Polydopamine-Coated Magnetic Iron Oxide Nanoparticles

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1		giulia siciliano	--	2445	2022-05-02 12:40:41	\|
2	format change	Peter Tang	+ 47 word(s)	2492	2022-05-05 11:54:29	\|

This entry is adapted from the peer-reviewed paper 10.3390/nano12071145

Magnetic iron oxide nanoparticles have been extensively investigated due to their applications in various fields such as biomedicine, sensing, and environmental remediation. However, they need to be coated with a suitable material in order to make them biocompatible and to add new functionalities on their surface. Polydopamine is a highly biocompatible bioinspired material that can be easily deposited on various substrates with a good control on film thickness. The functional groups on its surface (catechol, carboxylic groups amine and imine) can be used to bind specific molecules or to load transition metal ions.

magnetic nanoparticles iron oxide nanoparticles polydopamine surface functionalization bioinspired nanomaterials

1. Introduction

In the last decades, magnetic nanoparticles (MNPs) have been extensively investigated due to their various applications in fields such as biomedicine ^[1], hyperthermia ^[2], catalysis ^[3], wastewater treatment ^[4], and spintronics ^[5]^[6]. Among them, iron oxide nanoparticles have attracted major attention because of their magnetic properties, chemical stability, tuneable morphology, and ease of surface functionalization ^[7]. However, these nanoparticles need to be coated with a suitable material in order to prevent agglomeration or to add new functionalities on their surface. Surface modification can be carried out in different ways and using various biomaterials ^[8]. Typical purposes are to obtain in a single step reaction: the available material, the use of water as a solvent, and a coating exploitable for secondary functionalization with specific molecules. Taking inspiration from the adhesion properties of mussels, a uniform coating platform based on the use of dopamine has been developed, leading to the use of polydopamine as a novel coating material ^[9]. Polydopamine is a highly biocompatible bioinspired material that can be easily deposited on various substrates with a good control on film thickness ^[10]. The functional groups on its surface (catechol, carboxylic groups amine and imine) can be used to bind specific molecules or to load transition metal ions. These unique properties make polydopamine convenient not only as a coating material, but also as an innovative biomaterial with applications in the fields of chemistry, biology, and material science ^[11].

2. Magnetic Nanoparticles: Synthesis and Functionalization

Magnetic nanoparticles with specific features can be obtained using ferromagnetic elements such as Fe, Ni, Co or metal oxides (Fe₂O₃, Fe₃O₄), alloys (CoPt, FePt), and ferrites (MnFe₂O₄, CoFe₂O₄).

The electronic and magnetic properties of nanoparticles depend on their size ^[12]. In particular, finite-size effects derived from the electron quantum confinement, and surface effects related to the symmetry of the crystal structure, dominate the nanoparticles’ magnetic properties. Large particles have a multi-magnetic domain structure, with a remanent magnetization in the absence of an external magnetic field, and exhibit a ferromagnetic behavior. Decreasing the particle size to the nanoscale (typically around 10–25 nm) results in a single magnetic domain structure with all the spins lined in the same direction, but with a superparamagnetic behavior ^[13]. When an external magnetic field is absent, superparamagnetic nanoparticles exhibit zero magnetization, no coercivity, and less tendency to agglomerate at room temperature, which makes them good candidates for biomedical and adsorptive applications. However, for magnetic separation, particles with ferromagnetic properties are mainly used ^[14].

The strong connection between the size, the shape, and the magnetic properties of the nanoparticles leads to the development of a wide number of synthetic procedures to achieve high crystallinity, a narrow size distribution, uniform morphology, and tuneable properties ^[15]. Magnetic nanoparticles can be obtained by physical or chemical methods. Physical strategies include top-down approaches, leading to nano-sized materials from bulk materials (molecular beam epitaxy ^[16], chemical vapour deposition ^[17], and spray pyrolysis ^[18]). The main disadvantage of these techniques is the formation of powders with a wide side distribution. Chemical methods involve, on the contrary, bottom-up approaches, since they use molecular precursors to synthetize nanocrystals. Chemical methods for the synthesis of high-quality magnetic nanoparticles include co-precipitation ^[19], microemulsion ^[20], hydrothermal treatment ^[21], and thermal decomposition in the presence of molecular precursors ^[22]. The co-precipitation method is extensively used for the synthesis of MNPs, with a good control on size and magnetic properties for biomedical applications. However, MNPs obtained by this technique tend to agglomerate because of their small particle size ^[19]. The microemulsion technique allows for the obtainment of MNPs, with a good control over size and composition and high saturation magnetization. However, the type of surfactant used affects nanoparticles’ properties, and represents a great disadvantage ^[20]. The hydrothermal or solvothermal method is mainly used for the synthesis of ultrafine powder and crystals of different materials. For example, Zheng et al. ^[23] have reported the hydrothermal synthesis of Fe₃O₄ NPs in the presence of sodium bis (2-ethylhexyl) sulfosuccinate as surfactant. The main disadvantage associated with this synthetic route is that nanoparticles smaller than 10 nm in size cannot be obtained ^[21]. Among the various chemical methods used for the fabrication of MNPs, the thermal decomposition of organometallic precursors in the presence of stabilizing agents such as surfactants best allows the synthesis of inorganic nanoparticles in a wide range of composition, including oxides, metals, and semiconductors, with a good control of their size, shape, size dispersion, crystallinity, and, accordingly, the resulting physicochemical properties. MNPs obtained by means of such synthetic approaches are dispersible in organic solvent, and require post-synthetic treatments for their application in biological fields ^[22]. Alivisatos et al. ^[24] reported the synthesis of maghemite nanocrystals with size of 4–10 nm by the thermal decomposition of iron cupferron complexes (FeCup₃). Very recently, the γ-irradiation method, commonly named as the radiolytic method, has emerged as a new green synthetic route for magnetic oxides, exploiting the interaction between high energy γ-photons and an aqueous phase ^[25]. Recently, Jurkin et al. ^[26] have reported for the first time the synthesis of δ-FeOOH nanodiscs by γ-irradiation of a deoxygenate iron(III) chloride alkaline solution in the presence of diethylaminoethyl-dextran (DEAE-dextran) polymer, which is able to disperse the NPs and form colloidal solutions rather than suspensions.

Magnetic nanoparticles derived from iron, in the form of magnetite (Fe₃O₄) or maghemite (γ-Fe₂O₃), are the most extensively studied in the last decades, and have become promising candidates for various applications because of their magnetic properties, chemical stability, low toxicity, biological compatibility, tuneable size, and particle shapes that can be controlled by varying the synthesis conditions, as well as the fact that they can be easily coated by surface functionalization ^[27].

For most applications, the chemical stability of magnetic nanoparticles is crucial in order to prevent agglomeration, precipitation, or oxidation. Moreover, their surface functionalization is essential not only to make them stable against degradation, but also to convey additional properties that enable their specific activity towards target cells, such as tumor cells in order to address hyperthermia, towards biological ligands for the development of electrochemical sensors, and also towards pollutants for the uptake of contaminants from water, thus leading to the fabrication of various nanocomposites with applications in many technological fields ^[28]^[29]^[30]^[31]^[32]. The strategies developed for the protection of magnetic nanoparticles, their surface engineering, and their integration in functional structures and materials, can be divided into two major groups: surface coating with inorganic materials (silica shell ^[33]^[34], carbon ^[35]^[36], metals ^[37]) and coating with organic materials (surfactants, polymers ^[38]^[39]^[40]^[41]). In recent years, biopolymers including cellulose, alginate, chitosan, polyethylene glycol (PEG), and synthetic eumelanin-type biopolymers such as mussel-inspired polydopamine (PDA) have received much more attention for MNPs coating owing to their physicochemical properties, which are useful for different applications in various research areas. Surface modification of MNPs can be carried out by two main strategies, i.e., in situ and ex situ processes ^[42]. In the case of in situ surface functionalization, the coating is carried out during the synthesis of nanoparticles and it starts at the same time of nucleation, avoiding further growth of MNPs ^[42]. Generally, nanocomposites obtained this way have core-shell or mosaic structures ^[43] with a variable polymer shell in terms of morphology and thickness. The ex situ surface functionalization procedure, on the contrary, relies on two different stages: the synthesis of nanoparticles and their successive coating with biopolymers, allowing for better control of the nanocomposites’ morphology. In both cases, the interactions attending the adsorption mechanism of biopolymers on the surface of MNPs are mainly electrostatic and hydrophobic interactions, and hydrogen bonding ^[42]. All strategies available for the surface functionalization of MNPs lead to several magnetic bio-nanocomposites characterized by different structures, including core-shell, shell-core-shell, multicores or matrix-dispersed structures, and Janus-type hetero-structures ^[44]^[45]^[46]^[47]^[48]^[49].

3. Polydopamine Functionalized Iron Oxide Nanoparticles: Synthesis and Structures

Among the various biomaterials used for the protection and functionalization of magnetic nanoparticles, polydopamine—a mimic of the adhesive foot protein secreted from mussels—has stimulated extensive research in recent years for the surface modification of many inorganic and organic materials, because it shows much more flexibility and designability in the target structures compared to other biopolymers, and has singular features and physicochemical properties. Since polydopamine is the major pigment of eumelanin, it is biocompatible and displays many characteristics of natural melanin in terms of optical (UV absorption as photoprotective agent) and electrical properties ^[50]. One of the most exploited properties of polydopamine is its strong adhesion to all types of substrates, thanks to the many functional groups, such as imine, amine, and catechol incorporated in its structure. The catechol moieties in PDA have a certain redox activity that can be used both for transition metal binding and for covalent bonding with specific molecules, leading to the fabrication of diverse hybrid materials with powerful reducing capability towards metal ions such as Mn²⁺, Cu²⁺, and Zn²⁺. Moreover, the functional groups present in its chemical structure can react with various molecules, allowing the manufacture of heterostructures with applications in different fields. Finally, PDA has excellent biocompatibility, a crucial factor for specific applications in the biomedical field ^[50].

In light of these properties, a wide number of polydopamine-derived hybrid materials have been developed for diverse applications, including energy (solar cells ^[51], catalysts ^[52], supercapacitors ^[53]), the biomedical field (cells adhesion ^[54], antibacterial activity ^[55], photothermal therapy ^[56], bioimaging ^[57], drug delivery ^[58]), water treatment ^[59]^[60], and sensing ^[61]^[62]^[63].

The synthesis of polydopamine/iron oxides (PDA/Fe₃O₄) core-shell nanoparticles has been widely investigated in recent years. PDA/Fe₃O₄ core-shell nanospheres can be synthetized by the precipitation method ^[59], with PDA nanoparticles acting as templates. On the other hand, introducing a dopamine solution into an Fe₃O₄ suspension can result in magnetic nanoparticles coated by a polydopamine shell with a good control on the shell thickness. In these conditions, dopamine could form –COO–NH₂–ion pairs because of the carboxyl groups on Fe₃O₄ surface, and could generate a polymeric shell under basic conditions, leading to the formation of well-defined core/shell structures ^[64]. There are advantages and limitations related to these two approaches. In particular, the first method is useful for synthesizing iron oxide nanostructures after removing polydopamine. On the other hand, the second approach presents three valuable features. First, multicore nanostructures can be obtained, where polydopamine shell encapsulates magnetic nanoparticles. Second, since magnetic iron oxide nanoparticles tend to aggregate and can biodegrade when they are in biological systems, polydopamine shell can prevent their biodegradation and their direct contact with biological systems. Moreover, polydopamine shell, thanks to its chemistry and reducing ability, is a versatile platform for the surface modification of the inorganic core.

The polymerization process of PDA shell around the surface of iron oxide nanoparticles is affected by parameters such as the dopamine monomer concentration, the pH value, and the type of buffer and oxidation agent used. Usually, polydopamine is synthetized by a solution oxidation method, whereby the dopamine monomers (typically dopamine hydrochloride), added into an alkaline solution (generally tris(hydroxymethil)-aminomethane (Tris) buffer (pH 8.5)), are oxidized and spontaneously self-polymerize. The polymerization process can be easily monitored by a color change of the solution, from colorless to deep brown. Dopamine concentration considerably affects the morphology of PDA nanoparticles and the characteristics of film deposition. Increasing the dopamine monomer concentration from 0.1 to 5 g L⁻¹ results in an increase of the PDA shell thickness from a few nm to a maximum of about 50 nm ^[65], but also in an increase of the coating’s surface roughness. However, using dopamine concentrations lower than 0.5 g L⁻¹ for functionalizing iron oxide nanoparticles allows the reduction of the formation of insoluble PDA aggregates formed during the synthesis, and the increase of PDA shell roughness. Another factor affecting the polymerization process is the type of buffer used. Recent studies have demonstrated that using Tris-HCl buffer instead of sodium bicarbonate (NaHCO₃) and phosphate buffers, leads to the incorporation of Tris into the dopamine structure via covalent coupling between the primary amine of Tris and the dopamine-quinone intermediate, which is significant during the polymerization process ^[50]. The use of sodium hydroxide (NaOH) aqueous solutions instead of the above-mentioned buffers allows the preparation of PDA nanoparticles with good colloidal stability and a size lower than 100 nm. However, in all cases, the formation of large PDA aggregates can be observed, and additional purification steps are necessary for their removal from the final preparation ^[50]. In addition to these two parameters, the effect of the solution pH value must be considered. In fact, at basic pH, a consumption of the produced hydrogen protons can be observed as the PDA synthesis progresses, thus allowing the shifting of the redox equilibrium towards PDA production ^[50]. Therefore, an increase of the initial pH results in an increase of the PDA shell thickness in the case of coatings, and in a particle size reduction in the case of PDA nanoparticles production ^[50].

Owing to its described properties, polydopamine is an ideal candidate for the fabrication of hybrid materials with specific functionalities. The following sections will give some illustrative examples in order to describe the potential applications of polydopamine-coated magnetic iron oxide nanoparticles across the fields of bioremediation, biomedicine, and sensing.

4. Technological Applications of Polydopamine Functionalized Iron Oxide Nanoparticles

The use of nanoparticles for applications in the field of remediation, biomedicine, and sensing has been extensively researched in the last years, yielding significant advancement in the development of ultrasensitive nanosystems, as confirmed by the great number of publications (Tables 1, 2 and 3).

Table 1. Fe₃O₄@PDA nanocomposites for the uptake of organic and inorganic pollutants.

Biosorbent	Pollutants	Adsorption Capacity (mg/g)	pH	Reference
PDA-coated graphene oxide/Fe₃O₄ imprinted nanoparticles	Sulfonylurea	3.176	-	^[66]
Sodium alginate@CoFe₂O₄-PDA beads	Malachite green	248.8
Sodium alginate@CoFe₂O₄-PDA beads	Crystal violet Methylene blue	456.5 466.6	4	^[67]
PDA-coated graphene oxide/Fe₃O₄ imprinted nanoparticles	fluoroquinolone antibiotics	70.90	8	^[68]
Fe₃O₄@PDA@TiO₂ nanoparticles	U(VI)	87.74	8.2	^[69]
Fe₃O₄@PDA microspheres	Cd(II)	296.4	6	^[70]

Table 2. Fe₃O₄@PDA nanocomposites for biomedical applications.

Bionanocomposite	Application	Reference
Core-shell Fe₃O₄ polydopamine nanoparticles	pH responsive drug delivery	^[71]
Core-shell Fe₃O₄ polydopamine nanoparticles	Intracellular mRNA detection	^[39]
Nanoclusters@PDA-PEG@ICG	Cancer therapy	^[72]
Polydopamine-coated magnetic mesoporous silica nanoparticles	Multimode cancer theranostic	^[28]
IONPs@PDA	Drug delivery system for cancer therapy	^[73]
Polydopamine (PDA)-coated magnetite nanoparticles (NPs) and spheres (sMAG) with PAMAM dendrimers	Hepatocellular carcinoma treatment	^[74]
PDA-coated iron oxide nanorods	Drug delivery system for cancer therapy	^[75]
Porous Fe₃O₄@PDA-PEG nanocomposite	Magnetic resonance (MR) imaging Photothermal therapy (PTT) Chemotherapy	^[76]

Table 3. Fe₃O₄@PDA nanocomposites for sensing applications.

Bionanocomposite	Application	Analyte	Reference
Fe₃O₄@PDA nanoparticles	Recognition and separation	Haemoglobin	^[77]
Core–shell glucose oxidase–Au–PDA–Fe₃O₄ nanoparticles	Glucose sensor	Glucose	^[78]
PDA@Fe₃O₄ MIP (Molecularly Imprinted Polymer)	Electrochemical biosensor	Thionine	^[79]
Fe₃O₄@PDA@MnO₂	Electrochemical sensor	Pb²⁺	^[80]
PDA@Fe₃O₄ MIP	Impedance sensor	Dichlorodiphenyltrichloroethane (DDT)	^[81]

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giulia siciliano

Giuseppe Maruccio

Anna Grazia Monteduro

Antonio Turco

Elisabetta Primiceri

Silvia Rizzato

Nicoletta Depalo

Maria Lucia Curri

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Update Date: 05 May 2022

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