Glycans in infectious diseases. A molecular recognition perspective

Current Medicinal Chemistry

Volumn 24, Issue 36, 2017, Pages 4057-4080

  Unione, Luca ^a   Gimeno, Ana ^a   Valverde, Pablo ^a   Calloni, Ilaria ^a,c   Coelho, Helena ^a,c,d   Mirabella, Stefania ^a,e   Poveda, Ana ^a   Ardá, Ana ^a   Jiménez Barbero, Jesús ^a,b,c  

^a CIC BIOGUNE   (Spain)

^b BASQUE FOUNDATION FOR SCIENCE   (Spain)

^c UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^d UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^e UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Bacterial infection; Glycans; Lectin; Molecular recognition; NMR; Viral infection; X ray

Indexed keywords

CD14 ANTIGEN; GLYCAN DERIVATIVE; LANGERIN; TOLL LIKE RECEPTOR 4; VIRUS RECEPTOR; VIRUS SIALIDASE; ANTIVIRUS AGENT; CD207 PROTEIN, HUMAN; LECTIN; LEUKOCYTE ANTIGEN; MANNOSE BINDING LECTIN; POLYSACCHARIDE; PROTEIN BINDING; SIALIDASE;

ANTIVIRAL RESISTANCE; BACTERIAL INFECTION; BACTERIUM ADHERENCE; CLOSTRIDIUM DIFFICILE INFECTION; HOST CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE SYSTEM; INFECTION; INFLUENZA VIRUS; MOLECULAR RECOGNITION; NONHUMAN; PLAGUE; PROTEIN BINDING; PROTEIN STRUCTURE; REVIEW; ROTAVIRUS; ROTAVIRUS INFECTION; VIRUS INFECTION; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; COMMUNICABLE DISEASE; ENZYMOLOGY; INFLUENZA A VIRUS; METABOLISM; PATHOLOGY;

ANIMALS; ANTIGENS, CD; ANTIVIRAL AGENTS; BACTERIAL ADHESION; BACTERIAL INFECTIONS; COMMUNICABLE DISEASES; HUMANS; INFLUENZA A VIRUS; LECTINS, C-TYPE; MANNOSE-BINDING LECTINS; NEURAMINIDASE; POLYSACCHARIDES; PROTEIN BINDING; TOLL-LIKE RECEPTOR 4; VIRUS DISEASES;

EID: 85038218237     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/0929867324666170217093702     Document Type: Review

References (168)

1. Das, K. Antivirals targeting influenza A virus. J. Med. Chem., 2012, 55(14), 6263-6277.
2. Gamblin, S.J.; Skehel, J.J. Influenza hemagglutinin and neuraminidase membrane glycoproteins. J. Biol. Chem., 2010, 285(37), 28403-28409.
3. Gong, J.; Xu, W.; Zhang, J. Structure and functions of influenza virus neuraminidase. Curr. Med. Chem., 2007, 14(1), 113-122.
4. Varghese, J.N.; Laver, W.G.; Colman, P.M. Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 A resolution., Nature, 1983, 303(5912), 35-40.
5. Russell, R.J.; Haire, L.F.; Stevens, D.J.; Collins, P.J.; Lin, Y.P.; Blackburn, G.M.; Hay, A.J.; Gamblin, S. J.; Skehel, J.J. The structure of H5N1 avian influenza neuraminidase suggests new opportunities for drug design. Nature, 2006, 443(7107), 45-49.
6. Wang, M.; Qi, J.; Liu, Y.; Vavricka, C.J.; Wu, Y.; Li, Q.; Gao, G.F. Influenza A virus N5 neuraminidase has an extended 150-cavity. J. Virol., 2011, 85(16), 8431-8435.
7. Li, Q.; Qi, J.; Wu, Y.; Kiyota, H.; Tanaka, K.; Suhara, Y.; Ohrui, H.; Suzuki, Y.; Vavricka, C.J.; Gao, G.F. Functional and structural analysis of influenza virus neuraminidase N3 offers further insight into the mechanisms of oseltamivir resistance. J. Virol., 2013, 87(18), 10016-10024.
8. Sun, X.; Li, Q.; Wu, Y.; Wang, M.; Liu, Y.; Qi, J.; Vavricka, C.J.; Gao, G.F. Structure of influenza virus N7: the last piece of the neuraminidase "jigsaw" puzzle. J. Virol., 2014, 88(16), 9197-9207.
9. Bossart-Whitaker, P.; Carson, M.; Babu, Y.S.; Smith, C.D.; Laver, W.G.; Air, G.M. Three-dimensional structure of influenza A N9 neuraminidase and its complex with the inhibitor 2-deoxy 2,3-dehydro-N-acetyl neuraminic acid. J. Mol. Biol., 1993, 232(4), 1069-1083.
10. Burmeister, W.P.; Ruigrok, R.W.; Cusack, S. The 2.2 A resolution crystal structure of influenza B neuraminidase and its complex with sialic acid. Embo J., 1992, 11(1), 49-56.
11. Zhu, X.; Yang, H.; Guo, Z.; Yu, W.; Carney, P.J.; Li, Y.; Chen, L.M.; Paulson, J.C.; Donis, R.O.; Tong, S.; Stevens, J.; Wilson, I.A. Crystal structures of two subtype N10 neuraminidase-like proteins from bat influenza A viruses reveal a diverged putative active site. Proc. Natl. Acad. Sci. USA., 2012, 109(46), 18903-18908.
12. Colman, P.M.; Varghese, J.N.; Laver, W.G. Structure of the catalytic and antigenic sites in influenza virus neuraminidase. Nature, 1983, 303(5912), 41-44.
13. Varghese, J.N.; McKimm-Breschkin, J.L.; Caldwell, J.B.; Kortt, A.A.; Colman, P.M. The structure of the complex between influenza virus neuraminidase and sialic acid, the viral receptor. Proteins, 1992, 14(3), 327-332.
14. Zhu, X.; McBride, R.; Nycholat, C.M.; Yu, W.; Paulson, J.C.; Wilson, I.A. Influenza virus neuraminidases with reduced enzymatic activity that avidly bind sialic acid receptors. J. Virol., 2012, 86(24), 13371-13383.
15. Garcia, J.-M.; Lai, J. C.C.; Haselhorst, T.; Choy, K.T.; Yen, H.-L.; Peiris, J.S.M.; von Itzstein, M.; Nicholls, J.M. Investigation of the binding and cleavage characteristics of N1 neuraminidases from avian, seasonal, and pandemic influenza viruses using saturation transfer difference nuclear magnetic resonance. Influenza Other Respir. Viruses. 2014, 8(2), 235-242.
16. Influenza Antiviral Medications: Summary for Clinicians. Available at: http://www.cdc.gov/flu/professionals/antivirals/ summary-clinicians.htm [Accessed September 18, 2016].
17. Daiichi Sankyo Receives Approval to Manufacture and Market Inavir(R) Influenza Antiviral Inhalant for Treatment in Japan. Available at: http://www.daiichisankyo.com/ media- investors/media-relations/press-releases/detail/005703. html [Accessed September 18, 2016].
18. von Itzstein, M.; Wu, W.Y.; Kok, G.B.; Pegg, M.S.; Dyason, J.C.; Jin, B.; Van Phan, T.; Smythe, M. L.; White, H. F.; Oliver, S. W.; Colman, P.M.; Varghese, J. N.; Ryan, D.M.; Woods, J.M.; Bethell, R.C.; Hotham, V.J.; Cameron, J.M.; Penn, C.R. Rational design of potent sialidase-based inhibitors of influenza virus replication. Nature, 1993, 363(6428), 418-423.
19. Kim, C.U.; Lew, W.; Williams, M.A.; Liu, H.; Zhang, L.; Swaminathan, S.; Bischofberger, N.; Chen, M.S.; Mendel, D.B.; Tai, C.Y.; Laver, W.G.; Stevens, R.C. Influenza neuraminidase inhibitors possessing a novel hydrophobic interaction in the enzyme active site: Design, synthesis, and structural analysis of carbocyclic sialic acid analogues with potent anti-influenza activity. J. Am. Chem. Soc., 1997, 119(4), 681-690.
20. Babu, Y. S.; Chand, P.; Bantia, S.; Kotian, P.; Dehghani, A.; El-Kattan, Y.; Lin, T. H.; Hutchison, T.L.; Elliott, A.J.; Parker, C.D.; Ananth, S.L.; Horn, L.L.; Laver, G.W.; Montgomery, J.A. BCX-1812 (RWJ-270201): Discovery of a novel, highly potent, orally active, and selective influenza neuraminidase inhibitor through structure-based drug design. J. Med. Chem., 2000, 43(19), 3482-3486.
21. Vavricka, C.J.; Li, Q.; Wu, Y.; Qi, J.; Wang, M.; Liu, Y.; Gao, F.; Liu, J.; Feng, E.; He, J.; Wang, J.; Liu, H.; Jiang, H.; Gao, G.F. Structural and functional analysis of laninamivir and its octanoate prodrug reveals group specific mechanisms for influenza NA inhibition. PLoS Pathog., 2011, 7(10), e1002249.
22. Amaro, R.E.; Swift, R.V.; Votapka, L.; Li, W.W.; Walker, R.C.; Bush, R.M. Mechanism of 150-cavity formation in influenza neuraminidase. Nat. Commun., 2011, 2, 388.
23. Rudrawar, S.; Dyason, J.C.; Rameix-Welti, M.A.; Rose, F.J.; Kerry, P.S.; Russell, R.J.; van der Werf, S.; Thomson, R.J.; Naffakh, N.; von Itzstein, M. Novel sialic acid derivatives lock open the 150-loop of an influenza A virus group- 1 sialidase. Nat. Commun., 2010, 1(113).
24. Das, A.; Adak, A.K.; Ponnapalli, K.; Lin, C.H.; Hsu, K.C.; Yang, J.M.; Hsu, T.A.; Lin, C.C. Design and synthesis of 1,2,3-triazole-containing N-acyl zanamivir analogs as potent neuraminidase inhibitors. Eur. J. Med. Chem., 2016, 123 397-406.
25. Xie, Y.; Xu, D.; Huang, B.; Ma, X.; Qi, W.; Shi, F.; Liu, X.; Zhang, Y.; Xu, W. Discovery of N-substituted oseltamivir derivatives as potent and selective inhibitors of H5N1 influenza neuraminidase. J. Med. Chem., 2014, 57(20), 8445-8458.
26. Liu, P.; Wang, Z.; Zhang, L.; Li, D.; Lin, J. The Mechanism by which 146-N-glycan affects the active site of neuraminidase. PLoS One, 2015, 10(8), e0135487.
27. Lai, J.C.; Garcia, J.M.; Dyason, J.C.; Bohm, R.; Madge, P.D.; Rose, F.J.; Nicholls, J.M.; Peiris, J.S.; Haselhorst, T.; von Itzstein, M. A secondary sialic acid binding site on influenza virus neuraminidase: fact or fiction? Angew. Chem. Int. Ed. Engl., 2012, 51(9), 2221-2224.
28. Sung, J.C.; Van Wynsberghe, A.W.; Amaro, R.E.; Li, W.W.; McCammon, J. A. Role of secondary sialic acid binding sites in influenza N1 neuraminidase. J. Am. Chem. Soc., 2010, 132(9), 2883-2885.
29. Phillips, A.M.; Shoulders, M.D. The path of least resistance: Mechanisms to reduce influenza's sensitivity to oseltamivir. J. Mol. Biol., 2016, 428(3), 533-537.
30. Collins, P.J.; Haire, L.F.; Lin, Y.P.; Liu, J.; Russell, R.J.; Walker, P.A.; Skehel, J.J.; Martin, S.R.; Hay, A.J.; Gamblin, S.J. Crystal structures of oseltamivir-resistant influenza virus neuraminidase mutants. Nature, 2008, 453(7199), 1258-1261.
31. van der Vries, E.; Collins, P.J.; Vachieri, S.G.; Xiong, X.; Liu, J.; Walker, P.A.; Haire, L.F.; Hay, A.J.; Schutten, M.; Osterhaus, A.D.; Martin, S.R.; Boucher, C.A.; Skehel, J.J.; Gamblin, S.J. H1N1 2009 pandemic influenza virus: resistance of the I223R neuraminidase mutant explained by kinetic and structural analysis. PLoS Pathog., 2012, 8(9), e1002914.
32. Escuret, V.; Collins, P.J.; Casalegno, J.S.; Vachieri, S.G.; Cattle, N.; Ferraris, O.; Sabatier, M.; Frobert, E.; Caro, V.; Skehel, J.J.; Gamblin, S.; Valla, F.; Valette, M.; Ottmann, M.; McCauley, J.W.; Daniels, R. .; Lina, B. A novel I221L substitution in neuraminidase confers high-level resistance to oseltamivir in influenza B viruses. J. Infect. Dis., 2014, 210(8), 1260-1269.
33. Cheng, C.K.; Tsai, C.H.; Shie, J.J.; Fang, J.M. From neuraminidase inhibitors to conjugates: a step towards better anti-influenza drugs? Future Med. Chem., 2014, 6(7), 757-774.
34. Gouin, S. G. Multivalent inhibitors for carbohydrateprocessing enzymes: beyond the "lock-and-key" concept. Chem. Eur. J., 2014, 20(37), 11616-11628.
35. Macdonald, S.J.; Watson, K.G.; Cameron, R.; Chalmers, D.K.; Demaine, D.A.; Fenton, R.J.; Gower, D.; Hamblin, J.N.; Hamilton, S.; Hart, G.J.; Inglis, G.G.; Jin, B.; Jones, H.T.; McConnell, D.B.; Mason, A.M.; Nguyen, V.; Owens, I.J.; Parry, N.; Reece, P.A.; Shanahan, S.E.; Smith, D.; Wu, W.Y.; Tucker, S.P. Potent and long-acting dimeric inhibitors of Influenza virus neuraminidase are effective at a once-weekly dosing regimen. Antimicrob. Agents Chemother., 2004, 48(12), 4542-4549.
36. Fu, L.; Bi, Y.; Wu, Y.; Zhang, S.; Qi, J.; Li, Y.; Lu, X.; Zhang, Z.; Lv, X.; Yan, J.; Gao, G.F.; Li, X. Structure- Based Tetravalent Zanamivir with Potent Inhibitory Activity against drug-resistant influenza viruses. J. Med. Chem., 2016, 59(13), 6303-6312.
37. Kim, J.H.; Resende, R.; Wennekes, T.; Chen, H.M.; Bance, N.; Buchini, S.; Watts, A.G.; Pilling, P.; Streltsov, V.A.; Petric, M.; Liggins, R.; Barrett, S.; McKimm-Breschkin, J.L.; Niikura, M.; Withers, S.G. Mechanism-based covalent neuraminidase inhibitors with broad-spectrum influenza antiviral activity. Science, 2013, 340(6128), 71-75.
38. Weck, S.; Robinson, K.; Smith, M.R.; Withers, S.G. Understanding viral neuraminidase inhibition by substituted difluorosialic acids. Chem. Commun. (Camb)., 2015, 51(14), 2933-2935.
39. Papini, N.; Anastasia, L.; Tringali, C.; Croci, G.; Bresciani, R.; Yamaguchi, K.; Miyagi, T.; Preti, A.; Prinetti, A.; Prioni, S.; Sonnino, S.; Tettamanti, G.; Venerando, B.; Monti, E. The plasma membrane-associated sialidase MmNEU3 modifies the ganglioside pattern of adjacent cells supporting its involvement in cell-to-cell interactions. J. Biol. Chem., 2004, 279(17), 16989-16995.
40. Chavas, L.M.; Kato, R.; Suzuki, N.; von Itzstein, M.; Mann, M.C.; Thomson, R.J.; Dyason, J.C.; McKimm-Breschkin, J.; Fusi, P.; Tringali, C.; Venerando, B.; Tettamanti, G.; Monti, E.; Wakatsuki, S. Complexity in Influenza virus targeted drug design: Interaction with human sialidases. J. Med. Chem., 2010, 53(7), 2998-3002.
41. Jones, M.; Hama, R.; Jefferson, T.; Doshi, P. Neuropsychiatric adverse events and oseltamivir for prophylaxis. Drug. Saf., 2012, 35(12), 1187-1188.
42. Sriwilaijaroen, N.; Magesh, S.; Imamura, A.; Ando, H.; Ishida, H.; Sakai, M.; Ishitsubo, E.; Hori, T.; Moriya, S.; Ishikawa, T.; Kuwata, K.; Odagiri, T.; Tashiro, M.; Hiramatsu, H.; Tsukamoto, K.; Miyagi, T.; Tokiwa, H.; Kiso, M.; Suzuki, Y. A Novel potent and highly specific inhibitor against influenza viral N1-N9 neuraminidases: Insight into neuraminidase-inhibitor Interactions. J. Med. Chem., 2016, 59(10), 4563-4577.
43. Antanasijevic, A.; Kingsley, C.; Basu, A.; Bowlin, T. L.; Rong, L.; Caffrey, M. Application of virus-like particles (VLP) to NMR characterization of viral membrane protein interactions. J. Biomol. NMR., 2016, 64(3), 255-265.
44. Stencel-Baerenwald, J.E.; Reiss, K.; Reiter, D.M.; Stehle, T.; Dermody, T.S. The sweet spot: Defining virus-sialic acid interactions. Nat. Rev. Microbiol., 2014, 12(11), 739-749.
45. Fleming, F.E.; Bohm, R.; Dang, V.T.; Holloway, G.; Haselhorst, T.; Madge, P.D.; Deveryshetty, J.; Yu, X.; Blanchard, H.; von Itzstein, M.; Coulson, B.S. Relative roles of GM1 ganglioside, N-acylneuraminic acids, and alpha2beta1 integrin in mediating rotavirus infection. J. Virol., 2014, 88(8), 4558-4571.
46. Liu, Y.; Ramelot, T.A.; Huang, P.; Liu, Y.; Li, Z.; Feizi, T.; Zhong, W.; Wu, F.T.; Tan, M.; Kennedy, M.A.; Jiang, X. Glycan specificity of P[19] Rotavirus and comparison with those of related P genotypes. J. Virol., 2016, 90(21), 9983-9996.
47. Santos, N.; Hoshino, Y. Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev. Med. Virol., 2005, 15(1), 29-56.
48. Weiss, R.A. how does HIV cause AIDS? Science, 1993, 260(5112), 1273-1279.
49. Douek, D.C.; Roederer, M.; Koup, R.A. Emerging concepts in the immunopathogenesis of AIDS. Annu. Rev. Med., 2009, 60, 471-484.
50. Cunningham, A.L.; Donaghy, H.; Harman, A.N.; Kim, M.; Turville, S.G. Manipulation of dendritic cell function by viruses. Curr. Opin. Microbiol., 2010, 13 (4), 524-529.
51. Pancera, M.; Zhou, T.; Druz, A.; Georgiev, I. S.; Soto, C.; Gorman, J.; Huang, J.; Acharya, P.; Chuang, G. Y.; Ofek, G.; Stewart-Jones, G. B.; Stuckey, J.; Bailer, R. T.; Joyce, M. G.; Louder, M. K.; Tumba, N.; Yang, Y.; Zhang, B.; Cohen, M. S.; Haynes, B.F.; Mascola, J.R.; Morris, L.; Munro, J.B.; Blanchard, S.C.; Mothes, W.; Connors, M.; Kwong, P.D. Structure and immune recognition of trimeric pre-fusion HIV-1 Env. Nature, 2014, 514(7523), 455-461.
52. Doitsh, G.; Galloway, N.L.; Geng, X.; Yang, Z.; Monroe, K.M.; Zepeda, O.; Hunt, P.W.; Hatano, H.; Sowinski, S.; Munoz-Arias, I.; Greene, W.C. Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature, 2014, 505(7484), 509-514.
53. Banerjee, K.; Weliky, D.P. Folded monomers and hexamers of the ectodomain of the HIV gp41 membrane fusion protein: Potential roles in fusion and synergy between the fusion peptide, hairpin, and membrane-proximal external region. Biochemistry, 2014, 53(46), 7184-7198.
54. Pritchard, L.K.; Harvey, D.J.; Bonomelli, C.; Crispin, M.; Doores, K.J. Cell- and protein-directed glycosylation of native cleaved HIV-1 envelope. J. Virol., 2015, 89(17), 8932-8944.
55. 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.
56. Wolfert, M.A.; Boons, G.J. Adaptive immune activation: Glycosylation does matter. Nat. Chem. Biol., 2013, 9(12), 776-784.
57. Pritchard, L.K.; Vasiljevic, S.; Ozorowski, G.; Seabright, G.E.; Cupo, A.; Ringe, R.; Kim, H.J.; Sanders, R.W.; Doores, K.J.; Burton, D.R.; Wilson, I.A.; Ward, A.B.; Moore, J.P.; Crispin, M. Structural constraints determine the glycosylation of HIV-1 envelope trimers. Cell Rep., 2015, 11(10), 1604-1613.
58. Behrens, A.J.; Vasiljevic, S.; Pritchard, L.K.; Harvey, D.J.; Andev, R.S.; Krumm, S.A.; Struwe, W.B.; Cupo, A.; Kumar, A.; Zitzmann, N.; Seabright, G.E.; Kramer, H.B.; Spencer, D.I.; Royle, L.; Lee, J.H.; Klasse, P.J.; Burton, D.R.; Wilson, I.A.; Ward, A.B.; Sanders, R.W.; Moore, J.P.; Doores, K.J.; Crispin, M. Composition and antigenic effects of individual glycan sites of a trimeric HIV-1 envelope glycoprotein. Cell Rep., 2016, 14(11), 2695-2706.
59. Crooks, E.T.; Tong, T.; Osawa, K.; Binley, J.M. Enzyme digests eliminate nonfunctional Env from HIV-1 particle surfaces, leaving native Env trimers intact and viral infectivity unaffected. J. Virol., 2011, 85(12), 5825-5839.
60. Wu, X.; Yang, Z.Y.; Li, Y.; Hogerkorp, C.M.; Schief, W.R.; Seaman, M.S.; Zhou, T.; Schmidt, S.D.; Wu, L.; Xu, L.; Longo, N.S.; McKee, K.; O'Dell, S.; Louder, M.K.; Wycuff, D.L.; Feng, Y.; Nason, M.; Doria-Rose, N.; Connors, M.; Kwong, P.D.; Roederer, M.; Wyatt, R.T.; Nabel, G.J.; Mascola, J.R. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV- 1. Science, 2010, 329(5993), 856-861.
61. Julien, J.P.; Cupo, A.; Sok, D.; Stanfield, R.L.; Lyumkis, D.; Deller, M.C.; Klasse, P.J.; Burton, D.R.; Sanders, R.W.; Moore, J.P.; Ward, A.B.; Wilson, I.A. Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science, 2013, 342(6165), 1477-1483.
62. Kwong, P.D.; Mascola, J.R. Human antibodies that neutralize HIV-1: identification, structures, and B cell ontogenies. Immunity, 2012, 37(3), 412-425.
63. Kwon, Y.D.; Pancera, M.; Acharya, P.; Georgiev, I.S.; Crooks, E.T.; Gorman, J.; Joyce, M.G.; Guttman, M.; Ma, X.; Narpala, S.; Soto, C.; Terry, D.S.; Yang, Y.; Zhou, T.; Ahlsen, G.; Bailer, R. T.; Chambers, M.; Chuang, G.Y.; Doria-Rose, N. A.; Druz, A.; Hallen, M.A.; Harned, A.; Kirys, T.; Louder, M.K.; O'Dell, S.; Ofek, G.; Osawa, K.; Prabhakaran, M.; Sastry, M.; Stewart-Jones, G.B.; Stuckey, J.; Thomas, P.V.; Tittley, T.; Williams, C.; Zhang, B.; Zhao, H.; Zhou, Z.; Donald, B. R.; Lee, L. K.; Zolla-Pazner, S.; Baxa, U.; Schon, A.; Freire, E.; Shapiro, L.; Lee, K.K.; Arthos, J.; Munro, J.B.; Blanchard, S.C.; Mothes, W.; Binley, J.M.; McDermott, A.B.; Mascola, J.R.; Kwong, P.D. Crystal structure, conformational fixation and entry-related interactions of mature ligand-free HIV-1 Env. Nat. Struct. Mol. Biol., 2015, 22(7), 522-531.
64. Pancera, M.; Shahzad-Ul-Hussan, S.; Doria-Rose, N.A.; McLellan, J.S.; Bailer, R.T.; Dai, K.; Loesgen, S.; Louder, M.K.; Staupe, R.P.; Yang, Y.; Zhang, B.; Parks, R.; Eudailey, J.; Lloyd, K. E.; Blinn, J.; Alam, S.M.; Haynes, B.F.; Amin, M.N.; Wang, L.X.; Burton, D.R.; Koff, W.C.; Nabel, G.J.; Mascola, J.R.; Bewley, C.A.; Kwong, P.D. Structural basis for diverse N-glycan recognition by HIV-1- neutralizing V1-V2-directed antibody PG16. Nat. Struct. Mol. Biol., 2013, 20(7), 804-813.
65. McLellan, J.S.; Pancera, M.; Carrico, C.; Gorman, J.; Julien, J.P.; Khayat, R.; Louder, R.; Pejchal, R.; Sastry, M.; Dai, K.; O'Dell, S.; Patel, N.; Shahzad-ul-Hussan, S.; Yang, Y.; Zhang, B.; Zhou, T.; Zhu, J.; Boyington, J.C.; Chuang, G.Y.; Diwanji, D.; Georgiev, I.; Kwon, Y.D.; Lee, D.; Louder, M.K.; Moquin, S.; Schmidt, S.D.; Yang, Z.Y.; Bonsignori, M.; Crump, J.A.; Kapiga, S.H.; Sam, N.E.; Haynes, B.F.; Burton, D.R.; Koff, W.C.; Walker, L.M.; Phogat, S.; Wyatt, R.; Orwenyo, J.; Wang, L.X.; Arthos, J.; Bewley, C.A.; Mascola, J.R.; Nabel, G.J.; Schief, W.R.; Ward, A.B.; Wilson, I.A.; Kwong, P. D. Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature, 2011, 480(7377), 336-343.
66. Kong, L.; Wilson, I. A.; Kwong, P. D. Crystal structure of a fully glycosylated HIV-1 gp120 core reveals a stabilizing role for the glycan at Asn262. Proteins, 2015, 83(3), 590-596.
67. Kong, L.; Lee, J. H.; Doores, K. J.; Murin, C. D.; Julien, J. P.; McBride, R.; Liu, Y.; Marozsan, A.; Cupo, A.; Klasse, P. J.; Hoffenberg, S.; Caulfield, M.; King, C. R.; Hua, Y.; Le, K. M.; Khayat, R.; Deller, M. C.; Clayton, T.; Tien, H.; Feizi, T.; Sanders, R. W.; Paulson, J. C.; Moore, J. P.; Stanfield, R. L.; Burton, D. R.; Ward, A. B.; Wilson, I. A. Supersite of immune vulnerability on the glycosylated face of HIV-1 envelope glycoprotein gp120. Nat. Struct. Mol. Biol., 2013, 20(7), 796-803.
68. Gorman, J.; Soto, C.; Yang, M. M.; Davenport, T. M.; Guttman, M.; Bailer, R. T.; Chambers, M.; Chuang, G. Y.; DeKosky, B. J.; Doria-Rose, N. A.; Druz, A.; Ernandes, M. J.; Georgiev, I. S.; Jarosinski, M. C.; Joyce, M. G.; Lemmin, T. M.; Leung, S.; Louder, M. K.; McDaniel, J. R.; Narpala, S.; Pancera, M.; Stuckey, J.; Wu, X.; Yang, Y.; Zhang, B.; Zhou, T.; Mullikin, J. C.; Baxa, U.; Georgiou, G.; McDermott, A. B.; Bonsignori, M.; Haynes, B. F.; Moore, P. L.; Morris, L.; Lee, K. K.; Shapiro, L.; Mascola, J.R.; Kwong, P.D. Structures of HIV-1 Env V1V2 with broadly neutralizing antibodies reveal commonalities that enable vaccine design. Nat. Struct. Mol. Biol., 2016, 23(1), 81-90.
69. Stewart-Jones, G. B.; Soto, C.; Lemmin, T.; Chuang, G. Y.; Druz, A.; Kong, R.; Thomas, P.V.; Wagh, K.; Zhou, T.; Behrens, A.J.; Bylund, T.; Choi, C.W.; Davison, J.R.; Georgiev, I.S.; Joyce, M.G.; Kwon, Y.D.; Pancera, M.; Taft, J.; Yang, Y.; Zhang, B.; Shivatare, S.S.; Shivatare, V.S.; Lee, C.C.; Wu, C.Y.; Bewley, C.A.; Burton, D.R.; Koff, W.C.; Connors, M.; Crispin, M.; Baxa, U.; Korber, B.T.; Wong, C.H.; Mascola, J.R.; Kwong, P.D. Trimeric HIV-1-Env Structures Define Glycan Shields from Clades A, B, and G. Cell, 2016, 165(4), 813-826.
70. Dodson, K.W.; Pinkner, J.S.; Rose, T.; Magnusson, G.; Hultgren, S.J.; Waksman, G. Structural basis of the interact tion of the pyelonephritic E. coli adhesin to its human kidney receptor. Cell, 2001, 105(6), 733-743.
71. Buts, L.; Bouckaert, J.; De Genst, E.; Loris, R.; Oscarson, S.; Lahmann, M.; Messens, J.; Brosens, E.; Wyns, L.; De Greve, H. The fimbrial adhesin F17-G of enterotoxigenic Escherichia coli has an immunoglobulin-like lectin domain that binds N-acetylglucosamine. Mol. Microbiol., 2003, 49(3), 705-715.
72. Bouckaert, J.; Berglund, J.; Schembri, M.; De Genst, E.; Cools, L.; Wuhrer, M.; Hung, C.S.; Pinkner, J.; Slattegard, R.; Zavialov, A.; Choudhury, D.; Langermann, S.; Hultgren, S. J.; Wyns, L.; Klemm, P.; Oscarson, S.; Knight, S. D.; De Greve, H. Receptor binding studies disclose a novel class of high-affinity inhibitors of the Escherichia coli FimH adhesin. Mol. Microbiol., 2005, 55(2), 441-455.
73. Wellens, A.; Garofalo, C.; Nguyen, H.; Van Gerven, N.; Slattegard, R.; Hernalsteens, J.P.; Wyns, L.; Oscarson, S.; De Greve, H.; Hultgren, S.; Bouckaert, J. Intervening with urinary tract infections using anti-adhesives based on the crystal structure of the FimH-oligomannose-3 complex. PLoS One, 2008, 3(4), e2040.
74. Wellens, A.; Lahmann, M.; Touaibia, M.; Vaucher, J.; Oscarson, S.; Roy, R.; Remaut, H.; Bouckaert, J. The tyrosine gate as a potential entropic lever in the receptor-binding site of the bacterial adhesin FimH. Biochemistry, 2012, 51(24), 4790-4799.
75. Vanwetswinkel, S.; Volkov, A.N.; Sterckx, Y.G.; Garcia- Pino, A.; Buts, L.; Vranken, W.F.; Bouckaert, J.; Roy, R.; Wyns, L.; van Nuland, N. A. Study of the structural and dynamic effects in the FimH adhesin upon alpha-d-heptyl mannose binding. J. Med. Chem., 2014, 57(4), 1416-27.
76. Le Trong, I.; Aprikian, P.; Kidd, B.A.; Forero-Shelton, M.; Tchesnokova, V.; Rajagopal, P.; Rodriguez, V.; Interlandi, G.; Klevit, R.; Vogel, V.; Stenkamp, R.E.; Sokurenko, E.V.; Thomas, W.E. Structural basis for mechanical force regulation of the adhesin FimH via finger trap-like beta sheet twisting. Cell, 2010, 141(4), 645-655.
77. Sauer, M.M.; Jakob, R.P.; Eras, J.; Baday, S.; Eris, D.; Navarra, G.; Berneche, S.; Ernst, B.; Maier, T.; Glockshuber, R. Catch-bond mechanism of the bacterial adhesin FimH. Nat. Commun., 2016, 7, 10738.
78. Pang, L.; Kleeb, S.; Lemme, K.; Rabbani, S.; Scharenberg, M.; Zalewski, A.; Schadler, F.; Schwardt, O.; Ernst, B. FimH antagonists: Structure-activity and structure-property relationships for biphenyl alpha-D-mannopyranosides. Chem. Med. Chem., 2012, 7(8), 1404-1422.
79. Kleeb, S.; Pang, L.; Mayer, K.; Eris, D.; Sigl, A.; Preston, R.C.; Zihlmann, P.; Sharpe, T.; Jakob, R.P.; Abgottspon, D.; Hutter, A.S.; Scharenberg, M.; Jiang, X.; Navarra, G.; Rabbani, S.; Smiesko, M.; Ludin, N.; Bezencon, J.; Schwardt, O.; Maier, T.; Ernst, B. FimH antagonists: Bioisosteres to improve the in vitro and in vivo PK/PD profile. J. Med. Chem., 2015, 58(5), 2221-2239.
80. Kleeb, S.; Jiang, X.; Frei, P.; Sigl, A.; Bezencon, J.; Bamberger, K.; Schwardt, O.; Ernst, B. FimH antagonists: Phosphate prodrugs improve oral bioavailability. J. Med. Chem., 2016, 59(7), 3163-3182.
81. Jarvis, C.; Han, Z.; Kalas, V.; Klein, R.; Pinkner, J. S.; Ford, B.; Binkley, J.; Cusumano, C. K.; Cusumano, Z.; Mydock-McGrane, L.; Hultgren, S. J.; Janetka, J.W. Antivirulence isoquinolone mannosides: Optimization of the biaryl aglycone for fimh lectin binding affinity and efficacy in the Treatment of Chronic UTI. Chem. Med. Chem., 2016, 11(4), 367-373.
82. Fiege, B.; Rabbani, S.; Preston, R.C.; Jakob, R.P.; Zihlmann, P.; Schwardt, O.; Jiang, X.; Maier, T.; Ernst, B. The tyrosine gate of the bacterial lectin FimH: A conformational analysis by NMR spectroscopy and X-ray crystallography. Chem. biochem., 2015, 16(8), 1235-1246.
83. Walz, A.; Odenbreit, S.; Mahdavi, J.; Boren, T.; Ruhl, S. Identification and characterization of binding properties of Helicobacter pylori by glycoconjugate arrays. Glycobiology, 2005, 15(7), 700-708.
84. Hage, N.; Howard, T.; Phillips, C.; Brassington, C.; Overman, R.; Debreczeni, J.; Gellert, P.; Stolnik, S.; Winkler, G.S.; Falcone, F.H. Structural basis of Lewis(b) antigen binding by the Helicobacter pylori adhesin BabA. Sci. Adv., 2015, 1(7), e1500315.
85. Moonens, K.; Gideonsson, P.; Subedi, S.; Bugaytsova, J.; Romao, E.; Mendez, M.; Norden, J.; Fallah, M.; Rakhimova, L.; Shevtsova, A.; Lahmann, M.; Castaldo, G.; Brannstrom, K.; Coppens, F.; Lo, A.W.; Ny, T.; Solnick, J.V.; Vandenbussche, G.; Oscarson, S.; Hammarstrom, L.; Arnqvist, A.; Berg, D.E.; Muyldermans, S.; Boren, T.; Remaut, H. Structural insights into polymorphic ABO glycan binding by Helicobacter pylori. Cell. Host. Microbe, 2016, 19(1), 55-66.
86. Hazes, B.; Sastry, P.A.; Hayakawa, K.; Read, R.J.; Irvin, R.T. Crystal structure of Pseudomonas aeruginosa PAK pilin suggests a main-chain-dominated mode of receptor binding. J. Mol. Biol., 2000, 299(4), 1005-1017.
87. Giraud, C.; Bernard, C.; Ruer, S.; De Bentzmann, S. Biological 'glue' and 'Velcro': Molecular tools for adhesion and biofilm formation in the hairy and gluey bug Pseudomonas aeruginosa. Environ. Microbiol. Rep., 2010, 2(3), 343-358.
88. Blanchard, B.; Nurisso, A.; Hollville, E.; Tetaud, C.; Wiels, J.; Pokorna, M.; Wimmerova, M.; Varrot, A.; Imberty, A. Structural basis of the preferential binding for globo-series glycosphingolipids displayed by Pseudomonas aeruginosa lectin I. J. Mol. Biol., 2008, 383(4), 837-853.
89. Kadam, R.U.; Bergmann, M.; Hurley, M.; Garg, D.; Cacciarini, M.; Swiderska, M.A.; Nativi, C.; Sattler, M.; Smyth, A.R.; Williams, P.; Camara, M.; Stocker, A.; Darbre, T.; Reymond, J.-L. A Glycopeptide Dendrimer Inhibitor of the Galactose-Specific Lectin LecA and of Pseudomonas aeruginosa Biofilms. Angew. Chem. Int. ed., 2011, 123(45), 10819-10823.
90. Kadam, R. U.; Garg, D.; Schwartz, J.; Visini, R.; Sattler, M.; Stocker, A.; Darbre, T.; Reymond, J.L. CH-π "T-Shape" interaction with histidine explains binding of aromatic galactosides to Pseudomonas aeruginosa lectin LecA. ACS Chem. Biol., 2013, 8(9), 1925-1930.
91. Reymond, J.L.; Bergmann, M.; Darbre, T. Glycopeptide dendrimers as Pseudomonas aeruginosa biofilm inhibitors. Chem. Soc. Rev., 2013, 42(11), 4814-4822.
92. Wittmann, V.; Pieters, R.J. Bridging lectin binding sites by multivalent carbohydrates. Chem. Soc. Rev., 2013, 42(10), 4492-4503.
93. Novoa, A.; Eierhoff, T.; Topin, J.; Varrot, A.; Barluenga, S.; Imberty, A.; Romer, W.; Winssinger, N. A LecA ligand identified from a galactoside-conjugate array inhibits host cell invasion by Pseudomonas aeruginosa. Angew. Chem. Int. Ed., 2014, 53(34), 8885-8889.
94. Visini, R.; Jin, X.; Bergmann, M.; Michaud, G.; Pertici, F.; Fu, O.; Pukin, A.; Branson, T.R.; Thies-Weesie, D.M.; Kemmink, J.; Gillon, E.; Imberty, A.; Stocker, A.; Darbre, T.; Pieters, R.J.; Reymond, J.L. Structural Insight into Multivalent Galactoside Binding to Pseudomonas aeruginosa Lectin LecA. ACS Chem. Biol., 2015, 10(11), 2455-2462.
95. Chabre, Y.M.; Giguere, D.; Blanchard, B.; Rodrigue, J.; Rocheleau, S.; Neault, M.; Rauthu, S.; Papadopoulos, A.; Arnold, A.A.; Imberty, A.; Roy, R. Combining glycomimetic and multivalent strategies toward designing potent bacterial lectin inhibitors. Chem. Eur. J. 2011, 17(23), 6545-6562.
96. Kadam, R.U.; Bergmann, M.; Garg, D.; Gabrieli, G.; Stocker, A.; Darbre, T.; Reymond, J. L. Structure-based optimization of the terminal tripeptide in glycopeptide dendrimer inhibitors of Pseudomonas aeruginosa biofilms targeting LecA. Chem. Eur. J., 2013, 19(50), 17054-17063.
97. Wang, S.; Dupin, L.; Noel, M.; Carroux, C.J.; Renaud, L.; Gehin, T.; Meyer, A.; Souteyrand, E.; Vasseur, J.J.; Vergoten, G.; Chevolot, Y.; Morvan, F.; Vidal, S. Toward the rational design of galactosylated glycoclusters that target Pseudomonas aeruginosa Lectin A (LecA): Influence of linker arms that lead to low-nanomolar multivalent Ligands. Chem. Eur. J., 2016, 22(33), 11785-11794.
98. Buffet, K.; Nierengarten, I.; Galanos, N.; Gillon, E.; Holler, M.; Imberty, A.; Matthews, S.E.; Vidal, S.; Vincent, S.P.; Nierengarten, J.F. Pillar[5]arene-based glycoclusters: Synthesis and multivalent binding to pathogenic bacterial lectins. Chem. Eur. J., 2016, 22(9), 2955-2963.
99. Bini, D.; Marchetti, R.; Russo, L.; Molinaro, A.; Silipo, A.; Cipolla, L. Multivalent ligand mimetics of LecA from P. aeruginosa: synthesis and NMR studies. Carbohydr. Res., 2016, 429, 23-28.
100. Perret, S.; Sabin, C.; Dumon, C.; Pokorna, M.; Gautier, C.; Galanina, O.; Ilia, S.; Bovin, N.; Nicaise, M.; Desmadril, M.; Gilboa-Garber, N.; Wimmerova, M.; Mitchell, E. P.; Imberty, A. Structural basis for the interaction between human milk oligosaccharides and the bacterial lectin PA-IIL of Pseudomonas aeruginosa. Biochem. J., 2005, 389(Pt 2), 325-332.
101. Marotte, K.; Sabin, C.; Preville, C.; Moume-Pymbock, M.; Wimmerova, M.; Mitchell, E.P.; Imberty, A.; Roy, R. X-ray structures and thermodynamics of the interaction of PA-IIL from Pseudomonas aeruginosa with disaccharide derivatives. Chem. Med. Chem., 2007, 2(9), 1328-1338.
102. Sommer, R.; Exner, T.E.; Titz, A. A biophysical study with carbohydrate derivatives explains the molecular basis of monosaccharide selectivity of the Pseudomonas aeruginosa lectin LecB. PLoS One, 2014, 9(11), e112822.
103. Hauck, D.; Joachim, I.; Frommeyer, B.; Varrot, A.; Philipp, B.; Moller, H.M.; Imberty, A.; Exner, T.E.; Titz, A. Discovery of two classes of potent glycomimetic inhibitors of Pseudomonas aeruginosa LecB with distinct binding modes. ACS Chem. Biol., 2013, 8(8), 1775-1784.
104. Sommer, R.; Hauck, D.; Varrot, A.; Wagner, S.; Audfray, A.; Prestel, A.; Moller, H.M.; Imberty, A.; Titz, A. Cinnamide derivatives of d-mannose as inhibitors of the bacterial virulence factor LecB from Pseudomonas aeruginosa. Chem. Open, 2015, 4(6), 756-767.
105. Reymond, J.L.; Darbre, T. Peptide and glycopeptide dendrimer apple trees as enzyme models and for biomedical applications. Org. Biomol. Chem., 2012, 10(8), 1483-1492.
106. Michaud, G.; Visini, R.; Bergmann, M.; Salerno, G.; Bosco, R.; Gillon, E.; Richichi, B.; Nativi, C.; Imberty, A.; Stocker, A.; Darbre, T.; Reymond, J.-L. Overcoming antibiotic resistance in Pseudomonas aeruginosa biofilms using glycopeptide dendrimers. Chem. Sci., 2016, 7(1), 166-182.
107. Sommer, R.; Wagner, S.; Varrot, A.; Nycholat, C.M.; Khaledi, A.; Haussler, S.; Paulson, J. C.; Imberty, A.; Titz, A. The virulence factor LecB varies in clinical isolates: consequences for ligand binding and drug discovery. Chemical Science, 2016, 7(8), 4990-5001.
108. Nishat, S.; Andreana, P.R. Entirely Carbohydrate-Based Vaccines: An emerging field for specific and selective immune responses. Vaccines (Basel), 2016, 4(2), 19.
109. Astronomo, R.D.; Burton, D.R. Carbohydrate vaccines: Developing sweet solutions to sticky situations? Nat. Rev. Drug. Discov., 2010, 9(4), 308-324.
110. Lepenies, B.; Yin, J.; Seeberger, P.H. Applications of synthetic carbohydrates to chemical biology. Curr. Opin. Chem. Biol., 2010, 14(3), 404-411.
111. Ganeshapillai, J.; Vinogradov, E.; Rousseau, J.; Weese, J. S.; Monteiro, M.A. Clostridium difficile cell-surface polysaccharides composed of pentaglycosyl and hexaglycosyl phosphate repeating units. Carbohydr. Res., 2008, 343(4), 703-710.
112. Broecker, F.; Hanske, J.; Martin, C. E.; Baek, J.Y.; Wahlbrink, A.; Wojcik, F.; Hartmann, L.; Rademacher, C.; Anish, C.; Seeberger, P.H. Multivalent display of minimal Clostridium difficile glycan epitopes mimics antigenic properties of larger glycans. Nat. Commun., 2016, 7, 11224.
113. Anish, C.; Guo, X.; Wahlbrink, A.; Seeberger, P. H. Plague detection by anti-carbohydrate antibodies. Angew. Chem. Int. Ed., 2013, 52(36), 9524-9528.
114. Broecker, F.; Aretz, J.; Yang, Y.; Hanske, J.; Guo, X.; Reinhardt, A.; Wahlbrink, A.; Rademacher, C.; Anish, C.; Seeberger, P.H. Epitope recognition of antibodies against a Yersinia pestis lipopolysaccharide trisaccharide component. ACS Chem. Biol., 2014, 9(4), 867-873.
115. Akira, S. Innate immunity and adjuvants. Philos. Trans. R. Soc. Lond. B. Biol. Sci., 2011, 366(1579), 2748-2755.
116. Hoving, J.C.; Wilson, G.J.; Brown, G.D. Signalling C-type lectin receptors, microbial recognition and immunity. Cell Microbiol., 2014, 16(2), 185-194.
117. Molinaro, A.; Holst, O.; Di Lorenzo, F.; Callaghan, M.; Nurisso, A.; D'Errico, G.; Zamyatina, A.; Peri, F.; Berisio, R.; Jerala, R.; Jiménez-Barbero, J.; Silipo, A.; Martín- Santamaría, S. Chemistry of Lipid A: At the Heart of Innate Immunity. Chem. Eur. J., 2015, 21(2), 500-519.
118. Mogensen, T.H. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin. Microbiol. Rev., 2009, 22(2), 240-273.
119. Medzhitov, R. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 2001, 1(2), 135-145.
120. Zanoni, I.; Ostuni, R.; Marek, L. R.; Barresi, S.; Barbalat, R.; Barton, G.M.; Granucci, F.; Kagan, J.C. CD14 controls the LPS-induced endocytosis of Toll-like receptor 4. Cell, 2011, 147(4), 868-880.
121. Park, B.S.; Lee, J.O. Recognition of lipopolysaccharide pattern by TLR4 complexes. Exp. Mol. Med., 2013, 45, e66.
122. Yang, J.; Qin, N.; Zhang, H.; Yang, R.; Xiang, B.; Wei, Q. Cellular uptake of exogenous calcineurin B is dependent on TLR4/MD2/CD14 complexes, and CnB is an endogenous ligand of TLR4. Sci. Rep., 2016, 6, 24346.
123. Mancini, R.J.; Stutts, L.; Ryu, K.A.; Tom, J.K.; Esser- Kahn, A.P. Directing the immune system with chemical compounds. ACS Chem. Biol., 2014, 9(5), 1075-1085.
124. Funda, D.P.; Tuckova, L.; Farre, M.A.; Iwase, T.; Moro, I.; Tlaskalova-Hogenova, H. CD14 is expressed and released as soluble CD14 by human intestinal epithelial cells in vitro: lipopolysaccharide activation of epithelial cells revisited. Infect. Immun., 2001, 69(6), 3772-3781.
125. Kim, J.I.; Lee, C.J.; Jin, M.S.; Lee, C.H.; Paik, S.G.; Lee, H.; Lee, J.O. Crystal structure of CD14 and its implications for lipopolysaccharide signaling. J. Biol. Chem., 2005, 280(12), 11347-11351.
126. Albright, S.; Chen, B.; Holbrook, K.; Jain, N. U. Solution NMR studies provide structural basis for endotoxin pattern recognition by the innate immune receptor CD14. Biochem. Biophys. Res. Commun., 2008, 368(2), 231-237.
127. Kelley, S.L.; Lukk, T.; Nair, S.K.; Tapping, R.I. The crystal structure of human soluble CD14 reveals a bent solenoid with a hydrophobic amino-terminal pocket. J. Immunol., 2013, 190(3), 1304-1311.
128. Ciaramelli, C.; Calabrese, V.; Sestito, S. E.; Perez-Regidor, L.; Klett, J.; Oblak, A.; Jerala, R.; Piazza, M.; Martin Santamaria, S.; Peri, F. Glycolipid-based TLR4 modulators and fluorescent probes: Rational design, synthesis, and biological properties. Chem. Biol. Drug. Des., 2016, 88(2), 217-229.
129. Kim, H. M.; Park, B. S.; Kim, J. I.; Kim, S. E.; Lee, J.; Oh, S. C.; Enkhbayar, P.; Matsushima, N.; Lee, H.; Yoo, O. J.; Lee, J. O. Crystal structure of the TLR4-MD-2 complex with bound endotoxin antagonist Eritoran. Cell, 2007, 130(5), 906-917.
130. Park, B.S.; Song, D.H.; Kim, H.M.; Choi, B.S.; Lee, H.; Lee, J.O. The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature, 2009, 458(7242), 1191-1195.
131. Ohto, U.; Fukase, K.; Miyake, K.; Satow, Y. Crystal structures of human MD-2 and its complex with antiendotoxic lipid IVa. Science, 2007, 316(5831), 1632-1634.
132. Scior, T.; Lozano-Aponte, J.; Figueroa-Vazquez, V.; Yunes-Rojas, J. A.; Zahringer, U.; Alexander, C. Threedimensional mapping of differential amino acids of human, murine, canine and equine TLR4/MD-2 receptor complexes conferring endotoxic activation by lipid A, antagonism by Eritoran and species-dependent activities of Lipid IVA in the mammalian LPS sensor system. Comput. Struct. Biotechnol. J., 2013, 7, e201305003.
133. Cighetti, R.; Ciaramelli, C.; Sestito, S.E.; Zanoni, I.; Kubik, L.; Arda-Freire, A.; Calabrese, V.; Granucci, F.; Jerala, R.; Martin-Santamaria, S.; Jimenez-Barbero, J.; Peri, F. Modulation of CD14 and TLR4.MD-2 activities by a synthetic lipid A mimetic. Chem. Bio. Chem., 2014, 15(2), 250-258.
134. Han, J.; Kim, H. J.; Lee, S.C.; Hong, S.; Park, K.; Jeon, Y. H.; Kim, D.; Cheong, H. K.; Kim, H. S. Structure-based rational design of a toll-like receptor 4 (TLR4) decoy receptor with high binding affinity for a target protein. PLoS One, 2012, 7(2), e30929.
135. Ohto, U.; Fukase, K.; Miyake, K.; Shimizu, T. Structural basis of species-specific endotoxin sensing by innate immune receptor TLR4/MD-2. Proc. Natl. Acad. Sci. USA, 2012, 109(19), 7421-7426.
136. Ohto, U.; Yamakawa, N.; Akashi-Takamura, S.; Miyake, K.; Shimizu, T. Structural analyses of human Toll-like receptor 4 polymorphisms D299G and T399I. J. Biol. Chem., 2012, 287(48), 40611-40617.
137. Wang, Y.; Su, L.; Morin, M. D.; Jones, B. T.; Whitby, L. R.; Surakattula, M. M.; Huang, H.; Shi, H.; Choi, J.H.; Wang, K.W.; Moresco, E.M.; Berger, M.; Zhan, X.; Zhang, H.; Boger, D.L.; Beutler, B. TLR4/MD-2 activation by a synthetic agonist with no similarity to LPS. Proc. Natl. Acad. Sci. USA, 2016, 113(7), e884-e893.
138. Paramo, T.; Piggot, T.J.; Bryant, C.E.; Bond, P.J. The structural basis for endotoxin-induced allosteric regulation of the Toll-like receptor 4 (TLR4) innate immune receptor. J. Biol. Chem., 2013, 288(51), 36215-36225.
139. Teghanemt, A.; Re, F.; Prohinar, P.; Widstrom, R.; Gioannini, T. L.; Weiss, J.P. Novel roles in human MD-2 of phenylalanines 121 and 126 and tyrosine 131 in activation of toll-like receptor 4 by endotoxin. J. Biol. Chem., 2008, 283(3), 1257-1266.
140. Yu, L.; Phillips, R.L.; Zhang, D.; Teghanemt, A.; Weiss, J.P.; Gioannini, T.L. NMR studies of hexaacylated endotoxin bound to wild-type and F126A mutant MD-2 and MD-2.TLR4 ectodomain complexes. J. Biol. Chem., 2012, 287(20), 16346-16355.
141. Vasl, J.; Oblak, A.; Peternelj, T. T.; Klett, J.; Martin- Santamaria, S.; Gioannini, T. L.; Weiss, J. P.; Jerala, R. Molecular basis of the functional differences between soluble human versus murine MD-2: Role of val135 in transfer of lipopolysaccharide from CD14 to MD-2. J. Immunol., 2016, 196(5), 2309-2318.
142. Valladeau, J.; Duvert-Frances, V.; Pin, J.J.; Dezutter- Dambuyant, C.; Vincent, C.; Massacrier, C.; Vincent, J.; Yoneda, K.; Banchereau, J.; Caux, C.; Davoust, J.; Saeland, S. The monoclonal antibody DCGM4 recognizes Langerin, a protein specific of Langerhans cells, and is rapidly internalized from the cell surface. Eur. J. Immunol., 1999, 29(9), 2695-2704.
143. Valladeau, J.; Ravel, O.; Dezutter-Dambuyant, C.; Moore, K.; Kleijmeer, M.; Liu, Y.; Duvert-Frances, V.; Vincent, C.; Schmitt, D.; Davoust, J.; Caux, C.; Lebecque, S.; Saeland, S. Langerin, a novel C-type lectin specific to Langerhans cells, is an endocytic receptor that induces the formation of Birbeck granules. Immunity, 2000, 12(1), 71-81.
144. Drickamer, K. C-type lectin-like domains. Curr. Opin. Struct. Biol., 1999, 9(5), 585-590.
145. de Jong, M.A.; Vriend, L.E.; Theelen, B.; Taylor, M.E.; Fluitsma, D.; Boekhout, T.; Geijtenbeek, T.B. C-type lectin Langerin is a beta-glucan receptor on human langerhans cells that recognizes opportunistic and pathogenic fungi. Mol. Immunol., 2010, 47(6), 1216-1225.
146. Hunger, R.E.; Sieling, P.A.; Ochoa, M. T.; Sugaya, M.; Burdick, A.E.; Rea, T.H.; Brennan, P.J.; Belisle, J.T.; Blauvelt, A.; Porcelli, S.A.; Modlin, R. L. Langerhans cells utilize CD1a and langerin to efficiently present nonpeptide antigens to T cells. J. Clin. Invest., 2004, 113(5), 701-708.
147. de Witte, L.; Nabatov, A.; Pion, M.; Fluitsma, D.; de Jong, M. A.; de Gruijl, T.; Piguet, V.; van Kooyk, Y.; Geijtenbeek, T. B. Langerin is a natural barrier to HIV-1 transmission by Langerhans cells. Nat. Med., 2007, 13(3), 367-371.
148. Thepaut, M.; Valladeau, J.; Nurisso, A.; Kahn, R.; Arnou, B.; Vives, C.; Saeland, S.; Ebel, C.; Monnier, C.; Dezutter- Dambuyant, C.; Imberty, A.; Fieschi, F. Structural studies of langerin and Birbeck granule: A macromolecular organization model. Biochemistry, 2009, 48(12), 2684-2698.
149. Sattin, S.; Bernardi, A. Glycoconjugates and glycomimetics as microbial anti-adhesives. Trends Biotechnol., 2016, 34(6), 483-495.
150. Drickamer, K. Engineering galactose-binding activity into a C-type mannose-binding protein. Nature, 1992, 360(6400), 183-186.
151. Stambach, N. S.; Taylor, M. E. Characterization of carbohydrate recognition by langerin, a C-type lectin of langerhans cells. Glycobiology, 2003, 13(5), 401-410.
152. Cambi, A.; Figdor, C. G. Levels of complexity in pathogen recognition by C-type lectins. Curr. Opin. Immunol., 2005, 17(4), 345-351.
153. 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(6), 4202-4209.
154. Feinberg, H.; Powlesland, A. S.; Taylor, M. E.; Weis, W. I. Trimeric structure of langerin. J. Biol. Chem., 2010, 285(17), 13285-13293.
155. Feinberg, H.; Taylor, M. E.; Razi, N.; McBride, R.; Knirel, Y. A.; Graham, S. A.; Drickamer, K.; Weis, W. I. Structural basis for langerin recognition of diverse pathogen and mammalian glycans through a single binding site. J. Mol. Biol., 2011, 405(4), 1027-1039.
156. Powlesland, A. S.; Fisch, T.; Taylor, M. E.; Smith, D. F.; Tissot, B.; Dell, A.; Pohlmann, S.; Drickamer, K. A novel mechanism for LSECtin binding to Ebola virus surface glycoprotein through truncated glycans. J. Biol. Chem., 2008, 283(1), 593-602.
157. Chatwell, L.; Holla, A.; Kaufer, B. B.; Skerra, A. The carbohydrate recognition domain of Langerin reveals high structural similarity with the one of DC-SIGN but an additional, calcium-independent sugar-binding site. Mol. Immunol., 2008, 45(7), 1981-1994.
158. Feinberg, H.; Rowntree, T. J.; Tan, S. L.; Drickamer, K.; Weis, W. I.; Taylor, M. E. Common polymorphisms in human langerin change specificity for glycan ligands. J. Biol. Chem., 2013, 288(52), 36762-36771.
159. Stowell, S. R.; Arthur, C. M.; Dias-Baruffi, M.; Rodrigues, L. C.; Gourdine, J. P.; Heimburg-Molinaro, J.; Ju, T.; Molinaro, R. J.; Rivera-Marrero, C.; Xia, B.; Smith, D. F.; Cummings, R. D. Innate immune lectins kill bacteria expressing blood group antigen. Nat. Med., 2010, 16(3), 295-301.
160. Somers, W. S.; Tang, J.; Shaw, G. D.; Camphausen, R. T. Insights into the molecular basis of leukocyte tethering and rolling revealed by structures of P- and E-selectin bound to SLe(X) and PSGL-1. Cell, 2000, 103(3), 467-79.
161. Guo, Y.; Feinberg, H.; Conroy, E.; Mitchell, D. A.; Alvarez, R.; Blixt, O.; Taylor, M. E.; Weis, W. I.; Drickamer, K. Structural basis for distinct ligand-binding and targeting properties of the receptors DC-SIGN and DC-SIGNR. Nat. Struct. Mol. Biol., 2004, 11(7), 591-598.
162. Munoz-Garcia, J. C.; Chabrol, E.; Vives, R. R.; Thomas, A.; de Paz, J. L.; Rojo, J.; Imberty, A.; Fieschi, F.; Nieto, P. M.; Angulo, J. Langerin-heparin interaction: two binding sites for small and large ligands as revealed by a combination of NMR spectroscopy and cross-linking mapping experiments. J. Am. Chem. Soc., 2015, 137(12), 4100-4110.
163. Zhao, J.; Liu, X.; Kao, C.; Zhang, E.; Li, Q.; Zhang, F.; Linhardt, R. J. Kinetic and Structural Studies of interactions between glycosaminoglycans and langerin. Biochemistry, 2016, 55(32), 4552-4559.
164. Hanske, J.; Aleksic, S.; Ballaschk, M.; Jurk, M.; Shanina, E.; Beerbaum, M.; Schmieder, P.; Keller, B. G.; Rademacher, C. Intradomain allosteric network modulates calcium affinity of the c-type lectin receptor langerin. J. Am. Chem. Soc., 2016, 138(37), 12176-12186.
165. Wamhoff, E. C.; Hanske, J.; Schnirch, L.; Aretz, J.; Grube, M.; Varon Silva, D.; Rademacher, C. (19)F NMR-guided design of glycomimetic langerin ligands. ACS Chem. Biol., 2016, 11(9), 2407-2413.
166. Stuart, D. I.; Subramaniam, S.; Abrescia, N. G. A. The democratization of cryo-EM. Nat. Methods, 2016, 13, 607-608.
167. Canales, A.; Mallagaray, A.; Berbis, M. A.; Navarro- Vazquez, A.; Dominguez, G.; Canada, F. J.; Andre, S.; Gabius, H. J.; Perez-Castells, J.; Jimenez-Barbero, J. Lanthanide- chelating carbohydrate conjugates are useful tools to characterize carbohydrate conformation in solution and sensitive sensors to detect carbohydrate-protein interactions. J. Am. Chem. Soc., 2014, 136(22), 8011-8017.
168. Canales, A.; Mallagaray, A.; Perez-Castells, J.; Boos, I.; Unverzagt, C.; Andre, S.; Gabius, H.-J.; Canada, F. J.; Jimenez-Barbero, J. Breaking pseudo-symmetry in multiantennary complex n-glycans using lanthanide-binding tags and nmr pseudo-contact shifts. Angew. Chem. Int. Ed. 2013, 52(51), 13789-13793.