Hsa_circ_0007990 promotes breast cancer growth via inhibiting YBX1 protein degradation to activate E2F1 transcription.
Journal
Cell death & disease
ISSN: 2041-4889
Titre abrégé: Cell Death Dis
Pays: England
ID NLM: 101524092
Informations de publication
Date de publication:
20 Feb 2024
20 Feb 2024
Historique:
received:
22
07
2023
accepted:
31
01
2024
revised:
28
01
2024
medline:
21
2
2024
pubmed:
21
2
2024
entrez:
20
2
2024
Statut:
epublish
Résumé
Breast cancer (BC) is the most commonly diagnosed malignant tumour in females worldwide. Although remarkable advances in early detection and treatment strategies have led to decreased mortality, recurrence and metastasis remain the major causes of cancer death in BC patients. Increasing evidence has demonstrated that circular RNAs (circRNAs) play critical roles in cancer progression. However, the detailed biological functions and molecular mechanisms of circRNAs in BC are unclear. The aim of this study was to investigate the possible role of circRNAs in the progression of BC. Differentially expressed circRNAs in BC were identified by integrating breast tumour-associated somatic CNV data and circRNA high-throughput sequencing. Aberrant hsa_circ_0007990 expression and host gene copy number were detected in BC cell lines via quantitative polymerase chain reaction (qPCR). The expression level of hsa_circ_0007990 in BC tissues was validated by in situ hybridization (ISH). Loss- and gain-of-function experiments were performed in vitro and in vivo, respectively, to explore the potential biological function of hsa_circ_0007990 in BC. The underlying mechanisms of hsa_circ_0007990 were investigated through MS2 RNA pull-down, RNA immunoprecipitation, RNA fluorescence in situ hybridization, immunofluorescence, chromatin immunoprecipitation and luciferase reporter assays. The levels of hsa_circ_0007990 were elevated in BC tissues and cell lines, an effect that was partly due to host gene copy number gains. Functional assays showed that hsa_circ_0007990 promoted BC cell growth. Mechanistically, hsa_circ_0007990 could bind to YBX1 and inhibit its degradation by preventing ubiquitin/proteasome-dependent degradation, thus enhancing the expression of the cell cycle-associated gene E2F1. Rescue experiments suggested that hsa_circ_0007990 promoted BC progression through YBX1. In general, our study demonstrated that hsa_circ_0007990 modulates the ubiquitination and degradation of YBX1 protein and further regulates E2F1 expression to promote BC progression. We explored the possible function and molecular mechanism of hsa_circ_0007990 in BC and identified a novel candidate target for the treatment of BC.
Identifiants
pubmed: 38378679
doi: 10.1038/s41419-024-06527-7
pii: 10.1038/s41419-024-06527-7
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
153Informations de copyright
© 2024. The Author(s).
Références
Siegel RL, Miller KD, Wagle NS, Jemal A. Cancer statistics, 2023. CA Cancer J Clin. 2023;73:17–48.
pubmed: 36633525
doi: 10.3322/caac.21763
Loibl S, Poortmans P, Morrow M, Denkert C, Curigliano G. Breast cancer. Lancet. 2021;397:1750–69.
pubmed: 33812473
doi: 10.1016/S0140-6736(20)32381-3
Xu T, He B, Sun H, Xiong M, Nie J, Wang S, et al. Novel insights into the interaction between N6-methyladenosine modification and circular RNA. Mol Ther Nucleic Acids. 2022;27:824–37.
pubmed: 35141044
pmcid: 8807973
doi: 10.1016/j.omtn.2022.01.007
Kristensen LS, Jakobsen T, Hager H, Kjems J. The emerging roles of circRNAs in cancer and oncology. Nat Rev Clin Oncol. 2022;19:188–206.
pubmed: 34912049
doi: 10.1038/s41571-021-00585-y
Liu H, Fang D, Zhang C, Zhao Z, Liu Y, Zhao S, et al. Circular MTHFD2L RNA-encoded CM-248aa inhibits gastric cancer progression by targeting the SET-PP2A interaction. Mol Ther. 2023;31:1739–55.
pubmed: 37101395
doi: 10.1016/j.ymthe.2023.04.013
Xiong L, Liu HS, Zhou C, Yang X, Huang L, Jie HQ, et al. A novel protein encoded by circINSIG1 reprograms cholesterol metabolism by promoting the ubiquitin-dependent degradation of INSIG1 in colorectal cancer. Mol Cancer. 2023;22:72.
pubmed: 37087475
pmcid: 10122405
doi: 10.1186/s12943-023-01773-3
Yi J, Wang L, Hu GS, Zhang YY, Du J, Ding JC, et al. CircPVT1 promotes ER-positive breast tumorigenesis and drug resistance by targeting ESR1 and MAVS. EMBO J. 2023;42:e112408.
pubmed: 37009655
pmcid: 10183818
doi: 10.15252/embj.2022112408
Lee JH, Jung SM, Yang KM, Bae E, Ahn SG, Park JS, et al. A20 promotes metastasis of aggressive basal-like breast cancers through multi-monoubiquitylation of Snail1. Nat Cell Biol. 2017;19:1260–73.
pubmed: 28892081
doi: 10.1038/ncb3609
Xu T, He BS, Pan B, Pan YQ, Sun HL, Liu XX, et al. MiR-142-3p functions as a tumor suppressor by targeting RAC1/PAK1 pathway in breast cancer. J Cell Physiol. 2020;235:4928–40.
pubmed: 31674013
doi: 10.1002/jcp.29372
Ueno T, Emi M, Sato H, Ito N, Muta M, Kuroi K, et al. Genome-wide copy number analysis in primary breast cancer. Expert Opin Ther Targets. 2012;16(Suppl 1):S31–5.
pubmed: 22313367
doi: 10.1517/14728222.2011.636739
Tseng YY, Moriarity BS, Gong W, Akiyama R, Tiwari A, Kawakami H, et al. PVT1 dependence in cancer with MYC copy-number increase. Nature. 2014;512:82–6.
pubmed: 25043044
pmcid: 4767149
doi: 10.1038/nature13311
Qiu M, Xia W, Chen R, Wang S, Xu Y, Ma Z, et al. The circular RNA circPRKCI promotes tumor growth in lung adenocarcinoma. Cancer Res. 2018;78:2839–51.
pubmed: 29588350
doi: 10.1158/0008-5472.CAN-17-2808
Chen RX, Chen X, Xia LP, Zhang JX, Pan ZZ, Ma XD, et al. N(6)-methyladenosine modification of circNSUN2 facilitates cytoplasmic export and stabilizes HMGA2 to promote colorectal liver metastasis. Nat Commun. 2019;10:4695.
pubmed: 31619685
pmcid: 6795808
doi: 10.1038/s41467-019-12651-2
Cancer Genome Atlas N. Comprehensive molecular portraits of human breast tumours. Nature. 2012;490:61–70.
doi: 10.1038/nature11412
Zeng K, He B, Yang BB, Xu T, Chen X, Xu M, et al. The pro-metastasis effect of circANKS1B in breast cancer. Mol Cancer. 2018;17:160.
pubmed: 30454010
pmcid: 6240936
doi: 10.1186/s12943-018-0914-x
Misir S, Wu N, Yang BB. Specific expression and functions of circular RNAs. Cell Death Differ. 2022;29:481–91.
pubmed: 35169296
pmcid: 8901656
doi: 10.1038/s41418-022-00948-7
Wen SY, Qadir J, Yang BB. Circular RNA translation: novel protein isoforms and clinical significance. Trends Mol Med. 2022;28:405–20.
pubmed: 35379558
doi: 10.1016/j.molmed.2022.03.003
Das A, Sinha T, Shyamal S, Panda AC. Emerging role of circular RNA-protein interactions. Noncoding RNA. 2021;7:48.
pubmed: 34449657
pmcid: 8395946
Guens GP. YB-1 protein in breast cancer (scientific and personal meetings with Professor Ovchinnikov). Biochemistry. 2022;87(Suppl 1):S86–S93.
Eliseeva IA, Kim ER, Guryanov SG, Ovchinnikov LP, Lyabin DN. Y-box-binding protein 1 (YB-1) and its functions. Biochemistry. 2011;76:1402–33.
Alkrekshi A, Wang W, Rana PS, Markovic V, Sossey-Alaoui K. A comprehensive review of the functions of YB-1 in cancer stemness, metastasis and drug resistance. Cell Signal. 2021;85:110073.
pubmed: 34224843
doi: 10.1016/j.cellsig.2021.110073
Chen HZ, Tsai SY, Leone G. Emerging roles of E2Fs in cancer: an exit from cell cycle control. Nat Rev Cancer. 2009;9:785–97.
pubmed: 19851314
pmcid: 3616489
doi: 10.1038/nrc2696
Lasham A, Samuel W, Cao H, Patel R, Mehta R, Stern JL, et al. YB-1, the E2F pathway, and regulation of tumor cell growth. J Natl Cancer Inst. 2012;104:133–46.
pubmed: 22205655
doi: 10.1093/jnci/djr512
Dolfini D, Mantovani R. Targeting the Y/CCAAT box in cancer: YB-1 (YBX1) or NF-Y? Cell Death Differ. 2013;20:676–85.
pubmed: 23449390
pmcid: 3619239
doi: 10.1038/cdd.2013.13
Singh RR, Patel KP, Routbort MJ, Aldape K, Lu X, Manekia J, et al. Clinical massively parallel next-generation sequencing analysis of 409 cancer-related genes for mutations and copy number variations in solid tumours. Br J Cancer. 2014;111:2014–23.
pubmed: 25314059
pmcid: 4229640
doi: 10.1038/bjc.2014.518
Pan X, Hu X, Zhang YH, Chen L, Zhu L, Wan S, et al. Identification of the copy number variant biomarkers for breast cancer subtypes. Mol Genet Genomics. 2019;294:95–110.
pubmed: 30203254
doi: 10.1007/s00438-018-1488-4
Jun T, Chen W, Hailing C, Ning W, Qinxue C. The novel circular RNA circ-PGAP3 retards cervical cancer growth by regulating the miR-769-5p/p53 axis. Hum Cell. 2021;34:878–88.
pubmed: 33591461
doi: 10.1007/s13577-021-00493-4
He D, Yang X, Kuang W, Huang G, Liu X, Zhang Y. The novel circular RNA circ-PGAP3 promotes the proliferation and invasion of triple negative breast cancer by regulating the miR-330-3p/Myc axis. Onco Targets Ther. 2020;13:10149–59.
pubmed: 33116597
pmcid: 7553664
doi: 10.2147/OTT.S274574
Wu XB, Wu YT, Guo XX, Xiang C, Chen PS, Qin W, et al. Circular RNA hsa_circ_0007990 as a blood biomarker for unruptured intracranial aneurysm with aneurysm wall enhancement. Front Immunol. 2022;13:1061592.
pubmed: 36466848
pmcid: 9714537
doi: 10.3389/fimmu.2022.1061592
Qi X, Lin Y, Chen J, Shen B. Decoding competing endogenous RNA networks for cancer biomarker discovery. Brief Bioinform. 2020;21:441–57.
pubmed: 30715152
doi: 10.1093/bib/bbz006
Huang A, Zheng H, Wu Z, Chen M, Huang Y. Circular RNA-protein interactions: functions, mechanisms, and identification. Theranostics. 2020;10:3503–17.
pubmed: 32206104
pmcid: 7069073
doi: 10.7150/thno.42174
Goodarzi H, Liu X, Nguyen HC, Zhang S, Fish L, Tavazoie SF. Endogenous tRNA-derived fragments suppress breast cancer progression via YBX1 displacement. Cell. 2015;161:790–802.
pubmed: 25957686
pmcid: 4457382
doi: 10.1016/j.cell.2015.02.053
Lin Y, Zhang J, Li Y, Guo W, Chen L, Chen M, et al. CTPS1 promotes malignant progression of triple-negative breast cancer with transcriptional activation by YBX1. J Transl Med. 2022;20:17.
pubmed: 34991621
pmcid: 8734240
doi: 10.1186/s12967-021-03206-5
Jiang, Qiu D, Peng T, Li J, Tala S, Ren W, et al. YB-1 is a positive regulator of KLF5 transcription factor in basal-like breast cancer. Cell Death Differ. 2022;29:1283–95.
pubmed: 35022570
pmcid: 9177637
doi: 10.1038/s41418-021-00920-x
Zhang Y, Huang YX, Wang DL, Yang B, Yan HY, Lin LH, et al. LncRNA DSCAM-AS1 interacts with YBX1 to promote cancer progression by forming a positive feedback loop that activates FOXA1 transcription network. Theranostics. 2020;10:10823–37.
pubmed: 32929382
pmcid: 7482804
doi: 10.7150/thno.47830
Zheng S, Yang L, Zou Y, Liang JY, Liu P, Gao G, et al. Long non-coding RNA HUMT hypomethylation promotes lymphangiogenesis and metastasis via activating FOXK1 transcription in triple-negative breast cancer. J Hematol Oncol. 2020;13:17.
pubmed: 32138762
pmcid: 7059688
doi: 10.1186/s13045-020-00852-y
Wang M, Dai M, Wang D, Tang T, Xiong F, Xiang B, et al. The long noncoding RNA AATBC promotes breast cancer migration and invasion by interacting with YBX1 and activating the YAP1/Hippo signaling pathway. Cancer Lett. 2021;512:60–72.
pubmed: 33951538
doi: 10.1016/j.canlet.2021.04.025
Chen Q, Wang H, Li Z, Li F, Liang L, Zou Y, et al. Circular RNA ACTN4 promotes intrahepatic cholangiocarcinoma progression by recruiting YBX1 to initiate FZD7 transcription. J Hepatol. 2022;76:135–47.
pubmed: 34509526
doi: 10.1016/j.jhep.2021.08.027
Hong X, Li Q, Li J, Chen K, He Q, Zhao Y, et al. CircIPO7 promotes nasopharyngeal carcinoma metastasis and cisplatin chemoresistance by facilitating YBX1 nuclear localization. Clin Cancer Res. 2022;28:4521–35.
pubmed: 35917517
doi: 10.1158/1078-0432.CCR-22-0991
Xu J, Ji L, Liang Y, Wan Z, Zheng W, Song X, et al. CircRNA-SORE mediates sorafenib resistance in hepatocellular carcinoma by stabilizing YBX1. Signal Transduct Target Ther. 2020;5:298.
pubmed: 33361760
pmcid: 7762756
doi: 10.1038/s41392-020-00375-5
Chen S, Li K, Guo J, Chen HN, Ming Y, Jin Y, et al. circNEIL3 inhibits tumor metastasis through recruiting the E3 ubiquitin ligase Nedd4L to degrade YBX1. Proc Natl Acad Sci USA. 2023;120:e2215132120.
pubmed: 36961927
pmcid: 10068820
doi: 10.1073/pnas.2215132120
Li SY, Zhu Y, Li RN, Huang JH, You K, Yuan YF, et al. LncRNA Lnc-APUE is repressed by HNF4alpha and promotes G1/S phase transition and tumor growth by regulating MiR-20b/E2F1 axis. Adv Sci. 2021;8:2003094.
doi: 10.1002/advs.202003094
Pandolfi S, Montagnani V, Lapucci A, Stecca B. HEDGEHOG/GLI-E2F1 axis modulates iASPP expression and function and regulates melanoma cell growth. Cell Death Differ. 2015;22:2006–19.
pubmed: 26024388
pmcid: 4816112
doi: 10.1038/cdd.2015.56
Razpotnik R, Vidmar R, Fonovic M, Rozman D, Rezen T. Circular RNA hsa_circ_0062682 binds to YBX1 and promotes oncogenesis in hepatocellular carcinoma. Cancers. 2022;14:4524.
pubmed: 36139684
pmcid: 9497178
doi: 10.3390/cancers14184524