Microbial Subversion of Heparan Sulfate Proteoglycans

  • Chen, Ye (Department of Digestive Diseases, Nanfang Hospital, Southern Medical University) ;
  • Gotte, Martin (Department of Gynecology and Obstetrics, Munster University Medical Center) ;
  • Liu, Jian (Division of Medicinal Chemistry and Natural Products, University of North Carolina) ;
  • Park, Pyong Woo (Division of Respiratory Diseases, Children's Hospital, Harvard Medical School)
  • Received : 2008.09.15
  • Accepted : 2008.09.18
  • Published : 2008.11.30

Abstract

The interactions between the host and microbial pathogen largely dictate the onset, progression, and outcome of infectious diseases. Pathogens subvert host components to promote their pathogenesis and, among these, cell surface heparan sulfate proteoglycans are exploited by many pathogens for their initial attachment and subsequent cellular entry. The ability to interact with heparan sulfate proteoglycans is widespread among viruses, bacteria, and parasites. Certain pathogens also use heparan sulfate proteoglycans to evade host defense mechanisms. These findings suggest that heparan sulfate proteoglycans are critical in microbial pathogenesis, and that heparan sulfate proteoglycan-pathogen interactions are potential targets for novel prophylactic and therapeutic approaches.

Keywords

adhesin;cellular entry;heparan sulfate;host defense;microbial pathogenesis;proteoglycan;syndecan;virulence factor

Acknowledgement

Supported by : National Institutes of Health

References

  1. Alonso, S., Reveneau, N., Pethe, K., and Locht, C. (2002). Eightykilodalton N-terminal moiety of Bordetella pertussis filamentous hemagglutinin: adherence, immunogenicity, and protective role. Infect. Immun. 70,4142-4147 https://doi.org/10.1128/IAI.70.8.4142-4147.2002
  2. Andrianov, AM., and Veresov, V.G. (2007). Structural analysis of the HIV-1 gp120 V3loop: application to the HIV-Haiti isolates. J. Biomol. Struct. Dyn. 24, 597-608 https://doi.org/10.1080/07391102.2007.10507149
  3. Asokan, A, Hamra, J.B., Govindasamy, L., Agbandje-McKenna, M., and Samulski, R.J. (2006). Adeno-associated virus type 2 contains an integrin alpha5beta1 binding domain essential for Virol cell entry. J. Virol. 80, 8961-8969 https://doi.org/10.1128/JVI.00843-06
  4. Avirutnan, P., Zhang, L., Punyadee, N., Manuyakorn, A, Puttikhunt, C., Kasinrerk, W., Malasit, P., Atkinson, J.P., and Diamond, M.S. (2007). Secreted NS1 of dengue virus attaches to the surface of cells via interactions with heparan sulfate and chondroitin sulfate E. PLoS Pathog. 3, 1798-1812
  5. Bartlett, A.H., Foster, T.J., Hayashida, A, and Park, P.W. (2008). Alpha-toxin facilitates the generation of CXC chemokine gradients and stimulates neutrophil homing in Staphylococcus aureus pneumonia. J. Infect. Dis. (in press)
  6. Bernfield, M., Gotte, M., Park, P.W., Reizes, O., Fitzgerald, M.L, Lincecum, J., and Zako, M. (1999). Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68, 729-777 https://doi.org/10.1146/annurev.biochem.68.1.729
  7. Bhanot, P., and Nussenzweig, V. (2002). Plasmodium yoelii sporozoites infect Syndecan-1 deficient mice. Mol. Biochem. Parasitol. 123,143-144 https://doi.org/10.1016/S0166-6851(02)00132-9
  8. Chen, J.C., and Stephens, R.S. (1997). Chlamydia trachomatis glycosaminoglycan-dependent and independent attachment to eukaryotic cells. Microb. Pathog. 22, 23-30 https://doi.org/10.1006/mpat.1996.0087
  9. Chen, Y., Hayashida, A, Bennett, A.E., Hollingshead, S.K, and Park, P.W. (2007). Streptococcus pneumoniae sheds syndecan-1 ectodomains through ZmpC, a metalloproteinase virulence factor. J. BioI. Chem. 282, 159-167 https://doi.org/10.1074/jbc.M608542200
  10. Copeland, R., Balasubramaniam, A, Tiwari, V., Zhang, F., Bridges, A, Linhardt, R.J., Shukla, D., and Liu, J. (2008). Using a 3-Osulfated heparin octasaccharide to inhibit the entry of herpes simplex virus type 1. Biochemistry 47, 5774-5783 https://doi.org/10.1021/bi800205t
  11. Crublet, E., Andrieu, J.P., Vives, R.R., and Lortat-Jacob, H. (2008). The HIV-1 envelope glycoprotein gp120 features four heparan sulfate binding domains, including the co-receptor binding site. J. BioI. Chem. 283,15193-15200 https://doi.org/10.1074/jbc.M800066200
  12. de Agostini, A.I., Dong, J.C., de Vantery Arrighi, C., Ramus, M.A, Dentand-Quadri, I., Thalmann, S., Ventura, P., Ibecheole, V., Monge, F., Fischer, AM., et al. (2008). Human follicular fluid heparan sulfate contains abundant 3-O-sufated chains with anticoagulant activity. J. BioI. Chem. (in press)
  13. Grassme, H., Gulbins, E., Brenner, B., Ferlinz, K., Sand hoff, K., Harzer, K., Lang, F., and Meyer, T.F. (1997). Acidic sphingomyelinase mediates entry of N. gonorrhoeae into non phagocytic cells. Cell 91,605-615 https://doi.org/10.1016/S0092-8674(00)80448-1
  14. Ho, Y., Hsiao, J.C., Yang, M.H., Chung, C.S., Peng, Y.C., Lin, T.H., Chang, W, and Tzou, D.L. (2005). The oligomeric structure of vaccinia Virol envelope protein A27L is essential for binding to heparin and heparan sulfates on cell surfaces: a structural and functional approach using site-specific mutagenesis. J. Mol. BioI. 349, 1060-1071 https://doi.org/10.1016/j.jmb.2005.04.024
  15. Kirkpatrick, C.A, Knox, S.M., Staatz, W.D., Fox, B., Lercher, D.M., and Selleck, S.B. (2006). The function of a Drosophila glypican does not depend entirely on heparan sulfate modification. Dev. BioI. 300, 570-582 https://doi.org/10.1016/j.ydbio.2006.09.011
  16. Knappe, M., Bodevin, S., Selinka, H.C., Spillmann, D., Streeck, R.E., Chen, X.S., Lindahl, U., and Sapp, M. (2007). Surfaceexposed amino acid residues of HPV16 L 1 protein mediating interaction with cell surface heparan sulfate. J. BioI. Chem. 282, 27913-27922 https://doi.org/10.1074/jbc.M705127200
  17. Laquerre, S., Argnani, R., Anderson, D.B., Zucchini, S., Manservigi, R., and Glorioso, J.C. (1998). Heparan sulfate proteoglycan binding by herpes simplex virus type 1 glycoproteins Band C, which differ in their contributions to virus attachment, penetration, and cell-to-cell spread. J. Virol. 72, 6119-6130
  18. Maccarana, M., Sakura, Y., Tawada, A, Yoshida, K., and Lindahl, U. (1996). Domain structure of heparan sulfates from bovine organs. J. BioI. Chem. 271, 17804-17810 https://doi.org/10.1074/jbc.271.30.17804
  19. Menozzi, F.D., Reddy, V.M., Cayet, D., Raze, D., Debrie, A.S., Dehouck, M.P., Cecchelli, R., and Locht, C. (2006). Mycobacterium tuberculosis heparin-binding haemagglutinin adhesin (HBHA) triggers receptor-mediated transcytosis without altering the integrity of tight junctions. Microbes Infect. 8, 1-9 https://doi.org/10.1016/j.micinf.2005.03.023
  20. Pancake, S.J., Holt, G.D., Mellouk, S., and Hoffman, S.L. (1992). Malaria sporozoites and circumsporozoite proteins bind specifically to sulfated glycoconjugates. J. Cell BioI. 117, 1351-1357 https://doi.org/10.1083/jcb.117.6.1351
  21. Park, P.W., Pier, G.B., Preston, M.J., Goldberger, O., Fitzgerald, M.L., and Bernfield, M. (2000b). Syndecan-1 shedding is enhanced by LasA, a secreted virulence factor of Pseudomonas aeruginosa. J. BioI. Chem. 275, 3057-3064 https://doi.org/10.1074/jbc.275.5.3057
  22. Patel, V.N., Knox, S.M., Likar, K.M., Lathrop, C.A., Hossain, R., Eftekhari, S., Whitelock, J.M., Elkin, M., Vlodavsky, I., and Hoffman, M.P. (2007). Heparanase cleavage of perlecan heparan sulfate modulates FGF10 activity during ex vivo submandibular gland branching morphogenesis. Development 134,4177-4186 https://doi.org/10.1242/dev.011171
  23. Pethe, K., Alonso, S., Biet, F., Delogu, G., Brennan, M.J., Locht, C., and Menozzi, F.D. (2001). The heparin-binding haemagglutinin of M. tuberculosis is required for extrapulmonary dissemination. Nature 412,190-194 https://doi.org/10.1038/35084083
  24. Pinon, J.D., Klasse, P.J., Jassal, S.R., Welson, S., Weber, J., Brighty, D.W., and Sattentau, Q.J. (2003). Human T-cell leukemia virus type 1 envelope glycoprotein gp46 interacts with cell surface heparan sulfate proteoglycans. J. Virol. 77, 9922-9930 https://doi.org/10.1128/JVI.77.18.9922-9930.2003
  25. Ryman, K.D., Gardner, C.L., Burke, C.W., Meier, K.C., Thompson, J.M., and Klimstra, W.B. (2007). Heparan sulfate binding can contribute to the neurovirulence of neuroadapted and nonneuroadapted Sindbis viruses. J. Virol. 81, 3563-3573 https://doi.org/10.1128/JVI.02494-06
  26. Saphire, A.C., Bobardt, M.D., Zhang, Z., David, G., and Gallay, P.A. (2001). Syndecans serve as attachment receptors for human immunodeficiency virus type 1 on macrophages. J. Virol. 75, 9187-9200 https://doi.org/10.1128/JVI.75.19.9187-9200.2001
  27. Schulze, A, Gripon, P., and Urban, S. (2007). Hepatitis B virus infection initiates with a large surface protein-dependent binding to heparan sulfate proteoglycans. Hepatology 46,1759-1768 https://doi.org/10.1002/hep.21896
  28. Shafti-Keramat, S., Handisurya, A, Kriehuber, E., Meneguzzi, G., Siupetzky, K., and Kirnbauer, R. (2003). Different heparan sulfate proteoglycans serve as cellular receptors for human papillomaviruses. J. Virol. 77,13125-13135 https://doi.org/10.1128/JVI.77.24.13125-13135.2003
  29. Spear, P.G., Shieh, M.T, Herold, B.C., WuDunn, D., and Koshy, T.I. (1992). Heparan sulfate glycosaminoglycans as primary cell surface receptors for herpes simplex virus. Adv. Exp. Med. BioI. 313,341-353
  30. Spillmann, D. (2001). Heparan sulfate: anchor for Virol intruders? Biochimie 83, 811-817 https://doi.org/10.1016/S0300-9084(01)01290-1
  31. Taraktchoglou, M., Pacey, A.A., Turnbull, J.E., and Eley, A (2001). Infectivity of Chlamydia trachomatis serovar LGV but not E is dependent on host cell heparan sulfate. Infect. Immun. 69,968-976 https://doi.org/10.1128/IAI.69.2.968-976.2001
  32. Veettil, M.V., Sharma-Walia, N., Sadagopan, S., Raghu, H., Sivakumar, R., Naranatt, P.P., and Chandran, B. (2006). RhoA-GTPase facilitates entry of Kaposi's sarcoma-associated herpesvirus into adherent target cells in a Src-dependent manner. J. Virol. 80, 11432-11446 https://doi.org/10.1128/JVI.01342-06
  33. Weiland, M.E., Palm, J.E., Griffiths, W.J., McCaffery, J.M., and Svard, S.G. (2003). Characterisation of alpha-1 giardin: an immunodominant Giardia lamblia annexin with glycosaminoglycanbinding activity. Int. J. Parasitol. 33, 1341-1351 https://doi.org/10.1016/S0020-7519(03)00201-7
  34. Wuppermann, F.N., Hegemann, J.H., and Jantos, C.A. (2001). Heparan sulfate-like glycosaminoglycan is a cellular receptor for Chlamydiapneumoniae. J.lnfect. Dis. 184,181-187 https://doi.org/10.1086/322009
  35. Zautner, A.E., Jahn, B., Hammerschmidt, E., Wutzler, P., and Schmidtke, M. (2006). N- and 6-O-sulfated heparan sulfates mediate internalization of coxsackievirus B3 variant PD into CHO-K1 cells. J. Virol. 80, 6629-6636 https://doi.org/10.1128/JVI.01988-05
  36. Coppi, A, Tewari, R., Bishop, J.R., Bennett, B.L., Lawrence, R., Esko, J.D., Billker, O., and Sinnis, P. (2007). Heparan sulfate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells. Cell Host Microbe. 2, 316-327 https://doi.org/10.1016/j.chom.2007.10.002
  37. Crim, R.L., Audet, S.A, Feldman, S.A, Mostowski, H.S., and Beeler, J.A.(2007). Identification of linear heparin-binding peptides derived from human respiratory syncytial virus fusion glycoprotein that inhibit infectivity. J. Virol. 81,261-271 https://doi.org/10.1128/JVI.01226-06
  38. lozzo, R.V. (2005). Basement membrane proteoglycans: from cellar to ceiling. Nat. Rev. Mol. Cell BioI. 6, 646-656 https://doi.org/10.1038/nrm1702
  39. Jones, K.S., Petrow-Sadowski, C., Huang, YK, Bertolette, D.C., and Ruscetti, F.W. (2008). Cell-free HTLV-1 infects dendritic cells leading to transmission and transformation of CD4(+) T cells. Nat. Med. 14,429-436 https://doi.org/10.1038/nm1745
  40. O'Donnell, V., Larocco, M., and Baxt, B. (2008). Heparan sulfatebinding foot-and-mouth disease virus enters cells via caveolaemediated endocytosis. J. Virol. (in press)
  41. Tiwari, V., Clement, C., Xu, D., Valyi-Nagy, T., Vue, B.Y, Liu, J., and 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 https://doi.org/10.1128/JVI.00296-06
  42. Bishop, J.R., Crawford, B.E, and Esko, J.D. (2005). Cell surface heparan sulfate promotes replication of Toxoplasma gondii. Infect. Immun. 73,5395-5401 https://doi.org/10.1128/IAI.73.9.5395-5401.2005
  43. Boyle, K.A, and Compton, T. (1998). Receptor-binding properties of a soluble form of human cytomegalovirus glycoprotein B. J. Virol. 72,1826-1833
  44. Chen, Y., Maguire, T., Hileman, R.E., Fromm, J.R., Esko, J.D., Linhardt, R.J., and Marks, R.M. (1997). Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat. Med. 3, 866-871 https://doi.org/10.1038/nm0897-866
  45. Gotte, M. (2003). Syndecans in inflammation. FASEB J. 17,575-591 https://doi.org/10.1096/fj.02-0739rev
  46. Rostand, K.S., and Esko, J.D. (1997). Microbial adherence to and invasion through proteoglycans. Infect. Immun. 65, 1-8
  47. Takenouchi, N., Jones, K.S., Lisinski, I., Fugo, K., Yao, K., Cushman, S.W., Ruscetti, F.W., and Jacobson, S. (2007). GLUT1 is not the primary binding receptor but is associated with cell-tocell transmission of human T-cell leukemia virus type 1. J. Virol. 81,1506-1510 https://doi.org/10.1128/JVI.01522-06
  48. Bobardt, M.D., Saphire, A.C., Hung, H.C., Yu, X., Van der Schueren, B., Zhang, Z., David, G., and Gallay, P.A. (2003). Syndecan captures, protects, and transmits HIV to T lymphocytes. Immunity 18, 27-39 https://doi.org/10.1016/S1074-7613(02)00504-6
  49. Gallagher, J.T., and Lyon, M. (1989). Molecular organizations and functions of heparan sulphate. In Heparin, Chemical and Biological Properties: Clinical Applications, DA Lane, and U. Lindahl, eds. (London, UK; Edward Arnold, Ltd.), pp. 135-158
  50. Kim, H.R., Choi, M.S., and Kim, I.S. (2004). Role of syndecan-4 in the cellular invasion of Orientia tsutsugamushi. Microb. Pathog. 36,219-225 https://doi.org/10.1016/j.micpath.2003.12.005
  51. Leistner, C.M., Gruen-Bernhard, S., and Glebe, D. (2008). Role of glycosaminoglycans for binding and infection of hepatitis B virus. Cell. Microbiol. 10,122-133
  52. Bernfield, M., Kokenyesi, R., Kato, M., Hinkes, M.T, Spring, J., Gallo, R.L, and Lose, E.J. (1992). Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu. Rev. Cell BioI. 8, 365-393 https://doi.org/10.1146/annurev.cb.08.110192.002053
  53. Carruthers, V.B., Hakansson, S., Giddings, O.K, and Sibley, L.D. (2000). Toxoplasma gondii uses sulfated proteoglycans for substrate and host cell attachment. Infect. Immun. 68,4005-4011 https://doi.org/10.1128/IAI.68.7.4005-4011.2000
  54. Kim, C.W., Goldberger, O.A, Gallo, R.L., and Bernfield, M. (1994). Members of the syndecan family of heparan sulfate proteoglycans are expressed in distinct cell-, tissue-, and developmentspecific patterns. Mol. BioI. Cell. 5, 797-805 https://doi.org/10.1091/mbc.5.7.797
  55. O'Donnell, C.D., Tiwari, V., Oh, M.J., and Shukla, D. (2006). A role for heparan sulfate 3-O-sulfotransferase isoform 2 in herpes simplex virus type 1 entry and spread. Virology 346, 452-459 https://doi.org/10.1016/j.virol.2005.11.003
  56. Popova, T.G., Millis, B., Bradburne, C., Nazarenko, S., Bailey, C., Chandhoke, V., and Popov, S.G. (2006). Acceleration of epithelial cell syndecan-1 shedding by anthrax hemolytic virulence factors. BMC Microbiol. 6, 8-24 https://doi.org/10.1186/1471-2180-6-8
  57. van Putten, J.P., and Paul, S.M. (1995). Binding of syndecan-like cell surface proteoglycan receptors is required for Neisseria gonorrheae entry into human mucosal cells. EMBO J. 14,2144-2154
  58. de Haan, C.A, Haijema, B.J., Schellen, P., Schreur, P.W., te Lintelo, E., Vennema, H., and Rottier, P.J. (2008). Cleavage of group 1 coronavirus spike proteins: how furin cleavage is traded off against heparan sulfate binding upon cell culture adaptation. J. Virol. 82, 6078-6083 https://doi.org/10.1128/JVI.00074-08
  59. Moelleken, K., and Hegemann, J.H. (2008). The Chlamydia outer membrane protein OmcB is required for adhesion and exhibits biovar-specific differences in glycosaminoglycan binding. Mol. Microbiol. 67, 403-419 https://doi.org/10.1111/j.1365-2958.2007.06050.x
  60. Park, P.W., Reizes, O., and Bernfield, M. (2000a). Cell surface heparan sulfate proteoglycans: selective regulators of ligandreceptor encounters. J. BioI. Chem. 275, 29923-29926 https://doi.org/10.1074/jbc.R000008200
  61. Park, P.W., Pier, G.B., Hinkes, M.T., and Bernfield, M. (2001). Exploitation of syndecan-1 shedding by Pseudomonas aeruginosa enhances virulence. Nature 411, 98-102 https://doi.org/10.1038/35075100
  62. Selinka, H.C., Florin, L., Patel, H.D., Freitag, K., Schmidtke, M., Makarov, V.A, and Sapp, M. (2007). Inhibition of transfer to secondary receptors by heparan sulfate-binding drug or antibody induces noninfectious uptake of human papillomavirus. J. Virol. 81, 10970-10980 https://doi.org/10.1128/JVI.00998-07
  63. Southern, T.R., Jolly, C.E., Lester, M.E., and Hayman, J.R. (2007). EnP1, a microsporidian spore wall protein that enables spores to adhere to and infect host cells in vitro. Eukaryot. Cell 6, 1354-1362 https://doi.org/10.1128/EC.00113-07
  64. Spear, P.G. (2004). Herpes simplex virus: receptors and ligands for cell entry. Cell. Microbiol. 6, 401-410 https://doi.org/10.1111/j.1462-5822.2004.00389.x
  65. Zautner, A.E., Komer, U., Henke, A, Badorff, C., and Schmidtke, M. (2003). Heparan sulfates and coxsackievirus-adenovirus receptor: each one mediates coxsackievirus B3 PD infection. J. Virol. 77,10071-10077 https://doi.org/10.1128/JVI.77.18.10071-10077.2003
  66. Baldassarri, L., Bertuccini, L., Creti, R., Filippini, P., Ammendolia, M.G., Koch, S., Huebner, J., and Orefici, G. (2005). Glycosaminoglycans mediate invasion and survival of Enterococcus faecelts into macrophages. J. Infect. Dis.191,1253-1262 https://doi.org/10.1086/428778
  67. Klimstra, W.B., Ryman, K.D., and Johnston, R.E. (1998). Adaptation of Sindbis virus to BHK cells selects fro use of heparan sulfate as an attachment receptor. J. Virol. 72,7357-7366
  68. Park, P.W., Foster, T.J., Nishi, E., Duncan, S.J., Klagsbrun, M., and Chen, Y. (2004). Activation of syndecan-1 ectodomain shedding by Staphylococcus aureus alpha-toxin and beta-toxin. J. BioI. Chem. 279, 251-258 https://doi.org/10.1074/jbc.M308537200
  69. Boyd, A.P., Sory, M.P., Iriarte, M., and Cornelis, G.R. (1998) Heparin interferes with translocation of Yop proteins into HeLa cells and binds to LcrG, a regulatory component of the Yersinia Yop apparatus. Mol. Microbiol. 27, 425-436 https://doi.org/10.1046/j.1365-2958.1998.00691.x
  70. Frick, I.M., Schmidtchen, A, and Sjobring, U. (2003). Interactions between M proteins of Streptococcus pyogenes and glycosaminoglycans promote bacterial adhesion to host cells. Eur. J. BioChem. 270, 2303-2311 https://doi.org/10.1046/j.1432-1033.2003.03600.x
  71. Zhang, J.P., and Stephens, R.S. (1992). Mechanism of C. trachoma tis attachment to eukaryotic host cells. Cell 69, 861-869 https://doi.org/10.1016/0092-8674(92)90296-O
  72. Smith, T.A, Idamakanti, N., Rollence, M.L., Marshall-Neff, J., Kim, J., Mulgrew, K., Nemerow, G.R., Kaleko, M., and Stevenson, S.C. (2003). Adenovirus serotype 5 fiber shaft influences in vivo gene transfer in mice. Hum. Gene Ther. 14,777-787 https://doi.org/10.1089/104303403765255165
  73. Esko, J.D., and Selleck, S.B. (2002). Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71,435-471 https://doi.org/10.1146/annurev.biochem.71.110601.135458
  74. Feyzi, E., Trybala, E., Bergstrom, T., Lindahl, U., and Spillman, D. (1997). Structural requirement of heparan sulfate for interaction with herpes simplex virus type I virions and isolated glycoprotein C. J. BioI. Chem. 272, 24850-24857 https://doi.org/10.1074/jbc.272.40.24850
  75. Geraghty, R.J., Krummenacher, C., Cohen, G.H., Eisenberg, R.J., and Spear, P.G. (1998). Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor. Science 280,1618-1620 https://doi.org/10.1126/science.280.5369.1618
  76. Lima, A.P., Almeida, P.C., Tersariol, T.L., Schmitz, V., Schmaier, A.H., Juliano, L., Hirata, I.Y., Muller-Esterl, w., Chagas, J.R., and Scharfstein, J. (2002). Heparan sulfate modulates kinin release by Trypanosoma cruzi through the activity of cruzipain. J. BioI. Chem. 277, 5875-5881 https://doi.org/10.1074/jbc.M108518200
  77. Henry-Stanley, M.J., Hess, D.J., Erlandsen, S.L., and Wells, C.L. (2005). Ability of the heparan sulfate proteoglycan syndecan-1 to participate in bacterial translocation across the intestinal epithelial barrier. Shock 24, 571-576 https://doi.org/10.1097/01.shk.0000184286.95493.78
  78. Jones, K.S., Petrow-Sadowski, C., Bertolette, D.C., Huang, Y., and Ruscetti, FW. (2005). Heparan sulfate proteoglycans mediate attachment and entry of human T-cell leukemia virus type 1 virions into CD4+ T cells. J. Virol. 79,12692-12702 https://doi.org/10.1128/JVI.79.20.12692-12702.2005
  79. Tyagi, M., Rusnati, M., Presta, M., and Giacca, M. (2001). Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. J. BioI. Chem. 276, 3254-3261 https://doi.org/10.1074/jbc.M006701200
  80. Patterson, N.A, Smith, J.L., and Ozbun, M.A. (2005). Human papillomavirus type 31 b infection of human keratinocytes does not require heparan sulfate. J. Virol. 79, 6838-6847 https://doi.org/10.1128/JVI.79.11.6838-6847.2005
  81. van Putten, J.P., Duensing, T.D., and Cole, R.L. (1998). Entry of OpaA+ gonococci into HEp-2 cells requires concerted action of glycosaminoglycans, fibronectin and integrin receptors. Mol. Microbiol. 29, 369-379 https://doi.org/10.1046/j.1365-2958.1998.00951.x
  82. Baron, M.J., Bolduc, G.R., Goldberg, M.B., Auperin, T.C., and Madoff, L.C. (2004). Alpha C protein of group B Streptococcus binds host cell surface glycosaminoglycan and enters cells by an actin-dependent mechanism. J. BioI. Chem. 279, 24714-24723 https://doi.org/10.1074/jbc.M402164200
  83. Henry-Stanley, M.J., Hess, D.J., Erickson, E.A, Garni, R.M., and Wells, C.L. (2003). Role of heparan sulfate in interactions of Listeria monocytogenes with enterocytes. Med. Microbiol. Immunol. 192,107-115
  84. Shukla, D., and Spear, P.G. (2001). Herpesviruses and heparan sulfate: an intimate relationship in aid of Virol entry. J. Clin. Invest. 108,503-510 https://doi.org/10.1172/JCI200113799
  85. Alfsen, A, Yu, H., Magerus-Chatinet, A, Schmitt, A, and Bomsel, M. (2005). HIV-1-infected blood mononuclear cells form an integrin- and agrin-dependent Virol synapse to induce efficient HIV-1 transcytosis across epithelial cell monolayer. Mol. BioI. Cell 16,4267-4279 https://doi.org/10.1091/mbc.E05-03-0192
  86. Rathore, D., and McCutchan, T.F. (2000). Role of cysteines in Plasmodium falciparum circumsporozoite protein: interactions with heparin can rejuvenate inactive protein mutants. Proc. Natl. Acad. Sci. USA 97, 8530-8535
  87. Andrian, E., Grenier, D., and Rouabhia, M. (2005). Porphyromonas gingivalis lipopolysaccharide induces shedding of syndecan-1 expressed by gingival epithelial cells. J. Cell. Physiol. 204, 178-183 https://doi.org/10.1002/jcp.20287
  88. Barth, H., Schnober, E.K, Zhang, F., Linhardt, R.J., Depla, E., Boson, B., Cosset, F.L, Patel, A.H., Blum, H.E., and Baumert, T.F. (2006). Virol and cellular determinants of the hepatitis C virus envelope-heparan sulfate interaction. J. Virol. 80, 10579-10590 https://doi.org/10.1128/JVI.00941-06
  89. Chung, M.C., Popova, T.G., Millis, B.A., Mukherjee, D.V., Zhou, W., Liotta, L.A, Petricoin, E.F., Chandhoke, V., Bailey, C., and Popov, S.G. (2006). Secreted neutral metalloproteases of Bacillus anthracis as candidate pathogenic factors. J. BioI. Chem. 281,31408-31418 https://doi.org/10.1074/jbc.M605526200
  90. Davis, C.H., and Wyrick, P.B. (1997). Differences in the association of Chlamydia trachomatis serovar E and serovar L2 with epithelial cells in vitro may reflect biological differences in vivo. Infect. Immun. 65,2914-2924
  91. Jones, K.S., Fugo, K., Petrow-Sadowski, C., Huang, Y., Bertolette, D.C., Lisinski, I., Cushman, S.W., Jacobson, S., and Ruscetti, F.W. (2006). Human T-cell leukemia virus type 1 (HTLV-1) and HTLV-2 use different receptor complexes to enter T cells. J. Virol. 80, 8291-8302 https://doi.org/10.1128/JVI.00389-06
  92. Lambris, J.D., Ricklin, D., and Geisbrecht, B.V. (2008). Complement evasion by human pathogens. Nat. Rev. Microbiol. 6, 132-142 https://doi.org/10.1038/nrmicro1824
  93. Love, D.C., Esko, J.D., and Mosser, D.M (1993). A heparin-binding activity on Leishmania amastigotes which mediates adhesion to cellular proteoglycans. J. Cell BioI. 123,759-766 https://doi.org/10.1083/jcb.123.3.759
  94. Trybala, E., Bergstrom, T., Spillmann, D., Svennerholm, B., Flynn, S.J., and Ryan, P. (1998). Interaction between pseudorabies virus and heparin/heparan sulfate. Pseudorabies virus mutants differ in their interaction with heparin/heparan sulfate when altered for specific glycoprotein C heparin-binding domain. J. BioI. Chem. 273, 5047-5052 https://doi.org/10.1074/jbc.273.9.5047
  95. Lyon, M., Deakin, J.A, and Gallagher, J.T. (1994). Liver heparan sulfate structure. A novel molecular design. J. BioI. Chem. 269, 11208-11215
  96. Marchetti, M., Ammendolia, M.G., and Superti, F. (2008). Glycosaminoglycans are not indispensable for the anti-herpes simplex virus type 2 activity of lactoferrin. Biochimie (in press)
  97. Cheshenko, N., Liu, W., Satlin, L.M., and Herold, B.C. (2007). Multiple receptor interactions trigger release of membrane and intracellular calcium stores critical for herpes simplex virus entry. Mol. BioI. Cell. 18,3119-3130 https://doi.org/10.1091/mbc.E07-01-0062
  98. Feuer, G., and Green, P.L. (2005). Comparative biology of human T-cell Iymphotropic virus type 1 (HTLV-1) and HTLV-2. Oncogene 24, 5996-6004 https://doi.org/10.1038/sj.onc.1208971
  99. Dubreuil, J.D., Ruggiero, P., Rappuoli, R., and Del Giudice, G. (2004). Effect of heparin binding on Helicobacter pylori resistance to serum. J. Med. Microbiol. 53, 9-12 https://doi.org/10.1099/jmm.0.05389-0
  100. Fry, E.E., Lea, S.M., Jackson, T., Newman, J.W., Ellard, F.M., Blakemore, W.E., Abu-Ghazaleh, R., Samuel, A, King, A.M., and Stuart, D.I. (1999). The structure and function of a foot-andmouth disease virus-oligosaccharide receptor complex. EMBO J. 18,543-554 https://doi.org/10.1093/emboj/18.3.543
  101. Bobardt, M.D., Chatterji, U., Selvarajah, S., Van der Schueren, B., David, G., Kahn, B., and Gallay, P.A. (2007). Cell-free human immunodeficiency virus type 1 transcytosis though primary genital epithelial cells. J. Virol. 81,395-405 https://doi.org/10.1128/JVI.01303-06
  102. de Haan, C.A, Li, Z., te Lintelo, E., Bosch, B.J., Haijema, B.J., and Rottier, P.J. (2005). Murine coronavirus with an extended host range uses heparan sulfate as an entry receptor. J. Virol. 79, 14451-14456 https://doi.org/10.1128/JVI.79.22.14451-14456.2005
  103. Gingis-Velitski, S., Zetser, A, Kaplan, V., Ben-Zaken, O., Cohen, E., Levy-Adam, F., Bashenko, Y., Flugelman, M.Y., Vlodavsky, I., and lIan, N. (2004). Heparanase uptake is mediated by cell membrane heparan sulfate proteoglycans. J. BioI. Chem. 279, 44084-44092 https://doi.org/10.1074/jbc.M402131200
  104. Hybiske, K., and Stephens, R.S. (2008). Exit strategies of intracellular pathogens. Nat. Rev. Microbiol. 6, 99-110 https://doi.org/10.1038/nrmicro1821
  105. Woods, A (2001). Syndecans: transmembrane modulators of adhesion and matrix assembly. J. Clin. Invest. 107, 935-941 https://doi.org/10.1172/JCI12802
  106. Andreo, U., Maillard, P., Kalinina, O., Walic, M., Meurs, E., Marti not, M., Marcellin, P., and Budkowska, A (2007). Lipoprotein lipase mediates hepatitis C virus (HCV) cell entry and inhibits HCV infection. Cell. Microbiol. 9,2445-2456 https://doi.org/10.1111/j.1462-5822.2007.00972.x
  107. Bannai, H., Nishikawa, Y., Matsuo, T., Kawase, O., Watanabe, J., Sugimoto, C., and Xuan, X. (2008). Programmed cell death 5 from toxoplasma gondii: a secreted molecule that exerts a proapoptotic effect on host cells. Mol. Biochem. Parasitol. 159, 112-120 https://doi.org/10.1016/j.molbiopara.2008.02.012
  108. de Vries, F.P., Cole, R., Dankert, J., Frosch, M., and van Putten, J.P. (1998). Neisseria meningitidis producing the Opc adhesin binds epithelial cell proteoglycan receptors. Mol. Microbiol. 27, 1203-1212 https://doi.org/10.1046/j.1365-2958.1998.00763.x
  109. Rasmussen-Lathrop, S.J., Koshiyama, K., Phillips, N., and Stephens, R.S. (2000). Chlamydia-dependent biosynthesis of a heparan sulphate-like compound in eukaryotic cells. Cell Microbiol. 2, 137-144 https://doi.org/10.1046/j.1462-5822.2000.00039.x
  110. Xu, D., Tiwari, V., Xia, G., Clement, C., Shukla, D., and Liu, J. (2005). Characterization of heparan sulphate 3-O-sulphotransferase isoform 6 and its role in assisting the entry of herpes simplex virus type 1. Biochem. J. 385, 451-459 https://doi.org/10.1042/BJ20040908
  111. Duensing, T.D., Wing, J.S., and van Putten, J.P.M. (1999). Sulfated polysaccharide-directed recruitment of mammalian host proteins: a novel strategy in microbial pathogenesis. Infect. Immun. 67, 4463-4468
  112. Rathore, D., Hrstka, S.C., Sacci, J.B., Jr., De la Vega, P., Linhardt, R.J., Kumar, S., and McCutchan, T.F. (2003). Molecular mechanism of host specificity in Plasmodium falciparum infection: role of circumsporozoite protein. J. BioI. Chem. 278, 40905-40910 https://doi.org/10.1074/jbc.M306250200
  113. Renne, T., Dedio, J., David, G., and Muller-Esterl, W. (2000). High molecular weight kininogen utilizes heparan sulfate proteoglycans for accumulation on endothelial cells. J. BioI. Chem. 275, 33688-33696 https://doi.org/10.1074/jbc.M000313200
  114. Vogt, A.M., Pettersson, F., Moll, K., Jonsson, C., Normark, J., Ribacke, U., Egwang, T.G., Ekre, H.P., Spillmann, D., Chen, Q., et al. (2006). Release of sequestered malaria parasites upon injection of a glycosaminoglycan. PLoS Pathog. 2, e100 https://doi.org/10.1371/journal.ppat.0020100
  115. Xia, G., Che, J., Tiwari, V., Ju, W., Li, J.P., Malmstrom, A, Shukla, D., and 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. BioI. Chem. 277, 37912-37919 https://doi.org/10.1074/jbc.M204209200
  116. Van, Y., Silvennoinen-Kassinen, S., Leinonen, M., and Saikku, P. (2006). Inhibitory effect of heparan sulfate-like glycosaminoglycans on the infectivity of Chlamydia pneumoniae in HL cells varies between strains. Microbes Infect. 8, 866-872 https://doi.org/10.1016/j.micinf.2005.10.010
  117. Argyris, E.G., Acheampong, E., Nunnari, G., Mukhtar, M., Williams, K.J., and Pomerantz, R.J. (2003). Human immunodeficiency virus type 1 enters primary human brain microvascular endothelial cells by a mechanism involving cell surface proteoglycans independent of lipid rafts. J. Virol. 77, 12140-12151 https://doi.org/10.1128/JVI.77.22.12140-12151.2003
  118. Gallagher, J.T. (2001). Heparan sulfate: growth control with a restricted sequence menu. J. Clin. Invest. 108, 357-361 https://doi.org/10.1172/JCI13713
  119. Ortega-Barria, E., and Pereira, M.E. (1991). A novel T cruzi heparin-binding protein promotes fibroblast adhesion and penetration of engineered bacteria and trypanosomes into mammalian cells. Cell 67, 411-421 https://doi.org/10.1016/0092-8674(91)90192-2
  120. Shukla, D., Liu, J., Blaiklock, P., Shworak, N.W., Bai, X., Esko, J.D., Cohen, G.H., Eisenberg, R.J., Rosenberg, R.D., and Spear, P.G. (1999). A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 99, 13-22 https://doi.org/10.1016/S0092-8674(00)80058-6
  121. Wilsie, L.C., Gonzales, A.M., and Orlando, R.A (2006). Syndecan-1 mediates internalization of apoE-VLDL through a low density lipoprotein receptor-related protein (LRP)-independent, nonclathrin-mediated pathway. Lipids Health Dis. 5, 23 https://doi.org/10.1186/1476-511X-5-23
  122. Alvarez-Dominguez, C., Vasquez-Boland, J., Carrasco-Marin, E., Lopez-Mato, P., and Leyva-Cobian, F. (1997). Host cell heparan sulfate proteoglycans mediate attachment and entry of Listeria monocytogenes, and the listerial surface protein ActA is involved in heparan sulfate receptor recognition. Infect. Immun. 65, 78-88
  123. de Witte, L., Bobardt, M., Chatterji, U., Degeest, G., David, G., Geijtenbeek, T.B., and Gallay, P. (2007). Syndecan-3 is a dendritic cell-specific attachment receptor for HIV-1. Proc. Natl. Acad. Sci. USA 104, 19464-19469
  124. Jacquet, A, Coulon, L., De Neve, J., Daminet, V., Haumont, M., Garcia, L., Bollen, A, Jurado, M., and Biemans, R. (2001). The surface antigen SAG3 mediates the attachment of Toxoplasma gondii to cell-surface proteoglycans. Mol. Biochem. Parasitol. 116,35-44 https://doi.org/10.1016/S0166-6851(01)00297-3
  125. Yabushita, H., Noguchi, Y., Habuchi, H., Ashikari, S., Nakabe, K., Fujita, M., Noguchi, M., Esko, J.D., and Kimata, K. (2002). Effects of chemically modified heparin on Chlamydia trachomatis serovar L2 infection of eukaryotic cells in culture. Glycobiology 12, 345-351 https://doi.org/10.1093/glycob/12.5.345
  126. Freissler, E., Meyer auf der Heyde, A, David, G., Meyer, T.F., and Dehio, C. (2000). Syndecan-1 and syndecan-4 can mediate the invasion of Opa$Opa_{HSPG}$-expressing Neisseria gonorrhoeae into epithelial cells. Cell Microbiol. 2, 69-82 https://doi.org/10.1046/j.1462-5822.2000.00036.x
  127. Isaacs, R.D. (1994). Borrelia burgdorferi bind to epithelial proteoglycan. J. Clin. Invest. 93,809-819 https://doi.org/10.1172/JCI117035
  128. Scharfstein, J., Schmitz, V., Morandi, V., Capella, M.M., Lima, A.P., Morrot, A, Juliano, L., and Muller-Esterl, W. (2000). Host cell invasion by Trypanosoma cruzi is potentiated by activation of bradykinin B(2) receptors. J. Exp. Med. 192,1289-1300 https://doi.org/10.1084/jem.192.9.1289
  129. Vlasak, M., Goesler, I., and Blaas, D. (2005). Human rhinovirus type 89 variants use heparan sulfate proteoglycan for cell attachment. J. Virol. 79, 5963-5970 https://doi.org/10.1128/JVI.79.10.5963-5970.2005