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Functional Divergences of GAPDH Isoforms During Early Development in Two Perciform Fish Species

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Abstract

Glyceraldehyde-3-phospate dehydrogenase (GAPDH) is involved in basic cell catabolic processes and, as it is thought to be continuously expressed, belongs to the group of housekeeping genes. Thus, it is frequently used as an internal control in quantitative gene expression studies. However, the evidence of different expression patterns in a broad range of organisms and tissues, as well as the occurrence of different isoforms, shows that GAPDH has to be reevaluated as an internal control in qPCR studies, and its annotation has to be enriched. GAPDH has been shown to be involved in the pathway of energy and carbon molecule supply as well as in transcription and apoptosis. In the present study, we isolated the two isoforms, GAPDH-1 and GAPDH-2, of the gilthead sea bream (Sparus aurata) and the European sea bass (Dicentrarchus labrax). We inferred the phylogenetic relationships to ten other fish species and gave the gene structure of both genes. We further investigated gene expression analysis in both species for different developmental stages showing divergent gene expression of the two isoforms and the possible function of GAPDH-1 as a maternal gene.

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References

  • Brauhn J, Kincaid H (1982) Survival of growth and catchability of rainbow trout of four strains. N Am J Fish Manage 2:1–10

    Article  Google Scholar 

  • Carnevali O, Polzonetti V, Cardinali M, Pugnaloni A, Natalini P, Zmora N, Mosconi G, Polzonetti-Magni AM (2003) Apoptosis in sea bream Sparus aurata eggs. Mol Reprod Dev 66:291–296

    Article  PubMed  CAS  Google Scholar 

  • Casani D, Randelli E, Costantini S, Facchiano AM, Zou J, Martin S, Secombes CJ, Scapigliati G, Buonocore F (2009) Molecular characterisation and structural analysis of an interferon homologue in sea bass (Dicentrarchus labrax L.). Mol Immunol 46:943–952

    Article  PubMed  CAS  Google Scholar 

  • Cho YS, Lee SY, Kim KH, Nam YK (2008) Differential modulations of two glyceraldehyde 3-phosphate dehydrogenase mRNAs in response to bacterial and viral challenges in a marine teleost Oplegnathus fasciatus (Perciformes). Fish Shellfish Immunol 25:472–476

    Article  PubMed  CAS  Google Scholar 

  • Chuang D-M, Hough C, Senatorov VV (2005) Glyceraldeyde-3- dehydrogenase, apoptosis, and neurodegenerative diseases. Annu Rev Pharmacol Toxicol 45:269–290

    Article  PubMed  CAS  Google Scholar 

  • Darias MJ, Zambonino-Infante JL, Hugot K, Cahu CL, Mazurais D (2008) Gene expression patterns during the larval development of European sea bass (Dicentrarchus labrax) by microarray analysis. Mar Biotechnol (NY) 10:416–428

    Article  CAS  Google Scholar 

  • Divanach P (1985) Contribution á la connaissance de la biologie et de I'élevage de 6 Sparidis Mediterraneens: Sparus aurata, Diplodus sargus, Diplodus vuigaris, Diplodus annularis. Lithognathus mormyrus, Puntazzo puntazzo (Poissons Teleosteens). PhD, Universitite J des Sciences el Techniques du Languedoc. Montpellier, pp 479

  • Faliex E, Da Silva C, Simon G, Sasal P (2008) Dynamic expression of immune response genes in the sea bass, Dicentrarchus labrax, experimentally infected with the monogenean Diplectanum aequans. Fish Shellfish Immunol 24:759–767

    Article  PubMed  CAS  Google Scholar 

  • Franch R, Cardazzo B, Antonello J, Castagnaro M, Patarnello T, Bargelloni L (2006) Full-length sequence and expression analysis of toll-like receptor 9 in the gilthead seabream (Sparus aurata L.). Gene 378:42–51

    Article  PubMed  CAS  Google Scholar 

  • Fothergill-Gilmore LA, Michels PAM (1993) Evolution of glycolysis. Prog Biophys Mol Biol 59:105–235

    Article  PubMed  CAS  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Guindon S, Lethiec F, Duroux P, Gascuel O (2005) PHYML Online–a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33:W557–W559

    Article  PubMed  CAS  Google Scholar 

  • Hanauer A, Mandel JL (1984) The glyceraldehyde 3 phosphate dehydrogenase gene family: structure of a human cDNA and of an X chromosome linked pseudogene; amazing complexity of the gene family in mouse. EMBO J 3:2627–2633

    PubMed  CAS  Google Scholar 

  • Kapustin Y, Souvorov A, Tatusova T, Lipman D (2008) Splign: algorithms for computing spliced alignments with identification of paralogs. Biol Direct 3:20

    Article  PubMed  Google Scholar 

  • Kent WJ (2002) BLAT—the BLAST-like alignment tool. Genome Res 12:656–664

    PubMed  CAS  Google Scholar 

  • Manchado M, Infante C, Asensio E, Canavate JP (2007) Differential gene expression and dependence on thyroid hormones of two glyceraldehyde-3-phosphate dehydrogenases in the flatfish Senegalese sole (Solea senegalensis Kaup). Gene 400:1–8

    Article  PubMed  CAS  Google Scholar 

  • Mitter K, Kotoulas G, Magoulas A, Mulero V, Sepulcre P, Figueras A, Novoa B, Sarropoulou E (2009) Evaluation of candidate reference genes for QPCR during ontogenesis and of immune-relevant tissues of European sea bass (Dicentrarchus labrax). Comp Biochem Physiol B Biochem Mol Biol 153:340–347

    Article  PubMed  Google Scholar 

  • Mommens M, Fernandes JM, Bizuayehu TT, Bolla SL, Johnston IA, Babiak I (2010) Maternal gene expression in Atlantic halibut (Hippoglossus hippoglossus L.) and its relation to egg quality. BMC Res Notes 3:138

    Article  PubMed  Google Scholar 

  • Nylander JA, Ronquist F, Huelsenbeck JP, Nieves-Aldrey JL (2004) Bayesian phylogenetic analysis of combined data. Syst Biol 53:47–67

    Article  PubMed  Google Scholar 

  • Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36

    Article  PubMed  Google Scholar 

  • Piechaczyk M, Blanchard JM, Riaad-El Sabouty S, Dani C, Marty L, Jeanteur P (1984) Unusual abundance of vertebrate 3-phosphate dehydrogenase pseudogenes. Nature 312:469–471

    Article  PubMed  CAS  Google Scholar 

  • Reinitz G, Orme L, Hitzel F (1979) Variations in body composition and growth among strains of rainbow trout. Trans Am Fish Soc 108:204–207

    Article  Google Scholar 

  • 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 23:182–191

    Article  PubMed  CAS  Google Scholar 

  • Sarropoulou E, Sepulcre P, Poisa-Beiro L, Mulero V, Meseguer J, Figueras A, Novoa B, Terzoglou V, Reinhardt R, Magoulas A, Kotoulas G (2009) Profiling of infection specific mRNA transcripts of the European sea bass Dicentrarchus labrax. BMC Genomics 10:157

    Article  PubMed  Google Scholar 

  • Sepulcre MP, Sarropoulou E, Kotoulas G, Meseguer J, Mulero V (2007) Vibrio anguillarum evades the immune response of the bony fish sea bass (Dicentrarchus labrax L.) through the inhibition of leukocyte respiratory burst and down-regulation of apoptotic caspases. Mol Immunol 44:3751–3757

    Article  PubMed  CAS  Google Scholar 

  • Sirover MA (2005) New nuclear functions of the glycolytic protein, glyceraldehyde-3-phosphate dehydrogenase, in mammalian cells. J Cell Biochem 95:45–52

    Article  PubMed  CAS  Google Scholar 

  • Steinke D, Hoegg S, Brinkmann H, Meyer A (2006a) Three rounds (1R/2R/3R) of genome duplications and the evolution of the glycolytic pathway in vertebrates. BMC Biol 4:16

    Article  PubMed  Google Scholar 

  • Steinke D, Salzburger W, Meyer A (2006b) Novel relationships among ten fish model species revealed based on a phylogenomic analysis using ESTs. J Mol Evol 62:772–784

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F et al (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3(7):Research0034

    Article  PubMed  Google Scholar 

  • Vinas J, Piferrer F (2008) Stage-specific gene expression during fish spermatogenesis as determined by laser-capture microdissection and quantitative-PCR in sea bass (Dicentrarchus labrax) gonads. Biol Reprod 79:738–747

    Article  PubMed  CAS  Google Scholar 

  • Welch JE, Brown PL, O'brien DA, Magyar PL, Bunch DO, Mori C, Eddy EM (2000) Human glyceraldehyde 3-phosphate dehydrogenase-2 gene is expressed specifically in spermatogenic cells. J Androl 21:328–338

    PubMed  CAS  Google Scholar 

  • Wheelan SJ, Church DM, Ostell JM (2001) Spidey: a tool for mRNA-to-genomic alignments. Genome Res 11:1952–1957

    PubMed  CAS  Google Scholar 

  • Wilkes D, Xie SQ, Stickland NC, Alami-Durante H, Kentouri M, Sterioti A, Koumoundouros G, Fauconneau B, Goldspink G (2001) Temperature and myogenic factor transcript levels during early development determines muscle growth potential in rainbow trout (Oncorhynchus mykiss) and sea bass (Dicentrarchus labrax). J Exp Biol 204:2763–2771

    PubMed  CAS  Google Scholar 

  • Withler RE (1987) Genetic variation in survival of chinook salmon (Oncorhynchus tshawytscha) alevins exposed to an unidentified agent of mortality. Genome 29:839–845

    Article  PubMed  CAS  Google Scholar 

  • Zhao S, Fernald RD (2005) Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol 12:1047–1064

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

The authors would like to thank Dr. Richard Reinhard and Dr. Heiner Kuhl for access to the European Sea bass Genome Assemble database. The authors also thank Dr. Tsigenopoulos from the Institute of Marine Biology and Genetics, Dr. Constaninos Mylonas, Dr. Stavros Chatzifotiou, and Dr.Nikolas Papandroulaki from the Institute of Aquaculture for providing part of the European Sea bass larvae as well as the aquaculture facilities of Kastelorizo AE in Sitia, Crete for providing the possibility for egg and larvae sampling of gilthead sea bream.

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Correspondence to Elena Sarropoulou.

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Sarropoulou, E., Nousdili, D., Kotoulas, G. et al. Functional Divergences of GAPDH Isoforms During Early Development in Two Perciform Fish Species. Mar Biotechnol 13, 1115–1124 (2011). https://doi.org/10.1007/s10126-011-9375-6

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