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. 2021 Jan 4;11(2):1057-1065.
doi: 10.1039/d0ra08743b. eCollection 2020 Dec 24.

Analysis of the effects of Cu-MOFs on fungal cell inactivation

Mayura Veerana  1 , Hyun-Chul Kim  2 , Sarmistha Mitra  1 , Bishwa Chandra Adhikari  1 , Gyungsoon Park  1 , Seong Huh  2 , Sung-Jin Kim  3 , Youngmee Kim  3
Affiliations

Analysis of the effects of Cu-MOFs on fungal cell inactivation

Mayura Veerana et al. RSC Adv. .

Abstract

Three dimensional (3D) copper metal organic frameworks (Cu-MOFs) containing glutarates and bipyridyl ligands (bpa = 1,2-bis(4-pyridyl)ethane, bpe = 1,2-bis(4-pyridyl)ethylene, or bpp = 1,3-bis(4-pyridyl)propane) were synthesized by using previously reported hydrothermal reactions or a layering method. All three Cu-MOFs contained well-defined one dimensional (1D) channels with very similar pore shapes and different pore dimensions. The bulk purities of the Cu-MOFs were confirmed using powder X-ray diffraction (PXRD) and infrared spectroscopy (IR) spectra. When the three types of Cu-MOFs were applied to Candida albicans cells and Aspergillus niger spores, an average of about 50-80% inactivation was observed at the highest concentration of Cu-MOFs (2 mg mL-1). The efficiency of the fungal inactivation was not significantly different among the three different types (bpa, bpe, bpp). Treatment of the fungi using Cu-MOFs induced an apoptosis-like death and this was more severe in A. niger than C. albicans. This may be due to elevation of the intracellular level of reactive oxygen species (ROS) in A. niger. Generation of the reactive species in solution by Cu-MOFs was observed. However, there was a dramatic variation in the levels observed among the three types. Our results suggest that Cu-MOFs can produce antifungal effects and induce apoptosis-like death of the fungi, which was probably caused by the elevated level of intracellular reactive species.

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Conflict of interest statement

There are no conflicts to declare.

Figures

Scheme 1
Scheme 1. Chemical structures of glutaric acid, bpa, bpe, and bpp ligands.
Fig. 1
Fig. 1. 3D frameworks of MOF 1 (a), MOF 2 (b), and MOF 3 (c). Water solvent molecules have been omitted for clarity. Colour code: Cu: green; O: red; N: blue; C: grey; and H: white.
Fig. 2
Fig. 2. PXRD patterns of the Cu-MOFs: (a) MOF 1; (b) MOF 2; and (c) MOF 3; after 1 d and 4 d in water and 1× PBS solution.
Fig. 3
Fig. 3. Concentrations of CuII ions released from 1 mg of Cu-MOFs in 1 mL of PBS.
Fig. 4
Fig. 4. Antifungal activities of MOF 1 (a), MOF 2 (b) and MOF 3 (c) against C. albicans at different concentrations. The graphs on the left show the log scale CFU numbers for C. albicans in each treatment. The percentages shown in the graphs on the right were calculated as follows; (CFU number in each MOF treatment/CFU number for the control) x 100. Each bar represents the average and standard deviation of nine replicates. A Student's t-test was performed for the control and each treatment; *p < 0.05, **p < 0.01.
Fig. 5
Fig. 5. Antifungal activities of MOF 1 (a), MOF 2 (b) and MOF 3 (c) against A. niger in different concentrations. The graphs on the left show the log scale CFU numbers for A. niger in each treatment. The percentages shown in the graphs on the right were calculated as follows; (CFU number in each MOF treatment/CFU number of control) × 100. Each bar represents the average and standard deviations of nine replicates. A Student's t-test was performed for the control and each treatment; *p < 0.05, **p < 0.01.
Fig. 6
Fig. 6. TUNEL assay showing DNA fragmentation (as an indicator of apoptosis-like cell death) in C. albicans (a) and A. niger (b). (c) Transcription level of the metacaspase gene in C. albicans and A. niger treated with Cu-MOFs for 1 d. Each value is an average of three replicate measurements. A Student's t-test was performed for the control and each treatment; *p < 0.05, **p < 0.01.
Fig. 7
Fig. 7. Effect of Cu(NO3)2 and glutarate on the viability of C. albicans (a) and A. niger (b). Fungal cells were treated with Cu(NO3)2 or glutarate for 4 d. Each value represents an average of 18–27 replicates. A Student's t-test was performed on the control and each treatment; **p < 0.01.
Fig. 8
Fig. 8. Morphology of the C. albicans cells (a) and A. niger spores (b) after treatment with MOF 1, MOF 2 and MOF 3 for 4 d.
Fig. 9
Fig. 9. Level of ROS, RNS and lipid peroxidation. (a) Concentration of H2O2 and NOx in PBS 0 and 4 d after treatment with Cu-MOFs. Zoom-in graph of H2O2 level on 0 d was inserted. (b) Level of intracellular ROS and NO (nitric oxide) in C. albicans cells and A. niger spores after treatment with Cu-MOFs (2 mg mL−1) for 4 d. (c) Peroxidation of the membrane lipid in fungal cells after treatment with the Cu-MOFs for 4 d. Each value represents an average of six replicates. A Student's t-test was performed for the control and each treatment; *p < 0.05, **p < 0.01.
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