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Calcium activation of macrocilia in the ctenophoreBeroë

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Summary

  1. 1.

    Macrocilia on the lips of the ctenophoreBeroë are usually quiescent, but can be activated to beat rapidly and continuously by various stimuli.

  2. 2.

    During feeding, macrocilia beat actively and serve to spread the lips ofBeroë over its prey.

  3. 3.

    Vigorous, repetitive mechanical stimulation of the lips evokes widespread activation of macrocilia via a pathway that is probably neural.

  4. 4.

    Extracellular electrical stimulation (DC or bipolar pulse-trains) elicits immediate activation of macrocilia on lip pieces, but not on dissociated cells.

  5. 5.

    Macrocilia on lip pieces are activated to beat by high KCl artificial sea water (ASW), but not by high KCl Ca-free ASW. Continuous beating for long periods is also elicited by high Ca ASW or Mg-free ASW, but not by Ca-Mg-free ASW. Addition of La, Cd, Co or Mn (10 mM) to high KCl ASW reversibly blocks activation. Verapamil, D-600, nifedipine, or BAY K 8644 (10 μM) has no effect on KCl-induced activation, but the anticalmodulin drug W-7 (10 μM) reversibly inhibits beating.

  6. 6.

    Mild heat treatment dissociates macrociliary cells from lip tissue. Such isolated macrociliary cells usually beat continuously in normal sea water, and swim in circular paths. Ca-free ASW, or addition of Co or Mn to ASW, inhibits beating of dissociated cells. High KCl ASW activates beating of quiescent, isolated macrociliary cells.

  7. 7.

    Ca-Mg-free ASW inhibits beating of dissociated macrociliary cells, and return to Mg-free ASW activates motility, allowing one to activate macrocilia on isolated cells simply by addition of Ca.

  8. 8.

    These results indicate that sensory stimuli associated with feeding may excite the pharyngeal nerve net, thereby depolarizing macrociliary cells and opening voltage-sensitive Ca channels which mediate a Ca influx responsible for activation of beating.

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References

  • Bonini NM, Gustin MC, Nelson DL (1986) Regulation of ciliary motility by membrane potential inParamecium: a role for cyclic AMP. Cell Motil 6:256–272

    Google Scholar 

  • Brokaw CJ (1984) Cyclic AMP-dependent activation of sea urchin and tunicate sperm motility. Ann NY Acad Sci 438:132–141

    Google Scholar 

  • Brokaw CJ, Nagayama SM (1985) Modulation of the asymmetry of sea urchin sperm flagellar by calmodulin. J Cell Biol 100:1875–1883

    Google Scholar 

  • Eckert R, Murakami A (1972) Calcium dependence of ciliary activity in the oviduct of the salamanderNecturus. J Physiol 226:699–711

    Google Scholar 

  • Franc J-M (1970) Evolutions et interactions tissulaires au cours de la régeneration des lèvres deBeroë ovata (Chamisso et Eysenhardt), ctenaire nudictenide. Cah Biol Mar 11:57–76

    Google Scholar 

  • Hasegawa E, Hayashi H, Asakura S, Kamiya R (1987) Stimulation of in vitro motility ofChlamydomonas axonemes by inhibition of cAMP-dependent phosphorylation. Cell Mot Cytoskel 8:302–311

    Google Scholar 

  • Hennessey TM, Kung C (1984) An anticalmodulin drug, W-7, inhibits the voltage-dependent calcium current inParamecium caudatum. J Exp Biol 110:169–181

    Google Scholar 

  • Horridge GA (1965) Macrocilia with numerous shafts from the lips of the ctenophoreBeroë. Proc R Soc Lond B 162:351–364

    Google Scholar 

  • Ishiguro K, Murofushi H, Sakai H (1982) Evidence that cAMP-dependent protein kinase and a protein factor are involved in reactivation of Triton X-100 models of sea urchin and starfish spermatozoa. J Cell Biol 92:777–782

    Google Scholar 

  • Izumi A, Nakaoka Y (1987) cAMP-mediated inhibitory effect of calmodulin antagonists on ciliary reversal ofParamecium. Cell Motil 7:154–159

    Google Scholar 

  • Kung C, Saimi Y (1985) Ca2+ channels ofParamecium: a multidisciplinary study. Curr Topics Membr Transport 23:45–66

    Google Scholar 

  • Lee WI, Verdugo P, Schurr JM, Blandau RJ (1976) Control of oviductal ciliary activity. Effect of extracellular (Ca++). Biophys J 16:120a

    Google Scholar 

  • Lindemann CB (1978) A cAMP-induced increase in the motility of demembranated bull sperm models. Cell 13:9–18

    Google Scholar 

  • Malanga CJ, Poll KA (1979) Effects of the cilioexcitatory neurohumors dopamine and 5-hydroxytryptamine on cyclic AMP levels in the gill of the musselMytilus edulis. Life Sci 25:365–374

    Google Scholar 

  • Morisawa M, Hayashi H (1985) Phosphorylation of a 15K axonemal protein is the trigger initiating trout sperm motility. Biomed Res 6:181–184

    Google Scholar 

  • Morisawa M, Okuno M (1982) Cyclic AMP induces maturation of trout sperm axoneme to initiate motility. Nature 295:703–704

    Google Scholar 

  • Moss AG, Tamm SL (1986) Electrophysiological control of ciliary motor responses in the ctenophorePleurobrachia J Comp Physiol A 158:311–330

    Google Scholar 

  • Moss AG, Tamm SL (1987) A calcium regenerative potential controlling ciliary reversal is propagated along the length of ctenophore comb plates. Proc Natl Acad Sci USA 84:6476–6480

    Google Scholar 

  • Murakami A (1983) Control of ciliary beat frequency inMytilus. J Submicrosc Cytol 15:313–316

    Google Scholar 

  • Murakami A (1987a) Control of ciliary beat frequency in the gill ofMytilus. I. Activation of the lateral cilia by cyclic AMP. Comp Biochem Physiol 86C:273–279

    Google Scholar 

  • Murakami A (1987b) Control of ciliary frequency in the gill ofMytilus. II. Effects of saponin and Brij-58 on the lateral cilia. Comp Biochem Physiol 86C:281–287

    Google Scholar 

  • Murakami A, Eckert R (1972) Cilia: activation coupled to mechanical stimulation by calcium influx. Science 175:1375–1377

    Google Scholar 

  • Murakami A, Machemer H (1982) Mechanoreception in the lateral cells ofMytilus. J Comp Physiol 145:351–362

    Google Scholar 

  • Murofushi H, Ishiguro K, Takahashi D, Ikeda J, Sakai H (1986) Regulation of sperm flagellar movement by protein phosphorylation and dephosphorylation. Cell Motil 6:83–88

    Google Scholar 

  • Naitoh Y, Eckert R (1974) The control of ciliary activity in Protozoa. In: Sleigh MA (ed) Cilia and flagella. Academic Press, New York, pp 305–352

    Google Scholar 

  • Nakamura S, Tamm SL (1985) Calcium control of ciliary reversal in ionophore-treated and ATP-reactivated comb plates of ctenophores. J Cell Biol 100:1447–1454

    Google Scholar 

  • Opresko LK, Brokaw CJ (1983) cAMP-dependent phosphorylation associated with activation of motility ofCiona sperm flagella. Gamete Res 8:201–218

    Google Scholar 

  • Otter T, Satir B, Satir P (1984) Trifluoperazine-induced changes in swimming behavior ofParamecium: evidence for two sites of drug action. Cell Motil 4:249–267

    Google Scholar 

  • Reed W, Lebduska S, Satir P (1982) Effects of trifluoperazine upon the calcium dependent ciliary arrest response of fresh-water mussel gill lateral cells. Cell Motil 2:405–427

    Google Scholar 

  • Saimi Y, Murakami A, Takahashi K (1983a) Electrophysiological correlates of nervous control of ciliary arrest response in the gill epithelial cells ofMytilus. Comp Biochem Physiol 74A:499–506

    Google Scholar 

  • Saimi Y, Murakami A, Takahashi K (1983b) Ciliary and electrical responses to intracellular current injection in the ciliated epithelium of the gill ofMytilus. Comp Biochem Physiol 74A:507–511

    Google Scholar 

  • Sanderson MJ, Dirksen ER (1986) Mechanosensitivity of cultured ciliated cells from mammalian respiratory tract: implications for the regulation of mucociliary transport. Proc Natl Acad Sci USA 83:7302–7306

    Google Scholar 

  • Sanderson MJ, Dirksen ER, Satir P (1985) The antagonistic effects of 5-hydroxytryptamine and methylxanthine on the gill cilia ofMytilus edulis. Cell Motil 5:293–309

    Google Scholar 

  • Satir P (1985) Switching mechanisms in the control of ciliary motility. Mod Cell Biol 4:1–46

    Google Scholar 

  • Segal RA, Luck DJ (1985) Phosphorylation in isolatedChlamydomonas axonemes: a phosphoprotein may mediate the Cadependent photophobic response. J Cell Biol 101:1702–1712

    Google Scholar 

  • Stephens RE, Stommel EW (1988) The role of cAMP in ciliary and flagellar motility. In: Warner FD (ed) Cell movement, vol 1. The dynein ATPase. Alan R Liss, New York

    Google Scholar 

  • Stommel EW (1984a Calcium regenerative potentials inMytilus edulis gill abfrontal ciliated epithelial cells. J Comp Physiol A 155:445–456

    Google Scholar 

  • Stommel EW (1984b) Calcium activation of mussel gill abfrontal cilia. J Comp Physiol A 155:457–469

    Google Scholar 

  • Stommel EW (1986) Mechanical stimulation activates beating in calcium-arrested lateral cilia ofMytilus edulis gill. J Musc Res Cell Motil 7:237–244

    Google Scholar 

  • Stommel EW, Stephens RE (1985) Cyclic AMP and calcium in the differential control ofMytilus gill cilia. J Comp Physiol A 157:451–459

    Google Scholar 

  • Stommel EW, Stephens RE, Measure HR, Head JF (1982) Specific localization of scallop gill epithelial calmodulin in cilia. J Cell Biol 92:622–628

    Google Scholar 

  • Swanberg N (1974) The feeding behavior ofBeroë ovataMar Biol 24:69–76

    Google Scholar 

  • Tamm S, Tamm SL (1988) Development of macrociliary cells inBeroë. II. Formation of macrocilia. J Cell Sci 89:81–95

    Google Scholar 

  • Tamm SL (1982) Ctenophora. In: Shelton GAB (ed) Electrical conduction and behaviour in ‘simple’ invertebrates. Oxford Univ Press, Oxford, pp 266–358

    Google Scholar 

  • Tamm SL (1983) Motility and mechanosensitivity of macrocilia in the ctenophoreBeroë. Nature 305:430–433

    Google Scholar 

  • Tamm SL (1987) Calcium activation and location of calcium entry sites in macrocilia ofBeroë. J Cell Biol 105:95a

    Google Scholar 

  • Tamm SL, Tamm S (1984) Alternate patterns of doublet microtubule sliding in ATP-disintegrated macrocilia of the ctenophoreBeroë. J Cell Biol 99:1364–1371

    Google Scholar 

  • Tamm SL, Tamm S (1985) Visualization of changes in ciliary tip configuration caused by sliding displacement of microtubules in macrocilia of the ctenophoreBeroë. J Cell Sci 79:161–179

    Google Scholar 

  • Tash JS, Means AR (1982) Regulation of protein phosphorylation and motility of sperm by cyclic adenosine monophosphate and calcium. Biol Reprod 26:745–763

    Google Scholar 

  • Tash JS, Kakar SS, Means AR (1984) Flagellar motility requires the cAMP-dependent phosphorylation of a heat-stable NP-40-soluble 56 kd protein, axokinin. Cell 38:551–559

    Google Scholar 

  • Tash JS, Hidaka H, Means AR (1986) Axokinin phosphorylation by cAMP-dependent protein kinase is sufficient for activation of sperm flagellar motility. J Cell Biol 103:649–655

    Google Scholar 

  • Verdugo P, Rumery RE, Lee WI (1977) Calcium-induced activation of ciliary activity in mammalian ciliated cells. J Cell Biol 75:293a

    Google Scholar 

  • Verdugo P, Raes BV, Villalon M (1983) Calcium-dependent activation of ciliary movement: effect of calmodulin. Biophys J 41:83a

    Google Scholar 

  • Yeung CH (1984) Effects of cyclic AMP on the motility of mature and immature hamster epididymal spermatozoa studied by reactivation of demembranated cells. Gamete Res 9:99–114

    Google Scholar 

Download references

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  1. Marine Biological Laboratory, Boston University Marine Program, 02543, Woods Hole, Massachusetts, USA

    Sidney L. Tamm

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Tamm, S.L. Calcium activation of macrocilia in the ctenophoreBeroë . J. Comp. Physiol. 163, 23–31 (1988). https://doi.org/10.1007/BF00611993

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  • DOI: https://doi.org/10.1007/BF00611993

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