Lesion of the olfactory epithelium accelerates prion neuroinvasion and disease onset when prion replication is restricted to neurons

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Crowell, Jenna ^a   Wiley, James A ^b   Bessen, Richard A ^a  

^a Veterinary Dentistry and Oral Surgery   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DISEASE; BRAIN INFECTION; BRAIN STEM; CONTROLLED STUDY; EOSINOPHIL; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LYMPHOCYTE; MACROPHAGE; MOUSE; NEUTROPHIL; NONHUMAN; NOSE MUCOSA; OLFACTORY EPITHELIUM; OLFACTORY NERVE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRION DISEASE; SENSORY NERVE CELL; SURVIVAL; SYRIAN HAMSTER; TRANSGENIC MOUSE; WESTERN BLOTTING; ANIMAL; BIOLOGICAL MODEL; BRAIN DISEASES; C57BL MOUSE; CRANIAL NERVE; DISEASE MODEL; DRUG EFFECTS; HAMSTER; INNERVATION; MESOCRICETUS; NERVOUS SYSTEM DEVELOPMENT; OLFACTORY MUCOSA; OLFACTORY RECEPTOR NEURON; PATHOGENICITY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PRION; PRION DISEASES; RAT;

ANIMALIA; CRICETINAE; MUS MUSCULUS; MUSTELA;

PRION; PRION PROTEIN; THIAMAZOLE;

ANIMALS; BRAIN DISEASES; CRANIAL NERVES; CRICETINAE; DISEASE MODELS, ANIMAL; MESOCRICETUS; METHIMAZOLE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, NEUROLOGICAL; NEUROGENESIS; OLFACTORY MUCOSA; OLFACTORY NERVE; OLFACTORY RECEPTOR NEURONS; PRION DISEASES; PRIONS; PRPSC PROTEINS; RATS;

EID: 84926512816     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0119863     Document Type: Article

References (71)

1. van Keulen LJ, Schreuder BE, Meloen RH, Mooij-Harkes G, Vromans ME, Langeveld JP. Immunohistochemical detection of prion protein in lymphoid tissues of sheep with natural scrapie. J Clin Microbiol. 1996; 34: 1228-1231. PMID: 8727908
2. van Keulen LJ, Schreuder BE, Vromans ME, Langeveld JP, Smits MA. Scrapie-associated prion protein in the gastrointestinal tract of sheep with natural scrapie. J Comp Pathol. 1999; 121: 55-63. PMID: 10373293
3. Andreoletti O, Berthon P, Marc D, Sarradin P, Grosclaude J, van Keulen L, et al. Early accumulation of PrP(Sc) in gut-associated lymphoid and nervous tissues of susceptible sheep from a Romanov flock with natural scrapie. J Gen Virol. 2000; 81 Pt 12: 3115-3126. PMID: 11086143
4. Heggebo R, Press CM, Gunnes G, Lie KI, Tranulis MA, Ulvund M, et al. Distribution of prion protein in the ileal Peyer's patch of scrapie- free lambs and lambs naturally and experimentally exposed to the scrapie agent. J Gen Virol. 2000; 81 Pt 9: 2327-2337. PMID: 10950992
5. 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: 2757-2764. PMID: 10573172
6. McBride PA, Schulz-Schaeffer WJ, Donaldson M, Bruce ME, Diringer H, Kretzschmar HA, et al. 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; 75: 9320-9327. PMID: 11533195
7. Heggebo R, Press CM, Gunnes G, Ulvund MJ, Tranulis MA, Lsverk T. Detection of PrPSc in lymphoid tissues of lambs experimentally exposed to the scrapie agent. J Comp Pathol. 2003; 128: 172-181. PMID: 12634095
8. Aguzzi A, Heikenwalder M. Prions, cytokines, and chemokines: a meeting in lymphoid organs. Immunity. 2005; 22: 145-154. PMID: 15723804
9. Mabbott NA, MacPherson GG. Prions and their lethal journey to the brain. Nat Rev Microbiol. 2006; 4: 201-211. PMID: 16462753
10. Siso S, Gonzalez L, Jeffrey M. Neuroinvasion in prion diseases: the roles of ascending neural infection and blood dissemination. Interdiscip Perspect Infect Dis. 2010; 2010: 747892. doi: 10.1155/2010/747892 PMID: 20652006
11. Bartz JC, Dejoia C, Tucker T, Kincaid AE, Bessen RA. Extraneural prion neuroinvasion without lymphoreticular system infection. J Virol. 2005; 79: 11858-11863. PMID: 16140762
12. Bessen RA, Martinka S, Kelly J, Gonzalez D. Role of the lymphoreticular system in prion neuroinvasion from the oral and nasal mucosa. J Virol. 2009; 83: 6435-6445. doi: 10.1128/JVI.00018-09 PMID: 19369351
13. Haybaeck J, Heikenwalder M, Klevenz B, Schwarz P, Margalith I, Bridel C, et al. Aerosols transmit prions to immunocompetent and immunodeficient mice. PLoS Pathog. 2011; 7: e1001257. doi: 10.1371/journal.ppat.1001257 PMID: 21249178
14. Bartz JC, Kincaid AE, Bessen RA. Rapid prion neuroinvasion following tongue infection. J Virol. 2003; 77: 583-591. PMID: 12477862
15. Denkers ND, Telling GC, Hoover EA. Minor oral lesions facilitate transmission of chronic wasting disease. J Virol. 2011; 85: 1396-1399. doi: 10.1128/JVI.01655-10 PMID: 21084472
16. Bahrami F, van Hezik C, Bergman A, Brandt I. Target cells for methylsulphonyl-2,6-dichlorobenzene in the olfactory mucosa in mice. Chem Biol Interact. 2000; 128: 97-113. PMID: 11024450
17. Wagner JG, Hotchkiss JA, Harkema JR. Enhancement of nasal inflammatory and epithelial responses after ozone and allergen coexposure in Brown Norway rats. Toxicol Sci. 2002; 67: 284-294. PMID: 12011488
18. Mori I, Goshima F, Imai Y, Kohsaka S, Sugiyama T, Yoshida T, et al. Olfactory receptor neurons prevent dissemination of neurovirulent influenza A virus into the brain by undergoing virus-induced apoptosis. J Gen Virol. 2002; 83: 2109-2116. PMID: 12185263
19. Ge Y, Tsukatani T, Nishimura T, Furukawa M, Miwa T. Cell death of olfactory receptor neurons in a rat with nasosinusitis infected artificially with Staphylococcus. Chem Senses. 2002; 27: 521-527. PMID: 12142328
20. Franzen A, Carlsson C, Brandt I, Brittebo EB. Isomer-specific bioactivation and toxicity of dichlorophenyl methylsulphone in rat olfactory mucosa. Toxicol Pathol. 2003; 31: 364-372. PMID: 12851101
21. Islam Z, Harkema JR, Pestka JJ. Satratoxin G from the black mold Stachybotrys chartarum evokes olfactory sensory neuron loss and inflammation in the murine nose and brain. Environ Health Perspect. 2006; 114: 1099-1107. PMID: 16835065
22. Yagi S, Tsukatani T, Yata T, Tsukioka F, Miwa T, Furukawa M. Lipopolysaccharide-induced apoptosis of olfactory receptor neurons in rats. Acta Otolaryngol. 2007; 127: 748-753. PMID: 17573571
23. Epstein VA, Bryce PJ, Conley DB, Kern RC, Robinson AM. Intranasal Aspergillus fumigatus exposure induces eosinophilic inflammation and olfactory sensory neuron cell death in mice. Otolaryngol Head Neck Surg. 2008; 138: 334-339. doi: 10.1016/j.otohns.2007.11.029 PMID: 18312881
24. Corps KN, Islam Z, Pestka JJ, Harkema JR. Neurotoxic, inflammatory, and mucosecretory responses in the nasal airways of mice repeatedly exposed to the macrocyclic trichothecene mycotoxin roridin A: dose-response and persistence of injury. Toxicol Pathol. 2010; 38: 429-451. doi: 10.1177/0192623310364026 PMID: 20430879
25. Farbman AI. Olfactory neurogenesis: genetic or environmental controls? Trends Neurosci. 1990; 13: 362-365. PMID: 1699323
26. Blanco-Hernandez E, Valle-Leija P, Zomosa-Signoret V, Drucker-Colin R, Vidaltamayo R. Odor memory stability after reinnervation of the olfactory bulb. PLoS One. 2012; 7: e46338. doi: 10.1371/journal.pone.0046338 PMID: 23071557
27. Race RE, Priola SA, Bessen RA, Ernst D, Dockter J, Rall GF, et al. Neuron-specific expression of a hamster prion protein minigene in transgenic mice induces susceptibility to hamster scrapie agent. Neuron. 1995; 15: 1183-1191. PMID: 7576660
28. Race R, Oldstone M, Chesebro B. 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; 74: 828-833. PMID: 10623745
29. Marsh RF, Bessen RA. Physicochemical and biological characterizations of distinct strains of the transmissible mink encephalopathy agent. Philos Trans R Soc Lond B Biol Sci. 1994; 343: 413-414. PMID: 7913759
30. Shearin H, Bessen RA. Axonal and transynaptic spread of prions. J Virol. 2014; 88: 8640-8655. doi: 10.1128/JVI.00378-14 PMID: 24850738
31. Bessen RA, Wilham JM, Lowe D, Watschke CP, Shearin H, Martinka S, et al. Accelerated shedding of prions following damage to the olfactory epithelium. J Virol. 2012; 86: 1777-1788. doi: 10.1128/JVI.06626-11 PMID: 22130543
32. Bessen RA, Shearin H, Martinka S, Boharski R, Lowe D, Wilham JM, et al. Prion shedding from olfactory neurons into nasal secretions. PLoS Pathog. 2010; 6: e1000837. doi: 10.1371/journal.ppat.1000837 PMID: 20419120
33. Kascsak RJ, Rubenstein R, Merz PA, Tonna-DeMasi M, Fersko R, Carp RI, et al. Mouse polyclonal and monoclonal antibody to scrapie-associated fibril proteins. J Virol. 1987; 61: 3688-3693. PMID: 2446004
34. Shiroozu A, Okamura K, Ikenoue H, Sato K, Nakashima T, Yoshinari M, et al. Treatment of hyperthyroidism with a small single daily dose of methimazole. J Clin Endocrinol Metab. 1986; 63: 125-128. PMID: 3011835
35. Nakamura H, Noh JY, Itoh K, Fukata S, Miyauchi A, Hamada N. Comparison of methimazole and propylthiouracil in patients with hyperthyroidism caused by Graves' disease. J Clin Endocrinol Metab. 2007; 92: 2157-2162. PMID: 17389704
36. Brittebo EB. Metabolism-dependent toxicity of methimazole in the olfactory nasal mucosa. Pharmacol Toxicol. 1995; 76: 76-79. PMID: 7753763
37. Genter MB, Deamer NJ, Blake BL, Wesley DS, Levi PE. Olfactory toxicity of methimazole: dose-response and structure-activity studies and characterization of flavin-containing monooxygenase activity in the Long-Evans rat olfactory mucosa. Toxicol Pathol. 1995; 23: 477-486. PMID: 7501959
38. Bergman U, Brittebo EB. Methimazole toxicity in rodents: covalent binding in the olfactory mucosa and detection of glial fibrillary acidic protein in the olfactory bulb. Toxicol Appl Pharmacol. 1999; 155: 190-200. PMID: 10053173
39. Sakamoto T, Kondo K, Kashio A, Suzukawa K, Yamasoba T. Methimazole-induced cell death in rat olfactory receptor neurons occurs via apoptosis triggered through mitochondrial cytochrome c-mediated caspase-3 activation pathway. J Neurosci Res. 2007; 85: 548-557. PMID: 17171702
40. Bessen RA, Marsh RF. Identification of two biologically distinct strains of transmissible mink encephalopathy in hamsters. J Gen Virol. 1992; 73 (Pt 2): 329-334.
41. Sbriccoli M, Cardone F, Valanzano A, Lu M, Graziano S, De Pascalis A, et al. Neuroinvasion of the 263K scrapie strain after intranasal administration occurs through olfactory-unrelated pathways. Acta Neuropathol. 2009; 117: 175-184. doi: 10.1007/s00401-008-0474-z PMID: 19107494
42. Hadlow WJ, Eklund CM, Kennedy RC, Jackson TA, Whitford HW, Boyle CC. Course of experimental scrapie virus infection in the goat. J Infect Dis. 1974; 129: 559-567. PMID: 4207308
43. Hadlow WJ, Kennedy RC, Race RE. Natural infection of Suffolk sheep with scrapie virus. J Infect Dis. 1982; 146: 657-664. PMID: 6813384
44. Zanusso G, Ferrari S, Cardone F, Zampieri P, Gelati M, Fiorini M, et al. Detection of pathologic prion protein in the olfactory epithelium in sporadic Creutzfeldt-Jakob disease. N Engl J Med. 2003; 348: 711-719. PMID: 12594315
45. DeJoia C, Moreaux B, O'Connell K, Bessen RA. Prion infection of oral and nasal mucosa. J Virol. 2006; 80: 4546-4556. PMID: 16611915
46. Corona C, Porcario C, Martucci F, Iulini B, Manea B, Gallo M, et al. Olfactory system involvement in natural scrapie disease. J Virol. 2009; 83: 3657-3667. doi: 10.1128/JVI.01966-08 PMID: 19158242
47. Wilham JM, Orru CD, Bessen RA, Atarashi R, Sano K, Race B, et al. Rapid end-point quantitation of prion seeding activity with sensitivity comparable to bioassays. PLoS Pathog. 2010; 6: e1001217. doi: 10.1371/journal.ppat.1001217 PMID: 21152012
48. Orru CD, Bongianni M, Tonoli G, Ferrari S, Hughson AG, Groveman BR, et al. A test for Creutzfeldt-Jakob disease using nasal brushings. N Engl J Med. 2014; 371: 519-529. doi: 10.1056/NEJMoa1315200 PMID: 25099576
49. 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. PMID: 17030882
50. Hamir AN, Richt JA, Miller JM, Kunkle RA, Hall SM, Nicholson EM, et al. Experimental transmission of chronic wasting disease (CWD) of elk (Cervus elaphus nelsoni), white-tailed deer (Odocoileus virginianus), and mule deer (Odocoileus hemionus hemionus) to white-tailed deer by intracerebral route. Vet Pathol. 2008; 45: 297-306. doi: 10.1354/vp.45-3-297 PMID: 18487485
51. Mathiason CK, Hays SA, Powers J, Hayes-Klug J, Langenberg J, Dahmes SJ, et al. Infectious prions in pre-clinical deer and transmission of chronic wasting disease solely by environmental exposure. PLoS One. 2009; 4: e5916. doi: 10.1371/journal.pone.0005916 PMID: 19529769
52. Denkers ND, Hayes-Klug J, Anderson KR, Seelig DM, Haley NJ, Dahmes SJ, et al. Aerosol transmission of chronic wasting disease in white-tailed deer. J Virol. 2013; 87: 1890-1892. doi: 10.1128/JVI.02852-12 PMID: 23175370
53. Wells GA, Konold T, Arnold ME, Austin AR, Hawkins SA, Stack M, et al. Bovine spongiform encephalopathy: the effect of oral exposure dose on attack rate and incubation period in cattle. J Gen Virol. 2007; 88: 1363-1373. PMID: 17374783
54. Fryer HR, McLean AR. There is no safe dose of prions. PLoS One. 2011; 6: e23664. doi: 10.1371/journal.pone.0023664 PMID: 21858197
55. Foster JD, Parnham D, Chong A, Goldmann W, Hunter N. Clinical signs, histopathology and genetics of experimental transmission of BSE and natural scrapie to sheep and goats. Vet Rec. 2001; 148: 165-171. PMID: 11258721
56. Hamir AN, Kunkle RA, Richt JA, Miller JM, Cutlip RC, Jenny AL. Experimental transmission of sheep scrapie by intracerebral and oral routes to genetically susceptible Suffolk sheep in the United States. J Vet Diagn Invest. 2005; 17: 3-9. PMID: 15690944
57. Hamir AN, Kunkle RA, Richt JA, Miller JM, Greenlee JJ. Experimental transmission of US scrapie agent by nasal, peritoneal, and conjunctival routes to genetically susceptible sheep. Vet Pathol. 2008; 45: 7-11. doi: 10.1354/vp.45-1-7 PMID: 18192568
58. Hamir AN, Kunkle RA, Bulgin MS, Rohwer RG, Gregori L, et al. Experimental transmission of scrapie agent to susceptible sheep by intralingual or intracerebral inoculation. Can J Vet Res. 2008; 72: 63-67. PMID: 18214164
59. Kimberlin RH, Walker CA. Pathogenesis of mouse scrapie: effect of route of inoculation on infectivity titres and dose-response curves. J Comp Pathol. 1978; 88: 39-47. PMID: 563870
60. Bartz JC, Aiken JM, Bessen RA. Delay in onset of prion disease for the HY strain of transmissible mink encephalopathy as a result of prior peripheral inoculation with the replication-deficient DY strain. J Gen Virol. 2004; 85: 265-273. PMID: 14718642
61. Bartz JC, Kincaid AE, Bessen RA. Retrograde transport of transmissible mink encephalopathy within descending motor tracts. J Virol. 2002; 76: 5759-5768. PMID: 11992004
62. Glatzel M, Heppner FL, Albers KM, Aguzzi A Sympathetic innervation of lymphoreticular organs is rate limiting for prion neuroinvasion. Neuron. 2001; 31: 25-34. PMID: 11498048
63. Prinz M, Heikenwalder M, Junt T, Schwarz P, Glatzel M, et al. Positioning of follicular dendritic cells within the spleen controls prion neuroinvasion. Nature. 2003; 425: 957-962. PMID: 14562059
64. Walter BA, Valera VA, Takahashi S, Ushiki T. The olfactory route for cerebrospinal fluid drainage into the peripheral lymphatic system. Neuropathol Appl Neurobiol. 2006; 32: 388-396. PMID: 16866984
65. Verhaagen J, Oestreicher AB, Grillo M, Khew-Goodall YS, Gispen WH, et al. Neuroplasticity in the olfactory system: differential effects of central and peripheral lesions of the primary olfactory pathway on the expression of B-50/GAP43 and the olfactory marker protein. J Neurosci Res. 1990; 26: 31-44. PMID: 2141653
66. Carr VM, Farbman AI. Ablation of the olfactory bulb up-regulates the rate of neurogenesis and induces precocious cell death in olfactory epithelium. Exp Neurol. 1992; 115: 55-59. PMID: 1728573
67. Cummings DM, Emge DK, Small SL, Margolis FL. Pattern of olfactory bulb innervation returns after recovery from reversible peripheral deafferentation. J Comp Neurol. 2000; 421: 362-373. PMID: 10813792
68. Schwob JE. Neural regeneration and the peripheral olfactory system. Anat Rec. 2002; 269: 33-49. PMID: 11891623
69. 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. PMID: 12123696
70. 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. doi: 10.1002/cne.21698 PMID: 18338400
71. Bessen RA, Robinson CJ, Seelig DM, Watschke CP, Lowe D, et al. Transmission of chronic wasting disease identifies a prion strain causing cachexia and heart infection in hamsters. PLoS One. 2011; 6: e28026 doi: 10.1371/journal.pone.0028026 PMID: 22174765