Dosage and temporal thresholds in microRNA proteomics

Molecular and Cellular Proteomics

Volumn 14, Issue 2, 2015, Pages 289-302

  Lee, Thomas ^a   Wang, Nan ^a   Houel, Stephane ^a,b   Couts, Kasey ^a,c   Old, William ^a   Ahn, Natalie ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b WATERS CORPORATION   (United States)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MICRORNA; 3' UNTRANSLATED REGION;

3' UNTRANSLATED REGION; ARTICLE; BINDING SITE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; ENERGY; GENE DOSAGE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE REPRESSION; HUMAN; HUMAN CELL; ISOTOPE LABELING; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN RNA BINDING; PROTEOMICS; RNA RNA HYBRIDIZATION; RNA SEQUENCE; RNA STABILITY; STABLE ISOTOPE LABELING BY AMINO ACID IN CELL CULTURE; TRANSLATION REGULATION; ALGORITHM; GENETICS; KINETICS; METABOLISM; PROCEDURES; REPRODUCIBILITY; TIME; TUMOR CELL LINE;

3' UNTRANSLATED REGIONS; ALGORITHMS; CELL LINE, TUMOR; HUMANS; ISOTOPE LABELING; KINETICS; MICRORNAS; PROTEOMICS; REPRODUCIBILITY OF RESULTS; RNA, MESSENGER; TIME FACTORS;

EID: 84921918525     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M114.043851     Document Type: Article

References (66)

1. Bartel, D. P. (2009) MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233
2. Yi, R., Poy, M. N., Stoffel, M., and Fuchs, E. (2008) A skin microRNA promotes differentiation by repressing "stemness." Nature 452, 225-229
3. Chen, J.-F., Mandel, E. M., Thomson, J. M., Wu, Q., Callis, T. E., Hammond, S. M., Conlon, F. L., and Wang, D.-Z. (2006) The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat. Genet. 38, 228-233
4. Rottiers, V., and Nä ä r, A. M. (2012) MicroRNAs in metabolism and metabolic disorders. Nat. Rev. Mol. Cell Biol. 13, 239-250
5. Thum, T., Gross, C., Fiedler, J., Fischer, T., Kissler, S., Bussen, M., Galuppo, P., Just, S., Rottbauer, W., Frantz, S., Castoldi, M., Soutschek, J., Koteliansky, V., Rosenwald, A., Basson, M. A., Licht, J. D., Pena, J. T. R., Rouhanifard, S. H., Muckenthaler, M. U., Tuschl, T., Martin, G. R., Bauersachs, J., and Engelhardt, S. (2008) MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signaling in fibroblasts. Nature 456, 980-984
6. Carthew, R. W., and Sontheimer, E. J. (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136, 642-655
7. Huntzinger, E., and Izaurralde, E. (2011) Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat. Rev. Genet. 12, 99-110
8. Behm-Ansmant, I., Rehwinkel, J., Doerks, T., Stark, A., Bork, P., and Izaurralde, E. (2006) mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev. 20, 1885-1898
9. Fabian, M. R., Mathonnet, G., Sundermeier, T., Mathys, H., Zipprich, J. T., Svitkin, Y. V., Rivas, F., Jinek, M., Wohlschlegel, J., Doudna, J. A., Chen, C.-Y. A., Shyu, A.-B., Yates III, J. R., Hannon, G. J., Filipowicz, W., Duchaine, T. F., and Sonenberg, N. (2009) Mammalian miRNA RISC recruits CAF1 and PABP to affect PABP-dependent deadenylation. Mol. Cell 35, 868-880
10. Rehwinkel, J., Behm-Ansmant, I., Gatfield, D., and Izaurralde, E. (2005) A crucial role for GW182 and the DCP1:DCP2 decapping complex in miRNA-mediated gene silencing. RNA 11, 1640-1647
11. Chendrimada, T. P., Finn, K. J., Ji, X., Baillat, D., Gregory, R. I., Liebhaber, S. A., Pasquinelli, A. E., and Shiekhattar, R. (2007) MicroRNA silencing through RISC recruitment of eIF6. Nature 447, 823-828
12. Mukherji, S., Ebert, M. S., Zheng, G. X. Y., Tsang, J. S., Sharp, P. A., and van Oudenaarden, A. (2011) MicroRNAs can generate thresholds in target gene expression. Nat. Genet. 43, 854-859
13. Ebert, M. S., and Sharp, P. A. (2012) Roles for microRNAs in conferring robustness to biological processes. Cell 149, 515-524
14. Li, X., Cassidy, J. J., Reinke, C. A., Fischboeck, S., and Carthew, R. W. (2009) A microRNA imparts robustness against environmental fluctuation during development. Cell 137, 273-282
15. Stark, A., Brennecke, J., Bushati, N., Russell, R. B., and Cohen, S. M. (2005) Animal microRNAs confer robustness to gene expression and have a significant impact on 3-UTR evolution. Cell 123, 1133-1146
16. Enright, A. J., John, B., Gaul, U., Tuschl, T., Sander, C., and Marks, D. S. (2003) MicroRNA targets in Drosophila. Genome Biol. 5, R1
17. John, B., Enright, A. J., Aravin, A., Tuschl, T., Sander, C., and Marks, D. S. (2004) Human microRNA targets. PLoS Biol. 2, e363
18. Krek, A., Grü n, D., Poy, M. N., Wolf, R., Rosenberg, L., Epstein, E. J., MacMenamin, P., da Piedade, I., Gunsalus, K. C., Stoffel, M., and Rajewsky, N. (2005) Combinatorial microRNA target predictions. Nat. Genet. 37, 495-500
19. Grimson, A., Farh, K. K.-H., 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
20. Friedman, R. C., Farh, K. K.-H., Burge, C. B., and Bartel, D. P. (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19, 92-105
21. Kertesz, M., Iovino, N., Unnerstall, U., Gaul, U., and Segal, E. (2007) The role of site accessibility in microRNA target recognition. Nat. Genet. 39, 1278-1284
22. Johnson, C. D., Esquela-Kerscher, A., Stefani, G., Byrom, M., Kelnar, K., Ovcharenko, D., Wilson, M., Wang, X., Shelton, J., Shingara, J., Chin, L., Brown, D., and Slack, F. J. (2007) The let-7 microRNA represses cell proliferation pathways in human cells. Cancer Res. 67, 7713-7722
23. Jackson, A. L., Bartz, S. R., Schelter, J., Kobayashi, S. V., Burchard, J., Mao, M., Li, B., Cavet, G., and Linsley, P. S. (2003) Expression profiling reveals off-target gene regulation by RNAi. Nat. Biotechnol. 21, 635-637
24. Khan, A. A., Betel, D., Miller, M. L., Sander, C., Leslie, C. S., and Marks, D. S. (2009) Transfection of small RNAs globally perturbs gene regulation by endogenous microRNAs. Nat. Biotechnol. 27, 549-555
25. Ong, S.-E., Blagoev, B., Kratchmarova, I., Kristensen, D. B., Steen, H., Pandey, A., and Mann, M. (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1, 376-386
26. Ong, S.-E., and Mann, M. (2007) A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC). Nat. Protoc. 1, 2650-2660
27. Selbach, M., Schwanhä usser, B., Thierfelder, N., Fang, Z., Khanin, R., and Rajewsky, N. (2008) Widespread changes in protein synthesis induced by microRNAs. Nature 455, 58-63
28. Wioeniewski, J. R., Zougman, A., Nagaraj, N., and Mann, M. (2009) Universal sample preparation method for proteome analysis. Nat. Methods 6, 359-362
29. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
30. Kersey, P. J., Duarte, J., Williams, A., Karavidopoulou, Y., Birney, E., and Apweiler, R. (2004) The International Protein Index: an integrated database for proteomics experiments. Proteomics 4, 1985-1988
31. Cox, J., Matic, I., Hilger, M., Nagaraj, N., Selbach, M., Olsen, J. V., and Mann, M. (2009) A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat. Protoc. 4, 698-705
32. Schwanhä usser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., and Selbach, M. (2011) Global quantification of mammalian gene expression control. Nature 473, 337-342
33. Pruitt, K. D., Tatusova, T., and Maglott, D. R. (2005) NCBI Reference Sequence (RefSeq): a curated nonredundant sequence database of genomes, transcripts, and proteins. Nucleic Acids Res. 33, D501-D504
34. Betel, D., Koppal, A., Agius, P., Sander, C., and Leslie, C. (2010) Comprehensive modeling of microRNA targets predicts functional nonconserved and noncanonical sites. Genome Biol. 11, R90
35. Trapnell, C., Pachter, L., and Salzberg, S. L. (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111
36. Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., and Salzberg, S. L. (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions, and gene fusions. Genome Biol. 14, R36
37. Trapnell, C., Williams, B. A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M. J., Salzberg, S. L., Wold, B. J., and Pachter, L. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511-515
38. Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D. R., Pimentel, H., Salzberg, S. L., Rinn, J. L., and Pachter, L. (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562-578
39. Couts, K. L., Anderson, E. M., Gross, M. M., Sullivan, K., and Ahn, N. G. (2013) Oncogenic B-Raf signaling in melanoma cells controls a network of microRNAs with combinatorial functions. Oncogene 32, 1959-1970
40. Baek, D., Villé n, 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
41. Yang, Y., Chaerkady, R., Beer, M. A., Mendell, J. T., and Pandey, A. (2009) Identification of miR-21 targets in breast cancer cells using a quantitative proteomic approach. Proteomics 9, 1374-1384
42. Chen, Q.-R., Yu, L.-R., Tsang, P., Wei, J. S., Song, Y. K., Cheuk, A., Chung, J.-Y., Hewitt, S. M., Veenstra, T. D., and Khan, J. (2011) Systematic proteome analysis identifies transcription factor YY1 as a direct target of miR-34a. J. Proteome Res. 10, 479-487
43. Leivonen, S.-K., Rokka, A., Ö stling, P., Kohonen, P., Corthals, G. L., Kallioniemi, O., and Perä lä, M. (2011) Identification of miR-193b targets in breast cancer cells and systems biological analysis of their functional impact. Mol. Cell. Proteomics 10, M110.005322
44. Kaller, M., Liffers, S.-T., Oeljeklaus, S., Kuhlmann, K., Rö h, S., Hoffmann, R., Warscheid, B., and Hermeking, H. (2011) Genome-wide characterization of miR-34a induced changes in protein and mrna expression by a combined pulsed SILAC and microarray analysis. Mol. Cell. Proteomics 10, M111.010462
45. 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
46. 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
47. Raymond, C. K., Roberts, B. S., Garrett-Engele, P., Lim, L. P., and Johnson, J. M. (2005) Simple, quantitative primer-extension PCR assay for direct monitoring of microRNAs and short-interfering RNAs. RNA 11, 1737-1744
48. Schmittgen, T. D., Lee, E. J., Jiang, J., Sarkar, A., Yang, L., Elton, T. S., and Chen, C. (2008) Real-time PCR quantification of precursor and mature microRNA. Methods 44, 31-38
49. Bhattacharyya, S. N., Habermacher, R., Martine, U., Closs, E. I., and Filipowicz, W. (2006) Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125, 1111-1124
50. Goswami, S., Tarapore, R. S., TeSlaa, J. J., Grinblat, Y., Setaluri, V., and Spiegelman, V. S. (2010) MicroRNA-340-mediated degradation of microphthalmia-associated transcription factor mRNA is inhibited by the coding region determinant-binding protein. J. Biol. Chem. 285, 20532-20540
51. Jafarifar, F., Yao, P., Eswarappa, S. M., and Fox, P. L. (2011) Repression of VEGFA by CA-rich element-binding microRNAs is modulated by hnRNP L. EMBO J. 30, 1324-1334
52. Kedde, M., Strasser, M. J., Boldajipour, B., Vrielink, J. A. F. O., Slanchev, K., le Sage, C., Nagel, R., Voorhoeve, P. M., van Duijse, J., \Orom, U. A., Lund, A. H., Perrakis, A., Raz, E., and Agami, R. (2007) RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell 131, 1273-1286
53. Kundu, P., Fabian, M. R., Sonenberg, N., Bhattacharyya, S. N., and Filipowicz, W. (2012) HuR protein attenuates miRNA-mediated repression by promoting miRISC dissociation from the target RNA. Nucleic Acids Res. 40, 5088-5100
54. Mukherjee, N., Corcoran, D. L., Nusbaum, J. D., Reid, D. W., Georgiev, S., Hafner, M., Ascano Jr., M., Tuschl, T., Ohler, U., and Keene, J. D. (2011) Integrative regulatory mapping indicates that the RNA-binding protein HuR couples pre-mRNA processing and mRNA stability. Mol. Cell 43, 327-339
55. Hansen, T. B., Jensen, T. I., Clausen, B. H., Bramsen, J. B., Finsen, B., Damgaard, C. K., and Kjems, J. (2013) Natural RNA circles function as efficient microRNA sponges. Nature 495, 384-388
56. Poliseno, L., Salmena, L., Zhang, J., Carver, B., Haveman, W. J., and Pandolfi, P. P. (2010) A coding-independent function of gene and pseudogene mRNAs regulates tumor biology. Nature 465, 1033-1038
57. Fabian, M. R., Sonenberg, N., and Filipowicz, W. (2010) Regulation of mRNA translation and stability by microRNAs. Annu. Rev. Biochem. 79, 351-379
58. Djuranovic, S., Nahvi, A., and Green, R. (2012) miRNA-mediated gene silencing by translational repression followed by mRNA deadenylation and decay. Science 336, 237-240
59. Bazzini, A. A., Lee, M. T., and Giraldez, A. J. (2012) Ribosome profiling shows that miR-430 reduces translation before causing mRNA decay in zebrafish. Science 336, 233-237
60. Baccarini, A., Chauhan, H., Gardner, T. J., Jayaprakash, A. D., Sachidanandam, R., and Brown, B. D. (2011) Kinetic analysis reveals the fate of a microRNA following target regulation in mammalian cells. Curr. Biol. 21, 369-376
61. Gantier, M. P., McCoy, C. E., Rusinova, I., Saulep, D., Wang, D., Xu, D., Irving, A. T., Behlke, M. A., Hertzog, P. J., Mackay, F., and Williams, B. R. G. (2011) Analysis of microRNA turnover in mammalian cells following Dicer1 ablation. Nucleic Acids Res. 39, 5692-5703
62. Rü egger, S., and Gro-hans, H. (2012) MicroRNA turnover: when, how, and why. Trends Biochem. Sci. 37, 436-446
63. Asangani, I. A., Rasheed, S. a. K., Nikolova, D. A., Leupold, J. H., Colburn, N. H., Post, S., and Allgayer, H. (2007) MicroRNA-21 (miR-21) posttranscriptionally down-regulates tumor suppressor Pdcd4 and stimulates invasion, intravasation, and metastasis in colorectal cancer. Oncogene 27, 2128-2136
64. Liang, X., Zhou, D., Wei, C., Luo, H., Liu, J., Fu, R., and Cui, S. (2012) MicroRNA-34c enhances murine male germ cell apoptosis through targeting ATF1. PLoS One 7, e33861
65. Schotte, D., Chau, J. C. K., Sylvester, G., Liu, G., Chen, C., van der Velden, V. H. J., Broekhuis, M. J. C., Peters, T. C. J. M., Pieters, R., and Boer, M. L. den (2008) Identification of new microRNA genes and aberrant microRNA profiles in childhood acute lymphoblastic. Leukemia 23, 313-322
66. Bousquet, M., Harris, M. H., Zhou, B., and Lodish, H. F. (2010) MicroRNA miR-125b causes leukemia. Proc. Natl. Acad. Sci. 107, 21558-21563