Characterisation of the Dynamic Interactions between Complex N-Glycans and Human CD22.
N-glycans
NMR spectroscopy
Siglecs
molecular recognition
sialic acids
Journal
Chembiochem : a European journal of chemical biology
ISSN: 1439-7633
Titre abrégé: Chembiochem
Pays: Germany
ID NLM: 100937360
Informations de publication
Date de publication:
15 01 2020
15 01 2020
Historique:
received:
06
05
2019
pubmed:
17
5
2019
medline:
6
1
2021
entrez:
17
5
2019
Statut:
ppublish
Résumé
CD22 (Siglec-2) is a B-cell surface inhibitory protein capable of selectively recognising sialylated glycans, thus dampening autoimmune responses against self-antigens. Here we have characterised the dynamic recognition of complex-type N-glycans by human CD22 by means of orthogonal approaches including NMR spectroscopy, computational methods and biophysical assays. We provide new molecular insights into the binding mode of sialoglycans in complex with h-CD22, highlighting the role of the sialic acid galactose moieties in the recognition process, elucidating the conformational behaviour of complex-type N-glycans bound to Siglec-2 and dissecting the formation of CD22 homo-oligomers on the B-cell surface. Our results could enable the development of additional therapeutics capable of modulating the activity of h-CD22 in autoimmune diseases and malignancies derived from B-cells.
Identifiants
pubmed: 31095840
doi: 10.1002/cbic.201900295
doi:
Substances chimiques
CD22 protein, human
0
Polysaccharides
0
Sialic Acid Binding Ig-like Lectin 2
0
Galactose
X2RN3Q8DNE
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
129-140Informations de copyright
© 2019 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim.
Références
M. S. Macauley, P. R. Crocker, J. C. Paulson, Nat. Rev. Immunol. 2014, 14, 653-666.
P. R. Crocker, J. C. Paulson, A. Varki, Nat. Rev. Immunol. 2007, 7, 255-266.
O. M. T. Pearce, H. Läubli, Glycobiology 2016, 26, 111-128.
J. C. Paulson, M. S. Macauley, N. Kawasaki, Ann. N. Y. Acad. Sci. 2012, 1253, 37-48.
A. Varki in Essential Glycobiology, Vol. 2 (Eds.: A. Varki, R. D. Cummings, J. D. Esko, H. H. Freeze, P. Stanley, C. R. Bertozzi, G. W. Hart, M. E. Etzler), Cold Spring Harbor Laboratory Press, New York, 2009, Chapter 14.
S. von Gunten, B. S. Bochner, Ann. N. Y. Acad. Sci. 2008, 1143, 61-82.
P. R. Crocker, E. A. Clark, M. Filbin, S. Gordon, Y. Jones, J. H. Kehrl, S. Kelm, Nicole Le Douarin, L. Powell, J. Roder, R. L. Schnaar, D. C. Sgroi, I. Stamenkovic, R. Schauer, M. Schachner, T. K. van den Berg, P. A. van der Merwe, S. M. Watt, A. Varki, Glycobiology 1998, 8, V.
S. Kelm, R. Schauer, J. C. Manuguerra, H. J. Gross, P. R. Crocker, Glycoconjugate J. 1994, 11, 576-585.
P. R. Crocker, P. Redelinghuys, Biochem. Soc. Trans. 2008, 36, 1467-1471.
J. Lübbers, E. Rodríguez, Y. van Kooyk, Front. Immunol. 2018, 8, 2807.
B. S. Bochner, N. Zimmermann, J. Allergy Clin. Immunol. 2015, 135, 598-608.
Q. Wang, Y. Matsuo, A. R. Pradipta, N. Inohara, Y. Fujimoto, K. Fukase, Org. Biomol. Chem. 2016, 14, 1013-1023.
M. Vinson, P. A. van der Merwe, S. Kelm, A. May, E. Y. Jones, P. R. Crocker, J. Biol. Chem. 1996, 271, 9267-9272.
S. Mahajan Vinay, S. Pillai, Immunol. Rev. 2016, 269, 145-161.
J. Müller, L. Nitschke, Nat Rev Rheumatol. 2014, 10, 422-428.
J. C. Poe, T. F. Tedder, Trends Immunol. 2012, 33, 413-420.
S. Han, B. E. Collins, P. Bengtson, J. C. Paulson, Nat. Chem. Biol. 2005, 1, 93-97.
R. J. Cornall, J. G. Cyster, M. L. Hibbs, A. R. Dunn, K. L. Otipoby, E. A. Clark, C. C. Goodnow, Immunity 1998, 8, 497-508.
N. Kimura, K. Ohmori, K. Miyazaki, M. Izawa, Y. Matsuzaki, Y. Yasuda, H. Takematsu, Y. Kozutsumi, A. Moriyama, R. Kannagi, J. Biol. Chem. 2007, 282, 32200-32207.
C. Büll, T. Heise, G. J. Adema, T. J. Boltje, Trends Biochem. Sci. 2016, 41, 519-531.
H. Prescher, A. Schweizer, E. Kuhfeldt, L. Nitschke, R. Brossmer, ChemBioChem 2017, 18, 1216-1225.
W. Peng, J. C. Paulson, J. Am. Chem. Soc. 2017, 139, 12450-12458.
P. D. Madge, A. Maggioni, M. Pascolutti, M. Amin, M. Waespy, B. Bellette, R. J. Thomson, S. Kelm, M. von Itzstein, T. Haselhorst, Sci. Rep. 2016, 6, 36012.
M. S. Macauley, F. Pfrengle, C. Rademacher, C. M. Nycholat, A. J. Gale, A. von Drygalski, J. C. Paulson, J. Clin. Invest. 2013, 123, 3074-3083.
C. D. Rillahan, M. S. Macauley, E. Schwartz, Y. He, R. McBride, B. M. Arlian, J. Rangarajan, V. V. Fokin, J. C. Paulson, Chem. Sci. 2014, 5, 2398-2406.
S. Mesch, K. Lemme, M. Wittwer, H. Koliwer-Brandl, O. Schwardt, S. Kelm, B. Ernst, ChemMedChem 2012, 7, 134-143.
L. Sullivan-Chang, R. T. O'Donnell, J. M. Tuscano, BioDrugs 2013, 27, 293-304.
B. Meyer, T. Peters, Angew. Chem. Int. Ed. 2003, 42, 864-890;
Angew. Chem. 2003, 115, 890-918.
R. Marchetti, S. Perez, A. Arda, A. Imberty, J. Jimenez-Barbero, A. Silipo, A. Molinaro, ChemistryOpen 2016, 5, 274-296.
M. Mayer, B. Meyer, Angew. Chem. Int. Ed. 1999, 38, 1784-1788;
Angew. Chem. 1999, 111, 1902-1906.
J. Yan, A. D. Kline, H. Mo, M. J. Shapiro, E. R. Zartler, J. Magn. Reson. 2003, 163, 270-276.
M. Mayer, L. T. James, J. Am. Chem. Soc. 2004, 126, 4453-4460.
J. Angulo, P. M. Nieto, Eur. Biophys. J. 2011, 40, 1357-1369.
A. Chandrasekaran, A. Srinivasan, R. Raman, K. Viswanathan, S. Raguram, T. M. Tumpey, R. Sasisekharan, Nat. Biotechnol. 2008, 26, 107-113.
L. Poppe, R. Struike-Prill, B. Meyer, van Halbeek, J. Biomol. NMR 1992, 2, 109-136.
D. S. Patel, R. Pendrill, S. S. Mallajosyula, G. Widmalm, A. D. MacKerell, J. Phys. Chem. B 2014, 118, 2851-2871.
D. Xu, E. I. Newhouse, R. E. Amaro, H. C. Pao, L. S. Cheng, P. R. Markwick, J. A. McCammon, W. W. Li, P. W. Arzberger, J. Mol. Biol. 2009, 387, 465-491.
J. Ereño-Orbea, T. Sicard, H. Cui, M. T. Mazhab-Jafari, S. Benlekbir, A. Guarné, J. L. Rubinstein, J.-P. Julien, Nat. Commun. 2017, 8, 764.
G. M. Morris, G. M. Morris, R. Huey, W. Lindstrom, M. F. Sanner, R. K. Belew, D. S. Goodsell, A. J. Olson, J. Comput. Chem. 2009, 30, 2785-2791.
J. Ereño-Orbea, T. Sicard, H. Cui, M. T. Mazhab-Jafari, S. Benlekbir, A. Guarné, J. L. Rubinstein, J. P. Julien, Nat. Commun. 2017, 8, 764.
V. Jayalakshmi, N. R. Krishna, J. Magn. Reson. 2002, 155, 106-118.
A. Guillot, M. Dauchez, N. Belloy, J. Jonquet, L. Duca, B. Romier, P. Maurice, L. Debelle, L. Martiny, V. Durlach, S. Baud, S. Blaise, Sci. Rep. 2016, 6, 35666.
S. Jo, Y. Qi, W. Im, Glycobiology 2016, 26, 19-29.
W. Nishima, N. Miyashita, Y. Yamaguchi, Y. Sugita, S. Re, J. Phys. Chem. B 2012, 116, 8504-8512.
Y. Qi, S. Jo, W. Im, Glycobiology 2016, 26, 251-260.
B. Fernández de Toro, W. Peng, A. J. Thompson, G. Domínguez, F. J. Cañada, J. Pérez-Castells, J. C. Paulson, J. Jiménez-Barbero, Á. Canales, Angew. Chem. Int. Ed. 2018, 57, 15051-15055; Angew. Chem. 2018, 130, 15271-15275.
T. Angata, C. M. Nycholat, M. S. Macauley, Trends Pharmacol. Sci. 2015, 36, 645-660.
L. A. Abriata, M. Dal Peraro, Sci. Rep. 2015, 5, 10549.
J. M. Pröpster, F. Yang, S. Rabbani, B. Ernst, F. H.-T. Allaina, M. Schubert, Proc. Natl. Acad. Sci. USA 2016, 113, E4170-E4179.
A. Gimeno, N.-C. Reichardt, F. J. Canada, L. Perkams, C. Unverzagt, J. J. Barbero, A. Arda, ACS Chem. Biol. 2017, 12, 1104-1112.
D. J. States, R. A. Haberkorn, D. A. Ruben, J. Magn. Reson. 1982, 48, 286-292.
V. Jayalakshmi, N. R. Krishna, J. Magn. Reson. 2004, 168, 36-45.
X. Wen, Y. Yuan, D. A. Kuntz, D. R. Rose, B. M. Pinto, Biochemistry 2005, 44, 6729-6737.
A. Bhunia, V. Jayalakshmi, A. J. Benie, O. Schuster, S. Kelm, N. R. Krishna, T. Peters, Carbohydr. Res. 2004, 339, 259-267.
Schrödinger Release 2017-1: MS Jaguar, Schrödinger, LLC, New York, NY, 2017.
J. C. Shelley, A. Cholleti, L. L. Frye, J. R. Greenwood, M. R. Timlin, M. Uchimaya, J. Comput.-Aided Mol. Des. 2007, 21, 681-691.
E. Harder, W. Damm, J. Maple, C. Wu, M. Reboul, J. Y. Xiang, L. Wang, D. Lupyan, M. K. Dahlgren, J. L. Knight, J. W. Kaus, D. S. Cerutti, G. Krilov, W. L. Jorgensen, R. Abel, R. A. Friesner, J. Chem. Theory Comput. 2016, 12, 281-296.
Glycam Carbohydrate Builder. Available at www.glycam.org.
K. N. Kirschner, A. B. Yongye, S. M. Tschampel, J. González-Outeiriño, C. R. Daniels, B. L. Foley, R. J. Woods, J. Comput. Chem. 2008, 29, 622-655.
B. R. Brooks, C. L. Brooks, A. D. MacKerell, L. Nilsson, R. J. Petrella, B. Roux, Y. Won, G. Archontis, C. Bartels, S. Boresch, A. Caflisch, L. Caves, Q. Cui, A. R. Dinner, M. Feig, S. Fischer, J. Gao, M. Hodoscek, W. Im, K. Kuczera, T. Lazaridis, J. Ma, V. Ovchinnikov, E. Paci, R. W. Pastor, C. B. Post, J. Z. Pu, M. Schaefer, B. Tidor, R. M. Venable, H. L. Woodcock, X. Wu, W. Yang, D. M. York, M. Karplus, J. Comput. Chem. 2009, 30, 1545-1614.
J. A. Maier, C. Martinez, K. Kasavajhala, L. Wickstrom, K. E. Hauser, C. Simmerling, J. Chem. Theory Comput. 2015, 11, 3696-3713.
D. A. Case, V. Babin, J. Berryman, R. M. Betz, Q. Cai, D. S. Cerutti, T. E. Cheatham III, T. A. Darden, R. E. Duke, H. Gohlke, A. W. Goetz, S Gusarov, N. Homeyer, P. Janowski, J. Kaus, I. Kolossváry, A. Kovalenko, T. S. Lee, S. LeGrand, T. Luchko, R. Luo, B. Madej, K. M. Merz, F. Paesani, D. R. Roe, A. Roitberg, C. Sagui, R. Salomon-Ferrer, G. Seabra, C. L. Simmerling, W. Smith, J. Swails, R. C. Walker, J. Wang, R. M. Wolf, X. Wu, P. A. Kollman, AMBER14, University of California, San Francisco, 2014.
J.-P. Ryckaert, G. Ciccotti, H. J. C. Berendsen, J. Comput. Phys. 1977, 23, 327-341.
T. Darden, D. York, L. Pedersen, J. Chem. Phys. 1993, 98, 10089-10092.
W. Humphrey, A. Dalke, K. Schulten, J. Mol. Graphics 1996, 14, 33-38.
A. Bohne-Lang, C. W. von der Lieth, Nucleic Acids Res. 2005, 33, Web Server issue W214-9.
Y. Kajihara, Y. Suzuki, N. Yamamoto, K. Sasaki, T. Sakakibara, L. R. Juneja, Chem. Eur. J. 2004, 10, 971-985.
M. Nagasaki, Y. Manabe, N. Minamoto, K. Tanaka, A. Silipo, A. Molinaro, K. J. Fukase, Org. Chem. 2016, 81, 10600-10616.