Prion and prion-like diseases in animals

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Contents lists available at ScienceDirect

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Prion and prion-like diseases in animals

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Patricia Aguilar-Calvo a , Consolación García a , Juan Carlos Espinosa a , Olivier Andreoletti b , Juan María Torres a,∗ a b

Centro de Investigación en Sanidad Animal (CISA-INIA), 28130 Valdeolmos, Madrid, Spain INRA, UMR 1225, Interactions Hôtes Agents Pathogènes, Ecole Nationale Vétérinaire de Toulouse, 23 chemin des Capelles, 31076 Toulouse Cedex, France

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Article history: Available online xxx

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Keywords: Prion Amyloid Amyloidosis Protein misfolding Protein self-templating Prion-like transmission

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1. Introduction

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Transmissible spongiform encephalopaties (TSEs) are fatal neurodegenerative diseases characterized by the aggregation and accumulation of the misfolded prion protein in the brain. Other proteins such as ␤-amyloid, tau or Serum Amyloid-A (SAA) seem to share with prions some aspects of their pathogenic mechanism; causing a variety of so called prion-like diseases in humans and/or animals such as Alzheimer’s, Parkinson’s, Huntington’s, Type II diabetes mellitus or amyloidosis. The question remains whether these misfolding proteins have the ability to self-propagate and transmit in a similar manner to prions. In this review, we describe the prion and prion-like diseases affecting animals as well as the recent findings suggesting the prion-like transmissibility of certain non-prion proteins. © 2014 Published by Elsevier B.V.

Prion diseases or Transmissible Spongiform Encephalopaties (TSEs) are fatal neurodegenerative diseases that affect a diversity of mammal species including Creutzfeldt–Jacob disease (CJD), kuru, Gerstmann-Sträussler-Scheinker disease (GSS), and fatal familial insomnia (FFI) in humans, as well as scrapie in sheep and goats, bovine spongiform encephalopathy (BSE) in cattle, and chronic wasting disease (CWD) in deer and elk. Prion diseases are characterized by long incubation times (from months to decades), development of neuropathological alterations and symptoms primarily neurological including behavior abnormalities, motor dysfunction, cognitive impairment and cerebral ataxia. Prion diseases do not produce immune response and nowadays no effective therapies are available for their treatment. Prion diseases are caused by the conversion of the physiological cellular prion protein (PrPC ) into a pathogenic ␤-sheets enriched isoform designated PrPSc , which is able to self-propagate by recruiting PrPC . This conformational change confers PrPSc with an increased tendency to aggregate, insolubility in non-ionic detergents, high resistance to heat and chemical sterilization, and partial resistance to protease digestion. The concept of proteinaceous infectious particles, “Prions”, was first recapitulated in the “Prion Protein Only Hypothesis” (Prusiner, 1982). To date, a number of studies have supported this contention, including the successful

∗ Corresponding author. Tel.: +34 91 620 23 00; fax: +34 91 620 22 47. E-mail address: [email protected] (J.M. Torres).

induction of neurodegenerative diseases just from recombinant amyloid forms of prions (Castilla et al., 2005; Colby et al., 2009; Legname et al., 2004) or in combination with certain lipids and RNA factors (Wang et al., 2010). Nevertheless, some findings suggest that the misfolded PrPSc protein alone is not necessarily infectious by itself and needs some cofactors to self-propagate (Deleault et al., 2012; Saa et al., 2012; Telling et al., 1995). Hence, some authors proposed that PrPSc formation and infectious agent replication might constitute two separated processes where infectivity could lay on other non-PrP structures (reviewed in Manuelidis, 2013). Despite these arguments, prion diseases are entirely dependent on the expression of endogenous PrPC , as confirmed by the total resistance of prnp knock-out mice to prion infection (Bueler et al., 1993; Prusiner et al., 1993). PrPC is a glycosylphosphatidylinositol (GPI)-anchored plasma membrane protein encoded by the prnp gene which is well conserved throughout evolution in mammals (Nicolas et al., 2009). PrPC is mostly expressed in central nervous system (CNS) but also in the lymphoreticular system (LRS), skeletal muscle, heart, kidney, digestive tract, skin, blood plasma, mammary gland and endothelia (Nuvolone et al., 2009). Despite its ubiquitous expression and distribution, its physiological function is not yet clear. The mechanism by which PrPC converts into PrPSc adopting the capacity to self-template is neither well-known. PrPC can fold into a variety of thermodynamically stable PrPSc conformers (Prusiner, 1998; Wiltzius et al., 2009) whose mixture in a relative proportion may result in different prion strains (Angers et al., 2010). Each prion strain displays a specific disease phenotype (including incubation times, clinical signs, and histopathological lesions

http://dx.doi.org/10.1016/j.virusres.2014.11.026 0168-1702/© 2014 Published by Elsevier B.V.

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and PrPSc deposition patterns in the brain) which is faithfully recapitulated upon serial passage within the same host genotype (Beringue et al., 2008b; Collinge and Clarke, 2007). Prion strains may arise upon replication and transmission by “mutation” and/or “adaptation”. However, the molecular mechanism by which the range of PrPSc conformers would be produced and selected has not been yet elucidated. One possibility is that each PrPSc conformer might require a unique set of cofactors to propagate efficiently, and that the distribution and/or availability of these cofactors vary among different animal species, individuals or even distinct cell types. In line with this view, it was reported that different cell types within the same host can offer unique environments and selective pressures, each resulting in the emergence of different mutants as major constituents of the evolving population (Aguzzi and Sigurdson, 2004; Li et al., 2010; Mahal et al., 2007; Tremblay et al., 2004). On the other hand, studies in yeast have provided fundamental information for understanding the phenomenon of prion strain. A direct correlation between the frangibility (propensity to break) of yeast PrPSc fibrils and their rate of replication have been reported (Immel et al., 2007; Tanaka et al., 2004, 2006) and later extended to mammalian prions (Legname et al., 2006). Deciphering the structural features of PrPSc is a key issue to understand the molecular basis of prion formation, adaptation and propagation. Despite great efforts, the detailed tertiary structure of PrPSc is still unknown due to its insolubility and propensity to aggregate. Therefore, only partial structural information is available from low resolution techniques which failed to produce a shared explanation for the infectious capacity of prions (reviewed in Requena and Wille, 2014). The ability to misfold and self-propagate is not exclusive of prion proteins. Several neurodegenerative and non-neurodegenerative disorders are associated with the accumulation of self-templating amyloid forms of specific proteins in various organs and tissues of animals and humans. This heterogeneous group of diseases, called amyloidosis, are caused by the conformational change of a physiologically soluble protein into a ␤-sheet enriched form which self-assembly into amyloid fibrils. Similarly to prions, this conformational change triggers insolubility, aggregation and resistant to physical denaturants favoring the amyloid deposition and disrupting the physiological function of the tissues/organs where accumulates. The pathology and pathogenesis of amyloidosis are highly variable depending on the protein that causes the disease and the factors provoking this misfolding. To date, at least 28 different misfolding proteins, also called amyloid precursors, have been reported in humans and animals; including tau and Amyloid Precursor Protein (APP) in Alzheimer’s disease, huntingtin in Huntington’s disease, Serum Amyloid-A (SAA) in systemic amyloidosis or islet amyloid polypeptide in Type II diabetes mellitus. The exact mechanism through which these misfolding proteins are transformed and aggregated remains unknown but is reminiscent of prion replication. Thereby, amyloidosis have been labeled as “prion-like diseases” and included in the group of protein misfolding disorders (PMDs); where prion diseases belong. Moreover, increasing evidences attribute potential prion-like infectious properties to some of these amyloid precursors. In this way, tau, ␤-amyloid and ␣-synuclein have the ability to spread cell to cell, as demonstrated in mammalian cell cultures, in animals or even in humans (Costanzo and Zurzolo, 2013; Prusiner, 2012; Soto, 2012). In contrast, transmission between individuals has not been documented so far. The current key question is the possible infectious nature of these so-called “prion-like diseases” in a similar manner of prion diseases. In this review, an updated description of the prion and “prion-like diseases” affecting animals is presented. Pathogenesis of “prion-like diseases” in comparison with prion diseases as well as recent findings supporting the amyloidosis transmissibility are highlighted too.

2. Prion diseases in animals Prion diseases may occur as inherited disorders, arise spontaneously or be acquired by infection. Transmissions within the same animal species but also between different species have been reported for some prion diseases and at least one of them, the bovine spongiform encephalopathy (BSE), is considered a zoonosis to date.

2.1. Scrapie Scrapie is a TSE naturally affecting sheep, goats and mouflons (Jeffrey and Gonzalez, 2007); nowadays endemic in many countries worldwide. Scrapie is characterized by long incubation periods (2–5 years) and survival times ranging from 2 weeks to 6 months. Clinical signs comprise behavioral changes (fixed stare, isolation, hyperexcitability, loss of inquisitiveness), trembling, incoordination of gait, weight loss or emaciation, pruritus (main symptom in sheep, usually leads to wool loss) and impaired vision (Bellworthy et al., 2008; Dickinson, 1976; Hadlow et al., 1982). Neurological lesions deeply depend on scrapie strain, but generally include neuronal degeneration, non-inflammatory spongiform changes and astrogliosis detected mainly in diencephalon, midbrain, pons, medulla oblongata and cerebellar cortex (Hadlow et al., 1982). Apart from the nervous system, PrPSc deposition has been also observed in tonsils (Andreoletti et al., 2000), spleen (Hadlow et al., 1982), lymph nodes (van Keulen et al., 2008), nicitating membrane, muscles, placentas (Andreoletti et al., 2002), skin (Garza et al., 2014; Thomzig et al., 2007), mammary glands (Ligios et al., 2005), distal ilium, proximal colon (van Keulen et al., 2008); and more recently in pancreas, heart and urinary bladder (Garza et al., 2014). Although vertical transmission was evidenced (Spiropoulos et al., 2014), the most likely route of prion infection seems to be the contact transmission between ewes and her lambs around the time of birth (Imran and Mahmood, 2011). Besides, the presence of scrapie infectivity in blood (Bannach et al., 2012; Dassanayake et al., 2011, 2012; Lacroux et al., 2012), saliva (Gough et al., 2011; Tamguney et al., 2012), milk (Ligios et al., 2011) and colostum (Konold et al., 2013) in conjunction with the high resistance of this prion agent against denaturizing factors contributes to its permanency in the environment, i.e. in soil (Saunders et al., 2012b), and consequently favors the horizontal transmission within sheep and goats herds. Increased surveillance during the last two decades has led to the identification of a wide variety of scrapie disease phenotypes which are suggestive of scrapie strains. Moreover, an unusual type of scrapie was discovered in 1998 in Norway and therefore named atypical scrapie Nor-98 (Benestad et al., 2003). Currently, an increasing number of atypical/Nor98 scrapie cases have been reported in the majority of the European countries as well as in EEUU (Benestad et al., 2008) and New Zealand (Kittelberger et al., 2010). Its clinical signs are similar to classical scrapie disease; although generally less pronounced. Pruritus is uncommon and major clinical symptoms are ataxia and incoordination (Imran and Mahmood, 2011). Unlike classical scrapie, PrPSc deposition pattern in atypical scrapie infections is mild and restricted at the obex but more intense through cerebellum, substantia nigra, thalamus and basal nuclei (Moore et al., 2008). Atypical scrapie has been proposed to have a spontaneous origin since is quite spread and often occurrers in older animals as single cases in a flock (Benestad et al., 2008; Fediaevsky et al., 2010; Hopp et al., 2006). Nevertheless, some findings have demonstrated the oral transmissibility of the atypical scrapie agent (Simmons et al., 2007, 2011). This fact, together with the presence of prion infectivity in different tissues (including in lymphoid tissues, nerves, and

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muscles (Andreoletti et al., 2011; Simmons et al., 2011)) indicate that atypical scrapie might have the ability for natural transmission. To date, epidemiological and transmission studies have failed to demonstrate any link between classical or atypical scrapie diseases and any human prion disease, despite their worldwide endemicity (BIOHAZ, 2011; Wadsworth et al., 2013). However, studies founding this statement are quantitively limited and, therefore, further efforts must be done to draw final conculsions regarding the zoonotic potential of scrapie. The elevated economic losses caused by these prion dieases prompted to their control and eradication. As for other TSEs, scrapie occurrence and disease phenotype is strongly governed by the host prion protein encoding gene (prnp) and the prion strain (Agrimi et al., 2003; Aguilar-Calvo et al., 2014; Aguzzi et al., 2007; Baylis et al., 2004; Lacroux et al., 2014; Torres et al., 2014). In this context, breeding for genotype resistance programs arise as a suitable tool to control/eradicate scrapie in sheep and goat herds. Sheep A136 R154 R171 genotype was strongly associated with scrapie resistance (Belt et al., 1995; Bossers et al., 1996; Hunter, 1996, 1997) and therefore promoted within the ovine herds by selective breeding programs in some European countries (Dawson et al., 1998). This strategy has resulted in rapid control of scrapie outbreaks (Dawson et al., 2008; Fediaevsky et al., 2008; Hagenaars et al., 2010; Kanata et al., 2014; Nodelijk et al., 2011), decreasing the risk of scrapie infection even for animals of susceptible genotypes (Hagenaars et al., 2010). For goats, no programs of breeding for resistance have been so far implemented although several polymorphisms were linked with decreased susceptibility or even resistance against scrapie: I/M142 (Barillet et al., 2009; Goldmann et al., 2011; Gonzalez et al., 2010), three-repeat/glycine 102 (Goldmann et al., 1996, 1998), H/R143 , R/H154 and R/Q211 PrPC variants (Barillet et al., 2009; Bouzalas et al., 2010), N/D146 , N/S146 (Papasavva-Stylianou et al., 2011) and Q/K222 (Acin et al., 2013; Acutis et al., 2006; Barillet et al., 2009; Bouzalas et al., 2010; Corbiere et al., 2013; Fragkiadaki et al., 2011; Papasavva-Stylianou et al., 2011; Vaccari et al., 2006). More recently experimental studies in goats and transgenic mice expressing the K222 -PrPC variant confirmed the high resistance of this genotype against scrapie infection (Acutis et al., 2012; Aguilar-Calvo et al., 2014; Lacroux et al., 2014). Moreover, a protective effect of this PrPC variant over the scrapie replication of wild goat allele was also demonstrated (Aguilar-Calvo et al., 2014); pleading for the use of this K222 -PrPC variant in programs to control scrapie in goats populations. Interestingly, atypical scrapie is more common in A136 R154 R171 and A136 H154 R171 sheep than in genotypes associated with high susceptibility to classical scrapie such as V136 R154 Q171 (Benestad et al., 2008). Hence, selective breeding programs could have been indirectly favoring the incidence of atypical scrapie in sheep herds. Taken together these data prompted for new strategies to control and eradicate either classical or atypical scrapie in both sheep and goats herds. Recently, PrPC knockout goats were identified (Benestad et al., 2012). These goats, naturally devoid the prion protein because of a nonsense mutation located in codon 32 (32Stop), did not show any abnormal behavior or other characteristics distinct from their flock-mates (Benestad et al., 2012) and, therefore appear as an alternative for controlling scrapie endemicity.

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2.2. Bovine spongiform encephalopathy (BSE)

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BSE, commonly known as “Mad Cows Disease”, was firstly diagnosed in UK in 1986 (Wells et al., 1987) and soon spread worldwide; becoming epidemic. BSE-infected cattle display more than 2 years incubation periods and clinical signs including cachexia, alopecia, apprehension, lethargy or aggressive behavior, hyperresponsiveness to stimuli and abnormalities in movement (i.e. ataxia, particularly of hindlimb). Histolopathological lesions comprise vacuolation predominantly in the medulla oblongata at the

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level of the obex (Jeffrey and Gonzalez, 2004) but also in central gray matter, rostral colliculus and hypothalamus (Simmons et al., 1996; Wells et al., 2005). Unlike scrapie, PrPSc deposition in BSE-infected animals is mostly confined to the nervous system however; low infectivity in Peyer’s patches of the small intestine, distal ileum, jejunum, ileocecal juction (Hoffmann et al., 2011) and tonsils (Buschmann and Groschup, 2005; Espinosa et al., 2007; Hoffmann et al., 2011; Stack et al., 2011; Terry et al., 2003; Wells et al., 2005) have been described too. More recently, BSE infectivity in skeletal muscle was determined and associated to a probable centrifugal spread of the agent from central nervous tissues through the somatic motor and/or sensory pathways to peripheral muscle tissues (Okada et al., 2014). This observation is extremely relevant for redefining the Specified Risk Materials stated by Food Standards Agency to prevent the entry of BSE-contaminated material in the food-chain. Until today, no evidence of BSE infectivity in semen, embryos, placenta or milk (Bradley and Wilesmith, 1993; Buschmann and Groschup, 2005; Taylor et al., 1995; Wrathall et al., 2002) have been determined although increased risk of BSE development has been reported for the offspring of infected cows. The practice of feeding cattle with meat and bone meal (MBM) contaminated with infectious prions was proposed as the most likely responsible for the BSE epidemic (Wilesmith et al., 1991) and some hypotheses on the origin of BSE were considered: (i) the primary existence of sporadic or genetic BSE in cattle before its transmission via MBM (Baron et al., 2011; Capobianco et al., 2007; Nicholson et al., 2008; Richt and Hall, 2008; Torres et al., 2013); (ii) sheep or goat-scrapie transmission to cattle through MBM (Hill et al., 1998); and (iii) human CJD (Colchester and Colchester, 2005). European ban on the feeding of MBM to ruminants sharply declined the incidence of the disease although it is still not eradicated. BSE agent has demonstrated a high capacity to cross species barriers. During the BSE epidemic of 1980s, it spread to humans, with the emergence of variant Creutzfeldt–Jacob disease (vCJD) (Bruce et al., 1997; Hill et al., 1997) but also to cats and a variety of zoo animals probably originating Feline Spongiform Encephalopathy (FSE), Exotic Ungulate Spongiform Encephalopathy (EUE) and TSE in nonhuman primates (NHP) diseases (reviewed in Sigurdson and Miller, 2003). Furthermore, BSE has been experimentally transmitted to mice, hamster, sheep, goats, pigs, mink and non-human primates (Brown et al., 2003; Holznagel et al., 2013; Hunter, 2003; Lasmezas et al., 2005; Wells et al., 2003) with high efficiency. Upon passaged in sheep, BSE becomes more lymphotropic (Foster et al., 2001) but also increases its transmissibility to human PrP Tg mice (Padilla et al., 2011; Plinston et al., 2011; Priem et al., 2014). These facts have important implications for public health especially after two BSE “natural” cases in goats were reported (Eloit et al., 2005; Jeffrey et al., 2006). Consequently, political regulations were changed to prioritize biochemical differentiation between the BSE and scrapie agents in sheep and goats (Relevance, 2014) and prohibiting the use of processed animal protein in feed to all livestock. In the last years, active surveillance against BSE in cattle has led to the discovery of two BSE “atypical” variants, named H-type (Biacabe et al., 2004) and L-type BSE (Casalone et al., 2004). Both variants are often detected in fallen stocks and slaughtered old animals and differed from classical BSE in their biochemical properties and histopathological lesions. Their low prevalence worldwide is consistent with a sporadic origin. However their experimental transmission to bovinized, ovinized and wild type mice; suggested their potential infectious nature (Beringue et al., 2007; Buschmann et al., 2006; Capobianco et al., 2007; Torres et al., 2011). Unlike classical BSE agent, atypical BSE variants displayed several changes in their biological and biochemical properties when transmitted to other species. Much of these changes resulted in the emergence of classical BSE features; suggesting a possible relation of atypical

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BSE variants with the origin of BSE epidemic (Beringue et al., 2006, 2007; Capobianco et al., 2007). Although no epidemiological link between atypical BSE and any human prion disease has been determined, it has been reported that L-type BSE agent can propagate into humanized mice overexpressing the M129 -PrPC variant without any significant transmission barrier; being even more infectious for humans than epidemic classical BSE (Beringue et al., 2008a). Similar outcomes were obtained in non-human primates; presenting L-type BSE agent as a noted zoonotic risk (Comoy et al., 2008; Ono et al., 2011). Contrary, transmission studies have failed to transmit H-type BSE to humanized mice (Beringue et al., 2008a; Wilson et al., 2012).

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2.3. Chronic wasting disease (CWD)

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CWD is a TSE naturally affecting farmed and free-ranging cervids such as mule deer, whitetailed deer, black-tailed deer, Rocky Moun345 tain elk, and Shira’s moose. It mainly presents marked weight loss 346 but also rough and dry coat, excessive salivation, pacing, lassitude, 347 sudden death after handling, lowered head and drooping ears and 348 behavioral changes such as loss of fear to humans. Survival times 349 range from 7 to 8 months in deer (Williams and Young, 1980) but 350 can be longer in elks (Miller et al., 1998). In CWD-affected animals, 351 PrPSc can be widely distributed through nervous system but also 352 to lymphoreticular and hematopoietic systems, pancreas, muscles, 353 fat, retina, placenta, and the adrenal and salivary glands (Race et al., 354 2009a; Seelig et al., 2010; Sigurdson, 2008; Sigurdson and Miller, 355 2003; Spraker et al., 2010). It is unknown whether CWD arises spon356 taneously or was transmitted from other species. Scrapie would be 357 a possible origin since intracerebral inoculation of elks with this 358 agent induced CWD features (Hamir et al., 2004). 359 Since first case was recorded in 1967 in Colorado (Williams and 360 Young, 1980), CWD has unstoppably spread through at least 15 USA 361 states and 2 Canadian provinces (Saunders et al., 2012a); reach362 ing even South Korea by the importation of CWD-infected animals. 363 Prevalences in mule deer can reach 50% in endemic areas while for 364 deers are lower, affecting 10% of the population (Saunders et al., 365 2012a). Horizontal transmission is the most likely route of infec366 tion. It can efficiently occur by contact with affected animals, since 367 CWD prions are secreted and excreted to urine, feces, saliva and 368 blood; or through environmental exposure to CWD-contaminated 369 graze, soil or water (Almberg et al., 2011; Kuznetsova et al., 2014; 370 Mathiason et al., 2006; Miller et al., 2004; Nichols et al., 2009; 371 Safar et al., 2008; Sigurdson, 2008; Sigurdson and Miller, 2003; 372 Tamguney et al., 2009). A limited maternal transmission has also 373 been proposed (Nalls et al., 2013). 374 In contrast to its high transmissibility among cervids, no nat375 ural transmission to other species has been described until now. 376 Moreover, CWD is not able to cross species barrier through the oral 377 route as experimentally determined (Sigurdson, 2008; Sigurdson 378 and Miller, 2003; Tamguney et al., 2006; Wilson et al., 2012). Never379 theless, it is transmissible to cattle, sheep, goats, ferrets, hamsters, 380 bank voles, minks, raccoons and squirrel monkeys when intrac381 erebrally inoculated (Sigurdson, 2008). Recent studies evidenced 382 the capacity of this CWD to in vitro convert human PrPC only after 383 either passaged in transgenic mice expressing cervid PrPC or serial 384 PMCA amplification in deer PrPC substrate (Barria et al., 2011). In 385 addition, CWD has been successfully transmitted to squirrel mon386 keys albeit with lower efficiency than epidemic BSE (Marsh et al., 387 2005; Race et al., 2009b). Despite these findings, no epidemiolog388 ical evidence until today supports a potential zoonotic role of the 389 CWD agent. 390 CWD surveillance and control measures have been imple391 mented across the USA and Canada to reduce the disease spread, 392 Q2 mitigate the economic losses from reducing recreational hunting 393 and control its potential cross-species transmission (Williams, 394 344

2005; Joly et al., 2009; Wasserberg et al., 2009). Challenges comprise: (i) the high prion contamination of the environment due to excretion of the agent by multiple vias and the high persistence of its infectivity (Saunders et al., 2008, 2011; Smith et al., 2011); (ii) the geographical spread of the agent by the natural migration of cervids and by scavenger species; and (iii) the existence of different CWD strains (Angers et al., 2010). 2.4. Transmissible mink encephalopathy (TME) Transmissible mink encephalopathy (TME) is a rare TSE of mink which was first described in 1947 in Wisconsin and Minnesota (Marsh and Hadlow, 1992). Few cases of TME were also detected in Canada, Finland, East Germany and the former USSR (Barlow, 1972). TME normally occurs as localized epidemics in mink farms and mainly produces behavioral changes such as increased aggressiveness, depression, restlessness, compulsive biting, mutilation of objects or even themselves; but also hyperesthesia, ataxia, incoordination, difficulties in eating and swallowing, hindlimb weakness progressing to paresis, tremors and coat grooming; with incubation periods varying from 6 to 12 months (Schneider et al., 2012; Sigurdson and Miller, 2003). Around the end of the disease, within the 2–8 weeks after the appearance of clinical signs, animals may suffer convulsions and somnolence, not responding to stimuli (Sigurdson and Miller, 2003). TME-infected minks display intensive spongiform degeneration in cerebral cortex, thalamus, hypothalamus and corpus callosum which is less severe in the midbrain, pons and medulla. Besides TME PrPSc deposits have been also described in spleen, intestine, the mesenteric and retropharyngeal lymph nodes, thymus, rectoanal mucosa-lymphoid tissues, kidney, liver and salivary glands of experimentally infected mink (Schneider et al., 2012; Sigurdson and Miller, 2003). No vertical transmission of TME has been evidenced so far and the most likely route of transmission of the disease seems to be the horizontal one through cannibalism or biting of TME-infected minks. Mortality can raise 60–90% or even up to 100% during some outbreaks [http://www.cfsph.iastate.edu]. TME has been transmitted to a variety of species including cattle, sheep, goats, raccoons, skunks, ferrets, beech and pine martens, hamsters and some nonhuman primates but not to non-Tg mice (Bessen and Marsh, 1992; Hadlow et al., 1987; Hamir et al., 2005; Marsh et al., 1969; Robinson et al., 1994; Taylor et al., 1986). Two distinct strains, “hyper (HY)” and “drowsy (DY)”, were distinguished after transmission of TME in hamsters; exhibiting to the clinical symptoms, incubation periods, neuropathological lesions and biochemical profiles (Bessen and Marsh, 1992). The origin of TME is not clear, although it is presumed to be the result of feeding mink with prion-contaminated tissues from ruminants (Marsh and Bessen, 1993; Robinson et al., 1995). Scrapie agent was considered the most likely source of infection as minks experimentally inoculated with different scrapie isolates developed TME disease (Hanson et al., 1971). Epidemic BSE was also proposed since mice inoculated with this agent exhibited similar neurological lesion profiles than mice inoculated with FSE (Fraser et al., 1994). Finally, L-type BSE agent was recently linked to TME because it produced similar phenotypic features than bovine adapted-TME agent after inoculation in ovine Tg mice (Baron et al., 2007; Kimberlin et al., 1986). 2.5. Feline spongiform encephalopathy Feline Spongiform Encephalopathy (FSE) is a TSE of domestic cats and captive wild felids including lions, pumas, cheetahs, ocelots and tiggers. It was first documented in a domestic cat in 1990 in UK (Aldhous, 1990) shortly after the first cases of BSE were recorded in cattle herd. Since then, more than 100 cases have

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been reported in domestic cats from different countries including Ireland, Norway, Italy, Liechtenstein and Switzerland; although the majority (around 90%) occurred in UK. Besides, FSE cases were detected in wild felids housed in zoos from UK, Ireland, France, Germany and Australia. Interestingly, in all these cases except for two, wild felids were originated from UK zoos (Kirkwood and Cunningham, 1994). FSE clinical signs comprise behavioral alterations including fear, aggressiveness, hyperesthesia, timidity, hiding, depression or restlessness, but also movement abnormalities such as hypermetric gait, ataxia, coat grooming, and stare vacantly or circle. Tremors, convulsions, polyphagia, polidipsia, excessive salivation, and dilated pupils have been also reported (Imran and Mahmood, 2011). Survival times vary among the species from 3 to 10 weeks after the disease onset (Sigurdson and Miller, 2003) [http://www.cfsph.iastate.edu]. Neurological alterations consist of spongiform degeneration of the neuropil in the gray matter of the brain and spinal cord, more intense in the medial geniculate nucleus of the thalamus and the basal nuclei (Sigurdson and Miller, 2003; Wyatt et al., 1991). In addition to CNS, PrPSc florid plaques have been observed in peripheral nervous system, retina, lymphoreticular system, spleen, kidney and adrenal glands (Bencsik et al., 2009; Eiden et al., 2010; Lezmi et al., 2003; Ryder et al., 2001; Sigurdson and Miller, 2003) [http://www.cfsph.iastate.edu]. The origin of FSE remains unknown. Nonetheless, the use of BSE-contaminated meals to feed felids seems to be the most likely source of the disease since the majority of the FSE cases were reported in UK coinciding with the BSE epidemics. Moreover, similar neuropathological lesions and incubation periods were obtained in mice experimentally inoculated with brains of FSE or BSEinfected cats (Bencsik et al., 2009; Eiden et al., 2010). Nonetheless, in 1998 in Italy, a domestic cat and its owner were concurrently infected by a prion agent different from FSE or BSE. Man showed a clinical phenotype typical of sporadic CJD (sCJD), while his cat developed a disease clinically different from FSE (Zanusso et al., 1998); thus contradicting the view that FSE could have been caused by the infection of felids with BSE agent. The origin of these two cases has not yet been elucidated; and different ideas were postulated including horizontal transmission between the man and the cat, or if both contracted the disease from the same unknown source or merely by chance (Zanusso et al., 1998). Finally a maternal transmission of FSE was proposed in a case of captive cheetah in France (Bencsik et al., 2009). 3. Prion-like diseases in animals In animals, at least eight different diseases associated to misfolded proteins or amyloid precursors have been described (Mensua et al., 2003). These diseases, called amyloidosis may present as localized or systemic disorders (Sipe et al., 2012) with symptoms depending on the tissues where amyloid are depositted. Attending to their etiology, amyloidosis can be idiopathic, primary or secondary (associated to inflammatory or neoplastic pathologies) diseases. In animals, all of these forms have been described; although the most common are the systemic secondary AA-amyloidosis. 3.1. Systemic amyloidosis 3.1.1. AA-amyloidosis AA-amyloidosis is the most common amyloidosis disorder of mammals and birds. It has been reported in domestic animals including canines, felines, porcines, equines, bovines, sheep, goats and certain avian species, but also in wild animals such as

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black-footed cats, black-footed ferrets, Dorcas gazelles, water fowls, lioness, swans, rhesus and pig-tailed macaques (Rice et al., 2013) or bighorns (reviewed in Woldemeskel, 2012). AAamyloidosis can occur as idiopathic disorders as observed in some Siberian tiggers, cattle or chicken (Kim et al., 2005; Snyder et al., 2011; Steentjes et al., 2002; Yamada et al., 2006; Zekarias et al., 2000); although it normally appears in association with chronic inflammatory processes, viral or bacterial infections or neoplastic diseases (Snyder et al., 2011). For rhesus and pig-tailed macaques, AA-amyloidosis is often detected in individuals suffering from bacterial enterocolitis (Blanchard et al., 1986; Hukkanen et al., 2006; Naumenko and Krylova, 2003; Slattum et al., 1989), rheumatoid arthritis (Chapman and Crowell, 1977), respiratory diseases (Naumenko and Krylova, 2003; Slattum et al., 1989), parasitism (Bacciarini et al., 2004; Blanchard et al., 1986) or even trauma (Slattum et al., 1989); exhibiting prevalence as high as 30% in rhesus macaques (Blanchard et al., 1986), and 47% in pig-tailed macaques (Hukkanen et al., 2006). Avian AA-amyloidosis is quite common in waterfowls too, usually secondary to ulcerative pododermatitis caused by Staphylococcus spp. infection (Brassard, 1965; Dias and Montau, 1994). Contrary, bovine AA-amyloidosis is a relatively rare disease, generally associated with inflammatory disorders such as mastitis or arthritis (Elitok et al., 2008; Seifi et al., 1997). AAamyloidosis in feline immunodeficiency virus (FIV)-infected cats has also been reported (Asproni et al., 2012). In all cases, disease is caused by the conformational change of the acute phase reactant, Serum Amyloid-A (SAA) (Gruys, 2004; Kim et al., 2005; Kisilevsky, 1990), a protein encoded by multiple genes highly conserved through the evolution of eutherian mammals (Jacobsen et al., 2006; Uhlar and Whitehead, 1999). SAA is a apoliprotein of high-density lipoproteins mostly synthesized in liver in response to proinflammatory cytokines such as endogenous pyrogens IL-1 and IL-6 (Gruys, 2004). Its physiological functions comprise cholesterol transportation, chemoattraction in inflammatory processes (Badolato et al., 1994; Kisilevsky, 1990) and certain antimicrobial activity (Ray and Ray, 1999). When its concentration is increased (i.e. in inflammatory processes) some isoforms of SAA prone cleavage to a 76-residue N-terminal product, designated amyloid protein A (AA) and form fibrillar amyloid aggregates which deposited systemically (Husby et al., 1994). All the systemic inflammatory processes result in the deposition of amyloid fibrils, although only some of these inflammatory reactions produce amyloidosis (Woldemeskel, 2012). The overactivation of macrophages together with an enzyme abnormality in the degradation of SAA protein or the synthesis of SAA proteins abnormally resistant to their enzymatic degradation are the most likely factors producing AA-amyloid accumulation (Snyder et al., 2011). Amyloid deposits in kidney, liver and spleen result in the physical disruption of the organs and consequently give rise to hepatic or renal failure (Terio et al., 2008). Some animal species are prone to develop AA-amyloidosis. A familial form of AA-Amyloidosis has been reported in Siamese and Abissinian cats, and Sharpei dogs (Boyce et al., 1984; DiBartola et al., 1990; Niewold et al., 1999). These animals are genetically predisposed to form and accumulate amyloid structures. Interestingly, their SAA primary sequences and pattern of deposition differ from other mammal species and between them. Shar-pei dogs harbor a potential modifier locus for amyloidosis on chromosome 14 and display different expression of four genes associated with kidney or immune health (Olsson et al., 2013). Whereas Siamese and Abissinian cats exhibit two substitutions in their SAA amino acid sequence, Q/R46 and A/V52 ; the former (Q/R46 ) has not been reported in any other mammalian species (Niewold et al., 1999). The unusual high prevalence of renal and hepatic AA-amyloidosis in cheetahs is also suggestive of a genetic predisposition (Papendick et al., 1997). Evidences for familial amyloidosis

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appeared in brown layer chickens, Dorcas gazelles and black-footed cats too (Woldemeskel, 2012). On the other hand, stress seems to play a determinant role for the AA-amyloidosis development in cheetahs (Papendick et al., 1997) and other species (Cowan and Johnson, 1970; Germann et al., 1990; Zschiesche and Jakob, 1989). Stressful environmental situations may lead to an endogenous corticosteroid immune suppression; resulting in increase susceptibility to infectious or inflammatory diseases (Papendick et al., 1997). Furthermore foie gras, produced by stressing force feeding geese, frequently showed high amounts of AA fibrils (Solomon et al., 2007). Chickens may also present AA-amyloidosis after vaccination with multiple vaccines; probably as a result of the stress situation and/or the antigenic stimulation with either crude bacterial extracts or oil-emulsified bacterins (Murakami et al., 2013a). Long-term inflammatory stimulation can also induced AA-amyloidosis development, as experimentally demonstrated in chickens, ducks or cattle (Janigan, 1966; McAdam and Sipe, 1976; Ram et al., 1968; Skinner et al., 1977). More recently, a series of elegant studies have indicated the possible prion-like transmissibility of some AA-amyloidosis in mice, minks, cheetahs, chickens, and rabbits (Murakami et al., 2013c; Sorby et al., 2008; Zhang et al., 2008). This aspect is extensively aborded in Section 4.

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3.1.2. AL-amyloidosis AL-amyloidosis, also called immunoglobulinic amyloidosis, is uncommon in domestic animals, but the most extended systemic form of amyloidosis in humans (Picken, 2001). For domestic species AL-amyloidosis is normally associated to an immune dyscrasia, generally the neoplasm of plasma cell (Snyder et al., 2011). In this way, AL-amyloidosis have been encountered in a horse with multiple myeloma (Kim et al., 2005), a cow with bovine leukocyte adhesion deficiency (Cogne et al., 1991) or in cats and dogs with extramedullary plasmacytomas (Platz et al., 1997). Bronchial and tracheal AL-amyloidosis in dogs (Kyle et al., 1997; Skinner et al., 1996) as well as cutaneous amyloidosis in equines (Skinner et al., 2004) were also determined. Recently, a systemic case of ALamyloidosis in a beech marten with special involvement of kidney, liver, heart and spleen was reported (Scaglione et al., 2013). In AL-Amyloidosis, immunoglobulins secreting cells or plasma cells such as B lymphocytes produce excessive quantities of immunoglobulin light chains which misfold into beta-sheets rich conformations (Snyder et al., 2011). These misfolded structures are more resistant to complete enzymatic degradation and tend to form insoluble fibrils and systemically deposit (Desport et al., 2012). Not all the free monoclonal light chains form amyloid fibrils in vivo and this ability has been linked to structural properties of the light chain variable region (Abraham et al., 2003; Bellotti et al., 2000).

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Localized Amyloidosis is characterized by the deposition of amyloid fibrillar proteins as a grossly visible mass or microscopic deposit adjacent to the places of the synthesis of the precursor (Merlini and Stone, 2006; Woldemeskel, 2012). It appears in a heterogeneous range of diseases, associated with neoplasias (such as lymphoma (Gliatto and Alroy, 1995) or plasmocytoma (Linke et al., 1991) in horses) or even producing odontogenic tumors in cats and dogs (Gruys, 2004; Snyder et al., 2011). Localized amyloidosis is usually encountered in old animals giving rise to relevant diseases such as Type II diabetes mellitus in cats (Johnson et al., 1986; O’Brien et al., 1986), dogs (Mattin et al., 2014) and macaques (de Koning et al., 1993; Howard, 1986). Diabetes is caused by the misfolding of islet amyloid polypeptide (IAPP) which is synthesized by the pancreatic ␤ cells. The mechanism by which this protein misfolds is not clear but residues 20–29 of the mature

IAPP protein might be involved in amyloid fibril formation due to the elevated intrinsic ␤ sheet secondary structure and the high variability of the primary sequence of this region (O’Brien et al., 1993). Aged-related ␤-amyloid deposition with limited intraneuronal accumulation of tau has been also detected in brains from dogs showing signs of dementia (Gruys, 2004; Papaioannou et al., 2001).

4. Transmissibility of prion-like diseases Prion-like misfolding and self-propagation have been demonstrated for several non-prion proteins including SAA, ApoII, tau, ␣-synuclein or ␤-amyloid. These misfolding proteins or amyloid precursors are responsible for the appearance of highly relevant neurodegenerative and non-degenerative diseases in human and animal species such as Alzheimer’s disease, Huntigton’s disease (HD), Parkinson’s disease and Type II diabetes mellitus among others. Currently, the key question is whether these misfolding proteins harbor a prion-like transmission or infection capacity. Inoculation of samples containing Alzheimer’s- or Parkinson’sassociated aggregates has been reported to induce neuronal damage and neurological sings in different animal models (reviewed in Beekes et al., 2014). Moreover, the cell to cell spread of these proteins through the nervous system in a stereotypic temporal-spatial manner was also reported (Costanzo and Zurzolo, 2013; Prusiner, 2012; Soto, 2012). Despite these findings, no evidence of prion-like disease transmission between humans has been reported to date. In contrast, transmissibility of some animal prion-like disorders has been largely suspected. Thereby, the most likely route of transmission of avian AA-amyloidosis during epidemic outbreaks in fowl populations is the ingestion of amyloidcontaminated feed or feces (Sato et al., 2003; Tanaka et al., 2008). This assumption was extended to chickens where severe amyloid deposits were detected in the gut of amyloidosis-infected animals; suggesting a possible oral entry of the AA-fibrils (Murakami et al., 2013c). Moreover, the coexistence of hemorrhagic enteritis in AA-amyloid affected chickens was proposed as a possible via of amyloid shedding in feces (Murakami et al., 2013b). Similarly, the high incidence of AA-amyloidosis in captive cheetah was also linked to horizontal transmission by fecal AA-fibrils (Zhang et al., 2008). In the last decades, several experimental studies have shown that susceptibility of different species to AA-amyloidosis could be experimentally enhanced by different factors. Early studies on the transmissibility of non-prion proteins demonstrated that repeated injections of inflammatory-stimuli such as silver, casein or lipolysacharidae could induce the development of AA-amyloidosis in different animal species such as cows, mice, rabbits, ducks and chickens (Druet and Janigan, 1966; Janigan, 1966; Ling, 1992; Murakami et al., 2013b; Skinner et al., 1977) by increasing their concentrations of circulating SAA proteins. Remarkably, the lag phase of these AA-amyloids could be further shortened by coinjecting these proinflammatory factors with protein extracts from different tissues of AA-amyloidosis infected animals (Cui et al., 2008; Lundmark et al., 2003, 2005). The nature of these amyloid precursors was not known at the beginning and some hypothesis were proposed. Some authors proposed that these amyloid precursors could be a minute ␤ strand-containing fragment of the amyloid fibril (Niewold et al., 1987), while others associated it with an early AA peptide–glycosaminoglycan complex (Snow et al., 1987) or an amyloid itself (Shirahama et al., 1969). In this last line, Westemark’s group experimentally demonstrated that the biologically active principle responsible for the amyloid accelerating activity was the amyloid fibril itself. These results evidenced a “ProteinOnly” transmission of amyloids which is in accordance with the

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“Prion Protein Only Hypothesis” proposed for the prion transmissibility (Ganowiak et al., 1994; Johan et al., 1998; Lundmark et al., 2003) and therefore termed “prion-like” transmission. Similar “Protein-Only” or prion-like transmission has been documented for other non-prion disorders including avian, bovine, mouse and cheetah AA-amyloidosis as well as mouse ApoAII amyloidosis (Higuchi et al., 1998; Xing et al., 2001, 2002). Oral and/or intravenous inoculations with avian AA-amyloid fibrils produced amyloidosis in chickens, swans and mice (Liu et al., 2007; Murakami et al., 2013b,c). Furthermore, Solomon et al. (2007) were able to efficiently induce a systemic AA-amyloidosis in Tg mice expressing human interleukin (IL)-6 by oral or intravenous injection with AAfibrils extracted from commercial foie gras made of duck or goose liver. This work indicated for the first time the zoonotic potential of Avian AA-amyloidosis; pinpointing foi-gras as a dietary source of amyloid disorders. Bovine AA-amyloidosis has been transmitted to mice and rabbit by coinjection of AA-amyloid fibrils and inflammatory stimulus by either oral or intravenous routes too (Cui et al., 2008; Horiuchi et al., 2008; Murakami et al., 2011). Interestingly, transmission of bovine AA-fibrils to mice was less efficient than transmission with mouse AA-fibrils, suggesting the possible existence of amyloid transmission barrier similar to that of prion diseases (Liu et al., 2007). Other factors such as the route of inoculation or the dose of amyloid fibrils injected have been also considered as modulators of the transmission efficiency and extent of amyloid deposits (Murakami et al., 2013b). In this way, amyloid deposits were differently distributed when avian AA-amyloid fibrils were orally or intravenously inoculated in chickens (Murakami et al., 2013c). The existence of amyloid strains, similar to that reported for prions, has been also evidenced. In mice, at least three ApoAII variants can be encoded by the ApoAII gene (APOAIIA, APOAIIB, and APOAIIC) which give rise to different spontaneous senile disease phenotypes (Higuchi et al., 1999). APOAIIC protein with a glutamine at position 5, is related to high incidence of severe senile amyloidosis, while APOAIIB with a proline at position 5 is linked to very low incidence of the disease. For cattle, at least seven SAA isoforms have been documented although only those with isoelectric points of 5.2 and 8.6 are thought to induce bovine AA-amyloidosis (Takahashi et al., 2009). Other host genetic factors seem to influence the distribution patterns and severity of amyloid deposition. Thereby, aged C57BL/Ka mice exhibited high incidences of gastrointestinal AApoAII amyloidosis (HogenEsch et al., 1993) while CD-1 Swiss mice have an amyloid deposition mainly in ileum, lung, and heart (Gruys et al., 1996) or remained limited to renal glomeruli in NSY mice (Shimizu et al., 1993). Moreover, amyloidogenic fibrils isolated from the same mouse can show different pathological and structural characteristics and transmissibility properties (Korenaga et al., 2004). AA-fibrils isolated from cheetahs feces were remarkably more transmissible to mice than those fibrils isolated from cheetahs livers (Zhang et al., 2008). 5. Perspectives The data summarized in this review strongly argue that a growing number of amyloid proteins could be considered infectious agents with the capacity to transmit through a prion-like mechanism involving seeding-nucleation (Lundmark et al., 2003). The efficient transmission of some amyloid precursors within certain animal species or even between different animal species prompts to the implementation of measurements for their control. The question remains whether amyloidogenic proteins has a zoonotic potential similar to that previously demonstrated for other prion diseases such as BSE. To the best of our knowledge, at least avian AA-amyloidosis has been proposed as a zoonotic disorder and products harboring AA-amyloid fibrils have been considered hazardous

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for individuals who are prone, genetically or by other factors (i.e. chronic inflammatory diseases), to develop other types of amyloidassociated disorders, such as Type II diabetes, Alzheimer’s disease or Huntington’s disease (Solomon et al., 2007). However, further interspecies PMDs transmission assays are still needed to conclude on their zoonotic potential and assess the risk of food-borne PMDs (Murakami et al., 2013b). Previous knowledge in prion diseases may notably help scientists on understanding the nature of PMDs; offering opportunities for PMDs control and treatment. Conflict of interest The authors declare no competing financial interests. Acknowledgements This work was supported by grants from the Spanish Ministerio Q3 de Economía y Competitividad (AGL2012-37988-C04-04 and RTA2012-00004-00-00) and European Union (219235 FP7 ERA-NET EMIDA). References EFSA Panel on Biological Hazards (BIOHAZ), 2011. Joint scientific opinion on any possible epidemiological or molecular association between TSEs in animals and humans. EFSA J. 9, 1945–2056 (cited 11.09.13). Abraham, R.S., Geyer, S.M., Price-Troska, T.L., Allmer, C., Kyle, R.A., Gertz, M.A., Fonseca, R., 2003. Immunoglobulin light chain variable (V) region genes influence clinical presentation and outcome in light chain-associated amyloidosis (AL). Blood 101 (10), 3801–3808. Acin, C., Martin-Burriel, I., Monleon, E., Lyahyai, J., Pitarch, J.L., Serrano, C., Monzon, M., Zaragoza, P., Badiola, J.J., 2013. Prion protein gene variability in Spanish Goats. Inference through susceptibility to classical scrapie strains and pathogenic distribution of peripheral PrP(sc). PLOS ONE 8 (4), e61118. Acutis, P.L., Bossers, A., Priem, J., Riina, M.V., Peletto, S., Mazza, M., Casalone, C., Forloni, G., Ru, G., Caramelli, M., 2006. Identification of prion protein gene polymorphisms in goats from Italian scrapie outbreaks. J. Gen. Virol. 87 (Pt 4), 1029–1033. Acutis, P.L., Martucci, F., D’Angelo, A., Peletto, S., Colussi, S., Maurella, C., Porcario, C., Iulini, B., Mazza, M., Dell’atti, L., Zuccon, F., Corona, C., Martinelli, N., Casalone, C., Caramelli, M., Lombardi, G., 2012. Resistance to classical scrapie in experimentally challenged goats carrying mutation K222 of the prion protein gene. Vet. Res. 43 (1), 8. Agrimi, U., Conte, M., Morelli, L., Di Bari, M.A., Di Guardo, G., Ligios, C., Antonucci, G., Aufiero, G.M., Pozzato, N., Mutinelli, F., Nonno, R., Vaccari, G., 2003. Animal transmissible spongiform encephalopathies and genetics. Vet. Res. Commun. 27 (Suppl. 1), 31–38. Aguilar-Calvo, P., Espinosa, J.C., Pintado, B., Gutierrez-Adan, A., Alamillo, E., Miranda, A., Prieto, I., Bossers, A., Andreoletti, O., Torres, J.M., 2014. Role of the goat K222-PrPC polymorphic variant in prion infection resistance. J. Virol. 88 (5), 2670–2676. Aguzzi, A., Heikenwalder, M., Polymenidou, M., 2007. Insights into prion strains and neurotoxicity. Nat. Rev. Mol. Cell Biol. 8 (7), 552–561. Aguzzi, A., Sigurdson, C.J., 2004. Antiprion immunotherapy: to suppress or to stimulate? Nat. Rev. Immunol. 4 (9), 725–736. Aldhous, P., 1990. BSE: spongiform encephalopathy found in cat. Nature 345 (6272), 194. Almberg, E.S., Cross, P.C., Johnson, C.J., Heisey, D.M., Richards, B.J., 2011. Modeling routes of chronic wasting disease transmission: environmental prion persistence promotes deer population decline and extinction. PLoS ONE 6 (5), e19896. Andreoletti, O., Berthon, P., Marc, D., Sarradin, P., Grosclaude, J., van Keulen, L., Schelcher, F., Elsen, J.M., Lantier, F., 2000. Early accumulation of PrP(Sc) in gutassociated lymphoid and nervous tissues of susceptible sheep from a Romanov flock with natural scrapie. J. Gen. Virol. 81 (Pt 12), 3115–3126. Andreoletti, O., Lacroux, C., Chabert, A., Monnereau, L., Tabouret, G., Lantier, F., Berthon, P., Eychenne, F., Lafond-Benestad, S., Elsen, J.M., Schelcher, F., 2002. PrP(Sc) accumulation in placentas of ewes exposed to natural scrapie: influence of foetal PrP genotype and effect on ewe-to-lamb transmission. J. Gen. Virol. 83 (Pt 10), 2607–2616. Andreoletti, O., Orge, L., Benestad, S.L., Beringue, V., Litaise, C., Simon, S., Le Dur, A., Laude, H., Simmons, H., Lugan, S., Corbiere, F., Costes, P., Morel, N., Schelcher, F., Lacroux, C., 2011. Atypical/Nor98 scrapie infectivity in sheep peripheral tissues. PLoS Pathog. 7 (2), e1001285. Angers, R.C., Kang, H.E., Napier, D., Browning, S., Seward, T., Mathiason, C., Balachandran, A., McKenzie, D., Castilla, J., Soto, C., Jewell, J., Graham, C., Hoover, E.A., Telling, G.C., 2010. Prion strain mutation determined by prion protein conformational compatibility and primary structure. Science 328 (5982), 1154–1158.

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Please cite this article in press as: Aguilar-Calvo, P., et al., Prion and prion-like diseases in animals. Virus Res. (2014), http://dx.doi.org/10.1016/j.virusres.2014.11.026

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