Intravenous Infection of Small Ruminants Suggests a Goat-Restricted Host Tropism and Weak Humoral Immune Response for an Atypical Bluetongue Virus Isolate
Bluetongue virus (BTV) is the etiologic agent of bluetongue (BT), a viral WOAH-listed disease affecting wild and domestic ruminants, primarily sheep. The outermost capsid protein VP2, encoded by S2, is the virion’s most variable protein, and the ability of reference sera to neutralize an isolate has...
| Main Authors: | , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2023-01-01
|
| Series: | Viruses |
| Subjects: | |
| Online Access: | https://www.mdpi.com/1999-4915/15/1/257 |
| _version_ | 1827621303379558400 |
|---|---|
| author | Massimo Spedicato Giovanni Di Teodoro Liana Teodori Mariangela Iorio Alessandra Leone Barbara Bonfini Lilia Testa Maura Pisciella Claudia Casaccia Ottavio Portanti Emanuela Rossi Tiziana Di Febo Nicola Ferri Giovanni Savini Alessio Lorusso |
| author_facet | Massimo Spedicato Giovanni Di Teodoro Liana Teodori Mariangela Iorio Alessandra Leone Barbara Bonfini Lilia Testa Maura Pisciella Claudia Casaccia Ottavio Portanti Emanuela Rossi Tiziana Di Febo Nicola Ferri Giovanni Savini Alessio Lorusso |
| author_sort | Massimo Spedicato |
| collection | DOAJ |
| description | Bluetongue virus (BTV) is the etiologic agent of bluetongue (BT), a viral WOAH-listed disease affecting wild and domestic ruminants, primarily sheep. The outermost capsid protein VP2, encoded by S2, is the virion’s most variable protein, and the ability of reference sera to neutralize an isolate has so far dictated the differentiation of 24 classical BTV serotypes. Since 2008, additional novel BTV serotypes, often referred to as “atypical” BTVs, have been documented and, currently, the full list includes 36 putative serotypes. In March 2015, a novel atypical BTV strain was detected in the blood of asymptomatic goats in Sardinia (Italy) and named BTV-X ITL2015. The strain re-emerged in the same region in 2021 (BTV-X ITL2021). In this study, we investigated the pathogenicity and kinetics of infection of BTV-X ITL2021 following subcutaneous and intravenous infection of small ruminants. We demonstrated that, in our experimental settings, BTV-X ITL2021 induced a long-lasting viraemia only when administered by the intravenous route in goats, though the animals remained healthy and, apparently, did not develop a neutralizing immune response. Sheep were shown to be refractory to the infection by either route. Our findings suggest a restricted host tropism of BTV-X and point out goats as reservoirs for this virus in the field. |
| first_indexed | 2024-03-09T11:01:41Z |
| format | Article |
| id | doaj.art-ed26e11ad4fa49bc8e5fcbc704f69efd |
| institution | Directory Open Access Journal |
| issn | 1999-4915 |
| language | English |
| last_indexed | 2024-03-09T11:01:41Z |
| publishDate | 2023-01-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Viruses |
| spelling | doaj.art-ed26e11ad4fa49bc8e5fcbc704f69efd2023-12-01T01:14:13ZengMDPI AGViruses1999-49152023-01-0115125710.3390/v15010257Intravenous Infection of Small Ruminants Suggests a Goat-Restricted Host Tropism and Weak Humoral Immune Response for an Atypical Bluetongue Virus IsolateMassimo Spedicato0Giovanni Di Teodoro1Liana Teodori2Mariangela Iorio3Alessandra Leone4Barbara Bonfini5Lilia Testa6Maura Pisciella7Claudia Casaccia8Ottavio Portanti9Emanuela Rossi10Tiziana Di Febo11Nicola Ferri12Giovanni Savini13Alessio Lorusso14Istituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise, 64100 Teramo, ItalyIstituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise, 64100 Teramo, ItalyIstituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise, 64100 Teramo, ItalyIstituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise, 64100 Teramo, ItalyIstituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise, 64100 Teramo, ItalyIstituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise, 64100 Teramo, ItalyIstituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise, 64100 Teramo, ItalyIstituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise, 64100 Teramo, ItalyIstituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise, 64100 Teramo, ItalyIstituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise, 64100 Teramo, ItalyIstituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise, 64100 Teramo, ItalyIstituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise, 64100 Teramo, ItalyIstituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise, 64100 Teramo, ItalyIstituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise, 64100 Teramo, ItalyIstituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise, 64100 Teramo, ItalyBluetongue virus (BTV) is the etiologic agent of bluetongue (BT), a viral WOAH-listed disease affecting wild and domestic ruminants, primarily sheep. The outermost capsid protein VP2, encoded by S2, is the virion’s most variable protein, and the ability of reference sera to neutralize an isolate has so far dictated the differentiation of 24 classical BTV serotypes. Since 2008, additional novel BTV serotypes, often referred to as “atypical” BTVs, have been documented and, currently, the full list includes 36 putative serotypes. In March 2015, a novel atypical BTV strain was detected in the blood of asymptomatic goats in Sardinia (Italy) and named BTV-X ITL2015. The strain re-emerged in the same region in 2021 (BTV-X ITL2021). In this study, we investigated the pathogenicity and kinetics of infection of BTV-X ITL2021 following subcutaneous and intravenous infection of small ruminants. We demonstrated that, in our experimental settings, BTV-X ITL2021 induced a long-lasting viraemia only when administered by the intravenous route in goats, though the animals remained healthy and, apparently, did not develop a neutralizing immune response. Sheep were shown to be refractory to the infection by either route. Our findings suggest a restricted host tropism of BTV-X and point out goats as reservoirs for this virus in the field.https://www.mdpi.com/1999-4915/15/1/257bluetongueatypical serotypegoatsheep |
| spellingShingle | Massimo Spedicato Giovanni Di Teodoro Liana Teodori Mariangela Iorio Alessandra Leone Barbara Bonfini Lilia Testa Maura Pisciella Claudia Casaccia Ottavio Portanti Emanuela Rossi Tiziana Di Febo Nicola Ferri Giovanni Savini Alessio Lorusso Intravenous Infection of Small Ruminants Suggests a Goat-Restricted Host Tropism and Weak Humoral Immune Response for an Atypical Bluetongue Virus Isolate Viruses bluetongue atypical serotype goat sheep |
| title | Intravenous Infection of Small Ruminants Suggests a Goat-Restricted Host Tropism and Weak Humoral Immune Response for an Atypical Bluetongue Virus Isolate |
| title_full | Intravenous Infection of Small Ruminants Suggests a Goat-Restricted Host Tropism and Weak Humoral Immune Response for an Atypical Bluetongue Virus Isolate |
| title_fullStr | Intravenous Infection of Small Ruminants Suggests a Goat-Restricted Host Tropism and Weak Humoral Immune Response for an Atypical Bluetongue Virus Isolate |
| title_full_unstemmed | Intravenous Infection of Small Ruminants Suggests a Goat-Restricted Host Tropism and Weak Humoral Immune Response for an Atypical Bluetongue Virus Isolate |
| title_short | Intravenous Infection of Small Ruminants Suggests a Goat-Restricted Host Tropism and Weak Humoral Immune Response for an Atypical Bluetongue Virus Isolate |
| title_sort | intravenous infection of small ruminants suggests a goat restricted host tropism and weak humoral immune response for an atypical bluetongue virus isolate |
| topic | bluetongue atypical serotype goat sheep |
| url | https://www.mdpi.com/1999-4915/15/1/257 |
| work_keys_str_mv | AT massimospedicato intravenousinfectionofsmallruminantssuggestsagoatrestrictedhosttropismandweakhumoralimmuneresponseforanatypicalbluetonguevirusisolate AT giovanniditeodoro intravenousinfectionofsmallruminantssuggestsagoatrestrictedhosttropismandweakhumoralimmuneresponseforanatypicalbluetonguevirusisolate AT lianateodori intravenousinfectionofsmallruminantssuggestsagoatrestrictedhosttropismandweakhumoralimmuneresponseforanatypicalbluetonguevirusisolate AT mariangelaiorio intravenousinfectionofsmallruminantssuggestsagoatrestrictedhosttropismandweakhumoralimmuneresponseforanatypicalbluetonguevirusisolate AT alessandraleone intravenousinfectionofsmallruminantssuggestsagoatrestrictedhosttropismandweakhumoralimmuneresponseforanatypicalbluetonguevirusisolate AT barbarabonfini intravenousinfectionofsmallruminantssuggestsagoatrestrictedhosttropismandweakhumoralimmuneresponseforanatypicalbluetonguevirusisolate AT liliatesta intravenousinfectionofsmallruminantssuggestsagoatrestrictedhosttropismandweakhumoralimmuneresponseforanatypicalbluetonguevirusisolate AT maurapisciella intravenousinfectionofsmallruminantssuggestsagoatrestrictedhosttropismandweakhumoralimmuneresponseforanatypicalbluetonguevirusisolate AT claudiacasaccia intravenousinfectionofsmallruminantssuggestsagoatrestrictedhosttropismandweakhumoralimmuneresponseforanatypicalbluetonguevirusisolate AT ottavioportanti intravenousinfectionofsmallruminantssuggestsagoatrestrictedhosttropismandweakhumoralimmuneresponseforanatypicalbluetonguevirusisolate AT emanuelarossi intravenousinfectionofsmallruminantssuggestsagoatrestrictedhosttropismandweakhumoralimmuneresponseforanatypicalbluetonguevirusisolate AT tizianadifebo intravenousinfectionofsmallruminantssuggestsagoatrestrictedhosttropismandweakhumoralimmuneresponseforanatypicalbluetonguevirusisolate AT nicolaferri intravenousinfectionofsmallruminantssuggestsagoatrestrictedhosttropismandweakhumoralimmuneresponseforanatypicalbluetonguevirusisolate AT giovannisavini intravenousinfectionofsmallruminantssuggestsagoatrestrictedhosttropismandweakhumoralimmuneresponseforanatypicalbluetonguevirusisolate AT alessiolorusso intravenousinfectionofsmallruminantssuggestsagoatrestrictedhosttropismandweakhumoralimmuneresponseforanatypicalbluetonguevirusisolate |