Neuroprotective effects of PPAR-γ agonist rosiglitazone in N171-82Q mouse model of Huntington's disease

Journal of Neurochemistry

Volumn 125, Issue 3, 2013, Pages 410-419

  Jin, Jing ^a   Albertz, Jennifer ^a   Guo, Zhihong ^a   Peng, Qi ^a   Rudow, Gay ^a   Troncoso, Juan C ^a   Ross, Christopher A ^a   Duan, Wenzhen ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

BDNF; glucose metabolism; huntingtin; PGC 1 ; PPAR ; Sirt6

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; HUNTINGTIN; OREXIN A; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA AGONIST; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; ROSIGLITAZONE; SIRTUIN 6;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; HUNTINGTON CHOREA; HYPERGLYCEMIA; HYPOTHALAMUS; MALE; MOTOR PERFORMANCE; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN DEPLETION; PROTEIN SYNTHESIS INHIBITION; SIGNAL TRANSDUCTION; STRIATE CORTEX;

ADENOSINE TRIPHOSPHATE; ANILIDES; ANIMALS; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL LINE; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; GLUTAMATES; HUMANS; HUNTINGTON DISEASE; HYPERGLYCEMIA; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; L-LACTATE DEHYDROGENASE; MALE; MICE; MICE, TRANSGENIC; MOVEMENT DISORDERS; NERVE TISSUE PROTEINS; NEURONS; NEUROPEPTIDES; NEUROPROTECTIVE AGENTS; PPAR GAMMA; RNA, MESSENGER; SIRTUINS; THIAZOLIDINEDIONES; TRANS-ACTIVATORS; TRANSFECTION; TRINUCLEOTIDE REPEAT EXPANSION;

MUS;

EID: 84876665921     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12190     Document Type: Article

References (69)

1. Baquet Z. C., Gorski J. A., and, Jones K. R., (2004) Early striatal dendrite deficits followed by neuron loss with advanced age in the absence of anterograde cortical brain-derived neurotrophic factor. J. Neurosci. 24, 4250-4258.
2. Bithell A., Johnson R., and, Buckley N. J., (2009) Transcriptional dysregulation of coding and non-coding genes in cellular models of Huntington's disease. Biochem. Soc. Trans. 37, 1270-1275.
3. Canto C., and, Auwerx J., (2009) PGC-1alpha, SIRT1 and AMPK, an energy sensing network that controls energy expenditure. Curr. Opin. Lipidol. 20, 98-105.
4. Carta A. R., Frau L., Pisanu A., Wardas J., Spiga S., and, Carboni E., (2011) Rosiglitazone decreases peroxisome proliferator receptor-gamma levels in microglia and inhibits TNF-alpha production: new evidences on neuroprotection in a progressive Parkinson's disease model. Neuroscience 194, 250-261.
5. Chaturvedi R. K., Adhihetty P., Shukla S., et al,. (2009) Impaired PGC-1alpha function in muscle in Huntington's disease. Hum. Mol. Genet. 18, 3048-3065.
6. Chaturvedi R. K., Calingasan N. Y., Yang L., Hennessey T., Johri A., and, Beal M. F., (2010) Impairment of PGC-1alpha expression, neuropathology and hepatic steatosis in a transgenic mouse model of Huntington's disease following chronic energy deprivation. Hum. Mol. Genet. 19, 3190-3205.
7. Chiang M. C., Chen C. M., Lee M. R., 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.
8. Chiang M. C., Chern Y., and, Juo C. G., (2011) The dysfunction of hepatic transcriptional factors in mice with Huntington's Disease. Biochim. Biophys. Acta 1812, 1111-1120.
9. Chiang M. C., Chern Y., and, Huang R. N., (2012) PPARgamma rescue of the mitochondrial dysfunction in Huntington's disease. Neurobiol. Dis. 45, 322-328.
10. Chopra V., Fox J. H., Lieberman G., et al,. (2007) A small-molecule therapeutic lead for Huntington's disease: preclinical pharmacology and efficacy of C2-8 in the R6/2 transgenic mouse. Proc. Natl Acad. Sci. USA 104, 16685-16689.
11. Chou S. Y., Lee Y. C., Chen H. M., et al,. (2005) CGS21680 attenuates symptoms of Huntington's disease in a transgenic mouse model. J. Neurochem. 93, 310-320.
12. Cui L., Jeong H., Borovecki F., Parkhurst C. N., Tanese N., and, Krainc D., (2006) Transcriptional repression of PGC-1alpha by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration. Cell 127, 59-69.
13. Diano S., Liu Z. W., Jeong J. K., et al,. (2011) Peroxisome proliferation-associated control of reactive oxygen species sets melanocortin tone and feeding in diet-induced obesity. Nat. Med. 17, 1121-1127.
14. Diekmann H., Anichtchik O., Fleming A., Futter M., Goldsmith P., Roach A., and, Rubinsztein D. C., (2009) Decreased BDNF levels are a major contributor to the embryonic phenotype of huntingtin knockdown zebrafish. J. Neurosci. 29, 1343-1349.
15. Djousse L., Knowlton B., Cupples L. A., Marder K., Shoulson I., and, Myers R. H., (2002) Weight loss in early stage of Huntington's disease. Neurology 59, 1325-1330.
16. Duan W., Guo Z., Jiang H., Ware M., Li X. J., and, Mattson M. P., (2003) Dietary restriction normalizes glucose metabolism and BDNF levels, slows disease progression, and increases survival in huntingtin mutant mice. Proc. Natl Acad. Sci. USA 100, 2911-2916.
17. Ebrahim I. O., Howard R. S., Kopelman M. D., Sharief M. K., and, Williams A. J., (2002) The hypocretin/orexin system. J. R. Soc. Med. 95, 227-230.
18. Etgen G. J., Oldham B. A., Johnson W. T., et al,. (2002) A tailored therapy for the metabolic syndrome: the dual peroxisome proliferator-activated receptor-alpha/gamma agonist LY465608 ameliorates insulin resistance and diabetic hyperglycemia while improving cardiovascular risk factors in preclinical models. Diabetes 51, 1083-1087.
19. Fatehi-Hassanabad Z., and, Tasker R. A., (2011) Peroxisome proliferator-activated receptor-gamma (PPAR-gamma) activation confers functional neuroprotection in global ischemia. Neurotox. Res. 19, 462-471.
20. Fuenzalida K., Quintanilla R., Ramos P., Piderit D., Fuentealba R. A., Martinez G., Inestrosa N. C., and, Bronfman M., (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.
21. Gabery S., Sajjad M. U., Hult S., Soylu R., Kirik D., and, Petersen A., (2012) Characterization of a rat model of Huntington's disease based on targeted expression of mutant huntingtin in the forebrain using adeno-associated viral vectors. Eur J Neurosci.
22. Giralt A., Rodrigo T., Martin E. D., Gonzalez J. R., Mila M., Cena V., Dierssen M., Canals J. M., and, Alberch J., (2009) Brain-derived neurotrophic factor modulates the severity of cognitive alterations induced by mutant huntingtin: involvement of phospholipaseCgamma activity and glutamate receptor expression. Neuroscience 158, 1234-1250.
23. Giralt A., Carreton O., Lao-Peregrin C., Martin E. D., and, Alberch J., (2011) Conditional BDNF release under pathological conditions improves Huntington's disease pathology by delaying neuronal dysfunction. Mol. Neurodegener. 6, 71.
24. Hoppitt T., Calvert M., Pall H., Rickards H., and, Sackley C., (2010) Huntington's disease. Lancet 376, 1463-1464.
25. Hult S., Soylu R., Bjorklund T., Belgardt B. F., Mauer J., Bruning J. C., Kirik D., and, Petersen A., (2011) Mutant huntingtin causes metabolic imbalance by disruption of hypothalamic neurocircuits. Cell Metab. 13, 428-439.
26. Hunter J. M., Lesort M., and, Johnson G. V., (2007) Ubiquitin-proteasome system alterations in a striatal cell model of Huntington's disease. J. Neurosci. Res. 85, 1774-1788.
27. Jiang M., Wang J., Fu J., et al,. (2012) Neuroprotective role of Sirt1 in mammalian models of Huntington's disease through activation of multiple Sirt1 targets. Nat. Med. 18, 153-158.
28. Jin Y. N., and, Johnson G. V., (2010) The interrelationship between mitochondrial dysfunction and transcriptional dysregulation in Huntington disease. J. Bioenerg. Biomembr. 42, 199-205.
29. Jin Y. N., Hwang W. Y., Jo C., and, Johnson G. V., (2012) Metabolic state determines sensitivity to cellular stress in Huntington disease: normalization by activation of PPARgamma. PLoS ONE 7, e30406.
30. Johri A., Calingasan N. Y., Hennessey T. M., Sharma A., Yang L., Wille E., Chandra A., and, Beal M. F., (2012) Pharmacologic activation of mitochondrial biogenesis exerts widespread beneficial effects in a transgenic mouse model of Huntington's disease. Hum. Mol. Genet. 21, 1124-1137.
31. Jones L., and, Hughes A., (2011) Pathogenic mechanisms in Huntington's disease. Int. Rev. Neurobiol. 98, 373-418.
32. Kiaei M., (2008) Peroxisome Proliferator-Activated Receptor-gamma in Amyotrophic Lateral Sclerosis and Huntington's Disease. PPAR Res. 2008, 418765.
33. Kiaei M., Kipiani K., Chen J., Calingasan N. Y., and, Beal M. F., (2005) Peroxisome proliferator-activated receptor-gamma agonist extends survival in transgenic mouse model of amyotrophic lateral sclerosis. Exp. Neurol. 191, 331-336.
34. Li X. J., Orr A. L., and, Li S., (2010) Impaired mitochondrial trafficking in Huntington's disease. Biochim. Biophys. Acta 1802, 62-65.
35. Liang H., and, Ward W. F., (2006) PGC-1alpha: a key regulator of energy metabolism. Adv. Physiol. Educ. 30, 145-151.
36. Lin J., Wu P. H., Tarr P. T., et al,. (2004) Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice. Cell 119, 121-135.
37. Lombard D. B., Schwer B., Alt F. W., and, Mostoslavsky R., (2008) SIRT6 in DNA repair, metabolism and ageing. J. Intern. Med. 263, 128-141.
38. Martin E., Betuing S., Pages C., Cambon K., Auregan G., Deglon N., Roze E., and, Caboche J., (2011) Mitogen- and stress-activated protein kinase 1-induced neuroprotection in Huntington's disease: role on chromatin remodeling at the PGC-1-alpha promoter. Hum. Mol. Genet. 20, 2422-2434.
39. McGill J. K., and, Beal M. F., (2006) PGC-1alpha, a new therapeutic target in Huntington's disease? Cell 127, 465-468.
40. Napolitano M., Costa L., Palermo R., Giovenco A., Vacca A., and, Gulino A., (2011) Protective effect of pioglitazone, a PPARgamma ligand, in a 3 nitropropionic acid model of Huntington's disease. Brain Res. Bull. 85, 231-237.
41. Panov A. V., Gutekunst C. A., Leavitt B. R., Hayden M. R., Burke J. R., Strittmatter W. J., and, Greenamyre J. T., (2002) Early mitochondrial calcium defects in Huntington's disease are a direct effect of polyglutamines. Nat. Neurosci. 5, 731-736.
42. Petersen A., Gil J., Maat-Schieman M. L., et al,. (2005) Orexin loss in Huntington's disease. Hum. Mol. Genet. 14, 39-47.
43. Pouladi M. A., Xie Y., Skotte N. H., et al,. (2010) Full-length huntingtin levels modulate body weight by influencing insulin-like growth factor 1 expression. Hum. Mol. Genet. 19, 1528-1538.
44. Quintanilla R. A., and, Johnson G. V., (2009) Role of mitochondrial dysfunction in the pathogenesis of Huntington's disease. Brain Res. Bull. 80, 242-247.
45. Quintanilla R. A., Jin Y. N., Fuenzalida K., Bronfman M., and, Johnson G. V., (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.
46. Randy L. H., and, Guoying B., (2007) Agonism of Peroxisome Proliferator Receptor-Gamma may have Therapeutic Potential for Neuroinflammation and Parkinson's Disease. Curr. Neuropharmacol. 5, 35-46.
47. Rasbach K. A., and, Schnellmann R. G., (2007) PGC-1alpha over-expression promotes recovery from mitochondrial dysfunction and cell injury. Biochem. Biophys. Res. Commun. 355, 734-739.
48. Rosen E. D., and, Spiegelman B. M., (2001) PPARgamma: a nuclear regulator of metabolism, differentiation, and cell growth. J. Biol. Chem. 276, 37731-37734.
49. Rosenstock T. R., Duarte A. I., and, Rego A. C., (2010) Mitochondrial-Associated Metabolic Changes and Neurodegeneration in Huntington's Disease-From Clinical Features to the Bench. Curr Drug Targets.
50. Ross C. A., and, Tabrizi S. J., (2011) Huntington's disease: from molecular pathogenesis to clinical treatment. Lancet Neurol. 10, 83-98.
51. Schintu N., Frau L., Ibba M., Caboni P., Garau A., Carboni E., and, Carta A. R., (2009) PPAR-gamma-mediated neuroprotection in a chronic mouse model of Parkinson's disease. Eur. J. Neurosci. 29, 954-963.
52. Schutz B., Reimann J., Dumitrescu-Ozimek L., Kappes-Horn K., Landreth G. E., Schurmann B., Zimmer A., and, Heneka M. T., (2005) The oral antidiabetic pioglitazone protects from neurodegeneration and amyotrophic lateral sclerosis-like symptoms in superoxide dismutase-G93A transgenic mice. J. Neurosci. 25, 7805-7812.
53. Simmons D. A., Mehta R. A., Lauterborn J. C., Gall C. M., and, Lynch G., (2011) Brief ampakine treatments slow the progression of Huntington's disease phenotypes in R6/2 mice. Neurobiol. Dis. 41, 436-444.
54. Strand A. D., Baquet Z. C., Aragaki A. K., et al,. (2007) Expression profiling of Huntington's disease models suggests that brain-derived neurotrophic factor depletion plays a major role in striatal degeneration. J. Neurosci. 27, 11758-11768.
55. Strum J. C., Shehee R., Virley D., et al,. (2007) Rosiglitazone induces mitochondrial biogenesis in mouse brain. J. Alzheimers Dis. 11, 45-51.
56. 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. The Huntington's Disease Collaborative Research Group. Cell 72, 971-983.
57. Turner C., and, Schapira A. H., (2010) Mitochondrial matters of the brain: the role in Huntington's disease. J. Bioenerg. Biomembr. 42, 193-198.
58. Valle I., Alvarez-Barrientos A., Arza E., Lamas S., and, Monsalve M., (2005) PGC-1alpha regulates the mitochondrial antioxidant defense system in vascular endothelial cells. Cardiovasc. Res. 66, 562-573.
59. Watson G. S., Cholerton B. A., Reger M. A., et al,. (2005) Preserved cognition in patients with early Alzheimer disease and amnestic mild cognitive impairment during treatment with rosiglitazone: a preliminary study. Am. J. Geriatr. Psychiatry 13, 950-958.
60. Wenz T., Diaz F., Spiegelman B. M., and, Moraes C. T., (2008) Activation of the PPAR/PGC-1alpha pathway prevents a bioenergetic deficit and effectively improves a mitochondrial myopathy phenotype. Cell Metab. 8, 249-256.
61. Weydt P., Pineda V. V., Torrence A. E., et al,. (2006) Thermoregulatory and metabolic defects in Huntington's disease transgenic mice implicate PGC-1alpha in Huntington's disease neurodegeneration. Cell Metab. 4, 349-362.
62. Williams R. H., Morton A. J., and, Burdakov D., (2011) Paradoxical function of orexin/hypocretin circuits in a mouse model of Huntington's disease. Neurobiol. Dis. 42, 438-445.
63. Xiao C., Kim H. S., Lahusen T., Wang R. H., Xu X., Gavrilova O., Jou W., Gius D., and, Deng C. X., (2010) SIRT6 deficiency results in severe hypoglycemia by enhancing both basal and insulin-stimulated glucose uptake in mice. J. Biol. Chem. 285, 36776-36784.
64. Xie Y., Hayden M. R., and, Xu B., (2010) BDNF overexpression in the forebrain rescues Huntington's disease phenotypes in YAC128 mice. J. Neurosci. 30, 14708-14718.
65. Yang S. J., Choi J. M., Chae S. W., et al,. (2011) Activation of peroxisome proliferator-activated receptor gamma by rosiglitazone increases sirt6 expression and ameliorates hepatic steatosis in rats. PLoS ONE 6, e17057.
66. Zheng B., Liao Z., Locascio J. J,. et al. (2010) PGC-1alpha, a potential therapeutic target for early intervention in Parkinson's disease. Sci. Transl. Med., 2, 52ra73.
67. Zhong L., and, Mostoslavsky R., (2010) SIRT6: a master epigenetic gatekeeper of glucose metabolism. Transcription 1, 17-21.
68. Zhong L., D'Urso A., Toiber D., et al,. (2010) The histone deacetylase Sirt6 regulates glucose homeostasis via Hif1alpha. Cell 140, 280-293.
69. Zuccato C., Marullo M., Vitali B., et al,. (2011) Brain-derived neurotrophic factor in patients with Huntington's disease. PLoS ONE 6, e22966.