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The Journal of Immunology, 2001, 166: 7136-7143.
Copyright © 2001 by The American Association of Immunologists

Mammalian and Viral IL-10 Enhance C-C Chemokine Receptor 5 but Down-Regulate C-C Chemokine Receptor 7 Expression by Myeloid Dendritic Cells: Impact on Chemotactic Responses and In Vivo Homing Ability1

Takuya Takayama*, Adrian E. Morelli*, Nobuyuki Onai{ddagger}, Motohiro Hirao§, Kouji Matsushima{ddagger}, Hideaki Tahara*,§ and Angus W. Thomson2,*,{dagger}

* Thomas E. Starzl Transplantation Institute and Departments of Surgery and {dagger} Molecular Genetics and Biochemistry, University of Pittsburgh, Pittsburgh, PA 15213; and {ddagger} Department of Molecular Preventive Medicine, School of Medicine, and § Department of Surgery and Bioengineering, Institute of Medical Science, University of Tokyo, Tokyo, Japan

The immunosuppressive and anti-inflammatory cytokine IL-10 inhibits the phenotypic and functional maturation of dendritic cells (DC) and has been reported to confer tolerogenic properties on these important professional APC. Here, we exposed murine bone marrow-derived myeloid DC to either mouse (m) or viral (v) IL-10 early during their in vitro generation in response to GM-CSF and IL-4. Both mIL-10 and vIL-10 down-regulated the expression of CCR7 mRNA determined by RT-PCR, while mIL-10 up-regulated the expression of CCR5 transcripts. These changes in CCR7 and CCR5 expression were associated with inhibition and augmentation, respectively, of DC chemotaxis toward their respective agonists, macrophage inflammatory proteins 3{beta} and 1{alpha}, while in vivo homing of DC from peripheral s.c. sites to secondary lymphoid tissue of syngeneic or allogeneic recipients was significantly impaired. Anti-mIL-10R mAb reversed the effects of mIL-10 on CCR expression and restored DC homing ability. Retroviral transduction of mIL-10- and vIL-10-treated DC to overexpress transgenic CCR7 partially restored the cells’ lymphoid tissue homing ability in allogeneic recipients. However, CCR7 gene transfer did not reinstate the capacity of IL-10-treated DC to prime host naive T cells for ex vivo proliferative responses or Th1 cytokine (IFN-{gamma}) production in response to rechallenge with (donor) alloantigen. These findings suggest that in addition to their capacity to subvert DC maturation/function and confer tolerogenic potential on these cells, mIL-10 and vIL-10 regulate DC migratory responses via modulation of CCR expression.




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