Generic placeholder image

Anti-Cancer Agents in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1871-5206
ISSN (Online): 1875-5992

Research Article

CircFAT1 Promotes the Proliferation and Invasion of Malignant Melanoma through miR375-SLC7A11 Signal Axis

Author(s): Tao Lu, Danyang Yang and Xiaoli Li*

Volume 23, Issue 20, 2023

Published on: 03 October, 2023

Page: [2200 - 2208] Pages: 9

DOI: 10.2174/1871520623666230609163916

Price: $65

Abstract

Background: Circular RNA, as a member of noncoding RNA, plays an important role in the occurrence, development and metastasis of tumor cells. So far, the correlation between circular RNA and malignant melanoma remains obscure.

Methods: RNA expression of circFAT1 and miR-375 in malignant melanoma (MM) tissues and cell lines was detected by RT-PCR. The proliferation, cloning, migration and invasion of SK-Mel-28 and A375 cells were assessed using CCK-8 test, clone formation and Transwell assay, respectively. CircRNA immunoprecipitation was used to validate the relationship between circFAT1 and miR-375. The binding between circFAT1 and miR-375, as well as SLC7A11 and miR-375 were verified by luciferase assay.

Results: In our study,the circFAT1 was significantly overexpressed in the MM tissue than melanocytic nevi. Conversely, the expression of miR-375 in MM tissue was lower than in melanocytic nevi tissue. The underexpression of circFAT1 with siRNA plasmids significantly suppressed the proliferation, invasion and clone formation of MM cell line. Mechanistically, circFAT1 positively regulates the expression level of SLC7A11 by sponging miR-375. The promotive effects of circFAT1 on the proliferation and invasion ability of MM cells were reversed by the upregulation of miR-375.

Conclusion: circFAT1 promotes the proliferation, invasion and clone formation of malignant melanoma cells by improving the expression level of SLC7A11 via sponging miR-375.

Keywords: Malignant melanoma, miR-375, SLC7A11, circRNA, proliferation, invasion, circFAT1

Graphical Abstract
[1]
Hanniford, D.; Ulloa-Morales, A.; Karz, A.; Berzoti-Coelho, M.G.; Moubarak, R.S.; Sánchez-Sendra, B.; Kloetgen, A.; Davalos, V.; Imig, J.; Wu, P.; Vasudevaraja, V.; Argibay, D.; Lilja, K.; Tabaglio, T.; Monteagudo, C.; Guccione, E.; Tsirigos, A.; Osman, I.; Aifantis, I.; Hernando, E. Epigenetic silencing of CDR1as drives IGF2BP3-mediated melanoma invasion and metastasis. Cancer Cell, 2020, 37(1), 55-70.e15.
[http://dx.doi.org/10.1016/j.ccell.2019.12.007] [PMID: 31935372]
[2]
Law, M.H.; Bishop, D.T.; Lee, J.E.; Brossard, M.; Martin, N.G.; Moses, E.K.; Song, F.; Barrett, J.H.; Kumar, R.; Easton, D.F.; Pharoah, P.D.P.; Swerdlow, A.J.; Kypreou, K.P.; Taylor, J.C.; Harland, M.; Randerson-Moor, J.; Akslen, L.A.; Andresen, P.A.; Avril, M.F.; Azizi, E.; Scarrà, G.B.; Brown, K.M. Dȩbniak, T.; Duffy, D.L.; Elder, D.E.; Fang, S.; Friedman, E.; Galan, P.; Ghiorzo, P.; Gillanders, E.M.; Goldstein, A.M.; Gruis, N.A.; Hansson, J.; Helsing, P.; Hočevar, M.; Höiom, V.; Ingvar, C.; Kanetsky, P.A.; Chen, W.V.; Landi, M.T.; Lang, J.; Lathrop, G.M.; Lubiński, J.; Mackie, R.M.; Mann, G.J.; Molven, A.; Montgomery, G.W.; Novaković S.; Olsson, H.; Puig, S.; Puig-Butille, J.A.; Qureshi, A.A.; Radford-Smith, G.L.; van der Stoep, N.; van Doorn, R.; Whiteman, D.C.; Craig, J.E.; Schadendorf, D.; Simms, L.A.; Burdon, K.P.; Nyholt, D.R.; Pooley, K.A.; Orr, N.; Stratigos, A.J.; Cust, A.E.; Ward, S.V.; Hayward, N.K.; Han, J.; Schulze, H.J.; Dunning, A.M.; Bishop, J.A.N.; Demenais, F.; Amos, C.I.; MacGregor, S.; Iles, M.M. Genome-wide meta-analysis identifies five new susceptibility loci for cutaneous malignant melanoma. Nat. Genet., 2015, 47(9), 987-995.
[http://dx.doi.org/10.1038/ng.3373] [PMID: 26237428]
[3]
Smithy, J.W.; Shoushtari, A.N. Adjuvant PD-1 blockade in resected melanoma: Is preventing recurrence enough? Cancer Discov., 2022, 12(3), 599-601.
[http://dx.doi.org/10.1158/2159-8290.CD-21-1593] [PMID: 35257151]
[4]
McCulloch, J.A.; Davar, D.; Rodrigues, R.R.; Badger, J.H.; Fang, J.R.; Cole, A.M.; Balaji, A.K.; Vetizou, M.; Prescott, S.M.; Fernandes, M.R.; Costa, R.G.F.; Yuan, W.; Salcedo, R.; Bahadiroglu, E.; Roy, S.; DeBlasio, R.N.; Morrison, R.M.; Chauvin, J.M.; Ding, Q.; Zidi, B.; Lowin, A.; Chakka, S.; Gao, W.; Pagliano, O.; Ernst, S.J.; Rose, A.; Newman, N.K.; Morgun, A.; Zarour, H.M.; Trinchieri, G.; Dzutsev, A.K. Intestinal microbiota signatures of clinical response and immune-related adverse events in melanoma patients treated with anti-PD-1. Nat. Med., 2022, 28(3), 545-556.
[http://dx.doi.org/10.1038/s41591-022-01698-2] [PMID: 35228752]
[5]
Lee, K.A.; Thomas, A.M.; Bolte, L.A.; Björk, J.R.; de Ruijter, L.K.; Armanini, F.; Asnicar, F.; Blanco-Miguez, A.; Board, R.; Calbet-Llopart, N.; Derosa, L.; Dhomen, N.; Brooks, K.; Harland, M.; Harries, M.; Leeming, E.R.; Lorigan, P.; Manghi, P.; Marais, R.; Newton-Bishop, J.; Nezi, L.; Pinto, F.; Potrony, M.; Puig, S.; Serra-Bellver, P.; Shaw, H.M.; Tamburini, S.; Valpione, S.; Vijay, A.; Waldron, L.; Zitvogel, L.; Zolfo, M.; de Vries, E.G.E.; Nathan, P.; Fehrmann, R.S.N.; Bataille, V.; Hospers, G.A.P.; Spector, T.D.; Weersma, R.K.; Segata, N. Cross-cohort gut microbiome associations with immune checkpoint inhibitor response in advanced melanoma. Nat. Med., 2022, 28(3), 535-544.
[http://dx.doi.org/10.1038/s41591-022-01695-5] [PMID: 35228751]
[6]
Zhang, W.; Liu, Y.; Min, Z.; Liang, G.; Mo, J.; Ju, Z.; Zeng, B.; Guan, W.; Zhang, Y.; Chen, J.; Zhang, Q.; Li, H.; Zeng, C.; Wei, Y.; Chan, G.C.F. circMine: A comprehensive database to integrate, analyze and visualize human disease–related circRNA transcriptome. Nucleic Acids Res., 2022, 50(D1), D83-D92.
[http://dx.doi.org/10.1093/nar/gkab809] [PMID: 34530446]
[7]
Xu, J.; Ji, L.; Liang, Y.; Wan, Z.; Zheng, W.; Song, X.; Gorshkov, K.; Sun, Q.; Lin, H.; Zheng, X.; Chen, J.; Jin, R.; Liang, X.; Cai, X. CircRNA-SORE mediates sorafenib resistance in hepatocellular carcinoma by stabilizing YBX1. Signal Transduct. Target. Ther., 2020, 5(1), 298.
[http://dx.doi.org/10.1038/s41392-020-00375-5] [PMID: 33361760]
[8]
Zheng, X.; Huang, M.; Xing, L.; Yang, R.; Wang, X.; Jiang, R.; Zhang, L.; Chen, J. The circRNA circSEPT9 mediated by E2F1 and EIF4A3 facilitates the carcinogenesis and development of triple-negative breast cancer. Mol. Cancer, 2020, 19(1), 73.
[http://dx.doi.org/10.1186/s12943-020-01183-9] [PMID: 32264877]
[9]
Xu, X.; Zhang, J.; Tian, Y.; Gao, Y.; Dong, X.; Chen, W.; Yuan, X.; Yin, W.; Xu, J.; Chen, K.; He, C.; Wei, L. CircRNA inhibits DNA damage repair by interacting with host gene. Mol. Cancer, 2020, 19(1), 128.
[http://dx.doi.org/10.1186/s12943-020-01246-x] [PMID: 32838810]
[10]
Liu, G.; Huang, K.; Jie, Z.; Wu, Y.; Chen, J.; Chen, Z.; Fang, X.; Shen, S. CircFAT1 sponges miR-375 to promote the expression of Yes-associated protein 1 in osteosarcoma cells. Mol. Cancer, 2018, 17(1), 170.
[http://dx.doi.org/10.1186/s12943-018-0917-7] [PMID: 30514309]
[11]
Dong, W.; Zhang, H.; Dai, Y.; Zhou, Y.; Luo, Y.; Zhao, C.; Cao, Y.; Du, Y.; Chen, Y. circRNA circFAT1(e2) elevates the development of non-small-cell lung cancer by regulating miR-30e-5p and USP22. BioMed Res. Int., 2021, 2021, 1-8.
[http://dx.doi.org/10.1155/2021/6653387] [PMID: 33884267]
[12]
Liu, J.; Li, H.; Wei, C.; Ding, J.; Lu, J.; Pan, G.; Mao, A. circFAT1(e2) promotes papillary thyroid cancer proliferation, migration, and invasion via the miRNA-873/ZEB1 axis. Comput. Math. Methods Med., 2020, 2020, 1-9.
[http://dx.doi.org/10.1155/2020/1459368] [PMID: 33133224]
[13]
Hu, B.; Xian, Z.; Zou, Q. CircFAT1 suppresses colorectal cancer development through regulating/Axis or/Axis. Cancer Biother. Radiopharm., 2021, 36(1), 45-57.
[http://dx.doi.org/10.1089/cbr.2019.3291] [PMID: 32379550]
[14]
Liu, M. CircFAT1 is overexpressed in colorectal cancer and suppresses cancer cell proliferation, invasion and migration by increasing the maturation of miR-10a. Cancer Manag. Res., 2021, 13, 4309-4315.
[http://dx.doi.org/10.2147/CMAR.S287230] [PMID: 34103986]
[15]
Wei, H.; Yan, S.; Hui, Y.; Liu, Y.; Guo, H.; Li, Q.; Li, J.; Chang, Z. CircFAT1 promotes hepatocellular carcinoma progression via miR-‐30a‐-5p/REEP3 pathway. J. Cell. Mol. Med., 2020, 24(24), 14561-14570.
[http://dx.doi.org/10.1111/jcmm.16085] [PMID: 33179443]
[16]
Fang, J.; Hong, H.; Xue, X.; Zhu, X.; Jiang, L.; Qin, M.; Liang, H.; Gao, L. A novel circular RNA, circFAT1(e2), inhibits gastric cancer progression by targeting miR-548g in the cytoplasm and interacting with YBX1 in the nucleus. Cancer Lett., 2019, 442, 222-232.
[http://dx.doi.org/10.1016/j.canlet.2018.10.040] [PMID: 30419346]
[17]
Takaki, W.; Konishi, H.; Shoda, K.; Arita, T.; Kataoka, S.; Shibamoto, J.; Furuke, H.; Takabatake, K.; Shimizu, H.; Komatsu, S.; Shiozaki, A.; Fujiwara, H.; Masuda, K.; Otsuji, E. Significance of circular FAT1 as a prognostic factor and tumor suppressor for esophageal squamous cell carcinoma. Ann. Surg. Oncol., 2021, 28(13), 8508-8518.
[http://dx.doi.org/10.1245/s10434-021-10089-9] [PMID: 34185205]
[18]
Wu, P.; Li, C.; Ye, D.; Yu, K.; Li, Y.; Tang, H.; Xu, G.; Yi, S.; Zhang, Z. Circular RNA circEPSTI1 accelerates cervical cancer progression via miR-375/409-3P/515-5p-SLC7A11 axis. Aging , 2021, 13(3), 4663-4673.
[http://dx.doi.org/10.18632/aging.202518] [PMID: 33534779]
[19]
Ni, H.; Qin, H.; Sun, C.; Liu, Y.; Ruan, G.; Guo, Q.; Xi, T.; Xing, Y.; Zheng, L. MiR-375 reduces the stemness of gastric cancer cells through triggering ferroptosis. Stem Cell Res. Ther., 2021, 12(1), 325.
[http://dx.doi.org/10.1186/s13287-021-02394-7] [PMID: 34090492]
[20]
Koppula, P.; Zhuang, L.; Gan, B. Cystine transporter SLC7A11/xCT in cancer: Ferroptosis, nutrient dependency, and cancer therapy. Protein Cell, 2021, 12(8), 599-620.
[http://dx.doi.org/10.1007/s13238-020-00789-5] [PMID: 33000412]
[21]
Zhang, W.; Sun, Y.; Bai, L.; Zhi, L.; Yang, Y.; Zhao, Q.; Chen, C.; Qi, Y.; Gao, W.; He, W.; Wang, L.; Chen, D.; Fan, S.; Chen, H.; Piao, H.L.; Qiao, Q.; Xu, Z.; Zhang, J.; Zhao, J.; Zhang, S.; Yin, Y.; Peng, C.; Li, X.; Liu, Q.; Liu, H.; Wang, Y. RBMS1 regulates lung cancer ferroptosis through translational control of SLC7A11. J. Clin. Invest., 2021, 131(22), e152067.
[http://dx.doi.org/10.1172/JCI152067] [PMID: 34609966]

Rights & Permissions Print Export Cite as
© 2024 Bentham Science Publishers | Privacy Policy