Skip to main content

Advertisement

SpringerLink
Log in

A reference growth curve for nutritional experiments in zebrafish (Danio rerio) and changes in whole body proteome during development

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Zebrafish is one of the most used vertebrate model organisms in molecular and developmental biology, recently gaining popularity also in medical research. However, very little work has been done to assess zebrafish as a model species in nutritional studies in aquaculture in order to utilize the methodological toolbox that this species represents. As a starting point to acquire some baseline data for further nutritional studies, growth of a population of zebrafish was followed for 15 weeks. Furthermore, whole body proteome was screened during development by means of bi-dimensional gel electrophoresis and mass spectrometry. Fish were reared under best practice laboratory conditions from hatching until 103 days post-fertilization (dpf) and regularly fed ad libitum with Artemia nauplii from 12 dpf. A growth burst occurred within 9–51 dpf, reaching a plateau after 65 dpf. Fork length and body weight were significantly lower in males than in females from 58 dpf onwards. Proteomics analysis showed 28 spot proteins differently expressed through development and according to sex. Of these proteins, 20 were successfully identified revealing proteins involved in energy production, muscle development, eye lens differentiation, and sexual maturation. In summary, zebrafish exhibited a rapid growth until approximately 50 dpf, when most individuals started to allocate part of the dietary energy intake for sexual maturation. However, proteomic analysis revealed that some individuals reached sexual maturity earlier and already from 30 dpf onwards. Thus, in order to design nutritional studies with zebrafish fed Artemia nauplii, it is recommended to select a period between 20 and 40 dpf, when fish allocate most of the ingested energy for non-reproductive growth purposes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abnous K, Storey KB (2007) Regulation of skeletal muscle creatine kinase from a hibernating mammal. Arch Biochem Biophys 467:10–19

    Article  CAS  PubMed  Google Scholar 

  • Almansa E, Martian MV, Cejas JR, Badi P, Jerez S, Lorenzo A (2001) Lipid and fatty acid composition of female gilthead seabream during their reproductive cycle: effects of a diet lacking n-3 HUFA. J Fish Biol 59:267–286

    Article  CAS  Google Scholar 

  • Aragão C, Conceição LEC, Fyhn HJ, Dinis MT (2004) Estimated amino acid requirements during early ontogeny in fish with different life styles: gilthead seabream (Sparus aurata) and Senegalese sole (Solea senegalensis). Aquaculture 242:589–605

    Article  Google Scholar 

  • Assinder SJ, Stanton J-AL, Prasad PD (2009) Transgelin: an actin-binding protein and tumour suppressor. Int J Biochem Cell Biol 41:482–486

    Article  CAS  PubMed  Google Scholar 

  • Axelrod HR, Emmens CW, Burgess WE, Pronek N (1986) Exotic tropical fish. TFH Publications, Neptune City

    Google Scholar 

  • Biga PR, Goetz FW (2006) Zebrafish and giant danio as models for muscle growth: determinate vs. indeterminate growth as determined by morphometric analysis. Am J Physiol Regul Integr Comp Physiol 291:R1327–R1337

    CAS  PubMed  Google Scholar 

  • Billingsley G, Santhiya ST, Paterson AD, Ogata K, Wodak S, Hosseini SM, Manisastry SM, Vijayalakshmi P, Gopinath PM, Graw J, Héon E (2006) CRYBA4, a novel human cataract gene, is also involved in microphthalmia. Am J Hum Genet 79:702–709

    Article  CAS  PubMed  Google Scholar 

  • Bohne-Kjersem A, Skadsheim A, Goksøyr A, Grøsvik BE (2009) Candidate biomarker discovery in plasma of juvenile cod (Gadus morhua) exposed to crude North Sea oil, alkyl phenols and polycyclic aromatic hydrocarbons (PAHs). Mar Environ Res 68:268–277

    Article  CAS  PubMed  Google Scholar 

  • Bosworth CA, Chou CW, Cole RB, Rees BB (2005) Protein expression patterns in zebrafish skeletal muscle: initial characterization and the effects of hypoxic exposure. Proteomics 5:1362–1371

    Article  CAS  PubMed  Google Scholar 

  • Byrne BM, Gruber M, Gruber AB (1989) The evolution of yolk proteins. Prog Biophys Mol Biol 53:33–69

    Article  CAS  PubMed  Google Scholar 

  • Carvalho AP, Araújo L, Santos MM (2006) Rearing zebrafish (Danio rerio) larvae without live food: evaluation of a commercial, a practical and a purified starter diet on larval performance. Aquacult Res 37:1107–1111

    Article  CAS  Google Scholar 

  • Chen Z, Huang W, Dahme T, Rottbauer W, Ackerman MJ, Xu X (2008) Depletion of zebrafish essential and regulatory myosin light chains reduces cardiac function through distinct mechanisms. Cardiovasc Res 79:97–108

    Article  CAS  PubMed  Google Scholar 

  • Clemmesen C (1994) The effect of food availability, age or size on the RNA/DNA ratio of individually measured herring larvae: laboratory calibration. Mar Biol 118:377–382

    Article  Google Scholar 

  • Cohen SA, Michaud DP (1993) Synthesis of a fluorescent derivatizing reagent, 6-aminoquinolyl-N-hydroxysate amino acids via high-performance liquid chromatography. Anal Biochem 211:279–287

    Article  CAS  PubMed  Google Scholar 

  • Dahm R, Geisler R (2006) Learning from small fry: the zebrafish as a genetic model organism for aquaculture fish species. Mar Biotechnol 8:329–345

    Article  CAS  PubMed  Google Scholar 

  • Easter SS Jr, Nicola GN (1996) The development of vision in the zebrafish (Danio rerio). Dev Biol 180:646–663

    Article  CAS  PubMed  Google Scholar 

  • Eaton RC, Farley RD (1974) Growth and the reduction of depensation of zebrafish, Brachydanio rerio, reared in the laboratory. Copeia 1974:204–209

    Article  Google Scholar 

  • Fishman MC (2001) Zebrafish—the canonical vertebrate. Science 294:1290–1291

    Article  CAS  PubMed  Google Scholar 

  • Goishi K, Shimizu A, Najarro G, Watanabe S, Rogers R, Zon LI, Klagsbrun M (2006) αA-crystallin expression prevents gamma-crystallin insolubility and cataract formation in the zebrafish cloche mutant lens. Development 133:2585–2593

    Article  CAS  PubMed  Google Scholar 

  • Goolish EM, Okutake K, Lesure S (1999) Growth and survivorship of larval zebrafish Danio rerio on processed diets. N Am J Aquacult 61:189–198

    Article  Google Scholar 

  • Görg A, Boguth G, Obermaier C, Weiss W (1998) Two-dimensional electrophoresis of proteins in an immobilized pH 4–12 gradient. Electrophoresis 19:1516–1519

    Article  PubMed  Google Scholar 

  • Görg A, Obermaier C, Boguth G, Harder A, Scheibe B, Wildgruber R, Weiss W (2000) The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 21:1037–1053

    Article  PubMed  Google Scholar 

  • Graw J (1997) The crystallins: genes, proteins and diseases. Biol Chem 378:1331–1348

    CAS  PubMed  Google Scholar 

  • Gygi SP, Rochon Y, Franza BR, Aebersold R (1999) Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19:1720–1730

    CAS  PubMed  Google Scholar 

  • Hack CJ (2004) Integrated transcriptome and proteome data: the challenges ahead. Brief Funct Genomic Proteomic 3:212–219

    Article  CAS  PubMed  Google Scholar 

  • Hu S, Wang J, Meijer J, Ieong S, Xie Y, Yu T, Zhou H, Henry S, Vissink A, Pijpe J, Kallenberg C, Elashoff D, Loo JA, Wong DT (2007) Salivary proteomic and genomic biomarkers for primary Sjögren’s syndrome. Arthritis Rheum 56:3588–3600

    Article  CAS  PubMed  Google Scholar 

  • Jaya-Ram A, Kuah M-K, Lim P-S, Kolkovski S, Shu-Chien AC (2008) Influence of dietary HUFA levels on reproductive performance, tissue fatty acid profile and desaturase and elongase mRNAs expression in female zebrafish Danio rerio. Aquaculture 277:275–281

    Article  CAS  Google Scholar 

  • Jerez S, Rodriguez C, Cejas JR, Bolanos A, Lorenzo A (2006) Lipid dynamics and plasma level changes of 17 β-estradiol and testosterone during the spawning season of gilthead seabream (Sparus aurata) females of different ages. Comp Biochem Physiol 143B:180–189

    CAS  Google Scholar 

  • Jury DR, Kaveti S, Duan Z-H, Willard B, Kinter M, Londraville R (2008) Effects of calorie restriction on the zebrafish liver proteome. Comp Biochem Physiol 3D:275–282

    CAS  Google Scholar 

  • Lahm H-W, Langen H (2000) Mass spectometry: a tool for the identification of proteins separated by gels. Electrophoresis 21:2105–2114

    Article  CAS  PubMed  Google Scholar 

  • Lampi KJ, Ma Z, Shih M, Shearer TR, Smith JB, Smith DL, David LL (1997) Sequence analysis of bA3, bB3, and bA4 crystallins completes the identification of the major proteins in young human lens. J Biol Chem 272:2268–2275

    Article  CAS  PubMed  Google Scholar 

  • Lawrence C, Ebersole JP, Kesseli RV (2008) Rapid growth and out-crossing promote female development in zebrafish (Danio rerio). Environ Biol Fish 81:239–246

    Article  Google Scholar 

  • Lawson D, Harris M, Shapland C (1997) Fibroblast transgelin and smooth muscle SM22α are the same protein, the expression of which is down regulated in many cell lines. Cell Motil Cytoskeleton 38:250–257

    Article  CAS  PubMed  Google Scholar 

  • Lemeer SM, Ruijtenbeek R, Pinkse MW, Jopling C, Heck AJ, den Hertog J, Slijper M (2007) Endogenous phosphotyrosine signaling in zebrafish embryos. Mol Cell Proteomics 6:2088–2099

    Article  CAS  PubMed  Google Scholar 

  • Lemeer A, Pinkse MWH, Mohammed S, van Breukelen B, den Hertog J, Slijper M, Heck AJR (2008) Online automated in vivo zebrafish phosphoproteomics: from large-scale analysis down to a single embryo. J Proteome Res 7:1555–1564

    Article  CAS  PubMed  Google Scholar 

  • Li L, Joseph MM, Peter C, Eric NO (1996) SM22α, a marker of adult smooth muscle, is expressed in multiple myogenic lineages during embryogenesis. Circ Res 78:188–195

    CAS  PubMed  Google Scholar 

  • Link V, Carvalho L, Castanon I, Stockinger P, Shevchenko A, Heisenberg CP (2006a) Identification of regulators of germ layer morphogenesis using proteomics in zebrafish. J Cell Sci 119:2073–2083

    Article  CAS  PubMed  Google Scholar 

  • Link V, Shevchenko A, Heisenberg CP (2006b) Proteomics of early zebrafish embryos. BMC Dev Biol 6:1–9

    Article  PubMed  Google Scholar 

  • Littlechild JA, Watson HO (1993) A data-based reaction mechanism for type I fructose bisphosphate aldolase. Trends Biochem Sci 18:36–39

    Article  CAS  PubMed  Google Scholar 

  • Love DR, Pichler FB, Dodd A, Copp BR, Greenwood DR (2004) Technology for high-throughput screens: the present and future using zebra fish. Curr Opin Biotechnol 15:564–571

    Article  CAS  PubMed  Google Scholar 

  • Lucitt MB, Price TS, Pizarro A, Wu W, Yocum AK, Seiler C, Pack MA, Blair IA, Fitzgerald GA, Grosser T (2008) Analysis of the zebrafish proteome during embryonic development. Mol Cell Proteomics 7:981–994

    Article  CAS  PubMed  Google Scholar 

  • Markovich M, Brown P (2005) Determination of the proper feeding density of rotifers Brachionus plicatilis for larval zebrafish Danio rerio. Meeting Abstracts of Aquaculture America 2005, 235, New Orleans, LA, USA

  • Martin SAM (2009) Proteomics in aquaculture. In: Overturf K (ed) Molecular research in aquaculture. Wiley. (ISBN-13:978-0-8138-1851-1/2009)

  • Martin SAM, Cash P, Blaney S, Houlihan DF (2001) Proteome analysis of rainbow trout (Oncorhynchus mykiss) liver proteins during short term starvation. Fish Physiol Biochem 24:259–270

    Article  CAS  Google Scholar 

  • Martin SAM, Vilhelmsson O, Médale F, Watt P, Kaushik S, Houlihan DF (2003) Proteomic sensitivity to dietary manipulations in rainbow trout. Biochim Biophys Acta 1651:17–29

    CAS  PubMed  Google Scholar 

  • McCool S, Pierotti AR (2000) Expression of the thimet oligopeptidase gene is regulated by positively and negatively acting elements. DNA Cell Biol 19:729–738

    Article  CAS  PubMed  Google Scholar 

  • Meinelt T, Schulz C, Wirth M, Kürzinger H, Steinberg C (2000) Correlation of diets high in n-6 polyunsaturated fatty acids with high growth rate in zebrafish (Danio rerio). Comp Med 50:43–45

    CAS  PubMed  Google Scholar 

  • Mendelsohn BA, Malone JP, Townsend RR, Gitlin JD (2009) Proteomic analysis of anoxia tolerance in the developing zebrafish embryo. Comp Biochem Physiol 4D:21–31

    CAS  Google Scholar 

  • Muncan V, Faro A, Haramis A-PG, Hurlstone AFL, Wienholds E, Van Es J, Korving J, Begthel H, Zivkovic D, Clevers H (2007) T-cell factor 4 (Tcf7l2) maintains proliferative compartments in zebrafish intestine. EMBO Rep 8:966–973

    Article  CAS  PubMed  Google Scholar 

  • Neuhoff V, Arold N, Taube D, Ehrhardt W (1988) Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9:255–262

    Article  CAS  PubMed  Google Scholar 

  • O’Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 10:4007–4021

    Google Scholar 

  • Oliveira V, Gatti R, Rioli V, Ferro ES, Spisni A, Camargo ACM, Juliano MA, Juliano L (2002) Temperature and salts effects on the peptidase activities of the recombinant metallooligopeptidases neurolysin and thimet oligopeptidase. Eur J Biochem 269:4326–4334

    Article  CAS  PubMed  Google Scholar 

  • Perez MJ, Rodriguez C, Cejas JR, Martin MV, Jerez S, Lorenzo A (2007) Lipid and fatty acid content in wild white seabream (Diplodus sargus) broodstock at different stages of the reproductive cycle. Comp Biochem Physiol 146B:187–196

    CAS  Google Scholar 

  • Perkins DN, Pappin DJ, Creasy DM, Cottrell JS (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20:3551–3567

    Article  CAS  PubMed  Google Scholar 

  • Posner M, Hawke M, LaCava C, Prince CJ, Bellanco NR, Corbin RW (2008) A proteome map of the zebrafish (Danio rerio) lens reveals similarities between zebrafish and mammalian crystallin expression. Mol Vis 14:806–814

    CAS  PubMed  Google Scholar 

  • Robinson BD, Drew RE, Murdoch GK, Powell M, Rodnick KJ, Settles M, Stone D, Churchill E, Hill RA, Papasani MR, Lewis SS, Hardy RW (2008) Sexual dimorphism in hepatic gene expression and the response to dietary carbohydrate manipulation in the zebrafish (Danio rerio). Comp Biochem Physiol 3D:141–154

    Google Scholar 

  • Rottbauer W, Wessels G, Dahme T, Just S, Trano N, Hassel D, Burns CG, Katus HA, Fishman MC (2006) Cardiac myosin light chain-2: a novel essential component of thick myofilament assembly and contractility of the heart. Circ Res 99:323–331

    Article  CAS  PubMed  Google Scholar 

  • Saavedra M, Conceição LEC, Pousão-Ferreira P, Dinis MT (2006) Amino acid profiles of Diplodus sargus (L., 1758) larvae: implications for feed formulation. Aquaculture 261:587–593

    Article  CAS  Google Scholar 

  • Shrader EA, Henry TR, Greeley MS Jr, Bradley BP (2003) Proteomics in zebrafish exposed to endocrine disrupting chemicals. Ecotoxicology 12:485–488

    Article  CAS  PubMed  Google Scholar 

  • Smith RW, Cash P, Ellefsen S, Nilsson GE (2009) Proteomic changes in the crucian carp brain during exposure to anoxia. Proteomics 9:2217–2229

    Article  CAS  PubMed  Google Scholar 

  • Stainier DY, Lee RK, Fishman MC (1993) Cardiovascular development in the zebrafish. I. Myocardial fate map and heart tube formation. Development 119:31–40

    CAS  PubMed  Google Scholar 

  • Tay TL, Lin Q, Seow TK, Tan KH, Hew CL, Gong Z (2006) Proteomic analysis of protein profiles during early development of the zebrafish, Danio rerio. Proteomics 6:3176–3188

    Article  CAS  PubMed  Google Scholar 

  • Traut W, Winking H (2001) Meotic chromosomes and stages of sex chromosome evolution in fish: zebrafish, platyfish, and guppy. Chrom Res 9:659–672

    Article  CAS  PubMed  Google Scholar 

  • Vihtelic TS, Fadool JM, Gao J, Thornton KA, Hyde DR, Wistow GJ (2005) Expressed sequence tag analysis of zebrafish eye tissues for NEIBank. Mol Vis 11:1083–1100

    CAS  PubMed  Google Scholar 

  • Vilhelmsson OT, Martin SAM, Médale F, Kaushik SJ, Houlihan DF (2004) Dietary plant-protein substitution affects hepatic metabolism in rainbow trout (Oncorhynchus mykiss). Br J Nutr 92:71–80

    Article  CAS  PubMed  Google Scholar 

  • Wålinder O, Zetterqvist Ö, Enström L (1969) Intermediary phosphorylation of bovine liver nucleoside diphosphate kinase. J Biol Chem 244:1060–1064

    PubMed  Google Scholar 

  • Wallimann T, Wyss M, Brdiczka D, Nicolay K, Eppenberger HM (1992) Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the “phosphocreatine circuit” for cellular energy homeostasis. Biochem J 281:21–40

    CAS  PubMed  Google Scholar 

  • Wang H, Yan T, Tan JTT, Gong Z (2000) A zebrafish vitellogenin gene (vg3) encodes a novel vitellogenin without a phosvitin domain and may represent a primitive vertebrate vitellogenin gene. Gene 256:303–310

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Tan JTT, Emelyanov A, Korzh V, Gong Z (2005) Hepatic and extrahepatic expression of vitellogenin genes in the zebra fish. Gene 356:91–100

    Article  CAS  PubMed  Google Scholar 

  • Westerfield M (2000) The zebrafish book: a guide for the laboratory use of zebrafish (Danio rerio). University of Oregon Press, Eugene

    Google Scholar 

  • Wilson RP (1994) Amino acid requirements of finfish. In: D’Mello JPF (ed) Amino acids in farm animal nutrition. CAB International, Wallingford, pp 377–399

    Google Scholar 

  • Yang X-Y, Yao J-H, Cheng L, Wei D-W, Xue J-L, Lu D-R (2003) Molecular cloning and expression of a smooth muscle-specific gene SM22α in zebrafish. Biochem Biophys Res Commun 312:741–746

    Article  CAS  PubMed  Google Scholar 

  • Zhang JCL, Kim S, Helmke BP, Yu WW, Du KL, Lu MM, Strobeck M, Yu Q-C, Parmacek MS (2001) Analysis of SM22α-deficient mice reveals unanticipated insights into smooth muscle cell differentiation and function. Mol Cell Biol 21:1336–1344

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was funded by the Research Council of Norway (165203/S40). P.G.R. was recipient of a research contract from the University of Bergen (UiB). Authors are especially grateful to Heikki Savolainen for excellent rearing of the fish and to Dr. Katerina Kousoulaki (Nofima ingredients, Bergen) for analysis of the amino acids profiles. The technical staff at the Research group of Developmental Biology of Fish at UiB is thanked for assistance and Dr. Kari E. Fladmark and colleagues at the Proteomic Laboratory of UiB for helpful discussions during proteomic data analysis.

Author information

Author notes

  1. P. Gómez-Requeni

    Present address: Instituto Tecnológico de Chascomús (IIB-INTECH), Camino de Circunvalación Laguna Km. 6, CC 164, B7130IWA, Chascomús, (Provincia de Buenos Aires), Argentina

Authors and Affiliations

  1. Department of Biology, High Technology Center, University of Bergen, 5008, Bergen, Norway

    P. Gómez-Requeni, A.-E. Olderbakk Jordal & I. Rønnestad

  2. CCMAR, University of Algarve, Campus de Gambelas, 8000-117, Faro, Portugal

    L. E. C. Conceição

Authors
  1. P. Gómez-Requeni
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. E. C. Conceição
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A.-E. Olderbakk Jordal
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. I. Rønnestad
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. Gómez-Requeni.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gómez-Requeni, P., Conceição, L.E.C., Olderbakk Jordal, AE. et al. A reference growth curve for nutritional experiments in zebrafish (Danio rerio) and changes in whole body proteome during development. Fish Physiol Biochem 36, 1199–1215 (2010). https://doi.org/10.1007/s10695-010-9400-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-010-9400-0

Keywords

Search

Navigation