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Isolation of infectious Theileria parva sporozoites secreted by infected Rhipicephalus appendiculatus ticks into an in vitro tick feeding system

BACKGROUND: Vector-borne diseases pose an increasing threat to global food security. Vaccines, diagnostic tests, and therapeutics are urgently needed for tick-borne diseases that affect livestock. However, the inability to obtain significant quantities of pathogen stages derived from ticks has hinde...

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Autores principales: Vimonish, Rubikah, Dinkel, Kelcey D., Fry, Lindsay M., Johnson, Wendell C., Capelli-Peixoto, Janaina, Bastos, Reginaldo G., Scoles, Glen A., Knowles, Donald P., Madder, Maxime, Chaka, George, Ueti, Massaro W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8704063/
https://www.ncbi.nlm.nih.gov/pubmed/34952641
http://dx.doi.org/10.1186/s13071-021-05120-7
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author Vimonish, Rubikah
Dinkel, Kelcey D.
Fry, Lindsay M.
Johnson, Wendell C.
Capelli-Peixoto, Janaina
Bastos, Reginaldo G.
Scoles, Glen A.
Knowles, Donald P.
Madder, Maxime
Chaka, George
Ueti, Massaro W.
author_facet Vimonish, Rubikah
Dinkel, Kelcey D.
Fry, Lindsay M.
Johnson, Wendell C.
Capelli-Peixoto, Janaina
Bastos, Reginaldo G.
Scoles, Glen A.
Knowles, Donald P.
Madder, Maxime
Chaka, George
Ueti, Massaro W.
author_sort Vimonish, Rubikah
collection PubMed
description BACKGROUND: Vector-borne diseases pose an increasing threat to global food security. Vaccines, diagnostic tests, and therapeutics are urgently needed for tick-borne diseases that affect livestock. However, the inability to obtain significant quantities of pathogen stages derived from ticks has hindered research. In vitro methods to isolate pathogens from infected tick vectors are paramount to advance transcriptomic, proteomic, and biochemical characterizations of tick-borne pathogens. METHODS: Nymphs of Rhipicephalus appendiculatus were infected with Theileria parva by feeding on a calf during an acute infection. Isolation of sporozoites was accomplished by feeding infected adult ticks on an in vitro tick feeding system. Sporozoite viability was tested using in vitro bovine lymphocytes. RESULTS: We isolated infectious T. parva sporozoites secreted into an in vitro tick feeding system. Infected adult R. appendiculatus ticks attached to and successfully fed on silicone membranes in the in vitro tick feeding system. Bovine blood in the receptacle was replaced with cell-free medium and the ticks were allowed to feed for 3 h to collect secreted T. parva sporozoites. Secreted sporozoites infected in vitro bovine lymphocytes, demonstrating that isolated sporozoites remained viable and infectious. CONCLUSIONS: This work is the first to report the isolation of mature infectious T. parva sporozoites using an in vitro tick feeding system, which represents a significant step towards the development of a more efficient control strategy for T. parva. Isolation of infectious tick-stage parasites will facilitate the examination of the vector-pathogen interface, thereby accelerating the development of next-generation vaccines and treatment interventions for tick-borne pathogens. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-021-05120-7.
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spelling pubmed-87040632021-12-27 Isolation of infectious Theileria parva sporozoites secreted by infected Rhipicephalus appendiculatus ticks into an in vitro tick feeding system Vimonish, Rubikah Dinkel, Kelcey D. Fry, Lindsay M. Johnson, Wendell C. Capelli-Peixoto, Janaina Bastos, Reginaldo G. Scoles, Glen A. Knowles, Donald P. Madder, Maxime Chaka, George Ueti, Massaro W. Parasit Vectors Research BACKGROUND: Vector-borne diseases pose an increasing threat to global food security. Vaccines, diagnostic tests, and therapeutics are urgently needed for tick-borne diseases that affect livestock. However, the inability to obtain significant quantities of pathogen stages derived from ticks has hindered research. In vitro methods to isolate pathogens from infected tick vectors are paramount to advance transcriptomic, proteomic, and biochemical characterizations of tick-borne pathogens. METHODS: Nymphs of Rhipicephalus appendiculatus were infected with Theileria parva by feeding on a calf during an acute infection. Isolation of sporozoites was accomplished by feeding infected adult ticks on an in vitro tick feeding system. Sporozoite viability was tested using in vitro bovine lymphocytes. RESULTS: We isolated infectious T. parva sporozoites secreted into an in vitro tick feeding system. Infected adult R. appendiculatus ticks attached to and successfully fed on silicone membranes in the in vitro tick feeding system. Bovine blood in the receptacle was replaced with cell-free medium and the ticks were allowed to feed for 3 h to collect secreted T. parva sporozoites. Secreted sporozoites infected in vitro bovine lymphocytes, demonstrating that isolated sporozoites remained viable and infectious. CONCLUSIONS: This work is the first to report the isolation of mature infectious T. parva sporozoites using an in vitro tick feeding system, which represents a significant step towards the development of a more efficient control strategy for T. parva. Isolation of infectious tick-stage parasites will facilitate the examination of the vector-pathogen interface, thereby accelerating the development of next-generation vaccines and treatment interventions for tick-borne pathogens. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13071-021-05120-7. BioMed Central 2021-12-24 /pmc/articles/PMC8704063/ /pubmed/34952641 http://dx.doi.org/10.1186/s13071-021-05120-7 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Vimonish, Rubikah
Dinkel, Kelcey D.
Fry, Lindsay M.
Johnson, Wendell C.
Capelli-Peixoto, Janaina
Bastos, Reginaldo G.
Scoles, Glen A.
Knowles, Donald P.
Madder, Maxime
Chaka, George
Ueti, Massaro W.
Isolation of infectious Theileria parva sporozoites secreted by infected Rhipicephalus appendiculatus ticks into an in vitro tick feeding system
title Isolation of infectious Theileria parva sporozoites secreted by infected Rhipicephalus appendiculatus ticks into an in vitro tick feeding system
title_full Isolation of infectious Theileria parva sporozoites secreted by infected Rhipicephalus appendiculatus ticks into an in vitro tick feeding system
title_fullStr Isolation of infectious Theileria parva sporozoites secreted by infected Rhipicephalus appendiculatus ticks into an in vitro tick feeding system
title_full_unstemmed Isolation of infectious Theileria parva sporozoites secreted by infected Rhipicephalus appendiculatus ticks into an in vitro tick feeding system
title_short Isolation of infectious Theileria parva sporozoites secreted by infected Rhipicephalus appendiculatus ticks into an in vitro tick feeding system
title_sort isolation of infectious theileria parva sporozoites secreted by infected rhipicephalus appendiculatus ticks into an in vitro tick feeding system
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8704063/
https://www.ncbi.nlm.nih.gov/pubmed/34952641
http://dx.doi.org/10.1186/s13071-021-05120-7
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