Endogenous Drp1 mediates mitochondrial autophagy and protects the heart against energy stress
Both fusion and fission contribute to mitochondrial quality control. How unopposed fusion affects survival of cardiomyocytes and left ventricular function in the heart is poorly understood. We investigated the role of dynamin-related protein 1 (Drp1), a GTPase that mediates mitochondrial fission, in...
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| Vydané v: | Circulation research Ročník 116; číslo 2; s. 264 |
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| Hlavní autori: | , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
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United States
16.01.2015
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| ISSN: | 1524-4571, 1524-4571 |
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| Abstract | Both fusion and fission contribute to mitochondrial quality control. How unopposed fusion affects survival of cardiomyocytes and left ventricular function in the heart is poorly understood.
We investigated the role of dynamin-related protein 1 (Drp1), a GTPase that mediates mitochondrial fission, in mediating mitochondrial autophagy, ventricular function, and stress resistance in the heart.
Drp1 downregulation induced mitochondrial elongation, accumulation of damaged mitochondria, and increased apoptosis in cardiomyocytes at baseline. Drp1 downregulation also suppressed autophagosome formation and autophagic flux at baseline and in response to glucose deprivation in cardiomyocytes. The lack of lysosomal translocation of mitochondrially targeted Keima indicates that Drp1 downregulation suppressed mitochondrial autophagy. Mitochondrial elongation and accumulation of damaged mitochondria were also observed in tamoxifen-inducible cardiac-specific Drp1 knockout mice. After Drp1 downregulation, cardiac-specific Drp1 knockout mice developed left ventricular dysfunction, preceded by mitochondrial dysfunction, and died within 13 weeks. Autophagic flux is significantly suppressed in cardiac-specific Drp1 knockout mice. Although left ventricular function in cardiac-specific Drp1 heterozygous knockout mice was normal at 12 weeks of age, left ventricular function decreased more severely after 48 hours of fasting, and the infarct size/area at risk after ischemia/reperfusion was significantly greater in cardiac-specific Drp1 heterozygous knockout than in control mice.
Disruption of Drp1 induces mitochondrial elongation, inhibits mitochondrial autophagy, and causes mitochondrial dysfunction, thereby promoting cardiac dysfunction and increased susceptibility to ischemia/reperfusion. |
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| AbstractList | Both fusion and fission contribute to mitochondrial quality control. How unopposed fusion affects survival of cardiomyocytes and left ventricular function in the heart is poorly understood.
We investigated the role of dynamin-related protein 1 (Drp1), a GTPase that mediates mitochondrial fission, in mediating mitochondrial autophagy, ventricular function, and stress resistance in the heart.
Drp1 downregulation induced mitochondrial elongation, accumulation of damaged mitochondria, and increased apoptosis in cardiomyocytes at baseline. Drp1 downregulation also suppressed autophagosome formation and autophagic flux at baseline and in response to glucose deprivation in cardiomyocytes. The lack of lysosomal translocation of mitochondrially targeted Keima indicates that Drp1 downregulation suppressed mitochondrial autophagy. Mitochondrial elongation and accumulation of damaged mitochondria were also observed in tamoxifen-inducible cardiac-specific Drp1 knockout mice. After Drp1 downregulation, cardiac-specific Drp1 knockout mice developed left ventricular dysfunction, preceded by mitochondrial dysfunction, and died within 13 weeks. Autophagic flux is significantly suppressed in cardiac-specific Drp1 knockout mice. Although left ventricular function in cardiac-specific Drp1 heterozygous knockout mice was normal at 12 weeks of age, left ventricular function decreased more severely after 48 hours of fasting, and the infarct size/area at risk after ischemia/reperfusion was significantly greater in cardiac-specific Drp1 heterozygous knockout than in control mice.
Disruption of Drp1 induces mitochondrial elongation, inhibits mitochondrial autophagy, and causes mitochondrial dysfunction, thereby promoting cardiac dysfunction and increased susceptibility to ischemia/reperfusion. Both fusion and fission contribute to mitochondrial quality control. How unopposed fusion affects survival of cardiomyocytes and left ventricular function in the heart is poorly understood.RATIONALEBoth fusion and fission contribute to mitochondrial quality control. How unopposed fusion affects survival of cardiomyocytes and left ventricular function in the heart is poorly understood.We investigated the role of dynamin-related protein 1 (Drp1), a GTPase that mediates mitochondrial fission, in mediating mitochondrial autophagy, ventricular function, and stress resistance in the heart.OBJECTIVEWe investigated the role of dynamin-related protein 1 (Drp1), a GTPase that mediates mitochondrial fission, in mediating mitochondrial autophagy, ventricular function, and stress resistance in the heart.Drp1 downregulation induced mitochondrial elongation, accumulation of damaged mitochondria, and increased apoptosis in cardiomyocytes at baseline. Drp1 downregulation also suppressed autophagosome formation and autophagic flux at baseline and in response to glucose deprivation in cardiomyocytes. The lack of lysosomal translocation of mitochondrially targeted Keima indicates that Drp1 downregulation suppressed mitochondrial autophagy. Mitochondrial elongation and accumulation of damaged mitochondria were also observed in tamoxifen-inducible cardiac-specific Drp1 knockout mice. After Drp1 downregulation, cardiac-specific Drp1 knockout mice developed left ventricular dysfunction, preceded by mitochondrial dysfunction, and died within 13 weeks. Autophagic flux is significantly suppressed in cardiac-specific Drp1 knockout mice. Although left ventricular function in cardiac-specific Drp1 heterozygous knockout mice was normal at 12 weeks of age, left ventricular function decreased more severely after 48 hours of fasting, and the infarct size/area at risk after ischemia/reperfusion was significantly greater in cardiac-specific Drp1 heterozygous knockout than in control mice.METHODS AND RESULTSDrp1 downregulation induced mitochondrial elongation, accumulation of damaged mitochondria, and increased apoptosis in cardiomyocytes at baseline. Drp1 downregulation also suppressed autophagosome formation and autophagic flux at baseline and in response to glucose deprivation in cardiomyocytes. The lack of lysosomal translocation of mitochondrially targeted Keima indicates that Drp1 downregulation suppressed mitochondrial autophagy. Mitochondrial elongation and accumulation of damaged mitochondria were also observed in tamoxifen-inducible cardiac-specific Drp1 knockout mice. After Drp1 downregulation, cardiac-specific Drp1 knockout mice developed left ventricular dysfunction, preceded by mitochondrial dysfunction, and died within 13 weeks. Autophagic flux is significantly suppressed in cardiac-specific Drp1 knockout mice. Although left ventricular function in cardiac-specific Drp1 heterozygous knockout mice was normal at 12 weeks of age, left ventricular function decreased more severely after 48 hours of fasting, and the infarct size/area at risk after ischemia/reperfusion was significantly greater in cardiac-specific Drp1 heterozygous knockout than in control mice.Disruption of Drp1 induces mitochondrial elongation, inhibits mitochondrial autophagy, and causes mitochondrial dysfunction, thereby promoting cardiac dysfunction and increased susceptibility to ischemia/reperfusion.CONCLUSIONSDisruption of Drp1 induces mitochondrial elongation, inhibits mitochondrial autophagy, and causes mitochondrial dysfunction, thereby promoting cardiac dysfunction and increased susceptibility to ischemia/reperfusion. |
| Author | Abdellatif, Maha Egashira, Kensuke Mihara, Katsuyoshi Ohishi, Mitsuru Sciarretta, Sebastiano Toli, Jessica Shirakabe, Akihiro Nomura, Masatoshi Sadoshima, Junichi Maejima, Yasuhiro Zhai, Peiyong Ikeda, Yoshiyuki |
| Author_xml | – sequence: 1 givenname: Yoshiyuki surname: Ikeda fullname: Ikeda, Yoshiyuki organization: From the Department of Cell Biology and Molecular Medicine, Cardiovascular Research Institute, Rutgers New Jersey Medical School, Newark (Y.I., A.S., Y.M., P.Z., S.S., J.T., M.A., J.S.); IRCCS Neuromed, Pozzilli, Italy (S.S.); Department of Medicine and Bioregulatory Science (M.N.), Department of Molecular Biology (K.M.), Department of Cardiovascular Medicine, Department of Cardiovascular Research, Development, and Translational Medicine (K.E.), Graduate School of Medical Science, Kyushu University Hospital, Fukuoka, Japan; and Department of Cardiovascular Medicine and Hypertension, Graduate School of Medical and Dental Science, Kagoshima University, Kagoshima, Japan (M.O.) – sequence: 2 givenname: Akihiro surname: Shirakabe fullname: Shirakabe, Akihiro organization: From the Department of Cell Biology and Molecular Medicine, Cardiovascular Research Institute, Rutgers New Jersey Medical School, Newark (Y.I., A.S., Y.M., P.Z., S.S., J.T., M.A., J.S.); IRCCS Neuromed, Pozzilli, Italy (S.S.); Department of Medicine and Bioregulatory Science (M.N.), Department of Molecular Biology (K.M.), Department of Cardiovascular Medicine, Department of Cardiovascular Research, Development, and Translational Medicine (K.E.), Graduate School of Medical Science, Kyushu University Hospital, Fukuoka, Japan; and Department of Cardiovascular Medicine and Hypertension, Graduate School of Medical and Dental Science, Kagoshima University, Kagoshima, Japan (M.O.) – sequence: 3 givenname: Yasuhiro surname: Maejima fullname: Maejima, Yasuhiro organization: From the Department of Cell Biology and Molecular Medicine, Cardiovascular Research Institute, Rutgers New Jersey Medical School, Newark (Y.I., A.S., Y.M., P.Z., S.S., J.T., M.A., J.S.); IRCCS Neuromed, Pozzilli, Italy (S.S.); Department of Medicine and Bioregulatory Science (M.N.), Department of Molecular Biology (K.M.), Department of Cardiovascular Medicine, Department of Cardiovascular Research, Development, and Translational Medicine (K.E.), Graduate School of Medical Science, Kyushu University Hospital, Fukuoka, Japan; and Department of Cardiovascular Medicine and Hypertension, Graduate School of Medical and Dental Science, Kagoshima University, Kagoshima, Japan (M.O.) – sequence: 4 givenname: Peiyong surname: Zhai fullname: Zhai, Peiyong organization: From the Department of Cell Biology and Molecular Medicine, Cardiovascular Research Institute, Rutgers New Jersey Medical School, Newark (Y.I., A.S., Y.M., P.Z., S.S., J.T., M.A., J.S.); IRCCS Neuromed, Pozzilli, Italy (S.S.); Department of Medicine and Bioregulatory Science (M.N.), Department of Molecular Biology (K.M.), Department of Cardiovascular Medicine, Department of Cardiovascular Research, Development, and Translational Medicine (K.E.), Graduate School of Medical Science, Kyushu University Hospital, Fukuoka, Japan; and Department of Cardiovascular Medicine and Hypertension, Graduate School of Medical and Dental Science, Kagoshima University, Kagoshima, Japan (M.O.) – sequence: 5 givenname: Sebastiano surname: Sciarretta fullname: Sciarretta, Sebastiano organization: From the Department of Cell Biology and Molecular Medicine, Cardiovascular Research Institute, Rutgers New Jersey Medical School, Newark (Y.I., A.S., Y.M., P.Z., S.S., J.T., M.A., J.S.); IRCCS Neuromed, Pozzilli, Italy (S.S.); Department of Medicine and Bioregulatory Science (M.N.), Department of Molecular Biology (K.M.), Department of Cardiovascular Medicine, Department of Cardiovascular Research, Development, and Translational Medicine (K.E.), Graduate School of Medical Science, Kyushu University Hospital, Fukuoka, Japan; and Department of Cardiovascular Medicine and Hypertension, Graduate School of Medical and Dental Science, Kagoshima University, Kagoshima, Japan (M.O.) – sequence: 6 givenname: Jessica surname: Toli fullname: Toli, Jessica organization: From the Department of Cell Biology and Molecular Medicine, Cardiovascular Research Institute, Rutgers New Jersey Medical School, Newark (Y.I., A.S., Y.M., P.Z., S.S., J.T., M.A., J.S.); IRCCS Neuromed, Pozzilli, Italy (S.S.); Department of Medicine and Bioregulatory Science (M.N.), Department of Molecular Biology (K.M.), Department of Cardiovascular Medicine, Department of Cardiovascular Research, Development, and Translational Medicine (K.E.), Graduate School of Medical Science, Kyushu University Hospital, Fukuoka, Japan; and Department of Cardiovascular Medicine and Hypertension, Graduate School of Medical and Dental Science, Kagoshima University, Kagoshima, Japan (M.O.) – sequence: 7 givenname: Masatoshi surname: Nomura fullname: Nomura, Masatoshi organization: From the Department of Cell Biology and Molecular Medicine, Cardiovascular Research Institute, Rutgers New Jersey Medical School, Newark (Y.I., A.S., Y.M., P.Z., S.S., J.T., M.A., J.S.); IRCCS Neuromed, Pozzilli, Italy (S.S.); Department of Medicine and Bioregulatory Science (M.N.), Department of Molecular Biology (K.M.), Department of Cardiovascular Medicine, Department of Cardiovascular Research, Development, and Translational Medicine (K.E.), Graduate School of Medical Science, Kyushu University Hospital, Fukuoka, Japan; and Department of Cardiovascular Medicine and Hypertension, Graduate School of Medical and Dental Science, Kagoshima University, Kagoshima, Japan (M.O.) – sequence: 8 givenname: Katsuyoshi surname: Mihara fullname: Mihara, Katsuyoshi organization: From the Department of Cell Biology and Molecular Medicine, Cardiovascular Research Institute, Rutgers New Jersey Medical School, Newark (Y.I., A.S., Y.M., P.Z., S.S., J.T., M.A., J.S.); IRCCS Neuromed, Pozzilli, Italy (S.S.); Department of Medicine and Bioregulatory Science (M.N.), Department of Molecular Biology (K.M.), Department of Cardiovascular Medicine, Department of Cardiovascular Research, Development, and Translational Medicine (K.E.), Graduate School of Medical Science, Kyushu University Hospital, Fukuoka, Japan; and Department of Cardiovascular Medicine and Hypertension, Graduate School of Medical and Dental Science, Kagoshima University, Kagoshima, Japan (M.O.) – sequence: 9 givenname: Kensuke surname: Egashira fullname: Egashira, Kensuke organization: From the Department of Cell Biology and Molecular Medicine, Cardiovascular Research Institute, Rutgers New Jersey Medical School, Newark (Y.I., A.S., Y.M., P.Z., S.S., J.T., M.A., J.S.); IRCCS Neuromed, Pozzilli, Italy (S.S.); Department of Medicine and Bioregulatory Science (M.N.), Department of Molecular Biology (K.M.), Department of Cardiovascular Medicine, Department of Cardiovascular Research, Development, and Translational Medicine (K.E.), Graduate School of Medical Science, Kyushu University Hospital, Fukuoka, Japan; and Department of Cardiovascular Medicine and Hypertension, Graduate School of Medical and Dental Science, Kagoshima University, Kagoshima, Japan (M.O.) – sequence: 10 givenname: Mitsuru surname: Ohishi fullname: Ohishi, Mitsuru organization: From the Department of Cell Biology and Molecular Medicine, Cardiovascular Research Institute, Rutgers New Jersey Medical School, Newark (Y.I., A.S., Y.M., P.Z., S.S., J.T., M.A., J.S.); IRCCS Neuromed, Pozzilli, Italy (S.S.); Department of Medicine and Bioregulatory Science (M.N.), Department of Molecular Biology (K.M.), Department of Cardiovascular Medicine, Department of Cardiovascular Research, Development, and Translational Medicine (K.E.), Graduate School of Medical Science, Kyushu University Hospital, Fukuoka, Japan; and Department of Cardiovascular Medicine and Hypertension, Graduate School of Medical and Dental Science, Kagoshima University, Kagoshima, Japan (M.O.) – sequence: 11 givenname: Maha surname: Abdellatif fullname: Abdellatif, Maha organization: From the Department of Cell Biology and Molecular Medicine, Cardiovascular Research Institute, Rutgers New Jersey Medical School, Newark (Y.I., A.S., Y.M., P.Z., S.S., J.T., M.A., J.S.); IRCCS Neuromed, Pozzilli, Italy (S.S.); Department of Medicine and Bioregulatory Science (M.N.), Department of Molecular Biology (K.M.), Department of Cardiovascular Medicine, Department of Cardiovascular Research, Development, and Translational Medicine (K.E.), Graduate School of Medical Science, Kyushu University Hospital, Fukuoka, Japan; and Department of Cardiovascular Medicine and Hypertension, Graduate School of Medical and Dental Science, Kagoshima University, Kagoshima, Japan (M.O.) – sequence: 12 givenname: Junichi surname: Sadoshima fullname: Sadoshima, Junichi email: sadoshju@njms.rutgers.edu organization: From the Department of Cell Biology and Molecular Medicine, Cardiovascular Research Institute, Rutgers New Jersey Medical School, Newark (Y.I., A.S., Y.M., P.Z., S.S., J.T., M.A., J.S.); IRCCS Neuromed, Pozzilli, Italy (S.S.); Department of Medicine and Bioregulatory Science (M.N.), Department of Molecular Biology (K.M.), Department of Cardiovascular Medicine, Department of Cardiovascular Research, Development, and Translational Medicine (K.E.), Graduate School of Medical Science, Kyushu University Hospital, Fukuoka, Japan; and Department of Cardiovascular Medicine and Hypertension, Graduate School of Medical and Dental Science, Kagoshima University, Kagoshima, Japan (M.O.). sadoshju@njms.rutgers.edu |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25332205$$D View this record in MEDLINE/PubMed |
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