Sodium solute symporter and cadherin proteins act as bacillus thuringiensis CRY3BA toxin functional receptors in tribolium castaneum

Journal of Biological Chemistry

Volumn 288, Issue 25, 2013, Pages 18013-18021

  Contreras, Estefanía ^a   Schoppmeier, Michael ^b   Real, M Dolores ^a   Rausell, Carolina ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO PEPTIDASE; BACILLUS THURINGIENSIS; CADHERIN PROTEINS; E-CADHERINS; FUNCTIONAL RECEPTORS;

BACTERIOLOGY; SODIUM; TOXICITY;

GLYCOPROTEINS;

BACILLUS THURINGIENSIS TOXIN; BINDING PROTEIN; CRY3BA TOXIN; DOUBLE STRANDED RNA; MICROSOMAL AMINOPEPTIDASE; SODIUM SOLUTE SYMPORTER; UNCLASSIFIED DRUG; UVOMORULIN;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ARTHROPOD LARVA; ARTICLE; CONTROLLED STUDY; LIQUID CHROMATOGRAPHY; MANDUCA SEXTA; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RECEPTOR BINDING; RNA INTERFERENCE; SEQUENCE HOMOLOGY; TENEBRIO MOLITOR; TOXICITY TESTING; TRIBOLIUM CASTANEUM;

CADHERINS; HOST-PATHOGEN INTERACTIONS; RECEPTORS; RNA INTERFERENCE (RNAI); TRANSPORTERS;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD13; BACTERIAL PROTEINS; BINDING SITES; CADHERINS; ENDOTOXINS; EPITOPES; HEMOLYSIN PROTEINS; IMMUNOBLOTTING; INSECT PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; RECEPTORS, CELL SURFACE; RNA INTERFERENCE; SEQUENCE HOMOLOGY, AMINO ACID; SODIUM; SYMPORTERS; TRIBOLIUM;

EID: 84880074414     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.474445     Document Type: Article

References (48)

1. Crickmore, N. (2005) Using worms to better understand how Bacillus thuringiensis kills insects. Trends Microbiol. 13, 347-350 (Pubitemid 41073803)
2. Knight, P. J., Crickmore, N., and Ellar, D. J. (1994) The receptor for Bacillus thuringiensis CrylA(c)-?endotoxin in the brush border membrane of the lepidopteran Manduca sexta is aminopeptidase N. Mol. Microbiol. 11, 429-436 (Pubitemid 24205455)
3. Vadlamudi, R. K., Weber, E., Ji, I., Ji, T. H., and Bulla, L. A. Jr. (1995) Cloning and expression of a receptor for an insecticidal toxin of Bacillus thuringiensis. J. Biol. Chem. 270, 5490-5494
4. Jurat-Fuentes, J. L., and Adang, M. J. (2004) Characterization of a Cry1Acreceptor alkaline phosphatase in susceptible and resistant Heliothis virescens larvae. Eur. J. Biochem. 271, 3127-3135 (Pubitemid 38998682)
5. Tanaka, S., Miyamoto, K., Noda, H., Jurat-Fuentes, J. L., Yoshizawa, Y., Endo, H., and Sato, R. (2013) The ATP-binding cassette transporter subfamily C member 2 in Bombyx mori larvae is a functional receptor for Cry toxins from Bacillus thuringiensis. FEBS J. 280, 1782-1794
6. Likitvivatanavong, S., Chen, J., Bravo, A., Soberón, M., and Gill, S. S. (2011) Cadherin, alkaline phosphatase, and aminopeptidase N as receptors of Cry11Ba toxin from Bacillus thuringiensis subsp. jegathesan in Aedes aegypti. Appl. Environ. Microbiol. 77, 24-31
7. Fabrick, J., Oppert, C., Lorenzen, M. D., Morris, K., Oppert, B., and Jurat-Fuentes, J. L. (2009) A novel Tenebrio molitor cadherin is a functional receptor for Bacillus thuringiensis Cry3Aa toxin. J. Biol. Chem. 284, 18401-18410
8. Ochoa-Campuzano, C., Real, M. D., Martínez-Ramírez, A. C., Bravo, A., and Rausell, C. (2007) An ADAM metalloprotease is a Cry3Aa Bacillus thuringiensis toxin receptor. Biochem. Biophys. Res. Commun. 362, 437-442 (Pubitemid 47332428)
9. Martins, E. S., Monnerat, R. G., Queiroz, P. R., Dumas, V. F., Braz, S. V., de Souza Aguiar, R. W., Gomes, A. C., Sánchez, J., Bravo, A., and Ribeiro, B. M. (2010) Midgut GPI-anchored proteins with alkaline phosphatase activity from the cotton boll weevil (Anthonomus grandis) are putative receptors for the Cry1B protein of Bacillus thuringiensis. Insect Biochem. Mol. Biol. 40, 138-145
10. Rajagopal, R., Sivakumar, S., Agrawal, N., Malhotra, P., and Bhatnagar, R. K. (2002) Silencing of midgut aminopeptidaseNof Spodoptera litura by double-stranded RNA establishes its role as Bacillus thuringiensis toxin receptor. J. Biol. Chem. 277, 46849-46851 (Pubitemid 36159186)
11. Soberón, M., Pardo-López, L., López, I., Gómez, I., Tabashnik, B. E., and Bravo, A. (2007) Engineering modified Bt toxins to counter insect resistance. Science 318, 1640-1642 (Pubitemid 350233665)
12. Pigott, C. R., and Ellar, D. J. (2007) Role of receptors in Bacillus thuringi-ensis crystal toxin activity. Microbiol. Mol. Biol. Rev. 71, 255-281 (Pubitemid 46954306)
13. 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 aminopeptidase N genes. BMC Genomics 6, 96
14. Gómez, I., Oltean, D. I., Gill, S. S., Bravo, A., and Soberón, M. (2001) Mapping the epitope in cadherin-like receptors involved in Bacillus thuringiensis Cry1A toxin interaction using phage display. J. Biol. Chem. 276, 28906-28912
15. Dorsch, J. A., Candas, M., Griko, N. B., Maaty, W. S., Midboe, E. G., Vadlamudi, R. K., and Bulla, L. A., Jr. (2002) Cry1A toxins of Bacillus thuringiensis bind specifically to a region adjacent to the membrane-proximal extracellular domain of BT-R1 in Manduca sexta. Involvement of a cadherin in the entomopathogenicity of Bacillus thuringiensis. Insect Biochem. Mol. Biol. 32, 1025-1036 (Pubitemid 35025336)
16. Hua, G., Jurat-Fuentes, J. L., and Adang, M. J. (2004) Bt-R1a extracelular cadherin repeat 12 mediates Bacillus thuringiensis Cry1Ab binding and cytotoxicity. J. Biol. Chem. 279, 28051-28056 (Pubitemid 38900076)
17. Bravo, A., Gómez, I., Conde, J., Muñoz-Garay, C., Sánchez, J., Miranda, R.,Zhuang, M., Gill, S. S., and Soberón, M. (2004) Oligomerization triggers differential binding of a pore-forming toxin to a different receptor leading to efficient interaction with membrane microdomains. Biochim. Biophys. Acta 1667, 38-46 (Pubitemid 39463332)
18. McNall, R. J., and Adang, M. J. (2003) Identification of novel Bacillus thuringiensis Cry1Ac binding proteins in Manduca sexta midgut through proteomic analysis. Insect Biochem. Mol. Biol. 33, 999-1010 (Pubitemid 37245057)
19. Krishnamoorthy, M., Jurat-Fuentes, J. L., McNall, R. J., Andacht, T., and Adang, M. J. (2007) Identification of novel Cry1Ac binding proteins in midgut membranes from Heliothis virescens using proteomic analyses. Insect Biochem. Mol. Biol. 37, 189-201 (Pubitemid 46216813)
20. Chen, L. Z., Liang, G. M., Zhang, J., Wu, K. M., Guo, Y. Y., and Rector, B. G. (2010) Proteomic analysis of novel Cry1Ac binding proteins in Helicoverpa armigera (Hübner). Arch. Insect Biochem. Physiol. 73, 61-73
21. Bayyareddy, K., Andacht, T. M., Abdullah, M. A., and Adang, M. J. (2009) Proteomic identification of Bacillus thuringiensis subsp. israeliensis toxin Cry4Ba binding proteins in midgut membranes from Aedes (Stegomyia) aegypti Linnaeus (Diptera, Culicidae) larvae. Insect Biochem. Mol. Biol. 39, 279-286
22. Morris, K., Lorenzen, M. D., Hiromasa, Y., Tomich, J. M., and Oppert, C. (2009) Tribolium castaneum larval gut transcriptome and proteome. A resource for the study of the coleopteran gut. J. Proteome Res. 8, 3889-3898
23. Contreras, E., Rausell, C., and Real, M. D. (2013) Proteome response of Tribolium castaneum larvae to Bacillus thuringiensis toxin producing strains. PLoS One 8, e55330
24. Stewart, G. S., Johnstone, K., Hagelberg, E., and Ellar, D. J. (1981) Commitment of bacterial spores to germinate. A measure of the trigger reaction. Biochem. J. 198, 101-106
25. Rausell, C., García-Robles, I., Sánchez, J., Muñoz-Garay, C., Martínez-Ramírez, A. C., Real, M. D., and Bravo, A. (2004) Role of toxin activation on binding and pore formation activity of the Bacillus thuringiensis Cry3 toxins in membranes of Leptinotarsa decemlineata (Say). Biochim. Biophys. Acta 1660, 99-105 (Pubitemid 38125236)
26. Wolfersberger, M., Lüthy, P., Maurer, A., Parenti, P., Sacchi, F. V., Giordana, B., and Hanozet, G. M. (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. 86A, 301-308
27. Reuveni, M., and Dunn, P. E. (1991) Differential inhibition by Bacillus thuringiensis delta endotoxin of leucine and aspartic uptake in BBMV from midgut of Manduca sexta. Biochem. Biophys. Res. Commun. 181, 1089-1093
28. Hafkenscheid, J. C. (1984) Aminopeptidases and amino acid arylamidases. In Methods of Enzymatic Analysis (Bergmeyer, H. U., Bergmeyer, J. and Grassl, M., eds) Vol. V, 3rd Ed., pp. 2-34, Verlag Chemie, Weinheim
29. Xie, Y. S., Bodnaryk, R. P., and Fields, P. G. (1996) A rapid and simple flour-disk bioassay for testing substances active against stored-product insects. Can. Entomol. 128, 865-875 (Pubitemid 127553662)
30. Lord, J. C., Hartzer, K., Toutges, M., and Oppert, B. (2010) Evaluation of quantitative PCR reference genes for gene expression studies in Tribolium castaneum after fungal challenge. J. Microbiol. Methods 80, 219-221
31. Ma, G., Rahman, M. M., Grant, W., Schmidt, O., and Asgari, S. (2012) Insect tolerance to the crystal toxins Cry1Ac and Cry2Ab is mediated by the binding of monomeric toxin to lipophorin glycolipids causing oligomerization and sequestration reactions. Dev. Comp. Immunol. 37, 184-192
32. Whyard, S., Singh, A. D., and Wong, S. (2009) Ingested double-stranded RNAs can act as species-specific insecticides. Insect. Biochem. Mol. Biol. 39, 824-832
33. Petersen, T. N., Brunak, S., von Heijne, G., and Nielsen, H. (2011) SignalP 4.0. Discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785-786
34. Jung, H. (2002) The sodium/substrate symporter family. Structural and functional features. FEBS Lett. 529, 73-77 (Pubitemid 35283914)
35. Jonassen, I., Collins, J. F., and Higgins D. (1995) Finding flexible patterns in unaligned protein sequences. Protein Sci. 4, 1587-1595
36. Chen, J., Hua, G., Jurat-Fuentes, J. L., Abdullah, M. A., and Adang, M. J. (2007) Synergism of Bacillus thuringiensis toxins by a fragment of a toxinbinding cadherin. Proc. Natl. Acad. Sci. U.S.A. 104, 13901-13906 (Pubitemid 350003310)
37. Gao, Y., Jurat-Fuentes, J. L., Oppert, B., Fabrick, J. A., Liu, C., Gao, J., and Lei, Z. (2011) Increased toxicity of Bacillus thuringiensis Cry3Aa against Crioceris quatuordecimpunctata, Phaedon brassicae and Colaphellus bowringi by a Tenebrio molitor cadherin fragment. Pest Manag. Sci. 67, 1076-1081
38. Chen, J., Aimanova, K. G., Fernandez, L. E., Bravo, A., Soberon, M., and Gill, S. S. (2009) Aedes aegypti cadherin serves as a putative receptor of the Cry11Aa toxin from Bacillus thuringiensis subsp. israelensis. Biochem. J. 424, 191-200
39. Saier, M. H., Jr., Yen, M. R., Noto, K., Tamang, D. G., and Elkan, C. (2009) The Transporter Classification Database. Recent advances. Nucleic Acids Res. 37, 274-278
40. Wong, F. H., Chen, J. S., Reddy, V., Day, J. L., Shlykov, M. A., Wakabayashi, S. T., and Saier, M. H., Jr. (2012) The amino acid-polyamine- organocation superfamily. J. Mol. Microbiol. Biotechnol. 22, 105-113
41. Gahan, L. J., Pauchet, Y., Vogel, H., and Heckel, D. G. (2010) An ABC transporter mutation is correlated with insect resistance to Bacillus thuringiensis Cry1Ac toxin. PLoS Genet. 6, e1001248
42. Atsumi, S., Miyamoto, K., Yamamoto, K., Narukawa, J., Kawai, S., Sezutsu, H., Kobayashi, I., Uchino, K., Tamura, T., Mita, K., Kadono-Okuda, K., Wada, S., Kanda, K., Goldsmith, M. R., and Noda, H. (2012)Asingle amino acid mutation in an ABC transporter gene causes resistance to Bt toxin Cry1Ab in the silkworm, Bombyx mori. Proc. Natl. Acad. Sci. U.S.A. 109, E1591-E1598
43. Saier, M. H. Jr. (2000) A functional-phylogenetic classification system for transmembrane solute transporters. Microbiol. Mol. Biol. Rev. 64, 354-411 (Pubitemid 30412678)
44. Jardetzky, O. (1966) Simple allosteric model for membrane pumps. Nature 211, 969-970
45. Heckel, D. G. (2012) Learning the ABCs of Bt.ABCtransporters and insect resistance to Bacillus thuringiensis provide clues to a crucial step in toxin mode of action. Pestic. Biochem. Physiol. 104, 103-110
46. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011) MEGA5. Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739
47. Saitou, N., and Nei, M. (1987) The neighbor-joining method. A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425
48. Zuckerkandl, E., and Pauling, L. (1965) Evolutionary divergence and convergence in proteins. In Evolving Genes and Proteins (Bryson, V., and Vogel, H. J., eds) pp. 97-166, Academic Press, New York