Specification of actin filament function and molecular composition by tropomyosin isoforms

Nicole S. Bryce, Galina Schevzov, Vicki Ferguson, Justin Percival, Jim J C Lin, Fumio Matsumura, James R. Bamburg, Peter L. Jeffrey, Edna C. Hardeman, Peter Gunning, Ron P. Weinberger

Research output: Contribution to journalArticle

166 Citations (Scopus)

Abstract

The specific functions of greater than 40 vertebrate nonmuscle tropomyosins (Tms) are poorly understood. In this article we have tested the ability of two Tm isoforms, TmBr3 and the human homologue of Tm5 (hTM5NM1), to regulate actin filament function. We found that these Tms can differentially alter actin filament organization, cell size, and shape, hTm5NM1 was able to recruit myosin II into stress fibers, which resulted in decreased lamellipodia and cellular migration. In contrast, TmBr3 transfection induced lamellipodial formation, increased cellular migration, and reduced stress fibers. Based on coimmunoprecipitation and colocalization studies, TmBr3 appeared to be associated with actin-depolymerizing factor/cofilin (ADF)-bound actin filaments. Additionally, the Tms can specifically regulate the incorporation of other Tms into actin filaments, suggesting that selective dimerization may also be involved in the control of actin filament organization. We conclude that Tm isoforms can be used to specify the functional properties and molecular composition of actin filaments and that spatial segregation of isoforms may lead to localized specialization of actin filament function.

Original languageEnglish
Pages (from-to)1002-1016
Number of pages15
JournalMolecular Biology of the Cell
Volume14
Issue number3
DOIs
StatePublished - Mar 1 2003
Externally publishedYes

Fingerprint

Tropomyosin
Actin Cytoskeleton
Protein Isoforms
Stress Fibers
Destrin
Actin Depolymerizing Factors
Myosin Type II
Pseudopodia
Cell Shape
Dimerization
Cell Size
Transfection
Vertebrates

ASJC Scopus subject areas

  • Molecular Biology
  • Genetics
  • Cell Biology

Cite this

Bryce, N. S., Schevzov, G., Ferguson, V., Percival, J., Lin, J. J. C., Matsumura, F., ... Weinberger, R. P. (2003). Specification of actin filament function and molecular composition by tropomyosin isoforms. Molecular Biology of the Cell, 14(3), 1002-1016. https://doi.org/10.1091/mbc.E02-04-0244

Specification of actin filament function and molecular composition by tropomyosin isoforms. / Bryce, Nicole S.; Schevzov, Galina; Ferguson, Vicki; Percival, Justin; Lin, Jim J C; Matsumura, Fumio; Bamburg, James R.; Jeffrey, Peter L.; Hardeman, Edna C.; Gunning, Peter; Weinberger, Ron P.

In: Molecular Biology of the Cell, Vol. 14, No. 3, 01.03.2003, p. 1002-1016.

Research output: Contribution to journalArticle

Bryce, NS, Schevzov, G, Ferguson, V, Percival, J, Lin, JJC, Matsumura, F, Bamburg, JR, Jeffrey, PL, Hardeman, EC, Gunning, P & Weinberger, RP 2003, 'Specification of actin filament function and molecular composition by tropomyosin isoforms', Molecular Biology of the Cell, vol. 14, no. 3, pp. 1002-1016. https://doi.org/10.1091/mbc.E02-04-0244
Bryce, Nicole S. ; Schevzov, Galina ; Ferguson, Vicki ; Percival, Justin ; Lin, Jim J C ; Matsumura, Fumio ; Bamburg, James R. ; Jeffrey, Peter L. ; Hardeman, Edna C. ; Gunning, Peter ; Weinberger, Ron P. / Specification of actin filament function and molecular composition by tropomyosin isoforms. In: Molecular Biology of the Cell. 2003 ; Vol. 14, No. 3. pp. 1002-1016.
@article{02a914e450fe4dc9a75313cc8ed4ef53,
title = "Specification of actin filament function and molecular composition by tropomyosin isoforms",
abstract = "The specific functions of greater than 40 vertebrate nonmuscle tropomyosins (Tms) are poorly understood. In this article we have tested the ability of two Tm isoforms, TmBr3 and the human homologue of Tm5 (hTM5NM1), to regulate actin filament function. We found that these Tms can differentially alter actin filament organization, cell size, and shape, hTm5NM1 was able to recruit myosin II into stress fibers, which resulted in decreased lamellipodia and cellular migration. In contrast, TmBr3 transfection induced lamellipodial formation, increased cellular migration, and reduced stress fibers. Based on coimmunoprecipitation and colocalization studies, TmBr3 appeared to be associated with actin-depolymerizing factor/cofilin (ADF)-bound actin filaments. Additionally, the Tms can specifically regulate the incorporation of other Tms into actin filaments, suggesting that selective dimerization may also be involved in the control of actin filament organization. We conclude that Tm isoforms can be used to specify the functional properties and molecular composition of actin filaments and that spatial segregation of isoforms may lead to localized specialization of actin filament function.",
author = "Bryce, {Nicole S.} and Galina Schevzov and Vicki Ferguson and Justin Percival and Lin, {Jim J C} and Fumio Matsumura and Bamburg, {James R.} and Jeffrey, {Peter L.} and Hardeman, {Edna C.} and Peter Gunning and Weinberger, {Ron P.}",
year = "2003",
month = "3",
day = "1",
doi = "10.1091/mbc.E02-04-0244",
language = "English",
volume = "14",
pages = "1002--1016",
journal = "Molecular Biology of the Cell",
issn = "1059-1524",
publisher = "American Society for Cell Biology",
number = "3",

}

TY - JOUR

T1 - Specification of actin filament function and molecular composition by tropomyosin isoforms

AU - Bryce, Nicole S.

AU - Schevzov, Galina

AU - Ferguson, Vicki

AU - Percival, Justin

AU - Lin, Jim J C

AU - Matsumura, Fumio

AU - Bamburg, James R.

AU - Jeffrey, Peter L.

AU - Hardeman, Edna C.

AU - Gunning, Peter

AU - Weinberger, Ron P.

PY - 2003/3/1

Y1 - 2003/3/1

N2 - The specific functions of greater than 40 vertebrate nonmuscle tropomyosins (Tms) are poorly understood. In this article we have tested the ability of two Tm isoforms, TmBr3 and the human homologue of Tm5 (hTM5NM1), to regulate actin filament function. We found that these Tms can differentially alter actin filament organization, cell size, and shape, hTm5NM1 was able to recruit myosin II into stress fibers, which resulted in decreased lamellipodia and cellular migration. In contrast, TmBr3 transfection induced lamellipodial formation, increased cellular migration, and reduced stress fibers. Based on coimmunoprecipitation and colocalization studies, TmBr3 appeared to be associated with actin-depolymerizing factor/cofilin (ADF)-bound actin filaments. Additionally, the Tms can specifically regulate the incorporation of other Tms into actin filaments, suggesting that selective dimerization may also be involved in the control of actin filament organization. We conclude that Tm isoforms can be used to specify the functional properties and molecular composition of actin filaments and that spatial segregation of isoforms may lead to localized specialization of actin filament function.

AB - The specific functions of greater than 40 vertebrate nonmuscle tropomyosins (Tms) are poorly understood. In this article we have tested the ability of two Tm isoforms, TmBr3 and the human homologue of Tm5 (hTM5NM1), to regulate actin filament function. We found that these Tms can differentially alter actin filament organization, cell size, and shape, hTm5NM1 was able to recruit myosin II into stress fibers, which resulted in decreased lamellipodia and cellular migration. In contrast, TmBr3 transfection induced lamellipodial formation, increased cellular migration, and reduced stress fibers. Based on coimmunoprecipitation and colocalization studies, TmBr3 appeared to be associated with actin-depolymerizing factor/cofilin (ADF)-bound actin filaments. Additionally, the Tms can specifically regulate the incorporation of other Tms into actin filaments, suggesting that selective dimerization may also be involved in the control of actin filament organization. We conclude that Tm isoforms can be used to specify the functional properties and molecular composition of actin filaments and that spatial segregation of isoforms may lead to localized specialization of actin filament function.

UR - http://www.scopus.com/inward/record.url?scp=0037343138&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0037343138&partnerID=8YFLogxK

U2 - 10.1091/mbc.E02-04-0244

DO - 10.1091/mbc.E02-04-0244

M3 - Article

VL - 14

SP - 1002

EP - 1016

JO - Molecular Biology of the Cell

JF - Molecular Biology of the Cell

SN - 1059-1524

IS - 3

ER -