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Feline Morbillivirus, a New Paramyxovirus Possibly Associated with Feline Kidney Disease

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Feline Morbillivirus, a New Paramyxovirus Possibly Associated with Feline Kidney Disease viruses Review Feline Morbillivirus, a New Paramyxovirus Possibly Associated with Feline Kidney Disease 1, 2, 1,2, Eun Jin Choi y , Victoria Ortega y and Hector C. Aguilar * 1 Department of Microbiology, Cornell University, Ithaca, NY 14853, USA; [email protected] 2 Department of Microbiology and Immunology, College of Veterinary Medicine, Cornell University, Ithaca, NY 14850, USA; [email protected] * Correspondence: [email protected]; Tel.: +1-607-253-4029 These authors contributed equally to this work. y Received: 22 March 2020; Accepted: 28 April 2020; Published: 1 May 2020 Abstract: Feline morbillivirus (FeMV) was first isolated in stray cats in Hong Kong in 2012. Since its discovery, the virus has been reported in domestic cats worldwide, including in Hong Kong, Japan, Italy, US, Brazil, Turkey, UK, Germany, and Malaysia. FeMV is classified in the Morbillivirus genus within the Paramyxoviridae family. FeMV research has focused primarily on determining the host range, symptoms, and characteristics of persistent infections in vitro. Importantly, there is a potential association between FeMV infection and feline kidney diseases, such as tubulointerstitial nephritis (TIN) and chronic kidney diseases (CKD), which are known to significantly affect feline health and survival. However, the tropism and viral entry mechanism(s) of FeMV remain unknown. In this review, we summarize the FeMV studies up to date, including the discoveries of various FeMV strains, basic virology, pathogenicity, and disease signs. Keywords: chronic kidney disease; feline morbillivirus; paramyxovirus; persistent infection; tubulointerstitial nephritis 1. Introduction FeMV Belongs to Family Paramyxoviridae Paramyxoviruses are enveloped, non-segmented, negative-sense, single-stranded RNA viruses [1,2]. They infect a large variety of mammalian hosts, such as humans, mice, pandas, hyenas, whales, bats, rats, dogs, and cats, as well as non-mammalian hosts, such as birds and reptiles [1,3–7]. Many pathogenic viruses within the Paramyxoviridae family significantly affect animal and human health. Examples include measles virus (MeV), mumps virus (MuV), Newcastle disease virus (NDV), Rinderpest virus (RPV), and the highly pathogenic zoonotic Hendra virus (HeV) and Nipah virus (NiV) [1,4,8,9]. Therefore, the outbreak of these viruses can cause critical human and veterinary health burden, as well economic damage to several livestock industries [10–13]. The Morbillivirus genus within the Paramyxoviridae family contains highly infectious animal viruses, including peste-des-petits-ruminants virus (PPRV), canine distemper virus (CDV), and cetacean morbillivirus (CeMV), which can cause severe and sometimes fatal systemic disorders [14–16]. In 2012, a previously unknown virus now named feline morbillivirus (FeMV, formerly abbreviated FmoPV), was discovered in Hong Kong to infect cats and subsequently classified in the Morbillivirus genus [1,17,18]. There are six genes in the paramyxovirus genome arranged in order 30-N-P/V/W/C-M-F-HN/ H/G-L-50 [1]. The negative-strand RNA is tightly bound to the nucleocapsid (N) protein and forms a ribonucleoprotein complex (RNP) along with the large (L) RNA-dependent RNA polymerase and the phosphoprotein (P) [19]. The matrix protein (M) is a non-glycosylated peripheral Viruses 2020, 12, 501; doi:10.3390/v12050501 www.mdpi.com/journal/viruses Viruses 2020, 12, 501 2 of 10 membraneViruses 2020, protein 12, x FOR involvedPEER REVIEW in virus particle assembly and budding [20,21]. Viral attachment2 of 11 and entry into target cells depend on two surface glycoproteins, the fusion (F) and the attachment protein involved in virus particle assembly and budding [20,21]. Viral attachment and entry into or receptor binding [hemagglutinin–neuraminidase (HN)/hemagglutinin (H)/glycoprotein (G)] target cells depend on two surface glycoproteins, the fusion (F) and the attachment or receptor glycoproteins [3,22]. Paramyxovirus attachment glycoproteins bind to cellular receptors, such as binding [hemagglutinin–neuraminidase (HN) / hemagglutinin (H) / glycoprotein (G)] glycoproteins neuraminidase– proteinaceous receptors (for HN), ephrinB2 and ephrinB3 (for G), and SLAM (also [3,22]. Paramyxovirus attachment glycoproteins bind to cellular receptors, such as neuraminidase– knownproteinaceous as CD150, receptors for H) (for [23 –HN),26]. ephrinB2 After receptor and ephrinB3 binding, (for the G), two and surfaceSLAM (also glycoproteins known as CD150, undergo conformationalfor H) [23–26]. changes After receptor and trigger binding, F to the undergo two surface the viral-cell glycoproteins membrane undergo fusion conformational cascade that changes results in viraland entry. trigger This F to process undergo facilitates the viral fusion-cell membrane of viral and fusion host cellcascade membranes that results and in viral viral entry entry. into This host cellsprocess [27,28 facilitates]. fusion of viral and host cell membranes and viral entry into host cells [27,28]. 2. Discovery2. Discovery of of Various Various FeMV FeMV Strains Strains FeMVFeMV is anis emergingan emerging morbillivirus morbillivirus that that has has been been isolated isolated and studiedand studied by numerous by numerous research research groups worldwide.groups worldwide. Cats infected Cats infected with FeMV with have FeMV been have detected been detected in Hong in Hong Kong, Kong, Japan, Japan, Italy, Italy, United United States, Brazil,States, Turkey, Brazil, UnitedTurkey, Kingdom, United Kingdom, Germany, Germany Malaysia, Malaysia (Figure (Fig1).ure FeMV 1). FeMV RNA RNA was firstwas first detected detected in 56 outin of 56 457 out stray of 457 cats stray (12.3%, cats (12.3%, 53 urine 53 samples, urine samples, four rectal four swabsrectal swabs and one and blood one blood sample) sample) by reverse by transcriptionreverse transcription polymerase polymerase chain reaction chain (RT-PCR)reaction (RT utilizing-PCR) utilizing consensus consensus primers primers designed designed using the partialusing sequence the partial of thesequence morbillivirus of the m Lorbillivirus gene, a highly L gene, conserved a highly sequence conserved within sequence the genome within [the1,10 ]. Thegenome three complete [1,10]. The genome three complete sequences genome (761U, 776U,sequences and M252A)(761U, 776U, hadless and than M252A) 80% nucleotidehad less than identities 80% to knownnucleotide paramyxoviruses identities to known [1]. The paramyxoviruses three genomes [ followed1]. The three the genomes characteristic followed paramyxovirus the characteristic genome layout,paramyxovir the ruleus of genome six, and layout, the herringbone the rule of nucleoproteinsix, and the herringbone morphology nucleoprotein [1,29,30]. Based morphology on these observations[1,29,30]. Based and theon these phylogenetic observations analysis, and the the phylogenetic three strains analysis, were added the three to the strainsMorbillivirus were addedgenus to [ 1]. the Morbillivirus genus [1]. FigureFigure 1. 1World. World map map showing showingthe the countriescountries with reported FeMV FeMV infections infections in in felines felines inin red red.. SinceSince then, then, new new FeMV FeMV strainsstrains havehave beenbeen continuously isolated isolated from from cat cat urine urine samples samples and and identifiedidentified by by RT-PCR RT-PCR based based on on the the partial partial LL genegene sequences.sequences. In In 2014, 2014, viral viral RNA RNA was was de detectedtected in infive five outout of of 82 82 urine urine samples samples (6.1%) (6.1%) and and one one amongamong tenten bloodblood samples (10%) (10%) in in Japan. Japan. The The six six unknown unknown virusesviruses were were determined determined to to be be FeMV FeMV strainsstrains (SE4, CL5, SE7, SE7, SE14, SE14, MS25, MS25, and and MS26), MS26), as asthey they shared shared 92–94%92-94% identity identity with with the the three three viruses viruses identifiedidentified in Hong Kong Kong [31 [31].]. Furthermore, Furthermore, three three strains strains (SS1, (SS1, SS2SS2 and and SS3) SS3) were were isolated isolated from from 13 13 cat cat urine urine samplessamples and had a 90 90–99%-99% nucleotide nucleotide similarity similarity to tothe the isolatesisolates from from Hong Hong Kong. Kong. SS3 SS3 showed showed anan aroundaround 99% similarity to to strain strain M252A M252A [32 [32]. ].Based Based on on the the high similarity between FeMV strains identified in Japan and Hong Kong, the researchers suggested 2 Viruses 2020, 12, 501 3 of 10 high similarity between FeMV strains identified in Japan and Hong Kong, the researchers suggested a possible transmission of FeMV by unidentified vectors. For instance, infected cats may have been transported between the two countries [32]. Partial L gene sequences of FeMV strains were amplified using RT-PCR from samples such as cat urine, kidney, and blood [2,31]. The large protein sequences from the different FeMV strains were aligned in Figure2. Whole genome sequences of some viruses were determined by various techniques, such as overlapping RT-PCR amplicons, next-generation sequencing (NGS), and sequence-independent single primer amplification (SISPA) [2,5]. The partial and whole genome sequences known to date are shown in Table1. MiJP003 is one of the FeMV strains whose complete genome sequence has been determined [2]. Interestingly, the genomic organization and the similarity analysis results showed that theViruses intragenomic 2020, 12, x regionFOR PEER between REVIEW F and H is different from other
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