Bacterial polysaccharide specificity of the pattern recognition receptor langerin is highly species-dependent

Journal of Biological Chemistry

Volumn 292, Issue 3, 2017, Pages 862-871

  Hanske, Jonas ^a,b   Schulze, Jessica ^a,b   Aretz, Jonas ^a,b   McBride, Ryan ^c   Loll, Bernhard ^b   Schmidt, Henrik ^a,b   Knirel, Yuriy ^d   Rabsch, Wolfgang ^e   Wahl, Markus C ^b   Paulson, James C ^c   Rademacher, Christoph ^a,b  

^a MAX PLANCK INSTITUTE OF COLLOIDS AND INTERFACES   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d N D ZELINSKY INSTITUTE OF ORGANIC CHEMISTRY   (Russian Federation)

^e ROBERT KOCH INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LIGANDS; POLYSACCHARIDES; PROTEINS;

ANTIGEN PROCESSING; BACTERIAL POLYSACCHARIDES; EVOLUTIONARY CONSERVATIONS; HOST-PATHOGEN INTERACTIONS; LIGAND SPECIFICITY; PATTERN RECOGNITION RECEPTORS; STRUCTURAL INSIGHTS; THREE-DIMENSIONAL STRUCTURE;

PATTERN RECOGNITION;

BACTERIAL POLYSACCHARIDE; LANGERIN; CD207 PROTEIN, HUMAN; CD207 PROTEIN, MOUSE; LECTIN; LEUKOCYTE ANTIGEN; MANNOSE BINDING LECTIN; MEMBRANE ANTIGEN; PATTERN RECOGNITION RECEPTOR;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; ISOTHERMAL TITRATION CALORIMETRY; LIGAND BINDING; MOLECULAR CLONING; MOLECULAR EVOLUTION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; ANIMAL; CHEMISTRY; HUMAN; MOUSE; PROTEIN DOMAIN; SPECIES DIFFERENCE; X RAY CRYSTALLOGRAPHY;

ANIMALS; ANTIGENS, CD; ANTIGENS, SURFACE; CRYSTALLOGRAPHY, X-RAY; HUMANS; LECTINS, C-TYPE; MANNOSE-BINDING LECTINS; MICE; POLYSACCHARIDES, BACTERIAL; PROTEIN DOMAINS; RECEPTORS, PATTERN RECOGNITION; SPECIES SPECIFICITY;

EID: 85010333012     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.751750     Document Type: Article

References (44)

1. Gagneux, P., and Varki, A. (1999) Evolutionary considerations in relating oligosaccharide diversity to biological function. Glycobiology 9, 747-755
2. Varki, A. (2006) Nothing in glycobiology makes sense, except in the light of evolution. Cell 126, 841-845
3. Lebeer, S., Vanderleyden, J., and De Keersmaecker, S. C. (2010) Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat. Rev. Microbiol. 8, 171-184
4. Akira, S., Uematsu, S., and Takeuchi, O. (2006) Pathogen recognition and innate immunity. Cell 124, 783-801
5. Drickamer, K. (1995) Increasing diversity of animal lectin structures. Curr. Opin. Struct. Biol. 5, 612-616
6. Van Kooyk, Y., and Rabinovich, G. A. (2008) Protein-glycan interactions in the control of innate and adaptive immune responses. Nat. Immunol. 9, 593-601
7. Aretz, J., Wamhoff, E.-C., Hanske, J., Heymann, D., and Rademacher, C. (2014) Computational and experimental prediction of human C-type lectin receptor druggability. Front. Immunol. 5, 323
8. Drickamer, K., and Taylor, M. E. (2015) Recent insights into structures and functions of C-type lectins in the immune system. Curr. Opin. Struct. Biol. 34, 26-34
9. Zelensky, A. N., and Gready, J. E. (2005) The C-type lectin-like domain superfamily. FEBS J. 272, 6179-6217
10. Collins, B. E., and Paulson, J. C. (2004) Cell surface biology mediated by low affinity multivalent protein-glycan interactions. Curr. Opin. Chem. Biol. 8, 617-625
11. Geijtenbeek, T. B., and Gringhuis, S. I. (2009) Signalling through C-type lectin receptors: shaping immune responses. Nat. Rev. Immunol. 9, 465-479
12. Roach, J. C., Glusman, G., Rowen, L., Kaur, A., Purcell, M. K., Smith, K. D., Hood, L. E., and Aderem, A. (2005) The evolution of vertebrate Toll-like receptors. Proc. Natl. Acad. Sci. U. S. A. 102, 9577-9582
13. Garcia-Vallejo, J. J., and Van Kooyk, Y. (2013) The physiological role of DC-SIGN: a tale of mice and men. Trends Immunol. 34, 482-486
14. De Witte, L., Nabatov, A., Pion, M., Fluitsma, D., De Jong, M. A. W. P., De Gruijl, T., Piguet, V., Van Kooyk, Y., and Geijtenbeek, T. B. H. (2007) Langerin is a natural barrier to HIV-1 transmission by Langerhans cells. Nat. Med. 13, 367-371
15. Van Der Vlist, M., De Witte, L., De Vries, R. D., Litjens, M., De Jong, M. A., Fluitsma, D., De Swart, R. L., and Geijtenbeek, T. B. (2011) Human Langerhans cells capture measles virus through Langerin and present viral antigens to CD4α T cells but are incapable of cross-presentation. Eur. J. Immunol. 41, 2619-2631
16. De Jong, M. A. W. P., Vriend, L. E. M., Theelen, B., Taylor, M. E., Fluitsma, D., Boekhout, T., and Geijtenbeek, T. B. H. (2010) C-type lectin Langerin is a β-glucan receptor on human Langerhans cells that recognizes opportunistic and pathogenic fungi. Mol. Immunol. 47, 1216-1225
17. 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., and Modlin, R. L. (2004) Langerhans cells utilize CD1a and langerin to efficiently present nonpeptide antigens to T cells. J. Clin. Invest. 113, 701-708
18. Hsu, T.-L., Cheng, S.-C., Yang, W.-B., Chin, S.-W., Chen, B.-H., Huang, M.-T., Hsieh, S.-L., and Wong, C.-H. (2009) Profiling carbohydrate-receptor interaction with recombinant innate immunity receptor-Fc fusion proteins. J. Biol. Chem. 284, 34479-34489
19. Chabrol, E., Nurisso, A., Daina, A., Vassal-Stermann, E., Thepaut, M., Girard, E., Vivès, R. R., and Fieschi, F. (2012) Glycosaminoglycans are interactants of langerin: comparison with gp120 highlights an unexpected calcium-independent binding mode. PLoS One 7, e50722
20. Van Den Berg, L. M., Cardinaud, S., Van Der Aar, A. M., Sprokholt, J. K., De Jong, M. A., Zijlstra-Willems, E. M., Moris, A., and Geijtenbeek, T. B. (2015) Langerhans cell-dendritic cell cross-talk via langerin and hyaluronic acid mediates antigen transfer and cross-presentation of HIV-1. J. Immunol. 195, 1763-1773
21. Thépaut, M., Valladeau, J., Nurisso, A., Kahn, R., Arnou, B., Vivès, C., Saeland, S., Ebel, C., Monnier, C., Dezutter-Dambuyant, C., Imberty, A., and Fieschi, F. (2009) Structural studies of langerin and birbeck granule: a macromolecular organization model. Biochemistry 48, 2684-2698
22. Stambach, N. S., and Taylor, M. E. (2003) Characterization of carbohydrate recognition by langerin, a C-type lectin of Langerhans cells. Glycobiology 13, 401-410
23. Feinberg, H., Taylor, M. E., Razi, N., McBride, R., Knirel, Y. A., Graham, S. A., Drickamer, K., and Weis, W. I. (2011) Structural basis for langerin recognition of diverse pathogen and mammalian glycans through a single binding site. J. Mol. Biol. 405, 1027-1039
24. Tateno, H., Ohnishi, K., Yabe, R., Hayatsu, N., Sato, T., Takeya, M., Narimatsu, H., and Hirabayashi, J. (2010) Dual specificity of Langerin to sulfated and mannosylated glycans via a single C-type carbohydrate recognition domain. J. Biol. Chem. 285, 6390-6400
25. Feinberg, H., Rowntree, T. J. W., Tan, S. L. W., Drickamer, K., Weis, W. I., and Taylor, M. E. (2013) Common polymorphisms in human langerin change specificity for glycan ligands. J. Biol. Chem. 288, 36762-36771
26. Valladeau, J., Clair-Moninot, V., Dezutter-Dambuyant, C., Pin, J.-J., Kissenpfennig, A., Mattéi, M.-G., Ait-Yahia, S., Bates, E. E. M., Malissen, B., Koch, F., Fossiez, F., Romani, N., Lebecque, S., and Saeland, S. (2002) Identification of mouse langerin/CD207 in Langerhans cells and some dendritic cells of lymphoid tissues. J. Immunol. 168, 782-792
27. Galustian, C., Park, C. G., Chai, W., Kiso, M., Bruening, S. A., Kang, Y. S., Steinman, R. M., and Feizi, T. (2004) 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, 853-866
28. Drickamer, K. (1992) Engineering galactose-binding activity into a C-type mannose-binding protein. Nature 360, 183-186
29. Feinberg, H., Powlesland, A. S., Taylor, M. E., and Weis, W. I. (2010) Trimeric structure of langerin. J. Biol. Chem. 285, 13285-13293
30. Muñoz-García, J. C., Chabrol, E., Vivès, R. R., Thomas, A., De Paz, J. L., Rojo, J., Imberty, A., Fieschi, F., Nieto, P. M., and Angulo, J. (2015) Langerinheparin 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. 137, 4100-4110
31. Stowell, S. R., Arthur, C. M., McBride, R., Berger, O., Razi, N., Heimburg-Molinaro, J., Rodrigues, L. C., Gourdine, J. P., Noll, A. J., Von Gunten, S., Smith, D. F., Knirel, Y. A., Paulson, J. C., and Cummings, R. D. (2014) Microbial glycan microarrays define key features of host-microbial interactions. Nat. Chem. Biol. 10, 470-476
32. Guo, Y., Feinberg, H., Conroy, E., Mitchell, D. A., Alvarez, R., Blixt, O., Taylor, M. E., Weis, W. I., and Drickamer, K. (2004) Structural basis for distinct ligand-binding and targeting properties of the receptors DCSIGN and DC-SIGNR. Nat. Struct. Mol. Biol. 11, 591-598
33. Horan, N., Yan, L., Isobe, H., Whitesides, G. M., and Kahne, D. (1999) Nonstatistical binding of a protein to clustered carbohydrates. Proc. Natl. Acad. Sci. U. S. A. 96, 11782-11786
34. Forni, D., Cagliani, R., Tresoldi, C., Pozzoli, U., De Gioia, L., Filippi, G., Riva, S., Menozzi, G., Colleoni, M., Biasin, M., Lo Caputo, S., Mazzotta, F., Comi, G. P., Bresolin, N., Clerici, M., and Sironi, M. (2014) An evolutionary analysis of antigen processing and presentation across different timescales reveals pervasive selection. PLoS Genet. 10, e1004189
35. Mayer, M., and James, T. L. (2004) NMR-based characterization of phenothiazines as a RNA binding scaffold. J. Am. Chem. Soc. 126, 4453-4460
36. Kabsch, W. (2010) XDS. Acta Crystallogr. D 66, 125-132
37. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L.-W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc-Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221
38. Evans, P. R. (2011) An introduction to data reduction: space-group determination, scaling and intensity statistics. Acta Crystallogr. D 67, 282-292
39. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
40. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D 66, 486-501
41. Chen, V. B., Arendall W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12-21
42. Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Söding, J., Thompson, J. D., and Higgins, D. G. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal ω. Mol. Syst. Biol. 7, 539
43. Valdar, W. S. (2002) Scoring residue conservation. Proteins 48, 227-241
44. Meier, M., Bider, M. D., Malashkevich, V. N., Spiess, M., and Burkhard, P. (2000) Crystal structure of the carbohydrate recognition domain of the H1 subunit of the asialoglycoprotein receptor. J. Mol. Biol. 300, 857-865