Skip to main content
SpringerLink
Log in

Structural and biochemical characterization and evolutionary relationships of the fatty acid-binding protein 10 (Fabp10) of hake (Merluccius hubbsi)

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

Abstract

A fatty acid-binding protein (FABP) from the liver of Argentine hake (Merluccius hubbsi) was isolated and characterized and its expression analyzed. The determination of its partial primary structures (72 %) showed that it presents highest identity with Fabp10, commonly termed liver basic-type FABP. The evolutionary tree showed greater relationship between the Fabp10 of hake (Me Fabp10) and the Fabp10 and the Fabp10a of teleost fish. Me Fabp10 had low affinity for palmitic, oleic and palmitoleic acid and high affinity for bilirubin, lysophosphatidylcholine and lysophosphatidylethanolamine, all of them important in the metabolic functions of the liver. Me Fabp10 was able to bind only one cis-parinaric acid molecule and was found to be expressed only in the liver.

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
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Agulleiro MJ, André M, Morais S, Cerdá J, Babin PJ (2008) High transcript level of a fatty acid-binding protein 11 but not of vitellogenin receptor is correlated to ovarian follicle atresia in a teleost fish (Solea senegalensis). Cybium 32(2 suppl):225

    Google Scholar 

  • Alvarez HM, Mayer F, Fabritius D, Steinbüchel A (1996) Formation of intracytoplasmic lipid inclusions by Rhodococcus opacus strain PD630. Arch Microbiol 165:377–386

    Article  CAS  PubMed  Google Scholar 

  • Baba K, Takahashi Y, Aoyagi Y, Odani S (1999) The amino acid sequence of a lamprey (Entosphenus japonicus) liver fatty acid-binding protein identified its close relationship to cardiac fatty acid-binding proteins of mammalia. Comp Biochem Physiol B Biochem Mol Biol 123(2):223–228

    Article  CAS  PubMed  Google Scholar 

  • Babin PJ (2009) Fatty acid-binding proteins. In: Esteves A (ed) Molecular evolution of vertebrate fatty acid-binding proteins, 1st edn. Transworld Research Network, Kerala, pp 17–29

    Google Scholar 

  • Banaszak L, Winter N, Xu Z, Bernlohr DA, Cowan S, Jones TA (1994) Lipid-binding proteins: a family of fatty acid and retinoid transport proteins. Adv Protein Chem 45:89–151

    Article  CAS  PubMed  Google Scholar 

  • Bayır M, Bayır A, Wright JM (2015) Divergent spatial regulation of duplicated fatty acid-binding protein (fabp) genes in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol Part D 14:26–32

    Google Scholar 

  • Brandl H, Gross RA, Lenz RW, Füller RC (1988) Pseudomonas oleovorans as a source of poly(β-Hydroxyalkanoates) for potential applications as biodegradable polyesters. Appl Environ Microbiol 54(8):1977–1982

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bruslé J, Anadon GG (1996) The Structure and function of fish liver. In: Munshi JSD, Dutta HM (eds) Fish morphology: horizon of new research, 1st edn. Science Publishers Inc, Lebanon, pp 77–93

    Google Scholar 

  • Capaldi S, Guariento M, Saccomani G, Fessas D, Perduca M, Monaco HL (2007) A single amino acid mutation in zebrafish (Danio rerio) liver bile acid-binding protein can change the stoichiometry of ligand binding. J Biol Chem 282(42):31008–31018

    Article  CAS  PubMed  Google Scholar 

  • Ceciliani F, Mónaco HL, Ronchi S, Faotto L, Spadon P (1994) The primary structure of a basic (pI 9.0) fatty acid-binding protein from liver of Gallus domesticus. Comp Biochem Physiol B Biochem Mol Biol 109:261–271

    Article  CAS  PubMed  Google Scholar 

  • Conrotto P, Hellman U (2005) Sulfonation chemistry as a powerful tool for MALDI TOF/TOF de novo sequencing and post-translational modification analysis. J Biomol Techol 16(4):441–452

    Google Scholar 

  • Córdoba OL, Sánchez EI, Veerkamp JH, Santomé JA (1998) Presence of intestinal, liver and heart/adipocyte fatty acid-binding protein types in the liver of a chimaera fish. Int J Biochem Cell Biol 30(12):1403–1413

    Article  PubMed  Google Scholar 

  • Córdoba OL, Sánchez EI, Santomé JA (1999) The main fatty acid-binding protein in the liver of the shark (Halaetunus bivius) belongs to the liver basic type. Isolation, amino acid sequence determination and characterization. Eur J Biochem 265(2):832–838

    Article  PubMed  Google Scholar 

  • Cousseau MB, Perrotta RG (2000) Peces marinos de Argentina. Biología, distribución, pesca. Publicaciones especiales INIDEP, Mar del Plata

  • Denovan-Wright E, Pierce M, Sharma M, Wright J (2000) cDNA sequence and tissue-specific expression of a basic liver-type fatty acid binding protein in adult zebrafish (Danio rerio). Biochim Biophys Acta 1492(1):227–232

    Article  CAS  PubMed  Google Scholar 

  • Di Pietro SM, Santomé JA (1996) Presence of two new fatty acid binding proteins in catfish liver. Biochem Cell Biol 74:675–680

    Article  PubMed  Google Scholar 

  • Di Pietro SM, Santomé JA (2000) Isolation, characterization and binding properties of two rat liver fatty acid-binding protein isoforms. Biochem Biophys Acta 1478:186–200

    PubMed  Google Scholar 

  • Di Pietro SM, Santomé JA (2001) Structural and biochemical characterization of the lungfish (Lepidosiren paradoxa) liver basic fatty-acid binding protein. Arch Biochem Biophys 388(1):81–90

    Article  PubMed  Google Scholar 

  • Di Pietro SM, Dell´Angélica EC, Veerkamp JH, Sterin-Speziale N, Santomé JA (1997) Amino acid sequence, binding properties and evolutionary relationships of the basic liver fatty acid-binding protein from the catfish Rhamdia sapo. Eur J Biochem 249(2):510–517

    Article  PubMed  Google Scholar 

  • Di Pietro SM, Veerkamp JH, Santomé JA (1999) Isolation, amino acid sequencing and binding properties of two fatty acid-binding proteins from axolotl (Ambistoma mexicanum) liver. Evolutionary implications. Eur J Biochem 259:127–134

    Article  Google Scholar 

  • Di Pietro SM, Córsico B, Perduca M, Mónaco HL, Santomé JA (2003) Structural and biochemical characterization of toad liver fatty acid-binding protein. Biochemistry 42:8192–8203

    Article  PubMed  Google Scholar 

  • Falch E, Overby A, Rustad T (2006) Natural antioxidants in cod liver oil: pitfalls during oxidative stability assessment. In: Luten JB, Jacobsen C, Bekaert K, Sæbø A, Oehlenschlager J (eds) Seafood from fish to dish, quality, safety and processing of wild and farmed fish, 1st edn. Wageningen Academic Publishers, Wageningen, pp 127–137

    Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226(1):497–509

    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 

  • Glatz JFC, Veerkamp JH (1983) A radiochemical procedure for the assay of fatty acid-binding by proteins. Anal Biochem 132:89–95

    Article  CAS  PubMed  Google Scholar 

  • Guil-Guerrero JL, Venegas-Venegas E, Rincón-Cervera MA, Suarez MD (2011) Fatty acid profiles of livers from selected marine fish species. J Food Compos Anal 24:217–222

    Article  CAS  Google Scholar 

  • Hall TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Harlow E, Lane D (1999) Using antibodies: a laboratory manual. Cold Spryng Harb Lab Press, Cold Spryng Harbor

    Google Scholar 

  • Haunerland NH, Spener F (2004) Properties and physiological significance of fatty acid binding proteins. In: van der Vusse G (ed) Advances in molecular and cell biology, lipobiology, vol 33. Elsevier, New York, pp 99–120

    Google Scholar 

  • Hawkes R, Niday E, Gordon J (1982) A dot-immunobinding assay for monoclonal and other antibodies. Anal Biochem 119(1):142–147

    Article  CAS  PubMed  Google Scholar 

  • Hertzel AV, Bernlohr DA (2000) The mammalian fatty acid-binding protein multigene family: molecular and genetic insights into function. Trends Endocrinol Metab 11(5):175–180

    Article  CAS  PubMed  Google Scholar 

  • Kim S (2006) Basic liver-type fatty acid binding protein in rainbow trout Oncorhynchus mykiss: sequence and gene expression in tissue. Fish Sci 72:1316–1318

    Article  Google Scholar 

  • Kim HK, Storch J (1992) Mechanism of free fatty acid transfer from rat heart acid binding protein to phospholipid membrane. Evidence for a collitional process. J Biol Chem 267:20051–20056

    CAS  PubMed  Google Scholar 

  • Liu RZ, Li X, Godboor R (2008) A novel fatty acid-binding protein (FABP) gene resulting from tandem gene duplication in mammals: transcription in rat retina and testis. Genomics 92:436–445

    Article  CAS  PubMed  Google Scholar 

  • Lloret J, Demestre M, Sánchez-Pardo J (2008) Lipid (energy) reserves of European hake (Merluccius merluccius) in the North-Western mediterranean. Vie et Milieu-life Environ 58(1):75–85

    Google Scholar 

  • Matarese V, Stone RL, Waggoner DW, Bernlohr DA (1989) Intracellular fatty acid trafficking and the role of cytosolic lipid binding proteins. Prog Lipid Res 28:245–272

    Article  CAS  PubMed  Google Scholar 

  • Medina G, Castro L, Pantoja S (2014) Fatty acids in Merluccius australis tissues, a comparison between females from inshore and offshore spawning areas in the Chilean Patagonia. Fish Res 160:41–49

    Article  Google Scholar 

  • Mommsen TP, Walsh PJ (1989) Evolution of urea synthesis in vertebrates: the piscine connection. Science 243:72–75

    Article  CAS  PubMed  Google Scholar 

  • Nemecz G, Hubbell T, Jefferson JR, Lowe JB, Schroeder F (1991a) Interaction of fatty acids with recombinant rat intestinal and liver fatty acid-binding proteins. Arch Biochem Biophys 286:300–309

    Article  CAS  PubMed  Google Scholar 

  • Nemecz G, Jefferson JR, Schroeder F (1991b) Polyene fatty acid interactions with recombinant intestinal and liver fatty acid-binding proteins Spectroscopic studies. J Biol Chem 266(26):17112–17123

    CAS  PubMed  Google Scholar 

  • Ono T, Odani S (2010) Initial studies of the cytoplasmic FABP superfamily. Proc Jpn Acad Ser B Phys Biol Sci 86(3):220–228

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Parmar MB, Wright JM (2013) Comparative genomic organization and tissue specific transcription of the duplicated fabp7 and fabp10 genes in teleost fishes. Genome 56(11):291–701

    Article  Google Scholar 

  • Parmar MB, Venkatachalam AB, Wright JM (2012) The evolutionary relationship of the transcriptionally active fabp11a (intronless) and fabp11b genes of medaka with fabp11 genes of other teleost fishes. FEBS J 279(13):2310–2321

    Article  CAS  PubMed  Google Scholar 

  • Richieri GV, Ogata RT, Kleinfeld AM (1996) Kinetics of fatty acid interactions with fatty acid binding proteins from adipocyte, heart and intestine. J Biol Chem 271:11291–11300

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425

    CAS  PubMed  Google Scholar 

  • Santomé JA, Di Pietro SM, Cavagnari BM, Córdoba OL, Dell´Angélica EC (1998) Fatty acid-binding proteins. Chronological description and discussion of hypotheses involving their molecular evolution. Trends Comp Biochem Physiol 4:23–38

    Google Scholar 

  • Scapin G, Spadon P, Mammi M, Zanotti G, Mónaco HL (1990) Crystal structure of chicken liver basic fatty acid-binding protein at 2.7 Å resolution. Mol Cell Biochem 98:95–99

    Article  CAS  PubMed  Google Scholar 

  • Schägger H, von Jagow G (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166:368–379

    Article  PubMed  Google Scholar 

  • Schleicher CH, Santomé JA (1996) Purification. Characterization and partial amino acid sequencing of an amphibian liver fatty acid binding protein. Biochem Cell Biol 74:109–115

    Article  CAS  PubMed  Google Scholar 

  • Schleicher CH, Córdoba OL, Santomé JA, Dell´Angélica EC (1995) Molecular evolution of the multigene family of intracellular lipid-binding proteins. Biochem Mol Biol Int 36:1117–1125

    CAS  PubMed  Google Scholar 

  • Schroeder F, Myers-Payne SC, Billheimer JT, Wood WG (1995) Probing the ligand binding sites of fatty acid and sterol carrier proteins: effects of ethanol. Biochemistry 34(37):11919–11927

    Article  CAS  PubMed  Google Scholar 

  • Sharma MK, Liu RZ, Thisse C, Thisse B, Denovan-Wright EM, Wright JM (2006) Hierarchical subfunctionalization of fabp1a, fabp1b and fabp10 tissue-specific expression may account for retention of these duplicated genes in the zebrafish (Danio rerio) genome. FEBS J 273(14):3216–3229

    Article  CAS  PubMed  Google Scholar 

  • Smathers RL, Petersen DR (2011) The human fatty acid-binding protein family: evolutionary divergences and functions. Hum Genomics 5(3):170–191

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Storch J, McDermott L (2009) Structural and functional analysis of fatty acid-binding proteins. J Lipid Res 50 (Suppl.):126–131

    Google Scholar 

  • Storch J, Herr FM, Hsu KT, Kim HK, Liou HL, Smith ER (1996) The role of membranes and intracellular binding proteins in cytoplasmic transport of hydrophobic molecules: fatty acid-binding proteins. Comp Biochem Physiol 115B:333–339

    Article  CAS  Google Scholar 

  • Tatusova TA, Madden TL (1999) Blast 2 sequences, a new tool for comparing protein and nucleotide sequence. FEMS Microbiol Lett 174(2):247–250

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting. Position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thompson JB, Winters N, Terwey D, Bratt J, Banaszak L (1997) The crystal structure of the liver fatty acid-binding protein. J Biol Chem 272:7140–7150

    Article  CAS  PubMed  Google Scholar 

  • Thumser AE, Voysey J, Wilton DC (1996) Mutations of recombinant rat live fatty acid-binding protein at residues 102 and 122 alter its structural integrity and affinity for physiological ligands. Biochem J 314(3):943–949

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76(9):4350–4354

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Veerkamp JH, Peeters RA, Maatman RGHJ (1991) Structural and functional features of different types of cytoplasmatic fatty acid-binding proteins. Biochim Biophys Acta 1081:1–24

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Zhang Q, Shi H, Liu W, Wang Y, Wang Q, Li H (2013) Differential expression of L-FABP and L-BABP between fat and lean chickens. Genet Mol Res 12(4):4192–4206

    Article  CAS  PubMed  Google Scholar 

  • Zimmerman AW, van Moerkerk HTB, Veerkamp JH (2001) Ligand specificity and conformational stability of human fatty acid-binding proteins. Int J Biochem Cell Biol 33:865–876

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank Dr. Roxana Silva for her assistance in phylogenetic analysis, Ing. Enrique Rost for his assistance in fatty acid analysis, Dr. Eduardo Fernández for assistance in immunoblot and Lic. Hebe Pérez Gold for antibody production. Amino acid sequencing was performed in the LANAIS-PROEM (National Protein Sequencing Facility, UBA-CONICET, Buenos Aires, Argentina).

Author information

Authors and Affiliations

  1. Departamento de Bioquímica, GQBMRNP-CRIDECIT, Facultad de Ciencias Naturales, Universidad Nacional de la Patagonia San Juan Bosco, 9000, Comodoro Rivadavia, Chubut, Argentina

    Cecilia Alejandra Crovetto & Osvaldo León Córdoba

Authors
  1. Cecilia Alejandra Crovetto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Osvaldo León Córdoba
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Osvaldo León Córdoba.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Crovetto, C.A., Córdoba, O.L. Structural and biochemical characterization and evolutionary relationships of the fatty acid-binding protein 10 (Fabp10) of hake (Merluccius hubbsi). Fish Physiol Biochem 42, 149–165 (2016). https://doi.org/10.1007/s10695-015-0126-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-015-0126-x

Keywords

Search

Navigation