Concentration-dependent effects of the soy phytoestrogen genistein on the proteome of cultured cardiomyocytes

Journal of Proteomics

Volumn 75, Issue 12, 2012, Pages 3592-3604

  Sun, Zeyu ^a   Biela, Laurie M ^b   Hamilton, Karyn L ^b   Reardon, Kenneth F ^a  

^a Engineering Research Center and Hydraulics Laboratory   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

2D electrophoresis; Cardiomyocytes; Genistein

Indexed keywords

ADENOSINE TRIPHOSPHATASE; GENISTEIN; PROTEOME;

APOPTOSIS; ARTICLE; CELL CULTURE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; ENZYME ACTIVITY; GLYCOLYSIS; HEART MUSCLE CELL; HEART PROTECTION; HUMAN; HUMAN CELL; HYDROPHILICITY; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEOMICS; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANIMALS; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; GENISTEIN; MICE; MYOCYTES, CARDIAC; PHYTOESTROGENS; PROTEOME; SOYBEANS;

EID: 84862189612     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2012.04.001     Document Type: Article

References (99)

1. Menotti A., Keys A., Blackburn H., Kromhout D., Karvonen M., Nissinen A., et al. Comparison of multivariate predictive power of major risk factors for coronary heart diseases in different countries: results from eight nations of the Seven Countries Study, 25-year follow-up. J Cardiovasc Risk 1996, 3(1):69-75.
2. Al-Nakkash L., Markus B., Bowden K., Batia L.M., Prozialeck W.C., Broderick T.L. Effects of acute and 2-day genistein treatment on cardiac function and ischemic tolerance in ovariectomized rats. Gend Med 2009, 6(3):488-497.
3. Tissier R., Waintraub X., Couvreur N., Gervais M., Bruneval P., Mandet C., et al. Pharmacological postconditioning with the phytoestrogen genistein. J Mol Cell Cardiol 2007, 42(1):79-87.
4. Deodato B., Altavilla D., Squadrito G., Campo G.M., Arlotta M., Minutoli L., et al. Cardioprotection by the phytoestrogen genistein in experimental myocardial ischaemia-reperfusion injury. Br J Pharmacol 1999, 128(8):1683-1690.
5. Couvreur N., Tissier R., Pons S., Chenoune M., Waintraub X., Berdeaux A., et al. The ceiling effect of pharmacological postconditioning with the phytoestrogen genistein is reversed by the GSK3beta inhibitor SB 216763 [3-(2,4-dichlorophenyl)-4(1-methyl-1 H-indol-3-yl)-1 H-pyrrole-2,5-dione] through mitochondrial ATP-dependent potassium channel opening. J Pharmacol Exp Ther 2009, 329(3):1134-1141.
6. Souzeau E., Belanger S., Picard S., Deschepper C.F. Dietary isoflavones during pregnancy and lactation provide cardioprotection to offspring rats in adulthood. Am J Physiol Heart Circ Physiol 2005, 289(2):H715-H721.
7. Zhai P., Eurell T.E., Cotthaus R.P., Jeffery E.H., Bahr J.M., Gross D.R. Effects of dietary phytoestrogen on global myocardial ischemia-reperfusion injury in isolated female rat hearts. Am J Physiol Heart Circ Physiol 2001, 281(3):H1223-H1232.
8. Dang Z.C. Dose-dependent effects of soy phyto-oestrogen genistein on adipocytes: mechanisms of action. Obes Rev 2009, 10(3):342-349.
9. Stadnicka A., Kwok W.M., Warltier D.C., Bosnjak Z.J. Protein tyrosine kinase-dependent modulation of isoflurane effects on cardiac sarcolemmal K(ATP) channel. Anesthesiology 2002, 97(5):1198-1208.
10. Dang Z.C., Lowik C. Dose-dependent effects of phytoestrogens on bone. Trends Endocrinol Metab 2005, 16(5):207-213.
11. Carter M.W., Smart W.W., Matrone G. Estimation of estrogenic activity of genistein obtained from soybean meal. Proc Soc Exp Biol Med 1953, 84(2):506-508.
12. Miyazaki K. Novel approach for evaluation of estrogenic and anti-estrogenic activities of genistein and daidzein using B16 melanoma cells and dendricity assay. Pigment Cell Res 2004, 17(4):407-412.
13. Maggiolini M., Bonofiglio D., Marsico S., Panno M.L., Cenni B., Picard D., et al. Estrogen receptor alpha mediates the proliferative but not the cytotoxic dose-dependent effects of two major phytoestrogens on human breast cancer cells. Mol Pharmacol 2001, 60(3):595-602.
14. Kuiper G.G., Lemmen J.G., Carlsson B., Corton J.C., Safe S.H., van der Saag P.T., et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 1998, 139(10):4252-4263.
15. van Eickels M., Patten R.D., Aronovitz M.J., Alsheikh-Ali A., Gostyla K., Celestin F., et al. 17-beta-estradiol increases cardiac remodeling and mortality in mice with myocardial infarction. J Am Coll Cardiol 2003, 41(11):2084-2092.
16. Tsai C.H., Su S.F., Chou T.F., Lee T.M. Differential effects of sarcolemmal and mitochondrial K(ATP) channels activated by 17 beta-estradiol on reperfusion arrhythmias and infarct sizes in canine hearts. J Pharmacol Exp Ther 2002, 301(1):234-240.
17. Lee T.M., Su S.F., Tsai C.C., Lee Y.T., Tsai C.H. Cardioprotective effects of 17 beta-estradiol produced by activation ofmitochondrial ATP-sensitive K(+)Channels in canine hearts. J Mol Cell Cardiol 2000, 32(7):1147-1158.
18. Lee T.M., Lin M.S., Chou T.F., Tsai C.H., Chang N.C. Adjunctive 17beta-estradiol administration reduces infarct size by altered expression of canine myocardial connexin43 protein. Cardiovasc Res 2004, 63(1):109-117.
19. Hale S.L., Birnbaum Y., Kloner R.A. Estradiol, Administered Acutely, Protects Ischemic Myocardium in Both Female and Male Rabbits. J Cardiovasc Pharmacol Ther 1997, 2(1):47-52.
20. Booth E.A., Obeid N.R., Lucchesi B.R. Activation of estrogen receptor-alpha protects the in vivo rabbit heart from ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 2005, 289(5):H2039-H2047.
21. Booth E.A., Marchesi M., Kilbourne E.J., Lucchesi B.R. 17 beta-estradiol as a receptor-mediated cardioprotective agent. J Pharmacol Exp Ther 2003, 307(1):395-401.
22. Ng W.W., Keung W., Xu Y.C., Ng K.F., Leung G.P., Vanhoutte P.M., et al. Genistein potentiates protein kinase A activity in porcine coronary artery. Mol Cell Biochem 2008, 311(1-2):37-44.
23. Teoh H., Man R.Y. Enhanced relaxation of porcine coronary arteries after acute exposure to a physiological level of 17beta-estradiol involves non-genomic mechanisms and the cyclic AMP cascade. Br J Pharmacol 2000, 129(8):1739-1747.
24. Akiyama T., Ishida J., Nakagawa S., Ogawara H., Watanabe S., Itoh N., et al. Genistein, a specific inhibitor of tyrosine-specific protein kinases. J Biol Chem 1987, 262(12):5592-5595.
25. Baines C.P., Wang L., Cohen M.V., Downey J.M. Protein tyrosine kinase is downstream of protein kinase C for ischemic preconditioning's anti-infarct effect in the rabbit heart. J Mol Cell Cardiol 1998, 30(2):383-392.
26. Benter I.F., Juggi J.S., Khan I., Yousif M.H., Canatan H., Akhtar S. Signal transduction mechanisms involved in cardiac preconditioning: role of Ras-GTPase, Ca2+/calmodulin-dependent protein kinase II and epidermal growth factor receptor. Mol Cell Biochem 2005, 268(1-2):175-183.
27. Fryer R.M., Schultz J.E., Hsu A.K., Gross G.J. Pretreatment with tyrosine kinase inhibitors partially attenuates ischemic preconditioning in rat hearts. Am J Physiol 1998, 275(6 Pt 2):H2009-H2015.
28. Fryer R.M., Schultz J.E., Hsu A.K., Gross G.J. Importance of PKC and tyrosine kinase in single or multiple cycles of preconditioning in rat hearts. Am J Physiol 1999, 276(4 Pt 2):H1229-H1235.
29. Fryer R.M., Wang Y., Hsu A.K., Nagase H., Gross G.J. Dependence of delta1-opioid receptor-induced cardioprotection on a tyrosine kinase-dependent but not a Src-dependent pathway. J Pharmacol Exp Ther 2001, 299(2):477-482.
30. Germack R., Griffin M., Dickenson J.M. Activation of protein kinase B by adenosine A1 and A3 receptors in newborn rat cardiomyocytes. J Mol Cell Cardiol 2004, 37(5):989-999.
31. Hedayati N., Schomisch S.J., Carino J.L., Timothy Sherwood J., Lesnefsky E.J., Cmolik B.L. Cardioprotection by St Thomas' solution is mediated by protein kinase C and tyrosine kinase. J Surg Res 2003, 113(1):121-127.
32. Htun P., Ito W.D., Hoefer I.E., Schaper J., Schaper W. Intramyocardial infusion of FGF-1 mimics ischemic preconditioning in pig myocardium. J Mol Cell Cardiol 1998, 30(4):867-877.
33. Krenz M., Baines C.P., Heusch G., Downey J.M., Cohen M.V. Acute alcohol-induced protection against infarction in rabbit hearts: differences from and similarities to ischemic preconditioning. J Mol Cell Cardiol 2001, 33(11):2015-2022.
34. Lee S., Chanoit G., McIntosh R., Zvara D.A., Xu Z. Molecular mechanism underlying Akt activation in zinc-induced cardioprotection. Am J Physiol Heart Circ Physiol 2009, 297(2):H569-H575.
35. Liem D.A., Gho C.C., Gho B.C., Kazim S., Manintveld O.C., Verdouw P.D., et al. The tyrosine phosphatase inhibitor bis(maltolato)oxovanadium attenuates myocardial reperfusion injury by opening ATP-sensitive potassium channels. J Pharmacol Exp Ther 2004, 309(3):1256-1262.
36. Okubo S., Tanabe Y., Takeda K., Kitayama M., Kanemitsu S., Kukreja R.C., et al. Pretreatment with tyrosine kinase inhibitor attenuates the reduction of apoptosis 24 h after ischemic preconditioning. Jpn J Physiol 2004, 54(2):143-151.
37. Wang T.L., Huang Y.H., Chang H. Somatostatin analogue mimics acute ischemic preconditioning in a rat model of myocardial infarction. J Cardiovasc Pharmacol 2005, 45(4):327-332.
38. Schwab K., Neumann B., Vignon-Zellweger N., Fischer A., Stein R., Jungblut P.R., et al. Dietary phytoestrogen supplementation induces sex differences in the myocardial protein pattern of mice: a comparative proteomics study. Proteomics 2011, 11(19):3887-3904.
39. Schwab K., Neumann B., Vignon-Zellweger N., Scheler C., Theuring F. Sex specific proteome and phosphoproteome analysis and the effects of phytoestrogens in heart and kidney of mice. 18th scientific meeting of the european-society-of-hypertension, Berlin June, 2008.
40. Schwab K., Neumann B., Scheler C., Jungblut P.R., Theuring F. Adaptation of proteomic techniques for the identification and characterization of protein species from murine heart. Amino Acids 2011, 41(2):401-414.
41. White S.M., Constantin P.E., Claycomb W.C. Cardiac physiology at the cellular level: use of cultured HL-1 cardiomyocytes for studies of cardiac muscle cell structure and function. Am J Physiol Heart Circ Physiol 2004, 286(3):H823-H829.
42. Claycomb W.C., Lanson N.A., Stallworth B.S., Egeland D.B., Delcarpio J.B., Bahinski A., et al. HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc Natl Acad Sci U S A 1998, 95(6):2979-2984.
43. Yan J.X., Wait R., Berkelman T., Harry R.A., Westbrook J.A., Wheeler C.H., et al. A modified silver staining protocol for visualization of proteins compatible with matrix-assisted laser desorption/ionization and electrospray ionization-mass spectrometry. Electrophoresis 2000, 21(17):3666-3672.
44. Eisen M.B., Spellman P.T., Brown P.O., Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 1998, 95(25):14863-14868.
45. Page R.D. TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 1996, 12(4):357-358.
46. Jungblut P.R., Holzhutter H.G., Apweiler R., Schluter H. The speciation of the proteome. Chem Cent J 2008, 2:16.
47. Lim H.A., Kim J.H., Sung M.K., Kim M.K., Park J.H., Kim J.S. Genistein induces glucose-regulated protein 78 in mammary tumor cells. J Med Food 2006, 9(1):28-32.
48. Fu Y., Li J., Lee A.S. GRP78/BiP inhibits endoplasmic reticulum BIK and protects human breast cancer cells against estrogen starvation-induced apoptosis. Cancer Res 2007, 67(8):3734-3740.
49. Reddy R.K., Mao C., Baumeister P., Austin R.C., Kaufman R.J., Lee A.S. Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors: role of ATP binding site in suppression of caspase-7 activation. J Biol Chem 2003, 278(23):20915-20924.
50. Sun Y., Liu G., Song T., Liu F., Kang W., Zhang Y., et al. Upregulation of GRP78 and caspase-12 in diastolic failing heart. Acta Biochim Pol 2008, 55(3):511-516.
51. Thuerauf D.J., Marcinko M., Gude N., Rubio M., Sussman M.A., Glembotski C.C. Activation of the unfolded protein response in infarcted mouse heart and hypoxic cultured cardiac myocytes. Circ Res 2006, 99(3):275-282.
52. Shintani-Ishida K., Nakajima M., Uemura K., Yoshida K. Ischemic preconditioning protects cardiomyocytes against ischemic injury by inducing GRP78. Biochem Biophys Res Commun 2006, 345(4):1600-1605.
53. Pan Y.X., Ren A.J., Zheng J., Rong W.F., Chen H., Yan X.H., et al. Delayed cytoprotection induced by hypoxic preconditioning in cultured neonatal rat cardiomyocytes: role of GRP78. Life Sci 2007, 81(13):1042-1049.
54. Martindale J.J., Fernandez R., Thuerauf D., Whittaker R., Gude N., Sussman M.A., et al. Endoplasmic reticulum stress gene induction and protection from ischemia/reperfusion injury in the hearts of transgenic mice with a tamoxifen-regulated form of ATF6. Circ Res 2006, 98(9):1186-1193.
55. Pan Y.X., Lin L., Ren A.J., Pan X.J., Chen H., Tang C.S., et al. HSP70 and GRP78 induced by endothelin-1 pretreatment enhance tolerance to hypoxia in cultured neonatal rat cardiomyocytes. J Cardiovasc Pharmacol 2004, 44(Suppl. 1):S117-S120.
56. Zhang P.L., Lun M., Teng J., Huang J., Blasick T.M., Yin L., et al. Preinduced molecular chaperones in the endoplasmic reticulum protect cardiomyocytes from lethal injury. Ann Clin Lab Sci 2004, 34(4):449-457.
57. Sanada S., Kitakaze M., Papst P.J., Hatanaka K., Asanuma H., Aki T., et al. Role of phasic dynamism of p38 mitogen-activated protein kinase activation in ischemic preconditioning of the canine heart. Circ Res 2001, 88(2):175-180.
58. Dana A., Skarli M., Papakrivopoulou J., Yellon D.M. Adenosine A(1) receptor induced delayed preconditioning in rabbits: induction of p38 mitogen-activated protein kinase activation and Hsp27 phosphorylation via a tyrosine kinase- and protein kinase C-dependent mechanism. Circ Res 2000, 86(9):989-997.
59. Martin J.L., Mestril R., Hilal-Dandan R., Brunton L.L., Dillmann W.H. Small heat shock proteins and protection against ischemic injury in cardiac myocytes. Circulation 1997, 96(12):4343-4348.
60. Mehlen P., Kretz-Remy C., Preville X., Arrigo A.P. Human hsp27, Drosophila hsp27 and human alphaB-crystallin expression-mediated increase in glutathione is essential for the protective activity of these proteins against TNFalpha-induced cell death. EMBO J 1996, 15(11):2695-2706.
61. Scheler C., Li X.P., Salnikow J., Dunn M.J., Jungblut P.R. Comparison of two-dimensional electrophoresis patterns of heat shock protein Hsp27 species in normal and cardiomyopathic hearts. Electrophoresis 1999, 20(18):3623-3628.
62. Jayakumar J., Suzuki K., Sammut I.A., Smolenski R.T., Khan M., Latif N., et al. Heat shock protein 70 gene transfection protects mitochondrial and ventricular function against ischemia-reperfusion injury. Circulation 2001, 104(12 Suppl 1):I303-I307.
63. Gupta S., Knowlton A.A. HSP60, Bax, apoptosis and the heart. J Cell Mol Med 2005, 9(1):51-58.
64. Hamilton K.L., Gupta S., Knowlton A.A. Estrogen and regulation of heat shock protein expression in female cardiomyocytes: cross-talk with NF kappa B signaling. J Mol Cell Cardiol 2004, 36(4):577-584.
65. Trinklein N.D., Chen W.C., Kingston R.E., Myers R.M. Transcriptional regulation and binding of heat shock factor 1 and heat shock factor 2 to 32 human heat shock genes during thermal stress and differentiation. Cell Stress Chaperones 2004, 9(1):21-28.
66. Chen B., NelsonandY D.M. Sadovsky, N-myc down-regulated gene 1 modulates the response of term human trophoblasts to hypoxic injury. J Biol Chem 2006, 281(5):2764-2772.
67. Salnikow K., Kluz T., Costa M., Piquemal D., Demidenko Z.N., Xie K., et al. The regulation of hypoxic genes by calcium involves c-Jun/AP-1, which cooperates with hypoxia-inducible factor 1 in response to hypoxia. Mol Cell Biol 2002, 22(6):1734-1741.
68. Sekili S., McCay P.B., Li X.Y., Zughaib M., Sun J.Z., Tang L., et al. Direct evidence that the hydroxyl radical plays a pathogenetic role in myocardial "stunning" in the conscious dog and demonstration that stunning can be markedly attenuated without subsequent adverse effects. Circ Res 1993, 73(4):705-723.
69. Arora A., Nair M.G., Strasburg G.M. Antioxidant activities of isoflavones and their biological metabolites in a liposomal system. Arch Biochem Biophys 1998, 356(2):133-141.
70. Siow R.C., Li F.Y., Rowlands D.J., de Winter P., Mann G.E. Cardiovascular targets for estrogens and phytoestrogens: transcriptional regulation of nitric oxide synthase and antioxidant defense genes. Free Radic Biol Med 2007, 42(7):909-925.
71. Mann G.E., Rowlands D.J., Li F.Y., de Winter P., Siow R.C. Activation of endothelial nitric oxide synthase by dietary isoflavones: role of NO in Nrf2-mediated antioxidant gene expression. Cardiovasc Res 2007, 75(2):261-274.
72. Mann G.E., Bonacasa B., Ishii T., Siow R.C. Targeting the redox sensitive Nrf2-Keap1 defense pathway in cardiovascular disease: protection afforded by dietary isoflavones. Curr Opin Pharmacol 2009, 9(2):139-145.
73. Si H., Liu D. Genistein, a soy phytoestrogen, upregulates the expression of human endothelial nitric oxide synthase and lowers blood pressure in spontaneously hypertensive rats. J Nutr 2008, 138(2):297-304.
74. Han R.M., Tian Y.X., Liu Y., Chen C.H., Ai X.C., Zhang J.P., et al. Comparison of flavonoids and isoflavonoids as antioxidants. J Agric Food Chem 2009, 57(9):3780-3785.
75. Severino A., Campioni M., Straino S., Salloum F.N., Schmidt N., Herbrand U., et al. Identification of protein disulfide isomerase as a cardiomyocyte survival factor in ischemic cardiomyopathy. J Am Coll Cardiol 2007, 50(11):1029-1037.
76. Lin L., Anders M.W., Shen S.S. Mitochondrial glutathione protects cardiac myocytes from H2O2-induced apoptosis. 47th annual meeting of the biophysical-society, San Antonio March, 2003.
77. Cheng E.H., Sheiko T.V., Fisher J.K., Craigen W.J., Korsmeyer S.J. VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 2003, 301(5632):513-517.
78. Halestrap A.P., Clarke S.J., Javadov S.A. Mitochondrial permeability transition pore opening during myocardial reperfusion-a target for cardioprotection. Cardiovasc Res 2004, 61(3):372-385.
79. Rostovtseva T.K., Tan W., Colombini M. On the role of VDAC in apoptosis: fact and fiction. J Bioenerg Biomembr 2005, 37(3):129-142.
80. Guo Y., Cheong N., Zhang Z., De Rose R., Deng Y., Farber S.A., et al. Tim50, a component of the mitochondrial translocator, regulates mitochondrial integrity and cell death. J Biol Chem 2004, 279(23):24813-24825.
81. Takayama S., Xie Z., Reed J.C. An evolutionarily conserved family of Hsp70/Hsc70 molecular chaperone regulators. J Biol Chem 1999, 274(2):781-786.
82. Luders J., Demand J., Hohfeld J. The ubiquitin-related BAG-1 provides a link between the molecular chaperones Hsc70/Hsp70 and the proteasome. J Biol Chem 2000, 275(7):4613-4617.
83. Townsend P.A., Cutress R.I., Carroll C.J., Lawrence K.M., Scarabelli T.M., Packham G., et al. BAG-1 proteins protect cardiac myocytes from simulated ischemia/reperfusion-induced apoptosis via an alternate mechanism of cell survival independent of the proteasome. J Biol Chem 2004, 279(20):20723-20728.
84. Roberg K., Ollinger K. Oxidative stress causes relocation of the lysosomal enzyme cathepsin D with ensuing apoptosis in neonatal rat cardiomyocytes. Am J Pathol 1998, 152(5):1151-1156.
85. Fioravanti L., Cappelletti V., Miodini P., Ronchi E., Brivio M., Di Fronzo G. Genistein in the control of breast cancer cell growth: insights into the mechanism of action in vitro. Cancer Lett 1998, 130(1-2):143-152.
86. Spinozzi F., Pagliacci M.C., Migliorati G., Moraca R., Grignani F., Riccardi C., et al. The natural tyrosine kinase inhibitor genistein produces cell cycle arrest and apoptosis in Jurkat T-leukemia cells. Leuk Res 1994, 18(6):431-439.
87. Xiao J.X., Huang G.Q., Geng X., Qiu H.W. Soy-derived isoflavones inhibit HeLa cell growth by inducing apoptosis. Plant Foods Hum Nutr 2011, 66(2):122-128.
88. Mansoor T.A., Ramalho R.M., Luo X., Ramalhete C., Rodrigues C.M., Ferreira M.J. Isoflavones as apoptosis inducers in human hepatoma Huh-7 cells. Phytother Res 2011, 25(12):1819-1824.
89. Stanley W.C., Lopaschuk G.D., Hall J.L., McCormack J.G. Regulation of myocardial carbohydrate metabolism under normal and ischaemic conditions. Potential for pharmacological interventions. Cardiovasc Res 1997, 33(2):243-257.
90. Lopaschuk G.D., Stanley W.C. Glucose metabolism in the ischemic heart. Circulation 1997, 95(2):313-315.
91. He Y., Smith R. Nuclear functions of heterogeneous nuclear ribonucleoproteins A/B. Cell Mol Life Sci 2009, 66(7):1239-1256.
92. Honore B., Baandrup U., Vorum H. Heterogeneous nuclear ribonucleoproteins F and H/H' show differential expression in normal and selected cancer tissues. Exp Cell Res 2004, 294(1):199-209.
93. Zhang D., Tai Y.C., Wong C.H., Tai L.K., Koay E.S., Chen C.S. Molecular response of leukemia HL-60 cells to genistein treatment, a proteomics study. Leuk Res 2007, 31(1):75-82.
94. Seong J.K., Kim D.K., Choi K.H., Oh S.H., Kim K.S., Lee S.S., et al. Proteomic analysis of the cellular proteins induced by adaptive concentrations of hydrogen peroxide in human U937 cells. Exp Mol Med 2002, 34(5):374-378.
95. He B., Feng Q., Mukherjee A., Lonard D.M., DeMayo F.J., Katzenellenbogen B.S., et al. A repressive role for prohibitin in estrogen signaling. Mol Endocrinol 2008, 22(2):344-360.
96. Gamble S.C., Chotai D., Odontiadis M., Dart D.A., Brooke G.N., Powell S.M., et al. Prohibitin, a protein downregulated by androgens, represses androgen receptor activity. Oncogene 2007, 26(12):1757-1768.
97. Vendrell J.A., Magnino F., Danis E., Duchesne M.J., Pinloche S., Pons M., et al. Estrogen regulation in human breast cancer cells of new downstream gene targets involved in estrogen metabolism, cell proliferation and cell transformation. J Mol Endocrinol 2004, 32(2):397-414.
98. Szymanski P.T. Calponin (CaP) as a latch-bridge protein-a new concept in regulation of contractility in smooth muscles. J Muscle Res Cell Motil 2004, 25(1):7-19.
99. Lowenstein E.J., Daly R.J., Batzer A.G., Li W., Margolis B., Lammers R., et al. The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling. Cell 1992, 70(3):431-442.