Register      Login
Australian Journal of Chemistry Australian Journal of Chemistry Society
An international journal for chemical science
Shopping Cart: ( empty )
You are here: Home > Journals > CH > CH19409
REVIEW
Contents Vol 73(3)

Force Measurement of Living Professional Phagocytes of the Immune System

Anna Mularski A B C D and Florence Niedergang A B C
+ Author Affiliations
- Author Affiliations

A Institut National de la Santé et de la Recherche Médicale (Inserm), U1016, Institut Cochin, Paris 75014, France.

B Centre National de la Recherche Scientifique (CNRS), UMR 8104, Paris 75014, France.

C Université Paris Descartes, Sorbonne Paris Cité, Paris 75014, France.

D Corresponding author. Email: anna.mularski@gmail.com




Anna Mularski obtained her Ph.D. from the School of Chemistry at the University of Melbourne in 2016. Her research focused on studying the interaction of antimicrobial peptides with live bacterial cells using atomic force microscopy. Her post-doctoral work at Institut Cochin, Paris, involved using traction force microscopy to study phagocytosing macrophages. Anna’s current post-doctoral research at the University of Southern Denmark, Odense, focuses on atomic force microscopy studies of annexin-membrane interactions.


Florence Niedergang studied immunology and cell biology. She obtained her Ph.D. in 1997, studying T cell activation at Institut Pasteur. As a post-doctoral fellow at the University of Lausanne, she investigated the role of gut phagocytes in bacterial survival. She joined Institut Cochin (Inserm/ CNRS/ Université Paris Descartes) as a group leader in 2005. She is now director of the ‘Infection, Immunity and Inflammation’ department and scientific director of the IMAG’IC photonic imaging facility of Institut Cochin. Her present work focuses on the mechanisms of internalization and activation of phagocytic cells in normal and pathological conditions such as viral infections leading to bacterial super-infections.

Australian Journal of Chemistry 73(3) 104-111 https://doi.org/10.1071/CH19409
Submitted: 21 August 2019  Accepted: 30 October 2019   Published: 7 January 2020

Abstract

In higher organisms, the professional phagocytes of the immune system (dendritic cells, neutrophils, monocytes, and macrophages) are responsible for pathogen clearance, the development of immune responses via cytokine secretion and presentation of antigens derived from internalized material, and the normal turnover and remodelling of tissues and disposal of dead cells. These functions rely on the ability of phagocytes to migrate and adhere to sites of infection, dynamically probe their environments to make contact with phagocytic targets, and perform phagocytosis, a mechanism of internalization of large particles, microorganisms, and cellular debris for intracellular degradation. The cell-generated forces that are necessary for the professional phagocytes to act in their roles as ‘first responders’ of the immune system have been the subject of mechanical studies in recent years. Methods of force measurement such as atomic force microscopy, traction force microscopy, micropipette aspiration, magnetic and optical tweezers, and exciting new variants of these have accompanied classical biological methods to perform mechanical investigations of these highly dynamic immune cells.


References

[1]  R. S. Flannagan, V. Jaumouille, S. Grinstein, Annu. Rev. Pathol.: Mech. Dis. 2012, 7, 61.
         | Crossref | GoogleScholarGoogle Scholar |

[2]  F. Niedergang, in Encyclopedia of Cell Biology (Eds R. Bradshaw, P. Stahl) 2016, pp. 751–757 (Academic Press: Waltham, MA).

[3]  I. K. H. Poon, C. D. Lucas, A. G. Rossi, K. S. Ravichandran, Nat. Rev. Immunol. 2014, 14, 166.
         | Crossref | GoogleScholarGoogle Scholar |

[4]  D. A. Bloes, D. Kretschmer, A. Peschel, Nat. Rev. Microbiol. 2015, 13, 95.
         | Crossref | GoogleScholarGoogle Scholar | 25534805PubMed |

[5]  B. Heit, L. Liu, P. Colarusso, K. D. Puri, P. Kubes, J. Cell Sci. 2008, 121, 205.
         | Crossref | GoogleScholarGoogle Scholar | 18187452PubMed |

[6]  T. Devosse, A. Guillabert, N. Haene, A. Berton, P. De Nadai, S. Noel, M. Brait, J.-D. Franssen, S. Sozzani, I. Salmon, M. Parmentier, J. Immunol. 2009, 182, 4974.
         | Crossref | GoogleScholarGoogle Scholar | 19342677PubMed |

[7]  A. J. Ridley, FEBS Lett. 2001, 498, 168.
         | Crossref | GoogleScholarGoogle Scholar | 11412850PubMed |

[8]  A. J. Ridley, M. A. Schwartz, K. Burridge, R. A. Firtel, M. H. Ginsberg, G. Borisy, J. T. Parsons, A. R. Horwitz, Science 2003, 302, 1704.
         | Crossref | GoogleScholarGoogle Scholar | 14657486PubMed |

[9]  R. J. Pelham, Yl. Wang, Proc. Natl. Acad. Sci. USA 1997, 94, 13661.
         | Crossref | GoogleScholarGoogle Scholar | 9391082PubMed |

[10]  C. A. Reinhart‐King, in Methods in Enzymology (Ed. D. A. Cheresh) 2008, Vol. 443, Ch. 3, pp. 45–64 (Academic Press: New York, NY).

[11]  C. A. Reinhart-King, M. Dembo, D. A. Hammer, Biophys. J. 2005, 89, 676.
         | Crossref | GoogleScholarGoogle Scholar | 15849250PubMed |

[12]  C. M. Lo, H.-B. Wang, M. Dembo, Y.-l. Wang, Biophys. J. 2000, 79, 144.
         | Crossref | GoogleScholarGoogle Scholar | 10866943PubMed |

[13]  D. A. Lauffenburger, J. J. Linderman, Receptors: Models for Binding, Trafficking, and Signaling 1993 (Oxford University Press: Oxford).

[14]  C. M. Bidan, M. Fratzl, A. Coullomb, P. Moreau, A. H. Lombard, I. Wang, M. Balland, T. Boudou, N. M. Dempsey, T. Devillers, A. Dupont, Sci. Rep. 2018, 8, 1464.
         | Crossref | GoogleScholarGoogle Scholar | 29362476PubMed |

[15]  M. Kohyama, W. Ise, B. T. Edelson, P. R. Wilker, K. Hildner, C. Mejia, W. A. Frazier, T. L. Murphy, K. M. Murphy, Nature 2009, 457, 318.
         | Crossref | GoogleScholarGoogle Scholar | 19037245PubMed |

[16]  M. Bilzer, F. Roggel, A. L. Gerbes, Liver Int. 2006, 26, 1175.
         | Crossref | GoogleScholarGoogle Scholar | 17105582PubMed |

[17]  M. Y. Gerner, P. Torabi-Parizi, R. N. Germain, Immunity 2015, 42, 172.
         | Crossref | GoogleScholarGoogle Scholar | 25607462PubMed |

[18]  R. S. Flannagan, R. E. Harrison, C. M. Yip, K. Jaqaman, S. Grinstein, J. Cell Biol. 2010, 191, 1205.
         | Crossref | GoogleScholarGoogle Scholar | 21135140PubMed |

[19]  Y. I. Miller, M. K. Chang, C. D. Funk, J. R. Feramisco, J. L. Witztum, J. Biol. Chem. 2001, 276, 19431.
         | Crossref | GoogleScholarGoogle Scholar | 11278875PubMed |

[20]  A. Nimmerjahn, F. Kirchhoff, F. Helmchen, Science 2005, 308, 1314.
         | Crossref | GoogleScholarGoogle Scholar | 15831717PubMed |

[21]  J. Jubrail, K. Montauban, P. Regis-Burgel, N. Kurian, F. Niedergang, Eur. Respir. J. 2016, 48, PA1824.

[22]  I. Tabas, C. K. Glass, Science 2013, 339, 166.
         | Crossref | GoogleScholarGoogle Scholar | 23307734PubMed |

[23]  J. K. Jubrail, N. Kurian, F. Niedergang, Biomed. J. 2017, 40, 305.
         | Crossref | GoogleScholarGoogle Scholar |

[24]  R. S. Flannagan, G. Cosio, S. Grinstein, Nat. Rev. Microbiol. 2009, 7, 355.
         | Crossref | GoogleScholarGoogle Scholar | 19369951PubMed |

[25]  J. W. Pollard, Nat. Rev. Immunol. 2009, 9, 259.
         | Crossref | GoogleScholarGoogle Scholar | 19282852PubMed |

[26]  A. Mularski, F. Marie-Anaïs, J. Mazzolini, F. Niedergang, in Methods in Molecular Biology (Ed. G. Rousselet) 2018, pp. 165–175 (Springer: Berlin).

[27]  W. J. Polacheck, C. S. Chen, Nat. Methods 2016, 13, 415.
         | Crossref | GoogleScholarGoogle Scholar | 27123817PubMed |

[28]  W. R. Legant, C. K. Choi, J. S. Miller, L. Shao, L. Gao, E. Betzig, C. S. Chen, Proc. Natl. Acad. Sci. USA 2013, 110, 881.
         | Crossref | GoogleScholarGoogle Scholar | 23277584PubMed |

[29]  J. Toyjanova, E. Bar-Kochba, C. López-Fagundo, J. Reichner, D. Hoffman-Kim, C. Franck, PLoS One 2014, 9, e90976.
         | Crossref | GoogleScholarGoogle Scholar | 24740435PubMed |

[30]  S. A. Maskarinec, C. Franck, D. A. Tirrell, G. Ravichandran, Proc. Natl. Acad. Sci. USA 2009, 106, 22108.
         | Crossref | GoogleScholarGoogle Scholar | 20018765PubMed |

[31]  W. R. Legant, J. S. Miller, B. L. Blakely, D. M. Cohen, G. M. Genin, C. S. Chen, Nat. Methods 2010, 7, 969.
         | Crossref | GoogleScholarGoogle Scholar | 21076420PubMed |

[32]  J. L. Martiel, A. Leal, L. Kurzawa, M. Balland, I. Wang, T. Vignaud, Q. Tseng, M. Thery, Methods Cell Biol. 2015, 125, 269.
         | Crossref | GoogleScholarGoogle Scholar | 25640434PubMed |

[33]  D. T. Kovari, W. Wei, P. Chang, J. S. Toro, R. F. Beach, D. Chambers, K. Porter, D. Koo, J. E. Curtis, Biophys. J. 2016, 111, 2698.
         | Crossref | GoogleScholarGoogle Scholar | 28002746PubMed |

[34]  L. E. Hind, M. Dembo, D. A. Hammer, Integr. Biol. 2015, 7, 447.
         | Crossref | GoogleScholarGoogle Scholar |

[35]  L. E. Hind, E. B. Lurier, M. Dembo, K. L. Spiller, D. A. Hammer, Cell. Mol. Bioeng. 2016, 9, 455.
         | Crossref | GoogleScholarGoogle Scholar | 28458726PubMed |

[36]  L. A. Smith, H. Aranda-Espinoza, J. B. Haun, M. Dembo, D. A. Hammer, Biophys. J. 2007, 92, L58.
         | Crossref | GoogleScholarGoogle Scholar | 17218464PubMed |

[37]  R. A. Jannat, M. Dembo, D. A. Hammer, Biophys. J. 2011, 101, 575.
         | Crossref | GoogleScholarGoogle Scholar | 21806925PubMed |

[38]  M. Gupta, L. Kocgozlu, B. R. Sarangi, F. Margadant, M. Ashraf, B. Ladoux, in Methods in Cell Biology (Ed. E. K. Paluch) 2015, Vol. 125, Ch. 16, pp. 289–308 (Academic Press: New York, NY).

[39]  B. G. Ricart, M. T. Yang, C. A. Hunter, C. S. Chen, D. A. Hammer, Biophys. J. 2011, 101, 2620.
         | Crossref | GoogleScholarGoogle Scholar | 22261049PubMed |

[40]  C. Cougoule, E. Van Goethem, V. Le Cabec, F. Lafouresse, L. Dupré, V. Mehraj, J.-L. Mège, C. Lastrucci, I. Maridonneau-Parini, Eur. J. Cell Biol. 2012, 91, 938.
         | Crossref | GoogleScholarGoogle Scholar | 22999511PubMed |

[41]  E. Desvignes, A. Bouissou, A. Laborde, T. Mangeat, A. Proag, C. Vieu, C. Thibault, I. Maridonneau-Parini, R. Poincloux, Nano Lett. 2018, 18, 6326.
         | Crossref | GoogleScholarGoogle Scholar | 30232897PubMed |

[42]  D. Molino, S. Quignard, C. Gruget, F. Pincet, Y. Chen, M. Piel, J. Fattaccioli, Sci. Rep. 2016, 6, 29113.
         | Crossref | GoogleScholarGoogle Scholar | 27373558PubMed |

[43]  R. Buccione, J. D. Orth, M. A. McNiven, Nat. Rev. Mol. Cell Biol. 2004, 5, 647.
         | Crossref | GoogleScholarGoogle Scholar | 15366708PubMed |

[44]  Y. F. Dufrene, T. Ando, R. Garcia, D. Alsteens, D. Martinez-Martin, A. Engel, C. Gerber, D. J. Müller, Nat. Nanotechnol. 2017, 12, 295.
         | Crossref | GoogleScholarGoogle Scholar | 28383040PubMed |

[45]  A. Labernadie, C. Thibault, C. Vieu, I. Maridonneau-Parini, G. M. Charrière, Proc. Natl. Acad. Sci. USA 2010, 107, 21016.
         | Crossref | GoogleScholarGoogle Scholar | 21081699PubMed |

[46]  A. Labernadie, A. Bouissou, P. Delobelle, S. Balor, R. Voituriez, A. Proag, I. Fourquaux, C. Thibault, C. Vieu, R. Poincloux, G. M. Charrière, I. Maridonneau-Parini, Nat. Commun. 2014, 5, 5343.
         | Crossref | GoogleScholarGoogle Scholar | 25385672PubMed |

[47]  H. Kress, E. H. K. Stelzer, G. Griffiths, A. Rohrbach, Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 2005, 71, 061927.
         | Crossref | GoogleScholarGoogle Scholar | 16089785PubMed |

[48]  T. M. Svitkina, E. A. Bulanova, O. Y. Chaga, D. M. Vignjevic, S.-i. Kojima, J. M. Vasiliev, G. G. Borisy, J. Cell Biol. 2003, 160, 409.
         | Crossref | GoogleScholarGoogle Scholar | 12566431PubMed |

[49]  D. Cojoc, F. Difato, E. Ferrari, R. B. Shahapure, J. Laishram, M. Righi, E. M. Di Fabrizio, V. Torre, PLoS One 2007, 2, e1072.
         | Crossref | GoogleScholarGoogle Scholar | 17957254PubMed |

[50]  L. Vonna, A. Wiedemann, M. Aepfelbacher, E. Sackmann, Eur. Biophys. J. 2007, 36, 145.
         | Crossref | GoogleScholarGoogle Scholar | 17160406PubMed |

[51]  H. Kress, E. H. K. Stelzer, D. Holzer, F. Buss, G. Griffiths, A. Rohrbach, Proc. Natl. Acad. Sci. USA 2007, 104, 11633.
         | Crossref | GoogleScholarGoogle Scholar | 17620618PubMed |

[52]  K. O. Holevinsky, D. J. Nelson, Biophys. J. 1998, 75, 2577.
         | Crossref | GoogleScholarGoogle Scholar | 9788954PubMed |

[53]  L. Bajno, X.-R. Peng, A. D. Schreiber, H.-P. Moore, W. S. Trimble, S. Grinstein, J. Cell Biol. 2000, 149, 697.
         | Crossref | GoogleScholarGoogle Scholar | 10791982PubMed |

[54]  V. Braun, V. Fraisier, G. Raposo, I. Hurbain, J.-B. Sibarita, P. Chavrier, T. Galli, F. Niedergang, EMBO J. 2004, 23, 4166.
         | Crossref | GoogleScholarGoogle Scholar | 15470500PubMed |

[55]  M. Herant, V. Heinrich, M. Dembo, J. Cell Sci. 2005, 118, 1789.
         | Crossref | GoogleScholarGoogle Scholar | 15827090PubMed |

[56]  S. Marion, J. Mazzolini, F. Herit, P. Bourdoncle, N. Kambou-Pene, S. Hailfinger, M. Sachse, J. Ruland, A. Benmerah, A. Echard, M. Thome, F. Niedergang, Dev. Cell 2012, 23, 954.
         | Crossref | GoogleScholarGoogle Scholar | 23153494PubMed |

[57]  R. Levin, S. Grinstein, J. Canton, Immunol. Rev. 2016, 273, 156.
         | Crossref | GoogleScholarGoogle Scholar | 27558334PubMed |

[58]  E. Evans, A. Leung, D. Zhelev, J. Cell Biol. 1993, 122, 1295.
         | Crossref | GoogleScholarGoogle Scholar | 8376464PubMed |

[59]  N. Araki, T. Hatae, A. Furukawa, J. A. Swanson, J. Cell Sci. 2003, 116, 247.
         | Crossref | GoogleScholarGoogle Scholar | 12482911PubMed |

[60]  J. A. Swanson, M. T. Johnson, K. Beningo, P. Post, M. Mooseker, N. Araki, J. Cell Sci. 1999, 112, 307.
         | 9885284PubMed |

[61]  M. Diakonova, G. Bokoch, J. A. Swanson, Mol. Biol. Cell 2002, 13, 402.
         | Crossref | GoogleScholarGoogle Scholar | 11854399PubMed |

[62]  J. Boulais, M. Trost, C. Landry, R. Dieckmann, E. Levy, T. Soldati, S. Michnick, P. Thibault, M. Desjardins, Mol. Syst. Biol. 2010, 6, 423.
         | Crossref | GoogleScholarGoogle Scholar | 20959821PubMed |

[63]  N. Gopaldass, D. Patel, R. Kratzke, R. Dieckmann, S. Hausherr, M. Hagedorn, R. Monroy, J. Krüger, E. M. Neuhaus, E. Hoffmann, K. Hille, S. A. Kuznetsov, T. Soldati, Traffic 2012, 13, 120.
         | Crossref | GoogleScholarGoogle Scholar | 22008230PubMed |

[64]  S. R. Barger, N. S. Reilly, M. S. Shutova, Q. Li, P. Maiuri, J. M. Heddleston, M. S. Mooseker, R. A. Flavell, T. Svitkina, P. W. Oakes, M. Krendel, N. C. Gauthier, Nat. Commun. 2019, 10, 1249.
         | Crossref | GoogleScholarGoogle Scholar | 30890704PubMed |

[65]  I. M. Olazabal, E. Caron, R. C. May, K. Schilling, D. A. Knecht, L. M. Machesky, Curr. Biol. 2002, 12, 1413.
         | Crossref | GoogleScholarGoogle Scholar | 12194823PubMed |

[66]  M. Herant, V. Heinrich, M. Dembo, J. Cell Sci. 2006, 119, 1903.
         | Crossref | GoogleScholarGoogle Scholar | 16636075PubMed |

[67]  D. V. Zhelev, D. Needham, R. M. Hochmuth, Biophys. J. 1994, 67, 696.
         | Crossref | GoogleScholarGoogle Scholar | 7948682PubMed |

[68]  M. Herant, C. Y. Lee, M. Dembo, V. Heinrich, PLOS Comput. Biol. 2011, 7, e1001068.
         | Crossref | GoogleScholarGoogle Scholar | 21298079PubMed |

[69]  L. A. Allen, A. Aderem, J. Exp. Med. 1996, 184, 627.
         | Crossref | GoogleScholarGoogle Scholar | 8760816PubMed |

[70]  T. A. Masters, B. Pontes, V. Viasnoff, Y. Li, N. C. Gauthier, Proc. Natl. Acad. Sci. USA 2013, 110, 11875.
         | Crossref | GoogleScholarGoogle Scholar | 23821745PubMed |

[71]  F. Marie-Anaïs, J. Mazzolini, F. Herit, F. Niedergang, Traffic 2016, 17, 487.
         | Crossref | GoogleScholarGoogle Scholar | 26847957PubMed |

[72]  K. Guevorkian, J. L. Maître, in Methods in Cell Biology (Ed. T. Lecuit) 2017, Vol. 139, pp. 187–201 (Academic Press: New York, NY).

[73]  M. Herant, W. A. Marganski, M. Dembo, Biophys. J. 2003, 84, 3389.
         | Crossref | GoogleScholarGoogle Scholar | 12719267PubMed |

[74]  D. Vorselen, Y. Wang, M. M. de Jesus, P. K. Shah, M. J. Footer, M. Huse, W. Cai, J. A. Theriot, bioRxiv 2019, 431221.
         | Crossref | GoogleScholarGoogle Scholar |