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Invited Review Molecular Clues to Pathogenesis in Prion Diseases

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Invited Review Molecular Clues to Pathogenesis in Prion Diseases Histol Histopathol (1997) 12: 583-594 Histology and 001: 10.14670/HH-12.583 H istopatho logy http://www.hh.um.es From Cell Biology to Tissue Engineering Invited Review Molecular clues to pathogenesis in prion diseases M. Laurent and G. Johannin Service d' Imagerie Cellulaire, Universite Paris-Sud, Orsay Cedex, France Summary. The infecti ous agent of the trans missible Introduction spongiform encephalopathies (TSE) resembles a vi rus in that it propagates in vivo a nd has distinct s trai ns. A lthough recent a nd public developments about However, compelling evidence strongly suggests that a ' mad cow disease' and Creutzfeldt-Jakob disease go far posttranslational structural alteration in a glycoprotein beyond purely scienti fic concern , it would be wrong to PrPC (the normal, cellular isoform of the so-call ed prion believe that prion diseases - which is the generic name protein) is responsible for pathogenesis of these diseases. for all these transmissible neurodegenerative di seases - Accordi ng to this hypothesis - now c lose to being have been onl y recentl y discovered. The first case of a generall y accepted -, iatrogen, sporad ic and familial sheep which presented a ll the sympto m s of scrapie forms of TSE would h ave the sa m e m o lecul ar (excit ability, itc hing , ataxia and fina ll y paralysis and mechanism : th e conversion of PrPC into a pro tease­ death) was recogni zed in the middle of the 18th century resis ta nt isofo rm PrPSc kinetically behaves as an (Reibel, 1994; We issmann, 1994a). Of course, othe r autocatalyt ic process which, combined with the high unide ntified cases mig ht have occurred long before. turnover rate of the normal isoform , may e ndow the Scrapie is the prototype of w hat has proved to be a group system with bistability propert ies a nd s ubseque nt of lethal diseases affecting animals such as sheep, cows, threshold behavior between no rmal a nd pa thogeni c minks, moufflo ns, ostric hes, c heetahs, cats a nd also s tead y -s ta tes. Normal prio n protein see m s to be huma ns ( Re ibe l, 1994). In 1936, C uille a nd C he ll e necessa ry for lo ng- term s urvi va l of Purkinje showed that scrapie was due to an agent fo und in the neurons, regul at ion of circadian rh ythms a nd, more brain and in the spinal chord of diseased animals and controversiall y, for normal synaptic function. At least that the disease could be transmitted to sheep and goats part of the pathology mi ght be due to the unavailability by inoculating them with the lombard cord of affected of norm al isoform rather th an to the accumulation of animals (Weissmann, 1994a). This agent was s hown PrPSc. NMR structure of the normal mouse prion protein earl y on to be non-conventional because it has particul ar reveals a short , unexpected /3-sheet which might be a properties such as uncommon resistance to treatme nts nucleati on site for the conformational transition between that usuall y destroy nucleic acids found in viruses and PrPC and PrPSc. Prion diseases may challenge the edged bacteria. Moreover, incubation pe riods for the disease distinction that we use to make between informational are extraordinarily long (measured in months in animals (DNA) a nd functional (proteins) macromolecules. and years in man). In 1982, Prusiner proposed naming Pathogenic mechanism of prions might also be involved this agent as ' prion ' to distinguish it from conventional in o the r pro te ins to achieve a nd pass o n th e ir pathogenic agents such as bacteria and viruses (Prusiner, confo rma ti o n. He nce, s truc tura l inhe rita nce a t the 1982). molecular level mi g ht be th e mi ssing link for In humans, four slow degenerati ve diseases of the the unde rs ta nding of th e s tructura l inhe rita n ce central ne rvous syste m have been described: kuru ; processes featured a t the cellular level. Mo reover, Creutzfeldt-Jakob disease (CJD); Gerstmann-Straussler­ evolutio nary paradigm postulating a primitive RNA Scheinker disease (GSS); a nd fatal familial insomnia world is weakened by the m ech a ni s m of prio n (FFI). Kuru, hi storicall y contracted at the beginning of diseases. this century in Papua New Guinea's Fore hi ghl ande rs, may have o ri g ina ted fro m the cons umptio n of th e Key words: Prion diseases, Prion protein, Spongiform remains of a CJD sufferer (Dormont and Bursaux, 1996) encephalopathies, Bistability, Structural inheritance a nd was propagated thro ug h ritual cannibalism . Inoculation studies by Gajdusek's group (Gajdusek et Offprint requests to: Dr. Michel Laurent, Service d'imagerie Cellulaire, aI. , 1966) had demonstrated the infectious nature of kuru URA 116 CNRS. Bat 440, Universite Paris-Sud, 91405 Orsay Cedex, and then of CJD and GSS by transmitting the disease to France c himpanzees throug h th e injectio n of diseased brain 584 Molecular clues to prion diseases ti ssue. The infectious nature of FFI was shown much biology concerning the edged distinction that we make more recently (Tateishi e t a i. , 1995). Although between informational and functional macromolecules, incubation periods are particularly long, once the first namely DNA and proteins respectively. clinical symptoms such as loss of memory or motor disturbances appear, progression to death may take only Nature of the transmissible agent a few months. Tbe pathological changes vary in location and intensity but the brain tissue typicall y develops The unsual properties of prion diseases gave rise spongelike holes as neurons die while glia proliferate. early to specul atio ns about the nature of the trans­ No inflammato ry nor immuno logical counterpart is missible agent responsible fo r ne urodegenerative observed. diseases. In the 60s, the leading theory supposed that an The current epizooty of bovine spo ng ifo rm unidentified, slow-acting virus was the real culprit. encephalopathy (BSE or ' mad-cow disease' ) w hic h Although viruses can be very hard to find, no-scrapie­ principally occurs in Great Britain, is believed to result associated virus or nucleic acid has ever turned up, in f rom a c hange in the process of making fee d spite of many attempts to find traces of it, during the last supplements given to cattle. These supplements coming 30 years (Kellings et aI. , 1992). However, Alper 's from cattle (50%) and sheep (15%) offal were probably experiments (Alper et a I. , 1966, 1967) weakened this contaminated by a scrapie-like agent. In 1980, the theory by showing tha t scra pie infectivity resists stopping of the fat-extracting process by organic solvents inactivation by both ultraviolet and ionizing radiations, probably increased contamination of the feed which usually destroy nucleic acids. The possibility that supple me nts. He nce, at least in the corresponding the scrapie agent might be devoid of nucleic acid was species, the agent responsible for ESB and kuru can reinforced by Prusiner's group who later showed that diffuse through the digestive tract. Kuru has almost reagents - such as nucleases, psoralens, hydroxylamine disappeared with the cessation of ritual cannibalism, and Zn2+ io ns - th at specificall y modify o r damage stro ngly suggesting that this disease was transmitted nucleic acids , do not a lter scrapie infectiv it y in orally, as proposed for BSE. Iatrogen forms of CJD have homogenates or partially purified preparations (Diener et been observed as a result of the use of contaminated aI., 1982; McKinley et aI. , 1983; Gabizon et aI. , 1987). surg ical materi al, cornea o r eardrum transplants or A lthough it is known that some viruses can resist therapeutic use of hypophyse-derivated products from treatments th at normally destroy nucleic acids, two human origin. However, prion diseases may also arise additional observations go against the viral hypothesis. spontaneously without any apparent cause (so-called Modern subtraction hybridization experiments were sporadic) or be genetic (5 to 15% of CJD are tbought to unable to reveal the presence of DNA or RNA sequences be familial). Whatever its iatrogen, or sporadic o r in infected brain tissues which would be absent in fa milial orig in, the disease can usuall y be transmitted to normal ones (Mestel, 1996). Moreover, the occurrence animals by intracerebral inoculation. The possibility of a of some fa milial prion diseases makes it much more vertical transmission (from the cow to the calf for unlikely to be a virus, without definitively excluding instance) is as yet hypothetical, although such an such a possibility. One would have to im agine that occurrence has been reported in the case of captive mule although the virus would infect all the members of the deer and e lk in zoological garde ns (Re ibe l, 1994). fa mily, only those who have a putati ve mutation would However, much of th e current upheavals come from a develop the disease. recent report (Will et aI. , 1996) indicating that ten cases On the oth er h a nd , there is now a wealth of of CJD were detected in Great Britain whose clinical and biochemical a nd gene tic ev idence s upporting the pathological features seem significantl y distinct from contention that a protein (so-called prion protein or PrP) those of the common (although rare) disease, especiall y is th e key for infectivity. Prusiner first reported th e concerning the fact that the patients were unusually existence in scrapie brains of a protein that was required young.
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