Bone-Marrow-Resident NK Cells Prime Monocytes for Regulatory Function during Infection.

Michael H Askenase; Seong-Ji Han; Allyson L Byrd; Denise Morais da Fonseca; Nicolas Bouladoux; Christoph Wilhelm; Joanne E Konkel; Timothy W Hand; Norinne Lacerda-Queiroz; Xin-zhuan Su; Giorgio Trinchieri; John R Grainger; Yasmine Belkaid

doi:10.1016/j.immuni.2015.05.011

Bone-Marrow-Resident NK Cells Prime Monocytes for Regulatory Function during Infection.

Michael H Askenase, Seong-Ji Han, Allyson L Byrd, Denise Morais da Fonseca, Nicolas Bouladoux, Christoph Wilhelm, Joanne E Konkel, Timothy W Hand, Norinne Lacerda-Queiroz, Xin-zhuan Su, Giorgio Trinchieri, John R Grainger, Yasmine Belkaid

Research output: Contribution to journal › Article › peer-review

Abstract

Tissue-infiltrating Ly6C(hi) monocytes play diverse roles in immunity, ranging from pathogen killing to immune regulation. How and where this diversity of function is imposed remains poorly understood. Here we show that during acute gastrointestinal infection, priming of monocytes for regulatory function preceded systemic inflammation and was initiated prior to bone marrow egress. Notably, natural killer (NK) cell-derived IFN-γ promoted a regulatory program in monocyte progenitors during development. Early bone marrow NK cell activation was controlled by systemic interleukin-12 (IL-12) produced by Batf3-dependent dendritic cells (DCs) in the mucosal-associated lymphoid tissue (MALT). This work challenges the paradigm that monocyte function is dominantly imposed by local signals after tissue recruitment, and instead proposes a sequential model of differentiation in which monocytes are pre-emptively educated during development in the bone marrow to promote their tissue-specific function.

Original language	English
Pages (from-to)	1130-1142
Journal	Immunity
Volume	42
Issue number	6
DOIs	https://doi.org/10.1016/j.immuni.2015.05.011
Publication status	Published - 16 Jun 2015

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title = "Bone-Marrow-Resident NK Cells Prime Monocytes for Regulatory Function during Infection.",

abstract = "Tissue-infiltrating Ly6C(hi) monocytes play diverse roles in immunity, ranging from pathogen killing to immune regulation. How and where this diversity of function is imposed remains poorly understood. Here we show that during acute gastrointestinal infection, priming of monocytes for regulatory function preceded systemic inflammation and was initiated prior to bone marrow egress. Notably, natural killer (NK) cell-derived IFN-γ promoted a regulatory program in monocyte progenitors during development. Early bone marrow NK cell activation was controlled by systemic interleukin-12 (IL-12) produced by Batf3-dependent dendritic cells (DCs) in the mucosal-associated lymphoid tissue (MALT). This work challenges the paradigm that monocyte function is dominantly imposed by local signals after tissue recruitment, and instead proposes a sequential model of differentiation in which monocytes are pre-emptively educated during development in the bone marrow to promote their tissue-specific function.",

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AU - Askenase, Michael H

AU - Han, Seong-Ji

AU - Byrd, Allyson L

AU - Morais da Fonseca, Denise

AU - Bouladoux, Nicolas

AU - Wilhelm, Christoph

AU - Konkel, Joanne E

AU - Hand, Timothy W

AU - Lacerda-Queiroz, Norinne

AU - Su, Xin-zhuan

AU - Trinchieri, Giorgio

AU - Grainger, John R

AU - Belkaid, Yasmine

N1 - Z99 AI999999, Intramural NIH HHS, United States

PY - 2015/6/16

Y1 - 2015/6/16

N2 - Tissue-infiltrating Ly6C(hi) monocytes play diverse roles in immunity, ranging from pathogen killing to immune regulation. How and where this diversity of function is imposed remains poorly understood. Here we show that during acute gastrointestinal infection, priming of monocytes for regulatory function preceded systemic inflammation and was initiated prior to bone marrow egress. Notably, natural killer (NK) cell-derived IFN-γ promoted a regulatory program in monocyte progenitors during development. Early bone marrow NK cell activation was controlled by systemic interleukin-12 (IL-12) produced by Batf3-dependent dendritic cells (DCs) in the mucosal-associated lymphoid tissue (MALT). This work challenges the paradigm that monocyte function is dominantly imposed by local signals after tissue recruitment, and instead proposes a sequential model of differentiation in which monocytes are pre-emptively educated during development in the bone marrow to promote their tissue-specific function.

AB - Tissue-infiltrating Ly6C(hi) monocytes play diverse roles in immunity, ranging from pathogen killing to immune regulation. How and where this diversity of function is imposed remains poorly understood. Here we show that during acute gastrointestinal infection, priming of monocytes for regulatory function preceded systemic inflammation and was initiated prior to bone marrow egress. Notably, natural killer (NK) cell-derived IFN-γ promoted a regulatory program in monocyte progenitors during development. Early bone marrow NK cell activation was controlled by systemic interleukin-12 (IL-12) produced by Batf3-dependent dendritic cells (DCs) in the mucosal-associated lymphoid tissue (MALT). This work challenges the paradigm that monocyte function is dominantly imposed by local signals after tissue recruitment, and instead proposes a sequential model of differentiation in which monocytes are pre-emptively educated during development in the bone marrow to promote their tissue-specific function.

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SN - 1097-4180

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SP - 1130

EP - 1142

JO - Immunity

JF - Immunity

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ER -

Bone-Marrow-Resident NK Cells Prime Monocytes for Regulatory Function during Infection.

Abstract

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