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PMID: 25385367 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov't

Developmental endothelial locus-1 is a homeostatic factor in the central nervous system limiting neuroinflammation and demyelination.

Molecular psychiatry ·Vol. 20 ·No. 7 ·2015-07-00 ·Pages 880-888

Choi EY, Lim JH, Neuwirth A, Economopoulou M, Chatzigeorgiou A, Chung KJ, Bittner S, Lee SH, Langer H, Samus M, Kim H, Cho GS, Ziemssen T, Bdeir K, Chavakis E, Koh JY, Boon L, Hosur K, Bornstein SR, Meuth SG, Hajishengallis G, Chavakis T

Abstract

Inflammation in the central nervous system (CNS) and disruption of its immune privilege are major contributors to the pathogenesis of multiple sclerosis (MS) and of its rodent counterpart, experimental autoimmune encephalomyelitis (EAE). We have previously identified developmental endothelial locus-1 (Del-1) as an endogenous anti-inflammatory factor, which inhibits integrin-dependent leukocyte adhesion. Here we show that Del-1 contributes to the immune privilege status of the CNS. Intriguingly, Del-1 expression decreased in chronic-active MS lesions and in the inflamed CNS in the course of EAE. Del-1-deficiency was associated with increased EAE severity, accompanied by increased demyelination and axonal loss. As compared with control mice, Del-1(-/-) mice displayed enhanced disruption of the blood-brain barrier and increased infiltration of neutrophil granulocytes in the spinal cord in the course of EAE, accompanied by elevated levels of inflammatory cytokines, including interleukin-17 (IL-17). The augmented levels of IL-17 in Del-1-deficiency derived predominantly from infiltrated CD8(+) T cells. Increased EAE severity and neutrophil infiltration because of Del-1-deficiency was reversed in mice lacking both Del-1 and IL-17 receptor, indicating a crucial role for the IL-17/neutrophil inflammatory axis in EAE pathogenesis in Del-1(-/-) mice. Strikingly, systemic administration of Del-1-Fc ameliorated clinical relapse in relapsing-remitting EAE. Therefore, Del-1 is an endogenous homeostatic factor in the CNS protecting from neuroinflammation and demyelination. Our findings provide mechanistic underpinnings for the previous implication of Del-1 as a candidate MS susceptibility gene and suggest that Del-1-centered therapeutic approaches may be beneficial in neuroinflammatory and demyelinating disorders.

MeSH Terms
Animals Axons/drug effects,metabolism,pathology Blood-Brain Barrier/drug effects,metabolism,pathology Calcium-Binding Proteins Capillary Permeability/drug effects,physiology Carrier Proteins/genetics,metabolism Cell Adhesion Molecules Encephalomyelitis, Autoimmune, Experimental/drug therapy,metabolism,pathology Female Granulocytes/drug effects,metabolism,pathology Homeostasis/drug effects,physiology Intercellular Signaling Peptides and Proteins Interleukin-17/metabolism Mice, Inbred C57BL Mice, Knockout Myelin Sheath/drug effects,metabolism,pathology Neuroimmunomodulation/drug effects,physiology Neutrophils/drug effects,metabolism,pathology Receptors, Interleukin-17/genetics,metabolism Severity of Illness Index Spinal Cord/drug effects,metabolism,pathology
Chemicals
Calcium-Binding Proteins Carrier Proteins Cell Adhesion Molecules Edil3 protein, mouse Il17ra protein, mouse Intercellular Signaling Peptides and Proteins Interleukin-17 Receptors, Interleukin-17
Authors & Affiliations
22 authors, click to expand affiliations / ORCID
Choi Eun Young
Department of Biomedical Sciences and Department of Pharmacology, Cell Dysfunction Research Center (CDRC), University of Ulsan College of Medicine, Seoul, Republic of Korea. | Experimental Immunology Branch, National Cancer Institute (NCI), National Institutes of Health (NIH), Bethesda, Maryland, USA. | Department of Clinical Pathobiochemistry, Faculty of Medicine, Technische Universität Dresden, Germany. | Department of Internal Medicine III, Faculty of Medicine, Technische Universität Dresden, Dresden, Germany.
Lim Jong-Hyung
Department of Clinical Pathobiochemistry, Faculty of Medicine, Technische Universität Dresden, Germany.
Neuwirth Ales
Department of Clinical Pathobiochemistry, Faculty of Medicine, Technische Universität Dresden, Germany.
Economopoulou Matina
Clinic for Ophthalmology, Faculty of Medicine, Technische Universität Dresden, Dresden, Germany.
Chatzigeorgiou Antonios
Department of Clinical Pathobiochemistry, Faculty of Medicine, Technische Universität Dresden, Germany. | Department of Internal Medicine III, Faculty of Medicine, Technische Universität Dresden, Dresden, Germany.
Chung Kyoung-Jin
Department of Clinical Pathobiochemistry, Faculty of Medicine, Technische Universität Dresden, Germany.
Bittner Stefan
Department for Neurology, University Münster, Germany.
Lee Seung-Hwan
Department of Biomedical Sciences and Department of Pharmacology, Cell Dysfunction Research Center (CDRC), University of Ulsan College of Medicine, Seoul, Republic of Korea.
Langer Harald
Experimental Immunology Branch, National Cancer Institute (NCI), National Institutes of Health (NIH), Bethesda, Maryland, USA. | Medizinische Klinik III, Eberhard Karls-University Tübingen, Tübingen, Germany.
Samus Maryna
Department of Internal Medicine III, Faculty of Medicine, Technische Universität Dresden, Dresden, Germany.
Kim Hyesoon
Department of Biomedical Sciences and Department of Pharmacology, Cell Dysfunction Research Center (CDRC), University of Ulsan College of Medicine, Seoul, Republic of Korea.
Cho Geum-Sil
Department of Biomedical Sciences and Department of Pharmacology, Cell Dysfunction Research Center (CDRC), University of Ulsan College of Medicine, Seoul, Republic of Korea.
Ziemssen Tjalf
Department of Neurology, Faculty of Medicine, Technische Universität Dresden, Dresden, Germany.
Bdeir Khalil
Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA.
Chavakis Emmanouil
Department of Internal Medicine, Cardiology, Goethe University Frankfurt, Frankfurt, Germany.
Koh Jae-Young
Department of Neurology, University of Ulsan College of Medicine, Seoul, Republic of Korea.
Boon Louis
Bioceros, Utrecht, The Netherlands.
Hosur Kavita
Department of Microbiology, School of Dental Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
Bornstein Stefan R
Department of Internal Medicine III, Faculty of Medicine, Technische Universität Dresden, Dresden, Germany.
Meuth Sven G
Department for Neurology, University Münster, Germany.
Hajishengallis George
Department of Microbiology, School of Dental Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
Chavakis Triantafyllos
Experimental Immunology Branch, National Cancer Institute (NCI), National Institutes of Health (NIH), Bethesda, Maryland, USA. | Department of Clinical Pathobiochemistry, Faculty of Medicine, Technische Universität Dresden, Germany. | Department of Internal Medicine III, Faculty of Medicine, Technische Universität Dresden, Dresden, Germany. | Institute for Clinical Chemistry and Laboratory Medicine, Faculty of Medicine, Technische Universität Dresden, Dresden, Germany. | Center for Regenerative Therapies Dresden, Dresden, Germany.
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Article Info
Journal
Molecular psychiatry
Abbr.
Mol Psychiatry
ISSN
1476-5578
Published
2015-07-00
Epub
2014-00-11
Pages
880-888
Language
English
Region
England
NLM ID
9607835
PMCID
PMC4351922
Subset
IM
Grants
NIDCR NIH HHS · R01 DE015254 · United States
NIDCR NIH HHS · DE021685 · United States
NIDCR NIH HHS · DE017138 · United States
Intramural NIH HHS · United States
NIAID NIH HHS · R21 AI102177 · United States
European Research Council · 281296 · International
NIDCR NIH HHS · R01 DE021685 · United States
NIDCR NIH HHS · R01 DE017138 · United States
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