Protein glycosylation in infectious disease pathobiology and treatment

Central European Journal of Biology

Volumn 6, Issue 5, 2011, Pages 802-816

  Vigerust, David J ^a,b  

^a Department of Veteran Affairs ^*  (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Bacteria; Glycosylation; Infectious disease; Virus

Indexed keywords

BACTERIA (MICROORGANISMS); HUMAN IMMUNODEFICIENCY VIRUS; ORTHOMYXOVIRIDAE; PARAMYXOVIRIDAE;

EID: 80052301150     PISSN: 1895104X     EISSN: 16443632     Source Type: Journal    
DOI: 10.2478/s11535-011-0050-8     Document Type: Review

References (144)

1. Witze E. S., Old W. M., Resing K. A., Ahn N. G., Mapping protein post-translational modifications with mass spectrometry, Nat. Methods, 2007, 4, 798-806.
2. Spiro R. G., Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds, Glycobiology, 2002, 12, 43R-56R.
3. Stepper J., Shastri S., Loo T. S., Preston J. C., Novak P., Man P., et al., Cysteine S-glycosylation, a new post-translational modification found in glycopeptide bacteriocins, FEBS letters, 585, 645-650.
4. Furmanek A., Hofsteenge J., Protein C-mannosylation: facts and questions, Acta Biochim. Polon., 2000, 47, 781-789.
5. Falzarano D., Krokhin O., van Domselaar G., Wolf K., Seebach J., Schnittler H. J., et al., Ebola sGP-the first viral glycoprotein shown to be C-mannosylated, Virology, 2007, 368, 83-90.
6. Hartmann S., Hofsteenge J., Properdin, the positive regulator of complement, is highly C-mannosylated, J. Biol. Chem., 2000, 275, 28569-72854.
7. Ristl R., Steiner K., Zarschler K., Zayni S., Messner P., Schaffer C., The s-layer glycome-adding to the sugar coat of bacteria, Int. J. Microbiol., 2011, pi 127870.
8. Apweiler R., Hermjakob H., Sharon N., On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database, Biochim. Biophys. Acta, 1999, 1473, 4-8.
9. Messner P., Prokaryotic glycoproteins: unexplored but important, J. Bacteriol., 2004, 186, 2517-2519.
10. Weerapana E., Imperiali B., Asparagine-linked protein glycosylation: from eukaryotic to prokaryotic systems, Glycobiology, 2006, 16, 91R-101R.
11. Neuberger A., Carbohydrates in protein: The carbohydrate component of crystalline egg albumin, Biochem. J., 1938, 32, 1435-1451.
12. Sleytr, U. B. and Thorne, K. J. (1976) Chemical characterization of the regularly arranged surface layers of Clostridium thermosaccharolyticum and Clostridium thermohydrosulfuricum. J Bacteriol 126, 377-83.
13. Sleytr U. B., Heterologous reattachment of regular arrays of glycoproteins on bacterial surfaces, Nature, 1975, 257, 400-402.
14. Szymanski C. M., Logan S. M., Linton D., Wren B. W., Campylobacter-a tale of two protein glycosylation systems, Trends Microbiol., 2003, 11, 233-238.
15. Wacker M., Linton D., Hitchen P. G., Nita-Lazar M., Haslam S. M., North S. J., et al., N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli, Science, 2002, 298, 1790-1793.
16. Abu-Qarn M., Eichler J., Protein N-glycosylation in Archaea: defining Haloferax volcanii genes involved in S-layer glycoprotein glycosylation, Mol. Microbiol., 2006, 61, 511-525.
17. Logan S. M., Flagellar glycosylation - a new component of the motility repertoire?, Microbiology, 2006, 152, 1249-1262.
18. Castric P., pilO, a gene required for glycosylation of Pseudomonas aeruginosa 1244 pilin, Microbiology, 1995, 141, 1247-1254.
19. Fletcher C. M., Coyne M. J., Villa O. F., Chatzidaki-Livanis M., Comstock L. E. A general O-glycosylation system important to the physiology of a major human intestinal symbiont, Cell, 2009, 137, 321-331.
20. Coyne M. J., Reinap B., Lee M. M., Comstock L. E., Human symbionts use a host-like pathway for surface fucosylation, Science, 2005, 307, 1778-1781.
21. Power P. M., Seib K. L., Jennings M. P., Pilin glycosylation in Neisseria meningitidis occurs by a similar pathway to wzy-dependent O-antigen biosynthesis in Escherichia coli, Biochem. Biophys. Res. Commun., 2006, 347, 904-908.
22. Stimson E., Virji M., Makepeace K., Dell A., Morris H., Payne G., et al., Meningococcal pilin: a glycoprotein substituted with digalactosyl 2, 4-diacetamido-2, 4, 6-trideoxyhexose, Mol. Microbiol., 1995, 17, 1201-1214.
23. Virji M., Post-translational modifications of meningococcal pili. Identification of common substituents: glycans and alpha-glycerophosphate-a review, Gene, 1997, 192, 141-147.
24. Hegge F. T., Hitchen P. G., Aas F. E., Kristiansen H., Lovold C., Egge-Jacobsen W., Unique modifications with phosphocholine and phosphoethanolamine define alternate antigenic forms of Neisseria gonorrhoeae type IV pili, Proc. Natl. Acad. Sci. USA, 2004, 101, 10798-107803.
25. Castric P., Cassels F. J., Carlson R. W., Structural characterization of the Pseudomonas aeruginosa 1244 pilin glycan, J. Biol. Chem., 2001, 276, 26479-26485.
26. Schirm M., Soo E. C., Aubry A. J., Austin J., Thibault P., Logan S. M., Structural, genetic and functional characterization of the flagellin glycosylation process in Helicobacter pylori, Mol. Microbiol., 2003, 48, 1579-1592.
27. McNally D. J., Aubry A. J., Hui J. P., Khieu N. H., Whitfield D., Ewing C. P., et al., Targeted metabolomics analysis of Campylobacter coli VC167 reveals legionaminic acid derivatives as novel flagellar glycans, J. Biol. Chem., 2007, 282, 14463-14475.
28. Thibault P., Logan S. M., Kelly J. F., Brisson J. R., Ewing C. P., Trust T. J., et al., Identification of the carbohydrate moieties and glycosylation motifs in Campylobacter jejuni flagellin, J. Biol. Chem., 2001, 276, 34862-34870.
29. Sambri V., Stefanelli C., Cevenini R., Detection of glycoproteins in Borrelia burgdorferi, Arch. Microbiol., 1992, 157, 205-208.
30. Swanson A. F., Kuo C. C., Binding of the glycan of the major outer membrane protein of Chlamydia trachomatis to HeLa cells, Infect. Immun., 1994, 62, 24-28.
31. Swanson A. F., Kuo C. C., The characterization of lectin-binding proteins of Chlamydia trachomatis as glycoproteins, Microb. Pathog., 1991, 10, 465-473.
32. Swanson A. F., Kuo C. C., Evidence that the major outer membrane protein of Chlamydia trachomatis is glycosylated, Infect. Immun., 1991, 59, 2120-2125.
33. Lindenthal C., Elsinghorst E. A., Enterotoxigenic Escherichia coli TibA glycoprotein adheres to human intestine epithelial cells, Infect. Immun., 2001, 69, 52-57.
34. Lindenthal C., Elsinghorst E. A., Identification of a glycoprotein produced by enterotoxigenic Escherichia coli, Infect. Immun., 1999, 67, 4084-4091.
35. Espitia C., Mancilla R., Identification, isolation and partial characterization of Mycobacterium tuberculosis glycoprotein antigens, Clin. Exp. Immunol., 1989, 77, 378-383.
36. Mondotte J. A., Lozach P. Y., Amara A., Gamarnik A. V., Essential role of dengue virus envelope protein N glycosylation at asparagine-67 during viral propagation, J. Virol., 2007, 81, 7136-7148.
37. Korber B., Gaschen B., Yusim K., Thakallapally R., Kesmir C., Detours V., Evolutionary and immunological implications of contemporary HIV-1 variation, Br. Med. Bull., 2001, 58, 19-42.
38. Wei X., Decker J. M., Wang S., Hui H., Kappes J. C., Wu X., et al., Antibody neutralization and escape by HIV-1, Nature, 2003, 422, 307-312.
39. Land A., Braakman I., Folding of the human immunodeficiency virus type 1 envelope glycoprotein in the endoplasmic reticulum, Biochimie, 2001, 83, 783-790.
40. Slater-Handshy T., Droll D. A., Fan X., Di Bisceglie A. M., Chambers T. J., HCV E2 glycoprotein: mutagenesis of N-linked glycosylation sites and its effects on E2 expression and processing, Virology, 2004, 319, 36-48.
41. Meunier J. C., Fournillier A., Choukhi A., Cahour A., Cocquerel L., Dubuisson J., et al., Analysis of the glycosylation sites of hepatitis C virus (HCV) glycoprotein E1 and the influence of E1 glycans on the formation of the HCV glycoprotein complex, J. Gen. Virol., 1999, 80, 887-896.
42. Wagner R., Wolff T., Herwig A., Pleschka S., Klenk H. D., Interdependence of hemagglutinin glycosylation and neuraminidase as regulators of influenza virus growth: a study by reverse genetics, J. Virol., 2000, 74, 6316-6323.
43. Klenk H. D., Wagner R., Heuer D., Wolff T., Importance of hemagglutinin glycosylation for the biological functions of influenza virus, Virus Res., 2002, 82, 73-75.
44. Baigent S. J., McCauley J. W., Glycosylation of haemagglutinin and stalk-length of neuraminidase combine to regulate the growth of avian influenza viruses in tissue culture, Virus Res., 2001, 79, 177-185.
45. Tsuchiya E., Sugawara K., Hongo S., Matsuzaki Y., Muraki Y., Nakamura K., Role of overlapping glycosylation sequons in antigenic properties, intracellular transport and biological activities of influenza A/H2N2 virus haemagglutinin, J. Gen. Virol., 2002, 83, 3067-3074.
46. Tsuchiya E., Sugawara K., Hongo S., Matsuzaki Y., Muraki Y., Li Z. N., et al., Effect of addition of new oligosaccharide chains to the globular head of influenza A/H2N2 virus haemagglutinin on the intracellular transport and biological activities of the molecule, J. Gen. Virol., 2002, 83, 1137-1146.
47. Abe Y., Takashita E., Sugawara K., Matsuzaki Y., Muraki Y., Hongo S., Effect of the addition of oligosaccharides on the biological activities and antigenicity of influenza A/H3N2 virus hemagglutinin, J. Virol., 2004, 78, 9605-9611.
48. Kaverin N. V., Rudneva I. A., Ilyushina N. A., Varich N. L., Lipatov A. S., Smirnov Y. A., et al., Structure of antigenic sites on the haemagglutinin molecule of H5 avian influenza virus and phenotypic variation of escape mutants, J. Gen. Virol., 2002, 83, 2497-2505.
49. Londrigan S. L., Turville S. G., Tate M. D., Deng Y. M., Brooks A. G., Reading P. C., N-linked Glycosylation Facilitates Sialic Acid-Independent Attachment and Entry of Influenza A Viruses into Cells Expressing DC-SIGN or L-SIGN, J. Virol., 2010, 85, 2990-3000.
50. Daniels R., Kurowski B., Johnson A. E., Hebert D. N., N-linked glycans direct the cotranslational folding pathway of influenza hemagglutinin, Mol. Cell, 2003, 11, 79-90.
51. Skehel J. J., Wiley D. C., Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin, Ann. Rev. Biochem., 2000, 69, 531-569.
52. Vigerust D. J., Ulett K. B., Boyd K. L., Madsen J., Hawgood S., McCullers J. A., N-linked glycosylation attenuates H3N2 influenza viruses, J. Virol., 2007, 81, 8593-8600.
53. Job E. R., Deng Y. M., Tate M. D., Bottazzi B., Crouch E. C., Dean M. M., et al., Pandemic H1N1 influenza A viruses are resistant to the antiviral activities of innate immune proteins of the collectin and pentraxin superfamilies, J. Immunol., 2010, 185, 4284-4291.
54. Deshpande K. L., Fried V. A., Ando M., Webster R. G., Glycosylation affects cleavage of an H5N2 influenza virus hemagglutinin and regulates virulence, Proc. Natl. Acad. Sci. USA, 1987, 84, 36-40.
55. Zambon M. C., Epidemiology and pathogenesis of influenza, J. Antimicrob. Chemother., 1999, 44, 3-9.
56. Das S. R., Puigbo P., Hensley S. E., Hurt D. E., Bennink J. R., Yewdell J. W., Glycosylation focuses sequence variation in the influenza A virus H1 hemagglutinin globular domain, PLoS Pathog., 2010, 6, e1001211.
57. Martin-Gallardo A., Fleischer E., Doyle S. A., Arumugham R., Collins P. L., Hildreth S. W., et al., Expression of the G glycoprotein gene of human respiratory syncytial virus in Salmonella typhimurium, J. Gen. Virol., 1993, 74, 453-458.
58. Collins P. L., Mottet G., Oligomerization and posttranslational processing of glycoprotein G of human respiratory syncytial virus: altered O-glycosylation in the presence of brefeldin A, J. Gen. Virol., 1992, 73, 849-863.
59. Aguilar H. C., Matreyek K. A., Filone C. M., Hashimi S. T., Levroney E. L., Negrete O. A., et al., N-glycans on Nipah virus fusion protein protect against neutralization but reduce membrane fusion and viral entry, J. Virol., 2006, 80, 4878-4889.
60. Moll M., Kaufmann A., Maisner A., Influence of N-glycans on processing and biological activity of the nipah virus fusion protein, J. Virol., 2004, 78, 7274-7278.
61. Bossart K. N., Crameri G., Dimitrov A. S., Mungall B. A., Feng Y. R., Patch J. R., et al., Receptor binding, fusion inhibition, and induction of crossreactive neutralizing antibodies by a soluble G glycoprotein of Hendra virus, J. Virol., 2005, 79, 6690-6702.
62. Oostra M., de Haan C. A., de Groot R. J., Rottier P. J., Glycosylation of the severe acute respiratory syndrome coronavirus triple-spanning membrane proteins 3a and M., J. Virol., 2006, 80, 2326-2336.
63. Schowalter R. M., Smith S. E., Dutch R. E., Characterization of Human Metapneumovirus F Protein-Promoted Membrane Fusion: Critical Roles for Proteolytic Processing and Low pH, J. Virol., 2006, 80, 10931-10941.
64. Bowden T. A., Crispin M., Harvey D. J., Jones E. Y., Stuart D. I., Dimeric architecture of the Hendra virus attachment glycoprotein: evidence for a conserved mode of assembly, J. Virol., 2010, 84, 6208-6217.
65. Bowden T. A., Crispin M., Harvey D. J., Aricescu A. R., Grimes J. M., Jones E. Y., et al., Crystal structure and carbohydrate analysis of Nipah virus attachment glycoprotein: a template for antiviral and vaccine design, J. Virol., 2008, 82, 11628-11636.
66. Botarelli P., Houlden B. A., Haigwood N. L., Servis C., Montagna D., Abrignani S., N-glycosylation of HIV-gp120 may constrain recognition by T lymphocytes, J. Immunol., 1991, 147, 3128-3132.
67. Zhu, X., Borchers, C., Bienstock, R. J., Tomer, K. B. (2000) Mass spectrometric characterization of the glycosylation pattern of HIV-gp120 expressed in CHO cells. Biochemistry 39, 11194-204.
68. Doores K. J., Bonomelli C., Harvey D. J., Vasiljevic S., Dwek R. A., Burton D. R., et al., Envelope glycans of immunodeficiency virions are almost entirely oligomannose antigens, Proc. Natl. Acad. Sci. USA, 2010, 107, 13800-13805.
69. Fenouillet E., Gluckman J. C., Bahraoui E., Role of N-linked glycans of envelope glycoproteins in infectivity of human immunodeficiency virus type 1, J. Virol., 1990, 64, 2841-2848.
70. Montefiori D. C., Robinson W. E. Jr., Mitchell W. M., Role of protein N-glycosylation in pathogenesis of human immunodeficiency virus type 1, Proc. Natl. Acad. Sci. USA, 1988, 85, 9248-9252.
71. 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, 1998, 393, 705-711.
72. Poumbourios P., Maerz A. L., Drummer H. E., Functional evolution of the HIV-1 envelope glycoprotein 120 association site of glycoprotein 41, J. Biol. Chem., 2003, 278, 42149-42160.
73. Bunnik E. M., Euler Z., Welkers M. R., Boeser-Nunnink B. D., Grijsen M. L., Prins J. M., et al., Adaptation of HIV-1 envelope gp120 to humoral immunity at a population level, Nat. Med., 2010, 16, 995-997.
74. Chaillon A., Braibant M., Moreau T., Thenin S., Moreau A., Autran B., et al., The V1V2 domain and a N-linked glycosylation site in the V3 loop of the HIV-1 envelope glycoprotein modulate neutralization sensitivity to the human broadly neutralizing antibody 2G12, J. Virol., 2011, 85, 3642-3648.
75. Sanders R. W., Venturi M., Schiffner L., Kalyanaraman R., Katinger H., Lloyd K. O., et al., The mannose-dependent epitope for neutralizing antibody 2G12 on human immunodeficiency virus type 1 glycoprotein gp120, J. Virol., 2002, 76, 7293-7305.
76. Calarese D. A., Lee H. K., Huang C. Y., Best M. D., Astronomo R. D., Stanfield R. L., et al., Dissection of the carbohydrate specificity of the broadly neutralizing anti-HIV-1 antibody 2G12, Proc. Natl. Acad. Sci. USA, 2005, 102, 13372-13377.
77. Calarese D. A., Scanlan C. N., Zwick M. B., Deechongkit S., Mimura Y., Kunert R., et al., Antibody domain exchange is an immunological solution to carbohydrate cluster recognition, Science, 2003, 300, 2065-2071.
78. Lai J., Bernhard O. K., Turville S. G., Harman A. N., Wilkinson J., Cunningham A. L., Oligomerization of the macrophage mannose receptor enhances gp120-mediated binding of HIV-1, J. Biol. Chem., 2009, 284, 11027-110238.
79. Frost S. D., Wrin T., Smith D. M., Kosakovsky Pond S. L., Liu Y., Paxinos E., et al., Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 enveloped.
80. Bonhomme C. J., Capul A. A., Lauron E. J., Bederka L. H., Knopp K. A., Buchmeier M. J. Glycosylation modulates arenavirus glycoprotein expression and function, Virology, 2011, 409, 223-233.
81. Feldmann H., Nichol S. T., Klenk H. D., Peters C. J., Sanchez A., Characterization of filoviruses based on differences in structure and antigenicity of the virion glycoprotein, Virology, 1994, 199, 469-473.
82. Simmons G., Wool-Lewis R. J., Baribaud F., Netter R. C., Bates P., Ebola virus glycoproteins induce global surface protein down-modulation and loss of cell adherence, J. Virol., 2002, 76, 2518-2528.
83. Dowling W., Thompson E., Badger C., Mellquist J. L., Garrison A. R., Smith J. M., et al., Influences of glycosylation on antigenicity, immunogenicity, and protective efficacy of ebola virus GP DNA vaccines, J. Virol., 2007, 81, 1821-1837.
84. Shi X., Elliott R. M., Analysis of N-linked glycosylation of hantaan virus glycoproteins and the role of oligosaccharide side chains in protein folding and intracellular trafficking, J. Virol., 2004, 78, 5414-5422.
85. Zheng F., Ma L., Shao L., Wang G., Chen F., Zhang Y., et al., Defining the N-linked glycosylation site of Hantaan virus envelope glycoproteins essential for cell fusion, J. Microbiol., 2007, 45, 41-47.
86. Robinson M. J., Sancho D., Slack E. C., LeibundGut-Landmann S., Reis e Sousa C., Myeloid C-type lectins in innate immunity, Nat. Immunol., 2006, 7, 1258-1265.
87. Weis W. I., Taylor M. E., Drickamer K., The C-type lectin superfamily in the immune system, Immunol. Rev., 1998, 163, 19-34.
88. Cambi A., de Lange F., van Maarseveen N. M., Nijhuis M., Joosten B., van Dijk E. M., et al., Microdomains of the C-type lectin DC-SIGN are portals for virus entry into dendritic cells, J. Cell Biol., 2004, 64, 145-155.
89. Cambi A., Figdor C. G., Dual function of C-type lectin-like receptors in the immune system, Curr. Opin. Cell Biol., 2003, 15, 539-546.
90. Geijtenbeek T. B., van Vliet S. J., Engering A., Hart B. A., van Kooyk Y., Self- and nonself-recognition by C-type lectins on dendritic cells, Annu. Rev. Immunol., 2004, 22, 33-54.
91. Rogers N. C., Slack E. C., Edwards A. D., Nolte M. A., Schulz O., Schweighoffer E., et al., Sykdependent cytokine induction by Dectin-1 reveals a novel pattern recognition pathway for C type lectins, Immunity, 2005, 22, 507-517.
92. Meyer-Wentrup F., Cambi A., Adema G. J., Figdor C. G., "Sweet talk": closing in on C type lectin signaling, Immunity, 2005, 22, 399-400.
93. Upham J. P., Pickett D., Irimura T., Anders E. M., Reading P. C., Macrophage receptors for influenza A virus: role of the macrophage galactose-type lectin and mannose receptor in viral entry, J. Virol., 2010, 84, 3730-3737.
94. Reading P. C., Miller J. L., Anders E. M., Involvement of the mannose receptor in infection of macrophages by influenza virus, J. Virol., 2000, 74, 5190-5197.
95. Nguyen D. G., Hildreth J. E., Involvement of macrophage mannose receptor in the binding and transmission of HIV by macrophages, Eur. J. Immunol., 2003, 33, 483-493.
96. Vigerust D. J., Egan B. S., Shepherd V. L., HIV-1 Nef mediates post-translational down-regulation and redistribution of the mannose receptor, J. Leukoc. Biol., 2005, 77, 522-534.
97. Reiling N., Blumenthal A., Flad H. D., Ernst M., Ehlers S., Mycobacteria-induced TNF-alpha and IL-10 formation by human macrophages is differentially regulated at the level of mitogenactivated protein kinase activity, J. Immunol., 2001, 167, 3339-3345.
98. Bergman M., Del Prete G., van Kooyk Y., Appelmelk B., Helicobacter pylori phase variation, immune modulation and gastric autoimmunity, Nat. Rev. Microbiol., 2006, 4, 151-159.
99. Cocquerel L., Voisset C., Dubuisson J., Hepatitis C virus entry: potential receptors and their biological functions, J. Gen. Virol., 2006, 87, 1075-1084.
100. Lozach P. Y., Lortat-Jacob H., de Lacroix de Lavalette A., Staropoli I., Foung S., Amara, A., et al., DC-SIGN and L-SIGN are high affinity binding receptors for hepatitis C virus glycoprotein E2, J. Biol. Chem., 2003, 278, 20358-20366.
101. Martina B. E., Koraka P., van den Doel P., Rimmelzwaan G. F., Haagmans B. L., Osterhaus A. D., DC-SIGN enhances infection of cells with glycosylated West Nile virus in vitro and virus replication in human dendritic cells induces production of IFN-alpha and TNF-alpha, Virus Res., 2008, 135, 64-71.
102. Hacker K., White L., de Silva A. M., N-linked glycans on dengue viruses grown in mammalian and insect cells, J. Gen. Virol., 2009, 90, 2097-2106.
103. Davis C. W., Mattei L. M., Nguyen H. Y., Ansarah-Sobrinho C., Doms R. W., Pierson T. C., The location of asparagine-linked glycans on West Nile virions controls their interactions with CD209 (DCSIGN), J. Biol. Chem., 2006, 281, 37183-37194.
104. Davis C. W., Nguyen H. Y., Hanna S. L., Sanchez M. D., Doms R. W., Pierson T. C., West Nile virus discriminates between DC-SIGN and DC-SIGNR for cellular attachment and infection, J. Virol., 2006, 80, 1290-1301.
105. Lin G., Simmons G., Pohlmann S., Baribaud F., Ni H., Leslie G. J., et al., Differential N-linked glycosylation of human immunodeficiency virus and Ebola virus envelope glycoproteins modulates interactions with DC-SIGN and DC-SIGNR, J. Virol., 2003, 77, 1337-1346.
106. Turville S. G., Arthos J., Donald K. M., Lynch G., Naif H., Clark G., et al., HIV gp120 receptors on human dendritic cells, Blood, 2001, 98, 2482-2488.
107. Liu Y., Liu H., Kim B. O., Gattone V. H., Li J., Nath A., et al., CD4-independent infection of astrocytes by human immunodeficiency virus type 1: requirement for the human mannose receptor, J. Virol., 2004, 78, 4120-4133.
108. Gramberg T., Hofmann H., Moller P., Lalor P. F., Marzi A., Geier M., et al., LSECtin interacts with filovirus glycoproteins and the spike protein of SARS coronavirus, Virology, 2005, 340, 224-236.
109. Pipirou Z., Powlesland A. S., Steffen I., Pohlmann S., Taylor M. E., Drickamer K., Mouse LSECtin as a model for a human Ebola virus receptor, Glycobiology, 2011, 21, 806-812.
110. Li Y., Hao B., Kuai X., Xing G., Yang J., Chen J., et al., C-type lectin LSECtin interacts with DCSIGNR and is involved in hepatitis C virus binding, Mol. Cell. Biochem., 2009, 327, 183-190.
111. Francois K. O., Balzarini J., Potential of carbohydrate-binding agents as therapeutics against enveloped viruses, Med. Res. Rev., 2010, 31.
112. Witvrouw M., Fikkert V., Hantson A., Pannecouque C., O'Keefe B. R., McMahon J., et al., Resistance of human immunodeficiency virus type 1 to the high-mannose binding agents cyanovirin N and concanavalin A, J. Virol., 2005, 79, 7777-7784.
113. Williams D. C. Jr., Lee J. Y., Cai M., Bewley C. A., Clore G. M., Crystal structures of the HIV-1 inhibitory cyanobacterial protein MVL free and bound to Man3GlcNAc2: structural basis for specificity and high-affinity binding to the core pentasaccharide from n-linked oligomannoside, J. Biol. Chem., 2005, 280, 29269-29276.
114. Balzarini J., van Herrewege Y., Vermeire K., Vanham G., Schols D., Carbohydrate-binding agents efficiently prevent dendritic cell-specific intercellular adhesion molecule-3-grabbing nonintegrin (DC-SIGN)-directed HIV-1 transmission to T lymphocytes, Mol. Pharmacol., 2007, 71, 3-11.
115. O'Keefe B. R., Smee D. F., Turpin J. A., Saucedo C. J., Gustafson K. R., Mori T., et al., Potent antiinfluenza activity of cyanovirin-N and interactions with viral hemagglutinin, Antimicrob. Agents Chemother., 2003, 47, 2518-2525.
116. Balzarini J., Carbohydrate-binding agents: a potential future cornerstone for the chemotherapy of enveloped viruses?, Antivir. Chem. Chemother., 2007, 18, 1-11.
117. Bertaux C., Daelemans D., Meertens L., Cormier E. G., Reinus J. F., Peumans W. J., et al., Entry of hepatitis C virus and human immunodeficiency virus is selectively inhibited by carbohydrate-binding agents but not by polyanions, Virology, 2007, 36, 40-50.
118. Micewicz E. D., Cole A. L., Jung C. L., Luong H., Phillips M. L., Pratikhya P., et al., Grifonin-1: a small HIV-1 entry inhibitor derived from the algal lectin, Griffithsin, PLoS One, 2010, 5, e14360.
119. Romanelli F., Smith K. M., Hoven A. D., Chloroquine and hydroxychloroquine as inhibitors of human immunodeficiency virus (HIV-1) activity, Curr. Pharm. Des., 2004, 10, 2643-2648.
120. Boelaert J. R., Sperber K., Piette J., Chloroquine exerts an additive in vitro anti-HIV type 1 effect when associated with didanosine and hydroxyurea, AIDS Res. Hum. Retroviruses, 1999, 15, 1241-7124.
121. Sperber K., Louie M., Kraus T., Proner J., Sapira E., Lin S., et al., Hydroxychloroquine treatment of patients with human immunodeficiency virus type 1, Clin. Ther., 1995, 17, 622-636.
122. Paton N. I., Aboulhab J., Hydroxychloroquine, hydroxyurea and didanosine as initial therapy for HIV-infected patients with low viral load: safety, efficacy and resistance profile after 144 weeks, HIV Med., 2005, 6, 13-20.
123. Naarding M. A., Baan E., Pollakis G., Paxton W. A., Effect of chloroquine on reducing HIV-1 replication in vitro and the DC-SIGN mediated transfer of virus to CD4+ T-lymphocytes, Retrovirology, 2007, 4, 6.
124. Vincent M. J., Bergeron E., Benjannet S., Erickson B. R., Rollin P. E., Ksiazek T. G., et al., Chloroquine is a potent inhibitor of SARS coronavirus infection and spread, Virol. J., 2005, 2, 69.
125. De Clercq E., Potential antivirals and antiviral strategies against SARS coronavirus infections, Expert Rev. Anti Infect. Ther., 2006, 4, 291-302.
126. Keyaerts E., Vijgen L., Maes P., Neyts J., van Ranst M., In vitro inhibition of severe acute respiratory syndrome coronavirus by chloroquine, Biochem. Biophys. Res. Commun., 2004, 323, 264-268.
127. Di Trani L., Savarino A., Campitelli L., Norelli S., Puzelli S., D'Ostilio D., et al., Different pH requirements are associated with divergent inhibitory effects of chloroquine on human and avian influenza A viruses, Virol. J., 2007, 4, 39.
128. Ooi E. E., Chew J. S., Loh J. P., Chua R. C., In vitro inhibition of human influenza A virus replication by chloroquine, Virol. J., 2006, 3, 39.
129. Savarino A., Di Trani L., Donatelli I., Cauda R., Cassone A., New insights into the antiviral effects of chloroquine, Lancet Infect. Dis., 2006, 6, 67-69.
130. st century, Int. J. Antimicrob. Agents, 2007, 30, 297-308.
131. Vigerust D. J., McCullers J. A., Chloroquine is effective against influenza A virus in vitro but not in vivo, Influenza Other Respi Viruses, 2007, 1, 189-192.
132. Fedson D. S., Confronting an influenza pandemic with inexpensive generic agents: can it be done?, Lancet Infect. Dis., 2008, 8, 571-576.
133. Dwek R. A., Butters T. D., Platt F. M., Zitzmann N., Targeting glycosylation as a therapeutic approach, Nat. Rev. Drug Discov., 2002, 1, 65-75.
134. Chang J., Schul W., Butters T. D., Yip A., Liu B., Goh A., et al., Combination of alpha-glucosidase inhibitor and ribavirin for the treatment of dengue virus infection in vitro and in vivo, Antiviral Res., 2011, 89, 26-34.
135. Chang J., Wang L., Ma D., Qu X., Guo H., Xu X., et al., Novel imino sugar derivatives demonstrate potent antiviral activity against flaviviruses, Antimicrob. Agents Chemother., 2009, 53, 1501-1508.
136. Vancova M., Nebesarova J., Grubhoffer L., Lectin-binding characteristics of a Lyme borreliosis spirochete Borrelia burgdorferi sensu stricto, Folia Microbiol., (Praha), 2005, 50, 229-238.
137. Logan S. M., Hui J. P., Vinogradov E., Aubry A. J., Melanson J. E., Kelly J. F., et al., Identification of novel carbohydrate modifications on Campylobacter jejuni 11168 flagellin using metabolomics-based approaches, FEBS J., 2009, 276, 1014-1023.
138. Appelmelk B. J., den Dunnen J., Driessen N. N., Ummels R., Pak M., Nigou J., et al., The mannose cap of mycobacterial lipoarabinomannan does not dominate the Mycobacterium-host interaction, Cell Microbiol., 2008, 10, 930-944.
139. Twine S. M., Paul C. J., Vinogradov E., McNally D. J., Brisson J. R., Mullen J. A., et al., Flagellar glycosylation in Clostridium botulinum, FEBS J., 2008, 275, 4428-4444.
140. Romanova J., Katinger D., Ferko B., Voglauer R., Mochalova L., Bovin N., et al., Distinct host range of influenza H3N2 virus isolates in Vero and MDCK cells is determined by cell specific glycosylation pattern, Virology, 2003, 307, 90-97.
141. Wright K. E., Spiro R. C., Burns J. W., Buchmeier M. J., Post-translational processing of the glycoproteins of lymphocytic choriomeningitis virus, Virology, 1990, 177, 175-183.
142. Branco L. M., Garry R. F., Characterization of the Lassa virus GP1 ectodomain shedding: implications for improved diagnostic platforms, Virol. J., 2009, 6, 147.
143. Martinez I., Melero J. A., Binding of human respiratory syncytial virus to cells: implication of sulfated cell surface proteoglycans, J. Gen. Virol., 2000, 81, 2715-2722.
144. Feinberg H., Castelli R., Drickamer K., Seeberger P. H., Weis W. I., Multiple modes of binding enhance the affinity of DC-SIGN for high mannose N-linked glycans found on viral glycoproteins, J. Biol. Chem., 2007, 282, 4202-4209.