The conserved ubiquitin-like protein Hub1 plays a critical role in splicing in human cells

Journal of Molecular Cell Biology

Volumn 6, Issue 4, 2014, Pages 312-323

  Ammon, Tim ^a   Mishra, Shravan Kumar ^a,b   Kowalska, Kaja ^a   Popowicz, Grzegorz M ^a,c   Holak, Tad A ^a,d   Jentsch, Stefan ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b INDIAN INSTITUTE OF SCIENCE EDUCATION AND RESEARCH MOHALI   (India)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

apoptosis; Hub1; spliceosome; splicing; ubiquitin like proteins

Indexed keywords

HUB1 PROTEIN; MESSENGER RNA; PROTEIN; SNU66 PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG; RNA PRECURSOR; SACCHAROMYCES CEREVISIAE PROTEIN; SMALL INTERFERING RNA; SMALL NUCLEAR RIBONUCLEOPROTEIN; SNU66 PROTEIN, S CEREVISIAE;

APOPTOSIS; ARTICLE; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; EXON SKIPPING; FEMALE; HUMAN; HUMAN CELL; IN VIVO STUDY; INTRON RETENTION; MITOSIS; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN PROCESSING; SPLICEOSOME; SPLICING DEFECT; ALTERNATIVE RNA SPLICING; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL SURVIVAL; EXON; GENETICS; GROWTH, DEVELOPMENT AND AGING; INTRON; METABOLISM; PATHOLOGY; SACCHAROMYCES CEREVISIAE;

ALTERNATIVE SPLICING; CELL SURVIVAL; CELLS, CULTURED; EXONS; HUMANS; INTRONS; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA PRECURSORS; RNA, MESSENGER; RNA, SMALL INTERFERING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPLICEOSOMES; UBIQUITINS;

EID: 84905166370     PISSN: 16742788     EISSN: 17594685     Source Type: Journal    
DOI: 10.1093/jmcb/mju026     Document Type: Article

References (62)

1. Ahn, E.-Y., DeKelver, R.C., Lo,M.-C., et al. (2011).SONcontrols cell-cycle progression by coordinated regulation of RNA splicing. Mol. Cell 42, 185-198.
2. Bae, J., Leo, C.P., Hsu, S.Y., et al. (2000). MCL-1S, a splicing variant of the antiapoptotic BCL-2 family member MCL-1, encodes a proapoptotic protein possessing only the BH3 domain. J. Biol. Chem. 275, 25255-25261.
3. Bartke, T., Pohl, C., Pyrowolakis, G., et al. (2004). Dual role of BRUCE as an antiapoptotic IAP and a chimeric E2/E3 ubiquitin ligase. Mol. Cell 14, 801-811.
4. Benedetti, C., Haynes, C.M., Yang, Y., et al. (2006). Ubiquitin-like protein 5 positively regulates chaperone gene expression in the mitochondrial unfolded protein response. Genetics 174, 229-239.
5. Bessonov, S., Anokhina, M., Will, C.L., et al. (2008). Isolation of an active step I spliceosome and composition of its RNP core. Nature 452, 846-850.
6. Carpenter, A.E., Jones, T.R., Lamprecht, M.R., et al. (2006). CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol. 7, R100.
7. Clark, T.A., Schweitzer, A.C., Chen, T.X., et al. (2007). Discovery of tissue-specific exons using comprehensive human exon microarrays. Genome Biol. 8, R64.
8. Collaborative Computational Project, Number 4. (1994). The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763.
9. Deckert, J., Hartmuth, K., Boehringer, D., et al. (2006). Protein composition and electron microscopy structure of affinity-purified human spliceosomal B complexes isolated under physiological conditions. Mol. Cell. Biol. 26, 5528-5543.
10. Deveraux, Q.L., Leo, E., Stennicke, H.R., et al. (1999). Cleavage of human inhibitor of apoptosis protein XIAP results in fragments with distinct specificities for caspases. EMBO J. 18, 5242-5251.
11. Dias, A.P.,Dufu, K., Lei, H., et al. (2010). A role for TREX components in the release of spliced mRNA from nuclear speckle domains. Nat. Commun. 1, 1-10.
12. Dikic, I., Wakatsuki, S., and Walters, K.J. (2009). Ubiquitin-binding domains-from structures to functions. Nat. Rev. Mol. Cell Biol. 10, 659-671.
13. Dittmar, G.A.G., Wilkinson, C.R.M., Jedrzejewski, P.T., et al. (2002). Role of a ubiquitin-like modification in polarized morphogenesis. Science 295, 2442-2446.
14. Elbashir, S.M., Harborth, J., Lendeckel, W., et al. (2001). Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411, 494-498.
15. Fink, G.R. (1987). Pseudogenes in yeast? Cell 49, 5-6.
16. Gardina, P.J., Clark, T.A., Shimada, B., et al. (2006). Alternative splicing and differential gene expression in colon cancer detected by a whole genome exon array. BMC Genomics 7, 325.
17. Graham, I.R., Hamshere, M., and Eperon, I.C. (1992). Alternative splicing of a human alpha-tropomyosin muscle-specific exon: identification of determining sequences. Mol. Cell. Biol. 12, 3872-3882.
18. Gupta, M., Mungai, P.T., and Goldwasser, E. (2000). A newtransacting factor that modulates hypoxia-induced expression of the erythropoietin gene. Blood 96, 491-497.
19. Hatanaka, K., Ikegami, K., Takagi, H., et al. (2006). Hypo-osmotic shock induces nuclear export and proteasome-dependent decrease of UBL5. Biochem. Biophys. Res. Commun. 350, 610-615.
20. Haynes, C.M.C., Petrova, K.K., Benedetti, C.C., et al. (2007). ClpP mediates activation of a mitochondrial unfolded protein response in C. elegans. Dev. Cell 13, 467-480.
21. Hochstrasser, M. (2000). Evolution and function of ubiquitin-like proteinconjugation systems. Nat. Cell Biol. 2, E153-E157.
22. Hofmann, J.C., Husedzinovic, A., and Gruss, O.J. (2010). The function of spliceosome components in open mitosis. Nucleus 1, 447-459.
23. Huang, S., and Spector, D.L. (1992).U1 andU2 small nuclear RNAs are present in nuclear speckles. Proc. Natl Acad. Sci. USA 89, 305-308.
24. Jiménez-Garća, L.F., and Spector, D.L. (1993). In vivo evidence that transcription and splicing are coordinated by a recruiting mechanism. Cell 73, 47-59.
25. Kabsch, W. (1993). Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795-800.
26. Kaida, D., Motoyoshi, H., Tashiro, E., et al. (2007). Spliceostatin A targets SF3b and inhibits both splicing and nuclear retention of pre-mRNA. Nat. Chem. Biol. 3, 576-583.
27. Kanda, T., Sullivan, K.F., and Wahl, G.M. (1998). Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells. Curr. Biol. 8, 377-385.
28. Kantham, L., Kerr-Bayles, L., Godde, N., et al. (2003). Beaconinteracts with cdc2/cdc28-like kinases. Biochem. Biophys. Res. Commun. 304, 125-129.
29. Keren, H., Lev-Maor, G., and Ast, G. (2010). Alternative splicing and evolution: diversification, exon definition and function. Nat. Rev. Genet. 11, 345-355.
30. Laetsch, T.W., Liu, X., Vu, A., et al. (2014). Multiple components of the spliceosome regulate Mcl1 activity in neuroblastoma. Cell Death Dis. 5, e1072-e1012.
31. Lamond, A.I., and Spector, D.L. (2003). Nuclear speckles: a model for nuclear organelles. Nat. Rev. Mol. Cell Biol. 4, 605-612.
32. Lamzin, V.S., and Wilson, K.S. (1993). Automated refinement of protein models. Acta Crystallogr. D Biol. Crystallogr. 49, 129-147.
33. Lerner, E.A., Lerner, M.R., Janeway, C.A., et al. (1981). Monoclonal antibodies to nucleic acid-containing cellular constituents: probes for molecular biology and autoimmune disease. Proc. Natl Acad. Sci. USA 78, 2737-2741.
34. Lin, S., Coutinho-Mansfield, G., Wang, D., et al. (2008). The splicing factor SC35 has an active role in transcriptional elongation. Nat. Struct. Mol. Biol. 15, 819-826.
35. Liu, S., Rauhut, R., Vornlocher, H.-P., et al. (2006). The network of protein-protein interactions within the human U4/U6.U5 tri-snRNP. RNA 12, 1418-1430.
36. Luders, J., Pyrowolakis, G., and Jentsch, S. (2003). The ubiquitin-like protein HUB1 forms SDS-resistant complexes with cellular proteins in the absence of ATP. EMBO Rep. 4, 1169-1174.
37. Makarova, O.V., Makarov, E.M., and Lührmann, R. (2001). The 65 and 110 kDa SR-related proteins of the U4/U6.U5 tri-snRNP are essential for the assembly of mature spliceosomes. EMBO J. 20, 2553-2563.
38. McNally, T., Huang, Q., Janis, R., et al. (2003). Structural analysis of UBL5, a novel ubiquitin-like modifier. Protein Sci. 12, 1562-1566.
39. McRee, D.E. (1999). XtalView/Xfit-a versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125, 156-165.
40. Mishra, S.K., Ammon, T., Popowicz, G.M., et al. (2011). Role of the ubiquitin-like protein Hub1 in splice-site usage and alternative splicing.Nature 474, 173-178.
41. Misteli, T., Caceres, J.F., and Spector, D.L. (1997). The dynamics of a pre-mRNA splicing factor in living cells. Nature 387, 523-527.
42. Muro, A.F., Caputi, M., Pariyarath, R., et al. (1999). Regulation of fibronectin EDA exon alternative splicing: possible role of RNA secondary structure for enhancer display. Mol. Cell. Biol. 19, 2657-2671.
43. Neumann, B., Walter, T., Hériché, J.-K., et al. (2010). Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes. Nature 464, 721-727.
44. Noda, N.N., Kumeta, H., Nakatogawa, H., et al. (2008). Structural basis of target recognition by Atg8/LC3 during selective autophagy. Genes Cells 13, 1211-1218.
45. O'Keefe, R.T., Mayeda, A., Sadowski, C.L., et al. (1994). Disruption of pre-mRNA splicing in vivo results in reorganization of splicing factors. J. Cell Biol. 124, 249-260.
46. Politz, J.C.R., Tuft, R.A., Prasanth, K.V., et al. (2006). Rapid, diffusional shuttling of poly(A) RNA between nuclear speckles and the nucleoplasm. Mol. Biol. Cell 17, 1239-1249.
47. Ramelot, T.A., Cort, J.R., Yee, A.A., et al. (2003). Solution structure of the yeast ubiquitin-like modifier protein Hub1. J. Struct. Funct. Genomics 4, 25-30.
48. Rasche, A., and Herwig, R. (2010). ARH: predicting splice variants from genomewide data with modified entropy. Bioinformatics 26, 84-90.
49. Sharma, A., Markey, M., Torres-Muñoz, K., et al. (2011). Son maintains accurate splicing for a subset of human pre-mRNAs. J. Cell Sci. 124, 4286-4298.
50. Sleeman, J., Lyon, C.E., Platani, M., et al. (1998). Dynamic interactions between splicing snRNPs, coiled bodies and nucleoli revealed using snRNP protein fusions to the green fluorescent protein. Exp. Cell Res. 243, 290-304.
51. Song, J., Zhang, Z.M., Hu, W.D., et al. (2005). Small ubiquitin-like modifier (SUMO) recognition of a SUMO binding motif-a reversal of the bound orientation. J. Biol. Chem. 280, 40122-40129.
52. Spector, D.L., and Lamond, A.I. (2011). Nuclear speckles. Cold Spring Harb. Perspect. Biol. 3, a000646.
53. Stoss, O., Stoilov, P., Hartmann, A.M., et al. (1999). The in vivo minigene approach to analyze tissue-specific splicing. Brain Res. Brain Res. Protoc. 4, 383-394.
54. Svéda, M.,Castorálová M., Lipov, J., et al. (2013). Human UBL5 protein interacts with coilin and meets the Cajal bodies. Biochem. Biophys. Res. Commun. 436,240-245.
55. Tanackovic, G., and Krämer, A. (2005).Humansplicing factor SF3a, but not SF1, is essential for pre-mRNA splicing in vivo. Mol. Biol. Cell 16, 1366-1377.
56. Tokunaga, K., and Tani, T. (2008). Monitoring mRNA export. Curr. Protoc. Cell Biol. Chapter 22, Unit 22.13.
57. Venables, J.P. (2004). Aberrant and alternative splicing in cancer. Cancer Res. 64, 7647-7654.
58. Wang, Z., Hoffmann, H.M., and Grabowski, P.J. (1995). Intrinsic U2AF binding is modulated by exon enhancer signals in parallel with changes in splicing activity. RNA 1, 21-35.
59. Wilkinson, C., Dittmar, G., Ohi, M., et al. (2004). Ubiquitin-like protein hub1 is required for pre-mRNA splicing and localization of an essential splicing factor in fission yeast. Curr. Biol. 14, 2283-2288.
60. Wu, J.Y., and Maniatis, T. (1993). Specific interactions between proteins implicated in splice site selection and regulated alternative splicing. Cell 75, 1061-1070.
61. Xing, Y., Stoilov, P., Kapur, K., et al. (2008). MADS: a new and improved method for analysis of differential alternative splicing by exon-tiling microarrays. RNA 14, 1470-1479.
62. Yashiroda, H., and Tanaka, K. (2004). Hub1 is an essential ubiquitin-like protein without functioning as a typical modifier in fission yeast. Genes Cells 9, 1189-1197.