Gemin5 binds to the survival motor neuron mRNA to regulate SMN expression

Journal of Biological Chemistry

Volumn 290, Issue 25, 2015, Pages 15662-15669

  Workman, Eileen ^a   Kalda, Caitlin ^a   Patel, Aalapi ^a   Battle, Daniel J ^a  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEURODEGENERATIVE DISEASES; NEURONS;

BINDING PROTEINS; FEEDBACK MECHANISMS; HIGH SPECIFICITY; MRNA EXPRESSION; SPINAL MUSCULAR ATROPHY; STRUCTURAL ELEMENTS; SURVIVAL MOTOR NEURONS; UNTRANSLATED REGIONS;

PROTEINS;

GEMIN 5; MESSENGER RNA; RNA BINDING PROTEIN; SURVIVAL MOTOR NEURON PROTEIN; UNCLASSIFIED DRUG; GEMIN5 PROTEIN, HUMAN; GEMIN5 PROTEIN, MOUSE; NUCLEAR PROTEIN; PROTEIN BINDING; SMALL NUCLEAR RIBONUCLEOPROTEIN; SMN1 PROTEIN, HUMAN; SMN1 PROTEIN, MOUSE; SURVIVAL MOTOR NEURON PROTEIN 1;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; AUTOREGULATION; CONTROLLED STUDY; ENZYME REGULATION; FEEDBACK SYSTEM; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; POLYSOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; RNA TRANSLATION; ANIMAL; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; HELA CELL LINE; HUMAN; METABOLISM; PHYSIOLOGY; PROTEIN SYNTHESIS;

ANIMALS; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; MICE; NUCLEAR PROTEINS; POLYRIBOSOMES; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA, MESSENGER; SURVIVAL OF MOTOR NEURON 1 PROTEIN;

EID: 84940093430     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.646257     Document Type: Article

References (39)

1. Eggert, C., Chari, A., Laggerbauer, B., and Fischer, U. (2006) Spinal muscular atrophy: the RNP connection. Trends Mol. Med. 12, 113-121
2. Fischer, U., Englbrecht, C., and Chari, A. (2011) Biogenesis of spliceosomal small nuclear ribonucleoproteins. Wiley Interdiscip. Rev. RNA 2, 718-731
3. Liu, Q., Fischer, U., Wang, F., and Dreyfuss, G. (1997) The Spinal Muscular Atrophy Disease Gene Product, SMN, and Its Associated Protein SIP1 Are in a Complex with Spliceosomal snRNP Proteins. Cell 90, 1013-1021
4. Meister, G., Eggert, C., and Fischer, U. (2002) SMN-mediated assembly of RNPs: a complex story. Trends Cell Biol. 12, 472-478
5. Paushkin, S., Gubitz, A. K., Massenet, S., and Dreyfuss, G. (2002) The SMN complex, an assemblyosome of ribonucleoproteins. Curr. Opin. Cell Biol. 14, 305-312
6. Simic, G. (2008) Pathogenesis of proximal autosomal recessive spinal muscular atrophy. Acta Neuropathol. 116, 223-234
7. Wan, L., Battle, D. J., Yong, J., Gubitz, A. K., Kolb, S. J., Wang, J., and Dreyfuss, G. (2005) The Survival of Motor Neurons Protein Determines the Capacity for snRNP Assembly: Biochemical Deficiency in Spinal Muscular Atrophy. Mol. Cell Biol. 25, 5543-5551
8. Achsel, T., Stark, H., and Luhrmann, R. (2001) The Sm domain is an ancient RNA-binding motif with oligo(U) specificity. Proc. Natl. Acad. Sci. U.S.A. 98, 3685-3689
9. Kambach, C., Walke, S., and Nagai, K. (1999) Structure and assembly of the spliceosomal small nuclear ribonucleoprotein particles. Curr. Opin. Struct. Biol. 9, 222-230
10. Stark, H., Dube, P., Luhrmann, R., and Kastner, B. (2001) Arrangement of RNA and proteins in the spliceosomal U1 small nuclear ribonucleoprotein particle. Nature 409, 539-542
11. Battle, D. J., Lau, C. K., Wan, L., Deng, H., Lotti, F., and Dreyfuss, G. (2006) The Gemin5 protein of the SMN complex identifies snRNAs. Mol. Cell 23, 273-279
12. Yong, J., Kasim, M., Bachorik, J. L., Wan, L., and Dreyfuss, G. (2010) Gemin5 Delivers snRNA Precursors to the SMN Complex for snRNP Biogenesis. Mol. Cell 38, 551-562
13. Lau, C. K., Bachorik, J. L., and Dreyfuss, G. (2009) Gemin5-snRNA interaction reveals an RNA binding function for WD repeat domains. Nat. Struct. Mol. Biol. 16, 486-491
14. Golembe, T. J., Yong, J., and Dreyfuss, G. (2005) Specific Sequence Features, Recognized by the SMN Complex, Identify snRNAs and Determine Their Fate as snRNPs. Mol. Cell Biol. 25, 10989-11004
15. Castello, A., Fischer, B., Eichelbaum, K., Horos, R., Beckmann, B. M., Strein, C., Davey, N. E., Humphreys, D. T., Preiss, T., Steinmetz, L. M., Krijgsveld, J., and Hentze, M. W. (2012) Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 149, 1393-1406
16. Fierro-Monti, I., Mohammed, S., Matthiesen, R., Santoro, R., Burns, J. S., Williams, D. J., Proud, C. G., Kassem, M., Jensen, O. N., and Roepstorff, P. (2006) Quantitative proteomics identifies Gemin5, a scaffolding protein involved in ribonucleoprotein assembly, as a novel partner for eukaryotic initiation factor 4E. J. Proteome Res. 5, 1367-1378
17. Pacheco, A., López de Quinto, S., Ramajo, J., Fernández, N., and Martínez-Salas, E. (2009) A novel role for Gemin5 in mRNA translation. Nucleic Acids Res. 37, 582-590
18. Bradrick, S. S., and Gromeier, M. (2009) Identification of gemin5 as a novel 7-methylguanosine cap-binding protein. PLoS ONE 4, e7030
19. Lefebvre, S., Bürglen, L., Reboullet, S., Clermont, O., Burlet, P., Viollet, L., Benichou, B., Cruaud, C., Millasseau, P., Zeviani, M., and et al. (1995) Identification and characterization of a spinal muscular atrophy-determining gene. Cell 80, 155-165
20. Gabanella, F., Carissimi, C., Usiello, A., and Pellizzoni, L. (2005) The activity of the spinal muscular atrophy protein is regulated during development and cellular differentiation. Hum. Mol. Genet. 14, 3629-3642
21. Winkler, C., Eggert, C., Gradl, D., Meister, G., Giegerich, M., Wedlich, D., Laggerbauer, B., and Fischer, U. (2005) Reduced U snRNP assembly causes motor axon degeneration in an animal model for spinal muscular atrophy. Genes Dev. 19, 2320-2330
22. Arnold, W. D., and Burghes, A. H. (2013) Spinal muscular atrophy: Development and implementation of potential treatments. Ann. Neurol. 74, 348-362
23. Workman, E., Veith, A., and Battle, D. J. (2014) U1A regulates 3′ processing of the survival motor neuron mRNA. J. Biol. Chem. 289, 3703-3712
24. Hafner, M., Landthaler, M., Burger, L., Khorshid, M., Hausser, J., Berninger, P., Rothballer, A., Ascano, M., Jungkamp, A. C., Munschauer, M., Ulrich, A., Wardle, G. S., Dewell, S., Zavolan, M., and Tuschl, T. (2010) PAR-CliP-a method to identify transcriptome-wide the binding sites of RNA binding proteins. J. Vis. Exp. 41, e2034
25. Mukherjee, C., Patil, D. P., Kennedy, B. A., Bakthavachalu, B., Bundschuh, R., and Schoenberg, D. R. (2012) Identification of cytoplasmic capping targets reveals a role for cap homeostasis in translation and mRNA stability. Cell Rep. 2, 674-684
26. Hafner, M., Landthaler, M., Burger, L., Khorshid, M., Hausser, J., Berninger, P., Rothballer, A., Ascano, M., Jr., Jungkamp, A. C., Munschauer, M., Ulrich, A., Wardle, G. S., Dewell, S., Zavolan, M., and Tuschl, T. (2010) Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141, 129-141
27. Battle, D. J., Kasim, M., Wang, J., and Dreyfuss, G. (2007) SMN-independent subunits of the SMN complex. Identification of a small nuclear ribonucleoprotein assembly intermediate. J. Biol. Chem. 282, 27953-27959
28. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31, 3406-3415
29. Piñeiro, D., Fernández, N., Ramajo, J., and Martínez-Salas, E. (2013) Gemin5 promotes IRES interaction and translation control through its C-terminal region. Nucleic Acids Res. 41, 1017-1028
30. Gubitz, A. K., Mourelatos, Z., Abel, L., Rappsilber, J., Mann, M., and Dreyfuss, G. (2002) Gemin5, a novel WD repeat protein component of the SMN complex that binds Sm proteins. J. Biol. Chem. 277, 5631-5636
31. Feng, W., Gubitz, A. K., Wan, L., Battle, D. J., Dostie, J., Golembe, T. J., and Dreyfuss, G. (2005) Gemins modulate the expression and activity of the SMN complex. Hum. Mol. Genet. 14, 1605-1611
32. Todd, A. G., Morse, R., Shaw, D. J., Stebbings, H., and Young, P. J. (2010) Analysis of SMN-neurite granules: Core Cajal body components are absent from SMN-cytoplasmic complexes. Biochem. Biophys. Res. Commun. 397, 479-485
33. Jablonka, S., and Sendtner, M. (2003) Molecular and cellular basis of spinal muscular atrophy. Amyotroph. Lateral Scler Other Motor Neuron Disord. 4, 144-149
34. Zhang, H. L., Pan, F., Hong, D., Shenoy, S. M., Singer, R. H., and Bassell, G. J. (2003) Active Transport of the Survival Motor Neuron Protein and the Role of Exon-7 in Cytoplasmic Localization. J. Neurosci. 23, 6627-6637
35. Rossoll, W., Jablonka, S., Andreassi, C., Kröning, A. K., Karle, K., Monani, U. R., and Sendtner, M. (2003) Smn, the spinal muscular atrophy-determining gene product, modulates axon growth and localization of beta-actin mRNA in growth cones of motoneurons. J. Cell Biol. 163, 801-812
36. Hubers, L., Valderrama-Carvajal, H., Laframboise, J., Timbers, J., Sanchez, G., and Côté, J. (2011) HuD interacts with survival motor neuron protein and can rescue spinal muscular atrophy-like neuronal defects. Hum. Mol. Genet. 20, 553-579
37. Fallini, C., Zhang, H., Su, Y., Silani, V., Singer, R. H., Rossoll, W., and Bassell, G. J. (2011) The survival of motor neuron (SMN) protein interacts with the mRNA-binding protein HuD and regulates localization of poly(A) mRNA in primary motor neuron axons. J. Neurosci. 31, 3914-3925
38. Peter, C. J., Evans, M., Thayanithy, V., Taniguchi-Ishigaki, N., Bach, I., Kolpak, A., Bassell, G. J., Rossoll, W., Lorson, C. L., Bao, Z. Z., and Androphy, E. J. (2011) The COPI vesicle complex binds and moves with survival motor neuron within axons. Hum. Mol. Genet. 20, 1701-1711
39. Todd, A. G., Lin, H., Ebert, A. D., Liu, Y., and Androphy, E. J. (2013) COPI transport complexes bind to specific RNAs in neuronal cells. Hum. Mol. Genet. 22, 729-736