The triggering action of physiological saline in the miracidial transformation ofSchistosoma mansoni was analyzed using various agents affecting cAMP-and Ca2+-dependent pathways. Potent activators of adenylate cyclase such as forskolin and serotonin, strongly inhibited the transformation provoked by saline in RPMI-1640. These inhibitory actions were diminished by the combined administration of phosphodiesterase activators such as ammonium salts or imidazole. Furthermore the exposure of miracidia to ammonium salts or imidazole in dechlorinated tap water “mimicked” the transformation, i.e., the cessation, of swimming and then shedding of epithelial plates. This mimic transformation was also inhibited by serotonin or forskolin. In contrast, treatment of miracidia with Ca2+ antagonists such as TMB-8 (an inhibitor of Ca2+ release), nicardipine (a Ca2+ channel blocker), or W-7 (a calmodulin inhibitor) in tap water produced severe vesiculation on their body surfaces and resulted in death. However, these toxic effects were abolished by a combined administration of these Ca2+ antagonists with saline or NH4Cl, and the transformation was reestablished except with W-7 treatment. W-7 strongly inhibited the triggering action of saline and NH4Cl and the worms swam slowly, whereas W-5, an inactive analogue of W-7, had no inhibitory effect on the transformation. These results suggest that the initiation of micracidial transformation to young sporocysts may be synergistically, regulated by cAMP and Ca2+ and that a decrease in cAMP levels and an increase in Ca2+ mobilization may be provoked in worms transformed by saline, ammonium salts, or imidazole.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Bonting SL, De Pont JJHHM, Kempen HJM, Case RM, Smith PA, Scratcherd T (1977) The effects of alloxanate, nicotinic acid and imidazole on secretory processes and the activities of adenylate cyclase and 3′,5′-AMP phosphodiesterase in cat pancreas. Br J Pharmacol 61:243–250
Coombs J, Thompson S (1987) Forskolin's effect on transient K. current in Nudibranch neurons is not reproduced by cAMP. J Neurosci 7:443–452
Epstein PM, Fiss K, Hachisu R, Andrenyak DM (1982) Interaction of calcium antagonists with cyclic AMP phosphodiesterases and calmodulin. Biochem Biophys Res Commun 105:1142–1149
Estey SJ, Mansour TE (1987) Nature of serotonin-activated adenylate cyclase during development ofSchistosoma mansoni. Mol Biochem Parasitol 26:47–60
Gelman DB, Hayes DK, Schechter MS (1976) Ammonium sulfate activation of phosphodiesterase in homogenates of larvae of the European corn borer (39353). Proc Soc Exp Biol Med 152:170–174
Gill M, King CA (1975) The mechanism of action, of cholera toxin in pigeon erythrocyte lysates. J Biol Chem 250:6424–6432
Gross JD, Bradbury J, Kay RR, Peacey MJ (1983) Intracellular pH and the control of cell differentiation inDietyostelium discoideum. Nature 303:244–245
Heyworth CM, Wallace AV, Wilson SR, Houslay MD (1984) An assessment of the ability of insulin-stimulated cyclic AMP phosphodiesterase to decrease hepatocyte intracellular cyclic AMP concentrations. Biochem J 222:183–187
Hidaka H, Sasaki Y, Tanaka T, Endo T, Ohno S, Fujii Y, Nagata T (1981)N-(6-aminohexyl)-5-chloro-1-naphthalene-sulfonamide, a calmodulin antagonist, inhibits cell proliferation. Proc Natl Acad Sci USA 78:4354–4357
Hoshi T, Garber SS, Aldrich RW (1988) Effect of forskolin on voltage-gated K+ channels is independent of adenylate cyclase activation. Science 240:1652–1655
Huang YC, Kemp RG (1971) Properties of a phosphodiesterase with high affinity for adenosine 3′,5′-cyclic phosphate. Biochemistry 10:2278–2283
Kawamoto F, Fujioka H, Kumada N, Kojima K (1986)Mesocestoides lineatus: trypsin induced development to adult mediated by Ca2+ and protein kinase C. Exp Parasitol 62:309–315
Mansour TE (1984) Serotonin receptros in parasitic worms Adv Parasitol 23:1–36
Nishizuka Y (1984) Turnover of inositol phospholipids and signal transduction. Science 225:1365–1370
Nishizuka Y (1986) Studies and perspectives of protein kinase C. Science 233:305–312
Owen NE, Vilereal ML (1982) Effect of the intracellular Ca2+ antagonist TMB-8 on serum stimulated Na+ influx in human fibroblasts. Biochem Biophys Res Commun 109:762–768
Poenie M, Alderton J, Tsien RY, Steinhardt RA (1985) Changes of free calcium levels with stages of the cell division cycle. Nature 315:147–149
Poole B, Ohkuma S (1981) Effect of weak bases on the intralysosomal pH in mouse peritoneal macrophages. J Cell Biol 90:665–669
Ribeiro JA, Dominguez ML, Sa-Aimeida AM, Gonealves MJ (1981) The effects of imidazole on neuromuseular transmission and on synaptosomal calcium uptake in the rat. Arch Int Pharmacodyn 251:270–284
Samuelson JC, Caulfield JP (1985) Role of pleated septate junctions in the epithelium of miracidia ofSchistosoma mansoni during transformation to sporocysts in vitro. Tissue Cell 17:667–682
Samuelson JC, Quinn JJ, Caulfield JP (1984) Hatching, chemokinesis, and transformation of miracidia ofSchistosoma mansoni. J Parasitol 70:321–331
Scholz KP, Byrne JH (1988) Intracellular injection of cAMP induces a long-term reduction of neuronal K+ currents. Science 240:1664–1666
Shen SS, Steinhardt RA (1978) Direct measurement of intracellular pH during metabolic derepression of the sea urchin egg. Nature 272:253–254
Siegelbaum SA, Camardo JS, Kandel ER (1982) Serotonin and cyclic AMP close single K+ channels inAplysia sensory neurones. Nature 299:413–417
Singh M, Sharma PL (1985) Modulation of 5-hydroxytryptamine-evoked responses of the isolated rat uterus by imidazole, a phosphodiesterase stimulator. Ind J Physiol Pharmacol 29:39–42
Voge M, Seidel JS (1972) Transformation in vitro of miracidia ofSchistosoma mansoni andS. japonicum into young sporocysts. J Parasitol 58:699–704
Winkler MM, Grainger JL (1978) Mechanism of action of NH4Cl and other weak bases in the activation of sea urchiu eggs. Nature 273:536–538
Winkler MM, Steinhardt RA, Grainger JL, Minning L (1980) Dual ionic controls for the activation of protein synthesis at fertilization. Nature 287:558–560
About this article
Cite this article
Kawamoto, F., Shozawa, A., Kumada, N. et al. Possible roles of cAMP and Ca2+ in the regulation of miracidial transformation inSchistosoma mansoni . Parasitol Res 75, 368–374 (1989). https://doi.org/10.1007/BF00931132
- Channel Blocker
- Physiological Saline