Features of miRNA binding with mRNA of candidate genes of breast cancer subtypes

Authors

  • D. Aisina Scientific Research Institute of Biology and Biotechnology Problems, al-Farabi Kazakh National University, the Republic of Kazakhstan, Almaty
  • R. Niyazova Scientific Research Institute of Biology and Biotechnology Problems, al-Farabi Kazakh National University, the Republic of Kazakhstan, Almaty
  • Sh. Atambayeva Scientific Research Institute of Biology and Biotechnology Problems, al-Farabi Kazakh National University, the Republic of Kazakhstan, Almaty
  • E. Imyanitov National Medical Research Center of Oncology named after N.N. Petrov, Russia, Saint-Petersburg
  • A. Ivashchenko Scientific Research Institute of Biology and Biotechnology Problems, al-Farabi Kazakh National University, the Republic of Kazakhstan, Almaty

DOI:

https://doi.org/10.26577/EB-2017-4-1302
        125 74

Keywords:

miRNA, mRNA, subtypes of breast cancer, target genes.

Abstract

To determine associations of miRNA and mRNA of their target genes, binding characteristics of miRNA and mRNA of candidate genes of four subtypes of the breast cancer have been studied. Half of candidate genes of the triple-negative subtype had binding sites for several miRNAs. mRNA of ATM gene had seven binding sites for miR-5095, miR-619-5p, miR-5096, miR-5585-3p, miR-1273a, miR-1273g-3p, all of which bind in the 3'UTR. mRNA of AXL gene, the tyrosine kinase receptor, had binding sites for five miRNAs that are localized in 3'UTR, CDS, and 5'UTR. From five miRNA, miR-1908-3p may the most effective regulated the expression of protooncogene CBL. mRNA of СЕАСАМ5 gene contained binding sites of miR-5095, miR-619-5p, miR-5585-3p with a high degree of complementarity. mRNA of F2RL1, IAPP genes have binding sites predominantly for miR-5095, miR-619-5p, miR-5585-3p, miR-5096. Based on the obtained data, it is necessary to control the expression of candidate genes of the triple-negative subtype with miR-5095, miR-619-5p, miR-5585-3p, miR-5096 and miR-1273a, miR-1273e, miR-1273g-3p. A high free binding energy was detected for pairs of miR-6089 and triple-negative subtype RUNX1 and SFN candidate genes mRNA. mRNA of IL11, MAGEA10 and STMN1 genes had binding sites of miR-619-5p and miR-1273a, miR-1273d, miR-1273e, miR-1273f.

 mRNA of the subtype her2 candidate genes ADAM17, AURKA and BRCA2 strongly bind miR-619-5p. mRNA of BRIP1 gene has sites for miR-1285-5p, miR-5095, miR-619-5p, miR-5585-3p, miR-1273a, miR-1273g-3p. mRNA of CDK6 gene has binding sites for miR-548 family and multiple sites for miR-466. The presence of such binding sites in mRNA of CDK6 gene several times increases the probability of its interaction with these miRNAs. The key candidate gene ERBB3 of the her2 subtype interacts with miR-619-5p with high complementarity. 12 miRNAs can bind to mRNA of MAZ gene, binding sites are located in 5'UTR and CDS. mRNA of candidate genes of the subtype luminal A, B can bind: HMGA2 gene - five miRNA, MAPT gene - six miRNA, SMAD3 gene - four miRNA, TGFB1 gene - six miRNA. mRNA of TGFB1 and SMAD3 genes had four and three effective miR-6089 binding sites, respectively. A special feature of candidate genes of the subtype luminal A, B is the absence in their mRNA binding sites of the unique miRNA family miR-1273 and group miR-5095, miR-619-5p, miR-5585-3p, miR-5096, miR-1285-5p.

References

1 Atambayeva S., Niyazova R., Ivashchenko A., Pyrkova A., Pinsky I., Akimniyazova A., Labeit S. (2017) The Binding Sites of miR-619-5p in the mRNAs of Human and Orthologous Genes, BMC Genomics, vol. 18, no. 1, p. 428. doi: 10.1186/s12864-017-3811-6.
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3 Blakeman V., Williams J.L., Meng Q.J., Streuli C.H. (2016) Circadian clocks and breast cancer, Breast Cancer Research, vol. 18, p. 89. doi: 10.1186/s13058-016-0743-
4 Bonora M., Wieckowsk M.R., Chinopoulos C., Kepp O., Kroemer G., et al. (2015) Molecular mechanisms of cell death: central implication of ATP synthase in mitochondrial permeability transition, Oncogene, vol. 34, no. 12, p. 1608. doi: 10.1038/onc.2014.462.
5 Boudreau A., Tanner K., Wang D., Geyer F.C., Reis-Filho J.S., et al. (2013) 14-3-3σ stabilizes a complex of soluble actin and intermediate filament to enable breast tumor invasion, Proc Natl Acad Sci U S A, vol. 110, no. 41, pp. e3937-44. doi: 10.1073/pnas.1315022110.
6 Chistiakov D.A., Orekhov A.N., Bobryshev Y.V. (2016) MicroRNA regulation of macrophages in human pathologies, J Mol Cell Cardiol, vol. 94, pp. 107-121. doi: 10.1016/j.yjmcc.2016.03.015
7 Couch F.J., Sinilnikova O., Vierkant R.A. (2007) AURKA F31I polymorphism and breast cancer risk in BRCA1 and BRCA2 mutation carriers: a consortium of investigators of modifiers of BRCA1/2 study, Cancer Epidemiol Biomarkers Prev, vol. 16, no. 7, pp. 1416-21.
8 Ergün S., Ulasli M., Igci Y.Z., Igci M., Kırkbes S., et al. (2015) The association of the expression of miR-122-5p and its target ADAM10 with human breast cancer, Mol Biol Rep, vol. 42, no. 2, pp. 497-505. doi: 10.1007/s11033-014-3793-2.
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10 Grabinski N., Möllmann K., Milde-Langosch K., Müller V., Schumacher U., et al. (2014) AKT3 regulates ErbB2, ErbB3 and estrogen receptor α expression and contributes to endocrine therapy resistance of ErbB2(+) breast tumor cells from Balb-neuT mice, Cell Signal, vol. 26, no. 5, pp. 1021-9. doi: 10.1016/j.cellsig.2014.01.018.
11 Hannafon B.N., Trigoso Y.D., Calloway C.L., Zhao Y.D., Lum D.H., et al. (2016) Plasma exosome microRNAs are indicative of breast cancer, Breast Cancer Research, vol. 18, p. 90. doi: 10.1186/s13058-016-0753-x.
12 Hayes D.A., Kunde D.A., Taylor R.L., Pyecroft S.B., Sohal S.S., Snow E.T. (2017) ERBB3: A potential serum biomarker for early detection and therapeutic target for devil facial tumour 1 (DFT1), PLoS One, vol. 12, no. 6, p. e0177919. doi: 10.1371/journal.pone.0177919.
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14 Ivashchenko A., Berillo O., Pyrkova A., Niyazova R., Atambayeva Sh. (2014) The properties of binding sites of miR-619-5p, miR-5095, miR-5096 and miR-5585-3p in the mRNAs of human genes, Biomed Research International, vol. 2014, pp. e8.
15 Ivashchenko A., Berillo O., Pyrkova A., Niyazova R. (2014) Binding Sites of miR-1273 Family on the mRNA of Target Genes , Biomed Research International, vol. 2014, pp. e11.
16 Jo S.J., Park P.G., Cha H.R., Ahn S.G., Kim M.J., et al. (2017) Cellular inhibitor of apoptosis protein 2 promotes the epithelial-mesenchymal transition in triple-negative breast cancer cells through activation of the AKT signaling pathway, Oncotarget, vol. 8, no. 45, pp. 78781-78795. doi: 10.18632/oncotarget.20227.
17 Johnson J., Thijssen B., McDermott U., Garnett M., Wessels L.F., Bernards R. (2016) Targeting the RB-E2F pathway in breast cancer, Oncogene, vol. 35, no. 37, pp. 4829-35. doi: 10.1038/onc.2016.32.
18 Koutras A.K., Fountzilas G., Kalogeras K.T., Starakis I., Iconomou G., Kalofonos H.P. (2010) The upgraded role of HER3 and HER4 receptors in breast cancer, Crit Rev Oncol Hematol., vol. 74, no. 2, pp. 73-8. doi: 10.1016/j.critrevonc.2009.04.011.
19 Krishnan P., Ghosh S., Wang B., Li D., Narasimhan A, et al. (2015) Next generation sequencing profiling identifies miR-574-3p and miR-660-5p as potential novel prognostic markers for breast cancer, BMC Genomics, vol. 16, p. 735. doi: 10.1186/s12864-015-1899-0.
20 Lee S.T., Feng M., Wei Y., Li Z., Qiao Y., et al. (2013) Protein tyrosine phosphatase UBASH3B is overexpressed in triple-negative breast cancer and promotes invasion and metastasis, Proc Natl Acad Sci U S A, vol. 110, no. 27, pp. 11121-6.
21 Li H.Y., Liang J.L., Kuo Y.L., Lee H.H., Calkins M.J., et al. (2017) miR-105/93-3p promotes chemoresistance and circulating miR-105/93-3p acts as a diagnostic biomarker for triple negative breast cancer, Breast Cancer Research, vol. 19, p. 133. doi: 10.1186/s13058-017-0918-2
22 MacFarlane L.A., Murphy P.R. (2010) MicroRNA: Biogenesis, Function and Role in Cancer, Curr Genomics, vol. 11, no. 7, pp. 537-561. doi: 10.2174/138920210793175895
23 Mota J.M., Collier K.A., Barros Costa R.L., Taxter T., Kalyan A., et al. (2017) A comprehensive review of heregulins, HER3, and HER4 as potential therapeutic targets in cancer, Oncotarget, vol. 8, no. 51, pp. 89284-89306. doi: 10.18632/oncotarget.18467.
24 Pan H., He Z., Ling L., Ding Q., Chen L., Zha X., et al. (2014) Reproductive factors and breast cancer risk among BRCA1 or BRCA2 mutation carriers: results from ten studies, Cancer Epidemiol, vol. 38, no. 1, pp. 1-8. doi: 10.1016/j.canep.2013.11.004.
25 Pham D.H., Kim J.S., Kim S.K., Shin D.J., Uong N.T., et al. (2017) Effects of ADAM10 and ADAM17 Inhibitors on Natural Killer Cell Expansion and Antibody-dependent Cellular Cytotoxicity Against Breast Cancer Cells In Vitro, Anticancer Res, vol. 37, no. 10, pp. 5507-5513.
26 Yu Z.H., Lun S.M., He R., Tian H.P., Huang H.J., et al. (2017) Dual function of MAZ mediated by FOXF2 in basal-like breast cancer: Promotion of proliferation and suppression of progression, Cancer Lett, vol. 402, pp. 142-152. doi: 10.1016/j.canlet.2017.05.020.
27 Wang J., Song C., Tang H., Zhang C., Tang J., et al. (2017) miR-629-3p may serve as a novel biomarker and potential therapeutic target for lung metastases of triple-negative breast cancer, Breast Cancer Research, vol. 19, p. 72. doi: 10.1186/s13058-017-0865-y
28 Wang W., Xu X., Tian B., Wang Y., Du L., et al. (2017) The diagnostic value of serum tumor markers CEA, CA19-9, CA125, CA15-3, and TPS in metastatic breast cancer, Clin Chim Acta, vol. 470, pp. 51-55. doi: 10.1016/j.cca.2017.04.023.
29 Wu Y., Zhang Y., Wang M., Li Q., Qu Z., et al. (2013) Downregulation of HER3 by a novel antisense oligonucleotide, EZN-3920, improves the antitumor activity of EGFR and HER2 tyrosine kinase inhibitors in animal models, Mol Cancer Ther., vol. 12, no. 4, pp. 427-37. doi: 10.1158/1535-7163.MCT-12-0838.
30 Zhang X., Li Q., Zhao H., Ma L., Meng T., et al. (2017) Pathological expression of tissue factor confers promising antitumor response to a novel therapeutic antibody SC1 in triple negative breast cancer and pancreatic adenocarcinoma, Oncotarget, vol. 8, no. 35, pp. 59086-59102. doi: 10.18632/oncotarget.19175


References

1 Atambayeva S., Niyazova R., Ivashchenko A., Pyrkova A., Pinsky I., Akimniyazova A., Labeit S. The Binding Sites of miR-619-5p in the mRNAs of Human and Orthologous Genes // BMC Genomics. - 2017. - Vol. 18, No 1. - P. 428. doi: 10.1186/s12864-017-3811-6.
2 Balz L.M., Bartkowiak K., Andreas A., Pantel K., Niggemann B., et al. The interplay of HER2/HER3/PI3K and EGFR/HER2/PLC-γ1 signalling in breast cancer cell migration and dissemination // J Pathol. - 2012. - Vol. 227, No 2. - P. 234-44. doi: 10.1002/path.3991.
3 Blakeman V., Williams J.L., Meng Q.J., Streuli C.H. Circadian clocks and breast cancer // Breast Cancer Research. - 2016. - Vol. 18. - P. 89. doi: 10.1186/s13058-016-0743-
4 Bonora M., Wieckowsk M.R., Chinopoulos C., Kepp O., Kroemer G., et al. Molecular mechanisms of cell death: central implication of ATP synthase in mitochondrial permeability transition // Oncogene. - 2015. - Vol. 34, No 12. - P. 1608. doi: 10.1038/onc.2014.462.
5 Boudreau A., Tanner K., Wang D., Geyer F.C., Reis-Filho J.S., et al. 14-3-3σ stabilizes a complex of soluble actin and intermediate filament to enable breast tumor invasion // Proc Natl Acad Sci U S A. - 2013. - Vol. 110, No 41. - P. e3937-44. doi: 10.1073/pnas.1315022110.
6 Chistiakov D.A., Orekhov A.N., Bobryshev Y.V. MicroRNA regulation of macrophages in human pathologies // J Mol Cell Cardiol. - 2016. - Vol. 94. - P. 107-121. doi: 10.1016/j.yjmcc.2016.03.015
7 Couch F.J., Sinilnikova O., Vierkant R.A. AURKA F31I polymorphism and breast cancer risk in BRCA1 and BRCA2 mutation carriers: a consortium of investigators of modifiers of BRCA1/2 study // Cancer Epidemiol Biomarkers Prev. - 2007. - Vol. 16, No 7. - P. 1416-21.
8 Ergün S., Ulasli M., Igci Y.Z., Igci M., Kırkbes S., et al. The association of the expression of miR-122-5p and its target ADAM10 with human breast cancer // Mol Biol Rep. - 2015 - Vol. 42, No 2. - P. 497-505. doi: 10.1007/s11033-014-3793-2.
9 Golmohammadi R., Namazi M.J., Going J.J., Derakhshan M.H. A single nucleotide polymorphism in codon F31I and V57I of the AURKA gene in invasive ductal breast carcinoma in Middle East // Medicine (Baltimore). - 2017. - Vol. 96, No 37. - P. e7933. doi: 10.1097/MD.0000000000007933.
10 Grabinski N., Möllmann K., Milde-Langosch K., Müller V., Schumacher U., et al. AKT3 regulates ErbB2, ErbB3 and estrogen receptor α expression and contributes to endocrine therapy resistance of ErbB2(+) breast tumor cells from Balb-neuT mice // Cell Signal. - 2014. - Vol. 26, No 5. - P. 1021-9. doi: 10.1016/j.cellsig.2014.01.018.
11 Hannafon B.N., Trigoso Y.D., Calloway C.L., Zhao Y.D., Lum D.H., et al. Plasma exosome microRNAs are indicative of breast cancer // Breast Cancer Research. - 2016. - Vol. 18. - P. 90. doi: 10.1186/s13058-016-0753-x.
12 Hayes D.A., Kunde D.A., Taylor R.L., Pyecroft S.B., Sohal S.S., Snow E.T. ERBB3: A potential serum biomarker for early detection and therapeutic target for devil facial tumour 1 (DFT1) // PLoS One. - 2017 - Vol. 12, No 6. - P. e0177919. doi: 10.1371/journal.pone.0177919.
13 Ivashchenko A., Berillo O., Pyrkova A., Niyazova R., Atambayeva S. MiR-3960 binding sites with mRNA of human genes // Bioinformation. - 2014. - Vol. 10, No 7. - P. 423-427. doi: 10.6026/97320630010423
14 Ivashchenko A., Berillo O., Pyrkova A., Niyazova R., Atambayeva Sh. The properties of binding sites of miR-619-5p, miR-5095, miR-5096 and miR-5585-3p in the mRNAs of human genes // Biomed Research International. - 2014. - Vol. 2014. - P. e8.
15 Ivashchenko A., Berillo O., Pyrkova A., Niyazova R. Binding Sites of miR-1273 Family on the mRNA of Target Genes // Biomed Research International. - 2014. - Vol. 2014, P. e11.
16 Jo S.J., Park P.G., Cha H.R., Ahn S.G., Kim M.J., et al. Cellular inhibitor of apoptosis protein 2 promotes the epithelial-mesenchymal transition in triple-negative breast cancer cells through activation of the AKT signaling pathway // Oncotarget. - 2017. - Vol. 8, No 45. - P. 78781-78795. doi: 10.18632/oncotarget.20227.
17 Johnson J., Thijssen B., McDermott U., Garnett M., Wessels L.F., Bernards R. Targeting the RB-E2F pathway in breast cancer // Oncogene. - 2016. - Vol. 35, No 37. - P. 4829-35. doi: 10.1038/onc.2016.32.
18 Koutras A.K., Fountzilas G., Kalogeras K.T., Starakis I., Iconomou G., Kalofonos H.P. The upgraded role of HER3 and HER4 receptors in breast cancer // Crit Rev Oncol Hematol. - 2010. - Vol. 74, No 2. - P. 73-8. doi: 10.1016/j.critrevonc.2009.04.011.
19 Krishnan P., Ghosh S., Wang B., Li D., Narasimhan A., et al. Next generation sequencing profiling identifies miR-574-3p and miR-660-5p as potential novel prognostic markers for breast cancer // BMC Genomics. - 2015. - Vol. 16. - P. 735. doi: 10.1186/s12864-015-1899-0.
20 Lee S.T., Feng M., Wei Y., Li Z., Qiao Y., et al. Protein tyrosine phosphatase UBASH3B is overexpressed in triple-negative breast cancer and promotes invasion and metastasis // Proc Natl Acad Sci U S A. - 2013. - Vol. 110, No 27. - P. 11121-6.
21 Li H.Y., Liang J.L., Kuo Y.L., Lee H.H., Calkins M.J., et al. miR-105/93-3p promotes chemoresistance and circulating miR-105/93-3p acts as a diagnostic biomarker for triple negative breast cancer // Breast Cancer Research. - 2017. - Vol. 19. - P. 133. doi: 10.1186/s13058-017-0918-2
22 MacFarlane L.A., Murphy P.R. MicroRNA: Biogenesis, Function and Role in Cancer // Curr Genomics. 2010. - Vol. 11, No 7. - P. 537-561. doi: 10.2174/138920210793175895
23 Mota J.M., Collier K.A., Barros Costa R.L., Taxter T., Kalyan A., et al. A comprehensive review of heregulins, HER3, and HER4 as potential therapeutic targets in cancer // Oncotarget. - 2017. - Vol. 8, No 51. - P. 89284-89306. doi: 10.18632/oncotarget.18467.
24 Pan H., He Z., Ling L., Ding Q., Chen L., Zha X., et al. Reproductive factors and breast cancer risk among BRCA1 or BRCA2 mutation carriers: results from ten studies // Cancer Epidemiol. - 2014. - Vol. 38, No 1. - P. 1-8. doi: 10.1016/j.canep.2013.11.004.
25 Pham D.H., Kim J.S., Kim S.K., Shin D.J., Uong N.T., et al. Effects of ADAM10 and ADAM17 Inhibitors on Natural Killer Cell Expansion and Antibody-dependent Cellular Cytotoxicity Against Breast Cancer Cells In Vitro // Anticancer Res. - 2017. - Vol. 37, No 10. - P. 5507-5513.
26 Yu Z.H., Lun S.M., He R., Tian H.P., Huang H.J., et al. Dual function of MAZ mediated by FOXF2 in basal-like breast cancer: Promotion of proliferation and suppression of progression // Cancer Lett. - 2017. - Vol. 402. - P. 142-152. doi: 10.1016/j.canlet.2017.05.020.
27 Wang J., Song C., Tang H., Zhang C., Tang J., et al. miR-629-3p may serve as a novel biomarker and potential therapeutic target for lung metastases of triple-negative breast cancer // Breast Cancer Research. - 2017. - Vol. 19. - P. 72. doi: 10.1186/s13058-017-0865-y
28 Wang W., Xu X., Tian B., Wang Y., Du L., et al. The diagnostic value of serum tumor markers CEA, CA19-9, CA125, CA15-3, and TPS in metastatic breast cancer // Clin Chim Acta. - 2017. - Vol. 470. - P. 51-55. doi: 10.1016/j.cca.2017.04.023.
29 Wu Y., Zhang Y., Wang M., Li Q., Qu Z., et al. Downregulation of HER3 by a novel antisense oligonucleotide, EZN-3920, improves the antitumor activity of EGFR and HER2 tyrosine kinase inhibitors in animal models // Mol Cancer Ther. - 2013. - Vol. 12, No 4. - P. 427-37. doi: 10.1158/1535-7163.MCT-12-0838.
30 Zhang X., Li Q., Zhao H., Ma L., Meng T., et al. Pathological expression of tissue factor confers promising antitumor response to a novel therapeutic antibody SC1 in triple negative breast cancer and pancreatic adenocarcinoma // Oncotarget. - 2017. - Vol. 8, No 35. - P. 59086-59102. doi: 10.18632/oncotarget.19175.

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Aisina, D., Niyazova, R., Atambayeva, S., Imyanitov, E., & Ivashchenko, A. (2018). Features of miRNA binding with mRNA of candidate genes of breast cancer subtypes. Experimental Biology, 73(4), 52–66. https://doi.org/10.26577/EB-2017-4-1302

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МOLECULAR BIOLOGY AND GENETICS