title: Dynamic gradients of an intermediate filament-like cytoskeleton are recruited by a polarity landmark during apical growth.
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.
authors: Department of Biology, Lund University, 22362 Lund, Sweden.
authors: Katsuya
authors: K
authors: Fuchino
authors: Sonchita
authors: S
authors: Bagchi
authors: Stuart
authors: S
authors: Cantlay
authors: Linda
authors: L
authors: Sandblad
authors: Di
authors: D
authors: Wu
authors: Jessica
authors: J
authors: Bergman
authors: Masood
authors: M
authors: Kamali-Moghaddam
authors: Klas
authors: K
authors: Flärdh
authors: Nora
authors: N
authors: Ausmees
mesh_terms: D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism*; D018797:Cell Cycle Proteins / Q000235:genetics / Q000378:metabolism*; D003598:Cytoskeletal Proteins / Q000235:genetics / Q000378:metabolism*; D003599:Cytoskeleton / Q000235:genetics / Q000378:metabolism*; D011485:Protein Binding / Q000502:physiology; D055503:Protein Multimerization / Q000502:physiology*; D048372:Streptomyces coelicolor / Q000235:genetics / Q000378:metabolism*
chemical_list: D001426:Bacterial Proteins; D018797:Cell Cycle Proteins; D003598:Cytoskeletal Proteins; C104636:DivIVA protein, bacteria
references: Nat Prod Rep. 2011 Jul;28(7):1311-33
references: 21611665
references: Phys Rev Lett. 2006 Mar 3;96(8):088102
references: 16606229
references: Nat Methods. 2006 Dec;3(12):995-1000
references: 17072308
references: Methods Cell Biol. 2008;89:487-519
references: 19118688
references: Biochemistry. 1995 Jul 25;34(29):9389-402
references: 7626609
references: J Cell Biol. 2009 Aug 10;186(3):409-21
references: 19651890
references: Mol Microbiol. 1994 Oct;14(2):243-54
references: 7830569
references: Nature. 2003 Apr 17;422(6933):766-74
references: 12700771
references: J Mol Microbiol Biotechnol. 2006;11(3-5):159-66
references: 16983193
references: Expert Rev Proteomics. 2010 Jun;7(3):401-9
references: 20536310
references: Mol Microbiol. 2012 Aug;85(3):393-404
references: 22646484
references: J Gen Microbiol. 1990 Jun;136(6):1077-84
references: 1696612
references: Mol Microbiol. 1997 Sep;25(5):847-58
references: 9364911
references: Proc Natl Acad Sci U S A. 2013 Jan 29;110(5):E397-406
references: 23297235
references: Mol Microbiol. 2003 Sep;49(6):1523-36
references: 12950918
references: Nat Cell Biol. 2001 May;3(5):503-6
references: 11331879
references: Methods Enzymol. 1991;194:565-602
references: 2005809
references: Nat Rev Microbiol. 2009 Jan;7(1):36-49
references: 19079351
references: Annu Rev Biochem. 2004;73:749-89
references: 15189158
references: Fungal Genet Biol. 2002 Dec;37(3):271-82
references: 12431461
references: J Bacteriol. 2008 Nov;190(22):7579-83
references: 18805980
references: Cytoskeleton (Hoboken). 2011 Apr;68(4):205-19
references: 21360832
references: Curr Opin Microbiol. 2010 Dec;13(6):758-65
references: 21036658
references: Mol Biol Cell. 2011 Apr 15;22(8):1274-89
references: 21346197
references: Cell. 2003 Dec 12;115(6):705-13
references: 14675535
references: Biophys J. 2010 May 19;98(10):2147-53
references: 20483322
references: J Biol Chem. 2010 Sep 17;285(38):29387-97
references: 20622015
references: Proc Natl Acad Sci U S A. 2003 Feb 18;100(4):1541-6
references: 12563033
references: EMBO J. 2009 May 6;28(9):1208-19
references: 19279668
references: Proc Natl Acad Sci U S A. 2012 Aug 28;109(35):E2371-9
references: 22869733
references: FEMS Microbiol Rev. 2012 Jan;36(1):206-31
references: 22092088
references: J Mol Biol. 2010 Jun 18;399(4):637-44
references: 20447406
references: BMC Biol. 2011 Feb 28;9:16
references: 21356127
references: Methods Enzymol. 2000;328:59-73
references: 11075338
references: PLoS One. 2010 Jan 25;5(1):e8855
references: 20140233
references: Biophys J. 2010 Nov 3;99(9):2748-56
references: 21044571
references: Int Rev Cytol. 2003;223:83-175
references: 12641211
references: Mol Microbiol. 2006 May;60(4):838-52
references: 16677297
references: Eur J Biochem. 1982 Feb;122(1):193-7
references: 7037399
references: FEMS Microbiol Lett. 2009 Aug;297(1):101-9
references: 19552710
references: J Bacteriol. 2011 Sep;193(17):4523-30
references: 21642462
references: PLoS Comput Biol. 2012;8(3):e1002423
references: 22423220
references: Proc Natl Acad Sci U S A. 1979 Jul;76(7):3174-8
references: 290995
references: J Theor Biol. 2003 May 21;222(2):211-8
references: 12727456
references: PLoS Pathog. 2009 Nov;5(11):e1000669
references: 19936218
references: Nat Cell Biol. 2003 Sep;5(9):803-11
references: 12942086
references: J Cell Biol. 2001 Apr 30;153(3):503-16
references: 11331302
references: Nat Rev Mol Cell Biol. 2011 Oct 05;12(11):695-708
references: 21971041
references: Mol Microbiol. 2008 Nov;70(4):1037-50
references: 18976278
references: Nucleic Acids Res. 1998 Nov 15;26(22):5073-8
references: 9801302
references: J Proteome Res. 2011 Dec 2;10(12):5481-92
references: 21999169
references: Genes Dev. 2009 May 1;23(9):1131-44
references: 19417107