Bacillus sphaericus binary toxin elicits host cell autophagy as a response to intoxication

PLoS ONE

Volumn 6, Issue 2, 2011, Pages

  Opota, Onya ^a   Gauthier, Nils C ^b   Doye, Anne ^b   Berry, Colin ^c   Gounon, Pierre ^d   Lemichez, Emmanuel ^b   Pauron, David ^a  

^a UMR Interactions Biotiques et Sante Vegetale France

^b CENTRE MÉDITERRANÉEN DE MÉDECINE MOLÉCULAIRE C3M   (France)

^c CARDIFF UNIVERSITY   (United Kingdom)

^d Universite Co te d'Azur Parc Valrose   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; ALPHA GLUCOSIDASE; BINB PROTEIN, BACILLUS SPHAERICUS; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN;

ARTICLE; AUTOPHAGY; BACILLUS SPHAERICUS; CELL ASSAY; CELL MEDIATED CYTOTOXICITY; CELL MIGRATION; CELL PROTECTION; CELL STIMULATION; CELL VACUOLE; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; HOST CELL; INTRACELLULAR TRANSPORT; LYSOSOME; NONHUMAN; ANIMAL; ANOPHELES GAMBIAE; BACILLACEAE INFECTION; BACILLUS; CELL CULTURE; CULEX; DOG; DRUG EFFECT; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; PATHOLOGY; PHAGOSOME; PHYSIOLOGY;

ANOPHELES (GENUS); BACILLUS SPHAERICUS; CULEX PIPIENS; MAMMALIA;

ALPHA-GLUCOSIDASES; ANIMALS; ANOPHELES GAMBIAE; AUTOPHAGY; BACILLACEAE INFECTIONS; BACILLUS; BACTERIAL TOXINS; CELLS, CULTURED; CULEX; DOGS; GREEN FLUORESCENT PROTEINS; HOST-PATHOGEN INTERACTIONS; PHAGOSOMES; RECOMBINANT FUSION PROTEINS; TRANSFECTION; VACUOLES;

EID: 79952032608     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0014682     Document Type: Article

References (50)

1. de Maagd RA, Bravo A, Berry C, Crickmore N, Schnepf HE, (2003) Structure, diversity, and evolution of protein toxins from spore-forming entomopathogenic bacteria. Annu Rev Genet 37: 409-433.
2. Schnepf E, Crickmore N, Van Rie J, Lereclus D, Baum J, et al. (1998) Bacillus thuringiensis and its pesticidal crystal proteins. Microbiol Mol Biol Rev 62: 775-806.
3. Charles JF, Darboux I, Pauron D, Nielsen-Leroux C, (2005) Mosquitocidal Bacillus sphaericus: toxins, genetics, mode of action, use, and resistance mechanisms. In: Gilbert KIaSG LI, editors. Elsevier Pergamon pp. 207-231.
4. Darboux I, Nielsen-LeRoux C, Charles JF, Pauron D, (2001) The receptor of Bacillus sphaericus binary toxin in Culex pipiens (Diptera: Culicidae) midgut: molecular cloning and expression. Insect Biochem Mol Biol 31: 981-990.
5. Darboux I, Pauchet Y, Castella C, Silva-Filha MH, Nielsen-LeRoux C, et al. (2002) Loss of the membrane anchor of the target receptor is a mechanism of bioinsecticide resistance. Proc Natl Acad Sci U S A 99: 5830-5835.
6. Opota O, Charles JF, Warot S, Pauron D, Darboux I, (2007) Identification and characterization of the receptor for the Bacillus sphaericus binary toxin in the malaria vector mosquito, Anopheles gambiae. Comp Biochem Physiol B Biochem Mol Biol.
7. Silva-Filha MH, Nielsen-LeRoux C, Charles JF, (1999) Identification of the receptor for Bacillus sphaericus crystal toxin in the brush border membrane of the mosquito Culex pipiens (Diptera: Culicidae). Insect Biochem Mol Biol 29: 711-721.
8. Charles JF, Nielson-LeRoux C, Delecluse A, (1996) Bacillus sphaericus toxins: molecular biology and mode of action. Annu Rev Entomol 41: 451-472.
9. Barth H, Aktories K, Popoff MR, Stiles BG, (2004) Binary bacterial toxins: biochemistry, biology, and applications of common Clostridium and Bacillus proteins. Microbiol Mol Biol Rev 68: 373-402, table of contents.
10. Schwartz JL, Potvin L, Coux F, Charles JF, Berry C, et al. (2001) Permeabilization of model lipid membranes by Bacillus sphaericus mosquitocidal binary toxin and its individual components. J Membr Biol 184: 171-183.
11. Cokmus C, Davidson EW, Cooper K, (1997) Electrophysiological effects of Bacillus sphaericus binary toxin on cultured mosquito cells. J Invertebr Pathol 69: 197-204.
12. Pauchet Y, Luton F, Castella C, Charles JF, Romey G, et al. (2005) Effects of a mosquitocidal toxin on a mammalian epithelial cell line expressing its target receptor. Cell Microbiol 7: 1335-1344.
13. Gonzalez MR, Bischofberger M, Pernot L, van der Goot FG, Freche B, (2008) Bacterial pore-forming toxins: the (w)hole story? Cell Mol Life Sci 65: 493-507.
14. Soberon M, Fernandez LE, Perez C, Gill SS, Bravo A, (2007) Mode of action of mosquitocidal Bacillus thuringiensis toxins. Toxicon 49: 597-600.
15. Charles JF, (1987) Ultrastructural midgut events in Culicidae larvae fed with Bacillus sphaericus 2297 spore/crystal complex. Ann Inst Pasteur Microbiol 138: 471-484.
16. Silva-Filha MH, Peixoto CA, (2003) Immunocytochemical localization of the Bacillus sphaericus binary toxin components in Culex quinquefasciatus (Diptera: Culicidae) larvae midgut. Pesticide Biochem Physiol 77: 138-146.
17. Narasu ML, Gopinathan KP, (1988) Effect of Bacillus sphaericus 1593 toxin on choline acetyl transferase and mitochondrial oxidative activities of the mosquito larvae. Indian J Biochem Biophys 25: 253-256.
18. Liou W, Geuze HJ, Geelen MJ, Slot JW, (1997) The autophagic and endocytic pathways converge at the nascent autophagic vacuoles. J Cell Biol 136: 61-70.
19. Mizushima N, Levine B, Cuervo AM, Klionsky DJ, (2008) Autophagy fights disease through cellular self-digestion. Nature 451: 1069-1075.
20. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, et al. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. Embo J 19: 5720-5728.
21. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, et al. (1999) Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402: 672-676.
22. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y, (2004) In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 15: 1101-1111.
23. Kneen M, Farinas J, Li Y, Verkman AS, (1998) Green fluorescent protein as a noninvasive intracellular pH indicator. Biophys J 74: 1591-1599.
24. Tanida I, Minematsu-Ikeguchi N, Ueno T, Kominami E, (2005) Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 1: 84-91.
25. Corcelle E, Nebout M, Bekri S, Gauthier N, Hofman P, et al. (2006) Disruption of autophagy at the maturation step by the carcinogen lindane is associated with the sustained mitogen-activated protein kinase/extracellular signal-regulated kinase activity. Cancer Res 66: 6861-6870.
26. Klionsky DJ, Emr SD, (2000) Autophagy as a regulated pathway of cellular degradation. Science 290: 1717-1721.
27. Mizushima N, (2004) Methods for monitoring autophagy. Int J Biochem Cell Biol 36: 2491-2502.
28. Eskelinen EL, Prescott AR, Cooper J, Brachmann SM, Wang L, et al. (2002) Inhibition of autophagy in mitotic animal cells. Traffic 3: 878-893.
29. Gauthier NC, Monzo P, Gonzalez T, Doye A, Oldani A, et al. (2007) Early endosomes associated with dynamic F-actin structures are required for late trafficking of H. pylori VacA toxin. J Cell Biol 177: 343-354.
30. Gauthier NC, Monzo P, Kaddai V, Doye A, Ricci V, et al. (2005) Helicobacter pylori VacA cytotoxin: a probe for a clathrin-independent and Cdc42-dependent pinocytic pathway routed to late endosomes. Mol Biol Cell 16: 4852-4866.
31. Bergeland T, Widerberg J, Bakke O, Nordeng TW, (2001) Mitotic partitioning of endosomes and lysosomes. Curr Biol 11: 644-651.
32. Schweitzer JK, Burke EE, Goodson HV, D'Souza-Schorey C, (2005) Endocytosis resumes during late mitosis and is required for cytokinesis. J Biol Chem 280: 41628-41635.
33. Munafo DB, Colombo MI, (2001) A novel assay to study autophagy: regulation of autophagosome vacuole size by amino acid deprivation. J Cell Sci 114: 3619-3629.
34. Nakagawa I, Amano A, Mizushima N, Yamamoto A, Yamaguchi H, et al. (2004) Autophagy defends cells against invading group A Streptococcus. Science 306: 1037-1040.
35. Rich KA, Burkett C, Webster P, (2003) Cytoplasmic bacteria can be targets for autophagy. Cell Microbiol 5: 455-468.
36. Yano T, Mita S, Ohmori H, Oshima Y, Fujimoto Y, et al. (2008) Autophagic control of listeria through intracellular innate immune recognition in drosophila. Nat Immunol 9: 908-916.
37. Dorn BR, Dunn WA Jr, Progulske-Fox A, (2002) Bacterial interactions with the autophagic pathway. Cell Microbiol 4: 1-10.
38. Ogawa M, Yoshimori T, Suzuki T, Sagara H, Mizushima N, et al. (2005) Escape of intracellular Shigella from autophagy. Science 307: 727-731.
39. Schnaith A, Kashkar H, Leggio SA, Addicks K, Kronke M, et al. (2007) Staphylococcus aureus subvert autophagy for induction of caspase-independent host cell death. J Biol Chem 282: 2695-2706.
40. Gutierrez MG, Saka HA, Chinen I, Zoppino FC, Yoshimori T, et al. (2007) Protective role of autophagy against Vibrio cholerae cytolysin, a pore-forming toxin from V. cholerae. Proc Natl Acad Sci U S A 104: 1829-1834.
41. Terebiznik MR, Raju D, Vazquez CL, Torbricki K, Kulkarni R, et al. (2009) Effect of Helicobacter pylori's vacuolating cytotoxin on the autophagy pathway in gastric epithelial cells. Autophagy 5: 370-379.
42. Tan YK, Vu HA, Kusuma CM, Wu A, (2009) Implications of autophagy in anthrax pathogenicity. Autophagy 5: 734-735.
43. Ha SD, Ham B, Mogridge J, Saftig P, Lin S, et al. (2010) Cathepsin B-mediated autophagy flux facilitates the anthrax toxin receptor 2-mediated delivery of anthrax lethal factor into the cytoplasm. J Biol Chem 285: 2120-2129.
44. Ratner AJ, Hippe KR, Aguilar JL, Bender MH, Nelson AL, et al. (2006) Epithelial cells are sensitive detectors of bacterial pore-forming toxins. J Biol Chem 281: 12994-12998.
45. Sabharanjak S, Sharma P, Parton RG, Mayor S, (2002) GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev Cell 2: 411-423.
46. Mallard F, Antony C, Tenza D, Salamero J, Goud B, et al. (1998) Direct pathway from early/recycling endosomes to the Golgi apparatus revealed through the study of shiga toxin B-fragment transport. J Cell Biol 143: 973-990.
47. Singh GJ, Gill SS, (1988) An electron microscope study of the toxic action of Bacillus sphaericus in Culex quinquefasciatus larvae. J Invertebr Pathol 52: 237-247.
48. de Melo JV, Jones GW, Berry C, Vasconcelos RH, de Oliveira CM, et al. (2009) Cytopathological effects of Bacillus sphaericus Cry48Aa/Cry49Aa toxin on binary toxin-susceptible and-resistant Culex quinquefasciatus larvae. Appl Environ Microbiol 75: 4782-4789.
49. Oei C, Hindley J, Berry C, (1992) Binding of purified Bacillus sphaericus binary toxin and its deletion derivatives to Culex quinquefasciaBtus gut: elucidation of functional binding domains. J Gen Microbiol 138 (Pt 7): 1515-1526.
50. Gauthier NC, Ricci V, Gounon P, Doye A, Tauc M, et al. (2004) Glycosylphosphatidylinositol-anchored proteins and actin cytoskeleton modulate chloride transport by channels formed by the Helicobacter pylori vacuolating cytotoxin VacA in HeLa cells. J Biol Chem 279: 9481-9489.