The Effects of Nuclear Reprogramming on Mitochondrial DNA Replication

Stem Cell Reviews and Reports

Volumn 9, Issue 1, 2013, Pages 1-15

  Kelly, Richard D W ^a,b   Sumer, Huseyin ^a   McKenzie, Matthew ^a   Facucho Oliveira, Joao ^b,c   Trounce, Ian A ^d   Verma, Paul J ^a   St John, Justin C ^a,b  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c UNIVERSITY OF ALGARVE   (Portugal)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

mitochondrial DNA (mtDNA); mtDNA replication; Pluripotency; Reprogramming

Indexed keywords

IPS;

EID: 84873741361     PISSN: 15508943     EISSN: 15586804     Source Type: Journal    
DOI: 10.1007/s12015-011-9318-7     Document Type: Article

References (83)

1. Anderson, S., Bankier, A. T., Barrell, B. G., de Bruijn, M. H., Coulson, A. R., et al. (1981). Sequence and organization of the human mitochondrial genome. Nature, 290, 457-465.
2. Pfeiffer, T., Schuster, S., & Bonhoeffer, S. (2001). Cooperation and competition in the evolution of ATP-producing pathways. Science, 292, 504-507.
3. Fernandez-Vizarra, E., Tiranti, V., & Zeviani, M. (2009). Assembly of the oxidative phosphorylation system in humans: what we have learned by studying its defects. Biochimica et Biophysica Acta, 1793, 200-211.
4. Lazarou, M., Thorburn, D. R., Ryan, M. T., & McKenzie, M. (2009). Assembly of mitochondrial complex I and defects in disease. Biochimica et Biophysica Acta, 1793, 78-88.
5. McKenzie, M., & Ryan, M. T. (2010). Assembly factors of human mitochondrial complex I and their defects in disease. IUBMB Life, 62, 497-502.
6. Wallace, D. C. (1999). Mitochondrial diseases in man and mouse. Science, 283, 1482-1488.
7. Smeitink, J., van den Heuvel, L., & DiMauro, S. (2001). The genetics and pathology of oxidative phosphorylation. Nature Reviews Genetics, 2, 342-352.
8. Clayton, D. A. (1982). Replication of animal mitochondrial DNA. Cell, 28, 693-705.
9. Korhonen, J. A., Gaspari, M., & Falkenberg, M. (2003). TWINKLE Has 5′ -> 3′ DNA helicase activity and is specifically stimulated by mitochondrial single-stranded DNA-binding protein. Journal of Biological Chemistry, 278, 48627-48632.
10. Lazarou, M., McKenzie, M., Ohtake, A., Thorburn, D. R., & Ryan, M. T. (2007). Analysis of the assembly profiles for mitochondrial- and nuclear-DNA-encoded subunits into complex I. Molecular and Cellular Biology, 27, 4228-4237.
11. Spikings, E. C., Alderson, J., & St John, J. C. (2007). Regulated mitochondrial DNA replication during oocyte maturation is essential for successful porcine embryonic development. Biology of Reproduction, 76, 327-335.
12. Thundathil, J., Filion, F., & Smith, L. C. (2005). Molecular control of mitochondrial function in preimplantation mouse embryos. Molecular Reproduction and Development, 71, 405-413.
13. Cao, L., Shitara, H., Horii, T., Nagao, Y., Imai, H., et al. (2007). The mitochondrial bottleneck occurs without reduction of mtDNA content in female mouse germ cells. Nature Genetics, 39, 386-390.
14. Facucho-Oliveira, J. M., Alderson, J., Spikings, E. C., Egginton, S., & St John, J. C. (2007). Mitochondrial DNA replication during differentiation of murine embryonic stem cells. Journal of Cell Science, 120, 4025-4034.
15. Miller, F. J., Rosenfeldt, F. L., Zhang, C., Linnane, A. W., & Nagley, P. (2003). Precise determination of mitochondrial DNA copy number in human skeletal and cardiac muscle by a PCR-based assay: lack of change of copy number with age. Nucleic Acids Research, 31, e61.
16. Bowles, E. J., Lee, J. H., Alberio, R., Lloyd, R. E., Stekel, D., et al. (2007). Contrasting effects of in vitro fertilization and nuclear transfer on the expression of mtDNA replication factors. Genetics, 176, 1511-1526.
17. Leahy, A., Xiong, J. W., Kuhnert, F., & Stuhlmann, H. (1999). Use of developmental marker genes to define temporal and spatial patterns of differentiation during embryoid body formation. The Journal of Experimental Zoology, 284, 67-81.
18. Hance, N., Ekstrand, M. I., & Trifunovic, A. (2005). Mitochondrial DNA polymerase gamma is essential for mammalian embryogenesis. Human Molecular Genetics, 14, 1775-1783.
19. St John, J. C., Facucho-Oliveira, J., Jiang, Y., Kelly, R., & Salah, R. (2010). Mitochondrial DNA transmission, replication and inheritance: a journey from the gamete through the embryo and into offspring and embryonic stem cells. Human Reproductive Update, 16, 488-509.
20. Kelly, R. D., & St John, J. C. (2010). Role of mitochondrial DNA replication during differentiation of reprogrammed stem cells. International Journal of Developmental Biology, 54, 1659-1670.
21. Facucho-Oliveira, J. M., & St John, J. C. (2009). The relationship between pluripotency and mitochondrial DNA proliferation during early embryo development and embryonic stem cell differentiation. Stem Cell Reviews and Reports, 5, 140-158.
22. Cowan, C. A., Atienza, J., Melton, D. A., & Eggan, K. (2005). Nuclear reprogramming of somatic cells after fusion with human embryonic stem cells. Science, 309, 1369-1373.
23. Yu, J., Vodyanik, M. A., He, P., Slukvin, I. I., & Thomson, J. A. (2006). Human embryonic stem cells reprogram myeloid precursors following cell-cell fusion. Stem Cells, 24, 168-176.
24. Takahashi, K., & Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126, 663-676.
25. Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., et al. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell, 131, 861-872.
26. Wilmut, I., Schnieke, A. E., McWhir, J., Kind, A. J., & Campbell, K. H. (1997). Viable offspring derived from fetal and adult mammalian cells. Nature, 385, 810-813.
27. Blelloch, R., Wang, Z., Meissner, A., Pollard, S., Smith, A., et al. (2006). Reprogramming efficiency following somatic cell nuclear transfer is influenced by the differentiation and methylation state of the donor nucleus. Stem Cells, 24, 2007-2013.
28. Dean, W., Santos, F., Stojkovic, M., Zakhartchenko, V., Walter, J., et al. (2001). Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos. Proceedings of the National Academy of Sciences of the United States of America, 98, 13734-13738.
29. Gurdon, J. B., & Melton, D. A. (2008). Nuclear reprogramming in cells. Science, 322, 1811-1815.
30. Lloyd, R. E., Lee, J. H., Alberio, R., Bowles, E. J., Ramalho-Santos, J., et al. (2006). Aberrant nucleo-cytoplasmic cross-talk results in donor cell mtDNA persistence in cloned embryos. Genetics, 172, 2515-2527.
31. Brambrink, T., Hochedlinger, K., Bell, G., & Jaenisch, R. (2006). ES cells derived from cloned and fertilized blastocysts are transcriptionally and functionally indistinguishable. Proceedings of the National Academy of Sciences of the United States of America, 103, 933-938.
32. Kim, K., Doi, A., Wen, B., Ng, K., Zhao, R., et al. (2010). Epigenetic memory in induced pluripotent stem cells. Nature, 467, 285-290.
33. Feng, Q., Lu, S. J., Klimanskaya, I., Gomes, I., Kim, D., et al. (2010). Hemangioblastic derivatives from human induced pluripotent stem cells exhibit limited expansion and early senescence. Stem Cells, 28, 704-712.
34. Hu, B. Y., Weick, J. P., Yu, J., Ma, L. X., Zhang, X. Q., et al. (2010). Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency. Proceedings of the National Academy of Sciences of the United States of America, 107, 4335-4340.
35. Chin, M. H., Mason, M. J., Xie, W., Volinia, S., Singer, M., et al. (2009). Induced pluripotent stem cells and embryonic stem cells are distinguished by gene expression signatures. Cell Stem Cell, 5, 111-123.
36. Hanna, J., Saha, K., Pando, B., van Zon, J., Lengner, C. J., et al. (2009). Direct cell reprogramming is a stochastic process amenable to acceleration. Nature, 462, 595-601.
37. Polo, J. M., Liu, S., Figueroa, M. E., Kulalert, W., Eminli, S., et al. (2010). Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nature Biotechnology, 28, 848-855.
38. Stadtfeld, M., Apostolou, E., Akutsu, H., Fukuda, A., Follett, P., et al. (2010). Aberrant silencing of imprinted genes on chromosome 12qF1 in mouse induced pluripotent stem cells. Nature, 465, 175-181.
39. Mikkelsen, T. S., Hanna, J., Zhang, X., Ku, M., Wernig, M., et al. (2008). Dissecting direct reprogramming through integrative genomic analysis. Nature, 454, 49-55.
40. Sumer, H., Jones, K. L., Liu, J., Heffernan, C., Tat, P. A., et al. (2009). Reprogramming of somatic cells after fusion with iPS and ntES cells. Stem Cells and Development, 19, 239-246.
41. Sumer, H., Nicholls, C., Pinto, A. R., Indraharan, D., Liu, J., et al. (2010). Chromosomal and telomeric reprogramming following ES-somatic cell fusion. Chromosoma, 119, 167-176.
42. Sumer, H., Jones, K. L., Liu, J., Rollo, B. N., van Boxtel, A. L., et al. (2009). Transcriptional changes in somatic cells recovered from embryonic stem-somatic heterokaryons. Stem Cells and Development, 18, 1361-1368.
43. Munsie, M. J., Michalska, A. E., O'Brien, C. M., Trounson, A. O., Pera, M. F., et al. (2000). Isolation of pluripotent embryonic stem cells from reprogrammed adult mouse somatic cell nuclei. Current Biology, 10, 989-992.
44. Keller, G. M. (1995). In vitro differentiation of embryonic stem cells. Current Opinion in Cell Biology, 7, 862-869.
45. McKenzie, M., Lazarou, M., & Ryan, M. T. (2009). Chapter 18 analysis of respiratory chain complex assembly with radiolabeled nuclear- and mitochondrial-encoded subunits. Methods in Enzymology, 456, 321-339.
46. McKenzie, M., Trounce, I. A., Cassar, C. A., & Pinkert, C. A. (2004). Production of homoplasmic xenomitochondrial mice. Proceedings of the National Academy of Sciences of the United States of America, 101, 1685-1690.
47. Trounce, I., & Wallace, D. C. (1996). Production of transmitochondrial mouse cell lines by cybrid rescue of rhodamine-6G pre-treated L-cells. Somatic Cell and Molecular Genetics, 22, 81-85.
48. Silva, J., Chambers, I., Pollard, S., & Smith, A. (2006). Nanog promotes transfer of pluripotency after cell fusion. Nature, 441, 997-1001.
49. Silva, J., Nichols, J., Theunissen, T. W., Guo, G., van Oosten, A. L., et al. (2009). Nanog is the gateway to the pluripotent ground state. Cell, 138, 722-737.
50. Niwa, H., Miyazaki, J., & Smith, A. G. (2000). Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nature Genetics, 24, 372-376.
51. Chen, X., Xu, H., Yuan, P., Fang, F., Huss, M., et al. (2008). Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell, 133, 1106-1117.
52. Hanna, J. H., Saha, K., & Jaenisch, R. (2010). Pluripotency and cellular reprogramming: facts, hypotheses, unresolved issues. Cell, 143, 508-525.
53. Todd, L. R., Damin, M. N., Gomathinayagam, R., Horn, S. R., Means, A. R., et al. (2010). Growth factor erv1-like modulates Drp1 to preserve mitochondrial dynamics and function in mouse embryonic stem cells. Molecular Biology of the Cell, 21, 1225-1236.
54. Rae, P. C., Kelly, R. D., Egginton, S., & St John, J. C. (2011). Angiogenic potential of endothelial progenitor cells and embryonic stem cells. Vascular Cell, 3, 11.
55. Wai, T., Teoli, D., & Shoubridge, E. A. (2008). The mitochondrial DNA genetic bottleneck results from replication of a subpopulation of genomes. Nature Genetics, 40, 1484-1488.
56. Surani, M. A., Durcova-Hills, G., Hajkova, P., Hayashi, K., & Tee, W. W. (2008). Germ line, stem cells, and epigenetic reprogramming. Cold Spring Harbour Symposia on Quantative Biology, 73, 9-15.
57. Kang, J., Shakya, A., & Tantin, D. (2009). Stem cells, stress, metabolism and cancer: a drama in two Octs. Trends in Biochemical Sciences, 34, 491-499.
58. Chambers, I., Silva, J., Colby, D., Nichols, J., Nijmeijer, B., et al. (2007). Nanog safeguards pluripotency and mediates germline development. Nature, 450, 1230-1234.
59. Maldonado-Saldivia, J., van den Bergen, J., Krouskos, M., Gilchrist, M., Lee, C., et al. (2007). Dpp a2 and Dppa4 are closely linked SAP motif genes restricted to pluripotent cells and the germ line. Stem Cells, 25, 19-28.
60. Kehler, J., Tolkunova, E., Koschorz, B., Pesce, M., Gentile, L., et al. (2004). Oct4 is required for primordial germ cell survival. EMBO Reports, 5, 1078-1083.
61. Thomson, M., Liu, S. J., Zou, L. N., Smith, Z., Meissner, A., et al. (2011). Pluripotency factors in embryonic stem cells regulate differentiation into germ layers. Cell, 145, 875-889.
62. Larsson, N. G., Wang, J., Wilhelmsson, H., Oldfors, A., Rustin, P., et al. (1998). Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nature Genetics, 18, 231-236.
63. Larsson, N. G., Oldfors, A., Holme, E., & Clayton, D. A. (1994). Low levels of mitochondrial transcription factor A in mitochondrial DNA depletion. Biochemical and Biophysical Research Communications, 200, 1374-1381.
64. Poulton, J., Morten, K., Freeman-Emmerson, C., Potter, C., Sewry, C., et al. (1994). Deficiency of the human mitochondrial transcription factor h-mtTFA in infantile mitochondrial myopathy is associated with mtDNA depletion. Human Molecular Genetics, 3, 1763-1769.
65. Bhutani, N., Brady, J. J., Damian, M., Sacco, A., Corbel, S. Y., et al. (2010). Reprogramming towards pluripotency requires AID-dependent DNA demethylation. Nature, 463, 1042-1047.
66. Deng, W. (2010). AID in reprogramming: quick and efficient: identification of a key enzyme called AID, and its activity in DNA demethylation, may help to overcome a pivotal epigenetic barrier in reprogramming somatic cells toward pluripotency. Bioessays, 32, 385-387.
67. Evans, M. J., Kaufman, M. H. (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature, 292, 154-156.
68. Cibelli, J. B., Campbell, K. H. S., Seidel, G. E., West, M. D., & Lanza, R. P. (2002). The health profile of cloned animals. Nature Biotechnology, 20, 13-14.
69. Ying, Q. L., Wray, J., Nichols, J., Batlle-Morera, L., Doble, B., et al. (2008). The ground state of embryonic stem cell self-renewal. Nature, 453, 519-523.
70. Prigione, A., Fauler, B., Lurz, R., Lehrach, H., & Adjaye, J. (2010). The senescence-related mitochondrial/oxidative stress pathway is repressed in human induced pluripotent stem cells. Stem Cells, 28, 721-733.
71. Armstrong, L., Tilgner, K., Saretzki, G., Atkinson, S. P., Stojkovic, M., et al. (2010). Human induced pluripotent stem cell lines show stress defense mechanisms and mitochondrial regulation similar to those of human embryonic stem cells. Stem Cells, 28, 661-673.
72. Birket, M. J., Orr, A. L., Gerencser, A. A., Madden, D. T., Vitelli, C., et al. (2011). A reduction in ATP demand and mitochondrial activity with neural differentiation of human embryonic stem cells. Journal of Cell Science, 124, 348-358.
73. Tuppen, H. A., Hogan, V. E., He, L., Blakely, E. L., Worgan, L., et al. (2010). The p. M292T NDUFS2 mutation causes complex I-deficient Leigh syndrome in multiple families. Brain, 133, 2952-2963.
74. Munusamy, S., Saba, H., Mitchell, T., Megyesi, J. K., Brock, R. W., et al. (2009). Alteration of renal respiratory complex-III during experimental type-1 diabetes. BMC Endocrine Disorders, 9, 2.
75. Rossignol, R., Faustin, B., Rocher, C., Malgat, M., Mazat, J. P., et al. (2003). Mitochondrial threshold effects. Biochemical Journal, 370, 751-762.
76. Jeppesen, T. D., Schwartz, M., Olsen, D. B., & Vissing, J. (2003). Oxidative capacity correlates with muscle mutation load in mitochondrial myopathy. Annals of Neurology, 54, 86-92.
77. Trounce, I. (2000). Genetic control of oxidative phosphorylation and experimental models of defects. Human Reproduction, 15, 18-27.
78. Saladi, S. V., & de la Sema, I. L. (2010). ATP dependent chromatin remodeling enzymes in embryonic stem cells. Stem Cell Reviews, 6, 62-73.
79. Wallace, D. C., & Fan, W. (2010). Energetics, epigenetics, mitochondrial genetics. Mitochondrion, 10, 12-31.
80. Dawid, I. B. (1974). 5-methylcytidylic acid: absence from mitochondrial DNA of frogs and HeLa cells. Science, 184, 80-81.
81. Groot, G. S., & Kroon, A. M. (1979). Mitochondrial DNA from various organisms does not contain internally methylated cytosine in. Biochimica et Biophysica Acta, 564, 355-357.
82. Shock, L. S., Thakkar, P. V., Peterson, E. J., Moran, R. G., & Taylor, S. M. (2011). DNA methyltransferase 1, cytosine methylation, and cytosine hydroxymethylation in mammalian mitochondria. Proceedings of the National Academy of Sciences of the United States of America, 108, 3630-3635.
83. Oakes, C. C., La Salle, S., Smiraglia, D. J., Robaire, B., & Trasler, J. M. (2007). Developmental acquisition of genome-wide DNA methylation occurs prior to meiosis in male germ cells. Developmental Biology, 307, 368-379.