Global mapping of o-glycosylation of varicella zoster virus, human cytomegalovirus, and Epstein-Barr virus

Journal of Biological Chemistry

Volumn 291, Issue 23, 2016, Pages 12014-12028

  Bagdonaite, Ieva ^a   Nordén, Rickard ^b   Joshi, Hiren J ^a   King, Sarah L ^a   Vakhrushev, Sergey Y ^a   Olofsson, Sigvard ^b   Wandall, Hans H ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

DRUG PRODUCTS; ENZYME ACTIVITY; GLYCOPROTEINS; GLYCOSYLATION; IMMUNE SYSTEM; MAPPING; MASS SPECTROMETRY; POLYSACCHARIDES; PROTEINS; VACCINES;

ENVELOPE PROTEINS; EPSTEIN-BARR VIRUS; HERPES SIMPLEX VIRUS TYPE 1; HOMOLOGOUS PROTEINS; HUMAN CYTOMEGALOVIRUS; IMMUNE RESPONSE; VACCINE TARGETS; VARICELLA ZOSTER VIRUS;

VIRUSES;

GLYCAN; VIRUS ENVELOPE PROTEIN; VIRUS GLYCOPROTEIN; GLYCOPROTEIN; POLYSACCHARIDE; PROTEOME;

ARTICLE; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; PROTEIN STRUCTURE; PROTEOMICS; VARICELLA ZOSTER VIRUS; VIROGENESIS; VIRUS CELL INTERACTION; VIRUS ENTRY; BINDING SITE; CELL LINE; CYTOMEGALOVIRUS; FIBROBLAST; GLYCOSYLATION; HOST PATHOGEN INTERACTION; METABOLISM; PHYSIOLOGY; PROCEDURES; VIROLOGY; VIRUS INFECTION;

BINDING SITES; CELL LINE; CYTOMEGALOVIRUS; FIBROBLASTS; GLYCOPROTEINS; GLYCOSYLATION; HERPESVIRUS 3, HUMAN; HERPESVIRUS 4, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; MASS SPECTROMETRY; POLYSACCHARIDES; PROTEOME; PROTEOMICS; VIRAL ENVELOPE PROTEINS; VIRUS DISEASES; VIRUS INTERNALIZATION;

EID: 84973452237     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.721746     Document Type: Article

References (141)

1. Davison, A. J. (2002) Evolution of the herpesviruses. Vet. Microbiol. 86, 69-88
2. Grinde, B. (2013) Herpesviruses: latency and reactivation-viral strategies and host response. J. Oral Microbiol. 5, 22766
3. McGeoch, D. J., Rixon, F. J., and Davison, A. J. (2006) Topics in herpesvirus genomics and evolution. Virus Res. 117, 90-104
4. Fishman, J. A. (2013) Overview: cytomegalovirus and the herpesviruses in transplantation. Am. J. Transplant. 3, (Suppl. 3) 1- 8
5. Shiley, K., and Blumberg, E. (2010) Herpes viruses in transplant recipients: HSV, VZV, human herpes viruses, and EBV. Infect. Dis. Clin. North Am. 24, 373-393
6. Astuto, M., Palermo, C. I., Costanzo, C. M., Ettorre, G. C., Palmucci, S., Franchina, C., Russo, R., Valastro, P., Timpanaro, V., and Scalia, G. (2014)Fatal pulmonary disease and encephalic complication in a man with HSV-1 infection: A case report. J. Clin. Virol. 59, 59-62
7. Rowe, A. M., St Leger, A. J., Jeon, S., Dhaliwal, D. K., Knickelbein, J. E., and Hendricks, R. L. (2013) Herpes keratitis. Prog. Retin. Eye Res. 32, 88-101
8. Sabugo, F., Espinoza-Araya, R., Meneses, M. F., and Cuchacovich, M. (2014) Acute herpes simplex virus 1 pneumonitis in a patient with systemic lupus erythematosus. J. Clin. Rheumatol. 20, 42-44
9. Sili, U., Kaya, A., Mert, A., and HSV Encephalitis Study Group (2014)Herpes simplex virus encephalitis: clinical manifestations, diagnosis and outcome in 106 adult patients. J. Clin. Virol. 60, 112-118
10. Tsao, S. W., Tsang, C. M., To, K. F., and Lo, K. W. (2015) The role of Epstein-Barr virus in epithelial malignancies. J. Pathol. 235, 323-333
11. Gramolelli, S., and Schulz, T. F. (2015) The role of Kaposi sarcomaassociated herpesvirus in the pathogenesis of Kaposi sarcoma. J. Pathol. 235, 368-380
12. Davison, A. J. (2007) Overview of classification. In Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis (Arvin, A., Campadelli-Fiume, G., Mocarski, E., Moore, P. S., Roizman, B., Whitley, R., and Yamanishi, K., eds) pp. 3-9, Cambridge University Press, Cambridge, UK
13. Krummenacher, C., Carfí, A., Eisenberg, R. J., and Cohen, G. H. (2013)Entry of herpesviruses into cells: the enigma variations. Adv. Exp. Med. Biol. 790, 178-195
14. Corrales-Aguilar, E., Hoffmann, K., and Hengel, H. (2014) CMV-encoded Fcoγ receptors: modulators at the interface of innate and adaptive immunity. Semin. Immunopathol. 36, 627- 640
15. Favoreel, H. W., Van Minnebruggen, G., Van de Walle, G. R., Ficinska, J., and Nauwynck, H. J. (2006) Herpesvirus interference with virus-specific antibodies: bridging antibodies, internalizing antibodies, and hiding from antibodies. Vet. Microbiol. 113, 257-263
16. Hobman, T. C. (1993) Targeting of viral glycoproteins to the Golgi complex. Trends Microbiol. 1, 124-130
17. Olofsson, S., and Hansen, J. E. (1998) Host cell glycosylation of viral glycoproteins: a battlefield for host defence and viral resistance. Scand. J. Infect. Dis. 30, 435-440
18. Bennett, E. P., Mandel, U., Clausen, H., Gerken, T. A., Fritz, T. A., and Tabak, L. A. (2012) Control of mucin-type O-glycosylation: a classification of the polypeptide GalNAc-transferase gene family. Glycobiology 22, 736-756
19. Serafini-Cessi, F., Dall'Olio, F., Scannavini, M., and Campadelli-Fiume, G. (1983) Processing of herpes simplex virus-1 glycans in cells defective in glycosyl transferases of the Golgi system: relationship to cell fusion and virion egress. Virology 131, 59-70
20. Wang, J., Fan, Q., Satoh, T., Arii, J., Lanier, L. L., Spear, P. G., Kawaguchi, Y., and Arase, H. (2009) Binding of herpes simplex virus glycoprotein B (gB) to paired immunoglobulin-like type 2 receptor α depends on specific sialylated O-linked glycans on gB. J. Virol. 83, 13042-13045
21. Altgärde, N., Eriksson, C., Peerboom, N., Phan-Xuan, T., Moeller, S., Schnabelrauch, M., Svedhem, S., Trybala, E., Bergström, T., and Bally, M. (2015) Mucin-like region of herpes simplex virus type 1 attachment protein gC modulates the virus-glycosaminoglycan interaction. J. Biol. Chem. 290, 21473-21485
22. Davis, C. W., Mattei, L. M., Nguyen, H. Y., Ansarah-Sobrinho, C., Doms, R. W., and Pierson, T. C. (2006) The location of asparagine-linked glycans on West Nile virions controls their interactions with CD209 (dendritic cell-specific ICAM-3 grabbing nonintegrin). J. Biol. Chem. 281, 37183-37194
23. Helle, F., Vieyres, G., Elkrief, L., Popescu, C. I., Wychowski, C., Descamps, V., Castelain, S., Roingeard, P., Duverlie, G., and Dubuisson, J. (2010) Role of N-linked glycans in the functions of hepatitis C virus envelope proteins incorporated into infectious virions. J. Virol. 84, 11905-11915
24. Lennemann, N. J., Rhein, B. A., Ndungo, E., Chandran, K., Qiu, X., and Maury, W. (2014) Comprehensive functional analysis of N-linked glycans on Ebola virus GP1. mBio 5, e00862-e00813
25. Wang, W., Nie, J., Prochnow, C., Truong, C., Jia, Z., Wang, S., Chen, X. S., and Wang, Y. (2013) A systematic study of the N-glycosylation sites of HIV-1 envelope protein on infectivity and antibody-mediated neutralization. Retrovirology 10, 14
26. Chu, F. L., Wen, H. L., Hou, G. H., Lin, B., Zhang, W. Q., Song, Y. Y., Ren, G. J., Sun, C. X., Li, Z. M., and Wang, Z. (2013) Role of N-linked glycosylation of the human parainfluenza virus type 3 hemagglutininneuraminidase protein. Virus Res. 174, 137-147
27. Luo, S., Hu, K., He, S., Wang, P., Zhang, M., Huang, X., Du, T., Zheng, C., Liu, Y., and Hu, Q. (2015) Contribution of N-linked glycans on HSV-2 gB to cell-cell fusion and viral entry. Virology 483, 72-82
28. Suenaga, T., Matsumoto, M., Arisawa, F., Kohyama, M., Hirayasu, K., Mori, Y., and Arase, H. (2015) Sialic acids on varicella-zoster virus glycoprotein B required for cell-cell fusion. J. Biol. Chem. 290, 19833-19843
29. Pedersen, J. W., Bennett, E. P., Schjoldager, K. T., Meldal, M., Holmér, A. P., Blixt, O., Cló, E., Levery, S. B., Clausen, H., and Wandall, H. H. (2011) Lectin domains of polypeptide GalNAc transferases exhibit glycopeptide binding specificity. J. Biol. Chem. 286, 32684-32696
30. Wandall, H. H., Hassan, H., Mirgorodskaya, E., Kristensen, A. K., Roepstorff, P., Bennett, E. P., Nielsen, P. A., Hollingsworth, M. A., Burchell, J., Taylor-Papadimitriou, J., and Clausen, H. (1997) Substrate specificities of three members of the human UDP-N-acetyl-α-D-galactosamine:polypeptide N-acetylgalactosaminyltransferase family, GalNAc-T1, -T2, and -T3. J. Biol. Chem. 272, 23503-23514
31. Bagdonaite, I., Nordén, R., Joshi, H. J., Dabelsteen, S., Nyström, K., Vakhrushev, S. Y., Olofsson, S., and Wandall, H. H. (2015) A strategy for O-glycoproteomics of enveloped viruses: the O-glycoproteome of herpes simplex virus type 1. PLoS Pathog. 11, e1004784
32. Steentoft, C., Vakhrushev, S. Y., Vester-Christensen, M. B., Schjoldager, K. T., Kong, Y., Bennett, E. P., Mandel, U., Wandall, H., Levery, S. B., and Clausen, H. (2011) Mining the O-glycoproteome using zinc-finger nuclease-glycoengineered SimpleCell lines. Nat. Methods 8, 977-982
33. Iversen, M. B., Reinert, L. S., Thomsen, M. K., Bagdonaite, I., Nandakumar, R., Cheshenko, N., Prabakaran, T., Vakhrushev, S. Y., Krzyzowska, M., Kratholm, S. K., Ruiz-Perez, F., Petersen, S. V., Goriely, S., Bibby, B. M., Eriksson, K., et al. (2016) An innate antiviral pathway acting before interferons at epithelial surfaces. Nat. Immunol. 17, 150-158
34. Nordén, R., Halim, A., Nyström, K., Bennett, E. P., Mandel, U., Olofsson, S., Nilsson, J., and Larson, G. (2015) O-linked glycosylation of the mucin domain of the herpes simplex virus type 1-specific glycoprotein gC-1 is temporally regulated in a seed-and-spread manner. J. Biol. Chem. 290, 5078-5091
35. Lundström, M., Jeansson, S., and Olofsson, S. (1987) Host cell-induced differences in the O-glycosylation of herpes simplex virus gC-1: II. demonstration of cell-specific galactosyltransferase essential for formation of O-linked oligosaccharides. Virology 161, 395-402
36. Chiba, S., Striker, R. L., Jr., and Benyesh-Melnick, M. (1972) Microculture plaque assay for human and simian cytomegaloviruses. Appl. Microbiol. 23, 780-783
37. Bergström, T. (1996) Polymerase chain reaction for diagnosis of varicella zoster virus central nervous system infections without skin manifestations. Scand. J. Infect. Dis. Suppl. 100, 41-45
38. Steentoft, C., Vakhrushev, S. Y., Joshi, H. J., Kong, Y., Vester-Christensen, M. B., Schjoldager, K. T., Lavrsen, K., Dabelsteen, S., Pedersen, N. B., Marcos-Silva, L., Gupta, R., Bennett, E. P., Mandel, U., Brunak, S., Wandall, H. H., et al. (2013) Precision mapping of the human O-GalNAc glycoproteome through SimpleCell technology. EMBO J. 32, 1478-1488
39. Sadaoka, T., Yanagi, T., Yamanishi, K., and Mori, Y. (2010) Characterization of the varicella-zoster virus ORF50 gene, which encodes glycoprotein M. J. Virol. 84, 3488-3502
40. Zerboni, L., Sen, N., Oliver, S. L., and Arvin, A. M. (2014) Molecular mechanisms of varicella zoster virus pathogenesis. Nat. Rev. Microbiol. 12, 197-210
41. Suenaga, T., Satoh, T., Somboonthum, P., Kawaguchi, Y., Mori, Y., and Arase, H. (2010) Myelin-associated glycoprotein mediates membrane fusion and entry of neurotropic herpesviruses. Proc. Natl. Acad. Sci. U.S.A. 107, 866-871
42. Vleck, S. E., Oliver, S. L., Brady, J. J., Blau, H. M., Rajamani, J., Sommer, M. H., and Arvin, A. M. (2011) Structure-function analysis of varicellazoster virus glycoprotein H identifies domain-specific roles for fusion and skin tropism. Proc. Natl. Acad. Sci. U.S.A. 108, 18412-18417
43. Oliver, S. L., Sommer, M., Zerboni, L., Rajamani, J., Grose, C., and Arvin, A. M. (2009) Mutagenesis of varicella-zoster virus glycoprotein B: putative fusion loop residues are essential for viral replication, and the furin cleavage motif contributes to pathogenesis in skin tissue in vivo. J. Virol. 83, 7495-7506
44. Oliver, S. L., Brady, J. J., Sommer, M. H., Reichelt, M., Sung, P., Blau, H. M., and Arvin, A. M. (2013) An immunoreceptor tyrosine-based inhibition motif in varicella-zoster virus glycoprotein B regulates cell fusion and skin pathogenesis. Proc. Natl. Acad. Sci. U.S.A. 110, 1911-1916
45. Hannah, B. P., Cairns, T. M., Bender, F. C., Whitbeck, J. C., Lou, H., Eisenberg, R. J., and Cohen, G. H. (2009) Herpes simplex virus glycoprotein B associates with target membranes via its fusion loops. J. Virol. 83, 6825-6836
46. Mallory, S., Sommer, M., and Arvin, A. M. (1997) Mutational analysis of the role of glycoprotein I in varicella-zoster virus replication and its effects on glycoprotein E conformation and trafficking. J. Virol. 71, 8279-8288
47. Berarducci, B., Rajamani, J., Reichelt, M., Sommer, M., Zerboni, L., and Arvin, A. M. (2009) Deletion of the first cysteine-rich region of the varicella-zoster virus glycoprotein E ectodomain abolishes the gE and gI interaction and differentially affects cell-cell spread and viral entry. J. Virol. 83, 228-240
48. Berarducci, B., Rajamani, J., Zerboni, L., Che, X., Sommer, M., and Arvin, A. M. (2010) Functions of the unique N-terminal region of glycoprotein E in the pathogenesis of varicella-zoster virus infection. Proc. Natl. Acad. Sci. U.S.A. 107, 282-287
49. Li, Q., Ali, M. A., and Cohen, J. I. (2006) Insulin degrading enzyme is a cellular receptor mediating varicella-zoster virus infection and cell-tocell spread. Cell 127, 305-316
50. Li, Q., Krogmann, T., Ali, M. A., Tang, W. J., and Cohen, J. I. (2007) The amino terminus of varicella-zoster virus (VZV) glycoprotein E is required for binding to insulin-degrading enzyme, a VZV receptor. J. Virol. 81, 8525- 8532
51. Moffat, J., Ito, H., Sommer, M., Taylor, S., and Arvin, A. M. (2002) Glycoprotein I of varicella-zoster virus is required for viral replication in skin and T cells. J. Virol. 76, 8468-8471
52. Oliver, S. L., Sommer, M. H., Reichelt, M., Rajamani, J., Vlaycheva-Beisheim, L., Stamatis, S., Cheng, J., Jones, C., Zehnder, J., and Arvin, A. M. (2011) Mutagenesis of varicella-zoster virus glycoprotein I (gI)identifies a cysteine residue critical for gE/gI heterodimer formation, gI structure, and virulence in skin cells. J. Virol. 85, 4095- 4110
53. Moffat, J. F., Zerboni, L., Kinchington, P. R., Grose, C., Kaneshima, H., and Arvin, A. M. (1998) Attenuation of the vaccine Oka strain of varicella-zoster virus and role of glycoprotein C in alphaherpesvirus virulence demonstrated in the SCID-hu mouse. J. Virol. 72, 965-974
54. Grose, C., Carpenter, J. E., Jackson, W., and Duus, K. M. (2010) Overview of varicella-zoster virus glycoproteins gC, gH and gL. Curr. Top. Microbiol. Immunol. 342, 113-128
55. Varnum, S. M., Streblow, D. N., Monroe, M. E., Smith, P., Auberry, K. J., Pasa-Tolic, L., Wang, D., Camp, D. G., 2nd, Rodland, K., Wiley, S., Britt, W., Shenk, T., Smith, R. D., and Nelson, J. A. (2004) Identification of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. J. Virol. 78, 10960-10966
56. Mocarski Jr., E. (2007) Betaherpes viral genes and their functions. In Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis (Arvin, A., Campadelli-Fiume, G., Mocarski, E., Moore, P. S., Roizman, B., Whitley, R., and Yamanishi, K., eds) pp. 204-230, Cambridge University Press, Cambridge, UK
57. Dunn, W., Chou, C., Li, H., Hai, R., Patterson, D., Stolc, V., Zhu, H., and Liu, F. (2003) Functional profiling of a human cytomegalovirus genome. Proc. Natl. Acad. Sci. U.S.A. 100, 14223-14228
58. Zhou, M., Lanchy, J. M., and Ryckman, B. J. (2015) Human cytomegalovirus gH/gL/gO promotes the fusion step of entry into all cell types, whereas gH/gL/UL128-131 broadens virus tropism through a distinct mechanism. J. Virol. 89, 8999-9009
59. Ciferri, C., Chandramouli, S., Donnarumma, D., Nikitin, P. A., Cianfrocco, M. A., Gerrein, R., Feire, A. L., Barnett, S. W., Lilja, A. E., Rappuoli, R., Norais, N., Settembre, E. C., and Carfi, A. (2015) Structural and biochemical studies of HCMV gH/gL/gO and pentamer reveal mutually exclusive cell entry complexes. Proc. Natl. Acad. Sci. U.S.A. 112, 1767-1772
60. Sekulin, K., Görzer, I., Heiss-Czedik, D., and Puchhammer-Stöckl, E. (2007) Analysis of the variability of CMV strains in the RL11D domain of the RL11 multigene family. Virus Genes 35, 577-583
61. Corrales-Aguilar, E., Trilling, M., Hunold, K., Fiedler, M., Le, V. T., Reinhard, H., Ehrhardt, K., Mercé-Maldonado, E., Aliyev, E., Zimmermann, A., Johnson, D. C., and Hengel, H. (2014) Human cytomegalovirus Fcγ binding proteins gp34 and gp68 antagonize Fcoγ receptors I, II and III. PLoS Pathog. 10, e1004131
62. Cortese, M., Calò, S., D'Aurizio, R., Lilja, A., Pacchiani, N., and Merola, M. (2012) Recombinant human cytomegalovirus (HCMV) RL13 binds human immunoglobulin G Fc. PLoS One 7, e50166
63. Vomaske, J., Nelson, J. A., and Streblow, D. N. (2009) Human Cytomegalovirus US28: a functionally selective chemokine binding receptor. Infectious Disorders Drug Targets 9, 548-556
64. Tadagaki, K., Tudor, D., Gbahou, F., Tschische, P., Waldhoer, M., Bomsel, M., Jockers, R., and Kamal, M. (2012) Human cytomegalovirus-encoded UL33 and UL78 heteromerize with host CCR5 and CXCR4 impairing their HIV coreceptor activity. Blood 119, 4908-4918
65. Casarosa, P., Waldhoer, M., LiWang, P. J., Vischer, H. F., Kledal, T., Timmerman, H., Schwartz, T. W., Smit, M. J., and Leurs, R. (2005) CC and CX3C chemokines differentially interact with the N terminus of the human cytomegalovirus-encoded US28 receptor. J. Biol. Chem. 280, 3275-3285
66. Lesniewski, M., Das, S., Skomorovska-Prokvolit, Y., Wang, F. Z., and Pellett, P. E. (2006) Primate cytomegalovirus US12 gene family: a distinct and diverse clade of seven-transmembrane proteins. Virology 354, 286-298
67. Cavaletto, N., Luganini, A., and Gribaudo, G. (2015) Inactivation of the human cytomegalovirus US20 gene hampers productive viral replication in endothelial cells. J. Virol. 89, 11092-11106
68. Müllberg, J., Hsu, M. L., Rauch, C. T., Gerhart, M. J., Kaykas, A., and Cosman, D. (1999) The R27080 glycoprotein is abundantly secreted from human cytomegalovirus-infected fibroblasts. J. Gen. Virol. 80, 437-440
69. Wang, D., Bresnahan, W., and Shenk, T. (2004) Human cytomegalovirus encodes a highly specific RANTES decoy receptor. Proc. Natl. Acad. Sci. U.S.A. 101, 16642-16647
70. Lüttichau, H. R. (2010) The cytomegalovirus UL146 gene product vCXCL1 targets both CXCR1 and CXCR2 as an agonist. J. Biol. Chem. 285, 9137-9146
71. Geyer, H., Hartung, E., Mages, H. W., Weise, C., Beluiæ, R., Vugrek, O., Jonjic, S., Kroczek, R. A., and Voigt, S. (2014) Cytomegalovirus expresses the chemokine homologue vXCL1 capable of attracting XCR1 + CD4 - dendritic cells. J. Virol. 88, 292-302
72. Müller, S., Zocher, G., Steinle, A., and Stehle, T. (2010) Structure of the HCMV UL16-MICB complex elucidates select binding of a viral immunoevasin to diverse NKG2D ligands. PLoS Pathog. 6, e1000723
73. Tirabassi, R. S., and Ploegh, H. L. (2002) The human cytomegalovirus US8 glycoprotein binds to major histocompatibility complex class I products. J. Virol. 76, 6832-6835
74. Johannsen, E., Luftig, M., Chase, M. R., Weicksel, S., Cahir-McFarland, E., Illanes, D., Sarracino, D., and Kieff, E. (2004) Proteins of purified Epstein-Barr virus. Proc. Natl. Acad. Sci. U.S.A. 101, 16286-16291
75. Wang, X., Kenyon, W. J., Li, Q., Müllberg, J., and Hutt-Fletcher, L. M. (1998) Epstein-Barr virus uses different complexes of glycoproteins gH and gL to infect B lymphocytes and epithelial cells. J. Virol. 72, 5552-5558
76. Sathiyamoorthy, K., Jiang, J., Hu, Y. X., Rowe, C. L., Möhl, B. S., Chen, J., Jiang, W., Mellins, E. D., Longnecker, R., Zhou, Z. H., and Jardetzky, T. S. (2014) Assembly and architecture of the EBV B cell entry triggering complex. PLoS Pathog. 10, e1004309
77. Liu, F., Marquardt, G., Kirschner, A. N., Longnecker, R., and Jardetzky, T. S. (2010) Mapping the N-terminal residues of Epstein-Barr virus gp42 that bind gH/gL by using fluorescence polarization and cell-based fusion assays. J. Virol. 84, 10375-10385
78. Sorem, J., Jardetzky, T. S., and Longnecker, R. (2009) Cleavage and secretion of Epstein-Barr virus glycoprotein 42 promote membrane fusion with B lymphocytes. J. Virol. 83, 6664-6672
79. Lake, C. M., and Hutt-Fletcher, L. M. (2000) Epstein-Barr virus that lacks glycoprotein gN is impaired in assembly and infection. J. Virol. 74, 11162-11172
80. Nemerow, G. R., Houghten, R. A., Moore, M. D., and Cooper, N. R. (1989) Identification of an epitope in the major envelope protein of Epstein-Barr virus that mediates viral binding to the B lymphocyte EBV receptor (CR2). Cell 56, 369-377
81. Serafini-Cessi, F., Malagolini, N., Nanni, M., Dall'Olio, F., Campadelli-Fiume, G., Tanner, J., and Kieff, E. (1989) Characterization of N- and O-linked oligosaccharides of glycoprotein 350 from Epstein-Barr virus. Virology 170, 1-10
82. Janz, A., Oezel, M., Kurzeder, C., Mautner, J., Pich, D., Kost, M., Hammerschmidt, W., and Delecluse, H. J. (2000) Infectious Epstein-Barr virus lacking major glycoprotein BLLF1 (gp350/220) demonstrates the existence of additional viral ligands. J. Virol. 74, 10142-10152
83. Thorley-Lawson, D. A., and Poodry, C. A. (1982) Identification and isolation of the main component (gp350-gp220) of Epstein-Barr virus responsible for generating neutralizing antibodies in vivo. J. Virol. 43, 730-736
84. Olofsson, S., Sjöblom, I., Lundström, M., Jeansson, S., and Lycke, E. (1983) Glycoprotein C of herpes simplex virus type 1: characterization of O-linked oligosaccharides. J. Gen. Virol. 64, 2735-2747
85. Yang, Z. Y., Duckers, H. J., Sullivan, N. J., Sanchez, A., Nabel, E. G., and Nabel, G. J. (2000) Identification of the Ebola virus glycoprotein as the main viral determinant of vascular cell cytotoxicity and injury. Nat. Med. 6, 886-889
86. Levery, S. B., Steentoft, C., Halim, A., Narimatsu, Y., Clausen, H., and Vakhrushev, S. Y. (2015) Advances in mass spectrometry driven O-glycoproteomics. Biochim. Biophys. Acta 1850, 33- 42
87. Halim, A., Westerlind, U., Pett, C., Schorlemer, M., Rüetschi, U., Brinkmalm, G., Sihlbom, C., Lengqvist, J., Larson, G., and Nilsson, J. (2014)Assignment of saccharide identities through analysis of oxonium ion fragmentation profiles in LC-MS/MS of glycopeptides. J. Proteome Res. 13, 6024- 6032
88. Wandall, H. H., Rumjantseva, V., Sørensen, A. L., Patel-Hett, S., Josefsson, E. C., Bennett, E. P., Italiano, J. E., Jr., Clausen, H., Hartwig, J. H., and Hoffmeister, K. M. (2012) The origin and function of platelet glycosyltransferases.Blood 120, 626- 635
89. Nakamura, S., Horie, M., Daidoji, T., Honda, T., Yasugi, M., Kuno, A., Komori, T., Okuzaki, D., Narimatsu, H., Nakaya, T., and Tomonaga, K. (2015) Influenza A virus-induced expression of a GalNAc transferase, GALNT3, via miRNAs is required for enhanced viral replication. J. Virol. 90, 1788-1801
90. Schjoldager, K. T., Joshi, H. J., Kong, Y., Goth, C. K., King, S. L., Wandall, H. H., Bennett, E. P., Vakhrushev, S. Y., and Clausen, H. (2015) Deconstruction of O-glycosylation-GalNAc-T isoforms direct distinct subsets of the O-glycoproteome. EMBO Reports 16, 1713-1722
91. Kropff, B., Burkhardt, C., Schott, J., Nentwich, J., Fisch, T., Britt, W., and Mach, M. (2012) Glycoprotein N of human cytomegalovirus protects the virus from neutralizing antibodies. PLoS Pathog. 8, e1002999
92. Machiels, B., Lété, C., Guillaume, A., Mast, J., Stevenson, P. G., Vanderplasschen, A., and Gillet, L. (2011) Antibody evasion by a gammaherpesvirus O-glycan shield. PLoS Pathog. 7, e1002387
93. Olofsson, S., Blixt, O., Bergstrom, T., Frank, M., and Wandall, H. H. (2015) Viral O-GalNAc peptide epitopes: a novel potential target in viral envelope glycoproteins. Rev. Med. Virol. 26, 34-48
94. Madsen, C. B., Petersen, C., Lavrsen, K., Harndahl, M., Buus, S., Clausen, H., Pedersen, A. E., and Wandall, H. H. (2012) Cancer associated aberrant protein O-glycosylation can modify antigen processing and immune response. PLoS One 7, e50139
95. Roizman, B., and Campadelli-Fiume, G. (2007) Alphaherpes viral genes and their functions. In Human Herpesviruses: Biology, Therapy, and Immunoprophylaxis (Arvin, A., Campadelli-Fiume, G., Mocarski, E., Moore, P. S., Roizman, B., Whitley, R., and Yamanishi, K., eds) pp. 70-92, Cambridge University Press, Cambridge, UK
96. Heldwein, E. E., Lou, H., Bender, F. C., Cohen, G. H., Eisenberg, R. J., and Harrison, S. C. (2006) Crystal structure of glycoprotein B from herpes simplex virus 1. Science 313, 217-220
97. Goth, C. K., Halim, A., Khetarpal, S. A., Rader, D. J., Clausen, H., and Schjoldager, K. T. (2015) A systematic study of modulation of ADAMmediated ectodomain shedding by site-specific O-glycosylation. Proc. Natl. Acad. Sci. U.S.A. 112, 14623-14628
98. Bräutigam, J., Scheidig, A. J., and Egge-Jacobsen, W. (2013) Mass spectrometric analysis of hepatitis C viral envelope protein E2 reveals extended microheterogeneity of mucin-type O-linked glycosylation. Glycobiology 23, 453-474
99. Go, E. P., Hua, D., and Desaire, H. (2014) Glycosylation and disulfide bond analysis of transiently and stably expressed clade C HIV-1 gp140 trimers in 293T cells identifies disulfide heterogeneity present in both proteins and differences in O-linked glycosylation. J. Proteome Res. 13, 4012-4027
100. Breuza, L., Garcia, M., Delgrossi, M. H., and Le Bivic, A. (2002) Role of the membrane-proximal O-glycosylation site in sorting of the human receptor for neurotrophins to the apical membrane of MDCK cells. Exp. Cell Res. 273, 178-186
101. Leuenberger, B., Hahn, D., Pischitzis, A., Hansen, M. K., and Sterchi, E. E. (2003) Human meprin β O-linked glycans in the intervening region of the type I membrane protein protect the C-terminal region from proteolytic cleavage and diminish its secretion. Biochem. J. 369, 659- 665
102. Maryon, E. B., Zhang, J., Jellison, J. W., and Kaplan, J. H. (2009) Human copper transporter 1 lacking O-linked glycosylation is proteolytically cleaved in a Rab9-positive endosomal compartment. J. Biol. Chem. 284, 28104-28114
103. Remacle, A. G., Chekanov, A. V., Golubkov, V. S., Savinov, A. Y., Rozanov, D. V., and Strongin, A. Y. (2006) O-glycosylation regulates autolysis of cellular membrane type-1 matrix metalloproteinase (MT1-MMP). J. Biol. Chem. 281, 16897-16905
104. Schjoldager, K. T., and Clausen, H. (2012) Site-specific protein O-glycosylation modulates proprotein processing: deciphering specific functions of the large polypeptide GalNAc-transferase gene family. Biochim. Biophys. Acta 1820, 2079-2094
105. Rowe, C. L., Chen, J., Jardetzky, T. S., and Longnecker, R. (2015) Membrane anchoring of Epstein-Barr virus gp42 inhibits fusion with B cells even with increased flexibility allowed by engineered spacers. mBio 6, e02285-14
106. Borza, C. M., and Hutt-Fletcher, L. M. (2002) Alternate replication in B cells and epithelial cells switches tropism of Epstein-Barr virus. Nat. Med. 8, 594-599
107. Abaitua, F., Zia, F. R., Hollinshead, M., and O'Hare, P. (2013) Polarized cell migration during cell-to-cell transmission of herpes simplex virus in human skin keratinocytes. J. Virol. 87, 7921-7932
108. Gurevich, V. V., and Gurevich, E. V. (2008) How and why do GPCRs dimerize? Trends Pharmacol. Sci. 29, 234-240
109. Hakalahti, A. E., Vierimaa, M. M., Lilja, M. K., Kumpula, E. P., Tuusa, J. T., and Petäjä-Repo, U. E. (2010) Humanβ 1-adrenergic receptor is subject to constitutive and regulated N-terminal cleavage. J. Biol. Chem. 285, 28850-28861
110. Gabaev, I., Elbasani, E., Ameres, S., Steinbrück, L., Stanton, R., Döring, M., Lenac Rovis, T., Kalinke, U., Jonjic, S., Moosmann, A., and Messerle, M. (2014) Expression of the human cytomegalovirus UL11 glycoprotein in viral infection and evaluation of its effect on virus-specific CD8 T cells. J. Virol. 88, 14326-14339
111. Reimer, J. J., Backovic, M., Deshpande, C. G., Jardetzky, T., and Longnecker, R. (2009) Analysis of Epstein-Barr virus glycoprotein B functional domains via linker insertion mutagenesis. J. Virol. 83, 734-747
112. Backovic, M., Longnecker, R., and Jardetzky, T. S. (2009) Structure of a trimeric variant of the Epstein-Barr virus glycoprotein B. Proc. Natl. Acad. Sci. U.S.A. 106, 2880-2885
113. Magrané, J., Casaroli-Marano, R. P., Reina, M., Gåfvels, M., and Vilaró, S. (1999) The role of O-linked sugars in determining the very low density lipoprotein receptor stability or release from the cell. FEBS Lett. 451, 56-62
114. Schuman, J., Qiu, D., Koganty, R. R., Longenecker, B. M., and Campbell, A. P. (2000) Glycosylations versus conformational preferences of cancer associated mucin core. Glycoconj. J. 17, 835- 848
115. Fournillier, A., Wychowski, C., Boucreux, D., Baumert, T. F., Meunier, J. C., Jacobs, D., Muguet, S., Depla, E., and Inchauspé, G. (2001) Induction of hepatitis C virus E1 envelope protein-specific immune response can be enhanced by mutation of N-glycosylation sites. J. Virol. 75, 12088-12097
116. Bradel-Tretheway, B. G., Liu, Q., Stone, J. A., McInally, S., and Aguilar, H. C. (2015) Novel functions of Hendra virus G N-Glycans and comparisons to Nipah virus. J. Virol. 89, 7235-7247
117. Fowler, W. J., Garcia-Valcarcel, M., Hill-Perkins, M. S., Murphy, G., Harper, D. R., Jeffries, D. J., Burns, N. R., Adams, S. E., Kingsman, A. J., and Layton, G. T. (1995) Identification of immunodominant regions and linear B cell epitopes of the gE envelope protein of varicella-zoster virus. Virology 214, 531-540
118. Garcia-Valcarcel, M., Fowler, W. J., Harper, D. R., Jeffries, D. J., and Layton, G. T. (1997) Induction of neutralizing antibody and T-cell responses to varicella-zoster virus (VZV) using Ty-virus-like particles carrying fragments of glycoprotein E (gE). Vaccine 15, 709-719
119. Nejatollahi, F., Hodgetts, S. J., Vallely, P. J., and Burnie, J. P. (2002) Neutralising human recombinant antibodies to human cytomegalovirus glycoproteins gB and gH. FEMS Immunol. Med. Microbiol. 34, 237-244
120. Xing, Y., Oliver, S. L., Nguyen, T., Ciferri, C., Nandi, A., Hickman, J., Giovani, C., Yang, E., Palladino, G., Grose, C., Uematsu, Y., Lilja, A. E., Arvin, A. M., and Carfí, A. (2015) A site of varicella-zoster virus vulnerability identified by structural studies of neutralizing antibodies bound to the glycoprotein complex gHgL. Proc. Natl. Acad. Sci. U.S.A. 112, 6056-6061
121. Cló, E., Kracun, S. K., Nudelman, A. S., Jensen, K. J., Liljeqvist, J. Å., Olofsson, S., Bergström, T., and Blixt, O. (2012) Characterization of the viral O-glycopeptidome: a novel tool of relevance for vaccine design and serodiagnosis. J. Virol. 86, 6268-6278
122. D'Arrigo, I., Cló, E., Bergström, T., Olofsson, S., and Blixt, O. (2013)Diverse IgG serum response to novel glycopeptide epitopes detected within immunodominant stretches of Epstein-Barr virus glycoprotein 350/220: diagnostic potential of O-glycopeptide microarrays. Glycoconj. J. 30, 633-640
123. Norberg, P., Olofsson, S., Tarp, M. A., Clausen, H., Bergström, T., and Liljeqvist, J. A. (2007) Glycoprotein I of herpes simplex virus type 1 containsa unique polymorphic tandem-repeated mucin region. J. Gen. Virol. 88, 1683-1688
124. Norberg, P. (2010) Divergence and genotyping of human alpha-herpesviruses: an overview. Infect. Genet. Evol. 10, 14-25
125. Yang, Z., Wang, S., Halim, A., Schulz, M. A., Frodin, M., Rahman, S. H., Vester-Christensen, M. B., Behrens, C., Kristensen, C., Vakhrushev, S. Y., Bennett, E. P., Wandall, H. H., and Clausen, H. (2015) Engineered CHO cells for production of diverse, homogeneous glycoproteins. Nat. Biotechnol. 33, 842- 844
126. Sharma, S., Wisner, T. W., Johnson, D. C., and Heldwein, E. E. (2013)HCMV gB shares structural and functional properties with gB proteins from other herpesviruses. Virology 435, 239-249
127. Matsuura, H., Kirschner, A. N., Longnecker, R., and Jardetzky, T. S. (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
128. Szakonyi, G., Klein, M. G., Hannan, J. P., Young, K. A., Ma, R. Z., Asokan, R., Holers, V. M., and Chen, X. S. (2006) Structure of the Epstein-Barr virus major envelope glycoprotein. Nat. Struct. Mol. Biol. 13, 996-1001
129. Litwin, V., Jackson, W., and Grose, C. (1992) Receptor properties of two varicella-zoster virus glycoproteins, gpI and gpIV, homologous to herpes simplex virus gE and gI. J. Virol. 66, 3643-3651
130. Christensen, J., Steain, M., Slobedman, B., and Abendroth, A. (2013)Varicella-zoster virus glycoprotein I is essential for spread in dorsal root ganglia and facilitates axonal localization of structural virion components in neuronal cultures. J. Virol. 87, 13719-13728
131. Wille, P. T., Wisner, T. W., Ryckman, B., and Johnson, D. C. (2013)Human cytomegalovirus (HCMV) glycoprotein gB promotes virus entry in trans acting as the viral fusion protein rather than as a receptor-binding protein. mBio 4, e00332- 00313
132. Vanarsdall, A. L., Ryckman, B. J., Chase, M. C., and Johnson, D. C. (2008)Human cytomegalovirus glycoproteins gB and gH/gL mediate epithelial cell-cell fusion when expressed either in cis or in trans. J. Virol. 82, 11837-11850
133. Mach, M., Kropff, B., Kryzaniak, M., and Britt, W. (2005) Complex formation by glycoproteins M and N of human cytomegalovirus: structural and functional aspects. J. Virol. 79, 2160-2170
134. Engel, P., Pérez-Carmona, N., Albà, M. M., Robertson, K., Ghazal, P., and Angulo, A. (2011) Human cytomegalovirus UL7, a homologue of the SLAM-family receptor CD229, impairs cytokine production. Immunol. Cell Biol. 89, 753-766
135. MacManiman, J. D., Meuser, A., Botto, S., Smith, P. P., Liu, F., Jarvis, M. A., Nelson, J. A., and Caposio, P. (2014) Human cytomegalovirusencoded pUL7 is a novel CEACAM1-like molecule responsible for promotion of angiogenesis. mBio 5, e02035
136. Fielding, C. A., Aicheler, R., Stanton, R. J., Wang, E. C., Han, S., Seirafian, S., Davies, J., McSharry, B. P., Weekes, M. P., Antrobus, P. R., Prod'homme, V., Blanchet, F. P., Sugrue, D., Cuff, S., Roberts, D., et al. (2014) Two novel human cytomegalovirus NK cell evasion functions target MICA for lysosomal degradation. PLoS Pathog. 10, e1004058
137. Li, G., Nguyen, C. C., Ryckman, B. J., Britt, W. J., and Kamil, J. P. (2015) A viral regulator of glycoprotein complexes contributes to human cytomegalovirus cell tropism. Proc. Natl. Acad. Sci. U.S.A. 112, 4471-4476
138. Noriega, V. M., Hesse, J., Gardner, T. J., Besold, K., Plachter, B., and Tortorella, D. (2012) Human cytomegalovirus US3 modulates destruction of MHC class I molecules. Mol. Immunol. 51, 245-253
139. Bronzini, M., Luganini, A., Dell'Oste, V., De Andrea, M., Landolfo, S., and Gribaudo, G. (2012) The US16 gene of human cytomegalovirus is required for efficient viral infection of endothelial and epithelial cells. J. Virol. 86, 6875-6888
140. Noriega, V. M., Gardner, T. J., Redmann, V., Bongers, G., Lira, S. A., and Tortorella, D. (2014) Human cytomegalovirus US28 facilitates cell-tocell viral dissemination. Viruses 6, 1202-1218
141. Borza, C. M., and Hutt-Fletcher, L. M. (1998) Epstein-Barr virus recombinant lacking expression of glycoprotein gp150 infects B cells normally but is enhanced for infection of epithelial cells. J. Virol. 72, 7577-7582