Combinatorial control of mRNA fates by RNA-binding proteins and non-coding RNAs

Biomolecules

Volumn 5, Issue 4, 2015, Pages 2207-2222

  Iadevaia, Valentina ^a   Gerber, André P ^a  

^a UNIVERSITY OF SURREY   (United Kingdom)

Author keywords

Combinatorial control; Gene expression; MicroRNA; Post transcriptional control; Ribonucleoprotein complex; RNA binding protein

Indexed keywords

AMINO ACID TRANSPORTER; BETA TRANSDUCIN REPEAT CONTAINING PROTEIN; CAP BINDING PROTEIN; FRAGILE X MENTAL RETARDATION PROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN D; HYPOXIA INDUCIBLE FACTOR 2ALPHA; INITIATION FACTOR 4E; MESSENGER RNA; MICRORNA 101; MICRORNA 122; MICRORNA 144; MICRORNA 16; MICRORNA 221; MICRORNA 297; MICRORNA 299; MICRORNA 300; MICRORNA 376C; MICRORNA 385 5P; MICRORNA 410; MICRORNA 506; MICRORNA 567; MICRORNA 609; MYC PROTEIN; RNA BINDING PROTEIN; TRANSCRIPTION FACTOR E2F3; TRISTETRAPROLIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNTRANSLATED RNA; VASCULOTROPIN A; ZINC FINGER PROTEIN;

3' UNTRANSLATED REGION; CELL PROLIFERATION; DOWN REGULATION; GENE EXPRESSION; HUMAN; IMMUNOPRECIPITATION; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; GENETICS;

ANIMALS; HUMANS; RNA, MESSENGER; RNA, UNTRANSLATED; RNA-BINDING PROTEINS;

EID: 85012098139     PISSN: None     EISSN: 2218273X     Source Type: Journal    
DOI: 10.3390/biom5042207     Document Type: Review

References (87)

1. Cooper, T.A.; Wan, L.; Dreyfuss, G. RNA and disease. Cell 2009, 136, 777–793.
2. Castello, A.; Fischer, B.; Hentze, M.W.; Preiss, T. RNA-binding proteins in Mendelian disease. Trends Genet. 2013, 29, 318–327.
3. Wurth, L.; Gebauer, F. RNA-binding proteins, multifaceted translational regulators in cancer. Biochim. Biophys. Acta 2014, 1849, 881–886.
4. Mitchell, S.F.; Parker, R. Principles and properties of eukaryotic mRNPs. Mol. Cell 2014, 54, 547–558.
5. Gerstberger, S.; Hafner, M.; Tuschl, T. A census of human RNA-binding proteins. Nat. Rev. Genet. 2014, 15, 829–845.
6. Darnell, J.E., Jr. Reflections on the history of pre-mRNA processing and highlights of current knowledge: A unified picture. RNA 2013, 19, 443–460.
7. Johnston, D. Moving messages: The intracellular localization of mRNAs. Nat. Rev. Mol. Cell Biol. 2005, 6, 363–375.
8. Sonenberg, N.; Hinnebusch, A.G. Regulation of translation initiation in eukaryotes: Mechanisms and biological targets. Cell 2009, 136, 731–745.
9. Kishore, S.; Luber, S.; Zavolan, M. Deciphering the role of RNA-binding proteins in the post-transcriptional control of gene expression. Brief. Funct. Genomics 2010, 9, 391–404.
10. Imig, J.; Kanitz, A.; Gerber, A.P. RNA regulons and the RNA-protein interaction network. Biomol. Concepts 2012, 3, 403–414.
11. Cook, K.B.; Hughes, T.R.; Morris, Q.D. High-throughput characterization of protein-RNA interactions. Brief. Funct. Genomics 2015, 14, 74–89.
12. Tenenbaum, S.A.; Carson, C.C.; Lager, P.J.; Keene, J.D. Identifying mRNA subsets in messenger ribonucleoprotein complexes by using cDNA arrays. Proc. Natl. Acad. Sci. USA 2000, 97, 14085–14090.
13. Keene, J.D. RNA regulons: Coordination of post-transcriptional events. Nat. Rev. Genet. 2007, 8, 533–543.
14. Bartel, D.P. MicroRNAs: Target recognition and regulatory functions. Cell 2009, 136, 215–233.
15. Chekulaeva, M.; Filipowicz, W. Mechanisms of miRNA-mediated post-transcriptional regulation in animal cells. Curr. Opin. Cell Biol. 2009, 21, 452–460.
16. Kaboli, P.J.; Rahmat, A.; Ismail, P.; Ling, K.H. MicroRNA-based therapy and breast cancer: A comprehensive review of novel therapeutic strategies from diagnosis to treatment. Pharmacol. Res. 2015, 97, 104–121.
17. Adams, B.D.; Kasinski, A.L.; Slack, F.J. Aberrant regulation and function of microRNAs in cancer. Curr. Biol. 2014, 24, R762–R776.
18. Ha, M.; Kim, V.N. Regulation of microRNA biogenesis. Nat. Rev. Mol. Cell Biol. 2014, 15, 509–524.
19. Agami, R. MicroRNAs, RNA binding proteins and cancer. Eur. J. Clin. Invest. 2010, 40, 370–374.
20. Eom, T.; Muslimov, I.A.; Tsokas, P.; Berardi, V.; Zhong, J.; Sacktor, T.C.; Tiedge, H. Neuronal BC RNAs cooperate with eIF4B to mediate activity-dependent translational control. J. Cell Biol. 2014, 207, 237–252.
21. Kozomara, A.; Griffiths-Jones, S. MiRBase: Annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 2014, 42, D68–D73.
22. Jiang, P.; Singh, M.; Coller, H.A. Computational assessment of the cooperativity between RNA binding proteins and microRNAs in Transcript Decay. PLoS Comput. Biol. 2013, 9, e1003075.
23. Van Kouwenhove, M.; Kedde, M.; Agami, R. MicroRNA regulation by RNA-binding proteins and its implications for cancer. Nat. Rev. Cancer 2011, 11, 644–656.
24. Jiang, P.; Coller, H. Functional interactions between microRNAs and RNA binding proteins. MicroRNA 2012, 1, 70–79.
25. Ciafre, S.A.; Galardi, S. MicroRNAs and RNA-binding proteins: A complex network of interactions and reciprocal regulations in cancer. RNA Biol. 2013, 10, 935–942.
26. Srikantan, S.; Tominaga, K.; Gorospe, M. Functional interplay between RNA-binding protein HuR and microRNAs. Curr. Protein Pept. Sci. 2012, 13, 372–379.
27. De Silanes, I.L.; Lal, A.; Gorospe, M. HuR: Post-transcriptional paths to malignancy. RNA Biol. 2005, 2, 11–13.
28. Saunus, J.M.; French, J.D.; Edwards, S.L.; Beveridge, D.J.; Hatchell, E.C.; Wagner, S.A.; Stein, S.R.; Davidson, A.; Simpson, K.J.; Francis, G.D et al. Posttranscriptional regulation of the breast cancer susceptibility gene BRCA1 by the RNA binding protein HuR. Cancer Res. 2008, 68, 9469–9478.
29. Erkinheimo, T.L.; Lassus, H.; Sivula, A.; Sengupta, S.; Furneaux, H.; Hla, T.; Haglund, C.; Butzow, R.; Ristimaki, A. Cytoplasmic HuR expression correlates with poor outcome and with cyclooxygenase 2 expression in serous ovarian carcinoma. Cancer Res. 2003, 63, 7591–7594.
30. Lim, S.J.; Lee, S.H.; Joo, S.H.; Song, J.Y.; Choi, S.I. Cytoplasmic expression of HuR is related to cyclooxygenase-2 expression in colon cancer. Cancer Res. Treat. 2009, 41, 87–92.
31. Wang, J.; Wang, B.; Bi, J.; Zhang, C. Cytoplasmic HuR expression correlates with angiogenesis, lymphangiogenesis, and poor outcome in lung cancer. Med. Oncol. 2011, 28, 577–585.
32. Epis, M.R.; Barker, A.; Giles, K.M.; Beveridge, D.J.; Leedman, P.J. The RNA-binding protein HuR opposes the repression of ERBB-2 gene expression by microRNA miR-331–3p in prostate cancer cells. J. Biol. Chem. 2011, 286, 41442–41454.
33. Stoppoloni, D.; Cardillo, I.; Verdina, A.; Vincenzi, B.; Menegozzo, S.; Santini, M.; Sacchi, A.; Baldi, A.; Galati, R. Expression of the embryonic lethal abnormal vision-like protein HuR in human mesothelioma: Association with cyclooxygenase-2 and prognosis. Cancer 2008, 113, 2761–2769.
34. Wang, J.; Guo, Y.; Chu, H.; Guan, Y.; Bi, J.; Wang, B. Multiple Functions of the RNA-Binding Protein HuR in Cancer Progression, Treatment Responses and Prognosis. Int. J. Mol. Sci. 2013, 14, 10015–10041.
35. Bhattacharyya, S.N.; Habermacher, R.; Martine, U.; Closs, E.I.; Filipowicz, W. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 2006, 125, 1111–1124.
36. Young, L.E.; Moore, A.E.; Sokol, L.; Meisner-Kober, N.; Dixon, D.A. The mRNA stability factor HuR inhibits microRNA-16 targeting of COX-2. Mol. Cancer Res. 2012, 10, 167–180.
37. Ng, K.; Meyerhardt, J.A.; Chan, A.T.; Sato, K.; Chan, J.A.; Niedzwiecki, D.; Saltz, L.B.; Mayer, R.J.; Benson, A.B., 3rd; Schaefer, P.L et al. Aspirin and COX-2 inhibitor use in patients with stage III colon cancer. J. Natl. Cancer Inst. 2015, doi:10.1093/jnci/dju345.
38. 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 et al. RNA-binding protein Dnd1 inhibits microRNA access to target mRNA. Cell 2007, 131, 1273–1286.
39. Elcheva, I.; Goswami, S.; Noubissi, F.K.; Spiegelman, V.S. CRD-BP protects the coding region of betaTrCP1 mRNA from miR-183-mediated degradation. Mol. Cell 2009, 35, 240–246.
40. Kim, H.H.; Kuwano, Y.; Srikantan, S.; Lee, E.K.; Martindale, J.L.; Gorospe, M. HuR recruits let-7/RISC to repress c-Myc expression. Genes Dev. 2009, 23, 1743–1748.
41. Kedde, M.; van Kouwenhove, M.; Zwart, W.; Vrielink, J.A.F.O.; Elkon, R.; Agami, R. A Pumilio-induced RNA structure switch in p27-3' UTR controls miR-221 and miR-222 accessibility. Nat. Cell Biol. 2010, 12, 1014–1020.
42. Miles, W.O.; Tschop, K.; Herr, A.; Ji, J.Y.; Dyson, N.J. Pumilio facilitates miRNA regulation of the E2F3 oncogene. Genes Dev. 2012, 26, 356–368.
43. Xue, Y.; Ouyang, K.; Huang, J.; Zhou, Y.; Ouyang, H.; Li, H.; Wang, G.; Wu, Q.; Wei, C.; Bi, Y et al. Direct conversion of fibroblasts to neurons by reprogramming PTB-regulated microRNA circuits. Cell 2013, 152, 82–96.
44. Kenny, P.J.; Zhou, H.; Kim, M.; Skariah, G.; Khetani, R.S.; Drnevich, J.; Arcila, M.L.; Kosik, K.S.; Ceman, S. MOV10 and FMRP regulate AGO2 association with microRNA recognition elements. Cell Rep. 2014, 9, 1729–1741.
45. Maurin, T.; Zongaro, S.; Bardoni, B. Fragile X Syndrome: From molecular pathology to therapy. Neurosci. Biobehav. Rev. 2014, 46, 242–255.
46. Jacobsen, A.; Wen, J.; Marks, D.S.; Krogh, A. Signatures of RNA binding proteins globally coupled to effective microRNA target sites. Genome Res. 2010, 20, 1010–1019.
47. Galgano, A.; Forrer, M.; Jaskiewicz, L.; Kanitz, A.; Zavolan, M.; Gerber, A.P. Comparative analysis of mRNA targets for human PUF-family proteins suggests extensive interaction with the miRNA regulatory system. PLoS ONE 2008, 3, e3164.
48. Incarnato, D.; Neri, F.; Diamanti, D.; Oliviero, S. MREdictor: A two-step dynamic interaction model that accounts for mRNA accessibility and Pumilio binding accurately predicts microRNA targets. Nucleic Acids Res. 2013, 41, 8421–8433.
49. Mukherjee, N.; Corcoran, D.L.; Nusbaum, J.D.; Reid, D.W.; Georgiev, S.; Hafner, M.; Ascano, M., Jr.; Tuschl, T.; Ohler, U.; Keene, J.D. Integrative regulatory mapping indicates that the RNA-binding protein HuR couples pre-mRNA processing and mRNA stability. Mol. Cell 2011, 43, 327–339.
50. Doyle, F.; Tenenbaum, S.A. Trans-regulation of RNA-binding protein motifs by microRNA. Front. Genet. 2014, doi:10.3389/fgene.2014.00079.
51. Sugimoto, Y.; Vigilante, A.; Darbo, E.; Zirra, A.; Militti, C.; D’Ambrogio, A.; Luscombe, N.M.; Ule, J. hiCLIP reveals the in vivo atlas of mRNA secondary structures recognized by Staufen 1. Nature 2015, 519, 491–494.
52. Pandit, S.; Zhou, Y.; Shiue, L.; Coutinho-Mansfield, G.; Li, H.; Qiu, J.; Huang, J.; Yeo, G.W.; Ares, M., Jr.; Fu, X.D. Genome-wide analysis reveals SR protein cooperation and competition in regulated splicing. Mol. Cell 2013, 50, 223–235.
53. Zarnack, K.; Konig, J.; Tajnik, M.; Martincorena, I.; Eustermann, S.; Stevant, I.; Reyes, A.; Anders, S.; Luscombe, N.M.; Ule, J. Direct competition between hnRNP C and U2AF65 protects the transcriptome from the exonization of Alu elements. Cell 2013, 152, 453–466.
54. Fu, X.D.; Ares, M. Jr. Context-dependent control of alternative splicing by RNA-binding proteins. Nat. Rev. Genet. 2014, 15, 689–701.
55. Topisirovic, I.; Siddiqui, N.; Orolicki, S.; Skrabanek, L.A.; Tremblay, M.; Hoang, T.; Borden, K.L. Stability of eukaryotic translation initiation factor 4E mRNA is regulated by HuR, and this activity is dysregulated in cancer. Mol. Cell. Biol. 2009, 29, 1152–1162.
56. Tiedje, C.; Ronkina, N.; Tehrani, M.; Dhamija, S.; Laass, K.; Holtmann, H.; Kotlyarov, A.; Gaestel, M. The p38/MK2-driven exchange between tristetraprolin and HuR regulates AU-rich element-dependent translation. PLoS Genet. 2012, 8, e1002977.
57. Liu, L.; Ouyang, M.; Rao, J.N.; Zou, T.; Xiao, L.; Chung, H.K.; Wu, J.; Donahue, J.M.; Gorospe, M.; Wang, J.Y. Competition between RNA-binding proteins CELF1 and HuR modulates MYC translation and intestinal epithelium renewal. Mol. Biol. Cell 2015, 26, 1797–1810.
58. Mukherjee, N.; Jacobs, N.C.; Hafner, M.; Kennington, E.A.; Nusbaum, J.D.; Tuschl, T.; Blackshear, P.J.; Ohler, U. Global target mRNA specification and regulation by the RNA-binding protein ZFP36. Genome Biol. 2014, doi:10.1186/gb-2014-15-1-r12.
59. Nakamura, H.; Kawagishi, H.; Watanabe, A.; Sugimoto, K.; Maruyama, M.; Sugimoto, M. Cooperative role of the RNA-binding proteins Hzf and HuR in p53 activation. Mol. Cell. Biol. 2011, 31, 1997–2009.
60. Ray, P.S.; Jia, J.; Yao, P.; Majumder, M.; Hatzoglou, M.; Fox, P.L. A stress-responsive RNA switch regulates VEGFA expression. Nature 2009, 457, 915–919.
61. Jafarifar, F.; Yao, P.; Eswarappa, S.M.; Fox, P.L. Repression of VEGFA by CA-rich element-binding microRNAs is modulated by hnRNP L. EMBO J. 2011, 30, 1324–1334.
62. Goldberg-Cohen, I.; Furneauxb, H.; Levy, A.P. A 40-bp RNA element that mediates stabilization of vascular endothelial growth factor mRNA by HuR. J. Biol. Chem. 2002, 277, 13635–13640.
63. Yao, P.; Potdar, A.A.; Ray, P.S.; Eswarappa, S.M.; Flagg, A.C.; Willard, B.; Fox, P.L. The HILDA complex coordinates a conditional switch in the 3'-untranslated region of the VEGFA mRNA. PLoS Biol. 2013, 11, e1001635.
64. Pelletier, J.; Graff, J.; Ruggero, D.; Sonenberg, N. Targeting the eIF4F translation initiation complex: A critical nexus for cancer development. Cancer Res. 2015, 75, 250–263.
65. Uniacke, J.; Holterman, C.E.; Lachance, G.; Franovic, A.; Jacob, M.D.; Fabian, M.R.; Payette, J.; Holcik, M.; Pause, A.; Lee, S. An oxygen-regulated switch in the protein synthesis machinery. Nature 2012, 486, 126–129.
66. Poliseno, L.; Salmena, L.; Riccardi, L.; Fornari, A.; Song, M.S.; Hobbs, R.M.; Sportoletti, P.; Varmeh, S.; Egia, A.; Fedele, G.; et al. Identification of the miR-106b~25 microRNA cluster as a proto-oncogenic PTEN-targeting intron that cooperates with its host gene MCM7 in transformation. Sci. Signal. 2010, doi:10.1126/scisignal.2000594.
67. Chang, S.; Sharan, S.K. BRCA1 and microRNAs: Emerging networks and potential therapeutic targets. Mol. Cells 2012, 34, 425–432.
68. Shenoy, A.; Danial, M.; Blelloch, R.H. Let-7 and miR-125 cooperate to prime progenitors for astrogliogenesis. EMBO J. 2015, 34, 1180–1194.
69. Huang, Q.; Gumireddy, K.; Schrier, M.; le Sage, C.; Nagel, R.; Nair, S.; Egan, D.A.; Li, A.; Huang, G.; Klein-Szanto, A.J et al. The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nat. Cell Biol. 2008, 10, 202–210.
70. Brown, K.K.; Toker, A. The phosphoinositide 3-kinase pathway and therapy resistance in cancer. F1000Prime Rep. 2015, doi:10.12703/P7-13.
71. Yu, J.; Ryan, D.G.; Getsios, S.; Oliveira-Fernandes, M.; Fatima, A.; Lavker, R.M. MicroRNA-184 antagonizes microRNA-205 to maintain SHIP2 levels in epithelia. Proc. Natl. Acad. Sci. USA 2008, 105, 19300–19305.
72. Cook, K.B.; Kazan, H.; Zuberi, K.; Morris, Q.; Hughes, T.R. RBPDB: A database of RNA-binding specificities. Nucleic Acids Res. 2011, 39, D301–D308.
73. A Database of RNA-Binding Specificities. Available online: http://rbpdb.ccbr.utoronto.ca (accessed on 14 September 2015).
74. Ray, D.; Kazan, H.; Cook, K.B.; Weirauch, M.T.; Najafabadi, H.S.; Li, X.; Gueroussov, S.; Albu, M.; Zheng, H.; Yang, A.; et al. A compendium of RNA-binding motifs for decoding gene regulation. Nature 2013, 499, 172–177.
75. CIS-BP-RNA, the Online Library of RNA Binding Proteins and Their Motifs. Available online:http://cisbp-rna.ccbr.utoronto.ca (accessed on 14 September 2015).
76. Biswas, A.; Brown, C.M. Scan for motifs: A webserver for the analysis of post-transcriptional regulatory elements in the 3' untranslated regions (3' UTRs) of mRNAs. BMC Bioinform. 2014, doi:10.1186/1471-2105-15-174.
77. Scan for Motifs. Available online: http://bioanalysis.otago.ac.nz/sfm/sfm_main.pl (accessed on 14 September 2015).
78. Agarwal, V.; Bell, G.W.; Nam, J.W.; Bartel, D.P. Predicting effective microRNA target sites in mammalian mRNAs. Elife 2015, doi:10.7554/eLife.05005.
79. TargetScan. Available online: http://www.targetscan.org/ (accessed on 14 September 2015).
80. Yang, J.H.; Li, J.H.; Shao, P.; Zhou, H.; Chen, Y.Q.; Qu, L.H. StarBase: A database for exploring microRNA-mRNA interaction maps from Argonaute CLIP-Seq and Degradome-Seq data. Nucleic Acids Res. 2011, 39, D202–D209.
81. StarBase v2.0 CLIP-Seq, Pan-Cancer. Portal, Visualize, Analyze, Discover. Available online: http://starbase.sysu.edu.cn/ (accessed on 14 September 2015).
82. Chen, G.; Wang, Z.; Wang, D.; Qiu, C.; Liu, M.; Chen, X.; Zhang, Q.; Yan, G.; Cui, Q. LncRNADisease: A database for long-non-coding RNA-associated diseases. Nucleic Acids Res. 2013, 41, D983–D986.
83. The LncRNADisease Database. Available online: http://www.cuilab.cn/lncrnadisease (accessed on 14 September 2015).
84. Kanitz, A.; Gerber, A.P. Circuitry of mRNA regulation. Wiley Interdiscip. Rev. Syst. Biol. Med. 2010, 2, 245–251.
85. Pullmann, R., Jr.; Kim, H.H.; Abdelmohsen, K.; Lal, A.; Martindale, J.L.; Yang, X.; Gorospe, M. Analysis of turnover and translation regulatory RNA-binding protein expression through binding to cognate mRNAs. Mol. Cell. Biol. 2007, 27, 6265–6278.
86. Lin, S.; Gregory, R.I. MicroRNA biogenesis pathways in cancer. Nat. Rev. Cancer 2015, 15, 321–333.
87. Michlewski, G.; Caceres, J.F. Antagonistic role of hnRNP A1 and KSRP in the regulation of let-7a biogenesis. Nat. Struct. Mol. Biol. 2010, 17, 1011–1018.