Differential vector competence of Ornithodoros soft ticks for African swine fever virus: What if it involves more than just crossing organic barriers in ticks?

Background: Several species of soft ticks in genus Ornithodoros are known vectors and reservoirs of African swine fever virus (ASFV). However, the underlying mechanisms of vector competence for ASFV across Ornithodoros species remain to be fully understood. To that end, this study compared ASFV replication and dissemination as well as virus vertical transmission to descendants between Ornithodoros moubata, O. erraticus, and O. verrucosus in relation to what is known about the ability of these soft tick species to transmit ASFV to pigs. To mimic the natural situation, a more realistic model was used where soft ticks were exposed to ASFV by allowing them to engorge on viremic pigs. Methods: Ornithodoros moubata ticks were infected with the ASFV strains Liv13/33 (genotype I) or Georgia2007/1 (genotype II), O. erraticus with OurT88/1 (genotype I) or Georgia2007/1 (genotype II), and O. verrucosus with Ukr12/Zapo (genotype II), resulting in five different tick–virus pairs. Quantitative PCR (qPCR) assays targeting the VP72 ASFV gene was carried out over several months on crushed ticks to study viral replication kinetics. Viral titration assays were also carried out on crushed ticks 2 months post infection to confirm virus survival in soft ticks. Ticks were dissected. and DNA was individually extracted from the following organs to study ASFV dissemination: intestine, salivary glands, and reproductive organs. DNA extracts from each organ were tested by qPCR. Lastly, larval or first nymph-stage progeny emerging from hatching eggs were tested by qPCR to assess ASFV vertical transmission. Results: Comparative analyses revealed higher rates of ASFV replication and dissemination in O. moubata infected with Liv13/33, while the opposite was observed for O. erraticus infected with Georgia2007/1 and for O. verrucosus with Ukr12/Zapo. Intermediate profiles were found for O. moubata infected with Georgia2007/1 and for O. erraticus with OurT88/1. Vertical transmission occurred efficiently in O. moubata infected with Liv13/33, and at very low rates in O. erraticus infected with OurT88/1. Conclusions: This study provides molecular data indicating that viral replication and dissemination in Ornithodoros ticks are major mechanisms underlying ASFV horizontal and vertical transmission. However, our results indicate that other determinants beyond viral replication also influence ASFV vector competence. Further research is required to fully understand this process in soft ticks.

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Main Authors: Pereira De Oliveira, Rémi, Hutet, Evelyne, Lancelot, Renaud, Paboeuf, Frédéric, Duhayon, Maxime, Boinas, Fernando, Pérez de León, Adalberto A., Filatov, Sehrii, Le Potier, Marie-Frédérique, Vial, Laurence
Format: article biblioteca
Language:eng
Subjects:L72 - Organismes nuisibles des animaux, L73 - Maladies des animaux, transmission des maladies, virologie, vecteur de maladie, virus peste porcine africaine, Ornithodoros, Ornithodoros moubata, maladie transmissible par tiques, http://aims.fao.org/aos/agrovoc/c_2329, http://aims.fao.org/aos/agrovoc/c_8259, http://aims.fao.org/aos/agrovoc/c_8164, http://aims.fao.org/aos/agrovoc/c_8649, http://aims.fao.org/aos/agrovoc/c_5422, http://aims.fao.org/aos/agrovoc/c_30948, http://aims.fao.org/aos/agrovoc/c_24908,
Online Access:http://agritrop.cirad.fr/599782/
http://agritrop.cirad.fr/599782/1/599782.pdf
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id dig-cirad-fr-599782
record_format koha
institution CIRAD FR
collection DSpace
country Francia
countrycode FR
component Bibliográfico
access En linea
databasecode dig-cirad-fr
tag biblioteca
region Europa del Oeste
libraryname Biblioteca del CIRAD Francia
language eng
topic L72 - Organismes nuisibles des animaux
L73 - Maladies des animaux
transmission des maladies
virologie
vecteur de maladie
virus peste porcine africaine
Ornithodoros
Ornithodoros moubata
maladie transmissible par tiques
http://aims.fao.org/aos/agrovoc/c_2329
http://aims.fao.org/aos/agrovoc/c_8259
http://aims.fao.org/aos/agrovoc/c_8164
http://aims.fao.org/aos/agrovoc/c_8649
http://aims.fao.org/aos/agrovoc/c_5422
http://aims.fao.org/aos/agrovoc/c_30948
http://aims.fao.org/aos/agrovoc/c_24908
L72 - Organismes nuisibles des animaux
L73 - Maladies des animaux
transmission des maladies
virologie
vecteur de maladie
virus peste porcine africaine
Ornithodoros
Ornithodoros moubata
maladie transmissible par tiques
http://aims.fao.org/aos/agrovoc/c_2329
http://aims.fao.org/aos/agrovoc/c_8259
http://aims.fao.org/aos/agrovoc/c_8164
http://aims.fao.org/aos/agrovoc/c_8649
http://aims.fao.org/aos/agrovoc/c_5422
http://aims.fao.org/aos/agrovoc/c_30948
http://aims.fao.org/aos/agrovoc/c_24908
spellingShingle L72 - Organismes nuisibles des animaux
L73 - Maladies des animaux
transmission des maladies
virologie
vecteur de maladie
virus peste porcine africaine
Ornithodoros
Ornithodoros moubata
maladie transmissible par tiques
http://aims.fao.org/aos/agrovoc/c_2329
http://aims.fao.org/aos/agrovoc/c_8259
http://aims.fao.org/aos/agrovoc/c_8164
http://aims.fao.org/aos/agrovoc/c_8649
http://aims.fao.org/aos/agrovoc/c_5422
http://aims.fao.org/aos/agrovoc/c_30948
http://aims.fao.org/aos/agrovoc/c_24908
L72 - Organismes nuisibles des animaux
L73 - Maladies des animaux
transmission des maladies
virologie
vecteur de maladie
virus peste porcine africaine
Ornithodoros
Ornithodoros moubata
maladie transmissible par tiques
http://aims.fao.org/aos/agrovoc/c_2329
http://aims.fao.org/aos/agrovoc/c_8259
http://aims.fao.org/aos/agrovoc/c_8164
http://aims.fao.org/aos/agrovoc/c_8649
http://aims.fao.org/aos/agrovoc/c_5422
http://aims.fao.org/aos/agrovoc/c_30948
http://aims.fao.org/aos/agrovoc/c_24908
Pereira De Oliveira, Rémi
Hutet, Evelyne
Lancelot, Renaud
Paboeuf, Frédéric
Duhayon, Maxime
Boinas, Fernando
Pérez de León, Adalberto A.
Filatov, Sehrii
Le Potier, Marie-Frédérique
Vial, Laurence
Differential vector competence of Ornithodoros soft ticks for African swine fever virus: What if it involves more than just crossing organic barriers in ticks?
description Background: Several species of soft ticks in genus Ornithodoros are known vectors and reservoirs of African swine fever virus (ASFV). However, the underlying mechanisms of vector competence for ASFV across Ornithodoros species remain to be fully understood. To that end, this study compared ASFV replication and dissemination as well as virus vertical transmission to descendants between Ornithodoros moubata, O. erraticus, and O. verrucosus in relation to what is known about the ability of these soft tick species to transmit ASFV to pigs. To mimic the natural situation, a more realistic model was used where soft ticks were exposed to ASFV by allowing them to engorge on viremic pigs. Methods: Ornithodoros moubata ticks were infected with the ASFV strains Liv13/33 (genotype I) or Georgia2007/1 (genotype II), O. erraticus with OurT88/1 (genotype I) or Georgia2007/1 (genotype II), and O. verrucosus with Ukr12/Zapo (genotype II), resulting in five different tick–virus pairs. Quantitative PCR (qPCR) assays targeting the VP72 ASFV gene was carried out over several months on crushed ticks to study viral replication kinetics. Viral titration assays were also carried out on crushed ticks 2 months post infection to confirm virus survival in soft ticks. Ticks were dissected. and DNA was individually extracted from the following organs to study ASFV dissemination: intestine, salivary glands, and reproductive organs. DNA extracts from each organ were tested by qPCR. Lastly, larval or first nymph-stage progeny emerging from hatching eggs were tested by qPCR to assess ASFV vertical transmission. Results: Comparative analyses revealed higher rates of ASFV replication and dissemination in O. moubata infected with Liv13/33, while the opposite was observed for O. erraticus infected with Georgia2007/1 and for O. verrucosus with Ukr12/Zapo. Intermediate profiles were found for O. moubata infected with Georgia2007/1 and for O. erraticus with OurT88/1. Vertical transmission occurred efficiently in O. moubata infected with Liv13/33, and at very low rates in O. erraticus infected with OurT88/1. Conclusions: This study provides molecular data indicating that viral replication and dissemination in Ornithodoros ticks are major mechanisms underlying ASFV horizontal and vertical transmission. However, our results indicate that other determinants beyond viral replication also influence ASFV vector competence. Further research is required to fully understand this process in soft ticks.
format article
topic_facet L72 - Organismes nuisibles des animaux
L73 - Maladies des animaux
transmission des maladies
virologie
vecteur de maladie
virus peste porcine africaine
Ornithodoros
Ornithodoros moubata
maladie transmissible par tiques
http://aims.fao.org/aos/agrovoc/c_2329
http://aims.fao.org/aos/agrovoc/c_8259
http://aims.fao.org/aos/agrovoc/c_8164
http://aims.fao.org/aos/agrovoc/c_8649
http://aims.fao.org/aos/agrovoc/c_5422
http://aims.fao.org/aos/agrovoc/c_30948
http://aims.fao.org/aos/agrovoc/c_24908
author Pereira De Oliveira, Rémi
Hutet, Evelyne
Lancelot, Renaud
Paboeuf, Frédéric
Duhayon, Maxime
Boinas, Fernando
Pérez de León, Adalberto A.
Filatov, Sehrii
Le Potier, Marie-Frédérique
Vial, Laurence
author_facet Pereira De Oliveira, Rémi
Hutet, Evelyne
Lancelot, Renaud
Paboeuf, Frédéric
Duhayon, Maxime
Boinas, Fernando
Pérez de León, Adalberto A.
Filatov, Sehrii
Le Potier, Marie-Frédérique
Vial, Laurence
author_sort Pereira De Oliveira, Rémi
title Differential vector competence of Ornithodoros soft ticks for African swine fever virus: What if it involves more than just crossing organic barriers in ticks?
title_short Differential vector competence of Ornithodoros soft ticks for African swine fever virus: What if it involves more than just crossing organic barriers in ticks?
title_full Differential vector competence of Ornithodoros soft ticks for African swine fever virus: What if it involves more than just crossing organic barriers in ticks?
title_fullStr Differential vector competence of Ornithodoros soft ticks for African swine fever virus: What if it involves more than just crossing organic barriers in ticks?
title_full_unstemmed Differential vector competence of Ornithodoros soft ticks for African swine fever virus: What if it involves more than just crossing organic barriers in ticks?
title_sort differential vector competence of ornithodoros soft ticks for african swine fever virus: what if it involves more than just crossing organic barriers in ticks?
url http://agritrop.cirad.fr/599782/
http://agritrop.cirad.fr/599782/1/599782.pdf
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spelling dig-cirad-fr-5997822024-01-29T03:54:36Z http://agritrop.cirad.fr/599782/ http://agritrop.cirad.fr/599782/ Differential vector competence of Ornithodoros soft ticks for African swine fever virus: What if it involves more than just crossing organic barriers in ticks? Pereira De Oliveira Rémi, Hutet Evelyne, Lancelot Renaud, Paboeuf Frédéric, Duhayon Maxime, Boinas Fernando, Pérez de León Adalberto A., Filatov Sehrii, Le Potier Marie-Frédérique, Vial Laurence. 2020. Parasites and Vectors, 13:618, 15 p.https://doi.org/10.1186/s13071-020-04497-1 <https://doi.org/10.1186/s13071-020-04497-1> Differential vector competence of Ornithodoros soft ticks for African swine fever virus: What if it involves more than just crossing organic barriers in ticks? Pereira De Oliveira, Rémi Hutet, Evelyne Lancelot, Renaud Paboeuf, Frédéric Duhayon, Maxime Boinas, Fernando Pérez de León, Adalberto A. Filatov, Sehrii Le Potier, Marie-Frédérique Vial, Laurence eng 2020 Parasites and Vectors L72 - Organismes nuisibles des animaux L73 - Maladies des animaux transmission des maladies virologie vecteur de maladie virus peste porcine africaine Ornithodoros Ornithodoros moubata maladie transmissible par tiques http://aims.fao.org/aos/agrovoc/c_2329 http://aims.fao.org/aos/agrovoc/c_8259 http://aims.fao.org/aos/agrovoc/c_8164 http://aims.fao.org/aos/agrovoc/c_8649 http://aims.fao.org/aos/agrovoc/c_5422 http://aims.fao.org/aos/agrovoc/c_30948 http://aims.fao.org/aos/agrovoc/c_24908 Background: Several species of soft ticks in genus Ornithodoros are known vectors and reservoirs of African swine fever virus (ASFV). However, the underlying mechanisms of vector competence for ASFV across Ornithodoros species remain to be fully understood. To that end, this study compared ASFV replication and dissemination as well as virus vertical transmission to descendants between Ornithodoros moubata, O. erraticus, and O. verrucosus in relation to what is known about the ability of these soft tick species to transmit ASFV to pigs. To mimic the natural situation, a more realistic model was used where soft ticks were exposed to ASFV by allowing them to engorge on viremic pigs. Methods: Ornithodoros moubata ticks were infected with the ASFV strains Liv13/33 (genotype I) or Georgia2007/1 (genotype II), O. erraticus with OurT88/1 (genotype I) or Georgia2007/1 (genotype II), and O. verrucosus with Ukr12/Zapo (genotype II), resulting in five different tick–virus pairs. Quantitative PCR (qPCR) assays targeting the VP72 ASFV gene was carried out over several months on crushed ticks to study viral replication kinetics. Viral titration assays were also carried out on crushed ticks 2 months post infection to confirm virus survival in soft ticks. Ticks were dissected. and DNA was individually extracted from the following organs to study ASFV dissemination: intestine, salivary glands, and reproductive organs. DNA extracts from each organ were tested by qPCR. Lastly, larval or first nymph-stage progeny emerging from hatching eggs were tested by qPCR to assess ASFV vertical transmission. Results: Comparative analyses revealed higher rates of ASFV replication and dissemination in O. moubata infected with Liv13/33, while the opposite was observed for O. erraticus infected with Georgia2007/1 and for O. verrucosus with Ukr12/Zapo. Intermediate profiles were found for O. moubata infected with Georgia2007/1 and for O. erraticus with OurT88/1. Vertical transmission occurred efficiently in O. moubata infected with Liv13/33, and at very low rates in O. erraticus infected with OurT88/1. Conclusions: This study provides molecular data indicating that viral replication and dissemination in Ornithodoros ticks are major mechanisms underlying ASFV horizontal and vertical transmission. However, our results indicate that other determinants beyond viral replication also influence ASFV vector competence. Further research is required to fully understand this process in soft ticks. article info:eu-repo/semantics/article Journal Article info:eu-repo/semantics/publishedVersion http://agritrop.cirad.fr/599782/1/599782.pdf text cc_by info:eu-repo/semantics/openAccess https://creativecommons.org/licenses/by/4.0/ https://doi.org/10.1186/s13071-020-04497-1 10.1186/s13071-020-04497-1 info:eu-repo/semantics/altIdentifier/doi/10.1186/s13071-020-04497-1 info:eu-repo/semantics/altIdentifier/purl/https://doi.org/10.1186/s13071-020-04497-1 info:eu-repo/semantics/dataset/purl/https://figshare.com/articles/journal_contribution/Additional_file_1_of_Differential_vector_competence_of_Ornithodoros_soft_ticks_for_African_swine_fever_virus_What_if_it_involves_more_than_just_crossing_organic_barriers_in_ticks_/13357455