PGC-1α, a potential therapeutic target for early intervention in Parkinson's disease

Science Translational Medicine

Volumn 2, Issue 52, 2010, Pages

  Zheng, Bin ^a   Liao, Zhixiang ^a   Locascio, Joseph J ^b   Lesniak, Kristen A ^c   Roderick, Sarah S ^a   Watt, Marla L ^c   Eklund, Aron C ^a,d   Zhang James, Yanli ^e   Kim, Peter D ^e   Hauser, Michael A ^f   Grünblatt, Edna ^g   Moran, Linda B ^h   Mandel, Silvia A ⁱ   Riederer, Peter ^g   Miller, Renee M ^j   Federoff, Howard J ^k   Wüllner, Ullrich ^l   Papapetropoulos, Spyridon ^m,n   Youdim, Moussa B ^i,o   Cantuti Castelvetri, Ippolita ^b   Young, Anne B ^b   Vance, Jeffery M ^m   Davis, Richard L ^p   Hedreen, John C ^q   Adler, Charles H ^q   Beach, Thomas G ^r   Graeber, Manuel B ^r   Middleton, Frank A ^p   Rochet, Jean Christophe ^c   Scherzer, Clemens R ^a,s   more..

^a Brigham and Women's Hospital Center for Neurologic Diseases   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c PURDUE UNIVERSITY   (United States)

^d TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^e State University of New York Upstate Medical University: College of Medicine   (United States)

^f DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF WÜRZBURG   (Germany)

^h Technion Faculty of Medicine ^*

ⁱ TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^j UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^k GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^l UNIVERSITY OF BONN   (Germany)

^m UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

ⁿ ALLERGAN INC   (United States)

^o Yonsei University   (South Korea)

^p MCLEAN HOSPITAL   (United States)

^q MAYO CLINIC   (United States)

^r UNIVERSITY OF SYDNEY   (Australia)

^s BRIGHAM AND WOMEN S HOSPITAL   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; CYTOCHROME C OXIDASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE; SUCCINATE DEHYDROGENASE (UBIQUINONE); TRANSCRIPTOME; UBIQUINOL CYTOCHROME C REDUCTASE; DOPAMINE; HEAT SHOCK PROTEIN; PPARGC1A PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ADULT; AGED; ARTICLE; CELL ENERGY; CONTROLLED STUDY; DIFFUSE LEWY BODY DISEASE; DOPAMINERGIC NERVE CELL; DRUG TARGETING; EARLY INTERVENTION; FEMALE; GENE EXPRESSION; GENETIC ASSOCIATION; GLUCOSE UTILIZATION; HUMAN; HUMAN TISSUE; LASER CAPTURE MICRODISSECTION; MAJOR CLINICAL STUDY; MALE; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL RESPIRATION; PARKINSON DISEASE; PRIORITY JOURNAL; SUBSTANTIA NIGRA; BIOLOGY; EARLY DIAGNOSIS; GENETIC DATABASE; GENETICS; META ANALYSIS; METABOLISM; METHODOLOGY; MIDDLE AGED; NERVE CELL; PATHOLOGY;

ADULT; AGED; AGED, 80 AND OVER; ALPHA-SYNUCLEIN; COMPUTATIONAL BIOLOGY; DATABASES, GENETIC; DOPAMINE; EARLY DIAGNOSIS; GENOME-WIDE ASSOCIATION STUDY; HEAT-SHOCK PROTEINS; HUMANS; MALE; MIDDLE AGED; NEURONS; PARKINSON DISEASE; TRANSCRIPTION FACTORS;

EID: 77958072667     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3001059     Document Type: Article

References (66)

1. A. S. Dhillon, G. L. Tarbutton, J. L. Levin, G. M. Plotkin, L. K. Lowry, J. T. Nalbone, S. Shepherd, Pesticide/environmental exposures and Parkinson's disease in East Texas. J. Agromedicine 13, 37-48 (2008).
2. A. R. Chade, M. Kasten, C. M. Tanner, Nongenetic causes of Parkinson's disease. J. Neural Transm. Suppl. 147-151 (2006).
3. T. B. Sherer, R. Betarbet, C. M. Testa, B. B. Seo, J. R. Richardson, J. H. Kim, G. W. Miller, T. Yagi, A. Matsuno-Yagi, J. T. Greenamyre, Mechanism of toxicity in rotenone models of Parkinson's disease. J. Neurosci. 23, 10756-10764 (2003).
4. H. J. Park, H. J. Kim, H. K. Park, J. H. Chung, Protective effect of histamine H2 receptor antagonist ranitidine against rotenone-induced apoptosis. Neurotoxicology 30, 1114-1119 (2009).
5. R. Betarbet, T. B. Sherer, G. MacKenzie, M. Garcia-Osuna, A. V. Panov, J. T. Greenamyre, Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci. 3, 1301-1306 (2000).
6. J. W. Langston, P. Ballard, J. W. Tetrud, I. Irwin, Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science 219, 979-980 (1983).
7. C. Henchcliffe, M. F. Beal, Mitochondrial biology and oxidative stress in Parkinson disease pathogenesis. Nat. Clin. Pract. Neurol. 4, 600-609 (2008).
8. J. Park, S. B. Lee, S. Lee, Y. Kim, S. Song, S. Kim, E. Bae, J. Kim, M. Shong, J. M. Kim, J. Chung, Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 441, 1157-1161 (2006).
9. J. C. Greene, A. J. Whitworth, I. Kuo, L. A. Andrews, M. B. Feany, L. J. Pallanck, Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc. Natl. Acad. Sci. U.S.A. 100, 4078-4083 (2003).
10. L. Devi, V. Raghavendran, B. M. Prabhu, N. G. Avadhani, H. K. Anandatheerthavarada, Mitochondrial import and accumulation of α-synuclein impair complex I in human dopaminergic neuronal cultures and Parkinson disease brain. J. Biol. Chem. 283, 9089-9100 (2008).
11. S. Roy, L. Wolman, Ultrastructural observations in Parkinsonism. J. Pathol. 99, 39-44 (1969).
12. C. R. Scherzer, K. Offe, M. Gearing, H. D. Rees, G. Fang, C. J. Heilman, C. Schaller, H. Bujo, A. I. Levey, J. J. Lah, Loss of apolipoprotein E receptor LR11 in Alzheimer disease. Arch. Neurol. 61, 1200-1205 (2004).
13. C. R. Scherzer, Chipping away at diagnostics for neurodegenerative diseases. Neurobiol. Dis. 35, 148-156 (2009).
14. E. E. Schadt, J. Lamb, X. Yang, J. Zhu, S. Edwards, D. Guhathakurta, S. K. Sieberts, S. Monks, M. Reitman, C. Zhang, P. Y. Lum, A. Leonardson, R. Thieringer, J. M. Metzger, L. Yang, J. Castle, H. Zhu, S. F. Kash, T. A. Drake, A. Sachs, A. J. Lusis, An integrative genomics approach to infer causal associations between gene expression and disease. Nat. Genet. 37, 710-717 (2005).
15. C. R. Scherzer, A. C. Eklund, L. J. Morse, Z. Liao, J. J. Locascio, D. Fefer, M. A. Schwarzschild, M. G. Schlossmacher, M. A. Hauser, J. M. Vance, L. R. Sudarsky, D. G. Standaert, J. H. Growdon, R. V. Jensen, S. R. Gullans, Molecular markers of early Parkinson's disease based on gene expression in blood. Proc. Natl. Acad. Sci. U.S.A. 104, 955-960 (2007).
16. C. R. Scherzer, J. A. Grass, Z. Liao, I. Pepivani, B. Zheng, A. C. Eklund, P. A. Ney, J. Ng, M. McGoldrick, B. Mollenhauer, E. H. Bresnick, M. G. Schlossmacher, GATA transcription factors directly regulate the Parkinson's disease-linked gene α-synuclein. Proc. Natl. Acad. Sci. U.S.A. 105, 10907-10912 (2008).
17. E. Grunblatt, S. Mandel, J. Jacob-Hirsch, S. Zeligson, N. Amariglo, G. Rechavi, J. Li, R. Ravid, W. Roggendorf, P. Riederer, M. B. Youdim, Gene expression profiling of parkinsonian substantia nigra pars compacta; alterations in ubiquitin-proteasome, heat shock protein, iron and oxidative stress regulated proteins, cell adhesion/cellular matrix and vesicle trafficking genes. J. Neural Transm. 111, 1543-1573 (2004).
18. M. A. Hauser, Y. J. Li, H. Xu, M.A. Noureddine, Y. S. Shao, S. R. Gullans, C. R. Scherzer, R. V. Jensen, A. C. McLaurin, J. R. Gibson, B. L. Scott, R. M. Jewett, J. E. Stenger, D. E. Schmechel, C. M. Hulette, J. M. Vance, Expression profiling of substantia nigra in Parkinson disease, progressive supranuclear palsy, and frontotemporal dementia with parkinsonism. Arch. Neurol. 62, 917-921 (2005).
19. L. B. Moran, D. C. Duke, M. Deprez, D. T. Dexter, R. K. Pearce, M. B. Graeber, Whole genome expression profiling of the medial and lateral substantia nigra in Parkinson's disease. Neurogenetics 7, 1-11 (2006).
20. S. Papapetropoulos, J. Ffrench-Mullen, D. McCorquodale, Y. Qin, J. Pablo, D. C. Mash, Multiregional gene expression profiling identifies MRPS6 as a possible candidate gene for Parkinson's disease. Gene Expr. 13, 205-215 (2006).
21. I. Cantuti-Castelvetri, C. Keller-McGandy, B. Bouzou, G. Asteris, T. W. Clark, M. P. Frosch, D. G. Standaert, Effects of gender on nigral gene expression and Parkinson disease. Neurobiol. Dis. 26, 606-614 (2007).
22. Y. Zhang, M. James, F. A. Middleton, R. L. Davis, Transcriptional analysis of multiple brain regions in Parkinson's disease supports the involvement of specific protein processing, energy metabolism, and signaling pathways, and suggests novel disease mechanisms. Am. J. Med. Genet. B Neuropsychiatr. Genet. 137B, 5-16 (2005).
23. I. R. Vogt, A. J. Lees, B. O. Evert, T. Klockgether, M. Bonin, U. Wullner, Transcriptional changes in multiple system atrophy and Parkinson's disease putamen. Exp. Neurol. 199, 465-478 (2006).
24. F. Simunovic,M. Yi, Y.Wang, L.Macey, L. T. Brown, A.M. Krichevsky, S. L. Andersen, R.M. Stephens, F. M. Benes, K. C. Sonntag, Gene expression profiling of substantia nigra dopamine neurons: Further insights into Parkinson's disease pathology. Brain 132, 1795-1809 (2009).
25. A. Subramanian, P. Tamayo, V. K. Mootha, S. Mukherjee, B. L. Ebert, M. A. Gillette, A. Paulovich, S. L. Pomeroy, T. R.Golub, E. S. Lander, J. P.Mesirov,Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U.S.A. 102, 15545-15550 (2005).
26. A. Subramanian, H. Kuehn, J. Gould, P. Tamayo, J. P. Mesirov, GSEA-P: A desktop application for Gene Set Enrichment Analysis. Bioinformatics 23, 3251-3253 (2007).
27. V. K. Mootha, C. M. Lindgren, K. F. Eriksson, A. Subramanian, S. Sihag, J. Lehar, P. Puigserver, E. Carlsson, M. Ridderstråle, E. Laurila, N. Houstis, M. J. Daly, N. Patterson, J. P. Mesirov, T. R. Golub, P. Tamayo, B. Spiegelman, E. S. Lander, J. N. Hirschhorn, D. Altshuler, L. C. Groop, PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34, 267-273 (2003).
28. C. R. Blyth, On Simpson's paradox and the sure-thing principle. J. Am. Stat. Assoc. 67, 364-372 (1972).
29. M. Thomassen, Q. Tan, T. A. Kruse, Gene expression meta-analysis identifies chromosomal regions and candidate genes involved in breast cancer metastasis. Breast Cancer Res. Treat. 113, 239-249 (2009).
30. L. V. Hedges, J. L. Vevea, Fixed- and random-effects models in meta-analysis. Psychol. Methods 3, 486-504 (1998).
31. K. A. Jellinger, A critical evaluation of current staging of a-synuclein pathology in Lewy body disorders. Biochim. Biophys. Acta 1792, 730-740 (2009).
32. D. W. Dickson, H. Fujishiro, A. DelleDonne, J. Menke, Z. Ahmed, K. J. Klos, K. A. Josephs, R. Frigerio, M. Burnett, J. E. Parisi, J. E. Ahlskog, Evidence that incidental Lewy body disease is pre-symptomatic Parkinson's disease. Acta Neuropathol. 115, 437-444 (2008).
33. A. DelleDonne, K. J. Klos, H. Fujishiro, Z. Ahmed, J. E. Parisi, K. A. Josephs, R. Frigerio, M. Burnett, Z. K. Wszolek, R. J. Uitti, J. E. Ahlskog, D. W. Dickson, Incidental Lewy body disease and preclinical Parkinson disease. Arch. Neurol. 65, 1074-1080 (2008).
34. T. G. Beach, C. H. Adler, L. I. Sue, J. B. Peirce, J. Bachalakuri, J. E. Dalsing-Hernandez, L. F. Lue, J. N. Caviness, D. J. Connor, M. N. Sabbagh, D. G. Walker, Reduced striatal tyrosine hydroxylase in incidental Lewy body disease. Acta Neuropathol. 115, 445-451 (2008).
35. J. M. Fearnley, A. J. Lees, Ageing and Parkinson's disease: Substantia nigra regional selectivity. Brain 114, 2283-2301 (1991).
36. H. Braak, K. Del Tredici, U. Rüb, R. A. de Vos, E. N. Jansen Steur, E. Braak, Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol. Aging 24, 197-211 (2003).
37. R. Savica, W. A. Rocca, J. E. Ahlskog, When does Parkinson disease start? Arch. Neurol. 67, 798-801 (2010).
38. L. S. Forno, Concentric hyalin intraneuronal inclusions of Lewy type in the brains of elderly persons (50 incidental cases): Relationship to parkinsonism. J. Am. Geriatr. Soc. 17, 557-575 (1969).
39. G. W. Ross, H. Petrovitch, R. D. Abbott, J. Nelson, W. Markesbery, D. Davis, J. Hardman, L. Launer, K. Masaki, C. M. Tanner, L. R. White, Parkinsonian signs and substantia nigra neuron density in decendents elders without PD. Ann. Neurol. 56, 532-539 (2004).
40. K. A. Jellinger, Critical evaluation of the Braak staging scheme for Parkinson's disease. Ann. Neurol. 67, 550 (2010).
41. H. Braak, K. Del Tredici, Invited Article: Nervous system pathology in sporadic Parkinson disease. Neurology 70, 1916-1925 (2008).
42. R. E. Burke, W. T. Dauer, J. P. Vonsattel, A critical evaluation of the Braak staging scheme for Parkinson's disease. Ann. Neurol. 64, 485-491 (2008).
43. D. W. Dickson, H. Uchikado, H. Fujishiro, Y. Tsuboi, Evidence in favor of Braak staging of Parkinson's disease. Mov. Disord. 25 (Suppl. 1), S78-S82 (2010).
44. E. Dalfó, M. Portero-Otín, V. Ayala, A. Martínez, R. Pamplona, I. Ferrer, Evidence of oxidative stress in the neocortex in incidental Lewy body disease. J. Neuropathol. Exp. Neurol. 64, 816-830 (2005).
45. D. T. Dexter, J. Sian, S. Rose, J. G. Hindmarsh, V. M. Mann, J. M. Cooper, F. R. Wells, S. E. Daniel, A. J. Lees, A. H. Schapira, P. Jenner, C. D. Marsden, Indices of oxidative stress and mitochondrial function in individuals with incidental Lewy body disease. Ann. Neurol. 35, 38-44 (1994).
46. R. H. Haas, F. Nasirian, K. Nakano, D. Ward, M. Pay, R. Hill, C. W. Shults, Low platelet mitochondrial complex I and complex II/III activity in early untreated Parkinson's disease. Ann. Neurol. 37, 714-722 (1995).
47. P. Barbanti, G. Fabbrini, A. Ricci, R. Cerbo, E. Bronzetti, B. Caronti, C. Calderaro, L. Felici, F. Stocchi, G. Meco, F. Amenta, G. L. Lenzi, Increased expression of dopamine receptors on lymphocytes in Parkinson's disease. Mov. Disord. 14, 764-771 (1999).
48. C. R. Scherzer, M. B. Feany, Yeast genetics targets lipids in Parkinson's disease. Trends Genet. 20, 273-277 (2004).
49. B. C. Bowen, R. E. Block, J. Sanchez-Ramos, P. M. Pattany, D. A. Lampman, J. B. Murdoch, R. M. Quencer, Proton MR spectroscopy of the brain in 14 patients with Parkinson disease. AJNR Am. J. Neuroradiol. 16, 61-68 (1995).
50. 18FDG-PET study. Brain 123, 340-352 (2000).
51. J. Lin, C. Handschin, B. M. Spiegelman, Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 1, 361-370 (2005).
52. Z. Arany, H. He, J. Lin, K. Hoyer, C. Handschin, O. Toka, F. Ahmad, T. Matsui, S. Chin, P. H. Wu, I. I. Rybkin, J. M. Shelton, M. Manieri, S. Cinti, F. J. Schoen, R. Bassel-Duby, A. Rosenzweig, J. S. Ingwall, B. M. Spiegelman, Transcriptional coactivator PGC-1α controls the energy state and contractile function of cardiac muscle. Cell Metab. 1, 259-271 (2005).
53. L. M. Rohas, J. St-Pierre, M. Uldry, S. Jäger, C. Handschin, B. M. Spiegelman, A fundamental system of cellular energy homeostasis regulated by PGC-1a. Proc. Natl. Acad. Sci. U.S.A. 104, 7933-7938 (2007).
54. A. A. Cooper, A. D. Gitler, A. Cashikar, C. M. Haynes, K. J. Hill, B. Bhullar, K. Liu, K. Xu, K. E. Strathearn, F. Liu, S. Cao, K. A. Caldwell, G. A. Caldwell, G. Marsischky, R. D. Kolodner, J. Labaer, J. C. Rochet, N. M. Bonini, S. Lindquist, α-Synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson's models. Science 313, 324-328 (2006).
55. F. Liu, J. L. Nguyen, J. D. Hulleman, L. Li, J. C. Rochet, Mechanisms of DJ-1 neuroprotection in a cellular model of Parkinson's disease. J. Neurochem. 105, 2435-2453 (2008).
56. A. D. Gitler, A. Chesi, M. L. Geddie, K. E. Strathearn, S. Hamamichi, K. J. Hill, K. A. Caldwell, G. A. Caldwell, A. A. Cooper, J. C. Rochet, S. Lindquist, α-Synuclein is part of a diverse and highly conserved interaction network that includes PARK9 and manganese toxicity. Nat. Genet. 41, 308-315 (2009).
57. F. Liu, J. Hindupur, J. L. Nguyen, K. J. Ruf, J. Zhu, J. L. Schieler, C. C. Bonham, K. V. Wood, V. J. Davisson, J. C. Rochet, Methionine sulfoxide reductase A protects dopaminergic cells from Parkinson's disease-related insults. Free Radic. Biol. Med. 45, 242-255 (2008).
58. M. V. Berridge, A. S. Tan, Characterization of the cellular reduction of 3-(4,5-dimethylthiazol-2- yl)-2,5-diphenyltetrazolium bromide (MTT): Subcellular localization, substrate dependence, and involvement of mitochondrial electron transport in MTT reduction. Arch. Biochem. Biophys. 303, 474-482 (1993).
59. S. Przedborski, K. Tieu, C. Perier, M. Vila, MPTP as a mitochondrial neurotoxic model of Parkinson's disease. J. Bioenerg. Biomembr. 36, 375-379 (2004).
60. J. St-Pierre, S. Drori, M. Uldry, J. M. Silvaggi, J. Rhee, S. Jäger, C. Handschin, K. Zheng, J. Lin, W. Yang, D. K. Simon, R. Bachoo, B. M. Spiegelman, Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127, 397-408 (2006).
61. R. M. Silva, V. Ries, T. F. Oo, O. Yarygina, V. Jackson-Lewis, E. J. Ryu, P. D. Lu, S. J. Marciniak, D. Ron, S. Przedborski, N. Kholodilov, L. A. Greene, R. E. Burke, CHOP/GADD153 is a mediator of apoptotic death in substantia nigra dopamine neurons in an in vivo neurotoxin model of parkinsonism. J. Neurochem. 95, 974-986 (2005).
62. W. D. Parker Jr., J. K. Parks, R. H. Swerdlow, Complex I deficiency in Parkinson's disease frontal cortex. Brain Res. 1189, 215-218 (2008).
63. P. M. Keeney, J. Xie, R. A. Capaldi, J. P. Bennett Jr., Parkinson's disease brain mitochondrial complex I has oxidatively damaged subunits and is functionally impaired and misassembled. J. Neurosci. 26, 5256-5264 (2006).
64. V. A. Morais, B. De Strooper, Mitochondria dysfunction and neurodegenerative disorders: Cause or consequence. J. Alzheimers Dis. 20 (Suppl. 2), S255-S263 (2010).
65. S. Geisler, K. M. Holmström, D. Skujat, F. C. Fiesel, O. C. Rothfuss, P. J. Kahle, W. Springer, PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 12, 119-131 (2010).
66. R. C. Gentleman, V. J. Carey, D. M. Bates, B. Bolstad, M. Dettling, S. Dudoit, B. Ellis, L. Gautier, Y. Ge, J. Gentry, K. Hornik, T. Hothorn, W. Huber, S. Iacus, R. Irizarry, F. Leisch, C. Li, M. Maechler, A. J. Rossini, G. Sawitzki, C. Smith, G. Smyth, L. Tierney, J. Y. Yang, J. Zhang, Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol. 5, R80 (2004).