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Dynamic gradients of an intermediate filament-like cytoskeleton are recruited by a polarity landmark during apical growth.

Fuchino, Katsuya LU ; Bagchi, Sonchita ; Cantlay, Stuart LU ; Sandblad, Linda ; Wu, Di ; Bergman, Jessica ; Kamali-Moghaddam, Masood ; Flärdh, Klas LU and Ausmees, Nora (2013) In Proceedings of the National Academy of Sciences 110(21). p.1889-1897
Abstract
Intermediate filament (IF)-like cytoskeleton emerges as a versatile tool for cellular organization in all kingdoms of life, underscoring the importance of mechanistically understanding its diverse manifestations. We showed previously that, in Streptomyces (a bacterium with a mycelial lifestyle similar to that of filamentous fungi, including extreme cell and growth polarity), the IF protein FilP confers rigidity to the hyphae by an unknown mechanism. Here, we provide a possible explanation for the IF-like function of FilP by demonstrating its ability to self-assemble into a cis-interconnected regular network in vitro and its localization into structures consistent with a cytoskeletal network in vivo. Furthermore, we reveal that a spatially... (More)
Intermediate filament (IF)-like cytoskeleton emerges as a versatile tool for cellular organization in all kingdoms of life, underscoring the importance of mechanistically understanding its diverse manifestations. We showed previously that, in Streptomyces (a bacterium with a mycelial lifestyle similar to that of filamentous fungi, including extreme cell and growth polarity), the IF protein FilP confers rigidity to the hyphae by an unknown mechanism. Here, we provide a possible explanation for the IF-like function of FilP by demonstrating its ability to self-assemble into a cis-interconnected regular network in vitro and its localization into structures consistent with a cytoskeletal network in vivo. Furthermore, we reveal that a spatially restricted interaction between FilP and DivIVA, the main component of the Streptomyces polarisome complex, leads to formation of apical gradients of FilP in hyphae undergoing active tip extension. We propose that the coupling between the mechanism driving polar growth and the assembly of an IF cytoskeleton provides each new hypha with an additional stress-bearing structure at its tip, where the nascent cell wall is inevitably more flexible and compliant while it is being assembled and matured. Our data suggest that recruitment of cytoskeleton around a cell polarity landmark is a broadly conserved strategy in tip-growing cells. (Less)
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author
; ; ; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
in
Proceedings of the National Academy of Sciences
volume
110
issue
21
pages
1889 - 1897
publisher
National Academy of Sciences
external identifiers
  • wos:000320328700004
  • pmid:23641002
  • scopus:84878137161
  • pmid:23641002
ISSN
1091-6490
DOI
10.1073/pnas.1305358110
language
English
LU publication?
yes
id
ed32b002-527d-405f-bd43-8ed663337d38 (old id 3804953)
date added to LUP
2016-04-01 10:21:30
date last changed
2022-04-12 05:26:58
@article{ed32b002-527d-405f-bd43-8ed663337d38,
  abstract     = {{Intermediate filament (IF)-like cytoskeleton emerges as a versatile tool for cellular organization in all kingdoms of life, underscoring the importance of mechanistically understanding its diverse manifestations. We showed previously that, in Streptomyces (a bacterium with a mycelial lifestyle similar to that of filamentous fungi, including extreme cell and growth polarity), the IF protein FilP confers rigidity to the hyphae by an unknown mechanism. Here, we provide a possible explanation for the IF-like function of FilP by demonstrating its ability to self-assemble into a cis-interconnected regular network in vitro and its localization into structures consistent with a cytoskeletal network in vivo. Furthermore, we reveal that a spatially restricted interaction between FilP and DivIVA, the main component of the Streptomyces polarisome complex, leads to formation of apical gradients of FilP in hyphae undergoing active tip extension. We propose that the coupling between the mechanism driving polar growth and the assembly of an IF cytoskeleton provides each new hypha with an additional stress-bearing structure at its tip, where the nascent cell wall is inevitably more flexible and compliant while it is being assembled and matured. Our data suggest that recruitment of cytoskeleton around a cell polarity landmark is a broadly conserved strategy in tip-growing cells.}},
  author       = {{Fuchino, Katsuya and Bagchi, Sonchita and Cantlay, Stuart and Sandblad, Linda and Wu, Di and Bergman, Jessica and Kamali-Moghaddam, Masood and Flärdh, Klas and Ausmees, Nora}},
  issn         = {{1091-6490}},
  language     = {{eng}},
  number       = {{21}},
  pages        = {{1889--1897}},
  publisher    = {{National Academy of Sciences}},
  series       = {{Proceedings of the National Academy of Sciences}},
  title        = {{Dynamic gradients of an intermediate filament-like cytoskeleton are recruited by a polarity landmark during apical growth.}},
  url          = {{http://dx.doi.org/10.1073/pnas.1305358110}},
  doi          = {{10.1073/pnas.1305358110}},
  volume       = {{110}},
  year         = {{2013}},
}