Biopolym. Cell. 1996; 12(1):16-28.
Caldesmon and calponin – the thin filamentassociated proteins of smooth muscle: structure and mechanisms of functioning
1Danilova V. M., 1Kulikova N. V.
  1. Petr Bogach Institute of Physiology
    Taras Shevchenko National University of Kyiv
    2, Academika Glushkova Ave Str., Kyiv, Ukraine, 03187

Abstract

The structure and properties of two novel smooth muscle regulatory proteins associated with thin filament arereviewed. A detailed description of the «heavy» caldes man isofarm and of the localization of ca Ides man interaction sites withactin, calmodulin, tropomyosin and myosin are given. Current conceptions concerning the mechanism ofcaldcsmon and calponin function during regulation of myosin interaction with actin are considered.

References

[1] Sobue K, Muramoto Y, Fujita M, Kakiuchi S. Purification of a calmodulin-binding protein from chicken gizzard that interacts with F-actin. Proc Natl Acad Sci U S A. 1981;78(9):5652-5.
[2] Bretscher A, Lynch W. Identification and localization of immunoreactive forms of caldesmon in smooth and nonmuscle cells: a comparison with the distributions of tropomyosin and alpha-actinin. J Cell Biol. 1985;100(5):1656-63.
[3] Graceffa P, Wang CL, Stafford WF. Caldesmon. Molecular weight and subunit composition by analytical ultracentrifugation. J Biol Chem. 1988;263(28):14196-202.
[4] Kakiuchi R, Inui M, Morimoto K, Kanda K, Sobue K, Kakiuchi S. Caldesmon, a calmodulin-binding, F actin-interacting protein, is present in aorta, uterus and platelets. FEBS Lett. 1983;154(2):351-6.
[5] Lash JA, Haeberle JR, Hathaway DR. Vascular smooth muscle caldesmon: actin-binding properties and effects on skeletal muscle acto-HMM ATPase activity. Biophys J. 1985; 47: 187a.
[6] Sobue K, Tanaka T, Kanda K, Ashino N, Kakiuchi S. Purification and characterization of caldesmon77: a calmodulin-binding protein that interacts with actin filaments from bovine adrenal medulla. Proc Natl Acad Sci U S A. 1985;82(15):5025-9.
[7] Takahashi K, Hiwada K, Kokubu T. Isolation and characterization of a 34,000-dalton calmodulin- and F-actin-binding protein from chicken gizzard smooth muscle. Biochem Biophys Res Commun. 1986;141(1):20-6.
[8] F?rst DO, Cross RA, De Mey J, Small JV. Caldesmon is an elongated, flexible molecule localized in the actomyosin domains of smooth muscle. EMBO J. 1986;5(2):251-7.
[9] Lynch WP, Riseman VM, Bretscher A. Smooth muscle caldesmon is an extended flexible monomeric protein in solution that can readily undergo reversible intra- and intermolecular sulfhydryl cross-linking. A mechanism for caldesmon's F-actin bundling activity. J Biol Chem. 1987;262(15):7429-37.
[10] Moody C, Lehman W, Craig R. Caldesmon and the structure of smooth muscle thin filaments: electron microscopy of isolated thin filaments. J Muscle Res Cell Motil. 1990;11(2):176-85.
[11] Mabuchi K, Wang CL. Electron microscopic studies of chicken gizzard caldesmon and its complex with calmodulin. J Muscle Res Cell Motil. 1991;12(2):145-51.
[12] Hayashi K, Kanda K, Kimizuka F, Kato I, Sobue K. Primary structure and functional expression of h-caldesmon complementary DNA. Biochem Biophys Res Commun. 1989;164(1):503-11.
[13] Bryan J, Lee R. Sequence of an avian non-muscle caldesmon. J Muscle Res Cell Motil. 1991;12(4):372-5.
[14] Dingus J, Hwo S, Bryan J. Identification by monoclonal antibodies and characterization of human platelet caldesmon. J Cell Biol. 1986;102(5):1748-57.
[15] Hayashi K, Fujio Y, Kato I, Sobue K. Structural and functional relationships between h- and l-caldesmons. J Biol Chem. 1991;266(1):355-61.
[16] Novy RE, Lin JL, Lin JJ. Characterization of cDNA clones encoding a human fibroblast caldesmon isoform and analysis of caldesmon expression in normal and transformed cells. J Biol Chem. 1991;266(25):16917-24.
[17] Marston SB, Redwood CS. The molecular anatomy of caldesmon. Biochem J. 1991;279 ( Pt 1):1-16.
[18] Haeberle JR, Hathaway DR, Smith CL. Caldesmon content of mammalian smooth muscles. J Muscle Res Cell Motil. 1992;13(1):81-9.
[19] Horiuchi KY, Chacko S. Interaction between caldesmon and tropomyosin in the presence and absence of smooth muscle actin. Biochemistry. 1988;27(22):8388-93.
[20] Yamashiro-Matsumura S, Matsumura F. Characterization of 83-kilodalton nonmuscle caldesmon from cultured rat cells: stimulation of actin binding of nonmuscle tropomyosin and periodic localization along microfilaments like tropomyosin. J Cell Biol. 1988;106(6):1973-83.
[21] Bartegi A, Fattoum A, Derancourt J, Kassab R. Characterization of the carboxyl-terminal 10-kDa cyanogen bromide fragment of caldesmon as an actin-calmodulin-binding region. J Biol Chem. 1990;265(25):15231-8.
[22] Fujii T, Imai M, Rosenfeld GC, Bryan J. Domain mapping of chicken gizzard caldesmon. J Biol Chem. 1987;262(6):2757-63.
[23] Redwood CS, Marston SB. Binding and regulatory properties of expressed functional domains of chicken gizzard smooth muscle caldesmon. J Biol Chem. 1993;268(15):10969-76.
[24] Szpacenko A, Dabrowska R. Functional domain of caldesmon. FEBS Lett. 1986;202(2):182-6.
[25] Yazawa M, Yagi K, Sobue K. Isolation and characterization of a calmodulin binding fragment of chicken gizzard caldesmon. J Biochem. 1987;102(5):1065-73.
[26] Katayama E, Horiuchi KY, Chacko S. Characteristics of the myosin and tropomyosin binding regions of the smooth muscle caldesmon. Biochem Biophys Res Commun. 1989;160(3):1316-22.
[27] Leszyk J, Mornet D, Audemard E, Collins JH. Amino acid sequence of a 15 kilodalton actin-binding fragment of turkey gizzard caldesmon: similarity with dystrophin, tropomyosin and the tropomyosin-binding region of troponin T. Biochem Biophys Res Commun. 1989;160(1):210-6.
[28] Zhan QQ, Wong SS, Wang CL. A calmodulin-binding peptide of caldesmon. J Biol Chem. 1991;266(32):21810-4.
[29] Czury?o EA, Venyaminov SYu, Dabrowska R. Studies on secondary structure of caldesmon and its C-terminal fragments. Biochem J. 1993;293 ( Pt 2):363-8.
[30] Dabrowska R. Actin and thin-filament-associated proteins in smooth muscle. Airways smooth muscle: Biochcmical control of contraction nad relaxation. Eds D. Raeburn, AA. Giembycz. Switzerland: Birkhauser Verlag, 1994: 31-59.
[31] Velaz L, Ingraham RH, Chalovich JM. Dissociation of the effect of caldesmon on the ATPase activity and on the binding of smooth heavy meromyosin to actin by partial digestion of caldesmon. J Biol Chem. 1990;265(5):2929-34.
[32] Bretscher A. Smooth muscle caldesmon. Rapid purification and F-actin cross-linking properties. J Biol Chem. 1984;259(20):12873-80.
[33] Makuch R, Walsh MP, Dabrowska R. Location of the calmodulin- and actin-binding domains at the C-terminus of caldesmon. FEBS Lett. 1989;247(2):411-4.
[34] Makuch R, Kulikova N, Graziewicz MA, Nowak E, Dabrowska R. Polymerization of actin induced by actin-binding fragments of caldesmon. Biochim Biophys Acta. 1994;1206(1):49-54.
[35] Ga?azkiewicz B, Mossakowska M, Osi?ska H, Dabrowska R. Polymerization of G-actin by caldesmon. FEBS Lett. 1985;184(1):144-9.
[36] Leszyk J, Mornet D, Audemard E, Collins JH. Caldesmon structure and function: sequence analysis of a 35 kilodalton actin- and calmodulin-binding fragment from the C-terminus of the turkey gizzard protein. Biochem Biophys Res Commun. 1989;160(3):1371-8.
[37] Riseman VM, Lynch WP, Nefsky B, Bretscher A. The calmodulin and F-actin binding sites of smooth muscle caldesmon lie in the carboxyl-terminal domain whereas the molecular weight heterogeneity lies in the middle of the molecule. J Biol Chem. 1989;264(5):2869-75.
[38] Wang CL, Wang LW, Xu SA, Lu RC, Saavedra-Alanis V, Bryan J. Localization of the calmodulin- and the actin-binding sites of caldesmon. J Biol Chem. 1991;266(14):9166-72.
[39] Fujii T, Ozawa J, Ogoma Y, Kondo Y. Interaction between chicken gizzard caldesmon and tropomyosin. J Biochem. 1988;104(5):734-7.
[40] Graceffa P. Evidence for interaction between smooth muscle tropomyosin and caldesmon. FEBS Lett. 1987;218(1):139-42.
[41] Smith CW, Pritchard K, Marston SB. The mechanism of Ca2+ regulation of vascular smooth muscle thin filaments by caldesmon and calmodulin. J Biol Chem. 1987;262(1):116-22.
[42] Sutherland C, Walsh MP. Phosphorylation of caldesmon prevents its interaction with smooth muscle myosin. J Biol Chem. 1989;264(1):578-83.
[43] Lash JA, Sellers JR, Hathaway DR. The effects of caldesmon on smooth muscle heavy actomeromyosin ATPase activity and binding of heavy meromyosin to actin. J Biol Chem. 1986;261(34):16155-60.
[44] Marston SB. A tight-binding interaction between smooth-muscle native thin filaments and heavy meromyosin in the presence of MgATP. Biochem J. 1989;259(1):303-6.
[45] Takahashi K, Hiwada K, Kokubu T. Occurrence of anti-gizzard P34K antibody cross-reactive components in bovine smooth muscles and non-smooth muscle tissues. Life Sci. 1987;41(3):291-6.
[46] Takeuchi K, Takahashi K, Abe M, Nishida W, Hiwada K, Nabeya T, Maruyama K. Co-localization of immunoreactive forms of calponin with actin cytoskeleton in platelets, fibroblasts, and vascular smooth muscle. J Biochem. 1991;109(2):311-6.
[47] Takahashi K, Abe M, Hiwada K, Kokubu T. A novel troponin T-like protein (calponin) in vascular smooth muscle: interaction with tropomyosin paracrystals. J Hypertens Suppl. 1988;6(4):S40-3.
[48] Takahashi K, Nadal-Ginard B. Molecular cloning and sequence analysis of smooth muscle calponin. J Biol Chem. 1991;266(20):13284-8.
[49] Mezgueldi M, Fattoum A, Derancourt J, Kassab R. Mapping of the functional domains in the amino-terminal region of calponin. J Biol Chem. 1992;267(22):15943-51.
[50] Vancompernolle K, Gimona M, Herzog M, Van Damme J, Vandekerckhove J, Small V. Isolation and sequence of a tropomyosin-binding fragment of turkey gizzard calponin. FEBS Lett. 1990;274(1-2):146-50.
[51] Stafford WF 3rd, Mabuchi K, Takahashi K, Tao T. Physical properties of calponin. Biophys J. 1993;64:A31.
[52] Marston SB. The regulation of smooth muscle contractile proteins. Prog Biophys Mol Biol. 1983;41(1):1-41.
[53] Walsh MP. The Ayerst Award Lecture 1990. Calcium-dependent mechanisms of regulation of smooth muscle contraction. Biochem Cell Biol. 1991;69(12):771-800. Review.
[54] Marston SB, Smith CW. The thin filaments of smooth muscles. J Muscle Res Cell Motil. 1985;6(6):669-708. Review.
[55] Danilova VM, Kulikova NV, Tregubov VS, Omelyanuk VS, Filenko AM. Caldesmon is a Ca2+-regulatory protein component of native aorta smooth muscle filaments. Biopolym Cell. 1995; 11(5):28-36.
[56] Abe M, Takahashi K, Hiwada K. Effect of calponin on actin-activated myosin ATPase activity. J Biochem. 1990;108(5):835-8.
[57] Dabrowska R, Goch A, Ga?azkiewicz B, Osi?ska H. The influence of caldesmon on ATPase activity of the skeletal muscle actomyosin and bundling of actin filaments. Biochim Biophys Acta. 1985;842(1):70-5.
[58] Ngai PK, Walsh MP. Inhibition of smooth muscle actin-activated myosin Mg2+-ATPase activity by caldesmon. J Biol Chem. 1984;259(22):13656-9.
[59] Sobue K, Morimoto M, Iuui M. et al. Control of actin-myosin interaction of gizzard smooth muscle by calmodulin- and caldesmon-linked flip-flop mechanism. Biomed Res. 1982; 3: 188-96.
[60] Winder SJ, Walsh MP. Smooth muscle calponin. Inhibition of actomyosin MgATPase and regulation by phosphorylation. J Biol Chem. 1990;265(17):10148-55.
[61] Haeberle JR, Trybus KM, Hemric ME, Warshaw DM. The effects of smooth muscle caldesmon on actin filament motility. J Biol Chem. 1992;267(32):23001-6.
[62] Shirinsky VP, Biryukov KG, Hettasch JM, Sellers JR. Inhibition of the relative movement of actin and myosin by caldesmon and calponin. J Biol Chem. 1992;267(22):15886-92.
[63] Ikebe M, Hornick T. Determination of the phosphorylation sites of smooth muscle caldesmon by protein kinase C. Arch Biochem Biophys. 1991;288(2):538-42.
[64] Scott-Woo GC, Sutherland C, Walsh MP. Kinase activity associated with caldesmon is Ca2+/calmodulin-dependent kinase II. Biochem J. 1990;268(2):367-70.
[65] Umekawa H, Hidaka H. Phosphorylation of caldesmon by protein kinase C. Biochem Biophys Res Commun. 1985;132(1):56-62.
[66] Winder SJ, Walsh MP. Structural and functional characterization of calponin fragments. Biochem Int. 1990;22(2):335-41.
[67] Adams S, DasGupta G, Chalovich JM, Reisler E. Immunochemical evidence for the binding of caldesmon to the NH2-terminal segment of actin. J Biol Chem. 1990;265(32):19652-7.
[68] Bartegi A, Fattoum A, Kassab R. Cross-linking of smooth muscle caldesmon to the NH2-terminal region of skeletal F-actin. J Biol Chem. 1990;265(4):2231-7.
[69] Levine BA, Moir AJ, Audemard E, Mornet D, Patchell VB, Perry SV. Structural study of gizzard caldesmon and its interaction with actin. Binding involves residues of actin also recognised by myosin subfragment 1. Eur J Biochem. 1990;193(3):687-96.
[70] Ga?azkiewicz B, Belagyi J, Dabrowska R. The effect of caldesmon on assembly and dynamic properties of actin. Eur J Biochem. 1989;181(3):607-14.
[71] Harricane MC, Fabbrizio E, Arpin C, Mornet D. Involvement of caldesmon at the actin-myosin interface. Biochem J. 1992;287 ( Pt 2):633-7.
[72] Nowak E, Borovikov YS, Dabrowska R. Caldesmon weakens the bonding between myosin heads and actin in ghost fibers. Biochim Biophys Acta. 1989;999(3):289-92.
[73] Brenner B, Yu LC, Chalovich JM. Parallel inhibition of active force and relaxed fiber stiffness in skeletal muscle by caldesmon: implications for the pathway to force generation. Proc Natl Acad Sci U S A. 1991;88(13):5739-43.
[74] Chalovich JM, Yu LC, Brenner B. Involvement of weak binding crossbridges in force production in muscle. J Muscle Res Cell Motil. 1991;12(6):503-6.
[75] Marston S. Aorta caldesmon inhibits actin activation of thiophosphorylated heavy meromyosin Mg2+-ATPase activity by slowing the rate of product release. FEBS Lett. 1988;238(1):147-50.
[76] Marston SB, Redwood CS. Inhibition of actin-tropomyosin activation of myosin MgATPase activity by the smooth muscle regulatory protein caldesmon. J Biol Chem. 1992;267(24):16796-800.
[77] Horiuchi KY, Samuel M, Chacko S. Mechanism for the inhibition of acto-heavy meromyosin ATPase by the actin/calmodulin binding domain of caldesmon. Biochemistry. 1991;30(3):712-7.
[78] Miki M, Walsh MP, Hartshorne DJ. The mechanism of inhibition of the actin-activated myosin MgATPase by calponin. Biochem Biophys Res Commun. 1992;187(2):867-71.
[79] Vancompernolle K, Vandekerckhove J, Bubb MR, Korn ED. The interfaces of actin and Acanthamoeba actobindin. Identification of a new actin-binding motif. J Biol Chem. 1991;266(23):15427-31.
[80] Kabsch W, Mannherz HG, Suck D, Pai EF, Holmes KC. Atomic structure of the actin:DNase I complex. Nature. 1990;347(6288):37-44.
[81] Horiuchi KY, Chacko S. The mechanism for the inhibition of actin-activated ATPase of smooth muscle heavy meromyosin by calponin. Biochem Biophys Res Commun. 1991;176(3):1487-93.
[82] Pritchard K, Marston SB. Ca2+-calmodulin binding to caldesmon and the caldesmon-actin-tropomyosin complex. Its role in Ca2+ regulation of the activity of synthetic smooth-muscle thin filaments. Biochem J. 1989;257(3):839-43.
[83] Pritchard K, Marston SB. The Ca(2+)-sensitizing component of smooth muscle thin filaments: properties of regulatory factors that interact with caldesmon. Biochem Biophys Res Commun. 1993;190(2):668-73.
[84] Mani RS, McCubbin WD, Kay CM. Calcium-dependent regulation of caldesmon by an 11-kDa smooth muscle calcium-binding protein, caltropin. Biochemistry. 1992;31(47):11896-901.
[85] Tanaka T, Ohta H, Kanda K, Tanaka T, Hidaka H, Sobue K. Phosphorylation of high-Mr caldesmon by protein kinase C modulates the regulatory function of this protein on the interaction between actin and myosin. Eur J Biochem. 1990;188(3):495-500.
[86] Pinter K, Marston SB. Phosphorylation of vascular smooth muscle caldesmon by endogenous kinase. FEBS Lett. 1992;305(3):192-6.
[87] Yamashiro S, Yamakita Y, Hosoya H, Matsumura F. Phosphorylation of non-muscle caldesmon by p34cdc2 kinase during mitosis. Nature. 1991;349(6305):169-72.
[88] Mak AS, Watson MH, Litwin CM, Wang JH. Phosphorylation of caldesmon by cdc2 kinase. J Biol Chem. 1991;266(11):6678-81.
[89] Winder SJ, Pato MD, Walsh MP. Purification and characterization of calponin phosphatase from smooth muscle. Effect of dephosphorylation on calponin function. Biochem J. 1992;286 ( Pt 1):197-203.
[90] Pohl J, Walsh MP, Gerthoffer WT. Calponin and caldesmon phosphorylation in canine tracheal smooth muscle. Biophys J. 1991; 59: 58a.
[91] B?r?ny M, Rokolya A, B?r?ny K. Absence of calponin phosphorylation in contracting or resting arterial smooth muscle. FEBS Lett. 1991;279(1):65-8.
[92] Gimona M, Sparrow MP, Strasser P, Herzog M, Small JV. Calponin and SM 22 isoforms in avian and mammalian smooth muscle. Absence of phosphorylation in vivo. Eur J Biochem. 1992;205(3):1067-75.
[93] Szpacenko A, Wagner J, Dabrowska R, R?egg JC. Caldesmon-induced inhibition of ATPase activity of actomyosin and contraction of skinned fibres of chicken gizzard smooth muscle. FEBS Lett. 1985;192(1):9-12.
[94] Taggart MJ, Marston SB. The effects of vascular smooth muscle caldesmon on force production by 'desensitised' skeletal muscle fibres. FEBS Lett. 1988;242(1):171-4.
[95] Marston SB. What is latch? New ideas about tonic contraction in smooth muscle. J Muscle Res Cell Motil. 1989;10(2):97-100.
[96] Ikebe M, Reardon S. Binding of caldesmon to smooth muscle myosin. J Biol Chem. 1988;263(7):3055-8.
[97] Walsh MP, Sutherland C. A model for caldesmon in latch-bridge formation in smooth muscle. Adv Exp Med Biol. 1989;255:337-46.
[98] McDaniel NL, Rembold CM, Murphy RA. Covalent cross-bridge regulation in smooth muscle. Ann N Y Acad Sci. 1990;599:66-74.
[99] Sobue K, Kanda K, Tanaka T, Ueki N. Caldesmon: a common actin-linked regulatory protein in the smooth muscle and nonmuscle contractile system. J Cell Biochem. 1988;37(3):317-25.
[100] Shirinsky VP, Biryukov KG, Vorotnikov AV, Gusev NB. Caldesmon150, caldesmon77 and skeletal muscle troponin T share a common antigenic determinant. FEBS Lett. 1989;251(1-2):65-8.
[101] Chalovich JM. Caldesmon and thin-filament regulation of muscle contraction. Cell Biophys. 1988;12:73-85.
[102] Sobue K, Sellers JR. Caldesmon, a novel regulatory protein in smooth muscle and nonmuscle actomyosin systems. J Biol Chem. 1991;266(19):12115-8.
[103] Takahashi K, Hiwada K, Kokubu T. Vascular smooth muscle calponin. A novel troponin T-like protein. Hypertension. 1988;11(6 Pt 2):620-6.
[104] Marston S, Pritchard K, Redwood C, Taggart M. Ca2+ regulation of the thin filaments: biochemical mechanism and physiological role. Biochem Soc Trans. 1988;16(4):494-7.
[105] Ngai PK, Walsh MP. The effects of phosphorylation of smooth-muscle caldesmon. Biochem J. 1987;244(2):417-25.
[106] Lehman W, Craig R, Lui J, Moody C. Caldesmon and the structure of smooth muscle thin filaments: immunolocalization of caldesmon on thin filaments. J Muscle Res Cell Motil. 1989;10(2):101-12.
[107] Nishida W, Abe M, Takahashi K, Hiwada K. Do thin filaments of smooth muscle contain calponin? A new method for the preparation. FEBS Lett. 1990;268(1):165-8.
[108] Gimona M, Herzog M, Vandekerckhove J, Small JV. Smooth muscle specific expression of calponin. FEBS Lett. 1990;274(1-2):159-62.
[109] Birukov KG, Shirinsky VP, Vorotnikov AV, Gusev NB. Competitive binding of the troponin T-specific pool of caldesmon antibodies and tropomyosin to skeletal troponin T and smooth muscle caldesmon. FEBS Lett. 1990;262(2):263-5.
[110] Marston SB, Smith CW. Purification and properties of Ca2+-regulated thin filaments and F-actin from sheep aorta smooth muscle. J Muscle Res Cell Motil. 1984;5(5):559-75.