Mitochondrial Function and Male Infertility

  • Thomas Bourgeron
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 28)


During the recent years, alteration of mitochondrial function has been associated with an increasing numbers of phenotypes (Wallace 1992; Munnich et al. 1996). Although alteration of mtDNA is only rarely identified in patients, mtDNA has been claimed to be at the origin of aging (Wallace et al. 1995), several degenerative disorders (Wallace et al. 1995), and more recently male infertility (Cummins et al. 1994; St. Johns et al. 1997). Thus, some authors have suggested that some forms of infertility may be explained as premature aging of the testis (Cummins et al. 1994). Frank and Hurst (1996) have also hypothesized that a germ-line mutation of the mtDNA with severe effects on males but only mild effects on females might increase to a relatively high frequency because natural selection of mitochondria occurs only in females. Thus, the strictly maternal inheritance of mtDNA could create an important male-female asymmetry in the expected severity of mitochondrial disease. However, althrough in plants there is a direct role of mtDNA mutations in the phenotype of cytoplasmic male sterility (Hanson 1991), in mammals the evidence is not so convincing.


Sperm Motility Seminal Plasma Male Infertility Mitochondrial Disease Sperm Length 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Adham IM, Tessmann D, Soliman KA, Murphy D, Kremling H, Szpirer C, Engel W (1996) Cloning, expression and chromosomal localization of the rat mitochondrial capsule selenoprotein gene (MCS): the reading frame does not contain potential UGA selenocysteine codons. DNA Cell Biol 15: 159–166PubMedCrossRefGoogle Scholar
  2. Aitken J, Fisher H (1994) Reactive oxygen species generation and human spermatozoa: the balance of benefit and risk. BioEssays 16: 259–267Google Scholar
  3. Alcivar AA, Hake LE, Millette CF, Trasler JM, Hecht NB (1989) Mitochondrial gene expression in male germ cells of the mouse. Dev Biol 135: 263–271PubMedCrossRefGoogle Scholar
  4. Alexandre C, Bisson JP, David G (1978) Asthenospermie totale avec anomalie ultrastructurale du flagelle chez deux frères stériles. J Gynaecol Obstet Biol Reprod (Paris) 7: 31–38Google Scholar
  5. Allen JF (1996) Separate sexes and the mitochondrial theory of aging. J Theor Biol 180: 135–140PubMedCrossRefGoogle Scholar
  6. Ankel-Simons F, Cummins JM (1996) Misconceptions about mitochondria and mammalian fertilization: implications for theories on human evolution. Proc Natl Acad Sci USA 93: 13 859–13 863Google Scholar
  7. Armbrust EV, Ferris PJ, Goodenough UW (1993) A mating type-linked gene cluster expressed in Chlamydomonas zygotes participates in the uniparental inheritance of the chloroplast genome. Cell 74: 801–811PubMedCrossRefGoogle Scholar
  8. Bartoov B, Eltes F, Pansky M, Langzam J, Reichart M, Soffer Y (1994) Improved diagnosis of male fertility potential via a combination of quantitative ultramorphology and routine semen analyses. Hum Reprod 9: 2069–2075PubMedGoogle Scholar
  9. Bernadini G, Belgiojoso P, Canatini M (1988) Xenopus spermatozoon: is there any correlation between motility and oxygen consumption? Gamete Res 21: 403–408Google Scholar
  10. Bleau G, Lemarbre J, Faucher G, Roberts KD, Chapdelaine A (1984) Semen, selenium and human fertility. Fertil Steri142: 890–894Google Scholar
  11. Bourgeron T, Chretien D, Rötig A, Munnich A, Rustin P (1993) Fate and expression of the deleted mitochondrial DNA differ between heteroplasmic skin fibroblast and Epstein-Barr virus-transformed lymphocyte cultures. J Biol Chem 268:19 369–19 376Google Scholar
  12. Bourgeron T, Rustin P, Chretien D, Birch-Machin M, Bourgeois M, Viegas-Péquignot E, Munnich A, Rötig A (1995) A mutation in the flavoprotein subunit gene of the succinate dehydrogenase: the first nuclear gene mutation in mitochondrial respiratory chain deficiency. Nat Genet 11: 144–148PubMedCrossRefGoogle Scholar
  13. Brokaw CJ (1967) Adenosine triphosphate usage by flagella. Science 156: 76–78PubMedCrossRefGoogle Scholar
  14. Brokaw CJ, Benedict B (1968) Mechanochemical coupling in flagella. II. Effects of viscosity and thiourea on metabolism and motility of Ciona spermatozoa. J Gen Physiol 52: 283–299PubMedCrossRefGoogle Scholar
  15. Calvin HI, Cooper GW, Wallace E (1981) Evidence that selenium in rat sperm is associated with a cystein-rich structural protein of the mitochondrial capsule. Gamete Res 4: 139–149CrossRefGoogle Scholar
  16. Cardullo RA, Baltz JM (1991) Metabolic regulation in mammalian sperm: mitochondrial volume determines sperm length and flagellar beat frequency. Cell Motil Cytoskelet 19: 180–188CrossRefGoogle Scholar
  17. Cardullo RA, Cone RA (1986) Mechanical immobilization of rat sperm does not change their oxygen consumption rate. Biol Reprod 34: 820–830PubMedCrossRefGoogle Scholar
  18. Cataldo L, Baig K, Oko R, Mastrangelo M-A, Kleene KC (1996) Developmental expression, intracellular localization, and selenium content of the cysteine-rich protein associated with the mitochondrial capsules of mouse sperm. Mol Reprod Dev 45: 320–331PubMedCrossRefGoogle Scholar
  19. Chretien D, Gallego J, Barrientos A, Casademont J, Cardellach F, Munnich A, Rötig A, Rustin P (1998) The biochemical parameters for the diagnosis of respiratory chain deficiency in man and their lack of age-related changes. Biochem J 329: 249–254PubMedGoogle Scholar
  20. Comporti M (1989) Three models of free radical-induced cell injury. Chem Biol Interact 72: 1–56PubMedCrossRefGoogle Scholar
  21. Cummins JM, Jequier AM, Kan R (1994) Molecular biology of human male infertility: links with aging, mitochondrial genetics, and oxidative stress? Mol Reprod Dev 37: 345–362PubMedCrossRefGoogle Scholar
  22. de Lamirande E, Gagnon C (1992a) Reactive oxygen species and human spermatozoa. I. Effects on the motility of intact spermatozoa and on sperm axonemes. J Androl 13: 368–378Google Scholar
  23. de Lamirande E, Gagnon C (1992b) Reactive oxygen species and human spermatozoa. II. Depletion of adenosine triphosphate plays an important role in the inhibition of sperm motility. J Androl 13: 379–386Google Scholar
  24. De Martino C, Floridi A, Marcante ML, Malorni W, Scorza Barcellona P, Bellocci M, Silvestrini B (1979) Morphological, histochemical and biochemical studies on germ cell mitochondria of normal rats. Cell Tissue Res 196: 1–22PubMedCrossRefGoogle Scholar
  25. Folgero T, Bertheussen K, Lindal S, Torbergsen T, Dian P (1993) Mitochondrial disease and reduced sperm motility. Hum Reprod 8: 1863–1868PubMedGoogle Scholar
  26. Ford WCL, Harrison A (1981) The role of oxidative phosphorylation in the generation of ATP in human spermatozoa. J Reprod Fertil 63: 271–278PubMedCrossRefGoogle Scholar
  27. Fraga CG, Motchnik PA, Shigenaga MK, Helbock HJ, Jacob RA, Ames BN (1991) Ascorbic acid protects against endogenous oxidative DNA damage in human sperm. Proc Natl Acad Sci USA 88: 11003–11006PubMedCrossRefGoogle Scholar
  28. Frank SA, Hurst LD (1996) Mitochondrial and male disease. Nature 383: 224PubMedCrossRefGoogle Scholar
  29. Gallina FG, Gerez de Burgos NM, Burgos C, Coronel CE, Blanco A (1994) The lactate/pyruvate shuttle in Spermatozoa: operation in vitro. Arch Biochem Biophys 308: 515–519PubMedCrossRefGoogle Scholar
  30. Gopalkrishnan K, Padwal V, D’Souza S, Shah R (1995) Severe asthenozoospermia: a structural and functional study. Int J Androl 18: 67–74PubMedCrossRefGoogle Scholar
  31. Gottlieb C, Svanborg K, Bygdeman M (1991) Adenosine triphosphate ( ATP) in human spermatozoa. Andrologia 23: 421–425Google Scholar
  32. Gyllensten U, Wharton D, Josefsson A, Wilson AC (1991) Paternal inheritance of mitochondrial DNA in mice. Nature 352: 255–257PubMedCrossRefGoogle Scholar
  33. Halangk W, Bohnensack R, Kunz W (1985) Interdependence of mitochondrial ATP production and extramitochondrial ATP utilization in intact spermatozoa. Biochim Biophys Acta 808: 316–22PubMedCrossRefGoogle Scholar
  34. Halangk W, Dietz H, Bohnensack R, Kunz W (1987) Regulation of oxidative phosphorylation in mitochondria of epididymal bull spermatozoa. Biochim Biophys Acta 893: 100–108PubMedCrossRefGoogle Scholar
  35. Hammerstedt RH, Lardy HA (1983) The effect of substrate cycling on the ATP yield of sperm glycolysis. J Biol Chem 258: 8759–8768PubMedGoogle Scholar
  36. Hansen JC, Deguchi Y (1996) Selenium and fertility in animals and man–a review. Acta Vet Scand 37: 19–30PubMedGoogle Scholar
  37. Hanson MR (1991) Plant mitochondrial mutations and male sterility. Annu Rev Genet 25: 461–486PubMedCrossRefGoogle Scholar
  38. Hayashi JI, Ohta S, Kagawa Y, Kondo H, Kaneda H, Yonekawa H, Takai D, Miyabayashi S (1994) Nuclear but not mitochondrial genome involvement in human age-related mitochondrial dysfunction. J Biol Chem 269: 6878–6883PubMedGoogle Scholar
  39. Hecht NB, Liem H (1984) Mitochondrial DNA is synthesized during meiosis and spermiogenesis in the mouse. Exp Cell Res 154: 293–298PubMedCrossRefGoogle Scholar
  40. Houshmand M, Holme E, Hanson C, Wennerholm UB, Hamberger L (1997) Paternal mitochondrial DNA transferred to the offspring following intracytoplasmic sperm injection. J Assist Reprod Genet 14: 223–227PubMedCrossRefGoogle Scholar
  41. Hsu H-S, Wei Y-H, Li AF, Chen M-T, Chang LS (1986) Defective mitochondrial oxidative phosphorylation in varicocele-bearing testicles. Urology 46: 545–549CrossRefGoogle Scholar
  42. Huang CC, Chen RS, Chen CM, Wang HS, Lee CC, Pang CY, Hsu HS, Lee HC, Wei YH (1994) MELAS syndrome with mitochondrial tRNA Leu ( UUR) gene mutation in a chinese family. J Neurol Neurosurg Psychiatry 57: 586–589Google Scholar
  43. Hurt GS, Turner TT, Howard SS (1986) Repair of experimental varicocele in the rat: long-term effects on testicular blood flow and temperature and caudal epididymal sperm concentration and motility. J Androl 7: 271–276PubMedGoogle Scholar
  44. Huszar G, Vigue L, Corrales M (1990) Sperm creatine kinase activity in fertile and infertile oligospermic men. J Androl 11: 40–46PubMedGoogle Scholar
  45. Huszar G, Vigue L, Morshedi M (1992) Sperm creatine phosphokinase M-isoform ratios and fertilizing potential of men: a blinded study of 84 couples treated with in vitro fertilization. Fertil Steril 57: 882–888PubMedGoogle Scholar
  46. Jacobus WE, Lehninger AL (1973) Creatine kinase of rat heart mitochondria. J Biol Chem 248: 4803–4810PubMedGoogle Scholar
  47. Jones R, Mann T, Sherins R (1979) Peroxidative breakdown of phospholipids in human spermatozoa, spermicidal properties of fatty acid peroxides, and protective action of seminal plasma. Fertil Steril 31: 531–537PubMedGoogle Scholar
  48. Kaldis P, Stolz M, Wyss M, Zanolla E, Rothen-Rutishauser B, Vorherr T, Wallimann T (1996) Identification of two distinctly localized mitochondrial creatine kinase isoenzymes in spermatozoa. J Cell Sci 109: 2079–2088PubMedGoogle Scholar
  49. Kamp G, Büsselmann G, Lauterwein J (1996) Spermatozoa: models for studying regulatory aspects of energy metabolism. Experientia 52: 487–494PubMedCrossRefGoogle Scholar
  50. Kaneda H, Hayashi JI, Takahama S, Taya C, Lindahl KF, Yonekawa H (1995) Elimination of paternal mitochondrial DNA in intraspecific crosses during early mouse embryogenesis. Proc Natl Acad SCi USA 92: 4542–4546PubMedCrossRefGoogle Scholar
  51. Kao S-H, Chao H-T, Wei Y-H (1995) Mitochondrial deoxyribonucleic acid 4977-bp deletion is associated with diminished fertility and motility of human sperm. Biol Reprod 52: 729–736PubMedCrossRefGoogle Scholar
  52. Killian GJ, Gelerinter E, Chapman DA (1985) Alteration of oxygen uptake and the redox state of ubiquinone in rabbit sperm exposed to a variety of physiologic treatments. Biol Reprod 33: 859–869PubMedCrossRefGoogle Scholar
  53. Kleene KC (1989) Poly (A) shortening accompanies the activation of translation of five mRNAs during spermatogenesis in the mouse. Development 106: 367–373PubMedGoogle Scholar
  54. Kondo R, Satta Y, Matsuura ET, Ishiwa H, Takahata N, Chigusa SI (1990) Incomplete maternal transmission of mitochondrial DNA in Drosophila. Genetics 126: 657–63PubMedGoogle Scholar
  55. Larsson N-G, Garman JD, Oldorfs A, Barsh GS, Clayton DA (1996) A single mouse gene encodes the mitochondrial transcription factor A and a testis-specific nuclear HMG-box protein. Nat Genet 13: 296–302PubMedCrossRefGoogle Scholar
  56. Larsson N-G, Oldorfs A, Garman JD, Barsh GS, Clayton DA (1997) Down-regulation of mitochondrial transcription factor A during spermatogenesis in humans. Hum Mol Genet 6: 185–191PubMedCrossRefGoogle Scholar
  57. Luft R, Ikkos D, Palmieri G (1962) Severe hypermetabolism of non-thyroid origin with a defect in the maintenance of mitochondrial respiratory control: a correlated clinical, biochemical and morphological study. J Clin Invest 41: 1776–1804PubMedCrossRefGoogle Scholar
  58. McClure RD, Brawer J, Robaire B (1983) Ultrastructure of immotile spermatozoa in an infertile male: a spectrum of structural defects. Fertil Steril 40: 395–399PubMedGoogle Scholar
  59. McLeod J (1941) The metabolism of human spermatozoa. Am J Physiol 132: 193–201Google Scholar
  60. Mita M, Yasumasu I (1983) Metabolism of lipid and carbohydrate in sea urchin spermatozoa. Gamete Res 7: 133–144CrossRefGoogle Scholar
  61. Morshedi M (1990) Sperm ATP concentrations: the Norfolk experience. In: Acosta A, Swanson RJ, Ackerman SB et al. (eds) Human spermatozoa in assisted reproduction. Williams and Wilkins, Baltimore, pp 200–206Google Scholar
  62. Mundy AJ, Ryder TA, Edmonds DK (1995) Asthenozoospermia and the human sperm mid-piece. Hum Reprod 10: 116–119PubMedCrossRefGoogle Scholar
  63. Munnich A, Rötig A, Chretien D, Cormier V, Bourgeron T, Bonnefont JP, Saudubray JM, Rustin P (1996) Clinical presentation of mitochondrial disoders in chidhood. J Inherited Metab Dis 19: 521–527PubMedCrossRefGoogle Scholar
  64. Olds-Clarke P (1996) How does poor motility alter sperm fertilizing ability ? J Androl 17:183–186 Olson GE, Winfrey V (1990) Mitochondria-cytoskeleton interactions in the sperm midpiece. J Struct Biol 103: 13–22Google Scholar
  65. Olson GE, Winfrey V (1992) Structural organization of surface domains of sperm mitochondria. Mol Reprod Dev 33: 89–98PubMedCrossRefGoogle Scholar
  66. Otani H, Tanaka O, Kasai K-I, Yoshioka T (1988) Development of mitochondrial helical sheath in the middle piece of the mouse spermatid tail: Regular dispositions and synchronized changes. Anat Rec 222: 26–33Google Scholar
  67. Palermo G, Joris H, Devroey P, Van Steirteghem AC (1992) Pregnancies after intracytoplasmic sperm injection of a single spermatozoon into an oocyte. Lancet 340: 17PubMedCrossRefGoogle Scholar
  68. Pallini V, Baccetti B, Burrini AG (1979) A peculiar cysteine-rich polypeptide related to some unusual properties of mammalian sperm mitochondria. In: Fawcett DW, Bedfords JM (eds) The spermatozoon. Urban and Schwartzenberg, BaltimoreGoogle Scholar
  69. Pedersen H, Rebbe H, Hammen R (1971) Human sperm fine structure in a case of severe asthenospermia-necrospermia. Fertil Steril 22: 156–164PubMedGoogle Scholar
  70. Peterson RN, Freund M (1970) ATP synthesis and oxidative metabolism in human spermatozoa. Biol Reprod 3: 47–54PubMedGoogle Scholar
  71. Phillips DM (1977) Mitochondrial disposition in mammalian spermatozoa. J Ultrastruct Res 2: 144–154PubMedCrossRefGoogle Scholar
  72. Reynier P, Chrétien M-F, Penisson-Besnier I, Malthiéry Y, Rohmer V, Lestienne P (1997) Male infertility associated with multiple mitochondrial DNA rearrangements. C R Acad Sci 320: 629–636CrossRefGoogle Scholar
  73. Ross A, Christie S, Edmond P (1973) Ultrastructural tail defects in the spermatozoa from two men attending a subfertility clinic. J Reprod Fertil 32: 243–251PubMedCrossRefGoogle Scholar
  74. Rötig A, Cormier V, Blanche S, Bonnefont JP, Ledeist F, Romero N, Schmitz J, Rustin P, Fischer A, Saudubray JM, Munnich A (1990) Pearson’s marrow-pancreas syndrome. A multisystem mitochondrial disorder in infancy. J Clin Invest 86: 1601–1608Google Scholar
  75. Roveri A, Cassaco A, Maiorino M, Dalan P, Calligaro A, Ursini F (1992) Phospholipid hydroperoxide glutathione peroxidase of rat testis: gonadotropin dependence and immunocytochemical identification. J Biol Chem 267: 6142–6146PubMedGoogle Scholar
  76. Rustin P, Bourgeron T, Parfait B, Chretien D, Munnich A, Rotig A (1997) Inborn errors of the Krebs cycle: a group of unusual mitochondrial diseases in humans. Biochim Biophys Acta 1361: 185–197PubMedCrossRefGoogle Scholar
  77. Saypol DC, Howards SS, Turner TT, Miller ED Jr (1981) Influence of surgically induced varicocele on testicular blood flow, temperature, and histology in adult rats and dogs. J Clin Invest 68: 39–45PubMedCrossRefGoogle Scholar
  78. Schoff PK, Cheetham J, Lardy HA (1989) Adenylate kinase activity in ejaculated bovine sperm flagella. J Biol Chem 264: 6086–6091PubMedGoogle Scholar
  79. Selley ML, Lacey MJ, Bartlett MR, Copeland CM, Ardlie NG (1991) Content of significant amounts of a cytotoxic end-product of lipid peroxidation in human semen. J Reprod Fertil 92: 291–298PubMedCrossRefGoogle Scholar
  80. Shadel GS, Clayton DA (1997) Mitochondrial DNA maintenance in vertebrates. Annu Rev Biochem 66: 409–435PubMedCrossRefGoogle Scholar
  81. Shih DM, Kleene KC (1992) A study by in situ hybridization of the stage of appearance and disappearance of the transition protein 2 and mitochondrial capsule seleno-protein mRNA during spermatogenesis in the mouse. Mol Reprod Dev 33: 222–227PubMedCrossRefGoogle Scholar
  82. Shoubridge EA, Karpati G, Hastings KE (1990) Deletion mutants are functionally dominant over wild-type mitochondrial genomes in skeletal muscle fiber segments in mitochondrial disease. Cell 62: 43–49PubMedCrossRefGoogle Scholar
  83. Steeghs K, Oerlemans F, Wieringa B (1995) Mice deficient in ubiquitous mitochondrial creatine kinase are viable and fertile. Biochim Biophys Acta 1230: 130–138PubMedCrossRefGoogle Scholar
  84. St Johns JC, Cooke ID, Barratt CLR (1997) Mitochondrial mutations and male infertility. Nat Med 3: 124–125Google Scholar
  85. Suomalainen A, Kaukonen J Amati P, Timonen R, Haltia M, Weissenbach J, Zeviani M, Somer H, Peltonen (1995) An autosomal locus predisposing to deletions of mitochondrial DNA. Nat Genet 9: 146–151Google Scholar
  86. Sutovsky P, Navara CS, Shatten G (1996) Fate of sperm mitochondria, and the incorporation, conversion, and disassembly of the sperm tail structures during bovine fertilization. Biol Reprod 55: 1195–1205PubMedCrossRefGoogle Scholar
  87. Takahashi J, Higashi Y, La Nasa JA, Yoshida K-I, Winters SJ, Oshima H, Troen P (1983) Studies of the human testis. XVIII. Simultaneous measurement of nine intratesticular steroids: evidence for reduced mitochondrial function in testes of elderly men. J Endocrinol Metab 56: 1178–1187CrossRefGoogle Scholar
  88. Thyagarajan B, Padua RA, Campbell C (1996) Mammalian mitochondria pocess homologous DNA recombination activity. J Biol Chem 271: 27536–27543PubMedCrossRefGoogle Scholar
  89. Tombes RM, Shapiro BM (1985) Metabolite channeling: a phosphorylcreatine shuttle to mediate high energy phosphate transport between sperm mitochondrion and tail. Cell 41: 325–334PubMedCrossRefGoogle Scholar
  90. Tosic J, Walton A (1950) Metabolism of spermatozoa and its effect on motility and survival. Biochem J 47: 199–212PubMedGoogle Scholar
  91. Tyler DD (1992) The mitochondrion in health and disease 1st edn VCH Publishers, New YorkGoogle Scholar
  92. Vigue C, Vigue L, Huszar G (1992) Adenosine triphosphate (ATP) concentrations and ATP/adenosine diphosphate ratios in human sperm of normospermic, oligospermic, and asthenospermic specimens and in their swim-up fractions: lack of correlation between ATP parameters and sperm creatine kinase concentrations. J Androl 13: 305–311PubMedGoogle Scholar
  93. Wallace DC (1986) Mitotic segregation of mitochondrial DNAs in human cell hybrids and expression of chloramphenicol resistance. Somatic Cell Mol Genet 12: 41–49CrossRefGoogle Scholar
  94. Wallace DC (1992) Diseases of the mitochondrial DNA. Annu Rev Biochem 61:1175–1212 Wallace DC, Shoffner JM, Trounce I, Brown MD, Ballinger SW, Corral-Debrinski M, Horton T, Jun AS, Lott MT (1995) Mitochondrial DNA mutations in human degenerative diseases and aging. Biochim Biophys Acta 1271: 141–151Google Scholar
  95. Wallace E, Cooper GW, Calvin HI (1983) Effects of selenium deficiency on the shape and arrangement of rodent sperm mitochondria. Gamete Res 4: 389–399CrossRefGoogle Scholar
  96. Wallimann T, Hemmer W (1994) Creatine kinase in non-muscle tissues and cells. Mol Cell Biochem 133 /134: 193–220PubMedCrossRefGoogle Scholar
  97. Wilton LJ, Temple-Smith PD, de Kretser DM (1992) Quantitative ultrastructural analysis of sperm tails reveals flagellar defects associated with persistent asthenozoospermia. Hum Reprod 7: 510–516PubMedGoogle Scholar
  98. Wu SH, Olfield JE, Shull LR, Cheeke PR (1979) Specific effect of selenium deficiency on rat sperm. Biol Reprod 20, 793–798PubMedCrossRefGoogle Scholar
  99. Zinni A, de Lamirande E, Gragnon C (1993) Reactive oxygen species in semen of infertile patients: levels of superoxide dismutase and catalase-like activities in seminal plasma and spermatozoa. Int J Androl 16: 183–188CrossRefGoogle Scholar
  100. Zouros E. Oberhauser Ball A. Saavedra C. Freeman KR (1994) An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. Proc Natl Acad Sci USA 91: 7463–7467CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2000

Authors and Affiliations

  • Thomas Bourgeron
    • 1
  1. 1.Laboratoire d’Immunogénétique Humaine, INSERM U276Institut PasteurParis Cedex 15France

Personalised recommendations