Bcl-2-linked apoptosis due to increase in NO synthase in brain of SAMP10

Biochemical and Biophysical Research Communications

Volumn 297, Issue 3, 2002, Pages 517-522

  Numata, Takuya ^a   Saito, Takeshi ^b   Maekawa, Kazuyo ^b   Takahashi, Yasumitsu ^c   Saitoh, Hiroshi ^c   Hosokawa, Toshiyuki ^a   Fujita, Hiroyoshi ^b   Kurasaki, Masaaki ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c HEALTH SCIENCES UNIVERSITY OF HOKKAIDO   (Japan)

Author keywords

Aging; Apoptosis; Bcl 2; Brain; Cytochrome c; nNOS; NO; SAMP10; Senescence acceleration; TUNEL

Indexed keywords

CYTOCHROME C; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PROTEIN BCL 2; PROTEIN P53;

AGED; AGING; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CORTEX; BRAIN LEVEL; CONTROLLED STUDY; CYTOSOL; MALE; MOUSE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AGING; ANIMALS; APOPTOSIS; BRAIN; CEREBRAL CORTEX; CYTOCHROME C GROUP; MALE; MICE; MICE, MUTANT STRAINS; MICROSCOPY, CONFOCAL; MITOCHONDRIA; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE I; PROTO-ONCOGENE PROTEINS C-BCL-2; REFERENCE VALUES;

EID: 0036389727     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-291X(02)02155-1     Document Type: Article

References (44)

1. C.A. Barnes, Normal aging: Regionally specific changes in hippocampal synaptic transmission, Trends Neurosci. 17 (1994) 13-18.
2. T. Takeda, M. Hosokawa, S. Takeshita, M. Irino, K. Higuchi, T. Matsushita, Y. Tomita, K. Yasuhira, H. Hamamoto, K. Shimizu, M. Ishii, T. Yamamuro, A new murine model of accelerated senescence, Mech. Ageing Dev. 17 (1981) 183-194.
3. T. Takeda, T. Matsushita, M. Kurozumi, K. Takemura, K. Higuchi, M. Hosokawa, Pathobiology of the senescence-accelerated mouse (SAM), Exp. Gerontol. 32 (1997) 117-127.
4. A. Shimada, A. Ohta, I. Akiguchi, T. Takeda, Age-related deterioration in conditional avoidance task in the SAM-P/10 mouse, an animal model of spontaneous brain atrophy, Brain Res. 608 (1993) 266-272.
5. T. Saito, K. Takahashi, N. Nakagawa, T. Hosokawa, M. Kurasaki, O. Yamanoshita, Y. Yamamoto, H. Sasaki, K. Nagashima, H. Fujita, Deficiencies of hippocampal Zn and ZnT3 accelerate brain aging of rat, Biochem. Biophys. Res. Commun. 279 (2000) 505-511.
6. J.W. Johnson, P. Ascher, Glycine potentiates the NMDA response in cultured mouse brain neurons, Nature 325 (1987) 529-531.
7. S. Moncada, R.M. Palmer, E.A. Higgs, Nitric oxide: physiology, pathophysiology, and pharmacology, Pharmacol. Rev. 43 (1991) 109-142.
8. U. Forstermann, H.H.H.W. Schmidt, J.S. Pollock, H. Sheng, J.A. Mitchell, T.D. Warner, F. Murad, Isoforms of nitric oxide synthase. Characterization and purification from different cell types, Biochem. Pharmacol. 42 (1990) 1849-1857.
9. J.S. Pollock, U. Forstermann, J.A. Mitchell, T.D. Warner, H.H.H.W. Schmidt, M. Nakane, F. Murad, Purification and characterization of particulate endothelium-derived relaxing factor synthase from cultured and native bovine aortic endothelial cells, Proc. Natl. Acad. Sci. USA 88 (1991) 10480-10484.
10. S. Moncada, A. Higgs, The L-arginine-nitric oxide pathway, N. Engl. J. Med. 30 (1993) 2002-2011.
11. L.O. Uttenthal, D. Alonso, A.P. Fernandez, R.O. Cambell, M.A. Moro, J.C. Leza, I. Lizasoain, F.J. Esteban, J.B. Barroso, R. Valderrama, J.A. Pedorosa, M.A. Peinado, J. Serrano, A. Richart, M.L. Bentura, M. Santacana, R. Martinez-Murillo, J. Rodrigo, Neuronal and inducible nitric oxide synthase and nitrotyrosine immunoreactivities in the cerebral cortex of the aging rat, Microsc. Res. Tech. 43 (1998) 75-88.
12. B. van der Loo, R. Labugger, J.N. Skepper, M. Bachschmid, J. Kilo, J.M. Powell, M. Palacios-Callender, J.D. Erusalimsky, T. Quaschning, T. Malinsky, D. Gygi, V. Ullrich, T.F. Luscher, Enhanced Peroxynitrite formation is associated with vascular aging, J. Exp. Med. 192 (2000) 1731-1743.
13. J. Garthwaite, C.L. Boulton, Nitric oxide signaling in the central nervous system, Annu. Rev. Physiol. 57 (1995) 683-706.
14. C. Szabo, Physiological and pathophysiological roles of nitric oxide in the central nervous system, Brain Res. Bull. 41 (1996) 131-141.
15. V.L. Dawson, T.M. Dawson, Nitric oxide neurotoxicity, Chem. Neuroanat. 10 (1996) 179-190.
16. U.K. Messmer, B. Brune, Nitric oxide (NO) in apoptotic versus necrotic RAW 264.7 macrophage cell death: the role of NO-donor exposure, NAD+ content, and p53 accumulation, Arch. Biochem. Biophys. 327 (1996) 1-10.
17. M.P. Murphy, Nitric oxide and cell death, Biochim. Biophys. Acta 1411 (1999) 401-414.
18. A.Lopez-Farre, J.A.Rodriguez-Feo, L.Sanchez de Miguel, L.Rico, S. Casado, Role of nitric oxide in the control of apoptosis in the microvasculature, Int. J. Biochem. Cell Biol. 30 (1998) 1095-1106.
19. A.M. Davis, The Bcl-2 family of proteins, and the regulation of neuronal survival, Trends Neurosci. 18 (1995) 355-358.
20. G. Kroemer, The proto-oncogene Bcl-2 and its role in regulating apoptosis, Nat. Med. 3 (1997) 614-619.
21. Z. Oltvai, C.L. Milliman, S.J. Korsmeyer, Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death, Cell 74 (1993) 609-619.
22. C.D. Botner, N.B.E. Oldenburg, J.A. Cidlowski, The role of DNA fragmentation in apotosis, Trends Cell Biol. 5 (1995) 21-26.
23. B.A. Osborne, L.M. Schwartz, Essential genes that regulates apoptosis, Trends Cell Biol. 4 (1994) 399-403.
24. L.M. Schwartz, B.A. Osborne, Programmed cell death apoptosis and killer genes, Immunol. Today 14 (1993) 582-589.
25. M. Tamatani, S. Ogawa, Y. Niitsu, M. Tohyama, Involvement of Bcl-2 family and caspase-3-like protease in NO-mediated neuronal apoptosis, J. Neurochem. 71 (1998) 1588-1596.
26. M. Vega, L. Urrutia, G. Iniguez, F. Gabler, L. Devoto, M.C. Johnson, Nitric oxide induces apoptosis in the human corpus luteum, Mol. Hum. Reprod. 6 (2000) 681-687.
27. S. Hortelano, B. Dallaporta, N. Zamzami, T. Hirsch, S.A. Susin, Y. Marzo, L. Bosca, G. Kroemer, Nitric oxide induces apoptosis via triggering mitochondrial permeability transition, FEBS Lett. 410 (1997) 373-377.
28. S.P. Kantrow, C.A. Piantadosi, Release of cytochrome c from liver mitochondria during permeability transition, Biochem. Biophys. Res. Commun. 232 (1997) 669-671.
29. R.D. Palmiter, T.B. Cole, C.J. Quaife, S.D. Findley, ZnT-3, a putative transporter of zinc into synaptic vesicles, Proc. Natl. Acad. Sci. USA 93 (1996) 14934-14939.
30. L. Rossi, A. De Martino, E. Marchese, S. Piccirilli, G. Rotilio, M.R. Ciriolo, Neurodegeneration in the animal model of Menkes' disease involves Bcl-2-linked apoptosis, Neuroscience 103 (2001) 181-188.
31. M.M. Bradford, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem. 72 (1976) 248-254.
32. T. Hosokawa, M. Okabe, S. Saito, T. Saito, M. Kurasaki, Protective role of metallothionein on DNA damage in rat kidney caused by cis-diamminedichloroplatinum, Pharmacol. Toxicol. 86 (2000) 276-282.
33. K. Inada, I. Yokoi, H. Kabuto, H. Habu, A. Mori, N. Ogawa, Age-related increase in nitric oxide synthase activity in senescence-accelerated mouse brain and the effect of long-term administration of superoxide radical scavenger, Mech. Ageing Dev. 89 (1996) 95-102.
34. S.X. Ma, A.T. Holley, A. Sandra, M.D. Cassell, F.M. Abboud, Increased expression of nitric oxide synthase in the gracile nucleus of aged rats, Neuroscience 76 (1997) 659-663.
35. K. Yamada, Y. Noda, Y. Komori, H. Sugihara, T. Hasegawa, T. Nabeshima, Reduction in the number of NADPH-diaphorase-positive cells in the cerebral cortex and striatum in aged rats, Neurosci. Res. 24 (1996) 393-402.
36. B. Elibol, F. Soylemezoglu, I. Unal, M. Fujii, L. Hirt, P.L. Huang, M.A. Moskowitz, T. Dalkara, Nitric oxide is involved in ischemia-induced apoptosis in brain: A study in neuronal nitric oxide synthase null mice, Neuroscience 105 (2001) 79-86.
37. M. Lee, D.-H. Hyun, K.-A. Marshall, L.M. Ellerby, D.E. Bredesen, P. Jenner, B. Halliwell, Effect of overexpression of Bcl-2 on cellular oxidative damage, nitric oxide production, antioxidant defenses, and the proteasome, Free Rad. Biol. Med. 31(2001) 1550-1559.
38. R. Zamora, L. Alarcon, Y. Vodovotz, B. Betten, P.K.M. Kim, K.F. Gibson, T.R. Billiar, Nitric oxide suppresses the expression of Bcl-2-binding protein BNIP3 in hepatocytes, J. Biol. Chem. 276 (2001) 46887-46895.
39. C.S. Boyd, E. Cadenas, Nitric oxide and cell signaling pathways in mitochondrial-dependent apoptosis, Biol. Chem. 383 (2002) 411-423.
40. J. Yang, X. Liu, K. Bhalla, C.N. Kim, A.M. Ibrado, J. Cai, T.-I. Peng, D.P. Jones, X. Wang, Prevention of apoptosis by Bcl-2: release of cytochrome from mitochondria blocked, Science 275 (1997) 1129-1132.
41. M.D. Jacobson, M. Weil, M.C. Raff, Programmed cell death in animal development, Cell 88 (1997) 347-354.
42. G. Walkinshaw, C.M. Waters, Neurotoxin-induced cell death in neuronal PC12 cells is mediated by induction of apoptosis, Neuroscience 63 (1994) 975-987.
43. A. Shimada, A. Ohta, I. Akiguchi, T. Takeda, Inbred SAMP/10 as a mouse model of spontaneous inherited brain atrophy, J. Neuropathol. Exp. Neurol. 51 (1992) 440-450.
44. A. Shimada, Age-dependent cerebral atrophy and cognitive dysfunction in SAMP10 mice, Neurobiol. Aging 20 (1999) 125-136.