Identification of novel Cry1Ac binding proteins in midgut membranes from Heliothis virescens using proteomic analyses

Insect Biochemistry and Molecular Biology

Volumn 37, Issue 3, 2007, Pages 189-201

  Krishnamoorthy, M ^a   Jurat Fuentes, J L ^a   McNall, R J ^a   Andacht, T ^a   Adang, Michael J ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

2D electrophoresis; Alkaline phosphatase; Bacillus thuringiensis; Cry1Ac; Heliothis virescens; Peptide mass fingerprinting; Proteomics

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL TOXIN; CELL SURFACE RECEPTOR; CRY TOXIN RECEPTORS, BACILLUS THURINGIENSIS; ENDOTOXIN; GLYCOSYLPHOSPHATIDYLINOSITOL; HEMOLYSIN; INSECT PROTEIN; INSECTICIDAL CRYSTAL PROTEIN, BACILLUS THURINGIENSIS; UNCLASSIFIED DRUG;

ANIMAL; ARTICLE; CHEMISTRY; CYTOLOGY; GASTROINTESTINAL TRACT; MASS SPECTROMETRY; METABOLISM; MICROVILLUS; MOTH; PEPTIDE MAPPING; PROTEOMICS; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL TOXINS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ENDOTOXINS; GASTROINTESTINAL TRACT; GLYCOSYLPHOSPHATIDYLINOSITOLS; HEMOLYSIN PROTEINS; INSECT PROTEINS; MASS SPECTROMETRY; MICROVILLI; MOTHS; PEPTIDE MAPPING; PROTEOMICS; RECEPTORS, CELL SURFACE;

BACILLUS THURINGIENSIS; HELIOTHIS VIRESCENS;

EID: 33846821854     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2006.10.004     Document Type: Article

References (48)

1. Azuma M., and Eguchi M. Discrete localization of distinct alkaline phosphatase isozymes in the cell surface of silkworm midgut epithelium. J. Exp. Zool. 251 (1989) 108-112
2. Azuma M., Takeda S., Yamamoto H., Endo Y., and Eguchi M. Goblet cell alkaline phosphatase in silkworm midgut epithelium: its entity and role as an ATPase. J. Exp. Biol. 258 (1991) 294-302
3. Bandani A.R., Amiri B., Butt T.M., and Gordon-Weeks R. Effects of efrapeptin and destruxin, metabolites of entomogenous fungi, on the hydrolytic activity of a vacuolar type ATPase identified on the brush border membrane vesicles of Galleria mellonella midgut and on plant membrane bound hydrolytic enzymes. Biochim. Biophys. Acta 1510 (2001) 367-377
4. Banks D.J., Jurat-Fuentes J.L., Dean D.H., and Adang M.J. Bacillus thuringiensis Cry1Ac and Cry1Fa delta-endotoxin binding to a novel 110 kDa aminopeptidase in Heliothis virescens is not N-acetylgalactosamine mediated. Insect Biochem. Molec. Biol. 31 (2001) 909-918
5. Betz F.S., Hammond B.G., and Fuchs R.L. Safety and advantages of Bacillus thuringiensis-protected plants to control insect pests. Regul. Toxicol. Pharmacol. 32 (2000) 156-173
6. Bradford M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
7. Bravo A., Gomez I., Conde J., Munoz-Garay C., Sanchez J., Miranda R., Zhuang M., Gill S.S., and Soberon M. Oligomerization triggers binding of a Bacillus thuringiensis Cry1Ab pore-forming toxin to aminopeptidase N receptor leading to insertion into membrane microdomains. Biochim. Biophys. Acta 1667 (2004) 38-46
8. Candas M., Loseva O., Oppert B., Kosaraju P., and Bulla Jr. L.A. Insect Resistance to Bacillus thuringiensis: alterations in the Indianmeal Moth Larval Gut Proteome. Mol. Cell. Proteomics 2 (2003) 19-28
9. English L.H., and Cantley L.C. Delta endotoxin is a potent inhibitor of the (Na,K)-ATPase. J. Biol. Chem 261 (1986) 1170-1173
10. English L., and Readdy T.L. Delta endotoxin inhibits a phosphatase in midgut epithelial membranes of Heliothis virescens. Insect Biochem 19 (1989) 145-152
11. Fernandez L.E., Aimanova K.G., Gill S.S., Bravo A., and Soberon M. A GPI-anchored alkaline phosphatase is a functional midgut receptor of Cry11Aa toxin in Aedes aegypti larvae. Biochem. J. 394 (2006) 77-84
12. Gahan L.J., Gould F., and Heckel D.G. Identification of a gene associated with Bt resistance in Heliothis virescens. Science 293 (2001) 857-860
13. Gill S., Cowles E.A., and Francis V. Identification, isolation, and cloning of a Bacillus thuringiensis CryIAc toxin-binding protein from the midgut of the lepidopteran insect Heliothis virescens. J. Biol. Chem. 270 (1995) 27277-27282
14. Griffitts J.S., Huffman D.L., Whitacre J.L., Barrows B.D., Marroquin L.D., Muller R., Brown J.R., Hennet T., Esko J.D., and Aroian R.V. Resistance to a bacterial toxin is mediated by removal of a conserved glycosylation pathway required for toxin-host interactions. J. Biol. Chem. 278 (2003) 45594-45602
15. Han Y., Ma B., and Zhang K. SPIDER: software for protein identification from sequence tags with de novo sequencing error. J. Bioinform. Comput. Biol. 3 (2005) 697-716
16. Ikeda W., Nakanishi H., Miyoshi J., Mandai K., Ishizaki H., Tanaka M., Togawa A., Takahashi K., Nishioka H., Yoshida H., Mizoguchi A., Nishikawa S., and Takai Y. Afadin: a key molecule essential for structural organization of cell-cell junctions of polarized epithelia during embryogenesis. J. Cell Biol. 146 (1999) 1117-1132
17. Ishii K., and Green K.J. Cadherin function: breaking the barrier. Curr. Biol. 11 (2001) R569-R572
18. Jurat-Fuentes J.L., and Adang M.J. Importance of Cry1 delta-endotoxin domain II loops for binding specificity in Heliothis virescens (L.). Appl. Environ. Microbiol. 67 (2001) 323-329
19. Jurat-Fuentes J.L., and Adang M.J. Characterization of a Cry1Ac-receptor alkaline phosphatase in susceptible and resistant Heliothis virescens larvae. Eur. J. Biochem. 271 (2004) 3127-3135
20. Jurat-Fuentes J.L., Gould F.L., and Adang M.J. Altered Glycosylation of 63- and 68-kilodalton microvillar proteins in Heliothis virescens correlates with reduced Cry1 toxin binding, decreased pore formation, and increased resistance to Bacillus thuringiensis Cry1 toxins. Appl. Environ. Microbiol. 68 (2002) 5711-5717
21. Jurat-Fuentes J.L., Gahan L.J., Gould F.L., Heckel D.G., and Adang M.J. The HevCaLP protein mediates binding specificity of the Cry1A class of Bacillus thuringiensis toxins in Heliothis virescens. Biochemistry 43 (2004) 14299-14305
22. Knowles B.H. Mechanism of action of Bacillus thuringiensis insecticidal δ-endotoxins. Adv. Insect Physiol. 24 (1994) 275-308
23. Lester P.J., and Hubbard S.J. Comparative bioinformatic analysis of complete proteomes and protein parameters for cross-species identification in proteomics. Proteomics 2 (2002) 1392-1405
24. Luo K., Sangadala S., Masson L., Mazza A., Brousseau R., and Adang M.J. The Heliothis virescens 170 kDa aminopeptidase functions as "receptor A" by mediating specific Bacillus thuringiensis Cry1A delta-endotoxin binding and pore formation. Insect Biochem. Molec. Biol. 27 (1997) 735-743
25. Luo K., Banks D., and Adang M.J. Toxicity, binding and permeability analyses of four Bacillus thuringiensis Cry1 δ-endotoxins by use of brush border membrane vesicles of Spodoptera exigua and Spodoptera frugiperda. Appl. Environ. Microbiol. 65 (1999) 457-464
26. McNall R.J., and Adang M.J. Identification of novel Bacillus thuringiensis Cry1Ac binding proteins in Manduca sexta midgut through proteomic analysis. Insect Biochem. Molec. Biol. 33 (2003) 999-1010
27. Mechanic S., Raynor K., Hill J.E., and Cowin P. Desmocollins form a distinct subset of the cadherin family of cell adhesion molecules. Proc. Natl. Acad. Sci. USA 88 (1991) 4476-4480
28. Minami M., Indrasith L.S., and Hori H. Characterization of ATPase activity in brush border membrane vesicles from the silkworm, Bombyx mori. Agric. Biol. Chem. 55 (1991) 2693-2700
29. Nollet F., Kools P., and van Roy F. Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J. Mol. Biol. 299 (2000) 551-572
30. Okada N., Azuma M., and Egushi M. Alkaline phosphatase isozymes in the midgut of the silkworm: purification of high pH-stabile microvillus and labile cytosolic enzymes. Comp. Biochem. Physiol. 159B (1989) 123-150
31. Oltean D.I., Pullikuth A.K., Lee H.K., and Gill S.S. Partial purification and characterization of Bacillus thuringiensis Cry1A toxin receptor A from Heliothis virescens and cloning of the corresponding cDNA. Appl. Environ. Microbiol. 65 (1999) 4760-4766
32. + efflux in vitro. J. Biol. Chem. 269 (1994) 10088-10092
33. Shevchenko A., Sunyaev S., Loboda A., Shevchenko A., Bork P., Ens W., and Standing K.G. Charting the proteomes of organisms with unsequenced genomes by MALDI-quadrupole time-of-flight mass spectrometry and BLAST homology searching. Anal. Chem. 73 (2001) 1917-1926
34. Shimada Y., Usui T., Yanagawa S., Takeichi M., and Uemura T. Asymmetric colocalization of Flamingo, a seven-pass transmembrane cadherin, and Dishevelled in planar cell polarization. Curr. Biol. 11 (2001) 859-863
35. Takesue Y., Yokota K., Miyajima K., Taguchi R., and Ikezawa H. Membrane anchors of alkaline phosphatase and trehalase associated with the plasma membrane of larval midgut epithelial cells of the silkworm, Bombyx mori. J. Biochem. 105 (1989) 998-1001
36. Terra W.R., and Ferreira C. Insect digestive enzymes: properties, compartmentalization and function. Comp. Biochem. Physiol. 109B (1994) 1-62
37. Tuloup, M., Hernandez, C., Coro, I., Hoogland, C., Binz, P.A., Appel, R.D., 2003. Aldente and BioGraph: an improved peptide mass fingerprinting protein identification environment. In: FontisMedia (Ed.), Swiss Proteomics Society 2003 Congress: Understanding biological systems through proteomics, Basel, Switzerland, pp. 147-176.
38. Van Rie J., Jansens S., Höfte H., Degheele D., and Van Mellaert H. Specificity of Bacillus thuringiensis delta-endotoxins. Importance of specific receptors on the brush border membrane of the mid-gut of target insects. Eur. J. Biochem. 186 (1989) 239-247
39. Vitavska O., Wieczorek H., and Merzendorfer H. A novel role for subunit C in mediating binding of the H+-V-ATPase to the actin cytoskeleton. J. Biol. Chem. 278 (2003) 18499-18505
40. Vitavska O., Merzendorfer H., and Wieczorek H. The V-ATPase subunit C binds to polymeric F-actin as well as to monomeric G-actin and induces cross-linking of actin filaments. J. Biol. Chem. 280 (2005) 1070-1076
41. Wieczorek H., Gruber G., Harvey W.R., Huss M., and Merzendorfer H. The plasma membrane H+-V-ATPase from tobacco hornworm midgut. J. Bioenerg. Biomembr. 31 (1999) 67-74
42. Wieczorek H., Grber G., Harvey W., Huss M., Merzendorfer H., and Zeiske W. Structure and regulation of insect plasma membrane H(+)V-ATPase. J. Exp. Biol. 203 (2000) 127-135
43. Wolfersberger M.G., Luthy P., Maurer A., Parenti P., Sacchi V.F., Giordana B., and Hanozet G.M. Preparation and partial characterization of amino acid transporting brush border membrane vesicles from the larval midgut of the cabbage butterfly (Pieris brassicae). Comp. Biochem. Physiol. 86A (1987) 301-308
44. Woods D.F., Wu J.W., and Bryant P.J. Localization of proteins to the apico-lateral junctions of Drosophila epithelia. Dev. Genet. 20 (1997) 111-118
45. Xie R., Zhuang M., Ross L.S., Gomez I., Oltean D.I., Bravo A., Soberon M., and Gill S.S. Single amino acid mutations in the cadherin receptor from Heliothis virescens affect its toxin binding ability to Cry1A toxins. J. Biol. Chem. 280 (2005) 8416-8425
46. Zhang X., Candas M., Griko N.B., Rose-Young L., and Bulla L.A. Cytotoxicity of Bacillus thuringiensis Cry1Ab toxin depends on specific binding of the toxin to the cadherin receptor BT-R(1) expressed in insect cells. Cell Death Differ 12 (2005) 1407-1416
47. Zhang X., Candas M., Griko N.B., Taussig R., and Bulla Jr. L.A. A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proc. Natl. Acad. Sci. USA 103 (2006) 9897-9902
48. Zhuang M., Oltean D.I., Gomez I., Pullikuth A.K., Soberon M., Bravo A., and Gill S.S. Heliothis virescens and Manduca sexta lipid rafts are involved in Cry1A toxin binding to the midgut epithelium and subsequent pore formation. J. Biol. Chem. 277 (2002) 13863-13872