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Cervid Prion Protein Polymorphisms: Role in Chronic Wasting Disease Pathogenesis

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Cervid Prion Protein Polymorphisms: Role in Chronic Wasting Disease Pathogenesis International Journal of Molecular Sciences Review Cervid Prion Protein Polymorphisms: Role in Chronic Wasting Disease Pathogenesis Maria Immaculata Arifin 1,2,3, Samia Hannaoui 1,2,3, Sheng Chun Chang 1,2,3, Simrika Thapa 1,2,3, Hermann M. Schatzl 1,2,3 and Sabine Gilch 1,2,3,* 1 Department of Comparative Biology & Experimental Medicine, Faculty of Veterinary Medicine, University of Calgary, Calgary, AB T2N 4N1, Canada; maria.arifi[email protected] (M.I.A.); [email protected] (S.H.); [email protected] (S.C.C.); [email protected] (S.T.); [email protected] (H.M.S.) 2 Calgary Prion Research Unit, University of Calgary, Calgary, AB T2N 4N1, Canada 3 Hotchkiss Brain Institute, University of Calgary, Calgary, AB T2N 4N1, Canada * Correspondence: [email protected] Abstract: Chronic wasting disease (CWD) is a prion disease found in both free-ranging and farmed cervids. Susceptibility of these animals to CWD is governed by various exogenous and endogenous factors. Past studies have demonstrated that polymorphisms within the prion protein (PrP) sequence itself affect an animal’s susceptibility to CWD. PrP polymorphisms can modulate CWD pathogenesis in two ways: the ability of the endogenous prion protein (PrPC) to convert into infectious prions (PrPSc) or it can give rise to novel prion strains. In vivo studies in susceptible cervids, complemented by studies in transgenic mice expressing the corresponding cervid PrP sequence, show that each polymorphism has distinct effects on both PrPC and PrPSc. It is not entirely clear how these polymor- phisms are responsible for these effects, but in vitro studies suggest they play a role in modifying PrP epitopes crucial for PrPC to PrPSc conversion and determining PrPC stability. PrP polymorphisms Citation: Arifin, M.I.; Hannaoui, S.; are unique to one or two cervid species and most confer a certain degree of reduced susceptibility to Chang, S.C.; Thapa, S.; Schatzl, H.M.; Gilch, S. Cervid Prion Protein CWD. However, to date, there are no reports of polymorphic cervid PrP alleles providing absolute Polymorphisms: Role in Chronic resistance to CWD. Studies on polymorphisms have focused on those found in CWD-endemic areas, Wasting Disease Pathogenesis. Int. J. with the hope that understanding the role of an animal’s genetics in CWD can help to predict, contain, Mol. Sci. 2021, 22, 2271. https:// or prevent transmission of CWD. doi.org/10.3390/ijms22052271 Keywords: chronic wasting disease; prion protein; cervid; polymorphism; strain; pathogenesis Academic Editor: Byung-Hoon Jeong Received: 31 January 2021 Accepted: 22 February 2021 1. Introduction Published: 25 February 2021 Chronic wasting disease (CWD) is a prion disease, or transmissible spongiform en- cephalopathy (TSE), found in cervid species, such as elk, deer, reindeer, and moose [1]. It is Publisher’s Note: MDPI stays neutral an infectious and fatal neurodegenerative disease with no prophylaxis or cure available [1]. with regard to jurisdictional claims in Prions are proteinaceous infectious particles consisting of PrPSc, an abnormally folded published maps and institutional affil- C C iations. and infectious isoform of the endogenous prion protein (PrP ). Prions can convert PrP into PrPSc, leading to accumulation of aggregated PrPSc in the central nervous system (CNS) and ultimately death [2]. Pronounced weight loss is a hallmark in animals with CWD, thus the term ‘wasting disease’ [1]. Another important feature of CWD is that CWD prions, abbreviated as PrPCWD here onwards, are very contagious [1]. This is because Copyright: © 2021 by the authors. PrPCWD disseminates throughout the body of the infected cervid. PrPCWD has been de- Licensee MDPI, Basel, Switzerland. tected in the lymphatic system, salivary gland, intestinal tract, muscles, and blood, as This article is an open access article well as urine, saliva, and feces, of infected cervids [3–14]. PrPCWD is released into the distributed under the terms and conditions of the Creative Commons environment through bodily fluids and excreta and bind to soil and plants, remaining in- CWD Attribution (CC BY) license (https:// fectious even after decades [15–19]. Prolonged PrP shedding and its persistence in the creativecommons.org/licenses/by/ environment leads to efficient lateral transmission between both farmed and free-ranging 4.0/). cervids [10,14,20–23]. Int. J. Mol. Sci. 2021, 22, 2271. https://doi.org/10.3390/ijms22052271 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 2 of 24 CWD was first reported by the late E.S. Williams in captive mule deer in Colorado in Int. J. Mol. Sci. 2021, 22, 2271 2 of 24 the 1970s [24] and later on in free-ranging elk in 1981 [25]. In 1996, Saskatchewan reported the first case of CWD in Canada [26]. The disease was also reported in South Korea as a case of imported elk fromCWD Canada was first [27] reported. CWD by the is late currently E.S. Williams found in captive in 26 mule U. deerS. states in Colorado and in3 Canadian provinces the(Figure 1970s [ 241)] and[28] later. This on in efficien free-rangingt spread elk in 1981 highlight [25]. In 1996,s the Saskatchewan contagiousness reported the first case of CWD in Canada [26]. The disease was also reported in South Korea as and difficulty to containa case CWD. of imported Wild elk and from Canadafarmed [27 cervid]. CWD species is currently known found in to 26 be U.S. naturally states and affected by CWD in3 North Canadian America provinces (Figureinclude1)[ 28white]. This-tailed efficient deer spread ( highlightsOdocoileus the virginianus contagiousness), mule deer (O. hemionusand), difficulty elk (Cervus to contain canadensis CWD. Wild), red and farmeddeer (C. cervid elaphus species), knownand moose to be naturally (Alces affected by CWD in North America include white-tailed deer (Odocoileus virginianus), mule alces sp.) [29]. In 2016,deer the (O. first hemionus case), of elk CWD (Cervus in canadensis Europe), redwas deer reported (C. elaphus in), free and moose-ranging (Alces Nor- alces wegian reindeer (Rangifersp.) [29 ].tarandus In 2016, the tarandus first case) of, followed CWD in Europe by wasreports reported in inred free-ranging deer and Norwegian moose [30,31]. It was also recentlyreindeer (reporRangiferted tarandus in moose tarandus in), followedFinland by and reports Sweden in red deer (Figure and moose 2) [32 [30,–3134]]. It. To date, the origin ofwas CWD also recentlyis not well reported known. in moose in Finland and Sweden (Figure2)[ 32–34]. To date, the origin of CWD is not well known. FigureFigure 1.1.Chronic Chronic wasting wasting disease disease (CWD) distribution(CWD) distribution in North America. in North Courtesy America of the U.S.. C Geologicalourtesy Survey of the National U.S. Geo- Wildlife Health Center. logical Survey National Wildlife Health Center. Int. J. Mol. Sci. 2021, 22, 2271 3 of 24 Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 3 of 24 moose reindeer red deer 3 1 1 1 1 3 Sweden Norway Finland 19 2 FigureFigure 2.2. Chronic wasting wasting disease disease (CWD) (CWD) distribution distribution in inScandinavia Scandinavia,, based based on onMysterud Mysterud et al et., al., 2020 [35]. Numbers in circles represent the number of CWD-positive animals. 2020 [35]. Numbers in circles represent the number of CWD-positive animals. WhileWhile CWDCWD isis efficientlyefficiently transmittedtransmitted among and between cervid species, prions in in generalgeneral dodo notnot easilyeasily transmittransmit from their main host species to other species due to the presencepresence ofof transmissiontransmission barriersbarriers [[3636––4242]].. The host’s PrP primary sequence homology withwith thethe incomingincoming PrPPrPScSc is anan importantimportant factor inin thethe PrPPrPC to PrP Sc conversionconversion [38,43 [38,43––4545]].. MismatchMismatch betweenbetween thethe substratesubstrate (PrP(PrPC)) and template (PrP Sc)) can can result result in in less less efficient efficient conversionconversion andand hinderhinder disease disease transmission transmission [46 [46–48–48]]. Furthermore,. Furthermore, the the replication replication environ- envi- mentronment and and presence presence of cofactors of cofactors also also play play a role a role in successfulin successful prion prion propagation propagation [49 –[4956–]. Studies56]. Studies show show that differentthat different prion prion conformers conformers or strains or strains canpropagate can propagate within within a single a single host, resultinghost, resulting in a prion in a prion ‘cloud’ ‘cloud’ or isolate, or isolate, containing containing a mixture a mixture of strains of strains [57–60 [57]. The–60] prion. The strainprion conceptstrain concept is highly is highly debated, debated, but the but generally the generally accepted accepted notion notion is that is when that when a prion a inoculumprion inoculum retains retains its disease its disease phenotype phenotypein vivo inand vivo biochemical and biochemical features featuresin vitro throughin vitro serialthrough passages, serial passage it is recognizeds, it is recognized as a distinct as a straindistinct [41 strain,61–67 [].41, However,61–67]. However, prions can prions also ‘jump’can also from ‘jump one’ species from one to another, species including to another, zoonotic including transmission. zoonotic Antransmission. important exampleAn im- ofportant this phenomenon example of isthis bovine phenomenon spongiform is bovine encephalopathy spongiform (BSE) encephalopathy that was transmitted (BSE) that to humanswas transmitted
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