Cited by 70Antifungal resistance and susceptibilityFungal and yeast genetics researchFungal Infections and Studies

Adaptative survival of Aspergillus fumigatus to echinocandins arises from cell wall remodeling beyond β−1,3-glucan synthesis inhibition

Open access
Dickwella Widanage, Malitha C., Gautam, Isha, Sarkar, Daipayan, Mentink-Vigier, Frederic, Vermaas, Josh V., Ding, Shi-You, Lipton, Andrew S., Fontaine, Thierry +3 more·2024·Nature Communications

Published 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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41467-024-50799-8

Cites

11 of 11 references verified0 citation errors · 0 not checkable

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.

A few free checks a day · papers already verified open instantly · results are public

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 measured
  • The 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.”

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

Flagged first, then by citations

Research works printed but not linked: 94

  1. [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. [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
  3. [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
  4. [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
  5. [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
  6. [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
  7. [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
  8. [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
  9. [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
  10. [12]SC, D. & Stevens, D. A. Caspofungin. Clin. Infect. Dis. 36, 1445–1457 (2003). 12766841 10.1086/375080 · DOI
  11. [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
  12. [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
  13. [16]Latgé, J. P. The pathobiology of Aspergillus fumigatus. Trends Microbiol. 9, 382–389 (2001). 11514221 10.1016/S0966-842X(01)02104-7 · DOI
  14. [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
  15. [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
  16. [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
  17. [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
  18. [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
  19. [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
  20. [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
  21. [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
  22. [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
  23. [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
  24. [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
  25. [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
  26. [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
  27. [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
  28. [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
  29. [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
  30. [35]Ni, Q. Z. et al. High frequency dynamic nuclear polarization. Acc. Chem. Res. 46, 1933–1941 (2013). 23597038 10.1021/ar300348n PMC3778063 · DOI
  31. [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
  32. [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
  33. [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
  34. [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
  35. [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
  36. [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
  37. [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
  38. [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
  39. [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
  40. [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
  41. [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
  42. [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
  43. [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
  44. [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
  45. [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
  46. [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
  47. [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
  48. [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
  49. [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
  50. [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
  51. [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
  52. [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
  53. [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
  54. [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
  55. [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
  56. [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
  57. [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
  58. [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
  59. [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
  60. [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
  61. [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
  62. [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
  63. [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
  64. [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
  65. [73]Liu, Z. et al. Conidium specific polysaccharides in Aspergillus fumigatus. J. Fungi 9, 155 (2023). 10.3390/jof9020155 PMC9964227 36836270 · DOI
  66. [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
  67. [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
  68. [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
  69. [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
  70. [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
  71. [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
  72. [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
  73. [81]Hunter, J. D. Matplotlib: A 2D graphics environment. Comput Sci. Eng. 9, 90–95 (2007). 10.1109/MCSE.2007.55 · DOI · Paper page
  74. [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
  75. [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
  76. [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
  77. [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
  78. [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
  79. [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
  80. [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
  81. [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
  82. [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
  83. [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
  84. [93]Rinaudo, M. Chitin and chitosan: Properties and applications. Prog. Polym. Sci. 31, 603–632 (2006). 10.1016/j.progpolymsci.2006.06.001 · DOI
  85. [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
  86. [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
  87. [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
  88. [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
  89. [98]Essmann, U. et al. A smooth particle mesh Ewald method. J. Chem. Phys. 103, 8577–8593 (1995). 10.1063/1.470117 · DOI
  90. [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
  91. [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
  92. [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
  93. [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
  94. [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

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
Venue
Nature Communications
Published
2024-07-31
Volume
15
Issue
1
Pages
6382-6382
ISSN
2041-1723 (ISSN-L)
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
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