Intraperitoneal injection but not oral administration of ellagic acid: a novel immunomodulator via targeting casein kinase 2 signaling pathway

Immunosuppressants currently approved for the treatment of autoimmune diseases and organ transplant rejection present diverse adverse effects that impair the life quality of patients. Therefore, the development of novel immunomodulators with high efficiency and low toxicity is essential. Ellagic aci...

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Main Authors: Wenhui Qi, Bing Han, Tingting Cui, Peixin Shen, Zhuohua Zhao, Yaping Yan, Libin Wang, Xinyu Lu, Yuan Zhang, Xing Li
Format: Article
Language:English
Published: Tsinghua University Press 2025-07-01
Series:Food Science and Human Wellness
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Online Access:https://www.sciopen.com/article/10.26599/FSHW.2024.9250157
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author Wenhui Qi
Bing Han
Tingting Cui
Peixin Shen
Zhuohua Zhao
Yaping Yan
Libin Wang
Xinyu Lu
Yuan Zhang
Xing Li
author_facet Wenhui Qi
Bing Han
Tingting Cui
Peixin Shen
Zhuohua Zhao
Yaping Yan
Libin Wang
Xinyu Lu
Yuan Zhang
Xing Li
author_sort Wenhui Qi
collection DOAJ
description Immunosuppressants currently approved for the treatment of autoimmune diseases and organ transplant rejection present diverse adverse effects that impair the life quality of patients. Therefore, the development of novel immunomodulators with high efficiency and low toxicity is essential. Ellagic acid (EA), a natural polyphenol compound widely distributed in berries, is metabolically transformed by gut microbiome to exert systemic health benefits. Here, we identified that intraperitoneal administration of EA with no cytotoxicity, beyond its well-known oral metabolic fate, effectively decreased clinical severity and central nervous system (CNS) inflammation/demyelination in experimental autoimmune encephalomyelitis, a mouse model of an autoimmune disease multiple sclerosis. Interestingly, intraperitoneal EA administration at incredibly low doses (0.1 mg/(kg·day)) is dose-sparing with fingolimod (FTY720), the first FDA-approved oral drug for MS. In addition, intraperitoneal EA also ameliorated the brain damage in a neuromyelitis optica (NMO) model, and significantly prevented the immune rejection of allograft skin graft. Evidence from pharmacological studies combined with RNA-seq indicate that prototype EA functions by a mechanism that involves direct inhibition of casein kinase Ⅱ (CKⅡ) to suppress the expression of IL-17 and promote the expression of Cpt1a to regulate T helper cell 17 differentiation. In conclusion, our study demonstrates that the prototype EA entering the blood circulation acts as a novel therapeutic immunomodulator for the treatment of autoimmune diseases and transplant rejection through the CKⅡ-mediated Janus kinase/signal transducer and activator of transcription 3 Cpt1a signaling pathway.
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publishDate 2025-07-01
publisher Tsinghua University Press
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series Food Science and Human Wellness
spelling doaj-art-dbf9e01669c94b839115816b828f7ac22025-08-20T03:41:14ZengTsinghua University PressFood Science and Human Wellness2097-07652213-45302025-07-01147925015710.26599/FSHW.2024.9250157Intraperitoneal injection but not oral administration of ellagic acid: a novel immunomodulator via targeting casein kinase 2 signaling pathwayWenhui Qi0Bing Han1Tingting Cui2Peixin Shen3Zhuohua Zhao4Yaping Yan5Libin Wang6Xinyu Lu7Yuan Zhang8Xing Li9Key Laboratory of Medicinal Resources and Natural Pharmaceutical Chemistry (Shaanxi Normal University), Ministry of Education, College of Life Sciences, Shaanxi Normal University, Xi’an 710119, ChinaKey Laboratory of Medicinal Resources and Natural Pharmaceutical Chemistry (Shaanxi Normal University), Ministry of Education, College of Life Sciences, Shaanxi Normal University, Xi’an 710119, ChinaKey Laboratory of Medicinal Resources and Natural Pharmaceutical Chemistry (Shaanxi Normal University), Ministry of Education, College of Life Sciences, Shaanxi Normal University, Xi’an 710119, ChinaKey Laboratory of Medicinal Resources and Natural Pharmaceutical Chemistry (Shaanxi Normal University), Ministry of Education, College of Life Sciences, Shaanxi Normal University, Xi’an 710119, ChinaKey Laboratory of Medicinal Resources and Natural Pharmaceutical Chemistry (Shaanxi Normal University), Ministry of Education, College of Life Sciences, Shaanxi Normal University, Xi’an 710119, ChinaKey Laboratory of Medicinal Resources and Natural Pharmaceutical Chemistry (Shaanxi Normal University), Ministry of Education, College of Life Sciences, Shaanxi Normal University, Xi’an 710119, ChinaThe Nervous System Disease Diagnosis and Treatment Engineering Technology Research Center of Ningxia, Yinchuan 750001, ChinaKey Laboratory of Medicinal Resources and Natural Pharmaceutical Chemistry (Shaanxi Normal University), Ministry of Education, College of Life Sciences, Shaanxi Normal University, Xi’an 710119, ChinaKey Laboratory of Medicinal Resources and Natural Pharmaceutical Chemistry (Shaanxi Normal University), Ministry of Education, College of Life Sciences, Shaanxi Normal University, Xi’an 710119, ChinaKey Laboratory of Medicinal Resources and Natural Pharmaceutical Chemistry (Shaanxi Normal University), Ministry of Education, College of Life Sciences, Shaanxi Normal University, Xi’an 710119, ChinaImmunosuppressants currently approved for the treatment of autoimmune diseases and organ transplant rejection present diverse adverse effects that impair the life quality of patients. Therefore, the development of novel immunomodulators with high efficiency and low toxicity is essential. Ellagic acid (EA), a natural polyphenol compound widely distributed in berries, is metabolically transformed by gut microbiome to exert systemic health benefits. Here, we identified that intraperitoneal administration of EA with no cytotoxicity, beyond its well-known oral metabolic fate, effectively decreased clinical severity and central nervous system (CNS) inflammation/demyelination in experimental autoimmune encephalomyelitis, a mouse model of an autoimmune disease multiple sclerosis. Interestingly, intraperitoneal EA administration at incredibly low doses (0.1 mg/(kg·day)) is dose-sparing with fingolimod (FTY720), the first FDA-approved oral drug for MS. In addition, intraperitoneal EA also ameliorated the brain damage in a neuromyelitis optica (NMO) model, and significantly prevented the immune rejection of allograft skin graft. Evidence from pharmacological studies combined with RNA-seq indicate that prototype EA functions by a mechanism that involves direct inhibition of casein kinase Ⅱ (CKⅡ) to suppress the expression of IL-17 and promote the expression of Cpt1a to regulate T helper cell 17 differentiation. In conclusion, our study demonstrates that the prototype EA entering the blood circulation acts as a novel therapeutic immunomodulator for the treatment of autoimmune diseases and transplant rejection through the CKⅡ-mediated Janus kinase/signal transducer and activator of transcription 3 Cpt1a signaling pathway.https://www.sciopen.com/article/10.26599/FSHW.2024.9250157ellagic acidexperimental autoimmune encephalomyelitisneuromyelitis opticaorgan transplantationcasein kinase ⅱt helper cell 17
spellingShingle Wenhui Qi
Bing Han
Tingting Cui
Peixin Shen
Zhuohua Zhao
Yaping Yan
Libin Wang
Xinyu Lu
Yuan Zhang
Xing Li
Intraperitoneal injection but not oral administration of ellagic acid: a novel immunomodulator via targeting casein kinase 2 signaling pathway
Food Science and Human Wellness
ellagic acid
experimental autoimmune encephalomyelitis
neuromyelitis optica
organ transplantation
casein kinase ⅱ
t helper cell 17
title Intraperitoneal injection but not oral administration of ellagic acid: a novel immunomodulator via targeting casein kinase 2 signaling pathway
title_full Intraperitoneal injection but not oral administration of ellagic acid: a novel immunomodulator via targeting casein kinase 2 signaling pathway
title_fullStr Intraperitoneal injection but not oral administration of ellagic acid: a novel immunomodulator via targeting casein kinase 2 signaling pathway
title_full_unstemmed Intraperitoneal injection but not oral administration of ellagic acid: a novel immunomodulator via targeting casein kinase 2 signaling pathway
title_short Intraperitoneal injection but not oral administration of ellagic acid: a novel immunomodulator via targeting casein kinase 2 signaling pathway
title_sort intraperitoneal injection but not oral administration of ellagic acid a novel immunomodulator via targeting casein kinase 2 signaling pathway
topic ellagic acid
experimental autoimmune encephalomyelitis
neuromyelitis optica
organ transplantation
casein kinase ⅱ
t helper cell 17
url https://www.sciopen.com/article/10.26599/FSHW.2024.9250157
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