A stabilized headless measles virus attachment protein stalk efficiently triggers membrane fusion

Journal of Virology

Volumn 87, Issue 21, 2013, Pages 11693-11703

  Brindley, Melinda A ^a   Schestak, Isabel ^a   Suter, Rolf ^a   Kiss, Gabriella ^b   Wright, Elizabeth R ^b   Plemper, Richard K ^a,b  

^a GEORGIA STATE UNIVERSITY   (United States)

^b CHILDREN'S HEALTHCARE OF ATLANTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATTACHMENT PROTEIN; UNCLASSIFIED DRUG; VIRUS FUSION PROTEIN; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; MEASLES VIRUS; MEMBRANE FUSION; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; VIRUS PARTICLE; VIRUS VIABILITY;

ANIMALS; CELL LINE; MEASLES VIRUS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; SEQUENCE DELETION; VIRAL FUSION PROTEINS; VIRAL PROTEINS; VIRUS INTERNALIZATION;

EID: 84886927744     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01945-13     Document Type: Article

References (57)

1. Lamb RA, Parks GD. 2007. Paramyxoviridae: the viruses and their replication, p 1449-1496. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed, vol 1. Lippincott Williams & Wilkins, Philadelphia, PA.
2. Taylor G. 1996. Sialidases: structures, biological significance and therapeutic potential. Curr. Opin. Struct. Biol. 6:830-837.
3. Bowden TA, Aricescu AR, Gilbert RJ, Grimes JM, Jones EY, Stuart DI. 2008. Structural basis of Nipah and Hendra virus attachment to their cell-surface receptor ephrin-B2. Nat. Struct. Mol. Biol. 15:567-572.
4. Hashiguchi T, Ose T, Kubota M, Maita N, Kamishikiryo J, Maenaka K, Yanagi Y. 2011. Structure of the measles virus hemagglutinin bound to its cellular receptor SLAM. Nat. Struct. Mol. Biol. 18:135-141.
5. Lawrence MC, Borg NA, Streltsov VA, Pilling PA, Epa VC, Varghese JN, McKimm-Breschkin JL, Colman PM. 2004. Structure of the haemagglutinin-neuraminidase from human parainfluenza virus type III. J. Mol. Biol. 335:1343-1357.
6. Santiago C, Celma ML, Stehle T, Casasnovas JM. 2010. Structure of the measles virus hemagglutinin bound to the CD46 receptor. Nat. Struct. Mol. Biol. 17:124-129.
7. Xu K, Rajashankar KR, Chan YP, Himanen JP, Broder CC, Nikolov DB. 2008. Host cell recognition by the henipaviruses: crystal structures of the Nipah G attachment glycoprotein and its complex with ephrin-B3. Proc. Natl. Acad. Sci. U. S. A. 105:9953-9958.
8. Yuan P, Thompson TB, Wurzburg BA, Paterson RG, Lamb RA, Jardetzky TS. 2005. Structural studies of the parainfluenza virus 5 hemagglutinin-neuraminidase tetramer in complex with its receptor, sialyllactose. Structure 13:803-815.
9. Zhang X, Lu G, Qi J, Li Y, He Y, Xu X, Shi J, Zhang CW, Yan J, Gao GF. 2013. Structure of measles virus hemagglutinin bound to its epithelial receptor nectin-4. Nat. Struct. Mol. Biol. 20:67-72.
10. Plattet P, Plemper RK. 2013. Envelope protein dynamics in paramyxovirus entry. mBio 4:e00413-13. doi:10.1128/mBio.00413-13.
11. Brindley MA, Plemper RK. 2010. Blue native PAGE and biomolecular complementation reveal a tetrameric or higher-order oligomer organization of the physiological measles virus attachment protein H. J. Virol. 84:12174-12184.
12. Yuan P, Swanson KA, Leser GP, Paterson RG, Lamb RA, Jardetzky TS. 2011. Structure of the Newcastle disease virus hemagglutininneuraminidase (HN) ectodomain reveals a four-helix bundle stalk. Proc. Natl. Acad. Sci. U. S. A. 108:14920-14925.
13. Bose S, Welch BD, Kors CA, Yuan P, Jardetzky TS, Lamb RA. 2011. Structure and mutagenesis of the parainfluenza virus 5 hemagglutininneuraminidase stalk domain reveals a four-helix bundle and the role of the stalk in fusion promotion. J. Virol. 85:12855-12866.
14. Brindley MA, Takeda M, Plattet P, Plemper RK. 2012. Triggering the measles virus membrane fusion machinery. Proc. Natl. Acad. Sci. U. S. A. 109:E3018-E3027.
15. Ader N, Brindley MA, Avila M, Origgi FC, Langedijk JP, Orvell C, Vandevelde M, Zurbriggen A, Plemper RK, Plattet P. 2012. Structural rearrangements of the central region of the morbillivirus attachment protein stalk domain trigger F protein refolding for membrane fusion. J. Biol. Chem. 287:16324-16334.16
16. Paal T, Brindley MA, St Clair C, Prussia A, Gaus D, Krumm SA, Snyder JP, Plemper RK. 2009. Probing the spatial organization of measles virus fusion complexes. J. Virol. 83:10480-10493.
17. Deng R, Mirza AM, Mahon PJ, Iorio RM. 1997. Functional chimeric HN glycoproteins derived from Newcastle disease virus and human parainfluenza virus-3. Arch. Virol. Suppl. 13:115-130.
18. Hu XL, Ray R, Compans RW. 1992. Functional interactions between the fusion protein and hemagglutinin-neuraminidase of human parainfluenza viruses. J. Virol. 66:1528-1534.
19. Morrison T, McQuain C, McGinnes L. 1991. Complementation between avirulent Newcastle disease virus and a fusion protein gene expressed from a retrovirus vector: requirements for membrane fusion. J. Virol. 65:813-822.
20. Lamb RA, Paterson RG, Jardetzky TS. 2006. Paramyxovirus membrane fusion: lessons from the F andHNatomic structures. Virology 344:30-37.
21. Plemper RK. 2011. Cell entry of enveloped viruses. Curr. Opin. Virol. 1:92-100.
22. Lee JK, Prussia A, Paal T, White LK, Snyder JP, Plemper RK. 2008. Functional interaction between paramyxovirus fusion and attachment proteins. J. Biol. Chem. 283:16561-16572.
23. Tanabayashi K, Compans RW. 1996. Functional interaction of paramyxovirus glycoproteins: identification of a domain in Sendai virus HN which promotes cell fusion. J. Virol. 70:6112-6118.
24. Tsurudome M, Kawano M, Yuasa T, Tabata N, Nishio M, Komada H, Ito Y. 1995. Identification of regions on the hemagglutininneuraminidase protein of human parainfluenza virus type 2 important for promoting cell fusion. Virology 213:190-203.
25. Deng R, Wang Z, Mirza AM, Iorio RM. 1995. Localization of a domain on the paramyxovirus attachment protein required for the promotion of cellular fusion by its homologous fusion protein spike. Virology 209:457-469.
26. Apte-Sengupta S, Negi S, Leonard VH, Oezguen N, Navaratnarajah CK, Braun W, Cattaneo R. 2012. Base of the measles virus fusion trimer head receives the signal that triggers membrane fusion. J. Biol. Chem. 287: 33026-33035.
27. Bose S, Zokarkar A, Welch BD, Leser GP, Jardetzky TS, Lamb RA. 2012. Fusion activation by a headless parainfluenza virus 5 hemagglutininneuraminidase stalk suggests a modular mechanism for triggering. Proc. Natl. Acad. Sci. U. S. A. 109:E2625-E2634.
28. Plemper RK, Hammond AL, Cattaneo R. 2000. Characterization of a region of the measles virus hemagglutinin sufficient for its dimerization. J. Virol. 74:6485-6493.
29. Plemper RK, Brindley MA, Iorio RM. 2011. Structural and mechanistic studies of measles virus illuminate paramyxovirus entry. PLoS Pathog. 7:e1002058. doi:10.1371/journal.ppat.1002058.
30. Plemper RK, Hammond AL, Gerlier D, Fielding AK, Cattaneo R. 2002. Strength of envelope protein interaction modulates cytopathicity of measles virus. J. Virol. 76:5051-5061.
31. Plemper RK, Hammond AL, Cattaneo R. 2001. Measles virus envelope glycoproteins hetero-oligomerize in the endoplasmic reticulum. J. Biol. Chem. 276:44239-44246.
32. Plattet P, Langedijk JP, Zipperle L, Vandevelde M, Orvell C, Zurbriggen A. 2009. Conserved leucine residue in the head region of morbillivirus fusion protein regulates the large conformational change during fusion activity. Biochemistry 48:9112-9121.
33. 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.
34. Ono N, Tatsuo H, Hidaka Y, Aoki T, Minagawa H, Yanagi Y. 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.
35. Seki F, Ono N, Yamaguchi R, Yanagi Y. 2003. Efficient isolation of wild strains of canine distemper virus in Vero cells expressing canine SLAM (CD150) and their adaptability to marmoset B95a cells. J. Virol. 77:9943-9950.
36. Wyss-Fluehmann G, Zurbriggen A, Vandevelde M, Plattet P. 2010. Canine distemper virus persistence in demyelinating encephalitis by swift intracellular cell-to-cell spread in astrocytes is controlled by the viral attachment protein. Acta Neuropathol. 119:617-630.
37. Doyle J, Prussia A, White LK, Sun A, Liotta DC, Snyder JP, Compans RW, Plemper RK. 2006. Two domains that control prefusion stability andtransport competence of the measles virus fusion protein. J. Virol. 80: 1524-1536.
38. Singh M, Billeter MA. 1999. A recombinant measles virus expressing biologically active human interleukin-12. J. Gen. Virol. 80(Pt 1):101-106.
39. Duprex WP, McQuaid S, Roscic-Mrkic B, Cattaneo R, McCallister C, Rima BK. 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.
40. Mastronarde DN. 2005. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152: 36-51.
41. Kremer JR, Mastronarde DN, McIntosh JR. 1996. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116:71-76.
42. Heymann JB. 2001. Bsoft: image and molecular processing in electron microscopy. J. Struct. Biol. 133:156-169.
43. Plemper RK, Compans RW. 2003. Mutations in the putative HR-C region of the measles virus F2 glycoprotein modulate syncytium formation. J. Virol. 77:4181-4190.
44. Deng R, Mirza AM, Mahon PJ, Iorio RM. 1997. Functional chimeric HN glycoproteins derived from Newcastle disease virus and human parainfluenza virus-3. Arch. Virol. Suppl. 13:115-130.
45. Zwietering MH, Jongenburger I, Rombouts FM, van 't Riet K. 1990. Modeling of the bacterial growth curve. Appl. Environ. Microbiol. 56: 1875-1881.
46. Rodgers JL, Nicewander WA. 1988. Thirteen ways to look at the correlation coefficient. Am. Stat. 42:59-66.
47. Pearson K. 1895. Note on regression and inheritance in the case of two parents. Proc. R. Soc. London 58:240-242.
48. Tahara M, Ito Y, Brindley MA, Ma X, He J, Xu S, Fukuhara H, Sakai K, Komase K, Rota PA, Plemper RK, Maenaka K, Takeda M. 2013.Functional and structural characterization of neutralizing epitopes of measles virus hemagglutinin protein. J. Virol. 87:666-675.
49. Liljeroos L, Huiskonen JT, Ora A, Susi P, Butcher SJ. 2011. Electron cryotomography of measles virus reveals how matrix protein coats the ribonucleocapsid within intact virions. Proc. Natl. Acad. Sci. U. S. A. 108: 18085-18090.
50. Harbury PB, Zhang T, Kim PS, Alber T. 1993. A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants. Science 262:1401-1407.
51. Corey EA, Iorio RM. 2007. Mutations in the stalk of the measles virus hemagglutinin protein decrease fusion but do not interfere with virusspecific interaction with the homologous fusion protein. J. Virol. 81: 9900-9910.
52. Dutch RE. 2010. Entry and fusion of emerging paramyxoviruses. PLoS Pathog. 6:e1000881. doi:10.1371/journal.ppat.1000881.
53. Mirza AM, Iorio RM. 2013. A mutation in the stalk of the Newcastle disease virus hemagglutinin-neuraminidase (HN) protein prevents triggering of the F protein despite allowing efficient HN-F complex formation. J. Virol. 87:8813-8815.
54. Harrison MS, Sakaguchi T, Schmitt AP. 2010. Paramyxovirus assembly and budding: building particles that transmit infections. Int. J. Biochem. Cell Biol. 42:1416-1429.
55. Li M, Schmitt PT, Li Z, McCrory TS, He B, Schmitt AP. 2009. Mumps virus matrix, fusion, and nucleocapsid proteins cooperate for efficient production of virus-like particles. J. Virol. 83:7261-7272.
56. Pohl C, Duprex WP, Krohne G, Rima BK, Schneider-Schaulies S. 2007. Measles virus M and F proteins associate with detergent-resistant membrane fractions and promote formation of virus-like particles. J. Gen. Virol. 88:1243-1250.
57. Liljeroos L, Krzyzaniak MA, Helenius A, Butcher SJ. 2013. Architecture of respiratory syncytial virus revealed by electron cryotomography. Proc. Natl. Acad. Sci. U. S. A. 110:11133-11138.