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Journal of NeuroVirology

Erschienen in:

01.04.2015

The anterior commissure is a pathway for contralateral spread of herpes simplex virus type 1 after olfactory tract infection

verfasst von: Eva Jennische, Charlotta E. Eriksson, Stefan Lange, Edward Trybala, Tomas Bergström

Erschienen in: Journal of NeuroVirology | Ausgabe 2/2015

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Abstract

Herpes simplex encephalitis (HSE), targeting the limbic system, is the most common cause of viral encephalitis in the Western world. Two pathways for viral entry to the central nervous system (CNS) in HSE have been suggested: either via the trigeminal nerve or via the olfactory tract. This question remains unsettled, and studies of viral spread between the two brain hemispheres are scarce. Here, we investigated the olfactory infection as a model of infection and tropism of herpes simplex virus 1 (HSV-1), the causative agent of HSE, in the CNS of rats. Rats were instilled with HSV-1 in the right nostril and sacrificed 1–6 days post-infection, and tissues were analysed for viral spread using immunohistochemistry and quantitative PCR (qPCR). After nasal instillation, HSV-1 infected mitral cells of the olfactory bulb (OB) on the right side only, followed by limbic encephalitis. As a novel finding, the anterior commissure (AC) conveyed a rapid transmission of virus between the right and the left OB, acting as a shortcut also between the olfactory cortices. The neuronal cell population that conveyed the viral infection via the AC was positive for the water channel protein aquaporin 9 (AQP9) by immunohistochemistry. Quantification of AQP9 in cerebrospinal fluid samples of HSE patients showed increment as compared to controls. We conclude that the olfactory route and the AC are important for the spread of HSV-1 within the olfactory/limbic system of rats and furthermore, we suggest that AQP9 is involved in viral tropism and pathogenesis of HSE.

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Aravalli RN, Hu S, Rowen TN, Gekker G, Lokensgard JR (2006) Differential apoptotic signaling in primary glial cells infected with herpes simplex virus 1. J Neurovirol 12:501–510CrossRefPubMed

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 20:738–750CrossRefPubMedCentralPubMed

Ashwell KW, Marotte LR, Li L, Waite PM (1996) Anterior commissure of the wallaby (Macropus eugenii): adult morphology and development. J Comp Neurol 366:478–494CrossRefPubMed

Badaut J (2010) Aquaglyceroporin 9 in brain pathologies. Neuroscience 168:1047–1057CrossRefPubMed

Badaut J, Regli L (2004) Distribution and possible roles of aquaporin 9 in the brain. Neuroscience 129:971–981CrossRefPubMed

Badaut J, Petit JM, Brunet JF, Magistretti PJ, Charriaut-Marlangue C, Regli L (2004) Distribution of Aquaporin 9 in the adult rat brain: preferential expression in catecholaminergic neurons and in glial cells. Neuroscience 128:27–38CrossRefPubMed

Badaut J, Brunet JF, Regli L (2007) Aquaporins in the brain: from aqueduct to “multi-duct”. Metab Brain Dis 22:251–263CrossRefPubMed

Badaut J, Fukuda AM, Jullienne A, Petry KG (2014) Aquaporin and brain diseases. Biochimica et Biophysica Acta (BBA)—General Subjects 1840:1554–1565CrossRef

Barnett EM, Cassell MD, Perlman S (1993) Two neurotropic viruses, herpes simplex virus type 1 and mouse hepatitis virus, spread along different neural pathways from the main olfactory bulb. Neuroscience 57:1007–1025CrossRefPubMed

Bello-Morales R, Fedetz M, Alcina A, Tabares E, Lopez-Guerrero JA (2005) High susceptibility of a human oligodendroglial cell line to herpes simplex type 1 infection. J Neurovirol 11:190–198CrossRefPubMed

Bergstrom T, Alestig K, Svennerholm B, Horal P, Skoldenberg B, Vahlne A (1990) Neurovirulence of herpes simplex virus types 1 and 2 isolates in diseases of the central nervous system. Eur J Clin Microbiol Infect Dis 9:751–757CrossRefPubMed

Bergström T, Conradi N, Hansson E, Liljeroth A, Vahlne A (1994) Resistance of rat CNS to brain stem infection with herpes simplex virus type 1. Acta Neuropathol 87:398–404CrossRefPubMed

Damasio AR, Van Hoesen GW (1985) The limbic system and the localisation of herpes simplex encephalitis. J Neurol Neurosurg Psychiatry 48:297–301CrossRefPubMedCentralPubMed

Davis LE, Johnson RT (1979) An explanation for the localization of herpes simplex encephalitis? Ann Neurol 5:2–5CrossRefPubMed

De Tiege X, Rozenberg F, Heron B (2008) The spectrum of herpes simplex encephalitis in children. Eur J Paediatr Neurol 12:72–81CrossRefPubMed

Di Virgilio G, Clarke S, Pizzolato G, Schaffner T (1999) Cortical regions contributing to the anterior commissure in man. Exp Brain Res 124:1–7CrossRefPubMed

El-Habashi N, el El-Nahass S, Fukushi H, Hibi D, Sakai H, Sasseville V, Yanai T (2010) Experimental intranasal infection of equine herpesvirus 9 (EHV-9) in suckling hamsters: kinetics of viral transmission and inflammation in the nasal cavity and brain. J Neurovirol 16:242–248CrossRefPubMed

Elkjaer M, Vajda Z, Nejsum LN, Kwon T, Jensen UB, Amiry-Moghaddam M, Frokiaer J, Nielsen S (2000) Immunolocalization of AQP9 in liver, epididymis, testis, spleen, and brain. Biochem Biophys Res Commun 276:1118–1128CrossRefPubMed

Esiri MM (1982) Herpes simplex encephalitis. An immunohistological study of the distribution of viral antigen within the brain. J Neurol Sci 54:209–226CrossRefPubMed

Esiri MM, Tomlinson AH (1984) Herpes simplex encephalitis. Immunohistological demonstration of spread of virus via olfactory and trigeminal pathways after infection of facial skin in mice. J Neurol Sci 64:213–217CrossRefPubMed

Eslinger PJ, Damasio AR, Van Hoesen GW (1982) Olfactory dysfunction in man: anatomical and behavioral aspects. Brain Cogn 1:259–285CrossRefPubMed

Faber HK, Gebhardt LP (1933) Localizations of the virus of poliomyelitis in the central nervous system during the preparalytic period, after intranasal instillation. The Journal of Experimental Medicine 57:933–954CrossRefPubMedCentralPubMed

Fossdal G, Vik-Mo EO, Sandberg C, Varghese M, Kaarbo M, Telmo E, Langmoen IA, Murrell W (2012) Aqp 9 and brain tumour stem cells. ScientificWorldJournal 2012:915176CrossRefPubMedCentralPubMed

Granerod JAH, Davies NW, Clewley JP, Walsh AL, Morgan D, Cunningham R, Zuckerman M, Mutton KJ, Solomon T, Ward KN, Lunn MP, Irani SR, Vincent A, Brown DW, Crowcroft NS, UK Health Protection Agency (HPA) Aetiology of Encephalitis Study Group (2011) Causes of encephalitis and differences in their clinical presentations in England: a multicentre, population-based prospective study. The Lancet infectious diseases 10:835–844CrossRef

Heath CJ, Jones EG (1971) Interhemispheric pathways in the absence of a corpus callosum. An experimental study of commissural connexions in the marsupial phalanger. J Anat 109:253–270PubMedCentralPubMed

Hjalmarsson A, Blomqvist P, Skoldenberg B (2007) Herpes simplex encephalitis in Sweden, 1990–2001: incidence, morbidity, and mortality. Clin Infect Dis 45:875–880CrossRefPubMed

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 163:720–727CrossRefPubMed

Ishibashi K, Kuwahara M, Gu Y, Tanaka Y, Marumo F, Sasaki S (1998) Cloning and functional expression of a new aquaporin (AQP9) abundantly expressed in the peripheral leukocytes permeable to water and urea, but not to glycerol. Biochem Biophys Res Commun 244:268–274CrossRefPubMed

Jennische E, Bergstrom T, Johansson M, Nystrom K, Tarkowski A, Hansson HA, Lange S (2008) The peptide AF-16 abolishes sickness and death at experimental encephalitis by reducing increase of intracranial pressure. Brain Res 1227:189–197CrossRefPubMed

Johnson RT (1964) The pathogenesis of herpes virus encephalitis I. Virus pathways to the nervous system of suckling mice demonstrated by fluorescent antibody staining. J Exp Med 119:343–356CrossRefPubMedCentralPubMed

Jouandet ML, Hartenstein V (1983) Basal telencephalic origins of the anterior commissure of the rat. Exp Brain Res 50:183–192PubMed

Kennedy PG, Chaudhuri A (2002) Herpes simplex encephalitis. J Neurol Neurosurg Psychiatry 73:237–238CrossRefPubMedCentralPubMed

Kennedy PG, Steiner I (2013) Recent issues in herpes simplex encephalitis. J Neurovirol 19:346–350

Kiernan JA (2012) Anatomy of the temporal lobe. Epilepsy Res Treat 2012:176157PubMedCentralPubMed

Kristensson K, Nennesmo L, Persson L, Lycke E (1982) Neuron to neuron transmission of herpes simplex virus. Transport of virus from skin to brainstem nuclei. J Neurol Sci 54:149–156CrossRefPubMed

Kuypers HG, Ugolini G (1990) Viruses as transneuronal tracers. Trends Neurosci 13:71–75CrossRefPubMed

Lehmann GL, Gradilone SA, Marinelli RA (2004) Aquaporin water channels in central nervous system. Curr Neurovasc Res 1:293–303CrossRefPubMed

Liu H, Yang M, Qiu GP, Zhuo F, Yu WH, Sun SQ, Xiu Y (2012) Aquaporin 9 in rat brain after severe traumatic brain injury. Arq Neuropsiquiatr 70:214–220PubMed

Ludlow M, Duprex WP, Cosby SL, Allen IV, McQuaid S (2008) Advantages of using recombinant measles viruses expressing a fluorescent reporter gene with vibratome slice technology in experimental measles neuropathogenesis. Neuropathol Appl Neurobiol 34:424–434

Mann DMA, Tinkler AM, Yates PO (1983) Neurological disease and herpes simplex virus. An immunohistochemical study. Acta Neuropathol 60:24–28CrossRefPubMed

Martinez Torres FJ, Volcker D, Dorner N, Lenhard T, Nielsen S, Haas J, Kiening K, Meyding-Lamade U (2007) Aquaporin 4 regulation during acute and long-term experimental Herpes simplex virus encephalitis. J Neurovirol 13:38–46CrossRefPubMed

McGrath N, Anderson NE, Croxson MC, Powell KF (1997) Herpes simplex encephalitis treated with acyclovir: diagnosis and long term outcome. Journal of Neurology, Neurosurgery & Psychiatry 63:321–326CrossRef

Misra UK, Tan CT, Kalita J (2008) Viral encephalitis and epilepsy. Epilepsia 49(Suppl 6):13–18CrossRefPubMed

Moon SM, Kim T, Lee EM, Kang JK, Lee SA, Choi SH (2014) Comparison of clinical manifestations, outcomes and cerebrospinal fluid findings between herpes simplex type 1 and type 2 central nervous system infections in adults. J Med Virol 86:1766–1771CrossRefPubMed

Mori I, Nishiyama Y, Yokochi T, Kimura Y (2005) Olfactory transmission of neurotropic viruses. J Neurovirol 11:129–137CrossRefPubMed

Nagashima K, Kobayashi Y, Kojima H, Hasegawa H, Kurata T (1998) Herpes encephalitis and paraneoplastic limbic encephalitis. Neuropathology 18:215–221CrossRef

Namvar L, Olofsson S, Bergstrom T, Lindh M (2005) Detection and typing of Herpes Simplex virus (HSV) in mucocutaneous samples by TaqMan PCR targeting a gB segment homologous for HSV types 1 and 2. J Clin Microbiol 43:2058–2064CrossRefPubMedCentralPubMed

Norgren RB Jr, Lehman MN (1998) Herpes simplex virus as a transneuronal tracer. Neurosci Biobehav Rev 22:695–708CrossRefPubMed

Nyström K, Biller M, Grahn A, Lindh M, Larson G, Olofsson S (2004) Real time PCR for monitoring regulation of host gene expression in herpes simplex virus type 1-infected human diploid cells. J Virol Methods 118:83–94CrossRefPubMed

Oliva AA Jr, Kang Y, Truettner JS, Sanchez-Molano J, Furones C, Yool AJ, Atkins CM (2011) Fluid-percussion brain injury induces changes in aquaporin channel expression. Neuroscience 180:272–279CrossRefPubMed

Oyanguren B, Sanchez V, Gonzalez FJ, de Felipe A, Esteban L, Lopez-Sendon JL, Garcia-Barragan N, Martinez-San Millan J, Masjuan J, Corral I (2013) Limbic encephalitis: a clinical-radiological comparison between herpetic and autoimmune etiologies. Eur J Neurol

Papadopoulos MC, Verkman AS (2013) Aquaporin water channels in the nervous system. Nature reviews Neuroscience 14:265CrossRefPubMedCentralPubMed

Patel MD, Toussaint N, Charles-Edwards GD, Lin JP, Batchelor PG (2010) Distribution and fibre field similarity mapping of the human anterior commissure fibres by diffusion tensor imaging. MAGMA 23:399–408CrossRefPubMed

Perlman S, Evans G, Afifi A (1990) Effect of olfactory bulb ablation on spread of a neurotropic coronavirus into the mouse brain. J Exp Med 172:1127–1132CrossRefPubMed

Raschilas F, Wolff M, Delatour F, Chaffaut C, De Broucker T, Chevret S, Lebon P, Canton P, Rozenberg F (2002) Outcome of and prognostic factors for herpes simplex encephalitis in adult patients: results of a multicenter study. Clin Infect Dis 35:254–260CrossRefPubMed

Riancho J, Delgado-Alvarado M, Sedano MJ, Polo JM, Berciano J (2013) Herpes simplex encephalitis: clinical presentation, neurological sequelae and new prognostic factors. Ten years of experience. Neurol Sci

Risse GL, LeDoux J, Springer SP, Wilson DH, Gazzaniga MS (1978) The anterior commissure in man: functional variation in a multisensory system. Neuropsychologia 16:23–31CrossRefPubMed

Shipley MT, Ennis M (1996) Functional organization of olfactory system. J Neurobiol 30:123–176CrossRefPubMed

Sili U, Kaya A, Mert A (2014). Herpes simplex virus encephalitis: Clinical manifestations, diagnosis and outcome in 106 adult patients. J Clin Virol.

Skoldenberg B, Forsgren M, Alestig K, Bergstrom T, Burman L, Dahlqvist E, Forkman A, Fryden A, Lovgren K, Norlin K et al (1984) Acyclovir versus vidarabine in herpes simplex encephalitis. Randomised multicentre study in consecutive Swedish patients. Lancet 2:707–711CrossRefPubMed

Stahl JP, Mailles A, De Broucker T (2012) Herpes simplex encephalitis and management of acyclovir in encephalitis patients in France. Epidemiol Infect 140:372–381CrossRefPubMed

Steiner I (2011) Herpes simplex virus encephalitis: new infection or reactivation? Curr Opin Neurol 24:268–274CrossRefPubMed

Studahl M, Rosengren L, Günther G, Hagberg L (2000) Difference in pathogenesis between herpes simplex virus type 1 encephalitis and tick-borne encephalitis demonstrated by means of cerebrospinal fluid markers of glial and neuronal destruction. J Neurol 247:636–642CrossRefPubMed

Thomas EE, Lau AS, Kim SU, Osborne D, Kastrukoff LF (1991) Variation in resistance to herpes simplex virus type 1 of oligodendrocytes derived from inbred strains of mice. J Gen Virol 72(Pt 9):2051–2057CrossRefPubMed

Toft-Hansen H, Fuchtbauer L, Owens T (2011) Inhibition of reactive astrocytosis in established experimental autoimmune encephalomyelitis favors infiltration by myeloid cells over T cells and enhances severity of disease. Glia 59:166–176CrossRefPubMed

Turner SL, Jenkins FJ (1997) The roles of herpes simplex virus in neuroscience. J Neurovirol 3:110–125CrossRefPubMed

Wang H, Jin R, Tian P, Zhuo Z (2009) Enhanced expression of aquaporin-9 in rat brain edema induced by bacterial lipopolysaccharides. J Huazhong Univ Sci Technolog Med Sci 29:150–155CrossRefPubMed

Whitley RJ (2006) Herpes simplex encephalitis: adolescents and adults. Antiviral Res 71:141–148CrossRefPubMed

Whitley R, Lakeman AD, Nahmias A, Roizman B (1982) Dna restriction-enzyme analysis of herpes simplex virus isolates obtained from patients with encephalitis. N Engl J Med 307:1060–1062CrossRefPubMed

Whitley RJ, Alford CA, Hirsch MS, Schooley RT, Luby JP, Aoki FY, Hanley D, Nahmias AJ, Soong SJ (1986) Vidarabine versus acyclovir therapy in herpes simplex encephalitis. N Engl J Med 314:144–149CrossRefPubMed

Yool AJ (2007) Aquaporins: multiple roles in the central nervous system. Neuroscientist 13:470–485CrossRefPubMed

Titel: The anterior commissure is a pathway for contralateral spread of herpes simplex virus type 1 after olfactory tract infection
verfasst von: Eva Jennische
Charlotta E. Eriksson
Stefan Lange
Edward Trybala
Tomas Bergström
Publikationsdatum: 01.04.2015
Verlag: Springer US
Erschienen in: Journal of NeuroVirology / Ausgabe 2/2015
Print ISSN: 1355-0284
Elektronische ISSN: 1538-2443
DOI: https://doi.org/10.1007/s13365-014-0312-0

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