Home LiteratureArticle Details
PMID: 14671128 Published · ppublish English Evaluation Study Journal Article Research Support, Non-U.S. Gov't

Cultured peripheral neuroglial cells are highly permissive to sheep prion infection.

Journal of virology ·Vol. 78 ·No. 1 ·2004-01-00 ·Pages 482-90

Archer F, Bachelin C, Andreoletti O, Besnard N, Perrot G, Langevin C, Le Dur A, Vilette D, Baron-Van Evercooren A, Vilotte JL, Laude H

Abstract

Transmissible spongiform encephalopathies arise as a consequence of infection of the central nervous system (CNS) by prions. Spreading of the infectious agent through the peripheral nervous system (PNS) may represent a crucial step toward CNS neuroinvasion, but the modalities of this process have yet to be clarified. Here we provide further evidence that PNS glial cells are likely targets for infection by prions. Glial cell clones originating from dorsal root ganglia of transgenic mice expressing ovine PrP (tgOv) and simian virus 40 T antigen were found to be readily infectible by sheep scrapie agent. This led us to establish two stable cell lines that exhibited features of Schwann cells. These cells were shown to sustain an efficient and stable replication of sheep prion based on the high level of accumulation of abnormal PrP and infectivity in exposed cultures. We also provide evidence for abnormal PrP deposition in peripheral neuroglial cells from scrapie-infected tgOv mice and sheep. These findings have potential implications in terms of designing new cell systems permissive to prions and of peripheral pathobiology of prion infections.

MeSH Terms
Animals Cells, Cultured Female Ganglia, Spinal/cytology Mice Mice, Transgenic Neuroglia/metabolism Neurons/metabolism Peripheral Nervous System/metabolism PrPC Proteins/metabolism PrPSc Proteins/metabolism,pathogenicity Schwann Cells/metabolism Scrapie Sheep
Chemicals
PrPC Proteins PrPSc Proteins
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Archer Fabienne
Unité de Virologie Immunologie Moléculaires, INRA, Jouy-en-Josas, France.
Bachelin Corinne
Andreoletti Olivier
Besnard Nathalie
Perrot Gregory
Langevin Christelle
Le Dur Annick
Vilette Didier
Baron-Van Evercooren Anne
Vilotte Jean-Luc
Laude Hubert
References (59)
59 references, click to expand
  1. Deposition of disease-associated prion protein involves the peripheral nervous system in experimental scrapie.
    Acta Neuropathol. 1999 Nov;98(5):453-7 PMID: 10541866
  2. Incubation periods in six models of intraperitoneally injected scrapie depend mainly on the dynamics of agent replication within the nervous system and not the lymphoreticular system.
    J Gen Virol. 1988 Dec;69 ( Pt 12):2953-60 PMID: 3143808
  3. Entry versus blockade of brain infection following oral or intraperitoneal scrapie administration: role of prion protein expression in peripheral nerves and spleen.
    J Virol. 2000 Jan;74(2):828-33 PMID: 10623745
  4. Neuronal degeneration and neurofilament accumulation in the trigeminal ganglia in Creutzfeldt-Jakob disease.
    Ann Neurol. 1989 Jan;25(1):102-6 PMID: 2643917
  5. Scrapie prion proteins accumulate in the cytoplasm of persistently infected cultured cells.
    J Cell Biol. 1990 Jun;110(6):2117-32 PMID: 1693623
  6. N-terminal truncation of the scrapie-associated form of PrP by lysosomal protease(s): implications regarding the site of conversion of PrP to the protease-resistant state.
    J Virol. 1991 Dec;65(12):6597-603 PMID: 1682507
  7. Mammalian cell lines can be efficiently established in vitro upon expression of the SV40 large T antigen driven by a promoter sequence derived from the human vimentin gene.
    Biol Cell. 1991;73(1):7-14 PMID: 1668064
  8. Establishment and characterization of a mouse Schwann cell line which produces myelin in vivo.
    J Neurosci Res. 1992 May;32(1):15-26 PMID: 1629940
  9. Demyelinating peripheral neuropathy in Creutzfeldt-Jakob disease.
    Muscle Nerve. 1992 Nov;15(11):1234-9 PMID: 1362595
  10. Mice devoid of PrP are resistant to scrapie.
    Cell. 1993 Jul 2;73(7):1339-47 PMID: 8100741
  11. Spontaneously immortalized adult mouse Schwann cells secrete autocrine and paracrine growth-promoting activities.
    J Neurosci Res. 1995 Jun 1;41(2):279-90 PMID: 7650763
  12. Immune system-dependent and -independent replication of the scrapie agent.
    J Virol. 1996 Feb;70(2):1292-5 PMID: 8551598
  13. Sequential appearance and accumulation of pathognomonic markers in the central nervous system of hamsters orally infected with scrapie.
    J Gen Virol. 1996 Aug;77 ( Pt 8):1925-34 PMID: 8760444
  14. Demyelinating peripheral neuropathy with Creutzfeldt-Jakob disease and mutation at codon 200 of the prion protein gene.
    Neurology. 1996 Apr;46(4):1123-7 PMID: 8780103
  15. Generation of monoclonal antibodies against human prion proteins in PrP0/0 mice.
    Mol Med. 1996 Nov;2(6):725-34 PMID: 8972487
  16. Peripheral neuropathy in Creutzfeldt-Jakob disease.
    Neurology. 1997 Mar;48(3):784 PMID: 9065568
  17. Neuro-immune connection in spread of prions in the body?
    Lancet. 1997 Mar 15;349(9054):742-3 PMID: 9074567
  18. PrP-expressing tissue required for transfer of scrapie infectivity from spleen to brain.
    Nature. 1997 Sep 4;389(6646):69-73 PMID: 9288968
  19. A hypothalamic neuronal cell line persistently infected with scrapie prions exhibits apoptosis.
    J Virol. 1997 Nov;71(11):8821-31 PMID: 9343242
  20. A crucial role for B cells in neuroinvasive scrapie.
    Nature. 1997 Dec 18-25;390(6661):687-90 PMID: 9414161
  21. Cerebral targeting indicates vagal spread of infection in hamsters fed with scrapie.
    J Gen Virol. 1998 Mar;79 ( Pt 3):601-7 PMID: 9519840
  22. Prions.
    Proc Natl Acad Sci U S A. 1998 Nov 10;95(23):13363-83 PMID: 9811807
  23. Ectopic expression of prion protein (PrP) in T lymphocytes or hepatocytes of PrP knockout mice is insufficient to sustain prion replication.
    Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):3987-92 PMID: 10097150
  24. Pathological PrP is abundant in sympathetic and sensory ganglia of hamsters fed with scrapie.
    Neurosci Lett. 1999 Apr 16;265(2):135-8 PMID: 10327187
  25. Contact-dependent demyelination by Mycobacterium leprae in the absence of immune cells.
    Science. 2002 May 3;296(5569):927-31 PMID: 11988579
  26. Cultured cell sublines highly susceptible to prion infection.
    J Virol. 2000 May;74(9):4377-86 PMID: 10756052
  27. High yield purification and physico-chemical properties of full-length recombinant allelic variants of sheep prion protein linked to scrapie susceptibility.
    Eur J Biochem. 2000 May;267(10):2833-9 PMID: 10806380
  28. Peripheral pathogenesis of prion diseases.
    Microbes Infect. 2000 May;2(6):613-9 PMID: 10884612
  29. PrP(C) expression in the peripheral nervous system is a determinant of prion neuroinvasion.
    J Gen Virol. 2000 Nov;81(Pt 11):2813-21 PMID: 11038396
  30. Pathogenesis of natural scrapie in sheep.
    Arch Virol Suppl. 2000;(16):57-71 PMID: 11214935
  31. Lack of replicative senescence in normal rodent glia.
    Science. 2001 Feb 2;291(5505):872-5 PMID: 11157166
  32. Ex vivo propagation of infectious sheep scrapie agent in heterologous epithelial cells expressing ovine prion protein.
    Proc Natl Acad Sci U S A. 2001 Mar 27;98(7):4055-9 PMID: 11259656
  33. Prion diseases of humans and animals: their causes and molecular basis.
    Annu Rev Neurosci. 2001;24:519-50 PMID: 11283320
  34. Markedly increased susceptibility to natural sheep scrapie of transgenic mice expressing ovine prp.
    J Virol. 2001 Jul;75(13):5977-84 PMID: 11390599
  35. Scrapie prion protein accumulation by scrapie-infected neuroblastoma cells abrogated by exposure to a prion protein antibody.
    Proc Natl Acad Sci U S A. 2001 Jul 31;98(16):9295-9 PMID: 11470893
  36. Sympathetic innervation of lymphoreticular organs is rate limiting for prion neuroinvasion.
    Neuron. 2001 Jul 19;31(1):25-34 PMID: 11498048
  37. Trypanosoma cruzi trans-sialidase: a potent and specific survival factor for human Schwann cells by means of phosphatidylinositol 3-kinase/Akt signaling.
    Proc Natl Acad Sci U S A. 2001 Aug 14;98(17):9936-41 PMID: 11481434
  38. Early spread of scrapie from the gastrointestinal tract to the central nervous system involves autonomic fibers of the splanchnic and vagus nerves.
    J Virol. 2001 Oct;75(19):9320-7 PMID: 11533195
  39. The immunobiology of TSE diseases.
    J Gen Virol. 2001 Oct;82(Pt 10):2307-18 PMID: 11562524
  40. PrP(CWD) in the myenteric plexus, vagosympathetic trunk and endocrine glands of deer with chronic wasting disease.
    J Gen Virol. 2001 Oct;82(Pt 10):2327-34 PMID: 11562526
  41. The transgenic ICP4 promoter is activated in Schwann cells in trigeminal ganglia of mice latently infected with herpes simplex virus type 1.
    J Virol. 2001 Nov;75(21):10401-8 PMID: 11581408
  42. PrP expression and replication by Schwann cells: implications in prion spreading.
    J Virol. 2002 Mar;76(5):2434-9 PMID: 11836421
  43. New in vivo and ex vivo models for the experimental study of sheep scrapie: development and perspectives.
    C R Biol. 2002 Jan;325(1):49-57 PMID: 11862622
  44. Transfer of scrapie prion infectivity by cell contact in culture.
    Curr Biol. 2002 Apr 2;12(7):523-30 PMID: 11937020
  45. Retrograde transport of transmissible mink encephalopathy within descending motor tracts.
    J Virol. 2002 Jun;76(11):5759-68 PMID: 11992004
  46. Signals that determine Schwann cell identity.
    J Anat. 2002 Apr;200(4):367-76 PMID: 12090403
  47. Selective expression of prion protein in peripheral tissues of the adult mouse.
    Neuroscience. 2002;113(1):177-92 PMID: 12123696
  48. Unhampered prion neuroinvasion despite impaired fast axonal transport in transgenic mice overexpressing four-repeat tau.
    J Neurosci. 2002 Sep 1;22(17):7471-7 PMID: 12196569
  49. Phenotyping of protein-prion (PrPsc)-accumulating cells in lymphoid and neural tissues of naturally scrapie-affected sheep by double-labeling immunohistochemistry.
    J Histochem Cytochem. 2002 Oct;50(10):1357-70 PMID: 12364569
  50. Creutzfeldt-Jakob disease with amyotrophy and demyelinating polyneuropathy.
    Arch Neurol. 2002 Nov;59(11):1811-4 PMID: 12433270
  51. Transmission of prions.
    Proc Natl Acad Sci U S A. 2002 Dec 10;99 Suppl 4:16378-83 PMID: 12181490
  52. Rapid prion neuroinvasion following tongue infection.
    J Virol. 2003 Jan;77(1):583-91 PMID: 12477862
  53. Disease-associated PrP in the enteric nervous system of scrapie-affected Suffolk sheep.
    J Gen Virol. 2003 May;84(Pt 5):1327-38 PMID: 12692300
  54. Structure and behavior of rat primary and secondary Schwann cells in vitro.
    Exp Cell Res. 1981 Feb;131(2):283-97 PMID: 7202536
  55. Development of oligodendrocytes and Schwann cells studied with a monoclonal antibody against galactocerebroside.
    Proc Natl Acad Sci U S A. 1982 Apr;79(8):2709-13 PMID: 7045870
  56. Pathogenesis of mouse scrapie. Evidence for direct neural spread of infection to the CNS after injection of sciatic nerve.
    J Neurol Sci. 1983 Oct-Nov;61(3):315-25 PMID: 6418861
  57. In vitro replication of scrapie agent in a neuronal model: infection of PC12 cells.
    J Gen Virol. 1984 Dec;65 ( Pt 12):2191-8 PMID: 6439820
  58. Analyses of frequency of infection, specific infectivity, and prion protein biosynthesis in scrapie-infected neuroblastoma cell clones.
    J Virol. 1988 Aug;62(8):2845-9 PMID: 2899175
  59. Disease associated prion protein may deposit in the peripheral nervous system in human transmissible spongiform encephalopathies.
    Acta Neuropathol. 1999 Nov;98(5):458-60 PMID: 10541867
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
DOI
10.1128/jvi.78.1.482-490.2004
Published
2004-01-00
Pages
482-90
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC303391
Subset
IM
External Links
PubMed source DOI: 10.1128/jvi.78.1.482-490.2004 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2