A Model of the Anterior Esophagus in Snakes, with Functional and Developmental Implications

Cundall, David; Tuttman, Cassandra; Close, Matthew

doi:10.1002/ar.22860

Cited by 24 publications

(25 citation statements)

References 39 publications

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“…We found further evidence of that and of its pathogenicity, as we detected nidovirus N protein within a focal granulomatous-necrotizing nephritis in one animal. We also detected viral antigen in epithelial cells of the cranial esophagus in one affected animal; however, in M. viridis the esophagus carries a ciliated epithelium (data not shown), a feature also known for other snake species (57,58); infection could therefore be due to an overspill from the trachea and nasal cavity. We did not detect viral antigen in any cells of the stomach or intestine, and a previous study also did not find viral RNA by RNA-ISH, suggesting that the python nidoviruses are primarily respiratory (8).…”

Section: Fig 10mentioning

confidence: 60%

Nidovirus-Associated Proliferative Pneumonia in the Green Tree Python (Morelia viridis)

Dervas

Hepojoki

Laimbacher

et al. 2017

J Virol

117

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In 2014 we observed a noticeable increase in sudden deaths of green tree pythons (). Pathological examination revealed accumulation of mucoid material within airways and lung, associated with enlargement of the entire lung. We performed full necropsy and histological examination on 12 affected green tree pythons from 7 different breeders to characterise the pathogenesis of this "mucinous" pneumonia. By histology we could show a marked hyperplasia of the airway epithelium and of faveolar type II pneumocytes. Since routine microbiological tests failed to identify a causative agent, we studied lung samples of a few diseased snakes by next-generation sequencing (NGS). From the NGS data we could assemble a piece of RNA genome <85% identical to nidoviruses previously identified in ball pythons and Indian pythons. We then employed RT-PCR to demonstrate the presence of the novel nidovirus in all diseased snakes. To attempt virus isolation, we established primary cell cultures of liver and brain, which we inoculated with lung homogenates of infected individuals. Ultrastructural examination of concentrated cell culture supernatants showed the presence of nidovirus particles, and subsequent NGS analysis yielded the full genome of the novel virus, Morelia viridis nidovirus (MVNV). We then generated an antibody against MVNV nucleoprotein, which we used alongside RNA hybridisation to demonstrate viral antigen and RNA in the affected lungs. This suggests that in natural infection MVNV damages the respiratory tract epithelium which then results in epithelial hyperplasia, most likely as an exaggerated regenerative attempt in association with increased epithelial turnover. Fairly recently novel nidoviruses associated with severe respiratory disease were identified in ball pythons and Indian pythons. Herein we report isolation and identification of a further nidovirus from green tree pythons () with fatal pneumonia. We thoroughly characterize the pathological changes in the infected individuals, and show that nidovirus infection is associated with marked epithelial proliferation in the respiratory tract. We speculate that this and the associated excess mucus production can lead to the animals' death, by inhibitingthe normal gas exchange in the lung. The virus was predominantly detected in the respiratory tract, which renders transmission via the respiratory route likely. Nidoviruses cause sudden outbreaks with high mortality in breeding collections, most affected snakes die without prior clinical signs. These findings, together with those of other groups, indicate that nidoviruses are a likely cause of severe pneumonia in pythons.

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Section: Fig 10mentioning

confidence: 60%

Nidovirus-Associated Proliferative Pneumonia in the Green Tree Python (Morelia viridis)

Dervas

Hepojoki

Laimbacher

et al. 2017

J Virol

117

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“…However, studies of postnatal ontogeny can be crucial in revealing new information about organismal biology and evolution [8]. For example, macrostomy—or large-gaped feeding—is a fundamental and anatomically complex feature of the body plan of most extant snakes and has been hypothesized as one of the major factors enabling the diversification of this group [8,9]. Initially considered to have evolved only once [10], recent analyses of the postnatal cranial development of various major snake groups have revealed the macrostomatan condition to be achieved via different developmental pathways in different groups of snakes, suggesting that this feature is homoplastic [6].…”

Section: Introductionmentioning

confidence: 99%

Cranial ontogeny of Thamnophis radix (Serpentes: Colubroidea) with a re-evaluation of current paradigms of snake skull evolution

2019

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Accurate knowledge of skeletal ontogeny in extant organisms is crucial in understanding important morpho-functional systems and in enabling inferences of the ontogenetic stage of fossil specimens. However, detailed knowledge of skeletal ontogeny is lacking for most squamates, including snakes. Very few studies have discussed postnatal development in snakes, with none incorporating data from all three major ontogenetic stages—embryonic, juvenile and adult. Here, we provide the first analysis encompassing these three ontogenetic stages for any squamate, using the first complete micro-computed tomography (micro-CT)-based segmentations of any non-adult snake, based on fresh specimens of Thamnophis radix . The most significant ontogenetic changes involve the feeding apparatus, with major elongation of the tooth-bearing elements and jaw suspensorium causing a posterior shift in the jaw articulation. This shift enables macrostomy (large-gaped feeding in snakes) and occurs in T. radix via a different developmental trajectory than in most other macrostomatans, indicating that the evolution of macrostomy is more complex than previously thought. The braincase of T. radix is also evolutionarily unique among derived snakes in lacking a crista circumfenestralis, a phenomenon considered herein to represent paedomorphic retention of the embryonic condition. We thus present numerous important challenges to current paradigms regarding snake cranial evolution.

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“…In some snakes, we additionally observed an esophagitis; this is interpreted as a consequence of overspill and swallowing of virus-laden mucus, a theory also supported by previous studies (6, 7, 40). It is possible that the esophagus is involved because its epithelium contains ciliated cells in various snake species (13), and ciliated cells represent the primary site of viral replication, a feature also shown for human coronaviruses (13, 41, 42).…”

Section: Discussionmentioning

confidence: 99%

“…The infection was associated with necrotizing cystitis, nephritis, adenitis and vasculitis, and the presence of viral RNA in many tissues, indicating systemic spread of the virus (12). The target cell spectrum of python nidoviruses includes the epithelium of the respiratory tract and lungs (6), and in some cases also the oral cavity and the cranial esophagus (5–7, 11), the mucosa of which exhibits ciliated epithelium in snakes (13). Thus far little is known about the intra- and interspecies transmission of python nidoviruses.…”

Section: Introductionmentioning

confidence: 99%

Python nidoviruses, more than respiratory pathogens

Dervas

Hepojoki

Smura

et al. 2020

Preprint

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28In recent years nidoviruses have emerged as an important respiratory pathogen of reptiles, 29 affecting especially captive python populations. In pythons, nidovirus infection induces an 30 inflammation of the upper respiratory and alimentary tract which can develop into a severe and 31 often fatal proliferative pneumonia. We observed pyogranulomatous and fibrinonecrotic lesions 32 in organ systems other than the respiratory tract during full post mortem examinations on 30 33 nidovirus RT-PCR positive pythons of varying species originating from Switzerland and Spain. 34The observations prompted us to study whether the atypical tissue tropism associates with 35 previously unknown nidoviruses or changes in the nidovirus genome. RT-PCR and inoculation 36 of Morelia viridis cell cultures served to recruit the cases and to obtain virus isolates. 37 Immunohistochemistry and immunofluorescence staining against nidovirus nucleoprotein 38 demonstrated that the virus not only infects a broad spectrum of epithelial (respiratory and 39 alimentary epithelium, hepatocytes, renal tubules, pancreatic ducts etc.), but also intravascular 40 monocytes, intralesional macrophages and endothelial cells. By next-generation sequencing we 41 obtained full length genome for a novel nidovirus species circulating in Switzerland. Analysis of 42 viral genomes recovered from pythons showing nidovirus infection-associated respiratory or 43 systemic disease did not explain the observed phenotypes. The results indicate that python 44 nidoviruses have a broad cell and tissue tropism, further suggesting that the course of infection 45 could vary and involve lesions in a broad spectrum of tissues and organ systems as a 46 consequence of monocyte-mediated systemic spread of the virus. 47 IMPORTANCE 49During the last years, python nidoviruses have become a primary cause of fatal disease in 50 pythons. Nidoviruses represent a threat to captive snake collections, as they spread rapidly and 51 can be associated with high morbidity and mortality. Our study indicates that, different from 52 previously evidence, the viruses do not only affect the respiratory tract, but can spread in the 53 entire body with blood monocytes, have a broad spectrum of target cells, and can induce a 54 variety of lesions. Nidovirales is an order of animal and human viruses that compromise 55 important zoonotic pathogens such as MERS-CoV and SARS-CoV, as well as the recently 56 emerged SARS-CoV-2. Python nidoviruses belong to the same subfamily as the mentioned 57 human viruses and show similar characteristics (rapid spread, respiratory and gastrointestinal 58 tropism, etc.). The present study confirms the relevance of natural animal diseases to better 59 understand the complexity of viruses of the order nidovirales.

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A Model of the Anterior Esophagus in Snakes, with Functional and Developmental Implications

Cited by 24 publications

References 39 publications

Nidovirus-Associated Proliferative Pneumonia in the Green Tree Python (Morelia viridis)

Nidovirus-Associated Proliferative Pneumonia in the Green Tree Python (Morelia viridis)

Cranial ontogeny of Thamnophis radix (Serpentes: Colubroidea) with a re-evaluation of current paradigms of snake skull evolution

Python nidoviruses, more than respiratory pathogens

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