SDS-PAGE


SDS-PAGE, is a discontinuous electrophoretic system developed by Ulrich K. Laemmli which is commonly used as a method to separate proteins with molecular masses between 5 and 250 kDa. The combined use of sodium dodecyl sulfate and polyacrylamide gel allows to eliminate the influence of structure and charge, and proteins are separated solely on the basis of differences in their molecular weight.

Properties

SDS-PAGE is an electrophoresis method that allows protein separation by mass. The medium is a polyacrylamide-based discontinuous gel. In addition, SDS is used. About 1.4 grams of SDS bind to a gram of protein, corresponding to one SDS molecule per two amino acids. SDS acts as a surfactant, masking the proteins' intrinsic charge and conferring them very similar charge-to-mass ratios. The intrinsic charges of the proteins are negligible in comparison to the SDS loading, and the positive charges are also greatly reduced in the basic pH range of a separating gel. Upon application of a constant electric field, the protein migrate towards the anode, each with a different speed, depending on its mass. This simple procedure allows precise protein separation by mass.
SDS tends to form spherical micelles in aqueous solutions above a certain concentration called the critical micellar concentration. Above the critical micellar concentration of 7 to 10 millimolar in solutions, the SDS simultaneously occurs as single molecules and as micelles, below the CMC SDS occurs only as monomers in aqueous solutions. At the critical micellar concentration, a micelle consists of about 62 SDS molecules. However, only SDS monomers bind to proteins via hydrophobic interactions, whereas the SDS micelles are anionic on the outside and do not adsorb any protein. SDS is amphipathic in nature, which allows it to unfold both polar and nonpolar sections of protein structure. In SDS concentrations above 0.1 millimolar, the unfolding of proteins begins, and above 1 mM, most proteins are denatured. Due to the strong denaturing effect of SDS and the subsequent dissociation of protein complexes, quaternary structures can generally not be determined with SDS. Exceptions are proteins that are stabilised by covalent cross-linking e.g. -S-S- linkages and the SDS-resistant protein complexes, which are stable even in the presence of SDS. To denature the SDS-resistant complexes a high activation energy is required, which is achieved by heating. SDS resistance is based on a metastability of the protein fold. Although the native, fully folded, SDS-resistant protein does not have sufficient stability in the presence of SDS, the chemical equilibrium of denaturation at room temperature occurs slowly. Stable protein complexes are characterised not only by SDS resistance but also by stability against proteases and an increased biological half-life.
Alternatively, polyacrylamide gel electrophoresis can also be performed with the cationic surfactants CTAB in a CTAB-PAGE, or 16-BAC in a BAC-PAGE.

Procedure

The SDS-PAGE method is composed of gel preparation, sample preparation, electrophoresis, protein staining or western blotting and analysis of the generated banding pattern.

Gel production

When using different buffers in the gel, the gels are made up to one day prior to electrophoresis, so that the diffusion does not lead to a mixing of the buffers. The gel is produced by radical polymerisation in a mold consisting of two sealed glass plates with spacers between the glass plates. In a typical mini-gel setting, the spacers have a thickness of 0.75 mm or 1.5 mm, which determines the loading capacity of the gel. For pouring the gel solution, the plates are usually clamped in a stand which temporarily seals the otherwise open underside of the glass plates with the two spacers. For the gel solution, acrylamide is mixed as gel-former, methylenebisacrylamide as a cross-linker, stacking or separating gel buffer, water and SDS. By adding the catalyst TEMED and the radical initiator ammonium persulfate the polymerisation is started. The solution is then poured between the glass plates without creating bubbles. Depending on the amount of catalyst and radical starter and depending on the temperature, the polymerisation lasts between a quarter of an hour and several hours. The lower gel is poured first and covered with a few drops of a barely water-soluble alcohol, which eliminates bubbles from the meniscus and protects the gel solution of the radical scavenger oxygen. After the polymerisation of the separating gel, the alcohol is discarded and the residual alcohol is removed with filter paper. After addition of APS and TEMED to the stacking gel solution, it is poured on top of the solid separation gel. Afterwards, a suitable sample comb is inserted between the glass plates without creating bubbles. The sample comb is carefully pulled out after polymerisation, leaving pockets for the sample application. For later use of proteins for protein sequencing, the gels are often prepared the day before electrophoresis to reduce reactions of unpolymerised acrylamide with cysteines in proteins.
By using a gradient mixer, gradient gels with a gradient of acrylamide can be cast, which have a larger separation range of the molecular masses. Commercial gel systems usually use the buffer substance Bis-tris methane with a pH value between 6.4 and 7.2 both in the stacking gel and in the separating gel. These gels are delivered cast and ready-to-use. Since they use only one buffer and have a nearly neutral pH, they can be stored for several weeks. The more neutral pH slows the hydrolysis and thus the decomposition of the polyacrylamide. Furthermore, there are fewer acrylamide-modified cysteines in the proteins. Due to the constant pH in collecting and separating gel there is no stacking effect. Proteins in BisTris gels can not be stained with ruthenium complexes. This gel system has a comparatively large separation range, which can be varied by using MES or MOPS in the running buffer.

Sample preparation

During sample preparation, the sample buffer, and thus SDS, is added in excess to the proteins, and the sample is then heated to 95 °C for five minutes, or alternatively 70 °C for ten minutes. Heating disrupts the secondary and tertiary structures of the protein by disrupting hydrogen bonds and stretching the molecules. Optionally, disulfide bridges can be cleaved by reduction. For this purpose, reducing thiols such as β-mercaptoethanol, dithiothreitol or dithioerythritol are added to the sample buffer. After cooling to room temperature, each sample is pipetted into its own well in the gel, which was previously immersed in electrophoresis buffer in the electrophoresis apparatus.
In addition to the samples, a molecular-weight size marker is usually loaded onto the gel. This consists of proteins of known sizes and thereby allows the estimation of the sizes of the proteins in the actual samples, which migrate in parallel in different tracks of the gel. The size marker is often pipetted into the first or last pocket of a gel.

Electrophoresis

For separation, the denatured samples are loaded onto a gel of polyacrylamide, which is placed in an electrophoresis buffer with suitable electrolytes. Thereafter, a voltage is applied, which causes a migration of negatively charged molecules through the gel in the direction of the positively charged anode. The gel acts like a sieve. Small proteins migrate relatively easily through the mesh of the gel, while larger proteins are more likely to be retained and thereby migrate more slowly through the gel, thereby allowing proteins to be separated by molecular size. The electrophoresis lasts between half an hour to several hours depending on the voltage and length of gel used.
The fastest-migrating proteins form the buffer front together with the anionic components of the electrophoresis buffer, which also migrate through the gel. The area of the buffer front is made visible by adding the comparatively small, anionic dye bromophenol blue to the sample buffer. Due to the relatively small molecule size of bromophenol blue, it migrates faster than proteins. By optical control of the migrating colored band, the electrophoresis can be stopped before the dye and also the samples have completely migrated through the gel and leave it.
The most commonly used method is the discontinuous SDS-PAGE. In this method, the proteins migrate first into a collecting gel with neutral pH, in which they are concentrated and then they migrate into a separating gel with basic pH, in which the actual separation takes place. Stacking and separating gels differ by different size, ionic strength and pH values. The electrolyte most frequently used is an SDS-containing Tris-glycine-chloride buffer system. At neutral pH, glycine predominantly forms the zwitterionic form, at high pH the glycines lose positive charges and become predominantly anionic. In the collection gel, the smaller, negatively charged chloride ions migrate in front of the proteins and the slightly larger, negatively and partially positively charged glycinate ions migrate behind the proteins, whereas in the comparatively basic separating gel both ions migrate in front of the proteins. The pH gradient between the stacking and separation gel buffers leads to a stacking effect at the border of the stacking gel to the separation gel, since the glycinate partially loses its slowing positive charges as the pH increases and then, as the former trailing ion, overtakes the proteins and becomes a leading ion, which causes the bands of the different proteins to become narrower and sharper - the stacking effect. For the separation of smaller proteins and peptides, the TRIS-Tricine buffer system of Schägger and von Jagow is used due to the higher spread of the proteins in the range of 0.5 to 50 kDa.

Gel staining

At the end of the electrophoretic separation, all proteins are sorted by size and can then be analyzed by other methods, e. g. protein staining such as Coomassie staining, silver staining, stains all staining, Amido black 10B staining, Fast green FCF staining, fluorescent stains such as epicocconone stain and SYPRO orange stain, and immunological detection such as the Western Blot. The fluorescent dyes have a comparatively higher linearity between protein quantity and color intensity of about three orders of magnitude above the detection limit, i. e. the amount of protein can be estimated by color intensity. When using the fluorescent protein dye trichloroethanol, a subsequent protein staining is omitted if it was added to the gel solution and the gel was irradiated with UV light after electrophoresis.
In Coomassie Staining, Gel is Fixed in a 50% ethanol 10% glacial acetic acid solution for 1 hr. Then the solution is changed for fresh one and after 1 to 12 hrs Gel is changed to a Staining solution followed by destaining changing several times a destaining solution of 40% methanol, 10% glacial acetic acid.

Analysis

Protein staining in the gel creates a documentable banding pattern of the various proteins. Glycoproteins have differential levels of glycosylations and adsorb SDS more unevenly at the glycosylations, resulting in broader and blurred bands. Membrane proteins, because of their transmembrane domain, are often composed of the more hydrophobic amino acids, have lower solubility in aqueous solutions, tend to bind lipids, and tend to precipitate in aqueous solutions due to hydrophobic effects when sufficient amounts of detergent are not present. This precipitation manifests itself for membrane proteins in a SDS-PAGE in "tailing" above the band of the transmembrane protein. In this case, more SDS can be used and the amount of protein in the sample application can be reduced. An overloading of the gel with a soluble protein creates a semicircular band of this protein, allowing other proteins with similar molecular weights to be covered. A low contrast between bands within a lane indicates either the presence of many proteins or, if using purified proteins and a low contrast occurs only below one band, it indicates a proteolytic degradation of the protein, which first causes degradation bands, and after further degradation produces a homogeneous color below a band. The documentation of the banding pattern is usually done by photographing or scanning. For a subsequent recovery of the molecules in individual bands, a gel extraction can be performed.

Archiving

After protein staining and documentation of the banding pattern, the polyacrylamide gel can be dried for archival storage. Proteins can be extracted from it at a later date. The gel is either placed in a drying frame or in a vacuum dryer. The drying frame consists of two parts, one of which serves as a base for a wet cellophane film to which the gel and a one percent glycerol solution are added. Then a second wet cellophane film is applied bubble-free, the second frame part is put on top and the frame is sealed with clips. The removal of the air bubbles avoids a fragmentation of the gel during drying. The water evaporates through the cellophane film. In contrast to the drying frame, a vacuum dryer generates a vacuum and heats the gel to about 50 °C.

Molecular mass determination

For a more accurate determination of the molecular weight, the relative migration distances of the individual protein bands are measured in the separating gel. The measurements are usually performed in triplicate for increased accuracy. The relative mobility is the quotient of the distance of the band of the protein and the distance of the buffer front. The distances of the bands and the buffer front are each measured from the beginning of the separation gel. The distance of the buffer front roughly corresponds to the distance of the bromophenol blue contained in the sample buffer. The relative distances of the proteins of the size marker are plotted semi-logarithmically against their known molecular weights. By comparison with the linear part of the generated graph or by a regression analysis, the molecular weight of an unknown protein can be determined by its relative mobility. Bands of proteins with glycosylations can be blurred. Proteins with many basic amino acids can lead to an overestimation of the molecular weight or even not migrate into the gel at all, because they move slower in the electrophoresis due to the positive charges or even to the opposite direction. Accordingly, many acidic amino acids can lead to accelerated migration of a protein and an underestimation of its molecular mass.

Applications

The SDS-PAGE in combination with a protein stain is widely used in biochemistry for the quick and exact separation and subsequent analysis of proteins. It has comparatively low instrument and reagent costs and is an easy-to-use method. Because of its low scalability, it is mostly used for analytical purposes and less for preparative purposes, especially when larger amounts of a protein are to be isolated.
Additionally, SDS-PAGE is used in combination with the western blot for the determination of the presence of a specific protein in a mixture of proteins - or for the analysis of post-translational modifications. Post-translational modifications of proteins can lead to a different relative mobility or to a change in the binding of a detection antibody used in the western blot.
In mass spectrometry of proteins, SDS-PAGE is a widely used method for sample preparation prior to spectrometry, mostly using in-gel digestion. In regards to determining the molecular mass of a protein, the SDS-PAGE is a bit more exact than an analytical ultracentrifugation, but less exact than a mass spectrometry or - ignoring post-translational modifications - a calculation of the protein molecular mass from the DNA sequence.
In medical diagnostics, SDS-PAGE is used as part of the HIV test and to evaluate proteinuria. In the HIV test, HIV proteins are separated by SDS-PAGE and subsequently detected by Western Blot with HIV-specific antibodies of the patient, if they are present in his blood serum. SDS-PAGE for proteinuria evaluates the levels of various serum proteins in the urine, e.g. Albumin, Alpha-2-macroglobulin and IgG.

Variants

SDS-PAGE is the most widely used method for gel electrophoretic separation of proteins. Two-dimensional gel electrophoresis sequentially combines isoelectric focusing or BAC-PAGE with a SDS-PAGE. Native PAGE is used if native protein folding is to be maintained. For separation of membrane proteins, BAC-PAGE or CTAB-PAGE may be used as an alternative to SDS-PAGE. For electrophoretic separation of larger protein complexes, agarose gel electrophoresis can be used, e.g. the SDD-AGE. Some enzymes can be detected via their enzyme activity by zymography.

Alternatives

While being one of the more precise and low-cost protein separation and analysis methods, the SDS-PAGE denatures proteins. Where non-denaturing conditions are necessary, proteins are separated by a native PAGE or different chromatographic methods with subsequent photometric quantification, for example affinity chromatography, size exclusion chromatography, ion exchange chromatography. Proteins can also be separated by size in a tangential flow filtration or an ultrafiltration. Single proteins can be isolated from a mixture by affinity chromatography or by a pull-down assay. Some historically early and cost effective but crude separation methods usually based upon a series of extractions and precipitations using kosmotropic molecules, for example the ammonium sulfate precipitation and the polyethyleneglycol precipitation.

History

In 1948, Arne Tiselius was awarded the Nobel Prize in Chemistry for the discovery of the principle of electrophoresis as the migration of charged and dissolved atoms or molecules in an electric field. The use of a solid matrix in a zone electrophoresis improved the separation. The discontinuous electrophoresis of 1964 by L. Ornstein and B. J. Davis made it possible to improve the separation by the stacking effect. The use of cross-linked polyacrylamide hydrogels, in contrast to the previously used paper discs or starch gels, provided a higher stability of the gel and no microbial decomposition. The denaturing effect of SDS in continuous polyacrylamide gels and the consequent improvement in resolution was first described in 1965 by David F. Summers in the working group of James E. Darnell to separate poliovirus proteins. The current variant of the SDS-PAGE was described in 1970 by Ulrich K. Laemmli and initially used to characterise the proteins in the head of bacteriophage T4. This Laemmli paper is widely cited for the invention of modern SDS-PAGE, but the technique was actually invented by Jake Maizel, who was doing a sabbatical in the MRC laboratory when Laemmli joined lab as a postdoctoral fellow. Maizel shared his prior technology with Laemmli and together they made further improvements. Laemmli and Maizel had planned to follow up with a Methods paper but this never materialized. Maizel recounts the history of development of SDS-PAGE in brief commentary.