Opposing roles for caspase and calpain death proteases in l-glutamate-induced oxidative neurotoxicity

Toxicology and Applied Pharmacology

Volumn 232, Issue 2, 2008, Pages 258-267

  Elphick, Lucy M ^a   Hawat, Mohammad ^a   Toms, Nick J ^b   Meinander, Annika ^c,d   Mikhailov, Andrey ^c,d   Eriksson, John E ^c,d   Kass, George E N ^a  

^a UNIVERSITY OF SURREY   (United Kingdom)

^b PENINSULA MEDICAL SCHOOL   (United Kingdom)

^c TURKU CENTRE FOR BIOTECHNOLOGY   (Finland)

^d ÅBO AKADEMI UNIVERSITY   (Finland)

Author keywords

Apoptosis; Calcium; Calpains; Caspases; Ischemic injury; Necrosis; Stroke

Indexed keywords

ACETYLCYSTEINE; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; CALPAIN; CASPASE; CASPASE 8; CASPASE 9; CASPASE INHIBITOR; CYTOCHROME C; GLUTAMIC ACID; PROTEINASE; REACTIVE OXYGEN METABOLITE;

ARTICLE; CALCIUM CELL LEVEL; CHROMATIN CONDENSATION; CONTROLLED STUDY; CYTOTOXICITY; DNA FRAGMENTATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; NEUROTOXICITY;

ANIMALS; CALPAIN; CASPASES; CELL DEATH; CELLS, CULTURED; GLUTAMIC ACID; MICE; NEURONS; OXIDATIVE STRESS; PROTEASE INHIBITORS;

MURINAE;

EID: 52049118749     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2008.07.008     Document Type: Article

References (64)

1. Andreau K., Castedo M., Perfettini J.L., Roumier T., Pichart E., Souquere S., Vivet S., Larochette N., and Kroemer G. Preapoptotic chromatin condensation upstream of the mitochondrial checkpoint. J. Biol. Chem. 279 (2004) 55937-55945
2. Arataki S., Tomizawa K., Moriwaki A., Nishida K., Matsushita M., Ozaki T., Kunisada T., Yoshida A., Inoue H., and Matsui H. Calpain inhibitors prevent neuronal cell death and ameliorate motor disturbances after compression-induced spinal cord injury in rats. J. Neurotrauma 22 (2005) 398-406
3. Arnoult D., Parone P., Martinou J.C., Antonsson B., Estaquier J., and Ameisen J.C. Mitochondrial release of apoptosis-inducing factor occurs downstream of cytochrome c release in response to several proapoptotic stimuli. J. Cell Biol.. 159 (2002) 923-929
4. Bannai S. Exchange of cystine and glutamate across plasma membrane of human fibroblasts. J. Biol. Chem. 261 (1986) 2256-2263
5. Bezvenyuk Z., Miettinen R., and Solovyan V. Chromatin condensation during glutamate-induced excitotoxicity of celebellar granule neurons precedes disintegration of nuclear DNA into high molecular weight DNA fragments. Mol. Brain Res. 110 (2003) 140-146
6. Bizat N., Hermel J.M., Humbert S., Jacquard C., Creminon C., Escartin C., Saudou F., Krajewski S., Hantraye P., and Brouillet E. In vivo calpain/caspase cross-talk during 3-nitropropionic acid-induced striatal degeneration-implication of a calpain-mediated cleavage of active caspase-3. J. Biol. Chem. 278 (2003) 43245-43253
7. Cauwels A., Janssen B., Waeytens A., Cuvelier C., and Brouckaert P. Caspase inhibition causes hyperacute tumor necrosis factor-induced shock via oxidative stress and phospholipase A2. Nature Immunol. 4 (2003) 387-393
8. Chipuk J.E., and Green D.R. Do inducers of apoptosis trigger caspase-independent cell death? Nature Rev. Mol. Cell Biol. 6 (2005) 268-275
9. Cho S.G., Liu D., Fairman D., Li P., Jenkins L., McGonigle P., and Wood A. Spatiotemporal evidence of apoptosis-mediated ischemic injury in organotypic hippocampal slice cultures. Neurochem. Int. 45 (2004) 117-127
10. Dargusch R., and Schubert D. Specificity of resistance to oxidative stress. J. Neurochem. 81 (2002) 1394-1400
11. Das A., Sribnick E.A., Wingrave J.M., Del Re A.M., Woodward J.J., Appel S.H., Banik N.L., and Ray S.K. Calpain activation in apoptosis of ventral spinal cord 4.1 (VSC4.1) motoneurons exposed to glutamate: calpain inhibition provides functional neuroprotection. J. Neurosci. Res. 81 (2005) 551-562
12. Davis J.B., and Maher P. Protein kinase C activation inhibits glutamate-induced cytotoxicity in a neuronal cell line. Brain Res. 652 (1994) 169-173
13. Dhanjal P., and Fry J.R. Determinants of MTT reduction in rat hepatocytes. Biomarkers 2 (1997) 111-116
14. Dohrman A., Kataoka T., Cuenin S., Russell J.Q., Tschopp J., and Budd R.C. Cellular FLIP (long form) regulates CD8(+) T cell activation through caspase-8-dependent NF-kappa B activation. J. Immunol. 174 (2005) 5270-5278
15. Dutta S., Chiu Y.C., Probert A.W., and Wang K.K.W. Selective release of calpain produced aII-spectrin (a-fodrin) breakdown products by acute neuronal cell death. Biol. Chem. 383 (2002) 785-791
16. El-Hassan H., Anwar K., Macanas-Pirard P., Crabtree M., Chow S.C., Johnson V.L., Lee P.C., Hinton R.H., Price S.C., and Kass G.E.N. Involvement of mitochondria in acetaminophen-induced apoptosis and hepatic injury: roles of cytochrome c, bax, bid and caspases. Toxicol. Appl. Pharmacol. 191 (2003) 118-129
17. Elphick L., Meinander A., Mikhailov A., Richard M., Toms N.J., Eriksson J.E., and Kass G.E.N. Live cell detection of caspase-3 activation by a Discosoma-red-fluorescent protein-based fluorescence resonance energy transfer construct. Anal. Biochem. 349 (2006) 148-155
18. Friedrich P. The intriguing Ca2+ requirement of calpain activation. Biochem. Biophys. Res. Commun. 323 (2004) 1131-1133
19. Ha J.S., and Park S.S. Glutamate-induced oxidative stress, but not cell death, is largely dependent upon extracellular calcium in mouse neuronal HT22 cells. Neurosci. Lett. 393 (2006) 165-169
20. Halliwell B., and Gutteridge J.M.C. Free Radicals in Biology and Medicine (1999), Oxford University Press, Oxford
21. Herrera F., Martin V., Garcia-Santos G., Rodriguez-Blanco J., Antolin I., and Rodriguez C. Melatonin prevents glutamate-induced oxytosis in the HT22 mouse hippocampal cell line through an antioxidant effect specifically targeting mitochondria. J. Neurochem. 100 (2007) 736-746
22. Johnson V.L., Ko S.C.W., Holmstrom T.H., Eriksson J.E., and Chow S.C. Effector caspases are dispensable for the early nuclear morphological changes during chemical-induced apoptosis. J. Cell Sci. 113 (2000) 2941-2953
23. Jones R.A., Johnson V.L., Buck N.R., Dobrota M., Hinton R.H., Chow S.C., and Kass G.E.N. Fas-mediated apoptosis in mouse hepatocytes involves the processing and activation of caspases. Hepatology 27 (1998) 1632-1642
24. Kass G.E.N., Eriksson J.E., Weis M., Orrenius S., and Chow S.C. Chromatin condensation during apoptosis requires ATP. Biochem. J. 318 (1996) 749-752
25. Kawamura M., Nakajima W., Ishida A., Ohmura A., Miura S., and Takada G. Calpain inhibitor MDL 28170 protects hypoxic-ischemic brain injury in neonatal rats by inhibition of both apoptosis and necrosis. Brain Res. 1037 (2005) 59-69
26. Kim S.O., and Han J.H. Pan-caspase inhibitor zVAD enhances cell death in RAW246.7 macrophages. J. Endotox. Res. 7 (2001) 292-296
27. Kumar S. Caspase function in programmed cell death. Cell Death Diff. 14 (2007) 32-43
28. Lankiewicz S., Luetjens C.M., Bui N.T., Krohn A.J., Poppe M., Cole G.M., Saido T.C., and Prehn J.H.M. Activation of calpain I converts excitotoxic neuron death into a caspase-independent cell death. J. Biol. Chem. 275 (2000) 17064-17071
29. Lemmers B., Salmena L., Bidere N., Su H., Matysiak-Zablocki E., Murakami K., Ohashi P.S., Jurisicova A., Lenardo M., Hakem R., and Hakem A. Essential role for caspase-8 in toll-like receptors and NF kappa B signaling. J. Biol. Chem. 282 (2007) 7416-7423
30. Liu C.Y., Takemasa A., Liles W.C., Goodman R.B., Jonas M., Rosen H., Chi E., Winn R.K., Harlan J.M., and Chuang P.I. Broad-spectrum caspase inhibition paradoxically augments cell death in TNF-a-stimulated neutrophils. Blood 101 (2003) 295-304
31. Lobner D. Comparison of the LDH and MTT assays for quantifying cell death: validity for neuronal apoptosis?. J. Neurosci. Meth. 96 (2000) 147-152
32. Macanas-Pirard P., Yaacob N.S., Lee P.C., Holder J.C., Hinton R.H., and Kass G.E.N. Glycogen synthase kinase-3 mediates acetaminophen-induced apoptosis in human hepatoma cells. J. Pharmacol. Exp. Ther. 313 (2005) 780-789
33. Markgraf C.G., Velayo N.L., Johnson M.P., McCarty D.R., Medhi S., Koehl J.R., Chmielewski P.A., and Linnik M.D. Six-hour window of opportunity for calpain inhibition in focal cerebral ischemia in rats. Stroke 29 (1998) 152-158
34. Martinet W., De Meyer G.R.Y., Timmermans J.P., Herman A.G., and Kockx M.M. Macrophages but not smooth muscle cells undergo benzyloxycarbonyl-Val-Ala-DL-Asp(O-methyl)-fluoromethylketone-induced nonapoptotic cell death depending on receptor-interacting protein 1 expression: implications for the stabilization of macrophage-rich atherosclerotic plaques. J. Pharmacol. Exp. Ther. 317 (2006) 1356-1364
35. May M.J., and Madge L.A. Caspase inhibition sensitizes inhibitor of NF-kappa B kinase beta-deficient fibroblasts to caspase-independent cell death via the generation of reactive oxygen species. J. Biol. Chem. 282 (2007) 16105-16116
36. Momeni H.R., and Kanje M. The calpain inhibitor VI prevents apoptosis of adult motor neurons. Neurorep. 16 (2005) 1065-1068
37. Noh H.S., Hah Y.S., Nilufar R., Han J.H., Bong J.H., Kang S.S., Cho G.J., and Choi W.S. Acetoacetate protects neuronal cells from oxidative glutamate toxicity. J. Neurosci. Res. 83 (2006) 702-709
38. Pike B.R., Zhao X.R., Newcomb J.K., Posmantur R.M., Wang K.K.W., and Hayes R.L. Regional calpain and caspase-3 proteolysis of a-spectrin after traumatic brain injury. Neurorep. 9 (1998) 2437-2442
39. Prabhakaran K., Li L., Borowitz J.L., and Isom G.E. Caspase inhibition switches the mode of cell death induced by cyanide by enhancing reactive oxygen species generation and PARP-1 activation. Toxicol. Appl. Pharmacol. 195 (2004) 194-202
40. Rami A. Ischemic neuronal death in the rat hippocampus: the calpain-calpastatin-caspase hypothesis. Neurobiol. Dis. 13 (2003) 75-88
41. Riedl S.J., and Shi Y.G. Molecular mechanisms of caspase regulation during apoptosis. Nature Rev. Mol. Cell Biol. 5 (2004) 897-907
42. Rossler O.G., Giehl K.M., and Thiel G. Neuroprotection of immortalized hippocampal neurones by brain-derived neurotrophic factor and Raf-1 protein kinase: role of extracellular signal-regulated protein kinase and phosphatidylinositol 3-kinase. J. Neurochem. 88 (2004) 1240-1252
43. Ruchaud S., Korfali N., Villa P., Kottke T.J., Dingwall C., Kaufmann S.H., and Earnshaw W.C. Caspase-6 gene disruption reveals a requirement for lamin A cleavage in apoptotic chromatin condensation. EMBO J. 21 (2002) 1967-1977
44. Sato H., Tamba M., Ishii T., and Bannai S. Cloning and expression of a plasma membrane cystine/glutamate exchange transporter composed of two distinct proteins. J. Biol. Chem. 274 (1999) 11455-11458
45. Satoh T., Nakatsuka D., Watanabe Y., Nagata I., Kikuchi H., and Namura S. Neuroprotection by MAPK/ERK kinase inhibition with U0126 against oxidative stress in a mouse neuronal cell line and rat primary cultured cortical neurons. Neurosci. Lett. 288 (2000) 163-166
46. Schubert D., Kimura H., and Maher P. Growth factors and vitamin E modify neuronal glutamate toxicity. Proc. Natl. Acad. Sci. USA 89 (1992) 8264-8267
47. Shah N., Asch R.J., Lysholm A.S., and Lebien T.W. Enhancement of stress-induced apoptosis in B-lineage cells by caspase-9 inhibitor. Blood. 104 (2004) 2873-2878
48. Simonian N.A., and Coyle J.T. Oxidative stress in neurodegenerative diseases. Annu. Rev. Pharmacol. Toxicol. 36 (1996) 83-106
49. Stanciu M., and DeFranco D.B. Prolonged nuclear retention of activated extracellular signal-regulated protein kinase promotes cell death generated by oxidative toxicity or proteasome inhibition in a neuronal cell line. J. Biol. Chem. 277 (2002) 4010-4017
50. 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., and Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397 (1999) 441-446
51. Takano J., Tomioka M., Tsubuki S., Higuchi M., Iwata N., Itohara S., Maki M., and Saido T.C. Calpain mediates excitotoxic DNA fragmentation via mitochondrial pathways in adult brains-evidence from calpastatin mutant mice. J. Biol. Chem. 280 (2005) 16175-16184
52. Tan S.L., Sagara Y., Lin Y.B., Maher P., and Schubert D. The regulation of reactive oxygen species production during programmed cell death. J. Cell Biol. 141 (1998) 1423-1432
53. Tan S.L., Wood M., and Maher P. Oxidative stress induces a form of programmed cell death with characteristics of both apoptosis and necrosis in neuronal cells. J. Neurochem. 71 (1998) 95-105
54. Toyota H., Yanase N., Yoshimoto T., Moriyama M., Sudo T., and Mizuguchi J. Calpain-induced Bax-cleavage product is a more potent inducer of apoptotic cell death than wild-type Bax. Cancer Lett. 189 (2003) 221-230
55. Uchiyama R., Kawamura I., Fujimura T., Kawanishi M., Tsuchiya K., Tominaga T., Kaku T., Fukasawa Y., Sakai S., Nomura T., and Mitsuyama M. Involvement of caspase-9 in the inhibition of necrosis of RAW 264 cells infected with Mycobacterium tuberculosis. Infection and Immunity 75 (2007) 2894-2902
56. 2+ influx and not via calpain inhibition. Neuropharmacol. 42 (2002) 706-713
57. van Leyen K., Siddiq A., Ratan R.R., and Lo E.H. Proteasome inhibition protects HT22 neuronal cells from oxidative glutamate toxicity. J. Neurochem. 92 (2005) 824-830
58. Vercammen D., Beyaert R., Denecker G., Goossens V., Van Loo G., Declercq W., Grooten J., Fiers W., and Vandenabeele P. Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J. Exp. Med. 187 (1998) 1477-1485
59. Wang K.K. Calpain and caspase: can you tell the difference?. Trends Neurosci. 23 (2000) 20-26
60. Wood D.E., Thomas A., Devi L.A., Berman Y., Beavis R.C., Reed J.C., and Newcomb E.W. Bax cleavage is mediated by calpain during drug-induced apoptosis. Oncogene 17 (1998) 1069-1078
61. Yu L., Wan F.Y., Dutta S., Welsh S., Liu Z.H., Freundt E., Baehrecke E.H., and Lenardo M. Autophagic programmed cell death by selective catalase degradation. Proceedings of the National Academy of Sciences of the United States of America 103 (2006) 4952-4957
62. Zhang Y.M., and Bhavnani B.R. Glutamate-induced apoptosis in neuronal cells is mediated via caspase-dependent and independent mechanisms involving calpain and caspase-3 proteases as well as apoptosis inducing factor (AIF) and this process is inhibited by equine estrogens. BMC Neurosci. 7 (2006)
63. Zhao L.X., Chen Q., and Brinton R.D. Neuroprotective and neurotrophic efficacy of phytoestrogens in cultured hippocampal neurons. Experimental Biology and Medicine 227 (2002) 509-519
64. Zheng T.S., Schlosser S.F., Dao T., Hingorani R., Crispe I.N., Boyer J.L., and Flavell R.A. Caspase-3 controls both cytoplasmic and nuclear events associated with Fas-mediated apoptosis in vivo. Proc. Natl. Acad. Sci. USA 95 (1998) 13618-13623