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Original Articles

Effects of prolonged treatment of TGF-βR inhibitor SB431542 on radiation-induced signaling in breast cancer cells

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Pages 1630-1644 | Received 23 Jun 2021, Accepted 31 Mar 2022, Published online: 13 May 2022

References

  • Anestakis D, Petanidis S, Kalyvas S, Nday CM, Tsave O, Kioseoglou E, Salifoglou A. 2015. Mechanisms and applications of interleukins in cancer immunotherapy. Int J Mol Sci. 16(1):1691–710.
  • Anscher MS, Crocker IR, Jirtle RL. 1990. Transforming growth factor-beta 1 expression in irradiated liver. Radiat Res. 122(1):77–85.
  • Atun R, Jaffray DA, Barton MB, Bray F, Baumann M, Vikram B, Hanna TP, Knaul FM, Lievens Y, Lui TY, et al. 2015. Expanding global access to radiotherapy. Lancet Oncol. 16(10):1153–1186.
  • Avtanski DB, Nagalingam A, Bonner MY, Arbiser JL, Saxena NK, Sharma D. 2014. Honokiol inhibits epithelial-mesenchymal transition in breast cancer cells by targeting signal transducer and activator of transcription 3/Zeb1/E-cadherin axis. Mol Oncol. 8(3):565–580.
  • Bai M, Ma X, Li X, Wang X, Mei Q, Li X, Wu Z, Han W. 2015. The Accomplices of NF-κB Lead to Radioresistance. Curr Protein Pept Sci. 16(4):279–294.
  • Barthelemy-Brichant N, Bosquée L, Cataldo D, Corhay J-L, Gustin M, Seidel L, Thiry A, Ghaye B, Nizet M, Albert A, et al. 2004. Increased IL-6 and TGF-beta1 concentrations in bronchoalveolar lavage fluid associated with thoracic radiotherapy. Int J Radiat Oncol Biol Phys. 58(3):758–767.
  • Baugé C, Cauvard O, Leclercq S, Galéra P, Boumédiene K. 2011. Modulation of transforming growth factor beta signalling pathway genes by transforming growth factor beta in human osteoarthritic chondrocytes: involvement of Sp1 in both early and late response cells to transforming growth factor beta. Arthritis Res Ther. 13(1):R23.
  • Baumann M, Krause M, Overgaard J, Debus J, Bentzen SM, Daartz J, Richter C, Zips D, Bortfeld T. 2016. Radiation oncology in the era of precision medicine. Nat Rev Cancer. 16(4):234–249.
  • Belenkov AI, Shenouda G, Rizhevskaya E, Cournoyer D, Belzile JP, Souhami L, Devic S, Chow TY. 2004. Erythropoietin induces cancer cell resistance to ionizing radiation and to cisplatin. Mol Cancer Ther. 3(12):1525–1532.
  • Benigni A, Zoja C, Corna D, Zatelli C, Conti S, Campana M, Gagliardini E, Rottoli D, Zanchi C, Abbate M, et al. 2003. Add-on anti-TGF-beta antibody to ACE inhibitor arrests progressive diabetic nephropathy in the rat. J Am Soc Nephrol. 14(7):1816–1824.
  • Biswas S, Guix M, Rinehart C, Dugger TC, Chytil A, Moses HL, Freeman ML, Arteaga CL. 2007. Inhibition of TGF-beta with neutralizing antibodies prevents radiation-induced acceleration of metastatic cancer progression. J Clin Invest. 117(5):1305–1313.
  • Bogdahn U, Hau P, Stockhammer G, Venkataramana NK, Mahapatra AK, Suri A, Balasubramaniam A, Nair S, Oliushine V, Parfenov V, Trabedersen Glioma Study Group, et al. 2011. Targeted therapy for high-grade glioma with the TGF-β2 inhibitor trabedersen: results of a randomized and controlled phase IIb study. Neuro Oncol. 13(1):132–142.
  • Canney PA, Dean S. 1990. Transforming growth factor beta: a promotor of late connective tissue injury following radiotherapy? Br J Radiol. 63(752):620–623.
  • Cataldi A, di Giacomo V, Rapino M, Genovesi D, Rana RA. 2006. Cyclic nucleotide Response Element Binding protein (CREB) activation promotes survival signal in human K562 erythroleukemia cells exposed to ionising radiation/etoposide combined treatment. J Radiat Res. 47(2):113–120.
  • Chakraborty P, George JT, Tripathi S, Levine H, Jolly MK. 2020. Comparative Study of Transcriptomics-Based Scoring Metrics for the Epithelial-Hybrid-Mesenchymal Spectrum [10.3389/fbioe.2020.00220]. Front Bioeng Biotechnol. 8:220.
  • Connolly EC, Saunier EF, Quigley D, Luu MT, De Sapio A, Hann B, Yingling JM, Akhurst RJ. 2011. Outgrowth of drug-resistant carcinomas expressing markers of tumor aggression after long-term TβRI/II kinase inhibition with LY2109761. Cancer Res. 71(6):2339–2349.
  • Cui J, Placzek WJ. 2018. Post-transcriptional regulation of anti-apoptotic BCL2 family members. Int J Mol Sci. 19(1):308–330.
  • Derynck R, Zhang YE. 2003. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature. 425(6958):577–584.
  • Domina EA, Philchenkov A, Dubrovska A. 2018. Individual Response to Ionizing Radiation and Personalized Radiotherapy. Crit Rev Oncog. 23(1-2):69–92.
  • Dong W, Sun S, Cao X, Cui Y, Chen A, Li X, Zhang J, Cao J, Wang Y. 2017. Exposure to TNF‑α combined with TGF‑β induces carcinogenesis in vitro via NF-κB/Twist axis. Oncol Rep. 37(3):1873–1882.
  • Duan D, Derynck R. 2019. Transforming growth factor-β (TGF-β)-induced up-regulation of TGF-β receptors at the cell surface amplifies the TGF-β response. J Biol Chem. 294(21):8490–8504.
  • Feng H, Xiang H, Mao YW, Wang J, Liu JP, Huang XQ, Liu Y, Liu SJ, Luo C, Zhang XJ, et al. 2004. Human Bcl-2 activates ERK signaling pathway to regulate activating protein-1, lens epithelium-derived growth factor and downstream genes. Oncogene. 23(44):7310–7321.
  • Flavell RA, Sanjabi S, Wrzesinski SH, Licona-Limón P. 2010. The polarization of immune cells in the tumour environment by TGFbeta. Nat Rev Immunol. 10(8):554–567.
  • Grdina DJ, Murley JS, Miller RC, Woloschak GE, Li JJ. 2015. NFκB and Survivin-Mediated Radio-Adaptive Response. Radiat Res. 183(4):391–397.
  • Gregory PA, Bracken CP, Smith E, Bert AG, Wright JA, Roslan S, Morris M, Wyatt L, Farshid G, Lim YY, et al. 2011. An autocrine TGF-beta/ZEB/miR-200 signaling network regulates establishment and maintenance of epithelial-mesenchymal transition. Mol Biol Cell. 22(10):1686–1698.
  • Halder SK, Beauchamp RD, Datta PK. 2005. A specific inhibitor of TGF-beta receptor kinase, SB-431542, as a potent antitumor agent for human cancers. Neoplasia. 7(5):509–521.
  • Huang S, Xie K, Bucana CD, Ullrich SE, Bar-Eli M. 1996. Interleukin 10 suppresses tumor growth and metastasis of human melanoma cells: potential inhibition of angiogenesis. Clin Cancer Res. 2(12):1969–1979.
  • Hui L, Zheng Y, Yan Y, Bargonetti J, Foster DA. 2006. Mutant p53 in MDA-MB-231 breast cancer cells is stabilized by elevated phospholipase D activity and contributes to survival signals generated by phospholipase D. Oncogene. 25(55):7305–7310.
  • Inman GJ, Nicolás FJ, Callahan JF, Harling JD, Gaster LM, Reith AD, Laping NJ, Hill CS. 2002. SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol Pharmacol. 62(1):65–74.
  • Jolly MK, Boareto M, Huang B, Jia D, Lu M, Ben-Jacob E, Onuchic JN, Levine H. 2015. Implications of the Hybrid Epithelial/Mesenchymal Phenotype in Metastasis. Front Oncol. 5:155.
  • Jolly MK, Somarelli JA, Sheth M, Biddle A, Tripathi SC, Armstrong AJ, Hanash SM, Bapat SA, Rangarajan A, Levine H. 2019. Hybrid epithelial/mesenchymal phenotypes promote metastasis and therapy resistance across carcinomas. Pharmacol Ther. 194:161–184.
  • Kale J, Osterlund EJ, Andrews DW. 2018. BCL-2 family proteins: changing partners in the dance towards death. Cell Death Differ. 25(1):65–80.
  • Kim HS, Kim SC, Kim SJ, Park CH, Jeung HC, Kim YB, Ahn JB, Chung HC, Rha SY. 2012. Identification of a radiosensitivity signature using integrative metaanalysis of published microarray data for NCI-60 cancer cells. BMC Genomics. 13:348.
  • Kim JH, Kim JH, Lee GE, Kim SW, Chung IK. 2003. Identification of a quinoxaline derivative that is a potent telomerase inhibitor leading to cellular senescence of human cancer cells. Biochem J. 373(Pt 2):523–529.
  • Kundu N, Beaty TL, Jackson MJ, Fulton AM. 1996. Antimetastatic and antitumor activities of interleukin 10 in a murine model of breast cancer. J Natl Cancer Inst. 88(8):536–541.
  • Li YL, Chang JT, Lee LY, Fan KH, Lu YC, Li YC, Chiang CH, You GR, Chen HY, Cheng AJ. 2017. GDF15 contributes to radioresistance and cancer stemness of head and neck cancer by regulating cellular reactive oxygen species via a SMAD-associated signaling pathway. Oncotarget. 8(1):1508–1528.
  • Llorens MC, Lorenzatti G, Cavallo NL, Vaglienti MV, Perrone AP, Carenbauer AL, Darling DS, Cabanillas AM. 2016. Phosphorylation Regulates Functions of ZEB1 Transcription Factor. J Cell Physiol. 231(10):2205–2217.
  • Long J, Zuo D, Park M. 2005. Pc2-mediated sumoylation of Smad-interacting protein 1 attenuates transcriptional repression of E-cadherin. J Biol Chem. 280(42):35477–35489.
  • Massagué J. 1998. TGF-beta signal transduction. Annu Rev Biochem. 67:753–791.
  • Mourskaia AA, Dong Z, Ng S, Banville M, Zwaagstra JC, O'Connor-McCourt MD, Siegel PM. 2009. Transforming growth factor-beta1 is the predominant isoform required for breast cancer cell outgrowth in bone. Oncogene. 28(7):1005–1015.
  • Munro AJ. 2009. Bystander effects and their implications for clinical radiotherapy. J Radiol Prot. 29(2A):A133–142.
  • Nam J-S, Suchar AM, Kang M-J, Stuelten CH, Tang B, Michalowska AM, Fisher LW, Fedarko NS, Jain A, Pinkas J, et al. 2006. Bone sialoprotein mediates the tumor cell-targeted prometastatic activity of transforming growth factor beta in a mouse model of breast cancer. Cancer Res. 66(12):6327–6335.
  • Noordhuis MG, Eijsink JJ, Ten Hoor KA, Roossink F, Hollema H, Arts HJ, Pras E, Maduro JH, Reyners AK, de Bock GH, et al. 2009. Expression of epidermal growth factor receptor (EGFR) and activated EGFR predict poor response to (chemo)radiation and survival in cervical cancer. Clin Cancer Res. 15(23):7389–7397.
  • Ozeki M, Tamae D, Hou DX, Wang T, Lebon T, Spitz DR, Li JJ. 2004. Response of cyclin B1 to ionizing radiation: regulation by NF-kappaB and mitochondrial antioxidant enzyme MnSOD. Anticancer Res. 24(5A):2657–2663.
  • Peinado H, Olmeda D, Cano A. 2007. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer. 7(6):415–428.
  • Ricca A, Biroccio A, Del Bufalo D, Mackay AR, Santoni A, Cippitelli M. 2000. bcl-2 over-expression enhances NF-kappaB activity and induces mmp-9 transcription in human MCF7(ADR) breast-cancer cells. Int J Cancer. 86(2):188–196.
  • Rübe CE, Wilfert F, Uthe D, Schmid KW, Knoop R, Willich N, Schuck A, Rübe C. 2002. Modulation of radiation-induced tumour necrosis factor alpha (TNF-alpha) expression in the lung tissue by pentoxifylline. Radiother Oncol. 64(2):177–187.
  • Sanders YY, Cui Z, Le Saux CJ, Horowitz JC, Rangarajan S, Kurundkar A, Antony VB, Thannickal VJ. 2015. SMAD-independent down-regulation of caveolin-1 by TGF-β: effects on proliferation and survival of myofibroblasts. PLoS One. 10(2):e0116995.
  • Schiavoni G, Gabriele L, Mattei F. 2013. The tumor microenvironment: a pitch for multiple players. Front Oncol. 3:90.
  • Schultz N, Marenstein DR, De Angelis DA, Wang WQ, Nelander S, Jacobsen A, Marks DS, Massagué J, Sander C. 2011. Off-target effects dominate a large-scale RNAi screen for modulators of the TGF-β pathway and reveal microRNA regulation of TGFBR2. Silence. 2:3.
  • Seo N, Hayakawa S, Takigawa M, Tokura Y. 2001. Interleukin-10 expressed at early tumour sites induces subsequent generation of CD4(+) T-regulatory cells and systemic collapse of antitumour immunity. Immunology. 103(4):449–457.
  • Shirakihara T, Saitoh M, Miyazono K. 2007. Differential regulation of epithelial and mesenchymal markers by deltaEF1 proteins in epithelial mesenchymal transition induced by TGF-beta. Mol Biol Cell. 18(9):3533–3544.
  • Sinha D, Saha P, Samanta A, Bishayee A. 2020. Emerging concepts of hybrid epithelial-to-mesenchymal transition in cancer progression. Biomolecules. 10(11):1561.
  • Stuelten CH, DaCosta Byfield S, Arany PR, Karpova TS, Stetler-Stevenson WG, Roberts AB. 2005. Breast cancer cells induce stromal fibroblasts to express MMP-9 via secretion of TNF-alpha and TGF-beta. J Cell Sci. 118(Pt 10):2143–2153.
  • Sun Y, Cheng MK, Griffiths TR, Mellon JK, Kai B, Kriajevska M, Manson MM. 2013. Inhibition of STAT signalling in bladder cancer by diindolylmethane: relevance to cell adhesion, migration and proliferation. Curr Cancer Drug Targets. 13(1):57–68.
  • Teixeira AF, Ten Dijke P, Zhu HJ. 2020. On-target anti-TGF-β therapies are not succeeding in clinical cancer treatments: what are remaining challenges? Front Cell Dev Biol. 8(605):605–623.
  • Theys J, Yahyanejad S, Habets R, Span P, Dubois L, Paesmans K, Kattenbeld B, Cleutjens J, Groot AJ, Schuurbiers O, et al. 2013. High NOTCH activity induces radiation resistance in non small cell lung cancer. Radiother Oncol. 108(3):440–445.
  • Thuault S, Tan EJ, Peinado H, Cano A, Heldin CH, Moustakas A. 2008. HMGA2 and Smads co-regulate SNAIL1 expression during induction of epithelial-to-mesenchymal transition. J Biol Chem. 283(48):33437–33446.
  • Voboril R, Weberova-Voborilova J. 2007. Sensitization of colorectal cancer cells to irradiation by IL-4 and IL-10 is associated with inhibition of NF-kappaB. Neoplasma. 54(6):495–502.
  • Wang SS, Jiang J, Liang XH, Tang YL. 2015. Links between cancer stem cells and epithelial-mesenchymal transition. Onco Targets Ther. 8:2973–2980.
  • Wang LP, Wang YW, Wang BZ, Sun GM, Wang XY, Xu JL. 2014. Expression of interleukin-17A in lung tissues of irradiated mice and the influence of dexamethasone. ScientificWorldJournal. 2014:251067.
  • Wang X, Zhang X, Qiu C, Yang N. 2020. STAT3 contributes to radioresistance in cancer. Front Oncol. 10:1120.
  • Yadav P, Pandey VK, Shankar BS. 2021. Proteomic analysis of radio-resistant breast cancer xenografts: Increased TGF-β signaling and metabolism. Cell Biol Int. 45(4):804–819.
  • Yadav P, Shankar BS. 2019. Radio resistance in breast cancer cells is mediated through TGF-β signalling, hybrid epithelial-mesenchymal phenotype and cancer stem cells. Biomed Pharmacother. 111:119–130.
  • Zhang M, Kleber S, Röhrich M, Timke C, Han N, Tuettenberg J, Martin-Villalba A, Debus J, Peschke P, Wirkner U, et al. 2011. Blockade of TGF-β signaling by the TGFβR-I kinase inhibitor LY2109761 enhances radiation response and prolongs survival in glioblastoma. Cancer Res. 71(23):7155–7167.
  • Zhang H, Wang YA, Meng A, Yan H, Wang X, Niu J, Li J, Wang H. 2013. Inhibiting TGFβ1 has a protective effect on mouse bone marrow suppression following ionizing radiation exposure in vitro. J Radiat Res. 54(4):630–636.
  • Zhang P, Wei Y, Wang L, Debeb BG, Yuan Y, Zhang J, Yuan J, Wang M, Chen D, Sun Y, et al. 2014. ATM-mediated stabilization of ZEB1 promotes DNA damage response and radioresistance through CHK1. Nat Cell Biol. 16(9):864–875.
  • Zhao Y, Wang L, Huang Q, Jiang Y, Wang J, Zhang L, Tian Y, Yang H. 2016. Radiosensitization of Non-Small Cell Lung Cancer Cells by Inhibition of TGF-β1 Signaling With SB431542 Is Dependent on p53 Status. Oncol Res. 24(1):1–7.
  • Zheng G, Ma Y, Zou Y, Yin A, Li W, Dong D. 2018. HCMDB: the human cancer metastasis database. Nucleic Acids Res. 46(D1):D950–D955.
  • Zhong H, Chiles K, Feldser D, Laughner E, Hanrahan C, Georgescu MM, Simons JW, Semenza GL. 2000. Modulation of hypoxia-inducible factor 1alpha expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: implications for tumor angiogenesis and therapeutics. Cancer Res. 60(6):1541–1545.
  • Zhou HQ, Liu MS, Deng TB, Xie PB, Wang W, Shao T, Wu Y, Zhang P. 2019. The TGF-β/Smad Pathway Inhibitor SB431542 Enhances The Antitumor Effect Of Radiofrequency Ablation On Bladder Cancer Cells. Onco Targets Ther. 12:7809–7821.

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