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Cholecystokinin Downregulates Psoriatic Inflammation by Its Possible Self-Regulatory Effect on Epidermal Keratinocytes

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Cholecystokinin Downregulates Psoriatic Inflammation by Its Possible Self-Regulatory Effect on Epidermal Keratinocytes Cholecystokinin Downregulates Psoriatic Inflammation by Its Possible Self-Regulatory Effect on Epidermal Keratinocytes This information is current as Atsuko Funakoshi, Kazuki Tatsuno, Takatoshi Shimauchi, of September 23, 2021. Toshiharu Fujiyama, Taisuke Ito and Yoshiki Tokura J Immunol published online 22 March 2019 http://www.jimmunol.org/content/early/2019/03/21/jimmun ol.1801426 Downloaded from Supplementary http://www.jimmunol.org/content/suppl/2019/03/21/jimmunol.180142 Material 6.DCSupplemental http://www.jimmunol.org/ Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication by guest on September 23, 2021 *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2019 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Published March 22, 2019, doi:10.4049/jimmunol.1801426 The Journal of Immunology Cholecystokinin Downregulates Psoriatic Inflammation by Its Possible Self-Regulatory Effect on Epidermal Keratinocytes Atsuko Funakoshi, Kazuki Tatsuno, Takatoshi Shimauchi, Toshiharu Fujiyama, Taisuke Ito, and Yoshiki Tokura Cholecystokinin (CCK) is a peptide hormone that functions in digestive organs and the CNS. We previously showed that CCK downregulates peripheral pruritus by suppressing degranulation of mast cells. In this study, we demonstrated that CCK octapeptide (CCK8) was constitutively expressed in the epidermis of normal skin, whereas its expression was lost in acanthotic lesions of pso- riasis. In contrast, CCKA receptor (CCKAR), a high-affinity receptor for CCK, was constitutively expressed in the epidermis of psoriatic skin lesions. Expression of CCK was also reduced in skin lesions of an imiquimod (IMQ)-induced psoriatic mouse model. Notably, the expression level of CCK inversely correlated with the severity of epidermal inflammation, raising the possibility that CCK from epidermal keratinocytes suppresses the psoriatic inflammation. To verify this hypothesis, we investigated the effects of Downloaded from sulfated CCK octapeptide (CCK8S) on the development of IMQ-induced psoriatic inflammation. i.p. injection of CCK8S suppressed the IMQ-induced psoriatic inflammation accompanied by reduced mRNA expression of IL-17, IL-22, and IL-6 but not of IL-23. The suppressive effect of CCK8S was completely restored by administration of CCKAR antagonist. In vitro studies showed that ex- ogenous CCK8S suppressed IL-6 production in CCKAR-expressing cultured human keratinocytes, and blocking the endogenous CCK signaling with CCKAR antagonist markedly enhanced IL-6 production. When keratinocytes were stimulated with IL-17, the expression of endogenous CCK was significantly decreased. These findings suggest that CCK physiologically functions as a negative http://www.jimmunol.org/ regulator of keratinocyte-based inflammation in an autocrine or paracrine manner, although decreased CCK may pathologically contribute to continuous and aggravated skin lesions such as psoriasis. The Journal of Immunology, 2019, 202: 000–000. soriasis is a chronic inflammatory skin disease mediated (7, 8). Inflammatory DCs play an indispensable role in the path- by immunocompetent cells and nonhematopoietic cells ogenesis of psoriasis with their released IL-23, thereby main- P like keratinocytes. Th17 cells play a central role in the taining Th17 cells, whereas plasmacytoid DCs are stimulated pathogenesis of psoriasis, and Th17 cell–derived IL-17A and via TLRs and trigger psoriasis lesions by releasing IFN-a (1, 9). A IL-22 induce proliferation and activation of epidermal keratino- mouse model of psoriasis-like epidermal inflammation induced by by guest on September 23, 2021 cytes, leading to epidermal hyperplasia (acanthosis) and para- imiquimod (IMQ) has been widely used to investigate the path- keratosis (1, 2). In mice, gd T cells replace Th17 cells as IL-17A ogenesis of psoriasis. Topical application of IMQ, a synthetic producers (3, 4). Activated keratinocytes produce various cyto- ligand for TLR7, onto mouse skin activates plasmacytoid DCs and kines and chemokines, such as IL-1, IL-6, IL-8, CXCL10, CCL20, induces epidermal inflammation with histological changes con- and vascular endothelial growth factor, which promote cytokine siderably similar to human psoriasis (10–13). production and skin recruitment of T cells, neutrophils, and Cholecystokinin (CCK) is largely expressed in the CNS and dendritic cells (DCs) (5). Compelling evidence has been accu- small intestine, where it serves as a peptide hormone with specific mulated that IL-6 is associated with pathogenesis of psoriasis functions (14). CCK undergoes tissue-specific posttranscriptional (6–8). IL-6 promotes Th17 cell function by downregulating de- processing: brain makes mainly CCK8, whereas CCK12, 22, 33, velopment of regulatory T cells and induces proliferation of and 58 are found more often in the gastrointestinal tract. Another keratinocytes, resulting in continuous psoriatic inflammation important posttranscriptional modification is sulfation of the ty- rosine residue (14, 15). Recent studies have highlighted that CCK plays an immunomodulatory role by affecting immunocompe- Department of Dermatology, Hamamatsu University School of Medicine, Hama- matsu 431-3192, Japan tent cells such as T cells, B cells, macrophages, and DCs (16–19). ORCIDs: 0000-0002-0369-869X (T.S.); 0000-0002-9274-7050 (T.I.). In vitro studies have shown that sulfated CCK octapeptide Received for publication October 23, 2018. Accepted for publication February 27, (CCK8S), biologically active CCK, inhibits IgG1 production in 2019. LPS-stimulated B cells and differentiation of Th1 and Th17 cells, This work was supported by Grants-in-Aid for Scientific Research (18K16025 and whereas it enhances differentiation of regulatory T cells (16, 17). 25293243) from the Ministry of Education, Culture, Sports, Science and Technology It is noteworthy that CCK suppresses development of collagen- and a grant from Otsuka Pharmaceutical. induced arthritis by inhibiting differentiation of Th17 cells (18, Address correspondence and reprint requests to Dr. Atsuko Funakoshi, Department of 20). These findings indicate that CCK plays downregulatory roles in Dermatology, Hamamatsu University School of Medicine, 1-20-1 Handayama, Higashi-ku, Hamamatsu 431-3192, Japan. E-mail address: [email protected] immune-mediated inflammatory responses. To assess the function The online version of this article contains supplemental material. of CCK in the skin, we investigated the effect of CCK on peripheral Abbreviations used in this article: AEC, 3-amino-9-ethylcarbazole; CCK, cholecys- pruritus in mice (21). We found that CCK8S exerts an antipruritic tokinin; CCKAR, CCKA receptor; CCKBR, CCKB receptor; CCK8S, sulfated CCK activity by suppressing degranulation of mast cells. However, a role octapeptide; DC, dendritic cell; IMQ, imiquimod; NHEK, normal human epidermal of CCK in T cell–mediated skin diseases has not been elucidated. keratinocyte. Two types of CCK receptors, CCKA receptor (CCKAR) and Copyright Ó 2019 by The American Association of Immunologists, Inc. 0022-1767/19/$37.50 CCKB receptor (CCKBR), have been characterized (15). CCKAR www.jimmunol.org/cgi/doi/10.4049/jimmunol.1801426 2 DOWNREGULATORY ROLE OF CHOLECYSTOKININ IN PSORIASIS serves as a high-affinity receptor for CCK8S, whereas nonsulfated into mice according to the experimental protocol described in Figs. 5A CCK8 binds to CCKAR with much lower affinity. CCK33, 39, and and 8A. Ear thickness was sequentially measured using a micrometer 58 bind to CCKAR with similar affinity to CCK8 (15). Gastrin is (Mitutoyo, Kanagawa, Japan). The net increase in ear thickness was calculated by subtracting the ear thickness measured before IMQ treatment. Ears considered to be a major physiological ligand of CCKBR and were collected at the indicated time points and stored in RNAlater Stabi- is mainly expressed in the gastrointestinal tract. The expression lization Solution (Thermo Fisher Scientific, Waltham, MA) until RNA and functional role of CCK receptors in immunocompetent cells purification for real-time PCR analysis. Experiments were performed with have been investigated. CD4+ T cells express both CCKAR and at least five mice per group. CCKBR, whereas CCK8S suppresses IgG1 production of B cells Immunohistochemistry through CCKBR (16, 17). We found that fetal skin-derived mast Human skin and mouse ear samples were fixed in 10% buffered formalin cells expressed both CCKAR and CCKBR (21). Because the ex- and embedded in paraffin. Sections were deparaffinized and stained with pression of CCKBR on mast cells is upregulated by substance P, it H&E. For immunostaining of CCK and CCKAR, deparaffinized sections is more likely that CCK8S suppresses degranulation of mast cells were stained with anti-CCK8 Ab (ab27441; Abcam) (22, 23) overnight at via CCKBR, resulting in reduction of peripheral pruritus. 4˚C or with anti-CCKAR Ab (Bioss, Woburn, MA)
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