Bacillus thuringiensis Cry1A toxin-binding glycoconjugates present on the brush border membrane and in the peritrophic membrane of the Douglas-fir tussock moth are peritrophins

Adang, 1983, Permeability of the PM of the Douglas fir tussock moth (Orgyia pseudotsugata), Comp. Biochem. Physiol., 75A, 233, 10.1016/0300-9629(83)90075-0 Aranda, 1996, Interactions of Bacillus thuringiensis crystal proteins with the midgut epithelial cells of Spodoptera frugiperda (Lepidoptera: Noctuidae), J. Invertebr. Pathol., 68, 203, 10.1006/jipa.1996.0087 Baxter, 2011, Parallel evolution of Bacillus thuringiensis toxin resistance in Lepidoptera, Genetics, 189, 675, 10.1534/genetics.111.130971 Bolognesi, 2001, The PM of Spodoptera frugiperda: secretion of peritrophins and role in immobilization and recycling digestive enzymes, Arch. Insect Biochem. Physiol., 47, 62, 10.1002/arch.1037 Bravo, 1992, Immunocytochemical localization of Bacillus thuringiensis insecticidal crystal proteins in intoxicated insects, J. Invertebr. Pathol., 60, 237, 10.1016/0022-2011(92)90004-N Chen, 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, 10.1007/s00441-005-1124-6 Chen, 2009, Gangliosides as high affinity receptors for tetanus neurotoxin, J. Biol. Chem., 284, 26569, 10.1074/jbc.M109.027391 DeLello, 1984, Histopathological effects of Bacillus thuringiensis on the midgut of the tobacco hornworm larvae (Manduca sexta): low doses compared with fasting, J. Invertebr. Pathol., 43, 169, 10.1016/0022-2011(84)90135-6 Denolf, P., Jansens, S., Peferoen, M., Degheele, D., Van Rie, J. 1993. Two Different Bacillus thuringiensis Delta-Endotoxin Receptors in the Midgut Brush Border Membrane of the European Corn Borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Pyralidae). Dubois, 1995, Synergism between Cry1A insecticidal crystal proteins and spores of Bacillus thuringiensis, other bacterial spores, and vegetative cells against Lymantria dispar (Lepidoptera: Lymantriidae) larvae, Environ. Entomol., 24, 1741, 10.1093/ee/24.6.1741 Duk, 1997, β-elimination of O-glycans from glycoproteins transferred to immobilon P membranes: method and some applications, Anal. Biochem., 253, 98, 10.1006/abio.1997.9994 Griffitts, 2001, Bt toxin resistance from loss of a putative carbohydrate-modifying enzyme, Science, 293, 860, 10.1126/science.1062441 Hayakawa, 2004, GalNAc pretreatment inhibits trapping of Bacillus thuringiensis Cry1Ac on the PM of Bombyx mori, FEBS Lett., 576, 331, 10.1016/j.febslet.2004.09.029 Hegedus, 2009, New insights into peritrophic matrix synthesis, architecture, and function, Annu. Rev. Entomol., 54, 285, 10.1146/annurev.ento.54.110807.090559 Heimpel, 1959, The site of action of crystalliferous bacteria in lepidoptera larvae, J. Insect Pathol., 1, 152 Hofmann, 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, 10.1073/pnas.85.21.7844 Jenkins, 1999, Binding of Bacillus thuringiensis Cry1Ac toxin to Manduca sexta aminopeptidase-N receptor is not directly related to toxicity, FEBS Lett., 462, 373, 10.1016/S0014-5793(99)01559-8 Jurat-Fuentes, 2002, 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, 5711, 10.1128/AEM.68.11.5711-5717.2002 Kiessling, 1996, Strength in numbers: non-natural polyvalent carbohydrate derivatives, Chem. Biol., 3, 71, 10.1016/S1074-5521(96)90280-X Kitami, 2011, Bacillus thuringiensis Cry toxins bound specifically to various proteins via domain III, which has a galactose-binding domain-like fold, Biosci. Biotechnol. Biochem., 75, 305, 10.1271/bbb.100689 Knight, 2004, Analysis of glycan structures on the 120kDa aminopeptidase N of Manduca sexta and their interactions with Bacillus thuringiensis Cry1Ac toxin, Insect Biochem. Mol. Biol., 34, 101, 10.1016/j.ibmb.2003.09.007 Lehane, 1996, Composition of the peritrophic matrix of the tsetse fly Glossinia morsitans morsitans, Cell Tissue Res., 283, 375, 10.1007/s004410050548 Lehane, 1997, Peritrophic matrix structure and function, Ann. Rev. Entomol., 42, 525, 10.1146/annurev.ento.42.1.525 Martin, 1989, Dynamic role of microvilli in PM formation, Tissue Cell., 21, 627, 10.1016/0040-8166(89)90013-X Merzendorfer, 2003, Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinases, J. Exp. Biol., 206, 4393, 10.1242/jeb.00709 Michiels, 2010, Plant-insect interactions: what can we learn from plant lectins?, Arch. Insect Biochem. Physiol., 73, 193, 10.1002/arch.20351 Milne, 1995, A protein complex from Choristoneura fumiferana gut-juice involved in the precipitation of δ-endotoxin from Bacillus thuringiensis subsp. sotto, Insect Biochem. Mol. Biol., 25, 1101, 10.1016/0965-1748(95)00046-1 Mohan, 2006, Degradation of S. frugiperda peritrophic matrix by an inducible maize cysteine protease, J. Insect Physiol., 52, 21, 10.1016/j.jinsphys.2005.08.011 Moonsom, S., Chaisri, U., Wang, P., Angsuthanasombat, C. 2008. Effect of the Bacillus thuringiensis Cry4Ba toxin on the PM in Aedes aegypti mosquito larvae. In: Program and abstracts, 41st Annual Meeting of the Society of Invertebrate Pathology. August 3–7, 2008. Coventry, United Kingdom. Murdock, 2002, Lectins and protease inhibitors as plant defenses against insects, J. Agric. Food Chem., 50, 66015, 10.1021/jf020192c Ning, 2010, Characterization of a Cry1Ac toxin-binding alkaline phosphatase in the midgut from Helicoverpa armigera (Hübner) larvae, J. Insect Physiol., 56, 666, 10.1016/j.jinsphys.2010.02.003 Oppert, 1994, Altered protoxin activation by midgut enzymes from a Bacillus thuringiensis resistant strain of Plodia interpuctella, Biochem. Biophys. Res. Commun., 98, 940, 10.1006/bbrc.1994.1134 Pigott, 2007, Role of receptors in Bacillus thuringiensis crystal toxin activity, Microbiol. Mol. Biol. Rev., 71, 255, 10.1128/MMBR.00034-06 Rees, 2009, PM contribution to Bt Cry δ-endotoxin susceptibility in Lepidoptera and the effect of Calcofluor, J. Invertebr. Pathol., 100, 139, 10.1016/j.jip.2009.01.002 Rupp, 1985, Protein alterations in Manduca sexta midgut and haemolymph following treatment with a sublethal dose of Bacillus thuringiensis crystal endotoxin, Insect Biochem., 15, 147, 10.1016/0020-1790(85)90002-2 Sarkar, 2008, Homodimeric alkaline phosphatase located at Helicoverpa armigera midgut, a putative receptor of Cry1Ac contains α-GalNAc in terminal glycan structure as interactive epitope, J. Proteome Res., 8, 1838, 10.1021/pr8006528 Schnepf, 1998, Bacillus thuringiensis and its pesticidal crystal proteins, Microbiol. Mol. Biol. Rev., 62, 775, 10.1128/MMBR.62.3.775-806.1998 Sousa, 2010, Histopathology and ultrastructure of midgut of Alabama argillacea (Hübner) (Lepidoptera: Noctuidae) fed Bt-cotton, J. Insect Physiol., 56, 1019, 10.1016/j.jinsphys.2010.08.014 Stelzer, 1975, Aerial applications of a nucleopolyhedrosis virus and Bacillus thuringiensis against the Douglas fir tussock moth, J. Econom. Entomol., 68, 269, 10.1093/jee/68.2.269 Tellman, 1999, Peritrophic matrix proteins, Insect Biochem. Mol. Biol., 29, 87, 10.1016/S0965-1748(98)00123-4 Thompson, C.G., Peterson, L.J. 1978. Rearing the Douglas-fir tussock moth. USDA Agriculture Handbook No. 520, Combined Forestry Pest Research and Development Program, Washington, DC. Vachon, 2012, Current models of the mode of action of Bacillus thuringiensis insecticidal crystal proteins: a critical review, J. Invertebr. Pathol., 111, 1, 10.1016/j.jip.2012.05.001 Valaitis, 2001, Isolation and partial characterization of gypsy moth BTR-270, an anionic brush border membrane glycoconjugate that binds Bacillus thuringiensis Cry1A toxins with high affinity, Arch. Insect Biochem. Physiol., 46, 186, 10.1002/arch.1028 Valaitis, 2008, Bacillus thuringiensis pore-forming toxins trigger massive shedding of GPI-anchored aminopeptidase N from gypsy moth midgut epithelial cells, Insect Biochem. Mol. Biol., 38, 611, 10.1016/j.ibmb.2008.03.003 Valaitis, 2011, Localization of Bacillus thuringiensis Cry1A toxin-binding molecules in gypsy moth larval gut sections using fluorescence microscopy, J. Invertebr. Pathol., 108, 69 Van Rie, 1989, Specificity of Bacillus thuringiensis δ-endotoxins. Importance of specific receptors on the brush border membrane of the mid-gut of target insects, Eur. J. Biochem., 186, 239, 10.1111/j.1432-1033.1989.tb15201.x Wang, 2001, Molecular structure of the peritrophic membrane (PM): identification of potential PM target sites for insect control, Arch. Insect Biochem. Physiol., 47, 110, 10.1002/arch.1041 Wolfersberger, 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. A – Physiol., 86, 301, 10.1016/0300-9629(87)90334-3 Yi, 1996, Immunocytochemical localization of Bacillus thuringiensis CryI toxins in the midguts of three forest insects and Bombyx mori, Can J. Microbiol., 42, 634, 10.1139/m96-087 Zimoch, 2002, Immunolocalization of chitin synthase in the tobacco hornworm, Cell Tissue Res., 308, 287, 10.1007/s00441-002-0546-7 Zi-yan, 2006, Histopathological effects of the protein toxin from Xenorhabdus nematophila on the midgut of Helicoverpa armigera, Agric. Sci. China, 5, 685, 10.1016/S1671-2927(06)60111-9