Abstract
MicroRNAs (miRNAs) are a class of small non-coding RNAs involved in gene regulation. Approximately half of miRNAs are located within known genes and called intragenic miRNAs. 408 human intragenic miRNAs and their corresponding host genes were analyzed for genomic organization and functional characterization. Using quantitative real-time PCR, the expression levels of a subset of intragenic miRNAs and their host genes were examined in diverse myeloid leukemia cell lines, and their regulation in response to pharmacological stimuli was also evaluated. Expression of miR-22 strongly correlated with both myeloid leukemia subtypes and the expression of its host gene C17orf91 (p < 0.05). The latter was absent in hematopoietic progenitors but abundant in erythroid and monocytic lineages. These results demonstrated that the expression signatures of miR-22 and C17orf91 are associated with developmental lineages and specific leukemia subtypes.
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Albano F, Anelli L, Zagaria A, Pannunzio A, Liso V, Rocchi M, Specchia G (2009) Downregulated expression of genes mapping on chromosome 9 in chronic myeloid leukemia cases bearing genomic deletions on der(9). Leukemia 23:813–816
Baskerville S, Bartel DP (2005) Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. RNA 11:241–247
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57:289–300
Brach MA, Riedel D, Herrmann F (1990) Induction of monocytic differentiation and modulation of the expression of c-fos, c-fms and c-myc protooncogenes in human monoblasts by cytokines and phorbolester. Virchows Arch B Cell Pathol Incl Mol Pathol 59:54–58
Chen C, Ridzon DA, Broomer AJ et al (2005) Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res 33:179–188
Chen A, Luo M, Yuan G, Yu J, Deng T, Zhang L, Zhou Y, Mitchelson K, Cheng J (2008) Complementary analysis of microRNA and mRNA expression during phorbol 12-myristate 13-acetate (TPA)-induced differentiation of HL-60 cells. Biotechnol Lett 30:2045–2052
Gregory SG, Barlow KF, McLay KE et al (2006) The DNA sequence and biological annotation of human chromosome 1. Nature 441:315–321
Griffiths M, Mason J, Rindl M, Akiki S, McMullan D, Stinton V, Powell H, Curtis A, Bown N, Craddock C (2005) Acquired isodisomy for chromosome 13 is common in AML, and associated with FLT3-itd mutations. Leukemia 19:2355–2358
Griffiths-Jones S (2004) The microRNA Registry. Nucleic Acids Res 32:109–111
He C, Li Z, Chen P, Huang H, Hurst LD, Chen J (2012) Young intragenic miRNAs are less coexpressed with host genes than old ones: implications of miRNA-host gene coevolution. Nucleic Acids Res. doi:10.1093/nar/gkr1312
Hinske LC, Galante PA, Kuo WP, Ohno-Machado L (2010) A potential role for intragenic miRNAs on their hosts’ interactome. BMC Genomics 11:533–546
Jiang Q, Wang Y, Hao Y, Juan L, Teng M, Zhang X, Li M, Wang G, Liu Y (2009) miR2Disease: a manually curated database for microRNA deregulation in human disease. Nucleic Acids Res 37:98–104
Karolchik D, Hinrichs AS, Furey TS, Roskin KM, Sugnet CW, Haussler D, Kent WJ (2004) The UCSC Table Browser data retrieval tool. Nucleic Acids Res 32:493–496
Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854
Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB (2003) Prediction of mammalian microRNA targets. Cell 115:787–798
Lionetti M, Agnelli L, Mosca L, Fabris S, Andronache A, Todoerti K, Ronchetti D, Deliliers GL, Neri A (2009) Integrative high-resolution microarray analysis of human myeloma cell lines reveals deregulated miRNA expression associated with allelic imbalances and gene expression profiles. Genes Chromosomes Cancer 48:521–531
Mao X, Cai T, Olyarchuk JG, Wei L (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21:3787–3793
Nagaraja AK, Creighton CJ, Yu Z et al (2010) A link between mir-100 and FRAP1/mTOR in clear cell ovarian cancer. Mol Endocrinol 24:447–463
Patel JB, Appaiah HN, Burnett RM et al (2011) Control of EVI-1 oncogene expression in metastatic breast cancer cells through microRNA miR-22. Oncogene 30:1290–1301
Pinto LL, Vieira TA, Giugliani R, Schwartz IV (2010) Expression of the disease on female carriers of X-linked lysosomal disorders: a brief review. Orphanet J Rare Dis 5:14–24
Ronchetti D, Lionetti M, Mosca L, Agnelli L, Andronache A, Fabris S, Deliliers GL, Neri A (2008) An integrative genomic approach reveals coordinated expression of intronic miR-335, miR-342, and miR-561 with deregulated host genes in multiple myeloma. BMC Med Genomics 1:37–46
Sawyers CL, Denny CT, Witte ON (1991) Leukemia and the disruption of normal hematopoiesis. Cell 64:337–350
Stirewalt DL, Meshinchi S, Kopecky KJ et al (2008) Identification of genes with abnormal expression changes in acute myeloid leukemia. Genes Chromosomes Cancer 47:8–20
Su AI, Wiltshire T, Batalov S et al (2004) A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 101:6062–6067
Taganov KD, Boldin MP, Chang KJ, Baltimore D (2006) NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci USA 103:12481–12486
Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116–5121
Wang XS, Zhang JW (2008) The microRNAs involved in human myeloid differentiation and myelogenous/myeloblastic leukemia. J Cell Mol Med 12:1445–1455
Wang J, Xiang G, Mitchelson K, Zhou Y (2011) Microarray profiling of monocytic differentiation reveals miRNA–mRNA intrinsic correlation. J Cell Biochem 112:2443–2453
Acknowledgments
We thank Dr. Xizeng Mao for his help with manuscript preparation and Prof. Peng Liu for his assistance with manuscript revisions. We also thank Shuai Liu for his help with quantitative RT-PCR assays and Wengming Zhang for her help with microarray analysis.
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Wang, J., Xiang, G., Zhang, K. et al. Expression signatures of intragenic miRNAs and their corresponding host genes in myeloid leukemia cells. Biotechnol Lett 34, 2007–2015 (2012). https://doi.org/10.1007/s10529-012-1018-0
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DOI: https://doi.org/10.1007/s10529-012-1018-0