HCMV gB shares structural and functional properties with gB proteins from other herpesviruses

Virology

Volumn 435, Issue 2, 2013, Pages 239-249

  Sharma, Sapna ^a   Wisner, Todd W ^b   Johnson, David C ^b   Heldwein, Ekaterina E ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Cytomegalovirus; Entry; Fusion loop; Glycoprotein B; Glycosylation; Herpesvirus; Membrane fusion; Rosette

Indexed keywords

GLYCOPROTEIN B; VIRUS GLYCOPROTEIN;

ANIMAL CELL; ARTICLE; CELL FUSION; CELL MEMBRANE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; EPSTEIN BARR VIRUS; HERPES SIMPLEX VIRUS 1; HERPES VIRUS; HUMAN CYTOMEGALOVIRUS; HYDROPHOBICITY; LIGHT SCATTERING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; ROSETTE FORMATION; STRAIN IDENTIFICATION; VIRUS STRAIN;

AMINO ACID SEQUENCE; CYTOMEGALOVIRUS; HERPESVIRIDAE; HERPESVIRUS 1, HUMAN; HERPESVIRUS 4, HUMAN; MASS SPECTROMETRY; MEMBRANE FUSION; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; VIRAL ENVELOPE PROTEINS;

CYTOMEGALOVIRUS; HERPESVIRIDAE; HUMAN HERPESVIRUS 1; HUMAN HERPESVIRUS 4;

EID: 84871704386     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.09.024     Document Type: Article

References (49)

1. Atanasiu D., Saw W.T., Cohen G.H., Eisenberg R.J. Cascade of events governing cell-cell fusion induced by herpes simplex virus glycoproteins gD, gH/gL, and gB. J. Virol. 2010, 84:12292-12299.
2. Backovic M., Jardetzky T.S., Longnecker R. Hydrophobic residues that form putative fusion loops of Epstein-Barr virus glycoprotein B are critical for fusion activity. J. Virol. 2007, 81:9596-9600.
3. Backovic M., Leser G.P., Lamb R.A., Longnecker R., Jardetzky T.S. Characterization of EBV gB indicates properties of both class I and class II viral fusion proteins. Virology 2007, 368:102-113.
4. Backovic M., Longnecker R., Jardetzky T.S. Structure of a trimeric variant of the Epstein-Barr virus glycoprotein B. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:2880-2885.
5. Barton G.J. Alscript: a tool to format multiple sequence alignments. Protein Eng. 1993, 6:37-40.
6. Boyle K.A., Compton T. Receptor-binding properties of a soluble form of human cytomegalovirus glycoprotein B. J. Virol. 1998, 72:1826-1833.
7. Boyle K.A., Pietropaolo R.L., Compton T. Engagement of the cellular receptor for glycoprotein B of human cytomegalovirus activates the interferon-responsive pathway. Mol. Cell. Biol. 1999, 19:3607-3613.
8. Britt W.J. Neutralizing antibodies detect a disulfide-linked glycoprotein complex within the envelope of human cytomegalovirus. Virology 1984, 135:369-378.
9. Britt W.J., Jarvis M.A., Drummond D.D., Mach M. Antigenic domain 1 is required for oligomerization of human cytomegalovirus glycoprotein B. J. Virol. 2005, 79:4066-4079.
10. Britt W.J., Vugler L.G. Processing of the gp55-116 envelope glycoprotein complex (gB) of human cytomegalovirus. J. Virol. 1989, 63:403-410.
11. Britt W.J., Vugler L.G. Oligomerization of the human cytomegalovirus major envelope glycoprotein complex gB (gp55-116). J. Virol. 1992, 66:6747-6754.
12. Carlson C., Britt W.J., Compton T. Expression, purification, and characterization of a soluble form of human cytomegalovirus glycoprotein B. Virology 1997, 239:198-205.
13. Cieplik M., Klenk H.D., Garten W. Identification and characterization of spodoptera frugiperda furin: a thermostable subtilisin-like endopeptidase. Biol. Chem. 1998, 379:1433-1440.
14. Colugnati F.A., Staras S.A., Dollard S.C., Cannon M.J. Incidence of cytomegalovirus infection among the general population and pregnant women in the United States. BMC Infect. Dis. 2007, 7:71.
15. Compton T., Feire A. Early events in human cytomegalovirus infection. Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis 2007, Cambridge University Press.
16. Compton T., Nepomuceno R.R., Nowlin D.M. Human cytomegalovirus penetrates host cells by pH-independent fusion at the cell surface. Virology 1992, 191:387-395.
17. Connolly S.A., Jackson J.O., Jardetzky T.S., Longnecker R. Fusing structure and function: a structural view of the herpesvirus entry machinery. Nat. Rev. Microbiol. 2011, 9:369-381.
18. Cranage M.P., Kouzarides T., Bankier A.T., Satchwell S., Weston K., Tomlinson P., Barrell B., Hart H., Bell S.E., Minson A.C., G.L. Smith Identification of the human cytomegalovirus glycoprotein B gene and induction of neutralizing antibodies via its expression in recombinant vaccinia virus. EMBO J. 1986, 5:3057-3063.
19. Eisenberg R.J., Atanasiu D., Cairns T.M., Gallagher J.R., Krummenacher C., Cohen G.H. Herpes virus fusion and entry: a story with many characters. Viruses 2012, 4:800-832.
20. Eswar N., Webb B., Marti-Renom M.A., Madhusudhan M.S., Eramian D., Shen M.Y., Pieper U., Sali A. Comparative protein structure modeling using Modeller. Curr. Protoc. Bioinform. 2006, 6. (Chapter 5, Unit 5).
21. Feire A.L., Koss H., Compton T. Cellular integrins function as entry receptors for human cytomegalovirus via a highly conserved disintegrin-like domain. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:15470-15475.
22. Feire A.L., Roy R.M., Manley K., Compton T. The glycoprotein B disintegrin-like domain binds beta 1 integrin to mediate cytomegalovirus entry. J. Virol. 2010, 84:10026-10037.
23. Gibbons D.L., Vaney M.C., Roussel A., Vigouroux A., Reilly B., Lepault J., Kielian M., Rey F.A. Conformational change and protein-protein interactions of the fusion protein of Semliki Forest virus. Nature 2004, 427:320-325.
24. Hannah B.P., Cairns T.M., Bender F.C., Whitbeck J.C., Lou H., Eisenberg R.J., Cohen G.H. Herpes simplex virus glycoprotein B associates with target membranes via its fusion loops. J. Virol. 2009, 83:6825-6836.
25. Hannah B.P., Heldwein E.E., Bender F.C., Cohen G.H., Eisenberg R.J. Mutational evidence of internal fusion loops in herpes simplex virus glycoprotein B. J. Virol. 2007, 81:4858-4865.
26. Harrison S.C. Viral membrane fusion. Nat. Struct. Mol. Biol. 2008, 15:690-698.
27. Heldwein E.E., Lou H., Bender F.C., Cohen G.H., Eisenberg R.J., Harrison S.C. Crystal structure of glycoprotein B from herpes simplex virus 1. Science 2006, 313:217-220.
28. Isaacson M.K., Compton T. Human cytomegalovirus glycoprotein B is required for virus entry and cell-to-cell spread but not for virion attachment, assembly, or egress. J. Virol. 2009, 83:3891-3903.
29. Isaacson M.K., Feire A.L., Compton T. Epidermal growth factor receptor is not required for human cytomegalovirus entry or signaling. J. Virol. 2007, 81:6241-6247.
30. Jarvis D.L. Developing baculovirus-insect cell expression systems for humanized recombinant glycoprotein production. Virology 2003, 310:1-7.
31. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
32. Ruigrok R.W., Aitken A., Calder L.J., Martin S.R., Skehel J.J., Wharton S.A., Weis W., Wiley D.C. Studies on the structure of the influenza virus haemagglutinin at the pH of membrane fusion. J. Gen. Virol. 1988, 69(Pt. 11):2785-2795.
33. Ryckman B.J., Chase M.C., Johnson D.C. HCMV gH/gL/UL128-131 interferes with virus entry into epithelial cells: evidence for cell type-specific receptors. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:14118-14123.
34. Ryckman B.J., Chase M.C., Johnson D.C. Human cytomegalovirus TR strain glycoprotein O acts as a chaperone promoting gH/gL incorporation into virions but is not present in virions. J. Virol. 2010, 84:2597-2609.
35. Ryckman B.J., Jarvis M.A., Drummond D.D., Nelson J.A., Johnson D.C. Human cytomegalovirus entry into epithelial and endothelial cells depends on genes UL128 to UL150 and occurs by endocytosis and low-pH fusion. J. Virol. 2006, 80:710-722.
36. Silverman J.L., Sharma S., Cairns T.M., Heldwein E.E. Fusion-deficient insertion mutants of herpes simplex virus type 1 glycoprotein B adopt the trimeric postfusion conformation. J. Virol. 2010, 84:2001-2012.
37. Simpson J.A., Chow J.C., Baker J., Avdalovic N., Yuan S., Au D., Co M.S., Vasquez M., Britt W.J., Coelingh K.L. Neutralizing monoclonal antibodies that distinguish three antigenic sites on human cytomegalovirus glycoprotein H have conformationally distinct binding sites. J. Virol. 1993, 67:489-496.
38. Soroceanu L., Akhavan A., Cobbs C.S. Platelet-derived growth factor-alpha receptor activation is required for human cytomegalovirus infection. Nature 2008, 455:391-395.
39. Spaete R.R., Thayer R.M., Probert W.S., Masiarz F.R., Chamberlain S.H., Rasmussen L., Merigan T.C., Pachl C. Human cytomegalovirus strain Towne glycoprotein B is processed by proteolytic cleavage. Virology 1988, 167:207-225.
40. Stampfer S.D., Lou H., Cohen G.H., Eisenberg R.J., Heldwein E.E. Structural basis of local, pH-dependent conformational changes in glycoprotein B from herpes simplex virus type 1. J. Virol. 2010, 84:12924-12933.
41. Steven A.C., Spear P.G. Viral glycoproteins and an evolutionary conundrum. Science 2006, 313:177-178.
42. Sun X., Belouzard S., Whittaker G.R. Molecular architecture of the bipartite fusion loops of vesicular stomatitis virus glycoprotein G, a class III viral fusion protein. J. Biol. Chem. 2008, 283:6418-6427.
43. Urban M., Klein M., Britt W.J., Hassfurther E., Mach M. Glycoprotein H of human cytomegalovirus is a major antigen for the neutralizing humoral immune response. J. Gen. Virol. 1996, 77(Pt. 7):1537-1547.
44. Vanarsdall A.L., Chase M.C., Johnson D.C. Human cytomegalovirus glycoprotein gO complexes with gH/gL, promoting interference with viral entry into human fibroblasts but not entry into epithelial cells. J. Virol. 2011, 85:11638-11645.
45. Vanarsdall A.L., Ryckman B.J., Chase M.C., Johnson D.C. Human cytomegalovirus glycoproteins gB and gH/gL mediate epithelial cell-cell fusion when expressed either in cis or in trans. J. Virol. 2008, 82:11837-11850.
46. Vey M., Schafer W., Reis B., Ohuchi R., Britt W., Garten W., Klenk H.D., Radsak K. Proteolytic processing of human cytomegalovirus glycoprotein B (gpUL55) is mediated by the human endoprotease furin. Virology 1995, 206:746-749.
47. Wagner B., Kropff B., Kalbacher H., Britt W., Sundqvist V.A., Ostberg L., Mach M. A continuous sequence of more than 70 amino acids is essential for antibody binding to the dominant antigenic site of glycoprotein gp58 of human cytomegalovirus. J. Virol. 1992, 66:5290-5297.
48. Wang X., Huong S.M., Chiu M.L., Raab-Traub N., Huang E.S. Epidermal growth factor receptor is a cellular receptor for human cytomegalovirus. Nature 2003, 424:456-461.
49. Wille P.T., Knoche A.J., Nelson J.A., Jarvis M.A., Johnson D.C. A human cytomegalovirus gO-null mutant fails to incorporate gH/gL into the virion envelope and is unable to enter fibroblasts and epithelial and endothelial cells. J. Virol. 2010, 84:2585-2596.