Skip to main content
SpringerLink
Log in

Identification, Phylogeny, and Function of fabp2 Paralogs in Two Non-Model Teleost Fish Species

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

Intestinal fatty-acid-binding protein (IFABP or FABP2) is a cytosolic transporter of long-chain fatty acids, which is mainly expressed in cells of intestinal tissue. Fatty acids in teleosts are an important source of energy for growth, reproduction, and swimming and a main ingredient in the yolk sac of embryos and larvae. The fabp2 paralogs, fabp2a and fabp2b, were identified for 26 teleost fish species including the paralogs for the two non-model teleost fish species, namely the gilthead sea bream (Sparus aurata) and the European sea bass (Dicentrarchus labrax). Despite the high similarity of fabp2 paralogs, as well as the identical organization in four exons, paralogs were mapped to different chromosomes/linkage groups supporting the hypothesis that the identified transcripts are true paralogs originating from a single ancestor gene after genome duplication. This was also confirmed by phylogenetic analysis using fabp2 sequences of 26 teleosts and by synteny analysis carried out with ten teleosts. Differential expression analysis of the gilthead sea bream and European sea bass fabp2 paralogs in the intestine after fasting and refeeding experiment further revealed their altered implication in metabolism. Additional expression studies in seven developmental stages of the two species detected fabp2 paralogs relatively early in the embryonic development as well as possible complementary or separated roles of the paralogs. The identification and characterization of the two fabp2 paralogs will contribute significantly to the understanding of the fabp2 evolution as well as of the divergences in fatty acid metabolism.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abbas S, Raza ST, Chandra A et al (2014) Association of ACE, FABP2 and GST genes polymorphism with essential hypertension risk among a North Indian population. Ann Hum Biol 00:1–9. doi:10.3109/03014460.2014.968206

    Google Scholar 

  • Alves-Costa FA, Denovan-Wright EM, Thisse C et al (2008) Spatio-temporal distribution of fatty acid-binding protein 6 (fabp6) gene transcripts in the developing and adult zebrafish (Danio rerio). FEBS J 275:3325–3334. doi:10.1111/j.1742-4658.2008.06480.x

    Article  CAS  PubMed  Google Scholar 

  • André M, Ando S, Ballagny C (2000) Intestinal fatty acid binding protein gene expression reveals the cephalocaudal patterning during zebrafish gut morphogenesis. Int J Dev Biol 252:249–252

    Google Scholar 

  • Auinger A, Helwig U, Rubin D et al (2010) Human Intestinal fatty acid binding protein 2 expression is associated with fat. J Nutr Biochem Mol Gen Mech 140:1411–1417. doi:10.3945/jn.109.118034.following

    CAS  Google Scholar 

  • Bernlohr DA, Simpson MA, Hertzel AV, Banaszak LJ (1997) Intracellular lipid-binding protein and their genes. Annu Rev Nutr 17:277–303

    Article  CAS  PubMed  Google Scholar 

  • Besnard P, Niot I, Poirier H (2002) New insights into the fatty acid-binding protein (FABP) family in the small intestine. Mol Cell 239:139–147

    CAS  Google Scholar 

  • Biasini M, Bienert S, Waterhouse A et al (2014) SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42:W252–W258. doi:10.1093/nar/gku340

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Danzmann RG, Davidson EA, Ferguson MM et al (2008) Distribution of ancestral proto-actinopterygian chromosome arms within the genomes of 4R-derivative salmonid fishes (Rainbow trout and Atlantic salmon). BMC Genomics 9:557. doi:10.1186/1471-2164-9-557

    Article  PubMed Central  PubMed  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Meth 9:772

    Article  CAS  Google Scholar 

  • Divanach P (1985) Contribution to biology and rearing of six Mediterranean Sparids: Sparus aurata, Diplodus sargus, Diplodus vulgaris, Diplodus annularis, Lithognathus mormyrus, Puntazzo puntazzo (Teleostean fishes). University of Sciences & Techniques of Languedoc, Montpellier II, 479 p. (in French)

    Google Scholar 

  • Fernández CG, Roufidou C, Antonopoulou E, Sarropoulou E (2012) Expression of developmental-stage-specific genes in the gilthead sea bream Sparus aurata L. Mar Biotechnol (NY). doi:10.1007/s10126-012-9486-8

    Google Scholar 

  • Furuhashi M, Hotamisligil G (2008) Fatty acid-binding proteins: role in metabolic diseases and potential as drug targets. Nat Rev Drug Discov 7:489. doi:10.1038/nrd2589

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Glatz JFC, van der Vusse GJ (1996) Cellular fatty acid-binding proteins: their function and physiological significance. Prog Lipid Res 35:243–282

    Article  CAS  PubMed  Google Scholar 

  • Guyon R, Senger F, Rakotomanga M, Sadequi N, Volckaert FAM, Hitte C, Galibert F (2010)  A radiation hybrid map of the European sea bass (Dicentrarchus labrax) based on 1581 markers: synteny analysis with model fish genomes. Genomics 96:228–238

  • Jaillon O, Aury J-M, Brunet F et al (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431:946–957. doi:10.1038/nature03025

    Article  PubMed  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. doi:10.1093/molbev/mst010

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kent WJ (2002) BLAT—the BLAST-like alignment tool. Genome Res 12:656–664. doi:10.1101/gr.229202

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Koonin EV (2005) Orthologs, paralogs, and evolutionary genomics. Annu Rev Genet 39:309–338. doi:10.1146/annurev.genet.39.073003.114725

    Article  CAS  PubMed  Google Scholar 

  • Korf I, Yandell M, Bedell J (2003) BLAST, O'Reilly, Sebastopol

  • Kuhl H, Tine M, Hecht J et al (2011) Analysis of single nucleotide polymorphisms in three chromosomes of European sea bass Dicentrarchus labrax. Comp Biochem Physiol Part D Genomics Proteomics 6:70–75. doi:10.1016/j.cbd.2010.04.003

    Article  PubMed  Google Scholar 

  • Lai YYY, Lubieniecki KP, Phillips RB et al (2009) Genomic organization of Atlantic salmon (Salmo salar) fatty acid binding protein (fabp2) genes reveals independent loss of duplicate loci in teleosts. Mar Genomics 2:193–200. doi:10.1016/j.margen.2009.10.003

    Article  PubMed  Google Scholar 

  • Li WH, Yang J, Gu X (2005) Expression divergence between duplicate genes. Trends Genet 21:602–607. doi:10.1016/j.tig.2005.08.006

    Article  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408. doi:10.1006/meth.2001.1262

    Article  CAS  PubMed  Google Scholar 

  • Louis A, Muffato M, Roest Crollius H (2013) Genomicus: five genome browsers for comparative genomics in eukaryota. Nucleic Acids Res 41:D700–D705. doi:10.1093/nar/gks1156

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Maruyama K, Kojima A, Yasuda T et al (2008) Expression of brain-type fatty acid-binding protein (fabp7) in medaka during development. J Exp Zool B Mol Dev Evol 310:577–587. doi:10.1002/jez.b.21226

    Article  PubMed  Google Scholar 

  • Meyer A, Van de Peer Y (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). BioEssays 27:937–945. doi:10.1002/bies.20293

    Article  CAS  PubMed  Google Scholar 

  • Mininni AN, Milan M, Ferraresso S et al (2014) Liver transcriptome analysis in gilthead sea bream upon exposure to low temperature. BMC Genomics 15:765. doi:10.1186/1471-2164-15-765

    Article  PubMed Central  PubMed  Google Scholar 

  • Mitter K, Kotoulas G, Magoulas A et al (2009) Evaluation of candidate reference genes for QPCR during ontogenesis and of immune-relevant tissues of European seabass (Dicentrarchus labrax). Comp Biochem Physiol Part B Biochem Mol Biol 153:340–347

    Article  Google Scholar 

  • Nehrt NL, Clark WT, Radivojac P, Hahn MW (2011) Testing the ortholog conjecture with comparative functional genomic data from mammals. PLoS Comput Biol 7:e1002073. doi:10.1371/journal.pcbi.1002073

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. Springer-Verlag, New York

    Book  Google Scholar 

  • Parmar MB, Wright JM (2013) Comparative evolutionary genomics of medaka and three-spined stickleback fabp 2a and fabp2b genes with fabp2 of zebrafish. Genome 56:27–37

    Article  CAS  PubMed  Google Scholar 

  • Parmar MB, Venkatachalam AB, Wright JM (2012a) Comparative genomics and evolutionary diversification of the duplicated fabp6a and fabp6b genes in medaka and three-spined stickleback. Comp Biochem Physiol Part D Genomics Proteomics 7:311–321. doi:10.1016/j.cbd.2012.10.001

    Article  CAS  PubMed  Google Scholar 

  • Parmar MB, Venkatachalam AB, Wright JM (2012b) The evolutionary relationship of the transcriptionally active fabp11a (intronless) and fabp11b genes of medaka with fabp11 genes of other teleost fishes. FEBS J 279:2310–2321. doi:10.1111/j.1742-4658.2012.08611.x

    Article  CAS  PubMed  Google Scholar 

  • Peterson ME, Chen F, Saven JG et al (2009) Evolutionary constraints on structural similarity in orthologs and paralogs. Protein Sci 18:1306–1315. doi:10.1002/pro.143

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Poupard G, André M, Durliat M et al (2000) Apolipoprotein E gene expression correlates with endogenous lipid nutrition and yolk syncytial layer lipoprotein synthesis during fish development. Cell Tissue Res 300:251–261

    Article  CAS  PubMed  Google Scholar 

  • Qiu C-J, Ye X-Z, Yu X-J et al (2014) Association between FABP2 Ala54Thr polymorphisms and type 2 diabetes mellitus risk: a HuGE Review and Meta-Analysis. J Cell Mol Med 18:2530–2535. doi:10.1111/jcmm.12385

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rønnestad I, Koven WM, Tandler A et al (1994) Energy metabolism during development of eggs and larvae of gilthead sea bream (Sparus aurata). Mar Biol 120:187–196. doi:10.1007/BF00349678

    Article  Google Scholar 

  • Rønnestad I, Koven W, Tandler A et al (1998) Utilisation of yolk fuels in developing eggs and larvae of European sea bass (Dicentrarchus labrax). Aquaculture 162:157–170

    Article  Google Scholar 

  • Sacchettini JC, Gordon JI, Banaszak LJ (1989) Crystal structure of rat intestinal protein refinement and analysis of the Escherichia coli-derived protein with bound palmitate. J Mol Biol 208:327–339

    Article  CAS  PubMed  Google Scholar 

  • Sarropoulou E, Fernandes JMO (2011) Comparative genomics in teleost species: knowledge transfer by linking the genomes of model and non-model fish species. Comp Biochem Physiol Part D Genomics Proteomics 6:92–102

    Article  PubMed  Google Scholar 

  • Sarropoulou E, Nousdili D, Magoulas A, Kotoulas G (2008) Linking the genomes of nonmodel teleosts through comparative genomics. Mar Biotechnol (NY) 10:227–233

    Article  CAS  Google Scholar 

  • Sarropoulou E, Fernandes JMO, Mitter K et al (2010) Evolution of a multifunctional gene: the warm temperature acclimation protein Wap65 in the European seabass Dicentrarchus labrax. Mol Phylogenet Evol 55:640–649

    Article  CAS  PubMed  Google Scholar 

  • Sarropoulou E, Nousdili D, Kotoulas G, Magoulas A (2011) Functional divergences of GAPDH isoforms during early development in two perciform fish species. Mar Biotechnol (NY) 13:1115–1124. doi:10.1007/s10126-011-9375-6

    Article  CAS  Google Scholar 

  • Schaap FG, Van Der Vusse GJ, Glatz JFC (2002) Evolution of the family of intracellular lipid binding proteins in vertebrates. Mol Cell Biochem 239:69–77

    Article  CAS  PubMed  Google Scholar 

  • Sharma MK, Denovan-Wright EM, Degrave A et al (2004) Sequence, linkage mapping and early developmental expression of the intestinal-type fatty acid-binding protein gene (fabp2) from zebrafish (Danio rerio). Comp Biochem Physiol Part B Biochem Mol Biol 138:391–398. doi:10.1016/j.cbpc.2004.05.009

    Article  Google Scholar 

  • Stewart JM, Driedzic WR (1988) Fatty acid binding proteins in teleost fish. Can J Zool 66:2671–2675. doi:10.1139/z88-392

    Article  CAS  Google Scholar 

  • Storch J, Corsico B (2008) The emerging functions and mechanisms of mammalian fatty acid-binding proteins. Annu Rev Nutr 28:73–95. doi:10.1146/annurev.nutr.27.061406.093710

    Article  CAS  PubMed  Google Scholar 

  • Sweetser DA, Birkenmeier H, Klisak IJ et al (1987) The human and rodent intestinal fatty acid binding protein genes. J Biol Chem 262:16060–16071

    CAS  PubMed  Google Scholar 

  • Thirumaran A, Wright JM (2014) Fatty acid-binding protein (fabp) genes of spotted green pufferfish (Tetraodon nigroviridis): comparative genomics and spatial transcriptional regulation. Genome 57:289–301

    Article  CAS  PubMed  Google Scholar 

  • Tine M, Kuhl H, Gagnaire P-A et al (2014) European sea bass genome and its variation provide insights into adaptation to euryhalinity and speciation. Nat Commun. doi:10.1038/ncomms6770

    PubMed Central  PubMed  Google Scholar 

  • Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184. doi:10.1080/713610925

    Article  CAS  Google Scholar 

  • Venkatachalam AB, Thisse C, Thisse B, Wright JM (2009) Differential tissue-specific distribution of transcripts for the duplicated fatty acid-binding protein 10 (fabp10) genes in embryos, larvae and adult zebrafish (Danio rerio). FEBS J 276:6787–6797. doi:10.1111/j.1742-4658.2009.07393.x

    Article  CAS  PubMed  Google Scholar 

  • Venkatachalam AB, Sawler DL, Wright JM (2013) Tissue-specific transcriptional modulation of fatty acid-binding protein genes, fabp2, fabp3 and fabp6, by fatty acids and the peroxisome proliferator, clofibrate, in zebrafish (Danio rerio). Gene 520:14–21. doi:10.1016/j.gene.2013.02.034

    Article  CAS  PubMed  Google Scholar 

  • Venold FF, Penn MH, Thorsen J et al (2013) Intestinal fatty acid binding protein (fabp2) in Atlantic salmon (Salmo salar): localization and alteration of expression during development of diet induced enteritis. Comp Biochem Physiol A Mol Integr Physiol 164:229–240. doi:10.1016/j.cbpa.2012.09.009

    Article  CAS  PubMed  Google Scholar 

  • Vogel Hertzel A, Bernlohr D (2000) The mammalian fatty acid-binding protein multigene family: molecular and genetic insights into function. Trends Endocrinol Metab 11:175–180. doi:10.1016/S1043-2760(00)00257-5

    Article  CAS  Google Scholar 

  • Watanabe T (1982) Lipid nutrition in fish. Comp Biochem Physiol Part B Comp Biochem 73:3–15. doi:10.1016/0305-0491(82)90196-1

    Article  Google Scholar 

  • Weisiger RA (2002) Cytosolic fatty acid binding proteins catalyze two distinct steps in intracellular transport of their ligands. Mol Cell Biochem 239:35–42

    Article  CAS  PubMed  Google Scholar 

  • Wheelan SJ, Church DM, Ostell JM (2001) Spidey: a tool for mRNA-to-genomic alignments. Genome Res 11:1952–1957. doi:10.1101/gr.195301

    PubMed Central  CAS  PubMed  Google Scholar 

  • Xia JH, Lin G, He X et al (2013) Whole genome scanning and association mapping identified a significant association between growth and a SNP in the IFABP—a gene of the Asian seabass. BMC Genomics 14:295. doi:10.1186/1471-2164-14-295

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhao S, Fernald RD (2005) Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol 12:1047–1064. doi:10.1089/cmb.2005.12.1047

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Financial support for this study has been provided by the Ministry of Education and Religious Affairs, under the Call “ARISTEIA I” of the National Strategic Reference Framework 2007–2013 (ANnOTATE), co-funded by the EU and the Hellenic Republic through the European Social Fund. We would like to thank the Dr. C.S. Tsigenopoulos of the Institute of Marine Biology, Biotechnology and Aquaculture, Hellenic Centre for Marine Research, for providing fish eggs. We also thank the Informatics group of IMBBC for computational support.

Author information

Authors and Affiliations

  1. Institute of Marine Biology, Biotechnology and Aquaculture, Hellenic Centre for Marine Research, Thalassocosmos, Gournes Pediados, P.O. Box 2214, 71003, Heraklion, Crete, Greece

    Elisavet Kaitetzidou, Stavros Chatzifotis & Elena Sarropoulou

  2. Laboratory of Animal Physiology, Department of Zoology, School of Biology, Aristotle University of Thessaloniki, 54124, Thessaloniki, Greece

    Elisavet Kaitetzidou & Efthimia Antonopoulou

Authors
  1. Elisavet Kaitetzidou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stavros Chatzifotis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Efthimia Antonopoulou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elena Sarropoulou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elena Sarropoulou.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(TXT 3 kb)

ESM 2

(FASTA 42 kb)

ESM 3

(FASTA 56 kb)

ESM 4

(FASTA 47 kb)

ESM 5

(XLSX 11 kb)

ESM 6

(JPEG 717 kb)

ESM 7

(TXT 30 kb)

ESM 8

(TXT 10 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kaitetzidou, E., Chatzifotis, S., Antonopoulou, E. et al. Identification, Phylogeny, and Function of fabp2 Paralogs in Two Non-Model Teleost Fish Species. Mar Biotechnol 17, 663–677 (2015). https://doi.org/10.1007/s10126-015-9648-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-015-9648-6

Keywords

Search

Navigation