Canine distemper virus persistence in demyelinating encephalitis by swift intracellular cell-to-cell spread in astrocytes is controlled by the viral attachment protein

Acta Neuropathologica

Volumn 119, Issue 5, 2010, Pages 617-630

  Wyss Fluehmann, Gaby ^a   Zurbriggen, Andreas ^a   Vandevelde, Marc ^a   Plattet, Philippe ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

Attachment protein; CDV persistence; Demyelinating encephalitis; Primary brain cells; Swift cell to cell spread

Indexed keywords

CD150 ANTIGEN; GLYCOPROTEIN; UNCLASSIFIED DRUG; VIRUS ATTACHMENT PROTEIN; VIRUS FUSION PROTEIN; VIRUS PROTEIN; VIRUS RECEPTOR;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN NERVE CELL; CANINE DISTEMPER; CANINE DISTEMPER MORBILLIVIRUS; CELL SURFACE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DEMYELINATING DISEASE; ELECTRON MICROSCOPY; GLIA CELL; LENTIVIRINAE; NONHUMAN; PERSISTENT VIRUS INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; TARGET CELL; TITRIMETRY; VIRAL GENE DELIVERY SYSTEM; VIRUS ATTACHMENT; VIRUS RECOMBINANT; VIRUS REPLICATION; VIRUS TRANSMISSION; VIRUS VIRULENCE;

ANIMALS; ANTIGENS, CD; ASTROCYTES; CELL CULTURE TECHNIQUES; CELLS, CULTURED; CYTOPATHOGENIC EFFECT, VIRAL; DISTEMPER VIRUS, CANINE; DOGS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, VIRAL; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; MICROSCOPY, VIDEO; RECEPTORS, CELL SURFACE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TIME FACTORS;

EID: 77953025370     PISSN: 00016322     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00401-010-0644-7     Document Type: Article

References (44)

1. Bollo E, Zurbriggen A, Vandevelde M, Fankhauser R (1986) Canine distemper virus clearance in chronic inflammatory demyelination. Acta Neuropathol (Berl) 72:69-73.
2. Brettschneider J, Tumani H, Kiechle U, Muche R, Richards G, Lehmensiek V, Ludolph AC, Otto M (2009) IgG antibodies against measles, rubella, and varicella zoster virus predict conversion to multiple sclerosis in clinically isolated syndrome. PLoS One 4:e7638.
3. Brown HR, Goller N, Thormar H, Norrby E (1987) Fuzzy material surrounding measles virus nucleocapsids identified as matrix protein. Brief report. Arch Virol 94:163-168.
4. Buchholz UJ, Finke S, Conzelmann KK (1999) Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J Virol 73:251-259.
5. Calain P, Roux L (1993) The rule of six, a basic feature for efficient replication of Sendai virus defective interfering RNA. J Virol 67:4822-4830.
6. Dayer AG, Jenny B, Sauvain MO, Potter G, Salmon P, Zgraggen E, Kanemitsu M, Gascon E, Sizonenko S, Trono D, Kiss JZ (2007) Expression of FGF-2 in neural progenitor cells enhances their potential for cellular brain repair in the rodent cortex. Brain 130:2962-2976.
7. Duprex WP, McQuaid S, Hangartner L, Billeter MA, Rima BK (1999) Observation of measles virus cell-to-cell spread in astrocytoma cells by using a green fluorescent protein-expressing recombinant virus. J Virol 73:9568-9575.
8. Duprex WP, McQuaid S, Roscic-Mrkic B, Cattaneo R, McCallister C, RimaBK(2000) In vitro and in vivo infection of neural cells by a recombinant measles virus expressing enhanced green fluorescent protein. J Virol 74:7972-7979.
9. Ehrengruber MU, Ehler E, Billeter MA, Naim HY (2002) Measles virus spreads in rat hippocampal neurons by cell-to-cell contact and in a polarized fashion. J Virol 76:5720-5728.
10. Firsching R, Buchholz CJ, Schneider U, Cattaneo R, ter Meulen V, Schneider-Schaulies J (1999) Measles virus spread by cell-cell contacts: uncoupling of contact-mediated receptor (CD46) downregulation from virus uptake. J Virol 73:5265- 5273.
11. Glaus T, Griot C, Richard A, Althaus U, Herschkowitz N, Vandevelde M (1990) Ultrastructural and biochemical findings in brain cell cultures infected with canine distemper virus. Acta Neuropathol 80:59-67.
12. Higgins RJ, Krakowka S, Metzler AE, Koestner A (1982) Immunoperoxidase labeling of canine distemper virus replication cycle in Vero cells. Am J Vet Res 43:1820-1824.
13. Johnson DC, Webb M, Wisner TW, Brunetti C (2001) Herpes simplex virus gE/gI sorts nascent virions to epithelial cell junctions, promoting virus spread. J Virol 75:821-833.
14. Kielian T (2008) Glial connexins and gap junctions in CNS inflammation and disease. J Neurochem 106:1000-1016.
15. Krone B, Oeffner F, Grange JM (2009) Is the risk of multiple sclerosis related to the 'biography' of the immune system? J Neurol 256:1052-1060.
16. Lamb RA (1993) Paramyxovirus fusion: a hypothesis for changes. Virology 197:1-11.
17. Lamb RA, Jardetzky TS (2007) Structural basis of viral invasion: lessons from paramyxovirus F. Curr Opin Struct Biol 17:427-436.
18. Lamb RA, Kolakofsky D (2001) Paramyxoviridae: the viruses and their replication. In: Fileds BN, Knipe DM, Howley PM, Griffin DE (eds) Fields virology, 4th edn. Lippincott-Raven Publishers, Philadelphia, PA, pp 1305-1340.
19. Lassmann H, Bruck W, Lucchinetti CF (2007) The immunopathology of multiple sclerosis: an overview. Brain Pathol 17:210- 218.
20. Lawrence DM, Patterson CE, Gales TL, D'Orazio JL, Vaughn MM, Rall GF (2000) Measles virus spread between neurons requires cell contact but not CD46 expression, syncytium formation, or extracellular virus production. J Virol 74:1908-1918.
21. Makhortova NR, Askovich P, Patterson CE, Gechman LA, Gerard NP, Rall GF (2007) Neurokinin-1 enables measles virus trans-synaptic spread in neurons. Virology 362:235-244.
22. Marq JB, Brini A, Kolakofsky D, Garcin D (2007) Targeting of the Sendai virus C protein to the plasma membrane via a peptideonly membrane anchor. J Virol 81:3187-3197.
23. Moll M, Pfeuffer J, Klenk HD, Niewiesk S, Maisner A (2004) Polarized glycoprotein targeting affects the spread of measles virus in vitro and in vivo. J Gen Virol 85:1019-1027.
24. Muller CF, Fatzer RS, Beck K, Vandevelde M, Zurbriggen A (1995) Studies on canine distemper virus persistence in the central nervous system. Acta Neuropathol (Berl) 89:438-445.
25. Orlando EA, Imbschweiler I, Gerhauser I, Baumgartner W, Wewetzer K (2008) In vitro characterization and preferential infection by canine distemper virus of glial precursors with Schwann cell characteristics from adult canine brain. Neuropathol Appl Neurobiol 34:621-637.
26. Orvell C, Sheshberadaran H, Norrby E (1985) Preparation and characterization of monoclonal antibodies directed against four structural components of canine distemper virus. J Gen Virol 66(Pt 3):443-456. (Pubitemid 15136798)
27. Plattet P, Rivals JP, Zuber B, Brunner JM, Zurbriggen A, Wittek R (2005) The fusion protein of wild-type canine distemper virus is a major determinant of persistent infection. Virology 337:312-326.
28. Plattet P, Zweifel C, Wiederkehr C, Belloy L, Cherpillod P, Zurbriggen A, Wittek R (2004) Recovery of a persistent Canine distemper virus expressing the enhanced green fluorescent protein from cloned cDNA. Virus Res 101:147-153.
29. Rima BK, Duprex WP (2006) Morbilliviruses and human disease. J Pathol 208:199-214.
30. Rivals JP, Plattet P, Currat-Zweifel C, Zurbriggen A, Wittek R (2007) Adaptation of canine distemper virus to canine footpad keratinocytes modifies polymerase activity and fusogenicity through amino acid substitutions in the P/V/C and H proteins. Virology 359:6-18.
31. Rouach N, Koulakoff A, Abudara V, Willecke K, Giaume C (2008) Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 322:1551-1555.
32. Rudd PA, Cattaneo R, von Messling V (2006) Canine distemper virus uses both the anterograde and the hematogenous pathway for neuroinvasion. J Virol 80:9361-9370.
33. Russell CJ, Jardetzky TS, Lamb RA (2001) Membrane fusion machines of paramyxoviruses: capture of intermediates of fusion. EMBO J 20:4024-4034.
34. Sattentau Q (2008) Avoiding the void: cell-to-cell spread of human viruses. Nat Rev Microbiol 6:815-826.
35. Singethan K, Muller N, Schubert S, Luttge D, Krementsov DN, Khurana SR, Krohne G, Schneider-Schaulies S, Thali M, Schneider-Schaulies J (2008) CD9 clustering and formation of microvilli zippers between contacting cells regulates virusinduced cell fusion. Traffic 9:924-935.
36. Sips GJ, Chesik D, Glazenburg L, Wilschut J, De Keyser J, Wilczak N (2007) Involvement of morbilliviruses in the pathogenesis of demyelinating disease. Rev Med Virol 17:223-244.
37. Tatsuo H, Ono N, Tanaka K, Yanagi Y (2000) SLAM (CDw150) is a cellular receptor for measles virus. Nature 406:893-897.
38. Tatsuo H, Ono N, Yanagi Y (2001) Morbilliviruses use signaling lymphocyte activation molecules (CD150) as cellular receptors. J Virol 75:5842-5850.
39. Vandevelde M, Zurbriggen A (2005) Demyelination in canine distemper virus infection: a review.ActaNeuropathol (Berl) 109:56-68.
40. von Messling V, Milosevic D, Cattaneo R (2004) Tropism illuminated: lymphocyte-based pathways blazed by lethal morbillivirus through the host immune system. Proc Natl Acad Sci USA 101:14216-14221.
41. von Messling V, Svitek N, Cattaneo R (2006) Receptor (SLAM [CD150]) recognition and the V protein sustain swift lymphocyte- based invasion of mucosal tissue and lymphatic organs by a morbillivirus. J Virol 80:6084-6092.
42. Wenzlow N, Plattet P, Wittek R, Zurbriggen A, Grone A (2007) Immunohistochemical demonstration of the putative canine distemper virus receptor CD150 in dogs with and without distemper. Vet Pathol 44:943-948.
43. Zurbriggen A, Graber HU, Vandevelde M (1995) Selective spread and reduced virus release leads to canine distemper virus persistence in the nervous system. Vet Microbiol 44:281-288.
44. Zurbriggen A, Graber HU, Wagner A, Vandevelde M (1995) Canine distemper virus persistence in the nervous system is associated with noncytolytic selective virus spread. J Virol 69:1678-1686.