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Acquisition of the potential for sperm motility in steelhead (Oncorhynchus mykiss): effect of pH on dynein ATPase

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Abstract

Salmonid sperm pre-incubated at extracellular pH (pHe) values less than about 7.4 do not become motile upon water activation whereas sperm maintained above about pH 8.0 demonstrate maximal motility upon activation. The basis for this permissive effect of elevated pHe on sperm motility is not known. Since it is conceivable that the pH sensitivity of dyneinATPase (the molecular motor that drives flagellar movement) could be the basis of, or contribute to this pH dependency, the pH sensitivity of this enzymatic activity was evaluated in membrane-permeabilized axonemes (isolated flagella) ofsteelhead sperm. DyneinATPase activity was found to be sensitive to pH. This activity in permeabilized axonemes was about 3.5-fold higher at pH 7.6 compared to 7.0. To determine whether the pH sensitivity ofATP regeneration might affect the interpretation of the effect of pH on dyneinATPase activity, the pH sensitivities of creatine kinase and adenylate kinase were established. The rates ofATP generation by these enzymes were insensitive to pH between 6.5 and 8.0. The results of these studies are consistent with the hypothesis that prior maintenance at pHe, in part, controls the potential for sperm motility upon water activation via an influence on dyneinATPase activity. However, the potential for motility ofsteelhead sperm is particularly sensitive to prior maintenance at pHe values between about 7.4 and 8.0 whereas the dyneinATPase activity of permeabilized axonemes was particularly sensitive to pH values between 7.0 and 7.6. Phosphorus NMR spectroscopy was used to determine that sperm intracellular pH (pHi) increased with increasing pHe between 7.0 and 8.5 and pHi was, on average 0.4–0.5 pH units lower than pHe. Therefore the pHe sensitivity of the potential for motility appears to correspond to the pHi sensitivity of dyneinATPase activity. The data indicate that pHi is directly related to pHe and that prior incubation at pHe may, in part, control the sperm's potential for motility upon water activation via an influence on dyneinATPase activity.

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References

  • Bencic, D.C., Cloud, J.G. and Ingermann, R.L. 2000. Carbon dioxide reversibly inhibits sperm motility and fertilizing ability insteelhead (Oncorhynchus mykiss). Fish Physiol. Biochem. 23: 275–281.

    Article  Google Scholar 

  • Bencic, D.C., Ingermann, R.L. and Cloud, J.G 2001. Does CO2 enhance the short-term storage success of chinook salmon (Oncorhynchus tshawytscha) milt? Theriogenology 56: 157–166.

    Article  PubMed  Google Scholar 

  • Christen R., Schackmann, R.W. and Shapiro, B.M. 1982. Elevation of the internal pH activates respiration and motility of sperm of the sea urchin Stongylocentrotus purpuratus. J. Biol. Chem. 257: 14881–14890.

    PubMed  Google Scholar 

  • Christen, R., Schackmann, R.W. and Shapiro, B.M. 1983a Metabolism of sea urchin sperm. Interrelationships between intracellular pH,ATPase activity and mitochondrial respiration. J. Biol. Chem. 258: 5392–5399.

    PubMed  Google Scholar 

  • Christen, R., Schackmann, R.W., Dahlquist, F.W. and Shapiro, B.M. 1983b. 31P NMR analysis of sea urchin sperm activation. Exp. Cell Res. 149: 289–294.

    PubMed  Google Scholar 

  • Cosson, J., Billard, R., Cibert, C., Dréanno, C. and Suquet, M. 1999. Ionic factors regulating the motility of fish sperm. In: The Male Gamete From Basic Science to Clinical Applications, pp. 162–185. Edited by C. Gagnon. Cache River Press, Vienna, IL.

    Google Scholar 

  • Ellington, W.R. 2001. Evolution and physiological roles of phosphagen systems. Annu. Rev. Physiol. 63: 289–325.

    Article  PubMed  Google Scholar 

  • Gatti, J-L, King, S.M., Moss, A.G. and Witman, G.B. 1989. Outer arm dynein from trout spermatozoa. Purification, polypeptide composition, and enzymatic properties. J. Biol. Chem. 264: 11450–11457.

    PubMed  Google Scholar 

  • Gatti. J-L, Billard, R. and Christen, R. 1990. Ionic regulation of the plasma membrane potential of rainbow trout (Salmo gairdneri) spermatozoa: role in the initiation of sperm motility. J. Cell. Physiol. 143: 546–554.

    PubMed  Google Scholar 

  • Gibbons, I.R., Cosson, M.P., Evans, J.A., Gibbons, B.H., Houck, B., Martinson, K.H., Sale, W.S. and Tang, W.Y. 1978. Potent inhibition of dynein adenosinetriphosphatase and the motility of cilia and sperm flagella by vanadate. Proc. Natl. Acad. Sci. USA. 75: 2220–2224.

    PubMed  Google Scholar 

  • Hamamah, S and Gatti, J.L. 1998. Role of ionic environment and internal pH on sperm activity. Hum.Reprod. 13: 20–28.

    Article  Google Scholar 

  • Inaba, K., Dréanno, C., and Cosson, J. 2003. Control of flatfish sperm motility by CO2 and carbonic anhydrase. Cell Motil. Cytoskeleton. 55: 174–187.

    PubMed  Google Scholar 

  • Ingermann, R.L., Bencic, D.C. and Cloud, J.G. 2002. Low seminal plasma buffering capacity corresponds to high pH sensitivity of sperm motility in salmonids. Fish Physiol. Biochem. 24: 299–307.

    Article  Google Scholar 

  • Ingermann, R.L., Robinson, M.L. and Cloud, J.C. 2003. Respiration ofsteelhead (Oncorhynchus mykiss) sperm: Sensitivity to pH and CO2. J. Fish Biol. 62: 13–23.

    Article  Google Scholar 

  • King, S.M., Otter, T. and Witman, G.B. 1986. Purification and characterization of chlamydomonas flagellar dyneins. Methods Enzymol. 134: 291–306.

    PubMed  Google Scholar 

  • Miura, T., Yamauchi, K., Takahashi, H. and Nagahama, Y. 1992. The role of hormones in the acquisition of sperm motility in salmonid fish. J. Exp. Zool. 261: 359–363.

    PubMed  Google Scholar 

  • Morisawa, S. and Morisawa, M. 1986. Acquisition of potential for sperm motility in rainbow trout and chum salmon. J. Exp. Biol. 126: 89–96.

    PubMed  Google Scholar 

  • Morisawa, S and Morisawa, M. 1988. Induction of potential for sperm motility by bicarbonate and pH in rainbow trout and chum salmon. J. Exp. Biol. 136: 13–22.

    PubMed  Google Scholar 

  • Moss, A.G., Gatti, J.L., King, S.M. and Witman, G.B. 1991. Purification and characterization of Salmo gairdneriouter-arm dynein. Methods Enzymol. 196: 201–222.

    PubMed  Google Scholar 

  • Robitaille, P-M.L, Mumford, K.G. and Brown, G.G. 1986. 31P nuclear magnetic resonance study of trout spermatozoa at rest, after motility, and during short-term storage. Biochem. Cell Biol. 65: S474–485.

    Google Scholar 

  • Saudrais, C., Fierville, F., Loir, M., Le Rumeur, E., Cibert, C. and Cosson, J. 1998. The use of phosphocreatine plus ADP as energy source for motility of membrane deprived trout spermatozoa. Cell Motil. Cytoskeleton 41: 91–106.

    Article  PubMed  Google Scholar 

  • Tombes, R.M. and Shapiro, B.M. 1985. Metabolite channeling: a phosphorylcreatine shuttle to mediate high energy phosphate transport between sperm mitochondria and tail. Cell. 41: 325–334.

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Wang, C.S. and Smith, R.L. 1975. Lowry determination of protein in the presence of Triton X-100. Anal. Biochem. 63: 414–417.

    PubMed  Google Scholar 

  • Witman, G.B. 1989 Composition and molecular organization of the dyneins. In Cell Movement, The DyneinATPases, Vol.1, pp. 25–35. Edited by F.D. Warner, P. Satir, and I.R. Gibbons. Alan R. Liss, Inc., New York.

    Google Scholar 

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  1. Department of Biological Sciences & Center for Reproductive Biology, University of Idaho, Moscow, ID, 83844-3051, USA

    J. Woolsey & R.L. Ingermann*

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  1. J. Woolsey
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  2. R.L. Ingermann*
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Woolsey, J., Ingermann*, R. Acquisition of the potential for sperm motility in steelhead (Oncorhynchus mykiss): effect of pH on dynein ATPase. Fish Physiology and Biochemistry 29, 47–56 (2003). https://doi.org/10.1023/B:FISH.0000035896.84954.f6

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