Skip to main content
Log in

Phylogenetic analysis and expression patterns of p16 and p19 in Paracentrotus lividus embryos

  • Sequence Corner
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

Abstract

P16 and P19 are two small acidic proteins involved in the formation of the biomineralized skeleton of sea urchin embryos and adults. Here, we describe the cloning and the embryonic temporal and spatial expression profiles of p16 and p19 mRNAs, identified for the first time in Paracentrotus lividus. Phylogenetic analysis showed a high degree of similarity of the deduced Pl-P16 and Pl-P19 sequences with the Lytechinus variegatus and Strongylocentrotus purpuratus orthologs. While only a reduced similarity with other phyla, including mammals, was detected, their implication in biomineralized tissues calls for their conservation in evolution. By comparative quantitative PCR and in situ hybridization, we found that Pl-p16 and Pl-p19 expression was restricted to skeletogenic cells throughout embryogenesis, with transcript levels peaking at the late gastrula stage. Dissimilar Pl-p16 and Pl-p19 spatial expression within the primary mesenchyme cell syncytium at the gastrula and pluteus stages suggests the occurrence of a different regulation of gene transcription.

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

References

  • Addadi L, Weiner S (1985) Interactions between acidic proteins and crystals: stereochemical requirements in biomineralization. Proc Natl Acad Sci U S A 82:4110–4114

    Article  PubMed  CAS  Google Scholar 

  • Addadi L, Berman A, Oldak JM, Weiner S (1989) Structural and stereochemical relations between acidic macromolecules of organic matrices and crystals. Connect Tissue Res 21:127–134

    Article  PubMed  CAS  Google Scholar 

  • Alvares K, Dixit SN, Lux E, Veis A (2009) Echinoderm phosphorylated matrix proteins UTMP16 and UTMP19 have different functions in sea urchin. J Biol Chem 284:26149–26160

    Article  PubMed  CAS  Google Scholar 

  • Cheers MS, Ettensohn CA (2005) P16 is an essential regulator of skeletogenesis in the sea urchin embryo. Dev Biol 283:384–396

    Article  PubMed  CAS  Google Scholar 

  • Chu X, Jiang W, Zhang Z, Yan Y, Pan H, Xu X, Tang R (2011) Unique roles of acidic amino acids in phase transformation of calcium phosphates. J Phys Chem B 115:1151–1157

    Article  PubMed  CAS  Google Scholar 

  • Costa C, Cavalcante C, Zito F, Yokota Y, Matranga V (2010) Phylogenetic analysis and homology modelling of Paracentrotus lividus nectin. Mol Divers 14:653–665

    Article  PubMed  CAS  Google Scholar 

  • Fu G, Valiyaveettil S, Wopenka B, Morse DE (2005) CaCO3 biomineralization: acidic 8-kDa proteins isolated from aragonitic abalone shell nacre can specifically modify calcite crystal morphology. Biomacromolecules 6:1289–1298

    Article  PubMed  CAS  Google Scholar 

  • Gericke A, Qin C, Sun Y, Redfern R, Redfern D, Fujimoto Y, Taleb H, Butler WT, Boskey AL (2010) Different forms of DMP1 play distinct roles in mineralization. J Dent Res 89:355–359

    Article  PubMed  CAS  Google Scholar 

  • Hodor PG, Ettensohn CA (1998) The dynamics and regulation of mesenchymal cell fusion in the sea urchin embryo. Dev Biol 199:111–124

    Article  PubMed  CAS  Google Scholar 

  • Illies MR, Peeler MT, Dechtiaruk AM, Ettensohn CA (2002) Identification and developmental expression of new biomineralization proteins in the sea urchin Strongylocentrotus purpuratus. Dev Genes Evol 212:419–431

    Article  PubMed  CAS  Google Scholar 

  • Kiyomoto M, Zito F, Costa C, Poma V, Sciarrino S, Matranga V (2007) Skeletogenesis by transfated secondary mesenchyme cells is dependent on extracellular matrix-ectoderm interactions in Paracentrotus lividus sea urchin embryos. Dev Growth Differ 49:731–741

    Article  PubMed  CAS  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)) Methods 25:402–408

    Google Scholar 

  • Livingston BT, Killian CE, Wilt F, Cameron A, Landrum MJ, Ermolaeva O, Sapojnikov V, Maglott DR, Buchanan AM, Ettensohn CA (2006) A genome-wide analysis of biomineralization-related proteins in the sea urchin Strongylocentrotus purpuratus. Dev Biol 300:335–348

    Article  PubMed  CAS  Google Scholar 

  • MacDougall M, Gu TT, Luan X, Simmons D, Chen J (1998) Identification of a novel isoform of mouse dentin matrix protein: spatial expression in mineralized tissues. J Bone Miner Res 13:422–431

    Article  PubMed  CAS  Google Scholar 

  • Mann K, Wilt FH, Poustka AJ (2010) Proteomic analysis of sea urchin (Strongylocentrotus purpuratus) spicule matrix. Proteome Sci 8:33

    Article  PubMed  Google Scholar 

  • Marin F, Luquet G (2008) Unusually acidic proteins in biomineralization. In: Bäuerlein E (ed) Handbook of biomineralization: biological aspects and structure formation. Wiley, Weinheim. doi:10.1002/9783527619443.ch16

  • Matranga V, Bonaventura R, Costa C, Karakostis K, Pinsino A, Russo R, Zito F (2011) Echinoderms as blueprints for biocalcification: regulation of skeletogenic genes and matrices. Prog Mol Subcell Biol 52:225–248

    Article  PubMed  Google Scholar 

  • Okazaki K (1965) Skeleton formation of sea urchin larvae. V. Continuous observation of the process of matrix formation. Exp Cell Res 40:585–596

    Article  PubMed  CAS  Google Scholar 

  • Prasad M, Butler WT, Qin C (2010) Dentin sialophosphoprotein in biomineralization. Connect Tissue Res 51:404–417

    Article  PubMed  CAS  Google Scholar 

  • Qin C, D’Souza R, Feng JQ (2007) Dentin matrix protein 1 (DMP1): new and important roles for biomineralization and phosphate homeostasis. J Dent Res 86:1134–1141

    Article  PubMed  CAS  Google Scholar 

  • Rizzo F, Fernandez-Serra M, Squarzoni P, Archimandritis A, Arnone MI (2006) Identification and developmental expression of the ets gene family in the sea urchin (Strongylocentrotus purpuratus). Dev Biol 300:35–48

    Article  PubMed  CAS  Google Scholar 

  • Sea Urchin Genome Sequencing Consortium (2006) The genome of the sea urchin Strongylocentrotus purpuratus. Science 314:941–952

    Article  Google Scholar 

  • Veis A, Sabsay B, Wu CB (1991) Phosphoproteins as mediators of biomineralization. In: Comstock J (ed) Surface reactive peptides and polymers. ACS Symp Ser 444:1–12

    Article  CAS  Google Scholar 

  • Wang DG, Britten RJ, Davidson EH (1995) Maternal and embryonic provenance of a sea urchin embryo transcription factor, SpZ12-1. Mol Mar Biol Biotechnol 4:148–153

    PubMed  CAS  Google Scholar 

  • Weiner S, Addadi L (2011) Crystallization pathways in biomineralization. Annu Rev Mater Res 41:21–40

    Article  CAS  Google Scholar 

  • Wilt FH (2005) Developmental biology meets materials science: morphogenesis of biomineralized structures. Dev Biol 280:15–25

    Article  PubMed  CAS  Google Scholar 

  • Wojtas M, Dobryszycki P, Ożyhar A (2012) Intrinsically disordered proteins in biomineralization. In: Seto J (ed) Advanced topics in biomineralization. Intech, pp 1–32. ISBN: 978-953-51-0045-4

  • Zhu X, Mahairas G, Illies M, Cameron RA, Davidson EH, Ettensohn CA (2001) A large-scale analysis of mRNAs expressed by primary mesenchyme cells of the sea urchin embryo. Development 128:2615–2627

    PubMed  Google Scholar 

  • Zito F, Matranga V (2009) Secondary mesenchyme cells as potential stem cells of the sea urchin embryo. Stem cells in marine organisms, 187–213. doi:10.1007/978-90-481-2767-2_8

Download references

Acknowledgments

This work has been fully supported by the EU-ITN BIOMINTEC Project, contract number 215507 to V. Matranga. Authors are indebted to Prof. Dr. W. E. G. Mueller and Prof. Dr. H. C. Shroeder, providing BIOMINTEC coordination at the Johannes Gutenberg University, Mainz (see http://www.biomintec.de/), for their stimulating suggestions and continuous encouragement. The first author, K. Karakostis, has been the recipient of a Marie Curie ITN program fellowship in the frame of the above mentioned project.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Valeria Matranga.

Additional information

Communicated by H. Nishida

Caterina Costa and Konstantinos Karakostis contributed equally to the work and should be considered co-first authors.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Costa, C., Karakostis, K., Zito, F. et al. Phylogenetic analysis and expression patterns of p16 and p19 in Paracentrotus lividus embryos. Dev Genes Evol 222, 245–251 (2012). https://doi.org/10.1007/s00427-012-0405-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-012-0405-9

Keywords

Navigation