Mitochondrial-dependent Ca2+ handling in Huntington's disease striatal cells: Effect of histone deacetylase inhibitors

Journal of Neuroscience

Volumn 26, Issue 43, 2006, Pages 11174-11186

  Oliveira, Jorge M A ^a,b,d   Chen, Sylvia ^b   Almeida, Sandra ^d   Riley, Rebeccah ^b   Gonçalves, Jorge ^a   Oliveira, Catarina R ^d   Hayden, Michael R ^c   Nicholls, David G ^b   Ellerby, Lisa M ^b   Rego, A Cristina ^d  

^a UNIVERSITY OF PORTO   (Portugal)

^b BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^d UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Calcium; Excitotoxicity; HDAC inhibitors; Huntington's disease; Mitochondria; Striatal neurons

Indexed keywords

BUTYRIC ACID; HISTONE DEACETYLASE INHIBITOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; ENZYME INHIBITOR; HISTONE DEACETYLASE;

ANIMAL MODEL; ARTICLE; CALCIUM CELL LEVEL; CELL DEATH; CELL FUNCTION; GLYCOLYSIS; HUNTINGTON CHOREA; MALE; MITOCHONDRIAL MEMBRANE; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; TRANSGENIC MOUSE; ANIMAL; CALCIUM SIGNALING; CELL CULTURE; COMPARATIVE STUDY; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM; MITOCHONDRION; NEOSTRIATUM; PHYSIOLOGY;

ANIMALS; CALCIUM SIGNALING; CELLS, CULTURED; ENZYME INHIBITORS; HISTONE DEACETYLASES; HUNTINGTON DISEASE; MALE; MICE; MICE, TRANSGENIC; MITOCHONDRIA; NEOSTRIATUM;

EID: 33751106144     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3004-06.2006     Document Type: Article

References (56)

1. 2+ ionophore on mitochondria in intact cells. Cell Calc 33:101-112.
2. Ajamian F, Salminen A, Reeben M (2004) Selective regulation of class I and class II histone deacetylases expression by inhibitors of histone deacetylases in cultured mouse neural cells. Neurosci Lett 365:64-68.
3. Ankarcrona M, Dypbukt JM, Bonfoco E, Zhivotovsky B, Orrenius S, Lipton SA, Nicotera P (1995) Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15:961-973.
4. Bates GP (2001) Huntington's disease. Exploiting expression. Nature 413:691, 693-694.
5. Beal MF (2005) Mitochondria take center stage in aging and neurodegeneration. Ann Neurol 58:495-505.
6. Beal MF, Ferrante RJ (2004) Experimental therapeutics in transgenic mouse models of Huntington's disease. Nat Rev Neurosci 5:373-384.
7. Bezprozvanny I, Hayden MR (2004) Deranged neuronal calcium signaling and Huntington disease. Biochem Biophys Res Commun 322:1310-1317.
8. Brown AM (2004) Brain glycogen re-awakened. J Neurochem 89:537-552.
9. Brustovetsky N, LaFrance R, Purl KJ, Brustovetsky T, Keene CD, Low WC, Dubinsky JM (2005) Age-dependent changes in the calcium sensitivity of striatal mitochondria in mouse models of Huntington's Disease. J Neurochem 93:1361-1370.
10. Calabresi P, Pisani A, Mercuri NB, Bernardi G (1996) The corticostriatal projection: from synaptic plasticity to dysfunctions of the basal ganglia. Trends Neurosci 19:19-24.
11. Cha JH (2000) Transcriptional dysregulation in Huntington's disease. Trends Neurosci 23:387-392.
12. Chan EY, Luthi-Carter R, Strand A, Solano SM, Hanson SA, DeJohn MM, Kooperberg C, Chase KO, DiFiglia M, Young AB, Leavitt BR, Cha JH, Aronin N, Hayden MR, Olson JM (2002) Increased huntingtin protein length reduces the number of polyglutamine-induced gene expression changes in mouse models of Huntington's disease. Hum Mol Genet 11:1939-1951.
13. Choo YS, Johnson GV, MacDonald M, Detloff PJ, Lesort M (2004) Mutant huntingtin directly increases susceptibility of mitochondria to the calcium-induced permeability transition and cytochrome c release. Hum Mol Genet 13:1407-1420.
14. Ferrante RJ, Kubilus JK, Lee J, Ryu H, Beesen A, Zucker B, Smith K, Kowall NW, Ratan RR, Luthi-Carter R, Hersch SM (2003) Histone deacetylase inhibition by sodium butyrate chemotherapy ameliorates the neurodegenerative phenotype in Huntington's disease mice. J Neurosci 23:9418-9427.
15. Galas MC, Bizat N, Cuvelier L, Bantubungi K, Brouillet E, Schiffmann SN, Blum D (2004) Death of cortical and striatal neurons induced by mitochondrial defect involves differential molecular mechanisms. Neurobiol Dis 15:152-159.
16. Gines S, Seong IS, Fossale E, Ivanova E, Trettel F, Gusella JF, Wheeler VC, Persichetti F, Macdonald ME (2003a) Specific progressive cAMP reduction implicates energy deficit in presymptomatic Huntington's disease knock-in mice. Hum Mol Genet 12:497-508.
17. Gines S, Ivanova E, Seong IS, Saura CA, Macdonald ME (2003b) Enhanced Akt signaling is an early pro-survival response that reflects N-methyl-D-aspartate receptor activation in Huntington's disease knock-in striatal cells. J Biol Chem 278:50514-50522.
18. Gusella JF, Macdonald ME (2000) Molecular genetics: unmasking polyglutamine triggers in neurodegenerative disease. Nat Rev Neurosci 1:109-115.
19. 2+ indicators excited with UV light. In: Handbook of fluorescent probes and research products, pp 776-781. Eugene, OR: Molecular Probes.
20. Herzig RP, Scacco S, Scarpulla RC (2000) Sequential serum-dependent activation of CREB and NRF-1 leads to enhanced mitochondrial respiration through the induction of cytochrome c. J Biol Chem 275:13134-13141.
21. Hughes RE (2002) Polyglutamine disease: acetyltransferases awry. Curr Biol 12:R141-R143.
22. Huntington's Disease Collaborative Research Group (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. The Huntington's Disease Collaborative Research Group. Cell 72:971-983.
23. Kanai H, Sawa A, Chen RW, Leeds P, Chuang DM (2004) Valproic acid inhibits histone deacetylase activity and suppresses excitotoxicity-induced GAPDH nuclear accumulation and apoptotic death in neurons. Pharmacogenomics J 4:336-344.
24. Kawaguchi Y (1997) Neostriatal cell subtypes and their functional roles. Neurosci Res 27:1-8.
25. Kennedy L, Evans E, Chen CM, Craven L, Detloff PJ, Ennis M, Shelbourne PF (2003) Dramatic tissue-specific mutation length increases are an early molecular event in Huntington disease pathogenesis. Hum Mol Genet 12:3359-3367.
26. Li L, Fan M, Icton CD, Chen N, Leavitt BR, Hayden MR, Murphy TH, Raymond LA (2003) Role of NR2B-type NMDA receptors in selective neurodegeneration in Huntington disease. Neurobiol Aging 24:1113-1121.
27. Mao L, Wang JQ (2001) Upregulation of preprodynorphin and preproenkephalin mRNA expression by selective activation of group I metabotropic glutamate receptors in characterized primary cultures of rat striatal neurons. Brain Res Mol Brain Res 86:125-137.
28. Mao Z, Choo YS, Lesort M (2006) Cystamine and cysteamine prevent 3-NP-induced mitochondrial depolarization of Huntington's disease knock-in striatal cells. Eur J Neurosci 23:1701-1710.
29. Mariadason JM, Corner GA, Augenlicht LH (2000) Genetic reprogramming in pathways of colonic cell maturation induced by short chain fatty acids: comparison with trichostatin A, sulindac, and curcumin and implications for chemoprevention of colon cancer. Cancer Res 60:4561-4572.
30. McGuinness MC, Lu JF, Zhang HP, Dong GX, Heinzer AK, Watkins PA, Powers J, Smith KD (2003) Role of ALDP (ABCD1) and mitochondria in X-linked adrenoleukodystrophy. Mol Cell Biol 23:744-753.
31. Michael LF, Asahara H, Shulman AI, Kraus WL, Montminy M (2000) The phosphorylation status of a cyclic AMP-responsive activator is modulated via a chromatin-dependent mechanism. Mol Cell Biol 20:1596-1603.
32. Milakovic T, Johnson GV (2005) Mitochondrial respiration and ATP production are significantly impaired in striatal cells expressing mutant huntingtin. J Biol Chem 280:30773-30782.
33. Napolitano M, Centonze D, Gubellini P, Rossi S, Spiezia S, Bernardi G, Gulino A, Calabresi P (2004) Inhibition of mitochondrial complex II alters striatal expression of genes involved in glutamatergic and dopaminergic signaling: possible implications for Huntington's disease. Neurobiol Dis 15:407-414.
34. Nicholls DG (2004) Mitochondrial dysfunction and glutamate excitotoxicity studied in primary neuronal cultures. Curr Mol Med 4:149-177.
35. Nicholls DG (2006) Simultaneous monitoring of ionophore- and inhibitor-mediated plasma and mitochondrial membrane potential changes in cultured neurons. J Biol Chem 281:14864-14874.
36. Nicholls DG, Budd SL (2000) Mitochondria and neuronal survival. Physiol Rev 80:315-360.
37. 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.
38. Petersen A, Brundin P (1999) Effects of ciliary neurotrophic factor on excitotoxicity and calcium-ionophore A23187-induced cell death in cultured embryonic striatal neurons. Exp Neurol 160:402-412.
39. Petersen A, Castilho RF, Hansson O, Wieloch T, Brundin P (2000) Oxidative stress, mitochondrial permeability transition and activation of caspases in calcium ionophore A23187-induced death of cultured striatal neurons. Brain Res 857:20-29.
40. Rego AC, Ward MW, Nicholls DG (2001) Mitochondria control AMPA/kainate receptor-induced cytoplasmic calcium deregulation in rat cerebellar granule cells. J Neurosci 21:1893-1901.
41. Reiner A, Albin RL, Anderson KD, D'Amato CJ, Penney JB, Young AB (1988) Differential loss of striatal projection neurons in Huntington disease. Proc Natl Acad Sci USA 85:5733-5737.
42. Ruan Q, Lesort M, Macdonald ME, Johnson GV (2004) Striatal cells from mutant huntingtin knock-in mice are selectively vulnerable to mitochondrial complex II inhibitor-induced cell death through a non-apoptotic pathway. Hum Mol Genet 13:669-681.
43. Ryu H, Lee J, Olofsson BA, Mwidau A, Dedeoglu A, Escudero M, Flemington E, Azizkhan-Clifford J, Ferrante RJ, Ratan RR (2003) Histone deacetylase inhibitors prevent oxidative neuronal death independent of expanded polyglutamine repeats via an Sp1-dependent pathway. Proc Natl Acad Sci USA 100:4281-4286.
44. Saulle E, Gubellini P, Picconi B, Centonze D, Tropepi D, Pisani A, Morari M, Marti M, Rossi L, Papa M, Bernardi G, Calabresi P (2004) Neuronal vulnerability following inhibition of mitochondrial complex II: a possible ionic mechanism for Huntington's disease. Mol Cell Neurosci 25:9-20.
45. Seong IS, Ivanova E, Lee JM, Choo YS, Fossale E, Anderson M, Gusella JF, Laramie JM, Myers RH, Lesort M, MacDonald ME (2005) HD CAG repeat implicates a dominant property of huntingtin in mitochondrial energy metabolism. Hum Mol Genet 14:2871-2880.
46. Slow EJ, van Raamsdonk J, Rogers D, Coleman SH, Graham RK, Deng Y, Oh R, Bissada N, Hossain SM, Yang YZ, Li XJ, Simpson EM, Gutekunst CA, Leavitt BR, Hayden MR (2003) Selective striatal neuronal loss in a YAC128 mouse model of Huntington disease. Hum Mol Genet 12:1555-1567.
47. Steffan JS, Kazantsev A, Spasic-Boskovic O, Greenwald M, Zhu YZ, Gohler H, Wanker EE, Bates GP, Housman DE, Thompson LM (2000) The Huntington's disease protein interacts with p53 and CREB-binding protein and represses transcription. Proc Natl Acad Sci USA 97:6763-6768.
48. Sugars KL, Rubinsztein DC (2003) Transcriptional abnormalities in Huntington disease. Trends Genet 19:233-238.
49. Tobin AJ, Signer ER (2000) Huntington's disease: the challenge for cell biologists. Trends Cell Biol 10:531-536.
50. Trettel F, Rigamonti D, Hilditch-Maguire P, Wheeler VC, Sharp AH, Persichetti F, Cattaneo E, Macdonald ME (2000) Dominant phenotypes produced by the HD mutation in STHdh(Q111) striatal cells. Hum Mol Genet 9:2799-2809.
51. Tymianski M, Charlton MP, Carlen PL, Tator CH (1993) Source specificity of early calcium neurotoxicity in cultured embryonic spinal neurons. J Neurosci 13:2085-2104.
52. Vonsattel JP, DiFiglia M (1998) Huntington disease. J Neuropathol Exp Neurol 57:369-384.
53. Wang J, Gines S, Macdonald ME, Gusella JF (2005) Reversal of a full-length mutant huntingtin neuronal cell phenotype by chemical inhibitors of polyglutamine-mediated aggregation. BMC Neurosci 6:1.
54. Ward MW, Rego AC, Frenguelli BG, Nicholls DG (2000) Mitochondrial membrane potential and glutamate excitotoxicity in cultured cerebellar granule cells. J Neurosci 20:7208-7219.
55. Wokosin DL, Loughrey CM, Smith GL (2004) Characterization of a range of fura dyes with two-photon excitation. Biophys J 86:1726-1738.
56. Zeron MM, Fernandes HB, Krebs C, Shehadeh J, Wellington CL, Leavitt BR, Baimbridge KG, Hayden MR, Raymond LA (2004) Potentiation of NMDA receptor-mediated excitotoxicity linked with intrinsic apoptotic pathway in YAC transgenic mouse model of Huntington's disease. Mol Cell Neurosci 25:469-479.