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Molecular evolution of SPARC: absence of the acidic module and expression in the endoderm of the starlet sea anemone, Nematostella vectensis

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Abstract

The matricellular glycoprotein SPARC is composed of three functional domains that are evolutionarily conserved in organisms ranging from nematodes to mammals: a Ca2+-binding glutamic acid-rich acidic domain at the N-terminus (domain I), a follistatin-like module (domain II), and an extracellular Ca2+-binding (EC) module that contains two EF-hands and two collagen-binding epitopes (domain III). We report that four SPARC orthologs (designated nvSPARC1-4) are expressed by the genome of the starlet anemone Nematostella vectensis, a diploblastic basal cnidarian composed of an ectoderm and endoderm separated by collagen-based mesoglea. We also report that domain I is absent from all N. vectensis SPARC orthologs. In situ hybridization data indicate that N. vectensis SPARC mRNAs are restricted to the endoderm during post-gastrula development. The absence of the Ca2+-binding N-terminal domain in cnidarians and conservation of collagen-binding epitopes suggests that SPARC first evolved as a collagen-binding matricellular glycoprotein, an interaction likely to be dependent on the binding of Ca2+-ions to the two EF-hands in the EC domain. We propose that further Ca2+-dependent activities emerged with the acquisition of an acidic N-terminal module in triplobastic organisms.

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References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    CAS  PubMed  Google Scholar 

  • Bassuk JA et al (2000) Induction of TGF-beta1 by the matricellular protein SPARC in a rat model of glomerulonephritis. Kidney Int 57:117–128

    Article  CAS  PubMed  Google Scholar 

  • Bradshaw AD (2009) The role of SPARC in extracellular matrix assembly. J Cell Commun Signal (in press) doi:10.1007/s12079/009-0062-6

  • Bradshaw AD, Sage EH (2001) SPARC, a matricellular protein that functions in cellular differentiation and tissue response to injury. J Clin Invest 107:1049–1054

    Article  CAS  PubMed  Google Scholar 

  • Brown TJ, Shaw PA, Karp X, Huynh MH, Begley H, Ringuette MJ (1999) Activation of SPARC expression in reactive stroma associated with human epithelial ovarian cancer. Gynecol Oncol 75:25–33

    Article  CAS  PubMed  Google Scholar 

  • Damjanovski S, Malaval L, Ringuette MJ (1994) Transient expression of SPARC in the dorsal axis of early Xenopus embryos: correlation with calcium-dependent adhesion and electrical coupling. Int J Dev Biol 38:439–446

    CAS  PubMed  Google Scholar 

  • Damjanovski S, Karp X, Funk S, Sage EH, Ringuette MJ (1997) Ectopic expression of SPARC in Xenopus embryos interferes with tissue morphogenesis: identification of a bioactive sequence in the C-terminal EF hand. J Histochem Cytochem 45:643–655

    CAS  PubMed  Google Scholar 

  • Damjanovski S, Huynh MH, Motamed K, Sage EH, Ringuette M (1998) Regulation of SPARC expression during early Xenopus development: evolutionary divergence and conservation of DNA regulatory elements between amphibians and mammals. Dev Genes Evol 207:453–461

    Article  CAS  PubMed  Google Scholar 

  • Darling JA et al (2005) Rising starlet: the starlet sea anemone, Nematostella vectensis. Bioessays 27:211–221

    Article  CAS  PubMed  Google Scholar 

  • Davis LE, Haynes JF (1968) An ultrastructural examination of the mesoglea of Hydra. Z Zellforsch Mikrosk Anat 92:149–158

    Article  CAS  PubMed  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Fitzgerald MC, Schwarzbauer JE (1998) Importance of the basement membrane protein SPARC for viability and fertility in Caenorhabditis elegans. Curr Biol 8:1285–1288

    Article  CAS  PubMed  Google Scholar 

  • Francki A, Bradshaw AD, Bassuk JA, Howe CC, Couser WG, Sage EH (1999) SPARC regulates the expression of collagen type I and transforming growth factor-beta1 in mesangial cells. J Biol Chem 274:32145–32152

    Article  CAS  PubMed  Google Scholar 

  • Gelman A, Rubin DB (1992) Inference from interative simulation using multiple sequences. Statistical Science 7:457–511

    Article  Google Scholar 

  • Giudici C et al (2008) Mapping of SPARC/BM-40/osteonectin-binding sites on fibrillar collagens. J Biol Chem 283:19551–19560

    Article  CAS  PubMed  Google Scholar 

  • Greiling TM, Stone B, Clark JI (2009) Absence of SPARC leads to impaired lens circulation. Exp Eye Res 89:416–425

    Article  CAS  PubMed  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Google Scholar 

  • Guindon S, Letheic F, Duroux P, Gascuel O (2005) PHYML Online - a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33:W557–559

    Google Scholar 

  • Hohenester E, Maurer P, Timpl R (1997) Crystal structure of a pair of follistatin-like and EF-hand calcium-binding domains in BM-40. EMBO J 16:3778–3786

    Article  CAS  PubMed  Google Scholar 

  • Hohenester E, Sasaki T, Giudici C, Farndale RW, Bachinger HP (2008) Structural basis of sequence-specific collagen recognition by SPARC. Proc Natl Acad Sci USA 105:18273–18277

    Article  CAS  PubMed  Google Scholar 

  • Hunter GK, Kyle CL, Goldberg HA (1994) Modulation of crystal formation by bone phosphoproteins: structural specificity of the osteopontin-mediated inhibition of hydroxyapatite formation. Biochem J 300(Pt 3):723–728

    CAS  PubMed  Google Scholar 

  • Huynh MH, Sage EH, Ringuette M (1999) A calcium-binding motif in SPARC/osteonectin inhibits chordomesoderm cell migration during Xenopus laevis gastrulation: evidence of counter-adhesive activity in vivo. Dev Growth Differ 41:407–418

    Article  CAS  PubMed  Google Scholar 

  • Johnston IG, Paladino T, Gurd JW, Brown IR (1990) Molecular cloning of SC1: a putative brain extracellular matrix glycoprotein showing partial similarity to osteonectin/BM40/SPARC. Neuron 4:165–176

    Article  CAS  PubMed  Google Scholar 

  • Kawasaki K, Weiss KM (2006) Evolutionary genetics of vertebrate tissue mineralization: the origin and evolution of the secretory calcium-binding phosphoprotein family. J Exp Zool B Mol Dev Evol 306:295–316

    Article  PubMed  Google Scholar 

  • Kawasaki K, Suzuki T, Weiss KM (2004) Genetic basis for the evolution of vertebrate mineralized tissue. Proc Natl Acad Sci USA 101:11356–11361

    Article  CAS  PubMed  Google Scholar 

  • Kawasaki K, Buchanan AV, Weiss KM (2007) Gene duplication and the evolution of vertebrate skeletal mineralization. Cells Tissues Organs 186:7–24

    Article  PubMed  Google Scholar 

  • Lane TF, Sage EH (1990) Functional mapping of SPARC: peptides from two distinct Ca+(+)-binding sites modulate cell shape. J Cell Biol 111:3065–3076

    Article  CAS  PubMed  Google Scholar 

  • Lane TF, Sage EH (1994) The biology of SPARC, a protein that modulates cell–matrix interactions. Faseb J 8:163–173

    CAS  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

  • Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25:1307–1320

    Article  CAS  PubMed  Google Scholar 

  • Martindale MQ (2005) The evolution of metazoan axial properties. Nat Rev Genet 6:917–927

    Article  CAS  PubMed  Google Scholar 

  • Martindale MQ, Pang K, Finnerty JR (2004) Investigating the origins of triploblasty: ‘mesodermal’ gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 131:2463–2474

    Article  CAS  PubMed  Google Scholar 

  • Martinek N, Zou R, Berg M, Sodek J, Ringuette M (2002) Evolutionary conservation and association of SPARC with the basal lamina in Drosophila. Dev Genes Evol 212:124–133

    Article  CAS  PubMed  Google Scholar 

  • Martinek N, Shahab J, Sodek J, Ringuette M (2007) Is SPARC an evolutionarily conserved collagen chaperone? J Dent Res 86:296–305

    Article  CAS  PubMed  Google Scholar 

  • Martinek N, Shahab J, Saathoff M, Ringuette M (2008) Haemocyte-derived SPARC is required for collagen-IV-dependent stability of basal laminae in Drosophila embryos. J Cell Sci 121:1671–1680

    Article  CAS  PubMed  Google Scholar 

  • Mason IJ, Murphy D, Munke M, Francke U, Elliott RW, Hogan BL (1986) Developmental and transformation-sensitive expression of the Sparc gene on mouse chromosome 11. EMBO J 5:1831–1837

    CAS  PubMed  Google Scholar 

  • Maurer P et al (1992) High-affinity and low-affinity calcium binding and stability of the multidomain extracellular 40-kDa basement membrane glycoprotein (BM-40/SPARC/osteonectin). Eur J Biochem 205:233–240

    Article  CAS  PubMed  Google Scholar 

  • Maurer P, Hohenadl C, Hohenester E, Gohring W, Timpl R, Engel J (1995) The C-terminal portion of BM-40 (SPARC/osteonectin) is an autonomously folding and crystallisable domain that binds calcium and collagen IV. J Mol Biol 253:347–357

    Article  CAS  PubMed  Google Scholar 

  • Midwood KS, Williams LV, Schwarzbauer JE (2004) Tissue repair and the dynamics of the extracellular matrix. Int J Biochem Cell Biol 36:1031–1037

    Article  CAS  PubMed  Google Scholar 

  • Motamed K, Funk SE, Koyama H, Ross R, Raines EW, Sage EH (2002) Inhibition of PDGF-stimulated and matrix-mediated proliferation of human vascular smooth muscle cells by SPARC is independent of changes in cell shape or cyclin-dependent kinase inhibitors. J Cell Biochem 84:759–771

    Article  PubMed  Google Scholar 

  • Motamed K et al (2003) Fibroblast growth factor receptor-1 mediates the inhibition of endothelial cell proliferation and the promotion of skeletal myoblast differentiation by SPARC: a role for protein kinase A. J Cell Biochem 90:408–423

    Article  CAS  PubMed  Google Scholar 

  • Nie J et al (2008) IFATS collection: combinatorial peptides identify alpha5beta1 integrin as a receptor for the matricellular protein SPARC on adipose stromal cells. Stem Cells 26:2735–2745

    Article  CAS  PubMed  Google Scholar 

  • Norose K et al (1998) SPARC deficiency leads to early-onset cataractogenesis. Invest Ophthalmol Vis Sci 39:2674–2680

    CAS  PubMed  Google Scholar 

  • Novinec M, Kordis D, Turk V, Lenarcic B (2006) Diversity and evolution of the thyroglobulin type-1 domain superfamily. Mol Biol Evol 23:744–755

    Article  CAS  PubMed  Google Scholar 

  • Pottgiesser J et al (1994) Changes in calcium and collagen IV binding caused by mutations in the EF hand and other domains of extracellular matrix protein BM-40 (SPARC, osteonectin). J Mol Biol 238:563–574

    Article  CAS  PubMed  Google Scholar 

  • Putnam NH et al (2007) Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317:86–94

    Article  CAS  PubMed  Google Scholar 

  • Rentz TJ, Poobalarahi F, Bornstein P, Sage EH, Bradshaw AD (2007) SPARC regulates processing of procollagen I and collagen fibrillogenesis in dermal fibroblasts. J Biol Chem 282:22062–22071

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Sasaki T et al (1997) Limited cleavage of extracellular matrix protein BM-40 by matrix metalloproteinases increases its affinity for collagens. J Biol Chem 272:9237–9243

    Article  CAS  PubMed  Google Scholar 

  • Sasaki T, Hohenester E, Gohring W, Timpl R (1998) Crystal structure and mapping by site-directed mutagenesis of the collagen-binding epitope of an activated form of BM-40/SPARC/osteonectin. EMBO J 17:1625–1634

    Article  CAS  PubMed  Google Scholar 

  • Schmid V, Ono SI, Reber-Muller S (1999) Cell–substrate interactions in cnidaria. Microsc Res Tech 44:254–268

    Article  CAS  PubMed  Google Scholar 

  • Schwarzbauer JE, Spencer CS (1993) The Caenorhabditis elegans homologue of the extracellular calcium binding protein SPARC/osteonectin affects nematode body morphology and mobility. Mol Biol Cell 4:941–952

    CAS  PubMed  Google Scholar 

  • Schwarzbauer JE, Musset-Bilal F, Ryan CS (1994) Extracellular calcium-binding protein SPARC/osteonectin in Caenorhabditis elegans. Methods Enzymol 245:257–270

    Article  CAS  PubMed  Google Scholar 

  • Sodek KL et al (2008) Identification of pathways associated with invasive behavior by ovarian cancer cells using multidimensional protein identification technology (MudPIT). Mol Biosyst 4:762–773

    Article  CAS  PubMed  Google Scholar 

  • Tai IT, Tang MJ (2008) SPARC in cancer biology: its role in cancer progression and potential for therapy. Drug Resist Updat 11:231–246

    Article  CAS  PubMed  Google Scholar 

  • Termine JD, Kleinman HK, Whitson SW, Conn KM, McGarvey ML, Martin GR (1981) Osteonectin, a bone-specific protein linking mineral to collagen. Cell 26:99–105

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) ClustalW: 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

    Google Scholar 

  • Vannahme C et al (1999) Molecular cloning of testican-2: defining a novel calcium-binding proteoglycan family expressed in brain. J Neurochem 73:12–20

    Article  CAS  PubMed  Google Scholar 

  • Vannahme C et al (2002) Characterization of SMOC-1, a novel modular calcium-binding protein in basement membranes. J Biol Chem 277:37977–37986

    Article  CAS  PubMed  Google Scholar 

  • Vannahme C, Gosling S, Paulsson M, Maurer P, Hartmann U (2003) Characterization of SMOC-2, a modular extracellular calcium-binding protein. Biochem J 373:805–814

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by Discovery grants to B.C., M.R., S.D., and U.T. from National Sciences and Research Council of Canada and an Early Researcher Award to B.C.

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Correspondence to Maurice Ringuette.

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Communicated by M.Q. Martindale

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Koehler, A., Desser, S., Chang, B. et al. Molecular evolution of SPARC: absence of the acidic module and expression in the endoderm of the starlet sea anemone, Nematostella vectensis . Dev Genes Evol 219, 509–521 (2009). https://doi.org/10.1007/s00427-009-0313-9

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