A second receptor binding site on human parainfluenza virus type 3 hemagglutinin-neuraminidase contributes to activation of the fusion mechanism

Journal of Virology

Volumn 81, Issue 7, 2007, Pages 3216-3228

  Porotto, Matteo ^a   Fornabaio, Micaela ^b   Kellogg, Glen E ^b   Moscona, Anne ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; HYBRID PROTEIN; INFLUENZA VIRUS HEMAGGLUTININ; RECEPTOR; SIALIDASE; VIRUS FUSION PROTEIN; ZANAMIVIR;

ANIMAL CELL; ARTICLE; BINDING SITE; BIRD DISEASE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; NONHUMAN; PARAINFLUENZA VIRUS 3; PARAMYXOVIRUS; PRIORITY JOURNAL; RECEPTOR BINDING; VIRUS ACTIVATION; VIRUS CELL INTERACTION;

ALANINE; ANIMALS; BINDING SITES; CELL LINE; CERCOPITHECUS AETHIOPS; DIMERIZATION; HN PROTEIN; HUMANS; LIGANDS; MODELS, MOLECULAR; MUTATION; NAPHTHALENES; NEURAMINIDASE; PARAINFLUENZA VIRUS 3, HUMAN; PROTEIN STRUCTURE, QUATERNARY; RECEPTORS, VIRUS; VIRUS INTERNALIZATION; ZANAMIVIR;

HUMAN PARAINFLUENZA VIRUS 3; NEWCASTLE DISEASE VIRUS; PARAMYXOVIRIDAE;

EID: 33947363286     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02617-06     Document Type: Article

References (33)

1. Burnett, J. C., P. Botti, D. Abraham, and G. Kellogg. 2001. Computationally accessible method for estimating free energy changes resulting from site-specific mutations of biomolecules: systematic model building and structural/hydropathic analysis of deoxy and oxy hemoglobins. Proteins Struct. Funct. Genet. 42:355-377.
2. Connaris, H., T. Takimoto, R. Russell, S. Crennell, I. Moustafa, A: Portner, and G. Taylor. 2002. Probing the sialic acid binding site of the hemagglutinin-neuraminidase of Newcastle disease virus: identification of key amino acids involved in cell binding, catalysis, and fusion. J. Virol. 76:1816-1824.
3. Connolly, S. A., G. P. Leser, H. S. Yin, T. S. Jardetzky, and R. A. Lamb. 2006. Refolding of a paramyxovirus F protein from prefusion to postfusion conformations observed by liposome binding and electron microscopy. Proc. Natl. Acad. Sci. USA 103:17903-17908.
4. Corey, E. A., A. M. Mirza, E. Levandowsky, and R. M. Iorio. 2003. Fusion deficiency induced by mutations at the dimer interface in the Newcastle disease virus hemagglutinin-neuraminidase is due to a temperature-dependent defect in receptor binding. J. Virol. 77:6913-6922.
5. Cozzini, P., M. Fornabaio, A. Marabotti, D. J. Abraham, G. E. Kellogg, and A. Mozzarelli. 2002. Simple, intuitive calculations of free energy of binding for protein-ligand complexes. 1. Models without explicit constrained water. J. Med. Chem. 45:2469-2483.
6. Crennell, S., T. Takimoto. A. Portner, and G. Taylor. 2000. Crystal structure of the multifunctional paramyxovirus hemagglutinin- neuraminidase. Nat. Struct. Biol. 7:1068-1074.
7. Deng, R., Z. Wang, P. J. Mahon, M. Marinello, A. Mirza, and R. M. Iorio. 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.
8. Fornabaio, M., P. Cozzini, A. Mozzarelli, D. J. Abraham, and G. E. Kellogg. 2003. Simple, intuitive calculations of free energy of binding for protein-ligand complexes. 2. Computational titration and pH effects in molecular models of neuraminidase-inhibitor complexes. J. Med. Chem. 46:4487-4500.
9. Fornabaio, M., F. Spyrakis, A. Mozzarelli, P. Cozzini, D. J. Abraham, and G. E. Kellogg. 2004. Simple, intuitive calculations of free energy of binding for protein-ligand complexes. 3. The free energy contribution of structural water molecules in HIV-1 protease complexes. J. Med. Chem. 47:4507-4516.
10. Greengard, O., N. Poltoratskaia, E. Leikina, J. Zimmerberg, and A. Moscona. 2000. The anti-influenza virus agent 4-GU-DANA (Zanamivir) inhibits cell fusion mediated by human parainfluenza virus and influenza virus HA. J. Virol. 74:11108-11114.
11. Huberman, K., R. Peluso, and A. Moscona. 1995. The hemagglutinin-neuraminidase of human parainfluenza virus type 3: role of the neuraminidase in the viral life cycle. Virology. 214:294-300.
12. Jones, G., P. Willett, R. Glen, A. Leach, and R. Taylor. 1997. Development and validation of a genetic algorithm for flexible docking. J. Mol. Biol. 267:727-748.
13. olw more than the sum of its parts?. Eur. J. Med. Chem. 35:651-661.
14. Kellogg, G., and D. Chen. 2004. The importance of being exhaustive. Optimization of bridging structural water molecules and water networks in models of biological systems. Chem. Biodiv. 1:98-105.
15. Kellogg, G. E., M. Fornabaio, F. Spyrakis, A. Lodola, P. Cozzini, A. Mozzarelli, and D. J. Abraham. 2004. Getting it right: modeling of pH, solvent and "nearly" everything else in virtual screening of biological targets. J. Mol. Graph Model. 22:479-486.
16. Lamb, R. 1993. Paramyxovirus fusion: a hypothesis for changes. Virology 197:1-11.
17. Lawrence, M. C., N. A. Borg, V. A. Streltsov, P. A. Pilling, V. C. Epa, J. N. Varghese, J. L. McKimm-Breschkin, and P. M. Colman. 2004. Structure of the haemagglutinin-neuraminidase from human parainfluenza virus type III. J. Mol. Biol. 335:1343-1357.
18. Li, J., E. Quinlan, A. Mirza, and R. M. Iorio. 2004. Mutated form of the Newcastle disease virus hemagglutinin-neuraminidase interacts with the homologous fusion protein despite deficiencies in both receptor recognition and fusion promotion. J. Virol. 78:5299-5310.
19. Moosmann, P., and S. Rusconi. 1996. Alpha complementation of LacZ in mammalian cells. Nucleic Acids Res. 24:1171-1172.
20. Moscona, A., and R. W. Peluso. 1996. Analysis of human parainfluenza virus 3 receptor binding variants: evidence for the use of a specific sialic acid-containing receptor. Microb. Pathog. 20:179-184.
21. Moscona, A. 2005. Entry of parainfluenza virus into cells as a target for interrupting childhood respiratory disease. J. Clin. Investig. 115:1688-1698.
22. Moscona, A., and R. W. Peluso. 1993. Relative affinity of the human parainfluenza virus 3 hemagglutinin-neuraminidase for sialic acid correlates with virus-induced fusion activity. J. Virol. 67:6463-6468.
23. Murrell, M., M. Porotto, T. Weber, O. Greengard, and A. Moscona. 2003. Mutations in human parainfluenza virus type 3 HN causing increased receptor binding activity and resistance to the transition state sialic acid analog 4-GU-DANA (zanamivir). J. Virol. 77:309-317.
24. Porotto, M., O. Greengard, N. Poltoratskaia, M.-A. Horga, and A. Moscona. 2001. Human parainfluenza virus type 3 HN-receptor interaction: the effect of 4-GU-DANA on a neuraminidase-deficient variant. J. Virol. 76:7481-7488.
25. Porotto, M., M. Murrell, O. Greengard, L. Doctor, and A. Moscona. 2005. Influence of the human parainfluenza virus 3 attachment protein's neuraminidase activity on its capacity to activate the fusion protein. J. Virol. 79:2383-2392.
26. Porotto, M., L. Doctor, P. Carta, M. Fornabaio, O. Greengard, G. Kellogg, and A. Moscona. 2006. Inhibition of Hendra virus membrane fusion. J. Virol. 80:9837-9849.
27. Porotto, M., M. Murrell, O. Greengard, M. Lawrence, J. McKimm-Breschkin, and A. Moscona. 2004. Inhibition of parainfluenza virus type 3 and Newcastle disease virus hemagglutinin-neuraminidase receptor binding: effect of receptor avidity and steric hindrance at the inhibitor binding sites. J. Virol. 78:13911-13919.
28. Porotto, M., M. Fornabaio, O. Greengard, M. T. Murrell, G. E. Kellogg, and A. Moscona. 2006. Paramyxovirus receptor-binding molecules: engagement of one site on the hemagglutinin-neuraminidase protein modulates activity at the second site. J. Virol. 80:1204-1213.
29. Porotto, M., M. Murrell, O. Greengard, and A. Moscona. 2003. Triggering of human parainfluenza virus 3 fusion protein (F) by the hemagglutinin-neuraminidase (HN): an HN mutation diminishing the rate of F activation and fusion. J. Virol. 77:3647-3654.
30. Spyrakis, F., M. Fornabaio, P. Cozzini, A. Mozzarelli, D. Abraham, and G. Kellogg. 2004. Computational titration analysis of a multiprotic HIV-1 protease-ligand complex. J. Am. Chem. Soc. 126:11764-11765.
31. Wireko, F. C., G. E. Kellogg, and D. J. Abraham. 1991. Allosteric modifiers of hemoglobin. 2. Crystallographically determined binding sites and hydrophobic binding/interaction analysis of novel hemoglobin oxygen effectors. J. Med. Chem. 34:758-767.
32. Yuan, P., T. B. Thompson, B. A. Wurzburg, R. G. Paterson, R. A. Lamb, and T. S. Jardetzky. 2005. Structural studies of the parainfluenza virus 5 hemagglutinin-neuraminidase tetramer in complex with its receptor, sialyllactose. Structure 13:803-815.
33. Zaitsev, V., M. von Itzstein, D. Groves, M. Kiefel, T. Takimoto, A. Portner, and G. Taylor. 2004. Second sialic acid binding site in Newcastle disease virus hemagglutinin-neuraminidase: implications for fusion. J. Virol. 78: 3733-3741.