Transolfactory neuroinvasion by viruses threatens the human brain

Acta Virologica

Volumn 59, Issue 4, 2015, Pages 338-349

  Mori, I ^a  

^a SHUBUN UNIVERSITY   (Japan)

Author keywords

Encephalitis; Human brain; Neurodegenerative disorders; Olfactory neuron; Virus

Indexed keywords

BRAIN; CELL INVASION; CENTRAL NERVOUS SYSTEM; HERPES SIMPLEX ENCEPHALITIS; HERPES SIMPLEX VIRUS; HIGHLY PATHOGENIC AVIAN INFLUENZA; HUMAN; INFLUENZA A VIRUS; INNATE IMMUNITY; NERVE CELL NETWORK; NONHUMAN; OLFACTORY NERVE; OLFACTORY SYSTEM; SHORT SURVEY; VIRUS ENCEPHALITIS; VIRUS LATENCY; VIRUS TRANSMISSION; VIRUS VIRULENCE; ANIMAL; IMMUNOLOGY; OLFACTORY EPITHELIUM; VIRAL PHENOMENA AND FUNCTIONS; VIROLOGY; VIRUS INFECTION;

ANIMALS; BRAIN; HUMANS; OLFACTORY MUCOSA; VIRUS DISEASES; VIRUS PHYSIOLOGICAL PHENOMENA;

EID: 84975495359     PISSN: 0001723X     EISSN: None     Source Type: Journal    
DOI: 10.4149/av_2015_04_338     Document Type: Short Survey

References (110)

1. Baringer JR, Pisani P (1994): Herpes simplex virus genomes in human nervous system tissue analyzed by polymerase chain reaction. Ann. Neurol. 36, 823-829. http://dx.doi.org/10.1002/ana.410360605
2. Armien AG, Hu S, Little MR, Robinson N, Lokensgard JR, Low WC, Cheeran MC (2010): Chronic cortical and subcortical pathology with associated neurological deficits ensuing experimental herpes encephalitis. Brain Pathol. 20, 738-750. http://dx.doi.org/10.1111/j.1750-3639.2009.00354.x
3. Aronsson F, Robertson B, Ljunggren HG, Kristensson K (2003): Invasion and persistance of the neuroadapted influenza virus A/WSN/33 in the mouse olfactory system. Viral Immunol. 16, 415-423. http://dx.doi.org/10.1089/088282403322396208
4. Becker Y (1995): HSV-1 brain infection by the olfactory nerve route and virus latency and reactivation may cause learning and behavioral deficiencies and violence in children and adults: A point of view. Virus Genes 10, 217-226. http://dx.doi.org/10.1007/BF01701811
5. Beers DR, Henkel JS, Schaefer DC, Rose JW, Stroop WG (1993): Neuropathology of herpes simplex virus encephalitis in a rat seizure model. J. Neuropathol. Exp. Neurol. 52, 241-252. http://dx.doi.org/10.1097/00005072-199305000-00008
6. Beers DR, Henkel JS, Kesner RP, Stroop WG (1995): Spatial recognition memory deficits without notable CNS pathology in rats following herpes simplex encephalitis. J. Neurol. Sci. 131, 119-127. http://dx.doi.org/10.1016/0022-510-X(95)00099-N
7. Bennett RS, Cress CM, Ward JM, Firestone CY, Murphy BR, Whitehead SS (2008): La Crosse virus infectivity, pathogenesis, and immunogenicity in mice and monkeys. Virol. J. 5, 25. http://dx.doi.org/10.1186/1743-422X-5-25
8. Berri F, Haffar G, Le VB, Sadewasser A, Paki K, Lina B, Wolff T, Riteau B (2014): Annexin V incorporated into influenza virus particles inhibits gamma interferon signaling and promotes viral replication. J. Virol. 88, 11215-11228. http://dx.doi.org/10.1128/JVI.01405-14
9. Bodewes R, Kreijtz JH, van Amerongen G, Fouchier RA, Osterhaus AD, Rimmelzwaan GF, Kuiken T (2011): Pathogenesis of influenza A/H5N1 virus infection in ferrets differs between intranasal and intratracheal routes of inoculation. Am. J. Pathol. 179, 30-36. http://dx.doi.org/10.1016/j.ajpath.2011.03.026
10. Boggian I, Buzzacaro E, Calistri A, Calvi P, Cavaggioni A, Mucignat-Caretta C, Palu G (2000): Asymptomatic herpes simplex type 1 virus infection of the mouse brain. J. Neurovirol. 6, 303-313. http://dx.doi.org/10.3109/13550280009030756
11. Boivin N, Sergerie Y, Rivest S, Boivin G (2008): Effect of pretreatment with Toll-like receptor agonists in a mouse model of herpes simplex virus type 1 encephalitis. J. Infect. Dis. 198, 664-672. http://dx.doi.org/10.1086/590671
12. Carbone KM, Duchala CS, Griffin JW, Kincaid AL, Narayan O (1987): Pathogenesis of Borna disease in rats: Evidence that intra-axonal spread is the major route for virus dissemination and the determinant for disease incubation. J. Virol. 61, 3431-3440.
13. Carty M, Reinert L, Paludan SR, Bowie AG (2014): Innate antiviral signalling in the central nervous system. Trends Immunol. 35, 79-87. http://dx.doi.org/10.1016/j.it.2013.10.012
14. Charles PC, Walters E, Margolis F, Johnston RE (1995): Mechanism of neuroinvasion of Venezuelan equine encephalitis virus in the mouse. Virology 208, 662-671. http://dx.doi.org/10.1006/viro.1995.1197
15. Conomy JP, Leibovitz A, McCombs W, Stinson J (1977): Airborne rabies encephalitis: Demonstration of rabies virus in the human central nervous system. Neurology 27, 67-69. http://dx.doi.org/10.1212/WNL.27.1.67
16. Crotty S, Hix L, Sigal LJ, Andino R (2002): Poliovirus pathogenesis in a new poliovirus receptor transgenic mouse model: age-dependent paralysis and a mucosal route of infection. J. Gen. Virol. 83, 1707-1720. http://dx.doi.org/10.1099/0022-1317-83-7-1707
17. Danielyan L, Beer-Hammer S, Stolzing A, Schafer R, Siegel G, Fabian C, Kahle P, Biedermann T, Lourhmati A, Buadze M, Novakovic A, Proksch B, Gleiter CH, Frey WH, Schwab M (2014): Intranasal delivery of bone marrow-derived mesenchymal stem cells, macrophages, and microglia to the brain in mouse models of Alzheimer's and Parkinson's disease. Cell Transplant. 23 (Suppl. 1), 123-139. http://dx.doi.org/10.3727/096368914X684970
18. Davis KL, Korom M, Morrison LA (2014): Herpes simplex virus 2 ICP34.5 confers neurovirulence by regulating the type I interferon response. Virology 468-470, 330-339. http://dx.doi.org/10.1016/j.virol.2014.08.015
19. Davis LE and Johnson RT (1979): An explanation for the localization of herpes simplex encephalitis? Ann. Neurol. 5, 2-5. http://dx.doi.org/10.1002/ana.410050103
20. de Jong MD, Bach VC, Phan TQ, Vo MH, Tran TT, Nguyen BH, Beld M, Le TP, Truong HK, Nguyen VV, Tran TH, Do QH, Farrar J (2005):. Fatal avian influenza A (H5N1): in a child presenting with diarrhea followed by coma. N. Engl. J. Med. 352, 686-691. http://dx.doi.org/10.1056/nejmoa044307
21. DeLuca GC, Joseph A, George J, Yates RL, Hamard M, Hofer M, Esiri MM (2015): Olfactory pathology in central nervous system demyelinating diseases. Brain Pathol. 25, 543-551. http://dx.doi.org/10.1111/bpa.12209
22. Devireddy LR, Jones CJ (2000): Olf-1, a neuron-specific transcription factor, can activate the herpes simplex virus type 1-infected cell protein 0 promoter. J. Biol. Chem. 275, 77-81. http://dx.doi.org/10.1074/jbc.275.1.77
23. Dhuria SV, Hanson LR, Frey WH 2nd (2010): Intranasal delivery to the central nervous system: mechanisms and experimental considerations. J. Pharm. Sci. 99, 1654-1673.
24. Diefenbach RJ, Miranda-Saksena M, Douglas MW, Cunningham AL (2008): Transport and egress of herpes simplex virus in neurons. Rev. Med. Virol. 18, 35-51. http://dx.doi.org/10.1002/rmv.560
25. Dinn JJ (1980): Transolfactory spread of virus in herpes simplex encephalitis. Br. Med. J. 281, 1392. http://dx.doi.org/10.1136/bmj.281.6252.1392
26. Doorn KJ, Goudriaan A, Blits-Huizinga C, Bol JG, Rozemuller AJ, Hoogland PV, Lucassen PJ, Drukarch B, van de Berg WD, van Dam AM (2014): Increased amoeboid microglial density in the olfactory bulb of Parkinson's and Alzheimer's patients. Brain Pathol. 24, 152-165. http://dx.doi.org/10.1111/bpa.12088
27. Drummond CW, Eglin RP, Esiri MM (1994): Herpes simplex virus encephalitis in a mouse model: PCR evidence for CNS latency following acute infection. J. Neurol. Sci. 127, 159-163. http://dx.doi.org/10.1016/0022-510X(94)90068-X
28. Dups J, Middleton D, Yamada M, Monaghan P, Long F, Robinson R, Marsh GA, Wang LF (2012): A new model for Hendra virus encephalitis in the mouse. PLoS One 7, e40308. http://dx.doi.org/10.1371/journal.pone.0040308
29. Esiri MM (1982): Herpes simplex encephalitis. An immunohistological study of the distribution of viral antigen within the brain. J. Neurol. Sci. 54, 209-226. http://dx.doi.org/10.1016/0022-510X(82)90183-6
30. Faber HK, Silverberg RJ, Dong L (1944): Poliomyelitis in the cynomolgus monkey: III. Infection by inhalation of droplet nuclei and the nasopharyngeal portal of entry, with a note on this mode of infection in rhesus. J. Exp. Med. 80, 39-57. http://dx.doi.org/10.1084/jem.80.1.39
31. Fujimoto S, Kobayashi M, Uemura O, Iwasa M, Ando T, Katoh T, Nakamura C, Maki N, Togari H, Wada Y (1998): PCR on cerebrospinal fluid to show influenza-associated acute encephalopathy or encephalitis. Lancet 352, 873-875. http://dx.doi.org/10.1016/S0140-6736(98)12449-2
32. Gamboa ET, Wolf A, Yahr MD, Harter DH, Duffy PE, Barden H, Hsu KC (1974): Influenza virus antigen in postencephalitic parkinsonism brain. Arch. Neurol. 31, 228-232. http://dx.doi.org/10.1001/archneur.1974.00490400042003
33. Gizurarson S (2012): Anatomical and histological factors affecting intranasal drug and vaccine delivery. Curr. Drug Deliv. 9, 566-582. http://dx.doi.org/10.2174/156720112803529828
34. Haga S, Yoshimura M, Motoi Y, Arima K, Aizawa T, Ikuta K, Tashiro M, Ikeda K (1997): Detection of Borna disease virus genome in normal human brain tissue. Brain Res. 770, 307-309. http://dx.doi.org/10.1016/S0006-8993(97)00903-7
35. Harberts E, Yao K, Wohler JE, Maric D, Ohayon J, Henkin R, Jacobson S (2011): Human herpesvirus-6 entry into the central nervous system through the olfactory pathway. Proc. Natl. Acad. Sci. USA 108, 13734-13739. http://dx.doi.org/10.1073/pnas.1105143108
36. Hudson SJ, Dix RD, Streilein JW (1991): Induction of encephalitis in SJL mice by intranasal infection with herpes simplex virus type 1: A possible model of herpes simplex encephalitis in humans. J. Infect. Dis. 163, 720-727. http://dx.doi.org/10.1093/infdis/163.4.720
37. Ibarra-Soria X, Levitin MO, Logan DW (2014): The genomic basis of vomeronasal-mediated behaviour. Mamm. Genome 25, 75-86. http://dx.doi.org/10.1007/s00335-013-9463-1
38. Itzhaki RF (2014): Herpes simplex virus type 1 and Alzheimer's disease: increasing evidence for a major role of the virus. Front. Aging Neurosci. Volume, pages???
39. Johnson RT, Mims CA (1968): Pathogenesis of viral infections of the nervous system. N. Engl. J. Med. 278, 23-30.
40. Iwasaki T, Itamura S, Nishimura H, Sato Y, Tashiro M, Hashikawa T, Kurata T (2004): Productive infection in the murine central nervous system with avian influenza virus A (H5N1): after intranasal inoculation. Acta Neuropathol. 108, 485-492. http://dx.doi.org/10.1007/s00401-004-0909-0
41. Jang H, Boltz D, Sturm-Ramirez K, Shepherd KR, Jiao Y, Webster R, Smeyne RJ (2009): Highly pathogenic H5N1 influenza virus can enter the central nervous system and induce neuroinflammation and neurodegeneration. Proc. Natl. Acad. Sci. USA 106, 14063-14068. http://dx.doi.org/10.1073/pnas.0900096106
42. Kalinke U, Bechmann I, Detje CN (2011): Host strategies against virus entry via the olfactory system. Virulence 2, 367-370. http://dx.doi.org/10.4161/viru.2.4.16138
43. Kanazawa T, Akiyama F, Kakizaki S, Takashima Y, Seta Y (2013): Delivery of siRNA to the brain using a combination of nose-to-brain delivery and cell-penetrating peptidemodified nano-micelles. Biomaterials 34, 9220-9226. http://dx.doi.org/10.1016/j.biomaterials.2013.08.036
44. Kennedy PGE, Chaudhuri A (2002): Herpes simplex encephalitis. J. Neurol. Neurosurg. Psychiatry 73, 237-238. http://dx.doi.org/10.1136/jnnp.73.3.237
45. Korteweg C, Gu J (2008): Pathology, molecular biology, and pathogenesis of avian influenza A (H5N1): infection in humans. Am. J. Pathol. 172, 1155-1170. http://dx.doi.org/10.2353/ajpath.2008.070791
46. Koshizuka T, Kawaguchi Y, Nishiyama Y (2005): Herpes simplex virus type 2 membrane protein UL56 associates with the kinesin motor protein KIF1A. J. Gen. Virol. 86, 527-533. http://dx.doi.org/10.1099/vir.0.80633-0
47. Kristensson K (2006): Avian influenza and the brain-Comments on the occasion of resurrection of the Spanish fluvirus. Brain Res. Bull. 68, 406-413. http://dx.doi.org/10.1016/j.brainresbull.2005.11.022
48. Kristensson K (2011): Microbes' roadmap to neurons. Nat. Rev. Neurosci. 12, 345-357 http://dx.doi.org/10.1038/nrn3029
49. Kuno G (2001): Transmission of arboviruses without involvement of arthropod vectors. Acta Virol. 45, 139-150.
50. Lafay F, Coulon P, Astic L, Saucier D, Riche D, Holley A, Flamand A (1991): Spread of the CVS strain of rabies virus and of the avirulent mutant AvO1 along the olfactory pathways of the mouse aft er intranasal inoculation. Virology 183, 320-330. http://dx.doi.org/10.1016/0042-6822-(91)90145-2
51. Landis BN, Vodicka J, Hummel T (2010): Olfactory dysfunction following herpetic meningoencephalitis. J. Neurol. 257, 439-443. http://dx.doi.org/10.1007/s00415-009-5344-7
52. Lanfranca MP, Mostafa HH, Davido DJ (2014): HSV-1 ICP0: An E3 ubiquitin ligase that counteracts host intrinsic and innate immunity. Cells 3, 438-454. http://dx.doi.org/10.3390/cells3020438
53. Leyva-Grado VH, Churchill L, Wu M, Williams TJ, Taishi P, Majde JA, Krueger JM (2009): Influenza virus-and cytokineimmunoreactive cells in the murine olfactory and central autonomic nervous systems before and aft er illness onset. J. Neuroimmunol. 211, 73-83. http://dx.doi.org/10.1016/j.jneuroim.2009.03.016
54. Leyva-Grado VH, Churchill L, Harding J, Krueger JM (2010): The olfactory nerve has a role in the body temperature and brain cytokine responses to influenza virus. Brain Behav. Immun. 24, 281-288. http://dx.doi.org/10.1016/j.bbi.2009.10.007
55. Liedmann S, Hrincius ER, Guy C, Anhlan D, Dierkes R, Carter R, Wu G, Staeheli P, Green DR, Wolff T, McCullers JA, Ludwig S, Ehrhardt C (2014): Viral suppressors of the RIG-1-mediated interferon response are pre-packed in influenza virions. Nat. Commun. 5, 5645. http://dx.doi.org/10.1038/ncomms6645
56. Liedtke W, Opalka B, Zimmermann CW, Lignitz E (1993): Age distribution of latent herpes simplex virus 1 and varicella-zoster virus genome in human nervous system. J. Neurol. Sci. 116, 6-11. http://dx.doi.org/10.1016/0022-510X(93)90082-A
57. Livorsi D, Anderson E, Qureshi S, Howard M, Wang YF, Franco-Paredes C (2010): Brainstem encephalitis: an unusual presentation of herpes simplex virus infection. J. Neurol. 257, 1432-1437. http://dx.doi.org/10.1007/s00415-010-5600-x
58. Loseva E, Yuan TF, Karnup S (2009): Neurogliogenesis in the mature olfactory system: A possible protective role against infection and toxic dust. Brain Res. Rev. 59, 374-387. http://dx.doi.org/10.1016/j.brainresrev.2008.10.004
59. Majde JA (2010): Neuroinflammation resulting from covert brain invasion by common viruses-a potential role in local and global neurodegeneration. Med. Hypotheses 75, 204-213. http://dx.doi.org/10.1016/j.mehy.2010.02.023
60. McMinn PC, Dalgarno L, Weir RC (1996): A comparison of the spread of Murray Valley encephalitis viruses of high or low neuroinvasiveness in the tissues of Swiss mice aft er peripheral inoculation. Virology 220, 414-423. http://dx.doi.org/10.1006/viro.1996.0329
61. Monath TP, Cropp CB, Harrison AK (1983): Mode of entry of a neurotropic arbovirus into the central nervous system. Lab. Invest. 48, 399-410.
62. Morales JA, Herzog S, Kompter C, Frese K, Rott R (1988): Axonal transport of Borna disease virus along olfactory pathways in spontaneously and experimentally infected rats. Med. Microbiol. Immunol. 177, 51-68. http://dx.doi.org/10.1007/BF00189527
63. Mori I, Goshima F, Imai Y, Kohsaka S, Sugiyama T, Yoshida T, Yokochi T, Nishiyama Y, Kimura Y (2002): Olfactory receptor neurons prevent dissemination of neurovirulent influenza A virus into the brain by undergoing virusinduced apoptosis. J. Gen. Virol. 83, 2109-2116. http://dx.doi.org/10.1099/0022-1317-83-9-2109
64. Mori I, Nishiyama Y, Yokochi T, Kimura Y (2004): Virus-induced neuronal apoptosis as pathological and protective responses of the host. Rev. Med. Virol. 14, 209-216 http://dx.doi.org/10.1002/rmv.426
65. Mori I, Nishiyama Y, Yokochi T, Kimura Y (2005a): Olfactory transmission of neurotropic viruses. J. Neurovirol. 11, 129-137. http://dx.doi.org/10.1080/13550280590922793
66. Mori I, Goshima F, Ito H, Koide N, Yoshida T, Yokochi T, Kimura Y, Nishiyama Y (2005b): The vomeronasal chemosensory system as a route of neuroinvasion by herpes simplex virus. Virology 334, 51-58. http://dx.doi.org/10.1016/j.virol.2005.01.023
67. Mori I, Liu B, Goshima F, Ito H, Koide N, Yoshida T, Yokochi T, Kimura Y, Nishiyama Y (2005c): HF10, an attenuated herpes simplex virus (HSV): type 1 clone, lacks neuroinvasiveness and protects mice against lethal challenge with HSV types 1 and 2. Microb. Infect. 7, 1492-1500. http://dx.doi.org/10.1016/j.micinf.2005.05.007
68. Mori I, Nishiyama Y (2005): Herpes simplex virus and varicellazoster virus: why do these human alphaherpesviruses behave so differently from one another? Rev. Med. Virol. 15, 393-406. http://dx.doi.org/10.1002/rmv.478
69. Mori I, Goshima F, Watanabe D, Ito H, Koide N, Yoshida T, Liu B, Kimura Y, Yokochi T, Nishiyama Y (2006): Herpes simplex virus US3 protein kinase regulates virus-induced apoptosis in olfactory and vomeronasal chemosensory neurons in vivo. Microb. Infect. 8, 1806-1812. http://dx.doi.org/10.1016/j.micinf.2006.02.018
70. Mori I (2010): Herpes simplex virus type 1 persists in the aged brain through hypothetical expression of accessory genes. J. Neurovirol. 16, 203-207. http://dx.doi.org/10.3109/13550281003739040
71. Mori I (2012): Herpes simplex virus US3 protein kinase regulates host responses and determines neurovirulence. Microbiol. Immunol. 56, 351-355. http://dx.doi.org/10.1111/j.1348-0421.2012.00461.x
72. Munster VJ, Prescott JB, Bushmaker T, Long D, Rosenke R, Thomas T, Scott D, Fischer ER, Feldmann H, de Wit E (2012): Rapid Nipah virus entry into the central nervous system of hamsters via the olfactory route. Sci. Rep. 2, 736. http://dx.doi.org/10.1038/srep00736
73. Nir Y, Beemer A, Goldwasser RA (1965): West Nile virus infection in mice following exposure to a viral aerosol. Br. J. Exp. Pathol. 46, 443-449.
74. Oboti L, Peretto P, De Marchis S, Fasolo A (2011): From chemical neuroanatomy to an understanding of the olfactory system. Eur. J. Histochem. 55, e35. http://dx.doi.org/10.4081/ejh.2011.e35
75. Ojeda VJ, Archer M, Robertson TA, Bucens MR (1983): Necropsy study of the olfactory portal of entry in herpes simplex encephalitis. Med. J. Aust. 1, 79-81.
76. Park CH, Ishinaka M, Takada A, Kida H, Kimura T, Ochiai K, Umemura T (2002): The invasion routes of neurovirulent A/Hong Kong/483/97 (H5N1): influenza virus into the central nervous system aft er respiratory infection in mice. Arch. Virol. 147, 1425-1436. http://dx.doi.org/10.1007/s00705-001-0750-x
77. Peri P, Mattila RK, Kantola H, Broberg E, Karttunen HS, Waris M, Vuorinen T, Hukkanen V (2008): Herpes simplex virus type 1 Us3 gene deletion influences toll-like receptor responses in cultured monocytic cells. Virol. J. 5, 140. http://dx.doi.org/10.1186/1743-422X-5-140
78. Piroozmand A, Koyama AH, Shimada Y, Fujita M, Arakawa T, Adachi A (2004): Role of Us3 gene of herpes simplex virus type 1 for resistance to interferon. Int. J. Mol. Med. 14, 641-645. http://dx.doi.org/10.3892/ijmm.14.4.641
79. Plourde JR, Pyles JA, Layton RC, Vaughan SE, Tipper JL, Harrod KS (2012): Neurovirulence of H5N1 infection in ferrets is mediated by multifocal replication in distinct permissive neuronal cell regions. PLoS One 7, e46605. http://dx.doi.org/10.1371/journal.pone.0046605
80. Powers AM, Logue CH (2007): Changing patterns of chikungunya virus: re-emergence of a zoonotic arbovirus. J. Gen. Virol. 88, 2363-2377. http://dx.doi.org/10.1099/vir.0.82858-0
81. Rao P, Pham HT, Kulkarni A, Yang Y, Liu X, Knipe DM, Cresswell P, Yuan W (2011): Herpes simplex virus 1 glycoprotein B and US3 collaborate to inhibit CD1d antigen presentation and NKT cell function. J. Virol. 85, 8093-8104. http://dx.doi.org/10.1128/JVI.02689-10
82. Reinacher M, Bonin J, Narayan O, Scholtissek C (1983): Pathogenesis of neurovirulent influenza A virus infection in mice, Route of entry of virus into brain determines infection of different populations of cells. Lab. Invest. 49, 686-692.
83. Riegger D, Hai R, Dornfeld D, Manz B, Leyva-Grado V, Sanchez-Aparicio MT, Albrecht RA, Palese P, Haller O, Schwemmle M, Garcia-Sastre A, Kochs G, Schmolke M (2015): The nucleoprotein of newly emerged H7N9 influenza A virus harbors a unique motif conferring resistance to antiviral human MxA. J. Virol. 89, 2241-2252. http://dx.doi.org/10.1128/JVI.02406-14
84. Rodriguez S, Sickles HM, DeLeonardis C, Alcaraz A, Gridley T, Lin DM (2008): Notch2 is required for maintaining sustentacular cell function in the adult mouse main olfactory epithelium. Dev. Biol. 314, 40-58. http://dx.doi.org/10.1016/j.ydbio.2007.10.056
85. Sabin AB, Olitsky PK (1938): Fate of nasally instilled poliomyelitis virus in normal and convalescent monkeys with special reference to the problem of host to host transmission. J. Exp. Med. 68, 39-62. http://dx.doi.org/10.1084/jem.68.1.39
86. Sauder C, Staeheli P (2003): Rat model of Borna disease virus transmission: Epidemiological implications. J. Virol. 77, 12886-12890. http://dx.doi.org/10.1128/JVI.77.23.12886-12890.2003
87. Schrauwen EJ, Herfst S, Leijten LM, van Run P, Bestebroer TM, Linster M, Bodewes R, Kreijtz JH, Rimmelzwaan GF, Osterhaus AD, Fouchier RA, Kuiken T, van Riel D (2012): The multibasic cleavage site in H5N1 virus is critical for systemic spread along the olfactory and hematogenous routes in ferrets. J. Virol. 86, 3975-3984. http://dx.doi.org/10.1128/JVI.06828-11
88. Shen G, Wang K, Wang S, Cai M, Li ML, Zheng C (2014): Herpes simplex virus 1 counteracts viperin via its virion host shutoffprotein UL41. J. Virol. 88, 12163-12166. http://dx.doi.org/10.1128/JVI.01380-14
89. Shinya K, Makino A, Hatta M, Watanabe S, Kim JH, Hatta Y, Gao P, Ozawa M, Le QM, Kawaoka Y (2011): Subclinical brain injury caused by H5N1 influenza virus infection. J. Virol. 85, 5202-5207. http://dx.doi.org/10.1128/JVI.00239-11
90. Shivkumar M, Milho R, May JS, Nicoll MP, Efstathiou S, Stevenson PG (2013): Herpes simplex virus 1 targets the murine olfactory neuroepithelium for host entry. J. Virol. 87, 10477-10488. http://dx.doi.org/10.1128/JVI.01748-13
91. Simon M, Hernu R, Cour M, Casalegno JS, Lina B, Argaud L (2013): Fatal influenza A (H1N1): pdm09 encephalopathy in immunocompetent man. Emerg. Infect. Dis. 19, 1005-1007. http://dx.doi.org/10.3201/eid1906.130062
92. Smithson LJ, Kawaja MD (2010): Microglial/macrophage cells in mammalian olfactory nerve fascicles. J. Neurosci. Res. 88, 858-865.
93. Suh HS, Brosnan CF, Lee SC (2009): Toll-like receptors in CNS viral infections. Curr. Top. Microbiol. Immunol. 336, 63-81. http://dx.doi.org/10.1007/978-3-642-00549-7_4
94. Suzuki Y, Schafer J, Farbman AI (1995): Phagocytic cells in the rat olfactory epithelium aft er bulbectomy. Exp. Neurol. 136, 225-233. http://dx.doi.org/10.1006/exnr.1995.1099
95. Tan CS, Stevenson PG (2014): B cell response to herpesvirus infection of the olfactory neuroepithelium. J. Virol. 88, 14030-14039. http://dx.doi.org/10.1128/JVI.02345-14
96. Tanaka H, Park CH, Ninomiya A, Ozaki H, Takada A, Umemura T, Kida H (2003): Neurotropism of the 1997 Hong Kong H5N1 influenza virus in mice. Vet. Microbiol. 95, 1-13. http://dx.doi.org/10.1016/S0378-1135(03)00132-9
97. Twomey JA, Barker CM, Robinson G, Howell DA (1979): Olfactory mucosa in herpes simplex encephalitis. J. Neurol. Neurosurg. Psychiatry 42, 983-987. http://dx.doi.org/10.1136/jnnp.42.11.983
98. van den Brand JM, Stittelaar KJ, van Amerongen G, Reperant L, de Waal L, Osterhaus AD, Kuiken T (2012): Comparison of temporal and spatial dynamics of seasonal H3N2, pandemic H1N1 and highly pathogenic avian influenza H5N1 virus infections in ferrets. PLoS One 7, e42343. http://dx.doi.org/10.1371/journal.pone.0042343
99. van den Pol AN, Ding S, Robek MD (2014): Long-distance interferon signaling within the brain blocks virus spread. J. Virol. 88, 3695-3704. http://dx.doi.org/10.1128/JVI.03509-13
100. Van Poucke S, Uhlendorff J, Wang Z, Billiau V, Nicholls J, Matrosovich M, Van Reeth K (2013): Effect of receptor specificity of A/Hong Kong/1/68 (H3N2): influenza virus variants on replication and transmission in pigs. Influenza Other Respir. Viruses 7, 151-159. http://dx.doi.org/10.1111/j.1750-2659.2012.00376.x
101. van Riel D, Leijten LM, Verdijk RM, GeurtsvanKessel C, van der Vries E, van Rossum AM, Osterhaus AD, Kuiken T (2014): Evidence for influenza virus CNS invasion along the olfactory route in an immunocompromised infant. J. Infect. Dis. 210, 419-423. http://dx.doi.org/10.1093/infdis/jiu097
102. van Riel D, Verdijk R, Kuiken T (2015): The olfactory nerve: a shortcut for influenza and other viral diseases into the central nervous system. J. Pathol. 235, 277-287. http://dx.doi.org/10.1002/path.4461
103. Verhaeghe J, Gheysen R, Enzlin P (2013): Pheromones and their effect on women's mood and sexuality. Facts Views Vis. Obgyn. 5, 189-195.
104. Vilensky JA (2014): The neglected cranial nerve: Nervus terminalis (cranial nerve N): Clin. Anat. 27, 46-53. http://dx.doi.org/10.1002/ca.22130
105. Xu L, Bao L, Deng W, Zhu H, Chen T, Lv Q, Li F, Yuan J, Xiang Z, Gao K, Xu Y, Huang L, Li Y, Liu J, Yao Y, Yu P, Yong W, Wei Q, Zhang L, Qin C (2013): The mouse and ferret models for studying the novel avian-origin human influenza A (H7N9): virus. Virol J. 10, 253. http://dx.doi.org/10.1186/1743-422X-10-253
106. Xu L, Bao L, Deng W, Dong L, Zhu H, Chen T, Lv Q, Li F, Yuan J, Xiang Z, Gao K, Xu Y, Huang L, Li Y, Liu J, Yao Y, Yu P, Li X, Huang W, Zhao X, Lan Y, Guo J, Yong W, Wei Q, Chen H, Zhang L, Qin C (2014): Novel avian-origin human influenza A (H7N9): can be transmitted between ferrets via respiratory droplets. J. Infect. Dis. 209, 551-556. http://dx.doi.org/10.1093/infdis/jit474
107. Yamada M, Nakamura K, Yoshii M, Kaku Y, Narita M (2009): Brain lesions induced by experimental intranasal infection of Japanese encephalitis virus in piglets. J. Comp. Pathol. 141, 156-162. http://dx.doi.org/10.1016/j.jcpa.2009.04.006
108. Yamada M, Bingham J, Payne J, Rookes J, Lowther S, Haining J, Robinson R, Johnson D, Middleton D (2012): Multiple routes of invasion of wild-type Clade 1 highly pathogenic avian influenza H5N1 virus into the central nervous system (CNS): aft er intranasal exposure in ferrets. Acta Neuropathol. 124, 505-516. http://dx.doi.org/10.1007/s00401-012-1010-8
109. Zielinski MR, Souza G, Taishi P, Bohnet SG, Krueger JM (2013): Olfactory bulb and hypothalamic acute-phase responses to influenza virus: effects of immunization. Neuroimmunomodulation 20, 323-333. http://dx.doi.org/10.1159/000351716
110. Zlotnik I, Grant DP (1976): Further observations on subacute sclerosing encephalitis in adult hamsters: The effects of intranasal infections with Langat virus, measles virus and SSPE-measles virus. Br. J. Exp. Path. 57,49.