Sperm mitochondria in reproduction: Good or bad and where do they go?

Journal of Genetics and Genomics

Volumn 40, Issue 11, 2013, Pages 549-556

  Luo, Shi Ming ^a   Schatten, Heide ^b   Sun, Qing Yuan ^a,c  

^a QINGDAO AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF MISSOURI   (United States)

^c INSTITUTE OF ZOOLOGY   (China)

Author keywords

Autophagy; Maternal inheritance; Mitochondrial DNA; Oxidative phosphorylation; Paternal inheritance; Ubiquitination

Indexed keywords

MITOCHONDRIAL DNA; SUPEROXIDE;

CELL DIFFERENTIATION; COPY NUMBER VARIATION; ENERGY YIELD; EXTRACHROMOSOMAL INHERITANCE; FERTILIZATION; GENE DELETION; GENE INSERTION; GENE REARRANGEMENT; GLYCOLYSIS; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; POINT MUTATION; REPRODUCTION; REVIEW; SPERM; SPERMATOGENESIS; SPERMATOZOON MOTILITY; ZYGOTE; ANIMAL; AUTOPHAGY; GENETICS; MALE; METABOLISM; PHYSIOLOGY; SPERMATOZOON;

MAMMALIA; MUS;

ANIMALS; AUTOPHAGY; DNA, MITOCHONDRIAL; HUMANS; MALE; MITOCHONDRIA; OXIDATIVE PHOSPHORYLATION; REPRODUCTION; SPERMATOZOA;

EID: 84887610850     PISSN: 16738527     EISSN: 18735533     Source Type: Journal    
DOI: 10.1016/j.jgg.2013.08.004     Document Type: Review

References (93)

1. Aitken R.J., Jones K.T., Robertson S.A. Reactive oxygen species and sperm function - in sickness and in health. J. Androl. 2012, 33:1096-1106.
2. Al Rawi S., Louvet-Vallee S., Djeddi A., Sachse M., Culetto E., Hajjar C., Boyd L., Legouis R., Galy V. Postfertilization autophagy of sperm organelles prevents paternal mitochondrial DNA transmission. Science 2011, 334:1144-1147.
3. Amaral A., Ramalho-Santos J. Assessment of mitochondrial potential: implications for the correct monitoring of human sperm function. Int. J. Androl. 2010, 33: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. 2007, 22:1585-1596.
5. Ankel-Simons F., Cummins J.M. Misconceptions about mitochondria and mammalian fertilization: implications for theories on human evolution. Proc. Natl. Acad. Sci. USA 1996, 93:13859-13863.
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. 2001, 154:73-80.
7. Basse C.W. Mitochondrial inheritance in fungi. Curr. Opin. Microbiol. 2010, 13:712-719.
8. Bunch D.O., Welch J.E., Magyar P.L., Eddy E.M., O'Brien D.A. Glyceraldehyde 3-phosphate dehydrogenase-S protein distribution during mouse spermatogenesis. Biol. Reprod. 1998, 58:834-841.
9. Carra E., Sangiorgi D., Gattuccio F., Rinaldi A.M. Male infertility and mitochondrial DNA. Biochem. Biophys. Res. Commun. 2004, 322:333-339.
10. Chen H., Chan D.C. Emerging functions of mammalian mitochondrial fusion and fission. Hum. Mol. Genet. 2005, 14(Suppl. 2):R283-R289.
11. DeLuca S.Z., O'Farrell P.H. Barriers to male transmission of mitochondrial DNA in sperm development. Dev. Cell 2012, 22:660-668.
12. Diez-Sanchez C., Ruiz-Pesini E., Lapena A.C., Montoya J., Perez-Martos A., Enriquez J.A., Lopez-Perez M.J. Mitochondrial DNA content of human spermatozoa. Biol. Reprod. 2003, 68:180-185.
13. Dimauro S., Davidzon G. Mitochondrial DNA and disease. Ann. Med. 2005, 37:222-232.
14. Donnelly E.T., O'Connell M., McClure N., Lewis S.E. Differences in nuclear DNA fragmentation and mitochondrial integrity of semen and prepared human spermatozoa. Hum. Reprod. 2000, 15:1552-1561.
15. Ferramosca A., Focarelli R., Piomboni P., Coppola L., Zara V. Oxygen uptake by mitochondria in demembranated human spermatozoa: a reliable tool for the evaluation of sperm respiratory efficiency. Int. J. Androl. 2008, 31:337-345.
16. Folgero T., Bertheussen K., Lindal S., Torbergsen T., Oian P. Mitochondrial disease and reduced sperm motility. Hum. Reprod. 1993, 8:1863-1868.
17. Ford W.C. Regulation of sperm function by reactive oxygen species. Hum. Reprod. Update 2004, 10:387-399.
18. Gerez de Burgos N.M., Gallina F., Burgos C., Blanco A. Effect of L-malate on pyruvate dehydrogenase activity of spermatozoa. Arch. Biochem. Biophys. 1994, 308:520-524.
19. Gyllensten U., Wharton D., Josefsson A., Wilson A.C. Paternal inheritance of mitochondrial DNA in mice. Nature 1991, 352:255-257.
20. Holyoake A.J., McHugh P., Wu M., O'Carroll S., Benny P., Sin I.L., Sin F.Y. High incidence of single nucleotide substitutions in the mitochondrial genome is associated with poor semen parameters in men. Int. J. Androl. 2001, 24:175-182.
21. Huszar G., Stone K., Dix D., Vigue L. Putative creatine kinase M-isoform in human sperm is identified as the 70-kilodalton heat shock protein HspA2. Biol. Reprod. 2000, 63:925-932.
22. Hutchison C.A., Newbold J.E., Potter S.S., Edgell M.H. Maternal inheritance of mammalian mitochondrial DNA. Nature 1974, 251:536-538.
23. Huttemann M., Jaradat S., Grossman L.I. Cytochrome c oxidase of mammals contains a testes-specific isoform of subunit VIb - the counterpart to testes-specific cytochrome c?. Mol. Reprod. Dev. 2003, 66:8-16.
24. Ieremiadou F., Rodakis G.C. Correlation of the 4977bp mitochondrial DNA deletion with human sperm dysfunction. BMC Res. Notes 2009, 2:18.
25. John J.S., John B. Sperm mitochondrial DNA. Sperm Chromatin 2011, 81-94. Springer, New York. A. Zini, A. Agarwal (Eds.).
26. Kaneda H., Hayashi J., Takahama S., Taya C., Lindahl K.F., Yonekawa H. Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. Proc. Natl. Acad. Sci. USA 1995, 92:4542-4546.
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. 1995, 52:729-736.
28. Kao S.H., Chao H.T., Liu H.W., Liao T.L., Wei Y.H. Sperm mitochondrial DNA depletion in men with asthenospermia. Fertil. Steril. 2004, 82:66-73.
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. 1998, 4:657-666.
30. Lestienne P., Reynier P., Chretien M.F., Penisson-Besnier I., Malthiery Y., Rohmer V. Oligoasthenospermia associated with multiple mitochondrial DNA rearrangements. Mol. Hum. Reprod. 1997, 3:811-814.
31. Lewis S.E. Is sperm evaluation useful in predicting human fertility?. Reproduction 2007, 134:31-40.
32. Liesa M., Palacin M., Zorzano A. Mitochondrial dynamics in mammalian health and disease. Physiol. Rev. 2009, 89:799-845.
33. Logan D.C. The mitochondrial compartment. J. Exp. Bot. 2007, 58:1225-1243.
34. Lorenc A., Bryk J., Golik P., Kupryjanczyk J., Ostrowski J., Pronicki M., Semczuk A., Szolkowska M., Bartnik E. Homoplasmic MELAS A3243G mtDNA mutation in a colon cancer sample. Mitochondrion 2003, 3:119-124.
35. Luo S.M., Ge Z.J., Wang Z.W., Jiang Z.Z., Wang Z.B., Ouyang Y.C., Hou Y., Schatten H., Sun Q.Y. Unique insights into maternal mitochondrial inheritance in mice. Proc. Natl. Acad. Sci. USA 2013, 110:13038-13043.
36. Marchetti C., Obert G., Deffosez A., Formstecher P., Marchetti P. Study of mitochondrial membrane potential, reactive oxygen species, DNA fragmentation and cell viability by flow cytometry in human sperm. Hum. Reprod. 2002, 17:1257-1265.
37. May-Panloup P., Chretien M.F., Savagner F., Vasseur C., Jean M., Malthiery Y., Reynier P. Increased sperm mitochondrial DNA content in male infertility. Hum. Reprod. 2003, 18:550-556.
38. Mayr J.A., Meierhofer D., Zimmermann F., Feichtinger R., Kogler C., Ratschek M., Schmeller N., Sperl W., Kofler B. Loss of complex I due to mitochondrial DNA mutations in renal oncocytoma. Clin. Cancer Res. 2008, 14:2270-2275.
39. MITOMAP MITOMAP: A Human Mitochondrial Genome Database 2013, http://www.mitomap.org.
40. Mohri I., Taniike M., Fujimura H., Matsuoka T., Inui K., Nagai T., Okada S. 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. 1998, 158:106-109.
41. Mossman J.A., Slate J., Birkhead T.R., Moore H.D., Pacey A.A. Mitochondrial haplotype does not influence sperm motility in a UK population of men. Hum. Reprod. 2012, 27:641-651.
42. Nishimura Y., Yoshinari T., Naruse K., Yamada T., Sumi K., Mitani H., Higashiyama T., Kuroiwa T. Active digestion of sperm mitochondrial DNA in single living sperm revealed by optical tweezers. Proc. Natl. Acad. Sci. USA 2006, 103:1382-1387.
43. O'Connell M., McClure N., Powell L.A., Steele E.K., Lewis S.E. Differences in mitochondrial and nuclear DNA status of high-density and low-density sperm fractions after density centrifugation preparation. Fertil. Steril. 2003, 79(Suppl. 1):754-762.
44. Otani H., Tanaka O., Kasai K., Yoshioka T. Development of mitochondrial helical sheath in the middle piece of the mouse spermatid tail: regular dispositions and synchronized changes. Anat. Rec. 1988, 222:26-33.
45. Palanichamy M.G., Zhang Y.P. Identifying potential pitfalls in interpreting mitochondrial DNA mutations of male infertility cases. Indian J. Med. Res. 2011, 134:447-451.
46. Paoli D., Gallo M., Rizzo F., Baldi E., Francavilla S., Lenzi A., Lombardo F., Gandini L. Mitochondrial membrane potential profile and its correlation with increasing sperm motility. Fertil. Steril. 2011, 95:2315-2319.
47. Park C.B., Larsson N.G. Mitochondrial DNA mutations in disease and aging. J. Cell Biol. 2011, 193:809-818.
48. Pereira L., Goncalves J., Bandelt H.J. Mutation C11994T in the mitochondrial ND4 gene is not a cause of low sperm motility in Portugal. Fertil. Steril. 2008, 89:738-741.
49. Pereira L., Goncalves J., Franco-Duarte R., Silva J., Rocha T., Arnold C., Richards M., Macaulay V. No evidence for an mtDNA role in sperm motility: data from complete sequencing of asthenozoospermic males. Mol. Biol. Evol. 2007, 24:868-874.
50. Peterson R.N., Freund M. ATP synthesis and oxidative metabolism in human spermatozoa. Biol. Reprod. 1970, 3:47-54.
51. Pickworth S., Change M.C. Fertilization of Chinese hamster eggs invitro. J. Reprod. Fertil. 1969, 19:371-374.
52. Piomboni P., Focarelli R., Stendardi A., Ferramosca A., Zara V. The role of mitochondria in energy production for human sperm motility. Int. J. Androl. 2012, 35:109-124.
53. 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.
54. Quinn P., Kerin J.F., Warnes G.M. Improved pregnancy rate in human invitro fertilization with the use of a medium based on the composition of human tubal fluid. Fertil. Steril. 1985, 44:493-498.
55. Rao M., Li L., Demello C., Guo D., Jaber B.L., Pereira B.J., Balakrishnan V.S. Mitochondrial DNA injury and mortality in hemodialysis patients. J. Am. Soc. Nephrol. 2009, 20:189-196.
56. Rawe V.Y., Olmedo S.B., Benmusa A., Shiigi S.M., Chemes H.E., Sutovsky P. Sperm ubiquitination in patients with dysplasia of the fibrous sheath. Hum. Reprod. 2002, 17:2119-2127.
57. Reynier P., May-Panloup P., Chretien M.F., Morgan C.J., Jean M., Savagner F., Barriere P., Malthiery Y. Mitochondrial DNA content affects the fertilizability of human oocytes. Mol. Hum. Reprod. 2001, 7:425-429.
58. Rokas A., Ladoukakis E., Zouros E. Animal mitochondrial DNA recombination revisited. Trends Ecol. Evol. 2003, 18:411-417.
59. Sato M., Sato K. Degradation of paternal mitochondria by fertilization-triggered autophagy in C. elegans embryos. Science 2011, 334:1141-1144.
60. Sato M., Sato K. Maternal inheritance of mitochondrial DNA by diverse mechanisms to eliminate paternal mitochondrial DNA. Biochim. Biophys. Acta 2013, 1833:1979-1984.
61. Schwartz M., Vissing J. Paternal inheritance of mitochondrial DNA. N. Engl. J. Med. 2002, 347:576-580.
62. Selvi Rani D., Vanniarajan A., Gupta N.J., Chakravarty B., Singh L., Thangaraj K. A novel missense mutation C11994T in the mitochondrial ND4 gene as a cause of low sperm motility in the Indian subcontinent. Fertil. Steril. 2006, 86:1783-1785.
63. Sharpley M.S., Marciniak C., Eckel-Mahan K., McManus M., Crimi M., Waymire K., Lin C.S., Masubuchi S., Friend N., Koike M., Chalkia D., MacGregor G., Sassone-Corsi P., Wallace D.C. Heteroplasmy of mouse mtDNA is genetically unstable and results in altered behavior and cognition. Cell 2012, 151:333-343.
64. Shitara H., Hayashi J.I., Takahama S., Kaneda H., Yonekawa H. Maternal inheritance of mouse mtDNA in interspecific hybrids: segregation of the leaked paternal mtDNA followed by the prevention of subsequent paternal leakage. Genetics 1998, 148:851-857.
65. Smith L.C., Alcivar A.A. Cytoplasmic inheritance and its effects on development and performance. J. Reprod. Fertil. 1993, 48(Suppl.):31-43.
66. Song G.J., Lewis V. Mitochondrial DNA integrity and copy number in sperm from infertile men. Fertil. Steril. 2008, 90:2238-2244.
67. Sousa A.P., Amaral A., Baptista M., Tavares R., Caballero Campo P., Caballero Peregrin P., Freitas A., Paiva A., Almeida-Santos T., Ramalho-Santos J. Not all sperm are equal: functional mitochondria characterize a subpopulation of human sperm with better fertilization potential. PLoS ONE 2011, 6:e18112.
68. Spiropoulos J., Turnbull D.M., Chinnery P.F. Can mitochondrial DNA mutations cause sperm dysfunction?. Mol. Hum. Reprod. 2002, 8:719-721.
69. St John J., Sakkas D., Dimitriadi K., Barnes A., Maclin V., Ramey J., Barratt C., De Jonge C. Failure of elimination of paternal mitochondrial DNA in abnormal embryos. Lancet 2000, 355:200.
70. St John J.C., Facucho-Oliveira J., Jiang Y., Kelly R., Salah R. Mitochondrial DNA transmission, replication and inheritance: a journey from the gamete through the embryo and into offspring and embryonic stem cells. Hum. Reprod. Update 2010, 16:488-509.
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. 2001, 7:103-111.
72. St John J.C., Jokhi R.P., Barratt C.L. The impact of mitochondrial genetics on male infertility. Int. J. Androl. 2005, 28:65-73.
73. Steuerwald N., Barritt J.A., Adler R., Malter H., Schimmel T., Cohen J., Brenner C.A. Quantification of mtDNA in single oocytes, polar bodies and subcellular components by real-time rapid cycle fluorescence monitored PCR. Zygote 2000, 8:209-215.
74. Suen D.F., Norris K.L., Youle R.J. Mitochondrial dynamics and apoptosis. Genes. Dev. 2008, 22:1577-1590.
75. Sutovsky P. Ubiquitin-dependent proteolysis in mammalian spermatogenesis, fertilization, and sperm quality control: killing three birds with one stone. Microsc. Res. Tech. 2003, 61:88-102.
76. Sutovsky P., Moreno R.D., Ramalho-Santos J., Dominko T., Simerly C., Schatten G. Ubiquitin tag for sperm mitochondria. Nature 1999, 402:371-372.
77. Sutovsky P., Moreno R.D., Ramalho-Santos J., Dominko T., Simerly C., Schatten G. Ubiquitinated sperm mitochondria, selective proteolysis, and the regulation of mitochondrial inheritance in mammalian embryos. Biol. Reprod. 2000, 63:582-590.
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. 1996, 55:1195-1205.
79. Sutovsky P., Tengowski M.W., Navara C.S., Zoran S.S., Schatten G. Mitochondrial sheath movement and detachment in mammalian, but not nonmammalian, sperm induced by disulfide bond reduction. Mol. Reprod. Dev. 1997, 47:79-86.
80. Tait S.W., Green D.R. Mitochondria and cell signalling. J. Cell Sci. 2012, 125:807-815.
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. 2001, 45:811-816.
82. Thangaraj K., Joshi M.B., Reddy A.G., Rasalkar A.A., Singh L. Sperm mitochondrial mutations as a cause of low sperm motility. J. Androl. 2003, 24:388-392.
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. 2003, 69:254-260.
84. Vemuganti S.A., Bell T.A., Scarlett C.O., Parker C.E., de Villena F.P., O'Brien D.A. Three male germline-specific aldolase A isozymes are generated by alternative splicing and retrotransposition. Dev. Biol. 2007, 309:18-31.
85. Wai T., Ao A., Zhang X., Cyr D., Dufort D., Shoubridge E.A. The role of mitochondrial DNA copy number in mammalian fertility. Biol. Reprod. 2010, 83:52-62.
86. Wang H., Chen X.X., Wang L.R., Mao Y.D., Zhou Z.M., Sha J.H. AF-2364 is a prospective spermicide candidate. Asian J. Androl. 2010, 12:322-335.
87. White D.J., Mital D., Taylor S., St John J.C. Sperm mitochondrial DNA deletions as a consequence of long term highly active antiretroviral therapy. Aids 2001, 15:1061-1062.
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. 1992, 7:510-516.
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 1997, 94:514-519.
90. Yan H., Yan Z., Ma Q., Jiao F., Huang S., Zeng F., Zeng Y. Association between mitochondrial DNA haplotype compatibility and increased efficiency of bovine intersubspecies cloning. J. Genet. Genomics 2011, 38:21-28.
91. Yanagimachi R., Kamiguchi Y., Sugawara S., Mikamo K. Gametes and fertilization in the Chinese hamster. Gamete Res. 1983, 8:97-117.
92. Yang M., Ge Y., Wu J., Xiao J., Yu J. Coevolution study of mitochondria respiratory chain proteins: toward the understanding of protein-protein interaction. J. Genet. Genomics 2011, 38:201-207.
93. Zhou Q., Li H., Xue D. Elimination of paternal mitochondria through the lysosomal degradation pathway in C. elegans. Cell Res. 2011, 21:1662-1669.