Browse > Article

Cell Signaling Mechanisms of Sperm Motility in Aquatic Species  

Kho, Kang-Hee (Misaki Marine Biological Station, Graduate School of Science, The University of Tokyo)
Morisawa, Masaaki (Misaki Marine Biological Station, Graduate School of Science, The University of Tokyo)
Cho, Kap-Seong (Department of Food Science and Technology, Sunchon National University)
Publication Information
Journal of Microbiology and Biotechnology / v.15, no.3, 2005 , pp. 665-671 More about this Journal
Abstract
Initiation and activation of sperm motility are prerequisite processes for the contact and fusion of male and female gametes at fertilization. The phenomena are under the regulation of cAMP and $Ca^{2+}$ in vertebrates and invertebrates. Mammalian sperm requires $Ca^{2+}$ and cAMP for the activation of sperm motility. Cell signaling for the initiation and activation of sperm motility in the ascidians and salmonid fishes has drawn much attention. In the ascidians, the sperm-activating and attracting factors from unfertilized egg require extracellular $Ca^{2+}$ for activating sperm motility and eliciting chemotactic behavior toward the egg. On the other hand, the cAMP-dependent phosphorylation of protein is essential for the initiation of sperm motility in salmonid fishes. A decrease of the environmental $K^+$ concentration surrounding the spawned sperm causes $K^+$ efflux and $Ca^{2+}$ influx through the specific $K^+$ channel and dihydropyridine-sensitive L-/T-type $Ca^{2+}$ channel, respectively, thereby leading to the membrane hyperpolarization. The membrane hyperpolarization induces synthesis of cAMP, which triggers further cell signaling processes, such as cAMP-dependent protein phosphorylation, to initiate sperm motility in salmonid fishes. This article reviews the studies on the physiological mechanisms of sperm motility and its cell signaling in aquatic species.
Keywords
Sperm; motility; cell signaling; salmonid; teleost;
Citations & Related Records

Times Cited By Web Of Science : 1  (Related Records In Web of Science)
연도 인용수 순위
  • Reference
1 Ashizawa, K., H. Tomonaga, and Y. Tsuzuki. 1994. Regulation of flagellar motility of fowl spermatozoa: Evidence for the involvement of intracellular $Ca^{2+}$ and calmodulin. J. Reprod. Fert. 101: 265-272   DOI   ScienceOn
2 Ashizawa, K., G. J. Wishart, and Y. Tsuduki. 1995. Regulatory mechanisms of fowl sperm motility: Possible role of endogenous myosin light chain kinase-like protein. J. Reprod. Fertil. 104: 141-148   DOI   ScienceOn
3 Babcock, D. F., D. M. Stammerjohn, and T. Hutchison. 1978. Calcium redistribution in individual cells correlated with ionophore action on motility. J. Exp. Zool. 204: 391-400   DOI   ScienceOn
4 Brokaw, C. J. 1991. Calcium sensors in sea urchin sperm flagella. Cell Motil. Cytoskel. 18: 123-130   DOI   PUBMED   ScienceOn
5 Detweiler, C. and P. Thomas. 1998. Role of ions and ion channels in the regulation of Atlantic croaker sperm motility. J. Exp. Zool. 281: 139-148   DOI   ScienceOn
6 Galindo, B. E., C. Beltran, E. J. Cragoe, and A. Darszon. 2000. Participation of a $K^+$ channel modulated directly by cGMP in the speract-induced signaling cascade of Strongylocentrotus purpuratus sea urchin sperm. Dev. Biol. 221: 285-294   DOI   ScienceOn
7 Griffin, F. J., C. A. Vines, M. C. Pillai, R. Yanagimachi, and C. N. Cherr. 1996. Sperm motility initiation factor is a major component of the Pacific herring egg chorion. Dev. Growth Differ. 38: 193-202
8 Inaba, K., O. Kagami, and K. Ogawa. 1999. Tctex2-related outer arm dynein light chain is phosphorylated at activation of sperm motility. Biochem. Biophys. Res. Commun. 256: 177-183   DOI   ScienceOn
9 Means, A. R., J. S. Tash, and V. Guerriero. 1982. Regulation of the cytoskelton by $Ca^{2+}$-calmodulin and cAMP. Ann. NY. Acad. Sci. 383: 69-84   DOI   PUBMED
10 Morisawa, M. and M. Okuno. 1982. Cyclic AMP induces maturation of trout sperm axoneme to initiate motility. Nature 295: 703-704   DOI   ScienceOn
11 Morisawa, M., S. Tanimoto, and H. Ohtake. 1992. Characterization and partial purification of sperm-activating substance from eggs of the herring, Clupea plasii. J. Exp. Zool. 264: 225-230   DOI   ScienceOn
12 Morton, B. E., R. Sagadrac, and C. Fraser. 1978. Sperm motility within the mammalian epididymis: Species variation and correlation with free calcium levels in epididymal plasma. Fertil. Steril. 29: 695-698   DOI
13 Oda, S., Y. Igarashi, K. Manaka, N. Koibuchi, M. SakaiSawada, K. Sakai, M. Morisawa, H. Ohtake, and N. Shimizu. 1998. Sperm-activating proteins obtained from the herring egg are homologous to trypsin inhibitors and synthesized in follicle cells. Dev. Biol. 204: 55-63   DOI   ScienceOn
14 Heffiner, L. J. and B. T. Storey. 1981. The role of calcium in maintaining motility in mouse spermatozoa. J. Exp. Zool. 218: 427-434   DOI   ScienceOn
15 Ashizawa, K., G. J. Wishart, H. Tomonaga, K. Nishinakama, and Y. Tsuzuki. 1994. Presence of protein phosphatase type and its involvement in temperature-dependent flagellar movement of fowl spermatozoa. FEBS Lett. 350: 130-134   DOI   ScienceOn
16 Cosson, M. P., R. Billard, and L. Letellier. 1989. Rise of internal $Ca^{2+}$ accompanies the initiation of trout sperm motility. Cell Motil. Cytoskel. 14: 424-434   DOI
17 Morisawa, M. and H. Hayashi. 1985. Phosphorylation of a 15 K axonemal protein is the trigger initiating trout sperm motility. Biomed. Res. 6: 181-184   DOI
18 Amanze, D. and A. Iyenger. 1990. The micropyle: A sperm guidance system in teleost fertilization. Development 109: 495-500
19 Johnson, C. H., D. L. Clapper, M. M. Winkler, H. C. Lee, and D. Epel. 1983. A volatile inhibitor immobilizes sea urchin sperm in semen by depressing the intracellular pH. Dev. Biol. 98: 493-501   DOI   ScienceOn
20 Okamura, N., Y. Tajima, A. Soejima, H. Masuda, and Y. Sugita. 1985. Sodium bicarbonate in seminal plasma stimulates the motility of mammalian spermatozoa through direct activation of adenylyl cyclase. J. Biol. Chem. 260: 9699-9705
21 Kho, K. H., M. Morisawa, and K. S. Choi. 2003. Membrane hyperpolarization increases cAMP to induce the initiation of sperm motility in Salmonid fishes, rainbow trout and masu salmon. J. Microbiol. Biotechnol. 13: 833-840
22 Yoshida, K. 1998. The study on the mechanism of sperm activation by sperm-activation proteins in the Pacific herring, Clupea pallasii. Ph. D. Thesis, University of Tokyo, Tokyo
23 Gatti, J. L., R. Billard, and R. Christen. 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   DOI   PUBMED
24 Gray, J. 1928. The effect of dilution on the activity of spermatozoa. Br. J. Exp. Biol. 5: 337-344
25 Ishiguro, K., H. Murofushi, and H. Sakai. 1982. Evidence that cAMP-dependent protein kinase and a protein factor are involved in reactivation of Triton X-100 models of sea urchin and star-fish spermatozoa. J. Cell Biol. 92: 777-782   DOI   ScienceOn
26 Kho, K. H., T. Satomi, K. Inaba, Y. Oka, and M. Morisawa. 2001. Transmembrane cell signaling for the initiation of trout sperm motility: Roles of ion channels and membrane hyperpolarization for cyclic AMP synthesis. Zool. Sci. 18: 919-928   DOI   ScienceOn
27 Mazia, D., C. Petzelt, R. O. Williams, and I. Meza. 1972. A Ca-activated ATPase in the mitotic apparatus of the sea urchin egg (isolated by a new method). Exp. Cell Res. 70: 325-332   DOI   ScienceOn
28 Pillai, M. C., T. S. Shields, R. Yanagimachi, and G. N. B. Cherr. 1993. Isolation and partial characterization of the sperm motility initiation factor from eggs of the Pacific herring, Clupea pallasi. J. Exp. Zool. 265: 336-342   DOI   ScienceOn
29 Chang, Y. J., Y. H. Choi, H. K. Lim, and K. H. Kho. 1999. Cold storage and cryopreservation of grey mullet, Mugil cephalus, sperm. J. Aquaculture 12: 57-62
30 Lindermann, C. B. 1978. A cAMP-induced increase in the motility of demembranated bull sperm models. Cell 13: 918
31 Pires, E. M. V. and S. V. Perry. 1977. Purification and properties of myosin light chain kinase from fast skeletal muscle. J Biol. Chem. 167: 137-146
32 Kho, K. H., Y. J. Chang, and H. K. Lim. 1997. Effect of osmolality and $Ca^{2+}$ on sperm motility in marbled sole, Limanda yokohamae. J. Korean Fish. Soc. 30: 809-815
33 Babcock, D. F., J. P. Singh, and H. A. Lardy. 1979. Alteration of membrane permeability to calcium ions during maturation of bovine spermatozoa. Dev. Biol. 69: 85-93   DOI   ScienceOn
34 Cook, S. P. and D. F. Babcock. 1993. Activation of $Ca^{2+}$ permeability by cAMP is coordinated through the pH increase induced by speract. J. Biol. Chem. 268: 22408-22413
35 Cook, S. P. and D. F. Babcock. 1993. Selective modulation by cGMP of the $K^+$ channel activated by speract. J. Biol. Chem. 268: 22402-22407
36 Oda, S., Y. Igarashi, H. Ohtake, K. Sakai, N. Shimizu, and M. Morisawa. 1995. Sperm-activating proteins from unfertilized eggs of the Pacific herring, Clupia pallasii. Dev. Growth Differ. 37: 257-261   DOI   ScienceOn
37 Billard, R., T. Cosson, and L. W. Crim. 1993. Motility and survival of halibut sperm during short term storage. Aqua. Living Resour. 6: 67-75   DOI   ScienceOn
38 Boitano, S. and C. K. Omoto. 1991. Membrane hyperpolarization activates trout sperm without an increase in intracellular pH. J. Cell Sci. 98: 343-349
39 Bookbinder, H., G. W. Moy, and V. D. Vacquire. 1990. Purification of sea urchin sperm adenylyl cyclase. J. Cell Biol. 111: 1859-1866   DOI   ScienceOn
40 Storey, B. T. 1975. Energy metabolism of spermatozoa: Effect of calcium ion on respiration of mature epididymal sperm of rabbit. Biol. Reprod. 13: 1-9   DOI   PUBMED   ScienceOn
41 Nishioka, D. and N. Cross. 1978. The role of external sodium in sea urchin fertilization, pp. 403-413. In Dirksen, E. R., Prescott, D. M. and Fox, C. F. (eds.), Cell Reproduction. Academic Press
42 Morisawa, M. and K. Suzuki. 1980. Osmolarity and potassium ion: Their roles in initiation of sperm motility in teleosts. Science 210: 1145-1147   DOI   PUBMED
43 Tajima, Y., N. Okamura, and Y. Sugita. 1987. The activation effects of bicarbonate on sperm motility and respiration at ejaculation. Biochim. Biophys. Acta 924: 519-529   DOI   ScienceOn
44 Morton, B., J. Hrrigan-Lum, L. Albabli, and T. Jooss. 1974. The activation of motility in quiescent hamster sperm from the epididymis by calcium and cyclic nucleotides. Biochem. Biophys. Res. Commun. 56: 372-379   DOI   ScienceOn
45 Chafouleas, J. G., J. R. Dedman, R. P. Munjal, and A. R. Means. 1979. Calmodulin: Development and application of a sensitive radioimmunoassay. J. Biol. Chem. 254: 10262-10267
46 Gonzlez-Martnez, M. T., A. Guerrero, E. Morales, L. D. L. Torre, and A. Darszon. 1992. A depolarization can trigger $Ca^{2+}$ uptake and the acrosome reaction when preceded by a hyperpolarization in L. pictus sea urchin sperm. Dev. Biol. 150: 193-202   DOI   ScienceOn
47 Izumi, H., T. Mrin, K. Inaba, Y. Oka, and M. Morisawa. 1999. Membrane hyperpolarization by sperm activating and attracting factor increases cAMP level and activates sperm motility in the ascidian Ciona intestinalis. Dev. Biol. 213: 246-256   DOI   ScienceOn
48 Rothchild, L. 1948. The physiology of sea-urchin spermatozoa: Senescence and the dilution effect. J. Exp. Biol. 25: 353-368
49 Cheung, W. Y. 1970. Cyclic 3',5'-nucleotide phosphodiesterase: Demonstration of an activator. Biochem. Biophys. Res. Commun. 90: 1039-1047
50 Epel, D. E., R. W. Wallace, and W. Y. Cheung. 1981. Calmodulin activates NAD kinase of sea urchin eggs: An early event of fertilization. Cell 23: 543-549   DOI   ScienceOn
51 Strussmann, C. A., P, Renard, H. Ling, and F. Takashima. 1994. Motility of pejjerey Odontesthes bonariensis spermatozoa. Fish Sci. 60: 9-13   DOI
52 Tanimoto, S. and M. Morisawa. 1988. Roles of potassium and calcium channels in the initiation of sperm motility in rainbow trout. Dev. Growth Diff. 30: 117-124   DOI
53 Blum, J., G. A. Hayes, J. Jamieson, and T. C. Vanaman. 1980. Calmodulin confers calcium sensitivity on ciliary dynein ATPase. J. Cell Biol. 87: 386-397   DOI   ScienceOn
54 Babcock, D. F., M. M. Bosma, D. E. Battaglia, and A. Darszon. 1992. Early persistent activation of sperm $K^+$ channels by the egg peptide speract. Proc. Natl. Acad. Sci. USA 89: 6001-6005
55 Morisawa, M., M. Okuno, K. Suzuki, S. Morisawa, and K. Ishida. 1983. Initiation of sperm motility in telosts. J. Submicrosc. Cytol. 15: 61-65
56 Beltran, C., O. Zapata, and A. Darszon. 1996. Membrane potential regulates sea urchin sperm adenylylcyclase. Biochemistry 35: 7591-7598   DOI   ScienceOn
57 Brokaw, C. J. and S. M. Nagayama. 1985. Modulation of the asymmetry of sea urchin sperm flagellar bending by calmodulin. J Cell Biol. 100: 1875-1883   DOI   ScienceOn
58 Chang, Y. J., H. K. Lim, and K. H. Kho. 1995. Properties of semen and sperm motility in black seabream, Acanthopagrus schlegeli. J. Aquaculture 8: 149-157
59 Kakiuchi, S. and R. Yamazaki. 1970. Calcium-dependent phosphodiesterase activity and its activating factor (PAF) from brain: Studies on cyclic 3',5'-nucleotide phosphodiesterase. Biochem. Biophys. Res. Commun. 41: 1104-1110   DOI   ScienceOn
60 Krasznai, Z., T. Marian, H. Izumi, S. Damjanovich, L. Balkay, L. Tron, and M. Morisawa. 2000. Membrane hyperpolarization removes inactivation of $Ca^{2+}$ channels, leading to $Ca^{2+}$ influx and subsequent initiation of sperm motility in the common carp. Proc. Natl. Acad. Sci. USA 97: 2052-2057
61 Si, Y. and M. Okuno. 1995. Activation of mammalian sperm motility by regulation of microtuble sliding via cyclic adenosine 5'-monophosphate-dependent phosphorylation. Biol. Repr. 53: 1081-1087   DOI   ScienceOn
62 Si, Y. and M. Okuno. 1993. Multiple activation of mouse sperm motility. Mol. Reprod. Dev. 36: 89-95   DOI   ScienceOn
63 Tombes, R. M. and B. M. Shapiro. 1985. Metabolite channeling: A phosphocreatine shuttle to mediate high energy phosphate transport between sperm mitochondria. Cell 4: 325-334
64 Si, Y. and M. Okuno. 1999. Regulation of microtubule sliding by a 36-kDa phosphoprotein in hamster sperm flagella. Mol. Reprod. Dev. 52: 328-334   DOI   ScienceOn
65 Yoshida, T. and M. Nomura. 1972. A substance enhancing sperm motility in the ovarian fluid of rainbow trout. Bull. Japan Soc. Sci. Fish 38: 1073-1079   DOI
66 Si, Y. and M. Okuno. 1999. Role of tyrosine phosphorylation of flagellar proteins in hamster sperm hyperactivation. Biol. Reprod. 61: 240-246   DOI   ScienceOn
67 Tash, J. S., S. S. Kakar, and A. R. Means. 1984. Flagellar motility requires the cAMP-dependent phosphorylation of a heat-stable NP-40-soluble 56 kDa protein, axokinin. Cell 38: 551-559   DOI   ScienceOn
68 Yanagimachi, R., G. N. Cherr, M. C. Pillai, and J. D. Baldwin. 1992. Factors controlling sperm entry into the micropyles of salmonid and herring eggs. Dev. Growth Differ. 34: 447-461   DOI
69 Morisawa, M. and K. Ishida. 1987. Short-term changes in levels of cyclic AMP, adenylate cyclase, and phosphodiesterase during the initiation of sperm motility in rainbow trout. J. Exp. Zool. 242: 199-204   DOI   ScienceOn
70 Si, Y. and M. Okuno. 1995. Extrusion of microtubule doublet outer dense fiber 5-6 associating with fibrous sheath sliding in mouse sperm flagella. J. Exp. Zool. 273: 355-362   DOI   ScienceOn
71 Takai, H. and M. Morisawa. 1995. Changes in intracellular $K^+$ concentration caused by external osmolality change regulate sperm motility of marine and freshwater teleosts. J. Cell Sci. 108: 1175-1181
72 Tash, J. S. and A. R. Means. 1983. Cyclic adenosine 3,5 monophosphate, calcium and protein phosphorylation in flagellar motility. Biol. Reprod. 28: 75-104   DOI   ScienceOn
73 Nomura, M., K. Inaba, and M. Morisawa. 2000. Cyclic AMP- and calmodulin-dependent phosphorylation of 21 and 26 kDa proteins in axoneme is a prerequisite for SAAF-induced motile activation in ascidian spermatozoa. Dev. Growth Differ. 42: 129-138   DOI   ScienceOn
74 Billard, R. 1978. Changes in structure and fertilization ability of marine and fresh water fish spermatozoa diluted in media of various salinities. Aquaculture 14: 187-198   DOI   ScienceOn
75 Chao, N. H., H. P. Chen, and I. C. Liao. 1975. Study on cryogenic preservation of grey mullet sperm. Aquacultute 5: 389-406   DOI   ScienceOn
76 Kho, K. H., M. Morisawa, and K. S. Choi. 2004. Role of $Ca^{2+}$ and calmodulin on the initiation of sperm motility in salmonid fishes. J. Microbiol. Biotechnol. 14: 456-465
77 Tanimoto, S., Y. Kudo, T. Nakazawa, and M. Morisawa. 1994. Implication that potassium flux and increase in intracellular calcium are necessary for the initiation of sperm motility in salmonid fishes. Mol. Reprod. Dev. 39: 409-414   DOI   ScienceOn