The RNA-binding protein TDP-43 selectively disrupts MicroRNA-1/206 incorporation into the RNA-induced silencing complex

Journal of Biological Chemistry

Volumn 289, Issue 20, 2014, Pages 14263-14271

  King, Isabelle N ^a,c   Yartseva, Valeria ^a   Salas, Donaldo ^a   Kumar, Abhishek ^a   Heidersbach, Amy ^a,d   Ando, D Michael ^b,d   Stallings, Nancy R ^e   Elliott, Jeffrey L ^e   Srivastava, Deepak ^a,c,d   Ivey, Kathryn N ^a,c  

^a GLADSTONE INSTITUTE OF CARDIOVASCULAR DISEASE   (United States)

^b GLADSTONE INSTITUTE OF NEUROLOGICAL DISEASE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; GENE EXPRESSION; LOADING; MUSCLE; NEUROPHYSIOLOGY; PROTEINS;

AMYOTROPHIC LATERAL SCLEROSIS; DIFFERENTIAL REGULATION; DROSOPHILA ORTHOLOG; MYOGENIC DIFFERENTIATIONS; NEUROMUSCULAR DISEASE; PHYSICAL INTERACTIONS; RNA-BINDING PROTEIN; RNA-INDUCED SILENCING COMPLEXES;

RNA;

MICRORNA; MICRORNA 1; MICRORNA 133; MICRORNA 206; TAR DNA BINDING PROTEIN; UNCLASSIFIED DRUG; ARGONAUTE PROTEIN; DNA BINDING PROTEIN; EIF2C2 PROTEIN, MOUSE; MIRN1 MICRORNA, MOUSE; MIRN206 MICRORNA, MOUSE; PROTEIN BINDING; PROTEIN TDP-43; RNA INDUCED SILENCING COMPLEX;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ARTICLE; BIOGENESIS; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE ACTIVITY; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; GENE SILENCING; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; IN VIVO STUDY; MALE; MOUSE; NEUROMUSCULAR DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN RNA BINDING; SMOOTH MUSCLE FIBER; ANIMAL; DROSOPHILA MELANOGASTER; GENETICS; HUMAN; METABOLISM; SKELETAL MUSCLE; TRANSGENIC MOUSE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ARGONAUTE PROTEINS; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; HUMANS; MALE; MICE; MICE, TRANSGENIC; MICRORNAS; MUSCLE, SKELETAL; PROTEIN BINDING; RNA-INDUCED SILENCING COMPLEX;

EID: 84901006597     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.561902     Document Type: Article

References (29)

1. Cordes, K. R., Srivastava, D., and Ivey, K. N. (2010) MicroRNAs in cardiac development. Pediatr. Cardiol. 31, 349-356
2. Gagan, J., Dey, B. K., and Dutta, A. (2012) MicroRNAs regulate and provide robustness to the myogenic transcriptional network. Curr. Opin. Pharmacol. 12, 383-388
3. Kwon, C., Han, Z., Olson, E. N., and Srivastava, D. (2005) MicroRNA1 influences cardiac differentiation in Drosophila and regulates Notch signaling. Proc. Natl. Acad. Sci. U.S.A. 102, 18986-18991
4. Zhao, Y., Samal, E., and Srivastava, D. (2005) Serum response factor regulates a muscle-specific microRNA that targets Hand2 during cardiogenesis. Nature 436, 214-220
5. 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
6. Liu, N., Bezprozvannaya, S., Williams, A. H., Qi, X., Richardson, J. A., Bassel-Duby, R., and Olson, E. N. (2008) microRNA-133a regulates cardiomyocyte proliferation and suppresses smooth muscle gene expression in the heart. Genes Dev. 22, 3242-3254
7. Heidersbach, A., Saxby, C., Carver-Moore, K., Huang, Y., Ang, Y.-S., de Jong, P. J., Ivey, K. N., and Srivastava, D. (2013) microRNA-1 regulates sarcomere formation and suppresses smooth muscle gene expression in the mammalian heart. eLife 2, e01323
8. Zhao, Y., Ransom, J. F., Li, A., Vedantham, V., von Drehle, M., Muth, A. N., Tsuchihashi, T., McManus, M. T., Schwartz, R. J., and Srivastava, D. (2007) Dysregulation of cardiogenesis, cardiac conduction, and cell cycle in mice lacking miRNA-1-2. Cell 129, 303-317
9. Williams, A. H., Valdez, G., Moresi, V., Qi, X., McAnally, J., Elliott, J. L., Bassel-Duby, R., Sanes, J. R., and Olson, E. N. (2009) MicroRNA-206 delays ALS progression and promotes regeneration of neuromuscular synapses in mice. Science 326, 1549-1554
10. Wystub, K., Besser, J., Bachmann, A., Boettger, T., and Braun, T. (2013) miR-1/133a clusters cooperatively specify the cardiomyogenic lineage by adjustment of myocardin levels during embryonic heart development. PLoS Genet 9, e1003793
11. Wei, Y., Peng, S., Wu, M., Sachidanandam, R., Tu, Z., Zhang, S., Falce, C., Sobie, E. A., Lebeche, D., and Zhao, Y. (2014) Multifaceted roles of miR-1s in repressing the fetal gene program in the heart. Cell Res. 24, 278-292
12. Ivey, K. N., Muth, A., Arnold, J., King, F. W., Yeh, R.-F., Fish, J. E., Hsiao, E. C., Schwartz, R. J., Conklin, B. R., Bernstein, H. S., and Srivastava, D. (2008) MicroRNA regulation of cell lineages in mouse and human embryonic stem cells. Cell Stem Cell 2, 219-229
13. Rao, P. K., Missiaglia, E., Shields, L., Hyde, G., Yuan, B., Shepherd, C. J., Shipley, J., and Lodish, H. F. (2010) Distinct roles for miR-1 and miR-133a in the proliferation and differentiation of rhabdomyosarcoma cells. FASEB J. 24, 3427-3437
14. Simon, D. J., Madison, J. M., Conery, A. L., Thompson-Peer, K. L., Soskis, M., Ruvkun, G. B., Kaplan, J. M., and Kim, J. K. (2008) The microRNA miR-1 regulates a MEF-2-dependent retrograde signal at neuromuscular junctions. Cell 133, 903-915
15. Bruneteau, G., Simonet, T., Bauché, S., Mandjee, N., Malfatti, E., Girard, E., Tanguy, M. L., Behin, A., Khiami, F., Sariali, E., Hell-Remy, C., Salachas, F., Pradat, P. F., Fournier, E., Lacomblez, L., Koenig, J., Romero, N. B., Fontaine, B., Meininger, V., Schaeffer, L., and Hantaï, D. (2013) Muscle histone deacetylase 4 upregulation in amyotrophic lateral sclerosis: potential role in reinnervation ability and disease progression. Brain 136, 2359-2368
16. Rao, P. K., Kumar, R. M., Farkhondeh, M., Baskerville, S., and Lodish, H. F. (2006) Myogenic factors that regulate expression of muscle-specific microRNAs. Proc. Natl. Acad. Sci. U.S.A. 103, 8721-8726
17. Liu, N., Williams, A. H., Kim, Y., McAnally, J., Bezprozvannaya, S., Sutherland, L. B., Richardson, J. A., Bassel-Duby, R., and Olson, E. N. (2007) An intragenic MEF2-dependent enhancer directs muscle-specific expression of microRNAs 1 and 133. Proc. Natl. Acad. Sci. U.S.A. 104, 20844-20849
18. Trabucchi, M., Briata, P., Garcia-Mayoral, M., Haase, A. D., Filipowicz, W., Ramos, A., Gherzi, R., and Rosenfeld, M. G. (2009) The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs. Nature 459, 1010-1014
19. Rau, F., Freyermuth, F., Fugier, C., Villemin, J.-P., Fischer, M.-C., Jost, B., Dembele, D., Gourdon, G., Nicole, A., Duboc, D., Wahbi, K., Day, J. W., Fujimura, H., Takahashi, M. P., Auboeuf, D., Dreumont, N., Furling, D., and Charlet-Berguerand, N. (2011) Misregulation of miR-1 processing is associated with heart defects in myotonic dystrophy. Nat. Struct. Mol. Biol. 18, 840-845
20. Rao, P. K., Toyama, Y., Chiang, H. R., Gupta, S., Bauer, M., Medvid, R., Reinhardt, F., Liao, R., Krieger, M., Jaenisch, R., Lodish, H. F., and Blelloch, R. (2009) Loss of cardiac microRNA-mediated regulation leads to dilated cardiomyopathy and heart failure. Circ. Res. 105, 585-594
21. Nielsen, M., Hansen, J. H., Hedegaard, J., Nielsen, R. O., Panitz, F., Bendixen, C., and Thomsen, B. (2010) MicroRNA identity and abundance in porcine skeletal muscles determined by deep sequencing. Anim. Genet. 41, 159-168
22. Darnell, R. (2012) CLIP (cross-linking and immunoprecipitation) identification of RNAs bound by a specific protein. Cold Spring Harb. Protoc. 2012, 1146-1160
23. Lu, Y., Ferris, J., and Gao, F.-B. (2009) Frontotemporal dementia and amyotrophic lateral sclerosis-associated disease protein TDP-43 promotes dendritic branching. Mol. Brain 2, 30
24. Ling, S.-C., Albuquerque, C. P., Han, J. S., Lagier-Tourenne, C., Tokunaga, S., Zhou, H., and Cleveland, D. W. (2010) ALS-associated mutations in TDP-43 increase its stability and promote TDP-43 complexes with FUS/ TLS. Proc. Natl. Acad. Sci. U.S.A. 107, 13318-13323
25. King, I. N., Qian, L., Liang, J., Huang, Y., Shieh, J. T. C., Kwon, C., and Srivastava, D. (2011) A genome-wide screen reveals a role for microRNA-1 in modulating cardiac cell polarity. Dev. Cell 20, 497-510
26. Stallings, N. R., Puttaparthi, K., Luther, C. M., Burns, D. K., and Elliott, J. L. (2010) Progressive motor weakness in transgenic mice expressing human TDP-43. Neurobiol. Dis. 40, 404-414
27. Elia, L., Contu, R., Quintavalle, M., Varrone, F., Chimenti, C., Russo, M. A., Cimino, V., De Marinis, L., Frustaci, A., Catalucci, D., and Condorelli, G. (2009) Reciprocal regulation of microRNA-1 and insulinlike growth factor-1 signal transduction cascade in cardiac and skeletal muscle in physiological and pathological conditions. Circulation 120, 2377-2385
28. Arai, T., Hasegawa, M., Akiyama, H., Ikeda, K., Nonaka, T., Mori, H., Mann, D., Tsuchiya, K., Yoshida, M., Hashizume, Y., and Oda, T. (2006) TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem. Biophys. Res. Commun. 351, 602-611
29. Wang, W. X., Wilfred, B. R., Hu, Y., Stromberg, A. J., and Nelson, P. T. (2010) Anti-Argonaute RIP-Chip shows that miRNA transfections alter global patterns of mRNA recruitment to microribonucleoprotein complexes. RNA 16, 394-404