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Research ArticleArticle

Gossypetin Prevents the Progression of Nonalcoholic Steatohepatitis by Regulating Oxidative Stress and AMP-Activated Protein Kinase

Eunji Oh, Jae Lee, Sungji Cho, Sung Wook Kim, Kyung Won [Jo], Won Sik Shin, Seung Hee Gwak, Joohun Ha, So Yeon Jeon, Jin-Hyang Park, Im-Sook Song, Themis Thoudam, In-Kyu Lee, Seonyong Kim, Se-Young Choi and Kyong-Tai Kim
Molecular Pharmacology November 2023, 104 (5) 214-229; DOI: https://doi.org/10.1124/molpharm.123.000675
Eunji Oh
Department of Life Sciences, Pohang University of Science and Technology, Pohang Republic of Korea (E.O., J.L., S.C., S.W.K., K.W.J., W.S.S., S.H.G., K-T.K.); Department of Biochemistry and Molecular Biology, Graduate School, College of Medicine, Kyung Hee University, Seoul, Republic of Korea (J.H.); College of Pharmacy, Dankook University, Cheonan, Republic of Korea (S.Y.J.); College of Pharmacy, Kyungpook National University, Daegu, Republic of Korea (J-H.P., I.-M.S.); Research Institute of Aging and Metabolism, Kyungpook National University, Daegu, Republic of Korea (T.T., I.-K.L.); Department of Internal Medicine, School of Medicine, Kyungpook National University, Kyungpook National University Hospital, Daegu, Republic of Korea (I.-K.L.); Department of Physiology, Dental Research Institute, Seoul National University School of Dentistry, Seoul, Republic of Korea (S.K., S-Y.C.); and Generative Genomics Research Center, Global Green Research & Development Center, Handong Global University, Pohang, Republic of Korea (K.-T.K.)
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Jae Lee
Department of Life Sciences, Pohang University of Science and Technology, Pohang Republic of Korea (E.O., J.L., S.C., S.W.K., K.W.J., W.S.S., S.H.G., K-T.K.); Department of Biochemistry and Molecular Biology, Graduate School, College of Medicine, Kyung Hee University, Seoul, Republic of Korea (J.H.); College of Pharmacy, Dankook University, Cheonan, Republic of Korea (S.Y.J.); College of Pharmacy, Kyungpook National University, Daegu, Republic of Korea (J-H.P., I.-M.S.); Research Institute of Aging and Metabolism, Kyungpook National University, Daegu, Republic of Korea (T.T., I.-K.L.); Department of Internal Medicine, School of Medicine, Kyungpook National University, Kyungpook National University Hospital, Daegu, Republic of Korea (I.-K.L.); Department of Physiology, Dental Research Institute, Seoul National University School of Dentistry, Seoul, Republic of Korea (S.K., S-Y.C.); and Generative Genomics Research Center, Global Green Research & Development Center, Handong Global University, Pohang, Republic of Korea (K.-T.K.)
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Sungji Cho
Department of Life Sciences, Pohang University of Science and Technology, Pohang Republic of Korea (E.O., J.L., S.C., S.W.K., K.W.J., W.S.S., S.H.G., K-T.K.); Department of Biochemistry and Molecular Biology, Graduate School, College of Medicine, Kyung Hee University, Seoul, Republic of Korea (J.H.); College of Pharmacy, Dankook University, Cheonan, Republic of Korea (S.Y.J.); College of Pharmacy, Kyungpook National University, Daegu, Republic of Korea (J-H.P., I.-M.S.); Research Institute of Aging and Metabolism, Kyungpook National University, Daegu, Republic of Korea (T.T., I.-K.L.); Department of Internal Medicine, School of Medicine, Kyungpook National University, Kyungpook National University Hospital, Daegu, Republic of Korea (I.-K.L.); Department of Physiology, Dental Research Institute, Seoul National University School of Dentistry, Seoul, Republic of Korea (S.K., S-Y.C.); and Generative Genomics Research Center, Global Green Research & Development Center, Handong Global University, Pohang, Republic of Korea (K.-T.K.)
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Sung Wook Kim
Department of Life Sciences, Pohang University of Science and Technology, Pohang Republic of Korea (E.O., J.L., S.C., S.W.K., K.W.J., W.S.S., S.H.G., K-T.K.); Department of Biochemistry and Molecular Biology, Graduate School, College of Medicine, Kyung Hee University, Seoul, Republic of Korea (J.H.); College of Pharmacy, Dankook University, Cheonan, Republic of Korea (S.Y.J.); College of Pharmacy, Kyungpook National University, Daegu, Republic of Korea (J-H.P., I.-M.S.); Research Institute of Aging and Metabolism, Kyungpook National University, Daegu, Republic of Korea (T.T., I.-K.L.); Department of Internal Medicine, School of Medicine, Kyungpook National University, Kyungpook National University Hospital, Daegu, Republic of Korea (I.-K.L.); Department of Physiology, Dental Research Institute, Seoul National University School of Dentistry, Seoul, Republic of Korea (S.K., S-Y.C.); and Generative Genomics Research Center, Global Green Research & Development Center, Handong Global University, Pohang, Republic of Korea (K.-T.K.)
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Kyung Won
Department of Life Sciences, Pohang University of Science and Technology, Pohang Republic of Korea (E.O., J.L., S.C., S.W.K., K.W.J., W.S.S., S.H.G., K-T.K.); Department of Biochemistry and Molecular Biology, Graduate School, College of Medicine, Kyung Hee University, Seoul, Republic of Korea (J.H.); College of Pharmacy, Dankook University, Cheonan, Republic of Korea (S.Y.J.); College of Pharmacy, Kyungpook National University, Daegu, Republic of Korea (J-H.P., I.-M.S.); Research Institute of Aging and Metabolism, Kyungpook National University, Daegu, Republic of Korea (T.T., I.-K.L.); Department of Internal Medicine, School of Medicine, Kyungpook National University, Kyungpook National University Hospital, Daegu, Republic of Korea (I.-K.L.); Department of Physiology, Dental Research Institute, Seoul National University School of Dentistry, Seoul, Republic of Korea (S.K., S-Y.C.); and Generative Genomics Research Center, Global Green Research & Development Center, Handong Global University, Pohang, Republic of Korea (K.-T.K.)
Jo
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Won Sik Shin
Department of Life Sciences, Pohang University of Science and Technology, Pohang Republic of Korea (E.O., J.L., S.C., S.W.K., K.W.J., W.S.S., S.H.G., K-T.K.); Department of Biochemistry and Molecular Biology, Graduate School, College of Medicine, Kyung Hee University, Seoul, Republic of Korea (J.H.); College of Pharmacy, Dankook University, Cheonan, Republic of Korea (S.Y.J.); College of Pharmacy, Kyungpook National University, Daegu, Republic of Korea (J-H.P., I.-M.S.); Research Institute of Aging and Metabolism, Kyungpook National University, Daegu, Republic of Korea (T.T., I.-K.L.); Department of Internal Medicine, School of Medicine, Kyungpook National University, Kyungpook National University Hospital, Daegu, Republic of Korea (I.-K.L.); Department of Physiology, Dental Research Institute, Seoul National University School of Dentistry, Seoul, Republic of Korea (S.K., S-Y.C.); and Generative Genomics Research Center, Global Green Research & Development Center, Handong Global University, Pohang, Republic of Korea (K.-T.K.)
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Seung Hee Gwak
Department of Life Sciences, Pohang University of Science and Technology, Pohang Republic of Korea (E.O., J.L., S.C., S.W.K., K.W.J., W.S.S., S.H.G., K-T.K.); Department of Biochemistry and Molecular Biology, Graduate School, College of Medicine, Kyung Hee University, Seoul, Republic of Korea (J.H.); College of Pharmacy, Dankook University, Cheonan, Republic of Korea (S.Y.J.); College of Pharmacy, Kyungpook National University, Daegu, Republic of Korea (J-H.P., I.-M.S.); Research Institute of Aging and Metabolism, Kyungpook National University, Daegu, Republic of Korea (T.T., I.-K.L.); Department of Internal Medicine, School of Medicine, Kyungpook National University, Kyungpook National University Hospital, Daegu, Republic of Korea (I.-K.L.); Department of Physiology, Dental Research Institute, Seoul National University School of Dentistry, Seoul, Republic of Korea (S.K., S-Y.C.); and Generative Genomics Research Center, Global Green Research & Development Center, Handong Global University, Pohang, Republic of Korea (K.-T.K.)
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Joohun Ha
Department of Life Sciences, Pohang University of Science and Technology, Pohang Republic of Korea (E.O., J.L., S.C., S.W.K., K.W.J., W.S.S., S.H.G., K-T.K.); Department of Biochemistry and Molecular Biology, Graduate School, College of Medicine, Kyung Hee University, Seoul, Republic of Korea (J.H.); College of Pharmacy, Dankook University, Cheonan, Republic of Korea (S.Y.J.); College of Pharmacy, Kyungpook National University, Daegu, Republic of Korea (J-H.P., I.-M.S.); Research Institute of Aging and Metabolism, Kyungpook National University, Daegu, Republic of Korea (T.T., I.-K.L.); Department of Internal Medicine, School of Medicine, Kyungpook National University, Kyungpook National University Hospital, Daegu, Republic of Korea (I.-K.L.); Department of Physiology, Dental Research Institute, Seoul National University School of Dentistry, Seoul, Republic of Korea (S.K., S-Y.C.); and Generative Genomics Research Center, Global Green Research & Development Center, Handong Global University, Pohang, Republic of Korea (K.-T.K.)
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So Yeon Jeon
Department of Life Sciences, Pohang University of Science and Technology, Pohang Republic of Korea (E.O., J.L., S.C., S.W.K., K.W.J., W.S.S., S.H.G., K-T.K.); Department of Biochemistry and Molecular Biology, Graduate School, College of Medicine, Kyung Hee University, Seoul, Republic of Korea (J.H.); College of Pharmacy, Dankook University, Cheonan, Republic of Korea (S.Y.J.); College of Pharmacy, Kyungpook National University, Daegu, Republic of Korea (J-H.P., I.-M.S.); Research Institute of Aging and Metabolism, Kyungpook National University, Daegu, Republic of Korea (T.T., I.-K.L.); Department of Internal Medicine, School of Medicine, Kyungpook National University, Kyungpook National University Hospital, Daegu, Republic of Korea (I.-K.L.); Department of Physiology, Dental Research Institute, Seoul National University School of Dentistry, Seoul, Republic of Korea (S.K., S-Y.C.); and Generative Genomics Research Center, Global Green Research & Development Center, Handong Global University, Pohang, Republic of Korea (K.-T.K.)
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Jin-Hyang Park
Department of Life Sciences, Pohang University of Science and Technology, Pohang Republic of Korea (E.O., J.L., S.C., S.W.K., K.W.J., W.S.S., S.H.G., K-T.K.); Department of Biochemistry and Molecular Biology, Graduate School, College of Medicine, Kyung Hee University, Seoul, Republic of Korea (J.H.); College of Pharmacy, Dankook University, Cheonan, Republic of Korea (S.Y.J.); College of Pharmacy, Kyungpook National University, Daegu, Republic of Korea (J-H.P., I.-M.S.); Research Institute of Aging and Metabolism, Kyungpook National University, Daegu, Republic of Korea (T.T., I.-K.L.); Department of Internal Medicine, School of Medicine, Kyungpook National University, Kyungpook National University Hospital, Daegu, Republic of Korea (I.-K.L.); Department of Physiology, Dental Research Institute, Seoul National University School of Dentistry, Seoul, Republic of Korea (S.K., S-Y.C.); and Generative Genomics Research Center, Global Green Research & Development Center, Handong Global University, Pohang, Republic of Korea (K.-T.K.)
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Im-Sook Song
Department of Life Sciences, Pohang University of Science and Technology, Pohang Republic of Korea (E.O., J.L., S.C., S.W.K., K.W.J., W.S.S., S.H.G., K-T.K.); Department of Biochemistry and Molecular Biology, Graduate School, College of Medicine, Kyung Hee University, Seoul, Republic of Korea (J.H.); College of Pharmacy, Dankook University, Cheonan, Republic of Korea (S.Y.J.); College of Pharmacy, Kyungpook National University, Daegu, Republic of Korea (J-H.P., I.-M.S.); Research Institute of Aging and Metabolism, Kyungpook National University, Daegu, Republic of Korea (T.T., I.-K.L.); Department of Internal Medicine, School of Medicine, Kyungpook National University, Kyungpook National University Hospital, Daegu, Republic of Korea (I.-K.L.); Department of Physiology, Dental Research Institute, Seoul National University School of Dentistry, Seoul, Republic of Korea (S.K., S-Y.C.); and Generative Genomics Research Center, Global Green Research & Development Center, Handong Global University, Pohang, Republic of Korea (K.-T.K.)
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Themis Thoudam
Department of Life Sciences, Pohang University of Science and Technology, Pohang Republic of Korea (E.O., J.L., S.C., S.W.K., K.W.J., W.S.S., S.H.G., K-T.K.); Department of Biochemistry and Molecular Biology, Graduate School, College of Medicine, Kyung Hee University, Seoul, Republic of Korea (J.H.); College of Pharmacy, Dankook University, Cheonan, Republic of Korea (S.Y.J.); College of Pharmacy, Kyungpook National University, Daegu, Republic of Korea (J-H.P., I.-M.S.); Research Institute of Aging and Metabolism, Kyungpook National University, Daegu, Republic of Korea (T.T., I.-K.L.); Department of Internal Medicine, School of Medicine, Kyungpook National University, Kyungpook National University Hospital, Daegu, Republic of Korea (I.-K.L.); Department of Physiology, Dental Research Institute, Seoul National University School of Dentistry, Seoul, Republic of Korea (S.K., S-Y.C.); and Generative Genomics Research Center, Global Green Research & Development Center, Handong Global University, Pohang, Republic of Korea (K.-T.K.)
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In-Kyu Lee
Department of Life Sciences, Pohang University of Science and Technology, Pohang Republic of Korea (E.O., J.L., S.C., S.W.K., K.W.J., W.S.S., S.H.G., K-T.K.); Department of Biochemistry and Molecular Biology, Graduate School, College of Medicine, Kyung Hee University, Seoul, Republic of Korea (J.H.); College of Pharmacy, Dankook University, Cheonan, Republic of Korea (S.Y.J.); College of Pharmacy, Kyungpook National University, Daegu, Republic of Korea (J-H.P., I.-M.S.); Research Institute of Aging and Metabolism, Kyungpook National University, Daegu, Republic of Korea (T.T., I.-K.L.); Department of Internal Medicine, School of Medicine, Kyungpook National University, Kyungpook National University Hospital, Daegu, Republic of Korea (I.-K.L.); Department of Physiology, Dental Research Institute, Seoul National University School of Dentistry, Seoul, Republic of Korea (S.K., S-Y.C.); and Generative Genomics Research Center, Global Green Research & Development Center, Handong Global University, Pohang, Republic of Korea (K.-T.K.)
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Seonyong Kim
Department of Life Sciences, Pohang University of Science and Technology, Pohang Republic of Korea (E.O., J.L., S.C., S.W.K., K.W.J., W.S.S., S.H.G., K-T.K.); Department of Biochemistry and Molecular Biology, Graduate School, College of Medicine, Kyung Hee University, Seoul, Republic of Korea (J.H.); College of Pharmacy, Dankook University, Cheonan, Republic of Korea (S.Y.J.); College of Pharmacy, Kyungpook National University, Daegu, Republic of Korea (J-H.P., I.-M.S.); Research Institute of Aging and Metabolism, Kyungpook National University, Daegu, Republic of Korea (T.T., I.-K.L.); Department of Internal Medicine, School of Medicine, Kyungpook National University, Kyungpook National University Hospital, Daegu, Republic of Korea (I.-K.L.); Department of Physiology, Dental Research Institute, Seoul National University School of Dentistry, Seoul, Republic of Korea (S.K., S-Y.C.); and Generative Genomics Research Center, Global Green Research & Development Center, Handong Global University, Pohang, Republic of Korea (K.-T.K.)
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Se-Young Choi
Department of Life Sciences, Pohang University of Science and Technology, Pohang Republic of Korea (E.O., J.L., S.C., S.W.K., K.W.J., W.S.S., S.H.G., K-T.K.); Department of Biochemistry and Molecular Biology, Graduate School, College of Medicine, Kyung Hee University, Seoul, Republic of Korea (J.H.); College of Pharmacy, Dankook University, Cheonan, Republic of Korea (S.Y.J.); College of Pharmacy, Kyungpook National University, Daegu, Republic of Korea (J-H.P., I.-M.S.); Research Institute of Aging and Metabolism, Kyungpook National University, Daegu, Republic of Korea (T.T., I.-K.L.); Department of Internal Medicine, School of Medicine, Kyungpook National University, Kyungpook National University Hospital, Daegu, Republic of Korea (I.-K.L.); Department of Physiology, Dental Research Institute, Seoul National University School of Dentistry, Seoul, Republic of Korea (S.K., S-Y.C.); and Generative Genomics Research Center, Global Green Research & Development Center, Handong Global University, Pohang, Republic of Korea (K.-T.K.)
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Kyong-Tai Kim
Department of Life Sciences, Pohang University of Science and Technology, Pohang Republic of Korea (E.O., J.L., S.C., S.W.K., K.W.J., W.S.S., S.H.G., K-T.K.); Department of Biochemistry and Molecular Biology, Graduate School, College of Medicine, Kyung Hee University, Seoul, Republic of Korea (J.H.); College of Pharmacy, Dankook University, Cheonan, Republic of Korea (S.Y.J.); College of Pharmacy, Kyungpook National University, Daegu, Republic of Korea (J-H.P., I.-M.S.); Research Institute of Aging and Metabolism, Kyungpook National University, Daegu, Republic of Korea (T.T., I.-K.L.); Department of Internal Medicine, School of Medicine, Kyungpook National University, Kyungpook National University Hospital, Daegu, Republic of Korea (I.-K.L.); Department of Physiology, Dental Research Institute, Seoul National University School of Dentistry, Seoul, Republic of Korea (S.K., S-Y.C.); and Generative Genomics Research Center, Global Green Research & Development Center, Handong Global University, Pohang, Republic of Korea (K.-T.K.)
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Abstract

Nonalcoholic steatohepatitis (NASH) is a severe liver metabolic disorder, however, there are still no effective and safe drugs for its treatment. Previous clinical trials used various therapeutic approaches to target individual pathologic mechanisms, but these approaches were unsuccessful because of the complex pathologic causes of NASH. Combinatory therapy in which two or more drugs are administered simultaneously to patients with NASH, however, carries the risk of side effects associated with each individual drug. To solve this problem, we identified gossypetin as an effective dual-targeting agent that activates AMP-activated protein kinase (AMPK) and decreases oxidative stress. Administration of gossypetin decreased hepatic steatosis, lobular inflammation and liver fibrosis in the liver tissue of mice with choline-deficient high-fat diet and methionine-choline deficient diet (MCD) diet-induced NASH. Gossypetin functioned directly as an antioxidant agent, decreasing hydrogen peroxide and palmitate-induced oxidative stress in the AML12 cells and liver tissue of MCD diet-fed mice without regulating the antioxidant response factors. In addition, gossypetin acted as a novel AMPK activator by binding to the allosteric drug and metabolite site, which stabilizes the activated structure of AMPK. Our findings demonstrate that gossypetin has the potential to serve as a novel therapeutic agent for nonalcoholic fatty liver disease /NASH.

SIGNIFICANCE STATEMENT This study demonstrates that gossypetin has preventive effect to progression of nonalcoholic steatohepatitis (NASH) as a novel AMP-activated protein kinase (AMPK) activator and antioxidants. Our findings indicate that simultaneous activation of AMPK and oxidative stress using gossypetin has the potential to serve as a novel therapeutic approach for nonalcoholic fatty liver disease /NASH patients.

Footnotes

    • Received January 14, 2023.
    • Accepted July 25, 2023.
  • This work was carried out with the support of “Cooperative Research Program for Agriculture Science and Technology Development (Project No. PJ01640202)” Rural Development Administration, Republic of Korea and funds donated by Dr. Jae Kyu Lee and Mr. Jason Gim. This research was also supported by the BK21 FOUR funded by the Ministry of Education, Republic of Korea.

  • The authors declare no conflict of interest.

  • dx.doi.org/10.1124/molpharm.123.000675.

  • ↵Embedded ImageThis article has supplemental material available at molpharm.aspetjournals.org.

  • Copyright © 2023 by The American Society for Pharmacology and Experimental Therapeutics
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Molecular Pharmacology: 104 (5)
Molecular Pharmacology
Vol. 104, Issue 5
1 Nov 2023
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Research ArticleArticle

Gossypetin Alleviates NASH as Dual Targeting Agents

Eunji Oh, Jae Lee, Sungji Cho, Sung Wook Kim, Kyung Won, Won Sik Shin, Seung Hee Gwak, Joohun Ha, So Yeon Jeon, Jin-Hyang Park, Im-Sook Song, Themis Thoudam, In-Kyu Lee, Seonyong Kim, Se-Young Choi and Kyong-Tai Kim
Molecular Pharmacology November 1, 2023, 104 (5) 214-229; DOI: https://doi.org/10.1124/molpharm.123.000675

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Research ArticleArticle

Gossypetin Alleviates NASH as Dual Targeting Agents

Eunji Oh, Jae Lee, Sungji Cho, Sung Wook Kim, Kyung Won, Won Sik Shin, Seung Hee Gwak, Joohun Ha, So Yeon Jeon, Jin-Hyang Park, Im-Sook Song, Themis Thoudam, In-Kyu Lee, Seonyong Kim, Se-Young Choi and Kyong-Tai Kim
Molecular Pharmacology November 1, 2023, 104 (5) 214-229; DOI: https://doi.org/10.1124/molpharm.123.000675
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