Drosha and DGCR8 in MicroRNA Biogenesis

Enzymes

Volumn 32, Issue , 2012, Pages 101-121

  Guo, Feng ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

DiGeorge syndrome; Gene regulation; Heme; Hemoprotein; MicroRNA; Molecular recognition; Ribonuclease; RNA processing; RNA binding protein; RNase III; WW motif

Indexed keywords

EID: 84869225192     PISSN: 18746047     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-404741-9.00005-2     Document Type: Chapter

References (77)

1. Kim V.N., Han J., Siomi M.C. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 2009, 10:126-139.
2. Lee R.C., Feinbaum R.L., Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75:843-854.
3. Wightman B., Ha I., Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 1993, 75:855-862.
4. Lee Y., Jeon K., Lee J.T., Kim S., Kim V.N. MicroRNA maturation: stepwise processing and subcellular localization. EMBO J 2002, 21:4663-4670.
5. Westholm J.O., Lai E.C. Mirtrons: microRNA biogenesis via splicing. Biochimie 2011, 93:1897-1904.
6. Scott M.S., Ono M. From snoRNA to miRNA: dual function regulatory non-coding RNAs. Biochimie 2011, 93:1987-1992.
7. Voinnet O. Origin, biogenesis, and activity of plant microRNAs. Cell 2009, 136:669-687.
8. MacRae I.J., Doudna J.A. Ribonuclease revisited: structural insights into ribonuclease III family enzymes. Curr Opin Struct Biol 2007, 17:138-145.
9. Danin-Kreiselman M., Lee C.Y., Chanfreau G. RNAse III-mediated degradation of unspliced pre-mRNAs and lariat introns. Mol Cell 2003, 11:1279-1289.
10. MacRae I.J., et al. Structural basis for double-stranded RNA processing by Dicer. Science 2006, 311:195-198.
11. Drinnenberg I.A., et al. RNAi in budding yeast. Science 2009, 326:544-550.
12. Weinberg D.E., Nakanishi K., Patel D.J., Bartel D.P. The inside-out mechanism of Dicers from budding yeasts. Cell 2011, 146:262-276.
13. Bernstein D.A., Vyas V.K., Weinberg D.E., Drinnenberg I.A., Bartel D.P., Fink G.R. Candida albicans Dicer (CaDcr1) is required for efficient ribosomal and spliceosomal RNA maturation. Proc Natl Acad Sci USA 2012, 109:523-528.
14. Wu H., Xu H., Miraglia L.J., Crooke S.T. Human RNase III is a 160-kDa protein involved in preribosomal RNA processing. J Biol Chem 2000, 275:36957-36965.
15. Liang X.H., Crooke S.T. Depletion of key protein components of the RISC pathway impairs pre-ribosomal RNA processing. Nucleic Acids Res 2011, 39:4875-4889.
16. Fukuda T., et al. DEAD-box RNA helicase subunits of the Drosha complex are required for processing of rRNA and a subset of microRNAs. Nat Cell Biol 2007, 9:604-611.
17. Lee Y., et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 2003, 425:415-419.
18. Han J., Lee Y., Yeom K.H., Kim Y.K., Jin H., Kim V.N. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev 2004, 18:3016-3027.
19. Denli A.M., Tops B.B., Plasterk R.H., Ketting R.F., Hannon G.J. Processing of primary microRNAs by the Microprocessor complex. Nature 2004, 432:231-235.
20. Gregory R.I., et al. The Microprocessor complex mediates the genesis of microRNAs. Nature 2004, 432:235-240.
21. Landthaler M., Yalcin A., Tuschl T. The human DiGeorge syndrome critical region gene 8 and its D. melanogaster homolog are required for miRNA biogenesis. Curr Biol 2004, 14:2162-2167.
22. Mueller G.A., Miller M.T., Derose E.F., Ghosh M., London R.E., Hall T.M. Solution structure of the Drosha double-stranded RNA-binding domain. Silence 2010, 1:2.
23. Wostenberg C., Quarles K.A., Showalter S.A. Dynamic origins of differential RNA binding function in two dsRBDs from the miRNA " microprocessor" complex. Biochemistry 2010, 49:10728-10736.
24. Gupta V., Huang X., Patel R.C. The carboxy-terminal, M3 motifs of PACT and TRBP have opposite effects on PKR activity. Virology 2003, 315:283-291.
25. Haase A.D., et al. TRBP, a regulator of cellular PKR and HIV-1 virus expression, interacts with Dicer and functions in RNA silencing. EMBO Rep 2005, 6:961-967.
26. Giot L., et al. A protein interaction map of Drosophila melanogaster. Science 2003, 302:1727-1736.
27. Wang Y., Medvid R., Melton C., Jaenisch R., Blelloch R. DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat Genet 2007, 39:380-385.
28. Yi R., et al. DGCR8-dependent microRNA biogenesis is essential for skin development. Proc Natl Acad Sci USA 2009, 106:498-502.
29. Shiohama A., Sasaki T., Noda S., Minoshima S., Shimizu N. Nucleolar localization of DGCR8 and identification of eleven DGCR8-associated proteins. Exp Cell Res 2007, 313:4196-4207.
30. Han J., et al. Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 2006, 125:887-901.
31. Faller M., Matsunaga M., Yin S., Loo J.A., Guo F. Heme is involved in microRNA processing. Nat Struct Mol Biol 2007, 14:23-29.
32. Yeom K.H., Lee Y., Han J., Suh M.R., Kim V.N. Characterization of DGCR8/Pasha, the essential cofactor for Drosha in primary miRNA processing. Nucleic Acids Res 2006, 34:4622-4629.
33. Shiohama A., Sasaki T., Noda S., Minoshima S., Shimizu N. Molecular cloning and expression analysis of a novel gene DGCR8 located in the DiGeorge syndrome chromosomal region. Biochem Biophys Res Commun 2003, 304:184-190.
34. Sudol M. The WW domain. Modular protein domains 2005, 59-72. Wiley-VCH, Weinheim, Germany. G. Cesareni, M. Gimona, M. Sudol, M. Yaffe (Eds.).
35. Sudol M., Harvey K.F. Modularity in the Hippo signaling pathway. Trends Biochem Sci 2010, 35:627-633.
36. Gong M., Chen Y., Senturia R., Ulgherait M., Faller M., Guo F. Caspases cleave and inhibit the microRNA processing protein DiGeorge Critical Region 8. Protein Sci 2012, 21:797-808.
37. Senturia R., Laganowsky A., Barr I., Scheidemantle B.D., Guo F. Dimerization and heme binding are conserved in amphibian and starfish homologues of the microRNA processing protein DGCR8. PLoS One 2012, 7:e39688.
38. Barr I., Smith A.T., Chen Y., Senturia R., Burstyn J.N., Guo F. Ferric, not ferrous, heme activates RNA-binding protein DGCR8 for primary microRNA processing. Proc Natl Acad Sci USA 2012, 109:1919-1924.
39. Sohn S.Y., Bae W.J., Kim J.J., Yeom K.H., Kim V.N., Cho Y. Crystal structure of human DGCR8 core. Nat Struct Mol Biol 2007, 14:847-853.
40. Wostenberg C., Noid W.G., Showalter S.A. MD simulations of the dsRBP DGCR8 reveal correlated motions that may aid pri-miRNA binding. Biophys J 2010, 99:248-256.
41. Senturia R., et al. Structure of the dimerization domain of DiGeorge Critical Region 8. Protein Sci 2010, 19:1354-1365.
42. Rost B., Yachdav G., Liu J. The PredictProtein server. Nucleic Acids Res 2004, 32:W321-W326.
43. Paoli M., Marles-Wright J., Smith A. Structure-function relationships in heme-proteins. DNA Cell Biol 2002, 21:271-280.
44. Ortiz de Montellano P.R. Cytochrome P450: structure, mechanism, and biochemistry 2004, Springer, New York, NY. 3rd ed.
45. Barr I., et al. DiGeorge Critical Region 8 (DGCR8) is a double-cysteine-ligated heme protein. J Biol Chem 2011, 286:16716-16725.
46. Karayiorgou M., Simon T.J., Gogos J.A. 22q11.2 microdeletions: linking DNA structural variation to brain dysfunction and schizophrenia. Nat Rev Neurosci 2010, 11:402-416.
47. Stark K.L., et al. Altered brain microRNA biogenesis contributes to phenotypic deficits in a 22q11-deletion mouse model. Nat Genet 2008, 40:751-760.
48. Fenelon K., et al. Deficiency of Dgcr8, a gene disrupted by the 22q11.2 microdeletion, results in altered short-term plasticity in the prefrontal cortex. Proc Natl Acad Sci USA 2011, 108:4447-4452.
49. Schofield C.M., Hsu R., Barker A.J., Gertz C.C., Blelloch R., Ullian E.M. Monoallelic deletion of the microRNA biogenesis gene Dgcr8 produces deficits in the development of excitatory synaptic transmission in the prefrontal cortex. Neural Dev 2011, 6:11.
50. Berezikov E., Guryev V., van de Belt J., Wienholds E., Plasterk R.H., Cuppen E. Phylogenetic shadowing and computational identification of human microRNA genes. Cell 2005, 120:21-24.
51. Lim L.P., Glasner M.E., Yekta S., Burge C.B., Bartel D.P. Vertebrate microRNA genes. Science 2003, 299:1540.
52. Parisien M., Major F. The MC-Fold and MC-Sym pipeline infers RNA structure from sequence data. Nature 2008, 452:51-55.
53. Zeng Y., Wagner E.J., Cullen B.R. Both natural and designed micro RNAs can inhibit the expression of cognate mRNAs when expressed in human cells. Mol Cell 2002, 9:1327-1333.
54. Zeng Y., Cullen B.R. Sequence requirements for micro RNA processing and function in human cells. RNA 2003, 9:112-123.
55. Silva J.M., et al. Second-generation shRNA libraries covering the mouse and human genomes. Nat Genet 2005, 37:1281-1288.
56. Zeng Y., Cullen B.R. Efficient processing of primary microRNA hairpins by Drosha requires flanking nonstructured RNA sequences. J Biol Chem 2005, 280:27595-27603.
57. Zeng Y., Yi R., Cullen B.R. Recognition and cleavage of primary microRNA precursors by the nuclear processing enzyme Drosha. EMBO J 2005, 24:138-148.
58. Zhang X., Zeng Y. The terminal loop region controls microRNA processing by Drosha and Dicer. Nucleic Acids Res 2010, 38:7689-7697.
59. Faller M., et al. DGCR8 recognizes primary transcripts of microRNAs through highly cooperative binding and formation of higher-order structures. RNA 2010, 16:1570-1583.
60. Juneau K., Podell E., Harrington D.J., Cech T.R. Structural basis of the enhanced stability of a mutant ribozyme domain and a detailed view of RNA-solvent interactions. Structure 2001, 9:221-231.
61. Han J., et al. Posttranscriptional crossregulation between Drosha and DGCR8. Cell 2009, 136:75-84.
62. Triboulet R., Chang H.M., Lapierre R.J., Gregory R.I. Post-transcriptional control of DGCR8 expression by the Microprocessor. RNA 2009, 15:1005-1011.
63. Kadener S., et al. Genome-wide identification of targets of the drosha-pasha/DGCR8 complex. RNA 2009, 15:537-545.
64. Barad O., et al. Efficiency and specificity in microRNA biogenesis. Nat Struct Mol Biol 2012, 19:650-652.
65. Wada T., Kikuchi J., Furukawa Y. Histone deacetylase 1 enhances microRNA processing via deacetylation of DGCR8. EMBO Rep 2012, 13:142-149.
66. Ghodgaonkar M.M., et al. Abrogation of DNA vector-based RNAi during apoptosis in mammalian cells due to caspase-mediated cleavage and inactivation of Dicer-1. Cell Death Differ 2009, 16:858-868.
67. Matskevich A.A., Moelling K. Stimuli-dependent cleavage of Dicer during apoptosis. Biochem J 2008, 412:527-534.
68. Tang X., Zhang Y., Tucker L., Ramratnam B. Phosphorylation of the RNase III enzyme Drosha at Serine300 or Serine302 is required for its nuclear localization. Nucleic Acids Res 2010, 38:6610-6619.
69. Tang X., Li M., Tucker L., Ramratnam B. Glycogen synthase kinase 3 beta (GSK3beta) phosphorylates the RNAase III enzyme Drosha at S300 and S302. PLoS One 2011, 6:e20391.
70. Wu D., Pan W. GSK3: a multifaceted kinase in Wnt signaling. Trends Biochem Sci 2010, 35:161-168.
71. Suzuki H.I., Yamagata K., Sugimoto K., Iwamoto T., Kato S., Miyazono K. Modulation of microRNA processing by p53. Nature 2009, 460:529-533.
72. Davis B.N., Hilyard A.C., Lagna G., Hata A. SMAD proteins control DROSHA-mediated microRNA maturation. Nature 2008, 454:56-61.
73. Trabucchi M., et al. The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs. Nature 2009, 459:1010-1014.
74. Viswanathan S.R., Daley G.Q., Gregory R.I. Selective blockade of microRNA processing by Lin28. Science 2008, 320:97-100.
75. Piskounova E., et al. Lin28A and Lin28B inhibit let-7 microRNA biogenesis by distinct mechanisms. Cell 2011, 147:1066-1079.
76. Shenoy A., Blelloch R. Genomic analysis suggests that mRNA destabilization by the microprocessor is specialized for the auto-regulation of Dgcr8. PLoS One 2009, 4:e6971.
77. Macias S., Plass M., Stajuda A., Michlewski G., Eyras E., Caceres J.F. DGCR8 HITS-CLIP reveals novel functions for the Microprocessor. Nat Struct Mol Biol 2012, 19:760-766.