Sulfated K5 Escherichia coli polysaccharide derivatives: A novel class of candidate antiviral microbicides

Pharmacology and Therapeutics

Volumn 123, Issue 3, 2009, Pages 310-322

  Rusnati, Marco ^a   Vicenzi, Elisa ^b   Donalisio, Manuela ^c   Oreste, Pasqua ^d   Landolfo, Santo ^c   Lembo, David ^c  

^a UNIVERSITY OF BRESCIA   (Italy)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c UNIVERSITY OF TURIN   (Italy)

^d Glycores 2000 Srl   (Italy)

Author keywords

Antiviral microbicides; Heparan sulfates; HIV; K5 derivatives; Polyanions; Sexually transmitted infections

Indexed keywords

ACICLOVIR; CARRAGEENAN; CELLULOSE SULFATE; CHITIN DERIVATIVE; CHONDROITIN SULFATE; COLOMINIC ACID; CURDLAN; DEXTRAN SULFATE; FUCOIDIN; GALACTAN SULFATE; HEPARAN SULFATE; HEPARIN; HEPARIN DERIVATIVE; HERPES SIMPLEX VACCINE; HUMAN IMMUNODEFICIENCY VIRUS FUSION INHIBITOR; PENTOSAN POLYSULFATE; PLACEBO; POLYMETHYLENE HYDROQUINONE SULFONATE; POLYSACCHARIDE SULFATE; POLYSTYRENE SULFATE; PORPHYRIN DERIVATIVE; PRO 2000; PROTEINASE INHIBITOR; PROTEOHEPARAN SULFATE; RHAMNAN SULFATE; RNA DIRECTED DNA POLYMERASE INHIBITOR; SURAMIN; UNCLASSIFIED DRUG; UNINDEXED DRUG; WART VIRUS VACCINE; XYLOMANNAN SULFATE;

ANTIVIRAL ACTIVITY; ANTIVIRAL RESISTANCE; CLINICAL TRIAL; CONDOM; CONDYLOMA ACUMINATUM; DRUG EFFICACY; DRUG MEGADOSE; DRUG POTENCY; DRUG SAFETY; DRUG SPECIFICITY; DRUG SYNTHESIS; DRUG TARGETING; DRUG TREATMENT FAILURE; ESCHERICHIA COLI; HERPES SIMPLEX; HERPES SIMPLEX VIRUS; HERPES SIMPLEX VIRUS 1; HERPES SIMPLEX VIRUS 2; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IC 50; INFECTION PREVENTION; MONOGAMY; NONHUMAN; PRIORITY JOURNAL; REVIEW; UTERINE CERVIX CANCER; VACCINATION; VIRUS CELL INTERACTION; WART VIRUS;

ANTIVIRAL AGENTS; BACTERIAL CAPSULES; CLINICAL TRIALS AS TOPIC; ESCHERICHIA COLI; HERPES SIMPLEX; HIV INFECTIONS; HUMANS; PAPILLOMAVIRUS INFECTIONS;

EID: 68049098118     PISSN: 01637258     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2009.05.001     Document Type: Review

References (157)

1. Adamiak B., Ekblad M., Bergstrom T., Ferro V., and Trybala E. Herpes simplex virus type 2 glycoprotein G is targeted by the sulfated oligo- and polysaccharide inhibitors of virus attachment to cells. J Virol 81 (2007) 13424-13434
2. Aguilar J.S., Rice M., and Wagner E.K. The polysulfonated compound suramin blocks adsorption and lateral diffusion of herpes simplex virus type-1 in vero cells. Virology 258 (1999) 141-151
3. Albini A., Soldi R., Giunciuglio D., Giraudo E., Benelli R., Primo L., et al. The angiogenesis induced by HIV-1 tat protein is mediated by the Flk-1/KDR receptor on vascular endothelial cells. Nat Med 2 (1996) 1371-1375
4. Aoki Y., and Tosato G. Neoplastic conditions in the context of HIV-1 infection. Curr HIV Res 2 (2004) 343-349
5. Arduino P.G., and Porter S.R. Herpes Simplex Virus Type 1 infection: overview on relevant clinico-pathological features. J Oral Pathol Med 37 (2008) 107-121
6. Baba M., Snoeck R., Pauwels R., and de Clercq E. Sulfated polysaccharides are potent and selective inhibitors of various enveloped viruses, including herpes simplex virus, cytomegalovirus, vesicular stomatitis virus, and human immunodeficiency virus. Antimicrob Agents Chemother 32 (1988) 1742-1745
7. Barth H., Schnober E.K., Zhang F., Linhardt R.J., Depla E., Boson B., et al. Viral and cellular determinants of the hepatitis C virus envelope-heparan sulfate interaction. J Virol 80 (2006) 10579-10590
8. Batinic D., and Robey F. The V3 region of the envelope glycoprotein of human immunodeficiency virus type 1 binds sulfated polysaccharides and CD4-derived synthetic peptides. J Biol Chem 267 (1992) 6664-6667
9. Bender F.C., Whitbeck J.C., Lou H., Cohen G.H., and Eisenberg R.J. Herpes simplex virus glycoprotein B binds to cell surfaces independently of heparan sulfate and blocks virus entry. J Virol 79 (2005) 11588-11597
10. Benedetti J., Corey L., and Ashley R. Recurrence rates in genital herpes after symptomatic first-episode infection. Ann Intern Med 121 (1994) 847-854
11. Bobardt M.D., Saphire A.C., Hung H.C., Yu X., Van der Schueren B., Zhang Z., et al. Syndecan captures, protects, and transmits HIV to T lymphocytes. Immunity 18 (2003) 27-39
12. Bosch F.X., and de Sanjose S. Chapter 1, human papillomavirus and cervical cancer-burden and assessment of causality. J Natl Cancer Inst Monogr 31 (2003) 3-13
13. Bousarghin L., Touze A., Combita-Rojas L., and Coursaget P. Positively charged sequences of human papillomavirus type 16 capsid proteins are sufficient to mediate gene transfer into target cells via the heparan sulfate receptor. J Gen Virol 84 (2003) 157-164
14. Bousarghin L., Touze A., Yvonnet B., and Coursaget P. Positively charged synthetic peptides from structural proteins of papillomaviruses abrogate human papillomavirus infectivity. J Med Virol 73 (2004) 474-480
15. Brack-Werner R. Astrocytes: HIV cellular reservoirs and important participants in neuropathogenesis. Aids 13 (1999) 1-22
16. Buck C.B., Pastrana D.V., Lowy D.R., and Schiller J.T. Efficient intracellular assembly of papillomaviral vectors. J Virol 78 (2004) 751-757
17. Buck C.B., Thompson C.D., Pang Y.Y., Lowy D.R., and Schiller J.T. Maturation of papillomavirus capsids. J Virol 79 (2005) 2839-2846
18. Buck C.B., Pastrana D.V., Lowy D.R., and Schiller J.T. Generation of HPV pseudovirions using transfection and their use in neutralization assays. Methods Mol Med 119 (2005) 445-462
19. Buck C.B., Thompson C.D., Roberts J.N., Muller M., Lowy D.R., and Schiller J.T. Carrageenan is a potent inhibitor of papillomavirus infection. PLoS Pathog 2 (2006) e69
20. Callahan L., Phelan M., Mallinson M., and Norcross M. Dextran sulfate blocks antibody binding to the principal neutralizing domain of human immunodeficiency virus type 1 without interfering with gp120-CD4 interactions. J Virol 65 (1991) 1543-1550
21. Campadelli-Fiume G., Amasio M., Avitabile E., Cerretani A., Forghieri C., Gianni T., et al. The multipartite system that mediates entry of herpes simplex virus into the cell. Rev Med Virol 17 (2007) 313-326
22. Caputo A., Boarini B.M., Mantovani I., Corallini A., and Barbanti-Brodano G. Multiple functions of human immunodeficiency virus type 1 Tat protein in the pathogenesis of AIDS. Virology 1 (1999) 753-778
23. Carfi A., Willis S.H., Whitbeck J.C., Krummenacher C., Cohen G.H., Eisenberg R.J., et al. Herpes simplex virus glycoprotein D bound to the human receptor HveA. Mol Cell 8 (2001) 169-179
24. Carr D.J., and Tomanek L. Herpes simplex virus and the chemokines that mediate the inflammation. Curr Top Microbiol Immunol 303 (2006) 47-65
25. Cassol E., Alfano M., Biswas P., and Poli P. Monocyte-derived macrophages and myeloid cell lines as targets of HIV-1 replication and persistence. J Leukoc Biol 80 (2006) 1018-1030
26. Casu B., Petitou M., Provasoli M., and Sinay P. Conformational flexibility: a new concept for explaining binding and biological properties of iduronic acid-containing glycosaminoglycans. Trends Biochem Sci 13 (1988) 221-225
27. Casu B., Guerrini M., Naggi A., Perez M., Torri G., Ribatti D., et al. Short heparin sequences spaced by glycol-split uronate residues are antagonists of fibroblast growth factor 2 and angiogenesis inhibitors. Biochemistry 41 (2002) 10519-10528
28. Cernik C., Gallina K., and Brodell R.T. The treatment of herpes simplex infections: an evidence-based review. Arch Intern Med 168 (2008) 1137-1144
29. Check E. Scientists rethink approach to HIV gels. Nature 446 (2007) 12
30. Cheshenko N., and Herold B.C. 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 (2002) 2247-2255
31. Cheshenko N., Keller M.J., MasCasullo V.G., Jarvis A., Cheng H., John M., et al. Candidate topical microbicides bind herpes simplex virus glycoprotein B and prevent viral entry and cell-to-cell spread. Antimicrob Agents Chemother 48 (2004) 2025-2036
32. Christensen N.D., Cladel N.M., and Reed C.A. Postattachment neutralization of papillomaviruses by monoclonal and polyclonal antibodies. Virology 207 (1995) 136-142
33. Christensen N.D., Reed C.A., Culp T.D., Hermonat P.L., Howett M.K., Anderson R.A., et al. Papillomavirus microbicidal activities of high-molecular-weight cellulose sulfate, dextran sulfate, and polystyrene sulfonate. Antimicrob Agents Chemother 45 (2001) 3427-3432
34. Cicala C., Arthos J., Martinelli E., Censoplano N., Cruz C.C., Chung E., et al. R5 and X4 HIV envelopes induce distinct gene expression profiles in primary peripheral blood mononuclear cells. Proc Natl Acad Sci USA 103 (2006) 3746-3751
35. Clanton D.J., Buckheit Jr. R.W., Terpening S.J., Kiser R., Mongelli N., Borgia A.L., et al. Novel sulfonated and phosphonated analogs of distamycin which inhibit the replication of HIV. Antiviral Res 27 (1995) 335-354
36. Corey L. Challenges in genital herpes simplex virus management. J Infect Dis 186 Suppl 1 (2002) S29-33
37. Corey L., and Wald A. Genital herpes. Sexually transmitted diseases. 3rd edn. (1999), McGraw-Hill, New York 285-312
38. Corey L., Wald A., Celum C.L., and Quinn T.C. The effects of herpes simplex virus-2 on HIV-1 acquisition and transmission: a review of two overlapping epidemics. J Acquir Immune Defic Syndr 35 (2004) 435-445
39. Cormier E.G., Persuh M., Thompson D.A., Lin S.W., Sakmar T.P., Olson W.C., et al. Specific interaction of CCR5 amino-terminal domain peptides containing sulfotyrosines with HIV-1 envelope glycoprotein gp120. Proc Natl Acad Sci USA 97 (2000) 5762-5767
40. Crublet E., Andrieu J.P., Vivès R.R., and Lortat-Jacob H. The HIV-1 envelope glycoprotein gp120 features four heparan sulfate binding domains, including the co-receptor binding site. J Biol Chem 283 (2008) 15193-15200
41. Culp T.D., Budgeon L.R., Marinkovich M.P., Meneguzzi G., and Christensen N.D. Keratinocyte-secreted laminin 5 can function as a transient receptor for human papillomaviruses by binding virions and transferring them to adjacent cells. J Virol 80 (2006) 8940-8950
42. Day P.M., Lowy D.R., and Schiller J.T. Heparan sulfate-independent cell binding and infection with furin-precleaved papillomavirus capsids. J Virol 82 (2008) 12565-12568
43. de Parseval A., Bobardt M.D., Chatterji A., Chatterji U., Elder J.H., David G., et al. A highly conserved arginine in gp120 governs HIV-1 binding to both syndecans and CCR5 via sulfated motifs. J Biol Chem 280 (2005) 39493-39504
44. de Villiers E.M., Fauquet C., Broker T.R., Bernard H.U., and zur Hausen H. Classification of papillomaviruses. Virology 324 (2004) 17-27
45. Dewhurst S., Gelbard H.A., and Fine S.M. Neuropathogenesis of AIDS. Mol Med Today 2 (1996) 16-23
46. El-Sadr W.M., Mayer K.H., Maslankowski L., Hoesley C., Justman J., Gai F., et al. Safety and acceptability of cellulose sulfate as a vaginal microbicide in HIV-infected women. Aids 20 (2006) 1109-1116
47. Endo S., Kubota S., Siomi H., Adaki A., Oroszlan S., Maki M., et al. A region of basic amino-acid cluster in HIV-1 Tat protein is essential for trans-acting activity and nucleolar localization. Virus Genes 3 (1989) 99-110
48. Evander M., Frazer I.H., Payne E., Qi Y.M., Hengst K., and McMillan N.A. Identification of the alpha6 integrin as a candidate receptor for papillomaviruses. J Virol 71 (1997) 2449-2456
49. Farzan M., Mirzabekov T., Kolchinsky P., Wyatt R., Cayabyab M., Gerard N.P., et al. Tyrosine sulfation of the amino terminus of CCR5 facilitates HIV-1 entry. Cell 96 (1999) 667-676
50. Feyzi E., Trybala E., Bergstrom T., Lindahl U., and Spillmann D. Structural requirement of heparan sulfate for interaction with herpes simplex virus type 1 virions and isolated glycoprotein C. J Biol Chem 272 (1997) 24850-24857
51. Fleming D.T., McQuillan G.M., Johnson R.E., Nahmias A.J., Aral S.O., Lee F.K., et al. Herpes simplex virus type 2 in the United States, 1976 to 1994. N Engl J Med 337 (1997) 1105-1111
52. Freeman E.E., Weiss H.A., Glynn J.R., Cross P.L., Whitworth J.A., and Hayes R.J. Herpes simplex virus 2 infection increases HIV acquisition in men and women: systematic review and meta-analysis of longitudinal studies. Aids 20 (2006) 73-83
53. FUTURE II Study Group. Quadrivalent vaccine against human papillomavirus to prevent high-grade cervical lesions. N Engl J Med 356 (2007) 1915-1927
54. Gallay P. Syndecans and HIV-1 pathogenesis. Microbes Infect 6 (2004) 617-622
55. Galustian C., Park C.G., Chai W., Kiso M., Bruening S.A., Kang Y.S., et al. High and low affinity carbohydrate ligands revealed for murine SIGN-R1 by carbohydrate array and cell binding approaches, and differing specificities for SIGN-R3 and langerin. Int Immunol 16 (2004) 853-866
56. Garland S.M., Hernandez-Avila M., Wheeler C.M., Perez G., Harper D.M., Leodolter S., et al. Females United to Unilaterally Reduce Endo/Ectocervical Disease (FUTURE) I Investigators. Quadrivalent vaccine against human papillomavirus to prevent anogenital diseases. N Engl J Med 356 (2007) 1928-1943
57. Gatignol A., and Jeang K.T. Tat as a transcriptional activator and a potential therapeutic target for HIV-1. Adv Pharmacol 48 (2000) 209-227
58. Geijtenbeek T.B., Kwon D.S., Torensma R., van Vliet S.J., van Duijnhoven G.C., Middel J., et al. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100 (2000) 587-597
59. Giroglou T., Florin L., Schafer F., Streeck R.E., and Sapp M. Human papillomavirus infection requires cell surface heparan sulfate. J Virol 75 (2001) 1565-1570
60. Goldstein G. HIV-1 Tat protein as a potential AIDS vaccine. Nat Med 2 (1996) 960-964
61. Gordon M., Deeks S., De Marzo C., Goodgame J., Guralnik M., Lang W., et al. Curdlan sulfate (CRDS) in a 21-day intravenous tolerance study in human immunodeficiency virus (HIV) and cytomegalovirus (CMV) infected patients: indication of anti-CMV activity with low toxicity. J Med 28 (1997) 108-128
62. Gupta R., Warren T., and Wald A. Genital herpes. Lancet 370 (2007) 2127-2137
63. Hagner-Mcwhirter A., Lindahl U., and Li J. Biosynthesis of heparin/heparan sulphate: mechanism of epimerization of glucuronyl C-5. Biochem J 347 (2000) 69-75
64. Harrop H.A., and Rider C.C. Heparin and its derivatives bind to HIV-1 recombinant envelope glycoproteins, rather than to recombinant HIV-1 receptor, CD4. Glycobiology 8 (1998) 131-137
65. Haywood A.M. Virus receptors: binding, adhesion strengthening, and changes in viral structure. J Virol 68 (1994) 1-5
66. Heard I., Palefsky J.M., and Kazatchkine M.D. The impact of HIV antiviral therapy on human papillomavirus (HPV) infections and HPV-related diseases. Antivir Ther 9 (2004) 13-22
67. Herold B.C., Gerber S.I., Belval B.J., Siston A.M., and Shulman N. Differences in the susceptibility of herpes simplex virus types 1 and 2 to modified heparin compounds suggest serotype differences in viral entry. J Virol 70 (1996) 3461-3469
68. Holmes K.K., Levine R., and Weaver M. Effectiveness of condoms in preventing sexually transmitted infections. Bull World Health Organ 82 (2004) 454-461
69. Honey K. Microbicide trial screeches to a halt. J Clin Invest 117 (2007) 1116
70. Howley P.M., and Lowy D.R. Papillomaviruses and their replication. In: Fields B.N., Knipe D.M., and Howley P.M. (Eds). Fields virology (2001), Lippincott-Raven, Philadelphia, PA 2197-2229
71. Hricovini M., Guerrini M., Torri G., and Casu B. Motional properties of E. coli polysaccharide K5 in aqueous solution analyzed by NMR relaxation measurements. Carbohydr Res 300 (1997) 69-76
72. Ishihara C., Yoshimatsu K., Tsuji M., Arikawa J., Saiki I., Tokura S., et al. Anti-viral activity of sulfated chitin derivatives against Friend murine leukaemia and herpes simplex type-1 viruses. Vaccine 11 (1993) 670-674
73. Ishihara M., Shaklee P.N., Yang Z., Liang W., Wei Z., Stack R.J., et al. Structural features in heparin which modulate specific biological activities mediated by basic fibroblast growth factor. Glycobiology 4 (1994) 451-458
74. Jiang S. HIV-1-co-receptors binding. Nat Med 3 (1997) 367-368
75. Joyce J.G., Tung J.S., Przysiecki C.T., Cook J.C., Lehman E.D., Sands J.A., et al. The L1 major capsid protein of human papillomavirus type 11 recombinant virus-like particles interacts with heparin and cell-surface glycosaminoglycans on human keratinocytes. J Biol Chem 274 (1999) 5810-5822
76. Kang Y.S., Yamazaki S., Iyoda T., Pack M., Bruening S.A., Kim J.Y., et al. SIGN-R1, a novel C-type lectin expressed by marginal zone macrophages in spleen, mediates uptake of the polysaccharide dextran. Int Immunol 15 (2003) 177-186
77. Karger A., and Mettenleiter T.C. Glycoproteins gIII and gp50 play dominant roles in the biphasic attachment of pseudorabies virus. Virology 194 (1993) 654-664
78. Kedzierska K., and Crowe S.M. Cytokines and HIV-1: interactions and clinical implications. Antivir Chem Chemother 12 (2001) 133-150
79. Keller M.J., Zerhouni-Layachi B., Cheshenko N., John M., Hogarty K., Kasowitz A., et al. PRO 2000 gel inhibits HIV and herpes simplex virus infection following vaginal application: a double-blind placebo-controlled trial. J Infect Dis 193 (2006) 27-35
80. Knappe M., Bodevin S., Selinka H.C., Spillmann D., Streeck R.E., Chen X.S., et al. Surface-exposed amino acid residues of HPV16 L1 protein mediating interaction with cell surface heparan sulfate. J Biol Chem 282 (2007) 27913-27922
81. Koelle D.M., and Corey L. Herpes simplex: insights on pathogenesis and possible vaccines. Annu Rev Med 59 (2008) 381-395
82. Konlee M. Sulfated polysaccharides (chondroitin sulfate and carrageenan) plus glucosamine sulfate are potent inhibitors of HIV. Posit Health News 17 (1998) 4-7
83. Laquerre S., Argnani R., Anderson D.B., Zucchini S., Manservigi R., and Glorioso J.C. 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 (1998) 6119-6130
84. Lederman S., Bergmann J.E., Cleary A.M., Yellin M.J., Fusco P.J., and Chess L. Sulfated polyester interactions with the CD4 molecule and with the third variable loop domain (v3) of gp120 are chemically distinct. AIDS Res Hum Retrovir 8 (1992) 1599-1610
85. Lee J.B., Hayashi K., Hayashi T., Sankawa U., and Maeda M. Antiviral activities against HSV-1, HCMV, and HIV-1 of rhamnan sulfate from monostroma latissimum. Planta Med 65 (1999) 439-441
86. Lembo D., Donalisio M., Rusnati M., Bugatti A., Cornaglia M., Cappello P., et al. Sulfated K5 Escherichia coli polysaccharide derivatives as wide-range inhibitors of genital types of human papillomavirus. Antimicrob Agents Chemother 52 (2008) 1374-1381
87. Lindahl U., Bäckström G., Höök M., Thunberg M., Fransson L.Å., and Linker A. Structure of the antithrombin-binding site in heparin. Proc Natl Acad Sci USA 76 (1979) 3198-3202
88. Lindahl U., Lidholt K., Spillmann D., and Kjellen L. More to "heparin" than anticoagulation. Thromb Res 75 (1994) 1-32
89. Lindahl U., Li J.P., Kusche-Gullberg M., Salmivirta M., Alaranta S., Veromaa T., et al. Generation of "neoheparin" from E. coli K5 capsular polysaccharide. J Med Chem 48 (2005) 349-352
90. Looker K.J., and Garnett G.P. A systematic review of the epidemiology and interaction of herpes simplex virus types 1 and 2. Sex Transm Infect 81 (2005) 103-107
91. Lopalco L., Ciccomascolo F., Lanza P., Zoppetti G., Caramazza I., Leoni F., et al. Anti-HIV type 1 properties of chemically modified heparins with diminished anticoagulant activity. AIDS Res Hum Retrovir 10 (1994) 787-793
92. Lowy D.R., and Howley P.M. Papillomaviruses. In: Fields B.N., Knipe D.M., and Howley P.M. (Eds). Fields virology (2001), Lippincott-Raven, Philadelphia, PA 2231-2264
93. Lynch G., Low L., Li S., Sloane A., Adams S., Parish C., et al. Sulfated polyanions prevent HIV infection of lymphocytes by disruption of the CD4-gp120 interaction, but do not inhibit monocyte infection. J Leukoc Biol 56 (1994) 266-272
94. Madan R.P., Mesquita P.M., Cheshenko N., Jing B., Shende V., Guzman E., et al. Molecular umbrellas: a novel class of candidate topical microbicides to prevent human immunodeficiency virus and herpes simplex virus infections. J Virol 81 (2007) 7636-7646
95. Manhart L.E., and Koutsky L.A. Do condoms prevent genital HPV infection, external genital warts, or cervical neoplasia? A meta-analysis. Sex Transm Dis 29 (2002) 725-735
96. Marchetti M., Pisani S., Pietropaolo V., Seganti L., Nicoletti R., and Orsi N. Inhibition of herpes simplex virus infection by negatively charged and neutral carbohydrate polymers. J Chemother 7 (1995) 90-96
97. Mardberg K., Trybala E., Glorioso J.C., and Bergstrom T. Mutational analysis of the major heparan sulfate-binding domain of herpes simplex virus type 1 glycoprotein C. J Gen Virol 82 (2001) 1941-1950
98. Marechal V., Prevost M.C., Petit C., Perret E., Heard J.M., and Schwartz O. Human immunodeficiency virus type 1 entry into macrophages mediated by macropinocytosis. J Virol 75 (2001) 11166-11177
99. McClain D.S., and Fuller A.O. Cell-specific kinetics and efficiency of herpes simplex virus type 1 entry are determined by two distinct phases of attachment. Virology 198 (1994) 690-702
100. McGrath B.J., and Newman C.L. Genital herpes simplex infections in patients with the acquired immunodeficiency syndrome. Pharmacotherapy 14 (1994) 529-542
101. Mesquita P.M. 15th Conference on Retroviruses and Opportunistic Infections (2008) February 3-6, 2008, Boston, Massachusetts U.S.A. Abstract 26
102. Meylan P.R., Kornbluth R.S., Zbinden I., and Richman D.D. Influence of host cell type and V3 loop of the surface glycoprotein on susceptibility of human immunodeficiency virus type 1 to polyanion compounds. Antimicrob Agents Chemother 38 (1994) 2910-2916
103. Moelling K., Schulze T., and Diringer H. Inhibition of human immunodeficiency virus type 1 RNase H by sulfated polyanions. J Virol 63 (1989) 5489-5491
104. Mondor I., Ugolini S., and Sattentau Q.J. Human immunodeficiency virus type 1 attachment to HeLa CD4 cells is CD4 independent and gp120 dependent and requires cell surface heparans. J Virol 72 (1998) 3623-3634
105. Montefiori D.C. HIV-Specific Neutralizing Antibodies (2001), Humana Press, Totowa, New Jersey
106. Moore J.P., and Stevenson M. New targets for inhibitors of HIV-1 replication. Nat Rev Mol Cell Biol 1 (2000) 40-49
107. Moulard M., Lortat-Jacob H., Mondor I., Roca G., Wyatt R., Sodroski J., et al. Selective interactions of polyanions with basic surfaces on human immunodeficiency virus type 1 gp120. J Virol 74 (2000) 1948-1960
108. Noonan D., and Albini A. From the outside in: extracellular activities of HIV Tat. Adv Pharmacol 48 (2000) 229-250
109. Nyberg K., Ekblad M., Bergstrom T., Freeman C., Parish C.R., Ferro V., et al. The low molecular weight heparan sulfate-mimetic, PI-88, inhibits cell-to-cell spread of herpes simplex virus. Antiviral Res 63 (2004) 15-24
110. Olofsson S., and Bergstrom T. Glycoconjugate glycans as viral receptors. Ann Med 37 (2005) 154-172
111. Orenstein J.M., Fox C., and Wahl S.M. Macrophages as a source of HIV during opportunistic infections. Science 276 (1997) 1857-1861
112. Pacciarini F., Grezzi S., Pinna D., Cima S., Zappetti G., Oreste P., et al. Sulfated K5 Escherichia coli polysaccharide derivatives inhibit human immunodeficiency type-1 (HIV-1) infection: candidate microbicides to prevent sexual HIV transmission. New Microbiol 27 (2004) 5-9
113. Parish C.R., Low L., Warren H.S., and Cunningham A.L. A polyanion binding site on the CD4 molecule. Proximity to the HIV-gp120 binding region. J Immunol 145 (1990) 1188-1195
114. Peterlin B.M., Adams M., Alonso A., Baur A., Ghosh S., Lu X., et al. In: Cullen B.R. (Ed). Human retroviruses (1993), Oxford University Press, Oxford 75-100
115. Philippon V., Vellutini C., Gambarelli D., Harkiss G., Arbuthnott G., Metzger D., et al. The basic domain of the lentiviral Tat protein is responsible for damages in mouse brain: involvement of cytokines. Virology 205 (1994) 519-529
116. Pinna D., Oreste P., Coradin T., Kajaste-Rudnitski A., Ghezzi S., Zoppetti G., et al. Inhibition of herpes simplex virus types 1 and 2 in vitro infection by sulfated derivatives of Escherichia coli K5 polysaccharide. Antimicrob Agents Chemother 52 (2008) 3078-3084
117. Poignard P., Saphire E.O., Parren P.W., and Burton D.R. gp120: biologic aspects of structural features. Annu Rev Immunol 19 (2001) 253-274
118. Puglisi J.D., Tan R., Calnan B.J., Frankel A.D., and Williamson J.R. Conformation of the TAR RNA-arginine complex by NMR spectroscopy. Science 257 (1992) 76-80
119. Rideout D., Schinazi R., Pauza C.D., Lovelace K., Chiang L.C., Calogeropoulou T., et al. Derivatives of 4-amino-3,6-disulfonato-1,8-naphthalimide inhibit reverse transcriptase and suppress human and feline immunodeficiency virus expression in cultured cells. J Cell Biochem 51 (1993) 446-457
120. Roderiquez G., Oravecz T., Yanagishita M., Bou-Habib D.C., Mostowski H., and Norcross M.A. Mediation of human immunodeficiency virus type 1 binding by interaction of cell surface heparan sulfate proteoglycans with the V3 region of envelope gp120-gp41. J Virol 69 (1995) 2233-2239
121. Roizman B., Knipe M.M., and Whitley R.J. Herpes Simplex Viruses. In: Fields B.N., Knipe D.M., and Howley P.M. (Eds). Fields virology (2007), Lippincott-Raven, Philadelphia, PA 2501-2601
122. Rusnati M., and Presta M. Interaction of angiogenic basic fibroblast growth factor with endothelial cell heparan sulfate proteoglycans. Biological implications in neovascularization. Int J Clin Lab Res 26 (1996) 15-23
123. Rusnati M., and Presta M. Extracellular angiogenic growth factor interactions: an angiogenesis interactome survey. Endothelium 13 (2006) 93-111
124. Rusnati M., Tulipano G., Urbinati C., Tanghetti E., Giuliani R., Giacca M., et al. The basic domain in HIV-1 Tat protein as a target for polysulfonated heparin-mimicking extracellular Tat antagonists. J Biol Chem 273 (1998) 16027-16037
125. Rusnati M., Oreste P., Zappetti G., and Presta M. Biotechnological engineering of heparin/heparan sulphate: a novel area of multi-target drug discovery. Curr Pharm Des 11 (2005) 2489-2499
126. Saphire A.C., Bobardt M.D., and Gallay P.A. Host cyclophilin A mediates HIV-1 attachment to target cells via heparans. Embo J 18 (1999) 6771-6785
127. Saphire A.C., Bobardt M.D., Zhang Z., David G., and Gallay P.A. Syndecans serve as attachment receptors for human immunodeficiency virus type 1 on macrophages. J Virol 75 (2001) 9187-9200
128. Schiffman M., and Kruger Kjaer S. Chapter 2, Natural history of anogenital human papillomavirus infection and neoplasia. J Natl Cancer Inst Monogr 31 (2003) 14-19
129. Secchiero P., Zella D., Capitani S., Gallo R.C., and Zauli G. Extracellular HIV-1 tat protein up-regulates the expression of surface CXC-chemokine receptor 4 in resting CD4+ T cells. J Immunol 162 (1999) 2427-2431
130. Sekaly R.P. The failed HIV Merck vaccine study: a step back or a launching point for future vaccine development?. J Exp Med 205 (2008) 7-12
131. Shukla D., and Spear P.G. Herpesviruses and heparan sulfate: an intimate relationship in aid of viral entry. J Clin Invest 108 (2001) 503-510
132. Skoler-Karpoff S., Ramjee G., Ahmed K., Altini L., Plagianos M.G., Friedland B., et al. Efficacy of Carraguard for prevention of HIV infection in women in South Africa: a randomised, double-blind, placebo-controlled trial. Lancet 372 (2008) 1977-1987
133. Spillmann D. Heparan sulfate: anchor for viral intruders?. Biochimie 83 (2001) 811-817
134. Stanberry L.R., Spruance S.L., Cunningham A.L., Bernstein D.I., Mindel A., Sacks S., et al. Glycoprotein-D-adjuvant vaccine to prevent genital herpes. N Engl J Med 347 (2002) 1652-1661
135. Sydow G., and Klocking H.P. Effect of pentosan polysulfate (SP 54) on the reverse transcriptase activity of several retroviruses. Biomed Biochim Acta 46 (1987) 527-530
136. Tao W., Richards C., and Hamer D. Enhancement of HIV infection by cellulose sulfate. AIDS Res Hum Retrovir 24 (2008) 925-929
137. Taylor D.L., Brennan T.M., Bridges C.G., Mullins M.J., Tyms A.S., Jackson R., et al. Potent inhibition of human immunodeficiency virus by MDL 101028, a novel sulphonic acid polymer. Antiviral Res 28 (1995) 159-173
138. Trybala E., Liljeqvist J.A., Svennerholm B., and Bergstrom T. Herpes simplex virus types 1 and 2 differ in their interaction with heparan sulfate. J Virol 74 (2000) 9106-9114
139. Turnbull J., Powell A., and Guimond S. Heparan sulfate: decoding a dynamic multifunctional cell regulator. Trends Cell Biol 11 (2001) 75-82
140. Tyagi M., Rusnati M., Presta M., and Giacca M. Internalization of HIV-1 tat requires cell surface heparan sulfate proteoglycans. J Biol Chem 276 (2001) 3254-3261
141. Ueki M., Watanabe S., Saitoh T., Nakashima H., Yamamoto N., and Ogawara H. Synthesis and chain length-anti-HIV activity relationship of fully N- and O-sulfated homooligomers of tyrosine. Bioorg Med Chem 9 (2001) 487-492
142. Ugolini S., Mondor I., and Sattentau Q.J. HIV-1 attachment: another look. Trends Microbiol 7 (1999) 144-149
143. Urbinati C., Bugatti A., Oreste P., Zoppetti G., Waltenberger J., Mitola S., et al. Chemically sulfated Escherichia coli K5 polysaccharide derivatives as extracellular HIV-1 Tat protein antagonists. FEBS Lett 568 (2004) 171-177
144. Urbinati C., Chiodelli P., and Rusnati M. Polyanionic drugs and viral oncogenesis: a novel approach to control infection, tumor-associated inflammation and angiogenesis. Molecules 13 (2008) 2758-2785
145. Vann W.F., Schmidt M.A., Jann B., and Jann K. The structure of the capsular polysaccharide (K5 antigen) of urinary-tract-infective Escherichia coli 010:K5:H4. A polymer similar to desulfo-heparin. Eur J Biochem 116 (1981) 359-364
146. Vicenzi E., Gatti A., Ghezzi S., Oreste P., Zoppetti G., and Poli G. Broad spectrum inhibition of HIV-1 infection by sulfated K5 Escherichia coli polysaccharide derivatives. Aids 17 (2003) 177-181
147. Vives R.R., Imberty A., Sattentau Q.J., and Lortat-Jacob H. Heparan sulfate targets the HIV-1 envelope glycoprotein gp120 coreceptor binding site. J Biol Chem 280 (2005) 21353-21357
148. Vogel B.E., Lee S.J., Hildebrand A., Craig W., Pierschbacher M.D., Wong-Staal F., et al. A novel integrin specificity exemplified by binding of the alpha v beta 5 integrin to the basic domain of the HIV Tat protein and vitronectin. J Cell Biol 121 (1993) 461-468
149. Vzorov A.N., Bozja J., Dixon D.W., Marzilli L.G., and Compans R.W. Parameters of inhibition of HIV-1 infection by small anionic microbicides. Antiviral Res 73 (2007) 60-68
150. Wald A., Zeh J., Selke S., Ashley R.L., and Corey L. Virologic characteristics of subclinical and symptomatic genital herpes infections. N Engl J Med 333 (1995) 770-775
151. Witvrouw M., and De Clercq E. Sulfated polysaccharides extracted from sea algae as potential antiviral drugs. Gen Pharmacol 29 (1997) 497-511
152. Wyatt R., Kwong P.D., Desjardins E., Sweet R.W., Robinson J., Hendrickson W.A., et al. The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393 (1998) 705-711
153. Yang D.W., Ohta Y., Yamaguchi S., Tsukada Y., Haraguchi Y., Hoshino H., et al. Sulfated colominic acid: an antiviral agent that inhibits the human immunodeficiency virus type 1 in vitro. Antiviral Res 31 (1996) 95-104
154. Ylisastigui L., Bakri Y., Amzazi S., Gluckman J.C., and Benjouad A. Soluble glycosaminoglycans do not potentiate RANTES antiviral activity on the infection of primary macrophages by human immunodeficiency virus type 1. Virology 278 (2000) 412-422
155. Zaneveld L.J., Waller D.P., Anderson R.A., Chany II C., Rencher W.F., Feathergill K., et al. Efficacy and safety of a new vaginal contraceptive antimicrobial formulation containing high molecular weight poly(sodium 4-styrenesulfonate). Biol Reprod 66 (2002) 886-894
156. Zhang Y., Schols D., and De Clercq E. Selective activity of various antiviral compounds against HHV-7 infection. Antiviral Res 43 (1999) 23-35
157. Zhang Y.J., Hatziioannou T., Zang T., Braaten D., Luban J., Goff S.P., et al. Envelope-dependent, cyclophilin-independent effects of glycosaminoglycans on human immunodeficiency virus type 1 attachment and infection. J Virol 76 (2002) 6332-6343