Characterization of a β-1,3-glucanase active in the alkaline midgut of Spodoptera frugiperda larvae and its relation to β-glucan-binding proteins

Insect Biochemistry and Molecular Biology

Volumn 40, Issue 12, 2010, Pages 861-872

  Bragatto, Ivan ^a   Genta, Fernando A ^a,b   Ribeiro, Alberto F ^a   Terra, Walter R ^a   Ferreira, Clélia ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

Glucan binding proteins; Insect 1,3 glucanase; Molluskan 1,3 glucanase; PH optimum displacement; Processivity

Indexed keywords

CARRIER PROTEIN; GLUCAN 1,3 BETA GLUCOSIDASE; GLUCAN BINDING PROTEINS; GLUCAN-BINDING PROTEINS; INSECT PROTEIN; LAMINARAN; LECTIN; POLYSACCHARIDE;

AMINO ACID SEQUENCE; ANIMAL; ARMYWORM; ARTICLE; CHEMISTRY; ENZYMOLOGY; GASTROINTESTINAL TRACT; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; LARVA; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CARRIER PROTEINS; GASTROINTESTINAL TRACT; GLUCAN 1,3-BETA-GLUCOSIDASE; INSECT PROTEINS; LARVA; LECTINS; MOLECULAR SEQUENCE DATA; POLYSACCHARIDES; SEQUENCE ALIGNMENT; SPODOPTERA;

ARTHROPODA; HEXAPODA; LEPIDOPTERA; MOLLUSCA; SACCHAROMYCES; SPODOPTERA FRUGIPERDA;

EID: 78649633218     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2010.08.006     Document Type: Article

References (65)

1. Arnold K., Bordoli L., Kopp J., Schwede T. The SWISS-MODEL workspace: a web-based environment for protein structure homology modeling. Bioinformatics 2006, 22:195-201.
2. Bates P.A., Kelley L.A., MacCallum R.M., Sternberg M.J. Enhancement of protein modeling by human intervention in applying the automatic programs 3D-JIGSAW and 3D-PSSM. Proteins 2001, (Suppl. 5):39-46.
3. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: signalP 3.0. J. Mol. Biol. 2004, 340:783-795.
4. Blum H., Beier H., Gross H.J. Improved silver staining of plant-proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 1987, 8:93-99.
5. Bolognesi R., Ribeiro A.F., Terra W.R., Ferreira C. The peritrophic membrane of Spodoptera frugiperda: secretion of peritrophins and role in immobilization and recycling digestive enzymes. Arch. Insect Biochem. Physiol. 2001, 47:62-75.
6. Bolognesi R., Terra W.R., Ferreira C. Peritrophic membrane role in enhancing digestive efficiency. Theoretical and experimental models. J. Insect Physiol. 2008, 54:1413-1422.
7. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
8. Broderick N.A., Goodman R.M., Handelsman J., Raffa K.F. Effect of host diet and insect source on synergy of gypsy moth (Lepidoptera: Lymantriidae) mortality to Bacillus thuringiensis subsp kurstaki by zwittermicin A. Environ. Entomol. 2003, 32:387-391.
9. Bulmer M.S., Crozier R.H. Variation in posture selection in termite GNPs and relish. Mol. Biol. Evol. 2006, 23:317-326.
10. Combet C., Jambon M., Deleage G., Geourjon C. Geno3D: automatic comparative molecular modelling of protein. Bioinformatics 2002, 18:213-214.
11. Dahlqvist A. Assay of intestinal disaccharidases. Anal. Biochem. 1968, 22:99-107.
12. Davies G., Henrissat B. Structures and mechanisms of glycosyl hydrolases. Structure 1995, 3:853-859.
13. Davis I.W., Leaver-Fay A., Chen V.B., Block J.N., Kapral G.J., Wang X., Murray L.W., Arendall W.B., Snoeyink J., Richardson J.S., Richardson D.C. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 2007, 35:W375-W383.
14. Ewin B., Green P. Basecalling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 1998, 8:186-194.
15. Ewin B., Hillier L., Wendl M., Green P. Basecalling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 1998, 8:175-185.
16. Fabrick J.A., Baker J.E., Kanost M.R. cDNA cloning, purification, properties, and function of a beta-1,3-glucan recognition protein from a pyralid moth, Plodia interpunctella. Insect Biochem. Mol. Biol. 2003, 33:579-594.
17. Ferreira C., Capella A.N., Sitnik R., Terra W.R. Properties of the digestive enzymes and the permeability of the peritrophic membrane of Spodoptera frugiperda (Lepidoptera) larvae. Comp. Biochem. Phys. A 1994, 107:631-640.
18. Ferreira A.H., Marana S.R., Terra W.R., Ferreira C. Purification, molecular cloning, and properties of a beta-glycosidase isolated from midgut lumen of Tenebrio molitor (Coleoptera) larvae. Insect Biochem. Mol. Biol. 2001, 31:1065-1076.
19. Fibriansah G., Masuda S., Koizumi N., Nakamura S., Kumasaka T. The 1.3 A crystal structure of a novel endo-beta-1,3-glucanase of glycoside hydrolase family 16 from alkaliphilic Nocardiopsis sp. strain F96. Proteins 2007, 69:683-690.
20. Genta F.A., Terra W.R., Ferreira C. Action pattern, specificity, lytic activities, and physiological role of five digestive beta-glucanases isolated from Periplaneta americana. Insect Biochem. Mol. Biol. 2003, 33:1085-1097.
21. Genta F.A., Blanes L., Cristofoletti P.T., do Lago C.L., Terra W.R., Ferreira C. Purification, characterization and molecular cloning of the major chitinase from Tenebrio molitor larval midgut. Insect Biochem. Mol. Biol. 2006, 36:789-800.
22. Genta F.A., Dillon R.J., Terra W.R., Ferreira C. Potential role for gut microbiota in cell wall digestion and glucoside detoxification in Tenebrio molitor larvae. J. Insect Physyol. 2006, 52:593-601.
23. Genta F.A., Dumont A.F., Marana S.R., Terra W.R., Ferreira C. The interplay of processivity, substrate inhibition and a secondary substrate binding site of an insect exo-beta-1,3-glucanase. Biochim. Biophys. Acta 2007, 1774:1079-1091.
24. Genta F.A., Bragatto I., Terra W.R., Ferreira C. Purification, characterization and sequencing of the major beta-1,3-glucanase from the midgut of Tenebrio molitor larvae. Insect Biochem. Mol. Biol. 2009, 39:861-874.
25. Guex N., Peitsch M.C. SWISS-MODEL and the Swiss-Pdb viewer: an environment for comparative protein modeling. Electrophoresis 1997, 18:2714-2723.
26. Halanych K.M. The new view of animal phylogeny. Ann. Rev. Ecol. Evol. Syst. 2004, 35:229-256.
27. Higgins, D.R., Cregg, J.M., 1998. Introduction to Pichia Pastoris. Methods Mol. Biol: Pichia Protocols, Humana Press, Totowa, NJ, pp. 1-15.
28. Janeway C.A., Medzhitov R. Innate immune recognition. Annu. Rev. Immunol. 2002, 20:197-216.
29. Jordão B.P., Terra W.R., Ribeiro A.F., Lehane M.J., Ferreira C. Trypsin secretion in Musca domestica larval midguts. A biochemical and immunocytochemical study. Insect Biochem. Mol. Biol. 1996, 26:337-346.
30. Jordao B.P., Capella A.N., Terra W.R., Ribeiro A.F., Ferreira C. Nature of the anchors of membrane-bound aminopeptidase, amylase, and trypsin and secretory mechanisms in Spodoptera frugiperda (Lepidoptera) midgut cells. J. Insect Physiol. 1999, 45:29-37.
31. Kanost M.R., Jiang H., Yu X.Q. Innate immune responses of a lepidopteran insect, Manduca sexta. Immunol. Rev. 2004, 198:97-105.
32. Kelley L.A., Sternberg M.J. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 2009, 4:363-371.
33. Kovalchuk S.N., Sundukova E.V., Kusaykin M.I., Guzev K.V., Anastiuk S.D., Likhatskaya G.N., Trifonov E.V., Nurminski E.A., Kozhemyako V.B., Zvyagintseva T.N., Rasskazov V.A. Purification, cDNA cloning and homology modeling of endo-1,3-beta-D-glucanase from scallop Mizuhopecten yessoensis. Comp. Biochem. Phys. B. Biol. 2006, 143B:473-485.
34. Kovalchuk S.N., Bakunina I.Y., Burtseva Y.V., Emelyanenko V.I., Kim N.Y., Guzev K.V., Kozhemyako V.B., Rasskazov V.A., Zvyagintseva T.N. An endo-(1->3)-beta-D-glucanase from the scallop Chlamys albidus: catalytic properties, cDNA cloning and secondary-structure characterization. Carbohydr. Res. 2009, 344:191-197.
35. Kumagai Y., Ojima T. Enzymatic properties and the primary structure of a beta-1,3-glucanase from the digestive fluid of the Pacific abalone Haliotis discus hannai. Comp. Biochem. Phys. 2009, 154B:113-120.
36. Kumagai Y., Ojima T. Isolation and characterization of two types of beta-1,3-glucanases from the common sea hare Aplysia kurodai. Comp. Biochem. Phys. 2010, 155B:138-144.
37. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
38. Lambert C., Leonard N., De Bolle X., Depiereux E. ESyPred3D: prediction of proteins 3D structures. Bioinformatics 2002, 18:1250-1256.
39. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Cryst. 1993, 26:283-291.
40. Lund O., Nielsen M., Lundegaard C., Worning P. CPH Models 2.0 X3M a Computer Program to Extract 3D Models 2002, Abstracts of the CASP5 Conference A102.
41. Manchenko G.P. Handbook of Detection of Enzymes on Electrophoretic Gels 1994, CRC, Boca Raton.
42. Marana S.R., Jacobs-Lorena M., Terra W.R., Ferreira C. Amino acid residues involved in substrate binding and catalysis in an insect digestive beta-glycosidase. Biochim. Biophys. Acta 2001, 1545:41-52.
43. Marinotti O., Nguyen Q.K., Calvo E., James A.A., Ribeiro J.M. Microarray analysis of genes showing variable expression following a blood meal in Anopheles gambiae. Insect Mol. Biol. 2005, 14:365-373.
44. Mishima Y., Quintin J., Aimanianda V., Kellenberger C., Coste F., Clavaud C., Hetru C., Hoffman J.A., Latgé J.-P., Ferrandon D., Roussel A. The N-terminal domain of Drosophila Gram-negative binding protein 3 (GNBP3) defines a novel family of fungal pattern recognition receptors. J. Biol. Chem. 2009, 284:28687-28697.
45. Nakashima J., Laosinchai W., Cui X.J., Brown R.M. New insight into the mechanism of cellulose and callose biosynthesis: proteases may regulate callose biosynthesis upon wounding. Cellulose 2003, 10:369-389.
46. Noelting G., Bernfeld P. Sur les enzymes amylolitiques. III. La beta-amilase: dosage d'activité et contrôle de l'absence d'alfa-amilase. Helv. Chim. Acta 1948, 31:286-290.
47. Ochiai M., Ashida M. A pattern-recognition protein for beta-1,3-glucan. The binding domain and the cDNA cloning of beta-1,3-glucan recognition protein from the silkworm, Bombyx mori. J. Biol. Chem. 2000, 275:4995-5002.
48. Oviedo N.M., Vanekeris L., Corena-McLeod M.D., Linser P.J. A microarray-based analysis of transcriptional compartmentalization in the alimentary cAnal. of Anopheles gambiae (Diptera: Culicidae) larvae. Insect Mol. Biol. 2008, 17:61-72.
49. Parra J.R.P. Criação de Insetos para Estudos com Patógenos. Controle microbiano de Insetos. São Paulo: Editora Manole 1986, 348-373. S.B. Alvez (Ed.).
50. Pauchet Y., Freitak D., Heidel-Fischer H.M., Heckel D.G., Vogel H. Immunity or digestion: glucanase activity in a glucan-binding protein family from Lepidoptera. J. Biol. Chem. 2009, 284:2214-2224.
51. Radford J.E., Vesk M., Overall R.L. Callose deposition at plasmodesmata. Protoplasma 1998, 201:30-37.
52. Robyt J.F., French D. Multiple attach hypothesis of alpha-amylase action: action of porcine pancreatic, human salivary, and Aspergillus oryzae alpha-amylases. Arch. Biochem. Biophys. 1967, 122:8-16.
53. Rocchia W., Sridharan S., Nicholls A., Alexov E., Chiabrera A., Honig B. Rapid grid-based construction of the molecular surface and the use of induced surface charge to calculate reaction field energies: applications to the molecular systems and geometric objects. J. Comput. Chem. 2002, 23:128-137.
54. Shapiro A.L., Vinuela E., Maizel J.V. Molecular weight estimation of polypeptide chains by electrophoresis in SDS-polyacrylamide gels. Biochem. Biophys. Res. Commun. 1967, 28:815-820.
55. Silva M.C., Ribeiro A.F., Terra W.R., Ferreira C. Sequencing of Spodoptera frugiperda midgut trehalases and demonstration of secretion of soluble trehalase by midgut columnar cells. Insect Mol. Biol. 2009, 18:769-784.
56. Takahashi K., Ochiai M., Horiuchi M., Kumeta H., Ogura K., Ashida M., Inagaki F. Solution structure of the silkworm βGRP/GNBP3 N-terminal domain reveals the mechanism for β-1,3-glucan-specific recognition. Proc. Nat. Acad. Sci. 2009, 106:11679-11684.
57. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
58. Teodorescu O., Galor T., Pillardy J., Elber R. Enriching the sequence substitution matrix by structural information. Proteins 2004, 54:41-48.
59. Terra W.R., Ferreira C. Insect digestive enzymes - properties, compartmentalization and function. Comp. Biochem. Phys. 1994, 109B:1-62.
60. Terra W.R., Ferreira C. Biochemistry of digestion. Biochemistry and Molecular Biology 2005, vol. 4:171-224. Elsevier, Oxford. L.I. Gilbert, K. Iatrov, S.S. Gill (Eds.).
61. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 1979, 76:4350-4354.
62. Tusnady G.E., Simon I. Principles governing amino acid composition of integral membrane proteins: Applications to topology prediction. J. Mol. Biol. 1998, 283:489-506.
63. Tusnady G.E., Simon I. The HMMTOP transmembrane topology prediction server. Bioinformatics 2001, 17:849-850.
64. Warr E., Das S., Dong Y., Dimopoulos G. The Gram-negative bacteria-binding protein gene family: its role in the innate immune system of Anopheles gambiae and in anti-Plasmodium defence. Insect Mol. Biol. 2008, 17:39-51.
65. Zhang R., Cho H.Y., Kim H.S., Ma Y.G., Osaki T., Kawabata S., Soderhall K., Lee B.L. Characterization and properties of a 1,3-beta-D-glucan pattern recognition protein of Tenebrio molitor larvae that is specifically degraded by serine protease during prophenoloxidase activation. J. Biol. Chem. 2003, 278:42072-42079.