Migrating Platelets Are Mechano-scavengers that Collect and Bundle Bacteria

Florian Gaertner, Zerkah Ahmad, Gerhild Rosenberger, Shuxia Fan, Leo Nicolai, Benjamin Busch, Gökce Yavuz, Manja Luckner, Hellen Ishikawa-Ankerhold, Roman Hennel, Alexandre Benechet, Michael Lorenz, Sue Chandraratne, Irene Schubert, Sebastian Helmer, Bianca Striednig, Konstantin Stark, Marek Janko, Ralph T. Böttcher, Admar VerschoorCatherine Leon, Christian Gachet, Thomas Gudermann, Michael Mederos y Schnitzler, Zachary Pincus, Matteo Iannacone, Rainer Haas, Gerhard Wanner, Kirsten Lauber, Michael Sixt, Steffen Massberg

Research output: Contribution to journalArticle

87 Scopus citations

Abstract

Blood platelets are critical for hemostasis and thrombosis and play diverse roles during immune responses. Despite these versatile tasks in mammalian biology, their skills on a cellular level are deemed limited, mainly consisting in rolling, adhesion, and aggregate formation. Here, we identify an unappreciated asset of platelets and show that adherent platelets use adhesion receptors to mechanically probe the adhesive substrate in their local microenvironment. When actomyosin-dependent traction forces overcome substrate resistance, platelets migrate and pile up the adhesive substrate together with any bound particulate material. They use this ability to act as cellular scavengers, scanning the vascular surface for potential invaders and collecting deposited bacteria. Microbe collection by migrating platelets boosts the activity of professional phagocytes, exacerbating inflammatory tissue injury in sepsis. This assigns platelets a central role in innate immune responses and identifies them as potential targets to dampen inflammatory tissue damage in clinical scenarios of severe systemic infection. In addition to their role in thrombosis and hemostasis, platelets can also migrate to sites of infection to help trap bacteria and clear the vascular surface.

Original languageEnglish
Pages (from-to)1368-1382.e23
JournalCell
Volume171
Issue number6
DOIs
StatePublished - Nov 30 2017

Keywords

  • NETosis
  • cell migration
  • host-defense
  • innate immunity
  • mechanosensing
  • methicillin-resistant S. aureus
  • neutrophils
  • platelets
  • polarization
  • sepsis

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    Gaertner, F., Ahmad, Z., Rosenberger, G., Fan, S., Nicolai, L., Busch, B., Yavuz, G., Luckner, M., Ishikawa-Ankerhold, H., Hennel, R., Benechet, A., Lorenz, M., Chandraratne, S., Schubert, I., Helmer, S., Striednig, B., Stark, K., Janko, M., Böttcher, R. T., ... Massberg, S. (2017). Migrating Platelets Are Mechano-scavengers that Collect and Bundle Bacteria. Cell, 171(6), 1368-1382.e23. https://doi.org/10.1016/j.cell.2017.11.001