Rapid generation of mitochondrial superoxide induces mitochondrion-dependent but caspase-independent cell death in hippocampal neuronal cells that morphologically resembles necroptosis

Toxicology and Applied Pharmacology

Volumn 262, Issue 2, 2012, Pages 156-166

  Fukui, Masayuki ^a   Choi, Hye Joung ^a   Zhu, Bao Ting ^a  

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

Author keywords

Apoptosis inducing factor; ATP independent neuronal death; Caspase independent neuronal death; Endonuclease G; Mitochondrial damage induced cell death; Necrosis; Reactive oxygen species; Superoxide dismutase

Indexed keywords

ADENOSINE TRIPHOSPHATE; APOPTOSIS INDUCING FACTOR; CASPASE; ENDONUCLEASE G; MENADIONE; MITOGEN ACTIVATED PROTEIN KINASE; NUCLEASE; SMALL INTERFERING RNA; SUPEROXIDE; SUPEROXIDE DISMUTASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CULTURE; CELL IMMORTALIZATION; CELL STRAIN; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME RELEASE; GENE SILENCING; HIPPOCAMPUS; MITOCHONDRION; MITOCHONDRION SWELLING; MOUSE; NECROPTOSIS; NERVE CELL NECROSIS; NONHUMAN; OXIDATIVE STRESS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN SECRETION; REACTION TIME; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS INDUCING FACTOR; CELL DEATH; CELL LINE; ENDODEOXYRIBONUCLEASES; HIPPOCAMPUS; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; NEURODEGENERATIVE DISEASES; NEURONS; OXIDATIVE STRESS; SUPEROXIDE DISMUTASE; SUPEROXIDES; VITAMIN K 3;

EID: 84862267920     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2012.04.030     Document Type: Article

References (42)

1. Akiyoshi T., Matzno S., Sakai M., Okamura N., Matsuyama K. The potential of vitamin K3 as an anticancer agent against breast cancer that acts via the mitochondria-related apoptotic pathway. Cancer Chemother. Pharmacol. 2009, 65:143-150.
2. Banerjee R., Beal M.F., Thomas B. Autophagy in neurodegenerative disorders: pathogenic roles and therapeutic implications. Trends Neurosci. 2010, 33:541-549.
3. Behl C., Skutella T., Lezoualc'h F., Post A., Widmann M., Newton C.J., Holsboer F. Neuroprotection against oxidative stress by estrogens: structure-activity relationship. Mol. Pharmacol. 1997, 51:535-541.
4. Chance B., Sies H., Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 1979, 59:527-605.
5. Christofferson D.E., Yuan J. Necroptosis as an alternative form of programmed cell death. Curr. Opin. Cell Biol. 2010, 22:263-268.
6. Basic Neurochemistry: Molecular, Cellular and Medical Aspects 1999, 637-670. Lippincott, Philadelphia. D.D. Clark, L. Sokoloff, G.J. Siegel, B.W. Agranoff, R.W. Albers, S.K. Fisher, M.D. Uhler (Eds.).
7. 2 regulates the angiogenic phenotype via PTEN oxidation. J. Biol. Chem. 2005, 280:16916-16924.
8. Coyle J.T., Puttfarcken P. Oxidative stress, glutamate, and neurodegenerative disorders. Science 1993, 262:689-695.
9. Criddle D.N., Gillies S., Baumgartner-Wilson H.K., Jaffar M., Chinje E.C., Passmore S., Chvanov M., Barrow S., Gerasimenko O.V., Tepikin A.V., Sutton R., Petersen O.H. Menadione-induced reactive oxygen species generation via redox cycling promotes apoptosis of murine pancreatic acinar cells. J. Biol. Chem. 2006, 281:40485-40492.
10. 2 removal in brain mitochondria via the thioredoxin/peroxiredoxin system. J. Biol. Chem. 2010, 285:27850-27858.
11. Festjens N., Vanden Berghe T., Vandenabeele P. Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response. Biochim. Biophys. Acta 2006, 1757:1371-1387.
12. Fukui M., Zhu B.T. Mitochondrial superoxide dismutase SOD2, but not Cytosolic SOD1, plays a critical role in protection against glutamate-induced oxidative stress and cell death in HT22 neuronal cells. Free Radic. Biol. Med. 2010, 48:821-830.
13. Fukui M., Song J.H., Choi J.Y., Choi H.J., Zhu B.T. Mechanism of glutamate-induced neurotoxicity in culture HT22 cells. Eur. J. Pharmacol. 2009, 617:1-11.
14. Gerasimenko J.V., Gerasimenko O.V., Palejwala A., Tepikin A.V., Petersen O.H., Watson A.J. Menadione-induced apoptosis: roles of cytosolic Ca(2+) elevations and the mitochondrial permeability transition pore. J. Cell Sci. 2002, 115:485-497.
15. Golstein P., Kroemer G. Cell death by necrosis: towards a molecular definition. Trends Biochem. Sci. 2007, 32:37-43.
16. Halliwell B. Reactive oxygen species and the central nervous system. J. Neurochem. 1992, 59:1609-1623.
17. Hanaichi T., Sato T., Iwamoto T., Malavasi-Yamashiro J., Hoshino M., Mizuno N. A stable lead by modification of Sato's method. J. Electron Microsc. 1986, 35:304-306.
18. Hu Y., Benedict M.A., Ding L., Núñez G. Role of cytochrome c and dATP/ATP hydrolysis in Apaf-1-mediated caspase-9 activation and apoptosis. EMBO J. 1999, 18:3586-3595.
19. Iyanagi T., Yamazaki I. One-electron-transfer reactions in biochemical systems. V. Difference in the mechanism of quinone reduction by the NADH dehydrogenase and the NAD(P)H dehydrogenase (DT-diaphorase). Biochim. Biophys. Acta 1970, 216:282-294.
20. Kudin A.P., Bimpong-Buta N.Y., Vielhaber S., Elger C.E., Kunz W.S. Characterization of superoxide-producing sites in isolated brain mitochondria. J. Biol. Chem. 2004, 279:4127-4135.
21. Lamson D.W., Plaza S.M. The anticancer effects of vitamin K. Altern. Med. Rev. 2003, 8:303-318.
22. Li P., Nijhawan D., Budihardjo I., Srinivasula S.M., Ahmad M., Alnemri E.S., Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997, 14:479-489.
23. Lin M.T., Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443:787-795.
24. Maher P., Davis J.B. The role of monoamine metabolism in oxidative glutamate toxicity. J. Neurosci. 1996, 16:6394-6401.
25. Maier C.M., Chan P.H. Role of superoxide dismutases in oxidative damage and neurodegenerative disorders. Neuroscientist 2002, 8:323-334.
26. Murphy M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009, 417:1-13.
27. Nagata S., Nagase H., Kawane K., Mukae N., Fukuyama H. Degradation of chromosomal DNA during apoptosis. Cell Death Differ. 2003, 10:108-116.
28. Nunomura A., Perry G., Aliev G., Hirai K., Takeda A., Balraj E.K., Jones P.K., Ghanbari H., Wataya T., Shimohama S., Chiba S., Atwood C.S., Petersen R.B., Smith M.A. Oxidative damage is the earliest event in Alzheimer disease. J. Neuropathol. Exp. Neurol. 2001, 60:759-767.
29. Saitoh M., Nishitoh H., Fujii M., Takeda K., Tobiume K., Sawada Y., Kawabata M., Miyazono K., Ichijo H. Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 1998, 17:2596-2606.
30. Shiokawa D., Tanuma S. Differential DNases are selectively used in neuronal apoptosis depending on the differentiation state. Cell Death Differ. 2004, 11:1112-1120.
31. Smith M.A., Perry G., Richey P.L., Sayre L.M., Anderson V.E., Beal M.F., Kowall N. Oxidative damage in Alzheimer's. Nature 1996, 382:120-121.
32. Sompol P., Ittarat W., Tangpong J., Chen Y., Doubinskaia I., Batinic-Haberle I., Abdul H.M., Butterfield D.A., St Clair D.K. A neuronal model of Alzheimer's disease: an insight into the mechanisms of oxidative stress-mediated mitochondrial injury. Neuroscience 2008, 153:120-130.
33. Son J.H., Shim J.H., Kim K.H., Ha J.Y., Han J.Y. Neuronal autophagy and neurodegenerative diseases. Exp. Mol. Med. 2012, 44:89-98.
34. Sperandio S., de Belle I., Bredesen D.E. An alternative, nonapoptotic form of programmed cell death. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:14376-14381.
35. Thor H., Smith M.T., Hartzell P., Bellomo G., Jewell S.A., Orrenius S. The metabolism of menadione (2-methyl-1,4-naphthoquinone) by isolated hepatocytes. J. Biol. Chem. 1982, 257:12419-12425.
36. Tripathy D., Grammas P. Acetaminophen inhibits neuronal inflammation and protects neurons from oxidative stress. J. Neuroinflammation 2009, 6:10.
37. Trushina E., McMurray C.T. Oxidative stress and mitochondrial dysfunction in neurodegenerative diseases. Neuroscience 2007, 145:1233-1248.
38. Vandenabeele P., Galluzzi L., Vanden Berghe T., Kroemer G. Molecular mechanisms of necroptosis: an ordered cellular explosion. Nat. Rev. Mol. Cell Biol. 2010, 11:700-714.
39. White E.J., Clark J.B. Menadione-treated synaptosomes as a model for post-ischaemic neuronal damage. Biochem. J. 1988, 253:425-433.
40. Xilouri M., Stefanis L. Autophagy in the central nervous system: implications for neurodegenerative disorders. CNS Neurol. Disord. Drug Targets 2010, 9:701-719.
41. Xu X., Chua C.C., Kong J., Kostrzewa R.M., Kumaraguru U., Hamdy R.C., Chua B.H. Necrostatin-1 protects against glutamate-induced glutathione depletion and caspase-independent cell death in HT-22 cells. J. Neurochem. 2007, 103:2004-2014.
42. Zhang D.W., Shao J., Lin J., Zhang N., Lu B.J., Lin S.C., Dong M.Q., Han J. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 2009, 325:332-336.