Skip to main content
    • Aa
    • Aa

Role of calcium influx through voltage-operated calcium channels and of calcium mobilization in the physiology of Schistosoma mansoni muscle contractions

  • D. L. MENDONÇA-SILVA (a1), E. NOVOZHILOVA (a2), P. J. R. COBBETT (a3), C. L. M. SILVA (a1), F. NOËL (a1), M. I. J. TOTTEN (a4), A. G. MAULE (a4) and T. A. DAY (a2)...

We tested the hypothesis that voltage-operated Ca2+ channels mediate an extracellular Ca2+ influx in muscle fibres from the human parasite Schistosoma mansoni and, along with Ca2+ mobilization from the sarcoplasmic reticulum, contribute to muscle contraction. Indeed, whole-cell voltage clamp revealed voltage-gated inward currents carried by divalent ions with a peak current elicited by steps to +20 mV (from a holding potential of −70 mV). Depolarization of the fibres by elevated extracellular K+ elicited contractions that were completely dependent on extracellular Ca2+ and inhibited by nicardipine (half inhibition at 4·1 μM). However these contractions were not very sensitive to other classical blockers of voltage-gated Ca2+ channels, indicating that the schistosome muscle channels have an atypical pharmacology when compared to their mammalian counterparts. Futhermore, the contraction induced by 5 mM caffeine was inhibited after depletion of the sarcoplasmic reticulum either with thapsigargin (10 μM) or ryanodine (10 μM). These data suggest that voltage-operated Ca2+ channels do contribute to S. mansoni contraction as does the mobilization of stored Ca2+, despite the small volume of sarcoplasmic reticulum in schistosome smooth muscles.

Corresponding author
Department of Biomedical Sciences, Iowa State University, Ames, IA 50011, USA. Tel: +515 294 7100. Fax: +515 294 2315. E-mail:
Linked references
Hide All

This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

Blair, K. and Anderson, P. ( 1994). Physiological and pharmacological properties of muscle cells isolated from the flatworm Bdelloura candida. Parasitology109, 325335.

Blair, K. L., Day, T. A., Lewis, M. C., Bennett, J. L. and Pax, R. A. ( 1991). Studies on muscle cells isolated from Schistosoma mansoni: a Ca2+-dependent K+ channel. Parasitology102, 251258.

Buryi, V., Morel, N., Salomone, S., Kerger, S. and Godfraind, T. ( 1995). Evidence for a direct interaction of thapsigargin with voltage-dependent Ca2+ channel. Naunyn Schmiedebergs Archives of Pharmacology351, 4045.

Chitsulo, L., Loverde, P. and Engels, D. ( 2004). Schistosomiasis. Nature Review of Microbiology2, 1213.

Cobbett, P. and Day, T. A. ( 2003). Functional voltage-gated Ca2+ channels in muscle fibers of the platyhelminth Dugesia tigrina. Comparative Biochemistry and Physiology A134, 593605.

Cunha, V. M. and Noël, F. ( 1998). Ca2+-Mg2+ ATPase in Schistosoma mansoni: evidence for heterogeneity and resistance to praziquantel. Memorias do Instituto Oswaldo Cruz93 (Suppl. 1), 181182.

Cunha, V. M., Reis, J. M. and Noël, F. ( 1996). Evidence for the presence of two Ca2+-Mg2+ ATPases with different sensitivities to thapsigargin and cyclopiazonic acid in the human flatworm Schistosoma mansoni. Comparative Biochemistry and Physiology B114, 199205.

Day, T. A., Bennett, J. L. and Pax, R. A. ( 1994). Serotonin and its requirement for maintenance of contractility in muscle fibres isolated from Schistosoma mansoni. Parasitology108, 425432.

Day, T. A., Chen, G. Z., Miller, C., Tian, M., Bennett, J. L. and Pax, R. A. ( 1996). Cholinergic inhibition of muscle fibres isolated from Schistosoma mansoni (Trematoda[ratio ]Digenea). Parasitology113, 5561.

Day, T. A., Haithcock, J., Kimber, M. and Maule, A. G. ( 2000). Functional ryanodine receptor channels in flatworm muscle fibres. Parasitology120, 417422.

Day, T. A., Kim, E., Bennett, J. L. and Pax, R. A. ( 1995). Analysis of the kinetics and voltage-dependency of transient and delayed K+ currents in muscle fibers isolated from the flatworm Schistosoma mansoni. Comparative Biochemistry and Physiology A111, 7987.

Day, T. A., Orr, N., Bennett, J. L. and Pax, R. A. ( 1993). Voltage-gated currents in muscle cells of Schistosoma mansoni. Parasitology106, 471477.

de Mendonça, R. L., Beck, E., Rumjanek, F. D. and Goffeau, A. ( 1995). Cloning and characterization of a putative calcium-transporting ATPase gene from Schistosoma mansoni. Molecular and Biochemical Parasitology72, 129139.

Fetterer, R. H., Pax, R. A. and Bennett, J. L. ( 1980). Praziquantel, potassium and 2,4-dinitrophenol: analysis of their action on the musculature of Schistosoma mansoni. European Journal of Pharmacology64, 3138.

Hamill, O. P., Marty, A., Neher, E., Sakmann, B. and Sigworth, F. J. ( 1981). Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Archives391, 85100.

Hockerman, G. H., Peterson, B. Z., Johnson, B. D. and Catterall, W. A. ( 1997). Molecular determinants of drug binding and action on L-type calcium channels. Annual Review of Pharmacology and Toxicology37, 361396.

Itonaga, Y., Nakajima, T., Morita, H., Hanano, T., Miyauchi, Y., Ito, Y. and Inoue, R. ( 2002). Contribution of nifedipine-insensitive voltage-dependent Ca2+ channel to diameter regulation in rabbit mesenteric artery. Life Sciences72, 487500.

Kohn, A. B., Anderson, P. A., Roberts-Misterly, J. M. and Greenberg, R. M. ( 2001a). Schistosome calcium channel beta subunits. Unusual modulatory effects and potential role in the action of the antischistosomal drug praziquantel. Journal of Biological Chemistry276, 3687336876.

Kumar, D., McGeown, J. G., Reynoso-Ducoing, O., Ambrosio, J. R. and Fairweather, I. ( 2003). Observations on the musculature and isolated muscle fibres of the liver fluke, Fasciola hepatica. Parasitology127, 457473.

Mitterdorfer, J., Grabner, M., Kraus, R. L., Hering, S., Prinz, H., Glossmann, H. and Striessnig, J. ( 1998). Molecular basis of drug interaction with L-type Ca2+ channels. Journal of Bioenergetics and Biomembranes30, 319334.

Noël, F., Cunha, V. M., Silva, C. L. and Mendonça-Silva, D. L. ( 2001). Control of calcium homeostasis in Schistosoma mansoni. Memorias do Instituto Oswaldo Cruz96 (Suppl.), 8588.

Olivera, B. M., Miljanich, G. P., Ramachandran, J. and Adams, M. E. ( 1994). Calcium channel diversity and neurotransmitter release: the omega-conotoxins and omega-agatoxins. Annual Review of Biochemistry63, 823867.

Remme, J. H., Blas, E., Chitsulo, L., Desjeux, P. M., Engers, H. D., Kanyok, T. P., Kengeya Kayondo, J. F., Kioy, D. W., Kumaraswami, V., Lazdins, J. K., Nunn, P. P., Oduola, A., Ridley, R. G., Toure, Y. T., Zicker, F. and Morel, C. M. ( 2002). Strategic emphases for tropical diseases research: a TDR perspective. Trends in Parasitology18, 421426.

Silva, C. L., Cunha, V. M., Mendonça-Silva, D. L. and Noël, F. ( 1998). Evidence for ryanodine receptors in Schistosoma mansoni. Biochemical Pharmacology56, 9971003.

Striessnig, J., Grabner, M., Mitterdorfer, J., Hering, S., Sinnegger, M. J. and Glossmann, H. ( 1998). Structural basis of drug binding to L Ca2+ channels. Trends in Pharmacological Sciences19, 108115.

Talla, E., de Mendonca, R. L., Degand, I., Goffeau, A. and Ghislain, M. ( 1998). Schistosoma mansoni Ca2+-ATPase SMA2 restores viability to yeast Ca2+-ATPase-deficient strains and functions in calcineurin-mediated Ca2+ tolerance. Journal of Biological Chemistry273, 2783127840.

Tunctan, B., Altug, S., Uludag, O. and Abacioglu, N. ( 2000). Effects of econazole on receptor-operated and depolarization-induced contractions in rat isolated aorta. Life Sciences67, 23932401.

Yamaguchi, S., Okamura, Y., Nagao, T. and Adachi-Akahane, S. ( 2000). Serine residue in the IIIS5-S6 linker of the L-type Ca2+ channel alpha 1C subunit is the critical determinant of the action of dihydropyridine Ca2+ channel agonists. Journal of Biological Chemistry275, 4150441511.

Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 2
Total number of PDF views: 9 *
Loading metrics...

Abstract views

Total abstract views: 69 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 22nd May 2017. This data will be updated every 24 hours.