The measles virus fusion protein transmembrane region modulates availability of an active glycoprotein complex and fusion efficiency

Journal of Virology

Volumn 82, Issue 22, 2008, Pages 11437-11445

  Mühlebach, Michael D ^a,b   Leonard, Vincent H J ^a   Cattaneo, Roberto ^a  

^a MAYO CLINIC   (United States)

^b PAUL EHRLICH INSTITUT   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ENVELOPE PROTEIN; HEMAGGLUTININ; VIRUS FUSION PROTEIN; VIRUS GLYCOPROTEIN; VIRUS RECEPTOR;

ANIMAL CELL; ARTICLE; CELL SURFACE; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; LIPID BILAYER; MEASLES VIRUS; MEMBRANE FUSION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR BINDING; VERO CELL; VIRUS RECOMBINANT; AMINO ACID SUBSTITUTION; ANIMAL; CERCOPITHECUS; GENETICS; METABOLISM; PHYSIOLOGY; SITE DIRECTED MUTAGENESIS; VIRUS ATTACHMENT; VIRUS ENTRY;

MEASLES VIRUS;

AMINO ACID SUBSTITUTION; ANIMALS; CERCOPITHECUS AETHIOPS; HEMAGGLUTININS; MEASLES VIRUS; MUTAGENESIS, SITE-DIRECTED; RECEPTORS, VIRUS; VERO CELLS; VIRAL FUSION PROTEINS; VIRUS ATTACHMENT; VIRUS INTERNALIZATION;

EID: 55549088556     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00779-08     Document Type: Article

References (52)

1. Bolt, G., and I. R. Pedersen. 1998. The role of subtilisin-like proprotein convertases for cleavage of the measles virus fusion glycoprotein in different cell types. Virology 252:387-398.
2. Bossart, K. N., L. F. Wang, M. N. Flora, K. B. Chua, S. K. Lam, B. T. Eaton, and C. C. Broder. 2002. Membrane fusion tropism and heterotypic functional activities of the Nipah virus and Hendra virus envelope glycoproteins. J. Virol. 76:11186-11198.
3. Caballero, M., J. Carabana, J. Ortego, R. Fernandez-Munoz, and M. L. Celma. 1998. Measles virus fusion protein is palmitoylated on transmembrane-intracytoplasmic cysteine residues which participate in cell fusion. J. Virol. 72:8198-8204.
4. Calain, P., and L. Roux. 1993. The rule of six, a basic feature for efficient replication of Sendai virus defective interfering RNA. J. Virol. 67:4822-4830.
5. Cathomen, T., C. J. Buchholz, P. Spielhofer, and R. Cattaneo. 1995. Preferential initiation at the second AUG of the measles virus F mRNA: a role for the long untranslated region. Virology 214:628-632.
6. 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.
7. 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.
8. Cattaneo, R., and J. K. Rose. 1993. Cell fusion by the envelope glycoproteins of persistent measles viruses which causes lethal human brain disease. J. Virol. 67:1493-1502.
9. Cleverley, D. Z., and J. Lenard. 1998. The transmembrane domain in viral fusion: essential role for a conserved glycine residue in vesicular stomatitis virus G protein. Proc. Natl. Acad. Sci. USA 95:3425-3430.
10. Colf, L. A., Z. S. Juo, and K. C. Garcia. 2007. Structure of the measles virus hemagglutinin. Nat. Struct. Mol. Biol. 14:1227-1228.
11. Corey, E. A., and R. M. Iorio. 2007. Mutations in the stalk of the measles virus hemagglutinin protein decrease fusion but do not interfere with virus-specific interaction with the homologous fusion protein. J. Virol. 81:9900-9910.
12. Cuff, J. A., M. E. Clamp, A. S. Siddiqui, M. Finlay, and G. J. Barton. 1998. JPred: a consensus secondary structure prediction server. Bioinformatics 14:892-893.
13. Dennison, S. M., N. Greenfield, J. Lenard, and B. R. Lentz. 2002. VSV transmembrane domain (TMD) peptide promotes PEG-mediated fusion of liposomes in a conformationally sensitive fashion. Biochemistry 41:14925-14934.
14. de Swart, R. L., M. Ludlow, L. de Witte, Y. Yanagi, G. van Amerongen, S. McQuaid, S. Yuksel, T. B. Geijtenbeek, W. P. Duprex, and A. D. Osterhaus. 2007. Predominant infection of CD150+ lymphocytes and dendritic cells during measles virus infection of macaques. PLoS Pathog. 3:e178.
15. Devaux, P., V. von Messling, W. Songsungthong, C. Springfeld, and R. Cattaneo. 2007. Tyrosine 110 in the measles virus phosphoprotein is required to block STAT1 phosphorylation. Virology 360:72-83.
16. Dorig, R. E., A. Marcil, A. Chopra, and C. D. Richardson. 1993. The human CD46 molecule is a receptor for measles virus (Edmonston strain). Cell 75:295-305.
17. Hashiguchi, T., M. Kajikawa, N. Maita, M. Takeda, K. Kuroki, K. Sasaki, D. Kohda, Y. Yanagi, and K. Maenaka. 2007. Crystal structure of measles virus hemagglutinin provides insight into effective vaccines. Proc. Natl. Acad. Sci. USA 104:19535-19540.
18. Herschke, F., S. Plumet, T. Duhen, O. Azocar, J. Druelle, D. Laine, T. F. Wild, C. Rabourdin-Combe, D. Gerlier, and H. Valentin. 2007. Cell-cell fusion induced by measles virus amplifies the type I interferon response. J. Virol. 81:12859-12871.
19. Hofmann, M. W., K. Weise, J. Ollesch, P. Agrawal, H. Stalz, W. Stelzer, F. Hulsbergen, H. de Groot, K. Gerwert, J. Reed, and D. Langosch. 2004. De novo design of conformationally flexible transmembrane peptides driving membrane fusion. Proc. Natl. Acad. Sci. USA 101:14776-14781.
20. 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.
21. Kärber, G. 1931. Beitrag zur kollektiven Behandlung pharmakologischer Reihenversuche. Arch. Exp. Pathol. Pharmakol. 162:480-483.
22. Kemble, G. W., T. Danieli, and J. M. White. 1994. Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell 76:383-391.
23. Kneller, D. G., F. E. Cohen, and R. Langridge. 1990. Improvements in protein secondary structure prediction by an enhanced neural network. J. Mol. Biol. 214:171-182.
24. Langosch, D., B. Brosig, and R. Pipkorn. 2001. Peptide mimics of the vesicular stomatitis virus G-protein transmembrane segment drive membrane fusion in vitro. J. Biol. Chem. 276:32016-32021.
25. Langosch, D., J. M. Crane, B. Brosig, A. Hellwig, L. K. Tamm, and J. Reed. 2001. Peptide mimics of SNARE transmembrane segments drive membrane fusion depending on their conformational plasticity. J. Mol. Biol. 311:709-721.
26. Leonard, V. H. U., P. L. Sinn, G. Hodge, T. Miest, P. Devaux, N. Oezguen, W. Braun, P. B. McCray, 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. Investig. 118:2448-2458.
27. Lindwasser, O. W., and M. D. Resh. 2001. Multimerization of human immunodeficiency virus type 1 Gag promotes its localization to barges, raft-like membrane microdomains. J. Virol. 75:7913-7924.
28. Maisner, A., B. Mrkic, G. Herrler, M. Moll, M. A. Billeter, R. Cattaneo, and H. D. Klenk. 2000. Recombinant measles virus requiring an exogenous protease for activation of infectivity. J. Gen. Virol. 81:441-449.
29. McChesney, M. B., C. J. Miller, P. A. Rota, Y. D. Zhu, L. Antipa, N. W. Lerche, R. Ahmed, and W. J. Bellini. 1997. Experimental measles. I. Pathogenesis in the normal and the immunized host. Virology 233:74-84.
30. Melikyan, G. B., R. M. Markosyan, M. G. Roth, and F. S. Cohen. 2000. A point mutation in the transmembrane domain of the hemagglutinin of influenza virus stabilizes a hemifusion intermediate that can transit to fusion. Mol. Biol. Cell 11:3765-3775.
31. Murphy, S. K., and G. D. Parks. 1997. Genome nucleotide lengths that are divisible by six are not essential but enhance replication of defective interfering RNAs of the paramyxovirus simian virus 5. Virology 232:145-157.
32. Naniche, D., G. Varior-Krishnan, F. Cervoni, T. F. Wild, B. Rossi, C. Rabourdin-Combe, and D. Gerlier. 1993. Human membrane cofactor protein (CD46) acts as a cellular receptor for measles virus. J. Virol. 67:6025-6032.
33. Navaratnarajah, C. K., V. H. U. Leonard, and R. Cattaneo. 2009. Measles virus: glycoprotein complex assembly, receptor attachment, and cell entry. Curr. Top. Microbiol. Immunol. 329:57-74.
34. Navaratnarajah, C. K., S. Vongpunsawad, N. Oezguen, T. Stehle, W. Braun, T. Hashiguchi, K. Maenaka, Y. Yanagi, and R. Cattaneo. 2008. Dynamic interaction of the measles virus hemagglutinin with its receptor SLAM. J. Biol. Chem. 283:11763-11771.
35. 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.
36. Paterson, R. G., M. L. Johnson, and R. A. Lamb. 1997. Paramyxovirus fusion (F) protein and hemagglutinin-neuraminidase (HN) protein interactions: intracellular retention of F and HN does not affect transport of the homotypic HN or F protein. Virology 237:1-9.
37. Plemper, R. K., A. L. Hammond, and R. Cattaneo. 2000. Characterization of a region of the measles virus hemagglutinin sufficient for its dimerization. J. Virol. 74:6485-6493.
38. Plemper, R. K., A. L. Hammond, and R. Cattaneo. 2001. Measles virus envelope glycoproteins hetero-oligomerize in the endoplasmic reticulum. J. Biol. Chem. 276:44239-44246.
39. 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.
40. 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.
41. Richardson, C., D. Hull, P. Greer, K. Hasel, A. Berkovich, G. Englund, W. Bellini, B. Rima, and R. Lazzarini. 1986. The nucleotide sequence of the mRNA encoding the fusion protein of measles virus (Edmonston strain): a comparison of fusion proteins from several different paramyxoviruses. Virology 155:508-523.
42. Sutter, G., M. Ohlmann, and V. Erfle. 1995. Non-replicating vaccinia vector efficiently expresses bacteriophage T7 RNA polymerase. FEBS Lett. 371:9-12.
43. Tahara, M., M. Takeda, and Y. Yanagi. 2007. Altered interaction of the matrix protein with the cytoplasmic tail of hemagglutinin modulates measles virus growth by affecting virus assembly and cell-cell fusion. J. Virol. 81: 6827-6836.
44. Takeda, M., G. P. Leser, C. J. Russell, and R. A. Lamb. 2003. Influenza virus hemagglutinin concentrates in lipid raft microdomains for efficient viral fusion. Proc. Natl. Acad. Sci. USA 100:14610-14617.
45. 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.
46. Tatsuo, H., N. Ono, K. Tanaka, and Y. Yanagi. 2000. SLAM (CDw150) is a cellular receptor for measles virus. Nature 406:893-897.
47. Tomita, Y., T. Yamashita, H. Sato, and H. Taira. 1999. Kinetics of interactions of Sendai virus envelope glycoproteins, F and HN, with endoplasmic reticulum-resident molecular chaperones, BiP, calnexin, and calreticulin. J. Biochem. 126:1090-1100.
48. Vincent, S., D. Gerlier, and S. N. Manie. 2000. Measles virus assembly within membrane rafts. J. Virol. 74:9911-9915.
49. 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.
50. Watanabe, M., A. Hirano, S. Stenglein, J. Nelson, G. Thomas, and T. C. Wong. 1995. Engineered serine protease inhibitor prevents furin-catalyzed activation of the fusion glycoprotein and production of infectious measles virus. J. Virol. 69:3206-3210.
51. Yao, Q., X. Hu, and R. W. Compans. 1997. Association of the parainfluenza virus fusion and hemagglutinin-neuraminidase glycoproteins on cell surfaces. J. Virol. 71:650-656.
52. Yin, H. S., X. Wen, R. G. Paterson, R. A. Lamb, and T. S. Jardetzky. 2006. Structure of the parainfluenza virus 5 F protein in its metastable, prefusion conformation. Nature 439:38-44.