Skip to main content
SpringerLink
Log in

Evolution and Function of SPARC and Tenascins: Matricellular Counter-Adhesive Glycoproteins with Pleiotropic Effects on Angiogenesis and Tissue Fibrosis

  • Chapter
  • First Online:
Evolution of Extracellular Matrix

Part of the book series: Biology of Extracellular Matrix ((BEM))

Abstract

The evolution of multicellular organisms composed of tissues with distinct morphologies and physiological functions has involved the appearance of novel genes coding for extracellular matrix (ECM) molecules. The ECM consists of four major classes of proteins: collagens, proteoglycans, non-collagenous structural proteins, and glycoproteins. Our knowledge of how these molecules act in concert to assemble intricate networks that provide tissues with their unique design, biomechanical properties, and stability has advanced rapidly over the last three decades. Although the ECM was first perceived to be an inert scaffold, it is now common knowledge that ECM components have dynamic and complex activities that affect all cellular activities. The focus of this chapter is on the tenascin family and Secreted Protein, Acidic, Rich in Cysteine, which are members of the “matricellular” subset of ECM glycoproteins. In contrast to polymer-forming pro-adhesive glycoproteins, such as fibronectin and laminins, these glycoproteins are not integrated into ECM scaffolds but, rather, exist as transient, diffusible, components of interstitial matrices and basement membranes.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ballard VL, Sharma A, Duignan I, Holm JM, Chin A, Choi R, Hajjar KA, Wong S-C, Edelberg JM (2006) Vascular tenascin-C regulates cardiac endothelial phenotype and neovascularization. FASEB J 20(6):717–719

    PubMed  CAS  Google Scholar 

  • Barker TH, Baneyx G, Cardó-Vila M, Workman GA, Weaver M, Menon PM, Dedhar S, Rempel SA, Arap W, Pasqualini R, Vogel V, Sage EH (2005a) SPARC regulates extracellular matrix organization through its modulation of integrin-linked kinase activity. J Biol Chem 280(43): 36483–36493

    PubMed  CAS  Google Scholar 

  • Barker TH, Framson P, Puolakkainen PA, Reed M, Funk SE, Sage EH (2005b) Matricellular homologs in the foreign body response: hevin suppresses inflammation, but hevin and SPARC together diminish angiogenesis. Am J Pathol 166(3):923–933

    PubMed  CAS  Google Scholar 

  • Bassuk JA, Pichler R, Rothmier JD, Pippen J, Gordon K, Meek RL, Bradshaw AD, Lombardi D, Strandjord TP, Reed M, Sage EH, Couser WG, Johnson R (2000) Induction of TGF-[bgr]1 by the matricellular protein SPARC in a rat model of glomerulonephritis. Kidney Int 57(1): 117–128

    PubMed  CAS  Google Scholar 

  • Basu A, Kligman L, Samulewicz S, Howe C (2001) Impaired wound healing in mice deficient in a matricellular protein SPARC (osteonectin, BM-40). BMC Cell Biol 2(1):15

    PubMed  CAS  Google Scholar 

  • Battegay EJ, Rupp J, Iruela-Arispe L, Sage EH, Pech M (1994) PDGF-BB modulates endothelial proliferation and angiogenesis in vitro via PDGF beta-receptors. J Cell Biol 125(4): 917–928

    PubMed  CAS  Google Scholar 

  • Bhoopathi P, Chetty C, Gujrati M, Dinh DH, Rao JS, Lakka SS (2010) The role of MMP-9 in the anti-angiogenic effect of secreted protein acidic and rich in cysteine. Br J Cancer 102(3): 530–540

    PubMed  CAS  Google Scholar 

  • Bjarnegård M, Enge M, Norlin J, Gustafsdottir S, Fredriksson S, Abramsson A, Takemoto M, Gustafsson E, Fässler R, Betsholtz C (2004) Endothelium-specific ablation of PDGFB leads to pericyte loss and glomerular, cardiac and placental abnormalities. Development 131(8): 1847–1857

    PubMed  Google Scholar 

  • Blazejewski SLBB, Boussarie L, Blanc JF, Malaval L, Okubo K, Saric J, Bioulac-Sage P, Rosenbaum J (1997) Osteonectin (SPARC) expression in human liver and in cultured human liver myofibroblasts. Am J Pathol 151(3):651–657

    PubMed  CAS  Google Scholar 

  • Borsi L, Balza E, Castellani P, Carnemolla B, Ponassi M, Querzé G, Zardi L (1994) Cell-cycle dependent alternative splicing of the tenascin primary transcript. Cell Commun Adhes 1(4): 307–317

    CAS  Google Scholar 

  • Borsi L, Balza E, Gaggero B, Allemanni G, Zardi L (1995) The alternative splicing pattern of the tenascin-C pre-mRNA is controlled by the extracellular pH. J Biol Chem 270(11): 6243–6245

    PubMed  CAS  Google Scholar 

  • Boutet I, Jollivet D, Shillito B, Moraga D, Tanguy A (2009) Molecular identification of differentially regulated genes in the hydrothermal-vent species Bathymodiolus thermophilus and Paralvinella pandorae in response to temperature. BMC Genomics 10(1):222

    PubMed  Google Scholar 

  • Bradshaw A (2009) The role of SPARC in extracellular matrix assembly. J Cell Commun Signal 3(3–4):239–246

    PubMed  Google Scholar 

  • Bradshaw AD, Reed MJ, Carbon JG, Pinney E, Brekken RA, Sage EH (2001) Increased fibrovascular invasion of subcutaneous polyvinyl alcohol sponges in SPARC-null mice. Wound Repair Regen 9(6):522–530

    PubMed  CAS  Google Scholar 

  • Bradshaw AD, Puolakkainen P, Dasgupta J, Davidson JM, Wight TN, Sage EH (2003) SPARC-null mice display abnormalities in the dermis characterized by decreased collagen fibril diameter and reduced tensile strength. J Invest Dermatol 120(6):949–955

    PubMed  CAS  Google Scholar 

  • Brekken RA, Sage EH (2000) SPARC, a matricellular protein: at the crossroads of cell–matrix. Matrix Biol 19(7):569–580

    PubMed  CAS  Google Scholar 

  • Brellier F, Hostettler K, Hotz H-R, Ozcakir C, Çöloğlu SA, Togbe D, Ryffel B, Roth M, Chiquet-Ehrismann R (2011) Tenascin-C triggers fibrin accumulation by downregulation of tissue plasminogen activator. FEBS Lett 585(6):913–920

    PubMed  CAS  Google Scholar 

  • Brellier FME, Chiquet M, Ferralli J, van der Heyden M, Orend G, Schittny JC, Chiquet-Ehrismann R, Tucker RP (2012) The adhesion modulating properties of tenascin-W. Int J Biol Sci 8(2): 187–194

    PubMed  CAS  Google Scholar 

  • Bristow J, Tee M, Gitelman S, Mellon S, Miller W (1993) Tenascin-X: a novel extracellular matrix protein encoded by the human XB gene overlapping P450c21B. J Cell Biol 122(1):265–278

    PubMed  CAS  Google Scholar 

  • Busch E, Hohenester E, Timpl R, Paulsson M, Maurer P (2000) Calcium affinity, cooperativity, and domain interactions of extracellular EF-hands present in BM-40. J Biol Chem 275(33): 25508–25515

    PubMed  CAS  Google Scholar 

  • Cao Y (2009) Positive and negative modulation of angiogenesis by VEGFR1 ligands. Sci Signal 2(59):re1

    PubMed  Google Scholar 

  • Carey WA, Taylor GD, Dean WB, Bristow JD (2010) Tenascin-C deficiency attenuates TGF-β-mediated fibrosis following murine lung injury. Am J Physiol Lung Cell Mol Physiol 299(6):L785–L793

    PubMed  CAS  Google Scholar 

  • Chavez-Muñoz C, Hartwell R, Jalili RB, Jafarnejad M, Lai A, Nabai L, Ghaffari A, Hojabrpour P, Kanaan N, Duronio V, Guns E, Cherkasov A, Ghahary A (2012) SPARC/SFN interaction, suppresses type I collagen in dermal fibroblasts. J Cell Biochem 113(8):2622–2632

    PubMed  Google Scholar 

  • Chiquet-Ehrismann R (1990) What distinguishes tenascin from fibronectin? FASEB J 4(9): 2598–2604

    PubMed  CAS  Google Scholar 

  • Chiquet-Ehrismann R, Tucker, RP (2011) Tenascins and the importance of adhesion modulation. Cold Spring Harb Perspect Biol 3(5):pii: a004960

    Google Scholar 

  • Chiquet-Ehrismann R, Mackie EJ, Pearson CA, Sakakura T (1986) Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell 47(1):131–139

    PubMed  CAS  Google Scholar 

  • Chlenski A, Guerrero L, Peddinti R, Spitz J, Leonhardt P, Yang Q, Tian Y, Salwen H, Cohn S (2010) Anti-angiogenic SPARC peptides inhibit progression of neuroblastoma tumors. Mol Cancer 9(1):138

    PubMed  Google Scholar 

  • Clark MS, Thorne MAS, Reinhardt R, Drungowski M, Albrecht MW, Klages S, Beck A, Kube M, Lubzens E (2012) Long-term survival of hydrated resting eggs from Brachionus plicatilis. PLoS One 7(1):e29365

    PubMed  CAS  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(3):439–446

    PubMed  CAS  Google Scholar 

  • Degen M, Brellier F, Kain R, Ruiz C, Terracciano L, Orend G, Chiquet-Ehrismann R (2007) Tenascin-W is a novel marker for activated tumor stroma in low-grade human breast cancer and influences cell behavior. Cancer Res 67(19):9169–9179

    PubMed  CAS  Google Scholar 

  • Derr LB, Chiquet-Ehrismann R, Gandour-Edwards R, Spence J, Tucker RP (1997) The expression of tenascin-C with the AD1 variable repeat in embryonic tissues, cell lines and tumors in various vertebrate species. Differentiation 62(2):71–82

    PubMed  CAS  Google Scholar 

  • Desmoulière A, Guyot C, Gabbiani G (2004) The stroma reaction myofibroblast: a key player in the control of tumor cell behavior. Int J Dev Biol 48:509–517

    PubMed  Google Scholar 

  • Doolittle RF (1984) Fibrinogen and fibrin. Annu Rev Biochem 53(1):195–229

    PubMed  CAS  Google Scholar 

  • Dorries U, Schachner M (1994) Tenascin mRNA isoforms in the developing mouse brain. J Neurosci Res 37(3):336–347

    PubMed  CAS  Google Scholar 

  • Erickson H, Inglesias JL (1984) A six-armed oligomer isolated from cell surface fibronectin preparations. Nature 311(5983):267–269

    PubMed  CAS  Google Scholar 

  • Fischer D, Chiquet-Ehrismann R, Bernasconi C, Chiquet M (1995) A single heparin binding region within the fibrinogen-like domain is functional in chick tenascin-C. J Biol Chem 270(7): 3378–3384

    PubMed  CAS  Google Scholar 

  • Fischer D, Tucker RP, Chiquet-Ehrismann R, Adams JC (1997) Cell-adhesive responses to tenascin-C splice variants involve formation of fascin microspikes. Mol Biol Cell 8(10): 2055–2075

    PubMed  CAS  Google Scholar 

  • Fitzgerald MC, Schwarzbauer JE (1998) Importance of the basement membrane protein SPARC for viability and fertility in Caenorhabditis elegans. Curr Biol 8(23):1285–1288

    PubMed  CAS  Google Scholar 

  • Ford R, Wang G, Jannati P, Adler D, Racanelli P, Higgins PJ, Staiano-Coico L (1993) Modulation of SPARC expression during butyrate-induced terminal differentiation of cultured human keratinocytes: regulation via a TGF-β-dependent pathway. Exp Cell Res 206(2):261–275

    PubMed  CAS  Google Scholar 

  • Francki A, Sage EH (2001) SPARC and the kidney glomerulus: matricellular proteins exhibit diverse functions under normal and pathological conditions. Trends Cardiovasc Med 11(1): 32–37

    PubMed  CAS  Google Scholar 

  • Francki A, McClure TD, Brekken RA, Motamed K, Murri C, Wang T, Sage EH (2004) SPARC regulates TGF-beta1-dependent signaling in primary glomerular mesangial cells. J Cell Biochem 91(5):915–925

    PubMed  CAS  Google Scholar 

  • Frizell E, Shu-Ling L, Abraham A, Ozaki I, Eghbali M, Sage EH, Zern MA (1995) Expression of SPARC in normal and fibrotic livers. Hepatology 21(3):847–854

    PubMed  CAS  Google Scholar 

  • Fujita T, Shiba H, Sakata M, Uchida Y, Ogawa T, Kurihara H (2002) Effects of transforming growth factor-beta 1 and fibronectin on SPARC expression in cultures of human periodontal ligament cells. Cell Biol Int 26(12):1065–1072

    PubMed  CAS  Google Scholar 

  • Funk SE, Sage EH (1991) The Ca2(+)-binding glycoprotein SPARC modulates cell cycle progression in bovine aortic endothelial cells. Proc Natl Acad Sci U S A 88(7):2648–2652

    PubMed  CAS  Google Scholar 

  • Garrett Q, Khaw PT, Blalock TD, Schultz GS, Grotendorst GR, Daniels JT (2004) Involvement of CTGF in TGF-β1—stimulation of myofibroblast differentiation and collagen matrix contraction in the presence of mechanical stress. Invest Ophthalmol Vis Sci 45(4):1109–1116

    PubMed  Google Scholar 

  • Gilles C, Bassuk JA, Pulyaeva H, Sage EH, Foidart J-M, Thompson EW (1998) SPARC/osteonectin induces matrix metalloproteinase 2 activation in human breast cancer cell lines. Cancer Res 58(23):5529–5536

    PubMed  CAS  Google Scholar 

  • Giudici C, Raynal N, Wiedemann H, Cabral WA, Marini JC, Timpl R, Bächinger HP, Farndale RW, Sasaki T, Tenni R (2008) Mapping of SPARC/BM-40/osteonectin-binding sites on fibrillar collagens. J Biol Chem 283(28):19551–19560

    PubMed  CAS  Google Scholar 

  • Goldblum SE, Ding X, Funk SE, Sage EH (1994) SPARC (secreted protein acidic and rich in cysteine) regulates endothelial cell shape and barrier function. Proc Natl Acad Sci U S A 91(8): 3448–3452

    PubMed  CAS  Google Scholar 

  • Golledge J, Clancy P, Maguire J, Lincz L, Koblar S (2011) The role of tenascin C in cardiovascular disease. Cardiovasc Res 92(1):19–28

    PubMed  CAS  Google Scholar 

  • Gonzales TS, Coleman GC (1999) Periodontal manifestations of collagen vascular disorders. Periodontol 2000 21(1):94–105

    PubMed  CAS  Google Scholar 

  • Gooden MD, Vernon RB, Bassuk JA, Sage EH (1999) Cell cycle-dependent nuclear location of the matricellular protein SPARC: association with the nuclear matrix. J Cell Biochem 74(2): 152–167

    PubMed  CAS  Google Scholar 

  • Gulcher JR, Nies DE, Marton LS, Stefansson K (1989) An alternatively spliced region of the human hexabrachion contains a repeat of potential N-glycosylation sites. Proc Natl Acad Sci U S A 86(5):1588–1592

    PubMed  CAS  Google Scholar 

  • Gulcher JR, Nies DE, Alexakos MJ, Ravikant NA, Sturgill ME, Marton LS, Stefansson K (1991) Structure of the human hexabrachion (tenascin) gene. Proc Natl Acad Sci U S A 88(21): 9438–9442

    PubMed  CAS  Google Scholar 

  • Gundersen D, Tran-Than C, Sordat B, Mourali F, Ruegg C (1997) Plasmin-induced proteolysis of tenascin-C: modulation by T lymphocyte-derived urokinase-type plasminogen activator and effect on T lymphocyte adhesion, activation, and cell clustering. J Immunol 158(3):1051–1060

    PubMed  CAS  Google Scholar 

  • Hargus G, Cui Y, Schmid J-S, Xu J, Glatzel M, Schachner M, Bernreuther C (2008) Tenascin-R promotes neuronal differentiation of embryonic stem cells and recruitment of host-derived neural precursor cells after excitotoxic lesion of the mouse striatum. Stem Cells 26(8): 1973–1984

    PubMed  CAS  Google Scholar 

  • Hartenstein V, Mandal L (2006) The blood/vascular system in a phylogenetic perspective. Bioessays 28(12):1203–1210

    PubMed  Google Scholar 

  • Hasselaar P, Sage EH (1992) SPARC antagonizes the effect of basic fibroblast growth factor on the migration of bovine aortic endothelial cells. J Cell Biochem 49(3):272–283

    PubMed  CAS  Google Scholar 

  • Herold-Mende C, Mueller MM, Bonsanto MM, Schmitt HP, Kunze S, Steiner H-H (2002) Clinical impact and functional aspects of tenascin-C expression during glioma progression. Int J Cancer 98(3):362–369

    PubMed  CAS  Google Scholar 

  • Huxley-Jones J, Robertson DL, Boot-Handford RP (2007) On the origins of the extracellular matrix in vertebrates. Matrix Biol 26(1):2–11

    PubMed  CAS  Google Scholar 

  • Huynh M-H, Helene Sage E, 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(4):407–418

    PubMed  CAS  Google Scholar 

  • Huynh M-H, Hong H, Delovitch S, Desser S, Ringuette M (2000) Association of SPARC (osteonectin, BM-40) with extracellular and intracellular components of the ciliated surface ectoderm of Xenopus embryos. Cell Motil Cytoskeleton 47(2):154–162

    PubMed  CAS  Google Scholar 

  • Huynh M-H, Sodek K, Lee H, Ringuette M (2004) Interaction between SPARC and tubulin in Xenopus. Cell Tissue Res 317(3):313–317

    PubMed  CAS  Google Scholar 

  • Huynh M-H, Zhu S, Kollara A, Brown T, Winklbauer R, Ringuette M (2011) Knockdown of SPARC leads to decreased cell–cell adhesion and lens cataracts during post-gastrula development in Xenopus laevis. Dev Genes Evol 220(11):315–327

    PubMed  CAS  Google Scholar 

  • Hynes RO (1999) The dynamic dialogue between cells and matrices: Implications of fibronectin’s elasticity. Proc Natl Acad Sci U S A 96(6):2588–2590

    PubMed  CAS  Google Scholar 

  • Imai K, Kusakabe M, Sakakura T, Nakanishi I, Okada Y (1994) Susceptibility of tenascin to degradation by matrix metalloproteinases and serine proteinases. FEBS Lett 352(2):216–218

    PubMed  CAS  Google Scholar 

  • Iruela-Arispe M, Diglio C, Sage E (1991) Modulation of extracellular matrix proteins by endothelial cells undergoing angiogenesis in vitro. Arterioscler Thromb Vasc Biol 11(4):805–815

    CAS  Google Scholar 

  • Iruela-Arispe ML, Vernon RB, Wu H, Jaenisch R, Sage EH (1996) Type I collagen-deficient Mov-13 mice do not retain SPARC in the extracellular matrix: implications for fibroblast function. Dev Dyn 207(2):171–183

    PubMed  CAS  Google Scholar 

  • Järvinen TAH, Józsa L, Kannus P, Järvinen TLN, Hurme T, Kvist M, Pelto-Huikko M, Kalimo H, Järvinen M (2003) Mechanical loading regulates the expression of tenascin-C in the myotendinous junction and tendon but does not induce de novo synthesis in the skeletal muscle. J Cell Sci 116(5):857–866

    PubMed  Google Scholar 

  • Joester A, Faissner A (1999) Evidence for combinatorial variability of tenascin-C isoforms and developmental regulation in the mouse central nervous system. J Biol Chem 274(24): 17144–17151

    PubMed  CAS  Google Scholar 

  • Joester A, Faissner A (2001) The structure and function of tenascins in the nervous system. Matrix Biol 20(1):13–22

    PubMed  CAS  Google Scholar 

  • Jones FS, Burgoon MP, Hoffman S, Crossin KL, Cunningham BA, Edelman GM (1988) A cDNA clone for cytotactin contains sequences similar to epidermal growth factor-like repeats and segments of fibronectin and fibrinogen. Proc Natl Acad Sci U S A 85(7):2186–2190

    PubMed  CAS  Google Scholar 

  • Jones FS, Hoffman S, Cunningham BA, Edelman GM (1989) A detailed structural model of cytotactin: protein homologies, alternative RNA splicing, and binding regions. Proc Natl Acad Sci U S A 86(6):1905–1909

    PubMed  CAS  Google Scholar 

  • Jones FS, Jones PL (2000) The tenascin family of ECM glycoproteins: Structure, function and regulation during embryonic development and tissue remodeling. Dev Dyn 218(2):235–259

    PubMed  CAS  Google Scholar 

  • Kammerer RA, Schulthess T, Landwehr R, Lustig A, Fischer D, Engel J (1998) Tenascin-C hexabrachion assembly is a sequential two-step process initiated by coiled-coil α-helices. J Biol Chem 273(17):10602–10608

    PubMed  CAS  Google Scholar 

  • Kang Y-J, Stevenson A, Yau P, Kollmar R (2008) Sparc protein is required for normal growth of zebrafish otoliths. J Assoc Res Otolaryngol 9(4):436–451

    PubMed  Google Scholar 

  • Kaufmann B, Müller S, Hanisch F-G, Hartmann U, Paulsson M, Maurer P, Zaucke F (2004) Structural variability of BM-40/SPARC/osteonectin glycosylation: implications for collagen affinity. Glycobiology 14(7):609–619

    PubMed  CAS  Google Scholar 

  • Kaur BKF, Severson EA, Matheny SL, Brat DJ, Van Meir EG (2005) Hypoxia and the hypoxia-inducible-factor pathway in glioma growth and angiogenesis. Neuro Oncol 7(2):134–153

    PubMed  CAS  Google Scholar 

  • Kawakami K, Matsumoto K-I (2011) Behavioral alterations in mice lacking the gene for tenascin-X. Biol Pharm Bull 34(4):590–593

    PubMed  CAS  Google Scholar 

  • Kawasaki KST, Weiss K (2004) Genetic basis for the evolution of vertebrate mineralized tissue. Proc Natl Acad Sci U S A 101(31):11356–11361

    PubMed  CAS  Google Scholar 

  • Koehler A, Desser S, Chang B, MacDonald J, Tepass U, Ringuette M (2009) 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(9):509–521

    PubMed  CAS  Google Scholar 

  • Kuhn C, Mason RJ (1995) Immunolocalization of SPARC, tenascin, and thrombospondin in pulmonary fibrosis. Am J Pathol 147(6):1759–1769

    PubMed  CAS  Google Scholar 

  • 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(45):29635–29640

    PubMed  CAS  Google Scholar 

  • Laky D, Parascan L (2007) Hibernating myocardium, morphological studies on intraoperatory myocardial biopsies and on chronic ischemia experimental model. Rom J Morphol Embryol 48(4):407–413

    PubMed  CAS  Google Scholar 

  • Leahy DJ, Hendrickson WA, Aukhil I, Erickson HP (1992) Structure of a fibronectin type III domain from tenascin phased by MAD analysis of the selenomethionyl protein. Science 258(5084):987–991

    PubMed  CAS  Google Scholar 

  • Leask A, Abraham DJ (2003) The role of connective tissue growth factor, a multifunctional matricellular protein, in fibroblast biology. Biochem Cell Biol 81(6):355–363

    PubMed  CAS  Google Scholar 

  • Leask A, Abraham DJ (2004) TGF-ß signaling and the fibrotic response. FASEB J 18(7):816–827

    PubMed  CAS  Google Scholar 

  • Leask A, Holmes A, Black CM, Abraham DJ (2003) Connective tissue growth factor gene regulation. J Biol Chem 278(15):13008–13015

    PubMed  CAS  Google Scholar 

  • Leask A, Denton CP, Abraham DJ (2004) Insights into the molecular mechanism of chronic fibrosis: the role of connective tissue growth factor in scleroderma. J Invest Dermatol 122(1): 1–6

    PubMed  CAS  Google Scholar 

  • Limeback HF, Sodek J (1979) Procollagen synthesis and processing in periodontal ligament in vivo and in vitro. Eur J Biochem 100(2):541–550

    PubMed  CAS  Google Scholar 

  • Liu A, Mosher DF, Murphy-Ullrich JE, Goldblum SE (2009) The counteradhesive proteins, thrombospondin 1 and SPARC/osteonectin, open the tyrosine phosphorylation-responsive paracellular pathway in pulmonary vascular endothelia. Microvasc Res 77(1):13–20

    PubMed  CAS  Google Scholar 

  • Lussier C, Sodek J, Beaulieu J-F (2001) Expression of SPARC/osteonectin/BM4O in the human gut: predominance in the stroma of the remodeling distal intestine. J Cell Biochem 81(3): 463–476

    PubMed  CAS  Google Scholar 

  • Macko RF, Gelber AC, Young BA, Lowitt MH, White B, Wigley FM, Goldblum SE (2002) Increased circulating concentrations of the counteradhesive proteins SPARC and thrombospondin-1 in systemic sclerosis (scleroderma). Relationship to platelet and endothelial cell activation. J Rheumatol 29(12):2565–2570

    PubMed  CAS  Google Scholar 

  • Maillard C, Malaval L, Delmas PD (1992) Immunological screening of SPARC/osteonectin in nonmineralized tissues. Bone 13(3):257–264

    PubMed  CAS  Google Scholar 

  • Marr H, Basalamah MA, Edgell CJ (1997) Endothelial cell expression of testican mRNA. Endothelium 5(3):209–219

    PubMed  CAS  Google Scholar 

  • Martina E, Degen M, Rüegg C, Merlo A, Lino MM, Chiquet-Ehrismann R, Brellier F (2010a) Tenascin-W is a specific marker of glioma-associated blood vessels and stimulates angiogenesis in vitro. FASEB J 24(3):778–787

    PubMed  CAS  Google Scholar 

  • Martina E, Chiquet-Ehrismann R, Brellier F (2010b) Tenascin-W: an extracellular matrix protein associated with osteogenesis and cancer. Int J Biochem Cell Biol 42(9):1412–1415

    PubMed  CAS  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(3):124–133

    PubMed  CAS  Google Scholar 

  • Maschler S, Grunert S, Danielopol A, Beug H, Wirl G (2004) Enhanced tenascin-C expression and matrix deposition during Ras/TGF-[beta]-induced progression of mammary tumor cells. Oncogene 23(20):3622–3633

    PubMed  CAS  Google Scholar 

  • Masson S, Arosio B, Luvarà G, Gagliano N, Fiordaliso F, Santambrogio D, Vergani C, Latini R, Annoni G (1998) Remodelling of cardiac extracellular matrix during β-adrenergic stimulation: upregulation of SPARC in the myocardium of adult rats. J Mol Cell Cardiol 30(8):1505–1514

    PubMed  CAS  Google Scholar 

  • Matsumoto K-I, Arai M, Ishihara N, Ando A, Inoko H, Ikemura T (1992) Cluster of fibronectin type III repeats found in the human major histocompatibility complex class III region shows the highest homology with the repeats in an extracellular matrix protein, tenascin. Genomics 12(3):485–491

    PubMed  CAS  Google Scholar 

  • McCurdy S, Baicu CF, Heymans S, Bradshaw AD (2010) Cardiac extracellular matrix remodeling: fibrillar collagens and Secreted Protein Acidic and Rich in Cysteine (SPARC). J Mol Cell Cardiol 48(3):544–549

    PubMed  CAS  Google Scholar 

  • Meloty-Kapella CV, Degen M, Chiquet-Ehrismann R, Tucker RP (2006) Avian tenascin-W: expression in smooth muscle and bone, and effects on calvarial cell spreading and adhesion in vitro. Dev Dyn 235(6):1532–1542

    PubMed  CAS  Google Scholar 

  • Midwood K, Hussenet T, Langlois B, Orend G (2011) Advances in tenascin-C biology. Cell Mol Life Sci 68(19):3175–3199

    PubMed  CAS  Google Scholar 

  • Mitrovic N, Schachner M (1995) Detection of tenascin-C in the nervous system of the tenascin-C mutant mouse. J Neurosci Res 42(5):710–717

    PubMed  CAS  Google Scholar 

  • Motamed K, Blake DJ, Angello JC, Allen BL, Rapraeger AC, Hauschka SD, Sage EH (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(2):408–423

    PubMed  CAS  Google Scholar 

  • Nakatani K, Seki S, Kawada N, Kitada T, Yamada T, Sakaguchi H, Kadoya H, Ikeda K, Kaneda K (2002) Expression of SPARC by activated hepatic stellate cells and its correlation with the stages of fibrogenesis in human chronic hepatitis. Virchows Arch 441(5):466–474

    PubMed  CAS  Google Scholar 

  • Nishi T, Weinstein J, Gillespie WM, Paulson JC (1991) Complete primary structure of porcine tenascin. Eur J Biochem 202(2):643–648

    PubMed  CAS  Google Scholar 

  • Novinec M, Kordiš D, Turk V, Lenarčič B (2006) Diversity and evolution of the thyroglobulin type-1 domain superfamily. Mol Biol Evol 23(4):744–755

    PubMed  CAS  Google Scholar 

  • Nozaki M, Sakurai E, Raisler BJ, Baffi JZ, Witta J, Ogura Y, Brekken RA, Sage EH, Ambati BK, Ambati J (2006) Loss of SPARC-mediated VEGFR-1 suppression after injury reveals a novel antiangiogenic activity of VEGF-A. J Clin Invest 116(2):422–429

    PubMed  CAS  Google Scholar 

  • Parks WC (1999) Matrix metalloproteinases in repair. Wound Repair Regen 7(6):423–432

    PubMed  CAS  Google Scholar 

  • Patthy L (1990) Homology of a domain of the growth hormone/prolactin receptor family with type III modules of fibronectin. Cell 61(1):13–14

    PubMed  CAS  Google Scholar 

  • Pazin DE, Albrecht KH (2009) Developmental expression of Smoc1 and Smoc2 suggests potential roles in fetal gonad and reproductive tract differentiation. Dev Dyn 238(11):2877–2890

    PubMed  CAS  Google Scholar 

  • Pearson C, Pearson D, Shibahara S, Hofsteenge J, Chiquet-Ehrismann R (1988) Tenascin: cDNA cloning and induction by TGF-beta. EMBO J 7(10):2977–2982

    PubMed  CAS  Google Scholar 

  • Peterson MC (2005) Circulating transforming growth factor beta-1: a partial molecular explanation for associations between hypertension, diabetes, obesity, smoking and human disease involving fibrosis. Med Sci Monit 11(7):RA229–RA232

    PubMed  CAS  Google Scholar 

  • Pichler RH, Hugo C, Shankland SJ, Reed MJ, Bassuk JA, Andoh TF, Lombardi DM, Schwartz SM, Bennett WM, Alpers CE, Sage EH, Johnson RJ, Couser WG (1996) SPARC is expressed in renal interstitial fibrosis and in renal vascular injury. Kidney Int 50(6):1978–1989

    PubMed  CAS  Google Scholar 

  • Puolakkainen PA, Bradshaw AD, Brekken RA, Reed MJ, Kyriakides T, Funk SE, Gooden MD, Vernon RB, Wight TN, Bornstein P, Sage EH (2005) SPARC-thrombospondin-2-double-null mice exhibit enhanced cutaneous wound healing and increased fibrovascular invasion of subcutaneous polyvinyl alcohol sponges. J Histochem Cytochem 53(5):571–581

    PubMed  CAS  Google Scholar 

  • 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 U S A 89(4):1281–1285

    PubMed  CAS  Google Scholar 

  • Rathjen FG, Wolff JM, Chiquet-Ehrismann R (1991) Restrictin: a chick neural extracellular matrix protein involved in cell attachment co-purifies with the cell recognition molecule F11. Development 113(1):151–164

    PubMed  CAS  Google Scholar 

  • Reed MJ, Vernon RB, Abrass IB, Sage EH (1994) TGF-beta 1 induces the expression of type I collagen and SPARC, and enhances contraction of collagen gels, by fibroblasts from young and aged donors. J Cell Physiol 158(1):169–179

    PubMed  CAS  Google Scholar 

  • Rivera LB, Brekken RA (2011) SPARC promotes pericyte recruitment via inhibition of endoglin-dependent TGF-β1 activity. J Cell Biol 193(7):1305–1319

    PubMed  CAS  Google Scholar 

  • Rocnik EF, Liu P, Sato K, Walsh K, Vaziri C (2006) The novel SPARC family member SMOC-2 potentiates angiogenic growth factor activity. J Biol Chem 281(32):22855–22864

    PubMed  CAS  Google Scholar 

  • Sadlier DM, Connolly SB, Kieran NE, Roxburgh S, Brazil DP, Kairaitis L, Wang Y, Harris DCH, Doran P, Brady HR (2004) Sequential extracellular matrix-focused and baited-global cluster analysis of serial transcriptomic profiles identifies candidate modulators of renal tubulointerstitial fibrosis in murine adriamycin-induced nephropathy. J Biol Chem 279(28): 29670–29680

    PubMed  CAS  Google Scholar 

  • Sage E, Bassuk JA, Yost JC, Folkman MJ, Lane TF (1995) Inhibition of endothelial cell proliferation by SPARC is mediated through a Ca2+-binding EF-hand sequence. J Cell Biochem 57(1):127–140

    PubMed  CAS  Google Scholar 

  • Sage EH, Reed M, Funk SE, Truong T, Steadele M, Puolakkainen P, Maurice DH, Bassuk JA (2003) Cleavage of the matricellular protein SPARC by matrix metalloproteinase 3 produces polypeptides that influence angiogenesis. J Biol Chem 278(39):37849–37857

    PubMed  CAS  Google Scholar 

  • Salo T, Mäkelä M, Kylmäniemi M, Autio-Harmainen H, Larjava H (1994) Expression of matrix metalloproteinase-2 and -9 during early human wound healing. Lab Invest 70(2):176–182

    PubMed  CAS  Google Scholar 

  • Salonen J, Domenicucci C, Goldberg HA, Sodek J (1990) Immunohistochemical localization of SPARC (osteonectin) and denatured collagen and their relationship to remodelling in rat dental tissues. Arch Oral Biol 35(5):337–346

    PubMed  CAS  Google Scholar 

  • Sangaletti S, Stoppacciaro A, Guiducci C, Torrisi MR, Colombo MP (2003) Leukocyte, rather than tumor-produced SPARC, determines stroma and collagen type IV deposition in mammary carcinoma. J Exp Med 198(10):1475–1485

    PubMed  CAS  Google Scholar 

  • Schalkwijk J, Zweers MC, Steijlen PM, Dean WB, Taylor G, van Vlijmen IM, van Haren B, Miller WL, Bristow J (2001) A recessive form of the Ehlers–Danlos syndrome caused by tenascin-X deficiency. N Engl J Med 345(16):1167–1175

    PubMed  CAS  Google Scholar 

  • Schellings MW, Vanhoutte D, Swinnen M, Cleutjens JP, Debets J, van Leeuwen RE, d’Hooge J, Van de Werf F, Carmeliet P, Pinto YM, Sage EH, Heymans S (2009) Absence of SPARC results in increased cardiac rupture and dysfunction after acute myocardial infarction. J Exp Med 206(1):113–123

    PubMed  CAS  Google Scholar 

  • Schenk S, Chiquet-Ehrismann R (1994) Teanscins. In: Methods in Enzymology, Vol 245. New York Academic Press p 52–61

    Google Scholar 

  • Schenk S, Chiquet-Ehrismann R, Battegay EJ (1999) The fibrinogen globe of tenascin-C promotes basic fibroblast growth factor-induced endothelial cell elongation. Mol Biol Cell 10(9): 2933–2943

    PubMed  CAS  Google Scholar 

  • Scherberich A, Tucker RP, Samandari E, Brown-Luedi M, Martin D, Chiquet-Ehrismann R (2004) Murine tenascin-W: a novel mammalian tenascin expressed in kidney and at sites of bone and smooth muscle development. J Cell Sci 117(4):571–581

    PubMed  CAS  Google Scholar 

  • Schiemann BJ, Neil JR, Schiemann WP (2003) SPARC inhibits epithelial cell proliferation in part through stimulation of the transforming growth factor-β-signaling system. Mol Biol Cell 14(10):3977–3988

    PubMed  CAS  Google Scholar 

  • Schnepp A, Lindgren PK, Hülsmann H, Kröger S, Paulsson M, Hartmann U (2005) Mouse testican-2. J Biol Chem 280(12):11274–11280

    PubMed  CAS  Google Scholar 

  • Shankavaram UT, DeWitt DL, Funk SE, Sage EH, Wahl LM (1997) Regulation of human monocyte matrix metalloproteinases by SPARC. J Cell Physiol 173(3):327–334

    PubMed  CAS  Google Scholar 

  • Siri A, Knäuper V, Veirana N, Caocci F, Murphy G, Zardi L (1995) Different susceptibility of small and large human tenascin-C isoforms to degradation by matrix metalloproteinases. J Biol Chem 270(15):8650–8654

    PubMed  CAS  Google Scholar 

  • Sodek J, Zhu B, Huynh MH, Brown TJ, Ringuette M (2002) Novel functions of the matricellular proteins osteopontin and osteonectin/SPARC. Connect Tissue Res 43(2–3):308–319

    PubMed  CAS  Google Scholar 

  • Spring J, Beck K, Chiquet-Ehrismann R (1989) Two contrary functions of tenascin: dissection of the active sites by recombinant tenascin fragments. Cell 59(2):325–334

    PubMed  CAS  Google Scholar 

  • Sriramarao P, Bourdon MA (1993) A novel tenascin type III repeat is part of a complex of tenascin mRNA alternative splices. Nucleic Acids Res 21(1):163–168

    PubMed  CAS  Google Scholar 

  • 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 Lung Cell Mol Physiol 277(3):L628–L635

    CAS  Google Scholar 

  • Strup-Perrot C, Mathé D, Linard C, Violot D, Milliat F, François A, Bourhis J, Vozenin-Brotons M-C (2004) Global gene expression profiles reveal an increase in mRNA levels of collagens, MMPs, and TIMPs in late radiation enteritis. Am J Physiol Gastrointest Liver Physiol 287(4):G875–G885

    PubMed  CAS  Google Scholar 

  • Tahashi Y, Matsuzaki K, Date M, Yoshida K, Furukawa F, Sugano Y, Matsushita M, Himeno Y, Inagaki Y, Inoue K (2002) Differential regulation of TGF-β signal in hepatic stellate cells between acute and chronic rat liver injury. Hepatology 35(1):49–61

    PubMed  CAS  Google Scholar 

  • Taneda S, Pippin JW, Sage EH, Hudkins KL, Takeuchi Y, Couser WG, Alpers CE (2003) Amelioration of diabetic nephropathy in SPARC-null mice. J Am Soc Nephrol 14(4):968–980

    PubMed  CAS  Google Scholar 

  • Tucker RP, Chiquet-Ehrismann R (2009) Evidence for the evolution of tenascin and fibronectin early in the chordate lineage. Int J Biochem Cell Biol 41(2):424–434

    PubMed  CAS  Google Scholar 

  • Tucker R, Drabikowski K, Hess J, Ferralli J, Chiquet-Ehrismann R, Adams J (2006) Phylogenetic analysis of the tenascin gene family: evidence of origin early in the chordate lineage. BMC Evol Biol 6(1):60

    PubMed  CAS  Google Scholar 

  • Tufty RM, Kretsinger RH (1975) Troponin and parvalbumin calcium binding regions predicted in myosin light chain and T4 lysozyme. Science 187(4172):167–169

    PubMed  CAS  Google Scholar 

  • Tung PS, Domenicucci C, Wasi S, Sodek J (1985) Specific immunohistochemical localization of osteonectin and collagen types I and III in fetal and adult porcine dental tissues. J Histochem Cytochem 33(6):531–540

    PubMed  CAS  Google Scholar 

  • Unemori E, Amento EP (1991) Connective tissue metabolism including cytokines in scleroderma. Curr Opin Rheumatol 3(6):953–959

    PubMed  CAS  Google Scholar 

  • Van Obberghen-Schilling E, Tucker RP, Saupe F, Gasser I, Cseh B, Orend G (2011) Fibronectin and tenascin-C: accomplices in vascular morphogenesis during development and tumor growth. Int J Dev Biol 55:511–525

    PubMed  Google Scholar 

  • Wang X, Chen W, Huang Y, Sun J, Men J, Liu H, Luo F, Guo L, Lv X, Deng C, Zhou C, Fan Y, Li X, Huang L, Hu Y, Liang C, Hu X, Xu J, Yu X (2011) The draft genome of the carcinogenic human liver fluke Clonorchis sinensis. Genome Biol 12(10):R107

    PubMed  CAS  Google Scholar 

  • Wasi S, Otsuka K, Yao KL, Tung PS, Aubin JE, Sodek J, Termine JD (1984) An osteonectinlike protein in porcine periodontal ligament and its synthesis by periodontal ligament fibroblasts. Can J Biochem Cell Biol 62(6):470–478

    PubMed  CAS  Google Scholar 

  • Weber P, Montag D, Schachner M, Bernhardt RR (1998) Zebrafish tenascin-W, a new member of the tenascin family. J Neurobiol 35(1):1–16

    PubMed  CAS  Google Scholar 

  • Weller A, Beck S, Ekblom P (1991) Amino acid sequence of mouse tenascin and differential expression of two tenascin isoforms during embryogenesis. J Cell Biol 112(2):355–362

    PubMed  CAS  Google Scholar 

  • Willems IE, Arends J, Daemen M (1996) Tenascin and fibronectin expression in healing human myocardial scars. J Pathol 179(3):321–325

    PubMed  CAS  Google Scholar 

  • Wrana JL, Maeno M, Hawrylyshyn B, Yao KL, Domenicucci C, Sodek J (1988) Differential effects of transforming growth factor-beta on the synthesis of extracellular matrix proteins by normal fetal rat calvarial bone cell populations. J Cell Biol 106(3):915–924

    PubMed  CAS  Google Scholar 

  • Wrana JL, Overall CM, Sodek J (1991a) Regulation of the expression of a secreted acidic protein rich in cysteine (SPARC) in human fibroblasts by transforming growth factor β. Eur J Biochem 197(2):519–528

    PubMed  CAS  Google Scholar 

  • Wrana JLKT, Zhang Q, Overall CM, Aubin JE, Butler WT, Sodek J (1991b) Regulation of transformation-sensitive secreted phosphoprotein (SPPI/osteopontin) expression by transforming growth factor-beta. Comparisons with expression of SPARC (secreted acidic cysteine-rich protein). Biochem J 1(273):523–531

    Google Scholar 

  • Xueyong L, Shaozong C, Wangzhou L, Yuejun L, Xiaoxing L, Jing L, Yanli W, Jinqing L (2008) Differentiation of the pericyte in wound healing: the precursor, the process, and the role of the vascular endothelial cell. Wound Repair Regen 16(3):346–355

    PubMed  Google Scholar 

  • Yamada KM, Yamada SS, Pastan I (1975) The major cell surface glycoprotein of chick embryo fibroblasts is an agglutinin. Proc Natl Acad Sci U S A 72(8):3158–3162

    PubMed  CAS  Google Scholar 

  • Yan Q, Weaver M, Perdue N, Sage EH (2005) Matricellular protein SPARC is translocated to the nuclei of immortalized murine lens epithelial cells. J Cell Physiol 203(1):286–294

    PubMed  CAS  Google Scholar 

  • Yoshimura H, Michishita M, Ohkusu-Tsukada K, Takahasi K (2011) Appearance and distribution of stromal myofibroblasts and tenascin-C in feline mammary tumors. Histol Histopathol 26(3): 297–305

    PubMed  Google Scholar 

  • Youssef W, Tavill AS (2002) Connective tissue diseases and the liver. J Clin Gastroenterol 35(4): 345–349

    PubMed  Google Scholar 

  • Yunker CK, Golembieski W, Lemke N, Schultz CR, Cazacu S, Brodie C, Rempel SA (2008) SPARC-induced increase in glioma matrix and decrease in vascularity are associated with reduced VEGF expression and secretion. Int J Cancer 122(12):2735–2743

    PubMed  CAS  Google Scholar 

  • Zhao Y, Young SL (1995) TGF-beta regulates expression of tenascin alternative-splicing isoforms in fetal rat lung. Am J Physiol Lung Cell Mol Physiol 268(2):L173–L180

    CAS  Google Scholar 

  • Zhao Y, Young SL, McIntosh JC (1998) Induction of tenascin in rat lungs undergoing bleomycin-induced pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 274(6):L1049–L1057

    CAS  Google Scholar 

  • Zhou Y (2009) The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 460(7253):345–351

    CAS  Google Scholar 

  • Zhou X, Tan FK, Reveille JD, Wallis D, Milewicz DM, Ahn C, Wang A, Arnett FC (2002) Association of novel polymorphisms with the expression of SPARC in normal fibroblasts and with susceptibility to scleroderma. Arthritis Rheum 46(11):2990–2999

    PubMed  CAS  Google Scholar 

  • Zhou X, Tan FK, Guo X, Wallis D, Milewicz DM, Xue S, Arnett FC (2005) Small interfering RNA inhibition of SPARC attenuates the profibrotic effect of transforming growth factor β1 in cultured normal human fibroblasts. Arthritis Rheum 52(1):257–261

    PubMed  CAS  Google Scholar 

  • Zhou X, Tan FK, Guo X, Arnett FC (2006) Attenuation of collagen production with small interfering RNA of SPARC in cultured fibroblasts from the skin of patients with scleroderma. Arthritis Rheum 54(8):2626–2631

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Cell and Systems Biology, University of Toronto, 25 Harbord Street, Toronto, ON, Canada, M5S3G5

    Cristina A. Baratta, Fahd Al-Dhalaan & Maurice J. Ringuette

  2. Samuel Lunenfeld Research Institute, 600 University Avenue, Toronto, ON, Canada, M5G 1X5

    Theodore J. Brown

Authors
  1. Cristina A. Baratta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Theodore J. Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fahd Al-Dhalaan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maurice J. Ringuette
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maurice J. Ringuette .

Editor information

Editors and Affiliations

  1. Hospital for Sick Children, Toronto, Ontario, Canada

    Fred W. Keeley

  2. Dept. Cell Biology & Physiology, Washington University School of Medicine, St. Louis, Missouri, USA

    Robert P. Mecham

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Baratta, C.A., Brown, T.J., Al-Dhalaan, F., Ringuette, M.J. (2013). Evolution and Function of SPARC and Tenascins: Matricellular Counter-Adhesive Glycoproteins with Pleiotropic Effects on Angiogenesis and Tissue Fibrosis. In: Keeley, F., Mecham, R. (eds) Evolution of Extracellular Matrix. Biology of Extracellular Matrix. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-36002-2_7

Download citation

Publish with us

Policies and ethics

Search

Navigation