Abstract
Background
Colorectal cancer (CRC) is a prevalent type of gastrointestinal cancer, and its poor prognosis is mainly attributed to the occurrence of invasion and metastasis. CYP1B1-AS1, as non-coding RNA, plays an important role in tumorigenesis and progression. However, the mechanism by which CYP1B1-AS1 acts in CRC is not yet understood.
Aims
The objective of this study was to investigate how CYP1B1-AS1 contributes to the development of CRC, and provide a base for CRC diagnosis and treatment.
Methods
RT-qPCR was used to detect the expression level of CYP1B1-AS1 in CRC and adjacent tissues. CCK-8, Edu, scratch healing, and transwell experiments were used to detect the changes of proliferation, migration, and invasion ability of CRC cells after overexpression or knockdown of CYP1B1-AS1 respectively. The RNA binding protein NOP58 combined with CYP1B1-AS1 was verified by RIP and RNA Pull-down experiments. Functional recovery experiments validated the interaction between CYP1B1-AS1 and NOP58 in CRC cells. The changes of EMT-related proteins were detected by Western blot, and the half-life of transcription factor SNAIL mRNA were detected by RT-qPCR after overexpression or knockdown of NOP58.
Results
CYP1B1-AS1 was found to be significantly downregulated in CRC compared to adjacent noncancerous tissues. Experiments conducted in vitro and in vivo confirmed that upregulation of CYP1B1-AS1 significantly inhibited the proliferation, migration, and invasion of CRC cells. In addition, CYP1B1-AS1 can directly bind to NOP58 and negatively regulate NOP58. The effect of overexpression CYP1B1-AS1 was reversed by NOP58 overexpression. NOP58 regulates the EMT process of CRC cells by affecting the stability of EMT-related transcription factor SNAIL mRNA, and then affects the progress of CRC.
Conclusion
This research proves that CYP1B1-AS1 can inhibit the occurrence of EMT in CRC by binding with NOP58, thus delaying the progress of CRC. This finding indicates that CYP1B1-AS1 may be a novel biomarker to improve the diagnosis and treatment of CRC.
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References
Sung H, Ferlay J, Siegel RL et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: Cancer J Clin 2021;71:209–249.
Liang TJ, Wang HX, Zheng YY et al. APC hypermethylation for early diagnosis of colorectal cancer: a meta-analysis and literature review. Oncotarget 2017;8:46468–46479.
Miller KD, Nogueira L, Mariotto AB et al. Cancer treatment and survivorship statistics, 2019. CA: Cancer J Clin 2019;69:363–85.
Ponting CP, Oliver PL, Reik W. Evolution and functions of long noncoding RNAs. Cell 2009;136:629–641.
Gibb EA, Brown CJ, Lam WL. The functional role of long non-coding RNA in human carcinomas. Mol cancer 2011;10:38.
Mahdi Khanifar M, Zafari Z, Sheykhhasan M. Crosstalk between long non-coding RNAs and p53 signaling pathway in colorectal cancer: a review study. Pathol Res Pract 2023;249:154756.
Zhang Y, Luo M, Cui X, O’Connell D, Yang Y. Long noncoding RNA NEAT1 promotes ferroptosis by modulating the miR-362-3p/MIOX axis as a ceRNA. Cell Death Differ 2022;29:1850–1863.
Hua Q, Jin M, Mi B et al. LINC01123, a c-Myc-activated long non-coding RNA, promotes proliferation and aerobic glycolysis of non-small cell lung cancer through miR-199a-5p/c-Myc axis. J Hematol Oncol 2019;12:91.
Yang Z, OuYang X, Zheng L, Dai L, Luo W. Long intergenic noncoding RNA00265 promotes proliferation of gastric cancer via the microRNA-144-3p/Chromobox 4 axis. Bioengineered 2021;12:1012–1025.
Yao ZT, Yang YM, Sun MM et al. New insights into the interplay between long non-coding RNAs and RNA-binding proteins in cancer. Cancer Commun 2022;42(2):117–140.
Li B, Kang H, Xiao Y et al. LncRNA GAL promotes colorectal cancer liver metastasis through stabilizing GLUT1. Oncogene 2022;41:1882–1894.
Kim J, Abdelmohsen K, Yang X et al. LncRNA OIP5-AS1/cyrano sponges RNA-binding protein HuR. Nucleic Acids Res 2016;44:2378–2392.
Bridges MC, Daulagala AC, Kourtidis A. LNCcation: lncRNA localization and function. J Cell Biol 2021;220(2):e202009045.
Ye T, Li LL, Peng XM, Li Q. CYP1B1-AS1 is a novel biomarker in glioblastoma by comprehensive analysis. Dis Mark 2021;2021:8565943.
Ren J, Wang A, Liu J, Yuan Q. Identification and validation of a novel redox-related lncRNA prognostic signature in lung adenocarcinoma. Bioengineered 2021;12:4331–4348.
Dekker E, Tanis PJ, Vleugels JLA, Kasi PM, Wallace MB. Colorectal cancer. Lancet 2019;394(10207):1467–1480.
Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA: Cancer J Clin 2015;65:87–108.
He D, Ma L, Feng R et al. Analyzing large-scale samples highlights significant association between rs10411210 polymorphism and colorectal cancer. Biomed Pharmacother Biomed Pharmacother 2015;74:164–8.
Lévy J, Cacheux W, Bara MA et al. Intestinal inhibition of Atg7 prevents tumour initiation through a microbiome-influenced immune response and suppresses tumour growth. Nat Cell Biol 2015;17:1062–1073.
Nishihara R, Wu K, Lochhead P et al. Long-term colorectal-cancer incidence and mortality after lower endoscopy. N Engl J Med 2013;369:1095–1105.
Mittal V. Epithelial mesenchymal transition in tumor metastasis. Ann Rev Pathol 2018;13:395–412.
Lan Y, Xiao X, He Z et al. Long noncoding RNA OCC-1 suppresses cell growth through destabilizing HuR protein in colorectal cancer. Nucleic Acids Res 2018;46:5809–5821.
Ma Y, Yang Y, Wang F et al. Long non-coding RNA CCAL regulates colorectal cancer progression by activating Wnt/β-catenin signalling pathway via suppression of activator protein 2α. Gut 2016;65:1494–1504.
Taniue K, Kurimoto A, Sugimasa H et al. Long noncoding RNA UPAT promotes colon tumorigenesis by inhibiting degradation of UHRF1. Proc Natl Acad Sci USA 2016;113:1273–1278.
Sartorelli V, Lauberth SM. Enhancer RNAs are an important regulatory layer of the epigenome. Nat Struct Mol Biol 2020;27:521–528.
Di W, Weinan X, Xin L et al. Long noncoding RNA SNHG14 facilitates colorectal cancer metastasis through targeting EZH2-regulated EPHA7. Cell Death Dis 2019;10:514.
Zheng S, Lin F, Zhang M, Fu J, Ge X, Mu N. AK001058 promotes the proliferation and migration of colorectal cancer cells by regulating methylation of ADAMTS12. Am J Transl Res 2019;11:5869–5878.
Köster T, Marondedze C, Meyer K, Staiger D. RNA-binding proteins revisited—the emerging Arabidopsis mRNA INTERACTOME. Trends Plant Sci 2017;22:512–526.
Hentze MW, Castello A, Schwarzl T, Preiss T. A brave new world of RNA-binding proteins. Nat Rev Mol Cell Biol 2018;19:327–341.
Fang Y, Fullwood MJ. Roles, functions, and mechanisms of long non-coding RNAs in cancer. Genomics Proteom Bioinform 2016;14:42–54.
Cervantes M, Forné I, Ranjit S, Gratton E, Imhof A, Sassone-Corsi P. BMAL1 associates with NOP58 in the nucleolus and contributes to pre-rRNA processing. iScience 2020;23:101151.
He J, Yu J. Long noncoding RNA FAM83A-AS1 facilitates hepatocellular carcinoma progression by binding with NOP58 to enhance the mRNA stability of FAM83A. Biosci Rep 2019. https://doi.org/10.1042/BSR20192550.
Qi L, Sun B, Yang B, Lu S. PGM5P3-AS1 regulates MAP1LC3C to promote cell ferroptosis and thus inhibiting the malignant progression of triple-negative breast cancer. Breast Cancer Res Treat 2022;193:305–318.
Acknowledgment
The authors thank you sincerely to Jiangxi Key Laboratory of Molecular Medicine for offering excellent experimental facilities for this study.
Funding
This work was funded by Natural Science Foundation of Jiangxi Provincial [Grant No: 20171BAB205064] and National Natural Science Foundation of China [Grant No: 81860432].
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Study conception and design performed by WS and BL; Developed the methodology, wrote, reviewed, and revised the manuscript performed by ZW; FC, LY, XL, ZL, ZH, SM, XC, JW contributed to data acquisition, analysis, and interpretation, as well as statistical analysis; Wei Shen provided technical and material support. All authors have read and approved the final version of the manuscript.
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Wu, Z., Cheng, F., Yuan, L. et al. CYP1B1-AS1 Delays the Malignant Progression of Colorectal Cancer by Binding with NOP58. Dig Dis Sci 69, 437–452 (2024). https://doi.org/10.1007/s10620-023-08206-7
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DOI: https://doi.org/10.1007/s10620-023-08206-7