Inositol polyphosphate multikinase regulates Th1 and Th17 cell differentiation by controlling Akt-mTOR signaling

Summary: Activated proinflammatory T helper (Th) cells, including Th1 and Th17 cells, drive immune responses against pathogens and contribute to autoimmune diseases. We show that the expression of inositol polyphosphate multikinase (IPMK), an enzyme essential for inositol phosphate metabolism, is hi...

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Main Authors: Chae Min Yuk, Sehoon Hong, Dongeon Kim, Mingyo Kim, Hyun-Woo Jeong, Seung Ju Park, Hyungyu Min, Wooseob Kim, Jongbu Lim, Hyo Dam Kim, Sang-Gyu Kim, Rho Hyun Seong, Seyun Kim, Seung-Hyo Lee
Format: Article
Language:English
Published: Elsevier 2025-02-01
Series:Cell Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S221112472500052X
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author Chae Min Yuk
Sehoon Hong
Dongeon Kim
Mingyo Kim
Hyun-Woo Jeong
Seung Ju Park
Hyungyu Min
Wooseob Kim
Jongbu Lim
Hyo Dam Kim
Sang-Gyu Kim
Rho Hyun Seong
Seyun Kim
Seung-Hyo Lee
author_facet Chae Min Yuk
Sehoon Hong
Dongeon Kim
Mingyo Kim
Hyun-Woo Jeong
Seung Ju Park
Hyungyu Min
Wooseob Kim
Jongbu Lim
Hyo Dam Kim
Sang-Gyu Kim
Rho Hyun Seong
Seyun Kim
Seung-Hyo Lee
author_sort Chae Min Yuk
collection DOAJ
description Summary: Activated proinflammatory T helper (Th) cells, including Th1 and Th17 cells, drive immune responses against pathogens and contribute to autoimmune diseases. We show that the expression of inositol polyphosphate multikinase (IPMK), an enzyme essential for inositol phosphate metabolism, is highly induced in Th1 and Th17 subsets. Deletion of IPMK in CD4+ T cells leads to diminished Th1- and Th17-mediated responses, reducing resistance to Leishmania major and attenuating experimental autoimmune encephalomyelitis. IPMK-deficient CD4+ T cells show impaired activation and Th17 differentiation, linked to the decreased activation of Akt, mTOR, and STAT3. Mechanistically, IPMK functions as a phosphatidylinositol 3-kinase to regulate phosphatidylinositol (3,4,5)-trisphosphate (PtdIns(3,4,5)P3) production, promoting T cell activation and effector functions. In IPMK-deficient CD4+ T cells, T cell receptor-stimulated PtdIns(3,4,5)P3 generation is abolished by wortmannin, suggesting IPMK acts in a wortmannin-sensitive manner. These findings establish IPMK as a critical regulator of Th1 and Th17 differentiation, underscoring its role in maintaining immune homeostasis.
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spelling doaj-art-74bfab9162e74517b35dcb8dbfa41f4b2025-08-20T03:11:33ZengElsevierCell Reports2211-12472025-02-0144211528110.1016/j.celrep.2025.115281Inositol polyphosphate multikinase regulates Th1 and Th17 cell differentiation by controlling Akt-mTOR signalingChae Min Yuk0Sehoon Hong1Dongeon Kim2Mingyo Kim3Hyun-Woo Jeong4Seung Ju Park5Hyungyu Min6Wooseob Kim7Jongbu Lim8Hyo Dam Kim9Sang-Gyu Kim10Rho Hyun Seong11Seyun Kim12Seung-Hyo Lee13Graduate School of Medical Science and Engineering, Korea Advanced Institute of Science and Technology (KAIST), Yuseong-Gu, Daejeon 34141, Republic of KoreaDepartment of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST), Yuseong-Gu, Daejeon 34141, Republic of KoreaGraduate School of Medical Science and Engineering, Korea Advanced Institute of Science and Technology (KAIST), Yuseong-Gu, Daejeon 34141, Republic of Korea; Biomedical Research Center, Korea Advanced Institute of Science and Technology (KAIST), Yuseong-Gu, Daejeon 34141, Republic of Korea; Department of Medicine, Stanford University School of Medicine, Stanford, CA 94305, USA; VA Palo Alto Health Care System, Stanford University School of Medicine, Stanford, CA 94305, USADivision of Rheumatology, Department of Internal Medicine, Gyeongsang National University Hospital, Jinju 52727, Republic of KoreaDepartment of Tissue Morphogenesis, Max Planck Institute for Molecular Biomedicine, 48149 Münster, Germany; Faculty of Medicine, University of Münster, 48149 Münster, GermanyDepartment of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST), Yuseong-Gu, Daejeon 34141, Republic of KoreaSchool of Biological Sciences and Institute of Molecular Biology and Genetics, Seoul National University, Seoul 08826, Republic of KoreaSchool of Biological Sciences and Institute of Molecular Biology and Genetics, Seoul National University, Seoul 08826, Republic of KoreaDepartment of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST), Yuseong-Gu, Daejeon 34141, Republic of KoreaDepartment of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST), Yuseong-Gu, Daejeon 34141, Republic of KoreaDepartment of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST), Yuseong-Gu, Daejeon 34141, Republic of KoreaSchool of Biological Sciences and Institute of Molecular Biology and Genetics, Seoul National University, Seoul 08826, Republic of Korea; Corresponding authorDepartment of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST), Yuseong-Gu, Daejeon 34141, Republic of Korea; KAIST Institute for the BioCentury, Korea Advanced Institute of Science and Technology (KAIST), Yuseong-Gu, Daejeon 34141, Republic of Korea; KAIST Stem Cell Center, Korea Advanced Institute of Science and Technology (KAIST), Yuseong-Gu, Daejeon 34141, Republic of Korea; Corresponding authorGraduate School of Medical Science and Engineering, Korea Advanced Institute of Science and Technology (KAIST), Yuseong-Gu, Daejeon 34141, Republic of Korea; Biomedical Research Center, Korea Advanced Institute of Science and Technology (KAIST), Yuseong-Gu, Daejeon 34141, Republic of Korea; Department of Medicine, College of Medicine, Korea University, Seoul 02841, Republic of Korea; Corresponding authorSummary: Activated proinflammatory T helper (Th) cells, including Th1 and Th17 cells, drive immune responses against pathogens and contribute to autoimmune diseases. We show that the expression of inositol polyphosphate multikinase (IPMK), an enzyme essential for inositol phosphate metabolism, is highly induced in Th1 and Th17 subsets. Deletion of IPMK in CD4+ T cells leads to diminished Th1- and Th17-mediated responses, reducing resistance to Leishmania major and attenuating experimental autoimmune encephalomyelitis. IPMK-deficient CD4+ T cells show impaired activation and Th17 differentiation, linked to the decreased activation of Akt, mTOR, and STAT3. Mechanistically, IPMK functions as a phosphatidylinositol 3-kinase to regulate phosphatidylinositol (3,4,5)-trisphosphate (PtdIns(3,4,5)P3) production, promoting T cell activation and effector functions. In IPMK-deficient CD4+ T cells, T cell receptor-stimulated PtdIns(3,4,5)P3 generation is abolished by wortmannin, suggesting IPMK acts in a wortmannin-sensitive manner. These findings establish IPMK as a critical regulator of Th1 and Th17 differentiation, underscoring its role in maintaining immune homeostasis.http://www.sciencedirect.com/science/article/pii/S221112472500052XCP: ImmunologyCP: Metabolism
spellingShingle Chae Min Yuk
Sehoon Hong
Dongeon Kim
Mingyo Kim
Hyun-Woo Jeong
Seung Ju Park
Hyungyu Min
Wooseob Kim
Jongbu Lim
Hyo Dam Kim
Sang-Gyu Kim
Rho Hyun Seong
Seyun Kim
Seung-Hyo Lee
Inositol polyphosphate multikinase regulates Th1 and Th17 cell differentiation by controlling Akt-mTOR signaling
Cell Reports
CP: Immunology
CP: Metabolism
title Inositol polyphosphate multikinase regulates Th1 and Th17 cell differentiation by controlling Akt-mTOR signaling
title_full Inositol polyphosphate multikinase regulates Th1 and Th17 cell differentiation by controlling Akt-mTOR signaling
title_fullStr Inositol polyphosphate multikinase regulates Th1 and Th17 cell differentiation by controlling Akt-mTOR signaling
title_full_unstemmed Inositol polyphosphate multikinase regulates Th1 and Th17 cell differentiation by controlling Akt-mTOR signaling
title_short Inositol polyphosphate multikinase regulates Th1 and Th17 cell differentiation by controlling Akt-mTOR signaling
title_sort inositol polyphosphate multikinase regulates th1 and th17 cell differentiation by controlling akt mtor signaling
topic CP: Immunology
CP: Metabolism
url http://www.sciencedirect.com/science/article/pii/S221112472500052X
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