Overexpression of microRNA-205-5p promotes cholangiocarcinoma growth by reducing expression of homeodomain-interacting protein kinase 3.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
17 Dec 2023
17 Dec 2023
Historique:
received:
20
02
2023
accepted:
11
12
2023
medline:
18
12
2023
pubmed:
18
12
2023
entrez:
17
12
2023
Statut:
epublish
Résumé
The microRNA miR-205-5p has diverse effects in different malignancies, including cholangiocarcinoma (CCA), but its effects on CCA progression is unclear. Here we investigated the role and function of miR-205-5p in CCA. Three CCA cell lines and human serum samples were found to have much higher expression levels of miR-205-5p than seen in typical cholangiocyte cell lines and healthy controls. Inhibition of miR-205-5p suppressed CCA cell motility, invasion and proliferation of KKU-213B whereby overexpression of miR-205-5p promoted cell proliferation and motility of KKU-100 cells. Bioinformatics tools (miRDB, TargetScan, miRWalk, and GEPIA) all predicted various miR-205-5p targets. Experiments using miR-205-5p inhibitor and mimic indicated that homeodomain-interacting protein kinase 3 (HIPK3) was a potential direct target of miR-205-5p. Overexpression of HIPK3 using HIPK3 plasmid cloning DNA suppressed migration and proliferation of KKU-100 cells. Notably, HIPK3 expression was lower in human CCA tissues than in normal adjacent tissues. High HIPK3 expression was significantly associated with longer survival time of CCA patients. Multivariate regression analysis indicated tissue HIPK3 levels as an independent prognostic factor for CCA patients. These findings indicate that overexpression of miR-205-5p promotes CCA cells proliferation and migration partly via HIPK3-dependent way. Therefore, targeting miR-205-5p may be a potential treatment approach for CCA.
Identifiants
pubmed: 38105269
doi: 10.1038/s41598-023-49694-x
pii: 10.1038/s41598-023-49694-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
22444Subventions
Organisme : the National Research Council of Thailand
ID : NRCT grant no. 820/2563 to KN
Organisme : the Basic Research Fund of Khon Kaen University through the Cholangiocarcinoma Research Institute
ID : CARI-BRF64-2
Informations de copyright
© 2023. The Author(s).
Références
Banales, J. M. et al. Cholangiocarcinoma 2020: The next horizon in mechanisms and management. Nat. Rev. Gastroenterol. Hepatol. 17, 557–588. https://doi.org/10.1038/s41575-020-0310-z (2020).
doi: 10.1038/s41575-020-0310-z
pubmed: 32606456
pmcid: 7447603
Sarcognato, S. et al. Cholangiocarcinoma. Pathologica 113, 158–169. https://doi.org/10.32074/1591-951X-252 (2021).
doi: 10.32074/1591-951X-252
pubmed: 34294934
pmcid: 8299326
Bridgewater, J. et al. Guidelines for the diagnosis and management of intrahepatic cholangiocarcinoma. J. Hepatol. 60, 1268–1289. https://doi.org/10.1016/j.jhep.2014.01.021 (2014).
doi: 10.1016/j.jhep.2014.01.021
pubmed: 24681130
Kamsa-Ard, S. et al. Decreasing trends in cholangiocarcinoma incidence and relative survival in Khon Kaen, Thailand: An updated, inclusive, population-based cancer registry analysis for 1989–2018. PLoS One 16, e0246490. https://doi.org/10.1371/journal.pone.0246490 (2021).
doi: 10.1371/journal.pone.0246490
pubmed: 33592053
pmcid: 7886206
Banales, J. M. et al. Expert consensus document: Cholangiocarcinoma: Current knowledge and future perspectives consensus statement from the European network for the study of cholangiocarcinoma (ENS-CCA). Nat. Rev. Gastroenterol. Hepatol. 13, 261–280. https://doi.org/10.1038/nrgastro.2016.51 (2016).
doi: 10.1038/nrgastro.2016.51
pubmed: 27095655
Yousef, M. & Allmer, J. miRNomics: microRNA Biology and Computational Analysis (Springer, 2014).
doi: 10.1007/978-1-62703-748-8
Lu, T. X. & Rothenberg, M. E. MicroRNA. J. Allergy Clin. Immunol. 141, 1202–1207. https://doi.org/10.1016/j.jaci.2017.08.034 (2018).
doi: 10.1016/j.jaci.2017.08.034
pubmed: 29074454
Lee, D. & Shin, C. MicroRNA-target interactions: New insights from genome-wide approaches. Ann. NY Acad. Sci. 1271, 118–128. https://doi.org/10.1111/j.1749-6632.2012.06745.x (2012).
doi: 10.1111/j.1749-6632.2012.06745.x
pubmed: 23050973
Peng, Y. & Croce, C. M. The role of MicroRNAs in human cancer. Signal Transduct. Target Ther. 1, 15004. https://doi.org/10.1038/sigtrans.2015.4 (2016).
doi: 10.1038/sigtrans.2015.4
pubmed: 29263891
pmcid: 5661652
Menon, A., Abd-Aziz, N., Khalid, K., Poh, C. L. & Naidu, R. miRNA: A promising therapeutic target in cancer. Int. J. Mol. Sci. https://doi.org/10.3390/ijms231911502 (2022).
doi: 10.3390/ijms231911502
pubmed: 36361504
pmcid: 9657836
Shi, T., Morishita, A., Kobara, H. & Masaki, T. The role of microRNAs in cholangiocarcinoma. Int. J. Mol. Sci. https://doi.org/10.3390/ijms22147627 (2021).
doi: 10.3390/ijms22147627
pubmed: 35008672
pmcid: 8745729
Ferrari, E. & Gandellini, P. Unveiling the ups and downs of miR-205 in physiology and cancer: Transcriptional and post-transcriptional mechanisms. Cell Death Dis. 11, 980. https://doi.org/10.1038/s41419-020-03192-4 (2020).
doi: 10.1038/s41419-020-03192-4
pubmed: 33191398
pmcid: 7667162
Jiang, M. et al. Reduced expression of miR2055p promotes apoptosis and inhibits proliferation and invasion in lung cancer A549 cells by upregulation of ZEB2 and downregulation of erbB3. Mol. Med. Rep. 15, 3231–3238. https://doi.org/10.3892/mmr.2017.6398 (2017).
doi: 10.3892/mmr.2017.6398
pubmed: 28350117
Su, N. et al. miR-205 promotes tumor proliferation and invasion through targeting ESRRG in endometrial carcinoma. Oncol. Rep. 29, 2297–2302. https://doi.org/10.3892/or.2013.2400 (2013).
doi: 10.3892/or.2013.2400
pubmed: 23589079
Yi, L. et al. DNAJA1 stabilizes EF1A1 to promote cell proliferation and metastasis of liver cancer mediated by miR-205-5p. J. Oncol. 2022, 2292481. https://doi.org/10.1155/2022/2292481 (2022).
doi: 10.1155/2022/2292481
pubmed: 35586205
pmcid: 9110222
Yang, W. et al. Exosomal miR-205-5p enhances angiogenesis and nasopharyngeal carcinoma metastasis by targeting desmocollin-2. Mol. Ther. Oncolytics 24, 612–623. https://doi.org/10.1016/j.omto.2022.02.008 (2022).
doi: 10.1016/j.omto.2022.02.008
pubmed: 35284624
pmcid: 8892032
Pang, H. & Yue, X. MiR-205 serves as a prognostic factor and suppresses proliferation and invasion by targeting insulin-like growth factor receptor 1 in human cervical cancer. Tumour. Biol. 39, 1010428317701308. https://doi.org/10.1177/1010428317701308 (2017).
doi: 10.1177/1010428317701308
pubmed: 28651495
Zhang, G. F., Wu, J. C., Wang, H. Y., Jiang, W. D. & Qiu, L. Overexpression of microRNA-205-5p exerts suppressive effects on stem cell drug resistance in gallbladder cancer by down-regulating PRKCE. Biosci. Rep. https://doi.org/10.1042/BSR20194509 (2020).
Lin, L. F., Li, Y. T., Han, H. & Lin, S. G. MicroRNA-205-5p targets the HOXD9-Snail1 axis to inhibit triple negative breast cancer cell proliferation and chemoresistance. Aging (Albany NY) 13, 3945–3956. https://doi.org/10.18632/aging.202363 (2021).
doi: 10.18632/aging.202363
pubmed: 33428601
Huang, J., Wang, X., Wen, G. & Ren, Y. miRNA-205-5p functions as a tumor suppressor by negatively regulating VEGFA and PI3K/Akt/mTOR signaling in renal carcinoma cells. Oncol. Rep. 42, 1677–1688. https://doi.org/10.3892/or.2019.7307 (2019).
doi: 10.3892/or.2019.7307
pubmed: 31545453
pmcid: 6775807
Chen, X., Zhang, L., Geng, J., Chen, Z. & Cui, X. MiR-205-5p functions as a tumor suppressor in gastric cancer cells through downregulating FAM84B. J. Oncol. 2022, 8267891. https://doi.org/10.1155/2022/8267891 (2022).
doi: 10.1155/2022/8267891
pubmed: 35669244
pmcid: 9166972
Jiang, Z. L. et al. miR-181b-5p promotes the progression of cholangiocarcinoma by targeting PARK2 via PTEN/PI3K/AKT signaling pathway. Biochem. Genet. 60, 223–240. https://doi.org/10.1007/s10528-021-10084-5 (2022).
doi: 10.1007/s10528-021-10084-5
pubmed: 34169384
Ni, Q., Zhang, H., Shi, X. & Li, X. Exosomal microRNA-23a-3p contributes to the progression of cholangiocarcinoma by interaction with Dynamin3. Bioengineered 13, 6208–6221. https://doi.org/10.1080/21655979.2022.2037249 (2022).
doi: 10.1080/21655979.2022.2037249
pubmed: 35200104
pmcid: 8973721
Liu, C. et al. MiRNA-196-5p promotes proliferation and migration in cholangiocarcinoma via HAND1/Wnt/beta-catenin signaling pathway. J. Oncol. 2022, 4599676. https://doi.org/10.1155/2022/4599676 (2022).
doi: 10.1155/2022/4599676
pubmed: 35466323
pmcid: 9019430
Xie, C., Huang, Z., Huang, Z., Zhang, X. & Lou, S. microRNA-206 suppresses cholangiocarcinoma cell growth and invasion by targeting Jumonji AT-rich interactive domain 2. Dig. Dis. Sci. 67, 2994–3005. https://doi.org/10.1007/s10620-021-07121-z (2022).
doi: 10.1007/s10620-021-07121-z
pubmed: 34240323
Tang, Y., Tang, Z., Yang, J., Liu, T. & Tang, Y. MicroRNA-7-5p inhibits migration, invasion and metastasis of intrahepatic cholangiocarcinoma by inhibiting MyD88. J. Clin. Transl. Hepatol. 9, 809–817. https://doi.org/10.14218/JCTH.2021.00021 (2021).
doi: 10.14218/JCTH.2021.00021
pubmed: 34966644
pmcid: 8666375
Guo, D. et al. Downregulation of miR-451 in cholangiocarcinoma help the diagnsosi and promotes tumor progression. BMC Mol. Cell Biol. 23, 46. https://doi.org/10.1186/s12860-022-00445-2 (2022).
doi: 10.1186/s12860-022-00445-2
pubmed: 36352360
pmcid: 9647969
Kitdumrongthum, S. et al. Dysregulated microRNA expression profiles in cholangiocarcinoma cell-derived exosomes. Life Sci. 210, 65–75. https://doi.org/10.1016/j.lfs.2018.08.058 (2018).
doi: 10.1016/j.lfs.2018.08.058
pubmed: 30165035
Li, H. et al. MicroRNA-191 acts as a tumor promoter by modulating the TET1-p53 pathway in intrahepatic cholangiocarcinoma. Hepatology 66, 136–151. https://doi.org/10.1002/hep.29116 (2017).
doi: 10.1002/hep.29116
pubmed: 28194813
Chusorn, P. et al. Overexpression of microRNA-21 regulating PDCD4 during tumorigenesis of liver fluke-associated cholangiocarcinoma contributes to tumor growth and metastasis. Tumour Biol. 34, 1579–1588. https://doi.org/10.1007/s13277-013-0688-0 (2013).
doi: 10.1007/s13277-013-0688-0
pubmed: 23417858
Tang, C. et al. MiR-192-5p regulates the proliferation and apoptosis of cholangiocarcinoma cells by activating MEK/ERK pathway. 3 Biotech 11, 99. https://doi.org/10.1007/s13205-021-02650-w (2021).
doi: 10.1007/s13205-021-02650-w
pubmed: 33552829
pmcid: 7843823
Conte, A. & Pierantoni, G. M. Update on the regulation of HIPK1, HIPK2 and HIPK3 protein kinases by microRNAs. Microrna 7, 178–186. https://doi.org/10.2174/2211536607666180525102330 (2018).
doi: 10.2174/2211536607666180525102330
pubmed: 29793420
Li, H., Li, Q. & He, S. Hsa_circ_0025202 suppresses cell tumorigenesis and tamoxifen resistance via miR-197-3p/HIPK3 axis in breast cancer. World J. Surg. Oncol. 19, 39. https://doi.org/10.1186/s12957-021-02149-x (2021).
doi: 10.1186/s12957-021-02149-x
pubmed: 33536026
pmcid: 7860040
Liu, Y. et al. The expression level and prognostic value of HIPK3 among non-small-cell lung cancer patients in China. Onco Targets Ther. 11, 7459–7469. https://doi.org/10.2147/OTT.S166878 (2018).
doi: 10.2147/OTT.S166878
pubmed: 30498360
pmcid: 6207246
Tao, L. et al. HIPK3 inhibition by exosomal hsa-miR-101-3p Is related to metabolic reprogramming in colorectal cancer. Front. Oncol. 11, 758336. https://doi.org/10.3389/fonc.2021.758336 (2021).
doi: 10.3389/fonc.2021.758336
pubmed: 35096570
Xiao, W. et al. Identification of HIPK3 as a potential biomarker and an inhibitor of clear cell renal cell carcinoma. Aging (Albany NY) 13, 3536–3553. https://doi.org/10.18632/aging.202294 (2021).
doi: 10.18632/aging.202294
pubmed: 33495417
Ba, Y., Liu, Y., Li, C., Zhu, Y. & Xing, W. HIPK3 promotes growth and metastasis of esophageal squamous cell carcinoma via regulation of miR-599/c-MYC Axis. Onco Targets Ther. 13, 1967–1978. https://doi.org/10.2147/OTT.S217087 (2020).
doi: 10.2147/OTT.S217087
pubmed: 32189968
pmcid: 7064370
Jensen, K., Krusenstjerna-Hafstrom, R., Lohse, J., Petersen, K. H. & Derand, H. A novel quantitative immunohistochemistry method for precise protein measurements directly in formalin-fixed, paraffin-embedded specimens: Analytical performance measuring HER2. Mod. Pathol. 30, 180–193. https://doi.org/10.1038/modpathol.2016.176 (2017).
doi: 10.1038/modpathol.2016.176
pubmed: 27767098