BMB Reports

Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
권호 표지
DOI QR코드

DOI QR Code

Mitochondrial superoxide anion (O2·-) inducible "mev-1" animal models for aging research

  • Ishii, Takamasa (Department of Molecular Life Science, Basic Medical Science and Molecular Medicine, Tokai University School of Medicine) ;
  • Miyazawa, Masaki (Department of Molecular Life Science, Basic Medical Science and Molecular Medicine, Tokai University School of Medicine) ;
  • Hartman, Phil S. (Department of Biology, Texas Christian University) ;
  • Ishii, Naoaki (Department of Molecular Life Science, Basic Medical Science and Molecular Medicine, Tokai University School of Medicine)
  • Received : 2011.04.20
  • Published : 2011.05.31
Download PDF
⟨ Previous Next ⟩

Abstract

Most intracellular reactive oxygen species (ROS), especially superoxide anion ($O_2^{{\bullet}_-}$) that is converted from oxygen, are overproduced by excessive electron leakage from the mitochondrial respiratory chain. Intracellular oxidative stress that damages cellular components can contribute to lifestyle-related diseases such as diabetes and arteriosclerosis, and age-related diseases such as cancer and neuronal degenerative diseases. We have previously demonstrated that the excessive mitochondrial $O_2^{{\bullet}_-}$ production caused by SDHC mutations (G71E in C. elegans, I71E in Drosophila and V69E in mouse) results in premature death in C. elegans and Drosophila, cancer in mouse embryonic fibroblast cells and infertility in transgenic mice. SDHC is a subunit of mitochondrial complex II. In humans, it has been reported that mutations in SDHB, SDHC or SDHD often result in inherited head and neck paragangliomas (PGLs). Recently, we established Tet-mev-1 conditional transgenic mice using our uniquely developed Tet-On/Off system, which equilibrates transgene expression to endogenous levels. These mice experienced mitochondrial respiratory chain dysfunction that resulted in $O_2^{{\bullet}_-}$ overproduction. The mitochondrial oxidative stress caused excessive apoptosis leading to low birth weight and growth retardation in the neonatal developmental phase in Tet-mev-1 mice. Here, we briefly describe the relationships between mitochondrial $O_2^{{\bullet}_-}$ and aging phenomena in mev-1 animal models

Keywords

References

  1. Nohl, H. and Hegner, D. (1978) Do mitochondria produce oxygen radicals in vivo? Eur. J. Biochem. 82, 563-567. https://doi.org/10.1111/j.1432-1033.1978.tb12051.x
  2. Wallace, D. C. (1999) Mitochondrial diseases in man and mouse. Science 283, 1482-1488. https://doi.org/10.1126/science.283.5407.1482
  3. Leonard, J. V. and Schapira, A. H. (2000) Mitochondrial respiratory chain disorders: I. mitochondrial DNA defects. Lancet 355, 299-304. https://doi.org/10.1016/S0140-6736(99)05225-3
  4. Attardi, G. and Schatz, G. (1988) Biogenesis of mitochondria. Ann. Rev. Cell Biol. 4, 289-333. https://doi.org/10.1146/annurev.cb.04.110188.001445
  5. Turrens, J. F. (2003) Mitochondrial formation of reactive oxygen species. J. Physiol. 552, 335-344. https://doi.org/10.1113/jphysiol.2003.049478
  6. Chance, B., Sies, H. and Boveris, A. (1979) Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 59, 527-605. https://doi.org/10.1152/physrev.1979.59.3.527
  7. Fridovich, I. (2004) Mitochondria: are they the seat of senescence? Aging Cell 3, 13-16. https://doi.org/10.1046/j.1474-9728.2003.00075.x
  8. Turrens, J. F. (1997) Superoxide production by the mitochondrial respiratory chain. Biosci. Rep. 17, 3-8. https://doi.org/10.1023/A:1027374931887
  9. Lenaz, G. (1998) Role of mitochondria in oxidative stress and ageing. Biochim. Biophys. Acta. Bioenerg. 1366, 53- 67. https://doi.org/10.1016/S0005-2728(98)00120-0
  10. Finkel, T. and Holbrook, N. J. (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408, 239-247. https://doi.org/10.1038/35041687
  11. Raha, S. and Robinson, B. H. (2000) Mitochondria, oxygen free radicals, disease and ageing. Trends Biochem. Sci. 25, 502-508. https://doi.org/10.1016/S0968-0004(00)01674-1
  12. Sun, J. and Trumpower, B. L. (2003) Superoxide anion generation by the cytochrome bc1 complex. Arch. Biochem. Biophys. 419, 198-206. https://doi.org/10.1016/j.abb.2003.08.028
  13. St-Pierre, J., Buckingham, J. A., Roebuck, S. J. and Brand, M. D. (2002) Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 277, 44784-44790. https://doi.org/10.1074/jbc.M207217200
  14. Lenaz, G., Fato, R., Genova, M. L., Bergamini, C., Bianchi, C. and Biondi, A. (2006) Mitochondrial complex I: structural and functional aspects. Biochim. Biophys. Acta. 1757, 1406-1420. https://doi.org/10.1016/j.bbabio.2006.05.007
  15. Senoo-Matsuda, N., Yasuda, K., Tsuda, M., Ohkubo, T., Yoshimura, S., Nakazawa, H., Hartman, P. S. and Ishii, N. (2001) A defect in the cytochrome b large subunit in complex II causes both superoxide anion overproduction and abnormal energy metabolism in Caenorhabditis elegans. J. Biol. Chem. 276, 41553-41558. https://doi.org/10.1074/jbc.M104718200
  16. Ishii, T., Yasuda, K., Akatsuka, A., Hino, O., Hartman, P. S. and Ishii, N. (2005) A mutation in the SDHC gene of complex II increases oxidative stress, resulting in apoptosis and tumorigenesis. Cancer Res. 65, 203-209.
  17. Paranagama, M. P., Sakamoto, K., Amino, H., Awano, M., Miyoshi, H. and Kita, K. (2010) Contribution of the FAD and quinone binding sites to the production of reactive oxygen species from Ascaris suum mitochondrial complex II. Mitochondrion 10, 158-165. https://doi.org/10.1016/j.mito.2009.12.145
  18. Gottlieb, E. and Tomlinson, I. P. (2005) Mitochondrial tumour suppressors: a genetic and biochemical update. Nat. Rev. Cancer 5, 857-866. https://doi.org/10.1038/nrc1737
  19. Echtay, K. S. (2007) Mitochondrial uncoupling proteinswhat is their physiological role? Free Radic. Biol. Med. 43, 1351-1371. https://doi.org/10.1016/j.freeradbiomed.2007.08.011
  20. Chandel, N. S., Maltepe, E., Goldwasser, E., Mathieu, C. E., Simon, M. C. and Schumacker, P. T. (1998) Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl. Acad. Sci. U.S.A. 95, 11715-11720. https://doi.org/10.1073/pnas.95.20.11715
  21. Guzy, R. D., Hoyos, B., Robin, E., Chen, H., Liu, L., Mansfield, K. D., Simon, M. C., Hammerling, U. and Schumacker, P. T. (2005) Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab. 1, 401-408. https://doi.org/10.1016/j.cmet.2005.05.001
  22. Emerling, B. M., Weinberg, F., Snyder, C., Burgess, Z., Mutlu, G. M., Viollet, B., Budinger, G. R. and Chandel, N. S. (2009) Hypoxic activation of AMPK is dependent on mitochondrial ROS but independent of an increase in AMP/ATP ratio. Free Radic. Biol. Med. 46, 1386-1391. https://doi.org/10.1016/j.freeradbiomed.2009.02.019
  23. Vuillaume, M. (1987) Reduced oxygen species, mutation, induction and cancer initiation. Mutat. Res. 186, 43-72. https://doi.org/10.1016/0165-1110(87)90014-5
  24. Collins, A. R., Duthie, S. J., Fillion, L., Gedik, C. M., Vaughan, N. and Wood, S. G. (1997) Oxidative DNA damage in human cells: the influence of antioxidants and DNA repair. Biochem. Soc. Trans. 25, 326-331. https://doi.org/10.1042/bst0250326
  25. Uchida K. (2003) 4-Hydroxy-2-nonenal: a product and mediator of oxidative stress. Prog. Lipid Res. 42, 318-343. https://doi.org/10.1016/S0163-7827(03)00014-6
  26. Cross, C. E., Halliwell, B., Borish, E. T., Pryor, W. A., Ames, B. N., Saul, R. L., McCord, J. M. and Harman, D. (1987) Oxygen radicals and diseases. Ann. Intrern. Med. 107, 526-545. https://doi.org/10.7326/0003-4819-107-4-526
  27. Reddy, P. H. and Beal, M. F. (2005) Are mitochondria critical in the pathogenesis of Alzheimer's disease? Brain Res. Rev. 49, 618-632. https://doi.org/10.1016/j.brainresrev.2005.03.004
  28. Martin, I. and Grotewiel, M. S. (2006) Oxidative damage and age-related functional declines. Mech. Ageing Dev. 127, 411-423. https://doi.org/10.1016/j.mad.2006.01.008
  29. Valko, M., Rhodes, C. J., Moncol, J., Izakovic, M. and Mazur, M. (2006) Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Biol. Interact. 160, 1-40. https://doi.org/10.1016/j.cbi.2005.12.009
  30. Valko, M., Leibfritz, D., Moncol, J., Cronin, M. T., Mazur, M. and Telser, J. (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 39, 44-84. https://doi.org/10.1016/j.biocel.2006.07.001
  31. Murfitt, R. R., Vogel, K. and Sanadi, D. R. (1976) Characterization of the mitochondria of the free-living nematode, Caenorhabditis elegans. Comp. Biochem. Physiol. B. 53, 423-430. https://doi.org/10.1016/0305-0491(76)90191-7
  32. Okimoto, R., Macfarlane, J. L., Clary, D. O. and Wolstenholme, D. R. (1992) The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Genetics 130, 471-498.
  33. Ishii, N., Fujii, M., Hartman, P. S., Tsuda, M., Yasuda, K., Senoo-Matsuda, N., Yanase, S., Ayusawa, D. and Suzuki, K. (1998) A mutation in succinate dehydrogenase cytochrome b causes oxidative stress and ageing in nematodes. Nature 394, 694-697. https://doi.org/10.1038/29331
  34. Tsuda, M., Sugiura, T., Ishii, T., Ishii, N. and Aigaki, T. (2007) A mev-1-like dominant-negative SdhC increases oxidative stress and reduces lifespan in Drosophila. Biochem. Biophys. Res. Commun. 363, 342-346. https://doi.org/10.1016/j.bbrc.2007.08.168
  35. Ishii, N., Takahashi, K., Tomita, S., Keino, T., Honda, S., Yoshino, K. and Suzuki, K. (1990) A methyl viologen- sensitive mutant of the nematode Caenorhabditis elegans. Mutat. Res. 237, 165-171. https://doi.org/10.1016/0921-8734(90)90022-J
  36. Honda, S., Ishii, N., Suzuki, K. and Matsuo, M. (1993) Oxygen-dependent perturbation of life span and aging rate in the nematode. J. Gerontl. Ser. A Biol. Sci. 48, B57-B61.
  37. Strehler, B. L., Mark, D. D., Mildvan, A. S. and Gee, M. V. (1959) Rate and magnitude of age pigment accumulation in the human myocardium. J. Gerontl. 14, 257-264.
  38. Spoerri, P. E., Glass, P. and El Ghazzawi, E. (1974) Accumulation of lipofuscin in the myocardium of senile guinia pigs; dissolution and removal of lipofuscin following dimethylaminoethyl p-chloroohenoxyacetate administration. An electron microscopy study. Mech. Ageing Dev. 3, 311-321. https://doi.org/10.1016/0047-6374(74)90027-X
  39. Stadman, E. R. and Oliver, C. N. (1991) Metal-catalyzed oxidation of proteins. J. Biol. Chem. 266, 2005-2008.
  40. Stadman, E. R. (1992) Protein oxidation and aging. Science 257, 1220-1224. https://doi.org/10.1126/science.1355616
  41. Hosokawa, H., Ishii, N., Ishida, H., Ichimori, K., Nakazawa, H. and Suzuki, K. (1994) Rapid accumulation of fluorescent material with aging in an oxygen-sensitive mutant mev-1 of Caenorhabditis elegans. Mech. Ageing Dev. 74, 161-170. https://doi.org/10.1016/0047-6374(94)90087-6
  42. Adachi, H., Fujiwara, Y. and Ishii, N. (1998) Effects of oxygen on protein carbonyl and aging in Caenorhabditis elegans mutants with long (age-1) and short (mev-1) life spans. J. Gerontol. Ser. A Biol. Sci. Med. Sci. 53, B240- 244.
  43. Senoo-Matsuda, N., Hartman, P. S., Akatsuka, A., Yoshimura, S. and Ishii, N. (2003) A complex II defect affects mitochondrial structure, leading to ced-3- and ced-4-dependent apoptosis and aging. J. Biol. Chem. 278, 22031- 22036. https://doi.org/10.1074/jbc.M211377200
  44. Hartman, P. S, Ishii, N., Kayser, E. B., Morgan, P. G. and Sedensky, M. M. (2001) Mitochondrial mutations differentially affect aging, mutability and anesthetic sensitivity in Caenorhabditis elegans. Mech. Ageing Dev. 122, 1187- 1201. https://doi.org/10.1016/S0047-6374(01)00259-7
  45. Yankovskaya, V., Horsefield, R., Tornroth, S., Luna- Chavez, C., Miyoshi, H., Leger, C., Byrne, B., Cecchini, G. and Iwata, S. (2003) Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 299, 700-704. https://doi.org/10.1126/science.1079605
  46. Cecchini, G. (2003) Function and structure of complex II of the respiratory chain. Annu. Rev. Biochem. 72, 77-109. https://doi.org/10.1146/annurev.biochem.72.121801.161700
  47. Sun, F., Huo, X., Zhai, Y. A., Wang, A., Xu, J., Su, D., Bartlam, M. and Rao, Z. (2005) Crystal structure of mitochondrial respiratory membrane protein complex II. Cell 121, 1043-1057. https://doi.org/10.1016/j.cell.2005.05.025
  48. Bourgeron, T., Rustin, P., Chretien, D., Birch-Machin, M., Bourgeois, M., Viegas-Péquignot, E., Munnich, A. and Rötig, A. (1995) Mutation of a nuclear succinate dehydrogenase gene results in mitochondrial respiratory chain deficiency. Nat. Genet. 11, 144-149. https://doi.org/10.1038/ng1095-144
  49. Ackrell, B. A. (2000) Progress in understanding structure- function relationships in respiratory chain complex II. FEBS Lett. 466, 1-5. https://doi.org/10.1016/S0014-5793(99)01749-4
  50. Ackrell, B. A. (2002) Cytopathies involving mitochondrial complex II. Mol. Aspects. Med. 23, 369-384. https://doi.org/10.1016/S0098-2997(02)00012-2
  51. Baysal, B. E., Ferrell, R. E., Willett-Brozick, J. E., Lawrence, E. C., Myssiorek, D., Bosch, A., van der Mey, A., Taschner, P. E., Rubinstein, W. S., Myers, E. N., Richard, C. W. 3rd, Cornelisse, C. J., Devilee, P. and Devlin, B. (2000) Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science 287, 848-851. https://doi.org/10.1126/science.287.5454.848
  52. Niemann, S. and Müller U. (2000) Mutations in SDHC cause autosomal dominant paraganglioma, type 3. Nat. Genet. 26, 268-270. https://doi.org/10.1038/81551
  53. Astuti, D., Latif, F., Dallol, A., Dahia, P. L., Douglas, F., George, E., Sköldberg, F., Husebye, E. S., Eng, C. and Maher, E. R. (2001) Gene mutations in the succinate dehydrogenase subunit SDHB cause susceptibility to familial pheochromocytoma and to familial paraganglioma. Am. J. Hum. Genet. 69, 49-54. https://doi.org/10.1086/321282
  54. Gimenez-Roqueplo, A. P., Favier, J., Rustin, P., Mourad, J. J., Plouin, P. F., Corvol, P., Rötig, A. and Jeunemaitre, X. (2001) The R22X mutation of the SDHD gene in hereditary paraganglioma abolishes the enzymatic activity of complex II in the mitochondrial respiratory chain and activates the hypoxia pathway. Am. J. Hum. Genet. 69, 1186- 1197. https://doi.org/10.1086/324413
  55. Gimenez-Roqueplo, A. P., Favier, J., Rustin, P., Rieubland, C., Kerlan, V., Plouin, P. F., Rötig, A. and Jeunemaitre, X. (2002) Functional consequences of a SDHB gene mutation in an apparently sporadic pheochromocytoma. J. Clin. Endocrinol. Metab. 87, 4771- 4774. https://doi.org/10.1210/jc.2002-020525
  56. Selak, M. A., Armour, S. M., MacKenzie, E. D., Boulahbel, H., Watson, D. G., Mansfield, K. D., Pan, Y., Simon, M. C., Thompson, C. B. and Gottlieb, E. (2005) Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 7, 77-85. https://doi.org/10.1016/j.ccr.2004.11.022
  57. Semenza, G. L. (2003) Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3, 721-732. https://doi.org/10.1038/nrc1187
  58. Nakada, K., Inoue, K., Chen, C. S., Nonaka, I., Goto, Y., Ogura, A. and Hayashi, J. I. (2001) Correlation of functional and ultrastructural abnormalities of mitochondria in mouse heart carrying a pathogenic mutant mtDNA with a 4696-bp deletion. Biochem. Biophys. Res. Commun. 288, 901-907. https://doi.org/10.1006/bbrc.2001.5873
  59. Ichimiya, H., Huet, R. G., Hartman, P., Amino, H., Kita, K. and Ishii, N. (2002) Complex II inactivation is lethal in the nematode Caenorhabditis elegans. Mitochondrion 2, 191-198. https://doi.org/10.1016/S1567-7249(02)00069-7
  60. Miyazawa, M., Ishii, T., Kirinashizawa, M., Yasuda, K., Hino, O., Hartman, P. S. and Ishii, N. (2008) Cell growth of the mouse SDHC mutant cells was suppressed by apoptosis throughout mitochondrial pathway. BioScience Trends 2, 22-30.
  61. Ishii, T., Miyazawa, M., Onodera, A., Yasuda, K., Kawabe, N., Kirinashizawa, M., Yoshimura, S., Maruyama, N., Hartman, P. S. and Ishii, N. (2011) Mitochondrial reactive oxygen species generation by the SDHC V69E mutation causes low birth weight and neonatal growth retardation. Mitochondrion 11, 155-165. https://doi.org/10.1016/j.mito.2010.09.006
  62. Gossen, M. and Bujard, H. (1992) Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. U.S.A. 89, 5547-5551. https://doi.org/10.1073/pnas.89.12.5547
  63. Gossen, M., Freundlieb, S., Bender, G., Muller, G., Hillen, W. and Bujard, H. (1995) Transcriptional activation by tetracyclines in mammalian cells. Science 268, 1766-1769. https://doi.org/10.1126/science.7792603
  64. Freundlieb, S., Schirra-Muller, C. and Bujard, H. (1999) A tetracycline controlled activation/repression system with increased potential for gene transfer into mammalian cells. J. Gene Med. 1, 4-12. https://doi.org/10.1002/(SICI)1521-2254(199901/02)1:1<4::AID-JGM4>3.0.CO;2-Y
  65. Uchida, S., Sakai, S., Furuichi, T., Hosoda, H., Toyota, K., Ishii, T., Kitamoto, A., Sekine, M., Koike, K., Masushige, S., Murphy, G., Silva, A. J. and Kida, S. (2006) Tight regulation of transgene expression by tetracycline-dependent activator and repressor in brain. Genes Brain Behav. 5, 96-106.
  66. Oberley, L. W. and Buettner, G. R. (1979) Role of superoxide dismutase in cancer: a review. Cancer Res. 39, 1141-1149.
  67. Oberley, L. W., Oberley, T. D. and Buettner, G. R. (1980) Cell differentiation, aging and cancer: the possible roles of superoxide and superoxide dismutases. Med. Hypotheses 6, 249-268. https://doi.org/10.1016/0306-9877(80)90123-1
  68. Oberley, L. W. and Oberley, T. D. (1988) Role of antioxidant enzymes in cell immortalization and transformation. Mol. Cell. Biochem. 84, 147-153. https://doi.org/10.1007/BF00421049
  69. Tomitsuka, E., Kita, K. and Esumi H. (2010) The NADH-fumarate reductase system, a novel mitochondrial energy metabolism, is a new target for anticancer therapy in tumor microenvironments. Ann. NY Acad. Sci. 1201, 44-49. https://doi.org/10.1111/j.1749-6632.2010.05620.x

Cited by

  1. On the properties of calcium-induced permeability transition in neonatal heart mitochondria vol.43, pp.6, 2011, https://doi.org/10.1007/s10863-011-9401-4
  2. Genetically induced oxidative stress in mice causes thrombocytosis, splenomegaly and placental angiodysplasia that leads to recurrent abortion vol.2, 2014, https://doi.org/10.1016/j.redox.2014.05.001
  3. Mitochondria: Redox Metabolism and Dysfunction vol.2012, 2012, https://doi.org/10.1155/2012/896751
  4. The Interplay Between Respiratory Supercomplexes and ROS in Aging vol.23, pp.3, 2015, https://doi.org/10.1089/ars.2014.6214
  5. Natural compounds with anti-ageing activity vol.30, pp.11, 2013, https://doi.org/10.1039/c3np70031c
  6. Loss of mitochondrial peptidase Clpp leads to infertility, hearing loss plus growth retardation via accumulation of CLPX, mtDNA and inflammatory factors vol.22, pp.24, 2013, https://doi.org/10.1093/hmg/ddt338
  7. Antiarrhythmic effect of tamoxifen on the vulnerability induced by hyperthyroidism to heart ischemia/reperfusion damage vol.143, 2014, https://doi.org/10.1016/j.jsbmb.2014.06.006
  8. Reactive oxygen species are generated by the respiratory complex II - evidence for lack of contribution of the reverse electron flow in complex I 2013, https://doi.org/10.1111/febs.12086
  9. Gene expression profiling for human iPS-derived motor neurons from sporadic ALS patients reveals a strong association between mitochondrial functions and neurodegeneration vol.9, 2015, https://doi.org/10.3389/fncel.2015.00289
  10. Oxidation events and skin aging vol.21, 2015, https://doi.org/10.1016/j.arr.2015.01.001
  11. Infertility and recurrent miscarriage with complex II deficiency-dependent mitochondrial oxidative stress in animal models vol.155, 2016, https://doi.org/10.1016/j.mad.2016.02.013
  12. A New Mouse Model of Dry Eye Disease vol.31, 2012, https://doi.org/10.1097/ICO.0b013e31826a5de1
  13. Dimethyl sulfoxide induces oxidative stress in the yeastSaccharomyces cerevisiae vol.13, pp.8, 2013, https://doi.org/10.1111/1567-1364.12091