PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of jcellbiolHomeThe Rockefeller University PressEditorsContactInstructions for AuthorsThis issue
 
J Cell Biol. 1991 December 1; 115(5): 1437–1448.
PMCID: PMC2289239

Endogenous muscle lectin inhibits myoblast adhesion to laminin

Abstract

L-14, a dimeric lactose-binding lectin with subunits of 14 kD, is expressed in a wide range of vertebrate tissues. Several functions have been postulated for this lectin, but definitive evidence for a specific biological role has been elusive. In muscle, L-14 is secreted during differentiation and accumulates with laminin in basement membrane surrounding each myofiber. Here we present evidence that laminin is a major glycoprotein ligand for L-14 in differentiating mouse C2C12 muscle cells and that binding of secreted L-14 to polylactosamine oligosaccharides of substrate laminin induces loss of cell-substratum adhesion. These results suggest that one function of L-14 is to regulate myoblast detachment from laminin during differentiation and fusion into tubular myofibers.

Full Text

The Full Text of this article is available as a PDF (1.5M).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Abbott WM, Hounsell EF, Feizi T. Further studies of oligosaccharide recognition by the soluble 13 kDa lectin of bovine heart muscle. Ability to accommodate the blood-group-H and -B-related sequences. Biochem J. 1988 May 15;252(1):283–287. [PubMed]
  • Arumugham RG, Hsieh TC, Tanzer ML, Laine RA. Structures of the asparagine-linked sugar chains of laminin. Biochim Biophys Acta. 1986 Aug 6;883(1):112–126. [PubMed]
  • Barondes SH. Soluble lectins: a new class of extracellular proteins. Science. 1984 Mar 23;223(4642):1259–1264. [PubMed]
  • Barondes SH. Bifunctional properties of lectins: lectins redefined. Trends Biochem Sci. 1988 Dec;13(12):480–482. [PubMed]
  • Barondes SH, Haywood-Reid PL. Externalization of an endogenous chicken muscle lectin with in vivo development. J Cell Biol. 1981 Nov;91(2 Pt 1):568–572. [PMC free article] [PubMed]
  • Beyer EC, Barondes SH. Quantitation of two endogenous lactose-inhibitable lectins in embryonic and adult chicken tissues. J Cell Biol. 1982 Jan;92(1):23–27. [PMC free article] [PubMed]
  • Blau HM, Chiu CP, Webster C. Cytoplasmic activation of human nuclear genes in stable heterocaryons. Cell. 1983 Apr;32(4):1171–1180. [PubMed]
  • Bouzon M, Dussert C, Lissitzky JC, Martin PM. Spreading of B16 F1 cells on laminin and its proteolytic fragments P1 and E8: involvement of laminin carbohydrate chains. Exp Cell Res. 1990 Sep;190(1):47–56. [PubMed]
  • Catt JW, Harrison FL, Carleton JS. Distribution of an endogenous beta-galactoside-specific lectin during foetal and neonatal rabbit development. J Cell Sci. 1987 Jun;87(Pt 5):623–633. [PubMed]
  • Cerra RF, Gitt MA, Barondes SH. Three soluble rat beta-galactoside-binding lectins. J Biol Chem. 1985 Sep 5;260(19):10474–10477. [PubMed]
  • Childs RA, Feizi T. beta-Galactoside-binding muscle lectins of man and monkey show antigenic cross-reactions with those of bovine origin. Biochem J. 1979 Dec 1;183(3):755–758. [PubMed]
  • Cooper DN, Barondes SH. Colocalization of discoidin-binding ligands with discoidin in developing Dictyostelium discoideum. Dev Biol. 1984 Sep;105(1):59–70. [PubMed]
  • Cooper DN, Barondes SH. Evidence for export of a muscle lectin from cytosol to extracellular matrix and for a novel secretory mechanism. J Cell Biol. 1990 May;110(5):1681–1691. [PMC free article] [PubMed]
  • Couraud PO, Casentini-Borocz D, Bringman TS, Griffith J, McGrogan M, Nedwin GE. Molecular cloning, characterization, and expression of a human 14-kDa lectin. J Biol Chem. 1989 Jan 15;264(2):1310–1316. [PubMed]
  • Cullen BR. Use of eukaryotic expression technology in the functional analysis of cloned genes. Methods Enzymol. 1987;152:684–704. [PubMed]
  • Dean JW, 3rd, Chandrasekaran S, Tanzer ML. A biological role of the carbohydrate moieties of laminin. J Biol Chem. 1990 Jul 25;265(21):12553–12562. [PubMed]
  • Den H, Malinzak DA. Isolation and properties of beta-D-galactoside-specific lectin from chick embryo thigh muscle. J Biol Chem. 1977 Aug 10;252(15):5444–5448. [PubMed]
  • Den H, Chin JH. Endogenous lectin from chick embryo skeletal muscle is not involved in myotube formation in vitro. J Biol Chem. 1981 Aug 10;256(15):8069–8073. [PubMed]
  • Den H, Malinzak DA, Rosenberg A. Lack of evidence for the involvement of a beta-D-galactosyl-specific lectin in the fusion of chick myoblasts. Biochem Biophys Res Commun. 1976 Apr 5;69(3):621–627. [PubMed]
  • de Waard A, Hickman S, Kornfeld S. Isolation and properties of beta-galactoside binding lectins of calf heart and lung. J Biol Chem. 1976 Dec 10;251(23):7581–7587. [PubMed]
  • Drickamer K. Two distinct classes of carbohydrate-recognition domains in animal lectins. J Biol Chem. 1988 Jul 15;263(20):9557–9560. [PubMed]
  • Foster RF, Thompson JM, Kaufman SJ. A laminin substrate promotes myogenesis in rat skeletal muscle cultures: analysis of replication and development using antidesmin and anti-BrdUrd monoclonal antibodies. Dev Biol. 1987 Jul;122(1):11–20. [PubMed]
  • Fujiwara S, Shinkai H, Deutzmann R, Paulsson M, Timpl R. Structure and distribution of N-linked oligosaccharide chains on various domains of mouse tumour laminin. Biochem J. 1988 Jun 1;252(2):453–461. [PubMed]
  • Gartner TK, Podleski TR. Evidence that the types and specific activity of lectins control fusion of L6 myoblasts. Biochem Biophys Res Commun. 1976 Jun 21;70(4):1142–1149. [PubMed]
  • Goodman SL, Deutzmann R, Nurcombe V. Locomotory competence and laminin-specific cell surface binding sites are lost during myoblast differentiation. Development. 1989 Apr;105(4):795–802. [PubMed]
  • Goodman SL, Risse G, von der Mark K. The E8 subfragment of laminin promotes locomotion of myoblasts over extracellular matrix. J Cell Biol. 1989 Aug;109(2):799–809. [PMC free article] [PubMed]
  • Goring DR, Rossant J, Clapoff S, Breitman ML, Tsui LC. In situ detection of beta-galactosidase in lenses of transgenic mice with a gamma-crystallin/lacZ gene. Science. 1987 Jan 23;235(4787):456–458. [PubMed]
  • Greve JM, Gottlieb DI. Monoclonal antibodies which alter the morphology of cultured chick myogenic cells. J Cell Biochem. 1982;18(2):221–229. [PubMed]
  • Gunning P, Leavitt J, Muscat G, Ng SY, Kedes L. A human beta-actin expression vector system directs high-level accumulation of antisense transcripts. Proc Natl Acad Sci U S A. 1987 Jul;84(14):4831–4835. [PubMed]
  • Hinek A, Wrenn DS, Mecham RP, Barondes SH. The elastin receptor: a galactoside-binding protein. Science. 1988 Mar 25;239(4847):1539–1541. [PubMed]
  • Hirabayashi J, Ayaki H, Soma G, Kasai K. Production and purification of a recombinant human 14 kDa beta-galactoside-binding lectin. FEBS Lett. 1989 Jul 3;250(2):161–165. [PubMed]
  • Hynes MA, Gitt M, Barondes SH, Jessell TM, Buck LB. Selective expression of an endogenous lactose-binding lectin gene in subsets of central and peripheral neurons. J Neurosci. 1990 Mar;10(3):1004–1013. [PubMed]
  • Kaufman SJ, Lawless ML. Thiodigalactoside binding lectin and skeletal myogenesis. Differentiation. 1980 Feb;16(1):41–48. [PubMed]
  • Klagsbrun M. The affinity of fibroblast growth factors (FGFs) for heparin; FGF-heparan sulfate interactions in cells and extracellular matrix. Curr Opin Cell Biol. 1990 Oct;2(5):857–863. [PubMed]
  • Kleinman HK, Weeks BS. Laminin: structure, functions and receptors. Curr Opin Cell Biol. 1989 Oct;1(5):964–967. [PubMed]
  • Knibbs RN, Perini F, Goldstein IJ. Structure of the major concanavalin A reactive oligosaccharides of the extracellular matrix component laminin. Biochemistry. 1989 Jul 25;28(15):6379–6392. [PubMed]
  • Knudsen KA. Cell adhesion molecules in myogenesis. Curr Opin Cell Biol. 1990 Oct;2(5):902–906. [PubMed]
  • Knudsen KA, Horwitz AF. Differential inhibition of myoblast fusion. Dev Biol. 1978 Oct;66(2):294–307. [PubMed]
  • Kühl U, Timpl R, von der Mark K. Synthesis of type IV collagen and laminin in cultures of skeletal muscle cells and their assembly on the surface of myotubes. Dev Biol. 1982 Oct;93(2):344–354. [PubMed]
  • Kühl U, Ocalan M, Timpl R, Mayne R, Hay E, von der Mark K. Role of muscle fibroblasts in the deposition of type-IV collagen in the basal lamina of myotubes. Differentiation. 1984;28(2):164–172. [PubMed]
  • Kurachi K, Chandra T, Degen SJ, White TT, Marchioro TL, Woo SL, Davie EW. Cloning and sequence of cDNA coding for alpha 1-antitrypsin. Proc Natl Acad Sci U S A. 1981 Nov;78(11):6826–6830. [PubMed]
  • Leffler H, Barondes SH. Specificity of binding of three soluble rat lung lectins to substituted and unsubstituted mammalian beta-galactosides. J Biol Chem. 1986 Aug 5;261(22):10119–10126. [PubMed]
  • Leffler H, Masiarz FR, Barondes SH. Soluble lactose-binding vertebrate lectins: a growing family. Biochemistry. 1989 Nov 14;28(23):9222–9229. [PubMed]
  • Lesot H, Kühl U, Mark K. Isolation of a laminin-binding protein from muscle cell membranes. EMBO J. 1983;2(6):861–865. [PubMed]
  • MacBride RG, Przybylski RJ. Purified lectin from skeletal muscle inhibits myotube formation in vitro. J Cell Biol. 1980 Jun;85(3):617–625. [PMC free article] [PubMed]
  • MacBride RG, Przybylski RJ. Chicken lactose lectin: cell-to-cell or cell-to-matrix adhesion molecule? In Vitro Cell Dev Biol. 1986 Oct;22(10):568–574. [PubMed]
  • Mayne R, Sanderson RD. The extracellular matrix of skeletal muscle. Coll Relat Res. 1985 Nov;5(5):449–468. [PubMed]
  • Mecham RP, Hinek A, Griffin GL, Senior RM, Liotta LA. The elastin receptor shows structural and functional similarities to the 67-kDa tumor cell laminin receptor. J Biol Chem. 1989 Oct 5;264(28):16652–16657. [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]
  • Mercurio AM. Laminin: multiple forms, multiple receptors. Curr Opin Cell Biol. 1990 Oct;2(5):845–849. [PubMed]
  • Merkle RK, Cummings RD. Asparagine-linked oligosaccharides containing poly-N-acetyllactosamine chains are preferentially bound by immobilized calf heart agglutinin. J Biol Chem. 1988 Nov 5;263(31):16143–16149. [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]
  • Nowak TP, Haywood PL, Barondes SH. Developmentally regulated lectin in embryonic chick muscle and a myogenic cell line. Biochem Biophys Res Commun. 1976 Feb 9;68(3):650–657. [PubMed]
  • Nowak TP, Kobiler D, Roel LE, Barondes SH. Developmentally regulated lectin from embryonic chick pectoral muscle. Purification by affinity chromatography. J Biol Chem. 1977 Sep 10;252(17):6026–6030. [PubMed]
  • Ocalan M, Goodman SL, Kühl U, Hauschka SD, von der Mark K. Laminin alters cell shape and stimulates motility and proliferation of murine skeletal myoblasts. Dev Biol. 1988 Jan;125(1):158–167. [PubMed]
  • Oda Y, Kasai K. Photochemical cross-linking of beta-galactoside-binding lectin to polylactosamino-proteoglycan of chick embryonic skin. Biochem Biophys Res Commun. 1984 Sep 28;123(3):1215–1220. [PubMed]
  • Offner H, Celnik B, Bringman TS, Casentini-Borocz D, Nedwin GE, Vandenbark AA. Recombinant human beta-galactoside binding lectin suppresses clinical and histological signs of experimental autoimmune encephalomyelitis. J Neuroimmunol. 1990 Jul;28(2):177–184. [PubMed]
  • Olwin BB, Hall ZW. Developmental regulation of laminin accumulation in the extracellular matrix of a mouse muscle cell line. Dev Biol. 1985 Dec;112(2):359–367. [PubMed]
  • Picard D, Yamamoto KR. Two signals mediate hormone-dependent nuclear localization of the glucocorticoid receptor. EMBO J. 1987 Nov;6(11):3333–3340. [PubMed]
  • Podleski TR, Greenberg I, Schlessinger J, Yamada KM. Fibronectin delays the fusion of L6 myoblasts. Exp Cell Res. 1979 Sep;122(2):317–326. [PubMed]
  • Powell JT, Whitney PL. Endogenous ligands of rat lung beta-galactoside-binding protein (galaptin) isolated by affinity chromatography on carboxyamidomethylated-galaptin-Sepharose. Biochem J. 1984 Nov 1;223(3):769–774. [PubMed]
  • Regan LJ, Dodd J, Barondes SH, Jessell TM. Selective expression of endogenous lactose-binding lectins and lactoseries glycoconjugates in subsets of rat sensory neurons. Proc Natl Acad Sci U S A. 1986 Apr;83(7):2248–2252. [PubMed]
  • Rogelj S, Weinberg RA, Fanning P, Klagsbrun M. Basic fibroblast growth factor fused to a signal peptide transforms cells. Nature. 1988 Jan 14;331(6152):173–175. [PubMed]
  • Rogers J, Kalsheker N, Wallis S, Speer A, Coutelle CH, Woods D, Humphries SE. The isolation of a clone for human alpha 1-antitrypsin and the detection of alpha 1-antitrypsin in mRNA from liver and leukocytes. Biochem Biophys Res Commun. 1983 Oct 31;116(2):375–382. [PubMed]
  • Rosen SD. The LEC-CAMs: an emerging family of cell-cell adhesion receptors based upon carbohydrate recognition. Am J Respir Cell Mol Biol. 1990 Nov;3(5):397–402. [PubMed]
  • Sanes JR, Schachner M, Covault J. Expression of several adhesive macromolecules (N-CAM, L1, J1, NILE, uvomorulin, laminin, fibronectin, and a heparan sulfate proteoglycan) in embryonic, adult, and denervated adult skeletal muscle. J Cell Biol. 1986 Feb;102(2):420–431. [PMC free article] [PubMed]
  • Sanford GL, Harris-Hooker S. Stimulation of vascular cell proliferation by beta-galactoside specific lectins. FASEB J. 1990 Aug;4(11):2912–2918. [PubMed]
  • Sephel GC, Burrous BA, Kleinman HK. Laminin neural activity and binding proteins. Dev Neurosci. 1989;11(4-5):313–331. [PubMed]
  • Sharon N, Lis H. Lectins as cell recognition molecules. Science. 1989 Oct 13;246(4927):227–234. [PubMed]
  • Shur BD. Glycoconjugates as mediators of cellular interactions during development. Curr Opin Cell Biol. 1989 Oct;1(5):905–912. [PubMed]
  • Springer TA. The sensation and regulation of interactions with the extracellular environment: the cell biology of lymphocyte adhesion receptors. Annu Rev Cell Biol. 1990;6:359–402. [PubMed]
  • Springer WR, Cooper DN, Barondes SH. Discoidin I is implicated in cell-substratum attachment and ordered cell migration of Dictyostelium discoideum and resembles fibronectin. Cell. 1984 Dec;39(3 Pt 2):557–564. [PubMed]
  • Studier FW, Rosenberg AH, Dunn JJ, Dubendorff JW. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 1990;185:60–89. [PubMed]
  • Teichberg VI, Aberdam D, Erez U, Pinelli E. Affinity-repulsion chromatography. Principle and application to lectins. J Biol Chem. 1988 Oct 5;263(28):14086–14092. [PubMed]
  • Travis J, Salvesen GS. Human plasma proteinase inhibitors. Annu Rev Biochem. 1983;52:655–709. [PubMed]
  • Verbanac KM, Heath EC. Biosynthesis, processing, and secretion of M and Z variant human alpha 1-antitrypsin. J Biol Chem. 1986 Jul 25;261(21):9979–9989. [PubMed]
  • von der Mark K, Ocalan M. Antagonistic effects of laminin and fibronectin on the expression of the myogenic phenotype. Differentiation. 1989 May;40(2):150–157. [PubMed]
  • Walter P, Lingappa VR. Mechanism of protein translocation across the endoplasmic reticulum membrane. Annu Rev Cell Biol. 1986;2:499–516. [PubMed]
  • Wasano K, Hirakawa Y, Yamamoto T. Immunohistochemical localization of 14 kDa beta-galactoside-binding lectin in various organs of rat. Cell Tissue Res. 1990 Jan;259(1):43–49. [PubMed]
  • Wells V, Mallucci L. Identification of an autocrine negative growth factor: mouse beta-galactoside-binding protein is a cytostatic factor and cell growth regulator. Cell. 1991 Jan 11;64(1):91–97. [PubMed]
  • Whitney PL, Powell JT, Sanford GL. Oxidation and chemical modification of lung beta-galactoside-specific lectin. Biochem J. 1986 Sep 15;238(3):683–689. [PubMed]
  • Woo HJ, Shaw LM, Messier JM, Mercurio AM. The major non-integrin laminin binding protein of macrophages is identical to carbohydrate binding protein 35 (Mac-2). J Biol Chem. 1990 May 5;265(13):7097–7099. [PubMed]
  • Yaffe D, Saxel O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature. 1977 Dec 22;270(5639):725–727. [PubMed]
  • Zhou Q, Cummings RD. The S-type lectin from calf heart tissue binds selectively to the carbohydrate chains of laminin. Arch Biochem Biophys. 1990 Aug 15;281(1):27–35. [PubMed]
  • Zhu BC, Laine RA. Polylactosamine glycosylation on human fetal placental fibronectin weakens the binding affinity of fibronectin to gelatin. J Biol Chem. 1985 Apr 10;260(7):4041–4045. [PubMed]

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