MiR-138 downregulates miRNA processing in HeLa cells by targeting RMND5A and decreasing Exportin-5 stability

Nucleic Acids Research

Volumn 42, Issue 1, 2014, Pages 458-474

  Li, Jie ^a   Chen, Ying ^a   Qin, Xingliang ^a   Wen, Junzhi ^b   Ding, Hongmei ^a   Xia, Wei ^a   Li, Shaohua ^a   Su, Xueting ^a   Wang, Wei ^a   Li, Hui ^a   Zhao, Qiang ^a   Fang, Tao ^a   Qu, Lianghu ^b   Shao, Ningsheng ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; EXPORTIN 5; MICRORNA; MICRORNA 138; REQUIRED FOR MEIOTIC NUCLEAR DIVISION 5 HOMOLOG A; UNCLASSIFIED DRUG;

ARTICLE; CELL MIGRATION; CONTROLLED STUDY; DNA SEQUENCE; DOWN REGULATION; GENE CONTROL; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INTERACTION; GENE OVEREXPRESSION; GENETIC STABILITY; HELA CELL; NUCLEAR EXPORT SIGNAL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RNA ANALYSIS; RNA PROCESSING; GENE; HELA CELL LINE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN RNA BINDING; PROTEIN STABILITY; PROTEIN TARGETING; REQUIRED FOR MEIOTIC NUCLEAR DIVISION 5 HOMOLOG A GENE;

EID: 84891818589     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt839     Document Type: Article

References (63)

1. Bartel, D.P. (2004) MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell, 116, 281-297.
2. Djuranovic, S., Nahvi, A. and Green, R. (2011) A parsimonious model for gene regulation by miRNAs. Science, 331, 550-553.
3. Filipowicz, W., Bhattacharyya, S.N. and Sonenberg, N. (2008) Mechanisms of post-Transcriptional regulation by microRNAs: Are the answers in sight. Nat. Rev. Genet., 9, 102-114.
4. Kusenda, B., Mraz, M., Mayer, J. and Pospisilova, S. (2006) MicroRNA biogenesis, functionality and cancer relevance. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub., 150, 205-215.
5. Lim, L.P., Lau, N.C., Garrett-Engele, P., Grimson, A., Schelter, J.M., Castle, J., Bartel, D.P., Linsley, P.S. and Johnson, J.M. (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature, 433, 769-773.
6. Brennecke, J., Hipfner, D.R., Stark, A., Russell, R.B. and Cohen, S.M. (2003) bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell, 113, 25-36.
7. Cuellar, T.L. and McManus, M.T. (2005) MicroRNAs and endocrine biology. J. Endocrinol., 187, 327-332.
8. Poy, M.N., Eliasson, L., Krutzfeldt, J., Kuwajima, S., Ma, X., Macdonald, P.E., Pfeffer, S., Tuschl, T., Rajewsky, N., Rorsman, P. et al. (2004) A pancreatic islet-specific microRNA regulates insulin secretion. Nature, 432, 226-230.
9. Chen, C.Z., Li, L., Lodish, H.F. and Bartel, D.P. (2004) MicroRNAs modulate hematopoietic lineage differentiation. Science, 303, 83-86.
10. Wilfred, B.R., Wang, W.X. and Nelson, P.T. (2007) Energizing miRNA research: A review of the role of miRNAs in lipid metabolism, with a prediction that miR-103/107 regulates human metabolic pathways. Mol. Genet. Metab., 91, 209-217.
11. Ha, T.Y. (2011) MicroRNAs in human diseases: From lung, liver and kidney diseases to infectious disease, sickle cell disease and Endometrium disease. Immune Netw., 11, 309-323.
12. Martignani, E., Miretti, S., Accornero, P. and Baratta, M. (2011) miRNAs highlights in stem and cancer cells. Mini Rev. Med. Chem., 11, 1165-182.
13. Iorio, M.V. and Croce, C.M. (2012) MicroRNA dysregulation in cancer: Diagnostics, monitoring and therapeutics. EMBO Mol. Med., 4, 143-159.
14. Ivey, K.N., Muth, A., Arnold, J., King, F.W., Yeh, R.F., Fish, J.E., Hsiao, E.C., Schwartz, R.J., Conklin, B.R., Bernstein, H.S. et al. (2008) MicroRNA regulation of cell lineages in mouse and human embryonic stem cells. Cell Stem Cell, 2, 219-229.
15. Sun, G., Li, H., Wu, X., Covarrubias, M., Scherer, L., Meinking, K., Luk, B., Chomchan, P., Alluin, J., Gombart, A.F. et al. (2012) Interplay between HIV-1 infection and host microRNAs. Nucleic Acids Res., 40, 2181-2196.
16. Zampetaki, A. and Mayr, M. (2012) MicroRNAs in vascular and metabolic disease. Circ. Res., 110, 508-522.
17. Bartel, D.P. (2009) MicroRNAs: Target recognition and regulatory functions. Cell, 136, 215-233.
18. Cai, X., Hagedorn, C.H. and Cullen, B.R. (2004) Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA, 10, 1957-1966.
19. Lee, Y., Kim, M., Han, J., Yeom, K.H., Lee, S., Baek, S.H. and Kim, V.N. (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J., 23, 4051-4060.
20. Faller, M. and Guo, F. (2008) MicroRNA biogenesis: There's more than one way to skin a cat. Biochim. Biophys. Acta, 1779, 663-667.
21. Rodriguez, A., Griffiths-Jones, S., Ashurst, J.L. and Bradley, A. (2004) Identification of mammalian microRNA host genes and transcription units. Genome Res., 14, 1902-1910.
22. Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J., Provost, P., Radmark, O., Kim, S. et al. (2003) The nuclear RNase iii Drosha initiates microRNA processing. Nature, 425, 415-419.
23. Gregory, R.I., Chendrimada, T.P. and Shiekhattar, R. (2006) MicroRNA biogenesis: Isolation and characterization of the microprocessor complex. Methods Mol. Biol., 342, 33-47.
24. Yi, R., Qin, Y., Macara, I.G. and Cullen, B.R. (2003) Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev., 17, 3011-3016.
25. Lund, E., Guttinger, S., Calado, A., Dahlberg, J.E. and Kutay, U. (2004) Nuclear export of microRNA precursors. Science, 303, 95-98.
26. Bohnsack, M.T., Czaplinski, K. and Gorlich, D. (2004) Exportin 5 is a RanGTP-dependent dsRNA-binding protein that mediates nuclear export of pre-miRNAs. RNA, 10, 185-191.
27. Yi, R., Doehle, B.P., Qin, Y., Macara, I.G. and Cullen, B.R. (2005) Overexpression of exportin 5 enhances RNA interference mediated by short hairpin RNAs and microRNAs. RNA, 11, 220-226.
28. Lund, E. and Dahlberg, J.E. (2006) Substrate selectivity of exportin 5 and Dicer in the biogenesis of microRNAs. Cold Spring Harb. Symp. Quant. Biol., 71, 59-66.
29. Macrae, I.J., Zhou, K., Li, F., Repic, A., Brooks, A.N., Cande, W.Z., Adams, P.D. and Doudna, J.A. (2006) Structural basis for doublestranded RNA processing by Dicer. Science, 311, 195-198.
30. Gregory, R.I., Chendrimada, T.P., Cooch, N. and Shiekhattar, R. (2005) Human RISC couples microRNA biogenesis and posttranscriptional gene silencing. Cell, 123, 631-640.
31. Rana, T.M. (2007) Illuminating the silence: Understanding the structure and function of small RNAs. Nat. Rev. Mol. Cell Biol., 8, 23-36.
32. Lagos-Quintana, M., Rauhut, R., Yalcin, A., Meyer, J., Lendeckel, W. and Tuschl, T. (2002) Identification of tissue-specific microRNAs from mouse. Curr. Biol., 12, 735-739.
33. Griffiths-Jones, S. (2004) The microRNA Registry. Nucleic Acids Res., 32, D109-D111.
34. Weber, M.J. (2005) New human and mouse microRNA genes found by homology search. FEBS J., 272, 59-73.
35. Liu, X., Jiang, L., Wang, A., Yu, J., Shi, F. and Zhou, X. (2009) MicroRNA-138 suppresses invasion and promotes apoptosis in head and neck squamous cell carcinoma cell lines. Cancer Lett., 286, 217-222.
36. Liu, X., Wang, C., Chen, Z., Jin, Y., Wang, Y., Kolokythas, A., Dai, Y. and Zhou, X. (2011) MicroRNA-138 suppresses epithelialmesenchymal transition in squamous cell carcinoma cell lines. Biochem. J., 440, 23-31.
37. Jiang, L., Liu, X., Kolokythas, A., Yu, J., Wang, A., Heidbreder, C.E., Shi, F. and Zhou, X. (2010) Downregulation of the Rho GTPase signaling pathway is involved in the microRNA- 138-mediated inhibition of cell migration and invasion in tongue squamous cell carcinoma. Int. J. Cancer, 127, 505-512.
38. Yeh, Y.M., Chuang, C.M., Chao, K.C. and Wang, L.H. (2013) MicroRNA-138 suppresses ovarian cancer cell invasion and metastasis by targeting SOX4 and HIF-1alpha. Int. J. Cancer, 133, 867-878.
39. Jiang, L., Dai, Y., Liu, X., Wang, C., Wang, A., Chen, Z., Heidbreder, C.E., Kolokythas, A. and Zhou, X. (2011) Identification and experimental validation of G protein alpha inhibiting activity polypeptide 2 (GNAI2) as a microRNA-138 target in tongue squamous cell carcinoma. Hum. Genet., 129, 189-197.
40. Jin, Y., Wang, C., Liu, X., Mu, W., Chen, Z., Yu, D., Wang, A., Dai, Y. and Zhou, X. (2011) Molecular characterization of the microRNA-138-Fos-like antigen 1 (FOSL1) regulatory module in squamous cell carcinoma. J. Biol. Chem., 286, 40104-40109.
41. Siegel, G., Obernosterer, G., Fiore, R., Oehmen, M., Bicker, S., Christensen, M., Khudayberdiev, S., Leuschner, P.F., Busch, C.J., Kane, C. et al. (2009) A functional screen implicates microRNA- 138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. Nat. Cell Biol., 11, 705-716.
42. Yang, Z., Bian, C., Zhou, H., Huang, S., Wang, S., Liao, L. and Zhao, R.C. (2011) MicroRNA hsa-miR-138 inhibits adipogenic differentiation of human adipose tissue-derived mesenchymal stem cells through adenovirus EID-1. Stem Cells Dev., 20, 259-267.
43. Gong, H., Song, L., Lin, C., Liu, A., Lin, X., Wu, J., Li, M. and Li, J. (2013) Downregulation of miR-138 sustains NF-kappaB activation and promotes lipid raft formation in esophageal squamous cell carcinoma. Clin. Cancer Res., 19, 1083-1093.
44. Eskildsen, T., Taipaleenmaki, H., Stenvang, J., Abdallah, B.M., Ditzel, N., Nossent, A.Y., Bak, M., Kauppinen, S. and Kassem, M. (2011) MicroRNA-138 regulates osteogenic differentiation of human stromal (mesenchymal) stem cells in vivo. Proc. Natl Acad. Sci. USA, 108, 6139-6144.
45. Wang, Y., Huang, J.W., Li, M., Cavenee, W.K., Mitchell, P.S., Zhou, X., Tewari, M., Furnari, F.B. and Taniguchi, T. (2011) MicroRNA-138 modulates DNA damage response by repressing histone H2AX expression. Mol. Cancer Res., 9, 1100-1111.
46. Mitomo, S., Maesawa, C., Ogasawara, S., Iwaya, T., Shibazaki, M., Yashima-Abo, A., Kotani, K., Oikawa, H., Sakurai, E., Izutsu, N. et al. (2008) Downregulation of miR-138 is associated with overexpression of human telomerase reverse transcriptase protein in human anaplastic thyroid carcinoma cell lines. Cancer Sci., 99, 280-286.
47. Zhao, X., Yang, L., Hu, J. and Ruan, J. (2010) miR-138 might reverse multidrug resistance of leukemia cells. Leuk. Res., 34, 1078-1082.
48. Wong, T.S., Liu, X.B., Chung-Wai, H.A., Po-Wing, Y.A., Wai- Man, N.R. and Ignace, W.W. (2008) Identification of pyruvate kinase type M2 as potential oncoprotein in squamous cell carcinoma of tongue through microRNA profiling. Int. J. Cancer, 123, 251-257.
49. Wong, T.S., Liu, X.B., Wong, B.Y., Ng, R.W., Yuen, A.P. and Wei, W.I. (2008) Mature miR-184 as Potential Oncogenic microRNA of Squamous Cell Carcinoma of Tongue. Clin. Cancer Res., 14, 2588-2592.
50. Obernosterer, G., Leuschner, P.J., Alenius, M. and Martinez, J. (2006) Post-Transcriptional regulation of microRNA expression. RNA, 12, 1161-1167.
51. Huang, B.X. and Kim, H.Y. (2013) Effective identification of Akt interacting proteins by two-step chemical crosslinking, coimmunoprecipitation and mass spectrometry. PLoS One, 8, e61430.
52. Choo, Y.S. and Zhang, Z. (2009) Detection of protein ubiquitination. J Vis Exp., 19, pii.1293.
53. Strausberg, R.L., Feingold, E.A., Grouse, L.H., Derge, J.G., Klausner, R.D., Collins, F.S., Wagner, L., Shenmen, C.M., Schuler, G.D., Altschul, S.F. et al. (2002) Generation and initial analysis of more than 15, 000 full-length human and mouse cDNA sequences. Proc. Natl Acad. Sci. USA, 99, 16899-16903.
54. Kobayashi, N., Yang, J., Ueda, A., Suzuki, T., Tomaru, K., Takeno, M., Okuda, K. and Ishigatsubo, Y. (2007) RanBPM, Muskelin, p48EMLP, p44CTLH, and the armadillo-repeat proteins ARMC8alpha and ARMC8beta are components of the CTLH complex. Gene, 396, 236-247.
55. Nishitani, H., Hirose, E., Uchimura, Y., Nakamura, M., Umeda, M., Nishii, K., Mori, N. and Nishimoto, T. (2001) Full-sized RanBPM cDNA encodes a protein possessing a long stretch of proline and glutamine within the N-Terminal region, comprising a large protein complex. Gene, 272, 25-33.
56. Suresh, B., Ramakrishna, S. and Baek, K.H. (2012) Diverse roles of the scaffolding protein RanBPM. Drug Discov. Today, 17, 379-387.
57. Brownawell, A.M. and Macara, I.G. (2002) Exportin-5, a novel karyopherin, mediates nuclear export of double-stranded RNA binding proteins. J. Cell Biol., 156, 53-64.
58. Bennasser, Y., Chable-Bessia, C., Triboulet, R., Gibbings, D., Gwizdek, C., Dargemont, C., Kremer, E.J., Voinnet, O. and Benkirane, M. (2011) Competition for XPO5 binding between Dicer mRNA, pre-miRNA and viral RNA regulates human Dicer levels. Nat. Struct. Mol. Biol., 18, 323-327.
59. Yan, W., Lee, H., Yi, E.C., Reiss, D., Shannon, P., Kwieciszewski, B.K., Coito, C., Li, X.J., Keller, A., Eng, J. et al. (2004) System-based proteomic analysis of the interferon response in human liver cells. Genome Biol., 5, R54.
60. Resing, K.A., Meyer-Arendt, K., Mendoza, A.M., Aveline- Wolf, L.D., Jonscher, K.R., Pierce, K.G., Old, W.M., Cheung, H.T., Russell, S., Wattawa, J.L. et al. (2004) Improving reproducibility and sensitivity in identifying human proteins by shotgun proteomics. Anal. Chem., 76, 3556-3568.
61. Tanner, S., Shen, Z., Ng, J., Florea, L., Guigo, R., Briggs, S.P. and Bafna, V. (2007) Improving gene annotation using peptide mass spectrometry. Genome Res., 17, 231-239.
62. Martello, G., Rosato, A., Ferrari, F., Manfrin, A., Cordenonsi, M., Dupont, S., Enzo, E., Guzzardo, V., Rondina, M., Spruce, T. et al. (2010) A MicroRNA targeting dicer for metastasis control. Cell, 141, 1195-1207.
63. Tang, K.F., Song, G.B., Shi, Y.S., Yuan, L. and Li, Y.H. (2010) Dicer knockdown induces fibronectin-1 expression in HEK293T cells via induction of Egr1. Biochim. Biophys. Acta, 1800, 380-384.