Abstract
BM-40 is an extracellular matrix-associated protein and is characterized by an extracellular calcium-binding domain as well as a follistatin-like domain. Secreted modular calcium-binding protein-1 (SMOC-1) is a new member of the BM-40 family. It consists of two thyroglobulin-like domains, a follistatin-like domain and a new domain without known homologues and is expressed ubiquitously in many adult murine tissues. Immunofluorescence studies, as well as immunogold electron microscopy, have confirmed the localization of SMOC-1 in or around basement membranes of adult murine skin, blood vessels, brain, kidney, skeletal muscle, and the zona pellucida surrounding the oocyte. In the present work, light microscopic immunohistochemistry has revealed that SMOC-1 is localized in the early mouse embryo day 7 throughout the entire endodermal basement membrane zone of the embryo proper. SMOC-1 mRNA is synthesized, even in early stages of mouse development, by mesenchymal as well as epithelial cells deriving from all three germ layers. In embryonic stage day 12, and fetal stages day 14, 16, and 18, the protein is present in the basement membrane zones of brain, blood vessels, skin, skeletal muscle, lung, heart, liver, pancreas, intestine, and kidney. This broad and organ-specific distribution suggests multifunctional roles of SMOC-1 during mouse embryogenesis.
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Alliel PM, Perin JP, Jolles P, Bonnet FJ (1993) Testican, a multidomain testicular proteoglycan resembling modulators of cell social behaviour. Eur J Biochem 214:347–350
Basu A, Kligman LH, Samulewicz SJ, Howe CC (2000) Impaired wound healing in mice deficient in a matricellular protein SPARC (osteonectin, BM-40). BMC Cell Biol 2:15
Bornstein P (1995) Diversity of function is inherent in matricellular proteins: an appraisal of thrombospondin 1. J Cell Biol 130:503–506
Bornstein P, Sage EH (2002) Matricellular proteins: extracellular modulators of cell function. Curr Opin Cell Biol 14:608–616
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
Bradshaw AD, Reed MJ, Sage EH (2002a) SPARC-null mice exhibit accelerated cutaneous wound closure. J Histochem Cytochem 50:1–10
Bradshaw AD, Reed MJ, Sage EH (2002b) SPARC-null mice display enhanced fibrovascular invasion of subcutaneous sponge implants. Wound Repair Regen 9:522–530
Brekken RA, Sage EH (2000) SPARC, a matricellular protein: at the crossroads of cell-matrix communication. Matrix Biol 19:816–827
Brekken RA, Sullivan MM, Workman G, Bradshaw AD, Carbon J, Siadak A, Murri C, Framson PE, Sage EH (2004) Expression and characterization of murine hevon (SC1), a member of the SPARC family of matricellular proteins. J Histochem Cytochem 52:735–748
Clezardin P, Malaval L, Ehrensperger A, Delmas PD, Dechavanni M, McGregor J (1988) Complex formation of human thrombospondin with osteonectin. Eur J Biochem 175:275–284
Crawford SE, Stellbach V, Murphy-Ullrich JE, Ribeiro SMF, Lawler J, Hynes RO, Boivin GP, Bouck N (1998) Thrombospondin-1 is a major activator of TGF-β1 in vivo. Cell 93:1159–1170
Delany AM, Amling M, Priemel M, Howe C, Baron R, Canalis E (2000) Osteopenia and decreased bone formation in osteonectin-deficient mice. J Clin Invest 105:915–923
Dziadek M, Paulsson M, Aumailley M, Timpl R (1986) Purification and tissue distribution of a small protein (BM-40) extracted from a basement membrane tumor. Eur J Biochem 161:455–464
Gersdorff N, Kohfeldt E, Sasaki T, Timpl R, Miosge N (2005) Laminin γ3 chain binds to nidogen and is located in murine basement membranes. J Biol Chem 280:22146–22153
Gilmour DT, Lyon GJ, Carlton MBL, Sanes JR, Cunningham JM, Anderson JR, Hogan BLM, Evans MJ, Colledge WH (1998) Mice deficient for the secreted glycoprotein SPARC/osteonectin/BM40 develop normally but show severe age-onset cataract formation and disruption of the lens. EMBO J 17:1860–1870
Girard JP, Springer TA (1996) Modulation of endothelial cell adhesion by hevin, an acidic protein associated with high endothelial venules. J Biol Chem 271:4511–4517
Guermah M, Cristanti P, Laugier D, Dezelee P, Bidou L, Pessac B, Calothy G (1991) Transcription of a quail gene expressed in embryonic retinal cells is shut off sharply at hatching. Proc Natl Acad Sci USA 88:4503–4507
Hartmann U, Maurer P (2001) Proteoglycans in the nervous system—the quest for functional roles in vivo. Matrix Biol 20:23–35
Hohenester E, Maurer P, Hohenadl C, Timpl R, Jansonius JN, Engel J (1996) Structure of a novel extracellular Ca(2+)-binding module in BM-40. Nat Struct Biol 3:67–73
Johnston IG, Paladino T, Gurd JW, Brown IR (1990) Molecular cloning of SC1: a putative brain extracellular matrix glycoprotein showing partial similarity to osteonectin/BM-40/SPARC. Neuron 4:165–176
Kupprion C, Motamed K, Sage EH (1998) SPARC (BM-40, osteonectin) inhibits the mitogenic effect of vascular endothelial growth factor on microvascular endothelial cells. J Biol Chem 273:29635–29640
Lane TF, Iruela-Arispe ML, Sage EH (1992) Regulation of gene expression by SPARC during angiogenesis in vitro. Changes in fibronectin, thrombospondin-1, and plasminogen activator inhibitor-1. J Biol Chem 267:16736–16745
Lane TF, Sage EH (1994) The biology of SPARC, a protein that modulates cell-matrix interactions. FASEB J 8:163–173
Mason IJ, Taylor A, Williams JG, Sage EH, Hogan BLM (1986) Evidence from molecular cloning that SPARC, a major product of mouse embryo parietal endoderm, is related to an endothelial cell “culture shock” glycoprotein of M r=43,000. EMBO J 5:1465–1472
Maurer P, Hohenadl C, Hohenester E, Göhring W, Timpl R, Engel J (1995) The c-terminal portion of BM-40 (SPARC/Osteonectin) is autonomously folding and crystallisable domain that binds calcium and collagen IV. J Mol Biol 253:347–357
Mendis DB, Brown IR (1994) Expression of the gene encoding the extracellular matrix glycoprotein SPARC in the developing and adult mouse brain. Brain Res Mol Brain Res 24:11–19
Norose K, Clark JI, Sved NA, Basu A, Heber-Katz E, Sage EH, Howe CC (1998) SPARC deficiency leads to early-onset cataractogenesis. Invest Ophthalmol Vis Sci 39:2674–2680
Norose K, Lo WK, Clark JI, Sage EH, Howe CC (2000) Lenses of SPARC-null mice exhibit an abnormal cell surface-basement membrane interface. Exp Eye Res 71:295–307
Raines EW, Lane TF, Iruela-Arispe ML, Ross R, Sage EH (1992) The extracellular glycoprotein SPARC interacts with platelet derived growth factor PDGF-AB and BB and inhibits the binding of PDGF to its receptors. Proc Natl Acad Sci USA 89:1281–1285
Sasaki T, Hohenester E, Göhring 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
Savani RC, Zhou Z, Arguiri E, Wang S, Vu D, Howe CC, DeLisser HM (2000) Bleomycin-induced pulmonary injury in mice deficient in SPARC. Am J Physiol 279:743–750
Schnepp A, Lindgren PK, Hülsmann H, Kröger S, Paulsson M, Hartmann U (2005) Mouse testican-2: expression, glycosylation, and effects on neurite outgrowth. J Biol Chem 280:11274–11280
Shibanuma M, Mashimo J, Mita A, Kuroki T, Nose K (1993) Cloning from a mouse osteoblastic cell line of a set of transforming-growth-factor-beta 1-regulated genes, one of which seems to encode a follistatin-related polypeptide. Eur J Biochem 217:13–19
Strandjord TP, Madtes DK, Weiss DJ, Sage EH (1999) Collagen accumulation is decreased in SPARC-null mice with bleomycin-induced pulmonary fibrosis. Am J Physiol 277:628–635
Termine JD, Kleinmann HK, Whitson SW, Conn KM, McGarvey ML, Martin GR (1981) Osteonectin, a bone-specific protein linking mineral to collagen. Cell 26:99–105
Tesche F, Miosge N (2004) Perlecan in late stages of osteoarthritis of the human knee joint. Osteoarthritis Cartil 12:852–862
Theiler K (1989) The house mouse, 2nd edn. Springer, Berlin Heidelberg New York
Vannahme C, Schübel S, Herud M, Gösling S, Hülsmann H, Paulsson M, Hartmann U, Maurer P (1999) Molecular cloning of testican-2: defining a novel calcium-binding proteoglycan family expressed in Brain. J Neurochem 73:12–20
Vannahme C, Smyth N, Miosge N, Gösling S, Frie C, Paulsson M, Maurer P, Hartmann U (2002) Characterization of SMOC-1, a novel modular calcium-binding protein in basement membranes. J Biol Chem 277:37977–37986
Vanna hme C, Gösling S, Paulsson M, Maurer P, Hartmann U (2003) Characterization of SMOC-2, a modular extracellular calcium-binding protein. Biochem J 373:805–814
Acknowledgments
We would like to thank Mats Paulsson, Institute for Biochemistry, University of Cologne, for the antibodies. We would also like to thank Christina Zelent for technical assistance and Cyrilla Maelicke B.Sc. for editing the manuscript. Parts of the work were taken from the doctoral thesis of Antje Schall.
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Gersdorff, N., Müller, M., Schall, A. et al. Secreted modular calcium-binding protein-1 localization during mouse embryogenesis. Histochem Cell Biol 126, 705–712 (2006). https://doi.org/10.1007/s00418-006-0200-7
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DOI: https://doi.org/10.1007/s00418-006-0200-7