褪黑素的抗氧化机制及其在哺乳动物精子冷冻保存中的应用研究进展

doi:10.11843/j.issn.0366-6964.2023.11.004

摘要/Abstract

摘要： 哺乳动物中褪黑素(melatonin)主要是由松果体分泌的一种内源性吲哚胺,含有5-甲氧基和N-乙酰基侧链两个关键官能团,以此决定其特异性和双亲性。近年来,褪黑素及其代谢产物被认为具有抗氧化、抗炎、抗凋亡等多种生物活性,在哺乳动物复杂生理调节过程中发挥重要作用。本文主要围绕褪黑素生物合成与代谢、抗氧化机制及其在哺乳动物精子冷冻保存中的作用效应这3个方面对近期的研究进展进行综述,为深入研究褪黑素在动物细胞体外保存中的应用提供参考依据。

关键词: 褪黑素, 氧化应激, 线粒体, 精子冷冻保存

Abstract: Melatonin is an endogenous indole amine synthesized and secreted principally by the pineal gland in mammals. Distinct roles of 5-methoxy and N-acetyl groups determined the melatonin’s specificity and water-lipid solubility. In recent years, melatonin and its metabolites were proved to have an antioxidant, anti-inflammatory, anti-apoptotic and other biological activities, playing important roles in the complex physiological regulation of mammals. In this paper, we reviewed the research progress on biosynthesis and metabolism, antioxidant mechanisms of melatonin and its bio-effects on sperm cryopreservation, which will provide scientific basis for further research on the application of melatonin in in vitro preservation of animal cells.

Key words: melatonin, oxidative stress, mitochondria, sperm cryopreservation

中图分类号:

Q952
S813.3

李春艳, 张彦, 吕春荣, 邓卫东, 权国波. 褪黑素的抗氧化机制及其在哺乳动物精子冷冻保存中的应用研究进展[J]. 畜牧兽医学报, 2023, 54(11): 4468-4476.

LI Chunyan, ZHANG Yan, Lü Chunrong, DENG Weidong, QUAN Guobo. Research Progress on Antioxidant Mechanisms of Melatonin and Its Application in Cryopreservation of Mammalian Spermatozoa[J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(11): 4468-4476.

参考文献 61

[1]	ZHANG Y J,LIU T,YANG H L,et al.Melatonin:a novel candidate for the treatment of osteoarthritis[J].Ageing Res Rev,2022,78:101635.
[2]	LIU J B,CLOUGH S J,HUTCHINSON A J,et al.MT1 and MT2 melatonin receptors:a therapeutic perspective[J].Annu Rev Pharmacol Toxicol,2016,56:361-383.
[3]	OFOSU J,QAZI I H,FANG Y,et al.Use of melatonin in sperm cryopreservation of farm animals:A brief review[J].Anim Reprod Sci,2021,233:106850.
[4]	REITER R J,TAN D X,GALANO A.Melatonin:exceeding expectations[J].Physiology,2014,29(5):325-333.
[5]	YONG W,MA H Y,NA M,et al.Roles of melatonin in the field of reproductive medicine[J].Biomed Pharmacother,2021,144:112001.
[6]	PIVONELLO C,NEGRI M,PATALANO R,et al.The role of melatonin in the molecular mechanisms underlying metaflammation and infections in obesity:a narrative review[J].Obes Rev,2022,23(3):e13390.
[7]	XU Z Y,YOU W J,LIU J Q,et al.Elucidating the regulatory role of melatonin in brown,white,and beige adipocytes[J].Adv Nutr,2020,11(2):447-460.
[8]	LERNER A B,LEE T H,WRIGHT M R,et al.The mechanism of action of the melanocyte stimulating hormones[J].Acta Endocrinol Suppl (Copenh),1960(S50):73.
[9]	CLAUSTRAT B,LESTON J.Melatonin:physiological effects in humans[J].Neurochirurgie,2015,61(2-3):77-84.
[10]	HICKIE I B,ROGERS N L.Novel melatonin-based therapies:potential advances in the treatment of major depression[J].Lancet,2011,378(9791):621-631.
[11]	REITER R J,TAN D X,MANCHESTER L C,et al.Medical implications of melatonin:receptor-mediated and receptor-independent actions[J].Adv Med Sci,2007,52:11-28.
[12]	BOCHEVA G,SLOMINSKI R M,JANJETOVIC Z,et al.Protective role of melatonin and its metabolites in skin aging[J].Int J Mol Sci,2022,23(3):1238.
[13]	JUHNEVICA-RADENKOVA K,MORENO D A,IKASE L,et al.Naturally occurring melatonin:sources and possible ways of its biosynthesis[J].Compr Rev Food Sci Food Saf,2020,19(6):4008-4030.
[14]	LALANNE S,FOUGEROU-LEURENT C,ANDERSON G M,et al.Melatonin:from pharmacokinetics to clinical use in autism spectrum disorder[J].Int J Mol Sci,2021,22(3):1490.
[15]	TORDJMAN S,CHOKRON S,DELORME R,et al.Melatonin:pharmacology,functions and therapeutic benefits[J].Curr Neuropharmacol,2017,15(3):434-443.
[16]	MANNINO G,PERNICI C,SERIO G,et al.Melatonin and phytomelatonin:chemistry,biosynthesis,metabolism,distribution and bioactivity in plants and animals-an overview[J].Int J Mol Sci,2021,22(18):9996.
[17]	SEMAK I,NAUMOVA M,KORIK E,et al.A novel metabolic pathway of melatonin:oxidation by cytochrome c[J].Biochemistry,2005,44(26):9300-9307.
[18]	HOLTKAMP C E,WARMUS D,BONOWICZ K,et al.Ultraviolet radiation-induced mitochondrial disturbances are attenuated by metabolites of melatonin in human epidermal keratinocytes[J].Metabolites,2023,13(7):861.
[19]	SLOMINSKI A T,SEMAK I,FISCHER T W,et al.Metabolism of melatonin in the skin:why is it important?[J].Exp Dermatol,2017,26(7):563-568.
[20]	VERTERAMO R,PIERDOMENICO M,GRECO P,et al.The role of melatonin in pregnancy and the health benefits for the newborn[J].Biomedicines,2022,10(12):3252.
[21]	MUÑOZ-JURADO A,ESCRIBANO B M,CABALLERO-VILLARRASO J,et al.Melatonin and multiple sclerosis:antioxidant, anti-inflammatory and immunomodulator mechanism of action[J].Inflammopharmacology,2022,30(5): 1569-1596.
[22]	SHEN S N,LIAO Q W,WONG Y K,et al.The role of melatonin in the treatment of type 2 diabetes mellitus and Alzheimer’s disease[J].Int J Biol Sci,2022,18(3):983-994.
[23]	REITER R J,TAN D X,ROSALES-CORRAL S,et al.Mitochondria:central organelles for Melatonin’s antioxidant and anti-aging actions[J].Molecules,2018,23(2):509.
[24]	TIWARI R K,LAL M K,KUMAR R,et al.Insight into melatonin-mediated response and signaling in the regulation of plant defense under biotic stress[J].Plant Mol Biol,2022,109(4-5):385-399.
[25]	SIES H.Oxidative stress:a concept in redox biology and medicine[J].Redox Biol,2015,4:180-183.
[26]	KRUK J,ABOUL-ENEIN B H,DUCHNIK E.Exercise-induced oxidative stress and melatonin supplementation:current evidence[J]. J Physiol Sci,2021,71(1):27.
[27]	REITER R J,MAYO J C,TAN D X,et al.Melatonin as an antioxidant:under promises but over delivers[J].J Pineal Res,2016, 61(3):253-278.
[28]	GALANO A,TAN D X,REITER R J.Melatonin:a versatile protector against oxidative dna damage[J].Molecules,2018,23(3):530.
[29]	ÁLVAREZ-DIDUK R,GALANO A,TAN D X,et al.N-acetylserotonin and 6-hydroxymelatonin against oxidative stress: implications for the overall protection exerted by melatonin[J].J Phys Chem B,2015,119(27):8535-8543.
[30]	NAVARRO-ALARCÓN M,GIL-HERNÁNDEZ F,SÁNCHEZ-GONZÁLEZ C,et al.Melatonin improves levels of Zn and Cu in the muscle of diabetic obese rats[J].Pharmaceutics,2021,13(10):1535.
[31]	TAN D X,MANCHESTER L C,QIN L L,et al.Melatonin:a mitochondrial targeting molecule involving mitochondrial protection and dynamics[J].Int J Mol Sci,2016,17(12):2124.
[32]	PI H F,XU S C,REITER R J,et al.SIRT3-SOD2-mROS-dependent autophagy in cadmium-induced hepatotoxicity and salvage by melatonin[J].Autophagy,2015,11(7):1037-1051.
[33]	XU S Q,LI L L,WU J,et al.Melatonin attenuates sepsis-induced small-intestine injury by upregulating SIRT3-mediated oxidative-stress inhibition,mitochondrial protection,and autophagy induction[J].Front Immunol,2021,12:625627.
[34]	CHITIMUS D M,POPESCU M R,VOICULESCU S E,et al.Melatonin’s impact on antioxidative and anti-inflammatory reprogramming in homeostasis and disease[J].Biomolecules,2020,10(9):1211.
[35]	REITER R J,ROSALES-CORRAL S,TAN D X,et al.Melatonin as a mitochondria-targeted antioxidant:one of evolution’s best ideas[J].Cell Mol Life Sci,2017,74(21):3863-3881.
[36]	POLGE C,SMITH A U,PARKES A S.Revival of spermatozoa after vitrification and dehydration at low temperatures[J].Nature, 1949, 164(4172):666.
[37]	PERIS-FRAU P,SOLER A J,INIESTA-CUERDA M,et al.Sperm cryodamage in ruminants:understanding the molecular changes induced by the cryopreservation process to optimize sperm quality[J].Int J Mol Sci,2020,21(8):2781.
[38]	ZALAZAR L,INIESTA-CUERDA M,SÁNCHEZ-AJOFRÍN I,et al.Recombinant SPINK3 improves ram sperm quality and in vitro fertility after cryopreservation[J].Theriogenology,2020,144:45-55.
[39]	BISHT S,FAIQ M,TOLAHUNASE M,et al.Oxidative stress and male infertility[J].Nat Rev Urol,2017,14(8):470-485.
[40]	EZZATI M,SHANEHBANDI D,HAMDI K,et al.Influence of cryopreservation on structure and function of mammalian spermatozoa:an overview[J].Cell Tissue Bank,2020,21(1):1-15.
[41]	PONCHIA R,BRUNO A,RENZI A,et al.Oxidative stress measurement in frozen/thawed human sperm:the protective role of an in vitro treatment with Myo-inositol[J].Antioxidants (Basel),2022,11(1):10.
[42]	FERRUSOLA C O,FERNÁNDEZ L G,SANDOVAL C S,et al.Inhibition of the mitochondrial permeability transition pore reduces "apoptosis like" changes during cryopreservation of stallion spermatozoa[J].Theriogenology,2010,74(3):458-465.
[43]	TREULEN F,ARIAS M E,AGUILA L,et al.Cryopreservation induces mitochondrial permeability transition in a bovine sperm model[J].Cryobiology,2018,83:65-74.
[44]	DUTTA S,MAJZOUB A,AGARWAL A.Oxidative stress and sperm function:a systematic review on evaluation and management[J].Arab J Urol,2019,17(2):87-97.
[45]	GULBAHCE-MUTLU E,BALTACI S B,MENEVSE E,et al.The effect of zinc and melatonin administration on lipid peroxidation,il-6 levels,and element metabolism in dmba-induced breast cancer in rats[J].Biol Trace Elem Res,2021,199(3): 1044-1051.
[46]	MEHAISEN G M K,PARTYKA A,LIGOCKA Z,et al.Cryoprotective effect of melatonin supplementation on post-thawed rooster sperm quality[J].Anim Reprod Sci,2020,212:106238.
[47]	UGUR M R,ABDELRAHMAN A S,EVANS H C,et al.Advances in cryopreservation of bull sperm[J].Front Vet Sci,2019,6:268.
[48]	SU L J,ZHANG J H,GOMEZ H,et al.Reactive oxygen species-induced lipid peroxidation in apoptosis,autophagy,and ferroptosis[J].Oxid Med Cell Longev,2019,2019:5080843.
[49]	TAMURA H,JOZAKI M,TANABE M,et al.Importance of melatonin in assisted reproductive technology and ovarian aging[J].Int J Mol Sci,2020,21(3):1135.
[50]	POOL K R,RICKARD J P,DE GRAAF S P.Melatonin improves the motility and DNA integrity of frozen-thawed ram spermatozoa likely via suppression of mitochondrial superoxide production[J].Domest Anim Endocrinol,2021,74:106516.
[51]	FANG Y,ZHAO C Z,XIANG H,et al.Melatonin improves cryopreservation of ram sperm by inhibiting mitochondrial permeability transition pore opening[J].Reprod Domest Anim,2020,55(9):1240-1249.
[52]	WANG S Y,WANG L,QIN X,et al.ALDH2 contributes to melatonin-induced protection against APP/PS1 mutation-prompted cardiac anomalies through cGAS-STING-TBK1-mediated regulation of mitophagy[J].Sig Transduct Target Ther,2020,5(1):119.
[53]	DENG S L,SUN T C,YU K,et al.Melatonin reduces oxidative damage and upregulates heat shock protein 90 expression in cryopreserved human semen[J].Free Radic Biol Med,2017,113:347-354.
[54]	NAJAFI A,ADUTWUM E,YARI A,et al.Melatonin affects membrane integrity,intracellular reactive oxygen species,caspase3 activity and AKT phosphorylation in frozen thawed human sperm[J].Cell Tissue Res,2018,372(1):149-159.
[55]	PARIZ J R,RANÉA C,MONTEIRO R A C,et al.Melatonin and caffeine supplementation used,respectively,as protective and stimulating agents in the cryopreservation of human sperm improves survival,viability,and motility after thawing compared to traditional test-yolk buffer[J].Oxid Med Cell Longev,2019,2019:6472945.
[56]	INYAWILERT W,RUNGRUANGSAK J,LIAO Y J,et al.Melatonin supplementation improved cryopreserved Thai swamp buffalo semen[J].Reprod Domest Anim,2021,56(1):83-88.
[57]	SU G H,WU S S,WU M L,et al.Melatonin improves the quality of frozen bull semen and influences gene expression related to embryo genome activation[J].Theriogenology,2021,176:54-62.
[58]	SUCCU S,BERLINGUER F,PASCIU V,et al.Melatonin protects ram spermatozoa from cryopreservation injuries in a dose-dependent manner[J].J Pineal Res,2011,50(3):310-318.
[59]	LI C Y,REN C H,CHEN Y L,et al.Changes on proteomic and metabolomic profiling of cryopreserved sperm effected by melatonin[J].J Proteomics,2023,273:104791.
[60]	NOGUEIRA B G,PEREIRA R R,BITENCOURT J L,et al.Coenzyme Q10 and melatonin protect cryopreserved equine sperm against lipoperoxidation[J].Anim Reprod Sci,2022,243:107027.
[61]	TANHAEI VASH N,NADRI P,KARIMI A.Synergistic effects of myo-inositol and melatonin on cryopreservation of goat spermatozoa[J].Reprod Domest Anim,2022,57(8):876-885.