Morphologic transformation of human breast epithelial cells MCF-10A: dependence on an oxidative microenvironment and estrogen/epidermal growth factor receptors

Cancer Cell International

Volumn 10, Issue , 2010, Pages

  Yusuf, Rita ^a,c   Frenkel, Krystyna ^b  

^a INDEPENDENT UNIVERSITY   (Bangladesh)

^b PHL ^*  (Bangladesh)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; HYDROCORTISONE; PHENOLSULFONPHTHALEIN;

ARTICLE; CELL TRANSFORMATION; CONTROLLED STUDY; EPITHELIUM CELL; ESTROGEN THERAPY; GENE EXPRESSION; GENETIC ANALYSIS; HUMAN; HUMAN CELL; MICROENVIRONMENT; OXIDATIVE STRESS; WESTERN BLOTTING;

EID: 77956484003     PISSN: None     EISSN: 14752867     Source Type: Journal    
DOI: 10.1186/1475-2867-10-30     Document Type: Article

References (77)

1. Gullick JW, Bianco C, Normanno N, Martinez-Lacacia I, De Santis M, Ebert AD, Salomon DS. Growth factors and their receptors: a novel approach to the endocrinology of human breast cancer. Women and Cancer 1998, 1:29-57.
2. Ohshima H, Bartsche H. Chronic infections and inflammatory processes as cancer risk factors: possible role of nitric oxide in carcinogenesis. Mutation Res 1994, 305:253-256.
3. Li Y, Trush MA, Yager JD. DNA damage caused by reactive oxygen species originating from a copper-dependent oxidation of the 2-hydroxy catechol of estradiol. Carcinogenesis 1994, 15:1421-1427. 10.1093/carcin/15.7.1421, 8033320.
4. Yager JD. Endogenous estrogens as carcinogens through metabolic activation. J Natl Cancer Inst 2000, 27:67-73.
5. Hayashi N, Hasegawa K, Komine A, Tanaka Y, McLachlan JA, Barrett JC, Tsutsui T. Estrogen-induced cell transformation and DNA adduct formation in cultured Syrian hamster embryo cells. Mol Carcinogenesis 1996, 16:149-156.
6. Bolton JL, Thatcher GRJ. Potential mechanisms of estrogen quinone carcinogenesis. Chem Res Toxicol 2008, 21(1):93-101. 10.1021/tx700191p, 2556295, 18052105.
7. Hamada J, Nakata D, Nakae D, Kobayashi Y, Akai H, Konishi Y, Okada F, Shibata T, Hosokawa M, Moriuchi T. Increased oxidative DNA damage in mammary tumor cells by continuous epidermal growth factor stimulation. J Natl Cancer Inst 2001, 93:214-219. 10.1093/jnci/93.3.214, 11158190.
8. Arnold RS, Shi J, Murad E, Whalen AM, Sun CQ, Polavarapu R, Parthasarathy S, Petros JA, Lambeth JD. Hydrogen peroxide mediates the cell growth and transformation caused by the mitogenic oxidase Nox1. Proc Natl Acad Sci 2001, 98:5550-5555. 10.1073/pnas.101505898, 33250, 11331784.
9. Fishman J, Osborne MP, Telang NT. The role of estrogen in mammary carcinogenesis. Ann NY Acad Sci 1995, 768:91-100. 10.1111/j.1749-6632.1995.tb12113.x, 8526389.
10. Dickson RB, Stancel GM. Estrogen receptor-mediated processes in normal and cancer cells. J Natl Cancer Inst 2000, 27:135-145,.
11. Tsutsui T, Barrett CJ. Neoplastic transformation of cultured mammalian cells by estrogens and estrogen-like chemicals. Environ Health Perspect Suppl 1997, 105:619-624.
12. Normanno N, Ciardiello F. EGF-related peptides in the pathophysiology of the mammary gland. J. Mammary Gland Biol. Neoplasia 1997, 2:143-151.
13. Cormier EM, Wolf MF, Jordan VC. Decrease in estradiol-stimulated progesterone receptor production in MCF-7 cells by epidermal growth factor and possible clinical implication for paracrine-regulated breast cancer growth. Cancer Res 1989, 49(3):576-580.
14. Stoica A, Saceda M, Doraiswamy VL, Coleman C. Regulation of estrogen receptor-α gene expression by epidermal growth factor. J Endocrinol 2000, 165(2):371-378. 10.1677/joe.0.1650371, 10810301.
15. Clemons M, Goss P. Estrogen and the risk of breast cancer. N Engl J Med 2001, 344:276-285. 10.1056/NEJM200101253440407, 11172156.
16. Fuqua SAW, Russo J, Shackney SE, Stearns ME. Estrogen, estrogen receptors and selective estrogen receptor modulators in human breast cancer. Women and Cancer 2000, 2:21-32.
17. Khan SA, Sachdeva A, Naim S, Meguid MM, Marx W, Simon H, Halverson JD, Numann PJ. The normal breast epithelium of women with breast cancer displays an aberrant response to estradiol. Cancer Epidemiol. Biomarkers & Prev 1999, 8:867-872.
18. Shoker BS, Jarvis C, Clarke RB, Anderson E, Hewlett J, Davies MPA, Sibson DR, Sloane JP. Estrogen receptor-positive proliferating cells in the normal and pre-cancerous breast. Amer J Pathol 1999, 155:1811-1815.
19. Cavalieri E, Rogan E. The unifying mechanism in the initiation and prevention of breast and other cancers. BMC Proceedings 2009, 3(Suppl 5):S8.
20. Russo J, Russo IH. The role of estrogen in the initiation of breast cancer. J Steroid Biochem Mol Biol 2006, 102:89-96,. 10.1016/j.jsbmb.2006.09.004, 1832080, 17113977.
21. Russo IH, Russo J. Role of hormones in mammary cancer initiation and progression. J Mammary Gland Biol Neoplasia 1998, 3:49-61. 10.1023/A:1018770218022, 10819504.
22. Cavalieri E, Chakravarti D, Guttenplan J, Hart E, Ingle J, Jankowiak R, Muti P, Rogan E, Russo J, Santen R, Sutter T. Catechol estrogen quinones as initiators of breast and other human cancers: Implications for biomarkers of susceptibility and cancer prevention. Biochim Biophys Acta 2006, 1766:63-78.
23. Fernandez SV, Russo IH, Russo J. Estradiol and its metabolites 4-hydroxyestradiol and 2-hydroxyestradiol induce mutations in human breast epithelial cells. Int J Cancer 2006, 118:1862-1868. 10.1002/ijc.21590, 16287077.
24. Mense SM, Remotti F, Bhan A, Singh B, El-Tamer M, Hei TK, Bhat H. Estrogen-induced breast cancer: alterations in breast morphology and oxidative stress as a function of estrogen exposure. Toxicol Appl Pharmacol 2008, 232(1):78-85. 10.1016/j.taap.2008.06.007, 2593408, 18640140.
25. Liehr JG. 2-Fluoroestradiol, separation of estrogenicity from carcinogenicity. Mol Pharmacol 1983, 23(2):278-281.
26. Liehr JG, Stancel GM, Chorich LP, Bousfield GR, Ulubelen AA. Hormonal carcinogenesis: separation of estrogenicity from carcinogenicity. Chem Biol Interact 1986, 59(2):173-184. 10.1016/S0009-2797(86)80064-3, 3769051.
27. Liehr JG. Dual role of oestrogens as hormones and pro-carcinogens: tumour initiation by metabolic activation of oestrogens. Eur J Cancer Prev 1997, 6:3-10. 10.1097/00008469-199702000-00002, 9161806.
28. Han X, Liehr JG. 8-hydroxylation of guanine bases in kidney and liver DNA of hamsters treated with estradiol: role of free radicals in estrogen-induced carcinogenesis. Cancer Res 1994, 54:5515-5517.
29. Liehr JG, Ricci MJ. 4-Hydroxylation of estrogens as marker of human mammary tumors. Proc Natl Acad Sci 1996, 93:3294-3296. 10.1073/pnas.93.8.3294, 39600, 8622931.
30. Musarrat J, Arezina-Wilson J, Wani AA. Prognostic and aetiological relevance of 8-hydroxyguanosine in human breast carcinogenesis. Eur J Cancer 1996, 32A:1209-1214. 10.1016/0959-8049(96)00031-7, 8758255.
31. Anderson D, Schmid TE, Baumgartner A, Cemeli-Carratala E, Brinkworth MH, Wood JM. Oestrogenic compounds and oxidative stress (in human sperm and lymphocytes in the Comet assay). Mutat Res 2003, 544:173-178. 10.1016/j.mrrev.2003.06.016, 14644319.
32. Berthois Y, Katzenellenbogen JA, Katzenellenbogen BS. Phenol red in tissue culture media is a weak estrogen: implications concerning the study of estrogen-responsive cells in culture. Proc Natl Acad Sci USA 1986, 83(8):2496-2500. 10.1073/pnas.83.8.2496, 323325, 3458212.
33. Rajendran KG, Lopez T, Parikh I. Estrogenic effect of phenol red in MCF-7 cells is achieved through activation of estrogen receptor by interacting with a site distinct from the steroid binding site. Biochem Biophys Res Commun 1987, 142(3):724-731. 10.1016/0006-291X(87)91474-4, 3827898.
34. Grenman SE, Van Dyke DL, Worsham MJ, England B, McClatchey KD, Hopkins M, Babu VR, Grenman R, Carey TE. Phenotypic characterization, karyotype analysis and in vitro tamoxifen sensitivity of new ER-negative vulvar carcinoma cell lines, UM-SCV-1A and UM-SCV-1B. Int J Cancer 1990, 45(5):920-927. 10.1002/ijc.2910450524, 2335395.
35. El-Zarruk AA, van den Berg HW. The antiproliferative effects of tyrosine kinase inhibitors towards tamoxifen-sensitive and tamoxifen-resistant human breast cancer cell lines in relation to the expression of epidermal growth factor receptors (EGF-R) and the inhibition of EGF-R tyrosine kinase. Cancer Lett 1999, 142:185-193. 10.1016/S0304-3835(99)00167-6, 10463775.
36. Armelin MCS, Stocco RC, Armelin HA. Control of rat C6 glioma cell proliferation: uncoupling of the inhibitory effects of hydrocortisone hormone in suspension and monolayer cultures. J Cell Biol 2004, 97:455-458.
37. Valentini SR, Oliveira ML, Sasahara RM, Armelin MC. Glucocorticoid-regulated gene in transformed to normal phenotypic reversion. Braz J Med Biol Res 1994, 27(2):541-546.
38. Stanulis-Praeger BM, Jacobus CH, Nuttall AE. Hydrocortisone modulates RA-induced growth inhibition of normal and transformed human embryonic lung fibroblasts. Nutr Cancer 1986, 8(3):171-184. 10.1080/01635588609513891, 3016668.
39. Dandona P, Thusu K, Hafeez R, Abdel-Rahman E, Chaudhuri A. Effect of hydrocortisone on oxygen free radical generation by mononuclear cells. Metabolism 1998, 47(7):788-791. 10.1016/S0026-0495(98)90113-5, 9667222.
40. Marumo T, Schini-Kerth VB, Brandes RP, Busse R. Glucocorticoids inhibit superoxide anion production and p22 phox mRNA expression in human aortic smooth muscle cells. Hypertension 1998, 32:1083-1088.
41. Dandona P, Aljada A, Ghanim H, Mohanty P, Hamouda W, Al-Haddad W. Acute suppressive effect of hydrocortisone on p47phox subunit of nicotinamide adenine dinucleotide phosphate oxidase. Metabolism 2001, 50(5):548-552. 10.1053/meta.2001.22511, 11319715.
42. Okada Y, Okada M. Effect of a radical scavenger "water soluble protein" from broad beans (Vicia faba) on antioxidant enzyme activity in cellular aging. J Nutr Sci Vitaminol (Tokyo) 2000, 46(1):1-16.
43. Lieberthal W, Triaca V, Koh JS, Pagano PJ, Levine JS. Role of superoxide in apoptosis induced by growth factor withdrawal. Am J Physiol 1998, 275(Renal Physiol 44):F691-F702.
44. Briand P, Nielsen KV, Madsen MW, Petersen OW. Trisomy 7p and malignant transformation of human breast epithelial cells following epidermal growth factor withdrawal. Cancer Res 1996, 56:2039-2044.
45. Briand P, Lykkesfeldt AE. An in vitro model of human breast carcinogenesis: epigenetic aspects. Breast Cancer Res Treat 2001, 65:179-187. 10.1023/A:1006434503061, 11261834.
46. Manni A, Wechter R, Verderame MF, Mauger D. Cooperativity between the polyamine pathway and HER-2neu in transformation of human mammary epithelial cells in culture: role of the MAPK pathway. Int J Cancer 1998, 76:563-570. 10.1002/(SICI)1097-0215(19980518)76:4<563::AID-IJC20>3.0.CO;2-7, 9590135.
47. Russo J, Calaf G, Sohi N, Tahin Q, Zhang PL, Alvarado ME, Estrada S, Russo IH. Critical steps in breast carcinogenesis. Ann New York Acad Sci 1993, 698:1-20.
48. Mangold KA, Hubchak S, Mangino MM, Laconi S, Scarpelli DG. In vitro carcinogenesis of hamster pancreatic duct cells: cellular and molecular alterations. Carcinogenesis 1994, 15(9):1979-1984. 10.1093/carcin/15.9.1979, 7923593.
49. Burdick AD, Davis II JW, Liu KJ, Hudson LG, Shi H, Monske ML, Burchiel SW. Benzo(a)pyrene quinones increase cell proliferation, generate reactive oxygen species, and transactivate the epidermal growth factor receptor in breast epithelial cells. Cancer Res 2003, 63:7825-7833.
50. Stalford AC, Maggs JL, Gilchrist TL, Park BK. Catecholestrogens as mediators of carcinogenesis: correlation of aromatic hydroxylation of estradiol and its fluorinated analogs with tumor induction in Syrian hamsters. Mol Pharmacol 1994, 45(6):1259-1267.
51. Cavalieri E, Frenkel K, Liehr JG, Rogan E, Roy D. Estrogens as endogenous genotoxic agents--DNA adducts and mutations. J Natl Cancer Inst 2000, 27:75-93.
52. Tritscher AM, Seacat AM, Yager JD, Groopman JD, Miller BD, Bell D, Sutter TR, Lucier GW. Increased oxidative DNA damage in livers of 2,3,7,8-tetrachlorodibenzo-p-dioxin treated intact but not ovariectomized rats. Cancer Lett 1996, 98:219-225.
53. Dong XF, Berthois Y, Martin PM. Effect of epidermal growth factor on the proliferation of human epithelial cancer cell lines: correlation with the level of occupied EGF receptor. Anticancer Res 1991, 11(2):737-743.
54. Vorherr H. Pregnancy and lactation in relation to breast cancer risk. Semin Perinatol 1979, 3(3):299-311.
55. Lipsett MB. Hormones, medication, and cancer. Cancer 1983, 51(12 Suppl):2426-2429. 10.1002/1097-0142(19830615)51:12+<2426::AID-CNCR2820511307>3.0.CO;2-C, 6850519.
56. Erwin RA, Kirken RA, Malabarba MG, Farrar WL, Rui H. Prolactin activates Ras via signaling proteins SHC, growth factor receptor bound 2, and son of sevenless. Endocrinology 1995, 136(8):3512-3518,. 10.1210/en.136.8.3512, 7628388.
57. Arendt LM, Grafwallner-Huseth TL, Schuler LA. Prolactin-growth factor crosstalk reduces mammary estrogen responsiveness despite elevated ERα expression. Am J Pathol 2009, 174(3):1065-1074. 10.2353/ajpath.2009.080719, 2665765, 19179608.
58. Lydon JP, Ge G, Kittrell FS, Medina D, O'Malley BW. Murine mammary gland carcinogenesis is critically dependent on progesterone receptor function. Cancer Res 1999, 59(17):4276-4284.
59. Anderson E. The role of oestrogen and progesterone receptors in human mammary development and tumorigenesis. Breast Cancer Res 2002, 4:197-201. 10.1186/bcr452, 138744, 12223124.
60. Kurebayashi J, Otsuki T, Moriya T, Sonoo H. Hypoxia reduces responsiveness of human breast cancer cells. Jpn J Cancer Res 2001, 92(10):1093-1101.
61. Tamir S, Izrael S, Vaya J. The effect of oxidative stress on ERα and ERβ expression. J Steroid Biochem Mol Biol 2002, 81:327-332. 10.1016/S0960-0760(02)00115-2, 12361722.
62. Ohnishi A, Oda Y, Hayakawa Y. Characterization of receptors of insect cytokine, growth-blocking peptide, in human keratinocyte and insect Sf9 cells. J Biol Chem 2001, 276(41):37974-37979.
63. Pietras RJ. Interactions between estrogen and growth factor receptors in human breast cancers and the tumor-associated vasculature. Breast J 2003, 9(5):361-373. 10.1046/j.1524-4741.2003.09510.x, 12968955.
64. Marquez DC, Lee J, Lin T, Pietras RJ. Epidermal growth factor receptor and tyrosine phosphorylation of estrogen receptor. Endocrine 2001, 16(2):73-81. 10.1385/ENDO:16:2:073, 11887937.
65. Banerjee S, Sengupta K, Saxena NK, Dhar K, Banerjee SK. Epidermal growth factor induces WISP-2/CCN5 expression in estrogen receptor-α positive breast tumor cells through multiple molecular cross-talks. Mol Cancer Res 2005, 3(3):151-162. 10.1158/1541-7786.MCR-04-0130, 15798095.
66. Pietras R, Marquez DC, Chen H, Tsai E, Weinberg O, Fishbein M. Estrogen and growth factor receptor interactions in human breast and non-small cell lung cancer cells. Steroids 2005, 70:372-381. 10.1016/j.steroids.2005.02.017, 15862820.
67. Zhu Y, Sullivan LL, Nair SS, Williams CC, Pandey AK, Marrero L, Vadlamudi RK, Jones FE. Coregulation of estrogen receptor by ERBB4/HER4 establishes a growth-promoting autocrine signal in breast tumor cells. Cancer Res 2006, 66(16):7991-7998. 10.1158/0008-5472.CAN-05-4397, 16912174.
68. Boerner JL, Gibson MA, Fox EM, Posner ED, Parsons SJ, Silva CM, Shupnik MA. Estrogen negatively regulates epidermal growth factor (EGF)-mediated signal transducer and activator of transcription 5 signaling in human EGF family receptor-overexpressing breast cancer cells. Mol Endocrinol 2005, 19(11):2660-2670. 10.1210/me.2004-0439, 15976008.
69. Levin ER. Bidirectional signaling between the estrogen receptor and the epidermal growth factor receptor. Mol Endocrinol 2003, 17(3):309-317. 10.1210/me.2002-0368, 12554774.
70. Razandi M, Pedram A, Park ST, Levin ER. Proximal events in signaling by plasma membrane estrogen receptors. J Biol Chem 2003, 278(4):2701-2712. 10.1074/jbc.M205692200, 12421825.
71. Filardo EJ. Epidermal growth factor receptor (EGFR) transactivation by estrogen via the G-protein-coupled receptor, GPR30: a novel signaling pathway with potential significance for breast cancer. J Steroid Biochem Mol Biol 2002, 80:231-238. 10.1016/S0960-0760(01)00190-X, 11897506.
72. Lichtner RB. Estrogen/EGF receptor interactions in breast cancer: rationale for new therapeutic combination strategies. Biomed Pharmacother 2003, 57:447-451. 10.1016/j.biopha.2003.09.006, 14637387.
73. Hiraku Y, Yamashita N, Nishiguchi M, Kawanishi S. Catechol estrogens induce oxidative DNA damage and estradiol enhances proliferation. Int J Cancer 2001, 92:333-337. 10.1002/ijc.1193, 11291067.
74. Russo J, Lareef MH, Balogh G, Guo S, Russo IH. Estrogen and its metabolites are carcinogenic agents in human breast epithelial cells. J Steroid Biochem Mol Biol 2003, 87:1-25,. 10.1016/S0960-0760(03)00390-X, 14630087.
75. Rustom A, Saffrich R, Markovic I, Walther P, Gerdes H. Nanotubular highways for intercellular organelle transport. Science 2004, 303:1007-1010. 10.1126/science.1093133, 14963329.
76. Lippman ME, Krueger KA, Eckert S, Sashegyi A, Walls EL, Jamal S, Cauley JA, Cummings SR. Indicators of lifetime estrogen exposure: effect on breast cancer incidence and interaction with raloxifene therapy in the multiple outcomes of raloxifene evaluation study participants. J Clin Oncol 2001, 19(12):3111-3116.
77. Clamp A, Danson S, Clemons M. Hormonal risk factors for breast cancer: identification, chemoprevention, and other intervention strategies. Lancet Oncol 2002, 3(10):611-619. 10.1016/S1470-2045(02)00875-6, 12372723.