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The Journal of Neuroscience, May 15, 1998, 18(10):3659-3668

Activation and Cleavage of Caspase-3 in Apoptosis Induced by Experimental Cerebral Ischemia

Shobu Namura¹, Jinmin Zhu¹, Klaus Fink¹, Matthias Endres¹, Anu Srinivasan², Kevin J. Tomaselli², Junying Yuan³, and Michael A. Moskowitz¹

¹ Stroke and Neurovascular Regulation, Neurosurgical Service, Departments of Surgery and Neurology, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts 02129, ² IDUN Pharmaceuticals, Inc., La Jolla, California 92037, and ³ Department of Cell Biology, Harvard Medical School, Boston, Massachusetts 02115

We examined the expression, activation, and cellular localization of caspase-3 (CPP32) using immunohistochemistry, immunoblots, and cleavage of the fluorogenic substrate N-benzyloxycarbonyl-Asp-Glu-Val-Asp-7-amino-4-trifluoromethyl coumarin (zDEVD-afc) in adult mouse brain after temporary (2 hr) middle cerebral artery occlusion produced by filament insertion into the carotid artery. Immunoreactive caspase-3p32 but not its cleavage product caspase-3p20 was constitutively expressed in neurons throughout brain and was most prominent in neuronal perikarya within piriform cortex. Caspase-like enzyme activity was elevated in brain homogenate 0-3 hr after reperfusion and reached a peak within 30 to 60 min. Caspase-3p20 immunoreactivity became prominent in neuronal perikarya within the middle cerebral artery territory at the time of reperfusion and on immunoblots 1-12 hr later. DNA laddering (agarose gels) and terminal deoxynucleotidyl transferase-mediated dUTPbiotin nick-end labeling (TUNEL)-stained cells were detected 6-24 hr after reperfusion. At 12-24 hr, immunoreactive p20 was visualized in TUNEL-positive cells, a finding also observed in apoptotic mouse cerebellar granule cells on postnatal day 5. Together, these observations suggest the existence of a time-dependent evolution of ischemic injury characterized by the close correspondence between caspase-like enzyme activation and an associated increase in immunoreactive product (caspase-3p20) beginning at or before reperfusion and followed several hours later by morphological and biochemical features of apoptosis.

Key words: ischemia; caspase; CED-3/ICE proteases; mouse brain; apoptosis; caspase-3 cleavage; caspase-like enzyme activity; TUNEL; CNS development

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Copyright © 1998 Society for Neuroscience  0270-6474/98/18103659-10$05.00/0

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				J. T. Finn, M. Weil, F. Archer, R. Siman, A. Srinivasan, and M. C. Raff Evidence That Wallerian Degeneration and Localized Axon Degeneration Induced by Local Neurotrophin Deprivation Do Not Involve Caspases J. Neurosci., February 15, 2000; 20(4): 1333 - 1341. [Abstract] [Full Text] [PDF]

				F. Selimi, M. Doughty, N. Delhaye-Bouchaud, and J. Mariani Target-Related and Intrinsic Neuronal Death in Lurcher Mutant Mice Are Both Mediated by Caspase-3 Activation J. Neurosci., February 1, 2000; 20(3): 992 - 1000. [Abstract] [Full Text] [PDF]

				J. A. Connor and R. J. Cormier Cumulative Effects of Glutamate Microstimulation on Ca2+ Responses of CA1 Hippocampal Pyramidal Neurons in Slice J Neurophysiol, January 1, 2000; 83(1): 90 - 98. [Abstract] [Full Text] [PDF]

				D. G. Nicholls and S. L. Budd Mitochondria and Neuronal Survival Physiol Rev, January 1, 2000; 80(1): 315 - 360. [Abstract] [Full Text] [PDF]

				H. Li, F. Colbourne, P. Sun, Z. Zhao, A. M. Buchan, and C. Iadecola Caspase Inhibitors Reduce Neuronal Injury After Focal but Not Global Cerebral Ischemia in Rats Editorial Comment Stroke, January 1, 2000; 31(1): 176 - 182. [Abstract] [Full Text] [PDF]

				L. Lang-Lazdunski, K. Matsushita, L. Hirt, C. Waeber, J.-P. G. Vonsattel, M. A. Moskowitz, and W. D. Dietrich Spinal Cord Ischemia : Development of a Model in the Mouse Editorial Comment: Development of a Model in the Mouse Stroke, January 1, 2000; 31(1): 208 - 213. [Abstract] [Full Text] [PDF]

				M. Fujimura, Y. Morita-Fujimura, P. Narasimhan, J.-C. Copin, M. Kawase, P. H. Chan, and C. Y. Hsu Copper-Zinc Superoxide Dismutase Prevents the Early Decrease of Apurinic/Apyrimidinic Endonuclease and Subsequent DNA Fragmentation After Transient Focal Cerebral Ischemia in Mice • Editorial Comment Stroke, November 1, 1999; 30(11): 2408 - 2415. [Abstract] [Full Text] [PDF]

				M. Fujimura, Y. Morita-Fujimura, T. Sugawara, P. H. Chan, and C. Y. Hsu Early Decrease of XRCC1, a DNA Base Excision Repair Protein, May Contribute to DNA Fragmentation After Transient Focal Cerebral Ischemia in Mice • Editorial Comment Stroke, November 1, 1999; 30(11): 2456 - 2463. [Abstract] [Full Text] [PDF]

				G. Tezel and M. B. Wax Inhibition of Caspase Activity in Retinal Cell Apoptosis Induced by Various Stimuli In Vitro Invest. Ophthalmol. Vis. Sci., October 1, 1999; 40(11): 2660 - 2667. [Abstract] [Full Text] [PDF]

				J. W. ALLEN, S. M. KNOBLACH, and A. I. FADEN Combined mechanical trauma and metabolic impairment in vitro induces NMDA receptor-dependent neuronal cell death and caspase-3-dependent apoptosis FASEB J, October 1, 1999; 13(13): 1875 - 1882. [Abstract] [Full Text]

				P. Lipton Ischemic Cell Death in Brain Neurons Physiol Rev, October 1, 1999; 79(4): 1431 - 1568. [Abstract] [Full Text] [PDF]

				H. Ueda, J.M. Levine, R.H. Miller, and B.D. Trapp Rat Optic Nerve Oligodendrocytes Develop in the Absence of Viable Retinal Ganglion Cell Axons J. Cell Biol., September 20, 1999; 146(6): 1365 - 1374. [Abstract] [Full Text] [PDF]

				G. V. Putcha, M. Deshmukh, and E. M. Johnson Jr BAX Translocation Is a Critical Event in Neuronal Apoptosis: Regulation by Neuroprotectants, BCL-2, and Caspases J. Neurosci., September 1, 1999; 19(17): 7476 - 7485. [Abstract] [Full Text] [PDF]

				T. Uetsuki, K. Takemoto, I. Nishimura, M. Okamoto, M. Niinobe, T. Momoi, M. Miura, and K. Yoshikawa Activation of Neuronal Caspase-3 by Intracellular Accumulation of Wild-Type Alzheimer Amyloid Precursor Protein J. Neurosci., August 15, 1999; 19(16): 6955 - 6964. [Abstract] [Full Text] [PDF]

				D. B. Dubal, P. J. Shughrue, M. E. Wilson, I. Merchenthaler, and P. M. Wise Estradiol Modulates bcl-2 in Cerebral Ischemia: A Potential Role for Estrogen Receptors J. Neurosci., August 1, 1999; 19(15): 6385 - 6393. [Abstract] [Full Text] [PDF]

				J. J. Velier, J. A. Ellison, K. K. Kikly, P. A. Spera, F. C. Barone, and G. Z. Feuerstein Caspase-8 and Caspase-3 Are Expressed by Different Populations of Cortical Neurons Undergoing Delayed Cell Death after Focal Stroke in the Rat J. Neurosci., July 15, 1999; 19(14): 5932 - 5941. [Abstract] [Full Text] [PDF]

				D. A. Shackelford, T. Tobaru, S. Zhang, and J. A. Zivin Changes in Expression of the DNA Repair Protein Complex DNA-Dependent Protein Kinase after Ischemia and Reperfusion J. Neurosci., June 15, 1999; 19(12): 4727 - 4738. [Abstract] [Full Text] [PDF]

				C. Liu, Y. Li, M. Peng, A. M. Laties, and R. Wen Activation of Caspase-3 in the Retina of Transgenic Rats with the Rhodopsin Mutation S334ter during Photoreceptor Degeneration J. Neurosci., June 15, 1999; 19(12): 4778 - 4785. [Abstract] [Full Text] [PDF]

				D. Xu, Y. Bureau, D. C. McIntyre, D. W. Nicholson, P. Liston, Y. Zhu, W. G. Fong, S. J. Crocker, R. G. Korneluk, and G. S. Robertson Attenuation of Ischemia-Induced Cellular and Behavioral Deficits by X Chromosome-Linked Inhibitor of Apoptosis Protein Overexpression in the Rat Hippocampus J. Neurosci., June 15, 1999; 19(12): 5026 - 5033. [Abstract] [Full Text] [PDF]

				M. Fujimura, Y. Morita-Fujimura, M. Kawase, J.-C. Copin, B. Calagui, C. J. Epstein, and P. H. Chan Manganese Superoxide Dismutase Mediates the Early Release of Mitochondrial Cytochrome C and Subsequent DNA Fragmentation after Permanent Focal Cerebral Ischemia in Mice J. Neurosci., May 1, 1999; 19(9): 3414 - 3422. [Abstract] [Full Text] [PDF]

				M. D. Johnson, Y. Kinoshita, H. Xiang, S. Ghatan, and R. S. Morrison Contribution of p53-Dependent Caspase Activation to Neuronal Cell Death Declines with Neuronal Maturation J. Neurosci., April 15, 1999; 19(8): 2996 - 3006. [Abstract] [Full Text] [PDF]

				C. Gu, P. Casaccia-Bonnefil, A. Srinivasan, and M. V. Chao Oligodendrocyte Apoptosis Mediated by Caspase Activation J. Neurosci., April 15, 1999; 19(8): 3043 - 3049. [Abstract] [Full Text] [PDF]

				C. M. Coopersmith, D. O'Donnell, and J. I. Gordon Bcl-2 inhibits ischemia-reperfusion-induced apoptosis in the intestinal epithelium of transgenic mice Am J Physiol Gastrointest Liver Physiol, March 1, 1999; 276(3): G677 - G686. [Abstract] [Full Text] [PDF]

				C. Iadecola, C. A. Salkowski, F. Zhang, T. Aber, M. Nagayama, S. N. Vogel, and M. Elizabeth Ross The Transcription Factor Interferon Regulatory Factor 1 Is Expressed after Cerebral Ischemia and Contributes to Ischemic Brain Injury J. Exp. Med., February 15, 1999; 189(4): 719 - 727. [Abstract] [Full Text] [PDF]

				S. Cho, B. T. Volpe, Y. Bae, O. Hwang, H. J. Choi, J. Gal, L. C. H. Park, C. K. Chu, J. Du, and T. H. Joh Blockade of Tetrahydrobiopterin Synthesis Protects Neurons after Transient Forebrain Ischemia in Rat: A Novel Role for the Cofactor J. Neurosci., February 1, 1999; 19(3): 878 - 889. [Abstract] [Full Text] [PDF]

				M. Kawase, M. Fujimura, Y. Morita-Fujimura, P. H. Chan, and C. Iadecola Reduction of Apurinic/Apyrimidinic Endonuclease Expression After Transient Global Cerebral Ischemia in Rats : Implication of the Failure of DNA Repair in Neuronal Apoptosis • Editorial Comment: Implication of the Failure of DNA Repair in Neuronal Apoptosis Stroke, February 1, 1999; 30(2): 441 - 449. [Abstract] [Full Text] [PDF]

				K. L. Moulder, O. Onodera, J. R. Burke, W. J. Strittmatter, and E. M. Johnson Jr Generation of Neuronal Intranuclear Inclusions by Polyglutamine-GFP: Analysis of Inclusion Clearance and Toxicity as a Function of Polyglutamine Length J. Neurosci., January 15, 1999; 19(2): 705 - 715. [Abstract] [Full Text] [PDF]

				H. Borges and R Linden Gamma irradiation leads to two waves of apoptosis in distinct cell populations of the retina of newborn rats J. Cell Sci., January 12, 1999; 112(23): 4315 - 4324. [Abstract] [PDF]

				M. J. O'Hare, S. T. Hou, E. J. Morris, S. P. Cregan, Q. Xu, R. S. Slack, and D. S. Park Induction and Modulation of Cerebellar Granule Neuron Death by E2F-1 J. Biol. Chem., August 11, 2000; 275(33): 25358 - 25364. [Abstract] [Full Text] [PDF]

				K. Blomgren, C. Zhu, X. Wang, J.-O. Karlsson, A.-L. Leverin, B. A. Bahr, C. Mallard, and H. Hagberg Synergistic Activation of Caspase-3 by m-Calpain after Neonatal Hypoxia-Ischemia. A MECHANISM OF "PATHOLOGICAL APOPTOSIS"? J. Biol. Chem., March 23, 2001; 276(13): 10191 - 10198. [Abstract] [Full Text] [PDF]

				S. Namura, K. Iihara, S. Takami, I. Nagata, H. Kikuchi, K. Matsushita, M. A. Moskowitz, J. V. Bonventre, and A. Alessandrini Intravenous administration of MEK inhibitor U0126 affords brain protection against forebrain ischemia and focal cerebral ischemia PNAS, September 25, 2001; 98(20): 11569 - 11574. [Abstract] [Full Text] [PDF]

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