PGC-1α overexpression exacerbates β-amyloid and tau deposition in a transgenic mouse model of Alzheimer's disease

FASEB Journal

Volumn 28, Issue 4, 2014, Pages 1745-1755

  Dumont, Magali ^a   Stack, Cliona ^a   Elipenahli, Ceyhan ^a   Jainuddin, Shari ^a   Launay, Nathalie ^b,c   Gerges, Meri ^a   Starkova, Natalia ^a   Starkov, Anatoly A ^a   Calingasan, Noel Y ^a   Tampellini, Davide ^d   Pujol, Aurora ^b,c,e   Beal, M Flint ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d INSERM   (France)

^e INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

Behavior; Cell death; Mitochondria; Tg19959 mice

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; AMYLOID PRECURSOR PROTEIN; CITRATE SYNTHASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEASOME; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE; TAU PROTEIN;

ALZHEIMER DISEASE; AMNESIA; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR DISORDER; BRAIN CORTEX; CONTROLLED STUDY; DISEASE EXACERBATION; ENZYME ACTIVITY; FAMILIAL DISEASE; FEMALE; GENE MUTATION; GENOTYPE; HIPPOCAMPUS; HYPERACTIVITY; LOCOMOTION; MALE; MOUSE; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROPATHOLOGY; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION;

BEHAVIOR; CELL DEATH; MITOCHONDRIA; TG19959 MICE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BLOTTING, WESTERN; CELL DEATH; DISEASE MODELS, ANIMAL; GENE EXPRESSION; HUMANS; MEMORY DISORDERS; MENTAL DISORDERS; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICE, TRANSGENIC; MUTATION; PLAQUE, AMYLOID; PROTEASOME ENDOPEPTIDASE COMPLEX; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TAU PROTEINS; TRANSCRIPTION FACTORS;

EID: 84901049784     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-236331     Document Type: Article

References (61)

1. Terry, R. D., Masliah, E., Salmon, D. P., Butters, N., DeTeresa, R., Hill, R., Hansen, L. A., and Katzman, R. (1991) Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 30, 572-580
2. Higgins, G. C., Beart, P. M., Shin, Y. S., Chen, M. J., Cheung, N. S., and Nagley, P. (2010) Oxidative stress: emerging mitochondrial and cellular themes and variations in neuronal injury. J. Alzheimers. Dis. 20(Suppl. 2), S453-S473
3. Lin, M. T., and Beal, M. F. (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443, 787-795
4. Morais, V. A., and De Strooper, B. (2010) Mitochondria dysfunction and neurodegenerative disorders: cause or consequence. J. Alzheimers Dis. 20(Suppl. 2), S255-S263
5. Muller, W. E., Eckert, A., Kurz, C., Eckert, G. P., and Leuner, K. (2010) Mitochondrial dysfunction: common final pathway in brain aging and Alzheimer's disease-Therapeutic aspects. Mol. Neurobiol. 41, 159-171
6. Shi, Q., and Gibson, G. E. (2007) Oxidative stress and transcriptional regulation in Alzheimer disease. Alzheimer Dis. Assoc. Disord. 21, 276-291
7. Go, Y. M., and Jones, D. P. (2010) Redox control systems in the nucleus: mechanisms and functions. Antioxid. Redox Signal. 13, 489-509
8. Ma, Q. (2010) Transcriptional responses to oxidative stress: pathological and toxicological implications. Pharmacol. Ther. 125, 376-393
9. Puigserver, P., Wu, Z., Park, C. W., Graves, R., Wright, M., and Spiegelman, B. M. (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92, 829-839
10. Puigserver, P., and Spiegelman, B. M. (2003) Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr. Rev. 24, 78-90
11. Lin, J., Handschin, C., and Spiegelman, B. M. (2005) Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 1, 361-370
12. Scarpulla, R. C. (2008) Nuclear control of respiratory chain expression by nuclear respiratory factors and PGC-1-related coactivator. Ann. N. Y. Acad. Sci. 1147, 321-334
13. Wu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., Troy, A., Cinti, S., Lowell, B., Scarpulla, R. C., and Spiegelman, B. M. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98, 115-124
14. Qin, W., Haroutunian, V., Katsel, P., Cardozo, C. P., Ho, L., Buxbaum, J. D., and Pasinetti, G. M. (2009) PGC-1alpha expression decreases in the Alzheimer disease brain as a function of dementia. Arch. Neurol. 66, 352-361
15. Gong, B., Chen, F., Pan, Y., Arrieta-Cruz, I., Yoshida, Y., Haroutunian, V., and Pasinetti, G. M. (2010) SCFFbx2-E3-ligasemediated degradation of BACE1 attenuates Alzheimer's disease amyloidosis and improves synaptic function. Aging Cell. 9, 1018-1031
16. Sheng, B., Wang, X., Su, B., Lee, H. G., Casadesus, G., Perry, G., and Zhu, X. (2012) Impaired mitochondrial biogenesis contributes to mitochondrial dysfunction in Alzheimer's disease. J. Neurochem. 120, 419-429
17. Chishti, M. A., Yang, D. S., Janus, C., Phinney, A. L., Horne, P., Pearson, J., Strome, R., Zuker, N., Loukides, J., French, J., Turner, S., Lozza, G., Grilli, M., Kunicki, S., Morissette, C., Paquette, J., Gervais, F., Bergeron, C., Fraser, P. E., Carlson, G. A., George-Hyslop, P. S., and Westaway, D. (2001) Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J. Biol. Chem. 276, 21562-21570
18. Li, F., Calingasan, N. Y., Yu, F., Mauck, W. M., Toidze, M., Almeida, C. G., Takahashi, R. H., Carlson, G. A., Flint Beal, M., Lin, M. T., and Gouras, G. K. (2004) Increased plaque burden in brains of APP mutant MnSOD heterozygous knockout mice. J. Neurochem. 89, 1308-1312
19. Dumont, M., Wille, E., Calingasan, N. Y., Tampellini, D., Williams, C., Gouras, G. K., Liby, K., Sporn, M., Nathan, C., Flint Beal, M., and Lin, M. T. (2009) Triterpenoid CDDO-methylamide improves memory and decreases amyloid plaques in a transgenic mouse model of Alzheimer's disease. J. Neurochem. 109, 502-512
20. Dumont, M., Wille, E., Stack, C., Calingasan, N. Y., Beal, M. F., and Lin, M. T. (2009) Reduction of oxidative stress, amyloid deposition, and memory deficit by manganese superoxide dismutase overexpression in a transgenic mouse model of Alzheimer's disease. FASEB J. 23, 2459-2466
21. Liang, H., Balas, B., Tantiwong, P., Dube, J., Goodpaster, B. H., O'Doherty, R. M., DeFronzo, R. A., Richardson, A., Musi, N., and Ward, W. F. (2009) Whole body overexpression of PGC-1-has opposite effects on hepatic and muscle insulin sensitivity. Am. J. Physiol. Endocrinol. Metab. 296, E945-E954
22. Dumont, M., Wille, E., Calingasan, N. Y., Nathan, C., Flint Beal, M., and Lin, M. T. N-iminoethyl-L-lysine improves memory and reduces amyloid pathology in a transgenic mouse model of amyloid deposition. Neurochem. Int. 56, 345-351
23. Degli Esposti, M., Ghelli, A., Crimi, M., Estornell, E., Fato, R., and Lenaz, G. (1993) Complex I and complex III of mitochondria have common inhibitors acting as ubiquinone antagonists. Biochem. Biophys. Res. Commun. 190, 1090-1096
24. Arrigoni, O., and Singer, T. P. (1962) Limitations of the phenazine methosulphate assay for succinic and related dehydrogenases. Nature 193, 1256-1258
25. Srere, P. A. (1969) Citrate synthase. Methods Enzymol. 13, 3-11
26. Cheroni, C., Peviani, M., Cascio, P., Debiasi, S., Monti, C., and Bendotti, C. (2005) Accumulation of human SOD1 and ubiquitinated deposits in the spinal cord of SOD1G93A mice during motor neuron disease progression correlates with a decrease of proteasome. Neurobiol. Dis. 18, 509-522
27. Luo, W. J., Wang, H., Li, H., Kim, B. S., Shah, S., Lee, H. J., Thinakaran, G., Kim, T. W., Yu, G., and Xu, H. (2003) PEN-2 and APH-1 coordinately regulate proteolytic processing of presenilin 1. J. Biol. Chem. 278, 7850-7854
28. Ciechanover, A. (1994) The ubiquitin-proteasome proteolytic pathway. Cell 79, 13-21
29. Launay, N., Ruiz, M., Fourcade, S., Schlüter, A., Guilera, C., Ferrer, I., Knecht, E., and Pujol, A. (2013) Oxidative stress regulates the ubiquitin-proteasome system and immunoproteasome functioning in a mouse model of X-adrenoleukodystrophy. Brain 136, 891-904
30. Handschin, C., and Spiegelman, B. M. (2006) Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr. Rev. 27, 728-735
31. Rona-Voros, K., and Weydt, P. (2010) The role of PGC-1alpha in the pathogenesis of neurodegenerative disorders. Curr. Drug Targets 11, 1262-1269
32. Zheng, B., Liao, Z., Locascio, J. J., Lesniak, K. A., Roderick, S. S., Watt, M. L., Eklund, A. C., Zhang-James, Y., Kim, P. D., Hauser, M. A., Grunblatt, E., Moran, L. B., Mandel, S. A., Riederer, P., Miller, R. M., Federoff, H. J., Wullner, U., Papapetropoulos, S., Youdim, M. B., Cantuti-Castelvetri, I., Young, A. B., Vance, J. M., Davis, R. L., Hedreen, J. C., Adler, C. H., Beach, T. G., Graeber, M. B., Middleton, F. A., Rochet, J. C., and Scherzer, C. R. (2010) PGC-1-, a potential therapeutic target for early intervention in Parkinson's disease. Sci Transl. Med. 2, 52ra73
33. Lin, J., Wu, P. H., Tarr, P. T., Lindenberg, K. S., St-Pierre, J., Zhang, C. Y., Mootha, V. K., Jager, S., Vianna, C. R., Reznick, R. M., Cui, L., Manieri, M., Donovan, M. X., Wu, Z., Cooper, M. P., Fan, M. C., Rohas, L. M., Zavacki, A. M., Cinti, S., Shulman, G. I., Lowell, B. B., Krainc, D., and Spiegelman, B. M. (2004) Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1-null mice. Cell 119, 121-135
34. Weydt, P., Pineda, V. V., Torrence, A. E., Libby, R. T., Satterfield, T. F., Lazarowski, E. R., Gilbert, M. L., Morton, G. J., Bammler, T. K., Strand, A. D., Cui, L., Beyer, R. P., Easley, C. N., Smith, A. C., Krainc, D., Luquet, S., Sweet, I. R., Schwartz, M. W., and La Spada, A. R. (2006) Thermoregulatory and metabolic defects in Huntington's disease transgenic mice implicate PGC-1-in Huntington's disease neurodegeneration. Cell Metab. 4, 349-362
35. Zhai, W., Jeong, H., Cui, L., Krainc, D., and Tjian, R. (2005) In vitro analysis of huntingtin-mediated transcriptional repression reveals multiple transcription factor targets. Cell 123, 1241-1253
36. Chaturvedi, R. K., Adhihetty, P., Shukla, S., Hennessy, T., Calingasan, N., Yang, L., Starkov, A., Kiaei, M., Cannella, M., Sassone, J., Ciammola, A., Squitieri, F., and Beal, M. F. (2009) Impaired PGC-1-function in muscle in Huntington's disease. Hum. Mol. Genet. 18, 3048-3065
37. Chaturvedi, R. K., Calingasan, N. Y., Yang, L., Hennessey, T., Johri, A., and Beal, M. F. (2010) Impairment of PGC-1-expression, neuropathology and hepatic steatosis in a transgenic mouse model of Huntington's disease following chronic energy deprivation. Hum. Mol. Genet. 19, 3190-3205
38. Kim, J., Moody, J. P., Edgerly, C. K., Bordiuk, O. L., Cormier, K., Smith, K., Beal, M. F., and Ferrante, R. J. (2010) Mitochondrial loss, dysfunction and altered dynamics in Huntington's disease. Hum. Mol. Genet. 19, 3919-3935
39. 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
40. Shin, J. H., Ko, H. S., Kang, H., Lee, Y., Lee, Y. I., Pletinkova, O., Troconso, J. C., Dawson, V. L., and Dawson, T. M. (2011) PARIS (ZNF746) repression of PGC-1alpha contributes to neurodegeneration in Parkinson's disease. Cell 144, 689-702
41. Zhao, W., Varghese, M., Yemul, S., Pan, Y., Cheng, A., Marano, P., Hassan, S., Vempati, P., Chen, F., Qian, X., and Pasinetti, G. M. (2011) Peroxisome proliferator activator receptor gamma coactivator-1-(PGC-1-) improves motor performance and survival in a mouse model of amyotrophic lateral sclerosis. Mol. Neurodegener. 6, 51
42. Melov, S., Adlard, P. A., Morten, K., Johnson, F., Golden, T. R., Hinerfeld, D., Schilling, B., Mavros, C., Masters, C. L., Volitakis, I., Li, Q. X., Laughton, K., Hubbard, A., Cherny, R. A., Gibson, B., and Bush, A. I. (2007) Mitochondrial oxidative stress causes hyperphosphorylation of tau. PLoS ONE 2, e536
43. Katsouri, L., Parr, C., Bogdanovic, N., Willem, M., and Sastre, M. (2011) PPAR-coactivator-1-(PGC-1-) reduces amyloid-beta generation through a PPAR-dependent mechanism. J. Alzheimers Dis. 25, 151-162
44. Beal, M. F. (2009) Therapeutic approaches to mitochondrial dysfunction in Parkinson's disease. Parkinsonism Relat. Disord. 15(Suppl. 3), S189-S194
45. Keeney, P. M., Quigley, C. K., Dunham, L. D., Papageorge, C. M., Iyer, S., Thomas, R. R., Schwarz, K. M., Trimmer, P. A., Khan, S. M., Portell, F. R., Bergquist, K. E., and Bennett, J. P., Jr. (2009) Mitochondrial gene therapy augments mitochondrial physiology in a Parkinson's disease cell model. Hum. Gene Ther. 20, 897-907
46. McGill, J. K., and Beal, M. F. (2006) PGC-1-, a new therapeutic target in Huntington's disease? Cell 127, 465-468
47. Ciron, C., Lengacher, S., Dusonchet, J., Aebischer, P., and Schneider, B. L. (2012) Sustained expression of PGC-1-in the rat nigrostriatal system selectively impairs dopaminergic function. Hum. Mol. Genet. 21, 1861-1876
48. Miura, S., Tomitsuka, E., Kamei, Y., Yamazaki, T., Kai, Y., Tamura, M., Kita, K., Nishino, I., and Ezaki, O. (2006) Overexpression of peroxisome proliferator-activated receptor gamma co-activator-1-leads to muscle atrophy with depletion of ATP. Am. J. Pathol. 169, 1129-1139
49. Russell, L. K., Mansfield, C. M., Lehman, J. J., Kovacs, A., Courtois, M., Saffitz, J. E., Medeiros, D. M., Valencik, M. L., McDonald, J. A., and Kelly, D. P. (2004) Cardiac-specific induction of the transcriptional coactivator peroxisome proliferatoractivated receptor gamma coactivator-1- promotes mitochondrial biogenesis and reversible cardiomyopathy in a developmental stage-dependent manner. Circ. Res. 94, 525-533
50. Brault, J. J., Jespersen, J. G., and Goldberg, A. L. (2010) Peroxisome proliferator-activated receptor gamma coactivator 1-or 1-overexpression inhibits muscle protein degradation, induction of ubiquitin ligases, and disuse atrophy. J. Biol. Chem. 285, 19460-19471
51. Wenz, T., Rossi, S. G., Rotundo, R. L., Spiegelman, B. M., and Moraes, C. T. (2009) Increased muscle PGC-1-expression protects from sarcopenia and metabolic disease during aging. Proc. Natl. Acad. Sci. U. S. A. 106, 20405-20410
52. Cripps, D., Thomas, S. N., Jeng, Y., Yang, F., Davies, P., and Yang, A. J. (2006) Alzheimer disease-specific conformation of hyperphosphorylated paired helical filament-Tau is polyubiquitinated through Lys-48, Lys-11, and Lys-6 ubiquitin conjugation. J. Biol. Chem. 281, 10825-10838
53. Ii, K., Ito, H., Tanaka, K., and Hirano, A. (1997) Immunocytochemical co-localization of the proteasome in ubiquitinated structures in neurodegenerative diseases and the elderly. J. Neuropathol. Exp. Neurol. 56, 125-131
54. Ren, Q. G., Liao, X. M., Chen, X. Q., Liu, G. P., and Wang, J. Z. (2007) Effects of tau phosphorylation on proteasome activity. FEBS Lett. 581, 1521-1528
55. Li, Y. P., Chen, Y., Li, A. S., and Reid, M. B. (2003) Hydrogen peroxide stimulates ubiquitin-conjugating activity and expression of genes for specific E2 and E3 proteins in skeletal muscle myotubes. Am. J. Physiol. Cell Physiol. 285, C806-C812
56. Geng, T., Li, P., Yin, X., and Yan, Z. (2011) PGC-1-promotes nitric oxide antioxidant defenses and inhibits FOXO signaling against cardiac cachexia in mice. Am. J. Pathol. 178, 1738-1748
57. Hishiya, A., Iemura, S., Natsume, T., Takayama, S., Ikeda, K., and Watanabe, K. (2006) A novel ubiquitin-binding protein ZNF216 functioning in muscle atrophy. EMBO J. 25, 554-564
58. Tsunemi, T., Ashe, T. D., Morrison, B. E., Soriano, K. R., Au, J., Roque, R. A., Lazarowski, E. R., Damian, V. A., Masliah, E., and La Spada, A. R. PGC-1-rescues Huntington's disease proteotoxicity by preventing oxidative stress and promoting TFEB function. Sci. Transl. Med. 4, 142ra197
59. Lustbader, J. W., Cirilli, M., Lin, C., Xu, H. W., Takuma, K., Wang, N., Caspersen, C., Chen, X., Pollak, S., Chaney, M., Trinchese, F., Liu, S., Gunn-Moore, F., Lue, L. F., Walker, D. G., Kuppusamy, P., Zewier, Z. L., Arancio, O., Stern, D., Yan, S. S., and Wu, H. (2004) ABAD directly links Abeta to mitochondrial toxicity in Alzheimer's disease. Science 304, 448-452
60. Yao, J., Du, H., Yan, S., Fang, F., Wang, C., Lue, L. F., Guo, L., Chen, D., Stern, D. M., Gunn Moore, F. J., Xi Chen, J., Arancio, O., and Yan, S. S. (2011) Inhibition of amyloid-(A-) peptidebinding alcohol dehydrogenase-A- interaction reduces A-accumulation and improves mitochondrial function in a mouse model of Alzheimer's disease. J. Neurosci. 31, 2313-2320
61. Du, H., Guo, L., and Yan, S. S. (2012) Synaptic mitochondrial pathology in Alzheimer's disease. Antioxid. Redox Signal. 16, 1467-1475