Skip to main content
Log in

Micromechanics of filopodia mediated capture of pathogens by macrophages

  • Article
  • Published:
European Biophysics Journal Aims and scope Submit manuscript

Abstract

The biological function of filopodia has been extensively studied while only little work has been done on their mechanical properties. In the present study, we apply magnetic microbeads to explore the capturing and initial step of phagocytosis of pathogens by macrophages through filopodia. Microbeads were covered by the bacterial coat protein invasin which is known to trigger the invasion of the intestine by the bacteria Yersinia enterocolitica. These mimetics of bacteria were placed in the vicinity of J774 mouse macrophages exhibiting long filopodia. The specific adhesion of beads to the tip of a filopodium induced the retraction of the protrusion resulting in the dragging of the bead towards the cell body. The dynamics of the retraction process was analyzed by following the in-plane motion of the bead. We estimated the minimal force developed by filopodia and compared the results with previous magnetic tweezer studies of mechanical force induced growth of protrusions (Vonna et al. 2003). We show that very thin filopodia can generate astonishingly large retraction forces over large distances (>10 μm) and can act as an efficient mechanical tool to detach pathogens adhering on surfaces.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Chenevier P, Veyret B, Roux D, Henry-Toulmé N (2000) Interation of cationic colloids at the surface of J774 cells: a kinetic analysis. Biophys J 79:1298–1309

    Google Scholar 

  • Dai J, Sheetz MP (1999) Membrane tether formation from blebbing cells. Biophys J 77:3363–3370

    Google Scholar 

  • Davenport RW, Ping-Dou, Rehder V, Kater SB (1993) A sensory role for neuronal growth cone filopodia. Nature 361:721–724

    Article  ADS  Google Scholar 

  • De Joussineau C, Soulé J, Martin M, Anguille C, Montcourrier P, Alexandre D (2003) Delta-promoted filopodia mediate long-range lateral inhibition in Drosophila. Nature 426:555–559

    Article  ADS  Google Scholar 

  • Evans E, Leung A, Zhelev D (1993) Synchrony of cell spreading and contraction force as phagocytes engulf large pathogens. J Cell Biol 122:1295–1300

    Article  Google Scholar 

  • Gomez TM, Robles E, Poo MM, Spitzer NC (2001) Filopodial calcium transients promote substrate-dependent growth cone turning. Science 291:1983–1987

    Article  ADS  Google Scholar 

  • Herant M, Heinrich V, Dembo M (2006) Mechanics of neutrophil phagocytosis: experiments and quantitative models. J Cell Sci 119:1903–1913

    Article  Google Scholar 

  • Koerten HK, Ploem JS, Daems WT (1980) Ingestion of latex beads by filopodia of adherent mouse peritoneal macrophages. A scanning electron microscopical and reflection contrast microscopical study. Exp Cell Res 128:470–475

    Article  Google Scholar 

  • Lo CM, Wang HB, Dembo M, Wang YL (2000) Cell movement is guided by the rigidity of the substrate. Biophys J 79:144–152

    Google Scholar 

  • Loisel TP, Boujemaa R, Pantaloni D, Carlier MF (1999) Reconstitution of actin-based motility of Listeria and Shigella using pure proteins. Nature 401:613–616

    Article  ADS  Google Scholar 

  • Mallavarapu A, Mitchisona T (1999) Regulated actin cytoskeleton assembly at filopodium tips controls their extension and retraction. J Cell Biol 146:1097–1106

    Article  Google Scholar 

  • Miller J, Fraser SE, McClay D (1995) Dynamics of thin filopodia during sea urchin gastrulation. Development 121:2501–2511

    Google Scholar 

  • Miller YI, Chang MK, Funk CD, Feramisco JR, Witztum JL (2001) 12/15-lipoxygenase translocation enhances site-specific actin polymerization in macrophages phagocytosing apoptotic cells. J Biol Chem 276:19431–19439

    Article  Google Scholar 

  • Niedergang F, Chavrier P (2005) Regulation of phagocytosis by Rho GTPases. Curr Top Microbiol Immunol 291:43–60

    Article  Google Scholar 

  • Pepe JC, Miller VL (1993) Yersinia enterocolitica invasin: a primary role in the initiation of infection. Proc Natl Acad Sci USA 90:6473–6477

    Article  ADS  Google Scholar 

  • Ramirez-Weber FA, Kornberg TB (1999) Cytonemes: cellular processes that project to the principal signaling center in Drosophila imaginal discs. Cell 97:599–607

    Article  Google Scholar 

  • Sengupta K, Schilling J, Marx S, Fischer M, Bacher A, Sackmann E (2003) Mimicking tissue surfaces by supported membrane coupled ultrathin layer of Hyaluronic acid. Langmuir 19:1775–1781

    Article  Google Scholar 

  • Stopak D, Wessells NK, Harris AK (1985) Morphogenetic rearrangement of injected collagen in developing chicken limb buds. Proc Natl Acad Sci U S A 82:2804–2808

    Article  ADS  Google Scholar 

  • Svitkina TM, Bulanova EA, Chaga OY, Vignjevic DM, Kojima S, Vasiliev JM, Borisy GG (2003) Mechanism of filopodia initiation by reorganization of a dendritic network. J Cell Biol 160:409–421

    Article  Google Scholar 

  • Swanson JA, Johnson MT, Beningo K, Post P, Mooseker M, Araki N (1999) A contractile activity that closes phagosomes in macrophages. J Cell Sci 112:307–316

    Google Scholar 

  • Vonna L, Wiedemann A, Aepfelbacher M, Sackmann E (2003) Local force induced conical protrusions of phagocytic cells. J Cell Sci 116:785–790

    Article  Google Scholar 

  • Wago H (1984) In vitro evidence for the requirement of filopodial elongation for the progress of phagocytosis by phagocytic granular cells of the silkworm, Bombyx Mori. Dev Comp Immunol 8:7–14

    Article  Google Scholar 

  • Wiedemann A, Linder S, Grassl G, Albert M, Autenrieth I, Aepfelbacher M (2001) Yersinia enterocolitica invasin triggers phagocytosis via beta1 integrins, CDC42Hs and WASp in macrophages. Cell Microbiol 3:693–702

    Article  Google Scholar 

  • Young VB, Falkow S, Schoolnik GK (1992) The invasin protein of Yersinia enterocolitica: internalization of invasin-bearing bacteria by eukaryotic cells is associated with reorganization of the cytoskeleton. J Cell Biol 116:197–207

    Article  Google Scholar 

  • Zhelev DV, Hochmuth RM (1995) Mechanically stimulated cytoskeleton rearrangement and cortical contraction in human neutrophils. Biophys J 68:2004–14

    Article  Google Scholar 

Download references

Acknowledgments

The work was supported by the Deutsche Forschungsgemeinschaft (SFB 413) and the Fonds der Chemicher Industrie. Laurent Vonna acknowledges the fellowship received by the Alexander von Humboldt Foundation and the European Community (MCFI-1999–00252).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. Vonna.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vonna, L., Wiedemann, A., Aepfelbacher, M. et al. Micromechanics of filopodia mediated capture of pathogens by macrophages. Eur Biophys J 36, 145–151 (2007). https://doi.org/10.1007/s00249-006-0118-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00249-006-0118-y

Keywords

Navigation