Molecular architecture of fungal cell walls revealed by solid-state NMR

Kang, Xue; Kirui, Alex; Muszyński, Artur; Widanage, Malitha C.  Dickwella; Chen, Adrian; Azadi, Parastoo; Wang, Ping; Mentink-Vigier, Frederic; Wang, Tuo

doi:10.1038/s41467-018-05199-0

Title: Molecular architecture of fungal cell walls revealed by solid-state NMR

Journal Article · 16 July 2018 · Nature Communications

DOI: https://doi.org/10.1038/s41467-018-05199-0 · OSTI ID:1511439

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Louisiana State Univ., Baton Rouge, LA (United States)
Univ. of Georgia, Athens, GA (United States)
Louisiana State Univ. Health Sciences Center, New Orleans, LA (United States)
Florida State Univ., Tallahassee, FL (United States). National High Magnetic Field Lab. (MagLab)

The high mortality of invasive fungal infections, and the limited number and inefficacy of antifungals necessitate the development of new agents with novel mechanisms and targets. The fungal cell wall is a promising target as it contains polysaccharides absent in humans, however, its molecular structure remains elusive. Here we report the architecture of the cell walls in the pathogenic fungus Aspergillus fumigatus. Solid-state NMR spectroscopy, assisted by dynamic nuclear polarization and glycosyl linkage analysis, reveals that chitin and α-1,3-glucan build a hydrophobic scaffold that is surrounded by a hydrated matrix of diversely linked β-glucans and capped by a dynamic layer of glycoproteins and α-1,3-glucan. The two-domain distribution of α-1,3-glucans signifies the dual functions of this molecule: contributing to cell wall rigidity and fungal virulence. This study provides a high-resolution model of fungal cell walls and serves as the basis for assessing drug response to promote the development of wall-targeted antifungals.

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Research Organization:: Univ. of Georgia, Athens, GA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division

Grant/Contract Number:: SC0015662

OSTI ID:: 1511439

Journal Information:: Nature Communications, Vol. 9, Issue 1; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 165 works

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References (130)

Invasive Aspergillosis Rinaldi, M. G. Clinical Infectious Diseases, Vol. 5, Issue 6 https://doi.org/10.1093/clinids/5.6.1061	journal	November 1983
The Target of β-Expansin EXPB1 in Maize Cell Walls from Binding and Solid-State NMR Studies Wang, Tuo; Chen, Yuning; Tabuchi, Akira Plant Physiology, Vol. 172, Issue 4 https://doi.org/10.1104/pp.16.01311	journal	October 2016
A simple method for quantitative determination of polysaccharides in fungal cell walls François, Jean Marie Nature Protocols, Vol. 1, Issue 6 https://doi.org/10.1038/nprot.2006.457	journal	December 2006
Theory for cross effect dynamic nuclear polarization under magic-angle spinning in solid state nuclear magnetic resonance: The importance of level crossings Thurber, Kent R.; Tycko, Robert The Journal of Chemical Physics, Vol. 137, Issue 8 https://doi.org/10.1063/1.4747449	journal	August 2012
Secondary Structure, Dynamics, and Topology of a Seven-Helix Receptor in Native Membranes, Studied by Solid-State NMR Spectroscopy Etzkorn, Manuel; Martell, Swetlana; Andronesi, Ovidiu C. Angewandte Chemie International Edition, Vol. 46, Issue 3 https://doi.org/10.1002/anie.200602139	journal	January 2007
Cellulose Structural Polymorphism in Plant Primary Cell Walls Investigated by High-Field 2D Solid-State NMR Spectroscopy and Density Functional Theory Calculations Wang, Tuo; Yang, Hui; Kubicki, James D. Biomacromolecules, Vol. 17, Issue 6 https://doi.org/10.1021/acs.biomac.6b00441	journal	May 2016
Cell wall analysis Perez, P. Methods, Vol. 33, Issue 3 https://doi.org/10.1016/j.ymeth.2003.11.020	journal	July 2004
Surface hydrophobin prevents immune recognition of airborne fungal spores Aimanianda, Vishukumar; Bayry, Jagadeesh; Bozza, Silvia Nature, Vol. 460, Issue 7259 https://doi.org/10.1038/nature08264	journal	August 2009
Structural Rearrangements of Membrane Proteins Probed by Water-Edited Solid-State NMR Spectroscopy Ader, Christian; Schneider, Robert; Seidel, Karsten Journal of the American Chemical Society, Vol. 131, Issue 1 https://doi.org/10.1021/ja806306e	journal	January 2009
Highly Efficient, Water-Soluble Polarizing Agents for Dynamic Nuclear Polarization at High Frequency Sauvée, Claire; Rosay, Melanie; Casano, Gilles Angewandte Chemie International Edition, Vol. 52, Issue 41 https://doi.org/10.1002/anie.201304657	journal	August 2013
Highly Efficient, Water-Soluble Polarizing Agents for Dynamic Nuclear Polarization at High Frequency Sauvée, Claire; Rosay, Melanie; Casano, Gilles Angewandte Chemie, Vol. 125, Issue 41 https://doi.org/10.1002/ange.201304657	journal	August 2013
Quality Control Parameters for Broth Microdilution Tests of Anidulafungin Krisher, Karen; Brown, Steven D.; Traczewski, Maria M. Journal of Clinical Microbiology, Vol. 42, Issue 1 https://doi.org/10.1128/jcm.42.1.490.2004	journal	January 2004
High Frequency Dynamic Nuclear Polarization Ni, Qing Zhe; Daviso, Eugenio; Can, Thach V. Accounts of Chemical Research, Vol. 46, Issue 9 https://doi.org/10.1021/ar300348n	journal	April 2013
Revisit of α-Chitin Crystal Structure Using High Resolution X-ray Diffraction Data Sikorski, Pawel; Hori, Ritsuko; Wada, Masahisa Biomacromolecules, Vol. 10, Issue 5 https://doi.org/10.1021/bm801251e	journal	May 2009
Aspergillosis Case-Fatality Rate: Systematic Review of the Literature Lin, S. -J.; Schranz, J.; Teutsch, S. M. Clinical Infectious Diseases, Vol. 32, Issue 3 https://doi.org/10.1086/318483	journal	February 2001
Current perspectives on echinocandin class drugs Perlin, David S. Future Microbiology, Vol. 6, Issue 4 https://doi.org/10.2217/fmb.11.19	journal	April 2011
Cross polarization in the tilted frame: assignment and spectral simplification in heteronuclear spin systems Baldus, Marc; Petkova, Aneta T.; Herzfeld, Judith Molecular Physics, Vol. 95, Issue 6 https://doi.org/10.1080/00268979809483251	journal	December 1998
Determination of the degree of N-acetylation for chitin and chitosan by various NMR spectroscopy techniques: A review Kasaai, Mohammad R. Carbohydrate Polymers, Vol. 79, Issue 4 https://doi.org/10.1016/j.carbpol.2009.10.051	journal	March 2010
Analysis of peptidogalactomannans from the mycelial surface of Aspergillus fumigatus Haido, R. M. T.; Silva, M. H.; Ejzemberg, R. Medical Mycology, Vol. 36, Issue 5 https://doi.org/10.1080/02681219880000491	journal	January 1998
Multidimensional solid-state NMR spectroscopy of plant cell walls Wang, Tuo; Phyo, Pyae; Hong, Mei Solid State Nuclear Magnetic Resonance, Vol. 78 https://doi.org/10.1016/j.ssnmr.2016.08.001	journal	September 2016
Phosphoethanolamine cellulose: A naturally produced chemically modified cellulose Thongsomboon, Wiriya; Serra, Diego O.; Possling, Alexandra Science, Vol. 359, Issue 6373 https://doi.org/10.1126/science.aao4096	journal	January 2018
Two-dimensional magic angle spinning NMR investigation of naturally occurring chitins: Precise1H and13C resonance assignment of ?- and ?-chitin Kono, Hiroyuki Biopolymers, Vol. 75, Issue 3 https://doi.org/10.1002/bip.20124	journal	January 2004
Histoplasma capsulatum -(1,3)-glucan blocks innate immune recognition by the beta-glucan receptor Rappleye, C. A.; Eissenberg, L. G.; Goldman, W. E. Proceedings of the National Academy of Sciences, Vol. 104, Issue 4 https://doi.org/10.1073/pnas.0609848104	journal	January 2007
Sensitivity-enhanced solid-state NMR detection of expansin's target in plant cell walls Wang, T.; Park, Y. B.; Caporini, M. A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 41 https://doi.org/10.1073/pnas.1316290110	journal	September 2013
The cell wall: a carbohydrate armour for the fungal cell Latgé, Jean-Paul Molecular Microbiology, Vol. 66, Issue 2 https://doi.org/10.1111/j.1365-2958.2007.05872.x	journal	October 2007
Water–Polysaccharide Interactions in the Primary Cell Wall of Arabidopsis thaliana from Polarization Transfer Solid-State NMR White, Paul B.; Wang, Tuo; Park, Yong Bum Journal of the American Chemical Society, Vol. 136, Issue 29 https://doi.org/10.1021/ja504108h	journal	July 2014
Rapid Natural-Abundance 2D ¹³ C- ¹³ C Correlation Spectroscopy Using Dynamic Nuclear Polarization Enhanced Solid-State NMR and Matrix-Free Sample Preparation Takahashi, Hiroki; Lee, Daniel; Dubois, Lionel Angewandte Chemie International Edition, Vol. 51, Issue 47 https://doi.org/10.1002/anie.201206102	journal	October 2012
Relaxation-compensated difference spin diffusion NMR for detecting 13C–13C long-range correlations in proteins and polysaccharides Wang, Tuo; Williams, Jonathan K.; Schmidt-Rohr, Klaus Journal of Biomolecular NMR, Vol. 61, Issue 2 https://doi.org/10.1007/s10858-014-9889-0	journal	December 2014
Fungal glycans and the innate immune recognition Barreto-Bergter, Eliana; Figueiredo, Rodrigo T. Frontiers in Cellular and Infection Microbiology, Vol. 4 https://doi.org/10.3389/fcimb.2014.00145	journal	October 2014
Antifungal activity of a new triazole, voriconazole (UK-109,496), compared with three other antifungal agents tested against clinical isolates of filamentous fungi Marco, F.; Pfaller, M. A.; Messer, S. A. Medical Mycology, Vol. 36, Issue 6 https://doi.org/10.1046/j.1365-280x.1998.00170.x	journal	December 1998
Matrix-free dynamic nuclear polarization enables solid-state NMR 13C–13C correlation spectroscopy of proteins at natural isotopic abundance Takahashi, Hiroki; Hediger, Sabine; De Paëpe, Gaël Chemical Communications, Vol. 49, Issue 82 https://doi.org/10.1039/c3cc45195j	journal	January 2013
Research data supporting “Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR” Simmons, Thomas J.; Mortimer, Jenny C.; Bernardinelli, Oigres D. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.5896	dataset	January 2016
From the surface to the inner layer of the fungal cell wall Fontaine, T.; Mouyna, I.; Hartland, R. P. Biochemical Society Transactions, Vol. 25, Issue 1 https://doi.org/10.1042/bst0250194	journal	February 1997
Proton assisted recoupling and protein structure determination De Paëpe, Gaël; Lewandowski, Józef R.; Loquet, Antoine The Journal of Chemical Physics, Vol. 129, Issue 24 https://doi.org/10.1063/1.3036928	journal	December 2008
Determination of Through-Bond Carbon−Carbon Connectivities in Solid-State NMR Using the INADEQUATE Experiment Lesage, Anne; Auger, Céline; Caldarelli, Stefano Journal of the American Chemical Society, Vol. 119, Issue 33 https://doi.org/10.1021/ja971089k	journal	August 1997
Dynamic Nuclear Polarization Surface Enhanced NMR Spectroscopy Rossini, Aaron J.; Zagdoun, Alexandre; Lelli, Moreno Accounts of Chemical Research, Vol. 46, Issue 9 https://doi.org/10.1021/ar300322x	journal	March 2013
Homonuclear radio frequency-driven recoupling in rotating solids Bennett, Andrew E.; Rienstra, Chad M.; Griffiths, Janet M. The Journal of Chemical Physics, Vol. 108, Issue 22 https://doi.org/10.1063/1.476420	journal	June 1998
Theoretical aspects of Magic Angle Spinning - Dynamic Nuclear Polarization Mentink-Vigier, Frederic; Akbey, Ümit; Oschkinat, Hartmut Journal of Magnetic Resonance, Vol. 258 https://doi.org/10.1016/j.jmr.2015.07.001	journal	September 2015
Antifungal agents: mechanisms of action Odds, Frank C.; Brown, Alistair J. P.; Gow, Neil A. R. Trends in Microbiology, Vol. 11, Issue 6 https://doi.org/10.1016/S0966-842X(03)00117-3	journal	June 2003
Determination of Through-Bond Carbon−Carbon Connectivities in Solid-State NMR Using the INADEQUATE Experiment Lesage, Anne; Auger, Céline; Caldarelli, Stefano Journal of the American Chemical Society, Vol. 119, Issue 33 https://doi.org/10.1021/ja971089k	journal	August 1997
Fungal glycans and the innate immune recognition Barreto-Bergter, Eliana; Figueiredo, Rodrigo T. Frontiers in Cellular and Infection Microbiology, Vol. 4 https://doi.org/10.3389/fcimb.2014.00145	journal	October 2014
Rotational-echo double-resonance NMR Gullion, Terry; Schaefer, Jacob Journal of Magnetic Resonance (1969), Vol. 81, Issue 1 https://doi.org/10.1016/0022-2364(89)90280-1	journal	January 1989
The structure and synthesis of the fungal cell wall Bowman, Shaun M.; Free, Stephen J. BioEssays, Vol. 28, Issue 8 https://doi.org/10.1002/bies.20441	journal	January 2006
NMR-based structural biology enhanced by dynamic nuclear polarization at high magnetic field Koers, Eline J.; van der Cruijsen, Elwin A. W.; Rosay, Melanie Journal of Biomolecular NMR, Vol. 60, Issue 2-3 https://doi.org/10.1007/s10858-014-9865-8	journal	October 2014
Antifungal activity of a new triazole, voriconazole (UK-109,496), compared with three other antifungal agents tested against clinical isolates of filamentous fungi: Voriconazole in vitro activity against moulds Marco, F.; Pfaller, M. A.; Messer, S. A. Medical Mycology, Vol. 36, Issue 6 https://doi.org/10.1111/j.1365-280x.1998.00170.x	journal	December 1998
Invasive Aspergillosis Dehart, Ann L.; Ketai, Loren Chest, Vol. 94, Issue 5 https://doi.org/10.1378/chest.94.5.1117	journal	November 1988
The structure and synthesis of the fungal cell wall Bowman, Shaun M.; Free, Stephen J. BioEssays, Vol. 28, Issue 8 https://doi.org/10.1002/bies.20441	journal	January 2006
Architecture of the Yeast Cell Wall: THE LINKAGE BETWEEN CHITIN AND β(13)-GLUCAN Kollár, Roman; Petráková, Eva; Ashwell, Gilbert Journal of Biological Chemistry, Vol. 270, Issue 3 https://doi.org/10.1074/jbc.270.3.1170	journal	January 1995
¹⁵ N− ¹⁵ N Proton Assisted Recoupling in Magic Angle Spinning NMR Lewandowski, Józef R.; Paëpe, Gaël De; Eddy, Matthew T. Journal of the American Chemical Society, Vol. 131, Issue 16 https://doi.org/10.1021/ja806578y	journal	April 2009
Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR Simmons, Thomas; Mortimer, Jennifer; Bernardinelli, Od Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.7288	text	January 2016
Multidimensional solid-state NMR spectroscopy of plant cell walls Wang, Tuo; Phyo, Pyae; Hong, Mei Solid State Nuclear Magnetic Resonance, Vol. 78 https://doi.org/10.1016/j.ssnmr.2016.08.001	journal	September 2016
Homonuclear radio frequency-driven recoupling in rotating solids Bennett, Andrew E.; Rienstra, Chad M.; Griffiths, Janet M. The Journal of Chemical Physics, Vol. 108, Issue 22 https://doi.org/10.1063/1.476420	journal	June 1998
An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls Grantham, Nicholas J.; Wurman-Rodrich, Joel; Terrett, Oliver M. Nature Plants, Vol. 3, Issue 11 https://doi.org/10.1038/s41477-017-0030-8	journal	October 2017
Chitosan: An Update on Potential Biomedical and Pharmaceutical Applications Cheung, Randy; Ng, Tzi; Wong, Jack Marine Drugs, Vol. 13, Issue 8 https://doi.org/10.3390/md13085156	journal	August 2015
A simple and rapid method for the permethylation of carbohydrates Ciucanu, Ionel; Kerek, Francisc Carbohydrate Research, Vol. 131, Issue 2, p. 209-217 https://doi.org/10.1016/0008-6215(84)85242-8	journal	August 1984
Invasive Aspergillosis Denning, David W. Clinical Infectious Diseases, Vol. 26, Issue 4 https://doi.org/10.1086/513943	journal	April 1998
Following Fungal Melanin Biosynthesis with Solid-State NMR: Biopolymer Molecular Structures and Possible Connections to Cell-Wall Polysaccharides ^† Zhong, Junyan; Frases, Susana; Wang, Hsin Biochemistry, Vol. 47, Issue 16 https://doi.org/10.1021/bi702093r	journal	April 2008
De novo determination of peptide structure with solid-state magic-angle spinning NMR spectroscopy Rienstra, C. M.; Tucker-Kellogg, L.; Jaroniec, C. P. Proceedings of the National Academy of Sciences, Vol. 99, Issue 16 https://doi.org/10.1073/pnas.152346599	journal	July 2002
Secular Trends in the Epidemiology of Nosocomial Fungal Infections in the United States, 1980-1990 Sague, C. M. B.; Jarvis, W. R. Journal of Infectious Diseases, Vol. 167, Issue 5 https://doi.org/10.1093/infdis/167.5.1247	journal	May 1993
The cell wall: a carbohydrate armour for the fungal cell Latgé, Jean-Paul Molecular Microbiology, Vol. 66, Issue 2 https://doi.org/10.1111/j.1365-2958.2007.05872.x	journal	October 2007
Broadband homonuclear correlation spectroscopy driven by combined R2nv sequences under fast magic angle spinning for NMR structural analysis of organic and biological solids Hou, Guangjin; Yan, Si; Trébosc, Julien Journal of Magnetic Resonance, Vol. 232 https://doi.org/10.1016/j.jmr.2013.04.009	journal	July 2013
β-glucan: Crucial component of the fungal cell wall and elusive MAMP in plants Fesel, Philipp H.; Zuccaro, Alga Fungal Genetics and Biology, Vol. 90 https://doi.org/10.1016/j.fgb.2015.12.004	journal	May 2016
Revisit of α-Chitin Crystal Structure Using High Resolution X-ray Diffraction Data Sikorski, Pawel; Hori, Ritsuko; Wada, Masahisa Biomacromolecules, Vol. 10, Issue 5 https://doi.org/10.1021/bm801251e	journal	May 2009
Antifungal Agents: Mode of Action, Mechanisms of Resistance, and Correlation of These Mechanisms with Bacterial Resistance Ghannoum, Mahmoud A.; Rice, Louis B. Clinical Microbiology Reviews, Vol. 12, Issue 4 https://doi.org/10.1128/CMR.12.4.501	journal	October 1999
An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls Grantham, Nj; Wurman-Rodrich, J.; Terrett, Oliver Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.13865	text	January 2017
Cell Wall Assembly in Saccharomyces cerevisiae Lesage, G.; Bussey, H. Microbiology and Molecular Biology Reviews, Vol. 70, Issue 2 https://doi.org/10.1128/MMBR.00038-05	journal	June 2006
Melanin is an essential component for the integrity of the cell wall of Aspergillus fumigatus conidia Pihet, Marc; Vandeputte, Patrick; Tronchin, Guy BMC Microbiology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2180-9-177	journal	January 2009
From the surface to the inner layer of the fungal cell wall Fontaine, T.; Mouyna, I.; Hartland, R. P. Biochemical Society Transactions, Vol. 25, Issue 1 https://doi.org/10.1042/bst0250194	journal	February 1997
Cell wall analysis Perez, P. Methods, Vol. 33, Issue 3 https://doi.org/10.1016/j.ymeth.2003.11.020	journal	July 2004
Surface Glycans of Candida albicans and Other Pathogenic Fungi: Physiological Roles, Clinical Uses, and Experimental Challenges Masuoka, J. Clinical Microbiology Reviews, Vol. 17, Issue 2 https://doi.org/10.1128/CMR.17.2.281-310.2004	journal	April 2004
Secondary Structure, Dynamics, and Topology of a Seven-Helix Receptor in Native Membranes, Studied by Solid-State NMR Spectroscopy Etzkorn, Manuel; Martell, Swetlana; Andronesi, Ovidiu C. Angewandte Chemie International Edition, Vol. 46, Issue 3 https://doi.org/10.1002/anie.200602139	journal	January 2007
Water–Polysaccharide Interactions in the Primary Cell Wall of Arabidopsis thaliana from Polarization Transfer Solid-State NMR White, Paul B.; Wang, Tuo; Park, Yong Bum Journal of the American Chemical Society, Vol. 136, Issue 29 https://doi.org/10.1021/ja504108h	journal	July 2014
Cellulose Structural Polymorphism in Plant Primary Cell Walls Investigated by High-Field 2D Solid-State NMR Spectroscopy and Density Functional Theory Calculations Wang, Tuo; Yang, Hui; Kubicki, James D. Biomacromolecules, Vol. 17, Issue 6 https://doi.org/10.1021/acs.biomac.6b00441	journal	May 2016
Comparative structure and biomechanics of plant primary and secondary cell walls Cosgrove, Daniel J.; Jarvis, Michael C. Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00204	journal	January 2012
Sensitivity-enhanced solid-state NMR detection of expansin's target in plant cell walls Wang, T.; Park, Y. B.; Caporini, M. A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 41 https://doi.org/10.1073/pnas.1316290110	journal	September 2013
Combined zero-quantum and spin-diffusion mixing for efficient homonuclear correlation spectroscopy under fast MAS: broadband recoupling and detection of long-range correlations Lu, Xingyu; Guo, Changmiao; Hou, Guangjin Journal of Biomolecular NMR, Vol. 61, Issue 1 https://doi.org/10.1007/s10858-014-9875-6	journal	November 2014
Synthesis and assembly of fungal melanin Eisenman, Helene C.; Casadevall, Arturo Applied Microbiology and Biotechnology, Vol. 93, Issue 3 https://doi.org/10.1007/s00253-011-3777-2	journal	December 2011
The Target of β-Expansin EXPB1 in Maize Cell Walls from Binding and Solid-State NMR Studies Wang, Tuo; Chen, Yuning; Tabuchi, Akira Plant Physiology, Vol. 172, Issue 4 https://doi.org/10.1104/pp.16.01311	journal	October 2016
A simple method for quantitative determination of polysaccharides in fungal cell walls François, Jean Marie Nature Protocols, Vol. 1, Issue 6 https://doi.org/10.1038/nprot.2006.457	journal	December 2006
Solid-state NMR Reveals the Carbon-based Molecular Architecture of Cryptococcus neoformans Fungal Eumelanins in the Cell Wall Chatterjee, Subhasish; Prados-Rosales, Rafael; Itin, Boris Journal of Biological Chemistry, Vol. 290, Issue 22 https://doi.org/10.1074/jbc.M114.618389	journal	March 2015
Analysis of peptidogalactomannans from the mycelial surface of Aspergillus fumigatus Haido, R. M. T.; Silva, M. H.; Ejzemberg, R. Medical Mycology, Vol. 36, Issue 5 https://doi.org/10.1080/02681219880000491	journal	January 1998
Invasive Aspergillosis Darling, Bethany A.; Milder, Edmund A. Pediatrics in Review, Vol. 39, Issue 9 https://doi.org/10.1542/pir.2017-0129	journal	August 2018
3D TEDOR NMR Experiments for the Simultaneous Measurement of Multiple Carbon−Nitrogen Distances in Uniformly ¹³ C, ¹⁵ N-Labeled Solids Jaroniec, Christopher P.; Filip, Claudiu; Griffin, Robert G. Journal of the American Chemical Society, Vol. 124, Issue 36 https://doi.org/10.1021/ja026385y	journal	September 2002
Aspergillosis Case-Fatality Rate: Systematic Review of the Literature Lin, S. -J.; Schranz, J.; Teutsch, S. M. Clinical Infectious Diseases, Vol. 32, Issue 3 https://doi.org/10.1086/318483	journal	February 2001
Cross polarization in the tilted frame: assignment and spectral simplification in heteronuclear spin systems Baldus, Marc; Petkova, Aneta T.; Herzfeld, Judith Molecular Physics, Vol. 95, Issue 6 https://doi.org/10.1080/00268979809483251	journal	December 1998
Microstructure of Cell Wall-Associated Melanin in the Human Pathogenic Fungus Cryptococcus neoformans ^† Eisenman, Helene C.; Nosanchuk, Joshua D.; Webber, J. Beau W. Biochemistry, Vol. 44, Issue 10 https://doi.org/10.1021/bi047731m	journal	March 2005
Two-dimensional magic angle spinning NMR investigation of naturally occurring chitins: Precise1H and13C resonance assignment of ?- and ?-chitin Kono, Hiroyuki Biopolymers, Vol. 75, Issue 3 https://doi.org/10.1002/bip.20124	journal	January 2004
Aspergillus fumigatus melanins: interference with the host endocytosis pathway and impact on virulence Heinekamp, Thorsten; Thywißen, Andreas; Macheleidt, Juliane Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00440	journal	January 2013
Invasive Aspergillosis Denning, David W. Clinical Infectious Diseases, Vol. 26, Issue 4 https://doi.org/10.1086/513943	journal	April 1998
Antifungal activity of a new triazole, voriconazole (UK-109,496), compared with three other antifungal agents tested against clinical isolates of filamentous fungi Marco, F.; Pfaller, M. A.; Messer, S. A. Medical Mycology, Vol. 36, Issue 6 https://doi.org/10.1080/02681219880000691	journal	January 1998
A Trial of Itraconazole or Amphotericin B for HIV-Associated Talaromycosis Le, Thuy; Kinh, Nguyen Van; Cuc, Ngo T. K. New England Journal of Medicine, Vol. 376, Issue 24 https://doi.org/10.1056/NEJMoa1613306	journal	June 2017
Water Distribution, Dynamics, and Interactions with Alzheimer’s β-Amyloid Fibrils Investigated by Solid-State NMR Wang, Tuo; Jo, Hyunil; DeGrado, William F. Journal of the American Chemical Society, Vol. 139, Issue 17 https://doi.org/10.1021/jacs.7b02089	journal	April 2017
Infections with Aspergillus Species Andriole, Vincent T. Clinical Infectious Diseases, Vol. 17, Issue Supplement_2 https://doi.org/10.1093/clinids/17.supplement_2.s481	journal	November 1993
β-glucan: Crucial component of the fungal cell wall and elusive MAMP in plants Fesel, Philipp H.; Zuccaro, Alga Fungal Genetics and Biology, Vol. 90 https://doi.org/10.1016/j.fgb.2015.12.004	journal	May 2016
Efficient assignment and NMR analysis of an intact virus using sequential side-chain correlations and DNP sensitization Sergeyev, Ivan V.; Itin, Boris; Rogawski, Rivkah Proceedings of the National Academy of Sciences, Vol. 114, Issue 20 https://doi.org/10.1073/pnas.1701484114	journal	May 2017
Theory for cross effect dynamic nuclear polarization under magic-angle spinning in solid state nuclear magnetic resonance: The importance of level crossings Thurber, Kent R.; Tycko, Robert The Journal of Chemical Physics, Vol. 137, Issue 8 https://doi.org/10.1063/1.4747449	journal	August 2012
Exhaustive crystal structure search and crystal modeling of β-chitin Yui, Toshifumi; Taki, Naoto; Sugiyama, Junji International Journal of Biological Macromolecules, Vol. 40, Issue 4 https://doi.org/10.1016/j.ijbiomac.2006.08.017	journal	March 2007
Probing the Molecular Architecture of Arabidopsis thaliana Secondary Cell Walls Using Two- and Three-Dimensional ¹³ C Solid State Nuclear Magnetic Resonance Spectroscopy Dupree, Ray; Simmons, Thomas J.; Mortimer, Jennifer C. Biochemistry, Vol. 54, Issue 14 https://doi.org/10.1021/bi501552k	journal	March 2015
Proton-Assisted Recoupling (PAR) in Peptides and Proteins Donovan, Kevin J.; Jain, Sheetal K.; Silvers, Robert The Journal of Physical Chemistry B, Vol. 121, Issue 48 https://doi.org/10.1021/acs.jpcb.7b08934	journal	November 2017
Polarization-Enhanced NMR Spectroscopy of Biomolecules in Frozen Solution Hall, Dennis A.; Maus, Douglas C.; Gerfen, Gary J. Science, Vol. 276, Issue 5314 https://doi.org/10.1126/science.276.5314.930	journal	May 1997
Surface hydrophobin prevents immune recognition of airborne fungal spores Aimanianda, Vishukumar; Bayry, Jagadeesh; Bozza, Silvia Nature, Vol. 460, Issue 7259 https://doi.org/10.1038/nature08264	journal	August 2009
Theoretical aspects of Magic Angle Spinning - Dynamic Nuclear Polarization Mentink-Vigier, Frederic; Akbey, Ümit; Oschkinat, Hartmut Journal of Magnetic Resonance, Vol. 258 https://doi.org/10.1016/j.jmr.2015.07.001	journal	September 2015
Aspergillus fumigatus and Aspergillosis Latgé, Jean-Paul Clinical Microbiology Reviews, Vol. 12, Issue 2 https://doi.org/10.1128/CMR.12.2.310	journal	April 1999
Dynamic Nuclear Polarization Enhanced MAS NMR Spectroscopy for Structural Analysis of HIV-1 Protein Assemblies Gupta, Rupal; Lu, Manman; Hou, Guangjin The Journal of Physical Chemistry B, Vol. 120, Issue 2 https://doi.org/10.1021/acs.jpcb.5b12134	journal	January 2016
Dynamic Nuclear Polarization Surface Enhanced NMR Spectroscopy Rossini, Aaron J.; Zagdoun, Alexandre; Lelli, Moreno Accounts of Chemical Research, Vol. 46, Issue 9 https://doi.org/10.1021/ar300322x	journal	March 2013
Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR Simmons, Thomas J.; Mortimer, Jenny C.; Bernardinelli, Oigres D. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13902	journal	December 2016
The refocused INADEQUATE MAS NMR experiment in multiple spin-systems: Interpreting observed correlation peaks and optimising lineshapes Cadars, Sylvian; Sein, Julien; Duma, Luminita Journal of Magnetic Resonance, Vol. 188, Issue 1 https://doi.org/10.1016/j.jmr.2007.05.016	journal	September 2007
Proton-Assisted Recoupling (PAR) in Peptides and Proteins Donovan, Kevin J.; Jain, Sheetal K.; Silvers, Robert The Journal of Physical Chemistry B, Vol. 121, Issue 48 https://doi.org/10.1021/acs.jpcb.7b08934	journal	November 2017
Architecture of the Yeast Cell Wall: β(1→6)-GLUCAN INTERCONNECTS MANNOPROTEIN, β(1→3)-GLUCAN, AND CHITIN Kollár, Roman; Reinhold, Bruce B.; Petráková, Eva Journal of Biological Chemistry, Vol. 272, Issue 28 https://doi.org/10.1074/jbc.272.28.17762	journal	July 1997
Determination of the degree of N-acetylation for chitin and chitosan by various NMR spectroscopy techniques: A review Kasaai, Mohammad R. Carbohydrate Polymers, Vol. 79, Issue 4 https://doi.org/10.1016/j.carbpol.2009.10.051	journal	March 2010
Rapid Natural-Abundance 2D ¹³ C- ¹³ C Correlation Spectroscopy Using Dynamic Nuclear Polarization Enhanced Solid-State NMR and Matrix-Free Sample Preparation Takahashi, Hiroki; Lee, Daniel; Dubois, Lionel Angewandte Chemie International Edition, Vol. 51, Issue 47 https://doi.org/10.1002/anie.201206102	journal	October 2012
Neurotoxin II Bound to Acetylcholine Receptors in Native Membranes Studied by Dynamic Nuclear Polarization NMR Linden, Arne H.; Lange, Sascha; Franks, W. Trent Journal of the American Chemical Society, Vol. 133, Issue 48 https://doi.org/10.1021/ja206999c	journal	December 2011
3D TEDOR NMR Experiments for the Simultaneous Measurement of Multiple Carbon−Nitrogen Distances in Uniformly ¹³ C, ¹⁵ N-Labeled Solids Jaroniec, Christopher P.; Filip, Claudiu; Griffin, Robert G. Journal of the American Chemical Society, Vol. 124, Issue 36 https://doi.org/10.1021/ja026385y	journal	September 2002
Microstructure of Cell Wall-Associated Melanin in the Human Pathogenic Fungus Cryptococcus neoformans ^† Eisenman, Helene C.; Nosanchuk, Joshua D.; Webber, J. Beau W. Biochemistry, Vol. 44, Issue 10 https://doi.org/10.1021/bi047731m	journal	March 2005
Following Fungal Melanin Biosynthesis with Solid-State NMR: Biopolymer Molecular Structures and Possible Connections to Cell-Wall Polysaccharides ^† Zhong, Junyan; Frases, Susana; Wang, Hsin Biochemistry, Vol. 47, Issue 16 https://doi.org/10.1021/bi702093r	journal	April 2008
De novo determination of peptide structure with solid-state magic-angle spinning NMR spectroscopy Rienstra, C. M.; Tucker-Kellogg, L.; Jaroniec, C. P. Proceedings of the National Academy of Sciences, Vol. 99, Issue 16 https://doi.org/10.1073/pnas.152346599	journal	July 2002
An even pattern of xylan substitution is critical for interaction with cellulose in plant cell walls Grantham, Nicholas J.; Wurman-Rodrich, Joel; Terrett, Oliver M. Nature Plants, Vol. 3, Issue 11 https://doi.org/10.1038/s41477-017-0030-8	journal	October 2017
Matrix-free dynamic nuclear polarization enables solid-state NMR 13C–13C correlation spectroscopy of proteins at natural isotopic abundance Takahashi, Hiroki; Hediger, Sabine; De Paëpe, Gaël Chemical Communications, Vol. 49, Issue 82 https://doi.org/10.1039/c3cc45195j	journal	January 2013
Polarization-Enhanced NMR Spectroscopy of Biomolecules in Frozen Solution Hall, Dennis A.; Maus, Douglas C.; Gerfen, Gary J. Science, Vol. 276, Issue 5314 https://doi.org/10.1126/science.276.5314.930	journal	May 1997
Hidden Killers: Human Fungal Infections Brown, G. D.; Denning, D. W.; Gow, N. A. R. Science Translational Medicine, Vol. 4, Issue 165 https://doi.org/10.1126/scitranslmed.3004404	journal	December 2012
Synthesis and assembly of fungal melanin Eisenman, Helene C.; Casadevall, Arturo Applied Microbiology and Biotechnology, Vol. 93, Issue 3 https://doi.org/10.1007/s00253-011-3777-2	journal	December 2011
Relaxation-compensated difference spin diffusion NMR for detecting 13C–13C long-range correlations in proteins and polysaccharides Wang, Tuo; Williams, Jonathan K.; Schmidt-Rohr, Klaus Journal of Biomolecular NMR, Vol. 61, Issue 2 https://doi.org/10.1007/s10858-014-9889-0	journal	December 2014
Cell Wall Chitosan Is Necessary for Virulence in the Opportunistic Pathogen Cryptococcus neoformans Baker, Lorina G.; Specht, Charles A.; Lodge, Jennifer K. Eukaryotic Cell, Vol. 10, Issue 9 https://doi.org/10.1128/ec.05138-11	journal	July 2011
Therapeutic Outcome in Invasive Aspergillosis Denning, D. W. Clinical Infectious Diseases, Vol. 23, Issue 3 https://doi.org/10.1093/clinids/23.3.608	journal	September 1996
Cell Wall Architecture in Yeast: New Structure and New Challenges Lipke, Peter N.; Ovalle, Rafael Journal of Bacteriology, Vol. 180, Issue 15 https://doi.org/10.1128/JB.180.15.3735-3740.1998	journal	August 1998
Highly Efficient, Water-Soluble Polarizing Agents for Dynamic Nuclear Polarization at High Frequency Sauvée, Claire; Rosay, Melanie; Casano, Gilles Angewandte Chemie, Vol. 125, Issue 41 https://doi.org/10.1002/ange.201304657	journal	August 2013
Chitosan: An Update on Potential Biomedical and Pharmaceutical Applications Cheung, Randy; Ng, Tzi; Wong, Jack Marine Drugs, Vol. 13, Issue 8 https://doi.org/10.3390/md13085156	journal	August 2015
Phosphoethanolamine cellulose: A naturally produced chemically modified cellulose Thongsomboon, Wiriya; Serra, Diego O.; Possling, Alexandra Science, Vol. 359, Issue 6373 https://doi.org/10.1126/science.aao4096	journal	January 2018
¹⁵ N− ¹⁵ N Proton Assisted Recoupling in Magic Angle Spinning NMR Lewandowski, Józef R.; Paëpe, Gaël De; Eddy, Matthew T. Journal of the American Chemical Society, Vol. 131, Issue 16 https://doi.org/10.1021/ja806578y	journal	April 2009
Rapid Natural-Abundance 2D ¹³ C- ¹³ C Correlation Spectroscopy Using Dynamic Nuclear Polarization Enhanced Solid-State NMR and Matrix-Free Sample Preparation Takahashi, Hiroki; Lee, Daniel; Dubois, Lionel Angewandte Chemie, Vol. 124, Issue 47 https://doi.org/10.1002/ange.201206102	journal	October 2012

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