The kinase ABL phosphorylates the microprocessor subunit DGCR8 to stimulate primary microRNA processing in response to DNA damage

Science Signaling

Volumn 8, Issue 383, 2015, Pages

  Tu, Chi Chiang ^a,b   Zhong, Yan ^a   Nguyen, Louis ^a   Tsai, Aaron ^a   Sridevi, Priya ^a   Tarn, Woan Yuh ^b   Wang, Jean Y J ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ABELSON KINASE; MICRORNA; MICRORNA 34A; MICRORNA 34C; PROTEIN DGCR8; PROTEIN DROSHA; RIBONUCLEASE III; RNA BINDING PROTEIN; TYROSINE; UNCLASSIFIED DRUG; DGCR8 PROTEIN, HUMAN; DGCR8 PROTEIN, MOUSE; MIRN34 MICRORNA, HUMAN; MIRN34 MICRORNA, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CROSS LINKING; DNA DAMAGE; ENZYME PHOSPHORYLATION; EPITHELIUM CELL; KIDNEY; KIDNEY CELL; MOUSE; NONHUMAN; NUCLEAR IMPORT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN RNA BINDING; RNA PROCESSING; RNA SEQUENCE; ANIMAL; GENETICS; HUMAN; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

MUS;

ANIMALS; DNA DAMAGE; HUMANS; MICE; MICRORNAS; ONCOGENE PROTEINS V-ABL; PHOSPHORYLATION; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA-BINDING PROTEINS;

EID: 84937905575     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.aaa4468     Document Type: Article

References (63)

1. H. Guo, N. T. Ingolia, J. S. Weissman, D. P. Bartel, Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466, 835-840 (2010).
2. I. A. Qureshi, M. F. Mehler, Regulation of non-coding RNA networks in the nervous system-What's the REST of the story? Neurosci. Lett. 466, 73-80 (2009).
3. R. C. Friedman, K. K. Farh, C. B. Burge, D. P. Bartel, Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19, 92-105 (2009).
4. R. I. Gregory, K. P. Yan, G. Amuthan, T. Chendrimada, B. Doratotaj, N. Cooch, R. Shiekhattar, The Microprocessor complex mediates the genesis of microRNAs. Nature 432, 235-240 (2004).
5. V. N. Kim, J. Han, M. C. Siomi, Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10, 126-139 (2009).
6. G. Hutvágner, J. McLachlan, A. E. Pasquinelli, E. Bálint, T. Tuschl, P. D. Zamore, A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293, 834-838 (2001).
7. V. N. Kim, MicroRNA precursors in motion: Exportin-5 mediates their nuclear export. Trends Cell Biol. 14, 156-159 (2004).
8. M. Morlando, M. Ballarino, N. Gromak, F. Pagano, I. Bozzoni, N. J. Proudfoot, Primary microRNA transcripts are processed co-transcriptionally. Nat. Struct. Mol. Biol. 15, 902-909 (2008).
9. J. M. Pawlicki, J. A. Steitz, Primary microRNA transcript retention at sites of transcription leads to enhanced microRNA production. J. Cell Biol. 182, 61-76 (2008).
10. H. I. Suzuki, K. Yamagata, K. Sugimoto, T. Iwamoto, S. Kato, K. Miyazono, Modulation of microRNA processing by p53. Nature 460, 529-533 (2009).
11. S. Guil, J. F. Cáceres, The multifunctional RNA-binding protein hnRNP A1 is required for processing of miR-18a. Nat. Struct. Mol. Biol. 14, 591-596 (2007).
12. M. A. Newman, J. M. Thomson, S. M. Hammond, Lin-28 interaction with the Let-7 precursor loop mediates regulated microRNA processing. RNA 14, 1539-1549 (2008).
13. T. L. Cheng, Z. Wang, Q. Liao, Y. Zhu, W. H. Zhou, W. X u, Z. Qiu, MeCP2 suppresses nuclear microRNA processing and dendritic growth by regulating the DGCR8/Drosha complex. Dev. Cell 28, 547-560 (2014).
14. J. Han, J. S. Pedersen, S. C. Kwon, C. D. Belair, Y. K. Kim, K. H. Yeom, W. Y. Yang, D. Haussler, R. Blelloch, V. N. Kim, Posttranscriptional crossregulation between Drosha and DGCR8. Cell 136, 75-84 (2009).
15. R. Triboulet, R. I. Gregory, Autoregulatory mechanisms controlling the Microprocessor. Adv. Exp. Med. Biol. 700, 56-66 (2010).
16. X. Wang, X. Zhao, P. Gao, M. Wu, c-Myc modulates microRNA processing via the transcriptional regulation of Drosha. Sci. Rep. 3, 1942 (2013).
17. V. C. Auyeung, I. Ulitsky, S. E. McGeary, D. P. Bartel, Beyond secondary structure: Primary-sequence determinants license pri-miRNA hairpins for processing. Cell 152, 844-858 (2013).
18. G. Wan, R. Mathur, X. Hu, X. Zhang, X. Lu, miRNA response to DNA damage. Trends Biochem. Sci. 36, 478-484 (2011).
19. M. D. Wouters, D. C. Van Gent, J. H. Hoeijmakers, J. Pothof, MicroRNAs, the DNA damage response and cancer. Mutat. Res. 717, 54-66 (2011).
20. L. He, X. He, L. P. Lim, E. de Stanchina, Z. Xuan, Y. Liang, W. Xue, L. Zender, J. Magnus, D. Ridzon, A. L. Jackson, P. S. Linsley, C. Chen, S. W. Lowe, M. A. Cleary, G. J. Hannon, A microRNA component of the p53 tumour suppressor network. Nature 447, 1130-1134 (2007).
21. J. Han, Y. Lee, K. H. Yeom, Y. K. Kim, H. Jin, V. N. Kim, The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev. 18, 3016-3027 (2004).
22. G. T. Bommer I. Gerin Y. Feng A. J. Kaczorowski R. Kuick R. E. Love Y. Zhai T. J. Gio rdano Z. S. Qin B. B. Moore O. A. MacDougaldK. R. Cho E. R. Fearon, p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr. Biol. 17 1298-1307 2007
23. T. C. Chan g, E. A. Wentzel, O. A. Kent, K. Ramachandran, M. Mullendore, K. H. Lee, G. Feldmann, M. Yamakuchi, M. Ferlito, C. J. Lowenstein, D. E. Arking, M. A. Beer, A. Maitra, J. T. Mendell, Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol. Cell 26, 745-752 (2007).
24. C. P. Concepcion, Y. C. Han, P. Mu, C. Bonetti, E. Yao, A. D'Andrea, J. A. Vid igal, W. P. Maughan, P. Ogrodowski, A. Ventura, Intact p53-dependent responses in miR-34-deficient mice. PLOS Genet. 8, e1002797 (2012).
25. J. Bao D. Li, L.Wang, J. Wu, Y. Hu, Z. Wang, Y. Chen, X. Cao, C. Jiang, W. Yan, C. Xu, MicroRNA-449 and microRNA-34b/c function redundantly in murine testes by targeting E2F transcription factor-retinoblastoma protein (E2F-pRb) pathway. J. Biol. Chem. 287, 21686-21698 (2012).
26. R. Song, P. Walentek, N. Sponer, A. Klimke, J. S. Lee, G. Dixon, R. Harland, Y. Wan, P. Lishko, M. Lize, M. Kessel, L. He, miR-34/449 miRNAs are req uired for motile ciliogenesis by repressing cp110. Nature 510, 115-120 (2014).
27. M. Preyer, C. W. Shu, J. Y. Wang, Delayed activation of Bax by DNA damage in embryonic stem cells with knock-in mutations of the Abl nuclear localization signals. Cell Death Differ. 14, 1139-1148 (2007).
28. K. Yoshida, T. Yamaguchi, T. Natsume, D. Kufe, Y. Miki, JNK phosphorylation of 14-3-3 proteins regulates nuclear targeting of c-Abl in the apoptotic response to DNA damage. Nat. Cell Biol. 7, 278-285 (2005).
29. R. Baskaran, S. R. Escobar, J. Y. Wang, Nuclear c-Abl is a COOH-terminal repeated domain (CTD)-tyrosine (CTD)-tyrosine kinase-specific for the mammalian RNA polymerase II: Possible role in transcription elon gation. Cell Growth Differ. 10, 387-396 (1999).
30. J. G. Gong, A. Costanzo, H. Q. Yang, G. Melino, W. G. Kaelin Jr., M. Levrero, J. Y. Wang, The tyrosine kinase c-Abl regulates p73 i n apoptotic response to cisplatininduced DNA damage. Nature 399, 806-809 (1999).
31. R. V. Sionov,S.Coen, Z.Goldberg,M. Berger,B.Bercovich,Y.Ben-Neriah, A. Ciechanover, Y. Haupt, c-Abl regulates p53 levels under normal and stress conditions by preventing its nuclear export and ubiquitination. Mol. Cell Biol. 21, 5869-5878 (2001).
32. Z. Goldberg, R. Vogt Sionov, M. Berger, Y. Zwang, R. Perets, R. A. Van Etten, M. Oren, Y. Taya, Y. Haupt, Tyrosine phosphorylation of Mdm2 by c-Abl: Implications for p53 regulation. EMBO J. 21, 3715-3727 (2002).
33. V. Zuckerman, K. Lenos, G.M. Popowicz, I. Silberman, T. Grossman, J. C. Marine, T. A. Holak, A. G. Jochemsen, Y. Haupt, c-Abl phosphorylates Hdmx and regulates its interaction with p53. J. Biol. Chem. 284, 4031-4039 (2009).
34. R. Keshet, J. Adler, I. Ricardo Lax, M. Shanzer, Z. Porat, N. Reuven, Y. Shaul, c-Abl antagonizes the YAP oncogenic function. Cell Death Differ. 22, 935-945 (2014).
35. S. H. Shin, S. S. Kang, Phosphorylation of Tip60 tyrosine 327 by Abl kinase inhibits HAT activity through association with FE65. Open Biochem. J. 7, 66-72 (2013).
36. M. Gonzal ez-Zuñ iga, P. S. Contreras, L. D. Estrada, D. Chamorro, A. Villagra, S. Zanlungo, E. Seto, A. R. Alvarez, c-Abl stabilizes HDAC2 levels by tyrosine phosphorylation repressing neuronal gene expression in Alzheimer's disease. Mol. Cell 56, 163-173 (2014).
37. P. Sridevi, M. K. Nhiayi, J. Y. Wang, Genetic disruption of Abl nuclear import reduces renal apoptosis in a mouse model of cisplatin-induced nephrotoxicity. Cell Death Differ. 20, 953-962 (2013).
38. I. G. Cannell, Y. W. Kong, S. J. Johnston, M. L. Chen, H. M. Collins, H. C. Dobbyn, A. Elia, T. R. Kress, M. Dickens, M. J. Cl emens, D. M. Heery, M. Gaestel, M. Eilers, A. E. Willis, M. Bushell, p38 MAPK/MK2-mediated induction of miR-34c following DNA damage prevents Myc-dependent DNA replication. Proc. Natl. Acad. Sci. U.S.A. 107, 5375-5380 (2010).
39. M. Debbas, E. White, Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes Dev. 7, 546-554 (1993).
40. M. Bantscheff, D. Eberhard, Y. Abraham, S. Bastuck, M. Boesche, S. Hobson, T.Mathieson, J.Perrin,M.Raida,C.Rau,V.Reader,G.Sweetman,A.Bauer,T.Bouwmeester, C. Hopf, U. Kruse, G. Neubauer, N. Ramsden, J. Rick, B. Kuster, G. Drewes, Quan titative chemical proteomics reveals mechanisms of action of clinical ABL kinase inhibitors. Nat. Biotechnol. 25, 1035-1044 (2007).
41. I. Hussain, J. Fabrè gue, L. Anderes, S.Ousson, F.Borlat, V.Eli gert,S.Berger,M.Dimitrov, J. R. Alattia, P. C. Fraering,D. Beher, The role of g-secretase activating protein (GSAP) and imatinib in the regulation of g-secretase activity and amyloid-b generation. J. Biol. Chem. 288, 2521-2531 (2013).
42. D. Barilá,R.Mangano, S.Gonfloni, J.Kretzschmar, M. Moro,D.Bohmann, G. Superti-Furga, A nuclear tyrosine phosphorylation circuit: C-Jun as an activator and substrate of c-Abl and JNK. EMBO J. 19, 273-281 (2000).
43. S. Taagepera D.McDonald J. E. Loeb L. L. Whitaker A. K.McElroy J. Y.Wang T. J. Hope. Nuclear-cytoplasmic shuttling of C-ABL tyrosine kinase. Proc. Natl. Acad. Sci. U.S.A.95. 7457-7462(1998 ).
44. I. Heo, C. Joo, J. Cho, M. Ha, J. Han, V. N. Kim, Lin28 mediates the terminal uridylation of let-7 precursor MicroRNA. Mol. Cell 32, 276-284 (2008).
45. B. M. Roth, D. Ishimaru, M. Hennig, The core microprocessor component DiGeorge syndrome critical region 8 (DGCR8) is a nonspecific RNA-binding protein. J. Biol. Chem. 288, 26785-26799 (2013).
46. K. H. Yeom, Y. Lee, J. Han, M. R. Suh, V. N. Kim, Characterization of DGCR8/Pasha, the essential cofactor for Drosha in primary miRNA processing. Nucleic Acids Res. 34, 4622-4629 (2006).
47. K. M. Herbert, G. Pimienta, S. J. DeGregorio, A. Alexandrov, J. A. Steitz, Phosphorylation of DGCR8 increases its intracellular stability and induces a progrowth miRNA profile. Cell Rep. 5, 1070-1081 (2013).
48. J. Quick-Cleveland, J. P. Jacob, S. H. Weitz, G. Shoffner, R. Senturia, F. Guo, The DGCR8 RNA-binding heme domain recognizes primary microRNAs by clamping the hairpin. Cell Rep. 7, 1994-2005 (2014).
49. V. L. Tybulewicz, C. E. Crawford, P. K. Jackson, R. T. Bronson, R. C. Mulligan, Neonatal lethality and lymphopenia inmicewith a homozygous disruption of the c-abl proto-oncogene. Cell 65, 1153-1163 (1 991).
50. J. Han, Y. Lee, K. H. Yeom, J.W. Nam, I. Heo, J. K. Rhee, S. Y. Sohn, Y. Cho, B. T. Zhang, V. N. Kim, Molecular basis for the recognition of primarymicroRNAs by theDrosha-DGCR8 compl ex. Cell 125, 887-901 (2006).
51. C. Z. Chen, L. Li, H. F. Lodish, D. P. Bartel, MicroRNAs modulate hematopoietic lineage differentiation. Science 303, 83-86 (2004).
52. S. R.Viswanathan, G. Q. Daley, R. I. Gregory, Selective blockade of microRNA processing by Lin28. Science 320, 97-100 (2008).
53. J. Y. Wang, The capable ABL: What is its biological function? Mol. Cell Biol. 34, 1188-1197 (2014).
54. H. L. Borges, C. Chao, Y. Xu, R. Linden, J. Y. Wang, Radiation-induced apoptosis in developing mouse retina exhibits dose-dep endent requirement for ATM phosphorylation of p53. Cell Death Differ. 11, 494-502 (2004).
55. H.Wang, M. Li, R. Zhang, Y. Wang,W. Zang, Y. Ma,G. Zhao, G. Zhang, Effect of miR-335 upregula tion on the apoptosis and invasion of lung cancer cell A549 and H1299. Tumour Biol. 34, 3101-3109 (2013).
56. S. Wang, X. Chen, M. Tang, MicroRNA-216a inhibits pancreatic cancer by directly targeting Janus kinase 2. Oncol. Rep. 32, 2824-2830 (2014).
57. M.A.Havens, A. A. Reich, D. M. Duelli,M. L.Hastings, Biogenesis ofmammalianmicroRNAs by a non-canonical processing pathway. Nucleic Acids Res. 40, 4626-4640 (2012).
58. A. Mortazavi, B. A. Williams, K. McCue, L. Schaeffer, B. Wold, Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621-628 (2008).
59. M. B. Eisen, P. T. Spellman, P. O. Brown, D. Botstein, Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U.S.A. 95, 14863-14868 (1998).
60. S. Audic, J. M. Claverie, The significance of digital gene expression profiles. Genome Res. 7, 986-995 (1997).
61. C. Chen, D. A. Ridzon, A. J. Broomer, Z. Z hou, D. H. Lee, J. T. Nguyen, M. Barbisin,N. L.Xu, V. R. Mahuvakar, M. R. Andersen, K. Q. Lao, K. J. Livak, K. J. Guegler, Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res. 33, e179 (2005).
62. E. Várallyay, J. Burgyán, Z. Havelda, Detection of microRNAs by Northern blot analyses using LNA probes. Methods 43, 140-145 (2007).
63. B. K. Sun, A. M. Deaton, J. T. Lee, A transient heterochromatic state in Xist preempts X inactivation choice without RNA stabilization. Mol. Cell 21, 617-628 (2006).