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Dendritic organization of actin comet tails

2001; Elsevier BV; Volume: 11; Issue: 2 Linguagem: Inglês

10.1016/s0960-9822(01)00022-7

1879-0445

Lisa Cameron, Tatyana Svitkina, Danijela Matic Vignjevic, Julie A. Theriot, Gary G. Borisy,

Biocrusts and Microbial Ecology

Polymerization of actin filaments is necessary for both protrusion of the leading edge of crawling cells and propulsion of certain intracellular pathogens [1Dramsi S. Cossart P. Intracellular pathogens and the actin cytoskeleton.Annu Rev Cell Dev Biol. 1998; 14: 137-166Crossref PubMed Scopus (189) Google Scholar], and it is sufficient for generating force for bacterial motility in vitro [2Loisel T.P. Boujemaa R. Pantaloni D. Carlier M.-F. Reconstitution of actin-based motility of Listeria and Shigella using pure proteins.Nature. 1999; 401: 613-616Crossref PubMed Scopus (778) Google Scholar]. Motile intracellular pathogens are associated with actin-rich comet tails containing many of the same molecular components present in lamellipodia [3Borisy G.G. Svitkina T.M. Actin machinery pushing the envelope.Curr Opin Cell Biol. 2000; 12: 104-112Crossref PubMed Scopus (395) Google Scholar], and this suggests that these two systems use a similar mechanism for motility. However, available structural evidence suggests that the organization of comet tails differs from that of lamellipodia. Actin filaments in lamellipodia form branched arrays [4Svitkina T.M. Verkhovsky A.B. McQuade K.M. Borisy G.G. Analysis of the actin-myosin II system in fish epidermal keratocytes mechanism of cell body translocation.J Cell Biol. 1997; 139: 397-415Crossref PubMed Scopus (532) Google Scholar], which are thought to arise by dendritic nucleation mediated by the Arp2/3 complex [5Mullins 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: 6181-6186Crossref PubMed Scopus (968) Google Scholar, 6Blanchoin L. Amann K.J. Higgs H.N. Marchand J.B. Kaiser D.A. Pollard T.D. Direct observation of dendritic actin filament networks nucleated by Arp2/3 complex and WASP/Scar proteins.Nature. 2000; 404: 1007-1011Crossref PubMed Scopus (420) Google Scholar]. In contrast, comet tails have been variously described as consisting of short, randomly oriented filaments [7Tilney L.G. Portnoy D.A. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes.J Cell Biol. 1989; 109: 1597-1608Crossref PubMed Scopus (909) Google Scholar], with a higher degree of alignment at the periphery [8Zhukarev V. Ashton F. Sanger J.M. Sanger J.W. Shuman H. Organization and structure of actin filament bundles in Listeria-infected cells.Cell Motil Cytoskeleton. 1995; 30: 229-246Crossref PubMed Scopus (34) Google Scholar], or as containing long, straight axial filaments with a small number of oblique filaments [9Sechi A.S. Wehland J. Small J.V. The isolated comet tail pseudopodium of Listeria monocytogenes a tail of two actin filament populations, long and axial and short and random.J Cell Biol. 1997; 137: 155-167Crossref PubMed Scopus (86) Google Scholar]. Because the assembly of pathogen-associated comet tails has been used as a model system for lamellipodial protrusion, it is important to resolve this apparent discrepancy. Here, using a platinum replica approach, we show that actin filament arrays in comet tails in fact have a dendritic organization with the Arp2/3 complex localizing to Y-junctions as in lamellipodia [10Svitkina T.M. Borisy G.G. Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia.J Cell Biol. 1999; 145: 1009-1026Crossref PubMed Scopus (864) Google Scholar]. Thus, comet tails and lamellipodia appear to share a common dendritic nucleation mechanism for protrusive motility. However, comet tails differ from lamellipodia in that their actin filaments are usually twisted and appear to be under significant torsional stress.