Mitochondrial sensitivity and altered calcium handling underlie enhanced NMDA-induced apoptosis in YAC128 model of Huntington's disease

Journal of Neuroscience

Volumn 27, Issue 50, 2007, Pages 13614-13623

  Fernandes, Herman B ^a,b   Baimbridge, Kenneth G ^a   Church, John ^a   Hayden, Michael R ^a,b   Raymond, Lynn A ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Calcium; Mitochondria; Mutant huntingtin; NMDA receptor; Ratiometric imaging; Striatal neurons

Indexed keywords

CALCIUM; GLUTAMINE; HUNTINGTIN; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POTASSIUM ION;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; CYTOSOL; EXCITOTOXICITY; HUNTINGTON CHOREA; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL PERMEABILITY; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALS; APOPTOSIS; BONGKREKIC ACID; CALCIUM; CALCIUM SIGNALING; CELLS, CULTURED; CYCLOSPORINE; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID AGONISTS; FLUORESCENT DYES; HUNTINGTON DISEASE; IONOPHORES; MICE; MICE, NEUROLOGIC MUTANTS; MITOCHONDRIA; N-METHYLASPARTATE; NEUROTOXINS; PATCH-CLAMP TECHNIQUES; RECEPTORS, N-METHYL-D-ASPARTATE; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 37249083913     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3455-07.2007     Document Type: Article

References (63)

1. Abdel-Hamid KM, Baimbridge KG (1997) The effects of artificial calcium buffers on calcium responses and glutamate-mediated excitotoxicity in cultured hippocampal neurons. Neuroscience 81:673-687.
2. Alano CC, Beutner G, Dirksen RT, Gross RA, Sheu SS (2002) Mitochondrial permeability transition and calcium dynamics in striatal neurons upon intense NMDA receptor activation. J Neurochem 80:531-538.
3. Banke TG, Traynelis SF (2003) Activation of NR1/NR2B NMDA receptors. Nat Neurosci 6:144-152.
4. 2+ exchanger in excitotoxicity. Cell 120:275-285.
5. Bittenbender JB, Quadfasel FA (1962) Rigid and akinetic forms of Huntington's chorea. Arch Neurol 7:275-288.
6. Brinkman RR, Mezei MM, Theilmann J, Almqvist E, Hayden MR (1997) The likelihood of being affected with Huntington disease by a particular age, for a specific CAG size. Am J Hum Genet 60:1202-1210.
7. Brocard JB, Tassetto M, Reynolds IJ (2001) Quantitative evaluation of mitochondrial calcium content in rat cortical neurones following a glutamate stimulus. J Physiol (Lond) 531:793-805.
8. Brustovetsky N, Brustovetsky T, Purl KJ, Capano M, Crompton M, Dubinsky JM (2003) Increased susceptibility of striatal mitochondria to calcium-induced permeability transition. J Neurosci 23:4858-4867.
9. Castilho RF, Hansson O, Ward MW, Budd SL, Nicholls DG (1998) Mitochondrial control of acute glutamate excitotoxicity in cultured cerebellar granule cells. J Neurosci 18:10277-10286.
10. 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.
11. Cepeda C, Hurst RS, Calvert CR, Hernandez-Echeagaray E, Nguyen OK, Jocoy E, Christian LJ, Ariano MA, Levine MS (2003) Transient and progressive electrophysiological alterations in the corticostriatal pathway in a mouse model of Huntington's disease. J Neurosci 23:961-969.
12. Cha JH (2000) Transcriptional dysregulation in Huntington's disease. Trends Neurosci 23:387-392.
13. Chen N, Luo T, Wellington C, Metzler M, McCutcheon K, Hayden MR, Raymond LA (1999) Subtype-specific enhancement of NMDA receptor currents by mutant huntingtin. J Neurochem 72:1890-1898.
14. Chen N, Ren J, Raymond LA, Murphy TH (2001) Changes in agonist concentration dependence that are a function of duration of exposure suggest N-methyl-D-aspartate receptor nonsaturation during synaptic stimulation. Mol Pharmacol 59:212-219.
15. 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.
16. DeRidder MN, Simon MJ, Siman R, Auberson YP, Raghupathi R, Meaney DF (2006) Traumatic mechanical injury to the hippocampus in vitro causes regional caspase-3 and calpain activation that is influenced by NMDA receptor subunit composition. Neurobiol Dis 22:165-176.
17. Fan MM, Raymond LA (2007) N-Methyl-D-aspartate (NMDA) receptor function and excitotoxicity in Huntington's disease. Prog Neurobiol 81:272-293.
18. Fan MM, Fernandes HB, Zhang LY, Hayden MR, Raymond LA (2007) Altered NMDA receptor trafficking in a yeast artificial chromosome transgenic mouse model of Huntington's disease. J Neurosci 27:3768-3779.
19. Graham RK, Slow EJ, Deng Y, Bissada N, Lu G, Pearson J, Shehadeh J, Leavitt BR, Raymond LA, Hayden MR (2006a) Levels of mutant huntingtin influence the phenotypic severity of Huntington disease in YAC128 mouse models. Neurobiol Dis 21:444-455.
20. Graham RK, Deng Y, Slow EJ, Haigh B, Bissada N, Lu G, Pearson J, Shehadeh J, Bertram L, Murphy Z, Warby SC, Doty CN, Roy S, Wellington CL, Leavitt BR, Raymond LA, Nicholson DW, Hayden MR (2006b) Cleavage at the caspase-6 site is required for neuronal dysfunction and degeneration due to mutant huntingtin. Cell 125:1179-1191.
21. Hansson O, Petersen A, Leist M, Nicotera P, Castilho RF, Brundin P (1999) Transgenic mice expressing a Huntington's disease mutation are resistant to quinolinic acid-induced striatal excitotoxicity. Proc Natl Acad Sci USA 96:8727-8732.
22. Hansson O, Guatteo E, Mercuri NB, Bernardi G, Li XJ, Castilho RF, Brundin P (2001) Resistance to NMDA toxicity correlates with appearance of nuclear inclusions, behavioural deficits and changes in calcium homeostasis in mice transgenic for exon 1 of the huntington gene. Eur J Neurosci 14:1492-1504.
23. Hardingham GE, Chawla S, Cruzalegui FH, Bading H (1999) Control of recruitment and transcription-activating function of CBP determines gene regulation by NMDA receptors and L-type calcium channels. Neuron 22:789-798.
24. Hodgson JG, Agopyan N, Gutekunst CA, Leavitt BR, LePiane F, Singaraja R, Smith DJ, Bissada N, McCutcheon K, Nasir J, Jamot L, Li XJ, Stevens ME, Rosemond E, Roder JC, Phillips AG, Rubin EM, Hersch SM, Hayden MR (1999) A YAC mouse model for Huntington's disease with full-length mutant huntingtin, cytoplasmic toxicity, and selective striatal neurodegeneration. Neuron 23:181-192.
25. Hyrc K, Handran SD, Rothman SM, Goldberg MP (1997) Ionized intracellular calcium concentration predicts excitotoxic neuronal death: observations with low-affinity fluorescent calcium indicators. J Neurosci 17:6669-6677.
26. Kim MJ, Dunah AW, Wang YT, Sheng M (2005) Differential roles of NR2A-and NR2B-containing NMDA receptors in Ras-ERK signaling and AMPA receptor trafficking. Neuron 46:745-760.
27. 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.
28. Kovacs AD, Cebers G, Cebere A, Moreira T, Liljequist S (2001) Cortical and striatal neuronal cultures of the same embryonic origin show intrinsic differences in glutamate receptor expression and vulnerability to excitotoxicity. Exp Neurol 168:47-62.
29. 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.
30. Leavitt BR, Guttman JA, Hodgson JG, Kimel GH, Singaraja R, Vogl AW, Hayden MR (2001) Wild-type huntingtin reduces the cellular toxicity of mutant huntingtin in vivo. Am J Hum Genet 68:313-324.
31. Li L, Murphy TH, Hayden MR, Raymond LA (2004) Enhanced striatal NR2B-containing N-methyl-D-aspartate receptor-mediated synaptic currents in a mouse model of Huntington disease. J Neurophysiol 92:2738-2746.
32. Li S, Tian X, Hartley DM, Feig LA (2006) Distinct roles for Ras-guanine nucleotide-releasing factor 1 (Ras-GRF1) and Ras-GRF2 in the induction of long-term potentiation and long-term depression. J Neurosci 26:1721-1729.
33. Liu L, Wong TP, Pozza MF, Lingenhoehl K, Wang Y, Sheng M, Auberson YP, Wang YT (2004) Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304:1021-1024.
34. Luthi-Carter R, Strand A, Peters NL, Solano SM, Hollingsworth ZR, Menon AS, Frey AS, Spektor BS, Penney EB, Schilling G, Ross CA, Borchelt DR, Tapscott SJ, Young AB, Cha JH, Olson JM (2000) Decreased expression of striatal signaling genes in a mouse model of Huntington's disease.Hum Mol Genet 9:1259-1271.
35. Massey PV, Johnson BE, Moult PR, Auberson YP, Brown MW, Molnar E, Collingridge GL, Bashir ZI (2004) Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J Neurosci 24:7821-7828.
36. Mayer ML, Vyklicky Jr L, Westbrook GL (1989) Modulation of excitatory amino acid receptors by group IIB metal cations in cultured mouse hippocampal neurones. J Physiol (Lond) 415:329-350.
37. 2+ handling in Huntington's disease striatal cells: effect of histone deacetylase inhibitors. J Neurosci 26:11174-11186.
38. 2+-induced permeability transition in human lymphoblastoid cell mitochondria from normal and Huntington's disease individuals. Mol Cell Biochem 269:143-152.
39. 2+-dependent depolarization of rat and human mitochondria: relevance to Huntington's disease. Arch Biochem Biophys 410:1-6.
40. 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.
41. Rigby M, Le Bourdelles B, Heavens RP, Kelly S, Smith D, Butler A, Hammans R, Hills R, Xuereb JH, Hill RG, Whiting PJ, Sirinathsinghji DJ (1996) The messenger RNAs for the N-methyl-D-aspartate receptor subunits show region-specific expression of different subunit composition in the human brain. Neuroscience 73:429-447.
42. Ross CA (2002) Polyglutamine pathogenesis: emergence of unifying mechanisms for Huntington's disease and related disorders. Neuron 35:819-822.
43. Sawa A, Wiegand GW, Cooper J, Margolis RL, Sharp AH, Lawler Jr JF, Greenamyre JT, Snyder SH, Ross CA (1999) Increased apoptosis of Huntington disease lymphoblasts associated with repeat length-dependent mitochondrial depolarization. Nat Med 5:1194-1198.
44. Schinder AF, Olson EC, Spitzer NC, Montal M (1996) Mitochondrial dysfunction is a primary event in glutamate neurotoxicity. J Neurosci 16:6125-6133.
45. Shehadeh J, Fernandes HB, Zeron Mullins MM, Graham RK, Leavitt BR, Hayden MR, Raymond LA (2006) Striatal neuronal apoptosis is preferentially enhanced by NMDA receptor activation in YAC transgenic mouse model of Huntington disease. Neurobiol Dis 21:392-403.
46. Shi WX, Rayport S (1994) GABA synapses formed in vitro by local axon collaterals of nucleus accumbens neurons. J Neurosci 14:4548-4560.
47. 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.
48. Slow EJ, Graham RK, Osmand AP, Devon RS, Lu G, Deng Y, Pearson J, Vaid K, Bissada N, Wetzel R, Leavitt BR, Hayden MR (2005) Absence of behavioral abnormalities and neurodegeneration in vivo despite widespread neuronal huntingtin inclusions. Proc Natl Acad Sci USA 102:11402-11407.
49. Stout AK, Reynolds IJ (1999) High-affinity calcium indicators underestimate increases in intracellular calcium concentrations associated with excitotoxic glutamate stimulations. Neuroscience 89:91-100.
50. Stout AK, Raphael HM, Kanterewicz BI, Klann E, Reynolds IJ (1998) Glutamate-induced neuron death requires mitochondrial calcium uptake. Nat Neurosci 1:366-373.
51. Strong TV, Tagle DA, Valdes JM, Elmer LW, Boehm K, Swaroop M, Kaatz KW, Collins FS, Albin RL (1993) Widespread expression of the human and rat Huntington's disease gene in brain and nonneural tissues. Nat Genet 5:259-265.
52. Tang TS, Tu H, Chan EY, Maximov A, Wang Z, Wellington CL, Hayden MR, Bezprozvanny I (2003) Huntingtin and huntingtin-associated protein 1 influence neuronal calcium signaling mediated by inositol-(1,4,5) triphosphate receptor type 1. Neuron 39:227-239.
53. 2+ signaling and apoptosis of medium spiny neurons in Huntington's disease. Proc Natl Acad Sci USA 102:2602-2607.
54. Toescu EC, Verkhratsky A (2000) Assessment of mitochondrial polarization status in living cells based on analysis of the spatial heterogeneity of rhodamine 123 fluorescence staining. Pflügers Arch 440:941-947.
55. van Dijk JG, van der Velde EA, Roos RA, Bruyn GW (1986) Juvenile Huntington disease. Hum Genet 73:235-239.
56. Van Raamsdonk JM, Pearson J, Slow EJ, Hossain SM, Leavitt BR, Hayden MR (2005) Cognitive dysfunction precedes neuropathology and motor abnormalities in the YAC128 mouse model of Huntington's disease. J Neurosci 25:4169-4180.
57. Vonsattel JP, Myers RH, Stevens TJ, Ferrante RJ, Bird ED, Richardson Jr EP (1985) Neuropathological classification of Huntington's disease. J Neuropathol Exp Neurol 44:559-577.
58. 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.
59. Williams K (1993) Ifenprodil discriminates subtypes of the N-methyl-D-aspartate receptor: selectivity and mechanisms at recombinant heteromeric receptors. Mol Pharmacol 44:851-859.
60. 2+ homeostasis in aged cerebellar granule neurons in brain slices. J Neurosci 22:10761-10771.
61. 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.
62. 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.
63. Zuccato C, Ciammola A, Rigamonti D, Leavitt BR, Goffredo D, Conti L, MacDonald ME, Friedlander RM, Silani V, Hayden MR, Timmusk T, Sipione S, Cattaneo E (2001) Loss of huntingtin-mediated BDNF gene transcription in Huntington's disease. Science 293:493-498.