Skip to main content
Download PDF
  • Mini Review
  • Published:

Regulation of lncRNA expression

Cellular & Molecular Biology Letters volume 19, pages 561–575 (2014)Cite this article

Abstract

Long non-coding RNAs (lncRNAs) are series of transcripts with important biological functions. Various diseases have been associated with aberrant expression of lncRNAs and the related dysregulation of mRNAs. In this review, we highlight the mechanisms of dynamic lncRNA expression. The chromatin state contributes to the low and specific expression of lncRNAs. The transcription of non-coding RNA genes is regulated by many core transcription factors applied to protein-coding genes. However, specific DNA sequences may allow their unsynchronized transcription with their location-associated mRNAs. Additionally, there are multiple mechanisms involved in the post-transcriptional regulation of lncRNAs. Among these, microRNAs might have indispensible regulatory effects on lncRNAs, based on recent discoveries.

Abbreviations

ADAR:

adenosine deaminase

Ago2:

argonaute 2

AP-1:

activating protein-1

CDR1:

cerebellar degeneration-related protein 1

DNMT:

DNA methyltransferase

ESC:

embryonic stem cell

HBV:

hepatitis B virus

HCC:

hepatocellular carcinoma

HCG:

high CpG

HDAC3:

histone deacetylase 3

hnRNP I:

ribonucleoprotein I

LCG:

low CpG

lincRNAs:

large intergenic non-coding RNAs

lncRNAs:

long non-coding RNAs

MEG3:

maternally expressed gene 3

MEN β:

multiple endocrine neoplasia β

miRNAs:

microRNAs

pancRNAs:

promoter-associated non-coding RNAs

PRC2:

polycomb repressive complex2

SRF:

serum response factor

TFBS:

transcription factor binding sites

TSS:

transcription start site

UCA1:

urothelial carcinoma-associated 1

References

  1. Yang, F., Zhang, L., Huo, X.S., Yuan, J.H., Xu, D., Yuan, S.X., Zhu, N., Zhou, W.P., Yang, G.S., Wang, Y.Z., Shang, J.L., Gao, C.F., Zhang, F.R., Wang, F. and Sun, S.H. Long noncoding RNA high expression in hepatocellular carcinoma facilitates tumor growth through enhancer of zeste homolog 2 in humans. Hepatology 54 (2011) 1679–1689.

    Article  CAS  PubMed  Google Scholar 

  2. Zhang, Y., Yang, L. and Chen, L.L. Life without A tail: New formats of long noncoding RNAs. Int. J. Biochem Cell Biol. 2013. DOI: 10.1016/j.biocel.2013.10.009.

    Google Scholar 

  3. Martianov, I., Ramadass, A., Serra Barros, A., Chow, N. and Akoulitchev, A. Repression of the human dihydrofolate reductase gene by a non-coding interfering transcript. Nature 445 (2007) 666–670.

    Article  CAS  PubMed  Google Scholar 

  4. Uhler, J.P., Hertel, C. and Svejstrup, J.Q. A role for noncoding transcription in activation of the yeast PHO5 gene. Proc. Natl. Acad. Sci. USA 104 (2007) 8011–8816.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Martens, J.A., Laprade, L. and Winston, F. Intergenic transcription is required to repress the Saccharomyces cerevisiae SER3 gene. Nature 429 (2004) 571–574.

    Article  CAS  PubMed  Google Scholar 

  6. Rinn, J.L., Kertesz, M, Wang, J.K., Squazzo, S.L., Xu, X, Brugmann, S.A., Goodnough, L.H., Helms, J.A., Farnham, P.J., Segal, E. and Chang, H.Y. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell. 129 (2007) 1311–1323.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. Sleutels, F., Zwart, R. and Barlow, D.P. The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature 415 (2002) 810–813.

    Article  CAS  PubMed  Google Scholar 

  8. Martianov, I., Ramadass, A., Serra Barros, A., Chow, N. and Akoulitchev, A. Repression of the human dihydrofolate reductase gene by a non-coding interfering transcript. Nature 445 (2007) 666–670.

    Article  CAS  PubMed  Google Scholar 

  9. Yang, F., Zhang, L., Huo, X.S., Yuan, J.H., Xu, D., Yuan, S.X., Zhu, N., Zhou, W.P., Yang, G.S., Wang, Y.Z., Shang, J.L., Gao, C.F., Zhang, F.R., Wang, F. and Sun, S.H. Long noncoding RNA high expression in hepatocellular carcinoma facilitates tumor growth through enhancer of zeste homolog 2 in humans. Hepatology 54 (2011) 1679–1689.

    Article  CAS  PubMed  Google Scholar 

  10. Wan, G., Hu, X., Liu, Y., Han, C., Sood, A.K., Calin, G.A., Zhang, X. and Lu, X. A novel non-coding RNA lncRNA-JADE connects DNA damage signalling to histone H4 acetylation. EMBO J. 32 (2013) 2833–2847.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Gao, L., Mai, A., Li, X., Lai, Y., Zheng, J., Yang, Q., Wu, J., Nan, A., Ye, S. and Jiang, Y. LncRNA-DQ786227-mediated cell malignant transformation induced by benzo(a)pyrene. Toxicol Lett. 223 (2013) 205–210.

    Article  CAS  PubMed  Google Scholar 

  12. Song, G., Shen, Y., Zhu, J., Liu, H., Liu, M., Shen, Y.Q., Zhu, S., Kong, X., Yu, Z. and Qian, L. Integrated analysis of dysregulated lncRNA expression in fetal cardiac tissues with ventricular septal defect. PLoS One 8 (2013) e77492.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Sui, W., Lin, H., Peng, W., Huang, Y., Chen, J., Zhang, Y. and Dai, Y. Molecular dysfunctions in acute rejection after renal transplantation revealed by integrated analysis of transcription factor, microRNA and long noncoding RNA. Genomics 102 (2013) 310–322.

    Article  CAS  PubMed  Google Scholar 

  14. Ravasi, T., Suzuki, H., Pang, K.C., Katayama, S., Furuno, M., Okunishi, R., Fukuda, S., Ru, K., Frith, M.C., Gongora, M.M., Grimmond, S.M., Hume, D.A., Hayashizaki, Y. and Mattick, J.S. Experimental validation of the regulated expression of large numbers of non-coding RNAs from the mouse genome. Genome Res. 16 (2006) 11–19.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Hansen, T.B., Wiklund, E.D., Bramsen, J.B., Villadsen, S.B., Statham, A.L., Clark, S.J. and Kjems, J. miRNA-dependent gene silencing involving Ago2- mediated cleavage of a circular antisense RNA. EMBO J. 30 (2011) 4414–4422.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Yang, H., Zhong, Y., Xie, H., Lai, X., Xu, M., Nie, Y., Liu, S. and Wan, Y.J. Induction of the liver cancer-down-regulated long noncoding RNA uc002mbe.2 mediates trichostatin-induced apoptosis of liver cancer cells. Biochem Pharmacol. 85 (2013) 1761–1769.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Yang, F., Huo, X.S., Yuan, S.X., Zhang, L., Zhou, W.P., Wang, F. and Sun, S.H. Repression of the long noncoding RNA-LET by histone deacetylase 3 contributes to hypoxia-mediated metastasis. Mol. Cell. 49 (2013) 1083–1096.

    Article  CAS  PubMed  Google Scholar 

  18. Cawley, S., Bekiranov, S., Ng, H.H., Kapranov, P., Sekinger, E.A., Kampa, D., Piccolboni, A., Sementchenko, V., Cheng, J., Williams, A.J., Wheeler, R., Wong, B., Drenkow, J., Yamanaka, M., Patel, S., Brubaker, S., Tammana, H., Helt, G., Struhl, K. and Gingeras, T.R. Unbiased mapping of transcription factor binding sites along human chromosomes 21 and 22 points to widespread regulation of noncoding RNAs. Cell 116 (2004) 499–509.

    Article  CAS  PubMed  Google Scholar 

  19. Clark, M.B., Johnston, R.L., Inostroza-Ponta, M., Fox, A.H., Fortini, E., Moscato, P., Dinger, M.E. and Mattick, J.S. Genome-wide analysis of long noncoding RNA stability. Genome Res. 22 (2012) 885–898.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Diederichs, S. The four dimensions of noncoding RNA conservation. Trends Genet. 30 (2014) 121–123.

    Article  CAS  PubMed  Google Scholar 

  21. Plath, K., Mlynarczyk-Evans, S, Nusinow, D.A. and Panning, B. Xist RNA and the mechanism of X chromosome inactivation. Annu. Rev. Genet. 36 (2002) 233–278.

    Article  CAS  PubMed  Google Scholar 

  22. Guttman, M., Amit, I., Garber, M., French, C., Lin, M.F., Feldser, D., Huarte, M., Zuk, O., Carey, B.W., Cassady, J.P., Cabili, M.N., Jaenisch, R., Mikkelsen, T.S., Jacks, T., Hacohen, N., Bernstein, B.E., Kellis, M., Regev, A., Rinn, J.L. and Lander, E.S. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458 (2009) 223–227.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Derrien, T., Johnson, R., Bussotti, G., Tanzer, A., Djebali, S., Tilgner, H., Guernec, G., Martin, D., Merkel, A., Knowles, D.G., Lagarde, J., Veeravalli, L., Ruan, X., Ruan, Y., Lassmann, T., Carninci, P., Brown, J.B., Lipovich, L., Gonzalez, J.M., Thomas, M., Davis, C.A., Shiekhattar, R., Gingeras, T.R., Hubbard, T.J., Notredame, C., Harrow, J. and Guigó, R. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res. 22 (2012) 1775–1789.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Carninci, P., Kasukawa, T., Katayama, S., Gough, J., Frith, M.C., Maeda, N, Oyama, R., Ravasi, T., Lenhard, B., Wells, C., Kodzius, R., Shimokawa, K., Bajic, V.B., Brenner, S.E., Batalov, S., Forrest, A.R., Zavolan, M., Davis, M.J., Wilming, L.G., Aidinis, V., Allen, J.E., Ambesi-Impiombato, A., Apweiler, R., Aturaliya, R.N., Bailey, T.L., Bansal, M., Baxter, L., Beisel, K.W., Bersano, T., Bono, H., Chalk, A.M., Chiu, K.P., Choudhary, V., Christoffels, A., Clutterbuck, D.R., Crowe, M.L., Dalla, E., Dalrymple, B.P., de Bono, B., Della Gatta, G., di Bernardo, D., Down, T., Engstrom, P., Fagiolini, M., Faulkner, G., Fletcher, C.F., Fukushima, T., Furuno, M., Futaki, S., Gariboldi, M., Georgii-Hemming, P., Gingeras, T.R., Gojobori, T., Green, R.E., Gustincich, S., Harbers, M., Hayashi, Y., Hensch, T.K., Hirokawa, N., Hill, D., Huminiecki, L., Iacono, M., Ikeo, K., Iwama, A., Ishikawa, T., Jakt, M., Kanapin, A., Katoh, M., Kawasawa, Y., Kelso, J., Kitamura, H., Kitano, H., Kollias, G., Krishnan, S.P., Kruger, A., Kummerfeld, S.K., Kurochkin, I.V., Lareau, L.F., Lazarevic, D., Lipovich, L., Liu, J., Liuni, S., McWilliam, S., Madan Babu, M., Madera, M., Marchionni, L., Matsuda, H., Matsuzawa, S., Miki, H., Mignone, F., Miyake, S., Morris, K., Mottagui-Tabar, S., Mulder, N., Nakano, N., Nakauchi, H., Ng, P., Nilsson, R., Nishiguchi, S., Nishikawa, S., Nori, F., Ohara, O., Okazaki, Y., Orlando, V., Pang, K.C., Pavan, W.J., Pavesi, G., Pesole, G., Petrovsky, N., Piazza, S., Reed, J., Reid, J.F., Ring, B.Z., Ringwald, M., Rost, B., Ruan, Y., Salzberg, S.L., Sandelin, A., Schneider, C., Schönbach, C., Sekiguchi, K., Semple, C.A., Seno, S., Sessa, L., Sheng, Y., Shibata, Y., Shimada, H., Shimada, K., Silva, D., Sinclair, B., Sperling, S., Stupka, E., Sugiura, K, Sultana, R., Takenaka, Y., Taki, K., Tammoja, K., Tan, S.L., Tang, S., Taylor, M.S., Tegner, J., Teichmann, S.A., Ueda, H.R., van Nimwegen, E., Verardo, R., Wei, C.L., Yagi, K., Yamanishi, H., Zabarovsky, E., Zhu, S., Zimmer, A., Hide, W., Bult, C., Grimmond, S.M., Teasdale, R.D., Liu, E.T., Brusic, V., Quackenbush, J., Wahlestedt, C., Mattick, J.S., Hume, D.A., Kai, C., Sasaki, D., Tomaru, Y., Fukuda, S., Kanamori-Katayama, M., Suzuki, M., Aoki, J., Arakawa, T., Iida, J., Imamura, K., Itoh, M., Kato, T., Kawaji, H., Kawagashira, N., Kawashima, T., Kojima, M., Kondo, S., Konno, H., Nakano, K., Ninomiya, N., Nishio, T., Okada, M., Plessy, C., Shibata, K., Shiraki, T., Suzuki, S., Tagami, M., Waki, K., Watahiki, A., Okamura-Oho, Y., Suzuki, H., Kawai, J., Hayashizaki, Y.; FANTOM Consortium; RIKEN Genome Exploration Research Group and Genome Science Group (Genome Network Project Core Group). The transcriptional landscape of the mammalian genome. Science 309 (2005) 1559–1563.

    Article  CAS  PubMed  Google Scholar 

  25. Mohammad, F., Pandey, G.K., Mondal. T., Enroth, S., Redrup, L., Gyllensten, U. and Kanduri, C. Long noncoding RNA-mediated maintenance of DNA methylation and transcriptional gene silencing. Development 139 (2012) 2792–2803.

    Article  CAS  PubMed  Google Scholar 

  26. Chen, Z.J. and Pikaard, C.S. Epigenetic silencing of RNA polymerase I transcription: a role for DNA methylation and histone modification in nucleolar dominance. Genes Dev. 11 (1997) 2124–2136.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Selker, E.U. Trichostatin A causes selective loss of DNA methylation in Neurospora. Proc. Natl. Acad. Sci. USA 95 (1998) 9430–9435.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Braconi, C., Kogure, T., Valeri, N., Huang, N., Nuovo, G., Costinean, S., Negrini, M., Miotto, E., Croce, C.M. and Patel, T. microRNA-29 can regulate expression of the long non-coding RNA gene MEG3 in hepatocellular cancer. Oncogene 30 (2011) 4750–4756.

    Article  CAS  PubMed  Google Scholar 

  29. Amort, T., Soulière, M.F., Wille, A., Jia, X.Y., Fiegl, H., Wörle, H., Micura, R. and Lusser, A. Long non-coding RNAs as targets for cytosine methylation. RNA Biol. 10 (2013) 1003–1008.

    Article  PubMed  Google Scholar 

  30. Yang, H., Zhong, Y., Xie, H., Lai, X., Xu, M., Nie, Y., Liu, S. and Wan, Y.J. Induction of the liver cancer-down-regulated long noncoding RNA uc002mbe.2 mediates trichostatin-induced apoptosis of liver cancer cells. Biochem Pharmacol. 85 (2013) 1761–1769.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Saxonov, S., Berg, P. and Brutlag, D.L. A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proc. Natl. Acad. Sci. USA 103 (2006) 1412–1417.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Elango, N. and Yi, S.V. DNA methylation and structural and functional bimodality of vertebrate promoters. Mol. Biol. Evol. 25 (2008) 1602–1608.

    Article  CAS  PubMed  Google Scholar 

  33. Mikkelsen, T.S., Ku, M., Jaffe, D.B., Issac, B., Lieberman, E., Giannoukos, G., Alvarez, P., Brockman, W., Kim, T.K., Koche, R.P., Lee, W., Mendenhall, E., O’Donovan, A., Presser, A., Russ, C., Xie, X., Meissner, A., Wernig, M., Jaenisch, R., Nusbaum, C., Lander, E.S. and Bernstein, B.E. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448 (2007) 553–560.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Dinger, M.E., Amaral, P.P., Mercer, T.R., Pang, K.C., Bruce, S.J., Gardiner, B.B., Askarian-Amiri, M.E., Ru, K., Soldà, G., Simons, C., Sunkin, S.M., Crowe, M.L., Grimmond, S.M., Perkins, A.C. and Mattick, J.S. Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res. 18 (2008) 1433–1445.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. Khalil, A.M., Guttman, M., Huarte, M., Garber, M., Raj, A., Rivea Morales, D., Thomas, K., Presser, A., Bernstein, B.E., van, Oudenaarden, A., Regev, A., Lander, E.S. and Rinn, J.L. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc. Natl. Acad. Sci. USA 106 (2009) 11667–11672.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Dharap, A., Nakka, V.P., and Vemuganti, R. Effect of focal ischemia on long noncoding RNAs. Stroke 43 (2012) 2800–2802.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Uesaka, M., Nishimura, O., Go, Y., Nakashima, K., Agata, K., Imamura, T. Bidirectional promoters are the major source of gene activation-associated non-coding RNAs in mammals. BMC Genomics 15 (2014). DOI: 10.1186/1471-2164-15-35.

  38. Engstrom, P.G., Suzuki, H., Ninomiya, N., Akalin, A., Sessa, L., Lavorgna, G., Brozzi, A., Luzi, L., Tan, S.L., Yang, L., Kunarso, G., Ng, E.L., Batalov, S., Wahlestedt, C., Kai, C., Kawai, J., Carninci, P., Hayashizaki, Y., Wells, C., Bajic, V.B., Orlando, V., Reid, J.F., Lenhard, B., Lipovich, L. Complex Loci in human and mouse genomes. PLoS Genet. 2 (2006) e47.

    Article  PubMed Central  PubMed  Google Scholar 

  39. Wang, Y., Pang, W.J., Wei, N., Xiong, Y., Wu, W.J., Zhao, C.Z., Shen, Q.W. and Yang, G.S. Identification, stability and expression of Sirt1 antisense long non-coding RNA. Gene 539 (2014) 117–124.

    Article  CAS  PubMed  Google Scholar 

  40. Yoon, J.H., Abdelmohsen, K. and Gorospe, M. Posttranscriptional gene regulation by long noncoding RNA. J. Mol. Biol. 425 (2013) 3723–3730.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Wilusz, J.E., JnBaptiste, C.K., Lu, L.Y., Kuhn, C.D., Joshua-Tor, L. and Sharp, P.A. A triple helix stabilizes the 3’ ends of long noncoding RNAs that lack poly(A) tails. Genes Dev. 26 (2012) 2392–2407.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  42. Brown, J.A., Valenstein, M.L., Yario, T.A., Tycowski, K.T. and Steitz, J.A. Formation of triple-helical structures by the 3′-end sequences of MALAT1 and MENβnoncoding RNAs. Proc. Natl. Acad. Sci. USA 109 (2012) 19202–19207.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  43. Yoon, J.H., Abdelmohsen, K., Srikantan, S., Yang, X., Martindale, J.L., De, S., Huarte, M., Zhan, M., Becker, K.G. and Gorospe, M. LincRNA-p21 suppresses target mRNA translation. Mol. Cell. 47 (2012) 648–655.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. Jalali, S., Bhartiya, D., Lalwani, M.K., Sivasubbu, S. and Scaria, V. Systematic transcriptome wide analysis of lncRNA-miRNA interactions. PLoS One 8 (2013) e53823.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  45. Chiyomaru, T., Fukuhara, S., Saini, S., Majid, S., Deng, G., Shahryary, V., Chang, I., Tanaka, Y., Enokida, H., Nakagawa, M., Dahiya, R. and Yamamura, S. Long non-coding RNA HOTAIR is targeted and regulated by miR-141 in human cancer cells. J. Biol. Chem. 18 (2014) 12550–12565.

    Article  Google Scholar 

  46. Yoon, J.H., Abdelmohsen K., Kim J., Yang X., Martindale J.L., Tominaga-Yamanaka K., White E.J., Orjalo A.V., Rinn J.L., Kreft S.G., Wilson G.M. and Gorospe M. Scaffold function of long non-coding RNA HOTAIR in protein ubiquitination. Nat. Commun. 2013. DOI: 10.1038/ncomms3939.

    Google Scholar 

  47. Han, Y., Liu, Y., Zhang, H., Wang, T., Diao, R., Jiang, Z., Gui, Y. and Cai, Z. Hsa-miR-125b suppresses bladder cancer development by down-regulating oncogene SIRT7 and oncogenic long noncoding RNA MALAT1. FEBS Lett. 587 (2013) 3875–3882.

    Article  CAS  PubMed  Google Scholar 

  48. Huang, J., Zhou, N., Watabe, K., Lu, Z., Wu, F., Xu, M. and Mo, Y.Y. Long non-coding RNA UCA1 promotes breast tumor growth by suppression of p27 (Kip1). Cell Death Dis. 5 (2014) e1008.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  49. Mercer, T.R. and Mattick, J.S. Structure and function of long noncoding RNAs in epigenetic regulation. Nat. Struct. Mol. Biol. 20 (2013) 300–307.

    Article  CAS  PubMed  Google Scholar 

  50. Yang, Y., Zhou, X. and Jin, Y. ADAR-mediated RNA editing in non-coding RNA sequences. Sci. China Life Sci. 56 (2013) 944–952.

    Article  CAS  PubMed  Google Scholar 

  51. Cantara, W.A., Crain, P.F., Rozenski, J., McCloskey, J.A., Harris, K.A., Zhang, X., Vendeix, F.A., Fabris, D. and Agris, P.F. The RNA Modification Database, RNAMDB: 2011 update. Nucleic Acids Res. 39 (2011)(Database issue) D195–201.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  52. Wang, J., Liu, X., Wu, H., Ni, P., Gu, Z., Qiao, Y., Chen, N., Sun, F. and Fan, Q. CREB up-regulates long non-coding RNA, HULC expression through interaction with microRNA-372 in liver cancer. Nucleic Acids Res. 38 (2010) 5366–5383.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  53. Leucci, E., Patella, F., Waage, J., Holmstrøm, K., Lindow, M., Porse, B., Kauppinen, S. and Lund, A.H. microRNA-9 targets the long non-coding RNA MALAT1 for degradation in the nucleus. Sci. Rep. 3 (2013). DOI: 10.1038/srep02535.

  54. Chiyomaru, T., Yamamura, S., Fukuhara, S., Yoshino, H., Kinoshita, T., Majid, S., Saini, S., Chang, I., Tanaka, Y., Enokida, H., Seki, N., Nakagawa, M. and Dahiya, R. Genistein inhibits prostate cancer cell growth by targeting miR-34a and oncogenic HOTAIR. PLoS One 8 (2013) e70372.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Center for Drug Research and Development, Zhujiang Hospital, Southern Medical University, Zhujiang, China

    Zhuomin Wu, Xiaoxia Liu, Li Liu, Houliang Deng, Jingjing Zhang, Qian Xu, Bohong Cen & Aimin Ji

Authors
  1. Zhuomin Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaoxia Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Li Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Houliang Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jingjing Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Qian Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bohong Cen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Aimin Ji
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aimin Ji.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, Z., Liu, X., Liu, L. et al. Regulation of lncRNA expression. Cell Mol Biol Lett 19, 561–575 (2014). https://doi.org/10.2478/s11658-014-0212-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11658-014-0212-6

Keywords

Cellular & Molecular Biology Letters

ISSN: 1689-1392

Contact us