FGFR‑related phenotypic and functional profile of CAFs in prognostication of breast cancer (Review)
- Authors:
- Julia Solek
- Marcin Braun
- Rafal Sadej
- Hanna M. Romanska
-
Affiliations: Department of Pathology, Chair of Oncology, Medical University of Lodz, 92‑213 Łodz, Poland, Laboratory of Molecular Enzymology and Oncology, Intercollegiate Faculty of Biotechnology, University of Gdansk and Medical University of Gdansk, 80‑384 Gdansk, Poland - Published online on: August 26, 2024 https://doi.org/10.3892/ijo.2024.5682
- Article Number: 94
-
Copyright: © Solek et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Santolla MF and Maggiolini M: The FGF/FGFR system in breast cancer: Oncogenic features and therapeutic perspectives. Cancers (Basel). 12:30292020. View Article : Google Scholar : PubMed/NCBI | |
Servetto A, Formisano L and Arteaga CL: FGFR signaling and endocrine resistance in breast cancer: Challenges for the clinical development of FGFR inhibitors. Biochim Biophys Acta Rev Cancer. 1876:1885952021. View Article : Google Scholar : PubMed/NCBI | |
Braun M, Piasecka D, Tomasik B, Mieczkowski K, Stawiski K, Zielinska A, Kopczynski J, Nejc D, Kordek R, Sadej R and Romanska HM: Hormonal receptor status determines prognostic significance of FGFR2 in invasive breast carcinoma. Cancers (Basel). 12:27132020. View Article : Google Scholar : PubMed/NCBI | |
Mieczkowski K, Kitowska K, Braun M, Galikowska-Bogut B, Gorska-Arcisz M, Piasecka D, Stawiski K, Zaczek AJ, Nejc D, Kordek R, et al: FGF7/FGFR2-JunB signalling counteracts the effect of progesterone in luminal breast cancer. Mol Oncol. 16:2823–2842. 2022. View Article : Google Scholar : PubMed/NCBI | |
Meric-Bernstam F, Bahleda R, Hierro C, Sanson M, Bridgewater J, Arkenau HT, Tran B, Kelley RK, Park JO, Javle M, et al: Futibatinib, an irreversible FGFR1-4 inhibitor, in patients with advanced solid tumors harboring FGF/FGFR aberrations: A phase I dose-expansion study. Cancer Discov. 12:402–415. 2022. View Article : Google Scholar | |
Coombes RC, Badman PD, Lozano-Kuehne JP, Liu X, Macpherson IR, Zubairi I, Baird RD, Rosenfeld N, Garcia-Corbacho J, Cresti N, et al: Results of the phase IIa RADICAL trial of the FGFR inhibitor AZD4547 in endocrine resistant breast cancer. Nat Commun. 13:32462022. View Article : Google Scholar : PubMed/NCBI | |
De Luca A, Frezzetti D, Gallo M and Normanno N: FGFR-targeted therapeutics for the treatment of breast cancer. Expert Opin Investig Drugs. 26:303–311. 2017. View Article : Google Scholar : PubMed/NCBI | |
Chew NJ, Lim Kam Sian TCC, Nguyen EV, Shin SY, Yang J, Hui MN, Deng N, McLean CA, Welm AL, Lim E, et al: Evaluation of FGFR targeting in breast cancer through interrogation of patient-derived models. Breast Cancer Res. 23:822021. View Article : Google Scholar : PubMed/NCBI | |
Ronnov-Jessen L, Petersen OW, Koteliansky VE and Bissell MJ: The origin of the myofibroblasts in breast cancer. Recapitulation of tumor environment in culture unravels diversity and implicates converted fibroblasts and recruited smooth muscle cells. J Clin Invest. 95:859–873. 1995. View Article : Google Scholar : PubMed/NCBI | |
Elenbaas B and Weinberg RA: Heterotypic signaling between epithelial tumor cells and fibroblasts in carcinoma formation. Exp Cell Res. 264:169–184. 2001. View Article : Google Scholar : PubMed/NCBI | |
Erez N, Truitt M, Olson P, Arron ST and Hanahan D: Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-kappaB-dependent manner. Cancer Cell. 17:135–147. 2010. View Article : Google Scholar : PubMed/NCBI | |
Tejada ML, Yu L, Dong J, Jung K, Meng G, Peale FV, Frantz GD, Hall L, Liang X, Gerber HP and Ferrara N: Tumor-driven paracrine platelet-derived growth factor receptor alpha signaling is a key determinant of stromal cell recruitment in a model of human lung carcinoma. Clin Cancer Res. 12:2676–2688. 2006. View Article : Google Scholar : PubMed/NCBI | |
Tian H, Callahan CA, DuPree KJ, Darbonne WC, Ahn CP, Scales SJ and de Sauvage FJ: Hedgehog signaling is restricted to the stromal compartment during pancreatic carcinogenesis. Proc Natl Acad Sci USA. 106:4254–4259. 2009. View Article : Google Scholar : PubMed/NCBI | |
Aggarwal V, Tuli HS, Varol A, Thakral F, Yerer MB, Sak K, Varol M, Jain A, Khan MA and Sethi G: Role of reactive oxygen species in cancer progression: Molecular mechanisms and recent advancements. Biomolecules. 9:7352019. View Article : Google Scholar : PubMed/NCBI | |
Direkze NC, Hodivala-Dilke K, Jeffery R, Hunt T, Poulsom R, Oukrif D, Alison MR and Wright NA: Bone marrow contribution to tumor-associated myofibroblasts and fibroblasts. Cancer Res. 64:8492–8495. 2004. View Article : Google Scholar : PubMed/NCBI | |
Kidd S, Spaeth E, Watson K, Burks J, Lu H, Klopp A, Andreeff M and Marini FC: Origins of the tumor microenvironment: Quantitative assessment of adipose-derived and bone marrow-derived stroma. PLoS One. 7:e305632012. View Article : Google Scholar : PubMed/NCBI | |
Abe R, Donnelly SC, Peng T, Bucala R and Metz CN: Peripheral blood fibrocytes: Differentiation pathway and migration to wound sites. J Immunol. 166:7556–7562. 2001. View Article : Google Scholar : PubMed/NCBI | |
Zeisberg EM, Potenta S, Xie L, Zeisberg M and Kalluri R: Discovery of endothelial to mesenchymal transition as a source for carcinoma-associated fibroblasts. Cancer Res. 67:10123–10128. 2007. View Article : Google Scholar : PubMed/NCBI | |
Timperi E, Gueguen P, Molgora M, Magagna I, Kieffer Y, Lopez-Lastra S, Sirven P, Baudrin LG, Baulande S, Nicolas A, et al: Lipid-associated macrophages are induced by cancer-associated fibroblasts and mediate immune suppression in breast cancer. Cancer Res. 82:3291–3306. 2022. View Article : Google Scholar : PubMed/NCBI | |
Nurmik M, Ullmann P, Rodriguez F, Haan S and Letellier E: In search of definitions: Cancer-associated fibroblasts and their markers. Int J Cancer. 146:895–905. 2020. View Article : Google Scholar | |
Chen X and Song E: Turning foes to friends: Targeting cancer-associated fibroblasts. Nat Rev Drug Discov. 18:99–115. 2019. View Article : Google Scholar | |
Costa A, Kieffer Y, Scholer-Dahirel A, Pelon F, Bourachot B, Cardon M, Sirven P, Magagna I, Fuhrmann L, Bernard C, et al: Fibroblast heterogeneity and immunosuppressive environment in human breast cancer. Cancer Cell. 33:463–479.e410. 2018. View Article : Google Scholar : PubMed/NCBI | |
Glabman RA, Choyke PL and Sato N: Cancer-associated fibroblasts: Tumorigenicity and targeting for cancer therapy. Cancers (Basel). 14:39062022. View Article : Google Scholar : PubMed/NCBI | |
Paulsson J and Micke P: Prognostic relevance of cancer-associated fibroblasts in human cancer. Semin Cancer Biol. 25:61–68. 2014. View Article : Google Scholar : PubMed/NCBI | |
Marchini C, Montani M, Konstantinidou G, Orrù R, Mannucci S, Ramadori G, Gabrielli F, Baruzzi A, Berton G, Merigo F, et al: Mesenchymal/stromal gene expression signature relates to basal-like breast cancers, identifies bone metastasis and predicts resistance to therapies. PLoS One. 5:e141312010. View Article : Google Scholar : PubMed/NCBI | |
Frings O, Augsten M, Tobin NP, Carlson J, Paulsson J, Pena C, Olsson E, Veerla S, Bergh J, Ostman A and Sonnhammer EL: Prognostic significance in breast cancer of a gene signature capturing stromal PDGF signaling. Am J Pathol. 182:2037–2047. 2013. View Article : Google Scholar : PubMed/NCBI | |
Lappano R, Rigiracciolo DC, Belfiore A, Maggiolini M and De Francesco EM: Cancer associated fibroblasts: Role in breast cancer and potential as therapeutic targets. Expert Opin Ther Targets. 24:559–572. 2020. View Article : Google Scholar : PubMed/NCBI | |
Fernández-Nogueira P, Mancino M, Fuster G, López-Plana A, Jauregui P, Almendro V, Enreig E, Menéndez S, Rojo F, Noguera-Castells A, et al: Tumor-associated fibroblasts promote HER2-targeted therapy resistance through FGFR2 activation. Clin Cancer Res. 26:1432–1448. 2020. View Article : Google Scholar | |
Palmieri C, Roberts-Clark D, Assadi-Sabet A, Coope RC, O'Hare M, Sunters A, Hanby A, Slade MJ, Gomm JJ, Lam EW and Coombes RC: Fibroblast growth factor 7, secreted by breast fibroblasts, is an interleukin-1beta-induced paracrine growth factor for human breast cells. J Endocrinol. 177:65–81. 2003. View Article : Google Scholar : PubMed/NCBI | |
Kalluri R: The biology and function of fibroblasts in cancer. Nat Rev Cancer. 16:582–598. 2016. View Article : Google Scholar : PubMed/NCBI | |
Cerliani JP, Guillardoy T, Giulianelli S, Vaque JP, Gutkind JS, Vanzulli SI, Martins R, Zeitlin E, Lamb CA and Lanari C: Interaction between FGFR-2, STAT5, and progesterone receptors in breast cancer. Cancer Res. 71:3720–3731. 2011. View Article : Google Scholar : PubMed/NCBI | |
Mao Y, Keller ET, Garfield DH, Shen K and Wang J: Stromal cells in tumor microenvironment and breast cancer. Cancer Metastasis Rev. 32:303–315. 2013. View Article : Google Scholar | |
Louault K, Li RR and DeClerck YA: Cancer-associated fibroblasts: Understanding their heterogeneity. Cancers (Basel). 12:31082020. View Article : Google Scholar : PubMed/NCBI | |
Shee K, Yang W, Hinds JW, Hampsch RA, Varn FS, Traphagen NA, Patel K, Cheng C, Jenkins NP, Kettenbach AN, et al: Therapeutically targeting tumor microenvironment-mediated drug resistance in estrogen receptor-positive breast cancer. J Exp Med. 215:895–910. 2018. View Article : Google Scholar : PubMed/NCBI | |
Clayton NS, Wilson AS, Laurent EP, Grose RP and Carter EP: Fibroblast growth factor-mediated crosstalk in cancer etiology and treatment. Dev Dyn. 246:493–501. 2017. View Article : Google Scholar : PubMed/NCBI | |
Zhou Z, Wu B, Tang X, Ke R and Zou Q: Comprehensive analysis of fibroblast growth factor receptor (FGFR) family genes in breast cancer by integrating online databases and bioinformatics. Med Sci Monit. 26:e9235172020. View Article : Google Scholar : PubMed/NCBI | |
Suh J, Kim DH, Lee YH, Jang JH and Surh YJ: Fibroblast growth factor-2, derived from cancer-associated fibroblasts, stimulates growth and progression of human breast cancer cells via FGFR1 signaling. Mol Carcinog. 59:1028–1040. 2020. View Article : Google Scholar : PubMed/NCBI | |
Xie Y, Su N, Yang J, Tan Q, Huang S, Jin M, Ni Z, Zhang B, Zhang D, Luo F, et al: FGF/FGFR signaling in health and disease. Signal Transduct Target Ther. 5:1812020. View Article : Google Scholar : PubMed/NCBI | |
Otranto M, Sarrazy V, Bonte F, Hinz B, Gabbiani G and Desmouliere A: The role of the myofibroblast in tumor stroma remodeling. Cell Adh Migr. 6:203–219. 2012. View Article : Google Scholar : PubMed/NCBI | |
Chakrabarti R, Lee M and Higgs HN: Multiple roles for actin in secretory and endocytic pathways. Curr Biol. 31:R603–R618. 2021. View Article : Google Scholar : PubMed/NCBI | |
Ao Z, Shah SH, Machlin LM, Parajuli R, Miller PC, Rawal S, Williams AJ, Cote RJ, Lippman ME, Datar RH and El-Ashry D: Identification of cancer-associated fibroblasts in circulating blood from patients with metastatic breast cancer. Cancer Res. 75:4681–4687. 2015. View Article : Google Scholar : PubMed/NCBI | |
Kim S, You D, Jeong Y, Yu J, Kim SW, Nam SJ and Lee JE: TP53 upregulates α-smooth muscle actin expression in tamoxifen-resistant breast cancer cells. Oncol Rep. 41:1075–1082. 2019. | |
Wang T, Srivastava S, Hartman M, Buhari SA, Chan CW, Iau P, Khin LW, Wong A, Tan SH, Goh BC and Lee SC: High expression of intratumoral stromal proteins is associated with chemotherapy resistance in breast cancer. Oncotarget. 7:55155–55168. 2016. View Article : Google Scholar : PubMed/NCBI | |
Yamashita M, Ogawa T, Zhang X, Hanamura N, Kashikura Y, Takamura M, Yoneda M and Shiraishi T: Role of stromal myofibroblasts in invasive breast cancer: Stromal expression of alpha-smooth muscle actin correlates with worse clinical outcome. Breast Cancer. 19:170–176. 2012. View Article : Google Scholar | |
Vathiotis IA, Moutafi MK, Divakar P, Aung TN, Qing T, Fernandez A, Yaghoobi V, El-Abed S, Wang Y, Guillaume S, et al: Alpha-smooth muscle actin expression in the stroma predicts resistance to trastuzumab in patients with early-stage HER2-positive breast cancer. Clin Cancer Res. 27:6156–6163. 2021. View Article : Google Scholar : PubMed/NCBI | |
Busch S, Rydén L, Stål O, Jirström K and Landberg G: Low ERK phosphorylation in cancer-associated fibroblasts is associated with tamoxifen resistance in pre-menopausal breast cancer. PLoS One. 7:e456692012. View Article : Google Scholar : PubMed/NCBI | |
Hu G, Wang S, Xu F, Ding Q, Chen W, Zhong K, Huang L and Xu Q: Tumor-infiltrating podoplanin+ fibroblasts predict worse outcome in solid tumors. Cell Physiol Biochem. 51:1041–1050. 2018. View Article : Google Scholar : PubMed/NCBI | |
Yazhou C, Wenlv S, Weidong Z and Licun W: Clinicopathological significance of stromal myofibroblasts in invasive ductal carcinoma of the breast. Tumour Biol. 25:290–295. 2004. View Article : Google Scholar | |
Bresnick AR, Weber DJ and Zimmer DB: S100 proteins in cancer. Nat Rev Cancer. 15:96–109. 2015. View Article : Google Scholar : PubMed/NCBI | |
D'Ambrosi N, Milani M and Apolloni S: S100A4 in the physiology and pathology of the central and peripheral nervous system. Cells. 10:7982021. View Article : Google Scholar : PubMed/NCBI | |
Liu S, Zhang H, Li Y, Zhang Y, Bian Y, Zeng Y, Yao X, Wan J, Chen X, Li J, et al: S100A4 enhances protumor macrophage polarization by control of PPAR-γ-dependent induction of fatty acid oxidation. J Immunother Cancer. 9:e0025482021. View Article : Google Scholar | |
Friedman G, Levi-Galibov O, David E, Bornstein C, Giladi A, Dadiani M, Mayo A, Halperin C, Pevsner-Fischer M, Lavon H, et al: Cancer-associated fibroblast compositions change with breast cancer progression linking the ratio of S100A4+ and PDPN+ CAFs clinical outcome. Nat Cancer. 1:692–708. 2020. View Article : Google Scholar : PubMed/NCBI | |
Grum-Schwensen B, Klingelhofer J, Berg CH, El-Naaman C, Grigorian M, Lukanidin E and Ambartsumian N: Suppression of tumor development and metastasis formation in mice lacking the S100A4(mts1) gene. Cancer Res. 65:3772–3780. 2005. View Article : Google Scholar : PubMed/NCBI | |
Park CK, Jung WH and Koo JS: Expression of cancer-associated fibroblast-related proteins differs between invasive lobular carcinoma and invasive ductal carcinoma. Breast Cancer Res Treat. 159:55–69. 2016. View Article : Google Scholar : PubMed/NCBI | |
de Silva Rudland S, Martin L, Roshanlall C, Winstanley J, Leinster S, Platt-Higgins A, Carroll J, West C, Barraclough R and Rudland P: Association of S100A4 and osteopontin with specific prognostic factors and survival of patients with minimally invasive breast cancer. Clin Cancer Res. 12:1192–1200. 2006. View Article : Google Scholar : PubMed/NCBI | |
Pedersen KB, Nesland JM, Fodstad O and Maelandsmo GM: Expression of S100A4, E-cadherin, alphaand beta-catenin in breast cancer biopsies. Br J Cancer. 87:1281–1286. 2002. View Article : Google Scholar : PubMed/NCBI | |
Li WL, Zhang Y, Liu BG, Du Q, Zhou CX and Tian XS: Correlation between the expression of S100A4 and the efficacy of TAC neoadjuvant chemotherapy in breast cancer. Exp Ther Med. 10:1983–1989. 2015. View Article : Google Scholar : PubMed/NCBI | |
McKiernan E, McDermott EW, Evoy D, Crown J and Duffy MJ: The role of S100 genes in breast cancer progression. Tumour Biol. 32:441–450. 2011. View Article : Google Scholar | |
Park SY, Kim HM and Koo JS: Differential expression of cancer-associated fibroblast-related proteins according to molecular subtype and stromal histology in breast cancer. Breast Cancer Res Treat. 149:727–741. 2015. View Article : Google Scholar : PubMed/NCBI | |
Donovan J, Shiwen X, Norman J and Abraham D: Platelet-derived growth factor alpha and beta receptors have overlapping functional activities towards fibroblasts. Fibrogenesis Tissue Repair. 6:102013. View Article : Google Scholar : PubMed/NCBI | |
Claesson-Welsh L, Ronnstrand L and Heldin CH: Biosynthesis and intracellular transport of the receptor for platelet-derived growth factor. Proc Natl Acad Sci USA. 84:8796–8800. 1987. View Article : Google Scholar : PubMed/NCBI | |
Lavie D, Ben-Shmuel A, Erez N and Scherz-Shouval R: Cancer-associated fibroblasts in the single-cell era. Nat Cancer. 3:793–807. 2022. View Article : Google Scholar : PubMed/NCBI | |
Pietras K, Pahler J, Bergers G and Hanahan D: Functions of paracrine PDGF signaling in the proangiogenic tumor stroma revealed by pharmacological targeting. PLoS Med. 5:e192008. View Article : Google Scholar : PubMed/NCBI | |
Paulsson J, Sjöblom T, Micke P, Pontén F, Landberg G, Heldin CH, Bergh J, Brennan DJ, Jirström K and Ostman A: Prognostic significance of stromal platelet-derived growth factor beta-receptor expression in human breast cancer. Am J Pathol. 175:334–341. 2009. View Article : Google Scholar : PubMed/NCBI | |
Paulsson J, Rydén L, Strell C, Frings O, Tobin NP, Fornander T, Bergh J, Landberg G, Stål O and Östman A: High expression of stromal PDGFRβ is associated with reduced benefit of tamoxifen in breast cancer. J Pathol Clin Res. 3:38–43. 2017. View Article : Google Scholar : PubMed/NCBI | |
Hu G, Huang L, Zhong K, Meng L, Xu F, Wang S and Zhang T: PDGFR-β+ fibroblasts deteriorate survival in human solid tumors: a meta-analysis. Aging (Albany NY). 13:13693–13707. 2021. View Article : Google Scholar : PubMed/NCBI | |
Yam C, Murthy RK, Rauch GM, Murray JL, Walters RS, Valero V, Brewster AM, Bast RC Jr, Booser DJ, Giordano SH, et al: A phase II study of imatinib mesylate and letrozole in patients with hormone receptor-positive metastatic breast cancer expressing c-kit or PDGFR-b. Invest New Drugs. 36:1103–1109. 2018. View Article : Google Scholar : PubMed/NCBI | |
Wicki A, Lehembre F, Wick N, Hantusch B, Kerjaschki D and Christofori G: Tumor invasion in the absence of epithelial-mesenchymal transition: Podoplanin-mediated remodeling of the actin cytoskeleton. Cancer Cell. 9:261–272. 2006. View Article : Google Scholar : PubMed/NCBI | |
Niemiec J, Adamczyk A, Harazin-Lechowska A, Ambicka A, Grela-Wojewoda A, Majchrzyk K, Kruczak A, Sas-Korczyńska B and Ryś J: Podoplanin-positive cancer-associated stromal fibroblasts in primary tumor and synchronous lymph node metastases of HER2-overexpressing breast carcinomas. Anticancer Res. 38:1957–1965. 2018.PubMed/NCBI | |
Schoppmann SF, Berghoff A, Dinhof C, Jakesz R, Gnant M, Dubsky P, Jesch B, Heinzl H and Birner P: Podoplanin-expressing cancer-associated fibroblasts are associated with poor prognosis in invasive breast cancer. Breast Cancer Res Treat. 134:237–244. 2012. View Article : Google Scholar : PubMed/NCBI | |
Tanaka Y, Ohno T, Kadonaga T, Kidokoro Y, Wakahara M, Nosaka K, Sakabe T, Suzuki Y, Nakamura H and Umekita Y: Podoplanin expression in cancer-associated fibroblasts predicts unfavorable prognosis in node-negative breast cancer patients with hormone receptor-positive/HER2-negative subtype. Breast Cancer. 28:822–828. 2021. View Article : Google Scholar : PubMed/NCBI | |
Pula B, Jethon A, Piotrowska A, Gomulkiewicz A, Owczarek T, Calik J, Wojnar A, Witkiewicz W, Rys J and Ugorski M, et al: Podoplanin expression by cancer-associated fibroblasts predicts poor outcome in invasive ductal breast carcinoma. Histopathology. 59:1249–1260. 2011. View Article : Google Scholar : PubMed/NCBI | |
Pula B, Wojnar A, Werynska B, Ambicka A, Kruczak A, Witkiewicz W, Ugorski M, Podhorska-Okolow M and Dziegiel P: Impact of different tumour stroma assessment methods regarding podoplanin expression on clinical outcome in patients with invasive ductal breast carcinoma. Anticancer Res. 33:1447–1455. 2013.PubMed/NCBI | |
Liu R, Li H, Liu L, Yu J and Ren X: Fibroblast activation protein: A potential therapeutic target in cancer. Cancer Biol Ther. 13:123–129. 2012. View Article : Google Scholar : PubMed/NCBI | |
Sarkar M, Nguyen T, Gundre E, Ogunlusi O, El-Sobky M, Giri B and Sarkar TR: Cancer-associated fibroblasts: The chief architect in the tumor microenvironment. Front Cell Dev Biol. 11:10890682023. View Article : Google Scholar : PubMed/NCBI | |
Lo A, Wang LCS, Scholler J, Monslow J, Avery D, Newick K, O'Brien S, Evans RA, Bajor DJ, Clendenin C, et al: Tumor-promoting desmoplasia is disrupted by depleting FAP-expressing stromal cells. Cancer Res. 75:2800–2810. 2015. View Article : Google Scholar : PubMed/NCBI | |
Tashireva LA, Denisov EV, Gerashchenko TS, Pautova DN, Bulda kov MA, Zavyalova MV, Kzhysh kowska J, Cherdyntseva NV and Perelmuter VM: Intratumoral heterogeneity of macrophages and fibroblasts in breast cancer is associated with the morphological diversity of tumor cells and contributes to lymph node metastasis. Immunobiology. 222:631–640. 2017. View Article : Google Scholar | |
Ariga N, Sato E, Ohuchi N, Nagura H and Ohtani H: Stromal expression of fibroblast activation protein/seprase, a cell membrane serine proteinase and gelatinase, is associated with longer survival in patients with invasive ductal carcinoma of breast. Int J Cancer. 95:67–72. 2001. View Article : Google Scholar : PubMed/NCBI | |
Bonneau C, Eliès A, Kieffer Y, Bourachot B, Ladoire S, Pelon F, Hequet D, Guinebretière JM, Blanchet C, Vincent-Salomon A, et al: A subset of activated fibroblasts is associated with distant relapse in early luminal breast cancer. Breast Cancer Res. 22:762020. View Article : Google Scholar : PubMed/NCBI | |
Biernacka A, Dobaczewski M and Frangogiannis NG: TGF-β signaling in fibrosis. Growth Factors. 29:196–202. 2011. View Article : Google Scholar : PubMed/NCBI | |
Shi X, Young CD, Zhou H and Wang X: Transforming growth factor-β signaling in fibrotic diseases and cancer-associated fibroblasts. Biomolecules. 10:16662020. View Article : Google Scholar | |
Casey TM, Eneman J, Crocker A, White J, Tessitore J, Stanley M, Harlow S, Bunn JY, Weaver D, Muss H and Plaut K: Cancer associated fibroblasts stimulated by transforming growth factor beta1 (TGF-beta 1) increase invasion rate of tumor cells: A population study. Breast Cancer Res Treat. 110:39–49. 2008. View Article : Google Scholar | |
Koumoundourou D, Kassimatis T, Zolota V, Tzorakoeleftherakis E, Ravazoula P, Vassiliou V, Kardamakis D and Varakis J: Prognostic significance of TGFbeta-1 and pSmad2/3 in breast cancer patients with T1-2,N0 tumours. Anticancer Res. 27:2613–2620. 2007.PubMed/NCBI | |
Liu N, Qi D, Jiang J, Zhang J and Yu C: Significance of combined TGF-β1 and survivin expression on the prognosis of patients with triple-negative breast cancer. Oncol Lett. 23:1932022. View Article : Google Scholar | |
Nakamura H, Kambe H, Egawa T, Kimura Y, Ito H, Hayashi E, Yamamoto H, Sato J and Kishimoto S: Partial purification and characterization of human hepatoma-derived growth factor. Clin Chim Acta. 183:273–284. 1989. View Article : Google Scholar : PubMed/NCBI | |
Enomoto H, Nakamura H, Liu W and Nishiguchi S: Hepatoma-derived growth factor: Its possible involvement in the progression of hepatocellular carcinoma. Int J Mol Sci. 16:14086–14097. 2015. View Article : Google Scholar : PubMed/NCBI | |
Chen X, Yun J, Fei F, Yi J, Tian R, Li S and Gan X: Prognostic value of nuclear hepatoma-derived growth factor (HDGF) localization in patients with breast cancer. Pathol Res Pract. 208:437–443. 2012. View Article : Google Scholar : PubMed/NCBI | |
Qiu L, Ma Y, Chen X, Zhou L, Zhang H, Zhong G, Zhang L and Tang J: Heparin-binding growth factor (HDGF) drives radioresistance in breast cancer by activating the STAT3 signaling pathway. J Transl Med. 19:3442021. View Article : Google Scholar : PubMed/NCBI | |
Anderberg C and Pietras K: On the origin of cancer-associated fibroblasts. Cell Cycle. 8:1461–1462. 2009. View Article : Google Scholar : PubMed/NCBI | |
Kuzet SE and Gaggioli C: Fibroblast activation in cancer: When seed fertilizes soil. Cell Tissue Res. 365:607–619. 2016. View Article : Google Scholar : PubMed/NCBI | |
Jansson S, Aaltonen K, Bendahl PO, Falck AK, Karlsson M, Pietras K and Rydén L: The PDGF pathway in breast cancer is linked to tumour aggressiveness, triple-negative subtype and early recurrence. Breast Cancer Res Treat. 169:231–241. 2018. View Article : Google Scholar : PubMed/NCBI | |
Seymour L, Dajee D and Bezwoda WR: Tissue platelet derived-growth factor (PDGF) predicts for shortened survival and treatment failure in advanced breast cancer. Breast Cancer Res Treat. 26:247–252. 1993. View Article : Google Scholar : PubMed/NCBI | |
Liubomirski Y, Lerrer S, Meshel T, Rubinstein-Achiasaf L, Morein D, Wiemann S, Körner C and Ben-Baruch A: Tumor-stroma-inflammation networks promote pro-metastatic chemokines and aggressiveness characteristics in triple-negative breast cancer. Front Immunol. 10:7572019. View Article : Google Scholar : PubMed/NCBI | |
Lin S, Sun L, Lyu X, Ai X, Du D, Su N, Li H, Zhang L, Yu J and Yuan S: Lactate-activated macrophages induced aerobic glycolysis and epithelial-mesenchymal transition in breast cancer by regulation of CCL5-CCR5 axis: A positive metabolic feedback loop. Oncotarget. 8:110426–110443. 2017. View Article : Google Scholar | |
Qian BZ, Li J, Zhang H, Kitamura T, Zhang J, Campion LR, Kaiser EA, Snyder LA and Pollard JW: CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature. 475:222–225. 2011. View Article : Google Scholar : PubMed/NCBI | |
Zhou B, Sun C, Li N, Shan W, Lu H, Guo L, Guo E, Xia M, Weng D, Meng L, et al: Cisplatin-induced CCL5 secretion from CAFs promotes cisplatin-resistance in ovarian cancer via regulation of the STAT3 and PI3K/Akt signaling pathways. Int J Oncol. 48:2087–2097. 2016. View Article : Google Scholar : PubMed/NCBI | |
Yao M, Yu E, Staggs V, Fan F and Cheng N: Elevated expression of chemokine C-C ligand 2 in stroma is associated with recurrent basal-like breast cancers. Mod Pathol. 29:810–823. 2016. View Article : Google Scholar : PubMed/NCBI | |
Heiskala M, Leidenius M, Joensuu K and Heikkilä P: High expression of CCL2 in tumor cells and abundant infiltration with CD14 positive macrophages predict early relapse in breast cancer. Virchows Arch. 474:3–12. 2019. View Article : Google Scholar | |
Yamaguchi M, Takagi K, Narita K, Miki Y, Onodera Y, Miyashita M, Sasano H and Suzuki T: Stromal CCL5 promotes breast cancer progression by interacting with CCR3 in tumor cells. Int J Mol Sci. 22:19182021. View Article : Google Scholar : PubMed/NCBI | |
Yaal-Hahoshen N, Shina S, Leider-Trejo L, Barnea I, Shabtai EL, Azenshtein E, Greenberg I, Keydar I and Ben-Baruch A: The chemokine CCL5 as a potential prognostic factor predicting disease progression in stage II breast cancer patients. Clin Cancer Res. 12:4474–4480. 2006. View Article : Google Scholar : PubMed/NCBI | |
Liu S, Dontu G, Mantle ID, Patel S, Ahn NS, Jackson KW, Suri P and Wicha MS: Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 66:6063–6071. 2006. View Article : Google Scholar : PubMed/NCBI | |
Arnold KM, Pohlig RT and Sims-Mourtada J: Co-activation of Hedgehog and Wnt signaling pathways is associated with poor outcomes in triple negative breast cancer. Oncol Lett. 14:5285–5292. 2017.PubMed/NCBI | |
Beenken A and Mohammadi M: The FGF family: Biology, pathophysiology and therapy. Nat Rev Drug Discov. 8:235–253. 2009. View Article : Google Scholar : PubMed/NCBI | |
Babina IS and Turner NC: Advances and challenges in targeting FGFR signalling in cancer. Nat Rev Cancer. 17:318–332. 2017. View Article : Google Scholar : PubMed/NCBI | |
Colomer R, Aparicio J, Montero S, Guzmán C, Larrodera L and Cortés-Funes H: Low levels of basic fibroblast growth factor (bFGF) are associated with a poor prognosis in human breast carcinoma. Br J Cancer. 76:1215–1220. 1997. View Article : Google Scholar : PubMed/NCBI | |
Linderholm BK, Lindh B, Beckman L, Erlanson M, Edin K, Travelin B, Bergh J, Grankvist K and Henriksson R: Prognostic correlation of basic fibroblast growth factor and vascular endothelial growth factor in 1307 primary breast cancers. Clin Breast Cancer. 4:340–347. 2003. View Article : Google Scholar | |
Surowiak P, Murawa D, Materna V, Maciejczyk A, Pudelko M, Ciesla S, Breborowicz J, Murawa P, Zabel M, Dietel M and Lage H: Occurence of stromal myofibroblasts in the invasive ductal breast cancer tissue is an unfavourable prognostic factor. Anticancer Res. 27:2917–2924. 2007.PubMed/NCBI | |
Yiangou C, Gomm JJ, Coope RC, Law M, Luqmani YA, Shousha S, Coombes RC and Johnston CL: Fibroblast growth factor 2 in breast cancer: Occurrence and prognostic significance. Br J Cancer. 75:28–33. 1997. View Article : Google Scholar : PubMed/NCBI | |
Granato AM, Nanni O, Falcini F, Folli S, Mosconi G, De Paola F, Medri L, Amadori D and Volpi A: Basic fibroblast growth factor and vascular endothelial growth factor serum levels in breast cancer patients and healthy women: Useful as diagnostic tools? Breast Cancer Res. 6:R38–R45. 2004. View Article : Google Scholar : | |
Faridi A, Rudlowski C, Biesterfeld S, Schuh S, Rath W and Schröder W: Long-term follow-up and prognostic significance of angiogenic basic fibroblast growth factor (bFGF) expression in patients with breast cancer. Pathol Res Pract. 198:1–5. 2002. View Article : Google Scholar : PubMed/NCBI | |
Smith K, Fox SB, Whitehouse R, Taylor M, Greenall M, Clarke J and Harris AL: Upregulation of basic fibroblast growth factor in breast carcinoma and its relationship to vascular density, oestrogen receptor, epidermal growth factor receptor and survival. Ann Oncol. 10:707–713. 1999. View Article : Google Scholar : PubMed/NCBI | |
Meijer D, Sieuwerts AM, Look MP, van Agthoven T, Foekens JA and Dorssers LCJ: Fibroblast growth factor receptor 4 predicts failure on tamoxifen therapy in patients with recurrent breast cancer. Endocr Relat Cancer. 15:101–111. 2008. View Article : Google Scholar : PubMed/NCBI | |
Ivanović V, Demajo M, Krtolica K, Krajnović M, Konstantinović M, Baltić V, Prtenjak G, Stojiljković B, Breberina M, Nesković-Konstantinović Z, et al: Elevated plasma TGF-beta1 levels correlate with decreased survival of metastatic breast cancer patients. Clin Chim Acta. 371:191–193. 2006. View Article : Google Scholar | |
El-Abd E, El-Tahan R, Fahmy L, Zaki S, Faid W, Sobhi A, Kandil K and El-Kwisky F: Serum metastasin mRNA is an important survival predictor in breast cancer. Br J Biomed Sci. 65:90–94. 2008. View Article : Google Scholar : PubMed/NCBI | |
Tripsianis G, Papadopoulou E, Romanidis K, Katotomichelakis M, Anagnostopoulos K, Kontomanolis E, Botaitis S, Tentes I and Kortsaris A: Overall survival and clinicopathological characteristics of patients with breast cancer in relation to the expression pattern of HER-2, IL-6, TNF-α and TGF-b1. Asian Pac J Cancer Prev. 14:6813–6820. 2013. View Article : Google Scholar | |
Zhu X, Xu M, Zhao X, Shen F, Ruan C and Zhao Y: The detection of plasma soluble podoplanin of patients with breast cancer and its clinical signification. Cancer Manag Res. 12:13207–13214. 2020. View Article : Google Scholar : | |
Tripsianis G, Papadopoulou E, Anagnostopoulos K, Botaitis S, Katotomichelakis M, Romanidis K, Kontomanolis E, Tentes I and Kortsaris A: Coexpression of IL-6 and TNF-α: Prognostic significance on breast cancer outcome. Neoplasma. 61:205–212. 2014. View Article : Google Scholar | |
Cai S, Zheng J, Song H, Wu H and Cai W: Relationship between serum TGF-β 1, MMP-9 and IL-1β and pathological features and prognosis in breast cancer. Front Genet. 13:10953382023. View Article : Google Scholar | |
Al-Ashkar N and Zetoune AB: S100A14 serum level and its correlation with prognostic factors in breast cancer. J Egypt Natl Canc Inst. 32:372020. View Article : Google Scholar : PubMed/NCBI | |
Yahia S, Tahari Z, Medjdoub A, Tahari FZ, Bessaih N, Messatfa M, Deblaoui F, Raiah M, Ouldcadi H, Seddiki S and Sahraoui T: Expression profile of interleukin-6, 4-hydroxy-2-nonenal, and hypoxia-inducible factor 1-α in women with breast cancer and their association with clinicopathological parameters. Contemp Oncol (Pozn). 27:14–21. 2023. | |
Panis C, Herrera AC, Victorino VJ, Aranome AM and Cecchini R: Screening of circulating TGF-β levels and its clinicopathological significance in human breast cancer. Anticancer Res. 33:737–742. 2013.PubMed/NCBI | |
Milovanović J, Todorović-Raković N and Radulovic M: Interleukin-6 and interleukin-8 serum levels in prognosis of hormone-dependent breast cancer. Cytokine. 118:93–98. 2019. View Article : Google Scholar | |
Wang RX, Ji P, Gong Y, Shao ZM and Chen S: Value of CXCL8-CXCR1/2 axis in neoadjuvant chemotherapy for triple-negative breast cancer patients: A retrospective pilot study. Breast Cancer Res Treat. 181:561–570. 2020. View Article : Google Scholar : PubMed/NCBI | |
Paccagnella M, Abbona A, Michelotti A, Geuna E, Ruatta F, Landucci E, Denaro N, Vanella P, Lo Nigro C, Galizia D, et al: Circulating cytokines in metastatic breast cancer patients select different prognostic groups and patients who might benefit from treatment beyond progression. Vaccines (Basel). 10:782022. View Article : Google Scholar : PubMed/NCBI | |
Denys H, Derycke L, Hendrix A, Westbroek W, Gheldof A, Narine K, Pauwels P, Gespach C, Bracke M and De Wever O: Differential impact of TGF-beta and EGF on fibroblast differentiation and invasion reciprocally promotes colon cancer cell invasion. Cancer Lett. 266:263–274. 2008. View Article : Google Scholar : PubMed/NCBI | |
Kjær IM, Olsen DA, Brandslund I, Bechmann T, Jakobsen EH, Bogh SB and Madsen JS: Prognostic impact of serum levels of EGFR and EGFR ligands in early-stage breast cancer. Sci Rep. 10:165582020. View Article : Google Scholar : PubMed/NCBI |