The ATP-binding cassette transporter subfamily C member 2 in Bombyx mori larvae is a functional receptor for Cry toxins from Bacillus thuringiensis

FEBS Journal

Volumn 280, Issue 8, 2013, Pages 1782-1794

  Tanaka, Shiho ^a   Miyamoto, Kazuhisa ^b   Noda, Hiroaki ^b   Jurat Fuentes, Juan Luis ^c   Yoshizawa, Yasutaka ^a   Endo, Haruka ^a   Sato, Ryoichi ^a  

^a TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

^b NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^c UNIVERSITY OF TENNESSEE   (United States)

Author keywords

ATP binding cassette transporter C2; Bacillus thuringiensis; Bombyx mori; cadherin like receptor; Cry toxin

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER C2; BACILLUS THURINGIENSIS TOXIN; CADHERIN; CRY1AB TOXIN; CRY1AC TOXIN; CRY1F TOXIN; CRY8CA TOXIN; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACILLUS THURINGIENSIS; BIOLOGICAL PEST CONTROL; BOMBYX MORI; CONTROLLED STUDY; CORRELATION ANALYSIS; INSECT RESISTANCE; LARVA; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SF9 CELL; TRANSGENIC CROP;

ANIMALS; BOMBYX; CADHERINS; INSECT PROTEINS; LARVA; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; RECEPTORS, CELL SURFACE;

BACILLUS THURINGIENSIS; BOMBYX MORI; HEXAPODA;

EID: 84876291348     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12200     Document Type: Article

References (40)

1. van Frankenhuyzen K, (2009) Insecticidal activity of Bacillus thuringiensis crystal proteins. J Invertebr Pathol 101, 1-16.
2. Roh JY, Choi JY, Li MS, Jin BR, &, Je YH, (2007) Bacillus thuringiensis as a specific, safe, and effective tool for insect pest control. J Microbiol Biotechnol 17, 547-559.
3. Bravo A, Likitvivatanavong S, Gill SS, &, Soberon M, (2011) Bacillus thuringiensis: a story of a successful bioinsecticide. Insect Biochem Mol Biol 41, 423-431.
4. Pardo-Lõpez L, Soberõn M, &, Bravo A, (2012) Bacillus thuringiensis insecticidal three-domain Cry toxins: mode of action, insect resistance and consequences for crop protection. FEMS Microbiol Rev 37, 3-22.
5. Pigott CR, &, Ellar DJ, (2007) Role of receptors in Bacillus thuringiensis crystal toxin activity. Microbiol Mol Biol Rev 71, 255-281.
6. Gõmez I, Sánchez J, Miranda R, Bravo A, &, Soberõn M, (2002) Cadherin-like receptor binding facilitates proteolytic cleavage of helix alpha-1 in domain I and oligomer pre-pore formation of Bacillus thuringiensis Cry1Ab toxin. FEBS Lett 513, 242-246.
7. Arenas I, Bravo A, Soberõn M, &, Gõmez I, (2010) Role of alkaline phosphatase from Manduca sexta in the mechanism of action of Bacillus thuringiensis Cry1Ab toxin. J Biol Chem 285, 12497-12503.
8. Bravo A, Gõmez I, Conde J, Muñoz-Garay C, Sánchez J, Miranda R, Zhuang M, Gill SS, &, Soberõn 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.
9. Villalon M, Vachon V, Brousseau R, Schwartz JL, &, Laprade R, (1998) Video imaging analysis of the plasma membrane permeabilizing effects of Bacillus thuringiensis insecticidal toxins in Sf9 cells. Biochim Biophys Acta 1368, 27-34.
10. Zhang X, Candas M, Griko NB, Taussig R, &, Bulla LA Jr, (2006) 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, 9897-9902.
11. Nagamatsu Y, Koike T, Sasaki K, Yoshimoto A, &, Furukawa Y, (1999) The cadherin-like protein is essential to specificity determination and cytotoxic action of the Bacillus thuringiensis insecticidal CryIAa toxin. FEBS Lett 460, 385-390.
12. Hua G, Jurat-Fuentes JL, &, Adang MJ, (2004) Fluorescent-based assays establish Manduca sexta Bt-R(1a) cadherin as a receptor for multiple Bacillus thuringiensis Cry1A toxins in Drosophila S2 cells. Insect Biochem Mol Biol 34, 193-202.
13. Jurat-Fuentes JL, &, Adang MJ, (2006) The Heliothis virescens cadherin protein expressed in Drosophila S2 cells functions as a receptor for Bacillus thuringiensis Cry1A but not Cry1Fa toxins. Biochemistry 45, 9688-9695.
14. Flannagan RD, Yu CG, Mathis JP, Meyer TE, Shi X, Siqueira HA, &, Siegfried BD, (2005) Identification, cloning and expression of a Cry1Ab cadherin receptor from European corn borer, Ostrinia nubilalis (Hubner) (Lepidoptera: Crambidae). Insect Biochem Mol Biol 35, 33-40.
15. Gahan LJ, Gould F, &, Heckel DG, (2001) Identification of a gene associated with Bt resistance in Heliothis virescens. Science 293, 857-860.
16. Xu X, Yu L, &, Wu Y, (2005) Disruption of a cadherin gene associated with resistance to Cry1Ac δ-endotoxin of Bacillus thuringiensis in Helicoverpa armigera. Appl Environ Microbiol 71, 948-954.
17. Morin S, Biggs RW, Sisterson MS, Shriver L, Ellers-Kirk C, Higginson D, Holley D, Gahan LJ, Heckel DG, Carrière Y, et al,. (2003) Three cadherin alleles associated with resistance to Bacillus thuringiensis in pink bollworm. Proc Natl Acad Sci USA 100, 5004-5009.
18. Gill M, &, Ellar D, (2002) Transgenic Drosophila reveals a functional in vivo receptor for the Bacillus thuringiensis toxin Cry1Ac1. Insect Mol Biol 11, 619-625.
19. Zhang S, Cheng H, Gao Y, Wang G, Liang G, &, Wu K, (2009) Mutation of an aminopeptidase N gene is associated with Helicoverpa armigera resistance to Bacillus thuringiensis Cry1Ac toxin. Insect Biochem Mol Biol 39, 421-429.
20. Yang Y, Zhu YC, Ottea J, Husseneder C, Rogers Leonard B, Abel C, &, Huang F, (2010) Molecular characterization and RNA interference of three midgut aminopeptidase N isozymes from Bacillus thuringiensis-susceptible and -resistant strains of sugarcane borer, Diatraea saccharalis. Insect Biochem Mol Biol 40, 592-603.
21. Tiewsiri K, &, Wang P, (2011) Differential alteration of two aminopeptidases N. 207 associated with resistance to Bacillus thuringiensis toxin Cry1Ac in cabbage looper. Proc Natl Acad Sci USA 108, 14037-14042.
22. Jurat-Fuentes JL, Karumbaiah L, Jakka SRK, Ning C, Liu C, Wu K, Jackson J, Gould F, Blanco CA, Portilla M, et al,. (2011) Reduced levels of membrane-bound alkaline phosphatase are common to lepidopteran strains resistant to Cry toxins from Bacillus thuringiensis. PLoS One 6, e17606.
23. Jurat-Fuentes JL, &, Adang MJ, (2004) Characterization of a Cry1Ac-receptor alkaline phosphatase in susceptible and resistant Heliothis virescens larvae. Eur J Biochem 271, 3127-3135.
24. Gahan LJ, Pauchet Y, Vogel H, &, Heckel DG, (2010) An ABC transporter mutation is correlated with insect resistance to Bacillus thuringiensis Cry1Ac toxin. PLoS Genet 6, e1001248.
25. Atsumi S, Miyamoto K, Yamamoto K, Narukawa J, Kawai S, Sezutsu H, Kobayashi I, Uchino K, Tamura T, Mita K, et al,. (2012) A single amino acid mutation in an ABC transporter gene causes resistance to Bt toxin Cry1Ab in the silkworm, Bombyx mori. Proc Natl Acad Sci USA 109, E1591-E1598.
26. Baxter SW, Badenes-Perez FR, Morrison A, Vogel H, Crickmore N, Kain W, Wang P, Heckel DG, &, Jiggins CD, (2011) Parallel evolution of Bacillus thuringiensis toxin resistance in lepidoptera. Genetics 189, 675-679.
27. Ibiza-Palacios MS, Ferré J, Higurashi S, Miyamoto K, Sato R, &, Escriche B, (2008) Selective inhibition of binding of Bacillus thuringiensis Cry1Ab toxin to cadherin-like and aminopeptidase proteins in brush-border membranes and dissociated epithelial cells from Bombyx mori. Biochem J 409, 215-221.
28. Nakanishi K, Yaoi K, Nagino Y, Hara H, Kitami M, Atsumi S, Miura N, &, 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.
29. King MG, &, Baskin DG, (1991) Effect of paraformaldehyde fixation on localization and characterization of insulin-like growth factor-I (IGF-I) receptors in the rat brain. Anat Rec 231, 467-472.
30. Huang LZ, &, Winzer-Serhan UH, (2006) Effects of paraformaldehyde fixation on nicotinic acetylcholine receptor binding in adult and developing rat brain sections. J Neurosci Methods 153, 312-317.
31. Tsuda Y, Nakatani F, Hashimoto K, Ikawa S, Matsuura C, Fukada T, Sugimoto K, &, Himeno M, (2003) Cytotoxic activity of Bacillus thuringiensis Cry proteins on mammalian cells transfected with cadherin-like Cry receptor gene of Bombyx mori (silkworm). Biochem J 369, 697-703.
32. Pacheco S, Gõmez I, Arenas I, Saab-Rincon G, Rodríguez- Almazán C, Gill SS, Bravo A, &, Soberõn M, (2009) Domain II loop 3 of Bacillus thuringiensis Cry1Ab toxin is involved in a 'ping pong' binding mechanism with Manduca sexta aminopeptidase-N and cadherin receptors. J Biol Chem 284, 32750-32757.
33. Fernández-Luna MT, Tabashnik BE, Lanz-Mendoza H, Bravo A, Soberõn M, &, Miranda-Ríos J, (2010) Single concentration tests show synergism among Bacillus thuringiensis subsp. israelensis toxins against the malaria vector mosquito Anopheles albimanus. J Invertebr Pathol 104, 231-233.
34. Banks DJ, Jurat-Fuentes JL, Dean DH, &, Adang MJ, (2001) Bacillus thuringiensis Cry1Ac and Cry1Fa delta-endotoxins share common binding proteins in Heliothis virescens. Insect Biochem Mol Biol 31, 909-918.
35. Ohba M, Iwahana H, Asano S, Suzuki N, Sato R, &, Hori H, (1992) A unique isolate of Bacillus thuringiensis serovar japonensis with a high larvicidal activity specific for scarabaeid beetles. Lett Appl Microbiol 14, 54-57.
36. Donovan WP, Rupar MJ, Slaney AC, Malvar T, Gawron-Burke MC, &, Johnson TB, (1992) Characterization of two genes encoding Bacillus thuringiensis insecticidal crystal proteins toxic to Coleoptera species. Appl Environ Microbiol 58, 3921-3927.
37. Banks DJ, Hua G, &, Adang MJ, (2003) Cloning of a Heliothis virescens 110 kDa aminopeptidase N and expression in Drosophila S2 cells. Insect Biochem Mol Biol 33, 499-508.
38. Atsumi S, Mizuno E, Hara H, Nakanishi K, Kitami M, Miura N, Tabunoki H, Watanabe A, &, Sato R, (2005) Location of the Bombyx mori aminopeptidase N type 1 binding site on Bacillus thuringiensis Cry1Aa toxin. Appl Environ Microbiol 71, 3966-3977.
39. Obata F, Kitami M, Inoue Y, Atsumi S, Yoshizawa Y, &, Sato R, (2009) Analysis of the region for receptor binding and triggering of oligomerization on Bacillus thuringiensis Cry1Aa toxin. FEBS J 276, 5949-5959.
40. Bliss CI, (1934) The method of probits. Science 79, 38-39.