Towards clinical application of pronuclear transfer to prevent mitochondrial DNA disease

Nature

Volumn 534, Issue 7607, 2016, Pages 383-386

  Hyslop, Louise A ^a,b   Blakeley, Paul ^c   Craven, Lyndsey ^d   Richardson, Jessica ^a   Fogarty, Norah M E ^c   Fragouli, Elpida ^e   Lamb, Mahdi ^a   Wamaitha, Sissy E ^c   Prathalingam, Nilendran ^a,b   Zhang, Qi ^a,g   O'Keefe, Hannah ^a   Takeda, Yuko ^a   Arizzi, Lucia ^a,b   Alfarawati, Samer ^e   Tuppen, Helen A ^d   Irving, Laura ^a,h   Kalleas, Dimitrios ^a,i   Choudhary, Meenakshi ^b   Wells, Dagan ^f   Murdoch, Alison P ^b   Turnbull, Douglass M ^d   Niakan, Kathy K ^c   Herbert, Mary ^a,b   more..

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b Newcastle upon Tyne Hospitals NHS Trust   (United Kingdom)

^c THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

^e Reprogenetics LLC   (United States)

^f UNIVERSITY OF OXFORD   (United Kingdom)

^g BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^h QUEEN ELIZABETH HOSPITAL   (United Kingdom)

ⁱ ST MARY S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA;

CELLS AND CELL COMPONENTS; CHILD; DEVELOPMENTAL BIOLOGY; GENE EXPRESSION; MITOCHONDRIAL DNA; MUTATION;

ANEUPLOIDY; ANIMAL CELL; ARTICLE; BLASTOCYST; CELL LINEAGE; CELL NUCLEUS TRANSPLANTATION; CELL SURVIVAL; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; FEMALE; GENE EXPRESSION; HETEROPLASMY; HUMAN; HUMAN CELL; MEIOSIS; MITOCHONDRIAL DNA DISORDER; MITOCHONDRIAL GENE; MITOSIS; MOUSE; NONHUMAN; PRECLINICAL STUDY; PRIORITY JOURNAL; STEM CELL LINE; ZYGOTE; ADULT; CELL NUCLEUS; CYTOLOGY; CYTOPLASM; GENE EXPRESSION PROFILING; GENETICS; MALE; METABOLISM; MITOCHONDRIAL DISEASES; MITOCHONDRIAL REPLACEMENT THERAPY; MITOCHONDRION; PATHOLOGY; PROCEDURES; STEM CELL; TRANSLATIONAL RESEARCH; YOUNG ADULT;

ADULT; BLASTOCYST; CELL NUCLEUS; CYTOPLASM; DNA, MITOCHONDRIAL; FEMALE; GENE EXPRESSION PROFILING; HUMANS; MALE; MEIOSIS; MITOCHONDRIA; MITOCHONDRIAL DISEASES; MITOCHONDRIAL REPLACEMENT THERAPY; NUCLEAR TRANSFER TECHNIQUES; STEM CELLS; TRANSLATIONAL MEDICAL RESEARCH; YOUNG ADULT; ZYGOTE;

EID: 84975832568     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature18303     Document Type: Article

References (42)

1. Schon, E. A., DiMauro, S. & Hirano, M. Human mitochondrial DNA: roles of inherited and somatic mutations. Nature Rev. Genet. 13, 878-890 (2012).
2. Craven, L. et al. Pronuclear transfer in human embryos to prevent transmission of mitochondrial DNA disease. Nature 465, 82-85 (2010).
3. Wallace, D. C. & Chalkia, D. Mitochondrial DNA genetics and the heteroplasmy conundrum in evolution and disease. Cold Spring Harb. Perspect. Biol. 5, a021220 (2013).
4. McFarland, R. et al. Multiple neonatal deaths due to a homoplasmic mitochondrial DNA mutation. Nature Genet. 30, 145-146 (2002).
5. Steffann, J. et al. Data from artificial models of mitochondrial DNA disorders are not always applicable to humans. Cell Reports 7, 933-934 (2014).
6. Richardson, J. et al. Concise reviews: Assisted reproductive technologies to prevent transmission of mitochondrial DNA disease. Stem Cells 33, 639-645 (2015).
7. Tachibana, M. et al. Towards germline gene therapy of inherited mitochondrial diseases. Nature 493, 627-631 (2013).
8. Paull, D. et al. Nuclear genome transfer in human oocytes eliminates mitochondrial DNA variants. Nature 493, 632-637 (2013).
9. McGrath, J. & Solter, D. Nuclear transplantation in the mouse embryo by microsurgery and cell fusion. Science 220, 1300-1302 (1983).
10. Fenwick, J., Platteau, P., Murdoch, A. P. & Herbert, M. Time from insemination to first cleavage predicts developmental competence of human preimplantation embryos in vitro. Hum. Reprod. 17, 407-412 (2002).
11. Schatten, H. & Sun, Q. Y. The role of centrosomes in mammalian fertilization and its significance for ICSI. Mol. Hum. Reprod. 15, 531-538 (2009).
12. Niakan, K. K., Han, J., Pedersen, R. A., Simon, C. & Pera, R. A. R. Human pre-implantation embryo development. Development 139, 829-841 (2012).
13. Forman, E. J. et al. Oocyte vitrification does not increase the risk of embryonic aneuploidy or diminish the implantation potential of blastocysts created after intracytoplasmic sperm injection: A novel, paired randomized controlled trial using DNA fingerprinting. Fertil. Steril. 98, 644-649 (2012).
14. Blakeley, P. et al. Defining the three cell lineages of the human blastocyst by single-cell RNA-seq. Development 142, 3151-3165 (2015).
15. van der Maaten, L. & Hinton, G. Visualizing high-dimensional data using t-SNE. J. Mach. Learn. Res. 9, 2579-2605 (2008).
16. Hellebrekers, D. M. E. I. et al. PGD and heteroplasmic mitochondrial DNA point mutations: A systematic review estimating the chance of healthy offspring. Hum. Reprod. Update 18, 341-349 (2012).
17. Samuels, D. C., Wonnapinij, P. & Chinnery, P. F. Preventing the transmission of pathogenic mitochondrial DNA mutations: can we achieve long-Term benefits from germ-line gene transfer? Hum. Reprod. 28, 554-559 (2013).
18. Facucho-Oliveira, J. M. & St John, J. C. The relationship between pluripotency and mitochondrial DNA proliferation during early embryo development and embryonic stem cell differentiation. Stem Cell Rev. 5, 140-158 (2009).
19. Burgstaller, J. P., Johnston, I. G. & Poulton, J. Mitochondrial DNA disease and developmental implications for reproductive strategies. Mol. Hum. Reprod. 21, 11-22 (2015).
20. Hämäläinen, R. H. et al. Tissue-And cell-Type-specific manifestations of heteroplasmic mtDNA 3243A>G mutation in human induced pluripotent stem cell-derived disease model. Proc. Natl Acad. Sci. USA 110, E3622-E3630 (2013).
21. Lee, H. S. et al. Rapid mitochondrial DNA segregation in primate preimplantation embryos precedes somatic and germline bottleneck. Cell Reports 1, 506-515 (2012).
22. Treff, N. R. et al. Blastocyst preimplantation genetic diagnosis (PGD) of a mitochondrial DNA disorder. Fertil. Steril. 98, 1236-1240 (2012).
23. Mitalipov, S., Amato, P., Parry, S. & Falk, M. J. Limitations of preimplantation genetic diagnosis for mitochondrial DNA diseases. Cell Reports 7, 935-937 (2014).
24. Sallevelt, S. C. E. H. et al. Preimplantation genetic diagnosis in mitochondrial DNA disorders: challenge and success. J. Med. Genet. 50, 125-132 (2013).
25. Steffann, J. et al. Analysis of mtDNA variant segregation during early human embryonic development: A tool for successful NARP preimplantation diagnosis. J. Med. Genet. 43, 244-247 (2006).
26. Herbert, M., Kalleas, D., Cooney, D., Lamb, M. & Lister, L. Meiosis and maternal aging: insights from aneuploid oocytes and trisomy births. Cold Spring Harb. Perspect. Biol. 7, a017970 (2015).
27. Choudhary, M. et al. Egg sharing for research: A successful outcome for patients and researchers. Cell Stem Cell 10, 239-240 (2012).
28. HFEA Guidance on Payments for Donors. HFEA Code of Practice Section 13 http://www.hfea.gov.uk/500.html (Human Fertilisation and Embryology Authority, 2009).
29. Hyslop, L. et al. A novel isolator-based system promotes viability of human embryos during laboratory processing. PLoS ONE 7, e31010 (2012).
30. Cutting, R., Morroll, D., Roberts, S. A., Pickering, S. & Rutherford, A. Elective single embryo transfer: guidelines for practice British Fertility Society and Association of Clinical Embryologists. Hum. Fertil. (Camb.) 11, 131-146 (2008).
31. Stephenson, E. L., Braude, P. R. & Mason, C. International community consensus standard for reporting derivation of human embryonic stem cell lines. Regen. Med. 2, 349-362 (2007).
32. Wells, D. et al. Clinical utilisation of a rapid low-pass whole genome sequencing technique for the diagnosis of aneuploidy in human embryos prior to implantation. J. Med. Genet. 51, 553-562 (2014).
33. Kim, D. et al. TopHat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).
34. Anders, S., Pyl, P. T. & Huber, W. HTSeq-A Python framework to work with high-Throughput sequencing data. Bioinformatics 31, 166-169 (2015).
35. Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140 (2010).
36. Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
37. Taylor, R. W., Taylor, G. A., Durham, S. E. & Turnbull, D. M. The determination of complete human mitochondrial DNA sequences in single cells: implications for the study of somatic mitochondrial DNA point mutations. Nucleic Acids Res. 29, e74 (2001).
38. Andrews, R. M. et al. Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nature Genet. 23, 147 (1999).
39. Greaves, L. C. et al. Clonal expansion of early to mid-life mitochondrial DNA point mutations drives mitochondrial dysfunction during human ageing. PLoS Genet. 10, e1004620 (2014).
40. Wamaitha, S. E. et al. Gata6 potently initiates reprograming of pluripotent and differentiated cells to extraembryonic endoderm stem cells. Genes Dev. 29, 1239-1255 (2015).
41. Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L. & Wold, B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods 5, 621-628 (2008).
42. White, H. E. et al. Accurate detection and quantitation of heteroplasmic mitochondrial point mutations by pyrosequencing. Genet. Test. 9, 190-199 (2005).