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Direct evidence for natural transmission of small-ruminant lentiviruses of subtype A4 from goats to sheep and vice versa.

ABSTRACT: Small-ruminant lentiviruses (SRLV), which include the caprine arthritis-encephalitis and the maedi-visna virus, cause persistent inflammatory infections in goats and sheep. SRLV are mainly transmitted from mother to offspring through milk. Transmission after prolonged contact between adult animals has also been observed. The observation that certain SRLV subtypes are found in both goats and sheep suggests that interspecies transmission has occurred on several occasions in the past. We investigated seropositive goats and sheep that were kept together in small mixed herds. Phylogenetic analysis of long proviral sequences in gag and pol, combined with epidemiologic information, demonstrated natural sheep-to-goat transmission of the recently identified SRLV subtype A4 in two instances and goat-to-sheep transmission of the same subtype in one instance. In a further mixed cluster, the direction of the interspecies transmission could not be determined. These findings present for the first time direct evidence that natural interspecies transmission of SRLV is ongoing in both directions. The findings are of relevance to virus eradication programs in both species.

SUBMITTER: Shah C

PROVIDER: S-EPMC434116 | biostudies-literature | 2004 Jul

REPOSITORIES: biostudies-literature

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Direct evidence for natural transmission of small-ruminant lentiviruses of subtype A4 from goats to sheep and vice versa.

Shah Cyril C Huder Jon B JB Böni Jürg J Schönmann Marietta M Mühlherr Janine J Lutz Hans H Schüpbach Jörg J

Journal of virology 20040701 14

Small-ruminant lentiviruses (SRLV), which include the caprine arthritis-encephalitis and the maedi-visna virus, cause persistent inflammatory infections in goats and sheep. SRLV are mainly transmitted from mother to offspring through milk. Transmission after prolonged contact between adult animals has also been observed. The observation that certain SRLV subtypes are found in both goats and sheep suggests that interspecies transmission has occurred on several occasions in the past. We investigat ...[more]

PMID: 15220425

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Project description:BackgroundSmall ruminant lentiviruses escaping efficient serological detection are still circulating in Swiss goats in spite of a long eradication campaign that essentially eliminated clinical cases of caprine arthritis encephalitis in the country. This strongly suggests that the circulating viruses are avirulent for goats.To test this hypothesis, we isolated circulating viruses from naturally infected animals and tested the in vitro and in vivo characteristics of these field isolates.MethodsViruses were isolated from primary macrophage cultures. The presence of lentiviruses in the culture supernatants was monitored by reverse transcriptase assay. Isolates were passaged in different cells and their cytopathogenic effects monitored by microscopy. Proviral load was quantified by real-time PCR using customized primer and probes. Statistical analysis comprised Analysis of Variance and Bonferroni Multiple Comparison Test.ResultsThe isolated viruses belonged to the small ruminant lentiviruses A4 subtype that appears to be prominent in Switzerland. The 4 isolates replicated very efficiently in macrophages, displaying heterogeneous phenotypes, with two isolates showing a pronounced cytopathogenicity for these cells. By contrast, all 4 isolates had a poor replication capacity in goat and sheep fibroblasts. The proviral loads in the peripheral blood and, in particular, in the mammary gland were surprisingly high compared to previous observations. Nevertheless, these viruses appear to be of low virulence for goats except for the mammary gland were histopathological changes were observed.ConclusionsSmall ruminant lentiviruses continue to circulate in Switzerland despite a long and expensive caprine arthritis encephalitis virus eradication campaign. We isolated 4 of these lentiviruses and confirmed their phylogenetic association with the prominent A4 subtype. The pathological and histopathological analysis of the infected animals supported the hypothesis that these A4 viruses are of low pathogenicity for goats, with, however, a caveat about the potentially detrimental effects on the mammary gland. Moreover, the high proviral load detected indicates that the immune system of the animals cannot control the infection and this, combined with the phenotypic plasticity observed in vitro, strongly argues in favour of a continuous and precise monitoring of these SRLV to avoid the risk of jeopardizing a long eradication campaign.

Project description:Small ruminant lentiviruses (SRLVs) are widespread in sheep and goats in Poland, and several subtypes were identified and molecularly characterized up to date. This is the first study that characterizes the molecular properties of A5 strains of SRLV detected in naturally infected, but clinically healthy, Carpathian goats. Segments from three genomic regions (gag, env, and LTR) were analyzed. Genetic distance, pairwise comparison, and phylogenetic analysis revealed that Polish SRLV A5 sequences are closely related to the Swiss and German A5 sequences suggesting a common origin. The epidemiological linkage was identified particularly between the small ruminants of Germany and Poland. Amino acid sequences of immunodominant regions in CA protein were well-conserved within analyzed strains; however, they showed some remarkable changes like substitution (D) to (E), at position 90 in Major Homology Region (MHR) and (T) to (S), at position 141 in epitope 3. In contrast, aa sequences of surface glycoprotein exhibited the highest variability confirming type-specific variation in SU5 epitope. Two deletions in the U3 region of A5 strains were noted: One (8 nt) located near the 5' end of the U3 region and the other (29 nt) located in the central region of U3. Additionally, all A5 strains had specific deletion (10 nt) in the R region. Furthermore, we did not find a correlation between copies of the CAAAT motif and clinical manifestation in infected animals. These data showed some remarkable features in the viral genome of A5 strains, which may be related to the attenuated phenotype in vivo, characterized by the lack of any clinical signs in infected goats. Certainly, more studies are required to support the hypothesis that these A5 viruses are of low pathogenicity for goats. We want to focus our future studies on the analysis of the whole genomes of these isolates and their biological properties, as well as on clinicopathological studies of goats infected by A5 SRLV, aiming to clarify the pathogenic potential of these viruses.

Project description:Previous studies revealed that the small ruminant lentivirus (SRLV) population in Poland is highly heterogeneous. All SRLVs detected from Polish sheep and goats so far have belonged to subtypes B1, B2, A1, A5, A12, A13, A16, A17, A18, A23 and A24. However, all characterized strains originated from asymptomatic animals. This is the first study that characterizes the molecular properties of SRLVs isolated from different organs of six arthritic goats. Segments from three genomic regions (gag, LTR and env) were analyzed. In addition, we quantified the SRLV proviral load in the blood and different organs and examined its association with different degrees of histopathological lesions. All sequences obtained from the goats involved in this study were homogeneous, showing an average degree of variability of 4.8%, 3.7% and 8.8% for gag, LTR and env, respectively. Phylogenetic analysis revealed that the sequences from the analyzed goats were clustered within SRLVs group A and formed a new subtype within this group, tentatively named A27. The histopathological examination of the lung, mammary gland, synovial membranes of joints and brain of the analyzed goats revealed evidence of inflammatory processes associated with SRLV infection, which was confirmed by positive immunohistochemistry assays. No significant correlation was observed between histological features and alterations in the sequences from different tissues. No tissue-specific signature pattern was identified. It was shown that animals with a higher proviral load showed more lesion severity in various SRLV-affected tissues, indicating a positive association between these two parameters. Our results also revealed differences in the SRLV load between animals even though the sequences derived from all of the goats were closely related, suggesting that host factors may restrict and control viral replication. This study provides new information about SRLV variants isolated from arthritic goats; however, more studies, including the isolation and characterization of biological properties of these viruses, should be performed to evaluate their pathogenic potential.

Dataset Information

Direct evidence for natural transmission of small-ruminant lentiviruses of subtype A4 from goats to sheep and vice versa.

Publications

Direct evidence for natural transmission of small-ruminant lentiviruses of subtype A4 from goats to sheep and vice versa.

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