Extracellular Matrix Proteomics: The mdx-4cv Mouse Diaphragm as a Surrogate for Studying Myofibrosis in Dystrophinopathy
Abstract
:1. Introduction
2. Proteomic Strategies to Study the Extracellular Matrix
2.1. Bottom-Up Proteomics versus Top-Down Proteomics
2.2. Sample Handling and Protein Extraction for Gel-Free and Bottom-Up Proteomics
2.3. Sample Handling and Protein Extraction for Gel-Based and Top-Down Proteomics
2.4. Extracellular-Matrix-Enrichment-Based Proteomic-Profiling Approaches
2.5. Mass Spectrometry and Data Acquisition
3. The Extracellular Matrix of Skeletal Muscles
- The stabilization of skeletal muscle fibers, and the provision of tissue strength and elasticity;
- Structural support via physical scaffolding, and the provision of an embedding medium for motor units, capillaries, and pools of satellite cells;
- The provision of neuromuscular homeostasis;
- Mechanical force transduction from muscle fibers to the surrounding tissues;
- The provision of cell–matrix interactions for the support of cell adhesion and cell migration during embryonic myogenesis, adult myogenesis, and tissue repair;
- Cell–matrix support during cell differentiation, maturation, remodeling, fiber transitions, and muscle aging.
4. The mdx-4cv Mouse Model and Dystrophinopathy-Associated Myofibrosis
4.1. Duchenne Muscular Dystrophy and Fibrosis
4.2. Characterization of the mdx-4cv Mouse within the Context of Other Dystrophic Models
4.3. Histological and Biochemical Characterization of Fibrosis in the mdx-4cv Mouse Diaphragm
4.4. Proteomic Profiling of Fibrosis in the mdx-4cv Mouse Diaphragm
- (i)
- Basal-lamina-enriched extracellular matrix proteins:
- Collagen IV (COL4A1, COL4A2, COL4A3);
- Collagen XV (COL15A1);
- Collagen XVIII (COL18A1);
- Nidogen-2/Osteonidogen (NID2).
- (ii)
- Endomysium-enriched extracellular matrix proteins:
- Collagen V (COL5A1, COL5A2);
- Collagen VI (COL6A1, COL6A2, COL6A5, COL6A6).
- (iii)
- Matrisomal proteins of the endomysium, perimysium, and epimysium:
- Fibronectin (FN1);
- Vitronectin (VTN);
- Dermatopontin (DPT).
- (iv)
- Small leucine-rich proteoglycans:
- Asporin (ASPN);
- Biglycan (BGN);
- Decorin (DCN);
- Lumican (LUM);
- Mimecan/Osteoglycin (OGN).
- (v)
- Non-structural matricellular proteins:
- Periostin (POSTN).
- (vi)
- Extracellular-matrix-associated repair proteins:
- Annexin-2 (ANXA2);
- Annexin-6 (ANXA6).
- (vii)
- Adhesion receptors:
- Integrin, alpha-7 (ITGA7);
- Integrin, beta-1 (ITGB1);
- Dystroglycan, alpha/beta (DAG1).
- (viii)
- Myotendinous-junction-enriched proteins:
- Collagen XII (COL12A1).
- (ix)
- Tendon-enriched proteins:
- Collagen I (COL1A1, COL1A2).
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
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Accession Number | Extracellular Matrix Protein | Gene Name | Coverage (%) | Peptides | kDa |
---|---|---|---|---|---|
(i) Basal-lamina-enriched extracellular matrix proteins | |||||
Q60675 | Laminin-211, subunit alpha-2 | Lama2 | 21.8 | 47 | 343.6 |
P02469 | Laminin-211, subunit beta-1 | Lamb1 | 14.9 | 16 | 197.0 |
P02468 | Laminin-211, subunit gamma-1 | Lamc1 | 30.2 | 31 | 172.2 |
P02463 | Collagen IV, alpha-1 | Col4a1 | 4.4 | 5 | 160.6 |
P08122 | Collagen IV, alpha-2 | Col4a2 | 2.5 | 3 | 167.2 |
O35206 | Collagen XV, alpha-1 | Col15a1 | 10.0 | 9 | 140.4 |
P39061-2 | Collagen XVIII, alpha-1 | Col18a1 | 2.8 | 3 | 134.1 |
Q05793 | Perlecan (HSPG-2) | Hspg2 | 20.7 | 43 | 398.0 |
P10493 | Nidogen-1 (entactin) | Nid1 | 30.1 | 18 | 136.5 |
O88322 | Nidogen-2 (osteonidogen) | Nid2 | 5.9 | 6 | 153.8 |
(ii) Endomysium-enriched extracellular matrix proteins | |||||
O88207 | Collagen V, alpha-1 | Col5a1 | 1.6 | 2 | 183.6 |
Q04857 | Collagen VI, alpha-1 | Col6a1 | 29.2 | 20 | 108.4 |
Q02788 | Collagen VI, alpha-2 | Col6a2 | 21.2 | 14 | 110.3 |
A6H584 | Collagen VI, alpha-5 | Col6a5 | 9.2 | 17 | 289.4 |
Q8C6K9 | Collagen VI, alpha-6 | Col6a6 | 12.5 | 16 | 246.2 |
(iii) Extracellular matrix proteins throughout the endomysium, perimysium, and epimysium | |||||
Q9JK53 | Prolargin | Prelp | 25.7 | 7 | 43.3 |
Q9QZZ6 | Dermatopontin (tyrosine-rich acidic matrix protein) | Dpt | 19.4 | 2 | 24.0 |
P29788 | Vitronectin | Vtn | 6.7 | 2 | 54.8 |
P11276 | Fibronectin | Fn1 | 15.8 | 22 | 272.4 |
E9PV24 | Fibrinogen, alpha | Fga | 24.2 | 12 | 87.4 |
Q8K0E8 | Fibrinogen, beta | Fgb | 63.6 | 24 | 54.7 |
Q8VCM7 | Fibrinogen, gamma | Fgg | 64.5 | 18 | 49.4 |
Q9D1H9 | Microfibril-associated glycoprotein MFAP4 | Mfap4 | 17.1 | 3 | 28.9 |
Q61554 | Fibrillin-1 | Fbn1 | 21.6 | 39 | 312.1 |
(iv) Major muscle-associated small leucine-rich proteoglycans (SLRP type) | |||||
Q99MQ4 | Asporin | Aspn | 24.1 | 7 | 42.5 |
P28653 | Biglycan | Bgn | 26.6 | 7 | 41.6 |
P28654 | Decorin | Dcn | 34.5 | 11 | 39.8 |
P50608 | Fibromodulin | Fmod | 26.1 | 6 | 43.0 |
P51885 | Lumican | Lum | 27.2 | 6 | 38.2 |
Q62000 | Mimecan (Osteoglycin) | Ogn | 32.2 | 7 | 34.0 |
(v) Matricellular proteins | |||||
Q62009-5 | Periostin | Postn | 9.6 | 4 | 87.0 |
P35441 | Thrombospondin-1 | Thbs1 | 15.4 | 12 | 129.6 |
Q9Z1T2 | Thrombospondin-4 | Thbs4 | 23.7 | 2 | 106.3 |
Q9WVH9 | Fibulin-5 | Fbln5 | 8.3 | 3 | 50.2 |
(vi) Major sarcolemmal adhesion proteins/linkers to the extracellular matrix | |||||
Q61738-4 | Integrin, alpha-7 | Itga7 | 8.5 | 6 | 122.1 |
P09055 | Integrin, beta-1 | Itgb1 | 19.3 | 11 | 88.2 |
Q62165 | Dystroglycan, alpha/beta | Dag1 | 4.1 | 3 | 96.8 |
(vii) Myotendinous-junction-enriched proteins | |||||
Q60847-2 | Collagen XII, alpha-1 | Col12a1 | 18.5 | 36 | 333.5 |
Q8CIB5 | FERM-domain containing kindlin 2 (FERMT-2) | Fermt2 | 6.5 | 3 | 77.8 |
(viii) Tendon-enriched proteins | |||||
P11087 | Collagen I, alpha-1 | Col1a1 | 5.3 | 5 | 137.9 |
Q01149 | Collagen I, alpha-2 | Col1a2 | 5.0 | 5 | 129.5 |
(ix) Cartilage-enriched proteins | |||||
Q9R0G6 | Cartilage oligomeric matrix protein | Comp | 3.7 | 2 | 82.3 |
Q66K08 | Cartilage intermediate layer protein 1 | Cilp | 3.9 | 3 | 132.2 |
D3Z7H8 | Cartilage intermediate layer protein 2 | Cilp2 | 3.6 | 3 | 125.9 |
(x) Extracellular matrix proteins involved in cellular signaling | |||||
P82198 | Transforming growth factor-beta-induced protein ig-h3 | Tgfbi | 28.0 | 12 | 74.5 |
P21981 | Protein-glutamine gamma-glutamyltransferase 2 | Tgm2 | 36.0 | 15 | 77.0 |
(xi) Extracellular-matrix-associated proteins belonging to the annexin family | |||||
P07356 | Annexin A2 | Anxa2 | 56.3 | 16 | 38.7 |
P14824 | Annexin A6 | Anxa6 | 51.0 | 23 | 75.8 |
(xii) Extracellular matrix regulators | |||||
Q00897 | Alpha-1-antitrypsin 1-4 (A1AT4) | Serpina1d | 44.6 | 11 | 46.0 |
P22599 | Alpha-1-antitrypsin 1-2 (A1AT2) | Serpina1b | 38.0 | 9 | 45.2 |
Q00896 | Alpha-1-antitrypsin 1-3 (A1AT3) | Serpina1c | 35.9 | 9 | 45.8 |
Q00898 | Alpha-1-antitrypsin 1-5 (A1AT5) | Serpina1e | 26.2 | 8 | 45.9 |
P19324 | Serpin H1 (SERPH) | Serpinh1 | 9.6 | 3 | 46.5 |
P07759 | Serine protease inhibitor A3K | Serpina3k | 26.8 | 8 | 46.8 |
P10605 | Cathepsin B | Ctsb | 22.4 | 5 | 37.3 |
Mouse Model | Genetic Alteration | Affected Dystrophin Isoforms | Dystrophic Phenotype |
---|---|---|---|
mdx (mdx-23) | Exon-23 of Dmd gene; spontaneous premature stop codon | Dp427 | Moderate, but severely affected diaphragm; degeneration–regeneration cycles; considerable number of revertant muscle fibers; mildly affected heart muscle |
mdx/Dtna | Exon-23 of Dmd gene; plus dKO of Dtna gene | Dp427 | Severely affected general musculature; moderately affected heart muscle |
mdx/Cmah | Exon-23 of Dmd gene; plus Exon-6 deletion of Cmah gene | Dp427 | Severely affected general musculature; moderately affected diaphragm and heart |
mdx/Utr | Exon-23 of Dmd gene; plus targeted disruption of Utrn gene | Dp427; plus lacking autosomal dystrophin homologue utrophin (Up395) | Severely affected general musculature including diaphragm; moderately affected heart muscle |
mdx/α7 | Exon-23 of Dmd gene; plus dKO of Itga7 gene | Dp427 | Severely affected general musculature including diaphragm; mildly affected heart muscle |
mdx/Myod1 | Exon-23 of Dmd gene; plus dKO of Myod1 gene | Dp427 | Severely affected general musculature including diaphragm, and heart muscle |
mdx-2cv | Intron-42 of Dmd gene; ENU-mutagenesis-induced shift in reading frame | Dp427, Dp260 | Moderate with large variation in muscle fiber size; severely affected diaphragm |
mdx-3cv | Intron-65 of Dmd gene; ENU-mutagenesis-induced shift in reading frame | Dp427, Dp260, Dp140, Dp116, Dp71 | Moderate, but severely affected diaphragm; no revertant fibers |
mdx-4cv | Exon-53 of Dmd gene; ENU-mutagenesis-induced premature stop codon | Dp427, Dp260, Dp140 | Moderate with large variation in muscle fiber size; severely affected diaphragm; fewer revertant fibers than mdx-23 model |
NSG-mdx-4cv | Exon-54 of Dmd gene; immunodeficient muscular dystrophy model | Dp427, Dp260, Dp140 | Moderate, but severely affected diaphragm; fewer revertant fibers than mdx-23 model |
mdx-4cv/mTR-G2 | Exon-53 of Dmd gene; KO of mTR; model with humanized telomere lengths | Dp427, Dp260, Dp140 | Severely affected general musculature including diaphragm, and heart muscle |
mdx-5cv | Exon-10 of Dmd gene; ENU-mutagenesis-induced frame shift deletion | Dp427 | Moderate, but severely affected diaphragm; fewer revertant fibers than mdx-23 model |
mdx-52 | Exon-52 of Dmd gene; targeted disruption induced point mutation | Dp427, Dp260, Dp140 | Moderate, but severely affected diaphragm; fewer revertant fibers than mdx-23 model |
mdx-βgeo | Intron-63 of Dmd gene; insertion of β-geo gene trap cassette | Dp427, Dp260, Dp140, Dp116, Dp71 | Moderately affected general musculature |
Dmd-null | Dmd gene deletion; Cre-loxP system of entire Dmd gene | Dp427, Dp260, Dp140, Dp116, Dp71 | Severely affected general musculature |
hDMD/mdx-45 | Spontaneous Exon-23 mutation of Dmd gene; plus CRISPR/Cas-mediated Exon-45 deletion in hDMD gene | Dp427, Dp260, Dp140 (murine and human) | Moderate, but severely affected diaphragm; revertant muscle fibers |
hDMD/mdx-52 | Spontaneous Exon-23 mutation of Dmd gene; plus TALEN-based partial deletion of Exon-52 in hDMD gene | Dp427, Dp260, Dp140 (murine and human) | Moderate, but severely affected diaphragm; revertant muscle fibers |
Experimental Focus | Bioanalytical Approach | Major Findings | References |
---|---|---|---|
(i) Generation, genotyping, and phenotyping of the mdx-4cv model | |||
Generation of mdx-4cv model | Chemical mutagenesis with N-ethyl-N-nitrosourea (ENU) | Induction of a C-to-T transition at position 7916 in exon-53 of the Dmd gene leading to premature translation termination | [41] |
Genotyping of mdx-4cv model | DNA sequencing, polymerase chain reaction analysis | Protein-truncating nonsense mutation that introduces premature stop codon in exon-53 of Dmd gene | [42,43,44,237] |
Characterization of mdx-4cv model | Cell biological and biochemical analyses | Less revertant fibers compared to spontaneous mdx-23 mouse; reduced level of dystrophin–glycoprotein complex | [231] |
(ii) Evaluation of experimental therapies using the mdx-4cv model | |||
Exon-skipping therapy | Antisense molecule-based skipping of defective exon | Removal of exon-53 by-passed the protein-truncating mutation and restored the synthesis of semi-functional Dp427-M protein | [238] |
Micro-dystrophin gene therapy | Virus- or nano-carrier mediated delivery of micro-dystrophin gene | Increased numbers of micro-dystrophin positive fibers using a variety of delivery mechanisms | [239,240,241,242,243] |
Cell-based therapy | Cell transplantation to introduce mini-dystrophin protein in dystrophic fibers | High levels of mini-dystrophin expression, but no physiological improvements | [244,245,246] |
Genome editing | CRISPR/Cas9 (clustered regularly interspaced short palindromic repeats)/CRISPR-associated protein 9) | Increased dystrophin expression in CRISPR/Cas9-treated muscles and increased force generation. | [247,248] |
(iii) Proteomic profiling of skeletal muscle tissue specimens from the mdx-4cv model | |||
Skeletal muscle, hindlimb | Liquid chromatography– tandem mass spectrometry (LC-MS/MS) | Increased collagen VI, fibronectin, fibrinogen, asporin, annexin-2; reduced dystrophin complex, carbonic anhydrase CA3, parvalbumin, myozenin-2 | [229] |
Diaphragm muscle | LC-MS/MS | Increased extracellular matrix proteins (collagens, annexins, proteoglycans) and molecular chaperones; decreased dystrophin complex, parvalbumin, carbonic anhydrase CA3, excitation–contraction coupling proteins | [55,146] |
Extraocular muscle | LC-MS/MS | Mild phenotype lacking drastic changes in protein abundance | [252] |
Subcellular skeletal muscle fractions | Subcellular fractionation, affinity purification, LC-MS/MS | Increased membrane repair proteins (myoferlin, dysferlin, annexins) and extracellular matrix proteins (collagens); decrease in dystrophin complex | [230,251] |
Skeletal muscle protein fractions | Chemical crosslinking analysis | Altered patterns of protein interactions in dystrophin-deficient fibers | [249,250] |
(iv) Proteomic profiling of non-skeletal muscle tissue specimens from the mdx-4cv model | |||
Heart | LC-MS/MS | Decreased dystrophin complex; identified changes in laminin, periostin, asporin, and lumican, heat shock proteins, mitochondrial and glycolytic enzymes | [253] |
Liver | LC-MS/MS | Elevated levels of fatty-acid-binding protein FABP5; changes in proteins involved in fatty acid, carbohydrate, and amino acid metabolism | [254] |
Kidney | LC-MS/MS | Elevated levels of fatty-acid-binding protein FABP1; complex changes in metabolic and bioenergetic enzymes | [255,256] |
Stomach/pancreas interface | LC-MS/MS | Identification of dystrophin complex in normal stomach muscles; reduced dystrophin complex in mdx-4cv stomach/pancreas-interface | [258] |
Spleen | LC-MS/MS | Identification of short dystrophin isoform in spleen; altered proteins involved in metabolism, signaling, and cellular architecture; crosstalk between lymphoid system and muscle | [96,257] |
Brain | LC-MS/MS | Increased levels of gliosis marker GFAP (glial fibrillary acidic protein); altered abundance of a variety of neuronal proteins | [259] |
(v) Proteomic profiling of biofluids from the mdx-4cv model | |||
Serum | LC-MS/MS | Increased levels of various muscle damage markers in serum; high levels of the inflammation-induced plasma marker haptoglobin | [260,261] |
Saliva | LC-MS/MS | Increased levels of kallikrein Kkl-1 and the Klk1-related peptidases Klk1-b1, Klk1-b5 and Klk-b22 | [261,263] |
Urine | LC-MS/MS | Increased levels of various muscle damage markers in urine; high levels of titin fragments | [262] |
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Dowling, P.; Gargan, S.; Zweyer, M.; Swandulla, D.; Ohlendieck, K. Extracellular Matrix Proteomics: The mdx-4cv Mouse Diaphragm as a Surrogate for Studying Myofibrosis in Dystrophinopathy. Biomolecules 2023, 13, 1108. https://doi.org/10.3390/biom13071108
Dowling P, Gargan S, Zweyer M, Swandulla D, Ohlendieck K. Extracellular Matrix Proteomics: The mdx-4cv Mouse Diaphragm as a Surrogate for Studying Myofibrosis in Dystrophinopathy. Biomolecules. 2023; 13(7):1108. https://doi.org/10.3390/biom13071108
Chicago/Turabian StyleDowling, Paul, Stephen Gargan, Margit Zweyer, Dieter Swandulla, and Kay Ohlendieck. 2023. "Extracellular Matrix Proteomics: The mdx-4cv Mouse Diaphragm as a Surrogate for Studying Myofibrosis in Dystrophinopathy" Biomolecules 13, no. 7: 1108. https://doi.org/10.3390/biom13071108