Composite magnetic plasmonic nanoparticles for biomedicine: Manipulation and imaging

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1 Nano Today (2013) 8, Available online at journal homepage: REVIEW Composite magnetic plasmonic nanoparticles for biomedicine: Manipulation and imaging JitKang Lim a,b,, Sara A. Majetich b, a School of Chemical Engineering, Universiti Sains Malaysia, Nibong Tebal 14213, Penang, Malaysia b Physics Department, Carnegie Mellon University, Pittsburgh, PA 15213, USA Received 19 September 2012; received in revised form 13 November 2012; accepted 27 December 2012 Available online 12 February 2013 KEYWORDS Iron oxide gold nanoparticles; Surface plasmon resonance; Magnetophoresis; Colloidal stability; Core shell; Biomedical Summary Iron oxide gold nanoparticles that exhibit both magnetic and plasmonic behaviors have great potential for biomedical applications. The ability to remotely control the spatial position of a nanoparticle in real time while tracking its motion provides an exciting new tool for nanoscale sensing. In this review we summarize the major efforts in the design and synthesis of iron oxide gold nanoparticles. The underlying magnetophoretic and plasmonic characteristics of gold and iron oxide nanoparticles that enable their use for biomedical applications are described. We discuss the challenges associated with the integration of iron oxide and gold in one unified nanostructure, including the chemical techniques involved in making such composite material. We emphasize on the importance of colloidal stability, and explain how this property determines the functionality of iron oxide gold nanoparticles in physiological environment. Afterwards, we examine both the magnetophoresis and localized surface plasmon resonance of iron oxide core gold shell structure and provide theoretical explanations for these properties. Finally we suggest potential opportunities for use of iron oxide gold nanoparticles Elsevier Ltd. All rights reserved. Introduction Single particle sensing offers the possibility of probing small samples in precisely defined regions near, on, or within Corresponding author at: School of Chemical Engineering, Universiti Sains Malaysia, Nibong Tebal 14300, Penang, Malaysia. Tel.: ; fax: Corresponding author at: 5000 Forbes Ave., Physics Department, Carnegie Mellon University, Pittsburgh, PA 15213, USA. Tel.: ; fax: addresses: (J. Lim), (S.A. Majetich). biological cells. The ability to magnetically guide and manipulate the motion of individual particles is crucially important to modulate cellular behavior in a non-contact mode [1]. However, the techniques most commonly used to manipulate particles, including electrophoresis [2,3], dielectrophoresis [4,5], traveling-wave dielectrophoresis [6], magnetic tweezers [7] and acoustic traps [8], are focused mainly on the manipulation of micron size objects. Successful application of these schemes in manipulating the motion of nanoparticles (NPs) is quite challenging because nano-sized particles are extremely susceptible to Brownian motion [9] and inertial forces associated with their motion are negligible (i.e., they move with low Reynolds number) [10]. While optical tweezers offer high-resolution control of colloidal particles /$ see front matter 2013 Elsevier Ltd. All rights reserved.

2 Magnetic-plasmonic nanoparticles 99 from micron size down to a few nanometers [11], they have a limited manipulation area due to tight focusing requirements [12], and it is hard to implement them into a portable microfluidic system. Composite magnetic plasmonic NPs have advantages in two niche areas. First, for ex vivo studies, the bifunctionality gives the potential to move particles magnetically while imaging them optically. With dimensions approaching the size of important biological targets, including large proteins or protein clusters ( 5 50 nm), genes ( nm), or organelles ( nm), the NPs provide the ability to directly probe the activities associated to these important entities under magnetophoretic guidance while simultaneously providing visual feedback through its plasmonic signal. The ability to control the motion of NPs while imaging them on a submicron scale could be very important, for example in understanding the intracellular trafficking and gene transfection for gene therapy [13], where magnetic NPs are employed as DNA carriers [14]. Because the particles are small, this could be done within living cells [15]. Second, the magnetic plasmonic NPs could be used for increased range in selective binding. Cells that expressed a large number of receptor groups could be more easily differentiated from those with only a few, and the smaller NPs would block fewer unbound receptor sites. The design and synthesis of NPs suitable for controlled manipulation and single particle sensing requires two key behaviors; here we will focus on magnetophoretic motion control and optical imaging via the localized surface plasmon resonance (LSPR) [16]. A key advantage of magnetism here lies in the ability to control motion at a distance without perturbing the biological system, as would occur with a large electric field and the feasibility of integration into a microfluidic system. Noble metal nanostructures are beneficial not only because of their relative ease of biofunctionalization, high chemical stability, biocompatibility, but also for plasmonic biosensing, i.e., the detection of biomolecular targets via a shift in the LSPR spectrum [17,18]. Unlike organic fluorophores or luminescent semiconductor quantum dots, noble metal NPs are used for sensing via their scattering and extinction cross-sections. The main advantages of plasmonic particles are their extremely large molar extinction coefficients and resonant Rayleigh scattering efficiencies [19], and the exceptional sensitivity of the surface plasmon resonance peak wavelength to changes in the local dielectric environment [20]. Noble metal NPs do not photobleach, as do organic fluorophores, nor do they show the optical bistability or blinking exhibited by quantum dots [21]. Blinking can be problematic when tracking single particles using automated image tracking algorithms. In addition, noble metal NPs also do not share the high risk of toxicity associated with semiconductor quantum dots [22]. Understanding the requirements for rapid magnetic manipulation of NPs while imaging them by their LSPR response at the microscale, and developing suitable particles, is the focus of this review. There are a number of related review articles, including two that provide perspectives on the growth mechanisms of core shell nanoparticles [23] and fluorescence coupling in magnetic and plasmonic nanoparticles [24], and two that showcase the synthesis of a variety of heterogeneous structures, including iron oxide gold [25,26]. Magnetic nanoparticles for biomedicine A group of superparamagnetic particles will respond to an applied magnetic field, but will not have a net magnetization in the absence of a field. Most of the magnetic NPs used in biomedical applications are superparamagnetic at room temperature. This is important for any use that requires them to be suspended in a liquid, since a magnetic attraction between particles would promote flocculation and then sedimentation. For magnetite (Fe 3 O 4 ) particles at room temperature, the maximum superparamagnetic size is 35 nm in diameter [27]. The magnetic force F mag acting on a point-like magnetic dipole moment m is described by [28]: F mag = (m )B. (1) For example, if m =(m x, 0, 0) then m =m x ( / x) and a magnetic force will be experienced by the magnetic dipole m if there is a magnetic field gradient in db/dx in the x- direction. A magnetic field gradient is required to exert a force at a distance to induce the motion of the NP, whereas a uniform field gives rise to a torque but no translational motion [29]. The total moment of the particle can be written as [30], m = V mag M, where V mag is the volume of the magnetic materials (for core shell particle, V m represents the volume of its iron oxide core only) and M is its volumetric magnetization. The particle is free to rotate in its suspension medium, and its magnetization M is induced by the externally applied magnetic field with strength H, M = H,where is effective magnetic susceptibility of the particle relative to the medium. In an isotropic, weakly diamagnetic medium such as water, the magnetic field H and B differ only by a constant multiplicative factor, the magnetic permeability of vacuum 0, B = 0 H. Combining all the equations above gives: F mag = (m )B = V m (H )B = V mag (B )B. (2) 0 Eq. (2) provides the magnetophoretic force F mag experienced by a magnetic particle in a given magnetic field gradient. Intracellular magnetophoretic control of quantum dots coated by 4 nm iron oxide particles has been successfully demonstrated by Gao and co-workers (Fig. 1) [31]. However, up to 8 h was needed to drive the internalized particles across the cell when using a permanent magnet with a surface magnetic field of 3000 G, due to the extremely small size of the iron oxide particles. Magnetophoretic control for intracellular sensing requires a response on the time scale of cellular responses to stimuli in order to be useful. If NPs are to be used to probe biological cells, their motion must be controllable over length scales of a few micrometers, the size of typical eukaryotic cells. Under this scenario 4 nm can be viewed as a lower size limit for the magnetic particles. Since magnetophoretic force is directly proportional to the magnetic volume of the particle (Eq. (2)), hence, magnetite particles close to 35 nm approaching the superparamagnetic limit are desirable. In addition, magnetophoresis could also

3 100 J. Lim, S.A. Majetich Figure 1 Optical micrograph showing intracellular magnetic collection of quantum dots coated magnetite nanoparticles demonstrated by Gao and co-workers [31]. After the HEK293T cells are incubated with the Fe 3 O 4 nanoparticles and pegfp-n1 vector, these confocal images were taken of the cell (A) without a magnetic field (homogeneous fluorescent spots suggesting that the nanoparticles mainly distribute in the cytosol) and (B) under a magnetic field for 8 h. Copyright 2008 American Chemical Society. Reprinted with permission from [31]. provide extra controllability in manipulating nanoparticle such as for angular particle positioning and rotational control [32]. Magnetic NPs are used or being investigated for use in many areas of biomedicine [33 35]. As magnetic resonance imaging (MRI) contrast agents [36], their inhomogeneous magnetic field generated by the particles helps to differentiate protons in water molecules from those in tissue. In magnetic cell sorting [37], intracellular tracking [38], and guidance [31], there is a force on the particle from an external magnetic field and the particle is designed for selective binding of a biological species. In magnetic drug delivery [39,40] or gene therapy [41], the magnetic force acts on a particle bound to specific drug or gene, respectively. Finally, in magnetic hyperthermia, an AC magnetic field generates local heating near the particles, and if they are located near cancer cells they can kill them or make them more susceptible to chemotherapy or radiation [42]. The most common magnetic material for the particles is Fe 3 O 4, which the only ferro- or ferrimagnetic nanoparticle approved by the FDA for in vivo use. Plasmonic nanoparticles for biomedicine Noble metal NPs display a strong optical absorbance when the incident photon frequency is in resonance with the collective excitation of the conduction electrons, setting up the condition of localized surface plasmon resonance (LSPR) illustrated in Fig. 2. The plasmon mode of a noble metal such as gold falls in the visible spectral region. The LSPR gives the distinct ruby red color to many gold colloid suspensions. The resonant frequency is strongly dependent on the nanoparticle size [43,44] and shape [43,45], as well as the local dielectric properties of the surrounding medium [20,46]. This plasmon mode of a noble metal such as gold falls in the visible spectral region, making them an ideal candidate for applications in the field of surface enhanced Raman scattering [47], chemical sensors [48], and biological sensors [49]. The size and shape dependence of the LSPR set the most important constraints on the design and synthesis of the core shell particles. The LSPR absorbance curve would undergo significant broadening if the particle suspension

4 Magnetic-plasmonic nanoparticles 101 Figure 2 A scheme illustrating the excitation of the dipole surface plasmon oscillation [43]. The electric field of the incoming light induces a polarization of the free conduction electrons (gray area) with respect to the much heavier ionic core of a gold nanoparticle (dark sphere). The extension of the charge cloud is not to scale. were composed of a mixture of particles with different sizes (high polydispersity) [43]. The same scenario applies to the shape uniformity as well. A mixture of particles with different shapes is also going to exhibit broadening of the LSPR absorbance curve [45]. For any sensing purpose the signal employed for detection should be well defined. Hence, monodisperse particles with uniform shape are greatly desired to produce as sharp an LSPR spectrum as possible. The presence of LSPR makes direct imaging/tracking of noble metal NPs with sizes much smaller than diffraction limit possible by using darkfield optical microscopy. For an example, Van Duyne and co-workers [20] have successfully imaged 35 nm silver particles immobilized on top of a microscope coverslip. In addition, El-Sayed and co-workers have also demonstrated the potential of anti-egfr antibody conjugated gold NPs in cancer diagnostics relying on SPR scattering and absorption [50] (Fig. 3). Gold particles are also used in biomedicine. Their localized surface plasmon resonance is not vulnerable to photo-bleaching effects after prolonged and/or high intensity illumination compared to conventional fluorescent tags. Due to the exceptional sensitivity of the surface plasmon peak wavelength to changes in local dielectric environment, Au nanoparticles are an ideal candidate for biosensing and ex vivo optical imaging. Using gold-coated silica particles with diameters 150 nm, Hirsch and co-workers have demonstrated the capability of gold shell nanoparticle in detecting low concentration of analytes in whole blood [51]. Having gold as outer-shell is also beneficial since gold is non-toxic and chemically inert [52], and surface biofunctionalization, through either physisorption or wellestablished thiol chemistry is relatively easy [53]. Gold nanoshell particles have also been employed to provide rapid heating for near infrared photothermal cancer therapy [54,55]. Figure 3 Light scattering images and microabsorption spectra of HaCaT noncancerous cells (left column), HOC cancerous cells (middle column), and HSC cancerous cells (right column) after incubation with anti-egfr antibody conjugated gold nanoparticles. The figure shows clearly distinguished difference for the scattering images from the noncancerous cells (left column) and the cancerous cells (right two columns). The conjugated nanoparticles bind specifically with high concentrations to the surface of the cancer cells (right two columns). Conjugated nanoparticles did not show aggregation tendency (no long wavelength broad tail is observed). Copyright 2005 American Chemical Society. Reprinted with permission from [50].

5 102 J. Lim, S.A. Majetich Challenges in combining magnetic and plasmonic particles for biomedicine There are numerous challenges in the development of magnetic plasmonic NPs. Successfully applying magnetic NPs for in vitro biosensing, requires the particles to (1) be magnetically responsive within the times scale appropriate to the phenomenon of interest, (2) emit a well defined signal that can be used for characterization purposes, and (3) maintain good colloidal stability in biological media of moderate to high ionic strength. The magnetic manipulation of nanoscale objects is challenging because magnetic NPs are susceptible to the thermal displacements [10]. This scenario is further complicated with the fact that the magnetic, viscous drag and random Brownian forces scale differently with the particle size [9,56]. To overcome contributions from both viscous drag forces and Brownian diffusion, extremely large magnetic field gradients are needed to induce magnetophoretic motion in deterministic pattern. Another critical challenge in controlling the transport of NPs is the need for a visualization scheme with which to track the motion [57]. Having gold as part of the composite NP enables the particle location to be monitored optically, since gold NPs have a very large molar extinction coefficient, greater than 10 5 M 1 cm 1 at wavelengths in the nm range [58]. Both the magnetic manipulation and plasmonic imaging require reliable techniques to synthesize particles that are uniform in size and shape. The size and shape of the constituent particles can have a dramatic effect on the magnetic properties (iron oxide volume and superparamagnetic threshold) and plasmonic behavior (gold shell thickness) and a high degree of uniformity is desired [59]. Furthermore, the particles must have a surface coating that enables them to form stable dispersions in biological media (0.15 M NaCl). This requires steric, rather than charge-based, stabilization [60,61]. As illustrated in Fig. 4, these factors are interrelated, and hence a holistic approach should be adopted. Design and synthesis of magnetic plasmonic nanoparticles The section Magnetic nanoparticles for biomedicine described the constraints on the magnetic particle size in order to maximize the magnetic force on the particle without causing agglomeration. There are other constraints for biocompatibility and chemical stability that favor Fe 3 O 4 as a material rather than the higher magnetization Fe or Co. The section Plasmonic nanoparticles for biomedicine showed that there were fewer constraints on the plasmonic properties, except that uniformity in the local dielectric environment was important if the SPR wavelength was used to detect binding of biomolecules. For selective binding applications the use of NPs with a non-continuous gold coating for plasmonic sensing is limited as its SPR absorbance spectrum is strongly retarded [62]. If the plasmon signal is only used as a location marker, this requirement becomes less critical. Introduction of a gold layer onto the surface of iron oxide NPs is extremely challenging due to the large surface energy of the gold [63], which tends to form separate gold particles. During the gold deposition process the iron oxide NPs often aggregate irreversibly as the reductive gold materials forming complexes with the particle surface and suppress its stabilizing agent (either a capping agents or electric double layers). In numerous papers describing combination magnetic plasmonic NPs, the electron microscopy clearly shows that there are separate magnetic and Au particles, due to the large difference in the atomic number Z, and therefore the electron transparency. Special care is needed to promote attachment of Au to iron oxide. For plasmonic sensing, there is often a requirement for the LSPR signal to be tuned to a specific wavelength; for a core shell structure this is achieved by controlling the gold shell thickness with respect to core diameter [64]. All these factors make the synthesis of magnetic plasmonic NP for biomedical applications extremely challenging. There are three particle morphologies that meet these requirements: (i) iron oxide NPs decorated with Au seeds clusters [65,66], (ii) iron oxide gold dumbell particles [67], and (iii) iron oxide core gold shell particles [68 71]. Each has the potential for a uniform magnetic and plasmonic structure, and each could be coated with polymers to form a stable dispersion in biological media. Other iron oxide/gold hybrid nanomaterials have also been developed, and have found niche uses, including gold core iron oxide shell nanoparticles with spherical [72] and rod-like [73] structures. Such hybrid materials were proven to be useful for protein separation and optical imaging or catalysis [72,74]. However, for biofunctionalization, there are no obvious advantages of having iron oxide on the outside. Large quantities of iron oxide particles decorated with Au seeds, up to a few liters at a time, can be prepared by gamma ray irradiation [65,74]. NPs prepared by using this method were used to selectively separate the sulfur-containing amino acids, cystine and methionine, by a permanent magnet [74]. Binary Fe oxide/au particles with a dumbbell morphology are formed through epitaxial growth of iron oxide on the Au seeds, and the growth can be affected by the polarity of the solvent [67]. The advantage of this structure is its magnetic and plasmonic properties can be fined tuned by regulating the size, structure and chemical nature of each part of the dumbbell through adjusting the synthetic conditions. Structures like this possesses tremendous potential for applications involving catalytic reactions [75]. According to Amal and co-workers [60] the synthesis of plasmonic magnetic core shell NPs involves two main processes:iron oxide core synthesis followed by gold coating. Methods of obtaining gold-coated magnetite can be categorized according to the variations in each process [60]. In some cases reverse micelles are used as confined reactors for both particle synthesis and gold coating [76 81]. However, this technique suffers from low yield and poor reproducibility. Another approach involves both synthesis and coating of NPs in the aqueous phase [82,83], with the iron oxide core synthesized via coprecipitation of iron salts in an alkaline environment followed by the direct reduction of chloroauric acid to form a gold outer shell. This aqueous method produces well-dispersed NPs in water and there is no need for phase transfer. The gold shell thickness formed by using this technique, however, is difficult to control and

6 Magnetic-plasmonic nanoparticles 103 Figure 4 Schematic diagram showing the critical factors involved in designing magnetic plasmonic composite nanoparticle with core shell structure to serve as a single particle sensor. Copyright 2008 Wiley-VCH, and copyright 2011 American Chemical Society. Reprinted (adapted) with permission from [9,62]. the final particle suspension contains a mixture of coated and uncoated iron oxide that has proven problematic to separate [60]. A third scenario involves the formation of an iron oxide core and gold shell in the organic phase [84 87]. In this method, the iron oxide core and gold shell can either be synthesized as one-pot technique [75] or independently [85]. Thermal decomposition of an iron precursor is used to synthesize magnetic NPs, and is followed by coating via reduction of gold precursor in the presence of capping agents. Organic phase methods usually result in NPs with a narrow size distribution and good colloidal stability. The particles, however, often aggregate when they are transferred into an aqueous environment [60]. In addition, thorough washing steps are needed to separate the final NPs from the simultaneously formed iron oxide and gold NPs [75]. Fig. 5 illustrates the variety of structures that can be formed, depending on the synthesis route. To achieve size control and viability in an aqueous environment, our group [59,62] and others [88] proposed the combination of organic phase synthesis of magnetic cores followed by gold coating of particles in an aqueous environment. This method produces NPs with good magnetic and plasmonic properties. With proper surface modification by using macromolecules, the particles would remain colloidally stable in physiological relevant environment for weeks [61]. This synthesis technique is illustrated in Fig. 6 and can be briefly described as follows. First, the iron oxide particle and small gold colloid are prepared in organic and aqueous phases, respectively. Later, the iron oxide NPs are phase transferred into aqueous environment by gently replacing its capping agents with the formation of electric double layers promoted by tetramethylammonium hydroxide [62]. After being electrostatically stabilized in aqueous environment, the iron oxide NPs are further functionalized with a ligand, typically with a thiol group, to promote gold seeding. Finally, more gold is further reduced onto the gold seeded iron oxide NPs to complete the shell. The typical dimensions for iron/iron oxide core gold shell NP by all the methods discussed can be found in Table 1. In addition to iron/iron oxide, other magnetic materials have also been employed as cores in the synthesis of gold shell structures, including cobalt [91,92], nickel [93,94], FeCo [95], and FePt [96]. Colloidal stability of Fe oxide/au core shell nanoparticles The use of magnetic NPs for biomedical applications will normally require the particles to be hydrophilic and maintain good colloidal stability in biological media [97]. For advanced biomedical applications of NPs (e.g., in vivo diagnostics and therapy), additional requirements such as minimization of non-specific uptake by reticuloendothelial systems (RES) must be imposed, in order to achieve long blood circulation time and high diagnostic or

7 104 J. Lim, S.A. Majetich Figure 5 Iron oxide gold NPs (a) synthesized by reverse micelle techniques, reprinted with permission from Ref. [78], copyright 2005 American Chemical Society, (b) synthesized by iterative hydroxylamine seeding, reprinted with permission from Ref. [79], copyright 2009 American Chemical Society, (c) synthesized by a modified thermal activation process, reprinted with permission from Ref. [83], copyright 2007 American Chemical Society, (d) synthesized by a step-by-step reactive decomposition method, reprinted with permission from Ref. [62], copyright 2008 Wiley-VCH, (e) synthesized by gamma-ray irradiation, reprinted with permission from Ref. [65], copyright 2005 Elsevier, (f) synthesized by an aqueous phase technique, reprinted with permission from Ref. [90], copyright 2009 American Chemical Society. Also in this figure are iron oxide gold NPs with different shapes, such as (g) dumbbells, reprinted with permission from Ref. [67], copyright 2005 American Chemical Society, (h) nanostars, reprinted with permission from Ref. [84], copyright 2010 American Chemical Society, and, (i) nanorods. Reprinted with permission from Ref. [10], copyright 2009 Elsevier. therapeutic efficiency [98]. Commonly used surface modification strategies for coating magnetic NPs with hydrophilic macromolecules include ligand exchange [99], micelle encapsulation [100], and covalent bonding [101]. A variety of macromolecules have been used to stabilize magnetic iron oxide NPs at elevated ionic strengths [102,103]. The most commonly used macromolecules are derivatives of dextran [102] or polyethylene glycol (PEG) [104], amphiphilic polyether triblock copolymers such as Pluronics [105], and proteins [106]. For example, covalent grafting of dopamine-modified PEG maintained the stability of 9 nm magnetite NPs in phosphate buffered saline (PBS) for up to 24 h. PEG silane is another popular candidate for covalent grafting of a stabilizer to iron oxide NPs [107]. For most of the above-mentioned stabilizers, covalent bonds or strong specific interactions between the stabilizer and the iron oxide surface were required. The simplest mechanism to provide steric stabilization is to physically adsorb water-soluble macromolecules to the particle [108]. Intermediate layers sometimes play a role in this

8 Magnetic-plasmonic nanoparticles 105 Figure 6 Major steps involved for core shell structure formation. (a) Synthesis of iron oxide NPs and gold colloid separately, (b) surface functionalization of iron oxide with ligands that promote the gold attachment, (c) gold seeds bind to the iron oxide NP, and (d) complete coarsening of a gold seeded iron oxide NP forming a core shell structure. process. For example, iron oxide NPs coated by oleic acid to promote their dispersibility in organic solvents subsequently can be dispersed into water by adsorbing a layer of Pluronic F127 triblock copolymer onto the modified nanoparticle surface [105]. Most of the prior literature on iron oxide nanoparticle stabilization in high ionic strength media takes a pragmatic approach, emphasizing short-term stability for immediate use of the particles. The long-term stability (days and beyond) is not typically reported. The main challenge is to overcome the van der Waals and long-range magnetic attractions by relying entirely on steric repulsions at ionic strengths where electrostatic double layer repulsions are insignificant. Almost all the initial studies of magnetic plasmonic NPs have been devoted to synthesis and characterization of their Table 1 Typical dimension of iron oxide core gold shell nanoparticles. Core materials (shape) Core diameter (nm) Gold shell thickness (nm) Reference Iron (spherical) [84,85] [73,86,87] Magnetite [70,76] (spherical) [66] [63] [89] Maghemite/ magnetite (spherical) Magnetite (cubic) Wustite (faceted and tetracubic) [78] [74] [56,57] [60,69] [55,118] [88] optical and magnetic properties [62,65,82,84,85,109]. Most of the iron oxide gold NPs synthesized are electrostatically stabilized in deionized water [59,62,82,110]. Screening of the electrostatic repulsion between NPs in biological media of elevated ionic strength necessitates the use of other stabilization schemes to prevent flocculation. It is not until recently that our group [61] and others [60] have successfully demonstrated the long-term stability of the NPs in physiological relevant environments. The magnetic and plasmonic properties of discrete NPs are well defined but change dramatically upon flocculation. Estimating the collective magnetophoretic mobility of a floc of such NPs is difficult and depends on the uncertain, and polydisperse, total amount of magnetic material in the flocs [111] and their shape [112]. The unmodified NPs form blue suspensions in DI water due to the optical properties and geometry of the core shell constituents as discussed previously. As the NPs flocculate to form clusters of varying size and shape, a rapid color change is observed due to the plasmon plasmon interaction among the closely spaced particles [113]. The plasmon coupling broadens and shifts the SPR peak to higher wavelengths [45]. Formation of flocs with different shapes furthermore produces higher order multipole terms that also contribute to the SPR spectral broadening [43]. All these scenarios have further complicated the use of SPR signal for sensing purposes, and hence, aggregation for particles should be avoided. There is a large body of literature focusing on the colloidal stability of NPs composed of iron oxide [ ] and gold [ ]. However, there are relatively few papers on colloidal stability of iron oxide gold NPs [60,61,123]. The choices of macromolecules to provide steric hindrance for iron oxide gold NPs are similar to those used for iron oxide particles and typical stabilizers include Pluronic [61], polyethylene glycol (PEG) [61] and polyethyleneimine (PEI) [60]. Dynamic light scattering (DLS) is employed as the major analytical method to verify successful attachment of the

9 106 J. Lim, S.A. Majetich Figure 7 Schematic representation of the synthesis of iron oxide core gold shell NPs by Goon and co-workers [60]. (a) Cationic polyethyleneimine (PEI) self-assembled onto negatively charged magnetite (Fe 3 O 4 ). (b) Fe 3 O 4 PEI mixed with Au seeds, to obtain (c) Au-seeded Fe 3 O 4, after which PEI is again added to obtain (d) PEI-coated Au-seeded Fe 3 O 4. (e) One addition of HAuCl 4 and NH 2 OH results in an uneven gold shell. (f) Four subsequent additions of HAuCl 4 and NH 2 OH PEI form an even gold coating. (g) PEI is then added to increase stability against aggregation. Copyright 2009 American Chemical Society. Reprinted with permission from Ref. [60]. macromolecules [61,118], and to monitor the long term colloidal stability of the suspension [61,124]. By monitoring the colloidal stability of surface functionalized NPs suspension for 5 days, our group found out that Pluronic F127 is an effective stabilizer. This polymer is capable of maintaining the stability of the NPs in high ionic phosphate buffer solution (ionic strength equivalent to 154 mm NaCl) compared to Pluronic F68, dextran, bovine serum albumin (BSA), PEG with 10,000 and 100,000 g/mol molecular weight [61]. Others [60] have reported the ability of PEI with molecular weight of 25,000 g/mol to provide stability against aggregation when compared to PEI with molecular weights of 800 and 600,000 g/mol. Pictorial representation of introducing PEI onto iron oxide core gold shell NP is shown in Fig. 7 and after four subsequent reduction steps to form an even gold coating, PEI is then added to increase the stability particles formed. It was also found that PEI has significantly improved the biocompatibility of the NPs which imparts positive effects on its physical characteristics, cellular uptake, gene expression efficiency, and cellular viability [124]. In this study the high cellular viability at 95 99% was observed for PEI coated NPs with a full gold shell at high magnetite loading of 50 g/ml compared to those bare NPs, PEI coated NPs and PEI coated, gold seeded NPs. The colloidal stability of the magnetic plasmonic NP suspensions against flocculation is governed by the forces between the particles. If the attraction is greater than the repulsion, particles would tend to flocculate and forming larger clusters which would eventually settle out from the solution. The effect of the gold shell and adsorbed polymer layer on nanoparticle stability can be interpreted in terms van der Waals (U vdw ) and magnetic (U mag ) attractions, and electrostatic double layer (U elec ) and steric (U steric ) repulsions [63]. The total interparticle interaction energy becomes [125]: U total = U vdw + U mag + U elec + U steric. (3) U tot is used to rationalize the extent of interaction between the particles [126,127]. To calculate the magnetic attraction, the iron oxide cores of the two interacting particles are assumed to have their magnetic spins perfectly aligned, providing an upper bound on U mag. Adding polymer to a particles suspension can promote stability or destabilize the suspension depending on the nature of interactions between the polymer, the solvent, and the dispersed particles [128]. In most of the previous work [60,61], the macromolecules were either physically adsorbed [61], or immobilized via electrostatic attachment [129]. The predicted interaction energy between NPs with 20 nm diameter iron oxide cores surrounded by 15 nm thick gold shells and stabilized by adsorbed Pluronic F127 in 154 mm PBS, is plotted in Fig. 8a. Steric repulsion is the main factor to prevent the particles from falling into a deep attractive well. The well is only about 0.4 kt deep. Aggregation is expected to be weak for well depths less than 1.5 kt [130]. Hence, any weak aggregation should be disrupted by thermal motion. This is consistent with the observation that Pluronic F127 coated particles were still unflocculated after 45 days in PBS [61]. Coating the iron oxide particle with a gold shell having a large Hamaker constant comes at the risk of increasing the van der Waals attraction between particles. Fig. 8b shows that the depth of the attractive well in U tot does increase with increasing gold shell thickness, but the well depth is still less than 1 kt for shells as thick as 20 nm. The desirability of strong steric repulsion is evident in preventing particle access to deeper attractive wells.

10 Magnetic-plasmonic nanoparticles 107 Figure 8 Extended DLVO interaction potential between two Fe/Au nanoparticles. (a) Total and contributing interactions for two particles with 20 nm iron oxide cores, 15 nm thick gold shells, and a 13.4 nm thick adsorbed Pluronic F127 layer. (b) Comparison of total interaction energy between for particles with 20 nm iron oxide cores and varying gold shell thicknesses. All have a 13.4 nm thick Pluronic F127 layer. Copyright 2009 American Chemical Society. Reprinted with permission from Ref. [61]. Magnetic and plasmonic properties of iron oxide core gold shell nanoparticles Rayleigh light scattering theory is applicable to particles smaller than the wavelength of incident light [131]. The threshold limit for the maximum particle size that can be modeled by the Rayleigh approximation is ((2r)/) 1, where r is the particle radius and is the wavelength of the incident light in the medium of interest. Though most of the Fe oxide/au NPs synthesized have diameters between 10 and 100 nm (Table 1), the gold shell is sufficiently thin to obey the Rayleigh approximation. The first theoretical prediction of the scattering by core shell particles was done by Aden and Kerker [132] in 1953, and recently, Halas and co-workers [133,134] revisited their model, providing a useful functional form for calculation. Our group extended it to the case of an iron oxide core and gold shell in a dielectric medium [62]. If the only two mechanisms for energy loss are scattering C sca, absorption C abs, their sum C ext,or the extinction cross-section, gives the total energy received by the particle from the incident wave [131]. The scattering cross section represents a hypothetical area surrounding the particle where every single photon that passes through it is scattered. Using the optical properties of gold [135] and iron oxide [136], the extinction cross sections of Fe oxide core/au shell NPs of various dimensions are shown in Fig. 9. As the thickness of the gold shell increases from 5 nm to 20 nm, for a magnetite core with 20 nm in diameter, the SPR peak blue shifts from 600 nm to 530 nm (Fig. 9a). The SPR peak for a 20 nm core and 20 nm gold thickness is similar to that for a solid 20 nm gold particle [137]. Under this condition, the surface plasmon of gold does not penetrate the thick shell enough to be influenced by the dielectric function of the core, but it remains sensitive to the variations in the dielectric function near the particle surface. If the core diameter is changed from 10 nm to 30 nm, the SPR peak undergoes a redshift from 535 nm to 655 nm (Fig. 9b). Hence, by fine-tuning the iron oxide core and gold shell ratio, theoretically, it is possible to design particle with SPR peak at any wavelength within the visible spectrum. Fig. 9c also shows that the UV vis absorbance spectrum for the Fe oxide core/au shell NPs (as shown in Fig. 5d) was similar to that predicted for a uniform 18 nm Fe 3 O 4 core and 5 nm thick Au shell in water. The evolution from isolated Au clusters into a complete shell shows the theoretically predicted redshift in the plasmon peak, as indicated in Fig. 9c. The width of the resonance is a measure of the particle homogeneity. During electroless deposition, but before completion of the shell, considerable spectral broadening occurs owing to the creation of clusters of various sizes. As the shell is completed, the particles become more uniform and the peak sharpens again. The wide range of colors displayed in Fig. 9d resulting from the variation in Au shell development allows for potential use of these nanoparticles for spectroscopic or colorimetric labeling [90]. In most cases, the plasmon peaks for Fe oxide core/au shell NPs occurred at absorbance wavelengths between 500 and 600 nm [82 86]. By using an iterative hydroxylamine seeding method, Lyon and co-workers [82] have synthesized Fe oxide core/au shell NPs with a very well defined SPR signal at 550 nm after six Au iteration steps. A one step thermal processing treatment can be employed to produce Fe oxide core/au shell NPs with equally good SPR signal at the same wavelength but with a thinner gold shell [86]. For an incomplete gold shell, depending on the size and packing density of the gold seeds, a more pronounced SPR peak [60,62] and a small shoulder or flat peak have both been observed [65]. After assembling the Fe oxide core/au shell NPs into a thin film, the SPR wavelength can be varied from 520 nm to 620 nm by changing the dielectric properties of the surrounding media [85]. The SPR signal of Fe oxide core/au shell NPs can also be fine tuned by changing the ph of its suspension medium [83]. The calculated C ext for a uniform 18 nm Fe 3 O 4 core and 5 nm thick Au shell in water at the SPR resonance frequency

11 108 J. Lim, S.A. Majetich Figure 9 Theoretical predictions for plasmonic spectral for (a) a 20 nm magnetite particle with different gold shell thickness from 5 nm to 20 nm, and, (b) a magnetite particle with diameter from 10 nm to 30 nm with a 5 nm gold shell. (c) Experimental UV/vis absorbance spectra of composite nanoparticles suspended in water at different stages of Au coating as shown in figure (d). The rising absorbance below 500 nm is due to the iron oxide core (Fig. 8d(i)). Iron oxide cores seeded with discrete Au nanoparticles have a surface plasmon resonance near 530 nm (Fig. 8d(ii)). The peak red shifts to 605 nm as the Au seeds are grown to complete the shell, consistent with core shell scattering theory (Fig. 8d(iv)). Also shown is the theoretical extinction spectrum for a particle with an 18 nm Fe 3 O 4 core and 5 nm thick Au shell in water. (d) Observable color change from (i) the yellow iron oxide only suspension, (ii) to light red after binding small gold seeds to the iron oxide particle surface, followed by a color shift to (iii) dark purple due to the grow and merging of gold seeds on the iron oxide particle surface and eventually to (iv) light blue when the clusters have nearly merged into a complete shell by electroless deposition. Copyright 2008 Wiley-VCH. Reprinted with permission from Ref. [62]. is cm 2. To compare light-scattering from these core shell particles against fluorescent molecules, the following equation [138] was used to relate the C ext to the molar extinction coefficient ε (M 1 cm 1 ) that pertains to Beer s Law for spectrophotometry: N av C ext ε = (4) Here N av is Avogadro s number. The light scattering yield which is analogy to the fluorescence efficiency is defined by the expression [138]: ϕ s = C sca. (5) C ext Hence, the ϕ s for the core shell particle is around The fluorescence intensity or fluorescing power of a solution is determined by the product εϕ f where ϕ f is the fluorescence efficiency. For dianion form of fluorescein, ε is about 60,000 M 1 cm 1 and ϕ f is approximately equal to one [138]. Then one iron oxide core, gold shell particle is equivalent to 348 fluorescein molecules in light-producing power. Several groups have imaged noble metal NPs by using a darkfield optical microscopy [19,20, ]. However, very little has been done on iron oxide core gold shell NPs. Fig. 10a shows a typical darkfield optical micrograph of the magnetic plasmonic NPs suspension above a glass cover slip. Each specimen was assembled on a microscope slide, using thin spacers and a coverglass. The nanoparticle suspension in deionized water is put in between the slide and coverglass and flipped over for viewing in the inverted configuration. The strong scattering of the surface plasmon enables core shell NPs to be imaged as bright, diffractionlimited spots against a dark background [138]. Here we see that the plasmonic response is strong enough for real-time imaging of the motion of single particles freely suspended in water. Many of the earlier darkfield studies [20,49,142,143] of plasmonic particles imaged particles that were fixed on a substrate.

12 Magnetic-plasmonic nanoparticles 109 Figure 10 (a) Darkfield optical micrograph showing the initial positions of multiple particles relative to the mu-metal tip. (b) Trajectories of nanoparticles undergoing mainly magnetophoresis and accelerating toward the magnetic field source (black), magnetophoresis and diffusion (gray), and, mainly diffusion (red). Copyright 2011 American Chemical Society. Reprinted with permission from Ref. [9]. Due to the proportionality of F mag to volume of the particle V mag and the ease of detecting particle motion, most of the earlier works on magnetophoretic control of magnetic particles were conducted on micron size particles [144,145,7]. Typical F mag associated to a model system like this ranged from 50 fn to 20 pn [7]. For magnetophoretic control of nano-sized particles, the manipulation of a swarm of NPs with diameter at 10 nm has been achieved by using micro-patterned array [146]. The advantage of this technique is its ability to assemble various structures with the building blocks composed of both diamagnetic and paramagnetic materials [147]. Simultaneous magnetic manipulation and tracking the motion of multiple individual nanostructures have recently been achieved by our group [9] and others [57]. The ability of controlling multiple individual nanostructures is the cornerstone of bottom up assembly strategies [57], with possible applications that range from video displays to therapeutics that can diagnose, treat and monitor disease [148,149]. In Fig. 10a, the trajectories of the dimmest observable moving features far away from magnetic source were analyzed to determine the 2D diffusion coefficients, which were used to estimate the hydrodynamic diameters via the Stokes Einstein equation. The evidence suggested that most of the spots corresponded to individual single particles. The bright object at the top-center is the end of the mumetal tip used to introduce magnetic field into the system [9]. When the tip was magnetized, generating a large magnetic field gradient, nearby particles migrated toward the tip. Typically, the maximum magnetic field gradient scales with the dimensions of the tip ˇ and with the distance from the tip R dis as B ˇ R 1 dis. Therefore, small tip radii should be used and the tip should be positioned close to the NPs or even directly immersed into the particle suspension. By fine tuning both ˇ and R dis values, theoretically, it is possible to vary the applied magnetic field gradient from 10 2 to 10 7 T/m [150]. Analysis of the magnetophoretic trajectories of iron oxide core gold shell NPs observed using darkfield optical microscopy revealed a capture and acceleration range of the NPs [9]. Particles within capture range from the magnetized mu metal tip underwent noticeable magnetophoresis within 25 s (Fig. 10b). The magnetic field gradients within this region ranged from 100 to 1000 tesla per meter (T/m) and were sufficient for magnetophoresis to dominate Brownian motion. In the acceleration range, the particles show more deterministic pathways with estimated field gradients around T/m. After the withdrawal of the external field, the collected NPs dispersed back into the suspension, driven by thermal energy. This kind of analysis provides important feedback for the design of magnetic tweezers for manipulation of NPs both in microfluidic systems and within living cells. For an example, by using only a permanent magnet with surface magnetic field of 3000 G (Fig. 2), Gao and co-workers capable to magnetically collect and track the motion of Fe 3 O 4 CdSe particles internalized into a HEK293T cell [31]. Taking advantage of darkfield microscopy, Sokolov s group has magnetically actuated hybrid gold/iron oxide nanoparticles that increase the optical contrast in imaging of epidermal growth factor receptor, a common cancer biomarker [151]. In addition, biocompatible composite (Au/Ag/Fe/Au) nano-crescent probes that can be controlled magnetically to produce orientational and translational motion (Fig. 11) have been employed as surface-enhanced Raman scattering (SERS) enhancers to detect biomolecules within a living cell [152]. In addition to this high gradient ( B >1000 T/m) magnetophoretic control scheme, De Las Cuevas and co-workers have demonstrated the possible rapid collection of magnetic NPs under low magnetic field gradients ( B >100 T/m) [112]. Unlike in the single NP manipulation strategy, under low gradient magnetic separation, the magnetic NPs first go through field-induced aggregations followed by cooperative magnetophoresis, which is faster due to reduced drag of the large aggregate [153,154]. Since this is a concentration dependent phenomenon [155], low gradient separation is more suitable for separation of biological components than for nanoscale motion control and sensing [156].

13 110 J. Lim, S.A. Majetich Figure 11 Composite material magnetic nanocrescent SERS probes. (a) Schematic diagram of SERS detection on a single composite nanocrescent. (b) Transmission electron microscopy image of a single magnetic nanocrescent SERS probe. The scale bar represents 100 nm. (c) Schematic diagram of a SERS imaging system and the magnetic manipulation system for intracellular biomolecular imaging (in fluids) using standalone magnetic nanocrescent SERS probes. Copyright 2005 Wiley-VCH. Reprinted with permission from Ref. [152]. Conclusions and outlook Magnetic and plasmonic properties of iron oxide core gold shell nanoparticle are beneficial for nanoscale sensing where simultaneous motion control and imaging is needed. In this review, we have discussed a number of recently developed chemical synthesis techniques that are very effective in making iron oxide gold nanoparticles with well-defined morphologies. The particles should be uniform in size and shape, colloidally stable, biocompatible, and have a sharp plasmonic signal and large magnetic moment. Regulating the movement of nanoparticles in real-time is nontrivial, since this requires precise control of the nanoparticle direction as well as temporal and spatial guidance of the particle speed [157]. The magnetic field gradient involved in either accelerating or moving the particles at constant speed is important [9] and the use of multiple magnetic actuators and levitators to guide the particle motion in three dimension may be necessary [158]. Magnetic plasmonic nanoparticles could be used to enhance many of the techniques that currently use magnetic particles for actuation, and could provide real-time feedback about biological mechanisms. For example, magnetic nanoparticles are used to manipulate cells [159,160] and proteins [161,162]. Iron oxide core gold shell nanoparticles modified with Ni 2+ nitrilotriacetic acid have been successfully been used to capture, enrich and purify the His-tag maltose-binding proteins from cell lysate [163]. Park and co-workers have demonstrated that the feasibility of using iron oxide core gold shell NPs for immunoseparation with surface enhanced Raman scattering (SERS) detection [86]. These NPs could also be used as nanomagnetic actuators for several intriguing applications proposed by Dobson and co-workers, such as perturbing actin filaments, activating mechanosensitive ion-channels, targeting ion-channel activation and receptor clustering [ ]. In addition, the plasmonic signal could be correlated with specific functionality. For example, particles with different shell thicknesses,

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