Estrogenic gper signaling regulates mir144 expression in cancer cells and cancer-associated fibroblasts (cafs)

Oncotarget

Volumn 6, Issue 18, 2015, Pages 16573-16587

  Vivacqua, Adele ^a   De Marco, Paola ^a   Santolla, Maria Francesca ^a   Cirillo, Francesca ^a   Pellegrino, Michele ^a   Panno, Maria Luisa ^a   Abonante, Sergio ^b   Maggiolini, Marcello ^a  

^a UNIVERSITY OF CALABRIA   (Italy)

^b Regional Hospital   (Italy)

Author keywords

CAFs; Cancer; Estrogens; GPER; miRNAs

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; G PROTEIN COUPLED RECEPTOR 30; MICRORNA; MICRORNA 144; MITOGEN ACTIVATED PROTEIN KINASE 1; PHOSPHATIDYLINOSITOL 3 KINASE; TRANSCRIPTION FACTOR ELK 1; TRANSCRIPTION FACTOR RUNX1; UNCLASSIFIED DRUG; ELK1 PROTEIN, HUMAN; ESTROGEN RECEPTOR; G PROTEIN COUPLED RECEPTOR; GPER PROTEIN, HUMAN; MIRN144 MICRORNA, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE; RUNX1 PROTEIN, HUMAN;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER CELL LINE; CANCER ASSOCIATED FIBROBLAST; CANCER CELL LINE; CANCER GROWTH; CELL CYCLE PROGRESSION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FIBROBLAST; GENE CONTROL; GENE EXPRESSION; GENE TARGETING; HEPG2 CELL LINE; HUMAN; HUMAN CELL; LNCAP CELL LINE; MCF 7 CELL LINE; MOUSE; NONHUMAN; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SKBR3 CELL LINE; TUMOR MICROENVIRONMENT; UPREGULATION; ANIMAL; BIOSYNTHESIS; CANCER TRANSPLANTATION; GENE EXPRESSION REGULATION; GENETICS; HEP-G2 CELL LINE; MCF-7 CELL LINE; METABOLISM; NEOPLASM; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; CELL LINE, TUMOR; CORE BINDING FACTOR ALPHA 2 SUBUNIT; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ETS-DOMAIN PROTEIN ELK-1; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; HEP G2 CELLS; HETEROGRAFTS; HUMANS; MCF-7 CELLS; MICE; MICE, NUDE; MICRORNAS; NEOPLASM TRANSPLANTATION; NEOPLASMS; PHOSPHATIDYLINOSITOL 3-KINASES; RECEPTORS, ESTROGEN; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

EID: 84937919496     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4117     Document Type: Article

References (53)

1. Zamore PD, Haley B. Genetics. Ribo-gnome: the big world of small RNAs. Science. 2005; 309: 1519-1524.
2. Vasudevan S, Tong Y, Steitz JA. Switching from repression to activation: microRNAs can up-regulate translation. Science. 2007; 318:1931-1934.
3. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009; 136: 215-233.
4. Iorio MV, Croce CM. MicroRNAs in Cancer: Small Molecules With a Huge Impact. J Clin Oncol. 2009; 27: 5848-5856.
5. Ell B, Kang Y. MicroRNAs as regulators of tumorassociated stromal cells. Oncotarget. 2013; 4: 2166-2167.
6. Ben-Hamo R, Efroni S. MicroRNA regulation of molecular pathways as a generic mechanism and as a core disease phenotype. Oncotarget. 2015; 6:1594-1604.
7. Mendell JT, Olson EN. MicroRNAs in stress signaling and human disease. Cell. 2012; 148: 1172-1187.
8. Smigal C, Jemal A, Ward E, Cokkinides V, Smith R, Howe HL and Thun M. Trends in breast cancer by race and ethnicity: update 2006. CA Cancer J Clin. 2006; 56: 168-183.
9. Iorio MV, Ferracn M, Liu CG, Veronese A, Spizzo R, Sabbioni S, Magri E, Pedriali M, Fabbri M, Campiglio M, Ménard S, Palazzo JP, Rosenberg A, et al. MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 2005; 65:7065-7070.
10. Yan LX, Huang XF, Shao Q, Huang MY, Deng L, Wu QL, Zeng YX, Shao JY. MicroRNA miRNA-21 overexpression in human breast cancer is associated with advanced clinical stage, lymph node metastasis and patient poor prognosis. RNA 2008; 14: 2348-2360.
11. Iorio MV, Casalini P, Piovan C, Di Leva G, Merlo A, Triulzi T, Ménard S, Croce CM, Tagliabue E. MicroRNA-205 regulates HER3 in human breast cancer. Cancer Res. 2009; 69: 2195-2200.
12. Miller TE, Ghoshal K, Ramaswamy B, Roy S, Datta J, Shapiro CL, Jacob S, Majumder S. MicroRNA-221/222 confers tamoxifen resistance in breast cancer by targeting p27Kip1. J Biol Chem. 2008; 283:29897-29903.
13. Zhao JJ, Lin J, Yang H, Kong W, He L, Ma X, Coppola D, Cheng J.Q. MicroRNA-221/222 negatively regulates estrogen receptor alpha and is associated with tamoxifen resistance in breast cancer. J Biol Chem. 2008; 283: 31079-31086.
14. Di Leva GL, Piovan C, Gasparini P, Ngankeu A, Taccioli C, Briskin D, Cheung DG, Bolon B, Anderlucci L, Alder H, Nuovo G, Li M, Iorio MV et al. Estrogen mediatedactivation of miRNA-191/425 cluster modulates tumorigenicity of breast cancer cells depending on estrogen receptor status. PLoS Genet. 2013; 9: e1003311.
15. Murakami Y, Yasuda T, Saigo K, Urashima T, Toyoda H, Okanoue T, Shimotohno K. Comprehensive analysis of microRNA expression patterns in hepatocellular carcinoma and non-tumorous tissues. Oncogene. 2006; 25: 2537-2545.
16. Li Y, Xu D, Bao C, Zhang Y, Chen D, Zhao F, Ding J, Liang L, Wang Q, Liu L, Li J, Yao M, Huang S, et al. MicroRNA-135b, a HSF1 target, promotes tumor invasion and metastasis by regulating RECK and EVI5 in hepatocellular carcinoma. Oncotarget. 2014; 6:2421-433.
17. Li W, Xie L, He X, Li J, Tu K, Wei L, Wu J, Guo Y, Ma X, Zhang P, Pan Z, Hu X, Zhao Y et al. Diagnostic and prognostic implications of microRNAs in human hepatocellular carcinoma. Int J Cancer. 2008; 123:1616-1622.
18. Altuvia Y, Landgraf P, Lithwick G, Elefant N, Pfeffer S, Aravin A, Brownstein MJ, Tuschl T, Margalit H. Clustering and conservation patterns of human microRNAs. Nucleic Acids Res. 2005; 33: 2697-2706.
19. Rasmussen KD, Simmini S, Abreu-Goodger C, Bartonicek N, Di Giacomo M, Bilbao-Cortes D, Horos R, Von Lindern M, Enright AJ, O'Carroll D. The miRNA-144/451 locus is required for erythroid homeostasis. J Exp Med. 2010; 207: 1351-1358.
20. Zhang LY, Ho-Fun Lee V, Wong AM, Kwong DL, Zhu YH, Dong SS, Kong KL, Chen J, Tsao SW, Guan XY, Fu L. MicroRNA-144 promotes cell proliferation, migration and invasion in nasopharyngeal carcinoma through repression of PTEN. Carcinogenesis. 2013; 34: 454-463.
21. Iwaya T, Yokobori T, Nishida N, Kogo R, Sudo T, Tanaka F, Shibata K, Sawada G, Takahashi Y, Ishibashi M, Wakabayashi G, Mori M, Mimori K. Downregulation of miRNA-144 is associated with colorectal cancer progression via activation of mTOR signaling pathway. Carcinogenesis. 2012; 33: 2391-2397.
22. Cheng C, Li W, Zhang Z, Yoshimura S, Hao Q, Zhang C, Wang Z. MicroRNA-144 is regulated by activator protein-1 (AP-1) and decreases expression of Alzheimer diseaserelated a disintegrin and metalloprotease 10 (ADAM10). J Biol Chem. 2013; 288: 13748-13761.
23. Jacovetti C, Abderrahmani A, Parnaud G, Jonas JC, Peyot ML, Cornu M, Laybutt R, Meugnier E, Rome S, Thorens B, Prentki M, Bosco D, Regazzi R. MicroRNAs contribute to compensatory β cell expansion during pregnancy and obesity. J Clin Invest. 2012; 122: 3541-3551.
24. Burns KA, Korach KS. Estrogen receptors and human disease: an update. Arch Toxicol. 2012; 86: 1491-1504.
25. Prossnitz ER, Barton M. Estrogen biology: new insights into GPER function and clinical opportunities. Mol Cell Endocrinol. 2014; 389: 71-83.
26. Filardo EJ, Thomas P. Minireview: G protein-coupled estrogen receptor-1, GPER-1: its mechanism of action and role in female reproductive cancer, renal and vascular physiology. Endocrinology. 2012; 153: 2953-2962.
27. De Francesco EM, Pellegrino M, Santolla MF, Lappano R, Ricchio E, Abonante S, Maggiolini M. GPER Mediates Activation of HIF1a/VEGF Signaling by Estrogens. Cancer Res. 2014; 74: 4053-4064.
28. Vivacqua A, Romeo E, De Marco P, De Francesco EM, Abonante S, Maggiolini M. GPER mediates the Egr-1 expression induced by 17β-estradiol and 4-hydroxitamoxifen in breast and endometrial cancer cells. Breast Cancer Res Treat. 2012; 133:1025-35.
29. Santolla MF, Lappano R, De Marco P, Pupo M, Vivacqua A, Sisci D, Abonante S, Iacopetta D, Cappello AR, Dolce V, Maggiolini M. G protein-coupled estrogen receptor mediates the up-regulation of fatty acid synthase induced by 17β-estradiol in cancer cells and cancer-associated fibroblasts. J Biol Chem. 2012; 287: 43234-43245.
30. Albanito L, Madeo A, Lappano R, Vivacqua A, Rago V, Carpino A, Oprea TI, Prossnitz ER, Musti AM, Andò S, Maggiolini M. G protein-coupled receptor 30 (GPR30) mediates gene expression changes and growth response to 17beta-estradiol and selective GPR30 ligand G-1 in ovarian cancer cells. Cancer Res. 2007; 67: 1859-1866.
31. Vivacqua A, Bonofiglio D, Recchia AG, Musti AM, Picard D, Andò S, Maggiolini M. The G protein-coupled receptor GPR30 mediates the proliferative effects induced by 17beta-estradiol and hydroxytamoxifen in endometrial cancer cells. Mol Endocrinol. 2006; 20: 631-646.
32. Vivacqua A, Bonofiglio D, Albanito L, Madeo A, Rago V, Carpino A, Musti AM, Picard D, Andò S, Maggiolini M. 17beta-estradiol, genistein, and 4-hydroxytamoxifen induce the proliferation of thyroid cancer cells through the G protein-coupled receptor GPR30. Mol Pharmacol. 2006; 70: 1414-1423.
33. Maggiolini M, Vivacqua A, Fasanella G, Recchia AG, Sisci D, Pezzi V, Montanaro D, Musti AM, Picard D, Andò S. The G protein-coupled receptor GPR30 mediates c-fos upregulation by 17beta-estradiol and phytoestrogens in breast cancer cells. J Biol Chem. 2004; 279: 27008-27016.
34. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer. 2006; 6: 392-401.
35. Namløs HM, Meza-Zepeda LA, Barøy T, Østensen IH, Kresse SH, Kuijjer ML, Serra M, Bürger H, Cleton-Jansen AM, Myklebost O. Modulation of the osteosarcoma expression phenotype by microRNAs. PLoSOne. 2012; 7: e48086.
36. Guled M, Lahti L, Lindholm PM, Salmenkivi K, Bagwan I, Nicholson AG, Knuutila S. CDKN2A, NF2, and JUN are dysregulated among other genes by miRNANAs in malignant mesothelioma -A miRNA microarray analysis. Genes Chromosomes Cancer. 2009; 48: 615-623.
37. Akiyoshi S, Fukagawa T, Ueo H, Ishibashi M, Takahashi Y, Fabbri M, Sasako M, Maehara Y, Mimori K, Mori M. Clinical significance of miRNA-144-ZFX axis in disseminated tumour cells in bone marrow in gastric cancer cases. Br J Cancer. 2012; 107: 1345-1353.
38. Kalimutho M, Del Vecchio Blanco G, Di Cecilia S, Sileri P, Cretella M, Pallone F, Federici G, Bernardini S. Differential expression of miRNA-144* as a novel fecal-based diagnostic marker for colorectal cancer. J Gastroenterol. 2011; 46: 1391-1402.
39. Cheng AM, Byrom MW, Shelton J, Ford LP. Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res. 2005; 33: 1290-1297.
40. Ma Y, She XG, Ming YZ, Wan QQ, Ye QF. MicroRNA-144 suppresses tumorigenesis of hepatocellular carcinoma by targeting AKT3. Mol Med Rep. 2015; 11: 1378-1383.
41. Ito Y, Bae SC, Chuang LS. The RUNX family: developmental regulators in cancer. Nat Rev Cancer. 2015; 15: 81-95.
42. Chimge NO, Frenkel B. The RUNX family in breast cancer: relationships with estrogen signaling. Oncogene 2013; 32: 2121-2130.
43. Janes KA. RUNX1 and its understudied role in breast cancer. Cell Cycle. 2011; 10: 3461-3465.
44. Frederick AM, Lawrence MS, Sivachenko AY, Sougnez C, Zou L, Cortes ML, Fernandez-Lopez JC, Peng S, et al. Sequence analysis of mutations and translocations across breast cancer subtypes. Nature. 2012; 486: 405-409.
45. Kadota M, Yang HH, Gomez B, Sato M, Clifford RJ, Meerzaman D, Dunn BK, Wakefield LM, Lee MP. Delineating genetic alterations for tumor progression in the MCF10A series of breast cancer cell lines. PLoS One. 2010; 5: e9201.
46. Chuang LSH, Ito K, Ito Y. RUNX family: Regulation and diversification of roles through interacting proteins. Int. J. Cancer. 2013; 132: 1260-1271.
47. Wang L, Brugge JS, Janes KA. Intersection of FOXO-and RUNX1-mediated gene expression programs in single breast epithelial cells during morphogenesis and tumor progression. Proc Natl Acad Sci USA 2011; 108: E803-E812.
48. Vrtacnik P, Ostanek B, Mencej-Bedrac S, Marc J. The many faces of estrogen signaling. Biochem Med (Zagreb) 2014; 24: 329-342.
49. Tao S, He H, Chen Q, Yue W. GPER mediated estradiol reduces miRNA-148a to promote HLA-G expression in breast cancer. Biochem Biophys Res Commun. 2014; 451: 74-78.
50. Pupo M, Vivacqua A, Perrotta I, Pisano A, Aquila S, Abonante S, Gasperi-Campani A, Pezzi V, Maggiolini M. The nuclear localization signal is required for nuclear GPER translocation and function in breast Cancer-Associated Fibroblasts (CAFs). Mol Cell Endocrinol. 2013; 376: 23-32.
51. Pandey DP, Lappano R, Albanito L, Madeo A, Maggiolini M, Picard D. Estrogenic GPR30 signalling induces proliferation and migration of breast cancer cells through CTGF. EMBO J. 2009; 28: 523-532.
52. Gallo A, Cuozzo C, Esposito I, Maggiolini M, Bonofiglio D, Vivacqua A, Garramone M, Weiss C, Bohmann D, Musti AM. Menin uncouples ELK-1, JunD and c-Jun phosphorilation from MAP kinase activation. Oncogene. 2002; 21: 6434-6445.
53. Meyers S, Lenny N, Hiebert SW. The t(8;21) fusion protein interferes with AML-1B-dependent transcriptional activation. Mol Cell Biol 1995; 15: 1974-1982.