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MiRNAs in renal cell carcinoma

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Abstract

MicroRNAs (miRNAs) are small RNA sequences that act as post-transcriptional regulatory genes to control many cellular processes through pairing bases with a complementary messenger RNA (mRNA). A single miRNA molecule can regulate more than 200 different transcripts and the same mRNA can be regulated by multiple miRNAs. In this review, we highlight the importance of miRNAs and collect the existing evidence on their relationship with kidney cancer.

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References

  1. Esquela-Kerscher A, Slack FJ. Oncomirs—MicroRNAs with a role in cancer. Nat Rev Cancer. 2006;6(4):259–69.

    Article  CAS  Google Scholar 

  2. Pab V. MicroARNs una visión molecular MicroRNA (miRNA) a molecular view. Rev la Univ Ind Santander Salud. 2011;43(3):289–97.

    Google Scholar 

  3. Li C, Feng Y, Coukos G, Zhang L. Therapeutic microRNA strategies in human cancer. AAPS J. 2009;11(4):747–57.

    Article  CAS  Google Scholar 

  4. Sparano JA, Gray RJ, Makower DF, Pritchard KI, Albain KS, Hayes DF, et al. Adjuvant chemotherapy guided by a 21-gene expression assay in breast cancer. N Engl J Med. 2018;379(2):111–21.

    Article  CAS  Google Scholar 

  5. Liu W, Zabirnyk O, Wang H, Shiao Y-H, Nickerson ML, Khalil S, Anderson LM, Perantoni AO, Phang JM. MicroRNA-23b* targets proline oxidase, a mitochondrial tumor suppressor protein in renal cancer. Oncogene. 2015;29(35):4914–24.

    Article  Google Scholar 

  6. Tong AW, Fulgham P, Jay C, Chen P, Khalil I, Liu S, et al. MicroRNA profile analysis of human prostate cancers. Cancer Gene Ther. 2009;16(3):206–16.

    Article  CAS  Google Scholar 

  7. Spizzo R, Nicoloso MS, Croce CM, Calin GA. SnapShot: MicroRNAs in Cancer. Cell. 2009. https://doi.org/10.1016/j.cell.2009.04.040.

    Article  PubMed  Google Scholar 

  8. Li W, Wang Y, Liu R, Kasinski AL, Shen H, Slack FJ, et al. MicroRNA-34a: potent tumor suppressor, cancer stem cell inhibitor, and potential anticancer therapeutic. Front Cell Dev Biol. 2021;9(March):1–21.

    CAS  Google Scholar 

  9. Dutta KK, Zhong Y, Liu YT, Yamada T, Akatsuka S, Hu Q, et al. Association of microRNA-34a overexpression with proliferation is cell type-dependent. Cancer Sci. 2007;98(12):1845–52.

    Article  CAS  Google Scholar 

  10. Juan D, Alexe G, Antes T, Liu H, Madabhushi A, Delisi C, et al. Identification of a MicroRNA Panel for Clear-cell Kidney Cancer. Urology. 2017;75(4):835–41. https://doi.org/10.1016/j.urology.2009.10.033.

    Article  Google Scholar 

  11. Huang Y, Dai Y, Yang J, Chen T, Yin Y, Tang M, et al. Microarray analysis of microRNA expression in renal clear cell carcinoma. Eur J Surg Oncol. 2009;35(10):1119–23. https://doi.org/10.1016/j.ejso.2009.04.010.

    Article  CAS  PubMed  Google Scholar 

  12. Fridman E, Dotan Z, Barshack I, Ben DM, Dov A, Tabak S, et al. Accurate molecular classification of renal tumors using microRNA expression. J Mol Diagnostics. 2010;12(5):687–96. https://doi.org/10.2353/jmoldx.2010.090187.

    Article  CAS  Google Scholar 

  13. Petillo D, Kort EJ, Anema J, Furge KA, Yang XJ, Teh BT. MicroRNA profiling of human kidney cancer subtypes. Int J Oncol. 2009 Jul;35(1):109–14. http://www.ncbi.nlm.nih.gov/pubmed/19513557

  14. Trilla-Fuertes L, Miranda N, Castellano D, López-Vacas R, Farfán Tello CA, de Velasco G, et al. miRNA profiling in renal carcinoma suggest the existence of a group of pro-angionenic tumors in localized clear cell renal carcinoma. PLoS ONE. 2020;15(2): e0229075.

    Article  CAS  Google Scholar 

  15. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA. 2006;103(7):2257–61.

    Article  CAS  Google Scholar 

  16. Kulshreshtha R, Ferracin M, Wojcik SE, Garzon R, Alder H, Agosto-Perez FJ, et al. A MicroRNA signature of Hypoxia. Mol Cell Biol. 2007;27(5):1859–67.

    Article  CAS  Google Scholar 

  17. Maynard MA, Ohh M. Von hippel-lindau tumor suppressor protein and Hypoxia-inducible factor in kidney cancer. Am J Nephrol. 2004;24(1):1–13.

    Article  CAS  Google Scholar 

  18. Kurahashi R, Kadomatsu T, Baba M, Hara C, Itoh H, Miyata K, et al. MicroRNA-204–5p: A novel candidate urinary biomarker of Xp11.2 translocation renal cell carcinoma. Cancer Sci. 2019;110(6):1897–908.

    Article  CAS  Google Scholar 

  19. Dias F, Teixeira AL, Nogueira I, Morais M, Maia J, Bodo C, et al. Extracellular vesicles enriched in hsa-mir-301a-3p and hsa-mir-1293 dynamics in clear cell renal cell carcinoma patients: potential biomarkers of metastatic disease. Cancers (basel). 2020. https://doi.org/10.3390/cancers12061450.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Ge Y-Z, Wu R, Xin H, Zhu M, Lu T-Z, Liu H, et al. A tumor-specific microRNA signature predicts survival in clear cell renal cell carcinoma. J Cancer Res Clin Oncol. 2015;141(7):1291–9. https://doi.org/10.1007/s00432-015-1927-0.

    Article  CAS  PubMed  Google Scholar 

  21. Zhao X, Zhao Z, Xu W, Hou J, Du X. Down-regulation of miR-497 is associated with poor prognosis in renal cancer. Int J Clin Exp Pathol. 2015;8(1):758–64.

    PubMed  PubMed Central  Google Scholar 

  22. Yang G, Xiong G, Cao Z, Zheng S, You L, Zhang T, et al. miR-497 expression, function and clinical application in cancer. Oncotarget. 2016;7(34):55900–11.

    Article  Google Scholar 

  23. Qu F, Ye J, Pan X, Wang J, Gan S, Chu C, et al. MicroRNA-497–5p down-regulation increases PD-L1 expression in clear cell renal cell carcinoma. J Drug Target. 2019;27(1):67–74. https://doi.org/10.1080/1061186X.2018.1479755.

    Article  CAS  PubMed  Google Scholar 

  24. Huang M, Zhang T, Yao ZY, Xing C, Wu Q, Liu YW, et al. MicroRNA related prognosis biomarkers from high throughput sequencing data of kidney renal clear cell carcinoma. BMC Med Genomics. 2021;14(1):1–9. https://doi.org/10.1186/s12920-021-00932-z.

    Article  CAS  Google Scholar 

  25. Faragalla H, Youssef YM, Scorilas A, Khalil B, White NMA, Mejia-Guerrero S, et al. The clinical utility of miR-21 as a diagnostic and prognostic marker for renal cell carcinoma. J Mol Diagnostics. 2012;14(4):385–92. https://doi.org/10.1016/j.jmoldx.2012.02.003.

    Article  CAS  Google Scholar 

  26. Li W, Liu M, Feng Y, Xu YF, Huang YF, Che JP, et al. Downregulated miR-646 in clear cell renal carcinoma correlated with tumour metastasis by targeting the nin one binding protein (NOB1). Br J Cancer. 2014;111(6):1188–200.

    Article  CAS  Google Scholar 

  27. Yang FQ, Zhang HM, Chen SJ, Yan Y, Zheng JH. MiR-506 is down-regulated in clear cell renal cell carcinoma and inhibits cell growth and metastasis via targeting FLOT1. PLoS ONE. 2015;10(3):1–17.

    Article  Google Scholar 

  28. Li H, Wang RM, Liu SG, Zhang JP, Luo JY, Zhang BJ, et al. Abnormal expression of FLOT1 correlates with tumor progression and poor survival in patients with non-small cell lung cancer. Tumor Biol. 2014;35(4):3311–5.

    Article  CAS  Google Scholar 

  29. Fan B, Jin Y, Zhang H, Zhao R, Sun M, Sun M, et al. MicroRNA-21 contributes to renal cell carcinoma cell invasiveness and angiogenesis via the PDCD4/c-Jun (AP-1) signalling pathway. Vol. 56. Inter J Oncol. 2020. https://doi.org/10.3892/ijo.2019.4928.

    Article  Google Scholar 

  30. Bera A, Ghosh-Choudhury N, Dey N, Das F, Kasinath BS, Abboud HE, et al. NFκB-mediated cyclin D1 expression by microRNA-21 influences renal cancer cell proliferation. Vol. 25. Cell Signal. 2013. https://doi.org/10.1016/j.cellsig.2013.08.005.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Li M, Yin B, Chen M, Peng J, Mu X, Deng Z, et al. Downregulation of the lncRNA ASB16-AS1 decreases LARP1 expression and promotes clear cell renal cell carcinoma progression via miR-185-5p/miR-214-3p. Front Oncol. 2021;10(February):1–12.

    Google Scholar 

  32. Hirata H, Ueno K, Nakajima K, Tabatabai ZL, Hinoda Y, Ishii N, et al. Genistein downregulates onco-miR-1260b and inhibits Wnt-signalling in renal cancer cells. Br J Cancer. 2013;108(10):2070–8. https://doi.org/10.1038/bjc.2013.173.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Yang L, Zou X, Zou J, Zhang G. A review of recent research on the role of micrornas in renal cancer. Med Sci Monit. 2021;27:1–17.

    Article  CAS  Google Scholar 

  34. Kovacova J, Juracek J, Poprach A, Kopecky J, Fiala O, Svoboda M, et al. MiR-376b-3p is associated with long-term response to sunitinib in metastatic renal cell carcinoma patients. Cancer Genom Proteom. 2019;16(5):353–9.

    Article  CAS  Google Scholar 

  35. Ralla B, Busch J, Flörcken A, Westermann J, Zhao Z, Kilic E, et al. miR-9–5p in nephrectomy specimens is a potential predictor of primary resistance to first-line treatment with tyrosine kinase inhibitors in patients with metastatic renal cell carcinoma. Cancers (basel). 2018. https://doi.org/10.3390/cancers10090321.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Yuan H-X, Zhang J-P, Kong W-T, Liu Y-J, Lin Z-M, Wang W-P, et al. Elevated microRNA-185 is associated with high vascular endothelial growth factor receptor 2 expression levels and high microvessel density in clear cell renal cell carcinoma. Tumor Biol. 2014 Dec 14;35(12):12757–63. https://linkinghub.elsevier.com/retrieve/pii/S1534580708002876

  37. Fish JE, Santoro MM, Morton SU, Yu S, Yeh R-F, Wythe JD, et al. miR-126 Regulates Angiogenic Signaling and Vascular Integrity. Dev Cell. 2008 Aug;15(2):272–84. https://linkinghub.elsevier.com/retrieve/pii/S1534580708002876

  38. Harris TA, Yamakuchi M, Ferlito M, Mendell JT, Lowenstein CJ. MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1. Proc Natl Acad Sci USA. 2008;105(5):1516–21.

    Article  CAS  Google Scholar 

  39. Chen Y, Gorski DH. Regulation of angiogenesis through a microRNA (miR-130a) that down-regulates antiangiogenic homeobox genes GAX and HOXA5. Blood. 2008;111(3):1217–26.

    Article  CAS  Google Scholar 

  40. García-Donas J, Beuselinck B, Inglada-Pérez L, Graña O, Schöffski P, Wozniak A, et al. Deep sequencing reveals microRNAs predictive of antiangiogenic drug response. JCI Insight. 2019;1(10):1–10.

    Google Scholar 

  41. Incorvaia L, Fanale D, Badalamenti G, Porta C, Olive D, De Luca I, et al. Baseline plasma levels of soluble PD-1, PD-L1, and BTN3A1 predict response to nivolumab treatment in patients with metastatic renal cell carcinoma: a step toward a biomarker for therapeutic decisions. Oncoimmunology. 2020;9(1):1–11. https://doi.org/10.1080/2162402X.2020.1832348.

    Article  Google Scholar 

  42. Cortez MA, Anfossi S, Ramapriyan R, Menon H, Atalar SC, Aliru M, et al. Role of miRNAs in immune responses and immunotherapy in cancer. Genes Chromosomes Cancer . 2019;58(4):244–53. http://www.ncbi.nlm.nih.gov/pubmed/30578699

  43. Incorvaia L, Fanale D, Badalamenti G, Brando C, Bono M, De Luca I, et al. A “lymphocyte microrna signature” as predictive biomarker of immunotherapy response and plasma pd-1/pd-l1 expression levels in patients with metastatic renal cell carcinoma: pointing towards epigenetic reprogramming. Cancers (basel). 2020;12(11):1–17.

    Article  Google Scholar 

  44. Zaman MS, Thamminana S, Shahryari V, Chiyomaru T, Deng G, Saini S, et al. Inhibition of PTEN gene expression by oncogenic miR-23b-3p in renal cancer. PLoS ONE. 2012. https://doi.org/10.1371/journal.pone.0050203.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Sekino Y, Sakamoto N, Sentani K, Oue N, Teishima J, Matsubara A, et al. MiR-130b promotes sunitinib resistance through regulation of PTEN in renal cell carcinoma. Oncol. 2019;97(3):164–72.

    Article  CAS  Google Scholar 

  46. Majid S, Saini S, Dar AA, Hirata H, Shahryari V, Tanaka Y, et al. MicroRNA-205 inhibits Src-mediated oncogenic pathways in renal cancer. Cancer Res. 2011 Apr 1;71(7):2611–21: http://www.ncbi.nlm.nih.gov/pubmed/21330408

  47. Yonezawa Y, Nagashima Y, Sato H, Virgona N, Fukumoto K, Shirai S, et al. Contribution of the Src family of kinases to the appearance of malignant phenotypes in renal cancer cells. Mol Carcinog. 2005;43(4):188–97.

    Article  CAS  Google Scholar 

  48. Sinha S, Dutta S, Datta K, Ghosh AK, Mukhopadhyay D. Von Hippel-Lindau gene product modulates TIS11B expression in renal cell carcinoma: Impact on vascular endothelial growth factor expression in hypoxia. J Biol Chem. 2009;284(47):32610–8.

    Article  CAS  Google Scholar 

  49. Gowrishankar B, Ibragimova I, Zhou Y, Slifker MJ, Devarajan K, Al-Saleem T, et al. MicroRNA expression signatures of stage, grade, and progression in clear cell RCC. Cancer Biol Ther. 2014;15(3):329–41.

    Article  CAS  Google Scholar 

  50. Wang XJ, Yan ZJ, Luo GC, Chen YY, Bai PM. miR-26 suppresses renal cell cancer via down-regulating coronin-3. Vol. 463. Mol Cell Biochem. 2020. https://doi.org/10.1007/s11010-019-03636-2.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Xu C, Zeng H, Fan J, Huang W, Yu X, Li S, et al. A novel nine-microRNA-based model to improve prognosis prediction of renal cell carcinoma. BMC Cancer. 2022;22(1):1–13. https://doi.org/10.1186/s12885-022-09322-9.

    Article  CAS  Google Scholar 

  52. Solinas C, Migliori E, De Silva P, Willard-Gallo K. LAG3: the biological processes that motivate human cancer. Cancers (basel). 2019. https://doi.org/10.1186/s12885-022-09322-9.

    Article  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Medical Oncology, Hospital Universitario Quironsalud, Madrid, Spain

    Jesús Miranda-Poma

  2. Medical Oncology, Hospital Universitario La Paz, Madrid, Spain

    Ana Pertejo-Fernandez, Enrique Espinosa-Arranz & Álvaro Pinto-Marín

  3. Molecular Oncology Lab, Hospital Universitario La Paz-IdiPAZ, Madrid, Spain

    Lucía Trilla-Fuertes, Elena López-Camacho, Andrea Zapater-Moros, Rocío López-Vacas, María Isabel Lumbreras-Herrera, Juan Ángel Fresno-Vara & Angelo Gámez-Pozo

  4. Biomedica Molecular Medicine SL, Madrid, Spain

    Juan Ángel Fresno-Vara & Angelo Gámez-Pozo

  5. CIBERONC, ISCIII, Madrid, Spain

    Juan Ángel Fresno-Vara

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  1. Jesús Miranda-Poma
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  2. Lucía Trilla-Fuertes
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All authors have contributed intellectually to the writing, meet the conditions of authorship and have approved the final version of it. In its name, I declare that the work is original and has not been previously published or is in the process of being reviewed by any other journal. We are waiting for your notice.

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Correspondence to Jesús Miranda-Poma.

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Miranda-Poma, J., Trilla-Fuertes, L., López-Camacho, E. et al. MiRNAs in renal cell carcinoma. Clin Transl Oncol 24, 2055–2063 (2022). https://doi.org/10.1007/s12094-022-02866-z

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