Pathogenesis of chronic wasting disease in cervidized transgenic mice

American Journal of Pathology

Volumn 176, Issue 6, 2010, Pages 2785-2797

  Seelig, Davis M ^a   Mason, Gary L ^a   Telling, Glenn C ^b   Hoover, Edward A ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PRION PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; BRAIN; CHRONIC WASTING DISEASE; CONTROLLED STUDY; DEER; DISEASE COURSE; DISEASE TRANSMISSION; ENDOCRINE GLAND; EPITHELIUM; FEMALE; HEMATOPOIETIC TISSUE; IMMUNOHISTOCHEMISTRY; INCUBATION TIME; INOCULATION; LONGITUDINAL STUDY; LYMPH NODE; LYMPHOID TISSUE; MALE; MOUSE; NERVOUS TISSUE; NONHUMAN; NUCLEOTIDE SEQUENCE; PANCREAS ISLET; PATHOGENESIS; PEYER PATCH; PRION DISEASE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SALIVARY GLAND; SPLEEN; TRANSGENIC MOUSE; ANIMAL; BOVIDS; DISEASE MODEL; GENETICS; METABOLISM; PATHOLOGY; TISSUE DISTRIBUTION; TRANSMISSION;

ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; DISEASE TRANSMISSION, INFECTIOUS; MICE; MICE, TRANSGENIC; PRPC PROTEINS; RUMINANTS; TISSUE DISTRIBUTION; WASTING DISEASE, CHRONIC;

EID: 77953178818     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090710     Document Type: Article

References (84)

1. Miller MW, Williams ES: Prion disease: horizontal prion transmission in mule deer. Nature 2003, 425:35-36
2. Miller MW, Wild MA, Williams ES: Epidemiology of chronic wasting disease in captive Rocky Mountain elk. J Wildl Dis 1998, 34:532-538
3. Miller MW, Wild MA: Epidemiology of chronic wasting disease in captive white-tailed and mule deer. J Wildl Dis 2004, 40:320-327 (Pubitemid 39047954)
4. Williams ES, Young S: Spongiform encephalopathies in Cervidae. Rev Sci Tech 1992, 11:551-567
5. Angers RC, Browning SR, Seward TS, Sigurdson CJ, Miller MW, Hoover EA, Telling GC: Prions in skeletal muscles of deer with chronic wasting disease. Science 2006, 311:1117
6. Browning SR, Mason GL, Seward T, Green M, Eliason GA, Mathiason C, Miller MW, Williams ES, Hoover E, Telling GC: Transmission of prions from mule deer and elk with chronic wasting disease to transgenic mice expressing cervid PrP. J Virol 2004, 78:13345-13350
7. Kong Q, Huang S, Zou W, Vanegas D, Wang M, Wu D, Yuan J, Zheng M, Bai H, Deng H, Chen K, Jenny AL, O'Rourke K, Belay ED, Schonberger LB, Petersen RB, Sy MS, Chen SG, Gambetti P: Chronic wasting disease of elk: transmissibility to humans examined by transgenic mouse models. J Neurosci 2005, 25:7944-7949
8. Tamgüney G, Giles K, Bouzamondo-Bernstein E, Bosque PJ, Miller MW, Safar J, DeArmond SJ, Prusiner SB: Transmission of elk and deer prions to transgenic mice. J Virol 2006, 80:9104-9114
9. Trifilo MJ, Ying G, Teng C, Oldstone MB: Chronic wasting disease of deer and elk in transgenic mice: oral transmission and pathobiology. Virology 2007, 365:136-143
10. LaFauci G, Carp RI, Meeker HC, Ye X, Kim JI, Natelli M, Cedeno M, Petersen RB, Kascsak R, Rubenstein R: Passage of chronic wasting disease prion into transgenic mice expressing Rocky Mountain elk (Cervus elaphus nelsoni) PrPC. J Gen Virol 2006, 87:3773-3780
11. Scott MR, Safar J, Telling G, Nguyen O, Groth D, Torchia M, Koehler R, Tremblay P, Walther D, Cohen FE, DeArmond SJ, Prusiner SB: Identification of a prion protein epitope modulating transmission of bovine spongiform encephalopathy prions to transgenic mice. Proc Natl Acad Sci USA 1997, 94:14279-14284
12. Telling GC: Prion protein genes and prion diseases: studies in transgenic mice. Neuropathol Appl Neurobiol 2000, 26:209-220
13. Telling GC, Scott M, Hsiao KK, Foster D, Yang SL, Torchia M, Sidle KC, Collinge J, DeArmond SJ, Prusiner SB: Transmission of Creutzfeldt-Jakob disease from humans to transgenic mice expressing chimeric human-mouse prion protein. Proc Natl Acad Sci USA 1994, 91:9936-9940
14. Telling GC, Scott M, Mastrianni J, Gabizon R, Torchia M, Cohen FE, DeArmond SJ, Prusiner SB: Prion propagation in mice expressing human and chimeric PrP transgenes implicates the interaction of cellular PrP with another protein. Cell 1995, 83:79-90
15. Scott MR, Kohler R, Foster D, Prusiner SB: Chimeric prion protein expression in cultured cells and transgenic mice. Protein Sci 1992, 1:986-997 (Pubitemid 23009207)
16. Baron T: Mouse models of prion disease transmission. Trends Mol Med 2002, 8:495-500
17. Sigurdson CJ, Williams ES, Miller MW, Spraker TR, O'Rourke KI, Hoover EA: Oral transmission and early lymphoid tropism of chronic wasting disease PrPres in mule deer fawns (Odocoileus hemionus). J Gen Virol 1999, 80(Pt 10):2757-2764
18. Carlson GA, Kingsbury DT, Goodman PA, Coleman S, Marshall ST, DeArmond S, Westaway D, Prusiner SB: Linkage of prion protein and scrapie incubation time genes. Cell 1986, 46:503-511
19. Petrusz P, Bullock G. Edited by H. Hedrich: The laboratory mouse. Elsevier Academic Press 2004
20. Garssen GJ, Van Keulen LJ, Farquhar CF, Smits MA, Jacobs JG, Bossers A, Meloen RH, Langeveld JP: Applicability of three anti-PrP peptide sera including staining of tonsils and brainstem of sheep with scrapie. Microsc Res Tech 2000, 50:32-39
21. Sigurdson CJ, Barillas-Mury C, Miller MW, Oesch B, van Keulen LJ, Langeveld JP, Hoover EA: PrP(CWD) lymphoid cell targets in early and advanced chronic wasting disease of mule deer. J Gen Virol 2002, 83:2617-2628
22. Brandner S, Isenmann S, Raeber A, Fischer M, Sailer A, Kobayashi Y, Marino S, Weissmann C, Aguzzi A: Normal host prion protein necessary for scrapie-induced neurotoxicity. Nature 1996, 379:339-343
23. Glatzel M, Aguzzi A: PrP(C) expression in the peripheral nervous system is a determinant of prion neuroinvasion. J Gen Virol 2000, 81:2813-2821
24. Blättler T, Brandner S, Raeber AJ, Klein MA, Voigtlander T, Weissmann C, Aguzzi A: PrP-expressing tissue required for transfer of scrapie infectivity from spleen to brain. Nature 1997, 389:69-73
25. Le Pichon CE, Firestein S: Expression and localization of the prion protein PrP(C) in the olfactory system of the mouse. J Comp Neurol 2008, 508:487-499
26. Burthem J, Urban B, Pain A, Roberts DJ: The normal cellular prion protein is strongly expressed by myeloid dendritic cells. Blood 2001, 98:3733-3738
27. Liu T, Li R, Wong BS, Liu D, Pan T, Petersen RB, Gambetti P, Sy MS: Normal cellular prion protein is preferentially expressed on subpopulations of murine hemopoietic cells. J Immunol 2001, 166:3733-3742 (Pubitemid 32224896)
28. Ford MJ, Burton LJ, Morris RJ, Hall SM: Selective expression of prion protein in peripheral tissues of the adult mouse. Neuroscience 2002, 113:177-192
29. Mathiason C, Foos T, Eliason GA, Sigurdson CJ, Miller M, Lewis-Weis L, Fischer J, Hoover E: Cervid PrPc Quantitation and Tissue Mapping. Presented at the College of Veterinary Medicine and Biomedical Sciences Research Day (Microbiology, Immunology, and Pathology). 2004 January 29. Fort Collins, CO.
30. Zhang CC, Steele AD, Lindquist S, Lodish HF: 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
31. Brown KL, Ritchie DL, McBride PA, Bruce ME: Detection of PrP in extraneural tissues. Microsc Res Tech 2000, 50:40-45
32. Asante EA, Linehan JM, Desbruslais M, Joiner S, Gowland I, Wood AL, Welch J, Hill AF, Lloyd SE, Wadsworth JD, Collinge J: BSE prions propagate as either variant CJD-like or sporadic CJD-like prion strains in transgenic mice expressing human prion protein. EMBO J 2002, 21:6358-6366
33. Prusiner SB, Scott M, Foster D, Pan KM, Groth D, Mirenda C, Torchia M, Yang SL, Serban D, Carlson GA, Hoppe PC, Westaway D, DeArmond SJ: Transgenetic studies implicate interactions between homologous PrP isoforms in scrapie prion replication. Cell 1990, 63:673-686 (Pubitemid 120035041)
34. Scott M, Foster D, Mirenda C, Serban D, Coufal F, Walchli M, Torchia M, Groth D, Carlson G, DeArmond SJ, Westaway D, Prusiner SB: Transgenic mice expressing hamster prion protein produce species-specific scrapie infectivity and amyloid plaques. Cell 1989, 59:847-857
35. Tremblay P, Bouzamondo-Bernstein E, Heinrich C, Prusiner SB, DeArmond SJ: Developmental expression of PrP in the post-implantation embryo. Brain Res 2007, 1139:60-67
36. Sigurdson CJ, Spraker TR, Miller MW, Oesch B, Hoover EA: PrP(CWD) in the myenteric plexus, vagosympathetic trunk and endocrine glands of deer with chronic wasting disease. J Gen Virol 2001, 82:2327-2334 (Pubitemid 32936766)
37. Muramoto T, Kitamoto T, Tateishi J, Goto I: Accumulation of abnormal prion protein in mice infected with Creutzfeldt-Jakob disease via intraperitoneal route: a sequential study. Am J Pathol 1993, 143:1470-1479 (Pubitemid 124000661)
38. Mabbott NA, Mackay F, Minns F, Bruce ME: Temporary inactivation of follicular dendritic cells delays neuroinvasion of scrapie. Nat Med 2000, 6:719-720
39. Mabbott NA, MacPherson GG: Prions and their lethal journey to the brain. Nat Rev Microbiol 2006, 4:201-211
40. Mabbott NA, Young J, McConnell I, Bruce ME: Follicular dendritic cell dedifferentiation by treatment with an inhibitor of the lymphotoxin pathway dramatically reduces scrapie susceptibility. J Virol 2003, 77:6845-6854
41. Mohan J, Bruce ME, Mabbott NA: Follicular dendritic cell dedifferentiation reduces scrapie susceptibility following inoculation via the skin. Immunology 2005, 114:225-234
42. Sc from the gut. J Gen Virol 2002, 83:267-271
43. Kimberlin RH, Walker CA: The role of the spleen in the neuroinvasion of scrapie in mice. Virus Res 1989, 12:201-211
44. Prinz M, Heikenwalder M, Junt T, Schwarz P, Glatzel M, Heppner FL, Fu YX, Lipp M, Aguzzi A: Positioning of follicular dendritic cells within the spleen controls prion neuroinvasion. Nature 2003, 425:957-962
45. Glatzel M, Heppner FL, Albers KM, Aguzzi A: Sympathetic innervation of lymphoreticular organs is rate limiting for prion neuroinvasion. Neuron 2001, 31:25-34
46. Hunter N, Foster J, Chong A, McCutcheon S, Parnham D, Eaton S, MacKenzie C, Houston F: Transmission of prion diseases by blood transfusion. J Gen Virol 2002, 83:2897-2905 (Pubitemid 35276989)
47. Llewelyn CA, Hewitt PE, Knight RS, Amar K, Cousens S, Mackenzie J, Will RG: Possible transmission of variant Creutzfeldt-Jakob disease by blood transfusion. Lancet 2004, 363:417-421
48. Mathiason CK, Powers JG, Dahmes SJ, Osborn DA, Miller KV, Warren RJ, Mason GL, Hays SA, Hayes-Klug J, Seelig DM, Wild MA, Wolfe LL, Spraker TR, Miller MW, Sigurdson CJ, Telling GC, Hoover EA: Infectious prions in the saliva and blood of deer with chronic wasting disease. Science 2006, 314:133-136
49. Peden AH, Head MW, Ritchie DL, Bell JE, Ironside JW: Preclinical vCJD after blood transfusion in a PRNP codon 129 heterozygous patient. Lancet 2004, 364:527-529
50. Saá P, Castilla J, Soto C: Presymptomatic detection of prions in blood. Science 2006, 313:92-94
51. Viegas P, Chaverot N, Enslen H, Perriere N, Couraud PO, Cazaubon S: Junctional expression of the prion protein PrPC by brain endothelial cells: a role in trans-endothelial migration of human monocytes. J Cell Sci 2006, 119:4634-4643
52. Banks WA, Niehoff ML, Adessi C, Soto C: Passage of murine scrapie prion protein across the mouse vascular blood-brain barrier. Biochem Biophys Res Commun 2004, 318:125-130
53. Beekes M, McBride PA: The spread of prions through the body in naturally acquired transmissible spongiform encephalopathies. FEBS J 2007, 274:588-605
54. Mulcahy ER, Bartz JC, Kincaid AE, Bessen RA: Prion infection of skeletal muscle cells and papillae in the tongue. J Virol 2004, 78:6792-6798
55. Borchelt DR, Koliatsos VE, Guarnieri M, Pardo CA, Sisodia SS, Price DL: Rapid anterograde axonal transport of the cellular prion glycoprotein in the peripheral and central nervous systems. J Biol Chem 1994, 269:14711-14714 (Pubitemid 24194036)
56. Moya KL, Hassig R, Creminon C, Laffont I, Di Giamberardino L: Enhanced detection and retrograde axonal transport of PrPc in peripheral nerve. J Neurochem 2004, 88:155-160 (Pubitemid 38030218)
57. Bruce ME: Agent replication dynamics in a long incubation period model of mouse scrapie. J Gen Virol 1985, 66(Pt 12):2517-2522
58. Field EJ, Caspary EA, and Joyce G: Scrapie agent in blood. Vet Rec 1968, 83:109-110
59. Millson GC, Kimberlin RH, Manning EJ, Collis SC: Early distribution of radioactive liposomes and scrapie infectivity in mouse tissues following administration by different routes. Vet Microbiol 1979, 5:89-99
60. Zoukhri D, Kublin CL: Impaired neurotransmitter release from lacrimal and salivary gland nerves of a murine model of Sjögren's syndrome. Invest Ophthalmol Vis Sci 2001, 42:925-932 (Pubitemid 32289786)
61. Proctor GB, Carpenter GH: Regulation of salivary gland function by autonomic nerves. Auton Neurosci 2007, 133:3-18
62. Vascellari M, Nonno R, Mutinelli F, Bigolaro M, Di Bari MA, Melchiotti E, Marcon S, D'Agostino C, Vaccari G, Conte M, De Grossi L, Rosone F, Giordani F, Agrimi U: PrPSc in salivary glands of scrapie-affected sheep. J Virol 2007, 81:4872-4876
63. McManaman JL, Reyland ME, Thrower EC: Secretion and fluid transport mechanisms in the mammary gland: comparisons with the exocrine pancreas and the salivary gland. J Mammary Gland Biol Neoplasia 2006, 11:249-268
64. Eklund CM, Kennedy RC, Hadlow WJ: Pathogenesis of scrapie virus infection in the mouse. J Infect Dis 1967, 117:15-22
65. Fox KA, Jewell JE, Williams ES, Miller MW: Patterns of PrPCWD accumulation during the course of chronic wasting disease infection in orally inoculated mule deer (Odocoileus hemionus). J Gen Virol 2006, 87:3451-3461
66. Ye X, Carp RI, Yu Y, Kozielski R, Kozlowski P: Hyperplasia and hypertrophy of B cells in the islets of Langerhans in hamsters infected with the 139H strain of scrapie. J Comp Pathol 1994, 110:169-183 (Pubitemid 24091761)
67. Pattison IH, Millson GC: Further observations on the experimental production of scrapie in goats and sheep. J Comp Pathol 1960, 70:182-193
68. McBride PA, Eikelenboom P, Kraal G, Fraser H, Bruce ME: PrP protein is associated with follicular dendritic cells of spleens and lymph nodes in uninfected and scrapie-infected mice. J Pathol 1992, 168:413-418
69. Loewy AD, Franklin MF, Haxhiu MA: CNS monoamine cell groups projecting to pancreatic vagal motor neurons: a transneuronal labeling study using pseudorabies virus. Brain Res 1994, 638:248-260
70. Kesse WK, Parker TL, Coupland RE: The innervation of the adrenal gland. I. The source of pre- and postganglionic nerve fibres to the rat adrenal gland. J Anat 1988, 157:33-41
71. DeJoia C, Moreaux B, O'Connell K, Bessen RA: Prion infection of oral and nasal mucosa. J Virol 2006, 80:4546-4556
72. Thomzig A, Kratzel C, Lenz G, Kruger D, Beekes M: Widespread PrPSc accumulation in muscles of hamsters orally infected with scrapie. EMBO Rep 2003, 4:530-533
73. Andréoletti O, Simon S, Lacroux C, Morel N, Tabouret G, Chabert A, Lugan S, Corbiere F, Ferre P, Foucras G, Laude H, Eychenne F, Grassi J, Schelcher F: PrPSc accumulation in myocytes from sheep incubating natural scrapie. Nat Med 2004, 10:591-593
74. Saraswathi P: Neurohistological observations on the tongue of the monkey (Macaca radiata). J Anat Soc India 2003, 52:7-12
75. Williams ES: Chronic wasting disease. Vet Pathol 2005, 42:530-549
76. Morris JA, Gajdusek DC, Gibbs CJ Jr: Spread of scrapie from inoculated to uninoculated mice. Proc Soc Exp Biol Med 1965, 120:108-110
77. Spraker TR, Zink RR, Cummings BA, Sigurdson CJ, Miller MW, O'Rourke KI: Distribution of protease-resistant prion protein and spongiform encephalopathy in free-ranging mule deer (Odocoileus hemionus) with chronic wasting disease. Vet Pathol 2002, 39:546-556
78. Spraker TR, Zink RR, Cummings BA, Wild MA, Miller MW, O'Rourke KI: Comparison of histological lesions and immunohistochemical staining of proteinase-resistant prion protein in a naturally occurring spongiform encephalopathy of free-ranging mule deer (Odocoileus hemionus) with those of chronic wasting disease of captive mule deer. Vet Pathol 2002, 39:110-119
79. Karita M, Matsumoto S, Kamei T, Shinohara K, Sugiyama T: Direct transmission of H. pylori from challenged to nonchallenged mice in a single cage. Dig Dis Sci 2005, 50:1092-1096
80. Botten J, Mirowsky K, Ye C, Gottlieb K, Saavedra M, Ponce L, Hjelle B: Shedding and intracage transmission of Sin Nombre hantavirus in the deer mouse (Peromyscus maniculatus) model. J Virol 2002, 76:7587-7594
81. Haley NJ: Detection of CWD prions in urine and saliva of deer by transgenic mouse bioassay. PLoS One 2009, 4:e4848
82. Safar JG, Lessard P, Tamguney G, Freyman Y, Deering C, Letessier F, Dearmond SJ, Prusiner SB: Transmission and detection of prions in feces. J Infect Dis 2008, 198:81-89
83. Miller MW, Williams ES, Hobbs NT, Wolfe LL: Environmental sources of prion transmission in mule deer. Emerg Infect Dis 2004, 10:1003-1006
84. Hamir AN, Gidlewski T, Spraker TR, Miller JM, Creekmore L, Crocheck M, Cline T, O'Rourke KI: Preliminary observations of genetic susceptibility of elk (Cervus elaphus nelsoni) to chronic wasting disease by experimental oral inoculation. J Vet Diagn Invest 2006, 18:110-114 (Pubitemid 43188324)