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Proteomic profiling of the mouse diaphragm and refined mass spectrometric analysis of the dystrophic phenotype

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Abstract

The diaphragm is a crucial muscle involved in active inspiration and whole body homeostasis. Previous biochemical, immunochemical and cell biological investigations have established the distribution and fibre type-specific expression of key diaphragm proteins. Building on these findings, it was of interest to establish the entire experimentally assessable diaphragm proteome and verify the presence of specific protein isoforms within this specialized subtype of skeletal muscle. A highly sensitive Orbitrap Fusion Tribrid mass spectrometer was used for the systematic identification of the mouse diaphragm-associated protein population. Proteomics established 2925 proteins by high confidence peptide identification. Bioinformatics was used to determine the distribution of the main protein classes, biological processes and subcellular localization within the diaphragm proteome. Following the establishment of the respiratory muscle proteome with special emphasis on protein isoform expression in the contractile apparatus, the extra-sarcomeric cytoskeleton, the extracellular matrix and the excitation–contraction coupling apparatus, the mass spectrometric analysis of the diaphragm was extended to the refined identification of proteome-wide changes in X-linked muscular dystrophy. The comparative mass spectrometric profiling of the dystrophin-deficient diaphragm from the mdx-4cv mouse model of Duchenne muscular dystrophy identified 289 decreased and 468 increased protein species. Bioinformatics was employed to analyse the clustering of changes in protein classes and potential alterations in interaction patterns of proteins involved in metabolism, the contractile apparatus, proteostasis and the extracellular matrix. The detailed pathoproteomic profiling of the mdx-4cv diaphragm suggests highly complex alterations in a variety of crucial cellular processes due to deficiency in the membrane cytoskeletal protein dystrophin.

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References

  • Agbulut O, Noirez P, Beaumont F, Butler-Browne G (2003) Myosin heavy chain isoforms in postnatal muscle development of mice. Biol Cell 95:399–406

    Article  CAS  PubMed  Google Scholar 

  • Allen DG, Whitehead NP, Froehner SC (2016) Absence of dystrophin disrupts skeletal muscle signaling: roles of Ca2+, reactive oxygen species, and nitric oxide in the development of muscular dystrophy. Physiol Rev 96:253–305

    Article  CAS  PubMed  Google Scholar 

  • Bordoni B, Zanier E (2013) Anatomic connections of the diaphragm: influence of respiration on the body system. J Multidiscip Healthc 6:281–291

    Article  PubMed  PubMed Central  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Buu MC (2017) Respiratory complications, management and treatments for neuromuscular disease in children. Curr Opin Pediatr 29:326–333

    Article  PubMed  Google Scholar 

  • Capitanio D, Moriggi M, Gelfi C (2017) Mapping the human skeletal muscle proteome: progress and potential. Expert Rev Proteomics 14:825–839

    Article  CAS  PubMed  Google Scholar 

  • Carberry S, Zweyer M, Swandulla D, Ohlendieck K (2012) Proteomics reveals drastic increase of extracellular matrix proteins collagen and dermatopontin in the aged mdx diaphragm model of Duchenne muscular dystrophy. Int J Mol Med 30:229–234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chapman VM, Miller DR, Armstrong D, Caskey CT (1989) Recovery of induced mutations for X chromosome-linked muscular dystrophy in mice. Proc Natl Acad Sci USA 86:1292–1296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coirault C, Lambert F, Marchand-Adam S, Attal P, Chemla D, Lecarpentier Y (1999) Myosin molecular motor dysfunction in dystrophic mouse diaphragm. Am J Physiol 277:C1170–C1176

    Article  CAS  PubMed  Google Scholar 

  • Coirault C, Pignol B, Cooper RN, Butler-Browne G, Chabrier PE, Lecarpentier Y (2003) Severe muscle dysfunction precedes collagen tissue proliferation in mdx mouse diaphragm. J Appl Physiol 94:1744–1750

    Article  PubMed  Google Scholar 

  • Culligan K, Banville N, Dowling P, Ohlendieck K (2002) Drastic reduction of calsequestrin-like proteins and impaired calcium binding in dystrophic mdx muscle. J Appl Physiol 92:435–445

    Article  CAS  PubMed  Google Scholar 

  • De Luca A, Pierno S, Camerino C, Huxtable RJ, Camerino DC (1998) Effect of taurine on excitation-contraction coupling of extensor digitorum longus muscle of dystrophic mdx mouse. Adv Exp Med Biol 442:115–119

    Article  PubMed  Google Scholar 

  • Desguerre I, Mayer M, Leturcq F, Barbet JP, Gherardi RK, Christov C (2009) Endomysial fibrosis in Duchenne muscular dystrophy: a marker of poor outcome associated with macrophage alternative activation. J Neuropathol Exp Neurol 68:762–773

    Article  PubMed  Google Scholar 

  • Deshmukh AS, Murgia M, Nagaraj N, Treebak JT, Cox J, Mann M (2015) Deep proteomics of mouse skeletal muscle enables quantitation of protein isoforms, metabolic pathways, and transcription factors. Mol Cell Proteom 14:841–853

    Article  CAS  Google Scholar 

  • Doran P, Dowling P, Lohan J, McDonnell K, Poetsch S, Ohlendieck K (2004) Subproteomics analysis of Ca2+-binding proteins demonstrates decreased calsequestrin expression in dystrophic mouse skeletal muscle. Eur J Biochem 271:3943–3952

    Article  CAS  PubMed  Google Scholar 

  • Doran P, Martin G, Dowling P, Jockusch H, Ohlendieck K (2006) Proteome analysis of the dystrophin-deficient MDX diaphragm reveals a drastic increase in the heat shock protein cvHSP. Proteomics 6:4610–4621

    Article  CAS  PubMed  Google Scholar 

  • Doran P, Wilton SD, Fletcher S, Ohlendieck K (2009) Proteomic profiling of antisense-induced exon skipping reveals reversal of pathobiochemical abnormalities in dystrophic mdx diaphragm. Proteomics 9:671–685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dowling P, Murphy S, Ohlendieck K (2016) Proteomic profiling of muscle fibre type shifting in neuromuscular diseases. Expert Rev Proteom 13:783–799

    Article  CAS  Google Scholar 

  • Fuller HR, Graham LC, Llavero Hurtado M, Wishart TM (2016) Understanding the molecular consequences of inherited muscular dystrophies: advancements through proteomic experimentation. Expert Rev Proteom 13:659–671

    Article  CAS  Google Scholar 

  • Gamberi T, Fiaschi T, Valocchia E, Modesti A, Mantuano P, Rolland JF, Sanarica F, De Luca A, Magherini F (2018) Proteome analysis in dystrophic mdx mouse muscle reveals a drastic alteration of key metabolic and contractile proteins after chronic exercise and the potential modulation by anti-oxidant compounds. J Proteom 170:43–58

    Article  CAS  Google Scholar 

  • Geiger PC, Bailey JP, Mantilla CB, Zhan WZ, Sieck GC (2006) Mechanisms underlying myosin heavy chain expression during development of the rat diaphragm muscle. J Appl Physiol 101:1546–1555

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Freire M, Semba RD, Ubaida-Mohien Fabbri E, Scalzo P, Højlund K, Dufresne C, Lyashkov A, Ferrucci L (2017) The Human Skeletal Muscle Proteome Project: a reappraisal of the current literature. J Cachexia Sarcopenia Muscle 8:5–18

    Article  PubMed  Google Scholar 

  • Greising SM, Medina-Martínez JS, Vasdev AK, Sieck GC, Mantilla CB (2015) Analysis of muscle fiber clustering in the diaphragm muscle of sarcopenic mice. Muscle Nerve 52:76–82

    Article  PubMed  PubMed Central  Google Scholar 

  • Guiraud S, Aartsma-Rus A, Vieira NM, Davies KE, van Ommen GJ, Kunkel LM (2015) The pathogenesis and therapy of muscular dystrophies. Annu Rev Genom Hum Genet 16:281–308

    Article  CAS  Google Scholar 

  • Henderson CA, Gomez CG, Novak SM, Mi-Mi L, Gregorio CC (2017) Overview of the muscle cytoskeleton. Compr Physiol 7:891–944

    Article  PubMed  PubMed Central  Google Scholar 

  • Hernández-Ochoa EO, Schneider MF (2018) Voltage sensing mechanism in skeletal muscle excitation-contraction coupling: coming of age or midlife crisis? Skelet Muscle 8:22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Højlund K, Yi Z, Hwang H, Lefort N, Flynn CR, Langlais P, Weintraub ST, Mandarino LJ (2008) Characterization of the human skeletal muscle proteome by one-dimensional gel electrophoresis and HPLC-ESI-MS/MS. Mol Cell Proteom 7:257–267

    Article  CAS  Google Scholar 

  • Holland A, Ohlendieck K (2013) Proteomic profiling of the contractile apparatus from skeletal muscle. Expert Rev Proteom 10:239–257

    Article  CAS  Google Scholar 

  • Holland A, Carberry S, Ohlendieck K (2013) Proteomics of the dystrophin-glycoprotein complex and dystrophinopathy. Curr Protein Pept Sci 14:680–697

    Article  CAS  PubMed  Google Scholar 

  • Holland A, Dowling P, Meleady P, Henry M, Zweyer M, Mundegar RR, Swandulla D, Ohlendieck K (2015a) Label-free mass spectrometric analysis of the mdx-4cv diaphragm identifies the matricellular protein periostin as a potential factor involved in dystrophinopathy-related fibrosis. Proteomics 15:2318–2331

    Article  CAS  PubMed  Google Scholar 

  • Holland A, Henry M, Meleady P, Winkler CK, Krautwald M, Brinkmeier H, Ohlendieck K (2015b) Comparative label-free mass spectrometric analysis of mildly versus severely affected mdx mouse skeletal muscles identifies annexin, lamin, and vimentin as universal dystrophic markers. Molecules 20:11317–11344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holland A, Murphy S, Dowling P, Ohlendieck K (2016) Pathoproteomic profiling of the skeletal muscle matrisome in dystrophinopathy associated myofibrosis. Proteomics 16:345–366

    Article  CAS  PubMed  Google Scholar 

  • Hopf FW, Turner PR, Steinhardt RA (2007) Calcium misregulation and the pathogenesis of muscular dystrophy. Subcell Biochem 45:429–464

    Article  CAS  PubMed  Google Scholar 

  • Hor KN, Mah ML, Johnston P, Cripe TP, Cripe LH (2018) Advances in the diagnosis and management of cardiomyopathy in Duchenne muscular dystrophy. Neuromuscul Disord 28:711–716

    Article  PubMed  Google Scholar 

  • Hussain SN, Cornachione AS, Guichon C, Al Khunaizi A, Leite Fde S, Petrof BJ, Mofarrahi M, Moroz N, de Varennes B, Goldberg P, Rassier DE (2016) Prolonged controlled mechanical ventilation in humans triggers myofibrillar contractile dysfunction and myofilament protein loss in the diaphragm. Thorax 71:436–445

    Article  PubMed  Google Scholar 

  • Ishizaki M, Suga T, Kimura E, Shiota T, Kawano R, Uchida Y, Uchino K, Yamashita S, Maeda Y, Uchino M (2008) Mdx respiratory impairment following fibrosis of the diaphragm. Neuromuscul Disord 18:342–348

    Article  PubMed  Google Scholar 

  • Kanehisa M, Furumichi M, Tanabe M, Sato Y, Morishima K (2017) KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res 45(D1):D353–D361

    Article  CAS  PubMed  Google Scholar 

  • Kelley RC, McDonagh B, Ferreira LF (2018) Advanced aging causes diaphragm functional abnormalities, global proteome remodeling, and loss of mitochondrial cysteine redox flexibility in mice. Exp Gerontol 103:69–79

    Article  CAS  PubMed  Google Scholar 

  • Khirani S, Ramirez A, Aubertin G, Boulé M, Chemouny C, Forin V, Fauroux B (2014) Respiratory muscle decline in Duchenne muscular dystrophy. Pediatr Pulmonol 49:473–481

    Article  PubMed  Google Scholar 

  • Kocjan J, Adamek M, Gzik-Zroska B, Czyżewski D, Rydel M (2017) Network of breathing. Multifunctional role of the diaphragm: a review. Adv Respir Med 85:224–232

    Article  PubMed  Google Scholar 

  • Krüger M, Kötter S (2016) Titin, a central mediator for hypertrophic signaling, exercise-induced mechanosignaling and skeletal muscle remodeling. Front Physiol 7:76

    Article  PubMed  PubMed Central  Google Scholar 

  • Lieberman DA, Faulkner JA, Craig AB Jr, Maxwell LC (1973) Performance and histochemical composition of guinea pig and human diaphragm. J Appl Physiol 34:233–237

    Article  CAS  PubMed  Google Scholar 

  • LoMauro A, D’Angelo MG, Aliverti A (2017) Sleep disordered breathing in duchenne muscular dystrophy. Curr Neurol Neurosci Rep 17:44

    Article  PubMed  Google Scholar 

  • Matsumura CY, Taniguti AP, Pertille A, Santo Neto H, Marques MJ (2011) Stretch-activated calcium channel protein TRPC1 is correlated with the different degrees of the dystrophic phenotype in mdx mice. Am J Physiol Cell Physiol 301:C1344–C1350

    Article  CAS  PubMed  Google Scholar 

  • Matsumura CY, Menezes de Oliveira B, Durbeej M, Marques MJ (2013) Isobaric tagging-based quantification for proteomic analysis: a comparative study of spared and affected muscles from mdx mice at the early phase of dystrophy. PLoS One 8(6):e65831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mázala DA, Grange RW, Chin ER (2015) The role of proteases in excitation-contraction coupling failure in muscular dystrophy. Am J Physiol Cell Physiol 308:C33–C40

    Article  CAS  PubMed  Google Scholar 

  • Mi H, Huang X, Muruganujan A, Tang H, Mills C, Kang D, Thomas PD (2017) PANTHER version 11: expanded annotation data from Gene Ontology and Reactome pathways, and data analysis tool enhancements. Nucleic Acids Res 45:D183–D189

    Article  CAS  PubMed  Google Scholar 

  • Mizuno M (1991) Human respiratory muscles: fibre morphology and capillary supply. Eur Respir J 4:587–601

    CAS  PubMed  Google Scholar 

  • Muller J, Vayssiere N, Royuela M, Leger ME, Muller A, Bacou F, Pons F, Hugon G, Mornet D (2001) Comparative evolution of muscular dystrophy in diaphragm, gastrocnemius and masseter muscles from old male mdx mice. J Muscle Res Cell Motil 22:133–139

    Article  CAS  PubMed  Google Scholar 

  • Murgia M, Nagaraj N, Deshmukh AS, Zeiler M, Cancellara P, Moretti I, Reggiani C, Schiaffino S, Mann M (2015) Single muscle fiber proteomics reveals unexpected mitochondrial specialization. EMBO Rep 16:387–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murphy S, Ohlendieck K (2015) The biochemical and mass spectrometric profiling of the dystrophin complexome from skeletal muscle. Comput Struct Biotechnol J 14:20–27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murphy S, Ohlendieck K (2018) Proteomic profiling of large myofibrillar proteins from dried and long-term stored polyacrylamide gels. Anal Biochem 543:8–11

    Article  CAS  PubMed  Google Scholar 

  • Murphy S, Henry M, Meleady P, Zweyer M, Mundegar RR, Swandulla D, Ohlendieck K (2015a) Simultaneous pathoproteomic evaluation of the dystrophin-glycoprotein complex and secondary changes in the mdx-4cv mouse model of duchenne muscular dystrophy. Biology (Basel) 4:397–423

    CAS  Google Scholar 

  • Murphy S, Zweyer M, Mundegar RR, Henry M, Meleady P, Swandulla D, Ohlendieck K (2015b) Concurrent label-free mass spectrometric analysis of dystrophin isoform Dp427 and the myofibrosis marker collagen in crude extracts from mdx-4cv skeletal muscles. Proteomes 3:298–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murphy S, Dowling P, Ohlendieck K (2016) Comparative skeletal muscle proteomics using two-dimensional gel electrophoresis. Proteomes 4(3):E27

    Article  CAS  PubMed  Google Scholar 

  • Murphy S, Brinkmeier H, Krautwald M, Henry M, Meleady P, Ohlendieck K (2017) Proteomic profiling of the dystrophin complex and membrane fraction from dystrophic mdx muscle reveals decreases in the cytolinker desmoglein and increases in the extracellular matrix stabilizers biglycan and fibronectin. J Muscle Res Cell Motil 38:251–268

    Article  CAS  PubMed  Google Scholar 

  • Murphy S, Henry M, Meleady P, Ohlendieck K (2018) Utilization of dried and long-term stored polyacrylamide gels for the advanced proteomic profiling of mitochondrial contact sites from rat liver. Biol Methods Protoc 3(1):bpy008

    Article  PubMed  PubMed Central  Google Scholar 

  • Murphy S, Dowling P, Zweyer M, Swandulla D, Ohlendieck K (2019a) Proteomic profiling of giant skeletal muscle proteins. Expert Rev Proteom 16:241–256

    Article  CAS  Google Scholar 

  • Murphy S, Zweyer M, Henry M, Meleady P, Mundegar RR, Swandulla D, Ohlendieck K (2019b) Proteomic analysis of the sarcolemma-enriched fraction from dystrophic mdx-4cv skeletal muscle. J Proteom 191:212–227

    Article  CAS  Google Scholar 

  • O’Sullivan F, Keenan J, Aherne S, O’Neill F, Clarke C, Henry M, Meleady P, Breen L, Barron N, Clynes M, Horgan K, Doolan P, Murphy R (2017) Parallel mRNA, proteomics and miRNA expression analysis in cell line models of the intestine. World J Gastroenterol 23:7369–7386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohlendieck K, Swandulla D (2017) Molecular pathogenesis of Duchenne muscular dystrophy-related fibrosis. Pathologe 38:21–29

    Article  CAS  PubMed  Google Scholar 

  • Parker KC, Walsh RJ, Salajegheh M, Amato AA, Krastins B, Sarracino DA, Greenberg SA (2009) Characterization of human skeletal muscle biopsy samples using shotgun proteomics. J Proteome Res 8:3265–3277

    Article  CAS  PubMed  Google Scholar 

  • Petrof BJ, Stedman HH, Shrager JB, Eby J, Sweeney HL, Kelly AM (1993) Adaptations in myosin heavy chain expression and contractile function in dystrophic mouse diaphragm. Am J Physiol 265:C834–C841

    Article  CAS  PubMed  Google Scholar 

  • Polla B, D’Antona G, Bottinelli R, Reggiani C (2004) Respiratory muscle fibres: specialisation and plasticity. Thorax 59:808–817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rayavarapu S, Coley W, Cakir E, Jahnke V, Takeda S, Aoki Y, Grodish-Dressman H, Jaiswal JK, Hoffman EP, Brown KJ, Hathout Y, Nagaraju K (2013) Identification of disease specific pathways using in vivo SILAC proteomics in dystrophin deficient mdx mouse. Mol Cell Proteom 12:1061–1073

    Article  CAS  Google Scholar 

  • Santulli G, Lewis DR, Marks AR (2017) Physiology and pathophysiology of excitation-contraction coupling: the functional role of ryanodine receptor. J Muscle Res Cell Motil 38:37–45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith LR, Meyer G, Lieber RL (2013) Systems analysis of biological networks in skeletal muscle function. Wiley Interdiscip Rev Syst Biol Med 5:55–71

    Article  CAS  PubMed  Google Scholar 

  • Sollanek KJ, Burniston JG, Kavazis AN, Morton AB, Wiggs MP, Ahn B, Smuder AJ, Powers SK (2017) Global proteome changes in the rat diaphragm induced by endurance exercise training. PLoS One 12:e0171007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stedman HH, Sweeney HL, Shrager JB, Maguire HC, Panettieri RA, Petrof B, Narusawa M, Leferovich JM, Sladky JT, Kelly AM (1991) The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature 352:536–539

    Article  CAS  PubMed  Google Scholar 

  • Szklarczyk D, Morris JH, Cook H, Kuhn M, Wyder S, Simonovic M, Santos A, Doncheva NT, Roth A, Bork P, Jensen LJ, von Mering C (2017) The STRING database in 2017: quality-controlled protein-protein association networks, made broadly accessible. Nucleic Acids Res 45:D362–D368

    Article  CAS  PubMed  Google Scholar 

  • Tidball JG, Welc SS, Wehling-Henricks M (2018) Immunobiology of inherited muscular dystrophies. Compr Physiol 8:1313–1356

    Article  PubMed  PubMed Central  Google Scholar 

  • Wiśniewski JR, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation method for proteome analysis. Nat Methods 6:359–362

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Research was supported by project grants from Muscular Dystrophy Ireland and the Irish Health Research Board (HRB/MRCG-2016-20) and a Hume scholarship from Maynooth University. The Orbitrap Fusion Tribrid mass spectrometer was funded under a Science Foundation Ireland Infrastructure Award to Dublin City University (SFI 16/RI/3701).

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  1. Department of Biology, Maynooth University, National University of Ireland, Maynooth, Co. Kildare, Ireland

    Sandra Murphy & Kay Ohlendieck

  2. Newcastle Fibrosis Research Group, Institute of Cellular Medicine, Faculty of Medical Sciences, Newcastle University, Newcastle upon Tyne, UK

    Sandra Murphy

  3. Institute of Physiology II, University of Bonn, 53115, Bonn, Germany

    Margit Zweyer, Maren Raucamp & Dieter Swandulla

  4. National Institute for Cellular Biotechnology, Dublin City University, Dublin 9, Ireland

    Michael Henry & Paula Meleady

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  1. Sandra Murphy
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  2. Margit Zweyer
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Murphy, S., Zweyer, M., Raucamp, M. et al. Proteomic profiling of the mouse diaphragm and refined mass spectrometric analysis of the dystrophic phenotype. J Muscle Res Cell Motil 40, 9–28 (2019). https://doi.org/10.1007/s10974-019-09507-z

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