Green Tea Polyphenols Stimulate Mitochondrial Biogenesis and Improve Renal Function after Chronic Cyclosporin A Treatment in Rats

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Rehman, Hasibur ^a,e   Krishnasamy, Yasodha ^a   Haque, Khujista ^a   Thurman, Ronald G ^c   Lemasters, John J ^a,b   Schnellmann, Rick G ^a,b,d   Zhong, Zhi ^a,c  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d RALPH H JOHNSON VA MEDICAL CENTER   (United States)

^e UNIVERSITY OF TABUK   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

CATECHIN; CELL NUCLEUS DNA; CREATININE; CYCLOSPORIN A; CYTOCHROME C OXIDASE; EPICATECHIN; EPICATECHIN GALLATE; EPIGALLOCATECHIN; EPIGALLOCATECHIN GALLATE; GALLOCATECHIN; GREEN TEA EXTRACT; MESSENGER RNA; MITOCHONDRIAL DNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; POLYPHENOL; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; ATP SYNTHASE BETA SUBUNIT, RAT; CYCLOSPORIN; DNA BINDING PROTEIN; MITOCHONDRIAL PROTEIN; PPARGC1A PROTEIN, RAT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TEA; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOGENESIS; CELL VACUOLE; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DNA REPLICATION; DNA TRANSCRIPTION; DRUG MECHANISM; FOOD COMPOSITION; GENE DOSAGE; KIDNEY CALCIFICATION; KIDNEY FIBROSIS; KIDNEY FUNCTION; KIDNEY INJURY; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE EPITHELIUM; MALE; MITOCHONDRIAL RESPIRATION; NEPHROTOXICITY; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OXIDATIVE PHOSPHORYLATION; RAT; TRANSCRIPTION REGULATION; ANIMAL; CHEMISTRY; DIET; DRUG EFFECTS; GENETICS; KIDNEY; KIDNEY DISEASE; KIDNEY FUNCTION TEST; METABOLISM; MITOCHONDRIAL DYNAMICS; MITOCHONDRION; PATHOLOGY; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT; TEA;

CAMELLIA; RATTUS;

ANIMALS; CYCLOSPORINE; DIET; DNA, MITOCHONDRIAL; DNA-BINDING PROTEINS; ELECTRON TRANSPORT COMPLEX I; GENE DOSAGE; KIDNEY; KIDNEY DISEASES; KIDNEY FUNCTION TESTS; MALE; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; MITOCHONDRIAL TURNOVER; OXIDATIVE PHOSPHORYLATION; POLYPHENOLS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; TEA; TRANSCRIPTION FACTORS;

EID: 84878665072     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065029     Document Type: Article

References (97)

1. Borel JF, Feurer C, Gubler HU, Stahelin H, (1976) Biological effects of cyclosporin A: a new antilymphocytic agent. Agents Actions 6: 468-475.
2. Halloran PF, (1996) Molecular mechanisms of new immunosuppressants. Clin Transplant 10: 118-123.
3. Margreiter R, Huber C, Spielberger M, Konig P, (1983) Cyclosporine in the treatment of acute cadaveric kidney graft rejection refractory to high-dose methylprednisolone. Transplantation 36: 203-204.
4. Sibley RK, Rynasiewicz J, Ferguson RM, Fryd D, Sutherland DE, et al. (1983) Morphology of cyclosporine nephrotoxicity and acute rejection in patients immunosuppressed with cyclosporine and prednisone. Surgery 94: 225-234.
5. Naesens M, Kuypers DR, Sarwal M, (2009) Calcineurin inhibitor nephrotoxicity. Clin J Am Soc Nephrol 4: 481-508 4/2/481 [pii];10.2215/CJN.04800908 [doi].
6. Farthing MJG, Clark ML, (1981) Nature of the toxicity of cyclosporin A in the rat. Biochem Pharmacol 24: 3311-3316.
7. Tedesco D, Haragsim L, (2012) Cyclosporine: a review. J Transplant 2012: 230386 10.1155/2012/230386 [doi].
8. Williams D, Haragsim L, (2006) Calcineurin nephrotoxicity. Adv Chronic Kidney Dis 13: 47-55 S1548-5595(05)00202-8 [pii];10.1053/j.ackd.2005.11.001 [doi].
9. Textor SC, Burnett JC, Romero JC, Canzanello VJ, Taler SJ, et al. (1995) Urinary endothelin and renal vasoconstriction with cyclosporine or FK506 after liver transplantation. Kidney Int 47: 1426-1433.
10. Barros EJG, Boim MA, Ajzen H, Ramos OL, Schor N, (1987) Glomerular hemodynamics and hormonal participation in cyclosporine nephrotoxicity. Kidney Int 32: 19-25.
11. Zhong Z, Connor HD, Yin M, Moss N, Mason RP, Bunzendahl H, et al. (1999) Dietary glycine and renal denervation prevents cyclosporin A-induced hydroxyl radical production in rat kidney. Mol Pharmacol 56: 455-463.
12. Zhong Z, Arteel GE, Connor H, Yin M, Frankenberg Mv, et al. (1998) Cyclosporin A increases hypoxia and free radical production in the rat kidney: prevention by dietary glycine. Am J Physiol 275: F595-F604.
13. Diederich D, Skopec J, Diederich A, Dai FX, (1994) Cyclosporine produces endothelial dysfunction by increased production of superoxide. Hypertension 23: 957-961.
14. Lim SW, Li C, Ahn KO, Kim J, Moon IS, et al. (2005) Cyclosporine-induced renal injury induces toll-like receptor and maturation of dendritic cells. Transplantation 80: 691-699. 00007890-200509150-00023 [pii].
15. Shehata M, Cope GH, Johnson TS, Raftery AT, el Nahas AM, (1995) Cyclosporine enhances the expression of TGF-beta in the juxtaglomerular cells of the rat kidney. Kidney Int 48: 1487-1496.
16. Halestrap AP, Davidson AM, (1990) Inhibition of Ca2(+)-induced large-amplitude swelling of liver and heart mitochondria by cyclosporin is probably caused by the inhibitor binding to mitochondrial-matrix peptidyl-prolyl cis-trans isomerase and preventing it interacting with the adenine nucleotide translocase. Biochem J 268: 153-160.
17. Fournier N, Ducet G, Crevat A, (1999) Action of cyclosporine on mitochondrial calcium fluxes. J Bioenergetics Biomembranes 19: 297-303.
18. Zoratti M, Szabo I, (1995) The mitochondrial permeability transition. Biochim Biophys Acta 1241: 139-176.
19. Serkova N, Klawitter J, Niemann CU, (2003) Organ-specific response to inhibition of mitochondrial metabolism by cyclosporine in the rat. Transpl Int 16: 748-755 10.1007/s00147-003-0631-1 [doi].
20. Serkova N, Jacobsen W, Niemann CU, Litt L, Benet LZ, et al. (2001) Sirolimus, but not the structurally related RAD (everolimus), enhances the negative effects of cyclosporine on mitochondrial metabolism in the rat brain. Br J Pharmacol 133: 875-885 10.1038/sj.bjp.0704142 [doi].
21. Niemann CU, Saeed M, Akbari H, Jacobsen W, Benet LZ, et al. (2002) Close association between the reduction in myocardial energy metabolism and infarct size: dose-response assessment of cyclosporine. J Pharmacol Exp Ther 302: 1123-1128 10.1124/jpet.102.036848 [doi].
22. Handschin C, Rhee J, Lin J, Tarr PT, Spiegelman BM, (2003) An autoregulatory loop controls peroxisome proliferator-activated receptor gamma coactivator 1alpha expression in muscle. Proc Natl Acad Sci U S A 100: 7111-7116 10.1073/pnas.1232352100 [doi];1232352100 [pii].
23. Ryder JW, Bassel-Duby R, Olson EN, Zierath JR, (2003) Skeletal muscle reprogramming by activation of calcineurin improves insulin action on metabolic pathways. J Biol Chem 278: 44298-44304 10.1074/jbc.M304510200 [doi];M304510200 [pii].
24. Schaeffer PJ, Wende AR, Magee CJ, Neilson JR, Leone TC, et al. (2004) Calcineurin and calcium/calmodulin-dependent protein kinase activate distinct metabolic gene regulatory programs in cardiac muscle. J Biol Chem 279: 39593-39603 10.1074/jbc.M403649200 [doi];M403649200 [pii].
25. Biswas S, Hwang JW, Kirkham PA, Rahman I (2012) Pharmacologial and Dietary Antioxidant Therapies for Chronic Obstructive Pulmonary Disease. Curr Med Chem. CMC-EPUB-20120903-23 [pii].
26. Kishimoto Y, Tani M, Kondo K (2013) Pleiotropic preventive effects of dietary polyphenols in cardiovascular diseases. Eur J Clin Nutr. ejcn201329 [pii];10.1038/ejcn.2013.29 [doi].
27. Recio MC, Andujar I, Rios JL (2012) Anti-inflammatory agents from plants: progress and potential. Curr Med Chem 19: 2088-2103. CMC-EPUB-20120313-004 [pii].
28. Hugel HM, Jackson N (2012) Redox chemistry of green tea polyphenols: therapeutic benefits in neurodegenerative diseases. Mini Rev Med Chem 12: 380-387. MRMC-EPUB-20120203-003 [pii].
29. Zhong Z, Froh M, Connor HD, Li X, Conzelmann LO, et al. (2002) Prevention of hepatic ischemia-reperfusion injury by green tea extract. Am J Physiol Gastrointest Liver Physiol 283: G957-G964.
30. Zhong Z, Connor HD, Froh M, Bunzendahl H, Lind H, et al. (2005) Free radical-dependent dysfunction of small-for-size rat liver grafts: prevention by plant polyphenols. Gastroenterology 129: 652-664.
31. Zhong Z, Connor HD, Li X, Mason RP, Forman DT, et al. (2006) Reduction of ciclosporin and tacrolimus nephrotoxicity by plant polyphenols. J Pharm Pharmacol 58: 1533-1543 10.1211/jpp.58.11.0015 [doi].
32. Darvesh AS, Bishayee A, (2013) Chemopreventive and therapeutic potential of tea polyphenols in hepatocellular cancer. Nutr Cancer 65: 329-344 10.1080/01635581.2013.767367 [doi].
33. Kada T, Kaneko K, Matsuzaki S, Matsuzaki T, Hara Y, (1985) Detection and chemical identification of natural bio-antimutagens. A case of the green tea factor. Mutat Res 150: 127-132.
34. Frankel EN (1999) Natural phenolic antioxidants and their impact on health. In: Lester P, Hiramastu M, Yoshikawa T, editors. Antioxidant Food Supplements in Human Health. San Diego: Academic Press. pp. 385-392.
35. Vinson JA, (2000) Black and green tea and heart disease: a review. Biofactors 13: 127-132.
36. Lin AM, Chyi BY, Wu LY, Hwang LS, Ho LT, (1998) The antioxidative property of green tea against iron-induced oxidative stress in rat brain. Chin J Physiol 41: 189-194.
37. Miyagawa C, Wu C, Kennedy DO, Nakatani T, Ohtani K, et al. (1997) Protective effect of green tea extract and tea polyphenols against the cytotoxicity of 1,4-naphthoquinone in isolated rat hepatocytes. Biosci Biotechnol Biochem 61: 1901-1905.
38. Hara Y, (1994) Antioxidative action of tea polyphenols: Part 1. Am Biotechnol Lab 12: 48.
39. Yoshino M, Murakami K, (1998) Interaction of iron with polyphenolic compounds: application to antioxidant characterization. Anal Biochem 257: 40-44.
40. Zhong Z, Froh M, Lehnert M, Schoonhoven R, Yang L, et al. (2003) Polyphenols from Camellia sinenesis attenuate experimental cholestasis-induced liver fibrosis in rats. Am J Physiol Gastrointest Liver Physiol 285: G1004-G1013.
41. Rasbach KA, Schnellmann RG, (2008) Isoflavones promote mitochondrial biogenesis. J Pharmacol Exp Ther 325: 536-543 jpet.107.134882 [pii];10.1124/jpet.107.134882 [doi].
42. Taub PR, Ramirez-Sanchez I, Ciaraldi TP, Perkins G, Murphy AN, et al. (2012) Alterations in skeletal muscle indicators of mitochondrial structure and biogenesis in patients with type 2 diabetes and heart failure: effects of epicatechin rich cocoa. Clin Transl Sci 5: 43-47 10.1111/j.1752-8062.2011.00357.x [doi].
43. Yan J, Feng Z, Liu J, Shen W, Wang Y, et al. (2012) Enhanced autophagy plays a cardinal role in mitochondrial dysfunction in type 2 diabetic Goto-Kakizaki (GK) rats: ameliorating effects of (-)-epigallocatechin-3-gallate. J Nutr Biochem 23: 716-724 S0955-2863(11)00111-2 [pii];10.1016/j.jnutbio.2011.03.014 [doi].
44. Nogueira L, Ramirez-Sanchez I, Perkins GA, Murphy A, Taub PR, et al. (2011) (-)-Epicatechin enhances fatigue resistance and oxidative capacity in mouse muscle. J Physiol 589: 4615-4631 jphysiol.2011.209924 [pii];10.1113/jphysiol.2011.209924 [doi].
45. Nieman DC, Henson DA, Maxwell KR, Williams AS, McAnulty SR, et al. (2009) Effects of quercetin and EGCG on mitochondrial biogenesis and immunity. Med Sci Sports Exerc 41: 1467-1475 10.1249/MSS.0b013e318199491f [doi].
46. Funk JA, Odejinmi S, Schnellmann RG, (2010) SRT1720 induces mitochondrial biogenesis and rescues mitochondrial function after oxidant injury in renal proximal tubule cells. J Pharmacol Exp Ther 333: 593-601 jpet.109.161992 [pii];10.1124/jpet.109.161992 [doi].
47. Rasbach KA, Schnellmann RG, (2007) PGC-1alpha over-expression promotes recovery from mitochondrial dysfunction and cell injury. Biochem Biophys Res Commun 355: 734-739.
48. Seo AY, Joseph AM, Dutta D, Hwang JC, Aris JP, et al. (2010) New insights into the role of mitochondria in aging: mitochondrial dynamics and more. J Cell Sci 123: 2533-2542 123/15/2533 [pii];10.1242/jcs.070490 [doi].
49. Lee HC, Wei YH, (2005) Mitochondrial biogenesis and mitochondrial DNA maintenance of mammalian cells under oxidative stress. Int J Biochem Cell Biol 37: 822-834.
50. Wenz T, (2009) PGC-1alpha activation as a therapeutic approach in mitochondrial disease. IUBMB Life 61: 1051-1062 10.1002/iub.261 [doi].
51. Yoshioka N, Hiasa Y, Cho M, Kitahori Y, Hirao K, et al. (1999) Effect of polyphenon-60 on the development of renal cell tumors in rats treated with N-ethyl-N hydroxyethylnitrosamine. Cancer Lett 136: 79-82.
52. Rehman H, Ramshesh VK, Theruvath TP, Kim I, Currin RT, et al. (2008) NIM811, a Mitochondrial Permeability Transition Inhibitor, Attenuates Cholestatic Liver Injury But Not Fibrosis in Mice. J Pharmacol Exp Ther 327: 699-706.
53. Funk JA, Schnellmann RG, (2012) Persistent disruption of mitochondrial homeostasis after acute kidney injury. Am J Physiol Renal Physiol 302: F853-F864 ajprenal.00035.2011 [pii];10.1152/ajprenal.00035.2011 [doi].
54. Liu Q, Rehman H, Shi Y, Krishnasamy Y, Lemasters JJ, et al. (2012) Inhibition of sphingosine kinase-2 suppresses inflammation and attenuates graft injury after liver transplantation in rats. PLoS One 7: e41834 10.1371/journal.pone.0041834 [doi];PONE-D-12-14479 [pii].
55. Arany I, Faisal A, Clark JS, Vera T, Baliga R, et al. (2010) p66SHC-mediated mitochondrial dysfunction in renal proximal tubule cells during oxidative injury. Am J Physiol Renal Physiol 298: F1214-F1221 00639.2009 [pii];10.1152/ajprenal.00639.2009 [doi].
56. Attardi G, Schatz G, (1988) Biogenesis of mitochondria. Annu Rev Cell Biol 4: 289-333.
57. Herrmann JM, Longen S, Weckbecker D, Depuydt M, (2012) Biogenesis of mitochondrial proteins. Adv Exp Med Biol 748: 41-64 10.1007/978-1-4614-3573-0_3 [doi].
58. Puigserver P, Spiegelman BM, (2003) Peroxisome proliferator-activated receptor-gamma coactivator 1 alpha (PGC-1 alpha): transcriptional coactivator and metabolic regulator. Endocr Rev 24: 78-90.
59. Virbasius JV, Scarpulla RC, (1994) Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors: a potential regulatory link between nuclear and mitochondrial gene expression in organelle biogenesis. Proc Natl Acad Sci U S A 91: 1309-1313.
60. Thurman RG, Zhong Z, Frankenberg Mv, Stachlewitz RF, Bunzendahl H, (1997) Prevention of cyclosporin-induced nephrotoxicity with dietary glycine. Transplantation 63: 1661-1667.
61. Bennett M, Dent CL, Ma Q, Dastrala S, Grenier F, et al. (2008) Urine NGAL predicts severity of acute kidney injury after cardiac surgery: a prospective study. Clin J Am Soc Nephrol 3: 665-673 CJN.04010907 [pii];10.2215/CJN.04010907 [doi].
62. Goldstein SL, (2011) Acute kidney injury biomarkers: renal angina and the need for a renal troponin I. BMC Med. 9: 135 1741-7015-9-135 [pii];10.1186/1741-7015-9-135 [doi].
63. Bolignano D, Lacquaniti A, Coppolino G, Donato V, Campo S, et al. (2009) Neutrophil gelatinase-associated lipocalin (NGAL) and progression of chronic kidney disease. Clin J Am Soc Nephrol 4: 337-344 CJN.03530708 [pii];10.2215/CJN.03530708 [doi].
64. Bolignano D, Lacquaniti A, Coppolino G, Donato V, Fazio MR, et al. (2009) Neutrophil gelatinase-associated lipocalin as an early biomarker of nephropathy in diabetic patients. Kidney Blood Press Res 32: 91-98 000209379 [pii];10.1159/000209379 [doi].
65. Jung K, Pergande M, (1985) Influence of cyclosporin A on the respiration of isolated rat kidney mitochondria. FEBS Lett 183: 167-171.
66. Lee SH, Yoon YC, Jang YY, Song JH, Han ES, et al. (2001) Effect of iron and ascorbate on cyclosporine-induced oxidative damage of kidney mitochondria and microsomes. Pharmacol Res 43: 161-171 10.1006/phrs.2000.0759 [doi];S1043-6618(00)90759-X [pii].
67. Serkova N, Brand A, Christians U, Leibfritz D, (1996) Evaluation of the effects of immunosuppressants on neuronal and glial cells in vitro by multinuclear magnetic resonance spectroscopy. Biochim Biophys Acta 1314: 93-104.
68. Reichert AS, Neupert W, (2004) Mitochondriomics or what makes us breathe. Trends Genet 20: 555-562.
69. Robin ED, Wong R, (1988) Mitochondrial DNA molecules and virtual number of mitochondria per cell in mammalian cells. J Cell Physiol 136: 507-513.
70. Marechal X, Montaigne D, Marciniak C, Marchetti P, Hassoun SM, et al. (2011) Doxorubicin-induced cardiac dysfunction is attenuated by ciclosporin treatment in mice through improvements in mitochondrial bioenergetics. Clin Sci (Lond) 121: 405-413 CS20110069 [pii];10.1042/CS20110069 [doi].
71. Winder WW, Taylor EB, Thomson DM, (2006) Role of AMP-activated protein kinase in the molecular adaptation to endurance exercise. Med Sci Sports Exerc 38: 1945-1949.
72. Scarpulla RC, (2002) Nuclear activators and coactivators in mammalian mitochondrial biogenesis. Biochim Biophys Acta 1576: 1-14.
73. Scarpulla RC, (2002) Transcriptional activators and coactivators in the nuclear control of mitochondrial function in mammalian cells. Gene 286: 81-89.
74. Devaux F, Lelandais G, Garcia M, Goussard S, Jacq C (2010) Posttranscriptional control of mitochondrial biogenesis: Spatio-temporal regulation of the protein import process. FEBS Lett. S0014-5793(10)00762-3 [pii];10.1016/j.febslet.2010.09.030 [doi].
75. Huss JM, Torra IP, Staels B, Giguere V, Kelly DP, (2004) Estrogen-related receptor alpha directs peroxisome proliferator-activated receptor alpha signaling in the transcriptional control of energy metabolism in cardiac and skeletal muscle. Mol Cell Biol 24: 9079-9091.
76. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, et al. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98: 115-124.
77. Cote J, Ruiz-Carrillo A, (1993) Primers for mitochondrial DNA replication generated by endonuclease G. Science. 261: 765-769.
78. Lehman JJ, Barger PM, Kovacs A, Saffitz JE, Medeiros DM, et al. (2000) Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J Clin Invest 106: 847-856.
79. Lowell BB, Spiegelman BM, (2000) Towards a molecular understanding of adaptive thermogenesis. Nature 404: 652-660.
80. Zong H, Ren JM, Young LH, Pypaert M, Mu J, et al. (2002) AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc Natl Acad Sci U S A 99: 15983-15987.
81. Wu H, Kanatous SB, Thurmond FA, Gallardo T, Isotani E, et al. (2002) Regulation of mitochondrial biogenesis in skeletal muscle by CaMK. Science 296: 349-352.
82. Nemoto S, Fergusson MM, Finkel T, (2005) SIRT1 functionally interacts with the metabolic regulator and transcriptional coactivator PGC-1{alpha}. J Biol Chem 280: 16456-16460 M501485200 [pii];10.1074/jbc.M501485200 [doi].
83. Rodgers JT, Lerin C, Haas W, Gygi SP, Spiegelman BM, et al. (2005) Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 434: 113-118 nature03354 [pii];10.1038/nature03354 [doi].
84. Canto C, Auwerx J, (2009) PGC-1alpha, SIRT1 and AMPK, an energy sensing network that controls energy expenditure. Curr Opin Lipidol 20: 98-105 10.1097/MOL.0b013e328328d0a4 [doi];00041433-200904000-00004 [pii].
85. Garnier A, Fortin D, Zoll J, N'Guessan B, Mettauer B, et al. (2005) Coordinated changes in mitochondrial function and biogenesis in healthy and diseased human skeletal muscle. FASEB J 19: 43-52 19/1/43 [pii];10.1096/fj.04-2173com [doi].
86. Norrbom J, Sundberg CJ, Ameln H, Kraus WE, Jansson E, et al. (2004) PGC-1alpha mRNA expression is influenced by metabolic perturbation in exercising human skeletal muscle. J Appl Physiol 96: 189-194 10.1152/japplphysiol.00765.2003 [doi];00765.2003 [pii].
87. Lin J, Wu H, Tarr PT, Zhang CY, Wu Z, et al. (2002) Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 418: 797-801 10.1038/nature00904 [doi];nature00904 [pii].
88. Milne JC, Lambert PD, Schenk S, Carney DP, Smith JJ, et al. (2007) Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes. Nature 450: 712-716.
89. Rasbach KA, Funk JA, Jayavelu T, Green PT, Schnellmann RG, (2010) 5-hydroxytryptamine receptor stimulation of mitochondrial biogenesis. J Pharmacol Exp Ther 332: 632-639 jpet.109.159947 [pii];10.1124/jpet.109.159947 [doi].
90. Beeson CC, Beeson GC, Schnellmann RG, (2010) A high-throughput respirometric assay for mitochondrial biogenesis and toxicity. Anal Biochem 404: 75-81 S0003-2697(10)00292-7 [pii];10.1016/j.ab.2010.04.040 [doi].
91. Wills LP, Trager RE, Beeson GC, Lindsey CC, Peterson YK, et al. (2012) beta2 Adrenoceptor Agonist Formoterol Stimulates Mitochondrial Biogenesis. J Pharmacol Exp Ther. jpet.112.191528 [pii];10.1124/jpet.112.191528 [doi].
92. Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, et al. (2006) Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 127: 1109-1122 S0092-8674(06)01428-0 [pii];10.1016/j.cell.2006.11.013 [doi].
93. Yun JM, Jialal I, Devaraj S, (2010) Effects of epigallocatechin gallate on regulatory T cell number and function in obese v. lean volunteers. Br J Nutr 103: 1771-1777 S000711451000005X [pii];10.1017/S000711451000005X [doi].
94. Gundimeda U, McNeill TH, Elhiani AA, Schiffman JE, Hinton DR, et al. (2012) Green tea polyphenols precondition against cell death induced by oxygen-glucose deprivation via stimulation of laminin receptor, generation of reactive oxygen species, and activation of protein kinase Cepsilon. J Biol Chem 287: 34694-34708 M112.356899 [pii];10.1074/jbc.M112.356899 [doi].
95. Duluc L, Jacques C, Soleti R, Iacobazzi F, Simard G, et al. (2013) Modulation of mitochondrial capacity and angiogenesis by red wine polyphenols via estrogen receptor, NADPH oxidase and nitric oxide synthase pathways. Int J Biochem Cell Biol 45: 783-791 S1357-2725(13)00017-4 [pii];10.1016/j.biocel.2013.01.007 [doi].
96. Mitscher LA, Jung M, Shankel D, Dou JH, Steele L, et al. (1997) Chemoprotection: a review of the potential therapeutic antioxidant properties of green tea (Camellia sinensis) and certain of its constituents. Med Res Rev 17: 327-365.
97. Guo Q, Zhao B, Li M, Shen S, Xin W, (1996) Studies on protective mechanisms of four components of green tea polyphenols against lipid peroxidation in synaptosomes. Biochim Biophys Acta 1304: 210-222.