Inhibition of mTOR prevents ROS production initiated by ethidium bromide-induced mitochondrial DNA depletion

Frontiers in Endocrinology

Volumn 5, Issue JUL, 2014, Pages

  Nacarelli, Timothy ^a   Azar, Ashley ^a   Sell, Christian ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Aging; Ethidium bromide; Mitochondria; mTOR; p38; Rapamycin; ROS; Senescence

Indexed keywords

ETHIDIUM BROMIDE; MAMMALIAN TARGET OF RAPAMYCIN; MITOCHONDRIAL DNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; PARKIN; PROTEIN KINASE B; PROTEIN P62; REACTIVE OXYGEN METABOLITE; VOLTAGE DEPENDENT ANION CHANNEL;

ARTICLE; CELL CULTURE; CELL STRESS; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA EXTRACTION; GENE DOSAGE; HOMEOSTASIS; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MITOCHONDRIAL DNA DEPLETION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOPHAGY; PROTEIN ISOLATION; REAL TIME POLYMERASE CHAIN REACTION; RESPIRATORY CHAIN; WESTERN BLOTTING;

EID: 84905484180     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2014.00122     Document Type: Article

References (42)

1. Tuppen HA, Blakely EL, Turnbull DM, Taylor RW. Mitochondrial DNA mutations and human disease. Biochim Biophys Acta (2010) 1797:113-28. doi: 10.1016/j.bbabio.2009.09.005
2. Milone M, Wong LJ. Diagnosis of mitochondrial myopathies. Mol Genet Metab (2013) 110:35-41. doi:10.1016/j.ymgme.2013.07.007
3. Copeland WC, Longley MJ. Mitochondrial genome maintenance in health and disease. DNA Repair (Amst) (2014) 19:190-8. doi:10.1016/j.dnarep.2014.03.010
4. El-Hattab AW, Scaglia F. Mitochondrial DNA depletion syndromes: review and updates of genetic basis, manifestations, and therapeutic options. Neurotherapeutics (2013) 10:186-98. doi:10.1007/s13311-013-0177-6
5. Trifunovic A, Wredenberg A, Falkenberg M, Spelbrink JN, Rovio AT, Bruder CE, et al. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature (2004) 429:417-23. doi:10.1038/nature02517
6. Anderson S, Bankier AT, Barrell BG, De Bruijn MH, Coulson AR, Drouin J, et al. Sequence and organization of the human mitochondrial genome. Nature (1981) 290:457-65. doi:10.1038/290457a0
7. Shmookler Reis RJ, Goldstein S. Mitochondrial DNA in mortal and immortal human cells. Genome number, integrity, and methylation. J Biol Chem (1983) 258:9078-85.
8. Omura T. Mitochondria-targeting sequence, a multi-role sorting sequence recognized at all steps of protein import into mitochondria. J Biochem (1998) 123:1010-6. doi:10.1093/oxfordjournals.jbchem.a022036
9. Taylor SW, Fahy E, Zhang B, Glenn GM, Warnock DE, Wiley S, et al. Characterization of the human heart mitochondrial proteome. Nat Biotechnol (2003) 21:281-6. doi:10.1038/nbt793
10. Lefort N, Yi Z, Bowen B, Glancy B, De Filippis EA, Mapes R, et al. Proteome profile of functional mitochondria from human skeletal muscle using one-dimensional gel electrophoresis and HPLC-ESI-MS/MS. J Proteomics (2009) 72:1046-60. doi:10.1016/j.jprot.2009.06.011
11. Sena EP, Welch JW, Halvorson HO, Fogel S. Nuclear and mitochondrial deoxyribonucleic acid replication during mitosis in Saccharomyces cerevisiae. J Bacteriol (1975) 123:497-504.
12. Bogenhagen D, Clayton DA. Mouse L cell mitochondrial DNA molecules are selected randomly for replication throughout the cell cycle. Cell (1977) 11:719-27. doi:10.1016/0092-8674(77)90286-0
13. Davis AF, Clayton DA. In situ localization of mitochondrial DNA replication in intact mammalian cells. J Cell Biol (1996) 135:883-93. doi:10.1083/jcb.135.4.883
14. Magnusson J, Orth M, Lestienne P, Taanman JW. Replication of mitochondrial DNA occurs throughout the mitochondria of cultured human cells. Exp Cell Res (2003) 289:133-42. doi:10.1016/S0014-4827(03)00249-0
15. Nass MM. Abnormal DNA patterns in animal mitochondria: ethidium bromide-induced breakdown of closed circular DNA and conditions leading to oligomer accumulation. Proc Natl Acad Sci U S A (1970) 67:1926-33. doi:10.1073/pnas.67.4.1926
16. Zylber E, Penman S. Mitochondrial-associated 4 S RNA synthesis inhibition by ethidium bromide. J Mol Biol (1969) 46:201-4.
17. Zylber E, Vesco C, Penman S. Selective inhibition of the synthesis of mitochondria-associated RNA by ethidium bromide. J Mol Biol (1969) 44:195-204.
18. Nass MM. Differential effects of ethidium bromide on mitochondrial and nuclear DNA synthesis in vivo in cultured mammalian cells. Exp Cell Res (1972) 72:211-22. doi:10.1016/0014-4827(72)90583-6
19. Desjardins P, Frost E, Morais R. Ethidium bromide-induced loss of mitochondrial DNA from primary chicken embryo fibroblasts. Mol Cell Biol (1985) 5:1163-9.
20. Olgun A, Akman S. Mitochondrial DNA-deficient models and aging. Ann N Y Acad Sci (2007) 1100:241-5. doi:10.1196/annals.1395.025
21. Kao LP, Ovchinnikov D, Wolvetang E. The effect of ethidium bromide and chloramphenicol on mitochondrial biogenesis in primary human fibroblasts. Toxicol Appl Pharmacol (2012) 261:42-9. doi:10.1016/j.taap.2012.03.009
22. Ghosh S, Patel N, Rahn D, Mcallister J, Sadeghi S, Horwitz G, et al. The thiazolidinedione pioglitazone alters mitochondrial function in human neuron-like cells. Mol Pharmacol (2007) 71:1695-702. doi:10.1124/mol.106.033845
23. Behan A, Doyle S, Farrell M. Adaptive responses to mitochondrial dysfunction in the rho degrees Namalwa cell. Mitochondrion (2005) 5:173-93. doi:10.1016/j.mito.2005.03.002
24. Seidel-Rogol BL, Shadel GS. Modulation of mitochondrial transcription in response to mtDNA depletion and repletion in HeLa cells. Nucleic Acids Res (2002) 30:1929-34. doi:10.1093/nar/30.9.1929
25. Bitto A, Lerner C, Torres C, Roell M, Malaguti M, Perez V, et al. Long-term IGF-I exposure decreases autophagy and cell viability. PLoS One (2010) 5:e12592. doi:10.1371/journal.pone.0012592
26. Hashiguchi K, Zhang-Akiyama QM. Establishment of human cell lines lacking mitochondrial DNA. Methods Mol Biol (2009) 554:383-91. doi:10.1007/978-1-59745-521-3_23
27. Cristofalo VJ, Charpentier R. A standard procedure for cultivating human diploid fibroblast like cells to study cellular aging. J Tissue Cult Methods (1980) 6:117-21. doi:10.1007/BF02082862
28. Guo W, Jiang L, Bhasin S, Khan SM, Swerdlow RH. DNA extraction procedures meaningfully influence qPCR-based mtDNA copy number determination. Mitochondrion (2009) 9:261-5. doi:10.1016/j.mito.2009.03.003
29. Lerner C, Bitto A, Pulliam D, Nacarelli T, Konigsberg M, Van Remmen H, et al. Reduced mammalian target of rapamycin activity facilitates mitochondrial retrograde signaling and increases life span in normal human fibroblasts. Aging Cell (2013) 12:966-77. doi:10.1111/acel.12122
30. Rogaeva E, Johnson J, Lang AE, Gulick C, Gwinn-Hardy K, Kawarai T, et al. Analysis of the PINK1 gene in a large cohort of cases with Parkinson disease. Arch Neurol (2004) 61:1898-904. doi:10.1001/archneur.61.12.1898
31. Geisler S, Holmstrom KM, Treis A, Skujat D, Weber SS, Fiesel FC, et al. The PINK1/Parkin-mediated mitophagy is compromised by PD-associated mutations. Autophagy (2010) 6:871-8. doi:10.4161/auto.6.7.13286
32. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J, et al. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol (2010) 8:e1000298. doi:10.1371/journal.pbio.1000298
33. Luo Y, Hu Y, Zhang M, Xiao Y, Song Z, Xu Y. EtBr-induced selective degradation of mitochondria occurs via autophagy. Oncol Rep (2013) 30:1201-8. doi:10.3892/or.2013.2590
34. Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, et al. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature (2009) 460:392-5. doi:10.1038/nature08221
35. Miller RA, Harrison DE, Astle CM, Fernandez E, Flurkey K, Han M, et al. Rapamycin-mediated lifespan increase in mice is dose and sex dependent and metabolically distinct from dietary restriction. Aging Cell (2014) 13:468-77. doi:10.1111/acel.12194
36. Johnson SC, Yanos ME, Kayser EB, Quintana A, Sangesland M, Castanza A, et al. mTOR inhibition alleviates mitochondrial disease in a mouse model of Leigh syndrome. Science (2013) 342:1524-8. doi:10.1126/science.1244360
37. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy (2012) 8:445-544. doi:10.4161/auto.19496
38. Haruta T, Uno T, Kawahara J, Takano A, Egawa K, Sharma PM, et al. A rapamycin-sensitive pathway down-regulates insulin signaling via phosphorylation and proteasomal degradation of insulin receptor substrate-1. Mol Endocrinol (2000) 14:783-94. doi:10.1210/mend.14.6.0446
39. Zhang H, Hoff H, Sell C. Insulin-like growth factor I-mediated degradation of insulin receptor substrate-1 is inhibited by epidermal growth factor in prostate epithelial cells. J Biol Chem (2000) 275:22558-62. doi:10.1074/jbc.M000412200
40. Pederson TM, Kramer DL, Rondinone CM. Serine/threonine phosphorylation of IRS-1 triggers its degradation: possible regulation by tyrosine phosphorylation. Diabetes (2001) 50:24-31. doi:10.2337/diabetes.50.1.24
41. Huang J, Manning BD. A complex interplay between Akt, TSC2 and the two mTOR complexes. Biochem Soc Trans (2009) 37:217-22. doi:10.1042/BST0370217
42. Moiseeva O, Bourdeau V, Roux A, Deschenes-Simard X, Ferbeyre G. Mitochondrial dysfunction contributes to oncogene-induced senescence. Mol Cell Biol (2009) 29:4495-507. doi:10.1128/MCB.01868-08