Temporal relationships between de novo protein synthesis, calpain and caspase 3-like protease activation, anda DNA fragmentation during apoptosis in septo-hippocampal cultures

Journal of Neuroscience Research

Volumn 52, Issue 5, 1998, Pages 505-520

  Pike, Brian R ^a   Zhao, Xiurong ^a   Newcomb, Jennifer K ^a   Wang, Kevin K W ^b   Posmantur, Rand M ^b   Hayes, Ronald L ^a,c  

^a UNIVERSITY OF TEXAS   (United States)

^b PFIZER INC   (United States)

^c UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

spectrin; Brain; CPP32; Cysteine proteases; Fodrin; Rat; Trauma

Indexed keywords

CALPAIN; CYSTEINE PROTEINASE; DNA; DNA FRAGMENT; ENDONUCLEASE; FODRIN;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; ENZYME ACTIVATION; FETUS; HIPPOCAMPUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; SEPTUM PELLUCIDUM;

ANIMALS; APOPTOSIS; CALPAIN; CASPASE 3; CASPASES; CELLS, CULTURED; CYSTEINE ENDOPEPTIDASES; DNA FRAGMENTATION; ENZYME ACTIVATION; ENZYME INHIBITORS; HIPPOCAMPUS; NERVE TISSUE PROTEINS; NEUROGLIA; NEURONS; POLY(ADP-RIBOSE) POLYMERASES; PROTEINS; RATS; SEPTUM PELLUCIDUM; SPECTRIN; STAUROSPORINE; TIME FACTORS;

EID: 0032101643     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4547(19980601)52:5<505::AID-JNR3>3.0.CO;2-G     Document Type: Article

References (70)

1. Behrens MM, Marinez JL, Moratilla C, Renart J (1995): Apoptosis induced by protein kinase-C inhibition in a neuroblastoma cell line. Cell Growth Diff 6:1375-1380.
2. Bertrand R, Solary E, O'Connor P, Kohn KW, Pommier Y (1994): Induction of a common pathway of apoptosis by staurosporine. Exp Cell Res 211:314-321.
3. Bredesen DE (1995): Neural apoptosis. Ann Neurol 38:839-851.
4. Cagnoli CM, Kharlamov E, Atabay C, Uz T, Manev H (1996): Apoptosis induced in neuronal cultures by either the phosphatase inhibitor okadaic acid or the kinase inhibitor staurosporine is attenuated by isoquinolinesulfonamides H-7, H-8, and H-9. J Mol Neurosci 7:65-76.
5. Casciola-Rosen LA, Miller DK, Anhalt GJ, Rosen A (1994): Specific cleavage of the 70-kDa protein component of the U1 small nuclear ribonucleoprotein is a characteristic biochemical feature of apoptotic cell death. J Biol Chem 269:30757-30760.
6. Chopp M, Li Y, Zhang ZG, Freytag SO (1992): p53 expression in brain after middle cerebral artery occlusion in the rat. Biochem Biophys Res Commun 182:1201-1207.
7. Cohen GM (1997): Caspases: the executioners of apoptosis. Biochem J 326:1-16.
8. Cohen JJ (1991): Programmed cell death in the immune system. Adv Immunol 50:55-85.
9. Cohen JJ, Duke RC (1984): Glucocorticoid activation of a calcium dependent endonuclease in thymocyte nuclei leads to cell death. J Immunol 132:38-42.
10. Colicos MA, Dash PK (1996): Apoptotic morphology of dentate gyrus granule cells following experimental cortical impact injury in rats: possible role in spatial memory deficits. Brain Res 739:120-131.
11. Conti AC, Raghupathi R, Becher O, Rink AD, Trojanowski JO, McIntosh TK (1996): Delayed apoptotic cell death following lateral fluid percussion brain injury in the rat: a long-term study. J Neurotrauma 13:595 [abstract].
12. Eldadah BA, Yakovlev AG, Faden AI (1996): A new approach for the electrophoretic detection of apoptosis. Nucleic Acids Res 24: 4092-1093.
13. Eldadah BA, Yakovlev AG, Faden AI (1997): The role of CED-3 related cysteine proteases in apoptosis of cerebellar granule cells. J Neurosci 17:6105-6113.
14. Falcieri E, Marrtelli AM, Bareggi R, Cataldi A, Cocco L (1993): The protein kinase inhibitor staurosporine induces morphological changes typical of apoptosis in MOLT-4 cells without concomitant DNA fragmentation. Biochem Biophys Res Commun 193:19-25.
15. Forloni G, Angeretti N, Chiesa R, Monzani E, Salmona M, Bugiani O, Tagliavini F (1993): Neurotoxicity of a prion protein fragment. Nature 352:543-546.
16. Fraser A, Evan G (1996): A license to kill. Cell 85:781-784.
17. Furukawa K, Estus S, Fu W, Mark RJ, Mattson, MP (1997): Neuroprotective action of cycloheximide involves induction of bcl-2 and anti-oxidant pathways. J Cell Biol 136:1137-1149.
18. Ghayur T, Hugunin M, Talanian RV, Ratnofsky S, Quinlan C, Emoto Y, Pandey P, Datta R, Huang Y, Kharbanda S, Allen H, Kamen R, Wong W, Kufe D (1996): Proteolytic activation of protein kinase C delta by an ICE/CED 3-like protease induces characteristics of apoptosis. J Exp Med 184:2399-2404.
19. Gong J, Traganos F, Darzynkiewicz Z (1994): A selective procedure for DNA extraction from apoptotic cells applicable for gel electrophoresis and flow cytometry. Anal Biochem 218:314-319.
20. Honkaniemi J, Massa SM, Breckinridge M, Sharp FR (1996): Global ischemia induces apoptosis-associated genes in hippocampus. Mol Brain Res 42:79-88.
21. Jenkins LW, Moszynski K, Lyeth BG, Lewelt W, DeWitt DS, Allen A, Dixon CE, Povlishock JT, Majewski TJ, Clifton GL, Young HF, Becker DP, Hayes RL (1989): Increased vulnerability of the mildly traumatized brain to cerebral ischemia: the use of controlled secondary ischemia as a research tool to identify common or different mechanisms contributing to mechanical and ischemic brain injury. Brain Injury 477:211-224.
22. Johnson EM, Greenlund LJS, Akins PT, Hsu CY (1995): Neuronal apoptosis: current understanding of molecular mechanisms and potential role in ischemic brain injury. J Neurotrauma 12:843-852.
23. Jones KH, Senft, AJ (1985): An improved method to determine cell viability by simultaneous staining with fluorescein diacetate-propidium iodide. J Histochem Cytochem 33:77-79.
24. Jordan J, Galindo MF, Miller RJ (1997): Role of calpain-and interleukin-1 converting enzyme-like proteases in the β-amyloid-induced death of rat hippocampal neurons in culture. J Neurochem 68:1612-1621.
25. Kampfl A, Posmantur RM, Zhao X, Schmutzhard E, Clifton GL, Hayes RL (1997): Mechanisms of calpain proteolysis following traumatic brain injury: implications for pathology and therapy: a review and update. J Neurotrauma 14:121-134.
26. Kampfl A, Zhao X, Whitson JS, Posmantur RM, Dixon CE, Yang K, Clifton GL, Hayes RL (1996): Calpain inhibitors protect against depolarization-induced neurofilament protein loss of septo-hippocampal neurons in culture. Eur J Neurosci 8:344-352.
27. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD (1997): The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275:1132-1136.
28. Koh J, Wie MB, Gwag BJ, Sensi SL, Canzoniero MT, Demaro J, Csernansky C, Choi DW (1995): Staurosporine-induced neuronal apoptosis. Exp Neurol 135:153-159.
29. Kothakota S, Azuma T, Reinhard C, Klippel A, Tang J, Chu K, McGarry TJ, Kirschner MW, Koths K, Kwiatkowski DJ, Williams LT (1997): Caspase 3-generated fragment of gelsolin: effector of morphological change in apoptosis. Science 278:294-298.
30. Krajewski S, Krajewski M, Shabaik A, Miyashita T, Wang HG, Reed JC (1995): Upregulation of Bax protein levels in neurons following cerebral ishcemia. J Neurosci 15:6364-6376.
31. Lazebnik YA, Kaufmann SH, Desnoyers S, Poirer GG, Earnshaw WC (1994): Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 371:346-347.
32. Lazebnik YA, Takahashi A, Moir RD, Goldman RD, Poirier GG, Kaufmann SH, Earnshaw WC (1995): Studies of the lamin proteinase reveal multiple parallel biochemical pathways during apoptotic execution. Proc Natl Acad Sci USA 92:9042-9046.
33. Linnik MD, Zobrist RH, Hatfield MD (1993): Evidence supporting role for programmed cell death in focal cerebral ischemia in rats. Stroke 24:2002-2009.
34. Linnik MD, Markgraf CG, Mason PJ, Velayo N, Racke MM (1996): Calpain Inhibition attenuates apoptosis in vitro and decreases infarct size in vivo. In Krieglstein J (ed):"Pharmacology of Cerebral Ischemia." Boca Raton, FL: CRC Press, pp 33-40.
35. Loo DT, Copani AC, Pike CJ, Whittenmore, ER, Walencewicz AJ, Cotman CW (1993): Apoptosis is induced by β-amyloid in cultured central nervous system neurons. Proc Natl Acad Sci USA 90:7951-7955.
36. Lyeth BG, Jenkins LW, Hamm RJ, Dixon CE, Phillips LL, Clifton GL, Young HF, Hayes RL (1990): Prolonged memory impairment in the absence of hippocampal cell death following traumatic brain injury in the rat. Brain Res 526:249-258.
37. MacManus JP, Buchan AM, Hill IE, Rasquinha I, Preston E (1993): Global ischemia can cause DNA fragmentation indicative of apoptosis in rat brain. Neurosci Lett 164:89-92.
38. Martin DP, Schmidt RE, DiStefano PS, Lowry OH, Carter JG, Johnson EM (1988): Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J Cell Biol 106:829-844.
39. Martin SJ, O'Brien GA, Nishioka WK, McGahon AJ, Mahboubi A, Saido TC, Green DR (1995): Proteolysis of fodrin (nonerythroid spectrin) during apoptosis. J Biol Chem 270:6425-6428.
40. McConkey DJ, Hartzell P, Nicotera P, Orrenius S (1989): DNA fragmentation kills immature thymocytes. FASEB J 3:1843-1848.
41. Miura M, Zhu H, Rotello R, Hartwieg EA, Yuan J (1993): Induction of apoptosis in fibroblasts by IL-1 beta-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3. Cell 75:653-660.
42. Na S, Chuang TH, Cunningham A, Turi TG, Hanke JH, Bokoch GM, Danley DE (1996): D4-GDI, a substrate of CPP32, is proteolyzed during Fas-induced apoptosis. J Biol Chem 271:11209-11213.
43. Nath R, McGinnis KJ, Nadimpalli R, Stafford D, Wang KKW (1996a): Effects of ICE-like proteases and calpain inhibitors on neuronal apoptosis. Neuroreport 8:249-255.
44. Nath R, Raser KJ, Stafford D, Hajimohammadreza I, Posner A, Allen H, Talanian RV, Yuen P, Gilbertsen RB, Wang KKW (1996b): Non-erythroid α-spectrin breakdown by calpain and interleukin 1-converting-enzyme-like protease(s) in apoptotic cells: contributory roles of both protease families in neuronal apoptosis. Biochem J 319:683-690.
45. 2+-dependent endonuclease in thymocytes of irradiated rats. Int J Radiat Biol 53:749-765.
46. Newcomb JK, Zhao X, Pike BR, Clifton GL, Hayes RL (1997): Evidence of apoptosis following controlled cortical impact injury in the rat. J Neurotrauma 14:763. [abstract]
47. Nicholson DW, Ali A, Thornberry NA, Vaillancourt JP, Ding CK, Gallant M, Gareau Y, Griffin PR, Labelle M, Lazebnik YA, Munday NA, Raju SM, Smulson ME, Yamin T-T, Yu VL, Miller DK (1995): Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376: 37-43.
48. Nitatori T, Sato N, Waguri S, Karasawa Y, Araki H, Shibanai K, Kominami E, Uchiyama Y (1995): Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J Neurosci 15:1001-1011.
49. Oberhammer F, Fritsch G, Schmied M, Pavelka M, Printz D, Purchio T, Lassmann H, Schulte-Hermann R (1993): Condensation of the chromatin at the membrane of an apoptotic nucleus is not associated with activation of an endonuclease. J Cell Sci 104:317-326.
50. Papas S, Crepel V, Hasboun D, Jorquera I, Chinestra P, Ben-Ari Y (1992): Cycloheximide reduces the effects of anoxic insult in vivo and in vitro. Eur J Neurosci 4:758-765.
51. Pravdenkova SV, Basnakian AG, James SJ, Anderson BJ (1996): DNA fragmentation and nuclear endonuclease activity in rat brain after sever closed head injury. Brain Res 729:151-155.
52. Raff MC, Barres BA, Burne JF, Coles HS, Ishizaki Y, Jacobson MD (1993): Programmed cell death and the control of cell survival: lessons from the nervous system. Science 262:695-700.
53. Rink A, Fung K, Trojanowski JQ, Lee VM, Neugebauer E, McIntosh TK (1995): Evidence of apoptotic cell death after experimental traumatic brain injury in the rat. Am J Pathol 147:1575-1583.
54. Roberts-Lewis JM, Savage MJ, Marcy VR, Pinsker LR, Siman R (1994): Immunolocalization of μ-calpain mediated spectrin degradation to vulnerable neurons in ischemic gerbil brain. J Neurosci 14:3934-3944.
55. Rosen A, Casciola-Rosen L (1997): Macromolecular substrates for the ICE-like proteases during apoptosis. J Cell Biochem 64:50-54.
56. Saido TC, Sorimachi H, Suzuki K (1994): Calpain: new perspectives in molecular diversity and physiological-pathological involvement. FASEB J 8:814-822.
57. Shigeno T, Yamasaki Y, Kato G, Kausaka K, Mima T, Takakura K, Graham DI, Furukawa S (1990): Reduction of delayed neuronal death by inhibition of protein synthesis. Neurosci Lett 120:117-119.
58. Sloviter RS (1996): Hippocampal pathology and pathophysiology in temporal lobe epilepsy. Neuroglia 11(Suppl. 4):29-32.
59. Squier MKT, Miller ACK, Malkinson AM, Cohen JJ (1994): Calpain activation in apoptosis. J Cell Physiol 159:229-237.
60. Suzuki K, Sorimachi H, Yoshizawa T, Kinbara K, Ishiura S (1995): Calpain: novel family members, activation and physiological function. Biol Chem 376:523-529.
61. Vanags DM, Porn-Ares MI, Coppola S, Burgess DH, Orrenius S (1996): Protease involvement in fodrin cleavage and phosphatidylserine exposure in apoptosis. J Biol Chem 271:31075-31081.
62. Wang KKW, Yuen P (1994): Calpain inhibition: an overview of its therapeutic potential. Trends Pharmacol Sci 15:412-419.
63. Wang KKW, Villalobo A, Roufogalis BD (1989): Calmodulin-binding proteins as calpain substrates. Biochem J 262:693-706.
64. Wang KKW, Nath R, Posner A, Rasier KJ, Buroker-Kilgore M, Hajimohammadreza I, Probert AW, Marcoux FW, Ye Q, Takano E, Hatanaka M, Maki M, Caner H, Collins JL, Fergus A, Lee KS, Lunney EA, Hays SJ, Yuen P (1996): An alphamercaptoacrylic acid derivative is a selective nonpeptide cell-permeable calpain inhibitor and is neuroprotective. Proc Natl Acad Sci USA 93:6687-6692.
65. Waterhouse N, Kumar S, SongQ, Strike P, Sparrow L, Dreyfuss G, Alnemri ES, Litwack G, Lavin M, Watters D (1996): Heteronuclear ribonucleoproteins C1 and C2, components of the spliceosome, are specific targets of interleukin 1-converting enzyme-like proteases in apoptosis. J Biol Chem 271:29335-29341.
66. Wyllie AH (1980): Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284:555-556.
67. Yakovlev AG, Knoblach SM, Fan L, Fox GB, Goodnight R, Faden AI (1997): Activation of CPP32-like caspases contributes to neuronal apoptosis and neurological dysfunction after traumatic brain injury. J Neurosci 17:7415-7424.
68. Yang J, Xuesong L, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng T, Jones DP, Wang X (1997): Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275:1129-1132.
69. Yuen P, Wang KKW (1996): Therapeutic potential of calpain inhibitors in neurodegenerative disorders. Exp Opin Invest Drugs 5:1291-1304.
70. Zhivotovsky B, Burgess DH, Vanags DM, Orrenius S (1997): Involvement of cellular proteolytic machinery in apoptosis. Biochem Biophys Res Commun 230:481-488.