Abstract
Purpose
UV exposure is the main risk factor for development of cutaneous squamous cell carcinoma (cSCC). While early detection greatly improves cSCC prognosis, locally advanced or metastatic cSCC has a severely impaired prognosis. Notably, the mechanisms of progression to metastatic cSCC are not well understood. We hypothesized that UV exposure of already transformed epithelial cSCC cells further induces changes which might be involved in the progression to metastatic cSCCs and that UV-inducible microRNAs (miRNAs) might play an important role.
Methods
Thus, we analyzed the impact of UV radiation of different quality (UVA, UVB, UVA + UVB) on the miRNA expression pattern in established cell lines generated from primary and metastatic cSCCs (Met-1, Met-4) using the NanoString nCounter platform.
Results
This analysis revealed that the expression pattern of miRNAs depends on both the cell line used per se and on the quality of UV radiation. Comparison of UV-induced miRNAs in cSCC cell lines established from a primary tumor (Met-1) and the respective (un-irradiated) metastasis (Met-4) suggest that miR-7-5p, miR-29a-3p and miR-183-5p are involved in a UV-driven pathway of progression to metastasis. This notion is supported by the fact that these three miRNAs build up a network of 81 potential target genes involved e.g. in UVA/UVB-induced MAPK signaling and regulation of the epithelial–mesenchymal transition. As an example, PTEN, a target of UV-upregulated miRNAs (miR-29a-3p, miR-183-5p), could be shown to be down-regulated in response to UV radiation. We further identified CNOT8, the transcription complex subunit 8 of the CCR4-NOT complex, a deadenylase removing the poly(A) tail from miRNA-destabilized mRNAs, in the center of this network, targeted by all three miRNAs.
Conclusion
In summary, our results demonstrate that UV radiation induces an miRNA expression pattern in primary SCC cell line partly resembling those of metastatic cell line, thus suggesting that UV radiation impacts SCC progression beyond initiation.
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Acknowledgements
Prof. P. Boukamp for kindly providing cell lines and discussion. S. Balk, R. Börger-Hoppe, M. Brunsen, S. Engel-Haskiris and R. Keck for technical support.
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This project has been financially supported by Federal Ministry of Education and Research (BMBF), Grant Number: 02NUK036B and Hiege-Stiftung gegen Hautkrebs, Grant Number: D/106-21076.
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All authors had input into the manuscript and have approved the manuscript for publication. Conceptualization, R.G., B.V. and J.C.B.; methodology, I-P.C, M. B., M. M.-G., I.S., A.S., and S.H.; validation, M.B.; formal analysis, M.B.; investigation, I-P.C., I.S., A.S., K.F., L.K.; writing—original draft preparation, R.G.; writing—review and editing, R.G., J.C.B, I-P.C., M.B., A.S., S.D.; visualization, M.B..; supervision, R.G and J.C.B..; project administration, I-P.C., M.B..; funding acquisition, R.G. and J.C.B.
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Jürgen C. Becker has received speaker honoraria from Amgen, Merck Serono, Pfizer, and Sanofi advisory board honoraria from 4SC, Amgen, CureVac, eTheRNA, Lytix, Merck Serono, Novartis and ReProTher, as well as research funding from Alcedis, Boehringer Ingelheim, Bristol-Myers Squibb and Merck Serono; he also received travel support from 4SC and Incyte. The other authors declare no conflict of interest.
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Chen, IP., Bender, M., Spassova, I. et al. UV-type specific alteration of miRNA expression and its association with tumor progression and metastasis in SCC cell lines. J Cancer Res Clin Oncol 146, 3215–3231 (2020). https://doi.org/10.1007/s00432-020-03358-9
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DOI: https://doi.org/10.1007/s00432-020-03358-9