Literature DB >> 18385381

The role of filament-packing dynamics in powering amoeboid cell motility.

Long Miao1, Orion Vanderlinde, Jun Liu, Richard P Grant, Alan Wouterse, Katsuya Shimabukuro, Albert Philipse, Murray Stewart, Thomas M Roberts.   

Abstract

Although several models have been proposed to account for how cytoskeleton polymerization drives protrusion in cell motility, the precise mechanism remains controversial. Here, we show that, in addition to force exerted directly against the membrane by growing filaments, the way elongating filaments pack also contributes to protrusion by generating an expansion of the cytoskeleton gel. Tomography shows that filament packing in the major sperm protein (MSP) -based nematode sperm-motility machinery resembles that observed with rigid rods. Maximum rod-packing density decreases dramatically as the rods lengthen. Therefore, as filaments elongate, the cytoskeleton gel expands to accommodate their packing less densely. This volume expansion combines with polymerization to drive protrusion. Consistent with this hypothesis, an engineered MSP mutant that generates shorter filaments shows higher filament-packing density and slower movement.

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Year:  2008        PMID: 18385381      PMCID: PMC2291107          DOI: 10.1073/pnas.0708416105

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  34 in total

Review 1.  Cellular motility driven by assembly and disassembly of actin filaments.

Authors:  Thomas D Pollard; Gary G Borisy
Journal:  Cell       Date:  2003-02-21       Impact factor: 41.582

2.  2.6 A resolution crystal structure of helices of the motile major sperm protein (MSP) of Caenorhabditis elegans.

Authors:  Anne M E Baker; Thomas M Roberts; Murray Stewart
Journal:  J Mol Biol       Date:  2002-05-31       Impact factor: 5.469

Review 3.  The actin slingshot.

Authors:  Julie Plastino; Cécile Sykes
Journal:  Curr Opin Cell Biol       Date:  2005-02       Impact factor: 8.382

4.  Arp2/3 complex-deficient mouse fibroblasts are viable and have normal leading-edge actin structure and function.

Authors:  Alessia Di Nardo; Gregor Cicchetti; Hervé Falet; John H Hartwig; Thomas P Stossel; David J Kwiatkowski
Journal:  Proc Natl Acad Sci U S A       Date:  2005-10-27       Impact factor: 11.205

Review 5.  On the edge: modeling protrusion.

Authors:  Alex Mogilner
Journal:  Curr Opin Cell Biol       Date:  2005-11-28       Impact factor: 8.382

Review 6.  The great escape: when cancer cells hijack the genes for chemotaxis and motility.

Authors:  John Condeelis; Robert H Singer; Jeffrey E Segall
Journal:  Annu Rev Cell Dev Biol       Date:  2005       Impact factor: 13.827

7.  A conformational change in the actin subunit can change the flexibility of the actin filament.

Authors:  A Orlova; E H Egelman
Journal:  J Mol Biol       Date:  1993-07-20       Impact factor: 5.469

8.  ATP hydrolysis on actin-related protein 2/3 complex causes debranching of dendritic actin arrays.

Authors:  Christophe Le Clainche; Dominique Pantaloni; Marie-France Carlier
Journal:  Proc Natl Acad Sci U S A       Date:  2003-05-12       Impact factor: 11.205

9.  A unique cytoskeleton associated with crawling in the amoeboid sperm of the nematode, Ascaris suum.

Authors:  S Sepsenwol; H Ris; T M Roberts
Journal:  J Cell Biol       Date:  1989-01       Impact factor: 10.539

10.  Structure and macromolecular assembly of two isoforms of the major sperm protein (MSP) from the amoeboid sperm of the nematode, Ascaris suum.

Authors:  K L King; M Stewart; T M Roberts; M Seavy
Journal:  J Cell Sci       Date:  1992-04       Impact factor: 5.285

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  6 in total

1.  Simulation of cell motility that reproduces the force-velocity relationship.

Authors:  Christian H Schreiber; Murray Stewart; Thomas Duke
Journal:  Proc Natl Acad Sci U S A       Date:  2010-05-03       Impact factor: 11.205

2.  Biochemical mechanisms for regulating protrusion by nematode major sperm protein.

Authors:  Jelena Stajic; Charles W Wolgemuth
Journal:  Biophys J       Date:  2009-08-05       Impact factor: 4.033

3.  Cytosolic Ca(2+) as a multifunctional modulator is required for spermiogenesis in Ascaris suum.

Authors:  Yunlong Shang; Lianwan Chen; Zhiyu Liu; Xia Wang; Xuan Ma; Long Miao
Journal:  Protein Cell       Date:  2013-05-20       Impact factor: 14.870

4.  Sperm Lysozyme-Like Protein 1 (SLLP1), an intra-acrosomal oolemmal-binding sperm protein, reveals filamentous organization in protein crystal form.

Authors:  H Zheng; A Mandal; I A Shumilin; M D Chordia; S Panneerdoss; J C Herr; W Minor
Journal:  Andrology       Date:  2015-07       Impact factor: 3.842

5.  Dephosphorylation of major sperm protein (MSP) fiber protein 3 by protein phosphatase 2A during cell body retraction in the MSP-based amoeboid motility of Ascaris sperm.

Authors:  Kexi Yi; Xu Wang; Mark R Emmett; Alan G Marshall; Murray Stewart; Thomas M Roberts
Journal:  Mol Biol Cell       Date:  2009-05-20       Impact factor: 4.138

Review 6.  Cytoskeletal cross-linking and bundling in motor-independent contraction.

Authors:  Sean X Sun; Sam Walcott; Charles W Wolgemuth
Journal:  Curr Biol       Date:  2010-08-10       Impact factor: 10.834

  6 in total

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