Analysis of glycan structures on the 120 kDa aminopeptidase N of Manduca sexta and their interactions with Bacillus thuringiensis Cry1Ac toxin

Insect Biochemistry and Molecular Biology

Volumn 34, Issue 1, 2004, Pages 101-112

  Knight, Peter J K ^a   Carroll, Joe ^b   Ellar, David J ^c  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Aminopeptidase N; Bacillus thuringiensis; Cry1Ac; Deglycosylation; Insect glycosylation; Receptor

Indexed keywords

BACILLUS THURINGIENSIS; INSECTA; MANDUCA SEXTA;

EID: 0742288367     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2003.09.007     Document Type: Article

References (71)

1. Altmann F., Fabini G., Ahorn H., Wilson I.B. Genetic model organisms in the study of N-glycans. Biochimie. 83:2001;703-712.
2. Altmann F., Schweiszer S., Weber C. Kinetic comparison of peptide: N-glycosidases F and A reveals several differences in substrate specificity. Glycoconj. J. 12:1995a;84-93.
3. Altmann F., Schwihla H., Staudacher E., Glossl J., Marz L. Insect cells contain an unusual, membrane-bound beta-N-acetylglucosaminidase probably involved in the processing of protein N-glycans. J. Biol. Chem. 270:1995b;17344-17349.
4. Altmann F., Staudacher E., Wilson I.B., Marz L. Insect cells as hosts for the expression of recombinant glycoproteins. Glycoconj. J. 16:1999;109-123.
5. Bobbitt J.M. Periodate oxidation of carbohydrates. Adv. Carbohydr. Chem. 11:1956;1-41.
6. Burton S.L., Ellar D.J., Li J., Derbyshire D.J. N-acetylgalactosamine on the putative insect receptor aminopeptidase N is recognised by a site on the domain III lectin-like fold of a Bacillus thuringiensis insecticidal toxin. J. Mol. Biol. 287:1999;1011-1022.
7. Carroll J., Wolfersberger M.G., Ellar D.J. The Bacillus thuringiensis Cry1Ac toxin-induced permeability change in Manduca sexta midgut brush border membrane vesicles proceeds by more than one mechanism. J. Cell Sci. 110:1997;3099-3104.
8. Chu F.K. Requirements for the cleavage of high mannose oligosaccharides in glycoproteins by peptide-N-glycosidase F. J. Biol. Chem. 261:1986;172-177.
9. Cooper M.A., Carroll J., Travis E.R., Williams D.H., Ellar D.J. Bacillus thuringiensis Cry1Ac toxin interaction with Manduca sexta aminopeptidase N in a model membrane environment. Biochem. J. 333:1998;677-683.
10. Crickmore N., Zeigler D.R., Feitelson J., Schnepf E., Van Rie J., Lereclus D., Baum J., Dean D.H. Revision of the nomenclature for the Bacillus thuringiensis pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62:1998;807-813.
11. Crickmore, N., Zeigler, D.R., Schnepf, E., Van Rie, J., Lereclus, D., Baum, J., Bravo, A., Dean, D.H., 2002. Bacillus thuringiensis toxin nomenclature. Available from http://www.biols.susx.ac.uk/Home/Neil_Crickmore/ Bt/index.html.
12. Cross G.A.M. Glycolipid anchoring of plasma membrane proteins. Ann. Rev. Cell Biol. 6:1990;1-39.
13. Crowley J.F., Goldstein I.J. Datura stramonium lectin. Methods Enzymol. 83:1982;368-373.
14. Denolf P., Hendrickx K., Van Damme J., Jansens S., Peferoen M., Degheele D., Van Rie J. Cloning and characterization of Manduca sexta and Plutella xylostella midgut aminopeptidase N enzymes related to Bacillus thuringiensis toxin-binding proteins. Eur. J. Biochem. 248:1997;748-761.
15. Faye L., Gomord V., Fitchette-Laine A.C., Chrispeels M.J. Affinity purification of antibodies specific for Asn-linked glycans containing alpha 1→3 fucose or beta 1→2 xylose. Anal. Biochem. 209:1993;104-108.
16. Francis B.R., Bulla L.A. Jr. Further characterization of BT-R1, the cadherin-like receptor for Cry1Ab toxin in tobacco hornworm (Manduca sexta) midguts. Insect Biochem. Mol. Biol. 27:1997;541-550.
17. Garczynski S.F., Adang M.J. Bacillus thuringiensis CryIA(c) δ-endotoxin binding aminopeptidase in the Manduca sexta midgut has a glycosyl-phosphatidylinositol anchor. Insect Biochem. Mol. Biol. 25:1995;409-415.
18. Garczynski S.F., Crim J.W., Adang M.J. Identification of putative insect brush border membrane-binding molecules specific to Bacillus thuringiensis δ-endotoxin by protein blot analysis. Appl. Environ. Microbiol. 57:1991;2816-2820.
19. Gerken T.A., Gupta R., Jentoft N. A novel approach for chemically deglycosylating O-linked glycoproteins. The deglycosylation of submaxilliary and respiratory mucins. Biochemistry. 31:1992;639-648.
20. Gill M., Ellar D. Transgenic Drosophila reveals a functional in vivo receptor for the Bacillus thuringiensis toxin Cry1Ac. Insect Mol. Biol. 11:2002;619-625.
21. Gill S.S., Cowles E.A., 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.
22. Gomez I., Oltean D.I., Gill S.S., Bravo A., Soberon M. Mapping the epitope in cadherin-like receptors involved in Bacillus thuringiensis Cry1A toxin interaction using phage display. J. Biol. Chem. 276:2001;28906-28912.
23. Grochulski P., Masson L., Borisova S., Pusztai-Carey M., Schwartz J.L., Brousseau R., Cygler M. Bacillus thuringiensis CryIA(a) insecticidal toxin: crystal structure and channel formation. J. Mol. Biol. 254:1995;447-464.
24. Hansen J.E., Lund O., Tolstrup N., Gooley A.A., Williams K.L., Brunak S. NetOglyc: prediction of mucin type O-glycosylation sites based on sequence context and surface accessibility. Glycoconj. J. 15:1998;115-130.
25. Hawkes R., Niday E., Gordon J. A dot-immunoblotting assay for monoclonal and other antibodies. Anal. Biochem. 119:1982;142-147.
26. Hester G., Wright C.S. The mannose-specific bulb lectin from Galanthus nivalis (snowdrop) binds mono- and dimannosides at distinct sites. Structure analysis of refined complexes at 2.3 A and 3.0 A resolution. J. Mol. Biol. 262:1996;516-531.
27. Iwai T., Inaba N., Naundorf A., Zhang Y., Gotoh M., Iwasaki H., Kudo T., Togayachi A., Ishizuka Y., Nakanishi H., Narimatsu H. Molecular cloning and characterization of a novel UDP-GlcNAc:GalNAc-peptide beta1,3-N- acetylglucosaminyltransferase (beta 3Gn-T6), an enzyme synthesizing the core 3 structure of O-glycans. J. Biol. Chem. 277:2002;12802-12809.
28. Johnson P.E., Joshi M.D., Tomme P., Kilburn D.G., McIntosh L.P. Structure of the N-terminal cellulose-binding domain of Cellulomonas fimi CenC determined by nuclear magnetic resonance spectroscopy. Biochemistry. 35:1996;14381-14394.
29. Knight P.J., Crickmore N., Ellar D.J. The receptor for Bacillus thuringiensis CrylA(c) delta-endotoxin in the brush border membrane of the lepidopteran Manduca sexta is aminopeptidase N. Mol. Microbiol. 11:1994;429-436.
30. Knight P.J., Knowles B.H., Ellar D.J. Molecular cloning of an insect aminopeptidase N that serves as a receptor for Bacillus thuringiensis CryIA(c) toxin. J. Biol. Chem. 270:1995;17765-17770.
31. Knowles B.H., Knight P.J.K., Ellar D.J. N-acetyl galactosamine is part of the receptor in insect gut epithelia that recognises an insecticidal protein from Bacillus thuringiensis. Proc. Roy. Soc. Lond. B. 245:1991;31-35.
32. Knowles B.H., Thomas W.E., Ellar D.J. Lectin-like binding of Bacillus thuringiensis var. kurstaki lepidopteran-specific toxin is an initial step in insecticidal action. FEBS Lett. 168:1984;197-202.
33. Kurosaka A., Yano A., Itoh N., Kuroda Y., Nakagawa T., Kawasaki T. The structure of a neural specific carbohydrate epitope of horseradish peroxidase recognized by anti-horseradish peroxidase antiserum. J. Biol. Chem. 266:1991;4168-4172.
34. Lee M.K., You T.H., Young B.A., Cotrill J.A., Valaitis A.P., Dean D.H. Aminopeptidase N purified from gypsy moth brush border membrane vesicles is a specific receptor for Bacillus thuringiensis CryIAc toxin. Appl. Environ. Microbiol. 62:1996;2845-2849.
35. Lee X., Thompson A., Zhang Z., Ton-that H., Biesterfeldt J., Ogata C., Xu L., Johnston R.A., Young N.M. Structure of the complex of Maclura pomifera agglutinin and the T-antigen disaccharide, Galbeta1,3GalNAc. J. Biol. Chem. 273:1998;6312-6318.
36. Li J.D., Carroll J., Ellar D.J. Crystal structure of insecticidal delta-endotoxin from Bacillus thuringiensis at 2.5 A resolution. Nature. 353:1991;815-821.
37. Lopez M., Tetaert D., Juliant S., Gazon M., Cerutti M., Verbert A., Delannoy P. O-glycosylation potential of lepidopteran insect cell lines. Biochim. Biophys. Acta. 1427:1999;49-61.
38. Lu Y., Adang M.J. Conversion of Bacillus thuringiensis CryIAc-binding aminopeptidase to a soluble form by endogenous phosphatidylinositol phospholipase C. Insect Biochem. Mol. Biol. 226:1996;33-40.
39. Luo K., Sangadala S., Masson L., Mazza A., Brousseau R., Adang M.J. The Heliothis virescens 170 kDa aminopeptidase functions as "receptorA" by mediating specific Bacillus thuringiensis Cry1A delta-endotoxin binding and pore formation. Insect Biochem. Mol. Biol. 27:1997;735-743.
40. Maley F., Trimble R.B., Tarentino A.L., Plummer T.H. Characterisation of glycoproteins and their associated oligosaccharides through the use of endoglycosidases. Anal. Biochem. 180:1989.
41. Marz L., Altmann F., Staudacher E., Kubelka V. Protein glycosylation in insects. Montreuil J., Schachter H., Vliegenthart J. Glycoproteins. 1995;543-563 Elsevier Science BV, Amsterdam.
42. McConville M.J., Menon A.K. Recent developments in the cell biology and biochemistry of glycosylphosphatidylinositol lipids (review). Mol. Membr. Biol. 17:2000;1-16.
43. Oddou P., Hartmann H., Geiser M. Identification and characterisation of Heliothis virescens midgut membrane proteins binding Bacillus thuringiensis δ-endotoxin. Eur. J. Biochem. 202:1991;673-680.
44. Oddou P., Hartmann H., Radecke F., Geiser M. Immunologically unrelated Heliothis sp. and Spodoptera sp. midgut membrane proteins bind Bacillus thuringiensis CryIA(b) δ-endotoxin. Eur. J. Biochem. 212:1993;145-150.
45. Osawa T., Tsuji T. Fractionation and structural assessment of oligosaccharides and glycopeptides by use of immobilized lectins. Ann. Rev. Biochem. 56:1987;21-42.
46. Rosa J.C., De Oliveira P.S., Garratt R., Beltramini L., Resing K., Roque-Barreira M.C., Greene L.J. KM+, a mannose-binding lectin from Artocarpus integrifolia: amino acid sequence, predicted tertiary structure, carbohydrate recognition, and analysis of the beta-prism fold. Protein Sci. 8:1999;13-24.
47. Sangadala S., Azadi P., Carlson R., Adang M.J. Carbohydrate analyses of Manduca sexta aminopeptidase N, co-purifying neutral lipids and their functional interactions with Bacillus thuringiensis Cry1Ac toxin. Insect Biochem. Mol. Biol. 32:2001;97-107.
48. + efflux in vitro. J. Biol. Chem. 269:1994;10088-10092.
49. Sankaranarayanan R., Sekar K., Banerjee R., Sharma V., Surolia A., Vijayan M. A novel mode of carbohydrate recognition in jacalin, a Moraceae plant lectin with a beta-prism fold. Nat. Struct. Biol. 3:1996;596-603.
50. Schnepf E., Crickmore N., Van Rie J., Lereclus D., Baum J., Feitelson J., Zeigler D.R., Dean D.H. Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol. Mol. Biol. Rev. 62:1998;775-806.
51. Shimizu T., Vassylyev D.G., Kido S., Doi Y., Morikawa K. Crystal structure of vitelline membrane outer layer protein 1 (VMO-1): a folding motif with homologous Greek key structures related by an internal three-fold symmetry. EMBO J. 13:1994;1003-1010.
52. Staudacher E., Altmann F., Marz L., Hard K., Kamerling J.P., Vliegenthart J.F. Alpha 1-6(alpha 1-3)-difucosylation of the asparagine-bound N-acetylglucosamine in honeybee venom phospholipase A2. Glycoconj. J. 9:1992;82-85.
53. Staudacher E., Dalik T., Wawra P., Altmann F., Marz L. Functional purification and characterization of a GDP-fucose: beta-N-acetylglucosamine (Fuc to Asn linked GlcNAc) alpha 1,3-fucosyltransferase from mung beans. Glycoconj. J. 12:1995;780-786.
54. Staudacher E., Kubelka V., Marz L. Distinct N-glycan fucosylation potentials of three lepidopteran cell lines. Eur. J. Biochem. 207:1992;987-993.
55. Staudacher E., Marz L. Strict order of (Fuc to Asn-linked GlcNAc) fucosyltransferases forming core-difucosylated structures. Glycoconj. J. 15:1998;355-360.
56. Stewart G.S.A.B., Johnstone K., Hagelberg E., Ellar D.J. Commitment of bacterial spores to germinate. A measure of the trigger reaction. Biochem. J. 196:1981;101-106.
57. Sueyoshi S., Tsuji T., Osawa T. Carbohydrate-binding specificities of five lectins that bind to O-glycosyl-linked carbohydrate chains. Quantitative analysis by frontal-affinity chromatography. Carbohydr. Res. 178:1988;214-224.
58. Swords K.M.M., Staehelin L.A. Complementary immunolocalisation patterns of cell wall hydroxyproline-rich glycoproteins studied with the use of antibodies directed against different carbohydrate epitopes. Plant Physiol. 102:1993;891-901.
59. Thomas W.E., Ellar D.J. Bacillus thuringiensis var. israelensis crystal δ-endotoxin: effects on insect and mammalian cells in vitro and in vivo. J. Cell Sci. 60:1983;181-197.
60. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from acrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. 76:1979;4350-4354.
61. Tsuda Y., Nakatani F., Hashimoto K., Ikawa S., Matsuura C., Fukada T., Sugimoto K., Himeno M. Cytotoxic activity of Bacillus thuringiensis Cry proteins on mammalian cells transfected with cadherin-like Cry receptor gene of Bombyx mori (silkworm). Biochem. J. 369:2003;697-703.
62. Umemoto J., Bhavanandan V.P., Davidson E.A. Purification and properties of a endo-a-N-acetyl-D-galactosaminidase from Diplococcus pneumoniae. J. Biol. Chem. 252:1977;8609-8614.
63. Vadlamudi R.K., Weber E., Ji I., Ji T.H., Bulla L.A. Cloning and expression of a receptor for an insecticidal toxin of Bacillus thuringiensis. J. Biol. Chem. 270:1995;5490-5494.
64. Valaitis A.P., Lee M.K., Rajamohan F., Dean D.H. Brush border membrane aminopeptidase-N in the midgut of the gypsy moth serves as the receptor for the CryIA(c) delta-endotoxin of Bacillus thuringiensis. Insect Biochem. Mol. Biol. 25:1995;1143-1151.
65. Wagner R., Geyer H., Geyer R., Klenk H.D. N-acetyl-beta-glucosaminidase accounts for differences in glycosylation of influenza virus hemagglutinin expressed in insect cells from a baculovirus vector. J. Virol. 70:1996;4103-4109.
66. Wolfersberger M.G. Preparation and partial characterization of amino-acid transporting brush-border membrane-vesicles from the larval midgut of the gypsy-moth (Lymantria-Dispar). Arch. Insect Biochem. Physiol. 24:1993;139-147.
67. Wolfersberger M.G., Lüthy P., Maurer A., Parenti P., Sacchi F.V., Giordana B., Hanozet G.M. Preparation and partial characterisation 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.
68. Woodward M.P., Young W.W., Bloodgood R.A. Detection of monoclonal antibodies specific for carbohydrate epitopes using periodate oxidation. J. Immunol. Meth. 78:1985;143-153.
69. Yamashita K., Kochibe N., Ohkura T., Ueda I., Kobata A. Fractionation of L-fucose-containing ologosaccharides on immobolized Aleuria aurantia lectin. J. Biol. Chem. 260:1985;4688-4693.
70. Yamashita K., Totani K., Ohkura T., Takasaki S., Goldstein I.J., Kobata A. Carbohydrate binding properties of complex-type oligosaccharides on immobilized Datura stramonium lectin. J. Biol. Chem. 262:1987;1602-1607.
71. Yaoi K., Kadotani T., Kuwana H., Shinkawa A., Takahashi T., Iwahana H., Sato R. Aminopeptidase N from Bombyx mori as a candidate for the receptor of Bacillus thuringiensis Cry1Aa toxin. Eur. J. Biochem. 246:1997;652-657.