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Coronavirus Infections in Companion Animals: Virology, Epidemiology, Clinical and Pathologic Features

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Coronavirus Infections in Companion Animals: Virology, Epidemiology, Clinical and Pathologic Features viruses Review Coronavirus Infections in Companion Animals: Virology, Epidemiology, Clinical and Pathologic Features Christine Haake 1,* , Sarah Cook 2, Nicola Pusterla 3 and Brian Murphy 4 1 School of Veterinary Medicine, University of California, Davis, CA 95616, USA 2 Graduate Group Integrative Pathobiology, School of Veterinary Medicine, University of California, Davis, CA 95616, USA; [email protected] 3 Department of Medicine & Epidemiology, School of Veterinary Medicine, University of California, Davis, CA 95616, USA; [email protected] 4 Department of Pathology, Microbiology, and Immunology, School of Veterinary Medicine, University of California, Davis, CA 95616, USA; [email protected] * Correspondence: [email protected] Received: 28 July 2020; Accepted: 11 September 2020; Published: 13 September 2020 Abstract: Coronaviruses are enveloped RNA viruses capable of causing respiratory, enteric, or systemic diseases in a variety of mammalian hosts that vary in clinical severity from subclinical to fatal. The host range and tissue tropism are largely determined by the coronaviral spike protein, which initiates cellular infection by promoting fusion of the viral and host cell membranes. Companion animal coronaviruses responsible for causing enteric infection include feline enteric coronavirus, ferret enteric coronavirus, canine enteric coronavirus, equine coronavirus, and alpaca enteric coronavirus, while canine respiratory coronavirus and alpaca respiratory coronavirus result in respiratory infection. Ferret systemic coronavirus and feline infectious peritonitis virus, a mutated feline enteric coronavirus, can lead to lethal immuno-inflammatory systemic disease. Recent human viral pandemics, including severe acute respiratory syndrome (SARS), Middle East respiratory syndrome (MERS), and most recently, COVID-19, all thought to originate from bat coronaviruses, demonstrate the zoonotic potential of coronaviruses and their potential to have devastating impacts. A better understanding of the coronaviruses of companion animals, their capacity for cross-species transmission, and the sharing of genetic information may facilitate improved prevention and control strategies for future emerging zoonotic coronaviruses. This article reviews the clinical, epidemiologic, virologic, and pathologic characteristics of nine important coronaviruses of companion animals. Keywords: feline infectious peritonitis; coronavirus; canine; ferrets; spike glycoproteins; SARS Virus; COVID-19; zoonoses 1. Introduction Coronaviruses are spherical, enveloped, single-stranded, positive-sense RNA viruses within the family Coronaviridae, named for the ultrastructural “crown-like” (corona) appearance of the spike proteins on the virion surface. Coronaviruses infect humans as well as many other mammalian and avian species, generally causing variably severe intestinal, respiratory, neurologic, or systemic disease syndromes [1–4]. Genomically, coronaviruses are among the largest of the RNA viruses, with genomes spanning 27.6 to 31 kilobases (kb) in length [5], approximately three times the size of most retroviruses. On the basis of comparative genome sequence analyses, coronaviruses are subdivided into four genera: alphacoronavirus, betacoronavirus, gammacoronavirus, and deltacoronavirus. Alpha- and betacoronaviruses originate from bats and predominantly infect mammals, while gamma- Viruses 2020, 12, 1023; doi:10.3390/v12091023 www.mdpi.com/journal/viruses Viruses 2020, 12, x FOR PEER REVIEW 2 of 22 Viruses 2020, 12, 1023 2 of 22 Alpha- and betacoronaviruses originate from bats and predominantly infect mammals, while gamma- and deltacoronaviruses originate from birds and are capable of infecting both bird and andmammal deltacoronaviruses species [6]. Companion originate animals from birds presently and areconsidered capable include of infecting cats, dogs, both ferrets, bird and horses, mammal and speciesalpacas. [6 While]. Companion not universally animals recognized presently consideredas companion include animals, cats, alpacas dogs, ferrets,and horses horses, are andconsidered alpacas. Whileby the not authors universally to be recognized companion as animals companion and animals,are therefore alpacas included and horses in this are consideredreview. Notable by the authorscoronaviruses to be companion of companion animals animals and are include therefore feline included enteric in coronavirus this review. (FECV), Notable feline coronaviruses infectious of companionperitonitis animalsvirus (FIPV), include canine feline enteric enteric coronaviru coronaviruss (CCoV), (FECV), ferret feline enteric infectious coronavirus peritonitis (FRECV), virus (FIPV),ferret caninesystemic enteric coronavirus coronavirus (FRSCV), (CCoV), and ferret alpaca enteric respiratory coronavirus coronavirus, (FRECV), which ferret are systemicalphacoronaviruses, coronavirus (FRSCV),and canine and respiratory alpaca respiratory coronavirus coronavirus, (CRCoV), whichequine areenteric alphacoronaviruses, coronavirus (ECoV), and and canine alpaca respiratory enteric coronaviruscoronavirus, (CRCoV), which are equine betacoronavi entericruses coronavirus [7]. Phylogenetic (ECoV), and relation alpacaships enteric of these coronavirus, coronaviruses which are are betacoronavirusesshown in Figure [1,7]. while Phylogenetic clinical and relationships pathologic of features these coronaviruses are summarized are shownin Table in 1. Figure Other1, whilecoronaviruses clinical and belonging pathologic to the features betacoronavirus are summarized genus in include Table1. SARS-CoV-1, Other coronaviruses MERS-CoV, belonging and SARS- to the betacoronavirusCoV-2, zoonotic genus coronaviruses include SARS-CoV-1, that have recently MERS-CoV, transferred and SARS-CoV-2, from animal zoonoticto human coronaviruses populations and that haveare capable recently of transferred causing severe from animaldisease toand human death populations [8]. The ability and of are SARS-CoV-2 capable of causing to initiate severe infections disease andin companion death [8]. animals The ability is currently of SARS-CoV-2 poorly understood, to initiate infections although preliminary in companion studies animals have is indicated currently poorlythat ferrets understood, and cats although are permissive preliminary for SARS-CoV-2 studies have infection indicated and that replication, ferrets and while cats arethepermissive virus has forbeen SARS-CoV-2 shown to replicate infection poorly and replication, in dogs, pigs, while chicke thens, virus and has ducks been [9]. shown SARS-CoV-2 to replicate infection poorly of inhorses dogs, pigs,and chickens,camelids has and not ducks been [9 reported.]. SARS-CoV-2 infection of horses and camelids has not been reported. Figure 1. Phylogenetic relationships of coronaviruses of companion animals. The 3 portions of the Figure 1. Phylogenetic relationships of coronaviruses of companion animals. The 3′0 portions of the coronaviral genomes encoding the spike and other non-structural proteins (~9 kb) were compared coronaviral genomes encoding the spike and other non-structural proteins (~9 kb) were compared and plotted as a “guide tree” using MacVector software (ClustalW Multiple Sequence Alignment). and plotted as a “guide tree” using MacVector software (ClustalW Multiple Sequence Alignment). BetacoronavirusBetacoronavirus sequences sequences are are highlighted highlighted in yellow, in yellow, while alphacoronavirus while alphacoronavirus sequences sequences are highlighted are inhighlighted blue; the zoonoticin blue; the SARS zoonotic CoV-2 SARS coronavirus CoV-2 iscoronavirus surrounded is surrounded by a red box. by GenBanka red box. submission GenBank numberssubmission are numbers indicated are for indicated each sequence. for each sequence. Coronavirus genomes encode three classes of proteins: structural, accessory, and non-structural Coronavirus genomes encode three classes of proteins: structural, accessory, and non-structural proteins. Major structural proteins of coronaviruses include the nucleocapsid (N), spike (S), membrane proteins. Major structural proteins of coronaviruses include the nucleocapsid (N), spike (S), (M), and envelope (E) proteins [5]. The S protein is the primary viral binding protein and mediator membrane (M), and envelope (E) proteins [5]. The S protein is the primary viral binding protein and ofmediator membrane of membrane fusion and fusion viral and entry. viral The entry. N protein, The N protein, in close in association close association with genomicwith genomic viral viral RNA (gRNA),RNA (gRNA), forms forms the helical the helical nucleocapsid, nucleocapsid, which which is stabilized is stabilized via bindingvia binding to theto the M M protein protein (Figure (Figure2). The2). viralThe viral genome genome and helicaland helical nucleocapsid nucleocapsid are surrounded are surrounded by a host-derivedby a host-derived lipid bilayer,lipid bilayer, in which in thewhich S, E, the and S, ME, proteinsand M proteins are anchored. are anchored. The transmembrane The transmembrane E and ME and proteins M proteins are involved are involved in virion in assemblyvirion assembly and budding and budding [10]. In [10]. addition In addition to the to four the structuralfour structur proteins,al proteins, coronavirus coronavirus genomes genomes also encodealso encode a number a number of accessory of accessory proteins. proteins. While While the roles the ofroles most of ofmost the of accessory the accessory proteins proteins remain remain poorly understoodpoorly
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