Fusion of Epstein-Barr virus with epithelial cells can be triggered by αvβ5 in addition to αvβ6 and αvβ8, and integrin binding triggers a conformational change in glycoproteins ghgl

Journal of Virology

Volumn 85, Issue 24, 2011, Pages 13214-13223

  Chesnokova, Liudmila S ^a   Hutt Fletcher, Lindsey M ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHAVBETA5 INTEGRIN; ALPHAVBETA6 INTEGRIN; ALPHAVBETA8 INTEGRIN; BETA INTEGRIN; CYSTEINE; EPITOPE; GLYCOPROTEIN; GLYCOPROTEIN H; GLYCOPROTEIN L; IMMUNOGLOBULIN F(AB) FRAGMENT; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CELL FUSION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISSOCIATION CONSTANT; EPITHELIUM CELL; EPSTEIN BARR VIRUS; FLUORESCENCE SPECTROSCOPY; HUMAN; HUMAN CELL; MOLECULAR PROBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; SURFACE PLASMON RESONANCE; VIRUS CELL INTERACTION; VIRUS NEUTRALIZATION;

ANTIGENS, NEOPLASM; EPITHELIAL CELLS; HERPESVIRUS 4, HUMAN; HUMANS; INTEGRINS; MEMBRANE GLYCOPROTEINS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; PROTEIN BINDING; PROTEIN CONFORMATION; RECEPTORS, VITRONECTIN; SPECTRUM ANALYSIS; SURFACE PLASMON RESONANCE; VIRAL ENVELOPE PROTEINS; VIRAL PROTEINS; VIRUS INTERNALIZATION;

HUMAN HERPESVIRUS 4;

EID: 84855849822     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05580-11     Document Type: Article

References (54)

1. Atanasiu, D., et al. 2010. Bimolecular complementation defines functional regions of herpes simplex virus gB that are involved with H/gL as a necessary step leading to fusion. J. Virol. 84:3825-3834.
2. Backovic, M., et al. 2010. Structure of a core fragment of glycoprotein H from pseudorabies virus in complex with antibody. Proc. Natl. Acad. Sci. U. S. A. 107:22635-22640.
3. Backovic, M., R. Longnecker, and T. S. Jardetzky. 2009. Structure of a trimeric variant of the Epstein-Barr virus glycoprotein B. Proc. Natl. Acad. Sci. U. S. A. 106:2880-2885.
4. Borza, C. M., and L. M. Hutt-Fletcher. 2002. Alternate replication in B cells and epithelial cells switches tropism of Epstein-Barr virus. Nat. Med. 8:594-599.
5. Borza, C. M., A. J. Morgan, S. M. Turk, and L. M. Hutt-Fletcher. 2004. Use of gHgL for attachment of Epstein-Barr virus to epithelial cells compromises infection. J. Virol. 78:5007-5014.
6. Breuss, J. M., et al. 1995. Expression of the β6 integrin subunit in development, neoplasia and tissue repair suggests a role in epithelial remodeling. J. Cell Sci. 108:2241-2251.
7. Breuss, J. M., N. Gillerr, L. Lu, D. Sheppard, and R. Pytela. 1993. Restricted distribution of integrin β6 mRNA in primate epithelial tissues. J. Histochem. Cytochem. 41:1521-1527.
8. Chesnokova, L. S., S. Nishimura, and L. Hutt-Fletcher. 2009. Fusion of epithelial cells by Epstein-Barr virus proteins is triggered by binding of viral proteins gHgL to integrins αvβ6 or αvβ8. Proc. Natl. Acad. Sci. U. S. A. 106:20464-20469.
9. Chowdary, T. K., et al. 2010. Crystal structure of the conserved herpesvirus fusion regulator complex gH-gL. Nat. Struct. Mol. Biol. 17:882-888.
10. di Renzo, L., A. Altiok, G. Klein, and E. Klein. 1994. Endogenous TGF-beta contributes to the induction of the EBV lytic cycle in two Burkitt lymphoma cell lines. Int. J. Cancer 57:914-919.
11. Fahmi, H., C. Cochet, Z. Hmama, P. Opolon, and I. Joab. 2000. Transforming growth factor beta 1 stimulates expression of the Epstein-Barr virus BZLF1 immediate-early gene product ZEBRA by an indirect mechanism which requires the MAPK kinase pathway. J. Virol. 74:5810-5818.
12. Galdiero, M., et al. 1997. Site-directed and linker insertion mutagenesis of herpes simplex virus type 1 glycoprotein H. J. Virol. 71:2163-2170.
13. Gline, S. E., S. Cambier, C. Govaerts, and S. L. Nishimura. 2004. A 50-A separation of the integrin αvβ3 extracellular domain C termini reveals an intermediate activation state. J. Biol. Chem. 279:54567-54572.
14. Hadinoto, V., M. Shapiro, C. C. Sun, and D. A. Thorley-Lawson. 2009. The dynamics of EBV shedding implicate a central role for epithelial cells in amplifying viral output. PLoS Pathog. 7:e10000496.
15. Hannah, B. P., et al. 2009. Herpes simplex virus glycoprotein B associates with target membranes via its fusion loops. J. Virol. 83:6825-6836.
16. Heldwein, E. E., et al. 2006. Crystal structure of glycoprotein B from herpes simplex virus 1. Science 313:217-220.
17. Hibbs, R. E., T. T. Talley, and P. Taylor. 2004. Acrylodan-conjugated cysteine side chains reveal conformational state and ligand site interactions of the acetylcholine-binding protein. J. Biol. Chem. 279:28483-28491.
18. Hutt-Fletcher, L. M. 2007. Epstein-Barr virus entry. J. Virol. 81:7825-7832.
19. Jiang, R., R. S. Scott, and L. M. Hutt-Fletcher. 2006. Epstein-Barr virus shed in saliva is high in B cell tropic gp42. J. Virol. 80:7281-7283.
20. Kirschner, A. N., J. Sorem, R. Longnecker, and T. S. Jardetzky. 2009. Structure of Epstein-Barr virus glycoprotein gp42 suggests a mechanism for triggering receptor-activated virus entry. Structure 17:223-233.
21. Krummenacher, C., et al. 2005. Structure of unliganded HSV gD reveals a mechanism for receptor-mediated activation of virus entry. EMBO J. 24: 4144-4153.
22. Lake, C. M., S. J. Molesworth, and L. M. Hutt-Fletcher. 1998. The Epstein-Barr virus (EBV) gN homolog BLRF1 encodes a 15 kilodalton glycoprotein that cannot be authentically processed unless it is co-expressed with the EBV gM homolog BBRF3. J. Virol. 72:5559-5564.
23. Li, Q. X., S. M. Turk, and L. M. Hutt-Fletcher. 1995. The Epstein-Barr virus (EBV) BZLF2 gene product associates with the gH and gL homologs of EBV and carries an epitope critical to infection of B cells but not of epithelial cells. J. Virol. 69:3987-3994.
24. Li, Q. X., et al. 1992. Epstein-Barr virus infection and replication in a human epithelial system. Nature 356:347-350.
25. Liang, C.-L., J.-L. Chen, Y.-P. P. Hsu, J. T. Ou, and Y.-S. Chang. 2002. Epstein-Barr virus BZLF1 gene is activated by transforming growth factor-β through cooperativity of Smads and c-Jun/c-Fos proteins. J. Biol. Chem. 277:23345-23357.
26. Mathias, P., M. Glalleno, and G. R. Nemerow. 1998. Interactions of soluble recombinant integrin alphav beta5 with human adenovirus. J. Virol. 72:8669-8675.
27. Matsuura, H., A. N. Kirschner, R. Longnecker, and T. S. Jardetzky. 2010. Crystal structure of the Epstein-Barr virus (EBV) glycoprotein H/glycoprotein L (gH/gL) complex. Proc. Natl. Acad. Sci. U. S. A. 107:22641-22646.
28. Miller, N., and L. M. Hutt-Fletcher. 1992. Epstein-Barr virus enters B cells and epithelial cells by different routes. J. Virol. 66:3409-3414.
29. Molesworth, S. J., C. M. Lake, C. M. Borza, S. M. Turk, and L. M. Hutt-Fletcher. 2000. Epstein-Barr virus gH is essential for penetration of B cell but also plays a role in attachment of virus to epithelial cells. J. Virol. 74:6324-6332.
30. Mu, D., et al. 2002. The integrin αvβ8 mediates epithelial homeostasis through MT-1-MMP-dependent activation of TGF-β1. J. Cell Biol. 157:493-507.
31. Mullen, M. M., K. M. Haan, R. Longnecker, and T. S. Jardetzky. 2002. Structure of the Epstein-Barr virus gp42 protein bound to the MHC class II receptor HLA-DR1. Mol. Cell 9:375-385.
32. Munger, J. S., et al. 1999. The integrin αvβ6 binds and activates latent TGFβ1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 96:319-328.
33. Oba, D. E., and L. M. Hutt-Fletcher. 1988. Induction of antibodies to the Epstein-Barr virus glycoprotein gp85 with a synthetic peptide corresponding to a sequence in the BXLF2 open reading frame. J. Virol. 62:1108-1114.
34. Omerovic, J., L. Lev, and R. Longnecker. 2005. The amino terminus of Epstein-Barr virus glycoprotein gH is important for fusion with B cells and epithelial cells. J. Virol. 79:12408-12415.
35. Pegtel, D. M., J. Middeldorp, and D. A. Thorley-Lawson. 2004. Epstein-Barr virus infection in ex-vivo tonsil epithelial cell cultures of asymptomatic carriers. J. Virol. 78:12613-12624.
36. Prendergast, F. G., M. Meyer, G. L. Carlson, S. Iida, and J. D. Potter. 1983. Synthesis, spectral properties and use of 6-acryloyl-2-dimethylaminonaphthalene (Acrylodan). J. Biol. Chem. 258:7541-7544.
37. Pulford, D. J., P. Lowrey, and A. J. Morgan. 1995. Co-expression of the Epstein-Barr virus BXLF2 and BKRF2 genes with a recombinant baculovirus produces gp85 on the cell surface with antigenic similarity to the native protein. J. Gen. Virol. 76:3145-3152.
38. Rickinson, A. B., and E. Kieff. 2007. Epstein-Barr virus, p. 2655-2700. In D. M. Knipe et al. (ed.), Fields virology, 5th ed., vol. 2. Lippincott Williams & Wilkins, Philadelphia, PA.
39. Roche, S., S. Bressanelli, F. A. Rey, and Y. Gaudin. 2006. Crystal structure of the low-pH form of the vesicular stomatitis glycoprotein G. Science 313:187-191.
40. Scheibel, T., J. Bloom, and S. L. Lindquist. 2004. The elongation of yeast prion fibers involves separable steps of association and conversion. Proc. Natl. Acad. Sci. U. S. A. 101:2287-2292.
41. Sheppard, D. 2003. Functions of pulmonary epithelial integrins: from development to disease. Physiol. Rev. 83:673-686.
42. Shimizu, N. A., A. Tanabe-Tochikura, Y. Kuroiwa, and K. Takada. 1994. Isolation of Epstein-Barr virus (EBV)-negative cell clones from the EBVpositive Burkitt's lymphoma (BL) line Akata: malignant phenotypes of BL cells are dependent on EBV. J. Virol. 68:6069-6073.
43. Shore, J. D., et al. 1995. A fluorescent probe study of plasminogen activator inhibitor-1: evidence for reactive center loop insertion and its role in the inhibitory mechanism. J. Biol. Chem. 270:5395-5398.
44. Spear, P. G. 2004. Herpes simplex virus receptors and ligands for cell entry. Cell. Microbiol. 6:401-410.
45. Spear, P. G., and R. Longnecker. 2003. Herpesvirus entry: an update. J. Virol. 77:10179-10185.
46. Takagi, J., B. M. Petre, T. Walz, and T. A. Springer. 2002. Global conformational rearrangements in integrin extracellular domains in outside-in and inside out signaling. Cell 110:599-611.
47. Thomas, G. J., M. L. Nystrom, and J. F. Marshall. 2006. αvβ6 integrin in wound healing and cancer of the oral cavity. J. Oral Pathol. Med. 35:1-10.
48. Wang, X., W. J. Kenyon, Q. X. Li, J. Mullberg, and L. M. Hutt-Fletcher. 1998. Epstein-Barr virus uses different complexes of glycoproteins gH and gL to infect B lymphocytes and epithelial cells. J. Virol. 72:5552-5558.
49. Weinacker, A., et al. 1994. Role of the integrin αvβ6 in cell attachment to fibronectin. J. Biol. Chem. 269:6940-6948.
50. White, J. M., and I. A. Wilson. 1987. Anti-peptide antibodies detect steps in a protein conformational change: low-pH activation of the influenza virus hemagglutinin. J. Cell Biol. 106:2887-2896.
51. Wu, L., C. M. Borza, and L. M. Hutt-Fletcher. 2005. Mutations of Epstein- Barr virus gH that are differentially able to support fusion with B cells or epithelial cells. J. Virol. 79:10923-10930.
52. Wu, L., and L. M. Hutt-Fletcher. 2007. Point mutations in EBV gH that abrogate or differentially affect B cell and epithelial cell fusion. Virology 363:148-155.
53. Yoon, T.-Y., and Y.-K. Shin. 2009. Progress in understanding the neuronal SNARE function and its regulation. Cell. Mol. Life Sci. 66:460-469.
54. Young, D. F., T. S. Carlos, K. Hagmaier, L. Fan, and R. E. Randall. 2007. AGS and other tissue culture cells can unknowingly be persistently infected with PIV5: a virus that blocks interferon signalling by degrading STAT1. Virology 365:238-240.