Lipoamide acts as an indirect antioxidant by simultaneously stimulating mitochondrial biogenesis and phase II antioxidant enzyme systems in ARPE-19 cells

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Zhao, Lin ^a   Liu, Zhongbo ^a,b   Jia, Haiqun ^a,c   Feng, Zhihui ^a   Liu, Jiankang ^a,d   Li, Xuesen ^a,e  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b NEW YORK UNIVERSITY COLLEGE OF DENTISTRY   (United States)

^c California Institute for Biomedical Research   (United States)

^d TIANJIN UNIVERSITY OF SPORT   (China)

^e SOUTHWEST MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; CATALASE; CELL PROTEIN; COPPER ZINC SUPEROXIDE DISMUTASE; GAMMA GLUTAMYL CYSTEINYL LIGASE; GLUTATHIONE TRANSFERASE; LIGASE; LIPOAMIDE; MITOCHONDRIAL DNA; NADPH QUINONE OXIDOREDUCTASE 1; OXIDOREDUCTASE; PRX3 PROTEIN; PRX5 PROTEIN; REACTIVE OXYGEN METABOLITE; THIOCTIC ACID; TRANSCRIPTION FACTOR NRF2; TRX2 PROTEIN; UNCLASSIFIED DRUG; ENZYME; NFE2L2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ANTIOXIDANT ACTIVITY; ARTICLE; BIOGENESIS; CELL STIMULATION; CELL VOLUME; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; DRUG POTENCY; ELECTRON TRANSPORT; ENZYME ACTIVITY; ENZYME INDUCTION; GENE DOSAGE; HUMAN; HUMAN CELL; MITOCHONDRION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; UPREGULATION; ANALOGS AND DERIVATIVES; CELL LINE; COPY NUMBER VARIATION; CYTOLOGY; DRUG EFFECTS; ENZYMOLOGY; GENETICS; METABOLISM; ORGANELLE BIOGENESIS; RETINAL PIGMENT EPITHELIUM;

ANTIOXIDANTS; CELL LINE; DNA COPY NUMBER VARIATIONS; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT; ENZYMES; HUMANS; NF-E2-RELATED FACTOR 2; ORGANELLE BIOGENESIS; RETINAL PIGMENT EPITHELIUM; THIOCTIC ACID; TRANSCRIPTION FACTORS;

EID: 84933057133     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0128502     Document Type: Article

References (46)

1. Green WR, McDonnell PJ, Yeo JH. Pathologic features of senile macular degeneration. Ophthalmology. 1985; 92(5):615-27. PMID: 2409504.
2. Spraul CW, Lang GE, Grossniklaus HE. Morphometric analysis of the choroid, Bruch's membrane, and retinal pigment epithelium in eyes with age-related macular degeneration. Invest Ophthalmol Vis Sci. 1996; 37(13):2724-35. PMID: 8977488.
3. Liang FQ, Godley BF. Oxidative stress-induced mitochondrial DNA damage in human retinal pigment epithelial cells: a possible mechanism for RPE aging and age-related macular degeneration. Exp Eye Res. 2003; 76(4):397-403. PMID: 12634104.
4. Ames BN, Shigenaga MK, Hagen TM. Mitochondrial decay in aging. Biochim Biophys Acta. 1995; 1271(1):165-70. PMID: 7599204.
5. Wallace DC. The mitochondrial genome in human adaptive radiation and disease: on the road to therapeutics and performance enhancement. Gene. 2005; 354:169-80. PMID: 16024186.
6. Petersen KF, Dufour S, Befroy D, Garcia R, Shulman GI. Impaired mitochondrial activity in the insulinresistant offspring of patients with type 2 diabetes. N Engl J Med. 2004; 350(7):664-71. PMID: 14960743.
7. Liu J, Ames BN. Reducing mitochondrial decay with mitochondrial nutrients to delay and treat cognitive dysfunction, Alzheimer's disease, and Parkinson's disease. Nutr Neurosci. 2005; 8(2):67-89. PMID: 16053240.
8. Reznick RM, Shulman GI. The role of AMP-activated protein kinase in mitochondrial biogenesis. J Physiol. 2006; 574(Pt 1):33-9. PMID: 16709637.
9. Morino K, Petersen KF, Dufour S, Befroy D, Frattini J, Shatzkes N, et al. Reduced mitochondrial density and increased IRS-1 serine phosphorylation in muscle of insulin-resistant offspring of type 2 diabetic parents. J Clin Invest. 2005; 115(12):3587-93. PMID: 16284649.
10. Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, Kashyap S, et al. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1. Proc Natl Acad Sci U S A. 2003; 100(14):8466-71. PMID: 12832613.
11. Shen W, Liu K, Tian C, Yang L, Li X, Ren J, et al. R-alpha-lipoic acid and acetyl-L-carnitine complementarily promote mitochondrial biogenesis in murine 3T3-L1 adipocytes. Diabetologia. 2008; 51(1):165-74. Epub 2007/11/21. doi: 10.1007/s00125-007-0852-4 PMID: 18026715.
12. Nisoli E, Tonello C, Cardile A, Cozzi V, Bracale R, Tedesco L, et al. Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science. 2005; 310(5746):314-7. PMID: 16224023.
13. Guarente L. Mitochondria-a nexus for aging, calorie restriction, and sirtuins? Cell. 2008; 132(2):171-6. PMID: 18243090. doi: 10.1016/j.cell.2008.01.007
14. Puigserver P,Wu Z, Park CW, Graves R, Wright M, Spiegelman BM. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell. 1998; 92(6):829-39. PMID: 9529258.
15. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell. 1999; 98(1):115-24. PMID: 10412986.
16. Lee JM, Li J, Johnson DA, Stein TD, Kraft AD, Calkins MJ, et al. Nrf2, a multi-organ protector? Faseb J. 2005; 19(9):1061-6. PMID: 15985529.
17. Kensler TW, Wakabayashi N, Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol. 2007; 47:89-116. PMID: 16968214.
18. Packer L, Witt EH, Tritschler HJ. alpha-Lipoic acid as a biological antioxidant. Free Radic Biol Med. 1995; 19(2):227-50. PMID: 7649494.
19. Packer L, Kraemer K, Rimbach G. Molecular aspects of lipoic acid in the prevention of diabetes complications. Nutrition. 2001; 17(10):888-95. PMID: 11684397.
20. Liu J. The effects and mechanisms of mitochondrial nutrient alpha-lipoic acid on improving age-associated mitochondrial and cognitive dysfunction: an overview. Neurochem Res. 2008; 33(1):194-203. PMID: 17605107.
21. Jia L, Liu Z, Sun L, Miller SS, Ames BN, Cotman CW, et al. Acrolein, a toxicant in cigarette smoke, causes oxidative damage and mitochondrial dysfunction in RPE cells: protection by (R)-alpha-lipoic acid. Invest Ophthalmol Vis Sci. 2007; 48(1):339-48. PMID: 17197552.
22. Li X, Liu Z, Luo C, Jia H, Sun L, Hou B, et al. Lipoamide protects retinal pigment epithelial cells from oxidative stress and mitochondrial dysfunction. Free Radic Biol Med. 2008; 44(7):1465-74. PMID: 18258206. doi: 10.1016/j.freeradbiomed.2008.01.004
23. Liu Z, Sun L, Zhu L, Jia X, Li X, Jia H, et al. Hydroxytyrosol protects retinal pigment epithelial cells from acrolein-induced oxidative stress and mitochondrial dysfunction. J Neurochem. 2007; 103:2690-700. PMID: 17949413. doi: 10.1111/j.1471-4159.2007.04954.x
24. Fukuyama R, Nakayama A, Nakase T, Toba H, Mukainaka T, Sakaguchi H, et al. A newly established neuronal rho-0 cell line highly susceptible to oxidative stress accumulates iron and other metals. Relevance to the origin of metal ion deposits in brains with neurodegenerative disorders. J Biol Chem. 2002; 277(44):41455-62. PMID: 12194972.
25. Reers M, Smiley ST, Mottola-Hartshorn C, Chen A, Lin M, Chen LB. Mitochondrial membrane potential monitored by JC-1 dye. Methods Enzymol. 1995; 260:406-17. PMID: 8592463.
26. Royall JA, Ischiropoulos H. Evaluation of 2′,7′-dichlorofluorescin and dihydrorhodamine 123 as fluorescent probes for intracellular H2O2 in cultured endothelial cells. Arch Biochem Biophys. 1993; 302(2):348-55. PMID: 8387741.
27. Schieke SM, Phillips D, McCoy JP Jr., Aponte AM, Shen RF, Balaban RS, et al. The mammalian target of rapamycin (mTOR) pathway regulates mitochondrial oxygen consumption and oxidative capacity. J Biol Chem. 2006; 281(37):27643-52. PMID: 16847060.
28. Powelka AM, Seth A, Virbasius JV, Kiskinis E, Nicoloro SM, Guilherme A, et al. Suppression of oxidative metabolism and mitochondrial biogenesis by the transcriptional corepressor RIP140 in mouse adipocytes. J Clin Invest. 2006; 116(1):125-36. PMID: 16374519.
29. Cheung EC, Joza N, Steenaart NA, McClellan KA, Neuspiel M, McNamara S, et al. Dissociating the dual roles of apoptosis-inducing factor in maintaining mitochondrial structure and apoptosis. The EMBO journal. 2006; 25(17):4061-73. PMID: 16917506.
30. Kuroda Y, Mitsui T, Kunishige M, Shono M, Akaike M, Azuma H, et al. Parkin enhances mitochondrial biogenesis in proliferating cells. Hum Mol Genet. 2006; 15(6):883-95. PMID: 16449237.
31. 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(3):562-73. PMID: 15914121.
32. Nordfjall K, Larefalk A, Lindgren P, Holmberg D, Roos G. Telomere length and heredity: Indications of paternal inheritance. Proc Natl Acad Sci U S A. 2005; 102(45):16374-8. PMID: 16258070.
33. Jaiswal AK. Regulation of genes encoding NAD(P)H:quinone oxidoreductases. Free Radic Biol Med. 2000; 29(3-4):254-62. PMID: 11035254.
34. Pabst MJ, Habig WH, Jakoby WB. Glutathione S-transferase A. A novel kinetic mechanism in which the major reaction pathway depends on substrate concentration. J Biol Chem. 1974; 249(22):7140-7. PMID: 4436301.
35. White CC, Viernes H, Krejsa CM, Botta D, Kavanagh TJ. Fluorescence-based microtiter plate assay for glutamate-cysteine ligase activity. Anal Biochem. 2003; 318(2):175-80. PMID: 12814619.
36. Riganti C, Aldieri E, Bergandi L, Fenoglio I, Costamagna C, Fubini B, et al. Crocidolite asbestos inhibits pentose phosphate oxidative pathway and glucose 6-phosphate dehydrogenase activity in human lung epithelial cells. Free Radic Biol Med. 2002; 32(9):938-49. Epub 2002/04/30. doi: S0891584902008006 [pii]. PMID: 11978496.
37. Shen W, Liu K, Tian C, Yang L, Li X, Ren J, et al. R-alpha-Lipoic acid and acetyl-L:-carnitine complementarily promote mitochondrial biogenesis in murine 3T3-L1 adipocytes. Diabetologia. 2008; 51(1):165-74. PMID: 18026715.
38. Gardiner CS, Reed DJ. Synthesis of glutathione in the preimplantation mouse embryo. Arch Biochem Biophys. 1995; 318(1):30-6. PMID: 7726569.
39. Liu J, Atamna H, Kuratsune H, Ames BN. Delaying brain mitochondrial decay and aging with mitochondrial antioxidants and metabolites. Ann New York Acad Sci. 2002; 959:133-66. PMID: 11976193
40. Zhang H, Jia H, Liu J, Ao N, Yan B, Shen W, et al. Combined R-alpha-lipoic acid and acetyl-L-carnitine exerts efficient preventative effects in a cellular model of Parkinson's disease. J Cell Mol Med. 2008. Epub 2008/07/16. doi: JCMM390 [pii] doi: 10.1111/j.1582-4934.2008.00390.x PMID: 18624765.
41. Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants, and aging. Cell. 2005; 120(4):483-95. PMID: 15734681.
42. St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jager S, et al. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell. 2006; 127(2):397-408. PMID: 17055439.
43. Snoke JE, Yanari S, Bloch K. Synthesis of glutathione from gamma-glutamylcysteine. J Biol Chem. 1953; 201(2):573-86. PMID: 13061393.
44. Yanari S, Snoke JE, Bloch K. Energy sources in glutathione synthesis. J Biol Chem. 1953; 201(2):561-71. PMID: 13061392.
45. Slyshenkov VS, Dymkowska D, Wojtczak L. Pantothenic acid and pantothenol increase biosynthesis of glutathione by boosting cell energetics. FEBS Lett. 2004; 569(1-3):169-72. PMID: 15225628.
46. Vali S, Mythri RB, Jagatha B, Padiadpu J, Ramanujan KS, et al. (2007) Integrating glutathione metabolism and mitochondrial dysfunction with implications for Parkinson's disease: a dynamic model. Neuroscience 149: 917-930. PMID: 17936517