Kharon1 null mutants of Leishmania mexicana are avirulent in mice and exhibit a cytokinesis defect within macrophages
In a variety of eukaryotes, flagella play important roles both in motility and as sensory organelles that monitor the extracellular environment. In the parasitic protozoan Leishmania mexicana, one glucose transporter isoform, LmxGT1, is targeted selectively to the flagellar membrane where it appears...
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Published in | PloS one Vol. 10; no. 8; p. e0134432 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
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12.08.2015
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Abstract | In a variety of eukaryotes, flagella play important roles both in motility and as sensory organelles that monitor the extracellular environment. In the parasitic protozoan Leishmania mexicana, one glucose transporter isoform, LmxGT1, is targeted selectively to the flagellar membrane where it appears to play a role in glucose sensing. Trafficking of LmxGT1 to the flagellar membrane is dependent upon interaction with the KHARON1 protein that is located at the base of the flagellar axoneme. Remarkably, while Δkharon1 null mutants are viable as insect stage promastigotes, they are unable to survive as amastigotes inside host macrophages. Although Δkharon1 promastigotes enter macrophages and transform into amastigotes, these intracellular parasites are unable to execute cytokinesis and form multinucleate cells before dying. Notably, extracellular axenic amastigotes of Δkharon1 mutants replicate and divide normally, indicating a defect in the mutants that is only exhibited in the intra-macrophage environment. Although the flagella of Δkharon1 amastigotes adhere to the phagolysomal membrane of host macrophages, the morphology of the mutant flagella is often distorted. Additionally, these null mutants are completely avirulent following injection into BALB/c mice, underscoring the critical role of the KHARON1 protein for viability of intracellular amastigotes and disease in the animal model of leishmaniasis. |
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AbstractList | In a variety of eukaryotes, flagella play important roles both in motility and as sensory organelles that monitor the extracellular environment. In the parasitic protozoan Leishmania mexicana, one glucose transporter isoform, LmxGT1, is targeted selectively to the flagellar membrane where it appears to play a role in glucose sensing. Trafficking of LmxGT1 to the flagellar membrane is dependent upon interaction with the KHARON1 protein that is located at the base of the flagellar axoneme. Remarkably, while Δkharon1 null mutants are viable as insect stage promastigotes, they are unable to survive as amastigotes inside host macrophages. Although Δkharon1 promastigotes enter macrophages and transform into amastigotes, these intracellular parasites are unable to execute cytokinesis and form multinucleate cells before dying. Notably, extracellular axenic amastigotes of Δkharon1 mutants replicate and divide normally, indicating a defect in the mutants that is only exhibited in the intra-macrophage environment. Although the flagella of Δkharon1 amastigotes adhere to the phagolysomal membrane of host macrophages, the morphology of the mutant flagella is often distorted. Additionally, these null mutants are completely avirulent following injection into BALB/c mice, underscoring the critical role of the KHARON1 protein for viability of intracellular amastigotes and disease in the animal model of leishmaniasis. In a variety of eukaryotes, flagella play important roles both in motility and as sensory organelles that monitor the extracellular environment. In the parasitic protozoan Leishmania mexicana , one glucose transporter isoform, LmxGT1, is targeted selectively to the flagellar membrane where it appears to play a role in glucose sensing. Trafficking of LmxGT1 to the flagellar membrane is dependent upon interaction with the KHARON1 protein that is located at the base of the flagellar axoneme. Remarkably, while Δ kharon1 null mutants are viable as insect stage promastigotes, they are unable to survive as amastigotes inside host macrophages. Although Δ kharon1 promastigotes enter macrophages and transform into amastigotes, these intracellular parasites are unable to execute cytokinesis and form multinucleate cells before dying. Notably, extracellular axenic amastigotes of Δ kharon1 mutants replicate and divide normally, indicating a defect in the mutants that is only exhibited in the intra-macrophage environment. Although the flagella of Δ kharon1 amastigotes adhere to the phagolysomal membrane of host macrophages, the morphology of the mutant flagella is often distorted. Additionally, these null mutants are completely avirulent following injection into BALB/c mice, underscoring the critical role of the KHARON1 protein for viability of intracellular amastigotes and disease in the animal model of leishmaniasis. In a variety of eukaryotes, flagella play important roles both in motility and as sensory organelles that monitor the extracellular environment. In the parasitic protozoan Leishmania mexicana , one glucose transporter isoform, LmxGT1, is targeted selectively to the flagellar membrane where it appears to play a role in glucose sensing. Trafficking of LmxGT1 to the flagellar membrane is dependent upon interaction with the KHARON1 protein that is located at the base of the flagellar axoneme. Remarkably, while Δ kharon1 null mutants are viable as insect stage promastigotes, they are unable to survive as amastigotes inside host macrophages. Although Δ kharon1 promastigotes enter macrophages and transform into amastigotes, these intracellular parasites are unable to execute cytokinesis and form multinucleate cells before dying. Notably, extracellular axenic amastigotes of Δ kharon1 mutants replicate and divide normally, indicating a defect in the mutants that is only exhibited in the intra-macrophage environment. Although the flagella of Δ kharon1 amastigotes adhere to the phagolysomal membrane of host macrophages, the morphology of the mutant flagella is often distorted. Additionally, these null mutants are completely avirulent following injection into BALB/c mice, underscoring the critical role of the KHARON1 protein for viability of intracellular amastigotes and disease in the animal model of leishmaniasis. |
Author | Landfear, Scott M Sanchez, Marco A Tran, Khoa D Gluenz, Eva Vieira, Danielle P Valli, Jessica |
AuthorAffiliation | 2 Sir William Dunn School of Pathology, University of Oxford, Oxford, United Kingdom University at Buffalo, UNITED STATES 1 Department of Molecular Microbiology & Immunology, Oregon Health & Science University, Portland, Oregon, United States of America |
AuthorAffiliation_xml | – name: University at Buffalo, UNITED STATES – name: 2 Sir William Dunn School of Pathology, University of Oxford, Oxford, United Kingdom – name: 1 Department of Molecular Microbiology & Immunology, Oregon Health & Science University, Portland, Oregon, United States of America |
Author_xml | – sequence: 1 givenname: Khoa D surname: Tran fullname: Tran, Khoa D organization: Department of Molecular Microbiology & Immunology, Oregon Health & Science University, Portland, Oregon, United States of America – sequence: 2 givenname: Danielle P surname: Vieira fullname: Vieira, Danielle P organization: Department of Molecular Microbiology & Immunology, Oregon Health & Science University, Portland, Oregon, United States of America – sequence: 3 givenname: Marco A surname: Sanchez fullname: Sanchez, Marco A organization: Department of Molecular Microbiology & Immunology, Oregon Health & Science University, Portland, Oregon, United States of America – sequence: 4 givenname: Jessica surname: Valli fullname: Valli, Jessica organization: Sir William Dunn School of Pathology, University of Oxford, Oxford, United Kingdom – sequence: 5 givenname: Eva surname: Gluenz fullname: Gluenz, Eva organization: Sir William Dunn School of Pathology, University of Oxford, Oxford, United Kingdom – sequence: 6 givenname: Scott M surname: Landfear fullname: Landfear, Scott M organization: Department of Molecular Microbiology & Immunology, Oregon Health & Science University, Portland, Oregon, United States of America |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26266938$$D View this record in MEDLINE/PubMed |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: SML KDT DPV MAS EG JV. Performed the experiments: KDT DPV MAS JV. Analyzed the data: SML KDT DPV MAS EG JV. Wrote the paper: SML KDT DPV. Competing Interests: The authors have declared that no competing interests exist. |
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SubjectTerms | Amastigotes Animals Cell cycle Cell division Chemoreception Cytokinesis Cytokinesis - genetics Cytoskeletal Proteins - genetics Eukaryotes Flagella Flagella - genetics Flagella - parasitology Glucose Glucose Transport Proteins, Facilitative - genetics Glucose transporter Immunology Insects Intracellular Leishmania Leishmania donovani Leishmania major Leishmania mexicana Leishmania mexicana - genetics Leishmania mexicana - pathogenicity Leishmaniasis Leishmaniasis - genetics Leishmaniasis - parasitology Leishmaniasis - pathology Macrophages Macrophages - parasitology Mice Mutants Mutation Organelles Parasites Parasitic diseases Promastigotes Proteins Protozoa Protozoan Proteins - genetics Signal transduction Vector-borne diseases Viability |
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Title | Kharon1 null mutants of Leishmania mexicana are avirulent in mice and exhibit a cytokinesis defect within macrophages |
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