Home Journals Articles Updates About
CN
image
收藏切换
Red light-driven generation of reactive oxygen species for the targeted oxidation of glioma cells and thiols over covalent organic framework
收藏切换
PDF
Heng Wei1, Xia Li1, Fengwei Huang, Shujuan Wu, Huimin Ding, Qianxue Chen, Mingchang Li*, Xianjun Lang*
Chinese Chemical Letters | 2023, 34(12) : 108564
Less
收藏切换
Chinese Chemical Letters | 2023, 34(12): 108564
• Communication •
Red light-driven generation of reactive oxygen species for the targeted oxidation of glioma cells and thiols over covalent organic framework
Full
Heng Wei1, Xia Li1, Fengwei Huang, Shujuan Wu, Huimin Ding, Qianxue Chen, Mingchang Li*, Xianjun Lang*
Affiliations
  • Renmin Hospital of Wuhan University, College of Chemistry and Molecular Sciences, Wuhan University, Wuhan 430072, China
Published: 2023-12-15 doi: 10.1016/j.cclet.2023.108564
Outline
收藏切换

Reactive oxygen species (ROS) are essential for biological processes like cell signaling and chemical processes like organic oxidation. Moreover, the sufficient generation of ROS plays a significant role in targeted tumor treatments or oxidation of organics. Herein, a hydrazone-linked porphyrin covalent organic framework (Por-DETH-COF) is developed for red light-induced generation of ROS like singlet oxygen (1O2) or superoxide (O2•−) to undertake different but targeted oxidations. First, 1O2 is adopted in photodynamic therapy (PDT) for the oxidation of glioma cells. The PDT efficiency of Por-DETH-COF on the apoptosis of glioma cells is explored through flow cytometry and western blot assay. The apoptosis rate of glioma cells significantly increases over Por-DETH-COF under 660 nm red light illumination, suggestive of the potency of 1O2. Second, O2•− is employed for the targeted oxidation of thiols. A series of thiols could be efficiently oxidized to corresponding disulfides over Por-DETH-COF under 660 nm red light illumination, indicative of the significance of O2•−. This work highlights the potential of covalent organic frameworks in generating ROS for precise medical applications of complex chemical environments.

Reactive oxygen species  /  Covalent organic framework  /  Oxidation  /  Photodynamic therapy  /  Glioma cells
Heng Wei, Xia Li, Fengwei Huang, Shujuan Wu, Huimin Ding, Qianxue Chen, Mingchang Li, Xianjun Lang. Red light-driven generation of reactive oxygen species for the targeted oxidation of glioma cells and thiols over covalent organic framework[J]. Chinese Chemical Letters, 2023 , 34 (12) : 108564 - . DOI: 10.1016/j.cclet.2023.108564
Full Text
Less
Covalent organic frameworks (COFs) are an emerging type of porous organic materials with large specific surface areas, high crystallinity, low density, and good stability [1–6]. Besides, COFs, with excellent biocompatibility, have displayed enormous potential in biomedical applications [7–11]. Moreover, the exceptional light-harvesting capability and adjustable bandgaps of COFs provide them with remarkable efficiency for reactive oxygen species (ROS) generation, which has received considerable interest in photodynamic therapy (PDT) [12–19] and photocatalytic organic oxidations [20–22]. For instance, a corrole-based COF with evident absorption capability and high efficiency of singlet oxygen (1O2) generation has been proven to be outstanding in PDT [23]. Similarly, a glycosylated COF decorated with boron dipyrromethene (BODIPY) via post-synthetic modification has also displayed excellent performance in 1O2 generation, leading to notable antitumor effect on the colon tumor via the synergistic therapy of PDT and 1O2-triggered Ca2+ overload treatments [24]. Therefore, developing COFs in ROS-based PDT for tumor treatment is of great promise.
Generally, ROS consisting of oxygen-based free radicals and some non-radical derivatives of O2, such as superoxide (O2•–), 1O2, hydroxyl radical (•OH), and hydrogen peroxide (H2O2), are vital for life on Earth, which work as cell signaling molecules for normal biological processes [25–31]. However, excessive generation of ROS could provoke oxidative stress that induces cell death through autophagy, apoptosis, and other signal pathways, leading to uncountable pathologies [32–34]. It is now well-established that a subtle but dynamic balance exists between ROS generation and the antioxidant defenses that maintain the health of living organisms [35,36]. Due to oxidative damage toward cells, ROS could also play a significant role in tumor treatment. Diverse studies have focused on rapidly producing high levels of ROS at tumor sites to cause local peroxidation of tumor cells, thereby promoting ROS damage to DNA, lipid and protein peroxidation, and mitochondrial depolarization in tumors, eventually achieving the effect of killing tumor cells [37–42]. Among ROS-based therapy, PDT is an effective method based on oxidation reactions, which could convert tissue O2 into ROS by utilizing photosensitizers via light energy activation [43–47]. Compared with conventional therapy, PDT has numerous advantages over tumor treatment, including high tumor selectivity, low drug resistance, noninvasive nature, and devoid of side effects [48–52]. However, the therapeutic efficacy largely depends on the inherent capability to generate ROS.
To this end, the generation of ROS over photoactive COFs could be accomplished in a biocompatible environment without transition metals and heavy elements. Our recent study demonstrates that a porphyrin COF (Por-DETH-COF) is an excellent amplifier of O2•–, which could swiftly oxidize amines [53]. Nevertheless, the oxidation of amines proceeds via a nucleophilic attack pathway rather than direct oxidation. It would be more favorable to find direct and targeted oxidation for the generated ROS over Por-DETH-COF. Thiols are crucial components of many proteins and small molecules that play a vital role in maintaining redox homeostasis in living organisms [54,55]. Glutathione, the tripeptide thiol compound, is pervasive in cells of all organs, including the brain. Besides, glutathione is overexpressed in tumor chemical environments [56,57]. Therefore, the oxidation of thiol compounds is crucial in many biological processes [58]. Moreover, thiol compounds are highly reductive and could potentially impact the effectiveness of PDT, in which these thiol compounds are preferred to be partially eliminated. Fortunately, thiols could be directly oxidized by O2•− [59,60]. In addition, both 1O2 and O2•– can be simultaneously generated over COFs and specifically used in oxidations [61,62].
Herein, a hydrazone-linked porphyrin COF Por-DETH-COF is constructed based on p-Por-CHO (meso-tetrakis(4-formylphenyl)porphyrin) and DETH (2,5-diethoxyterephthalohydrazide). Por-DETH-COF is employed for the generation of 1O2 or O2•− to undertake different but targeted oxidations. First, 1O2 is adopted in PDT for glioma treatment. Glioma is the most common primary malignant tumor of adult human central nervous system, accounting for 80% of all tumors [63], which can significantly affect the immune system with avoided apoptosis, unlimited cell growth, and enhanced transfer ability. Due to the existence of the blood-brain barrier, it is often difficult for drugs to reach tumors through blood circulation and aggregate sufficient concentration to achieve local therapeutic function. The PDT efficiency of Por-DETH-COF is explored to induce the apoptosis of glioma cells through flow cytometry and western blot assay. The results reveal that the apoptosis rate of glioma cells significantly increases over Por-DETH-COF under red light illumination, influencing the expression level of proapoptotic and anti-apoptosis-related proteins. Second, O2•− is employed for the targeted oxidation of thiols. The photocatalytic oxidation of thiols is used to mimic the effects of the generation of ROS over Por-DETH-COF under complex chemical environments. The results indicate that a series of thiols could be efficiently transformed into corresponding disulfides under red light illumination, confirming that Por-DETH-COF is a brilliant platform for ROS generation. This work highlights the great potential of COFs in ROS-based PDT applications under complex chemical environments.
Por-DETH-COF was constructed with p-Por-CHO and DETH according to our prior work [53] with some modifications (Supporting information and Scheme S1). Subsequently, powder X-ray diffraction (PXRD) and Fourier transform infrared (FTIR) spectra were collected to prove the successful construction of Por-DETH-COF. The crystallinity of Por-DETH-COF was determined by PXRD (Fig. 1a). The diffracted peaks around 3.0° and 6.1° were ascribed to the (110) and (220) facets, respectively. Additionally, other weak diffraction peaks at 4.3°, 9.0°, and 22.0° further demonstrated good crystallinity. Furthermore, the experimental PXRD pattern of Por-DETH-COF matched well with the calculated diffraction pattern with AA eclipsed stacking model in the prior report [64]. The hump centered at ~22.0° is probably indexed to zigzag π–π stacking of 2D layers [65]. FTIR spectra (Fig. 1b) were also gathered to analyze the characteristic functionalities of Por-DETH-COF. Due to the establishment of hydrazone linkage, the FTIR spectrum of Por-DETH-COF emerged with peaks at 1665 cm−1 and 1201 cm−1. The observed band at around 3400 cm−1 was attributed to the −OH group of adsorbed water on Por-DETH-COF.
Next, the construction of Por-DETH-COF was identified by solid-state 13C nuclear magnetic resonance (NMR) spectroscopy. The 13C resonance signal at ~162 ppm (marked 1) might be assigned to the hydrazone bond (Fig. 2a). The resonance signal at ~150 ppm (marked 2) was probably ascribed to the carbon of the C=N bond. The permanent porosity of the Por-DETH-COF was assessed by N2 sorption analysis at 77 K, demonstrating a Brunauer–Emmett–Teller (BET) specific surface area of 925 m2/g and a pore volume of 0.517 cm3/g (Fig. 2b). The high specific surface area and large pore volume are conducive to the generation and diffusion of ROS over Por-DETH-COF, offering a brilliant platform for targeted oxidations.
Using scanning electron microscopy (SEM) and transmission electron microscopy (TEM), the morphology of Por-DETF-COF was investigated (Figs. 3a and b). Por-DETF-COF was composed of stacked and interwoven network structures. The solid-state UV–visible spectrum of Por-DETH-COF exhibited a wide absorption edge around 400–700 nm (Fig. 4a). Based on the Kubelka–Munk function, the bandgap (Eg) of Por-DETH-COF was roughly estimated at 1.75 eV from the absorption edge (Fig. 4b). In principle, the Eg of Por-DETH-COF is narrow enough to efficiently harvest visible light. Namely, it is well-founded to realize red light-induced generation of ROS over Por-DETH-COF. Red light is essential for biomedical applications because it can penetrate cells more efficiently.
The electron paramagnetic resonance (EPR) spectra of Por-DETH-COF were collected. Compellingly, Por-DETH-COF is a brilliant platform for ROS generation. According to EPR results (Fig. 4c), the signal of 1O2 trapped by 2,2,6,6-tetramethyl-4-piperidone (TMPD) was generated and enhanced with red light illumination, implying that 1O2 is produced under red light illumination through an energy transfer pathway [66]. Moreover, the production of O2•− was also confirmed, whose EPR signal was displayed by 5,5-dimethyl-1-pyrroline N-oxide (DMPO). The signal of DMPO-O2•– adducts was noticeable under red light illumination and increased with time of illumination (Fig. 4d), which evidences the efficient generation of O2•−. By and large, two types of ROS, namely 1O2 and O2•−, could be sufficiently generated over Por-DETH-COF under 660 nm red light illumination.
After confirming the capability of ROS generation over Por-DETH-COF, the generated 1O2 over Por-DETH-COF was applied in tumor treatments. Glioma cells were first taken as the targeted oxidation over Por-DETH-COF. The GBM cell lines (U87) were purchased from the American Type Culture Collection (ATCC). These cells were cultured at 37 ℃ with 5% CO2 in Dulbecco's modified Eagle's medium, 10% fetal bovine serum (Gibco), and 1% penicillin/streptomycin (4 mg/mL; Sigma Aldrich). Experiments were conducted at a cell density of 70%–80%. Antibodies against B-cell lymphoma-2 (Bcl-2), Bcl-2-Associated X (Bax), Cleaved Caspase-3 (CC3), and glyceral-dehyde-3-phosphate dehydrogenase (GAPDH) were purchased from Cell Signaling Technology (Beverly, USA). Glioma cells and red light-emitting diodes (LEDs) (λ = 660 ± 8 nm) were used as target object and light source, respectively. Flow cytometry showed the effect of red light illumination over Por-DETH-COF on the apoptosis of glioma cells. The results showed that after adding Por-DETH-COF to the sample along with illumination of red light for 24 h, the apoptosis rate of glioma cells significantly increased in light + Por-DETH-COF group, which is substantially higher than that of the control group, light group, and Por-DETH-COF group (P < 0.05). The apoptosis rate slightly increased in the light group and the Por-DETH-COF group compared with the control group (Figs. 5a and b).
In addition, western blot assay was used to detect the expression level of glioma-related proteins. Western blot analysis was performed as described in Supporting information. It showed that compared with the control group, light group, and Por-DETH-COF group, the expression level of proapoptotic-related proteins Bax and CC3 was significantly increased, while the expression level of anti-apoptosis-related protein Bcl-2 was considerably suppressed in light + Por-DETH-COF group (Figs. 5c and d). Meanwhile, only a slight increase in apoptosis was observed in the light group and the Por-DETH-COF group. The Western blot results showed that Por-DETH-COF under red light illumination could significantly induce the apoptosis of glioma cells and inhibit the growth of glioma cells, which is consistent with flow cytometry results. However, one should not take it for granted that the apoptosis of glioma cells was solely caused by PDT of 1O2 over Por-DETH-COF. Glioma cells live alongside complex cellular chemical environments, which could impact the effectiveness of ROS.
Next, Por-DETH-COF was then applied to the targeted oxidation of thiols. Notably, the red light-induced oxidation of 4-methoxybenzenethiol smoothly occurred in an atmosphere of O2 (Fig. 6, bar a). Additionally, the production of disulfide was also possible under air (Fig. 6, bar b). In comparison, the yield of disulfide benefited from the improved O2 pressure. As observed, it was practical but less effective when C2H5OH was replaced by CH3OH or CH3CN (Fig. 6, bars c and d). Moreover, the functions of the rest components of the system were also studied. Under comparable conditions, self-oxidation under red light illumination could not be completed when only 4-methoxybenzenethiol existed (Fig. 6, bar e). In contrast to the experiment performed in the dark, where no products were formed, thiol conversion equally did not occur when O2 was removed by N2 (Fig. 6, bars f and g). Por-DETH-COF, O2, and light source were all essential for this system, confirming the suspicions that the oxidation is induced by activating O2 to proper ROS over Por-DETH-COF under red light illumination. Deutered solvent could prolong the lifetime of 1O2, which in turn could improve the conversion. Notwithstanding, the photocatalytic conversion of 4-methoxybenzenethiol was not improved when C2H5OH was replaced by C2D5OD, suggesting that 1O2 does not partake in the oxidation of thiol and O2•− is the pivotal ROS.
To verify the universality, a series of thiols were investigated as the substrates for photocatalytic oxidation over Por-DETH-COF (Table 1). In comparison with benzenethiol, electron-donating derivatives were smoothly converted into corresponding disulfides with less reaction time (Table 1, entries 1–4). As for electron-withdrawing groups like −F, −Cl, and −Br substituted thiols, the rate of transformation was comparable to that of benzenethiol (Table 1, entries 7–9). However, 4-(trifluoromethyl)benzenethiol suffered from decreased conversion for the stronger electron-withdrawing effect of −CF3 (Table 1, entry 10). For comparison, the performances of the same substituent (−OCH3) at different positions on targeted oxidation of thiols were displayed (Table 1, entries 4–6). It was shown that the steric effect could partly inhibit the effective conversion of thiols. Under red light illumination, Por-DETH-COF induced the efficient conversion of various thiols and enabled the generation of disulfides with O2•−.
Eventually, a mechanism for the targeted oxidation of benzenethiol over Por-DETH-COF is proposed in Fig. 7. Initially, Por-DETH-COF is excited by red light illumination, resulting in the separation of electron (e−) and hole (h+). Then e− combines with O2 to generate O2•−. Benzenethiol is activated by O2•− and converted to a sulfur-centered radical. The sulfur-centered radical couples with another benzenethiol, forming a disulfide and releasing hydrogen radical (H•). For the steady generation of O2•−, the h+ should be partially quenched by H• to release H+. The released H+ reacts with the O2•–, which is eventually converted to H2O2.
In summary, Por-DETH-COF has been successfully developed as a platform for ROS generation to undertake targeted oxidations. Firstly, the PDT efficiency of the generated 1O2 over Por-DETH-COF was explored on the apoptosis of glioma cells through flow cytometry and western blot assay. The results revealed that Por-DETH-COF significantly increased the apoptosis rate of glioma cells under red light illumination by influencing the expression level of proapoptotic and anti-apoptosis-related proteins. Second, the effectiveness of the afforded O2•− over Por-DETH-COF was assessed by the photocatalytic oxidation of thiols. A series of thiols could be efficiently transformed into corresponding disulfides under red light illumination. Overall, Por-DETH-COF is a brilliant platform for ROS generation. This work highlights the great potential of COFs in generating ROS for precise medical applications of complex chemical environments.
Declaration of competing interest
Less
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgment
Less
This work was supported by the National Natural Science Foundation of China (No. 22072108). We also acknowledge the Core Facility of Wuhan University for materials characterizations.
Supplementary materials
Less
Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.cclet.2023.108564.
References
Less
[1]
T. Zhang, G. Zhang, L. Chen, Acc. Chem. Res. 55 (2022) 795–808.
[2]
Y.F. Zhi, P.P. Shao, X. Feng, et al., J. Mater. Chem. A 6 (2018) 374–382.
[3]
L.P. Guo, J. Zhang, Q. Huang, et al., Chin. Chem. Lett. 33 (2022) 2856–2866.
[4]
S.H. Wu, Y. Pan, H. Lin, et al., ChemSusChem 14 (2021) 4958–4972.
[5]
H.X. Lin, C.P. Chen, T.H. Zhou, et al., Sol. RRL 2 (2021) 2000458.
[6]
Y. Xie, Y.L. Chen, X. Sun, et al., Chin. Chem. Lett. 32 (2021) 2061–2065.
[7]
S.M. Li, J. Zou, L.F. Tan, et al., Chem. Eng. J. 446 (2022) 137148.
[8]
S. Bhunia, K.A. Deo, A.K. Gaharwar, Adv. Funct. Mater. 30 (2020) 2002046.
[9]
Y.L. Zheng, S.N. Zhang, J.B. Guo, et al., Angew. Chem. Int. Ed. 61 (2022) e202208744.
[10]
Q. Sun, B. Aguila, P.C. Lan, et al., Adv. Mater. 31 (2019) 1900008.
[11]
G.Y. Zhang, X.L. Li, Q.B. Liao, et al., Nat. Commun. 9 (2018) 2785.
[12]
J. Tian, B.X. Huang, M.H. Nawaz, et al., Coord. Chem. Rev. 420 (2020) 213410.
[13]
D.W. Wang, Z. Zhang, L. Lin, et al., Biomaterials 223 (2019) 119459.
[14]
F. Lu, L.M. Pan, T. Wu, et al., Chem. Commun. 58 (2022) 11013–11016.
[15]
L. Zhang, Y. Xiao, Q.C. Yang, et al., Adv. Funct. Mater. 32 (2022) 2201542.
[16]
A.R. Bagheri, C.J. Li, X.L. Zhang, et al., Biomater. Sci. 9 (2021) 5745–5761.
[17]
S.N. Liu, Z.D. Liu, Q. Meng, et al., ACS Appl. Mater. Interfaces 13 (2021) 56873–56880.
[18]
P. Gao, M.Z. Wang, Y.Y. Chen, et al., Chem. Sci. 11 (2020) 6882–6888.
[19]
S. Chen, T.T. Sun, M. Zheng, et al., Adv. Funct. Mater. 30 (2020) 2004680.
[20]
H.M. Hao, F.L. Zhang, X.Y. Dong, et al., Appl. Catal. B 299 (2021) 120691.
[21]
X. Li, S.X. Yang, F.L. Zhang, et al., Appl. Catal. B 303 (2022) 120846.
[22]
J.Y. Guo, D.G. Ma, F.L. Sun, et al., Sci. China Chem. 65 (2022) 1704–1709.
[23]
Y.M. Zhao, W.H. Dai, Y.L. Peng, et al., Angew. Chem. Int. Ed. 59 (2020) 4354–4359.
[24]
Q. Guan, L.L. Zhou, F.H. Lv, et al., Angew. Chem. Int. Ed. 59 (2020) 18042–18047.
[25]
R.P. Ostrowski, E.B. Pucko, Neurochem. Int. 154 (2022) 105281.
[26]
S. Liu, L. Dong, W. Shi, et al., Front. Pharmacol. 13 (2022) 921070.
[27]
S. George, M.R. Hamblin, H. Abrahamse, J. Photochem. Photobiol. B 188 (2018) 60–68.
[28]
K.B. Mollers, H. Mikkelsen, T.I. Simonsen, et al., Carbohydr. Res. 448 (2017) 182–186.
[29]
X.X. Ren, H. Liu, X.M. Wu, et al., Front. Bioeng. Biotechnol. 9 (2022) 820468.
[30]
L. Luo, T.T. Zhang, M. Wang, et al., ChemSusChem 13 (2020) 5173–5184.
[31]
H. Li, X. Li, J. Zhou, et al., Chin. Chem. Lett. 33 (2022) 3733–3738.
[32]
B.W. Yang, Y. Chen, J.L. Shi, Chem. Rev. 119 (2019) 4881–4985.
[33]
H. Sies, D.P. Jones, Nat. Rev. Mol. Cell Biol. 21 (2020) 363–383.
[34]
B.M. Scavuzzi, J. Holoshitz, Antioxidants 11 (2022) 1306.
[35]
X.Q. Hu, D.L. Dong, M.H. Xia, et al., New J. Chem. 44 (2020) 11405–11419.
[36]
T. Liu, L. Sun, Y.B. Zhang, et al., J. Biochem. Mol. Toxicol. 36 (2022) e22942.
[37]
M. Ismail, W. Yang, Y. Li, et al., Biomaterials 289 (2022) 121760.
[38]
S.Y. Liu, Z.L. Zhong, C.W. Zhang, et al., Nanoscale Adv. 4 (2022) 894–903.
[39]
A. Xie, H. Li, Y.M. Hao, et al., Nanoscale Res. Lett. 16 (2021) 142.
[40]
Q. Guan, L.L. Zhou, Y.A. Li, et al., ACS Nano 13 (2019) 13304–13316.
[41]
Z.J. Zhang, L. Wang, W.X. Liu, et al., Natl. Sci. Rev. 8 (2021) nwaa155.
[42]
S. Malekkhaiat Häffner, E. Parra-Ortiz, M.W.A. Skoda, et al., J. Colloid Interface Sci. 584 (2021) 19–33.
[43]
Y. Nosaka, A.Y. Nosaka, Chem. Rev. 117 (2017) 11302–11336.
[44]
F.M. Wei, T.W. Rees, X.X. Liao, et al., Coord. Chem. Rev. 432 (2021) 213714.
[45]
H. Huang, W. Feng, Y. Chen, Chem. Soc. Rev. 50 (2021) 11381–11485.
[46]
W.H. Sun, Y.G. Xiang, Z.H. Jiang, et al., Sci. Bull. 67 (2022) 61–70.
[47]
Y.C. Zhang, L. She, Z.Y. Xu, et al., Chin. Chem. Lett. 33 (2022) 3277–3280.
[48]
M.Y. Yang, T. Yang, C.B. Mao, Angew. Chem. Int. Ed. 58 (2019) 14066–14080.
[49]
M. Pan, Q.Y. Jiang, J.L. Sun, et al., Angew. Chem. Int. Ed. 59 (2020) 1897–1905.
[50]
X.J. He, B. Situ, M. Gao, et al., Small 15 (2019) 1905080.
[51]
L.G. Yu, Q. Wang, R.C.H. Wong, et al., Dyes Pigm. 163 (2019) 197–203.
[52]
C.L. Wu, Y.Y. Li, Z.H. Cheng, et al., Chin. Chem. Lett. 33 (2022) 4339–4344.
[53]
S.J. Wu, Y.F. Zhang, H.M. Ding, et al., J. Colloid Interface Sci. 610 (2022) 446–454.
[54]
Y.L. Luo, B. Cao, M.J. Zhong, et al., Angew. Chem. Int. Ed. 61 (2022) e2022126.
[55]
C.H. Foyer, Environ. Exp. Bot. 154 (2018) 134–142.
[56]
L.L. Feng, B. Liu, R. Xie, et al., Adv. Funct. Mater. 31 (2021) 2006216.
[57]
H.J. Zhang, R.L. Han, P.X. Song, et al., J. Colloid Interface Sci. 629 (2023) 103–113.
[58]
D. Schilter, Nat. Rev. Chem. 1 (2017) 0013.
[59]
H. Xu, Y.F. Zhang, X.J. Lang, Chin. Chem. Lett. 31 (2020) 1520–1524.
[60]
X.B. Li, Z.J. Li, Y.J. Gao, et al., Angew. Chem. Int. Ed. 53 (2014) 2085–2089.
[61]
F.L. Zhang, X.M. Ma, X.Y. Dong, et al., Chem. Eng. J. 451 (2023) 138802.
[62]
S.X. Yang, X. Li, Y. Qin, et al., ACS Appl. Mater. Interfaces 13 (2021) 29471–29481.
[63]
Q.T. Ostrom, L. Bauchet, F.G. Davis, et al., Neuro-oncology 16 (2014) 896–913.
[64]
R.F. Chen, Y. Wang, Y. Ma, et al., Nat. Commun. 12 (2021) 1354.
[65]
Z.X. Lu, Y.X. Liu, X.L. Liu, et al., J. Mater. Chem. B 7 (2019) 1469–1474.
[66]
Y.J. Fu, M. Tan, Z.L. Guo, et al., Chem. Eng. J. 452 (2023) 139417.
Appendix
Less
Year 2023 volume 34 Issue 12
PDF
40
22
Cite this Article
BibTeX
Article Info
doi: 10.1016/j.cclet.2023.108564
  • Receive Date：2023-01-08
  • Online Date：2025-11-21
  • Published：2023-12-15
Article Data
Affiliations
History
  • Received：2023-01-08
  • Revised：2023-05-08
  • Accepted：2023-05-10
Affiliations
    Renmin Hospital of Wuhan University, College of Chemistry and Molecular Sciences, Wuhan University, Wuhan 430072, China
References
Share
https://castjournals.cast.org.cn/joweb/ccl/EN/10.1016/j.cclet.2023.108564
Share to
QR

Scan QR to access full text

Cite this article
BibTeX
Citations
表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
关闭全屏
  • BibTeX
  • EndNote
  • RefWorks
  • TxT
Links
Articles
Latest Articles
Most Read
Collections
Updates
Events
News
Multimedia
About
About Us
Contact
No. 86 Xueyuan South Road, Haidian District, Beijing
100081
010-62199257
qkjq@cast.org.cn

Copyright © 2025 China Association for Science and Technology. All rights reserved. For all open access content, the relevant licensing terms apply.
Sponsored by the Office of the Leading Group for Cybersecurity and Informatization of CAST, and supported by Science and Technology Review Publishing House