Skip to main content
Top
Published in: Reproductive Biology and Endocrinology 1/2019

Open Access 01-12-2019 | Review

New Frontiers in IVF: mtDNA and autologous germline mitochondrial energy transfer

Authors: Mauro Cozzolino, Diego Marin, Giovanni Sisti

Published in: Reproductive Biology and Endocrinology | Issue 1/2019

Login to get access

Abstract

Many infertility specialists support the existence of a relationship between the levels of mitochondrial DNA and the quality of the blastocysts. Despite the extensive use of pre-implantation genetic testing for aneuploidy, a significant percentage of euploid embryos do not implant even though the endometrium is normal. Mitochondrial DNA may be used as a new test in evaluating embryonic vitality.
Ovarian aging leads to a decrease in the quantity and quality of oocytes and aged oocytes have a reduced number of mitochondria. Mitochondria are the energy factories of the cells and their lacked could leads to lower fertilization rates and poor embryonic development. Various strategies have been tested to increase the mitochondria quantity and thus improve the quality of oocytes used in in vitro fertilization. Results of ovarian rejuvenation techniques such as autologous mitochondrial transplantation have been controversial. In this review, we describe the state of the art concerning the use of mitochondrial DNA and autologous mitochondrial transplantation as new possibilities to increase success in vitro fertilization.
Literature
1.
go back to reference Paulson RJ, Sauer MV, Lobo RA. Factors affecting embryo implantation after human in vitro fertilization: a hypothesis. Am J Obstet Gynecol. 1990;163:2020–3.PubMedCrossRef Paulson RJ, Sauer MV, Lobo RA. Factors affecting embryo implantation after human in vitro fertilization: a hypothesis. Am J Obstet Gynecol. 1990;163:2020–3.PubMedCrossRef
2.
go back to reference Baxter Bendus AE, Mayer JF, Shipley SK, Catherino WH. Interobserver and intraobserver variation in day 3 embryo grading. Fertil Steril. 2006;86:1608–15.PubMedCrossRef Baxter Bendus AE, Mayer JF, Shipley SK, Catherino WH. Interobserver and intraobserver variation in day 3 embryo grading. Fertil Steril. 2006;86:1608–15.PubMedCrossRef
3.
go back to reference Paternot G, Wetzels AM, Thonon F, Vansteenbrugge A, Willemen D, Devroe J, et al. Intra- and interobserver analysis in the morphological assessment of early stage embryos during an IVF procedure: a multicentre study. Reprod Biol Endocrinol. 2011;9:127,7827–9–127.CrossRef Paternot G, Wetzels AM, Thonon F, Vansteenbrugge A, Willemen D, Devroe J, et al. Intra- and interobserver analysis in the morphological assessment of early stage embryos during an IVF procedure: a multicentre study. Reprod Biol Endocrinol. 2011;9:127,7827–9–127.CrossRef
4.
go back to reference Dunson DB, Colombo B, Baird DD. Changes with age in the level and duration of fertility in the menstrual cycle. Hum Reprod. 2002;17:1399–403.PubMedCrossRef Dunson DB, Colombo B, Baird DD. Changes with age in the level and duration of fertility in the menstrual cycle. Hum Reprod. 2002;17:1399–403.PubMedCrossRef
5.
go back to reference O'Connor KA, Holman DJ, Wood JW. Declining fecundity and ovarian ageing in natural fertility populations. Maturitas. 1998;30:127–36.PubMedCrossRef O'Connor KA, Holman DJ, Wood JW. Declining fecundity and ovarian ageing in natural fertility populations. Maturitas. 1998;30:127–36.PubMedCrossRef
6.
go back to reference Noventa M, Vitagliano A, Andrisani A, Blaganje M, Vigano P, Papaelo E, et al. Testosterone therapy for women with poor ovarian response undergoing IVF: a meta-analysis of randomized controlled trials. J Assist Reprod Genet. 2019;36(4):673–83.PubMedCrossRefPubMedCentral Noventa M, Vitagliano A, Andrisani A, Blaganje M, Vigano P, Papaelo E, et al. Testosterone therapy for women with poor ovarian response undergoing IVF: a meta-analysis of randomized controlled trials. J Assist Reprod Genet. 2019;36(4):673–83.PubMedCrossRefPubMedCentral
7.
go back to reference Franasiak JM, Forman EJ, Hong KH, Werner MD, Upham KM, Treff NR, et al. The nature of aneuploidy with increasing age of the female partner: a review of 15,169 consecutive trophectoderm biopsies evaluated with comprehensive chromosomal screening. Fertil Steril. 2014;101:656,663.e1. Franasiak JM, Forman EJ, Hong KH, Werner MD, Upham KM, Treff NR, et al. The nature of aneuploidy with increasing age of the female partner: a review of 15,169 consecutive trophectoderm biopsies evaluated with comprehensive chromosomal screening. Fertil Steril. 2014;101:656,663.e1.
8.
go back to reference Navot D, Bergh PA, Williams MA, Garrisi GJ, Guzman I, Sandler B, et al. Poor oocyte quality rather than implantation failure as a cause of age-related decline in female fertility. Lancet. 1991;337:1375–7.PubMedCrossRef Navot D, Bergh PA, Williams MA, Garrisi GJ, Guzman I, Sandler B, et al. Poor oocyte quality rather than implantation failure as a cause of age-related decline in female fertility. Lancet. 1991;337:1375–7.PubMedCrossRef
9.
go back to reference Bentov Y, Casper RF. The aging oocyte--can mitochondrial function be improved? Fertil Steril. 2013;99:18–22.PubMedCrossRef Bentov Y, Casper RF. The aging oocyte--can mitochondrial function be improved? Fertil Steril. 2013;99:18–22.PubMedCrossRef
10.
go back to reference Marteil G, Richard-Parpaillon L, Kubiak JZ. Role of oocyte quality in meiotic maturation and embryonic development. Reprod Biol. 2009;9:203–24.PubMedCrossRef Marteil G, Richard-Parpaillon L, Kubiak JZ. Role of oocyte quality in meiotic maturation and embryonic development. Reprod Biol. 2009;9:203–24.PubMedCrossRef
11.
go back to reference Wang T, Babayev E, Jiang Z, Li G, Zhang M, Esencan E, et al. Mitochondrial unfolded protein response gene Clpp is required to maintain ovarian follicular reserve during aging, for oocyte competence, and development of pre-implantation embryos. Aging Cell 2018:e12784.PubMedPubMedCentralCrossRef Wang T, Babayev E, Jiang Z, Li G, Zhang M, Esencan E, et al. Mitochondrial unfolded protein response gene Clpp is required to maintain ovarian follicular reserve during aging, for oocyte competence, and development of pre-implantation embryos. Aging Cell 2018:e12784.PubMedPubMedCentralCrossRef
13.
go back to reference Van Blerkom J. Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion. 2011;11:797–813.PubMedCrossRef Van Blerkom J. Mitochondrial function in the human oocyte and embryo and their role in developmental competence. Mitochondrion. 2011;11:797–813.PubMedCrossRef
14.
go back to reference Fragouli E, Wells D. Mitochondrial dna assessment to determine oocyte and embryo viability. Semin Reprod Med. 2015;33:401–9.PubMedCrossRef Fragouli E, Wells D. Mitochondrial dna assessment to determine oocyte and embryo viability. Semin Reprod Med. 2015;33:401–9.PubMedCrossRef
15.
go back to reference Wells D. Mitochondrial DNA quantity as a biomarker for blastocyst implantation potential. Fertil Steril. 2017;108:742–7.PubMedCrossRef Wells D. Mitochondrial DNA quantity as a biomarker for blastocyst implantation potential. Fertil Steril. 2017;108:742–7.PubMedCrossRef
17.
go back to reference Satoh M, Kuroiwa T. Organization of multiple nucleoids and DNA molecules in mitochondria of a human cell. Exp Cell Res. 1991;196:137–40.PubMedCrossRef Satoh M, Kuroiwa T. Organization of multiple nucleoids and DNA molecules in mitochondria of a human cell. Exp Cell Res. 1991;196:137–40.PubMedCrossRef
18.
go back to reference Balaresque P, Bowden GR, Adams SM, Leung HY, King TE, Rosser ZH, et al. A predominantly neolithic origin for European paternal lineages. PLoS Biol. 2010;8:e1000285.PubMedPubMedCentralCrossRef Balaresque P, Bowden GR, Adams SM, Leung HY, King TE, Rosser ZH, et al. A predominantly neolithic origin for European paternal lineages. PLoS Biol. 2010;8:e1000285.PubMedPubMedCentralCrossRef
19.
go back to reference Seli E. Mitochondrial DNA as a biomarker for in-vitro fertilization outcome. Curr Opin Obstet Gynecol. 2016;28:158–63.PubMedCrossRef Seli E. Mitochondrial DNA as a biomarker for in-vitro fertilization outcome. Curr Opin Obstet Gynecol. 2016;28:158–63.PubMedCrossRef
20.
21.
23.
go back to reference Alexeyev M, Shokolenko I, Wilson G, LeDoux S. The maintenance of mitochondrial DNA integrity--critical analysis and update. Cold Spring Harb Perspect Biol. 2013;5:a012641.PubMedPubMedCentralCrossRef Alexeyev M, Shokolenko I, Wilson G, LeDoux S. The maintenance of mitochondrial DNA integrity--critical analysis and update. Cold Spring Harb Perspect Biol. 2013;5:a012641.PubMedPubMedCentralCrossRef
24.
go back to reference Hutchison CA 3rd, Newbold JE, Potter SS, Edgell MH. Maternal inheritance of mammalian mitochondrial DNA. Nature. 1974;251:536–8.PubMedCrossRef Hutchison CA 3rd, Newbold JE, Potter SS, Edgell MH. Maternal inheritance of mammalian mitochondrial DNA. Nature. 1974;251:536–8.PubMedCrossRef
26.
go back to reference Hajjar C, Sampuda KM, Boyd L. Dual roles for ubiquitination in the processing of sperm organelles after fertilization. BMC Dev Biol. 2014;14(6):213X-14-6. Hajjar C, Sampuda KM, Boyd L. Dual roles for ubiquitination in the processing of sperm organelles after fertilization. BMC Dev Biol. 2014;14(6):213X-14-6.
27.
go back to reference Cummins JM, Wakayama T, Yanagimachi R. Fate of microinjected spermatid mitochondria in the mouse oocyte and embryo. Zygote. 1998;6:213–22.PubMedCrossRef Cummins JM, Wakayama T, Yanagimachi R. Fate of microinjected spermatid mitochondria in the mouse oocyte and embryo. Zygote. 1998;6:213–22.PubMedCrossRef
28.
go back to reference Luo S, Valencia CA, Zhang J, Lee NC, Slone J, Gui B, et al. Biparental Inheritance of Mitochondrial DNA in Humans. Proc Natl Acad Sci U S A. 2018;115:13039–44.PubMedPubMedCentralCrossRef Luo S, Valencia CA, Zhang J, Lee NC, Slone J, Gui B, et al. Biparental Inheritance of Mitochondrial DNA in Humans. Proc Natl Acad Sci U S A. 2018;115:13039–44.PubMedPubMedCentralCrossRef
29.
go back to reference Tranah GJ, Katzman SM, Lauterjung K, Yaffe K, Manini TM, Kritchevsky S, et al. Mitochondrial DNA m.3243A > G heteroplasmy affects multiple aging phenotypes and risk of mortality. Sci Rep. 2018;8:11887,018–30255-6.CrossRef Tranah GJ, Katzman SM, Lauterjung K, Yaffe K, Manini TM, Kritchevsky S, et al. Mitochondrial DNA m.3243A > G heteroplasmy affects multiple aging phenotypes and risk of mortality. Sci Rep. 2018;8:11887,018–30255-6.CrossRef
30.
go back to reference Rebolledo-Jaramillo B, Su MS, Stoler N, McElhoe JA, Dickins B, Blankenberg D, et al. Maternal age effect and severe germ-line bottleneck in the inheritance of human mitochondrial DNA. Proc Natl Acad Sci U S A. 2014;111:15474–9.PubMedPubMedCentralCrossRef Rebolledo-Jaramillo B, Su MS, Stoler N, McElhoe JA, Dickins B, Blankenberg D, et al. Maternal age effect and severe germ-line bottleneck in the inheritance of human mitochondrial DNA. Proc Natl Acad Sci U S A. 2014;111:15474–9.PubMedPubMedCentralCrossRef
31.
go back to reference Cao L, Shitara H, Horii T, Nagao Y, Imai H, Abe K, et al. The mitochondrial bottleneck occurs without reduction of mtDNA content in female mouse germ cells. Nat Genet. 2007;39:386–90.PubMedCrossRef Cao L, Shitara H, Horii T, Nagao Y, Imai H, Abe K, et al. The mitochondrial bottleneck occurs without reduction of mtDNA content in female mouse germ cells. Nat Genet. 2007;39:386–90.PubMedCrossRef
32.
go back to reference Wai T, Teoli D, Shoubridge EA. The mitochondrial DNA genetic bottleneck results from replication of a subpopulation of genomes. Nat Genet. 2008;40:1484–8.PubMedCrossRef Wai T, Teoli D, Shoubridge EA. The mitochondrial DNA genetic bottleneck results from replication of a subpopulation of genomes. Nat Genet. 2008;40:1484–8.PubMedCrossRef
33.
go back to reference Dumollard R, Duchen M, Carroll J. The role of mitochondrial function in the oocyte and embryo. Curr Top Dev Biol. 2007;77:21–49.PubMedCrossRef Dumollard R, Duchen M, Carroll J. The role of mitochondrial function in the oocyte and embryo. Curr Top Dev Biol. 2007;77:21–49.PubMedCrossRef
34.
go back to reference Bentov Y, Yavorska T, Esfandiari N, Jurisicova A, Casper RF. The contribution of mitochondrial function to reproductive aging. J Assist Reprod Genet. 2011;28:773–83.PubMedPubMedCentralCrossRef Bentov Y, Yavorska T, Esfandiari N, Jurisicova A, Casper RF. The contribution of mitochondrial function to reproductive aging. J Assist Reprod Genet. 2011;28:773–83.PubMedPubMedCentralCrossRef
35.
go back to reference Duran HE, Simsek-Duran F, Oehninger SC, Jones HW Jr, Castora FJ. The association of reproductive senescence with mitochondrial quantity, function, and DNA integrity in human oocytes at different stages of maturation. Fertil Steril. 2011;96:384–8.PubMedCrossRef Duran HE, Simsek-Duran F, Oehninger SC, Jones HW Jr, Castora FJ. The association of reproductive senescence with mitochondrial quantity, function, and DNA integrity in human oocytes at different stages of maturation. Fertil Steril. 2011;96:384–8.PubMedCrossRef
36.
go back to reference May-Panloup P, Chretien MF, Jacques C, Vasseur C, Malthiery Y, Reynier P. Low oocyte mitochondrial DNA content in ovarian insufficiency. Hum Reprod. 2005;20:593–7.PubMedCrossRef May-Panloup P, Chretien MF, Jacques C, Vasseur C, Malthiery Y, Reynier P. Low oocyte mitochondrial DNA content in ovarian insufficiency. Hum Reprod. 2005;20:593–7.PubMedCrossRef
37.
go back to reference Murakoshi Y, Sueoka K, Takahashi K, Sato S, Sakurai T, Tajima H, et al. Embryo developmental capability and pregnancy outcome are related to the mitochondrial DNA copy number and ooplasmic volume. J Assist Reprod Genet. 2013;30:1367–75.PubMedPubMedCentralCrossRef Murakoshi Y, Sueoka K, Takahashi K, Sato S, Sakurai T, Tajima H, et al. Embryo developmental capability and pregnancy outcome are related to the mitochondrial DNA copy number and ooplasmic volume. J Assist Reprod Genet. 2013;30:1367–75.PubMedPubMedCentralCrossRef
38.
go back to reference Santos TA, El Shourbagy S, St John JC. Mitochondrial content reflects oocyte variability and fertilization outcome. Fertil Steril. 2006;85:584–91.PubMedCrossRef Santos TA, El Shourbagy S, St John JC. Mitochondrial content reflects oocyte variability and fertilization outcome. Fertil Steril. 2006;85:584–91.PubMedCrossRef
39.
go back to reference Motta PM, Nottola SA, Makabe S, Heyn R. Mitochondrial morphology in human fetal and adult female germ cells. Hum Reprod. 2000;15(Suppl 2):129–47.PubMedCrossRef Motta PM, Nottola SA, Makabe S, Heyn R. Mitochondrial morphology in human fetal and adult female germ cells. Hum Reprod. 2000;15(Suppl 2):129–47.PubMedCrossRef
40.
go back to reference Jansen RP, de Boer K. The bottleneck: mitochondrial imperatives in oogenesis and ovarian follicular fate. Mol Cell Endocrinol. 1998;145:81–8.PubMedCrossRef Jansen RP, de Boer K. The bottleneck: mitochondrial imperatives in oogenesis and ovarian follicular fate. Mol Cell Endocrinol. 1998;145:81–8.PubMedCrossRef
41.
go back to reference Van Blerkom J, Davis PW, Lee J. ATP content of human oocytes and developmental potential and outcome after in-vitro fertilization and embryo transfer. Hum Reprod. 1995;10:415–24.PubMedCrossRef Van Blerkom J, Davis PW, Lee J. ATP content of human oocytes and developmental potential and outcome after in-vitro fertilization and embryo transfer. Hum Reprod. 1995;10:415–24.PubMedCrossRef
42.
go back to reference Larsson NG, Wang J, Wilhelmsson H, Oldfors A, Rustin P, Lewandoski M, et al. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat Genet. 1998;18:231–6.PubMedCrossRef Larsson NG, Wang J, Wilhelmsson H, Oldfors A, Rustin P, Lewandoski M, et al. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat Genet. 1998;18:231–6.PubMedCrossRef
43.
go back to reference El Shourbagy SH, Spikings EC, Freitas M, St John JC. Mitochondria directly influence fertilisation outcome in the pig. Reproduction. 2006;131:233–45.PubMedCrossRef El Shourbagy SH, Spikings EC, Freitas M, St John JC. Mitochondria directly influence fertilisation outcome in the pig. Reproduction. 2006;131:233–45.PubMedCrossRef
44.
go back to reference Van Blerkom J, Davis P, Alexander S. Differential mitochondrial distribution in human pronuclear embryos leads to disproportionate inheritance between blastomeres: relationship to microtubular organization, ATP content and competence. Hum Reprod. 2000;15:2621–33.PubMedCrossRef Van Blerkom J, Davis P, Alexander S. Differential mitochondrial distribution in human pronuclear embryos leads to disproportionate inheritance between blastomeres: relationship to microtubular organization, ATP content and competence. Hum Reprod. 2000;15:2621–33.PubMedCrossRef
45.
go back to reference Piko L, Matsumoto L. Number of mitochondria and some properties of mitochondrial DNA in the mouse egg. Dev Biol. 1976;49:1–10.PubMedCrossRef Piko L, Matsumoto L. Number of mitochondria and some properties of mitochondrial DNA in the mouse egg. Dev Biol. 1976;49:1–10.PubMedCrossRef
46.
go back to reference Reynier P, May-Panloup P, Chretien MF, Morgan CJ, Jean M, Savagner F, et al. Mitochondrial DNA content affects the fertilizability of human oocytes. Mol Hum Reprod. 2001;7:425–9.PubMedCrossRef Reynier P, May-Panloup P, Chretien MF, Morgan CJ, Jean M, Savagner F, et al. Mitochondrial DNA content affects the fertilizability of human oocytes. Mol Hum Reprod. 2001;7:425–9.PubMedCrossRef
48.
go back to reference Piko L, Taylor KD. Amounts of mitochondrial DNA and abundance of some mitochondrial gene transcripts in early mouse embryos. Dev Biol. 1987;123:364–74.PubMedCrossRef Piko L, Taylor KD. Amounts of mitochondrial DNA and abundance of some mitochondrial gene transcripts in early mouse embryos. Dev Biol. 1987;123:364–74.PubMedCrossRef
49.
go back to reference Desquiret-Dumas V, Clement A, Seegers V, Boucret L, Ferre-L'Hotellier V, Bouet PE, et al. The mitochondrial DNA content of cumulus granulosa cells is linked to embryo quality. Hum Reprod. 2017;32:607–14.PubMed Desquiret-Dumas V, Clement A, Seegers V, Boucret L, Ferre-L'Hotellier V, Bouet PE, et al. The mitochondrial DNA content of cumulus granulosa cells is linked to embryo quality. Hum Reprod. 2017;32:607–14.PubMed
50.
go back to reference Diez-Juan A, Rubio C, Marin C, Martinez S, Al-Asmar N, Riboldi M, et al. Mitochondrial DNA content as a viability score in human euploid embryos: less is better. Fertil Steril. 2015;104:534,41.e1.CrossRef Diez-Juan A, Rubio C, Marin C, Martinez S, Al-Asmar N, Riboldi M, et al. Mitochondrial DNA content as a viability score in human euploid embryos: less is better. Fertil Steril. 2015;104:534,41.e1.CrossRef
51.
go back to reference Fragouli E, Spath K, Alfarawati S, Kaper F, Craig A, Michel CE, et al. Altered levels of mitochondrial DNA are associated with female age, aneuploidy, and provide an independent measure of embryonic implantation potential. PLoS Genet. 2015;11:e1005241.PubMedPubMedCentralCrossRef Fragouli E, Spath K, Alfarawati S, Kaper F, Craig A, Michel CE, et al. Altered levels of mitochondrial DNA are associated with female age, aneuploidy, and provide an independent measure of embryonic implantation potential. PLoS Genet. 2015;11:e1005241.PubMedPubMedCentralCrossRef
52.
go back to reference Ogino M, Tsubamoto H, Sakata K, Oohama N, Hayakawa H, Kojima T, et al. Mitochondrial DNA copy number in cumulus cells is a strong predictor of obtaining good-quality embryos after IVF. J Assist Reprod Genet. 2016;33:367–71.PubMedPubMedCentralCrossRef Ogino M, Tsubamoto H, Sakata K, Oohama N, Hayakawa H, Kojima T, et al. Mitochondrial DNA copy number in cumulus cells is a strong predictor of obtaining good-quality embryos after IVF. J Assist Reprod Genet. 2016;33:367–71.PubMedPubMedCentralCrossRef
53.
go back to reference Boucret L, Chao de la Barca JM, Moriniere C, Desquiret V, Ferre-L'Hotellier V, Descamps P, et al. Relationship between diminished ovarian reserve and mitochondrial biogenesis in cumulus cells. Hum Reprod. 2015;30:1653–64.PubMedCrossRef Boucret L, Chao de la Barca JM, Moriniere C, Desquiret V, Ferre-L'Hotellier V, Descamps P, et al. Relationship between diminished ovarian reserve and mitochondrial biogenesis in cumulus cells. Hum Reprod. 2015;30:1653–64.PubMedCrossRef
54.
go back to reference Dumesic DA, Guedikian AA, Madrigal VK, Phan JD, Hill DL, Alvarez JP, et al. Cumulus Cell Mitochondrial Resistance to Stress In Vitro Predicts Oocyte Development During Assisted Reproduction. J Clin Endocrinol Metab. 2016;101:2235–45.PubMedCrossRef Dumesic DA, Guedikian AA, Madrigal VK, Phan JD, Hill DL, Alvarez JP, et al. Cumulus Cell Mitochondrial Resistance to Stress In Vitro Predicts Oocyte Development During Assisted Reproduction. J Clin Endocrinol Metab. 2016;101:2235–45.PubMedCrossRef
55.
go back to reference Chan CC, Liu VW, Lau EY, Yeung WS, Ng EH, Ho PC. Mitochondrial DNA content and 4977 bp deletion in unfertilized oocytes. Mol Hum Reprod. 2005;11:843–6.PubMedCrossRef Chan CC, Liu VW, Lau EY, Yeung WS, Ng EH, Ho PC. Mitochondrial DNA content and 4977 bp deletion in unfertilized oocytes. Mol Hum Reprod. 2005;11:843–6.PubMedCrossRef
56.
go back to reference Konstantinidis M, Alfarawati S, Hurd D, Paolucci M, Shovelton J, Fragouli E, et al. Simultaneous assessment of aneuploidy, polymorphisms, and mitochondrial DNA content in human polar bodies and embryos with the use of a novel microarray platform. Fertil Steril. 2014;102:1385–92.PubMedCrossRef Konstantinidis M, Alfarawati S, Hurd D, Paolucci M, Shovelton J, Fragouli E, et al. Simultaneous assessment of aneuploidy, polymorphisms, and mitochondrial DNA content in human polar bodies and embryos with the use of a novel microarray platform. Fertil Steril. 2014;102:1385–92.PubMedCrossRef
57.
go back to reference Barritt JA, Brenner CA, Malter HE, Cohen J. Mitochondria in human offspring derived from ooplasmic transplantation. Hum Reprod. 2001;16:513–6.PubMedCrossRef Barritt JA, Brenner CA, Malter HE, Cohen J. Mitochondria in human offspring derived from ooplasmic transplantation. Hum Reprod. 2001;16:513–6.PubMedCrossRef
58.
go back to reference Hashimoto S, Morimoto N, Yamanaka M, Matsumoto H, Yamochi T, Goto H, et al. Quantitative and qualitative changes of mitochondria in human preimplantation embryos. J Assist Reprod Genet. 2017;34:573–80.PubMedPubMedCentralCrossRef Hashimoto S, Morimoto N, Yamanaka M, Matsumoto H, Yamochi T, Goto H, et al. Quantitative and qualitative changes of mitochondria in human preimplantation embryos. J Assist Reprod Genet. 2017;34:573–80.PubMedPubMedCentralCrossRef
59.
go back to reference Victor AR, Brake AJ, Tyndall JC, Griffin DK, Zouves CG, Barnes FL, et al. Accurate quantitation of mitochondrial DNA reveals uniform levels in human blastocysts irrespective of ploidy, age, or implantation potential. Fertil Steril. 2017;107:34,42.e3.CrossRef Victor AR, Brake AJ, Tyndall JC, Griffin DK, Zouves CG, Barnes FL, et al. Accurate quantitation of mitochondrial DNA reveals uniform levels in human blastocysts irrespective of ploidy, age, or implantation potential. Fertil Steril. 2017;107:34,42.e3.CrossRef
60.
go back to reference Ravichandran K, McCaffrey C, Grifo J, Morales A, Perloe M, Munne S, et al. Mitochondrial DNA quantification as a tool for embryo viability assessment: retrospective analysis of data from single euploid blastocyst transfers. Hum Reprod. 2017;32:1282–92.PubMedCrossRef Ravichandran K, McCaffrey C, Grifo J, Morales A, Perloe M, Munne S, et al. Mitochondrial DNA quantification as a tool for embryo viability assessment: retrospective analysis of data from single euploid blastocyst transfers. Hum Reprod. 2017;32:1282–92.PubMedCrossRef
61.
go back to reference de Los Santos MJ, Diez Juan A, Mifsud A, Mercader A, Meseguer M, Rubio C, et al. Variables associated with mitochondrial copy number in human blastocysts: what can we learn from trophectoderm biopsies? Fertil Steril. 2018;109:110–7.PubMedCrossRef de Los Santos MJ, Diez Juan A, Mifsud A, Mercader A, Meseguer M, Rubio C, et al. Variables associated with mitochondrial copy number in human blastocysts: what can we learn from trophectoderm biopsies? Fertil Steril. 2018;109:110–7.PubMedCrossRef
62.
go back to reference Treff NR, Zhan Y, Tao X, Olcha M, Han M, Rajchel J, et al. Levels of trophectoderm mitochondrial DNA do not predict the reproductive potential of sibling embryos. Hum Reprod. 2017;32:954–62.PubMedPubMedCentral Treff NR, Zhan Y, Tao X, Olcha M, Han M, Rajchel J, et al. Levels of trophectoderm mitochondrial DNA do not predict the reproductive potential of sibling embryos. Hum Reprod. 2017;32:954–62.PubMedPubMedCentral
63.
go back to reference Klimczak AM, Pacheco LE, Lewis KE, Massahi N, Richards JP, Kearns WG, et al. Embryonal mitochondrial DNA: relationship to embryo quality and transfer outcomes. J Assist Reprod Genet. 2018;35:871–7.PubMedPubMedCentralCrossRef Klimczak AM, Pacheco LE, Lewis KE, Massahi N, Richards JP, Kearns WG, et al. Embryonal mitochondrial DNA: relationship to embryo quality and transfer outcomes. J Assist Reprod Genet. 2018;35:871–7.PubMedPubMedCentralCrossRef
64.
go back to reference Muggleton-Harris A, Whittingham DG, Wilson L. Cytoplasmic control of preimplantation development in vitro in the mouse. Nature. 1982;299:460–2.PubMedCrossRef Muggleton-Harris A, Whittingham DG, Wilson L. Cytoplasmic control of preimplantation development in vitro in the mouse. Nature. 1982;299:460–2.PubMedCrossRef
65.
go back to reference Cohen J, Scott R, Alikani M, Schimmel T, Munne S, Levron J, et al. Ooplasmic transfer in mature human oocytes. Mol Hum Reprod. 1998;4:269–80.PubMedCrossRef Cohen J, Scott R, Alikani M, Schimmel T, Munne S, Levron J, et al. Ooplasmic transfer in mature human oocytes. Mol Hum Reprod. 1998;4:269–80.PubMedCrossRef
66.
go back to reference Cohen J, Scott R, Schimmel T, Levron J, Willadsen S. Birth of infant after transfer of anucleate donor oocyte cytoplasm into recipient eggs. Lancet. 1997;350:186–7.PubMedCrossRef Cohen J, Scott R, Schimmel T, Levron J, Willadsen S. Birth of infant after transfer of anucleate donor oocyte cytoplasm into recipient eggs. Lancet. 1997;350:186–7.PubMedCrossRef
67.
go back to reference Labarta E, de Los Santos MJ, Escriba MJ, Pellicer A, Herraiz S. Mitochondria as a tool for oocyte rejuvenation. Fertil Steril. 2019;111:219–26.PubMedCrossRef Labarta E, de Los Santos MJ, Escriba MJ, Pellicer A, Herraiz S. Mitochondria as a tool for oocyte rejuvenation. Fertil Steril. 2019;111:219–26.PubMedCrossRef
68.
go back to reference Zhang J, Liu H, Luo S, Lu Z, Chavez-Badiola A, Liu Z, et al. Live birth derived from oocyte spindle transfer to prevent mitochondrial disease. Reprod Biomed Online. 2017;34:361–8.PubMedCrossRef Zhang J, Liu H, Luo S, Lu Z, Chavez-Badiola A, Liu Z, et al. Live birth derived from oocyte spindle transfer to prevent mitochondrial disease. Reprod Biomed Online. 2017;34:361–8.PubMedCrossRef
69.
go back to reference Van Blerkom J, Sinclair J, Davis P. Mitochondrial transfer between oocytes: potential applications of mitochondrial donation and the issue of heteroplasmy. Hum Reprod. 1998;13:2857–68.PubMedCrossRef Van Blerkom J, Sinclair J, Davis P. Mitochondrial transfer between oocytes: potential applications of mitochondrial donation and the issue of heteroplasmy. Hum Reprod. 1998;13:2857–68.PubMedCrossRef
70.
go back to reference Yesodi V, Yaron Y, Lessing JB, Amit A, Ben-Yosef D. The mitochondrial DNA mutation (deltamtDNA5286) in human oocytes: correlation with age and IVF outcome. J Assist Reprod Genet. 2002;19:60–6.PubMedPubMedCentralCrossRef Yesodi V, Yaron Y, Lessing JB, Amit A, Ben-Yosef D. The mitochondrial DNA mutation (deltamtDNA5286) in human oocytes: correlation with age and IVF outcome. J Assist Reprod Genet. 2002;19:60–6.PubMedPubMedCentralCrossRef
71.
go back to reference Woods DC, Tilly JL. The next (re) generation of ovarian biology and fertility in women: is current science tomorrow's practice? Fertil Steril. 2012;98:3–10.PubMedPubMedCentralCrossRef Woods DC, Tilly JL. The next (re) generation of ovarian biology and fertility in women: is current science tomorrow's practice? Fertil Steril. 2012;98:3–10.PubMedPubMedCentralCrossRef
72.
go back to reference Alikani M, Fauser BCJ, Garcia-Valesco JA, Simpson JL, Johnson MH. First birth following spindle transfer for mitochondrial replacement therapy: hope and trepidation. Reprod Biomed Online. 2017;34:333–6.PubMedCrossRef Alikani M, Fauser BCJ, Garcia-Valesco JA, Simpson JL, Johnson MH. First birth following spindle transfer for mitochondrial replacement therapy: hope and trepidation. Reprod Biomed Online. 2017;34:333–6.PubMedCrossRef
73.
go back to reference Alikani M, Fauser BCJ, Garcia-Velasco JA, Simpson JL, Johnson MH. Response from the Editors: First birth following spindle transfer. Reprod Biomed Online. 2017;35:548.PubMedCrossRef Alikani M, Fauser BCJ, Garcia-Velasco JA, Simpson JL, Johnson MH. Response from the Editors: First birth following spindle transfer. Reprod Biomed Online. 2017;35:548.PubMedCrossRef
74.
go back to reference Boiani JA, Cohen J. Response: First birth following spindle transfer. Reprod Biomed Online. 2017;35:544–5.PubMedCrossRef Boiani JA, Cohen J. Response: First birth following spindle transfer. Reprod Biomed Online. 2017;35:544–5.PubMedCrossRef
75.
go back to reference Gleicher N, Kushnir VA, Albertini DA, Barad DH. First birth following spindle transfer. Reprod Biomed Online. 2017;35:542–3.PubMedCrossRef Gleicher N, Kushnir VA, Albertini DA, Barad DH. First birth following spindle transfer. Reprod Biomed Online. 2017;35:542–3.PubMedCrossRef
76.
go back to reference Liu Z, Merhi Z, Zhang J, Huang T. Response: First birth following spindle transfer - should we stay or should we go? Reprod Biomed Online. 2017;35:546–7.PubMedCrossRef Liu Z, Merhi Z, Zhang J, Huang T. Response: First birth following spindle transfer - should we stay or should we go? Reprod Biomed Online. 2017;35:546–7.PubMedCrossRef
77.
go back to reference Tesarik J. Oocyte spindle transfer for prevention of mitochodrial disease: the question of membrane fusion technique. Reprod Biomed Online. 2017;35:432.PubMedCrossRef Tesarik J. Oocyte spindle transfer for prevention of mitochodrial disease: the question of membrane fusion technique. Reprod Biomed Online. 2017;35:432.PubMedCrossRef
78.
go back to reference Miguel-Escalada I, Basalmeda R, Garcia M, Vanrell I, Gonzalez J, Calderon G. Meiotic spindle transfer overcomes embryo developmental arrest in compromised oocytes: proof of concept in the mouse model. American Society for Reproductive Medicine Annual Meeting October 28–November 1, 2017, San Antonio, Texas . Miguel-Escalada I, Basalmeda R, Garcia M, Vanrell I, Gonzalez J, Calderon G. Meiotic spindle transfer overcomes embryo developmental arrest in compromised oocytes: proof of concept in the mouse model. American Society for Reproductive Medicine Annual Meeting October 28–November 1, 2017, San Antonio, Texas .
79.
go back to reference Costa-Borges N, Spath K, Nikitos E, Ribustello L, Miguel-Escalada I, Rink K, et al. Cytoplasm replacement by spindle transfer demonstrates enhanced embryo development without compromising euploidy rates: pre-clinical study with donor oocytes. . American Society for Reproductive Medicine Annual Meeting, October 6–10, 2018, Denver, Colorado .CrossRef Costa-Borges N, Spath K, Nikitos E, Ribustello L, Miguel-Escalada I, Rink K, et al. Cytoplasm replacement by spindle transfer demonstrates enhanced embryo development without compromising euploidy rates: pre-clinical study with donor oocytes. . American Society for Reproductive Medicine Annual Meeting, October 6–10, 2018, Denver, Colorado .CrossRef
80.
go back to reference Wang X, Song D, Mykytenko D, Kuang Y, Lv Q, Li B, et al. Novel mutations in genes encoding subcortical maternal complex proteins may cause human embryonic developmental arrest. Reprod Biomed Online. 2018;36:698–704.PubMedCrossRef Wang X, Song D, Mykytenko D, Kuang Y, Lv Q, Li B, et al. Novel mutations in genes encoding subcortical maternal complex proteins may cause human embryonic developmental arrest. Reprod Biomed Online. 2018;36:698–704.PubMedCrossRef
81.
go back to reference P. Mazur, V. Veselovsky, Y. Masliy, M. Borisov, D. Mykytenko, V. Zukin. O-135 Three babies born after pronuclear transplantation in young women with unexplained infertility and repeated implantation failure of euploid embryos. Human Reproduction ESHRE 2018, Barcelona, Spain 2018;33:i60. P. Mazur, V. Veselovsky, Y. Masliy, M. Borisov, D. Mykytenko, V. Zukin. O-135 Three babies born after pronuclear transplantation in young women with unexplained infertility and repeated implantation failure of euploid embryos. Human Reproduction ESHRE 2018, Barcelona, Spain 2018;33:i60.
82.
go back to reference Johnson J, Canning J, Kaneko T, Pru JK, Tilly JL. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature. 2004;428:145–50.PubMedCrossRef Johnson J, Canning J, Kaneko T, Pru JK, Tilly JL. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature. 2004;428:145–50.PubMedCrossRef
83.
go back to reference Tilly JL, Niikura Y, Rueda BR. The current status of evidence for and against postnatal oogenesis in mammals: a case of ovarian optimism versus pessimism? Biol Reprod. 2009;80:2–12.PubMedPubMedCentralCrossRef Tilly JL, Niikura Y, Rueda BR. The current status of evidence for and against postnatal oogenesis in mammals: a case of ovarian optimism versus pessimism? Biol Reprod. 2009;80:2–12.PubMedPubMedCentralCrossRef
84.
go back to reference Zou K, Yuan Z, Yang Z, Luo H, Sun K, Zhou L, et al. Production of offspring from a germline stem cell line derived from neonatal ovaries. Nat Cell Biol. 2009;11:631–6.PubMedCrossRef Zou K, Yuan Z, Yang Z, Luo H, Sun K, Zhou L, et al. Production of offspring from a germline stem cell line derived from neonatal ovaries. Nat Cell Biol. 2009;11:631–6.PubMedCrossRef
85.
go back to reference Pacchiarotti J, Maki C, Ramos T, Marh J, Howerton K, Wong J, et al. Differentiation potential of germ line stem cells derived from the postnatal mouse ovary. Differentiation. 2010;79:159–70.PubMedCrossRef Pacchiarotti J, Maki C, Ramos T, Marh J, Howerton K, Wong J, et al. Differentiation potential of germ line stem cells derived from the postnatal mouse ovary. Differentiation. 2010;79:159–70.PubMedCrossRef
86.
go back to reference Johnson J, Bagley J, Skaznik-Wikiel M, Lee HJ, Adams GB, Niikura Y, et al. Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood. Cell. 2005;122:303–15.PubMedCrossRef Johnson J, Bagley J, Skaznik-Wikiel M, Lee HJ, Adams GB, Niikura Y, et al. Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood. Cell. 2005;122:303–15.PubMedCrossRef
87.
go back to reference Fakih MH, El Shmoury M, Szeptycki J, dela Cruz DB, Lux C, Verjee S, Burgess CM, Cohn GM, Casper R. The AUGMENTSM treatment: physician reported outcomes of the initial global patient experience. JFIV Reprod Med Genet. 2015;3:154.CrossRef Fakih MH, El Shmoury M, Szeptycki J, dela Cruz DB, Lux C, Verjee S, Burgess CM, Cohn GM, Casper R. The AUGMENTSM treatment: physician reported outcomes of the initial global patient experience. JFIV Reprod Med Genet. 2015;3:154.CrossRef
88.
go back to reference White YA, Woods DC, Takai Y, Ishihara O, Seki H, Tilly JL. Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nat Med. 2012;18:413–21.PubMedPubMedCentralCrossRef White YA, Woods DC, Takai Y, Ishihara O, Seki H, Tilly JL. Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nat Med. 2012;18:413–21.PubMedPubMedCentralCrossRef
89.
go back to reference Wu C, Xu B, Li X, Ma W, Zhang P, Chen X, et al. Tracing and Characterizing the Development of Transplanted Female Germline Stem Cells In Vivo. Mol Ther. 2017;25:1408–19.PubMedPubMedCentralCrossRef Wu C, Xu B, Li X, Ma W, Zhang P, Chen X, et al. Tracing and Characterizing the Development of Transplanted Female Germline Stem Cells In Vivo. Mol Ther. 2017;25:1408–19.PubMedPubMedCentralCrossRef
90.
go back to reference Guo K, Li CH, Wang XY, He DJ, Zheng P. Germ stem cells are active in postnatal mouse ovary under physiological conditions. Mol Hum Reprod. 2016;22:316–28.PubMedPubMedCentralCrossRef Guo K, Li CH, Wang XY, He DJ, Zheng P. Germ stem cells are active in postnatal mouse ovary under physiological conditions. Mol Hum Reprod. 2016;22:316–28.PubMedPubMedCentralCrossRef
91.
go back to reference Wang N, Satirapod C, Ohguchi Y, Park ES, Woods DC, Tilly JL. Genetic studies in mice directly link oocytes produced during adulthood to ovarian function and natural fertility. Sci Rep. 2017;7:10011,017–10033-6. Wang N, Satirapod C, Ohguchi Y, Park ES, Woods DC, Tilly JL. Genetic studies in mice directly link oocytes produced during adulthood to ovarian function and natural fertility. Sci Rep. 2017;7:10011,017–10033-6.
92.
go back to reference Lipskind S, Lindsey JS, Gerami-Naini B, Eaton JL, O'Connell D, Kiezun A, et al. An Embryonic and Induced Pluripotent Stem Cell Model for Ovarian Granulosa Cell Development and Steroidogenesis. Reprod Sci. 2018;25:712–26.PubMedCrossRef Lipskind S, Lindsey JS, Gerami-Naini B, Eaton JL, O'Connell D, Kiezun A, et al. An Embryonic and Induced Pluripotent Stem Cell Model for Ovarian Granulosa Cell Development and Steroidogenesis. Reprod Sci. 2018;25:712–26.PubMedCrossRef
94.
go back to reference St John JC, Tsai TS, Cagnone GL. Mitochondrial DNA supplementation as an enhancer of female reproductive capacity. Curr Opin Obstet Gynecol. 2016;28:211–6.PubMedCrossRef St John JC, Tsai TS, Cagnone GL. Mitochondrial DNA supplementation as an enhancer of female reproductive capacity. Curr Opin Obstet Gynecol. 2016;28:211–6.PubMedCrossRef
95.
go back to reference Hua S, Zhang Y, Li XC, Ma LB, Cao JW, Dai JP, et al. Effects of granulosa cell mitochondria transfer on the early development of bovine embryos in vitro. Cloning Stem Cells. 2007;9:237–46.PubMedCrossRef Hua S, Zhang Y, Li XC, Ma LB, Cao JW, Dai JP, et al. Effects of granulosa cell mitochondria transfer on the early development of bovine embryos in vitro. Cloning Stem Cells. 2007;9:237–46.PubMedCrossRef
96.
go back to reference Oktay K, Baltaci V, Sonmezer M, Turan V, Unsal E, Baltaci A, et al. 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. 2015;22:1612–7.PubMedCrossRef Oktay K, Baltaci V, Sonmezer M, Turan V, Unsal E, Baltaci A, et al. 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. 2015;22:1612–7.PubMedCrossRef
97.
go back to reference Labarta E, de Los Santos MJ, Herraiz S, Escriba MJ, Marzal A, Buigues A, et al. Autologous mitochondrial transfer as a complementary technique to intracytoplasmic sperm injection to improve embryo quality in patients undergoing in vitro fertilization-a randomized pilot study. Fertil Steril. 2018. Labarta E, de Los Santos MJ, Herraiz S, Escriba MJ, Marzal A, Buigues A, et al. Autologous mitochondrial transfer as a complementary technique to intracytoplasmic sperm injection to improve embryo quality in patients undergoing in vitro fertilization-a randomized pilot study. Fertil Steril. 2018.
98.
go back to reference Ghevaria H, SenGupta S, Sarna U, Sargeant S, Serhal P, Delhanty J. The contribution of germinal mosaicism to human aneuploidy. Cytogenet Genome Res. 2014;144:264–74.PubMedCrossRef Ghevaria H, SenGupta S, Sarna U, Sargeant S, Serhal P, Delhanty J. The contribution of germinal mosaicism to human aneuploidy. Cytogenet Genome Res. 2014;144:264–74.PubMedCrossRef
99.
go back to reference Hunt PA, Hassold TJ. Human female meiosis: what makes a good egg go bad? Trends Genet. 2008;24:86–93.PubMedCrossRef Hunt PA, Hassold TJ. Human female meiosis: what makes a good egg go bad? Trends Genet. 2008;24:86–93.PubMedCrossRef
Metadata
Title
New Frontiers in IVF: mtDNA and autologous germline mitochondrial energy transfer
Authors
Mauro Cozzolino
Diego Marin
Giovanni Sisti
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2019
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-019-0501-z

Other articles of this Issue 1/2019

Reproductive Biology and Endocrinology 1/2019 Go to the issue