Caloric restriction and the nutrient-sensing PGC-1α in mitochondrial homeostasis: New perspectives in neurodegeneration

International Journal of Cell Biology

Volumn , Issue , 2012, Pages

  Lettieri Barbato, Daniele ^a   Baldelli, Sara ^a   Pagliei, Beatrice ^a   Aquilano, Katia ^a   Ciriolo, Maria Rosa ^a,b  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b IRCCS SAN RAFFAELE PISANA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; MITOGEN ACTIVATED PROTEIN KINASE 14; MYOCYTE ENHANCER FACTOR 2; NEURONAL NITRIC OXIDE SYNTHASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; REACTIVE OXYGEN METABOLITE; RESVERATROL; SIRTUIN 1; STEROID RECEPTOR COACTIVATOR 3; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR NRF1; TRANSCRIPTION FACTOR NRF2; TRANSCRIPTION FACTOR YY1; UBIQUITIN PROTEIN LIGASE E3;

BIOGENESIS; CALORIC RESTRICTION; CELL COMMUNICATION; CELL FUNCTION; CELL METABOLISM; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION; HOMEOSTASIS; HUMAN; LIPID DIET; MITOCHONDRION; NERVE DEGENERATION; NUTRIENT; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION;

EID: 84864960619     PISSN: 16878876     EISSN: 16878884     Source Type: Journal    
DOI: 10.1155/2012/759583     Document Type: Review

References (92)

1. Nunnari J., Suomalainen A., Mitochondria: in sickness and in health Cell 2012 148 6 1145 1159
2. Johnson D. T., Harris R. A., French S., Blair P. V., You J., Bemis K. G., Wang M., Balaban R. S., Tissue heterogeneity of the mammalian mitochondrial proteome American Journal of Physiology 2007 292 2 C689 C697
3. Hock M. B., Kralli A., Transcriptional control of mitochondrial biogenesis and function Annual Review of Physiology 2009 71 177 203
4. Hardie D. G., Signal transduction: how cells sense energy Nature 2011 472 7342 176 177
5. Mihaylova M. M., Shaw R. J., The AMPK signalling pathway coordinates cell growth, autophagy and metabolism Nature Cell Biology 2011 13 9 1016 1023
6. Cant C., Auwerx J., PGC-1, SIRT1 and AMPK, an energy sensing network that controls energy expenditure Current Opinion in Lipidology 2009 20 2 98 105
7. Jeninga E. H., Schoonjans K., Auwerx J., Reversible acetylation of PGC-1: connecting energy sensors and effectors to guarantee metabolic flexibility Oncogene 2010 29 33 4617 4624
8. Aquilano K., Baldelli S., Rotilio G., Ciriolo M. R., trans -Resveratrol inhibits H 2 O 2 -induced adenocarcinoma gastric cells proliferation via inactivation of MEK1/2-ERK1/2-c-Jun signalling axis Biochemical Pharmacology 2009 77 3 337 347
9. Cui X., Reactive oxygen species: the achilles' heel of cancer cells? Antioxidants Redox Signaling 2012 16 11 1212 1214
10. Bustamante J., Czerniczyniec A., Lores-Arnaiz S., Brain nitric oxide synthases and mitochondrial function Frontiers in Bioscience 2007 12 3 1034 1040 (Pubitemid 46846876)
11. Aquilano K., Filomeni G., Baldelli S., Piccirillo S., De Martino A., Rotilio G., Ciriolo M. R., Neuronal nitric oxide synthase protects neuroblastoma cells from oxidative stress mediated by garlic derivatives Journal of Neurochemistry 2007 101 5 1327 1337 (Pubitemid 46718814)
12. Baldelli S., Aquilano K., Rotilio G., Ciriolo M. R., Glutathione and copper, zinc superoxide dismutase are modulated by overexpression of neuronal nitric oxide synthase International Journal of Biochemistry Cell Biology 2008 40 11 2660 2670
13. Aquilano K., Baldelli S., Cardaci S., Rotilio G., Ciriolo M. R., Nitric oxide is the primary mediator of cytotoxicity induced by GSH depletion in neuronal cells Journal of Cell Science 2011 124, part 7 1043 1054
14. Doherty G. H., Nitric oxide in neurodegeneration: potential benefits of non-steroidal anti-inflammatories Neuroscience Bulletin 2011 27 6 366 382
15. Oddi S., Latini L., Viscomi M. T., Bisicchia E., Molinari M., Maccarrone M., Distinct regulation of nNOS and iNOS by CB(2) receptor in remote delayed neurodegeneration Journal of Molecular Medicine 2012 90 4 371 387
16. Aquilano K., Baldelli S., Rotilio G., Ciriolo M. R., Role of nitric oxide synthases in Parkinson's disease: a review on the antioxidant and anti-inflammatory activity of polyphenols Neurochemical Research 2008 33 12 2416 2426
17. Aquilano K., Baldelli S., Ciriolo M. R., Glutathione is a crucial guardian of protein integrity in the brain upon nitric oxide imbalance Communicative Integrative Biology 2011 4 4 477 479
18. Aquilano K., Vigilanza P., Rotilio G., Ciriolo M. R., Mitochondrial damage due to SOD1 deficiency in SH-SY5Y neuroblastoma cells: a rationale for the redundancy of SOD1 The FASEB Journal 2006 20 10 1683 1685
19. Vigilanza P., Aquilano K., Rotilio G., Ciriolo M. R., Transient cytoskeletal alterations after SOD1 depletion in neuroblastoma cells Cellular Molecular Life Sciences 2008 65 6 991 1004
20. Jones A. W., Yao Z., Vicencio J. M., Karkucinska-Wieckowska A., Szabadkai G., PGC-1 family coactivators and cell fate: roles in cancer, neurodegeneration, cardiovascular disease and retrograde mitochondria-nucleus signalling Mitochondrion 2012 12 1 86 99
21. Sibson N. R., Dhankhar A., Mason G. F., Rothman D. L., Behar K. L., Shulman R. G., Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity Proceedings of the National Academy of Sciences of the United States of America 1998 95 1 316 321 (Pubitemid 28103951)
22. Waagepetersen H. S., Sonnewald U., Gegelashvili G., Larsson O. M., Schousboe A., Metabolic distinction between vesicular and cytosolic GABA in cultured GABAergic neurons using 13C magnetic resonance spectroscopy Journal of Neuroscience Research 2001 63 4 347 355 (Pubitemid 32115282)
23. Perry T. L., Haworth J. C., Robinson B. H., Brain amino acid abnormalities in pyruvate carboxylase deficiency Journal of Inherited Metabolic Disease 1985 8 2 63 66 (Pubitemid 15086003)
24. Mayr J. A., Zimmermann F. A., Fauth C., Bergheim C., Meierhofer D., Radmayr D., Zschocke J., Koch J., Sperl W., Lipoic acid synthetase deficiency causes neonatal-onset epilepsy, defective mitochondrial energy metabolism, and glycine elevation American Journal of Human Genetics 2011 89 6 792 797
25. Nisoli E., Tonello C., Cardile A., Cozzi V., Bracale R., Tedesco L., Falcone S., Valerio A., Cantoni O., Clementi E., Moncada S., Carruba M. O., Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS Science 2005 310 5746 314 317 (Pubitemid 41457197)
26. Finley L. W., Lee J., Souza A., Desquiret-Dumas V., Bullock K., Rowe G. C., Procaccio V., Clish C. B., Arany Z., Haigis M. C., Skeletal muscle transcriptional coactivator PGC-1 mediates mitochondrial, but not metabolic, changes during calorie restriction Proceedings of the National Academy of Sciences of the United States of America 2012 109 8 2931 2936
27. Ching L. C., Chen C. Y., Su K. H., Implication of AMP-activated protein kinase in transient receptor potential vanilloid type 1-mediated activation of endothelial nitric oxide synthase. Molecular Medicine. In press
28. Rodgers J. T., Lerin C., Gerhart-Hines Z., Puigserver P., Metabolic adaptations through the PGC-1 and SIRT1 pathways FEBS Letters 2008 582 1 46 53 (Pubitemid 350297246)
29. Puigserver P., Wu Z., Park C. W., Graves R., Wright M., Spiegelman B. M., A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis Cell 1998 92 6 829 839 (Pubitemid 28155321)
30. Handschin C., Spiegelman B. M., Peroxisome proliferator-activated receptor coactivator 1 coactivators, energy homeostasis, and metabolism Endocrine Reviews 2006 27 7 728 735 (Pubitemid 44936056)
31. Cowell R. M., Blake K. R., Russell J. W., Localization of the transcriptional coactivator PGC-1 to GABAergic neurons during maturation of the rat brain The Journal of Comparative Neurology 2007 502 1 1 18 (Pubitemid 46481928)
32. Puigserver P., Spiegelman B. M., Peroxisome proliferator-activated receptor- coactivator 1 (PGC-1 ): transcriptional coactivator and metabolic regulator Endocrine Reviews 2003 24 1 78 90 (Pubitemid 36223280)
33. Kelly D. P., Scarpulla R. C., Transcriptional regulatory circuits controlling mitochondrial biogenesis and function Genes Development 2004 18 4 357 368 (Pubitemid 38316342)
34. D'Errico I., Salvatore L., Murzilli S., Lo Sasso G., Latorre D., Martelli N., Egorova A. V., Polishuck R., Madeyski-Bengtson K., Lelliott C., Vidal-Puig A. J., Seibel P., Villani G., Moschetta A., Peroxisome proliferator-activated receptor- coactivator 1- (PGC1 ) is a metabolic regulator of intestinal epithelial cell fate Proceedings of the National Academy of Sciences of the United States of America 2011 108 16 6603 6608
35. Ciron C., Lengacher S., Dusonchet J., Aebischer P., Schneider B. L., Sustained expression of PGC-1alpha in the rat nigrostriatal system selectively impairs dopaminergic function Human Molecular Genetics 2012 21 8 1861 1876
36. Cui L., Jeong H., Borovecki F., Parkhurst C. N., Tanese N., Krainc D., Transcriptional repression of PGC-1 by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration Cell 2006 127 1 59 69 (Pubitemid 44466642)
37. St-Pierre J., Drori S., Uldry M., Silvaggi J. M., Rhee J., Jger S., Handschin C., Zheng K., Lin J., Yang W., Simon D. K., Bachoo R., Spiegelman B. M., Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators Cell 2006 127 2 397 408 (Pubitemid 44572377)
38. Shin J. H., Ko H. S., Kang H., Lee Y., Lee Y. I., Pletinkova O., Troconso J. C., Dawson V. L., Dawson T. M., PARIS (ZNF746) repression of PGC-1 contributes to neurodegeneration in Parkinson's disease Cell 2011 144 5 689 702
39. Zhao W., Varghese M., Yemul S., Pan Y., Cheng A., Marano P., Hassan S., Vempati P., Chen F., Qian X., Pasinetti G. M., Peroxisome proliferator activator receptor gamma coactivator-1alpha (PGC-1alpha) improves motor performance and survival in a mouse model of amyotrophic lateral sclerosis Molecular Neurodegeneration 2011 6 1 51
40. Martin E., Betuing S., Pags C., Cambon K., Auregan G., Deglon N., Roze E., Caboche J., Mitogen- and stress-activated protein kinase 1-induced neuroprotection in Huntington's disease: role on chromatin remodeling at the PGC-1-alpha promoter Human Molecular Genetics 2011 20 12 2422 2434
41. Finkel T., Cell biology: a clean energy programme Nature 2006 444 7116 151 152 (Pubitemid 44722041)
42. Barger P. M., Browning A. C., Garner A. N., Kelly D. P., p38 mitogen-activated protein kinase activates peroxisome proliferator-activated receptor : a potential role in the cardiac metabolic stress response The Journal of Biological Chemistry 2001 276 48 44495 44501
43. Puigserver P., Adelmant G., Wu Z., Fan M., Xu J., O'Malley B., Spiegelman B. M., Activation of PPAR coactivator-1 through transcription factor docking Science 1999 286 5443 1368 1371
44. Anderson R. M., Barger J. L., Edwards M. G., Braun K. H., O'connor C. E., Prolla T. A., Weindruch R., Dynamic regulation of PGC-1 localization and turnover implicates mitochondrial adaptation in calorie restriction and the stress response Aging Cell 2008 7 1 101 111
45. Cant C., Auwerx J., Caloric restriction, SIRT1 and longevity Trends in Endocrinology Metabolism 2009 20 7 325 331
46. Canto C., Auwerx J., Targeting sirtuin 1 to improve metabolism: all you need is NAD(+)? Pharmacological Reviews 2012 64 1 166 187
47. Wareski P., Vaarmann A., Choubey V., Safiulina D., Liiv J., Kuum M., Kaasik A., PGC-1 and PGC-1 regulate mitochondrial density in neurons The Journal of Biological Chemistry 2009 284 32 21379 21385
48. Brunet A., A CRTCal link between energy and life span Cell Metabolism 2011 13 4 358 360
49. Liu C. T., Brooks G. A., Mild heat stress induces mitochondrial biogenesis in C2C12 myotubes Journal of Applied Physiology 2012 112 3 354 361
50. Hardie D. G., Energy sensing by the AMP-activated protein kinase and its effects on muscle metabolism Proceedings of the Nutrition Society 2011 70 1 92 99
51. Winder W. W., Taylor E. B., Thomson D. M., Role of AMP-activated protein kinase in the molecular adaptation to endurance exercise Medicine and Science in Sports and Exercise 2006 38 11 1945 1949 (Pubitemid 44707799)
52. Crunkhorn S., Dearie F., Mantzoros C., Gami H., Da Silva W. S., Espinoza D., Faucette R., Barry K., Bianco A. C., Patti M. E., Peroxisome proliferator activator receptor coactivator-1 expression is reduced in obesity: potential pathogenic role of saturated fatty acids and p38 mitogen-activated protein kinase activation The Journal of Biological Chemistry 2007 282 21 15439 15450 (Pubitemid 47093279)
53. Wellen K. E., Lu C., Mancuso A., Lemons J. M. S., Ryczko M., Dennis J. W., Rabinowitz J. D., Coller H. A., Thompson C. B., The hexosamine biosynthetic pathway couples growth factor-induced glutamine uptake to glucose metabolism Genes Development 2010 24 24 2784 2799
54. Sparks L. M., Xie H., Koza R. A., Mynatt R., Hulver M. W., Bray G. A., Smith S. R., A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle Diabetes 2005 54 7 1926 1933 (Pubitemid 40911253)
55. Barroso E., Rodrguez-Calvo R., Serrano-Marco L., Astudillo A. M., Balsinde J., Palomer X., Vzquez-Carrera M., The PPAR / activator GW501516 prevents the down-regulation of AMPK caused by a high-fat diet in liver and amplifies the PGC-1 -lipin 1-PPAR pathway leading to increased fatty acid oxidation Endocrinology 2011 152 5 1848 1859
56. Fontana L., Partridge L., Longo V. D., Extending healthy life span-from yeast to humans Science 2010 328 5976 321 326
57. Kiebish M. A., Young D. M., Lehman J. J., Han X., Chronic caloric restriction attenuates a loss of sulfatide content in PGC-1alpha-/- mouse cortex: a potential lipidomic role of PGC-1alpha in neurodegeneration The Journal of Lipid Research 2012 53 2 273 281
58. Piper M. D., Bartke A., Diet and aging Cell Metabolism 2008 8 2 99 104
59. Park H. R., Lee J., Neurogenic contributions made by dietary regulation to hippocampal neurogenesis Annals of the New York Academy of Sciences 2011 1229 1 23 28
60. Finley L. W., Haigis M. C., The coordination of nuclear and mitochondrial communication during aging and calorie restriction Ageing Research Reviews 2009 8 3 173 188
61. Reddy P. H., Reddy T. P., Mitochondria as a therapeutic target for aging and neurodegenerative diseases Current Alzheimer Research 2011 8 4 393 409
62. Hardie D. G., AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function Genes Development 2011 25 18 1895 1908
63. Canto C., Auwerx J., Calorie restriction: is AMPK a key sensor and effector? Physiology 2011 26 4 214 224
64. Guarente L., Mitochondria-a nexus for aging, calorie restriction, and sirtuins? Cell 2008 132 2 171 176 (Pubitemid 351172441)
65. Scarpulla R. C., Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network Biochimica et Biophysica Acta 2011 1813 7 1269 1278
66. Civitarese A. E., Carling S., Heilbronn L. K., Hulver M. H., Ukropcova B., Deutsch W. A., Smith S. R., Ravussin E., Calorie restriction increases muscle mitochondrial biogenesis in healthy humans PLoS Medicine 2007 4 3 e76
67. Lpez-Lluch G., Hunt N., Jones B., Zhu M., Jamieson H., Hilmer S., Cascajo M. V., Allard J., Ingram D. K., Navas P., De Cabo R., Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency Proceedings of the National Academy of Sciences of the United States of America 2006 103 6 1768 1773 (Pubitemid 43228768)
68. Chalkiadaki A., Guarente L., Sirtuins mediate mammalian metabolic responses to nutrient availability Nature Review Endocrinology 2012 8 287 296
69. Wang J., Fivecoat H., Ho L., Pan Y., Ling E., Pasinetti G. M., The role of Sirt1: at the crossroad between promotion of longevity and protection against Alzheimer's disease neuropathology Biochimica et Biophysica Acta 2010 1804 8 1690 1694
70. Srivastava S., Haigis M. C., Role of sirtuins and calorie restriction in neuroprotection: implications in Alzheimer's and Parkinson's diseases Current Pharmaceutical Designno 2011 17 31 3418 3433
71. Wang P., Xu T. Y., Guan Y. F., Tian W. W., Viollet B., Rui Y. C., Zhai Q. W., Su D. F., Miao C. Y., Nicotinamide phosphoribosyltransferase protects against ischemic stroke through SIRT1-dependent adenosine monophosphate- activated kinase pathway Annals of Neurology 2011 69 2 360 374
72. Hu Y., Liu J., Wang J., Liu Q., The controversial links among calorie restriction, SIRT1, and resveratrol Free Radical Biology Medicine 2011 51 2 250 256
73. Tan L., Yu J. T., Guan H. S., Resveratrol exerts pharmacological preconditioning by activating PGC-1 Medical Hypotheses 2008 71 5 664 667
74. Cagnol S., Chambard J. C., ERK and cell death: mechanisms of ERK-induced cell deathapoptosis, autophagy and senescence FEBS Journal 2010 277 1 2 21
75. Liu Y., Yang Y., Ye Y. C., Shi Q. F., Chai K., Tashiro S., Onodera S., Ikejima T., Activation of ERK-p53 and ERK-mediated phosphorylation of Bcl-2 are involved in autophagic cell death induced by the c-met inhibitor SU11274 in human lung cancer A549 cells Journal of Pharmacol Sciencesno 2012 118 4 423 432
76. Fusco S., Ripoli C., Podda M. V., Ranieri S. C., Leone L., Toietta G., McBurney M. W., Schutz G., Riccio A., Grassi C., Galeotti T., Pani G., A role for neuronal cAMP responsive-element binding (CREB)-1 in brain responses to calorie restriction Proceedings of the National Academy of Sciences of the United States of America 2012 109 2 621 626
77. Santin K., da Rocha R. F., Cechetti F., Quincozes-Santos A., de Souza D. F., Nardin P., Rodrigues L., Leite M. C., Moreira J. C., Salbego C. G., Goncalves C. A., Moderate exercise training and chronic caloric restriction modulate redox status in rat hippocampus Brain Research 2011 1421 1 10
78. Cho C. G., Kim H. J., Chung S. W., Jung K. J., Shim K. H., Yu B. P., Yodoi J., Chung H. Y., Modulation of glutathione and thioredoxin systems by calorie restriction during the aging process Experimental Gerontology 2003 38 5 539 548 (Pubitemid 36549040)
79. Chang J. S., Huypens P., Zhang Y., Black C., Kralli A., Gettys T. W., Regulation of NT-PGC-1 subcellular localization and function by protein kinase A-dependent modulation of nuclear export by CRM1 The Journal of Biological Chemistry 2010 285 23 18039 18050
80. Chang J. S., Fernand V., Zhang Y., Shin J., Jun H. J., Joshi Y., Gettys T. W., NT-PGC-1alpha is sufficient to link beta3-adrenergic receptor activation to the transcriptional and physiological components of adaptive thermogenesis The Journal of Biological Chemistry 2012 287 12 9100 9111
81. Aquilano K., Vigilanza P., Baldelli S., Pagliei B., Rotilio G., Ciriolo M. R., Peroxisome proliferator-activated receptor co-activator 1 (PGC-1 ) and sirtuin 1 (SIRT1) reside in mitochondria: possible direct function in mitochondrial biogenesis The Journal of Biological Chemistry 2010 285 28 21590 21599
82. Safdar A., Little J. P., Stokl A. J., Hettinga B. P., Akhtar M., Tarnopolsky M. A., Exercise increases mitochondrial PGC-1 content and promotes nuclear-mitochondrial cross-talk to coordinate mitochondrial biogenesis The Journal of Biological Chemistry 2011 286 12 10605 10617
83. Emanuelsson O., Nielsen H., Brunak S., von Heijne G., Predicting subcellular localization of proteins based on their N-terminal amino acid sequence Journal of Molecular Biology 2000 300 4 1005 1016
84. Mootha V. K., Bunkenborg J., Olsen J. V., Hjerrild M., Wisniewski J. R., Stahl E., Bolouri M. S., Ray H. N., Sihag S., Kamal M., Patterson N., Lander E. S., Mann M., Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria Cell 2003 115 5 629 640 (Pubitemid 37508523)
85. Sen C. K., Glutathione homeostasis in response to exercise training and nutritional supplements Molecular and Cellular Biochemistry 1999 196 1-2 31 42 (Pubitemid 29338776)
86. Merry T. L., McConell G. K., Skeletal muscle glucose uptake during exercise: a focus on reactive oxygen species and nitric oxide signaling IUBMB Life 2009 61 5 479 484
87. Sundar I. K., Caito S., Yao H., Rahman I., Oxidative stress, thiol redox signaling methods in epigenetics Methods in Enzymology 2010 474 213 244
88. Cardaci S., Filomeni G., Rotilio G., Ciriolo M. R., P38 MAPK /p53 signalling axis mediates neuronal apoptosis in response to tetrahydrobiopterin- induced oxidative stress and glucose uptake inhibition: implication for neurodegeneration Biochemical Journal 2010 430 3 439 451
89. Filomeni G., Cardaci S., Da Costa Ferreira A. M., Rotilio G., Ciriolo M. R., Metabolic oxidative stress elicited by the copper(II) complex [Cu(isaepy) 2 ] triggers apoptosis in SH-SY5Y cells through the induction of the AMP-activated protein kinase/p38 MAPK /p53 signalling axis: evidence for a combined use with 3-bromopyruvate in neuroblastoma treatment Biochemical Journal 2011 437 3 443 453
90. Chao J., Yu M. S., Ho Y. S., Wang M., Chang R. C., Dietary oxyresveratrol prevents parkinsonian mimetic 6-hydroxydopamine neurotoxicity Free Radical Biology Medicine 2008 45 7 1019 1026
91. Albani D., Polito L., Batelli S., De Mauro S., Fracasso C., Martelli G., Colombo L., Manzoni C., Salmona M., Caccia S., Negro A., Forloni G., The SIRT1 activator resveratrol protects SK-N-BE cells from oxidative stress and against toxicity caused by -synuclein or amyloid- (1-42) peptide Journal of Neurochemistry 2009 110 5 1445 1456
92. Reddy P. H., Mao P., Manczak M., Mitochondrial structural and functional dynamics in Huntington's disease Brain Research Reviews 2009 61 1 33 48