Bone Marrow Mesenchymal Stem and Progenitor Cells Induce Monocyte Emigration in Response to Circulating Toll-like Receptor Ligands

Chao Shi, Ting Jia, Simon Mendez-Ferrer, Tobias M. Hohl, Natalya V. Serbina, Lauren Lipuma, Ingrid Leiner, Ming O. Li, Paul S. Frenette, Eric G. Pamer

Research output: Contribution to journalArticle

274 Citations (Scopus)

Abstract

Inflammatory (Ly6Chi CCR2+) monocytes provide defense against infections but also contribute to autoimmune diseases and atherosclerosis. Monocytes originate from bone marrow and their entry into the bloodstream requires stimulation of CCR2 chemokine receptor by monocyte chemotactic protein-1 (MCP1). How monocyte emigration from bone marrow is triggered by remote infections remains unclear. We demonstrated that low concentrations of Toll-like receptor (TLR) ligands in the bloodstream drive CCR2-dependent emigration of monocytes from bone marrow. Bone marrow mesenchymal stem cells (MSCs) and their progeny, including CXC chemokine ligand (CXCL)12-abundant reticular (CAR) cells, rapidly expressed MCP1 in response to circulating TLR ligands or bacterial infection and induced monocyte trafficking into the bloodstream. Targeted deletion of MCP1 from MSCs impaired monocyte emigration from bone marrow. Our findings suggest that bone marrow MSCs and CAR cells respond to circulating microbial molecules and regulate bloodstream monocyte frequencies by secreting MCP1 in proximity to bone marrow vascular sinuses.

Original languageEnglish (US)
Pages (from-to)590-601
Number of pages12
JournalImmunity
Volume34
Issue number4
DOIs
StatePublished - Apr 22 2011

Fingerprint

Toll-Like Receptors
Emigration and Immigration
Mesenchymal Stromal Cells
Monocytes
Bone Marrow
Ligands
Chemokine CCL2
CCR2 Receptors
CXC Chemokines
Chemokine Receptors
Infection
Bacterial Infections
Autoimmune Diseases
Blood Vessels
Atherosclerosis

ASJC Scopus subject areas

  • Immunology and Allergy
  • Infectious Diseases
  • Immunology

Cite this

Shi, C., Jia, T., Mendez-Ferrer, S., Hohl, T. M., Serbina, N. V., Lipuma, L., ... Pamer, E. G. (2011). Bone Marrow Mesenchymal Stem and Progenitor Cells Induce Monocyte Emigration in Response to Circulating Toll-like Receptor Ligands. Immunity, 34(4), 590-601. https://doi.org/10.1016/j.immuni.2011.02.016

Bone Marrow Mesenchymal Stem and Progenitor Cells Induce Monocyte Emigration in Response to Circulating Toll-like Receptor Ligands. / Shi, Chao; Jia, Ting; Mendez-Ferrer, Simon; Hohl, Tobias M.; Serbina, Natalya V.; Lipuma, Lauren; Leiner, Ingrid; Li, Ming O.; Frenette, Paul S.; Pamer, Eric G.

In: Immunity, Vol. 34, No. 4, 22.04.2011, p. 590-601.

Research output: Contribution to journalArticle

Shi, C, Jia, T, Mendez-Ferrer, S, Hohl, TM, Serbina, NV, Lipuma, L, Leiner, I, Li, MO, Frenette, PS & Pamer, EG 2011, 'Bone Marrow Mesenchymal Stem and Progenitor Cells Induce Monocyte Emigration in Response to Circulating Toll-like Receptor Ligands', Immunity, vol. 34, no. 4, pp. 590-601. https://doi.org/10.1016/j.immuni.2011.02.016
Shi, Chao ; Jia, Ting ; Mendez-Ferrer, Simon ; Hohl, Tobias M. ; Serbina, Natalya V. ; Lipuma, Lauren ; Leiner, Ingrid ; Li, Ming O. ; Frenette, Paul S. ; Pamer, Eric G. / Bone Marrow Mesenchymal Stem and Progenitor Cells Induce Monocyte Emigration in Response to Circulating Toll-like Receptor Ligands. In: Immunity. 2011 ; Vol. 34, No. 4. pp. 590-601.
@article{c2c0a67121754707bacad70b8bb3af69,
title = "Bone Marrow Mesenchymal Stem and Progenitor Cells Induce Monocyte Emigration in Response to Circulating Toll-like Receptor Ligands",
abstract = "Inflammatory (Ly6Chi CCR2+) monocytes provide defense against infections but also contribute to autoimmune diseases and atherosclerosis. Monocytes originate from bone marrow and their entry into the bloodstream requires stimulation of CCR2 chemokine receptor by monocyte chemotactic protein-1 (MCP1). How monocyte emigration from bone marrow is triggered by remote infections remains unclear. We demonstrated that low concentrations of Toll-like receptor (TLR) ligands in the bloodstream drive CCR2-dependent emigration of monocytes from bone marrow. Bone marrow mesenchymal stem cells (MSCs) and their progeny, including CXC chemokine ligand (CXCL)12-abundant reticular (CAR) cells, rapidly expressed MCP1 in response to circulating TLR ligands or bacterial infection and induced monocyte trafficking into the bloodstream. Targeted deletion of MCP1 from MSCs impaired monocyte emigration from bone marrow. Our findings suggest that bone marrow MSCs and CAR cells respond to circulating microbial molecules and regulate bloodstream monocyte frequencies by secreting MCP1 in proximity to bone marrow vascular sinuses.",
author = "Chao Shi and Ting Jia and Simon Mendez-Ferrer and Hohl, {Tobias M.} and Serbina, {Natalya V.} and Lauren Lipuma and Ingrid Leiner and Li, {Ming O.} and Frenette, {Paul S.} and Pamer, {Eric G.}",
year = "2011",
month = "4",
day = "22",
doi = "10.1016/j.immuni.2011.02.016",
language = "English (US)",
volume = "34",
pages = "590--601",
journal = "Immunity",
issn = "1074-7613",
publisher = "Cell Press",
number = "4",

}

TY - JOUR

T1 - Bone Marrow Mesenchymal Stem and Progenitor Cells Induce Monocyte Emigration in Response to Circulating Toll-like Receptor Ligands

AU - Shi, Chao

AU - Jia, Ting

AU - Mendez-Ferrer, Simon

AU - Hohl, Tobias M.

AU - Serbina, Natalya V.

AU - Lipuma, Lauren

AU - Leiner, Ingrid

AU - Li, Ming O.

AU - Frenette, Paul S.

AU - Pamer, Eric G.

PY - 2011/4/22

Y1 - 2011/4/22

N2 - Inflammatory (Ly6Chi CCR2+) monocytes provide defense against infections but also contribute to autoimmune diseases and atherosclerosis. Monocytes originate from bone marrow and their entry into the bloodstream requires stimulation of CCR2 chemokine receptor by monocyte chemotactic protein-1 (MCP1). How monocyte emigration from bone marrow is triggered by remote infections remains unclear. We demonstrated that low concentrations of Toll-like receptor (TLR) ligands in the bloodstream drive CCR2-dependent emigration of monocytes from bone marrow. Bone marrow mesenchymal stem cells (MSCs) and their progeny, including CXC chemokine ligand (CXCL)12-abundant reticular (CAR) cells, rapidly expressed MCP1 in response to circulating TLR ligands or bacterial infection and induced monocyte trafficking into the bloodstream. Targeted deletion of MCP1 from MSCs impaired monocyte emigration from bone marrow. Our findings suggest that bone marrow MSCs and CAR cells respond to circulating microbial molecules and regulate bloodstream monocyte frequencies by secreting MCP1 in proximity to bone marrow vascular sinuses.

AB - Inflammatory (Ly6Chi CCR2+) monocytes provide defense against infections but also contribute to autoimmune diseases and atherosclerosis. Monocytes originate from bone marrow and their entry into the bloodstream requires stimulation of CCR2 chemokine receptor by monocyte chemotactic protein-1 (MCP1). How monocyte emigration from bone marrow is triggered by remote infections remains unclear. We demonstrated that low concentrations of Toll-like receptor (TLR) ligands in the bloodstream drive CCR2-dependent emigration of monocytes from bone marrow. Bone marrow mesenchymal stem cells (MSCs) and their progeny, including CXC chemokine ligand (CXCL)12-abundant reticular (CAR) cells, rapidly expressed MCP1 in response to circulating TLR ligands or bacterial infection and induced monocyte trafficking into the bloodstream. Targeted deletion of MCP1 from MSCs impaired monocyte emigration from bone marrow. Our findings suggest that bone marrow MSCs and CAR cells respond to circulating microbial molecules and regulate bloodstream monocyte frequencies by secreting MCP1 in proximity to bone marrow vascular sinuses.

UR - http://www.scopus.com/inward/record.url?scp=79954591540&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=79954591540&partnerID=8YFLogxK

U2 - 10.1016/j.immuni.2011.02.016

DO - 10.1016/j.immuni.2011.02.016

M3 - Article

C2 - 21458307

AN - SCOPUS:79954591540

VL - 34

SP - 590

EP - 601

JO - Immunity

JF - Immunity

SN - 1074-7613

IS - 4

ER -