Communication
different linkage types, allowing strategic flexibility. One
example of the usefulness of this new methodology could
be in the ready creation and then comparison of glyco-
conjugates as vaccines, where some linkages, but not
Chem. Commun. 2011, 47, 1698–1700; c) C. D. Spicer, T.
Triemer, B. G. Davis, J. Am. Chem. Soc. 2012, 134, 800–803.
9] G. J. L. Bernardes, L. Linderoth, K. J. Doores, O. Boutur-
eira, B. G. Davis, ChemBioChem 2011, 12, 1383–1386.
[
[
10] Y. A. Lin, J. M. Chalker, N. Floyd, G. J. L. Bernardes, B. G.
[
25]
others, may generate so-called ꢀanti-linkerꢁ responses.
Davis, J. Am. Chem. Soc. 2008, 130, 9642–9643.
The ability to take, for example, the same glycan immu-
nogen from a pathogen and rapidly create similar copy
numbers for protein loading but differing linkage types,
as we have shown here, may be highly advantageous in
[11] a) O. Boutureira, G. J. Bernardes, F. DꢁHooge, B. G. Davis,
Chem. Commun. 2011, 47, 10010–10012; b) O. Boutureira,
F. DꢁHooge, M. Fernandez-Gonzalez, G. J. Bernardes, M.
Sanchez-Navarro, J. R. Koeppe, B. G. Davis, Chem.
Commun. 2010, 46, 8142–8144.
[26]
the study of synthetic glycoconjugates as vaccines.
[
12] a) C. D. Spicer, B. G. Davis, Chem. Commun. 2013, 49,
2
747–2749; b) M. Yang, J. Li, P. R. Chen, Chem. Soc. Rev.
2
014, 43, 6511–6526.
Acknowledgements
[
13] M. A. Robinson, S. T. Charlton, P. Garnier, X. T. Wang, S. S.
Davis, A. C. Perkins, M. Frier, R. Duncan, T. J. Savage,
D. A. Wyatt, S. A. Watson, B. G. Davis, Proc. Natl. Acad.
Sci. U.S.A. 2004, 101, 14527–14532.
We would like to thank the EU FP7-ITN Marie-Curie
Network programme RADDEL (290023) and the EU
FP7-Integrated Infrastructure InitiativeÀI3 programme
ESTEEM2 (312483) for funding. We would also like to
thank Dr. T. B. Parsons for useful discussions.
[14] M. K. Patel, B. Vijayakrishnan, J. R. Koeppe, J. M. Chalker,
K. J. Doores, B. G. Davis, Chem. Commun. 2010, 46, 9119–
9
121.
[
[
15] D. Srimani, M. Feller, Y. Ben-David, D. Milstein, Chem.
Commun. 2012, 48, 11853–11855.
16] M. Breysse, R. Frety, J. Catal. 1987, 154, 144–154.
References
[17] N. Fischer, E. D. Goddard-Borger, R. Greiner, T. M. Kla-
potke, B. W. Skelton, J. Stierstorfer, J. Org. Chem. 2012, 77,
[1] a) B. G. Davis, Chem. Rev. 2002, 102, 579–602; b) D. P.
Gamblin, E. M. Scanlan, B. G. Davis, Chem. Rev. 2009, 109,
1
760–1764.
18] Y. C. Lee, C. P. Stowell, M. J. Krantz, Biochemistry 1976, 15,
956–3963.
[
[
[
[
[
1
31–163; c) L. X. Wang, M. N. Amin, Chem. Biol. 2014, 21,
3
5
1–66.
19] Z. Wang, in Comprehensive Organic Name Reactions and
Reagents, John Wiley & Sons, Inc., 2010, pp. 3123–3128.
20] M. W. Vetting, S. S. Hegde, K. Z. Hazleton, J. S. Blanchard,
Protein Sci. 2007, 16, 755–760.
[
2] a) C. P. R. Hackenberger, D. Schwarzer, Angew. Chem. Int.
Ed. 2008, 47, 10030–10074; b) A. J. de Graaf, M. Kooijman,
W. E. Hennink, E. Mastrobattista, Bioconjugate Chem.
2
009, 20, 1281–1295; c) Y. Takaoka, A. Ojida, I. Hamachi,
21] M. Kajitani, A. Kato, A. Wada, Y. Inokuchi, A. Ishihama, J.
Angew. Chem. Int. Ed. 2013, 52, 4088–4106; d) C. D. Spicer,
B. G. Davis, Nat. Commun. 2014, 5, 4740.
3] A. Varki, Glycobiology 1993, 3, 97–130.
Bacteriol. 1994, 176, 531–534.
22] M. Fernµndez-Gonzµlez, O. Boutureira, G. J. L. Bernardes,
J. M. Chalker, M. A. Young, J. C. Errey, B. G. Davis, Chem.
Sci. 2010, 1, 709–715.
[
[
4] B. G. Davis, in Biotherapeutics: Recent Developments using
Chemical and Molecular Biology (Eds.: L. H. Jones, A. J.
McKnight), Royal Society of Chemistry, Cambridge, 2013,
pp. 130–144.
[
23] Y. Nagata, M. M. Burger, J. Biol. Chem. 1974, 249, 3116–
3
122.
[
24] R. Ribeiro-Viana, M. Sµnchez-Navarro, J. Luczkowiak, J. R.
[
5] J. M. Chalker, G. J. L. Bernardes, B. G. Davis, Acc. Chem.
Res. 2011, 44, 730–741.
Koeppe, R. Delgado, J. Rojo, B. G. Davis, Nat. Commun.
2
012, 3, 1303.
25] T. Buskas, Y. Li, G. J. Boons, Chem. Eur. J. 2004, 10, 3517–
524.
[
6] a) S. I. van Kasteren, H. B. Kramer, D. P. Gamblin, B. G.
Davis, Nat. Protoc. 2007, 2, 3185–3194; b) S. I. van Kaste-
ren, H. B. Kramer, H. H. Jensen, S. J. Campbell, J. Kirkpa-
trick, N. J. Oldham, D. C. Anthony, B. G. Davis, Nature
[
[
3
26] Y. L. Huang, J. T. Hung, S. K. Cheung, H. Y. Lee, K. C.
Chu, S. T. Li, Y. C. Lin, C. T. Ren, T. J. Cheng, T. L. Hsu,
A. L. Yu, C. Y. Wu, C. H. Wong, Proc. Natl. Acad. Sci.
U.S.A. 2013, 110, 2517–2522.
2
007, 446, 1105–1109.
[
7] a) N. Floyd, B. Vijayakrishnan, J. R. Koeppe, B. G. Davis,
Angew. Chem. Int. Ed. 2009, 48, 7798–7802; b) M. Lo
Conte, S. Staderini, A. Marra, M. Sanchez-Navarro, B. G.
Davis, A. Dondoni, Chem. Commun. 2011, 47, 11086–
1
1088.
Received: November 15, 2014
Accepted: December 16, 2014
Published online: March 3, 2015
[
8] a) J. M. Chalker, C. S. C. Wood, B. G. Davis, J. Am. Chem.
Soc. 2009, 131, 16346–16347; b) C. D. Spicer, B. G. Davis,
Isr. J. Chem. 2015, 55, 387 – 391
ꢀ 2015 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim
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