Summary
The physiological properties of mechanical responses and the intracellular localization and translocation of calcium as a pyroantimonate precipitate were studied in the longitudinal retractor muscle (LRM) of a Bermuda sea cucumber. Acetylcholine (ACh)-induced contraction was reduced by lowering the external Ca concentration, and suppressed completely by prolonged soaking in Ca-free solution. The magnitude of ACh-induced contraction was decreased by Mn and La ions. Furthermore, procaine reduced the ACh-induced contraction. The complete removal of Ca and Mg ions from the external medium induced a socalled Ca · Mg-removal contraction. Electron microscopically, numerous subsarcolemmal vesicles were observed in the LRM fibers. In the resting fibers, pyroantimonate precipitates were localized in the subsarcolemmal vesicles and along the inner surface of plasma membrane. While, in the fiber fixed during mechanical activity, the pyroantimonate precipitates were decreased remarkably in the subsarcolemmal vesicles and at the plasma membrane, and diffusely distributed in the myoplasm. Electronprobe X-ray microanalysis showed that the precipitate contains Ca in a significant amount. These results indicate that the contraction of the LRM fibers is caused not only by Ca-influx but also by Ca-release from the intracellular storage sites, such as the subsarcolemmal vesicles and the inner surface of plasma membrane.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Atsumi S, Sugi H (1976) Localization of calcium-accumulating structures in the anterior byssal retractor muscle of Mytilus edulis and their role in the regulation of active and catch contraction. J Physiol (Lond) 257:549–560
Debbas G, Hoffman L, Landon EJ, Hurwitz L (1975) Electron microscopic localization of calcium in vascular smooth muscle. Anat Rec 182:447–472
Devine CE, Somlyo AV, Somlyo AP (1972) Sarcoplasmic reticulum and excitation-contraction coupling in mammalian smooth muscle. J Cell Biol 52:690–718
Ebashi S, Endo M (1968) Calcium ions and muscle contraction. Prog Biophys Mol Biol 18:123–183
Feinstein MB (1963) Inhibition of caffeine rigor and radio calcium movements by local anesthetic in frog sartorius muscle. J Gen Physiol 47:151–172
Fukuoka H, Takagi T, Nagai H, Hotta K, Suzuki S, Sugi H (1980) Localization and translocation of intracellular calcium in smooth muscle cells of bovine cerebral artery. J Electron Microsc 29:266–269
Goodford PJ, Wolowyk MW (1972) Localization of cation interactions in the smooth muscle of the guinea-pig taenia coli. J Physiol (Lond) 224:521–535
Hagiwara E, Nakajima T (1966) Difference in Na and Ca spikes as examined by application of tetrodotoxin, procaine, and manganese ions. J Gen Physiol 49:793–806
Hill RB, Sanger JW, Yantorono RE, Deutsch C (1978) Contraction in a muscle with negligible sarcoplasmic reticulum: The longitudinal retractor of the sea cucumber Isostichopus badionotus (Selenka), Holothuria Aspidochirota. J Exp Zool 206:137–150
Hurwitz L (1975) Some characteristics of the excitation-contraction coupling process in smooth muscle. In: Rochae Silva M, Suarez-Kurtz G (eds) Concepts of membranes in regulation and excitation. Raven Press, New York, pp 55–72
Jonas L, Zelck U (1974) The subcellular calcium distribution in the smooth muscle cells of the pig coronary artery. Exp Cell Res 89:352–358
Klein RL, Yen S-S, Thureson-Klein Å (1972) Critique on the K-pyroantimonate method for semiquantitative estimation of cations in conjunction with electron microscopy. J Histochem Cytochem 20:65–78
Mizuhira V (1976) Elemental analysis of biological specimens by electron probe X-ray microanalysis. Acta Histochem Cytochem 9:69–87
Oschman JL, Wall BL (1972) Calcium binding to intestine membrane. J Cell Biol 55:58–73
Prescott L, Brightman MW (1976) The sarcolemma of Aplysia smooth muscle in freeze-fracture preparation. Tissue Cell 9:241–258
Prosser CL, Mackie GO (1980) Contractions of holothurian muscles. J Comp Physiol 136:103–112
Russ JC (1974) The direct element ratio model for quantitative analysis of thin sections. In: Hall T, Echlin P, Kaufman R (eds) Microprobe analysis as applied to cells and tissues. Academic Press, New York, pp 269–276
russ JC (1977) Analyzing calcium in the presence of antimony. Edax Editor 7:18–20
Somlyo AP, Devine CE, Somlyo AV, North SR (1971) Sarcoplasmic reticulum and the temperature dependent contraction of smooth muscle in calcium-free solutions. J Cell Biol 51:722–741
Somlyo AP, Somlyo AV, Devine CE, Peters PD, Hall TA (1974) Electron microscopy and electron probe analysis of mitochondrial cation accumulation in smooth muscle. J Cell Biol 61:723–742
Sugi H, Atsumi S (1973) Localization of calcium-accumulating structures in the anterior byssal retractor muscle of Mytilus edulis and their role in excitation-contraction coupling. Proc Japan Acad 49:638–642
Sugi H, Daimon T (1977) Translocation of intracellularly stored calcium during the contractionrelaxation cycle in guinea-pig taenia coli. Nature (Lond) 269:436–438
Sugi H, Suzuki S (1978) Ultrastructural and physiological studies on the longitudinal body wall muscle of Dolabella auricularia. I. Mechanical response and ultrastructure. J Cell Biol 79:454–466
Sugi H, Yamaguchi T (1976) Activation of the contractile mechanism in the anterior byssal retractor muscle of Mytilus edulis. J Physiol (Lond) 257:531–547
Suzuki S (1978) Qualitative and semiquantitative X-ray microanalysis of pyroantimonte precipitates in molluscan smooth muscle, with special reference to the presence of calcium. Teikyo Med J 1:259–268
Suzuki S, Sugi H (1978) Ultrastructural and physiological studies on the longitudinal body wall muscle of Dolabella auricularia. II. Localization of intracellular calcium and its translocation during mechanical activity. J Cell Biol 79:467–478
Van Breemen C, Farinas BR, Casteels R, Gerba P, Wuytack F, Deth R (1973) Factors controlling cytoplasmic Ca2+ concentration. Phil Trans R Soc Lond B 265:57–71
Weber A, Herz R (1968) The relationship between caffeine contracture of intact muscle and the effect of caffeine on reticulum. J Gen Physiol 52:750–759
Zelck U, Jonas L, Wiegershausen B (1972) Ultrahistochemischer Nachweis von Calcium in glatten Muskelzellen der Arteria coronaria sinistra des Schweins. Acta Histochem 44:180–182
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Suzuki, S. Physiological and cytochemical studies on activator calcium in contraction by smooth muscle of a sea cucumber, Isostichopus badionotus . Cell Tissue Res. 222, 11–24 (1982). https://doi.org/10.1007/BF00218285
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00218285