Ferroptosis driven by radical oxidation of n-6 polyunsaturated fatty acids mediates acetaminophen-induced acute liver failure

Acetaminophen (APAP) overdose is a common cause of drug-induced acute liver failure. Although hepatocyte cell death is considered to be the critical event in APAP-induced hepatotoxicity, the underlying mechanism remains unclear. Ferroptosis is a newly discovered type of cell death that is caused by...

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Vydané v:	Cell death & disease Ročník 11; číslo 2; s. 144 - 16
Hlavní autori:	Yamada, Naoya, Karasawa, Tadayoshi, Kimura, Hiroaki, Watanabe, Sachiko, Komada, Takanori, Kamata, Ryo, Sampilvanjil, Ariunaa, Ito, Junya, Nakagawa, Kiyotaka, Kuwata, Hiroshi, Hara, Shuntaro, Mizuta, Koichi, Sakuma, Yasunaru, Sata, Naohiro, Takahashi, Masafumi
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	London Nature Publishing Group UK 24.02.2020 Springer Nature B.V Nature Publishing Group
Predmet:	13 13/51 38 42 631/443 692/699/1503/1607/2749 82 82/58 Acetaminophen alpha-Tocopherol - pharmacology Analgesics Animal models Animals Antibodies Antioxidants - pharmacology Apoptosis Arachidonic acid Biochemistry Biomedical and Life Sciences Cell Biology Cell Culture Cell death Coenzyme A Ligases - genetics Coenzyme A Ligases - metabolism Cyclohexylamines - pharmacology Cyclooxygenase 2 - genetics Cyclooxygenase 2 - metabolism Deferoxamine Deferoxamine - pharmacology Disease Models, Animal Drug overdose Fatty acids Fatty Acids, Omega-6 - metabolism Ferroptosis Ferroptosis - drug effects Glutathione Hepatocytes Hepatocytes - drug effects Hepatocytes - metabolism Hepatocytes - pathology Hepatotoxicity Homeostasis Humans Immunology Iron Chelating Agents - pharmacology Life Sciences Lipid peroxidation Lipid Peroxidation - drug effects Lipids Liver Liver - drug effects Liver - metabolism Liver - pathology Liver failure Liver Failure, Acute - chemically induced Liver Failure, Acute - metabolism Liver Failure, Acute - pathology Liver Failure, Acute - prevention & control Mass spectroscopy Mice, Inbred C57BL Mice, Knockout mRNA Overdose Oxidation Oxidation-Reduction Phenylenediamines - pharmacology Polyunsaturated fatty acids Supplements Therapeutic applications Vitamin E
ISSN:	2041-4889, 2041-4889
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Abstract	Acetaminophen (APAP) overdose is a common cause of drug-induced acute liver failure. Although hepatocyte cell death is considered to be the critical event in APAP-induced hepatotoxicity, the underlying mechanism remains unclear. Ferroptosis is a newly discovered type of cell death that is caused by a loss of cellular redox homeostasis. As glutathione (GSH) depletion triggers APAP-induced hepatotoxicity, we investigated the role of ferroptosis in a murine model of APAP-induced acute liver failure. APAP-induced hepatotoxicity (evaluated in terms of ALT, AST, and the histopathological score), lipid peroxidation (4-HNE and MDA), and upregulation of the ferroptosis maker PTGS2 mRNA were markedly prevented by the ferroptosis-specific inhibitor ferrostatin-1 (Fer-1). Fer-1 treatment also completely prevented mortality induced by high-dose APAP. Similarly, APAP-induced hepatotoxicity and lipid peroxidation were prevented by the iron chelator deferoxamine. Using mass spectrometry, we found that lipid peroxides derived from n-6 fatty acids, mainly arachidonic acid, were elevated by APAP, and that auto-oxidation is the predominant mechanism of APAP-derived lipid oxidation. APAP-induced hepatotoxicity was also prevented by genetic inhibition of acyl-CoA synthetase long-chain family member 4 or α-tocopherol supplementation. We found that ferroptosis is responsible for APAP-induced hepatocyte cell death. Our findings provide new insights into the mechanism of APAP-induced hepatotoxicity and suggest that ferroptosis is a potential therapeutic target for APAP-induced acute liver failure.
AbstractList	Acetaminophen (APAP) overdose is a common cause of drug-induced acute liver failure. Although hepatocyte cell death is considered to be the critical event in APAP-induced hepatotoxicity, the underlying mechanism remains unclear. Ferroptosis is a newly discovered type of cell death that is caused by a loss of cellular redox homeostasis. As glutathione (GSH) depletion triggers APAP-induced hepatotoxicity, we investigated the role of ferroptosis in a murine model of APAP-induced acute liver failure. APAP-induced hepatotoxicity (evaluated in terms of ALT, AST, and the histopathological score), lipid peroxidation (4-HNE and MDA), and upregulation of the ferroptosis maker PTGS2 mRNA were markedly prevented by the ferroptosis-specific inhibitor ferrostatin-1 (Fer-1). Fer-1 treatment also completely prevented mortality induced by high-dose APAP. Similarly, APAP-induced hepatotoxicity and lipid peroxidation were prevented by the iron chelator deferoxamine. Using mass spectrometry, we found that lipid peroxides derived from n-6 fatty acids, mainly arachidonic acid, were elevated by APAP, and that auto-oxidation is the predominant mechanism of APAP-derived lipid oxidation. APAP-induced hepatotoxicity was also prevented by genetic inhibition of acyl-CoA synthetase long-chain family member 4 or α-tocopherol supplementation. We found that ferroptosis is responsible for APAP-induced hepatocyte cell death. Our findings provide new insights into the mechanism of APAP-induced hepatotoxicity and suggest that ferroptosis is a potential therapeutic target for APAP-induced acute liver failure.Acetaminophen (APAP) overdose is a common cause of drug-induced acute liver failure. Although hepatocyte cell death is considered to be the critical event in APAP-induced hepatotoxicity, the underlying mechanism remains unclear. Ferroptosis is a newly discovered type of cell death that is caused by a loss of cellular redox homeostasis. As glutathione (GSH) depletion triggers APAP-induced hepatotoxicity, we investigated the role of ferroptosis in a murine model of APAP-induced acute liver failure. APAP-induced hepatotoxicity (evaluated in terms of ALT, AST, and the histopathological score), lipid peroxidation (4-HNE and MDA), and upregulation of the ferroptosis maker PTGS2 mRNA were markedly prevented by the ferroptosis-specific inhibitor ferrostatin-1 (Fer-1). Fer-1 treatment also completely prevented mortality induced by high-dose APAP. Similarly, APAP-induced hepatotoxicity and lipid peroxidation were prevented by the iron chelator deferoxamine. Using mass spectrometry, we found that lipid peroxides derived from n-6 fatty acids, mainly arachidonic acid, were elevated by APAP, and that auto-oxidation is the predominant mechanism of APAP-derived lipid oxidation. APAP-induced hepatotoxicity was also prevented by genetic inhibition of acyl-CoA synthetase long-chain family member 4 or α-tocopherol supplementation. We found that ferroptosis is responsible for APAP-induced hepatocyte cell death. Our findings provide new insights into the mechanism of APAP-induced hepatotoxicity and suggest that ferroptosis is a potential therapeutic target for APAP-induced acute liver failure. Acetaminophen (APAP) overdose is a common cause of drug-induced acute liver failure. Although hepatocyte cell death is considered to be the critical event in APAP-induced hepatotoxicity, the underlying mechanism remains unclear. Ferroptosis is a newly discovered type of cell death that is caused by a loss of cellular redox homeostasis. As glutathione (GSH) depletion triggers APAP-induced hepatotoxicity, we investigated the role of ferroptosis in a murine model of APAP-induced acute liver failure. APAP-induced hepatotoxicity (evaluated in terms of ALT, AST, and the histopathological score), lipid peroxidation (4-HNE and MDA), and upregulation of the ferroptosis maker PTGS2 mRNA were markedly prevented by the ferroptosis-specific inhibitor ferrostatin-1 (Fer-1). Fer-1 treatment also completely prevented mortality induced by high-dose APAP. Similarly, APAP-induced hepatotoxicity and lipid peroxidation were prevented by the iron chelator deferoxamine. Using mass spectrometry, we found that lipid peroxides derived from n-6 fatty acids, mainly arachidonic acid, were elevated by APAP, and that auto-oxidation is the predominant mechanism of APAP-derived lipid oxidation. APAP-induced hepatotoxicity was also prevented by genetic inhibition of acyl-CoA synthetase long-chain family member 4 or α-tocopherol supplementation. We found that ferroptosis is responsible for APAP-induced hepatocyte cell death. Our findings provide new insights into the mechanism of APAP-induced hepatotoxicity and suggest that ferroptosis is a potential therapeutic target for APAP-induced acute liver failure. Abstract Acetaminophen (APAP) overdose is a common cause of drug-induced acute liver failure. Although hepatocyte cell death is considered to be the critical event in APAP-induced hepatotoxicity, the underlying mechanism remains unclear. Ferroptosis is a newly discovered type of cell death that is caused by a loss of cellular redox homeostasis. As glutathione (GSH) depletion triggers APAP-induced hepatotoxicity, we investigated the role of ferroptosis in a murine model of APAP-induced acute liver failure. APAP-induced hepatotoxicity (evaluated in terms of ALT, AST, and the histopathological score), lipid peroxidation (4-HNE and MDA), and upregulation of the ferroptosis maker PTGS2 mRNA were markedly prevented by the ferroptosis-specific inhibitor ferrostatin-1 (Fer-1). Fer-1 treatment also completely prevented mortality induced by high-dose APAP. Similarly, APAP-induced hepatotoxicity and lipid peroxidation were prevented by the iron chelator deferoxamine. Using mass spectrometry, we found that lipid peroxides derived from n-6 fatty acids, mainly arachidonic acid, were elevated by APAP, and that auto-oxidation is the predominant mechanism of APAP-derived lipid oxidation. APAP-induced hepatotoxicity was also prevented by genetic inhibition of acyl-CoA synthetase long-chain family member 4 or α-tocopherol supplementation. We found that ferroptosis is responsible for APAP-induced hepatocyte cell death. Our findings provide new insights into the mechanism of APAP-induced hepatotoxicity and suggest that ferroptosis is a potential therapeutic target for APAP-induced acute liver failure.
ArticleNumber	144
Author	Karasawa, Tadayoshi Sakuma, Yasunaru Kamata, Ryo Kuwata, Hiroshi Takahashi, Masafumi Komada, Takanori Sata, Naohiro Sampilvanjil, Ariunaa Mizuta, Koichi Kimura, Hiroaki Nakagawa, Kiyotaka Yamada, Naoya Watanabe, Sachiko Ito, Junya Hara, Shuntaro
Author_xml	– sequence: 1 givenname: Naoya surname: Yamada fullname: Yamada, Naoya 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 – sequence: 2 givenname: Tadayoshi surname: Karasawa fullname: Karasawa, Tadayoshi organization: Division of Inflammation Research, Center for Molecular Medicine, Jichi Medical University – sequence: 3 givenname: Hiroaki orcidid: 0000-0002-7441-0382 surname: Kimura fullname: Kimura, Hiroaki organization: Division of Inflammation Research, Center for Molecular Medicine, Jichi Medical University – sequence: 4 givenname: Sachiko surname: Watanabe fullname: Watanabe, Sachiko organization: Division of Inflammation Research, Center for Molecular Medicine, Jichi Medical University – sequence: 5 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: 6 givenname: Ryo surname: Kamata fullname: Kamata, Ryo organization: Division of Inflammation Research, Center for Molecular Medicine, Jichi Medical University – sequence: 7 givenname: Ariunaa surname: Sampilvanjil fullname: Sampilvanjil, Ariunaa organization: Division of Inflammation Research, Center for Molecular Medicine, Jichi Medical University – sequence: 8 givenname: Junya surname: Ito fullname: Ito, Junya organization: Food and Biodynamic Chemistry Laboratory, Graduate School of Agricultural Science, Tohoku University – sequence: 9 givenname: Kiyotaka surname: Nakagawa fullname: Nakagawa, Kiyotaka organization: Food and Biodynamic Chemistry Laboratory, Graduate School of Agricultural Science, Tohoku University – sequence: 10 givenname: Hiroshi surname: Kuwata fullname: Kuwata, Hiroshi organization: Division of Health Chemistry, Department of Healthcare and Regulatory Sciences, School of Pharmacy, Showa University – sequence: 11 givenname: Shuntaro surname: Hara fullname: Hara, Shuntaro organization: Division of Health Chemistry, Department of Healthcare and Regulatory Sciences, School of Pharmacy, Showa University – sequence: 12 givenname: Koichi surname: Mizuta fullname: Mizuta, Koichi organization: Department of Transplant Surgery, Saitama Children’s Medical Center – sequence: 13 givenname: Yasunaru surname: Sakuma fullname: Sakuma, Yasunaru organization: Division of Gastroenterological, General and Transplant Surgery, Department of Surgery, Jichi Medical University – sequence: 14 givenname: Naohiro surname: Sata fullname: Sata, Naohiro organization: Division of Gastroenterological, General and Transplant Surgery, Department of Surgery, Jichi Medical University – sequence: 15 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/32094346$$D View this record in MEDLINE/PubMed
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Snippet	Acetaminophen (APAP) overdose is a common cause of drug-induced acute liver failure. Although hepatocyte cell death is considered to be the critical event in... Abstract Acetaminophen (APAP) overdose is a common cause of drug-induced acute liver failure. Although hepatocyte cell death is considered to be the critical...
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SubjectTerms	13 13/51 38 42 631/443 692/699/1503/1607/2749 82 82/58 Acetaminophen alpha-Tocopherol - pharmacology Analgesics Animal models Animals Antibodies Antioxidants - pharmacology Apoptosis Arachidonic acid Biochemistry Biomedical and Life Sciences Cell Biology Cell Culture Cell death Coenzyme A Ligases - genetics Coenzyme A Ligases - metabolism Cyclohexylamines - pharmacology Cyclooxygenase 2 - genetics Cyclooxygenase 2 - metabolism Deferoxamine Deferoxamine - pharmacology Disease Models, Animal Drug overdose Fatty acids Fatty Acids, Omega-6 - metabolism Ferroptosis Ferroptosis - drug effects Glutathione Hepatocytes Hepatocytes - drug effects Hepatocytes - metabolism Hepatocytes - pathology Hepatotoxicity Homeostasis Humans Immunology Iron Chelating Agents - pharmacology Life Sciences Lipid peroxidation Lipid Peroxidation - drug effects Lipids Liver Liver - drug effects Liver - metabolism Liver - pathology Liver failure Liver Failure, Acute - chemically induced Liver Failure, Acute - metabolism Liver Failure, Acute - pathology Liver Failure, Acute - prevention & control Mass spectroscopy Mice, Inbred C57BL Mice, Knockout mRNA Overdose Oxidation Oxidation-Reduction Phenylenediamines - pharmacology Polyunsaturated fatty acids Supplements Therapeutic applications Vitamin E
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Title	Ferroptosis driven by radical oxidation of n-6 polyunsaturated fatty acids mediates acetaminophen-induced acute liver failure
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