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Effects of targeting inhibitors of plasmacytoid dendritic cell migration in immune diseases

張 玥 富山大学

2021.09.28

概要

Trafficking of dendritic cells (DCs) in vivo is essential in maintaining immunological homeostasis by orchestrating innate and adaptive immune responses. DCs respond to foreign substances and activate immunocytes such as T cells and B cells via migration to inflamed sites and lymph nodes (LNs). DCs are mainly divided into 2 subtypes: conventional DCs (cDCs) and plasmacytoid DCs (pDCs). pDCs rarely exist in peripheral tissues in the normal state but accumulate in infected sites and rapidly secrete massive amounts of type 1 IFN once viral infection occurs. Chemokine (C-C motif) ligand 19 (CCL19) and chemokine (C-C motif) ligand 21 (CCL21), as ligands of C-C chemokine receptor type 7 (CCR7) expressed on mature pDCs guide pDCs into the LNs.

Migration of pDCs towards LNs is involved in the pathogenesis of many immune diseases via interaction with other immunocytes. Infiltration of pDCs has been found in the skin of systemic sclerosis patients. Depletion of B220+ PDCA-1+ pDCs reduces skin thickness in a skin fibrosis model. In addition, increase of pDCs has been found in inflamed sites in patients with contact dermatitis and atopic dermatitis. Accordingly, pDCs are required for the pathogenic mechanism and defense mechanism of skin disorders, such as atopic dermatitis.

Furthermore, pDCs reportedly play a pivotal role in the onset of inflammatory bowel disease (IBD). A large number of pDCs infiltrate in the colonic mucosa of IBD patients. pDCs are increased in the inflamed colon of ulcerative colitis (UC) patient and Crohn’s disease patients. Also, it is reported that pDCs are decreased in the peripheral blood of UC patients. The population of pDCs is increased in the mouse colon in a dextran sulfate sodium (DSS)-induced colitis model, and the depletion of pDCs suppresses the inflammation in the colon of DSS-induced colitis mice. On the contrary, the depletion of pDCs aggravates severe colitis in a Citrobacter rodentium- induced colitis model by impairing gut barrier functions. Thus, pDCs are considered to play various roles in the pathology of many inflammatory diseases, while the roles of pDCs remain unclear.

To the best of our knowledge, few agents have been found to effectively and potently regulate pDC functions, especially pDC migration. Therefore, we utilized traditional Japanese herbal medicines as a resource for drug discovery. Traditional Japanese herbal medicines have been widely used for various immune diseases, such as rheumatoid arthritis and IBD. Kampo formulas or compounds in natural medicines have been used in the study of inflammatory diseases. Our study focused on the pDC migration in allergic dermatitis model and DSS-induced colitis model. Furthermore, Kampo formulas and compounds in natural medicines were used in the disease models to elucidate the effect and role of inhibition of pDC migration in inflammatory diseases.

1. Therapeutic benefit in allergic dermatitis derived from the inhibitory effect of byakkokaninjinto on the migration of plasmacytoid dendritic cells [1]
pDCs have been reportedly related to inflammatory skin disorders for the increase and accumulation in inflamed sites in patients with contact dermatitis. Even pDCs are increased in the lesional skin of atopic dermatitis patients. Similarly, pDCs also infiltrate in the skin of systemic sclerosis patients and meanwhile, depletion of pDCs reduces skin thickness in a skin fibrosis model.

CCR7-driven migration of pDCs to the lymph nodes is considered play a pivotal role in pathogenesis of immune diseases via activating T cells or B cells. Therefore, our study focused on the inhibition of pDC migration. We screened 86 kinds of Kampo formulas and examined that byakkokaninjinto was the inhibitor of pDC migration by reducing the number of migrated bone marrow-derived pDCs (BMpDCs) and suppressing the velocity and directionality of BMpDC migration in a chemotaxis assay. Furthermore, Gypsum Fibrosum and Ginseng Radix which are the components of byakkokaninjinto, obviously suppressed the velocity of BMpDC migration. Gypsum Fibrosum significantly suppressed the directionality of BMpDC migration. Besides, byakkokaninjinto had no effect on the expression of CCR7 on BMpDCs. Then the effect of byakkokaninjinto on a (1-fluoro-2,4-dinitrobenzene) DNFB-induced allergic contact dermatitis model was investigated. Orally administration of byakkokaninjinto markedly relieved ear swelling in the late-phase allergic reactions.

These findings prove that byakkokaninjinto which has an inhibitory effect on pDC migration may contribute to ameliorate the occurrence of allergic contact dermatitis. Inhibition of pDC migration is anticipated to become a therapeutic agent for pDC-related diseases, such as atopic dermatitis.

2. Suppression of plasmacytoid dendritic cell migration to colonic isolated lymphoid follicles abrogates the development of colitis [2]
It has been reported that pDCs participate in the onset of IBD. Infiltration of pDCs is found in the colonic mucosa of IBD patients. And highly enrichment of pDCs correlates with disease severity of IBD patients. In a DSS-induced colitis model, pDCs are increased in the mouse colon. And depletion of pDCs suppresses inflammation in the colon. However, depletion of pDCs also impairs gut barrier function and causes heavy colitis in a pathogenic bacterium induced colitis model. In another Wiskott-Aldrich syndrome (WAS) disease model, ablating type-I IFN signaling in WAS protein null mice rescues colitis and makes pDCs show tolerance to further stimulation. On the other hand, pDC has been reported that it does not have a major role in the pathology of colitis caused by deficiency in WAS protein. Therefore, these contradictory reports suggest that pDCs perform multiple functions in the intestine.

Our study targets the inhibition of pDC migration. 80 compounds in natural medicines were searched for inhibitors of pDC migration using BMpDCs. Astragaloside IV (As-IV) and oxymatrine (Oxy) suppressed the migration of BMpDC by reducing the number of migrated BMpDCs and suppressing the velocity and directionality of BMpDC migration in a chemotaxis assay. Meanwhile, As-IV and Oxy had no effect on bone marrow-derived conventional DCs. To elucidate the pathogenesis role of pDCs in the intestinal immunity, DSS-induced colitis model was established. The number of pDCs was markedly increased in the colonic lamina propria (LP) of DSS-induced colitis model. Intraperitoneal injection of As-IV or Oxy reduced symptoms of colitis but not affect the number of pDCs in the colonic LP. By the immunohistochemical staining, expression of CCL21 was obviously observed in colonic isolated lymphoid follicles (ILFs). As- IV or Oxy reduced the accumulation of pDCs in colonic ILFs. Furthermore, migration of BMpDCs to colonic ILFs was significantly decreased by treatment with As-IV or Oxy in a BMpDC adoptive transfer model.

These findings prove that accumulation of pDCs in the ILFs is relative to the onset and progression of colitis. As-IV and Oxy exert preventive effects on colitis by suppressing pDC migration to colonic ILFs. The inhibitor of pDC migration may become a potential therapeutic approach for treating colonic inflammatory diseases.

Conclusion
CCR7-driven migration of pDCs to the lymph nodes leads to activation of T cells or B cells. In this study, we discovered inhibitors of pDC migration toward the lymphoid tissues. Our present results have demonstrated that the migration of pDCs toward the lymphoid tissues is involved in the pathogenesis of immune diseases such as contact dermatitis and colonic inflammation. Inhibition of pDC migration contributes to alleviate these diseases. Therefore, the inhibitors of pDC migration may have potentials to become useful lead drugs for immunological diseases.

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