microRNAs: tiny RNA molecules, huge driving forces to move the cell
microRNAs: tiny RNA molecules, huge driving forces to move the cell
Shenglin Huang, Xianghuo He()
State Key Laboratory of Oncogenes and Related Genes, Shanghai Cancer Institute, Shanghai Jiao Tong University School of Medicine, Shanghai 200032, China
Cell migration or movement is a highly dynamic cellular process, requiring precise regulation that is essential for a variety of biological processes. microRNAs (miRNAs) are a class of tiny non-coding RNA molecules that function as critical post-transcriptional regulators of gene expression. Emerging evidence demonstrates that miRNAs play important roles in cell migration and directly contribute to extracellular matrix (ECM) remodeling, cell adhesion, and cell signalling that controls cell migration by targeting a large number of protein-coding genes. Accordingly, the dysregulation of these miRNAs has been linked to several migration-related diseases. In this review, we summarize and highlight the recent advances concerning the roles and validated targets of miRNAs in the control of cell movement.
Bentwich, I., Avniel, A., Karov, Y., Aharonov, R., Gilad, S., Barad, O., Barzilai, A., Einat, P., Einav, U., Meiri, E., . (2005). Identification of hundreds of conserved and nonconserved human microRNAs. Nat Genet 37, 766-770 . doi: 10.1038/ng1590
5
Crawford, M., Brawner, E., Batte, K., Yu, L., Hunter, M.G., Otterson, G.A., Nuovo, G., Marsh, C.B., and Nana-Sinkam, S.P. (2008). MicroRNA-126 inhibits invasion in non-small cell lung carcinoma cell lines. Biochem Biophys Res Commun 373, 607-612 . doi: 10.1016/j.bbrc.2008.06.090
6
Crist, C.G., Montarras, D., Pallafacchina, G., Rocancourt, D., Cumano, A., Conway, S.J., and Buckingham, M. (2009). Muscle stem cell behavior is modified by microRNA-27 regulation of Pax3 expression. Proc Natl Acad Sci U S A 106, 13383-13387 . doi: 10.1073/pnas.0900210106
7
Delaloy, C., Liu, L., Lee, J.A., Su, H., Shen, F., Yang, G.Y., Young, W.L., Ivey, K.N., and Gao, F.B. (2010). MicroRNA-9 coordinates proliferation and migration of human embryonic stem cell-derived neural progenitors. Cell Stem Cell 6, 323-335 .
8
Ding, J., Huang, S., Wu, S., Zhao, Y., Liang, L., Yan, M., Ge, C., Yao, J., Chen, T., Wan, D., . (2010). Gain of miR-151 on chromosome 8q24.3 facilitates tumour cell migration and spreading through downregulating RhoGDIA. Nat Cell Biol 12, 390-399 . doi: 10.1038/ncb2039
9
Esquela-Kerscher, A., and Slack, F.J. (2006). Oncomirs- microRNAs with a role in cancer. Nat Rev Cancer 6, 259-269 . doi: 10.1038/nrc1840
10
Evangelisti, C., Florian, M.C., Massimi, I., Dominici, C., Giannini, G., Galardi, S., Buè, M.C., Massalini, S., McDowell, H.P., Messi, E., . (2009). miR-128 up-regulation inhibits Reelin and DCX expression and reduces neuroblastoma cell motility and invasiveness. FASEB J 23, 4276-4287 . doi: 10.1096/fj.09-134965
11
Fasanaro, P., D’Alessandra, Y., Di Stefano, V., Melchionna, R., Romani, S., Pompilio, G., Capogrossi, M.C., and Martelli, F. (2008). MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. J Biol Chem 283, 15878-15883 . doi: 10.1074/jbc.M800731200
12
Fornari, F., Milazzo, M., Chieco, P., Negrini, M., Calin, G.A., Grazi, G.L., Pollutri, D., Croce, C.M., Bolondi, L., and Gramantieri, L. (2010). miR-199a-3p regulates mTOR and c-Met to influence the doxorubicin sensitivity of human hepatocarcinoma cells. Cancer Res 70, 5184-5193 .
13
Friedl, P., and Wolf, K. (2010). Plasticity of cell migration: a multiscale tuning model. J Cell Biol 188, 11-19 . doi: 10.1083/jcb.200909003
14
Friedman, R.C., Farh, K.K., Burge, C.B., and Bartel, D.P. (2009). Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19, 92-105 . doi: 10.1101/gr.082701.108
Garofalo, M., Di Leva, G., Romano, G., Nuovo, G., Suh, S.S., Ngankeu, A., Taccioli, C., Pichiorri, F., Alder, H., Secchiero, P., . (2009). miR-221&222 regulate TRAIL resistance and enhance tumorigenicity through PTEN and TIMP3 downregulation. Cancer Cell 16, 498-509 . doi: 10.1016/j.ccr.2009.10.014
17
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 .
18
He, L., and Hannon, G.J. (2004). MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5, 522-531 . doi: 10.1038/nrg1379
19
Huang, Q., Gumireddy, K., Schrier, M., le Sage, C., Nagel, R., Nair, S., Egan, D.A., Li, A., Huang, G., Klein-Szanto, A.J., . (2008). The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nat Cell Biol 10, 202-210 . doi: 10.1038/ncb1681
20
Ji, J., Zhao, L., Budhu, A., Forgues, M., Jia, H.L., Qin, L.X., Ye, Q.H., Yu, J., Shi, X., Tang, Z.Y., . (2010). Let-7g targets collagen type I alpha2 and inhibits cell migration in hepatocellular carcinoma. J Hepatol 52, 690-697 . doi: 10.1016/j.jhep.2009.12.025
21
Ji, X. (2008). The mechanism of RNase III action: how dicer dices. Curr Top Microbiol Immunol 320, 99-116 . doi: 10.1007/978-3-540-75157-1_5
22
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 . doi: 10.1002/ijc.25320
23
Korpal, M., Lee, E.S., Hu, G., and Kang, Y. (2008). The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem 283, 14910-14914 . doi: 10.1074/jbc.C800074200
24
Lauffenburger, D.A., and Horwitz, A.F. (1996). Cell migration: a physically integrated molecular process. Cell 84, 359-369 .
25
Lee, R.C., Feinbaum, R.L., and Ambros, V. (1993). The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843-854 .
26
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 .
27
Li, G., Luna, C., Qiu, J., Epstein, D.L., and Gonzalez, P. (2010). Targeting of integrin beta1 and kinesin 2alpha by microRNA 183. J Biol Chem 285, 5461-5471 . doi: 10.1074/jbc.M109.037127
28
Li, N., Fu, H., Tie, Y., Hu, Z., Kong, W., Wu, Y., and Zheng, X. (2009a). miR-34a inhibits migration and invasion by down-regulation of c-Met expression in human hepatocellular carcinoma cells. Cancer Lett 275, 44-53 . doi: 10.1016/j.canlet.2008.09.035
29
Li, S., Fu, H., Wang, Y., Tie, Y., Xing, R., Zhu, J., Sun, Z., Wei, L., and Zheng, X. (2009b). MicroRNA-101 regulates expression of the v-fos FBJ murine osteosarcoma viral oncogene homolog (FOS) oncogene in human hepatocellular carcinoma. Hepatology 49, 1194-1202 . doi: 10.1002/hep.22757
30
Li, Y., Song, Y.H., Li, F., Yang, T., Lu, Y.W., and Geng, Y.J. (2009c). MicroRNA-221 regulates high glucose-induced endothelial dysfunction. Biochem Biophys Res Commun 381, 81-83 . doi: 10.1016/j.bbrc.2009.02.013
31
Lin, S.L., Chiang, A., Chang, D., and Ying, S.Y. (2008). Loss of mir-146a function in hormone-refractory prostate cancer. RNA 14, 417-424 .
32
Ma, L., Teruya-Feldstein, J., and Weinberg, R.A. (2007). Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449, 682-688 . doi: 10.1038/nature06174
33
Ma, L., Young, J., Prabhala, H., Pan, E., Mestdagh, P., Muth, D., Teruya-Feldstein, J., Reinhardt, F., Onder, T.T., Valastyan, S., . (2010). miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol 12, 247-256 .
34
Meng, F., Henson, R., Wehbe-Janek, H., Ghoshal, K., Jacob, S.T., and Patel, T. (2007). MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 133, 647-658 . doi: 10.1053/j.gastro.2007.05.022
35
Murchison, E.P., and Hannon, G.J. (2004). miRNAs on the move: miRNA biogenesis and the RNAi machinery. Curr Opin Cell Biol 16, 223-229 . doi: 10.1016/j.ceb.2004.04.003
36
Parent, C.A., and Devreotes, P.N. (1999). A cell’s sense of direction. Science 284, 765-770 . doi: 10.1126/science.284.5415.765
37
Pineau, P., Volinia, S., McJunkin, K., Marchio, A., Battiston, C., Terris, B., Mazzaferro, V., Lowe, S.W., Croce, C.M., and Dejean, A. (2010). miR-221 overexpression contributes to liver tumorigenesis. Proc Natl Acad Sci U S A 107, 264-269 . doi: 10.1073/pnas.0907904107
38
Poliseno, L., Tuccoli, A., Mariani, L., Evangelista, M., Citti, L., Woods, K., Mercatanti, A., Hammond, S., and Rainaldi, G. (2006). MicroRNAs modulate the angiogenic properties of HUVECs. Blood 108, 3068-3071 . doi: 10.1182/blood-2006-01-012369
39
Rana, T.M. (2007). Illuminating the silence: understanding the structure and function of small RNAs. Nat Rev Mol Cell Biol 8, 23-36 . doi: 10.1038/nrm2085
40
Reddy, S.D., Ohshiro, K., Rayala, S.K., and Kumar, R. (2008). MicroRNA-7, a homeobox D10 target, inhibits p21-activated kinase 1 and regulates its functions. Cancer Res 68, 8195-8200 . doi: 10.1158/0008-5472.CAN-08-2103
41
Reddy, S.D., Pakala, S.B., Ohshiro, K., Rayala, S.K., and Kumar, R. (2009). MicroRNA-661, a c/EBPalpha target, inhibits metastatic tumor antigen 1 and regulates its functions. Cancer Res 69, 5639-5642 . doi: 10.1158/0008-5472.CAN-09-0898
42
Ridley, A.J., Schwartz, M.A., Burridge, K., Firtel, R.A., Ginsberg, M.H., Borisy, G., Parsons, J.T., and Horwitz, A.R. (2003). Cell migration: integrating signals from front to back. Science 302, 1704-1709 . doi: 10.1126/science.1092053
43
Salvi, A., Sabelli, C., Moncini, S., Venturin, M., Arici, B., Riva, P., Portolani, N., Giulini, S.M., De Petro, G., and Barlati, S. (2009). MicroRNA-23b mediates urokinase and c-met downmodulation and a decreased migration of human hepatocellular carcinoma cells. FEBS J 276, 2966-2982 . doi: 10.1111/j.1742-4658.2009.07014.x
44
Scott, G.K., Goga, A., Bhaumik, D., Berger, C.E., Sullivan, C.S., and Benz, C.C. (2007). Coordinate suppression of ERBB2 and ERBB3 by enforced expression of micro-RNA miR-125a or miR-125b. J Biol Chem 282, 1479-1486 . doi: 10.1074/jbc.M609383200
45
Segura, M.F., Hanniford, D., Menendez, S., Reavie, L., Zou, X., Alvarez-Diaz, S., Zakrzewski, J., Blochin, E., Rose, A., Bogunovic, D., . (2009). Aberrant miR-182 expression promotes melanoma metastasis by repressing FOXO3 and microphthalmia-associated transcription factor. Proc Natl Acad Sci U S A 106, 1814-1819 . doi: 10.1073/pnas.0808263106
46
Sehm, T., Sachse, C., Frenzel, C., and Echeverri, K. (2009). miR-196 is an essential early-stage regulator of tail regeneration, upstream of key spinal cord patterning events. Dev Biol 334, 468-480 . doi: 10.1016/j.ydbio.2009.08.008
47
Sengupta, S., den Boon, J.A., Chen, I.H., Newton, M.A., Stanhope, S.A., Cheng, Y.J., Chen, C.J., Hildesheim, A., Sugden, B., and Ahlquist, P. (2008). MicroRNA 29c is down-regulated in nasopharyngeal carcinomas, up-regulating mRNAs encoding extracellular matrix proteins. Proc Natl Acad Sci U S A 105, 5874-5878 . doi: 10.1073/pnas.0801130105
Song, H., and Bu, G. (2009). MicroRNA-205 inhibits tumor cell migration through down-regulating the expression of the LDL receptor-related protein 1. Biochem Biophys Res Commun 388, 400-405 . doi: 10.1016/j.bbrc.2009.08.020
50
Tavazoie, S.F., Alarcón, C., Oskarsson, T., Padua, D., Wang, Q., Bos, P.D., Gerald, W.L., and Massagué, J. (2008). Endogenous human microRNAs that suppress breast cancer metastasis. Nature 451, 147-152 . doi: 10.1038/nature06487
51
Tian, Y., Luo, A., Cai, Y., Su, Q., Ding, F., Chen, H., and Liu, Z. (2010). MicroRNA-10b promotes migration and invasion through KLF4 in human esophageal cancer cell lines. J Biol Chem 285, 7986-7994 . doi: 10.1074/jbc.M109.062877
Valastyan, S., Reinhardt, F., Benaich, N., Calogrias, D., Szász, A.M., Wang, Z.C., Brock, J.E., Richardson, A.L., and Weinberg, R.A. (2009). A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell 137, 1032-1046 .
54
Wang, B., Hsu, S.H., Majumder, S., Kutay, H., Huang, W., Jacob, S.T., and Ghoshal, K. (2010a). TGFbeta-mediated upregulation of hepatic miR-181b promotes hepatocarcinogenesis by targeting TIMP3. Oncogene 29, 1787-1797 .
55
Wang, C.H., Lee, D.Y., Deng, Z., Jeyapalan, Z., Lee, S.C., Kahai, S., Lu, W.Y., Zhang, Y., Yang, B.B., and B?hler, J. (2008a). MicroRNA miR-328 regulates zonation morphogenesis by targeting CD44 expression. PLoS ONE 3, e2420. doi: 10.1371/journal.pone.0002420
56
Wang, G., Mao, W., and Zheng, S. (2008b). MicroRNA-183 regulates Ezrin expression in lung cancer cells. FEBS Lett 582, 3663-3668 . doi: 10.1016/j.febslet.2008.09.051
57
Wang, G., Mao, W., Zheng, S., and Ye, J. (2009). Epidermal growth factor receptor-regulated miR-125a-5p—a metastatic inhibitor of lung cancer. FEBS J 276, 5571-5578 . doi: 10.1111/j.1742-4658.2009.07238.x
58
Wang, X., Hu, G., and Zhou, J. (2010b). Repression of versican expression by microRNA-143. J Biol Chem 285, 23241-23250 . doi: 10.1074/jbc.M109.084673
59
Xia, H., Qi, Y., Ng, S.S., Chen, X., Li, D., Chen, S., Ge, R., Jiang, S., Li, G., Chen, Y., . (2009). microRNA-146b inhibits glioma cell migration and invasion by targeting MMPs. Brain Res 1269, 158-165 . doi: 10.1016/j.brainres.2009.02.037
60
Yan, D., Dong, X.E., Chen, X., Wang, L., Lu, C., Wang, J., Qu, J., and Tu, L. (2009). MicroRNA-1/206 targets c-Met and inhibits rhabdomyosarcoma development. J Biol Chem 284, 29596-29604 . doi: 10.1074/jbc.M109.020511
61
Yao, J., Liang, L., Huang, S., Ding, J., Tan, N., Zhao, Y., Yan, M., Ge, C., Zhang, Z., Chen, T., . (2010). MicroRNA-30d promotes tumor invasion and metastasis by targeting Galphai2 in hepatocellular carcinoma. Hepatology 51, 846-856 .
62
Yu, Z., Willmarth, N.E., Zhou, J., Katiyar, S., Wang, M., Liu, Y., McCue, P.A., Quong, A.A., Lisanti, M.P., and Pestell, R.G. (2010). microRNA 17/20 inhibits cellular invasion and tumor metastasis in breast cancer by heterotypic signaling. Proc Natl Acad Sci U S A 107, 8231-8236 . doi: 10.1073/pnas.1002080107
63
Zhang, X., Liu, S., Hu, T., Liu, S., He, Y., and Sun, S. (2009). Up-regulated microRNA-143 transcribed by nuclear factor kappa B enhances hepatocarcinoma metastasis by repressing fibronectin expression. Hepatology 50, 490-499 . doi: 10.1002/hep.23008