Dual-Track Clearance of Circulating Bacteria Balances Rapid Restoration of Blood Sterility with Induction of Adaptive Immunity

Steven P. Broadley; Ann Plaumann; Raffaele Coletti; Christin Lehmann; Andreas Wanisch; Amelie Seidlmeier; Knud Esser; Shanshan Luo; Patrick C. Rämer; Steffen Massberg; Dirk H. Busch; Menno van Lookeren Campagne; Admar Verschoor

doi:10.1016/j.chom.2016.05.023

Dual-Track Clearance of Circulating Bacteria Balances Rapid Restoration of Blood Sterility with Induction of Adaptive Immunity

Steven P. Broadley, Ann Plaumann, Raffaele Coletti, Christin Lehmann, Andreas Wanisch, Amelie Seidlmeier, Knud Esser, Shanshan Luo, Patrick C. Rämer, Steffen Massberg, Dirk H. Busch, Menno van Lookeren Campagne, Admar Verschoor^*

^*Corresponding author for this work

Institute of Systemic Inflamation Research

127 Citations (Scopus)

Abstract

Efficient clearance of bacteremia prevents life-threatening disease. Platelet binding to intravascular bacteria, a process involving platelet glycoprotein GPIb and bacterial opsonization with activated complement C3, influences blood clearance and anti-infective immunity. Using intravital microscopy of the bloodstream of mice infected with Listeria monocytogenes, we show that bacterial clearance is not a uniform process but a “dual-track” mechanism consisting of parallel “fast” and “slow” pathways. “Slow clearance” is regulated by time-dependent bacterial opsonization, stochastic platelet binding, and capture of bacteria-platelet-complexes via the complement receptor of the immunoglobulin superfamily, CRIg. The mechanism spares some bacteria from “fast clearance” and rapid destruction in the liver via Kupffer cell scavenger receptors, keeping them available for adaptive immunity induction by splenic CD8α⁺ dendritic cells. We consistently find “fast” and “slow” clearance patterns for a broad panel of other Gram+ and Gram− bacteria. Thus, dual-track clearance balances rapid restoration of blood sterility with induction of specific antibacterial immunity.

Original language	English
Journal	Cell Host and Microbe
Volume	20
Issue number	1
Pages (from-to)	36-48
Number of pages	13
ISSN	1931-3128
DOIs	https://doi.org/10.1016/j.chom.2016.05.023
Publication status	Published - 13.07.2016

Funding

We thank S. Gordon (Oxford) for input and critical discussion; M.C. Carroll (Harvard Medical School), S. Gordon (Oxford University), C.M. Ballantyne (Baylor College of Medicine), and B. Nieswandt (University of Würzburg) for kindly providing mouse strains; the diagnostics department of the Institute for Medical Microbiology, Immunology and Hygiene (Technische Universität München) for providing ATCC bacterial reference strains; L. Henkel, M. Schiemann, and I. Andrae for expert flow cytometry cell sorting; and P. Graef for experimental assistance. We gratefully acknowledge support by the Technische Universität München Graduate School. Funded by German Research Foundation (DFG) grant SFB 914 (projects Z01 and B02) to S.M. and (project B04) to D.H.B. and A.V. M.L.C. is a current employee of Genentech, Inc. but has no financial conflict of interest.

Research Areas and Centers

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

UN SDGs

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

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10.1016/j.chom.2016.05.023

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Broadley, S. P., Plaumann, A., Coletti, R., Lehmann, C., Wanisch, A., Seidlmeier, A., Esser, K., Luo, S., Rämer, P. C., Massberg, S., Busch, D. H., van Lookeren Campagne, M., & Verschoor, A. (2016). Dual-Track Clearance of Circulating Bacteria Balances Rapid Restoration of Blood Sterility with Induction of Adaptive Immunity. Cell Host and Microbe, 20(1), 36-48. https://doi.org/10.1016/j.chom.2016.05.023

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abstract = "Efficient clearance of bacteremia prevents life-threatening disease. Platelet binding to intravascular bacteria, a process involving platelet glycoprotein GPIb and bacterial opsonization with activated complement C3, influences blood clearance and anti-infective immunity. Using intravital microscopy of the bloodstream of mice infected with Listeria monocytogenes, we show that bacterial clearance is not a uniform process but a “dual-track” mechanism consisting of parallel “fast” and “slow” pathways. “Slow clearance” is regulated by time-dependent bacterial opsonization, stochastic platelet binding, and capture of bacteria-platelet-complexes via the complement receptor of the immunoglobulin superfamily, CRIg. The mechanism spares some bacteria from “fast clearance” and rapid destruction in the liver via Kupffer cell scavenger receptors, keeping them available for adaptive immunity induction by splenic CD8α+ dendritic cells. We consistently find “fast” and “slow” clearance patterns for a broad panel of other Gram+ and Gram− bacteria. Thus, dual-track clearance balances rapid restoration of blood sterility with induction of specific antibacterial immunity.",

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Broadley, SP, Plaumann, A, Coletti, R, Lehmann, C, Wanisch, A, Seidlmeier, A, Esser, K, Luo, S, Rämer, PC, Massberg, S, Busch, DH, van Lookeren Campagne, M & Verschoor, A 2016, 'Dual-Track Clearance of Circulating Bacteria Balances Rapid Restoration of Blood Sterility with Induction of Adaptive Immunity', Cell Host and Microbe, vol. 20, no. 1, pp. 36-48. https://doi.org/10.1016/j.chom.2016.05.023

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T1 - Dual-Track Clearance of Circulating Bacteria Balances Rapid Restoration of Blood Sterility with Induction of Adaptive Immunity

AU - Broadley, Steven P.

AU - Plaumann, Ann

AU - Coletti, Raffaele

AU - Lehmann, Christin

AU - Wanisch, Andreas

AU - Seidlmeier, Amelie

AU - Esser, Knud

AU - Luo, Shanshan

AU - Rämer, Patrick C.

AU - Massberg, Steffen

AU - Busch, Dirk H.

AU - van Lookeren Campagne, Menno

AU - Verschoor, Admar

PY - 2016/7/13

Y1 - 2016/7/13

N2 - Efficient clearance of bacteremia prevents life-threatening disease. Platelet binding to intravascular bacteria, a process involving platelet glycoprotein GPIb and bacterial opsonization with activated complement C3, influences blood clearance and anti-infective immunity. Using intravital microscopy of the bloodstream of mice infected with Listeria monocytogenes, we show that bacterial clearance is not a uniform process but a “dual-track” mechanism consisting of parallel “fast” and “slow” pathways. “Slow clearance” is regulated by time-dependent bacterial opsonization, stochastic platelet binding, and capture of bacteria-platelet-complexes via the complement receptor of the immunoglobulin superfamily, CRIg. The mechanism spares some bacteria from “fast clearance” and rapid destruction in the liver via Kupffer cell scavenger receptors, keeping them available for adaptive immunity induction by splenic CD8α+ dendritic cells. We consistently find “fast” and “slow” clearance patterns for a broad panel of other Gram+ and Gram− bacteria. Thus, dual-track clearance balances rapid restoration of blood sterility with induction of specific antibacterial immunity.

AB - Efficient clearance of bacteremia prevents life-threatening disease. Platelet binding to intravascular bacteria, a process involving platelet glycoprotein GPIb and bacterial opsonization with activated complement C3, influences blood clearance and anti-infective immunity. Using intravital microscopy of the bloodstream of mice infected with Listeria monocytogenes, we show that bacterial clearance is not a uniform process but a “dual-track” mechanism consisting of parallel “fast” and “slow” pathways. “Slow clearance” is regulated by time-dependent bacterial opsonization, stochastic platelet binding, and capture of bacteria-platelet-complexes via the complement receptor of the immunoglobulin superfamily, CRIg. The mechanism spares some bacteria from “fast clearance” and rapid destruction in the liver via Kupffer cell scavenger receptors, keeping them available for adaptive immunity induction by splenic CD8α+ dendritic cells. We consistently find “fast” and “slow” clearance patterns for a broad panel of other Gram+ and Gram− bacteria. Thus, dual-track clearance balances rapid restoration of blood sterility with induction of specific antibacterial immunity.

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Dual-Track Clearance of Circulating Bacteria Balances Rapid Restoration of Blood Sterility with Induction of Adaptive Immunity

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