Skip to main content
Log in

Localization and possible function of nrF-AGP, an alpha-1-acid glycoprotein-like protein in viviparous fish Neoditrema ransonnetii (Perciformes, Embiotocidae)

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

Abstract

The nrF-AGP, a 51-kDa acidic glycoprotein found in surfperch (Neoditrema ransonnetii; Perciformes, Embiotocidae), is a member of the lipocalin superfamily. nrF-AGP is the major component in ovarian cavity fluid (OCF), but not in plasma of pregnant females, which suggests its potential relevance in pregnancy. However, its production in the liver, irrespective of reproductive cycle and sex, indicates that the protein also has physiological functions other than its contribution to reproduction. In the present study, Western blot analysis indicated that this protein is widely distributed in the cutaneous and intestinal mucosa, bile, and abdominal adipose tissue of fish, as well as plasma and OCF. Immunohistochemical staining of nrF-AGP was observed in hepatocytes, adipocytes, pancreatic cells, epidermal cells, and epithelial cells of ovigerous lamellae. Transcripts were detected in adipose tissue as well as hepatocytes by reverse transcription PCR analysis. This broad distribution of nrF-AGP suggests that this protein participates in various biological processes through its ability to bind to hydrophobes. After administration of biotinylated F-AGP into the ovarian cavity, the protein was detected in the cytoplasm of the intestinal epithelial cells of the fetus within 4 h. This suggests that nrF-AGP in the ovarian cavity acts as a transporter delivering maternal resources to the fetus.

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

Access this article

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

  • Akerstrom B, Flower DR, Salier JP (2000) Lipocalins: unity in diversity. Biochim Biophys Acta 1482:1–8

    Article  CAS  PubMed  Google Scholar 

  • Bennett M, Schmid K (1980) Immunosuppression by human plasma α1-acid glycoprotein: importance of the carbohydrate moiety. Proc Natl Acad Sci USA 77:6109–6113

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ceciliani F, Pocacqua V (2007) The acute phase protein α1-acid glycoprotein: a model for altered glycosylation during diseases. Curr Protein Pept Sci 8:91–108

    Article  CAS  PubMed  Google Scholar 

  • Dobbs GH (1975) Scanning electron microscopy of intraovarian embryos of the viviparous teleost, Micrometrus minimus (Gibbons), (Perciformes: Embiotocidae). J Fish Biol 7:209–214

    Article  Google Scholar 

  • Fantuzzi G (2005) Adipose tissue, adipokines, and inflammation. J Allergy Clin Immunol 115:911–919

    Article  CAS  PubMed  Google Scholar 

  • Flower DR, North AC, Sansom CE (2000) The lipocalin protein family; structural and sequence overview. Biochim Biophys Acta 1482:9–24

    Article  CAS  PubMed  Google Scholar 

  • Fournier T, Medjoubi-N N, Porquet D (2000) Alpha-1-acid glycoprotein. Biochim Biophys Acta 1482:157–171

    Article  CAS  PubMed  Google Scholar 

  • Ganfornina MD, Guetierrez G, Bastiani M, Sanchez D (2000) A phylogenetic analysis of the lipocalin protein family. Mol Biol Evol 17:114–126

    Article  CAS  PubMed  Google Scholar 

  • Grzyb J, Latowski D, Strazalka K (2006) Lipocalins: a family portrait. J Plant Physiol 163:895–915

    Article  CAS  PubMed  Google Scholar 

  • Hochepied T, Berger FG, Baumann H, Libert C (2003) α1-Acid glycoprotein: an acute phase protein with inflammatory and immunomodulating properties. Cytokine Growth Factor Rev 14:25–34

    Article  CAS  PubMed  Google Scholar 

  • Israili ZH, Dayton PG (2001) Human alpha-1-glycoprotein and its interactions with drugs. Drug Metab Rev 33:161–235

    Article  CAS  PubMed  Google Scholar 

  • Lacunza I, Diez-Masa JC, de Frutos M (2007) CIEF with hydrodynamic and chemical mobilization for the separation of forms of alpha-1-acid glycoprotein. Electrophoresis 28:1204–1213

    Article  CAS  PubMed  Google Scholar 

  • Lee YS, Choi JW, Hwang I, Lee WJ, Lee HJ, Kim AY, Huh JY, Koh WY, Koy GY, Son HJ, Masuzaki H, Hotta K, Alfadda AA, Kim JB (2010) Adipocytokine orosomucoid integrates inflammatory and metabolic signals to preserve energy homeostasis by resolving immoderate inflammation. J Biol Chem 285:22174–22185

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lin Y, Rajala MW, Berger JP, Moller DE, Barzilai N, Scherer PE (2001) Hyperglycemia-induced production of acute phase reactants in adipose tissue. J Biol Chem 276:42077–42083

    Article  CAS  PubMed  Google Scholar 

  • Machnes Z, Avtalion R, Shirak A, Trombka D, Wides R, Fellous M, Don J (2008) Male-specific protein (MSP): a new gene linked to sexual behavior and aggressiveness of tilapia males. Horm Behav 54:442–449

    Article  CAS  PubMed  Google Scholar 

  • Meador JP (2000) Predicting the fate and effects of tributyltin in marine systems. Rev Environ Contam Toxicol 166:1–48

    CAS  PubMed  Google Scholar 

  • Nakamura O, Tazumi Y, Muro T, Yasuhara Y, Watanabe T (2004) Active uptake and transport of protein by the intestinal epithelial cells in embryo of viviparous fish, Neoditrema ransonnetii (Perciformes, Embiotocidae). J Exp Zool 301A:38–48

    Article  Google Scholar 

  • Nakamura O, Kudo R, Aoki H, Watanabe T (2006) IgM secretion and absorption in the materno-fetal interface of a viviparous teleost, Neoditrema ransonnetii (Perciformes, Embiotocidae). Dev Comp Immunol 30:493–502

    Article  CAS  PubMed  Google Scholar 

  • Nakamura O, Nozawa Y, Saito E, Ikeda D, Tsutsui S (2009) An alpha-1-acid glycoprotein-like protein as a major component of the ovarian cavity fluid of viviparous fish, Neoditrema ransonnetii (Perciformes, Embiotocidae). Comp Biochem Physiol A 153:222–229

    Article  Google Scholar 

  • Oba Y, Shimasaki Y, Oshima Y, Satone H, Kitano T, Nakao M, Kawabata S, Honjo T (2007) Purification and characterization of tributyltin-binding protein type2 from plasma of Japanese flounder. Paralichthys olivaceus. J. Biochem 142:229–238

    Article  CAS  Google Scholar 

  • Oba Y, Yamauchi A, Hashiguchi Y, Satone H, Miki S, Nassef M, Shimasaki Y, Kitano T, Nakao M, Kawabata S, Honjo T, Oshima Y (2011) Purification and characterization of tributyltin-binding protein of tiger puffer, Takifugu rubripes. Comp Biochem Physiol 153:17–23

    Google Scholar 

  • Ohji M, Arai T, Miyazaki N (2006) Transfer of tributyltin from parental female to offspring in the viviparous surfperch Ditrema temmincki. Mar Ecol-Prog Ser 307:307–310

    Article  CAS  Google Scholar 

  • Pos O, Oostendorp RAJ, Van der Stelt ME, Scheper RJ, Van Dijk W (1990) Con A-nonreactive human α1-acid glycoprotein (AGP) is more effective in modulation of lymphocyte proliferation than con A-reactive AGP serum variants. Inflammation 14:133–141

    Article  CAS  PubMed  Google Scholar 

  • Satone H, Oshima Y, Shimasaki Y, Tawaratsumida T, Oba Y, Takahashi E, Kitano T, Kawabata S, Kakuta Y, Honjo T (2008) Tributyltin-binding protein type 1 has a distinctive lipocalin-like structure and is involved in the excretion of tributyltin in Japanese flounder, Paralichthys olivaceus. Aquat Toxicol 90:292–299

    Article  CAS  PubMed  Google Scholar 

  • Shimasaki Y, Oshima Y, Yokota Y, Kitano T, Nakao M, Kawabata S, Imada N, Honjo T (2002) Purification and identification of a tributyltin-binding protein from serum of Japanese flounder, Paralichthys olivaceus. Environ Toxicol Chem 21:1229–1235

    Article  CAS  PubMed  Google Scholar 

  • Shirak A, Reicher S, Uliel S, Mehlman T, Shainskaya A, Ron M, Seroussi E (2012) Gender and sexual behavior modulate the composition of serum lipocalins in Nile tilapia (Oreochromis niloticus). Gene 504:22–30

    Article  CAS  PubMed  Google Scholar 

  • Turner CL (1938) Histological and cytological changes in the ovary of Cymatogaster aggregata during gestation. J Morph 62:351–373

    Article  Google Scholar 

  • Wourms JP (1981) Viviparity: the maternal –fetal relationship in fishes. Am J Zool 21:473–515

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Osamu Nakamura.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nakamura, O., Watabe, Y., Matsumoto, N. et al. Localization and possible function of nrF-AGP, an alpha-1-acid glycoprotein-like protein in viviparous fish Neoditrema ransonnetii (Perciformes, Embiotocidae). Fish Physiol Biochem 40, 1907–1915 (2014). https://doi.org/10.1007/s10695-014-9978-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-014-9978-8

Keywords

Navigation