Bacillus thuringiensis Cry14A family proteins as novel anthelmintics against gastrointestinal nematode parasites
Bacillus thuringiensis crystal (Cry) proteins have been expressed in commercial transgenic crops for nearly 30 years, providing safe and effective control of insect pests and significantly reducing the application of hazardous chemical pesticides. B . thuringiensis crystal proteins have also been sh...
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| Published in | PLoS neglected tropical diseases Vol. 18; no. 10; p. e0012611 |
|---|---|
| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
25.10.2024
Public Library of Science (PLoS) |
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| Abstract | Bacillus thuringiensis
crystal (Cry) proteins have been expressed in commercial transgenic crops for nearly 30 years, providing safe and effective control of insect pests and significantly reducing the application of hazardous chemical pesticides.
B
.
thuringiensis
crystal proteins have also been shown to target parasitic nematodes, including plant parasitic nematodes. Recently, transgenic soybean crops expressing Cry14Ab have been shown to provide control against the soybean cyst nematode
Heterodera glycines
, marking the first time a crystal protein is being commercialized in transgenic crops for control of a nematode pest. However, apart from
H
.
glycines
and the free-living nematode,
Caenorhabditis elegans
, the breadth of nematode activity of Cry14Ab,
e
.
g
., against gastrointestinal parasitic nematodes (GINs), has not been reported. Here we study the efficacy of Cry14Ab against a wide range of gastrointestinal nematode parasites (GINs) in vitro and in vivo. We find that Cry14Ab is effective in vitro against the barber’s pole worm
Haemonchus contortus
larvae, small strongyles cyathostomin larvae, the hookworm
Ancylostoma ceylanicum
adults, the roundworm
Ascaris suum
L4 larvae, and the whipworm
Trichuris muris
adults. In rodents infected with GIN parasites, Cry14Ab is effective as an in vivo anthelmintic against the hookworms
A
.
ceylanicum
and
N
.
americanus
, against the mouse parasite
Heligmosomoides polygyrus bakeri
, and against the roundworm
A
.
suum
. Cry14Ab also variably reduces the reproduction of the whipworm
T
.
muris
in vivo. Using optimized profile Markov Models, we looked for other putative anthelmintic Cry proteins and, within this list, identified a Bt crystal protein, GenBank accession no. MF893203, that we produced and demonstrated intoxicated GINs. This protein, with 90% amino acid identity to Cry14Ab, is active against
C
.
elegans
,
A
.
ceylanicum
adults, and
A
.
suum
L4 larvae in vitro. MF893203 was given the official designation of Cry14Ac. Cry14Ac is also an effective in vivo anthelmintic against
A
.
ceylanicum
hookworms in hamsters and intestinal
A
.
suum
in mice. Taken together, our results demonstrate that Cry14Ab and Cry14Ac have wide therapeutic utility against GINs. |
|---|---|
| AbstractList | Bacillus thuringiensis crystal (Cry) proteins have been expressed in commercial transgenic crops for nearly 30 years, providing safe and effective control of insect pests and significantly reducing the application of hazardous chemical pesticides. B. thuringiensis crystal proteins have also been shown to target parasitic nematodes, including plant parasitic nematodes. Recently, transgenic soybean crops expressing Cry14Ab have been shown to provide control against the soybean cyst nematode Heterodera glycines, marking the first time a crystal protein is being commercialized in transgenic crops for control of a nematode pest. However, apart from H. glycines and the free-living nematode, Caenornabditis elegans, the breadth of nematode activity of Cry14Ab, e.g., against gastrointestinal parasitic nematodes (GINs), has not been reported. Here we study the efficacy of Cry14Ab against a wide range of gastrointestinal nematode parasites (GINs) in vitro and in vivo. We find that Cry14Ab is effective in vitro against the barber's pole worm Haemonchus contortus larvae, small strongyles cyathostomin larvae, the hookworm Ancylostoma ceylanicum adults, the roundworm Ascaris suum L4 larvae, and the whipworm Trichuris muris adults. In rodents infected with GIN parasites, Cry14Ab is effective as an in vivo anthelmintic against the hookworms A. ceylanicum and N. americanus, against the mouse parasite Heligmosomoides polygyrus bakeri, and against the roundworm A. suum. Cry14Ab also variably reduces the reproduction of the whipworm T. muris in vivo. Using optimized profile Markov Models, we looked for other putative anthelmintic Cry proteins and, within this list, identified a Bt crystal protein, GenBank accession no. MF893203, that we produced and demonstrated intoxicated GINs. This protein, with 90% amino acid identity to Cry14Ab, is active against C. elegans, A. ceylanicum adults, and A. suum L4 larvae in vitro. MF893203 was given the official designation of Cry14Ac. Cry14Ac is also an effective in vivo anthelmintic against A. ceylanicum hookworms in hamsters and intestinal A. suum in mice. Taken together, our results demonstrate that Cry14Ab and Cry14Ac have wide therapeutic utility against GINs. Bacillus thuringiensis crystal (Cry) proteins have been expressed in commercial transgenic crops for nearly 30 years, providing safe and effective control of insect pests and significantly reducing the application of hazardous chemical pesticides. B. thuringiensis crystal proteins have also been shown to target parasitic nematodes, including plant parasitic nematodes. Recently, transgenic soybean crops expressing Cry14Ab have been shown to provide control against the soybean cyst nematode Heterodera glycines, marking the first time a crystal protein is being commercialized in transgenic crops for control of a nematode pest. However, apart from H. glycines and the free-living nematode, Caenorhabditis elegans, the breadth of nematode activity of Cry14Ab, e.g., against gastrointestinal parasitic nematodes (GINs), has not been reported. Here we study the efficacy of Cry14Ab against a wide range of gastrointestinal nematode parasites (GINs) in vitro and in vivo. We find that Cry14Ab is effective in vitro against the barber's pole worm Haemonchus contortus larvae, small strongyles cyathostomin larvae, the hookworm Ancylostoma ceylanicum adults, the roundworm Ascaris suum L4 larvae, and the whipworm Trichuris muris adults. In rodents infected with GIN parasites, Cry14Ab is effective as an in vivo anthelmintic against the hookworms A. ceylanicum and N. americanus, against the mouse parasite Heligmosomoides polygyrus bakeri, and against the roundworm A. suum. Cry14Ab also variably reduces the reproduction of the whipworm T. muris in vivo. Using optimized profile Markov Models, we looked for other putative anthelmintic Cry proteins and, within this list, identified a Bt crystal protein, GenBank accession no. MF893203, that we produced and demonstrated intoxicated GINs. This protein, with 90% amino acid identity to Cry14Ab, is active against C. elegans, A. ceylanicum adults, and A. suum L4 larvae in vitro. MF893203 was given the official designation of Cry14Ac. Cry14Ac is also an effective in vivo anthelmintic against A. ceylanicum hookworms in hamsters and intestinal A. suum in mice. Taken together, our results demonstrate that Cry14Ab and Cry14Ac have wide therapeutic utility against GINs.Bacillus thuringiensis crystal (Cry) proteins have been expressed in commercial transgenic crops for nearly 30 years, providing safe and effective control of insect pests and significantly reducing the application of hazardous chemical pesticides. B. thuringiensis crystal proteins have also been shown to target parasitic nematodes, including plant parasitic nematodes. Recently, transgenic soybean crops expressing Cry14Ab have been shown to provide control against the soybean cyst nematode Heterodera glycines, marking the first time a crystal protein is being commercialized in transgenic crops for control of a nematode pest. However, apart from H. glycines and the free-living nematode, Caenorhabditis elegans, the breadth of nematode activity of Cry14Ab, e.g., against gastrointestinal parasitic nematodes (GINs), has not been reported. Here we study the efficacy of Cry14Ab against a wide range of gastrointestinal nematode parasites (GINs) in vitro and in vivo. We find that Cry14Ab is effective in vitro against the barber's pole worm Haemonchus contortus larvae, small strongyles cyathostomin larvae, the hookworm Ancylostoma ceylanicum adults, the roundworm Ascaris suum L4 larvae, and the whipworm Trichuris muris adults. In rodents infected with GIN parasites, Cry14Ab is effective as an in vivo anthelmintic against the hookworms A. ceylanicum and N. americanus, against the mouse parasite Heligmosomoides polygyrus bakeri, and against the roundworm A. suum. Cry14Ab also variably reduces the reproduction of the whipworm T. muris in vivo. Using optimized profile Markov Models, we looked for other putative anthelmintic Cry proteins and, within this list, identified a Bt crystal protein, GenBank accession no. MF893203, that we produced and demonstrated intoxicated GINs. This protein, with 90% amino acid identity to Cry14Ab, is active against C. elegans, A. ceylanicum adults, and A. suum L4 larvae in vitro. MF893203 was given the official designation of Cry14Ac. Cry14Ac is also an effective in vivo anthelmintic against A. ceylanicum hookworms in hamsters and intestinal A. suum in mice. Taken together, our results demonstrate that Cry14Ab and Cry14Ac have wide therapeutic utility against GINs. Bacillus thuringiensis crystal (Cry) proteins have been expressed in commercial transgenic crops for nearly 30 years, providing safe and effective control of insect pests and significantly reducing the application of hazardous chemical pesticides. B . thuringiensis crystal proteins have also been shown to target parasitic nematodes, including plant parasitic nematodes. Recently, transgenic soybean crops expressing Cry14Ab have been shown to provide control against the soybean cyst nematode Heterodera glycines , marking the first time a crystal protein is being commercialized in transgenic crops for control of a nematode pest. However, apart from H . glycines and the free-living nematode, Caenorhabditis elegans , the breadth of nematode activity of Cry14Ab, e . g ., against gastrointestinal parasitic nematodes (GINs), has not been reported. Here we study the efficacy of Cry14Ab against a wide range of gastrointestinal nematode parasites (GINs) in vitro and in vivo. We find that Cry14Ab is effective in vitro against the barber’s pole worm Haemonchus contortus larvae, small strongyles cyathostomin larvae, the hookworm Ancylostoma ceylanicum adults, the roundworm Ascaris suum L4 larvae, and the whipworm Trichuris muris adults. In rodents infected with GIN parasites, Cry14Ab is effective as an in vivo anthelmintic against the hookworms A . ceylanicum and N . americanus , against the mouse parasite Heligmosomoides polygyrus bakeri , and against the roundworm A . suum . Cry14Ab also variably reduces the reproduction of the whipworm T . muris in vivo. Using optimized profile Markov Models, we looked for other putative anthelmintic Cry proteins and, within this list, identified a Bt crystal protein, GenBank accession no. MF893203, that we produced and demonstrated intoxicated GINs. This protein, with 90% amino acid identity to Cry14Ab, is active against C . elegans , A . ceylanicum adults, and A . suum L4 larvae in vitro. MF893203 was given the official designation of Cry14Ac. Cry14Ac is also an effective in vivo anthelmintic against A . ceylanicum hookworms in hamsters and intestinal A . suum in mice. Taken together, our results demonstrate that Cry14Ab and Cry14Ac have wide therapeutic utility against GINs. Gastrointestinal parasitic nematodes or worms pose a significant threat to global health, causing illness in millions-billions of people and animals. Current treatments have limitations, including concerns about drug resistance. We are exploring a promising new approach using natural Crystal (Cry) proteins from Bacillus thuringiensis (Bt) bacteria, which are already widely used as safe and effective insecticides. To date, we have focused on the anthelmintic (deworming) properties of Bt Cry protein Cry5Ba. Here, our research demonstrates that a newly characterized and different Bt Cry protein, Cry14Ab, can also effectively target and kill various types of harmful parasitic nematodes in both laboratory and animal models. Moreover, we identify another related Bt protein, Cry14Ac, with similar activities against parasitic nematodes. These findings highlight the potential of Bt proteins as a novel class of deworming medications, offering hope for the development and clinical deployment of safer and more effective treatments against parasitic nematode infections. Bacillus thuringiensis crystal (Cry) proteins have been expressed in commercial transgenic crops for nearly 30 years, providing safe and effective control of insect pests and significantly reducing the application of hazardous chemical pesticides. B. thuringiensis crystal proteins have also been shown to target parasitic nematodes, including plant parasitic nematodes. Recently, transgenic soybean crops expressing Cry14Ab have been shown to provide control against the soybean cyst nematode Heterodera glycines, marking the first time a crystal protein is being commercialized in transgenic crops for control of a nematode pest. However, apart from H. glycines and the free-living nematode, Caenorhabditis elegans, the breadth of nematode activity of Cry14Ab, e.g., against gastrointestinal parasitic nematodes (GINs), has not been reported. Here we study the efficacy of Cry14Ab against a wide range of gastrointestinal nematode parasites (GINs) in vitro and in vivo. We find that Cry14Ab is effective in vitro against the barber's pole worm Haemonchus contortus larvae, small strongyles cyathostomin larvae, the hookworm Ancylostoma ceylanicum adults, the roundworm Ascaris suum L4 larvae, and the whipworm Trichuris muris adults. In rodents infected with GIN parasites, Cry14Ab is effective as an in vivo anthelmintic against the hookworms A. ceylanicum and N. americanus, against the mouse parasite Heligmosomoides polygyrus bakeri, and against the roundworm A. suum. Cry14Ab also variably reduces the reproduction of the whipworm T. muris in vivo. Using optimized profile Markov Models, we looked for other putative anthelmintic Cry proteins and, within this list, identified a Bt crystal protein, GenBank accession no. MF893203, that we produced and demonstrated intoxicated GINs. This protein, with 90% amino acid identity to Cry14Ab, is active against C. elegans, A. ceylanicum adults, and A. suum L4 larvae in vitro. MF893203 was given the official designation of Cry14Ac. Cry14Ac is also an effective in vivo anthelmintic against A. ceylanicum hookworms in hamsters and intestinal A. suum in mice. Taken together, our results demonstrate that Cry14Ab and Cry14Ac have wide therapeutic utility against GINs. Bacillus thuringiensis crystal (Cry) proteins have been expressed in commercial transgenic crops for nearly 30 years, providing safe and effective control of insect pests and significantly reducing the application of hazardous chemical pesticides. B . thuringiensis crystal proteins have also been shown to target parasitic nematodes, including plant parasitic nematodes. Recently, transgenic soybean crops expressing Cry14Ab have been shown to provide control against the soybean cyst nematode Heterodera glycines , marking the first time a crystal protein is being commercialized in transgenic crops for control of a nematode pest. However, apart from H . glycines and the free-living nematode, Caenorhabditis elegans , the breadth of nematode activity of Cry14Ab, e . g ., against gastrointestinal parasitic nematodes (GINs), has not been reported. Here we study the efficacy of Cry14Ab against a wide range of gastrointestinal nematode parasites (GINs) in vitro and in vivo. We find that Cry14Ab is effective in vitro against the barber’s pole worm Haemonchus contortus larvae, small strongyles cyathostomin larvae, the hookworm Ancylostoma ceylanicum adults, the roundworm Ascaris suum L4 larvae, and the whipworm Trichuris muris adults. In rodents infected with GIN parasites, Cry14Ab is effective as an in vivo anthelmintic against the hookworms A . ceylanicum and N . americanus , against the mouse parasite Heligmosomoides polygyrus bakeri , and against the roundworm A . suum . Cry14Ab also variably reduces the reproduction of the whipworm T . muris in vivo. Using optimized profile Markov Models, we looked for other putative anthelmintic Cry proteins and, within this list, identified a Bt crystal protein, GenBank accession no. MF893203, that we produced and demonstrated intoxicated GINs. This protein, with 90% amino acid identity to Cry14Ab, is active against C . elegans , A . ceylanicum adults, and A . suum L4 larvae in vitro. MF893203 was given the official designation of Cry14Ac. Cry14Ac is also an effective in vivo anthelmintic against A . ceylanicum hookworms in hamsters and intestinal A . suum in mice. Taken together, our results demonstrate that Cry14Ab and Cry14Ac have wide therapeutic utility against GINs. |
| Audience | Academic |
| Author | Nielsen, Martin K. Ding, Qian Cazeault, Nicholas R. Li, Hanchen Rus, Florentina Liesegang, Heiko Darfour, Esther A. Ostroff, Gary R. Petersson, Katherine H. Aroian, Raffi V. Flanagan, Kelly Díaz-Valerio, Stefani Hoang, Duy Kass, Elizabeth |
| AuthorAffiliation | George Washington University School of Medicine and Health Sciences, UNITED STATES OF AMERICA 4 M.H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, United States of America 1 Program in Molecular Medicine, UMASS Chan Medical School, Worcester, Massachusetts, United States of America 2 Department of Genomic and Applied Microbiology & Göttingen Genomics Laboratory, Institute of Microbiology and Genetics, Georg-August University of Göttingen, Göttingen, Germany 3 Department of Fisheries, Animal, and Veterinary Sciences, University of Rhode Island, Kingston, Rhode Island, United States of America |
| AuthorAffiliation_xml | – name: 1 Program in Molecular Medicine, UMASS Chan Medical School, Worcester, Massachusetts, United States of America – name: 3 Department of Fisheries, Animal, and Veterinary Sciences, University of Rhode Island, Kingston, Rhode Island, United States of America – name: 4 M.H. Gluck Equine Research Center, Department of Veterinary Science, University of Kentucky, Lexington, Kentucky, United States of America – name: 2 Department of Genomic and Applied Microbiology & Göttingen Genomics Laboratory, Institute of Microbiology and Genetics, Georg-August University of Göttingen, Göttingen, Germany – name: George Washington University School of Medicine and Health Sciences, UNITED STATES OF AMERICA |
| Author_xml | – sequence: 1 givenname: Duy surname: Hoang fullname: Hoang, Duy – sequence: 2 givenname: Kelly surname: Flanagan fullname: Flanagan, Kelly – sequence: 3 givenname: Qian surname: Ding fullname: Ding, Qian – sequence: 4 givenname: Nicholas R. surname: Cazeault fullname: Cazeault, Nicholas R. – sequence: 5 givenname: Hanchen surname: Li fullname: Li, Hanchen – sequence: 6 givenname: Stefani surname: Díaz-Valerio fullname: Díaz-Valerio, Stefani – sequence: 7 givenname: Florentina surname: Rus fullname: Rus, Florentina – sequence: 8 givenname: Esther A. surname: Darfour fullname: Darfour, Esther A. – sequence: 9 givenname: Elizabeth surname: Kass fullname: Kass, Elizabeth – sequence: 10 givenname: Katherine H. surname: Petersson fullname: Petersson, Katherine H. – sequence: 11 givenname: Martin K. surname: Nielsen fullname: Nielsen, Martin K. – sequence: 12 givenname: Heiko surname: Liesegang fullname: Liesegang, Heiko – sequence: 13 givenname: Gary R. surname: Ostroff fullname: Ostroff, Gary R. – sequence: 14 givenname: Raffi V. orcidid: 0000-0002-9741-3834 surname: Aroian fullname: Aroian, Raffi V. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/39453964$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | Copyright: © 2024 Hoang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. COPYRIGHT 2024 Public Library of Science 2024 Hoang et al 2024 Hoang et al |
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| Notes | new_version ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 I have read the journal’s policy and the authors of this manuscript have the following competing interests: The University of Massachusetts Chan Medical School is pursuing patent protection related to the use of Cry14Ab as anthelmintic via U.S. Provisional Patent Application Serial No. 63/439,759 (K.F. and R.V.A. as inventors) and the University of Massachusetts Chan Medical School and University of Göttingen are pursing patent protection related to the use of Cry14Ac as anthelmintic via U.S. Provisional Patent Application Serial No. 63/649,526 (K.F., S.D.V., H.L., and R.V.A. as inventors). QD, NRC and HL also contributed equally to this work. |
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crystal (Cry) proteins have been expressed in commercial transgenic crops for nearly 30 years, providing safe and effective control of... Bacillus thuringiensis crystal (Cry) proteins have been expressed in commercial transgenic crops for nearly 30 years, providing safe and effective control of... |
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| Title | Bacillus thuringiensis Cry14A family proteins as novel anthelmintics against gastrointestinal nematode parasites |
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