Inhibition of Drp1 protects against senecionine-induced mitochondria-mediated apoptosis in primary hepatocytes and in mice

Redox Biology

Volumn 12, Issue , 2017, Pages 264-273

  Yang, Xiao ^a,b   Wang, Hua ^b   Ni, Hong Min ^b   Xiong, Aizhen ^a   Wang, Zhengtao ^a   Sesaki, Hiromi ^c   Ding, Wen Xing ^b   Yang, Li ^a  

^a SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Drp1; Liver injury; Mitochondria; Senecionine

Indexed keywords

ALANINE AMINOTRANSFERASE; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CASPASE 3; CASPASE INHIBITOR; CYTOCHROME C; DYNAMIN I; PYRROLIZIDINE ALKALOID; SENECIONINE; UNCLASSIFIED DRUG; ZVAD FMK; DNM1L PROTEIN, HUMAN; DNM1L PROTEIN, MOUSE; DYNAMIN; GUANOSINE TRIPHOSPHATASE; MICROTUBULE ASSOCIATED PROTEIN; MITOCHONDRIAL PROTEIN;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DAMAGE; CELL PROTECTION; CONTROLLED STUDY; DNA FRAGMENTATION; HUMAN; HUMAN CELL; HUMAN TISSUE; KNOCKOUT MOUSE; LIVER CELL; LIVER HEMORRHAGE; LIVER INJURY; LIVER TOXICITY; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOLECULAR MECHANICS; MOUSE; NONHUMAN; TUNEL ASSAY; WILD TYPE MOUSE; ANIMAL; BLOOD; CELL SURVIVAL; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; GENE KNOCKOUT; GENETICS; METABOLISM; MITOCHONDRION; TOXIC HEPATITIS;

ALANINE TRANSAMINASE; ANIMALS; CELL SURVIVAL; CHEMICAL AND DRUG INDUCED LIVER INJURY; DISEASE MODELS, ANIMAL; DYNAMINS; GENE KNOCKOUT TECHNIQUES; GTP PHOSPHOHYDROLASES; HEPATOCYTES; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PYRROLIZIDINE ALKALOIDS;

EID: 85014716151     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2017.02.020     Document Type: Article

References (39)

1. [1] Neuman, M.G., et al. Hepatotoxicity of Pyrrolizidine Alkaloids. J. Pharm. Pharm. Sci. 18:4 (2015), 825–843.
2. [2] Chojkier, M., Hepatic sinusoidal-obstruction syndrome: toxicity of pyrrolizidine alkaloids. J. Hepatol. 39:3 (2003), 437–446.
3. [3] Wang, J.Y., Gao, H., Tusanqi and hepatic sinusoidal obstruction syndrome. J. Dig. Dis. 15:3 (2014), 105–107.
4. [4] Stegelmeier, B.L., et al. Pyrrolizidine alkaloid plants, metabolism and toxicity. J. Nat. Toxins 8:1 (1999), 95–116.
5. [5] Lin, G., et al. Hepatic sinusoidal obstruction syndrome associated with consumption of Gynura segetum. J. Hepatol. 54:4 (2011), 666–673.
6. [6] DeLeve, L.D., et al. Toxicity of azathioprine and monocrotaline in murine sinusoidal endothelial cells and hepatocytes: the role of glutathione and relevance to hepatic venoocclusive disease. Hepatology 23:3 (1996), 589–599.
7. [7] Ji, L., et al. Involvement of Bcl-xL degradation and mitochondrial-mediated apoptotic pathway in pyrrolizidine alkaloids-induced apoptosis in hepatocytes. Toxicol. Appl Pharm. 231:3 (2008), 393–400.
8. [8] Fu, P.P., et al. Pyrrolizidine alkaloids–genotoxicity, metabolism enzymes, metabolic activation, and mechanisms. Drug Metab. Rev. 36:1 (2004), 1–55.
9. [9] Copple, B.L., et al. Modes of cell death in rat liver after monocrotaline exposure. Toxicol. Sci. 77:1 (2004), 172–182.
10. [10] Ji, L., et al. Protective mechanisms of N-acetyl-cysteine against pyrrolizidine alkaloid clivorine-induced hepatotoxicity. J. Cell Biochem 108:2 (2009), 424–432.
11. [11] Ni, H.M., Williams, J.A., Ding, W.X., Mitochondrial dynamics and mitochondrial quality control. Redox Biol. 4 (2015), 6–13.
12. [12] Pernas, L., Scorrano, L., Mito-morphosis: mitochondrial fusion, fission, and cristae remodeling as key mediators of cellular function. Annu. Rev. Physiol. 78 (2016), 505–531.
13. [13] Youle, R.J., van der Bliek, A.M., Mitochondrial fission, fusion, and stress. Science 337:6098 (2012), 1062–1065.
14. [14] Mishra, P., Chan, D.C., Mitochondrial dynamics and inheritance during cell division, development and disease. Nat. Rev. Mol. Cell Biol. 15:10 (2014), 634–646.
15. [15] Mishra, P., Chan, D.C., Metabolic regulation of mitochondrial dynamics. J. Cell Biol. 212:4 (2016), 379–387.
16. [16] Frank, S., et al. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell 1:4 (2001), 515–525.
17. [17] Cassidy-Stone, A., et al. Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization. Dev. Cell 14:2 (2008), 193–204.
18. [18] Naylor, K., et al. Mdv1 interacts with assembled dnm1 to promote mitochondrial division. J. Biol. Chem. 281:4 (2006), 2177–2183.
19. [19] He, Y.Q., et al. Identification of the UDP-glucuronosyltransferase isozyme involved in senecionine glucuronidation in human liver microsomes. Drug Metab. Dispos. 38:4 (2010), 626–634.
20. [20] Kageyama, Y., et al. Parkin-independent mitophagy requires Drp1 and maintains the integrity of mammalian heart and brain. EMBO J. 33:23 (2014), 2798–2813.
21. [21] Ni, H.M., et al. Activation of autophagy protects against acetaminophen-induced hepatotoxicity. Hepatology 55:1 (2012), 222–232.
22. [22] Ni, H.M., et al. Caspase inhibition prevents tumor necrosis factor-alpha-induced apoptosis and promotes necrotic cell death in mouse hepatocytes in vivo and in vitro. Am. J. Pathol. 186:10 (2016), 2623–2636.
23. [23] Ni, H.M., et al. Critical role of FoxO3a in alcohol-induced autophagy and hepatotoxicity. Am. J. Pathol. 183:6 (2013), 1815–1825.
24. [24] Dhanasekaran, D.N., Reddy, E.P., JNK signaling in apoptosis. Oncogene 27:48 (2008), 6245–6251.
25. [25] Park, S.W., et al. A selective inhibitor of drp1, mdivi-1, increases retinal ganglion cell survival in acute ischemic mouse retina. Invest. Ophthalmol. Vis. Sci. 52:5 (2011), 2837–2843.
26. [26] Zhang, N., et al. A selective inhibitor of Drp1, mdivi-1, acts against cerebral ischemia/reperfusion injury via an anti-apoptotic pathway in rats. Neurosci. Lett. 535 (2013), 104–109.
27. [27] Williams, J.A., et al. Parkin regulates mitophagy and mitochondrial function to protect against alcohol-induced liver injury and steatosis in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 309:5 (2015), G324–G340.
28. [28] Williams, J.A., et al. Chronic Deletion and Acute Knockdown of Parkin Have Differential Responses to Acetaminophen-induced Mitophagy and Liver Injury in Mice. J. Biol. Chem. 290:17 (2015), 10934–10946.
29. [29] Xiong, A., et al. Metabolomic and genomic evidence for compromised bile acid homeostasis by senecionine, a hepatotoxic pyrrolizidine alkaloid. Chem. Res. Toxicol. 27:5 (2014), 775–786.
30. [30] Fang, L., et al. Mass-spectrometry-directed analysis and purification of pyrrolizidine alkaloid cis/trans isomers in Gynura japonica. J. Sep. Sci. 37:15 (2014), 2032–2038.
31. [31] DeLeve, L.D., et al. Characterization of a reproducible rat model of hepatic veno-occlusive disease. Hepatology 29:6 (1999), 1779–1791.
32. [32] Nakamura, K., et al. Sorafenib attenuates monocrotaline-induced sinusoidal obstruction syndrome in rats through suppression of JNK and MMP-9. J. Hepatol. 57:5 (2012), 1037–1043.
33. [33] Taguchi, N., et al. Mitotic phosphorylation of dynamin-related GTPase Drp1 participates in mitochondrial fission. J. Biol. Chem. 282:15 (2007), 11521–11529.
34. [34] Xu, S., et al. CaMKII induces permeability transition through Drp1 phosphorylation during chronic beta-AR stimulation. Nat. Commun., 7, 2016, 13189.
35. [35] Czaja, M.J., et al. Functions of autophagy in normal and diseased liver. Autophagy 9:8 (2013), 1131–1158.
36. [36] Ding, W.X., Yin, X.M., Mitophagy: mechanisms, pathophysiological roles, and analysis. Biol. Chem. 393:7 (2012), 547–564.
37. [37] Oinonen, T., et al. Zonation of cytochrome P450 enzyme expression in rat liver. Isozyme-specific regulation by pituitary dependent hormones. Biochem. Pharm. 51:10 (1996), 1379–1387.
38. [38] Seki, E., Brenner, D.A., Karin, M., A liver full of JNK: signaling in regulation of cell function and disease pathogenesis, and clinical approaches. Gastroenterology 143:2 (2012), 307–320.
39. [39] Zorov, D.B., Juhaszova, M., Sollott, S.J., Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol. Rev. 94:3 (2014), 909–950.