CCR2+ monocytes infiltrate atrophic lesions in age‐related macular disease and mediate photoreceptor degeneration in experimental subretinal inflammation in Cx3cr1 deficient mice

Abstract Atrophic age‐related macular degeneration (AMD) is associated with the subretinal accumulation of mononuclear phagocytes (MPs). Their role in promoting or inhibiting retinal degeneration is unknown. We here show that atrophic AMD is associated with increased intraocular CCL2 levels and subr...

Full description

Saved in:
Bibliographic Details
Main Authors: Florian Sennlaub, Constance Auvynet, Bertrand Calippe, Sophie Lavalette, Lucie Poupel, Shulong J. Hu, Elisa Dominguez, Serge Camelo, Olivier Levy, Elodie Guyon, Noah Saederup, Israel F. Charo, Nico Van Rooijen, Emeline Nandrot, Jean‐Louis Bourges, Francine Behar‐Cohen, José‐Alain Sahel, Xavier Guillonneau, William Raoul, Christophe Combadiere
Format: Article
Language:English
Published: Springer Nature 2013-10-01
Series:EMBO Molecular Medicine
Subjects:
Online Access:https://doi.org/10.1002/emmm.201302692
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850179378021924864
author Florian Sennlaub
Constance Auvynet
Bertrand Calippe
Sophie Lavalette
Lucie Poupel
Shulong J. Hu
Elisa Dominguez
Serge Camelo
Olivier Levy
Elodie Guyon
Noah Saederup
Israel F. Charo
Nico Van Rooijen
Emeline Nandrot
Jean‐Louis Bourges
Francine Behar‐Cohen
José‐Alain Sahel
Xavier Guillonneau
William Raoul
Christophe Combadiere
author_facet Florian Sennlaub
Constance Auvynet
Bertrand Calippe
Sophie Lavalette
Lucie Poupel
Shulong J. Hu
Elisa Dominguez
Serge Camelo
Olivier Levy
Elodie Guyon
Noah Saederup
Israel F. Charo
Nico Van Rooijen
Emeline Nandrot
Jean‐Louis Bourges
Francine Behar‐Cohen
José‐Alain Sahel
Xavier Guillonneau
William Raoul
Christophe Combadiere
author_sort Florian Sennlaub
collection DOAJ
description Abstract Atrophic age‐related macular degeneration (AMD) is associated with the subretinal accumulation of mononuclear phagocytes (MPs). Their role in promoting or inhibiting retinal degeneration is unknown. We here show that atrophic AMD is associated with increased intraocular CCL2 levels and subretinal CCR2+ inflammatory monocyte infiltration in patients. Using age‐ and light‐induced subretinal inflammation and photoreceptor degeneration in Cx3cr1 knockout mice, we show that subretinal Cx3cr1 deficient MPs overexpress CCL2 and that both the genetic deletion of CCL2 or CCR2 and the pharmacological inhibition of CCR2 prevent inflammatory monocyte recruitment, MP accumulation and photoreceptor degeneration in vivo. Our study shows that contrary to CCR2 and CCL2, CX3CR1 is constitutively expressed in the retina where it represses the expression of CCL2 and the recruitment of neurotoxic inflammatory CCR2+ monocytes. CCL2/CCR2 inhibition might represent a powerful tool for controlling inflammation and neurodegeneration in AMD.
format Article
id doaj-art-2ff2d9d1430a4fa785a7b34aa7d9d130
institution OA Journals
issn 1757-4676
1757-4684
language English
publishDate 2013-10-01
publisher Springer Nature
record_format Article
series EMBO Molecular Medicine
spelling doaj-art-2ff2d9d1430a4fa785a7b34aa7d9d1302025-08-20T02:18:31ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842013-10-015111775179310.1002/emmm.201302692CCR2+ monocytes infiltrate atrophic lesions in age‐related macular disease and mediate photoreceptor degeneration in experimental subretinal inflammation in Cx3cr1 deficient miceFlorian Sennlaub0Constance Auvynet1Bertrand Calippe2Sophie Lavalette3Lucie Poupel4Shulong J. Hu5Elisa Dominguez6Serge Camelo7Olivier Levy8Elodie Guyon9Noah Saederup10Israel F. Charo11Nico Van Rooijen12Emeline Nandrot13Jean‐Louis Bourges14Francine Behar‐Cohen15José‐Alain Sahel16Xavier Guillonneau17William Raoul18Christophe Combadiere19Inserm, U 968Inserm, U 968Inserm, U 968Inserm, U 968Inserm UMR_S 945, Laboratoire Immunité et InfectionInserm, U 968Inserm, U 968Inserm, U 968Inserm, U 968Inserm, U 968Gladstone Institute of Cardiovascular Disease, San FranciscoGladstone Institute of Cardiovascular Disease, San FranciscoDepartment of Molecular Cell Biology, Free University Medical CenterInserm, U 968Hôtel Dieu, Service d'Ophtalmologie, Centre de Recherche OphtalmologiqueHôtel Dieu, Service d'Ophtalmologie, Centre de Recherche OphtalmologiqueInserm, U 968Inserm, U 968Inserm, U 968Inserm UMR_S 945, Laboratoire Immunité et InfectionAbstract Atrophic age‐related macular degeneration (AMD) is associated with the subretinal accumulation of mononuclear phagocytes (MPs). Their role in promoting or inhibiting retinal degeneration is unknown. We here show that atrophic AMD is associated with increased intraocular CCL2 levels and subretinal CCR2+ inflammatory monocyte infiltration in patients. Using age‐ and light‐induced subretinal inflammation and photoreceptor degeneration in Cx3cr1 knockout mice, we show that subretinal Cx3cr1 deficient MPs overexpress CCL2 and that both the genetic deletion of CCL2 or CCR2 and the pharmacological inhibition of CCR2 prevent inflammatory monocyte recruitment, MP accumulation and photoreceptor degeneration in vivo. Our study shows that contrary to CCR2 and CCL2, CX3CR1 is constitutively expressed in the retina where it represses the expression of CCL2 and the recruitment of neurotoxic inflammatory CCR2+ monocytes. CCL2/CCR2 inhibition might represent a powerful tool for controlling inflammation and neurodegeneration in AMD.https://doi.org/10.1002/emmm.201302692age‐related macular diseasechemokinesmonocyteneurodegenerationneuroinflammation
spellingShingle Florian Sennlaub
Constance Auvynet
Bertrand Calippe
Sophie Lavalette
Lucie Poupel
Shulong J. Hu
Elisa Dominguez
Serge Camelo
Olivier Levy
Elodie Guyon
Noah Saederup
Israel F. Charo
Nico Van Rooijen
Emeline Nandrot
Jean‐Louis Bourges
Francine Behar‐Cohen
José‐Alain Sahel
Xavier Guillonneau
William Raoul
Christophe Combadiere
CCR2+ monocytes infiltrate atrophic lesions in age‐related macular disease and mediate photoreceptor degeneration in experimental subretinal inflammation in Cx3cr1 deficient mice
EMBO Molecular Medicine
age‐related macular disease
chemokines
monocyte
neurodegeneration
neuroinflammation
title CCR2+ monocytes infiltrate atrophic lesions in age‐related macular disease and mediate photoreceptor degeneration in experimental subretinal inflammation in Cx3cr1 deficient mice
title_full CCR2+ monocytes infiltrate atrophic lesions in age‐related macular disease and mediate photoreceptor degeneration in experimental subretinal inflammation in Cx3cr1 deficient mice
title_fullStr CCR2+ monocytes infiltrate atrophic lesions in age‐related macular disease and mediate photoreceptor degeneration in experimental subretinal inflammation in Cx3cr1 deficient mice
title_full_unstemmed CCR2+ monocytes infiltrate atrophic lesions in age‐related macular disease and mediate photoreceptor degeneration in experimental subretinal inflammation in Cx3cr1 deficient mice
title_short CCR2+ monocytes infiltrate atrophic lesions in age‐related macular disease and mediate photoreceptor degeneration in experimental subretinal inflammation in Cx3cr1 deficient mice
title_sort ccr2 monocytes infiltrate atrophic lesions in age related macular disease and mediate photoreceptor degeneration in experimental subretinal inflammation in cx3cr1 deficient mice
topic age‐related macular disease
chemokines
monocyte
neurodegeneration
neuroinflammation
url https://doi.org/10.1002/emmm.201302692
work_keys_str_mv AT floriansennlaub ccr2monocytesinfiltrateatrophiclesionsinagerelatedmaculardiseaseandmediatephotoreceptordegenerationinexperimentalsubretinalinflammationincx3cr1deficientmice
AT constanceauvynet ccr2monocytesinfiltrateatrophiclesionsinagerelatedmaculardiseaseandmediatephotoreceptordegenerationinexperimentalsubretinalinflammationincx3cr1deficientmice
AT bertrandcalippe ccr2monocytesinfiltrateatrophiclesionsinagerelatedmaculardiseaseandmediatephotoreceptordegenerationinexperimentalsubretinalinflammationincx3cr1deficientmice
AT sophielavalette ccr2monocytesinfiltrateatrophiclesionsinagerelatedmaculardiseaseandmediatephotoreceptordegenerationinexperimentalsubretinalinflammationincx3cr1deficientmice
AT luciepoupel ccr2monocytesinfiltrateatrophiclesionsinagerelatedmaculardiseaseandmediatephotoreceptordegenerationinexperimentalsubretinalinflammationincx3cr1deficientmice
AT shulongjhu ccr2monocytesinfiltrateatrophiclesionsinagerelatedmaculardiseaseandmediatephotoreceptordegenerationinexperimentalsubretinalinflammationincx3cr1deficientmice
AT elisadominguez ccr2monocytesinfiltrateatrophiclesionsinagerelatedmaculardiseaseandmediatephotoreceptordegenerationinexperimentalsubretinalinflammationincx3cr1deficientmice
AT sergecamelo ccr2monocytesinfiltrateatrophiclesionsinagerelatedmaculardiseaseandmediatephotoreceptordegenerationinexperimentalsubretinalinflammationincx3cr1deficientmice
AT olivierlevy ccr2monocytesinfiltrateatrophiclesionsinagerelatedmaculardiseaseandmediatephotoreceptordegenerationinexperimentalsubretinalinflammationincx3cr1deficientmice
AT elodieguyon ccr2monocytesinfiltrateatrophiclesionsinagerelatedmaculardiseaseandmediatephotoreceptordegenerationinexperimentalsubretinalinflammationincx3cr1deficientmice
AT noahsaederup ccr2monocytesinfiltrateatrophiclesionsinagerelatedmaculardiseaseandmediatephotoreceptordegenerationinexperimentalsubretinalinflammationincx3cr1deficientmice
AT israelfcharo ccr2monocytesinfiltrateatrophiclesionsinagerelatedmaculardiseaseandmediatephotoreceptordegenerationinexperimentalsubretinalinflammationincx3cr1deficientmice
AT nicovanrooijen ccr2monocytesinfiltrateatrophiclesionsinagerelatedmaculardiseaseandmediatephotoreceptordegenerationinexperimentalsubretinalinflammationincx3cr1deficientmice
AT emelinenandrot ccr2monocytesinfiltrateatrophiclesionsinagerelatedmaculardiseaseandmediatephotoreceptordegenerationinexperimentalsubretinalinflammationincx3cr1deficientmice
AT jeanlouisbourges ccr2monocytesinfiltrateatrophiclesionsinagerelatedmaculardiseaseandmediatephotoreceptordegenerationinexperimentalsubretinalinflammationincx3cr1deficientmice
AT francinebeharcohen ccr2monocytesinfiltrateatrophiclesionsinagerelatedmaculardiseaseandmediatephotoreceptordegenerationinexperimentalsubretinalinflammationincx3cr1deficientmice
AT josealainsahel ccr2monocytesinfiltrateatrophiclesionsinagerelatedmaculardiseaseandmediatephotoreceptordegenerationinexperimentalsubretinalinflammationincx3cr1deficientmice
AT xavierguillonneau ccr2monocytesinfiltrateatrophiclesionsinagerelatedmaculardiseaseandmediatephotoreceptordegenerationinexperimentalsubretinalinflammationincx3cr1deficientmice
AT williamraoul ccr2monocytesinfiltrateatrophiclesionsinagerelatedmaculardiseaseandmediatephotoreceptordegenerationinexperimentalsubretinalinflammationincx3cr1deficientmice
AT christophecombadiere ccr2monocytesinfiltrateatrophiclesionsinagerelatedmaculardiseaseandmediatephotoreceptordegenerationinexperimentalsubretinalinflammationincx3cr1deficientmice