DOI QR코드

DOI QR Code

Hsa-miR-422a Originated from Short Interspersed Nuclear Element Increases ARID5B Expression by Collaborating with NF-E2

  • Kim, Woo Ryung (Department of Integrated Biological Science, Pusan National University) ;
  • Park, Eun Gyung (Department of Integrated Biological Science, Pusan National University) ;
  • Lee, Hee-Eun (National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Park, Sang-Je (National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Huh, Jae-Won (National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Kim, Jeong Nam (Department of Microbiology, College of Natural Sciences, Pusan National University) ;
  • Kim, Heui-Soo (Institute of Systems Biology, Pusan National University)
  • 투고 : 2021.06.17
  • 심사 : 2021.12.27
  • 발행 : 2022.07.31

초록

MicroRNAs (miRNAs) are a class of small non-coding RNAs that regulate the expression of target messenger RNA (mRNA) complementary to the 3' untranslated region (UTR) at the post-transcriptional level. Hsa-miR-422a, which is commonly known as miRNA derived from transposable element (MDTE), was derived from short interspersed nuclear element (SINE). Through expression analysis, hsa-miR-422a was found to be highly expressed in both the small intestine and liver of crab-eating monkey. AT-Rich Interaction Domain 5 B (ARID5B) was selected as the target gene of hsa-miR-422a, which has two binding sites in both the exon and 3'UTR of ARID5B. To identify the interaction between hsa-miR-422a and ARID5B, a dual luciferase assay was conducted in HepG2 cell line. The luciferase activity of cells treated with the hsa-miR-422a mimic was upregulated and inversely downregulated when both the hsa-miR-422a mimic and inhibitor were administered. Nuclear factor erythroid-2 (NF-E2) was selected as the core transcription factor (TF) via feed forward loop analysis. The luciferase expression was downregulated when both the hsa-miR-422a mimic and siRNA of NF-E2 were treated, compared to the treatment of the hsa-miR-422a mimic alone. The present study suggests that hsa-miR-422a derived from SINE could bind to the exon region as well as the 3'UTR of ARID5B. Additionally, hsa-miR-422a was found to share binding sites in ARID5B with several TFs, including NF-E2. The hsa-miR-422a might thus interact with TF to regulate the expression of ARID5B, as demonstrated experimentally. Altogether, hsa-miR-422a acts as a super enhancer miRNA of ARID5B by collaborating with TF and NF-E2.

키워드

과제정보

This research was supported by the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2018R1D1A1B07049460).

참고문헌

  1. Ahl, V., Keller, H., Schmidt, S., and Weichenrieder, O. (2015). Retrotransposition and crystal structure of an Alu RNP in the ribosome-stalling conformation. Mol. Cell 60, 715-727. https://doi.org/10.1016/j.molcel.2015.10.003
  2. Ambros, V. (2004). The functions of animal microRNAs. Nature 431, 350-355. https://doi.org/10.1038/nature02871
  3. Andrews, N.C., Erdjument-Bromage, H., Davidson, M.B., Tempst, P., and Orkin, S.H. (1993). Erythroid transcription factor NF-E2 is a haematopoietic-specific basic-leucine zipper protein. Nature 362, 722-728. https://doi.org/10.1038/362722a0
  4. Arora, S., Rana, R., Chhabra, A., Jaiswal, A., and Rani, V. (2013). miRNA-transcription factor interactions: a combinatorial regulation of gene expression. Mol. Genet. Genomics 288, 77-87. https://doi.org/10.1007/s00438-013-0734-z
  5. Bailey, J.A., Liu, G., and Eichler, E.E. (2003). An Alu transposition model for the origin and expansion of human segmental duplications. Am. J. Hum. Genet. 73, 823-834. https://doi.org/10.1086/378594
  6. Baniwal, S.K., Chan, K.Y., Scharf, K.D., and Nover, L. (2007). Role of heat stress transcription factor HsfA5 as specific repressor of HsfA4. J. Biol. Chem. 282, 3605-3613. https://doi.org/10.1074/jbc.M609545200
  7. Barros-Viegas, A.T., Carmona, V., Ferreiro, E., Guedes, J., Cardoso, A.M., Cunha, P., de Almeida, L.P., de Oliveira, C.R., de Magalhaes, J.P., Peca, J., et al. (2020). miRNA-31 improves cognition and abolishes amyloid-β pathology by targeting APP and BACE1 in an animal model of Alzheimer's disease. Mol. Ther. Nucleic Acids 19, 1219-1236. https://doi.org/10.1016/j.omtn.2020.01.010
  8. Baskerville, S. and Bartel, D.P. (2005). Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 11, 241-247. https://doi.org/10.1261/rna.7240905
  9. Batlle, E., Sancho, E., Franci, C., Dominguez, D., Monfar, M., Baulida, J., and De Herreros, A.G. (2000). The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2, 84-89. https://doi.org/10.1038/35000034
  10. Becker, K.G., Swergold, G., Ozato, K., and Thayer, R.E. (1993). Binding of the ubiquitous nuclear transcription factor YY1 to a cis regulatory sequence in the human LINE-1 transposable element. Hum. Mol. Genet. 2, 1697-1702. https://doi.org/10.1093/hmg/2.10.1697
  11. Behnke, M., Reimers, M., and Fisher, R. (2012). The expression of embryonic liver development genes in hepatitis C induced cirrhosis and hepatocellular carcinoma. Cancers (Basel) 4, 945-968. https://doi.org/10.3390/cancers4030945
  12. Bhattacharyya, S.N., Habermacher, R., Martine, U., Closs, E.I., and Filipowicz, W. (2006). Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125, 1111-1124. https://doi.org/10.1016/j.cell.2006.04.031
  13. Bonnin, N., Armandy, E., Carras, J., Ferrandon, S., Battiston-Montagne, P., Aubry, M., Guihard, S., Meyronet, D., Foy, J.P., Saintigny, P., et al. (2016). MiR-422a promotes loco-regional recurrence by targeting NT5E/CD73 in head and neck squamous cell carcinoma. Oncotarget 7, 44023-44038. https://doi.org/10.18632/oncotarget.9829
  14. Borges, F., Parent, J.S., van Ex, F., Wolff, P., Martinez, G., Kohler, C., and Martienssen, R.A. (2018). Transposon-derived small RNAs triggered by miR845 mediate genome dosage response in Arabidopsis. Nat. Genet. 50, 186-192. https://doi.org/10.1038/s41588-017-0032-5
  15. Bourque, G., Burns, K.H., Gehring, M., Gorbunova, V., Seluanov, A., Hammell, M., Imbeault, M., Izsvak, Z., Levin, H.L., Macfarlan, T.S., et al. (2018). Ten things you should know about transposable elements. Genome Biol. 19, 199. https://doi.org/10.1186/s13059-018-1577-z
  16. Brosh, R., Shalgi, R., Liran, A., Landan, G., Korotayev, K., Nguyen, G.H., Enerly, E., Johnsen, H., Buganim, Y., Solomon, H., et al. (2008). p53-repressed miRNAs are involved with E2F in a feed-forward loop promoting proliferation. Mol. Syst. Biol. 4, 229. https://doi.org/10.1038/msb.2008.65
  17. Burns, K.H. (2017). Transposable elements in cancer. Nat. Rev. Cancer 17, 415-424. https://doi.org/10.1038/nrc.2017.35
  18. Chen, W., Zhao, W., Yang, A., Xu, A., Wang, H., Cong, M., Liu, T., Wang, P., and You, H. (2017). Integrated analysis of microRNA and gene expression profiles reveals a functional regulatory module associated with liver fibrosis. Gene 636, 87-95. https://doi.org/10.1016/j.gene.2017.09.027
  19. Cheng, A.M., Byrom, M.W., Shelton, J., and Ford, L.P. (2005). Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res. 33, 1290-1297. https://doi.org/10.1093/nar/gki200
  20. Clayton, E.A., Wang, L., Rishishwar, L., Wang, J., McDonald, J.F., and Jordan, I.K. (2016). Patterns of transposable element expression and insertion in cancer. Front. Mol. Biosci. 3, 76.
  21. Coste, A.T., Karababa, M., Ischer, F., Bille, J., and Sanglard, D. (2004). TAC1, transcriptional activator of CDR genes, is a new transcription factor involved in the regulation of Candida albicans ABC transporters CDR1 and CDR2. Eukaryot. Cell 3, 1639-1652. https://doi.org/10.1128/EC.3.6.1639-1652.2004
  22. Dalal, S.R. and Kwon, J.H. (2010). The role of microRNA in inflammatory bowel disease. Gastroenterol. Hepatol. (N.Y.) 6, 714-722.
  23. Dewannieux, M., Esnault, C., and Heidmann, T. (2003). LINE-mediated retrotransposition of marked Alu sequences. Nat. Genet. 35, 41-48. https://doi.org/10.1038/ng1223
  24. Djuranovic, S., Nahvi, A., and Green, R. (2012). miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science 336, 237-240. https://doi.org/10.1126/science.1215691
  25. Duellman, T., Warren, C., and Yang, J. (2014). Single nucleotide polymorphism-specific regulation of matrix metalloproteinase-9 by multiple miRNAs targeting the coding exon. Nucleic Acids Res. 42, 5518-5531. https://doi.org/10.1093/nar/gku197
  26. Fang, L., Kong, D., and Xu, W. (2018). MicroRNA-625-3p promotes the proliferation, migration and invasion of thyroid cancer cells by up-regulating astrocyte elevated gene 1. Biomed. Pharmacother. 102, 203-211. https://doi.org/10.1016/j.biopha.2018.03.043
  27. Feschotte, C. and Pritham, E.J. (2007). DNA transposons and the evolution of eukaryotic genomes. Annu. Rev. Genet. 41, 331-368. https://doi.org/10.1146/annurev.genet.40.110405.090448
  28. Fischer, M., Steiner, L., and Engeland, K. (2014). The transcription factor p53: not a repressor, solely an activator. Cell Cycle 13, 3037-3058. https://doi.org/10.4161/15384101.2014.949083
  29. Forman, J.J. and Coller, H.A. (2010). The code within the code: microRNAs target coding regions. Cell Cycle 9, 1533-1541. https://doi.org/10.4161/cc.9.8.11202
  30. Fujimoto, A., Totoki, Y., Abe, T., Boroevich, K.A., Hosoda, F., Nguyen, H.H., Aoki, M., Hosono, N., Kubo, M., Miya, F., et al. (2012). Whole-genome sequencing of liver cancers identifies etiological influences on mutation patterns and recurrent mutations in chromatin regulators. Nat. Genet. 44, 760-764. https://doi.org/10.1038/ng.2291
  31. Goerttler, P.S., Kreutz, C., Donauer, J., Faller, D., Maiwald, T., Marz, E., Rumberger, B., Sparna, T., Schmitt-Graff, A., Wilpert, J., et al. (2005). Gene expression profiling in polycythaemia vera: overexpression of transcription factor NF-E2. Br. J. Haematol. 129, 138-150. https://doi.org/10.1111/j.1365-2141.2005.05416.x
  32. Gregory, P., Marsh, W.H., Cunningham, J.T., and Lee, W.M. (1983). Hepatomegaly and ascites in an elderly woman with polycythemia vera. J. Clin. Gastroenterol. 5, 367-376. https://doi.org/10.1097/00004836-198308000-00017
  33. Guichard, C., Amaddeo, G., Imbeaud, S., Ladeiro, Y., Pelletier, L., Maad, I.B., Calderaro, J., Bioulac-Sage, P., Letexier, M., Degos, F., et al. (2012). Integrated analysis of somatic mutations and focal copy-number changes identifies key genes and pathways in hepatocellular carcinoma. Nat. Genet. 44, 694-698. https://doi.org/10.1038/ng.2256
  34. Han, X., Luan, T., Sun, Y., Yan, W., Wang, D., and Zeng, X. (2020). MicroRNA 449c mediates the generation of monocytic myeloid-derived suppressor cells by targeting STAT6. Mol. Cells 43, 793-803. https://doi.org/10.14348/molcells.2020.2307
  35. He, L., Yuan, H., Liang, J., Hong, J., and Qu, C. (2020). Expression of hepatic stellate cell activation-related genes in HBV-, HCV-, and nonalcoholic fatty liver disease-associated fibrosis. PLoS One 15, e0233702. https://doi.org/10.1371/journal.pone.0233702
  36. He, Z., Li, Z., Zhang, X., Yin, K., Wang, W., Xu, Z., Li, B., Zhang, L., Xu, J., Sun, G., et al. (2018). MiR-422a regulates cellular metabolism and malignancy by targeting pyruvate dehydrogenase kinase 2 in gastric cancer. Cell Death Dis. 9, 505. https://doi.org/10.1038/s41419-018-0564-3
  37. Hirsch, C.D. and Springer, N.M. (2017). Transposable element influences on gene expression in plants. Biochim. Biophys. Acta Gene Regul. Mech. 1860, 157-165. https://doi.org/10.1016/j.bbagrm.2016.05.010
  38. Hu, S., Cao, M., He, Y., Zhang, G., Liu, Y., Du, Y., Yang, C., and Gao, F. (2020). CD44v6 targeted by miR-193b-5p in the coding region modulates the migration and invasion of breast cancer cells. J. Cancer 11, 260-271. https://doi.org/10.7150/jca.35067
  39. Hung, H.L., Kim, A.Y., Hong, W., Rakowski, C., and Blobel, G.A. (2001). Stimulation of NF-E2 DNA binding by CREB-binding protein (CBP)-mediated acetylation. J. Biol. Chem. 276, 10715-10721. https://doi.org/10.1074/jbc.M007846200
  40. Hwang, H. and Mendell, J. (2006). MicroRNAs in cell proliferation, cell death, and tumorigenesis. Br. J. Cancer 94, 776-780. https://doi.org/10.1038/sj.bjc.6603023
  41. Jelkmann, W. (2001). The role of the liver in the production of thrombopoietin compared with erythropoietin. Eur. J. Gastroenterol. Hepatol. 13, 791-801. https://doi.org/10.1097/00042737-200107000-00006
  42. Jiao, A.L. and Slack, F.J. (2014). RNA-mediated gene activation. Epigenetics 9, 27-36. https://doi.org/10.4161/epi.26942
  43. Jones-Rhoades, M.W. and Bartel, D.P. (2004). Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol. Cell 14, 787-799. https://doi.org/10.1016/j.molcel.2004.05.027
  44. Jutzi, J.S., Bogeska, R., Nikoloski, G., Schmid, C.A., Seeger, T.S., Stegelmann, F., Schwemmers, S., Grunder, A., Peeken, J.C., Gothwal, M., et al. (2013). MPN patients harbor recurrent truncating mutations in transcription factor NF-E2. J. Exp. Med. 210, 1003-1019. https://doi.org/10.1084/jem.20120521
  45. Kacena, M.A., Shivdasani, R.A., Wilson, K., Xi, Y., Troiano, N., Nazarian, A., Gundberg, C.M., Bouxsein, M.L., Lorenzo, J.A., and Horowitz, M.C. (2004). Megakaryocyte-osteoblast interaction revealed in mice deficient in transcription factors GATA-1 and NF-E2. J. Bone Miner. Res. 19, 652-660. https://doi.org/10.1359/jbmr.0301254
  46. Kahraman, M., Roske, A., Laufer, T., Fehlmann, T., Backes, C., Kern, F., Kohlhaas, J., Schrors, H., Saiz, A., Zabler, C., et al. (2018). MicroRNA in diagnosis and therapy monitoring of early-stage triple-negative breast cancer. Sci. Rep. 8, 11584. https://doi.org/10.1038/s41598-018-29917-2
  47. Kumar, A., Wong, A.K.L., Tizard, M.L., Moore, R.J., and Lefevre, C. (2012). miRNA_Targets: a database for miRNA target predictions in coding and non-coding regions of mRNAs. Genomics 100, 352-356. https://doi.org/10.1016/j.ygeno.2012.08.006
  48. Latorre, J., Moreno-Navarrete, J., Mercader, J., Sabater, M., Rovira, O., Girones, J., Ricart, W., Fernandez-Real, J., and Ortega, F. (2017). Decreased lipid metabolism but increased FA biosynthesis are coupled with changes in liver microRNAs in obese subjects with NAFLD. Int. J. Obes. (Lond.) 41, 620-630. https://doi.org/10.1038/ijo.2017.21
  49. Lee, H.E., Huh, J.W., and Kim, H.S. (2020a). Bioinformatics analysis of evolution and human disease related transposable element-derived microRNAs. Life (Basel) 10, 95.
  50. Lee, H.E., Jo, A., Im, J., Cha, H.J., Kim, W.J., Kim, H.H., Kim, D.S., Kim, W., Yang, T.J., and Kim, H.S. (2019). Characterization of the long terminal repeat of the endogenous retrovirus-derived microRNAs in the olive flounder. Sci. Rep. 9, 14007. https://doi.org/10.1038/s41598-019-50492-7
  51. Lee, H.E., Park, S.J., Huh, J.W., Imai, H., and Kim, H.S. (2020b). Enhancer function of microRNA-3681 derived from long terminal repeats represses the activity of variable number tandem repeats in the 3'UTR of SHISA7. Mol. Cells 43, 607-618. https://doi.org/10.14348/molcells.2020.0058
  52. Lee, H.E., Park, S.J., Huh, J.W., Imai, H., and Kim, H.S. (2021). The enhancer activity of long interspersed nuclear element derived microRNA 625 induced by NF-κB. Sci. Rep. 11, 3139. https://doi.org/10.1038/s41598-021-82735-x
  53. Liang, H., Wang, R., Jin, Y., Li, J., and Zhang, S. (2016). MiR-422a acts as a tumor suppressor in glioblastoma by targeting PIK3CA. Am. J. Cancer Res. 6, 1695-1707.
  54. Lin, S.L., Kim, H., and Ying, S.Y. (2008). Intron-mediated RNA interference and microRNA (miRNA). Front. Biosci. 13, 2216-2230. https://doi.org/10.2741/2836
  55. Loginov, V., Rykov, S., Fridman, M., and Braga, E. (2015). Methylation of miRNA genes and oncogenesis. Biochemistry (Mosc.) 80, 145-162. https://doi.org/10.1134/s0006297915020029
  56. Lytle, J.R., Yario, T.A., and Steitz, J.A. (2007). Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5' UTR as in the 3' UTR. Proc. Natl. Acad. Sci. U. S. A. 104, 9667-9672. https://doi.org/10.1073/pnas.0703820104
  57. Majid, S., Dar, A.A., Saini, S., Yamamura, S., Hirata, H., Tanaka, Y., Deng, G., and Dahiya, R. (2010). MicroRNA-205-directed transcriptional activation of tumor suppressor genes in prostate cancer. Cancer 116, 5637-5649. https://doi.org/10.1002/cncr.25488
  58. Markljung, E., Jiang, L., Jaffe, J.D., Mikkelsen, T.S., Wallerman, O., Larhammar, M., Zhang, X., Wang, L., Saenz-Vash, V., Gnirke, A., et al. (2009). ZBED6, a novel transcription factor derived from a domesticated DNA transposon regulates IGF2 expression and muscle growth. PLoS Biol. 7, e1000256. https://doi.org/10.1371/journal.pbio.1000256
  59. Matsui, M., Chu, Y., Zhang, H., Gagnon, K.T., Shaikh, S., Kuchimanchi, S., Manoharan, M., Corey, D.R., and Janowski, B.A. (2013). Promoter RNA links transcriptional regulation of inflammatory pathway genes. Nucleic Acids Res. 41, 10086-10109. https://doi.org/10.1093/nar/gkt777
  60. Molina-Pinelo, S., Gutierrez, G., Pastor, M.D., Hergueta, M., Moreno-Bueno, G., Garcia-Carbonero, R., Nogal, A., Suarez, R., Salinas, A., Pozo-Rodriguez, F., et al. (2014). MicroRNA-dependent regulation of transcription in non-small cell lung cancer. PLoS One 9, e90524. https://doi.org/10.1371/journal.pone.0090524
  61. Neilson, J.R., Zheng, G.X., Burge, C.B., and Sharp, P.A. (2007). Dynamic regulation of miRNA expression in ordered stages of cellular development. Genes Dev. 21, 578-589. https://doi.org/10.1101/gad.1522907
  62. Ohnishi, Y., Totoki, Y., Toyoda, A., Watanabe, T., Yamamoto, Y., Tokunaga, K., Sakaki, Y., Sasaki, H., and Hohjoh, H. (2012). Active role of small non-coding RNAs derived from SINE/B1 retrotransposon during early mouse development. Mol. Biol. Rep. 39, 903-909. https://doi.org/10.1007/s11033-011-0815-1
  63. Ohta, Y., Shichinohe, H., and Nagashima, K. (2002). Spinal cord compression due to extramedullary hematopoiesis associated with polycythemia vera-case report-. Neurol. Med. Chir. (Tokyo) 42, 40-43. https://doi.org/10.2176/nmc.42.40
  64. Orom, U.A., Nielsen, F.C., and Lund, A.H. (2008). MicroRNA-10a binds the 5' UTR of ribosomal protein mRNAs and enhances their translation. Mol. Cell 30, 460-471. https://doi.org/10.1016/j.molcel.2008.05.001
  65. Payer, L.M. and Burns, K.H. (2019). Transposable elements in human genetic disease. Nat. Rev. Genet. 20, 760-772. https://doi.org/10.1038/s41576-019-0165-8
  66. Peng, C., Wang, M., Shen, Y., Feng, H., and Li, A. (2013). Reconstruction and analysis of transcription factor-miRNA co-regulatory feed-forward loops in human cancers using filter-wrapper feature selection. PLoS One 8, e78197. https://doi.org/10.1371/journal.pone.0078197
  67. Piriyapongsa, J. and Jordan, I.K. (2007). A family of human microRNA genes from miniature inverted-repeat transposable elements. PLoS One 2, e203. https://doi.org/10.1371/journal.pone.0000203
  68. Piriyapongsa, J., Marino-Ramirez, L., and Jordan, I.K. (2007). Origin and evolution of human microRNAs from transposable elements. Genetics 176, 1323-1337. https://doi.org/10.1534/genetics.107.072553
  69. Sawado, T., Igarashi, K., and Groudine, M. (2001). Activation of β-major globin gene transcription is associated with recruitment of NF-E2 to the β-globin LCR and gene promoter. Proc. Natl. Acad. Sci. U. S. A. 98, 10226-10231. https://doi.org/10.1073/pnas.181344198
  70. Shivdasani, R.A. (2006). MicroRNAs: regulators of gene expression and cell differentiation. Blood 108, 3646-3653. https://doi.org/10.1182/blood.v108.11.3646.3646
  71. Song, K.H., Li, T., Owsley, E., and Chiang, J.Y. (2010). A putative role of micro RNA in regulation of cholesterol 7α-hydroxylase expression in human hepatocytes. J. Lipid Res. 51, 2223-2233. https://doi.org/10.1194/jlr.M004531
  72. Spivak, J.L. (2010). Narrative review: thrombocytosis, polycythemia vera, and JAK2 mutations: the phenotypic mimicry of chronic myeloproliferation. Ann. Intern. Med. 152, 300-306. https://doi.org/10.7326/0003-4819-152-5-201003020-00008
  73. Sun, W., Samimi, H., Gamez, M., Zare, H., and Frost, B. (2018). Pathogenic tau-induced piRNA depletion promotes neuronal death through transposable element dysregulation in neurodegenerative tauopathies. Nat. Neurosci. 21, 1038-1048. https://doi.org/10.1038/s41593-018-0194-1
  74. Suzuki, H.I., Young, R.A., and Sharp, P.A. (2017). Super-enhancer-mediated RNA processing revealed by integrative microRNA network analysis. Cell 168, 1000-1014.e15.
  75. Tsai, N.P., Lin, Y.L., and Wei, L.N. (2009). MicroRNA mir-346 targets the 5'-untranslated region of receptor-interacting protein 140 (RIP140) mRNA and up-regulates its protein expression. Biochem. J. 424, 411-418. https://doi.org/10.1042/BJ20090915
  76. Turner, M., Jiao, A., and Slack, F.J. (2014). Autoregulation of lin-4 microRNA transcription by RNA activation (RNAa) in C. elegans. Cell Cycle 13, 772-781. https://doi.org/10.4161/cc.27679
  77. Ullu, E. and Tschudi, C. (1984). Alu sequences are processed 7SL RNA genes. Nature 312, 171-172. https://doi.org/10.1038/312171a0
  78. Wang, H., Tang, C., Na, M., Ma, W., Jiang, Z., Gu, Y., Ma, G., Ge, H., Shen, H., and Lin, Z. (2017). miR-422a inhibits glioma proliferation and invasion by targeting IGF1 and IGF1R. Oncol. Res. 25, 187-194. https://doi.org/10.3727/096504016X14732772150389
  79. Wang, R., Zhang, S., Chen, X., Li, N., Li, J., Jia, R., Pan, Y., and Liang, H. (2018). CircNT5E acts as a sponge of miR-422a to promote glioblastoma tumorigenesis. Cancer Res. 78, 4812-4825. https://doi.org/10.1158/0008-5472.CAN-18-0532
  80. Wei, F., Yang, L., Jiang, D., Pan, M., Tang, G., Huang, M., and Zhang, J. (2020). Long noncoding RNA DUXAP8 contributes to the progression of hepatocellular carcinoma via regulating miR-422a/PDK2 axis. Cancer Med. 9, 2480-2490. https://doi.org/10.1002/cam4.2861
  81. Wei, W.T., Nian, X.X., Wang, S.Y., Jiao, H.L., Wang, Y.X., Xiao, Z.Y., Yang, R.W., Ding, Y.Q., Ye, Y.P., and Liao, W.T. (2017). miR-422a inhibits cell proliferation in colorectal cancer by targeting AKT1 and MAPK1. Cancer Cell Int. 17, 91. https://doi.org/10.1186/s12935-017-0461-3
  82. Wienholds, E. and Plasterk, R.H. (2005). MicroRNA function in animal development. FEBS Lett. 579, 5911-5922. https://doi.org/10.1016/j.febslet.2005.07.070
  83. Wu, L., Hu, B., Zhao, B., Liu, Y., Yang, Y., Zhang, L., and Chen, J. (2017). Circulating microRNA-422a is associated with lymphatic metastasis in lung cancer. Oncotarget 8, 42173-42188. https://doi.org/10.18632/oncotarget.15025
  84. Wu, Q., Qin, H., Zhao, Q., and He, X.X. (2015). Emerging role of transcription factor-microRNA-target gene feed-forward loops in cancer. Biomed. Rep. 3, 611-616. https://doi.org/10.3892/br.2015.477
  85. Xiao, M., Li, J., Li, W., Wang, Y., Wu, F., Xi, Y., Zhang, L., Ding, C., Luo, H., Li, Y., et al. (2017). MicroRNAs activate gene transcription epigenetically as an enhancer trigger. RNA Biol. 14, 1326-1334. https://doi.org/10.1080/15476286.2015.1112487
  86. Yang, W., Wang, J., Chen, Z., Chen, J., Meng, Y., Chen, L., Chang, Y., Geng, B., Sun, L., Dou, L., et al. (2017). NFE2 induces miR-423-5p to promote gluconeogenesis and hyperglycemia by repressing the hepatic FAM3A-ATP-Akt pathway. Diabetes 66, 1819-1832. https://doi.org/10.2337/db16-1172
  87. Yuan, Z., Sun, X., Jiang, D., Ding, Y., Lu, Z., Gong, L., Liu, H., and Xie, J. (2010). Origin and evolution of a placental-specific microRNA family in the human genome. BMC Evol. Biol. 10, 346. https://doi.org/10.1186/1471-2148-10-346
  88. Zhang, H., He, Q.Y., Wang, G.C., Tong, D.K., Wang, R.K., Ding, W.B., Li, C., Wei, Q., Ding, C., Liu, P.Z., et al. (2018a). miR-422a inhibits osteosarcoma proliferation by targeting BCL2L2 and KRAS. Biosci. Rep. 38, BSR20170339. https://doi.org/10.1042/BSR20170339
  89. Zhang, H.M., Kuang, S., Xiong, X., Gao, T., Liu, C., and Guo, A.Y. (2015a). Transcription factor and microRNA co-regulatory loops: important regulatory motifs in biological processes and diseases. Brief. Bioinform. 16, 45-58. https://doi.org/10.1093/bib/bbt085
  90. Zhang, J., Yang, Y., Yang, T., Yuan, S., Wang, R., Pan, Z., Yang, Y., Huang, G., Gu, F., Jiang, B., et al. (2015b). Double-negative feedback loop between microRNA-422a and forkhead box (FOX) G1/Q1/E1 regulates hepatocellular carcinoma tumor growth and metastasis. Hepatology 61, 561-573. https://doi.org/10.1002/hep.27491
  91. Zhang, Y., Wan, J., Liu, S., Hua, T., and Sun, Q. (2018b). Exercise induced improvements in insulin sensitivity are concurrent with reduced NFE2/miR-432-5p and increased FAM3A. Life Sci. 207, 23-29. https://doi.org/10.1016/j.lfs.2018.05.040
  92. Zhou, X., Duan, X., Qian, J., and Li, F. (2009). Abundant conserved microRNA target sites in the 5'-untranslated region and coding sequence. Genetica 137, 159-164. https://doi.org/10.1007/s10709-009-9378-7
  93. Zhou, Y., Ferguson, J., Chang, J.T., and Kluger, Y. (2007). Inter-and intra-combinatorial regulation by transcription factors and microRNAs. BMC Genomics 8, 396. https://doi.org/10.1186/1471-2164-8-396
  94. Zou, Y., Chen, Y., Yao, S., Deng, G., Liu, D., Yuan, X., Liu, S., Rao, J., Xiong, H., Yuan, X., et al. (2018). MiR-422a weakened breast cancer stem cells properties by targeting PLP2. Cancer Biol. Ther. 19, 436-444. https://doi.org/10.1080/15384047.2018.1433497