Abstract
To investigate the controversial issue concerning the role of calponin in smooth muscle contraction, this study examined the relationship between smooth muscle calponin and the contraction of aortic rings from different strains of rats: Sprague-Dawley (SD), Wistar, and Wistar Kyoto (WKY). Western blot analysis demonstrated that h1- and h2-calponins are present in aortic smooth muscle from adult SD rats but not Wistar or WKY rats. Nevertheless, h1-calponin is detectable in stomach from Wistar rats, although at a much lower level compared with that in the SD rat stomach. This suggests that a repressed expression of the gene, instead of a simple null mutation, may have caused its absence from the aortic smooth muscle. Despite the presence or absence of calponin, the aortic smooth muscles from the different strains of rats all develop contractions in response to the physiological agonist norepinephrine (NE) and following activation with the plasma membrane receptor-independent NaF induction. The data indicate that h1- and h2-calponins are not essential for NE- and NaF-induced contractions in aortic smooth muscle. The calponin-positive adult SD rat aorta was found to be more sensitive in contractile response to NE and NaF inductions compared with the calponin-negative rat aortae. This may imply a potential modulator function of calponin in the contraction of smooth muscle, whereas other contractile protein isoform differences between these rat strains may also play a role.
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ABE, M., TAKAHASHI, K. & HIWADA, K. (1990) Effect of calponin on actin-activated myosin ATPase activity. J. Biochem. 108, 835–8.
ADAM, L. P., HAEBERLE, J. R. & HATHAWAY, D. R. (1995) Calponin is not phosphorylated during contractions of porcine carotid arteries. Am. J. Physiol. 268, C903–9.
ADEAGBO, A. S. & TRIGGLE, C. R. (1991) Mechanism of vascular smooth muscle contraction by sodium fluoride in the isolated aorta of rat and rabbit. J. Pharmacol. Exper. Therap. 258, 66–73.
ADEAGBO, A. S. & TRIGGLE, C. R. (1993) Interactions of nitric oxide synthase inhibitors and dexamethasone with a-adrenoceptor-mediated responses in rat aorta. Br. J. Pharmacol. 109, 495–501.
APPLEGATE, D., FENG, W., GREEN, R. S. & TAUBMAN, M. B. (1994) Cloning and expression of a novel acidic calponin isoform from rat aortic vascular smooth muscle. J. Biol. Chem. 269, 10683–90.
BÁRÁNY, M., ROKOLYA, A. & BÁRÁNY, K. (1991) Absence of calponin phosphorylation in contracting or resting arterial smooth muscle. FEBS Lett. 279, 65–8.
BOGATCHEVA, N. V. & GUSEV, N. (1995) Interaction of smooth muscle calponin with phospholipids. FEBS Lett. 371, 123–6.
CHILDS, T. J., WATSON, M. H., NOVY, R. E., LIN, J. J.-C. & MAK, A. S. (1992) Calponin and tropomyosin interaction. Biochem. Biophys. Acta 1121, 41–6.
DRAEGER, A., GIMONA, M., STUCKERT, A., CELIS, J. E. & SMALL, J. V. (1991) Calponin: developmental isoforms and low molecular weight variant. FEBS Lett. 291, 24–8.
EL-MEZGUELDI, M., STRASSER, P., FATTOUM, A. & GIMONA, M. (1996) Expressing functional domains of mouse calponin: involvement of the region around alanine 145 in the actomyosin ATPase inhibitory activity of calponin. Biochemistry 35, 3654–61.
FUJ II, T., HIROMORI, T., HAMAMOTO, M. & SUZUKI, T. (1997) Interaction of chicken gizzard smooth muscle calponin with brain microtubules. J. Biochem. 122, 344–51.
GAO, J., HWANG, J. M. & JIN, J.-P. (1996) Complete nucleotide sequence, structural organization and an alternative spliced exon of mouse h1-calponin gene. Biochem. Biophys. Res. Commun. 218, 292–7.
GIMONA, M., HERZOG, M., VANDEKERECKHOVE, J. & SMALL, J. V. (1990) Smooth muscle specific expression of calponin. FEBS Lett. 274, 159–62.
GIMONA, M., SPARROW, M. P., STRASSER, P., HERZOG, M. & SMALL, J. V. (1992) Calponin and SM 22 isoforms in avian and mammalian smooth muscle. Absence of phosphorylation in vivo. Eur. J. Biochem. 205, 1067–75.
GLUKHOVA, M. A., FRID, M. G. & KOTELIANSKY, V. E. (1990) Developmental changes in expression of contractile and cytoskeletal proteins in human aortic smooth muscle. J. Biol. Chem. 265, 13042–6.
GONG, M. C., IIZUKA, K., NIXON, G., BROWNE, J. P., HALL, A., ECCLESTON, J. F., SUGAI, M., KOBAYASHI, S., SOMLYO, A. V. & SOMLYO, A. P. (1996) Role of guanine nucleotide-binding proteins-ras-family or trimeric proteins or both-in Ca2+ sensitization of smooth muscle. Proc. Natl Acad. Sci. USA 93, 1340–45.
GRACEFFA, P., ADAM, L. P. & MORGAN, K. G. (1996) Strong interaction between caldesmon and calponin. J. Biol. Chem. 271, 30336–9.
HAEBERLE, J. R. (1994) Calponin decreases the rate of crossbridge cycling and increases maximum force production by smooth muscle myosin in an in vitro motility assay. J. Biol. Chem. 269, 12424–31.
HAI, C.-M. & MURPHY, R. A. (1988) Cross-bridge phosphorylation and regulation of latch state in smooth muscle. Am. J. Physiol. 254, C99-C106.
HARTSHORNE, D. J. (1987) Biochemistry of contractile process in smooth muscle. In Physiology of the Gastrointestinal Tract (2nd edn) (edited by JOHNSON, L. R.), pp. 423–82 New York: Raven Press.
HERLIHY, J. T. & MURPHY, R. A. (1973) Length-tension relationship of smooth muscle of the hog carotid artery. Circ. Res. 33, 275–83.
HORIUCHI, K. Y. & CHACKO, S. (1991) The mechanism for the inhibition of actin-activated ATPase of smooth muscle heavy meromyosin by calponin. Biochem. Biophys. Res. Commun. 176, 1487–93.
ITOH, T., SUZUKI, S., SUZUKI, A., NAKAMURA, F., NAKA, M. & TANAKA, T. (1994) Effects of exogenously applied calponin on Ca2+-regulated force in skinned smooth muscle of rabbit mesenteric artery. Eur. J. Physiol. 427, 301–8.
JAWOROWSKI, A., ANDERSON, K. I., ARNER, A., ENGSTROM, M., GIMONA, M., STRASSER, P. & SMALL, J. V. (1995) Calponin reduces shortening velocity in skinned taenia coli smooth muscle fibers. FEBS Lett. 365, 167–71.
JIANG, Z., GRANGE, R. W., WALSH, M. P., & KAMM, K. E. (1997) Adenovirus-mediated transfer of the smooth muscle cell calponin gene inhibits proliferation of smooth muscle cells and fibroblasts. FEBS Lett. 413, 441–5.
JIN, J.-P., WALSH, M. P., RESEK, M. R. & MCMARTIN, G. A. (1996) Expression and epitopic conservation of calponin in different smooth muscles and during development. Biochem. Cell Biol. 74, 187–96.
LEHMAN, W. (1991) Calponin and the composition of smooth muscle thin filaments. J. Muscle Res. Cell Motil. 12, 221–4.
LI, X.-F. & TRIGGLE, C. R. (1993) Effects of pertussis and cholera toxins on a-adrenoceptor function in rat tail artery: differences in hypertension. Can. J. Physiol. Pharmacol. 71, 791–9.
LIN, Y., YE, L.-H., ISHIKAWA, R., FUJITA, K. & KOHAMA, K. (1993) Stimulatory effect of calponin on myosin ATPase activity. J. Biochem. 113, 643–5.
MABUCHI, K., LI, B., IP, W. & TAO, T. (1997) Association of calponin with desmin intermediate filaments. J. Biol. Chem. 272, 22662–6.
MAKUCH, R., BIRUKOV, K., SHIRINSKY, V. & DABROWSKA, R. (1991) Functional interrelationship between calponin and caldesmon. Biochem. J. 280, 33–8.
MARSTON, S. B. & SMITH, C. W. J. (1985) The thin filaments of smooth muscles. J. Muscle. Res. Cell Motil. 6, 669–708.
MENICE, C. B., HULVERSHORN, J., ADAM, L. P., WANG, C.-L. A. & MORGAN, K. G. (1997) Calponin and mitogen-activated protein kinase signaling in differentiated vascular smooth muscle. J. Biol. Chem. 272, 25157–61.
MINO, T., YUASA, U., NAKA, M. & TANAKA, T. (1995) Phosphorylation of calponin mediated by protein kinase C in association with contraction in porcine coronary artery. Biochem. Biophys. Res. Commun. 208, 397–404.
NIGAM, R., TRIGGLE, C. R., RESEK, M. E., MCMARTIN, G. A. & JIN, J.-P. (1996) Relationships between expression of smooth muscle calponin and contraction of the developing rat aorta. Biophys. J. 70, A379.
NISHIDA, W., KITAMI, Y. & HIWADA, K. (1993) cDNA cloning and mRNA expression of calponin and SM22 in rat aorta smooth muscle cells. Gene 130, 297–302.
NORTH, A. J., GIMONA, M., CROSS, R. A. & SMALL, J. V. (1994) Calponin is localized in both the contractile apparatus and the cytoskeleton of smooth muscle cells. J. Cell Sci. 107, 437–44.
SHIRINSKY, V. P., BIRYNKOV, K. G., HETTACH, J. M. & SELLERS, J. R. (1992) Inhibition of the relative movement of actin and myosin by caldesmon and calponin. J. Biol. Chem. 267, 15886–992.
SOMLYO, A. P. & SOMLYO, A. V. (1994) Signal transduction and regulation in smooth muscle. Nature 372, 231–6.
STRASSER, P., GIMONA, M., HERBERT, M., HERZOG, M. & SMALL, J. V. (1993) Mammalian calponin: identification and expression of genetic variants. FEBS Lett. 330, 13–18.
STULL, J. T., GALLAGHER, J. P., HERRING, B. P. & KAMM, K. E. (1991) Vascular smooth muscle contractile elements: cellular regulation. Hypertension 17, 723–32.
SZYMANSKI, P. T. & TAO, T. (1993) Interaction between calponin and smooth muscle myosin. FEBS Lett. 331, 256–9.
TAKAHASHI, K., HIWADA, K. & KOKUBU, T. (1986) Isolation and characterization of a 34000-dalton calmodulinand F-actin-binding protein from chicken gizzard smooth muscle. Biochem. Biophys. Res. Commun. 141, 20–26.
TAKAHASHI, K., HIWADA, K. & KOKUBU, T. (1988) Vascular smooth muscle calponin. A novel troponin T-like protein. Hypertension 11, 620–26.
TAKAHASHI, K. & NADAL-GINARD, B. (1991) Molecular cloning and sequence analysis of smooth muscle calponin. J. Biol. Chem. 266, 13284–8.
TANG, D.-C., KANG, H.-M., JIN, J.-P., FRASER, E. D. & WALSH, M. P. (1996) Structure-function relations of smooth muscle calponin: the critical role of serine-175. J. Biol. Chem. 271, 8605–11.
TRABELSI-TERZIDIS, H., FATTOUM, A., REPRESA, A., DESSI, F., BEN-ARI, Y. & DER TERROSSIAN, E. (1995) Expression of an acidic isoform of calponin in rat brain: Western blot on one-or two-dimensional gels and immunolocalization in cultured cells. Biochem. J. 306, 211–15.
UEKI, N., SOBUE, K., KANDA, K., HADA, T. & HIGASHINO, K. (1987) Expression of high and low molecular weight caldesmons during phenotypic modulation of smooth muscle cells. Proc. Natl Acad. Sci. USA 84, 9049–53.
WALSH, M. P. (1991) Calcium-dependent mechanisms of regulation of smooth muscle contraction. Biochem. Cell Biol. 69, 771–800.
WINDER, S. J. & WALSH, M. P. (1990) Smooth muscle calponin. Inhibition of actomyosin MgATPase and regulation by phosphorylation. J. Biol. Chem. 265, 10148–55.
WINDER, S. J., ALLEN, B. G., FRASER, E. D., KANG, H.-M., KARGACIN, G. J. & WALSH, M. P. (1993) Calponin phosphorylation in in vitro and intact muscle. Biochem. J. 296, 827–36.
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Nigam, R., Jin, JP. & Triggle, C.R. h1- and h2-calponins are not essential for norepinephrine- or sodium fluoride-induced contraction of rat aortic smooth muscle. J Muscle Res Cell Motil 19, 695–703 (1998). https://doi.org/10.1023/A:1005389300151
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DOI: https://doi.org/10.1023/A:1005389300151