A Bacillus thuringiensis δ-endotoxin induces programmed cell death in mosquito larvae

Cell Death and Differentiation

Volumn 4, Issue 7, 1997, Pages 560-569

  Smouse, David ^a   Nishiura, James ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

Apoptosis; Endotoxin; Mosquito; Thuringiensis

Indexed keywords

EID: 0000772773     PISSN: 13509047     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.cdd.4400277     Document Type: Article

References (53)

1. Abrams JM, White K, Fessler LI and Steller H (1993) Programmed cell death during Drosophila embryogenesis. Development 177: 29-43
2. Bayer EA and Wilchek M (1990) Protein biotinylation. Meth. Enzymol. 184: 138-159
3. Berke G (1995) The CTL's kiss of death. Cell 81: 9-12
4. Charles j-F and de Barjac H (1983) Action des cristaux de Bacillus thuringiensis var. israelensis sur l'intes moyen des larves de Aedes aegypti L., en microscope electronique. Ann. Microbiol. Inst. Pasteur 134A: 197-218
5. Chen P, Nordstrom W, Gish B and Abrams JM (1996) grim, a novel cell death gene in Drosophila. Genes Dev. 10: 1773-1782
6. Clements AN (1992) The Biology of Mosquitoes: development, nutrition and reproduction. (London: Chapman and Hall)
7. Curtiss A, Alcantara E, Dean DH and Chen XJ (1995) Mutations in domain I of Bacillus thuringiensis delta-endotoxin CrylAb reduce the irreversible binding of toxin to Manduca sexta brush border membrane vesicles. J. Biol. Chem. 270: 6412-6419
8. Duckett CS, Nava VE, Gedrich RW, Clem RJ, Van Dongen JL, Gilfillan MC, Shiels H, Hardwick JM and Thompson CB (1996) A conserved family of cellular genes related to the baculovirus iap gene and encoding apoptosis inhibitors. EMBO J. 15: 2685-2694
9. de Barjac H (1978) Etude cytologique de l'action de Bacillus thuringiensis var israelensis sur larves de Moustiques. C.R. Acad. Sc. 286 Serie D: 1629-1632
10. 2+associated with apoptosis. In Methods in Cell Biology, vol 46, LM Schwartz and BA Osborne, eds. (San Diego: Academic Press) pp. 41-56
11. Elus RE, Yuan JY and Hortitz HR (1991) Mechanisms and functions of cell death. Annu. Rev. Cell Biol. 7: 663-698
12. Ferré J, Real MD, van Rie J, Jansens S and Peferoen M (1991) Resistance to the Bacillus thuringiensis bioinsecticide in a field population of Plutella xylostella is due to a change in a midgut membrane receptor. Proc. Natl. Acad. Sci. USA 88: 5119-5123
13. Gill SS, Cowles EA and Francis V (1995) Identification, Isolation, and Cloning of a Bacillus thuringiensis CrylAc Toxin-binding Protein from the Midgut of the Lepidopteran Insect Heliothis virescens. J. Biol. Chem. 270: 27277-27282
14. Gill SS, Cowles EA and Paietrantinio PV (1992) The mode of action of Bacillus thuringiensis endotoxins. Annu. Rev. Entomol. 47: 615-636
15. Gravrieli Y, Sherman Yand Ben-Sasson SA (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119: 493-501
16. Grether ME, Abrams JM, Agapite J, White K and Steller H (1995) The head involution defective gene of Drosophila melanogaster functions in programmed cell death. Genes and Dev. 9: 1694-1708
17. Haider MZ, Knowles BH and Ellar DJ (1986) Specificity of Bacillus thuringiensis var. colmeri insecticidal delta-endotoxin is determined by differential proteolytic processing of the protoxin by larval gut proteases. Eur. J. Biochem. 156: 531-540
18. Hay BA, Wassarman DA and Rubin GM (1995) Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 83: 1253-1262
19. Hofmann C, Vanderbruggen H, Höfte H, van Rie J, Jansens S and Van Mellaert H (1988) Specificity of Bacillus thuringiensis delta-endotoxins is correlated with the presence of high-affinity binding sites in the brush border membrane of target insect midguts. Proc. Natl. Acad. Sci. 85: 7844-7848
20. Hofmann C, Luthy P, Hutter R and Pliska V (1988) Binding of the delta endotoxin from Bacillus thuringiensis to brush-border membrane vesicles of the cabbage butterfly (Pieris brassicae). Eur. J. Biochem. 173: 85-91
21. Höfte H and Whitely HR (1989) Insecticidal crystal proteins of Bacillus thuringiensis. Microbiol. Rev. 53: 242-255
22. Knight PJ, Knowles BH and Ellar DJ (1995) Molecular cloning of an insect aminopeptidase N that serves as a receptor for Bacillus thuringiensis CrylA(c) toxin. J. Biol. Chem. 270: 17765-17770
23. Knight PJ, Crickmore N and Ellar DJ (1994) The receptor for Bacillus thuringiensis CrylA(c) delta-endotoxin in the brush border membrane of the lepidopteran Manduca sexta is aminopeptidase N. Mol. Microbiol. 11: 429-436
24. Knowles BH and Ellar DJ (1984) Colloid-osmotic lysis is a general feature of the mechanism of action of Bacillus thuringiensis delta endotoxin with different specificities. Biochem. Biophys. ACTA 924: 509-518
25. MacIntosh SC, Stone TB, Jokers TRS and Fuchs RL (1991) Binding of Bacillus thuringiensis proteins to a laboratory-selected line of Heliothis virescens. Proc. Natl. Acad. Sci. 88: 8930-8933
26. Martin SJ and Green DR (1995) Protease activation during apoptosis: death by a thousand cuts. Cell 82: 349-352
27. Masson L, Mazza A, Brousseau R and Tabashnik B (1995) Kinetics of Bacillus thuringiensis toxin binding with brushborder membrane vesicles from susceptible and resistant larvae of Plutella xylostella. J. Biol. Chem. 270: 11887-11896
28. Masson L, Lu YU, Mazza A, Brousseau R and Adang MJ (1995) The CrylA(c) receptor purified from Manduca sexta displays multiple specificities. J. Biol. Chem. 270: 20309-20315
29. McGaughey WH and Whalon ME (1992) Managing insect resistance to Bacillus thuringiensis toxins. Science 258: 1451-1455
30. Muthukuma RG and Nickerson KW (1987) The glycoprotein toxin of Bacillus thuringiensis ssp israelensis indicates a lectin-like receptor in the larval mosquito gut. Appl. Environ. Microbiol. 53: 2550-2655
31. O'Brien JF (1965) Development of the Muscular Network of the Midgut in the larval stages of the Mosquito, Ades Aegypti Linnaeus. New York Entomological Society LXXIII: 226-231
32. O'Brien JF (1966) Origin and structural function of the basal gells of the larval midgut in the mosquito, Aedes aegypti Linnaeus. New York Entomological Society LXXIV: 59-63
33. Oppert B, Kramer KJ, Johnson DE, MacIntosh SC and McGaughey WH (1994) Altered protoxin activation by midgut enzymes from a thuringiensis resistant strain of Plodia interpunctella. Biochem. Biophys. Res. Commun. 198: 940-947
34. Pronk GJ, Ramer K, Amiri P and Williams LT (1996) Requirement of an ICE-like proteases for induction of apoptosis and ceramide generation by REAPER. Science 271: 808-810
35. Raff MA (1992) Social controls on cell survival and cell death. Nature 356: 397-400
36. Ravoahangimalala O and Charles J-F (1995) In vitro binding of Bacillus thuringiensis var. israelensis individual toxins to midgut cells of Anopheles gambiae larvae (Diptera: Culicidae). FEBS Letters 362: 111-115
37. Richins CA (1945) The development of the midgut in the larva of Aedes dorssalis Meigen. Annals Entomological Society of America XXXVIII: 314-320
38. Robinow S, Talbot WS, Hogness DS and Truman JW (1993) Programmed cell death in the Drosophila CNS is ecdysone-regulated and coupled with a specific ecdysone receptor isoform. Development 119: 1251-1259
39. Sacchi VF, Parenti P, Hanozet GM, Giordana B, Luthy P and Wolfersberger MG (1986) Bacillus thuringiensis toxin inhibits K+-gradient-dependent amino acid transport across the brush borer membrane of Pieris brassicae midgut cells. FEBS Lett. 204: 213-218
40. Sanchis V, Chaufaux J and Pauron D (1994) A comparison and analysis of the toxicity and receptor binding properties of Bacillus thuringiensis CrylC delta-endotoxin on Spodoptera littoralis and Bombyx mon. FEBS Lett. 353: 259-263
41. Schwartz LM, Kosz L and Kay BK (1990) Gene activation is required for developmentally programmed cell death. Proc. Natl. Acad. Sci. 87: 6594-6598
42. Steller H (1995) Mechanism and genes of cellular suicide. Science 267: 1445-1449
43. Tabashnik BE (1994) Evolution of resistance to Bacillus thuringiensis. Annu. Rev. Entomol. 39: 47-79
44. Thompson CB (1995) Apoptosis in the pathogenesis and treatment of disease. Science 267: 1456-1452
45. Vadlamudi RK, Weber E, Ji I, Ji TH and Bulla LAJ (1995) Cloning and expression of a receptor for an insecticidal toxin of Bacillus thuringiensis. J. Biol. Chem. 270: 5490-5494
46. van Rie J, Jansens S, Höfte H, Degheele D and van Mellaert H (1989) Specificity of Bacillus thuringiensis delta-endotoxins. Importance of specific receptors on the brush border membrane of the mid-gut of target insects. Eur. J. Biochem. 186: 239-247
47. van Rie J, McGaughey WH, Johnson DE, Barnett BD and van Mellaert H (1990) Mechanism of insect resistance to the microbial insecticide Bacillus thuringiensis. Science 247: 72-74
48. Villa M, Hanozet GM, Tasca M, Giordana B and Parenti P (1995) Interaction of the insecticidal crystal protein CrylA from Bacillus thuringiensis with amino acid transport into brush border membranes from Bombyx mori larval midgut. J. Invertebr. Pathol. 65: 35-42
49. Von Tersch MA, Slatin SL, Kulesza CA and English LH (1994) Membrane-permeabilizing activities of Bacillus thuringiensis coleopteran-active toxin CrylllB2 and CrylllB2 domain I peptide. Appl. Environ. Microbiol. 60: 3711-3717
50. White K, Grether ME, Abrams JM, Young L, Farrell K and Steller H (1994) Genetic control of programmed cell death in Drosophila. Science 264: 677-683
51. White K, Tahaoglu E and Steller H (1996) Cell killing by the Drosophila gene reaper. Science 271: 805-807
52. Wyllie AH, Kerr JFR and Currie AR (1980) Cell death: the significance of apoptosis. Int. Rev. Cytol. 68: 251-306
53. Zakeri Z and Lockshin RA (1994) The Aging Clock. In (Pieraoli W, Regelson W, and Fabris N, Eds.), pp. 212-229