PPARγ regulates the mitochondrial dysfunction in human neural stem cells with tumor necrosis factor alpha

Neuroscience

Volumn 229, Issue , 2013, Pages 118-129

  Chiang, M C ^a   Cheng, Y C ^b   Lin, K H ^c   Yen, C H ^d  

^a FU JEN CATHOLIC UNIVERSITY   (Taiwan)

^b CHANG GUNG UNIVERSITY   (Taiwan)

^c CHINESE CULTURE UNIVERSITY   (Taiwan)

^d MING CHUAN UNIVERSITY   (Taiwan)

Author keywords

HNSCs; Mitochondrial function; PGC1 ; PPAR ; TNF

Indexed keywords

ADENOSINE MONOPHOSPHATE ACTIVATED PROTEIN KINASE; AMYLOID BETA PROTEIN; CASPASE 3; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN KINASE; ROSIGLITAZONE; SIRTUIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOWN REGULATION; HUMAN; HUMAN CELL; NEURAL STEM CELL; NEUROPROTECTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; UPREGULATION;

ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE; CASPASE 3; CELL SURVIVAL; CHROMANS; HUMANS; MITOCHONDRIA; NEURAL STEM CELLS; OXIDATIVE STRESS; PPAR GAMMA; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SIRTUIN 1; THIAZOLIDINEDIONES; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 84870911857     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.11.003     Document Type: Article

References (116)

1. Barth B.M., Gustafson S.J., Kuhn T.B. Neutral sphingomyelinase activation precedes NADPH oxidase-dependent damage in neurons exposed to the proinflammatory cytokine tumor necrosis factor-alpha. J Neurosci Res 2012, 90:229-242.
2. Ben-Hur T., Ben-Menachem O., Furer V., Einstein O., Mizrachi-Kol R., Grigoriadis N. Effects of proinflammatory cytokines on the growth, fate, and motility of multipotential neural precursor cells. Mol Cell Neurosci 2003, 24:623-631.
3. Berger J., Moller D.E. The mechanisms of action of PPARs. Annu Rev Med 2002, 53:409-435.
4. Bergeron R., Ren J.M., Cadman K.S., Moore I.K., Perret P., Pypaert M., Young L.H., Semenkovich C.F., Shulman G.I. Chronic activation of AMP kinase results in NRF-1 activation and mitochondrial biogenesis. Am J Physiol Endocrinol Metab 2001, 281:E1340-E1346.
5. Bernardino L., Agasse F., Silva B., Ferreira R., Grade S., Malva J.O. Tumor necrosis factor-alpha modulates survival, proliferation, and neuronal differentiation in neonatal subventricular zone cell cultures. Stem Cells 2008, 26:2361-2371.
6. Bernardo A., Minghetti L. PPAR-gamma agonists as regulators of microglial activation and brain inflammation. Curr Pharm Des 2006, 12:93-109.
7. Bernardo A., Levi G., Minghetti L. Role of the peroxisome proliferator-activated receptor-gamma (PPAR-gamma) and its natural ligand 15-deoxy-Delta12,14-prostaglandin J2 in the regulation of microglial functions. Eur J Neurosci 2000, 12:2215-2223.
8. Bordet R., Ouk T., Petrault O., Gele P., Gautier S., Laprais M., Deplanque D., Duriez P., Staels B., Fruchart J.C., Bastide M. PPAR: a new pharmacological target for neuroprotection in stroke and neurodegenerative diseases. Biochem Soc Trans 2006, 34:1341-1346.
9. Bordone L., Guarente L. Calorie restriction, SIRT1 and metabolism: understanding longevity. Nat Rev Mol Cell Biol 2005, 6:298-305.
10. Brunmair B., Staniek K., Gras F., Scharf N., Althaym A., Clara R., Roden M., Gnaiger E., Nohl H., Waldhausl W., Furnsinn C. Thiazolidinediones, like metformin, inhibit respiratory complex I: a common mechanism contributing to their antidiabetic actions?. Diabetes 2004, 53:1052-1059.
11. Cacci E., Claasen J.H., Kokaia Z. Microglia-derived tumor necrosis factor-alpha exaggerates death of newborn hippocampal progenitor cells in vitro. J Neurosci Res 2005, 80:789-797.
12. Calingasan N.Y., Ho D.J., Wille E.J., Campagna M.V., Ruan J., Dumont M., Yang L., Shi Q., Gibson G.E., Beal M.F. Influence of mitochondrial enzyme deficiency on adult neurogenesis in mouse models of neurodegenerative diseases. Neuroscience 2008, 153:986-996.
13. Canto C., Gerhart-Hines Z., Feige J.N., Lagouge M., Noriega L., Milne J.C., Elliott P.J., Puigserver P., Auwerx J. AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 2009, 458:1056-1060.
14. Chaturvedi R.K., Beal M.F. PPAR: a therapeutic target in Parkinson's disease. J Neurochem 2008, 106:506-518.
15. Chen S.D., Lin T.K., Yang D.I., Lee S.Y., Shaw F.Z., Liou C.W., Chuang Y.C. Protective effects of peroxisome proliferator-activated receptors gamma coactivator-1alpha against neuronal cell death in the hippocampal CA1 subfield after transient global ischemia. J Neurosci Res 2010, 88:605-613.
16. Chiang M.C., Chern Y., Juo C.G. The dysfunction of hepatic transcriptional factors in mice with Huntington's Disease. Biochim Biophys Acta 2011, 1812:1111-1120.
17. Chiang M.C., Chern Y., Huang R.N. PPARgamma rescue of the mitochondrial dysfunction in Huntington's disease. Neurobiol Dis 2012, 45:322-328.
18. Chiang M.C., Lin H., Cheng Y.C., Yen C.H., Huang R.N., Lin K.H. Beta-adrenoceptor pathway enhances mitochondrial function in human neural stem cells via rotary cell culture system. J Neurosci Methods 2012, 207:130-136.
19. Chung S., Yao H., Caito S., Hwang J.W., Arunachalam G., Rahman I. Regulation of SIRT1 in cellular functions: role of polyphenols. Arch Biochem Biophys 2010, 501:79-90.
20. Chung E.Y., Kim B.H., Hong J.T., Lee C.K., Ahn B., Nam S.Y., Han S.B., Kim Y. Resveratrol down-regulates interferon-gamma-inducible inflammatory genes in macrophages: molecular mechanism via decreased STAT-1 activation. J Nutr Biochem 2011, 22:902-909.
21. Cimini A., Benedetti E., Cristiano L., Sebastiani P., D'Amico M.A., D'Angelo B., Di Loreto S. Expression of peroxisome proliferator-activated receptors (PPARs) and retinoic acid receptors (RXRs) in rat cortical neurons. Neuroscience 2005, 130:325-337.
22. Combs C.K., Johnson D.E., Karlo J.C., Cannady S.B., Landreth G.E. Inflammatory mechanisms in Alzheimer's disease: inhibition of beta-amyloid-stimulated proinflammatory responses and neurotoxicity by PPARgamma agonists. J Neurosci 2000, 20:558-567.
23. Cristiano L., Bernardo A., Ceru M.P. Peroxisome proliferator-activated receptors (PPARs) and peroxisomes in rat cortical and cerebellar astrocytes. J Neurocytol 2001, 30:671-683.
24. Csiszar A., Labinskyy N., Podlutsky A., Kaminski P.M., Wolin M.S., Zhang C., Mukhopadhyay P., Pacher P., Hu F., de Cabo R., Ballabh P., Ungvari Z. Vasoprotective effects of resveratrol and SIRT1: attenuation of cigarette smoke-induced oxidative stress and proinflammatory phenotypic alterations. Am J Physiol Heart Circ Physiol 2008, 294:H2721-H2735.
25. Cullingford T.E., Bhakoo K., Peuchen S., Dolphin C.T., Patel R., Clark J.B. Distribution of mRNAs encoding the peroxisome proliferator-activated receptor alpha, beta, and gamma and the retinoid X receptor alpha, beta, and gamma in rat central nervous system. J Neurochem 1998, 70:1366-1375.
26. Drew P.D., Chavis J.A. The cyclopentone prostaglandin 15-deoxy-Delta(12,14) prostaglandin J2 represses nitric oxide, TNF-alpha, and IL-12 production by microglial cells. J Neuroimmunol 2001, 115:28-35.
27. Ekdahl C.T., Claasen J.H., Bonde S., Kokaia Z., Lindvall O. Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci U S A 2003, 100:13632-13637.
28. Feinstein D.L. Therapeutic potential of peroxisome proliferator-activated receptor agonists for neurological disease. Diabetes Technol Ther 2003, 5:67-73.
29. Fuenzalida K., Quintanilla R., Ramos P., Piderit D., Fuentealba R.A., Martinez G., Inestrosa N.C., Bronfman M. 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 2007, 282:37006-37015.
30. Gao Z., He Q., Peng B., Chiao P.J., Ye J. Regulation of nuclear translocation of HDAC3 by IkappaBalpha is required for tumor necrosis factor inhibition of peroxisome proliferator-activated receptor gamma function. J Biol Chem 2006, 281:4540-4547.
31. Gerhart-Hines Z., Rodgers J.T., Bare O., Lerin C., Kim S.H., Mostoslavsky R., Alt F.W., Wu Z., Puigserver P. Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1alpha. EMBO J 2007, 26:1913-1923.
32. Giri S., Nath N., Smith B., Viollet B., Singh A.K., Singh I. 5-Aminoimidazole-4-carboxamide-1-beta-4-ribofuranoside inhibits proinflammatory response in glial cells: a possible role of AMP-activated protein kinase. J Neurosci 2004, 24:479-487.
33. Greig N.H., Mattson M.P., Perry T., Chan S.L., Giordano T., Sambamurti K., Rogers J.T., Ovadia H., Lahiri D.K. New therapeutic strategies and drug candidates for neurodegenerative diseases: p53 and TNF-alpha inhibitors, and GLP-1 receptor agonists. Ann N Y Acad Sci 2004, 1035:290-315.
34. Hallenbeck J.M. The many faces of tumor necrosis factor in stroke. Nat Med 2002, 8:1363-1368.
35. Hanisch U.K. Microglia as a source and target of cytokines. Glia 2002, 40:140-155.
36. Hardie D.G. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 2007, 8:774-785.
37. Heneka M.T., O'Banion M.K. Inflammatory processes in Alzheimer's disease. J Neuroimmunol 2007, 184:69-91.
38. Heneka M.T., Klockgether T., Feinstein D.L. Peroxisome proliferator-activated receptor-gamma ligands reduce neuronal inducible nitric oxide synthase expression and cell death in vivo. J Neurosci 2000, 20:6862-6867.
39. Hou X., Xu S., Maitland-Toolan K.A., Sato K., Jiang B., Ido Y., Lan F., Walsh K., Wierzbicki M., Verbeuren T.J., Cohen R.A., Zang M. SIRT1 regulates hepatocyte lipid metabolism through activating AMP-activated protein kinase. J Biol Chem 2008, 283:20015-20026.
40. Howitz K.T., Bitterman K.J., Cohen H.Y., Lamming D.W., Lavu S., Wood J.G., Zipkin R.E., Chung P., Kisielewski A., Zhang L.L., Scherer B., Sinclair D.A. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 2003, 425:191-196.
41. Imamura K., Hishikawa N., Sawada M., Nagatsu T., Yoshida M., Hashizume Y. Distribution of major histocompatibility complex class II-positive microglia and cytokine profile of Parkinson's disease brains. Acta Neuropathol 2003, 106:518-526.
42. Inestrosa N.C., Godoy J.A., Quintanilla R.A., Koenig C.S., Bronfman M. Peroxisome proliferator-activated receptor gamma is expressed in hippocampal neurons and its activation prevents beta-amyloid neurodegeneration: role of Wnt signaling. Exp Cell Res 2005, 304:91-104.
43. Iosif R.E., Ekdahl C.T., Ahlenius H., Pronk C.J., Bonde S., Kokaia Z., Jacobsen S.E., Lindvall O. Tumor necrosis factor receptor 1 is a negative regulator of progenitor proliferation in adult hippocampal neurogenesis. J Neurosci 2006, 26:9703-9712.
44. Iosif R.E., Ahlenius H., Ekdahl C.T., Darsalia V., Thored P., Jovinge S., Kokaia Z., Lindvall O. Suppression of stroke-induced progenitor proliferation in adult subventricular zone by tumor necrosis factor receptor 1. J Cereb Blood Flow Metab 2008, 28:1574-1587.
45. Jager S., Handschin C., St-Pierre J., Spiegelman B.M. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc Natl Acad Sci U S A 2007, 104:12017-12022.
46. Jiang C., Ting A.T., Seed B. PPAR-gamma agonists inhibit production of monocyte inflammatory cytokines. Nature 1998, 391:82-86.
47. Kalaria R.N. Microglia and Alzheimer's disease. Curr Opin Hematol 1999, 6:15-24.
48. Kersten S., Desvergne B., Wahli W. Roles of PPARs in health and disease. Nature 2000, 405:421-424.
49. Kielian T., Drew P.D. Effects of peroxisome proliferator-activated receptor-gamma agonists on central nervous system inflammation. J Neurosci Res 2003, 71:315-325.
50. Kirby D.M., Rennie K.J., Smulders-Srinivasan T.K., Acin-Perez R., Whittington M., Enriquez J.A., Trevelyan A.J., Turnbull D.M., Lightowlers R.N. Transmitochondrial embryonic stem cells containing pathogenic mtDNA mutations are compromised in neuronal differentiation. Cell Prolif 2009, 42:413-424.
51. Knobloch J., Sibbing B., Jungck D., Lin Y., Urban K., Stoelben E., Strauch J., Koch A. Resveratrol impairs the release of steroid-resistant inflammatory cytokines from human airway smooth muscle cells in chronic obstructive pulmonary disease. J Pharmacol Exp Ther 2010, 335:788-798.
52. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
53. Lan F., Cacicedo J.M., Ruderman N., Ido Y. SIRT1 modulation of the acetylation status, cytosolic localization, and activity of LKB1. Possible role in AMP-activated protein kinase activation. J Biol Chem 2008, 283:27628-27635.
54. Landreth G.E., Heneka M.T. Anti-inflammatory actions of peroxisome proliferator-activated receptor gamma agonists in Alzheimer's disease. Neurobiol Aging 2001, 22:937-944.
55. LeBrasseur N.K., Kelly M., Tsao T.S., Farmer S.R., Saha A.K., Ruderman N.B., Tomas E. Thiazolidinediones can rapidly activate AMP-activated protein kinase in mammalian tissues. Am J Physiol Endocrinol Metab 2006, 291:E175-E181.
56. Lee J.H., Song M.Y., Song E.K., Kim E.K., Moon W.S., Han M.K., Park J.W., Kwon K.B., Park B.H. Overexpression of SIRT1 protects pancreatic beta-cells against cytokine toxicity by suppressing the nuclear factor-kappaB signaling pathway. Diabetes 2009, 58:344-351.
57. Li J., Zeng Z., Viollet B., Ronnett G.V., McCullough L.D. Neuroprotective effects of adenosine monophosphate-activated protein kinase inhibition and gene deletion in stroke. Stroke 2007, 38:2992-2999.
58. Liu B., Hong J.S. Role of microglia in inflammation-mediated neurodegenerative diseases: mechanisms and strategies for therapeutic intervention. J Pharmacol Exp Ther 2003, 304:1-7.
59. Liu Y.P., Lin H.I., Tzeng S.F. Tumor necrosis factor-alpha and interleukin-18 modulate neuronal cell fate in embryonic neural progenitor culture. Brain Res 2005, 1054:152-158.
60. Locksley R.M., Killeen N., Lenardo M.J. The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 2001, 104:487-501.
61. Luo Y., Yin W., Signore A.P., Zhang F., Hong Z., Wang S., Graham S.H., Chen J. Neuroprotection against focal ischemic brain injury by the peroxisome proliferator-activated receptor-gamma agonist rosiglitazone. J Neurochem 2006, 97:435-448.
62. Marmolino D., Manto M., Acquaviva F., Vergara P., Ravella A., Monticelli A., Pandolfo M. PGC-1alpha down-regulation affects the antioxidant response in Friedreich's ataxia. PLoS ONE 2010, 5:e10025.
63. McGeer P.L., Schulzer M., McGeer E.G. Arthritis and anti-inflammatory agents as possible protective factors for Alzheimer's disease: a review of 17 epidemiologic studies. Neurology 1996, 47:425-432.
64. Monje M.L., Toda H., Palmer T.D. Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003, 302:1760-1765.
65. Moreno S., Farioli-Vecchioli S., Ceru M.P. Immunolocalization of peroxisome proliferator-activated receptors and retinoid X receptors in the adult rat CNS. Neuroscience 2004, 123:131-145.
66. Muppidi J.R., Tschopp J., Siegel R.M. Life and death decisions: secondary complexes and lipid rafts in TNF receptor family signal transduction. Immunity 2004, 21:461-465.
67. Nguyen M.D., Julien J.P., Rivest S. Innate immunity: the missing link in neuroprotection and neurodegeneration?. Nat Rev Neurosci 2002, 3:216-227.
68. Onyango I.G., Lu J., Rodova M., Lezi E., Crafter A.B., Swerdlow R.H. Regulation of neuron mitochondrial biogenesis and relevance to brain health. Biochim Biophys Acta 2010, 1802:228-234.
69. Papa S., Petruzzella V., Scacco S., Vergari R., Panelli D., Tamborra R., Corsi P., Picciariello M., Lambo R., Bertini E., Santorelli F.M. Respiratory complex I in brain development and genetic disease. Neurochem Res 2004, 29:547-560.
70. Peng H., Whitney N., Wu Y., Tian C., Dou H., Zhou Y., Zheng J. HIV-1-infected and/or immune-activated macrophage-secreted TNF-alpha affects human fetal cortical neural progenitor cell proliferation and differentiation. Glia 2008, 56:903-916.
71. Pfluger P.T., Herranz D., Velasco-Miguel S., Serrano M., Tschop M.H. Sirt1 protects against high-fat diet-induced metabolic damage. Proc Natl Acad Sci U S A 2008, 105:9793-9798.
72. Puigserver P., Spiegelman B.M. Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr Rev 2003, 24:78-90.
73. Quintanilla R.A., Jin Y.N., Fuenzalida K., Bronfman M., Johnson G.V. 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 2008, 283:25628-25637.
74. Rajendrasozhan S., Yang S.R., Kinnula V.L., Rahman I. SIRT1, an antiinflammatory and antiaging protein, is decreased in lungs of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2008, 177:861-870.
75. Reznick R.M., Shulman G.I. The role of AMP-activated protein kinase in mitochondrial biogenesis. J Physiol 2006, 574:33-39.
76. Richter E.A., Ruderman N.B. AMPK and the biochemistry of exercise: implications for human health and disease. Biochem J 2009, 418:261-275.
77. Ricote M., Li A.C., Willson T.M., Kelly C.J., Glass C.K. The peroxisome proliferator-activated receptor-gamma is a negative regulator of macrophage activation. Nature 1998, 391:79-82.
78. Rodgers J.T., Lerin C., Haas W., Gygi S.P., Spiegelman B.M., Puigserver P. Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 2005, 434:113-118.
79. Rodgers J.T., Lerin C., Gerhart-Hines Z., Puigserver P. Metabolic adaptations through the PGC-1 alpha and SIRT1 pathways. FEBS Lett 2008, 582:46-53.
80. Rosen E.D., Spiegelman B.M. PPARgamma: a nuclear regulator of metabolism, differentiation, and cell growth. J Biol Chem 2001, 276:37731-37734.
81. Ruan H., Hacohen N., Golub T.R., Van Parijs L., Lodish H.F. Tumor necrosis factor-alpha suppresses adipocyte-specific genes and activates expression of preadipocyte genes in 3T3-L1 adipocytes: nuclear factor-kappaB activation by TNF-alpha is obligatory. Diabetes 2002, 51:1319-1336.
82. Ruderman N.B., Xu X.J., Nelson L., Cacicedo J.M., Saha A.K., Lan F., Ido Y. AMPK and SIRT1: a long-standing partnership?. Am J Physiol Endocrinol Metab 2010, 298:E751-E760.
83. Saha A.K., Avilucea P.R., Ye J.M., Assifi M.M., Kraegen E.W., Ruderman N.B. Pioglitazone treatment activates AMP-activated protein kinase in rat liver and adipose tissue in vivo. Biochem Biophys Res Commun 2004, 314:580-585.
84. Samavati L., Lee I., Mathes I., Lottspeich F., Huttemann M. Tumor necrosis factor alpha inhibits oxidative phosphorylation through tyrosine phosphorylation at subunit I of cytochrome c oxidase. J Biol Chem 2008, 283:21134-21144.
85. Schug T.T., Xu Q., Gao H., Peres-da-Silva A., Draper D.W., Fessler M.B., Purushotham A., Li X. Myeloid deletion of SIRT1 induces inflammatory signaling in response to environmental stress. Mol Cell Biol 2010, 30:4712-4721.
86. Schwab C., Klegeris A., McGeer P.L. Inflammation in transgenic mouse models of neurodegenerative disorders. Biochim Biophys Acta 2010, 1802:889-902.
87. Selkoe D.J. Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 2001, 81:741-766.
88. Shen Z., Ajmo J.M., Rogers C.Q., Liang X., Le L., Murr M.M., Peng Y., You M. Role of SIRT1 in regulation of LPS- or two ethanol metabolites-induced TNF-alpha production in cultured macrophage cell lines. Am J Physiol Gastrointest Liver Physiol 2009, 296:G1047-G1053.
89. Sheng W.S., Hu S., Ni H.T., Rowen T.N., Lokensgard J.R., Peterson P.K. TNF-alpha-induced chemokine production and apoptosis in human neural precursor cells. J Leukoc Biol 2005, 78:1233-1241.
90. Sparkman N.L., Johnson R.W. Neuroinflammation associated with aging sensitizes the brain to the effects of infection or stress. NeuroImmunoModulation 2008, 15:323-330.
91. Spiegelman B.M. PPAR-gamma: adipogenic regulator and thiazolidinedione receptor. Diabetes 1998, 47:507-514.
92. Stadler J., Bentz B.G., Harbrecht B.G., Di Silvio M., Curran R.D., Billiar T.R., Hoffman R.A., Simmons R.L. Tumor necrosis factor alpha inhibits hepatocyte mitochondrial respiration. Ann Surg 1992, 216:539-546.
93. St-Pierre J., Drori S., Uldry M., Silvaggi J.M., Rhee J., Jager 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, 127:397-408.
94. Sundararajan S., Jiang Q., Heneka M., Landreth G. PPARgamma as a therapeutic target in central nervous system diseases. Neurochem Int 2006, 49:136-144.
95. Turrin N.P., Rivest S. Tumor necrosis factor alpha but not interleukin 1 beta mediates neuroprotection in response to acute nitric oxide excitotoxicity. J Neurosci 2006, 26:143-151.
96. Valle I., Alvarez-Barrientos A., Arza E., Lamas S., Monsalve M. PGC-1alpha regulates the mitochondrial antioxidant defense system in vascular endothelial cells. Cardiovasc Res 2005, 66:562-573.
97. Varfolomeev E.E., Ashkenazi A. Tumor necrosis factor: an apoptosis JuNKie?. Cell 2004, 116:491-497.
98. Vila M., Przedborski S. Targeting programmed cell death in neurodegenerative diseases. Nat Rev Neurosci 2003, 4:365-375.
99. Voloboueva L.A., Giffard R.G. Inflammation, mitochondria, and the inhibition of adult neurogenesis. J Neurosci Res 2011, 89:1989-1996.
100. Voloboueva L.A., Lee S.W., Emery J.F., Palmer T.D., Giffard R.G. Mitochondrial protection attenuates inflammation-induced impairment of neurogenesis in vitro and in vivo. J Neurosci 2010, 30:12242-12251.
101. Wahner A.D., Bronstein J.M., Bordelon Y.M., Ritz B. Nonsteroidal anti-inflammatory drugs may protect against Parkinson disease. Neurology 2007, 69:1836-1842.
102. Wajant H., Pfizenmaier K., Scheurich P. Tumor necrosis factor signaling. Cell Death Differ 2003, 10:45-65.
103. Watson G.S., Craft S. Insulin resistance, inflammation, and cognition in Alzheimer's Disease: lessons for multiple sclerosis. J Neurol Sci 2006, 245:21-33.
104. Wong G., Goldshmit Y., Turnley A.M. Interferon-gamma but not TNF alpha promotes neuronal differentiation and neurite outgrowth of murine adult neural stem cells. Exp Neurol 2004, 187:171-177.
105. Wu Z., Puigserver P., Andersson U., Zhang C., Adelmant G., Mootha V., Troy A., Cinti S., Lowell B., Scarpulla R.C., Spiegelman B.M. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 1999, 98:115-124.
106. Yang S.R., Wright J., Bauter M., Seweryniak K., Kode A., Rahman I. Sirtuin regulates cigarette smoke-induced proinflammatory mediator release via RelA/p65 NF-kappaB in macrophages in vitro and in rat lungs in vivo: implications for chronic inflammation and aging. Am J Physiol Lung Cell Mol Physiol 2007, 292:L567-L576.
107. Yang Z., Kahn B.B., Shi H., Xue B.Z. Macrophage alpha1 AMP-activated protein kinase (alpha1AMPK) antagonizes fatty acid-induced inflammation through SIRT1. J Biol Chem 2010, 285:19051-19059.
108. Yeung F., Hoberg J.E., Ramsey C.S., Keller M.D., Jones D.R., Frye R.A., Mayo M.W. Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J 2004, 23:2369-2380.
109. Yoshizaki T., Milne J.C., Imamura T., Schenk S., Sonoda N., Babendure J.L., Lu J.C., Smith J.J., Jirousek M.R., Olefsky J.M. SIRT1 exerts anti-inflammatory effects and improves insulin sensitivity in adipocytes. Mol Cell Biol 2009, 29:1363-1374.
110. Yu L., Yang S.J. AMP-activated protein kinase mediates activity-dependent regulation of peroxisome proliferator-activated receptor gamma coactivator-1alpha and nuclear respiratory factor 1 expression in rat visual cortical neurons. Neuroscience 2010, 169:23-38.
111. Zell R., Geck P., Werdan K., Boekstegers P. TNF-alpha and IL-1 alpha inhibit both pyruvate dehydrogenase activity and mitochondrial function in cardiomyocytes: evidence for primary impairment of mitochondrial function. Mol Cell Biochem 1997, 177:61-67.
112. Zhang B., Berger J., Hu E., Szalkowski D., White-Carrington S., Spiegelman B.M., Moller D.E. Negative regulation of peroxisome proliferator-activated receptor-gamma gene expression contributes to the antiadipogenic effects of tumor necrosis factor-alpha. Mol Endocrinol 1996, 10:1457-1466.
113. Zhao Y., Patzer A., Herdegen T., Gohlke P., Culman J. Activation of cerebral peroxisome proliferator-activated receptors gamma promotes neuroprotection by attenuation of neuronal cyclooxygenase-2 overexpression after focal cerebral ischemia in rats. FASEB J 2006, 20:1162-1175.
114. Zhu L., Wang Q., Zhang L., Fang Z., Zhao F., Lv Z., Gu Z., Zhang J., Wang J., Zen K., Xiang Y., Wang D., Zhang C.Y. Hypoxia induces PGC-1alpha expression and mitochondrial biogenesis in the myocardium of TOF patients. Cell Res 2010, 20:676-687.
115. Zingarelli B., Sheehan M., Hake P.W., O'Connor M., Denenberg A., Cook J.A. Peroxisome proliferator activator receptor-gamma ligands, 15-deoxy-Delta(12,14)-prostaglandin J2 and ciglitazone, reduce systemic inflammation in polymicrobial sepsis by modulation of signal transduction pathways. J Immunol 2003, 171:6827-6837.
116. Zong H., Ren J.M., Young L.H., Pypaert M., Mu J., Birnbaum M.J., Shulman G.I. AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc Natl Acad Sci U S A 2002, 99:15983-15987.