Name: assembly and characterization of polyelectrolyte complex micelles
Uploaded: 2020-03-02T14:00:00
Description: Watch this Scientific Journal Video about Assembly and Characterization of Polyelectrolyte Complex Micelles at JoVE.com

We thank Phil Griffin and Tera Lavoie of the Soft Matter Characterization Facility and Advanced Electron Microscopy Facility, respectively, at The University of Chicago. We also thank Xiaobing Zuo and Soenke Seifert of the Advanced Photon Source at Argonne National Laboratory and NIST Center for Hierarchical Materials Design (CHiMaD) for support. We thank Jeff Ting and Michael Lueckheide for their contributions to this work.

1. Preparation of Materials
<ol>
	<li>Weigh out lyophilized diblock polymer and add water up to nearly the volume required for a stock solution of 10 mg/mL final concentration. Vortex at maximum speed for 2 min.</li>
	<li>Sonicate for 5 min. Very long diblocks may require additional sonication. The stock solution should appear completely transparent and homogeneous.</li>
	<li>Adjust pH to 7.4 using NaOH or HCl as needed. Add water to the final volume. pLys-PEG solutions are fairly stable but should be refrigerated for ...

As mentioned above, the protocols presented here are written with a focus on oligonucleotides as the polyanion component and pLys-PEG as the cationic-neutral block copolymer, but we have tested them with a variety of polymers, such as poly(acrylic acid), polyglutamate, and PEG-poly(vinylbenzyl trimethylammonium), and believe they will be generally applicable for most polyelectrolyte pairs. One parameter that may need to be optimized is the salt concentration used for annealing, because it should be high enough that PCMs ...

When oppositely charged polyelectrolytes are mixed in aqueous solution, entropy gain from release of their counterions causes demixing of the solution into a polymer-rich condensed phase and a polymer-depleted supernatant1,2,3,4,5, a phenomenon known as polyelectrolyte complexation. If a neutral hydrophilic block is conjugated to one or both of the polyelectrolytes, nanoscale phase separation occurs instead (Figure 1A). The resulting self-assembled core-shell nanoparticles are variously referred to as polyelectrolyte complex micelles (PCMs), polyion complex micelles, block ionomer complexes, or coacervate-core micelles by analogy to surfactant micellization, even though all components of the system are hydrophilic6,7. A PCM&#39;s ability to encapsulate hydrophilic molecules such as proteins and nucleic acids, as well as the extensive tunability offered by the block copolymer carrier architecture makes them attractive candidates for delivering therapeutic molecules in vivo8,9,10,11,12,13.
Delivering therapeutic nucleic acids to cellular targets is a particularly important challenge, and one for which PCMs offer several advantages. Therapeutic nucleic acids (genetic DNA, mRNA, and oligonucleotides such as siRNA) have immense potential for improving human health, but must overcome numerous biological and physical barriers to realize that potential14,15,16. Bare nucleic acids are degraded by serum and cellular nucleases, are quickly cleared from circulation, and their strong negative charge makes it difficult for them to penetrate cell membranes without assistance. Current approaches for overcoming these barriers include costly chemical modifications to prevent damage from nucleases and/or encapsulation into various lipid nanoparticles assembled via hydrophobic interactions15,17,18. While these methods have proven effective for local injections and liver targeting, systemic use presents significant limitations of toxicity, immunogenicity, and limited biodistribution16. By contrast, PCMs use the negative charge of nucleic acids to condense them within the phase-separated core, while the neutral corona provides a steric barrier against degradation as well as a platform for incorporating ligands to enhance targeting or internalization11,19. In vitro and animal studies have shown that PCMs can effectively deliver various nucleic acid payloads20,21,22,23,24, but weaknesses in our ability to predict PCM properties such as size, shape, and stability from the properties of the constituent polymers have hindered their wider adoption.
Recent work by our group and others in the field has begun to address this problem by developing structure-property, and in some cases structure-property-function relationships for PCMs formed from nucleic acids and various cationic-neutral polymers7,25,26,27. Two consistent themes that have emerged from these studies are the importance of developing well-controlled, repeatable protocols for PCM assembly and the benefit of using multiple techniques to characterize the resulting nanoparticles. Polyelectrolytes, particularly those with high charge density like nucleic acids, interact with each other very strongly, and appear to readily become kinetically trapped upon mixing, resulting in PCM preparations that are highly sensitive to small variations in procedure and display high polydispersity and poor repeatability from batch to batch. PCMs have also been shown to adopt a wide range of shapes and sizes depending on the atomic-level configurations of their components, and capturing this diversity with any individual characterization technique is very difficult, particularly since some common techniques such as dynamic light scattering (DLS) require assumptions about particle shape for their interpretation.
In this article, we discuss material design and selection for PCMs, with a focus on oligonucleotides and cationic-neutral diblock copolymers. We then describe a salt annealing protocol that uses high salt concentrations followed by slow dialysis to avoid kinetic trapping during PCM assembly. The polyelectrolytes are mixed in high salt conditions where electrostatic attractions are screened, then the salt concentration is slowly lowered to allow the polyelectrolytes to settle into their most energetically favorable configurations, analogous to the slow cooling process of thermal annealing. Using this protocol, we are regularly able to achieve exceptionally low polydispersity and high repeatability for oligonucleotide PCMs7,26. Finally, we describe how four separate measurement techniques can be used to characterize PCMs over a very wide range of length scales, from external morphology to internal structure: DLS, multi-angle light scattering (MALS), small angle X-ray scattering (SAXS), and transmission electron microscopy (TEM). We hope that these protocols will enable more researchers to effectively explore the capabilities of these interesting nanoparticles.
Polymer Selection and Preparation 
PCM properties are strongly influenced by the physical and chemical characteristics of the constituent polymers, making polymer selection a critical step in the design process. The most well-characterized block copolymers for nucleic acid PCMs are linear diblocks such as poly(lysine)-poly(ethylene glycol) (pLys-PEG), but PCMs can be formed between polyelectrolytes and a variety of hydrophilic neutral-charged polymers, which can be generated in a high throughput manner28. The choice of charged group strongly affects the stability of ion pairing and shape of micelles26, and PCM size has been shown to increase with the length of the charged block5,7,26 (Figure 2), thus allowing PCM properties to be tuned for the requirements of a desired application. For linear diblocks, we have found that the charged block should have at least 10 charges and be strongly charged at the desired pH. Longer charged blocks may promote PCM formation with oligonucleotides such as siRNA, which are difficult to complex with shorter blocks21. We have successfully observed PCM formation with block lengths up to 200, and the literature describes longer polymers. More flexibility is available in the choice of neutral blocks24, but experience has shown that very short neutral blocks lead to aggregation rather than nanoparticle formation, and that the minimum neutral length increases with charged block length. For pLys-PEG, a PEG MW of at least 3,000&#8211;5,000 is required for pLys lengths below ~50, and longer lengths are required as the charged block is increased further. Increased neutral block length results in increased PCM size, particularly shell thickness, due to steric crowding of the neutral polymers.
This manuscript presents a protocol for preparing PCMs from lyophilized high-purity pLys-PEG and oligonucleotides of known quantity, but should be readily adaptable to other systems as well. We have tested it successfully with several charged polypeptides, including polyarginine and polyglutamic acid, as well as several synthetic polyelectrolytes, such as polyacrylic acid and poly(vinylbenzyl trimethylammonium). We also describe preparing PCMs with a stoichiometric ratio of polyelectrolyte charges, but this is easily modified. We find it easiest to work in charge concentration units (c.c.), which also naturally accommodates polymers that are not fully charged. If either polymer is not well-characterized, care should be taken to accurately determine the polymer lengths/masses and ensure that excess salt is not present beyond that needed for charge neutralization by dialysis, for example. The presence of any retained water should also be accounted for when concentrations are calculated. Nucleic acid concentration can be conveniently quantified by absorbance at 260 nm, and the presence or absence of terminal phosphates should be considered when calculating the c.c.
When using oligonucleotides as polyanions, the hybridization state and chemical structure help determine the propensity for self-assembly and the characteristics of the resulting PCM5,7,26. Optimizing these, within the requirements for biological efficacy if using PCMs for delivery, will increase the likelihood of forming the desired structures. Helpful tools for analyzing hybridization include MATLAB functions for nucleic acids, NUPACK29, and IDT OligoAnalyzer. We recommend analyzing a candidate sequence to understand the strength of binding to 1) itself in a hairpin formation; 2) another copy of the same sequence (self-dimer); and 3) to other oligonucleotides present in the system. DNA and RNA melting temperatures for a specific sequence can also be calculated using the nearest-neighbor method30,31. Thermal annealing of nucleic acids (step 2.3) denatures any residual secondary structure in the individual nucleotides and promotes equilibrium folding.
PCM Characterization and Analysis 
A wide range of techniques are available for characterizing nanoparticles, including static and dynamic light scattering, small angle scattering of electrons or neutrons, and electron microscopy. In this article, we provide protocols for two light scattering techniques, small angle X-ray scattering, and two electron microscopy techniques.
DLS measures the autocorrelation of temporal fluctuations in scattering intensity at one angle from Brownian motion of the sample. Fitting this data can provide hydrodynamic radius and polydispersity for spherical micelles (Figure 3). Multiple angle light scattering (MALS) measures the static scattering intensity at many angles. This angular dependence describes the shape of the nanoparticle but is limited to length scales longer than ~50 nm for visible light, which limits its effectiveness for smaller nanoparticles. Both techniques are based on refractive index mismatch and primarily describe the outside dimensions of the nanoparticle.
Small angle X-ray scattering (SAXS) uses X-rays as the scattering probe, and their shorter wavelength allows measurements over a range of ~0.1&#8211;100 nm. Fitting the observed scattering intensity vs. angle (conventionally expressed as momentum transfer q) provides information on PCM morphology (i.e., size and shape) and also internal structure. If an absolute intensity calibration is available, and if the scattering intensity can be extrapolated to zero angle, PCM mass and aggregation number can also be estimated32, making SAXS an extremely versatile and valuable method. Small angle neutron scattering (SANS) is sensitive over a similar range of length scales but is only available at specialized facilities and will not be explicitly discussed in this article33,34,35.
Recent years have seen the advent of benchtop SAXS instruments, but we find that synchrotron sources are better suited for PCM characterization, as their higher intensity allows data to be collected much faster for these low-contrast samples. We provide a brief protocol for acquiring PCM SAXS data at Beamline 12-ID-B at the Advanced Photon Source (Argonne National Laboratory, USA) from a user perspective. This protocol should be applicable to most synchrotron sources, but consulting with local staff before proposing an experiment is highly recommended. We also provide a data reduction and analysis protocol using Irena36, a free set of macros written for Igor Pro. Irena includes a versatile set of form factors for modeling SAXS data and allows for construction of multicomponent models that are capable of describing the complex scattering profile of PCMs (see Representative Results, Figure 4). Irena also has comprehensive documentation and tutorials available online. Before attempting the procedures below, we recommend familiarization with these, particularly the tutorial &#34;Modeling of SAXS data with two main scatterer populations&#34;.
Radiation damage is a concern for X-ray scattering, but several measures can be employed to minimize it. In particular, we recommend using a flow cell setup with a syringe pump and PCM sample flowing during data acquisition, rather than a sealed capillary. This also greatly simplifies background subtraction. We also suggest taking multiple exposures of the flowing sample rather than one longer one in order to limit the flux that any single volume of sample sees and to allow for comparison of the exposure data to identify any damage.
In contrast to the scattering techniques, which generally require fitting to interpret, transmission electron microscopy (TEM) provides a real space visual image of the nanoparticles by passing an electron beam through the sample and projecting an image on a scintillation screen (Figure 5). We present protocols for two TEM techniques in this article. Cryo TEM freezes micelle samples into a thin layer of vitreous ice, preserving structural conformation with minimal foreign substances, optimal for micelles &#8804;~10-100 nm in radius. Negative stain TEM uses a heavy metal salt (e.g., uranium) to surround the sample after it has been dried on the surface of a grid. The dense stain will scatter more electrons than the sample, adding contrast and producing a negative image of the sample. Cryo TEM is recommended for high-quality images. However, it is more costly, time consuming, and may not provide sufficient contrast. When this is a concern, negative stained samples should be used. Examples of each are shown in Figure 5.
Each of these techniques reports on slightly different aspects of the nanoparticles, with different strengths and limitations. Light scattering is readily available, and is often the fastest approach, but has substantial limitations in size and shape resolution. SAXS can provide information over a large range of length scales at reasonably high throughput, but requires specialized equipment to acquire the data, as well as modeling to interpret it. TEM images are straightforward to interpret but can be limited in contrast and are inherently low throughput. Our experience has shown that using multiple techniques for characterization greatly increases the information that can be obtained about PCM properties and simplifies interpretation of data sets obtained from each one alone. For example, SAXS and TEM primarily examine a PCM&#39;s dense core, while light scattering reports on the overall dimensions of the nanoparticle. Thus, combining them allows measurement of both core and corona size. TEM&#39;s ability to acquire real space images can provide ground truth data to enable selection of appropriate form factors for modeling SAXS data that might otherwise be ambiguous. This article describes protocols for all four techniques, and an example process for using them to characterize an unknown sample is given in the Discussion section.

<table border="1" fo:keep-together.within-page="1" fo:keep-with-next.within-page="always">
	<tbody>
		<tr>
			<td>70 mm circle filter paper</td>
			<td>Whatman</td>
			<td>1001-070</td>
			<td>Filter paper for wicking during grid prep</td>
		</tr>
		<tr>
			<td>Carbon Film TEM grid</td>
			<td>Electron Microscopy Sciences</td>
			<td>CF200-Cu</td>
			<td>TEM grid</td>
		</tr>
		<tr>
			<td>DAWN</td>
			<td>Wyatt Technology</td>
			<td>DAWN</td>
			<td>MALS instrument</td>
		</tr>
		<tr>
			<td>DNA oligonucleotide</td>
			<td>Integrated DNA Nanotechnologies Inc</td>
			<td></td>
			<td>Custom oligonucleotide</td>
		</tr>
		<tr>
			<td>Lacey Carbon TEM grid</td>
			<td>Electron Microscopy Sciences</td>
			<td>LC200-Cu</td>
			<td>TEM grid</td>
		</tr>
		<tr>
			<td>Methoxy-poly(ethylene glycol)-block-poly(l-lysine hydrochloride) PEG5k - PLKC50</td>
			<td>Alamanda Polymers Inc</td>
			<td>mPEG5K-b-PLKC50</td>
			<td>Example block copolymer</td>
		</tr>
		<tr>
			<td>Milli-Q</td>
			<td>Millipore Sigma</td>
			<td></td>
			<td>Ultrapure water</td>
		</tr>
		<tr>
			<td>NanoDrop</td>
			<td>Thermo Scientific</td>
			<td></td>
			<td>For measuring nucleic acid concentration</td>
		</tr>
		<tr>
			<td>negative-action tweezers</td>
			<td>Dumont</td>
			<td>N7</td>
			<td>Tweezers for grid preparation</td>
		</tr>
		<tr>
			<td>Parafilm &#34;M&#34;</td>
			<td>Bemis Company Inc</td>
			<td>PM996</td>
			<td>Laboratory film</td>
		</tr>
		<tr>
			<td>Quantifoil Holey Carbon TEM grid</td>
			<td>Electron Microscopy Sciences</td>
			<td>Q210CR1.3</td>
			<td>TEM grid</td>
		</tr>
		<tr>
			<td>Research Goniometer and Laser Light Scattering System</td>
			<td>Brookhaven Instruments</td>
			<td>BI-200SM</td>
			<td>DLS/MALS instrument</td>
		</tr>
		<tr>
			<td>Slide-A-Lyzer G2 2K 0.5 mL</td>
			<td>Thermo Scientific Pierce Protein Biology</td>
			<td>87723</td>
			<td>Dialysis cartridge</td>
		</tr>
		<tr>
			<td>small volume cuvette</td>
			<td>Brookhaven Instruments</td>
			<td>BI-SVC</td>
			<td>Cuvette for DLS/MALS</td>
		</tr>
		<tr>
			<td>Solarus 950 Advanced Plasma System</td>
			<td>Gatan</td>
			<td>Solarus 950</td>
			<td>Plasma system for TEM grids</td>
		</tr>
		<tr>
			<td>Talos TEM</td>
			<td>FEI</td>
			<td>Talos</td>
			<td>TEM used for cryo samples</td>
		</tr>
		<tr>
			<td>Tecnai Spirit TEM</td>
			<td>FEI</td>
			<td>Spirit</td>
			<td>TEM used for dry samples</td>
		</tr>
		<tr>
			<td>Uranyl Formate</td>
			<td>SPI-Chem</td>
			<td>16984-59-1</td>
			<td>For negative staining samples for TEM</td>
		</tr>
		<tr>
			<td>Vitrobot</td>
			<td>FEI</td>
			<td>Vitrobot</td>
			<td>Vitrification robot for cryo grid preparation</td>
		</tr>
	</tbody>
</table>

assembly and characterization of polyelectrolyte complex micelles

Polyelectrolyte complex micelles (PCMs), core-shell nanoparticles formed by self-assembly of charged polymers in aqueous solution, provide a powerful platform for exploring the physics of polyelectrolyte interactions and also offer a promising solution to the pressing problem of delivering therapeutic oligonucleotides in vivo. Developing predictive structure-property relationships for PCMs has proven difficult, in part due to the presence of strong kinetic traps during nanoparticle self-assembly. This article discusses criteria for choosing polymers for PCM construction and provides protocols based on salt annealing that enable assembly of repeatable, low-polydispersity nanoparticles. We also discuss PCM characterization using light scattering, small-angle X-ray scattering, and electron microscopy.

In order to illustrate the characterization methods described above, we show typical results for PCMs assembled from oligonucleotides and block copolymers of various lengths and chemistries (Figure 1). Figure 2 provides an example of how PCM core size (as determined from SAXS and TEM, Figure 4 and Figure 5) varied with charged block length. Figure 3 shows DLS data and fitti...

Watch this Scientific Journal Video about Assembly and Characterization of Polyelectrolyte Complex Micelles at JoVE.com

Assembly and Characterization of Polyelectrolyte Complex Micelles

We provide protocols and representative data for designing, assembling, and characterizing polyelectrolyte complex micelles, core-shell nanoparticles formed by polyelectrolytes and hydrophilic charged-uncharged block copolymers.

Polyelectrolyte complex micelles (PCMs), core-shell nanoparticles formed by self-assembly of charged polymers in aqueous solution, provide a powerful ...

This method describes the full path of the design, assembly, and characterization of polyelectrolyte complex micelles which are nanoparticles that are formed from the self-assembly of oppositely charged polymers. Some major challenges with polyelectrolyte self-assembly are avoiding kinetic traps and characterizing the nanoparticles. The salt annealing technique that we describe allows for the repeatable assembly of micelles with low dispersity in both size and shape and we describe characterization methods including light scattering, small angle x-ray scattering, and electron microscopy.Delivering therapeutic nucleic acids is a longstanding challenge for nanomedicine. These polyelectrolyte complex micelles take advantage of the strong negative charge of the nucleic acid to sequester them in the core of the micelle where the neutral polymer corona protects them from nucleases and immune response. The assembly method should be applicable to any type of charged polymers.We've tested them with several polyanions and polycations and the characterization method should be applicable to any self-assembled nanoparticles including surfactant nanoparticles and other hydrophobically-driven systems. Begin by incubating the oligonucleotide solution at 70 degrees Celsius for five minutes. After the incubation, cool it for 15 minutes at room temperature to thermally anneal the nucleic acids, then add 40 microliters of 20 millimolar charged concentration diblock copolymer.Vortex the solution immediately and incubate it for five minutes at room temperature. To perform the salt anneal, add sodium chloride solution to the oligonucleotide solution for a final concentration of one molar and vortex it for 10 seconds at maximum speed. Incubate the mixture for 10 minutes at room temperature, then proceed with loading it into the dialysis cartridge.Prior to loading, label cartridges with permanent marker and soak them in buffer for at least two minutes to hydrate the membranes. Remove the cap by twisting counterclockwise and load the sample using a gel loading pipette tip. Gently squeeze the membrane to remove excess air and replace the cap.Put the cartridges into 1X PBS 0.5 molar sodium chloride dialysis bath making sure that they are floating with both membranes exposed to the bath. After 24 hours, transfer the cartridges into 1X PBS and soak it for an additional 24 hours. After the final dialysis, recover the sample by removing the cartridges from the bath, removing the cap and removing the sample with a gel loading pipette tip.Place the sample into a clean 1.5 milliliter microcentrifuge tube and refrigerate it until ready to use. Prepare the sample in DLS instrument according to manuscript directions, then acquire data for at least one minute making sure that the count rate is constant over the entire acquisition time. Examine the autocorrelation data.The long time baseline should be flat and the autocorrelation curve should be smooth with minimal scatter. Noise in the data can be improved by acquiring more data. To perform data reduction and analysis using Irena, start by importing micelle in background data sets.Plot the sample and background together on a log-log scale and compute the sample to background ratio and verify the high Q asymptote. Compute the average ratio over this Q range and use the data manipulation macro to scale the background with the calculated ratio. Then plot the background subtracted signal over Q and save the data with a new name making sure to not overwrite the original data.Open the modeling macro, then load and plot the background subtracted data. To find an approximate model for the external surface of the polyelectrolyte complex micelle, or PCM, select flow to moderate Q range in the data controls making sure to include oscillations if they are present. In model controls, select the first scattering population and make sure it is the only one in use.Select size distribution for model, choose the desired distribution type, and select the form factor. This example is for a flexible cylinder which must be added manually under the user form factor. Download and add the flexible cylinder form factor, then input the function names and initial values for parameters one and two which correspond to the length of the cylinder and the Kuhn length respectively.These cylinders are longer than can be resolved by SAXS so the cylinder length parameter is fixed at a large value. Set initial parameters for the search by entering values in the scale, mean size, and width fields. Then click calculate model to draw the resulting form factor.Once reasonable parameters have been found, click fit model to perform a nonlinear least squares fit to the data. Next, model the scattering of the individual polymers within the PCM core. Adjust the data controls to select the Q range where excess scattering occurs which is typically in the moderate to high range.Add a second scattering population and make sure it is the only one in use. Select unified level for the model, adjust the GDA factors G and RG to ensure that the model does not predict excessive scattering at low Q and use the fit PB between cursors macro to obtain an initial guess for these parameters. As for the form factor, perform a nonlinear fit for the unified level model.If a diffraction peak is present, add a third model for the diffraction peak in the Q range of interest. Once approximate fit values are obtained for the individual scattering populations, turn on all three together and optimize the combined fit. Finally, check that each value remains physically reasonable and save the fit by selecting store in folder.The result of this procedure should be a composite model that describes the small angle x-ray scattering data well over a large range of size scales. This protocol was used to design, assemble, and characterize nucleic acid polyelectrolyte complex micelles or PCMs. Micelle core size is primarily driven by the length of the charged block of the block copolymer and is largely independent of the length of the homopolymer.Dynamic light scattering data was acquired for spherical PCMs formed from relatively long block copolymers in short single-stranded oligonucleotides. The autocorrelation function decayed to a flat value with the single time scale resulting in the single size peak in the repIS size distribution. Complex small angel x-ray scattering or SAXS intensity spectra can be accurately fit by combining models for the multiple spatial correlations that are present and multiangle light scattering can be used to extend scattering measurements to longer length scales.PCMs of varying morphology can also be imaged with electron microscopy to verify that core radii and shape are consistent with the values obtained from fitting SAXS data. When fitting SAXS data, it's important to account for each scattering feature and to use complimentary methods like TEM to make sure you're using the correct form factor.

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