Proteomic reference map for sarcopenia research: mass spectrometric identification of key muscle proteins of organelles, cellular signaling, bioenergetic metabolism and molecular chaperoning

Published: 24 May 2024
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During the natural aging process, frailty is often associated with abnormal muscular performance. Although inter-individual differences exit, in most elderly the tissue mass and physiological functionality of voluntary muscles drastically decreases. In order to study age-related contractile decline, animal model research is of central importance in the field of biogerontology. Here we have analyzed wild type mouse muscle to establish a proteomic map of crude tissue extracts. Proteomics is an advanced and large-scale biochemical method that attempts to identify all accessible proteins in a given biological sample. It is a technology-driven approach that uses mass spectrometry for the characterization of individual protein species. Total protein extracts were used in this study in order to minimize the potential introduction of artefacts due to excess subcellular fractionation procedures. In this report, the proteomic survey of aged muscles has focused on organellar marker proteins, as well as proteins that are involved in cellular signaling, the regulation of ion homeostasis, bioenergetic metabolism and molecular chaperoning. Hence, this study has establish a proteomic reference map of a highly suitable model system for future aging research.

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Aebersold R, Mann M. Mass-spectrometric exploration of proteome structure and function. Nature 2016;537:347-55. DOI: https://doi.org/10.1038/nature19949
Dowling P, Swandulla D, Ohlendieck K. Mass spectrometry-based proteomic technology and its application to study skeletal muscle cell biology. Cells 2023;12:2560. DOI: https://doi.org/10.3390/cells12212560
Uzozie AC, Aebersold R. Advancing translational research and precision medicine with targeted proteomics. J Proteomics 2018;189:1-10. DOI: https://doi.org/10.1016/j.jprot.2018.02.021
Sobsey CA, Ibrahim S, Richard VR, et al. Targeted and untargeted proteomics approaches in biomarker development. Proteomics 2020;20:e1900029. DOI: https://doi.org/10.1002/pmic.201900029
Nakka K, Ghigna C, Gabellini D, Dilworth FJ. Diversification of the muscle proteome through alternative splicing. Skelet Muscle 2018;8:8. DOI: https://doi.org/10.1186/s13395-018-0152-3
Zhong Q, Zheng K, Li W, et al. Post-translational regulation of muscle growth, muscle aging and sarcopenia. J Cachexia Sarcopenia Muscle 2023;14:1212-27. DOI: https://doi.org/10.1002/jcsm.13241
Schaffer LV, Millikin RJ, Miller RM, et al. Identification and quantification of proteoforms by mass spectrometry. Proteomics 2019;19:e1800361. DOI: https://doi.org/10.1002/pmic.201800361
Carbonara K, Andonovski M, Coorssen JR. Proteomes are of proteoforms: embracing the complexity. Proteomes 2021;9:38. DOI: https://doi.org/10.3390/proteomes9030038
Murphy S, Dowling P, Ohlendieck K. Comparative skeletal muscle proteomics using two-dimensional gel electrophoresis. Proteomes 2016;4:27. DOI: https://doi.org/10.3390/proteomes4030027
Adhikari S, Nice EC, Deutsch EW, et al. A high-stringency blueprint of the human proteome. Nat Commun 2020;11:5301. DOI: https://doi.org/10.1038/s41467-020-19045-9
Capitanio D, Moriggi M, Gelfi C. Mapping the human skeletal muscle proteome: progress and potential. Expert Rev Proteomics 2017;14:825-39. DOI: https://doi.org/10.1080/14789450.2017.1364996
Gonzalez-Freire M, Semba RD, Ubaida-Mohien C, et al. The human skeletal muscle proteome project: a reappraisal of the current literature. J Cachexia Sarcopenia Muscle 2017;8:5-18. DOI: https://doi.org/10.1002/jcsm.12121
Dowling P, Zweyer M, Swandulla D, Ohlendieck K. Characterization of contractile proteins from skeletal muscle using gel-based top-down proteomics. Proteomes 2019;7:25. Erratum in: Proteomes 2019;7. DOI: https://doi.org/10.3390/proteomes7030028
Lermyte F, Tsybin YO, O'Connor PB, Loo JA. Top or Middle? Up or Down? Toward a standard lexicon for protein top-down and allied mass spectrometry approaches. J Am Soc Mass Spectrom 2019;30:1149-57. DOI: https://doi.org/10.1007/s13361-019-02201-x
Ercan H, Resch U, Hsu F, et al. A practical and analytical comparative study of gel-based top-down and gel-free bottom-up proteomics including unbiased proteoform detection. Cells 2023;12:747. DOI: https://doi.org/10.3390/cells12050747
Zhang Y, Fonslow BR, Shan B, et al. Protein analysis by shotgun/bottom-up proteomics. Chem Rev 2013;113:2343-94. DOI: https://doi.org/10.1021/cr3003533
Manes NP, Nita-Lazar A. Application of targeted mass spectrometry in bottom-up proteomics for systems biology research. J Proteomics 2018;189:75-90 DOI: https://doi.org/10.1016/j.jprot.2018.02.008
Melby JA, Roberts DS, Larson EJ, et al. Novel strategies to address the challenges in top-down proteomics. J Am Soc Mass Spectrom 2021;32:1278-94. DOI: https://doi.org/10.1021/jasms.1c00099
Ohlendieck K. Top-down proteomics and comparative 2D-DIGE analysis. Methods Mol Biol 2023;2596:19-38. DOI: https://doi.org/10.1007/978-1-0716-2831-7_2
Burniston JG, Connolly J, Kainulainen H, et al. Label-free profiling of skeletal muscle using high-definition mass spectrometry. Proteomics 2014;14:2339-44. DOI: https://doi.org/10.1002/pmic.201400118
Cervone DT, Moreno-Justicia R, Quesada JP, Deshmukh AS. Mass spectrometry-based proteomics approaches to interrogate skeletal muscle adaptations to exercise. Scand J Med Sci Sports 2024;34:e14334. DOI: https://doi.org/10.1111/sms.14334
Florin A, Lambert C, Sanchez C, et al. The secretome of skeletal muscle cells: A systematic review. Osteoarthr Cartil Open 2020;2:100019. DOI: https://doi.org/10.1016/j.ocarto.2019.100019
Ohlendieck K. Skeletal muscle proteomics: current approaches, technical challenges and emerging techniques. Skelet Muscle 2011;1:6. DOI: https://doi.org/10.1186/2044-5040-1-6
Deshmukh AS, Murgia M, Nagaraj N, et al. Deep proteomics of mouse skeletal muscle enables quantitation of protein isoforms, metabolic pathways, and transcription factors. Mol Cell Proteomics 2015;14:841-53. DOI: https://doi.org/10.1074/mcp.M114.044222
Højlund K, Yi Z, Hwang H, et al. Characterization of the human skeletal muscle proteome by one-dimensional gel electrophoresis and HPLC-ESI-MS/MS. Mol Cell Proteomics 2008;7:257-67. DOI: https://doi.org/10.1074/mcp.M700304-MCP200
Parker KC, Walsh RJ, Salajegheh M, et al. Characterization of human skeletal muscle biopsy samples using shotgun proteomics. J Proteome Res 2009;8:3265-77. DOI: https://doi.org/10.1021/pr800873q
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 2019;40:9-28. DOI: https://doi.org/10.1007/s10974-019-09507-z
Hadrévi J, Hellström F, Kieselbach T, et al. Protein differences between human trapezius and vastus lateralis muscles determined with a proteomic approach. BMC Musculoskelet Disord 2011;12:181. DOI: https://doi.org/10.1186/1471-2474-12-181
Eggers B, Schork K, Turewicz M, et al. Advanced fiber type-specific protein profiles derived from adult murine skeletal muscle. Proteomes 2021;9:28. DOI: https://doi.org/10.3390/proteomes9020028
Murgia M, Nagaraj N, Deshmukh AS, et al. Single muscle fiber proteomics reveals unexpected mitochondrial specialization. EMBO Rep 2015;16:387-95. DOI: https://doi.org/10.15252/embr.201439757
Fomchenko KM, Walsh EM, Yang X, et al. Spatial proteomic approach to characterize skeletal muscle myofibers. J Proteome Res 2021;20:888-94. DOI: https://doi.org/10.1021/acs.jproteome.0c00673
Donoghue P, Doran P, Wynne K, et al K. Proteomic profiling of chronic low-frequency stimulated fast muscle. Proteomics 2007;7:3417-30. DOI: https://doi.org/10.1002/pmic.200700262
Dowling P, Murphy S, Ohlendieck K. Proteomic profiling of muscle fibre type shifting in neuromuscular diseases. Expert Rev Proteomics 2016;13:783-99. DOI: https://doi.org/10.1080/14789450.2016.1209416
Hunt LC, Graca FA, Pagala V, et al. Integrated genomic and proteomic analyses identify stimulus-dependent molecular changes associated with distinct modes of skeletal muscle atrophy. Cell Rep 2021;37:109971. DOI: https://doi.org/10.1016/j.celrep.2021.109971
Deshmukh AS, Steenberg DE, Hostrup M, et al. Deep muscle-proteomic analysis of freeze-dried human muscle biopsies reveals fiber type-specific adaptations to exercise training. Nat Commun 2021;12:304. Erratum in: Nat Commun 2021;12:1600. DOI: https://doi.org/10.1038/s41467-020-20556-8
Li FH, Sun L, Wu DS, Gao HE, Min Z. Proteomics-based identification of different training adaptations of aged skeletal muscle following long-term high-intensity interval and moderate-intensity continuous training in aged rats. Aging (Albany NY) 2019;11:4159-4182. Erratum in: Aging (Albany NY) 2019;11:10781-2. DOI: https://doi.org/10.18632/aging.102044
de Sousa Neto IV, Carvalho MM, Marqueti RC, et al. Proteomic changes in skeletal muscle of aged rats in response to resistance training. Cell Biochem Funct 2020;38:500-9. DOI: https://doi.org/10.1002/cbf.3497
Hesketh SJ, Stansfield BN, Stead CA, Burniston JG. The application of proteomics in muscle exercise physiology. Expert Rev Proteomics 2020;17:813-25. DOI: https://doi.org/10.1080/14789450.2020.1879647
Gelfi C, Vasso M, Cerretelli P. Diversity of human skeletal muscle in health and disease: contribution of proteomics. J Proteomics 2011;74:774-95. DOI: https://doi.org/10.1016/j.jprot.2011.02.028
Choi YC, Hong JM, Park KD, et al. Proteomic analysis of the skeletal muscles from dysferlinopathy patients. J Clin Neurosci 2020;71:186-90. DOI: https://doi.org/10.1016/j.jocn.2019.08.068
Gargan S, Dowling P, Zweyer M, et al. Proteomic Identification of Markers of Membrane Repair, Regeneration and Fibrosis in the Aged and Dystrophic Diaphragm. Life (Basel) 2022;12:1679. DOI: https://doi.org/10.3390/life12111679
Giebelstein J, Poschmann G, Højlund K, et al. The proteomic signature of insulin-resistant human skeletal muscle reveals increased glycolytic and decreased mitochondrial enzymes. Diabetologia 2012;55:1114-27. Erratum in: Diabetologia 2012;55:2083. DOI: https://doi.org/10.1007/s00125-012-2456-x
Kruse R, Højlund K. Proteomic study of skeletal muscle in obesity and type 2 diabetes: progress and potential. Expert Rev Proteomics 2018;15:817-28. DOI: https://doi.org/10.1080/14789450.2018.1528147
Shum AMY, Poljak A, Bentley NL, et al. Proteomic profiling of skeletal and cardiac muscle in cancer cachexia: alterations in sarcomeric and mitochondrial protein expression. Oncotarget 2018;9:22001-22. DOI: https://doi.org/10.18632/oncotarget.25146
Gelfi C, Vigano A, Ripamonti M, et al. The human muscle proteome in aging. J Proteome Res 2006;5:1344-53. DOI: https://doi.org/10.1021/pr050414x
Staunton L, Zweyer M, Swandulla D, Ohlendieck K. 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 2012;30:723-33. DOI: https://doi.org/10.3892/ijmm.2012.1056
Ohlendieck K. Two-CyDye-Based 2D-DIGE Analysis of Aged Human Muscle Biopsy Specimens. Methods Mol Biol 2023;2596:265-89. DOI: https://doi.org/10.1007/978-1-0716-2831-7_19
Gueugneau M, Coudy-Gandilhon C, Gourbeyre O, et al. Proteomics of muscle chronological ageing in post-menopausal women. BMC Genomics 2014;15:1165. DOI: https://doi.org/10.1186/1471-2164-15-1165
Baraibar MA, Gueugneau M, Duguez S, et al. Expression and modification proteomics during skeletal muscle ageing. Biogerontology 2013;14:339-52. DOI: https://doi.org/10.1007/s10522-013-9426-7
Théron L, Gueugneau M, Coudy C, et al. Label-free quantitative protein profiling of vastus lateralis muscle during human aging. Mol Cell Proteomics 2014;13:283-94. DOI: https://doi.org/10.1074/mcp.M113.032698
Murphy S, Zweyer M, Henry M, et al. Proteomic analysis of the sarcolemma-enriched fraction from dystrophic mdx-4cv skeletal muscle. J Proteomics 2019;191:212-27. DOI: https://doi.org/10.1016/j.jprot.2018.01.015
Dowling P, Gargan S, Zweyer M, et al. Proteomic profiling of the interface between the stomach wall and the pancreas in dystrophinopathy. Eur J Transl Myol 2021;31:9627. DOI: https://doi.org/10.4081/ejtm.2020.9627
Gargan S, Ohlendieck K. Sample Preparation and Protein Determination for 2D-DIGE Proteomics. Methods Mol Biol 2023;2596:325-37. DOI: https://doi.org/10.1007/978-1-0716-2831-7_22
Wiśniewski JR, Zougman A, Nagaraj N, Mann M. Universal sample preparation method for proteome analysis. Nat Methods 2009;6:359-62. DOI: https://doi.org/10.1038/nmeth.1322
Wiśniewski JR. Filter Aided Sample Preparation - A tutorial. Anal Chim Acta 2019;1090:23-30. DOI: https://doi.org/10.1016/j.aca.2019.08.032
Dowling P, Gargan S, Zweyer M, et al. Protocol for the Bottom-Up Proteomic Analysis of Mouse Spleen. STAR Protoc 2020;1:100196. DOI: https://doi.org/10.1016/j.xpro.2020.100196
Szklarczyk D, Gable AL, Nastou KC, et al. The STRING database in 2021: customizable protein-protein networks, and functional characterization of user-uploaded gene/measurement sets. Nucleic Acids Res 2021;49:D605-12. Erratum in: Nucleic Acids Res 2021;49:10800. DOI: https://doi.org/10.1093/nar/gkaa1074
Doran P, O'Connell K, Gannon J, Kavanagh M, Ohlendieck K. Opposite pathobiochemical fate of pyruvate kinase and adenylate kinase in aged rat skeletal muscle as revealed by proteomic DIGE analysis. Proteomics 2008;8:364-77. DOI: https://doi.org/10.1002/pmic.200700475
Capitanio D, Vasso M, Fania C, et al. Comparative proteomic profile of rat sciatic nerve and gastrocnemius muscle tissues in ageing by 2-D DIGE. Proteomics 2009;9:2004-20. DOI: https://doi.org/10.1002/pmic.200701162
Lombardi A, Silvestri E, Cioffi F, et al. 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 2009;72:708-21. DOI: https://doi.org/10.1016/j.jprot.2009.02.007
Gannon J, Doran P, Kirwan A, Ohlendieck K. 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 2009;88:685-700. DOI: https://doi.org/10.1016/j.ejcb.2009.06.004
Lourenço Dos Santos S, Baraibar MA, Lundberg S, et al. Oxidative proteome alterations during skeletal muscle ageing. Redox Biol 2015;5:267-74. DOI: https://doi.org/10.1016/j.redox.2015.05.006
Gregorich ZR, Peng Y, Cai W, et al. Top-down targeted proteomics reveals decrease in myosin regulatory light-chain phosphorylation that contributes to sarcopenic muscle dysfunction. J Proteome Res 2016;15:2706-16. DOI: https://doi.org/10.1021/acs.jproteome.6b00244
Capitanio D, Vasso M, De Palma S, et al. Specific protein changes contribute to the differential muscle mass loss during ageing. Proteomics 2016;16:645-56. DOI: https://doi.org/10.1002/pmic.201500395
Doran P, Gannon J, O'Connell K, Ohlendieck K. Aging skeletal muscle shows a drastic increase in the small heat shock proteins alphaB-crystallin/HspB5 and cvHsp/HspB7. Eur J Cell Biol 2007;86:629-40. DOI: https://doi.org/10.1016/j.ejcb.2007.07.003
Dowling P, Gargan S, Swandulla D, Ohlendieck K. Fiber-type shifting in sarcopenia of old age: proteomic profiling of the contractile apparatus of skeletal muscles. Int J Mol Sci 2023;24:2415. DOI: https://doi.org/10.3390/ijms24032415
Hatton IA, Galbraith ED, Merleau NSC, et al. The human cell count and size distribution. Proc Natl Acad Sci U S A 2023;120:e2303077120. DOI: https://doi.org/10.1073/pnas.2303077120
Frontera WR, Ochala J. Skeletal muscle: a brief review of structure and function. Calcif Tissue Int 2015;96:183-95. DOI: https://doi.org/10.1007/s00223-014-9915-y
Mukund K, Subramaniam S. Skeletal muscle: A review of molecular structure and function, in health and disease. Wiley Interdiscip Rev Syst Biol Med 2020;12:e1462. DOI: https://doi.org/10.1002/wsbm.1462
Brooks SV, Guzman SD, Ruiz LP. Skeletal muscle structure, physiology, and function. Handb Clin Neurol 2023;195:3-16. DOI: https://doi.org/10.1016/B978-0-323-98818-6.00013-3
Thompson R, Spendiff S, Roos A, et al. Advances in the diagnosis of inherited neuromuscular diseases and implications for therapy development. Lancet Neurol 2020;19:522-532. DOI: https://doi.org/10.1016/S1474-4422(20)30028-4
Cruz-Jentoft AJ, Sayer AA. Sarcopenia. Lancet 2019;393:2636-46. Erratum in: Lancet 2019;393:2590. DOI: https://doi.org/10.1016/S0140-6736(19)31138-9
Larsson L, Degens H, Li M, et al. Sarcopenia: aging-related loss of muscle mass and function. Physiol Rev 2019;99:427-511. DOI: https://doi.org/10.1152/physrev.00061.2017
Nishikawa H, Fukunishi S, Asai A, et al. Pathophysiology and mechanisms of primary sarcopenia (Review). Int J Mol Med 2021;48:156. DOI: https://doi.org/10.3892/ijmm.2021.4989
Kim JW, Kim R, Choi H, et al. Understanding of sarcopenia: from definition to therapeutic strategies. Arch Pharm Res 2021;44:876-89. DOI: https://doi.org/10.1007/s12272-021-01349-z
Zheng Y, Feng J, Yu Y, et al. Advances in sarcopenia: mechanisms, therapeutic targets, and intervention strategies. Arch Pharm Res. 2024;47:301-324. DOI: https://doi.org/10.1007/s12272-024-01493-2
Liu JC, Dong SS, Shen H, et al. Multi-omics research in sarcopenia: Current progress and future prospects. Ageing Res Rev 2022;76:101576. DOI: https://doi.org/10.1016/j.arr.2022.101576
Rivero-Segura NA, Bello-Chavolla OY, Barrera-Vázquez OS, et al. Promising biomarkers of human aging: In search of a multi-omics panel to understand the aging process from a multidimensional perspective. Ageing Res Rev 2020;64:101164. DOI: https://doi.org/10.1016/j.arr.2020.101164
Pan Y, Ji T, Li Y, Ma L. Omics biomarkers for frailty in older adults. Clin Chim Acta 2020;510:363-72. DOI: https://doi.org/10.1016/j.cca.2020.07.057
Danese E, Montagnana M, Lippi G. Proteomics and frailty: a clinical overview. Expert Rev Proteomics 2018;15:657-64. DOI: https://doi.org/10.1080/14789450.2018.1505511
Fernández-Lázaro D, Garrosa E, Seco-Calvo J, Garrosa M. Potential satellite cell-linked biomarkers in aging skeletal muscle tissue: proteomics and proteogenomics to monitor sarcopenia. Proteomes 2022;10:29. DOI: https://doi.org/10.3390/proteomes10030029
Moaddel R, Ubaida-Mohien C, Tanaka T, et al. Proteomics in aging research: A roadmap to clinical, translational research. Aging Cell 2021;20:e13325. DOI: https://doi.org/10.1111/acel.13325
O'Connell K, Ohlendieck K. Proteomic DIGE analysis of the mitochondria-enriched fraction from aged rat skeletal muscle. Proteomics 2009;9:5509-24. DOI: https://doi.org/10.1002/pmic.200900472
Xu X, Wen Z. The mediating role of inflammaging between mitochondrial dysfunction and sarcopenia in aging: a review. Am J Clin Exp Immunol 2023;12:109-26.
Miao Y, Xie L, Song J, et al. Unraveling the causes of sarcopenia: Roles of neuromuscular junction impairment and mitochondrial dysfunction. Physiol Rep 2024;12:e15917. DOI: https://doi.org/10.14814/phy2.15917
Staunton L, O'Connell K, Ohlendieck K. Proteomic profiling of mitochondrial enzymes during skeletal muscle aging. J Aging Res 2011;2011:908035. DOI: https://doi.org/10.4061/2011/908035
Ohlendieck K. Proteomics of skeletal muscle glycolysis. Biochim Biophys Acta 2010;1804:2089-101. DOI: https://doi.org/10.1016/j.bbapap.2010.08.001
Vogt C, Ardehali H, Iozzo P, et al. Regulation of hexokinase II expression in human skeletal muscle in vivo. Metabolism 2000;49:814-8. DOI: https://doi.org/10.1053/meta.2000.6245
Xu H, Ahn B, Van Remmen H. Impact of aging and oxidative stress on specific components of excitation contraction coupling in regulating force generation. Sci Adv 2022;8:eadd7377. DOI: https://doi.org/10.1126/sciadv.add7377
O'Connell K, Gannon J, Doran P, Ohlendieck K. Reduced expression of sarcalumenin and related Ca2+ -regulatory proteins in aged rat skeletal muscle. Exp Gerontol 2008;43:958-61. DOI: https://doi.org/10.1016/j.exger.2008.07.006
Delbono O. Expression and regulation of excitation-contraction coupling proteins in aging skeletal muscle. Curr Aging Sci 2011;4:248-59. DOI: https://doi.org/10.2174/1874609811104030248
Fennel ZJ, Amorim FT, Deyhle MR, et al. The heat shock connection: skeletal muscle hypertrophy and atrophy. Am J Physiol Regul Integr Comp Physiol 2022;323:R133-48. DOI: https://doi.org/10.1152/ajpregu.00048.2022
Brinkmeier H, Ohlendieck K. Chaperoning heat shock proteins: proteomic analysis and relevance for normal and dystrophin-deficient muscle. Proteomics Clin Appl 2014;8:875-95. DOI: https://doi.org/10.1002/prca.201400015
Dimauro I, Antonioni A, Mercatelli N, Caporossi D. The role of αB-crystallin in skeletal and cardiac muscle tissues. Cell Stress Chaperones 2018;23:491-505. DOI: https://doi.org/10.1007/s12192-017-0866-x
Tedesco B, Cristofani R, Ferrari V, et al. Insights on human small heat shock proteins and their alterations in diseases. Front Mol Biosci 2022;9:842149. DOI: https://doi.org/10.3389/fmolb.2022.842149
Senf SM. Skeletal muscle heat shock protein 70: diverse functions and therapeutic potential for wasting disorders. Front Physiol 2013;4:330. DOI: https://doi.org/10.3389/fphys.2013.00330
Schopf FH, Biebl MM, Buchner J. The HSP90 chaperone machinery. Nat Rev Mol Cell Biol 2017;18:345-60. DOI: https://doi.org/10.1038/nrm.2017.20
Schiene-Fischer C. Multidomain peptidyl prolyl cis/trans isomerases. Biochim Biophys Acta 2015;1850:2005-16. DOI: https://doi.org/10.1016/j.bbagen.2014.11.012
Islam R, Yoon H, Shin HR, et al. Peptidyl-prolyl cis-trans isomerase NIMA interacting 1 regulates skeletal muscle fusion through structural modification of Smad3 in the linker region. J Cell Physiol 2018;233:9390-403. DOI: https://doi.org/10.1002/jcp.26774
Van Long N, Chien PN, Tung TX, et al. Complementary combination of biomarkers for diagnosis of sarcopenia in C57BL/6J mice. Life Sci 2023;312:121213. DOI: https://doi.org/10.1016/j.lfs.2022.121213
Aging Biomarker Consortium; Bao H, Cao J, et al. Biomarkers of aging. Sci China Life Sci 2023;66:893-1066. DOI: https://doi.org/10.1007/s11427-023-2305-0
Ohlendieck K. Proteomic profiling of fast-to-slow muscle transitions during aging. Front Physiol 2011;2:105. DOI: https://doi.org/10.3389/fphys.2011.00105
Liu C, Cheung WH, Li J, et al. Understanding the gut microbiota and sarcopenia: a systematic review. J Cachexia Sarcopenia Muscle 2021;12:1393-407. DOI: https://doi.org/10.1002/jcsm.12784
Sakuma K, Hamada K, Yamaguchi A, Aoi W. Current nutritional and pharmacological approaches for attenuating sarcopenia. Cells 2023;12:2422. DOI: https://doi.org/10.3390/cells12192422
Shen Y, Shi Q, Nong K, et al. Exercise for sarcopenia in older people: A systematic review and network meta-analysis. J Cachexia Sarcopenia Muscle 2023;14:1199-211. DOI: https://doi.org/10.1002/jcsm.13225
Mo Y, Zhou Y, Chan H, et al. The association between sedentary behaviour and sarcopenia in older adults: a systematic review and meta-analysis. BMC Geriatr 2023;23:877. DOI: https://doi.org/10.1186/s12877-023-04489-7
Ganapathy A, Nieves JW. Nutrition and sarcopenia-what do we know? Nutrients 2020;12:1755. DOI: https://doi.org/10.3390/nu12061755
Kim J, Lee JY, Kim CY. A comprehensive review of pathological mechanisms and natural dietary ingredients for the management and prevention of sarcopenia. Nutrients 2023;15:2625. DOI: https://doi.org/10.3390/nu15112625
Cochet C, Belloni G, Buondonno I, et al. The role of nutrition in the treatment of sarcopenia in old patients: from restoration of mitochondrial activity to improvement of muscle performance, a systematic review. Nutrients 2023;15:3703. DOI: https://doi.org/10.3390/nu15173703
Granic A, Suetterlin K, Shavlakadze T, et al. Hallmarks of ageing in human skeletal muscle and implications for understanding the pathophysiology of sarcopenia in women and men. Clin Sci (Lond) 2023;137:1721-51. DOI: https://doi.org/10.1042/CS20230319
Coletta G, Phillips SM. An elusive consensus definition of sarcopenia impedes research and clinical treatment: A narrative review. Ageing Res Rev 2023;86:101883. DOI: https://doi.org/10.1016/j.arr.2023.101883
Alhmly HF, Fielding RA. A critical review of current worldwide definitions of sarcopenia. Calcif Tissue Int 2024;114:74-81. DOI: https://doi.org/10.1007/s00223-023-01163-3
Yuan S, Larsson SC. Epidemiology of sarcopenia: Prevalence, risk factors, and consequences. Metabolism 2023;144:155533. DOI: https://doi.org/10.1016/j.metabol.2023.155533
Montero-Errasquín B, Cruz-Jentoft AJ. Acute sarcopenia. Gerontology 2023;69:519-25. DOI: https://doi.org/10.1159/000529052
Christian CJ, Benian GM. Animal models of sarcopenia. Aging Cell 2020;19:e13223. DOI: https://doi.org/10.1111/acel.13223
Xie WQ, He M, Yu DJ, et al. Mouse models of sarcopenia: classification and evaluation. J Cachexia Sarcopenia Muscle 2021;12:538-54. DOI: https://doi.org/10.1002/jcsm.12709

Supporting Agencies

Kathleen Lonsdale Institute for Human Health Research, Science Foundation Ireland Infrastructure Award

How to Cite

Dowling, P., Gargan, S., Zweyer, M., Henry, M., Meleady, P., Swandulla, D., & Ohlendieck, K. (2024). Proteomic reference map for sarcopenia research: mass spectrometric identification of key muscle proteins of organelles, cellular signaling, bioenergetic metabolism and molecular chaperoning. European Journal of Translational Myology, 34(2). https://doi.org/10.4081/ejtm.2024.12565

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