Structural basis for selective recognition of endogenous and microbial polysaccharides by macrophage receptor SIGN-R1

Structure

Volumn 22, Issue 11, 2014, Pages 1595-1606

  Silva Martín, Noella ^a   Bartual, Sergio G ^a   Ramírez Aportela, Erney ^a   Chacón, Pablo ^a   Park, Chae Gyu ^b,c   Hermoso, Juan A ^a  

^a INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

^b ROCKEFELLER UNIVERSITY   (United States)

^c Yonsei University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE; DEXTRAN SULFATE; GLYCOPROTEIN; POLYSACCHARIDE; SIALIC ACID; SIGN R1 RECEPTOR; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; CELL SURFACE RECEPTOR; DC-SPECIFIC ICAM-3 GRABBING NONINTEGRIN; IMMUNOGLOBULIN FC FRAGMENT; LECTIN; N ACETYLNEURAMINIC ACID;

ARTICLE; BINDING SITE; CALCIUM BINDING; CRYSTAL STRUCTURE; HUMAN; MACROPHAGE; MICROORGANISM; NONHUMAN; STRUCTURE ANALYSIS; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CHO CELL LINE; CRICETULUS; METABOLISM; MOUSE; PROTEIN SECONDARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

ANIMALS; BINDING SITES; CELL ADHESION MOLECULES; CHO CELLS; CRICETULUS; CRYSTALLOGRAPHY, X-RAY; DEXTRAN SULFATE; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; LECTINS, C-TYPE; MICE; MODELS, MOLECULAR; N-ACETYLNEURAMINIC ACID; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, CELL SURFACE;

EID: 84908501531     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2014.09.001     Document Type: Article

References (56)

1. M. Abeyta, G.G. Hardy, and J. Yother Genetic alteration of capsule type but not PspA type affects accessibility of surface-bound complement and surface antigens of Streptococcus pneumoniae Infect. Immun. 71 2003 218 225
2. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, and R.W. Grosse-Kunstleve PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
3. R.M. Anthony, and J.V. Ravetch A novel role for the IgG Fc glycan: the anti-inflammatory activity of sialylated IgG Fcs J. Clin. Immunol. 30 Suppl 1 2010 S9 S14
4. R.M. Anthony, F. Wermeling, M.C.I. Karlsson, and J.V. Ravetch Identification of a receptor required for the anti-inflammatory activity of IVIG Proc. Natl. Acad. Sci. USA 105 2008 19571 19578
5. R.M. Anthony, T. Kobayashi, F. Wermeling, and J.V. Ravetch Intravenous gammaglobulin suppresses inflammation through a novel T(H)2 pathway Nature 475 2011 110 113
6. J.S. Brown, T. Hussell, S.M. Gilliland, D.W. Holden, J.C. Paton, M.R. Ehrenstein, M.J. Walport, and M. Botto The classical pathway is the dominant complement pathway required for innate immunity to Streptococcus pneumoniae infection in mice Proc. Natl. Acad. Sci. USA 99 2002 16969 16974
7. A.T. Brünger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, R.W. Grosse-Kunstleve, J.S. Jiang, J. Kuszewski, M. Nilges, and N.S. Pannu Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54 1998 905 921
8. I. Caminschi, A.J. Corbett, C. Zahra, M. Lahoud, K.M. Lucas, M. Sofi, D. Vremec, T. Gramberg, S. Pöhlmann, and J. Curtis Functional comparison of mouse CIRE/mouse DC-SIGN and human DC-SIGN Int. Immunol. 18 2006 741 753
9. CCP4 (Collaborative Computational Project, Number 4) The CCP4 suite: programs for protein crystallography Acta Crystallogr. D Biol. Crystallogr. 50 1994 760 763
10. J. Chehimi, Q. Luo, L. Azzoni, L. Shawver, N. Ngoubilly, R. June, G. Jerandi, M. Farabaugh, and L.J. Montaner HIV-1 transmission and cytokine-induced expression of DC-SIGN in human monocyte-derived macrophages J. Leukoc. Biol. 74 2003 757 763
11. C. Cheong, I. Matos, J.H. Choi, D.B. Dandamudi, E. Shrestha, M.P. Longhi, K.L. Jeffrey, R.M. Anthony, C. Kluger, and G. Nchinda Microbial stimulation fully differentiates monocytes to DC-SIGN/CD209(+) dendritic cells for immune T cell areas Cell 143 2010 416 429
12. J. Colino, and C.M. Snapper Dendritic cell-derived exosomes express a Streptococcus pneumoniae capsular polysaccharide type 14 cross-reactive antigen that induces protective immunoglobulin responses against pneumococcal infection in mice Infect. Immun. 75 2007 220 230
13. M. Crispin, X. Yu, and T.A. Bowden Crystal structure of sialylated IgG Fc: implications for the mechanism of intravenous immunoglobulin therapy Proc. Natl. Acad. Sci. USA 110 2013 E3544 E3546
14. B.M. Curtis, S. Scharnowske, and A.J. Watson Sequence and expression of a membrane-associated C-type lectin that exhibits CD4-independent binding of human immunodeficiency virus envelope glycoprotein gp120 Proc. Natl. Acad. Sci. USA 89 1992 8356 8360
15. T. Darden, D. York, and L. P Particle mesh Ewald. An N-log(N) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
16. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
17. H. Feinberg, R. Castelli, K. Drickamer, P.H. Seeberger, and W.I. Weis Multiple modes of binding enhance the affinity of DC-SIGN for high mannose N-linked glycans found on viral glycoproteins J. Biol. Chem. 282 2007 4202 4209
18. C. Gaboriaud, J. Juanhuix, A. Gruez, M. Lacroix, C. Darnault, D. Pignol, D. Verger, J.C. Fontecilla-Camps, and G.J. Arlaud The crystal structure of the globular head of complement protein C1q provides a basis for its versatile recognition properties J. Biol. Chem. 278 2003 46974 46982
19. C. Galustian, C.G. Park, W. Chai, M. Kiso, S.A. Bruening, Y.-S. Kang, R.M. Steinman, and T. Feizi 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
20. T.B. Geijtenbeek, R. Torensma, S.J. van Vliet, G.C. van Duijnhoven, G.J. Adema, Y. van Kooyk, and C.G. Figdor Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses Cell 100 2000 575 585
21. T.B. Geijtenbeek, P.C. Groot, M.A. Nolte, S.J. van Vliet, S.T. Gangaram-Panday, G.C. van Duijnhoven, G. Kraal, A.J. van Oosterhout, and Y. van Kooyk Marginal zone macrophages express a murine homologue of DC-SIGN that captures blood-borne antigens in vivo Blood 100 2002 2908 2916
22. S. Gordon Pattern recognition receptors: doubling up for the innate immune response Cell 111 2002 927 930
23. A. Granelli-Piperno, A. Pritsker, M. Pack, I. Shimeliovich, J.F. Arrighi, C.G. Park, C. Trumpfheller, V. Piguet, T.M. Moran, and R.M. Steinman Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin/CD209 is abundant on macrophages in the normal human lymph node and is not required for dendritic cell stimulation of the mixed leukocyte reaction J. Immunol. 175 2005 4265 4273
24. L.W. Guddat, J.N. Herron, and A.B. Edmundson Three-dimensional structure of a human immunoglobulin with a hinge deletion Proc. Natl. Acad. Sci. USA 90 1993 4271 4275
25. Y. Guo, H. Feinberg, E. Conroy, D.A. Mitchell, R. Alvarez, O. Blixt, M.E. Taylor, W.I. Weis, and K. Drickamer Structural basis for distinct ligand-binding and targeting properties of the receptors DC-SIGN and DC-SIGNR Nat. Struct. Mol. Biol. 11 2004 591 598
26. B. Hess, C. Kutzner, D. van der Spoel, and E. Lindahl GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 4 2008 435 447
27. V. Hornak, R. Abel, A. Okur, B. Strockbine, A. Roitberg, and C. Simmerling Comparison of multiple Amber force fields and development of improved protein backbone parameters Proteins 65 2006 712 725
28. W.L. Jorgensen, J. Chandrasekhar, J.D. Madura, R.D. Impey, and M.L. Klein Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 79 1993 926 935
29. Y. Kaneko, F. Nimmerjahn, and J.V. Ravetch Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation Science 313 2006 670 673
30. Y.-S. Kang, S. Yamazaki, T. Iyoda, M. Pack, S.A. Bruening, J.Y. Kim, K. Takahara, K. Inaba, R.M. Steinman, and C.G. Park 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
31. Y.-S. Kang, J.Y. Kim, S.A. Bruening, M. Pack, A. Charalambous, A. Pritsker, T.M. Moran, J.M. Loeffler, R.M. Steinman, and C.G. Park The C-type lectin SIGN-R1 mediates uptake of the capsular polysaccharide of Streptococcus pneumoniae in the marginal zone of mouse spleen Proc. Natl. Acad. Sci. USA 101 2004 215 220
32. Y.-S. Kang, Y. Do, H.-K. Lee, S.H. Park, C. Cheong, R.M. Lynch, J.M. Loeffler, R.M. Steinman, and C.G. Park A dominant complement fixation pathway for pneumococcal polysaccharides initiated by SIGN-R1 interacting with C1q Cell 125 2006 47 58
33. K.N. Kirschner, A.B. Yongye, S.M. Tschampel, J. González-Outeiriño, C.R. Daniels, B.L. Foley, and R.J. Woods GLYCAM06: a generalizable biomolecular force field. Carbohydrates J. Comput. Chem. 29 2008 622 655
34. J. Koesling, B. Lucas, L. Develioglou, T. Aebischer, and T.F. Meyer Vaccination of mice with live recombinant Salmonella typhimurium aroA against H. pylori: parameters associated with prophylactic and therapeutic vaccine efficacy Vaccine 20 2001 413 420
35. A. Lanoue, M.R. Clatworthy, P. Smith, S. Green, M.J. Townsend, H.E. Jolin, K.G.C. Smith, P.G. Fallon, and A.N.J. McKenzie SIGN-R1 contributes to protection against lethal pneumococcal infection in mice J. Exp. Med. 200 2004 1383 1393
36. R.A. Laskowski, D.S. Moss, and J.M. Thornton Main-chain bond lengths and bond angles in protein structures J. Mol. Biol. 231 1993 1049 1067
37. C.F. Macrae, I.J. Bruno, J.A. Chisholm, P.R. Edgington, P. McCabe, E. Pidcock, L. Rodriguez-Monge, R. Taylor, J. van de Streek, and P.A. Wood Mercury CSD 2.0 - new features for the visualization and investigation of crystal structures J. Appl. Cryst. 41 2008 466 470
38. F. Meyer-Wentrup, A. Cambi, G.J. Adema, and C.G. Figdor "Sweet talk": closing in on C type lectin signaling Immunity 22 2005 399 400
39. T. Mizuochi, K. Yonemasu, K. Yamashita, and A. Kobata The asparagine-linked sugar chains of subcomponent C1q of the first component of human complement J. Biol. Chem. 253 1978 7404 7409
40. D. Moras, A.D. Podjarny, and J.C. Thierry Crystallographic Computing 5: From Chemistry to Biology 1992 Oxford University Press Oxford, UK 39 50
41. K. Nagaoka, K. Takahara, K. Tanaka, H. Yoshida, R.M. Steinman, S. Saitoh, S. Akashi-Takamura, K. Miyake, Y.S. Kang, C.G. Park, and K. Inaba Association of SIGNR1 with TLR4-MD-2 enhances signal transduction by recognition of LPS in gram-negative bacteria Int. Immunol. 17 2005 827 836
42. K. Nagaoka, K. Takahara, K. Minamino, T. Takeda, Y. Yoshida, and K. Inaba Expression of C-type lectin, SIGNR3, on subsets of dendritic cells, macrophages, and monocytes J. Leukoc. Biol. 88 2010 913 924
43. C.G. Park, K. Takahara, E. Umemoto, Y. Yashima, K. Matsubara, Y. Matsuda, B.E. Clausen, K. Inaba, and R.M. Steinman Five mouse homologues of the human dendritic cell C-type lectin, DC-SIGN Int. Immunol. 13 2001 1283 1290
44. S.H. Park, C. Cheong, J. Idoyaga, J.Y. Kim, J.H. Choi, Y. Do, H. Lee, J.H. Jo, Y.S. Oh, and W. Im Generation and application of new rat monoclonal antibodies against synthetic FLAG and OLLAS tags for improved immunodetection J. Immunol. Methods 331 2008 27 38
45. A.S. Powlesland, E.M. Ward, S.K. Sadhu, Y. Guo, M.E. Taylor, and K. Drickamer Widely divergent biochemical properties of the complete set of mouse DC-SIGN-related proteins J. Biol. Chem. 281 2006 20440 20449
46. M.G. Prabagar, Y. Do, S. Ryu, J.Y. Park, H.J. Choi, W.S. Choi, T.J. Yun, J. Moon, I.S. Choi, and K. Ko SIGN-R1, a C-type lectin, enhances apoptotic cell clearance through the complement deposition pathway by interacting with C1q in the spleen Cell Death Differ. 20 2013 535 545
47. D.W. Ritchie, D. Kozakov, and S. Vajda Accelerating and focusing protein-protein docking correlations using multi-dimensional rotational FFT generating functions Bioinformatics 24 2008 1865 1873
48. A.W. Schüttelkopf, and D.M. van Aalten PRODRG: a tool for high-throughput crystallography of protein-ligand complexes Acta Crystallogr. D Biol. Crystallogr. 60 2004 1355 1363
49. N. Silva-Martin, J.D. Schauer, C.G. Park, and J.A. Hermoso Crystallization and preliminary X-ray diffraction studies of the carbohydrate-recognition domain of SIGN-R1, a receptor for microbial polysaccharides and sialylated antibody on splenic marginal zone macrophages Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 65 2009 1264 1266
50. P. Sondermann, A. Pincetic, J. Maamary, K. Lammens, and J.V. Ravetch General mechanism for modulating immunoglobulin effector function Proc. Natl. Acad. Sci. USA 110 2013 9868 9872
51. P. Sondermann, A. Pincetic, J. Maamary, K. Lammens, and J.V. Ravetch Reply to Crispin et al.: Molecular model that accounts for the biological and physical properties of sialylated Fc Proc. Natl. Acad. Sci. USA 110 2013 E3547
52. K. Takahara, Y. Yashima, Y. Omatsu, H. Yoshida, Y. Kimura, Y.S. Kang, R.M. Steinman, C.G. Park, and K. Inaba Functional comparison of the mouse DC-SIGN, SIGNR1, SIGNR3 and Langerin, C-type lectins Int. Immunol. 16 2004 819 829
53. S. Varchetta, P. Lusso, K. Hudspeth, J. Mikulak, D. Mele, S. Paolucci, R. Cimbro, M. Malnati, A. Riva, and R. Maserati Sialic acid-binding Ig-like lectin-7 interacts with HIV-1 gp120 and facilitates infection of CD4pos T cells and macrophages Retrovirology 10 2013 154
54. M.L. Verdonk, J.C. Cole, M.J. Hartshorn, C.W. Murray, and R.D. Taylor Improved protein-ligand docking using GOLD Proteins 52 2003 609 623
55. C. Weidenmaier, and A. Peschel Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions Nat. Rev. Microbiol. 6 2008 276 287
56. A.N. Zelensky, and J.E. Gready Comparative analysis of structural properties of the C-type-lectin-like domain (CTLD) Proteins 52 2003 466 477