A study of microRNAs as new prognostic biomarkers in anal cancer patients
DOI:
https://doi.org/10.2340/1651-226X.2024.27976Keywords:
Anal cancer biopsies, MicroRNAs, Prognostic factorsAbstract
Background: MicroRNA (MiR) influences the growth of cancer by regulation of mRNA for 50–60% of all genes. We present as per our knowledge the first global analysis of microRNA expression in anal cancer patients and their prognostic impact.
Methods: Twenty-nine patients with T1-4 N0-3 M0 anal cancer treated with curative intent from September 2003 to April 2011 were included in the study. RNA was extracted from fresh frozen tissue and sequenced using NGS. Differentially expressed microRNAs were identified using the R-package DEseq2 and the endpoints were time to progression (TTP) and cancer specific survival (CSS).
Results: Five microRNAs were significantly associated with 5-year progression free survival (PFS): Low expression of two microRNAs was associated with higher PFS, miR-1246 (100% vs. 55.6%, p = 0.008), and miR-135b-5p (92.9% vs. 59.3%, p = 0.041). On the other hand, high expressions of three microRNAs were associated with higher PFS, miR-148a-3p (93.3% vs. 53.6%, p = 0.025), miR-99a-5p (92.9% vs. 57.1%, p = 0.016), and let-7c-3p (92.9% vs. 57.1%, p = 0.016). Corresponding findings were documented for CSS.
Interpretation: Our study identified five microRNAs as prognostic markers in anal cancer. MiR-1246 and microRNA-135b-5p were oncoMiRs (miRs with oncogene effects), while miR-148a-3p, miR- 99a-5p, and let-7c-3p acted as tumour suppressors in anal cancer patients.
Downloads
References
Guren MG, Aagnes B, Nygard M, Dahl O, Møller B. Rising incidence and improved survival of anal squamous cell carcinoma in Norway, 1987–2016. Clin Colorectal Cancer. 2019;18:e96–103. https://doi.org/10.1016/j.clcc.2018.10.001 DOI: https://doi.org/10.1016/j.clcc.2018.10.001
Islami F, Ferlay J, Lortet-Tieulent J, Bray F, Jemal A. International trends in anal cancer incidence rates. Int J Epidemiol. 2017;46:924–38. https://doi.org/10.1093/ije/dyx200 DOI: https://doi.org/10.1093/ije/dyx200
Dahl O, Myklebust MP, Dale JE, Leon O, Serup-Hansen E, Jakobsen A et al. Evaluation of the stage classification of anal cancer by the TNM 8th version versus the TNM 7th version. Acta Oncol. 2020;59:1016–23. https://doi.org/10.1080/0284186X.2020.1778180 DOI: https://doi.org/10.1080/0284186X.2020.1778180
James RD, Glynne-Jones R, Meadows HM, Cunningham D, Sun Myint A, Saunders MP et al. Mitomycin or cisplatin chemoradiation with or without maintenance chemotherapy for treatment of squamous-cell carcinoma of the anus (ACT II): a randomised, phase 3, open-label, 2 x 2 factorial trial. Lancet Oncol. 2013;14:516–24. https://doi.org/10.1016/S1470-2045(13)70086-X DOI: https://doi.org/10.1016/S1470-2045(13)70086-X
Leon O, Guren M, Hagberg O, Glimelius B, Dahl O, Havsteen H et al. Anal carcinoma – survival and recurrence in a large cohort of patients treated according to Nordic guidelines. Radiother Oncol. 2014;113:352–8. https://doi.org/10.1016/j.radonc.2014.10.002 DOI: https://doi.org/10.1016/j.radonc.2014.10.002
Balermpas P, Martin D, Wieland U, Rave-Fränk M, Strebhardt K, Rödel C et al. Human papilloma virus load and PD-1/PD-L1, CD8(+) and FOXP3 in anal cancer patients treated with chemoradiotherapy: rationale for immunotherapy. Oncoimmunology. 2017;6:e1288331. https://doi.org/10.1080/2162402X.2017.1288331 DOI: https://doi.org/10.1080/2162402X.2017.1288331
Bruland O, Fluge O, Immervoll H, Balteskard L, Myklebust, Skarstein A et al. Gene expression reveals two distinct groups of anal carcino-mas with clinical implications. Br J Cancer. 2008;98:1264–73. https://doi.org/10.1038/sj.bjc.6604285 DOI: https://doi.org/10.1038/sj.bjc.6604285
Meulendijks D, Tomasoa NB, Dewit L, Smits PH, Bakker R, van Velthuysen ML et al. HPV-negative squamous cell carcinoma of the anal canal is unresponsive to standard treatment and frequently carries disruptive mutations in TP53. Br J Cancer. 2015;112:1358–66. https://doi.org/10.1038/bjc.2015.20 DOI: https://doi.org/10.1038/bjc.2015.20
Soares PC, Abdelhay ES, Thuler LCS, Moreia Soares B, Demachki S, Rocha Fero GV et al. HPV positive, wild type TP53, and p16 overexpres-sion correlate with the absence of residual tumors after chemoradiotherapy in anal squamous cell carcinoma. BMC Gastroenterol. 2018;18:30. https://doi.org/10.1186/s12876-018-0758-2 DOI: https://doi.org/10.1186/s12876-018-0758-2
Kim T, Croce CM. MicroRNA: trends in clinical trials of cancer diagnosis and therapy strategies. Exp Mol Med. 2023;55:1314–21. https://doi.org/10.1038/s12276-023-01050-9 DOI: https://doi.org/10.1038/s12276-023-01050-9
Myklebust MP, Bruland O, Fluge O, Skarstein A, Balteskard L, Dahl O. MicroRNA-15b is induced with E2F-controlled genes in HPV-related cancer. Br J Cancer. 2011;105:1719–25. https://doi.org/10.1038/bjc.2011.457 DOI: https://doi.org/10.1038/bjc.2011.457
Hermanek P, Sobin LH. TNM classification of malignant tumours. UICC. Berlin: Springer Verlag; 1987, 1–197. DOI: https://doi.org/10.1007/978-3-642-82982-6_1
Brierley JD, Gospodarowicz M, Wittekind C. TNM classification of malignant tumours. 8th ed. Hoboken (NL): Wiley-Blackwell; 2016, 1–272. DOI: https://doi.org/10.1002/9780471420194.tnmc01.pub3
Sobin LH, Gospodarowicz M, Wittekind C. TNM classification of malignant tumours 7th ed. Chichester (UK): Wiley-Blackwell; 2009: 1–256. DOI: https://doi.org/10.1002/9780471420194.tnmc26
Bentzen AG, Guren MG, Wanderås EH, Frykholm G, Tveit KM, Wilsgaard T et al. Chemoradiotherapy of anal carcinoma: survival and recurrence in an unselected national cohort. Int J Radiat Oncol Biol Phys. 2012;83:e173–80. https://doi.org/10.1016/j.ijrobp.2011.12.062 DOI: https://doi.org/10.1016/j.ijrobp.2011.12.062
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550. https://doi.org/10.1186/s13059-014-0550-8 DOI: https://doi.org/10.1186/s13059-014-0550-8
Licursi V, Conte F, Fiscon G, Paci P. MIENTURNET: an interactive web tool for microRNA-target enrichment and network-based analysis. BMC Bioinform. 2019;20:545. DOI: https://doi.org/10.1186/s12859-019-3105-x
Huang H-Y, Lin YCD, Li J, Huang KY, Shrestha S, Hong HC, et al. miRTarBase 2020: updates to the experimentally validated microRNA-target interaction database. Nucl Acids Res. 2020;48:D148–54. https://doi.org/10.1093/nar/gkz896 DOI: https://doi.org/10.1093/nar/gkz896
Wu T, Hu E, Xu S, Chen M, Guo P, Dai Z et al. clusterProfiler 4.0: a universal enrichment tool for interpreting omics data. Innovation (N Y). 2021;2:100141. https://doi.org/10.1016/j.xinn.2021.100141 DOI: https://doi.org/10.1016/j.xinn.2021.100141
Du P, Lai YH, Yao DS, Chen JY, Ding N. Downregulation of microRNA-1246 inhibits tumor growth and promotes apoptosis of cervical cancer cells by targeting thrombospondin-2. Oncol Lett. 2019;18:2491–9. DOI: https://doi.org/10.3892/ol.2019.10571
Chen J, Yao D, Li Y, Chen H, He C, Ding N et al. Serum microRNA expression levels can predict lymph node metastasis in patients with early-stage cervical squamous cell carcinoma. Int J Mol Med. 2013;32:557–67. ttps://doi.org/10.3892/ijmm.2013.1424 DOI: https://doi.org/10.3892/ijmm.2013.1424
Sakha S, Muramatsu T, Ueda K, Inazawa J. Exosomal microRNA miR-1246 induces cell motility and invasion through the regulation of DENND2D in oral squamous cell carcinoma. Sci Rep. 2016;6:38750. DOI: https://doi.org/10.1038/srep38750
Yang F, Xiong H, Duan L, Li Q, Li X, Zhou Y et al. MiR-1246 promotes metastasis and invasion of A549 cells by targeting GSK-3betaMediated Wnt/beta-Catenin pathway. Cancer Res Treat. 2019;51:1420–9. https://doi.org/10.4143/crt.2018.638 DOI: https://doi.org/10.4143/crt.2018.638
Yu Y, Yu F, Sun P. MicroRNA-1246 promotes melanoma progression through targeting FOXA2. Onco Targets Ther. 2020;13:1245–53. DOI: https://doi.org/10.2147/OTT.S234276
Peng W, Li J, Chen, Gu Q, Yang P, Qian W et al. Upregulated METTL3 promotes metastasis of colorectal cancer via miR-1246/SPRED2/MAPK signaling pathway. J Exp Clin Cancer Res. 2019;38:393. https://doi.org/10.1186/s13046-019-1408-4 DOI: https://doi.org/10.1186/s13046-019-1408-4
Zhang Y, Liao JM, Zeng SX, Lu H. p53 downregulates Down syndrome-associated DYRK1A through miR-1246. EMBO Rep. 2011;12:811–7. DOI: https://doi.org/10.1038/embor.2011.98
Cooks T, Pateras IS, Jenkins LM, Patel KM, Robles A, Morris J et al. Mutant p53 cancers reprogram macrophages to tumor supporting macrophages via exosomal miR-1246. Nat Commun. 2018;9:771. https://doi.org/10.1038/s41467-018-03224-w DOI: https://doi.org/10.1038/s41467-018-03224-w
Qian M, Wang S, Guo X, Wang J, Zhang Z, Qui W et al. Hypoxic glioma-derived exosomes deliver microRNA-1246 to induce M2 macrophage polarization by targeting TERF2IP via the STAT3 and NF-kappaB pathways. Oncogene. 2020;39:428–42. DOI: https://doi.org/10.1038/s41388-019-0996-y
Xu YF, Hannafon BN, Khatri U, Gin A, Ding WQ. The origin of exosomal miR-1246 in human cancer cells. RNA Biol. 2019;16:770–84. DOI: https://doi.org/10.1080/15476286.2019.1585738
Hannafon BN, Trigoso YD, Calloway CL, Zhao YD, Lum DH, Welm AL et al. Plasma exosome microRNAs are indicative of breast cancer. Breast Cancer Res. 2016;18:90. https://doi.org/10.1186/s13058-016-0753-x DOI: https://doi.org/10.1186/s13058-016-0753-x
Li XJ, Ren ZJ, Tang JH, Yu Q. Exosomal MicroRNA MiR-1246 promotes cell proliferation, invasion and drug resistance by targeting CCNG2 in breast cancer. Cell Physiol Biochem. 2017;44:1741–8. DOI: https://doi.org/10.1159/000485780
Chuma M, Toyoda H, Matsuzaki J, Saito Y, Kumada T, Tada T et al. Circulating microRNA-1246 as a possible biomarker for early tumor recurrence of hepatocellular carcinoma. Hepatol Res. 2019;49:810–22. https://doi.org/10.1111/hepr.13338 DOI: https://doi.org/10.1111/hepr.13338
Wang Y, Zhang C, Zhang P, Guo G, Jiang T, Zhao X et al. Serum exosomal microRNAs combined with alpha-fetoprotein as diagnostic markers of hepatocellular carcinoma. Cancer Med. 2018;7:1670–9. DOI: https://doi.org/10.1002/cam4.1390
Ishige F, Hoshino I, Iwatate Y, Arimitsu H, Yanagibashi H, Nagase H et al. MIR1246 in body fluids as a biomarker for pancreatic cancer. Sci Rep. 2020;10:8723. https://doi.org/10.1038/s41598-020-65695-6 DOI: https://doi.org/10.1038/s41598-020-65695-6
Shi Y, Wang Z, Zhu X, Chen L, Ma Y, Wang J et al. Exosomal miR-1246 in serum as a potential biomarker for early diagnosis of gastric can-cer. Int J Clin Oncol. 2020;25:89–99. DOI: https://doi.org/10.1007/s10147-019-01532-9
Desmond BJ, Dennett ER, Danielson KM. Circulating extracellular vesicle MicroRNA as diagnostic biomarkers in early colorectal cancer – a review. Cancers (Basel). 2019;12:52. https://doi.org/10.3390/cancers12010052 DOI: https://doi.org/10.3390/cancers12010052
Hoshino I, Yokota H, Ishige F, Iwatate Y, Takeshita N, Nagase H et al. Radiogenomics predicts the expression of microRNA-1246 in the serum of esophageal cancer patients. Sci Rep. 2020;10:2532. DOI: https://doi.org/10.1038/s41598-020-59500-7
Takeshita N, Hoshino I, Mori M, Akutsu Y, Hanari N, Yoneyama Y et al. Serum microRNA expression profile: miR-1246 as a novel diagnostic and prognostic biomarker for oesophageal squamous cell carcinoma. Br J Cancer. 2013;108:644–52. DOI: https://doi.org/10.1038/bjc.2013.8
Bhagirath D, Yang TL, Bucay N, Sekhon K, Majid S, Shahryari V et al. microRNA-1246 is an exosomal biomarker for aggressive prostate cancer. Cancer Res. 2018;78:1833–44. https://doi.org/10.1158/0008-5472.CAN-17-2069 DOI: https://doi.org/10.1158/0008-5472.CAN-17-2069
Chen Z, Li Z, Soutto M, Wang W, Blanca Piazuelo M, Zhu S et al. Integrated analysis of mouse and human gastric neoplasms identifies conserved microRNA networks in gastric carcinogenesis. Gastroenterology. 2019;156:1127–39.e1128. https://doi.org/10.1053/j.gastro.2018.11.052 DOI: https://doi.org/10.1053/j.gastro.2018.11.052
Gao S, Zhou F, Zhao C, Ma Z, Jia R, Liang S et al. Gastric cardia adenocarcinoma microRNA profiling in Chinese patients. Tumour Biol. 2016;37:9411–22. https://doi.org/10.1007/s13277-016-4824-5 DOI: https://doi.org/10.1007/s13277-016-4824-5
Lu M, Huang Y, Sun W, Li P, Li L, Li L. miR-135b-5p promotes gastric cancer progression by targeting CMTM3. Int J Oncol. 2018;52:589–98. DOI: https://doi.org/10.3892/ijo.2017.4222
Han X, Saiyin H, Zhao J, Fang Y, Shi C, Lou W et al. Overexpression of miR-135b-5p promotes unfavorable clinical characteristics and poor prognosis via the repression of SFRP4 in pancreatic cancer. Oncotarget. 2017;8:62195–207. https://doi.org/10.18632/oncotarget.19150 DOI: https://doi.org/10.18632/oncotarget.19150
Zhang Z, Che X, Yang N, Bai Z, Wu Y, Zhao L et al. miR-135b-5p Promotes migration, invasion and EMT of pancreatic cancer cells by targeting NR3C2. Biomed Pharmacother. 2017;96:1341–8. DOI: https://doi.org/10.1016/j.biopha.2017.11.074
Li CY, Zhang WW, Xiang JL, Wang XH, Li J, Wang JL. Identification of microRNAs as novel biomarkers for esophageal squamous cell carcino-ma: a study based on The Cancer Genome Atlas (TCGA) and bioinformatics. Chin Med J (Engl). 2019;132:2213–22. https://doi.org/10.1097/CM9.0000000000000427 DOI: https://doi.org/10.1097/CM9.0000000000000427
Zhao CC, Jiao Y, Zhang YY, Ning J, Zhang YR, Xu J et al. Lnc SMAD5-AS1 as ceRNA inhibit proliferation of diffuse large B cell lymphoma via Wnt/beta-catenin pathway by sponging miR-135b-5p to elevate expression of APC. Cell Death Dis. 2019;10:252. DOI: https://doi.org/10.1038/s41419-019-1479-3
Amirnasr A, Verdijk RM, van Kuijk PF, Kartal P, Vriends ALM, French P et al. Deregulated microRNAs in neurofibromatosis type 1 derived malignant peripheral nerve sheath tumors. Sci Rep. 2020;10:2927. https://doi.org/10.1038/s41598-020-59789-4 DOI: https://doi.org/10.1038/s41598-020-59789-4
Zeljic K, Jovanovic I, Jovanovic J, Magic Z, Stankovic A, Supic G. MicroRNA meta-signature of oral cancer: evidence from a meta-analysis. Ups J Med Sci. 2018;123:43–9. DOI: https://doi.org/10.1080/03009734.2018.1439551
Kanth P, Hazel MW, Boucher KM, Yang Z, Wang L, Bronner MP et al. Small RNA sequencing of sessile serrated polyps identifies microRNA profile associated with colon cancer. Genes Chromosomes Cancer. 2019;58:23–33. https://doi.org/10.1002/gcc.22686 DOI: https://doi.org/10.1002/gcc.22686
Nagel R, le Sage C, Diosdado B, van der Vaal M, Oude Vrielink JAF, Bolijn A et al. Regulation of the adenomatous polyposis coli gene by the miR-135 family in colorectal cancer. Cancer Res. 2008;68:5795–802. https://doi.org/10.1158/0008-5472.CAN-08-0951 DOI: https://doi.org/10.1158/0008-5472.CAN-08-0951
Yin L, Xiao X, Georgikou C, Luo Y, Liu L, Gladkich J et al. Sulforaphane induces miR135b-5p and its target gene, RASAL2, thereby inhibiting the progression of pancreatic cancer. Mol Ther Oncolytics. 2019;14:74–81. DOI: https://doi.org/10.1016/j.omto.2019.03.011
Milanesi E, Dobre M, Bucuroiu AI, Herlea V, Manuc TE, Salvi A et al. miRNAs-based molecular signature for KRAS mutated and wild type colorectal cancer: an explorative study. J Immunol Res. 2020;2020:4927120. https://doi.org/10.1155/2020/4927120 DOI: https://doi.org/10.1155/2020/4927120
Li Y, Deng X, Zeng X, Peng X. The role of Mir-148a in cancer. J Cancer. 2016;7:1233–41. DOI: https://doi.org/10.7150/jca.14616
Bao C, Guo L. MicroRNA-148a-3p inhibits cancer progression and is a novel screening biomarker for gastric cancer. J Clin Lab Anal. 2020;34:e23454. https://doi.org/10.1002/jcla.23454 DOI: https://doi.org/10.1002/jcla.23454
Ghafouri-Fard S, Shoorei H, Dashti S, Branicki W, Taheri M. Expression profile of lncRNAs and miRNAs in esophageal cancer: implications in diagnosis, prognosis, and therapeutic response. J Cell Physiol. 2020;235:9269–90. DOI: https://doi.org/10.1002/jcp.29825
Lin Z, Chen Y, Lin Y, Lin H, Li H, Su X et al. Potential miRNA biomarkers for the diagnosis and prognosis of esophageal cancer detected by a novel absolute quantitative RT-qPCR method. Sci Rep. 2020;10:20065. DOI: https://doi.org/10.1038/s41598-020-77119-6
Wang Y, Hu Y, Guo J, Wang L. miR-148a-3p suppresses the proliferation and invasion of esophageal cancer by targeting DNMT1. Genet Test Mol Biomarkers. 2019;23:98–104. https://doi.org/10.1089/gtmb.2018.0285 DOI: https://doi.org/10.1089/gtmb.2018.0285
Fu X, Hong L, Yang Z, Tu Y, Xin W, Zha M et al. MicroRNA-148a-3p suppresses epithelial-to-mesenchymal transition and stemness properties via Wnt1-mediated Wnt/beta-catenin pathway in pancreatic cancer. J Cell Mol Med. 2020;24:13020–35. DOI: https://doi.org/10.1111/jcmm.15900
Xie Q, Yu Z, Lu Y, Fan J, Ni Y, Ma L. microRNA-148a-3p inhibited the proliferation and epithelial-mesenchymal transition progression of non-small-cell lung cancer via modulating Ras/MAPK/Erk signaling. J Cell Physiol. 2019;234:12786–99. https://doi.org/10.1002/jcp.27899 DOI: https://doi.org/10.1002/jcp.27899
Ieong C, Ma J, Lai W. RALBP1 regulates oral cancer cells via Akt and is a novel target of miR-148a-3p and miR-148b-3p. J Oral Pathol Med. 2019;48:919–28. https://doi.org/10.1111/jop.12936 DOI: https://doi.org/10.1111/jop.12936
Wu T, Qu L, He G, Tian L, Li L, Zhou H et al. Regulation of laryngeal squamous cell cancer progression by the lncRNA H19/miR-148a-3p/DNMT1 axis. Oncotarget. 2016;7:11553–66. DOI: https://doi.org/10.18632/oncotarget.7270
Huang Z, Wen J, Yu J, Liao J, Liu S, Cai N et al. MicroRNA-148a-3p inhibits progression of hepatocelluar carcinoma by repressing SMAD2 expression in an Ago2 dependent manner. J Exp Clin Cancer Res. 2020;39:150. https://doi.org/10.1186/s13046-020-01649-0 DOI: https://doi.org/10.1186/s13046-020-01649-0
Wang X, Liang Z, Xu X, Li J, Meng S, Li S et al. miR-148a-3p represses proliferation and EMT by establishing regulatory circuits between ERBB3/AKT2/c-myc and DNMT1 in bladder cancer. Cell Death Dis. 2016;7:e2503. DOI: https://doi.org/10.1038/cddis.2016.373
Wang W, Dong J, Wang M, Yao S, Tian X, Cui X et al. miR-148a-3p suppresses epithelial ovarian cancer progression primarily by targeting c-Met. Oncol Lett. 2018;15:6131–6. DOI: https://doi.org/10.3892/ol.2018.8110
Liu Y, Huang X, Lu D, Feng Y, Xu R, Li X et al. LncRNA SNHG4 promotes the increased growth of endometrial tissue outside the uterine cavity via regulating c-Met mediated by miR-148a-3p. Mol Cell Endocrinol 2020;514:110887,1-9. https://doi.org/10.1016/j.mce.2020.110887 DOI: https://doi.org/10.1016/j.mce.2020.110887
Ashizawa M, Okayama H, Ishigame T, Min AKT, Saito K, Ujiie D et al. miRNA-148a-3p regulates immunosuppression in DNA mismatch repair-deficient colorectal cancer by targeting PD-L1. Mol Cancer Res. 2019;17:1403–13. DOI: https://doi.org/10.1158/1541-7786.MCR-18-0831
Okada R, Koshizuka K, Yamada Y, Moriya S, Kikkawa N, Kinoshita T et al. Regulation of oncogenic targets by miR-99a-3p (Passenger Strand of miR-99a-Duplex) in head and neck squamous cell carcinoma. Cells. 2019;8:1535. https://doi.org/10.3390/cells8121535 DOI: https://doi.org/10.3390/cells8121535
Wei GG, Guo WP, Tang ZY, Li SH, Wu HY, Zhang LC. Expression level and prospective mechanism of miRNA-99a-3p in head and neck squa-mous cell carcinoma based on miRNA-chip and miRNA-sequencing data in 1, 167 cases. Pathol Res Pract. 2019;215:963–76. DOI: https://doi.org/10.1016/j.prp.2019.02.002
Wu C, Tong L, Wu C, Chen D, Chen J, Li Q et al. Two miRNA prognostic signatures of head and neck squamous cell carcinoma: a bioinformatic analysis based on the TCGA dataset. Cancer Med. 2020;9:2631–42. DOI: https://doi.org/10.1002/cam4.2915
Mizuno K, Tanigawa K, Nohata N, Misono S, Okada R, Asai S et al. FAM64A: a novel oncogenic target of lung adenocarcinoma regulated by both strands of miR-99a (miR-99a-5p and miR-99a-3p). Cells. 2020;9:2083. https://doi.org/10.3390/cells9092083 DOI: https://doi.org/10.3390/cells9092083
Shinden Y, Hirashima T, Nohata N, Toda H, Okada R, Asai S et al. Molecular pathogenesis of breast cancer: impact of miR-99a-5p and miR-99a-3p regulation on oncogenic genes. J Hum Genet. 2020;66:519–34. https://doi.org/10.1038/s10038-020-00865-y DOI: https://doi.org/10.1038/s10038-020-00865-y
Arai T, Okato A, Yamada Y, Sugawara S, Kurozumi A, Kojima S et al. Regulation of NCAPG by miR-99a-3p (passenger strand) inhibits cancer cell aggressiveness and is involved in CRPC. Cancer Med. 2018;7:1988–2002. DOI: https://doi.org/10.1002/cam4.1455
Kalinkova L, Kajo K, Karhanek M, Waschmannova L, Suran P, Zmetakova I et al. Discriminating miRNA profiles between endometrioid well- and poorly-differentiated tumours and endometrioid and serous subtypes of endometrial cancers. Int J Mol Sci. 2020;21:6071. DOI: https://doi.org/10.3390/ijms21176071
Garrido-Cano I, Constancio V, Adam-Artigues A, Lamerinhas A, Simon S, Ortega B et al. Circulating miR-99a-5p expression in plasma: a potential biomarker for early diagnosis of breast cancer. Int J Mol Sci. 2020;21:7427. https://doi.org/10.3390/ijms21197427 DOI: https://doi.org/10.3390/ijms21197427
Saito R, Maruyama S, Kawaguchi Y, Akaike H, Shimizu H, Furya S et al. miR-99a-5p as possible diagnostic and prognostic marker in patients with gastric cancer. J Surg Res. 2020;250:193–9. DOI: https://doi.org/10.1016/j.jss.2020.01.004
Barh D, Malhotra R, Ravi B, Sindhurani P. MicroRNA let-7: an emerging next-generation cancer therapeutic. Curr Oncol. 2010;17:70–80. https://doi.org/10.3747/co.v17i1.356 DOI: https://doi.org/10.3747/co.v17i1.356
Wang T, Wang G, Hao D, Liu X, Wang D, Ning N et al. Aberrant regulation of the LIN28A/LIN28B and let-7 loop in human malignant tumors and its effects on the hallmarks of cancer. Mol Cancer. 2015;14:125. DOI: https://doi.org/10.1186/s12943-015-0402-5
Chen Y, Xie C, Zheng X, Nie X, Wang Z, Liu H et al. LIN28/let-7/PD-L1 pathway as a target for cancer immunotherapy. Cancer Immunol Res. 2019;7:487–97. DOI: https://doi.org/10.1158/2326-6066.CIR-18-0331
Lee YS, Dutta A. The tumor suppressor microRNA let-7 represses the HMGA2 oncogene. Genes Dev. 2007;21:1025–30. https://doi.org/10.1101/gad.1540407 DOI: https://doi.org/10.1101/gad.1540407
Mayr C, Hemann MT, Bartel DP. Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation. Science. 2007;315:1576–9. DOI: https://doi.org/10.1126/science.1137999
Park SM, Shell S, Radjabi AR, Schickel R, Feig C, Boyerinas B et al. Let-7 prevents early cancer progression by suppressing expression of the embryonic gene HMGA2. Cell Cycle. 2007;6:2585–90. https://doi.org/10.4161/cc.6.21.4845 DOI: https://doi.org/10.4161/cc.6.21.4845
Shell S, Park SM, Radjabi AR, Schickel R, Kistner EO, Jewell DA et al. Let-7 expression defines two differentiation stages of cancer. Proc Natl Acad Sci U S A. 2007;104:11400–5. https://doi.org/10.1073/pnas.0704372104 DOI: https://doi.org/10.1073/pnas.0704372104
Johnson CD, Esquela-Kerscher A, Stefani G, Byrom M, Kelnar K, Ovcharenko D et al. The let-7 microRNA represses cell proliferation path-ways in human cells. Cancer Res. 2007;67:7713–22. DOI: https://doi.org/10.1158/0008-5472.CAN-07-1083
Wu Y, Zhang Y, Zheng X, Dai F, Lu Y, Dai L et al. Circular RNA circCORO1C promotes laryngeal squamous cell carcinoma progression by modulating the let-7c-5p/PBX3 axis. Mol Cancer. 2020;19:99. DOI: https://doi.org/10.1186/s12943-020-01215-4
Wu Q, Liu P, Lao G, Liu Y, Zhang W, Ma C. Comprehensive analysis of circRNA-miRNA-mRNA network in cervical squamous cell carcinoma by integrated analysis. Onco Targets Ther. 2020;13:8641–50. https://doi.org/10.2147/OTT.S254323 DOI: https://doi.org/10.2147/OTT.S254323
Huang L, Lin JX, Yu YH, Zhang MY, Wang HY, Zheng M. Downregulation of six microRNAs is associated with advanced stage, lymph node metastasis and poor prognosis in small cell carcinoma of the cervix. PLoS One. 2012;7:e33762. DOI: https://doi.org/10.1371/journal.pone.0033762
D’Souza W, Kumar A. microRNAs in oral cancer: moving from bench to bed as next generation medicine. Oral Oncol. 2020;111:104916. https://doi.org/10.1016/j.oraloncology.2020.104916 DOI: https://doi.org/10.1016/j.oraloncology.2020.104916
Ma J, Zhan Y, Xu Z, Li Y, Luo A, Ding F et al. ZEB1 induced miR-99b/let-7e/miR-125a cluster promotes invasion and metastasis in esophageal squamous cell carcinoma. Cancer Lett. 2017;398:37–45. https://doi.org/10.1016/j.canlet.2017.04.006 DOI: https://doi.org/10.1016/j.canlet.2017.04.006
Spagnuolo M, Costantini M, Ferriero M, Varmi M, Sperduti I, Regazzo G et al. Urinary expression of let-7c cluster as non-invasive tool to assess the risk of disease progression in patients with high grade non-muscle invasive bladder cancer: a pilot study. J Exp Clin Can-cer Res. 2020;39:68. https://doi.org/10.1186/s13046-020-01550-w DOI: https://doi.org/10.1186/s13046-020-01550-w
Chang TC, Yu D, Lee YS, Wentzel EA, Arking DE, West KM et al. Widespread microRNA repression by Myc contributes to tumorigenesis. Nat Genet. 2008;40:43–50. https://doi.org/10.1038/ng.2007.30 DOI: https://doi.org/10.1038/ng.2007.30
Frenzel A, Loven J, Henriksson MA. Targeting MYC-regulated miRNAs to combat cancer. Genes Cancer. 2010;1:660–7. https://doi.org/10.1177/1947601910377488 DOI: https://doi.org/10.1177/1947601910377488
Mulholland EJ, Green WP, Buckley NE, McCarthy HO. Exploring the potential of MicroRNA Let-7c as a therapeutic for prostate cancer. Mol Ther Nucleic Acids. 2019;18:927–37. https://doi.org/10.1016/j.omtn.2019.09.031 DOI: https://doi.org/10.1016/j.omtn.2019.09.031
Yu D, Liu X, Han G, Liu Y, Zhao X, Wang D et al. The let-7 family of microRNAs suppresses immune evasion in head and neck squamous cell carcinoma by promoting PD-L1 degra-dation. Cell Commun Signal. 2019;17:173. https://doi.org/10.1186/s12964-019-0490-8 DOI: https://doi.org/10.1186/s12964-019-0490-8
Published
How to Cite
Issue
Section
License
Copyright (c) 2023 Olav Dahl, Mette Pernille Myklebust
This work is licensed under a Creative Commons Attribution 4.0 International License.
Funding data
-
Trond Mohn stiftelse
Grant numbers BFS2015PAR2
