Prion protein expression differences in microglia and astroglia influence scrapie-induced neurodegeneration in the retina and brain of transgenic mice

Journal of Virology

Volumn 81, Issue 19, 2007, Pages 10340-10351

  Kercher, Lisa ^a   Favara, Cynthia ^a   Striebel, James F ^a   LaCasse, Rachel ^a   Chesebro, Bruce ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; PRION PROTEIN; PROTEINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEGENERATION; CELL ACTIVATION; CELL STRUCTURE; CELL TYPE; CELL VACUOLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; MACROGLIA; MICROGLIA; MOUSE; MOUSE STRAIN; NONHUMAN; PRION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA DEGENERATION; SCRAPIE AGENT; STRAIN DIFFERENCE; TRANSGENIC MOUSE; UPREGULATION;

ANIMALS; ASTROCYTES; BRAIN; CHEMOKINES; MICE; MICE, TRANSGENIC; MICROGLIA; NEURODEGENERATIVE DISEASES; PRPSC PROTEINS; RETINA; SCRAPIE; UP-REGULATION;

MUS; MUS MUSCULUS;

EID: 34648834051     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00865-07     Document Type: Article

References (54)

1. Ambrosini, E., and F. Aloisi. 2004. Chemokines and glial cells: a complex network in the central nervous system Neurochem. Res. 29:1017-1038.
2. Baker, C. A., D. Martin, and L. Manuelidis. 2002. Microglia from Creutzfeldt-Jakob disease-infected brains are infectious and show specific mRNA activation profiles J. Virol. 76:10905-10913.
3. Barmada, S. J., and D. A. Harris. 2005. Visualization of prion infection in transgenic mice expressing green fluorescent protein-tagged prion protein. J. Neurosci. 25:5824-5832.
4. Bate, C., R. S. Boshuizen, J. P. Langeveld, and A. Williams. 2002. Temporal and spatial relationship between the death of PrP-damaged neurones and microglial activation. Neuroreport 13:1695-1700.
5. Bate, C., S. Reid, and A. Williams. 2001. Killing of prion-damaged neurones by microglia. Neuroreport 12:2589-2594.
6. Betmouni, S., and V. H. Perry. 1999. The acute inflammatory response in CNS following injection of prion brain homogenate or normal brain homogenate. Neuropathol. Appl. Neurobiol. 25:20-28.
7. Brandner, S., A. Raeber, A. Sailer, T. Blattler, M. Fischer, C. Weissmann, and A. Aguzzi. 1996. Normal host prion protein (PrPC) is required for scrapie spread within the central nervous system. Proc. Natl. Acad. Sci. USA 93:13148-13151.
8. Brown, D. R., B. Schmidt, and H. A. Kretzschmar. 1996. Role of microglia and host prion protein in neurotoxicity of a prion protein fragment. Nature 380:345-347.
9. Bueler, H., A. Aguzzi, A. Sailer, R. A. Greiner, P. Autenried, M. Aguet, and C. Weissmann. 1993. Mice devoid of PrP are resistant to scrapie. Cell 73:1339-1347.
10. Burwinkel, M., C. Riemer, A. Schwarz, J. Schultz, S. Neidhold, T. Bamme, and M. Baier. 2004. Role of cytokines and chemokines in prion infections of the central nervous system. Int. J. Dev. Neurosci. 22:497-505.
11. Cashman, N. R., R. Loertscher, J. Nalbantoglu, I. Shaw, R. J. Kascsak, D. C. Bolton, and P. E. Bendheim. 1990. Cellular isoform of the scrapie agent protein participates in lymphocyte activation. Cell 61:185-192.
12. Caughey, B., R. E. Race, and B. Chesebro. 1988. Detection of prion protein mRNA in normal and scrapie-infected tissues and cell lines. J. Gen. Virol. 69:711-716.
13. Chen, L., P. Yang, and A. Kijlstra. 2002. Distribution, markers, and functions of retinal microglia. Ocul. Immunol. Inflamm. 10:27-39.
14. Dimcheff, D. E., S. Askovic, A. H. Baker, C. Johnson-Fowler, and J. L. Portis. 2003. Endoplasmic reticulum stress is a determinant of retrovirus-induced spongiform neurodegeneration. J. Virol. 77:12617- 12629.
15. Dougherty, R. M. 1964. Animal virus titration techniques, p. 183-186. In R. J. C. Harris (ed.), Techniques in experimental virology. Academic Press, San Diego, CA.
16. Eikelenboom, P., C. Bate, W. A. Van Gool, J. J. Hoozemans, J. M. Rozemuller, R. Veerhuis, and A. Williams. 2002. Neuroinflammation in Alzheimer's disease and prion, disease. Glia 40:232-239.
17. Fraser, H., and A. G. Dickinson. 1985. Targeting of scrapie lesions and spread of agent via the retino-tectal projection. Brain Res. 346:32-41.
18. Galea, I., K. Palin, T. A. Newman, R. N. Van, V. H. Perry, and D. Boche. 2005. Mannose receptor expression specifically reveals perivascular macrophages in normal, injured, and diseased mouse brain. Glia 49:375-384.
19. Giese, A., D. R. Brown, M. H. Groschup, C. Feldmann, I. Haist, and H. A. Kretzschmar. 1998. Role of microglia in neuronal cell death in prion disease. Brain Pathol. 8:449-457.
20. Hardt, M., T. Baron, and M. H. Groschup. 2000. A comparative study of immunohistochemical methods for detecting abnormal prion protein with monoclonal and polyclonal antibodies. J. Comp. Pathol. 122:43-53.
21. Hortells, P., M. Monzon, E. Monleon, C. Acin, A. Vargas, R. Bolea, L. Lujan, and J. J. Badiola. 2006. Pathological findings in retina and visual pathways associated to natural scrapie in sheep. Brain Res. 1108:188-194.
22. Ito, D., Y. Imai, K. Ohsawa, K. Nakajima, Y. Fukuuchi, and S. Kohsaka. 1998. Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res. Mol. Brain Res. 57:1-9.
23. Jeffrey, M., W. G. Halliday, J. Bell, A. R. Johnston, N. K. MacLeod, C. Ingham, A. R. Sayers, D. A. Brown, and J. R. Fraser. 2000. Synapse loss associated with abnormal PrP precedes neuronal degeneration in the scrapie-infected murine hippocampus. Neuropathol. Appl. Neurobiol. 26: 41-54.
24. Kascsak, R. J., R. Rubenstein, P. A. Merz, M. Tonna-DeMasi, R. Fersko, R. I. Carp, H. M. Wisniewski, and H. Diringer. 1987. Mouse polyclonal and monoclonal antibody to scrapie-associated fibril proteins. J. Virol. 61:3688-3693.
25. Kercher, L., C. Favara, C. C. Chan, R. Race, and B. Chesebro. 2004. Differences in scrapie-induced pathology of the retina and brain in transgenic mice that express hamster prion protein in neurons, astrocytes, or multiple cell types. Am. J. Pathol. 165:2055-2067.
26. Kielian, T. 2004. Microglia and chemokines in infectious diseases of the nervous system: views and reviews. Front. Biosci. 9:732-750.
27. Kitamoto, T., J. Tateishi, T. Tashima, I. Takeshita, R. A. Barry, S. J. DeArmond, and S. B. Prusiner. 1986. Amyloid plaques in Creutzfeldt-Jakob disease stain with prion protein antibodies. Ann. Neurol. 20:204-208.
28. Kretzschmar, H. A., S. B. Prusiner, L. E. Stowring, and S. J. DeArmond. 1986. Scrapie prion proteins are synthesized in neurons. Am. J. Pathol. 122:1-5.
29. Lee, H. P., Y. C. Jun, J. K. Choi, J. I. Kim, R. I. Carp, and Y. S. Kim. 2005. The expression of RANTES and chemokine receptors in the brains of scrapie-infected mice. J. Neuroimmunol. 158:26-33.
30. Lewicki, H., A. Tishon, D. Homann, H. Mazarguil, F. Laval, V. C. Asensio, I. L. Campbell, S. DeArmond, B. Coon, C. Teng, J. E. Gairin, and M. B. Oldstone. 2003. T cells infiltrate the brain in murine and human transmissible spongiform encephalopathies. J. Virol. 77:3799-3808.
31. Mallucci, G., A. Dickinson, J. Linehan, P. C. Klohn, S. Brandner, and J. Collinge. 2003. Depleting neuronal PrP in prion infection prevents disease and reverses spongiosis. Science 302:871-874.
32. Mander, P., and G. C. Brown. 2005. Activation of microglial NADPH oxidase is synergistic with glial iNOS expression in inducing neuronal death: a dual-key mechanism of inflammatory neurodegeneration J. Neuroinflamm. 2:20.
33. Marella, M., and J. Chabry. 2004. Neurons and astrocytes respond to prion infection by inducing microglia recruitment. J. Neurosci. 24:620-627.
34. McBride, P. A., P. Eikelenboom, G. Kraal, H. Fraser, and M. E. Bruce. 1992. PrP protein is associated with follicular dendritic cells of spleens and lymph nodes in uninfected and scrapie-infected mice. J. Pathol. 168:413-418.
35. Moser, M., R. J. Colello, U. Pott, and B. Oesch. 1995. Developmental expression of the prion protein gene in glial cells Neuron 14:509-517.
36. Mouillet-Richard, S., M. Ermonval, C. Chebassier, J. L. Laplanche, S. Lehmann, J. M. Launay, and O. Kellermann. 2000. Signal transduction through prion protein. Science 289:1925-1928.
37. Perry, V. H., S. J. Bolton, D. C. Anthony, and S. Betmouni. 1998. The contribution of inflammation to acute and chronic neurodegeneration. Res. Immunol. 149:721-725.
38. Peterson, K. E., J. S. Errett, T. Wei, D. E. Dimcheff, R. Ransohoff, W. A. Kuziel, L. Evans, and B. Chesebro. 2004. MCP-1 and CCR2 contribute to non-lymphocyte-mediated brain disease induced by Fr98 polytropic retrovirus infection in mice: role for astrocytes in retroviral neuropathogenesis. J. Virol. 78:6449-6458.
39. Peyrin, J. M., C. I. Lasmezas, S. Haik, F. Tagliavini, M. Salmona, A. Williams, D. Richie, J. P. Deslys, and D. Dormont. 1999. Microglial cells respond to amyloidogenic PrP peptide by the production of inflammatory cytokines. Neuroreport 10:723-729.
40. Pietri, M., A. Caprini, S. Mouillet-Richard, E. Pradines, M. Ermonval, J. Grassi, O. Kellermann, and B. Schneider. 2006. Overstimulation of PrPC signaling pathways by prion peptide 106-126 causes oxidative injury of bioaminergic neuronal cells. J. Biol. Chem. 281:28470-28479.
41. Priller, J., M. Prinz, M. Heikenwalder, N. Zeller, P. Schwarz, F. L. Heppner, and A. Aguzzi. 2006. Early and rapid engraftment of bone marrow-derived microglia in scrapie. J. Neurosci. 26:11753-11762.
42. Race, R., D. Ernst, A. Jenny, W. Taylor, D. Sutton, and B. Caughey. 1992. Diagnostic implications of detection of proteinase K-resistant protein in spleen, lymph nodes, and brain of sheep. Am. J. Vet. Res. 53:883-889.
43. Race, R., M. Oldstone, and B. Chesebro. 2000. Entry versus blockade of brain infection following oral or intraperitoneal scrapie administration: role of prion protein expression in peripheral nerves and spleen. J. Virol. 74:828-833.
44. Race, R. E., S. A. Priola, R. A. Bessen, D. Ernst, J. Dockter, G. F. Rall, L. Mucke, B. Chesebro, and M. B. Oldstone. 1995. Neuron-specific expression of a hamster prion protein minigene in transgenic mice induces susceptibility to hamster scrapie agent. Neuron 15:1183-1191.
45. Raeber, A. J., R. E. Race, S. Brandner, S. A. Priola, A. Sailer, R. A. Bessen, L. Mucke, J. Manson, A. Aguzzi, M. B. Oldstone, C. Weissmann, and B. Chesebro. 1997. Astrocyte-specific expression of hamster prion protein (PrP) renders PrP knockout mice susceptible to hamster scrapie. EMBO J. 16: 6057-6065.
46. Rock, R. B., G. Gekker, S. Hu, W. S. Sheng, M. Cheeran, J. R. Lokensgard, and P. K. Peterson. 2004. Role of microglia in central nervous system infections. Clin. Microbiol. Rev. 17:942-964.
47. Russelakis-Carneiro, M., S. Betmouni, and V. H. Perry. 1999. Inflammatory response and retinal ganglion cell degeneration following intraocular injection of ME7. Neuropathol. Appl. Neurobiol. 25:196-206.
48. Scott, J. R., and H. Fraser. 1989. Transport and targeting of scrapie infectivity and pathology in the optic nerve projections following intraocular infection. Prog. Clin. Biol. Res. 317:645-652.
49. Tsunoda, I., T. E. Lane, J. Blackett, and R. S. Fujinami. 2004. Distinct roles for IP-10/CXCL10 in three animal models, Theiler's virus infection, EAE, and MHV infection, for multiple sclerosis: implication of differing roles for IP-10. Mult. Scler. 10:26-34.
50. van Keulen, L. J., B. E. Schreuder, R. H. Meloen, B. M. van den Poelen, G. Mooy-Harkes, M. E. Vromans, and J. P. Langeveld. 1995. Immunohistochemical detection and localization of prion protein in brain tissue of sheep with natural scrapie. Vet. Pathol. 32:299-308.
51. Williams, A., P. J. Lucassen, D. Ritchie, and M. Bruce. 1997. PrP deposition, microglial activation, and neuronal apoptosis in murine scrapie. Exp. Neurol. 144:433-438.
52. Williams, A. E., A. M. van Dam, A. H. W. Man, F. Berkenbosch, P. Eikelenboom, and H. Fraser. 1994. Cytokines, prostaglandins and lipocortin-1 are present in the brains of scrapie-infected mice. Brain Res. 654:200-206.
53. Wojtera, M., B. Sikorska, T. Sobow, and P. P. Liberski. 2005. Microglial cells in neurodegenerative disorders. Folia Neuropathol. 43:311-321.
54. Xiang, W., O. Windl, G. Wunsch, M. Dugas, A. Kohlmann, N. Dierkes, I. M. Westner, and H. A. Kretzschmar. 2004. Identification of differentially expressed genes in scrapie-infected mouse brains by using global gene expression technology. J. Virol. 78:11051-11060.