Identification of two distinctly localized mitochondrial creatine kinase isoenzymes in spermatozoa

Journal of Cell Science

Volumn 109, Issue 8, 1996, Pages 2079-2088

  Kaldis, Philipp ^a,c   Stolz, Martin ^a   Wyss, Markus ^a,b   Zanolla, Else ^a   Rothen Rutishauser, Barbara ^a   Vorherr, Thomas ^b,d   Wallimann, Theo ^a  

^a ETH ZURICH   (Switzerland)

^b F HOFFMANN LA ROCHE LTD   (Switzerland)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Amplimmun AG   (Switzerland)

Author keywords

Anti peptide antibody; Chicken; Confocal microscopy; Creatine kinase compartmentation; Fertility; Immunofluorescence; Rooster; Seminal plasma; Sperm motility

Indexed keywords

CREATINE KINASE ISOENZYME; MITOCHONDRIAL ENZYME;

ACROSOME; ANIMAL CELL; ARTICLE; CONFOCAL LASER MICROSCOPY; HEN; IMMUNOFLUORESCENCE; MALE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; SARCOMERE; SEA URCHIN; SEMINAL PLASMA; SPERMATOZOON; SPERMATOZOON MOTILITY; SPERMATOZOON TAIL;

ANIMALS; CHICKENS; CREATINE KINASE; ELECTROPHORESIS, CELLULOSE ACETATE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ISOENZYMES; MALE; MICROSCOPY, CONFOCAL; MITOCHONDRIA; SEA URCHINS; SPERMATOZOA;

ANIMALIA; ECHINOIDEA; GALLUS GALLUS;

EID: 0029791357     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (49)

1. Asseo, P. P., Panidis, D. K., Papadimas, J. S. and Ikkos, D. G. (1981). Creatine kinase in seminal plasma of infertile man: activity and isoenzymes. Int. J. Androl. 4, 431-439.
2. Caravatti, M., Perriard, J.-C. and Eppenberger, H. M. (1979). Developmental regulation of creatine kinase isoenzymes in myogenic cultures from chicken. J. Biol. Chem. 254, 1388-1394.
3. Chida, K., Kasahara, K., Tsunenaga, M., Kohno, Y., Yamada, S., Ohmi, S. and Kuroki, T. (1990a). Purification and identification of creatine phosphokinase B as a substrate of protein kinase C in mouse skin in vivo. Biochem. Biophys. Res. Commun. 173, 351-357.
4. Chida, K., Tsunenaga, M., Kasahara, K., Kohno, Y. and Kuroki, T. (1990b). Regulation of creatine phosphokinase B activity by protein kinase C. Biochem. Biophys. Res. Commun. 173, 346-350.
5. Ellington, W. R. (1989). Phosphocreatine represents a thermodynamic and functional improvement over other phosphagens. J. Exp. Biol. 143, 177-194.
6. Fakih, H., MacLusky, N., DeCherney, A., Wallimann, T. and Huszar, G. (1986). Enhancement of human sperm motility and velocity in vitro: effects of calcium and creatine phosphate. Fertil. Steril. 46, 938-944.
7. Hammerstedt, R. H. and Lardy, H. A. (1983). The effect of substrate cycling on the ATP yield of sperm glycolysis. J. Biol. Chem. 258, 8759-8768.
8. Hemmer, W., Glaser, S. J., Hartmann, G. R., Eppenberger, H. M. and Wallimann, T. (1991). Covalent modification of creatine kinase by ATP: evidence for autophosphorylation. In Cellular Regulation by Protein Phosphorylation, vol. H 56 (ed. L. M. G. Heilmeyer), pp. 143-147. Springer Verlag, Berlin.
9. Hemmer, W., Skarli, M., Perriard, J.-C. and Wallimann, T. (1993). Effect of okadaic acid on protein phosphorylation patterns of chicken myogenic cells with special reference to creatine kinase. FEBS Lett. 327, 35-40.
10. Hemmer, W., Zanolla, E., Furter-Graves, E. M., Eppenberger, H. M. and Wallimann, T. (1994). Creatine kinase isoenzymes in chicken cerebellum: specific localization of brain-type CK in Bergmann glial cells and muscle-type CK in Purkinje neurons. Eur. J. Neurosci. 6, 538-549.
11. Huszar, G., Vigue, L. and 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, 882-888.
12. Jacobus, W. E. and Lehninger, A. L. (1973). Creatine kinase of rat heart mitochondria. J. Biol. Chem. 248, 4803-4810.
13. Kaldis, P. (1994). Mitochondrial creatine kinase isoenzymes: structure/function-relationship. Dissertation No. 10686. Swiss Federal Institute of Technology (ETH) Zürich, Switzerland.
14. Kaldis, P., Hemmer, W., Zanolla, E., Holtzman, D. and Wallimann, T. (1996). 'Hot spots' of creatine kinase localization in brain: cerebellum, hippocampus and choroid plexus. Dev. Neurosci. 18 (in press).
15. Knorr, R., Trzeciak, A., Bannwarth, W. and Gillessen, D. (1989). New coupling reagents in peptide chemistry. Tetrahedron Lett. 30, 1927-1930.
16. 2+-ATPase. Eur. J. Biochem. 213, 973-980.
17. 2+ pump function. Am. J. Physiol. 267, C357-C366.
18. Krause, S. M. and Jacobus, W. E. (1992). Specific enhancement of the cardiac myofibrillar ATPase by bound creatine kinase. J. Biol. Chem. 267, 2480-2486.
19. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
20. Lake, P. E., Smith, W. and Young, D. (1968). The ultrastructure of the ejaculated fowl spermatozoon. Q. J. Exp. Physiol. 53, 356-366.
21. Lee, H., Gong, C., Wu, S. and Iyengar, M. R. (1991). Accumulation of phosphocreatine and creatine in the cell and fluid of mouse seminal vesicles is regulated by testosterone. Biol. Reprod. 44, 540-545.
22. Moreland, B., Watts, D. C. and Virden, R. (1967). Phosphagen kinases and evolution in the echinodermata. Nature 214, 458-462.
23. Mühlebach, S. M., Gross, M., Wirz, T., Wallimann, T., Perriard, J.-C. and Wyss, M. (1994). Sequence homology and structure predictions of the creatine kinase isoenzymes. Mol. Cell. Biochem. 133/134, 245-262.
24. O'Farrell, P. H. (1975). High-resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250, 4007-4021.
25. O'Farrell, P. Z., Goodman, H. M. and O'Farrell, P. H. (1977). High resolution two-dimensional electrophoresis of basic as well as acidic proteins. Cell 12, 1133-1142.
26. Payne, R. M., Haas, R. C. and Strauss, A. W. (1991). Structural characterization and tissue-specific expression of the messenger RNAs encoding isoenzymes from two rat mitochondrial creatine kinase genes. Biochim. Biophys. Acta 1089, 352-361.
27. Quest, A. F. G., Eppenberger, H. M. and Wallimann, T. (1989) Purification of brain-type creatine kinase (B-CK) from several tissues of the chicken: B-CK subspecies. Enzyme 41, 33-42.
28. Quest, A. F. G., Soldati, T., Hemmer, W., Perriard, J.-C., Eppenberger, H. M. and Wallimann, T. (1990). Phosphorylation of chicken brain-type creatine kinase affects a physiologically important kinetic parameter and gives rise to protein microheterogeneity in vivo. FEBS Lett. 269, 457-464.
29. Quest, A. F. G. and Shapiro, B. M. (1991). Membrane association of flagellar creatine kinase in the sperm phosphocreatine shuttle. J. Biol. Chem. 266, 19803-19811.
30. Quest, A. F. G., Chadwick, J. K., Wothe, D. D., McIlhinney, R. H. J. and Shapiro, B. M. (1992). Myristoylation of flagellar creatine kinase in the sperm phosphocreatine shuttle is linked to its membrane association properties. J. Biol. Chem. 267, 15080-15085.
31. 2+ uptake and regulate local ATP/ADP ratios. J. Biol. Chem. 265, 5258-5266.
32. Schlegel, J., Wyss, M., Schürch, U., Schnyder, T., Quest, A., Wegmann, G., Eppenberger, H. M. and Wallimann, T. (1988a). Mitochondrial creatine kinase from cardiac muscle and brain are two distinct isoenzymes but both form octameric molecules. J. Biol. Chem. 263, 16963-16969.
33. Schlegel, J., Zurbriggen, B., Wegmann, G., Wyss, M., Eppenberger, H. M. and Wallimann, T. (1988b). Native mitochondrial creatine kinase forms octameric structures. I. Isolation of two interconvertible mitochondrial creatine kinase forms, dimeric and octameric mitochondrial creatine kinase: characterization, localization and structure-function relationships. J. Biol. Chem. 263, 16942-16953.
34. 2-terminus of the low density lipoprotein receptor in the plasma membrane of fibroblasts. J. Biol. Chem. 97, 1635-1640.
35. Soldati, T., Schäfer, B. W. and Perriard, J.-C. (1990). Alternative ribosomal initiation gives rise to chicken brain-type creatine kinase isoproteins with heterogeneous amino termini. J. Biol. Chem. 265, 4498-4506.
36. Soufir, J. C. (1979). Creatine kinase in human seminal plasma: activity, origin and isoenzymes. Clin. Chem. 25, 1183.
37. Steeghs, K., Oerlemans, F. and Wieringa, B. (1995). Mice deficient in ubiquitous mitochondrial creatine kinase are viable and fertile. Biochim. Biophys. Acta 1230, 130-138.
38. Thoai, N. V. and Robin, Y. (1964). Distribution of phosphagens in errant and sedentary polychaeta. In Studies in Comparative Biochemistry, vol. ?? (ed. K. Munday), pp. 152-161. Pergamon Press, London.
39. Tingari, M. D. (1973). Observations on the fine structure of spermatozoa in the testis and excurrent ducts of the male fowl, Gallus domesticus. J. Reprod. Fert. 34, 255-265.
40. Tombes, R. M. and Shapiro, B. M. (1985). Metabolite channeling: a phosphorylcreatine shuttle to mediate high energy phosphate transport between sperm mitochondrion and tail. Cell 41, 325-334.
41. Tombes, R. M. and Shapiro, B. M. (1987). Enzyme termini of a phosphocreatine shuttle. Purification and characterization of two creatine kinase isoenzymes from sea urchin sperm. J. Biol. Chem. 262, 16011-16019.
42. Wallimann, T., Schlösser, T. and Eppenberger, H. M. (1984). Function of M-line bound creatine kinase as intramyofibrillar ATP regenerator at the receiving end of the phosphorylcreatine shuttle in muscle. J. Biol. Chem. 259, 5238-5246.
43. Wallimann, T., Moser, H., Zurbriggen, B., Wegmann, G. and Eppenberger, H. M. (1986). Creatine kinase isozymes in spermatozoa. J. Muscle Res. Cell Motil. 7, 25-34.
44. Wallimann, T., Wyss, M., Brdiczka, D., Nicolay, K. and Eppenberger, H. M. (1992). Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the 'phosphocreatine circuit' for cellular energy homeostasis. Biochem. J. 281, 21-40.
45. Wallimann, T. and Hemmer, W. (1994). Creatine kinase in non-muscle tissues and cells. Mol. Cell. Biochem. 133/134, 193-220.
46. Wothe, D. D., Charbonneau, H. and Shapiro, B. M. (1990) The phosphocreatine shuttle of sea urchin sperm: flagellar creatine kinase resulted from a gene triplication. Proc. Nat. Acad Sci. USA 87, 5203-5207.
47. Wyss, M., Schlegel, J., James, P., Eppenberger, H. M. and Wallimann, T. (1990). Mitochondrial creatine kinase from chicken brain. J. Biol. Chem. 265, 15900-15908.
48. Wyss, M., Smeitink, J., Wevers, R. A. and Wallimann, T. (1992). Mitochondrial creatine kinase: a key enzyme of aerobic energy metabolism. Biochim. Biophys. Acta 1102, 119-166.
49. Wyss, M., Maughan, D. and Wallimann, T. (1995). Re-evaluation of the structure and physiological function of guanidino kinases in fruitfly (Drosophila), sea urchin (Psammechinus miliaris) and man. Biochem. J. 309, 255-261.