Integrative omics analysis reveals the importance and scope of translational repression in microRNA-mediated regulation

Molecular and Cellular Proteomics

Volumn 12, Issue 7, 2013, Pages 1900-1911

  Liu, Qi ^a   Halvey, Patrick J ^a   Shyr, Yu ^a,b   Slebos, Robbert J C ^a,b   Liebler, Daniel C ^a,b   Zhang, Bing ^a,b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT INGRAM CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MICRORNA; TRANSCRIPTOME;

3' UNTRANSLATED REGION; ARTICLE; AU RICH ELEMENT; BASE PAIRING; COLORECTAL CANCER; GENE EXPRESSION; GENE REPRESSION; GENE SEQUENCE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEOMICS; REGULATORY MECHANISM; RNA TRANSLATION; GENE EXPRESSION REGULATION; GENETICS; TUMOR CELL LINE;

CELL LINE, TUMOR; GENE EXPRESSION REGULATION; HUMANS; MICRORNAS; PROTEOMICS; RNA, MESSENGER; TRANSCRIPTOME;

EID: 84880063582     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.025783     Document Type: Article

References (50)

1. Bartel, D. P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297
2. Baek, D., Villén, J., Shin, C., Camargo, F. D., Gygi, S. P., and Bartel, D. P. (2008) The impact of microRNAs on protein output. Nature 455, 64-71
3. Selbach, M., Schwanháusser, B., Thierfelder, N., Fang, Z., Khanin, R., and Rajewsky, N. (2008) Widespread changes in protein synthesis induced by microRNAs. Nature 455, 58-63
4. Farh, K. K., Grimson, A., Jan, C., Lewis, B. P., Johnston, W. K., Lim, L. P., Burge, C. B., and Bartel, D. P. (2005) The widespread impact of mammalian MicroRNAs on mRNA repression and evolution. Science 310, 1817-1821 (Pubitemid 41814382)
5. 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
6. Olsen, P. H., and Ambros, V. (1999) The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev. Biol. 216, 671-680 (Pubitemid 30013313)
7. Zeng, Y., Wagner, E. J., and Cullen, B. R. (2002) Both natural and designed micro RNAs can inhibit the expression of cognate mRNAs when expressed in human cells. Mol. Cell 9, 1327-1333 (Pubitemid 34722311)
8. Guo, H., Ingolia, N. T., Weissman, J. S., and Bartel, D. P. (2010) Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466, 835-840
9. Hendrickson, D. G., Hogan, D. J., McCullough, H. L., Myers, J. W., Herschlag, D., Ferrell, J. E., and Brown, P. O. (2009) Concordant regulation of translation and mRNA abundance for hundreds of targets of a human microRNA. PLoS Biol 7, e1000238
10. Grimson, A., Farh, K. K., Johnston, W. K., Garrett-Engele, P., Lim, L. P., and Bartel, D. P. (2007) MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell 27, 91-105 (Pubitemid 46991392)
11. Nielsen, C. B., Shomron, N., Sandberg, R., Hornstein, E., Kitzman, J., and Burge, C. B. (2007) Determinants of targeting by endogenous and exogenous microRNAs and siRNAs. RNA 13, 1894-1910 (Pubitemid 350005216)
12. Huang, G. T., Athanassiou, C., and Benos, P. V. (2011) mirConnX: condition-specific mRNA-microRNA network integrator. Nucleic Acids Res. 39, W416-423
13. Huang, J. C., Babak, T., Corson, T. W., Chua, G., Khan, S., Gallie, B. L., Hughes, T. R., Blencowe, B. J., Frey, B. J., and Morris, Q. D. (2007) Using expression profiling data to identify human microRNA targets. Nat. Methods 4, 1045-1049 (Pubitemid 350201777)
14. Jayaswal, V., Lutherborrow, M., Ma, D. D., and Hwa Yang, Y. (2009) Identification of microRNAs with regulatory potential using a matched microRNA-mRNA time-course data. Nucleic Acids Res. 37, e60
15. Volinia, S., Visone, R., Galasso, M., Rossi, E., and Croce, C. M. (2010) Identification of microRNA activity by Targets' Reverse EXpression. Bioinformatics 26, 91-97
16. Wang, Y. P., and Li, K. B. (2009) Correlation of expression profiles between microRNAs and mRNA targets using NCI-60 data. BMC Genomics 10, 218
17. Sprung, R. W., Jr., Brock, J. W., Tanksley, J. P., Li, M., Washington, M. K., Slebos, R. J., and Liebler, D. C. (2009) Equivalence of protein inventories obtained from formalin-fixed paraffin-embedded and frozen tissue in multidimensional liquid chromatography-tandem mass spectrometry shotgun proteomic analysis. Mol. Cell. Proteomics 8, 1988-1998
18. Tabb, D. L., Fernando, C. G., and Chambers, M. C. (2007) MyriMatch: highly accurate tandem mass spectral peptide identification by multivariate hypergeometric analysis. J. Proteome Res. 6, 654-661 (Pubitemid 46340169)
19. Zhang, B., Chambers, M. C., and Tabb, D. L. (2007) Proteomic parsimony through bipartite graph analysis improves accuracy and transparency. J. Proteome Res. 6, 3549-3557 (Pubitemid 47522746)
20. Ma, Z. Q., Dasari, S., Chambers, M. C., Litton, M. D., Sobecki, S. M., Zimmerman, L. J., Halvey, P. J., Schilling, B., Drake, P. M., Gibson, B. W., and Tabb, D. L. (2009) IDPicker 2.0: Improved protein assembly with high discrimination peptide identification filtering. J. Proteome Res. 8, 3872-3881
21. Elias, J. E., Haas, W., Faherty, B. K., and Gygi, S. P. (2005) Comparative evaluation of mass spectrometry platforms used in large-scale proteomics investigations. Nat. Methods 2, 667-675 (Pubitemid 41223093)
22. Halvey, P. J., Zhang, B., Coffey, R., Liebler, D. C., and Slebos, R. J. (2011) Proteomic Consequences of a Single Gene Mutation in a Colorectal Cancer Model. J. Proteome Res. 11, 1184-1195
23. Kislinger, T., Cox, B., Kannan, A., Chung, C., Hu, P., Ignatchenko, A., Scott, M. S., Gramolini, A. O., Morris, Q., Hallett, M. T., Rossant, J., Hughes, T. R., Frey, B., and Emili, A. (2006) Global survey of organ and organelle protein expression in mouse: combined proteomic and transcriptomic profiling. Cell 125, 173-186
24. Zhang, B., VerBerkmoes, N. C., Langston, M. A., Uberbacher, E., Hettich, R. L., and Samatova, N. F. (2006) Detecting differential and correlated protein expression in label-free shotgun proteomics. J. Proteome Res. 5, 2909-2918 (Pubitemid 44749209)
25. Li, M., Gray, W., Zhang, H., Chung, C. H., Billheimer, D., Yarbrough, W. G., Liebler, D. C., Shyr, Y., and Slebos, R. J. (2010) Comparative shotgun proteomics using spectral count data and quasi-likelihood modeling. J. Proteome Res. 9, 4295-4305
26. Ning, K., Fermin, D., and Nesvizhskii, A. I. (2012) Comparative analysis of different label-free mass spectrometry based protein abundance estimates and their correlation with RNA-Seq gene expression data. J. Proteome Res. 11, 2261-2271
27. Vogel, C., Abreu Rde, S., Ko, D., Le, S. Y., Shapiro, B. A., Burns, S. C., Sandhu, D., Boutz, D. R., Marcotte, E. M., and Penalva, L. O. (2010) Sequence signatures and mRNA concentration can explain two-thirds of protein abundance variation in a human cell line. Mol. Syst. Biol. 6, 400
28. de Sousa Abreu, R., Penalva, L. O., Marcotte, E. M., and Vogel, C. (2009) Global signatures of protein and mRNA expression levels. Mol. Biosyst. 5, 1512-1526
29. Lewis, B. P., Burge, C. B., and Bartel, D. P. (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15-20 (Pubitemid 40094598)
30. Lewis, B. P., Shih, I. H., Jones-Rhoades, M. W., Bartel, D. P., and Burge, C. B. (2003) Prediction of mammalian microRNA targets. Cell 115, 787-798 (Pubitemid 38058492)
31. John, B., Enright, A. J., Aravin, A., Tuschl, T., Sander, C., and Marks, D. S. (2004) Human MicroRNA targets. PLoS Biol. 2, e363
32. Wang, X., and El Naqa, I. M. (2008) Prediction of both conserved and nonconserved microRNA targets in animals. Bioinformatics 24, 325-332 (Pubitemid 351189007)
33. Durinck, S., Spellman, P. T., Birney, E., and Huber, W. (2009) Mapping identifiers for the integration of genomic datasets with the R/Bioconductor package biomaRt. Nat. Protoc. 4, 1184-1191
34. Durinck, S., Moreau, Y., Kasprzyk, A., Davis, S., De Moor, B., Brazma, A., and Huber, W. (2005) BioMart and Bioconductor: a powerful link between biological databases and microarray data analysis. Bioinformatics 21, 3439-3440 (Pubitemid 41222455)
35. Bartel, D. P. (2009) MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233
36. 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 (Pubitemid 40292988)
37. Siegel, G., Obernosterer, G., Fiore, R., Oehmen, M., Bicker, S., Christensen, M., Khudayberdiev, S., Leuschner, P. F., Busch, C. J., Kane, C., Hübel, K., Dekker, F., Hedberg, C., Rengarajan, B., Drepper, C., Waldmann, H., Kauppinen, S., Greenberg, M. E., Draguhn, A., Rehmsmeier, M., Martinez, J., and Schratt, G. M. (2009) A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. Nat. Cell Biol. 11, 705-716
38. 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
39. 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
40. Burk, U., Schubert, J., Wellner, U., Schmalhofer, O., Vincan, E., Spaderna, S., and Brabletz, T. (2008) A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 9, 582-589 (Pubitemid 351772923)
41. Gregory, P. A., Bert, A. G., Paterson, E. L., Barry, S. C., Tsykin, A., Farshid, G., Vadas, M. A., Khew-Goodall, Y., and Goodall, G. J. (2008) The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 10, 593-601 (Pubitemid 351627379)
42. 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
43. Park, S. M., Gaur, A. B., Lengyel, E., and Peter, M. E. (2008) The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev. 22, 894-907 (Pubitemid 351482843)
44. Buck, E., Eyzaguirre, A., Barr, S., Thompson, S., Sennello, R., Young, D., Iwata, K. K., Gibson, N. W., Cagnoni, P., and Haley, J. D. (2007) Loss of homotypic cell adhesion by epithelial-mesenchymal transition or mutation limits sensitivity to epidermal growth factor receptor inhibition. Mol. Cancer Ther. 6, 532-541 (Pubitemid 46332455)
45. Loboda, A., Nebozhyn, M. V., Watters, J. W., Buser, C. A., Shaw, P. M., Huang, P. S., Van't Veer, L., Tollenaar, R. A., Jackson, D. B., Agrawal, D., Dai, H., and Yeatman, T. J. (2011) EMT is the dominant program in human colon cancer. BMC Med. Genomics 4, 9
46. Aleman, L. M., Doench, J., and Sharp, P. A. (2007) Comparison of siRNA-induced off-target RNA and protein effects. RNA, 2007/01/24 Ed., pp. 385-395
47. Valencia-Sanchez, M. A., Liu, J., Hannon, G. J., and Parker, R. (2006) Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev. 20, 515-524 (Pubitemid 43345317)
48. Okamura, K., Ishizuka, A., Siomi, H., and Siomi, M. C. (2004) Distinct roles for Argonaute proteins in small RNA-directed RNA cleavage pathways. Genes Dev. 18, 1655-1666 (Pubitemid 38938183)
49. Liu, J., Carmell, M. A., Rivas, F. V., Marsden, C. G., Thomson, J. M., Song, J. J., Hammond, S. M., Joshua-Tor, L., and Hannon, G. J. (2004) Argonaute2 is the catalytic engine of mammalian RNAi. Science 305, 1437-1441 (Pubitemid 39167657)
50. Grosshans, H., and Filipowicz, W. (2008) Proteomics joins the search for microRNA targets. Cell 134, 560-562