Original Article

You have full text access to this OnlineOpen article

Circulating fibronectin affects bone matrix, whereas osteoblast fibronectin modulates osteoblast function

  1. Anke Bentmann1,2,
  2. Nina Kawelke1,2,
  3. David Moss3,
  4. Hanswalter Zentgraf4,
  5. Yohann Bala5,
  6. Irina Berger6,
  7. Juerg A Gasser7,
  8. Inaam A Nakchbandi1,2,*

Article first published online: 14 DEC 2009

DOI: 10.1359/jbmr.091011

Issue

Journal of Bone and Mineral Research

Journal of Bone and Mineral Research

Volume 25, Issue 4, pages 706–715, April 2010

Additional Information

How to Cite

Bentmann, A., Kawelke, N., Moss, D., Zentgraf, H., Bala, Y., Berger, I., Gasser, J. A. and Nakchbandi, I. A. (2010), Circulating fibronectin affects bone matrix, whereas osteoblast fibronectin modulates osteoblast function. J Bone Miner Res, 25: 706–715. doi: 10.1359/jbmr.091011

Author Information

  1. 1

    Max-Planck Institute for Biochemistry, 82152 Martinsried, Germany

  2. 2

    Institute for Immunology, University of Heidelberg, 69120 Heidelberg, Germany

  3. 3

    Research Center Karlsruhe, ANKA Facility, 76344 Eggenstein-Leopoldshafen, Germany

  4. 4

    Electron Microscopy, German Cancer Research Center, 69120 Heidelberg, Germany

  5. 5

    INSERM Unit 831, University of Lyon, Faculty of Medicine R. Laennec, 69372 Lyon Cedex 08, France

  6. 6

    Pathology Institute, University of Heidelberg, 69120 Heidelberg, Germany

  7. 7

    Novartis Institutes for Biomedical Research, Musculoskeletal Diseases, 4002 Basel, Switzerland

*University of Heidelberg, Im Neuenheimer Feld 305, 2. OG, 69120 Heidelberg, Germany

Publication History

  1. Issue published online: 9 APR 2010
  2. Article first published online: 14 DEC 2009
  3. Accepted manuscript online: 27 JAN 2010 12:00AM EST
  4. Manuscript Accepted: 9 OCT 2009
  5. Manuscript Revised: 11 AUG 2009
  6. Manuscript Received: 15 JAN 2009

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (405K)

References

  • 1
    Burr D, Turner C. Biomechanics of bone. In: FavusM, ed. Primer on the Metabolic Bone Diseases and Disorders of Mineral Metabolism, 5th ed. Washington, DC: American Society for Bone and Mineral Research; 2003: 58–64.
  • 2
    Robey P, Boskey AL. The biochemistry of bone. In: MarcusR, FeldmanD, KelseyJ, eds. Osteoporosis. San Diego: Academic Press; 1996: 95–183.
  • 3
    Stein GS, Lian JB, Stein JL, Van Wijnen AJ, Montecino M. Transcriptional control of osteoblast growth and differentiation. Physiol Rev. 1996; 76: 593–629.
  • 4
    Velling T, Risteli J, Wennerberg K, Mosher DF, Johansson S. Polymerization of type I and III collagens is dependent on fibronectin and enhanced by integrins α11β1 and α2β1. J Biol Chem. 2002; 277: 37377–37381.
  • 5
    Stein GS, Lian JB. Molecular mechanisms mediating proliferation/differentiation interrelationships during progressive development of the osteoblast phenotype. Endocr Rev. 1993; 14: 424–442.
  • 6
    Sottile J, Hocking DC. Fibronectin polymerization regulates the composition and stability of extracellular matrix fibrils and cell-matrix adhesions. Mol Biol Cell. 2002; 13: 3546–3559.
  • 7
    Whyte M. Osteogenesis imperfecta. In: FavusM, ed. Primer on the metabolic bone diseases and disorders of mineral metabolism. Philadelphia: Lippincott Williams and Wilkins; 1999: 470–473.
  • 8
    McKee M, Farach-Carson M, Butler W, Hauschka P, Nanci A. Ultrastructural immunolocalization of noncollagenous (osteopontin and osteocalcin) and plasma (albumin and alpha 2HS-glycoprotein) proteins in rat bone. J Bone Miner Res. 1993; 8: 485–496.
    Direct Link:
  • 9
    Triffitt JT, Gebauer U, Ashton BA, Owen ME, Reynolds JJ. Origin of plasma alpha2HS-glycoprotein and its accumulation in bone. Nature. 1976; 262: 226–227.
  • 10
    Moursi AM, Damsky CH, Lull J, Zimmerman D, Doty SB, Aota S, Globus RK. Fibronectin regulates calvarial osteoblast differentiation. J Cell Sci. 1996; 109: 1369–1380.
  • 11
    Moursi AM, Globus RK, Damsky CH. Interactions between integrin receptors and fibronectin are required for calvarial osteoblast differentiation in vitro. J Cell Sci. 1997; 110: 2187–2196.
  • 12
    Chen Q, Zhao J, Dallas MR, Fassler R, Peters DM, Dallas SL. Fibronectin plays a role in osteoblast differentiation which may be mediated via regulation of BMP activity. J Bone Mineral Res. 2006; 21: s13.
  • 13
    Hynes R. Structure of fibronectins. In: RichA, ed. Fibronectins. New York: Springer; 1990: 113–175.
  • 14
    Matsuura H, Takio K, Titani K, Greene T, Levery SB, Salyan ME, Hakomori S. The oncofetal structure of human fibronectin defined by monoclonal antibody FDC-6. Unique structural requirement for the antigenic specificity provided by a glycosylhexapeptide. J Biol Chem. 1988; 263: 3314–3322.
  • 15
    Hynes R. Distribution of Fibronectins in vivo: Plasma. In: RichA, ed. Fibronectins. New York: Springer; 1990: 27–30.
  • 16
    Leiss M, Beckmann K, Giros A, Costell M, Fassler R. The role of integrin binding sites in fibronectin matrix assembly in vivo. Curr Opin Cell Biol. 2008; 20: 502–507.
  • 17
    Grzesik W, Robey P. Bone matrix RGD glycoproteins: immunolocalization and interaction with human primary osteoblastic bone cells in vitro. J Bone Miner Res. 1994; 9: 487–496.
    Direct Link:
  • 18
    Cheng SL, Lai CF, Fausto A, Chellaiah M, Feng X, McHugh KP, Teitelbaum SL, Civitelli R, Hruska KA, Ross FP, Avioli LV. Regulation of αVβ3 and αVβ5 integrins by dexamethasone in normal human osteoblastic cells. J Cell Biochem. 2000; 77: 265–276.
    Direct Link:
  • 19
    Pistone M, Sanguineti C, Federici A, Sanguineti F, Defilippi P, Santolini F, Querze G, Marchisio P, Manduca P. Integrin synthesis and utilization in cultured human osteoblasts. Cell Biol Int. 1996; 20: 471–479.
  • 20
    Saito T, Albelda S, Brighton C. Identification of integrin receptors on cultured human bone cells. J Orthop Res. 1994; 12: 384–394.
    Direct Link:
  • 21
    George EL, Georges-Labouesse EN, Patel-King RS, Rayburn H, Hynes RO. Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development. 1993; 119: 1079–1091.
  • 22
    Aszodi A, Hunziker EB, Brakebusch C, Fassler R. Beta1 integrins regulate chondrocyte rotation, G1 progression, and cytokinesis. Genes Dev. 2003; 17: 2465–2479.
  • 23
    Sakai T, Johnson K, Murozono M, Sakai K, Magnuson M, Wieloch T, Cronberg T, Isshiki A, Erickson H, Fassler R. Plasma fibronectin supports neuronal survival and reduces brain injury following transient focal cerebral ischemia but is not essential for skin-wound healing and hemostasis. Nature Medicine. 2001; 7: 324–330.
  • 24
    Dacquin R, Starbuck M, Schinke T, Karsenty G. Mouse α1(I)-collagen promoter is the best known promoter tp drive efficient Cre recombinase expression in osteoblasts. Develpmental Dynamics. 2002; 224: 245–251.
    Direct Link:
  • 25
    Constien R, Forde A, Liliensiek B, Grone HJ, Nawroth P, Hammerling G, Arnold B. Characterization of a novel EGFP reporter mouse to monitor Cre recombination as demonstrated by a Tie2 Cre mouse line. Genesis. 2001; 30: 36–44.
    Direct Link:
  • 26
    Takahashi S, Leiss M, Moser M, Ohashi T, Kitao T, Heckmann D, Pfeifer A, Kessler H, Takagi J, Erickson HP, Fassler R. The RGD motif in fibronectin is essential for development but dispensable for fibril assembly. J Cell Biol. 2007; 178: 167–178.
  • 27
    Kawelke N, Bentmann A, Hackl N, Hager HD, Feick P, Geursen A, Singer MV, Nakchbandi IA. Isoform of fibronectin mediates bone loss in patients with primary biliary cirrhosis by suppressing bone formation. J Bone Miner Res. 2008; 23: 1278–1286.
    Direct Link:
  • 28
    Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR. Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res. 1987; 2: 595–610.
    Direct Link:
  • 29
    Boskey AL, Goldberg M, Kulkarni A, Gomez S. Infrared imaging microscopy of bone: illustrations from a mouse model of Fabry disease. Biochim Biophys Acta. 2006; 1758: 942–947.
  • 30
    Boivin G, Bala Y, Doublier A, Farlay D, Ste-Marie LG, Meunier PJ, Delmas PD. The role of mineralization and organic matrix in the microhardness of bone tissue from controls and osteoporotic patients. Bone. 2008; 43: 532–538.
  • 31
    Zentgraf H, Franke WW. Differences of supranucleosomal organization in different kinds of chromatin: cell type-specific globular subunits containing different numbers of nucleosomes. J Cell Biol. 1984; 99: 272–286.
  • 32
    Chung DJ, Castro CH, Watkins M, Stains JP, Chung MY, Szejnfeld VL, Willecke K, Theis M, Civitelli R. Low peak bone mass and attenuated anabolic response to parathyroid hormone in mice with an osteoblast-specific deletion of connexin43. J Cell Sci. 2006; 119: 4187–4198.
  • 33
    Manabe R, Ohe N, Maeda T, Fukuda T, Sekiguchi K. Modulation of cell-adhesive activity of fibronectin by the alternatively spliced EDA segment. J Cell Biol. 1997; 139: 295–307.
  • 34
    Liao YF, Gotwals P, Koteliansky VE, Sheppard D, Van De Water L. The EIIIA segment of fibronectin is a ligand for integrins α9β1 and α4β1 providing a novel mechanism for regulating cell adhesion by alternative splicing. J Biol Chem. 2002; 277: 14467–14474.
  • 35
    Mould AP, Komoriya A, Yamada KM, Humphries MJ. The CS5 peptide is a second site in the IIICS region of fibronectin recognized by the integrin α4β1: inhibition of α4β1 function by RGD peptide homologues. J Biol Chem. 1991; 266: 3579–3585.
  • 36
    Grabner B, Landis WJ, Roschger P, Rinnerthaler S, Peterlik H, Klaushofer K, Fratzl P. Age- and genotype-dependence of bone material properties in the osteogenesis imperfecta murine model (oim). Bone. 2001; 29: 453–457.
  • 37
    McBride DJ Jr, Choe V, Shapiro JR, Brodsky B. Altered collagen structure in mouse tail tendon lacking the α2(I) chain. J Mol Biol. 1997; 270: 275–284.
  • 38
    Cassella JP, Barber P, Catterall AC, Ali SY. A morphometric analysis of osteoid collagen fibril diameter in osteogenesis imperfecta. Bone. 1994; 15: 329–334.
  • 39
    Leslie WD, Bernstein CN, Leboff MS. AGA technical review on osteoporosis in hepatic disorders. Gastroenterology. 2003; 125: 941–966.
  • 40
    Manabe R, Oh-e N, Sekiguchi K. Alternatively spliced EDA segment regulates fibronectin-dependent cell cycle progression and mitogenic signal transduction. J Biol Chem. 1999; 274: 5919–5924.
View Full Article (HTML) Get PDF (405K)