线粒体自噬调控哺乳动物胚胎发育的研究进展

doi:10.11843/j.issn.0366-6964.2024.03.005

摘要/Abstract

摘要： 线粒体自噬（mitophagy）是一个进化保守的过程，它可以选择性地识别、隔离和降解特定靶标。当细胞处于不利的环境下，线粒体自噬通过降解异常或过量的线粒体来维持细胞稳态，减轻细胞运行的压力。线粒体自噬在哺乳动物生殖调控过程中发挥着重要的作用，主要涉及卵母细胞的成熟、衰老和早期胚胎的发育等多种生理过程。本文主要综述了线粒体自噬的生物学功能、线粒体自噬的相关因子调控以及线粒体自噬在哺乳动物生殖中的作用机制，为进一步研究线粒体自噬在哺乳动物生殖发育过程中发挥的作用提供参考依据。

关键词: 线粒体自噬, 哺乳动物, 卵母细胞, 胚胎

Abstract: Mitochondrial autophagy (mitophagy) is an evolutionarily conserved process that selectively identifies, isolates and degrades specific targets. When cells are under adverse conditions, mitophagy eliminates excess or damaged mitochondria to maintain cellular homeostasis and reduce stress on cellular operations. Mitophagy plays an important role in regulation of mammalian reproduction, mainly involving in various physiological processes such as oocyte maturation, senescence and early embryonic development. This paper reviewed the biological functions of mitochondrial autophagy, the regulation of mitochondrial autophagy and the mechanisms of mitochondrial autophagy in mammalian reproduction, providing a reference for further studies on the role of mitochondrial autophagy in mammalian reproductive development.

Key words: mitophagy, mammals, oocyte, embryos

中图分类号:

S813.1

李钰浚, 何翃闳, 杨丽雪, 杨小耿, 李键, 张慧珠. 线粒体自噬调控哺乳动物胚胎发育的研究进展[J]. 畜牧兽医学报, 2024, 55(3): 905-912.

LI Yujun, HE Honghong, YANG Lixue, YANG Xiaogeng, LI Jian, ZHANG Huizhu. Advances in Regulation of Mammalian Embryonic Development by Mitochondrial Autophagy[J]. Acta Veterinaria et Zootechnica Sinica, 2024, 55(3): 905-912.

参考文献

[1] ZHU C L, YAO R Q, LI L X, et al.Mechanism of mitophagy and its role in sepsis induced organ dysfunction:a review[J].Front Cell Dev Biol, 2021, 9:664896.
[2] NIE T J, ZHU L, YANG Q.The classification and basic processes of autophagy[M]//XIE Z P.Autophagy:Biology and Diseases:Technology and Methodology.Singapore:Springer, 2021:3-16.
[3] CHOUBEY V, ZEB A, KAASIK A.Molecular mechanisms and regulation of mammalian mitophagy[J].Cells, 2022, 11(1):38.
[4] 岳锴铭.自噬调节酮病奶牛乳腺上皮细胞氧化应激的作用机制[D].长春:吉林大学, 2022.
YUE K M.The mechanism of autophagy in regulating oxidative stress in mammary epithelial cells in dairy cows with ketosis[D].Changchun:Jilin University, 2022.(in Chinese)
[5] LIN S X, YANG F, HU M W, et al.Selenium alleviates cadmium-induced mitophagy through FUNDC1-mediated mitochondrial quality control pathway in the lungs of sheep[J].Environ Pollut, 2023, 319:120954.
[6] SONG C K, PAN S Z, ZHANG J J, et al.Mitophagy:a novel perspective for insighting into cancer and cancer treatment[J].Cell Prolif, 2022, 55(12):e13327.
[7] BOUDOURES A L, SABEN J, DRURY A, et al.Obesity-exposed oocytes accumulate and transmit damaged mitochondria due to an inability to activate mitophagy[J].Dev Biol, 2017, 426(1):126-138.
[8] YADAV A K, YADAV P K, CHAUDHARY G R, et al.Autophagy in hypoxic ovary[J].Cell Mol Life Sci, 2019, 76(17):3311-3322.
[9] ROJANSKY R, CHA M Y, CHAN D C.Elimination of paternal mitochondria in mouse embryos occurs through autophagic degradation dependent on PARKIN and MUL1[J].eLife, 2016, 5:e17896.
[10] RAWI S A, LOUVET-VALLÉE S, DJEDDI A, et al.Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission[J].Science, 2011, 334(6059):1144-1147.
[11] XU Y Y, LIU Y, CUI L, et al.Hypoxic effects on the mitochondrial content and functions of the placenta in fetal growth restriction[J].Placenta, 2021, 114:100-107.
[12] SEOK J, JUN S J, LEE J O, et al.Mitochondrial dynamics in placenta-derived mesenchymal stem cells regulate the invasion activity of trophoblast[J].Int J Mol Sci, 2020, 21(22):8599.
[13] BARTHO L A, FISHER J J, WALTON S L, et al.The effect of gestational age on mitochondrial properties of the mouse placenta[J].Reprod Fertil, 2022, 3(1):19-29.
[14] ABATE M, FESTA A, FALCO M, et al.Mitochondria as playmakers of apoptosis, autophagy and senescence[J].Semin Cell Dev Biol, 2020, 98:139-153.
[15] GARZA-LOMBÓ C, PAPPA A, PANAYIOTIDIS M I, et al.Redox homeostasis, oxidative stress and mitophagy[J].Mitochondrion, 2020, 51:105-117.
[16] LI W, HE P C, HUANG Y G, et al.Selective autophagy of intracellular organelles:recent research advances[J].Theranostics, 2021, 11(1):222-256.
[17] FARUK M O, ICHIMURA Y, KOMATSU M.Selective autophagy[J].Cancer Sci, 2021, 112(10):3972-3978.
[18] GARZA-LOMBÓ C, PAPPA A, PANAYIOTIDIS M I, et al.Redox homeostasis, oxidative stress and mitophagy[J].Mitochondrion, 2020, 51:105-117.
[19] 梁文清, 刘忠华, 常晓月, 等.长期高铜暴露通过影响线粒体自噬和细胞焦亡诱导大鼠肝组织损伤[J].畜牧兽医学报, 2022, 53(12):4490-4500.
LIANG W Q, LIU Z H, CHANG X Y, et al.Long-term exposure to high levels of copper induced liver injury in rats by affecting mitophagy and pyroptosis[J].Acta Veterinaria et Zootechnica Sinica, 2022, 53(12):4490-4500.(in Chinese)
[20] BONORA M, GIORGI C, PINTON P.Molecular mechanisms and consequences of mitochondrial permeability transition[J].Nat Rev Mol Cell Biol, 2021, 23(4):266-285.
[21] 刘麒薇, 张俊辉, 杨袁, 等.脐带间充质干细胞治疗多囊卵巢综合征的作用及机制[J].中国组织工程研究, 2024, 28(7):1015-1020.
LIU Q W, ZHANG J H, YANG Y, et al.Role and mechanism of umbilical cord mesenchymal stem cells on polycystic ovary syndrome[J].Chinese Journal of Tissue Engineering Research, 2024, 28(7):1015-1020.(in Chinese)
[22] GONÇALVES V F.Mitochondrial genetics[M]//URBANI A, BABU M.Mitochondria in Health and in Sickness. Singapore:Springer, 2019:247-255.
[23] NG M Y W, WAI T, SIMONSEN A.Quality control of the mitochondrion[J].Dev Cell, 2021, 56(7):881-905.
[24] CHOONG C J, OKUNO T, IKENAKA K, et al.Alternative mitochondrial quality control mediated by extracellular release[J]. Autophagy, 2021, 17(10):2962-2974.
[25] SHEN Q Z, LIU Y, LI H G, et al.Effect of mitophagy in oocytes and granulosa cells on oocyte quality[J].Biol Reprod, 2021, 104(2):294-304.
[26] DUNHAM-SNARY K J, SANDEL M W, SAMMY M J, et al.Mitochondrial-nuclear genetic interaction modulates whole body metabolism, adiposity and gene expression in vivo[J].EBioMedicine, 2018, 36:316-328.
[27] SONG W H, BALLARD J W O, YI Y J, et al.Regulation of mitochondrial genome inheritance by autophagy and ubiquitin-proteasome system:implications for health, fitness, and fertility[J].Biomed Res Int, 2014, 2014:981867.
[28] SASAKI T, SATO M.Degradation of paternal mitochondria via mitophagy[J].Biochim Biophys Acta Gen Subj, 2021, 1865(6):129886.
[29] SHEN X H, ZHANG N, WANG Z D, et al.Induction of autophagy improves embryo viability in cloned mouse embryos[J].Sci Rep, 2015, 5:17829.
[30] GÓMEZ-SÁNCHEZ R, TOOZE S A, REGGIORI F.Membrane supply and remodeling during autophagosome biogenesis[J]. Curr Opin Cell Biol, 2021, 71:112-119.
[31] HAMASAKI M, FURUTA N, MATSUDA A, et al.Autophagosomes form at ER-mitochondria contact sites[J].Nature, 2013, 495(7441):389-393.
[32] KORNFELD O S, QVIT N, HAILESELASSIE B, et al.Interaction of mitochondrial fission factor with dynamin related protein 1 governs physiological mitochondrial function in vivo[J].Sci Rep, 2018, 8(1):14034.
[33] WU W X, LIN C X, WU K, et al.FUNDC1 regulates mitochondrial dynamics at the ER-mitochondrial contact site under hypoxic conditions[J].EMBO J, 2016, 35(13):1368-1384.
[34] WU M, TU H Q, CHANG Y, et al.USP19 deubiquitinates HDAC1/2 to regulate DNA damage repair and control chromosomal stability[J].Oncotarget, 2017, 8(2):2197-2208.
[35] CHAI P Y, CHENG Y R C, HOU C Y, et al.USP19 promotes hypoxia-induced mitochondrial division via FUNDC1 at ER-mitochondria contact sites[J].J Cell Biol, 2021, 220(7):e202010006.
[36] TÁBARA L C, MORRIS J L, PRUDENT J.The complex dance of organelles during mitochondrial division[J].Trends Cell Biol, 2021, 31(4):214-253.
[37] MURATA D, ARAI K, IIJIMA M, et al.Mitochondrial division, fusion and degradation[J].J Biochem, 2020, 167(3):233-241.
[38] LAMPERT M A, OROGO A M, NAJOR R H, et al.BNIP3L/NIX and FUNDC1-mediated mitophagy is required for mitochondrial network remodeling during cardiac progenitor cell differentiation[J].Autophagy, 2019, 15(7):1182-1198.
[39] SHIN K T, NIE Z W, ZHOU W J, et al.Connexin 43 knockdown induces mitochondrial dysfunction and affects early developmental competence in porcine embryos[J].Microsc Microanal, 2020, 26(2):287-296.
[40] ISHII T, MANN G E.Redox status in mammalian cells and stem cells during culture in vitro:critical roles of Nrf2 and cystine transporter activity in the maintenance of redox balance[J].Redox Biol, 2014, 2:786-794.
[41] ZHANG Y P, LI Q Q, LI W C, et al.2-Mercaptoethanol promotes porcine oocyte maturation in vitro by maintaining autophagy homeostasis[J].Theriogenology, 2022, 186:155-167.
[42] KUBO N, CAYO-COLCA S I, MIYANO T.Effect of estradiol-17β during in vitro growth culture on the growth, maturation, cumulus expansion and development of porcine oocytes from early antral follicles[J].Anim Sci J, 2015, 86(3):251-259.
[43] DUAN J X, CHEN H L, XU D J, et al.17β-estradiol improves the developmental ability, inhibits reactive oxygen species levels and apoptosis of porcine oocytes by regulating autophagy events[J].J Steroid Biochem Mol Biol, 2021, 209:105826.
[44] GONG Y B, TANG N, LIU P R, et al.Newcastle disease virus degrades SIRT3 via PINK1-PRKN-dependent mitophagy to reprogram energy metabolism in infected cells[J].Autophagy, 2021, 18(7):1503-1521.
[45] TEREŠAK P, LAPAO A, SUBIC N, et al.Regulation of PRKN-independent mitophagy[J].Autophagy, 2022, 18(1):24-39.
[46] PALIKARAS K, LIONAKI E, TAVERNARAKIS N.Mechanisms of mitophagy in cellular homeostasis, physiology and pathology[J].Nat Cell Biol, 2018, 20(9):1013-1022.
[47] XIAN H X, LIOU Y C.Loss of MIEF1/MiD51 confers susceptibility to BAX-mediated cell death and PINK1-PRKN-dependent mitophagy[J].Autophagy, 2019, 15(12):2107-2125.
[48] JIANG M, LIU Z F, SHAO J J, et al.Estrogen receptor α regulates phenotypic switching and proliferation of vascular smooth muscle cells through the NRF1-OMI-mitophagy signaling pathway under simulated microgravity[J].Front Physiol, 2022, 13:1039913.
[49] 李瑞萌, 赵进, 刘岩.PINK1/Parkin介导的线粒体自噬[J].中国生物化学与分子生物学报, 2019, 35(10):1072-1079.
LI R M, ZHAO J, LIU Y.PINK1/Parkin-mediated mitophagy[J].Chinese Journal of Biochemistry and Molecular Biology, 2019, 35(10):1072-1079.(in Chinese)
[50] PAUL S, PICKRELL A M.Hidden phenotypes of PINK1/Parkin knockout mice[J].Biochim Biophys Acta Gen Subj, 2021, 1865(6):129871.
[51] HARPER J W, ORDUREAU A, HEO J M.Building and decoding ubiquitin chains for mitophagy[J].Nat Rev Mol Cell Biol, 2018, 19(2):93-108.
[52] TANAKA K.The PINK1-Parkin axis:an overview[J].Neurosci Res, 2020, 159:9-15.
[53] WANG C Q, LIU K, CAO J N, et al.PINK1-mediated mitophagy maintains pluripotency through optineurin[J].Cell Prolif, 2021, 54(5):e13034.
[54] MATSUDA N, YAMANO K.Two sides of a coin:physiological significance and molecular mechanisms for damage-induced mitochondrial localization of PINK1 and Parkin[J].Neurosci Res, 2020, 159:16-24.
[55] FIESEL F C, FRI AČG OVÁ D, HAYES C S, et al.Substitution of PINK1 Gly411 modulates substrate receptivity and turnover[J]. Autophagy, 2023, 19(6):1711-1732.
[56] UM J H, YUN J.Emerging role of mitophagy in human diseases and physiology[J].BMB Rep, 2017, 50(6):299-307.
[57] LEVINE B, KROEMER G.Biological functions of autophagy genes:a disease perspective[J].Cell, 2019, 176(1-2):11-42.
[58] NIU Y J, NIE Z W, SHIN K T, et al.PINK1 regulates mitochondrial morphology via promoting mitochondrial fission in porcine preimplantation embryos[J].FASEB J, 2019, 33(7):7882-7895.
[59] SHEN M, JIANG Y, GUAN Z Q, et al.Protective mechanism of FSH against oxidative damage in mouse ovarian granulosa cells by repressing autophagy[J].Autophagy, 2017, 13(8):1364-1385.
[60] MCWILLIAMS T G, PRESCOTT A R, MONTAVA-GARRIGA L, et al.Basal mitophagy occurs independently of PINK1 in mouse tissues of high metabolic demand[J].Cell Metab, 2018, 27(2):439-449.
[61] SHEN M, JIANG Y, GUAN Z Q, et al.FSH protects mouse granulosa cells from oxidative damage by repressing mitophagy[J]. Sci Rep, 2016, 6:38090.
[62] ELDEEB M A, RAGHEB M A.N-degron-mediated degradation and regulation of mitochondrial PINK1 kinase[J].Curr Genet, 2020, 66(4):693-701.
[63] LIU Y, AO X, DING W, et al.Critical role of FOXO3a in carcinogenesis[J].Mol Cancer, 2018, 17(1):104.
[64] 熊显荣, 王艳, 李键, 等.SIRT1对牦牛卵母细胞体外成熟与老化的影响[J].畜牧兽医学报, 2019, 50(12):2440-2448.
XIONG X R, WANG Y, LI J, et al.Effects of SIRT1 on the in vitro maturation and aging of yak oocytes[J].Acta Veterinaria et Zootechnica Sinica, 2019, 50(12):2440-2448.(in Chinese)
[65] HE C, LU S, WANG X Z, et al.FOXO3a protects glioma cells against temozolomide-induced DNA double strand breaks via promotion of BNIP3-mediated mitophagy[J].Acta Pharmacol Sin, 2021, 42(8):1324-1337.
[66] CHEN H, TANG X, HAN T L, et al.Potential role of FoxO3a in the regulation of trophoblast development and pregnancy complications[J].J Cell Mol Med, 2021, 25(9):4363-4372.
[67] LONG J, YANG C S, HE J L, et al.FOXO3a is essential for murine endometrial decidualization through cell apoptosis during early pregnancy[J].J Cell Physiol, 2019, 234(4):4154-4166.
[68] MA S, CHEN J W, FENG J, et al.Melatonin ameliorates the progression of atherosclerosis via mitophagy activation and NLRP3 inflammasome inhibition[J].Oxid Med Cell Longev, 2018, 2018:9286458.
[69] ZHANG X Y, LIU Q, ZHANG X E, et al.FOXO3a regulates lipid accumulation and adipocyte inflammation in adipocytes through autophagy[J].Inflamm Res, 2021, 70(5):591-603.
[70] CHEN L L, LI S T, ZHU J Y, et al.Mangiferin prevents myocardial infarction-induced apoptosis and heart failure in mice by activating the Sirt1/FoxO3a pathway[J].J Cell Mol Med, 2021, 25(6):2944-2955.
[71] XU J H, SUN L W, HE M Q, et al.Resveratrol protects against zearalenone-induced mitochondrial defects during porcine oocyte maturation via PINK1/Parkin-mediated mitophagy[J].Toxins (Basel), 2022, 14(9):641.
[72] XING P, ZHANG J J, WU T, et al.SIRT1 reduces epigenetic and non-epigenetic changes to maintain the quality of postovulatory aged oocytes in mice[J].Exp Cell Res, 2021, 399(2):112421.
[73] SUN Y L, TANG S B, SHEN W, et al.Roles of resveratrol in improving the quality of postovulatory aging oocytes in vitro[J].Cells, 2019, 8(10):1132.
[74] ZHOU J L, XUE Z Y Y, HE H N, et al.Resveratrol delays postovulatory aging of mouse oocytes through activating mitophagy[J].Aging (Albany NY), 2019, 11(23):11504-11519.
[75] PIRAS A R, MENÉNDEZ-BLANCO I, SOTO-HERAS S, et al.Resveratrol supplementation during in vitro maturation improves embryo development of prepubertal goat oocytes selected by brilliant cresyl blue staining[J].J Reprod Dev, 2019, 65(2):113-120.
[76] ONISHI M, YAMANO K, SATO M, et al.Molecular mechanisms and physiological functions of mitophagy[J].EMBO J, 2021, 40(3):e104705.
[77] DOBLADO L, LUECK C, REY C, et al.Mitophagy in human diseases[J].Int J Mol Sci, 2021, 22(8):3903.
[78] CHEN Y R, ZHANG P, LIN X Y, et al.Mitophagy impairment is involved in sevoflurane-induced cognitive dysfunction in aged rats[J].Aging(Albany NY), 2020, 12(17):17235-17256.
[79] YIN K L, LEE J, LIU Z L, et al.Mitophagy protein PINK1 suppresses colon tumor growth by metabolic reprogramming via p53 activation and reducing acetyl-CoA production[J].Cell Death Differ, 2021, 28(8):2421-2435.
[80] LIU F, YUAN Y J, BAI L, et al.LRRc17 controls BMSC senescence via mitophagy and inhibits the therapeutic effect of BMSCs on ovariectomy-induced bone loss[J].Redox Biol, 2021, 43:101963.