8-Oxoguanine accumulation in mitochondrial DNA causes mitochondrial dysfunction and impairs neuritogenesis in cultured adult mouse cortical neurons under oxidative conditions

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Leon, Julio ^a   Sakumi, Kunihiko ^a   Castillo, Erika ^a   Sheng, Zijing ^a   Oka, Sugako ^a   Nakabeppu, Yusaku ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

8-HYDROXYGUANINE; DNA GLYCOSYLTRANSFERASE; GUANINE; MITOCHONDRIAL DNA; NUDT1 PROTEIN, MOUSE; OGG1 PROTEIN, MOUSE; PHOSPHATASE;

ANALOGS AND DERIVATIVES; ANIMAL; BRAIN CORTEX; CELL CULTURE; GENETICS; KNOCKOUT MOUSE; METABOLISM; MITOCHONDRION; MOUSE; NEURITE; OXIDATION REDUCTION REACTION;

ANIMALS; CELLS, CULTURED; CEREBRAL CORTEX; DNA GLYCOSYLASES; DNA, MITOCHONDRIAL; GUANINE; MICE; MICE, KNOCKOUT; MITOCHONDRIA; NEURITES; OXIDATION-REDUCTION; PHOSPHORIC MONOESTER HYDROLASES;

EID: 84959419639     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep22086     Document Type: Article

References (44)

1. Riemer, J., & Kins, S. Axonal transport and mitochondrial dysfunction in Alzheimer?s disease. Neurodegener Dis 12, 111-124 (2013).
2. Hokama, M., et al. Altered expression of diabetes-related genes in Alzheimer?s disease brains: the hisayama study. Cereb Cortex 24, 2476-2488 (2014).
3. Henchcliffe, C., & Beal, M. F. Mitochondrial biology and oxidative stress in Parkinson disease pathogenesis. Nat Clin Pract Neurol 4, 600-609 (2008).
4. Ayala-Pena, S. Role of oxidative DNA damage in mitochondrial dysfunction and Huntington?s disease pathogenesis. Free Radic Biol Med 62, 102-110 (2013).
5. Kang, D., Takeshige, K., Sekiguchi, M., & Singh, K. K. Introduction. In: Mitochondrial DNA mutations in aging, disease and cancer (ed. Singh, K. K.) Ch. 1, 1-15 (Springer-Verlag, 1999).
6. Nunnari, J., & Suomalainen, A. Mitochondria: in sickness and in health. Cell 148, 1145-1159 (2012).
7. Nakabeppu, Y., Behmanesh, M., Yamaguchi, H., Yoshimura, D., & Sakumi, K. Prevention of the Mutagnecity and Cytotoxicity of Oxidized Purine Nucleotides. In: Oxidative Damage to Nucleic Acids (eds Evans M. D., Cooke M. S.) Ch. 3, 40-53 (Landes Bioscience and Springer Science+Business Media, 2007).
8. Nakabeppu, Y., Oka, S., Sheng, Z., Tsuchimoto, D., & Sakumi, K. Programmed cell death triggered by nucleotide pool damage and its prevention by MutT homolog-1 (MTH1) with oxidized purine nucleoside triphosphatase. Mutat Res 703, 51-58 (2010).
9. Nakabeppu, Y. Cellular Levels of 8-Oxoguanine in either DNA or the nucleotide pool play pivotal roles in carcinogenesis and survival of cancer cells. Int J Mol Sci 15, 12543-12557 (2014).
10. de la Monte, S. M., Luong, T., Neely, T. R., Robinson, D., Wands, J. R., & Mitochondrial, D. N. A. damage as a mechanism of cell loss in Alzheimer?s disease. Lab Invest 80, 1323-1335 (2000).
11. Bradley-Whitman, M. A., Timmons, M. D., Beckett, T. L., Murphy, M. P., Lynn, B. C., & Lovell, M. A. Nucleic acid oxidation: an early feature of Alzheimer?s disease. J Neurochem 128, 294-304 (2014).
12. Shimura-Miura, H., Hattori, N., Kang, D., Miyako, K., Nakabeppu, Y., & Mizuno, Y. Increased 8-oxo-DGTPase in the mitochondria of substantia nigral neurons in Parkinson?s disease. Ann Neurol 46, 920-924 (1999).
13. Siddiqui, A., et al. Mitochondrial DNA damage is associated with reduced mitochondrial bioenergetics in Huntington?s disease. Free Radic Biol Med 53, 1478-1488 (2012).
14. Ohno, M., et al. 8-oxoguanine causes spontaneous de novo germline mutations in mice. Sci Rep 4, 4689 (2014).
15. Kang, D., et al. Intracellular localization of 8-oxo-DGTPase in human cells, with special reference to the role of the enzyme in mitochondria. J Biol Chem 270, 14659-14665 (1995).
16. Sheng, Z., et al. 8-Oxoguanine causes neurodegeneration during MUTYH-mediated DNA base excision repair. J Clin Invest 122, 4344-4361 (2012).
17. Boiteux, S., & Radicella, J. P. The human OGG1 gene: structure, functions, and its implication in the process of carcinogenesis. Arch Biochem Biophys 377, 1-8 (2000).
18. Nishioka, K., et al. Expression and differential intracellular localization of two major forms of human 8-oxoguanine DNA glycosylase encoded by alternatively spliced OGG1 mRNAs. Mol Biol Cell 10, 1637-1652 (1999).
19. Yoshimura, D., et al. An oxidized purine nucleoside triphosphatase, MTH1, suppresses cell death caused by oxidative stress. J Biol Chem 278, 37965-37973 (2003).
20. Ichikawa, J., et al. Oxidation of mitochondrial deoxynucleotide pools by exposure to sodium nitroprusside induces cell death. DNA Repair 7, 418-430 (2008).
21. Oka, S., Ohno, M., Tsuchimoto, D., Sakumi, K., Furuichi, M., & Nakabeppu, Y. Two distinct pathways of cell death triggered by oxidative damage to nuclear and mitochondrial DNAs. EMBO J 27, 421-432 (2008).
22. de Souza-Pinto, N. C., et al. Repair of 8-oxodeoxyguanosine lesions in mitochondrial dna depends on the oxoguanine DNA glycosylase (OGG1) gene and 8-oxoguanine accumulates in the mitochondrial DNA of OGG1-Defective mice. Cancer Res 61, 5378-5381 (2001).
23. Li, Z., Okamoto, K., Hayashi, Y., & Sheng, M. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119, 873-887 (2004).
24. Fukumitsu, K., Fujishima, K., Yoshimura, A., Wu, Y. K., Heuser, J., & Kengaku, M. Synergistic action of dendritic mitochondria and creatine kinase maintains ATP homeostasis and actin dynamics in growing neuronal dendrites. J Neurosci 35, 5707-5723 (2015).
25. Kambe, Y., & Miyata, A. Role of mitochondrial activation in PACAP dependent neurite outgrowth. J Mol Neurosci 48, 550-557 (2012).
26. Dent, E. W., et al. Filopodia are required for cortical neurite initiation. Nat Cell Biol 9, 1347-1359 (2007).
27. Ohno, M., Oka, S., & Nakabeppu, Y. Quantitative analysis of oxidized guanine, 8-oxoguanine, in mitochondrial DNA by immunofluorescence method. Methods Mol Biol 554, 199-212 (2009).
28. Reers, M., Smiley, S., Mottola-Hartshorn, C., Chen, A., Lin, M., & Chen, L. Mitochondrial membrane potential monitored by JC-1 dye. Methods Enzymol 260, 406-417 (1995).
29. Cline, S. D., & Mitochondrial, D. N. A. damage and its consequences for mitochondrial gene expression. Biochim Biophys Acta 1819, 979-991 (2012).
30. Shokolenko, I., Venediktova, N., Bochkareva, A., Wilson, G. L., & Alexeyev, M. F. Oxidative stress induces degradation of mitochondrial DNA. Nucleic Acids Res 37, 2539-2548 (2009).
31. Mattson, M., & Partin, J. Evidence for mitochondrial control of neuronal polarity. J Neurosci Res 56, 8-20 (1999).
32. Gupton, S. L., & Gertler, F. B. Integrin signaling switches the cytoskeletal and exocytic machinery that drives neuritogenesis. Dev Cell 18, 725-736 (2010).
33. Conde, C., & Caceres, A. Microtubule assembly, organization and dynamics in axons and dendrites. Nat Rev Neurosci 10, 319-332 (2009).
34. Schaefer, A. W., Schoonderwoert, V. T., Ji, L., Mederios, N., Danuser, G., & Forscher, P. Coordination of actin filament and microtubule dynamics during neurite outgrowth. Dev Cell 15, 146-162 (2008).
35. Goto, A., Hoshino, M., Matsuda, M., & Nakamura, T. Phosphorylation of STEF/Tiam2 by protein kinase A is critical for Rac1 activation and neurite outgrowth in dibutyryl cAMP-Treated PC12D cells. Mol Biol Cell 22, 1780-1790 (2011).
36. Sann, S., Wang, Z., Brown, H., & Jin, Y. Roles of endosomal trafficking in neurite outgrowth and guidance. Trends Cell Biol 19, 317-324 (2009).
37. Morris, R., & Hollenbeck, P. The regulation of bidirectional mitochondrial transport is coordinated with axonal outgrowth. J Cell Sci 104, 917-927 (1993).
38. Kimura, T., & Murakami, F. Evidence that dendritic mitochondria negatively regulate dendritic branching in pyramidal neurons in the neocortex. J Neurosci 34, 6938-6951 (2014).
39. Kauppinen, T. M., & Swanson, R. A. Poly(ADP-ribose) polymerase-1 promotes microglial activation, proliferation, and matrix metalloproteinase-9-mediated neuron death. J Immunol 174, 2288-2296 (2005).
40. Tsuzuki, T., et al. Spontaneous tumorigenesis in mice defective in the MTH1 gene encoding 8-oxo-DGTPase. Proc Natl Acad Sci USA 98, 11456-11461 (2001).
41. Sakumi, K., et al. Ogg1 knockout-Associated lung tumorigenesis and its suppression by Mth1 gene disruption. Cancer Res 63, 902-905 (2003).
42. Brewer, G. J., & Torricelli, J. R. Isolation and culture of adult neurons and neurospheres. Nat Protoc 2, 1490-1498 (2007).
43. Kakuma, T., Nishida, J., Tsuzuki, T., & Sekiguchi, M. Mouse MTH1 protein with 8-oxo-7, 8-Dihydro-2'-Deoxyguanosine 5'-Triphosphatase activity that prevents transversion mutation. cDNA cloning and tissue distribution. J Biol Chem 270, 25942-25948 (1995).
44. Schindelin, J., et al. Fiji: an open-source platform for biological-image analysis. Nat Methods 9, 676-682 (2012).