A post-transcriptional mechanism pacing expression of neural genes with precursor cell differentiation status

Nature Communications

Volumn 6, Issue , 2015, Pages

  Dai, Weijun ^a   Li, Wencheng ^b   Hoque, Mainul ^b   Li, Zhuyun ^a   Tian, Bin ^b   Makeyev, Eugene V ^a,c  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^c KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MICRORNA 9; TRANSCRIPTOME; TRISTETRAPROLIN; MICRORNA; MIRN9 MICRORNA, MOUSE; ZFP36 PROTEIN, MOUSE;

CELLS AND CELL COMPONENTS; GENE EXPRESSION; GENETIC DIFFERENTIATION; MOLECULAR ANALYSIS; NERVOUS SYSTEM; NEUROLOGY; PROTEIN; RNA;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; AU RICH ELEMENT; BRAIN DEVELOPMENT; CONTROLLED STUDY; DOWN REGULATION; FIBROBLAST; GENE EXPRESSION; GENETIC TRANSCRIPTION; MOUSE; NERVE CELL DIFFERENTIATION; NEUROBLASTOMA CELL; NONHUMAN; RNA DEGRADATION; STEADY STATE; STEM CELL; UPREGULATION; ANIMAL; CELL DIFFERENTIATION; CELL LINE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; NERVE CELL; PHYSIOLOGY; PLASMID; RNA PROCESSING;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; GENE EXPRESSION REGULATION; HUMANS; MICRORNAS; NEURONS; PLASMIDS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; STEM CELLS; TRISTETRAPROLIN; UP-REGULATION;

EID: 84936138862     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8576     Document Type: Article

References (63)

1. Glisovic, T., Bachorik, J. L., Yong, J. & Dreyfuss, G. RNA-binding proteins and post-transcriptional gene regulation. FEBS Lett. 582, 1977-1986 (2008).
2. Bolognani, F. & Perrone-Bizzozero, N. I. RNA-protein interactions and control of mRNA stability in neurons. J. Neurosci. Res. 86, 481-489 (2008).
3. Kishore, S., Luber, S. & Zavolan, M. Deciphering the role of RNA-binding proteins in the post-transcriptional control of gene expression. Brief. Funct. Genomics 9, 391-404 (2010).
4. Darnell, R. B. RNA protein interaction in neurons. Annu. Rev. Neurosci. 36, 243-270 (2013).
5. Keppetipola, N., Sharma, S., Li, Q. & Black, D. L. Neuronal regulation of pre-mRNA splicing by polypyrimidine tract binding proteins, PTBP1 and PTBP2. Crit. Rev. Biochem. Mol. Biol. 47, 360-378 (2012).
6. Yap, K. & Makeyev, E. V. Regulation of gene expression in mammalian nervous system through alternative pre-mRNA splicing coupled with RNA quality control mechanisms. Mol. Cell Neurosci. 56, 420-428 (2013).
7. Makeyev, E. V., Zhang, J., Carrasco, M. A. & Maniatis, T. The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol. Cell 27, 435-448 (2007).
8. Xue, Y. et al. Direct conversion of fibroblasts to neurons by reprogramming PTB-regulated microRNA circuits. Cell 152, 82-96 (2013).
9. Yap, K., Lim, Z. Q., Khandelia, P., Friedman, B. & Makeyev, E. V. Coordinated regulation of neuronal mRNA steady-state levels through developmentally controlled intron retention. Genes Dev. 26, 1209-1223 (2012).
10. Fiore, R., Khudayberdiev, S., Saba, R. & Schratt, G. MicroRNA function in the nervous system. Prog. Mol. Biol. Transl. Sci. 102, 47-100 (2011).
11. Coolen, M., Katz, S. & Bally-Cuif, L. miR-9: a versatile regulator of neurogenesis. Front. Cell. Neurosci. 7, 220 (2013).
12. McKee, A. E. et al. A genome-wide in situ hybridization map of RNA-binding proteins reveals anatomically restricted expression in the developing mouse brain. BMC Dev. Biol. 5, 14 (2005).
13. Akamatsu, W. et al. The RNA-binding protein HuD regulates neuronal cell identity and maturation. Proc. Natl Acad. Sci. USA 102, 4625-4630 (2005).
14. Ince-Dunn, G. et al. Neuronal Elav-like (Hu) proteins regulate RNA splicing and abundance to control glutamate levels and neuronal excitability. Neuron 75, 1067-1080 (2012).
15. Ruggiu, M. et al. Rescuing Z\+ agrin splicing in Nova null mice restores synapse formation and unmasks a physiologic defect in motor neuron firing. Proc. Natl Acad. Sci. USA 106, 3513-3518 (2009).
16. Hinman, M. N. & Lou, H. Diverse molecular functions of Hu proteins. Cell. Mol. Life Sci. 65, 3168-3181 (2008).
17. Perrone-Bizzozero, N. & Bird, C. W. Role of HuD in nervous system function and pathology. Front. Biosci. 5, 554-563 (2013).
18. Ule, J. et al. An RNA map predicting Nova-dependent splicing regulation. Nature 444, 580-586 (2006).
19. Eom, T. et al. NOVA-dependent regulation of cryptic NMD exons controls synaptic protein levels after seizure. eLife 2, e00178 (2013).
20. Bakheet, T., Williams, B. R. & Khabar, K. S. ARED 3.0: the large and diverse AU-rich transcriptome. Nucleic Acids Res. 34, D111-D114 (2006).
21. Gruber, A. R., Fallmann, J., Kratochvill, F., Kovarik, P. & Hofacker, I. L. AREsite: a database for the comprehensive investigation of AU-rich elements. Nucleic Acids Res. 39, D66-D69 (2011).
22. von Roretz, C., Di Marco, S., Mazroui, R. & Gallouzi, I. E. Turnover of AU-rich-containing mRNAs during stress: a matter of survival. Wiley Interdiscip. Rev. RNA 2, 336-347 (2011).
23. Schoenberg, D. R. & Maquat, L. E. Regulation of cytoplasmic mRNA decay. Nat. Rev. Genet. 13, 246-259 (2012).
24. Brooks, S. A. & Blackshear, P. J. Tristetraprolin (TTP): interactions with mRNA and proteins, and current thoughts on mechanisms of action. Biochim. Biophys. Acta 1829, 666-679 (2013).
25. Carballo, E., Lai, W. S. & Blackshear, P. J. Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin. Science 281, 1001-1005 (1998).
26. Taylor, G. A. et al. A pathogenetic role for TNF alpha in the syndrome of cachexia, arthritis, and autoimmunity resulting from tristetraprolin (TTP) deficiency. Immunity 4, 445-454 (1996).
27. Ross, C. R., Brennan-Laun, S. E. & Wilson, G. M. Tristetraprolin: roles in cancer and senescence. Ageing Res. Rev. 11, 473-484 (2012).
28. Dai, W., Zhang, G. & Makeyev, E. V. RNA-binding protein HuR autoregulates its expression by promoting alternative polyadenylation site usage. Nucleic Acids Res. 40, 787-800 (2012).
29. Mansfield, K. D. & Keene, J. D. Neuron-specific ELAV/Hu proteins suppress HuR mRNA during neuronal differentiation by alternative polyadenylation. Nucleic Acids Res. 40, 2734-2746 (2012).
30. Mukherjee, N. et al. Global target mRNA specification and regulation by the RNA-binding protein ZFP36. Genome Biol. 15, R12 (2014).
31. Suzuki, H. et al. Comprehensive analysis of alternative splicing and functionality in neuronal differentiation of P19 cells. PLoS ONE 6, e16880 (2011).
32. Hoque, M. et al. Analysis of alternative cleavage and polyadenylation by 3' region extraction and deep sequencing. Nat. Methods 10, 133-139 (2012).
33. Miura, P., Sanfilippo, P., Shenker, S. & Lai, E. C. Alternative polyadenylation in the nervous system: To what lengths will 3' UTR extensions take us? BioEssays 36, 766-777 (2014).
34. Elkon, R., Ugalde, A. P. & Agami, R. Alternative cleavage and polyadenylation: extent, regulation and function. Nat. Rev. Genet. 14, 496-506 (2013).
35. Tian, B. & Manley, J. L. Alternative cleavage and polyadenylation: the long and short of it. Trends Biochem. Sci. 38, 312-320 (2013).
36. Zhang, H., Lee, J. Y. & Tian, B. Biased alternative polyadenylation in human tissues. Genome Biol. 6, R100 (2005).
37. Al-Ahmadi, W., Al-Ghamdi, M., Al-Haj, L., Al-Saif, M. & Khabar, K. S. Alternative polyadenylation variants of the RNA binding protein, HuR: abundance, role of AU-rich elements and auto-Regulation. Nucleic Acids Res. 37, 3612-3624 (2009).
38. Khandelia, P., Yap, K. & Makeyev, E. V. Streamlined platform for short hairpin RNA interference and transgenesis in cultured mammalian cells. Proc. Natl Acad. Sci. USA 108, 12799-12804 (2011).
39. Sempere, L. F. et al. Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol. 5, R13 (2004).
40. Torres, A. G., Fabani, M. M., Vigorito, E. & Gait, M. J. MicroRNA fate upon targeting with anti-miRNA oligonucleotides as revealed by an improved northern-blot-based method for miRNA detection. RNA 17, 933-943 (2011).
41. Lai, W. S., Parker, J. S., Grissom, S. F., Stumpo, D. J. & Blackshear, P. J. Novel mRNA targets for tristetraprolin (TTP) identified by global analysis of stabilized transcripts in TTP-deficient fibroblasts. Mol. Cell Biol. 26, 9196-9208 (2006).
42. Lim, L. P. et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433, 769-773 (2005).
43. Bolognani, F., Contente-Cuomo, T. & Perrone-Bizzozero, N. I. Novel recognition motifs and biological functions of the RNA-binding protein HuD revealed by genome-wide identification of its targets. Nucleic Acids Res. 38, 117-130 (2010).
44. Chung, S., Eckrich, M., Perrone-Bizzozero, N., Kohn, D. T. & Furneaux, H. The Elav-like proteins bind to a conserved regulatory element in the 3'-untranslated region of GAP-43 mRNA. J. Biol. Chem. 272, 6593-6598 (1997).
45. Menezes, J. R. & Luskin, M. B. Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon. J. Neurosci. 14, 5399-5416 (1994).
46. Bithell, A. REST: transcriptional and epigenetic regulator. Epigenomics 3, 47-58 (2011).
47. Follert, P., Cremer, H. & Beclin, C. MicroRNAs in brain development and function: a matter of flexibility and stability. Front. Mol. Neurosci. 7, 5 (2014).
48. Krichevsky, A. M., Sonntag, K. C., Isacson, O. & Kosik, K. S. Specific microRNAs modulate embryonic stem cell-derived neurogenesis. Stem Cells 24, 857-864 (2006).
49. Yoo, A. S. et al. MicroRNA-mediated conversion of human fibroblasts to neurons. Nature 476, 228-231 (2011).
50. Ray, D. et al. A compendium of RNA-binding motifs for decoding gene regulation. Nature 499, 172-177 (2013).
51. Simone, L. E. & Keene, J. D. Mechanisms coordinating ELAV/Hu mRNA regulons. Curr. Opin. Genet. Dev. 23, 35-43 (2013).
52. Ratti, A. et al. Post-transcriptional regulation of neuro-oncological ventral antigen 1 by the neuronal RNA-binding proteins ELAV. J. Biol. Chem. 283, 7531-7541 (2008).
53. Darnell, R. B. & Posner, J. B. Paraneoplastic syndromes involving the nervous system. N. Engl. J. Med. 349, 1543-1554 (2003).
54. Lamberts, S. W., Hofland, L. J. & Nobels, F. R. Neuroendocrine tumor markers. Front. Neuroendocrinol. 22, 309-339 (2001).
55. Al-Ahmadi, W., Al-Ghamdi, M., Al-Souhibani, N. & Khabar, K. S. miR-29a inhibition normalizes HuR over-expression and aberrant AU-rich mRNA stability in invasive cancer. J. Pathol. 230, 28-38 (2013).
56. Gebeshuber, C. A., Zatloukal, K. & Martinez, J. miR-29a suppresses tristetraprolin, which is a regulator of epithelial polarity and metastasis. EMBO Rep. 10, 400-405 (2009).
57. Sambrook, J. & Russell, R. W. Molecular Cloning: A Laboratory Manual, 3rd edn. (Cold Spring Harbor Laboratory Press, 2001).
58. Kaech, S. & Banker, G. Culturing hippocampal neurons. Nat. Protoc. 1, 2406-2415 (2006).
59. Juvvuna, P. K., Khandelia, P., Lee, L. M. & Makeyev, E. V. Argonaute identity defines the length of mature mammalian microRNAs. Nucleic Acids Res. 40, 6808-6820 (2012).
60. Hu, J., Lutz, C. S., Wilusz, J. & Tian, B. Bioinformatic identification of candidate cis-regulatory elements involved in human mRNA polyadenylation. RNA 11, 1485-1493 (2005).
61. Lattin, J. E. et al. Expression analysis of G protein-coupled receptors in mouse macrophages. Immunome Res. 4, 5 (2008).
62. Kruger, J. & Rehmsmeier, M. RNAhybrid: microRNA target prediction easy, fast and flexible. Nucleic Acids Res. 34, W451-W454 (2006).
63. Siepel, A. et al. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res. 15, 1034-1050 (2005).