Regulation of neuron mitochondrial biogenesis and relevance to brain health

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1802, Issue 1, 2010, Pages 228-234

  Onyango, Isaac G ^a   Lu, Jianghua ^a   Rodova, Mariana ^a   Lezi, E ^a   Crafter, Adam B ^a   Swerdlow, Russell H ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Antioxidant; Mitochondrial biogenesis; Mitohormesis; Mitophagy; mtDNA; Neurodegenerative disease; Oxidative stress; PGC1a; Redox

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; ACETYLCARNITINE; ADENYLATE KINASE; ANTIOXIDANT; DIMEBON; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; MAMMALIAN TARGET OF RAPAMYCIN; MITOCHONDRIAL TRANSCRIPTION FACTOR A; MITOCHONDRIAL TRANSCRIPTION FACTOR B; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PIOGLITAZONE; PYRUVIC ACID; REACTIVE OXYGEN METABOLITE; RECOMBINANT HUMAN MITOCHONDRIAL TRANSCRIPTION FACTOR A; RECOMBINANT PROTEIN; RESVERATROL; ROSIGLITAZONE; SIRTUIN 1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

AGING; ALZHEIMER DISEASE; ANTIOXIDANT ACTIVITY; BIOGENESIS; BRAIN MITOCHONDRION; CALORIC RESTRICTION; DEGENERATIVE DISEASE; DRUG MECHANISM; EXERCISE; HUMAN; MITOCHONDRIAL RESPIRATION; NERVE CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW;

AGING; ANIMALS; BRAIN; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; NEURODEGENERATIVE DISEASES; NEURONS; REACTIVE OXYGEN SPECIES;

EID: 71849092123     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2009.07.014     Document Type: Review

References (159)

1. Larsson N., and Clayton D. Molecular genetic aspects of human mitochondrial disorders. Annu. Rev. Genet. 29 (1995) 151-178
2. Chan D. Mitochondrial fusion and fission in mammals. Annu. Rev. Cell Dev. Biol 22 (2006) 79-99
3. Chen H., Chomyn A., and Chan D. Disruption of fusion results in mitochondrial heterogeneity and dysfunction. J. Biol. Chem. 280 (2005) 26185-26192
4. McBride H.M., Neuspiel M., and Wasiak S. Mitochondria: more than just a powerhouse. Curr. Biol. 16 (2006) R551-R560
5. Yu T., Robotham J.L., and Yoon Y. Increased production of reactive oxygen species in hyperglycemic conditions requires dynamic change of mitochondrial morphology. Proc. Natl. Acad. Sci. USA 103 (2006) 2653-2658
6. Kim I., Rodriguez-Enriquez S., and Lemasters J. Selective degradation of mitochondria by mitophagy. Arch. Biochem. Biophys. 462 (2007) 245-253
7. Maiuri M., Zalckvar E., Kimchi A., and Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat. Rev., Mol. Cell Biol. 8 (2007) 741-752
8. Chen H., McCaffery J., and Chan D. Mitochondrial fusion protects against neurodegeneration in the cerebellum. Cell 130 (2007) 548-562
9. Cheng X., Kanki T., Fukuoh A., Ohgaki K., Takeya R., Aoki Y., Hamasaki N., and Kang D. PDIP38 associates with proteins constituting the mitochondrial DNA nucleoid. J. Biochem. 138 (2005) 673-678
10. Twig G., Elorza A., Molina A., Mohamed H., Wikstrom J., Walzer G., Stiles L., Haigh S., Katz S., Las G., Alroy J., Wu M., Py B., Yuan J., Deeney J., Corkey B., and Shirihai O. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 27 (2008) 433-446
11. Zuchner S., Mersiyanova I., and Muglia M.E.A. Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat. Genet. 36 (2004) 449-451
12. Kijima K., Numakura C., and Izumino H.E.A. Mitochondrial GTPase mitofusin 2 mutation in Charcot-Marie-Tooth neuropathy type 2A. Hum. Genet. 116 (2005) 23-27
13. Alexander C., Votruba M., and Pesch U.E.E.A. OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat. Genet. 26 (2000) 211-215
14. Delettre C., Lenaers G., and Griffoin J.E.A. Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat. Genet. 26 (2000) 207-210
15. Poole A., Thomas R., Andrews L., McBride H., Whitworth A., and Pallanck L. The PINK1/Parkin pathway regulates mitochondrial morphology. Proc. Natl. Acad. Sci. USA 105 (2008) 1638-1643
16. Exner N., Treske B., and Paquet D.E.A. Loss-of-function of human PINK1 results in mitochondrial pathology and can be rescued by parkin. J. Neurosci. Res. 27 (2007) 12413-12418
17. Wang X., Su B., Zheng L., Perry G., Smith M., and Zhu X. The role of abnormal mitochondrial dynamics in the pathogenesis of Alzheimer's disease. J. Neurochem. 109 (2009) 153-159
18. Knott A., and Bossy-Wetzel E. Impairing the mitochondrial fission and fusion balance: a new mechanism of neurodegeneration. Ann. N.Y. Acad. Sci. 1147 (2008) 283-292
19. Reddy P., Mao P., and Manczak M. Mitochondrial structural and functional dynamics in Huntington's disease. Brain Res. Rev. 61 (2009) 33-48
20. Wallace D., Singh G., Lott M., Hodge J., Schurr T., Lezza A., Elsas L.N., and Nikoskelainen E. Mitochondrial DNA mutation associated with Leber's hereditary optic neuropathy. Science 242 (1988) 1427-1430
21. Holt I., Harding A., and Morgan-Hughes J. Deletions of muscle mitochondrial DNA in patients with mitochondrial myopathies. Nature 331 (1988) 717-719
22. Clayton D. Replication of animal mitochondrial DNA. Cell 28 (1982) 693-705
23. Rolfe D., and Brown G. Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol. Rev. 77 (1997) 731-758
24. Balaban R., Nemoto S., and Finkel T. Mitochondria, oxidants, and aging. Cell 120 (2005) 483-495
25. Brown G., and Borutaite V. Nitric oxide, mitochondria, and cell death. IUBMB Life 52 (2001) 189-195
26. Navarro A., and Boveris A. The mitochondrial energy transduction system and the aging process. Am. J. Physiol., Cell Physiol. 292 (2007) C670-C686
27. Corral-Debrinski M., Horton T., Lott M., Shoffner J., Beal M., and Wallace D. Mitochondrial DNA deletions in human brain: regional variability and increase with advanced age. Nat. Genet. 2 (1992) 324-329
28. Simon D., Lin M., Zheng L., Liu G., Ahn C., Kim L., Mauck W., Twu F., Beal M., and Johns D. Somatic mitochondrial DNA mutations in cortex and substantia nigra in aging and Parkinson's disease. Neurobiol. Aging 25 (2004) 71-81
29. Lin M., Simon D., Ahn C., Kim L., and Beal M. High aggregate burden of somatic mtDNA point mutations in aging and Alzheimer's disease brain. Hum. Mol. Genet. 11 (2002) 133-145
30. Zhang D., Mott J., Chang S., Stevens M., Mikolajczak P., and Zassenhaus H. Mitochondrial DNA mutations activate programmed cell survival in the mouse heart. Am. J. Physiol., Heart Circ. Physiol. 288 (2005) H2476-H2483
31. Kujoth G., Hiona A., Pugh T., Someya S., Panzer K., Wohlgemuth S., Hofer T., Seo A., Sullivan R., Jobling W., Morrow J., Van Remmen H., Sedivy J., Yamasoba T., Tanokura M., Weindruch R., Leeuwenburgh C., and Prolla T. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 309 (2005) 481-484
32. Trifunovic A., Wredenberg A., Falkenberg M., Spelbrink J., Rovio A., Bruder C., Bohlooly-Y M., Gidlöf S., Oldfors A., Wibom R., Törnell J., Jacobs H., and Larsson N. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429 (2004) 417-423
33. Swerdlow R. Treating neurodegeneration by modifying mitochondria: potential solutions to a "complex" problem. Antioxid. Redox Signal. 9 (2007) 1591-1603
34. Swerdlow R. Mitochondria in cybrids containing mtDNA from persons with mitochondriopathies. J. Neurosci. Res. 85 (2007) 3416-3428
35. Hirai K., Aliev G., Nunomura A., Fujioka H., Russell R., Atwood C., Johnson A., Kress Y., Vinters H., Tabaton M., Shimohama S., Cash A., Siedlak S., Harris P., Jones P., Petersen R., Perry G., and Smith M. Mitochondrial abnormalities in Alzheimer's disease. J. Neurosci. 21 (2001) 3017-3023
36. Barrientos A., Casademont J., Cardellach F., Estivill X., Urbano-arquez A., and Nunes V. Reduced steady-state levels of mitochondrial RNA and increased mitochondrial DNA amount in human brain with aging. Brain Res. Mol. Brain Res. 52 (1997) 284-289
37. Manczak M., Jung Y., Park B., Partovi D., and Reddy P. Timecourse of mitochondrial gene expressions in mice brains: implications for mitochondrial dysfunction, oxidative damage, and cytochrome c in aging. J. Neurochem. 92 (2005) 494-504
38. Diana A., Simic G., Sinforiani E., Orru N., Pichiri G., and Bono G. Mitochondria morphology and DNA content upon sublethal exposure to beta-amyloid(1-42) peptide. Coll. Antropol. 32 (2008) 51-58
39. Liang W., Reiman E., Valla J., Dunckley T., Beach T., Grovr A., Niedzielko T., Schneider L., Mastroeni D., Caselli R., Kukull W., Morris J., Hulette C., Schmechel D., Rogers J., and Stephan D. Alzheimer's disease is associated with reduced expression of energy metabolism genes in posterior cingulate neurons. Proc. Natl. Acad. Sci. USA 105 (2008) 4441-4446
40. de la Monte S., Luong T., Neely T., Robinson D., and Wands J. Mitochondrial DNA damage as a mechanism of cell loss in Alzheimer's disease. Lab. Invest. 80 (2000) 1323-1335
41. Chandrasekaran K., Giordano T., Brady D., Stoll J., Martin J., and Rapoport S. Impairment in mitochondrial cytochrome oxidase gene expression in Alzheimer disease. Brain Res. Mol. Brain Res. 24 (1994) 336-340
42. Liang W., Reiman E., Valla J., Dunckley T., Beach T., Grover A., Niedzielko T., Schneider L., Mastroeni D., Caselli R., Kukull W., Morris J., Hulette C., Schmechel D., Rogers J., and Stephan D. Alzheimer's disease is associated with reduced expression of energy metabolism genes in posterior cingulate neurons. Proc. Natl. Acad. Sci. USA 105 (2008) 4441-4446
43. Cui L., Jeong H., Borovecki F., Parkhurst C., Tanese N., and Krainc D. Transcriptional repression of PGC-1alpha by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration. Cell 127 (2006) 59-69
44. Swerdlow R. The neurodegenerative mitochondriopathies. J. Alzheimer's Dis. (2009) (Electornic publication ahead of print)
45. Nisoli E., Tonello C., Cardile A., Cozzi V., Bracale R., Tedesco L., Falcone S., Valerio A., Cantoni O., Clementi E., Moncada S., and Carruba M. Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310 (2005) 314-317
46. Lopez-Lluch G., Hunt N., Jones B., Zhu M., Jamieson H., Hilmer S., Cascajo M., Allard J., Ingram D., Navas P., and de Cabo R. Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proc. Natl. Acad. Sci. USA 103 (2006) 1768-1773
47. Vellai T. Autophagy genes and ageing. Cell Death Differ. 16 (2009) 94-102
48. Hansen M., Chandra A., Mitic L., Onken B., Driscoll M., and Kenyon C. A role for autophagy in the extension of lifespan by dietary restriction in C. elegans. PLoS Genet. 4 (2008) e24
49. Tapia P. Sublethal mitochondrial stress with an attendant stoichiometric augmentation of reactive oxygen species may precipitate many of the beneficial alterations in cellular physiology produced by caloric restriction, intermittent fasting, exercise and dietary phytonutrients: "Mitohormesis" for health and vitality. Med. Hypotheses 66 (2006) 832-843
50. Gu Y., Wang C., and Cohen A. Effect of IGF-1 on the balance between autophagy of dysfunctional mitochondria and apoptosis. FEBS Lett. (2004) 357-360
51. Calabrese E., and Baldwin L. Hormesis: the dose-response revolution. Annu. Rev. Pharmacol. Toxicol. 43 (2003) 175-197
52. Shang T., Joseph J., Hillard C., and Kalyanaraman B. Death associated protein kinase as a sensor of mitochondrial membrane potential - role of lysosome in mitochondrial toxin induced cell death. J. Biol. Chem. 280 (2005) 34644-34653
53. Radak Z., Chung H., and Goto S. Exercise and hormesis: oxidative stress-related adaptation for successful aging. Biogerontology 6 (2005) 71-75
54. Ji L., Gomez-Cabrera M., and Vina J. Exercise and hormesis: activation of cellular antioxidant signaling pathway. Ann. N.Y. Acad. Sci. 1067 (2006) 425-435
55. Gomez-Cabrera M., Domenech E., Romagnoli M., Arduini A., Borras C., Pallardo F., Sastre J., Viña J., and Dickson D. Oral administration of vitamin C decreases muscle mitochondrial biogenesis and hampers training-induced adaptations in endurance performance. Am. J. Clin. Nutr. 87 (2008) 142-149
56. St-Pierre J., Drori S., Uldry M., Silvaggi J., Rhee J., Jäger S., Handschin C., Zheng K., Lin J., Yang W., Simon D., Bachoo R., and Spiegelman B. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127 (2006) 397-408
57. Baur J., and Sinclair D. Therapeutic potential of resveratrol: the in vivo evidence. Nat. Rev., Drug Discov. 5 (2006) 493-506
58. Howitz K., Bitterman K., Cohen H., Lamming D., Lavu S., Wood J., Zipkin R., Chung P., Kisielewski A., Zhang L., Scherer B., and Sinclair D. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 425 (2003) 191-196
59. Lin S., Defossez P., and Guarente L. Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae. Science 289 (2000) 2126-2128
60. Rogina B., and Helfand S. Sir2 mediates longevity in the fly through a pathway related to calorie restriction. Proc. Natl. Acad. Sci. USA 101 (2004) 15998-16003
61. Booth F.W., and Baldwin K.M. Exercise regulation and integration of multiple systems. In: Rowell L.B., and Shephard J.T. (Eds). Handbook of Physiology (1997), Oxford University Press, New York 1075-1123
62. Holloszy J., and Booth F. Biochemical adaptations to endurance exercise in muscle. Annu. Rev. Physiol. 38 (1976) 273-291
63. Chabi B., Adhihetty P.J., Ljubicic V., and Hood D. How is mitochondrial biogenesis affected in mitochondrial disease. Med. Sci. Sports Exerc. 37 (2005) 2102-2110
64. Semple R., Chatterjee V., and O'Rahilly S. PPAR gamma and human metabolic disease. J. Clin. Invest. Ophthalmol. Vis. Sci. 16 (2006) 581-589
65. Lehrke M., and Lazar M. The many faces of PPARgamma. Cell 123 (2005) 993-999
66. Yki-Jarvinen H. Thiazolidinediones. New Engl. J. Med. 351 (2004) 1106-1118
67. Ghosh S., Patel N., Rahn D., McAllister J., Sadeghi S., Horwitz G., Berry D., Wang K., and Swerdlow R. The thiazolidinedione pioglitazone alters mitochondrial function in human neuronal-like cells. Mol. Pharmacol. 71 (2007) 1695-1702
68. Feinstein D., Spagnolo A., Akar C., Weinberg G., Murphy P., Gavrilyuk V., and Dello Russo C. Receptor-independent actions of PPAR thiazolidinedione agonists: is mitochondrial function the key?. Biochem. Pharmacol. 70 (2005) 177-188
69. Dello Russo C., Gavrilyuk V., Weinberg G., Almeida A., Bolanos J., Palmer J., Pelligrino D., Galea E., and Feinstein D. Peroxisome proliferator-activated receptor gamma thiazolidinedione agonists increase glucose metabolism in astrocytes. J. Biol. Chem. 278 (2003) 5823-5836
70. Kelly L., Vicario P., Thompson G., Caldelore M., Doebber T., Ventre J., Wu M., Meurer R., Forrest M., Conner M., Cascieri M., and Muller D. Peroxisome proliferator-activated receptors gamma and alpha mediate in vivo regulation of uncoupling protein (UCP-1, UCP-2, UCP-3) gene expression. Endocrinology 139 (1998) 4920-4927
71. Shimokawa T., Kato M., Watanabe Y., Hirayama R., Kurosaki E., Shikama H., and Hashimoto S. In vivo effects of pioglitazone on uncoupling protein-2 and -3 mRNA levels in skeletal muscle of hyperglycemic KK mice. Biochem. Biophys. Res. Commun. 251 (1998) 374-378
72. Digby J., Montague C., Sewter C., Sanders L., Wilkison W., O'Rahilly S., and Prins J. Thiazolidinedione exposure increases the expression of uncoupling protein 1 in cultured human preadipocytes. Diabetes 47 (1998) 138-141
73. Strum J., Shehee R., Virley D., Richardson J., Mattie M., Selley P., Ghosh S., Nock C., Saunders A., and Roses A. Rosiglitazone induces mitochondrial biogenesis in mouse brain. J. Alzheimer's Dis. 11 (2007) 45-51
74. Bogacka I., Xie H., Bray G., and Smith S. Pioglitazone induces mitochondrial biogenesis in human subcutaneous adipose tissue in vivo. Diabetes 54 (2005) 1392-1399
75. Heneka M., Sastre M., Dumitrescu-Ozimek L., Hanke A., Dewachter I., Klockgether T., and Van Leuven F. Acute treatment with the PPARgamma agonist pioglitazone and ibuprofen reduces glial inflammation and Abeta1-42 levels in APPV717I transgenic mice. Brain Res. 128 (2005) 1442-1453
76. Watson G., Cholerton B., Reger M., Baker L., Phymate S., Asthana S., Fishel M., Kulstad J., Green P., Cook D., Kahn S., Keeling M., and Craft S. 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 (2005) 950-958
77. Risner M., Saunders A.M., Altman J.F., Ormandy G.C., Craft S., Foley I.M., Zvatau-Hind M.E., Hosford D., and Roses A. Efficacy of rosiglitazone in a genetically defined population with mild-to-moderate Alzheimer's disease. Pharmacogenomics J. 6 (2006) 246-254
78. Landreth G. PPARγ agonists as new therapeutic agents for the treatment of Alzheimer's disease. Exp. Neurol. 199 (2006) 245-248
79. Craft S. Insulin resistance syndrome and Alzheimer disease: pathophysiologic mechanisms and therapeutic implications. Alzheimer Dis. Assoc. Disord. 20 (2006) 298-301
80. Roses A., Saunders A., Huang Y., Strum J., Weisgraber K., and Mahley R. Complex disease-associated pharmacogenetics: drug efficacy, drug safety, and confirmation of a pathogenetic hypothesis (Alzheimer's disease). Pharmacogenomics J. 7 (2007) 10-28
81. Wilson L., Yang Q., Szustakowski J., Gullicksen P., and Halse R. Pyruvate induces mitochondrial biogenesis by a PGC-1 alpha-independent mechanism. Am. J. Physiol., Cell Physiol. 292 (2007) C1599-C1605
82. Hagen T., Liu J., Lykkesfeldt J., Wehr C., Ingersoll R., Vinasky V., Bartholomew J., and Ames B. Feeding acetyl-l-carnitine and lipoic acid to old rats significantly improves metabolic function while decreasing oxidative stress. Proc. Natl. Acad. Sci. USA 99 (2002) 1870-1875
83. Hagen T., Wehr C., and Ames B. Mitochondrial decay in aging. Reversal through supplementation of acetyl-l-carnitine and N-tert-butyl-alpha-phenyl-nitrone. Ann. N.Y. Acad. Sci. 854 (1998) 214-223
84. Nemoto S., Takeda K., Yu Z., Ferrans V., and Finkel T. Role for mitochondrial oxidants as regulators of cellular metabolism. Mol. Cell. Biol. 20 (2000) 7311-7318
85. Rodgers J., Lerin C., Haas W., Gygi S., Spiegelman B., and Puigserver P. Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 434 (2005) 113-118
86. Corton J., Apte U., Anderson S., Limaye P., Yoon L., Latendresse J., Dunn C., Everitt J., Voss K., Swanson C., Kimbrough C., Wong J., Gill S., Chandraratna R., Kwak M., Kensler T., Stulnig T., Steffensen K., Gustafsson J., and Mehendale H. Mimetics of caloric restriction include agonists of lipid-activated nuclear receptors. J. Biol. Chem. 279 (2004) 46204-46212
87. Houten S., and Auwerx J. Turbocharging mitochondria. Cell 119 (2004) 5-7
88. Handschin C., and Spiegelman B. Peroxisome proliferators-activated receptor γ coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr. Rev. 27 (2006) 728-735
89. Fink B., and Kelly D. PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J. Clin. Invest. 116 (2006) 615-622
90. Scarpulla R. Transcriptional activators and coactivators in the nuclear control of mitochondrial function in mammalian cells. Gene 286 (2002) 81-89
91. Kang D., and Hamasaki N. Mitochondrial transcription factor A in the maintenance of mitochondrial DNA: overview of its multiple roles. Ann. N.Y. Acad. Sci. 1042 (2005) 101-108
92. Scarpulla R. Nuclear control of respiratory gene expression in mammalian cells. J. Cell. Biochem. 97 (2006) 673-683
93. Schreiber S., Knutti D., Brogli K., Uhlmann T., and Kralli A. The transcriptional coactivator PGC-1 regulates the expression and activity of the orphan nuclear receptor estrogen-related receptor alpha (ERRalpha). J. Biol. Chem. 278 (2003) 9013-9018
94. Mootha V., Handschin C., Arlow D., Xie X., St J., Pierre S.S., Yang W., Altshuler D., Puigserver P., Patterson N., Willy P., Schulman I., Heyman R., Lander E., and Spiegelman B. Err Aand Gabpa/b specify PGC-1a-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc. Natl. Acad. Sci. USA 101 (2004) 6575-6579
95. St-Pierre J., Drori S., Uldry M., Silvaggi J., Rhee J., Jager S., Hanschin C., Zheng K., Lin J., Yang W., Simon D., Bachoo R., and Spiegelman B. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127 (2006) 397-408
96. Koo S., Satoh H., Herzig S., Lee C., Hedrick S., Kulkarni R., Evans R., Olefsky J., and Montminy M. PGC-1 promotes insulin resistance in liver through PPARα-dependent induction of TRB-3. Nat. Med. 10 (2004) 530-534
97. Knutti D., Kressler K., and Kralli A. Regulation of the transcriptional coactivator PGC-1 via MAPK-sensitive interaction with a corepressor. Proc. Natl. Acad. Sci. USA 98 (2001) 9713-9718
98. Fan M., Rhee J., St-Pierre J., Handschin C., Puigserver P., Lin J., Jaeger S., Erdjument-Bromage H., Tempst P., and Spiegelman B. Suppression of mitochondrial respiration through recruitment of p160 myb binding protein to PGC-1alpha: modulation by p38 MAPK. Genes Dev. 18 (2004) 278-289
99. Feige J., and Auwerx J. Transcriptional coregulators in the control of energy homeostasis. Trends Cell Biol. 17 (2007) 292-301
100. Puigserver P., Rhee J., Lin J., Wu Z., Yoon J., Zhang C., Krauss S., Mootha V., Lowell B., and Spiegelman B. Cytokine stimulation of energy expenditure through p38 MAP kinase activation of PPAR coactivator-1. Mol. Cell 8 (2001) 971-982
101. Herzig S., Long F., Jhala U., Hedrick S., Quinn R., Bauer A., Rudolph D., Schutz G., Yoonk C., Puigserver P., Spiegelman B., and Montminy M. CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature 413 (2001) 179-183
102. Wu Z., Huang X., Feng Y., Handschin C., Feng Y., Gullicksen P., Bare O., Labow M., Spiegelman B., and Stevenson S. Transducer of regulated CREB-binding proteins (TORCs) induce PGC-1 transcription and mitochondrial biogenesis in muscle cells. Proc. Natl. Acad. Sci. USA 103 (2006) 14379-14384
103. Daitoku H., Yamagata K., Matsuzaki H., Hatta M., and Fukamizu A. Regulation of PGC-1 promoter activity by protein kinase B and the forkhead transcription factor FKHR. Diabetes 52 (2003) 642-649
104. Frescas D., Valenti L., and Accili D. Nuclear trapping of the forkhead transcription factor FoxO1 via Sirt-dependent deacetylation promotes expression of glucogenetic genes. J. Biol. Chem. 280 (2005) 20589-20595
105. Nakae J., Oki M., and Cao Y. The FoxO transcription factors and metabolic regulation. FEBS Lett. 582 (2008) 54-67
106. Greer E., and Brunet A. FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene 24 (2005) 7410-7425
107. Kelly D., and Scarpulla R. Transcriptional regulatory circuits controlling mitochondrial biogenesis and function. Genes Dev. 18 (2004) 357-368
108. Scarpulla R. Nuclear activators and coactivators in mammalian mitochondrial biogenesis. Biochim. Biophys. Acta 1576 (2002) 1-14
109. Lin S., Ford E., Haigis M., Liszt G., and Guarente L. Calorie restriction extends yeast life span by lowering the level of NADH. Genes Dev. 18 (2004) 12-16
110. Tanner K., Landry J., Sternglanz R., and Denu J. Silent information regulator 2 family of NAD-dependent histone/protein deacetylases generates a unique product, 1-O-acetyl-ADP-ribose. Proc. Natl. Acad. Sci. USA 97 (2000) 14178-14182
111. Schmidt M., Smith B., Jackson M., and Denu J. Coenzyme specificity of Sir2 protein deacetylases: implications for physiological regulation. J. Biol. Chem. 279 (2004) 40122-40129
112. Landry J., Sutton A., Tafrov S., Heller R., Stebbins J., Pillus L., and Sternglanz R. The silencing protein SIR2 and its homologs are NAD+-dependent protein deacetylases. Proc. Natl. Acad. Sci. USA 97 (2000) 5807-5811
113. Imai S., Armstrong C., Kaeberlein M., and Guarente L. Transcriptional silencing and longevity protein Sir2 is an NAD? Dependent histone deacetylase. Nature 403 (2000) 795-800
114. Lagouge M., Argmann C., Gerhart-Hines Z., Meziane H., Lerin C., Daussin F., Messadeq N., Milne J., Lambert P., Elliott P., Geny B., Laakso M., Puigserver P., and Auwerx J. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 127 (2006) 1109-1122
115. Tanno M., Sakamoto J., Miura T., Shimamoto K., and Horio Y. Nucleocytoplasmic shuttling of the NAD+-dependent histone deacetylase SIRT1. J. Biol. Chem. 282 (2007) 6823-6832
116. Saunders L., and Verdin E. Sirtuins: critical regulators at the crossroads between cancer and aging. Oncogene 26 (2007) 5489-5504
117. Hisahara S., Chiba S., Matsumoto H., Tanno M., Yagi H., Shimohama S., Sato M., and Horio Y. Histone deacetylase SIRT1 modulates neuronal differentiation by its nuclear translocation. Proc. Natl. Acad. Sci. USA 105 (2008) 15599-15604
118. Kim E., Kho J., Kang M., and Um S. Active regulator of SIRT1 cooperates with SIRT1 and facilitates suppression of p53 activity. Mol. Cell 28 (2007) 277-290
119. Araki T., Sasaki Y., and Milbrandt J. Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science 305 (2004) 1010-1013
120. Green K., Steffan J., Martinez-Coria H., Sun X., Schreiber S., Thompson L., and LaFerla F. Nicotinamide restores cognition in Alzheimer's disease transgenic mice via a mechanism involving sirtuin inhibition and selective reduction of Thr231-phosphotau. J. Neurosci. 28 (2008) 11500-11510
121. Langley B., Gensert J., Beal M., and Ratan R. Remodeling chromatin and stress resistance in the central nervous system: histone deacetylase inhibitors as novel and broadly effective neuroprotective agents. Current Drug Targets CNS Neurol. Disord. 4 (2005) 41-50
122. Kolthur-Seetharam U., Dantzer F., McBurney M., de Murcia G., and Sassone-Corsi P. Control of AIF-mediated cell death by the functional interplay of SIRT1 and PARP-1 in response to DNA damage. Cell Cycle 5 (2006) 873-877
123. Pillai J., Isbatan A., Imai S., and Gupta M. Poly(ADP-ribose) polymerase-1-dependent cardiac myocyte cell death during heart failure is mediated by NAD+ depletion and reduced sir2α deacetylase activity. J. Biol. Chem. 280 (2005) 43121-43130
124. Jager S., Handschin C., St-Pierre J., and Spiegelman B. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc. Natl. Acad. Sci. USA 104 (2007) 12017-12022
125. Reznick R., and Shulman G. The role of AMP-activated protein kinase in mitochondrial biogenesis. J. Physiol. 574 (2006) 33-39
126. Hardie D. AMP-activated/SNF1 protein kinases:conserved guardians of cellular energy. Nat. Rev., Mol. Cell Biol. 8 (2007) 774-785
127. Birnbaum M. Activating AMP-activated protein kinase without AMP. Mol. Cell 19 (2005) 289-290
128. Wu H., Kanatous S., Thurmond F., Gallardo T., Isotani E., Bassel-Duby R., and Williams R. Regulation of mitochondrial biogenesis in skeletal muscle by CaMK. Science 296 (2002) 349-352
129. Baur J., Pearson K.J., Price N.L., Jamieson H.A., Lerin C., Kalra A., Prabhu V.V., Allard J.S., Lopez-Lluch G., Lewis K., Pistell P.J., Poosala S., Becker K.G., Boss O., Gwinn D., Wang M., Ramaswamy S., Fishbein K.W., Spencer R.G., Lakatta E.G., Le Couteur D., Shaw R.J., Navas P., Puigserver P., Ingram D.K., de Cabo R., and Sinclair D. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444 (2006) 337-342
130. Zang M., Xu S., Maitland-Toolan K., Zuccollo A., Hou X., Jiang B., Wierzbick I.M., Verbeuren T., and Cohen R. Polyphenols stimulate AMP-activated protein kinase, lower lipids, and inhibit accelerated atherosclerosis in diabetic LDL receptor-deficient mice. Diabetes 55 (2006) 2180-2191
131. Fryer L., Parbu-Patel A., and Carling D. The anti-diabetic drugs rosiglitazone and metformin stimulate AMP-activated protein kinase through distinct signaling pathways. J. Biol. Chem. 277 (2002) 25226-25232
132. LeBrasseur N., Kelly M., Tsao T., Farmer S., Saha A., Ruderman N., and Tomas E. Thiazolidinediones can rapidly activate AMP-activated protein kinase in mammalian tissues. Am. J. Physiol., Endocrinol. Metabol. 291 (2006) E175-E181
133. Saha A., Avilucea P., Ye J., Assifi M., Kraegen E., and Ruderman N. Pioglitazone treatment activates AMP-activated protein kinase in rat liver and adipose tissue in vivo. Biochem. Biophys. Res. Commun. 314 (2004) 580-585
134. Ye J., Dzamko N., Cleasby M., Hegarty B., Furler S., Cooney G., and Kraegen E. Direct demonstration of lipid sequestration as a mechanism by which rosiglitazone prevents fatty-acid-induced insulin resistance in the rat: comparison with metformin. Diabetologia 47 (2004) 1306-1313
135. Zhou G., Myers R., Li Y., Chen Y., Shen X., Fenyk-Melody J., Wu M., Ventre J., Doebber T., Fujii N., Musi N., Hirshman M., Goodyear L., and Moller D. Role of AMP-activated protein kinase in mechanism of metformin action. J. Clin. Invest. 108 (2001) 1167-1174
136. Greer E., Oskoui P., Banko M., Maniar J., Gygi M., Gygi S., and Brunet A. The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J. Biol. Chem. 282 (2007) 30107-30119
137. Schieke S., Phillips D., McCoy Jr. J.P., Aponte A.M., Shen R.F., Balaban R.S., and Finkel T. The mammalian target of rapamycin (mTOR) pathway regulates mitochondrial oxygen consumption and oxidative capacity. J. Biol. Chem. 281 (2006) 27643-27652
138. Schieke S., Phillips D., McCoy Jr. J., Aponte A., Shen R., Balaban R., and Finkel T. The mammalian target of rapamycin (mTOR) pathway regulates mitochondrial oxygen consumption and oxidative capacity. J. Biol. Chem. 281 (2006) 27643-27652
139. Niedernhofer L., and Robbins P. Signaling mechanisms involved in the response to genotoxic stress and regulating lifespan. Int. J. Biochem. Cell Biol. 40 (2008) 176-180
140. Cunningham J., Rodgers J., Arlow D., Vazquez F., Mootha V., and Puigserver P. mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex. Nature 450 (2007) 736-740
141. Dann S., Selvaraj A., and Thomas G. mTOR Complex1-S6K1 signaling: at the crossroads of obesity, diabetes and cancer. Trends Mol. Med. 13 (2007) 252-259
142. Mason S., Rundqvist H., Papandreou I., Duh R., McNulty W., Howlett R., Olfert I., Sundberg C., Denko N., Poellinger L., and Johnson R. HIF-1 in endurance training: suppression of oxidative metabolism. Am. J. Physiol., Regul. Integr. Comp. Physiol. 293 (2007) 2059-2069
143. Gutsaeva D., Carraway M., Suliman H., Demchenko I., Shitara H., Yonekawa H., and Piantadosi C. Transient hypoxia stimulates mitochondrial biogenesis in brain subcortex by a neuronal nitric oxide synthase-dependent mechanism. J. Neurosci. 28 (2008) 2015-2024
144. Rasbach K., and Schnellmann R. Signaling of mitochondrial biogenesis following oxidant injury. J. Biol. Chem. 282 (2007) 2355-2362
145. Lehman J., Barger P., Kovacs A., Saffitz J., Medeiros D., and Kelly D. Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J. Clin. Invest. 106 (2000) 847-856
146. Scarpulla R. Nuclear control of respiratory chain expression in mammalian cells. J. Bioenerg. Biomembranes 29 (1997) 109-119
147. Suliman H., Carraway M., Welty-Wolf K., Whorton A., and Piantadosi C. Lipopolysaccharide stimulates mitochondrial biogenesis via activation of nuclear respiratory factor-1. J. Biol. Chem. 278 (2003) 41510-41518
148. Suliman H., Welty-Wolf K., Carraway M., Tatro L., and Piantados I.C. Lipopolysaccharide induces oxidative cardiac mitochondrial damage and biogenesis. Cardiovasc. Res. 64 (2004) 279-288
149. Lee H., and Wei Y. Mitochondrial biogenesis and mitochondrial DNA maintenance of mammalian cells under oxidative stress. Int. J. Biochem. Cell Biol. 37 (2005) 822-834
150. Ling C., Poulsen P., Carlsson E., Ridderstrale M., Almgren P., Wojtaszewski J., Beck-Nielsen H., Groop L., and Vaag A. Multiple environmental and genetic factors influence skeletal muscle PGC-1a and PGC-1β gene expression in twins. J. Clin. Invest. 114 (2004) 1518-1526
151. de la Monte S., Luong T., Neely T.R., Robinson D., and Wands J. Mitochondrial DNA damage as a mechanism of cell loss in Alzheimer's disease. Lab. Invest. 80 (2000) 1323-1335
152. Reddy P. Mitochondrial oxidative damage in aging and Alzheimer's disease: implications for mitochondrially targeted antioxidant therapeutics. J. Biomed. Biotechnol. 2006 (2006) 31372
153. Lehman J., Barger P.M., Kovacs A., Saffitz J.E., Medeiros D., and Kelly D. Peroxisome proliferator-activated receptor g coactivator-1 promotes cardiac mitochondrial biogenesis. J. Clin. Invest. 106 (2000) 847-856
154. Iyer S., Khan S., Portell F., Thomas R., Borland K., Quigley C., Dunham L., and Bennett Jr. J. Protein-mediated mtDNA transfection ("Protofection®") increases respiration and mitochondrial DNA gene copy numbers and expression in G11778A LHON cybrids. Mitochondrion 9 (2009) 62
155. Iyer S., Thomas R., Portell F., Dunham L., Quigley C., and Bennett Jr. J. Recombinant mitochondrial transcription factor A with N-terminal mitochondrial transduction domain increases respiration and mitochondrial gene expression. Mitochondrion 9 (2009) 196-203
156. Bachurin S., Shevtsova E., Kireeva E., Oxenkrug G., and Sablin S. Mitochondria as a target for neurotoxins and neuroprotective agents. Ann. N.Y. Acad. Sci. 993 (2003) 334-344
157. Bachurin S., Bukatina E., Lermontova N., Tkachenko S., Afanasiev A., Grigoriev V., Grigorieva I., Ivanov Y., Sabli S., and Zefirov N. Antihistamine agent Dimebon as a novel neuroprotector and a cognition enhancer. Ann. N.Y. Acad. Sci. 939 (2001) 425-435
158. Lin M., and Beal M. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443 (2006) 787-795
159. Reddy P., and Beal M. Amyloid beta, mitochondrial dysfunction and synaptic damage: implications for cognitive decline in aging and Alzheimer's disease. Trends Mol. Med. 14 (2008) 45-53