The spliceosome-activating complex: Molecular mechanisms underlying the function of a pleiotropic regulator

Frontiers in Plant Science

Volumn 3, Issue JAN, 2012, Pages

  Koncz, Csaba ^a,b   deJong, Femke ^a,c,d   Villacorta, Nicolas ^a   Szakonyi, Dóra ^a   Koncz, Zsuzsa ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^b INSTITUTE OF BIOCHEMISTRY   (Hungary)

^c JOHN INNES CENTRE   (United Kingdom)

^d GHENT UNIVERSITY   (Belgium)

Author keywords

Arabidopsis; Cell death signaling; Co transcriptional splicing; DNA repair; NineTeen complex; Spliceosome

Indexed keywords

EID: 84861666408     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2012.00009     Document Type: Review

References (139)

1. Agafonov, D. E., Deckert, J., Wolf, E., Odenwälder, P., Bessonov, S., Will, C. L., Urlaub, H., and Lührmann, R. (2011). Semiquantitative proteomic analysis of the human spliceosome via a novel two-dimensional gel electrophoresis method. Mol. Cell. Biol. 31, 2667-2682.
2. Ajuh, P., Kuster, B., Panov, K., Zomerdijk, J. C., Mann, M., and Lamond, A. I. (2000). Functional analysis of the human CDC5L complex and identification of its components by mass spectrometry. EMBO J. 19, 6569-6581.
3. Ajuh, P., Sleeman, J., Chusainow, J., and Lamond, A. I. (2001). A direct interaction between the carboxyl-terminal region of CDC5L and the WD40 domain of PLRG1 is essential for pre-mRNA splicing. J. Biol. Chem. 276, 42370-42381.
4. Akhtar, M. S., Heidemann, M., Tietjen, J. R., Zhang, D. W., Chapman, R. D., Eick, D., and Ansari, A. Z. (2009). TFIIH kinase places bivalent marks on the carboxy-terminal domain of RNA polymerase II. Mol. Cell 34, 387-393.
5. Aksaas, A. K., Larsen, A. C., Rogne, M., Rosendal, K., Kvissel, A. K., and Skålhegg, B. S. (2011). G-patch domain and KOW motifs-containing protein, GPKOW; a nuclear RNA-binding protein regulated by protein kinase A. J. Mol. Signal. 6, 10.
6. Ambrozková, M., Puta, F., Fuková, I., Skruzný, M., Brábek, J., and Folk, P. (2001). The fission yeast ortholog of the coregulator SKIP interacts with the small subunit of U2AF. Biochem. Biophys. Res. Commun. 284, 1148-1154.
7. Barta, A., Kalyna, M., and Reddy, A. S. (2010). Implementing a rational and consistent nomenclature for serine/arginine-rich protein splicing factors (SR proteins) in plants. Plant Cell 22, 2926-2929.
8. Baruah, A., Simková, K., Hincha, D. K., Apel, K., and Laloi, C. (2009). Modulation of O-mediated retrograde signaling by the PLEIOTROPIC RESPONSE LOCUS 1 (PRL1) protein, a central integrator of stress and energy signaling. Plant J. 60, 22-32.
9. Behzadnia, N., Golas, M. M., Hartmuth, K., Sander, B., Kastner, B., Deckert, J., Dube, P., Will, C. L., Urlaub, H., Stark, H., and Lührmann, R. (2007). Composition and three-dimensional EM structure of double affinity-purified, human prespliceosomal A complexes. EMBO J. 26, 1737-1748.
10. Bessonov, S., Anokhina, M., Krasauskas, A., Golas, M. M., Sander, B., Will, C. L., Urlaub, H., Stark, H., and Lührmann, R. (2010). Characterization of purified human Bact spliceosomal complexes reveals compositional and morphological changes during spliceosome activation and first step catalysis. RNA 16, 2384-2403.
11. Bessonov, S., Anokhina, M., Will, C. L., Urlaub, H., and Lührmann, R. (2008). Isolation of an active step I spliceosome and composition of its RNP core. Nature 452, 846-850.
12. Bhalerao, R. P., Salchert, K., Bakó, L., Ökrész, L., Szabados, L., Muranaka, T., Machida, Y., Schell, J., and Koncz, C. (1999). Regulatory interaction of PRL1 WD protein with Arabidopsis SNF1-like protein kinases. Proc. Natl. Acad. Sci. U.S.A. 96, 5322-5327.
13. Brès, V., Yoshida, T., Pickle, L., and Jones, K. A. (2009). SKIP interacts with c-Myc and Menin to promote HIV-1 Tat transactivation. Mol. Cell 36, 75-87.
14. Brown, J. W., and Simpson, C. G. (1998). Splice site selection in plant pre-mRNA splicing. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 77-95.
15. Buratowski, S. (2009). Progression through the RNA polymerase II CTD cycle. Mol. Cell 36, 541-546.
16. Burns, C. G., Ohi, R., Krainer, A. R., and Gould, K. L. (1999). Evidence that Myb-related CDC5 proteins are required for pre-mRNA splicing. Proc. Natl. Acad. Sci. U.S.A. 96, 13789-13794.
17. Burns, C. G., Ohi, R., Mehta, S., O'Toole, E. T., Winey, M., Clark, T. A., Sugnet, C. W., Ares, M. Jr., and Gould, K. L. (2002). Removal of a single alpha-tubulin gene intron suppresses cell cycle arrest phenotypes of splicing factor mutations in Saccharomyces cerevisiae. Mol. Cell. Biol. 22, 801-815.
18. Casson, S. A., Topping, J. F., and Lindsey, K. (2009). MERISTEM-DEFECTIVE, an RS domain protein, is required for the correct meristem patterning and function in Arabidopsis. Plant J. 57, 857-869.
19. Chan, S. P., and Cheng, S. C. (2005). The Prp19-associated complex is required for specifying interactions of U5 and U6 with pre-mRNA during spliceosome activation. J. Biol. Chem. 280, 31190-31199.
20. Chan, S. P., Kao, D. I., Tsai, W. Y., and Cheng, S. C. (2003). The Prp19p-associated complex in spliceosome activation. Science 302, 279-282.
21. Chanarat, S., Seizl, M., and Sträber, K. (2011). The Prp19 complex is a novel transcription elongation factor required for TREX occupancy at transcribed genes. Genes Dev. 25, 1147-1158.
22. Chang, K. J., Chen, H. C., and Cheng, S. C. (2009). Ntc90 is required for recruiting first step factor Yju2 but not for spliceosome activation. RNA 15, 1729-1739.
23. Chaouki, A. S., and Salz, H. K. (2006). Drosophila SPF45: a bifunctional protein with roles in both splicing and DNA repair. PLoS Genet. 2, e178. doi:10.1371/journal.pgen.0020178
24. Chen, C. H., Kao, D. I., Chan, S. P., Kao, T. C., Lin, J. Y., and Cheng, S. C. (2006). Functional links between the Prp19-associated complex, U4/U6 biogenesis, and spliceosome recycling. RNA 12, 765-774.
25. Chen, C. H., Yu, W. C., Tsao, T. Y., Wang, L. Y., Chen, H. R., Lin, J. Y., Tsai, W. Y., and Cheng, S. C. (2002). Functional and physical interactions between components of the Prp19p-associated complex. Nucleic Acids Res.30, 1029-1037.
26. Chen, Y., Zhang, L., and Jones, K. A. (2011). SKIP counteracts p53-mediated apoptosis via selective regulation of p21Cip1 mRNA splicing. Genes Dev. 25, 701-716.
27. Chu, P. C., Yang, Y. C., Lu, Y. T., Chen, H. T., Yu, L. C., and Chang, M. S. (2006). Silencing of p29 affects DNA damage responses with UV irradiation. Cancer Res. 66, 8484-8491.
28. Chung, S., McLean, M. R., and Rymond, B. C. (2011). Yeast ortholog of the Drosophila crooked neck protein promotes spliceosome assembly through stable U4/U6. U5 snRNP addition. RNA 5, 1042-1054.
29. Chung, S., Zhou, Z., Huddleston, K. A., Harrison, D. A., Reed, R., Coleman, T. A., and Rymond, B. C. (2002). Crooked neck is a component of the human spliceosome and implicated in the splicing process. Biochim. Biophys. Acta1576, 287-297.
30. Dagher, S. F., and Fu, X. D. (2001). Evidence for a role of Sky1p-mediated phosphorylation in 3′ splice site recognition involving both Prp8 and Prp17/Slu4. RNA 7, 1284-1297.
31. David, C. J., Boyne, A. R., Millhouse, S. R., and Manley, J. L. (2011). The RNA polymerase II C-terminal domain promotes splicing activation through recruitment of a U2AF65-Prp19 complex. Genes Dev. 25, 972-983.
32. Deckert, J., Hartmuth, K., Boehringer, D., Behzadnia, N., Will, C. L., Kastner, B., Stark, H., Urlaub, H., and Lührmann, R. (2006). Protein composition and electron microscopy structure of affinity-purified human spliceosomal B complexes isolated under physiological conditions. Mol. Cell. Biol. 26, 5528-5543.
33. Deng, X., Gu, L., Liu, C., Lu, T., Lu, F., Lu, Z., Cui, P., Pei, Y., Wang, B., Hu, S., and Cao, X. (2010). Arginine methylation mediated by the Arabidopsis homolog of PRMT5 is essential for proper pre-mRNA splicing. Proc. Natl. Acad. Sci. U.S.A. 107, 19114-19119.
34. Fabrizio, P., Dannenberg, J., Dube, P., Kastner, B., Stark, H., Urlaub, H., and Lührmann, R. (2009). The evolutionarily conserved core design of the catalytic activation step of the yeast spliceosome. Mol. Cell 36, 593-608.
35. Farrás, R., Ferrando, A., Jásik, J., Kleinow, T., Ökrész, L., Tiburcio, A., Salchert, K., del Pozo, C., Schell, J., and Koncz, C. (2001). SKP1-SnRK protein kinase interactions mediate proteasomal binding of a plant SCF ubiquitin ligase. EMBO J. 20, 2742-2756.
36. Fluhr, R. (2008). Regulation of splicing by protein phosphorylation. Curr. Top. Microbiol. Immunol. 326, 119-138.
37. Fortes, P., Bilbao-Cortés, D., Fornerod, M., Rigaut, G., Raymond, W., Séraphin, B., and Mattaj, I. W. (1999). Luc7p, a novel yeast U1 snRNP protein with a role in 5′ splice site recognition. Genes Dev. 13, 2425-2438.
38. Fortschegger, K., Wagner, B., Voglauer, R., Katinger, H., Sibilia, M., and Grillari, J. (2007). Early embryonic lethality of mice lacking the essential protein SNEV. Mol. Cell. Biol. 27, 3123-3130.
39. Fousteri, M., Vermeulen, W., van Zeeland, A. A., and Mullenders, L. H. (2006). Cockayne syndrome A and B proteins differentially regulate recruitment of chromatin remodeling and repair factors to stalled RNA polymerase II in vivo. Mol. Cell 23, 471-482.
40. Gahura, O., Abrhámová, K., Skruzný, M., Valentová, A., Munzarová, V., Folk, P., and Puta, F. (2009). Prp45 affects Prp22 partition in spliceosomal complexes and splicing efficiency of non-consensus substrates. J. Cell. Biochem.106, 139-151.
41. Gehring, N. H., Kunz, J. B., Neu-Yilik, G., Breit, S., Viegas, M. H., Hentze, M. W., and Kulozik, A. E. (2005). Exon-junction complex components specify distinct routes of nonsense-mediated mRNA decay with differential cofactor requirements. Mol. Cell 20, 65-75.
42. Grainger, R. J., and Beggs, J. D. (2005). Prp8 protein: at the heart of the spliceosome. RNA 11, 533-557.
43. Gräub, R., Lancero, H., Pedersen, A., Chu, M., Padmanabhan, K., Xu, X. Q., Spitz, P., Chalkley, R., Burlingame, A. L., Stokoe, D., and Bernstein, H. S. (2008). Cell cycle-dependent phosphorylation of human CDC5 regulates RNA processing. Cell Cycle 7, 1795-1803.
44. Grillari, J., Löscher, M., Denegri, M., Lee, K., Fortschegger, K., Eisenhaber, F., Ajuh, P., Lamond, A. I., Katinger, H., and Grillari-Voglauer, R. (2009). Blom7alpha is a novel heterogeneous nuclear ribonucleoprotein K homology domain protein involved in pre-mRNA splicing that interacts with SNEVPrp19-Pso4. J. Biol. Chem. 284, 29193-29204.
45. Grote, M., Wolf, E., Will, C. L., Lemm, I., Agafonov, D. E., Schomburg, A., Fischle, W., Urlaub, H., and Lührmann, R. (2010). Molecular architecture of the human Prp19/CDC5L complex. Mol. Cell. Biol. 30, 2105-2119.
46. Gunderson, F. Q., and Johnson, T. L. (2009). Acetylation by the transcriptional coactivator Gcn5 plays a novel role in co-transcriptional spliceosome assembly. PLoS Genet. 5, e1000682. doi:10.1371/journal.pgen.1000682
47. Han, J., Xiong, J., Wang, D., and Fu, X. D. (2011). Pre-mRNA splicing: where and when in the nucleus. Trends Cell Biol. 21, 336-343.
48. Hausmann, S., Zheng, S., Costanzo, M., Brost, R. L., Garcin, D., Boone, C., Shuman, S., and Schwer, B. (2008). Genetic and biochemical analysis of yeast and human cap trimethylguanosine synthase: functional overlap of 2,2,7-trimethylguanosine caps, small nuclear ribonucleoprotein components, pre-mRNA splicing factors, and RNA decay pathways. J. Biol. Chem. 283, 31706-31718.
49. He, F., Wang, C. T., and Gou, L. T. (2009). RNA-binding motif protein RBM22 is required for normal development of zebrafish embryos. Genet. Mol. Res. 8, 1466-1473.
50. Herold, N., Will, C. L., Wolf, E., Kastner, B., Urlaub, H., and Lührmann, R. (2009). Conservation of the protein composition and electron microscopy structure of Drosophila melanogaster and human spliceosomal complexes. Mol. Cell. Biol. 29, 281-301.
51. Herr, A. J., Molnàr, A., Jones, A., and Baulcombe, D. C. (2006). Defective RNA processing enhances RNA silencing and influences flowering of Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 103, 14994-15001.
52. + homolog of a higher plant, Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 93, 13371-13376.
53. Hirose, T., Ideue, T., Nagai, M., Hagiwara, M., Shu, M. D., and Steitz, J. A. (2006) A spliceosomal intron binding protein, IBP160, links position-dependent assembly of intron-encoded box C/D snoRNP to pre-mRNA splicing. Mol. Cell 23, 673-684.
54. Hogg, R., McGrail, J. C., and O'Keefe, R. T. (2010). The function of the nineteen complex (NTC) in regulating spliceosome conformations and fidelity during pre-mRNA splicing. Biochem. Soc. Trans. 38, 1110-1115.
55. Holt, B. F. III, Boyes, D. C., Ellerström, M., Siefers, N., Wiig, A., Kauffman, S., Grant, M. R., and Dangl, J. L. (2002). An evolutionarily conserved mediator of plant disease resistance gene function is required for normal Arabidopsisdevelopment. Dev. Cell 2, 807-817.
56. Kaida, D., Motoyoshi, H., Tashiro, E., Nojima, T., Hagiwara, M., Ishigami, K., Watanabe, H., Kitahara, T., Yoshida, T., Nakajima, H., Tani, T., Horinouchi, S., and Yoshida, M. (2007). Spliceostatin A targets SF3b and inhibits both splicing and nuclear retention of pre-mRNA. Nat. Chem. Biol. 3, 576-583.
57. Kang, C. H., Feng, Y., Vikram, M., Jeong, I. S., Lee, J. R., Bahk, J. D., Yun, D. J., Lee, S. Y., and Koiwa, H. (2009). Arabidopsis thaliana PRP40s are RNA polymerase II C-terminal domain-associating proteins. Arch. Biochem. Biophys. 484, 30-38.
58. Kang, M. R., Lee, S. W., Um, E., Kang, H. T., Hwang, E. S., Kim, E. J., and Um, S. J. (2010). Reciprocal roles of SIRT1 and SKIP in the regulation of RAR activity: implication in the retinoic acid-induced neuronal differentiation of P19 cells. Nucleic Acids Res. 38, 822-831.
59. Khanna, M., Van Bakel, H., Tang, X., Calarco, J. A., Babak, T., Guo, G., Emili, A., Greenblatt, J. F., Hughes, T. R., Krogan, N. J., and Blencowe, B. J. (2009). A systematic characterization of Cwc21, the yeast ortholog of the human spliceosomal protein SRm300. RNA 15, 2174-2185.
60. Kleinridders, A., Pogoda, H. M., Irlenbusch, S., Smyth, N., Koncz, C., Hammerschmidt, M., and Brüning, J. C. (2009). PLRG1 is an essential regulator of cell proliferation and apoptosis during vertebrate development and tissue homeostasis. Mol. Cell. Biol. 29, 3173-3185.
61. Kuo, P. C., Tsao, Y. P., Chang, H. W., Chen, P. H., Huang, C. W., Lin, S. T., Weng, Y. T., Tsai, T. C., Shieh, S. Y., and Chen, S. L. (2009). Breast cancer amplified sequence 2, a novel negative regulator of the p53 tumor suppressor. Cancer Res. 69, 8877-8885.
62. Kuraoka, I., Ito, S., Wada, T., Hayashida, M., Lee, L., Saijo, M., Nakatsu, Y., Matsumoto, M., Matsunaga, T., Handa, H., Qin, J., Nakatani, Y., and Tanaka, K. (2008). Isolation of XAB2 complex involved in pre-mRNA splicing, transcription, and transcription-coupled repair. J. Biol. Chem. 283, 940-950.
63. Lagerwerf, S., Vrouwe, M. G., Overmeer, R. M., Fousteri, M. I., and Mullenders, L. H. (2011). DNA damage response and transcription. DNA Repair (Amst.) 10, 743-750.
64. Laubinger, S., Sachsenberg, T., Zeller, G., Busch, W., Lohmann, J. U., Rätsch, G., and Weigel, D. (2008). Dual roles of the nuclear cap-binding complex and SERRATE in pre-mRNA splicing and microRNA processing in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 105, 8795-8800.
65. Lee, B. H., Kapoor, A., Zhu, J., and Zhu, J. K. (2006). Stabilized1, a stress-upregulated nuclear protein, is required for pre-mRNA splicing, mRNA turnover, and stress tolerance in Arabidopsis. Plant Cell 18, 1736-1749.
66. Lee, J. H., Terzaghi, W., Gusmaroli, G., Charron, J. B., Yoon, H. J., Chen, H., He, Y. J., Xiong, Y., and Deng, X. W. (2008). Characterization of Arabidopsis and rice DWD proteins and their roles as substrate receptors for CUL4-RING E3 ubiquitin ligases. Plant Cell 20, 152-167.
67. Legerski, R. J. (2009). The Pso4 complex splices into the DNA damage response. Cell Cycle 8, 3448-3449.
68. Lenasi, T., and Barboric, M. (2010). P-TEFb stimulates transcription elongation and pre-mRNA splicing through multilateral mechanisms. RNA Biol. 7, 145-150.
69. Leonard, D., Ajuh, P., Lamond, A. I., and Legerski, R. J. (2003). hLodestar/HuF2 interacts with CDC5L and is involved in pre-mRNA splicing. Biochem. Biophys. Res. Commun. 308, 793-801.
70. Lim, G. H., Zhang, X., Chung, M. S., Lee, D. J., Woo, Y. M., Cheong, H. S., and Kim, C. S. (2010). A putative novel transcription factor, AtSKIP, is involved in abscisic acid signalling and confers salt and osmotic tolerance inArabidopsis. New Phytol. 185, 103-113.
71. Lin, Z., Yin, K., Wang, X., Liu, M., Chen, Z., Gu, H., and Qu, L. J. (2007a). Virus induced gene silencing of AtCDC5 results in accelerated cell death in Arabidopsis leaves. Plant Physiol. Biochem. 45, 87-94.
72. Lin, Z., Yin, K., Zhu, D., Chen, Z., Gu, H., and Qu, L. J. (2007b). AtCDC5 regulates the G2 to M transition of the cell cycle and is critical for the function of Arabidopsis shoot apical meristem. Cell Res. 17, 815-828.
73. Liu, M., Yuan, L., Liu, N. Y., Shi, D. Q., Liu, J., and Yang, W. C. (2009). GAMETOPHYTIC FACTOR 1, involved in pre-mRNA splicing, is essential for megagametogenesis and embryogenesis in Arabidopsis. J. Integr. Plant Biol. 51, 261-271.
74. Liu, Y., Xu, X., and Kuo, M. H. (2010). Snf1p regulates Gcn5p transcriptional activity by antagonizing Spt3p. Genetics 184, 91-105.
75. Lo, W. S., Duggan, L., Emre, N. C., Belotserkovskya, R., Lane, W. S., Shiekhattar, R., and Berger, S. L. (2001). Snf1-a histone kinase that works in concert with the histone acetyltransferase Gcn5 to regulate transcription. Science 293, 1142-1146.
76. Lorkovic, Z. J., and Barta, A. (2002). Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana. Nucleic Acids Res. 30, 623-635.
77. Löscher, M., Fortschegger, K., Ritter, G., Wostry, M., Voglauer, R., Schmid, J. A., Watters, S., Rivett, A. J., Ajuh, P., Lamond, A. I., Katinger, H., and Grillari, J. (2005). Interaction of U-box E3 ligase SNEV with PSMB4, the beta7 subunit of the 20 S proteasome. Biochem. J. 388, 593-603.
78. Lu, X., and Legerski, R. J. (2007). The Prp19/Pso4 core complex undergoes ubiquitylation and structural alterations in response to DNA damage. Biochem. Biophys. Res. Commun. 354, 968-974.
79. Luco, R. F., Allo, M., Schor, I. E., Kornblihtt, A. R., and Misteli, T. (2011). Epigenetics in alternative pre-mRNA splicing. Cell 144, 16-26.
80. Mahajan, K. N., and Mitchell, B. S. (2003). Role of human Pso4 in mammalian DNA repair and association with terminal deoxynucleotidyl transferase. Proc. Natl. Acad. Sci. U.S.A. 100, 10746-10751.
81. Makarov, E. M., Makarova, O. V., Urlaub, H., Gentzel, M., Will, C. L., Wilm, M., and Lührmann, R. (2002). Small nuclear ribonucleoprotein remodeling during catalytic activation of the spliceosome. Science 298, 2205-2208.
82. Makarova, O. V., Makarov, E. M., Urlaub, H., Will, C. L., Gentzel, M., Wilm, M., and Lührmann, R. (2004). A subset of human 35S U5 proteins, including Prp19, function prior to catalytic step 1 of splicing. EMBO J. 23, 2381-2391.
83. Martinez, E., Palhan, V. B., Tjernberg, A., Lymar, E. S., Gamper, A. M., Kundu, T. K., Chait, B. T., and Roeder, R. G. (2001). Human STAGA complex is a chromatin-acetylating transcription coactivator that interacts with pre-mRNA splicing and DNA damage-binding factors in vivo. Mol. Cell. Biol. 21, 6782-6795.
84. McDonald, W. H., Ohi, R., Smelkova, N., Frendewey, D., and Gould, K. L. (1999). Myb-related fission yeast cdc5p is a component of a 40S snRNP-containing complex and is essential for pre-mRNA splicing. Mol. Cell. Biol. 19, 5352-5362.
85. Moll, C., von Lyncker, L., Zimmermann, S., Kägi, C., Baumann, N., Twell, D., Grossniklaus, U., and Gross-Hardt, R. (2008). CLO/GFA1 and ATO are novel regulators of gametic cell fate in plants. Plant J. 56, 913-921.
86. Monaghan, J., Xu, F., Gao, M., Zhao, Q., Palma, K., Long, C., Chen, S., Zhang, Y., and Li, X. (2009). Two Prp19-like U-box proteins in the MOS4-associated complex play redundant roles in plant innate immunity. PLoS Pathog. 5, e1000526. doi:10.1371/journal.ppat.1000526
87. Monaghan, J., Xu, F., Xu, S., Zhang, Y., and Li, X. (2010). Two putative RNA-binding proteins function with unequal genetic redundancy in the MOS4-associated complex. Plant Physiol. 154, 1783-1793.
88. Muñoz, M. J., de la Mata, M., and Kornblihtt, A. R. (2010). The carboxy terminal domain of RNA polymerase II and alternative splicing. Trends Biochem. Sci. 35, 497-504.
89. Németh, K., Salchert, K., Putnoky, P., Bhalerao, R., Koncz-Kálmán, Z., Stankovic-Stangeland, B., Bakó, L., Mathur, J., Ökrész, L., Stabel, S., Geigenberger, P., Stitt, M., Rédei, G. P., Schell, J., and Koncz, C. (1998). Pleiotropic control of glucose and hormone responses by PRL1, a nuclear WD protein, in Arabidopsis. Genes Dev. 12, 3059-3073.
90. Oesterreich, F. C., Bieberstein, N., and Neugebauer, K. M. (2011). Pause locally, splice globally. Trends Cell Biol. 21, 328-335.
91. Ohi, M. D., and Gould, K. L. (2002). Characterization of interactions among the Cef1p-Prp19p-associated splicing complex. RNA 8, 798-815.
92. Ohi, M. D., Link, A. J., Ren, L., Jennings, J. L., McDonald, W. H., and Gould, K. L. (2002). Proteomics analysis reveals stable multiprotein complexes in both fission and budding yeasts containing Myb-related Cdc5p/Cef1p, novel pre-mRNA splicing factors, and snRNAs. Mol. Cell. Biol. 22, 2011-2024.
93. Ohi, M. D., Vander Kooi, C. W., Rosenberg, J. A., Ren, L., Hirsch, J. P., Chazin, W. J., Walz, T., and Gould, K. L. (2005). Structural and functional analysis of essential pre-mRNA splicing factor Prp19p. Mol. Cell. Biol. 25, 451-460.
94. Pagnussat, G. C., Yu, H. J., Ngo, Q. A., Rajani, S., Mayalagu, S., Johnson, C. S., Capron, A., Xie, L. F., Ye, D., and Sundaresan, V. (2005). Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development 132, 603-614.
95. Palma, K., Zhang, Y., and Li, X. (2005). An importin alpha homolog, MOS6, plays an important role in plant innate immunity. Curr. Biol. 15, 1129-1135.
96. Palma, K., Zhao, Q., Cheng, Y. T., Bi, D., Monaghan, J., Cheng, W., Zhang, Y., and Li, X. (2007). Regulation of plant innate immunity by three proteins in a complex conserved across the plant and animal kingdoms. Genes Dev. 21, 1484-1493.
97. Perales, R., and Bentley, D. (2009). "Cotranscriptionality": the transcription elongation complex as a nexus for nuclear transactions. Mol. Cell 36, 178-191.
98. Petricka, J. J., Clay, N. K., and Nelson, T. M. (2008). Vein patterning screens and the defectively organized tributaries mutants in Arabidopsis thaliana. Plant J. 56, 251-263.
99. Rappsilber, J., Ryder, U., Lamond, A. I., and Mann, M. (2002). Large-scale proteomic analysis of the human spliceosome. Genome Res. 12, 1231-1245.
100. Reddy, A. S. (2007). Alternative splicing of pre-messenger RNAs in plants in the genomic era. Annu. Rev. Plant Biol. 58, 267-294.
101. Ren, L., McLean, J. R., Hazbun, T. R., Fields, S., Van der Kooi, C., Ohi, M. D., and Gould, K. L. (2011). Systematic two-hybrid and comparative proteomic analyses reveal novel yeast pre-mRNA splicing factors connected to Prp19. PLoS ONE 6, e16719. doi:10.1371/journal.pone.0016719
102. Roy, J., Kim, K., Maddock, J. R., Anthony, J. G., and Woolford, J. L. Jr. (1995). The final stages of spliceosome maturation require Spp2p that can interact with the DEAH box protein Prp2p and promote step 1 of splicing. RNA1, 375-390.
103. Sanchez, S. E., Petrillo, E., Beckwith, E. J., Zhang, X., Rugnone, M. L., Hernando, C. E., Cuevas, J. C., Godoy Herz, M. A., Depetris-Chauvin, A., Simpson, C. G., Brown, J. W., Cerdán, P. D., Borevitz, J. O., Mas, P., Ceriani, M. F., Kornblihtt, A. R., and Yanovsky, M. J. (2010). A methyl transferase links the circadian clock to the regulation of alternative splicing. Nature 468, 112-116.
104. Sapra, A. K., Khandelia, P., and Vijayraghavan, U. (2008). The splicing factor Prp17 interacts with the U2, U5 and U6 snRNPs and associates with the spliceosome pre-and post-catalysis. Biochem. J. 416, 365-374.
105. Sihn, C. R., Cho, S. Y., Lee, J. H., Lee, T. R., and Kim, S. H. (2007). Mouse homologue of yeast Prp19 interacts with mouse SUG1, the regulatory subunit of 26S proteasome. Biochem. Biophys. Res. Commun. 356, 175-180.
106. Simpson, C. G., and Brown, J. W. (2008). U12-dependent intron splicing in plants. Curr. Top. Microbiol. Immunol.326, 61-82.
107. Simpson, C. G., Thow, G., Clark, G. P., Jennings, S. N., Watters, J. A., and Brown, J. W. (2002). Mutational analysis of a plant branch point and polypyrimidine tract required for constitutive splicing of a mini-exon. RNA 8, 47-56.
108. Sims, R. J., Millhouse, S., Chen, C. F., Lewis, B. A., Erdjument-Bromage, H., Tempst, P., Manley, J. L., and Reinberg, D. (2007). Recognition of trimethylated histone H3 lysine 4 facilitates the recruitment of transcription post initiation factors and pre-mRNA splicing. Mol. Cell 28, 665-676.
109. Smith, D. J., Query, C. C., and Konarska, M. M. (2008). "Nought may endure but mutability": spliceosome dynamics and the regulation of splicing. Mol. Cell 30, 657-666.
110. Song, E. J., Werner, S. L., Neubauer, J., Stegmeier, F., Aspden, J., Rio, D., Harper, J. W., Elledge, S. J., Kirschner, M. W., and Rape, M. (2011). The Prp19 complex and the Usp4Sart3 deubiquitinating enzyme control reversible ubiquitination at the spliceosome. Genes Dev. 24, 1434-1447.
111. Song, H. R., Song, J. D., Cho, J. N., Amasino, R. M., Noh, B., and Noh, Y. S. (2009). The RNA binding protein ELF9 directly reduces suppressor of overexpression of CO1 transcript levels in Arabidopsis, possibly via nonsense-mediated mRNA decay. Plant Cell 21, 1195-1211.
112. Spiluttini, B., Gu, B., Belagal, P., Smirnova, A. S., Nguyen, V. T., Hébert, C., Schmidt, U., Bertrand, E., Darzacq, X., and Bensaude, O. (2010). Splicing-independent recruitment of U1 snRNP to a transcription unit in living cells. J. Cell. Sci. 123, 2085-2093.
113. Stevens, S. W., Ryan, D. E., Ge, H. Y., Moore, R. E., Young, M. K., Lee, T. D., and Abelson, J. (2002). Composition and functional characterization of the yeast spliceosomal penta-snRNP. Mol. Cell 9, 31-44.
114. Tanabe, N., Kimura, A., Yoshimura, K., and Shigeoka, S. (2009). Plant-specific SR-related protein atSR45a interacts with spliceosomal proteins in plant nucleus. Plant Mol. Biol. 70, 241-252.
115. Taniue, K., Oda, T., Hayashi, T., Okuno, M., and Akiyama, T. (2011). A member of the ETS family, EHF, and the ATPase RUVBL1 inhibit p53-mediated apoptosis. EMBO Rep. 12, 682-689.
116. Tanuma, N., Kim, S. E., Beullens, M., Tsubaki, Y., Mitsuhashi, S., Nomura, M., Kawamura, T., Isono, K., Koseki, H., Sato, M., Bollen, M., Kikuchi, K., and Shima, H. (2008). Nuclear inhibitor of protein phosphatase-1 (NIPP1) directs protein phosphatase-1 (PP1) to dephosphorylate the U2 small nuclear ribonucleoprotein particle (snRNP) component, spliceosome-associated protein 155 (Sap155). J. Biol. Chem. 283, 35805-35814.
117. Tarn, W. Y., Lee, K. R., and Cheng, S. C. (1993). Yeast precursor mRNA processing protein PRP19 associates with the spliceosome concomitant with or just after dissociation of U4 small nuclear RNA. Proc. Natl. Acad. Sci. U.S.A.90, 10821-10825.
118. Tharun, S. (2009). Roles of eukaryotic Lsm proteins in the regulation of mRNA function. Int. Rev. Cell Mol. Biol.272, 149-189.
119. Valadkhan, S., and Jaladat, Y. (2010). The spliceosomal proteome: at the heart of the largest cellular ribonucleoprotein machine. Proteomics 10, 4128-4141.
120. Villa, T., and Guthrie, C. (2005). The Isy1p component of the NineTeen complex interacts with the ATPase Prp16p to regulate the fidelity of pre-mRNA splicing. Genes Dev. 19, 1894-1904.
121. Voglauer, R., Chang, M. W., Dampier, B., Wieser, M., Baumann, K., Sterovsky, T., Schreiber, M., Katinger, H., and Grillari, J. (2006). SNEV overexpression extends the life span of human endothelial cells. Exp. Cell Res. 312, 746-759.
122. Wahl, M. C., Will, C. L., and Lührmann, R. (2009). The spliceosome: design principles of a dynamic RNP machine. Cell 136, 701-718.
123. Wang, B. B., and Brendel, V. (2004). The ASRG database: identification and survey of Arabidopsis thaliana genes involved in pre-mRNA splicing. Genome Biol. 5, R102.
124. Wang, C., Tian, Q., Hou, Z., Mucha, M., Aukerman, M., and Olsen, O. A. (2007). The Arabidopsis thaliana ATPRP39-1 gene, encoding a tetratricopeptide repeat protein with similarity to the yeast pre-mRNA processing protein PRP39, affects flowering time. Plant Cell Rep. 26, 1357-1366.
125. Wang, Q., He, J., Lynn, B., and Rymond, B. C. (2005). Interactions of the yeast SF3b splicing factor. Mol. Cell. Biol.25, 10745-10754.
126. Wang, Y., Fu, Y., Gao, L., Zhu, G., Liang, J., Gao, C., Huang, B., Fenger, U., Niehrs, C., Chen, Y. G., and Wu, W. (2010). Xenopus skip modulates Wnt/beta-catenin signaling and functions in neural crest induction. J. Biol. Chem.285, 10890-10901.
127. Weber, G., Trowitzsch, S., Kastner, B., Lührmann, R., and Wahl, M. C. (2010). Functional organization of the Sm core in the crystal structure of human U1 snRNP. EMBO J. 29, 4172-4184.
128. Will, C. L., and Lührmann, R. (2011). Spliceosome structure and function. Cold Spring Harb. Perspect. Biol. 3, doi:10.1101/cshperspect.a003707.
129. Xiong, L., Gong, Z., Rock, C. D., Subramanian, S., Guo, Y., Xu, W., Galbraith, D., and Zhu, J. K. (2001). Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis. Dev. Cell 1, 771-781.
130. Xu, D., and Friesen, J. D. (2001). Splicing factor slt11p and its involvement in formation of U2/U6 helix II in activation of the yeast spliceosome. Mol. Cell. Biol. 21, 1011-1023.
131. Yagi, N., Takeda, S., Matsumoto, N., and Okada, K. (2009). VAJ/GFA1/CLO is involved in the directional control of floral organ growth. Plant Cell Physiol. 50, 515-527.
132. Yeh, T. C., Liu, H. L., Chung, C. S., Wu, N. Y., Liu, Y. C., and Cheng, S. C. (2011). Splicing factor Cwc22 is required for the function of Prp2 and for the spliceosome to escape from a futile pathway. Mol. Cell. Biol. 31, 43-53.
133. Yoshida, S., Ito, M., Nishida, I., and Watanabe, A. (2001). Isolation and RNA gel blot analysis of genes that could serve as potential molecular markers for leaf senescence in Arabidopsis thaliana. Plant Cell Physiol. 42, 170-178.
134. Zhang, N., Kaur, R., Akhter, S., and Legerski, R. J. (2009). Cdc5L interacts with ATR and is required for the S-phase cell-cycle checkpoint. EMBO Rep. 10, 1029-1035.
135. Zhang, Y., Cheng, Y. T., Bi, D., Palma, K., and Li, X. (2005a). MOS2, a protein containing G-patch and KOW motifs, is essential for innate immunity in Arabidopsis thaliana. Curr. Biol. 15, 1936-1942.
136. Zhang, N., Kaur, R., Lu, X., Shen, X., Li, L., and Legerski, R. J. (2005b). The Pso4 mRNA splicing and DNA repair complex interacts with WRN for processing of DNA interstrand cross-links. J. Biol. Chem. 280, 40559-40567.
137. Zhou, S., and Hayward, S. D. (2001). Nuclear localization of CBF1 is regulated by interactions with the SMRT corepressor complex. Mol. Cell. Biol. 21, 6222-6232.
138. Zhou, Z., Licklider, L. J., Gygi, S. P., and Reed, R. (2002). Comprehensive proteomic analysis of the human spliceosome. Nature 419, 182-185.
139. Zhu, W., Rainville, I. R., Ding, M., Bolus, M., Heintz, N. H., and Pederson, D. S. (2002). Evidence that the pre-mRNA splicing factor Clf1p plays a role in DNA replication in Saccharomyces cerevisiae. Genetics 160, 1319-1333.