Mitochondrial replacement: From basic research to assisted reproductive technology portfolio tool-technicalities and possible risks

Molecular Human Reproduction

Volumn 21, Issue 1, 2015, Pages 3-10

  Cree, Lynsey ^a,b   Loi, Pasqualino ^c  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b Fertility Associates   (New Zealand)

^c UNIVERSITY OF TERAMO   (Italy)

Author keywords

Cytoplasmic transfer; Mitochondrial disease; Mitochondrial DNA; Nuclear transfer; PGD

Indexed keywords

ARTICLE; AUTISM; BASIC RESEARCH; CELL NUCLEUS TRANSPLANTATION; CELL TRANSFER; CYTOPLASM; DISORDERS OF MITOCHONDRIAL FUNCTIONS; EMBRYO DEVELOPMENT; GENE MUTATION; HUMAN; INFERTILITY THERAPY; MICROMANIPULATION; MITOCHONDRION; NONHUMAN; OOCYTE; OOCYTE DONATION; OOCYTE MATURATION; PREGNANCY; PRIORITY JOURNAL; PROGENY; TURNER SYNDROME; ZYGOTE; GENE THERAPY; GENETICS; GERMLINE MUTATION; MITOCHONDRIAL DISEASES; MUTATION;

MITOCHONDRIAL DNA;

DNA, MITOCHONDRIAL; GENETIC THERAPY; GERM-LINE MUTATION; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DISEASES; MUTATION; REPRODUCTIVE TECHNIQUES, ASSISTED;

EID: 84922420186     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gau082     Document Type: Article

References (81)

1. Acton BM, Lai I, Shang X, Jurisicova A, Casper RF. Neutral mitochondrial heteroplasmy alters physiological function in mice. Biol Reprod 2007; 77: 569-576.
2. Barritt JA, Brenner CA, Willadsen S, Cohen J. Spontaneous and artificial changes in human ooplasmic mitochondria. Hum Reprod 2000; 15 Suppl 2:207-217.
3. Barritt J, Willadsen S, Brenner C, Cohen J. Cytoplasmic transfer in assisted reproduction. Hum Reprod Update 2001a; 7: 428-435.
4. Barritt JA, Brenner CA, Malter HE, Cohen J. Mitochondria in human offspring derived from ooplasmic transplantation. Hum Reprod 2001b; 16: 513-516.
5. Bredenoord AL, Pennings G, Smeets HJ, de Wert G. Dealing with uncertainties: ethics of prenatal diagnosis and preimplantation genetic diagnosis to prevent mitochondrial disorders. Hum Reprod update 2008; 14: 83-94.
6. Bredenoord A, Dondorp W, Pennings G, de Die-Smulders C, Smeets B, de Wert G. Preimplantation genetic diagnosis for mitochondrial DNA disorders: ethical guidance for clinical practice. Eur J Hum Genet 2009; 17: 1550-1559.
7. Brenner CA, Barritt JA, Willadsen S, Cohen J. Mitochondrial DNA heteroplasmy after human ooplasmic transplantation. Fertil Steril 2000; 74: 573-578.
8. Brenner CA, Kubisch HM, Pierce KE. Role of the mitochondrial genome in assisted reproductive technologies and embryonic stem cell-based therapeutic cloning. Reprod Fertil Dev 2004; 16: 743-751.
9. Brown DT, Samuels DC, Michael EM, Turnbull DM, Chinnery PF. Random genetic drift determines the level of mutant mtDNA in human primary oocytes. Am J Hum Genet 2001; 68: 533-536.
10. Brown DT, Herbert M, Lamb VK, Chinnery PF, Taylor RW, Lightowlers RN, Craven L, Cree L, Gardner JL, Turnbull DM. Transmission of mitochondrial DNA disorders: possibilities for the future. Lancet 2006; 368: 87-89.
11. Cheng Y, Lei L, Wen DC, Zhu Z, Sun QY, Chen DY. Development of mouse embryos derived from oocytes reconstructed by metaphase I spindle transfer. Zygote 2003; 11: 53-59.
12. Chiaratti MR, Bressan FF, Ferreira CR, Caetano AR, Smith LC, Vercesi AE, Meirelles FV. Embryo mitochondrial DNA depletion is reversed during early embryogenesis in cattle. Biol Reprod 2010; 82: 76-85.
13. Chinnery PF, Howell N, Lightowlers RN, Turnbull DM. Molecular pathology of MELAS and MERRF. The relationship between mutation load and clinical phenotypes. Brain 1997;120(Pt 10):1713-1721.
14. Chinnery PF, Johnson MA, Wardell TM, Singh-Kler R, Hayes C, Brown DT, Taylor RW, Bindoff LA, Turnbull DM. The epidemiology of pathogenic mitochondrial DNA mutations. Ann Neurol 2000a; 48: 188-193.
15. Chinnery PF, Thorburn DR, Samuels DC, White SL, Dahl HM, Turnbull DM, Lightowlers RN, Howell N. The inheritance of mitochondrial DNA heteroplasmy: random drift, selection or both? Trends Genet 2000b; 16:500-505.
16. 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: 186-187.
17. Craven L, Tuppen HA, Greggains GD, Harbottle SJ, Murphy JL, Cree LM, Murdoch AP, Chinnery PF, Taylor RW, Lightowlers RN et al. Pronuclear transfer in human embryos to prevent transmission of mitochondrial DNA disease. Nature 2010; 465: 82-85.
18. Craven L, Elson JL, Irving L, Tuppen HA, Lister LM, Greggains GD, Byerley S, Murdoch AP, Herbert M, Turnbull D. Mitochondrial DNA disease: new options for prevention. Hum Mol Genet 2011; 20(R2): R168-R174.
19. Cree LM, Samuels DC, Chinnery PF. The inheritance of pathogenic mitochondrial DNA mutations. Biochim Biophys Acta 2009; 1792: 1097-1102.
20. Cummins JM. Mitochondria: potential roles in embryogenesis and nucleocytoplasmic transfer. Hum Reprod Update 2001; 7: 217-228.
21. Desmyttere S, De Rycke M, Staessen C, Liebaers I, De Schrijver F, Verpoest W, Haentjens P, Bonduelle M. Neonatal follow-up of 995 consecutively born children after embryo biopsy for PGD. Hum Reprod 2012; 27: 288-293.
22. Elliott HR, Samuels DC, Eden JA, Relton CL, Chinnery PF. Pathogenic mitochondrial DNA mutations are common in the general population. Am J Hum Genet 2008; 83: 254-260.
23. Fan W, Waymire KG, Narula N, Li P, Rocher C, Coskun PE, Vannan MA, Narula J, Macgregor GR, Wallace DC. A mouse model of mitochondrial disease reveals germline selection against severe mtDNA mutations. Science 2008; 319: 958-962.
24. Ferreira CR, Burgstaller JP, Perecin F, Garcia JM, Chiaratti MR, Meo SC, Muller M, Smith LC, Meirelles FV, Steinborn R. Pronounced segregation of donor mitochondria introduced by bovine ooplasmic transfer to the female germ-line. Biol Reprod 2010; 82: 563-571.
25. Haites N, R L-B. Scientific review of the safety and efficacy methods to avoid mitochondrial disease through assistedconception. 2011; from www.hfea.gov.uk/docs2011-04-16_Mitochondria_review_-_final_report.PD.
26. Hellebrekers DM, Wolfe R, Hendrickx AT, de Coo IF, de Die CE, Geraedts JP, Chinnery PF, Smeets HJ. PGD and heteroplasmic mitochondrial DNA point mutations: a systematic review estimating the chance of healthy offspring. Hum Reprod Update 2012; 18: 341-349.
27. Hiiragi T, Solter D. First cleavage plane of the mouse egg is not predetermined but defined by the topology of the two apposing pronuclei. Nature 2004; 430: 360-364.
28. Iuso D, Czernik M, Zacchini F, Ptak G, Loi P. A simplified approach for oocyte enucleation in Mammalian cloning. Cell Reprogram 2013; 15: 490-494.
29. Jin HX, Xin ZM, Song WY, Dai SJ, Sun YP. Effects of human cumulus cells on in vitro fertilization outcomes and its significance in short-term insemination. J Reprod Med 2013; 58: 51-54.
30. Keefe D, Liu L, Wang W, Silva C. Imaging meiotic spindles by polarization light microscopy: principles and applications to IVF. Reprod Biomed Online 2003; 7: 24-29.
31. Kono T, Tsunoda Y. Effects of induction current and other factors on large-scale electrofusion for pronuclear transplantation of mouse eggs. Gamete Res 1988; 19: 349-357.
32. Larsson NG, Holme E, Kristiansson B, Oldfors A, Tulinius M. Progressive increase of the mutated mitochondrial DNA fraction in Kearns-Sayre syndrome. Pediatr Res 1990; 28: 131-136.
33. Levy R, Elder K, Menezo Y. Cytoplasmic transfer in oocytes: biochemical aspects. Hum Reprod Update 2004; 10: 241-250.
34. Li GP, Chen DY, Lian L, Sun QY, Wang MK, Liu JL, Li JS, Han ZM. Viable rabbits derived from reconstructed oocytes by germinal vesicle transfer after intracytoplasmic sperm injection (ICSI). Mol Reprod Dev 2001; 58: 180-185.
35. Liu H, Wang CW, Grifo JA, Krey LC, Zhang J. Reconstruction of mouse oocytes by germinal vesicle transfer: maturity of host oocyte cytoplasm determines meiosis. Hum Reprod 1999; 14: 2357-2361.
36. Liu S, Li Y, Gao X, Yan JH, Chen ZJ. Changes in the distribution of mitochondria before and after in vitro maturation of human oocytes and the effect of in vitro maturation on mitochondria distribution. Fertil Steril 2010; 93: 1550-1555.
37. Malter HE, Cohen J. Ooplasmic transfer: animal models assist human studies. Reprod Biomed Online 2002; 5: 26-35.
38. McFarland R, Taylor RW, Turnbull DM. A neurological perspective on mitochondrial disease. Lancet Neurol 2010; 9: 829-840.
39. McGrath J, Solter D. Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 1984; 37: 179-183.
40. Mitalipov S, Amato P, Parry S, Falk MJ. Limitations of preimplantation genetic diagnosis for mitochondrial DNA diseases. Cell Rep 2014; 7: 935-937.
41. Monnot S, Gigarel N, Samuels DC, Burlet P, Hesters L, Frydman N, Frydman R, Kerbrat V, Funalot B, Martinovic J et al. Segregation of mtDNA throughout human embryofetal development: m.3243A>G as a model system. Hum Mutat 2011;32:116-125.
42. Muggleton-Harris A, Whittingham DG, Wilson L. Cytoplasmic control of preimplantation development in vitro in the mouse. Nature 1982; 299: 460-462.
43. Parikh S, Saneto R, Falk MJ, Anselm I, Cohen BH, Haas R, Medicine Society TM. A modern approach to the treatment of mitochondrial disease. Curr Treat Options Neurol 2009; 11: 414-430.
44. Paull D, Emmanuele V, Weiss KA, Treff N, Stewart L, Hua H, Zimmer M, Kahler DJ, Goland RS, Noggle SA et al. Nuclear genome transfer in human oocytes eliminates mitochondrial DNA variants. Nature 2013; 493: 632-637.
45. Piotrowska K, Zernicka-Goetz M. Early patterning of the mouse embryo-contributions of sperm and egg. Development 2002; 129: 5803-5813.
46. Piotrowska-Nitsche K, Perea-Gomez A, Haraguchi S, Zernicka-Goetz M. Four-cell stage mouse blastomeres have different developmental properties. Development 2005; 132: 479-490.
47. Poulton J, Bredenoord AL. 174th ENMC international workshop: applying pre-implantation genetic diagnosis to mtDNA diseases: implications of scientific advances 19-21 March 2010, Naarden, The Netherlands. Neuromuscul Disord 2010; 20: 559-563.
48. Poulton J, Kennedy S, Oakeshott P, Wells D. Preventing transmission of maternally inherited mitochondrial DNA diseases. BMJ 2009; 338: b94.
49. Poulton J, Chiaratti MR, Meirelles FV, Kennedy S, Wells D, Holt IJ. Transmission of mitochondrial DNA diseases and ways to prevent them. PLoS Genet 2010; 6: e1001066.
50. Rahman S, Poulton J, Marchington d, Suomalainen A. Decrease of 3243 A->G mtDNA mutation from blood in MELAS syndrome: a longitudinal study. Am J Hum Genet 2001; 68: 238-240.
51. Reinhardt K, Dowling DK, Morrow EH. Medicine. Mitochondrial replacement, evolution, and the clinic. Science 2013;341:1345-1346.
52. Sacconi S, Salviati L, Nishigaki Y, Walker WF, Hernandez-Rosa E, Trevisson E, Delplace S, Desnuelle C, Shanske S, Hirano M et al. A functionally dominant mitochondrial DNA mutation. Hum Mol Genet 2008; 17: 1814-1820.
53. Sallevelt SC, Dreesen JC, Drusedau M, Spierts S, Coonen E, van Tienen FH, van Golde RJ, de Coo IF, Geraedts JP, de Die-Smulders CE et al. Preimplantation genetic diagnosis in mitochondrial DNA disorders: challenge and success. J Med Genet 2013; 50: 125-132.
54. Sato A, Kono T, Nakada K, Ishikawa K, Inoue S, Yonekawa H, Hayashi J. Gene therapy for progeny of mito-mice carrying pathogenic mtDNA by nuclear transplantation. Proc Natl Acad Sci USA 2005; 102: 16765-16770.
55. Samuels DC, Wonnapinij P, Chinnery PF. Preventing the transmission of pathogenic mitochondrial DNA mutations: Can we achieve long-term benefits from germ-line gene transfer?. Hum Reprod 2013; 28: 554-559.
56. Schaefer AM, McFarland R, Blakely EL, He L, Whittaker RG, Taylor RW, Chinnery PF, Turnbull DM. Prevalence of mitochondrial DNA disease in adults. Ann Neurol 2008; 63: 35-39.
57. Soini S, Ibarreta D, Anastasiadou V, Ayme S, Braga S, Cornel M, Coviello DA, Evers-Kiebooms G, Geraedts J, Gianaroli L et al. The interface between assisted reproductive technologies and genetics: technical, social, ethical and legal issues. Eur J Hum Genet 2006; 14: 588-645.
58. Spikings EC, Alderson J, St John JC. Transmission of mitochondrial DNA following assisted reproduction and nuclear transfer. Hum Reprod Update 2006; 12: 401-415.
59. Steffann J, Frydman N, Gigarel N, Burlet P, Ray PF, Fanchin R, Feyereisen E, Kerbrat V, Tachdjian G, Bonnefont JP et al. Analysis of mtDNA variant segregation during early human embryonic development: a tool for successful NARP preimplantation diagnosis. J Med Genet 2006; 43: 244-247.
60. Steffann J, Gigarel N, Corcos J, Bonniere M, Encha-Razavi F, Sinico M, Prevot S, Dumez Y, Yamgnane A, Frydman R et al. Stability of the m.8993T->G mtDNA mutation load during human embryofetal development has implications for the feasibility of prenatal diagnosis in NARP syndrome. J Med Genet 2007;44:664-669.
61. Stewart JB, Freyer C, Elson JL, Wredenberg A, Cansu Z, Trifunovic A, Larsson NG. Strong purifying selection in transmission of mammalian mitochondrial DNA. PLoS Biol 2008; 6: e10.
62. St John JC, Campbell KH. The battle to prevent the transmission of mitochondrial DNA disease: is karyoplast transfer the answer? Gene Ther 2010;17:147-149.
63. Tachibana M, Sparman M, Sritanaudomchai H, Ma H, Clepper L, Woodward J, Li Y, Ramsey C, Kolotushkina O, Mitalipov S. Mitochondrial gene replacement in primate offspring and embryonic stem cells. Nature 2009; 461: 367-372.
64. Tachibana M, Sparman M, Mitalipov S. Chromosome transfer in mature oocytes. Nat Protoc 2010; 5: 1138-1147.
65. Tachibana M, Amato P, Sparman M, Woodward J, Sanchis DM, Ma H, Gutierrez NM, Tippner-Hedges R, Kang E, Lee HS et al. Towards germline gene therapy of inherited mitochondrial diseases. Nature 2013; 493: 627-631.
66. Takeuchi T, Gong J, Veeck LL, Rosenwaks Z, Palermo GD. Preliminary findings in germinal vesicle transplantation of immature human oocytes. Hum Reprod 2001; 16: 730-736.
67. Takeuchi T, Rosenwaks Z, Palermo GD. A successful model to assess embryo development after transplantation of prophase nuclei. Hum Reprod 2004; 19: 975-981.
68. Tanaka A, Nagayoshi M, Awata S, Himeno N, Tanaka I, Watanabe S, Kusunoki H. Metaphase II karyoplast transfer from human in-vitro matured oocytes to enucleated mature oocytes. Reprod Biomed Online 2009a; 19: 514-520.
69. Tanaka A, Nagayoshi M, Awata S, Tanaka I, Watanabe S, Kusunoki H. A novel trial of nuclear transfer for repairing an aged oocyte. Fertil Steril 2009b; 92:S58.
70. Tarkowski AK, Balakier H. Nucleo-cytoplasmic interactions in cell hybrids between mouse oocytes, blastomeres and somatic cells. J Embryol Exp Morphol 1980; 55: 319-330.
71. Torres-Padilla ME, Parfitt DE, Kouzarides T, Zernicka-Goetz M. Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 2007; 445: 214-218.
72. Treff NR, Campos J, Tao X, Levy B, Ferry KM, Scott RT Jr. Blastocyst preimplantation genetic diagnosis (PGD) of a mitochondrial DNA disorder. Fertil Steril 2012; 98: 1236-1240.
73. 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: 2621-2633.
74. Wallace DC, Chalkia D. Mitochondrial DNA genetics and the heteroplasmy conundrum in evolution and disease. Cold Spring Harb Perspect Med 2013; 3: a021220.
75. Wang MK, Chen DY, Liu JL, Li GP, Sun QY. In vitro fertilisation of mouse oocytes reconstructed by transfer of metaphase II chromosomes results in live births. Zygote 2001; 9: 9-14.
76. White SL, Collins VR, Wolfe R, Cleary MA, Shanske S, DiMauro S, Dahl HH, Thorburn DR. Genetic counseling and prenatal diagnosis for the mitochondrial DNA mutations at nucleotide 8993. Am J Hum Genet 1999a; 65: 474-482.
77. White SL, Shanske S, Biros I, Warwick L, Dahl HM, Thorburn DR, Di Mauro S. Two cases of prenatal analysis for the pathogenic T to G substitution at nucleotide 8993 in mitochondrial DNA. Prenat Diagn 1999b; 19: 1165-1168.
78. Wigglesworth K, Lee KB, O'Brien MJ, Peng J, Matzuk MM, Eppig JJ. Bidirectional communication between oocytes and ovarian follicular somatic cells is required for meiotic arrest of mammalian oocytes. Proc Natl Acad Sci USA 2013; 110:E3723-E3729.
79. Wilding M, Dale B, Marino M, di Matteo L, Alviggi C, Pisaturo ML, Lombardi L, De Placido G. Mitochondrial aggregation patterns and activity in human oocytes and preimplantation embryos. Hum Reprod 2001; 16: 909-917.
80. Yu Y, Wu J, Fan Y, Lv Z, Guo X, Zhao C, Zhou R, Zhang Z, Wang F, Xiao M et al. Evaluation of blastomere biopsy using a mouse model indicates the potential high risk of neurodegenerative disorders in the offspring. Mol Cell Proteomics 2009; 8: 1490-1500.
81. Zhang J, Wang CW, Krey L, Liu H, Meng L, Blaszczyk A, Adler A, Grifo J. In vitro maturation of human preovulatoryoocytes reconstructed by germinal vesicle transfer. Fertil Steril 1999; 71: 726-731.