Upregulated autophagy protects cardiomyocytes from oxidative stress-induced toxicity

References

• Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants, and aging. Cell 2005; 120:483 - 95; http://dx.doi.org/10.1016/j.cell.2005.02.001; PMID: 15734681
   PubMed Web of Science ®Google Scholar
• Judge S, Jang YM, Smith A, Hagen T, Leeuwenburgh C. Age-associated increases in oxidative stress and antioxidant enzyme activities in cardiac interfibrillar mitochondria: implications for the mitochondrial theory of aging. FASEB J 2005; 19:419 - 21; PMID: 15642720
   PubMed Web of Science ®Google Scholar
• Grivennikova VG, Kareyeva AV, Vinogradov AD. What are the sources of hydrogen peroxide production by heart mitochondria?. Biochim Biophys Acta 2010; 1797:939 - 44; http://dx.doi.org/10.1016/j.bbabio.2010.02.013; PMID: 20170624
   PubMed Web of Science ®Google Scholar
• Starkov AA. The role of mitochondria in reactive oxygen species metabolism and signaling. Ann N Y Acad Sci 2008; 1147:37 - 52; http://dx.doi.org/10.1196/annals.1427.015; PMID: 19076429
   PubMed Web of Science ®Google Scholar
• Brand MD. The sites and topology of mitochondrial superoxide production. Exp Gerontol 2010; 45:466 - 72; http://dx.doi.org/10.1016/j.exger.2010.01.003; PMID: 20064600
   PubMed Web of Science ®Google Scholar
• Finkel T. Signal transduction by mitochondrial oxidants. J Biol Chem 2012; 287:4434 - 40; http://dx.doi.org/10.1074/jbc.R111.271999; PMID: 21832045
   PubMed Web of Science ®Google Scholar
• Lin MT, Beal MF. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006; 443:787 - 95; http://dx.doi.org/10.1038/nature05292; PMID: 17051205
   PubMed Web of Science ®Google Scholar
• Judge S, Leeuwenburgh C. Cardiac mitochondrial bioenergetics, oxidative stress, and aging. Am J Physiol Cell Physiol 2007; 292:C1983 - 92; http://dx.doi.org/10.1152/ajpcell.00285.2006; PMID: 17344313
   PubMed Web of Science ®Google Scholar
• Yakes FM, Van Houten B. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci U S A 1997; 94:514 - 9; http://dx.doi.org/10.1073/pnas.94.2.514; PMID: 9012815
   PubMed Web of Science ®Google Scholar
• Sohal RS, Ku HH, Agarwal S, Forster MJ, Lal H. Oxidative damage, mitochondrial oxidant generation and antioxidant defenses during aging and in response to food restriction in the mouse. Mech Ageing Dev 1994; 74:121 - 33; http://dx.doi.org/10.1016/0047-6374(94)90104-X; PMID: 7934203
   PubMed Web of Science ®Google Scholar
• Barja G, Herrero A. Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals. FASEB J 2000; 14:312 - 8; PMID: 10657987
   PubMed Web of Science ®Google Scholar
• Abel ED, Doenst T. Mitochondrial adaptations to physiological vs. pathological cardiac hypertrophy. Cardiovasc Res 2011; 90:234 - 42; http://dx.doi.org/10.1093/cvr/cvr015; PMID: 21257612
   PubMed Web of Science ®Google Scholar
• Lesnefsky EJ, Moghaddas S, Tandler B, Kerner J, Hoppel CL. Mitochondrial dysfunction in cardiac disease: ischemia--reperfusion, aging, and heart failure. J Mol Cell Cardiol 2001; 33:1065 - 89; http://dx.doi.org/10.1006/jmcc.2001.1378; PMID: 11444914
   PubMed Web of Science ®Google Scholar
• Dai DF, Santana LF, Vermulst M, Tomazela DM, Emond MJ, MacCoss MJ, et al. Overexpression of catalase targeted to mitochondria attenuates murine cardiac aging. Circulation 2009; 119:2789 - 97; http://dx.doi.org/10.1161/CIRCULATIONAHA.108.822403; PMID: 19451351
   PubMed Web of Science ®Google Scholar
• Mizushima N, Levine B. Autophagy in mammalian development and differentiation. Nat Cell Biol 2010; 12:823 - 30; http://dx.doi.org/10.1038/ncb0910-823; PMID: 20811354
   PubMed Web of Science ®Google Scholar
• He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43:67 - 93; http://dx.doi.org/10.1146/annurev-genet-102808-114910; PMID: 19653858
   PubMed Web of Science ®Google Scholar
• Tait SW, Green DR. Mitochondria and cell death: outer membrane permeabilization and beyond. Nat Rev Mol Cell Biol 2010; 11:621 - 32; http://dx.doi.org/10.1038/nrm2952; PMID: 20683470
   PubMed Web of Science ®Google Scholar
• Cuervo AM, Bergamini E, Brunk UT, Dröge W, Ffrench M, Terman A. Autophagy and aging: the importance of maintaining “clean” cells. Autophagy 2005; 1:131 - 40; http://dx.doi.org/10.4161/auto.1.3.2017; PMID: 16874025
   PubMed Web of Science ®Google Scholar
• Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 2007; 26:1749 - 60; http://dx.doi.org/10.1038/sj.emboj.7601623; PMID: 17347651
   PubMed Web of Science ®Google Scholar
• Dewaele M, Maes H, Agostinis P. ROS-mediated mechanisms of autophagy stimulation and their relevance in cancer therapy. Autophagy 2010; 6:838 - 54; http://dx.doi.org/10.4161/auto.6.7.12113; PMID: 20505317
   PubMed Web of Science ®Google Scholar
• Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, et al. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet 2004; 36:585 - 95; http://dx.doi.org/10.1038/ng1362; PMID: 15146184
   PubMed Web of Science ®Google Scholar
• Jung CH, Jun CB, Ro SH, Kim YM, Otto NM, Cao J, et al. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 2009; 20:1992 - 2003; http://dx.doi.org/10.1091/mbc.E08-12-1249; PMID: 19225151
   PubMed Web of Science ®Google Scholar
• Khan S, Salloum F, Das A, Xi L, Vetrovec GW, Kukreja RC. Rapamycin confers preconditioning-like protection against ischemia-reperfusion injury in isolated mouse heart and cardiomyocytes. J Mol Cell Cardiol 2006; 41:256 - 64; http://dx.doi.org/10.1016/j.yjmcc.2006.04.014; PMID: 16769083
   PubMed Web of Science ®Google Scholar
• McMullen JR, Sherwood MC, Tarnavski O, Zhang L, Dorfman AL, Shioi T, et al. Inhibition of mTOR signaling with rapamycin regresses established cardiac hypertrophy induced by pressure overload. Circulation 2004; 109:3050 - 5; http://dx.doi.org/10.1161/01.CIR.0000130641.08705.45; PMID: 15184287
   PubMed Web of Science ®Google Scholar
• Harada M, Hanada S, Toivola DM, Ghori N, Omary MB. Autophagy activation by rapamycin eliminates mouse Mallory-Denk bodies and blocks their proteasome inhibitor-mediated formation. Hepatology 2008; 47:2026 - 35; http://dx.doi.org/10.1002/hep.22294; PMID: 18454506
   PubMed Web of Science ®Google Scholar
• Nakayama K, Okamoto F, Harada Y. Antimycin A: isolation from a new Streptomyces and activity against rice plant blast fungi. J Antibiot (Tokyo) 1956; 9:63 - 6; PMID: 13345726
   PubMed Web of Science ®Google Scholar
• Potter VR, Reif AE. Inhibition of an electron transport component by antimycin A. J Biol Chem 1952; 194:287 - 97; PMID: 14927618
   PubMed Web of Science ®Google Scholar
• Pham NA, Robinson BH, Hedley DW. Simultaneous detection of mitochondrial respiratory chain activity and reactive oxygen in digitonin-permeabilized cells using flow cytometry. Cytometry 2000; 41:245 - 51; http://dx.doi.org/10.1002/1097-0320(20001201)41:4<245::AID-CYTO2>3.0.CO;2-#; PMID: 11084609
   PubMedGoogle Scholar
• Park WH, Han YW, Kim SH, Kim SZ. An ROS generator, antimycin A, inhibits the growth of HeLa cells via apoptosis. J Cell Biochem 2007; 102:98 - 109; http://dx.doi.org/10.1002/jcb.21280; PMID: 17372917
   PubMed Web of Science ®Google Scholar
• Park WH, Han YW, Kim SW, Kim SH, Cho KW, Kim SZ. Antimycin A induces apoptosis in As4.1 juxtaglomerular cells. Cancer Lett 2007; 251:68 - 77; http://dx.doi.org/10.1016/j.canlet.2006.11.002; PMID: 17189668
   PubMed Web of Science ®Google Scholar
• Mukhopadhyay P, Rajesh M, Haskó G, Hawkins BJ, Madesh M, Pacher P. Simultaneous detection of apoptosis and mitochondrial superoxide production in live cells by flow cytometry and confocal microscopy. Nat Protoc 2007; 2:2295 - 301; http://dx.doi.org/10.1038/nprot.2007.327; PMID: 17853886
   PubMed Web of Science ®Google Scholar
• Scaduto RC Jr., Grotyohann LW. Measurement of mitochondrial membrane potential using fluorescent rhodamine derivatives. Biophys J 1999; 76:469 - 77; http://dx.doi.org/10.1016/S0006-3495(99)77214-0; PMID: 9876159
   PubMed Web of Science ®Google Scholar
• Hofer T, Seo AY, Prudencio M, Leeuwenburgh C. A method to determine RNA and DNA oxidation simultaneously by HPLC-ECD: greater RNA than DNA oxidation in rat liver after doxorubicin administration. Biol Chem 2006; 387:103 - 11; http://dx.doi.org/10.1515/BC.2006.014; PMID: 16497170
   PubMed Web of Science ®Google Scholar
• Chen Y, Azad MB, Gibson SB. Superoxide is the major reactive oxygen species regulating autophagy. Cell Death Differ 2009; 16:1040 - 52; http://dx.doi.org/10.1038/cdd.2009.49; PMID: 19407826
   PubMed Web of Science ®Google Scholar
• Hamacher-Brady A, Brady NR, Gottlieb RA. Enhancing macroautophagy protects against ischemia/reperfusion injury in cardiac myocytes. J Biol Chem 2006; 281:29776 - 87; http://dx.doi.org/10.1074/jbc.M603783200; PMID: 16882669
   PubMed Web of Science ®Google Scholar
• Yuan H, Perry CN, Huang C, Iwai-Kanai E, Carreira RS, Glembotski CC, et al. LPS-induced autophagy is mediated by oxidative signaling in cardiomyocytes and is associated with cytoprotection. Am J Physiol Heart Circ Physiol 2009; 296:H470 - 9; http://dx.doi.org/10.1152/ajpheart.01051.2008; PMID: 19098111
   PubMed Web of Science ®Google Scholar
• Su H, Wang X. Autophagy and p62 in cardiac protein quality control. Autophagy 2011; 7:1382 - 3; http://dx.doi.org/10.4161/auto.7.11.17339; PMID: 21997373
   PubMed Web of Science ®Google Scholar
• Bjørkøy G, Lamark T, Pankiv S, Øvervatn A, Brech A, Johansen T. Monitoring autophagic degradation of p62/SQSTM1. Methods Enzymol 2009; 452:181 - 97; http://dx.doi.org/10.1016/S0076-6879(08)03612-4; PMID: 19200883
   PubMed Web of Science ®Google Scholar
• Larsen KB, Lamark T, Øvervatn A, Harneshaug I, Johansen T, Bjørkøy G. A reporter cell system to monitor autophagy based on p62/SQSTM1. Autophagy 2010; 6:784 - 93; http://dx.doi.org/10.4161/auto.6.6.12510; PMID: 20574168
   PubMed Web of Science ®Google Scholar
• Henics T, Wheatley DN. Cytoplasmic vacuolation, adaptation and cell death: a view on new perspectives and features. Biol Cell 1999; 91:485 - 98; http://dx.doi.org/10.1016/S0248-4900(00)88205-2; PMID: 10572624
   PubMed Web of Science ®Google Scholar
• Shang F, Taylor A. Ubiquitin-proteasome pathway and cellular responses to oxidative stress. Free Radic Biol Med 2011; 51:5 - 16; http://dx.doi.org/10.1016/j.freeradbiomed.2011.03.031; PMID: 21530648
   PubMed Web of Science ®Google Scholar
• Dudek EJ, Shang F, Valverde P, Liu Q, Hobbs M, Taylor A. Selectivity of the ubiquitin pathway for oxidatively modified proteins: relevance to protein precipitation diseases. FASEB J 2005; 19:1707 - 9; PMID: 16099947
   PubMed Web of Science ®Google Scholar
• Gnaiger E. Polarographic oxygen sensors, the oxygraph, and high-resolution respirometry to assess mitochondrial function. In: Dykens; JA, Will; Y e, eds. Drug-Induced Mitochondrial Dysfunction. Hoboken, NJ, USA: John Wiley & Sons, Inc, 2008.
   Google Scholar
• Seglen PO, Gordon PB. 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc Natl Acad Sci U S A 1982; 79:1889 - 92; http://dx.doi.org/10.1073/pnas.79.6.1889; PMID: 6952238
   PubMed Web of Science ®Google Scholar
• Stroikin Y, Dalen H, Lööf S, Terman A. Inhibition of autophagy with 3-methyladenine results in impaired turnover of lysosomes and accumulation of lipofuscin-like material. Eur J Cell Biol 2004; 83:583 - 90; http://dx.doi.org/10.1078/0171-9335-00433; PMID: 15679103
   PubMed Web of Science ®Google Scholar
• Sohal RS, Sohal BH. Hydrogen peroxide release by mitochondria increases during aging. Mech Ageing Dev 1991; 57:187 - 202; http://dx.doi.org/10.1016/0047-6374(91)90034-W; PMID: 1904965
   PubMed Web of Science ®Google Scholar
• Ide T, Tsutsui H, Kinugawa S, Utsumi H, Kang D, Hattori N, et al. Mitochondrial electron transport complex I is a potential source of oxygen free radicals in the failing myocardium. Circ Res 1999; 85:357 - 63; http://dx.doi.org/10.1161/01.RES.85.4.357; PMID: 10455064
   PubMed Web of Science ®Google Scholar
• Hüttemann M, Lee I, Pecinova A, Pecina P, Przyklenk K, Doan JW. Regulation of oxidative phosphorylation, the mitochondrial membrane potential, and their role in human disease. J Bioenerg Biomembr 2008; 40:445 - 56; http://dx.doi.org/10.1007/s10863-008-9169-3; PMID: 18843528
   PubMed Web of Science ®Google Scholar
• Vayssier-Taussat M, Kreps SE, Adrie C, Dall’Ava J, Christiani D, Polla BS. Mitochondrial membrane potential: a novel biomarker of oxidative environmental stress. Environ Health Perspect 2002; 110:301 - 5; http://dx.doi.org/10.1289/ehp.02110301; PMID: 11882482
   PubMed Web of Science ®Google Scholar
• Andreyev AY, Kushnareva YE, Starkov AA. Mitochondrial metabolism of reactive oxygen species. Biochemistry (Mosc) 2005; 70:200 - 14; http://dx.doi.org/10.1007/s10541-005-0102-7; PMID: 15807660
   PubMed Web of Science ®Google Scholar
• Kuchino Y, Mori F, Kasai H, Inoue H, Iwai S, Miura K, et al. Misreading of DNA templates containing 8-hydroxydeoxyguanosine at the modified base and at adjacent residues. Nature 1987; 327:77 - 9; http://dx.doi.org/10.1038/327077a0; PMID: 3574469
   PubMed Web of Science ®Google Scholar
• Cheng KC, Cahill DS, Kasai H, Nishimura S, Loeb LA. 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G----T and A----C substitutions. J Biol Chem 1992; 267:166 - 72; PMID: 1730583
   PubMed Web of Science ®Google Scholar
• Lin HS, Jenner AM, Ong CN, Huang SH, Whiteman M, Halliwell B. A high-throughput and sensitive methodology for the quantification of urinary 8-hydroxy-2′-deoxyguanosine: measurement with gas chromatography-mass spectrometry after single solid-phase extraction. Biochem J 2004; 380:541 - 8; http://dx.doi.org/10.1042/BJ20040004; PMID: 14992687
   PubMed Web of Science ®Google Scholar
• Gedik CM, Collins A, ESCODD (European Standards Committee on Oxidative DNA Damage). Establishing the background level of base oxidation in human lymphocyte DNA: results of an interlaboratory validation study. FASEB J 2005; 19:82 - 4; PMID: 15533950
   PubMed Web of Science ®Google Scholar
• Sachs HG, Colgan JA, Lazarus ML. Ultrastructure of the aging myocardium: a morphometric approach. Am J Anat 1977; 150:63 - 71; http://dx.doi.org/10.1002/aja.1001500105; PMID: 930852
   PubMedGoogle Scholar
• Bova MP, Tam D, McMahon G, Mattson MN. Troglitazone induces a rapid drop of mitochondrial membrane potential in liver HepG2 cells. Toxicol Lett 2005; 155:41 - 50; http://dx.doi.org/10.1016/j.toxlet.2004.08.009; PMID: 15585358
   PubMed Web of Science ®Google Scholar
• Masubuchi Y, Kano S, Horie T. Mitochondrial permeability transition as a potential determinant of hepatotoxicity of antidiabetic thiazolidinediones. Toxicology 2006; 222:233 - 9; http://dx.doi.org/10.1016/j.tox.2006.02.017; PMID: 16621215
   PubMed Web of Science ®Google Scholar
• Kaufmann P, Török M, Zahno A, Waldhauser KM, Brecht K, Krähenbühl S. Toxicity of statins on rat skeletal muscle mitochondria. Cell Mol Life Sci 2006; 63:2415 - 25; http://dx.doi.org/10.1007/s00018-006-6235-z; PMID: 17013560
   PubMed Web of Science ®Google Scholar
• Bjelakovic G, Nikolova D, Gluud LL, Simonetti RG, Gluud C. Mortality in randomized trials of antioxidant supplements for primary and secondary prevention: systematic review and meta-analysis. JAMA 2007; 297:842 - 57; http://dx.doi.org/10.1001/jama.297.8.842; PMID: 17327526
   PubMed Web of Science ®Google Scholar
• Levonen AL, Vähäkangas E, Koponen JK, Ylä-Herttuala S. Antioxidant gene therapy for cardiovascular disease: current status and future perspectives. Circulation 2008; 117:2142 - 50; http://dx.doi.org/10.1161/CIRCULATIONAHA.107.718585; PMID: 18427144
   PubMed Web of Science ®Google Scholar
• Tinkel J, Hassanain H, Khouri SJ. Cardiovascular antioxidant therapy: a review of supplements, pharmacotherapies, and mechanisms. Cardiol Rev 2012; 20:77 - 83; PMID: 22293859
   PubMed Web of Science ®Google Scholar
• Kiffin R, Bandyopadhyay U, Cuervo AM. Oxidative stress and autophagy. Antioxid Redox Signal 2006; 8:152 - 62; http://dx.doi.org/10.1089/ars.2006.8.152; PMID: 16487049
   PubMed Web of Science ®Google Scholar
• Mendl N, Occhipinti A, Müller M, Wild P, Dikic I, Reichert AS. Mitophagy in yeast is independent of mitochondrial fission and requires the stress response gene WHI2. J Cell Sci 2011; 124:1339 - 50; http://dx.doi.org/10.1242/jcs.076406; PMID: 21429936
   PubMed Web of Science ®Google Scholar
• Ma X, Jin M, Cai Y, Xia H, Long K, Liu J, et al. Mitochondrial electron transport chain complex III is required for antimycin A to inhibit autophagy. Chem Biol 2011; 18:1474 - 81; http://dx.doi.org/10.1016/j.chembiol.2011.08.009; PMID: 22118681
   PubMed Web of Science ®Google Scholar
• Pan T, Rawal P, Wu Y, Xie W, Jankovic J, Le W. Rapamycin protects against rotenone-induced apoptosis through autophagy induction. Neuroscience 2009; 164:541 - 51; http://dx.doi.org/10.1016/j.neuroscience.2009.08.014; PMID: 19682553
   PubMed Web of Science ®Google Scholar
• Ravikumar B, Berger Z, Vacher C, O’Kane CJ, Rubinsztein DC. Rapamycin pre-treatment protects against apoptosis. Hum Mol Genet 2006; 15:1209 - 16; http://dx.doi.org/10.1093/hmg/ddl036; PMID: 16497721
   PubMed Web of Science ®Google Scholar
• Gershon H, Gershon D. Detection of inactive enzyme molecules in ageing organisms. Nature 1970; 227:1214 - 7; http://dx.doi.org/10.1038/2271214a0; PMID: 5212575
   PubMed Web of Science ®Google Scholar
• Miquel J, Tappel AL, Dillard CJ, Herman MM, Bensch KG. Fluorescent products and lysosomal components in aging Drosophila melanogaster. J Gerontol 1974; 29:622 - 37; http://dx.doi.org/10.1093/geronj/29.6.622; PMID: 4214300
   PubMedGoogle Scholar
• Iwai K, Drake SK, Wehr NB, Weissman AM, LaVaute T, Minato N, et al. Iron-dependent oxidation, ubiquitination, and degradation of iron regulatory protein 2: implications for degradation of oxidized proteins. Proc Natl Acad Sci U S A 1998; 95:4924 - 8; http://dx.doi.org/10.1073/pnas.95.9.4924; PMID: 9560204
   PubMed Web of Science ®Google Scholar
• Webb JL, Ravikumar B, Atkins J, Skepper JN, Rubinsztein DC. Alpha-Synuclein is degraded by both autophagy and the proteasome. J Biol Chem 2003; 278:25009 - 13; http://dx.doi.org/10.1074/jbc.M300227200; PMID: 12719433
   PubMed Web of Science ®Google Scholar
• Dosenko VE, Nagibin VS, Tumanovska LV, Moibenko AA. Protective effect of autophagy in anoxia-reoxygenation of isolated cardiomyocyte?. Autophagy 2006; 2:305 - 6; PMID: 16874046
   PubMed Web of Science ®Google Scholar
• Cohen MV, Downey JM. Adenosine: trigger and mediator of cardioprotection. Basic Res Cardiol 2008; 103:203 - 15; http://dx.doi.org/10.1007/s00395-007-0687-7; PMID: 17999026
   PubMed Web of Science ®Google Scholar
• Nakai A, Yamaguchi O, Takeda T, Higuchi Y, Hikoso S, Taniike M, et al. The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat Med 2007; 13:619 - 24; http://dx.doi.org/10.1038/nm1574; PMID: 17450150
   PubMed Web of Science ®Google Scholar
• Kitsis RN, Peng CF, Cuervo AM. Eat your heart out. Nat Med 2007; 13:539 - 41; http://dx.doi.org/10.1038/nm0507-539; PMID: 17479097
   PubMed Web of Science ®Google Scholar
• Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000; 19:5720 - 8; http://dx.doi.org/10.1093/emboj/19.21.5720; PMID: 11060023
   PubMed Web of Science ®Google Scholar
• Kuma A, Matsui M, Mizushima N. LC3, an autophagosome marker, can be incorporated into protein aggregates independent of autophagy: caution in the interpretation of LC3 localization. Autophagy 2007; 3:323 - 8; PMID: 17387262
   PubMed Web of Science ®Google Scholar
• Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72:248 - 54; http://dx.doi.org/10.1016/0003-2697(76)90527-3; PMID: 942051
   PubMed Web of Science ®Google Scholar