[email protected] hybrid nanoparticles with antimicrobial properties from in-situ reduction and NTA polymerization

Journal Pre-proofs Ag@polyDOPA-b-polysarcosine hybrid nanoparticles with antimicrobial properties from in-situ reduction and NTA polymerization Jiayu Cen, Botuo Zheng, Yang Yang, Jindan Wu, Zhengwei Mao, Jun Ling, Guocan Han PII: DOI: Reference:

S0014-3057(19)31321-7 https://doi.org/10.1016/j.eurpolymj.2019.109269 EPJ 109269

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European Polymer Journal

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Please cite this article as: Cen, J., Zheng, B., Yang, Y., Wu, J., Mao, Z., Ling, J., Han, G., Ag@polyDOPA-bpolysarcosine hybrid nanoparticles with antimicrobial properties from in-situ reduction and NTA polymerization, European Polymer Journal (2019), doi: https://doi.org/10.1016/j.eurpolymj.2019.109269

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Ag@polyDOPA-b-polysarcosine hybrid nanoparticles with antimicrobial properties from in-situ reduction and NTA polymerization

Jiayu Cen,2 Botuo Zheng,2 Yang Yang,3 Jindan Wu,3 Zhengwei Mao,2 Jun Ling,*,2 Guocan Han*,1

1

Department of Radiology, Sir Run Run Shaw Hospital, School of Medicine,

Zhejiang University, Hangzhou 310016, China.

2

MOE Key Laboratory of

Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou 310027, China.

3

MOE Key

Laboratory of Advanced Textile Materials & Manufacturing Technology, Zhejiang Sci-Tech University, Hangzhou 310018, China. * Corresponding authors: [email protected] (J.L) and [email protected] (G.H.)

ABSTRACT Poly(-amino acid)s

are promising materials

due to

their excellent

biocompatibility and biodegradability. -Amino acid N-thiocarboxyanhydrides (NTAs), the thio-analogues of the corresponding N-carboxyanhydrides (NCAs), are able to synthesize polypept(o)ides by ring-opening polymerization with the tolerance of hydroxyl’s nucleophilic attack. In this work, polyDOPA-b-polysarcosine (PDOPA-b-PSar, named as DoS) copolymers are synthesized by sequential polymerizations

of

3,4-dihydroxy-L-phenylalanine

N-thiocarboxyanhydride

(DOPA-NTA) and sarcosine N-thiocarboxyanhydride (Sar-NTA) initiated by benzylamine in tetramethylene sulfone. With the reduction of catechol ligand, PDOPA-b-PSar act as the reducing and stabilizing agents for silver nanoparticles. The obtained Ag@PDOPA-b-PSar (Ag@DoS) nanoparticles have the average diameters of 81 nm with 10 nm core and narrow distributions. More than 95% bacterial killing efficiency to E.coil and S.aureus by Ag@DoS nanoparticles shows the potential for biomedical applications.

Keywords: poly(amino acid)s; ring-opening polymerization; silver nanoparticles; antibacterial agent

INTRODUCTION Since the discovery of penicillin by Fleming in 1928, antibiotics have been widely used to treat bacterial infections and have saved countless human lives. However, the overuse and misuse of antibiotics have caused the increase in bacterial resistance, leading to the decrease of antibiotic efficacy, even the growth of multiple resistant bacteria[1-4]. Therefore, it is urgent to develop new broad-spectrum antibacterial agents. Silver nanoparticles have attracted much attention due to the robust antimicrobial effect against various microorganisms and relatively low toxicity[5]. Typically, silver nanoparticle are prepared by reduction of soluble silver salts with reduction agents such as citrate, glucose, ethylene, or sodium borohydride[6], and protection by the stabilizers like polymers[7, 8], silica[9] and so on. But the use of non-biocompatible reductants and stabilizers can be toxic to the environment and human beings. Catechol ligands have strong reduction to Ag(I) cation due to their oxidation process of

catechol to quinone. Various catechol-bearing materials have been reported for the synthesis and protection of silver nanoparticles[10-36]. Early studies on the reduction of Ag+ by small molecular dopamine[16-22] and DOPA amino acid[26, 27] have been reported. Besides, Messersmith et al. prepared antibacterial hydrogels by utilizing a branched catechol-derivatized poly(ethylene glycol) and employing silver nitrate to oxidize

polymer

catechols[28].

They

also

synthesized

DOPA-containing

poly(ethylene glycol) (PEG) polymers by solid phase peptide synthesis strategy and in situ produced polymer-coated gold and silver nanoparticles[29]. Catechol-containing methacrylate[30], methacrylamide[31-33] and styrene[34, 35] derivatives have been reported to prepare silver nanoparticles. Recently, Char and coworkers developed polypept(o)ide block copolymers of polysarcosine with a dopamine-modified poly(glutamic acid) for surface coating and silver nanoparticles formation[36]. Due to the excellent biocompatibility and biodegradability, poly(amino acid)s are widely used in surface coating, drug delivery, gene transfection, tumour imaging, stimuli-responsive material and self-assembly systems[37-51]. Recently, our group developed α-amino acid N-thiocarboxyanhydride (NTA) monomers for poly(amino acid)s by amine-initiated ring-opening polymerizations (ROPs). NTA monomers and polymerizations exhibited good tolerance of the hydroxyl group, thoil group and water[51-55]. In 2018, we firstly reported the synthesis of DOPA-NTA and its controlled ROP without protection on the phenolic hydroxyl group [56]. In the contribution, we improve the synthesis of block copolymer polyDOPA-b-polysarcosine (PDOPA-b-PSar, simplified as DoS) by sequential ROP of DOPA-NTA and Sar-NTA in tetramethylene sulfone. PDOPA-b-PSar were used as both reducing and stabilizing agents to prepare silver nanoparticles. Based on the adhesion of PDOPA segment and protection of PSar, Ag@DoS nanoparticles remain

stable in water for more than half a year and suppress the growth of E.coil and S.aureus effectively.

EXPERIMENTAL SECTION Measurements Nuclear magnetic resonance (NMR) spectra were collected on a Bruker Avance DMX 400 spectrometer (1H: 400 MHz and 13C: 100 MHz) with DMSO-d6 or CDCl3 as the solvent. Molecular weights and polydispersities (Đ) were determined by size-exclusion chromatography (SEC) which consisted of a Waters 1515 isocratic HPLC pump, a Waters 2414 interferometric refractometer (RI) and two Shodex KF series columns. Hexafluoroisopropanol (HFIP) containing 3 mg/mL CF3COOK was used as the eluent with a flow rate of 0.8 mL/min at 40 C. Commercial polymethyl methacrylate were used as the calibration standards. Matrix-assisted laser desorption ionization-time of flight (MALDI-ToF) mass spectra were collected on a Bruker Ultraflextreme

MALDI-ToF

2,5-Dihydroxybenzoic

acid

mass

spectrometer

(DHB) was

used as

in

the

matrices

reflector and

mode.

potassium

trifluoroacetate was used as the cationic agent. Dynamic light scattering (DLS) measurements were carried out using a particle size analyzer (Zetasizer Nano Series, Malvern Instruments) at 25 °C. Each reported measurement was conducted for three repeating times. Transmission electron microscopy (TEM) images were obtained using a HITACHI HT7700 instrument. X-ray photoelectron spectroscopy (XPS) analysis was performed on an ESCALAB 250 spectrometer (ThermoVG Scientific, UK). X-ray diffraction (XRD) patterns were performed on a X-pert Powder diffractometer (PANalytical B.V.). The concentrations of Ag+ was determined by

inductively coupled plasma optical emission spectrometer (ICP-OES) (Spectro Arcos MV). Materials L-DOPA (98%, Energy Chemical, China), sarcosine (98%, Energy Chemical, China), phosphorous tribromide (99%, Energy Chemical, China) and silver nitrate (AR, Sinopharm Chemical Reagent) were used as received. Benzylamine and tetramethylene sulfone was stirred over CaH2 and followed by distillation under reduced pressure. DOPA-NTA and Sar-NTA were prepared according to the procedure described in the literatures[56-58] (Scheme S1) and analyzed by 1H and 13C NMR spectra (Figure S1-S4). Polymerization of DOPA-NTA All polymerizations were performed using Schlenk technique and all reaction tubes were previously flame-dried and purged with argon. As a typical homopolymerization, DOPA-NTA (0.2433 g, 1.018 mmol) was dissolved in 2.0 mL dry tetramethylene sulfone, followed by 0.54 mL of benzylamine solution in tetramethylene sulfone (0.1874 mol/L). The tube was sealed and placed in a 60 C oil bath for 72 h. The polymer product was precipitated from diethyl ether and dried in vacuum (0.184 g, 95.3%). Diblock copolymerizations of DOPA-NTA with Sar-NTA As a typical diblock copolymerization, DOPA-NTA (0.386 g, 1.62 mmol) was dissolved in 10.8 mL of dry tetramethylene sulfone, followed by 1.14 mL of benzylamine solution in tetramethylene sulfone (0.1294 mol/L). The tube was sealed and placed in a 60 C oil bath for 24 h. Then Sar-NTA (0.955 g, 7.29 mmol) was added into the tube and allowed for another 24 h polymerization. The copolymer was precipitated from diethyl ether and dried in vacuum (0.736 g, 89.5%).

Acetylation of polyDOPA 63.6 mg polyDOPA was dissolved in 2 mL DMF, followed by 1.5 mL acetic anhydride (20 equiv.). The reaction mixture was stirred overnight at room temperature and the product was precipitated from diethyl ether and dried in vacuum (77 mg, 82.5%). Preparation of PDOPA-b-PSar nanoparticles Polymer micelles were prepared by a solvent exchange method. 10.3 mg PDOPA10-b-PSar36 was dissolved in 1.0 mL DMF in a spawn bottle, after which 3.0 mL deionized water was added dropwise in 20 min. After another 30 min of vigorous stirring, the mixture was dialyzed against deionized water. The mixture was filtered through a filter (0.45 m) and stored at room temperature. Preparation of Ag@PDOPA-b-PSar nanoparticles As an example, 10.2 mg PDOPA10-b-PSar36 was dissolved in 1.0 mL DMF in a spawn bottle, followed by 0.47 mL of silver nitrate in water solution (0.197mol/L). Deionized water (3.0 mL) was added dropwise in 20 min. After another 30 min of vigorous stirring, the mixture was dialyzed for 48 h by changing deionized water every 4 h to remove DMF completely. The mixture was filtered through a filter (0.45 m) and stored at room temperature. Antibacterial test Gram-negative E.coil and Gram-positive S.aureus were used for the antibacterial tests. The samples (200 L) were incubated with 200 L bacterial suspension (1.0 x 108 CFU mL-1, PBS with pH 7.4) with shaking at 150 rpm at 37 C for 4 h. Afterwards, in serious dilutions, the mixture was placed onto the agar surface and incubated at 37 C for 18 h. The concentration of bacteria was calculated by flat colony counting method[59].

RESULT AND DISCUSSION Homopolymerizations of DOPA-NTA and block copolymerizations of DOPA-NTA with Sar-NTA were initiated by benzylamine in tetramethylene sulfone as shown in Scheme 1 and Table 1. Differing from our previous work[56], the polymerization solvent and the sequence of monomer addition were changed. Tetramethylene sulfone is an excellent solvent with better solubility and thermostability than acetonitrile, DMF, DMAc and DMSO. Both PDOPA and PDOPA-b-PSar can dissolve in tetramethylene sulfone. DPs of PDOPA are calculated from the intensities of Hd,e,f and Hc in 1H NMR spectra (Figure 1A) which increase with the increase of feed ratio of [DOPA-NTA]0/[benzylamine]0 (Figure S5) exhibiting a good control of ROP DOPA-NTA. MALDI-ToF mass spectra (Figure S6) show that PDOPA contains benzyl and amino groups with a monomodal and symmetrical distribution. Here we report PDOPA54 as the new record[56] of the longest backbone which were synthesized from the monomer bearing unprotected hydroxyl groups. Diblock copolymers PDOPA-b-PSar were successfully synthesized by sequential ROPs of DOPA-NTA with Sar-NTA initiated by benzylamine. Both signals of DOPA and Sar units are observed in 1H NMR spectrum (Figure 1A). The DP of the PDOPA and PSar segments, as well as the molecular weight of PDOPA-b-PSar are calculated according to the intensities of Hd,e,f and Hi with Hc. SEC trace shows the retention time of PDOPA-b-PSar decreases obviously from the first block of PDOPA (Figure 1B), indicating PSar segment successfully grew on the terminal amine group of PDOPA. It is worthy of mentioning that adsorption phenomenon of PDOPA-b-PSar onto the

polystyrene column may be responsible for the slight tailing of copolymer in SEC trace.

Scheme 1. Homopolymerization of DOPA-NTA and copolymerization of DOPA-NTA with Sar-NTA initiated by benzylamine.

Table 1. Homopolymerization of DOPA-NTA and copolymerization of DOPA-NTA with Sar-NTA initiated by benzylamine in tetramethylene sulfone. Sample

[DOPA]/[Sar]/[BnNH2]

Yield (%)

Producta

Mn (kg/mol)a

Đb

PD1c

10/0/1

95.3

PDOPA9

1.7

1.19

PD2c

20/0/1

87.5

PDOPA15

2.8

1.18

PD3c

30/0/1

85.1

PDOPA21

3.9

1.19

PD4c

50/0/1

80.8

PDOPA30

5.5

1.21

PD5c

100/0/1

81.4

PDOPA54

9.8

1.22

DoS1d

5/50/1

94.9

PDOPA5-b-PSar40

3.8

1.15

DoS2d

11/50/1

89.5

PDOPA10-b-PSar36

4.5

1.22

DoS3d

10/60/1

>99

PDOPA10-b-PSar46

5.2

1.27

a

Determined by 1H NMR. b Determined by HFIP GPC. c Polymerization conditions: [DOPA-NTA]0= 0.5 mol/L, 72 h in tetramethylene sulfone at 60 ºC. d Polymerization conditions: [DOPA-NTA]0= 0.15 mol/L, 24h in tetramethylene sulfone at 60 ºC, the

second block was polymerized at 60 ºC for additional 24 h.

Figure 1. (A) 1H NMR spectra of PDOPA and PDOPA-b-PSar in DMSO-d6. (B) SEC traces of the first block (acetylated with acetic anhydride, I) and PDOPA10-b-PSar36 (II) in HFIP.

Attributing to reducibility of catechol group, PDOPA-b-PSar copolymer can reduce silver nitrate to silver nanoparticles in situ. Aqueous solution of silver nitrate was added into the DMF solution of PDOPA-b-PSar under continuous stirring to produce Ag nanoparticles, and the carbonyl group of quinone on PDOPA-b-PSar copolymers attached at the surface of Ag nanoparticles. Figure 2 displays the size distribution of Ag@DoS nanoparticles measured by DLS and TEM. The DLS result suggests the average diameter of Ag@DoS nanoparticles as 81 nm with a narrow size distribution (PDI = 0.136). TEM image reveals the silver core of Ag@DoS is ca. 10 nm surrounded by oxidized PDOPA segments. Its chemical composition is confirmed by XPS test (Figure 3A) showing distinct C1s, N1s, O1s and Ag3d signals. In the

close scan of Ag3d (Figure 3B), the two peaks at 367.5 and 373.5 eV are assigned to Ag 3d5/2 and Ag 3d3/2, respectively, indicating the in situ formation of silver(0) metal. In addition, XRD determines the crystal structure of Ag@DoS nanoparticles. As shown in Figure S7, the peaks at 2 angles of 38.0, 64.4 and 77.2 correspond to the reflections of (111), (220) and (311) crystalline planes of Ag with face center cubic (fcc) structure. The concentration of Ag in aqueous solution is found to be 74.9 ppm according to ICP-OES test. The concentration of nanoparticles is 1.27 mg/mL where silver is 5.9 wt%. Agar plating of colonies was applied to evaluate the antibacterial activities of samples. We selected both E.coil and S.aureus as Gram-negative and Gram-positive bacteria, respectively. The DoS micelles and Ag@DoS nanoparticles with the same polymer concentration were incubated with bacterial suspension for 4 h. Then, in series dilutions, the bacterial suspension was plated onto agar for bacterial colony unit counting. As shown in Figure 4, numerous bacterial columns are observed in the agar plates treated by DoS micelles. On the contrary, little, if not none, bacterial adhesion can be seen on the ones with Ag@DoS nanoparticles. Quantitatively over 95% of bacterial attachment is suppressed for E.coil and S.aureus on Ag@DoS nanoparticles. In addition, the antibacterial effect of Ag@DoS against Gram-negative bacteria E.coil is much better than Gram-positive bacteria S.aureus, which may be resulted from the different structure and function between the two sorts of bacteria.

Figure 2. (A) Size distribution of Ag@PDOPA10-b-PSar36 nanoparticles measured by DLS test. (B) TEM image of Ag@PDOPA10-b-PSar36 nanoparticles.

Figure 3. (A) XPS spectrum of Ag@DoS nanoparticles (wide scan). (B) Ag3d core-level spectrum of Ag@DoS nanoparticles. (C) Schematic diagram of formation process of Ag@DoS nanoparticles.

Figure 4. The images and numbers of E.coil and S.aureus colonies treated with DoS nanoparticles and Ag@DoS nanoparticles, respectively.

CONCLUSION We improve the synthesis of PDOPA-b-PSar by sequential ROP of DOPA-NTA and Sar-NTA in tetramethylene sulfone, and use PDOPA-b-PSar as both the reductant and stabilizer to prepare Ag@DoS nanoparticles thanks to the reducibility of catechols of PDOPA segment and excellent hydrophilicity of PSar segment. Ag@DoS nanoparticles effectively kill E.coil and S.aureus, exhibiting the potential as new antibacterial reagents for biomedical and pharmaceutical applications.

ASSOCIATED CONTENT Supporting Information

1

H and

13

C NMR spectra of NTA monomers, SEC curves and MALDI-ToF mass

spectra of PDOPA and XRD of Ag@DoS nanoparticles.

AUTHOR INFORMATION Corresponding Authors * E-mail: [email protected] (G.H.) and [email protected] (J.L) Notes The authors declare no competing financial interest.

ACKNOWLEDGEMENTS The financial support from the National Natural Science Foundation of China (21674091), National Key Research and Development Program from the Ministry of Science and Technology of China (2016YFA0200301), Joint Foundation of Shaanxi Province Natural Science Basic Research Program and Shaanxi Coal Chemical Group Co., Ltd. (2019JLM-46), and Fundamental Research Funds for the Central Universities (2018QNA4057).

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Highlight

1. Conditions are optimized for polymerization of NTAs to synthesize PDOPA-b-PSar. 2. Ag@PDOPA-b-PSar nanoparticles are prepared after the reduction of Ag(I) by PDOPA-b-Psar. 3. More than 95% bacterial killing efficiency to E.coil and S.aureus by Ag@PDOPA-b-PSar nanoparticles.

Conflict of interest The authors declare no conflicts of interest.