期刊论文详细信息
BMC Genomics
The human cardiac and skeletal muscle proteomes defined by transcriptomics and antibody-based profiling
Mathias Uhlén4  Fredrik Pontén3  Erik Larsson2  Jens Nielsen5  Adil Mardinoglu5  Leif Väremo5  Peipei Ping4  David A Liem4  Howard Choi4  Caroline Kampf3  Mikael Huss6  Malene Lindholm7  Carl Johan Sundberg7  Björn M Hallström1  Linn Fagerberg1  Jerker Linné3  Cecilia Lindskog3 
[1] Science for Life Laboratory, KTH - Royal Institute of Technology, AlbaNova University Center, Stockholm, SE-171 21, Sweden;Department of Immunology, Genetics and Pathology, Rudbeck Laboratory, Uppsala University, Uppsala, SE-751 85, Sweden;Science for Life Laboratory, Dept of Immunology Genetics and Pathology, Uppsala University, Uppsala, SE-751 85, Sweden;NHLBI Proteomics Center at UCLA, Departments of Physiology and Medicine, Division of Cardiology, David Geffen School of Medicine, University of California, Los Angeles, CA, USA;Department of Chemical and Biological Engineering, Chalmers University of Technology, Gothenburg, SE-412 58, Sweden;Science for Life Laboratory, Dept of Biochemistry and Biophysics, Stockholm University, Solna, SE-17121, Sweden;Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, SE-171 77, Sweden
关键词: Cardiac and skeletal muscle;    Proteome;    Transcriptome;   
Others  :  1219272
DOI  :  10.1186/s12864-015-1686-y
 received in 2014-08-18, accepted in 2015-06-05,  发布年份 2015
PDF
【 摘 要 】

Background

To understand cardiac and skeletal muscle function, it is important to define and explore their molecular constituents and also to identify similarities and differences in the gene expression in these two different striated muscle tissues. Here, we have investigated the genes and proteins with elevated expression in cardiac and skeletal muscle in relation to all other major human tissues and organs using a global transcriptomics analysis complemented with antibody-based profiling to localize the corresponding proteins on a single cell level.

Results

Our study identified a comprehensive list of genes expressed in cardiac and skeletal muscle. The genes with elevated expression were further stratified according to their global expression pattern across the human body as well as their precise localization in the muscle tissues. The functions of the proteins encoded by the elevated genes are well in line with the physiological functions of cardiac and skeletal muscle, such as contraction, ion transport, regulation of membrane potential and actomyosin structure organization. A large fraction of the transcripts in both cardiac and skeletal muscle correspond to mitochondrial proteins involved in energy metabolism, which demonstrates the extreme specialization of these muscle tissues to provide energy for contraction.

Conclusions

Our results provide a comprehensive list of genes and proteins elevated in striated muscles. A number of proteins not previously characterized in cardiac and skeletal muscle were identified and localized to specific cellular subcompartments. These proteins represent an interesting starting point for further functional analysis of their role in muscle biology and disease.

【 授权许可】

   
2015 Lindskog et al.

【 预 览 】
附件列表
Files Size Format View
20150715163710301.pdf 2314KB PDF download
Fig. 6. 245KB Image download
Fig. 5. 125KB Image download
Fig. 4. 205KB Image download
Fig. 3. 120KB Image download
Fig. 2. 59KB Image download
Fig. 1. 121KB Image download
【 图 表 】

Fig. 1.

Fig. 2.

Fig. 3.

Fig. 4.

Fig. 5.

Fig. 6.

【 参考文献 】
  • [1]Ounzain S, Micheletti R, Beckmann T, Schroen B, Alexanian M, Pezzuto I, Crippa S, Nemir M, Sarre A, Johnson R, et al.. Genome-wide profiling of the cardiac transcriptome after myocardial infarction identifies novel heart-specific long non-coding RNAs. Eur Heart J. 2015;36:353-68a.
  • [2]Barth AS, Chakir K, Kass DA, Tomaselli GF. Transcriptome, proteome, and metabolome in dyssynchronous heart failure and CRT. J Cardiovasc Transl Res. 2012; 5:180-7.
  • [3]Thygesen K, Alpert JS, Jaffe AS, Simoons ML, Chaitman BR, White HD. Third universal definition of myocardial infarction. Nat Rev Cardiol. 2012; 9:620-33.
  • [4]Fagerberg L, Hallstrom BM, Oksvold P, Kampf C, Djureinovic D, Odeberg J, Habuka M, Tahmasebpoor S, Danielsson A, Edlund K et al.. Analysis of the human tissue-specific expression by genome-wide integration of transcriptomics and antibody-based proteomics. Mol Cell Proteomics. 2014; 13:397-406.
  • [5]Hebenstreit D, Fang M, Gu M, Charoensawan V, van Oudenaarden A, Teichmann SA. RNA sequencing reveals two major classes of gene expression levels in metazoan cells. Mol Syst Biol. 2011; 7:497.
  • [6]Zong NC, Li H, Li H, Lam MP, Jimenez RC, Kim CS, Deng N, Kim AK, Choi JH, Zelaya I et al.. Integration of cardiac proteome biology and medicine by a specialized knowledgebase. Circ Res. 2013; 113:1043-53.
  • [7]Gunning P, O’Neill G, Hardeman E. Tropomyosin-based regulation of the actin cytoskeleton in time and space. Physiol Rev. 2008; 88:1-35.
  • [8]Roberts JD, Davies RW, Lubitz SA, Thibodeau IL, Nery PB, Birnie DH, Benjamin EJ, Lemery R, Ellinor PT, Gollob MH. Evaluation of non-synonymous NPPA single nucleotide polymorphisms in atrial fibrillation. Europace. 2010; 12:1078-83.
  • [9]Laflamme MA, Murry CE. Heart regeneration. Nature. 2011; 473:326-35.
  • [10]Berry SE, Andruszkiewicz P, Chun JL, Hong J. Nestin expression in end-stage disease in dystrophin-deficient heart: implications for regeneration from endogenous cardiac stem cells. Stem Cells Transl Med. 2013; 2:848-61.
  • [11]El-Helou V, Chabot A, Gosselin H, Villeneuve L, Clavet-Lanthier ME, Tanguay JF, Enikolopov G, Fernandes KJ, Jasmin JF, Calderone A. Cardiac resident nestin(+) cells participate in reparative vascularisation. J Cell Physiol. 2013; 228:1844-53.
  • [12]Vasavada TK, DiAngelo JR, Duncan MK. Developmental expression of Pop1/Bves. J Histochem Cytochem. 2004; 52:371-7.
  • [13]Friedrich M, Grahnert A, Paasch U, Tannapfel A, Koch-Nolte F, Hauschildt S. Expression of toxin-related human mono-ADP-ribosyltransferase 3 in human testes. Asian J Androl. 2006; 8:281-7.
  • [14]Nagano T, Yoneda T, Hatanaka Y, Kubota C, Murakami F, Sato M. Filamin A-interacting protein (FILIP) regulates cortical cell migration out of the ventricular zone. Nat Cell Biol. 2002; 4:495-501.
  • [15]Froese A, Breher SS, Waldeyer C, Schindler RF, Nikolaev VO, Rinne S, Wischmeyer E, Schlueter J, Becher J, Simrick S et al.. Popeye domain containing proteins are essential for stress-mediated modulation of cardiac pacemaking in mice. J Clin Invest. 2012; 122:1119-30.
  • [16]Larsson L, Moss RL. Maximum velocity of shortening in relation to myosin isoform composition in single fibres from human skeletal muscles. J Physiol. 1993; 472:595-614.
  • [17]Barton PJ, Cullen ME, Townsend PJ, Brand NJ, Mullen AJ, Norman DA, Bhavsar PK, Yacoub MH. Close physical linkage of human troponin genes: organization, sequence, and expression of the locus encoding cardiac troponin I and slow skeletal troponin T. Genomics. 1999; 57:102-9.
  • [18]Richard I, Broux O, Allamand V, Fougerousse F, Chiannilkulchai N, Bourg N, Brenguier L, Devaud C, Pasturaud P, Roudaut C et al.. Mutations in the proteolytic enzyme calpain 3 cause limb-girdle muscular dystrophy type 2A. Cell. 1995; 81:27-40.
  • [19]Mardinoglu A, Agren R, Kampf C, Asplund A, Nookaew I, Jacobson P, Walley AJ, Froguel P, Carlsson LM, Uhlen M, Nielsen J. Integration of clinical data with a genome-scale metabolic model of the human adipocyte. Mol Syst Biol. 2013; 9:649.
  • [20]Mardinoglu A, Agren R, Kampf C, Asplund A, Uhlen M, Nielsen J. Genome-scale metabolic modelling of hepatocytes reveals serine deficiency in patients with non-alcoholic fatty liver disease. Nat Commun. 2014; 5:3083.
  • [21]Comi GP, Fortunato F, Lucchiari S, Bordoni A, Prelle A, Jann S, Keller A, Ciscato P, Galbiati S, Chiveri L et al.. Beta-enolase deficiency, a new metabolic myopathy of distal glycolysis. Ann Neurol. 2001; 50:202-7.
  • [22]Keller A, Demeurie J, Merkulova T, Geraud G, Cywiner-Golenzer C, Lucas M, Chatelet FP. Fibre-type distribution and subcellular localisation of alpha and beta enolase in mouse striated muscle. Biol Cell. 2000; 92:527-35.
  • [23]Ravenscroft G, Miyatake S, Lehtokari VL, Todd EJ, Vornanen P, Yau KS, Hayashi YK, Miyake N, Tsurusaki Y, Doi H et al.. Mutations in KLHL40 are a frequent cause of severe autosomal-recessive nemaline myopathy. Am J Hum Genet. 2013; 93:6-18.
  • [24]Exton JH. Mechanisms of hormonal regulation of hepatic glucose metabolism. Diabetes Metab Rev. 1987; 3:163-83.
  • [25]Martinez-Pena y Valenzuela I, Mouslim C, Akaaboune M. Calcium/calmodulin kinase II-dependent acetylcholine receptor cycling at the mammalian neuromuscular junction in vivo. J Neurosci. 2010; 30:12455-65.
  • [26]Gyorke S, Gyorke I, Terentyev D, Viatchenko-Karpinski S, Williams SC. Modulation of sarcoplasmic reticulum calcium release by calsequestrin in cardiac myocytes. Biol Res. 2004; 37:603-7.
  • [27]Gregory KN, Ginsburg KS, Bodi I, Hahn H, Marreez YM, Song Q, Padmanabhan PA, Mitton BA, Waggoner JR, Del Monte F et al.. Histidine-rich Ca binding protein: a regulator of sarcoplasmic reticulum calcium sequestration and cardiac function. J Mol Cell Cardiol. 2006; 40:653-65.
  • [28]Morelli RL, Carlson CJ, Emilson B, Abendschein DR, Rapaport E. Serum creatine kinase MM isoenzyme sub-bands after acute myocardial infarction in man. Circulation. 1983; 67:1283-9.
  • [29]Burwinkel B, Bakker HD, Herschkovitz E, Moses SW, Shin YS, Kilimann MW. Mutations in the liver glycogen phosphorylase gene (PYGL) underlying glycogenosis type VI. Am J Hum Genet. 1998; 62:785-91.
  • [30]Selcen D, Engel AG. Mutations in ZASP define a novel form of muscular dystrophy in humans. Ann Neurol. 2005; 57:269-76.
  • [31]Ogata T, Ueyama T, Isodono K, Tagawa M, Takehara N, Kawashima T, Harada K, Takahashi T, Shioi T, Matsubara H, Oh H. MURC, a muscle-restricted coiled-coil protein that modulates the Rho/ROCK pathway, induces cardiac dysfunction and conduction disturbance. Mol Cell Biol. 2008; 28:3424-36.
  • [32]Soejima H, Kawamoto S, Akai J, Miyoshi O, Arai Y, Morohka T, Matsuo S, Niikawa N, Kimura A, Okubo K, Mukai T. Isolation of novel heart-specific genes using the BodyMap database. Genomics. 2001; 74:115-20.
  • [33]Cho Y, Hazen BC, Russell AP, Kralli A. Peroxisome proliferator-activated receptor gamma coactivator 1 (PGC-1)- and estrogen-related receptor (ERR)-induced regulator in muscle 1 (Perm1) is a tissue-specific regulator of oxidative capacity in skeletal muscle cells. J Biol Chem. 2013; 288:25207-18.
  • [34]Fowler VM. The human erythrocyte plasma membrane: a Rosetta Stone for decoding membrane-cytoskeleton structure. Curr Top Membr. 2013; 72:39-88.
  • [35]Uhlen M, Oksvold P, Fagerberg L, Lundberg E, Jonasson K, Forsberg M, Zwahlen M, Kampf C, Wester K, Hober S et al.. Towards a knowledge-based human protein atlas. Nat Biotechnol. 2010; 28:1248-50.
  • [36]Uhlen M, Bjorling E, Agaton C, Szigyarto CA, Amini B, Andersen E, Andersson AC, Angelidou P, Asplund A, Asplund C et al.. A human protein atlas for normal and cancer tissues based on antibody proteomics. Mol Cell Proteomics. 2005; 4:1920-32.
  • [37]Savarese G, Trimarco B, Dellegrottaglie S, Prastaro M, Gambardella F, Rengo G, Leosco D, Perrone-Filardi P. Natriuretic peptide-guided therapy in chronic heart failure: a meta-analysis of 2,686 patients in 12 randomized trials. PLoS One. 2013; 8: Article ID e58287
  • [38]Ellis SG, Chew D, Chan A, Whitlow PL, Schneider JP, Topol EJ. Death following creatine kinase-MB elevation after coronary intervention: identification of an early risk period: importance of creatine kinase-MB level, completeness of revascularization, ventricular function, and probable benefit of statin therapy. Circulation. 2002; 106:1205-10.
  • [39]Lindholm ME, Huss M, Solnestam BW, Kjellqvist S, Lundeberg J, Sundberg CJ. The human skeletal muscle transcriptome: sex differences, alternative splicing, and tissue homogeneity assessed with RNA sequencing. FASEB J. 2014;28:4571-81.
  • [40]Guda P, Subramaniam S, Guda C. Mitoproteome: human heart mitochondrial protein sequence database. Methods Mol Biol. 2007; 357:375-83.
  • [41]Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT et al.. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000; 25:25-9.
  • [42]Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics. 2009; 10:48. BioMed Central Full Text
  • [43]Kampf C, Olsson I, Ryberg U, Sjostedt E, Ponten F. Production of tissue microarrays, immunohistochemistry staining and digitalization within the human protein atlas. J Vis Exp. 2012;63. http://www. ncbi.nlm.nih.gov/pubmed/22688270 webcite
  文献评价指标  
  下载次数:50次 浏览次数:4次