Preclinical Detection of Variant CJD and BSE Prions in Blood

PLoS Pathogens

Volumn 10, Issue 6, 2014, Pages

  Lacroux, Caroline ^a   Comoy, Emmanuel ^b   Moudjou, Mohammed ^c   Perret Liaudet, Armand ^d   Lugan, Séverine ^a   Litaise, Claire ^a   Simmons, Hugh ^e   Jas Duval, Christelle ^f   Lantier, Isabelle ^g   Béringue, Vincent ^c   Groschup, Martin ^h   Fichet, Guillaume ^c,i   Costes, Pierrette ^a   Streichenberger, Nathalie ^c   Lantier, Frederic ^g   Deslys, Jean Philippe ^b   Vilette, Didier ^a   Andréoletti, Olivier ^a  

^a IHAP   (France)

^b INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^c INRA Institut National de la Recherche Agronomique   (France)

^d HOSPICES CIVILS DE LYON   (France)

^e VETERINARY LABORATORIES AGENCY   (United Kingdom)

^f Service des Aphérèses   (France)

^g UR1282   (France)

^h FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

ⁱ Franklab ^*  (France)

Author keywords

[No Author keywords available]

Indexed keywords

PRION PROTEIN; PRION;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD; BLOOD TRANSFUSION; BOVINE SPONGIFORM ENCEPHALOPATHY; BOVINE SPONGIFORM ENCEPHALOPATHY AGENT; CONTROLLED STUDY; GENOTYPE; HUMAN; NONHUMAN; PRIMATE; PROTEIN ANALYSIS; PROTEIN MISFOLDING; PROTEIN MISFOLDING CYCLIC AMPLIFICATION; PROTEIN STRUCTURE; SHEEP; VARIANT CREUTZFELDT JAKOB DISEASE; VARIANT CREUTZFELDT JAKOB DISEASE AGENT; VIREMIA; VIRUS DETECTION; VIRUS GENE; VIRUS TRANSMISSION; WESTERN BLOTTING; ANIMAL; BLOOD EXAMINATION; BOVINE; CREUTZFELDT-JAKOB SYNDROME; EARLY DIAGNOSIS; ENCEPHALOPATHY, BOVINE SPONGIFORM; MACACA FASCICULARIS; MALE; PIG; PRION; PROCEDURES; TRANSMISSION;

AMINO ACID SEQUENCE; ANIMALS; CATTLE; CREUTZFELDT-JAKOB SYNDROME; EARLY DIAGNOSIS; ENCEPHALOPATHY, BOVINE SPONGIFORM; HEMATOLOGIC TESTS; HUMANS; MACACA FASCICULARIS; MALE; PRIONS; SHEEP; SWINE;

EID: 84903443659     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004202     Document Type: Article

References (66)

1. Bruce ME, Will RG, Ironside JW, McConnell I, Drummond D, et al. (1997) Transmissions to mice indicate that 'new variant' CJD is caused by the BSE agent [see comments]. Nature 389: 498-501.
2. Herzog C, Riviere J, Lescoutra-Etchegaray N, Charbonnier A, Leblanc V, et al. (2005) PrPTSE distribution in a primate model of variant, sporadic, and iatrogenic Creutzfeldt-Jakob disease. J Virol 79: 14339-14345.
3. Houston F, Foster JD, Chong A, Hunter N, Bostock CJ, (2000) Transmission of BSE by blood transfusion in sheep. Lancet 356: 999-1000.
4. Llewelyn CA, Hewitt PE, Knight RS, Amar K, Cousens S, et al. (2004) Possible transmission of variant Creutzfeldt-Jakob disease by blood transfusion. Lancet 363: 417-421.
5. Peden AH, Head MW, Ritchie DL, Bell JE, Ironside JW, (2004) Preclinical vCJD after blood transfusion in a PRNP codon 129 heterozygous patient. Lancet 364: 527-529.
6. Peden A, McCardle L, Head MW, Love S, Ward HJ, et al. (2010) Variant CJD infection in the spleen of a neurologically asymptomatic UK adult patient with haemophilia. Haemophilia 16: 296-304.
7. Garske T, Ghani AC, (2010) Uncertainty in the tail of the variant Creutzfeldt-Jakob disease epidemic in the UK. PLoS One 5: e15626.
8. Hilton DA, Ghani AC, Conyers L, Edwards P, McCardle L, et al. (2004) Prevalence of lymphoreticular prion protein accumulation in UK tissue samples. J Pathol 203: 733-739.
9. Gill ON, Spencer Y, Richard-Loendt A, Kelly C, Dabaghian R, et al. (2013) Prevalent abnormal prion protein in human appendixes after bovine spongiform encephalopathy epizootic: large scale survey. BMJ 347: f5675.
10. Beringue V, Herzog L, Jaumain E, Reine F, Sibille P, et al. (2012) Facilitated cross-species transmission of prions in extraneural tissue. Science 335: 472-475.
11. Cooper JK, Ladhani K, Minor P, (2012) Comparison of candidate vCJD in vitro diagnostic assays using identical sample sets. Vox Sang 102: 100-109.
12. Douet JY, Zafar S, Perret-Liaudet A, Lacroux C, Lugan S, et al. (2014) Detection of infectivity in blood of persons with variant and sporadic Creutzfeldt-Jakob disease. Emerg Infect Dis 20: 114-117.
13. Brown P, Rohwer RG, Dunstan BC, MacAuley C, Gajdusek DC, et al. (1998) The distribution of infectivity in blood components and plasma derivatives in experimental models of transmissible spongiform encephalopathy. Transfusion 38: 810-816.
14. Lacroux C, Vilette D, Fernandez-Borges N, Litaise C, Lugan S, et al. (2012) Prionemia and leuco-platelet associated infectivity in sheep TSE models. J Virol 86 (4) (): 2056-66.
15. Mathiason CK, Hayes-Klug J, Hays SA, Powers J, Osborn DA, et al. (2010) B cells and platelets harbor prion infectivity in the blood of deer infected with chronic wasting disease. J Virol 84: 5097-5107.
16. McCutcheon S, Alejo Blanco AR, Houston EF, de Wolf C, Tan BC, et al. (2011) All Clinically-Relevant Blood Components Transmit Prion Disease following a Single Blood Transfusion: A Sheep Model of vCJD. PLoS One 6: e23169.
17. Saborio GP, Permanne B, Soto C, (2001) Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature 411: 810-813.
18. Castilla J, Saa P, Soto C, (2005) Detection of prions in blood. Nat Med 11: 982-985.
19. Thorne L, Terry LA, (2008) In vitro amplification of PrPSc derived from the brain and blood of sheep infected with scrapie. J Gen Virol 89: 3177-3184.
20. Jones M, Peden AH, Yull H, Wight D, Bishop MT, et al. (2009) Human platelets as a substrate source for the in vitro amplification of the abnormal prion protein (PrP) associated with variant Creutzfeldt-Jakob disease. Transfusion 49: 376-384.
21. Jones M, Peden AH, Prowse CV, Groner A, Manson JC, et al. (2007) In vitro amplification and detection of variant Creutzfeldt-Jakob disease PrPSc. J Pathol 213: 21-26.
22. Simmons HA, Simmons MM, Spencer YI, Chaplin MJ, Povey G, et al. (2009) Atypical scrapie in sheep from a UK research flock which is free from classical scrapie. BMC Vet Res 5: 8.
23. Lacroux C, Corbiere F, Tabouret G, Lugan S, Costes P, et al. (2007) Dynamics and genetics of PrPSc placental accumulation in sheep. J Gen Virol 88: 1056-1061.
24. Moreno CR, Moazami-Goudarzi K, Laurent P, Cazeau G, Andreoletti O, et al. (2007) Which PrP haplotypes in a French sheep population are the most susceptible to atypical scrapie? Arch Virol 152: 1229-1232.
25. Comoy EEC, Jaffre N, Mikol J, Durand V, Luccantoni S, et al. (2013) Contaminated Blood Products Induce an Atypical Prion Disease in Primates in the Absence of Detectable Abnormal Prion Protein. Vox Sanguinis 105: 198-198.
26. Edgeworth JA, Farmer M, Sicilia A, Tavares P, Beck J, et al. (2011) Detection of prion infection in variant Creutzfeldt-Jakob disease: a blood-based assay. Lancet 377: 487-493.
27. Uro-Coste E, Cassard H, Simon S, Lugan S, Bilheude JM, et al. (2008) Beyond PrP res type 1/type 2 dichotomy in Creutzfeldt-Jakob disease. PLoS Pathog 4: e1000029.
28. Castilla J, Gutierrez Adan A, Brun A, Pintado B, Ramirez MA, et al. (2003) Early detection of PrPres in BSE-infected bovine PrP transgenic mice. Arch Virol 148: 677-691.
29. Le Dur A, Beringue V, Andreoletti O, Reine F, Lai TL, et al. (2005) A newly identified type of scrapie agent can naturally infect sheep with resistant PrP genotypes. Proc Natl Acad Sci U S A 102: 16031-16036.
30. Weissmann C, Fischer M, Raeber A, Bueler H, Sailer A, et al. (1998) The use of transgenic mice in the investigation of transmissible spongiform encephalopathies. Rev Sci Tech 17: 278-290.
31. Beringue V, Herzog L, Reine F, Le Dur A, Casalone C, et al. (2008) Transmission of atypical bovine prions to mice transgenic for human prion protein. Emerg Infect Dis 14: 1898-1901.
32. Fischer M, Rulicke T, Raeber A, Sailer A, Moser M, et al. (1996) Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. Embo J 15: 1255-1264.
33. Kupfer L, Eiden M, Buschmann A, Groschup MH, (2007) Amino acid sequence and prion strain specific effects on the in vitro and in vivo convertibility of ovine/murine and bovine/murine prion protein chimeras. Biochim Biophys Acta 1772: 704-713.
34. Groschup MH, Buschmann A, (2008) Rodent models for prion diseases. Vet Res 39: 32.
35. Andreoletti O, Orge L, Benestad SL, Beringue V, Litaise C, et al. (2011) Atypical/Nor98 scrapie infectivity in sheep peripheral tissues. PLoS Pathog 7: e1001285.
36. Espinosa JC, Andreoletti O, Castilla J, Herva ME, Morales M, et al. (2007) Sheep-passaged bovine spongiform encephalopathy agent exhibits altered pathobiological properties in bovine-PrP transgenic mice. J Virol 81: 835-843.
37. Espinosa JC, Herva ME, Andreoletti O, Padilla D, Lacroux C, et al. (2009) Transgenic mice expressing porcine prion protein resistant to classical scrapie but susceptible to sheep bovine spongiform encephalopathy and atypical scrapie. Emerg Infect Dis 15: 1214-1221.
38. Feraudet C, Morel N, Simon S, Volland H, Frobert Y, et al. (2005) Screening of 145 anti-PrP monoclonal antibodies for their capacity to inhibit PrPSc replication in infected cells. J Biol Chem 280: 11247-11258.
39. Baron TG, Biacabe AG, Bencsik A, Langeveld JP, (2006) Transmission of new bovine prion to mice. Emerg Infect Dis 12: 1125-1128.
40. Kocisko DA, Come JH, Priola SA, Chesebro B, Raymond GJ, et al. (1994) Cell-free formation of protease-resistant prion protein. Nature 370: 471-474.
41. Bossers A, Belt P, Raymond GJ, Caughey B, de Vries R, et al. (1997) Scrapie susceptibility-linked polymorphisms modulate the in vitro conversion of sheep prion protein to protease-resistant forms. Proc Natl Acad Sci U S A 94: 4931-4936.
42. Bossers A, de Vries R, Smits MA, (2000) Susceptibility of sheep for scrapie as assessed by in vitro conversion of nine naturally occurring variants of PrP. J Virol 74: 1407-1414.
43. Horiuchi M, Priola SA, Chabry J, Caughey B, (2000) Interactions between heterologous forms of prion protein: binding, inhibition of conversion, and species barriers. Proc Natl Acad Sci U S A 97: 5836-5841.
44. Raymond GJ, Bossers A, Raymond LD, O'Rourke KI, McHolland LE, et al. (2000) Evidence of a molecular barrier limiting susceptibility of humans, cattle and sheep to chronic wasting disease. Embo J 19: 4425-4430.
45. Raymond GJ, Hope J, Kocisko DA, Priola SA, Raymond LD, et al. (1997) Molecular assessment of the potential transmissibilities of BSE and scrapie to humans. Nature 388: 285-288.
46. Panza G, Luers L, Stohr J, Nagel-Steger L, Weiss J, et al. (2010) Molecular interactions between prions as seeds and recombinant prion proteins as substrates resemble the biological interspecies barrier in vitro. PLoS One 5: e14283.
47. Collinge J, Clarke AR, (2007) A general model of prion strains and their pathogenicity. Science 318: 930-936.
48. Barria MA, Ironside JW, Head MW, (2014) Exploring the zoonotic potential of animal prion diseases: In vivo and in vitro approaches. Prion 8[epub ahead of print].
49. Castilla J, Morales R, Saa P, Barria M, Gambetti P, et al. (2008) Cell-free propagation of prion strains. Embo J 27: 2557-2566.
50. Green KM, Castilla J, Seward TS, Napier DL, Jewell JE, et al. (2008) Accelerated high fidelity prion amplification within and across prion species barriers. PLoS Pathog 4: e1000139.
51. Padilla D, Beringue V, Espinosa JC, Andreoletti O, Jaumain E, et al. (2011) Sheep and goat BSE propagate more efficiently than cattle BSE in human PrP transgenic mice. PLoS Pathog 7: e1001319.
52. Arsac JN, Betemps D, Morignat E, Feraudet C, Bencsik A, et al. (2009) Transmissibility of atypical scrapie in ovine transgenic mice: major effects of host prion protein expression and donor prion genotype. PLoS One 4: e7300.
53. Cordier C, Bencsik A, Philippe S, Betemps D, Ronzon F, et al. (2006) Transmission and characterization of bovine spongiform encephalopathy sources in two ovine transgenic mouse lines (TgOvPrP4 and TgOvPrP59). J Gen Virol 87: 3763-3771.
54. Beringue V, Andreoletti O, Le Dur A, Essalmani R, Vilotte JL, et al. (2007) A bovine prion acquires an epidemic bovine spongiform encephalopathy strain-like phenotype on interspecies transmission. J Neurosci 27: 6965-6971.
55. Jackson GS, Burk-Rafel J, Edgeworth JA, Sicilia A, Abdilahi S, et al. (2014) A highly specific blood test for vCJD. Blood 123: 452-453.
56. Jackson GS, Burk-Rafel J, Edgeworth JA, Sicilia A, Abdilahi S, et al. (2014) Population Screening for Variant Creutzfeldt-Jakob Disease Using a Novel Blood Test: Diagnostic Accuracy and Feasibility Study. JAMA Neurol 71 (4) (): 421-8.
57. Mead S, Wadsworth JD, Porter MC, Linehan JM, Pietkiewicz W, et al. (2014) Variant creutzfeldt-jakob disease with extremely low lymphoreticular deposition of prion protein. JAMA Neurol 71: 340-343.
58. Vamvakas EC, (2011) Universal white blood cell reduction in Europe: has transmission of variant Creutzfeldt-Jakob disease been prevented? Transfus Med Rev 25: 133-144.
59. Cosseddu GM, Nonno R, Vaccari G, Bucalossi C, Fernandez-Borges N, et al. (2011) Ultra-efficient PrP(Sc) amplification highlights potentialities and pitfalls of PMCA technology. PLoS Pathog 7: e1002370.
60. Moudjou M, Sibille P, Fichet G, Reine F, Chapuis J, et al. (2013) Highly infectious prions generated by a single round of microplate-based protein misfolding cyclic amplification. MBio 5: e00829-00813.
61. Mays CE, Yeom J, Kang HE, Bian J, Khaychuk V, et al. (2011) In vitro amplification of misfolded prion protein using lysate of cultured cells. PLoS One 6: e18047.
62. Atarashi R, Wilham JM, Christensen L, Hughson AG, Moore RA, et al. (2008) Simplified ultrasensitive prion detection by recombinant PrP conversion with shaking. Nat Methods 5: 211-212.
63. Orru CD, Wilham JM, Vascellari S, Hughson AG, Caughey B, (2012) New generation QuIC assays for prion seeding activity. Prion 6: 147-52.
64. Bessen RA, Shearin H, Martinka S, Boharski R, Lowe D, et al. (2010) Prion shedding from olfactory neurons into nasal secretions. PLoS Pathog 6: e1000837.
65. Peden AH, McGuire LI, Appleford NE, Mallinson G, Wilham JM, et al. (2012) Sensitive and specific detection of sporadic Creutzfeldt-Jakob disease brain prion protein using real-time quaking-induced conversion. J Gen Virol 93: 438-449.
66. Orru CD, Wilham JM, Raymond LD, Kuhn F, Schroeder B, et al. (2011) Prion disease blood test using immunoprecipitation and improved quaking-induced conversion. MBio 2: e00078-00011.