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01-09-2007 | Original Paper

Morphological and biochemical characterisation of sensory neurons infected in vitro with rabies virus

Authors: Marlén Martínez-Gutiérrez, Jaime E. Castellanos

Published in: Acta Neuropathologica | Issue 3/2007

Abstract

This work was aimed at the morphological and biochemical characterisation of the most susceptible neuronal subpopulation to rabies virus (RABV) infection. Adult mouse DRG cultures were infected with RABV and double-processed for viral antigen detection and neuropeptides: calcitonine gene-related peptide (CGRP), galanin (GAL), substance P (SP), neuropeptide Y (NPY) and vasoactive intestinal peptide (VIP). It was found that 56% of the neurons in culture were small (diameter <20 μm) but, in spite of this, 69% of the infected neurons had intermediate and large diameters (≥20 μm). More than 50% of infected neurons expressed NPY, VIP or SP, whereas no association was found between infected neurons and the presence of CGRP or GAL. Despite SP having been shown to be a small neuron marker, it was found that RABV infects medium and large-sized SP positive cells. RABV preference for larger neurons could explain part of the neuropathogenesis since it can be suggested that, following a rabid accident, the virus uses large neurons (mainly innervating muscle and joints) in vivo to be transported later on to the central nervous system.

Baer GM, Shanta TR, Bourne GH (1968) The pathogenesis of street rabies virus in rats. Bull World Health Org 38:119–125PubMed

Castellanos JE, Hurtado H, Arias JC, Velandia A (1996) Rabies virus infection of cultured adult mouse dorsal root ganglion neurons. Mem Inst Oswaldo Cruz 91:621–625PubMedCrossRef

Castellanos JE, Hurtado H (1999) Viral infection studied in adult sensory neurons. In: Chichester LH (ed) The neuron in tissue culture. Wiley, Chichester, pp 289–293

Castellanos JE, Martínez M, Hurtado H, Acosta O (2000) Nerve growth factor and neurotrophin-3 modulates the rabies infection of adult sensory neurons in primary cultures. Brain Res 871:120–126PubMedCrossRef

Charlton KM, Casey GA (1979) Experimental rabies in skunks: immunofluorescence light and electron microscopic studies. Lab Invest 41:36–44PubMed

Charlton KM, Nadin-Davis S, Casey GA, Wandeler AI (1997) The long incubation period in rabies: delayed progression of infection in muscle at the site of exposure. Acta Neuropathol Berl 94:73–77PubMedCrossRef

Frieri M (2003) Neuroimmunology and inflammation: implications for therapy of allergic and autoimmune diseases. Ann Allergy Asthma Immunol 90:34–40PubMedCrossRef

Harper AA, Lawson SN (1985) Conduction velocity is related to morphological cell type in rat dorsal root ganglion neurons. J Physiol 359:31–46PubMed

Hemachudha T, Laothamatas J, Rupprecht CE (2002) Human rabies: a disease of complex neuropathogenetic mechanisms and diagnostic challenges. Lancet Neurol 1:101–109PubMedCrossRef

10.

Henken DB, Martin JR (1991) Herpes simplex virus infection in populations of mouse dorsal root ganglion neurons: effects of inoculation route and virus strain. J Neurol Sci 105:29–36PubMedCrossRef

11.

Hokfelt T, Wiesenfeld-Hallin Z, Villar ML, Melander T (1987) Increase of galanin-like immunoreactivity in rat dorsal root ganglion cells after peripheral axotomy. Neurosci Lett 83:217–220PubMedCrossRef

12.

Holford LC, Case P, Lawson N (1994) Substance P, neurofilament, peripherin and SSEA4 immunocytochemistry of human dorsal root ganglion neurons obtained from post-mortem tissue: a quantitative morphometric analysis. J Neurocytol 23:577–589PubMedCrossRef

13.

Hu P, McLachlan EM (2003) Selective reactions of cutaneous and muscle afferent neurons to peripheral nerve transection in rats. J Neurosci 23:10559–10567PubMed

14.

Jackson AC (2003) Rabies virus infection: an update. J Neurovirol 9:253–258PubMedCrossRef

15.

Lawson NS, Perry MJ, Prabhakar E, McCarthy W (1993) Primary sensory neurons: neurofilament, neuropeptides and conduction velocity. Brain Res Bull 30:239–243PubMedCrossRef

16.

Lentz T, Burrage T, Smith A, Crick J, Tignor G (1982) Is the acetylcholine receptor a rabies virus receptor? Science 215:182–184PubMedCrossRef

17.

Lewis P, Fu Y, Lentz TL (2000) Rabies virus entry at the neuromuscular junction in nerve-muscle cocultures. Muscle Nerve 23:720–730PubMedCrossRef

18.

Lycke E, Tsiang H (1987) Rabies virus infection of cultured rat sensory neurons. J Virol 61:2733–2741PubMed

19.

Matsumoto S, Schneider LG, Kawal A, Yonezawa T (1974) Further studies on the replication of rabies and rabies-like viruses in organized cultures of mammalian neural cells. J Virol 61:981–996

20.

McCarthy PW, Lawson SN (1989) Cell type and conduction velocity of rat primary sensory neurons with substance P-like immunoreactivity. Neuroscience 28:745–753PubMedCrossRef

21.

McCarthy PW, Lawson SN (1990) Cell type and conduction velocity of rat primary sensory neurons with calcitonin gene-related peptide-like immunoreactivity. Neuroscience 34:623–632PubMedCrossRef

22.

McMahon SB, Armanini MP, Ling LH, Phillips HS (1994) Expression and coexpression of Trk receptors in subpopulations of adult primary sensory neurons projecting to identified peripheral targets. Neuron 12:1161–1171PubMedCrossRef

23.

Meslin FX, Kaplan MM, Koprowski H (1996) Laboratory techniques in rabies, 4th edn. WHO, Geneva

24.

Molliver DC, Wright DE, Leitner ML, Parsadanian AS, Doster K, Wen D, Yan Q, Snider WD (1997) IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron 4:849–861CrossRef

25.

Mulderry PK (1994) Neuropeptide expression by newborn and adult rat sensory neurons in culture: effects of nerve growth factor and other neurotrophic factors. Neuroscience 59:673–688PubMedCrossRef

26.

Murphy FA, Bauer SP, Harrison AK, Winn WC (1973) Comparative pathogenesis of rabies and rabies-like viruses. Viral infection and transit from inoculation site to the central nervous system. Lab Invest 28:361–376PubMed

27.

Ninomiya T, Walter B, Droz B (1994) Neuronal phenotypes in mouse dorsal root ganglion cell cultures: enrichment of substance P and calbindin D-28k expressing neurons in a defined medium. Int J Dev Neurosci 12:99–106PubMedCrossRef

28.

Noguchi K, Senba E, Morita Y, Sato M, Tohyama M (1990) α-CGRP and β-CGRP mRNAs are deferentially regulated in the rat spinal cord and dorsal root ganglion. Mol Brain Res 7:299–304PubMedCrossRef

29.

Rambourg A, Clermont Y, Beaudet A (1983) Ultrastructural features of six types of neurons in rat dorsal root ganglia. J Neurocytol 12:47–66PubMedCrossRef

30.

Ruiz G, Banos JE (2005) The effect of endoneurial nerve growth factor on calcitonin gene-related peptide expression in primary sensory neurons. Brain Res 1042:44–52PubMedCrossRef

31.

Schoenen J, Delree P, Leprince P, Moonen G (1989) Neurotransmitter phenotype plasticity in cultured dissociated adult rat dorsal root ganglia: an immunocytochemical study. J Neurosci Res 22:473–478PubMedCrossRef

32.

Shankar V, Dietzschold B, Koprowski H (1991) Direct entry of rabies virus into the central nervous system without prior local replication. J Virol 65:2736–2738PubMed

33.

Sommer E, Kazimierczak J, Droz B (1985) Neuronal subpopulations in the dorsal root ganglion of the mouse as characterised by combination of ultrastructural and cytochemical features. Brain Res 346:310–326PubMedCrossRef

34.

Thoulouze MI, Lafage M, Schachner M, Hartmann U, Cremer H, Lafon M (1998) The neural cell adhesion molecule is a receptor for rabies virus. J Virol 72:7181–7190PubMed

35.

Tsiang H, Ceccaldi PE, Lycke E (1991) Rabies virus infection and transport in human sensory dorsal root ganglia neurons. J Gen Virol 72:1191–1194PubMed

36.

Tuffereau C, Bénéjean J, Blondel D, Kieffer B, Flamand A (1998) Low-affinity nerve growth factor receptor (p75NTR) can serve as a receptor for rabies virus. EMBO J 17:7250–259PubMedCrossRef

37.

Tuominen M, Leppaluoto J (1987) Peptides and neurotransmission in the central nervous system. Med Biol 65:137–42PubMed

38.

Velandia ML, Martínez-Gutierrez M, Lafon M, Castellanos JE (2004) Transynaptical jump of rabies virus from ipsi- to contralateral sensory neurons, evidence of a spinal cord complex connectivity. J Neurovirol 10:s127–s128

39.

Verge VM, Richardson PM, Wiesenfeld-Hallin Z, Hokfelt T (1995) Differential influence of nerve growth factor on neuropeptide expression in vivo: a novel role in peptide suppression in adult sensory neurons. J Neurosci 15:2081–2096PubMed

40.

Villar MJ, Cortes R, Theodorsson E, Wiesenfeld-Hallin Z, Schalling M, Fahrenkrug J, Emson PC, Hokfelt T (1989) Neuropeptide expression in rat dorsal root ganglion cells and spinal cord after peripheral nerve injury with special reference to galanin. Neuroscience 33:587–604PubMedCrossRef

41.

Wakisaka S, Kajander KC, Bennett GJ (1991) Increased neuropeptide (NPY)-like immunoreactivity in rat sensory neurons following peripheral axotomy. Neurosci Lett 124:200–203PubMedCrossRef

42.

Watson HD, Tignor GH, Smith AL (1981) Entry of rabies virus into the peripheral nerves of mice. J Gen Virol 56:372–382PubMedCrossRef

43.

Weissner W, Winterson BJ, Stuart-Tilley A, Devor M, Bove GM (2006) Time course of substance P expression in dorsal root ganglia following complete spinal nerve transaction. J Comp Neurol 497:78–87PubMedCrossRef

44.

White DM, Mansfield K (1996) Vasoactive intestinal polypeptide and neuropeptide Y act indirectly to increase neurite outgrowth of dissociated dorsal root ganglion cells. Neuroscience 73:881–887PubMedCrossRef

Title: Morphological and biochemical characterisation of sensory neurons infected in vitro with rabies virus
Authors: Marlén Martínez-Gutiérrez
Jaime E. Castellanos
Publication date: 01-09-2007
Publisher: Springer-Verlag
Published in: Acta Neuropathologica / Issue 3/2007
Print ISSN: 0001-6322
Electronic ISSN: 1432-0533
DOI: https://doi.org/10.1007/s00401-007-0222-9

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Morphological and biochemical characterisation of sensory neurons infected in vitro with rabies virus

Abstract

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