Human embryonic stem cells rapidly take up and then clear exogenous human and animal prions in vitro

Journal of Pathology

Volumn 223, Issue 5, 2011, Pages 635-645

  Krejciova, Zuzana ^a   Pells, Steve ^b   Cancellotti, Enrico ^c   Freile, Paz ^b   Bishop, Matthew ^a   Samuel, Kay ^b,d   Barclay, G Robin ^b,d   Ironside, James W ^a   Manson, Jean C ^c   Turner, Marc L ^b,d   De Sousa, Paul ^b   Head, Mark W ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d SCOTTISH NATIONAL BLOOD TRANSFUSION SERVICE   (United Kingdom)

Author keywords

BSE; Cell culture; Creutzfeldt Jakob disease (CJD); Iatrogenic transmission; Prion protein (PrP); Prions; Stem cells

Indexed keywords

MESSENGER RNA; PRION PROTEIN;

ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL POPULATION; CELL RENEWAL; CODON; CONTROLLED STUDY; DISEASE PREDISPOSITION; EMBRYO; EMBRYONIC STEM CELL; GENETIC TRAIT; GENOTYPE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; NONHUMAN; PRION; PRION DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

ANIMALS; CATTLE; CELL DIFFERENTIATION; CELLS, CULTURED; CREUTZFELDT-JAKOB SYNDROME; EMBRYONIC STEM CELLS; ENCEPHALOPATHY, BOVINE SPONGIFORM; HUMANS; POLYMORPHISM, GENETIC; PRIONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; UP-REGULATION;

EID: 79952551284     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2832     Document Type: Article

References (50)

1. Akimov S, Vasilyeva I, Yakovleva O, et al. Murine bone marrow stromal cell culture with features of mesenchymal stem cells susceptible to mouse-adapted human TSE. Folia Neuropathol 2009; 47: 205-214.
2. Cobo F, Talavera P, Concha A. Diagnostic approaches for viruses and prions in stem cell banks. Virology 2006; 247: 1-10.
3. Cushman M, Johnson BS, King OD, et al. Prion-like disorders: blurring the divide between transmissibility and infectivity. J Cell Sci 2010; 123: 1191-1201.
4. Prusiner SB. Shattuck lecture - neurodegenerative diseases and prions. N Engl J Med 2001; 344: 1516-1526. (Pubitemid 32429212)
5. Aguzzi A, Heikenwalder M, Polymenidou M. Insights into prion strains and neurotoxicity. Nat Rev Mol Cell Biol 2007; 8: 552-561. (Pubitemid 46985384)
6. Caughey B, Baron GS. Prions and their partners in crime. Nature 2006; 443: 803-810. (Pubitemid 44622685)
7. Collinge J, Clarke AR. A general model of prion strains and their pathogenicity. Science 2007; 318: 930-936. (Pubitemid 350098981)
8. Stephenson J. Halting the spread of human prion disease - exceptional measures for an exceptional problem. J Hosp Infect 2007; 65: 14-18. (Pubitemid 46823049)
9. Peden AH, Head MW, Jones M, et al. Advances in the development of a screening test for variant Creutzfeldt-Jakob disease. Expert Opin Med Diag 2008; 2: 207-219. (Pubitemid 351338049)
10. Turner ML, Ludlam CA. An update on the assessment and management of the risk of transmission of variant Creutzfeldt-Jakob disease by blood and plasma products. Br J Haematol 2009; 144: 14-23.
11. Bruce ME, Will RG, Ironside JW, et al. Transmission to mice indicate that 'new variant' CJD is caused by the BSE agent. Nature 1997; 389: 498-501.
12. Collinge J, Sidle KC, Meads J, et al. Molecular analysis of prion strain variation and the aetiology of 'new variant' CJD. Nature 1996; 383: 685-690.
13. Will RG, Ironside JW, Zeidler M, et al. A new variant of Creutzfeldt-Jakob disease in the UK. Lancet 1996; 347: 921-925. (Pubitemid 26102546)
14. Hewitt PE, Llewelyn CA, Mackenzie J, et al. Creutzfeldt-Jakob disease and blood transfusion: results of the UK Transfusion Medicine Epidemiological Review study. Vox Sang 2006; 91: 221-230. (Pubitemid 44337279)
15. Llewelyn CA, Hewitt PE, Knight RSG, et al. Possible transmission of variant Creutzfeldt-Jakob disease by blood transfusion. Lancet 2004; 363: 417-421. (Pubitemid 38210057)
16. Peden AH, Head MW, Ritchie DL, et al. Preclinical vCJD after blood transfusion in a PRNP codon 129 heterozygous patient. Lancet 2004; 364: 527-529. (Pubitemid 39070413)
17. Wroe SJ, Pal S, Siddique D, et al. Clinical presentation and premortem diagnosis of variant Creutzfeldt-Jakob disease associated with blood transfusion. Lancet 2006; 368: 2061-2067. (Pubitemid 44855106)
18. Brown P, Preece M, Brandel JP, et al. Iatrogenic Creutzfeldt-Jakob disease at the millennium. Neurology 2000; 55: 1075-1081.
19. Brown P, Brandel JP, Preese M, et al. Iatrogenic Creutzfeldt-Jakob disease: the waning of an era. Neurology 2006; 67: 389-393. (Pubitemid 44214958)
20. De Sousa P. Optimising the therapeutic safety of human embryo stem cells through the evolution of defined culture systems supporting their isolation. Expert Opin Biol Ther 2006; 6: 551-554. (Pubitemid 43837182)
21. Ironside JW, Ghetti B, Head MW, et al.: Prion diseases. In Greenfield's Neuropathology, 8th edn, Love S, Lious DN, Ellison D (eds). Hodder Arnold: London, 2008; 1197-1273.
22. Watts JC, Balachandran J, Westaway D. The expanding universe of prion diseases. PLoS Pathog 2006; 2: e26.
23. Gambetti P, Dong Z, Yuan J, et al. A novel human prion disease with abnormal prion protein sensitive to protease. Ann Neurol 2008; 63: 697-708. (Pubitemid 351945529)
24. Barron R, Campbell SL, King D, et al. High titres of transmissible spongiform encephalopathy infectivity associated with extremely low levels of PrPSc in vivo. J Biol Chem 2007; 282: 35878-35886. (Pubitemid 350277109)
25. Piccardo P, Manson JC, King D, et al. Accumulation of prion protein in the brain that is not associated with transmissible disease. Proc Natl Acad Sci USA 2007; 104: 4712-4717. (Pubitemid 47186290)
26. Bueler H, Aguzzi A, Sailer A, et al. Mice devoid of PrP are resistant to scrapie. Cell 1993; 73: 1339-1347. (Pubitemid 23201147)
27. Manson JC, Clarke AR, McBride PA, et al. PrP gene dosage determines the timing but not the final intensity or distribution of lesions in scrapie pathology. Neurodegeneration 1994; 3: 331-340.
28. Bishop MT, Pennington C, Heath CA, et al. PRNP variation in UK sporadic and variant Creutzfeldt-Jakob disease highlights genetic risk factors and a novel non-synonymous polymorphism. BMC Med Genet 2009; 10: 146.
29. Collinge J, Whitfield J, McKintosh E, et al. Kuru in the 21st century - an acquired human prion disease with very long incubation times. Lancet 2006; 367: 2068-2074.
30. Mastrianni, JA. The genetics of prion diseases. Genet Med 2010; 12: 187-195.
31. Sc types: an updated classification. Acta Neuropathol 2009; 118: 659-671.
32. Fletcher JM, Ferrier PM, Gardner JO, et al. Variation in humanized and defined culture conditions supporting derivation of new human embryonic stem cell lines. Cloning Stem Cells 2006; 8: 319-334. (Pubitemid 46146039)
33. De Sousa, PA, Gardner J, Sneddon S, et al. Clinically failed eggs as a source of normal human embryo stem cells. Stem Cell Res 2009; 2: 188-197.
34. Starke R, Harrison P, Mackie I, et al. The expression of prion protein (PrPC) in the megakaryocyte lineage. J Thromb Haemost 2005; 3: 1266-1273. (Pubitemid 41725252)
35. Xu C, Inokuma MS, Denham K, et al. Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol 2001; 19: 971-974. (Pubitemid 32947578)
36. Yull, HM, Ritchie DL, Langeveld JP, et al. Detection of type 1 prion protein in variant Creutzfeldt-Jakob disease. Am J Pathol 2006; 168: 151-157. (Pubitemid 43062568)
37. Watts JC, Westaway D. The prion protein family: diversity, rivalry and dysfunction. Biochem Biophys Acta 2007; 1772: 654-672. (Pubitemid 46880210)
38. Westergard L, Christensen HM, Harris DA: The cellular prion protein (PrPC): its physiological function and role in disease. Biochem Biophys Acta 2007; 1772: 629-644. (Pubitemid 46880208)
39. Zhang CC, Steele AD, Lindquist S, et al. Prion protein is expressed on long-term repopulating hematopoietic stem cells and is important for their self-renewal. Proc Natl Acad Sci USA 2006; 103: 2184-2189. (Pubitemid 43271644)
40. Kent DG, Copley MR, Benz C, et al. Prospective isolation and molecular characterisation of hematopoietic stem cells with durable self-renewal potential. Blood 2009; 113: 6342-6350.
41. Lee YJ, Baskakov IV. Treatment with normal prion protein delays differentiation and helps maintain high proliferation activity in human embryonic stem cells. J Neurochem 2010; 114: 362-373.
42. Manson JC, West JD, Thomson V, et al. The prion protein gene: a role in mouse embryogenesis? Development 1992; 15: 117-122.
43. Kaski D, Mead S, Hyare H, et al. Variant CJD in an individual heterozygous for PRNP codon 129. Lancet 2009; 374: 2128.
44. Peden AH, McCardle L, Head MW, et al. Variant CJD infection in the spleen of a neurologically asymptomatic UK adult patient with haemophilia. Haemophilia 2010; 16: 296-304.
45. Bishop MT, Hart P, Aitchison L, et al. Predicting susceptibility and incubation time of human-to-human transmission of vCJD. Lancet Neurol 2006; 5: 393-398.
46. Greil CS, Vorberg IM, Ward AE, et al. Acute cellular uptake of abnormal prion protein is cell type and scrapie strain independent. Virology 2008; 379: 284-293.
47. Yuan J, Xiao X, McGeehan J, et al. Insoluble aggregates and protease-resistant conformers of prion protein in uninfected human brains. J Biol Chem 2006; 281: 34848-34858. (Pubitemid 46036524)
48. Milhavet O, Casanova D, Chevallier N, et al. Neural stem cell model for prion propagation. Stem Cells 2006; 24: 2284-2291. (Pubitemid 44527482)
49. Giri RK, Young R, Pitstick R, et al. Prion infection of mouse neurospheres. Proc Natl Acad Sci USA 2006; 103: 3875-3880.
50. Paquet S, Daude N, Courageot MP, et al. PrPc does not mediate internalization of PrPSc but is required at an early stage for de novo prion infection of Rov cells. J Virology 2007; 81: 10786-10791. (Pubitemid 47463351)