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 Verschoor; Catherine Leon; Christian Gachet; Thomas Gudermann; Michael Mederos y Schnitzler; Zachary Pincus; Matteo Iannacone; Rainer Haas; Gerhard Wanner; Kirsten Lauber; Michael Sixt; Steffen Massberg

doi:10.1016/j.cell.2017.11.001

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

^*Corresponding author for this work

Institute of Systemic Inflamation Research

287 Citations (Scopus)

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 language	English
Journal	Cell
Volume	171
Issue number	6
Pages (from-to)	1368-1382.e23
ISSN	0092-8674
DOIs	https://doi.org/10.1016/j.cell.2017.11.001
Publication status	Published - 30.11.2017

Funding

We thank Christin Lehmann, Anja Titova, Nicole Blount, and Cornelia Niemann for excellent technical assistance. We thank Reinhard Fässler, Barbara Walzog, Eva Kiermaier, and Joachim Pilcher for helpful discussions. This study was supported by the DFG SFB 914 (S.M. [B02 and Z01], K.S. [B02], R.T.B. [A05], A.V. [B04], and R. Haas [B05]), the DFG SFB 1123 (S.M. [B06]), the DFG FOR 2033 (S.M. and F.G.), the German Centre for Cardiovascular Research (DZHK) ( MHA 1.4VD [S.M.]), FP7 program (project 260309, PRESTIGE [S.M.]), FöFoLe project 947 (F.G.), the Friedrich-Baur-Stiftung project 41/16 (F.G.), Marie Skłodowska Curie Individual Fellowship ( EU project 747687 , LamelliActin [F.G.]).

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

Research Areas and Centers

Academic Focus: Center for Infection and Inflammation Research (ZIEL)

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10.1016/j.cell.2017.11.001

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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

@article{5041fa5174494a5fab4e5c8270540760,

title = "Migrating Platelets Are Mechano-scavengers that Collect and Bundle Bacteria",

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.",

author = "Florian Gaertner and Zerkah Ahmad and Gerhild Rosenberger and Shuxia Fan and Leo Nicolai and Benjamin Busch and G{\"o}kce Yavuz and Manja Luckner and Hellen Ishikawa-Ankerhold and Roman Hennel and Alexandre Benechet and Michael Lorenz and Sue Chandraratne and Irene Schubert and Sebastian Helmer and Bianca Striednig and Konstantin Stark and Marek Janko and B{\"o}ttcher, \{Ralph T.\} and Admar Verschoor and Catherine Leon and Christian Gachet and Thomas Gudermann and \{Mederos y Schnitzler\}, Michael and Zachary Pincus and Matteo Iannacone and Rainer Haas and Gerhard Wanner and Kirsten Lauber and Michael Sixt and Steffen Massberg",

note = "Funding Information: We thank Christin Lehmann, Anja Titova, Nicole Blount, and Cornelia Niemann for excellent technical assistance. We thank Reinhard F{\"a}ssler, Barbara Walzog, Eva Kiermaier, and Joachim Pilcher for helpful discussions. This study was supported by the DFG SFB 914 (S.M. [B02 and Z01], K.S. [B02], R.T.B. [A05], A.V. [B04], and R. Haas [B05]), the DFG SFB 1123 (S.M. [B06]), the DFG FOR 2033 (S.M. and F.G.), the German Centre for Cardiovascular Research (DZHK) ( MHA 1.4VD [S.M.]), FP7 program (project 260309, PRESTIGE [S.M.]), F{\"o}FoLe project 947 (F.G.), the Friedrich-Baur-Stiftung project 41/16 (F.G.), Marie Sk{\l}odowska Curie Individual Fellowship ( EU project 747687 , LamelliActin [F.G.]). Publisher Copyright: {\textcopyright} 2017 Elsevier Inc. Copyright: Copyright 2017 Elsevier B.V., All rights reserved.",

year = "2017",

month = nov,

day = "30",

doi = "10.1016/j.cell.2017.11.001",

language = "English",

volume = "171",

pages = "1368--1382.e23",

journal = "Cell",

issn = "0092-8674",

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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, RT, Verschoor, A, Leon, C, Gachet, C, Gudermann, T, Mederos y Schnitzler, M, Pincus, Z, Iannacone, M, Haas, R, Wanner, G, Lauber, K, Sixt, M & Massberg, S 2017, 'Migrating Platelets Are Mechano-scavengers that Collect and Bundle Bacteria', Cell, vol. 171, no. 6, pp. 1368-1382.e23. https://doi.org/10.1016/j.cell.2017.11.001

TY - JOUR

T1 - Migrating Platelets Are Mechano-scavengers that Collect and Bundle Bacteria

AU - Gaertner, Florian

AU - Ahmad, Zerkah

AU - Rosenberger, Gerhild

AU - Fan, Shuxia

AU - Nicolai, Leo

AU - Busch, Benjamin

AU - Yavuz, Gökce

AU - Luckner, Manja

AU - Ishikawa-Ankerhold, Hellen

AU - Hennel, Roman

AU - Benechet, Alexandre

AU - Lorenz, Michael

AU - Chandraratne, Sue

AU - Schubert, Irene

AU - Helmer, Sebastian

AU - Striednig, Bianca

AU - Stark, Konstantin

AU - Janko, Marek

AU - Böttcher, Ralph T.

AU - Verschoor, Admar

AU - Leon, Catherine

AU - Gachet, Christian

AU - Gudermann, Thomas

AU - Mederos y Schnitzler, Michael

AU - Pincus, Zachary

AU - Iannacone, Matteo

AU - Haas, Rainer

AU - Wanner, Gerhard

AU - Lauber, Kirsten

AU - Sixt, Michael

AU - Massberg, Steffen

N1 - Funding Information: We thank Christin Lehmann, Anja Titova, Nicole Blount, and Cornelia Niemann for excellent technical assistance. We thank Reinhard Fässler, Barbara Walzog, Eva Kiermaier, and Joachim Pilcher for helpful discussions. This study was supported by the DFG SFB 914 (S.M. [B02 and Z01], K.S. [B02], R.T.B. [A05], A.V. [B04], and R. Haas [B05]), the DFG SFB 1123 (S.M. [B06]), the DFG FOR 2033 (S.M. and F.G.), the German Centre for Cardiovascular Research (DZHK) ( MHA 1.4VD [S.M.]), FP7 program (project 260309, PRESTIGE [S.M.]), FöFoLe project 947 (F.G.), the Friedrich-Baur-Stiftung project 41/16 (F.G.), Marie Skłodowska Curie Individual Fellowship ( EU project 747687 , LamelliActin [F.G.]). Publisher Copyright: © 2017 Elsevier Inc. Copyright: Copyright 2017 Elsevier B.V., All rights reserved.

PY - 2017/11/30

Y1 - 2017/11/30

N2 - 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.

AB - 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.

UR - https://www.scopus.com/pages/publications/85036574507

U2 - 10.1016/j.cell.2017.11.001

DO - 10.1016/j.cell.2017.11.001

M3 - Journal articles

C2 - 29195076

AN - SCOPUS:85036574507

SN - 0092-8674

VL - 171

SP - 1368-1382.e23

JO - Cell

JF - Cell

IS - 6

ER -

Migrating Platelets Are Mechano-scavengers that Collect and Bundle Bacteria

Abstract

Funding

UN SDGs

Research Areas and Centers

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