Olfactory system involvement in natural scrapie disease

Journal of Virology

Volumn 83, Issue 8, 2009, Pages 3657-3667

  Corona, Cristiano ^a   Porcario, Chiara ^a   Martucci, Francesca ^a   Iulini, Barbara ^a   Manea, Barbara ^a   Gallo, Marina ^a   Palmitessa, Claudia ^a   Maurella, Cristiana ^a   Mazza, Maria ^a   Pezzolato, Marzia ^a   Acutis, Pierluigi ^a   Casalone, Cristina ^a,b  

^a DIF   (France)

^b Liguria e Valle d'Aosta   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

PRION PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CEREBROSPINAL FLUID; CONTROLLED STUDY; DURA MATER; IMMUNOHISTOCHEMISTRY; LYMPHOID TISSUE; NERVE CELL; NERVE ROOT; NONHUMAN; NOSE; NOSE MUCOSA; OLFACTORY BULB; OLFACTORY CORTEX; OLFACTORY NERVE; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; PERINEURIUM; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SCRAPIE; SHEEP; VIRUS INFECTIVITY; ANIMAL; CHEMISTRY; PATHOLOGY; PERIPHERAL NERVE;

ANIMALIA; OVIS ARIES;

ANIMALS; NASAL MUCOSA; OLFACTORY BULB; OLFACTORY NERVE; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS; PERIPHERAL NERVES; PRPSC PROTEINS; SCRAPIE; SHEEP;

EID: 64049116825     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01966-08     Document Type: Article

References (65)

1. Atarashi, R., R. A. Moore, V. L. Sim, A. G. Hughson, D. W. Dorward, H. A. Onwubiko, S. A. Priola, and B. Caughey. 2007. Ultrasensitive detection of scrapie prion protein using seeded conversion of recombinant prion protein. Nat. Methods 4:645-650. (Pubitemid 47202476)
2. Banks, W. A., M. L. Niehoff, C. Adessi, and C. Soto. 2004. Passage of murine scrapie prion protein across the mouse vascular blood-brain barrier. Biochem. Biophys. Res. Commun. 318:125-130. (Pubitemid 38526254)
3. Bartz, J. C., A. E. Kincaid, and R. A. Bessen. 2003. Rapid prion neuroinvasion following tongue infection. J. Virol. 77:583-591. (Pubitemid 36004996)
4. Bonfanti, L., P. Peretto, S. De Marchis, and A. Fasolo. 1999. Carnosine-related dipeptides in the mammalian brain. Prog. Neurobiol. 59:333-353. (Pubitemid 29352340)
5. Boulton, M., M. Flessner, D. Armstrong, J. Hay, and M. Johnston. 1998. Determination of volumetric cerebrospinal fluid absorption into extracranial lymphatics in sheep. Am. J. Physiol. 274:R88-R96. (Pubitemid 28092618)
6. Brown, P., and D. C. Gajdusek. 1991. Survival of scrapie virus after 3 years' internment. Lancet 337:269-270.
7. Casalone, C., G. Zanusso, P. Acutis, S. Ferrari, L. Capucci, F. Tagliavini, S. Monaco, and M. Caramelli. 2004. Identification of a second bovine amyloidotic spongiform encephalopathy: molecular similarities with sporadic Creutzfeldt-Jacob disease. Proc. Natl. Acad. Sci. USA 101:3065-3070.
8. Corona, C., F. Martucci, B. Iulini, M. Mazza, P. L. Acutis, C. Porcario, M. Pezzolato, B. Manea, A. Maroni, S. Barocci, E. Bozzetta, M. Caramelli, and C. Casalone. 2006. Could Oestrus ovis act as vector for scrapie?, abstr. PA-10, p. 239. Abstr. Prion 2006: strategies, advances and trends towards protection of society, Turin, Italy.
9. Cowan, C. M., and A. J. Roskams. 2002. Apoptosis in the mature and developing olfactory neuroepithelium. Microsc. Res. Tech. 58:204-215.
10. DeJoia, C., B. Moreaux, K. O' Connell, and R. A. Bessen. 2006. Prion infection of oral and nasal mucosa. J. Virol. 80:4546-4556.
11. Doty, R. L. 2008. The olfactory vector hypothesis of neurodegenerative disease: is it viable? Ann. Neurol. 63:7-15.
12. Doucette, R. 1991. PNS-CNS transitional zone of the first cranial nerve. J. Comp. Neurol. 312:451-466.
13. Erlich, S. S., J. G. McComb, S. Hyman, and M. H. Weiss. 1986. Ultrastructural morphology of the olfactory pathway for cerebrospinal fluid drainage in the rabbit. J. Neurosurg. 64:466-473. (Pubitemid 16035070)
14. Fournier, J. G., K. Adjou, V. Grigoriev, and J. P. Deslys. 2008. Ultrastructural evidence that ependymal cells are infected in experimental scrapie. Acta Neuropathol. 115:643-650.
15. Frank, E. H., B. W. Burge, B. H. Liwnicz, L. J. Lotspeich, J. C. White, S. L. Wechsler, F. H. Mayfield, and J. T. Keller. 1983. Cytokeratin provides a specific marker for human arachnoid cells grown in vitro. Exp. Cell Res. 146:371-376.
16. Franke, W. W., D. Mayer, E. Schmid, H. Denk, and E. Borenfreund. 1981. Differences of expression of cytoskeletal proteins in cultured rat hepatocytes and hepatoma cells. Exp. Cell Res. 134:345-365. (Pubitemid 12243910)
17. Gil, D. R., and G. D. Ratto. 1973. Contribution to the study of the origin of leptomeninges in the human embryo. Acta Anat. 85:620-623.
18. Hamir, A. N., R. A. Kunkle, J. A. Richt, J. M. Miller, and J. J. Greenlee. 2008. Experimental transmission of US scrapie agent by nasal, peritoneal, and conjunctival routes to genetically susceptible sheep. Vet. Pathol. 45:7-11.
19. Harmeyer, S., E. Pfaff, and M. H. Groschup. 1998. Synthetic peptide vaccines yield monoclonal antibodies to cellular and pathological prion proteins of ruminants. J. Gen. Virol. 79:937-945. (Pubitemid 28163402)
20. Harvey, S. C., and H. S. Burr. 1926. The development of the meninges. Arch. Neurol. Psychiat. 15:545-567.
21. Haybaeck, J., M. Heikenwalder, I. Margalith, N. Zeller, C. Bridel, P. Schwarz, K. Merz, L. Stitz, and A. Aguzzi. 2007. Intranasal and aereosolic prion transmission, abstr. P03.103, p. 72. Abstr. Prion 2007, Edinburgh, Scotland, United Kingdom.
22. Heikenwalder, M., N. Zeller, H. Seeger, M. Prinz, P. C. Klohn, P. Schwarz, N. H. Ruddle, C. Weissman, and A. Aguzzi. 2005. Chronic lymphocytic inflammation specifies the organ tropism of prions. Science 307:1107-1110.
23. Jackson, R. T., J. Tigges, and W. Arnold. 1979. Subarachnoid space of the CNS, nasal mucosa, and lymphatic system. Arch. Otolaryngol. 105:180-184.
24. Jeffrey, M., S. Martin, L. González, S. J. Ryder, S. J. Bellworthy, and R. Jackman. 2001. Differential diagnosis of infections with the bovine spongiform encephalopathy (BSE) and scrapie agents in sheep. J. Comp. Pathol. 125:271-284. (Pubitemid 34023740)
25. Johnson, C. J., K. E. Phillips, P. T. Schramm, D. McKenzie, J. M. Aiken, and J. A. Pedersen. 2006. Prions adhere to soil minerals and remain infectious. PloS Pathog. 2:296-302.
26. Johnson, R. T. 2005. Prion diseases. Lancet Neurol. 4:635-642. (Pubitemid 41317298)
27. Johnston, M., A. Zakharov, C. Papaiconomou, G. Salmasi, and D. Armstrong. 2004. Evidence of connections between cerebrospinal fluid and nasal lymphatic vessels in humans, non-human primates and other mammalian species. Cerebrospinal Fluid Res. 1:2.
28. Kincaid, A. E., and J. C. Bartz. 2007. The nasal cavity is a route for prion infection in hamsters. J. Virol. 81:4482-4491. (Pubitemid 46668646)
29. Klika, E. 1968. Ultrastructure of the meninges during human ontogeny. Z. Mikrosk. Anat. Forsch. 79:209-222.
30. Kolb, A. 1979. Lichtmikroskopische Untersuchungen an der Riechschleimhaut des Hausschafes (Ovis aries L.). Anat. Anz. 146:444-455.
31. Konold, T., S. J. Moore, S. J. Bellworthy, and H. A. Simmons. 2008. Evidence of scrapie transmission via milk. BMC Vet. Res. 4:14.
32. Lazarides, E. 1980. Intermediate filaments as mechanical integrators of cellular space. Nature 283:249-256.
33. Marsh, R. F., and R. H. Kimberlin. 1975. Comparison of scrapie and transmissible mink encephalopathy in hamsters. II. Clinical signs, pathology and pathogenesis. J. Infect. Dis. 131:104-110.
34. Mathiason, C. K., J. G. Powers, S. J. Dahmes, D. A. Osborn, K. V. Miller, R. J. Warren, G. L. Mason, S. A. Hays, J. Hayes-Klug, D. M. Seelig, M. A. Wild, L. L. Wolfe, T. R. Spraker, M. W. Miller, C. J. Sigurdson, G. C. Telling, and E. A. Hoover. 2006. Infectious prions in the saliva and blood of deer with chronic wasting disease. Science 314:133-136.
35. Miller, M. W., and E. S. Williams. 2003. Prion disease: horizontal prion transmission in mule deer. Nature 425:35-36.
36. Mori, I., Y. Nishiyama, T. Yokochi, and Y. Rimura. 2005. Olfactory transmission of neurotropic viruses. J. Neurovirol. 11:129-137. (Pubitemid 40852420)
37. Nicholson, C., and E. Syková. 1998. Extracellular space structure revealed by diffusion analysis. Trends Neurosci. 21:207-215. (Pubitemid 28191815)
38. Pease, D. C., and R. L. Schultz. 1958. Electron microscopy of rat cranial meninges. Am. J. Anat. 102:301-321.
39. Picard-Hagen, N., V. Gayrard, C. Viguie, M. Moudjou, C. Imbs, and P. L. Toutain. 2006. Prion protein in the cerebrospinal fluid of healthy and naturally scrapie-affected sheep. J. Gen. Virol. 87:3723-3727.
40. Prusiner, S. B. 1982. Novel proteinaceus infectious particles cause scrapie. Science 216:136-144.
41. Prusiner, S. B. 1998. The prion diseases. Brain Pathol. 8:499-513. (Pubitemid 28308848)
42. Race, R., A. Jenny, and D. Sutton. 1998. Scrapie infectivity and proteinase K-resistant prion protein in sheep placenta, brain, spleen and lymph node: implications for transmission and antemortem diagnosis. J. Infect. Dis. 178:949-953.
43. Ritchie, D. L., M. W. Head, and J. W. Ironside. 2004. Advances in the detection of prion protein in peripheral tissues of variant Creutzfeldt-Jakob disease patients using paraffin-embedded tissue blotting. Neuropathol. Appl. Neurobiol. 30:360-368. (Pubitemid 39120297)
44. Salès, N., K. Rodolfo, R. Hässig, B. Faucheux, L. Di Giamberardino, and K. L. Moya. 1998. Cellular prion protein localization in rodent and primate brain. Eur. J. Neurosci. 10:2464-2471. (Pubitemid 28302347)
45. Salman, M. D. 2003. Chronic wasting disease in deer and elk: scientific facts and findings. J. Vet. Med. Sci. 65:761-768.
46. Sawcer, S. J., G. M. Yuill, T. F. G. Esmonde, P. Estibeiro, J. W. Ironside, J. E. Bell, and R. G. Will. 1993. Creutzfeldt-Jacob disease in an individual occupationally exposed to BSE. Lancet 341:642.
47. Schaefer, M. L., B. Böttger, W. L. Silver, and T. E. Finger. 2002. Trigeminal collaterals in the nasal epithelium and olfactory bulb: a potential route for direct modulation of olfactory information by trigeminal stimuli. J. Comp. Neurol. 444:221-226.
48. Seeger, H., M. Heikenwalder, N. Zeller, J. Kranich, P. Schwarz, A. Gaspert, B. Seifert, G. Miele, and A. Aguzzi. 2005. Coincident scrapie infection and nephritis lead to urinary prion excretion. Science 310:324-326.
49. Shaw, I. C. 1995. BSE and farmworkers. Lancet 346:1365.
50. Sisó, S., M. Jeffrey, H. Baird, S. Martin, S. Bellworthy, F. Chianini, and L. Gonzalez. 2006. The topographical distribution of prion protein in the brains of sheep challenges the current hypothesis of neuroinvasion, abstr. PA-52, p. 281. Abstr. Prion 2006: Strategies, advances and trends towards protection of society, Turin, Italy.
51. Smith, P. E. M., M. Zeidler, J. W. Ironside, P. Estibeiro, and T. H. Moss. 1995. Creutzfeldt-Jacob disease in a dairy farmer. Lancet 346:898.
52. Spraker, T. R., K. I. O' Rourke, A. Balachandran, R. R. Zink, B. A. Cummings, M. W. Miller, and B. E. Powers. 2002. Validation of monoclonal antibody F99/97.6.1 for immunohistochemical staining of brain and tonsil in mule deer (Odocoileus hemionus) with chronic wasting disease. J. Vet. Diagn. Investig. 14:3-7.
53. Spraker, T. R., R. R. Zink, B. A. Cummings, M. A. Wild, M. W. Miller, and K. I. O' Rourke. 2002. 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. 39:110-119.
54. Stanley, A. C., J. F. Huntley, M. Jeffrey, and D. Buxton. 2001. Characterization of ovine nasal-associated lymphoid tissue and identification of M cells in the overlying follicle-associated epithelium. J. Comp. Pathol. 125:262-270. (Pubitemid 34023739)
55. Tabaton, M., S. Monaco, M. P. Cordone, M. Colucci, G. Giaccone, F. Tagliavini, and G. Zanusso. 2004. Prion deposition in olfactory biopsy of sporadic Creutzfeldt-Jacob disease. Ann. Neurol. 55:294-296. (Pubitemid 38167009)
56. Treloar, H. B., J. C. Bartolomei, B. W. Lipscomb, and C. A. Greer. 2001. Mechanisms of axonal plasticity: lessons from the olfactory pathway. Neuroscientist 7:55-63.
57. sc in salivary glands of scrapie-affected sheep. J. Virol. 81:4872-4876.
58. Vella, L. J., D. L. V. Greenwood, R. Cappai, J. P. Y. Scheerlinck, and A. F. Hill. 2008. Enrichment of prion protein in exosomes derived from ovine cerebral spinal fluid. Vet. Immunol. Immunopathol. 124:385-393.
59. Vidal, E., M. Ordonez, J. M. Vela, and M. Pumarola. 2003. Study of the olfactory pathway and related structures of 19 BSE naturally affected cows, abstr. PG-26, p. 203. Abstr. Prion 2003: prion diseases: from basic research to intervention concepts, Gasteig, Munich, Germany.
60. Walter, B. A., V. A. Valera, S. Takahashi, and T. Ushiki. 2006. The olfactory route for cerebrospinal fluid drainage into the peripheral lymphatic system. Neuropathol. Appl. Neurobiol. 32:388-396. (Pubitemid 44015580)
61. Weller, R. O. 1998. Pathology of cerebrospinal fluid and interstitial fluid of the CNS: significance for Alzheimer disease, prion disorders and multiple sclerosis. J. Neuropathol. Exp. Neurol. 57:885-894.
62. Zakharov, A., C. Papaiconomou, J. Djenic, R. Midha, and M. Johnston. 2003. Lymphatic cerebrospinal fluid absorption pathways in neonatal sheep revealed by subarachnoid injection of Microfil. Neuropathol. Appl. Neurobiol. 29:563-573. (Pubitemid 37548351)
63. Zanusso, G., S. Ferrari, F. Cardone, P. Zampieri, M. Gelati, M. Fiorini, Farinazzo, A., M. Gardiman, T. Cavallaro, M. Bentivoglio, P. G. Rigetti, M. Pocchiari, N. Rizzato, and S. Monaco. 2003. Detection of pathologic prion protein in the olfactory epithelium in sporadic Creutzfeldt-Jacob disease. N. Engl. J. Med. 348:711-719. (Pubitemid 36237040)
64. Zhang, E. T., C. B. E. Inman, and R. O. Weller. 1990. Interrelationships of the pia mater and the perivascular (Virchow-Robin) spaces in the human cerebrum. J. Anat. 170:111-123. (Pubitemid 20209323)
65. Zhang, E. T., H. K. Richards, S. Kida, and R. O. Weller. 1992. Directional and compartimentalised drainage of interstitial fluid and cerebrospinal fluid from the rat brain. Acta Neuropathol. 83:233-239.