The F gene of the Osaka-2 strain of measles virus derived from a case of subacute sclerosing panencephalitis is a major determinant of neurovirulence

Journal of Virology

Volumn 84, Issue 21, 2010, Pages 11189-11199

  Ayata, Minoru ^a   Takeuchi, Kaoru ^b   Takeda, Makoto ^c   Ohgimoto, Shinji ^a   Kato, Seiichi ^a   Sharma, Luna Bhatta ^a   Tanaka, Miyuu ^d   Kuwamura, Mitsuru ^d   Ishida, Hiroshi ^a,e   Ogura, Hisashi ^a  

^a OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^d Osaka Prefecture University   (Japan)

^e Izumi Municipal Hospital   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

F PROTEIN; H PROTEIN; M PROTEIN; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; VIRUS PROTEIN; VIRUS FUSION PROTEIN;

ACUTE BRAIN DISEASE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; FEMALE; HAMSTER; HIPPOCAMPUS; HUMAN; INOCULATION; MEASLES VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SUBACUTE SCLEROSING PANENCEPHALITIS; SYNCYTIUM; VIRUS GENE; VIRUS RECOMBINANT; VIRUS STRAIN; VIRUS VIRULENCE; WILD TYPE; ANIMAL; CHLOROCEBUS AETHIOPS; GENETICS; PATHOGENICITY; PHYSIOLOGY; SPECIES DIFFERENCE; VERO CELL LINE; VIROLOGY; VIRULENCE;

CRICETINAE; MEASLES VIRUS;

ANIMALS; CERCOPITHECUS AETHIOPS; CRICETINAE; MEASLES VIRUS; SPECIES SPECIFICITY; SUBACUTE SCLEROSING PANENCEPHALITIS; VERO CELLS; VIRAL FUSION PROTEINS; VIRULENCE;

EID: 77957949604     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01075-10     Document Type: Article

References (70)

1. Albrecht, P., and H. P. Schumacher. 1971. Neurotropic properties of measles virus in hamsters and mice. J. Infect. Dis. 124:86-93.
2. Albrecht, P., T. Burnstein, M. J. Klutch, H. T. Hicks, and F. A. Ennis. 1977. Subacute sclerosing panencephalitis: experimental infection in primates. Science 195:64-66.
3. Ayata, M., A. Hirano, and T. C. Wong. 1989. Structural defect linked to nonrandom mutations in the matrix gene of Biken strain subacute sclerosing panencephalitis virus defined by cDNA cloning and expression of chimeric genes. J. Virol. 63:1162-1173.
4. Ayata, M., K. Hayashi, T. Seto, R. Murata, and H. Ogura. 1998. The matrix gene expression of subacute sclerosing panencephalitis (SSPE) virus (Osaka-1 strain): a comparison of two sibling viruses isolated from different lobes of an SSPE brain. Microbiol. Immunol. 42:773-780.
5. Ayata, M., K. Komase, M. Shingai, I. Matsunaga, Y. Katayama, and T. C. Wong. 2002. Mutations affecting transcriptional termination in the P gene end of subacute sclerosing panencephalitis viruses. J. Virol. 76:13062-13068.
6. Ayata, M., M. Shingai, X. Ning, M. Matsumoto, T. Seya, S. Otani, T. Seto, S. Ohgimoto, and H. Ogura. 2007. Effect of the alterations in the fusion protein of measles virus isolated from brains of patients with subacute sclerosing panencephalitis on syncytium formation. Virus Res. 130:260-268.
7. Baringer, J. R., and J. F. Griffith. 1970. Experimental measles virus encephalitis. A light, phase, fluorescence, and electron microscopic study. Lab. Invest. 23:335-346.
8. Billeter, M. A., R. Cattaneo, P. Spielhofer, K. Kaelin, M. Huber, A. Schmid, K. Baczko, and V. ter Meulen. 1994. Generation and properties of measles virus mutations typically associated with subacute sclerosing panencephalitis. Ann. N. Y. Acad. Sci. 724:367-377.
9. Byington, D. P., and K. P. Johnson. 1972. Experimental subacute sclerosing panencephalitis in the hamster: correlation of age with chronic inclusion-cell encephalitis. J. Infect. Dis. 126:18-26.
10. Cathomen, T., B. Mrkic, D. Spehner, R. Drillien, R. Naef, J. Pavlovic, A. Aguzzi, M. A. Billeter, and R. Cattaneo. 1998. A matrix-less measles virus is infectious and elicits extensive cell fusion: consequences for propagation in the brain. EMBO J. 17:3899-3908.
11. Cathomen, T., H. Y. Naim, and R. Cattaneo. 1998. Measles viruses with altered envelope protein cytoplasmic tails gain cell fusion competence. J. Virol. 72:1224-1234. (Pubitemid 28116907)
12. Cattaneo, R., A. Schmid, G. Rebmann, K. Baczko, V. ter Meulen, W. J. Bellini, S. Rozenblatt, and M. A. Billeter. 1986. Accumulated measles virus mutations in a case of subacute sclerosing panencephalitis: interrupted matrix protein reading frame and transcription alteration. Virology 154:97-107.
13. Cattaneo, R., G. Rebmann, A. Schmid, K. Baczko, V. ter Meulen, and M. A. Billeter. 1987. Altered transcription of a defective measles virus genome derived from a diseased human brain. EMBO J. 6:681-688.
14. Cattaneo, R., A. Schmid, M. A. Billeter, R. D. Sheppard, and S. A. Udem. 1988. Multiple viral mutations rather than host factors cause defective measles virus gene expression in a subacute sclerosing panencephalitis cell line. J. Virol. 62:1388-1397.
15. Cattaneo, R., A. Schmid, D. Eschle, K. Baczko, V. ter Meulen, and M. A. Billeter. 1988. Biased hypermutation and other genetic changes in defective measles viruses in human brain infections. Cell 55:255-265.
16. Cattaneo, R., A. Schmid, P. Spielhofer, K. Kaelin, K. Baczko, V. ter Meulen, J. Pardowits, S. Flanagan, B. K. Rima, S. A. Udem, and M. A. Billeter. 1989. Mutated and hypermutated genes of persistent measles viruses which caused lethal human brain diseases. Virology 173:415-425.
17. Doyle, J., A. Prussia, L. K. White, A. Sun, D. C. Liotta, J. P. Snyder, R. W. Compans, and R. K. Plemper. 2006. Two domains that control prefusion stability and transport competence of the measles virus fusion protein. J. Virol. 80:1524-1536.
18. Duprex, W. P., I. Duffy, S. McQuaid, L. Hamill, S. L. Cosby, M. A. Billeter, J. Schneider-Schaulies, V. ter Meulen, and B. K. Rima. 1999. The H gene of rodent brain-adapted measles virus confers neurovirulence to the Edmonston vaccine strain. J. Virol. 73:6916-6922.
19. Duprex, W. P., S. McQuaid, B. Roscic-Mrkic, R. Cattaneo, C. McCallister, and B. K. Rima. 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.
20. Eckert, D. M., and P. S. Kim. 2001. Mechanisms of viral membrane fusion and its inhibition. Annu. Rev. Biochem. 70:777-810.
21. Ehrengruber, M. U., E. Ehler, M. A. Billeter, and H. Y. Naim. 2002. Measles virus spreads in rat hippocampal neurons by cell-to-cell contact and in a polarized fashion. J. Virol. 76:5720-5728.
22. Erlenhoefer, C., W. J. Wurzer, S. Löffler, S. Schneider-Schaulies, V. ter Meulen, and J. Schneider-Schaulies. 2001. CD150 (SLAM) is a receptor for measles virus but is not involved in viral contact-mediated proliferation inhibition. J. Virol. 75:4499-4505.
23. Furukawa, K., M. Ayata, M. Kimura, T. Seto, I. Matsunaga, R. Murata, T. Yamano, and H. Ogura. 2001. Hemadsorption expressed by cloned H genes from subacute sclerosing panencephalitis (SSPE) viruses and their possible progenitor measles viruses isolated in Osaka, Japan. Microbiol. Immunol. 45:59-68.
24. Griffin, D. E., J. Mullinix, O. Narayan, and R. Johnson. 1974. Age dependence of viral expression: comparative pathogenesis of two rodent-adapted strains of measles virus in mice. Infect. Immun. 126:690-695.
25. Griffin, D. E. 2007. Measles virus, p. 1551-1585. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields Virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
26. Hsu, E. C., F. Sarangi, C. Iorio, M. S. Sidhu, S. A. Udem, D. L. Dillehay, W. Xu, P. A. Rota, W. J. Bellini, and C. D. Richardson. 1998. A single amino acid change in the hemagglutinin protein of measles virus determines its ability to bind CD46 and reveals another receptor on marmoset B cells. J. Virol. 72:2905-2916.
27. Hsu, E. C., C. Iorio, F. Sarangi, A. A. Khine, and C. D. Richardson. 2001. CDw150(SLAM) is a receptor for a lymphotropic strain of measles virus and may account for the immunosuppressive properties of this virus. Virology 279:9-21.
28. Ishida, H., M. Ayata, M. Shingai, I. Matsunaga, Y. Seto, Y. Katayama, N. Iritani, T. Seya, Y. Yanagi, O. Matsuoka, T. Yamano, and H. Ogura. 2004. Infection of different cell lines of neural origin with subacute sclerosing panencephalitis (SSPE) virus. Microbiol. Immunol. 48:277-287.
29. Ito, N., M. Ayata, M. Shingai, K. Furukawa, T. Seto, I. Matsunaga, M. Muraoka, and H. Ogura. 2002. Comparison of the neuropathogenicity of two SSPE sibling viruses of the Osaka-2 strain isolated with Vero and B95a cells. J. Neurovirol. 8:6-13. (Pubitemid 34196410)
30. Iwata, K., T. Seya, H. Ariga, and S. Nagasawa. 1994. Expression of a hybrid complement regulatory protein, membrane cofactor protein decay accelerating factor on Chinese hamster ovary: comparison of its regulatory effect with those of decay accelerating factor and membrane cofactor protein. J. Immunol. 152:3436-3444.
31. Johnson, K. P., and D. P. Byington. 1971. Subacute sclerosing panencephalitis (SSPE) agent in hamsters. I. Acute giant cell encephalitis in newborn animals. Exp. Mol. Pathol. 15:339-379.
32. Johnson, K. P., and D. P. Byington. 1977. Subacute sclerosing panencephalitis: animal models, p. 511-515. In D. Schlessinger (ed.), Microbiology. American Society for Microbiology, Washington DC.
33. Katz, M., L. B. Rorke, W. S. Masland, G. B. Brodano, and H. Koprowski. 1970. Subacute sclerosing panencephalitis: isolation of a virus encephalitogenic for ferrets. J. Infect. Dis. 121:188-195.
34. Kobune, F., H. Sakata, and A. Sugiura. 1990. Marmoset lymphoblastoid cells as a sensitive host for isolation of measles virus. J. Virol. 64:700-705.
35. Lamb, R. A. 1993. Paramyxovirus fusion: a hypothesis for changes. Virology 197:1-11.
36. Lamb, R. A., and T. S. Jardetzky. 2007. Structural basis of viral invasion: lessons from paramyxovirus F. Curr. Opin. Struct. Biol. 17:427-436.
37. Lawrence, D. M., M. M. Vaughn, A. R. Belman, J. S. Cole, and G. F. Rall. 1999. Immune response-mediated protection of adult but not neonatal mice from neuron-restricted measles virus infection and central nervous system disease. J. Virol. 73:1795-1801.
38. Lawrence, D. M., C. E. Patterson, T. L. Gales, J. L. D'Orazio, M. M. Vaughn, and G. F. Rall. 2000. Measles virus spread between neurons requires cell contact but not CD46 expression, syncytium formation, or extracellular virus production. J. Virol. 74:1908-1918.
39. Lecouturier, V., J. Fayolle, M. Caballero, J. Carabana, M. L. Celma, R. Fernandez-Munoz, T. F. Wild, and R. Buckland. 1996. Identification of two amino acids in the hemagglutinin glycoprotein of measles virus (MV) that govern hemadsorption, HeLa cell fusion, and CD46 downregulation: phenotypic markers that differentiate vaccine and wild-type MV strains. J. Virol. 70:4200-4204. (Pubitemid 26187419)
40. Lemon, K., B. K. Rima, S. McQuaid, I. V. Allen, and W. P. Duprex. 2007. The F gene of rodent brain-adapted mumps virus is a major determinant of neurovirulence. J. Virol. 81:8293-8302.
41. Leonard, V. H. J., P. L. Sinn, G. Hodge, T. Miest, P. Devaux, N. Oezguen, W. Braun, P. B. McCray, Jr., M. B. McChesney, and R. Cattaneo. 2008. Measles virus blind to its epithelial cell receptor remains virulent in rhesus monkeys but cannot cross the airway epithelium and is not shed. J. Clin. Invest. 118:2448-2458.
42. Li, L., and Y. Qi. 2002. A novel amino acid position in hemagglutinin glycoprotein of measles virus is responsible for hemadsorption and CD46 binding. Arch. Virol. 147:775-786.
43. Makhortova, N., P. Askovich, C. E. Patterson, L. A. Gechman, N. P. Gerard, and G. F. Rall. 2007. Neurokinin-1 enables measles virus trans-synaptic spread in neurons. Virology 362:235-244.
44. Moeller-Ehrlich, K., M. Ludlow, R. Beschorner, R. Meyermann, B. K. Rima, W. P. Duprex, S. Niewiesk, and J. Schneider-Schaulies. 2007. Two functionally linked amino acids in the stem 2 region of measles virus haemagglutinin determine infectivity and virulence in the rodent central nervous system. J. Gen. Virol. 88:3112-3120.
45. Mrkic, B., J. Pavlovic, T. Rulicke, P. Volpe, C. J. Buchholz, D. Hourcade, J. P. Atkinson, A. Aguzzi, and R. Cattaneo. 1998. Measles virus spread and pathogenesis in genetically modified mice. J. Virol. 72:7420-7427.
46. Nielsen, L., M. Blixenkrone-Moller, M. Thylstrup, N. J. V. Hansen, and G. Bolt. 2001. Adaptation of wild-type measles virus to CD46 receptor usage. Arch. Virol. 146:197-208.
47. Ning, X., M. Ayata, M. Kimura, K. Komase, K. Furukawa, T. Seto, N. Ito, M. Shingai, I. Matusnaga, T. Yamano, and H. Ogura. 2002. Alterations and diversity in the cytoplasmic tail of the fusion protein of subacute sclerosing panencephalitis virus strains isolated in Osaka, Japan. Virus Res. 86:123-131.
48. Ogura, H., M. Ayata, K. Hayashi, T. Seto, O. Matsuoka, H. Hattori, K. Tanaka, K. Tanaka, Y. Takano, and R. Murata. 1997. Efficient isolation of subacute sclerosing panencephalitis virus from patient brains by reference to magnetic resonance and computed tomographic images. J. Neurovirol. 3:304-309. (Pubitemid 27389979)
49. Okada, H., M. Itoh, K. Nagata, and K. Takeuchi. 2009. Previously unrecognized amino acid substitutions in the hemagglutinin and fusion proteins of measles virus modulate cell-cell fusion, hemadsorption, virus growth, and penetration rate. J. Virol. 83:8713-8721.
50. Oldstone, M. B., H. Lewicki, D. Thomas, A. Tishon, S. Dales, J. Patterson, M. Manchester, D. Homann, D. Naniche, and A. Holz. 1999. Measles virus infection in a transgenic model: virus-induced immunosuppression and central nervous system disease. Cell 98:629-640.
51. Ono, N., H. Tatsuo, Y. Hidaka, T. Aoki, H. Minagawa, and Y. Yanagi. 2001. Measles viruses on throat swabs from measles patients use signaling lymphocytic activation molecule (CDw150) but not CD46 as a cellular receptor. J. Virol. 75:4399-4401.
52. Patterson, J. B., T. I. Cornu, J. Redwine, S. Dales, H. Lewicki, A. Holz, D. Thomas, M. A. Billeter, and M. B. Oldstone. 2001. Evidence that the hypermutated M protein of a subacute sclerosing panencephalitis measles virus actively contributes to the chronic progressive CNS disease. Virology 291:215-225.
53. Radecke, F., P. Spielhofer, H. Schneider, K. Kaelin, M. Huber, C. Dotsch, G. Christiansen, and M. A. Billeter. 1995. Rescue of measles viruses from cloned DNA. EMBO J. 14:5773-5784.
54. Richardson, C. D., A. Scheid, and P. W. Choppin. 1980. Specific inhibition of paramyxovirus and myxovirus replication by oligopeptides with amino acid sequences similar to those at the N-terminal of the F1 or HA2 viral polypeptides. Virology 105:205-222.
55. Richardson, C. D., and P. W. Choppin. 1983. Oligopeptides that specifically inhibit membrane fusion by paramyxoviruses: studies on the site of action. Virology 131:518-532.
56. Rima, B. K., J. A. P. Earle, K. Baczko, V. ter Meulen, U. G. Liebert, C. Carstens, J. Carabana, M. Caballero, M. L. Celma, and R. Fernandez-Munoz. 1997. Sequence divergence of measles virus haemagglutinin during natural evolution and adaptation to cell culture. J. Gen. Virol. 78:97-106.
57. Schmid, A., P. Spielhofer, R. Cattaneo, K. Baczko, V. ter Meulen, and M. A. Billeter. 1992. Subacute sclerosing panencephalitis is typically characterized by alterations in the fusion protein cytoplasmic domain of the persisting measles virus. Virology 188:910-915.
58. Schneider, H., P. Spielhofer, K. Kaelin, C. Dötsch, F. Radecke, G. Sutter, and M. A. Billeter. 1997. Rescue of measles virus using a replication-deficient vaccinia-T7 vector. J. Virol. Methods 64:57-64.
59. Schneider-Schaulies, J., V. ter Meulen, and S. Schneider-Schaulies. 2003. Measles infection of the central nervous system. J. Neurovirol. 9:247-252.
60. Sellin, C. I., N. Davoust, V. Guillaume, D. Baas, M. F. Belin, R. Buckland, T. F. Wild, and B. Horvat. 2006. High pathogenicity of wild-type measles virus infection in CD150 (SLAM) transgenic mice. J. Virol. 80:6420-6429.
61. Seto, T., M. Ayata, K. Hayashi, K. Furukawa, R. Murata, and H. Ogura. 1999. Different transcriptional expression of the matrix gene of the two sibling viruses of the subacute sclerosing panencephalitis virus (Osaka-2 strain) isolated from a biopsy specimen of patient brain. J. Neurovirol. 5:151-160. (Pubitemid 29187081)
62. Shibahara, K., H. Hotta, Y. Katayama, and M. Homma. 1994. Increased binding activity of measles virus to monkey red blood cells after long-term passage in Vero cell cultures. J. Gen. Virol. 75:3511-3516.
63. Shingai, M., M. Ayata, H. Ishida, I. Matsunaga, Y. Katayama, T. Seya, H. Tatsuo, Y. Yanagi, and H. Ogura. 2003. Receptor use by vesicular stomatitis virus pseudotypes with glycoproteins of defective variants of measles virus isolated from brains of patients with subacute sclerosing panencephalitis. J. Gen. Virol. 84:2133-2143.
64. Sugita, T., K. Shiraki, S. Ueda, N. Iwa, H. Shoji, M. Ayata, and S. Kato. 1984. Induction of acute myoclonic encephalopathy in hamsters by subacute sclerosing panencephalitis virus. J. Infect. Dis. 150:340-347.
65. Takeda, M., K. Takeuchi, N. Miyajima, F. Kobune, Y. Ami, N. Nagata, Y. Suzaki, Y. Nagai, and M. Tashiro. 2000. Recovery of pathogenic measles virus from cloned cDNA. J. Virol. 74:6643-6647.
66. Takeda, M., S. Ohno, F. Seki, K. Hashimoto, N. Miyajima, K. Takeuchi, and Y. Yanagi. 2005. Efficient rescue of measles virus from cloned cDNA using SLAM-expressing Chinese hamster ovary cells. Virus Res. 108:161-165.
67. Takeda, M., M. Tahara, T. Hashiguchi, T. A. Sato, F. Jinnouchi, S. Ueki, S. Ohno, and Y. Yanagi. 2007. A human lung carcinoma cell line supports efficient measles virus growth and syncytium formation via a SLAM- and CD46-independent mechanism. J. Virol. 81:12091-12096. (Pubitemid 47623842)
68. Takeuchi, K., N. Miyajima, N. Nagata, M. Takeda, and M. Tashiro. 2003. Wild-type measles virus induces large syncytium formation in primary human small airway epithelial cells by a SLAM(CD150)-independent mechanism. Virus Res. 94:11-16.
69. Tatsuo, H., N. Ono, K. Tanaka, and Y. Yanagi. 2000. SLAM (CDw150) is a cellular receptor for measles virus. Nature 406:893-897.
70. Thormar, H., K. Arnesen, and P. D. Mehta. 1977. Encephalitis in ferrets caused by a nonproductive strain of measles virus (D.R.) isolated from patient with subacute sclerosing panencephalitis. J. Infect. Dis. 136:229-238.