Marine Biotechnology

, Volume 16, Issue 4, pp 423–435 | Cite as

Transcriptional Assessment by Microarray Analysis and Large-Scale Meta-analysis of the Metabolic Capacity of Cardiac and Skeletal Muscle Tissues to Cope With Reduced Nutrient Availability in Gilthead Sea Bream (Sparus aurata L.)

  • Josep A. Calduch-Giner
  • Yann Echasseriau
  • Diego Crespo
  • Daniel Baron
  • Josep V. Planas
  • Patrick Prunet
  • Jaume Pérez-Sánchez
Original Article

Abstract

The effects of nutrient availability on the transcriptome of cardiac and skeletal muscle tissues were assessed in juvenile gilthead sea bream fed with a standard diet at two feeding levels: (1) full ration size and (2) 70 % satiation followed by a finishing phase at the maintenance ration. Microarray analysis evidenced a characteristic transcriptomic profile for each muscle tissue following changes in oxidative capacity (heart > red skeletal muscle > white skeletal muscle). The transcriptome of heart and secondly that of red skeletal muscle were highly responsive to nutritional changes, whereas that of glycolytic white skeletal muscle showed less ability to respond. The highly expressed and nutritionally regulated genes of heart were mainly related to signal transduction and transcriptional regulation. In contrast, those of white muscle were enriched in gene ontology (GO) terms related to proteolysis and protein ubiquitination. Microarray meta-analysis using the bioinformatic tool Fish and Chips (http://fishandchips.genouest.org/index.php) showed the close association of a representative cluster of white skeletal muscle with some of cardiac and red skeletal muscle, and many GO terms related to mitochondrial function appeared to be common links between them. A second round of cluster comparisons revealed that mitochondria-related GOs also linked differentially expressed genes of heart with those of liver from cortisol-treated gilthead sea bream. These results show that mitochondria are among the first responders to environmental and nutritional stress stimuli in gilthead sea bream, and functional phenotyping of this cellular organelle is highly promising to obtain reliable markers of growth performance and well-being in this fish species.

Keywords

Feeding level Skeletal muscle Heart Microarray Meta-analysis Mitochondria 

Supplementary material

10126_2014_9562_MOESM1_ESM.docx (53 kb)
Supplemental Table A1Datasets included in the bioinformatic meta-analysis tool Fish and Chips. (DOCX 53 kb)
10126_2014_9562_MOESM2_ESM.docx (28 kb)
Supplemental Table A2Genes differentially expressed by restricted ration size in white skeletal muscle. Genes sharing the enriched GO terms “protein ubiquitination”, “proteolysis”, or “ubiquitin-dependent protein catabolic process” are highlighted in bold. (DOCX 28 kb)
10126_2014_9562_MOESM3_ESM.docx (20 kb)
Supplemental Table A3Genes differentially expressed by restricted ration size in red skeletal muscle. (DOCX 19 kb)
10126_2014_9562_MOESM4_ESM.docx (47 kb)
Supplemental Table A4Genes differentially expressed by restricted ration size in cardiac muscle. Genes sharing the enriched GO terms “regulation of transcription”, “signal transduction”, or “signaling pathway” are highlighted in bold. (DOCX 46 kb)
10126_2014_9562_MOESM5_ESM.docx (39 kb)
Supplemental Table A5Overlapping annotated genes between clusters in the first and second round of cluster comparison. (DOCX 38 kb)

References

  1. Agilent Technologies (2009) One-color microarray-based gene expression analysis (Quick Amp Labeling) with Tecan HS Pro Hybridization. Publication number G4140-90041. Available: http://www.chem.agilent.com/library/usermanuals/public/g4140-90041_one-color_tecan.pdf
  2. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25–29PubMedCentralCrossRefPubMedGoogle Scholar
  3. Baron D, Houlgatte R, Fostier A, Guiguen Y (2005) Large-scale temporal gene expression profiling during gonadal differentiation and early gametogenesis in rainbow trout. Biol Reprod 73:959–966CrossRefPubMedGoogle Scholar
  4. Baron D, Montfort J, Houlgatte R, Fostier A, Guiguen Y (2007a) Androgen-induced masculinization in rainbow trout results in a marked dysregulation of early gonadal gene expression profiles. BMC Genomics 8:357PubMedCentralCrossRefPubMedGoogle Scholar
  5. Baron D, Raharijaona M, Houlgatte R (2007b) DNA microarrays. IRBM 28:210–215CrossRefGoogle Scholar
  6. Baron D, Bihouée A, Teusan R, Dubois E, Savagner F, Steenman M, Houlgatte R, Ramstein G (2011a) MADGene: retrieval and processing of gene identifier lists for the analysis of heterogeneous microarray datasets. Bioinformatics 27(5):725–726PubMedCentralCrossRefPubMedGoogle Scholar
  7. Baron D, Dubois E, Bihouée A, Teusan R, Steenman M, Jourdon P, Magot A, Peréon Y, Veitia R, Savagner F, Ramstein G, Houlgatte R (2011b) Meta-analysis of muscle transcriptome data using the MADMuscle database reveals biologically relevant gene patterns. BMC Genomics 12:113PubMedCentralCrossRefPubMedGoogle Scholar
  8. Baron D, Magot A, Ramstein G, Steenman M, Fayet G, Chevalier C, Jourdon P, Houlgatte R, Savagner F, Pereon Y (2011c) Immune response and mitochondrial metabolism are commonly deregulated in DMD and aging skeletal muscle. PLoS One 6:e26952PubMedCentralCrossRefPubMedGoogle Scholar
  9. Bauer M, Hamm AC, Bonaus M, Jacob A, Jaekel J, Schorle H, Pankratz MJ, Katzenberger JD (2004) Starvation response in mouse liver shows strong correlation with life-span-prolonging processes. Physiol Genomics 17:230–244CrossRefPubMedGoogle Scholar
  10. Benedito-Palos L, Saera-Vila A, Calduch-Giner JA, Kaushik S, Pérez-Sánchez J (2007) Combined replacement of fish meal and oil in practical diets for fast growing juveniles of gilthead sea bream (Sparus aurata L.): networking of systemic and local components of GH/IGF axis. Aquaculture 267:199–212CrossRefGoogle Scholar
  11. Benedito-Palos L, Calduch-Giner JA, Ballester-Lozano GF, Pérez-Sánchez J (2013) Effect of ration size on fillet fatty acid composition, phospholipid allostasis and mRNA expression patterns of lipid regulatory genes in gilthead sea bream (Sparus aurata). British J Nutr 109:1175–1187CrossRefGoogle Scholar
  12. Bermejo-Nogales A, Benedito-Palos L, Calduch-Giner JA, Pérez-Sánchez J (2011) Feed restriction up-regulates uncoupling protein 3 (UCP3) gene expression in heart and red muscle tissues of gilthead sea bream (Sparus aurata L.). New insights in substrate oxidation and energy expenditure. Comp Biochem Physiol A 159:296–302CrossRefGoogle Scholar
  13. Briggs J, Paoloni M, Chen QR, Wen X, Khan J, Khanna C (2011) A compendium of canine normal tissue gene expression. PLoS One 6:e17107PubMedCentralCrossRefPubMedGoogle Scholar
  14. Calduch-Giner JA, Davey G, Saera-Vila A, Houeix B, Talbot A, Prunet P, Cairns MT, Pérez-Sánchez J (2010) Use of microarray technology to assess the time course of liver stress response after confinement exposure in gilthead sea bream (Sparus aurata L.). BMC Genomics 11:193PubMedCentralCrossRefPubMedGoogle Scholar
  15. Calduch-Giner JA, Sitjà-Bobadilla A, Davey GC, Cairns MT, Kaushik S, Pérez-Sánchez J (2012) Dietary vegetable oils do not alter the intestine transcriptome of gilthead sea bream (Sparus aurata), but modulate the transcriptomic response to infection with Enteromyxum leei. BMC Genomics 13:470PubMedCentralCrossRefPubMedGoogle Scholar
  16. Calduch-Giner JA, Bermejo-Nogales A, Benedito-Palos L, Estensoro I, Ballester-Lozano G, Sitjà-Bobadilla A, Pérez-Sánchez J (2013) Deep sequencing for de novo construction of a marine fish (Sparus aurata) transcriptome database with a large coverage of protein-coding transcripts. BMC Genomics 14:178PubMedCentralCrossRefPubMedGoogle Scholar
  17. Castro LFC, Wilson JM, Gonçalves O, Galante-Oliveira S, Rocha E, Cunha I (2011) The evolutionary history of the stearoyl-CoA desaturase gene family in vertebrates. BMC Evol Biol 11:132PubMedCentralCrossRefPubMedGoogle Scholar
  18. Civitarese AE, Carling S, Heilbronn LK, Hulver MH, Ukropcova B, Deutsch WA, Smith SR, Ravussin E (2007) Calorie restriction increases muscle mitochondrial biogenesis in healthy humans. PLoS Med 4:e76PubMedCentralCrossRefPubMedGoogle Scholar
  19. Cleveland BM, Weber GM, Blemings KP, Silverstein JT (2009) Insulin-like growth factor-I and genetic effects on indexes of protein degradation in response to feed deprivation in rainbow trout (Oncorhynchus mykiss). Am J Physiol Regul Integr Comp Physiol 297:R1332–R1342CrossRefPubMedGoogle Scholar
  20. Collins SA, Øverland M, Skrede A, Drew MD (2013) Effect of plant protein sources on growth rate in salmonids: meta-analysis of dietary inclusion of soybean, pea and canola/rapeseed meals and protein concentrates. Aquaculture 400–401:85–100CrossRefGoogle Scholar
  21. Conceição LEC, Aragão RN, Engrola S, Gavaia P, Mira S, Dias J (2010) Novel methodologies in marine fish larval nutrition. Fish Physiol Biochem 36:1–16CrossRefPubMedGoogle Scholar
  22. Conesa A, Götz S, García-Gómez JM, Perol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676CrossRefPubMedGoogle Scholar
  23. Davey GC, Calduch-Giner JA, Houeix B, Talbot A, Sitjà-Bobadilla A, Prunet P, Pérez-Sánchez J, Cairns MT (2011) Molecular profiling of the gilthead sea bream (Sparus aurata L.) response to chronic exposure to the myxosporean parasite Enteromyxum leei. Mol Immunol 48:2102–2112CrossRefPubMedGoogle Scholar
  24. Dejean S, Martin PG, Baccini A, Besse P (2007) Clustering time-series gene expression data using smoothing spline derivatives. EURASIP J Bioinform Syst Biol 70561Google Scholar
  25. Desert C, Duclos MJ, Blavy P, Lecerf F, Moreews F, Klopp C, Aubry M, Herault F, Le Roy P, Berri C, Douaire M, Diot C, Lagarrigue S (2008) Transcriptome profiling of the feeding-to-fasting transition in chicken liver. BMC Genomics 9:611PubMedCentralCrossRefPubMedGoogle Scholar
  26. Feichtinger J, McFarlane RJ, Larcombe LD (2012) CancerMA: a web-based tool for automatic meta-analysis of public cancer microarray data. Database bas055Google Scholar
  27. Fernandes JMO, Kinghorn JR, Johnston IA (2007) Differential expression of multiple alternatively spliced transcripts of MyoD. Gene 391:178–185CrossRefPubMedGoogle Scholar
  28. Ferraresso S, Vitulo N, Mininni AN, Romualdi C, Cardazzo B, Negrisolo E, Reinhardt R, Canario AVM, Patarnello T, Bargelloni L (2008) Development and validation of a gene expression oligo microarray for the gilthead sea bream (Sparus aurata). BMC Genomics 9:580PubMedCentralCrossRefPubMedGoogle Scholar
  29. Feuerstein P, Puard V, Chevalier C, Teusan R, Cadoret V, Guerif F, Houlgatte R, Royere D (2012) Genomic assessment of human cumulus cell marker genes as predictors of oocyte developmental competence: impact of various experimental factors. PLoS One 7:e40449PubMedCentralCrossRefPubMedGoogle Scholar
  30. Fraser KPP, Rogers AD (2007) Protein metabolism in marine animals: the underlying mechanism of growth. Adv Mar Biol 52:267–362Google Scholar
  31. Fuller SJ, Randel PJ (1984) Reversible phosphorylation of pyruvate dehydrogenase in rat skeletal-muscle mitochondria. Effects of starvation and diabetes. Biochem J 219:635–646PubMedCentralCrossRefPubMedGoogle Scholar
  32. Garcia de la Serrana D, Estévez A, Andree K, Johnston IA (2012) Fast skeletal muscle transcriptome of the gilthead sea bream (Sparus aurata) determined by next generation sequencing. BMC Genomics 13:181PubMedCentralCrossRefPubMedGoogle Scholar
  33. Gershman B, Puig O, Hang L, Peitzsch RM, Tatar M, Garofalo RS (2007) High resolution dynamics of the transcriptional response to nutrition in Drosophila: a key role for dFOXO. Physiol Genomics 29:24–34CrossRefPubMedGoogle Scholar
  34. Glass DJ (2005) Skeletal muscle hypertrophy and atrophy signalling pathways. Int J Bioch Cell Biol 37:1974–1984CrossRefGoogle Scholar
  35. Gómez-Requeni P, Calduch-Giner J, Vega-Rubín de Celis S, Medale F, Kaushik S, Pérez-Sánchez J (2005) Regulation of somatotropic axis by dietary factors in rainbow trout (Onchorhynchus mykiss). Br J Nutr 94:353–361CrossRefPubMedGoogle Scholar
  36. Haghikia A, Stapel B, Hoch M, Hilfiker-Kleiner D (2011) STAT3 and cardiac remodeling. Heart Fail Rev 16:35–47Google Scholar
  37. Higami Y, Pugh TD, Page GP, Allison DB, Prolla TA, Weindruch R (2004) Adipose tissue energy metabolism: altered gene expression profile of mice subjected to long-term caloric restriction. FASEB J 18:415–417PubMedGoogle Scholar
  38. Hinits Y, Osborn DP, Hughes SM (2009) Differential requirements for myogenic regulatory factors distinguish medial and lateral somitic, cranial and fin muscle fibre populations. Development 136:403–414PubMedCentralCrossRefPubMedGoogle Scholar
  39. Holt LJ, Siddle K (2005) Grb10 and Grb14: enigmatic regulators of insulin action—and more? Biochem J 388:393–406PubMedCentralCrossRefPubMedGoogle Scholar
  40. Hua K, Bureau DP (2012) Exploring the possibility of quantifying the effects of plant protein ingredients in fish feeds using meta-analysis and nutritional model simulation-based approaches. Aquaculture 356–357:284–301CrossRefGoogle Scholar
  41. Hulver MW, Berggren JR, Carper MJ, Miyazaki M, Ntambi JM, Hoffman EP, Thyfault JP, Stevens R, Dohm GL, Houmard JA, Muoio DM (2005) Elevated stearoyl-CoA desaturase-1 expression in skeletal muscle contributes to abnormal fatty acid partitioning in obese humans. Cell Metab 2:251–261PubMedCentralCrossRefPubMedGoogle Scholar
  42. Johnston I (2006) Environment and plasticity of myogenesis in teleost fish. J Exp Biol 209:2249–2264CrossRefPubMedGoogle Scholar
  43. Johnston IA, Bower NI, Macqueen DJ (2011) Growth and the regulation of myotomal muscle mass in teleost fish. J Exp Biol 214:1617–16228CrossRefPubMedGoogle Scholar
  44. Jung T, Catalgol B, Grune T (2009) The proteasomal system. Mol Aspects Med 30:191–296CrossRefPubMedGoogle Scholar
  45. Kang-Decker N, Cao S, Chatterjee S, Yao J, Egan LJ, Semela D, Mukhopadhyay D, Shah V (2007) Nitric oxide promotes endothelial cell survival signaling through S-nitrosylation and activation of dynamin-2. J Cell Sci 120:492–501CrossRefPubMedGoogle Scholar
  46. Kayo T, Allison DB, Weindruch R, Prolla TA (2001) Influences of aging and caloric restriction on the transcriptional profile of skeletal muscle from rhesus monkeys. Proc Natl Acad Sci U S A 98:5093–5098PubMedCentralCrossRefPubMedGoogle Scholar
  47. Kurokawa K, Akaike Y, Masuda K, Kuwano Y, Nishida K, Yamagishi N, Kajita K, Tanahashi T, Rokutan K (2013) Downregulation of serine/arginine-rich splicing factor 3 induces G1 cell cycle arrest and apoptosis in colon cancer cells. Oncogene. doi:10.1038/onc.2013.86 PubMedCentralGoogle Scholar
  48. Lamirault G, Meur NL, Roussel JC, Cunff MF, Baron D, Bihouée A, Guisle I, Raharijaona M, Ramstein G, Teusan R, Chevalier C, Gueffet JP, Trochu JN, Léger JJ, Houlgatte R, Steenman M (2010) Molecular risk stratification in advanced heart failure patients. J Cell Mol Med 14:1443–1452PubMedCentralCrossRefPubMedGoogle Scholar
  49. Lecker SH, Goldberg AL, Mitch WE (2006) Protein degradation by the ubiquitin–proteasome pathway in normal and disease states. J Am Soc Nephrol 17:1807–1819CrossRefPubMedGoogle Scholar
  50. Liesa M, Palacín M, Zorzano A (2009) Mitochondrial dynamics in mammalian health and disease. Physiol Rev 89:799–845CrossRefPubMedGoogle Scholar
  51. Lin RCY, Weeks KL, Gao X-M, Williams RBH, Bernardo BC, Kiriazis H, Matthews VB, Woodcock EA, Bouwman RD, Mollica JP, Speirs HJ, Dawes IW, Daly RJ, Shioi T, Izumo S, Febbraio MA, Du X-J, McMullen JR (2010) PI3K(p110α) protects against myocardial infarction-induced heart failure: identification of PI3K-regulated miRNA and mRNA. Arterioscler Thromb Vasc Biol 30:724–732CrossRefPubMedGoogle Scholar
  52. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔC T method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  53. Lkhagvadorj S, Qu L, Cai W, Couture OP, Barb CR, Hausman GJ, Nettleton D, Anderson LL, Dekkers JC, Tuggle CK (2010) Gene expression profiling of the short-term adaptive response to acute caloric restriction in liver and adipose tissues of pigs differing in feed efficiency. Am J Physiol Regul Integr Comp Physiol 298:R494–R507CrossRefPubMedGoogle Scholar
  54. Lukk M, Kapushesky M, Nikkilä J, Parkinson H, Goncalves A, Huber W, Ukkonen E, Brazma A (2010) A global map of human gene expression. Nat Biotechnol 28:322–324PubMedCentralCrossRefPubMedGoogle Scholar
  55. Martin B, Pearson M, Brenneman R, Golden E, Wood W, Prabhu V, Becker KG, Mattson MP, Maudsley S (2009) Gonadal transcriptome alterations in response to dietary energy intake: sensing the reproductive environment. PLoS ONE 4:e4146PubMedCentralCrossRefPubMedGoogle Scholar
  56. Mingarro M, Vega-Rubín de Celis S, Astola A, Pendón C, Valdivia MM, Pérez-Sánchez J (2002) Endocrine mediators of seasonal growth in gilthead sea bream: the growth hormone and somatolactin paradigm. Gen Comp Endocrinol 128:102–111CrossRefPubMedGoogle Scholar
  57. Moreau Y, Aerts S, De MB, Dabrowski M (2003) Comparison and meta-analysis of microarray data: from the bench to the computer desk. Trends Genet 19:570–577CrossRefPubMedGoogle Scholar
  58. Ntambi JM, Miyazaki M, Stoehr JP, Lan H, Kendziorski CM, Yandell BS, Song Y, Cohen P, Friedman JM, Attie AD (2002) Loss of stearoyl-CoA desaturase-1 function protects mice against adiposity. Proc Natl Acad Sci U S A 99:11482–11486PubMedCentralCrossRefPubMedGoogle Scholar
  59. Oksbjerg N, Gondret F, Vestergaard M (2004) Basic principles of muscle development and growth in meat-producing mammals as affected by the insulin-like growth factor (IGF) system. Domest Anim Endocrinol 27:219–240CrossRefPubMedGoogle Scholar
  60. Palstra AP, Beltran S, Burgerhout E, Brittijn SA, Magnoni LJ, Henkel CV, Jansen HJ, van den Thillart GEEJM, Spaink SP, Planas JV (2013) Deep RNA sequencing of the skeletal muscle transcriptome in swimming fish. PLoS ONE 8:e53171PubMedCentralCrossRefPubMedGoogle Scholar
  61. Pérez-Sánchez J, Calduch-Giner J, Mingarro M, Vega-Rubín de Celis S, Gómez-Requeni P, Saera-Vila A, Astola A, Valdivia MM (2002) Overview of fish growth hormone family. New insights in genomic organization and heterogeneity of fish growth hormone receptors. Fish Physiol Biochem 27:243–258CrossRefGoogle Scholar
  62. Pérez-Sánchez J, Borrel M, Bermejo-Nogales A, Benedito-Palos L, Saera-Vila A, Calduch-Giner JA, Kaushik S (2013) Dietary oils mediate cortisol kinetics and the hepatic mRNA expression profile of stress-responsive genes in gilthead sea bream (Sparus aurata) exposed to crowding stress. Implications on energy homeostasis and stress susceptibility. Comp Biochem Physiology D 8:123–130Google Scholar
  63. Prunet P, Øverli Ø, Douxfils J, Bernardini G, Kestemont P, Baron D (2012) Fish welfare and genomics. Fish Physiol Biochem 38:43–60CrossRefPubMedGoogle Scholar
  64. Quillé ML, Carat S, Quéméner-Redon S, Hirchaud E, Baron D, Benech C, Guihot J, Placet M, Mignen O, Férec C, Houlgatte R, Friocourt G (2011) High-throughput analysis of promoter occupancy reveals new targets for Arx, a gene mutated in mental retardation and interneuronopathies. PLoS One 6:e25181PubMedCentralCrossRefPubMedGoogle Scholar
  65. Rafael MS, Laizé V, Bensimon-Brito A, Leite RB, Schüle R, Cancela ML (2012) Four-and-a-half LIM domains protein 2 (FHL2) is associated with the development of craniofacial musculature in the teleost fish Sparus aurata. Cell Mol Life Sci 69:423–434CrossRefPubMedGoogle Scholar
  66. Rescan PY (2001) Regulation and functions of myogenic regulatory factors in lower vertebrates. Comp Biochem Physiol B 130:1–12CrossRefPubMedGoogle Scholar
  67. Saera-Vila A, Calduch-Giner JA, Pérez-Sánchez J (2007) Co-expression of IGFs and GH receptors (GHRs) in gilthead sea bream (Sparus aurata L.): sequence analysis of the GHR-flanking region. J Endocrinol 194:361–372CrossRefPubMedGoogle Scholar
  68. Saera-Vila A, Calduch-Giner JA, Prunet P, Pérez-Sánchez J (2009) Dynamics of liver GH/IGF axis and selected stress markers in juvenile gilthead sea bream (Sparus aurata) exposed to acute confinement. Differential stress response of growth hormone receptors. Comp Biochem Physiol A 154:197–203CrossRefGoogle Scholar
  69. Sales J (2011) First feeding of freshwater fish larvae with live feed versus compound diets: a meta-analysis. Aquacult Int 19:1217–1228CrossRefGoogle Scholar
  70. Sampath H, Ntambi JM (2011) The role of stearoyl-CoA desaturase in obesity, insulin resistance, and inflammation. Ann NY Acad Sci 1243:47–53CrossRefPubMedGoogle Scholar
  71. Sarropoulou E, Kotoulas G, Power DM, Geisler R (2005) Gene expression profiling of gilthead sea bream during early development and detection of stress-related genes by the application of cDNA microarray technology. Physiol Genomics 23:182–191CrossRefPubMedGoogle Scholar
  72. Schmidt D, Müller S (2003) PIAS/SUMO: new partners in transcriptional regulation. Cell Mol Life Sci 60:2561–2574CrossRefPubMedGoogle Scholar
  73. Singh AM, Li F-Q, Hamazaki T, Kasahara H, Takemaru K-H, Terada N (2007) Chibby, an antagonist of the Wnt/β-catenin pathway, facilitates cardiomyocyte differentiation of murine embryonic stem cells. Circulation 115:617–626PubMedCentralCrossRefPubMedGoogle Scholar
  74. Son CG, Bilke S, Davis S, Greer BT, Wei JS, Whiteford CC, Chen Q-R, Cenacchi N, Khan J (2005) Database of mRNA gene expression profiles of multiple human organs. Genome Res 15:443–450PubMedCentralCrossRefPubMedGoogle Scholar
  75. Spurney CF, Knoblach S, Pistilli EE, Nagaraju K, Martin GR, Hoffman EP (2008) Dystrophin-deficient cardiomyopathy in mouse: expression of Nox4 and Lox are associated with fibrosis and altered functional parameters in the heart. Neuromuscul Disord 18:371–381PubMedCentralCrossRefPubMedGoogle Scholar
  76. Sreekumar R, Unnikrishnan J, Fu A, Nygren J, Short KR, Schimke J, Barazzoni R, Nair KS (2002) Effects of caloric restriction on mitochondrial function and gene transcripts in rat muscle. Am J Physiol Endocrinol Metab 283:E38–E43CrossRefPubMedGoogle Scholar
  77. Sugden MC, Kraus A, Harris RA, Holness MJ (2000) Fibre-type specific modification of the activity and regulation of skeletal muscle pyruvate dehydrogenase kinase (PDK) by prolonged starvation and refeeding is associated with targeted regulation of PDK isoenzyme 4 expression. Biochem J 346:651–657PubMedCentralCrossRefPubMedGoogle Scholar
  78. Taegtmeyer H, Golfman L, Sharma S, Razeghi P, van Arsdall M (2004) Linking gene expression to function: metabolic flexibility in the normal and diseased heart. Ann N Y Acad Sci 1015:202–213CrossRefPubMedGoogle Scholar
  79. Teleman AA, Hietakangas V, Sayadian AC, Cohen SM (2008) Nutritional control of protein biosynthetic capacity by insulin via Myc in Drosophila. Cell Metab 7:21–32CrossRefPubMedGoogle Scholar
  80. Teles M, Boltaña S, Reyes-López F, Santos MA, Mackenzie S, Tort L (2013) Effects of chronic cortisol administration of GR and the liver transcriptome in Sparus aurata. Mar Biotechnol 15:104–114CrossRefPubMedGoogle Scholar
  81. Valente LMP, Moutou KA, Conceição LEC, Engrola S, Fernandes JMO, Johnston IA (2013) What determines growth potential and juvenile quality of farmed fish species? Reviews in Aquaculture 5:S168–S193CrossRefGoogle Scholar
  82. Vieira FA, Gregório SF, Ferraresso S, Thorne MAS, Costa R, Milan M, Bargelloni L, Clark MS, Canario AVM, Power DM (2011) Skin healing and scale regeneration in fed and unfed sea bream Sparus auratus. BMC Genomics 12:490PubMedCentralCrossRefPubMedGoogle Scholar
  83. Vieira FA, Thorne MAS, Stueber K, Darias M, Reinhardt R, Clark MS, Gisbert E, Power DM (2013) Comparative analysis of a teleost skeleton transcriptome provides insight into its regulation. Gen Comp Endocrinol 191:45–58CrossRefPubMedGoogle Scholar
  84. Workman C, Jensen LJ, Jarmer H, Berka R, Gautier L, Nielser HB, Saxild HH, Nielsen C, Brunak S, Knudsen S (2002) A new non-linear normalization method for reducing variability in DNA microarray experiments. Genome Biol 3:research0048Google Scholar
  85. Yúfera M, Halm S, Beltrán S, Fusté B, Planas JV, Martínez-Rodríguez G (2012) Transcriptomic characterization of the larval stage in gilthead sea bream (Sparus aurata) by 454 pyrosequencing. Mar Biotechnol 14:423–435CrossRefPubMedGoogle Scholar
  86. Zeeberg BR, Feng W, Wang G, Wang MD, Fojo AT, Sunshine M, Narasimhan S, Kane DW, Reinhold WC, Lababidi S, Bussey KJ, Riss J, Barrett JC, Weinstein JN (2003) GoMiner: a resource for biological interpretation of genomic and proteomic data. Genome Biol 4:R28PubMedCentralCrossRefPubMedGoogle Scholar
  87. Zheng-Bradley X, Rung J, Parkinson H, Brazma A (2010) Large scale comparison of global gene expression patterns in human and mouse. Genome Biol 11:R124PubMedCentralCrossRefPubMedGoogle Scholar
  88. Zinke I, Schutz CS, Katzenberger JD, Bauer M, Pankratz MJ (2002) Nutrient control of gene expression in Drosophila: microarray analysis of starvation and sugar dependent response. EMBO J 21:6162–6173PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Josep A. Calduch-Giner
    • 1
  • Yann Echasseriau
    • 2
  • Diego Crespo
    • 3
  • Daniel Baron
    • 4
  • Josep V. Planas
    • 3
  • Patrick Prunet
    • 2
  • Jaume Pérez-Sánchez
    • 1
  1. 1.Nutrigenomics and Fish Growth Endocrinology GroupInstituto de Acuicultura Torre de la Sal (IATS–CSIC)CastellónSpain
  2. 2.INRA, UR1037 LPGP Fish Physiology and GenomicsRennesFrance
  3. 3.Departament de Fisiologia i Immunologia, Facultat de BiologiaUniversitat de Barcelona and Institut de Biomedicina de la Universitat de Barcelona (IBUB)BarcelonaSpain
  4. 4.INSERM, UMR 1064NantesFrance

Personalised recommendations