A 106-kDa aminopeptidase is a putative receptor for Bacillus thuringiensis Cry11Ba toxin in the mosquito Anopheles gambiae

Biochemistry

Volumn 47, Issue 43, 2008, Pages 11263-11272

  Zhang, Rui ^a   Hua, Gang ^a   Andacht, Tracy M ^c   Adang, Michael J ^a,b  

^a UNIVERSITY OF GEORGIA   (United States)

^b NONE   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLUS THURINGIENSIS; BINDING ASSAYS; BINDING MOTIFS; BRUSH BORDER MEMBRANE VESICLES; DOT BLOTTED; EPITHELIAL CELLS; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORS; IMMUNOHISTOCHEMISTRY; INSECT MORTALITIES; MICROTITER PLATES; MICROVILLI; PHOSPHATIDYLINOSITOL; PHOSPHOLIPASE C; SPECIFIC BINDINGS; SURFACE PLASMONS;

AMINES; BACTERIOLOGY; CELL MEMBRANES; ESCHERICHIA COLI; FORECASTING; SURFACE PLASMON RESONANCE; ZINC;

BINDING SITES;

AMINOPEPTIDASE; BACTERIAL TOXIN; COMPLEMENTARY DNA; CRY11BA TOXIN; GLYCOSYLPHOSPHATIDYLINOSITOL; IODINE 125; MICROSOMAL AMINOPEPTIDASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE PHOSPHODIESTERASE; UNCLASSIFIED DRUG; ZINC BINDING PROTEIN;

ANOPHELES GAMBIAE; ARTICLE; BACILLUS THURINGIENSIS; BINDING SITE; BRUSH BORDER; CONTROLLED STUDY; DOT HYBRIDIZATION; GLYCOSYLATION; IMMUNOHISTOCHEMISTRY; MEMBRANE VESICLE; MICROVILLUS; MOLECULAR CLONING; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN LOCALIZATION; SURFACE PLASMON RESONANCE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; ANOPHELES GAMBIAE; ANTIGENS, CD13; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; ENDOTOXINS; HEMOLYSIN PROTEINS; INSECTICIDES; LARVA; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; PHYLOGENY; RECOMBINANT PROTEINS;

ANOPHELES GAMBIAE; ANOPHELES QUADRIMACULATUS; BACILLUS THURINGIENSIS; ESCHERICHIA COLI; HEXAPODA;

EID: 54849424737     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801181g     Document Type: Article

References (40)

1. Walker, K., and Lynch, M. (2007) Contributions of Anopheles larval control to malaria suppression in tropical Africa: review of achievements and potential. Med. Vet. Entomol. 21, 2-21.
2. Federici, B. A., Park, H. W., Bideshi, D. K., Wirth, M. C., Johnson, J. J., Sakano, Y., and Tang, M. (2007) Developing recombinant bacteria for control of mosquito larvae. J. Am. Mosq. Control Assoc. 23, 164-175.
3. Pigott, C. R., and Ellar, D. J. (2007) Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol. Mol. Biol. Rev. 71, 255-281.
4. Bravo, A., Gomez, I., Conde, J., Munoz-Garay, C., Sanchez, J., Miranda, R., Zhuang, M., Gill, S. S., and Soberon, M. (2004) 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, 38-46.
5. Ravoahangimalala, O., and Charles, J. F. (1995) In vitro binding of Bacillus thuringiensis var. israelensis individual toxins to midgut cells of Anopheles gambiae larvae (Diptera: Culicidae). FEBS Lett. 362, 111-115.
6. Yamagiwa, M., Kamauchi, S., Okegawa, T., Esaki, M., Otake, K., Amachi, T., Komano, T., and Sakai, H. (2001) Binding properties of Bacillus thuringiensis Cry4A toxin to the apical microvilli of larval midgut of Culex pipiens. Biosci., Biotechnol., Biochem. 65, 2419-2427.
7. Kamauchi, S., Yamagiwa, M., Esaki, M., Otake, K., and Sakai, H. (2003) Binding properties of Bacillus thuringiensis Cry1C delta-endotoxin to the midgut epithelial membranes of Culex pipiens. Biosci., Biotechnol., Biochem. 67, 94-99.
8. Clark, T. M., Hutchinson, M. J., Huegel, K. L., Moffett, S. B., and Moffett, D. F. (2005) Additional morphological and physiological heterogeneity within the midgut of larval Aedes aegypti (Diptera: Culicidae) revealed by histology, electrophysiology, and effects of Bacillus thuringiensis endotoxin. Tissue Cell 37, 457-468.
9. Buzdin, A. A., Revina, L. P., Kostina, L. I., Zalunin, I. A., and Chestukhina, G. G. (2002) Interaction of 65- and 62-kD proteins from the apical membranes of the Aedes aegypti larvae midgut epithelium with Cry4B and Cry11A endotoxins of Bacillus thuringiensis. Biochemistry (Moscow) 67, 540-546.
10. Fernandez, L. E., Aimanova, K. G., Gill, S. S., Bravo, A., and Soberon, M. (2006) A GPI-anchored alkaline phosphatase is a functional midgut receptor of Cry11Aa toxin in Aedes aegypti larvae. Biochem. J. 394, 77-84.
11. Hua, G., Zhang, R., Abdullah, M. A., and Adang, M. J. (2008) Anopheles gambiae cadherin AgCad1 binds the Cry4Ba toxin of Bacillus thuringiensis israelensis and a fragment of AgCad1 synergizes toxicity. Biochemistry 47, 5101-5110.
12. Abdullah, M. A., Valaitis, A. P., and Dean, D. H. (2006) Identification of a Bacillus thuringiensis Cry11Ba toxin-binding aminopeptidase from the mosquito Anopheles quadrimaculatus. BMC Biochem. 7, 16.
13. Delecluse, A., Rosso, M. L., and Ragni, A. (1995) Cloning and expression of a novel toxin gene from Bacillus thuringiensis subsp. jegathesan encoding a highly mosquitocidal protein. Appl. Environ. Microbiol. 61, 4230-4235.
14. Schaeffer, P., Millet, J., and Aubert, J. P. (1965) Catabolic repression of bacterial sporulation. Proc. Natl. Acad. Sci. U.S.A. 54, 704-711.
15. Eisenhaber, B., Bork, P., and Eisenhaber, F. (1998) Sequence properties of GPI-anchored proteins near the omega-site: constraints for the polypeptide binding site of the putative transamidase. Protein Eng. 11, 1155-1161.
16. Eisenhaber, B., Bork, P., and Eisenhaber, F. (1999) Prediction of potential GPI-modification sites in proprotein sequences. J. Mol. Biol. 292, 741-758.
17. Sunyaev, S. R., Eisenhaber, F., Rodchenkov, I. V., Eisenhaber, B., Tumanyan, V. G., and Kuznetsov, E. N. (1999) PSIC: profile extraction from sequence alignments with position-specific counts of independent observations. Protein Eng. 12, 387-394.
18. Eisenhaber, B., Bork, P., Yuan, Y., Loffler, G., and Eisenhaber, F. (2000) Automated annotation of GPI anchor sites: case study C. elegans. Trends Biochem. Sci. 25, 340-341.
19. Harlow, E., and Lane, D. (1988) Storing and purifying antibodies, in Antibodies: A Laboratory Manual, 1st ed., p 310, Cold Spring Harbor Laboratory Press, New York.
20. Bradford, M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
21. Silva-Filha, M. H., Nielsen-Leroux, C., and Charles, J.-F. (1997) Binding kinetics of Bacillus sphaericus binary toxin to midgut brush-border membranes of Anopheles and Culex sp. mosquito larvae. Eur. J. Biochem. 247, 754-761.
22. Garczynski, S. F., and Adang, M. J. (1995) Bacillus thuringiensis CryIA(c) δ-endotoxin binding aminopeptidase in the Manduca sexta midgut has a glycosyl-phosphatidylinositol anchor. Insect Biochem. Mol. Biol. 25, 409-415.
23. He, N., Botelho, J. M. C., McNall, R. J., Belozerov, V., Dunn, W. A., Mize, T., Orlando, R., and Willis, J. H. (2007) Proteomic analysis of cast cuticles from Anopheles gambiae by tandem mass spectrometry. Insect Biochem. Mol. Biol. 37, 135-146.
24. Chen, J., Brown, M. R., Hua, G., and Adang, M. J. (2005) Comparison of the localization of Bacillus thuringiensis Cry1A delta-endotoxins and their binding proteins in larval midgut of tobacco hornworm Manduca sexta. Cell Tissue Res. 321, 123-129.
25. Garczynski, S. F., Crim, J. W., and Adang, M. J. (1991) Identification of putative insect brush border membrane-binding molecules specific to Bacillus thuringiensis delta-endotoxin by protein blot analysis. Appl. Environ. Microbiol. 57, 2816-2820.
26. Braitbard, O., Glickstein, H., Bishara-Shieban, J., Pace, U., and Stein, W. D. (2006) Competition between bound and free peptides in an ELISA-based procedure that assays peptides derived from protein digests. Proteome Sci. 4, 12.
27. Dinglasan, R. R., Kalume, D. E., Kanzok, S. M., Ghosh, A. K., Muratova, O., Pandey, A., and Jacobs-Lorena, M. (2007) Disruption of Plasmodium falciparum development by antibodies against a conserved mosquito midgut antigen. Proc. Natl. Acad. Sci. U.S.A. 104, 13461-13466.
28. Kozak, M. (1987) An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res. 15, 8125-8148.
29. Laustsen, P. G., Rasmussen, T. E., Petersen, K., Pedraza-Diaz, S., Moestrup, S. K., Gliemann, J., Sottrup-Jensen, L., and Kristensen, T. (1997) The complete amino acid sequence of human placental oxytocinase. Biochim. Biophys. Acta 1352, 1-7.
30. Hooper, N. M. (1994) Families of zinc metalloproteases. FEBS Lett. 354, 1-6.
31. Takesue, S., Yokota, K., Miyajima, s., Taguchi, R., and Ikezawa, H., and Takesue, Y. (1992) Partial release of aminopeptidase N from larval midgut cell membranes of the silkworm, Bombyx mori, by phosphatidylinositol-specific phospholipase C. Comp. Biochem. Physiol. 102B, 7-11.
32. Nakanishi, K., Yaoi, K., Nagino, Y., Hara, H., Kitami, M., Atsumi, S., Miura, N., and Sato, R. (2002) Aminopeptidase N isoforms from the midgut of Bombyx mori and Plutella xylostella - their classification and the factors that determine their binding specificity to Bacillus thuringiensis Cry1A toxin. FEBS Lett. 519, 215-220.
33. Herrero, S., Gechev, T., Bakker, P. L., Moar, W. J., and de Maagd, R. A. (2005) Bacillus thuringiensis Cry1Ca-resistant Spodoptera exigua lacks expression of one of four aminopeptiase N genes. BMC Genomics 6, 96.
34. Wang, P., Zhang, X., and Zhang, J. (2005) Molecular characterization of four midgut aminopeptidase N isozymes from the cabbage looper Trichoplusia ni. Insect Biochem. Mol. Biol. 6, 611-620.
35. Angelucci, C., Barrett-Wilt, G. A., Hunt, D. F., Akhurst, R. J., East, P. D., Gordon, K. H. J., and Campbell, P. M. (2008) Diversity of aminopeptidases, derived from four lepidopteran gene duplications, and polycalins expressed in the midgut of Helicoverpa armigera: Identification of proteins binding the δ-endotoxin, Cry1Ac of Bacillus thuringiensis. Insect Biochem. Mol. Biol. 38, 685-696.
36. Adang, M. J. (2004) Insect aminopeptidase N, in Handbook of Proteolytic Enzymes (Barrett, A. J., Rawlings, N. D., and Woessner, J. F., Eds.) 2nd ed., Elsevier, Amsterdam.
37. Volkmann, A., and Peters, W. (1989) Investigations on the midgut caeca of mosquito larvae - I. Fine structure. Tissue Cell 21, 243-251.
38. Volkmann, A., and Peters, W. (1989) Investigations on the midgut caeca of mosquito larvae - II. Functional aspects. Tissue Cell 21, 253-261.
39. Neira Oviedo, M., Vanekeris, L., Corena-McLeod, M. D., and Linser, P. J. (2008) A microarray-based analysis of transcriptional compartmentalization in the alimentary canal of Anopheles gambiae (Diptera: Culicidae) larvae. Insect Mol. Biol. 17, 61-72.
40. Boudko, D. Y., Moroz, L. L., Linser, P. J., Trimarchi, J. R., Smith, P. J., and Harvey, W. R. (2001) In situ analysis of pH gradients in mosquito larvae using non-invasive, self-referencing, pH-sensitive microelectrodes. J. Exp. Biol. 204, 691-699.