Single muscle fiber proteomics reveals unexpected mitochondrial specialization

EMBO Reports

Volumn 16, Issue 3, 2015, Pages 387-395

  Murgia, Marta ^a,b   Nagaraj, Nagarjuna ^a   Deshmukh, Atul S ^a,c   Zeiler, Marlis ^a   Cancellara, Pasqua ^b   Moretti, Irene ^d   Reggiani, Carlo ^b   Schiaffino, Stefano ^d   Mann, Matthias ^a,c  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b UNIVERSITY OF PADOVA   (Italy)

^c University of Copenhagen   (Denmark)

^d VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

Author keywords

exercise; metabolism; mitochondria; muscle fibers; single cell

Indexed keywords

MITOCHONDRIAL PROTEIN; MYOSIN HEAVY CHAIN; PROTEOME; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; STRUCTURAL PROTEIN; TRANSCRIPTION FACTOR RELA;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CELL LEVEL; CELL SPECIFICITY; CITRIC ACID CYCLE; EXTENSOR DIGITORUM LONGUS MUSCLE; EXTRAOCULAR MUSCLE; GLYCOLYSIS; ISOELECTRIC FOCUSING; LIMB; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MITOCHONDRION; MOUSE; MUSCLE CELL; MUSCLE METABOLISM; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEOMICS; SLOW MUSCLE; SOLEUS MUSCLE; ANIMAL; BIOLOGY; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; PROCEDURES; SKELETAL MUSCLE;

MAMMALIA;

ANIMALS; CHROMATOGRAPHY, LIQUID; COMPUTATIONAL BIOLOGY; IMMUNOHISTOCHEMISTRY; MASS SPECTROMETRY; MICE; MITOCHONDRIA; MUSCLE FIBERS, SKELETAL; PROTEOME; PROTEOMICS;

EID: 84924052631     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201439757     Document Type: Article

References (44)

1. Richter EA, Ruderman NB, (2009) AMPK and the biochemistry of exercise: implications for human health and disease. Biochem J 418: 261-275
2. Boström P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo JC, Rasbach KA, Boström EA, Choi JH, Long JZ, et al, (2012) A PGC1-alpha-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481: 463-468
3. Ciciliot S, Rossi AC, Dyar KA, Blaauw B, Schiaffino S, (2013) Muscle type and fiber type specificity in muscle wasting. Int J Biochem Cell Biol 45: 2191-2199
4. Bassel-Duby R, Olson EN, (2006) Signaling pathways in skeletal muscle remodeling. Annu Rev Biochem 75: 19-37
5. Baldwin KM, Haddad F, Pandorf CE, Roy RR, Edgerton VR, (2013) Alterations in muscle mass and contractile phenotype in response to unloading models: role of transcriptional/pretranslational mechanisms. Front Physiol 4: 284
6. Egan B, Zierath JR, (2013) Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab 17: 162-184
7. Lowry CV, Kimmey JS, Felder S, Chi MM, Kaiser KK, Passonneau PN, Kirk KA, Lowry OH, (1978) Enzyme patterns in single human muscle fibers. J Biol Chem 253: 8269-8277
8. Luff AR, Atwood HL, (1972) Membrane properties and contraction of single muscle fibers in the mouse. Am J Physiol 222: 1435-1440
9. Pette D, Peuker H, Staron RS, (1999) The impact of biochemical methods for single muscle fibre analysis. Acta Physiol Scand 166: 261-277
10. Chemello F, Bean C, Cancellara P, Laveder P, Reggiani C, Lanfranchi G, (2011) Microgenomic analysis in skeletal muscle: expression signatures of individual fast and slow myofibers. PLoS ONE 6: e16807
11. Cox J, Mann M, (2011) Quantitative, high-resolution proteomics for data-driven systems biology. Annu Rev Biochem 80: 273-299
12. Altelaar AF, Heck AJ, (2012) Trends in ultrasensitive proteomics. Curr Opin Chem Biol 16: 206-213
13. Ohlendieck K, (2013) Proteomic identification of biomarkers of skeletal muscle disorders. Biomark Med 7: 169-186
14. Drexler HC, Ruhs A, Konzer A, Mendler L, Bruckskotten M, Looso M, Günther S, Boettger T, Krüger M, Braun T, (2012) On marathons and Sprints: an integrated quantitative proteomics and transcriptomics analysis of differences between slow and fast muscle fibers. Mol Cell Proteomics 11: M111.010801
15. Gelfi C, Vasso M, Cerretelli P, (2011) Diversity of human skeletal muscle in health and disease: contribution of proteomics. J Proteomics 74: 774-795
16. Wisniewski JR, Zougman A, Nagaraj N, Mann M, (2009) Universal sample preparation method for proteome analysis. Nat Methods 6: 359-362
17. Hubner NC, Ren S, Mann M, (2008) Peptide separation with immobilized pI strips is an attractive alternative to in-gel protein digestion for proteome analysis. Proteomics 8: 4862-4872
18. Michalski A, Damoc E, Hauschild JP, Lange O, Wieghaus A, Makarov A, Nagaraj N, Cox J, Mann M, Horning S, (2011) Mass spectrometry-based proteomics using Q Exactive, a high-performance benchtop quadrupole Orbitrap mass spectrometer. Mol Cell Proteomics 10: M111.011015
19. Kulak NA, Pichler G, Paron I, Nagaraj N, Mann M, (2014) Minimal, encapsulated proteomic-sample processing applied to copy-number estimation in eukaryotic cells. Nat Methods 11: 319-324
20. Cox J, Mann M, (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26: 1367-1372
21. Zeiler M, Straube WL, Lundberg E, Uhlen M, Mann M, (2012) A Protein Epitope Signature Tag (PrEST) library allows SILAC-based absolute quantification and multiplexed determination of protein copy numbers in cell lines. Mol Cell Proteomics 11: O111.009613
22. Park KA, Lim J, Sohn S, Oh SY, (2012) Myosin heavy chain isoform expression in human extraocular muscles: longitudinal variation and patterns of expression in global and orbital layers. Muscle Nerve 45: 713-720
23. Staron RS, Pette D, (1987) Nonuniform myosin expression along single fibers of chronically stimulated and contralateral rabbit tibialis anterior muscles. Pflugers Arch 409: 67-73
24. Edman KA, Reggiani C, te Kronnie G, (1985) Differences in maximum velocity of shortening along single muscle fibres of the frog. J Physiol 365: 147-163
25. Schaab C, Geiger T, Stoehr G, Cox J, Mann M, (2012) Analysis of high accuracy, quantitative proteomics data in the MaxQB database. Mol Cell Proteomics 11: M111.014068
26. Schiaffino S, Hanzlikova V, Pierobon S, (1970) Relations between structure and function in rat skeletal muscle fibers. J Cell Biol 47: 107-119
27. Nelson BR, Wu F, Liu Y, Anderson DM, McAnally J, Lin W, Cannon SC, Bassel-Duby R, Olson EN, (2013) Skeletal muscle-specific T-tubule protein STAC3 mediates voltage-induced Ca2 + release and contractility. Proc Natl Acad Sci USA 110: 11881-11886
28. Voeltz GK, Prinz WA, Shibata Y, Rist JM, Rapoport TA, (2006) A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124: 573-586
29. Chen S, Novick P, Ferro-Novick S, (2013) ER structure and function. Curr Opin Cell Biol 25: 428-433
30. Luff AR, Atwood HL, (1971) Changes in the sarcoplasmic reticulum and transverse tubular system of fast and slow skeletal muscles of the mouse during postnatal development. J Cell Biol 51: 369-383
31. Mootha VK, Bunkenborg J, Olsen JV, Hjerrild M, Wisniewski JR, Stahl E, Bolouri MS, Ray HN, Sihag S, Kamal M, et al, (2003) Integrated analysis of protein composition, tissue diversity, and gene regulation in mouse mitochondria. Cell 115: 629-640
32. Glancy B, Balaban RS, (2011) Protein composition and function of red and white skeletal muscle mitochondria. Am J Physiol Cell Physiol 300: C1280-C1290
33. Jackman MR, Willis WT, (1996) Characteristics of mitochondria isolated from type I and type IIb skeletal muscle. Am J Physiol 270: C673-C678
34. Arany Z, Lebrasseur N, Morris C, Smith E, Yang W, Ma Y, Chin S, Spiegelman BM, (2007) The transcriptional coactivator PGC-1beta drives the formation of oxidative type IIX fibers in skeletal muscle. Cell Metab 5: 35-46
35. Wise DR, Ward PS, Shay JE, Cross JR, Gruber JJ, Sachdeva UM, Platt JM, DeMatteo RG, Simon MC, Thompson CB, et al, (2011) Hypoxia promotes isocitrate dehydrogenase-dependent carboxylation of alpha-ketoglutarate to citrate to support cell growth and viability. Proc Natl Acad Sci USA 108: 19611-19616
36. Hartong DT, Dange M, McGee TL, Berson EL, Dryja TP, Colman RF, (2008) Insights from retinitis pigmentosa into the roles of isocitrate dehydrogenases in the Krebs cycle. Nat Genet 40: 1230-1234
37. Speijer D, (2014) How the mitochondrion was shaped by radical differences in substrates: what carnitine shuttles and uncoupling tell us about mitochondrial evolution in response to ROS. BioEssays 36: 634-643
38. Mracek T, Drahota Z, Houstek J, (2013) The function and the role of the mitochondrial glycerol-3-phosphate dehydrogenase in mammalian tissues. Biochim Biophys Acta 1827: 401-410
39. Bricker DK, Taylor EB, Schell JC, Orsak T, Boutron A, Chen YC, Cox JE, Cardon CM, Van Vranken JG, Dephoure N, et al, (2012) A mitochondrial pyruvate carrier required for pyruvate uptake in yeast, Drosophila, and humans. Science 337: 96-100
40. Herzig S, Raemy E, Montessuit S, Veuthey JL, Zamboni N, Westermann B, Kunji ER, Martinou JC, (2012) Identification and functional expression of the mitochondrial pyruvate carrier. Science 337: 93-96
41. Pette D, Staron RS, (1990) Cellular and molecular diversities of mammalian skeletal muscle fibers. Rev Physiol Biochem Pharmacol 116: 1-76
42. Scheltema RA, Mann M, (2012) SprayQc: a real-time LC-MS/MS quality monitoring system to maximize uptime using off the shelf components. J Proteome Res 11: 3458-3466
43. Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, Mann M, (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res 10: 1794-1805
44. Dyar KA, Ciciliot S, Wright LE, Biensø RS, Malagoli Tagliazucchi G, Patel VR, Forcato M, Peña Paz MI, Gudiksen A, Solagna F, et al, (2014) Muscle insulin sensitivity and glucose metabolism are controlled by the intrinsic muscle clock. Mol Metab 3: 29-41