Unraveling the complexity of the rhomboid serine protease 4 family of Babesia bovis using bioinformatics and experimental studies

Autores
Gallenti, Romina Josefina; Hussein, Hala E.; Alzan, Heba F.; Suarez, Carlos Esteban; Ueti, Massaro W.; Asurmendi, Sebastian; Benitez, Daniel Francisco; Araujo, Flabio Ribeiro de; Rolls, Peter; Sibeko, Kgomotso; Schnittger, Leonhard; Florin-Christensen, Mónica
Año de publicación
2022
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Babesia bovis, a tick-transmitted apicomplexan protozoon, infects cattle in tropical and subtropical regions around the world. In the apicomplexans Toxoplasma gondii and Plasmodium falciparum, rhomboid serine protease 4 (ROM4) fulfills an essential role in host cell invasion. We thus investigated B. bovis ROM4 coding genes; their genomic organization; their expression in in vitro cultured asexual (AS) and sexual stages (SS); and strain polymorphisms. B. bovis contains five rom4 paralogous genes in chromosome 2, which we have named rom4.1, 4.2, 4.3, 4.4 and 4.5. There are moderate degrees of sequence identity between them, except for rom4.3 and 4.4, which are almost identical. RT-qPCR analysis showed that rom4.1 and rom4.3/4.4, respectively, display 18-fold and 218-fold significantly higher (p < 0.01) levels of transcription in SS than in AS, suggesting a role in gametogenesis-related processes. In contrast, transcription of rom4.4 and 4.5 differed non-significantly between the stages. ROM4 polymorphisms among geographic isolates were essentially restricted to the number of tandem repeats of a 29-amino acid sequence in ROM4.5. This sequence repeat is highly conserved and predicted as antigenic. B. bovis ROMs likely participate in relevant host–pathogen interactions and are possibly useful targets for the development of new control strategies against this pathogen.
Instituto de Patobiología
Fil: Gallenti, Romina Josefina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Patobiología Veterinaria; Argentina
Fil: Gallenti, Romina Josefina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Hussein, Hala E. Washington State University. Department of Veterinary Microbiology and Pathology; Estados Unidos
Fil: Hussein, Hala E. Cairo University. Faculty of Science. Department of Entomology; Egipto
Fil: Alzan, Heba F. Washington State University. Department of Veterinary Microbiology and Pathology; Estados Unidos
Fil: Alzan, Heba F. National Research Center. Tick and Tick-Borne Disease Research Unit; Egipto
Fil: Suarez, Carlos Esteban. Washington State University. College of Veterinary Medicine. Department of Veterinary Microbiology and Pathology; Estados Unidos
Fil: Suarez, Carlos Esteban. United States Department of Agricultural-Agricultural Research Service. Animal Disease Research Unit; Estados Unidos
Fil: Ueti, Massaro W. Washington State University. College of Veterinary Medicine. Department of Veterinary Microbiology and Pathology; Estados Unidos
Fil: Ueti, Massaro W. United States Department of Agricultural-Agricultural Research Service. Animal Disease Research Unit; Estados Unidos
Fil: Asurmendi, Sebastian. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina
Fil: Asurmendi, Sebastian. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Benitez, Daniel Francisco. Instituto Nacional de Tecnología Agropecuaria (INTA). Estación Experimental Agropecuaria Mercedes; Argentina
Fil: Araujo, Flabio R. EMBRAPA ; Brasil
Fil: Rolls, P. Tick Fever Centre. Department of Agriculture & Fisheries; Australia
Fil: Sibeko, Kgomotso. University of Pretoria. Faculty of Veterinary Science. Department of Veterinary Tropical Diseases. Vectors and Vector-borne Diseases Research Programme; Sudáfrica
Fil: Schnittger, Leonhard. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Patobiología Veterinaria; Argentina
Fil: Schnittger, Leonhard. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Florin-Christensen, Mónica. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Patobiología Veterinaria; Argentina
Fil: Florin-Christensen, Mónica. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fuente
Pathogens 11 (3) : 344 (Marzo 2022)
Materia
Tick-borne Diseases
Babesiosis
Gene Expression
Polymorphism
Bioinformatics
Enfermedades Transmitidas por Garrapatas
Bovinae
Babesia bovis
Expresión Génica
Polimorfismo
Bioinformática
Experimental Studies
Rhomboid Serine Protease
Estudios Experimentales
Proteasa de Serina Romboidal
Nivel de accesibilidad
acceso abierto
Condiciones de uso
http://creativecommons.org/licenses/by-nc-sa/4.0/
Repositorio
INTA Digital (INTA)
Institución
Instituto Nacional de Tecnología Agropecuaria
OAI Identificador
oai:localhost:20.500.12123/11886
Acceder
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network_name_str INTA Digital (INTA)
spelling Unraveling the complexity of the rhomboid serine protease 4 family of Babesia bovis using bioinformatics and experimental studiesGallenti, Romina JosefinaHussein, Hala E.Alzan, Heba F.Suarez, Carlos EstebanUeti, Massaro W.Asurmendi, SebastianBenitez, Daniel FranciscoAraujo, Flabio Ribeiro deRolls, PeterSibeko, KgomotsoSchnittger, LeonhardFlorin-Christensen, MónicaTick-borne DiseasesBabesiosisGene ExpressionPolymorphismBioinformaticsEnfermedades Transmitidas por GarrapatasBovinaeBabesia bovisExpresión GénicaPolimorfismoBioinformáticaExperimental StudiesRhomboid Serine ProteaseEstudios ExperimentalesProteasa de Serina RomboidalBabesia bovis, a tick-transmitted apicomplexan protozoon, infects cattle in tropical and subtropical regions around the world. In the apicomplexans Toxoplasma gondii and Plasmodium falciparum, rhomboid serine protease 4 (ROM4) fulfills an essential role in host cell invasion. We thus investigated B. bovis ROM4 coding genes; their genomic organization; their expression in in vitro cultured asexual (AS) and sexual stages (SS); and strain polymorphisms. B. bovis contains five rom4 paralogous genes in chromosome 2, which we have named rom4.1, 4.2, 4.3, 4.4 and 4.5. There are moderate degrees of sequence identity between them, except for rom4.3 and 4.4, which are almost identical. RT-qPCR analysis showed that rom4.1 and rom4.3/4.4, respectively, display 18-fold and 218-fold significantly higher (p < 0.01) levels of transcription in SS than in AS, suggesting a role in gametogenesis-related processes. In contrast, transcription of rom4.4 and 4.5 differed non-significantly between the stages. ROM4 polymorphisms among geographic isolates were essentially restricted to the number of tandem repeats of a 29-amino acid sequence in ROM4.5. This sequence repeat is highly conserved and predicted as antigenic. B. bovis ROMs likely participate in relevant host–pathogen interactions and are possibly useful targets for the development of new control strategies against this pathogen.Instituto de PatobiologíaFil: Gallenti, Romina Josefina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Patobiología Veterinaria; ArgentinaFil: Gallenti, Romina Josefina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Hussein, Hala E. Washington State University. Department of Veterinary Microbiology and Pathology; Estados UnidosFil: Hussein, Hala E. Cairo University. Faculty of Science. Department of Entomology; EgiptoFil: Alzan, Heba F. Washington State University. Department of Veterinary Microbiology and Pathology; Estados UnidosFil: Alzan, Heba F. National Research Center. Tick and Tick-Borne Disease Research Unit; EgiptoFil: Suarez, Carlos Esteban. Washington State University. College of Veterinary Medicine. Department of Veterinary Microbiology and Pathology; Estados UnidosFil: Suarez, Carlos Esteban. United States Department of Agricultural-Agricultural Research Service. Animal Disease Research Unit; Estados UnidosFil: Ueti, Massaro W. Washington State University. College of Veterinary Medicine. Department of Veterinary Microbiology and Pathology; Estados UnidosFil: Ueti, Massaro W. United States Department of Agricultural-Agricultural Research Service. Animal Disease Research Unit; Estados UnidosFil: Asurmendi, Sebastian. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; ArgentinaFil: Asurmendi, Sebastian. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Benitez, Daniel Francisco. Instituto Nacional de Tecnología Agropecuaria (INTA). Estación Experimental Agropecuaria Mercedes; ArgentinaFil: Araujo, Flabio R. EMBRAPA ; BrasilFil: Rolls, P. Tick Fever Centre. Department of Agriculture & Fisheries; AustraliaFil: Sibeko, Kgomotso. University of Pretoria. Faculty of Veterinary Science. Department of Veterinary Tropical Diseases. Vectors and Vector-borne Diseases Research Programme; SudáfricaFil: Schnittger, Leonhard. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Patobiología Veterinaria; ArgentinaFil: Schnittger, Leonhard. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Florin-Christensen, Mónica. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Patobiología Veterinaria; ArgentinaFil: Florin-Christensen, Mónica. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaMDPI2022-05-16T16:34:13Z2022-05-16T16:34:13Z2022-03info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfhttp://hdl.handle.net/20.500.12123/11886https://www.mdpi.com/2076-0817/11/3/3442076-0817https://doi.org/10.3390/pathogens11030344Pathogens 11 (3) : 344 (Marzo 2022)reponame:INTA Digital (INTA)instname:Instituto Nacional de Tecnología Agropecuariaenginfo:eu-repograntAgreement/INTA/2019-PD-E5-I102-001/2019-PD-E5-I102-001/AR./Desarrollo de vacunas y tecnologías para mejorar las estrategias profilácticas y terapéuticas de las enfermedades que afectan la producción animal y la salud públicainfo:eu-repograntAgreement/INTA/2019-PD-E5-I105-001/2019-PD-E5-I105-001/AR./Patógenos animales: su interacción con el hospedador y el medio ambiente. Impacto en productividad, ecosistemas, sanidad animal y salud pública en el marco “Una Salud”info:eu-repograntAgreement/INTA/2019-PE-E5-I109-001/2019-PE-E5-I109-001/AR./Convocatoria: Estudios para el control de enfermedades subtropicales y/o transmitidas por vectores (Tristeza Bovina, Garrapatas, Miasis, Tripanosomiasis, Lengua Azul y lainfo:eu-repo/semantics/openAccesshttp://creativecommons.org/licenses/by-nc-sa/4.0/Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)2025-09-29T13:45:33Zoai:localhost:20.500.12123/11886instacron:INTAInstitucionalhttp://repositorio.inta.gob.ar/Organismo científico-tecnológicoNo correspondehttp://repositorio.inta.gob.ar/oai/requesttripaldi.nicolas@inta.gob.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:l2025-09-29 13:45:34.252INTA Digital (INTA) - Instituto Nacional de Tecnología Agropecuariafalse
dc.title.none.fl_str_mv Unraveling the complexity of the rhomboid serine protease 4 family of Babesia bovis using bioinformatics and experimental studies
title Unraveling the complexity of the rhomboid serine protease 4 family of Babesia bovis using bioinformatics and experimental studies
spellingShingle Unraveling the complexity of the rhomboid serine protease 4 family of Babesia bovis using bioinformatics and experimental studies
Gallenti, Romina Josefina
Tick-borne Diseases
Babesiosis
Gene Expression
Polymorphism
Bioinformatics
Enfermedades Transmitidas por Garrapatas
Bovinae
Babesia bovis
Expresión Génica
Polimorfismo
Bioinformática
Experimental Studies
Rhomboid Serine Protease
Estudios Experimentales
Proteasa de Serina Romboidal
title_short Unraveling the complexity of the rhomboid serine protease 4 family of Babesia bovis using bioinformatics and experimental studies
title_full Unraveling the complexity of the rhomboid serine protease 4 family of Babesia bovis using bioinformatics and experimental studies
title_fullStr Unraveling the complexity of the rhomboid serine protease 4 family of Babesia bovis using bioinformatics and experimental studies
title_full_unstemmed Unraveling the complexity of the rhomboid serine protease 4 family of Babesia bovis using bioinformatics and experimental studies
title_sort Unraveling the complexity of the rhomboid serine protease 4 family of Babesia bovis using bioinformatics and experimental studies
dc.creator.none.fl_str_mv Gallenti, Romina Josefina
Hussein, Hala E.
Alzan, Heba F.
Suarez, Carlos Esteban
Ueti, Massaro W.
Asurmendi, Sebastian
Benitez, Daniel Francisco
Araujo, Flabio Ribeiro de
Rolls, Peter
Sibeko, Kgomotso
Schnittger, Leonhard
Florin-Christensen, Mónica
author Gallenti, Romina Josefina
author_facet Gallenti, Romina Josefina
Hussein, Hala E.
Alzan, Heba F.
Suarez, Carlos Esteban
Ueti, Massaro W.
Asurmendi, Sebastian
Benitez, Daniel Francisco
Araujo, Flabio Ribeiro de
Rolls, Peter
Sibeko, Kgomotso
Schnittger, Leonhard
Florin-Christensen, Mónica
author_role author
author2 Hussein, Hala E.
Alzan, Heba F.
Suarez, Carlos Esteban
Ueti, Massaro W.
Asurmendi, Sebastian
Benitez, Daniel Francisco
Araujo, Flabio Ribeiro de
Rolls, Peter
Sibeko, Kgomotso
Schnittger, Leonhard
Florin-Christensen, Mónica
author2_role author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Tick-borne Diseases
Babesiosis
Gene Expression
Polymorphism
Bioinformatics
Enfermedades Transmitidas por Garrapatas
Bovinae
Babesia bovis
Expresión Génica
Polimorfismo
Bioinformática
Experimental Studies
Rhomboid Serine Protease
Estudios Experimentales
Proteasa de Serina Romboidal
topic Tick-borne Diseases
Babesiosis
Gene Expression
Polymorphism
Bioinformatics
Enfermedades Transmitidas por Garrapatas
Bovinae
Babesia bovis
Expresión Génica
Polimorfismo
Bioinformática
Experimental Studies
Rhomboid Serine Protease
Estudios Experimentales
Proteasa de Serina Romboidal
dc.description.none.fl_txt_mv Babesia bovis, a tick-transmitted apicomplexan protozoon, infects cattle in tropical and subtropical regions around the world. In the apicomplexans Toxoplasma gondii and Plasmodium falciparum, rhomboid serine protease 4 (ROM4) fulfills an essential role in host cell invasion. We thus investigated B. bovis ROM4 coding genes; their genomic organization; their expression in in vitro cultured asexual (AS) and sexual stages (SS); and strain polymorphisms. B. bovis contains five rom4 paralogous genes in chromosome 2, which we have named rom4.1, 4.2, 4.3, 4.4 and 4.5. There are moderate degrees of sequence identity between them, except for rom4.3 and 4.4, which are almost identical. RT-qPCR analysis showed that rom4.1 and rom4.3/4.4, respectively, display 18-fold and 218-fold significantly higher (p < 0.01) levels of transcription in SS than in AS, suggesting a role in gametogenesis-related processes. In contrast, transcription of rom4.4 and 4.5 differed non-significantly between the stages. ROM4 polymorphisms among geographic isolates were essentially restricted to the number of tandem repeats of a 29-amino acid sequence in ROM4.5. This sequence repeat is highly conserved and predicted as antigenic. B. bovis ROMs likely participate in relevant host–pathogen interactions and are possibly useful targets for the development of new control strategies against this pathogen.
Instituto de Patobiología
Fil: Gallenti, Romina Josefina. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Patobiología Veterinaria; Argentina
Fil: Gallenti, Romina Josefina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Hussein, Hala E. Washington State University. Department of Veterinary Microbiology and Pathology; Estados Unidos
Fil: Hussein, Hala E. Cairo University. Faculty of Science. Department of Entomology; Egipto
Fil: Alzan, Heba F. Washington State University. Department of Veterinary Microbiology and Pathology; Estados Unidos
Fil: Alzan, Heba F. National Research Center. Tick and Tick-Borne Disease Research Unit; Egipto
Fil: Suarez, Carlos Esteban. Washington State University. College of Veterinary Medicine. Department of Veterinary Microbiology and Pathology; Estados Unidos
Fil: Suarez, Carlos Esteban. United States Department of Agricultural-Agricultural Research Service. Animal Disease Research Unit; Estados Unidos
Fil: Ueti, Massaro W. Washington State University. College of Veterinary Medicine. Department of Veterinary Microbiology and Pathology; Estados Unidos
Fil: Ueti, Massaro W. United States Department of Agricultural-Agricultural Research Service. Animal Disease Research Unit; Estados Unidos
Fil: Asurmendi, Sebastian. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Agrobiotecnología y Biología Molecular; Argentina
Fil: Asurmendi, Sebastian. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Benitez, Daniel Francisco. Instituto Nacional de Tecnología Agropecuaria (INTA). Estación Experimental Agropecuaria Mercedes; Argentina
Fil: Araujo, Flabio R. EMBRAPA ; Brasil
Fil: Rolls, P. Tick Fever Centre. Department of Agriculture & Fisheries; Australia
Fil: Sibeko, Kgomotso. University of Pretoria. Faculty of Veterinary Science. Department of Veterinary Tropical Diseases. Vectors and Vector-borne Diseases Research Programme; Sudáfrica
Fil: Schnittger, Leonhard. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Patobiología Veterinaria; Argentina
Fil: Schnittger, Leonhard. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Florin-Christensen, Mónica. Instituto Nacional de Tecnología Agropecuaria (INTA). Instituto de Patobiología Veterinaria; Argentina
Fil: Florin-Christensen, Mónica. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
description Babesia bovis, a tick-transmitted apicomplexan protozoon, infects cattle in tropical and subtropical regions around the world. In the apicomplexans Toxoplasma gondii and Plasmodium falciparum, rhomboid serine protease 4 (ROM4) fulfills an essential role in host cell invasion. We thus investigated B. bovis ROM4 coding genes; their genomic organization; their expression in in vitro cultured asexual (AS) and sexual stages (SS); and strain polymorphisms. B. bovis contains five rom4 paralogous genes in chromosome 2, which we have named rom4.1, 4.2, 4.3, 4.4 and 4.5. There are moderate degrees of sequence identity between them, except for rom4.3 and 4.4, which are almost identical. RT-qPCR analysis showed that rom4.1 and rom4.3/4.4, respectively, display 18-fold and 218-fold significantly higher (p < 0.01) levels of transcription in SS than in AS, suggesting a role in gametogenesis-related processes. In contrast, transcription of rom4.4 and 4.5 differed non-significantly between the stages. ROM4 polymorphisms among geographic isolates were essentially restricted to the number of tandem repeats of a 29-amino acid sequence in ROM4.5. This sequence repeat is highly conserved and predicted as antigenic. B. bovis ROMs likely participate in relevant host–pathogen interactions and are possibly useful targets for the development of new control strategies against this pathogen.
publishDate 2022
dc.date.none.fl_str_mv 2022-05-16T16:34:13Z
2022-05-16T16:34:13Z
2022-03
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/20.500.12123/11886
https://www.mdpi.com/2076-0817/11/3/344
2076-0817
https://doi.org/10.3390/pathogens11030344
url http://hdl.handle.net/20.500.12123/11886
https://www.mdpi.com/2076-0817/11/3/344
https://doi.org/10.3390/pathogens11030344
identifier_str_mv 2076-0817
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repograntAgreement/INTA/2019-PD-E5-I102-001/2019-PD-E5-I102-001/AR./Desarrollo de vacunas y tecnologías para mejorar las estrategias profilácticas y terapéuticas de las enfermedades que afectan la producción animal y la salud pública
info:eu-repograntAgreement/INTA/2019-PD-E5-I105-001/2019-PD-E5-I105-001/AR./Patógenos animales: su interacción con el hospedador y el medio ambiente. Impacto en productividad, ecosistemas, sanidad animal y salud pública en el marco “Una Salud”
info:eu-repograntAgreement/INTA/2019-PE-E5-I109-001/2019-PE-E5-I109-001/AR./Convocatoria: Estudios para el control de enfermedades subtropicales y/o transmitidas por vectores (Tristeza Bovina, Garrapatas, Miasis, Tripanosomiasis, Lengua Azul y la
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
http://creativecommons.org/licenses/by-nc-sa/4.0/
Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)
eu_rights_str_mv openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by-nc-sa/4.0/
Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv MDPI
publisher.none.fl_str_mv MDPI
dc.source.none.fl_str_mv Pathogens 11 (3) : 344 (Marzo 2022)
reponame:INTA Digital (INTA)
instname:Instituto Nacional de Tecnología Agropecuaria
reponame_str INTA Digital (INTA)
collection INTA Digital (INTA)
instname_str Instituto Nacional de Tecnología Agropecuaria
repository.name.fl_str_mv INTA Digital (INTA) - Instituto Nacional de Tecnología Agropecuaria
repository.mail.fl_str_mv tripaldi.nicolas@inta.gob.ar
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