Cloning and characterization of Manduca sexta and Plutella xylostella midgut aminopeptidase N enzymes related to Bacillus thuringiensis toxin-binding proteins

European Journal of Biochemistry

Volumn 248, Issue 3, 1997, Pages 748-761

  Denolf, Peter ^a,b   Hendrickx, Koen ^c   Van Damme, José ^b   Jansens, Stefan ^a   Peferoen, Marnix ^a   Degheele, Danny ^b   Van Rie, Jeroen ^a  

^a Bayer Cropscience Belgium   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c Zöologisch Instituut   (Belgium)

Author keywords

Aminopeptidase N; Bacillus thuringiensis; Insecticidal crystal protein binding protein; Manduca sexta; Plutella xylostella

Indexed keywords

MICROSOMAL AMINOPEPTIDASE;

AFFINITY CHROMATOGRAPHY; AMINO ACID SEQUENCE; ANIMAL TISSUE; BACILLUS THURINGIENSIS; CONTROLLED STUDY; DNA LIBRARY; INFECTION SENSITIVITY; LEPIDOPTERA; MIDGUT; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; REVIEW; SEQUENCE HOMOLOGY;

ANIMALIA; BACILLUS THURINGIENSIS; COLEOPTERA; EUKARYOTA; INSECTA; LEPIDOPTERA; MANDUCA SEXTA; PLUTELLA XYLOSTELLA; PROKARYOTA;

EID: 0030767349     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1997.t01-1-00748.x     Document Type: Review

References (106)

1. Hofmann, C., Lüthy, P., Hütter, R. & Pliska, V. (1988) Binding of the δ-endotoxin from Bacillus thuringiensis to brush-border membrane vesicles of the cabbage butterfly (Pieris brassicae), Eur. J. Biochem. 173, 85-91.
2. Hofmann, C., Vanderbruggen, H., Höfte, H., Van Rie, J., Jansens, S. & Van Mellaert, H. (1988) Specificity of Bacillus thuringiensis δ-endotoxins is correlated with the presence of high-affinity binding sites in the brush-border membrane of target insect midguts, Proc. Natl Acad. Sci. USA 85, 7844-7848.
3. Van Rie, J., Jansens, S., Höfte, H., Degheele, D. & Van Meliaert, H. (1989) Specificity of Bacillus thuringiensis δ-endotoxins. Eur. J. Biochem. 186, 239-247.
4. Van Rie, J., Jansens, S., Höfte, H., Degheele, D. & Van Mellaert, H. (1990) Receptors on the brush-border membrane of the insect midgut as determinants of the specificity of Bacillus thuringiensis δ-endotoxins, Appl. Env. Microbiol. 56, 1378-1385.
5. Denolf, P., Jansens, S., Peferoen, M., Degheele, D. & Van Rie, J. (1993) Two different Bacillus thuringiensis δ-endotoxin receptors in the midgut brush-border membrane of the European corn borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Pyralidae), Appl. Env. Microbiol. 59, 1828-1837.
6. Escriche, B., Martinez-Ramirez, A. C., Real, M. D., Silva F. J. & Ferré J. (1994) Occurence of three different binding sites for Bacillus thuringiensis δ-endotoxins in the midgut brush-border membrane of the potato tuber moth Phthorimaea operculella (Zeller), Arch. Insect Biochem. Physiol. 26, 315-327.
7. Estada, U. & Ferré, J. (1994) Binding of insecticidal crystal proteins of Bacillus thuringiensis to the midgut brush-border of the cabbage looper. Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae), and selection for resistance to one of the crystal proteins, Appl. Env. Microbiol. 60, 3840-3846.
8. Sanchis, V. Chaufaux, J. & Pauron, D. (1994) A comparison and analysis of the toxicity and receptor binding properties of Bacillus thuringiensis CryIC δ-endotoxin on Spodoptera littoralis and Bombyx mori, FEBS Lett. 353, 259-263.
9. Tang, J. D., Shelton, A. M., Van Rie, J., De Roeck, S., Moar, W. J., Roush, R. T. & Peferoen, M. (1996) Toxicity of Bacillus thuringiensis spore and crystal protein to resistant diamondback moth (Plutella xylostella), Appl. Environm. Microbiol. 62, 564-569.
10. Lambert, B., Buysse, L., Decock, C., Jansens, S., Piens, C., Saey, B., Seurinck, J., Van Audenhove, K., Van Rie, J., Van Vliet, A. & Peferoen, M. (1996) A Bacillus thuringiensis insecticidal crystal protein with a high activity against members of the family Noctuidae, Appl. Env. Microbiol. 62, 80-86.
11. Knowles, B., Knight, P. & Ellar, D. (1991) N-acetyl galactosamine is part of the receptor in insect gut epithelia that recognizes an insecticidal protein from Bacillus thuringiensis, Proc. R. Soc. Lond. B 245, 31-35.
12. Garczynski, S., Crim, J. & Adang, M. (1991) Identification of putative insect brush-border membrane-binding molecules specific to Bacillus thuringiensis δ-endotoxin by protein blot analysis, Appl. Env. Microbiol. 57, 2816-2820.
13. Oddou, P., Hartmann, H. & Geiser, M. (1991) Identification and characterization of Heliothis virescens midgut membrane proteins binding Bacillus thuringiensis δ-endotoxins, Eur. J. Biochem. 202, 673-680.
14. Indrasith, L. & Hori, H. (1992) Isolation and partial characterization of binding proteins for immobilized delta endotoxin from solubilized brush-border membrane vesicles of the silkworm, Bombyx mori, and the common cutworm, Spodoptera litura, Comp. Biochem. Physiol. 102B, 605-610.
15. Oddou, P., Hartmann, H. & Geiser, M. (1993) Immunologically unrelated Heliothis sp. and Spodoptera sp. midgut membrane-proteins bind Bacillus thuringiensis CryIA(b) δ-endotoxin, Eur. J. Biochem. 212, 145-150.
16. Sanchis, V. & Ellar, D. (1993) Identification and partial purification of a Bacillus thuringiensis CryIC δ-endotoxin binding protein from Spodoptera littoralis gut membranes, FEBS Lett. 316, 264-268.
17. Vadlamudi, R., Ji, T. & Bulla, L. (1993) A specific binding protein from Manduca sexta for the insecticidal toxin of Bacillus thuringiensis subsp. berliner, J. Biol. Chem. 268, 12334-12340.
18. Feldman, F., Dullemans, A. & Waalwijk, C. (1995) Binding of the CryIVD toxin of Bacillus thuringiensis subsp. to larval dipteran midgut proteins, Appl. Env. Microbiol. 61, 2601-2605.
19. Cowles, E., Yunovitz, H., Charles, J.-F. & Gill, S. (1995) Comparison of toxin overlay and solid-phase binding assays to identify diverse CryIA(c) toxin-binding proteins in Heliothis virescens midgut, Appl. Env. Microbiol. 61, 2738-2744.
20. Bravo, A., Hendrickx, K., Jansens, S. & Peferoen, M. (1992) Immunohistochemical analysis of specific binding of Bacillus thuringiensis insecticidal crystal proteins to lepidopteran and coleopteran midgut membranes, J. Invertebr. Pathol. 60, 247-253.
21. Denolf, P., Jansens, S., Van Houdt, S., Peferoen, M., Degheele, D. & Van Rie, J. (1993) Biotinylation of Bacillus thuringiensis insecticidal crystal proteins, Appl. Env. Microbiol. 59, 1821-1827.
22. Ravoahangimalala, O. & Charles, J.-F. (1995) In vitro binding of Bacillus thuringiensis var. individual toxins to midgut cells of Anopheles gambiae larvae (Diptera: Culicidae), FEBS Lett. 362, 111-115.
23. Masson, L., Mazza, A. & Brousseau, R. (1994) Stable immobilization of lipid vesicles for kinetic studies using surface plasmon resonance, Anal. Biochem. 218, 405-412.
24. Masson, L., Mazza, A., Brousseau, R. & Tabashnik, B. (1995) Kinetics of Bacillus thuringiensis toxin binding with brush-border membrane vesicles from susceptible and resistant larvae of Plutella xylostella, J. Biol. Chem. 270, 11887-11896.
25. Masson, L., Lu, Y.-J., Mazza, A., Brousseau, R. & Adang, M. (1995) The CryIA(c) receptor purified from Manduca sexta displays multiple specificities, J. Biol. Chem. 270, 20309-20315.
26. Roush, R. (1994) Managing pests and their resistance to Bacillus thuringiensis: can transgenic crops be better than sprays? Biocontrol Sci. Technol. 4, 501-516.
27. Wolfersberger, M., Hofmann, C. & Lüthy, P. (1986) Interaction of Bacillus thuringiensis δ-endotoxin with membrane vesicles isolated from lepidopteran larval midgut, in Bacterial Protein Toxins (Falmagne, P., Alouf, J., Fehrenbach, F., Jeljaszewicz, J. & Thelestam, M., eds) pp. 237-238. Gustav Fisher Verlag, Stuttgart, Germany.
28. Ihara, H., Kuroda, E., Wadano, A. & Himeno, M. (1993) Specific toxicity of δ-endotoxins from Bacillus thuringiensis to Bombyx mori. Biosci. Biotechnol. Biochem. 57, 200-204.
29. Liang, Y., Patel, S. & Dean, D. (1995) Irreversible binding kinetics of Bacillus thuringiensis CryIA δ-endotoxins to Gypsy moth brush-border membrane vesicles is directly correlated to toxicity, J. Biol. Chem. 270, 24719-24724.
30. Schnepf, H., Tomczak, K., Ortega, J. & Whiteley, H. (1990) Specificity-determining regions of a lepidopteran-specific insecticidal protein produced by Bacillus thuringiensis, J. Biol. Chem. 265, 20923-20930.
31. Honée, G., Convents, D., Van Rie, J., Jansens, S., Peferoen, M. & Visser, B. (1991) The C-terminal domain of the toxic fragment of a Bacillus thuringiensis crystal protein determines receptor binding, Mol. Microbiol. 5, 2799-2806.
32. Ge, A., Rivers, D., Milne, R. & Dean, D. (1991) Functional domains of Bacillus thuringiensis insecticidal crystal proteins, J. Biol. Chem. 266, 17954-17958.
33. Lee, M., Milne, R., Ge, A. & Dean, D. (1992) Location of a Bombyx mori receptor binding region on a Bacillus thuringiensis δ-endotoxin. J. Biol. Chem. 267, 3115-3121.
34. Wu, D. & Aronson, A. (1992) Localized mutagenesis defines regions of the Bacillus thuringienxis δ-endotoxin involved in toxicity and specificity, J. Biol. Chem. 267, 2311-2317.
35. Cuminings, C. & Ellar, D. (1994) Chemical modification of Bacillus thuringiensis activated δ-endotoxin and its effect on toxicity and binding to Manduca sexta midgut membranes, Microbiology, 140, 2737-2747.
36. Lu, H., Rajamohan, F. & Dean, D. (1994) Identification of amino acid residues of Bacillus thuringiensis δ-endotoxin CryIAa associated with membrane binding and toxicity to Bombyx mori, J. Bacteriol. 176, 5554-5559.
37. Rajamohan, F., Alcantara, E., Lee, M., Chen, X., Curtiss, A. & Dean, D. (1995) Single amino acid changes in domain II of Bacillus thuringiensis CryIAb δ-endotoxin affect irreversible binding to Manduca sexta midgut membrane vesicles, J. Bacteriol. 177, 2276-2282.
38. Aronson, A., Wu, D. & Zhang, C. (1995) Mutagenesis of specificity and toxicity regions of a Bacillus thuringiensis protoxin gene, J. Bacteriol. 177, 4059-4065.
39. De Maagd, R., Kwa, M., Van der Klei, H., Yamamoto, T., Schipper, B., Vlak, J., Stiekema, W. & Bosch, D. (1996) Domain III substitution in Bacillus thuringiensis δ-endotoxin CryIA(b) results in superior toxicity for Spodoptera exigua and altered membrane protein recognition, Appl. Env. Microbiol. 62, 1537-1543.
40. De Maagd, R., Van der Klei, H., Bakker, P. Stiekema, W. & Bosch, D. (1996) Different domains of Bacillus thuringiensis δ-endotoxins can bind to insect midgut membrane proteins on ligand blots, Appl. Env. Microbiol. 62, 2753-2757.
41. Gazit, E. & Shai, Y. (1993) Structural and functional characterization of the α5 segment of Bacillus thuringiensis δ-endotoxin, Biochemistry 32, 3429-3436.
42. Gazit, E., Bach, D., Kerr, I., Sansom, M., Chejanovski, N. & Shai, Y. (1994) The α5 segment of Bacillus thuringiensis δ-endotoxin: in vitro activity, ion channel formation and molecular modelling, Biochem. J. 304, 895-902.
43. Gazit, E. & Shai, Y. (1995) The assembly and organization of the α5 and α7 helices from the pore-forming domain of Bacillus thuringiensis δ-endotoxin, J. Biol. Chem. 270, 2571-2578.
44. Pang, A. (1993) Use of synthetic peptides to probe functional domains of a Bacillus thuringiensis toxin, J. Invertebr. Pathol. 61, 260-266.
45. Cummings, C., Armstrong, G., Hodgman, T. & Ellar, D. (1994) Structural und functional studies of a synthetic peptide mimicking a proposed membrane inserting region of a Bacillus thuringiensis δ-endotoxin, Mol. Membr. Biol. 11, 87-92.
46. Chen, X., Curtiss, A., Alcantara, E. & Dean, D. (1995) Mutations in domain I of Bacillus thuringiensis δ-endotoxin CryIAb reduce the irreversible binding of toxin to Manduca sexta brush-border membrane vesicles, J. Biol. Chem. 270, 6412-6419.
47. Wolfersberger, M. Chen, X. & Dean, D. (1996) Site-directed mutations in the third domain of Bacillus thuringiensis δ-endotoxin CryIAa affect its ability to increase the permeability of Bombyx mori midgut brush-border membrane vesicles, Appl. Env. Microbiol. 62, 279-282.
48. Vadlamudi, R., Weber, E., Ji, I., Ji, T. & Bulla, L. (1995) Cloning and expression of a receptor for an insecticidal toxin of Bacillus thuringiensis, J. Biol. Chem. 270, 5490-5494.
49. Knight, P., Crickmore, N. & Ellar, D. J. (1994) The receptor for Bacillus tthuringiensis CryIA(c) δ-endotoxin in the brush-border membrane of the lepidopteran Manduca sexta is aminopeptidase N, Mol. Microbiol. 11, 429-436.
50. + efflux in vitro. J. Biol. Chem. 269, 10088-10092.
51. Knight, P., Knowles, B. & Ellar, D. (1995) Molecular cloning of an insect aminopeptidase N that serves as a receptor for Bacillus thuringiensis CryIA(c) toxin. J. Biol. Chem. 270, 17765-17770.
52. Gill, S., Cowles, E. & Francis, V. (1995) 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, 27277-27282.
53. Valaitis, A., Lee, M.-K., Rajamohan, F. & Dean, D. (1995) Brush-border membrane aminopeptidase-N in the midgut of the gypsy moth serves as the receptor for the CryIA[c] δ-endotoxin of Bacillus thuringiensis, Insect Biochem. Molec. Biol. 25, 1143-1151.
54. Lee, M., You, T., Young, B., Cotrill, J., Valaitis, A. & Dean, D. (1996) Aminopeptidase N purified from gypsy moth brush-border membrane vesicles is a specific receptor for Bacillus thuringiensis CryIAc toxin, Appl. Env. Microbiol. 62, 2845-2849.
55. Luo, K., Lu, Y.-J. & Adang, M. (1996) A 106 kDa form of aminopeptidase is a receptor for Bacillus thuringiensis Cry1C δ-endotoxin in the brush-border membrane of Manduca sexta, Insect Biochem. Molec. Biol. 26, 783-791.
56. Höfte, H., De Greve, H., Scurinck, J., Jansens, S., Mahillon, J., Ampe, C., Vandekerckhove, J., Vanderhruggen, H., Van Montagu, M., Zabeau, M. & Vaeck, M. (1986) Structural and functional analysis of a cloned δ-endotoxin of Bacillus thuringiensis berliner 1715, Eur. J. Biochem. 161, 273-280.
57. Brizzard, B. & Whiteley, H. (1988) Nucleotide sequence of an additional crystal protein gene cloned from Bacillus thuringiensis subsp. thuringiensis, Nucleic Acids Res. 16, 4168-4169.
58. Kronstad, J. & Whiteley, H. (1986) Three classes of homologous Bacillus thuringiensis crystal protein genes, Gene 43, 29-40.
59. Hunter, W. & Greenwood, F. (1962) Preparation of iodine-131 labelled human growth hormone of high specific activity. Science 194, 495-496.
60. Fraker, P. & Speck, J. (1978) Protein and cell membrane iodinations with a sparingly soluble chloroamide, 1,3,4,6-tetrachloro-3a,6a-diphenylglycoluril. Biochem. Biophys. Res. Commun. 80, 849-857.
61. Wolfersberger, M., Lüithy, P., Maurer, A., Parenti, P., Sacchi, V., Giordana, B. & Hanozet, G. (1987) 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. 86, 301-308.
62. Bradford, M. 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.
63. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227, 680-685.
64. Towbin, H., Staehelin, T. & Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications, Proc. Natl Acad. Sci. USA, 76, 4350-4354.
65. Bauw, G., Van Damme, J., Puype, M., Vandekerckhove, J., Gesser, B., Ratz, G., Lauridsen, J. & Celis, J. (1989) Protein-electroblotting and -microsequencing strategies in generating protein data bases from two-dimensional gels. Proc. Natl Acad. Sci. USA 86, 7701-7705.
66. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
67. Beckers, T., Schmidt, P. & Hilgard, P. (1994) Highly sensitive northern hyhridization of rare mRNA using a positively charged nylon membrane. Biotechniques 16, 1075-1078.
68. 1A receptor in Sf9 cells, J. Biol. Chem. 270, 18691-18699.
69. Kunz, D., Bühling, F., Hütter, H.-J., Aoyagi, T. & Ansorge, S. (1993) Aminopeptidase N (CD13, EC 3.4.11.2) occurs on the surface of resting and concanavalin A-stimulated lymphocytes, Biol. Chem. Hoppe-Seyler 374, 291-296.
70. Watt, V. & Yip, C. (1989) Amino acid sequence deduced from a rat kidney cDNA suggests it encodes the Zn-peptidase aminopeptidase N, J. Biol. Chem. 264, 5480-5487.
71. Noren, O., Dabelsteen, E., Hoyer, P., Olsen, J., Sjöström, H. & Hansen, G. (1989) Onset of transcription of the aminopeptidase N (leukemia antigen CD 13) gene at the crypt/villus transition zone during rabbit enterocyte differentiation. FEBS Lett. 259, 107-112.
72. Olsen, J., Cowell, G., Konigshofer, E., Danielsen, E., Moller, J., Lausten, L., Hansen, O., Welinder, K., Engberg, J., Hunziker, W., Spiess, M., Sjöström, H. & Noren, O. (1988) Complete amino acid sequence of human intestinal aminopeptidase N as deduced from cloned cDNA, FEBS Lett. 238, 307-314.
73. Wu, Q., Lahti, J., Air, G., Burrows, P. & Cooper, M. (1990) Molecular cloning of the murine BP-1/6C3 antigen: a member of the zinc-dependent metallopeptidase family, Proc. Natl Acad. Sci. USA, 87, 993-997.
74. Kozak, M. (1987) An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs, Nucleic Acids Res. 15, 8125-8148.
75. Kyte, J. & Doolittle, R. (1982) A simple method for displaying the hydropathic character of a protein, J. Mol. Biol 157, 105-132.
76. von Heijne, G. (1986) A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 14, 4683-4690.
77. Fletcher, T., Alhadeff, M., Craik, C. & Largman, C. (1987) Isolation and characterization of a cDNA encoding rat cationic trypsinogen. Biochemistry 26, 3081-3086.
78. Levy, N., Malipiero, U., Lebecque, S. & Gearhart, P. (1989) Early onset of somatic mulation in immunoglobulin VH genes during the primary immune response, J. Exp. Med. 169, 2007-2019.
79. Kodukula, K., Gerber, L., Amthauer, R., Brink, L. & Udenfriend, S. (1993) Biosynthesis of glycosylphosphatidylinositol (glycosyl-PtdIns)-anchored membrane proteins in intact cells: specific amino acid requirements adjacent to the site of cleavage and glycosyl-PtdIns attachment. J. Cell Biol. 120, 657-664.
80. Jongeneel, C., Bouvier, J. & Bairoch, A. (1989) A unique signature identifies a family of zinc-dependent metallopeptidases. FEBS Lett. 242, 211-214.
81. Delmas, B., Gelfi, J., Kut, E., Sjöström, H., Noren, O. & Laude, H. (1994) Determinants essential for the transmissible gastroenteritis virus-receptor interaction reside within a domain of aminopeptidase-N that is distinct from the enzymatic site, J. Virol. 68, 5216-5224.
82. Nanus, D., Engelstein, D., Gastl, G., Gluck, L., Vidal, M., Morrison, M., Finstad, C., Bander, N. & Albino, A. (1993) Molecular cloning of the human kidney differentiation antigen gp160: human aminopeptidase A. Proc. Natl Acad. Sci. USA 90, 7069-7073.
83. Myers, E. & Miller, W. (1988) Optimal alignments in linear space. Comput. Appl. Biosci. 4, 11-17.
84. Hendrickx, K. (1992) On the mode of action of the Cry1Ab delta-endotoxin from the bacterium Bacillus thuringiensis in the midgut of Manduca sexta [Insecta: Lepidoptera], PhD thesis, Katholieke Universiteit Leuven, Belgium.
85. Martinez-Ramírez, A. C., Gonzales-Nebauer, S., Escriche, B. & Real, M. D. (1994) Ligand blot identification of a Manduca sexta midgut binding protein specific to three Bacillus thuringiensis Cry1A-type ICPs. Biochem. Biophys. Res. Commun. 201, 782-787.
86. Bosch, D., Visser, B. & Stiekema, W. (1994) Analysis of non-active engineered Bacillus thuringiensis crystal proteins, FEMS Microbiol. Lett. 118, 129-134.
87. Lee, M. & Dean, D. (1996) Inconcistencies in determining Bacillus thuringiensis toxin binding sites relationship by comparing competition assays with ligand blotting, Biochem. Biophys. Res. Commun. 220, 575-580.
88. Harris, E. & Angal, S. (1990) Protein purification applications: a practical approach. Oxford University Press, Oxford.
89. Semenza, G. (1986) Anchoring and biosynthesis of stalked brush-border membrane proteins: glycosidases and peptidases of enterocytes and renal tubuli. Annu. Rev. Cell. Biol. 2, 255-313.
90. Kirsch, K. & Schmutterer, H. (1988) Low efficacy of a Bacillus thuringiensis (Berl.) formulation in controlling the diamondback moth. Plutella xylostella (L.), in the Philippines, J. Appl. Ent. 105, 249-255.
91. Tabashnik, B., Cushing, N., Finson, N. & Johnson, M. (1990) Field development of resistance to Bacillus thuringiensis in diamondback moth [Lepidoptera: Plutellidae], J. Econ. Entomol. 83, 1671-1676.
92. Shelton, A., Robertson, J., Tang, J., Perez, C., Eigenbrode, S., Preisler, H., Wilsey, W. & Cooley, R. (1993) Resistance of diamondback moth to Bacillus thuringiensis subspecies in the field, J. Econ. Entomol. 86, 697-705.
93. Takesue, S., Yokota, K., Miyajima, S., Taguchi, R., Ikezawa, H. & 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.
94. Tomita, M., Obara, H., Takesue, Y., Tamura, H.-O., Miyajima, S., Taguchi, R. & Ikezawa, H. (1994) Purification of glycosylphosphatidylinositol-anchoring aminopeptidase N from the plasma membrane of larval midgut epithelial cells of the silkworm. Bombyx mori, Int. J. Biochem. 26, 977-986.
95. Udenfriend, S. & Kodukula, K. (1995) How glycosylphosphatidylinositol-anchored membrane proteins are made, Annu. Rev. Biochem. 64, 563-591.
96. Lee, M. & Anstee, J. (1995) Characterization of midgut exopeptidase activity from larval Spodoptera littoralis, Insect Biochem. Molec. Biol. 25, 63-71.
97. Takeda, J. & Kinoshita, T. (1995) Glycosyl-PtdIns-anchor biosynthesis, Trends Biochem. Sci. 20, 367-371.
98. Lu, Y.-J. & Adang, M. (1996) Conversion of Bacillus thuringiensis CryIAc-binding aminopeptidase to a soluble form by endogenous phosphalidylinositol phospholipase C. Insect Biochem. Mol. Biol. 26, 33-40.
99. Higgins, D. & Sharp, P. (1988) CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene (Amst.) 73, 237-244.
100. Tan, P., van Alen-Boerrigter I., Poolman, B., Siezen, R., de Vos, W. & Konings, W. (1992) Characterization of the Lactococcus lactis pepN gene encoding aminopeptidase homologous to mammalian amiopeptidase N, FEBS Lett. 306, 9-16.
101. Germann, U., Willingham, M., Pastan, I. & Gottesman, M. (1990) Expression of the human multidrug transporter in insect cells by a recombinant baculovirus. Biochemistry 29, 2295-2303.
102. Kartner, N., Hanrahan, J., Jensen, T., Naismith, A., Sun, S., Ackerley, C., Reyes, E., Tsui, L.-C., Rommens, J., Bear, C. & Riordan, J. (1991) Expression of the cystic fibrosis gene in non-epithelial invertebrate cells produces a regulated anion conductance. Cell 64, 681-691.
103. Fountoulakis, M., Schlaeger, E.-J., Gentz, R., Juranville, J.-F., Manneberg, M., Ozmen, L. & Garotta, G. (1991) Purification and biochemical characterization of a soluble mouse interteron-receptor produced in insect cells. Eur. J. Biochem. 198, 441-450.
104. + antiporter (NHE-1) in baculovirus-infected cells, Biochemistry 30, 9510-9515.
105. Rankl, N., Rice, J., Gurganus, T., Barbee, J. & Burns, J. (1994) The production of an active protein kinase C-in insect cells is greatly enhanced by the use of the basic protein promoter. Protein Expr. Purif. 5, 346-356.
106. Jarvis, D. & Finn, E. (1995) Biochemical analysis of the N-glycosylation pathway in baculovirus-infected lepidopteran insect cells, Virology 212, 500-511.