Cytotoxicity Analysis of Three Bacillus thuringiensis Subsp. israelensis δ-Endotoxins towards Insect and Mammalian Cells

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Teixeira Corrêa, Roberto Franco ^a   Ardisson Araújo, Daniel Mendes Pereira ^a   Monnerat, Rose Gomes ^b   Ribeiro, Bergmann Morais ^a  

^a UNIVERSITY OF BRASILIA   (Brazil)

^b EMBRAPA RECURSOS GENÉTICOS E BIOTECNOLOGIA   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLUS THURINGIENSIS TOXIN; CRY11A TOXIN; CRY2BA TOXIN; CRY4AA TOXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACILLUS ISRAELENSIS; BACILLUS THURINGIENSIS; BACTERIAL STRAIN; CELL STRAIN MCF 7; CONTROLLED STUDY; CRY11A GENE; CRY2BA GENE; CRY4AA GENE; CYTOTOXICITY; DIPTERA; HUMAN; HUMAN CELL; IN VITRO STUDY; INSECT CELL; INSECT CELL CULTURE; LARVA; LEPIDOPTERA; MAMMAL CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN EXPRESSION; PROTEIN PURIFICATION; STOMACH JUICE; TOXICITY TESTING;

ANIMALS; BACILLUS THURINGIENSIS; BACTERIAL PROTEINS; CELL LINE; CELL LINE, TUMOR; CELL SURVIVAL; CLONING, MOLECULAR; DIPTERA; ENDOTOXINS; GENE EXPRESSION; HUMANS; LEPIDOPTERA;

BACILLUS THURINGIENSIS; BACILLUS THURINGIENSIS SEROVAR ISRAELENSIS; HEXAPODA; MAMMALIA; SPODOPTERA FRUGIPERDA;

EID: 84866714160     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046121     Document Type: Article

References (57)

1. Estruch JJ, Carozzi NB, Desai N, Duck NB, Warren GW, et al. (1997) Transgenic plants: an emerging approach to pest control. Nat Biotechnol 15: 137-141.
2. WHO (1996) Chapter 1: The state of world health. Insect-borne diseases. In The world health report 1996-Fighting Disease, Fostering Development. Geneva, Switzerland: WHO 46-56.
3. Cook RJ, (1993) Making greater use of introduced microorganisms for biological control of plant pathogens. Ann Rev Phytopathol 31: 53-80.
4. Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, et al. (1998) Bacillus thuringiensis and pesticidal crystal proteins. Microbiol Mol Biol Rev 62: 775-806.
5. Bravo A, Gill SS, Soberon M, (2007) Mode of action of Bacillus thuringiensis Cry and Cyt toxins and their potential for insect control. Toxicon Rev 49: 423-35.
6. Crickmore N, (2005) Beyond the spore - past and future developments of Bacillus thuringiensis as a biopesticide. J Appl Microbiol 101: 616-619.
7. de Maagd RA, Bravo A, Berry C, Crickmore N, (2001) How Bacillus thuringiensis has evolved specific toxins to colonize the insect world. Trends Genet 17: 193-199.
8. Li J, Koni PA, Ellar DJ, (1996) Structure of the mosquitocidal d-endotoxin CytB from Bacillus thuringiensis sp. kyushuensis and implications for membrane pore formation. J Mol Biol 257: 129-152.
9. Butko P, (2003) Cytolytic toxin Cyt1A and its mechanism of membrane damage: data and hypotheses. Appl Environ Microbiol 69: 2415-2422.
10. Terra W, Ferreira C, (1994) Insect digestive enzymes: properties, compartmentalization and function. Comp Biochem Physiol 109B: 1-62.
11. Chang C, Yu YM, Dai SM, Law SK, Gill SS, (1993) High-level cryIVD and cytA gene expression in Bacillus thuringiensis does not require the 20-kilodalton protein, and the coexpressed gene products are synergistic in their toxicity to mosquitoes. Appl Environ Microbiol 59: 815-821.
12. Thomas WE, Ellar DJ, (1983) Bacillus thuringiensis var. israelensis crystal endotoxin: Effects on insect and mammalian cells in vitro and in vivo. J Cell Sci 60: 181-197.
13. Knowles BH, White PJ, Nicholls CN, Ellar DJ, (1992) A broad-spectrum cytolytic toxin from Bacillus thuringiensis var. kyushuensis. Proc R Soc 248: 1-7.
14. Gill SS, Cowles GJ, Pietrantonio PV, (1992) The mode of action of Bacillus thuringiensis endotoxins. Annu Rev Entomol 37: 615-636.
15. Mizuki E, Ohba M, Akao T, Yamashita H, Saitoh, et al, (1999) Unique activity associated with non-insecticidal Bacillus thuringiensis parasporal inclusions: in vitro cell-killing action on human cancer cells. J Appl Microbiol 86: 477-486.
16. Wirth MC, Park HW, Walton WE, Federici BA, (2005) Cyt1A of Bacillus thuringiensis delays evolution of resistence to Cry11A in the mosquito Culex quinquefasciatus Appl Env Microbiol. 71: 185-189.
17. Pérez C, Fernandez LE, Sun J, Folch JL, Gill SS, et al. (2005) Bacillus thuringiensis subsp. israelensis Cyt1Aa synergizes Cry11Aa toxin by functioning as a membrane-bound receptor. PNAS 102: 18303-18308.
18. Beltrão HBM, Silva-Filha MHN, (2007) Interaction of Bacillus thuringiensis var. israelensis Cry toxins with binding sites from Aedes aegypti (Diptera: Culicidae) larvae midgut. FEMS Microbiol Lett 266: 163-169.
19. Berry C, ÓNeil S, Bem-Dov E, Jones AF, Murphy L, et al. (2002) Complete sequence and organization of pBtoxis, the toxin-coding plasmid of Bacillus thuringiensis subsp. israelensis. Appl Environ Microbiol 68: 5082-5095.
20. Guerchicoff A, Ugalde RA, Rubinstein CP, (1997) Identification and chacterization of a previously undescribed cyt gene in bacillus thuringiensis subsp. israelensis Appl Environ Microbiol 63: 2716-2721.
21. Ward ES, Ellar DJ, (1987) Nucleotide sequence of a Bacillus thuringiensis var. israelensis gene encoding a 130 kDa delta-endotoxin. Nucl Ac Res 15: 7195.
22. Xu Y, Nagai M, Bagdasarian M, Smith TW, Walker ED, (2001) Expression of the p20 gene from Bacillus thuringiensis H-14 increases Cry11A toxin production and enhances mosquito larvicidal activity in recombinant gram-negative bacteria. Appl Environ Microbiol 67: 3010-3015.
23. Höfte H, Whiteley HR, (1989) Insecticidal crystal protein of Bacillus thuringiensis. Microbiol Rev 53: 242-255.
24. Angsuthanasombat C, Uawithya P, Leetachewa S, Pornwiroon W, Ounjai P, et al. (2004) Bacillus thuringiensis Cry4Aa and Cry4Ba mosquito-larvicidal proteins: Homology-based 3D model and implications for toxin activity. J Biochem Mol Biol 37: 304-313.
25. Yamagiwa M, Sakagawa K, Sakai H, (2004) Functional analysis of two processed fragments of Bacillus thuringiensis Cry11A toxin. Biosci Biotechnol Biochem 68: 523-528.
26. Chilcott CN, Ellar DJ, (1988) Comparative toxicity of Bacillus thuringiensis var. israelensis crystal proteins in vivo and in vitro. J Gen Microbiol 134: 2551-2558.
27. Gringorten JL, Sohi SS, Masson L, (1999) Activity spectra of Bacillus thuringiensis δ-endotoxins against eight insect cell lines in vitro. Cell Dev Biol 35: 299-303.
28. Sauka DH, Sánchez J, Bravo A, Benintende GB, (2007) Toxicity of Bacillus thuringiensis δ-endotoxins against bean shoot borer (Epinotia aporema Wals.) larvae, a major soybean pest in Argentina. J Invertebr Pathol 94: 125-129.
29. Tabashnik BE, (1992) Evaluation of synergism among Bacillus thuringiensis toxins. Appl Environ Microbiol 58: 3343-3346.
30. Poncet S, Delécluse A, Klier A, Rapoport G, (1995) Evaluation of synergistic interactions among the CryIVA, CryIVB and CryIVD toxic components of B. thuringiensis subsp. israelensis crystals. J Invertebr Pathol 66: 131-135.
31. Promdonkoy B, Chewawiwat N, Tanapongpipat S, Luxananil P, Panyim S, (2003) Cloning and characterization of a cytolitic and mosquitocidal δ-endotoxin from B. thuringiensis subsp. darmistadiensis. Curr Microbiol 46: 94-98.
32. Cheong H, Gill SS, (1997) Cloning and characterization of a cytolytic and mosquitocidal δ-endotoxin from B. thuringiensis subsp. jegathesan. Appl Environ Microbiol 63: 3254-3260.
33. Wirth MC, Georghiou GP, Federici BA, (1997) CytA enables CryIV endotoxins of Bacillus thuringiensis to overcome high levels of CryIV resistance in the mosquito, Culex quinquefasciatus. Proc Natl Acad Sci USA 94: 10536-10540.
34. Hughes PA, Stevens MM, Park HW, Federici BA, (2005) Response of larval Chironomus tepperi (Diptera: Chironomidae) to individual Bacillus thuringiensis var. israelensis toxins and toxin mixtures. J Invertebr Pathol 88: 34-39.
35. Carmona D, Rodríguez-Almazán C, Portugal L, Pérez C, et al. (2011) Dominant negative phenotype of Bacillus thuringiensis Cry1Ab, Cry11Aa and Cry4Ba mutants suggest hetero-oligomer formation among different Cry toxins. PloS One 6(5): e19952.
36. Uawithya P, Tuntitppawan T, Katzenmeier G, Panyim S, Angsuthanasombat C, (1998) Effects on larvicidal activity of single proline substitutions in alpha 3 or alpha 4 of the Bacillus thuringiensis Cry4B toxin. Biochem Mol Int 44: 825-832.
37. Gerber D, Shay Y, (2000) Insertion and organization within membranes of the delta-endotoxin pore-forming domain, helix 4-loop-helix 5, and inhibition of its activity by a mutant helix 4 peptide. J Biol Chem 275: 23602-23607.
38. Christeller JT, Laing WA, Shaw BP, Burguess EPJ, (1990) Characterization and partial purification of the digestive protease of the black field cricket Teleogryflus commodus (Walker): elastase is a major component. Insect Biochem 20: 157-164.
39. Rausell C, Garcia-Robles I, Sanchez J, Muñoz-Garay C, Martinez-Ramirez AC, et al. (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 166: 99-105.
40. Pootanakit K, Angsuthanasombat C, Panyim (2003) Identification of two isoforms of aminopeptidase N in Aedes aegypti larval midgut. J Biochem Mol Biol 36: 508-513.
41. Mizuki E, Ohba M, Akao T, Yamashita H, Saitoh, et al, (1999) Unique activity associated with non-insecticidal Bacillus thuringiensis parasporal inclusions: in vitro cell-killing action on human cancer cells. J Appl Microbiol 86: 477-486.
42. Mizuki E, Park YS, Saitoh H, Yamashita S, Akao T, et al. (2000) Parasporin, a human leukemic cell-recognizing parasporal protein of Bacillus thuringiensis. Clin Diagn Lab Immunol 7: 625-634.
43. Ohba M, Mizuki E, Uemori A, (2009) Parasporin, a new anticancer protein group from Bacillus thuringiensis. Anticanc Res 29: 427-434.
44. Vaughn JL, Goowin RH, Tompkins GJ, McCawley P, (1977) The establishment of two cell lines from insect Spodoptera frugiperda (Lepidoptera: Noctuidae). In Vitro 13: 213-217.
45. McClintock T, Dougherty EE, Weiner RM, (1986) Semipermissive replication of a polihedrosis virus of Autographa californica in a gypsy moth cell line. J Virol 57: 197-204.
46. Grace TD, (1967) Establishment of a line of cells from the silkworm Bombyx mori. Nature London 216: 613.
47. Igarashi A, (1978) Isolation of Singhs Aedes albopictus cell clone sensitive to dengue and chinkugunya viruses. J Gen Vir 40: 531-544.
48. Soule HD, Vazquez J, Long A, Albert S, Brennan M, (1973) A human cell line from a pleural effusion derived from a breast carcinoma. J Nat Can Ins 51: 1409-1416.
49. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 3° ed. Cold Spring Harbor, New York.
50. Crickmore N, Nicholls C, Earp DJ, Hodman C, Ellar DJ, (1990) The construction of Bacillus thuringiensis strains expressing novel entomocidal δ-endotoxins combinations. J Biochem 270: 133-136.
51. Crickmore N, Ellar DJ, (1992) Comparison of Bacillus thuringiensis subsp. israelensis CryIVA and CryIVB cloned toxins reveals synergism in vivo. FEMS Microbiol Lett 94: 63-68.
52. Peng D, Luo Y, Guo S, Zeng H, Ju S, et al. (2009) Elaboration of an electroporation protocol for large plasmids and wild-type strains of Bacillus thuringiensis. J Appl Microbiol 106: 1849-1858.
53. Yousten AA, (1984) Bacillus sphaericus: Microbiological factors related to its potential as a mosquitocidal larvicide. Adv In Biotechnol Proc 3: 315-343.
54. Bravo A, Arrieta G, Benintende G, Real MD, Espinoza AM, et al. (2001) Metodologias utilizadas en investigacíon sobre bactérias entomopatógenas, Unam, México.
55. Vilchez S, Jacoby J, Ellar DJ, (2004) Display of biological functional insecticidal toxin on the surface of lambda phage. Appl Env Microbiol 70: 6587-6594.
56. Ben-Dov E, Boussiba S, Zaritsky A, (1995) Mosquito larvicidal activity of Escherichia coli with combinations of genes from Bacillus thuringiensis subsp. israelensis. J Bacteriol 177: 2851-2857.
57. Finney DJ (1971) Probit analysis, third ed. Cambridge: Cambridge University Press.