Conidial surface proteins of Metarhizium anisopliae: Source of activities related with toxic effects, host penetration and pathogenesis

Toxicon

Volumn 55, Issue 4, 2010, Pages 874-880

  Santi, Lucélia ^a   Beys da Silva, Walter O ^a   Berger, Markus ^a   Guimarães, Jorge A ^a   Schrank, Augusto ^a   Vainstein, Marilene H ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Chitinase; Conidia; Host infection; Lipase; Metarhizium anisopliae; Protease; Spore surface protein

Indexed keywords

CATALASE; CHITINASE; ENDOCHITINASE; EXOCHITINASE; FUNGAL PROTEIN; PEROXIDASE; PHOSPHOLIPASE C; PROTEASE PR1; PROTEASE PR2; PROTEINASE; REACTIVE OXYGEN METABOLITE; SPORE SURFACE PROTEIN; SUBTILISIN; SUPEROXIDE DISMUTASE; TREHALASE; TRYPSIN; UNCLASSIFIED DRUG;

ARTHROPOD; ARTICLE; CONIDIUM; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; FUNGAL VIRULENCE; HOST PATHOGEN INTERACTION; HYDROLYSIS; METARHIZIUM ANISOPLIAE; MOLECULAR PATHOLOGY; NONHUMAN; PHYSIOLOGICAL STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; TOXICITY TESTING; ZYMOGRAPHY; CHEMISTRY; METABOLISM; METARHIZIUM; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS;

ANIMALIA; ARTHROPODA; FUNGI; METARHIZIUM ANISOPLIAE;

ELECTROPHORESIS, POLYACRYLAMIDE GEL; FUNGAL PROTEINS; HOST-PATHOGEN INTERACTIONS; HYDROLYSIS; METARHIZIUM;

EID: 77953432815     PISSN: 00410101     EISSN: 18793150     Source Type: Journal    
DOI: 10.1016/j.toxicon.2009.12.012     Document Type: Article

References (53)

1. Bagga S., Hu G., Screen S.E., St Leger R.J. Reconstructing the diversity of subtilisins in the pathogenic fungus Metarhizium anisopliae. Gene 2004, 324:159-169.
2. Berger M., Pinto A.F.M., Guimarães J.A. Purification and functional characterization of bothrojaractivase, a prothormbin-activating metalloproteinase isolated from Bothrops jararaca snake venom. Toxicon 2008, 51(4):488-501.
3. Berto P., Comménil P., Belingheri L., Dehorter B. Occurrence of a lipase in spores of Alternaria brassicicola with a crucial role in infection of cauliflower leaves. FEMS Microbiol. Lett. 1999, 180(2):183-189.
4. Beyer W.F., Fridovich I. Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal. Biochem. 1987, 161:559-566.
5. Bogo M.R., Rota C.A., Pinto H., Ocampos M., Correa C.T., Vainstein M.H., Schrank A. A chitinase encoding gene (chit1 gene) from the entomopathogenic Metarhizium anisopliae: isolation and characterization of genomic and full-length cDNA. Curr. Microbiol. 1998, 37(4):221-225.
6. Cakmak I., Marschner H. Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase and glutathione reductase in bean leaves. Plant Physiol. 1992, 98(4):1222-1227.
7. Charnley A.K. Fungal pathogens of insects: cuticle degrading enzymes and toxins. Adv Bot Res. 2003, 40:241-321.
8. Dani M.P., Edwards J.P., Richards E.H. Hydrolase activity in the venom of the pupal endoparasitic wasp, Pimpla hypochondriaca. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2005, 141(3):373-381.
9. Davies K.A., De Lorono I., Foster S.J., Li D., Johnstone K., Ashby A.M. Evidence for a role of cutinase in pathogenicity of Pyrenopeziza brassicae on brassicas. Phys. Mol. Plant Pathol. 2000, 57:63-75.
10. Diaz P., Prim N., Javier Pastor F.I. Direct fluorescence based lipase activity assay. Biotechniques 1999, 27(4):696-700.
11. Donatti A.C., Furlaneto-Maia L., Fungaro M.H., Furlaneto M.C. Production and regulation of cuticle-degrading proteases from Beauveria bassiana in the presence of Rhammatocercus schistocercoides cuticle. Curr. Microbiol. 2008, 56(3):256-260.
12. Fan Y., Fang W., Guo S., Pei X., Zhang Y., Xiao Y., Li D., Jin K., Bidochka M.J., Pei Y. Increased insect virulence in Beauveria bassiana strains overexpressing an e engineered chitinase. Appl. Environ. Microbiol. 2007, 73(1):295-302.
13. Frazzon A.P.G., Da Silva Vaz Junior I., Masuda A., Schrank A., Vainstein M.H. In vitro assessment of Metarhizium anisopliae isolates to control the cattle tick Boophilus microplus. Vet. Parasitol. 2000, 94(1-2):117-125.
14. Freimoser F.M., Hu G., St Leger R.J. Variation in gene expression patterns as the insect pathogen Metarhizium anisopliae adapts to different host cuticles or nutrient deprivation in vitro. Microbiology 2005, 151(2):361-371.
15. Garre V., Tenberge K.V., Eising R. Secretion of a fungal extracellular catalase by Claviceps purpurea during infection of rye: putative role in pathogenicity and suppression of host defense. Phytopathology 1998, 88(8):744-753.
16. Ghannoum M.A. Potential role of phospholipases in virulence and fungal pathogenesis. Clin. Microbiol. Rev. 2000, 13(1):122-143.
17. Gillespie J.P., Bateman R., Charnley A.K. Role of cuticle-degrading proteases in the virulence of Metarhizium spp. for the desert locust, Schistocerca gregaria. J. Invert. Pathol. 1998, 71(2):128-137.
18. Göttlich E., de Hong G.S., Yoshida S., Takeo K., Nishimura K., Miyaji M. Cell-surface hydrophobicity and lipolysis as essential factors in human tinea nigra. Mycoses 1995, 38(12-13):489-494.
19. Ibrahim A.S., Mirbod F., Filler S.G., Banno Y., Cole G.T., Kitajima Y., Edwards J.E., Nozawa Y., Ghannoum M.A. Evidence implicating phospholipase as a virulence factor of Candida albicans. Infect. Immun. 1995, 63(5):1993-1998.
20. Joshi L., St Leger R.J. Cloning, expression, and substrate specificity of MeCPA, a zinc carboxypeptidase that is secreted into infected tissues by the fungal entomopathogen Metarhizium anisopliae. J. Biol. Chem. 1999, 274(14):9803-9811.
21. Krieger de Moraes C., Schrank A., Vainstein M.H. Regulation of extracellular chitinases and proteases in the entomopathogen and acaricide Metarhizium anisopliae. Curr. Microbiol. 2003, 46(3):205-210.
22. Kurioka S., Matsuda M. Phospholipase C assay using p-nitrophosphorylcholine together with sorbitol and its application to studying the metal and detergent requirement of the enzyme. Anal. Biochem. 1976, 75:281-289.
23. Liu Y., Wag Z., Yin Y., Cao Y., Zhao H., Xia Y. Expression, purification, and characterization of recombinant Metarhizium anisopliae acid trehalase in Pichia pastoris. Protein Expr. Purif. 2004, 54(1):66-72.
24. Pedrini N., Crespo R., Juarez M.P. Biochemistry of insect epicuticle degradation by entomopathogenic fungi. Comput. Biochem. Physiol. C Toxicol. Pharmacol. 2007, 146(1-2):124-137.
25. Pinto A.F.M., Silva K.R.L.M., Guimarães J.A. Proteases from Lonomia obliqua venomous secretions: comparison of procoagulant, fibrin(ogen)olytic and amidolytic activities. Toxicon 2006, 47(1):113-121.
26. Qazi S.S., Khachatourians G.G. Hydrated conidia of Metarhizium anisopliae release a family of metalloproteases. J. Invert. Pathol. 2007, 95(1):48-59.
27. Quesada-Moraga E., Santos-Quirós R., Valverde-García P., Santiago-álarez C. Virulence, horizontal transmission, and sublethal reproductive effects of Metarhizium anisopliae (Anamorphic fungi) on the German cockroach (Blattodea: Blattellidae). J. Invertebr. Pathol. 2004, 87(1):51-58.
28. Rangel D.E.N., Braga G.U., Flint S.D., Anderson A.J., Roberts D.W. Variations in UV-B tolerance and germination speed of Metarhizium anisopliae conidia produced on insects and artificial substrates. J. Invertebr. Pathol. 2004, 87(2-3):77-83.
29. Rangel D.E.N., Alston D.G., Roberts D.W. Effects of physical and nutritional stress conditions during mycelial growth on conidial germination speed, adhesion to host cuticle, and virulence of Metarhizium anisopliae, an entomopathogenic fungus. Mycol. Res. 2008, 112(11):1355-1361.
30. Roberts D.W., St Leger R.J. Metarhizium spp., cosmopolitan insect-pathogenic fungi: mycological aspects. Adv. Appl. Microbiol. 2004, 54:1-70.
31. Salyers A., Witt D. Virulence factors that promote colonization. Bacterial Pathogenesis: A Molecular Approach 1994, 30-46. ASM Press, Washington, DC. A. Salyers, D. Witt (Eds.).
32. Schofield D.A., Westwater C., Warner T., Balish E. A diferential Candida albicans lipase gene expression during alimentary tract colonization and infection. FEMS Microbiol. Lett. 2005, 244(2):359-365.
33. Scholte E.-J., Ng'habi K., Kihonda J., Takken W., Paaijman K., Abdulla S., Killeen G.F., Knols B.G.J. An entomopathogenic fungus for control of adult african malaria mosquitoes. Science 2005, 308(5728):1641-1642.
34. Schrank A., Bassanesi M.C., Pinto H., Costa S.V., Bogo M.R., Silva M.S.N. Superoxide dismutases in the entomopathogenic fungus Metarhizium anisopliae. Ciência e Cultura 1993, 45:200-205.
35. Screen S.E., St Leger R.J. Cloning, expression, and substrate specificity of a fungal chymotrypsin. Evidence for lateral gene transfer from an actinomycete bacterium. J. Biol. Chem. 2000, 275(9):6689-6694.
36. Selvaggini S., Munro C.A., Paschoud S., Sanglard D., Gow N.A. Independent regulation of chitin synthase and chitinase activity in Candida albicans and Saccharomyces cerevisiae. Microbiology 2004, 150(4):921-928.
37. Shah P.A., Pell J.K. Entomopathogenic fungi as biological control agents. Appl. Microbiol. Biotechnol. 2003, 61(5-6):413-423.
38. Shah F.A., Allen N., Wright C.J., Butt T.M. Repeated in vitro subculturing alters spore surface properties and virulence of Metarhizium anisopliae. FEMS Microbiol. Lett. 2007, 276(1):60-66.
39. Silva M.V., Santi L., Staats C.C., Costa A.M., Colodel E.M., Driemeier D., Vainstein M.H., Schrank A. Cuticle-induced endo/exoacting chitinase CHIT30 from Metarhizium anisopliae is encoded by an ortholog of the chi3 gene. Res. Microbiol. 2005, 156(3):382-392.
40. Silva W.O.B., Mitidieri S., Schrank A., Vainstein M.H. Production and extraction of an extracellular lipase from the entomopathogenic fungus Metarhizium anisopliae. Proc. Biochem. 2005, 40(1):321-326.
41. Small C.L.N., Bidochka M.J. Up-regulation of Pr1, a subtilisin-like protease, during conidiation in the insect pathogen Metarhizium anisopliae. Mycol. Res. 2005, 109(3):307-313.
42. Smith P.K., Krohn R.I., Hermanson G.T., Mallia A.K., Gartner F.H., Provenzano M.D., et al. Measurement of the principle of protein-dye binding. Anal. Biochem. 1985, 150:76-85.
43. St Leger R.J., Staples R.C., Roberts D.W. Entomopathogenic isolates of Metarhizium anisopliae, Beauveria bassiana, and Aspergillus flavus produce multiple extracellular chitinase isozymes. J. Invert. Pathol. 1993, 61:81-84.
44. St Leger R.J., Joshi L., Bidochka R.J., Rizzo N.W., Roberts D.W. Biochemical characterization and ultrastructural localization of two extracellular trypsins produced by Metarhizium anisopliae in infected insect cuticles. Appl. Env. Microbiol. 1996, 62(4):1257-1264.
45. St Leger R.J., Joshi L., Bidochka M.J., Rizzo N.W., Roberts D.W. Characterization and ultrastructural localization of chitinases from Metarhizium anisopliae, M. flavoviride, and Beauveria bassiana during fungal invasion of host (Manduca sexta) cuticle. Appl. Environ. Microbiol. 1996, 62(3):907-912.
46. St Leger R.J., Joshi L., Roberts D.W. Ambient pH is a major determinant in the expression of cuticle-degrading enzymes and hydrophobin by Metarhizium anisopliae. Appl. Env. Microbiol. 1998, 64(2):709-713.
47. Stehr F., Kretschmar M., Kroger C., Hube B., Schafer W. Microbial lipases as virulence factors. J. Mol. Catal. B Enzym. 2003, 22(5-6):347-355.
48. Tolfo Bittencourt S.E., Castro L.A., Farias S.E., Bao S.N., Schrank A., Vainstein M.H. Purification and ultrastructural localization of a copper-zinc superoxide dismutase (CuZnSOD) from the entomopathogenic and acaricide fungus Metarhizium anisopliae. Res. Microbiol. 2004, 155(8):681-687.
49. Vieira I.C., Lupetti K.O., Fatibello-Filho O. Determination of paracetamol in pharmaceutical products using a carbon paste biosensor modified with crude extract of zucchini (Cucurbita pepo). Quimica Nova 2003, 26:39-43.
50. Voigt C.A., Schafer W., Salomon S. A secreted lipase of Fusarium graminearum is a virulence factor required for infection of cereals. Plant J. 2005, 42(3):364-375.
51. Xia Y., Clarkson J.M., Charnley A.K. Trehalose-hydrolysis enzymes of Metarhizium anisopliae and their role in pathogenesis of the tobacco hornworm, Manduca sexta. J. Invert. Pathol. 2002, 80(3):139-147.
52. Zhang Y., Liu X., Wang M. Cloning, expression, and characterization of two novel cuticle-degrading serine proteases from the entomopathogenic fungus Cordyceps sinensis. Res. Microbiol. 2008, 159(6):462-469.
53. Zimmermann P., Heinlein C., Orendi G., Zentgraf U. Senescence-specific regulation of catalases in Arabidopsis thaliana (L.) Heynh. Plant Cell Environ. 2006, 29:1049-1060.