Current Science

Open Access Open Access  Restricted Access Subscription Access

Spliceosomal Proteins Encoded by Fungal Genomes


Affiliations
1 Abteilung Botanische Genetik und Molekularbiologie, Botanisches Institut und Botanischer Garten, Christian-Albrechts-Universitat zu Kiel, Olshausenstr. 40 24098 Kiel, Germany
2 Molecular Genetic Epidemiology (C050), German Cancer Research Center (DKFZ), Im Neuenheimer Feld 580 69120 Heidelberg, Germany
 

A large number of spliceosomal proteins are required for proper RNA splicing. While spliceosomal proteins from several model organisms have been analysed, only limited studies are available for fungal species. Hence, we have performed a comparative genomic analysis using eight fungal species belonging to three taxa (Ascomycetes, Basidiomycetes and Glomeromycota). We identified variable number of spliceosomal proteins in fungal species. From the small nuclear ribonucleoproteins (snRNPs), all the snRNPs were identified. In non-snRNPs, only some sub-groups were found extensively conserved in all fungal species, including PRP19 complex proteins, catalytic step II and late-acting proteins. In heterogeneous nuclear ribonucleoproteins (hnRNPs), variable number of proteins was identified. The number of spliceosomal proteins identified in filamentous fungi was higher than that in yeast. The collection of these spliceosomal proteins provides further insight into pre-mRNA splicing in fungi.

Keywords

Fungal Genomes, pre-mRNA, snRNPs, Spliceosomal Proteins.
User
Notifications
Font Size

  • Brow, D. A., Allosteric cascade of spliceosome activation. Annu. Rev. Genet., 2002, 36, 333–360.

  • Irimia, M. and Roy, S. W., Origin of spliceosomal introns and alternative splicing. Cold Spring Harb. Perspect. Biol., 2014, 6.

  • Calarco, J. A., Zhen, M. and Blencowe, B. J., Networking in a global world: establishing functional connections between neural splicing regulators and their target transcripts. RNA, 2011, 17, 775–791.

  • Hoskins, A. A. and Moore, M. J., The spliceosome: a flexible, reversible macromolecular machine. Trends Biochem. Sci., 2012, 37, 179–188.

  • Ramani, A. K. et al., Genome-wide analysis of alternative splicing in Caenorhabditis elegans. Genome Res., 2011, 21, 342–348.

  • Will, C. L. and Luhrmann, R., Spliceosome structure and function. Cold Spring Harb. Perspect. Biol., 2011, 3.

  • Will, C. L. and Lührmann, R., The RNA World, Cold Spring Harbor Laboratory Press, New York, 2006.

  • Yu, B. et al., Spliceosomal genes in the D. discoideum genome: A comparison with those in H. sapiens, D. melanogaster, A. thaliana and S. cerevisiae. Protein Cell, 2011, 2, 395–409.

  • Beggs, J. D., Lsm proteins and RNA processing. Biochem. Soc. Trans., 2005, 33, 433–438.

  • He, W. and Parker, R., Functions of lsm proteins in mRNA degradation and splicing. Curr. Opin. Cell Biol., 2000, 12, 346–350.

  • Salgado-Garrido, J., Bragado-Nilsson, E., Kandels-Lewis, S. and Seraphin, B., Sm and Sm-like proteins assemble in two related complexes of deep evolutionary origin. EMBO. J., 1999, 18, 3451–3462.

  • Fromont-Racine, M., Rain, J. C. and Legrain, P., Toward a functional analysis of the yeast genome through exhaustive two-hybrid screens. Nat. Genet., 1997, 16, 277–282.

  • Klein Gunnewiek, J. M., Hussein, R. I., van Aarssen, Y., Palacios, D., de Jong, R., van Venrooij, W. J. and Gunderson, S. I., Fourteen residues of the U1 snRNP-specific U1a protein are required for homodimerization, cooperative RNA binding, and inhibition of polyadenylation. Mol. Cell Biol., 2000, 20, 2209–2217.

  • Aasland, R., Stewart, A. F. and Gibson, T., The SANT domain: a putative DNA-binding domain in the SWI-SNF and ADA complexes, the transcriptional co-repressor N-CoR and TFIIIB. Trends Biochem. Sci., 1996, 21, 87–88.

  • Chaudhury, A., Chander, P. and Howe, P. H., Heterogeneous nuclear ribonucleoproteins (hnrNPS) in cellular processes: focus on hnRNP E1’s multifunctional regulatory roles. RNA, 2010, 16, 1449–1462.

  • Dreyfuss, G., Matunis, M. J., Pinol-Roma, S. and Burd, C. G., hnRNP proteins and the biogenesis of mRNA. Annu. Rev. Biochem., 1993, 62, 289–321.

  • Mourelatos, Z., Abel, L., Yong, J., Kataoka, N. and Dreyfuss, G., Smn interacts with a novel family of hnRNP and spliceosomal proteins. Embo. J., 2001, 20, 5443–5452.

  • Miau, L. H., Chang, C. J., Shen, B. J., Tsai, W. H. and Lee, S. C., Identification of heterogeneous nuclear ribonucleoprotein K (hnRNP K) as a repressor of C/EBP -mediated gene activation. J. Biol. Chem., 1998, 273, 10784–10791.

  • Mayeda, A. and Krainer, A. R., Regulation of alternative pre-mRNA splicing by hnRNP A1 and splicing factor SF2. Cell, 1992, 68, 365–375.

  • Finn, R. D., Clements, J. and Eddy, S. R., HMMER web server: interactive sequence similarity searching. Nucleic Acids Res., 2011, 39, W29–W37.

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S., MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol., 2011, 28, 2731–2739.

  • Pomeranz Krummel, D. A., Oubridge, C., Leung, A. K., Li, J. and Nagai, K., Crystal structure of human spliceosomal U1 snRNP at 5.5 a resolution. Nature, 2009, 458, 475–480.

  • Forch, P., Puig, O., Martinez, C., Seraphin, B. and Valcarcel, J., The splicing regulator TIA-1 interacts with U1-C to promote U1 snRNP recruitment to 5 splice sites. EMBO J., 2002, 21, 6882–6892.

  • Query, C. C., Bentley, R. C. and Keene, J. D., A common RNA recognition motif identified within a defined U1 RNA binding domain of the 70K U1 snRNP protein. Cell, 1989, 57, 89–101.

  • Kobe, B. and Kajava, A. V., The leucine-rich repeat as a protein recognition motif. Curr. Opin. Struct. Biol., 2001, 11, 725–732.

  • Kramer, A., Mulhauser, F., Wersig, C., Groning, K. and Bilbe, G., Mammalian splicing factor SF3a120 represents a new member of the SURP family of proteins and is homologous to the essential splicing factor Prp21p of Saccharomyces cerevisiae. RNA, 1995, 1, 260–272.

  • Kuwasako, K., He, F., Inoue, M., Tanaka, A., Sugano, S., Guntert, P., Muto, Y. and Yokoyama, S., Solution structures of the SURP domains and the subunit-assembly mechanism within the splicing factor SF3a complex in 17S U2 snRNP. Structure, 2006, 14, 1677–1689.

  • Will, C. L., Urlaub, H., Achsel, T., Gentzel, M., Wilm, M. and Luhrmann, R., Characterization of novel SF3b and 17S U2 snRNP proteins, including a human Prp5p homologue and an SF3b dead-box protein. EMBO. J., 2002, 21, 4978–4988.

  • Trappe, R., Ahmed, M., Glaser, B., Vogel, C., Tascou, S., Burfeind, P. and Engel, W., Identification and characterization of a novel murine multigene family containing a PHD-finger-like motif. Biochem. Biophys. Res. Commun., 2002, 293, 816–826.

  • Hryciw, T., Tang, M., Fontanie, T. and Xiao, W., MMS1 protects against replication-dependent DNA damage in saccharomyces cerevisiae. Mol. Genet. Genomics, 2002, 266, 848–857.

  • Li, Y., Chen, Z. Y., Wang, W., Baker, C. C. and Krug, R. M., The 3'-end-processing factor CPSF is required for the splicing of singleintron pre-mRNAS in vivo. RNA, 2001, 7, 920–931.

  • Freund, C., Dotsch, V., Nishizawa, K., Reinherz, E. L. and Wagner, G., The GYF domain is a novel structural fold that is involved in lymphoid signaling through proline-rich sequences. Nat. Struct. Biol., 1999, 6, 656–660.

  • Nishizawa, K., Freund, C., Li, J., Wagner, G. and Reinherz, E. L., Identification of a proline-binding motif regulating CD2-triggered T lymphocyte activation. Proc. Natl. Acad. Sci. USA, 1998, 95, 14897–14902.

  • Reuter, K., Nottrott, S., Fabrizio, P., Luhrmann, R. and Ficner, R., Identification, characterization and crystal structure analysis of the human spliceosomal U5 snRNP-specific 15 KD protein. J. Mol. Biol., 1999, 294, 515–525.

  • Jermy, A. J., Willer, M., Davis, E., Wilkinson, B. M. and Stirling, C. J., The BRL domain in Sec63p is required for assembly of functional endoplasmic reticulum translocons. J. Biol. Chem., 2006, 281, 7899–7906.

  • Ponting, C. P., Proteins of the endoplasmic-reticulum-associated degradation pathway: Domain detection and function prediction. Biochem. J., 2000, 351(Pt 2), 527–535.

  • Aubourg, S., Kreis, M. and Lecharny, A., The dead box RNA helicase family in Arabidopsis thaliana. Nucleic Acids Res., 1999, 27, 628–636.

  • de la Cruz, J., Kressler, D. and Linder, P., Unwinding RNA in Saccharomyces cerevisiae: dead-box proteins and related families. Trends Biochem. Sci., 1999, 24, 192–198.

  • Urushiyama, S., Tani, T. and Ohshima, Y., Isolation of novel pre-mRNA splicing mutants of Schizosaccharomyces pombe. Mol. Gen. Genet, 1996, 253, 118–127.

  • Blatch, G. L. and Lassle, M., The tetratricopeptide repeat: a structural motif mediating protein–protein interactions. Bioessays, 1999, 21, 932–939.

  • Staub, E., Fiziev, P., Rosenthal, A. and Hinzmann, B., Insights into the evolution of the nucleolus by an analysis of its protein domain repertoire. Bioessays, 2004, 26, 567–581.

  • Ritchie, D. B., Schellenberg, M. J., Gesner, E. M., Raithatha, S. A., Stuart, D. T. and Macmillan, A. M., Structural elucidation of a Prp8 core domain from the heart of the spliceosome. Nat. Struct. Mol. Biol., 2008, 15, 1199–1205.

  • Ayadi, L., Callebaut, I., Saguez, C., Villa, T., Mornon, J. P. and Banroques, J., Functional and structural characterization of the Prp3 binding domain of the yeast Prp4 splicing factor. J. Mol. Biol., 1998, 284, 673–687.

  • Wang, P. and Heitman, J., The cyclophilins. Genome Biol., 2005, 6, 226.

  • Stirnimann, C. U., Petsalaki, E., Russell, R. B. and Muller, C. W., WD40 proteins propel cellular networks. Trends Biochem. Sci., 2010, 35, 565–574.

  • Weidenhammer, E. M., Singh, M., Ruiz-Noriega, M. and Wool-ford Jr., J. L., The Prp31 gene encodes a novel protein required for pre-mRNA splicing in Saccharomyces cerevisiae. Nucleic Acids Res., 1996, 24, 1164–1170.

  • Wilkinson, C. R., Dittmar, G. A., Ohi, M. D., Uetz, P., Jones, N. and Finley, D., Ubiquitin-like protein HUB1 is required for pre-mRNA splicing and localization of an essential splicing factor in fission yeast. Curr. Biol., 2004, 14, 2283–2288.

  • Hershko, A. and Ciechanover, A., The ubiquitin system. Annu. Rev. Biochem., 1998, 67, 425–479.

  • Wilkinson, K. D., Regulation of ubiquitin-dependent processes by deubiquitinating enzymes. FASEB J., 1997, 11, 1245–1256.

  • Grillari, J. et al., SNEV is an evolutionarily conserved splicing factor whose oligomerization is necessary for spliceosome assembly. Nucleic Acids Res., 2005, 33, 6868–6883.

  • Ohi, M. D., Link, A. J., Ren, L., Jennings, J. L., McDonald, W. H. and Gould, K. L., Proteomics analysis reveals stable multiprotein complexes in both fission and budding yeasts containing Myb-related Cdc5p/Cef1p, novel pre-mRNA splicing factors, and snR-NAS. Mol. Cell Biol., 2002, 22, 2011–2024.

  • Dix, I., Russell, C., Yehuda, S.B., Kupiec, M. and Beggs, J. D., The identification and characterization of a novel splicing protein, Isy1p of Saccharomyces cerevisiae. RNA, 1999, 5, 360–368.

  • Shepard, P. J. and Hertel, K. J., The SR protein family. Genome Biol., 2009, 10, 242.

  • Kempken, F., Alternative splicing in ascomycetes. Appl. Microbiol. Biotechnol., 2013, 97, 4235–4241.

  • Sauliere, J., Haque, N., Harms, S., Barbosa, I., Blanchette, M. and Le Hir, H., The exon junction complex differentially marks spliced junctions. Nat. Struct. Mol. Biol., 2010, 17, 1269–1271.

  • Bordonne, R., Banroques, J., Abelson, J. and Guthrie, C., Domains of yeast U4 spliceosomal RNA required for Prp4 protein binding, snRNP–snRNP interactions, and pre-mRNA splicing in vivo. Genes Dev., 1990, 4, 1185–1196.

  • Galej, W. P., Oubridge, C., Newman, A. J. and Nagai, K., Crystal structure of Prp8 reveals active site cavity of the spliceosome. Nature, 2013, 493, 638-+.

  • Kondo, Y., Oubridge, C., van Roon, A. M. M. and Nagai, K., Crystal structure of human U1 snRNP, a small nuclear ribonucleo-protein particle, reveals the mechanism of 5 splice site recognition. Elife, 2015, 4.

  • Korneta, I., Magnus, M. and Bujnicki, J. M., Structural bioinformatics of the human spliceosomal proteome. Nucleic Acids Res., 2012, 40, 7046–7065.


Abstract Views: 364

PDF Views: 109




  • Spliceosomal Proteins Encoded by Fungal Genomes

Abstract Views: 364  |  PDF Views: 109

Authors

Sandeep J. Sarde
Abteilung Botanische Genetik und Molekularbiologie, Botanisches Institut und Botanischer Garten, Christian-Albrechts-Universitat zu Kiel, Olshausenstr. 40 24098 Kiel, Germany
Frank Kempken
Abteilung Botanische Genetik und Molekularbiologie, Botanisches Institut und Botanischer Garten, Christian-Albrechts-Universitat zu Kiel, Olshausenstr. 40 24098 Kiel, Germany
Abhishek Kumar
Molecular Genetic Epidemiology (C050), German Cancer Research Center (DKFZ), Im Neuenheimer Feld 580 69120 Heidelberg, Germany

Abstract


A large number of spliceosomal proteins are required for proper RNA splicing. While spliceosomal proteins from several model organisms have been analysed, only limited studies are available for fungal species. Hence, we have performed a comparative genomic analysis using eight fungal species belonging to three taxa (Ascomycetes, Basidiomycetes and Glomeromycota). We identified variable number of spliceosomal proteins in fungal species. From the small nuclear ribonucleoproteins (snRNPs), all the snRNPs were identified. In non-snRNPs, only some sub-groups were found extensively conserved in all fungal species, including PRP19 complex proteins, catalytic step II and late-acting proteins. In heterogeneous nuclear ribonucleoproteins (hnRNPs), variable number of proteins was identified. The number of spliceosomal proteins identified in filamentous fungi was higher than that in yeast. The collection of these spliceosomal proteins provides further insight into pre-mRNA splicing in fungi.

Keywords


Fungal Genomes, pre-mRNA, snRNPs, Spliceosomal Proteins.

References





DOI: https://doi.org/10.18520/cs%2Fv114%2Fi08%2F1677-1686