Tropomyosin isoform 3 promotes the formation of filopodia by regulating the recruitment of actin-binding proteins to actin filaments

Experimental Cell Research

Volumn 317, Issue 3, 2011, Pages 249-261

  Creed, Sarah J ^a,d,e   Desouza, Melissa ^c   Bamburg, James R ^b   Gunning, Peter ^c   Stehn, Justine ^c  

^a CHILDREN S HOSPITAL AT WESTMEAD   (Australia)

^b Department of Environmental and Radiological Health Sciences   (United States)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d UNIVERSITY OF SYDNEY   (Australia)

^e UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Actin; Fascin; Filopodia; Isoform; Tropomyosin

Indexed keywords

ACTIN BINDING PROTEIN; ACTIN DEPOLYMERIZING FACTOR; ACTIN RELATED PROTEIN 2-3 COMPLEX; COFILIN; DEOXYRIBONUCLEASE I; FASCIN; ISOPROTEIN; TROPOMYOSIN; TROPOMYOSIN 3; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; FILOPODIUM; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SOLUBILITY; UPREGULATION;

EID: 78650056157     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2010.10.019     Document Type: Article

References (58)

1. Rubenstein P.A. The functional importance of multiple actin isoforms. Bioessays 1990, 12:309-315.
2. Steinmetz M.O., Stoffler D., Hoenger A., Bremer A., Aebi U. Actin: from cell biology to atomic detail. J. Struct. Biol. 1997, 119:295-320.
3. Guan J.Q., Takamoto K., Almo S.C., Reisler E., Chance M.R. Structure and dynamics of the actin filament. Biochemistry 2005, 44:3166-3175.
4. Gunning P., Hardeman E., Jeffrey P., Weinberger R. Creating intracellular structural domains: spatial segregation of actin and tropomyosin isoforms in neurons. Bioessays 1998, 20:892-900.
5. Gunning P., Weinberger R., Jeffrey P., Hardeman E. Isoform sorting and the creation of intracellular compartments. Annu. Rev. Cell Dev. Biol. 1998, 14:339-372.
6. Hall A. Rho GTPases and the actin cytoskeleton. Science 1998, 279:509-514.
7. Hall A., Nobes C.D. Rho GTPases: molecular switches that control the organization and dynamics of the actin cytoskeleton. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2000, 355:965-970.
8. Etienne-Manneville S., Hall A. Rho GTPases in cell biology. Nature 2002, 420:629-635.
9. Winder S.J., Ayscough K.R. Actin-binding proteins. J. Cell Sci. 2005, 118:651-654.
10. Lees-Miller J.P., Goodwin L.O., Helfman D.M. Three novel brain tropomyosin isoforms are expressed from the rat alpha-tropomyosin gene through the use of alternative promoters and alternative RNA processing. Mol. Cell. Biol. 1990, 10:1729-1742.
11. Beisel K.W., Kennedy J.E. Identification of novel alternatively spliced isoforms of the tropomyosin-encoding gene, TMnm, in the rat cochlea36. Gene 1994, 143:251-256.
12. Dufour C., Weinberger R.P., Schevzov G., Jeffrey P.L., Gunning P. Splicing of two internal and four carboxyl-terminal alternative exons in nonmuscle tropomyosin 5 pre-mRNA is independently regulated during development. J. Biol. Chem. 1998, 273:18547-18555.
13. Cooley B.C., Bergtrom G. Multiple combinations of alternatively spliced exons in rat tropomyosin-alpha gene mRNA: evidence for 20 new isoforms in adult tissues and cultured cells. Arch. Biochem. Biophys. 2001, 390:71-77.
14. Bernstein B.W., Bamburg J.R. Tropomyosin binding to F-actin protects the F-actin from disassembly by brain actin-depolymerizing factor (ADF). Cell Motil. 1982, 2:1-8.
15. Hitchcock-DeGregori S.E., Sampath P., Pollard T.D. Tropomyosin inhibits the rate of actin polymerization by stabilizing actin filaments. Biochemistry 1988, 27:9182-9185.
16. Broschat K.O., Weber A., Burgess D.R. Tropomyosin stabilizes the pointed end of actin filaments by slowing depolymerization. Biochemistry 1989, 28:8501-8506.
17. Ishikawa R., Yamashiro S., Matsumura F. 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. 1989, 264:7490-7497.
18. Broschat K.O. Tropomyosin prevents depolymerization of actin filaments from the pointed end. J. Biol. Chem. 1990, 265:21323-21329.
19. Matsumura F., Yamashiro-Matsumura S. Purification and characterization of multiple isoforms of tropomyosin from rat cultured cells. J. Biol. Chem. 1985, 260:13851-13859.
20. Broschat K.O., Burgess D.R. Low Mr tropomyosin isoforms from chicken brain and intestinal epithelium have distinct actin-binding properties. J. Biol. Chem. 1986, 261:13350-13359.
21. Pittenger M.F., Helfman D.M. In vitro and in vivo characterization of four fibroblast tropomyosins produced in bacteria: TM-2, TM-3, TM-5a, and TM-5b are co-localized in interphase fibroblasts. J. Cell Biol. 1992, 118:841-858.
22. Novy R.E., Sellers J.R., Liu L.F., Lin J.J. In vitro functional characterization of bacterially expressed human fibroblast tropomyosin isoforms and their chimeric mutants. Cell Motil. Cytoskel. 1993, 26:248-261.
23. Pittenger M.F., Kazzaz J.A., Helfman D.M. Functional properties of non-muscle tropomyosin isoforms. Curr. Opin. Cell Biol. 1994, 6:96-104.
24. Lin J.J., Warren K.S., Wamboldt D.D., Wang T., Lin J.L. Tropomyosin isoforms in nonmuscle cells. Int. Rev. Cytol. 1997, 170:1-38.
25. 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. Tissue-specific tropomyosin isoform composition. J. Histochem. Cytochem. 2005, 53:557-570.
26. Perry S.V. Vertebrate tropomyosin: distribution, properties and function. J. Muscle Res. Cell Motil. 2001, 22:5-49.
27. Stehn J.R., Schevzov G., O'Neill G.M., Gunning P.W. Specialisation of the tropomyosin composition of actin filaments provides new potential targets for chemotherapy. Curr. Cancer Drug Targets 2006, 6:245-256.
28. O'Neill G.M., Stehn J., Gunning P.W. Tropomyosins as interpreters of the signaling environment to regulate the local cytoskeleton. Semin. Cancer Biol. 2008, 18:35-44.
29. Warren K.S., Lin J.L., McDermott J.P., Lin J.J. Forced expression of chimeric human fibroblast tropomyosin mutants affects cytokinesis. J. Cell Biol. 1995, 129:697-708.
30. Percival J.M., Thomas G., Cock T.A., Gardiner E.M., Jeffrey P.L., Lin J.J., Weinberger R.P., Gunning P. Sorting of tropomyosin isoforms in synchronised NIH 3T3 fibroblasts: evidence for distinct microfilament populations. Cell Motil. Cytoskel. 2000, 47:189-208.
31. Creed S.J., Bryce N., Naumanen P., Weinberger R., Lappalainen P., Stehn J., Gunning P. Tropomyosin isoforms define distinct microfilament populations with different drug susceptibility. Eur. J. Cell Biol. 2008, 87:709-720.
32. Bryce N.S., Schevzov G., Ferguson V., Percival J.M., Lin J.J., Matsumura F., Bamburg J.R., Jeffrey P.L., Hardeman E.C., Gunning P., Weinberger R.P. Specification of actin filament function and molecular composition by tropomyosin isoforms. Mol. Biol. Cell 2003, 14:1002-1016.
33. Otey C.A., Boukhelifa M., Maness P. B35 neuroblastoma cells: an easily transfected, cultured cell model of central nervous system neurons. Meth. Cell Biol. 2003, 71:287-304.34.
34. Schubert D., Heinemann S., Carlisle W., Tarikas H., Kimes B., Patrick J., Steinbach J.H., Culp W., Brandt B.L. Clonal cell lines from the rat central nervous system. Nature 1974, 249:224-227.
35. Qin H., Gunning P. The 3'-end of the human beta-actin gene enhances activity of the beta-actin expression vector system: construction of improved vectors. J. Biochem. Biophys. Meth. 1997, 36:63-72.
36. Leavitt J., Ng S.Y., Aebi U., Varma M., Latter G., Burbeck S., Kedes L., Gunning P. Expression of transfected mutant beta-actin genes: alterations of cell morphology and evidence for autoregulation in actin pools. Mol. Cell. Biol. 1987, 7:2457-2466.
37. Percival J.M., Hughes J.A., Brown D.L., Schevzov G., Heimann K., Vrhovski B., Bryce N., Stow J.L., Gunning P.W. Targeting of a tropomyosin isoform to short microfilaments associated with the Golgi complex. Mol. Biol. Cell 2004, 15:268-280.
38. Vrhovski B., Schevzov G., Dingle S., Lessard J.L., Gunning P., Weinberger R.P. Tropomyosin isoforms from the gamma gene differing at the C-terminus are spatially and developmentally regulated in the brain. J. Neurosci. Res. 2003, 72:373-383.
39. Meberg P.J., Ono S., Minamide L.S., Takahashi M., Bamburg J.R. Actin depolymerizing factor and cofilin phosphorylation dynamics: response to signals that regulate neurite extension. Cell Motil. Cytoskel. 1998, 39:172-190.
40. Minamide L.S., Striegl A.M., Boyle J.A., Meberg P.J., Bamburg J.R. Neurodegenerative stimuli induce persistent ADF/cofilin-actin rods that disrupt distal neurite function. Nat. Cell Biol. 2000, 2:628-636.
41. Vignjevic D., Yarar D., Welch M.D., Peloquin J., Svitkina T., Borisy G.G. Formation of filopodia-like bundles in vitro from a dendritic network. J. Cell Biol. 2003, 160:951-962.
42. Carlier M.F. Actin: protein structure and filament dynamics. J. Biol. Chem. 1991, 266:1-4.
43. Holmes K.C., Popp D., Gebhard W., Kabsch W. Atomic model of the actin filament. Nature 1990, 347:44-49.
44. Cramer L.P., Briggs L.J., Dawe H.R. Use of fluorescently labelled deoxyribonuclease I to spatially measure G-actin levels in migrating and non-migrating cells. Cell Motil. Cytoskel. 2002, 51:27-38.
45. Andrianantoandro E., Pollard T.D. Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol. Cell. 2006, 24:13-23.
46. Hotulainen P., Paunola E., Vartiainen M.K., Lappalainen P. Actin-depolymerizing factor and cofilin-1 play overlapping roles in promoting rapid F-actin depolymerization in mammalian nonmuscle cells. Mol. Biol. Cell. 2005, 16:649-664.
47. Arber S., Barbayannis F.A., Hanser H., Schneider C., Stanyon C.A., Bernard O., Caroni P. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 1998, 393:805-809.
48. Yang N., Higuchi O., Ohashi K., Nagata K., Wada A., Kangawa K., Nishida E., Mizuno K. Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature 1998, 393:809-812.
49. Ma L., Rohatgi R., Kirschner M.W. The Arp2/3 complex mediates actin polymerization induced by the small GTP-binding protein Cdc42. Proc. Natl Acad. Sci. USA 1998, 95:15362-15367.
50. Mullins R.D., Heuser J.A., Pollard T.D. The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc. Natl Acad. Sci. USA 1998, 95:6181-6186.
51. Mullins R.D., Pollard T.D. Structure and function of the Arp2/3 complex. Curr. Opin. Struct. Biol. 1999, 9:244-249.
52. Yamashiro-Matsumura S., Matsumura F. Purification and characterization of an F-actin-bundling 55-kilodalton protein from HeLa cells. J. Biol. Chem. 1985, 260:5087-5097.
53. Yamashiro S., Yamakita Y., Ono S., Matsumura F. Fascin, an actin-bundling protein, induces membrane protrusions and increases cell motility of epithelial cells. Mol. Biol. Cell 1998, 9:993-1006.
54. Vignjevic D., Kojima S.i., Aratyn Y., Danciu O., Svitkina T., Borisy G.G. Role of fascin in filopodial protrusion. J. Cell Biol. 2006, 174:863-875.
55. Gunning P.W., Schevzov G., Kee A.J., Hardeman E.C. Tropomyosin isoforms: divining rods for actin cytoskeleton function. Trends Cell Biol. 2005, 15:333-341.
56. Gunning P., O'Neill G., Hardeman E. Tropomyosin-based regulation of the actin cytoskeleton in time and space. Physiol. Rev. 2008, 88:1-35.
57. Lehman W., Hatch V., Korman V., Rosol M., Thomas L., Maytum R., Geeves M.A., Van Eyk J.E., Tobacman L.S., Craig R. Tropomyosin and actin isoforms modulate the localization of tropomyosin strands on actin filaments. J. Mol. Biol. 2000, 302:593-606.
58. Jaffe A.B., Hall A. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 2005, 21:247-269.