Structure and mutagenesis of the parainfluenza virus 5 hemagglutinin-neuraminidase stalk domain reveals a four-helix bundle and the role of the stalk in fusion promotion

Journal of Virology

Volumn 85, Issue 24, 2011, Pages 12855-12866

  Bose, Sayantan ^a   Welch, Brett D ^a   Kors, Christopher A ^a   Yuan, Ping ^b   Jardetzky, Theodore S ^b   Lamb, Robert A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMAGGLUTININ NEURAMINIDASE; HYBRID PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME GLYCOSYLATION; ENZYME STRUCTURE; HYDROPHOBICITY; MUTAGENESIS; NONHUMAN; OLIGOMERIZATION; PARAINFLUENZA VIRUS; PARAINFLUENZA VIRUS 5; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING;

AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE; CRYSTALLOGRAPHY, X-RAY; GLYCOSYLATION; HN PROTEIN; HUMANS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; PARAMYXOVIRIDAE; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; VIRUS INTERNALIZATION;

PARAINFLUENZA VIRUS; PARAMYXOVIRIDAE;

EID: 84855845971     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.06350-11     Document Type: Article

References (52)

1. Abe, Y., et al. 2004. Effect of the addition of oligosaccharides on the biological activities and antigenicity of influenza A/H3N2 virus hemagglutinin. J. Virol. 78:9605-9611.
2. Adams, P. D., et al. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. Sect. D Biol. Crystallogr. 66:213-221.
3. Aguilar, H. C., et al. 2006. N-glycans on Nipah virus fusion protein protect against neutralization but reduce membrane fusion and viral entry. J. Virol. 80:4878-4889.
4. Bishop, K. A., et al. 2007. Identification of Hendra virus G glycoprotein residues that are critical for receptor binding. J. Virol. 81:5893-5901.
5. Bousse, T., T. Takimoto, W. L. Gorman, T. Takahashi, and A. Portner. 1994. Regions on the hemagglutinin-neuraminidase proteins of human parainfluenza virus type-1 and Sendai virus important for membrane fusion. Virology 204:506-514.
6. Bowden, T. A., et al. 2008. Crystal structure and carbohydrate analysis of Nipah virus attachment glycoprotein: a template for antiviral and vaccine design. J. Virol. 82:11628-11636.
7. Chen, V. B., et al. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. Sect. D Biol. Crystallogr. 66:12-21.
8. Colf, L. A., Z. S. Juo, and K. C. Garcia. 2007. Structure of the measles virus hemagglutinin. Nat. Struct. Mol. Biol. 14:1227-1228.
9. Connolly, S. A., G. P. Leser, T. S. Jardetzky, and R. A. Lamb. 2009. Bimolecular complementation of paramyxovirus fusion and hemagglutinin-neuraminidase proteins enhances fusion: implications for the mechanism of fusion triggering. J. Virol. 83:10857-10868.
10. 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 virusspecific interaction with the homologous fusion protein. J. Virol. 81:9900-9910.
11. Crennell, S., T. Takimoto, A. Portner, and G. Taylor. 2000. Crystal structure of the multifunctional paramyxovirus hemagglutinin-neuraminidase. Nat. Struct. Biol. 7:1068-1074.
12. Deng, R., et al. 1999. Mutations in the Newcastle disease virus hemagglutinin-neuraminidase protein that interfere with its ability to interact with the homologous F protein in the promotion of fusion. Virology 253:43-54.
13. Deng, R., Z. Wang, A. M. Mirza, and R. M. Iorio. 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.
14. Emsley, P., and K. Cowtan. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. Sect. D Biol. Crystallogr. 60:2126-2132.
15. Ennis, M. K., et al. 2010. Mutations in the stalk region of the measles virus hemagglutinin inhibit syncytium formation but not virus entry. J. Virol. 84:10913-10917.
16. Gallagher, P., J. Henneberry, I. Wilson, J. Sambrook, and M.-J. Gething. 1988. Addition of carbohydrate side chains at novel sites on influenza hemagglutinin can modulate the folding, transport, and activity of the molecule. J. Cell Biol. 107:2059-2073.
17. Harbury, P. B., J. J. Plecs, B. Tidor, T. Alber, and P. S. Kim. 1998. Highresolution protein design with backbone freedom. Science 282:1462-1467.
18. Hashiguchi, T., et al. 2007. Crystal structure of measles virus hemagglutinin provides insight into effective vaccines. Proc. Natl. Acad. Sci. U. S. A. 104:19535-19540.
19. Heminway, B. R., Y. Yu, and M. S. Galinski. 1994. Paramyxovirus mediated cell fusion requires co-expression of both the fusion and hemagglutininneuraminidase glycoproteins. Virus Res. 31:1-16.
20. Horvath, C. M., R. G. Paterson, M. A. Shaughnessy, R. Wood, and R. A. Lamb. 1992. Biological activity of paramyxovirus fusion proteins: factors influencing formation of syncytia. J. Virol. 66:4564-4569.
21. Hsu, M.-C., A. Scheid, and P. W. Choppin. 1979. Reconstitution of membranes with individual paramyxovirus glycoproteins and phospholipid in cholate solution. Virology 95:476-491.
22. Hu, X., R. Ray, and R. W. Compans. 1992. Functional interactions between the fusion protein and hemagglutinin-neuraminidase of human parainfluenza viruses. J. Virol. 66:1528-1534.
23. Lamb, R. A., and T. S. Jardetzky. 2007. Structural basis of viral invasion: lessons from paramyxovirus F. Curr. Opin. Struct. Biol. 17:427-436.
24. Lamb, R. A., and G. D. Parks. 2007. Paramyxoviridae: the viruses and their replication, p. 1449-1496. In D. M. Knipe et al. (ed.), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
25. Lawrence, M. C., et al. 2004. Structure of the haemagglutinin-neuraminidase from human parainfluenza virus type III. J. Mol. Biol. 335:1343-1357.
26. Lee, J. K., et al. 2008. Functional interaction between paramyxovirus fusion and attachment proteins. J. Biol. Chem. 283:16561-16572.
27. Melanson, V. R., and R. M. Iorio. 2006. Addition of N-glycans in the stalk of the Newcastle disease virus HN protein blocks its interaction with the F protein and prevents fusion. J. Virol. 80:623-633.
28. Melanson, V. R., and R. M. Iorio. 2004. Amino acid substitutions in the F-specific domain in the stalk of the Newcastle disease virus HN protein modulate fusion and interfere with its interaction with the F protein. J. Virol. 78:13053-13061.
29. Morrison, T., C. McQuain, and L. McGinnes. 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.
30. Navaratnarajah, C. K., et al. 2011. The heads of the measles virus attachment protein move to transmit the fusion-triggering signal. Nat. Struct. Mol. Biol. 18:128-134.
31. Ng, D. T., S. W. Hiebert, and R. A. Lamb. 1990. Different roles of individual N-linked oligosaccharide chains in folding, assembly, and transport of the simian virus 5 hemagglutinin-neuraminidase. Mol. Cell. Biol. 10:1989-2001.
32. Ng, D. T., R. E. Randall, and R. A. Lamb. 1989. Intracellular maturation and transport of the SV5 type II glycoprotein hemagglutinin-neuraminidase: specific and transient association with GRP78-BiP in the endoplasmic reticulum and extensive internalization from the cell surface. J. Cell Biol. 109:3273-3289.
33. Otwinowski, Z., and W. Minor. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307-326.
34. Paal, T., et al. 2009. Probing the spatial organization of measles virus fusion complexes. J. Virol. 83:10480-10493.
35. Parks, G. D., and R. A. Lamb. 1990. Folding and oligomerization properties of a soluble and secreted form of the paramyxovirus hemagglutinin-neuraminidase glycoprotein. Virology 178:498-508.
36. Paterson, R. G., and R. A. Lamb. 1990. Conversion of a class II integral membrane protein into a soluble and efficiently secreted protein: multiple intracellular and extracellular oligomeric and conformational forms. J. Cell Biol. 110:999-1011.
37. 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.
38. Paterson, R. G., C. J. Russell, and R. A. Lamb. 2000. Fusion protein of the paramyxovirus SV5: destabilizing and stabilizing mutants of fusion activation. Virology 270:17-30.
39. Porotto, M., M. Murrell, O. Greengard, and A. Moscona. 2003. Triggering of human parainfluenza virus 3 fusion protein (F) by the hemagglutinin-neuraminidase (HN) protein: an HN mutation diminishes the rate of F activation and fusion. J. Virol. 77:3647-3654.
40. Randall, R. E., D. F. Young, K. K. A. Goswami, and W. C. Russell. 1987. Isolation and characterization of monoclonal antibodies to simian virus 5 and their use in revealing antigenic differences between human, canine and simian isolates. J. Gen. Virol. 68:2769-2780.
41. Robach, J. G., and R. A. Lamb. 2010. Analysis of parainfluenza virus-5 hemagglutinin-neuraminidase protein mutants that are blocked in internalization and degradation. Virology 406:189-201.
42. Sales, M., J. J. Plecs, J. M. Holton, and T. Alber. 2007. Structure of a designed, right-handed coiled-coil tetramer containing all biological amino acids. Protein Sci. 16:2224-2232.
43. Stetefeld, J., et al. 2000. Crystal structure of a naturally occurring parallel right-handed coiled coil tetramer. Nat. Struct. Biol. 7:772-776.
44. Stone-Hulslander, J., and T. G. Morrison. 1999. Mutational analysis of heptad repeats in the membrane-proximal region of Newcastle disease virus HN protein. J. Virol. 73:3630-3637.
45. Tanabayashi, K., and R. W. Compans. 1996. Functional interaction of paramyxovirus glycoproteins: identification of a domain in Sendai virus HN which promotes cell fusion. J. Virol. 70:6112-6118.
46. Terwilliger, T. C., et al. 2008. Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard. Acta Crystallogr. Sect. D Biol. Crystallogr. 64:61-69.
47. Thompson, S. D., W. G. Laver, K. G. Murti, and A. Portner. 1988. Isolation of a biologically active soluble form of the hemagglutinin-neuraminidase protein of Sendai virus. J. Virol. 62:4653-4660.
48. Xu, K., et al. 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.
49. 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.
50. Yuan, P., G. P. Leser, B. Demeler, R. A. Lamb, and T. S. Jardetzky. 2008. Domain architecture and oligomerization properties of the paramyxovirus PIV 5 hemagglutinin-neuraminidase (HN) protein. Virology 378:282-291.
51. Yuan, P., et al. 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.
52. Yuan, P., et al. 2005. Structural studies of the parainfluenza virius 5 hemagglutinin-neuraminidase tetramer in complex with its receptor, sialyllactose. Structure 13:803-815.