Apoptosis and Related Mechanisms in Cerebral Ischemia

Stroke

Volumn , Issue , 2011, Pages 107-121

  Dalkara, Turgay ^a   Moskowitz, Michael A ^b  

^a HACETTEPE UNIVERSITY   (Turkey)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84874743438     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-1-4160-5478-8.10007-7     Document Type: Chapter

References (225)

1. Dirnagl U., Iadecola C., Moskowitz M.A. Pathobiology of ischaemic stroke: An integrated view. Trends Neurosci 1999, 22:391-397.
2. Lipton P. Ischemic cell death in brain neurons. Physiol Rev 1999, 79:1431-1568.
3. Lo E.H., Dalkara T., Moskowitz M.A. Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 2003, 4:399-415.
4. Unal-Cevik I., Kilinc M., Can A., Gursoy-Ozdemir Y., Dalkara T. Apoptotic and necrotic death mechanisms are concomitantly activated in the same cell after cerebral ischemia. Stroke 2004, 35:2189-2194.
5. Degterev A., Huang Z., Boyce M., Li Y., Jagtap P., Mizushima N., Cuny G.D., Mitchison T.J., Moskowitz M.A., Yuan J. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol 2005, 1:112-119.
6. Graham S.H., Chen J. Programmed cell death in cerebral ischemia. J Cereb Blood Flow Metab 2001, 21:99-109.
7. Schulz J.B., Weller M., Moskowitz M.A. Caspases as treatment targets in stroke and neurodegenerative diseases. Ann Neurol 1999, 45:421-429.
8. Silva M.T. do Vale A, dos Santos NM: Secondary necrosis in multicellular animals: An outcome of apoptosis with pathogenic implications. Apoptosis 2008, 13:463-482.
9. Rami A., Langhagen A., Steiger S. Focal cerebral ischemia induces upregulation of beclin 1 and autophagy-like cell death. Neurobiol Dis 2008, 29:132-141.
10. Adhami F., Schloemer A., Kuan C.Y. The roles of autophagy in cerebral ischemia. Autophagy 2007, 3:42-44.
11. Cuervo A.M. Autophagy: In sickness and in health. Trends Cell Biol 2004, 14:70-77.
12. Puyal J., Vaslin A., Mottier V., Clarke P.G. Postischemic treatment of neonatal cerebral ischemia should target autophagy. Ann Neurol 2009, 66:378-389.
13. Ginet V., Puyal J., Clarke P.G., Truttmann A.C. Enhancement of autophagic flux after neonatal cerebral hypoxia-ischemia and its region-specific relationship to apoptotic mechanisms. Am J Pathol 2009, 175:1962-1974.
14. Gao Y., Liang W., Hu X., Zhang W., Stetler R.A., Vosler P., Cao G., Chen J. Neuroprotection against hypoxic-ischemic brain injury by inhibiting the apoptotic protease activating factor-1 pathway. Stroke 2010, 41:166-172.
15. Hu B.R., Liu C.L., Ouyang Y., Blomgren K., Siesjo B.K. Involvement of caspase-3 in cell death after hypoxia-ischemia declines during brain maturation. J Cereb Blood Flow Metab 2000, 20:1294-1300.
16. Hirsch T., Marchetti P., Susin S.A., Dallaporta B., Zamzami N., Marzo I., Geuskens M., Kroemer G. The apoptosis-necrosis paradox. Apoptogenic proteases activated after mitochondrial permeability transition determine the mode of cell death. Oncogene 1997, 15:1573-1581.
17. Martin L.J., Al-Abdulla N.A., Brambrink A.M., Kirsch J.R., Sieber F.E., Portera-Cailliau C. Neurodegeneration in excitotoxicity, global cerebral ischemia, and target deprivation: A perspective on the contributions of apoptosis and necrosis. Brain Res Bull 1998, 46:281-309.
18. Nicotera P., Leist M., Manzo L. Neuronal cell death: A demise with different shapes. Trends Pharmacol Sci 1999, 20:46-51.
19. MacManus J.P., Buchan A.M. Apoptosis after experimental stroke: Fact or fashion?. J Neurotrauma 2000, 17:899-914.
20. Syntichaki P., Tavernarakis N. The biochemistry of neuronal necrosis: Rogue biology?. Nat Rev Neurosci 2003, 4:672-684.
21. Degterev A., Yuan J. Expansion and evolution of cell death programmes. Nat Rev Mol Cell Biol 2008, 9:378-390.
22. Leist M., Jaattela M. Four deaths and a funeral: From caspases to alternative mechanisms. Nat Rev Mol Cell Biol 2001, 2:589-598.
23. Wang X. The expanding role of mitochondria in apoptosis. Genes Dev 2001, 15:2922-2933.
24. Kroemer G., Reed J.C. Mitochondrial control of cell death. Nat Med 2000, 6:513-519.
25. Fiskum G. Mitochondrial participation in ischemic and traumatic neural cell death. J Neurotrauma 2000, 17:843-855.
26. Hengartner M.O. The biochemistry of apoptosis. Nature 2000, 407:770-776.
27. Christofferson D.E., Yuan J. Necroptosis as an alternative form of programmed cell death. Curr Opin Cell Biol 2010, 22:263-268.
28. Budd R.C. Death receptors couple to both cell proliferation and apoptosis. J Clin Invest 2002, 109:437-441.
29. Zhang D.W., Shao J., Lin J., Zhang N., Lu B.J., Lin S.C., Dong M.Q., Han J. RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 2009, 325:332-336.
30. Gurer G., Gursoy-Ozdemir Y., Erdemli E., Can A., Dalkara T. Astrocytes are more resistant to focal cerebral ischemia than neurons and die by a delayed necrosis. Brain Pathol 2009, 19:630-641.
31. Kerr J.F., Wyllie A.H., Currie A.R. Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972, 26:239-257.
32. Majno G., Joris I. Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 1995, 146:3-15.
33. Wyllie A.H., Kerr J.F., Currie A.R. Cell death: The significance of apoptosis. Int Rev Cytol 1980, 68:251-306.
34. Benn S.C., Woolf C.J. Adult neuron survival strategies-slamming on the brakes. Nat Rev Neurosci 2004, 5:686-700.
35. 2+ exchanger in excitotoxicity. Cell 2005, 120:275-285.
36. Clarke P.G. Developmental cell death: Morphological diversity and multiple mechanisms. Anat Embryol (Berl) 1990, 181:195-213.
37. White E. Autophagic cell death unraveled: Pharmacological inhibition of apoptosis and autophagy enables necrosis. Autophagy 2008, 4:399-401.
38. Koike M., Shibata M., Tadakoshi M., Gotoh K., Komatsu M., Waguri S., Kawahara N., Kuida K., Nagata S., Kominami E., Tanaka K., Uchiyama Y. Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury. Am J Pathol 2008, 172:454-469.
39. Meier P., Finch A., Evan G. Apoptosis in development. Nature 2000, 407:796-801.
40. Renehan A.G., Bach S.P., Potten C.S. The relevance of apoptosis for cellular homeostasis and tumorigenesis in the intestine. Can J Gastroenterol 2001, 15:166-176.
41. Mattson M.P. Apoptosis in neurodegenerative disorders. Nat Rev Mol Cell Biol 2000, 1:120-129.
42. Yuan J., Yankner B.A. Apoptosis in the nervous system. Nature 2000, 407:802-809.
43. Metzstein M.M., Stanfield G.M., Horvitz H.R. Genetics of programmed cell death in C. elegans: Past, present and future. Trends Genet 1998, 14:410-416.
44. Yuan J.Y., Horvitz H.R. The Caenorhabditis elegans genes ced-3 and ced-4 act cell autonomously to cause programmed cell death. Dev Biol 1990, 138:33-41.
45. Yuan J., Shaham S., Ledoux S., Ellis H.M., Horvitz H.R. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 1993, 75:641-652.
46. Joza N., Kroemer G., Penninger J.M. Genetic analysis of the mammalian cell death machinery. Trends Genet 2002, 18:142-149.
47. Murphy A.N., Fiskum G., Beal M.F. Mitochondria in neurodegeneration: Bioenergetic function in cell life and death. J Cereb Blood Flow Metab 1999, 19:231-245.
48. Willis S.N., Adams J.M. Life in the balance: How BH3-only proteins induce apoptosis. Curr Opin Cell Biol 2005, 17:617-625.
49. Li H., Zhu H., Xu C.J., Yuan J. Cleavage of Bid by caspase 8 mediates the mitochondrial damage in the FAS pathway of apoptosis. Cell 1998, 94:491-501.
50. 2+-induced apoptosis through calcineurin dephosphorylation of Bad. Science 1999, 284:339-343.
51. Puthalakath H., Strasser A. Keeping killers on a tight leash: Transcriptional and post-translational control of the pro-apoptotic activity of BH3-only proteins. Cell Death Differ 2002, 9:505-512.
52. Zou H., Henzel W.J., Liu X., Lutschg A., Wang X. Apaf-1, a human protein homologous to C. elegans ced-4, participates in cytochrome c-dependent activation of caspase-3. Cell 1997, 90:405-413.
53. Stennicke H.R., Ryan C.A., Salvesen G.S. Reprieval from execution: The molecular basis of caspase inhibition. Trends Biochem Sci 2002, 27:94-101.
54. Susin S.A., Lorenzo H.K., Zamzami N., Marzo I., Snow B.E., Brothers G.M., Mangion J., Jacotot E., Costantini P., Loeffler M., Larochette N., Goodlett D.R., Aebersold R., Siderovski D.P., Penninger J.M., Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999, 397:441-446.
55. Cande C., Cohen I., Daugas E., Ravagnan L., Larochette N., Zamzami N., Kroemer G. Apoptosis-inducing factor (AIF): A novel caspase-independent death effector released from mitochondria. Biochimie 2002, 84:215-222.
56. Lorenzo H.K., Susin S.A., Penninger J., Kroemer G. Apoptosis inducing factor (AIF): A phylogenetically old, caspase-independent effector of cell death. Cell Death Differ 1999, 6:516-524.
57. Yu S.W., Wang H., Poitras M.F., Coombs C., Bowers W.J., Federoff H.J., Poirier G.G., Dawson T.M., Dawson V.L. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 2002, 297:259-263.
58. Cipriani G., Rapizzi E., Vannacci A., Rizzuto R., Moroni F., Chiarugi A. Nuclear poly(ADP-ribose) polymerase-1 rapidly triggers mitochondrial dysfunction. J Biol Chem 2005, 280:17227-17234.
59. Eguchi K. Apoptosis in autoimmune diseases. Intern Med 2001, 40:275-284.
60. Itoh N., Nagata S. A novel protein domain required for apoptosis. Mutational analysis of human FAS antigen. J Biol Chem 1993, 268:10932-10937.
61. Kischkel F.C., Hellbardt S., Behrmann I., Germer M., Pawlita M., Krammer P.H., Peter M.E. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J 1995, 14:5579-5588.
62. Medema J.P., Scaffidi C., Kischkel F.C., Shevchenko A., Mann M., Krammer P.H., Peter M.E. FLICE is activated by association with the CD95 death-inducing signaling complex (DISC). EMBO J 1997, 16:2794-2804.
63. Stennicke H.R., Jurgensmeier J.M., Shin H., Deveraux Q., Wolf B.B., Yang X., Zhou Q., Ellerby H.M., Ellerby L.M., Bredesen D., Green D.R., Reed J.C., Froelich C.J., Salvesen G.S. Pro-caspase-3 is a major physiologic target of caspase-8. J Biol Chem 1998, 273:27084-27090.
64. Luo X., Budihardjo I., Zou H., Slaughter C., Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 1998, 94:481-490.
65. Korsmeyer S.J., Wei M.C., Saito M., Weiler S., Oh K.J., Schlesinger P.H. Pro-apoptotic cascade activates BID, which oligomerizes BAK or BAX into pores that result in the release of cytochrome c. Cell Death Differ 2000, 7:1166-1173.
66. Wei M.C., Zong W.X., Cheng E.H., Lindsten T., Panoutsakopoulou V., Ross A.J., Roth K.A., MacGregor G.R., Thompson C.B., Korsmeyer S.J. Proapoptotic BAX and BAK: A requisite gateway to mitochondrial dysfunction and death. Science 2001, 292:727-730.
67. Slee E.A., Harte M.T., Kluck R.M., Wolf B.B., Casiano C.A., Newmeyer D.D., Wang H.G., Reed J.C., Nicholson D.W., Alnemri E.S., Green D.R., Martin S.J. Ordering the cytochrome c-initiated caspase cascade: Hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J Cell Biol 1999, 144:281-292.
68. Vercammen D., Brouckaert G., Denecker G., Van de Craen M., Declercq W., Fiers W., Vandenabeele P. Dual signaling of the Fas receptor: Initiation of both apoptotic and necrotic cell death pathways. J Exp Med 1998, 188:919-930.
69. Holler N., Zaru R., Micheau O., Thome M., Attinger A., Valitutti S., Bodmer J.L., Schneider P., Seed B., Tschopp J. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol 2000, 1:489-495.
70. Khwaja A., Tatton L. Resistance to the cytotoxic effects of tumor necrosis factor alpha can be overcome by inhibition of a FADD/caspase-dependent signaling pathway. J Biol Chem 1999, 274:36817-36823.
71. Rich T., Allen R.L., Wyllie A.H. Defying death after DNA damage. Nature 2000, 407:777-783.
72. Zhou B.B., Elledge S.J. The DNA damage response: Putting checkpoints in perspective. Nature 2000, 408:433-439.
73. Banin S., Moyal L., Shieh S., Taya Y., Anderson C.W., Chessa L., Smorodinsky N.I., Prives C., Reiss Y., Shiloh Y., Ziv Y. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 1998, 281:1674-1677.
74. Maya R., Balass M., Kim S.T., Shkedy D., Leal J.F., Shifman O., Moas M., Buschmann T., Ronai Z., Shiloh Y., Kastan M.B., Katzir E., Oren M. ATM-dependent phosphorylation of Mdm2 on serine 395: Role in p53 activation by DNA damage. Genes Dev 2001, 15:1067-1077.
75. Culmsee C., Mattson M.P. p53 in neuronal apoptosis. Biochem Biophys Res Commun 2005, 331:761-777.
76. Leist M., Single B., Kunstle G., Volbracht C., Hentze H., Nicotera P. Apoptosis in the absence of poly-(ADP-ribose) polymerase. Biochem Biophys Res Commun 1997, 233:518-522.
77. Ha H.C., Snyder S.H. Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc Natl Acad Sci U S A 1999, 96:13978-13982.
78. Chiarugi A. Poly(ADP-ribose) polymerase: Killer or conspirator? The 'suicide hypothesis' revisited. Trends Pharmacol Sci 2002, 23:122-129.
79. Chiarugi A., Moskowitz M.A. Cell biology. PARP-1-a perpetrator of apoptotic cell death?. Science 2002, 297:200-201.
80. Xu Y., Huang S., Liu Z.G., Han J. Poly(ADP-ribose) polymerase-1 signaling to mitochondria in necrotic cell death requires RIP1/TRAF2-mediated JNK1 activation. J Biol Chem 2006, 281:8788-8795.
81. Paschen W. Shutdown of translation: Lethal or protective? Unfolded protein response versus apoptosis. J Cereb Blood Flow Metab 2003, 23:773-779.
82. Nakagawa T., Zhu H., Morishima N., Li E., Xu J., Yankner B.A., Yuan J. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000, 403:98-103.
83. Morishima N., Nakanishi K., Takenouchi H., Shibata T., Yasuhiko Y. An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. J Biol Chem 2002, 277:34287-34294.
84. Rao R.V., Castro-Obregon S., Frankowski H., Schuler M., Stoka V., del Rio G., Bredesen D.E., Ellerby H.M. Coupling endoplasmic reticulum stress to the cell death program. An Apaf-1-independent intrinsic pathway. J Biol Chem 2002, 277:21836-21842.
85. Li H., Yuan J. Deciphering the pathways of life and death. Curr Opin Cell Biol 1999, 11:261-266.
86. Tamatani M., Che Y.H., Matsuzaki H., Ogawa S., Okado H., Miyake S., Mizuno T., Tohyama M. Tumor necrosis factor induces Bcl-2 and Bcl-x expression through NFkappaB activation in primary hippocampal neurons. J Biol Chem 1999, 274:8531-8538.
87. Datta S.R., Brunet A., Greenberg M.E. Cellular survival: A play in three Akts. Genes Dev 1999, 13:2905-2927.
88. Cardone M.H., Roy N., Stennicke H.R., Salvesen G.S., Franke T.F., Stanbridge E., Frisch S., Reed J.C. Regulation of cell death protease caspase-9 by phosphorylation. Science 1998, 282:1318-1321.
89. Datta S.R., Dudek H., Tao X., Masters S., Fu H., Gotoh Y., Greenberg M.E. Akt phosphorylation of Bad couples survival signals to the cell-intrinsic death machinery. Cell 1997, 91:231-241.
90. Bryckaert M., Guillonneau X., Hecquet C., Courtois Y., Mascarelli F. Both FGF1 and bcl-x synthesis are necessary for the reduction of apoptosis in retinal pigmented epithelial cells by FGF2: Role of the extracellular signal-regulated kinase 2. Oncogene 1999, 18:7584-7593.
91. Finkbeiner S. CREB couples neurotrophin signals to survival messages. Neuron 2000, 25:11-14.
92. Kaltschmidt B., Kaltschmidt C., Hofmann T.G., Hehner S.P., Droge W., Schmitz M.L. The pro- or anti-apoptotic function of NF-kappaB is determined by the nature of the apoptotic stimulus. Eur J Biochem 2000, 267:3828-3835.
93. 2+ concentration, and neurotoxicity and increase antioxidant enzyme activities in hippocampal neurons. J Neurochem 1995, 65:1740-1751.
94. Mattson M.P., Scheff S.W. Endogenous neuroprotection factors and traumatic brain injury: Mechanisms of action and implications for therapy. J Neurotrauma 1994, 11:3-33.
95. Saleh A., Srinivasula S.M., Balkir L., Robbins P.D., Alnemri E.S. Negative regulation of the Apaf-1 apoptosome by Hsp70. Nat Cell Biol 2000, 2:476-483.
96. Ravagnan L., Gurbuxani S., Susin S.A., Maisse C., Daugas E., Zamzami N., Mak T., Jaattela M., Penninger J.M., Garrido C., Kroemer G. Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nat Cell Biol 2001, 3:839-843.
97. Meriin A.B., Yaglom J.A., Gabai V.L., Zon L., Ganiatsas S., Mosser D.D., Sherman M.Y. Protein-damaging stresses activate c-Jun N-terminal kinase via inhibition of its dephosphorylation: A novel pathway controlled by HSP72. Mol Cell Biol 1999, 19:2547-2555.
98. Linnik M.D., Zobrist R.H., Hatfield M.D. Evidence supporting a role for programmed cell death in focal cerebral ischemia in rats. Stroke 1993, 24:2002-2008. discussion 2008-2009.
99. Krajewski S., Mai J.K., Krajewska M., Sikorska M., Mossakowski M.J., Reed J.C. Upregulation of bax protein levels in neurons following cerebral ischemia. J Neurosci 1995, 15:6364-6376.
100. Li Y., Chopp M., Jiang N., Yao F., Zaloga C. Temporal profile of in situ DNA fragmentation after transient middle cerebral artery occlusion in the rat. J Cereb Blood Flow Metab 1995, 15:389-397.
101. Charriaut-Marlangue C., Margaill I., Represa A., Popovici T., Plotkine M., Ben-Ari Y. Apoptosis and necrosis after reversible focal ischemia: An in situ DNA fragmentation analysis. J Cereb Blood Flow Metab 1996, 16:186-194.
102. Chen J., Zhu R.L., Nakayama M., Kawaguchi K., Jin K., Stetler R.A., Simon R.P., Graham S.H. Expression of the apoptosis-effector gene, Bax, is up-regulated in vulnerable hippocampal CA1 neurons following global ischemia. J Neurochem 1996, 67:64-71.
103. Colbourne F., Sutherland G.R., Auer R.N. Electron microscopic evidence against apoptosis as the mechanism of neuronal death in global ischemia. J Neurosci 1999, 19:4200-4210.
104. Deshpande J., Bergstedt K., Linden T., Kalimo H., Wieloch T. Ultrastructural changes in the hippocampal CA1 region following transient cerebral ischemia: Evidence against programmed cell death. Exp Brain Res 1992, 88:91-105.
105. van Lookeren Campagne M., Gill R. Ultrastructural morphological changes are not characteristic of apoptotic cell death following focal cerebral ischaemia in the rat. Neurosci Lett 1996, 213:111-114.
106. Pagnussat A.S., Faccioni-Heuser M.C., Netto C.A., Achaval M. An ultrastructural study of cell death in the CA1 pyramidal field of the hippocapmus in rats submitted to transient global ischemia followed by reperfusion. J Anat 2007, 211:589-599.
107. Chen J., Nagayama T., Jin K., Stetler R.A., Zhu R.L., Graham S.H., Simon R.P. Induction of caspase-3-like protease may mediate delayed neuronal death in the hippocampus after transient cerebral ischemia. J Neurosci 1998, 18:4914-4928.
108. Hara H., Friedlander R.M., Gagliardini V., Ayata C., Fink K., Huang Z., Shimizu-Sasamata M., Yuan J., Moskowitz M.A. Inhibition of interleukin 1beta converting enzyme family proteases reduces ischemic and excitotoxic neuronal damage. Proc Natl Acad Sci U S A 1997, 94:2007-2012.
109. Wang K.K. Calpain and caspase: Can you tell the difference?. Trends Neurosci 2000, 23:20-26.
110. Yamashima T. Implication of cysteine proteases calpain, cathepsin and caspase in ischemic neuronal death of primates. Prog Neurobiol 2000, 62:273-295.
111. Kilinc M., Gürsoy-Özdemir Y., Gurer G. Hysosomal rupture, necroapoptotic interactions and potential crosstalk between proteases in neurons shortly after focal ischemia. Neurobiol Dis 2010, 40:293-302.
112. Heron A., Pollard H., Dessi F., Moreau J., Lasbennes F., Ben-Ari Y., Charriaut-Marlangue C. Regional variability in DNA fragmentation after global ischemia evidenced by combined histological and gel electrophoresis observations in the rat brain. J Neurochem 1993, 61:1973-1976.
113. MacManus J.P., Buchan A.M., Hill I.E., Rasquinha I., Preston E. Global ischemia can cause DNA fragmentation indicative of apoptosis in rat brain. Neurosci Lett 1993, 164:89-92.
114. Tominaga T., Kure S., Narisawa K., Yoshimoto T. Endonuclease activation following focal ischemic injury in the rat brain. Brain Res 1993, 608:21-26.
115. MacManus J.P., Hill I.E., Huang Z.G., Rasquinha I., Xue D., Buchan A.M. DNA damage consistent with apoptosis in transient focal ischaemic neocortex. Neuroreport 1994, 5:493-496.
116. Charriaut-Marlangue C., Margaill I., Plotkine M., Ben-Ari Y. Early endonuclease activation following reversible focal ischemia in the rat brain. J Cereb Blood Flow Metab 1995, 15:385-388.
117. Li Y., Chopp M., Jiang N., Zhang Z.G., Zaloga C. Induction of DNA fragmentation after 10 to 120 minutes of focal cerebral ischemia in rats. Stroke 1995, 26:1252-1257. discussion 1257-1258.
118. Li Y., Chopp M., Powers C., Jiang N. Apoptosis and protein expression after focal cerebral ischemia in rat. Brain Res 1997, 765:301-312.
119. Eliasson M.J., Sampei K., Mandir A.S., Hurn P.D., Traystman R.J., Bao J., Pieper A., Wang Z.Q., Dawson T.M., Snyder S.H., Dawson V.L. Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia. Nat Med 1997, 3:1089-1095.
120. Endres M., Wang Z.Q., Namura S., Waeber C., Moskowitz M.A. Ischemic brain injury is mediated by the activation of poly(ADP-ribose)polymerase. J Cereb Blood Flow Metab 1997, 17:1143-1151.
121. Katchanov J., Harms C., Gertz K., Hauck L., Waeber C., Hirt L., Priller J., von Harsdorf R., Bruck W., Hortnagl H., Dirnagl U., Bhide P.G., Endres M. Mild cerebral ischemia induces loss of cyclin-dependent kinase inhibitors and activation of cell cycle machinery before delayed neuronal cell death. J Neurosci 2001, 21:5045-5053.
122. Antonawich F.J., Krajewski S., Reed J.C., Davis J.N. Bcl-x(l) Bax interaction after transient global ischemia. J Cereb Blood Flow Metab 1998, 18:882-886.
123. Elibol B., Soylemezoglu F., Unal I., Fujii M., Hirt L., Huang P.L., Moskowitz M.A., Dalkara T. Nitric oxide is involved in ischemia-induced apoptosis in brain: A study in neuronal nitric oxide synthase null mice. Neuroscience 2001, 105:79-86.
124. Isenmann S., Stoll G., Schroeter M., Krajewski S., Reed J.C., Bahr M. Differential regulation of Bax, Bcl-2, and Bcl-x proteins in focal cortical ischemia in the rat. Brain Pathol 1998, 8:49-62. discussion 62-43.
125. Fujimura M., Morita-Fujimura Y., Murakami K., Kawase M., Chan P.H. Cytosolic redistribution of cytochrome c after transient focal cerebral ischemia in rats. J Cereb Blood Flow Metab 1998, 18:1239-1247.
126. Krajewski S., Krajewska M., Ellerby L.M., Welsh K., Xie Z., Deveraux Q.L., Salvesen G.S., Bredesen D.E., Rosenthal R.E., Fiskum G., Reed J.C. Release of caspase-9 from mitochondria during neuronal apoptosis and cerebral ischemia. Proc Natl Acad Sci U S A 1999, 96:5752-5757.
127. Namura S., Zhu J., Fink K., Endres M., Srinivasan A., Tomaselli K.J., Yuan J., Moskowitz M.A. Activation and cleavage of caspase-3 in apoptosis induced by experimental cerebral ischemia. J Neurosci 1998, 18:3659-3668.
128. Velier J.J., Ellison J.A., Kikly K.K., Spera P.A., Barone F.C., Feuerstein G.Z. 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 1999, 19:5932-5941.
129. Thornberry N.A., Lazebnik Y. Caspases: Enemies within. Science 1998, 281:1312-1316.
130. Zhang J., Xu M. Apoptotic DNA fragmentation and tissue homeostasis. Trends Cell Biol 2002, 12:84-89.
131. Hara H., Fink K., Endres M., Friedlander R.M., Gagliardini V., Yuan J., Moskowitz M.A. Attenuation of transient focal cerebral ischemic injury in transgenic mice expressing a mutant ICE inhibitory protein. J Cereb Blood Flow Metab 1997, 17:370-375.
132. Friedlander R.M., Gagliardini V., Hara H., Fink K.B., Li W., MacDonald G., Fishman M.C., Greenberg A.H., Moskowitz M.A., Yuan J. Expression of a dominant negative mutant of interleukin-1 beta converting enzyme in transgenic mice prevents neuronal cell death induced by trophic factor withdrawal and ischemic brain injury. J Exp Med 1997, 185:933-940.
133. Loddick S.A., MacKenzie A., Rothwell N.J. An ICE inhibitor, z-VAD-DCB attenuates ischaemic brain damage in the rat. Neuroreport 1996, 7:1465-1468.
134. Schielke G.P., Yang G.Y., Shivers B.D., Betz A.L. Reduced ischemic brain injury in interleukin-1 beta converting enzyme-deficient mice. J Cereb Blood Flow Metab 1998, 18:180-185.
135. Asahi M., Hoshimaru M., Uemura Y., Tokime T., Kojima M., Ohtsuka T., Matsuura N., Aoki T., Shibahara K., Kikuchi H. Expression of interleukin-1 beta converting enzyme gene family and bcl-2 gene family in the rat brain following permanent occlusion of the middle cerebral artery. J Cereb Blood Flow Metab 1997, 17:11-18.
136. Endres M., Fink K., Zhu J., Stagliano N.E., Bondada V., Geddes J.W., Azuma T., Mattson M.P., Kwiatkowski D.J., Moskowitz M.A. Neuroprotective effects of gelsolin during murine stroke. J Clin Invest 1999, 103:347-354.
137. Fink K., Zhu J., Namura S., Shimizu-Sasamata M., Endres M., Ma J., Dalkara T., Yuan J., Moskowitz M.A. Prolonged therapeutic window for ischemic brain damage caused by delayed caspase activation. J Cereb Blood Flow Metab 1998, 18:1071-1076.
138. Matsushita K., Wu Y., Qiu J., Lang-Lazdunski L., Hirt L., Waeber C., Hyman B.T., Yuan J., Moskowitz M.A. Fas receptor and neuronal cell death after spinal cord ischemia. J Neurosci 2000, 20:6879-6887.
139. Martin-Villalba A., Hahne M., Kleber S., Vogel J., Falk W., Schenkel J., Krammer P.H. Therapeutic neutralization of CD95-ligand and TNF attenuates brain damage in stroke. Cell Death Differ 2001, 8:679-686.
140. Martin-Villalba A., Herr I., Jeremias I., Hahne M., Brandt R., Vogel J., Schenkel J., Herdegen T., Debatin K.M. CD95 ligand (Fas-L/APO-1L) and tumor necrosis factor-related apoptosis-inducing ligand mediate ischemia-induced apoptosis in neurons. J Neurosci 1999, 19:3809-3817.
141. Rosenbaum D.M., Gupta G., D'Amore J., Singh M., Weidenheim K., Zhang H., Kessler J.A. Fas (CD95/APO-1) plays a role in the pathophysiology of focal cerebral ischemia. J Neurosci Res 2000, 61:686-692.
142. Mehmet H. Stroke treatment enters the Fas lane. Cell Death Differ 2001, 8:659-661.
143. Stoll G., Jander S., Schroeter M. Inflammation and glial responses in ischemic brain lesions. Prog Neurobiol 1998, 56:149-171.
144. Plesnila N., Zinkel S., Le D.A., Amin-Hanjani S., Wu Y., Qiu J., Chiarugi A., Thomas S.S., Kohane D.S., Korsmeyer S.J., Moskowitz M.A. Bid mediates neuronal cell death after oxygen/glucose deprivation and focal cerebral ischemia. Proc Natl Acad Sci U S A 2001, 98:15318-15323.
145. Wei M.C., Lindsten T., Mootha V.K., Weiler S., Gross A., Ashiya M., Thompson C.B., Korsmeyer S.J. tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 2000, 14:2060-2071.
146. Harrison D.C., Davis R.P., Bond B.C., Campbell C.A., James M.F., Parsons A.A., Philpott K.L. Caspase mRNA expression in a rat model of focal cerebral ischemia. Brain Res Mol Brain Res 2001, 89:133-146.
147. Kang S.J., Wang S., Hara H., Peterson E.P., Namura S., Amin-Hanjani S., Huang Z., Srinivasan A., Tomaselli K.J., Thornberry N.A., Moskowitz M.A., Yuan J. Dual role of caspase-11 in mediating activation of caspase-1 and caspase-3 under pathological conditions. J Cell Biol 2000, 149:613-622.
148. Shibata M., Hattori H., Sasaki T., Gotoh J., Hamada J., Fukuuchi Y. Activation of caspase-12 by endoplasmic reticulum stress induced by transient middle cerebral artery occlusion in mice. Neuroscience 2003, 118:491-499.
149. Bergeron L., Perez G.I., Macdonald G., Shi L., Sun Y., Jurisicova A., Varmuza S., Latham K.E., Flaws J.A., Salter J.C., Hara H., Moskowitz M.A., Li E., Greenberg A., Tilly J.L., Yuan J. Defects in regulation of apoptosis in caspase-2-deficient mice. Genes Dev 1998, 12:1304-1314.
150. Kinoshita M., Tomimoto H., Kinoshita A., Kumar S., Noda M. Up-regulation of the Nedd2 gene encoding an ICE/Ced-3-like cysteine protease in the gerbil brain after transient global ischemia. J Cereb Blood Flow Metab 1997, 17:507-514.
151. Panickar K.S., Norenberg M.D. Astrocytes in cerebral ischemic injury: Morphological and general considerations. Glia 2005, 50:287-298.
152. Cheng Y., Deshmukh M., D'Costa A., Demaro J.A., Gidday J.M., Shah A., Sun Y., Jacquin M.F., Johnson E.M., Holtzman D.M. Caspase inhibitor affords neuroprotection with delayed administration in a rat model of neonatal hypoxic-ischemic brain injury. J Clin Invest 1998, 101:1992-1999.
153. Gillardon F., Bottiger B., Schmitz B., Zimmermann M., Hossmann K.A. Activation of CPP-32 protease in hippocampal neurons following ischemia and epilepsy. Brain Res Mol Brain Res 1997, 50:16-22.
154. Bhat R.V., DiRocco R., Marcy V.R., Flood D.G., Zhu Y., Dobrzanski P., Siman R., Scott R., Contreras P.C., Miller M. Increased expression of IL-1beta converting enzyme in hippocampus after ischemia: Selective localization in microglia. J Neurosci 1996, 16:4146-4154.
155. Gillardon F., Kiprianova I., Sandkuhler J., Hossmann K.A., Spranger M. Inhibition of caspases prevents cell death of hippocampal CA1 neurons, but not impairment of hippocampal long-term potentiation following global ischemia. Neuroscience 1999, 93:1219-1222.
156. Ni B., Wu X., Su Y., Stephenson D., Smalstig E.B., Clemens J., Paul S.M. Transient global forebrain ischemia induces a prolonged expression of the caspase-3 mRNA in rat hippocampal CA1 pyramidal neurons. J Cereb Blood Flow Metab 1998, 18:248-256.
157. Ouyang Y.B., Tan Y., Comb M., Liu C.L., Martone M.E., Siesjo B.K., Hu B.R. Survival- and death-promoting events after transient cerebral ischemia: Phosphorylation of Akt, release of cytochrome c and activation of caspase-like proteases. J Cereb Blood Flow Metab 1999, 19:1126-1135.
158. Antonawich F.J., Federoff H.J., Davis J.N. Bcl-2 transduction, using a herpes simplex virus amplicon, protects hippocampal neurons from transient global ischemia. Exp Neurol 1999, 156:130-137.
159. Nakatsuka H., Ohta S., Tanaka J., Toku K., Kumon Y., Maeda N., Sakanaka M., Sakaki S. Release of cytochrome c from mitochondria to cytosol in gerbil hippocampal CA1 neurons after transient forebrain ischemia. Brain Res 1999, 849:216-219.
160. Sugawara T., Fujimura M., Morita-Fujimura Y., Kawase M., Chan P.H. Mitochondrial release of cytochrome c corresponds to the selective vulnerability of hippocampal CA1 neurons in rats after transient global cerebral ischemia. J Neurosci 1999, 19. RC39.
161. Perez-Pinzon M.A., Xu G.P., Born J., Lorenzo J., Busto R., Rosenthal M., Sick T.J. Cytochrome c is released from mitochondria into the cytosol after cerebral anoxia or ischemia. J Cereb Blood Flow Metab 1999, 19:39-43.
162. Lin R., Roseborough G., Dong Y., Williams G.M., Wei C. DNA damage and repair system in spinal cord ischemia. J Vasc Surg 2003, 37:847-858.
163. Wang P., Cao X., Nagel D.J., Yin G. Activation of ASK1 during reperfusion of ischemic spinal cord. Neurosci Lett 2007, 415:248-252.
164. Chan P.H. Reactive oxygen radicals in signaling and damage in the ischemic brain. J Cereb Blood Flow Metab 2001, 21:2-14.
165. Endres M., Hirt L., Moskowitz M.A. Apoptosis and cerebral ischemia. Apoptosis: Role in disease, pathogenesis and prevention 2001, 137-167. Elsevier Science, Amsterdam. V.M. Rangnekar (Ed.).
166. Nakka V.P., Gusain A., Mehta S.L., Raghubir R. Molecular mechanisms of apoptosis in cerebral ischemia: Multiple neuroprotective opportunities. Mol Neurobiol 2008, 37:7-38.
167. Himi T., Ishizaki Y., Murota S. A caspase inhibitor blocks ischaemia-induced delayed neuronal death in the gerbil. Eur J Neurosci 1998, 10:777-781.
168. Aktas Y., Yemisci M., Andrieux K., Gursoy R.N., Alonso M.J., Fernandez-Megia E., Novoa-Carballal R., Quinoa E., Riguera R., Sargon M.F., Celik H.H., Demir A.S., Hincal A.A., Dalkara T., Capan Y., Couvreur P. Development and brain delivery of chitosan-PEG nanoparticles functionalized with the monoclonal antibody OX26. Bioconjug Chem 2005, 16:1503-1511.
169. Karatas H., Aktas Y., Gursoy-Ozdemir Y., Bodur E., Yemisci M., Caban S., Vural A., Pinarbasli O., Capan Y., Fernandez-Megia E., Novoa-Carballal R., Riguera R., Andrieux K., Couvreur P., Dalkara T. A nanomedicine transports a peptide caspase-3 inhibitor across the blood-brain barrier and provides neuroprotection. J Neurosci 2009, 29:13761-13769.
170. Rothwell N.J., Loddick S.A., Stroemer P. Interleukins and cerebral ischaemia. Int Rev Neurobiol 1997, 40:281-298.
171. Ma J., Endres M., Moskowitz M.A. Synergistic effects of caspase inhibitors and MK-801 in brain injury after transient focal cerebral ischaemia in mice. Br J Pharmacol 1998, 124:756-762.
172. Ma J., Qiu J., Hirt L., Dalkara T., Moskowitz M.A. Synergistic protective effect of caspase inhibitors and bFGF against brain injury induced by transient focal ischaemia. Br J Pharmacol 2001, 133:345-350.
173. Endres M., Fan G., Hirt L., Fujii M., Matsushita K., Liu X., Jaenisch R., Moskowitz M.A. Ischemic brain damage in mice after selectively modifying BDNF or NT4 gene expression. J Cereb Blood Flow Metab 2000, 20:139-144.
174. Beck T., Lindholm D., Castren E., Wree A. Brain-derived neurotrophic factor protects against ischemic cell damage in rat hippocampus. J Cereb Blood Flow Metab 1994, 14:689-692.
175. Chan K.M., Lam D.T., Pong K., Widmer H.R., Hefti F. Neurotrophin-4/5 treatment reduces infarct size in rats with middle cerebral artery occlusion. Neurochem Res 1996, 21:763-767.
176. Schabitz W.R., Schwab S., Spranger M., Hacke W. Intraventricular brain-derived neurotrophic factor reduces infarct size after focal cerebral ischemia in rats. J Cereb Blood Flow Metab 1997, 17:500-506.
177. Tsukahara T., Yonekawa Y., Tanaka K., Ohara O., Wantanabe S., Kimura T., Nishijima T., Taniguchi T. The role of brain-derived neurotrophic factor in transient forebrain ischemia in the rat brain. Neurosurgery 1994, 34:323-331. discussion 331.
178. Love S., Barber R., Wilcock G.K. Neuronal death in brain infarcts in man. Neuropathol Appl Neurobiol 2000, 26:55-66.
179. Sairanen T., Carpen O., Karjalainen-Lindsberg M.L., Paetau A., Turpeinen U., Kaste M., Lindsberg P.J. Evolution of cerebral tumor necrosis factor-alpha production during human ischemic stroke. Stroke 2001, 32:1750-1758.
180. Hara A., Yoshimi N., Hirose Y., Ino N., Tanaka T., Mori H. DNA fragmentation in granular cells of human cerebellum following global ischemia. Brain Res 1995, 697:247-250.
181. Kingsbury A.E., Mardsen C.D., Foster O.J. DNA fragmentation in human substantia nigra: Apoptosis or perimortem effect?. Mov Disord 1998, 13:877-884.
182. Anlar B., Soylemezoglu F., Elibol B., Dalkara T., Aysun S., Kose G., Belen D., Yalaz K. Apoptosis in brain biopsies of subacute sclerosing panencephalitis patients. Neuropediatrics 1999, 30:239-242.
183. Benjelloun N., Menard A., Charriaut-Marlangue C., Mokhtari K., Perron H., Hauw J.J., Rieger F. Case report: DNA fragmentation in glial cells in a cerebral biopsy from a multiple sclerosis patient. Cell Mol Biol (Noisy-le-grand) 1998, 44:579-583.
184. Dorr J., Bechmann I., Waiczies S., Aktas O., Walczak H., Krammer P.H., Nitsch R., Zipp F. Lack of tumor necrosis factor-related apoptosis-inducing ligand but presence of its receptors in the human brain. J Neurosci 2002, 22:RC209.
185. Ferrer I. Nuclear DNA fragmentation in Creutzfeldt-Jakob disease: Does a mere positive in situ nuclear end-labeling indicate apoptosis?. Acta Neuropathol 1999, 97:5-12.
186. Uysal H., Cevik I.U., Soylemezoglu F., Elibol B., Ozdemir Y.G., Evrenkaya T., Saygi S., Dalkara T. Is the cell death in mesial temporal sclerosis apoptotic?. Epilepsia 2003, 44:778-784.
187. Yuzbasioglu A., Karatas H., Gursoy-Ozdemir Y., Saygi S., Akalan N., Soylemezoglu F., Dalkara T., Kocaefe Y.C., Ozguc M. Changes in the expression of selenoproteins in mesial temporal lobe epilepsy patients. Cell Mol Neurobiol 2009, 29:1223-1231.
188. Marshall K.A., Daniel S.E., Cairns N., Jenner P., Halliwell B. Upregulation of the anti-apoptotic protein Bcl-2 may be an early event in neurodegeneration: Studies on Parkinson's and incidental Lewy body disease. Biochem Biophys Res Commun 1997, 240:84-87.
189. Su J.H., Deng G., Cotman C.W. Bax protein expression is increased in Alzheimer's brain: Correlations with DNA damage, Bcl-2 expression, and brain pathology. J Neuropathol Exp Neurol 1997, 56:86-93.
190. Vyas S., Javoy-Agid F., Herrero M.T., Strada O., Boissiere F., Hibner U., Agid Y. Expression of Bcl-2 in adult human brain regions with special reference to neurodegenerative disorders. J Neurochem 1997, 69:223-231.
191. Yachnis A.T., Powell S.Z., Olmsted J.J., Eskin T.A. Distinct neurodevelopmental patterns of bcl-2 and bcl-x expression are altered in glioneuronal hamartias of the human temporal lobe. J Neuropathol Exp Neurol 1997, 56:186-198.
192. Desjardins P., Ledoux S. Expression of ced-3 and ced-9 homologs in Alzheimer's disease cerebral cortex. Neurosci Lett 1998, 244:69-72.
193. Kitamura Y., Shimohama S., Kamoshima W., Ota T., Matsuoka Y., Nomura Y., Smith M.A., Perry G., Whitehouse P.J., Taniguchi T. Alteration of proteins regulating apoptosis, Bcl-2, Bcl-x, Bax, Bak, Bad, ICH-1 and CPP32, in Alzheimer's disease. Brain Res 1998, 780:260-269.
194. Clark R.S., Kochanek P.M., Chen M., Watkins S.C., Marion D.W., Chen J., Hamilton R.L., Loeffert J.E., Graham S.H. Increases in Bcl-2 and cleavage of caspase-1 and caspase-3 in human brain after head injury. FASEB J 1999, 13:813-821.
195. Henshall D.C., Clark R.S., Adelson P.D., Chen M., Watkins S.C., Simon R.P. Alterations in bcl-2 and caspase gene family protein expression in human temporal lobe epilepsy. Neurology 2000, 55:250-257.
196. Jarskog L.F., Gilmore J.H. Developmental expression of Bcl-2 protein in human cortex. Brain Res Dev Brain Res 2000, 119:225-230.
197. Tatton N.A. Increased caspase 3 and Bax immunoreactivity accompany nuclear GAPDH translocation and neuronal apoptosis in Parkinson's disease. Exp Neurol 2000, 166:29-43.
198. Engidawork E., Gulesserian T., Seidl R., Cairns N., Lubec G. Expression of apoptosis related proteins: RAIDD, ZIP kinase, Bim/BOD, p21, Bax, Bcl-2 and NF-kappaB in brains of patients with Down syndrome. J Neural Transm Suppl 2001, 61:181-192.
199. Hartmann A., Michel P.P., Troadec J.D., Mouatt-Prigent A., Faucheux B.A., Ruberg M., Agid Y., Hirsch E.C. Is Bax a mitochondrial mediator in apoptotic death of dopaminergic neurons in Parkinson's disease?. J Neurochem 2001, 76:1785-1793.
200. Pompl P.N., Yemul S., Xiang Z., Ho L., Haroutunian V., Purohit D., Mohs R., Pasinetti G.M. Caspase gene expression in the brain as a function of the clinical progression of Alzheimer disease. Arch Neurol 2003, 60:369-376.
201. Engidawork E., Gulesserian T., Yoo B.C., Cairns N., Lubec G. Alteration of caspases and apoptosis-related proteins in brains of patients with Alzheimer's disease. Biochem Biophys Res Commun 2001, 281:84-93.
202. Hartmann A., Hunot S., Michel P.P., Muriel M.P., Vyas S., Faucheux B.A., Mouatt-Prigent A., Turmel H., Srinivasan A., Ruberg M., Evan G.I., Agid Y., Hirsch E.C. Caspase-3: A vulnerability factor and final effector in apoptotic death of dopaminergic neurons in Parkinson's disease. Proc Natl Acad Sci U S A 2000, 97:2875-2880.
203. Matsui T., Ramasamy K., Ingelsson M., Fukumoto H., Conrad C., Frosch M.P., Irizarry M.C., Yuan J., Hyman B.T. Coordinated expression of caspase 8, 3 and 7 mRNA in temporal cortex of Alzheimer disease: Relationship to formic acid extractable abeta42 levels. J Neuropathol Exp Neurol 2006, 65:508-515.
204. Rohn T.T., Head E., Nesse W.H., Cotman C.W., Cribbs D.H. Activation of caspase-8 in the Alzheimer's disease brain. Neurobiol Dis 2001, 8:1006-1016.
205. Nishimura T., Akiyama H., Yonehara S., Kondo H., Ikeda K., Kato M., Iseki E., Kosaka K. Fas antigen expression in brains of patients with Alzheimer-type dementia. Brain Res 1995, 695:137-145.
206. de la Monte S.M., Sohn Y.K., Wands J.R. Correlates of p53- and Fas (CD95)-mediated apoptosis in Alzheimer's disease. J Neurol Sci 1997, 152:73-83.
207. Ferrer I., Puig B., Krupinsk J., Carmona M., Blanco R. Fas and Fas ligand expression in Alzheimer's disease. Acta Neuropathol 2001, 102:121-131.
208. Gulesserian T., Engidawork E., Yoo B.C., Cairns N., Lubec G. Alteration of caspases and other apoptosis regulatory proteins in Down syndrome. J Neural Transm Suppl 2001, 61:163-179.
209. Newman S.J., Bond B., Crook B., Darker J., Edge C., Maycox P.R. Neuron-specific localisation of the TR3 death receptor in Alzheimer's disease. Brain Res 2000, 857:131-140.
210. O'Barr S., Schultz J., Rogers J. Expression of the protooncogene bcl-2 in Alzheimer's disease brain. Neurobiol Aging 1996, 17:131-136.
211. Stadelmann C., Deckwerth T.L., Srinivasan A., Bancher C., Bruck W., Jellinger K., Lassmann H. Activation of caspase-3 in single neurons and autophagic granules of granulovacuolar degeneration in Alzheimer's disease. Evidence for apoptotic cell death. Am J Pathol 1999, 155:1459-1466.
212. Su J.H., Anderson A.J., Cummings B.J., Cotman C.W. Immunohistochemical evidence for apoptosis in Alzheimer's disease. Neuroreport 1994, 5:2529-2533.
213. Anderson A.J., Su J.H., Cotman C.W. DNA damage and apoptosis in Alzheimer's disease: Colocalization with c-Jun immunoreactivity, relationship to brain area, and effect of postmortem delay. J Neurosci 1996, 16:1710-1719.
214. Rohn T.T., Head E., Su J.H., Anderson A.J., Bahr B.A., Cotman C.W., Cribbs D.H. Correlation between caspase activation and neurofibrillary tangle formation in Alzheimer's disease. Am J Pathol 2001, 158:189-198.
215. Yang F., Sun X., Beech W., Teter B., Wu S., Sigel J., Vinters H.V., Frautschy S.A., Cole G.M. Antibody to caspase-cleaved actin detects apoptosis in differentiated neuroblastoma and plaque-associated neurons and microglia in Alzheimer's disease. Am J Pathol 1998, 152:379-389.
216. Mochizuki H., Goto K., Mori H., Mizuno Y. Histochemical detection of apoptosis in Parkinson's disease. J Neurol Sci 1996, 137:120-123.
217. Dragunow M., Faull R.L., Lawlor P., Beilharz E.J., Singleton K., Walker E.B., Mee E. In situ evidence for DNA fragmentation in Huntington's disease striatum and Alzheimer's disease temporal lobes. Neuroreport 1995, 6:1053-1057.
218. Portera-Cailliau C., Hedreen J.C., Price D.L., Koliatsos V.E. Evidence for apoptotic cell death in Huntington disease and excitotoxic animal models. J Neurosci 1995, 15:3775-3787.
219. Butterworth N.J., Williams L., Bullock J.Y., Love D.R., Faull R.L., Dragunow M. Trinucleotide (CAG) repeat length is positively correlated with the degree of DNA fragmentation in Huntington's disease striatum. Neuroscience 1998, 87:49-53.
220. Garden G.A., Budd S.L., Tsai E., Hanson L., Kaul M., D'Emilia D.M., Friedlander R.M., Yuan J., Masliah E., Lipton S.A. Caspase cascades in human immunodeficiency virus-associated neurodegeneration. J Neurosci 2002, 22:4015-4024.
221. Adle-Biassette H., Levy Y., Colombel M., Poron F., Natchev S., Keohane C., Gray F. Neuronal apoptosis in HIV infection in adults. Neuropathol Appl Neurobiol 1995, 21:218-227.
222. Shi B., De Girolami U., He J., Wang S., Lorenzo A., Busciglio J., Gabuzda D. Apoptosis induced by HIV-1 infection of the central nervous system. J Clin Invest 1996, 98:1979-1990.
223. Qiu J., Whalen M.J., Lowenstein P., Fiskum G., Fahy B., Darwish R., Aarabi B., Yuan J., Moskowitz M.A. Upregulation of the Fas receptor death-inducing signaling complex after traumatic brain injury in mice and humans. J Neurosci 2002, 22:3504-3511.
224. Smith F.M., Raghupathi R., MacKinnon M.A., McIntosh T.K., Saatman K.E., Meaney D.F., Graham D.I. TUNEL-positive staining of surface contusions after fatal head injury in man. Acta Neuropathol 2000, 100:537-545.
225. Williams S., Raghupathi R., MacKinnon M.A., McIntosh T.K., Saatman K.E., Graham D.I. In situ DNA fragmentation occurs in white matter up to 12 months after head injury in man. Acta Neuropathol 2001, 102:581-590.