Characterization of a new toxin from the entomopathogenic fungus Metarhizium anisopliae: the ribotoxin anisoplin

References

Abdul-Ghani, R., Al-Mekhlafi, A.M., and Alabsi, M.S. (2012). Microbial control of malaria: biological warfare against the parasite and its vector. Acta Trop. 121, 71–84.10.1016/j.actatropica.2011.11.001Search in Google Scholar

Álvarez-García, E., Martínez-del-Pozo, A., and Gavilanes, J.G. (2009). Role of the basic character of alpha-sarcin’s NH₂-terminal β-hairpin in ribosome recognition and phospholipid interaction. Arch. Biochem. Biophys. 481, 37–44.10.1016/j.abb.2008.10.012Search in Google Scholar

Boucias, D.G., Farmerie, W.G., and Pendland, J.C. (1998). Cloning and sequencing of cDNA of the insecticidal toxin hirsutellin A. J. Invertebr. Pathol. 72, 258–261.10.1006/jipa.1998.4762Search in Google Scholar

Brandhorst, T.T. and Kenealy, W.R. (1992). Production and localization of restrictocin in Aspergillus restrictus. J. Gen. Microbiol. 138, 1429–1435.10.1099/00221287-138-7-1429Search in Google Scholar

Brandhorst, T., Dowd, P.F., and Kenealy, W.R. (1996). The ribosome-inactivating protein restrictocin deters insect feeding on Aspergillus restrictus. Microbiology 142, 1551–1556.10.1099/13500872-142-6-1551Search in Google Scholar

Carreras-Sangrá, N., Tomé-Amat, J., García-Ortega, L., Batt, C.A., Oñaderra, M., Martínez-del-Pozo, A., Gavilanes, J.G., and Lacadena, J. (2012). Production and characterization of a colon cancer-specific immunotoxin based on the fungal ribotoxin α-sarcin. Protein Eng. Des. Sel. 25, 425–435.10.1093/protein/gzs032Search in Google Scholar

de Bekker, C., Smith, P.B., Patterson, A.D., and Hughes, D.P. (2013). Metabolomics reveals the heterogeneous secretome of two entomopathogenic fungi to ex vivo cultured insect tissues. PLoS One 8, e70609.10.1371/journal.pone.0070609Search in Google Scholar

Endo, Y. and Wool, I.G. (1982). The site of action of α-sarcin on eukaryotic ribosomes. The sequence at the α-sarcin cleavage site in 28 S ribosomal ribonucleic acid. J. Biol. Chem. 257, 9054–9060.10.1016/S0021-9258(18)34241-8Search in Google Scholar

Endo, Y., Oka, T., Tsurugi, K., and Natori, Y. (1993a). The biosynthesis of a cytotoxic protein, α-sarcin, in a mold Aspergillus giganteus. I. Synthesis of prepro- and pro-α-sarcin in vitro. Tokushima J. Exp. Med. 40, 1–6.Search in Google Scholar

Endo, Y., Oka, T., Yokota, S., Tsurugi, K., and Natori, Y. (1993b). The biosynthesis of a cytotoxic protein, α-sarcin, in a mold of Aspergillus giganteus. II. Maturation of precursor form of α-sarcin in vivo. Tokushima J. Exp. Med. 40, 7–12.Search in Google Scholar

Fang, W., Vega-Rodríguez, J., Ghosh, A.K., Jacobs-Lorena, M., Kang, A., and St Leger, R.J. (2011). Development of transgenic fungi that kill human malaria parasites in mosquitoes. Science 331, 1074–1077.10.1126/science.1199115Search in Google Scholar PubMed PubMed Central

Faria, M.R. and Wraight, S.P. (2007). Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol. Control. 43, 237–256.10.1016/j.biocontrol.2007.08.001Search in Google Scholar

Gao, Q., Jin, K., Ying, S.H., Zhang, Y., Xiao, G., Shang, Y., Duan, Z., Hu, X., Xie, X.Q., Zhou, G., et al. (2011). Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genet. 7, e1001264.10.1371/journal.pgen.1001264Search in Google Scholar

García-Mayoral, F., García-Ortega, L., Álvarez-García, E., Bruix, M., Gavilanes, J.G., and del Pozo, A.M. (2005). Modeling the highly specific ribotoxin recognition of ribosomes. FEBS Lett 579, 6859–6864.10.1016/j.febslet.2005.11.027Search in Google Scholar

García-Ortega, L., Lacadena, J., Lacadena, V., Masip, M., De Antonio, C., Martínez-Ruiz, A., and Martínez Del Pozo, A. (2000). The solubility of the ribotoxin α-sarcin, produced as a recombinant protein in Escherichia coli, is increased in the presence of thioredoxin. Lett. Appl. Microbiol. 30, 298–302.10.1046/j.1472-765x.2000.00714.xSearch in Google Scholar

García-Ortega, L., Masip, M., Mancheño, J.M., Oñaderra, M., Lizarbe, M.A., García-Mayoral, M.F., Bruix, M., Martínez del Pozo, A., and Gavilanes, J.G. (2002). Deletion of the NH₂-terminal α-hairpin of the ribotoxin α-sarcin produces a nontoxic but active ribonuclease. J. Biol. Chem. 277, 18632–18639.10.1074/jbc.M200922200Search in Google Scholar

García-Ortega, L., Álvarez-García, E., Gavilanes, J.G., Martínez-del-Pozo, A., and Joseph, S. (2010). Cleavage of the sarcin-ricin loop of 23S rRNA differentially affects EF-G and EF-Tu binding. Nucleic Acids Res. 38, 4108–4119.10.1093/nar/gkq151Search in Google Scholar

Herrero-Galán, E., Lacadena, J., Martínez del Pozo, A., Boucias, D.G., Olmo, N., Oñaderra, M., and Gavilanes, J.G. (2008). The insecticidal protein hirsutellin A from the mite fungal pathogen Hirsutella thompsonii is a ribotoxin. Proteins 72, 217–228.10.1002/prot.21910Search in Google Scholar

Howard, A.F., Koenraadt, C.J., Farenhorst, M., Knols, B.G., and Takken, W. (2010). Pyrethroid resistance in Anopheles gambiae leads to increased susceptibility to the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana. Malar. J. 9, 168.10.1186/1475-2875-9-168Search in Google Scholar

Kanga, L.H., James, R.R., and Boucias, D.G. (2002). Hirsutella thompsonii and Metarhizium anisopliae as potential microbial control agents of Varroa destructor, a honey bee parasite. J. Invertebr. Pathol. 81, 175–184.10.1016/S0022-2011(02)00177-5Search in Google Scholar

Kanzok, S.M. and Jacobs-Lorena, M. (2006). Entomopathogenic fungi as biological insecticides to control malaria. Trends Parasitol. 22, 49–51.10.1016/j.pt.2005.12.008Search in Google Scholar PubMed

Koch, M., Flur, S., Kreutz, C., Ennifar, E., Micura, R., and Polacek, N. (2015). Role of a ribosomal RNA phosphate oxygen during the EF-G-triggered GTP hydrolysis. Proc. Natl. Acad Sci. USA 112, E2561–E2568.10.1073/pnas.1505231112Search in Google Scholar PubMed PubMed Central

Lacadena, J., Martínez del Pozo, A., Barbero, J.L., Mancheño, J.M., Gasset, M., Oñaderra, M., López-Otín, C., Ortega, S., García, J., and Gavilanes, J.G. (1994). Overproduction and purification of biologically active native fungal alpha-sarcin in Escherichia coli. Gene 142, 147–151.10.1016/0378-1119(94)90370-0Search in Google Scholar

Lacadena, J., Álvarez-García, E., Carreras-Sangrá, N., Herrero-Galán, E., Alegre-Cebollada, J., García-Ortega, L., Oñaderra, M., Gavilanes, J.G., and Martínez del Pozo, A. (2007). Fungal ribotoxins: molecular dissection of a family of natural killers. FEMS Microbiol. Rev. 31, 212–237.10.1111/j.1574-6976.2006.00063.xSearch in Google Scholar PubMed

Lai, Y., Liu, K., Zhang, X., Zhang, X., Li, K., Wang, N., Shu, C., Wu, Y., Wang, C., Bushley, K.E., et al. (2014). Comparative genomics and transcriptomics analyses reveal divergent lifestyle features of nematode endoparasitic fungus Hirsutella minnesotensis. Genome Biol. Evol. 6, 3077–3093.10.1093/gbe/evu241Search in Google Scholar PubMed PubMed Central

Liu, B.L. and Tzeng, Y.M. (2012) Development and applications of destruxins: a review. Biotechnol. Adv. 30, 1242–1254.10.1016/j.biotechadv.2011.10.006Search in Google Scholar PubMed

Martínez-Ruiz, A., Martínez del Pozo, A., Lacadena, J., Mancheño, J.M., Oñaderra, M., López-Otín, C., and Gavilanes, J.G. (1998). Secretion of recombinant pro- and mature fungal α-sarcin ribotoxin by the methylotrophic yeast Pichia pastoris: the Lys-Arg motif is required for maturation. Protein Expr. Purif. 12, 315–322.10.1006/prep.1997.0846Search in Google Scholar PubMed

Martínez-Ruiz, A., Martínez del Pozo, A., Lacadena, J., Oñaderra, M., and Gavilanes, J.G. (1999). Hirsutellin A displays significant homology to microbial extracellular ribonucleases. J. Invertebr. Pathol. 74, 96–97.10.1006/jipa.1999.4859Search in Google Scholar PubMed

Mazet, I. and Vey, A. (1995). Hirsutellin A, a toxic protein produced in vitro by Hirsutella thompsonii. Microbiology 141, 1343–1348.10.1099/13500872-141-6-1343Search in Google Scholar PubMed

Mnyone, L.L., Kirby, M.J., Lwetoijera, D.W., Mpingwa, M.W., Knols, B.G., Takken, W., and Russell, T.L. (2009). Infection of the malaria mosquito, Anopheles gambiae, with two species of entomopathogenic fungi: effects of concentration, co-formulation, exposure time and persistence. Malar. J. 8, 309.10.1186/1475-2875-8-309Search in Google Scholar PubMed PubMed Central

Oka, T., Natori, Y., Tanaka, S., Tsurugi, K., and Endo, Y. (1990). Complete nucleotide sequence of cDNA for the cytotoxin α-sarcin. Nucleic Acids Res. 18, 1897.10.1093/nar/18.7.1897Search in Google Scholar PubMed PubMed Central

Olombrada, M., Herrero-Galán, E., Tello, D., Oñaderra, M., Gavilanes, J.G., Martínez-del-Pozo, A., and García-Ortega, L. (2013). Fungal extracellular ribotoxins as insecticidal agents. Insect. Biochem. Mol. Biol. 43, 39–46.10.1016/j.ibmb.2012.10.008Search in Google Scholar PubMed

Olombrada, M., Martínez-del-Pozo, A., Medina, P., Budia, F., Gavilanes, J.G., and García-Ortega, L. (2014a). Fungal ribotoxins: natural protein-based weapons against insects. Toxicon. 83, 69–74.10.1016/j.toxicon.2014.02.022Search in Google Scholar PubMed

Olombrada, M., Rodríguez-Mateos, M., Prieto, D., Pla, J., Remacha, M., Martínez-del-Pozo, A., Gavilanes, J.G., Ballesta, J.P., and García-Ortega, L. (2014b). The acidic ribosomal stalk proteins are not required for the highly specific inactivation exerted by alpha-sarcin of the eukaryotic ribosome. Biochemistry 53, 1545–1547.10.1021/bi401470uSearch in Google Scholar PubMed

Olson, B.H., Jennings, J.C., Roga, V., Junek, A.J., and Schuurmans, D.M. (1965). Alpha sarcin, a new antitumor agent: II. Fermentation and antitumor spectrum. Appl. Microbiol. 13, 322–326.10.1128/am.13.3.322-326.1965Search in Google Scholar PubMed PubMed Central

Ortiz-Urquiza, A., Luo, Z., and Keyhani, N.O. (2015). Improving mycoinsecticides for insect biological control. Appl. Microbiol. Biotechnol. 99, 1057–1068.10.1007/s00253-014-6270-xSearch in Google Scholar PubMed

Pattemore, J.A., Hane, J.K., Williams, A.H., Wilson, B.A., Stodart, B.J., and Ash, G.J. (2014). The genome sequence of the biocontrol fungus Metarhizium anisopliae and comparative genomics of Metarhizium species. BMC Genomics 15, 660.10.1186/1471-2164-15-660Search in Google Scholar PubMed PubMed Central

Schindler, D.G. and Davies, J.E. (1977). Specific cleavage of ribosomal RNA caused by alpha sarcin. Nucleic Acids Res. 4, 1097–1110.10.1093/nar/4.4.1097Search in Google Scholar PubMed PubMed Central

Scholte, E.J., Knols, B.G., Samson, R.A., and Takken, W. (2004). Entomopathogenic fungi for mosquito control: a review. J. Insect. Sci. 4, 19.10.1093/jis/4.1.19Search in Google Scholar PubMed PubMed Central

Schrank, A. and Vainstein, M.H. (2010). Metarhizium anisopliae enzymes and toxins. Toxicon. 56, 1267–1274.10.1016/j.toxicon.2010.03.008Search in Google Scholar PubMed

Shi, X., Khade, P.K., Sanbonmatsu, K.Y., and Joseph, S. (2012). Functional role of the sarcin-ricin loop of the 23S rRNA in the elongation cycle of protein synthesis. J. Mol. Biol. 419, 125–138.10.1016/j.jmb.2012.03.016Search in Google Scholar PubMed PubMed Central

Staats, C.C., Junges, A., Guedes, R.L., Thompson, C.E., de Morais, G.L., Boldo, J.T., de Almeida, L.G., Andreis, F.C., Gerber, A.L., Sbaraini, N., et al. (2014). Comparative genome analysis of entomopathogenic fungi reveals a complex set of secreted proteins. BMC Genomics 15, 822.10.1186/1471-2164-15-822Search in Google Scholar PubMed PubMed Central

Stirpe, F. and Battelli, M.G. (2006). Ribosome-inactivating proteins: progress and problems. Cell Mol. Life Sci. 63, 1850–1866.10.1007/s00018-006-6078-7Search in Google Scholar PubMed

Tomé-Amat, J., Olombrada, M., Ruiz-de-la-Herrán, J., Pérez-Gómez, E., Andradas, C., Sánchez, C., Martínez, L., Martínez-Del-Pozo, A., Gavilanes, J.G., and Lacadena, J. (2015). Efficient in vivo antitumor effect of an immunotoxin based on ribotoxin α-sarcin in nude mice bearing human colorectal cancer xenografts. Springerplus 4, 168.10.1186/s40064-015-0943-5Search in Google Scholar PubMed PubMed Central

Viegas, A., Herrero-Galán, E., Oñaderra, M., Macedo, A.L., and Bruix, M. (2009). Solution structure of hirsutellin A – new insights into the active site and interacting interfaces of ribotoxins. FEBS J. 276, 2381–2390.10.1111/j.1742-4658.2009.06970.xSearch in Google Scholar PubMed

Voorhees, R.M., Schmeing, T.M., Kelley, A.C., and Ramakrishnan, V. (2010). The mechanism for activation of GTP hydrolysis on the ribosome. Science 330, 835–838.10.1126/science.1194460Search in Google Scholar PubMed PubMed Central

Wang, B., Kang, Q., Lu, Y., Bai, L., and Wang, C. (2012). Unveiling the biosynthetic puzzle of destruxins in Metarhizium species. Proc. Natl. Acad Sci. USA 109, 1287–1292.10.1073/pnas.1115983109Search in Google Scholar PubMed PubMed Central