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

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....

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Main Authors: 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
Format: Artículo
Language:Inglés
Published: MDPI 2022
Subjects:
Online Access:http://hdl.handle.net/20.500.12123/11886
https://www.mdpi.com/2076-0817/11/3/344
https://doi.org/10.3390/pathogens11030344
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author 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_browse Alzan, Heba F.
Araujo, Flabio Ribeiro de
Asurmendi, Sebastian
Benitez, Daniel Francisco
Florin-Christensen, Mónica
Gallenti, Romina Josefina
Hussein, Hala E.
Rolls, Peter
Schnittger, Leonhard
Sibeko, Kgomotso
Suarez, Carlos Esteban
Ueti, Massaro W.
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_sort Gallenti, Romina Josefina
collection INTA Digital
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.
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institution Instituto Nacional de Tecnología Agropecuaria (INTA -Argentina)
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spelling INTA118862022-05-16T16:42:37Z Unraveling the complexity of the rhomboid serine protease 4 family of Babesia bovis using bioinformatics and experimental studies 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 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 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 2022-05-16T16:34:13Z 2022-05-16T16:34:13Z 2022-03 info:ar-repo/semantics/artículo info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion 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 eng 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 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) application/pdf MDPI Pathogens 11 (3) : 344 (Marzo 2022)
spellingShingle 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
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
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
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_short 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
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
url http://hdl.handle.net/20.500.12123/11886
https://www.mdpi.com/2076-0817/11/3/344
https://doi.org/10.3390/pathogens11030344
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