Logo of jcellbiolHomeThe Rockefeller University PressEditorsContactInstructions for AuthorsThis issue
J Cell Biol. May 1, 1990; 110(5): 1681–1691.
PMCID: PMC2200163

Evidence for export of a muscle lectin from cytosol to extracellular matrix and for a novel secretory mechanism

Abstract

A soluble lactose-binding lectin with subunit Mr of 14,500 is believed to function by interacting with extracellular glycoconjugates, because it has been detected extracellularly by immunohistochemistry. This localization has been questioned, however, since the lectin lacks a secretion signal sequence, which challenges the contention that it is secreted. We have demonstrated externalization of this lectin from C2 mouse muscle cells by both immunoprecipitation of metabolically labeled protein and immunohistochemical localization. We further show that externalization of the lectin is a developmentally regulated process that accompanies myoblast differentiation and that the lectin codistributes with laminin in myotube extracellular matrix. Immunohistochemical localization during intermediate stages of externalization suggests that the lectin becomes concentrated in evaginations of plasma membrane, which pinch off to form labile lectin- rich extracellular vesicles. This suggests a possible mechanism for lectin export from the cytosol to the extracellular matrix.

Full Text

The Full Text of this article is available as a PDF (2.3M).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Abbott WM, Feizi T. Evidence that the 14 kDa soluble beta-galactoside-binding lectin in man is encoded by a single gene. Biochem J. 1989 Apr 1;259(1):291–294. [PMC free article] [PubMed]
  • Abbott WM, Mellor A, Edwards Y, Feizi T. Soluble bovine galactose-binding lectin. cDNA cloning reveals the complete amino acid sequence and an antigenic relationship with the major encephalitogenic domain of myelin basic protein. Biochem J. 1989 Apr 1;259(1):283–290. [PMC free article] [PubMed]
  • Abraham JA, Mergia A, Whang JL, Tumolo A, Friedman J, Hjerrild KA, Gospodarowicz D, Fiddes JC. Nucleotide sequence of a bovine clone encoding the angiogenic protein, basic fibroblast growth factor. Science. 1986 Aug 1;233(4763):545–548. [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]
  • Bakouche O, Brown DC, Lachman LB. Subcellular localization of human monocyte interleukin 1: evidence for an inactive precursor molecule and a possible mechanism for IL 1 release. J Immunol. 1987 Jun 15;138(12):4249–4255. [PubMed]
  • Barondes SH. Soluble lectins: a new class of extracellular proteins. Science. 1984 Mar 23;223(4642):1259–1264. [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, Tokuyasu KT, Barondes SH. Localization of an endogenous lectin in chicken liver, intestine, and pancreas. J Cell Biol. 1979 Aug;82(2):565–571. [PMC free article] [PubMed]
  • Catt JW, Harrison FL. Selective association of an endogenous lectin with connective tissues. J Cell Sci. 1985 Feb;73:347–359. [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, Haywood-Reid PL, Barondes SH. Endogenous mammalian lectin localized extracellularly in lung elastic fibers. J Cell Biol. 1984 Apr;98(4):1580–1589. [PMC free article] [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]
  • Clerch LB, Whitney P, Hass M, Brew K, Miller T, Werner R, Massaro D. Sequence of a full-length cDNA for rat lung beta-galactoside-binding protein: primary and secondary structure of the lectin. Biochemistry. 1988 Jan 26;27(2):692–699. [PubMed]
  • Clinton M, Frangou-Lazaridis M, Panneerselvam C, Horecker BL. The sequence of human parathymosin deduced from a cloned human kidney cDNA. Biochem Biophys Res Commun. 1989 Feb 15;158(3):855–862. [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]
  • 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]
  • Didier E, Didier P, Bayle D, Chevalier M. Lectin activity and distribution of chicken lactose lectin I in the extracellular matrix of the chick developing kidney. Cell Differ. 1988 Jul;24(2):83–95. [PubMed]
  • Dixon SJ, Pitaru S, Bhargava U, Aubin JE. Membrane blebbing is associated with Ca2+-activated hyperpolarizations induced by serum and alpha 2-macroglobulin. J Cell Physiol. 1987 Sep;132(3):473–482. [PubMed]
  • Gitt MA, Barondes SH. Evidence that a human soluble beta-galactoside-binding lectin is encoded by a family of genes. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7603–7607. [PMC free article] [PubMed]
  • Goodall GJ, Dominguez F, Horecker BL. Molecular cloning of cDNA for human prothymosin alpha. Proc Natl Acad Sci U S A. 1986 Dec;83(23):8926–8928. [PMC free article] [PubMed]
  • Haigler HT, Fitch JM, Jones JM, Schlaepfer DD. Two lipocortin-like proteins, endonexin II and anchorin CII, may be alternate splices of the same gene. Trends Biochem Sci. 1989 Feb;14(2):48–50. [PubMed]
  • Hale JE, Wuthier RE. The mechanism of matrix vesicle formation. Studies on the composition of chondrocyte microvilli and on the effects of microfilament-perturbing agents on cellular vesiculation. J Biol Chem. 1987 Feb 5;262(4):1916–1925. [PubMed]
  • Hirabayashi J, Kawasaki H, Suzuki K, Kasai K. Complete amino acid sequence of 14 kDa beta-galactoside-binding lectin of chick embryo. J Biochem. 1987 Mar;101(3):775–787. [PubMed]
  • Hirabayashi J, Kawasaki H, Suzuki K, Kasai K. Further characterization and structural studies on human placenta lectin. J Biochem. 1987 Apr;101(4):987–995. [PubMed]
  • Hosokawa R, Uchida Y, Fujiwara S, Noguchi T. Lactate dehydrogenase isoenzymes are present in matrix vesicles. J Biol Chem. 1988 Jul 25;263(21):10045–10047. [PubMed]
  • Janet T, Miehe M, Pettmann B, Labourdette G, Sensenbrenner M. Ultrastructural localization of fibroblast growth factor in neurons of rat brain. Neurosci Lett. 1987 Sep 23;80(2):153–157. [PubMed]
  • Jaye M, Howk R, Burgess W, Ricca GA, Chiu IM, Ravera MW, O'Brien SJ, Modi WS, Maciag T, Drohan WN. Human endothelial cell growth factor: cloning, nucleotide sequence, and chromosome localization. Science. 1986 Aug 1;233(4763):541–545. [PubMed]
  • Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem. 1987 Jul 5;262(19):9412–9420. [PubMed]
  • Kaufman SJ, Foster RF, Haye KR, Faiman LE. Expression of a developmentally regulated antigen on the surface of skeletal and cardiac muscle cells. J Cell Biol. 1985 Jun;100(6):1977–1987. [PMC free article] [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]
  • Levi G, Teichberg VI. Isolation and physicochemical characterization of electrolectin, a beta-D-galactoside binding lectin from the electric organ of Electrophorus electricus. J Biol Chem. 1981 Jun 10;256(11):5735–5740. [PubMed]
  • Liepins A, Younghusband HB. Low temperature-induced cell surface membrane vesicle shedding is associated with DNA fragmentation. Exp Cell Res. 1985 Dec;161(2):525–532. [PubMed]
  • Lipsick JS, Beyer EC, Barondes SH, Kaplan NO. Lectins from chicken tissues are mitogenic for Thy-1 negative murine spleen cells. Biochem Biophys Res Commun. 1980 Nov 17;97(1):56–61. [PubMed]
  • LOWRY OH, ROSEBROUGH NJ, FARR AL, RANDALL RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed]
  • March CJ, Mosley B, Larsen A, Cerretti DP, Braedt G, Price V, Gillis S, Henney CS, Kronheim SR, Grabstein K, et al. Cloning, sequence and expression of two distinct human interleukin-1 complementary DNAs. Nature. 1985 Jun 20;315(6021):641–647. [PubMed]
  • McNeil PL, Muthukrishnan L, Warder E, D'Amore PA. Growth factors are released by mechanically wounded endothelial cells. J Cell Biol. 1989 Aug;109(2):811–822. [PMC free article] [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]
  • 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]
  • Oda Y, Ohyama Y, Obinata A, Endo H, Kasai K. Endogenous beta-galactoside-binding lectin expression is suppressed in retinol-induced mucous metaplasia of chick embryonic epidermis. Exp Cell Res. 1989 May;182(1):33–43. [PubMed]
  • Ohyama Y, Hirabayashi J, Oda Y, Ohno S, Kawasaki H, Suzuki K, Kasai K. Nucleotide sequence of chick 14K beta-galactoside-binding lectin mRNA. Biochem Biophys Res Commun. 1986 Jan 14;134(1):51–56. [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]
  • Pfäffle M, Ruggiero F, Hofmann H, Fernández MP, Selmin O, Yamada Y, Garrone R, von der Mark K. Biosynthesis, secretion and extracellular localization of anchorin CII, a collagen-binding protein of the calpactin family. EMBO J. 1988 Aug;7(8):2335–2342. [PMC free article] [PubMed]
  • Pitts MJ, Yang DC. Mitogenicity and binding properties of beta-galactoside-binding lectin from chick-embryo kidney. Biochem J. 1981 May 1;195(2):435–439. [PMC free article] [PubMed]
  • Powell JT. Evidence against lung galaptin being important to the synthesis or organization of the elastic fibril. Biochem J. 1988 Jun 1;252(2):447–452. [PMC free article] [PubMed]
  • Raz A, Carmi P, Pazerini G. Expression of two different endogenous galactoside-binding lectins sharing sequence homology. Cancer Res. 1988 Feb 1;48(3):645–649. [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]
  • Scott RE. Plasma membrane vesiculation: a new technique for isolation of plasma membranes. Science. 1976 Nov 12;194(4266):743–745. [PubMed]
  • Singer II, Scott S, Hall GL, Limjuco G, Chin J, Schmidt JA. Interleukin 1 beta is localized in the cytoplasmic ground substance but is largely absent from the Golgi apparatus and plasma membranes of stimulated human monocytes. J Exp Med. 1988 Feb 1;167(2):389–407. [PMC free article] [PubMed]
  • Whitney P, Maxwell S, Ryan U, Massaro D. Synthesis and binding of lactose-specific lectin by isolated lung cells. Am J Physiol. 1985 Mar;248(3 Pt 1):C258–C264. [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. [PMC free article] [PubMed]
  • Wilson TJ, Firth MN, Powell JT, Harrison FL. The sequence of the mouse 14 kDa beta-galactoside-binding lectin and evidence for its synthesis on free cytoplasmic ribosomes. Biochem J. 1989 Aug 1;261(3):847–852. [PMC free article] [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

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...