N-butyl benzyl phthalate promotes breast cancer progression by inducing expression of lymphoid enhancer factor 1

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Hsieh, Tsung Hua ^a   Tsai, Cheng Fang ^a   Hsu, Chia Yi ^a   Kuo, Po Lin ^a,b   Hsi, Edward ^a   Suen, Jau Ling ^a   Hung, Chih Hsing ^c   Lee, Jau Nan ^a,c   Chai, Chee Yin ^a,c   Wang, Shao Chun ^d   Tsai, Eing Mei ^a,c  

^a KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^c KAOHSIUNG MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYMPHOID ENHANCER FACTOR 1; MATRIGEL; MESSENGER RNA; N BUTYL BENZYL PHTHALATE; PHTHALIC ACID DERIVATIVE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BREAST CANCER; CANCER GROWTH; CANCER STEM CELL; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL STRAIN MCF 7; CELL VIABILITY; CHEMICAL CARCINOGENESIS; COMPUTER PROGRAM; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA MICROARRAY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE TARGETING; GENETIC TRANSFECTION; GENOME ANALYSIS; HUMAN; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR VASCULARIZATION; UPREGULATION;

BREAST NEOPLASMS; CELL LINE, TUMOR; CELL SURVIVAL; DISEASE PROGRESSION; DNA, COMPLEMENTARY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOME, HUMAN; HUMANS; LYMPHOID ENHANCER-BINDING FACTOR 1; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHTHALIC ACIDS; RNA; SIGNAL TRANSDUCTION; TETRAZOLIUM SALTS; WOUND HEALING;

EID: 84864697428     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042750     Document Type: Article

References (51)

1. Janjua NR, Mortensen GK, Andersson AM, Kongshoj B, Skakkebaek NE, et al. (2007) Systemic uptake of diethyl phthalate, dibutyl phthalate, and butyl paraben following whole-body topical application and reproductive and thyroid hormone levels in humans. Environ Sci Technol 41: 5564-5570.
2. Wormuth M, Scheringer M, Vollenweider M, Hungerbuhler K, (2006) What are the sources of exposure to eight frequently used phthalic acid esters in Europeans? Risk Anal 26: 803-824.
3. Lopez-Carrillo L, Hernandez-Ramirez RU, Calafat AM, Torres-Sanchez L, Galvan-Portillo M, et al. (2010) Exposure to phthalates and breast cancer risk in northern Mexico. Environ Health Perspect 118: 539-544.
4. Huang PC, Tsai EM, Li WF, Liao PC, Chung MC, et al. (2010) Association between phthalate exposure and glutathione S-transferase M1 polymorphism in adenomyosis, leiomyoma and endometriosis. Hum Reprod 25: 986-994.
5. Moore NP, (2000) The oestrogenic potential of the phthalate esters. Reprod Toxicol 14: 183-192.
6. Ma M, Kondo T, Ban S, Umemura T, Kurahashi N, et al. (2006) Exposure of prepubertal female rats to inhaled di(2-ethylhexyl)phthalate affects the onset of puberty and postpubertal reproductive functions. Toxicol Sci 93: 164-171.
7. Jobling S, Reynolds T, White R, Parker MG, Sumpter JP, (1995) A variety of environmentally persistent chemicals, including some phthalate plasticizers, are weakly estrogenic. Environ Health Perspect 103: 582-587.
8. Harris CA, Henttu P, Parker MG, Sumpter JP, (1997) The estrogenic activity of phthalate esters in vitro. Environ Health Perspect 105: 802-811.
9. Hsieh TH, Tsai CF, Hsu CY, Kuo PL, Lee JN, et al. (2011) Phthalates induce proliferation and invasiveness of estrogen receptor-negative breast cancer through the AhR/HDAC6/c-Myc signaling pathway. FASEB J.
10. Kim IY, Han SY, Moon A, (2004) Phthalates inhibit tamoxifen-induced apoptosis in MCF-7 human breast cancer cells. J Toxicol Environ Health A 67: 2025-2035.
11. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF, (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100: 3983-3988.
12. Wang KH, Kao AP, Chang CC, Lee JN, Chai CY, et al. (2010) Modulation of tumorigenesis and oestrogen receptor-alpha expression by cell culture conditions in a stem cell-derived breast epithelial cell line. Biol Cell 102: 159-172.
13. Patrawala L, Calhoun T, Schneider-Broussard R, Zhou J, Claypool K, et al. (2005) Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2- cancer cells are similarly tumorigenic. Cancer Res 65: 6207-6219.
14. Alfranca A, Lopez-Oliva JM, Genis L, Lopez-Maderuelo D, Mirones I, et al. (2008) PGE2 induces angiogenesis via MT1-MMP-mediated activation of the TGFbeta/Alk5 signaling pathway. Blood 112: 1120-1128.
15. Zhang Y, Daaka Y, (2011) PGE2 promotes angiogenesis through EP4 and PKA Cgamma pathway. Blood 118: 5355-5364.
16. Kamiyama M, Pozzi A, Yang L, DeBusk LM, Breyer RM, et al. (2006) EP2, a receptor for PGE2, regulates tumor angiogenesis through direct effects on endothelial cell motility and survival. Oncogene 25: 7019-7028.
17. Platet N, Cathiard AM, Gleizes M, Garcia M, (2004) Estrogens and their receptors in breast cancer progression: a dual role in cancer proliferation and invasion. Crit Rev Oncol Hematol 51: 55-67.
18. May CD, Sphyris N, Evans KW, Werden SJ, Guo W, et al. (2011) Epithelial-mesenchymal transition and cancer stem cells: a dangerously dynamic duo in breast cancer progression. Breast Cancer Res 13: 202.
19. Sharma MR, Koltowski L, Ownbey RT, Tuszynski GP, Sharma MC, (2006) Angiogenesis-associated protein annexin II in breast cancer: selective expression in invasive breast cancer and contribution to tumor invasion and progression. Exp Mol Pathol 81: 146-156.
20. Strizzi L, Postovit LM, Margaryan NV, Seftor EA, Abbott DE, et al. (2008) Emerging roles of nodal and Cripto-1: from embryogenesis to breast cancer progression. Breast Dis 29: 91-103.
21. Leushacke M, Sporle R, Bernemann C, Brouwer-Lehmitz A, Fritzmann J, et al. (2011) An RNA interference phenotypic screen identifies a role for FGF signals in colon cancer progression. PLoS One 6: e23381.
22. Merkle D, Hoffmann R, (2011) Roles of cAMP and cAMP-dependent protein kinase in the progression of prostate cancer: cross-talk with the androgen receptor. Cell Signal 23: 507-515.
23. Konno H, Ohta M, Baba M, Suzuki S, Nakamura S, (2003) The role of circulating IL-8 and VEGF protein in the progression of gastric cancer. Cancer Sci 94: 735-740.
24. Carvalho I, Milanezi F, Martins A, Reis RM, Schmitt F, (2005) Overexpression of platelet-derived growth factor receptor alpha in breast cancer is associated with tumour progression. Breast Cancer Res 7: R788-795.
25. Obermair A, Kucera E, Mayerhofer K, Speiser P, Seifert M, et al. (1997) Vascular endothelial growth factor (VEGF) in human breast cancer: correlation with disease-free survival. Int J Cancer 74: 455-458.
26. Buteau-Lozano H, Velasco G, Cristofari M, Balaguer P, Perrot-Applanat M, (2008) Xenoestrogens modulate vascular endothelial growth factor secretion in breast cancer cells through an estrogen receptor-dependent mechanism. J Endocrinol 196: 399-412.
27. Zoller M, (2011) CD44: can a cancer-initiating cell profit from an abundantly expressed molecule? Nat Rev Cancer 11: 254-267.
28. Kang KS, Sun W, Nomata K, Morita I, Cruz A, et al. (1998) Involvement of tyrosine phosphorylation of p185(c-erbB2/neu) in tumorigenicity induced by X-rays and the neu oncogene in human breast epithelial cells. Mol Carcinog 21: 225-233.
29. Tai MH, Chang CC, Kiupel M, Webster JD, Olson LK, et al. (2005) Oct4 expression in adult human stem cells: evidence in support of the stem cell theory of carcinogenesis. Carcinogenesis 26: 495-502.
30. Hsieh TH, Tsai CF, Hsu CY, Kuo PL, Lee JN, et al. (2012) Phthalates stimulate the epithelial to mesenchymal transition through an HDAC6-dependent mechanism in human breast epithelial stem cells. Toxicol Sci.
31. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, et al. (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715.
32. Morel AP, Lievre M, Thomas C, Hinkal G, Ansieau S, et al. (2008) Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One 3: e2888.
33. Polyak K, Weinberg RA, (2009) Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 9: 265-273.
34. Morimoto K, Kim SJ, Tanei T, Shimazu K, Tanji Y, et al. (2009) Stem cell marker aldehyde dehydrogenase 1-positive breast cancers are characterized by negative estrogen receptor, positive human epidermal growth factor receptor type 2, and high Ki67 expression. Cancer Sci 100: 1062-1068.
35. Charafe-Jauffret E, Ginestier C, Iovino F, Wicinski J, Cervera N, et al. (2009) Breast cancer cell lines contain functional cancer stem cells with metastatic capacity and a distinct molecular signature. Cancer Res 69: 1302-1313.
36. Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, et al. (2005) Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 65: 5506-5511.
37. Fillmore CM, Gupta PB, Rudnick JA, Caballero S, Keller PJ, et al. (2010) Estrogen expands breast cancer stem-like cells through paracrine FGF/Tbx3 signaling. Proc Natl Acad Sci U S A 107: 21737-21742.
38. Barbieri F, Wurth R, Ratto A, Campanella C, Vito G, et al. (2012) Isolation of stem-like cells from spontaneous feline mammary carcinomas: phenotypic characterization and tumorigenic potential. Exp Cell Res 318: 847-860.
39. Ao A, Morrison BJ, Wang H, Lopez JA, Reynolds BA, et al. (2011) Response of estrogen receptor-positive breast cancer tumorspheres to antiestrogen treatments. PLoS One 6: e18810.
40. Rhodes LV, Antoon JW, Muir SE, Elliott S, Beckman BS, et al. (2010) Effects of human mesenchymal stem cells on ER-positive human breast carcinoma cells mediated through ER-SDF-1/CXCR4 crosstalk. Mol Cancer 9: 295.
41. Love JJ, Li X, Case DA, Giese K, Grosschedl R, et al. (1995) Structural basis for DNA bending by the architectural transcription factor LEF-1. Nature 376: 791-795.
42. Teng Y, Wang X, Wang Y, Ma D, (2010) Wnt/beta-catenin signaling regulates cancer stem cells in lung cancer A549 cells. Biochem Biophys Res Commun 392: 373-379.
43. Bisson I, Prowse DM, (2009) WNT signaling regulates self-renewal and differentiation of prostate cancer cells with stem cell characteristics. Cell Res 19: 683-697.
44. Ray S, Xu F, Wang H, Das SK, (2008) Cooperative control via lymphoid enhancer factor 1/T cell factor 3 and estrogen receptor-alpha for uterine gene regulation by estrogen. Mol Endocrinol 22: 1125-1140.
45. Wang SH, Nan KJ, Wang YC, (2009) Endothelial cells promote the proliferation of lymphocytes partly through the Wnt pathway via LEF-1. Biochem Biophys Res Commun 388: 67-72.
46. Nguyen A, Rosner A, Milovanovic T, Hope C, Planutis K, et al. (2005) Wnt pathway component LEF1 mediates tumor cell invasion and is expressed in human and murine breast cancers lacking ErbB2 (her-2/neu) overexpression. Int J Oncol 27: 949-956.
47. Eger A, Stockinger A, Schaffhauser B, Beug H, Foisner R, (2000) Epithelial mesenchymal transition by c-Fos estrogen receptor activation involves nuclear translocation of beta-catenin and upregulation of beta-catenin/lymphoid enhancer binding factor-1 transcriptional activity. J Cell Biol 148: 173-188.
48. Kim K, Lu Z, Hay ED, (2002) Direct evidence for a role of beta-catenin/LEF-1 signaling pathway in induction of EMT. Cell Biol Int 26: 463-476.
49. Mei JM, Hord NG, Winterstein DF, Donald SP, Phang JM, (2000) Expression of prostaglandin endoperoxide H synthase-2 induced by nitric oxide in conditionally immortalized murine colonic epithelial cells. FASEB J 14: 1188-1201.
50. Marchenko ND, Marchenko GN, Weinreb RN, Lindsey JD, Kyshtoobayeva A, et al. (2004) Beta-catenin regulates the gene of MMP-26, a novel metalloproteinase expressed both in carcinomas and normal epithelial cells. Int J Biochem Cell Biol 36: 942-956.
51. Gustavson MD, Crawford HC, Fingleton B, Matrisian LM, (2004) Tcf binding sequence and position determines beta-catenin and Lef-1 responsiveness of MMP-7 promoters. Mol Carcinog 41: 125-139.