Size-Controlled Synthesis of Carboxyl-Functionalized Magnetite

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Article Cite This: ACS Omega 2018, 3, 17904−17913

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Size-Controlled Synthesis of Carboxyl-Functionalized Magnetite Particles: Effects of Molecular Weight of the Polymer and Aging Yingying Song,†,§ Ying Li,†,§,⊥ Zi Teng,† Yukun Huang,‡ Xianggui Chen,*,‡ and Qin Wang*,†,‡ †

Department of Nutrition and Food Science, University of Maryland, 0112 Skinner Building, College Park, Maryland 20742, United States ‡ School of Food and Bioengineering, Xihua University, Chengdu, Sichuan 610039, China

ACS Omega 2018.3:17904-17913. Downloaded from pubs.acs.org by 5.8.47.44 on 12/23/18. For personal use only.

S Supporting Information *

ABSTRACT: Magnetic particles (MPs) are of great interest in many varied applications in the fields of biotechnology, biomedicine, and environmental remediation. To accommodate different applications, size-control synthesis of MPs is of particular interest. Here, we report a simple synthesis of MPs in the range of nano to microsize (23 nm to 1.2 μm). Specifically, the particle size of MPs was tuned by the (i) molecular weight (Mw) of poly(acrylic acid) (PAA) and (ii) aging process. Three different hydrothermal procedures using different Mw of PAA were compared, namely, one-step hydrothermal, two-step hydrothermal, and coating-after hydrothermal methods. The Mw of PAA used was 1.8k, 30k, 50k, and 100k g/mol. The resulted particle sizes of the onestep hydrothermally synthesized 1.8k, 30k, 50k, and 100k MPs were 1202 ± 359, 447 ± 156, 418 ± 88, and 247 ± 34 nm, respectively, and those of the two-step ones were 23 ± 3, 100 ± 14.1, 116 ± 26, and 78 ± 6 nm, respectively. The crystal composition, ζ-potentials, magnetic properties, magnetic separation efficiencies, and protein conjugation properties were studied systematically. The results showed that MPs synthesized via one-step hydrothermal synthesis demonstrated the highest yield and the highest magnetic separation efficiency. Bovine serum albumin, lysozyme, and enhanced green fluorescent protein as protein models were successfully conjugated with the MPs, and the application of antibody-conjugated PAA-MPs for bacterial capture was demonstrated.

1. INTRODUCTION Recently, magnetic particles (MPs) have received considerable attention because of their advantages in recognizing magnetic stimuli and responding by controllable movements.1 Particularly, magnetite (Fe3O4) particles are known for their excellent magnetic properties and biocompatibility.2,3 These MPs have been increasingly studied for drug delivery, magnetic resonance imaging (MRI) and hyperthermia creation,4−6 enzyme immobilization and protein purification,7−9 bacterial separation,10 and pollutant removal.11 Depending on the applications, the desirable particle size of MPs varies greatly. In biomedicine, nanoscale materials are of special interest because of their compatibility with biomolecules for interaction (protein, 5−50 nm; virus, 20−450 nm; cell, 10−100 μm).12 MRI requires MPs with sizes smaller than 30 nm, so that they can escape the initial uptake by liver and spleen for the demarcation of arteries and veins.13 MPs with sizes ranging from 10 to 100 nm are optimal for intravenous injection and have the most prolonged blood circulation time.14 For high gradient magnetic separation (HGMS) of biomaterials, it has been demonstrated that MPs (or MP clusters) of 50 nm or larger can be effectively separated from process streams.15 For targeted drug delivery, research has © 2018 American Chemical Society

shown that medium-sized MPs (30−110 nm) accumulate in the heart, liver, kidney, bladder, vertebral column, and bone marrow,16 and larger MPs (200−300 nm) have been found in the spleen.5,17 Micrometer-sized MPs were desired for separation and purification. For example, magnetic microparticles of 1.6 and 26 μm were applied in separations from blood or other clinical samples in a microfluidic device to selectively pull molecules and living cells, bound to MPs from flowing biological fluids, without wash steps.18 Magnetic microspheres were used for rapid affinity-based purification of lysozyme.19 Multipurpose applications may require a more complex size range of MPs with similar surface functionalities. Efforts have been devoted to synthesizing wide-range monodispersed MPs. Nakaya et al. synthesized MPs of 5.3− 20.4 nm using a codeposition method in a bath of oleic acid and oleylamine.20 Tanaka reported a relatively wide range (20−200 nm) size control of spherical ferrite particles.21 Liu et al. fabricated polyacid-conjugated Fe3O4 nanostructures by a microwave-assisted method, and their size can be tuned in the Received: September 11, 2018 Accepted: December 6, 2018 Published: December 20, 2018 17904

DOI: 10.1021/acsomega.8b02351 ACS Omega 2018, 3, 17904−17913

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Figure 1. (a) SEM images of one-step hydrothermally synthesized MPs. (b) Schematics of possible particle formation mechanism during the onestep hydrothermal reaction.

and 100k-MPs were estimated to be 1202 ± 359, 447 ± 156, 418 ± 88, and 247 ± 34 nm, respectively. The lower panel of Figure 1a indicates that all these particles are porous and consisted of small nanocrystals. Generally, the particle size of MPs decreased as the Mw of PAA increased from 1.8k to 100k. The analysis of hydrodynamic sizes using dynamic light scattering (DLS) showed a similar trend (Table 1).

range of 100−400 nm by varying the amount of FeCl3 in the system.22 However, to the best of our knowledge, there is no report on nano- to microrange size-controlled synthesis of MPs. Here, we report a hydrothermal approach to obtain MPs with a controllable size in a wide range (23 nm to 1.2 μm) by adjusting the molecular weight (Mw) of the stabilizer with the combination of an aging step. Poly(acrylic acid) (PAA) with different Mw (1.8k, 30k, 50k, and 100k) was incorporated during one-step or two-step hydrothermal process for size control and carboxyl-functionalized coating for further chemical modification. Specifically, we demonstrated that hydrothermally reacting ferric ions with a reducing agent and varied Mw of PAA (i) afforded spherical MPs of controllable size, (ii) conferred MPs with a high negative ζ-potential at neutral pH, and (iii) yielded MPs that were able to conjugate with functional proteins [e.g., enzyme, fluorescent protein, and antibody (AB)] while they had no binding of bacterial cells per se.

Table 1. Hydrodynamic Sizes of One-Step Hydrothermally Synthesized PAA-MPs Measured by DLS Mw of PAA (g/mol)

temperature (°C)

bare particles 1.8k 30k 50k 100k 30k 30k

180 180 180 180 180 160 200

hydrodynamic size (nm)a 192 2527 596 396 258 1021 437

± ± ± ± ± ± ±

22 345 142 5 50 6 22

The data are expressed as mean ± standard deviation. Means of sizes of the MPs are significantly different from each other based on ANOVA (P < 0.05).

a

2. RESULTS AND DISCUSSION 2.1. One-Step Hydrothermal Synthesis of MPs. 2.1.1. Adjusting the Particle Sizes of One-Step Hydrothermally Synthesized PAA-MPs. Previous studies showed that using the coprecipitation or hydrothermal reaction, the particle sizes of Fe3O4 were controlled by varying the concentrations of sodium salts, solvents, and polyelectrolytes or by adding a seed-mediated growth procedure.21,23−25 First, our study was to evaluate the effect of different Mw of PAA (1.8k, 30k, 50k, and 100k g/mol) of the same mass concentration on the particle size and morphology of onestep hydrothermal reacted MPs (designated as one-step 1.8kMPs, 30k-MPs, 50k-MPs, and 100k-MPs, respectively). Figure 1a shows the scanning electron microscopy (SEM) images of one-step MPs synthesized using PAA of various Mw. All Fe3O4 particles were spherical except that 1.8k-MPs were elongated clusters of spherical particles, as shown in the upper panels of Figure 1a. The particle sizes of 1.8k-MPs, 30k-MPs, 50k-MPs,

The following explanation was offered for the difference in the particle size of MPs synthesized by one-step hydrothermal reaction (Figure 1b). Although the molar concentrations of carboxyl groups in the reactants were the same (mass concentrations of PAA in the reaction bath were the same), the conformations of PAA of different Mw were different. Low Mw PAA tends to form long linear polymer chains, whereas high Mw PAA molecules tend to coil up to conceal the aliphatic backbone from water.26 Therefore, high Mw PAA may form a tougher polymer matrix and offer a more constrained environment, leading to a slower growth of Fe3O4 particles.27 It is noteworthy to mention that the hydrodynamic sizes (Table 1) of the one-step MPs matched with their respective particle size measured by SEM, suggesting that the MPs dispersed individually without clustering. The particle size of 17905


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bare one-step MPs (without PAA coating) was 25 ± 4 nm (based on SEM images, data not shown), whereas their hydrodynamic size measured by DLS was about 7.6 times the particle size (Table 1), indicating the clustering of bare MPs without PAA coating. PAA may serve as the adhesion agent to attach primary Fe3O4 crystallites,28 which resulted in the larger particle size of PAA-MPs compared to that of bare MPs. In addition, the synthesis temperature also affected the size of MPs. We tested the effect of synthesizing temperature on the hydrodynamic size of the MPs using PAA30k-MPs as a model. Three different temperatures (160, 180, and 200 °C) were adopted for the one-step hydrothermal synthesis of PAA30k-MPs. As presented in Table 1, when the synthesis temperature increased from 160 to 200 °C, the hydrodynamic size of the one-step PAA30k-MPs decreased from 1021 ± 6 to 437 ± 22 nm as a function of the reaction temperature. 2.1.2. Crystallite Size of the One-Step Hydrothermally Synthesized MPs. Crystallite size of the one-step hydrothermally synthesized MPs was measured by X-ray diffraction (XRD) (Figure S1, Supporting Information). All XRD spectra of bare MPs, 50k-MPs, and 100k-MPs matched that of Fe3O4 (PDF 01-076-0955, ICDD database). Compared to the other two samples, 100k-MPs showed apparent broadened peaks and decreased intensity, suggesting that increasing the Mw of PAA reduced the crystallinity of Fe3O4 crystalline in the MPs. Table 2 indicates that the crystallite size of 100k-MPs was Table 2. Crystallite Sizes of One-Step Hydrothermally Synthesized MPs without PAA, with PAA-50k, and with PAA-100k samples

crystallite size (nm)a

bare MPs 50k-MPs 100k-MPs

23.7 ± 0.4b 24.5 ± 0.3a 18.2 ± 0.4c

Figure 2. (a) TEM images of one-step hydrothermally synthesized one-step 50k-MPs and 100k-MPs; (b) TG analysis of the percentage of PAA on one-step MPs.

The data are expressed as mean ± standard deviation. Means of crystallite sizes of the MPs with different letters are significantly different based on ANOVA analysis (P < 0.05). a

around 10%. Furthermore, ζ-potentials were used to indicate the PAA coatings on the one-step MPs. Table 3 shows that all Table 3. ζ-Potential of One-Step MPs

significantly smaller than those of bare MPs and PAA50kMPs. These suggest that the high Mw of PAA inhibited the crystallite growth of MPs. Again, we ascribe the smaller crystallite size of MPs to the more constrained environment that higher Mw PAA offered. Similar results of decreased relative XRD peak intensities with increased PAA concentration were also found in PAA-magnetic nanoparticles synthesized by a coprecipitation method, indicating that PAA is able to alter the crystallinity of Fe3O4 crystalline.24 Other polymers [cellulose, poly(ethylene oxide), and poly(propylene oxide)] were also reported slowing the nucleation rate of nanocrystals.29,30 2.1.3. Characterization of Coatings on One-Step Hydrothermally Synthesized MPs. Transmission electron microscopy (TEM), thermogravimetric (TG), and ζ-potential analysis were carried out to measure the coating of PAA on the MPs. TEM images in Figure 2a illustrate the “hollow” and porous structure of the MPs as well as the PAA coating of MPs. The PAA layer adsorbed on 100k-MPs was much thicker than that on 50k-MPs. The TG method measured the PAA content of MPs based on the weight difference before and after thermal decomposition of PAA on MPs (Figure 2b). The highest PAA content was observed at 12.3% for the one-step 100k-MPs, whereas those for the one-step 1.8k, 30k, and 50k-MPs were all

samples 1.8k-MPs 30k-MPs 50k-MPs 100k-MPs

ζ-potential (mV)a −54.0 −52.1 −47.3 −52.0

± ± ± ±

1.7a 8.1a 1.4b 2.2a

Data are expressed as mean ± standard deviation. Means that have different letters are significantly different (ANOVA, P < 0.05).

a

one-step PAA coated MPs exhibited a large negative ζpotential, indicating the incorporation of PAA on the particles. The absolute value of ζ-potentials of these MPs was greater than 30 mV, suggesting they had high colloidal stability. In summary, it was demonstrated that adjusting the Mw of PAA resulted in tuning of the particle size, hydrodynamic size, crystallite size, and thickness of PAA coating of one-step hydrothermally synthesized MPs. 2.2. Two-Step Hydrothermal Synthesis of MPs. Next, we investigated the effects of two-step hydrothermal synthesis on the particle size and morphology of MPs. Here, the twostep hydrothermal synthesis referred to a hydrothermal reaction step at a relatively low temperature (120 °C, 10 h) at first and an aging step at room temperature (25 °C) afterwards and then a second hydrothermal reaction at 180 °C 17906


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Figure 3. (a) SEM images of two-step hydrothermally synthesis of 1.8k-MPs with different aging times. (b) SEM images of two-step hydrothermal synthesis of MPs using different Mw of PAA (aged for 3 days). (c) Schematics of possible particle formation mechanism during two-step hydrothermal reactions.

the two-step hydrothermal synthesized PAA-MPs (Figure 3c), that is, the possible formation of the microenvironment containing hydrophobic groups of degraded products of PAA occurred within a continuous phase, similar to an emulsification process. Fe3O4 nanocrystals tended to incorporate into this microenvironment because of hydrophobic interaction. Moreover, decarboxylation occurred randomly along the polymer chain of PAA,34 so the particle size of two-step MPs did not change in a Mw-dependent pattern. 2.3. Posthydrothermal Coating Synthesis. To understand the role of PAA during the hydrothermal reaction, a comparative synthesizing process was performed to synthesize PAA-coated MPs. The experimental procedures included synthesizing bare MPs at 180 °C for 10 h and further coating being applied to them with different Mw of PAA (1.8k, 30k, 50k, and 100k g/mol) at room temperature using 1-ethyl-3-(3dimethylaminopropyl)carbodiimide (EDC).32 The particle sizes evaluated by SEM showed no significant difference among treatments (∼30 nm, P > 0.05, see Figure S3 in the Supporting Information for a typical SEM image of posthydrothermal-coated 30k-MPs). Therefore, participation of PAA during the one-step and two-step hydrothermal syntheses of PAA-MPs was critical for adjusting their particle sizes. On the other hand, DLS analysis showed that the hydrodynamic sizes of the MPs with posthydrothermal PAA coating increased as the Mw of PAA increased. The hydrodynamic sizes for bare MPs, posthydrothermal-coated 1.8k, 30k, 50k, and 100k were 192 ± 22, 270 ± 24, 414 ± 28, 500 ± 67, and 461 ± 20 nm, respectively, probably because the coating of PAA on MPs in this method was based on absorption and PAA with higher Mw had a bigger radius of gyration.33 2.4. Magnetic Properties of the MPs Synthesized by Three Different Methods. The magnetic properties of the MPs synthesized by one-step and two-step hydrothermal reactions and posthydrothermal coating process were charac-

for 5 h. Figure 3a demonstrates the effect of aging time on the particle size of 1.8k-MPs. Interestingly, while aging for 0.5d resulted in two-step 1.8k-MPs with a particle size similar to that of the one-step 1.8k-MPs (elongated particle clusters with a micrometer size), the particle sizes of two-step 1.8k-MPs aged for 3 and 5 d are on the nanoscale (23 ± 3 and 23 ± 4 nm, respectively). The particle size of the ones aged for 15 d was 26 ± 3 nm, slightly larger than those reacted for the first step (120 °C for 10 h) (P < 0.05). XRD analysis showed that the two-step 1.8k-MPs aged 15 days were also Fe3O4 (Figure S2, Supporting Information). The oxidation degree of Fe3O4 requires further studies. An aging time of 3 d was subsequently applied for the twostep hydrothermal synthesis of MPs with PAA having different Mw (1.8k, 30k, 50k, and 100k g/mol). Figure 3b illustrates that the two-step MPs with different Mw of PAA are mostly spheres containing small nanocrystals. The particle sizes of two-step MPs (no PAA), 1.8k-MPs, 30k-MPs, 50k-MPs, and 100k-MPs were 21 ± 3, 23 ± 3, 100 ± 14.1, 116 ± 26, and 78 ± 6 nm, respectively. The maximum particle sizes were found in MPs synthesized with medium Mw PAA [i.e., 30k and 50k g/mol, no significant difference between these two (P > 0.05)]. Interestingly, the two-step MPs had a much smaller size (200 nm). Presumably, the addition of a hydrothermal reaction step at 120 °C and an aging step at 25 °C played a key role in forming reduced-size particles. Previous research showed that PAA in aqueous solution underwent decarboxylation and chain scission for a prolonged heating time at a high temperature (e.g., 180−325 °C).24,27,31 Water-insoluble products from the decarboxylated reaction were observed because of the loss of ionic functionality.32 However, very limited degradation (22%) of PAA with ammonia at 180 °C at pH 10.5 occurred after 168 h.33 We postulated that during the first hydrothermal step and the subsequent aging steps, the hydrophobic decarboxylated/ esterified products of PAA resulted in a size redistribution of 17907


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Figure 4. Magnetic properties of MPs synthesized via one-step and two-step hydrothermal reactions and posthydrothermal coating process. (a) Hysteresis loop of one-step 30k-MPs. Inset is the magnified graph for the magnetic field range from −100 to +100 Oe. (b) Remanent magnetization, Mr, (c) squareness ratio, Mr/Ms, and (d) coercivity (Hc) of PAA-MPs.

dependent.39 It is worth noting that 100k-MPs from both onestep and two-step hydrothermal syntheses had very low levels of Mr/Ms and Hc, which were comparable to the behavior of single-domain superparamagnetic particles (particle size < 20 nm).40 However, their particle size was much larger than that of the superparamagnetic particles. Presumably, one of the benefits of having a relatively larger particle size than singledomain particles is that during magnetophoresis, larger particles always have greater magnetic responsiveness than smaller versions of the same particle and enable easy magnetic separation.41 2.5. Magnetic Collection of MPs in Water. Many bioapplications of MPs, including drug delivery, MRI, separation, and immunoassay, are based on their magnetic responses in liquid systems, especially in aqueous solutions. For HGMS application of biomaterials, the capability for magnetic collection (or localization) of MPs is an important feature. The magnetophoretic mobility of MPs varied in great degree depending on the particle size,42,43 shape,15 and surface coating,15 but not directly proportional to Ms of the MPs.43 It was demonstrated that small MPs (98.0%) were purchased from VWR International (PA, USA). All reagents were of analytical grade. EGFP (with 6 × His-tagged N terminal and 7 × Lys-tagged C-terminal) was a gift from Dr. Willian E. Bentley at the University of Maryland. 17910


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of variance (ANOVA) with a significant level of 0.05 using the SPSS 16.0 statistical software package for Windows (SPSS Inc., Chicago, IL, USA).

the crystal composition of MPs and their crystallite size. The crystallite size of the Fe3O4 particles is calculated using the Scherrer equation L=

0.9λ β cos θ

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ASSOCIATED CONTENT

S Supporting Information *

(1)

where L is the average crystallite size (nm), λ is the X-ray wavelength (∼1.5418 Å), β is the peak breadth measured at half the maximum intensity (radians), and θ is the Bragg’s angle (degrees).64 Whereas the absolute crystallite size of one sample determined by Scherrer equation is roughly accurate, the difference in relative sizes between the two samples is more meaningful (refs 29 and 30). Particle sizes of MPs were measured by analyzing the SEM images obtained on a Hitachi SU-70 SEM microscope (Hitachi, Pleasanton, CA, USA). For each MP, at least 30 particles were randomly selected to obtain the mean particle sizes. The hydrodynamic sizes of MPs were measured by dynamic laser scattering using a BI-200 SM Goniometer Version 2 (Brookhaven Instrument Corp., Holtsville, NY, USA). To estimate the amount of PAA on MPs, TG analysis was performed using a Shimadzu TGA-50 TG analyzer (Shimadzu, Japan). Experimental procedures and calculations are provided in the Supporting Information. The images of PAA coating on MPs were recorded on a JEM 2100 LaB6 transmission electron microscope (JEOL, Tokyo, Japan). The magnetic properties of the MPs were determined by VSM (VSM 7400, LakeShore Cryotronics, Inc.). ζ-potential of MPs was measured by laser Doppler velocimetry using a Nano ZS90 Zetasizer (Malvern, UK). One-step MPs were suspended at 0.1 mg/mL using 10 mM phosphate buffer (pH 7.0) and subjected to ζ-potential measurements. The electrophoretic mobility of each sample (prepared in triplicates) was measured three times. Each time, at least 15 runs were performed. The data are reported in mV.65 4.4. Magnetic Collection of MPs in Water. Five milligrams of the MPs were resuspended in 10 mL of water in scintillation vials (27 mm × 61 mm) by sonication for 5 min. A N48 neodymium disc magnet (13 mm × 3 mm) was placed on the sidewall of each vial. Magnetically collected MPs were separated from the supernatant of each sample and weighed at selected time points (10 min, 12, and 24 h). 4.5. Protein Conjugation of MPs. The conjugation of proteins to MPs was performed in MES buffer through EDC cross-linking. Three milligrams of MPs, 1800 μL of MES buffer (50 mM, pH 4.7), and 210 μL of EDC solution (200 mg/mL in 50 mM pH 4.7 MES buffer) were mixed for 30 min. Then, the MPs were magnetically separated from the solution and mixed with 3 mL of protein solutions (3 mg/mL in 50 mM pH 7.0 MES buffer) for 50 min. The resultant MPs−protein conjugates were separated from the liquid magnetically. The amount of protein conjugated to MPs was calculated by comparing the difference in the concentration of protein before and after conjugation.66 The protein concentration was measured by absorbance at 280 nm with an ultraviolet−visible spectrophotometer (DU-730, Beckman Coulter Inc., Fullerton, CA, USA). 4.6. Statistical Analysis. All measurements were carried out in triplicate. Data was calculated and reported as mean ± standard deviation for each treatment. The mean values of properties of different MPs were compared by one-way analysis

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsomega.8b02351. XRD patterns of one-step hydrothermally synthesized bare MPs, PAA-MPs, and Fe3O4, TG analysis, XRD patterns of two-step hydrothermally synthesized 1.8kMPs (aged 15 days), SEM images of posthydrothermalcoated 30k-MPs, Ms of MPs synthesized via one-step and two-step hydrothermal reactions and posthydrothermal coating process, and photographs of magnetic collection of two-step MPs and posthydrothermalcoated MPs in their water suspensions at 10 min, 12 h, and 24 h of magnet application (PDF)

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. Phone: +86 (028) 8772-0550 (X.C.). *E-mail: [email protected]. Phone: (301) 405-8421. Fax: (301)-314-3313 (Q.W.). ORCID

Ying Li: 0000-0001-6622-2915 Zi Teng: 0000-0002-6029-7024 Qin Wang: 0000-0002-7496-3921 Present Address ⊥

10300 Baltimore Ave, Nutrient Data Laboratory, Beltsville Human Nutrition Research Center, Agriculture Research Service, US Department of Agriculture, Beltsville, Maryland 20705, United States. Author Contributions §

Co-first author.

Funding

The authors gratefully acknowledge the financial support from the USDA-National Institute of Food Agriculture (no: 201467021-21585). Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We appreciate the support of the Maryland NanoCenter, Juan Pablo Hurtado Padilla, and Dr Wen-An Chiou for their professional assistance on SEM imaging, Dr Jessica Terrell and Dr Chen-Yu Tsao for offering EGFP, E. coli, and technical support, and Dr. Peter Zavalij for interpretation of XRD results.

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ABBREVIATIONS MPs, magnetic microparticles; PAA, poly(acrylic acid); MRI, magnetic resonance imaging; HGMS, high gradient magnetic separation; Mw, molecular weight; SEM, scanning electron microscopy; DLS, dynamic light scattering; PDF, powder diffraction file; ICDD, The International Centre for Diffraction Data; XRD, X-ray powder diffraction; ANOVA, analysis of variance; EDC, 1-ethyl-3-(3-dimethylaminopropyl)carbodiimide; VSM, vibrating sample magnetometry; Mr, 17911


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remanent magnetization; Ms, saturation magnetization; Hc, coercivity; ms, the saturation magnetic moment; EGFP, enhanced green fluorescent protein; MES, 2-(N-morpholino)-ethanesulfonic acid; PBS, phosphate buffered saline; AB, antibody

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REFERENCES

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