Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.21451/1984-3143-AR2018-0069
Animal Reproduction (AR)
Conference Paper

Oocyte mitochondria: role on fertility and disease transmission

Marcos R. Chiaratti, Bruna M. Garcia, Karen F. Carvalho, Carolina H. Macabelli, Fernanda Karina da Silva Ribeiro, Amanda F. Zangirolamo, Fabiana D. Sarapião, Marcelo M. Seneda, Flávio V. Meirelles, Francisco E. G. Guimarães, Thiago S. Machado

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Abstract

Oocyte mitochondria are increased in number, smaller, and rounder in appearance than mitochondria in somatic cells. Moreover, mitochondrial numbers and activity are narrowly tied with oocyte quality because of the key role of mitochondria to oocyte maturation. During oocyte maturation, mitochondria display great mobility and cluster at specific sites to meet the high energy demand. Conversely, oocyte mitochondria are not required during early oogenesis as coupling with granulosa cells is sufficient to support gamete’s needs. In part, this might be explained by the importance of protecting mitochondria from oxidative damage that result in mutations in mitochondrial DNA (mtDNA). Considering mitochondria are transmitted exclusively by the mother, oocytes with mtDNA mutations may lead to diseases in offspring. Thus, to counterbalance mutation expansion, the oocyte has developed specific mechanisms to filter out deleterious mtDNA molecules. Herein, we discuss the role of mitochondria on oocyte developmental potential and recent evidence supporting a purifying filter against deleterious mtDNA mutations in oocytes.

Keywords

dynamics, fertility, mitochondria, mtDNA, oocyte.

References

Aanen DK, Spelbrink JN, Beekman M. 2014. What cost mitochondria? The maintenance of functional mitochondrial DNA within and across generations. Philos Trans R Soc Lond B Biol Sci, 369:20130438.

Al Rawi S, Louvet-Vallée S, Djeddi A, Sachse M, Culetto E, Hajjar C, Boyd L, Legouis R, Galy V. 2011. Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science, 334:1144-1147.

Ben-Meir A, Burstein E, Borrego-Alvarez A, Chong J, Wong E, Yavorska T, Naranian T, Chi M, Wang Y, Bentov Y, Alexis J, Meriano J, Sung HK, Gasser DL, Moley KH, Hekimi S, Casper RF, Jurisicova A. 2015. Coenzyme Q10 restores oocyte mitochondrial function and fertility during reproductive aging. Aging Cell, 14:887-895.

Binelli M, Murphy BD. 2010. Coordinated regulation of follicle development by germ and somatic cells. Reprod Fertil Dev, 22:1-12. doi: 10.1071/RD09218.

Boucret L, Chao De La Barca JM, Morinière C, Desquiret V, Ferré-L’Hôtellier V, Descamps P, Marcaillou C, Reynier P, Procaccio V, May-Panloup P. 2015. Relationship between diminished ovarian reserve and mitochondrial biogenesis in cumulus cells. Hum Reprod, 30:1653-1664.

Cao L, Shitara H, Horii T, Nagao Y, Imai H, Abe K, Hara T, Hayashi J-I, Yonekawa H. 2007. The mitochondrial bottleneck occurs without reduction of mtDNA content in female mouse germ cells. Nat Genet, 39:386-390.

Chen H, Detmer SA, Ewald AJ, Griffin EE, Fraser SE, Chan DC. 2003. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J Cell Biol, 160:189-200.

Chen H, Chomyn A, Chan DC. 2005. Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J Biol Chem, 280:26185-2692.

Chen H, Vermulst M, Wang YE, Chomyn A, Prolla TA, McCaffery JM, Chan DC. 2010. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell, 141:280-289.

Chen H, Chan DC. 2017. Mitochondrial dynamics in regulating the unique phenotypes of cancer and stem cells. Cell Metab, 26:39-48.

Chen Y, Dorn G. 2013. PINK1-phosphorylated mitofusin 2 is a Parkin receptor for culling damaged mitochondria. Science, 340:471-476.

Chiaratti MR, Ferreira CR, Perecin F, Méo SC, Sangalli JR, Mesquita LG, de Carvalho Balieiro JC, Smith LC, Garcia JM, Meirelles FV. 2011. Ooplastmediated developmental rescue of bovine oocytes exposed to ethidium bromide. Reprod Biomed Online, 22:172-183.

Chiaratti MR, Garcia BM, Carvalho KF, Machado TS, Ribeiro FK da S, Macabelli CH. 2018. The role of mitochondria in the female germline: Implications to fertility and inheritance of mitochondrial diseases. Cell Biol Int, 42:711-724.

Cohen J, Scott R, Schimmel T, Levron J, Willadsen S. 1997. Birth of infant after transfer of anucleate donor oocyte cytoplasm into recipient eggs. Lancet, 350:186- 187.

Collado-Fernandez E, Picton HM, Dumollard R. 2012. Metabolism throughout follicle and oocyte development in mammals. Int J Dev Biol, 56:799-808.

Cree LM, Samuels DC, de Sousa Lopes SC, Rajasimha HK, Wonnapinij P, Mann JR, Dahl HHM, Chinnery PF. 2008. A reduction of mitochondrial DNA molecules during embryogenesis explains the rapid segregation of genotypes. Nat Genet, 40:49-54.

Dale B, Wilding M, Botta G, Rasile M, Marino M, Di Matteo L, De Placido G, Izzo A. 2001. Pregnancy after cytoplasmic transfer in a couple suffering from idiopathic infertility: case report. Hum Reprod, 16:1469-1472.

de Paz P, Sànchez AJ,De la Fuente J,Chamorro CA, Alvarez M, Anel E, Anel L. 2001. Ultrastructural and cytochemical comparison between calf and cow oocytes. Theriogenology, 55:1107-1116.

Duran HE, Simsek-Duran F, Oehninger SC, Jones HW, Castora FJ. 2011. The association of reproductive senescence with mitochondrial quantity, function, and DNA integrity in human oocytes at different stages of maturation. Fertil Steril, 96:384-388.

El-Hayek S, Yang Q, Abbassi L, FitzHarris G, Clarke HJ. 2018. Mammalian oocytes locally remodel follicular architecture to provide the foundation for germline-soma communication. Curr Biol, 28:1124-1131.e3.

El Shourbagy SH, Spikings EC, Freitas M, St John JC. 2006. Mitochondria directly influence fertilisation outcome in the pig. Reproduction, 131:233-245.

Fair T, Hulshof SCJ, Hyttel P, Greve T, Boland M. 1997. Oocyte ultrastructure in bovine primordial to early tertiary follicles. Anat Embryol, 195:327-336.

Fan W, Waymire KG, Narula N, Li P, Rocher C, Coskun PE, Vannan MA, Narula J, Macgregor GR, Wallace DC. 2008. A mouse model of mitochondrial disease reveals germline selection against severe mtDNA mutations. Science, 319:958-962.

Floros VI, Pyle A, Dietmann S, Wei W, Tang WCW, Irie N, Payne B, Capalbo A, Noli L, Coxhead J, Hudson G, Crosier M, Strahl H, Khalaf Y, Saitou M, Ilic D, Surani MA, Chinnery PF. 2018. Segregation of mitochondrial DNA heteroplasmy through a developmental genetic bottleneck in human embryos. Nat Cell Biol, 20:144-151.

Freyer C, Cree LM, Mourier A, Stewart JB, Koolmeister C, Milenkovic D, Wai T, Floros VI, Hagström E, Chatzidaki EE, Wiesner RJ, Samuels DC, Larsson N-G, Chinnery PF. 2012. Variation in germline mtDNA heteroplasmy is determined prenatally but modified during subsequent transmission. Nat Genet, 44:1282-1285.

Guo J, Zhang T, Guo Y, Sun T, Li H, Zhang X, Yin H, Cao G, Yin Y, Wang H, Shi L, Guo X, Sha J, Eppig JJ, Su Y-Q. 2018. Oocyte stage-specific effects of MTOR determine granulosa cell fate and oocyte quality in mice. Proc Natl Acad Sci USA, 115:E5326- E5333.

Hua S, Zhang Y, Li X-C, Ma L-B, Cao J-W, Dai J-P, Li R. 2007. Effects of granulosa cell mitochondria transfer on the early development of bovine embryos in vitro. Cloning Stem Cells, 9:237-246.

Huang CC, Cheng TC, Chang HH, Chang CC, Chen CI, Liu J, Lee MS. 1999. Birth after the injection of sperm and the cytoplasm of tripronucleate zygotes into metaphase II oocytes in patients with repeated implantation failure after assisted fertilization procedures. Fertil Steril, 72:702:706.

Jansen RPS, De Boer K. 1998. The bottleneck: mitochondrial imperatives in oogenesis and ovarian follicular fate. Mol Cell Endocrinol, 145:81-88.

Jenuth J, Peterson A, Fu K, Shoubridge E. 1996. Random genetic drift in the female germline explains the rapid segregation of mammalian mitochondrial DNA. Nat Genet, 14:146-151.

Johnson MT, Freeman EA, Gardner DK, Hunt PA. 2007. Oxidative metabolism of pyruvate is required for meiotic maturation of murine oocytes in vivo. Biol Reprod, 77:2-8. doi: 10.1095/biolreprod.106.059899.

Knight PG, Glister C. 2006. TGF-beta superfamily members and ovarian follicle development. Reproduction, 132:191-206.

Kowald A, Kirkwood TBL. 2011. Evolution of the mitochondrial fusion-fission cycle and its role in aging. Proc Natl Acad Sci USA, 108:10237-10242.

Kruip TAM, Cran DG, van Beneden TH, Dieleman SJ. 1983. Structural changes in bovine oocytes during final maturation in vivo. Gamete Res, 8:29-47.

Lanzendorf SE, Mayer JF, Toner J, Oehninger S, Saffan DS, Muasher S. 1999. Pregnancy following transfer of ooplasm from cryopreserved-thawed donor oocytes into recipient oocytes. Fertil Steril, 71:575-577.

Lazarou M, Sliter DA, Kane LA, Sarraf SA, Wang C, Burman JL, Sideris DP, Fogel AI, Youle RJ. 2015. The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature, 524:309-314.

Lee S, Zhao M, Kwon J, Li Y, Lin Z, Jin Y, Kim N, Cui X. 2014. The association of mitochondrial potential and copy number with pig oocyte maturation and developmental potential. J Reprod Dev, 60:128-135.

Liu K, Zhang H, Risal S, Gorre N, Busayavalasa K, Li X, Shen Y, Bosbach B, Brännström M, 2014. Somatic cells initiate primordial follicle activation and govern the development of dormant oocytes in mice. Curr Biol, 24:2501-2508.

May-Panloup P, Chrétien MF, Jacques C, Vasseur C, Malthièry Y, Reynier P. 2005. Low oocyte mitochondrial DNA content in ovarian insufficiency. Hum Reprod, 20:593-597.

May-Panloup P, Boucret L, Chao de la Barca J-M, Desquiret-Dumas V, Ferré-L’Hotellier V, Morinière C, Descamps P, Procaccio V, Reynier P. 2016. Ovarian ageing: the role of mitochondria in oocytes and follicles. Hum Reprod Update, 22:725-743.

Mishra P, Chan DC. 2014. Mitochondrial dynamics and inheritance during cell division, development and disease. Nat Rev Mol Cell Biol, 15:634-646.

Motta PM, Nottola SA, Makabe S, Heyn R. 2000. Mitochondrial morphology in human fetal and adult female germ cells. Hum Reprod, 15(suppl. 2):129-147.

Narendra D, Tanaka A, Suen D-F, Youle RJ. 2008. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol, 183:795-803.

O’Brien J, Dwarte D, Ryan J, Maxwell W, Evans G. 1996. Developmental capacity, energy metabolism and ultrastructure of mature oocytes from prepubertal and adult sheep. Reprod Fertil Dev, 8:1029-1037.

Oktay K, Baltaci V, Sonmezer M, Turan V, Unsal E, Baltaci A, Aktuna S, Moy F. 2015. Oogonial precursor cell-derived autologous mitochondria injection to improve outcomes in women with multiple IVF failures due to low oocyte quality: a clinical translation. Reprod Sci, 22:1612-1617.

Papanicolaou KN, Kikuchi R, Ngoh GA, Coughlan KA, Dominguez I, Stanley WC, Walsh K. 2012. Mitofusins 1 and 2 are essential for postnatal metabolic remodeling in heart. Circ Res, 111:1012-1026.

Reader KL, Cox NR, Stanton JAL, Juengel JL. 2015a. Effects of acetyl-L-carnitine on lamb oocyte blastocyst rate, ultrastructure, and mitochondrial DNA copy number. Theriogenology, 83:1484-1492.

Reader KL, Cox NR, Stanton JAL, Juengel JL. 2015b. Mitochondria and vesicles differ between adult and prepubertal sheep oocytes during IVM. Reprod Fertil Dev, 27:513-522.

Reynier P, May-Panloup P, Chrétien MF, Morgan CJ, Jean M, Savagner F, Barrière P, Malthièry Y. 2001. Mitochondrial DNA content affects the fertilizability of human oocytes. Mol Hum Reprod, 7:425-429.

Rojansky R, Cha M-Y, Chan DC. 2016. Elimination of paternal mitochondria in mouse embryos occurs through autophagic degradation dependent on PARKIN and MUL1. Elife, 5:pii:e17896. doi: 10.7554/eLife.17896.

Saatcioglu HD, Cuevas I, Castrillon DH. 2016. Control of oocyte reawakening by kit. PLoS Genet, 12:e1006215. doi: 10.1371/journal.pgen.1006215.

Sato A, Nakada K, Shitara H, Kasahara A, Yonekawa H, Hayashi J-I. 2007. Deletion-mutant mtDNA increases in somatic tissues but decreases in female germ cells with age. Genetics, 177:2031-2037.

Schon E a DiMauro S, Hirano M. 2012. Human mitochondrial DNA: roles of inherited and somatic mutations. Nat Rev Genet, 13:878-890.

Schrepfer E, Scorrano L. 2016. Mitofusins, from mitochondria to metabolism. Mol Cell, 61:683-694. Sebastián D, Zorzano A, 2016. When MFN2 (mitofusin 2) met autophagy: a new age for old muscles. Autophagy, 12:2250-2251.

Sharpley MS, Marciniak C, Eckel-Mahan K, McManus M, Crimi M, Waymire K, Lin CS, Masubuchi S, Friend N, Koike M, Chalkia D, MacGregor G, Sassone-Corsi P, Wallace DC. 2012.

Heteroplasmy of mouse mtDNA is genetically unstable and results in altered behavior and cognition. Cell, 151:333-343.

Stewart JB, Freyer C, Elson JL, Wredenberg A, Cansu Z, Trifunovic A, Larsson N-G. 2008. Strong purifying selection in transmission of mammalian mitochondrial DNA. PLoS Biol, 6:e10. doi: 10.1371/journal.pbio.0060010.

Stewart JB, Chinnery PF. 2015. The dynamics of mitochondrial DNA heteroplasmy: implications for human health and disease. Nat Rev Genet, 16:530-542.

Su Y-Q, Sugiura K, Wigglesworth K, O’Brien MJ, Affourtit JP, Pangas SA, Matzuk MM, Eppig JJ. 2007. Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development, 135:111-121.

Sugiura K, Su Y-Q, Diaz FJ, Pangas S a Sharma S, Wigglesworth K, O’Brien MJ, Matzuk MM, Shimasaki S, Eppig JJ. 2007. Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development, 134:2593-2603.

Sutovsky P, Moreno RD, Ramalho-Santos J, Dominko T, Simerly C, Schatten G. 1999. Ubiquitin tag for sperm mitochondria. Nature, 402:371-372.

Swatek KN, Komander D. 2016. Ubiquitin modifications. Cell Res, 26:399-422. Tang BL. 2015. MIRO GTPases in mitochondrial transport, homeostasis and pathology. Cells, 5(1).pii:E1. doi: 10.3390/cells5010001.

Tarín JJ, Pérez-Albalá S, Cano A. 2001. Cellular and morphological traits of oocytes retrieved from aging mice after exogenous ovarian stimulation. Biol Reprod, 65:141-150.

Thouas GA, Trounson AO, Wolvetang EJ, Jones GM. 2004. Mitochondrial dysfunction in mouse oocytes results in preimplantation embryo arrest in vitro. Biol Reprod, 71:1936-1942.

Twig G, Shirihai OS. 2011. The interplay between mitochondrial dynamics and mitophagy. Antioxid Redox Signal, 14:1939-1951.

Udagawa O, Ishihara T, Maeda M, Matsunaga Y, Tsukamoto S, Kawano N, Miyado K, Shitara H, Yokota S, Nomura M, Mihara K, Mizushima N, Ishihara N. 2014. Mitochondrial fission factor Drp1 maintains oocyte quality via dynamic rearrangement of multiple organelles. Curr Biol, 24:2451-2458.

Wai T, Teoli D, Shoubridge EA. 2008. The mitochondrial DNA genetic bottleneck results from replication of a subpopulation of genomes. Nat Genet, 40:1484-1488.

Wai T, Ao A, Zhang X, Cyr D, Dufort D, Shoubridge EA. 2010. The role of mitochondrial DNA copy number in mammalian fertility. Biol Reprod, 83:52-62.

Wakai T, Harada Y, Miyado K, Kono T. 2014. Mitochondrial dynamics controlled by mitofusins define organelle positioning and movement during mouse oocyte maturation. Mol Hum Reprod, 20:1090-1100.

Wallace DC, Chalkia D. 2013. Mitochondrial DNA genetics and the heteroplasmy conundrum in evolution and disease. Cold Spring Harb Perspect Biol, 5:a021220. doi: 10.1101/cshperspect.a021220.

Wassarman PM, Josefowicz WJ. 1978. Oocyte development in the mouse: an ultrastructural comparison of oocytes isolated at various stages of growth and meiotic competence. J Morphol, 156:209- 235.

Yu Y, Dumollard R, Rossbach A, Lai FA, Swann K. 2010. Redistribution of mitochondria leads to bursts of ATP production during spontaneous mouse oocyte maturation. J Cell Physiol, 224:672-680.

Zhang X, Wu XQ, Lu S, Guo YL, Ma X. 2006. Deficit of mitochondria-derived ATP during oxidative stress impairs mouse MII oocyte spindles. Cell Res, 16:841-850.

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