Comparative Skeletal Muscle Proteomics Using Two-Dimensional Gel Electrophoresis
Abstract
:1. Introduction
2. Two-Dimensional Gel Electrophoresis of Skeletal Muscle Proteins
3. Cataloguing of the Skeletal Muscle Proteome Using Two-Dimensional Gel Electrophoresis
- Possible under-estimation of particular types of proteins, including highly hydrophobic proteins, very high-molecular-mass proteins and low-copy-number proteins. Changing gel conditions, the introduction of suitable pre- and post-fractionation steps, as well as higher sensitivity detection protocols can often overcome some of these technical limitations [84,85,86,87].
- Hypothetical under-representation or 2D streaking of proteins with extreme pI-values, which however depends heavily on the particular IEF conditions employed in the first dimensional separation step. Often very acidic protein species form vertical streaking patterns at the pH 3 region and very basic proteins at the pH 11 region. To at least partially overcome this problem, the usage of narrow-range immobilized pH gradients can be applied for zooming in on protein species that do not fall into the commonly applied range of approximately pI 3 to 11 [88,89,90,91]. In addition, combining the findings from several different IEF gels in the first dimension with slightly overlapping pI-values can be advantageous for producing more comprehensive protein coverage [15,92,93].
- Potentially restricted separation of complex protein mixtures with greatly differing molecular masses using routine 2D-GE approaches. Often the usage of large-scale gels, optimized gradient SDS-PAGE slab gel systems in the second dimension and the reduction of sample complexity can overcome some of these technical problems and be used to cover protein species that do not fall into in the routinely analyzed range of approximately 10 to 250 kDa [67,94].
- Latent cross-contamination of individual 2D protein spots through highly abundant polypeptides that are dragged throughout the 2D gel system due to their exceedingly high density. These abnormal electrophoretic mobility patterns of particular proteins cause a certain degree of 2D streaking, which can be minimized by (i) decreasing the total amount of protein loading; (ii) using very large gel systems with a higher discriminatory capacity and/or (iii) applying optimized pre-fractionation techniques to decisively decrease sample complexity [95,96,97,98]. Artifacts can be kept to a minimum using 50 to 200 μg of total protein in first dimension gels. Lower protein concentrations usually result in weak staining patterns. Comparative studies with fluorescent dyes give optimum results with approximately 50 μg of protein per sample.
- Potential discrepancies between the findings from the densitometric scanning of gel images and the MS-based protein identification in case of a heterogeneous composition of a single 2D protein spot. For example, if a protein spot contains more than one protein species and the most abundant protein is not as susceptible to digestion as the low-copy-number proteins in its vicinity, then the concentration change of this 2D protein spot (as determined by densitometric scanning) may be misleading. However, this analytical complication is a relatively rare occurrence and the use of simple post-fractionation approaches and/or independent verification of gel-based proteomic data by immunoblotting surveys or immunofluorescence microscopical analysis can effectively assess the rate of these kinds of analytical discrepancies [21].
- Extremely reliable protein separation system that can be routinely used in large-scale and high-throughput proteomic surveys. Multi-gel systems using large buffer tanks can run a considerable number of 2D gels in parallel making this approach both cost-effective and highly reproducible for systematic biochemical studies [15,16,17].
- Technical provision of a bioanalytical platform that is ideally suited for the subsequent identification of specific protein isoforms and their PTMs [46,47,48]. Many in-gel staining or labeling methods can specifically highlight PTMs, such as enzyme-conjugated lectin labeling or Pro-Q Emerald staining for glycosylation or the fluorescent Pro-Q Diamond dye for phosphorylation [58,105,106,107].
- Direct visualization of proteins of interest as discrete 2D spots, enabling the exact evaluation of the characteristic combination of the pI-value and relative molecular mass of a particular protein subunit or isoform. This provides a unique analytical advantage over simpler 1D gel systems that display heterogeneous protein bands or LC methods. Often MS data from LC-based analyses do not given efficient information on sequence coverage to unequivocally determine whether a fully intact protein species or fragments have been detected. In contrast, proteomic data from the analysis of distinct 2D-GE spots can be directly correlated with the electrophoretic mobility and thereby the relative molecular mass of the protein of interest [21].
- Since potential discrepancies between the mass spectrometric identification of a protein and its position in a 2D gel in relation to its pI-value and/or molecular mass can be easily assessed, the rate of false positive protein hits can be conveniently measured and swiftly eliminated from the final list of altered protein species. Additional analyses can then determine whether an abnormal or unexpected electrophoretic mobility pattern is due to protein degradation, protein clustering or a technical artifact caused by 2D streaking and cross-contamination [18].
- Rapid and quantitative analyses of paired protein samples can be conducted. An example of an extremely powerful comparative 2D-GE method is the fluorescence 2D-DIGE technique [108] that eliminates gel-to-gel variations by the differential pre-electrophoretic labeling of protein fractions and the subsequent separation on the same 2D gel followed by image analysis [109]. See below section for details on the DIGE method and its application in skeletal muscle proteomics.
4. Comparative Skeletal Muscle Proteomics Using Two-Dimensional Gel Electrophoresis
4.1. Proteome Signature of Skeletal Muscle Development
4.2. Muscle Plasticity and Fiber Type Specification
4.3. Exercise-Induced Proteome Signature
4.4. Hypoxia-Related Muscle Adaptations
4.5. Proteome-Wide Changes during Disuse Atrophy
4.6. Sarcopenia of Old Age
5. Conclusions
Acknowledgments
Author Contributions
Conflicts of Interest
Abbreviations
2D | two-dimensional |
ACT | actin |
DIGE | difference in-gel electrophoresis |
GE | gel electrophoresis |
Hsp | heat shock protein |
IEF | isoelectric focusing |
LC | liquid chromatography |
MBP | myosin binding protein |
MLC | myosin light chain |
MS | mass spectrometry |
MyHC | myosin heavy chain |
PAGE | polyacrylamide gel electrophoresis |
p I | isoelectric point |
PTM | post-translational modification |
SDS | sodium dodecyl sulfate |
TM | tropomyosin |
TN | troponin |
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Proteomic Analysis | Tissue and Species | References |
---|---|---|
Human 2D gel reference maps | Human vastus lateralis and laryngeal muscle | Gelfi et al. [111]; Li et al. [112]; Kovalyova et al. [124] |
Human fast versus slow muscle fibre type specification | Normal human deltoideus and vastus lateralis muscles | Capitanio et al. [115] |
Mouse 2D gel reference maps | Normal mouse gastrocnemius and quadriceps muscle | Sanchez et al. [69]; Raddatz et al. [121] |
Mouse fast versus slow muscle fibre type specification | Normal and kyphoscoliotic mouse soleus and vastus lateralis muscles | Le Bihan et al. [117] |
Rat 2D gel reference map | Normal rat skeletal muscle from the abdominal wall | Yan et al. [70] |
Rat fast versus slow muscle fibre type specification | Normal rat soleus, gastrocnemius and extensor digitorum longus muscles | Okumura et al. [116]; Gelfi et al. [118] |
Rabbit 2D gel reference map | Rabbit gastrocnemius muscle | Almeida et al. [122] |
Bovine 2D gel reference maps | Bovine semitendinosus muscle | Bouley et al. [113]; Chaze et al. [119] |
Pig fast versus slow muscle fibre type specification | Normal pig longissimus dorsi and soleus muscles | Kim et al. [114] |
Pufferfish and killifish 2D gel reference maps | Skeletal muscles from Takifugu rubripes and Fundulus grandis | Lu et al. [125]; Abbaraju et al. [126] |
Mitochondrial 2D gel maps | Subsarcolemmal and intermyofibrillar mitochondria from various rat muscles | Reifschneider et al. [129]; O’Connell et al. [130]; Lombardi et al. [131]; Ferreira et al. [132] |
Contractile apparatus 2D gel map | Enriched acto-myosin apparatus from rat gastrocnemius muscle | Gannon et al. [133] |
Cytosol and nucleus 2D gel map | Nucleus and cytosolic fraction from mouse gastrocnemius and soleus muscles | Vitorino et al. [128] |
Muscle secretome 2D gel maps | Seretome from cultured muscle cells | Gajendran et al. [134]; Hartwig et al. [135] |
2D PTM gel maps of protein glycosylation | Rat leg skeletal muscles | O’Connell et al. [105]; Cieniewski-Bernard et al. [137] |
2D PTM gel map of protein phosphorylation | Rat gastrocnemius muscle | Gannon et al. [106,133] |
2D PTM gel map of protein nitration | Rat leg skeletal muscles | Kanski et al. [136] |
Proteomic Analysis | Skeletal Muscle Tissue | References |
---|---|---|
Postnatal development | Rat tibialis anterior and porcine longissimus dorsi muscle | Sun et al. [158]; Xu et al. [159] |
Myoblast differentiation and myotube formation | C2C12 cell culture model | Tannu et al. [156]; Casadei et al. [157] |
Interval training | Human vastus lateralis muscle | Holoway et al. [172] |
Endurance training | Human vastus lateralis muscle | Egan et al. [173] |
Vibration exercise during long-term bed rest | Human soleus and vastus lateralis | Moriggi et al. [174]; Salanova et al. [175] |
Repeated eccentric exercises | Human rectus femoris muscle | Hody et al. [176] |
Downhill running-induced muscle damage | Human vastus lateralis muscle | Malm and Yu [177] |
Various types of animal endurance training | Rat plantaris, gastrocnemius, tibialis anterior, soleus and epitrochlearis muscles; and horse vastus lateralis muscle | Burniston [178]; Guelfi et al. [181]; Yamaguchi et al. [182]; Gandra et al. [183]; Magherini et al. [185]; Bouwman et al. [186] |
One bout of an exhaustive exercise | Rat gastrocnemius muscle | Gandra et al. [184] |
Endurance training following gene doping | Various mouse leg muscles | Macedo et al. [187] |
Chronic low-frequency electro-stimulation | Rabbit tibialis anterior muscle | Donoghue et al. [179,180] |
High-capacity versus low-capacity runners | Rat soleus muscles | Burniston et al. [188] |
Myostatin-related muscle hypertrophy | Belgium Blue bulls semitendious muscle lacking myostatin | Bouley et al. [164]; Keady et al. [165] |
Hypoxia-induced muscle adaptations | Zebrafish, rat and human vastus lateralis muscle | Bosworth et al. [191]; De Palma et al. [192]; Vigano et al. [193]; Levett et al. [194] |
Disuse atrophy due to neuromuscular unloading, immobilization or denervation | Rat soleus, tibialis anterior, laryngeal and gastrocnemius muscles | Isfort et al. [196,197,198]; Seo et al. [199]; Moriggi et al. [200]; Ferreira et al. [201]; Basco et al. [202]; Wang et al. [203]; Li et al. [204]; Sato et al. [205] |
Skeletal muscle aging | Various aged rat skeletal muscles, including the gastrocnemius muscle | O’Connell et al. [105,216]; Gannon et al. [106,133] Kanski et al. [136]; Feng et al. [239]; Doran et al. [217,220]; Piec et al. [240]; Capitanio et al. [221,223] |
Sarcopenia of old age | Various aged human skeletal muscles, including the vastus lateralis muscle | Gelfi et al. [219]; Staunton et al. [222] |
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Murphy, S.; Dowling, P.; Ohlendieck, K. Comparative Skeletal Muscle Proteomics Using Two-Dimensional Gel Electrophoresis. Proteomes 2016, 4, 27. https://doi.org/10.3390/proteomes4030027
Murphy S, Dowling P, Ohlendieck K. Comparative Skeletal Muscle Proteomics Using Two-Dimensional Gel Electrophoresis. Proteomes. 2016; 4(3):27. https://doi.org/10.3390/proteomes4030027
Chicago/Turabian StyleMurphy, Sandra, Paul Dowling, and Kay Ohlendieck. 2016. "Comparative Skeletal Muscle Proteomics Using Two-Dimensional Gel Electrophoresis" Proteomes 4, no. 3: 27. https://doi.org/10.3390/proteomes4030027
APA StyleMurphy, S., Dowling, P., & Ohlendieck, K. (2016). Comparative Skeletal Muscle Proteomics Using Two-Dimensional Gel Electrophoresis. Proteomes, 4(3), 27. https://doi.org/10.3390/proteomes4030027