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Role of Mitochondrial Associated Endoplasmic Reticulum in Oocyte Maturation |
TENG Ming-Ming, GAO Lei-Lei, LEI An-Min* |
College of Veterinary Medicine, Shaanxi Stem Cell Engineering and Technology Research Center, Northwest A&F University, Yangling 712100, China |
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Abstract The specific sites of physical association between endoplasmic reticulum (ER) and mitochondria are known as mitochondria-associated endoplasmic reticulum membrane (MAM), which plays an important role in the regulation of mitochondrial dynamics, calcium signaling, lipid processing and transportation, mitochondrial autophagy and endoplasmic reticulum stress. These physiological functions of MAM are very important for oocyte maturation. It has recently become clear that many proteins in MAM are crucial for oocyte maturation. This article reviews the research progress of MAM involved in oocyte maturation in recent years in order to provide a new direction for understanding the regulation mechanism of oocyte maturation, oocyte quality identification and improving the success rate of assisted reproduction.
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Received: 06 August 2020
Published: 01 February 2021
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Corresponding Authors:
* anminleiryan@nwsuaf.edu.cn
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[1] Berridge M J, Lipp P, Bootman M D.2000. The versatility and universality of calcium signalling[J]. Nature Reviews, Molecular Cell Biology, 1(1): 11-21. [2] Blachly-Dyson E, Forte M.2001. VDAC channels[J]. IUBMB Life, 52(3-5): 113-118. [3] Bonora M, Wieckowsk M R, Chinopoulos C, et al.2015. Molecular mechanisms of cell death: Central implication of ATP synthase in mitochondrial permeability transition[J]. Oncogene, 34(12): 1608. [4] Carroll J, Swann K.1992. Spontaneous cytosolic calcium oscillations driven by inositol trisphosphate occur during in vitro maturation of mouse oocytes[J]. Journal of Biological Chemistry, 267(16): 11196‐11201. [5] Cassará M C, Menzel V A, Hinsch K D, et al.2009. Voltage-dependent anion channels 1 and 2 are expressed in porcine oocytes[J]. Bioscience Reports, 30(3): 193-200. [6] Chen H.2003. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development[J]. Journal of Cell Biology, 160: 189-200. [7] Cipolat S, De Brito O M, Dal Zilio B, et al.2004. OPA1 requires mitofusin 1 to promote mitochondrial fusion[J]. Proceedings of the National Academy of Sciences of the USA, 101(45): 15927-15932. [8] Colombini M.2012. VDAC structure, selectivity, and dynamics[J]. Biochimica et Biophysica Acta, 1818(6): 1457-1465. [9] Dalton C M, Carroll J.2013. Biased inheritance of mitochondria during asymmetric cell division in the mouse oocyte[J]. Journal of Cell Science, 126(Pt 13): 2955-2964. [10] de Brito O M, Scorrano L.2008. Mitofusin 2 tethers endoplasmic reticulum to mitochondria[J]. Nature, 456(7222): 605‐610. [11] De Stefani D, Bononi A, Romagnoli A, et al.2012. VDAC1 selectively transfers apoptotic Ca2+ signals to mitochondria[J]. Cell Death and Differentiation, 19(2): 267‐273. [12] Elbaz Y, Schuldiner M.2011. Staying in touch: The molecular era of organelle contact sites[J]. Trends in Biochemical Sciences, 36(11): 616-623. [13] Filadi R, Greotti E, Turacchio G, et al.2015. Mitofusin 2 ablation increases endoplasmic reticulum-mitochondria coupling[J]. Proceedings of the National Academy of Sciences of the USA, 112(17): E2174-E2181. [14] Filadi R, Theurey P, Pizzo P.2017. The endoplasmic reticulum-mitochondria coupling in health and disease: Molecules, functions and significance[J]. Cell Calcium, 62: 1‐15. [15] Friedman J R, Voeltz G K.2011. The ER in 3D: A multifunctional dynamic membrane network[J]. Trends in Biochemical Sciences, 21(12): 709‐717. [16] Fröhlich C, Grabiger S, Schwefel D, et al.2013. Structural insights into oligomerization and mitochondrial remodelling of dynamin 1-like protein[J]. EMBO Journal, 32(9): 1280‐1292. [17] Gao J, Wang L, Liu J, et al.2017. Abnormalities of mitochondrial dynamics in neurodegenerative diseases[J]. Antioxidants (Basel), 6(2): 25. [18] Gilchrist R B, Lane M, Thompson J G.2008. Oocyte-secreted factors: Regulators of cumulus cell function and oocyte quality[J]. Human Reproduction Update, 14: 159‐177. [19] Gomez-Suaga P, Paillusson S, Stoica R, et al.2017. The ER-Mitochondria Tethering Complex VAPB-PTPIP51 Regulates Autophagy[J]. Current Biology, 27(3): 371‐385. [20] Hayashi T, Su T P.2007. Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca2+ signaling and cell survival[J]. Cell, 131(3): 596‐610. [21] He C L, Damiani P, Ducibella T, et al.1999. Isoforms of the inositol 1,4,5-trisphosphate receptor are expressed in bovine oocytes and ovaries: The type-1 isoform is down-regulated by fertilization and by injection of adenophostin A[J]. Biology of Reproduction, 61(4): 935-943. [22] Hedgepeth S C, Garcia M I, Wagner L E, et al.2015. The BRCA1 tumor suppressor binds to inositol 1,4,5-trisphosphate receptors to stimulate apoptotic calcium release[J]. Journal of Biological Chemistry, 290(11): 7304-7313. [23] Hernández-Alvarez M I, Sebastián D, Vives S, et al.2019. Deficient endoplasmic reticulum-mitochondrial phosphatidylserine transfer causes liver disease[J]. Cell, 177(4): 881-895. [24] Hiller S, Abramson J, Mannella C, et al.2010. The 3D structures of VDAC represent a native conformation[J]. Trends in Biochemical Sciences, 35(9): 514-521. [25] Homa S T, Carroll J, Swann K.1993. Fertilization and early embryology: The role of calcium in mammalian oocyte maturation and egg activation[J]. Human Reproduction, 8(8): 1274-1281. [26] Hou X, Zhu S, Zhang H, et al.2019. Mitofusin1 in oocyte is essential for female fertility[J]. Redox Biology, 21: 101-110. [27] Huang H, Shah K, Bradbury N A, et al.2014. Mcl-1 promotes lung cancer cell migration by directly interacting with VDAC to increase mitochondrial Ca2+ uptake and reactive oxygen species generation[J]. Cell Death & Disease, 5(10): e1482. [28] Ishihara N, Nomura M, Jofuku A, et al.2009. Mitochondrial fission factor Drp1 is essential for embryonic development and synapse formation in mice[J]. Nature Cell Biology, 11(8): 958-966. [29] Iwasawa R, Mahul-Mellier A L, Datler C, et al.2011. Fis1 and Bap31 bridge the mitochondria-ER interface to establish a platform for apoptosis induction[J]. EMBO Journal, 30(3): 556‐568. [30] Ji W K, Hatch A L, Merrill R A, et al.2015. Actin filaments target the oligomeric maturation of the dynamin GTPase Drp1 to mitochondrial fission sites[J]. Elife, 4: e11553. [31] Joseph S K, Bokkala S, Boehning D, et al.2000. Factors determining the composition of inositol trisphosphate receptor hetero-oligomers expressed in COS cells[J]. The Journal of Biological Chemistry, 275(21): 16084-16090. [32] Kalia R, Wang R Y, Yusuf A, et al.2018. Structural basis of mitochondrial receptor binding and constriction by Drp1[J]. Nature, 558(7710): 401-405. [33] Kornmann B.2013. The molecular hug between the ER and the mitochondria[J]. Current Opinion in Cell Biology, 25(4): 443-448. [34] Lee B, Yoon S Y, Fissore R A.2006. Regulation of fertilization-initiated [Ca2+]i oscillations in mammalian eggs: A multi-pronged approach[J]. Seminars in Cell and Developmental Biology, 17(2): 274-284. [35] Liang S L, Zhao Q J, Li X C, et al.2011. Dynamic analysis of Ca²+ level during bovine oocytes maturation and early embryonic development[J]. Journal of Veterinary Science, 12(2): 133-142. [36] Machaty Z.2016. Signal transduction in mammalian oocytes during fertilization[J]. Cell and Tissue Research, 363(1): 169-183. [37] Mak D O, McBride S M, Petrenko N B, et al.2003. Novel regulation of calcium inhibition of the inositol 1,4,5-trisphosphate receptor calcium-release channel[J]. Journal of General Physiology, 122(5): 569-581. [38] Mehlmann L M, Mikoshiba K, Kline D.1996. Redistribution and increase in cortical inositol 1,4,5-trisphosphate receptors after meiotic maturation of the mouse oocyte[J]. Developmental Biology, 180(2): 489-498. [39] Mehlmann L M.2005. Stops and starts in mammalian oocytes: Recent advances in understanding the regulation of meiotic arrest and oocyte maturation[J]. Reproduction, 130(6): 791-799. [40] Merkwirth C, Langer T.2008. Mitofusin 2 builds a bridge between ER and mitochondria[J]. Cell, 135(7): 1165‐1167. [41] Orrenius S, Zhivotovsky B, Nicotera P.2003. Regulation of cell death: The calcium-apoptosis link[J]. Nature Reviews, Molecular Cell Biology, 4(7): 552‐565. [42] Paleos G A, Powers R D.1981. The effect of calcium on the first meiotic division of the mammalian oocyte[J]. Journal of Experimental Zoology Part A, 217(3): 409‐416. [43] Pinton P, Ferrari D, Rapizzi E, et al.2001. The Ca2+ concentration of the endoplasmic reticulum is a key determinant of ceramide-induced apoptosis: Significance for the molecular mechanism of Bcl-2 action[J]. EMBO Journal, 20(11): 2690‐2701. [44] Rojo M, Frédéric Legros, Chateau D, et al.2002. Membrane topology and mitochondrial targeting of mitofusins, ubiquitous mammalian homologs of the transmembrane GTPase Fzo[J]. Journal of Cell Science, 115(Pt 8): 1663-1674. [45] Rowland A A, Voeltz G K.2012. Endoplasmic reticulum-mitochondria contacts: Function of the junction.[J]. Nature Reviews, Molecular Cell Biology, 13(10): 607-25. [46] Rusiñol A E, Cui Z, Chen M H, et al.1994. A unique mitochondria-associated membrane fraction from rat liver has a high capacity for lipid synthesis and contains pre-Golgi secretory proteins including nascent lipoproteins[J]. Journal of Biological Chemistry, 269(44): 27494‐27502. [47] Sampson M J, Decker W K, Beaudet A L, et al.2001. Immotile sperm and infertility in mice lacking mitochondrial voltage-dependent anion channel type 3[J]. Journal of Biological Chemistry, 276(42): 39206‐39212. [48] Santel A, Fuller M T, 2001. Control of mitochondrial morphology by a human mitofusin[J]. Journal of Cell Science, 114: 867‐874. [49] Schredelseker J, Paz A, López C J, et al.2014. High resolution structure and double electron-electron resonance of the zebrafish voltage-dependent anion channel 2 reveal an oligomeric population[J]. Journal of Biological Chemistry, 289(18): 12566‐12577. [50] Stojanovski D, Koutsopoulos O S, Okamoto K, et al.2004. Levels of human Fis1 at the mitochondrial outer membrane regulate mitochondrial morphology[J]. Journal of Cell Science, 117(Pt 7): 1201‐1210. [51] Su Y Q, Sugiura K, Eppig J J.2009. Mouse oocyte control of granulosa cell development and function: Paracrine regulation of cumulus cell metabolism[J]. Seminars in Reproductive Medicine, 27: 32‐42. [52] Sun Q Y, Wu G M, Lai L, et al.2001. Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro[J]. Reproduction, 122(1): 155‐163. [53] Szabadkai G, Bianchi K, Várnai P, et al.2006. Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2+ channels[J]. The Journal of Cell Biology, 175(6): 901‐911. [54] Tosti E.2006. Calcium ion currents mediating oocyte maturation events[J]. Reproductive Biology and Endocrinology, 4: 26. [55] Tu H P, Wang Z N, Nosyreva E, et al.2005. Functional characterization of mammalian inositol 1,4,5-trisphosphate receptor isoforms[J]. Biophysical Journal, 88(2): 1046‐1055. [56] Udagawa O, Ishihara T, Maeda M, et al.2014. Mitochondrial fission factor Drp1 maintains oocyte quality via dynamic rearrangement of multiple organelles[J]. Current Biology, 24(20): 2451‐2458. [57] Ullah G, Jung P, Machaca K.2007. Modeling Ca2+ signaling differentiation during oocyte maturation[J]. Cell Calcium. 42(6): 556‐564. [58] Vance, Jean E.2014. MAM (mitochondria-associated membranes) in mammalian cells: Lipids and beyond[J]. BBA-Molecular and Cell Biology of Lipids, 1841(4): 595-609. [59] Wakana Y, Takai S, Nakajima K, et al.2008. Bap31 is an itinerant protein that moves between the peripheral endoplasmic reticulum (ER) and a juxtanuclear compartment related to ER-associated Degradation[J]. Molecular Biology of the Cell, 19(5): 1825‐1836. [60] Yu Y, Dumollard R, Rossbach A, et al.2010. Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation[J]. Journal of Cellular Physiology, 224(3): 672‐680. [61] Zhang J H, Zhang T, Gao S H, et al.2016. Mitofusin-2 is required for mouse oocyte meiotic maturation[J]. Scientific Reports, 6: 30970. [62] Zhang N, Yoon S Y, Parys J B, et al.2015. Effect of M-phase kinase phosphorylations on type 1 inositol 1,4,5-trisphosphate receptor-mediated Ca2+ responses in mouse eggs[J]. Cell Calcium, 58(5): 476‐488. |
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