Distinct cell tropism of canine distemper virus strains to adult olfactory ensheathing cells and Schwann cells in vitro

Virus Research

Volumn 144, Issue 1-2, 2009, Pages 195-201

  Techangamsuwan, Somporn ^a,b   Haas, Ludwig ^a   Rohn, Karl ^a   Baumgärtner, Wolfgang ^a,b   Wewetzer, Konstantin ^a,c  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b CENTER FOR SYSTEMS NEUROSCIENCE   (Germany)

^c HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Canine distemper virus; Cell tropism; Olfactory ensheathing cell; Schwann cell

Indexed keywords

ANIMAL CELL; ARTICLE; CANINE DISTEMPER MORBILLIVIRUS; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; IN VITRO STUDY; NERVE CELL NECROSIS; NONHUMAN; OLFACTORY ENSHEATHING CELL; PRIORITY JOURNAL; SCHWANN CELL; STRAIN DIFFERENCE; VIRUS CELL INTERACTION; VIRUS PATHOGENESIS; VIRUS REPLICATION; VIRUS STRAIN; VIRUS VIRULENCE;

ANIMALS; CELLS, CULTURED; CYTOPATHOGENIC EFFECT, VIRAL; DISTEMPER VIRUS, CANINE; DOGS; SCHWANN CELLS;

CANINE DISTEMPER VIRUS;

EID: 69249222583     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virusres.2009.04.027     Document Type: Article

References (59)

1. Alldinger S., Fonfara S., Kremmer E., and Baumgärtner W. Up-regulation of the hyaluronate receptor CD44 in canine distemper demyelinated plaques. Acta Neuropathol. (Berl.) 99 (2000) 138-146
2. Appel M.J., and Jones O.R. Use of alveolar macrophages for cultivation of canine distemper virus. Proc. Soc. Exp. Biol. Med. 126 (1967) 571-574
3. Aronsson F., Robertson B., Ljunggren H.G., and Kristensson K. Invasion and persistence of the neuroadapted influenza virus A/WSN/33 in the mouse olfactory system. Viral Immunol. 16 (2003) 415-423
4. Barber P.C., and Lindsay R.M. Schwann cells of the olfactory nerves contain glial fibrillary acidic protein and resemble astrocytes. Neuroscience 7 (1982) 3077-3390
5. Baumgärtner W., and Alldinger S. The pathogenesis of canine distemper virus induced demyelination-a biphasic process. In: Lavi E., and Constantinescu C.S. (Eds). Experimental Models of Multiple Sclerosis (2005), Springer, New York 871-887
6. Baumgärtner W., Alldinger S., Beineke A., Gröters S., Herden C., Kaim U., Müller G., Seeliger F., Van Moll P., and Wohlsein P. Canine distemper virus-an agent looking for new hosts. Dtsch. Tierarztl. Wochenschr. 110 (2003) 137-142
7. Baumgärtner W., Krakowka S., and Blakeslee J.R. Persistent infection of Vero cells by paramyxoviruses. A morphological and immunoelectron microscopic investigation. Intervirology 27 (1987) 218-223
8. Beineke A., Puff C., Seehusen F., and Baumgärtner W. Pathogenesis and immunopathology of systemic and nervous canine distemper. Vet. Immunol. Immunopathol. 127 (2009) 1-18
9. Bock P., Beineke A., Techangamsuwan S., Baumgärtner W., and Wewetzer K. Differential expression of HNK-1 and p75(NTR) in adult canine Schwann cells and olfactory ensheathing cells in situ but not in vitro. J. Comp. Neurol. 505 (2007) 572-585
10. Chuah M.I., Tennent R., and Jacobs I. Response of olfactory Schwann cells to intranasal zinc sulfate irrigation. J. Neurosci. Res. 42 (1995) 470-478
11. Chuah M.I., Vincent A.J., and West A.K. Do olfactory ensheathing cells play a role in the defense of the brain against infection?. Neuroembryol. Aging 3 (2004-2005) 152-156
12. Das Sarma J., Iacono K., Gard L., Marek R., Kenyon L.C., Koval M., and Weiss S.R. Demyelinating and nondemyelinating strains of mouse hepatitis virus differ in their neural cell tropism. J. Virol. 82 (2008) 5519-5526
13. Doucette J.R. The glial cells in the nerve fiber layer of the rat olfactory bulb. Anat. Rec. 210 (1984) 385-391
14. Doucette R. Glial influences on axonal growth in the primary olfactory system. Glia 3 (1990) 433-449
15. Esiri M.M., and Tomlinson A.H. 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 (1984) 213-217
16. Field P., Li Y., and Raisman G. Ensheathment of the olfactory nerves in the adult rat. J. Neurocytol. 32 (2003) 317-324
17. Franssen E.H., De Bree F.M., Essing A.H., Ramon-Cueto A., and Verhaagen J. Comparative gene expression profiling of olfactory ensheathing glia and Schwann cells indicates distinct tissue repair characteristics of olfactory ensheathing glia. Glia 56 (2008) 1285-1298
18. Frisk A.L., Baumgärtner W., and Gröne A. Dominating interleukin-10 mRNA expression induction in cerebrospinal fluid cells of dogs with natural canine distemper virus induced demyelinating and non-demyelinating CNS lesions. J. Neuroimmunol. 97 (1999) 102-109
19. Frisk A.L., Konig M., Moritz A., and Baumgärtner W. Detection of canine distemper virus nucleoprotein RNA by reverse transcription-PCR using serum, whole blood, and cerebrospinal fluid from dogs with distemper. J. Clin. Microbiol. 37 (1999) 3634-3643
20. Getchell T.V., Subhedar N.K., Shah D.S., Hackley G., Partin J.V., Sen G., and Getchell M.L. Chemokine regulation of macrophage recruitment into the olfactory epithelium following target ablation: involvement of macrophage inflammatory protein-1alpha and monocyte chemoattractant protein-1. J. Neurosci. Res. 70 (2002) 784-793
21. Gröne A., Fonfara S., and Baumgärtner W. Cell type-dependent cytokine expression after canine distemper virus infection. Viral Immunol. 15 (2002) 493-505
22. Gröne A., Groeters S., Koutinas A., Saridomichelakis M., and Baumgärtner W. Non-cytocidal infection of keratinocytes by canine distemper virus in the so-called hard pad disease of canine distemper. Vet. Microbiol. 96 (2003) 157-163
23. Harvey A.R., and Plant G.W. Olfactory ensheathing glia and spinal cord injury: basic mechanisms to transplantation. Future Neurol. 1 (2006) 453-463
24. Higgins R.J., Krakowka S.G., Metzler A.E., and Koestner A. Experimental canine distemper encephalomyelitis in neonatal gnotobiotic dogs. A sequential ultrastructural study. Acta Neuropathol. (Berl.) 57 (1982) 287-295
25. Jessen K.R., and Mirsky R. Schwann cell precursors and their development. Glia 4 (1991) 185-194
26. Jessen K.R., Morgan L., Stewart H.J., and Mirsky R. Three markers of adult non-myelin-forming Schwann cells, 217c(Ran-1). A5E3 and GFAP: development and regulation by neuron-Schwann cell interactions. Development 109 (1990) 91-103
27. Kai C., Ochikubo F., Okita M., Iinuma T., Mikami T., Kobune F., and Yamanouchi K. Use of B95a cells for isolation of canine distemper virus from clinical cases. J. Vet. Med. Sci. 55 (1993) 1067-1070
28. Keogh B., Sheahan B.J., Atkins G.J., and Mills K.H.G. Inhibition of matrix metalloproteinases ameliorates blood-brain barrier disruption and neuropathological lesions caused by avirulent Semliki Forest virus infection. Vet. Immunol. Immunopathol. 94 (2003) 185-190
29. Koutinas A.F., Baumgärtner W., Tontis D., Polizopoulou Z., Saridomichelakis M.N., and Lekkas S. Histopathology and immunohistochemistry of canine distemper virus-induced footpad hyperkeratosis (hard pad disease) in dogs with natural canine distemper. Vet. Pathol. 41 (2004) 2-9
30. Krudewig C., Deschl U., and Wewetzer K. Purification and in vitro characterization of adult canine olfactory ensheathing cells. Cell Tissue Res. 326 (2006) 687-696
31. Kumnok J., Ulrich R., Wewetzer K., Rohn K., Hansmann F., Baumgärtner W., and Alldinger S. Differential transcription of matrix-metalloproteinase genes in primary mouse astrocytes and microglia infected with Theiler's murine encephalomyelitis virus. J. Neurovirol. 14 (2008) 205-217
32. Lafay F., Coulon P., Astic L., Saucier D., Riche D., Holley A., and Flamand A. Spread of the CVS strain of rabies virus and of the avirulent mutant AvO1 along the olfactory pathways of the mouse after intranasal inoculation. Virology 183 (1991) 320-330
33. Li Y., Field P.M., and Raisman G. Olfactory ensheathing cells and olfactory nerve fibroblasts maintain continuous open channels for regrowth of olfactory nerve fibres. Glia 52 (2005) 245-251
34. Loseva E., Yuan T.F., and Karnup S. Neurogliogenesis in the mature olfactory system: a possible protective role against infection and toxic dust. Brain Res. Rev. (2008) 10.1016/j.brainresrev.2008.10.004
35. Morales J.A., Herzog S., Kompter C., Frese K., and Rott R. Axonal transport of Borna disease virus along olfactory pathways in spontaneously and experimentally infected rats. Med. Microbiol. Immunol. 177 (1988) 51-68
36. Orlando E.A., Imbschweiler I., Gerhauser I., Baumgärtner W., and Wewetzer K. In vitro characterization and preferential infection by canine distemper virus of glial precursors with Schwann cell characteristics from adult canine brain. Neuropathol. Appl. Neurobiol. 34 (2008) 621-637
37. Puff C., Krudewig C., Imbschweiler I., Baumgärtner W., and Alldinger S. Influence of persistent canine distemper virus infection on expression of RECK, matrix-metalloproteinases and their inhibitors in a canine macrophage/monocytic tumour cell line (DH82). Vet. J. (2008) 10.1016/j.tvjl.2008.03.026
38. Radtke C., and Wewetzer K. Translating basic research into clinical practice or what else do we have to learn about olfactory ensheathing cells?. Neurosci. Lett. 456 (2009) 133-136
39. Raisman G. Specialized neuroglial arrangement may explain the capacity of vomeronasal axons to reinnervate central neurons. Neuroscience 14 (1985) 237-254
40. Rudd P.A., Cattaneo R., and von Messling V. Canine distemper virus uses both the anterograde and the hematogenous pathway for neuroinvasion. J. Virol. 80 (2006) 9361-9370
41. Seehusen F., Orlando E.A., Wewetzer K., and Baumgärtner W. Vimentin-positive astrocytes in canine distemper: a target for canine distemper virus especially in chronic demyelinating lesions?. Acta Neuropathol. 114 (2007) 597-608
42. Shindler K.S., Kenyon L.C., Dutt M., Hingley S.T., and Das Sarma J. Experimental optic neuritis induced by a demyelinating strain of mouse hepatitis virus. J. Virol. 82 (2008) 8882-8886
43. Stern L.B., Greenberg M., Gershoni J.M., and Rozenblatt S. The hemagglutinin envelope protein of canine distemper virus (CDV) confers cell tropism as illustrated by CDV and measles virus complementation analysis. J. Virol. 69 (1995) 1661-1668
44. Suter S.E., Chein M.B., von Messling V., Yip B., Cattaneo R., Vernau W., Madewell B.R., and London C.A. In vitro canine distemper virus infection of canine lymphoid cells: a prelude to oncolytic therapy for lymphoma. Clin. Cancer Res. 11 (2005) 1579-1587
45. Takeda M. Measles virus breaks through epithelial cell barriers to achieve transmission. J. Clin. Invest. 118 (2008) 2386-2389
46. Techangamsuwan S., Imbschweiler I., Kreutzer R., Kreutzer M., Baumgärtner W., and Wewetzer K. Similar behaviour and primate-like properties of adult canine Schwann cells and olfactory ensheathing cells in long-term culture. Brain Res. 1240 (2008) 31-38
47. Techangamsuwan S., Kreutzer R., Kreutzer M., Imbschweiler I., Rohn K., Wewetzer K., and Baumgärtner W. Transfection of adult canine Schwann cells and olfactory ensheathing cells at early and late passage with human TERT differentially affects growth factor responsiveness and in vitro growth. J. Neurosci. Methods 176 (2009) 112-120
48. NTR) can serve as a receptor for rabies virus. EMBO J. 17 (1998) 7250-7259
49. NTR is not essential for rabies virus infection. J. Virol. 81 (2007) 13622-13630
50. Ulrich R., Baumgärtner W., Gerhauser I., Seeliger F., Haist V., Deschl U., and Alldinger S. MMP-12, MMP-3, and TIMP-1 are markedly upregulated in chronic demyelinating theiler murine encephalomyelitis. J. Neuropathol. Exp. Neurol. 65 (2006) 783-793
51. Van Moll P., Alldinger S., Baumgärtner W., and Adami M. Distemper in wild carnivores: an epidemiological, histological and immunocytochemical study. Vet. Microbiol. 44 (1995) 193-199
52. Vandevelde M., and Zurbriggen A. Demyelination in canine distemper virus infection: a review. Acta Neuropathol. 109 (2005) 56-68
53. von Messling V., Milosevic D., and Cattaneo R. Tropism illuminated: lymphocyte-based pathways blazed by lethal morbillivirus through the host immune system. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 14216-14221
54. von Messling V., Zimmer G., Herrler G., Haas L., and Cattaneo R. The hemagglutinin of canine distemper virus determines tropism and cytopathogenicity. J. Virol. 75 (2001) 6418-6427
55. Wewetzer K., and Brandes G. Axonal signaling and the making of olfactory ensheathing cells: a hypothesis. Neuron Glia Biol. 2 (2006) 217-224
56. - neonatal rat olfactory ensheathing cells. Glia 49 (2005) 577-587
57. Wewetzer K., Verdu E., Angelov D.N., and Navarro X. Olfactory ensheathing glia and Schwann cells: two of a kind?. Cell Tissue Res. 309 (2002) 337-345
58. Wiener D., Plattet P., Cherpillod P., Zipperle L., Doherr M.G., Vandevelde M., and Zurbriggen A. Synergistic inhibition in cell-cell fusion mediated by the matrix and nucleocapsid protein of canine distemper virus. Virus Res. 129 (2007) 145-154
59. Wohlsein P., Puff C., Kreutzer M., Siebert U., and Baumgärtner W. Distemper in a dolphin. Emerg. Infect. Dis. 13 (2007) 1959-1961