Cry1Ac, a Bacillus thuringiensis toxin, triggers extracellular Ca2+ influx and Ca2+ release from intracellular stores in Cf1 cells (Choristoneura fumiferana, Lepidoptera)

Journal of Experimental Biology

Volumn 201, Issue 12, 1998, Pages 1851-1858

  Potvin, L ^a   Laprade, R ^b   Schwartz, J L ^a,b  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Bacillus thuringiensis; Ca2+ transport; Fura 2; Intracellular Ca2+; Ion channel; Lepidopteran cell line; Planar lipid bilayer

Indexed keywords

EID: 0031857851     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (54)

1. BUTKO, P., COURNOYER, M., PUSZTAI-CAREY, M. AND SUREWICZ, W. K. (1994). Membrane interactions and surface hydrophobicity of Bacillus thuringiensis δ-endotoxin CryIC. FEBS Lett. 340, 89-92.
2. CANNON, R. J. C. (1996). Bacillus thuringiensis use in agriculture: a molecular perspective. Biol. Rev. 71, 561-636.
3. CARROLL, J. AND ELLAR, D. J. (1993). An analysis of Bacillus thuringiensis δ-endotoxin action on insect-midgut-membrane permeability using a light-scattering assay. Eur. J. Biochem. 214, 771-778.
4. 2+ antagonist, 8-(N,N-diethylamino)octyl 3,4,5-trimethoxybenzoate hydrochloride in smooth and skeletal muscles. Br. J. Pharmac. 53, 279-285.
5. DENT, D. R. (1993). The use of Bacillus thuringiensis as an insecticide. In Exploitation of Microorganisms (ed. D. G. Jones), pp. 19-44. London: Chapman & Hall.
6. 2O from phospholipid vesicles is catalyzed by reconstituted midgut membrane. Insect Biochem. 21, 177-184.
7. FEDERICI, B. A. (1995). The future of microbial insecticides as vector control agents. J. am. Mosquito Contr. Ass. 11, 260-268.
8. GILL, S. S., COWLES, E. A. AND PIETRANTONIO, P. V. (1992). The mode of action of Bacillus thuringiensis endotoxins. A. Rev. Ent. 37, 615-636.
9. GOLE, J. W. D., ORR, G. L. AND DOWNER, R. G. H. (1987). Forskolin-insensitive adenylate cyclase in cultured cells of Choristoneura fumiferana (Insecta). Biochem. biophys. Res. Commun. 145, 1192-1197.
10. GROCHULSKI, P., MASSON, L., BORISOVA, S., PUSZTAI-CAREY, M., SCHWARTZ, J. L., BROUSSEAU, R. AND CYGLER, M. (1995). Bacillus thuringiensis Cry1A(a) insecticidal toxin: crystal structure and channel formation. J. molec. Biol. 254, 447-464.
11. 2+ indicators with greatly improved fluorescence properties. J. biol. Chem. 260, 3440-3450.
12. GUPTA, J. AND DOWNER, R. G. H. (1993). Partial characterization of protein kinase C from an insect cell line. Biochim. biophys. Acta 1203, 210-214.
13. HAIDER, M. Z. AND ELLAR, D. J. (1989). Mechanism of action of Bacillus thuringiensis insecticidal δ-endotoxin: interaction with phospholipid vesicles. Biochim. biophys. Acta 978, 216-222.
14. HARVEY, W. R. AND WOLFERSBERGER, M. G. (1979). Mechanism of inhibition of active potassium transport in isolated midgut of Manduca sexta by Bacillus thuringiensis endotoxin. J. exp. Biol. 83, 293-304.
15. HÖFTE, H. AND WHITELEY, H. R. (1989). Insecticidal crystal proteins of Bacillus thuringiensis. Microbiol. Rev. 53, 242-255.
16. HENDRICKX, K., DE LOOF, A. AND VAN MELLAERT, H. (1990). Effects of Bacillus thuringiensis δ-endotoxin on the permeability of brush border membrane vesicles from tobacco hornworm (Manduca sexta) midgut. Comp. Biochem. Physiol. 95C, 241-245.
17. 5 muscarinic receptor. Am. J. Physiol. 266, C1736-C1743.
18. 2+ influx pathway in Sf9 insect cells following expression of the transient receptor potential-like (trpl) protein of Drosophila. Biochem. biophys. Res. Commun. 201, 1050-1056.
19. JOHNSON, D. E. (1994). Cellular toxicities and membrane binding characteristics of insecticidal crystal proteins from Bacillus thuringiensis toward cultured insect cells. J. Invert. Pathol. 63, 123-129.
20. KNOWLES, B. H. (1994). Mechanism of action of Bacillus thuringiensis insecticidal δ-endotoxins. Adv. Insect Physiol. 24, 275-308.
21. KNOWLES, B. H. AND ELLAR, D. J. (1986). Characterization and partial purification of a plasma membrane receptor for Bacillus thuringiensis var. kurstaki lepidopteran-specifk δ-endotoxin. J. Cell Sci. 83, 89-101.
22. KNOWLES, B. H. AND FARNDALE, R. W. (1988). Activation of insect cell adenylate cyclase by Bacillus thuringiensis δ-endotoxins and melittin. Biochem. J. 253, 235-241.
23. LI, J., CARROLL, J. AND ELLAR, D. J. (1991). Crystal structure of insecticidal δ-endotoxin from Bacillus thuringiensis at 2 Å resolution. Nature 353, 815-821.
24. LIEBIG, B., STETSON, D. L. AND DEAN, D. H. (1995). Quantification of the effect of Bacillus thuringiensis toxins on short-circuit current in the midgut of Bombyx mori. J. Insect Physiol. 41, 17-22.
25. LORENCE, A., DARSZON, A., DIAZ, C., LIEVANO, A., QUINTERO, R. AND BRAVO, A. (1995). 8-Endotoxins induce cation channels in Spodoptera frugiperda brush border membranes in suspension and in planar lipid bilayers. FEBS Lett. 360, 217-222.
26. MARTIN, F. G. AND WOLFERSBERGER, M. G. (1995). Bacillus thuringiensis δ-endotoxin and larval Manduca sexta midgut brush-border membrane vesicles act synergistically to cause very large increases in the conductance of planar lipid bilayers. J. exp. Biol. 198, 91-96.
27. MASSON, L., PRÉFONTAINE, G., PÉLOQUIN, L., LAU, P. C. K. AND BROUSSEAU, R. (1989). Comparative analysis of the individual protoxin components in P1 crystals of Bacillus thuringiensis subsp. kurstaki isolates NRD-12 and HD-1. Biochem. J. 262, 507-512.
28. MCCARTHY, W. J. (1994a). Application of insect cell culture to the study of Bacillus thuringiensis toxins. In Insect Cell Biotechnology (ed. K. Maramorosch and A. McIntosh), pp. 71-88. Boca Raton, FL: CRC Press.
29. MCCARTHY, W. J. (1994b). Cytolytic differences among lepidopteran cell lines exposed to toxins of Bacillus thuringiensis subsp. kurstaki (HD-263) and aizawai (HD-112): effect of aminosugars and N-glycosylation. In Vitro cell. devl. Biol. 30A, 690-695.
30. MONETTE, R., POTVIN, L., BAINES, D., LAPRADE, R. AND SCHWARTZ, J. L. (1997). Interaction between calcium ions and Bacillus thuringiensis toxin activity against Sf9 cells (Spodoptera frugiperda, Lepidoptera). Appl. env. Microbiol. 63, 440-447.
31. MONETTE, R., SAVARIA, D., MASSON, L., BROUSSEAU, R. AND SCHWARTZ, J. L. (1994). Calcium-activated potassium channels in the UCR-SE-1a lepidopteran cell line from the beet armyworm (Spodoptera exigua). J. Insect Physiol. 40, 273-282.
32. MORRIS, O. N., TROTTIER, M., MCLAUGHLIN, N. B. AND CONVERSE, V. (1994). Interaction of caffeine and related compounds with Bacillus thuringiensis ssp. kurstaki in Bertha armyworm (Lepidoptera: Noctuidae). J. econ. Ent. 87, 610-617.
33. ORR, G. L., GOLE, J. W. D., GUPTA, J. AND DOWNER, R. G. H. (1988). Modulation of octopamine-mediated production of cyclic AMP by phorbol-ester-sensitive protein kinase C in an insect cell line. Biochim. biophys. Acta 970, 324-332.
34. PEYRONNET, O., VACHON, V., BROUSSEAU, R., BAINES, D., SCHWARTZ, J. L. AND LAPRADE, R. (1997). Effect of Bacillus thuringiensis toxins on the membrane potential of lepidopteran insect midgut cells. Appl. env. Microbiol. 63, 1679-1684.
35. RASMUSSEN, H. AND BARRETT, P. Q. (1984). Calcium messenger system: an integrated view. Physiol. Rev. 64, 938-984.
36. +-gradient-dependent amino acid transport across the brush border membrane of Pieris brassicae midgut cells. FEBS Lett. 204, 213-218.
37. SCHWARTZ, J. L., GARNEAU, L., MASSON, L. AND BROUSSEAU, R. (1991). Early response of cultured lepidopteran cells to exposure to δ-endotoxin from Bacillus thuringiensis: involvement of calcium and anionic channels. Biochim. biophys. Acta 1065, 250-260.
38. SCHWARTZ, J. L., GARNEAU, L., SAVARIA, D., MASSON, L. AND BROUSSEAU, R. (1993). Lepidopteran-specific crystal toxins from Bacillus thuringiensis form cation- and anion-selective channels in planar lipid bilayers. J. Membr. Biol. 132, 53-62.
39. SCHWARTZ, J. L., LU, Y.-J., SÖHNLEIN, P., BROUSSEAU R., LAPRADE R., MASSON, L. AND ADANG, M. J. (1997). Ion channels formed in planar lipid bilayers by Bacillus thuringiensis toxins in the presence of Manduca sexta midgut receptors. FEBS Lett. 412, 270-276.
40. SHIBUYA, I. AND DOUGLAS, W. W. (1992). Calcium channels in rat melanotrophs are permeable to manganese, cobalt, cadmium and lanthanum, but not to nickel: evidence provided by fluorescence changes in Fura-2-loaded cells. Endocrinology 131, 1936-1941.
41. SLATIN, S. L., ABRAMS, C. K. AND ENGLISH, L. (1990). Delta-endotoxins form cation-selective channels in planar lipid bilayers. Biochem. biophys. Res. Commun. 169, 765-772.
42. TABASHNIK, B. E. (1994). Evolution of resistance to Bacillus thuringiensis. A. Rev. Ent. 39, 47-79.
43. 2+-ATPase. Proc. natn. Acad. Sci. U.S.A. 87, 2466-2470.
44. TRIGGLE, D. J. (1990). Calcium, calcium channels and calcium channel antagonists. Can. J. Physiol. Pharmac. 68, 1474-1481.
45. TSIEN, R. W. (1990). Calcium channels, stores and oscillations. A. Rev. Cell Biol. 6, 715-760.
46. UEMURA, T., IHARA, H., WADANO, A. AND HIMENO, M. (1992). Fluorometric assay of potential change of Bombyx mori midgut brush border membrane induced by δ-endotoxin from Bacillus thuringiensis. Biosci. Biotech. Biochem. 56, 1976-1979.
47. + exchange activity in the Sf9 insect cell line. Biochemistry 34, 15157-15164.
48. VACHON, V., PARADIS, M. J., MARSOLAIS, M., SCHWARTZ, J. L. AND LAPRADE, R. (1995b). Ionic permeabilities induced by Bacillus thuringiensis in Sf9 cells. J. Membr. Biol. 148, 57-63.
49. VAN FRANKENHUYZEN, K., GRINGORTEN, J. L., GAUTHIER, D., MILNE, R. E., MASSON, L. AND PEFEROEN, M. (1993). Toxicity of activated CryI proteins from Bacillus thuringiensis to six forest Lepidoptera and Bombyx mori. J. Invert. Path. 62, 295-301.
50. VAN FRANKENHUYZEN, K., GRINGORTEN, J. L., MILNE, R. E., GAUTHIER, D., PUSZTAI-CAREY, M., BROUSSEAU, R. AND MASSON, L. (1991). Specificity of activated CryIA proteins from Bacillus thuringiensis subsp. kurstaki HD-1 for defoliating forest Lepidoptera. Appl. env. Microbiol. 57, 1650-1655.
51. VILLALON, M., VACHON, V., BROUSSEAU, R., SCHWARTZ, J. L. AND LAPRADE, R. (1997). Video imaging analysis of the plasma membrane permeabilizing effects of Bacillus thuringiensis insecticidal toxins in Sf9 cells. Biochim. biophys. Acta 1368, 27-34.
52. VON TERSCHE, M. A., SLATIN, S. L., KULESZA, C. A. AND ENGLISH, L. H. (1994). Membrane-permeabilizing activities of Bacillus thuringiensis coleopteran-active toxin CryIIIB2 and CryIIIB2 domain I peptide. Appl. env. Microbiol. 60, 3711-3717.
53. WOLFERSBERGER, M. G. (1989). Neither barium nor calcium prevents the inhibition by Bacillus thuringiensis δ-endotoxin of sodium-or potassium gradient-dependent amino acid accumulation by tobacco hornworm midgut brush border membrane vesicles. Archs Insect Biochem. Physiol. 12, 267-277.
54. YUNOVITZ, H. AND YAWETZ, A. (1988). Interaction between the δ-endotoxin produced by Bacillus thuringiensis ssp. entomocidus and liposomes. Eur. J. Biochem. 230, 105-108.