Origin of the Lamina Propria Dendritic Cell Network

Milena Bogunovic; Florent Ginhoux; Julie Helft; Limin Shang; Daigo Hashimoto; Melanie Greter; Kang Liu; Claudia Jakubzick; Molly A. Ingersoll; Marylene Leboeuf; E. Richard Stanley; Michel Nussenzweig; Sergio A. Lira; Gwendalyn J. Randolph; Miriam Merad

doi:10.1016/j.immuni.2009.08.010

Origin of the Lamina Propria Dendritic Cell Network

Milena Bogunovic, Florent Ginhoux, Julie Helft, Limin Shang, Daigo Hashimoto, Melanie Greter, Kang Liu, Claudia Jakubzick, Molly A. Ingersoll, Marylene Leboeuf, E. Richard Stanley, Michel Nussenzweig, Sergio A. Lira, Gwendalyn J. Randolph, Miriam Merad

Developmental & Molecular Biology

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

712 Scopus citations

Abstract

CX₃CR1⁺ and CD103⁺ dendritic cells (DCs) in intestinal lamina propria play a key role in mucosal immunity. However, the origin and the developmental pathways that regulate their differentiation in the lamina propria remain unclear. We showed that monocytes gave rise exclusively to CD103^-CX₃CR1⁺ lamina propria DCs under the control of macrophage-colony-stimulating factor receptor (M-CSFR) and Fms-like thyrosine kinase 3 (Flt3) ligands. In contrast, common DC progenitors (CDP) and pre-DCs, which give rise to lymphoid organ DCs but not to monocytes, differentiated exclusively into CD103⁺CX₃CR1^- lamina propria DCs under the control of Flt3 and granulocyte-macrophage-colony-stimulating factor receptor (GM-CSFR) ligands. CD103⁺CX₃CR1^- DCs but not CD103^-CX₃CR1⁺ DCs in the lamina propria constitutively expressed CCR7 and were the first DCs to transport pathogenic Salmonella from the intestinal tract to the mesenteric lymph nodes. Altogether, these results underline the diverse origin of the lamina propria DC network and identify mucosal DCs that arise from pre-DCs as key sentinels of the gut immune system.

Original language	English (US)
Pages (from-to)	513-525
Number of pages	13
Journal	Immunity
Volume	31
Issue number	3
DOIs	https://doi.org/10.1016/j.immuni.2009.08.010
State	Published - Sep 18 2009

Keywords

CELLIMMUNO
MOLIMMUNO

ASJC Scopus subject areas

Immunology and Allergy
Immunology
Infectious Diseases

UN SDGs

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

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10.1016/j.immuni.2009.08.010

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@article{d1e2ec2f434546f495f879a099cfe521,

title = "Origin of the Lamina Propria Dendritic Cell Network",

abstract = "CX3CR1+ and CD103+ dendritic cells (DCs) in intestinal lamina propria play a key role in mucosal immunity. However, the origin and the developmental pathways that regulate their differentiation in the lamina propria remain unclear. We showed that monocytes gave rise exclusively to CD103-CX3CR1+ lamina propria DCs under the control of macrophage-colony-stimulating factor receptor (M-CSFR) and Fms-like thyrosine kinase 3 (Flt3) ligands. In contrast, common DC progenitors (CDP) and pre-DCs, which give rise to lymphoid organ DCs but not to monocytes, differentiated exclusively into CD103+CX3CR1- lamina propria DCs under the control of Flt3 and granulocyte-macrophage-colony-stimulating factor receptor (GM-CSFR) ligands. CD103+CX3CR1- DCs but not CD103-CX3CR1+ DCs in the lamina propria constitutively expressed CCR7 and were the first DCs to transport pathogenic Salmonella from the intestinal tract to the mesenteric lymph nodes. Altogether, these results underline the diverse origin of the lamina propria DC network and identify mucosal DCs that arise from pre-DCs as key sentinels of the gut immune system.",

keywords = "CELLIMMUNO, MOLIMMUNO",

author = "Milena Bogunovic and Florent Ginhoux and Julie Helft and Limin Shang and Daigo Hashimoto and Melanie Greter and Kang Liu and Claudia Jakubzick and Ingersoll, {Molly A.} and Marylene Leboeuf and Stanley, {E. Richard} and Michel Nussenzweig and Lira, {Sergio A.} and Randolph, {Gwendalyn J.} and Miriam Merad",

note = "Funding Information: We would like to thank Y. Yokota (University of Fukui, Fukui, Japan) for providing the Id2 −/− mice. M.M. is supported by NIH grants CA112100 and CA086899. E.R.S. is supported by NIH grants CA32551 and CA26504. M.B. is supported by a grant from the Amy Strelzer Foundation. F.G. is supported by a grant from the Leukemia and Lymphoma Society (LLS 3220-08). K.L. was supported by a C.H.Li Memorial Scholarship Award from The Rockefeller University. M.N. is an HHMI investigator. M.A.I. was supported by an institutional training grant from the NIDDK. S.A.L. was supported by P01 DK072201, and G.J.R. was supported by NIH grant AI49653 and AHA Established Investigator grant 0740052. ",

year = "2009",

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doi = "10.1016/j.immuni.2009.08.010",

language = "English (US)",

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pages = "513--525",

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T1 - Origin of the Lamina Propria Dendritic Cell Network

AU - Bogunovic, Milena

AU - Ginhoux, Florent

AU - Helft, Julie

AU - Shang, Limin

AU - Hashimoto, Daigo

AU - Greter, Melanie

AU - Liu, Kang

AU - Jakubzick, Claudia

AU - Ingersoll, Molly A.

AU - Leboeuf, Marylene

AU - Stanley, E. Richard

AU - Nussenzweig, Michel

AU - Lira, Sergio A.

AU - Randolph, Gwendalyn J.

AU - Merad, Miriam

N1 - Funding Information: We would like to thank Y. Yokota (University of Fukui, Fukui, Japan) for providing the Id2 −/− mice. M.M. is supported by NIH grants CA112100 and CA086899. E.R.S. is supported by NIH grants CA32551 and CA26504. M.B. is supported by a grant from the Amy Strelzer Foundation. F.G. is supported by a grant from the Leukemia and Lymphoma Society (LLS 3220-08). K.L. was supported by a C.H.Li Memorial Scholarship Award from The Rockefeller University. M.N. is an HHMI investigator. M.A.I. was supported by an institutional training grant from the NIDDK. S.A.L. was supported by P01 DK072201, and G.J.R. was supported by NIH grant AI49653 and AHA Established Investigator grant 0740052.

PY - 2009/9/18

Y1 - 2009/9/18

N2 - CX3CR1+ and CD103+ dendritic cells (DCs) in intestinal lamina propria play a key role in mucosal immunity. However, the origin and the developmental pathways that regulate their differentiation in the lamina propria remain unclear. We showed that monocytes gave rise exclusively to CD103-CX3CR1+ lamina propria DCs under the control of macrophage-colony-stimulating factor receptor (M-CSFR) and Fms-like thyrosine kinase 3 (Flt3) ligands. In contrast, common DC progenitors (CDP) and pre-DCs, which give rise to lymphoid organ DCs but not to monocytes, differentiated exclusively into CD103+CX3CR1- lamina propria DCs under the control of Flt3 and granulocyte-macrophage-colony-stimulating factor receptor (GM-CSFR) ligands. CD103+CX3CR1- DCs but not CD103-CX3CR1+ DCs in the lamina propria constitutively expressed CCR7 and were the first DCs to transport pathogenic Salmonella from the intestinal tract to the mesenteric lymph nodes. Altogether, these results underline the diverse origin of the lamina propria DC network and identify mucosal DCs that arise from pre-DCs as key sentinels of the gut immune system.

AB - CX3CR1+ and CD103+ dendritic cells (DCs) in intestinal lamina propria play a key role in mucosal immunity. However, the origin and the developmental pathways that regulate their differentiation in the lamina propria remain unclear. We showed that monocytes gave rise exclusively to CD103-CX3CR1+ lamina propria DCs under the control of macrophage-colony-stimulating factor receptor (M-CSFR) and Fms-like thyrosine kinase 3 (Flt3) ligands. In contrast, common DC progenitors (CDP) and pre-DCs, which give rise to lymphoid organ DCs but not to monocytes, differentiated exclusively into CD103+CX3CR1- lamina propria DCs under the control of Flt3 and granulocyte-macrophage-colony-stimulating factor receptor (GM-CSFR) ligands. CD103+CX3CR1- DCs but not CD103-CX3CR1+ DCs in the lamina propria constitutively expressed CCR7 and were the first DCs to transport pathogenic Salmonella from the intestinal tract to the mesenteric lymph nodes. Altogether, these results underline the diverse origin of the lamina propria DC network and identify mucosal DCs that arise from pre-DCs as key sentinels of the gut immune system.

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KW - MOLIMMUNO

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ER -

Origin of the Lamina Propria Dendritic Cell Network

Abstract

Keywords

ASJC Scopus subject areas

UN SDGs

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