Polar body genome transfer for preventing the transmission of inherited mitochondrial diseases

Cell

Volumn 157, Issue 7, 2014, Pages 1591-1604

  Wang, Tian ^a   Sha, Hongying ^a   Ji, Dongmei ^b   Zhang, Helen L ^c   Chen, Dawei ^b   Cao, Yunxia ^b   Zhu, Jianhong ^a  

^a FUDAN UNIVERSITY   (China)

^b ANHUI MEDICAL UNIVERSITY   (China)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL TRANSFER; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; COPY NUMBER VARIATION; DISEASE TRANSMISSION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA METHYLATION; EMBRYO; EMBRYO TRANSFER; EPIGENETICS; FEMALE; FERTILIZATION; GENETIC ANALYSIS; GENETIC DISORDER; GENOMICS; GENOTYPE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; OOCYTE MATURATION; POLAR BODY; POLAR BODY TRANSFER; PRIORITY JOURNAL; PROGENY; PRONUCLEAR TRANSFER; PROTEIN AGGREGATION; PYROSEQUENCING; SPINDLE CHROMOSOME TRANSFER; ANIMAL TISSUE; FIRST POLAR BODY TRANSFER; GENE TRANSFER; GERM LINE GENE THERAPY; HUMAN; HUMAN CELL; INFANT; MALE; MITOCHONDRIAL REPLACEMENT THERAPY; POLAR BODY GENOME TRANSFER; SECOND POLAR BODY TRANSFER;

ANIMALS; HUMANS; MICE; MITOCHONDRIAL DISEASES; MODELS, ANIMAL; NUCLEAR TRANSFER TECHNIQUES; OOCYTES; POLAR BODIES; SPINDLE APPARATUS;

EID: 84903127483     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.04.042     Document Type: Article

References (57)

1. E. Ballana, N. Govea, R. de Cid, C. Garcia, C. Arribas, J. Rosell, and X. Estivill Detection of unrecognized low-level mtDNA heteroplasmy may explain the variable phenotypic expressivity of apparently homoplasmic mtDNA mutations Hum. Mutat. 29 2008 248 257
2. F.R. Bieber, W.E. Nance, C.C. Morton, J.A. Brown, F.O. Redwine, R.L. Jordan, and T. Mohanakumar Genetic studies of an acardiac monster: evidence of polar body twinning in man Science 213 1981 775 777
3. E.L. Blakely, J.W. Yarham, C.L. Alston, K. Craig, J. Poulton, C. Brierley, S.-M. Park, A. Dean, J.H. Xuereb, and K.N. Anderson et al. Pathogenic mitochondrial tRNA point mutations: nine novel mutations affirm their importance as a cause of mitochondrial disease Hum. Mutat. 34 2013 1260 1268
4. A.L. Bredenoord, W. Dondorp, G. Pennings, C.E. De Die-Smulders, and G. De Wert PGD to reduce reproductive risk: the case of mitochondrial DNA disorders Hum. Reprod. 23 2008 2392 2401
5. D.T. Brown, M. Herbert, V.K. Lamb, P.F. Chinnery, R.W. Taylor, R.N. Lightowlers, L. Craven, L. Cree, J.L. Gardner, and D.M. Turnbull Transmission of mitochondrial DNA disorders: possibilities for the future Lancet 368 2006 87 89
6. I. Cantone, and A.G. Fisher Epigenetic programming and reprogramming during development Nat. Struct. Mol. Biol. 20 2013 282 289
7. L. Cao, H. Shitara, T. Horii, Y. Nagao, H. Imai, K. Abe, T. Hara, J.-I. Hayashi, and H. Yonekawa The mitochondrial bottleneck occurs without reduction of mtDNA content in female mouse germ cells Nat. Genet. 39 2007 386 390
8. P.F. Chinnery, H.R. Elliott, G. Hudson, D.C. Samuels, and C.L. Relton Epigenetics, epidemiology and mitochondrial DNA diseases Int. J. Epidemiol. 41 2012 177 187
9. D. Christopikou, E. Tsorva, K. Economou, P. Shelley, S. Davies, M. Mastrominas, and A.H. Handyside Polar body analysis by array comparative genomic hybridization accurately predicts aneuploidies of maternal meiotic origin in cleavage stage embryos of women of advanced maternal age Hum. Reprod. 28 2013 1426 1434
10. L. Craven, H.A. Tuppen, G.D. Greggains, S.J. Harbottle, J.L. Murphy, L.M. Cree, A.P. Murdoch, P.F. Chinnery, R.W. Taylor, and R.N. Lightowlers et al. Pronuclear transfer in human embryos to prevent transmission of mitochondrial DNA disease Nature 465 2010 82 85
11. L.M. Cree, D.C. Samuels, S.C. de Sousa Lopes, H.K. Rajasimha, P. Wonnapinij, J.R. Mann, H.-H.M. Dahl, and P.F. Chinnery A reduction of mitochondrial DNA molecules during embryogenesis explains the rapid segregation of genotypes Nat. Genet. 40 2008 249 254
12. C.M. Dalton, and J. Carroll Biased inheritance of mitochondria during asymmetric cell division in the mouse oocyte J. Cell Sci. 126 2013 2955 2964
13. W. Fan, K.G. Waymire, N. Narula, P. Li, C. Rocher, P.E. Coskun, M.A. Vannan, J. Narula, G.R. Macgregor, and D.C. Wallace A mouse model of mitochondrial disease reveals germline selection against severe mtDNA mutations Science 319 2008 958 962
14. FDA (2014). Cellular Tissue, and Gene Therapies Advisory Committee. Briefing Document-Oocyte Modification in Assisted Reproduction for the Prevention of Transmission of Mitochondrial Disease or Treatment of Infertility http://www.fda.gov/AdvisoryCommittees/CommitteesMeetingMaterials/ BloodVaccinesandOtherBiologics/CellularTissueandGeneTherapiesAdvisoryCommittee/ ucm380047.
15. J. Geraedts, M. Montag, M.C. Magli, S. Repping, A. Handyside, C. Staessen, J. Harper, A. Schmutzler, J. Collins, and V. Goossens et al. Polar body array CGH for prediction of the status of the corresponding oocyte. Part I: clinical results Hum. Reprod. 26 2011 3173 3180
16. N. Gigarel, L. Hesters, D.C. Samuels, S. Monnot, P. Burlet, V. Kerbrat, F. Lamazou, A. Benachi, R. Frydman, and J. Feingold et al. Poor correlations in the levels of pathogenic mitochondrial DNA mutations in polar bodies versus oocytes and blastomeres in humans Am. J. Hum. Genet. 88 2011 494 498
17. R.E. Giles, H. Blanc, H.M. Cann, and D.C. Wallace Maternal inheritance of human mitochondrial DNA Proc. Natl. Acad. Sci. USA 77 1980 6715 6719
18. M.W. Goldberg, I. Huttenlauch, C.J. Hutchison, and R. Stick Filaments made from A- and B-type lamins differ in structure and organization J. Cell Sci. 121 2008 215 225
19. L. Gu, Q. Wang, and Q.-Y. Sun Histone modifications during mammalian oocyte maturation: dynamics, regulation and functions Cell Cycle 9 2010 1942 1950
20. HFEA (2012). Mitochondria public consultation 2012. Mitochondria replacement consultation-advice for Government. http://www.hfea.gov.uk/6896. html.
21. T. Hino, H. Kusakabe, and H. Tateno Chromosomal stability of second polar bodies in mouse embryos J. Assist. Reprod. Genet. 30 2013 91 98
22. Y. Hou, W. Fan, L. Yan, R. Li, Y. Lian, J. Huang, J. Li, L. Xu, F. Tang, X.S. Xie, and J. Qiao Genome analyses of single human oocytes Cell 155 2013 1492 1506
23. E. Houliston, M.N. Guilly, J.C. Courvalin, and B. Maro Expression of nuclear lamins during mouse preimplantation development Development 102 1988 271 278
24. C.A. Hutchison 3rd, J.E. Newbold, S.S. Potter, and M.H. Edgell Maternal inheritance of mammalian mitochondrial DNA Nature 251 1974 536 538
25. T.S. Kitajima, M. Ohsugi, and J. Ellenberg Complete kinetochore tracking reveals error-prone homologous chromosome biorientation in mammalian oocytes Cell 146 2011 568 581
26. S.K. Kota, and R. Feil Epigenetic transitions in germ cell development and meiosis Dev. Cell 19 2010 675 686
27. J. Link, D. Jahn, J. Schmitt, E. Göb, J. Baar, S. Ortega, R. Benavente, and M. Alsheimer The meiotic nuclear lamina regulates chromosome dynamics and promotes efficient homologous recombination in the mouse PLoS Genet. 9 2013 e1003261
28. H. Liu, J.-M. Kim, and F. Aoki Regulation of histone H3 lysine 9 methylation in oocytes and early pre-implantation embryos Development 131 2004 2269 2280
29. C. Lorthongpanich, L.F. Cheow, S. Balu, S.R. Quake, B.B. Knowles, W.F. Burkholder, D. Solter, and D.M. Messerschmidt Single-cell DNA-methylation analysis reveals epigenetic chimerism in preimplantation embryos Science 341 2013 1110 1112
30. B. Maro, M.H. Johnson, M. Webb, and G. Flach Mechanism of polar body formation in the mouse oocyte: an interaction between the chromosomes, the cytoskeleton and the plasma membrane J. Embryol. Exp. Morphol. 92 1986 11 32
31. F.V. Meirelles, and L.C. Smith Mitochondrial genotype segregation in a mouse heteroplasmic lineage produced by embryonic karyoplast transplantation Genetics 145 1997 445 451
32. Nuffield Council on Bioethics (2012). Novel techniques for the prevention of mitochondrial DNA disorders: an ethical review. http://www. nuffieldbioethics.org/mitochondrial-dna-disorders.
33. D. Paull, V. Emmanuele, K.A. Weiss, N. Treff, L. Stewart, H. Hua, M. Zimmer, D.J. Kahler, R.S. Goland, and S.A. Noggle et al. Nuclear genome transfer in human oocytes eliminates mitochondrial DNA variants Nature 493 2013 632 637
34. L. Pikó, and K.D. Taylor Amounts of mitochondrial DNA and abundance of some mitochondrial gene transcripts in early mouse embryos Dev. Biol. 123 1987 364 374
35. K. Reinhardt, D.K. Dowling, and E.H. Morrow Medicine. Mitochondrial replacement, evolution, and the clinic Science 341 2013 1345 1346
36. R. Sanders, J.F. Huggett, C.A. Bushell, S. Cowen, D.J. Scott, and C.A. Foy Evaluation of digital PCR for absolute DNA quantification Anal. Chem. 83 2011 6474 6484
37. F. Santos, A.H. Peters, A.P. Otte, W. Reik, and W. Dean Dynamic chromatin modifications characterise the first cell cycle in mouse embryos Dev. Biol. 280 2005 225 236
38. T.A. Santos, S. El Shourbagy, and J.C. St John Mitochondrial content reflects oocyte variability and fertilization outcome Fertil. Steril. 85 2006 584 591
39. A. Sato, T. Kono, K. Nakada, K. Ishikawa, S.-I. Inoue, H. Yonekawa, and J.-I. Hayashi Gene therapy for progeny of mito-mice carrying pathogenic mtDNA by nuclear transplantation Proc. Natl. Acad. Sci. USA 102 2005 16765 16770
40. E.A. Schon, S. DiMauro, and M. Hirano Human mitochondrial DNA: roles of inherited and somatic mutations Nat. Rev. Genet. 13 2012 878 890
41. J. Steffann, N. Frydman, N. Gigarel, P. Burlet, P.F. Ray, R. Fanchin, E. Feyereisen, V. Kerbrat, G. Tachdjian, and J.-P. Bonnefont et al. Analysis of mtDNA variant segregation during early human embryonic development: a tool for successful NARP preimplantation diagnosis J. Med. Genet. 43 2006 244 247
42. N. Steuerwald, J.A. Barritt, R. Adler, H. Malter, T. Schimmel, J. Cohen, and C.A. Brenner Quantification of mtDNA in single oocytes, polar bodies and subcellular components by real-time rapid cycle fluorescence monitored PCR Zygote 8 2000 209 215
43. J.B. Stewart, C. Freyer, J.L. Elson, A. Wredenberg, Z. Cansu, A. Trifunovic, and N.-G. Larsson Strong purifying selection in transmission of mammalian mitochondrial DNA PLoS Biol. 6 2008 e10
44. M. Tachibana, M. Sparman, H. Sritanaudomchai, H. Ma, L. Clepper, J. Woodward, Y. Li, C. Ramsey, O. Kolotushkina, and S. Mitalipov Mitochondrial gene replacement in primate offspring and embryonic stem cells Nature 461 2009 367 372
45. M. Tachibana, P. Amato, M. Sparman, J. Woodward, D.M. Sanchis, H. Ma, N.M. Gutierrez, R. Tippner-Hedges, E. Kang, and H.-S. Lee et al. Towards germline gene therapy of inherited mitochondrial diseases Nature 493 2013 627 631
46. S.D. Taylor, N.G. Ericson, J.N. Burton, T.A. Prolla, J.R. Silber, J. Shendure, and J.H. Bielas Targeted enrichment and high-resolution digital profiling of mitochondrial DNA deletions in human brain Aging Cell 13 2014 29 38
47. G.W. van der Heijden, J.W. Dieker, A.A.H.A. Derijck, S. Muller, J.H.M. Berden, D.D.M. Braat, J. van der Vlag, and P. de Boer Asymmetry in histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote Mech. Dev. 122 2005 1008 1022
48. B. Vogelstein, and K.W. Kinzler Digital PCR Proc. Natl. Acad. Sci. USA 96 1999 9236 9241
49. T. Wai, D. Teoli, and E.A. Shoubridge The mitochondrial DNA genetic bottleneck results from replication of a subpopulation of genomes Nat. Genet. 40 2008 1484 1488
50. T. Wakayama, and R. Yanagimachi The first polar body can be used for the production of normal offspring in mice Biol. Reprod. 59 1998 100 104
51. T. Wakayama, Y. Hayashi, and A. Ogura Participation of the female pronucleus derived from the second polar body in full embryonic development of mice J. Reprod. Fertil. 110 1997 263 266
52. S. Wakayama, T. Hikichi, R. Suetsugu, Y. Sakaide, H.-T. Bui, E. Mizutani, and T. Wakayama Efficient establishment of mouse embryonic stem cell lines from single blastomeres and polar bodies Stem Cells 25 2007 986 993
53. D.C. Wallace, and W. Fan The pathophysiology of mitochondrial disease as modeled in the mouse Genes Dev. 23 2009 1714 1736
54. H.E. White, V.J. Durston, A. Seller, C. Fratter, J.F. Harvey, and N.C.P. Cross Accurate detection and quantitation of heteroplasmic mitochondrial point mutations by pyrosequencing Genet. Test. 9 2005 190 199
55. D. Gray, B. Plusa, K. Piotrowska, J. Na, B. Tom, D.M. Glover, and M. Zernicka-Goetz First cleavage of the mouse embryo responds to change in egg shape at fertilization Curr. Biol. 14 2004 397 405
56. J.F. Huggett, C.A. Foy, V. Benes, K. Emslie, J.A. Garson, R. Haynes, J. Hellemans, M. Kubista, R.D. Mueller, and T. Nolan et al. The digital MIQE guidelines: Minimum Information for Publication of Quantitative Digital PCR Experiments Clin. Chem. 59 2013 892 902
57. V. Marx PCR: paths to sensitivity Nat. Methods 11 2014 241 245