Fish Physiology and Biochemistry

, Volume 40, Issue 3, pp 731–738 | Cite as

Teleost fish osteocalcin 1 and 2 share the ability to bind the calcium mineral phase

  • Sofia Cavaco
  • Matthew K. Williamson
  • Joana Rosa
  • Vânia Roberto
  • Odete Cordeiro
  • Paul A. Price
  • M. Leonor Cancela
  • Vincent Laizé
  • Dina C. Simes
Article

Abstract

The occurrence of a second osteocalcin (OC2) has been reported in teleost fish, where it coexists with OC1 in some species. While it has been proposed that OC2 gene originated from OC1 through the fish whole-genome duplication event, little information is available on its molecular function and physiological role. The present study brings biological data supporting the presence of OC2 in the mineral phase of teleost fish bone and its association with the mineral phase together with OC1. The occurrence of OC2 forms with different levels of phosphorylation or γ-carboxylation, and with amino acid substitutions was observed. Comparative analysis of mature peptide sequences revealed the high conservation existing between OC1 and OC2, in particular within the core γ-carboxyglutamic acid domain, and suggests that both protein forms may have the same function, i.e., binding of calcium ions or hydroxyapatite crystals.

Keywords

Osteocalcin Vitamin K-dependent proteins Protein purification Bone tissue Teleost fish 

Supplementary material

10695_2013_9880_MOESM1_ESM.pdf (165 kb)
Supplementary material 1 (PDF 165 kb)
10695_2013_9880_MOESM2_ESM.pdf (63 kb)
Supplementary material 2 (PDF 62 kb)
10695_2013_9880_MOESM3_ESM.pdf (186 kb)
Supplementary material 3 (PDF 185 kb)
10695_2013_9880_MOESM4_ESM.pdf (51 kb)
Supplementary material 4 (PDF 51 kb)

References

  1. Boskey AL, Gadaleta S, Gundberg C, Doty SB, Ducy P, Karsenty G (1998) Fourier transform infrared microspectroscopic analysis of bones of osteocalcin-deficient mice provides insight into the function of osteocalcin. Bone 23:187–196PubMedCrossRefGoogle Scholar
  2. Ducy P, Desbois C, Boyce B, Pinero G, Story B, Dunstan C, Smith E, Bonadio J, Goldstein S, Gundberg C, Bradley A, Karsenty G (1996) Increased bone formation in osteocalcin-deficient mice. Nature 382:448–452PubMedCrossRefGoogle Scholar
  3. Ferron M, Hinoi E, Karsenty G, Ducy P (2008) Osteocalcin differentially regulates β cell and adipocyte gene expression and affects the development of metabolic diseases in wild-type mice. Proc Natl Acad Sci USA 105:5266–5270PubMedCentralPubMedCrossRefGoogle Scholar
  4. Frazão C, Simes DC, Coelho R, Alves D, Williamson MK, Price PA, Cancela ML, Carrondo MA (2005) Structural evidence of a fourth Gla residue in fish osteocalcin: biological implications. Biochemistry 44:1234–1242PubMedCrossRefGoogle Scholar
  5. Gundberg CM, Clough ME (1992) The osteocalcin propeptide is not secreted in vivo or in vitro. J Bone Miner Res 7:73–80PubMedGoogle Scholar
  6. Hauschka PV, Carr SA (1982) Calcium-dependent α-helical structure in osteocalcin. Biochemistry 21:2538–2547PubMedGoogle Scholar
  7. Hauschka PV, Wians FH Jr (1989) Osteocalcin-hydroxyapatite interaction in the extracellular organic matrix of bone. Anat Rec 224:180–188PubMedGoogle Scholar
  8. Hosoda K, Kanzaki S, Eguchi H, Kiyoki M, Yamaji T, Koshiharam Y, Shiraki M, Seino Y (1993) Secretion of osteocalcin and its propeptide from human osteoblastic cells: dissociation of the secretory patterns of osteocalcin and its propeptide. J Bone Miner Res 8:553–565PubMedGoogle Scholar
  9. Hunter GK, Hauschka PV, Poole AR, Rosenberg LC, Goldberg HA (1996) Nucleation and inhibition of hydroxyapatite formation by mineralized tissue proteins. Biochem J 317:59–64PubMedCentralPubMedGoogle Scholar
  10. Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C et al (2004) Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431:946–957PubMedGoogle Scholar
  11. Jie KSG, Gijsbers BLMG, Vermeer C (1995) A specific colorimetric staining method for γ-carboxyglutamic acid-containing proteins in polyacrylamide gels. Anal Biochem 224:163–165PubMedGoogle Scholar
  12. Karsenty M, Ferron G (2012) The contribution of bone to whole-organism physiology. Nature 481:314–320PubMedGoogle Scholar
  13. Laizé V, Viegas CSB, Price PA, Cancela ML (2006) Identification of an osteocalcin isoform in fish with a large acidic prodomain. J Biol Chem 281:15037–15043PubMedGoogle Scholar
  14. Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD, Confavreux C, Dacquin R, Mee PJ, McKee MD, Jung DY, Zhang Z, Kim JK, Mauvais-Jarvis F, Ducy P, Karsenty G (2007) Endocrine regulation of energy metabolism by the skeleton. Cell 130:456–469PubMedCentralPubMedGoogle Scholar
  15. Lie KK, Moren M (2012) Retinoic acid induces two osteocalcin isoforms and inhibits markers of osteoclast activity in Atlantic cod (Gadus morhua) ex vivo cultured craniofacial tissues. Comp Biochem Physiol A: Mol Integr Physiol 161:174–184Google Scholar
  16. Moghadam HK, Fergunson MM, Danzmann RG (2005) Evolution of Hox clusters in Salmonidae: a comparative analysis between Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss). J Mol Evol 61:636–649PubMedGoogle Scholar
  17. Nakayama K (1997) Furin: a mammalian subtilisin/Kex2p-like endoprotease involved in processing of a wide variety of precursor proteins. Biochem J 327:625–635PubMedCentralPubMedGoogle Scholar
  18. Poser JW, Price PA (1979) A method for decarboxylation of γ-carboxyglutamic acid in proteins. properties of the decarboxylated γ-carboxyglutamic acid protein from calf bone. J Biol Chem 254:431–436PubMedGoogle Scholar
  19. Renn J, Winkler C (2010) Characterization of collagen type 10a1 and osteocalcin in early and mature osteoblasts during skeleton formation in medaka. J Appl Ichthyol 26:196–201Google Scholar
  20. Simes DC, Williamson MK, Ortiz-Delgado JB, Viegas CSB, Price PA, Cancela ML (2003) Purification of matrix Gla protein (MGP) from a marine teleost fish, Argyrosomus regius: calcified cartilage and not bone as the primary site of MGP accumulation in fish. J Bone Miner Res 18:244–259PubMedGoogle Scholar
  21. Simes DC, Williamson MK, Schaff BJ, Gavaia PJ, Ingleton PM, Price PA, Cancela ML (2004) Characterization of osteocalcin (BGP) and matrix Gla protein (MGP) fish specific antibodies: validation for immunodetection studies in lower vertebrates. Calcif Tissue Int 74:170–180PubMedGoogle Scholar
  22. Sommer B, Bickel M, Hofstetter W, Wetterwald A (1996) Expression of matrix proteins during the development of mineralized tissues. Bone 19:371–380PubMedGoogle Scholar
  23. Viegas CSB, Simes DC, Laizé V, Williamson MK, Price PA, Cancela ML (2008) Gla-rich protein (GRP), a new vitamin K-dependent protein identified from sturgeon cartilage and highly conserved in vertebrates. J Biol Chem 283:36655–36664PubMedCentralPubMedGoogle Scholar
  24. Wajih N, Borras T, Xue W, Hutson SM, Wallin R (2004) Processing and transport of matrix γ-carboxyglutamic acid protein and bone morphogenetic protein-2 in cultured human vascular smooth muscle cells: evidence for an uptake mechanism for serum fetuin. J Biol Chem 279:43052–43060PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Sofia Cavaco
    • 1
    • 2
  • Matthew K. Williamson
    • 3
  • Joana Rosa
    • 1
    • 4
  • Vânia Roberto
    • 1
    • 4
  • Odete Cordeiro
    • 1
  • Paul A. Price
    • 3
  • M. Leonor Cancela
    • 1
    • 4
  • Vincent Laizé
    • 1
  • Dina C. Simes
    • 1
    • 2
    • 5
  1. 1.Centre of Marine Sciences (CCMAR/CIMAR-LA)University of AlgarveFaroPortugal
  2. 2.Faculty of Sciences and TechnologyUniversity of AlgarveFaroPortugal
  3. 3.Division of BiologyUniversity of California San DiegoLa JollaUSA
  4. 4.Department of Biomedical Sciences and MedicineUniversity of AlgarveFaroPortugal
  5. 5.GenoGla Diagnostics, CCMARUniversity of AlgarveFaroPortugal

Personalised recommendations