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Identification of a new Schistosoma mansoni SMYB1 partner: putative roles in RNA metabolism

  • ELIZÂNGELA A. ROCHA (a1), ANALINA F. VALADÃO (a2), CÍNTIA M. REZENDE (a1), SILVIA REGINA COSTA DIAS (a1), ANDRÉA M. MACEDO (a1), CARLOS R. MACHADO (a1), MARCELO R. FANTAPPIÉ (a3), FRANKLIN D. RUMJANEK (a3), ALFREDO M. GOES (a1), DAWIDSON A. GOMES (a1), PHILIP T. LOVERDE (a4), MARCELA G. DRUMMOND (a1) and GLÓRIA R. FRANCO (a1)...
Summary

SMYB1 is a Schistosoma mansoni protein highly similar to members of the Y-box binding protein family. Similar to other homologues, SMYB1 is able to bind double- and single-stranded DNA, as well as RNA molecules. The characterization of proteins involved in the regulation of gene expression in S. mansoni is of great importance for the understanding of molecular events that control morphological and physiological changes in this parasite. Here we demonstrate that SMYB1 is located in the cytoplasm of cells from different life-cycle stages of S. mansoni, suggesting that this protein is probably acting in mRNA metabolism in the cytoplasm and corroborating previous findings from our group that showed its ability to bind RNA. Protein–protein interactions are important events in all biological processes, since most proteins execute their functions through large supramolecular structures. Yeast two-hybrid screenings using SMYB1 as bait identified a partner in S. mansoni similar to the SmD3 protein of Drosophila melanogaster (SmRNP), which is important in the assembly of small nuclear ribonucleoprotein complexes. Also, pull-down assays were conducted using immobilized GST-SMYB1 proteins and confirmed the SMYB1-SmRNP interaction. The interaction of SMYB1 with a protein involved in mRNA processing suggests that it may act in processes such as turnover, transport and stabilization of RNA molecules.

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Corresponding author
*Corresponding author: Departamento de Bioquímica e Imunologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais – UFMG, Avenida Antônio Carlos 6627, Belo Horizonte, MG, 31270-010, Brazil. E-mail: gfrancoufmg@gmail.com
References
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Allemand, E., Hastings, M. L., Murray, M. V., Myers, M. P. and Krainer, A. R. (2007). Alternative splicing regulation by interaction of phosphatase PP2Cg with nucleic acid–binding protein YB-1. Nature Structural and Molecular Biology 14, 630637.
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology 215, 403410.
Bitar, M., Drummond, M. G., Costa, M. G., Lobo, F. P., Calzavara-Silva, C. E., Bisch, P. M., Machado, C. R., Macedo, A. M., Pierce, R. J. and Franco, G. R. (2012). Modeling the zing finger protein SmZF1 from Schistosoma mansoni: insights into DNA binding and gene regulation. Journal of Molecular Graphical Model 39C, 2938.
Bruckner, A., Polge, C., Lentze, N., Auerbach, D. and Schlattner, U. (2009). Yeast two-hybrid, a powerful tool for systems biology. International Journal of Molecular Science 10, 27632788.
Ceman, S., Nelson, R. and Warren, S. T. (2000). Identification of mouse YB1/p50 as a component of the FMRP-associated mRNP particle. Biochemical and Biophysical Research Communications 279, 904908.
Chernukhin, I. V., Shamsuddin, S., Robinson, A. F., Carne, A. F., Paul, A., El-Kady, A. I., Lobanenkov, V. V. and Klenova, E. M. (2000). Physical and functional interaction between two pluripotent proteins, the Y-box DNA/RNA-binding factor, YB-1, and the multivalent zinc finger factor, CTCF. Journal of Biological Chemistry 275, 2991529921.
de Oliveira, F. M., da Silva, I. C., Rumjanek, F. D., Valadao, A. F., Franco, G. R., Mesquita, R. D., da Silva-Neto, M. A. and Fantappie, M. R. (2004). Functional properties of Schistosoma mansoni single-stranded DNA-binding protein SmPUR-alpha. Description of the interaction between SmPUR-alpha and SMYB1. Molecular and Biochemical Parasitology 135, 2130.
de Souza-Pinto, N. C., Mason, P. A., Hashiguchi, K., Weissman, L., Tian, J., Guay, D., Lebel, M., Stevnsner, T. V., Rasmussen, L. J. and Bohr, V. A. (2009). Novel DNA mismatch-repair activity involving YB-1 in human mitochondria. DNA Repair (Amst) 8, 704719.
Didier, D. K., Schiffenbauer, J., Woulfe, S. L., Zacheis, M. and Schwartz, B. D. (1988). Characterization of the cDNA encoding a protein binding to the major histocompatibility complex class II Y box. Proceedings of the National Academy of Sciences, USA 85, 73227326.
Dong, J., Akcakanat, A., Stivers, D. N., Zhang, J., Kim, D. and Meric-Bernstam, F. (2009). RNA-binding specificity of Y-box protein 1. RNA Biology 6, 5964.
Dorn, A., Durand, B., Marfing, C., Le Meur, M., Benoist, C. and Mathis, D. (1987). Conserved major histocompatibility complex class II boxes–X and Y–are transcriptional control elements and specifically bind nuclear proteins. Proceedings of the National Academy of Sciences, USA 84, 62496253.
Drummond, M. G., Calzavara-Silva, C. E., D'Astolfo, D. S., Cardoso, F. C., Rajao, M. A., Mourao, M. M., Gava, E., Oliveira, S. C., Macedo, A. M., Machado, C. R., Pena, S. D., Kitten, G. T. and Franco, G. R. (2009). Molecular characterization of the Schistosoma mansoni zinc finger protein SmZF1 as a transcription factor. PLOS Neglected Tropical Diseases 3, e547.
El-Ansary, A. and Al-Daihan, S. (2005). Stage-specifically expressed schistosome proteins as potential chemotherapeutic targets. Medical Science Monitor 11, RA94103.
Eliseeva, I. A., Kim, E. R., Guryanov, S. G., Ovchinnikov, L. P. and Lyabin, D. N. (2011). Y-box-binding protein 1 (YB-1) and its functions. Biochemistry (Mosc) 76, 14021433.
Evdokimova, V., Ruzanov, P., Imataka, H., Raught, B., Svitkin, Y., Ovchinnikov, L. P. and Sonenberg, N. (2001). The major mRNA-associated protein YB-1 is a potent 5′ cap-dependent mRNA stabilizer. EMBO Journal 20, 54915502.
Evdokimova, V., Ovchinnikov, L. P. and Sorensen, P. H. (2006). Y-box binding protein 1: providing a new angle on translational regulation. Cell Cycle 5, 11431147.
Fantappie, M. R., Osman, A., Niles, E. G. and LoVerde, P. T. (2000). Identification and functional characterization of a member of the PUR-alpha family from Schistosoma mansoni. Molecular and Biochemical Parasitology 110, 373390.
Fantappie, M. R., de Oliveira, F. M., de Moraes Maciel dos Santos, R., Mansure, J. J., Furtado, D. R., de Abreu da Silva, I. C. and Rumjanek, F. D. (2008). Control of transcription in Schistosoma mansoni: chromatin remodeling and other regulatory elements. Acta Tropica 108, 186193.
Franco, G. R., Garratt, R. C., Tanaka, M., Simpson, A. J. and Pena, S. D. (1997). Characterization of a Schistosoma mansoni gene encoding a homologue of the Y-box binding protein. Gene 198, 516.
Goldsmith, M. E., Madden, M. J., Morrow, C. S. and Cowan, K. H. (1993). A Y-box consensus sequence is required for basal expression of the human multidrug resistance (mdr1) gene. Journal of Biological Chemistry 268, 58565860.
Harrop, R. and Wilson, R. A. (1993). Protein synthesis and release by cultured schistosomula of Schistosoma mansoni. Parasitology 107, 265274.
Izumi, H., Imamura, T., Nagatani, G., Ise, T., Murakami, T., Uramoto, H., Torigoe, T., Ishiguchi, H., Yoshida, Y., Nomoto, M., Okamoto, T., Uchiumi, T., Kuwano, M., Funa, K. and Kohno, K. (2001). Y box-binding protein-1 binds preferentially to single-stranded nucleic acids and exhibits 3′–>5′ exonuclease activity. Nucleic Acids Research 29, 12001207.
Jolly, E. R., Chin, C. S., Miller, S., Bahgat, M. M., Lim, K. C., DeRisi, J. and McKerrow, J. H. (2007). Gene expression patterns during adaptation of a helminth parasite to different environmental niches. Genome Biology 8, R65.
Kelm, R. J. Jr., Elder, P. K. and Getz, M. J. (1999). The single-stranded DNA-binding proteins, Puralpha, Purbeta, and MSY1 specifically interact with an exon 3-derived mouse vascular smooth muscle alpha-actin messenger RNA sequence. Journal of Biological Chemistry 274, 3826838275.
Kohno, K., Izumi, H., Uchiumi, T., Ashizuka, M. and Kuwano, M. (2003). The pleiotropic functions of the Y-box-binding protein, YB-1. Bioessays 25, 691698.
Kuwano, M., Oda, Y., Izumi, H., Yang, S. J., Uchiumi, T., Iwamoto, Y., Toi, M., Fujii, T., Yamana, H., Kinoshita, H., Kamura, T., Tsuneyoshi, M., Yasumoto, K. and Kohno, K. (2004). The role of nuclear Y-box binding protein 1 as a global marker in drug resistance. Molecular Cancer Therapeutics 3, 14851492.
Lehmeier, T., Foulaki, K. and Luhrmann, R. (1990). Evidence for three distinct D proteins, which react differentially with anti-Sm autoantibodies, in the cores of the major snRNPs U1, U2, U4/U6 and U5. Nucleic Acids Research 18, 64756484.
Lipson, K. E., Chen, S. T., Koniecki, J., Ku, D. H. and Baserga, R. (1989). S-phase-specific regulation by deletion mutants of the human thymidine kinase promoter. Proceedings of the National Academy of Sciences, USA 86, 68486852.
Lu, C., Wu, W., Niles, E. G. and LoVerde, P. T. (2006). Identification and characterization of a novel fushi tarazu factor 1 (FTZ-F1) nuclear receptor in Schistosoma mansoni. Molecular and Biochemical Parasitology 150, 2536.
Lyabin, D. N., Eliseeva, I. A., Skabkina, O. V. and Ovchinnikov, L. P. (2011). Interplay between Y-box-binding protein 1 (YB-1) and poly(A) binding protein (PABP) in specific regulation of YB-1 mRNA translation. RNA Biology 8, 883892.
Mathis, D. J., Benoist, C. O., Williams, V. E. II, Kanter, M. R. and McDevitt, H. O. (1983). The murine E alpha immune response gene. Cell 32, 745754.
Matsumoto, K. and Bay, B. H. (2005). Significance of the Y-box proteins in human cancers. Journal of Molecular and Genetic Medicine 1, 1117.
Matsumoto, K. and Wolffe, A. P. (1998). Gene regulation by Y-box proteins: coupling control of transcription and translation. Trends in Cell Biology 8, 318323.
Matsumoto, S., Uchiumi, T., Saito, T., Yagi, M., Takazaki, S., Kanki, T. and Kang, D. (2012). Localization of mRNAs encoding human mitochondrial oxidative phosphorylation proteins. Mitochondrion 12, 391398.
Murray, M. T., Schiller, D. L. and Franke, W. W. (1992). Sequence analysis of cytoplasmic mRNA-binding proteins of Xenopus oocytes identifies a family of RNA-binding proteins. Proceedings of the National Academy of Sciences, USA 89, 1115.
Nie, M., Aijaz, S., Leefa Chong San, I. V., Balda, M. S. and Matter, K. (2009). The Y-box factor ZONAB/DbpA associates with GEF-H1/Lfc and mediates Rho-stimulated transcription. EMBO Reports 10, 11251131.
Okamoto, T., Izumi, H., Imamura, T., Takano, H., Ise, T., Uchiumi, T., Kuwano, M. and Kohno, K. (2000). Direct interaction of p53 with the Y-box binding protein, YB-1: a mechanism for regulation of human gene expression. Oncogene 19, 61946202.
Pearson, B. E., Nasheuer, H. P. and Wang, T. S. (1991). Human DNA polymerase alpha gene: sequences controlling expression in cycling and serum-stimulated cells. Molecular and Cellular Biology 11, 20812095.
Raffetseder, U., Frye, B., Rauen, T., Jurchott, K., Royer, H. D., Jansen, P. L. and Mertens, P. R. (2003). Splicing factor SRp30c interaction with Y-box protein-1 confers nuclear YB-1 shuttling and alternative splice site selection. Journal of Biological Chemistry 278, 1824118248.
Ruzanov, P. V., Evdokimova, V. M., Korneeva, N. L., Hershey, J. W. and Ovchinnikov, L. P. (1999). Interaction of the universal mRNA-binding protein, p50, with actin: a possible link between mRNA and microfilaments. Journal of Cell Science 112(Pt 20), 34873496.
Rymond, B. (2007). Targeting the spliceosome. Nature Chemical Biology 3, 533535.
Safak, M., Gallia, G. L. and Khalili, K. (1999). Reciprocal interaction between two cellular proteins, Puralpha and YB-1, modulates transcriptional activity of JCVCY in glial cells. Molecular and Cellular Biology 19, 27122723.
Saito, H., Maki, R. A., Clayton, L. K. and Tonegawa, S. (1983). Complete primary structures of the E beta chain and gene of the mouse major histocompatibility complex. Proceedings of the National Academy of Sciences, USA 80, 55205524.
Sakura, H., Maekawa, T., Imamoto, F., Yasuda, K. and Ishii, S. (1988). Two human genes isolated by a novel method encode DNA-binding proteins containing a common region of homology. Gene 73, 499507.
Salvetti, A., Batistoni, R., Deri, P., Rossi, L. and Sommerville, J. (1998). Expression of DjY1, a protein containing a cold shock domain and RG repeat motifs, is targeted to sites of regeneration in planarians. Developmental Biology 201, 217229.
Schindelin, H., Marahiel, M. A. and Heinemann, U. (1993). Universal nucleic acid-binding domain revealed by crystal structure of the B. subtilis major cold-shock protein. Nature 364, 164168.
Serebriiskii, I., Estojak, J., Berman, M. and Golemis, E. A. (2000). Approaches to detecting false positives in yeast two-hybrid systems. Biotechniques 28, 328330, 332–326.
Shnyreva, M., Schullery, D. S., Suzuki, H., Higaki, Y. and Bomsztyk, K. (2000). Interaction of two multifunctional proteins. Heterogeneous nuclear ribonucleoprotein K and Y-box-binding protein. Journal of Biological Chemistry 275, 1549815503.
Skabkina, O. V., Lyabin, D. N., Skabkin, M. A. and Ovchinnikov, L. P. (2005). YB-1 autoregulates translation of its own mRNA at or prior to the step of 40S ribosomal subunit joining. Molecular and Cellular Biology 25, 33173323.
Skehel, P. A. and Bartsch, D. (1994). Characterization of a Y-Box factor from Aplysia californica. Gene 145, 231235.
Sommerville, J. and Ladomery, M. (1996). Transcription and masking of mRNA in germ cells: involvement of Y-box proteins. Chromosoma 104, 469478.
Valadão, A. F., Fantappie, M. R., LoVerde, P. T., Pena, S. D., Rumjanek, F. D. and Franco, G. R. (2002). Y-box binding protein from Schistosoma mansoni: interaction with DNA and RNA. Molecular and Biochemical Parasitology 125, 4757.
van Alphen, R. J., Wiemer, E. A. C., Burger, H. and Eskens, F. (2009). The spliceosome as target for anticancer treatment. British Journal of Cancer 100, 228232.
WHO (2013). Parasitic disease: Schistosomiasis. http://www.who.int/mediacentre/factsheets/fs115/en/
Wistow, G. (1990). Cold shock and DNA binding. Nature 344, 823824.
Wu, W. and Loverde, P. T. (2008). Schistosoma mansoni: identification of SmNR4A, a member of nuclear receptor subfamily 4. Experimental Parasitology 120, 208213.
Wu, W., Niles, E. G., Hirai, H. and LoVerde, P. T. (2007). Identification and characterization of a nuclear receptor subfamily I member in the Platyhelminth Schistosoma mansoni (SmNR1). FEBS Journal 274, 390405.
Wu, W., Tak, E. Y. and LoVerde, P. T. (2008). Schistosoma mansoni: SmE78, a nuclear receptor orthologue of Drosophila ecdysone-induced protein 78. Experimental Parasitology 119, 313318. doi: S0014-4894(08)00064-7 [pii]10.1016/j.exppara.2008.03.001.
Yang, J., Medvedev, S., Yu, J., Schultz, R. M. and Hecht, N. B. (2006). Deletion of the DNA/RNA-binding protein MSY2 leads to post-meiotic arrest. Molecular and Cellular Endocrinology 250, 2024.
Zambrano, N., De Renzis, S., Minopoli, G., Faraonio, R., Donini, V., Scaloni, A., Cimino, F. and Russo, T. (1997). DNA-binding protein Pur alpha and transcription factor YY1 function as transcription activators of the neuron-specific FE65 gene promoter. The Biochemical Journal 328(Pt 1), 293300.
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