Altered interaction of the matrix protein with the cytoplasmic tail of hemagglutinin modulates measles virus growth by affecting virus assembly and cell-cell fusion

Journal of Virology

Volumn 81, Issue 13, 2007, Pages 6827-6836

  Tahara, Maino ^a   Takeda, Makoto ^a   Yanagi, Yusuke ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD150 ANTIGEN; CELL RECEPTOR; M PROTEIN; MATRIX PROTEIN; MEMBRANE COFACTOR PROTEIN; VIRUS HEMAGGLUTININ; VIRUS PROTEIN;

ADAPTATION; ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; CELL FUSION; CELL TYPE; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; MEASLES VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; VERO CELL; VIROGENESIS; VIRUS ASSEMBLY; VIRUS ATTENUATION; VIRUS CELL INTERACTION; VIRUS REPLICATION; VIRUS STRAIN;

ADAPTATION, PHYSIOLOGICAL; AMINO ACID SUBSTITUTION; ANIMALS; ANTIGENS, CD; ANTIGENS, CD46; CELL FUSION; CERCOPITHECUS AETHIOPS; HEMAGGLUTININS, VIRAL; HUMANS; MEASLES VACCINE; MEASLES VIRUS; MUTATION, MISSENSE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CELL SURFACE; VERO CELLS; VIRAL MATRIX PROTEINS; VIRUS REPLICATION;

MEASLES VIRUS;

EID: 34250844903     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00248-07     Document Type: Article

References (62)

1. Ali, A., and D. P. Nayak. 2000. Assembly of Sendai virus: M protein interacts with F and HN proteins and with the cytoplasmic tail and transmembrane domain of F protein. Virology 276:289-303.
2. Andres, O., K. Obojes, K. S. Kim, V. ter Meulen, and J. Schneider-Schaulies. 2003. CD46- and CD150-independent endothelial cell infection with wild-type measles viruses. J. Gen. Virol. 84:1189-1197.
3. Ballart, I., D. Eschle, R. Cattaneo, A. Schmid, M. Metzler, J. Chan, S. Pifko-Hirst, S. A. Udem, and M. A. Billeter. 1990. Infectious measles virus from cloned cDNA. EMBO J. 9:379-384.
4. 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.
5. Cathomen, T., H. Y. Nairn, and R. Cattaneo. 1998. Measles viruses with altered envelope protein cytoplasmic tails gain cell fusion competence. J. Virol. 72:1224-1234.
6. Cattaneo, R., and J. K. Rose. 1993. Cell fusion by the envelope glycoproteins of persistent measles viruses which caused lethal human brain disease. J. Virol. 67:1493-1502.
7. Coronel, E. C., T. Takimoto, K. G. Murti, N. Varich, and A. Portner. 2001. Nucleocapsid incorporation into parainfluenza virus is regulated by specific interaction with matrix protein. J. Virol. 75:1117-1123.
8. Dolganiuc, V., L. McGinnes, E. J. Luna, and T. G. Morrison. 2003. Role of the cytoplasmic domain of the Newcastle disease virus fusion protein in association with lipid rafts. J. Virol. 77:12968-12979.
9. Fouillot-Coriou, N., and L. Roux. 2000. Structure-function analysis of the Sendai virus F and HN cytoplasmic domain: different role for the two proteins in the production of virus particle. Virology 270:464-475.
10. Fuerst, T. R., E. G. Niles, F. W. Studier, and B. Moss. 1986. Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc. Natl. Acad. Sci. USA 83:8122-8126.
11. Ghildyal, R., D. Li, I. Peroulls, B. Shields, P. G. Bardin, M. N. Teng, P. L. Collins, J. Meanger, and J. Mills. 2005. Interaction between the respiratory syncytial virus G glycoprotein cytoplasmic domain and the matrix protein. J. Gen. Virol. 86:1879-1884.
12. Griffin, D. E. 2001. Measles virus, p. 1401-1441. 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, 4th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
13. Hashimoto, K., N. Ono, H. Tatsuo, H. Minagawa, M. Takeda, K. Takeuchi, and Y. Yanagi. 2002. SLAM (CD150)-independent measles virus entry as revealed by recombinant virus expressing green fluorescent protein. J. Virol. 76:6743-6749.
14. Henis, Y. I., Y. Herman-Barhom, B. Aroeti, and O. Gutman. 1989. Lateral mobility of both envelope proteins (F and HN) of Sendai virus in the cell membrane is essential for cell-cell fusion. J. Biol. Chem. 264:17119-17125.
15. Hirano, A., M. Ayata, A. H. Wang, and T. C. Wong. 1993. Functional analysis of matrix proteins expressed from cloned genes of measles virus variants that cause subacute sclerosing panencephalitis reveals a common defect in nucleocapsid binding. J. Virol. 67:1848-1853.
16. Huber, M., R. Cattaneo, P. Spielhofer, C. Orvell, E. Norrby, M. Messerli, J. C. Perriard, and M. A. Billeter. 1991. Measles virus phosphoprotein retains the nucleocapsid protein in the cytoplasm. Virology 185:299-308.
17. Januszeski, M. M., P. M. Cannon, D. Chen, Y. Rozenberg, and W. F. Anderson. 1997. Functional analysis of the cytoplasmic tail of Moloney murine leukemia virus envelope protein. J. Virol. 71:3613-3619.
18. Jin, H., G. P. Leser, J. Zhang, and R. A. Lamb. 1997. Influenza virus hemagglutinin and neuraminidase cytoplasmic tails control particle shape. EMBO J. 16:1236-1247.
19. Kashiwakuma, T., A. Hasegawa, T. Kajita, A. Takata, H. Mori, Y. Ohta, E. Tanaka, K. Kiyosawa, T. Tanaka, S. Tanaka, N. Hattori, and M. Kohara. 1996. Detection of hepatitis C virus specific core protein in serum of patients by a sensitive fluorescence enzyme immunoassay (FEIA). J. Immunol. Methods 190:79-89.
20. 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.
21. Kobune, F., H. Takahashi, K. Terao, T. Ohkawa, Y. Ami, Y. Suzaki, N. Nagata, H. Sakata, K. Yamanouchi, and C. Kai. 1996. Nonhuman primate models of measles. Lab. Anim. Sci. 46:315-320.
22. Kouomou, D. W., and T. F. Wild. 2002. Adaptation of wild-type measles virus to tissue culture. J. Virol. 76:1505-1509.
23. Markwell, M. A., and C. F. Fox. 1980. Protein-protein interactions within paramyxoviruses identified by native disulfide bonding or reversible chemical cross-linking. J. Virol. 33:152-166.
24. Mitnaul, L. J., M. R. Castrucci, K. G. Murti, and Y. Kawaoka. 1996. The cytoplasmic tail of influenza A virus neuraminidase (NA) affects NA incorporation into virions, virion morphology, and virulence in mice but is not essential for virus replication. J. Virol. 70:873-879.
25. Moll, M., H. D. Klenk, and A. Maisner. 2002. Importance of the cytoplasmic tails of the measles virus glycoproteins for fusogenic activity and the generation of recombinant measles viruses. J. Virol. 76:7174-7186.
26. Naim, H. Y., E. Ehler, and M. A. Billeter. 2000. Measles virus matrix protein specifies apical virus release and glycoprotein sorting in epithelial cells. EMBO J. 19:3576-3585.
27. Nakatsu, Y., M. Takeda, M. Kidokoro, M. Kohara, and Y. Yanagi. 2006. Rescue system for measles virus from cloned cDNA driven by vaccinia virus Lister vaccine strain. J. Virol. Methods 137:152-155.
28. Nakatsu, Y., M. Takeda, S. Ohno, R. Koga, and Y. Yanagi. 2006. Translational inhibition and increased interferon induction in cells infected with a C protein-deficient measles virus. J. Virol. 80:11861-11867.
29. Niwa, H., K. Yamamura, and J. Miyazaki. 1991. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108:193-199.
30. Nussbaum, O., C. C. Broder, and E. A. Berger. 1994. Fusogenic mechanisms of enveloped-virus glycoproteins analyzed by a novel recombinant vaccinia virus-based assay quantitating cell fusion-dependent reporter gene activation. J. Virol. 68:5411-5422.
31. 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.
32. Parks, C. L., R. A. Lerch, P. Walpita, H. P. Wang, M. S. Sidhu, and S. A. Udem. 2001. Comparison of predicted amino acid sequences of measles virus strains in the Edmonston vaccine lineage. J. Virol. 75:910-920.
33. Paterson, R. G., and R. A. Lamb. 1993. The molecular biology of influenza viruses and paramyxoviruses, p. 35-73. In A. Davidson and R. M. Elliott (ed.), Molecular virology: a practical approach. IRL Oxford University Press, Oxford, United Kingdom.
34. Piller, S. C., J. W. Dubay, C. A. Derdeyn, and E. Hunter. 2000. Mutational analysis of conserved domains within the cytoplasmic tail of gp41 from human immunodeficiency virus type 1: effects on glycoprotein incorporation and infectivity. J. Virol. 74:11717-11723.
35. Plemper, R. K., A. L. Hammond, D. Gerlier, A. K. Fielding, and R. Cattaneo. 2002. Strength of envelope protein interaction modulates cytopathicity of measles virus. J. Virol. 76:5051-5061.
36. 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.
37. 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-termini of the F1 or HA2 viral polypeptides. Virology 105:205-222.
38. Rota, J. S., Z. D. Wang, P. A. Rota, and W. J. Bellini. 1994. Comparison of sequences of the H, F, and N coding genes of measles virus vaccine strains. Virus Res. 31:317-330.
39. Santos, P. R., M. L. Azevedo, M. B. Borges, M. S. Freire, J. P. Nascimento, and M. T. Moraes. 2003. Comparative sequence analysis of the P-, M- and L-coding region of the measles virus CAM-70 live attenuated vaccine strain. Braz. J. Med. Biol. Res. 36:1475-1484.
40. Schmitt, A. P., B. He, and R. A. Lamb. 1999. Involvement of the cytoplasmic domain of the hemagglutinin-neuraminidase protein in assembly of the paramyxovirus simian virus 5. J. Virol. 73:8703-8712.
41. Schmitt, A. P., and R. A. Lamb. 2004. Escaping from the cell: assembly and budding of negative-strand RNA viruses. Curr. Top. Microbiol. Immunol. 283:145-196.
42. Schmitt, A. P., G. P. Leser, D. L. Waning, and R. A. Lamb. 2002. Requirements for budding of paramyxovirus simian virus 5 virus-like particles. J. Virol. 76:3952-3964.
43. Spielhofer, P., T. Bachi, T. Fehr, G. Christiansen, R. Cattaneo, K. Kaelin, M. A. Billeter, and H. Y. Naim. 1998. Chimeric measles viruses with a foreign envelope. J. Virol. 72:2150-2159.
44. Tahara, M., M. Takeda, F. Seki, T. Hashiguchi, and Y. Yanagi. 2007. Multiple amino acid substitutions in hemagglutinin are necessary for wild-type measles virus to acquire the ability to use receptor CD46 efficiently. J. Virol. 81:2564-2572.
45. Tahara, M., M. Takeda, and Y. Yanagi. 2005. Contributions of matrix and large protein genes of the measles virus Edmonston strain to growth in cultured cells as revealed by recombinant viruses. J. Virol. 79:15218-15225.
46. Takeda, M., A. Kato, F. Kobune, H. Sakata, Y. Li, T. Shioda, Y. Sakai, M. Asakawa, and Y. Nagai. 1998. Measles virus attenuation associated with transcriptional impediment and a few amino acid changes in the polymerase and accessory proteins. J. Virol. 72:8690-8696.
47. 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.
48. Takeda, M., S. Ohno, F. Seki, Y. Nakatsu, M. Tahara, and Y. Yanagi. 2005. Long untranslated regions of the measles virus M and F genes control virus replication and cytopathogenicity. J. Virol. 79:14346- 14354.
49. 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.
50. Takeuchi, K., N. Miyajima, F. Kobune, and M. Tashiro. 2000. Comparative nucleotide sequence analysis of the entire genomes of B95a cell-isolated and Vero cell-isolated measles viruses from the same patient. Virus Genes 20: 253-257.
51. Takimoto, T., T. Bousse, E. C. Coronel, R. A. Scroggs, and A. Portner. 1998. Cytoplasmic domain of Sendai virus HN protein contains a specific sequence required for its incorporation into virions. J. Virol. 72:9747-9754.
52. Tao, T., M. H. Skiadopoulos, F. Davoodi, J. M. Riggs, P. L. Collins, and B. R. Murphy. 2000. Replacement of the ectodomains of the hemagglutinin-neuraminidase and fusion glycoproteins of recombinant parainfluenza virus type 3 (PIV3) with their counterparts from PIV2 yields attenuated PIV2 vaccine candidates. J. Virol. 74:6448-6458.
53. Tatsuo, H., N. Ono, K. Tanaka, and Y. Yanagi. 2000. SLAM (CDw150) is a cellular receptor for measles virus. Nature 406:893-897.
54. Waning, D. L., C. J. Russell, T. S. Jardetzky, and R. A. Lamb. 2004. Activation of a paramyxovirus fusion protein is modulated by inside-out signaling from the cytoplasmic tail. Proc. Natl. Acad. Sci. USA 101:9217-9222.
55. Waning, D. L., A. P. Schmitt, G. P. Leser, and R. A. Lamb. 2002. Roles for the cytoplasmic tails of the fusion and hemagglutinin-neuraminidase proteins in budding of the paramyxovirus simian virus 5. J. Virol. 76: 9284-9297.
56. Whitt, M. A., L. Chong, and J. K. Rose. 1989. Glycoprotein cytoplasmic domain sequences required for rescue of a vesicular stomatitis virus glycoprotein mutant. J. Virol. 63:3569-3578.
57. Wild, T. F., E. Malvoisin, and R. Buckland. 1991. Measles virus: both the haemagglutinin and fusion glycoproteins are required for fusion. J. Gen. Virol. 72:439-442.
58. Wyatt, L. S., B. Moss, and S. Rozenblatt. 1995. Replication-deficient vaccinia virus encoding bacteriophage T7 RNA polymerase for transient gene expression in mammalian cells. Virology 210:202-205.
59. Yanagi, Y., M. Takeda, and S. Ohno. 2006. Measles virus: cellular receptors, tropism and pathogenesis. J. Gen. Virol. 87:2767-2779.
60. Yanagi, Y., M. Takeda, S. Ohno, and F. Seki. 2006. Measles virus receptors and tropism. Jpn. J. Infect. Dis. 59:1-5.
61. Yasui, K., T. Wakita, K. Tsukiyama-Kohara, S. I. Funahashi, M. Ichikawa, T. Kajita, D. Moradpour, J. R. Wands, and M. Kohara. 1998. The native form and maturation process of hepatitis C virus core protein. J. Virol. 72:6048-6055.
62. Zhang, J., A. Pekosz, and R. A. Lamb. 2000. Influenza virus assembly and lipid raft microdomains: a role for the cytoplasmic tails of the spike glycoproteins. J. Virol. 74:4634-4644.