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Volume 40 Issue 11
Nov.  2013
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Article Navigation >  Journal of Genetics and Genomics  > 2013  >  40(11): 549-556

Sperm Mitochondria in Reproduction: Good or Bad and Where Do They Go?

doi: 10.1016/j.jgg.2013.08.004
  • a 

    Key Laboratory of Animal Reproduction and Germplasm Enhancement in Universities of Shandong, Qingdao Agricultural University, Qingdao 266109, China

  • b 

    Department of Veterinary Pathobiology, University of Missouri, Columbia, MO 65211, USA

  • c 

    State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China

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  • Corresponding author: E-mail address: sunqy@ioz.ac.cn (Qing-Yuan Sun)
  • Received Date: 2013-07-18
  • Accepted Date: 2013-08-27
  • Rev Recd Date: 2013-08-12
    • Available Online: 2013-09-18
  • Publish Date: 2013-11-20
    Abstract
  • The mitochondrion is the major energy provider to power sperm motility. In mammals, aside from the nuclear genome, mitochondrial DNA (mtDNA) also contributes to oxidative phosphorylation to impact production of ATP by coding 13 polypeptides. However, the role of sperm mitochondria in fertilization and its final fate after fertilization are still controversial. The viewpoints that sperm bearing more mtDNA will have a better fertilizing capability and that sperm mtDNA is actively eliminated during early embryogenesis are widely accepted. However, this may be not true for several mammalian species, including mice and humans. Here, we review the sperm mitochondria and their mtDNA in sperm functions, and the mechanisms of maternal mitochondrial inheritance in mammals.
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  • [1]
    Aitken, R.J., Jones, K.T., Robertson, S.A. Reactive oxygen species and sperm function – in sickness and in health J. Androl., 33 (2012),pp. 1096-1106
    [2]
    Al Rawi, S., Louvet-Vallee, S., Djeddi, A. et al. Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission Science, 334 (2011),pp. 1144-1147
    [3]
    Amaral, A., Ramalho-Santos, J. Assessment of mitochondrial potential: implications for the correct monitoring of human sperm function Int. J. Androl., 33 (2010),pp. e180-e186
    [4]
    Amaral, A., Ramalho-Santos, J., St John, J.C. The expression of polymerase gamma and mitochondrial transcription factor A and the regulation of mitochondrial DNA content in mature human sperm Hum. Reprod., 22 (2007),pp. 1585-1596
    [5]
    Ankel-Simons, F., Cummins, J.M. Misconceptions about mitochondria and mammalian fertilization: implications for theories on human evolution Proc. Natl. Acad. Sci. USA, 93 (1996),pp. 13859-13863
    [6]
    Bai, U., Seidman, M.D. A specific mitochondrial DNA deletion (mtDNA4977) is identified in a pedigree of a family with hearing loss Hear. Res., 154 (2001),pp. 73-80
    [7]
    Basse, C.W. Mitochondrial inheritance in fungi Curr. Opin. Microbiol., 13 (2010),pp. 712-719
    [8]
    Bunch, D.O., Welch, J.E., Magyar, P.L. et al. Glyceraldehyde 3-phosphate dehydrogenase-S protein distribution during mouse spermatogenesis Biol. Reprod., 58 (1998),pp. 834-841
    [9]
    Carra, E., Sangiorgi, D., Gattuccio, F. et al. Male infertility and mitochondrial DNA Biochem. Biophys. Res. Commun., 322 (2004),pp. 333-339
    [10]
    Chen, H., Chan, D.C. Emerging functions of mammalian mitochondrial fusion and fission Hum. Mol. Genet., 14 (2005),pp. R283-R289
    [11]
    DeLuca, S.Z., O'Farrell, P.H. Barriers to male transmission of mitochondrial DNA in sperm development Dev. Cell, 22 (2012),pp. 660-668
    [12]
    Diez-Sanchez, C., Ruiz-Pesini, E., Lapena, A.C. et al. Mitochondrial DNA content of human spermatozoa Biol. Reprod., 68 (2003),pp. 180-185
    [13]
    Dimauro, S., Davidzon, G. Mitochondrial DNA and disease Ann. Med., 37 (2005),pp. 222-232
    [14]
    Donnelly, E.T., O'Connell, M., McClure, N. et al. Differences in nuclear DNA fragmentation and mitochondrial integrity of semen and prepared human spermatozoa Hum. Reprod., 15 (2000),pp. 1552-1561
    [15]
    Ferramosca, A., Focarelli, R., Piomboni, P. et al. Oxygen uptake by mitochondria in demembranated human spermatozoa: a reliable tool for the evaluation of sperm respiratory efficiency Int. J. Androl., 31 (2008),pp. 337-345
    [16]
    Folgero, T., Bertheussen, K., Lindal, S. et al. Mitochondrial disease and reduced sperm motility Hum. Reprod., 8 (1993),pp. 1863-1868
    [17]
    Ford, W.C. Regulation of sperm function by reactive oxygen species Hum. Reprod. Update, 10 (2004),pp. 387-399
    [18]
    Gerez de Burgos, N.M., Gallina, F., Burgos, C. et al. Effect of L-malate on pyruvate dehydrogenase activity of spermatozoa Arch. Biochem. Biophys., 308 (1994),pp. 520-524
    [19]
    Gyllensten, U., Wharton, D., Josefsson, A. et al. Paternal inheritance of mitochondrial DNA in mice Nature, 352 (1991),pp. 255-257
    [20]
    Holyoake, A.J., McHugh, P., Wu, M. et al. High incidence of single nucleotide substitutions in the mitochondrial genome is associated with poor semen parameters in men Int. J. Androl., 24 (2001),pp. 175-182
    [21]
    Huszar, G., Stone, K., Dix, D. et al. Putative creatine kinase M-isoform in human sperm is identified as the 70-kilodalton heat shock protein HspA2 Biol. Reprod., 63 (2000),pp. 925-932
    [22]
    , Newbold, J.E., Potter, S.S., Edgell, M.H. Maternal inheritance of mammalian mitochondrial DNA Nature, 251 (1974),pp. 536-538
    [23]
    Huttemann, M., Jaradat, S., Grossman, L.I. Mol. Reprod. Dev., 66 (2003),pp. 8-16
    [24]
    Ieremiadou, F., Rodakis, G.C. Correlation of the 4977 bp mitochondrial DNA deletion with human sperm dysfunction BMC Res. Notes, 2 (2009),p. 18
    [25]
    John, J.S., John, B.
    [26]
    Kaneda, H., Hayashi, J., Takahama, S. et al. Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis Proc. Natl. Acad. Sci. USA, 92 (1995),pp. 4542-4546
    [27]
    Kao, S., Chao, H.T., Wei, Y.H. Mitochondrial deoxyribonucleic acid 4977-bp deletion is associated with diminished fertility and motility of human sperm Biol. Reprod., 52 (1995),pp. 729-736
    [28]
    Kao, S.H., Chao, H.T., Liu, H.W. et al. Sperm mitochondrial DNA depletion in men with asthenospermia Fertil. Steril., 82 (2004),pp. 66-73
    [29]
    Kao, S.H., Chao, H.T., Wei, Y.H. Multiple deletions of mitochondrial DNA are associated with the decline of motility and fertility of human spermatozoa Mol. Hum. Reprod., 4 (1998),pp. 657-666
    [30]
    Lestienne, P., Reynier, P., Chretien, M.F. et al. Oligoasthenospermia associated with multiple mitochondrial DNA rearrangements Mol. Hum. Reprod., 3 (1997),pp. 811-814
    [31]
    Lewis, S.E. Is sperm evaluation useful in predicting human fertility? Reproduction, 134 (2007),pp. 31-40
    [32]
    Liesa, M., Palacin, M., Zorzano, A. Mitochondrial dynamics in mammalian health and disease Physiol. Rev., 89 (2009),pp. 799-845
    [33]
    Logan, D.C. The mitochondrial compartment J. Exp. Bot., 58 (2007),pp. 1225-1243
    [34]
    Lorenc, A., Bryk, J., Golik, P. et al. Homoplasmic MELAS A3243G mtDNA mutation in a colon cancer sample Mitochondrion, 3 (2003),pp. 119-124
    [35]
    Luo, S.M., Ge, Z.J., Wang, Z.W. et al. Unique insights into maternal mitochondrial inheritance in mice Proc. Natl. Acad. Sci. USA, 110 (2013),pp. 13038-13043
    [36]
    Marchetti, C., Obert, G., Deffosez, A. et al. Study of mitochondrial membrane potential, reactive oxygen species, DNA fragmentation and cell viability by flow cytometry in human sperm Hum. Reprod., 17 (2002),pp. 1257-1265
    [37]
    May-Panloup, P., Chretien, M.F., Savagner, F. et al. Increased sperm mitochondrial DNA content in male infertility Hum. Reprod., 18 (2003),pp. 550-556
    [38]
    Mayr, J.A., Meierhofer, D., Zimmermann, F. et al. Loss of complex I due to mitochondrial DNA mutations in renal oncocytoma Clin. Cancer Res., 14 (2008),pp. 2270-2275
    [39]
    MITOMAP
    [40]
    Mohri, I., Taniike, M., Fujimura, H. et al. A case of Kearns–Sayre syndrome showing a constant proportion of deleted mitochondrial DNA in blood cells during 6 years of follow-up J. Neurol. Sci., 158 (1998),pp. 106-109
    [41]
    Mossman, J.A., Slate, J., Birkhead, T.R. et al. Mitochondrial haplotype does not influence sperm motility in a UK population of men Hum. Reprod., 27 (2012),pp. 641-651
    [42]
    Nishimura, Y., Yoshinari, T., Naruse, K. et al. Active digestion of sperm mitochondrial DNA in single living sperm revealed by optical tweezers Proc. Natl. Acad. Sci. USA, 103 (2006),pp. 1382-1387
    [43]
    O'Connell, M., McClure, N., Powell, L.A. et al. Differences in mitochondrial and nuclear DNA status of high-density and low-density sperm fractions after density centrifugation preparation Fertil. Steril., 79 (2003),pp. 754-762
    [44]
    Otani, H., Tanaka, O., Kasai, K. et al. Development of mitochondrial helical sheath in the middle piece of the mouse spermatid tail: regular dispositions and synchronized changes Anat. Rec., 222 (1988),pp. 26-33
    [45]
    Palanichamy, M.G., Zhang, Y.P. Identifying potential pitfalls in interpreting mitochondrial DNA mutations of male infertility cases Indian J. Med. Res., 134 (2011),pp. 447-451
    [46]
    Paoli, D., Gallo, M., Rizzo, F. et al. Mitochondrial membrane potential profile and its correlation with increasing sperm motility Fertil. Steril., 95 (2011),pp. 2315-2319
    [47]
    Park, C.B., Larsson, N.G. Mitochondrial DNA mutations in disease and aging J. Cell Biol., 193 (2011),pp. 809-818
    [48]
    Pereira, L., Goncalves, J., Bandelt, H.J. Fertil. Steril., 89 (2008),pp. 738-741
    [49]
    Pereira, L., Goncalves, J., Franco-Duarte, R. et al. No evidence for an mtDNA role in sperm motility: data from complete sequencing of asthenozoospermic males Mol. Biol. Evol., 24 (2007),pp. 868-874
    [50]
    Peterson, R.N., Freund, M. ATP synthesis and oxidative metabolism in human spermatozoa Biol. Reprod., 3 (1970),pp. 47-54
    [51]
    Pickworth, S., Change, M.C. J. Reprod. Fertil., 19 (1969),pp. 371-374
    [52]
    Piomboni, P., Focarelli, R., Stendardi, A. et al. The role of mitochondria in energy production for human sperm motility Int. J. Androl., 35 (2012),pp. 109-124
    [53]
    Piotrowska-Nitsche, K., Perea-Gomez, A., Haraguchi, S. et al. Four-cell stage mouse blastomeres have different developmental properties Development, 132 (2005),pp. 479-490
    [54]
    Quinn, P., Kerin, J.F., Warnes, G.M. Improved pregnancy rate in human in vitro fertilization with the use of a medium based on the composition of human tubal fluid Fertil. Steril., 44 (1985),pp. 493-498
    [55]
    Rao, M., Li, L., Demello, C. et al. Mitochondrial DNA injury and mortality in hemodialysis patients J. Am. Soc. Nephrol., 20 (2009),pp. 189-196
    [56]
    Rawe, V.Y., Olmedo, S.B., Benmusa, A. et al. Sperm ubiquitination in patients with dysplasia of the fibrous sheath Hum. Reprod., 17 (2002),pp. 2119-2127
    [57]
    Reynier, P., May-Panloup, P., Chretien, M.F. et al. Mitochondrial DNA content affects the fertilizability of human oocytes Mol. Hum. Reprod., 7 (2001),pp. 425-429
    [58]
    Rokas, A., Ladoukakis, E., Zouros, E. Animal mitochondrial DNA recombination revisited Trends Ecol. Evol., 18 (2003),pp. 411-417
    [59]
    Sato, M., Sato, K. Science, 334 (2011),pp. 1141-1144
    [60]
    Sato, M., Sato, K. Maternal inheritance of mitochondrial DNA by diverse mechanisms to eliminate paternal mitochondrial DNA Biochim. Biophys. Acta, 1833 (2013),pp. 1979-1984
    [61]
    Schwartz, M., Vissing, J. Paternal inheritance of mitochondrial DNA N. Engl. J. Med., 347 (2002),pp. 576-580
    [62]
    Selvi Rani, D., Vanniarajan, A., Gupta, N.J. et al. Fertil. Steril., 86 (2006),pp. 1783-1785
    [63]
    Sharpley, M.S., Marciniak, C., Eckel-Mahan, K. et al. Heteroplasmy of mouse mtDNA is genetically unstable and results in altered behavior and cognition Cell, 151 (2012),pp. 333-343
    [64]
    Shitara, H., Hayashi, J.I., Takahama, S. et al. Maternal inheritance of mouse mtDNA in interspecific hybrids: segregation of the leaked paternal mtDNA followed by the prevention of subsequent paternal leakage Genetics, 148 (1998),pp. 851-857
    [65]
    Smith, L.C., Alcivar, A.A. Cytoplasmic inheritance and its effects on development and performance J. Reprod. Fertil., 48 (1993),pp. 31-43
    [66]
    Song, G.J., Lewis, V. Mitochondrial DNA integrity and copy number in sperm from infertile men Fertil. Steril., 90 (2008),pp. 2238-2244
    [67]
    Sousa, A.P., Amaral, A., Baptista, M. et al. Not all sperm are equal: functional mitochondria characterize a subpopulation of human sperm with better fertilization potential PLoS ONE, 6 (2011),p. e18112
    [68]
    Spiropoulos, J., Turnbull, D.M., Chinnery, P.F. Can mitochondrial DNA mutations cause sperm dysfunction? Mol. Hum. Reprod., 8 (2002),pp. 719-721
    [69]
    St John, J., Sakkas, D., Dimitriadi, K. et al. Failure of elimination of paternal mitochondrial DNA in abnormal embryos Lancet, 355 (2000),p. 200
    [70]
    St John, J.C., Facucho-Oliveira, J., Jiang, Y. et al. Mitochondrial DNA transmission, replication and inheritance: a journey from the gamete through the embryo and into offspring and embryonic stem cells Hum. Reprod. Update, 16 (2010),pp. 488-509
    [71]
    St John, J.C., Jokhi, R.P., Barratt, C.L. Men with oligoasthenoteratozoospermia harbour higher numbers of multiple mitochondrial DNA deletions in their spermatozoa, but individual deletions are not indicative of overall aetiology Mol. Hum. Reprod., 7 (2001),pp. 103-111
    [72]
    St John, J.C., Jokhi, R.P., Barratt, C.L. The impact of mitochondrial genetics on male infertility Int. J. Androl., 28 (2005),pp. 65-73
    [73]
    Steuerwald, N., Barritt, J.A., Adler, R. et al. Quantification of mtDNA in single oocytes, polar bodies and subcellular components by real-time rapid cycle fluorescence monitored PCR Zygote, 8 (2000),pp. 209-215
    [74]
    Suen, D.F., Norris, K.L., Youle, R.J. Mitochondrial dynamics and apoptosis Genes. Dev., 22 (2008),pp. 1577-1590
    [75]
    Sutovsky, P. Ubiquitin-dependent proteolysis in mammalian spermatogenesis, fertilization, and sperm quality control: killing three birds with one stone Microsc. Res. Tech., 61 (2003),pp. 88-102
    [76]
    Sutovsky, P., Moreno, R.D., Ramalho-Santos, J. et al. Ubiquitin tag for sperm mitochondria Nature, 402 (1999),pp. 371-372
    [77]
    Sutovsky, P., Moreno, R.D., Ramalho-Santos, J. et al. Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos Biol. Reprod., 63 (2000),pp. 582-590
    [78]
    Sutovsky, P., Navara, C.S., Schatten, G. Fate of the sperm mitochondria, and the incorporation, conversion, and disassembly of the sperm tail structures during bovine fertilization Biol. Reprod., 55 (1996),pp. 1195-1205
    [79]
    Sutovsky, P., Tengowski, M.W., Navara, C.S. et al. Mitochondrial sheath movement and detachment in mammalian, but not nonmammalian, sperm induced by disulfide bond reduction Mol. Reprod. Dev., 47 (1997),pp. 79-86
    [80]
    Tait, S.W., Green, D.R. Mitochondria and cell signalling J. Cell Sci., 125 (2012),pp. 807-815
    [81]
    Tarkowski, A.K., Ozdzenski, W., Czolowska, R. How many blastomeres of the 4-cell embryo contribute cells to the mouse body? Int. J. Dev. Biol., 45 (2001),pp. 811-816
    [82]
    Thangaraj, K., Joshi, M.B., Reddy, A.G. et al. Sperm mitochondrial mutations as a cause of low sperm motility J. Androl., 24 (2003),pp. 388-392
    [83]
    Thompson, W.E., Ramalho-Santos, J., Sutovsky, P. Ubiquitination of prohibitin in mammalian sperm mitochondria: possible roles in the regulation of mitochondrial inheritance and sperm quality control Biol. Reprod., 69 (2003),pp. 254-260
    [84]
    Vemuganti, S.A., Bell, T.A., Scarlett, C.O. et al. Three male germline-specific aldolase A isozymes are generated by alternative splicing and retrotransposition Dev. Biol., 309 (2007),pp. 18-31
    [85]
    Wai, T., Ao, A., Zhang, X. et al. The role of mitochondrial DNA copy number in mammalian fertility Biol. Reprod., 83 (2010),pp. 52-62
    [86]
    Wang, H., Chen, X.X., Wang, L.R. et al. AF-2364 is a prospective spermicide candidate Asian J. Androl., 12 (2010),pp. 322-335
    [87]
    White, D.J., Mital, D., Taylor, S. et al. Sperm mitochondrial DNA deletions as a consequence of long term highly active antiretroviral therapy Aids, 15 (2001),pp. 1061-1062
    [88]
    Wilton, L.J., Temple-Smith, P.D., de Kretser, D.M. Quantitative ultrastructural analysis of sperm tails reveals flagellar defects associated with persistent asthenozoospermia Hum. Reprod., 7 (1992),pp. 510-516
    [89]
    Yakes, F.M., Van Houten, B. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress Proc. Natl. Acad. Sci. USA, 94 (1997),pp. 514-519
    [90]
    Yan, H., Yan, Z., Ma, Q. et al. Association between mitochondrial DNA haplotype compatibility and increased efficiency of bovine intersubspecies cloning J. Genet. Genomics, 38 (2011),pp. 21-28
    [91]
    Yanagimachi, R., Kamiguchi, Y., Sugawara, S. et al. Gametes and fertilization in the Chinese hamster Gamete Res., 8 (1983),pp. 97-117
    [92]
    Yang, M., Ge, Y., Wu, J. et al. Coevolution study of mitochondria respiratory chain proteins: toward the understanding of protein–protein interaction J. Genet. Genomics, 38 (2011),pp. 201-207
    [93]
    Zhou, Q., Li, H., Xue, D. Cell Res., 21 (2011),pp. 1662-1669
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