Sperm mitochondrial function in men with normozoospermia and asthenozoospermia


Authors: M. Čedíková 1,2;  M. Miklíková 1;  M. Grundmanová 3;  N. H. Zech 4;  M. Králíčková 1,2,5;  J. Kuncová 2,3
Authors‘ workplace: Ústav histologie a embryologie LF UK, Plzeň, přednostka doc. MUDr. M. Králíčková, Ph. D. 1;  Biomedicínské centrum LF UK, Plzeň, vědecký ředitel doc. MUDr. M. Štengl, Ph. D. 2;  Ústav fyziologie LF UK, Plzeň, přednosta doc. MUDr. M. Štengl, Ph. D. 3;  Institut reprodukční medicíny a endokrinologie, IVF Centrum Prof. Zecha, Plzeň, přednosta Univ. Doz. Dr. med. Nicolas H. Zech 4;  Gynekologicko-porodnická klinika LF UK a FN, Plzeň, přednosta doc. MUDr. Z. Novotný, CSc. 5
Published in: Ceska Gynekol 2014; 79(1): 22-28

Overview

Objective:
One of causes of male infertility is reduced sperm motility. It turns out that the reduced efficiency of the mitochondrial respiratory activity may play a role in the development of this disorder. The aim of our study was to comprehensively determine mitochondrial respiratory activity of sperm with normal and reduced motility.

Design:
Prospective study.

Setting:
Department of Histology and Embryology, Faculty of Medicine in Pilsen, Charles University in Prague; Department of Physiology, Faculty of Medicine in Pilsen, Charles University in Prague; Institute of Reproductive Medicine and Endocrinology, IVF Centers Prof. Zech, Plzeň.

Methods:
Ejaculates of 14 men were obtained from IVF Center Prof. Zech, Pilsen. According to the World Health Organization classification, samples were divided into normozoospermatic (n = 7) and asthenozoospermatic(n = 7) groups. Respiratory activity of sperm was measured on two-chamber oxygraph Oroboros.

Results:
In asthenozoospermatic samples, significantly reduced activity of complex I (p = 0.007) and increased respiration after application of ATP-synthase inhibitor oligomycin (showing increased uncoupled oxidation and phosphorylation, p = 0.046) were found. Inhibition of complex I by rotenone showed that complex I contribution to the total capacity of oxidative phosphorylation of healthy sperm was relatively lower than it is typical for somatic cells.

Conclusion:
In our study, we measured mitochondrial respiratory activity of human sperm, permeabilized by digitonin, by high-resolution oxygraphy, which allows the determination of oxygen consumption from the smallest possible number of germ cells. The study results confirm reduced activity of complex I in asthenozoospermatics and suggest that increased leakage of protons from the mitochondrial matrix, which leads to reduced efficiency of phosphorylating process, could participate in the reduced sperm motility.

Better characterization of male germ cells, either completely healthy or with affected motility, will help us to understand better the physiological process of fertilization and also to choose the most viable sperm for infertility treatment by methods of assisted reproduction.

Keywords:
infertility – sperm – respirometry


Sources

1. Aitken, RJ., Ryan, AL., Baker, MA., et al. Redox activity associated with the maturation and capacitation of mammalian spermatozoa. Free Radic Biol Med, 2004, 36, 8, p. 994–1010.

2. Ankel-Simons, F., Cummins, JM. Misconceptions about mitochondria and mammalian fertilization: implications for theories on human evolution. Proc Natl Acad Sci U S A, 1996, 93, 24, p. 13859–13863.

3. Blum, AE., Walsh, BC., Dubyak, GR. Extracellular osmolarity modulates G protein-coupled receptor-dependent ATP release from 1321N1 astrocytoma cells. Am J Physiol Cell Physiol, 2010, 298, 2, p. 386–396.

4. El-Mir, MY., Nogueira, V., Fontaine, E., et al. Dimethylbiguanide inhibits cell respiration via an indirect effect targeted on the respiratory chain complex I. J Biol Chem, 2000, 7, 275, 1, p. 223–228.

5. Escalier, D. Knockout mouse models of sperm flagellum anomalies. Hum Reprod Update, 2006, 12, 4, p. 449–461.

6. Evenson, DP., Darzynkiewicz, Z., Melamed, MR. Simultaneous measurement by flow cytometry of sperm cell viability and mitochondrial membrane potential related to cell motility. J Histochem Cytochem, 1982, 30, 3, p. 279–280.

7. 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, 2008, 31, 3, p. 337–345.

8. Ferramosca, A., Provenzano, SP., Coppola, L., Zara, V. Mitochondrial respiratory efficiency is positively correlated with human sperm motility. Urology, 2012, 79, 4, p. 809–814.

9. Folgerø, T., Bertheussen, K., Lindal, S., et al. Mitochondrial disease and reduced sperm motility. Hum Reprod, 1993, 8, 11, p. 1863–1868.

10. Ford, WC. Glycolysis and sperm motility: does a spoonful of sugar help the flagellum go round? Hum Reprod Update, 2006, 12, 3, p. 269–274.

11. Gnaiger, E., Kuznetsov, AV., Schneeberger, S., et al. Mitochondria in the cold. In: Life in the Cold. In Heldmaier G, Klingenspor M. Heidelberg, Berlin, New York: Springer, 2000, p. 431–442.

12. Inaba, K. Sperm flagella: comparative and phylogenetic perspectives of protein components. Mol Hum Reprod, 2011, 17, 8, p. 524–538.

13. Jansen, RP., Burton, GJ. Mitochondrial dysfunction in reproduction. Mitochondrion, 2004, 4, 5–6, p. 577–600.

14. Kao, SH., Chao, HT., Wei, YH. Multiple deletions of mitochondrial DNA are associated with the decline of motility and fertility of human spermatozoa. Mol Hum Reprod, 1998, 4, 7, p. 657–666.

15. Katz, DF., Vanagimachi, R. Movement characteristics of hamster spermatozoa within the oviduct. Biol Reprod, 1980, 22, 4, p. 759–764.

16. Marchetti, P., Ballot, C., Jouy, N., et al. Influence of mitochondrial membrane potential of spermatozoa on in vitro fertilisation outcome. Andrologia, 2012, 44, 2, p. 136–141.

17. Marin, S., Chiang, K., Bassilian, S., et al. Metabolic strategy of boar spermatozoa revealed by a metabolomic characterization. FEBS Lett, 2003, 554, 3, p. 342–346.

18. Mukai, C., Okuno, M. Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement. Biol Reprod, 2004, 71, 2, p. 540–547.

19. Mundy, AJ., Ryder, TA., Edmonds, DK. Asthenozoospermia and the human sperm mid-piece. Hum Reprod, 1995, 10, 1, p. 116–119.

20. Okada, Y., Maeno, E. Apoptosis, cell volume regulation and volume-regulatory chloride channels. Comp Biochem Physiol A Mol Integr Physiol, 2001, 130, 3, p. 377–383.

21. Peña, FJ., Rodríguez Martínez, H., Tapia, JA., et al. Mitochondria in mammalian sperm physiology and pathology: a review. Reprod Domest Anim, 2009, 44, 2, p. 345–349.

22. Pesta, D., Gnaiger, E. High-resolution respirometry: OXPHOS protocols for human cells and permeabilized fibers from small biopsies of human muscle. Methods Mol Biol, 2012, 810, p. 25–58.

23. Piasecka, M., Kawiak, J. Sperm mitochondria of patients with normal sperm motility and with asthenozoospermia: morphological and functional study. Folia Histochem Cytobiol, 2003, 41, 3, p. 125–139.

24. Piasecka, M., Gaczarzewicz, D., Laszczyńska, M., et al. Flow cytometry application in the assessment of sperm DNA integrity of men with asthenozoospermia. Folia Histochem Cytobiol, 2007, 45, Suppl. 1, p. 127–136.

25. Piomboni, P., Focarelli, R., Stendardi, A., et al. The role of mitochondria in energy production for human sperm motility. Int J Androl, 2012, 35, 2, p. 109–124.

26. Rajender, S., Rahul, P., Mahdi, AA. Mitochondria, spermatogenesis and male infertility. Mitochondrion, 2010, 10, 5, p. 419–428.

27. Rousset, S., Alves-Guerra, MC., Mozo, J., et al. The biology of mitochondrial uncoupling proteins. Diabetes, 2004, 53, Suppl. 1, p. 130–135.

28. Ruiz-Pesini, E., Díez-Sánchez, C., López-Pérez, MJ. The role of the mitochondrion in sperm function: is there a place for oxidative phosphorylation or is this a purely glycolytic process? Curr Top Dev Biol, 2007, 77, p. 3–19.

29. Scheibye-Knudsen, M., Quistorff, B. Regulation of mitochondrial respiration by inorganic phosphate; comparing permeabilized muscle fibers and isolated mitochondria prepared from type-1 and type-2 rat skeletal muscle. Eur J Appl Physiol, 2009, 105, 2, p. 279–287.

30. Spiropoulos, J., Turnbull, DM., Chinnery, PF. Can mitochondrial DNA mutations cause sperm dysfunction? Mol Hum Reprod, 2002, 8, 8, p. 719–721.

31. Stendardi, A., Focarelli, R., Piomboni, P., et al. Evaluation of mitochondrial respiratory efficiency during in vitro capacitation of human spermatozoa. Int J Androl, 2011, 34, 3, p. 247–255.

32. St. John, JC., Sakkas, D., Barratt, CL. A role for mitochondrial DNA and sperm survival. J Androl, 2000, 21, 2, p. 189–199.

33. Storey, BT., Kayne, FJ. Properties of pyruvate kinase and flagellar ATPase in rabbit spermatozoa: relation to metabolic strategy of the sperm cell. J Exp Zool, 1980, 211, 3, p. 361–367.

34. Storey, BT. Mammalian sperm metabolism: oxygen and sugar, friend and foe. Int J Dev Biol, 2008, 52, 5–6, p. 427–437.

35. Suarez, SS., Osman, RA. Initiation of hyperactivated flagellar bending in mouse sperm within the female reproductive tract. Biol Reprod, 1987, 36, 5, p. 1191–1198.

36. Suarez, SS., Ho, HC. Hyperactivation of mammalian sperm. Cell Mol Biol (Noisy-le-grand), 2003, 49, 3, p. 351–356.

37. Suarez, SS. Control of hyperactivation in sperm. Hum Reprod Update, 2008, 14, 6, p. 647–657.

38. Turner, RM. Moving to the beat: a review of mammalian sperm motility regulation. Reprod Fertil Dev, 2006, 18, 1–2, p. 25–38.

39. World Health Organization. WHO laboratory manual for the examination and processing of human semen. 5th ed. Geneva: World Health Organization, 2010, 287 p.

40. Zhang, K., Shang, Y., Liao, S., et al. Uncoupling protein 2 protects testicular germ cells from hyperthermia-induced apo-ptosis. Biochem Biophys Res Commun, 2007, 360, 2, p. 327–332.

Labels
Paediatric gynaecology Gynaecology and obstetrics Reproduction medicine

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