A
correction
to this article has been published: J. Cell Biol. 157 (4) 727
Published 18 March 2002. doi:10.1083/jcb.200110013
© The Rockefeller University Press,
0021-9525/2002/3/1065 $5.00
The Journal of Cell Biology, Volume 156, Number 6, March 18, 2002 1065-1076
Tropomyosin inhibits ADF/cofilin-dependent actin filament dynamics
Shoichiro Ono and
Kanako Ono
Department of Pathology, Emory University, Atlanta, Georgia 30322
Address correspondence to Shoichiro Ono, Dept. of Pathology, Emory University, 615 Michael St., Whitehead Research Bldg., Rm. 105N, Atlanta, GA 30322. Tel.: (404) 727-3916. Fax: (404) 727-8538. E-mail: sono{at}emory.edu
Tropomyosin binds to actin filaments and is implicated in stabilization of actin cytoskeleton. We examined biochemical and cell biological properties of Caenorhabditis elegans tropomyosin (CeTM) and obtained evidence that CeTM is antagonistic to ADF/cofilin-dependent actin filament dynamics. We purified CeTM, actin, and UNC-60B (a muscle-specific ADF/cofilin isoform), all of which are derived from C. elegans, and showed that CeTM and UNC-60B bound to F-actin in a mutually exclusive manner. CeTM inhibited UNC-60Binduced actin depolymerization and enhancement of actin polymerization. Within isolated native thin filaments, actin and CeTM were detected as major components, whereas UNC-60B was present at a trace amount. Purified UNC-60B was unable to interact with the native thin filaments unless CeTM and other associated proteins were removed by high-salt extraction. Purified CeTM was sufficient to restore the resistance of the salt-extracted filaments from UNC-60B. In muscle cells, CeTM and UNC-60B were localized in different patterns. Suppression of CeTM by RNA interference resulted in disorganized actin filaments and paralyzed worms in wild-type background. However, in an ADF/cofilin mutant background, suppression of CeTM did not worsen actin organization and worm motility. These results suggest that tropomyosin is a physiological inhibitor of ADF/cofilin-dependent actin dynamics.
Key Words: myofibrils; thin filaments; actin; ADF/cofilin; tropomyosin

CiteULike
Complore
Connotea
Del.icio.us
Digg
Facebook
Reddit
Technorati
Twitter What's this?
Related Article
-
Tropomyosin keeps actin tough
- Alan W. Dove
J. Cell Biol. 2002 156: 939.
[Full Text]
[PDF]
This article has been cited by other articles:
-
Kueh, H. Y., Mitchison, T. J.
(2009). Structural Plasticity in Actin and Tubulin Polymer Dynamics. Science
325: 960-963
[Abstract]
[Full Text]
-
Skau, C. T., Neidt, E. M., Kovar, D. R.
(2009). Role of Tropomyosin in Formin-mediated Contractile Ring Assembly in Fission Yeast. Mol. Biol. Cell
20: 2160-2173
[Abstract]
[Full Text]
-
Vlahovich, N., Kee, A. J., Van der Poel, C., Kettle, E., Hernandez-Deviez, D., Lucas, C., Lynch, G. S., Parton, R. G., Gunning, P. W., Hardeman, E. C.
(2009). Cytoskeletal Tropomyosin Tm5NM1 Is Required for Normal Excitation-Contraction Coupling in Skeletal Muscle. Mol. Biol. Cell
20: 400-409
[Abstract]
[Full Text]
-
Zhao, R., Du, L., Huang, Y., Wu, Y., Gunst, S. J.
(2008). Actin Depolymerization Factor/Cofilin Activation Regulates Actin Polymerization and Tension Development in Canine Tracheal Smooth Muscle. J. Biol. Chem.
283: 36522-36531
[Abstract]
[Full Text]
-
Yamashiro, S., Cox, E. A., Baillie, D. L., Hardin, J. D., Ono, S.
(2008). Sarcomeric actin organization is synergistically promoted by tropomodulin, ADF/cofilin, AIP1 and profilin in C. elegans. J. Cell Sci.
121: 3867-3877
[Abstract]
[Full Text]
-
Kueh, H. Y., Brieher, W. M., Mitchison, T. J.
(2008). Dynamic stabilization of actin filaments. Proc. Natl. Acad. Sci. USA
105: 16531-16536
[Abstract]
[Full Text]
-
Chaudhuri, S., Smith, P. G.
(2008). Cyclic Strain-Induced HSP27 Phosphorylation Modulates Actin Filaments in Airway Smooth Muscle Cells. Am. J. Respir. Cell Mol. Bio.
39: 270-278
[Abstract]
[Full Text]
-
Gunst, S. J., Zhang, W.
(2008). Actin cytoskeletal dynamics in smooth muscle: a new paradigm for the regulation of smooth muscle contraction. Am. J. Physiol. Cell Physiol.
295: C576-C587
[Abstract]
[Full Text]
-
Ono, K., Yamashiro, S., Ono, S.
(2008). Essential role of ADF/cofilin for assembly of contractile actin networks in the C. elegans somatic gonad. J. Cell Sci.
121: 2662-2670
[Abstract]
[Full Text]
-
Noda, Y., Horikawa, S., Kanda, E., Yamashita, M., Meng, H., Eto, K., Li, Y., Kuwahara, M., Hirai, K., Pack, C., Kinjo, M., Okabe, S., Sasaki, S.
(2008). Reciprocal interaction with G-actin and tropomyosin is essential for aquaporin-2 trafficking. JCB
182: 587-601
[Abstract]
[Full Text]
-
Guettler, S., Vartiainen, M. K., Miralles, F., Larijani, B., Treisman, R.
(2008). RPEL Motifs Link the Serum Response Factor Cofactor MAL but Not Myocardin to Rho Signaling via Actin Binding. Mol. Cell. Biol.
28: 732-742
[Abstract]
[Full Text]
-
Schevzov, G., Fath, T., Vrhovski, B., Vlahovich, N., Rajan, S., Hook, J., Joya, J. E., Lemckert, F., Puttur, F., Lin, J. J.-C., Hardeman, E. C., Wieczorek, D. F., O'Neill, G. M., Gunning, P. W.
(2008). Divergent Regulation of the Sarcomere and the Cytoskeleton. J. Biol. Chem.
283: 275-283
[Abstract]
[Full Text]
-
Gunning, P., O'neill, G., Hardeman, E.
(2008). Tropomyosin-Based Regulation of the Actin Cytoskeleton in Time and Space. Physiol. Rev.
88: 1-35
[Abstract]
[Full Text]
-
Yamashiro, S., Gimona, M., Ono, S.
(2007). UNC-87, a calponin-related protein in C. elegans, antagonizes ADF/cofilin-mediated actin filament dynamics. J. Cell Sci.
120: 3022-3033
[Abstract]
[Full Text]
-
Clark, M. G., Amberg, D. C.
(2007). Biochemical and Genetic Analyses Provide Insight Into the Structural and Mechanistic Properties of Actin Filament Disassembly by the Aip1p Cofilin Complex in Saccharomyces cerevisiae. Genetics
176: 1527-1539
[Abstract]
[Full Text]
-
Kurita, S., Gunji, E., Ohashi, K., Mizuno, K.
(2007). Actin filaments-stabilizing and -bundling activities of cofilin-phosphatase Slingshot-1. GENES CELLS
12: 663-676
[Abstract]
[Full Text]
-
Moseley, J. B., Goode, B. L.
(2006). The Yeast Actin Cytoskeleton: from Cellular Function to Biochemical Mechanism. Microbiol. Mol. Biol. Rev.
70: 605-645
[Abstract]
[Full Text]
-
Ono, K., Yu, R., Mohri, K., Ono, S.
(2006). Caenorhabditis elegans Kettin, a Large Immunoglobulin-like Repeat Protein, Binds to Filamentous Actin and Provides Mechanical Stability to the Contractile Apparatuses in Body Wall Muscle. Mol. Biol. Cell
17: 2722-2734
[Abstract]
[Full Text]
-
Mohri, K., Ono, K., Yu, R., Yamashiro, S., Ono, S.
(2006). Enhancement of Actin-depolymerizing Factor/Cofilin-dependent Actin Disassembly by Actin-interacting Protein 1 Is Required for Organized Actin Filament Assembly in the Caenorhabditis elegans Body Wall Muscle. Mol. Biol. Cell
17: 2190-2199
[Abstract]
[Full Text]
-
Dixon, S. J., Roy, P. J.
(2005). Muscle arm development in Caenorhabditis elegans. Development
132: 3079-3092
[Abstract]
[Full Text]
-
Galkin, V. E., Esashi, F., Yu, X., Yang, S., West, S. C., Egelman, E. H.
(2005). BRCA2 BRC motifs bind RAD51-DNA filaments. Proc. Natl. Acad. Sci. USA
102: 8537-8542
[Abstract]
[Full Text]
-
Schevzov, G., Vrhovski, B., Bryce, N. S., Elmir, S., Qiu, M. R., O'Neill, G. M., Yang, N., Verrills, N. M., Kavallaris, M., Gunning, P. W.
(2005). Tissue-specific Tropomyosin Isoform Composition. J. Histochem. Cytochem.
53: 557-570
[Abstract]
[Full Text]
-
Giganti, A., Plastino, J., Janji, B., Van Troys, M., Lentz, D., Ampe, C., Sykes, C., Friederich, E.
(2005). Actin-filament cross-linking protein T-plastin increases Arp2/3-mediated actin-based movement. J. Cell Sci.
118: 1255-1265
[Abstract]
[Full Text]
-
Hotulainen, P., Paunola, E., Vartiainen, M. K., Lappalainen, P.
(2005). Actin-depolymerizing Factor and Cofilin-1 Play Overlapping Roles in Promoting Rapid F-Actin Depolymerization in Mammalian Nonmuscle Cells. Mol. Biol. Cell
16: 649-664
[Abstract]
[Full Text]
-
DesMarais, V., Ghosh, M., Eddy, R., Condeelis, J.
(2005). Cofilin takes the lead. J. Cell Sci.
118: 19-26
[Abstract]
[Full Text]
-
Anyanful, A., Ono, K., Johnsen, R. C., Ly, H., Jensen, V., Baillie, D. L., Ono, S.
(2004). The RNA-binding protein SUP-12 controls muscle-specific splicing of the ADF/cofilin pre-mRNA in C. elegans. JCB
167: 639-647
[Abstract]
[Full Text]
-
Van Troys, M., Ono, K., Dewitte, D., Jonckheere, V., De Ruyck, N., Vandekerckhove, J., Ono, S., Ampe, C.
(2004). TetraThymosin{beta} Is Required for Actin Dynamics in Caenorhabditis elegans and Acts via Functionally Different Actin-binding Repeats. Mol. Biol. Cell
15: 4735-4748
[Abstract]
[Full Text]
-
Bakin, A. V., Safina, A., Rinehart, C., Daroqui, C., Darbary, H., Helfman, D. M.
(2004). A Critical Role of Tropomyosins in TGF-{beta} Regulation of the Actin Cytoskeleton and Cell Motility in Epithelial Cells. Mol. Biol. Cell
15: 4682-4694
[Abstract]
[Full Text]
-
Ono, K., Ono, S.
(2004). Tropomyosin and Troponin Are Required for Ovarian Contraction in the Caenorhabditis elegans Reproductive System. Mol. Biol. Cell
15: 2782-2793
[Abstract]
[Full Text]
-
Pichon, S., Bryckaert, M., Berrou, E.
(2004). Control of actin dynamics by p38 MAP kinase - Hsp27 distribution in the lamellipodium of smooth muscle cells. J. Cell Sci.
117: 2569-2577
[Abstract]
[Full Text]
-
Malmstrom, J., Lindberg, H., Lindberg, C., Bratt, C., Wieslander, E., Delander, E.-L., Sarnstrand, B., Burns, J. S., Mose-Larsen, P., Fey, S., Marko-Varga, G.
(2004). Transforming Growth Factor-{beta}1 Specifically Induce Proteins Involved in the Myofibroblast Contractile Apparatus. Mol. Cell. Proteomics
3: 466-477
[Abstract]
[Full Text]
-
Bharadwaj, S., Hitchcock-DeGregori, S., Thorburn, A., Prasad, G. L.
(2004). N Terminus Is Essential for Tropomyosin Functions: N-TERMINAL MODIFICATION DISRUPTS STRESS FIBER ORGANIZATION AND ABOLISHES ANTI-ONCOGENIC EFFECTS OF TROPOMYOSIN-1. J. Biol. Chem.
279: 14039-14048
[Abstract]
[Full Text]
-
Kostyukova, A. S., Hitchcock-DeGregori, S. E.
(2004). Effect of the Structure of the N Terminus of Tropomyosin on Tropomodulin Function. J. Biol. Chem.
279: 5066-5071
[Abstract]
[Full Text]
-
Percival, J. M., Hughes, J. A. I., Brown, D. L., Schevzov, G., Heimann, K., Vrhovski, B., Bryce, N., Stow, J. L., Gunning, P. W.
(2004). Targeting of a Tropomyosin Isoform to Short Microfilaments Associated with the Golgi Complex. Mol. Biol. Cell
15: 268-280
[Abstract]
[Full Text]
-
Fritz-Six, K. L., Cox, P. R., Fischer, R. S., Xu, B., Gregorio, C. C., Zoghbi, H. Y., Fowler, V. M.
(2003). Aberrant myofibril assembly in tropomodulin1 null mice leads to aborted heart development and embryonic lethality. JCB
163: 1033-1044
[Abstract]
[Full Text]
-
Mohri, K., Ono, S.
(2003). Actin filament disassembling activity of Caenorhabditis elegans actin-interacting protein 1 (UNC-78) is dependent on filament binding by a specific ADF/cofilin isoform. J. Cell Sci.
116: 4107-4118
[Abstract]
[Full Text]
-
Mudry, R. E., Perry, C. N., Richards, M., Fowler, V. M., Gregorio, C. C.
(2003). The interaction of tropomodulin with tropomyosin stabilizes thin filaments in cardiac myocytes. JCB
162: 1057-1068
[Abstract]
[Full Text]
-
Gimona, M., Kaverina, I., Resch, G. P., Vignal, E., Burgstaller, G.
(2003). Calponin Repeats Regulate Actin Filament Stability and Formation of Podosomes in Smooth Muscle Cells. Mol. Biol. Cell
14: 2482-2491
[Abstract]
[Full Text]
-
Ono, K., Parast, M., Alberico, C., Benian, G. M., Ono, S.
(2003). Specific requirement for two ADF/cofilin isoforms in distinct actin-dependent processes in Caenorhabditis elegans. J. Cell Sci.
116: 2073-2085
[Abstract]
[Full Text]
-
Bryce, N. S., Schevzov, G., Ferguson, V., Percival, J. M., Lin, J. J.-C., Matsumura, F., Bamburg, J. R., Jeffrey, P. L., Hardeman, E. C., Gunning, P., Weinberger, R. P.
(2003). Specification of Actin Filament Function and Molecular Composition by Tropomyosin Isoforms. Mol. Biol. Cell
14: 1002-1016
[Abstract]
[Full Text]
-
Nyakern-Meazza, M., Narayan, K., Schutt, C. E., Lindberg, U.
(2002). Tropomyosin and Gelsolin Cooperate in Controlling the Microfilament System. J. Biol. Chem.
277: 28774-28779
[Abstract]
[Full Text]
-
DesMarais, V., Ichetovkin, I., Condeelis, J., Hitchcock-DeGregori, S. E.
(2002). Spatial regulation of actin dynamics: a tropomyosin-free, actin-rich compartment at the leading edge. J. Cell Sci.
115: 4649-4660
[Abstract]
[Full Text]