Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans

doi:10.1083/jcb.116.5.1273

This Article

	Full Text (PDF, 1067K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Shieh, M. T.
	Articles by Spear, P. G.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Shieh, M. T.
	Articles by Spear, P. G.


Social Bookmarking

	What's this?

ARTICLES

Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans

MT Shieh, D WuDunn, RI Montgomery, JD Esko and PG Spear
Department of Microbiology-Immunology, Northwestern University Medical School, Chicago, Illinois 60611.

The role of cell surface heparan sulfate in herpes simplex virus (HSV) infection was investigated using CHO cell mutants defective in various aspects of glycosaminoglycan synthesis. Binding of radiolabeled virus to the cells and infection were assessed in mutant and wild-type cells. Virus bound efficiently to wild-type cells and initiated an abortive infection in which immediate-early or alpha viral genes were expressed, despite limited production of late viral proteins and progeny virus. Binding of virus to heparan sulfate-deficient mutant cells was severely impaired and mutant cells were resistant to HSV infection. Intermediate levels of binding and infection were observed for a CHO cell mutant that produced undersulfated heparan sulfate. These results show that heparan sulfate moieties of cell surface proteoglycans serve as receptors for HSV.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Kalia, M., Chandra, V., Rahman, S. A., Sehgal, D., Jameel, S. (2009). Heparan Sulfate Proteoglycans Are Required for Cellular Binding of the Hepatitis E Virus ORF2 Capsid Protein and for Viral Infection. J. Virol. 83: 12714-12724 [Abstract] [Full Text]
Fan, Q., Lin, E., Satoh, T., Arase, H., Spear, P. G. (2009). Differential Effects on Cell Fusion Activity of Mutations in Herpes Simplex Virus 1 Glycoprotein B (gB) Dependent on Whether a gD Receptor or a gB Receptor Is Overexpressed. J. Virol. 83: 7384-7390 [Abstract] [Full Text]
Mok, W., Stylianopoulos, T., Boucher, Y., Jain, R. K. (2009). Mathematical Modeling of Herpes Simplex Virus Distribution in Solid Tumors: Implications for Cancer Gene Therapy. Clin. Cancer Res. 15: 2352-2360 [Abstract] [Full Text]
Stiles, J., Guptill-Yoran, L., Moore, G. E., Pogranichniy, R. M. (2008). Effects of {lambda}-Carrageenan on In Vitro Replication of Feline Herpesvirus and on Experimentally Induced Herpetic Conjunctivitis in Cats. IOVS 49: 1496-1501 [Abstract] [Full Text]
Jovasevic, V., Liang, L., Roizman, B. (2008). Proteolytic Cleavage of VP1-2 Is Required for Release of Herpes Simplex Virus 1 DNA into the Nucleus. J. Virol. 82: 3311-3319 [Abstract] [Full Text]
Ono, E., Tomioka, Y., Watanabe, Y., Amagai, K., Morimatsu, M., Shinya, K., Cherel, P. (2007). Comparison of the antiviral potentials among the pseudorabies-resistant transgenes encoding different soluble forms of porcine nectin-1 in transgenic mice. J. Gen. Virol. 88: 2636-2641 [Abstract] [Full Text]
Cheshenko, N., Liu, W., Satlin, L. M., Herold, B. C. (2007). Multiple Receptor Interactions Trigger Release of Membrane and Intracellular Calcium Stores Critical for Herpes Simplex Virus Entry. Mol. Biol. Cell 18: 3119-3130 [Abstract] [Full Text]
Tiwari, V., O'Donnell, C., Copeland, R. J., Scarlett, T., Liu, J., Shukla, D. (2007). Soluble 3-O-sulfated heparan sulfate can trigger herpes simplex virus type 1 entry into resistant Chinese hamster ovary (CHO-K1) cells. J. Gen. Virol. 88: 1075-1079 [Abstract] [Full Text]
Finnen, R. L., Mizokami, K. R., Banfield, B. W., Cai, G.-Y., Simpson, S. A., Pizer, L. I., Levin, M. J. (2006). Postentry events are responsible for restriction of productive varicella-zoster virus infection in chinese hamster ovary cells.. J. Virol. 80: 10325-10334 [Abstract] [Full Text]
Tiwari, V., Clement, C., Xu, D., Valyi-Nagy, T., Yue, B. Y. J. T., Liu, J., Shukla, D. (2006). Role for 3-o-sulfated heparan sulfate as the receptor for herpes simplex virus type 1 entry into primary human corneal fibroblasts.. J. Virol. 80: 8970-8980 [Abstract] [Full Text]
Jenssen, H., Hamill, P., Hancock, R. E. W. (2006). Peptide Antimicrobial Agents. Clin. Microbiol. Rev. 19: 491-511 [Abstract] [Full Text]
Kwon, H., Bai, Q., Baek, H.-J., Felmet, K., Burton, E. A., Goins, W. F., Cohen, J. B., Glorioso, J. C. (2006). Soluble V Domain of Nectin-1/HveC Enables Entry of Herpes Simplex Virus Type 1 (HSV-1) into HSV-Resistant Cells by Binding to Viral Glycoprotein D. J. Virol. 80: 138-148 [Abstract] [Full Text]
Aravalli, R. N., Hu, S., Rowen, T. N., Palmquist, J. M., Lokensgard, J. R. (2005). Cutting Edge: TLR2-Mediated Proinflammatory Cytokine and Chemokine Production by Microglial Cells in Response to Herpes Simplex Virus. J. Immunol. 175: 4189-4193 [Abstract] [Full Text]
Bergefall, K., Trybala, E., Johansson, M., Uyama, T., Naito, S., Yamada, S., Kitagawa, H., Sugahara, K., Bergstrom, T. (2005). Chondroitin Sulfate Characterized by the E-disaccharide Unit Is a Potent Inhibitor of Herpes Simplex Virus Infectivity and Provides the Virus Binding Sites on gro2C Cells. J. Biol. Chem. 280: 32193-32199 [Abstract] [Full Text]
Conner, J., Rixon, F. J., Brown, S. M. (2005). Herpes Simplex Virus Type 1 Strain HSV1716 Grown in Baby Hamster Kidney Cells Has Altered Tropism for Nonpermissive Chinese Hamster Ovary Cells Compared to HSV1716 Grown in Vero Cells. J. Virol. 79: 9970-9981 [Abstract] [Full Text]
Zahn, A., Allain, J.-P. (2005). Hepatitis C virus and hepatitis B virus bind to heparin: purification of largely IgG-free virions from infected plasma by heparin chromatography. J. Gen. Virol. 86: 677-685 [Abstract] [Full Text]
Ono, E., Amagai, K., Taharaguchi, S., Tomioka, Y., Yoshino, S., Watanabe, Y., Cherel, P., Houdebine, L.-M., Adam, M., Eloit, M., Inobe, M., Uede, T. (2004). Transgenic mice expressing a soluble form of porcine nectin-1/herpesvirus entry mediator C as a model for pseudorabies-resistant livestock. Proc. Natl. Acad. Sci. USA 101: 16150-16155 [Abstract] [Full Text]
Bundesen, L. Q. (2004). Inaugural Article: Biography of Patricia G. Spear. Proc. Natl. Acad. Sci. USA 101: 12411-12413 [Full Text]
Tiwari, V., Clement, C., Duncan, M. B., Chen, J., Liu, J., Shukla, D. (2004). A role for 3-O-sulfated heparan sulfate in cell fusion induced by herpes simplex virus type 1. J. Gen. Virol. 85: 805-809 [Abstract] [Full Text]
Wei, H.-Y., Jiang, L.-F., Fang, D.-Y., Guo, H.-Y. (2003). Dengue virus type 2 infects human endothelial cells through binding of the viral envelope glycoprotein to cell surface polypeptides. J. Gen. Virol. 84: 3095-3098 [Abstract] [Full Text]
Yoon, M., Zago, A., Shukla, D., Spear, P. G. (2003). Mutations in the N Termini of Herpes Simplex Virus Type 1 and 2 gDs Alter Functional Interactions with the Entry/Fusion Receptors HVEM, Nectin-2, and 3-O-Sulfated Heparan Sulfate but Not with Nectin-1. J. Virol. 77: 9221-9231 [Abstract] [Full Text]
Zago, A., Spear, P. G. (2003). Differences in the N Termini of Herpes Simplex Virus Type 1 and 2 gDs That Influence Functional Interactions with the Human Entry Receptor Nectin-2 and an Entry Receptor Expressed in Chinese Hamster Ovary Cells. J. Virol. 77: 9695-9699 [Abstract] [Full Text]
Nicola, A. V., McEvoy, A. M., Straus, S. E. (2003). Roles for Endocytosis and Low pH in Herpes Simplex Virus Entry into HeLa and Chinese Hamster Ovary Cells. J. Virol. 77: 5324-5332 [Abstract] [Full Text]
Herold, B. C., Scordi-Bello, I., Cheshenko, N., Marcellino, D., Dzuzelewski, M., Francois, F., Morin, R., Casullo, V. M., Anderson, R. A., Chany, C. II, Waller, D. P., Zaneveld, L. J. D., Klotman, M. E. (2002). Mandelic Acid Condensation Polymer: Novel Candidate Microbicide for Prevention of Human Immunodeficiency Virus and Herpes Simplex Virus Entry. J. Virol. 76: 11236-11244 [Abstract] [Full Text]
Xia, G., Chen, J., Tiwari, V., Ju, W., Li, J.-P., Malmstrom, A., Shukla, D., Liu, J. (2002). Heparan Sulfate 3-O-Sulfotransferase Isoform 5 Generates Both an Antithrombin-binding Site and an Entry Receptor for Herpes Simplex Virus, Type 1. J. Biol. Chem. 277: 37912-37919 [Abstract] [Full Text]
Cheshenko, N., Herold, B. C. (2002). Glycoprotein B plays a predominant role in mediating herpes simplex virus type 2 attachment and is required for entry and cell-to-cell spread. J. Gen. Virol. 83: 2247-2255 [Abstract] [Full Text]
Jnaoui, K., Minet, M., Michiels, T. (2002). Mutations That Affect the Tropism of DA and GDVII Strains of Theiler's Virus In Vitro Influence Sialic Acid Binding and Pathogenicity. J. Virol. 76: 8138-8147 [Abstract] [Full Text]
Anderson, R. A., Feathergill, K. A., Diao, X.-H., Cooper, M. D., Kirkpatrick, R., Herold, B. C., Doncel, G. F., Chany, C. J., Waller, D. P., Rencher, W. F., Zaneveld, L. J.D. (2002). Preclinical Evaluation of Sodium Cellulose Sulfate (Ushercell) as a Contraceptive Antimicrobial Agent. J Androl 23: 426-438 [Abstract] [Full Text]
Dennissen, M. A. B. A., Jenniskens, G. J., Pieffers, M., Versteeg, E. M. M., Petitou, M., Veerkamp, J. H., van Kuppevelt, T. H. (2002). Large, Tissue-regulated Domain Diversity of Heparan Sulfates Demonstrated by Phage Display Antibodies. J. Biol. Chem. 277: 10982-10986 [Abstract] [Full Text]
Birkmann, A., Mahr, K., Ensser, A., Titgemeyer, F., Fleckenstein, B., Neipel, F. (2001). Cell Surface Heparan Sulfate Is a Receptor for Human Herpesvirus 8 and Interacts with Envelope Glycoprotein K8.1. J. Virol. 75: 11583-11593 [Abstract] [Full Text]
Tolba, K. A., Bowers, W. J., Hilchey, S. P., Halterman, M. W., Howard, D. F., Giuliano, R. E., Federoff, H. J., Rosenblatt, J. D. (2001). Development of herpes simplex virus-1 amplicon-based immunotherapy for chronic lymphocytic leukemia. Blood 98: 287-295 [Abstract] [Full Text]
Schwartz, J. A., Lium, E. K., Silverstein, S. J. (2001). Herpes Simplex Virus Type 1 Entry Is Inhibited by the Cobalt Chelate Complex CTC-96. J. Virol. 75: 4117-4128 [Abstract] [Full Text]
Kingham, B. F., Zelnik, V., Kopácek, J., Majerciak, V., Ney, E., Schmidt, C. J. (2001). The genome of herpesvirus of turkeys: comparative analysis with Marek's disease viruses. J. Gen. Virol. 82: 1123-1135 [Abstract] [Full Text]
Bultmann, H., Busse, J. S., Brandt, C. R. (2001). Modified FGF4 Signal Peptide Inhibits Entry of Herpes Simplex Virus Type 1. J. Virol. 75: 2634-2645 [Abstract] [Full Text]
Giroglou, T., Florin, L., Schäfer, F., Streeck, R. E., Sapp, M. (2001). Human Papillomavirus Infection Requires Cell Surface Heparan Sulfate. J. Virol. 75: 1565-1570 [Abstract] [Full Text]
Rauch, D. A., Rodriguez, N., Roller, R. J. (2000). Mutations in Herpes Simplex Virus Glycoprotein D Distinguish Entry of Free Virus from Cell-Cell Spread. J. Virol. 74: 11437-11446 [Abstract] [Full Text]
Biller, M., Mardberg, K., Hassan, H., Clausen, H., Bolmstedt, A., Bergstrom, T., Olofsson, S. (2000). Early steps in O-linked glycosylation and clustered O-linked glycans of herpes simplex virus type 1 glycoprotein C: effects on glycoprotein properties. Glycobiology 10: 1259-1269 [Abstract] [Full Text]
Stray, S. J., Cummings, R. D., Air, G. M. (2000). Influenza virus infection of desialylated cells. Glycobiology 10: 649-658 [Abstract] [Full Text]
McCormick, C. J., Newbold, C. I., Berendt, A. R. (2000). Sulfated glycoconjugates enhance CD36-dependent adhesion of Plasmodium falciparum-infected erythrocytes to human microvascular endothelial cells. Blood 96: 327-333 [Abstract] [Full Text]
Schneider-Schaulies, J. (2000). Cellular receptors for viruses: links to tropism and pathogenesis. J. Gen. Virol. 81: 1413-1429 [Full Text]
Stephens, R. S., Fawaz, F. S., Kennedy, K. A., Koshiyama, K., Nichols, B., van Ooij, C., Engel, J. N. (2000). Eukaryotic Cell Uptake of Heparin-Coated Microspheres: a Model of Host Cell Invasion by Chlamydia trachomatis. Infect. Immun. 68: 1080-1085 [Abstract] [Full Text]
Lander, A. D., Selleck, S. B. (2000). The Elusive Functions of Proteoglycans: In Vivo Veritas. JCB 148: 227-232 [Full Text]
Vazquez, M.-I., Esteban, M. (1999). Identification of Functional Domains in the 14-Kilodalton Envelope Protein (A27L) of Vaccinia Virus. J. Virol. 73: 9098-9109 [Abstract] [Full Text]
Nixdorf, R., Schmidt, J., Karger, A., Mettenleiter, T. C. (1999). Infection of Chinese Hamster Ovary Cells by Pseudorabies Virus. J. Virol. 73: 8019-8026 [Abstract] [Full Text]
Jan, J.-T., Byrnes, A. P., Griffin, D. E. (1999). Characterization of a Chinese Hamster Ovary Cell Line Developed by Retroviral Insertional Mutagenesis That Is Resistant to Sindbis Virus Infection. J. Virol. 73: 4919-4924 [Abstract] [Full Text]
Bai, X., Wei, G., Sinha, A., Esko, J. D. (1999). Chinese Hamster Ovary Cell Mutants Defective in Glycosaminoglycan Assembly and Glucuronosyltransferase I. J. Biol. Chem. 274: 13017-13024 [Abstract] [Full Text]
Shukla, D., Rowe, C. L., Dong, Y., Racaniello, V. R., Spear, P. G. (1999). The Murine Homolog (Mph) of Human Herpesvirus Entry Protein B (HveB) Mediates Entry of Pseudorabies Virus but Not Herpes Simplex Virus Types 1�and 2. J. Virol. 73: 4493-4497 [Abstract] [Full Text]
Laquerre, S., Anderson, D. B., Stolz, D. B., Glorioso, J. C. (1998). Recombinant Herpes Simplex Virus Type 1�Engineered for Targeted Binding to Erythropoietin Receptor-Bearing Cells. J. Virol. 72: 9683-9697 [Abstract] [Full Text]
Krummenacher, C., Nicola, A. V., Whitbeck, J. C., Lou, H., Hou, W., Lambris, J. D., Geraghty, R. J., Spear, P. G., Cohen, G. H., Eisenberg, R. J. (1998). Herpes Simplex Virus Glycoprotein D Can Bind to Poliovirus Receptor-Related Protein 1�or Herpesvirus Entry Mediator, Two Structurally Unrelated Mediators of Virus Entry. J. Virol. 72: 7064-7074 [Abstract] [Full Text]
Karger, A., Schmidt, J., Mettenleiter, T. C. (1998). Infectivity of a Pseudorabies Virus Mutant Lacking Attachment Glycoproteins C and D. J. Virol. 72: 7341-7348 [Abstract] [Full Text]
Byrnes, A. P., Griffin, D. E. (1998). Binding of Sindbis Virus to Cell Surface Heparan Sulfate. J. Virol. 72: 7349-7356 [Abstract] [Full Text]
Terry-Allison, T., Montgomery, R. I., Whitbeck, J. C., Xu, R., Cohen, G. H., Eisenberg, R. J., Spear, P. G. (1998). HveA (Herpesvirus Entry Mediator A), a Coreceptor for Herpes Simplex Virus Entry, also Participates in Virus-Induced Cell Fusion. J. Virol. 72: 5802-5810 [Abstract] [Full Text]
Laquerre, S., Argnani, R., Anderson, D. B., Zucchini, S., Manservigi, R., Glorioso, J. C. (1998). Heparan Sulfate Proteoglycan Binding by Herpes Simplex Virus Type 1�Glycoproteins B and C, Which Differ in Their Contributions to Virus Attachment, Penetration, and Cell-to-Cell Spread. J. Virol. 72: 6119-6130 [Abstract] [Full Text]
Geraghty, R. J., Krummenacher, C., Cohen, G. H., Eisenberg, R. J., Spear, P. G. (1998). Entry of Alphaherpesviruses Mediated by Poliovirus Receptor-Related Protein 1 and Poliovirus Receptor. Science 280: 1618-1620 [Abstract] [Full Text]
Ji, Z.-S., Pitas, R. E., Mahley, R. W. (1998). Differential Cellular Accumulation/Retention of Apolipoprotein E Mediated by Cell Surface Heparan Sulfate Proteoglycans. APOLIPOPROTEINS E3 AND E2 GREATER THAN E4. J. Biol. Chem. 273: 13452-13460 [Abstract] [Full Text]
Neff, S., Sa-Carvalho, D., Rieder, E., Mason, P. W., Blystone, S. D., Brown, E. J., Baxt, B. (1998). Foot-and-Mouth Disease Virus Virulent for Cattle Utilizes the Integrin alpha vbeta 3 as Its Receptor. J. Virol. 72: 3587-3594 [Abstract] [Full Text]
Nicola, A. V., Ponce de Leon, M., Xu, R., Hou, W., Whitbeck, J. C., Krummenacher, C., Montgomery, R. I., Spear, P. G., Eisenberg, R. J., Cohen, G. H. (1998). Monoclonal Antibodies to Distinct Sites on Herpes Simplex Virus (HSV) Glycoprotein D Block HSV Binding to HVEM. J. Virol. 72: 3595-3601 [Abstract] [Full Text]
Brunetti, C. R., Dingwell, K. S., Wale, C., Graham, F. L., Johnson, D. C. (1998). Herpes Simplex Virus gD and Virions Accumulate in Endosomes by Mannose 6-Phosphate-Dependent and -Independent Mechanisms. J. Virol. 72: 3330-3339 [Abstract] [Full Text]
Immergluck, L., Domowicz, M., Schwartz, N., Herold, B. (1998). Viral and cellular requirements for entry of herpes simplex virus type 1 into primary neuronal cells. J. Gen. Virol. 79: 549-559 [Abstract]
Roller, R. J., Rauch, D. (1998). Herpesvirus Entry Mediator HVEM Mediates Cell-Cell Spread in BHK(TK-) Cell Clones. J. Virol. 72: 1411-1417 [Abstract] [Full Text]
Summerford, C., Samulski, R. J. (1998). Membrane-Associated Heparan Sulfate Proteoglycan Is a Receptor for Adeno-Associated Virus Type 2�Virions. J. Virol. 72: 1438-1445 [Abstract] [Full Text]
Chung, C.-S., Hsiao, J.-C., Chang, Y.-S., Chang, W. (1998). A27L Protein Mediates Vaccinia Virus Interaction with Cell Surface Heparan Sulfate. J. Virol. 72: 1577-1585 [Abstract] [Full Text]
Feyzi, E., Trybala, E., Bergstrom, T., Lindahl, U., Spillmann, D. (1997). Structural Requirement of Heparan Sulfate for Interaction with Herpes Simplex Virus Type 1�Virions and Isolated Glycoprotein C. J. Biol. Chem. 272: 24850-24857 [Abstract] [Full Text]
Ho, G., Broze Jr., G. J., Schwartz, A. L. (1997). Role of Heparan Sulfate Proteoglycans in the Uptake and Degradation of Tissue Factor Pathway Inhibitor-Coagulation Factor Xa Complexes. J. Biol. Chem. 272: 16838-16844 [Abstract] [Full Text]
Chen, T., Grunert, F., Medina-Marino, A., Gotschlich, E. C. (1997). Several Carcinoembryonic Antigens (CD66) Serve as Receptors for Gonococcal Opacity Proteins. JEM 185: 1557-1564 [Abstract] [Full Text]
Sodeik, B., Ebersold, M. W., Helenius, A. (1997). Microtubule-mediated Transport of Incoming Herpes Simplex Virus 1 Capsids to the Nucleus. JCB 136: 1007-1021 [Abstract] [Full Text]
Sosnowski, B. A., Gonzalez, A. M., Chandler, L. A., Buechler, Y. J., Pierce, G. F., Baird, A. (1996). Targeting DNA to Cells with Basic Fibroblast Growth Factor (FGF2). J. Biol. Chem. 271: 33647-33653 [Abstract] [Full Text]
Chen, J. C.-R., Zhang, J. P., Stephens, R. S. (1996). Structural Requirements of Heparin Binding to Chlamydia trachomatis. J. Biol. Chem. 271: 11134-11140 [Abstract] [Full Text]
Edwards, I. J., Xu, H., Obunike, J. C., Goldberg, I. J., Wagner, W. D. (1995). Differentiated Macrophages Synthesize a Heparan Sulfate Proteoglycan and an Oversulfated Chondroitin Sulfate Proteoglycan That Bind Lipoprotein Lipase. Arterioscler. Thromb. Vasc. Bio. 15: 400-409 [Abstract] [Full Text]
Elenius, K, Jalkanen, M (1994). Function of the syndecans--a family of cell surface proteoglycans. J. Cell Sci. 107: 2975-2982
Wei, G., Bai, X., Gabb, M. M. G., Bame, K. J., Koshy, T. I., Spear, P. G., Esko, J. D. (2000). Location of the Glucuronosyltransferase Domain in the Heparan Sulfate Copolymerase EXT1 by Analysis of Chinese Hamster Ovary Cell Mutants. J. Biol. Chem. 275: 27733-27740 [Abstract] [Full Text]