Skip to main content
Log in

Spermatozoa: models for studying regulatory aspects of energy metabolism

  • Multi-Author Reviews
  • Published:
Experientia Aims and scope Submit manuscript

Abstract

Spermatozoa are highly specialized cells, and they offer advantages for studying several basic aspects of metabolic control such as the role of adenosine triphosphate-(ATP)-homeostasis for cell function, the mechanisms of fatigue and metabolic depression, the metabolic channelling through the cytoplasm and the organization and regulation of glycolytic enzymes. Spermatozoa of four species with different reproductive modes are, introduced and the first results are presented: Spermatozoa of the marine wormArenicola marina are well adapted to external fertilization in sea water with fluctuating oxygen tension: they are motile for several hours in oxygen-free sea water, even when the ATP level is dramatically reduced. Anaerobic ATP production occurs by alanine, acetate and propionate fermentation probably by the same pathways known from somatic cells of this species. Under aerobic conditions the phosphagen system might function like a shuttle for energy-rich phosphate from mitochondria to the dynein-ATPases. Storage of turkey and carp spermatozoa for several hours without exogenous substrates and oxygen results in the degradation of phosphocreatine and ATP to inorganic phosphate and adenosine monophosphate (AMP), respectively. Despite low energy charges, stored spermatozoa of both species are capable of progressive movements. In carp spermatozoa fatigue of motility is not accompanied by the dramatic acidosis one discusses as an important effect in muscle fatigue. Energy metabolism of boar spermatozoa is typically based on glycolysis consuming extracellular carbohydrates and producing lactate and protons. The sperm seem to tolerate low intracellular pH (<6.5). The lack of a phosphagen system (no energy shuttle from mitochondria to the distal dynein-ATPases) is probably compensated by a high glycolytic ATP-production in the mitochondria-free piece of the flagellum.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Ahluwalia, B. C., and Graham, E. F., Free amino acids in the semen of the fowl and turkey. J. Reprod. Fert.12 (1966) 365–368.

    Google Scholar 

  2. Anderson, W. A., and Personne, P., The localization of glycogen in the spermatozoa of various invertebrate and vertebrate species. J. Cell Biol.44 (1970) 29–51.

    Article  PubMed  Google Scholar 

  3. Arrata, W. S. M., Burt, T., and Corder, S., The role of phosphate esters in male fertility. Fert. Steril.30 (1978) 329–333.

    Google Scholar 

  4. Baccetti, B., Pallini, V., and Burrini, A. G., Localization and catalytic properties of lactate dehydrogenase in different sperm models. Expl Cell Res.90 (1975) 183–190.

    Article  Google Scholar 

  5. Baccetti, B., Evolution of the sperm cell, in: Biology of Fertilization, vol. 2 pp. 3–58. Eds. C. B. Metz and A. Monroy. Academic Press, London 1985.

    Google Scholar 

  6. Billard, R., and Cosson, M.-P., The energetics of fish sperm motility. in: Controls of Sperm Motility: Biological and Clinical Aspects, pp. 153–173. Ed. C. Gagnon. CRC Press, Boca Raton (USA) 1990.

    Google Scholar 

  7. Billard, R., Cosson, J., Perchec, G., and Linhart, O., Biology of sperm and artificial reproduction in carp. Aquaculture129 (1995) 95–112.

    Article  Google Scholar 

  8. Brillard, J. P., Sperm storage and transport following natural mating and artificial insemination. Poult. Sci.72 (1993) 923–928.

    PubMed  Google Scholar 

  9. Brooks, D. E., Examination of bull semen and of the bull and rabbit testis for the presence of creatine phosphate and arginine phosphate. J. Reprod. Fert.26 (1971) 275–278.

    Google Scholar 

  10. Brown, G. C., Control of respiration and ATP synthesis in mammalian mitochondria and cells. Biochem. J.284 (1992) 1–13.

    PubMed  Google Scholar 

  11. Burt, C. T., and Chalovich, J. M., Serine ethanolamine phosphodiester: a major component in chicken semen. Biochim. biophys. Acta529 (1978) 186–188.

    PubMed  Google Scholar 

  12. Büsselmann, G., Kamp, G., and Lauterwein, J.,31P-NMR studies on turkey semen. Abstract XVIth ICMRBS Intern. Conference of Magnetic Resonance in Biological Systems, p. 63. Veldhoven (1994).

  13. Cain, D. F., and Davies, R. E., Breakdown of adenosine triphosphate during a single contraction of working muscle. Biochem. biophys. Res. Comm.8 (1962) 361–366.

    Article  PubMed  Google Scholar 

  14. Christen, R., Schackmann, R. W., Dahlquist, F. W., and Shapiro, B. M.,31P-NMR analysis of sea urchin sperm activation. Expl Cell Res.149 (1983) 289–294.

    Article  Google Scholar 

  15. Christen, R., Gatti, J.-L., and Billard, R., Trout sperm motility. Eur. J. Biochem.166 (1987) 667–671.

    Article  PubMed  Google Scholar 

  16. Duncan, A., The spawning ofArenicola marina (L.) in the British Isles. Proc. zool. Soc. Lond.134 (1960) 37–156.

    Google Scholar 

  17. Elsing, A., Untersuchungen zum Energiestoffwechsel von Spermazellen des marinen AnnelidenArenicola marina. Diploma thesis, University of Münster 1994.

  18. Fioroni, P., Allgemeine und vergleichende Embryologie der Tiere. Springer, Berlin 1987.

    Google Scholar 

  19. Fitts, R. H., Cellular mechanisms of muscle fatigue. Physiol. Rev.74 (1994) 49–94.

    PubMed  Google Scholar 

  20. Gallina, F. G., Gerez de Burgos, N. M., Burgos, C., Coronel, C. E., and Blanco, A., The lactate/pyruvate shuttle in Spermatozoa: Operation in vitro. Archs Biochem. Biophys.308 (1994) 515–519.

    Article  Google Scholar 

  21. Gellerich, F. N., Kapischke, M., Kunz, W., Neumann, W., Kuznetsov, A., Brdiczka, D., and Nicolay, K., The influence of the cytosolic oncotic pressure on the permeability of the mitochondrial outer membrane for ADP: implications for the kinetic properties of mitochondrial creatine kinase and for ADP channelling into the intermembrane space. Molec. cell. Biochem.133/134 (1994) 85–104.

    Article  Google Scholar 

  22. Gibbons, B. H., and Gibbons, I. R., Flagellar movement and adenosine triphosphatase activity in sea urchin sperm extracted with triton X-100. J. Cell Biol.54 (1972) 75–97.

    Article  PubMed  Google Scholar 

  23. Howarth, B., and Palmer, M. B., An examination, of the need for sperm capacitation in the turkey. J. Reprod. Fertil.28 (1972) 443–445.

    PubMed  Google Scholar 

  24. Ishida, Y., Riesinger, I., Wallimann, T., and Paul, R. J., Compartmentation of ATP synthesis and utilization in smooth muscle: role of arobic glycolysis and creatine kinase. Molec. cell. Biochem.133/134 (1994) 39–50.

    Article  Google Scholar 

  25. Jamieson, B. G. M., and Rouse, G. W., The spermatozoa of the Polychaeta (Annelida): an ultrastructural review. Biol. Rev.64 (1989) 93–157.

    PubMed  Google Scholar 

  26. Jamieson, B. G. M., Fish Evolution and Systematics: Evidence from Spermatozoa, p. 141. Cambridge University Press. Cambridge 1991.

    Google Scholar 

  27. Kamp, G., and Juretschke, H. P., Hypercapnic and hypocapnic hypoxia in the lugwormArenicola marina: a31P-NMR study. J. expl Zool.252 (1989) 219–227.

    Article  Google Scholar 

  28. Kamp, G., and Lauterwein, J., Multinuclear magnetic resonance studies of boar seminal plasma. Biochim. biophys. Acta1243 (1995) 101–109.

    PubMed  Google Scholar 

  29. Kamp, G., Englisch, H., Müller, R., Westhoff, D., and Elsing, A., Comparison of two different phosphagen systems in the lugwormArenicola marina. J. comp. Physiol.165 (1995) 496–505.

    Google Scholar 

  30. Krasznai, Z., Marian, T., Balkay, L., Gaspar, R., and Tron, L., Potassium channels regulate hypo-osmotic shock-induced motility of common carp (Cyprinus carpio) sperm. Aquaculture129 (1995) 123–128.

    Article  Google Scholar 

  31. Lake, P. E., Male genital organs. in: Form and Function in Birds, Vol. 2, pp. 1–61. Eds. A. S. King and J. McLelland. Academic Press, London 1981.

    Google Scholar 

  32. Lamming, G. E. (Ed.), Marshall's Physiology of Reproduction, 4th edition, vol. 2. Churchill Livingstone, Edinburgh 1990.

    Google Scholar 

  33. Lipmann, F., Metabolic generation and utilization of phosphate bond energy. Adv. Enzymol.1 (1941) 99–162.

    Google Scholar 

  34. Lohmann, K., Über die Pyrophosphatfraktion im Muskel. Naturwiss.31 (1929) 624–625.

    Google Scholar 

  35. Lynch, M. J., Masters, J., Pryor, J. P., Lindon, J. C., Spraul, M., Foxall, P. J. D., and Nicholson, J. K., Ultra high field NMR spectroscopic studies on human seminal fluid, seminal vesicle and prostatic secretions. J. Pharm. Biomed. Anal.12 (1994) 5–19.

    Article  PubMed  Google Scholar 

  36. Mann, Th., Metabolism of semen. Adv. Enzymol.9 (1949) 329–390.

    Google Scholar 

  37. Mann, Th., and Lutwak-Mann, C. (Eds.), Male Reproductive Function and Semen. Springer, Berlin 1981.

    Google Scholar 

  38. Mita, M., and Yasumasu, I., Metabolism of lipid and carbohydrate in sea urchin spermatozoa. Gamete Res.7 (1983) 133–144.

    Article  Google Scholar 

  39. Mita, M., Diacyl choline phosphoglyceride — the endogenous substrate for energy metabolism in Sea Urchin spermatozoa. Zool. Sci.9 (1992) 563–568.

    Google Scholar 

  40. Okuno, M., and Brokaw, C. J., Inhibition of movement of triton-demembranated sea-urchin sperm flagella by Mg2+, ATP4−, ADP and Pi. J. Cell Sci.38 (1979) 105–123.

    PubMed  Google Scholar 

  41. Oppenheimer, J. R., Mouthbreeding fishes. Anim. Behav.18 (1970) 493–503.

    Article  PubMed  Google Scholar 

  42. Overstreet, J. W., and Katz, D. F., Interaction between the female reproductive tract and spermatozoa, in: Controls of Sperm Motility: Biological and Clinical Aspects, pp. 63–75. Ed. C. Gagnon. CRC Press, Boca Raton (USA) 1990.

    Google Scholar 

  43. Perchec, G., Jeulin, C., Cosson, J., Andre, F., and Billard, R., Relationship between sperm ATP content and motility of carp spermatozoa. J. Cell Sci.108 (1995) 747–753.

    PubMed  Google Scholar 

  44. Robitaille, P. A., Robitaille, P.-M. L., and Brown, G. G.,31P-NMR studies ofLimulus polyphemus: spermatozoa at rest and after motility. J. expl Zool.238 (1986) 89–98.

    Article  Google Scholar 

  45. Robitaille, P.-M. L., Robitaille, P. A., Martin, P. A., and Brown, G. G., Phosphorus-31 nuclear magnetic resonance studies of spermatozoa from the boar, ram, goat and bull. Comp. Biochem. Physiol.87B (1987) 285–296.

    Google Scholar 

  46. Robitaille, P.-M. L., Mumford, K. G., and Brown, G. G.,31P-NMR nuclear magnetic resonance study of trout spermatozoa at rest, after motility, and during short-term storage. Biochem. Cell Biol.65 (1987) 474–485.

    Google Scholar 

  47. Strong, S. J., and Ellington, W. R., Horseshoe crab sperm contain a unique isoform of arginine kinase that is present in midpiece and flagellum. J. expl Zool.267 (1993) 563–571.

    Google Scholar 

  48. Taggart, D. A., A comparison of sperm and embryo transport in the female reproductive tract of marsupial and eutherian mammals. Repord. Fert. Dev.6 (1994) 451–472.

    Google Scholar 

  49. Thoai, R. M., and Robin, Y., Guanidine compounds and phosphagens. in: Chemical Zoology, pp. 163–203. Eds. M. Florkin and B. T. Scheer. Academic Press, New York 1979.

    Google Scholar 

  50. Tombes, R. M., and Shapiro, B. M., Metabolite channeling: a phosphorylcreatine shuttle to mediate high energy phosphate transport between sperm mitochondrion and tail. Cell41 (1985) 325–334.

    Article  PubMed  Google Scholar 

  51. Tombes, R. M., and Shapiro, B. M., Energy transport and cell polarity: relationship of phosphagen kinase activity to sperm function. J. expl Zool.251 (1989) 82–90.

    Article  Google Scholar 

  52. Thompson, L. V., and Fitts, R. H., Muscle fatigue in the frog semitendinosus: role of high-energy phosphates and Pi. Am. J. Physiol.263 (1992) C803-C809.

    PubMed  Google Scholar 

  53. Wallimann, Th., Moser, H., Zurbriggen, B., Wegmann, G., and Eppenberger, H. M., Creatine kinase isoenzymes in spermatozoa. J. Muscle Res. Cell Motil.7 (1986) 25–34.

    Article  PubMed  Google Scholar 

  54. Wallimann, Th., and Hemmer, W., Creatine kinase in non-muscle tissues and cells. Molec. Cell Biochem.133/134 (1994) 193–220.

    Article  Google Scholar 

  55. Westhoff, D., Bohne, W., and Kamp, G., Unusual binding of a glycolytic enzyme to structures of mammalian spermatozoa. in: Proceedings of the German Zoological Society 87th Meeting in Jena. Fischer. Stuttgart 1994.

    Google Scholar 

  56. Wilkie, D. R., Muscular fatigue: effects of hydrogen ions and inorganic phosphate. Federation Proc.45 (1986) 2921–2923.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kamp, G., Büsselmann, G. & Lauterwein, J. Spermatozoa: models for studying regulatory aspects of energy metabolism. Experientia 52, 487–494 (1996). https://doi.org/10.1007/BF01919321

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01919321

Key words

Navigation