Enzyme-Like MetalâOrganic Frameworks in Polymeric Membranes for

Subscriber access provided by UNIV OF SOUTHERN INDIANA

Biological and Medical Applications of Materials and Interfaces

Enzyme-like Metal-Organic Frameworks in Polymeric Membrane for Efficient Removal of Aflatoxin B1 Zhongyuan Ren, Jianquan Luo, and Yinhua Wan ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.9b08011 • Publication Date (Web): 31 Jul 2019 Downloaded from pubs.acs.org on July 31, 2019

Just Accepted “Just Accepted” manuscripts have been peer-reviewed and accepted for publication. They are posted online prior to technical editing, formatting for publication and author proofing. The American Chemical Society provides “Just Accepted” as a service to the research community to expedite the dissemination of scientific material as soon as possible after acceptance. “Just Accepted” manuscripts appear in full in PDF format accompanied by an HTML abstract. “Just Accepted” manuscripts have been fully peer reviewed, but should not be considered the official version of record. They are citable by the Digital Object Identifier (DOI®). “Just Accepted” is an optional service offered to authors. Therefore, the “Just Accepted” Web site may not include all articles that will be published in the journal. After a manuscript is technically edited and formatted, it will be removed from the “Just Accepted” Web site and published as an ASAP article. Note that technical editing may introduce minor changes to the manuscript text and/or graphics which could affect content, and all legal disclaimers and ethical guidelines that apply to the journal pertain. ACS cannot be held responsible for errors or consequences arising from the use of information contained in these “Just Accepted” manuscripts.

is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Published by American Chemical Society. Copyright © American Chemical Society. However, no copyright claim is made to original U.S. Government works, or works produced by employees of any Commonwealth realm Crown government in the course of their duties.

Page 1 of 38 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ACS Applied Materials & Interfaces

1

Enzyme-Like Metal-Organic Frameworks in

2

Polymeric Membrane for Efficient Removal of

3

Aflatoxin B1

4

Zhongyuan Ren,†,‡ Jianquan Luo,*,†,‡ Yinhua Wan*,†,‡

5

†State

6

7

Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences, Beijing 100190, PR China

‡School

of Chemical Engineering, University of Chinese Academy of Sciences, Beijing

8

100049, PR China

9

KEYWORDS: metal-organic framework, biomimetic catalysis, membrane, aflatoxin,

10

peroxidase, degradation, detoxification

11

ABSTRACT. Biodegradation is a mild and efficient way to protect humans and animals

12

from mycotoxins. However, microbes and enzymes are susceptible to environmental

ACS Paragon Plus Environment

1

ACS Applied Materials & Interfaces 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Page 2 of 38

13

change, lack of stability and reusability. In this work, three peroxidase-like metal-organic

14

frameworks (MOFs), as artificial substitutes of natural peroxidase, are used for aflatoxin

15

B1 (AFB1) removal, demonstrating strong removal ability for AFB1 and anti-interference

16

ability towards other substances. There are distinct adsorption and catalytic properties

17

among those MOFs that are mainly due to the differences in structure and Fe ion active

18

sites. Then we immobilized those MOFs into ultrafiltration membranes to form a

19

multifunctional membrane (i.e., filtration, adsorption and catalysis) for AFB1 removal with

20

good reusability that can be operated in simultaneous adsorption/catalysis or adsorption

21

followed by catalysis/regeneration modes. Physicochemical analysis and animal

22

experiments showed that the degradation products are probably several low-carbon

23

substances whose toxic groups are cleaved.

24

1. INTRODUCTION

25

Mycotoxins are metabolites produced by fungi in mouldy food that are toxic and

26

carcinogenic to animals and humans.1-2 Aflatoxin B1 (AFB1), as the most toxic

27

mycotoxin, has strong chemical and thermal stability.3 Biodegradation is a mild and


2

Page 3 of 38 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


28

efficient strategy for AFB1 degradation.4 However, some inherent defects lead to many

29

difficulties in application. Microbes and enzymes are always susceptible to

30

environmental change, lack of stability, difficulty of reuse and, in a sense, cost. In recent

31

years, varieties of biomimetic materials, such as metal/metallic oxide nanoparticles and

32

supramolecular compounds, have emerged as potential alternatives to microbes and

33

enzymes that have been successfully applied in biosensing,5 pharmacy,6 energy,7

34

biology and green chemistry.8-9 Metal-organic frameworks (MOFs), as a new class of

35

porous inorganic-organic hybrid materials, has been used for air and water purification

36

by adsorption or separation in free or fixed states, like nanofibrous membrane.10-12

37

Moreover, two strategies are generally used to construct MOFs-based enzymes. One is

38

to encapsulate natural enzymes in pores or shells of MOFs.13-16 This method can

39

greatly improve the stability of enzymes. The role of MOFs, however, is merely a carrier

40

or a barrier in which natural enzymes are indispensable. The other is to function as a

41

mimetic enzyme itself without the addition of natural catalyst.17-19 Zhang et al. reported

42

that two Fe(III)-based MOFs, MIL-100 and MIL-68, showed peroxidase-like catalytic

43

activity to work as colorimetric biosensing platforms.20 Other Fe-containing MOFs, such


3


Page 4 of 38

44

as MIL-53,21 MIL-68-NH2,22 PCN-22223 and PCN-600,24 are also applied to similar

45

sensing applications. However, this enzyme-like characteristic of MOFs is rarely applied

46

to aqueous mycotoxin removal through either adsorption or catalysis. Replacing

47

enzymes and other biocatalysts with artificial biomimetic catalysts under mild conditions

48

for mycotoxin degradation still remains an arduous challenge.

49

In this work, considering the similarity of active site and the cost, we choose Fe-based

50

MOFs as peroxidase mimics to remove AFB1 from water for the first time. Interestingly,

51

we find that three different Fe-based MOFs, MIL-100, MIL-53 and MIL-68, have distinct

52

adsorption and catalytic capacities to AFB1, although all of those MOFs show

53

remarkable AFB1 removal efficiency compared with horseradish peroxidase. The

54

sequence of adsorption capacity is: MIL-68 > MIL-100 > MIL-53, while the order of

55

apparent catalysis ability is reversed. These distinct properties of the MOFs are taken

56

advantage of for different applications. “Weak-adsorption” MIL-53 is used for AFB1

57

degradation to define the total toxicity of the catalysed products by animal

58

experimentation. “Strong-adsorption” MIL-100 is employed in “adsorption followed by

59

catalysis/regeneration” mode to create an H2O2-free condition during AFB1 removal in


4

Page 5 of 38 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


60

food. We provide a complete set of artificial “weapons” (peroxidase-like MOFs), “support

61

equipment” (corresponding membranes) and “strategies” (two operating modes) to fight

62

“enemies” (mycotoxins).

63 64

2. EXPERIMENTAL SECTION

65

2.1. Materials. 1,3,5-benzenetricarboxylic acid (H3BTC, 98%), polyethyleneimine (PEI,

66

Mw = 600), starch from corn, α-cellulose, and corn oil were obtained from Aladdin

67

(Shanghai, China). Iron (III) chloride hexahydrate (FeCl3·6H2O, 99%) was obtained from

68

Xilong (Guangdong, China). Iron powder (99%, 300 mesh) and zein from corn were

69

purchased from Macklin (Shanghai, China). Dopamine hydrochloride (DA·HCl) and

70

peroxidase (150 U mg-1, from horseradish) were purchased from Sigma-Aldrich (USA).

71

Aflatoxin B1 (AFB1) from aspergillus flavus was purchased from J&K (Beijing, China).

72

1,4-benzenedicarboxylic acid (H2BDC, 99%) was supplied by Sinopharm (China). Other

73

reagents that were not mentioned here were supplied by Beijing Chemical Works

74

(Beijing, China). All chemicals were used as received without further purification.


5


Page 6 of 38

75

Amicon stirred cells (Millipore Corporation, USA) with total volumes of 50 mL and

76

effective areas of 13.4 cm2 were used to fabricate membranes and test their

77

performance. PAN membrane, PAN350, which has a polyacrylonitrile separation layer

78

and polyester non-woven fabric support with molecular weight cut-off (MWCO) of 20

79

kDa was purchased from Sepro Membranes, Inc. (USA).

80

2.2. Preparation of peroxidase-like MOFs. MIL-100,25 MIL-5321 and MIL-6820 are

81

synthesized by a hydrothermal/solvothermal method with little modification. For MIL-

82

100, 0.2775 g Fe0 powder and 0.6875 g H3BTC were added into 20 mL deionized water.

83

Then, 175 μL HF and 190 μL HNO3 were added and treated by ultrasound for 10 min.

84

The mixture was heated at 150 °C for 12 h and cooled at room temperature. After

85

washing with hot water and ethanol, MIL-100 powder was obtained by centrifugation

86

and vacuum drying at 60 °C. For MIL-53, 1.3515 g FeCl3·6H2O and 0.8305 g H2BDC

87

were added into 25 mL N,N-dimethylformamide (DMF) and treated by ultrasound for 10

88

min. The solution was then heated at 150 °C for 6 h and naturally cooled to room

89

temperature. The obtained solid was washed with DMF and a large amount of ultrapure

90

water, followed by drying at room temperature. For MIL-68, 0.6480 g FeCl3·6H2O and


6

Page 7 of 38 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


91

0.7980 g H3BTC were added into 24 mL DMF. Then, 240 μL HF (5 M) and 240 μL HCl

92

(1 M) were added and ultrasonically treated for 10 min. The mixture was heated at 100

93

°C for 5 days and cooled at room temperature. After washing with water and acetone,

94

the solid was obtained by centrifugation and vacuum drying at 60 °C.

95

2.3. Preparation of peroxidase-like MOFs-loaded membrane. A facile and fast method

96

has been used to immobilize MOFs in PAN membrane, based on our previous work

97

with improvement.26 The pristine membrane was first immersed in 50% ethanol for 3

98

min, and then in water overnight, to remove the protective agent residue. Then, the

99

membrane was installed in an Amicon stirred cell under reverse mode (with the support

100

layer facing feed and an extra non-woven fabric support beneath the skin layer). After

101

adding a MOFs dispersion into deionized water (100 mL) and sonicating (50 W, below

102

35 °C) for 60 min, the resulting uniform suspension, containing 7.0 mg MOFs, was

103

filtered through the membrane with 150 rpm agitation under 0.06 bar. The MOFs-loaded

104

membrane was then fiercely washed with buffer to remove unstable MOFs on the

105

surface of the support layer. Tris-HCl buffer (10 mL, pH=8.5, 20 mM) containing DA·HCl

106

(20 mg) and PEI (20 mg, MW = 600) was poured upon the membrane and stirred for 4


7


Page 8 of 38

107

min to rapidly form a polydopamine-PEI coating layer.27 The obtained membrane was

108

washed using deionized water at 0.02 bar and then was stored in water at 4 °C.

109

2.4. AFB1 removal. 2 mg mL-1 AFB1 stock solution was prepared by dissolving 10 mg

110

AFB1 in DMF and stored at -20 °C. AFB1 removal by peroxidase-like MOFs was carried

111

out using free and immobilized MOFs. The disperse system with free MOFs was used

112

to provide a fundamental and comprehensive understanding about the properties of

113

peroxidase-like MOFs in mycotoxin removal. The MOFs-loaded membrane system

114

investigated the reusability of MOFs in continuous mycotoxin removal.

115

As for the dispersion system, MOFs solid was dispersed in 10 mL sodium acetate

116

buffer or HEPES buffer (pH=4.0~7.0) by ultrasonic agitation to form a uniform

117

suspension (0.1, 0.3 and 0.5 mg mL-1). Peroxidase solution (1.5 U mL-1) was prepared

118

by dissolving lyophilized peroxidase powder into the same buffers. Then, AFB1 (final

119

concentrations: 50 ppb, 1000 ppb) and H2O2 (1 mM, 5 mM, or 20 mM) were added

120

alone or together and transferred to a shaker (100 rpm) at a certain temperature (30~60

121

°C). After a certain time, 1 mL of the suspension was filtered by a 0.22 μm filter, boiled

122

for 5-10 min to remove residual H2O2 and stored at -20 °C for HPLC analysis. In


8

Page 9 of 38 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


123

addition, to investigate the possibility of application in feedstuff, some primary nutrients

124

in corn, including starch, zein, α-cellulose, and corn oil, were respectively added to the

125

system to a final concentration of 1 g L-1. Then, the results were compared with those of

126

the blank.

127

As for the membrane system, the MOFs-loaded membrane was installed in a stirred

128

cell under normal mode (skin layer facing the feed), and 23 mL of AFB1 solution (50

129

ppb) that contained H2O2 (20 mM) was filtered at 40 °C for 2.5 h under gravity. 20 mL of

130

permeate and 3 mL of retentate were collected and heated for 5 min at 100 °C. Then,

131

samples were stored at -20 °C for HPLC analysis. The AFB1 removal efficiency was

132

calculated using the following formula:

133 134

(

AFB1 removal efficiency = 1 ―

) × 100%

cpVp + crVr c0V0

(1)

135 136 137

where c0 and V0 were the initial AFB1 concentrations and volumes, and cp (cr) and Vp (Vr) were the AFB1 concentrations and volumes of permeate (retentate), respectively.


9


Page 10 of 38

138

Interference tests were performed in the same way by pre-mixing corn, starch,

139

cellulose, zein or corn oil in the system. The AFB1 relative amount before and after

140

nutrients adsorption was calculated as:

141 142

c

AFB1 relative amount = c0 × 100%

(2)

143 144

where c0 (c) was the AFB1 concentration before (after) nutrients adsorption.

145

All samples were analysed by a high-performance liquid chromatography system

146

(HPLC, Agilent, 1100 series) equipped with a column (ZORBAX SB-C18, 250 mm × 4.6

147

mm i.d.; 5 μm; Agilent, USA), a VWD detector (Agilent, G1314A, USA) and an FLD

148

detector (Agilent, G1321B, USA). All vessels contaminated by AFB1 should be soaked

149

in sodium hypochlorite solution (2% w/v) for 24 h and washed with ethanol thoroughly.

150

2.5. Animal experiment. The detoxification of AFB1 by peroxidase-like MOFs has been

151

tested and verified by animal experimentation. To obtain a low bio-toxic environment,

152

propanediol (PG) and dimethyl sulfoxide (DMSO) were used as cosolvent of AFB1

153

instead of DMF in the animal experiment. AFB1 was dissolved in PG-DMSO (volume


10

Page 11 of 38 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


154

ratio, 1:1) to a final concentration of 1 mg mL-1 as mother liquid. By mixing the mother

155

liquid with a specific amount of sodium acetate buffer (20 mM, pH=4.0), an initial

156

solution that contained 30 μg mL-1 AFB1 was prepared and used to feed mice. This

157

solution was detoxified by adding MIL-53 (1 mg mL-1), H2O2 (50 mM) and incubating at

158

40 °C for 8 h, then filtered by microfiltration membrane and boiled for 5 min. In addition,

159

a blank solution was prepared by adding only PG and DMSO into sodium acetate buffer

160

without AFB1 to investigate the toxicity of the cosolvent.

161

Six-week-old male ICR mice were obtained from Beijing HFK Bioscience Co., Ltd.

162

The mice were divided into 4 groups and administered different solutions orally twice a

163

week for 5 weeks as follows: group I mice received normal saline; group II mice

164

received blank solution; mice in group III were fed with initial AFB1 solution and group IV

165

mice received detoxified solution. The body weights of mice were measured twice a

166

week. On day 39, venous blood was drawn from the orbits of mice. The serum was

167

obtained by centrifugation and stored at -80 °C for further testing. The activities of

168

alkaline

169

aminotransferase (ALT) in serum were measured by an OLYMPUS AU 400 automatic

phosphatase

(ALP),

lactate

dehydrogenase

(LDH)

and

alanine


11


Page 12 of 38

170

biochemical analyser (Japan). Significant differences between groups were calculated

171

by one-way ANOVA using SPSS software. Values of P < 0.05 were considered

172

statistically significant.

173

2.6. Degradation products analysis. Degradation products were analysed by an

174

ultraviolet-visible spectrophotometer (UV9000S, Metash, China) and mass spectrometer

175

(micrOTOF-Q II, Bruker, Germany).

176

2.7. Characterization. The crystal phase of MOFs samples was verified using a

177

powder X-ray diffractometer (PXRD, PANalytical B.V., Empyrean). The chemical

178

composition of MOFs was proven by X-ray photoelectron spectroscopy (XPS, Thermo

179

Fisher Scientific, ESCALAB 250Xi). The morphologies of MOFs and membranes were

180

observed using cold field emission scanning electron microscope (FESEM, JEOL, JSM

181

6700F), thermal field emission scanning electron microscope (FESEM, JEOL, JSM-

182

7001F) and energy dispersive spectroscopy (EDS, Oxford, Inca X-Max). Particle size

183

and zeta-potential of MOFs were analysed by a light scattering particle size and zeta

184

potential analyser (Beckman Coulter, DelsaNano C). Nitrogen adsorption-desorption

185

isotherms were measured by a gas sorption analyser (Quantachrome, Autosorb-iQ-


12

Page 13 of 38 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


186

MP), and the BET surface areas and the distributions of pore sizes were calculated

187

based on the obtained isotherms.

188 189

3. RESULTS AND DISCUSSION

190

3.1. Characterization of peroxidase-like MOFs. Three peroxidase-like MOFs were

191

analysed by XRD, XPS, SEM, DLS, zeta potential and nitrogen adsorption/desorption

192

isotherms. XRD patterns of all synthesized MOFs matched very well with simulated

193

ones, which revealed the successful synthesis of MIL-100, MIL-53 and MIL-68 (Figures

194

S1-S3). In XPS spectra, the two peaks of Fe 2p1/2 and Fe 2p3/2 were distributed

195

approximately 724.8 eV and 711.3 eV, respectively (Figure 1a). The peak differential

196

analysis showed that the fitted peaks at 711.3, 713.9, 717.8, 724.8, 727.3 and 731.7 eV

197

are assigned to the FeIII cation. New multiple peaks at 709.6 and 723.1 eV were

198

attributable to the characteristics of FeII in MIL-53.28 Fe species, especially FeIII in

199

MOFs, imitated the active sites in Fe-based peroxidase. In addition, the FeII cation in

200

MIL-53 provided an extra Fenton-type property that might enhance the catalytic activity.

201

According to DSL and zeta-potential analysis, the mean sizes of MIL-100, MIL-53 and


13


Page 14 of 38

202

MIL-68 were 3617.9, 1116.4 and 2879.5 nm, respectively, while the zeta potentials were

203

37.4, 33.2 and 23.0 mV, respectively (Figures S4-S6). SEM images gave the

204

morphology and particle size of MOFs (Figures S7-S9). MIL-53 was a mixture of large

205

and small particles. The size of MIL-53 was relatively uniform. For MIL-68,

206

agglomeration appears because of the long synthesis time. The morphology and size of

207

MOFs would influence subsequent loading in the membrane. Elements mapping

208

showed that C, O and Fe were uniformly distributed in all MOFs (Figures S10-S12). The

209

relative contents of Fe were 14.79%, 22.09% and 24.05% in MIL-100, MIL-53 and MIL-

210

68, respectively, which was another key factor affecting catalytic activity besides Fe

211

valence. The N2-adsorption/desorption isotherms of MIL-100 and MIL-68 belonged to

212

type I, according to IUPAC, which suggested that MIL-100 and MIL-68 were typical

213

microporous materials (Figures 1b and 1d). The BET specific surface areas of MIL-100

214

and MIL-68 were 1528.5 and 248.9 m2 g-1, and the pore sizes were 11.8 and 14.1 Å,

215

respectively, which were consistent with the results in the literature.20, 29 The pores and

216

cages of MOFs might be key factors affecting adsorption capacity. For MIL-53, the

217

isotherm was categorized as type III, implying the imporosity of MIL-53 (Figure 1c).


14

Page 15 of 38 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


218

Because of the breathing framework, MIL-53 has closed pores and shows almost no

219

porosity after degassing.30

220 221

Figure 1. (a) High resolution scanning XPS spectra for Fe 2p regions of MOFs; N2-

222

adsorption/desorption isotherms and pore size distributions (insets) of (b) MIL-100, (c)

223

MIL-53 and (d) MIL-68.


15


Page 16 of 38

224

3.2. AFB1 removal by free peroxidase-like MOFs. The AFB1 removal by three typical

225

peroxidase-like MOFs and peroxidase were first compared in the free system in order to

226

obtain their intrinsic properties of catalysis and adsorption (Figure 2). The AFB1 removal

227

by MOF alone was caused by adsorption (black line), and only H2O2 addition can also

228

slowly oxidize AFB1 (red line). When both H2O2 and MOF were added, a synergistic

229

effect of adsorption and catalysis promotes AFB1 removal (blue line). As seen in Figure

230

2, AFB1 was rapidly adsorbed to approximate equilibrium by MOFs within 10 h.

231

However, the adsorption rates of three MOFs to AFB1 were quite different. Strong,

232

medium and weak absorbability corresponded to MIL-68, MIL-100 and MIL-53,

233

respectively. All H2O2-containing groups exhibited a trend of continuous degradation of

234

AFB1. Thus, MOFs, as peroxidase-like catalysts, improve the AFB1 degradation rate to

235

different degrees. Contrary to adsorption, the order of catalytic ability from strong to

236

weak was given as follows: MIL-53, MIL-100 and MIL-68. By simple subtraction, the

237

contributions of adsorption and catalysis to AFB1 removal were illustrated in Figure 2d.

238

Briefly, there is a “trade-off” between adsorption and catalysis for each peroxidase-like

239

MOF. MIL-100 and MIL-53 show much greater catalytic ability than the natural


16

Page 17 of 38 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


240

horseradish peroxidase and H2O2, and MIL-68 own the highest AFB1 removal during 8

241

h, owing to its strong adsorption capacity. The similarity of MOFs and natural

242

peroxidase arises from similar catalytic mechanisms: a ping–pong mechanism.31-33

243

Regarding the catalytic mechanism of the peroxidase-like MOFs, it is widely accepted

244

that they could promote the conversion of H2O2 into OH· radicals through electron

245

transfer.20-21

246


17


Page 18 of 38

247

Figure 2. AFB1 removal with time by (a) MIL-100, (b) MIL-53, (c) MIL-68 and

248

horseradish peroxidase with or without H2O2. (d) Contribution of adsorption and

249

catalysis to AFB1 removal in 8 h by H2O2, MOFs and peroxidase. Concentration: 0.1 g L-

250

1

251

Volume: 10 mL; Temperature: 40 °C; pH: 4.0; Shaking speed: 100 r min-1. Condition

252

optimization can be seen below.

of MOFs, 1.5 U mL-1 of peroxidase, 1000 ppb of AFB1 and 20 mmol L-1 of H2O2;

253

To further explain the reasons for the entirely different properties of these MOFs,

254

more simulations and characterizations were carried out. Simulation results show that

255

the pore size of MOFs is mainly responsible for the adsorption capacity (Figure 3). Both

256

MIL-68 and MIL-100 have two kinds of pores. The smaller pores of both MOFs are too

257

narrow for AFB1 molecules to pass through. The diameters of the larger pores of MIL-68

258

and MIL-100 are approximately 16.0 and 10.4 Å, respectively, while the size of AFB1 is

259

approximately 10.8 Å × 8.7 Å. MIL-68, with larger pores, is more accessible to AFB1

260

molecules than MIL-100. In addition, MIL-68 has a 2D topological structure with an

261

inter-connective porous structure, which makes it more efficient for molecules to move


18

Page 19 of 38 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


262

in/out. However, for MIL-100, the 3D structure limits molecular mobility. On the one

263

hand, all small cages are forbidden for AFB1 molecules due to being full of small

264

windows. On the other hand, only partial windows of large cages are large pores, so

265

that the molecular pathways are tortuous. Thus, although MIL-100’s BET surface area is

266

many times larger than that of MIL-68, the adsorption capacity of MIL-100 is weaker

267

than that of MIL-68. For MIL-53, the flexible framework makes it difficult to estimate the

268

real pore size during dynamic processes, especially the multicomponent adsorption

269

process. An approximate state in which only water molecules are adsorbed reveals that

270

the pore size is unfit for AFB1 molecule transfer. For the adsorption mechanism,

271

hydrophobic adsorption and “π- π” interactions may play major roles, while electrostatic

272

interactions are relatively weak. This is due to the high hydrophobicity and nonpolarity of

273

AFB1 molecules.34-35 When H2O2 is added, the additional AFB1 removal is mainly due to

274

the oxidation reaction catalysed by MOFs. We consider that such increment in the AFB1

275

removal is attributed to “apparent catalysis,” since it is difficult to precisely define the

276

real contribution proportions of adsorption and catalytic oxidation to the AFB1 removal.

277

Obviously, MIL-53 has the strongest catalytic capacity, which may benefit from the


19


Page 20 of 38

278

combination of peroxidase-like/Fenton-like properties and high Fe content, according to

279

the results of XPS and EDS (Figure. 1a and Figures. S10-13). For MIL-68, the apparent

280

catalysis seems to be weakest though its Fe content is the highest. The real catalytic

281

capacity may be obscured by its high adsorption efficiency, leading to a low “apparent

282

catalysis”, which will be proven by the interference experiments below.

283

The effects of temperature (Figures S13-S16), H2O2 concentration (Figures S17-S20)

284

and pH (Figures S21-S23) on the AFB1 removal efficiency were studied systematically.

285

The adsorption capacity of all MOFs remained unchanged within the temperature range

286

from 30 °C to 60 °C, while the catalytic capacity increased with increasing temperature.

287

This means that the catalytic capacities of MOFs are more sensitive to temperature than

288

adsorption within a narrow temperature range. MIL-68 is insensitive to temperature

289

change, due to the dominant adsorption. The catalytic capacities of all MOFs are

290

positively correlated with the concentration of H2O2. For peroxidase-like MOFs, 20 mM

291

of H2O2 is an appropriate concentration for AFB1 removal. In addition, both adsorption

292

and catalytic capacities of MOFs decrease with the increase of pH, indicating that a


20

Page 21 of 38 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


293

slightly acidic environment is conducive to AFB1 removal, which is similar to natural

294

peroxidase.20-21

295


21


Page 22 of 38

296

Figure 3. Schematic diagram of crystal structures and channel/pore characteristics of

297

MIL-100, MIL-53 and MIL-68. Crystal data were obtained by CCDC, and AFB1

298

molecular structure was optimized by the DMol3 module in Material Studio version 8.0.

299 300

Figure 4. Interference of nutrients on AFB1 removal. (a) AFB1 residues in water with

301

addition of four common food nutrients. (b-d) Influences of nutrients on MOFs-catalysed

302

AFB1 removal. Concentration: 1 g L-1 of nutrients, 0.1 g L-1 of MOFs, 1000 ppb of AFB1


22

Page 23 of 38 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


303

and 20 mmol L-1 of H2O2; Volume: 10 mL; Operation time; 8 h; pH: 4.0; Temperature: 40

304

°C; Shaking speed: 100 r min-1.

305

Another important issue is that AFB1 always comes from agriculture and the food

306

industry. Very low concentrations of AFB1 and the interference from other substances

307

make it difficult to be removed. Almost 100%, 100% and 85% of AFB1 were respectively

308

removed by MIL-53, MIL-68 and MIL-100 when the initial concentration was reduced to

309

50 ppb (Figure S24). Four main nutrients in corn as interferents, including corn starch,

310

cellulose, zein and corn oil, were added into AFB1 aqueous solutions with MOFs. AFB1

311

is hardly adsorbed by those nutrients, except for zein, which adorbs 10% of AFB1

312

(Figure 4a). Therefore, the interference of zein was subtracted before subsequent

313

calculations. As shown in Figures 4b-4d, corn starch, cellulose and corn oil have no or

314

little effect on the AFB1 removal. However, zein has a negative effect on the AFB1

315

removal efficiency. Interestingly, when the adsorption capacity of MIL-68 was greatly

316

weakened, the catalytic ability was instead enhanced, resulting in only a slight decrease

317

of the total removal efficiency. This meant that the real catalytic capacity of MIL-68 is


23


Page 24 of 38

318

much stronger than its “apparent catalysis,” which makes MIL-68 a potential anti-

319

interference buffer.

320

3.3. AFB1 removal by MOFs-loaded membrane. To facilitate adsorbent/catalyst

321

recovery and continuous operation, the peroxidase-like MOFs were loaded into an

322

ultrafiltration membrane through reverse filtration of MOFs and subsequent dopamine-

323

polyethyleneimine (DA/PEI) co-deposition coating (Figure 5a). SEM images showed

324

that a large number of MIL-100 and MIL-53 particles were loaded on nonwoven fibers

325

and in the interfibre spaces, while only a few MIL-68 particles were filled in the spaces

326

(Figures S25-S27). Large particle size restricted the accessibility of MIL-68, which was

327

proved by the MOFs loading experiments (Figures S28). The sequence of loading rate

328

was: MIL-100 > MIL-53 > MIL-68. As a result, the AFB1 removal efficiency of three

329

MOFs-loaded membranes showed the same trend as loading amount/rate (Figures

330

S29) Then, “adsorption followed by catalysis/regeneration (adsorption-regeneration)”

331

and “simultaneous adsorption/catalysis (synergistic removal)” modes were evaluated for

332

AFB1 removal (Figure 5b); the former was suitable for the situations in which H2O2

333

residue was not allowed or H2O2-induced oxidation acted on the nutrients, and the latter


24

Page 25 of 38 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


334

met the requirements of a continuous and H2O2-tolerable process. In “adsorption-

335

regeneration” mode, taking the MIL-100-loaded membrane as an example, there was a

336

slight decrease in the AFB1 removal efficiency by adsorption without chemical

337

regeneration (Figure 5c), implying that hydrogen bonding might be the main adsorption

338

mechanism. When H2O2 was used to degrade AFB1 molecules adhered on the MOFs-

339

loaded membrane, the adsorption capacity of the regenerated membrane was

340

unexpectedly enhanced. It was speculated that the OH· radicals also degraded the

341

incompact polydopamine with increasing regeneration cycles and that more adsorption

342

sites on the loaded MOFs were exposed. In “synergistic removal” mode, adsorption and

343

catalysis worked synergistically during the gravity-driven flow-through process (Figures

344

5d-5f). The membranes with MIL-100 showed a super stable removal efficiency of AFB1

345

with H2O2, while there was only a slight decrease with reuse cycle for the other two

346

membranes. Moreover, the membrane with MIL-68 exhibited very low adsorption

347

capacity to AFB1, though MIL-68 has the highest adsorption capacity among the three

348

MOFs, which is caused by its lowest loading amount due to agglomeration (Figures

349

S27-28). It was worth mentioning that for the MIL-100-loaded membrane, the AFB1


25


Page 26 of 38

350

removal by adsorption was decreasing with reuse cycle without regeneration; however,

351

when H2O2 was added, the AFB1 removal remained almost constant through four

352

cycles, verifying that the catalytic ability of the membrane could avoid the adsorption

353

saturation.

354


26

Page 27 of 38 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


355

Figure 5. MOFs-loaded membranes for AFB1 removal. (a) Schematic diagram of

356

membrane preparation. (b) Two operation modes of MOFs-loaded membranes. (c)

357

Reusability of MIL-100-loaded membrane (0.9 cm × 0.9 cm) in “adsorption-

358

regeneration” mode. Reusability of (d) MIL-100 membrane, (e) MIL-53 membrane and

359

(f) MIL-68 membrane in “synergistic removal” mode.

360 361

3.4. Toxicity analysis of degradation products of AFB1. Aflatoxins mainly damage the

362

livers of humans and animals, and thus, the levels of serum enzymes from liver reflect

363

the degree of liver damage.36 After a 38 day oral toxicity test, the experimental mice

364

were weighed, and blood was collected. Three serum enzymes, alkaline phosphatase

365

(ALP), alanine aminotransferase (ALT) and lactate dehydrogenase (LDH), were chosen

366

to illustrate the detoxification effect.37 In addition, the effects of cosolvents, 1,2-

367

propanediol (PG) and dimethyl sulfoxide (DMSO), were also taken into account. The

368

levels of ALP and LDH increased slightly in the control group (PG+DMSO) but were

369

significantly elevated in the original AFB1 group, which indicated that the cosolvents and

370

AFB1 both caused liver injury (Figure 6). After detoxification, the levels of ALP and LDH


27


Page 28 of 38

371

returned to the normal range, confirming the effectiveness of detoxification. Meanwhile,

372

the results also verified that MIL-53 exposure to feeding solution was safe for liver. Fe

373

ions scarcely leached from MIL-53 under experimental conditions.21 In addition, no

374

significant difference was found in the levels of ALT and body weight between four

375

groups (Figures. S30-S31).

376 377

Figure 6. Levels of serum enzymes, (a) ALP and (b) LDH, in mice after different gavage

378

administrations. Significant differences between groups are marked on bars with

379

specific symbols. #P < 0.05, and

380

< 0.05, **P < 0.01 and***P < 0.001 vs. the value of the group administered initial AFB1.

###P

< 0.001 vs. the value of control (normal saline). *P

381


28

Page 29 of 38 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


382

3.5. Analysis of degradation products. After verifying the detoxification effect through

383

animal experiments, we attempted to obtain more information about AFB1 degradation

384

products. MIL-53 was chosen as the catalyst due to possessing the weakest adsorption

385

and strongest catalysis. Two groups of HPLC curves obtained over time from variable

386

wavelength detector (VWD) and fluorescence detector (FLD) showed similar trends

387

(Figures S32-S33). AFB1 (retention time: 20.5 min) was gradually degraded within 4 or

388

8 h. However, no obvious new peak appeared, except multiple peaks appearing during

389

a short retention time window (3~8 min). This indicated that the products are nonspecific

390

and relatively hydrophilic. The results of UV-Vis full spectrum scanning show that no

391

new products can be detected clearly in a wide wavelength range (Figure S34). The

392

molecular weights of the possible products were obtained by high resolution mass

393

spectrometry, and the possible molecular formulas were also inferred (Figures S35-

394

S39). Compared with the structure of AFB1 (Figure S40), all possible products contain

395

incomplete lactone or bifuran rings, indicating that the main toxic structural components

396

are destroyed.38-39 Compared with other oxidation processes, the peroxidase-like


29


Page 30 of 38

397

catalytic system could degrade aflatoxin more thoroughly by oxidative ring-opening

398

processes.40-41

399 400

4. CONCLUSIONS

401

Peroxidase-like MOFs have much more efficient detoxification capacity than natural

402

peroxidase with respect to aflatoxin-contaminated liquid, but they show different

403

behaviours regarding AFB1 removal. The structures of frameworks and pores play key

404

roles in AFB1 adsorption, while the valence states and content of Fe ions affect the

405

catalytic performance. Even in the field of food processing, the nutrients as interfering

406

substances in the system have negligible impact on the AFB1 removal by these MOFs.

407

A MOFs-loaded membrane is developed by a simple strategy inspired by mussel

408

adhesive protein to reuse MOFs conveniently. As a result, excellent removal efficiency

409

and reusability are achieved in both “adsorption-regeneration” and “synergistic removal”

410

modes. Animal experiments confirm that the toxicity of AFB1 to liver can be detoxified by

411

peroxidase-like MOFs because AFB1 is degraded to a variety of low-carbon substances

412

with strong hydrophilicity and weak toxicity, according to MS analysis. The outcomes of


30

Page 31 of 38 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


413

this work will open the gate to the development of MOF-based antidotes to mycotoxins.

414

In the future, our research will focus on developing more efficient and lower-cost

415

enzyme-like catalysts for broad mycotoxin removal.

416 417

ASSOCIATED CONTENT

418

Supporting Information

419

XRD, DLS, zeta-potential, SEM images and EDS mapping of three peroxidase-like

420

MOFs, SEM images of MOFs-loaded membrane, effect of temperature, concentration of

421

H2O2, pH and low AFB1 concentration on AFB1 removal efficiency, MOFs loading

422

amount/rate in membranes and its influence on AFB1 removal, levels of ALT and weight

423

changes in mice, HPLC signal curves and UV-Vis full spectrum scan of samples, mass

424

spectra of possible degradation products and the molecular structure of AFB1 (PDF).

425

The Supporting Information is available free of charge on the ACS Publications website

426

at http://pubs.acs.org.

427

AUTHOR INFORMATION


31


428

Corresponding Author

429

*Email: [email protected] (J. Luo).

430

* Email: [email protected] (Y. Wan).

431

ACKNOWLEDGMENT

Page 32 of 38

432

The financial supports are supplied by the National Key Research and Development

433

Plan of China (2017YFC1600906), the National Natural Science Foundation of China

434

(No. 21878306) and Youth Innovation Promotion Association (2017069) of Chinese

435

Academy of Sciences.

436

NOTE

437

The authors declare no competing financial interest.

438 439

REFERENCES

440

1.

441

Regulatory Standards. Environ. Sci. Technol. 2004, 38 (15), 4049-4055.

442

2.

443

16 (3), 116-119.

Wu, F., Mycotoxin Risk Assessment for the Purpose of Setting International Moss, M. O., Mycotoxin review - 1. Aspergillus and Penicillium. Mycologist 2002,


32

Page 33 of 38 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


444

3.

Loi, M.; Fanelli, F.; Liuzzi, V. C.; Logrieco, A. F.; Mule, G., Mycotoxin

445

Biotransformation by Native and Commercial Enzymes: Present and Future

446

Perspectives. Toxins 2017, 9 (4), 111-141.

447

4.

448

Kinetics of Degrading Aflatoxin B1 by Salt Tolerant Candida Versatilis CGMCC 3790. J.

449

Hazard. Mater. 2018, 359, 382-387.

450

5.

451

POMOF/SWNT Nanocomposites with Prominent Peroxidase-Mimicking Activity for l-

452

Cysteine “On–Off Switch” Colorimetric Biosensing. ACS Appl. Mater. Interfaces 2019,

453

11 (18), 16896-16904.

454

6.

455

Mimetic for Biomedical Applications. Theranostics 2017, 7 (13), 3207-3227.

456

7.

457

Chloroplast Mimics Capable of Photoenzymatic Reactions for Sustainable Fuel

458

Synthesis. Angew. Chem. 2017, 129 (27), 7984-7988.

459

8.

460

Carbonyl Catalysis enables a biomimetic asymmetric Mannich reaction. Science 2018,

461

360 (6396), 1438-1442.

462

9.

463

Ammonium Polymer as a Single Catalyst for Glucose Dehydration to 5-

464

Hydroxymethylfurfural. Green Chem. 2015, 17 (4), 2348-2352.

465

10.

466

Cationic Metal–Organic Framework as a Dual Adsorbent of Oxoanion Pollutants.

467

Angew. Chem. Int. Ed. 2016, 55 (27), 7811-7815.

468

11.

469

Nanofibrous Metal–Organic Framework Filters for Efficient Air Pollution Control. J. Am.

470

Chem. Soc. 2016, 138 (18), 5785-5788.

471

12.

472

Organic Framework Nanofibrous Membrane Adsorption and Activation for Heavy Metal

473

Ions Removal from Aqueous Solution. ACS Appl. Mater. Interfaces 2018, 10 (22),

474

18619-18629.

Li, J.; Huang, J.; Jin, Y.; Wu, C.; Shen, D.; Zhang, S.; Zhou, R., Mechanism and

Li, X.; Yang, X.-Y.; Sha, J.-Q.; Han, T.; Du, C.-J.; Sun, Y.-J.; Lan, Y.-Q.,

Gao, L.; Fan, K.; Yan, X., Iron Oxide Nanozyme: A Multifunctional Enzyme Liu, K.; Yuan, C.; Zou, Q.; Xie, Z.; Yan, X., Self-Assembled Zinc/Cystine-Based

Chen, J.; Gong, X.; Li, J.; Li, Y.; Ma, J.; Hou, C.; Zhao, G.; Yuan, W.; Zhao, B.,

Cao, X.; Teong, S. P.; Wu, D.; Yi, G.; Su, H.; Zhang, Y., An Enzyme Mimic

Desai, A. V.; Manna, B.; Karmakar, A.; Sahu, A.; Ghosh, S. K., A Water-Stable

Zhang, Y.; Yuan, S.; Feng, X.; Li, H.; Zhou, J.; Wang, B., Preparation of

Efome, J. E.; Rana, D.; Matsuura, T.; Lan, C. Q., Insight Studies on Metal-


33


Page 34 of 38

475

13.

Lyu, F.; Zhang, Y.; Zare, R. N.; Ge, J.; Liu, Z., One-Pot Synthesis of Protein-

476

Embedded Metal–Organic Frameworks with Enhanced Biological Activities. Nano Lett.

477

2014, 14 (10), 5761-5765.

478

14.

479

Wang, X.; Wang, K.; Lian, X.; Gu, Z.-Y.; Park, J.; Zou, X.; Zhou, H.-C., Stable Metal-

480

Organic Frameworks Containing Single-Molecule Traps for Enzyme Encapsulation. Nat.

481

Commun. 2015, 6, 5979-5986.

482

15.

483

Enzymes Orient When Trapped on Metal–Organic Framework (MOF) Surfaces? J. Am.

484

Chem. Soc. 2018, 140 (47), 16032-16036.

485

16.

486

Mimic Multienzyme Systems in Hierarchically Porous Biomimetic Metal–Organic

487

Frameworks. ACS Appl. Mater. Interfaces 2018, 10 (39), 33407-33415.

488

17.

489

S.; Yu, Y.; Lu, Q.; Chen, J.; Zhao, W.; Ying, Y.; Zhang, H., Bioinspired Design of

490

Ultrathin 2D Bimetallic Metal–Organic-Framework Nanosheets Used as Biomimetic

491

Enzymes. Adv. Mater. 2016, 28 (21), 4149-4155.

492

18.

493

Modified Metal–Organic Framework Nanoparticles: A Peroxidase-Mimicking

494

Nanoenzyme. Small 2018, 14 (5), 1703149.

495

19.

496

Gold Nanoparticles/Metal–Organic Gels Hybrids with Excellent Peroxidase-Like Activity

497

for Sensitive Chemiluminescence Detection of Organophosphorus Pesticides. ACS

498

Appl. Mater. Interfaces 2018, 10 (34), 28868-28876.

499

20.

500

Stable Metal-Organic Frameworks with Intrinsic Peroxidase-Like Catalytic Activity as a

501

Colorimetric Biosensing Platform. Chem. Commun. 2014, 50 (9), 1092-1094.

502

21.

503

Framework with Intrinsic Peroxidase‐Like Catalytic Activity for Colorimetric Biosensing.

504

Chem. Eur. J. 2013, 19 (45), 15105-15108.

Feng, D.; Liu, T.-F.; Su, J.; Bosch, M.; Wei, Z.; Wan, W.; Yuan, D.; Chen, Y.-P.;

Pan, Y.; Li, H.; Farmakes, J.; Xiao, F.; Chen, B.; Ma, S.; Yang, Z., How Do

Liu, X.; Qi, W.; Wang, Y.; Lin, D.; Yang, X.; Su, R.; He, Z., Rational Design of

Wang, Y.; Zhao, M.; Ping, J.; Chen, B.; Cao, X.; Huang, Y.; Tan, C.; Ma, Q.; Wu,

Chen, W.-H.; Vázquez-González, M.; Kozell, A.; Cecconello, A.; Willner, I., Cu2+-

He, L.; Jiang, Z. W.; Li, W.; Li, C. M.; Huang, C. Z.; Li, Y. F., In Situ Synthesis of

Zhang, J.-W.; Zhang, H.-T.; Du, Z.-Y.; Wang, X.; Yu, S.-H.; Jiang, H.-L., Water-

Ai, L.; Li, L.; Zhang, C.; Fu, J.; Jiang, J., MIL‐53(Fe): A Metal–Organic


34

Page 35 of 38 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


505

22.

Liu, Y. L.; Zhao, X. J.; Yang, X. X.; Li, Y. F., A Nanosized Metal–Organic

506

Framework of Fe-MIL-88NH2 as a Novel Peroxidase Mimic Used for Colorimetric

507

Detection of Glucose. Analyst 2013, 138 (16), 4526-4531.

508

23.

509

Metalloporphyrin PCN-222: Mesoporous Metal–Organic Frameworks with Ultrahigh

510

Stability as Biomimetic Catalysts. Angew. Chem. Int. Ed. 2012, 51 (41), 10307-10310.

511

24.

512

Zhou, H.-C., A Series of Highly Stable Mesoporous Metalloporphyrin Fe-MOFs. J. Am.

513

Chem. Soc. 2014, 136 (40), 13983-13986.

514

25.

515

Bazin, P.; Vimont, A.; Daturi, M.; Bloch, E.; Llewellyn, P. L.; Serre, C.; Horcajada, P.;

516

Grenèche, J.-M.; Rodrigues, A. E.; Férey, G., Controlled Reducibility of a Metal–Organic

517

Framework with Coordinatively Unsaturated Sites for Preferential Gas Sorption. Angew.

518

Chem. 2010, 122 (34), 6085-6088.

519

26.

520

3D Modification: Metal-Organic Frameworks Ameliorate Its Stability for Micropollutants

521

Removal. Chem. Eng. J. 2018, 348, 389-398.

522

27.

523

Inspired Modification of a Polymer Membrane for Ultra-High Water Permeability and Oil-

524

in-Water Emulsion Separation. J. Mater. Chem. A 2014, 2 (26), 10225-10230.

525

28.

526

Sites as Efficient Fenton-like Catalyst for Enhanced Degradation of Sulfamethazine.

527

Environ. Sci. Technol. 2018, 52 (9), 5367-5377.

528

29.

529

Greneche, J.-M.; Margiolaki, I.; Ferey, G., Synthesis and Catalytic Properties of MIL-

530

100(Fe), an Iron(iii) Carboxylate with Large Pores. Chem. Commun. 2007, (27), 2820-

531

2822.

532

30.

533

S.; Serre, C.; Vincent, D.; Loera-Serna, S.; Filinchuk, Y.; Férey, G., Complex Adsorption

534

of Short Linear Alkanes in the Flexible Metal-Organic-Framework MIL-53(Fe). J. Am.

535

Chem. Soc. 2009, 131 (36), 13002-13008.

Feng, D.; Gu, Z.-Y.; Li, J.-R.; Jiang, H.-L.; Wei, Z.; Zhou, H.-C., Zirconium-

Wang, K.; Feng, D.; Liu, T.-F.; Su, J.; Yuan, S.; Chen, Y.-P.; Bosch, M.; Zou, X.;

Yoon, J. W.; Seo, Y.-K.; Hwang, Y. K.; Chang, J.-S.; Leclerc, H.; Wuttke, S.;

Ren, Z.; Luo, J.; Wan, Y., Highly Permeable Biocatalytic Membrane Prepared by

Yang, H.-C.; Liao, K.-J.; Huang, H.; Wu, Q.-Y.; Wan, L.-S.; Xu, Z.-K., Mussel-

Tang, J.; Wang, J., Metal Organic Framework with Coordinatively Unsaturated

Horcajada, P.; Surble, S.; Serre, C.; Hong, D.-Y.; Seo, Y.-K.; Chang, J.-S.;

Llewellyn, P. L.; Horcajada, P.; Maurin, G.; Devic, T.; Rosenbach, N.; Bourrelly,


35


Page 36 of 38

536

31.

Gao, L.; Zhuang, J.; Nie, L.; Zhang, J.; Zhang, Y.; Gu, N.; Wang, T.; Feng, J.;

537

Yang, D.; Perrett, S.; Yan, X., Intrinsic Peroxidase-Like Activity of Ferromagnetic

538

Nanoparticles. Nat Nanotechnol 2007, 2 (9), 577-583.

539

32.

540

Organic Framework with Peroxidase-Like Activity and Its Application to Glucose

541

Detection. Catal. Sci. Technol. 2013, 3 (10), 2761-2768.

542

33.

543

Facile Microwave-Assisted Synthesis and Use as a Highly Active Peroxidase Mimetic

544

for Glucose Biosensing. RSC Advances 2015, 5 (23), 17451-17457.

545

34.

546

Yang, W., Current Major Degradation Methods for Aflatoxins: A Review. Trends Food

547

Sci. Technol. 2018, 80, 155-166.

548

35.

549

Adsorbing Agents, with an Emphasis on Their Multi-Binding Capacity, for Animal Feed

550

Decontamination. Food Chem. Toxicol. 2018, 114, 246-259.

551

36.

552

1966, 209 (5020), 312-313.

553

37.

554

Y.; Lee, J. C., Inhibitory Effects of Quercetin on Aflatoxin B1-Induced Hepatic Damage in

555

Mice. Food Chem. Toxicol. 2010, 48 (10), 2747-2753.

556

38.

557

Castro, M., Role of Lactone Ring in Structural, Electronic, and Reactivity Properties of

558

Aflatoxin B1: A Theoretical Study. Arch. Environ. Contam. Toxicol. 2010, 59 (3), 393-

559

406.

560

39.

561

in Toxicity and Carcinogenicity of Aflatoxins and Analogs. Cancer Res. 1971, 31 (12),

562

1936-1942.

563

40.

564

Myeloperoxidase-Hydrogen Peroxide-Chloride System. Arch. Oral Biol. 1981, 26 (4),

565

339-340.

Qin, F.-X.; Jia, S.-Y.; Wang, F.-F.; Wu, S.-H.; Song, J.; Liu, Y., Hemin@Metal–

Dong, W.; Liu, X.; Shi, W.; Huang, Y., Metal-Organic Framework MIL-53(Fe):

Peng, Z.; Chen, L.; Zhu, Y.; Huang, Y.; Hu, X.; Wu, Q.; Nüssler, A. K.; Liu, L.;

Vila-Donat, P.; Marín, S.; Sanchis, V.; Ramos, A. J., A Review of the Mycotoxin

Clifford, J. I.; Rees, K. R., Aflatoxin: a Site of Action in the Rat Liver Cell. Nature Choi, K. C.; Chung, W. T.; Kwon, J. K.; Yu, J. Y.; Jang, Y. S.; Park, S. M.; Lee, S.

Nicolás-Vázquez, I.; Méndez-Albores, A.; Moreno-Martínez, E.; Miranda, R.;

Wogan, G. N.; Edwards, G. S.; Newberne, P. M., Structure-Activity Relationships

Odajima, T., Oxidative Destruction of the Microbial Metabolite Aflatoxin by the


36

Page 37 of 38 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


566

41.

Luo, X.; Wang, R.; Wang, L.; Wang, Y.; Chen, Z., Structure Elucidation and

567

Toxicity Analyses of the Degradation Products of Aflatoxin B1 by Aqueous Ozone. Food

568

Control 2013, 31 (2), 331-336.

569


37


Page 38 of 38

570

571 572

TOC

573


38

Enzyme-Like MetalâOrganic Frameworks in Polymeric Membranes for

Recommend Documents

Enzyme-Like MetalâOrganic Frameworks in Polymeric Membranes for