• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of jcellbiolHomeThe Rockefeller University PressEditorsContactInstructions for AuthorsThis issue
J Cell Biol. Oct 1, 1989; 109(4): 1779–1786.
PMCID: PMC2115793

Involvement of cell surface phosphatidylinositol-anchored glycoproteins in cell-cell adhesion of chick embryo myoblasts

Abstract

During myogenesis myoblasts fuse to form multinucleate cells that express muscle-specific proteins. A specific cell-cell adhesion process precedes lipid bilayer union during myoblast fusion (Knudsen, K. A., and A. F. Horwitz. 1977. Dev. Biol. 58:328-338) and is mediated by cell surface glycoproteins (Knudsen, K. A., 1985. J. Cell Biol. 101:891- 897). In this paper we show that myoblast adhesion and myotube formation are inhibited by treating fusion-competent myoblasts with phosphatidylinositol-specific phospholipase C (PI-PLC). The effect of PI-PLC on myoblast adhesion is dose dependent and inhibited by D-myo- inositol 1-monophosphate and the effect on myotube formation is reversible, suggesting a specific, nontoxic effect on myogenesis by the enzyme. A soluble form of adhesion-related glycoproteins is released from fusion-competent myoblasts by treatment with PI-PLC as evidenced by (a) the ability of phospholipase C (PLC)-released material to block the adhesion-perturbing activity of a polyclonal antiserum to intact myoblasts; and (b) the ability of PLC-released glycoprotein to stimulate adhesion-perturbing antisera when injected into mice. PI-PLC treatment of fusion-competent myoblasts releases an isoform of N-CAM into the supernate, suggesting that N-CAM may participate in mediating myoblast interaction during myogenesis.

Full Text

The Full Text of this article is available as a PDF (1.6M).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Barton CH, Dickson G, Gower HJ, Rowett LH, Putt W, Elsom V, Moore SE, Goridis C, Walsh FS. Complete sequence and in vitro expression of a tissue-specific phosphatidylinositol-linked N-CAM isoform from skeletal muscle. Development. 1988 Sep;104(1):165–173. [PubMed]
  • Behrens J, Birchmeier W, Goodman SL, Imhof BA. Dissociation of Madin-Darby canine kidney epithelial cells by the monoclonal antibody anti-arc-1: mechanistic aspects and identification of the antigen as a component related to uvomorulin. J Cell Biol. 1985 Oct;101(4):1307–1315. [PMC free article] [PubMed]
  • Bertolotti R, Rutishauser U, Edelman GM. A cell surface molecule involved in aggregation of embryonic liver cells. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4831–4835. [PMC free article] [PubMed]
  • Bixby JL, Pratt RS, Lilien J, Reichardt LF. Neurite outgrowth on muscle cell surfaces involves extracellular matrix receptors as well as Ca2+-dependent and -independent cell adhesion molecules. Proc Natl Acad Sci U S A. 1987 Apr;84(8):2555–2559. [PMC free article] [PubMed]
  • Brackenbury R, Rutishauser U, Edelman GM. Distinct calcium-independent and calcium-dependent adhesion systems of chicken embryo cells. Proc Natl Acad Sci U S A. 1981 Jan;78(1):387–391. [PMC free article] [PubMed]
  • Buck CA, Horwitz AF. Cell surface receptors for extracellular matrix molecules. Annu Rev Cell Biol. 1987;3:179–205. [PubMed]
  • Burnette WN. "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate--polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem. 1981 Apr;112(2):195–203. [PubMed]
  • Cross GA. Eukaryotic protein modification and membrane attachment via phosphatidylinositol. Cell. 1987 Jan 30;48(2):179–181. [PubMed]
  • Cunningham BA, Hemperly JJ, Murray BA, Prediger EA, Brackenbury R, Edelman GM. Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science. 1987 May 15;236(4803):799–806. [PubMed]
  • Damsky CH, Richa J, Solter D, Knudsen K, Buck CA. Identification and purification of a cell surface glycoprotein mediating intercellular adhesion in embryonic and adult tissue. Cell. 1983 Sep;34(2):455–466. [PubMed]
  • Dickson G, Gower HJ, Barton CH, Prentice HM, Elsom VL, Moore SE, Cox RD, Quinn C, Putt W, Walsh FS. Human muscle neural cell adhesion molecule (N-CAM): identification of a muscle-specific sequence in the extracellular domain. Cell. 1987 Sep 25;50(7):1119–1130. [PubMed]
  • Dustin ML, Selvaraj P, Mattaliano RJ, Springer TA. Anchoring mechanisms for LFA-3 cell adhesion glycoprotein at membrane surface. Nature. 329(6142):846–848. [PubMed]
  • Edelman GM. Cell adhesion molecules. Science. 1983 Feb 4;219(4584):450–457. [PubMed]
  • Edelman GM, Murray BA, Mege RM, Cunningham BA, Gallin WJ. Cellular expression of liver and neural cell adhesion molecules after transfection with their cDNAs results in specific cell-cell binding. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8502–8506. [PMC free article] [PubMed]
  • Ferguson MA, Williams AF. Cell-surface anchoring of proteins via glycosyl-phosphatidylinositol structures. Annu Rev Biochem. 1988;57:285–320. [PubMed]
  • Gallin WJ, Edelman GM, Cunningham BA. Characterization of L-CAM, a major cell adhesion molecule from embryonic liver cells. Proc Natl Acad Sci U S A. 1983 Feb;80(4):1038–1042. [PMC free article] [PubMed]
  • Gallin WJ, Prediger EA, Edelman GM, Cunningham BA. Isolation of a cDNA clone for the liver cell adhesion molecule (L-CAM). Proc Natl Acad Sci U S A. 1985 May;82(9):2809–2813. [PMC free article] [PubMed]
  • Gallin WJ, Sorkin BC, Edelman GM, Cunningham BA. Sequence analysis of a cDNA clone encoding the liver cell adhesion molecule, L-CAM. Proc Natl Acad Sci U S A. 1987 May;84(9):2808–2812. [PMC free article] [PubMed]
  • Gibralter D, Turner DC. Dual adhesion systems of chick myoblasts. Dev Biol. 1985 Dec;112(2):292–307. [PubMed]
  • Grumet M, Rutishauser U, Edelman GM. Neural cell adhesion molecule is on embryonic muscle cells and mediates adhesion to nerve cells in vitro. Nature. 1982 Feb 25;295(5851):693–695. [PubMed]
  • Grunwald GB, Geller RL, Lilien J. Enzymatic dissection of embryonic cell adhesive mechanisms. J Cell Biol. 1980 Jun;85(3):766–776. [PMC free article] [PubMed]
  • Hatta K, Takeichi M. Expression of N-cadherin adhesion molecules associated with early morphogenetic events in chick development. Nature. 1986 Apr 3;320(6061):447–449. [PubMed]
  • He HT, Barbet J, Chaix JC, Goridis C. Phosphatidylinositol is involved in the membrane attachment of NCAM-120, the smallest component of the neural cell adhesion molecule. EMBO J. 1986 Oct;5(10):2489–2494. [PMC free article] [PubMed]
  • Hemperly JJ, Edelman GM, Cunningham BA. cDNA clones of the neural cell adhesion molecule (N-CAM) lacking a membrane-spanning region consistent with evidence for membrane attachment via a phosphatidylinositol intermediate. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9822–9826. [PMC free article] [PubMed]
  • Homans SW, Ferguson MA, Dwek RA, Rademacher TW, Anand R, Williams AF. Complete structure of the glycosyl phosphatidylinositol membrane anchor of rat brain Thy-1 glycoprotein. Nature. 1988 May 19;333(6170):269–272. [PubMed]
  • Hyafil F, Morello D, Babinet C, Jacob F. A cell surface glycoprotein involved in the compaction of embryonal carcinoma cells and cleavage stage embryos. Cell. 1980 Oct;21(3):927–934. [PubMed]
  • Hyafil F, Babinet C, Jacob F. Cell-cell interactions in early embryogenesis: a molecular approach to the role of calcium. Cell. 1981 Nov;26(3 Pt 1):447–454. [PubMed]
  • Knudsen KA. The calcium-dependent myoblast adhesion that precedes cell fusion is mediated by glycoproteins. J Cell Biol. 1985 Sep;101(3):891–897. [PMC free article] [PubMed]
  • Knudsen KA, Horwitz AF. Tandem events in myoblast fusion. Dev Biol. 1977 Jul 15;58(2):328–338. [PubMed]
  • Knudsen KA, Horwitz AF. Differential inhibition of myoblast fusion. Dev Biol. 1978 Oct;66(2):294–307. [PubMed]
  • Knudsen KA, Rao PE, Damsky CH, Buck CA. Membrane glycoproteins involved in cell--substratum adhesion. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6071–6075. [PMC free article] [PubMed]
  • Knudsen KA, Horwitz AF, Buck CA. A monoclonal antibody identifies a glycoprotein complex involved in cell-substratum adhesion. Exp Cell Res. 1985 Mar;157(1):218–226. [PubMed]
  • Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. [PubMed]
  • Lesley JF, Lennon VA. Transitory expression of Thy-1 antigen in skeletal muscle development. Nature. 1977 Jul 14;268(5616):163–165. [PubMed]
  • Low MG. Biochemistry of the glycosyl-phosphatidylinositol membrane protein anchors. Biochem J. 1987 May 15;244(1):1–13. [PMC free article] [PubMed]
  • Low MG, Saltiel AR. Structural and functional roles of glycosyl-phosphatidylinositol in membranes. Science. 1988 Jan 15;239(4837):268–275. [PubMed]
  • Low MG, Stiernberg J, Waneck GL, Flavell RA, Kincade PW. Cell-specific heterogeneity in sensitivity of phosphatidylinositol-anchored membrane antigens to release by phospholipase C. J Immunol Methods. 1988 Oct 4;113(1):101–111. [PubMed]
  • Magnani JL, Thomas WA, Steinberg MS. Two distinct adhesion mechanisms in embryonic neural retina cells. I. A kinetic analysis. Dev Biol. 1981 Jan 15;81(1):96–105. [PubMed]
  • Menko AS, Boettiger D. Occupation of the extracellular matrix receptor, integrin, is a control point for myogenic differentiation. Cell. 1987 Oct 9;51(1):51–57. [PubMed]
  • Moore SE, Thompson J, Kirkness V, Dickson JG, Walsh FS. Skeletal muscle neural cell adhesion molecule (N-CAM): changes in protein and mRNA species during myogenesis of muscle cell lines. J Cell Biol. 1987 Sep;105(3):1377–1386. [PMC free article] [PubMed]
  • Nameroff M, Munar E. Inhibition of cellular differentiation by phospholipase C. II. Separation of fusion and recognition among myogenic cells. Dev Biol. 1976 Mar;49(1):288–293. [PubMed]
  • Nameroff M, Trotter JA, Keller JM, Munar E. Inhibition of cellular differentiation by phospholipase C. I. Effects of the enzyme on myogenesis and chondrogenesis in vitro. J Cell Biol. 1973 Jul;58(1):107–118. [PMC free article] [PubMed]
  • Neff NT, Lowrey C, Decker C, Tovar A, Damsky C, Buck C, Horwitz AF. A monoclonal antibody detaches embryonic skeletal muscle from extracellular matrices. J Cell Biol. 1982 Nov;95(2 Pt 1):654–666. [PMC free article] [PubMed]
  • Nishizuka Y. Studies and perspectives of protein kinase C. Science. 1986 Jul 18;233(4761):305–312. [PubMed]
  • Nose A, Takeichi M. A novel cadherin cell adhesion molecule: its expression patterns associated with implantation and organogenesis of mouse embryos. J Cell Biol. 1986 Dec;103(6 Pt 2):2649–2658. [PMC free article] [PubMed]
  • Pizzey JA, Jones GE, Walsh FS. Requirements for the Ca2+-independent component in the initial intercellular adhesion of C2 myoblasts. J Cell Biol. 1988 Dec;107(6 Pt 1):2307–2317. [PMC free article] [PubMed]
  • Rieger F, Grumet M, Edelman GM. N-CAM at the vertebrate neuromuscular junction. J Cell Biol. 1985 Jul;101(1):285–293. [PMC free article] [PubMed]
  • Ringwald M, Schuh R, Vestweber D, Eistetter H, Lottspeich F, Engel J, Dölz R, Jähnig F, Epplen J, Mayer S, et al. The structure of cell adhesion molecule uvomorulin. Insights into the molecular mechanism of Ca2+-dependent cell adhesion. EMBO J. 1987 Dec 1;6(12):3647–3653. [PMC free article] [PubMed]
  • Rutishauser U, Grumet M, Edelman GM. Neural cell adhesion molecule mediates initial interactions between spinal cord neurons and muscle cells in culture. J Cell Biol. 1983 Jul;97(1):145–152. [PMC free article] [PubMed]
  • Rutishauser U, Acheson A, Hall AK, Mann DM, Sunshine J. The neural cell adhesion molecule (NCAM) as a regulator of cell-cell interactions. Science. 1988 Apr 1;240(4848):53–57. [PubMed]
  • Schweitzer JS, Dichter MA, Kaufman SJ. Fibroblasts modulate expression of Thy-1 on the surface of skeletal myoblasts. Exp Cell Res. 1987 Sep;172(1):1–20. [PubMed]
  • Sefton BM, Buss JE. The covalent modification of eukaryotic proteins with lipid. J Cell Biol. 1987 Jun;104(6):1449–1453. [PMC free article] [PubMed]
  • Shainberg A, Yagil G, Yaffe D. Control of myogenesis in vitro by Ca 2 + concentration in nutritional medium. Exp Cell Res. 1969 Nov;58(1):163–167. [PubMed]
  • Takeichi M. Functional correlation between cell adhesive properties and some cell surface proteins. J Cell Biol. 1977 Nov;75(2 Pt 1):464–474. [PMC free article] [PubMed]
  • Takeichi M. The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development. 1988 Apr;102(4):639–655. [PubMed]
  • Thomas WA, Steinberg MS. Two distinct adhesion mechanisms in embryonic neural retina cells. II. An immunological analysis. Dev Biol. 1981 Jan 15;81(1):106–114. [PubMed]
  • Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. [PMC free article] [PubMed]
  • Vestweber D, Kemler R. Identification of a putative cell adhesion domain of uvomorulin. EMBO J. 1985 Dec 16;4(13A):3393–3398. [PMC free article] [PubMed]
  • Volk T, Geiger B. A 135-kd membrane protein of intercellular adherens junctions. EMBO J. 1984 Oct;3(10):2249–2260. [PMC free article] [PubMed]
  • Wakelam MJ. The fusion of myoblasts. Biochem J. 1985 May 15;228(1):1–12. [PMC free article] [PubMed]
  • Wheelock MJ, Buck CA, Bechtol KB, Damsky CH. Soluble 80-kd fragment of cell-CAM 120/80 disrupts cell-cell adhesion. J Cell Biochem. 1987 Jul;34(3):187–202. [PubMed]
  • Yoshida-Noro C, Suzuki N, Takeichi M. Molecular nature of the calcium-dependent cell-cell adhesion system in mouse teratocarcinoma and embryonic cells studied with a monoclonal antibody. Dev Biol. 1984 Jan;101(1):19–27. [PubMed]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

  • Compound
    Compound
    PubChem Compound links
  • MedGen
    MedGen
    Related information in MedGen
  • PubMed
    PubMed
    PubMed citations for these articles
  • Substance
    Substance
    PubChem Substance links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...