Comparative analysis of the attachment protein gene (H) of dolphin morbillivirus

doi:10.1016/0168-1702(95)01254-0

Virus Research

Volume 40, Issue 1, January 1996, Pages 47-55

https://doi.org/10.1016/0168-1702(95)01254-0 Get rights and content

Abstract

DMV, dolphin morbillivirus, a paramyxovirus of uncertain origin recently emerged in Mediterranean dolphins. This study presents the complete nucleotide sequence of the hemagglutinin (H) gene including the gene boundaries. The single open reading frame of the DMV H gene encodes a protein of 604 residues which exhibits overall sequence characteristics similar to the H genes of other morbilliviruses. When compared to its closest homologues, measles virus (MV) and rinderpest virus (RPV), DMV has, respectively, 44 and 46% of amino acid residues in identical positions. The primary sequence of the DMV H protein is markedly less conserved than that of the fusion protein. The comparative data at the genomic level correspond with cross-neutralization studies with different morbilliviruses. Retrospective serogical studies dating back to 1983 indicate DMV-like infections in whales of the eastern Atlantic. The presented data support and extend previous studies suggesting that this novel morbillivirus is one of the phylogenetically oldest morbilliviruses known to circulate today. The relationship of DMV and established morbilliviruses to the newly emerged candidate morbillivirus infecting horse and man is discussed.

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Cetacean morbillivirus (CeMV) is an enveloped, non-segmented, negative-stranded RNA virus that infects marine mammals, spreading across species and causing lethal disease outbreaks worldwide. Among the eight proteins encoded by the CeMV genome, the haemagglutinin (H) glycoprotein is responsible for the virus attachment to host cell receptors. CeMV H represents an attractive target for antiviral and diagnostic research, yet the elucidation of the molecular mechanisms underlying its role in infection and inter-species transmission was hampered thus far due to the unavailability of recombinant versions of the protein. Here we present the cloning, expression and purification of a recombinant CeMV H ectodomain (rH-ecto), providing an initial characterization of its biophysical and structural properties. Sodium dodecyl sulphate - polyacrylamide gel electrophoresis (PAGE) combined to Western blot analysis and periodic acid Schiff assay showed that CeMV rH-ecto is purifiable at homogeneity from insect cells as a secreted, soluble and glycosylated protein. Miniaturized differential scanning fluorimetry, Blue Native PAGE and size exclusion chromatography coupled to multiangle light scattering revealed that CeMV rH-ecto is globularly folded, thermally stable and exists in solution in the oligomeric states of dimer and multiple of dimers. Furthermore, negative stain electron microscopy single particle analysis allowed us to delineate a low-resolution molecular architecture of the CeMV rH-ecto dimer, which recapitulates native assemblies from other morbilliviral H proteins, such as those from measles virus and canine distemper virus. This set of experiments by orthogonal techniques validates the CeMV rH-ecto as an experimental model for future biochemical studies on its structure and functions.
Diagnosis of Cetacean morbillivirus: A sensitive one step real time RT fast-PCR method based on SYBR<sup>®</sup> Green
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Cetacean morbillivirus (CeMV) (family Paramyxoviridae, genus Morbillivirus) is considered the most pathogenic virus of cetaceans. It was first implicated in the bottlenose dolphin (Tursiops truncatus) mass stranding episode along the Northwestern Atlantic coast in the late 1980s, and in several more recent worldwide epizootics in different Odontoceti species. This study describes a new one step real-time reverse transcription fast polymerase chain reaction (real-time RT-fast PCR) method based on SYBR^® Green to detect a fragment of the CeMV fusion protein gene. This primer set also works for conventional RT-PCR diagnosis. This method detected and identified all three well-characterized strains of CeMV: porpoise morbillivirus (PMV), dolphin morbillivirus (DMV) and pilot whale morbillivirus (PWMV). Relative sensitivity was measured by comparing the results obtained from 10-fold dilution series of PMV and DMV positive controls and a PWMV field sample, to those obtained by the previously described conventional phosphoprotein gene based RT-PCR method. Both the conventional and real-time RT-PCR methods involving the fusion protein gene were 100- to 1000-fold more sensitive than the previously described conventional RT-PCR method.
Genetic comparison among dolphin morbillivirus in the 1990-1992 and 2006-2008 Mediterranean outbreaks
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Citation Excerpt :
In the M gene, the only amino acid mutation (59 L→V) is located outside of a highly conserved region (Bolt et al., 1994). In the H gene, the only expressed mutation (164 V→A) is located outside the highly conserved hydrophobic domain between residues 29 and 61, which anchors the protein to the virus membrane (Blixenkrone-Moller et al., 1996). In MeV, the H glycoprotein stimulates the immune response, probably primarily by triggering the production of neutralizing antibodies (Rima et al., 1997).
In 1990, dolphin morbillivirus (DMV) killed thousands of striped dolphins in the Mediterranean. Subsequently, the prevalence of the infection declined in this species. In 2006–2008, the virus killed not only numerous striped dolphins but also long-finned pilot whales. All partial sequences of the phosphoprotein and nucleoprotein genes obtained thus far from different host species during the 2006–2008 outbreak show 100% identity, suggesting that a single virus was involved, and these sequences are nearly identical to the 1990 Spanish strain. Here our first objective was to determine the sequence identity between the morbillivirus from the 2006–2008 outbreak and the 1990 Spanish strain by sequencing more extensive genomic regions of strains from one pilot whale and one striped dolphin stranded in 2007. The second objective was to investigate the relationship between the 1990 and 2007 strains by constructing a phylogenetic tree based on the phosphoprotein gene to compare several Cetacean morbilliviruses, and another tree based on the nearly complete genomes of Mediterranean DMV. The third objective was to identify the most variable regions in the DMV genomes.
Results showed that the two 2007 Spanish strains were 99.9% identical over 9050 bp and should be considered the same virus, and that this virus is 99.3–99.4% similar to the 1990 Spanish strain. The phylogenetic trees, together with the common geographical area for the two outbreaks, suggest that the 2007 DMV strains evolved from the 1990 DMV strain. Pilot whales do not seem to have been exposed or infected during the 1990–1992 epidemic, since these populations appeared to be immunologically naïve in 2006–2008. Our results suggest that the virus may have evolved in striped dolphin populations prior to the 2006–2008 outbreak, after which it entered the long-finned pilot whale, perhaps aided by an alanine to valine mutation in the N-terminal domain of the fusion protein.
Phylogenetic analysis of a new Cetacean morbillivirus from a short-finned pilot whale stranded in the Canary Islands
2011, Research in Veterinary Science
Citation Excerpt :
Morbilliviral infections in cetaceans were initially described in dolphins and porpoises from European waters (Domingo et al., 1990; Kennedy et al., 1988). Subsequent publications demonstrated that these viruses though closely related differ antigenically and genetically, and should be considered strains of CeMV (Barrett et al., 1993; Blixenkrone-Moller et al., 1996; Bolt et al., 1994; Visser et al., 1993). A later report, in the Atlantic coast of USA, a long-finned pilot whale (Globicephala melas) was stranded with lesions compatible with morbilliviral infection.
Cetacean morbillivirus (CeMV) is considered the most pathogenic virus in cetaceans. Three strains have been already described: the dolphin morbillivirus (DMV), the porpoise morbillivirus (PMV) and the tentatively named pilot whale morbillivirus (PWMV).
This study describes the molecular characterization of a strain of CeMV detected in the brain of a short-finned pilot whale that had stranded in the Eastern Atlantic Ocean around the Canary Islands and that showed lesions compatible with morbilliviral disease. Sequences for the nucleoprotein, phosphoprotein, fusion protein and haemagglutinin genes were obtained. The phylogenetic study showed high homology (97%) with the PWMV strain previously detected from a long-finned pilot whale stranded in the Western Atlantic Ocean. These results support the existing classification of CeMV into three principal genetic clusters.
Genetic diversity and phylogenetic analysis of the attachment glycoprotein of phocine distemper viruses of the 2002 and 1988 epizootics
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To investigate the possible origin and spread of the dramatic re-emergent 2002 distemper epizootic observed among seals in Danish Waters, we have sequenced wild-type genes of the attachment (H) glycoproteins of viruses from both the 2002 and 1988 epizootics. Phylogenetic analysis of the H genes of phocine distemper virus (PDV) together with other morbilliviruses, suggests that the re-emergent 2002 PDV is more closely related to a putative recent ancestral PDV than the 1988 PDV isolates. Moreover, upsurges of distemper disease in land-living carnivores linked in time and locality to the 2002 seal epizootic in Danish Waters was investigated and determined to be caused by canine distemper virus, the closest relative of PDV, revealing no direct epidemiological link to the seal epizootics.
Full genome sequence of peste des petits ruminants virus, a member of the Morbillivirus genus
2005, Virus Research
Peste des petits ruminants virus (PPRV) causes an acute febrile illness in small ruminant species, mostly sheep and goats. PPRV is a member of the Morbillivirus genus which includes measles, rinderpest (cattle plague), canine distemper, phocine distemper and the morbilliviruses found in whales, porpoises and dolphins. Full length genome sequences for these morbilliviruses are available and reverse genetic rescue systems have been developed for the viruses of terrestrial mammals, with the exception of PPRV. This paper presents the first published full length genome sequence for PPRV. The genome was found to be consistent with the rule-of-six and open reading frames (ORFs) were identified that encoded the eight proteins characteristic of morbilliviruses. At the nucleotide (nt) level, the full length genome of PPRV was most similar to that of rinderpest, the other ruminant morbillivirus. However, at the protein level five of the six structural proteins and the V protein showed a greater similarity to the dolphin morbillivirus (DMV) while only the C and L proteins showed a high relationship to rinderpest.

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^☆: The nucleotide sequence reported in this paper have been submitted to the GenBank/EMBL and assigned the accession number Z36978.

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Research paperComparative analysis of the attachment protein gene (H) of dolphin morbillivirus☆

Abstract

Virology

Vet. Microbiol.

Virus. Res.

Anal. Biochem.

Vet. Microbiol.

Vet. Microbiol.

Virology

PC Gene

Sequencing and analysis of the nucleocapsid (N) and polymerase (L) genes and the terminal extragenic domains of the vaccine strain of rinderpest virus

J. Gen. Virol.

The molecular biology of morbilliviruses

Biological properties of phocine distemper virus and canine distemper virus

APMIS

Detection of IgM antibodies against canine distemper virus in dog and mink sera employing enzyme-linked immunosorbent assay (ELISA)

J. Vet. Diagn. Invest.

Antigenic relationships between field isolates of morbilliviruses from different carnivores

Arch. Virol.

Comparative analysis of the gene encoding the nucleocapsid protein of dolphin morbillivirus reveals its distant evolutionary relationship to measles virus and ruminant morbilliviruses

J. Gen. Virol.

Measles virus L protein evidences elements of ancestral RNA polymerase

Virology

Altered transcription of a defective measles virus genome derived from a human brain

EMBO J.

Enzyme immunoassay versus plaque neutralization and other methods for determination of immune status to measles and varicella-zoster viruses and versus complement fixation for serodiagnosis of infections with those viruses

J. Clin. Microbiol.

The nucleotide sequence of the gene encoding the attachment protein H of canine distemper virus

J. Gen. Virol.

Molecular characterization of phocine distemper virus: gene order and sequence of the gene encoding the attachment (H) protein

J. Gen. Virol.

A comprehensive set of sequence analysis programs for the VAX

Nucleic Acid Res.

Morbillivirus in dolphins

Nature

Morbillivirus infection in two species of Pilot Whale (Globicephala sp.) from the western Atlantic

Mar. Mamm. Sci.

Confidence limits on phylogenies: an approach using bootstrap

Evolution

Annotated nucleotide and protein sequences for selected Paramyxovirudae

Research paper
Comparative analysis of the attachment protein gene (H) of dolphin morbillivirus☆