Adaptative survival of Aspergillus fumigatus to echinocandins arises from cell wall remodeling beyond β−1,3-glucan synthesis inhibition
Open accessPublished version of a preprint
Abstract
Antifungal echinocandins inhibit the biosynthesis of β−1,3-glucan, a major and essential polysaccharide component of the fungal cell wall. However, the efficacy of echinocandins against the pathogen Aspergillus fumigatus is limited. Here, we use solid-state nuclear magnetic resonance (ssNMR) and other techniques to show that echinocandins induce dynamic changes in the assembly of mobile and rigid polymers within the A. fumigatus cell wall. The reduction of β−1,3-glucan induced by echinocandins is accompanied by a concurrent increase in levels of chitin, chitosan, and highly polymorphic α−1,3-glucans, whose physical association with chitin maintains cell wall integrity and modulates water permeability. The rearrangement of the macromolecular network is dynamic and controls the permeability and circulation of the drug throughout the cell wall. Thus, our results indicate that echinocandin treatment triggers compensatory rearrangements in the cell wall that may help A. fumigatus to tolerate the drugs’ antifungal effects.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Reduced water permeability is a common response previously observed in several Aspergillus species under stress.
“Both C. albicans and C. auris AR386 exhibit reduced water permeability (Fig. 4a), a common response previously also observed in several Aspergillus species under stress50,53.”
From Distinct echinocandin responses of Candida albicans and Candida auris cell walls revealed by solid-state NMR (2025) · cites this paper as [50]
The Results section, “Reduced water retention and polymer dynamics” (page unavailable), reports reduced water accessibility in A. fumigatus cell walls after caspofungin treatment and suggests this should reduce cell-wall permeability. It does not establish reduced water permeability as a common response across several Aspergillus species or under stress generally, and permeability was inferred rather than directly measured. (LLM, conf=0.87)
Experimental — accuracy not yet measuredThe balance between rigid structural components and mobile, water-accessible regions allows fungi to fine-tune cell wall permeability, aiding adaptive survival.
“Recent observations suggest that the balance between rigid structural components and mobile, water-accessible regions allows fungi to fine-tune cell wall permeability, aiding adaptive survival50,65.”
From Distinct echinocandin responses of Candida albicans and Candida auris cell walls revealed by solid-state NMR (2025) · cites this paper as [50]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Harris, C. R., Millman, K. J., van der Walt, S. J., Gommers, R., Virtanen, P., Cournapeau, D., Wieser, E., Taylor, J., Berg, S., Smith, N. J., et al. (2020) · Nature · doi:10.1038/s41586-020-2649-2 · Cited by 23,826 · see citing works
Global incidence and mortality of severe fungal disease
Denning, D. W. (2024) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(23)00692-8 · Cited by 1,640 · cited 1× · see citing works
“Invasive Aspergillus infections have high and increasing occurrence and mortality among immunocompromised and immunocompetent patients 1 – 3 , including, more recently, critically ill individuals suffering from SARS-CoV-2 infections 4,5 .”
Anidulafungin versus Fluconazole for Invasive Candidiasis
Reboli, A. C., Rotstein, C., Pappas, P. G., Chapman, S. W., Kett, D. H., Kumar, D., Betts, R., Wible, M., Goldstein, B. P., Schranz, J., et al. (2007) · New England Journal of Medicine · doi:10.1056/nejmoa066906 · Cited by 894 · see citing works
Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR
Simmons, T. J., Mortimer, J. C., Bernardinelli, O. D., Pöppler, A.-C., Brown, S. P., deAzevedo, E. R., Dupree, R., & Dupree, P. (2016) · Nature Communications · doi:10.1038/ncomms13902 · Cited by 436 · see citing works
Bowman, J. C., Hicks, P. S., Kurtz, M. B., Rosen, H., Schmatz, D. M., Liberator, P. A., & Douglas, C. M. (2002) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.46.9.3001-3012.2002 · Cited by 303 · see citing works
Stress, drugs, and evolution: the role of cellular signaling in fungal drug resistance.
Cowen, L. E., & Steinbach, W. J. (2008) · Eukaryotic Cell · doi:10.1128/ec.00041-08 · Cited by 285 · see citing works
Current Perspectives on Echinocandin Class Drugs
Perlin, D. S. (2011) · Future Microbiology · doi:10.2217/fmb.11.19 · Cited by 274 · see citing works
Chiou, C. C., Mavrogiorgos, N., Tillem, E., Hector, R., & Walsh, T. J. (2001) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.45.12.3310-3321.2001 · Cited by 117 · see citing works
Ries, L. N. A., Rocha, M. C., de Castro, P. A., Silva-Rocha, R., Silva, R. N., Freitas, F. Z., de Assis, L. J., Bertolini, M. C., Malavazi, I., & Goldman, G. H. (2017) · mBio · doi:10.1128/mbio.00705-17 · Cited by 76 · see citing works
Jiménez-Ortigosa, C., Moore, C., Denning, D. W., & Perlin, D. S. (2017) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01277-17 · Cited by 72 · cited 1× · see citing works
“Mutations in the fks1 genes preventing the binding of echino-candins to the catalytic subunit FKS1 of β -1,3-glucan synthase 62,63 have been identi fi ed as responsible for the drug ’ s limited ef fi cacy.”
Satish, S., Jiménez-Ortigosa, C., Zhao, Y., Lee, M. H., Dolgov, E., Krüger, T., Park, S., Denning, D. W., Kniemeyer, O., Brakhage, A. A., et al. (2019) · mBio · doi:10.1128/mbio.00779-19 · Cited by 64 · see citing works
Flagged first, then by citations
Research works printed but not linked: 94
- [1]Garcia-Vidal, C., Viasus, D. & Carratala, J. Pathogenesis of invasive fungal infections. Curr. Opin. Infect. Dis. 26, 270–276 (2013). 23449139 10.1097/QCO.0b013e32835fb920 · DOI
- [2]Erwig, L. P. & Gow, N. A. R. Interactions of fungal pathogens with phagocytes. Nat. Rev. Microbiol. 14, 163–176 (2016). 26853116 10.1038/nrmicro.2015.21 · DOI · Paper page
- [4]Hoenigl, M. Invasive fungal disease complicating Coronavirus Disease 2019: When it rains, it spores. Clin. Infect. Dis. 73, e1645–e1648 (2021). 32887998 10.1093/cid/ciaa1342 PMC7499555 · DOI
- [5]Hoenigl, M. et al. COVID-19-associated fungal infections. Nat. Microbiol. 7, 1127–1140 (2022). 35918423 10.1038/s41564-022-01172-2 PMC9362108 · DOI · Paper page
- [6]Ghannoum, M. A. & Rice, L. B. Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin. Microbiol. Rev. 12, 501–517 (1999). 10515900 10.1128/CMR.12.4.501 PMC88922 · DOI
- [7]Verweij, P. E., Snelders, E., Kema, G. H. J., Mellado, E. & Melchers, W. J. G. Azole resistance in Aspergillus fumigatus: a side-effect of environmental fungicide use? Lancet Infect. Dis. 9, 789–795 (2009). 19926038 10.1016/S1473-3099(09)70265-8 · DOI · Paper page
- [8]Odds, F. C., Brown, A. J. P. & Gow, N. A. R. Antifungal agents: Mechanisms of action. Trends Microbiol 11, 272–279 (2003). 12823944 10.1016/S0966-842X(03)00117-3 · DOI · Paper page
- [9]Hasim, S. & Coleman, J. J. Targeting the fungal cell wall: current therapies and implications for development of alternative antifungal agents. Future Med. Chem. 11, 869–883 (2019). 30994368 10.4155/fmc-2018-0465 PMC6543504 · DOI · Paper page
- [11]Chen, S. C. A., Slavin, M. A. & Sorrell, T. C. Echinocandin antifungal drugs in fungal infections. Drugs 71, 11–41 (2011). 21175238 10.2165/11585270-000000000-00000 · DOI · Paper page
- [12]SC, D. & Stevens, D. A. Caspofungin. Clin. Infect. Dis. 36, 1445–1457 (2003). 12766841 10.1086/375080 · DOI
- [13]Hu, X. et al. Structural and mechanistic insights into fungal β-1,3-glucan synthase FKS1. Nature 616, 190–198 (2023). 36949198 10.1038/s41586-023-05856-5 PMC10032269 · DOI · Paper page
- [15]Pappas, P. G. et al. Micafungin versus caspofungin for treatment of candidemia and other forms of invasive candidiasis. Clin. Infect. Dis. 45, 883–893 (2007). 17806055 10.1086/520980 · DOI · Paper page
- [16]Latgé, J. P. The pathobiology of Aspergillus fumigatus. Trends Microbiol. 9, 382–389 (2001). 11514221 10.1016/S0966-842X(01)02104-7 · DOI
- [17]Latgé, J. P. Aspergillus fumigatus and aspergillosis. Clin. Microbiol. Rev. 12, 310–350 (1999). 10194462 10.1128/CMR.12.2.310 PMC88920 · DOI · Paper page
- [19]Hopke, A., Brown, A. J. P., Hall, R. A. & Wheeler, R. T. Dynamic fungal cell wall architecture in stress adaptation and immune evasion. Trends Microbiol. 26, 284–295 (2018). 29452950 10.1016/j.tim.2018.01.007 PMC5869159 · DOI
- [20]Garcia-Rubio, R., de Oliveira, H. C., Rivera, J. & Trevijano-Contador, N. The fungal cell wall: Candida, Cryptococcus, and Aspergillus species. Front. Microbiol. 10, 2993 (2020). 31993032 10.3389/fmicb.2019.02993 PMC6962315 · DOI · Paper page
- [21]Klis, F. M., Mol, P., Hellingwerf, K. & Brul, S. Dynamics of cell wall structure in Saccharomyces cerevisiae. FEMS Microbiol. Rev. 26, 239–256 (2002). 12165426 10.1111/j.1574-6976.2002.tb00613.x · DOI
- [23]Safeer, A. et al. Probing cell-surface interactions in fungal cell walls by high-resolution 1H-detected solid-state NMR Spectroscopy. Chem. Eur. J. 29, e202202616 (2022). 36181715 10.1002/chem.202202616 PMC10099940 · DOI
- [24]Chrissian, C. et al. Solid-state NMR spectroscopy identifies three classes of lipids in Cryptococcus neoformans melanized cell walls whole fungal cells. J. Biol. Chem. 295, 15083–15096 (2020). 32859751 10.1074/jbc.RA120.015201 PMC7606693 · DOI
- [25]Ghassemi, N. et al. Solid-state NMR investigations of extracellular matrixes and cell walls of algae, bacteria, fungi, and plants. Chem. Rev. 122, 10036–10086 (2022). 34878762 10.1021/acs.chemrev.1c00669 PMC9486976 · DOI
- [26]Kang, X. et al. Molecular architecture of fungal cell walls revealed by solid-state NMR. Nat. Commun. 9, 2747 (2018). 30013106 10.1038/s41467-018-05199-0 PMC6048167 · DOI · Paper page
- [27]Latgé, J. P. & Wang, T. Modern biophysics redefines our understanding of fungal cell wall structure, complexity, and dynamics. mBio 13, e0114522 (2022). 35638742 10.1128/mbio.01145-22 PMC9239136 · DOI · Paper page
- [28]Lamon, G. et al. Solid-state NMR molecular snapshots of Aspergillus fumigatus cell wall architecture during a conidial morphotype transition. Proc. Natl Acad. Sci. USA 120, e2212003120 (2023). 36719915 10.1073/pnas.2212003120 PMC9963690 · DOI
- [29]Chakraborty, A. et al. A molecular vision of fungal cell wall organization by functional genomics and solid-state NMR. Nat. Commun. 12, 6346 (2021). 34732740 10.1038/s41467-021-26749-z PMC8566572 · DOI
- [30]Fontaine, T. et al. Molecular organization of the alkali-insoluble fraction of Aspergillus fumigatus cell wall. J. Biol. Chem. 275, 27594–27607 (2000). 10869365 10.1074/jbc.M909975199 · DOI · Paper page
- [31]Samar, D., Kieler, J. B. & Klutts, J. S. Identification and deletion of Tft1, a predicted glycosyltransferase necessary for cell wall β-1, 3; 1, 4-glucan synthesis in Aspergillus fumigatus. PLoS One 10, e0117336 (2015). 25723175 10.1371/journal.pone.0117336 PMC4344333 · DOI
- [32]Chevalier, L. et al. Cell wall dynamics stabilize tip growth in a filamentous fungus. PloS Biol. 21, e3001981 (2023). 36649360 10.1371/journal.pbio.3001981 PMC9882835 · DOI
- [33]Davi, V. et al. Systematic mapping of cell wall mechanics in the regulation of cell morphogenesis. Proc. Natl Acad. Sci. USA 116, 13833–13838 (2019). 31235592 10.1073/pnas.1820455116 PMC6628811 · DOI
- [34]Zhao, L. et al. Elastic properties of the cell wall of Aspergillus nidulans studied with atomic force microscopy. Biotechnol. Prog. 21, 292–299 (2005). 15903268 10.1021/bp0497233 · DOI
- [35]Ni, Q. Z. et al. High frequency dynamic nuclear polarization. Acc. Chem. Res. 46, 1933–1941 (2013). 23597038 10.1021/ar300348n PMC3778063 · DOI
- [36]Mentink-Vigier, F., Akbey, Ü., Oschkinat, H., Vega, S. & Feintuch, A. Theoretical aspects of magic angle spinning-dynamic nuclear polarization. J. Magn. Reson. 258, 102–120 (2015). 26232770 10.1016/j.jmr.2015.07.001 · DOI
- [37]Koers, E. J. et al. NMR-based structural biology enhanced by dynamic nuclear polarization at high magnetic field. J. Biomol. NMR 60, 157–168 (2014). 25284462 10.1007/s10858-014-9865-8 · DOI
- [38]Fernando, L. D. et al. Structural polymorphism of chitin and chitosan in fungal cell walls from solid-state NMR and principal component analysis. Front. Mol. Biosci. 8, 727053 (2021). 34513930 10.3389/fmolb.2021.727053 PMC8423923 · DOI
- [39]Sarkar, D. et al. Diffusion in intact secondary cell wall models of plants at different equilibrium moisture content. Cell Surf. 9, 100105 (2023). 37063382 10.1016/j.tcsw.2023.100105 PMC10090443 · DOI
- [40]Vermaas, J. V. et al. Mechanism of lignin inhibition of enzymatic biomass deconstruction. Biotechnol. Biofuels Bioprod. 8, 217 (2015). 10.1186/s13068-015-0379-8 PMC4687093 26697106 · DOI
- [41]Gow N. A. R., Latge, J. P. & Munro, C. A. The fungal cell wall: structure, biosynthesis, and function. Microbiol. Spectr. 5, FUNK-0035-2016 (2017). PMC11687499 28513415
- [42]Wessels, J. G. H. Developmental regulation of fungal cell wall formation. Annu. Rev. Phytopathol. 32, 413–437 (1994). 10.1146/annurev.py.32.090194.002213 · DOI
- [43]Latgé, J. P. The cell wall: a carbohydrate armour for the fungal cell. Mol. Microbiol. 66, 279–290 (2007). 17854405 10.1111/j.1365-2958.2007.05872.x · DOI · Paper page
- [44]Walker, L. A., Lee, K. K., Munro, C. A. & Gow, N. A. Caspofungin treatment of aspergillus fumigatus results in ChsG-dependent upregulation of Chitin synthesis and the formation of Chitin-rich microcolonies. Antimicrob. Agents Chemother. 59, 5932–5941 (2015). 26169407 10.1128/AAC.00862-15 PMC4576100 · DOI
- [45]Wagner, A. S., Lumsdaine, S. W., Mangrum, M. M. & Reynolds, T. B. Caspofungin-induced β(1,3)-glucan exposure in Candida albicans is driven by increased chitin levels. mBio 14, e0007423 (2023). 37377417 10.1128/mbio.00074-23 PMC10470516 · DOI · Paper page
- [46]Jiménez-Ortigosa, C. et al. Chitin synthases with a myosin motor-like domain control the resistance of Aspergillus fumigatus to echinocandins. Antimicrob. Agents Chemother. 56, 6121–6131 (2012). 22964252 10.1128/AAC.00752-12 PMC3497188 · DOI
- [47]Muszkieta, L. et al. Deciphering the role of the chitin synthase families 1 and 2 in the in vivo and in vitro growth of Aspergillus fumigatus by multiple gene targeting deletion. Cell Microbiol. 16, 1784–1805 (2014). 24946720 10.1111/cmi.12326 · DOI · Paper page
- [48]Verwer, P. E., van Duijn, M. L., Tavakol, M., Bakker-Woudenberg, I. A. & van de Sande, W. W. Reshuffling of Aspergillus fumigatus cell wall components chitin and β-glucan under the influence of caspofungin or nikkomycin Z alone or in combination. Antimicrob. Agents Chemother. 56, 1595–1598 (2012). 22203603 10.1128/AAC.05323-11 PMC3294952 · DOI
- [49]Ganesan, L. T., Manavathu, E. K., Cutright, J. L., Alangaden, G. J. & Chandrasekar, P. H. In-vitro activity of nikkomycin Z alone and in combination with polyenes, triazoles or echinocandins against Aspergillus fumigatus. Clin. MIcrobiol. Infect. 10, 961–966 (2004). 15521997 10.1111/j.1469-0691.2004.00996.x · DOI
- [50]Mouyna, I. et al. What are the functions of Chitin Deacetylases in Aspergillus fumigatus? Front. Cell. Infect. Microbiol. 10, 28 (2020). 32117802 10.3389/fcimb.2020.00028 PMC7016196 · DOI
- [51]Fernando, L. D. et al. Structural adaptation of fungal cell wall in hypersaline environment. Nat. Commun. 14, 7082 (2023). 37925437 10.1038/s41467-023-42693-6 PMC10625518 · DOI · Paper page
- [53]Kirui, A. et al. Carbohydrate-aromatic interface and molecular architecture of lignocellulose. Nat. Commun. 13, 538 (2022). 35087039 10.1038/s41467-022-28165-3 PMC8795156 · DOI · Paper page
- [54]Temple, H. et al. Golgi-localized putative S-adenosyl methionine transporters required for plant cell wall polysaccharide methylation. Nat. Plants 8, 656–669 (2022). 35681018 10.1038/s41477-022-01156-4 · DOI
- [55]Valsecchi, I. et al. The puzzling construction of the conidial outer layer of Aspergillus fumigatus. Cell Microbiol 21, e12994 (2019). 30552790 10.1111/cmi.12994 · DOI · Paper page
- [56]Fontaine, T. et al. Cell wall alpha1-3glucans induce the aggregation of germinating conidia of Aspergillus fumigatus. Fungal Genet. Biol. 47, 707–712 (2010). 20447463 10.1016/j.fgb.2010.04.006 · DOI · Paper page
- [57]Loussert, C. et al. In vivo biofilm composition of Aspergillus fumigatus. Cell Microbiol 12, 405–410 (2010). 19889082 10.1111/j.1462-5822.2009.01409.x · DOI · Paper page
- [58]Mouyna, I. et al. Glycosylphosphatidylinositol-anchored glucanosyltransferases play an active role in the biosynthesis of the fungal cell wall. J. Biol. Chem. 275, 14882–14889 (2000). 10809732 10.1074/jbc.275.20.14882 · DOI · Paper page
- [59]Gravelat, F. N. et al. Aspergillus galactosaminogalactan mediates adherence to host constituents and conceals hyphal β-glucan from the immune system. PLOS Pathog. 9, e1003575 (2013). 23990787 10.1371/journal.ppat.1003575 PMC3749958 · DOI · Paper page
- [60]Lamarre, C. et al. Galactofuranose attenuates cellular adhesion of Aspergillus fumigatus. Cell Microbiol 11, 1612–1623 (2009). 19563461 10.1111/j.1462-5822.2009.01352.x · DOI · Paper page
- [61]Aimanianda, V. et al. The dual activity responsible for the elongation and branching of β-(1,3)-Glucan in the fungal cell wall. mBio 8, 00619–00617 (2017). 10.1128/mBio.00619-17 PMC5478894 28634239 · DOI
- [64]Loiko, V. & Wagener, J. The paradoxical effect of echinocandins in Aspergillus fumigatus relies on recovery of the β-1, 3-glucan synthase Fks1. Antimicrob. Agents Chemother. 61, e01690–01616 (2017). 27872079 10.1128/AAC.01690-16 PMC5278722 · DOI · Paper page
- [65]Valero, C. et al. Caspofungin paradoxical effect is a Tolerant “Eagle Effect” in the filamentous fungal pathogen Aspergillus fumigatus. mBio 13, e0044722 (2022). 35420487 10.1128/mbio.00447-22 PMC9239232 · DOI · Paper page
- [66]Gonzalez-Jimenez, I., Perlin, D. S. & Shor, E. Reactive oxidant species induced by antifungal drugs: identity, origins, functions, and connection to stress-induced cell death. Front. Cell. Infect. Microbiol. 13, 1276406 (2023). 37900311 10.3389/fcimb.2023.1276406 PMC10602735 · DOI
- [67]Zhao, S. et al. Genomic and molecular identification of genes contributing to the Caspofungin Paradoxical effect in Aspergillus fumigatus. Microbiol. Spectr. 10, 00519–00522 (2022). 10.1128/spectrum.00519-22 PMC9603777 36094204 · DOI
- [68]Liu, Z. et al. Functional genomic and biochemical analysis reveals pleiotropic effect of Congo red on Aspergillus fumigatus. mBio 12, e00863–00821 (2021). 34006660 10.1128/mBio.00863-21 PMC8262895 · DOI
- [69]Widederhold, N. P., Locke, J. B., Daruwala, P. & Bartizal, K. Rezafungin (CD101) demonstrates potent in vitro activity against Aspergillus, including azole-resistant Aspergillus fumigatus isolates and cryptic species. J. Antimicrob. Chemother. 73, 3063–3067 (2018). 30032217 10.1093/jac/dky280 · DOI · Paper page
- [70]Shaw, K. J. & Ibrahim, A. S. Fosmanogepix: A review of the first-in-class broad spectrum agent for the treatment of invasive fungal infections. J. Fungi 6, 239 (2020). 10.3390/jof6040239 PMC7711534 33105672 · DOI · Paper page
- [71]Palliyil, S. et al. Monoclonal antibodies targeting surface-exposed Epitopes of Candida albicans cell wall proteins confer in vivo protection in an infection model. Antimicrob. Agents Chemother. 66, e0195721 (2022). 35285676 10.1128/aac.01957-21 PMC9017365 · DOI
- [72]Kirui, A. et al. Preparation of fungal and plant materials for structural elucidation using dynamic nuclear polarization solid-state NMR. J. Vis. Exp. 144, e59152 (2019). 30829332
- [73]Liu, Z. et al. Conidium specific polysaccharides in Aspergillus fumigatus. J. Fungi 9, 155 (2023). 10.3390/jof9020155 PMC9964227 36836270 · DOI
- [74]Johnson, S. B. & Brown, R. E. Simplified derivatization for determining sphingolipid fatty acyl composition by gas chromatography-mass spectrometry. J. Chromatogr. 605, 281–286 (1992). 1500464 10.1016/0021-9673(92)85248-R PMC4003555 · DOI
- [75]Rienstra, C. M. et al. De novo determination of peptide structure with solid-state magic-angle spinning NMR spectroscopy. Proc. Natl Acad. Sci. USA 99, 10260–10265 (2002). 12149447 10.1073/pnas.152346599 PMC124901 · DOI
- [76]Massiot, D. et al. Modelling one and two-dimensional solid-state NMR spectra. Magn. Reson. Chem. 40, 70–76 (2002). 10.1002/mrc.984 · DOI
- [77]Baldus, M., Petkova, A. T., Herzfeld, J. & Griffin, R. G. Cross polarization in the tilted frame: assignment and spectral simplification in heteronuclear spin systems. Mol. Phys. 95, 1197–1207 (1998). 10.1080/00268979809483251 · DOI
- [78]Ader, C. et al. Structural rearrangements of membrane proteins probed by water-edited solid-state NMR. Spectrosc. J. Am. Chem. Soc. 131, 170–176 (2009). 10.1021/ja806306e 19063626 · DOI · Paper page
- [79]White, P. B., Wang, T., Park, Y. B., Cosgrove, D. J. & Hong, M. Water–polysaccharide interactions in the primary cell wall of Arabidopsis thaliana from polarization transfer solid-state NMR. J. Am. Chem. Soc. 136, 10399–10409 (2014). 24984197 10.1021/ja504108h · DOI · Paper page
- [80]Helmus, J. J. & Jaroniec, C. P. Nmrglue: an open source Python package for the analysis of multidimensional NMR data. J. Biomol. NMR 55, 355–367 (2013). 23456039 10.1007/s10858-013-9718-x PMC3636164 · DOI
- [81]Hunter, J. D. Matplotlib: A 2D graphics environment. Comput Sci. Eng. 9, 90–95 (2007). 10.1109/MCSE.2007.55 · DOI · Paper page
- [82]Wang, T., Williams, J. K., Schmidt-Rohr, K. & Hong, M. Relaxation-compensated difference spin diffusion NMR for detecting 13 C–13 C long-range correlations in proteins and polysaccharides. J. Biomol. NMR 61, 97–107 (2015). 25510834 10.1007/s10858-014-9889-0 PMC4522165 · DOI
- [83]Sauvée, C. et al. Highly efficient, water‐soluble polarizing agents for dynamic nuclear polarization at high frequency. Angew. Chem. Int. Ed. 125, 11058–11061 (2013). 10.1002/ange.201304657 23956072 · DOI
- [84]Dubroca, T. et al. A quasi-optical and corrugated waveguide microwave transmission system for simultaneous dynamic nuclear polarization NMR on two separate 14.1 T spectrometers. J. Magn. Reson. 289, 35–44 (2018). 29459343 10.1016/j.jmr.2018.01.015 PMC5978701 · DOI
- [85]De Paëpe, G., Lewandowski, J. R., Loquet, A., Böckmann, A. & Griffin, R. G. Proton assisted recoupling and protein structure determination. J. Chem. Phys. 129, 12B615 (2008). 10.1063/1.3036928 PMC2755343 19123534 · DOI
- [86]Pauli, J., Baldus, M., van Rossum, B., de Groot, H. & Oschkinat, H. Backbone and Side-chain 13 C and 15 N signal assignments of the α-Spectrin SH3 domain by magic angle spinning solid-state NMR at 17.6 Tesla. ChemBioChem 2, 272–281 (2001). 11828455 10.1002/1439-7633(20010401)2:4<272::AID-CBIC272>3.0.CO;2-2 · DOI
- [87]Wang, T., Salazar, A., Zabotina, O. A. & Hong, M. Structure and dynamics of Brachypodium primary cell wall polysaccharides from two-dimensional 13 C solid-state nuclear magnetic Resonance Spectroscopy. Biochemistry 53, 2840–2854 (2014). 24720372 10.1021/bi500231b · DOI
- [88]Addison, B. et al. Atomistic, macromolecular model of the Populus secondary cell wall informed by solid-state NMR. Sci. Adv. 10, adi7965 (2024). 10.1126/sciadv.adi7965 PMC10776008 38170770 · DOI
- [89]Jo, S., Kim, T., Iyer, V. G. & Wonpil, I. CHARMM-GUI: A web-based graphical user interface for CHARMM. J. Comput. Chem. 29, 1859–1865 (2008). 18351591 10.1002/jcc.20945 · DOI · Paper page
- [90]Jo, S., Song, K. C., Desaire, H., MacKerell, A. D. & Im, W. Glycan reader: Automated sugar identification and simulation preparation for carbohydrates and glycoproteins. J. Comput. Chem. 32, 3135–3141 (2011). 21815173 10.1002/jcc.21886 PMC3188666 · DOI
- [92]Humphrey, W., Dalke, A. & Schulten, K. VMD: Visual. Mol. Dyn. J. Mol. Graph. 14, 33–38 (1996). 10.1016/0263-7855(96)00018-5 8744570 · DOI · Paper page
- [93]Rinaudo, M. Chitin and chitosan: Properties and applications. Prog. Polym. Sci. 31, 603–632 (2006). 10.1016/j.progpolymsci.2006.06.001 · DOI
- [94]Guvench, O., Hatcher, E., Venable, R. M., Pastor, R. W. & MacKerell, A. D. CHARMM additive all-atom force field for glycosidic linkages between Hexopyranoses. J. Chem. Theory Comput. 5, 2353–2370 (2009). 20161005 10.1021/ct900242e PMC2757763 · DOI
- [95]Guvench, O. et al. Additive empirical force field for hexopyranose monosaccharides. J. Comput. Chem. 29, 2543–2564 (2008). 18470966 10.1002/jcc.21004 PMC2882059 · DOI
- [96]Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W. & Klein, M. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926–935 (1983). 10.1063/1.445869 · DOI
- [97]Beglov, D. & Roux, B. Finite representation of an infinite bulk system: Solvent boundary potential for computer simulations. J. Chem. Phys. 100, 9050–9063 (1994). 10.1063/1.466711 · DOI
- [98]Essmann, U. et al. A smooth particle mesh Ewald method. J. Chem. Phys. 103, 8577–8593 (1995). 10.1063/1.470117 · DOI
- [99]Miyamoto, S. & Kollman, P. A. Settle: An analytical version of the SHAKE and RATTLE algorithm for rigid water models. J. Comput. Chem. 13, 952–962 (1992). 10.1002/jcc.540130805 · DOI
- [100]Paterlini, M. G. & Ferguson, D. M. Constant temperature simulations using the Langevin equation with velocity Verlet integration. Chem. Phys. 236, 243–252 (1998). 10.1016/S0301-0104(98)00214-6 · DOI
- [101]Feller, S. E., Zhang, Y., Pastor, R. W. & Brooks, B. R. Constant pressure molecular dynamics simulation: The Langevin piston method. J. Chem. Phys. 103, 4613–4621 (1995). 10.1063/1.470648 · DOI
- [103]Fiorin, G., Klein, M. L. & Henin, J. Using collective variables to drive molecular dynamics simulations. Mol. Phys. 111, 3345–3362 (2013). 10.1080/00268976.2013.813594 · DOI · Paper page
- [104]Latgé, J. P. & Chamilos, G. Aspergillus fumigatus and Aspergillosis in 2019. Clin. Microbiol. Rev. 33, e00140–00118 (2019). 31722890 10.1128/CMR.00140-18 PMC6860006 · DOI · Paper page
Cited by
Sorted by citations
Dickwella Widanage, M. C., Singh, K., Li, J., Yarava, J. R., Scott, F. J., Xu, Y., Gow, N. A. R., Mentink-Vigier, F., Wang, P., Lamoth, F., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-61678-1 · Cited by 51 · see citing works
Self-citation
- Authors
- Dickwella Widanage, M. C., Gautam, I., Sarkar, D., Mentink-Vigier, F., Vermaas, J. V., Ding, S.-Y., Lipton, A. S., Fontaine, T., Latgé, J.-P., Wang, P., & Wang, T.
- Affiliations
- Michigan State University (US)
- Pacific Northwest National Laboratory (US)
- Institut Pasteur (FR)
- University of Crete (GR)
- Louisiana State University Health Sciences Center New Orleans (US)
- Corresponding author
- Wang, Tuo
- ORCID
- Venue
- Nature Communications
- Published
- 2024-07-31
- Volume
- 15
- Issue
- 1
- Pages
- 6382-6382
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC11291495
- OpenAlex
- W4401184074
- Cited by
- 70
- References
- 11
- Citations by year
- 2026: 34 · 2025: 31 · 2024: 5
- FWCI
- 24.07
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by)
- OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- U.S. Department of Health & Human Services | National Institutes of Health (AI173270, R35GM155317)
- U.S. Department of Energy (DE-SC0019072)
- National Science Foundation (2321398)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Health Sciences › Medicine › Epidemiology › Fungal Infections and Studies
- Keywords
- Aspergillus fumigatus, echinocandins, antifungal resistance, β-1,3-glucan, chitin, chitosan, α-1,3-glucan, cell wall integrity, water permeability, drug permeation, antifungal tolerance
- MeSH terms
- Antifungal Agents, Aspergillus fumigatus, Cell Wall, Chitin, Glucans, Microbial Sensitivity Tests, Magnetic Resonance Spectroscopy, beta-Glucans, Chitosan, Echinocandins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review