Effects of atrazine on estrogen receptor α– and G protein–coupled receptor 30–mediated signaling and proliferation in cancer cells and cancer-associated fibroblasts

Environmental Health Perspectives

Volumn 123, Issue 5, 2015, Pages 493-499

  Albanito, Lidia ^a   Lappano, Rosamaria ^a   Madeo, Antonio ^a   Chimento, Adele ^a   Prossnitz, Eric R ^b,c   Cappello, Anna Rita ^a   Dolce, Vincenza ^a   Abonante, Sergio ^a   Pezzi, Vincenzo ^a   Maggiolini, Marcello ^a  

^a UNIVERSITY OF CALABRIA   (Italy)

^b UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATRAZINE; ESTROGEN RECEPTOR ALPHA; G PROTEIN COUPLED RECEPTOR 30; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN C FOS; G PROTEIN COUPLED RECEPTOR;

ARTICLE; BREAST CANCER CELL LINE; CANCER GROWTH; CELL CYCLE; CELL MIGRATION ASSAY; CELL PROLIFERATION ASSAY; CONTROLLED STUDY; DRUG EFFECT; FIBROBLAST; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LUCIFERASE ASSAY; NEOPLASM; ONCOGENE SRC; OVARIAN CANCER CELL LINE; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RECEPTOR BINDING ASSAY; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSACTIVATION ASSAY; TUMOR ASSOCIATED FIBROBLAST; TUMOR MICROENVIRONMENT; UPREGULATION; WESTERN BLOTTING; CELL MOTION; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; METABOLISM; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ATRAZINE; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; ESTROGEN RECEPTOR ALPHA; FIBROBLASTS; HUMANS; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 84929484212     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.1408586     Document Type: Article

References (41)

1. Albanito L, Madeo A, Lappano R, Vivacqua A, Rago V, Carpino A, et al. 2007. G protein-coupled receptor 30 (GPR30) mediates gene expression changes and growth response to 17β-estradiol and selective GPR30 ligand G-1 in ovarian cancer cells. Cancer Res 67:1859–1866.
2. Bhowmick NA, Neilson EG, Moses HL. 2004. Stromal fibroblasts in cancer initiation and progression. Nature 432:332–337.
3. Bulayeva NN, Watson CS. 2004. Xenoestrogen-induced ERK-1 and ERK-2 activation via multiple membraneinitiated signaling pathways. Environ Health Perspect 112:1481–1487; doi:10.1289/ehp.7175.
4. Bunone G, Briand PA, Miksicek RJ, Picard D. 1996. Activation of the unliganded estrogen receptor by EGF involves the MAP kinase pathway and direct phosphorylation. EMBO J 15:2174–2183.
5. Connor K, Howell J, Chen I, Liu H, Berhane K, Sciarretta C, et al. 1996. Failure of chloro-S-triazinederived compounds to induce estrogen receptormediated responses in vivo and in vitro. Fundam Appl Toxicol 30:93–101.
6. Cooper RL, Laws SC, Das PC, Narotsky MG, Goldman JM, Tyrey EL, et al. 2007. Atrazine and reproductive function: mode and mechanism of action studies. Birth Defects Res B Dev Reprod Toxicol 80:98–112.
7. Davidson IWF. 1988. Metabolism and Kinetics of Atrazine in Man. Winston-Salem, NC:Department of Pysiology/Pharmacology, Bowman Gray School of Medicine. Submitted to the World Health Organization by Syngenta Crop Protection AG.
8. Di Domenico M, Castoria G, Bilancio A, Migliaccio A, Auricchio F. 1996. Estradiol activation of human colon carcinoma-derived Caco-2 cell growth. Cancer Res 56:4516–4521.
9. Donna A, Crosignani P, Robutti F, Betta PG, Bocca R, Mariani N, et al. 1989. Triazine herbicides and ovarian epithelial neoplasms. Scand J Work Environ Health 15:47–53.
10. Dudek P, Picard D. 2008. Genomics of signaling crosstalk of estrogen receptor α in breast cancer cells. PLoS One 3:e1859; doi:10.1371/journal.pone.0001859.
11. Gammon DW, Aldous CN, Carr WC Jr, Sanborn JR, Pfeifer KF. 2005. A risk assessment of atrazine use in California: human health and ecological aspects. Pest Manag Sci 61:331–355.
12. Kettles MK, Browning SR, Prince TS, Horstman SW. 1997. Triazine herbicide exposure and breast cancer incidence: an ecologic study of Kentucky counties. Environ Health Perspect 105:1222–1227.
13. Lappano R, Maggiolini M. 2011. G protein-coupled receptors: novel targets for drug discovery in cancer. Nat Rev Drug Discov 10:47–60.
14. Lappano R, Rosano C, De Marco P, De Francesco EM, Pezzi V, Maggiolini M. 2010. Estriol acts as a GPR30 antagonist in estrogen receptor-negative breast cancer cells. Mol Cell Endocrinol 320:162–170.
15. Lappano R, Rosano C, Santolla MF, Pupo M, De Francesco EM, De Marco P, et al. 2012a. Two novel GPER agonists induce gene expression changes and growth effects in cancer cells. Curr Cancer Drug Targets 12:531–542.
16. Lappano R, Santolla MF, Pupo, M, Sinicropi MS, Caruso A, Rosano C, et al. 2012b. MIBE acts as antagonist ligand of both estrogen receptor α and GPER in breast cancer cells. Breast Cancer Res 14(1):R12; doi:10.1186/bcr3096.
17. Madeo A, Maggiolini M. 2010. Nuclear alternate estrogen receptor GPR30 mediates 17β-estradiolinduced gene expression and migration in breast cancer-associated fibroblasts. Cancer Res 70:6036–6046.
18. Maggiolini M, Donzé O, Picard D. 1999. A non-radioactive method for inexpensive quantitative RT-PCR. Biol Chem 380:695–700.
19. Maggiolini M, Picard D. 2010. The unfolding stories of GPR30, a new membrane-bound estrogen receptor. J Endocrinol 204:105–114.
20. Maggiolini M, Vivacqua A, Fasanella G, Recchia AG, Sisci D, Pezzi V, et al. 2004. The G protein-coupled receptor GPR30 mediates c-fos up-regulation by 17β-estradiol and phytoestrogens in breast cancer cells. J Biol Chem 279:27008–27016.
21. Migliaccio A, Castoria G, Auricchio F. 2007. Src-dependent signalling pathway regulation by sex-steroid hormones: therapeutic implications. Int J Biochem Cell Biol 39:1343–1348.
22. Migliaccio A, Castoria G, Di Domenico M, Ciociola A, Lombardi M, De Falco A, et al. 2006. Crosstalk between EGFR and extranuclear steroid receptors. Ann NY Acad Sci 1089:194-200.
23. Miller SM, Sweet CW, DePinto JV, Hornbuckle KC. 2000. Atrazine and nutrients in precipitation: results from the Lake Michigan Mass Balance Study. Environ Sci Technol 34:55–61.
24. Nadal A, Ropero AB, Laribi O, Maillet M, Fuentes E, Soria B. 2000. Nongenomic actions of estrogens and xenoestrogens by binding at a plasma membrane receptor unrelated to estrogen receptor α and estrogen receptor β. Proc Natl Acad Sci USA 97:11603–11608.
25. Norman AW, Mizwicki MT, Norman DP. 2004. Steroidhormone rapid actions, membrane receptors and a conformational ensemble model. Nat Rev Drug Discov 3:27-41.
26. Pandey DP, Lappano R, Albanito L, Madeo A, Maggiolini M, Picard D. 2009. Estrogenic GPR30 signalling induces proliferation and migration of breast cancer cells through CTGF. EMBO J 28:523–532.
27. Pintér A, Török G, Börzsönyi M, Surján A, Csík M, Kelecsényi Z, et al. 1990. Long-term carcinogenicity bioassay of the herbicide atrazine in F344 rats. Neoplasma 37:533–544.
28. Prossnitz ER, Barton M. 2014. Estrogen biology: new insights into GPER function and clinical opportunities. Mol Cell Endocrinol 389:71–83.
29. Pupo M, Pisano A, Lappano R, Santolla MF, De Francesco EM, Abonante S, et al. 2012. Bisphenol A induces gene expression changes and proliferative effects through GPER in breast cancer cells and cancer-associated fibroblasts. Environ Health Perspect 120:1177-1182; doi:10.1289/ ehp.1104526.
30. Roberge M, Hakk H, Larsen G. 2004. Atrazine is a competitive inhibitor of phosphodiesterase but does not affect the estrogen receptor. Toxicol Lett 154:61–68.
31. Safaei R, Katano K, Larson BJ, Samimi G, Holzer AK, Naerdemann W, et al. 2005. Intracellular localization and trafficking of fluorescein-labeled cisplatin in human ovarian carcinoma cells. Clin Cancer Res 11:756–767.
32. Sanderson JT, Letcher RJ, Heneweer M, Giesy JP, van den Berg M. 2001. Effects of chloro-s-triazine herbicides and metabolites on aromatase activity in various human cell lines and on vitellogenin production in male carp hepatocytes. Environ Health Perspect 109:1027–1031.
33. Sass JB, Colangelo A. 2006. European Union bans atrazine, while the United States negotiates continued use. Int J Occup Environ Health 12:260–267.
34. Seipel K, Georgiev O, Schaffner W. 1992. Different activation domains stimulate transcription from remote (‘enhancer’) and proximal (‘promoter’) positions. EMBO J 11:4961–4968.
35. Tennant MK, Hill DS, Eldridge JC, Wetzel LT, Breckenridge CB, Stevens JT. 1994. Chloro- s-triazine antagonism of estrogen action: limited interaction with estrogen receptor binding. J Toxicol Environ Health 43:197–211.
36. Thomas P. 2000. Chemical interference with the genomic and nongenomic actions of steroids in fishes: role of receptor binding. Mar Environ Res 50:127–134.
37. Thomas P, Dong J. 2006. Binding and activation of the seven-transmembrane estrogen receptor GPR30 by environmental estrogens: a potential novel mechanism of endocrine disruption. J Steroid Biochem Mol Biol 102:175–179.
38. Vivacqua A, Bonofiglio D, Albanito L, Madeo A, Rago V, Carpino A, et al. 2006a. 17β-Estradiol, genistein, and 4-hydroxytamoxifen induce the proliferation of thyroid cancer cells through the G protein coupled- receptor GPR30. Mol Pharmacol 70:1414-1423.
39. Vivacqua A, Bonofiglio D, Recchia AG, Musti AM, Picard D, Andò S, et al. 2006b. The G protein- coupled receptor GPR30 mediates the proliferative effects induced by 17β-estradiol and hydroxytamoxifen in endometrial cancer cells. Mol Endocrinol 20:631–646.
40. Vivacqua A, Lappano R, De Marco P, Sisci D, Aquila S, De Amicis F, et al. 2009. G protein-coupled receptor 30 expression is up-regulated by EGF and TGFα in estrogen receptor α-positive cancer cells. Mol Endocrinol 23:1815–1826.
41. Webb P, Nguyen P, Shinsako J, Anderson C, Feng W, Nguyen MP, et al. 1998. Estrogen receptor activation function 1 works by binding p160 coactivator proteins. Mol Endocrinol 12:1605–1618.