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Expression and modification proteomics during skeletal muscle ageing

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Abstract

Skeletal muscle ageing is characterized by a progressive and dramatic loss of muscle mass and strength leading to decreased muscular function resulting in muscle weakness which is often referred to as sarcopenia. Following the standardisation of “omics” approaches to study the genome (genomics) and the transcriptome (transcriptomics), the study of the proteins encoded by the genome, referred to as proteomics, is a tremendous challenge. Unlike the genome, the proteome varies in response to many physiological or pathological factors. In addition, the proteome is orders of magnitude more complex than the transcriptome due to post-translational modifications, protein oxidation and limited protein degradation. Proteomic studies, including the analysis of protein abundance as well as post-translational modified proteins have been shown to provide valuable information to unravel the key molecular pathways implicated in complex biological processes, such as tissue and organ ageing. In this article, we will describe proteomic approaches for the analysis of protein abundance as well as the specific protein targets for oxidative damage upon oxidative stress and/or during skeletal muscle ageing.

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References

  • Ahmed EK, Rogowska-Wrzesinska A, Roepstorff P, Bulteau AL, Friguet B (2010) Protein modification and replicative senescence of WI-38 human embryonic fibroblasts. Aging Cell 9(2):252–272. doi:10.1111/j.1474-9726.2010.00555.x

    Article  PubMed  CAS  Google Scholar 

  • Andersson DC, Betzenhauser MJ, Reiken S, Meli AC, Umanskaya A, Xie W, Shiomi T, Zalk R, Lacampagne A, Marks AR (2011) Ryanodine receptor oxidation causes intracellular calcium leak and muscle weakness in aging. Cell Metab 14:196–207

    Article  PubMed  CAS  Google Scholar 

  • Bandopadhyay R, Kingsbury AE et al (2004) The expression of DJ-1 (PARK7) in normal human CNS and idiopathic Parkinson’s disease. Brain 127:420–430

    Article  PubMed  Google Scholar 

  • Baraibar MA, Friguet B (2012) Changes of the proteasomal system during the aging process. Prog Mol Biol Transl Sci 109:249–275. doi:10.1016/B978-0-12-397863-9.00007-9

    Article  PubMed  CAS  Google Scholar 

  • Baraibar MA, Friguet B (2013) Oxidative proteome modifications target specific cellular pathways during oxidative stress, cellular senescence and aging. Exp Gerontol. doi: 10.1016/j.exger.2012.10.007

  • Baraibar MA, Hyzewicz J, Rogowska-Wrzesinska A, Ladouce R, Roepstorff P, Mouly V, Friguet B (2011) Oxidative stress-induced proteome alterations target different cellular pathways in human myoblasts. Free Radic Biol Med 51(8):1522–1532. doi:10.1016/j.freeradbiomed.2011.06.032

    Article  PubMed  CAS  Google Scholar 

  • Baraibar MA, Liu L, Ahmed EK, Friguet B (2012a) Protein oxidative damage at the crossroads of cellular senescence, aging, and age-related diseases. Oxid Med Cell Longev 2012:919832. doi:10.1155/2012/919832

    Article  PubMed  Google Scholar 

  • Baraibar MA, Barbeito AG, Muhoberac BB, Vidal R (2012b) A mutant light-chain ferritin that causes neurodegeneration has enhanced propensity toward oxidative damage. Free Radic Biol Med 52(9):1692–1697. doi:10.1016/j.freeradbiomed.2012.02.015

    Article  PubMed  CAS  Google Scholar 

  • Baraibar MA, Ladouce R, Friguet B (2012c) A method for detecting and/or quantifying carbonylated proteins, PCT/EP2012/061749. http://patentscope.wipo.int/search/en/WO2012175519. Accessed 27 Dec 2012

  • Barreiro E, Hussain SN (2010) Protein carbonylation in skeletal muscles: impact on function. Antioxid Redox Signal 12(3):417–429. doi:10.1089/ars.2009.2808

    Article  PubMed  CAS  Google Scholar 

  • Barreiro E, Coronell V, Laviña B et al (2006) Aging, sex differences, and oxidative stress in human respiratory and limb muscles. Free Radic Biol Med 41(5):797–809

    Article  PubMed  CAS  Google Scholar 

  • Baumgartner RN, Koehler KM, Gallagher D, Romero L, Heymsfield SB, Ross RR, Garry PJ, Lindeman RD (1998) Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol 147(8):755–763

    Article  PubMed  CAS  Google Scholar 

  • Berlett BS, Stadtman ER (1997) Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 272(33):20313–20316

    Article  PubMed  CAS  Google Scholar 

  • Biteau B, Labarre J, Toledano MB (2003) ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425(6961):980–984

    Article  PubMed  CAS  Google Scholar 

  • Breusing N, Grune T (2008) Regulation of proteasome-mediated protein degradation during oxidative stress and aging. Biol Chem 389:203–209

    Article  PubMed  CAS  Google Scholar 

  • Capitanio D, Vasso M, Fania C, Moriggi M, Viganò A, Procacci P, Magnaghi V, Gelfi C (2009) Comparative proteomic profile of rat sciatic nerve and gastrocnemius muscle tissues in ageing by 2-D DIGE. Proteomics 9:2004–2020. doi:10.1002/pmic.200701162

    Article  PubMed  CAS  Google Scholar 

  • Chan CY, McDermott JC, Siu KW (2011) Secretome analysis of skeletal myogenesis using SILAC and shotgun proteomics. Int J Proteomics 2011:329467. doi:10.1155/2011/329467

    PubMed  Google Scholar 

  • Choksi KB, Papaconstantinou J (2008) Age-related alterations in oxidatively damaged proteins of mouse heart mitochondrial electron transport chain complexes. Free Radic Biol Med 44(10):1795–1805. doi:10.1016/j.freeradbiomed.2008.01.032

    Article  PubMed  CAS  Google Scholar 

  • Clark KA, McElhinny AS, Beckerle MC, Gregorio CC (2002) Striated muscle cytoarchitecture: an intricate web of form and function. Annu Rev Cell Dev Biol 18:637–706

    Article  PubMed  CAS  Google Scholar 

  • Donoghue P, Staunton L, Mullen E, Manning G, Ohlendieck K (2010) DIGE analysis of rat skeletal muscle proteins using nonionic detergent phase extraction of young adult versus aged gastrocnemius tissue. J Proteomics 73(8):1441–1453. doi:10.1016/j.jprot.2010.01.014

    Article  PubMed  CAS  Google Scholar 

  • Doran P, Gannon J, O’Connell K, Ohlendieck K (2007) Ageing skeletal muscle shows a drastic increase in the small heat shock proteins B-crystallin/HspB5 and cvHsp/HspB7. Eur J Cell Biol 86:629–640

    Article  PubMed  CAS  Google Scholar 

  • Doran P, O’Connell K, Gannon J, Kavanagh M, Ohlendieck K (2008) Opposite pathobiochemical fate of pyruvate kinase and adenylate kinase in aged rat skeletal muscle as revealed by proteomic DIGE analysis. Proteomics 8:364–377

    Article  PubMed  CAS  Google Scholar 

  • Droge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95

    PubMed  CAS  Google Scholar 

  • Duguez S, Duddy W, Johnston H, Laine J, Le Bihan MC, Brown KJ, Bigot A, Hathout Y, Butler-Browne G, Partridge T (2013) Dystrophin deficiency leads to disturbance of LAMP1-vesicle-associated protein secretion. Cell Mol Life Sci. doi:10.1007/s00018-012-1248-2

  • Engerson TD, McKelvey TG, Rhyne DB, Boggio EB, Snyder SJ, Jones HP (1987) Conversion of xanthine dehydrogenase to oxidase in ischemic rat tissues. J Clin Invest 79:1564–1570

    Article  PubMed  CAS  Google Scholar 

  • Engler D (2007) Hypothesis: Musculin is a hormone secreted by skeletal muscle, the body’s largest endocrine organ. Evidence for actions on the endocrine pancreas to restrain the beta-cell mass and to inhibit insulin secretion and on the hypothalamus to co-ordinate the neuroendocrine and appetite responses to exercise. Acta Biomed 78(Suppl 1):156–206

    PubMed  Google Scholar 

  • Evans WJ (1995) What is sarcopenia? J Gerontol A Biol Sci Med Sci 50 Spec No, 5–8

  • Fedorova M, Kuleva N, Hoffmann R (2010) Identification, quantification, and functional aspects of skeletal muscle protein-carbonylation in vivo during acute oxidative stress. J Proteome Res 9(5):2516–2526. doi:10.1021/pr901182r

    Article  PubMed  CAS  Google Scholar 

  • Ferreira LF, Reid MB (2008) Muscle-derived ROS and thiol regulation in muscle fatigue. J Appl Physiol 104:853–860

    Article  PubMed  CAS  Google Scholar 

  • Friguet B (2002) Aging of proteins and the proteasome. Prog Mol Subcell Biol 29:17–33

    Article  PubMed  CAS  Google Scholar 

  • Friguet B (2006) Oxidized protein degradation and repair in ageing and oxidative stress. FEBS Lett 580(12):2910–2916. doi:10.1016/j.febslet.2006.03.028

    Article  PubMed  CAS  Google Scholar 

  • Friguet B, Bulteau AL, Chondrogianni N, Conconi M, Petropoulos I (2000) Protein degradation by the proteasome and its implications in aging. Ann N Y Acad Sci 908:143–154

    Article  PubMed  CAS  Google Scholar 

  • Fugere NA, Ferrington DA, Thompson LV (2006) Protein nitration with aging in the rat semimembranosus and soleus muscles. J Gerontol Ser A Biol Sci Med Sci 61(8):806–812

    Article  Google Scholar 

  • Gannon J, Staunton L, O’Connell K, Doran P, Ohlendieck K (2008) Phosphoproteomic analysis of aged skeletal muscle. Int J Mol Med 22:33–42

    PubMed  CAS  Google Scholar 

  • Gannon J, Doran P, Kirwan A, Ohlendieck K (2009) Drastic increase of myosin light chain MLC-2 in senescent skeletal muscle indicates fast-to-slow fibre transition in sarcopenia of old age. Eur J Cell Biol 88:685–700. doi:10.1016/j.ejcb.2009.06.004

    Article  PubMed  CAS  Google Scholar 

  • Gelfi C, Vigano A, Ripamonti M, Pontoglio A, Begum S, Pellegrino MA, Grassi B, Bottinelli R, Wait R, Cerretelli P (2006) The human muscle proteome in aging. J Proteome Res 5:1344–1353

    Article  PubMed  CAS  Google Scholar 

  • Gianni P, Jan KJ, Douglas MJ, Stuart PM, Tarnopolsky MA (2004) Oxidative stress and the mitochondrial theory of aging in human skeletal muscle. Exp Gerontol 39(9):1391–1400

    Article  PubMed  CAS  Google Scholar 

  • Gilmore JM, Washburn MP (2010) Advances in shotgun proteomics and the analysis of membrane proteomes. J Proteomics 73(11):2078–2091. doi:10.1016/j.jprot.2010.08.005

    Article  PubMed  CAS  Google Scholar 

  • Giulivi C, Traaseth NJ, Davies KJ (2003) Tyrosine oxidation products: analysis and biological relevance. Amino Acids 25(3–4):227–232

    Article  PubMed  CAS  Google Scholar 

  • Goldfarb LG, Dalakas MC (2009) Tragedy in a heartbeat: malfunctioning desmin causes skeletal and cardiac muscle disease. J Clin Invest 119:1806–1813

    Article  PubMed  CAS  Google Scholar 

  • Gorg A, Drews O, Luck C, Weiland F, Weiss W (2009) 2-DE with IPGs. Electrophoresis 30(Suppl 1):S122–S132. doi:10.1002/elps.200900051

    Article  PubMed  Google Scholar 

  • Görg A, Weiss W, Dunn MJ (2004) Current two-dimensional electrophoresis technology for proteomics. Proteomics 4:3665–3685

    Article  PubMed  Google Scholar 

  • Henningsen J, Rigbolt KT, Blagoev B, Pedersen BK, Kratchmarova I (2010) Dynamics of the skeletal muscle secretome during myoblast differentiation. Mol Cell Proteomics 9(11):2482–2496. doi:10.1074/mcp.M110.002113

    Article  PubMed  CAS  Google Scholar 

  • Hojlund K, Yi Z, Hwang H, Bowen B, 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 Proteomics 7:257–267

    PubMed  CAS  Google Scholar 

  • Horiuchi S, Araki N (1994) Advanced glycation end products of the Maillard reaction and their relation to aging. Gerontology 40(Suppl 2):10–15

    Article  PubMed  CAS  Google Scholar 

  • Jackson MJ, Papa S, Bolanos J et al (2002) Antioxidants, reactive oxygen and nitrogen species, gene induction and mitochondrial function. Mol Aspects Med 23:209–285

    Article  PubMed  CAS  Google Scholar 

  • Kanski J, Hong SJ, Schöneich C (2005) Proteomic analysis of protein nitration in ageing skeletal muscle and identification of nitrotyrosine-containing sequences in vivo by nanoelectrospray ionization tandem mass spectrometry. J Biol Chem 280:24261–24266

    Article  PubMed  CAS  Google Scholar 

  • Kondo H, Miura M, Itokawa Y (1991) Oxidative stress in skeletal muscle atrophied by immobilization. Acta Physiol Scand 142:527–528

    Article  PubMed  CAS  Google Scholar 

  • Kondo H, Nishino K, Itokawa Y (1994) Hydroxyl radical generation in skeletal muscle atrophied by immobilization. FEBS Lett 349:169–172

    Article  PubMed  CAS  Google Scholar 

  • Le Bihan MC, Bigot A, Jensen SS, Dennis JL, Rogowska-Wrzesinska A, Lainé J, Gache V, Furling D, Jensen ON, Voit T, Mouly V, Coulton GR, Butler-Browne G (2012) In-depth analysis of the secretome identifies three major independent secretory pathways in differentiating human myoblasts. J Proteomics 77:344–356. doi:10.1016/j.jprot.2012.09.008

    Article  PubMed  Google Scholar 

  • Lefort N, Yi Z, Bowen B, Glancy B, De Filippis EA, Mapes R, Hwang H, Flynn CR, Willis WT, Civitarese A, Højlund K, Mandarino LJ (2009) Proteome profile of functional mitochondria from human skeletal muscle using one-dimensional gel electrophoresis and HPLC ESI-MS/MS. J Proteomics 72:1046–1060. doi:10.1016/j.jprot.2009.06.011

    Article  PubMed  CAS  Google Scholar 

  • Levine RL, Stadtman ER (2001) Oxidative modification of proteins during aging. Exp Gerontol 36(9):1495–1502

    Article  PubMed  CAS  Google Scholar 

  • Levine RL, Wehr N, Williams JA, Stadtman ER, Shacter E (2000) Determination of carbonyl groups in oxidized proteins. Methods Mol Biol 99:15–24

    PubMed  CAS  Google Scholar 

  • Lombardi A, Silvestri E, Cioffi F, Senese R, Lanni A, Goglia F, de Lange P, Moreno M (2009) Defining the transcriptomic and proteomic profiles of rat ageing skeletal muscle by the use of a cDNA array, 2D- and Blue native-PAGE approach. J Proteomics 72:708–721. doi:10.1016/j.jprot.2009.02.007

    Article  PubMed  CAS  Google Scholar 

  • Madian AG, Regnier FE (2010) Proteomic identification of carbonylated proteins and their oxidation sites. J Proteome Res 9(8):3766–3780. doi:10.1021/pr1002609

    Article  PubMed  CAS  Google Scholar 

  • Marzani B, Felzani G, Bellomo RG, Vecchiet J, Marzatico F (2005) Human muscle ageing: ROS-mediated alterations in rectus abdominis and vastus lateralis muscles. Exp Gerontol 40:959–965

    Article  PubMed  CAS  Google Scholar 

  • Meunier B, Dumas E, Piec I, Béchet D, Hébraud M, Hocquette JF (2007) Assessment of hierarchical clustering methodologies for proteomic data mining. J Proteome Res 6:358–366

    Article  PubMed  CAS  Google Scholar 

  • Moreau R, Heath SH, Doneanu CE, Lindsay JG, Hagen TM (2003) Age-related increase in 4-hydroxynonenal adduction to rat heart alpha-ketoglutarate dehydrogenase does not cause loss of its catalytic activity. Antioxid Redox Signal 5(5):517–527

    Article  PubMed  CAS  Google Scholar 

  • O’Connell K, Ohlendieck K (2009) Proteomic DIGE analysis of the mitochondria-enriched fraction from aged rat skeletal muscle. Proteomics 9:5509–5524

    Article  PubMed  Google Scholar 

  • Pansarasa O, Castagna B, Colombi J, Vecchiet J, Felzani C, Marzatico F (2000) Age and sex differences in human skeletal muscle: role of reactive oxygen species. Free Radic Res 33(3):287–293

    Article  PubMed  CAS  Google Scholar 

  • Petropoulos I, Friguet B (2006) Maintenance of proteins and aging: the role of oxidized protein repair. Free Radic Res 40(12):1269–1276

    Article  PubMed  CAS  Google Scholar 

  • Piec I, Listrat A, Alliot J, Chambon C, Taylor RG, Bechet D (2005) Differential proteome analysis of aging in rat skeletal muscle. FASEB J 19(9):1143–1145. doi:10.1096/fj.04-3084fje

    PubMed  CAS  Google Scholar 

  • Powers SK, Jackson MJ (2008) Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 88:1243–1276

    Article  PubMed  CAS  Google Scholar 

  • Rabilloud T (2002) Two-dimensional gel electrophoresis in proteomics: old, old fashioned, but it still climbs up the mountains. Proteomics 2:3–10

    Article  PubMed  CAS  Google Scholar 

  • Rabilloud T, Lelong C (2011) Two-dimensional gel electrophoresis in proteomics: a tutorial. J Proteomics 74(10):1829–1841. doi:10.1016/j.jprot.2011.05.040

    Article  PubMed  CAS  Google Scholar 

  • Rabilloud T, Heller M, Gasnier F, Luche S, Rey C, Aebersold R, Benahmed M, Louisot P, Lunardi J (2002) Proteomics analysis of cellular response to oxidative stress: evidence for in vivo overoxidation of peroxiredoxins at their active site. J Biol Chem 277:19396–19401

    Article  PubMed  CAS  Google Scholar 

  • Reid MB (2001) Nitric oxide, reactive oxygen species, and skeletal muscle contraction. Med Sci Sports Exerc 33:371–376

    Article  PubMed  CAS  Google Scholar 

  • Roca-Rivada A, Al-Massadi O, Castelao C, Senin LL, Alonso J, Seoane LM, Garcia-Caballero T, Casanueva FF, Pardo M (2012) Muscle tissue as an endocrine organ: comparative secretome profiling of slow-oxidative and fast-glycolytic rat muscle explants and its variation with exercise. J Proteomics 75(17):5414–5425. doi:10.1016/j.jprot.2012.06.037

    Article  PubMed  CAS  Google Scholar 

  • Rogowska-Wrzesinska A, Le Bihan MC, Thaysen-Andersen M, Roepstorff P (2013) 2D gels still have a niche in proteomics. J Proteomics. doi:10.1016/j.jprot.2013.01.010

    Google Scholar 

  • Schiaffino S (2010) Fibre types in skeletal muscle: a personal account. Acta Physiol 199(4):451–463. doi:10.1111/j.1748-1716.2010.02130

    Article  CAS  Google Scholar 

  • Shenton D, Smirnova JB, Selley JN, Carroll K, Hubbard SJ, Pavitt GD, Ashe MP, Grant CM (2006) Global translational responses to oxidative stress impact upon multiple levels of protein synthesis. J Biol Chem 281:29011–29021

    Article  PubMed  CAS  Google Scholar 

  • Shindoh C, DiMarco A, Nethery D, Supinski G (1992) Effect of PEG-superoxide dismutase on the diaphragmatic response to endotoxin. Am Rev Respir Dis 145:1350–1354

    Article  PubMed  CAS  Google Scholar 

  • Short KR, Bigelow ML, Kahl J, Singh R, Coenen-Schimke J, Raghavakaimal S, Nair KS (2005) Decline in skeletal muscle mitochondrial function with ageing in humans. Proc Natl Acad Sci USA 102:5618–5623

    Article  PubMed  CAS  Google Scholar 

  • Snijders T, Verdijk LB, van Loon LJ (2009) The impact of sarcopenia and exercise training on skeletal muscle satellite cells. Ageing Res Rev 8(4):328–338. doi:10.1016/j.arr.2009.05.003

    Article  PubMed  Google Scholar 

  • Snow LM, Fugere NA, Thompson LV (2007) Advanced glycation end-product accumulation and associated protein modification in type II skeletal muscle with ageing. J Gerontol Ser A Biol Sci Med Sci 62(11):1204–1210

    Article  Google Scholar 

  • Stadtman ER, Levine RL (2003) Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids 25(3–4):207–218

    Article  PubMed  CAS  Google Scholar 

  • Staunton L, Zweyer M, Swandulla D, Ohlendieck K (2012) Mass spectrometry-based proteomic analysis of middle-aged vs. aged vastus lateralis reveals increased levels of carbonic anhydrase isoform 3 in senescent human skeletal muscle. Int J Mol Med 30:723–733. doi:10.3892/ijmm.2012.1056

    PubMed  CAS  Google Scholar 

  • Thompson LV, Durand D, Fugere NA, Ferrington DA (2006) Myosin and actin expression and oxidation in aging muscle. J Appl Physiol 101(6):1581–1587. doi:10.1152/japplphysiol.00426.2006

    Article  PubMed  CAS  Google Scholar 

  • Ünlü M, Minden JS (2002) Difference gel electrophoresis. In: Walker JM (ed) The protein protocols handbook. Humana Press, Totowa, pp 185–196

    Chapter  Google Scholar 

  • Whidden MA, McClung JM, Falk DJ, Hudson MB, Smuder AJ, Nelson WB, Powers SK (2009) Xanthine oxidase contributes to mechanical ventilation-induced diaphragmatic oxidative stress and contractile dysfunction. J Appl Physiol 106:385–394

    Article  PubMed  CAS  Google Scholar 

  • Yan LJ, Forster MJ (2011) Chemical probes for analysis of carbonylated proteins: a review. J Chromatogr B Anal Technol Biomed Life Sci 879(17–18):1308–1315. doi:10.1016/j.jchromb.2010.08.004

    Article  CAS  Google Scholar 

  • Yoon JH, Kim J, Song P, Lee TG, Suh PG, Ryu SH (2012) Secretomics for skeletal muscle cells: a discovery of novel regulators? Adv Biol Regul 52(2):340–350. doi:10.1016/j.jbior.2012.03.001

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors are very thankful to the FP7 EU-funded project MyoAge (No. 223576), Inserm, UPMC, AFLD and the Association Française contre les Myopathies (AFM). M.A.B has received a post-doctoral fellowship from MyoAge and is currently the recipient of a post-doctoral fellowship from the Association Française contre les Myopathies (AFM). S.D. has received a post-doctoral fellowship from MyoAge. M.G. is supported by a PhD fellowship from the Conseil Régional Auvergne and Fonds Européens de Développement Régional (FEDER). The authors are grateful to Romain Ladouce for his expert assistance with the Oxi-DIGE.

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  1. Laboratoire de Biologie Cellulaire du Vieillissement, UR4, UPMC Paris 6 University, 4 place Jussieu, 75252, Paris Cedex 05, France

    Martin A. Baraibar & Bertrand Friguet

  2. INRA, UMR1019, Centre de Recherche en Nutrition Humaine, Université d’Auvergne, 63122, Saint Genès Champanelle, France

    Marine Gueugneau & Daniel Bechet

  3. Thérapie des maladies du muscle strié, Institut de Myologie, UMRS 974, UPMC Université Paris 6, U974-Inserm, UMR7215-CNRS/AIM, GH Pitié-Salpétrière, 47 bd de l’Hôpital, 75651, Paris cedex 13, France

    Stephanie Duguez & Gillian Butler-Browne

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  1. Martin A. Baraibar
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  2. Marine Gueugneau
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Correspondence to Bertrand Friguet.

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Baraibar, M.A., Gueugneau, M., Duguez, S. et al. Expression and modification proteomics during skeletal muscle ageing. Biogerontology 14, 339–352 (2013). https://doi.org/10.1007/s10522-013-9426-7

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