Metabolic state determines sensitivity to cellular stress in Huntington disease: Normalization by activation of PPARγ

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Jin, Youngnam N ^a   Hwang, Woong Y ^a   Jo, Chulman ^a   Johnson, Gail V W ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CASPASE 3; CASPASE 8; CASPASE 9; HUNTINGTIN; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; REACTIVE OXYGEN METABOLITE; ROSIGLITAZONE; SHORT HAIRPIN RNA; SUPEROXIDE; 2 CHLORO 5 NITROBENZANILIDE; 2,4 THIAZOLIDINEDIONE DERIVATIVE; 2-CHLORO-5-NITROBENZANILIDE; ANILIDE; GLUCOSE; HYDROGEN PEROXIDE; PYRUVIC ACID; ROLIPRAM; THAPSIGARGIN;

ANIMAL CELL; ARTICLE; BIOENERGY; CELL DEATH; CELL TYPE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME INHIBITION; GENE; GENE EXPRESSION REGULATION; GENE MUTATION; HUNTINGTIN GENE; HUNTINGTON CHOREA; MEMBRANE DAMAGE; METABOLIC STRESS; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYSICAL SENSITIVITY; PROTEIN FUNCTION; RAT; STABLE EXPRESSION; TRANSCRIPTION REGULATION; WILD TYPE; ANIMAL; CELL CULTURE; CELL LINE; DRUG EFFECT; METABOLISM; MOUSE; POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANILIDES; ANIMALS; BLOTTING, WESTERN; CELL LINE; CELLS, CULTURED; GLUCOSE; HUNTINGTON DISEASE; HYDROGEN PEROXIDE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; POLYMERASE CHAIN REACTION; PPAR GAMMA; PYRUVIC ACID; RATS; REACTIVE OXYGEN SPECIES; ROLIPRAM; SUPEROXIDES; THAPSIGARGIN; THIAZOLIDINEDIONES;

EID: 84856035740     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030406     Document Type: Article

References (66)

1. Ferrante RJ, Kowall NW, Richardson EP Jr, (1991) Proliferative and degenerative changes in striatal spiny neurons in Huntington's disease: a combined study using the section-Golgi method and calbindin D28k immunocytochemistry. J Neurosci 11: 3877-3887.
2. The 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.
3. Djousse L, Knowlton B, Cupples LA, Marder K, Shoulson I, et al. (2002) Weight loss in early stage of Huntington's disease. Neurology 59: 1325-1330.
4. Gil JM, Rego AC, (2008) Mechanisms of neurodegeneration in Huntington's disease. Eur J Neurosci 27: 2803-2820.
5. Jin YN, Johnson GV, (2010) The interrelationship between mitochondrial dysfunction and transcriptional dysregulation in Huntington disease. J Bioenerg Biomembr 42: 199-205.
6. Quintanilla RA, Jin YN, Fuenzalida K, Bronfman M, Johnson GV, (2008) Rosiglitazone treatment prevents mitochondrial dysfunction in mutant huntingtin-expressing cells: possible role of peroxisome proliferator-activated receptor-gamma (PPARgamma) in the pathogenesis of Huntington disease. J Biol Chem 283: 25628-25637.
7. Milakovic T, Quintanilla RA, Johnson GV, (2006) Mutant huntingtin expression induces mitochondrial calcium handling defects in clonal striatal cells: functional consequences. J Biol Chem 281: 34785-34795.
8. Browne SE, Ferrante RJ, Beal MF, (1999) Oxidative stress in Huntington's disease. Brain Pathol 9: 147-163.
9. Sorolla MA, Rodriguez-Colman MJ, Tamarit J, Tamarit J, Ortega Z, et al. (2010) Protein oxidation in Huntington disease affects energy production and vitamin B6 metabolism. Free Radic Biol Med 49: 612-621.
10. Perluigi M, Poon HF, Maragos W, Pierce WM, Klein JB, et al. (2005) Proteomic analysis of protein expression and oxidative modification in r6/2 transgenic mice: a model of Huntington disease. Mol Cell Proteomics 4: 1849-1861.
11. Ross CA, Thompson LM, (2006) Transcription meets metabolism in neurodegeneration. Nat Med 12: 1239-1241.
12. Cui L, Jeong H, Borovecki F, Parkhurst CN, Tanese N, et al. (2006) Transcriptional repression of PGC-1alpha by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration. Cell 127: 59-69.
13. Glass CK, Ogawa S, (2006) Combinatorial roles of nuclear receptors in inflammation and immunity. Nat Rev Immunol 6: 44-55.
14. Chiang MC, Chen CM, Lee MR, Chen HW, Chen HM, et al. (2010) Modulation of energy deficiency in Huntington's disease via activation of the peroxisome proliferator-activated receptor gamma. Hum Mol Genet 19: 4043-4058.
15. Heneka MT, Sastre M, Dumitrescu-Ozimek L, Hanke A, Dewachter I, et al. (2005) Acute treatment with the PPARgamma agonist pioglitazone and ibuprofen reduces glial inflammation and Abeta1-42 levels in APPV717I transgenic mice. Brain 128: 1442-1453.
16. Breidert T, Callebert J, Heneka MT, Landreth G, Launay JM, et al. (2002) Protective action of the peroxisome proliferator-activated receptor-gamma agonist pioglitazone in a mouse model of Parkinson's disease. J Neurochem 82: 615-624.
17. Kiaei M, Kipiani K, Chen J, Calingasan NY, Beal MF, (2005) Peroxisome proliferator-activated receptor-gamma agonist extends survival in transgenic mouse model of amyotrophic lateral sclerosis. Exp Neurol 191: 331-336.
18. Luo Y, Yin W, Signore AP, Zhang F, Hong Z, et al. (2006) Neuroprotection against focal ischemic brain injury by the peroxisome proliferator-activated receptor-gamma agonist rosiglitazone. J Neurochem 97: 435-448.
19. Niino M, Iwabuchi K, Kikuchi S, Ato M, Morohashi T, et al. (2001) Amelioration of experimental autoimmune encephalomyelitis in C57BL/6 mice by an agonist of peroxisome proliferator-activated receptor-gamma. J Neuroimmunol 116: 40-48.
20. 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.
21. Seong IS, Ivanova E, Lee JM, Choo YS, Fossale E, et al. (2005) HD CAG repeat implicates a dominant property of huntingtin in mitochondrial energy metabolism. Human Molecular Genetics 14: 2871-2880.
22. Oliveira JM, Chen S, Almeida S, Riley R, Goncalves J, et al. (2006) Mitochondrial-dependent Ca2+ handling in Huntington's disease striatal cells: effect of histone deacetylase inhibitors. J Neurosci 26: 11174-11186.
23. Rossignol R, Gilkerson R, Aggeler R, Yamagata K, Remington SJ, et al. (2004) Energy substrate modulates mitochondrial structure and oxidative capacity in cancer cells. Cancer Res 64: 985-993.
24. Murthy VV, (1995) Use of pyruvate oxidase to overcome pyruvate inhibition during the lactate to pyruvate reaction for assaying lactate dehydrogenase in serum. J Clin Lab Anal 9: 225-229.
25. Gundemir S, Johnson GV, (2009) Intracellular localization and conformational state of transglutaminase 2: implications for cell death. PLoS ONE 4: e6123.
26. DeMarch Z, Giampa C, Patassini S, Bernardi G, Fusco FR, (2008) Beneficial effects of rolipram in the R6/2 mouse model of Huntington's disease. Neurobiol Dis 30: 375-387.
27. Gines S, Seong IS, Fossale E, Ivanova E, Trettel F, et al. (2003) Specific progressive cAMP reduction implicates energy deficit in presymptomatic Huntington's disease knock-in mice. Hum Mol Genet 12: 497-508.
28. Shoshan-Barmatz V, De Pinto V, Zweckstetter M, Raviv Z, Keinan N, et al. (2010) VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol Aspects Med 31: 227-285.
29. Zheng Z, Chen H, Wang H, Ke B, Zheng B, et al. (2010) Improvement of retinal vascular injury in diabetic rats by statins is associated with the inhibition of mitochondrial reactive oxygen species pathway mediated by peroxisome proliferator-activated receptor gamma coactivator 1alpha. Diabetes 59: 2315-2325.
30. Troiano L, Ferraresi R, Lugli E, Nemes E, Roat E, et al. (2007) Multiparametric analysis of cells with different mitochondrial membrane potential during apoptosis by polychromatic flow cytometry. Nat Protoc 2: 2719-2727.
31. Jo DG, Jun JI, Chang JW, Hong YM, Song S, et al. (2004) Calcium binding of ARC mediates regulation of caspase 8 and cell death. Mol Cell Biol 24: 9763-9770.
32. Yamaguchi H, Bhalla K, Wang HG, (2003) Bax plays a pivotal role in thapsigargin-induced apoptosis of human colon cancer HCT116 cells by controlling Smac/Diablo and Omi/HtrA2 release from mitochondria. Cancer Res 63: 1483-1489.
33. Gervais FG, Singaraja R, Xanthoudakis S, Gutekunst CA, Leavitt BR, et al. (2002) Recruitment and activation of caspase-8 by the Huntingtin-interacting protein Hip-1 and a novel partner Hippi. Nat Cell Biol 4: 95-105.
34. Maglione V, Cannella M, Gradini R, Cislaghi G, Squitieri F, (2006) Huntingtin fragmentation and increased caspase 3, 8 and 9 activities in lymphoblasts with heterozygous and homozygous Huntington's disease mutation. Mech Ageing Dev 127: 213-216.
35. Zhang Y, Ona VO, Li M, Drozda M, Dubois-Dauphin M, et al. (2003) Sequential activation of individual caspases, and of alterations in Bcl-2 proapoptotic signals in a mouse model of Huntington's disease. Journal of Neurochemistry 87: 1184-1192.
36. Nasrallah R, Clark J, Corinaldi J, Paris G, Miura P, et al. (2010) Thiazolidinediones alter growth and epithelial cell integrity, independent of PPAR{gamma} and MAPK activation, in mouse M1 Cortical Collecting Duct Cells. Am J Physiol Renal Physiol 298: 1105-1112.
37. Zielonka J, Kalyanaraman B, (2010) Hydroethidine- and MitoSOX-derived red fluorescence is not a reliable indicator of intracellular superoxide formation: another inconvenient truth. Free Radic Biol Med 48: 983-1001.
38. Doonan F, Wallace DM, O'Driscoll C, Cotter TG, (2009) Rosiglitazone acts as a neuroprotectant in retinal cells via up-regulation of sestrin-1 and SOD-2. J Neurochem 109: 631-643.
39. Sorbi S, Bird ED, Blass JP, (1983) Decreased pyruvate dehydrogenase complex activity in Huntington and Alzheimer brain. Ann Neurol 13: 72-78.
40. Butterworth J, Yates CM, Reynolds GP, (1985) Distribution of phosphate-activated glutaminase, succinic dehydrogenase, pyruvate dehydrogenase and gamma-glutamyl transpeptidase in post-mortem brain from Huntington's disease and agonal cases. J Neurol Sci 67: 161-171.
41. Perluigi M, Poon HF, Maragos W, Pierce WM, Klein JB, et al. (2005) Proteomic analysis of protein expression and oxidative modification in r6/2 transgenic mice: a model of Huntington disease. Mol Cell Proteomics 4: 1849-1861.
42. Matas J, Young NT, Bourcier-Lucas C, Ascah A, Marcil M, et al. (2009) Increased expression and intramitochondrial translocation of cyclophilin-D associates with increased vulnerability of the permeability transition pore to stress-induced opening during compensated ventricular hypertrophy. J Mol Cell Cardiol 46: 420-430.
43. King AL, Swain TM, Dickinson DA, Lesort MJ, Bailey SM, (2010) Chronic ethanol consumption enhances sensitivity to Ca(2+)-mediated opening of the mitochondrial permeability transition pore and increases cyclophilin D in liver. Am J Physiol Gastrointest Liver Physiol 299: G954-966.
44. Rasola A, Sciacovelli M, Pantic B, Bernardi P, (2010) Signal transduction to the permeability transition pore. FEBS Lett 584: 1989-1996.
45. Perry GM, Tallaksen-Greene S, Kumar A, Heng MY, Kneynsberg A, et al. (2010) Mitochondrial calcium uptake capacity as a therapeutic target in the R6/2 mouse model of Huntington's disease. Hum Mol Genet 19: 3354-3371.
46. Fuenzalida K, Quintanilla R, Ramos P, Piderit D, Fuentealba RA, et al. (2007) Peroxisome proliferator-activated receptor gamma up-regulates the Bcl-2 anti-apoptotic protein in neurons and induces mitochondrial stabilization and protection against oxidative stress and apoptosis. J Biol Chem 282: 37006-37015.
47. Martinez JA, Zhang Z, Svetlov SI, Hayes RL, Wang KK, et al. (2010) Calpain and caspase processing of caspase-12 contribute to the ER stress-induced cell death pathway in differentiated PC12 cells. Apoptosis 15: 1480-1493.
48. Sasaya H, Utsumi T, Shimoke K, Nakayama H, Matsumura Y, et al. (2008) Nicotine suppresses tunicamycin-induced, but not thapsigargin-induced, expression of GRP78 during ER stress-mediated apoptosis in PC12 cells. J Biochem 144: 251-257.
49. 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.
50. Panov AV, Gutekunst CA, Leavitt BR, Hayden MR, Burke JR, et al. (2002) Early mitochondrial calcium defects in Huntington's disease are a direct effect of polyglutamines. Nat Neurosci 5: 731-736.
51. Zhang X, Li L, Prabhakaran K, Zhang L, Leavesley HB, et al. (2007) Uncoupling protein-2 up-regulation and enhanced cyanide toxicity are mediated by PPARalpha activation and oxidative stress. Toxicol Appl Pharmacol 223: 10-19.
52. Jucker BM, Yang D, Casey WM, Olzinski AR, Williams C, et al. (2007) Selective PPARdelta agonist treatment increases skeletal muscle lipid metabolism without altering mitochondrial energy coupling: an in vivo magnetic resonance spectroscopy study. Am J Physiol Endocrinol Metab 293: E1256-1264.
53. Wu Z, Zhang J, Zhao B, (2009) Superoxide anion regulates the mitochondrial free Ca2+ through uncoupling proteins. Antioxid Redox Signal 11: 1805-1818.
54. Chan SH, Wu CA, Wu KL, Ho YH, Chang AY, et al. (2009) Transcriptional upregulation of mitochondrial uncoupling protein 2 protects against oxidative stress-associated neurogenic hypertension. Circ Res 105: 886-896.
55. Echtay KS, Roussel D, St-Pierre J, Jekabsons MB, Cadenas S, et al. (2002) Superoxide activates mitochondrial uncoupling proteins. Nature 415: 96-99.
56. Krauss S, Zhang CY, Scorrano L, Dalgaard LT, St-Pierre J, et al. (2003) Superoxide-mediated activation of uncoupling protein 2 causes pancreatic beta cell dysfunction. J Clin Invest 112: 1831-1842.
57. Echtay KS, (2007) Mitochondrial uncoupling proteins-what is their physiological role? Free Radic Biol Med 43: 1351-1371.
58. Fong WH, Tsai HD, Chen YC, Wu JS, Lin TN, (2010) Anti-apoptotic actions of PPAR-gamma against ischemic stroke. Mol Neurobiol 41: 180-186.
59. Schock SC, Xu J, Duquette PM, Qin Z, Lewandowski AJ, et al. (2008) Rescue of neurons from ischemic injury by peroxisome proliferator-activated receptor-gamma requires a novel essential cofactor LMO4. J Neurosci 28: 12433-12444.
60. Du Y, Wooten MC, Wooten MW, (2009) Oxidative damage to the promoter region of SQSTM1/p62 is common to neurodegenerative disease. Neurobiol Dis 35: 302-310.
61. Kim JB, Wright HM, Wright M, Spiegelman BM, (1998) ADD1/SREBP1 activates PPARgamma through the production of endogenous ligand. Proc Natl Acad Sci USA 95: 4333-4337.
62. Handschin C, Rhee J, Lin J, Tarr PT, Spiegelman BM, (2003) An autoregulatory loop controls peroxisome proliferator-activated receptor gamma coactivator 1alpha expression in muscle. Proc Natl Acad Sci USA 100: 7111-7116.
63. Hondares E, Mora O, Yubero P, Rodriguez de la Concepcion M, Iglesias R, et al. (2006) Thiazolidinediones and rexinoids induce peroxisome proliferator-activated receptor-coactivator (PGC)-1alpha gene transcription: an autoregulatory loop controls PGC-1alpha expression in adipocytes via peroxisome proliferator-activated receptor-gamma coactivation. Endocrinology 147: 2829-2838.
64. Qin XF, An DS, Chen IS, Baltimore D, (2003) Inhibiting HIV-1 infection in human T cells by lentiviral-mediated delivery of small interfering RNA against CCR5. Proc Natl Acad Sci USA 100: 183-188.
65. Trettel F, Rigamonti D, Hilditch-Maguire P, Wheeler VC, Sharp AH, et al. (2000) Dominant phenotypes produced by the HD mutation in STHdh(Q111) striatal cells. Hum Mol Genet 9: 2799-2809.
66. Kress GJ, Dineley KE, Reynolds IJ, (2002) The relationship between intracellular free iron and cell injury in cultured neurons, astrocytes, and oligodendrocytes. J Neurosci 22: 5848-5855.