Structural changes of mitochondria related to apoptosis: swelling and megamitochondria formation

• Autorzy: Wakabayashi T.
• Języki publikacji: EN

Abstrakty

EN

Recently we have found that the formation of megamitochondria in culture cells of various sources, induced by chemicals capable of generating free radicals, is followed by apoptotic changes of the cell. Detailed analysis on functional and morphological aspects of megamitochondria has enabled us to speculate that the formation of megamitochondria may be a prerequisite for free radical-mediated apoptosis: free radicals modify the mitochondrial membranes resulting in the fusion of adjacent mitochondria (megamitochondria formation). If the intracellular level of free radicals is continuously kept high, the permeability transition pores of the megamitochondria membranes are opened and megamitochondria become swollen. Oxygen consumption and the ability to synthesise ATP by swollen megamitochondria decrease distinctly. At the same time, cytochrome c is released from swollen megamitochondria into the cytoplasm. If lowered rates of the generation of reactive oxygen species from swollen megamitochondria, possibly due to decrease in their oxygen consumption, are effective enough to lower the intracellular level of free radicals, megamitochondria may return to normal. If not, decrease in the membrane potential of megamitochondria membranes causes the release of apoptosis-inducing factor into the cytoplasm. Cytochrome c and apoptosis-inducing factor thus released into the cytoplasm may cause cytoplasmic and nuclear apoptotic changes. Experimental data to support this hypothesis are presented.

Słowa kluczowe

EN

megamitochondrion; cell; mitochondrion; mitochondrial swelling; free radical; cytoplasm; apoptosis

• Wydawca: -
• Czasopismo: Acta Biochimica Polonica
• Rocznik: 1999
• Tom: 46
• Numer: 2
• Opis fizyczny: p.223-237,fig.

Twórcy

autor

Wakabayashi T.

• Nagoya University School of Medicine, 65, Tsurumai-cho, Showa-ku, Nagoya 466-8550, Japan, e-mail: [e-mail]

Bibliografia

• 1. Collins, M., Marbel, J., Malde, P. & Rivas, A. (1992) Interleukin 3 protects murine bone marrow cells from apoptosis induced by DNA damaging agents. J. Exp. Med. 176, 1043- 1051.
• 2. Bisonette, R.P., Echeverri, R.H., Mahboubi, A. & Green, D.R. (1992) Apoptotic cell death induced by c-mic is inhibited by bcl-2. Nature 359. 552-554.
• 3. Fanidi, A., Harrington, E.A. & Evans, G.I. (1992) Cooperative interaction between c-myc and bcl-2 proto-oncogenes. Nature 359. 554- 556.
• 4. Oliver, F.C., Marvel, J., Collins, M.K. & Lopez- Rivas, A. (1993) Bcl-2 oncogene protects a bone marrow-derived pre-B-cell line from 5'- fluor-2-deoxyuridine-induced apoptosis. Bio- chem. Biophys. Res. Commun. 194. 126-132.
• 5. Zhong, L.T., Sarafian, T„ Kane, D.J., Charles, A.C., Mah, S.P., Edward, R.H. & Bredesen, D.E. (1993) Bcl-2 inhibits death of central neu­ral cells induced by multiple agents. Proc. Natl Acad. Sci. U.S.A. 90, 4533-4537.
• 6. Lotem, J. & Sachs, L. (1993) Regulation by bcl- 2, c-myc, and p53 of susceptibility to induction of apoptosis by heat shock and cancer chemo­therapy compounds in differentiation-compe­tent and -defective myeloid leukemic cells. Cell Growth & Differ. 4, 41-47.
• 7. Slater, A.F.G., Nobel, C.S.I., Maellaro, E., Bustamante, J., Kimland, M. & Orrenius, S. (1995) Nitrone spin traps and a nitroxide anti­oxidant inhibit a common pathway of thymo­cyte apoptosis. Biochem. J. 306, 771-778.
• 8. Korsmeyer, S.J., Yin, X.M., Oltvai, Z.N., Veis- Novak, D.J. & Linette, G.P. (1995) Reactive oxygen species and the regulation of cell death by the Bcl-2 gene family. Biochim. Biophys. Acta 1271, 63-66.
• 9. Clearly, M.L. & Sklar, J. (1985) Nucleotide se­quence of a t(14:18) chromosomal breakpoint in follicular lymphoma and demonstration of a breakpoint-cluster region near a transcrip­tionally active locus on chromosome 18. Proc. Natl. Acad. Sci. U.S.A. 82. 7439-7443.
• 10. Miyashita, T. & Reed, J.C. (1992) Bcl-2 trans­fer increases relative resistance of S49.1 and WEHI7.2 lymphoid cells to cell death and DNA fragmentation induced by glucocorti­coids and multiple chemotherapeutic drugs. Cancer Res. 52. 5401-5411.
• 11. Hockenbery, D.M., Oltvai, Z.N., Yin, X.-M., Milliman, C.L. & Korsmeyer. S.J. (1993) Bcl-2 functions in an antioxidant pathway to pre­vent apoptosis. Cell 75, 241-251.
• 12. Newmeyer, D.D., Farschon, D.iM. & Reed, J.C. (1994) Cell-free apoptosis in Xenopus egg ex­tracts: Inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochon­dria. Cell 79, 353-364.
• 13.Srinivasula, S.M., Fernandes-Alnemri, T., Zangrilli, J., Robertson, N., Armstrong, R.C., Wang, L., Trapani, J.A., Tomaselli, K.J., Lit- wack, G. & Alnemri, E.S. (1996) The Ced-3/in- terleukin 1/? converting enzyme-like homolog Mch6 and the lamin-cleaving enzyme Mch2cr are substrates for the apoptotic mediator CPP32. J. Biol Chem. 271, 27099-27106.
• 14.Shimizu, S., Eguchei, Y., Kamiike, W., Mat- suda, H. & Tsujimoto, Y. (1996) Bcl-2 expres­sion prevents activation of the ICE protease cascade. Oncogene 12, 2251-2257.
• 15. Yang, J., Liu, X., Kim, C.N., Ibrado, A.M., Cai, J., Peng. T.I., Jones, D.P. & Wang. X. (1997) Prevention of apoptosis by Bcl-2: Release of cytochrome c from mitochondria blocked. Sci­ence 275. 1129-1132.
• 16. Kluck, R.M., Bossy-Wetzel, E., Green, D.R. & Newmeyer, D.D. (1997) The release of cyto­chrome c from mitochondria: A primary site for Bcl-2 regulation of apoptosis. Science 275. 1132-1136.
• 17. Zamzami, N., Marchetti, P., Castedo, M., Za- nin, C., Vayssiere, J.L., Petit. P.X. & Kroemer, G. (1995) Reduction in mitochondria potential constitutes an early irreversible step of pro­grammed lymphocyte. J. Exp. Med. 181, 1661-1672.
• 18. Zamzami, N., Marchetti, P., Castedo. M., De- caudin, D., Macho, A., Hirsch, T., Susin. S.-A., Petit, P.X., Mignotte, B. & Kroemer, G. (1995) Sequential reduction of mitochondrial trans­membrane potential and generation of reac­tive oxygen species in early programmed cell death. J. Exp. Med. 182. 367-377.
• 19. Zamzami, N., Susin, S.A., Marechetti, T., Hirsch, T., Castedo. M. & Kroemer. G. (1996) Mitochondrial control of nuclear apoptosis. J. Exp. Med. 183, 1533-1544.
• 20. Petit, P.X., Susin, S.A., Zamzami. N., Mign­otte, B. & Kroemer, G. (1996) Mitochondria and programmed cell death: Back to the fu­ture. FEBS Lett. 396. 7-13.
• 21. Kane, D.J., Sarafian, T.A., Anton, R., Hahn, H., Gralla, E.B., Valentine, J.S., Ord, T. & Bre- desen, D.E. (1993) Bcl-2 inhibition of neural death: Decreased generation of reactive oxy­gen species. Science 262, 1274-1277.
• 22. Gimeno, A., Trueba, J.L., Blanco, M. & Gosal- vez, M. (1973) Mitochondrial functions in five cases of human neuromuscular disorders. J. Neurol Neurosurg. Psychiat. 36, 806-812.
• 23. Worsfold, M., Park, D.C. & Pennington, R.J. (1973) Familial "mitochondrial" myopathy. A myopathy associated with disordered oxida­tive metabolism in muscle fibers. 2. Biochemi­cal findings. J. Neurol. Sci. 19, 261-274.
• 24. Cederbaum, A.I., Lieber, C.S. & Rubin, E. (1974) Unexpected oxidation of a nitroxide al­cohol with m-chlorobenzoic acid. Arch. Bio- chem. Biophys. 165, 560-569.
• 25.Schotland, D.L., DiMauro, S., Bonilla, E., Scarpa, A. & Lee, C.-P. (1976) Neuromuscular disorder associated with a defect in mitochon­drial energy supply. Arch. Neurol. 33, 475- 479.
• 26. DiMauro, S., Bonilla, E.. Lee, C.-P., Schatland, D.L., Scarpa, A., Conn, H., Jr. & Chance, B. (1976) Luft's disease. Further biochemical and ultrastructural studies of skeletal muscle in the second case. J. Neurol. Sci. 27, 217- 232.
• 27. Wakabayashi, T., Asano, M. & Kawamoto, S. (1979) Induction of megamitochondria in the mouse liver by isonicotinic acid derivatives. Exp. Mol Pathol 31, 387-399.
• 28. Wakabayashi, T., Horiuchi, M., Sakaguchi, M., Onda, H. & Misawa, K. (1983) Induction of megamitochondria in the mouse and rat livers by hydrazine. Exp. Mol Pathol 39, 139-153.
• 29. Wakabayashi, T., Horiuchi, M., Sakaguchi, M., Misawa, K., Onda, H., Iijima, M. & All- mann, D.W. (1984) Mechanism of hepatic me­gamitochondria formation by ammonia de­rivatives. Correlation between structure of chemicals and their ability to induce the for­mation of megamitochondria. Eur. J. Bio- chem. 143, 455-465.
• 30. Wakabayashi, T., Adachi, K. & Popinigis, J. (1991) Effects of alkyl alcohols and related chemicals on rat liver structure and function. I. Induction of two distinct types of megamito­chondria. Acta Pathol Jpn. 41, 405-413.
• 31. Matsuhashi, T., Liu, X.-R., Usukura, J., Wozniak, M. & Wakabayashi, T. (1996) Mechanism of the formation of megamito­chondria in the mouse liver induced by chlo­ramphenicol. Toxicol Lett. 86, 47-54.
• 32. Wakabayashi. T., Yamashita, K., Adachi, K., Kawai, K., Iijima, M., Gekko, K., Tsudzuki, T., Popinigis, J. & Momota, M. (1987) Changes in physicochemical properties of mitochondria membranes during the formation process of megamitochondria induced by hydrazine. Toxicol Appl Pharmacol 87, 235-248.
• 33. Adachi, K., Wakabayashi, T. & Popinigis, J. (1991) Effects of alkyl alcohols and related chemicals on rat liver structure and function. II. Some biochemical properties of ethanol-, propanol- and butanol-treated rat liver mito­chondria. Acta Pathol Jpn. 41, 414-427.
• 34. Adachi, K., Momota, Y., Teranishi, Y., Ueki, R., Hagiwara, T. & Wakabayashi, T. (1992) Ef­fects of alkyl alcohols arid related chemicals on rat liver structure and function. III. Physi­cochemical properties of ethanol-, propanol- and butanol-treated rat liver mitochondria membrane. Acta Pathol Jpn. 42, 544-557.
• 35. Adachi, K., Matsuhashi, T., Nishizawa, Y., Usukura, J., Momota, M., Popinigis, J. & Wakabayashi, T. (1994) Further studies on physicochemical properties of mitochondrial membranes during the formation process of megamitochondria in the rat livers by hydra­zine. Exp. Mol Pathol 61, 134-151.
• 36. Matsuhashi, T., Karbowski, M., Liu, X.-R.. Usukura, J., Nishizawa, Y., Wozniak, M. & Wakabayashi, T. (1998) Complete suppres­sion of ethanol-induced formation of megami­tochondria by 4-hydroxy-2,2,6,6-tetramethyl-piperidine-l-oxyl (4-OH-TEMPO). Free Radical RioL Méd. 24, 139-147.
• 37. Matsuhashi, T., Liu, X.-R., Nishizawa, Y., Kar- bowski, M., Antosiewicz, J. & Wakabayashi, T. (1997) Role of free radicals in the mecha­nism of the hydrazine-induced formation of megamitochondria. Free Radical Biol Med. 23. 285-293.
• 38. Antosiewicz, J.. Nishizawa, Y., Liu. X.-R., Usu- kura, J. & Wakabayashi, T. (1994) Suppres­sion of the hydrazine-induced formation of megamitochondria in the rat liver by a-to- copherol. Exp. Mol Pathol 60, 173-187.
• 39. Adachi, K., Matsuhashi, T., Nishizawa, Y., Usukura, J., Popinigis, J. & Wakabayashi, T. (1995) Suppression of the hydrazine-induced formation of megamitochondria in the rat liver by CoQ10 Toxicol. Pathol. 23, 667-676.
• 40. Matsuhashi, T., Karbowski. M., Liu, X.-R, Usu­kura, J., Wozniak, M. & Wakabayashi. T. (1998) Complete suppression of ethanol-in- duced formation of megamitochondria by 4- hydroxy-2,2,6,6-tetramethvlpiperidine-l-oxyl (4-OH-TEMPO). Free Radical Biol Med. 24. 139-147.
• 41. Wakabayashi. T., Adachi, K., Matsuhashi, T., Wozniak, M., Antosiewicz, J. & Karbowski. M. (1997) Suppression of the formation of me­gamitochondria by scavengers for free radi­cals. Molec. Aspects Med. 18 (Suppl.) s5l- s61.
• 42. Karbowski, M., Kurono. C., Nishizawa, Y. & Wakabayashi, T. (1997) Induction of megami­tochondria by some chemicals inducing oxida­tive stress in primary cultured rat hepato- cytes. Biochim. Biophys. Acta 1349. 242-250.
• 43. Karbowski, M., Kurono, C.. Wozniak, M., Os- trowski, M., Teranishi, M., Soji, T. & Waka­bayashi, T. (1999) Cycloheximide and 4-OH- TEMPO suppress chloramphenicol-induced apoptosis in RL-34 cells via the suppression of the formation of megamitochondria. Biochim. Biophys. Acta 1449, 25-40.
• 44. Bernstein. J.D. & Pennial, R. (1978) Effects of chronic ethanol treatment upon rat liver mito­chondria. Biochem. Pharmacol. 27. 2337- 2342.
• 45. Wakabayashi, T. & Green, D.E. (1974) On the mechanism of cuprizone-induced formation of megamitochondria. Bioenergetics6. 179-192.
• 46. Wakabayashi, T., Horiuchi, M., Sakaguchi, M., Onda, H. & Misawa, K. (1983) Induction of megamitochondria in the mouse and rat livers by hydrazine. Exp. Mol Pathol 39,139-153.
• 47. Thayer, W.S. (1987) Effects of ethanol on pro­teins of mitochondrial membranes. Ann. N.Y. Acad. Sei. 492, 193-206.
• 48. Quintaniella, M.E. & Tampier, L. (1971) Etha­nol intake effect on liver and brain mitochon­drial function and acetaldehyde oxidation. Al­coholism 9, 375-380.
• 49. Adachi, K.. Matsuhashi. T., Nishizawa, Y., Usukura, J., Popinigis, S. & Wakabayashi, T. (1995) Studies on urea synthesis in the liver of rats treated chronically with ethanol using perfused livers, isolated hepatocytes and mito­chondria. Biochem. Pharmacol 50, 1391- 1399.
• 50. McConnell, S.J., Stewart. L.C., Talin, A. & Yaffe, M.P. (1990) Temperature-sensitive yeast mutants defective in mitochondrial in­heritance. J. Cell Biol 111, 967-976.
• 51. McConnell, S.J. & Yaffe, M.P. (1992) Nuclear and mitochondrial inheritance in yeast de­pends on novel cytoplasmic structures defined by MDM1 protein. J. Cell Biol 118. 385-395.
• 52. Jones, B.A. & Fangman, W.L. (1992) Mito­chondrial DNA maintenance in yeast requires a protein containing a region related to the GTP-binding domain of dynamin. Genes Dev. 6, 380-389.
• 53. Guan, K., Fahr. L., Marshall, T.K. & Des- cenes, R.J. (1993) Normal mitochondrial structure and genome maintenance in yeast requires the dynamin-like product of the MGM1 gene. Curr. Genet. 24, 141-148.
• 54.Sogo, L.F. & Yaffe, M.P. (1994) Regulation of mitochondrial morphology and inheritance by MdmlOp, a protein of the mitochondrial outer membrane. J. Cell BiolL 126, 385-395.
• 55. Burgess, S.M., Delannoy, M. & Jensen, R.E. (1994) MMMl encodes a mitochondrial outer membrane protein essential for establishing and maintaining the structure of yeast mito­chondria. J. Cell Biol. 126, 1375-1391.
• 56. Hermann, G.T., King, E.J. & Shaw, J.M. (1997) The yeast gene, MDM20, is necessary for mitochondrial inheritance and organiza­tion of the actin cytoskeleton. J. Cell Biol. 137, 141-153.
• 57. Hales, K.G. & Fuller, M.T. (1997) Develop- mentally regulated mitochondrial fusion me­diated by a conserved, novel, predicted GTPase. Cell 90. 121-129.
• 58. Berger, K.H., Sogo. L.F. & Yaffe, M.P. (1997) Mdml2p, a component required for mitochon­drial inheritance that is conserved between budding and fission yeast J. Cell Biol. 136, 545-553.
• 59.Boldogh, I., Vojtov, N., Karmon, S. & Pon, L.A. (1998) Interaction between mitochondria and the actin cytoskeleton in budding yeast re­quires two integral mitochondrial outer mem­brane proteins Mmmlp and MdmlOp. J. Cell Biol. 141, 1371-1381.
• 60.0tsuga, D., Keegan, B.R., Brisch, E., That­cher, J.W., Hermann, G.J., Bleazard, W. & Shaw, J.M. (1998) The dynamin-related GTPase, Dnmlp, controls mitochondrial mor­phology in yeast. J. Cell Biol. 143. 333-349.
• 61.Smirnova, E., Shurland, D.-L., Ryazantsev, S.N. & van den Bliek, A.M. (1998) A human dynamin-related protein controls the distribu­tion of mitochondria. J. Cell Biol. 143. 351-358.
• 62. Hermann, G.T., Thatcher, J.W., Mills, J.P., Hales, K.G., Fuller, M.T., Nunnari, J. & Shaw, J.M. (1998) Mitochondrial function in yeast requires the transmembrane GTPase Fzolp. J. Cell Biol. 143. 359-373.