Viral and cellular contributions to herpes simplex virus entry into the cell

Current Opinion in Virology

Volumn 2, Issue 1, 2012, Pages 28-36

  Campadelli Fiume, Gabriella ^a   Menotti, Laura ^a   Avitabile, Elisa ^a   Gianni, Tatiana ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

GD PROTEIN; GLYCOPROTEIN; HYBRID PROTEIN; NECTIN 1; PROTEIN GB; SYNDECAN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG; VIRUS PROTEIN; VITRONECTIN RECEPTOR;

ARTICLE; BINDING SITE; CELL MEMBRANE; CHO CELL; CRYSTAL STRUCTURE; CYTOPLASM; ENDOCYTOSIS; HERPES SIMPLEX VIRUS; IMMUNE RESPONSE; MOLECULAR INTERACTION; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; VIRION; VIRUS ENTRY; VIRUS ENVELOPE;

EID: 84857369888     PISSN: 18796257     EISSN: 18796265     Source Type: Journal    
DOI: 10.1016/j.coviro.2011.12.001     Document Type: Review

References (85)

1. G. Campadelli-Fiume, M. Amasio, E. Avitabile, A. Cerretani, C. Forghieri, T. Gianni, and L. Menotti The multipartite system that mediates entry of herpes simplex virus into the cell Rev Med Virol 17 2007 313 326 (Pubitemid 47425869)
2. A. Turner, B. Bruun, T. Minson, and H. Browne Glycoproteins gB, gD, and gHgL of herpes simplex virus type 1 are necessary and sufficient to mediate membrane fusion in a Cos cell transfection system J Virol 72 1998 873 875 (Pubitemid 28048916)
3. W.H. Cai, B. Gu, and S. Person Role of glycoprotein B of herpes simplex virus type 1 in viral entry and cell fusion J Virol 62 1988 2596 2604
4. M.W. Ligas, and D.C. Johnson A herpes simplex virus mutant in which glycoprotein D sequences are replaced by beta-galactosidase sequences binds to but is unable to penetrate into cells J Virol 62 1988 1486 1494
5. A. Forrester, H. Farrell, G. Wilkinson, J. Kaye, N. Davis Poynter, and T. Minson Construction and properties of a mutant of herpes simplex virus type 1 with glycoprotein H coding sequences deleted J Virol 66 1992 341 348
6. L. Hutchinson, H. Browne, V. Wargent, N. Davis-Poynter, S. Primorac, K. Goldsmith, A.C. Minson, and D.C. Johnson A novel herpes simplex virus glycoprotein, gL, forms a complex with glycoprotein H (gH) and affects normal folding and surface expression of gH J Virol 66 1992 2240 2250
7. R.J. Geraghty, C. Krummenacher, G.H. Cohen, R.J. Eisenberg, and P.G. Spear Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor Science 280 1998 1618 1620 (Pubitemid 28277708)
8. R.I. Montgomery, M.S. Warner, B.J. Lum, and P.G. Spear Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family Cell 87 1996 427 436 (Pubitemid 26374317)
9. F. Cocchi, L. Menotti, P. Mirandola, M. Lopez, and G. Campadelli-Fiume The ectodomain of a novel member of the immunoglobulin subfamily related to the poliovirus receptor has the attributes of a bona fide receptor for herpes simplex virus types 1 and 2 in human cells J Virol 72 1998 9992 10002 (Pubitemid 28520867)
10. D. Shukla, J. Liu, P. Blaiklock, N.W. Shworak, X. Bai, J.D. Esko, G.H. Cohen, R.J. Eisenberg, R.D. Rosenberg, and P.G. Spear A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry Cell 99 1999 13 22 v (Pubitemid 29468626)
11. F. Cocchi, L. Menotti, V. Di Ninni, M. Lopez, and G. Campadelli-Fiume The herpes simplex virus JMP mutant enters receptor-negative J cells through a novel pathway independent of the known receptors nectin1, HveA, and nectin2 J Virol 78 2004 4720 4729 (Pubitemid 38501093)
12. R. Dixit, V. Tiwari, and D. Shukla Herpes simplex virus type 1 induces filopodia in differentiated P19 neural cells to facilitate viral spread Neurosci Lett 440 2008 113 118
13. P. Petermann, I. Haase, and D. Knebel-Morsdorf Impact of Rac1 and Cdc42 signaling during early herpes simplex virus type 1 infection of keratinocytes J Virol 83 2009 9759 9772
14. M.J. Oh, J. Akhtar, P. Desai, and D. Shukla A role for heparan sulfate in viral surfing Biochem Biophys Res Commun 391 2010 176 181
15. A.V. Nicola, A.M. McEvoy, and S.E. Straus Roles for endocytosis and low pH in herpes simplex virus entry into HeLa and Chinese hamster ovary cells J Virol 77 2003 5324 5332 (Pubitemid 36460946)
16. T. Gianni, G. Campadelli-Fiume, and L. Menotti Entry of herpes simplex virus mediated by chimeric forms of nectin1 retargeted to endosomes or to lipid rafts occurs through acidic endosomes J Virol 78 2004 12268 12276 (Pubitemid 39458746)
17. C. Clement, V. Tiwari, P.M. Scanlan, T. Valyi-Nagy, B.Y. Yue, and D. Shukla A novel role for phagocytosis-like uptake in herpes simplex virus entry J Cell Biol 174 2006 1009 1021
18. Q. Li, S.M. Turk, and L.M. Hutt-Fletcher 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 1995 3987 3994
19. J. Sorem, T.S. Jardetzky, and R. Longnecker Cleavage and secretion of Epstein-Barr virus glycoprotein 42 promote membrane fusion with B lymphocytes J Virol 83 2009 6664 6672
20. G. Hahn, M.G. Revello, M. Patrone, E. Percivalle, G. Campanini, A. Sarasini, M. Wagner, A. Gallina, G. Milanesi, and U. Koszinowski Human cytomegalovirus UL131-128 genes are indispensable for virus growth in endothelial cells and virus transfer to leukocytes J Virol 78 2004 10023 10033 (Pubitemid 39187120)
21. D. Wang, and T. Shenk Human cytomegalovirus virion protein complex required for epithelial and endothelial cell tropism Proc Natl Acad Sci U S A 102 2005 18153 18158 (Pubitemid 41798517)
22. B.J. Ryckman, M.C. Chase, and D.C. Johnson 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 105 2008 14118 14123
23. T. Gianni, V. Gatta, and G. Campadelli-Fiume {alpha}V{beta}3-integrin routes herpes simplex virus to an entry pathway dependent on cholesterol-rich lipid rafts and dynamin2 Proc Natl Acad Sci U S A 107 2010 22260 22265
24. Gianni T, Campadelli-Fiume G: αVβ3-integrin relocalizes nectin1 and routes herpes simplex virus to lipid rafts. J Virol 2012, 86; in press.
25. L.S. Chesnokova, S.L. Nishimura, and L.M. Hutt-Fletcher Fusion of epithelial cells by Epstein-Barr virus proteins is triggered by binding of viral glycoproteins gHgL to integrins {alpha}v{beta}6 or {alpha}v{beta}8 Proc Natl Acad Sci U S A 106 2009 20464 20469
26. M.V. Veettil, S. Sadagopan, N. Sharma-Walia, F.Z. Wang, H. Raghu, L. Varga, and B. Chandran Kaposi's sarcoma-associated herpesvirus forms a multimolecular complex of integrins (alphaVbeta5, alphaVbeta3, and alpha3beta1) and CD98-xCT during infection of human dermal microvascular endothelial cells, and CD98-xCT is essential for the postentry stage of infection J Virol 82 2008 12126 12144
27. A.L. Feire, H. Koss, and T. Compton Cellular integrins function as entry receptors for human cytomegalovirus via a highly conserved disintegrin-like domain Proc Natl Acad Sci U S A 101 2004 15470 15475 (Pubitemid 39441565)
28. C. Parry, S. Bell, T. Minson, and H. Browne Herpes simplex virus type 1 glycoprotein H binds to alphavbeta3 integrins J Gen Virol 86 2005 7 10 (Pubitemid 40081145)
29. T. Satoh, J. Arii, T. Suenaga, J. Wang, A. Kogure, J. Uehori, N. Arase, I. Shiratori, S. Tanaka, and Y. Kawaguchi PILRalpha is a herpes simplex virus-1 entry coreceptor that associates with glycoprotein B Cell 132 2008 935 944 (Pubitemid 351381742)
30. J. Arii, M. Uema, T. Morimoto, H. Sagara, H. Akashi, E. Ono, H. Arase, and Y. Kawaguchi Entry of herpes simplex virus 1 and other alphaherpesviruses via the paired immunoglobulin-like type 2 receptor alpha J Virol 83 2009 4520 4527
31. N. Cheshenko, W. Liu, L.M. Satlin, and B.C. Herold Focal adhesion kinase plays a pivotal role in herpes simplex virus entry J Biol Chem 280 2005 31116 31125 (Pubitemid 41291847)
32. V. Tiwari, and D. Shukla PI3-Kinase signaling may affect multiple steps during herpes simplex virus-1 entry J Gen Virol 2010
33. A. Carfi, S.H. Willis, J.C. Whitbeck, C. Krummenacher, G.H. Cohen, R.J. Eisenberg, and D.C. Wiley Herpes simplex virus glycoprotein D bound to the human receptor HveA Mol Cell 8 2001 169 179 (Pubitemid 32772915)
34. C. Krummenacher, V.M. Supekar, J.C. Whitbeck, E. Lazear, S.A. Connolly, R.J. Eisenberg, G.H. Cohen, D.C. Wiley, and A. Carfi Structure of unliganded HSV gD reveals a mechanism for receptor-mediated activation of virus entry EMBO J 24 2005 4144 4153 (Pubitemid 41752883)
35. S.A. Connolly, D.J. Landsburg, A. Carfi, C.J. Whitbeck, Y. Zuo, D.C. Wiley, G.H. Cohen, and R.J. Eisenberg Potential nectin-1 binding site on herpes simplex virus glycoportein D J Virol 79 2005 1282 1295 (Pubitemid 40053910)
36. S. Manoj, C.R. Jogger, D. Myscofski, M. Yoon, and P.G. Spear Mutations in herpes simplex virus glycoprotein D that prevent cell entry via nectins and alter cell tropism Proc Natl Acad Sci U S A 101 2004 12414 12421 (Pubitemid 39122038)
37. P. Di Giovine, E.C. Settembre, A.K. Bhargava, M.A. Luftig, H. Lou, G.H. Cohen, R.J. Eisenberg, C. Krummenacher, and A. Carfi Structure of herpes simplex virus glycoprotein d bound to the human receptor nectin-1 PLoS Pathog 7 2011 e1002277
38. N. Zhang, J. Yan, G. Guangwen Lu, Z. Guo, Z. Fan, J. Jiawei Wang, Y. Shi, J. Qi, and G.F. Gao Binding of herpes simplex virus glycoprotein D to nectin-1 exploits host cell adhesion Nat Commun 2 2011 577
39. F. Cocchi, D. Fusco, L. Menotti, T. Gianni, R.J. Eisenberg, G.H. Cohen, and G. Campadelli-Fiume The soluble ectodomain of herpes simplex virus gD contains a membrane-proximal pro-fusion domain and suffices to mediate virus entry Proc Natl Acad Sci U S A 101 2004 7445 7450 (Pubitemid 38638052)
40. H. Matsuura, A.N. Kirschner, R. Longnecker, and T.S. Jardetzky Crystal structure of the Epstein-Barr virus (EBV) glycoprotein H/glycoprotein L (gH/gL) complex Proc Natl Acad Sci U S A 107 2010 22641 22646
41. T.K. Chowdary, T.M. Cairns, D. Atanasiu, G.H. Cohen, R.J. Eisenberg, and E.E. Heldwein Crystal structure of the conserved herpesvirus fusion regulator complex gH-gL Nat Struct Mol Biol 17 2010 882 888
42. M. Backovic, R.M. DuBois, J.J. Cockburn, A.J. Sharff, M.C. Vaney, H. Granzow, B.G. Klupp, G. Bricogne, T.C. Mettenleiter, and F.A. Rey Structure of a core fragment of glycoprotein H from pseudorabies virus in complex with antibody Proc Natl Acad Sci U S A 107 2010 22635 22640
43. T. Gianni, P.L. Martelli, R. Casadio, and G. Campadelli-Fiume The ectodomain of herpes simplex virus glycoprotein H contains a membrane alpha-helix with attributes of an internal fusion peptide, positionally conserved in the Herpesviridae family J Virol 79 2005 2931 2940 (Pubitemid 40270571)
44. S. Galdiero, A. Falanga, M. Vitiello, H. Browne, C. Pedone, and M. Galdiero Fusogenic domains in herpes simplex virus type 1 glycoprotein H J Biol Chem 280 2005 28632 28643 (Pubitemid 41105764)
45. T. Gianni, R. Fato, C. Bergamini, G. Lenaz, and G. Campadelli-Fiume Hydrophobic alpha-helices 1 and 2 of herpes simplex virus gH interact with lipids, and their mimetic peptides enhance virus infection and fusion J Virol 80 2006 8190 8198 (Pubitemid 44182319)
46. J.O. Jackson, and R. Longnecker Reevaluating herpes simplex virus hemifusion J Virol 84 2010 11814 11821
47. E.E. Heldwein, H. Lou, F.C. Bender, G.H. Cohen, R.J. Eisenberg, and S.C. Harrison Crystal structure of glycoprotein B from herpes simplex virus 1 Science 313 2006 217 220 (Pubitemid 44066251)
48. M. Backovic, R. Longnecker, and T.S. Jardetzky Structure of a trimeric variant of the Epstein-Barr virus glycoprotein B Proc Natl Acad Sci U S A 106 2009 2880 2885
49. J. Arii, J. Wang, T. Morimoto, T. Suenaga, H. Akashi, H. Arase, and Y. Kawaguchi A single-amino-acid substitution in herpes simplex virus 1 envelope glycoprotein B at a site required for binding to the paired immunoglobulin-like type 2 receptor alpha (PILRalpha) abrogates PILRalpha-dependent viral entry and reduces pathogenesis J Virol 84 2010 10773 10783
50. J. Arii, H. Goto, T. Suenaga, M. Oyama, H. Kozuka-Hata, T. Imai, A. Minowa, H. Akashi, H. Arase, and Y. Kawaoka Non-muscle myosin IIA is a functional entry receptor for herpes simplex virus-1 Nature 467 2010 859 862
51. T. Suenaga, T. Satoh, P. Somboonthum, Y. Kawaguchi, Y. Mori, and H. Arase Myelin-associated glycoprotein mediates membrane fusion and entry of neurotropic herpesviruses Proc Natl Acad Sci U S A 107 2010 866 871
52. T. Gianni, A. Cerretani, R. Dubois, S. Salvioli, S.S. Blystone, F. Rey, and G. Campadelli-Fiume Herpes simplex virus glycoproteins H/L bind to cells independently of {alpha}V{beta}3 integrin and inhibit virus entry, and their constitutive expression restricts infection J Virol 84 2010 4013 4025
53. E.E. Heldwein, and C. Krummenacher Entry of herpesviruses into mammalian cells Cell Mol Life Sci 65 2008 1653 1668
54. D. Fusco, C. Forghieri, and G. Campadelli-Fiume The pro-fusion domain of herpes simplex virus glycoprotein D (gD) interacts with the gD N terminus and is displaced by soluble forms of viral receptors Proc Natl Acad Sci U S A 102 2005 9323 9328 (Pubitemid 40923562)
55. Navaratnarajah CK, Miest T, Carfi A, Cattaneo R: Targeted entry of enveloped viruses: measles and herpes simplex virus 1. Curr Opin Virol 2; in press.
56. G. Zhou, G.J. Ye, W. Debinski, and B. Roizman Engineered herpes simplex virus 1 is dependent on IL13Ralpha2 receptor for cell entry and independent of glycoprotein D receptor interaction Proc Natl Acad Sci U S A 99 2002 15124 15129 (Pubitemid 35334620)
57. G. Zhou, and B. Roizman Characterization of a recombinant herpes simplex virus 1 designed to enter cells via the IL13Ralpha2 receptor of malignant glioma cells J Virol 79 2005 5272 5277 (Pubitemid 40548195)
58. H. Kamiyama, G. Zhou, and B. Roizman Herpes simplex virus 1 recombinant virions exhibiting the amino terminal fragment of urokinase-type plasminogen activator can enter cells via the cognate receptor Gene Ther 13 2006 621 629
59. G. Zhou, and B. Roizman Construction and properties of a herpes simplex virus 1 designed to enter cells solely via the IL-13alpha2 receptor Proc Natl Acad Sci U S A 103 2006 5508 5513
60. L. Menotti, A. Cerretani, H. Hengel, and G. Campadelli-Fiume Construction of a fully retargeted herpes simplex virus 1 recombinant capable of entering cells solely via human epidermal growth factor receptor 2 J Virol 20 2008 10153 10161
61. L. Menotti, G. Nicoletti, V. Gatta, S. Croci, L. Landuzzi, C. De Giovanni, P. Nanni, P.L. Lollini, and G. Campadelli-Fiume Inhibition of human tumor growth in mice by an oncolytic herpes simplex virus designed to target solely HER-2-positive cells Proc Natl Acad Sci U S A 106 2009 9039 9044
62. C.K. Navaratnarajah, N. Oezguen, L. Rupp, L. Kay, V.H. Leonard, W. Braun, and R. Cattaneo The heads of the measles virus attachment protein move to transmit the fusion-triggering signal Nat Struct Mol Biol 18 2011 128 134
63. D. Atanasiu, J.C. Whitbeck, T.M. Cairns, B. Reilly, G.H. Cohen, and R.J. Eisenberg Bimolecular complementation reveals that glycoproteins gB and gH/gL of herpes simplex virus interact with each other during cell fusion Proc Natl Acad Sci U S A 104 2007 18718 18723 (Pubitemid 350210763)
64. D. Atanasiu, W.T. Saw, G.H. Cohen, and R.J. Eisenberg Cascade of events governing cell-cell fusion induced by herpes simplex virus glycoproteins gD, gH/gL, and gB J Virol 84 2010 12292 12299
65. E. Avitabile, C. Forghieri, and G. Campadelli-Fiume Complexes between Herpes Simplex Virus glycoproteins gD, gB, and gH detected in cells by complementation of split enhanced green fluorescent protein J Virol 81 2007 11532 11537 (Pubitemid 47536124)
66. E. Avitabile, C. Forghieri, and G. Campadelli-Fiume Cross talk among the glycoproteins involved in herpes simplex virus entry and fusion: the interaction between gB and gH/gL does not necessarily require gD J Virol 83 2009 10752 10760
67. T. Gianni, M. Amasio, and G. Campadelli-Fiume Herpes simplex virus gD forms distinct complexes with fusion executors gB and gH/gL through the C-terminal profusion J Biol Chem 284 2009 17370 17382
68. S.A. Connolly, G.P. Leser, T.S. Jardetzky, and R.A. Lamb Bimolecular complementation of paramyxovirus fusion and hemagglutinin-neuraminidase proteins enhances fusion: implications for the mechanism of fusion triggering J Virol 83 2009 10857 10868
69. S.A. Connolly, J.O. Jackson, T.S. Jardetzky, and R. Longnecker Fusing structure and function: a structural view of the herpesvirus entry machinery Nat Rev Microbiol 9 2011 369 381
70. S.D. Stampfer, H. Lou, G.H. Cohen, R.J. Eisenberg, and E.E. Heldwein Structural basis of local, pH-dependent conformational changes in glycoprotein B from herpes simplex virus type 1 J Virol 84 2010 12924 12933
71. S.J. Dollery, C.C. Wright, D.C. Johnson, and A.V. Nicola Low-pH-dependent changes in the conformation and oligomeric state of the prefusion form of herpes simplex virus glycoprotein B are separable from fusion activity J Virol 85 2011 9964 9973
72. S.R. Paludan, A.G. Bowie, K.A. Horan, and K.A. Fitzgerald Recognition of herpesviruses by the innate immune system Nat Rev Immunol 11 2011 143 154
73. P. Paladino, and K.L. Mossman Mechanisms employed by herpes simplex virus 1 to inhibit the interferon response J Interferon Cytokine Res 29 2009 599 607
74. H.J. Ramos, and M. Gale Jr. RIG-I like receptors and their signaling crosstalk in the regulation of antiviral immunity Curr Opin Virol 1 2011 167 176
75. J. Melchjorsen Sensing herpes: more than toll Rev Med Virol 2011
76. C. Amici, A. Rossi, A. Costanzo, S. Ciafre, B. Marinari, M. Balsamo, M. Levrero, and M.G. Santoro Herpes simplex virus disrupts NF-kappaB regulation by blocking its recruitment on the IkappaBalpha promoter and directing the factor on viral genes J Biol Chem 281 2006 7110 7117 (Pubitemid 43847475)
77. C.M. Preston, A.N. Harman, and M.J. Nicholl Activation of interferon response factor-3 in human cells infected with herpes simplex virus type 1 or human cytomegalovirus J Virol 75 2001 8909 8916 (Pubitemid 32851895)
78. M.A. Medici, M.T. Sciortino, D. Perri, C. Amici, E. Avitabile, M. Ciotti, E. Balestrieri, E. De Smaele, G. Franzoso, and A. Mastino Protection by herpes simplex virus glycoprotein D against Fas-mediated apoptosis: role of nuclear factor kappaB J Biol Chem 278 2003 36059 36067 (Pubitemid 37139926)
79. M.T. Sciortino, M.A. Medici, F. Marino-Merlo, D. Zaccaria, M. Giuffre-Cuculletto, A. Venuti, S. Grelli, and A. Mastino Involvement of HVEM receptor in activation of nuclear factor kappaB by herpes simplex virus 1 glycoprotein D Cell Microbiol 10 2008 2297 2311
80. P. Paladino, D.T. Cummings, R.S. Noyce, and K.L. Mossman The IFN-independent response to virus particle entry provides a first line of antiviral defense that is independent of TLRs and retinoic acid-inducible gene I J Immunol 177 2006 8008 8016 (Pubitemid 44846318)
81. E.A. Kurt-Jones, M. Chan, S. Zhou, J. Wang, G. Reed, R. Bronson, M.M. Arnold, D.M. Knipe, and R.W. Finberg Herpes simplex virus 1 interaction with Toll-like receptor 2 contributes to lethal encephalitis Proc Natl Acad Sci U S A 101 2004 1315 1320 (Pubitemid 38182686)
82. S.B. Rasmussen, L.N. Sorensen, L. Malmgaard, N. Ank, J.D. Baines, Z.J. Chen, and S.R. Paludan Type I interferon production during herpes simplex virus infection is controlled by cell-type-specific viral recognition through Toll-like receptor 9, the mitochondrial antiviral signaling protein pathway, and novel recognition systems J Virol 81 2007 13315 13324 (Pubitemid 350247828)
83. K.W. Boehme, M. Guerrero, and T. Compton Human cytomegalovirus envelope glycoproteins B and H are necessary for TLR2 activation in permissive cells J Immunol 177 2006 7094 7102 (Pubitemid 44715077)
84. M.G. Santoro, A. Rossi, and Amici C NF-kappaB and virus infection: who controls whom EMBO J 22 2003 2552 2560 (Pubitemid 36712353)
85. I.J. MacLeod, and T. Minson Binding of herpes simplex virus type-1 virions leads to the induction of intracellular signalling in the absence of virus entry PLoS ONE 5 2010 e9560