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Journal of Experimental & Clinical Cancer Research
Published in: Journal of Experimental & Clinical Cancer Research 1/2019

Open Access 01-12-2019 | Breast Cancer | Review

FGFs/FGFRs-dependent signalling in regulation of steroid hormone receptors – implications for therapy of luminal breast cancer

Authors: Dominika Piasecka, Marcin Braun, Kamila Kitowska, Kamil Mieczkowski, Radzislaw Kordek, Rafal Sadej, Hanna Romanska

Published in: Journal of Experimental & Clinical Cancer Research | Issue 1/2019

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Abstract

Stromal stimuli mediated by growth factor receptors, leading to ligand-independent activation of steroid hormone receptors, have long been implicated in development of breast cancer resistance to endocrine therapy. Mutations in fibroblast growth factor receptor (FGFR) genes have been associated with a higher incidence and progression of breast cancer. Increasing evidence suggests that FGFR-mediated interaction between luminal invasive ductal breast carcinoma (IDC) and its microenvironment contributes to the progression to hormone-independence. Therapeutic strategies based on FGFR inhibitors hold promise for overcoming resistance to the ER-targeting treatment. A series of excellent reviews discuss a potential role of FGFR in development of IDC. Here, we provide a concise updated summary of existing literature on FGFR-mediated signalling with an emphasis on an interaction between FGFR and estrogen/progesterone receptors (ER/PR) in IDC. Focusing on the regulatory role of tumour microenvironment in the activity of steroid hormone receptors, we compile the available functional data on FGFRs-mediated signalling, as a fundamental mechanism of luminal IDC progression and failure of anti-ER treatment. We also highlight the translational value of the presented findings and summarize ongoing oncologic clinical trials investigating FGFRs inhibition in interventional studies in breast cancer.
Literature
1.
Vollenweider-Zerargui L, Barrelet L, Wong Y, Lemarchand-Beraud T, Gomez F. The predictive value of estrogen and progesterone receptors' concentrations on the clinical behavior of breast cancer in women. Clinical correlation on 547 patients. Cancer. 1986;57(6):1171–80.PubMedCrossRef
2.
Sinn HP, Kreipe H. A brief overview of the WHO classification of breast tumors, 4th edition, focusing on issues and updates from the 3rd edition. Breast Care (Basel). 2013;8(2):149–54.CrossRef
3.
Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, et al. Molecular portraits of human breast tumours. Nature. 2000;406(6797):747–52.PubMedCrossRef
4.
Sørlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci U S A. 2001;98(19):10869–74.PubMedPubMedCentralCrossRef
5.
Fan C, Oh DS, Wessels L, Weigelt B, Nuyten DS, Nobel AB, et al. Concordance among gene-expression-based predictors for breast cancer. N Engl J Med. 2006;355(6):560–9.PubMedCrossRef
6.
Parker JS, Mullins M, Cheang MC, Leung S, Voduc D, Vickery T, et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol. 2009;27(8):1160–7.PubMedPubMedCentralCrossRef
7.
Dai X, Li T, Bai Z, Yang Y, Liu X, Zhan J, et al. Breast cancer intrinsic subtype classification, clinical use and future trends. Am J Cancer Res. 2015;5(10):2929–43.PubMedPubMedCentral
8.
Nielsen TO, Parker JS, Leung S, Voduc D, Ebbert M, Vickery T, et al. A comparison of PAM50 intrinsic subtyping with immunohistochemistry and clinical prognostic factors in tamoxifen-treated estrogen receptor-positive breast cancer. Clin Cancer Res. 2010;16(21):5222–32.PubMedPubMedCentralCrossRef
9.
Fisher B, Costantino J, Redmond C, Poisson R, Bowman D, Couture J, et al. A randomized clinical trial evaluating tamoxifen in the treatment of patients with node-negative breast cancer who have estrogen-receptor-positive tumors. N Engl J Med. 1989;320(8):479–84.PubMedCrossRef
10.
Clarke R, Liu MC, Bouker KB, Gu Z, Lee RY, Zhu Y, et al. Antiestrogen resistance in breast cancer and the role of estrogen receptor signaling. Oncogene. 2003;22(47):7316–39.PubMedCrossRef
11.
12.
Braun L, Mietzsch F, Seibold P, Schneeweiss A, Schirmacher P, Chang-Claude J, et al. Intrinsic breast cancer subtypes defined by estrogen receptor signalling-prognostic relevance of progesterone receptor loss. Mod Pathol. 2013;26(9):1161–71.PubMedCrossRef
13.
Cheang MC, Chia SK, Voduc D, Gao D, Leung S, Snider J, et al. Ki67 index, HER2 status, and prognosis of patients with luminal B breast cancer. J Natl Cancer Inst. 2009;101(10):736–50.PubMedPubMedCentralCrossRef
14.
Bardou VJ, Arpino G, Elledge RM, Osborne CK, Clark GM. Progesterone receptor status significantly improves outcome prediction over estrogen receptor status alone for adjuvant endocrine therapy in two large breast cancer databases. J Clin Oncol. 2003;21(10):1973–9.PubMedCrossRef
15.
Arpino G, Weiss H, Lee AV, Schiff R, De Placido S, Osborne CK, et al. Estrogen receptor-positive, progesterone receptor-negative breast cancer: association with growth factor receptor expression and tamoxifen resistance. J Natl Cancer Inst. 2005;97:1254–61.PubMedCrossRef
16.
Prat A, Cheang MC, Martin M, Parker JS, Carrasco E, Caballero R, et al. Prognostic significance of progesterone receptor-positive tumor cells within immunohistochemically defined luminal a breast cancer. J Clin Oncol. 2013;31(2):203–9.PubMedCrossRef
17.
Trédan O, Galmarini CM, Patel K, Tannock IF. Drug resistance and the solid tumor microenvironment. J Natl Cancer Inst. 2007;99(19):1441–54.PubMedCrossRef
18.
Son B, Lee S, Youn H, Kim E, Kim W, Youn B. The role of tumor microenvironment in therapeutic resistance. Oncotarget. 2017;8(3):3933–45.PubMedCrossRef
19.
20.
Balkwill FR, Capasso M, Hagemann T. The tumor microenvironment at a glance. J Cell Sci. 2012;125(Pt 23:5591–6.PubMedCrossRef
21.
22.
Polyak K, Haviv I, Campbell IG. Co-evolution of tumor cells and their microenvironment. Trends Genet. 2009;25(1):30–8.PubMedCrossRef
23.
Chen F, Zhuang X, Lin L, Yu P, Wang Y, Shi Y, et al. New horizons in tumor microenvironment biology: challenges and opportunities. BMC Med. 2015;13(1):45.PubMedPubMedCentralCrossRef
24.
Lin EY, Pollard JW. Macrophages: modulators of breast cancer progression. Novartis Found Symp. 2004;256:158–68; discussion 68-72, 259-69.PubMed
25.
Qiu SQ, Waaijer SJH, Zwager MC, de Vries EGE, van der Vegt B, Schroder CP. Tumor-associated macrophages in breast cancer: innocent bystander or important player? Cancer Treat Rev. 2018;70:178–89.PubMedCrossRef
26.
27.
Wyckoff J, Wang W, Lin EY, Wang Y, Pixley F, Stanley ER, et al. A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res. 2004;64(19):7022–9.CrossRefPubMed
28.
Su S, Liu Q, Chen J, Chen F, He C, Huang D, et al. A positive feedback loop between mesenchymal-like cancer cells and macrophages is essential to breast cancer metastasis. Cancer Cell. 2014;25(5):605–20.PubMedCrossRef
29.
Brechbuhl HM, Finlay-Schultz J, Yamamoto TM, Gillen AE, Cittelly DM, Tan AC, et al. Fibroblast subtypes regulate responsiveness of luminal breast Cancer to estrogen. Clin Cancer Res. 2017;23(7):1710–21.PubMedCrossRef
30.
Fabris VT, Sahores A, Vanzulli SI, Colombo L, Molinolo AA, Lanari C, et al. Inoculated mammary carcinoma-associated fibroblasts: contribution to hormone independent tumor growth. BMC Cancer. 2010;10:293.PubMedPubMedCentralCrossRef
31.
Giulianelli S, Cerliani JP, Lamb CA, Fabris VT, Bottino MC, Gorostiaga MA, et al. Carcinoma-associated fibroblasts activate progesterone receptors and induce hormone independent mammary tumor growth: a role for the FGF-2/FGFR-2 axis. Int J Cancer. 2008;123(11):2518–31.PubMedCrossRef
32.
Turczyk L, Kitowska K, Mieszkowska M, Mieczkowski K, Czaplinska D, Piasecka D, et al. FGFR2-driven signaling counteracts tamoxifen effect on ERα-positive breast Cancer cells. Neoplasia. 2017;19(10):791–804.PubMedPubMedCentralCrossRef
33.
Pontiggia O, Sampayo R, Raffo D, Motter A, Xu R, Bissell MJ, et al. The tumor microenvironment modulates tamoxifen resistance in breast cancer: a role for soluble stromal factors and fibronectin through β1 integrin. Breast Cancer Res Treat. 2012;133(2):459–71.PubMedCrossRef
34.
Yuan J, Liu M, Yang L, Tu G, Zhu Q, Chen M, et al. Acquisition of epithelial-mesenchymal transition phenotype in the tamoxifen-resistant breast cancer cell: a new role for G protein-coupled estrogen receptor in mediating tamoxifen resistance through cancer-associated fibroblast-derived fibronectin and β1-integrin signaling pathway in tumor cells. Breast Cancer Res. 2015;17:69.PubMedPubMedCentralCrossRef
35.
Shekhar MP, Santner S, Carolin KA, Tait L. Direct involvement of breast tumor fibroblasts in the modulation of tamoxifen sensitivity. Am J Pathol. 2007;170(5):1546–60.PubMedPubMedCentralCrossRef
36.
Burke D, Wilkes D, Blundell TL, Malcolm S. Fibroblast growth factor receptors: lessons from the genes. Trends Biochem Sci. 1998;23(2):59–62.PubMedCrossRef
37.
Sleeman M, Fraser J, McDonald M, Yuan S, White D, Grandison P, et al. Identification of a new fibroblast growth factor receptor, FGFR5. Gene. 2001;271(2):171–82.PubMedCrossRef
38.
Babina IS, Turner NC. Advances and challenges in targeting FGFR signalling in cancer. Nat Rev Cancer. 2017;17(5):318–32.PubMedCrossRef
39.
Wesche J, Haglund K, Haugsten EM. Fibroblast growth factors and their receptors in cancer. Biochem J. 2011;437(2):199–213.PubMedCrossRef
40.
Brooks AN, Kilgour E, Smith PD. Molecular pathways: fibroblast growth factor signaling: a new therapeutic opportunity in cancer. Clin Cancer Res. 2012;18(7):1855–62.PubMedCrossRef
41.
42.
Mailleux AA, Spencer-Dene B, Dillon C, Ndiaye D, Savona-Baron C, Itoh N, et al. Role of FGF10/FGFR2b signaling during mammary gland development in the mouse embryo. Development. 2002;129(1):53–60.PubMed
43.
Parsa S, Ramasamy SK, De Langhe S, Gupte VV, Haigh JJ, Medina D, et al. Terminal end bud maintenance in mammary gland is dependent upon FGFR2b signaling. Dev Biol. 2008;317(1):121–31.PubMedCrossRef
44.
Pond AC, Bin X, Batts T, Roarty K, Hilsenbeck S, Rosen JM. Fibroblast growth factor receptor signaling is essential for normal mammary gland development and stem cell function. Stem Cells. 2013;31(1):178–89.PubMedCrossRef
45.
Adnane J, Gaudray P, Dionne CA, Crumley G, Jaye M, Schlessinger J, et al. BEK and FLG, two receptors to members of the FGF family, are amplified in subsets of human breast cancers. Oncogene. 1991;6(4):659–63.PubMed
46.
Jaakkola S, Salmikangas P, Nylund S, Partanen J, Armstrong E, Pyrhönen S, et al. Amplification of fgfr4 gene in human breast and gynecological cancers. Int J Cancer. 1993;54(3):378–82.PubMedCrossRef
47.
Penault-Llorca F, Bertucci F, Adélaïde J, Parc P, Coulier F, Jacquemier J, et al. Expression of FGF and FGF receptor genes in human breast cancer. Int J Cancer. 1995;61(2):170–6.PubMedCrossRef
48.
Elbauomy Elsheikh S, Green AR, Lambros MB, Turner NC, Grainge MJ, Powe D, et al. FGFR1 amplification in breast carcinomas: a chromogenic in situ hybridisation analysis. Breast Cancer Res. 2007;9(2):R23.PubMedPubMedCentralCrossRef
49.
Helsten T, Elkin S, Arthur E, Tomson BN, Carter J, Kurzrock R. The FGFR landscape in Cancer: analysis of 4,853 tumors by next-generation sequencing. Clin Cancer Res. 2016;22(1):259–67.PubMedCrossRef
50.
Bange J, Prechtl D, Cheburkin Y, Specht K, Harbeck N, Schmitt M, et al. Cancer progression and tumor cell motility are associated with the FGFR4 Arg (388) allele. Cancer Res. 2002;62(3):840–7.PubMed
51.
Thussbas C, Nahrig J, Streit S, Bange J, Kriner M, Kates R, et al. FGFR4 Arg388 allele is associated with resistance to adjuvant therapy in primary breast cancer. J Clin Oncol. 2006;24(23):3747–55.PubMedCrossRef
52.
Fillmore CM, Gupta PB, Rudnick JA, Caballero S, Keller PJ, Lander ES, et al. Estrogen expands breast cancer stem-like cells through paracrine FGF/Tbx3 signaling. Proc Natl Acad Sci U S A. 2010;107(50):21737–42.PubMedPubMedCentralCrossRef
53.
Yu M, Bardia A, Aceto N, Bersani F, Madden MW, Donaldson MC, et al. Cancer therapy. Ex vivo culture of circulating breast tumor cells for individualized testing of drug susceptibility. Science. 2014;345(6193):216–20.PubMedPubMedCentralCrossRef
54.
Garcia-Murillas I, Schiavon G, Weigelt B, Ng C, Hrebien S, Cutts RJ, et al. Mutation tracking in circulating tumor DNA predicts relapse in early breast cancer. Sci Transl Med. 2015;7(302):302ra133.PubMedCrossRef
55.
Wang S, Ding Z. Fibroblast growth factor receptors in breast cancer. Tumour Biol. 2017;39(5):1010428317698370.PubMed
56.
Cox DG, Curtit E, Romieu G, Fumoleau P, Rios M, Bonnefoi H, et al. GWAS in the SIGNAL/PHARE clinical cohort restricts the association between the FGFR2 locus and estrogen receptor status to HER2-negative breast cancer patients. Oncotarget. 2016;7(47):77358–64.PubMedPubMedCentralCrossRef
57.
Jia C, Cai Y, Ma Y, Fu D. Quantitative assessment of the effect of FGFR2 gene polymorphism on the risk of breast cancer. Breast Cancer Res Treat. 2010;124(2):521–8.PubMedCrossRef
58.
Zhou L, Yao F, Luan H, Wang Y, Dong X, Zhou W, et al. Three novel functional polymorphisms in the promoter of FGFR2 gene and breast cancer risk: a HuGE review and meta-analysis. Breast Cancer Res Treat. 2012;136(3):885–97.PubMedCrossRef
59.
Cui F, Wu D, Wang W, He X, Wang M. Variants of FGFR2 and their associations with breast cancer risk: a HUGE systematic review and meta-analysis. Breast Cancer Res Treat. 2016;155(2):313–35.PubMedCrossRef
60.
Boyarskikh UA, Zarubina NA, Biltueva JA, Sinkina TV, Voronina EN, Lazarev AF, et al. Association of FGFR2 gene polymorphisms with the risk of breast cancer in population of West Siberia. Eur J Hum Genet. 2009;17:1688–91.PubMedPubMedCentralCrossRef
61.
Marian C, Ochs-Balcom HM, Nie J, Kallakury BV, Ambrosone CB, Trevisan M, et al. FGFR2 intronic SNPs and breast cancer risk: associations with tumor characteristics and interactions with exogenous exposures and other known breast cancer risk factors. Int J Cancer. 2011;129(3):702–12.PubMedCrossRef
62.
Wang H, Yang Z, Zhang H. Assessing interactions between the associations of fibroblast growth factor receptor 2 common genetic variants and hormone receptor status with breast cancer risk. Breast Cancer Res Treat. 2013;137(2):511–22.PubMedCrossRef
63.
Zhang Y, Lu H, Ji H, Lu L, Liu P, Hong R, et al. Association between rs11200014, rs2981579, and rs1219648 polymorphism and breast cancer susceptibility: a meta-analysis. Medicine (Baltimore). 2017;96(50):e9246.CrossRef
64.
Wu J, Wang Y, Liu J, Chen Q, Pang D, Jiang Y. Effects of FGFR1 gene polymorphisms on the risk of breast Cancer and FGFR1 protein expression. Cell Physiol Biochem. 2018;47(6):2569–78.PubMedCrossRef
65.
Ghoussaini M, French JD, Michailidou K, Nord S, Beesley J, Canisus S, et al. Evidence that the 5p12 variant rs10941679 confers susceptibility to estrogen-receptor-positive breast Cancer through FGF10 and MRPS30 regulation. Am J Hum Genet. 2016;99(4):903–11.PubMedPubMedCentralCrossRef
66.
Tiong KH, Mah LY, Leong CO. Functional roles of fibroblast growth factor receptors (FGFRs) signaling in human cancers. Apoptosis. 2013;18(12):1447–68.PubMedPubMedCentralCrossRef
67.
Garcia-Closas M, Hall P, Nevanlinna H, Pooley K, Morrison J, Richesson DA, et al. Heterogeneity of breast cancer associations with five susceptibility loci by clinical and pathological characteristics. PLoS Genet. 2008;4(4):e1000054.PubMedPubMedCentralCrossRef
68.
Liang J, Chen P, Hu Z, Zhou X, Chen L, Li M, et al. Genetic variants in fibroblast growth factor receptor 2 (FGFR2) contribute to susceptibility of breast cancer in Chinese women. Carcinogenesis. 2008;29(12):2341–6.PubMedCrossRef
69.
70.
71.
Owen GI, Richer JK, Tung L, Takimoto G, Horwitz KB. Progesterone regulates transcription of the p21(WAF1) cyclin- dependent kinase inhibitor gene through Sp1 and CBP/p300. J Biol Chem. 1998;273(17):10696–701.PubMedCrossRef
72.
Stossi F, Madak-Erdogan Z, Katzenellenbogen BS. Estrogen receptor alpha represses transcription of early target genes via p300 and CtBP1. Mol Cell Biol. 2009;29(7):1749–59.PubMedPubMedCentralCrossRef
73.
Mohammed H, Russell IA, Stark R, Rueda OM, Hickey TE, Tarulli GA, et al. Progesterone receptor modulates ERα action in breast cancer. Nature. 2015;523(7560):313–7.PubMedPubMedCentralCrossRef
74.
Ballare C, Uhrig M, Bechtold T, Sancho E, Di Domenico M, Migliaccio A, et al. Two domains of the progesterone receptor interact with the estrogen receptor and are required for progesterone activation of the c-Src/Erk pathway in mammalian cells. Mol Cell Biol. 2003;23(6):1994–2008.PubMedPubMedCentralCrossRef
75.
Denner LA, Weigel NL, Maxwell BL, Schrader WT, O'Malley BW. Regulation of progesterone receptor-mediated transcription by phosphorylation. Science. 1990;250(4988):1740–3.PubMedCrossRef
76.
Labriola L, Salatino M, Proietti CJ, Pecci A, Coso OA, Kornblihtt AR, et al. Heregulin induces transcriptional activation of the progesterone receptor by a mechanism that requires functional ErbB-2 and mitogen-activated protein kinase activation in breast cancer cells. Mol Cell Biol. 2003;23(3):1095–111.PubMedPubMedCentralCrossRef
77.
Cui X, Zhang P, Deng W, Oesterreich S, Lu Y, Mills GB, et al. Insulin-like growth factor-I inhibits progesterone receptor expression in breast cancer cells via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin pathway: progesterone receptor as a potential indicator of growth factor activity in breast cancer. Mol Endocrinol. 2003;17(4):575–88.PubMedCrossRef
78.
Daniel AR, Faivre EJ, Lange CA. Phosphorylation-dependent antagonism of sumoylation derepresses progesterone receptor action in breast cancer cells. Mol Endocrinol. 2007;21(12):2890–906.PubMedCrossRef
79.
Cerliani JP, Guillardoy T, Giulianelli S, Vaque JP, Gutkind JS, Vanzulli SI, et al. Interaction between FGFR-2, STAT5, and progesterone receptors in breast cancer. Cancer Res. 2011;71(10):3720–31.PubMedCrossRef
80.
Piasecka D, Kitowska K, Czaplinska D, Mieczkowski K, Mieszkowska M, Turczyk L, et al. Fibroblast growth factor signalling induces loss of progesterone receptor in breast cancer cells. Oncotarget. 2016;7(52):86011–25.PubMedPubMedCentralCrossRef
81.
Ma ZQ, Santagati S, Patrone C, Pollio G, Vegeto E, Maggi A. Insulin-like growth factors activate estrogen receptor to control the growth and differentiation of the human neuroblastoma cell line SK-ER3. Mol Endocrinol. 1994;8(7):910–8.PubMed
82.
Kato S, Endoh H, Masuhiro Y, Kitamoto T, Uchiyama S, Sasaki H, et al. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science. 1995;270(5241):1491–4.PubMedCrossRef
83.
Ignar-Trowbridge DM, Nelson KG, Bidwell MC, Curtis SW, Washburn TF, McLachlan JA, et al. Coupling of dual signaling pathways: epidermal growth factor action involves the estrogen receptor. Proc Natl Acad Sci U S A. 1992;89(10):4658–62.PubMedPubMedCentralCrossRef
84.
Bunone G, Briand PA, Miksicek RJ, Picard D. Activation of the unliganded estrogen receptor by EGF involves the MAP kinase pathway and direct phosphorylation. EMBO J. 1996;15(9):2174–83.PubMedPubMedCentralCrossRef
85.
Joel PB, Traish AM, Lannigan DA. Estradiol-induced phosphorylation of serine 118 in the estrogen receptor is independent of p42/p44 mitogen-activated protein kinase. J Biol Chem. 1998;273(21):13317–23.PubMedCrossRef
86.
Zhou W, Slingerland JM. Links between oestrogen receptor activation and proteolysis: relevance to hormone-regulated cancer therapy. Nat Rev Cancer. 2014;14(1):26–38.PubMedCrossRef
87.
Qiu M, Olsen A, Faivre E, Horwitz KB, Lange CA. Mitogen-activated protein kinase regulates nuclear association of human progesterone receptors. Mol Endocrinol. 2003;17(4):628–42.PubMedCrossRef
88.
Qiu M, Lange CA. MAP kinases couple multiple functions of human progesterone receptors: degradation, transcriptional synergy, and nuclear association. J Steroid Biochem Mol Biol. 2003;85(2–5):147–57.PubMedCrossRef
89.
Shen T, Horwitz KB, Lange CA. Transcriptional hyperactivity of human progesterone receptors is coupled to their ligand-dependent down-regulation by mitogen-activated protein kinase-dependent phosphorylation of serine 294. Mol Cell Biol. 2001;21(18):6122–31.PubMedPubMedCentralCrossRef
90.
Gee JM, Robertson JF, Gutteridge E, Ellis IO, Pinder SE, Rubini M, et al. Epidermal growth factor receptor/HER2/insulin-like growth factor receptor signalling and oestrogen receptor activity in clinical breast cancer. Endocr Relat Cancer. 2005;12(Suppl 1):S99–S111.PubMedCrossRef
91.
Knutson TP, Daniel AR, Fan D, Silverstein KA, Covington KR, Fuqua SA, et al. Phosphorylated and sumoylation-deficient progesterone receptors drive proliferative gene signatures during breast cancer progression. Breast Cancer Res. 2012;14(3):R95.PubMedPubMedCentralCrossRef
92.
Abdel-Hafiz H, Dudevoir ML, Horwitz KB. Mechanisms underlying the control of progesterone receptor transcriptional activity by SUMOylation. J Biol Chem. 2009;284(14):9099–108.PubMedPubMedCentralCrossRef
93.
Knutson TP, Truong TH, Ma S, Brady NJ, Sullivan ME, Raj G, et al. Posttranslationally modified progesterone receptors direct ligand-specific expression of breast cancer stem cell-associated gene programs. J Hematol Oncol. 2017;10(1):89.PubMedPubMedCentralCrossRef
94.
McLeskey SW, Zhang L, El-Ashry D, Trock BJ, Lopez CA, Kharbanda S, et al. Tamoxifen-resistant fibroblast growth factor-transfected MCF-7 cells are cross-resistant in vivo to the antiestrogen ICI 182,780 and two aromatase inhibitors. Clin Cancer Res. 1998;4(3):697–711.PubMed
95.
Ruohola JK, Viitanen TP, Valve EM, Seppanen JA, Loponen NT, Keskitalo JJ, et al. Enhanced invasion and tumor growth of fibroblast growth factor 8b-overexpressing MCF-7 human breast cancer cells. Cancer Res. 2001;61(10):4229–37.PubMed
96.
Turner N, Pearson A, Sharpe R, Lambros M, Geyer F, Lopez-Garcia MA, et al. FGFR1 amplification drives endocrine therapy resistance and is a therapeutic target in breast cancer. Cancer Res. 2010;70(5):2085–94.PubMedPubMedCentralCrossRef
97.
Formisano L, Stauffer KM, Young CD, Bhola NE, Guerrero-Zotano AL, Jansen VM, et al. Association of FGFR1 with ERalpha maintains ligand-independent ER transcription and mediates resistance to estrogen deprivation in ER(+) breast Cancer. Clin Cancer Res. 2017;23(20):6138–50.PubMedCrossRefPubMedCentral
98.
Itoh N, Ohta H. Fgf10: a paracrine-signaling molecule in development, disease, and regenerative medicine. Curr Mol Med. 2014;14(4):504–9.PubMedCrossRef
99.
Campbell TM, Castro MAA, de Santiago I, Fletcher MNC, Halim S, Prathalingam R, et al. FGFR2 risk SNPs confer breast cancer risk by augmenting oestrogen responsiveness. Carcinogenesis. 2016;37(8):741–50.PubMedPubMedCentralCrossRef
100.
Campbell TM, Castro MAA, de Oliveira KG, Ponder BAJ, Meyer KB. ERα binding by transcription factors NFIB and YBX1 enables FGFR2 signaling to modulate estrogen responsiveness in breast Cancer. Cancer Res. 2018;78(2):410–21.PubMedCrossRef
101.
Lanari C, Lamb CA, Fabris VT, Helguero LA, Soldati R, Bottino MC, et al. The MPA mouse breast cancer model: evidence for a role of progesterone receptors in breast cancer. Endocr Relat Cancer. 2009;16:333–50.PubMedCrossRef
102.
Santen RJ, Santner SJ, Pauley RJ, Tait L, Kaseta J, Demers LM, et al. Estrogen production via the aromatase enzyme in breast carcinoma: which cell type is responsible? J Steroid Biochem Mol Biol. 1997;61(3–6):267–71.PubMedCrossRef
103.
Busch S, Rydén L, Stål O, Jirström K, Landberg G. Low ERK phosphorylation in cancer-associated fibroblasts is associated with tamoxifen resistance in pre-menopausal breast cancer. PLoS One. 2012;7(9):e45669.PubMedPubMedCentralCrossRef
104.
105.
Zhang L, Kharbanda S, Chen D, Bullocks J, Miller DL, Ding IY, et al. MCF-7 breast carcinoma cells overexpressing FGF-1 form vascularized, metastatic tumors in ovariectomized or tamoxifen-treated nude mice. Oncogene. 1997;15(17):2093–108.PubMedCrossRef
106.
McLeskey SW, Kurebayashi J, Honig SF, Zwiebel J, Lippman ME, Dickson RB, et al. Fibroblast growth factor 4 transfection of MCF-7 cells produces cell lines that are tumorigenic and metastatic in ovariectomized or tamoxifen-treated athymic nude mice. Cancer Res. 1993;53(9):2168–77.PubMed
107.
Giltnane JM, Hutchinson KE, Stricker TP, Formisano L, Young CD, Estrada MV, et al. Genomic profiling of ER(+) breast cancers after short-term estrogen suppression reveals alterations associated with endocrine resistance. Sci Transl Med. 2017;9(402).
108.
Tomlinson DC, Knowles MA, Speirs V. Mechanisms of FGFR3 actions in endocrine resistant breast cancer. Int J Cancer. 2012;130(12):2857–66.PubMedCrossRef
109.
Meijer D, Sieuwerts AM, Look MP, van Agthoven T, Foekens JA, Dorssers LC. Fibroblast growth factor receptor 4 predicts failure on tamoxifen therapy in patients with recurrent breast cancer. Endocr Relat Cancer. 2008;15(1):101–11.PubMedCrossRef
110.
Brady N, Chuntova P, Bade LK, Schwertfeger KL. The FGF/FGFR axis as a therapeutic target in breast cancer. Expert Rev Endocrinol Metab. 2013;8(4):391–402.PubMedPubMedCentralCrossRef
111.
Katoh M. Fibroblast growth factor receptors as treatment targets in clinical oncology. Nat Rev Clin Oncol. 2019;16(2):105–22.PubMedCrossRef
112.
André F, Bachelot T, Campone M, Dalenc F, Perez-Garcia JM, Hurvitz SA, et al. Targeting FGFR with dovitinib (TKI258): preclinical and clinical data in breast cancer. Clin Cancer Res. 2013;19(13):3693–702.PubMedCrossRef
113.
Musolino A, Campone M, Neven P, Denduluri N, Barrios CH, Cortes J, et al. Phase II, randomized, placebo-controlled study of dovitinib in combination with fulvestrant in postmenopausal patients with HR(+), HER2(−) breast cancer that had progressed during or after prior endocrine therapy. Breast Cancer Res. 2017;19(1):18.PubMedPubMedCentralCrossRef
114.
Cheng FT, Ou-Yang F, Lapke N, Tung KC, Chen YK, Chou YY, et al. Pazopanib sensitivity in a patient with breast Cancer and FGFR1 amplification. J Natl Compr Cancer Netw. 2017;15(12):1456–9.CrossRef
115.
Matsui J, Funahashi Y, Uenaka T, Watanabe T, Tsuruoka A, Asada M. Multi-kinase inhibitor E7080 suppresses lymph node and lung metastases of human mammary breast tumor MDA-MB-231 via inhibition of vascular endothelial growth factor-receptor (VEGF-R) 2 and VEGF-R3 kinase. Clin Cancer Res. 2008;14(17):5459–65.PubMedCrossRef
116.
Chae YK, Ranganath K, Hammerman PS, Vaklavas C, Mohindra N, Kalyan A, et al. Inhibition of the fibroblast growth factor receptor (FGFR) pathway: the current landscape and barriers to clinical application. Oncotarget. 2017;8:16052–74.PubMed
117.
Smyth EC, Turner NC, Pearson A, Peckitt C, Chau I, Watkins DJ, et al. Phase II study of AZD4547 in FGFR amplified tumours: gastroesophageal cancer (GC) cohort pharmacodynamic and biomarker results. J Clin Oncol. 2016;34(4) (Suppl):154.CrossRef
118.
Nogova L, Sequist LV, Perez Garcia JM, Andre F, Delord JP, Hidalgo M, et al. Evaluation of BGJ398, a fibroblast growth factor receptor 1-3 kinase inhibitor, in patients with advanced solid tumors harboring genetic alterations in fibroblast growth factor receptors: results of a global phase I, dose-escalation and dose-expansion study. J Clin Oncol. 2017;35(2):157–65.PubMedCrossRef
119.
Harding TC, Long L, Palencia S, Zhang H, Sadra A, Hestir K, et al. Blockade of nonhormonal fibroblast growth factors by FP-1039 inhibits growth of multiple types of cancer. Sci Transl Med. 2013;5(178):178ra39.PubMedCrossRef
120.
Donnell O, Goldman PJW, Gordon MS, Shih K, Choi YJ, Lu D, et al. A phase I dose-escalation study of MFGR1877S, a human monoclonal anti-fibroblast growth factor receptor 3 (FGFR3) antibody, in patients (pts) with advanced solid tumors. Eur J Cancer. 2012;48:191–2.CrossRef
121.
Gemo AT, Deshpande AM, Palencia S, Bellovin DI, Brennan TJ, Patil NS, et al. FPA144: a therapeutic antibody for treating patients with gastric cancers bearing FGFR2 gene amplification. Cancer Res. 2014;74(Suppl:5446).
Metadata
Title
FGFs/FGFRs-dependent signalling in regulation of steroid hormone receptors – implications for therapy of luminal breast cancer
Authors
Dominika Piasecka
Marcin Braun
Kamila Kitowska
Kamil Mieczkowski
Radzislaw Kordek
Rafal Sadej
Hanna Romanska
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Journal of Experimental & Clinical Cancer Research / Issue 1/2019
Electronic ISSN: 1756-9966
DOI
https://doi.org/10.1186/s13046-019-1236-6

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