Blocking C-Raf alleviated high-dose small-volume radiation-induced epithelial mesenchymal transition in mice lung.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
07 07 2020
Historique:
received: 01 11 2019
accepted: 12 06 2020
entrez: 9 7 2020
pubmed: 9 7 2020
medline: 15 12 2020
Statut: epublish

Résumé

The goal of this study was to develop a potential druggable target for lung injury after SABR through the small animal model. Utilising the model, a radiation dose of 70 Gy or 90 Gy was focally (small volume) delivered to the left lung of mice. The highly expressed phosphorylation form of C-Raf was discovered through a protein array experiment, with the protein being extracted from the area of radiated mouse lung tissue, and was confirmed by IHC and western blot. C-Raf activation, along with morphological change and EMT (Epithelial to Mesenchymal Transition) marker expression, was observed after radiation to the mouse type II alveolar cell line MLE-12. C-Raf inhibitor GW5074 was able to reverse the EMT in cells effectively, and was found to be dependent on Twist1 expression. In the animal experiment, pretreatment of GW5074 alleviated EMT and lung injury after 70 Gy radiation was focally delivered to the lung of mice. Conclusively, these results demonstrate that C-Raf inhibitor GW5074 inhibits high-dose small-volume radiation-induced EMT via the C-Raf/Twist1 signalling pathway in mice. Therefore, pharmacological C-Raf inhibitors may be used effectively as inhibitors of SABR-induced lung fibrosis.

Identifiants

pubmed: 32636458
doi: 10.1038/s41598-020-68175-z
pii: 10.1038/s41598-020-68175-z
pmc: PMC7341876
doi:

Substances chimiques

Indoles 0
Phenols 0
Proto-Oncogene Proteins c-raf EC 2.7.11.1
Raf1 protein, mouse EC 2.7.11.1
5-iodo-3-((3,5-dibromo-4-hydroxyphenyl)methylene)-2-indolinone P0LE4QW0S6

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

11158

Références

Videtic, G. M. & Stephans, K. L. The role of stereotactic body radiotherapy in the management of non-small cell lung cancer: an emerging standard for the medically inoperable patient?. Curr. Oncol. Rep. 12, 235–241. https://doi.org/10.1007/s11912-010-0108-1 (2010).
doi: 10.1007/s11912-010-0108-1 pubmed: 20446066
Choi, S. H. et al. A hypoxia-induced vascular endothelial-to-mesenchymal transition in development of radiation-induced pulmonary fibrosis. Clin. Cancer Res. 21, 3716–3726. https://doi.org/10.1158/1078-0432.CCR-14-3193 (2015).
doi: 10.1158/1078-0432.CCR-14-3193 pubmed: 25910951
Farhood, B. et al. Intercellular communications-redox interactions in radiation toxicity; potential targets for radiation mitigation. J. Cell Commun. Signal 13, 3–16. https://doi.org/10.1007/s12079-018-0473-3 (2019).
doi: 10.1007/s12079-018-0473-3 pubmed: 29911259
Willis, B. C., DuBois, R. M. & Borok, Z. Epithelial origin of myofibroblasts during fibrosis in the lung. Proc. Am. Thorac. Soc. 3, 377–382. https://doi.org/10.1513/pats.200601-004TK (2006).
doi: 10.1513/pats.200601-004TK pubmed: 16738204 pmcid: 2658689
Radisky, D. C. Epithelial-mesenchymal transition. J. Cell Sci. 118, 4325–4326. https://doi.org/10.1242/jcs.02552 (2005).
doi: 10.1242/jcs.02552 pubmed: 16179603
Balli, D. et al. Foxm1 transcription factor is required for lung fibrosis and epithelial-to-mesenchymal transition. EMBO J. 32, 231–244. https://doi.org/10.1038/emboj.2012.336 (2013).
doi: 10.1038/emboj.2012.336 pubmed: 23288041 pmcid: 3553386
Hong, Z. Y. et al. Development of a small animal model to simulate clinical stereotactic body radiotherapy-induced central and peripheral lung injuries. J. Radiat. Res. 55, 648–657. https://doi.org/10.1093/jrr/rrt234 (2014).
doi: 10.1093/jrr/rrt234 pubmed: 24556815 pmcid: 4099992
Hong, Z. Y., Song, K. H., Yoon, J. H., Cho, J. & Story, M. D. An experimental model-based exploration of cytokines in ablative radiation-induced lung injury in vivo and in vitro. Lung 193, 409–419. https://doi.org/10.1007/s00408-015-9705-y (2015).
doi: 10.1007/s00408-015-9705-y pubmed: 25749666
Reimann, T. et al. Transforming growth factor-beta1 induces activation of Ras, Raf-1, MEK and MAPK in rat hepatic stellate cells. FEBS Lett. 403, 57–60. https://doi.org/10.1016/s0014-5793(97)00024-0 (1997).
doi: 10.1016/s0014-5793(97)00024-0 pubmed: 9038360
Axmann, A., Seidel, D., Reimann, T., Hempel, U. & Wenzel, K. W. Transforming growth factor-beta1-induced activation of the Raf-MEK-MAPK signaling pathway in rat lung fibroblasts via a PKC-dependent mechanism. Biochem. Biophys. Res. Commun. 249, 456–460. https://doi.org/10.1006/bbrc.1998.9188 (1998).
doi: 10.1006/bbrc.1998.9188 pubmed: 9712718
Morrison, D. K., Kaplan, D. R., Rapp, U. & Roberts, T. M. Signal transduction from membrane to cytoplasm: growth factors and membrane-bound oncogene products increase Raf-1 phosphorylation and associated protein kinase activity. Proc. Natl. Acad. Sci. USA 85, 8855–8859. https://doi.org/10.1073/pnas.85.23.8855 (1988).
doi: 10.1073/pnas.85.23.8855 pubmed: 3057494
Huang, Q. et al. Raf kinase inhibitory protein down-expression exacerbates hepatic fibrosis in vivo and in vitro. Cell Physiol. Biochem. 40, 49–61. https://doi.org/10.1159/000452524 (2016).
doi: 10.1159/000452524 pubmed: 27842313
Wang, Y. et al. New insights into the antifibrotic effects of sorafenib on hepatic stellate cells and liver fibrosis. J. Hepatol. 53, 132–144. https://doi.org/10.1016/j.jhep.2010.02.027 (2010).
doi: 10.1016/j.jhep.2010.02.027 pubmed: 20447716
Vargha, R. et al. Effects of epithelial-to-mesenchymal transition on acute stress response in human peritoneal mesothelial cells. Nephrol. Dial. Transpl. 23, 3494–3500. https://doi.org/10.1093/ndt/gfn353 (2008).
doi: 10.1093/ndt/gfn353
Vidyasagar, A., Reese, S., Acun, Z., Hullett, D. & Djamali, A. HSP27 is involved in the pathogenesis of kidney tubulointerstitial fibrosis. Am. J. Physiol. Renal Physiol. 295, F707-716. https://doi.org/10.1152/ajprenal.90240.2008 (2008).
doi: 10.1152/ajprenal.90240.2008 pubmed: 18596079 pmcid: 2536879
Wei, L. et al. Hsp27 participates in the maintenance of breast cancer stem cells through regulation of epithelial-mesenchymal transition and nuclear factor-kappaB. Breast Cancer Res. 13, R101. https://doi.org/10.1186/bcr3042 (2011).
doi: 10.1186/bcr3042 pubmed: 22023707 pmcid: 3262214
Ansieau, S. et al. Induction of EMT by twist proteins as a collateral effect of tumor-promoting inactivation of premature senescence. Cancer Cell 14, 79–89. https://doi.org/10.1016/j.ccr.2008.06.005 (2008).
doi: 10.1016/j.ccr.2008.06.005 pubmed: 18598946
Yang, J. et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117, 927–939. https://doi.org/10.1016/j.cell.2004.06.006 (2004).
doi: 10.1016/j.cell.2004.06.006 pubmed: 15210113
Kwok, W. K. et al. Up-regulation of TWIST in prostate cancer and its implication as a therapeutic target. Cancer Res. 65, 5153–5162. https://doi.org/10.1158/0008-5472.CAN-04-3785 (2005).
doi: 10.1158/0008-5472.CAN-04-3785 pubmed: 15958559
Mironchik, Y. et al. Twist overexpression induces in vivo angiogenesis and correlates with chromosomal instability in breast cancer. Cancer Res. 65, 10801–10809. https://doi.org/10.1158/0008-5472.CAN-05-0712 (2005).
doi: 10.1158/0008-5472.CAN-05-0712 pubmed: 16322226 pmcid: 5575828
Burgess, S. & Echeverria, V. Raf inhibitors as therapeutic agents against neurodegenerative diseases. CNS Neurol. Disord. Drug. Targets 9, 120–127 (2010).
doi: 10.2174/187152710790966632
Hong, Z. Y. et al. A preclinical rodent model of acute radiation-induced lung injury after ablative focal irradiation reflecting clinical stereotactic body radiotherapy. Radiat. Res. 182, 83–91. https://doi.org/10.1667/RR13535.1 (2014).
doi: 10.1667/RR13535.1 pubmed: 24937781
Mehta, V. Radiation pneumonitis and pulmonary fibrosis in non-small-cell lung cancer: pulmonary function, prediction, and prevention. Int. J. Radiat. Oncol. Biol. Phys. 63, 5–24. https://doi.org/10.1016/j.ijrobp.2005.03.047 (2005).
doi: 10.1016/j.ijrobp.2005.03.047 pubmed: 15963660
Kang, Y. & Massague, J. Epithelial-mesenchymal transitions: twist in development and metastasis. Cell 118, 277–279. https://doi.org/10.1016/j.cell.2004.07.011 (2004).
doi: 10.1016/j.cell.2004.07.011 pubmed: 15294153
Yang, J. & Weinberg, R. A. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 14, 818–829. https://doi.org/10.1016/j.devcel.2008.05.009 (2008).
doi: 10.1016/j.devcel.2008.05.009 pubmed: 18539112
Wellbrock, C., Karasarides, M. & Marais, R. The RAF proteins take centre stage. Nat. Rev. Mol. Cell Biol. 5, 875–885. https://doi.org/10.1038/nrm1498 (2004).
doi: 10.1038/nrm1498 pubmed: 15520807
Fischer, A. et al. Regulation of RAF activity by 14–3-3 proteins: RAF kinases associate functionally with both homo- and heterodimeric forms of 14–3-3 proteins. J. Biol. Chem. 284, 3183–3194. https://doi.org/10.1074/jbc.M804795200 (2009).
doi: 10.1074/jbc.M804795200 pubmed: 19049963
Rapp, U. R., Gotz, R. & Albert, S. BuCy RAFs drive cells into MEK addiction. Cancer Cell 9, 9–12. https://doi.org/10.1016/j.ccr.2005.12.022 (2006).
doi: 10.1016/j.ccr.2005.12.022 pubmed: 16413467
Xie, L. et al. Activation of the Erk pathway is required for TGF-beta1-induced EMT in vitro. Neoplasia 6, 603–610. https://doi.org/10.1593/neo.04241 (2004).
doi: 10.1593/neo.04241 pubmed: 15548370 pmcid: 1531665
Lin, X. et al. Didymin alleviates hepatic fibrosis through inhibiting ERK and PI3K/Akt pathways via regulation of raf kinase inhibitor protein. Cell Physiol. Biochem. 40, 1422–1432. https://doi.org/10.1159/000453194 (2016).
doi: 10.1159/000453194 pubmed: 27997902
Leicht, D. T. et al. Raf kinases: function, regulation and role in human cancer. Biochim. Biophys. Acta 1773, 1196–1212. https://doi.org/10.1016/j.bbamcr.2007.05.001 (2007).
doi: 10.1016/j.bbamcr.2007.05.001 pubmed: 17555829 pmcid: 1986673
Strumberg, D. & Seeber, S. Raf kinase inhibitors in oncology. Onkologie 28, 101–107. https://doi.org/10.1159/000083373 (2005).
doi: 10.1159/000083373 pubmed: 15665559
Sridhar, S. S., Hedley, D. & Siu, L. L. Raf kinase as a target for anticancer therapeutics. Mol. Cancer Ther. 4, 677–685. https://doi.org/10.1158/1535-7163.MCT-04-0297 (2005).
doi: 10.1158/1535-7163.MCT-04-0297 pubmed: 15827342
Chen, Y. L. et al. Sorafenib ameliorates bleomycin-induced pulmonary fibrosis: potential roles in the inhibition of epithelial-mesenchymal transition and fibroblast activation. Cell Death Dis. 4, e665. https://doi.org/10.1038/cddis.2013.154 (2013).
doi: 10.1038/cddis.2013.154 pubmed: 23764846 pmcid: 3698540
Hay, J., Shahzeidi, S. & Laurent, G. Mechanisms of bleomycin-induced lung damage. Arch. Toxicol. 65, 81–94. https://doi.org/10.1007/bf02034932 (1991).
doi: 10.1007/bf02034932 pubmed: 1711838
Kim, W. et al. Cellular stress responses in radiotherapy. Cells https://doi.org/10.3390/cells8091105 (2019).
doi: 10.3390/cells8091105 pubmed: 31905972 pmcid: 7017379
Sato, S. et al. Anti-fibrotic efficacy of nintedanib in pulmonary fibrosis via the inhibition of fibrocyte activity. Respir. Res. 18, 172. https://doi.org/10.1186/s12931-017-0654-2 (2017).
doi: 10.1186/s12931-017-0654-2 pubmed: 28915889 pmcid: 5603061
Chin, P. C. et al. The c-Raf inhibitor GW5074 provides neuroprotection in vitro and in an animal model of neurodegeneration through a MEK-ERK and Akt-independent mechanism. J. Neurochem. 90, 595–608. https://doi.org/10.1111/j.1471-4159.2004.02530.x (2004).
doi: 10.1111/j.1471-4159.2004.02530.x pubmed: 15255937
Bain, J. et al. The selectivity of protein kinase inhibitors: a further update. Biochem. J. 408, 297–315. https://doi.org/10.1042/BJ20070797 (2007).
doi: 10.1042/BJ20070797 pubmed: 17850214 pmcid: 2267365
Palumbo-Zerr, K. et al. Composition of TWIST1 dimers regulates fibroblast activation and tissue fibrosis. Ann. Rheum. Dis. 76, 244–251. https://doi.org/10.1136/annrheumdis-2015-208470 (2017).
doi: 10.1136/annrheumdis-2015-208470 pubmed: 27113414
Murre, C. et al. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58, 537–544. https://doi.org/10.1016/0092-8674(89)90434-0 (1989).
doi: 10.1016/0092-8674(89)90434-0 pubmed: 2503252
Gort, E. H. et al. The TWIST1 oncogene is a direct target of hypoxia-inducible factor-2alpha. Oncogene 27, 1501–1510. https://doi.org/10.1038/sj.onc.1210795 (2008).
doi: 10.1038/sj.onc.1210795 pubmed: 17873906
Yoo, Y. G., Christensen, J., Gu, J. & Huang, L. E. HIF-1alpha mediates tumor hypoxia to confer a perpetual mesenchymal phenotype for malignant progression. Sci. Signal https://doi.org/10.1126/scisignal.2002072 (2011).
doi: 10.1126/scisignal.2002072 pubmed: 21693763
Kida, Y., Asahina, K., Teraoka, H., Gitelman, I. & Sato, T. Twist relates to tubular epithelial-mesenchymal transition and interstitial fibrogenesis in the obstructed kidney. J. Histochem. Cytochem.. 55, 661–673. https://doi.org/10.1369/jhc.6A7157.2007 (2007).
doi: 10.1369/jhc.6A7157.2007 pubmed: 17341474
Pozharskaya, V. et al. Twist: a regulator of epithelial-mesenchymal transition in lung fibrosis. PLoS ONE 4, e7559. https://doi.org/10.1371/journal.pone.0007559 (2009).
doi: 10.1371/journal.pone.0007559 pubmed: 19851501 pmcid: 2761603
Hong, Z. Y. et al. Inhibition of Akt/FOXO3a signaling by constitutively active FOXO3a suppresses growth of follicular thyroid cancer cell lines. Cancer Lett. 314, 34–40. https://doi.org/10.1016/j.canlet.2011.09.010 (2012).
doi: 10.1016/j.canlet.2011.09.010 pubmed: 21974806

Auteurs

Zhen-Yu Hong (ZY)

Department of Medical Oncology, The First Affiliated Hospital of Xinxiang Medical University, 88 Jiangkang Road, Weihui, Henan, China.
Department of Radiation Oncology, Yonsei University College of Medicine, 50 Yonsei-ro, Seodaemun-gu, Seoul, 120-752, South Korea.

Sanke Li (S)

Department of Hematology, The 3rd People's Hospital of Zhengzhou, Zhengzhou, China.

Xiaomei Liu (X)

Department of Medical Oncology, The First Affiliated Hospital of Xinxiang Medical University, 88 Jiangkang Road, Weihui, Henan, China.

Xiao-Min Leng (XM)

Henan Key Laboratory of Neural Regeneration, Department of Neurology, The First Affiliated Hospital of Xinxiang Medical University, Weihui, Henan, China.

Zhanhui Miao (Z)

Department of Medical Oncology, The First Affiliated Hospital of Xinxiang Medical University, 88 Jiangkang Road, Weihui, Henan, China.

Xiaohong Kang (X)

Department of Medical Oncology, The First Affiliated Hospital of Xinxiang Medical University, 88 Jiangkang Road, Weihui, Henan, China.

Hongrui Niu (H)

Department of Medical Oncology, The First Affiliated Hospital of Xinxiang Medical University, 88 Jiangkang Road, Weihui, Henan, China.

Ming-Qing Gao (MQ)

School of Medicine, Northwest University, Taibai North Road 229, Xi'an, 710069, Shaanxi, China. gmq126@126.com.

Ping Lu (P)

Department of Medical Oncology, The First Affiliated Hospital of Xinxiang Medical University, 88 Jiangkang Road, Weihui, Henan, China. lupingdoctor@163.com.

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