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Autoimmune CD4⁺ T Cell Memory: Lifelong Persistence of Encephalitogenic T Cell Clones in Healthy Immune Repertoires ¹

Naoto Kawakami^*, Francesca Odoardi^*, Tjalf Ziemssen^*, Monika Bradl, Thomas Ritter, Oliver Neuhaus^*, Hans Lassmann, Hartmut Wekerle^* and Alexander Flügel^2,*

^* Department of Neuroimmunology, Max-Planck-Institute for Neurobiology, Martinsried, Germany; Neurological Institute, University of Vienna, Vienna, Austria; and Institute of Medical Immunology, Charité, Humboldt-University, Berlin, Germany

We embedded green fluorescent CD4⁺ T cells specific for myelin basic protein (MBP) (T_MBP-GFP cells) in the immune system of syngeneic neonatal rats. These cells persisted in the animals for the entire observation period spanning >2 years without affecting the health of the hosts. They maintained a memory phenotype with low levels of L-selectin and CD45RC, but high CD44. Although persisting in low numbers (0.01–0.1% of lymph node cells) they were sufficient to raise susceptibility toward clinical autoimmune disease. Immunization with MBP in IFA induced CNS inflammation and overt clinical disease in animals carrying neonatally transferred T_MBP-GFP cells, but not in controls. The onset of the clinical disease coincided with mass infiltration of T_MBP-GFP cells into the CNS. In the periphery, following the amplification phase a rapid contraction of the T cell population was observed. However, elevated numbers of fully reactive T_MBP-GFP cells remained in the peripheral immune system after acute experimental autoimmune encephalomyelitis mediating reimmunization-induced disease relapses.

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