Multiple ovarian lipoprotein receptors in teleosts

Abstract

Recent investigations have revealed multiplicity in maternal yolk precursors and their corresponding ovarian lipoprotein receptors (LRs) in diverse oviparous vertebrates, including fishes. This mini-review describes further evidence for the system of fish egg yolk formation mediated by multiple ovarian LRs, which have been obtained by studies utilizing a combination of conventional molecular and biochemical analyses, and modern proteome and transcriptome technologies. A hypothetical “multiple ovarian LR” model is proposed based on our current and previous knowledge of fish yolk formation.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. Amano H, Fujita T, Hiramatsu N, Kagawa H, Matsubara T, Sullivan CV, Hara A (2008) Multiple vitellogenin-derived yolk proteins in grey mullet (Mugil cephalus): disparate proteolytic patterns associated with ovarian follicle maturation. Mol Reprod Dev 75(8):1307–1317

    PubMed  Article  CAS  Google Scholar 

  2. Babin PJ (2008) Conservation of a vitellogenin gene cluster in oviparous vertebrates and identification of its traces in the platypus genome. Gene 413(1–2):76–82

    PubMed  Article  CAS  Google Scholar 

  3. Bujo H, Lindstedt KA, Hermann M, Dalmau LM, Nimpf J, Schneider WJ (1995) Chicken oocytes and somatic cells express different splice variants of a multifunctional receptor. J Biol Chem 270:23546–23551

    PubMed  Article  CAS  Google Scholar 

  4. Davail B, Pakdel F, Bujo H, Perazzolo LM, Waclawek M, Schneider WJ, Le Menn F (1998) Evolution of oogenesis: the receptor for vitellogenin from the rainbow trout. J Lipid Res 39:1929–1937

    PubMed  CAS  Google Scholar 

  5. Endo T, Todo T, Lokman PM, Kudo H, Ijiri S, Adachi S, Yamauchi K (2010) Androgens and very low density lipoprotein are essential for the growth of previtellogenic oocytes from Japanese eel, Anguilla japonica, in vitro. Biol Reprod 84(4):816–825

    PubMed  Article  Google Scholar 

  6. Finn RN, Kristoffersen BA (2007) Vertebrate vitellogenin gene duplication in relation to the “3R hypothesis”: correlation to the pelagic egg and the oceanic radiation of teleosts. PLos One 2(1):e169

    PubMed  Article  Google Scholar 

  7. Hiramatsu N, Hara A, Matsubara T, Hiramatsu K, Sullivan CV (2003) Oocyte growth in temperate basses: multiple forms of vitellogenin and their receptor. Fish Physiol Biochem 28:301–303

    Article  CAS  Google Scholar 

  8. Hiramatsu N, Chapman RW, Lindzey JK, Haynes MR, Sullivan CV (2004) Molecular characterization and expression of vitellogenin receptor from white perch (Morone americana). Biol Reprod 70(6):1720–1730

    PubMed  Article  CAS  Google Scholar 

  9. Hiramatsu N, Cheek AO, Sullivan CV, Matsubara T, Hara A (2005) Vitellogenesis and endocrine disruption. In: Mommsen TP, Moon TW (eds) Biochemistry and molecular biology of fishes, 6th edn. Elsevier, Amsterdam, pp 431–471

    Google Scholar 

  10. Hummel S, Lynn EG, Osanger A, Hirayama S, Nimpf J, Schneider WJ (2003) Molecular characterization of the first avian LDL receptor: role in sterol metabolism of ovarian follicular cells. J Lipid Res 44:1633–1642

    PubMed  Article  CAS  Google Scholar 

  11. Hussain MM, Strickland DK, Bakillah A (1999) The mammalian low-density lipoprotein receptor family. Annu Rev Nutr 19:141–172

    PubMed  Article  CAS  Google Scholar 

  12. Kwon JY, Prat F, Randall C, Tyler CR (2001) Molecular characterization of putative yolk processing enzymes and their expression during oogenesis and embryogenesis in rainbow trout Oncorhynchus mykiss. Biol Reprod 65(6):1701–1709

    PubMed  Article  CAS  Google Scholar 

  13. Mahley RW, Ji ZS (1999) Remnant lipoprotein metabolism: key pathways involving cell-surface heparin sulfate proteoglycans and apolipoprotein E. J Lipid Res 40:1–16

    PubMed  CAS  Google Scholar 

  14. Mizuta H, Hiramatsu N, Todo T, Ito Y, Gen K, Kazeto Y, Sullivan CV, Reading BJ, Hara A (2011) Molecular cloning and localization of two classical ovarian lipoprotein receptors in cutthroat trout Oncorhynchus clarki. Indian J Sci Technol, 9th ISRPF issue, 4(S8):192–193

    Google Scholar 

  15. Nishimiya O, Kunihiro Y, Hiramatsu N, Inagawa H, Todo T, Matsubara T, Reading BJ, Sullivan CV, Hara A (2011) Molecular characterization and expression analysis of estrogen receptor and vitellogenins in inshore hagfish (Eptatretus Burgeri). Indian J Sci Technol, 9th ISRPF issue, 4(S8):194–195

    Google Scholar 

  16. Prat F, Coward K, Sumpter JP, Tyler CR (1998) Molecular characterization and expression of two ovarian lipoprotein receptors in the rainbow trout, Oncorhynchus mykiss. Biol Reprod 58(5):1146–1153

    PubMed  Article  CAS  Google Scholar 

  17. Reading BJ, Hiramatsu N, Sullivan CV (2011) Disparate binding of three types of vitellogenin to multiple forms of vitellogenin receptor in white perch. Biol Reprod 84(2):392–399

    PubMed  Article  CAS  Google Scholar 

  18. Ryu Y-W, Tanaka R, Kasahara A, Saito K, Kanno K, Ito Y, Hiramatsu N, Todo T, Sullivan CV, Hara A (2011) Expression of genes involved in oocyte lipidation in cutthroat trout, Oncorhynchus clarki. Indian J Sci Technol, 9th ISRPF issue, 4(S8):203–204

    Google Scholar 

  19. Stifani S, Le Menn F, Rodriguez JN, Schneider WJ (1990) Regulation of oogenesis: the piscine receptor for vitellogenin. Biochem Biophys Acta 1045(3):271–279

    PubMed  Article  CAS  Google Scholar 

  20. Tyler CR, Lubberink K (1996) Identification of four ovarian receptor proteins that bind vitellogenin but not other homologous plasma lipoproteins in the rainbow trout, Oncorhynchus mykiss. J Comp Physiol B 166(1):11–20

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by JSPS KAKENHI (#22380103: Grant-in-Aid for Scientific Research B; #19380106, #19780143, and #23580243: Grant-in-Aid for Young Scientists B).

Author information

Affiliations

Authors

Corresponding author

Correspondence to N. Hiramatsu.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Hiramatsu, N., Luo, W., Reading, B.J. et al. Multiple ovarian lipoprotein receptors in teleosts. Fish Physiol Biochem 39, 29–32 (2013). https://doi.org/10.1007/s10695-012-9612-6

Download citation

Keywords

  • Low-density lipoprotein receptor superfamily
  • Oogenesis
  • Ovarian lipidation
  • Vitellogenesis
  • Yolk formation