Structure of the Complex between a Heparan Sulfate Octasaccharide and Mycobacterial Heparin-Binding Hemagglutinin
Dr. Teng-Yi Huang
Genomics Research Center, Academia Sinica, No. 128, Section 2, Academia Road, Taipei, 115 Taiwan
These authors contributed equally to this work.
Search for more papers by this authorDr. Deli Irene
Department of Chemistry, National Dong Hwa University, No. 1, Section 2, Da Hsueh Road, Shoufeng, Hualien, 974 Taiwan
These authors contributed equally to this work.
Search for more papers by this authorDr. Medel Manuel L. Zulueta
Genomics Research Center, Academia Sinica, No. 128, Section 2, Academia Road, Taipei, 115 Taiwan
Search for more papers by this authorTzu-Jui Tai
Department of Chemistry, National Dong Hwa University, No. 1, Section 2, Da Hsueh Road, Shoufeng, Hualien, 974 Taiwan
Search for more papers by this authorShih-Han Lain
Department of Chemistry, National Dong Hwa University, No. 1, Section 2, Da Hsueh Road, Shoufeng, Hualien, 974 Taiwan
Search for more papers by this authorDr. Cheng-Po Cheng
Genomics Research Center, Academia Sinica, No. 128, Section 2, Academia Road, Taipei, 115 Taiwan
Search for more papers by this authorDr. Ping-Xi Tsai
Genomics Research Center, Academia Sinica, No. 128, Section 2, Academia Road, Taipei, 115 Taiwan
Search for more papers by this authorDr. Shu-Yi Lin
Genomics Research Center, Academia Sinica, No. 128, Section 2, Academia Road, Taipei, 115 Taiwan
Search for more papers by this authorDr. Zhi-Geng Chen
Genomics Research Center, Academia Sinica, No. 128, Section 2, Academia Road, Taipei, 115 Taiwan
Search for more papers by this authorChiao-Chu Ku
Institute of Molecular Biology, Academia Sinica, No. 128, Section 2, Academia Road, Taipei, 115 Taiwan
Search for more papers by this authorProf. Dr. Chwan-Deng Hsiao
Institute of Molecular Biology, Academia Sinica, No. 128, Section 2, Academia Road, Taipei, 115 Taiwan
Search for more papers by this authorCorresponding Author
Prof. Dr. Chia-Lin Chyan
Department of Chemistry, National Dong Hwa University, No. 1, Section 2, Da Hsueh Road, Shoufeng, Hualien, 974 Taiwan
Search for more papers by this authorCorresponding Author
Prof. Dr. Shang-Cheng Hung
Genomics Research Center, Academia Sinica, No. 128, Section 2, Academia Road, Taipei, 115 Taiwan
Search for more papers by this authorDr. Teng-Yi Huang
Genomics Research Center, Academia Sinica, No. 128, Section 2, Academia Road, Taipei, 115 Taiwan
These authors contributed equally to this work.
Search for more papers by this authorDr. Deli Irene
Department of Chemistry, National Dong Hwa University, No. 1, Section 2, Da Hsueh Road, Shoufeng, Hualien, 974 Taiwan
These authors contributed equally to this work.
Search for more papers by this authorDr. Medel Manuel L. Zulueta
Genomics Research Center, Academia Sinica, No. 128, Section 2, Academia Road, Taipei, 115 Taiwan
Search for more papers by this authorTzu-Jui Tai
Department of Chemistry, National Dong Hwa University, No. 1, Section 2, Da Hsueh Road, Shoufeng, Hualien, 974 Taiwan
Search for more papers by this authorShih-Han Lain
Department of Chemistry, National Dong Hwa University, No. 1, Section 2, Da Hsueh Road, Shoufeng, Hualien, 974 Taiwan
Search for more papers by this authorDr. Cheng-Po Cheng
Genomics Research Center, Academia Sinica, No. 128, Section 2, Academia Road, Taipei, 115 Taiwan
Search for more papers by this authorDr. Ping-Xi Tsai
Genomics Research Center, Academia Sinica, No. 128, Section 2, Academia Road, Taipei, 115 Taiwan
Search for more papers by this authorDr. Shu-Yi Lin
Genomics Research Center, Academia Sinica, No. 128, Section 2, Academia Road, Taipei, 115 Taiwan
Search for more papers by this authorDr. Zhi-Geng Chen
Genomics Research Center, Academia Sinica, No. 128, Section 2, Academia Road, Taipei, 115 Taiwan
Search for more papers by this authorChiao-Chu Ku
Institute of Molecular Biology, Academia Sinica, No. 128, Section 2, Academia Road, Taipei, 115 Taiwan
Search for more papers by this authorProf. Dr. Chwan-Deng Hsiao
Institute of Molecular Biology, Academia Sinica, No. 128, Section 2, Academia Road, Taipei, 115 Taiwan
Search for more papers by this authorCorresponding Author
Prof. Dr. Chia-Lin Chyan
Department of Chemistry, National Dong Hwa University, No. 1, Section 2, Da Hsueh Road, Shoufeng, Hualien, 974 Taiwan
Search for more papers by this authorCorresponding Author
Prof. Dr. Shang-Cheng Hung
Genomics Research Center, Academia Sinica, No. 128, Section 2, Academia Road, Taipei, 115 Taiwan
Search for more papers by this authorAbstract
Heparin-binding hemagglutinin (HBHA) is a 199 amino acid virulence factor at the envelope of Mycobacterium tuberculosis that contributes to latent tuberculosis. The binding of HBHA to respiratory epithelial cells, which leads to extrapulmonary dissemination of the pathogen, is mediated by cell-surface heparan sulfate (HS). We report the structural characterization of the HBHA/HS complex by NMR spectroscopy. To develop a model for the molecular recognition, the first chemically synthesized uniformly 13C- and 15N-labeled HS octasaccharide and a uniformly 13C- and 15N-labeled form of HBHA were prepared. Residues 180–195 at the C-terminal region of HBHA show large chemical shift perturbation upon association with the octasaccharide. Molecular dynamics simulations conforming to the multidimensional NMR data revealed key electrostatic and even hydrophobic interactions between the binding partners that may aid in the development of agents targeting the binding event.
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References
- 1World Health Organization (WHO), Global Tuberculosis Report, 20th ed., WHO Press, Geneva, 2015.
- 2A. Koul, E. Arnoult, N. Lounis, J. Guillemont, K. Andries, Nature 2011, 469, 483–490.
- 3
- 3aK. Pethe, S. Alonso, F. Biet, G. Delogu, M. J. Brennan, C. Locht, F. D. Menozzi, Nature 2001, 412, 190–194;
- 3bN. Krishnan, B. D. Robertson, G. Thwaites, Tuberculosis 2010, 90, 361–366.
- 4
- 4aG. Delogu, M. J. Brennan, J. Bacteriol. 1999, 181, 7464–7469;
- 4bP. Lebrun, D. Raze, B. Fritzinger, J.-M. Wieruszeski, F. Biet, A. Dose, M. Carpentier, D. Schwarzer, F. Allain, G. Lippens, C. Locht, PLoS ONE 2012, 7, e 32421.
- 5
- 5aJ. V. Lomino, A. Tripathy, M. R. Redinbo, J. Bacteriol. 2011, 193, 2089–2096;
- 5bC. Esposito, M. Cantisani, G. D'Auria, L. Falcigno, E. Pedone, S. Galdiero, R. Berisio, FEBS Lett. 2012, 586, 659–667.
- 6D. Xu, J. D. Esko, Annu. Rev. Biochem. 2014, 83, 129–157.
- 7M. M. L. Zulueta, S.-Y. Lin, Y.-P. Hu, S.-C. Hung, Curr. Opin. Chem. Biol. 2013, 17, 1023–1029.
- 8N. S. Gandhi, R. L. Mancera, Chem. Biol. Drug Des. 2008, 72, 455–482.
- 9F. D. Menozzi, V. M. Reddy, D. Cayet, D. Raze, A.-S. Debrie, M.-P. Dehouck, R. Cecchelli, C. Locht, Microbes Infect. 2006, 8, 1–9.
- 10K. Pethe, V. Puech, M. Daffé, C. Josenhans, H. Drobecq, C. Locht, F. D. Menozzi, Mol. Microbiol. 2001, 39, 89–99.
- 11M. M. L. Zulueta, S.-Y. Lin, Y.-T. Lin, C.-J. Huang, C.-C. Wang, C.-C. Ku, Z. Shi, C.-L. Chyan, D. Irene, L.-H. Lim, T.-I. Tsai, Y.-P. Hu, S. D. Arco, C.-H. Wong, S.-C. Hung, J. Am. Chem. Soc. 2012, 134, 8988–8995.
- 12Y.-P. Hu, S.-Y. Lin, C.-Y. Huang, M. M. L. Zulueta, J.-Y. Liu, W. Chang, S.-C. Hung, Nat. Chem. 2011, 3, 557–563.
- 13S.-C. Hung, X.-A. Lu, J.-C. Lee, M. D.-T. Chang, S.-l. Fang, T.-c. Fan, M. M. L. Zulueta, Y.-Q. Zhong, Org. Biomol. Chem. 2012, 10, 760–772.
- 14S. Arndt, L. C. Hsieh-Wilson, Org. Lett. 2003, 5, 4179–4182.
- 15
- 15aL. Whitmore, B. A. Wallace, Nucleic Acids Res. 2004, 32, W 668–W673;
- 15bL. Whitmore, B. A. Wallace, Biopolymers 2008, 89, 392–400.
- 16The complete 1H, 13C, and 15N chemical-shift assignments the free and bound HBHA110-199 have been deposited in the Biological Magnetic Resonance Bank (BMRB) with accession numbers 26887 and 26888, respectively.
- 17D. S. Wishart, B. D. Sykes, J. Biomol. NMR 1994, 4, 171–180.
- 18P. Güntert, L. Buchner, J. Biomol. NMR 2015, 62, 453–471.
- 19P.-H. Hsieh, D. F. Thieker, M. Guerrini, R. J. Woods, J. Liu, Sci. Rep. 2016, 6, 29602.
- 20M. Hricovíni, F. Bízik, Carbohydr. Res. 2007, 342, 779–783.
- 21M. Hricovíni, P.-A. Driguez, O. L. Malkina, J. Phys. Chem. B 2014, 118, 11931–11942.
- 22
- 22aM. Guerrini, S. Guglieri, D. Beccati, G. Torri, C. Viskov, P. Mourier, Biochem. J. 2006, 399, 191–198;
- 22bZ. Zhang, S. A. McCallum, J. Xie, L. Nieto, F. Corzana, J. Jiménez-Barbero, M. Chen, J. Liu, R. J. Linhardt, J. Am. Chem. Soc. 2008, 130, 12998–13007;
- 22cL. Nieto, Á. Canales, G. Giménez-Gallego, P. M. Nieto, J. Jiménez-Barbero, Chem. Eur. J. 2011, 17, 11204–11209;
- 22dL. Nieto, Á. Canales, I. S. Fernández, E. Santillana, R. González-Corrochano, M. Redondo-Horcajo, F. J. Cañada, P. Nieto, M. Martín-Lomas, G. Giménez-Gallego, J. Jiménez-Barbero, ChemBioChem 2013, 14, 1732–1744.
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