on gene expression in preimplantation mouse embryos[J].Fertil Steril, 2006, 86:1252-1265, 1265 e1251-1236.
[28]Takahashi M, Keicho K, Takahashi H, et al. Effect of oxidativestress on development and DNA damage in in-vitro culturedbovine embryos by comet assay[J]. Theriogenology, 2000,54(1):137-145.
[29]Katz-Jaffe M G, Schoolcraft W B, Gardner D K. Analysis of proteinexpression(secretome)by human and mouse preimplantationembryos[J]. Fertil Steril, 2006, 86(3):678-685.
[30]Kovacic B, Vlaisavljevic V. Influence of atmospheric versus reducedoxygen concentration on development of human blastocysts in vitro:a prospective study on sibling oocytes[J]. Reprod Biomed Online,2008, 17(2):229-236.
[30]Lane M, Gardner D K. Understanding cellular disruptionsduring early embryo development that perturb viability andfetal development[J]. Reprod Fertil Dev, 2005, 17(3):371-378.
[31]Wale P L, Gardner D K. Oxygen regulates amino acid turnoverand carbohydrate uptake during the preimplantation period ofmouse embryo development[J]. Biol Reprod, 2012, 87(1):24,1-8.
[32]Gaspar R C, Arnold D R, Correa C A P, et al. Oxygen tensionaffects histone remodeling of in vitro-produced embryos in abovine model[J]. Theriogenology, 2015, 83(9):1408-1415.
[33]Kere M, Siriboon C, Lo N W, et al. Ascorbic acid improves thedevelopmental competence of porcine oocytes after parthenogeneticactivation and somatic cell nuclear transplantation[J]. J ReprodDev, 2013, 59(1):78-84.
[34]Farzollahi M, Tayefi-Nasrabadi H, Mohammadnejad D, et al.Supplementation of culture media with vitamin E improves mouseantral follicle maturation and embryo development from vitrifiedovarian tissue[J]. J Obstet Gynaecol Res, 2016, 42(5):526-535.
[35]Takeo S, Sato D, Kimura K, et al. Resveratrol improves themitochondrial function and fertilization outcome of bovineoocytes[J]. J Reprod Dev, 2014, 60(2):92-99.
[36]Wang Z G, Yu S D, Xu Z R. Effect of supplementation of greentea polyphenols on the developmental competence of bovineoocytes in vitro[J]. Braz J Med Biol Res, 2007, 40(8):1079-1085.
[37]Takaishi N, Yoshida K, Satsu H, et al. Transepithelial transport ofalpha-lipoic acid across human intestinal Caco-2 cell monolayers[J].J Agric Food Chem, 2007, 55(13):5253-5259.
[38]Balamurugan K, Vaziri N D, Said H M. Biotin uptake byhuman proximal tubular epithelial cells:cellular and molecularaspects[J]. Am J Physiol Renal Physiol, 2005, 288(4):F823-831.
[39]Vadlapudi A D, Vadlapatla R K, Mitra A K. Sodium dependentmultivitamin transporter(SMVT):a potential target for drugdelivery[J]. Curr Drug Targets, 2012, 13(7):994-1003.
[40]Bellagamba F, Moretti V M, Mentasti T, et al. High-performanceliquid chromatographic determination of polyamines in milk astheir 9-fluorenylmethoxycarbonyl derivatives using a column-switching technique[J]. J Chromatogr A, 1997, 791(1-2):79-84.
[41]Ghibu S, Lauzier B, Delemasure S, et al. Antioxidant propertiesof alpha-lipoic acid:effects on red blood membrane permeabilityand adaptation of isolated rat heart to reversible ischemia[J]. MolCell Biochem, 2009, 320(1-2):141-148.
[42]Trujillo M, Radi R. Peroxynitrite reaction with the reduced andthe oxidized forms of lipoic acid:New insights into the reactionof peroxynitrite with thiols[J]. Arch Biochem Biophys, 2002,397(1):91-98.
[43]Ou P, Tritschler H J, Wolff S P. Thioctic(lipoic)acid:a therapeuticmetal-chelating antioxidant?[J]. Biochem Pharmacol, 1995, 50(1):123-126.
[44]Suh J H, Moreau R, Heath S H, et al. Dietary supplementationwith(R)-alpha-lipoic acid reverses the age-related accumulationof iron and depletion of antioxidants in the rat cerebral cortex[J].Redox Rep, 2005, 10(1):52-60.
[45]Bush A I. Metal complexing agents as therapies for Alzheimer'sdisease[J]. Neurobiol Aging, 2002, 23(6):1031-1038.
[46]Lodge J K, Traber M G, Packer L. Thiol chelation of Cu2+bydihydrolipoic acid prevents human low density lipoproteinperoxidation[J]. Free Radic Biol Med, 1998, 25:287-297.
[47]Niki E. Lipid peroxidation:Physiological levels and dual bio-logical effects[J]. Free Radic Biol Med, 2009, 47(5):469-484.
[48]Ullery J C, Marnett L J. Protein modification by oxidized phosp-holipids and hydrolytically released lipid electrophiles:Investigatingcellular responses[J]. Biochim Biophys Acta, 2012, 1818(10):2424-2435.
[49]Rochette L, Ghibu S, Richard C, et al. Direct and indirect anti-oxidant properties of alpha-lipoic acid and therapeutic potential[J].Mol Nutr Food Res, 2013, 57(1):114-125.
[50]Berne J P, Lauzier B, Rochette L, et al. Carbon monoxide protectsagainst ischemia-reperfusion injury in vitro via antioxidantproperties[J]. Cell Physiol Biochem, 2012, 29(3-4):475-484.
[51]Chan K H, Ng M K, Stocker R. Haem oxygenase-1 and cardiovasculardisease:mechanisms and therapeutic potential[J]. Clin Sci(Lond), 2011, 120(12):493-504.
[52]Motterlini R, Otterbein L E. The therapeutic potential of carbonmonoxide[J]. Nat Rev Drug Discov, 2010, 9(9):728-U724.
[53]Durante W. Protective role of heme oxygenase-1 against infla-mmation in atherosclerosis[J]. Front Biosci(Landmark Ed), 2011,16:2372-2388.
[54]Ogborne R M, Rushworth S A, O'Connell M A. Alpha-lipoic acid-induced heme oxygenase-1 expression is mediated by nuclearfactor erythroid 2-related factor 2 and p38 mitogen-activatedprotein kinase in human monocytic cells[J]. Arterioscler ThrombVasc Biol, 2005, 25(10):2100-2105.
[55]Huerta-Olvera S G, Macias-Barragan J, Ramos-Marquez M E, etal. Alpha-lipoic acid regulates heme oxygenase gene expressionand nuclear Nrf2 activation as a mechanism of protection againstarsenic exposure in HepG2 cells[J]. Environ Toxicol Pharmacol,2010, 29(2):144-149.
[56]Dinkova-Kostova A T, Talalay P. Direct and indirect antioxidantproperties of inducers of cytoprotective proteins[J]. Mol NutrFood Res, 2008, 52:S128-S138.
[57]Yeni D, Fidan A F, Cigerci I H, et al. Effect of alpha-lipoic acidon sperm quality, reproductive tract measures in thinner exposedrats[J]. Andrologia, 2012, 44:74-80.
[58]Shen T, Jiang Z L, Li C J, et al. Effect of alpha-lipoic acid on boarspermatozoa quality during freezing-thawing[J]. Zygote, 2016,24(2):259-265.
[59]Zavareh S, Karimi I, Salehnia M, et al. Effect of in vitro maturationtechnique and alpha lipoic acid supplementation on oocytematuration rate:focus on oxidative status of oocytes[J]. Int J FertilSteril, 2016, 9(4):442-451.
[60]Hatami S, Zavareh S, Salehnia M, et al. Total oxidative status ofmouse vitrified pre-antral follicles with pre-treatment of alphalipoic acid[J]. Iran Biomed J, 2014, 18(3):181-188.
[61]Linck D W, Larman M G, Gardner D K.α-lipoic acid:an antioxidantthat improves embryo development and protects against oxidativestress[J]. Fertil Steril, 2007, 88(Suppl 1):S36-S37.
[62]Silva E, Greene A F, Strauss K, et al. Antioxidant supplementationduring in vitro culture improves mitochondrial function anddevelopment of embryos from aged female mice[J]. Reprod FertilDev, 2015, 27(6):975-983.
[5]Tripathi A, Khatun S, Pandey A N, et al. Intracellular levels ofhydrogen peroxide and nitric oxide in oocytes at various stagesof meiotic cell cycle and apoptosis[J]. Free Radic Res, 2009,43(3):287-294.
[6]Li C Y, Zhao Y H, Hao H S, et al. Resveratrol significantlyimproves the fertilisation capacity of bovine sex-sorted semenby inhibiting apoptosis and lipid peroxidation[J]. Sci Rep, 2018,8(1):7603.
[7]Zhao X M, Wang N, Hao H S, et al. Melatonin improves thefertilization capacity and developmental ability of bovineoocytes by regulating:cytoplasmic maturation events[J]. JPineal Res, 2018, 64(1)12445.
[8]Haritoglou C, Gerss J, Hammes H P, et al. Alpha-lipoic acid forthe prevention of diabetic macular edema[J]. Ophthalmologica,2011, 226(3):127-137.
[9]Vasdev S, Gill V, Longerich L, et al. Salt-induced hyperten-sionin WKY rats:prevention by alpha-lipoic acid supplementation[J].Mol Cell Biochem, 2003, 254(1-2):319-326.
[10]Ibrahim S F, Osman K, Das S, et al. A study of the antioxidanteffect of alpha lipoic acids on sperm quality[J]. Clinics, 2008,63(4):545-550.
[11]Zhang H, Wu B, Liu H, et al. Improving development of clonedgoat embryos by supplementing alpha-lipoic acid to oocyte invitro maturation medium[J]. Theriogenology, 2013, 80(3):228-233.
[12]Vergely C, Maupoil W, Clermont G, et al. Identification andqantification of free radicals during myocardial ischemia andreperfusion using electron paramagnetic resonance spectroscopy[J].Arch Biochem Biophys, 2003, 420(2):209-216.
[13]de Lamirande E, Lamothe G. Reactive oxygen-induced reactiveoxygen formation during human sperm capacitation[J]. FreeRadic Biol Med, 2009, 46(4):502-510.
[14]Shi T Y, Chen G, Huang X, et al. Effects of reactive oxygenspecies from activated leucocytes on human sperm motility,viability and morphology[J]. Andrologia, 2012, 44(Suppl 1):696-703.
[15]Luczaj W, Skrzydlewska E. DNA damage caused by lipid per-oxidation products[J]. Cell Mol Biol Lett, 2003, 8(2):391-413.
[16]Agarwal A, Said T M, Bedaiwy M A, et al. Oxidative stressin an assisted reproductive techniques setting[J]. Fertil Steril,2006, 86(3):503-512.
[17]Sapanidou V, Taitzoglou I, Tsakmakidis I, et al. Antioxidant effectof crocin on bovine sperm quality and in vitro fertilization[J].Theriogenology, 2015, 84(8):1273-1282.
[18]Cummins J M, Jequier A M, Kan R. Molecular biology of humanmale infertility:links with aging, mitochondrial genetics, andoxidative stress?[J]. Mol Reprod Dev, 1994, 37(3):345-362.
[19]Alexiou M, Leese H J. Purine utilisation, de novo synthesisand degradation in mouse preimplantation embryos[J].Development, 1992, 114(1):185-192.
[20]Raha S, Robinson B H. Mitochondria, oxygen free radicals, andapoptosis[J]. Am J Med Genet, 2001, 106(1):62-70.
[21]Liu L, Keefe D L. Cytoplasm mediates both development andoxidation-induced apoptotic cell death in mouse zygotes[J].Biol Reprod, 2000, 62(6):1828-1834.
[22]Tripathi A, Shrivastav T G, Chaube S K. An increase of gran-ulosa cell apoptosis mediates aqueous neem(Azadirachtaindica)leaf extract-induced oocyte apoptosis in rat[J]. Int JAppl Basic Med Res, 2013, 3(1):27-36.
[23]Ishii T, Miyazawa M, Takanashi Y, et al. Genetically inducedoxidative stress in mice causes thrombocytosis, splenomegalyand placental angiodysplasia that leads to recurrent abortion[J].Redox Biology, 2014, 2:679-685.
[24]Kitagawa Y, Suzuki K, Yoneda A, et al. Effects of oxygen con-centration and antioxidants on the in vitro developmentalability, production of reactive oxygen species(ROS), and DNAfragmentation in porcine embryos[J]. Theriogenology, 2004,62(7):1186-1197.
[25]Favetta L A, St John E J, King W A, et al. High levels of p66(shc)and intracellular ROS in permanently arrested early embryos[J].Free Radic Biol Me, 2007, 42(8):1201-1210.
[26]Guerin P, El Mouatassim S, Menezo Y. Oxidative stress andprotection against reactive oxygen species in the pre-implantationembryo and its surroundings[J]. Hum Reprod Update, 2001, 7(2):175-189.
[27]Rinaudo P F, Giritharan G, Talbi S, et al. Effects of oxygentension on gene expression in preimplantation mouse embryos[J].Fertil Steril, 2006, 86:1252-1265, 1265 e1251-1236.
[28]Takahashi M, Keicho K, Takahashi H, et al. Effect of oxidativestress on development and DNA damage in in-vitro culturedbovine embryos by comet assay[J]. Theriogenology, 2000,54(1):137-145.
[29]Katz-Jaffe M G, Schoolcraft W B, Gardner D K. Analysis of proteinexpression(secretome)by human and mouse preimplantationembryos[J]. Fertil Steril, 2006, 86(3):678-685.
[30]Kovacic B, Vlaisavljevic V. Influence of atmospheric versus reducedoxygen concentration on development of human blastocysts in vitro:a prospective study on sibling oocytes[J]. Reprod Biomed Online,2008, 17(2):229-236.
[30]Lane M, Gardner D K. Understanding cellular disruptionsduring early embryo development that perturb viability andfetal development[J]. Reprod Fertil Dev, 2005, 17(3):371-378.
[31]Wale P L, Gardner D K. Oxygen regulates amino acid turnoverand carbohydrate uptake during the preimplantation period ofmouse embryo development[J]. Biol Reprod, 2012, 87(1):24,1-8.
[32]Gaspar R C, Arnold D R, Correa C A P, et al. Oxygen tensionaffects histone remodeling of in vitro-produced embryos in abovine model[J]. Theriogenology, 2015, 83(9):1408-1415.
[33]Kere M, Siriboon C, Lo N W, et al. Ascorbic acid improves thedevelopmental competence of porcine oocytes after parthenogeneticactivation and somatic cell nuclear transplantation[J]. J ReprodDev, 2013, 59(1):78-84.
[34]Farzollahi M, Tayefi-Nasrabadi H, Mohammadnejad D, et al.Supplementation of culture media with vitamin E improves mouseantral follicle maturation and embryo development from vitrifiedovarian tissue[J]. J Obstet Gynaecol Res, 2016, 42(5):526-535.
[35]Takeo S, Sato D, Kimura K, et al. Resveratrol improves themitochondrial function and fertilization outcome of bovineoocytes[J]. J Reprod Dev, 2014, 60(2):92-99.
[36]Wang Z G, Yu S D, Xu Z R. Effect of supplementation of greentea polyphenols on the developmental competence of bovineoocytes in vitro[J]. Braz J Med Biol Res, 2007, 40(8):1079-1085.
[37]Takaishi N, Yoshida K, Satsu H, et al. Transepithelial transport ofalpha-lipoic acid across human intestinal Caco-2 cell monolayers[J].J Agric Food Chem, 2007, 55(13):5253-5259.
[38]Balamurugan K, Vaziri N D, Said H M. Biotin uptake byhuman proximal tubular epithelial cells:cellular and molecularaspects[J]. Am J Physiol Renal Physiol, 2005, 288(4):F823-831.
[39]Vadlapudi A D, Vadlapatla R K, Mitra A K. Sodium dependentmultivitamin transporter(SMVT):a potential target for drugdelivery[J]. Curr Drug Targets, 2012, 13(7):994-1003.
[40]Bellagamba F, Moretti V M, Mentasti T, et al. High-performanceliquid chromatographic determination of polyamines in milk astheir 9-fluorenylmethoxycarbonyl derivatives using a column-switching technique[J]. J Chromatogr A, 1997, 791(1-2):79-84.
[41]Ghibu S, Lauzier B, Delemasure S, et al. Antioxidant propertiesof alpha-lipoic acid:effects on red blood membrane permeabilityand adaptation of isolated rat heart to reversible ischemia[J]. MolCell Biochem, 2009, 320(1-2):141-148.
[42]Trujillo M, Radi R. Peroxynitrite reaction with the reduced andthe oxidized forms of lipoic acid:New insights into the reactionof peroxynitrite with thiols[J]. Arch Biochem Biophys, 2002,397(1):91-98.
[43]Ou P, Tritschler H J, Wolff S P. Thioctic(lipoic)acid:a therapeuticmetal-chelating antioxidant?[J]. Biochem Pharmacol, 1995, 50(1):123-126.
[44]Suh J H, Moreau R, Heath S H, et al. Dietary supplementationwith(R)-alpha-lipoic acid reverses the age-related accumulationof iron and depletion of antioxidants in the rat cerebral cortex[J].Redox Rep, 2005, 10(1):52-60.
[45]Bush A I. Metal complexing agents as therapies for Alzheimer'sdisease[J]. Neurobiol Aging, 2002, 23(6):1031-1038.
[46]Lodge J K, Traber M G, Packer L. Thiol chelation of Cu2+bydihydrolipoic acid prevents human low density lipoproteinperoxidation[J]. Free Radic Biol Med, 1998, 25:287-297.
[47]Niki E. Lipid peroxidation:Physiological levels and dual bio-logical effects[J]. Free Radic Biol Med, 2009, 47(5):469-484.
[48]Ullery J C, Marnett L J. Protein modification by oxidized phosp-holipids and hydrolytically released lipid electrophiles:Investigatingcellular responses[J]. Biochim Biophys Acta, 2012, 1818(10):2424-2435.
[49]Rochette L, Ghibu S, Richard C, et al. Direct and indirect anti-oxidant properties of alpha-lipoic acid and therapeutic potential[J].Mol Nutr Food Res, 2013, 57(1):114-125.
[50]Berne J P, Lauzier B, Rochette L, et al. Carbon monoxide protectsagainst ischemia-reperfusion injury in vitro via antioxidantproperties[J]. Cell Physiol Biochem, 2012, 29(3-4):475-484.
[51]Chan K H, Ng M K, Stocker R. Haem oxygenase-1 and cardiovasculardisease:mechanisms and therapeutic potential[J]. Clin Sci(Lond), 2011, 120(12):493-504.
[52]Motterlini R, Otterbein L E. The therapeutic potential of carbonmonoxide[J]. Nat Rev Drug Discov, 2010, 9(9):728-U724.
[53]Durante W. Protective role of heme oxygenase-1 against infla-mmation in atherosclerosis[J]. Front Biosci(Landmark Ed), 2011,16:2372-2388.
[54]Ogborne R M, Rushworth S A, O'Connell M A. Alpha-lipoic acid-induced heme oxygenase-1 expression is mediated by nuclearfactor erythroid 2-related factor 2 and p38 mitogen-activatedprotein kinase in human monocytic cells[J]. Arterioscler ThrombVasc Biol, 2005, 25(10):2100-2105.
[55]Huerta-Olvera S G, Macias-Barragan J, Ramos-Marquez M E, etal. Alpha-lipoic acid regulates heme oxygenase gene expressionand nuclear Nrf2 activation as a mechanism of protection againstarsenic exposure in HepG2 cells[J]. Environ Toxicol Pharmacol,2010, 29(2):144-149.
[56]Dinkova-Kostova A T, Talalay P. Direct and indirect antioxidantproperties of inducers of cytoprotective proteins[J]. Mol NutrFood Res, 2008, 52:S128-S138.
[57]Yeni D, Fidan A F, Cigerci I H, et al. Effect of alpha-lipoic acidon sperm quality, reproductive tract measures in thinner exposedrats[J]. Andrologia, 2012, 44:74-80.
[58]Shen T, Jiang Z L, Li C J, et al. Effect of alpha-lipoic acid on boarspermatozoa quality during freezing-thawing[J]. Zygote, 2016,24(2):259-265.
[59]Zavareh S, Karimi I, Salehnia M, et al. Effect of in vitro maturationtechnique and alpha lipoic acid supplementation on oocytematuration rate:focus on oxidative status of oocytes[J]. Int J FertilSteril, 2016, 9(4):442-451.
[60]Hatami S, Zavareh S, Salehnia M, et al. Total oxidative status ofmouse vitrified pre-antral follicles with pre-treatment of alphalipoic acid[J]. Iran Biomed J, 2014, 18(3):181-188.
[61]Linck D W, Larman M G, Gardner D K.α-lipoic acid:an antioxidantthat improves embryo development and protects against oxidativestress[J]. Fertil Steril, 2007, 88(Suppl 1):S36-S37.
[62]Silva E, Greene A F, Strauss K, et al. Antioxidant supplementationduring in vitro culture improves mitochondrial function anddevelopment of embryos from aged female mice[J]. Reprod FertilDev, 2015, 27(6):975-983.