Abstract
Microfilaments are intimately involved in the morphological alterations observed both in cell transformation and mitosis. In both cases, microfilamenets show significant re-organization. While “normal” cells with well-spread morphologies have numerous bundles of microfilaments, transformed cells with rounded morphologies show dispersed microfilament patterns1. These changes in the structure of actin cables, as well as in substrate adhesion, are closely coupled with proliferation in both normal and transformed cells1, suggesting that the microfilament cytoskeleton may play an important role in oncogenic transformation. The process of cell division causes similar alterations in microfilament patterns to those seen in transformed cells. Microfilament bundles disassemble when cells become rounded-up during prophase2,3 resulting in a cytoarchitecture resembling the dispersed microfilament patterns seen in the many transformed cell types which exhibit rounded morphologies. Microfilament bundles that are anchored to focal contacts are also disrupted in both mitotic and transformed cells, causing reduced adhesion of such cells to their substrates. These observations suggest that cell transformation and cell division control are intimately related, not just superficially, but at the level of molecular control.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
R Pollack, M Osborn, and K Weber, Patterns of organization of actin and myosin in normal and transformed cultured cells, Proc. Natl. Acad. Sci. U. S. A. 72: 994 (1975).
JW Sanger, JM Sanger Actin localization during cell division. in: Cell Motility R Goldman, T Pollard, J Rosenbaum, eds., Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, 1295.(1976)
TE Schroeder Actin in dividing cells: evidence for its role in cleavage but not mitosis. in: Cell Motility R Goldman, T Pollard, J Rosenbaum, eds., Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, 265. (1976)
S Yamashiro, Y Yamakita, R Ishikawa, and F Matsumura, Mitosis-specific phosphorylation causes 83K non-muscle caldesmon to dissociate from microfilaments, Nature 344: 675 (1990).
RE Novy, JL Lin, and JJ Lin, Characterization of cDNA clones encoding a human fibroblast caldesmon isoform and analysis of caldesmon expression in normal and transformed cells, J. Biol. Chem. 266: 16917 (1991).
M Koji-Owada, A Hakura, K Iida, I Yahara, K Sobue, and S Kakiuchi, Occurrence of caldesmon (a calmodulin-binding protein) in cultured cells: Comparison of normal and transformed cells, Proc. Natl. Acad. Sci. USA 81: 3133 (1984).
K Sobue and JR Sellers, Caldesmon, a novel regulatory protein in smooth muscle and nonmuscle actomyosin systems, J. Biol. Chem. 266: 12115 (1991).
R Ishikawa, S Yamashiro, and F Matsumura, Differential modulation of actin-severing activity of gelsolin by multiple isoforms of cultured rat cell tropomyosin. Potentiation of protective ability of tropomyosins by 83-kDa nonmuscle caldesmon, J. Biol. Chem. 264: 7490 (1989).
R Ishikawa, S Yamashiro, and F Matsumura, Annealing of gelsolin-severed actin fragments by tropomyosin in the presence of Ca2+. Potentiation of the annealing process by caldesmon, J. Biol. Chem. 264: 16764 (1989).
K Sobue, Y Muramoto, M Fujita, and S Kakiuchi, Purification of a calmodulin-binding protein from chicken gizzard that interacts with F-actin, Proc. Natl. Acad. Sci. USA 78: 5652 (1981).
A Bretscher and W Lynch, 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. 100: 1656 (1985).
PE Hoar, WGL Kerrick, and PS Cassidy, Chicken Gizzard: Relation between calciumactivated phosphorylation and contraction, Science 204: 503 (1979).
F Matsumura and S Yamashiro-Matsumura, Purification and characterization of multiple isoforms of tropomyosin from rat cultured cells, J. Biol. Chem. 260: 13851 (1985).
K Sobue, T Tanaka, K Kanda, N Ashino, and S Kakiushi, Purification and characterization of caldesmon 77: a calmodulin-binding protein that interacts with actin frilaments from bovine adrenal medulla, Proc. Natl. Acad. Sci. USA 82: 5025 (1985).
S Yamashiro-Matsumura, R Ishikawa, and F Matsumura, Purification and characterization of 83 kDa nonmuscle caldesmon from cultured rat cells: Changes in its expression upon L6 myogenesis, Protoplasma Suppl. 2: 9 (1988).
Y Yamakita, S Yamashiro, and F Matsumura, Microinjection of nonmuscle and smooth muscle caldesmon into fibroblasts and muscle cells, J. Cell Biol. 111: 2487 (1990).
J Bryan, M Imai, R Lee, P Moore, RG Cook, and WG Lin, Cloning and expression of a smooth muscle caldesmon, J. Biol. Chem. 264: 13873 (1989).
K Hayashi, Y Fujio, I Kato, and K Sobue, Structural and functional relationships between h-and 1-caldesmons, J. Biol. Chem. 266: 355 (1991).
T Fujii, M Imai, GC Rosenfeld, and J Bryan, Domain mapping of chicken gizzard caldesmon, J. Biol. Chem. 262: 2757 (1987).
VM Riseman, WP Lynch, B Nefsky, and A Bretscher, 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. 264: 2869 (1989).
M Urban:c:ikov: a and M Gröfov:a, Quantitative changes of tropomyosin synthesis in RSV-transformed mammalian cells in comparison with normal fibroblasts, Neoplasma. 29: 655 (1982).
CW Smith, K Pritchard, and SB Marston, The mechanism of Ca2+ regulation of vascular smooth muscle thin filaments by caldesmon and calmodulin, J. Biol. Chem. 262: 116 (1987).
DB Sacks and JM McDonald, Effects of cationic polypeptides on the activity, substrate interaction, and autophosphorylation of casein kinase II: a study with calmodulin, Arch. Biochem. Biophys. 299: 275 (1992).
KY Horiuchi, H Miyata, and S Chacko, Modulation of smooth muscle actomyosin ATPase by thin filament associated proteins, Biochem. Biophys. Res. Commun. 136: 962 (1986).
R Dabrowska, A Goch, B Galazkiewiecz, and H Osinska, The infuluence of caldesmon on ATPase activity of the skeletal muscle actomyosin and bundling of actin filaments, Biochim. Biophys. Acta 842: 70 (1985).
ME Hemric and JM Chalovich, Effect of caldesmon on the ATPase activity and the binding of smooth and skeletal myosin subfragments to actin, J. Biol. Chem. 263: 1878 (1988).
B Galazkiewicz, J Belagyi, and R Dabrowska, The effect of caldesmon on assembly and dynamic properties of actin, Eur. J. Biochem. 181: 607 (1989).
B Galazkiewicz, F Buss, BM Jockusch, and R Dabrowska, Caldesmon-induced polymerization of actin from profilactin, Eur. J. Biochem. 195: 543 (1991).
I Mabuchi and M Okuno, The effect of myosin antibody on the division of starfish blastomeres, J. Cell Biol. 74: 251 (1977).
D Knecht and WF Loomis, Antisense RNA inactivation of myosin heavy chain gene expression in Dictyostelium discoideum, Science 236: 1081 (1987).
A DeLozanne and JA Spudich, Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination, Science 236: 1086 (1987).
LA Shuvalova, MV Ostrovskaia, EA Sosunov, and VV Lednev, The effect of a weak magnetic field in the paramagnetic resonance mode on the rate of the calmodulin-dependent phosphorylation of myosin in solution, Dokl. Akad. Nauk. SSSR. 317: 227 (1991).
M Peter, J Nakagawa, M Doree, JC Labbe, and EA Nigg, In vitro disassemblyu of the nuclear lamina and M-phase specific phosphorylation of lamins by cdc2 kinase, Cell 61: 591 (1990).
Y-H Chou, JR Bischott, D Beach, and RD Goldman, Intermediate filament reorganization during mitosis is mediated by p34cdc2; Phosphorylation of vimentin, Cell 62: 1063 (1990).
F Matsumura and S Yamashiro-Matsumura, Modulation of actin-bundling activity of 55-kDa protein by multiple isoforms of tropomyosin, J. Biol. Chem. 261: 4655 (1986).
N Hosoya, H Hosoya, S Yamashiro, H Mohri, and F Matsumura, Localization of caldesmon and its dephosphorylation during cell division, J. Cell Biol. 121: 1075 (1993).
CL Wang, LW Wang, SA Xu, RC Lu, V Saavedra-Alanis, and J Bryan, Localization of the calmodulin-and the actin-binding sites of caldesmon, J. Biol. Chem. 266: 9166 (1991).
F Matsumura and S Yamashiro-Matsumura, Tropomyosin in cell transformation, Cancer Rev. 6: 21 (1986).
F Matsumura and S Yamashiro-Matsumura, Purification and characterization of multiple isoforms of tropomyosin from rat cultured cells, J. Biol. Chem. 260: 13851 (1985).
K Sobue, K Takahashi, and I Wakabayashi, Caldesmon 150 regulates the tropomyosin-enhanced actin-myosin interaction in gizzard smooth muscle, Biochem. Biophys. Res. Commun. 132: 645 (1985).
K Pritchard and SB Marston, 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. 257: 839 (1989).
Y Yamakita, S Yamashiro, and F Matsumura, Characterization of mitotically phosphorylated caldesmon, J. Biol Chem. 267: 12022 (1992).
F Matsumura, JJ-C Lin, S Yamashiro-Matsumura, GP Thomas, and WC Topp, Differential expression of tropomyosin forms in the microfilament isolated from normal and transformed rat cultured cells, J. Biol Chem. 258: 13954 (1983).
F Matsumura, S Yamashiro-Matsumura, and JJ-C Lin, Isolation and characterization of tropomyosin-containing microfilaments from cultured cells, J. Biol. Chem. 258: 6636 (1983).
JJ-C Lin, S Yamashiro-Matsumura, F Matsumura Microfilaments in normal and transformed cells: Changes in the multiple forms of tropomyosin. in: Cancer Cells. I A Levine, G Vande Woude, WC Topp, J Watson, eds., Cold Spring Harbor Laboratory, New York, 57. (1984)
M Hendricks and H Weintraub, Multiple tropomyosin polypeptides in chicken embryo fibroblasts: differential repression of transcription by Rous sarcoma virus transformation, Mol Cell Biol. 4: 1823 (1984).
M Hendricks and H Weintraub, Tropomyosin is decreased in transformed cells, Proc. Natl. Acad. Sci. U. S. A. 78: 5633 (1981).
CL Leonardi, RH Warren, and RW Rubin, Lack of tropomyosin correlates with the absence of stress fibers in transformed rat kidney cells, Biochim. Biophys. Acta 720: 154 (1982).
JJ Lin, DM Helfman, SH Hughes, and CS Chou, Tropomyosin isoforms in chicken embryo fibroblasts: purification, characterization, and changes in Rous sarcoma virus-transformed cells, J. Cell Biol. 100: 692 (1985).
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1994 Springer Science+Business Media New York
About this chapter
Cite this chapter
Yamashiro, S., Yoshida, K., Yamakita, Y., Matsumura, F. (1994). Caldesmon: Possible Functions in Microfilament Reorganization During Mitosis and Cell Transformation. In: Estes, J.E., Higgins, P.J. (eds) Actin. Advances in Experimental Medicine and Biology, vol 358. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-2578-3_11
Download citation
DOI: https://doi.org/10.1007/978-1-4615-2578-3_11
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4613-6102-2
Online ISBN: 978-1-4615-2578-3
eBook Packages: Springer Book Archive