Bacillus thuringiensis toxins divert progenitor cells toward enteroendocrine fate by decreasing cell adhesion with intestinal stem cells in Drosophila
subsp. ( ) is a strong pathogen toward lepidopteran larvae thanks to specific Cry toxins causing leaky gut phenotypes. Hence, and its toxins are used worldwide as microbial insecticide and in genetically modified crops, respectively, to fight crop pests. However, belongs to the group, some strains o...
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Published in | eLife Vol. 12 |
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Main Authors | , , , , , , , , |
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Language | English |
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27.02.2023
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Abstract | subsp.
(
) is a strong pathogen toward lepidopteran larvae thanks to specific Cry toxins causing leaky gut phenotypes. Hence,
and its toxins are used worldwide as microbial insecticide and in genetically modified crops, respectively, to fight crop pests. However,
belongs to the
group, some strains of which are well known human opportunistic pathogens. Therefore, ingestion of
along with food may threaten organisms not susceptible to
infection. Here we show that Cry1A toxins induce enterocyte death and intestinal stem cell (ISC) proliferation in the midgut of
, an organism non-susceptible to
. Surprisingly, a high proportion of the ISC daughter cells differentiate into enteroendocrine cells instead of their initial enterocyte destiny. We show that Cry1A toxins weaken the E-Cadherin-dependent adherens junction between the ISC and its immediate daughter progenitor, leading the latter to adopt an enteroendocrine fate. Hence, although not lethal to non-susceptible organisms, Cry toxins can interfere with conserved cell adhesion mechanisms, thereby disrupting intestinal homeostasis and endocrine functions. |
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AbstractList | Bacillus thuringiensis subsp. kurstaki (Btk) is a strong pathogen toward lepidopteran larvae thanks to specific Cry toxins causing leaky gut phenotypes. Hence, Btk and its toxins are used worldwide as microbial insecticide and in genetically modified crops, respectively, to fight crop pests. However, Btk belongs to the B. cereus group, some strains of which are well known human opportunistic pathogens. Therefore, ingestion of Btk along with food may threaten organisms not susceptible to Btk infection. Here we show that Cry1A toxins induce enterocyte death and intestinal stem cell (ISC) proliferation in the midgut of Drosophila melanogaster, an organism non-susceptible to Btk. Surprisingly, a high proportion of the ISC daughter cells differentiate into enteroendocrine cells instead of their initial enterocyte destiny. We show that Cry1A toxins weaken the E-Cadherin-dependent adherens junction between the ISC and its immediate daughter progenitor, leading the latter to adopt an enteroendocrine fate. Hence, although not lethal to non-susceptible organisms, Cry toxins can interfere with conserved cell adhesion mechanisms, thereby disrupting intestinal homeostasis and endocrine functions.Bacillus thuringiensis subsp. kurstaki (Btk) is a strong pathogen toward lepidopteran larvae thanks to specific Cry toxins causing leaky gut phenotypes. Hence, Btk and its toxins are used worldwide as microbial insecticide and in genetically modified crops, respectively, to fight crop pests. However, Btk belongs to the B. cereus group, some strains of which are well known human opportunistic pathogens. Therefore, ingestion of Btk along with food may threaten organisms not susceptible to Btk infection. Here we show that Cry1A toxins induce enterocyte death and intestinal stem cell (ISC) proliferation in the midgut of Drosophila melanogaster, an organism non-susceptible to Btk. Surprisingly, a high proportion of the ISC daughter cells differentiate into enteroendocrine cells instead of their initial enterocyte destiny. We show that Cry1A toxins weaken the E-Cadherin-dependent adherens junction between the ISC and its immediate daughter progenitor, leading the latter to adopt an enteroendocrine fate. Hence, although not lethal to non-susceptible organisms, Cry toxins can interfere with conserved cell adhesion mechanisms, thereby disrupting intestinal homeostasis and endocrine functions. Bacillus thuringiensis subsp. kurstaki ( Btk ) is a strong pathogen toward lepidopteran larvae thanks to specific Cry toxins causing leaky gut phenotypes. Hence, Btk and its toxins are used worldwide as microbial insecticide and in genetically modified crops, respectively, to fight crop pests. However, Btk belongs to the B. cereus group, some strains of which are well known human opportunistic pathogens. Therefore, ingestion of Btk along with food may threaten organisms not susceptible to Btk infection. Here we show that Cry1A toxins induce enterocyte death and intestinal stem cell (ISC) proliferation in the midgut of Drosophila melanogaster , an organism non-susceptible to Btk . Surprisingly, a high proportion of the ISC daughter cells differentiate into enteroendocrine cells instead of their initial enterocyte destiny. We show that Cry1A toxins weaken the E-Cadherin-dependent adherens junction between the ISC and its immediate daughter progenitor, leading the latter to adopt an enteroendocrine fate. Hence, although not lethal to non-susceptible organisms, Cry toxins can interfere with conserved cell adhesion mechanisms, thereby disrupting intestinal homeostasis and endocrine functions. Bacillus thuringiensis subsp. kurstaki ( Btk ) is a strong pathogen toward lepidopteran larvae thanks to specific Cry toxins causing leaky gut phenotypes. Hence, Btk and its toxins are used worldwide as microbial insecticide and in genetically modified crops, respectively, to fight crop pests. However, Btk belongs to the B. cereus group, some strains of which are well known human opportunistic pathogens. Therefore, ingestion of Btk along with food may threaten organisms not susceptible to Btk infection. Here we show that Cry1A toxins induce enterocyte death and intestinal stem cell (ISC) proliferation in the midgut of Drosophila melanogaster , an organism non-susceptible to Btk . Surprisingly, a high proportion of the ISC daughter cells differentiate into enteroendocrine cells instead of their initial enterocyte destiny. We show that Cry1A toxins weaken the E-Cadherin-dependent adherens junction between the ISC and its immediate daughter progenitor, leading the latter to adopt an enteroendocrine fate. Hence, although not lethal to non-susceptible organisms, Cry toxins can interfere with conserved cell adhesion mechanisms, thereby disrupting intestinal homeostasis and endocrine functions. subsp. ( ) is a strong pathogen toward lepidopteran larvae thanks to specific Cry toxins causing leaky gut phenotypes. Hence, and its toxins are used worldwide as microbial insecticide and in genetically modified crops, respectively, to fight crop pests. However, belongs to the group, some strains of which are well known human opportunistic pathogens. Therefore, ingestion of along with food may threaten organisms not susceptible to infection. Here we show that Cry1A toxins induce enterocyte death and intestinal stem cell (ISC) proliferation in the midgut of , an organism non-susceptible to . Surprisingly, a high proportion of the ISC daughter cells differentiate into enteroendocrine cells instead of their initial enterocyte destiny. We show that Cry1A toxins weaken the E-Cadherin-dependent adherens junction between the ISC and its immediate daughter progenitor, leading the latter to adopt an enteroendocrine fate. Hence, although not lethal to non-susceptible organisms, Cry toxins can interfere with conserved cell adhesion mechanisms, thereby disrupting intestinal homeostasis and endocrine functions. |
Author | Fichant, Arnaud Jneid, Rouba Nawrot-Esposito, Marie-Paule Zucchini-Pascal, Nathalie Loudhaief, Rihab Bonis, Mathilde Gallet, Armel Rousset, Raphael Osman, Dani |
Author_xml | – sequence: 1 givenname: Rouba surname: Jneid fullname: Jneid, Rouba organization: Faculty of Sciences III and Azm Center for Research in Biotechnology and its Applications, LBA3B, EDST, Lebanese University, Tripoli, Lebanon – sequence: 2 givenname: Rihab surname: Loudhaief fullname: Loudhaief, Rihab organization: Universite Cote d'Azur, CNRS, INRAE, Sophia Antipolis, France – sequence: 3 givenname: Nathalie surname: Zucchini-Pascal fullname: Zucchini-Pascal, Nathalie organization: Universite Cote d'Azur, CNRS, INRAE, Sophia Antipolis, France – sequence: 4 givenname: Marie-Paule surname: Nawrot-Esposito fullname: Nawrot-Esposito, Marie-Paule organization: Universite Cote d'Azur, CNRS, INRAE, Sophia Antipolis, France – sequence: 5 givenname: Arnaud surname: Fichant fullname: Fichant, Arnaud organization: Laboratory for Food Safety, University Paris-Est, French Agency for Food, Environmental and Occupational Health & Safety, Maisons-Alfort, France – sequence: 6 givenname: Raphael surname: Rousset fullname: Rousset, Raphael organization: Universite Cote d'Azur, CNRS, INRAE, Sophia Antipolis, France – sequence: 7 givenname: Mathilde surname: Bonis fullname: Bonis, Mathilde organization: Laboratory for Food Safety, University Paris-Est, French Agency for Food, Environmental and Occupational Health & Safety, Maisons-Alfort, France – sequence: 8 givenname: Dani surname: Osman fullname: Osman, Dani organization: Faculty of Sciences III and Azm Center for Research in Biotechnology and its Applications, LBA3B, EDST, Lebanese University, Tripoli, Lebanon – sequence: 9 givenname: Armel orcidid: 0000-0002-2054-4780 surname: Gallet fullname: Gallet, Armel organization: Universite Cote d'Azur, CNRS, INRAE, Sophia Antipolis, France |
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CitedBy_id | crossref_primary_10_1098_rsos_230565 crossref_primary_10_1016_j_pestbp_2023_105596 crossref_primary_10_3390_foods13081140 crossref_primary_10_1016_j_resmic_2023_104089 |
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Keywords | enteroendocrine cells bacillus thurigiensis cell biology E-Cadherins intestinal stem cells Cry1A toxins D. melanogaster Drosophila melanogaster |
Language | English |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 PMCID: PMC9977296 Department of Biology, Faculty of Science, University of Copenhagen, Copenhagen, Denmark. UMR PIMIT (Processus Infectieux en Milieu Insulaire Tropical) CNRS 9192- INSERM 1187-IRD 249-Université de La Réunion, île de La Réunion, France. K8520 IWK Health Centre 8th Floor East Research 5850/5980 University Avenue Halifax, Nova Scotia, Canada. |
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Snippet | subsp.
(
) is a strong pathogen toward lepidopteran larvae thanks to specific Cry toxins causing leaky gut phenotypes. Hence,
and its toxins are used worldwide... Bacillus thuringiensis subsp. kurstaki ( Btk ) is a strong pathogen toward lepidopteran larvae thanks to specific Cry toxins causing leaky gut phenotypes.... Bacillus thuringiensis subsp. kurstaki (Btk) is a strong pathogen toward lepidopteran larvae thanks to specific Cry toxins causing leaky gut phenotypes. Hence,... Bacillus thuringiensis subsp. kurstaki ( Btk ) is a strong pathogen toward lepidopteran larvae thanks to specific Cry toxins causing leaky gut phenotypes.... |
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SubjectTerms | Animals bacillus thurigiensis Bacillus thuringiensis Bacillus thuringiensis Toxins - adverse effects Bacteriology Cell Adhesion Cell Biology Crops, Agricultural Cry1A toxins Drosophila melanogaster E-Cadherins enteroendocrine cells intestinal stem cells Life Sciences Microbiology and Parasitology Plants, Genetically Modified Stem Cells - drug effects Toxicology Toxicology and food chain |
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Title | Bacillus thuringiensis toxins divert progenitor cells toward enteroendocrine fate by decreasing cell adhesion with intestinal stem cells in Drosophila |
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