Cited by 245Cell Adhesion Molecules ResearchMultiple Sclerosis Research StudiesNeuroinflammation and Neurodegeneration Mechanisms

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Molecular Mechanisms Involved in Lymphocyte Recruitment in Inflamed Brain Microvessels: Critical Roles for P-Selectin Glycoprotein Ligand-1 and Heterotrimeric Gi-Linked Receptors

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Piccio, Laura, Rossi, Barbara, Scarpini, Elio, Laudanna, Carlo, Giagulli, Cinzia, Issekutz, Andrew C, Vestweber, Dietmar, Butcher, Eugene C, Constantin, Gabriela·2002·The Journal of Immunology

DOI 10.4049/jimmunol.168.4.1940

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Abstract

Lymphocyte recruitment into the brain is a critical event in the pathogenesis of multiple sclerosis and experimental autoimmune encephalomyelitis. We developed a novel intravital microscopy model to directly analyze through the skull the interactions between lymphocytes and the endothelium in cerebral venules of mice. No adhesive interactions were observed between lymphocytes and the nonactivated endothelium in the cerebral microcirculation. When brain venules were activated by pretreating mice with TNF-α or LPS, proteolipid protein 139–151 autoreactive T lymphocytes rolled and arrested; notably, only a few peripheral lymph node cells rolled and firmly adhered. Abs anti-P-selectin glycoprotein ligand-1 and anti-E- and P-selectin blocked tethering and rolling of autoreactive lymphocytes, suggesting that P-selectin glycoprotein ligand-1/endothelial selectins are critical in the recruitment of lymphocytes in inflamed brain venules. E- and P-selectin were expressed on cerebral vessels upon in vivo activation and had a patchy distribution during the preclinical phase of active and passive experimental autoimmune encephalomyelitis. LFA-1/ICAM-1 and α4 integrins/VCAM-1 supported rolling, but were not relevant to rolling velocity. Firm arrest was mainly mediated by LFA-1 and ICAM-1. Pretreatment of autoreactive lymphocytes with pertussis toxin blocked integrin-dependent arrest, implicating a requirement for Gi protein-dependent signaling in vessels from nonlymphoid districts. In conclusion, our data unveils the molecular mechanisms controlling the recruitment of autoreactive lymphocytes in inflamed cerebral vessels and suggest new insights into the pathogenesis of autoimmune inflammatory diseases of the CNS.

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Authors: Piccio, L., Rossi, B., Scarpini, E., Laudanna, C., Giagulli, C., Issekutz, A. C., Vestweber, D., Butcher, E. C., & Constantin, G.
Affiliations: University of Verona (IT)
Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico (IT)
Dalhousie University (CA)
University of Münster (DE)
Stanford University (US)
ORCID: Piccio, Laura
Rossi, Barbara
Scarpini, Elio
Laudanna, Carlo
Giagulli, Cinzia
Vestweber, Dietmar
Butcher, Eugene C
Constantin, Gabriela
Venue: The Journal of Immunology
Publisher: Oxford University Press (OUP)
Published: 2002-02
Volume: 168
Issue: 4
Pages: 1940-1949
ISSN: 0022-1767 (ISSN-L)
1550-6606
DOI: 10.4049/jimmunol.168.4.1940
OpenAlex: W1960336193
Cited by: 245
References: 56
Citations by year: 2026: 4 · 2025: 2 · 2024: 5 · 2023: 7 · 2022: 9 · 2021: 4 · 2020: 4 · 2019: 5 · 2018: 2 · 2017: 7 · 2016: 7 · 2015: 12 · 2014: 11 · 2013: 8 · 2012: 16
FWCI: 9.00
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: The Journal of Immunology (publishedVersion)
PubMed (publishedVersion)
Max Planck Institute for Plasma Physics (submittedVersion)
INFM-OAR (INFN Catania) (submittedVersion, other-oa)
Funders: Fondazione Italiana Sclerosi Multipla
Deutsche Forschungsgemeinschaft
Consiglio Nazionale delle Ricerche
Topics: Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords: lymphocyte recruitment, PSGL-1, E-selectin, P-selectin, endothelial activation, multiple sclerosis, experimental autoimmune encephalomyelitis, autoreactive T cells, heterotrimeric G protein signaling, pertussis toxin, intravital microscopy, TNF-α, LPS, lymphocyte-endothelial interactions
MeSH terms: Animals, Autoantigens, Brain, Cell Movement, Cerebrovascular Circulation, Encephalomyelitis, Autoimmune, Experimental, Endothelium, Vascular, Female, Hemodynamics, Membrane Glycoproteins, Microcirculation, Microscopy, Fluorescence, Receptors, Cell Surface, T-Lymphocytes, Venules, Cell Adhesion Molecules, Integrins, Models, Immunological, Selectins, GTP-Binding Protein alpha Subunits, Gi-Go, Mice

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Molecular Mechanisms Involved in Lymphocyte Recruitment in Inflamed Brain Microvessels: Critical Roles for P-Selectin Glycoprotein Ligand-1 and Heterotrimeric Gi-Linked Receptors

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