Calpain is a major cell death effector in selective striatal degeneration induced in vivo by 3-nitropropionate: Implications for Huntington's disease

Journal of Neuroscience

Volumn 23, Issue 12, 2003, Pages 5020-5030

  Bizat, Nicolas ^a   Hermel, Jean Michel ^a   Boyer, Frédéric ^a   Jacquard, Carine ^a   Créminon, Christophe ^b   Ouary, Stéphane ^a   Escartin, Carole ^a   Hantraye, Philippe ^a   Krajewski, Stan ^c   Brouillet, Emmanuel ^a  

^a SERVICE HOSPITALIER FRÉDÉRIC JOLIOT   (France)

^b CEA SACLAY   (France)

^c BURNHAM INSTITUTE   (United States)

Author keywords

Calpain; Calpain inhibitor; Caspase; Excitotoxicity; Mitochondrial complex II inhibitor; Neurodegenerative disease; Neuroprotection

Indexed keywords

3 NITROPROPIONIC ACID; CALPAIN; CASPASE; HUNTINGTIN; N METHYL DEXTRO ASPARTIC ACID; PROTEINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEGENERATION; CELL DEATH; CONTROLLED STUDY; DISEASE COURSE; DNA STRUCTURE; DOSE TIME EFFECT RELATION; EFFECTOR CELL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUNTINGTON CHOREA; INHIBITION KINETICS; MALE; MITOCHONDRIAL MEMBRANE; NERVE EXCITABILITY; NEUROTOXICITY; NONHUMAN; OSMOTIC PUMP; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN PROCESSING; RAT; STRIATE CORTEX;

EID: 0037775906     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-12-05020.2003     Document Type: Article

References (60)

1. Albin RL, Greenamyre JT (1992) Alternative excitotoxic hypotheses. Neurology 42:733-738.
2. Beal MF (1992) Does impairment of energy metabolism result in excitotoxic neuronal death in neurodegenerative illness? Ann Neurol 31:119-130.
3. Beal MF (2000) Energetics in the pathogenesis of neurodegenerative disorders. Trends Neurosci 7:298-304.
4. Beal MF, Brouillet E, Jenkins B, Ferrante R, Kowall N, Miller J, Storey E, Srivastava R, Rosen B, Hyman BT (1993) Neurochemical and histologic characterization of the striatal lesions produced by the mitochondrial toxin 3-nitropropionic acid. J Neurosci 13:4181-4192.
5. Benchoua A, Guegan C, Couriaud C, Hosseini H, Sampaio N, Morin D, Onteniente B (2001) Specific caspase pathways are activated in the two stages of cerebral infarction. J Neurosci 21:7127-7134.
6. Blum D, Gall D, Galas MC, d'Alcantara P, Bantubungi K, Schiffmann SN (2002) The adenosine A1 receptor agonist ADAC exerts a neuroprotective effect against the development of striatal lesions and motor impairments in the 3-nitropropionic acid of neurotoxicity. J Neurosci 22:9122-9133.
7. Brouillet E, Guyot M-C, Mittoux V, Altairac S, Condé F, Palfi S, Hantraye P (1998) Partial inhibition of brain succinate dehydrogenase by 3-nitropropionic acid is sufficient to initiate striatal degeneration in Rat. J Neurochem 70:794-805.
8. Brouillet E, Condé F, Beal MF, Hantraye P (1999) Replicating Huntington's disease in experimental animals. Prog Neurobiol 59:427-458.
9. Browne SE, Bowling AC, Mac Garvey U, Baik MJ, Berger SC, Muqit MK, Bird ED, Beal MF (1997) Oxidative damage and metabolic dysfunction in Huntington's disease: selective vulnerability of the basal ganglia. Ann Neurol 41:646-653.
10. Calabresi P, Gubellini P, Picconi B, Centonze D, Pisani A, Bonsi P, Greengard P, Hipskind RA, Borrelli E, Bernardi G (2001) Inhibition of mitochondrial complex II induces a long-term potentiation of NMDA-mediated synaptic excitation in the striatum requiring endogenous dopamine. J Neurosci 21:5110-5120.
11. Cattaneo E, Rigamonti D, Goffredo D, Zuccato C, Squitieri F, Sipione S (2001) Loss of normal huntingtin function: new developments in Huntington's disease research. Trends Neurosci 24:182-188.
12. Cepeda C, Ariano MA, Calvert CR, Flores-Hernandez J, Chandler SH, Leavitt BR, Hayden MR, Levine MS (2001) NMDA receptor function in mouse models of Huntington disease. J Neurosci Res 66:525-539.
13. Chan SL, Mattson MP (1999) Caspase and calpain substrates: roles in synaptic plasticity and cell death. J Neurosci Res 58:167-190.
14. Dautry C, Vauffrey F, Brouillet E, Bizat N, Conde F, Bloch G, Hantraye P (2000) Early N-acetylaspartate depletion is a marker of neuronal dysfunction in rats and primates chronically treated with the mitochondrial toxin 3-nitropropionic acid. J Cereb Blood Flow Metab 20:789-799.
15. DiFiglia M (1990) Excitotoxic injury of the neostriatum: a model for Huntington's disease. Trends Neurosci 13:286-289.
16. Di Rosa G, Odrijin T, Nixon RA, Arancio O (2002) Calpain inhibitors: a treatment for Alzheimer's disease. J Mol Neurosci 19:135-141.
17. Du Y, Dodel RC, Bales KR, Jemmerson R, Hamilton-Byrd E, Paul SM (1997) Involvement of a caspase-3-like cysteine protease in 1-methyl-4-phenylpyridinium-mediated apoptosis of cultured cerebellar granule neurons. J Neurochem 69:1382-1388.
18. Duan W, Zhiong G, Mattson M (2000) Participation of Par-4 in the degeneration of striatal neurons induced by metabolic compromise with 3-nitropropionic acid. Exp Neurol 165:1-11.
19. Gafni J, Ellerby LM (2002) Calpain activation in Huntington's disease. J Neurosci 22:4842-4849.
20. Garcia M, Vanhoutte P, Pages C, Besson MJ, Brouillet E, Caboche J (2002) Activation of the c-jun-N-terminal kinase/c-Jun module occurs in striatal neurons in response to 3-nitropropionic acid: a comparative in vivo and in vitro analysis. J Neurosci 22:2174-2184.
21. Greene JG, Greenamyre JT (1995) Characterization of the excitotoxic potential of the reversible succinate dehydrogenase inhibitor malonate. J Neurochem 64:430-436.
22. Greene JG, Sheu S-S, Gross RA, Greenamyre JT (1998) 3-nitropropionic acid exacerbates N-methyl-D-aspartate toxicity in striatal culture by multiple mechanisms. Neuroscience 84:503-510.
23. Gu M, Gash MT, Mann VM, Javoy-Agid F, Cooper JM, Shapira AH (1996) Mitochondrial defect in Huntington's disease caudate nucleus. Ann Neurol 39:385-389.
24. Hackam AS, Singaraja R, Wellington CL, Metzler M, McCutcheon K, Zhang T, Kalchman M, Hayden MR (1998) The influence of huntingtin protein size on nuclear localization and cellular toxicity. J Cell Biol 141:1097-1105.
25. Harper PS (1991) Huntington's disease (Harper PS, ed). London: Saunders.
26. Hartmann A, Hunot S, Michel PP, Muriel MP, Vyas S, Faucheux BA, Mouatt-Prigent A, Turmel H, Srinivasan A, Ruberg M, Evan GI, Agid Y, Hirsch EC (2000) Caspase-3: a vulnerability factor and final effector in apoptotic death of dopaminergic neurons in Parkinson's disease. Proc Natl Acad Sci USA 97:2875-2880.
27. Hermel J-M, Dirkx R, Solimena M (1999) Post-translational modifications of ICA512 a receptor tyrosine phosphatase-like protein of secretory granules. Eur J Neurosci 11:2609-2620.
28. Huntington's Disease Collaborative Research Group (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72:971-983.
29. Jenkins BG, Koroshetz WJ, Beal MF, Rosen R (1993) Evidence for an energy metabolic defect in Huntington's Disease using localized proton spectroscopy. Neurology 43:2689-2693.
30. Jenkins BG, Rosas HD, Chen YCI, Makabe T, Myers R, MacDonald M, Rosen BR, Beal MF, Koroshetz WJ (1998) 1H NMR spectroscopy studies of Huntington's Disease correlation with CAG repeat numbers. Neurology 50:1357-1365.
31. Kim GW, Copin JC, Kawase M, Chen SF, Sato S, Gobbel GT, Chan PH (2000) Excitotoxicity is required for induction of oxidative stress and apoptosis in mouse striatum by the mitochondrial toxin 3-nitropropionic acid. J Cereb Blood Flow Metab 20:119-129.
32. Kim YJ, Yi Y, Sapp E, Wang Y, Cuiffo B, Kegel KB, Qin ZH, Aronin N, DiFiglia M (2001) Caspase-3-cleaved N-terminal fragments of wild-type and mutant huntingtin are present in normal and Huntington's disease brains associate with membranes and undergo calpain-dependent proteolysis. Proc Natl Acad Sci USA 98:12784-12789.
33. Krajewski S, Krajewska M, Ellerby LM, Welsh K, Xie Z, Deveraux QL, Salvesen GS, Bredesen DE, Rosenthal RE, Fiskum G, Reed JC (1999) Release of caspase-9 from mitochondria during neuronal apoptosis and cerebral ischemia. Proc Natl Acad Sci USA 96:5752-5757.
34. Laforet GA, Sapp E, Chase K, McIntyre C, Boyce FM, Campbell M, Cadigan BA, Warzecki L, Tagle DA, Reddy PH, Cepeda C, Calvert CR, Jokel ES, Klapstein GJ, Ariano MA, Levine MS, DiFiglia M, Aronin N (2001) Changes in cortical and striatal neurons predict behavioral and electrophysiological abnormalities in a transgenic murine model of Huntington's disease. J Neurosci 21:9112-9123.
35. Lee M-S, Kwon YT, Li M, Peng J, Friedlander RM, Tsai LH (2000) Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 405:360-364.
36. Leist M, Volbracht C, Fava E, Nicotera P (1998) 1-Methyl-4-phenylpy ridinium induces autocrine excitotoxicity protease activation and neuronal apoptosis. Mol Pharmacol 54:789-801.
37. McDonald MC, Mota-Filipe H, Paul A, Cuzzocrea S, Adbelrahman M, Harwood S, Plevin R, Chatterje PK, Yaqoob MM, Thiemermann C (2001) Calpain inhibitor I reduces the activation of nuclear factor-kappaB and organ injury/dysfunction in hemorrhagic shock. FASEB 15:171-186.
38. Mittoux V, Ouary S, Monville C, Lisovoski F, Poyot T, Conde F, Escartin C, Robichon R, Brouillet E, Peschanski M, Hantraye P (2002) Corticostriatopallidal neuroprotection by adenovirus-mediated ciliary neurotrophic factor gene transfer in a rat model of progressive striatal degeneration. J Neurosci 22:4478-4486.
39. Namura S, Zhu J, Fink K, Endres M, Srinivasan A, Tomaselli KJ, Yuan J, Moskowitz MA (1998) Activation and cleavage of caspase-3 in apoptosis induced by experimental cerebral ischemia. J Neurosci 18:3659-3668.
40. Newcomb-Fernandez JK, Zhao X, Pike BR, Wang KK, Kampfl A, Beer R, DeFord SM, Hayes RL (2001) Concurrent assessment of calpain and caspase-3 activation after oxygen-glucose deprivation in primary septo-hippocampal cultures. J Cereb Blood Flow Metab 21:1281-1294.
41. Nicholson DW, Thornberry NA (1997) Caspases: killer proteases. Trends Biochem Sci 22:299-306.
42. Ohgoh M, Shimizu H, Ogura H, Nishizawa Y (2000) Astroglial trophic support and neuronal cell death: Influence of cellular energy level on type of cell death influenced by mitochondrial toxin in cultured rat cortical neurons. J Neurochem 75:925-933.
43. Ouary S, Bizat N, Altérac S, Ménétrat H, Mittoux V, Condé F, Hantraye P, Brouillet E (2000) Major strain differences in response to chronic systemic administration of the mitochondrial toxin 3-nitropropionate in rats: implications for neuroprotection studies. Neurosci 97:521-530.
44. Panov AV, Gutekunst CA, Leavitt BR, Hayden MR, Burke JR, Strittmatter WJ, Greenamyre JT (2002) Early mitochondrial calcium defects in Huntington's disease are a direct effect of polyglutamines. Nat Neurosci 5:731-736.
45. Peng TI, Greenamyre JT (1998) Privileged access to mitochondria of calcium influx through N-methyl-D-aspartate receptors. Mol Pharmacol 53:974-980.
46. Petersen A, Mani K, Brundin P (1999) Recent advances on the pathogenesis of Huntington's disease. Exp Neurol 157:1-18.
47. Qin Z, Wang Y, Chasea TN (2000) A caspase-3-like protease is involved in NF-kappaB activation induced by stimulation of N-methyl-D-aspartate receptors in rat striatum. Brain Res Mol Brain Res 80:111-122.
48. Sanchez I, Xu CJ, Juo P, Kakizaka A, Blenis J, Yuan J (1999) Caspase-8 is required for cell death induced by expanded polyglutamine repeats. Neuron 22:623-633.
49. Saudou F, Finkbeiner S, Devys D, Greenberg M (1998) Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell 95:55-66.
50. Sawa A, Wiegand GW, Cooper J, Margolis R, Sharp AH, Lawler JF, Greenamyre JT, Snyder SH, Ross C (1999) Increased apoptosis of Huntington disease lymphoblasts associated with repeat length- dependent mitochondrial depolarization. Nat Med 5:1194-1198.
51. Schulz JB, Weller M, Matthews RT, Heneka MT, Groscurth P, Martinou JC, Lommatzsch J, Coelin RV, Wulner U, Loschmann PA, Beal MF, Dichgans J, Klockgether T (1998) Extended therapeutic window for caspase inhibition and synergy with MK-801 in the treatment of cerebral histotoxic hypoxia. Cell Death Differ 5:847-857.
52. Simpson JR, Isacson O (1993) Mitochondrial impairment reduces the threshold for in vivo NMDA-mediated neuronal death in the striatum. Exp Neurol 121:57-64.
53. Stoka V, Turk B, Schendel S, Cirman T, Snipas SJ, Ellerby L, Bredesen D, Freeze H, Abrahamson M, Broemme D, Krajewski S, Reed JC, Yin X-M, Turk V, Salvesen G (2001) Lysosomal protease pathways to apoptosis: cleavage of BID, not pro-caspases, is the most likely route. J Biol Chem 276:3149-3157.
54. Tabrizi SJ, Cleeter MW, Xuereb J, Taanman J-W, Cooper JM, Shapira AHV (1999) Biochemical abnormalities and excitotoxicity in Huntington's disease brain. Ann Neurol 45:25-32.
55. Tompa P, Baki A, Schad E, Friedrich P (1996) The calpain cascade. Mucalpain activates m-calpain. J Biol Chem 271:33161-33164.
56. Wang K (2000) Calpain and caspase: can you tell the difference? Trends Neurosci 23:20-26.
57. Wellington CL, Ellerby LM, Gutekunst CA, Rogers D, Warby S, Graham RK, Loubser O, van Raamsdonk J, Singaraja R, Yang YZ, Gafni J, Bredesen D, Hersch SM, Leavitt BR, Roy S, Nicholson DW, Hayden MR (2002) Caspase cleavage of mutant huntingtin precedes neurodegeneration in Huntington's disease. J Neurosci 22:7862-7872.
58. Wüliner U, Young A, Penney J, Beal MF (1994) 3-nitropropionic acid toxicity in the striatum. J Neurochem 63:1772-1781.
59. Zeevalk GD, Derr-Yellin E, Nicklas WJ (1995) Relative vulnerability of dopamine and GABA neurons in mesencephalic culture to inhibition of succinate dehydrogenase by malonate and 3-nitropropionic acid and protection by NMDA receptor blockade. J Pharmacol Exp Ther 275:1124-1130.
60. Zeron MM, Hansson O, Chen N, Wellington CL, Leavitt BR, Brundin P, Hayden MR, Raymond LA (2002) Increased sensitivity to N-methyl-D-aspartate receptor-mediated excitotoxicity in a mouse model of Huntington's disease. Neuron 33:849-860.