A Critical Review of the Inheritance of Mitochondrial DNA in Humans
DOI:
https://doi.org/10.47611/jsrhs.v12i4.5753Keywords:
Mitochondrial inheritance, Mitochondria, Maternal inheritance, Mitochondrial DNAAbstract
The dogma of mitochondrial inheritance states that mitochondrial DNA (mtDNA) is inherited solely down the maternal line. Traditionally, the elimination of paternal mtDNA happens through various mechanisms. Elimination mechanisms such as autophagy degradation or endonuclease G (EndoG) degradation have been widely studied in model organisms, while ubiquitin-mediated elimination has been identified in mammals and humans. Despite the existence of several research papers that support maternal inheritance, a controversial 2018 research paper by Luo et al. counters this longstanding dogma and proposes biparental inheritance of mtDNA. Since its publication, multiple studies have tried to justify this transmission through nuclear-mitochondrial DNA (NUMTs) or nuclear mtDNA concatemers (mega-NUMTs). It has been established that the phenomenon of biparental inheritance is not frequent since maternal inheritance entirely dominates over paternal transmission in the evolutionary timescale. This review explores the research linked with mitochondrial elimination and mitochondrial transmission, showing that further research is required to thoroughly understand this area of genetics.
Downloads
References or Bibliography
Balciuniene, J., & Balciunas, D. (2019). A nuclear mtDNA concatemer (Mega-NUMT) could mimic paternal inheritance of mitochondrial genome. Frontiers in Genetics, 10–2019. https://doi.org/10.3389/fgene.2019.00518
Carelli, V. (2015). Keeping in shape the dogma of mitochondrial DNA maternal inheritance. PLOS Genetics, 11(5). https://doi.org/10.1371/journal.pgen.1005179
Cihlar, J. C., Strobl, C., Lagacé, R., Muenzler, M., Parson, W., & Budowle, B. (2020). Distinguishing mitochondrial DNA and NUMT sequences amplified with the precision ID mtDNA whole genome panel. Mitochondrion, 55, 122–133. https://doi.org/10.1016/j.mito.2020.09.001
DeLuca, S. Z., & O’Farrell, P. H. (2012). Barriers to male transmission of mitochondrial DNA in sperm development. Developmental Cell, 22(3), 660–668. https://doi.org/10.1016/j.devcel.2011.12.021
Filosto, M., Mancuso, M., Vives-Bauza, C., Vilà, M. R., Shanske, S., Hirano, M., Andreu, A. L., & DiMauro, S. (2003). Lack of paternal inheritance of muscle mitochondrial DNA in sporadic mitochondrial myopathies. Annals of Neurology, 54(4), 524–526. https://doi.org/10.1002/ana.10709
Giles, R. E., Blanc, H., Cann, H. M., & Wallace, D. C. (1980). Maternal inheritance of human mitochondrial DNA. Proceedings of the National Academy of Sciences, 77(11), 6715–6719. https://doi.org/10.1073/pnas.77.11.6715
Gyllensten, U., Wharton, D., Josefsson, A., & Wilson, A. C. (1991). Paternal inheritance of mitochondrial DNA in mice. Nature, 352(6332), 255–257. https://doi.org/10.1038/352255a0
Hutchison, C. A., Newbold, J. E., Potter, S. S., & Edgell, M. H. (1974). Maternal inheritance of mammalian mitochondrial DNA. Nature, 251(5475), 536–538. https://doi.org/10.1038/251536a0
Kujoth, G. C., Hiona, A., Pugh, T. D., Someya, S., Panzer, K., Wohlgemuth, S. E., Hofer, T., Seo, A. Y., Sullivan, R., Jobling, W. A., Morrow, J. D., Van Remmen, H., Sedivy, J. M., Yamasoba, T., Tanokura, M., Weindruch, R., Leeuwenburgh, C., & Prolla, T. A. (2005). Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science, 309(5733), 481–484. https://doi.org/10.1126/science.1112125
Luo, S., Valencia, C. A., Zhang, J., Lee, N.-C., Slone, J., Gui, B., Wang, X., Li, Z., Dell, S., Brown, J., Chen, S. M., Chien, Y.-H., Hwu, W.-L., Fan, P.-C., Wong, L.-J., Atwal, P. S., & Huang, T. (2018). Biparental inheritance of mitochondrial DNA in humans. Proceedings of the National Academy of Sciences, 115(51), 13039–13044. https://doi.org/10.1073/pnas.1810946115
Luo, S., Valencia, C. A., Zhang, J., Lee, N.-C., Slone, J., Gui, B., Wang, X., Li, Z., Dell, S., Brown, J., Chen, S. M., Chien, Y.-H., Hwu, W.-L., Fan, P.-C., Wong, L.-J., Atwal, P. S., & Huang, T. (2019). Reply to Lutz-Bonengel et al.: Biparental mtdna transmission is unlikely to be the result of nuclear mitochondrial DNA segments. Proceedings of the National Academy of Sciences, 116(6), 1823–1824. https://doi.org/10.1073/pnas.1821357116
Lutz-Bonengel, S., & Parson, W. (2019). No further evidence for paternal leakage of mitochondrial DNA in humans yet. Proceedings of the National Academy of Sciences, 116(6), 1821–1822. https://doi.org/10.1073/pnas.1820533116
Pyle, A., Hudson, G., Wilson, I. J., Coxhead, J., Smertenko, T., Herbert, M., Santibanez-Koref, M., & Chinnery, P. F. (2015). Extreme-depth re-sequencing of mitochondrial DNA finds no evidence of paternal transmission in humans. PLOS Genetics, 11(5). https://doi.org/10.1371/journal.pgen.1005040
Rius, R., Cowley, M. J., Riley, L., Puttick, C., Thorburn, D. R., & Christodoulou, J. (2019). Biparental inheritance of mitochondrial DNA in humans is not a common phenomenon. Genetics in Medicine, 21(12), 2823–2826. https://doi.org/10.1038/s41436-019-0568-0
Sato, K., & Sato, M. (2017). Multiple ways to prevent transmission of paternal mitochondrial DNA for maternal inheritance in Animals. The Journal of Biochemistry, 162(4), 247–253. https://doi.org/10.1093/jb/mvx052
Sato, M., & Sato, K. (2011). Degradation of paternal mitochondria by fertilization-triggered autophagy in C. elegans embryos. Science, 334(6059), 1141–1144. https://doi.org/10.1126/science.1210333
Sato, M., & Sato, K. (2013). Maternal inheritance of mitochondrial DNA by diverse mechanisms to eliminate paternal mitochondrial DNA. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, 1833(8), 1979–1984. https://doi.org/10.1016/j.bbamcr.2013.03.010
Schwartz, M., & Vissing, J. (2002). Paternal inheritance of mitochondrial DNA. New England Journal of Medicine, 347(8), 576–580. https://doi.org/10.1056/nejmoa020350
Shokolenko, I., Venediktova, N., Bochkareva, A., Wilson, G. L., & Alexeyev, M. F. (2009). Oxidative stress induces degradation of mitochondrial DNA. Nucleic Acids Research, 37(8), 2539–2548. https://doi.org/10.1093/nar/gkp100
Song, W.-H., Yi, Y.-J., Sutovsky, M., Meyers, S., & Sutovsky, P. (2016). Autophagy and Ubiquitin–proteasome system contribute to sperm mitophagy after mammalian fertilization. Proceedings of the National Academy of Sciences, 113(36), 5261–5270. https://doi.org/10.1073/pnas.1605844113
Sutovsky, P., Moreno, R. D., Ramalho-Santos, J., Dominko, T., Simerly, C., & Schatten, G. (1999). Ubiquitin tag for sperm mitochondria. Nature, 402(6760), 371–372. https://doi.org/10.1038/46466
Sutovsky, P., Moreno, R. D., Ramalho-Santos, J., Dominko, T., Simerly, C., & Schatten, G. (2000). Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian Embryos. Biology of Reproduction, 63(2), 582–590. https://doi.org/10.1095/biolreprod63.2.582
Taanman, J.-W. (1999). The mitochondrial genome: Structure, transcription, translation and replication. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1410(2), 103–123. https://doi.org/10.1016/s0005-2728(98)00161-3
Thompson, W. E., Ramalho-Santos, J., & Sutovsky, P. (2003). Ubiquitination of Prohibitin in mammalian sperm mitochondria: Possible roles in the regulation of mitochondrial inheritance and sperm quality control. Biology of Reproduction, 69(1), 254–260. https://doi.org/10.1095/biolreprod.102.010975
Wei, W., Pagnamenta, A. T., Gleadall, N., Sanchis-Juan, A., Stephens, J., Broxholme, J., Tuna, S., Odhams, C. A., Fratter, C., Turro, E., Caulfield, M. J., Taylor, J. C., Rahman, S., & Chinnery, P. F. (2020). Nuclear-mitochondrial DNA segments resemble paternally inherited mitochondrial DNA in humans. Nature Communications, 11(1740). https://doi.org/10.1038/s41467-020-15336-3
Yan, C., Duanmu, X., Zeng, L., Liu, B., & Song, Z. (2019). Mitochondrial DNA: Distribution, mutations, and elimination. Cells, 8(4), 379. https://doi.org/10.3390/cells8040379
Zhou, Q., Li, H., Li, H., Nakagawa, A., Lin, J. L., Lee, E.-S., Harry, B. L., Skeen-Gaar, R. R., Suehiro, Y., William, D., Mitani, S., Yuan, H. S., Kang, B.-H., & Xue, D. (2016). Mitochondrial endonuclease G mediates breakdown of paternal mitochondria upon fertilization. Science, 353(6297), 394–399. https://doi.org/10.1126/science.aaf4777
Published
How to Cite
Issue
Section
Copyright (c) 2023 Zuzanna Malinowska
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
Copyright holder(s) granted JSR a perpetual, non-exclusive license to distriute & display this article.
