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The Journal of Immunology, 2006, 176: 7207-7220.
Copyright © 2006 by The American Association of Immunologists

Transgenic Galectin-1 Induces Maturation of Dendritic Cells That Elicit Contrasting Responses in Naive and Activated T Cells1

Marcelo J. Perone*, Adriana T. Larregina{dagger},{ddagger}, William J. Shufesky*, Glenn D. Papworth§, Mara L. G. Sullivan§, Alan F. Zahorchak*, Donna Beer Stolz§, Linda G. Baum, Simon C. Watkins{ddagger},§, Angus W. Thomson*,{ddagger} and Adrian E. Morelli2,*

* Thomas E. Starzl Transplantation Institute and Department of Surgery, {dagger} Department of Dermatology, {ddagger} Department of Immunology, and § Center for Biological Imaging, University of Pittsburgh Medical Center, Pittsburgh, PA 15213; and Department of Pathology and Jonsson Comprehensive Cancer Center, University of California Los Angeles School of Medicine, Los Angeles, CA 90095

Dendritic cells (DC) are professional APC that control the balance between T cell immunity and tolerance. Genetic engineering of DC to regulate the outcome of the immune response is an area of intense research. Galectin (gal)-1 is an endogenous lectin that binds to glycoproteins and exerts potent regulatory effects on T cells. Consequently, gal-1 participates in central deletion of thymocytes and exerts therapeutic effects on experimental models of T cell-mediated autoimmune disorders and graft-vs-host disease. Together, these observations strongly indicate that engineering DC to express transgenic (tg) gal-1 may be beneficial to treat T cell-mediated disorders. In this study, we have investigated the impact of the expression of high levels of tg gal-1 on maturation/activation of DC and on their T cell stimulatory function. Murine DC were transduced with a recombinant adenovirus encoding hu gal-1 (gal-1-DC). Tg gal-1 was exported by a nonclassical pathway through exosomes and was retained on the DC surface inducing segregation of its ligand CD43. Expression of tg gal-1 triggered activation of DC determined by induction of a more mature phenotype, increased levels of mRNA for proinflammatory cytokines, and enhanced ability to stimulate naive T cells. Conversely, gal-1-DC induced rapid apoptosis of activated T cells. In vivo, gal-1-DC increased significantly the sensitization phase of contact hypersensitivity assays while inducing a drastic inhibition of the elicitation phase by triggering apoptosis of activated T cells in the dermis. Gal-1-DC represent a novel tool to control differentially the afferent and efferent arms of the T cell response.




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