Inhibition of 7-dehydrocholesterol reductase prevents hepatic ferroptosis under an active state of sterol synthesis

Recent evidence indicates ferroptosis is implicated in the pathophysiology of various liver diseases; however, the organ-specific regulation mechanism is poorly understood. Here, we demonstrate 7-dehydrocholesterol reductase (DHCR7), the terminal enzyme of cholesterol biosynthesis, as a regulator of...

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Published in:	Nature communications Vol. 15; no. 1; pp. 2195 - 14
Main Authors:	Yamada, Naoya, Karasawa, Tadayoshi, Ito, Junya, Yamamuro, Daisuke, Morimoto, Kazushi, Nakamura, Toshitaka, Komada, Takanori, Baatarjav, Chintogtokh, Saimoto, Yuma, Jinnouchi, Yuka, Watanabe, Kazuhisa, Miura, Kouichi, Yahagi, Naoya, Nakagawa, Kiyotaka, Matsumura, Takayoshi, Yamada, Ken-ichi, Ishibashi, Shun, Sata, Naohiro, Conrad, Marcus, Takahashi, Masafumi
Format:	Journal Article
Language:	English
Published:	London Nature Publishing Group UK 12.03.2024 Nature Publishing Group Nature Portfolio
Subjects:	13 14/19 38/43 49/40 631/80/82 64/60 692/4020/4021/288/2032 692/699/1503/1607 7-Dehydrocholesterol reductase 82/1 82/58 82/80 Ablation Acetaminophen Animals Biosynthesis Cholesterol Cyclodextrins Electron paramagnetic resonance Electron spin Electron spin resonance Electrons Enzymes Ferroptosis Hepatocellular carcinoma Hepatocytes Humanities and Social Sciences Humans Injury prevention Ischemia Liver Liver cancer Liver Diseases Liver failure Metabolites Mice multidisciplinary Oxidation Oxidoreductases Acting on CH-CH Group Donors - metabolism Pathophysiology Reductases Regulatory mechanisms (biology) Reperfusion Science Science (multidisciplinary) Spin resonance Substrate inhibition trans-1,4-Bis(2-chlorobenzaminomethyl)cyclohexane Dihydrochloride β-Cyclodextrin
ISSN:	2041-1723, 2041-1723
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Abstract	Recent evidence indicates ferroptosis is implicated in the pathophysiology of various liver diseases; however, the organ-specific regulation mechanism is poorly understood. Here, we demonstrate 7-dehydrocholesterol reductase (DHCR7), the terminal enzyme of cholesterol biosynthesis, as a regulator of ferroptosis in hepatocytes. Genetic and pharmacological inhibition (with AY9944) of DHCR7 suppress ferroptosis in human hepatocellular carcinoma Huh-7 cells. DHCR7 inhibition increases its substrate, 7-dehydrocholesterol (7-DHC). Furthermore, exogenous 7-DHC supplementation using hydroxypropyl β-cyclodextrin suppresses ferroptosis. A 7-DHC-derived oxysterol metabolite, 3β,5α-dihydroxycholest-7-en-6-one (DHCEO), is increased by the ferroptosis-inducer RSL-3 in DHCR7 -deficient cells, suggesting that the ferroptosis-suppressive effect of DHCR7 inhibition is associated with the oxidation of 7-DHC. Electron spin resonance analysis reveals that 7-DHC functions as a radical trapping agent, thus protecting cells from ferroptosis. We further show that AY9944 inhibits hepatic ischemia-reperfusion injury, and genetic ablation of Dhcr7 prevents acetaminophen-induced acute liver failure in mice. These findings provide new insights into the regulatory mechanism of liver ferroptosis and suggest a potential therapeutic option for ferroptosis-related liver diseases. Ferroptosis has been connected to liver disease through unclear mechanisms. Here, the authors identify the terminal enzyme of cholesterol synthesis, 7-dehydrocholesterol reductase, as a regulator of ferroptosis in hepatocytes that suppresses ferroptosis through 7-dehydrocholesterol accumulation.
AbstractList	Recent evidence indicates ferroptosis is implicated in the pathophysiology of various liver diseases; however, the organ-specific regulation mechanism is poorly understood. Here, we demonstrate 7-dehydrocholesterol reductase (DHCR7), the terminal enzyme of cholesterol biosynthesis, as a regulator of ferroptosis in hepatocytes. Genetic and pharmacological inhibition (with AY9944) of DHCR7 suppress ferroptosis in human hepatocellular carcinoma Huh-7 cells. DHCR7 inhibition increases its substrate, 7-dehydrocholesterol (7-DHC). Furthermore, exogenous 7-DHC supplementation using hydroxypropyl β-cyclodextrin suppresses ferroptosis. A 7-DHC-derived oxysterol metabolite, 3β,5α-dihydroxycholest-7-en-6-one (DHCEO), is increased by the ferroptosis-inducer RSL-3 in DHCR7 -deficient cells, suggesting that the ferroptosis-suppressive effect of DHCR7 inhibition is associated with the oxidation of 7-DHC. Electron spin resonance analysis reveals that 7-DHC functions as a radical trapping agent, thus protecting cells from ferroptosis. We further show that AY9944 inhibits hepatic ischemia-reperfusion injury, and genetic ablation of Dhcr7 prevents acetaminophen-induced acute liver failure in mice. These findings provide new insights into the regulatory mechanism of liver ferroptosis and suggest a potential therapeutic option for ferroptosis-related liver diseases. Ferroptosis has been connected to liver disease through unclear mechanisms. Here, the authors identify the terminal enzyme of cholesterol synthesis, 7-dehydrocholesterol reductase, as a regulator of ferroptosis in hepatocytes that suppresses ferroptosis through 7-dehydrocholesterol accumulation. Recent evidence indicates ferroptosis is implicated in the pathophysiology of various liver diseases; however, the organ-specific regulation mechanism is poorly understood. Here, we demonstrate 7-dehydrocholesterol reductase (DHCR7), the terminal enzyme of cholesterol biosynthesis, as a regulator of ferroptosis in hepatocytes. Genetic and pharmacological inhibition (with AY9944) of DHCR7 suppress ferroptosis in human hepatocellular carcinoma Huh-7 cells. DHCR7 inhibition increases its substrate, 7-dehydrocholesterol (7-DHC). Furthermore, exogenous 7-DHC supplementation using hydroxypropyl β-cyclodextrin suppresses ferroptosis. A 7-DHC-derived oxysterol metabolite, 3β,5α-dihydroxycholest-7-en-6-one (DHCEO), is increased by the ferroptosis-inducer RSL-3 in DHCR7-deficient cells, suggesting that the ferroptosis-suppressive effect of DHCR7 inhibition is associated with the oxidation of 7-DHC. Electron spin resonance analysis reveals that 7-DHC functions as a radical trapping agent, thus protecting cells from ferroptosis. We further show that AY9944 inhibits hepatic ischemia-reperfusion injury, and genetic ablation of Dhcr7 prevents acetaminophen-induced acute liver failure in mice. These findings provide new insights into the regulatory mechanism of liver ferroptosis and suggest a potential therapeutic option for ferroptosis-related liver diseases. Ferroptosis has been connected to liver disease through unclear mechanisms. Here, the authors identify the terminal enzyme of cholesterol synthesis, 7-dehydrocholesterol reductase, as a regulator of ferroptosis in hepatocytes that suppresses ferroptosis through 7-dehydrocholesterol accumulation. Recent evidence indicates ferroptosis is implicated in the pathophysiology of various liver diseases; however, the organ-specific regulation mechanism is poorly understood. Here, we demonstrate 7-dehydrocholesterol reductase (DHCR7), the terminal enzyme of cholesterol biosynthesis, as a regulator of ferroptosis in hepatocytes. Genetic and pharmacological inhibition (with AY9944) of DHCR7 suppress ferroptosis in human hepatocellular carcinoma Huh-7 cells. DHCR7 inhibition increases its substrate, 7-dehydrocholesterol (7-DHC). Furthermore, exogenous 7-DHC supplementation using hydroxypropyl β-cyclodextrin suppresses ferroptosis. A 7-DHC-derived oxysterol metabolite, 3β,5α-dihydroxycholest-7-en-6-one (DHCEO), is increased by the ferroptosis-inducer RSL-3 in DHCR7-deficient cells, suggesting that the ferroptosis-suppressive effect of DHCR7 inhibition is associated with the oxidation of 7-DHC. Electron spin resonance analysis reveals that 7-DHC functions as a radical trapping agent, thus protecting cells from ferroptosis. We further show that AY9944 inhibits hepatic ischemia-reperfusion injury, and genetic ablation of Dhcr7 prevents acetaminophen-induced acute liver failure in mice. These findings provide new insights into the regulatory mechanism of liver ferroptosis and suggest a potential therapeutic option for ferroptosis-related liver diseases. Recent evidence indicates ferroptosis is implicated in the pathophysiology of various liver diseases; however, the organ-specific regulation mechanism is poorly understood. Here, we demonstrate 7-dehydrocholesterol reductase (DHCR7), the terminal enzyme of cholesterol biosynthesis, as a regulator of ferroptosis in hepatocytes. Genetic and pharmacological inhibition (with AY9944) of DHCR7 suppress ferroptosis in human hepatocellular carcinoma Huh-7 cells. DHCR7 inhibition increases its substrate, 7-dehydrocholesterol (7-DHC). Furthermore, exogenous 7-DHC supplementation using hydroxypropyl β-cyclodextrin suppresses ferroptosis. A 7-DHC-derived oxysterol metabolite, 3β,5α-dihydroxycholest-7-en-6-one (DHCEO), is increased by the ferroptosis-inducer RSL-3 in DHCR7 -deficient cells, suggesting that the ferroptosis-suppressive effect of DHCR7 inhibition is associated with the oxidation of 7-DHC. Electron spin resonance analysis reveals that 7-DHC functions as a radical trapping agent, thus protecting cells from ferroptosis. We further show that AY9944 inhibits hepatic ischemia-reperfusion injury, and genetic ablation of Dhcr7 prevents acetaminophen-induced acute liver failure in mice. These findings provide new insights into the regulatory mechanism of liver ferroptosis and suggest a potential therapeutic option for ferroptosis-related liver diseases. Abstract Recent evidence indicates ferroptosis is implicated in the pathophysiology of various liver diseases; however, the organ-specific regulation mechanism is poorly understood. Here, we demonstrate 7-dehydrocholesterol reductase (DHCR7), the terminal enzyme of cholesterol biosynthesis, as a regulator of ferroptosis in hepatocytes. Genetic and pharmacological inhibition (with AY9944) of DHCR7 suppress ferroptosis in human hepatocellular carcinoma Huh-7 cells. DHCR7 inhibition increases its substrate, 7-dehydrocholesterol (7-DHC). Furthermore, exogenous 7-DHC supplementation using hydroxypropyl β-cyclodextrin suppresses ferroptosis. A 7-DHC-derived oxysterol metabolite, 3β,5α-dihydroxycholest-7-en-6-one (DHCEO), is increased by the ferroptosis-inducer RSL-3 in DHCR7-deficient cells, suggesting that the ferroptosis-suppressive effect of DHCR7 inhibition is associated with the oxidation of 7-DHC. Electron spin resonance analysis reveals that 7-DHC functions as a radical trapping agent, thus protecting cells from ferroptosis. We further show that AY9944 inhibits hepatic ischemia-reperfusion injury, and genetic ablation of Dhcr7 prevents acetaminophen-induced acute liver failure in mice. These findings provide new insights into the regulatory mechanism of liver ferroptosis and suggest a potential therapeutic option for ferroptosis-related liver diseases. Recent evidence indicates ferroptosis is implicated in the pathophysiology of various liver diseases; however, the organ-specific regulation mechanism is poorly understood. Here, we demonstrate 7-dehydrocholesterol reductase (DHCR7), the terminal enzyme of cholesterol biosynthesis, as a regulator of ferroptosis in hepatocytes. Genetic and pharmacological inhibition (with AY9944) of DHCR7 suppress ferroptosis in human hepatocellular carcinoma Huh-7 cells. DHCR7 inhibition increases its substrate, 7-dehydrocholesterol (7-DHC). Furthermore, exogenous 7-DHC supplementation using hydroxypropyl β-cyclodextrin suppresses ferroptosis. A 7-DHC-derived oxysterol metabolite, 3β,5α-dihydroxycholest-7-en-6-one (DHCEO), is increased by the ferroptosis-inducer RSL-3 in DHCR7-deficient cells, suggesting that the ferroptosis-suppressive effect of DHCR7 inhibition is associated with the oxidation of 7-DHC. Electron spin resonance analysis reveals that 7-DHC functions as a radical trapping agent, thus protecting cells from ferroptosis. We further show that AY9944 inhibits hepatic ischemia-reperfusion injury, and genetic ablation of Dhcr7 prevents acetaminophen-induced acute liver failure in mice. These findings provide new insights into the regulatory mechanism of liver ferroptosis and suggest a potential therapeutic option for ferroptosis-related liver diseases.Recent evidence indicates ferroptosis is implicated in the pathophysiology of various liver diseases; however, the organ-specific regulation mechanism is poorly understood. Here, we demonstrate 7-dehydrocholesterol reductase (DHCR7), the terminal enzyme of cholesterol biosynthesis, as a regulator of ferroptosis in hepatocytes. Genetic and pharmacological inhibition (with AY9944) of DHCR7 suppress ferroptosis in human hepatocellular carcinoma Huh-7 cells. DHCR7 inhibition increases its substrate, 7-dehydrocholesterol (7-DHC). Furthermore, exogenous 7-DHC supplementation using hydroxypropyl β-cyclodextrin suppresses ferroptosis. A 7-DHC-derived oxysterol metabolite, 3β,5α-dihydroxycholest-7-en-6-one (DHCEO), is increased by the ferroptosis-inducer RSL-3 in DHCR7-deficient cells, suggesting that the ferroptosis-suppressive effect of DHCR7 inhibition is associated with the oxidation of 7-DHC. Electron spin resonance analysis reveals that 7-DHC functions as a radical trapping agent, thus protecting cells from ferroptosis. We further show that AY9944 inhibits hepatic ischemia-reperfusion injury, and genetic ablation of Dhcr7 prevents acetaminophen-induced acute liver failure in mice. These findings provide new insights into the regulatory mechanism of liver ferroptosis and suggest a potential therapeutic option for ferroptosis-related liver diseases.
ArticleNumber	2195
Author	Karasawa, Tadayoshi Morimoto, Kazushi Takahashi, Masafumi Jinnouchi, Yuka Miura, Kouichi Komada, Takanori Conrad, Marcus Sata, Naohiro Baatarjav, Chintogtokh Watanabe, Kazuhisa Matsumura, Takayoshi Yahagi, Naoya Nakagawa, Kiyotaka Yamada, Naoya Yamamuro, Daisuke Yamada, Ken-ichi Nakamura, Toshitaka Saimoto, Yuma Ishibashi, Shun Ito, Junya
Author_xml	– sequence: 1 givenname: Naoya orcidid: 0000-0003-0111-028X surname: Yamada fullname: Yamada, Naoya email: naoya.yamada@helmholtz-munich.de organization: Division of Inflammation Research, Center for Molecular Medicine, Jichi Medical University, Division of Gastroenterological, General and Transplant Surgery, Department of Surgery, Jichi Medical University, Institute of Metabolism and Cell Death, Molecular Target and Therapeutics Center, Helmholtz Munich – sequence: 2 givenname: Tadayoshi orcidid: 0000-0002-6738-2360 surname: Karasawa fullname: Karasawa, Tadayoshi email: tdys.karasawa@jichi.ac.jp organization: Division of Inflammation Research, Center for Molecular Medicine, Jichi Medical University – sequence: 3 givenname: Junya surname: Ito fullname: Ito, Junya organization: Laboratory of Food Function Analysis, Graduate School of Agricultural Science, Tohoku University – sequence: 4 givenname: Daisuke surname: Yamamuro fullname: Yamamuro, Daisuke organization: Division of Endocrinology and Metabolism, Department of Medicine, Jichi Medical University – sequence: 5 givenname: Kazushi orcidid: 0000-0001-7698-9378 surname: Morimoto fullname: Morimoto, Kazushi organization: Department of Molecular Pathobiology, Faculty of Pharmaceutical Sciences, Kyushu University, Fukuoka – sequence: 6 givenname: Toshitaka orcidid: 0000-0002-4248-2058 surname: Nakamura fullname: Nakamura, Toshitaka organization: Institute of Metabolism and Cell Death, Molecular Target and Therapeutics Center, Helmholtz Munich – sequence: 7 givenname: Takanori orcidid: 0000-0003-3360-3185 surname: Komada fullname: Komada, Takanori organization: Division of Inflammation Research, Center for Molecular Medicine, Jichi Medical University – sequence: 8 givenname: Chintogtokh orcidid: 0000-0002-4565-9146 surname: Baatarjav fullname: Baatarjav, Chintogtokh organization: Division of Inflammation Research, Center for Molecular Medicine, Jichi Medical University – sequence: 9 givenname: Yuma surname: Saimoto fullname: Saimoto, Yuma organization: Department of Molecular Pathobiology, Faculty of Pharmaceutical Sciences, Kyushu University, Fukuoka – sequence: 10 givenname: Yuka surname: Jinnouchi fullname: Jinnouchi, Yuka organization: Department of Molecular Pathobiology, Faculty of Pharmaceutical Sciences, Kyushu University, Fukuoka – sequence: 11 givenname: Kazuhisa surname: Watanabe fullname: Watanabe, Kazuhisa organization: Division of Human Genetics, Center for Molecular Medicine, Jichi Medical University – sequence: 12 givenname: Kouichi surname: Miura fullname: Miura, Kouichi organization: Division of Gastroenterology, Department of Medicine, Jichi Medical University – sequence: 13 givenname: Naoya orcidid: 0000-0002-1823-1865 surname: Yahagi fullname: Yahagi, Naoya organization: Division of Endocrinology and Metabolism, Department of Medicine, Jichi Medical University – sequence: 14 givenname: Kiyotaka orcidid: 0000-0003-3026-7358 surname: Nakagawa fullname: Nakagawa, Kiyotaka organization: Laboratory of Food Function Analysis, Graduate School of Agricultural Science, Tohoku University – sequence: 15 givenname: Takayoshi orcidid: 0000-0003-3394-9506 surname: Matsumura fullname: Matsumura, Takayoshi organization: Division of Inflammation Research, Center for Molecular Medicine, Jichi Medical University, Division of Human Genetics, Center for Molecular Medicine, Jichi Medical University – sequence: 16 givenname: Ken-ichi orcidid: 0000-0003-2100-8477 surname: Yamada fullname: Yamada, Ken-ichi organization: Department of Molecular Pathobiology, Faculty of Pharmaceutical Sciences, Kyushu University, Fukuoka – sequence: 17 givenname: Shun surname: Ishibashi fullname: Ishibashi, Shun organization: Division of Endocrinology and Metabolism, Department of Medicine, Jichi Medical University – sequence: 18 givenname: Naohiro surname: Sata fullname: Sata, Naohiro organization: Division of Gastroenterological, General and Transplant Surgery, Department of Surgery, Jichi Medical University – sequence: 19 givenname: Marcus orcidid: 0000-0003-1140-5612 surname: Conrad fullname: Conrad, Marcus organization: Institute of Metabolism and Cell Death, Molecular Target and Therapeutics Center, Helmholtz Munich – sequence: 20 givenname: Masafumi orcidid: 0000-0003-2716-7532 surname: Takahashi fullname: Takahashi, Masafumi email: masafumi2@jichi.ac.jp organization: Division of Inflammation Research, Center for Molecular Medicine, Jichi Medical University
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/38472233$$D View this record in MEDLINE/PubMed
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Snippet	Recent evidence indicates ferroptosis is implicated in the pathophysiology of various liver diseases; however, the organ-specific regulation mechanism is... Abstract Recent evidence indicates ferroptosis is implicated in the pathophysiology of various liver diseases; however, the organ-specific regulation mechanism...
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SubjectTerms	13 14/19 38/43 49/40 631/80/82 64/60 692/4020/4021/288/2032 692/699/1503/1607 7-Dehydrocholesterol reductase 82/1 82/58 82/80 Ablation Acetaminophen Animals Biosynthesis Cholesterol Cyclodextrins Electron paramagnetic resonance Electron spin Electron spin resonance Electrons Enzymes Ferroptosis Hepatocellular carcinoma Hepatocytes Humanities and Social Sciences Humans Injury prevention Ischemia Liver Liver cancer Liver Diseases Liver failure Metabolites Mice multidisciplinary Oxidation Oxidoreductases Acting on CH-CH Group Donors - metabolism Pathophysiology Reductases Regulatory mechanisms (biology) Reperfusion Science Science (multidisciplinary) Spin resonance Substrate inhibition trans-1,4-Bis(2-chlorobenzaminomethyl)cyclohexane Dihydrochloride β-Cyclodextrin
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Title	Inhibition of 7-dehydrocholesterol reductase prevents hepatic ferroptosis under an active state of sterol synthesis
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