Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1988 Aug 1;107(2):687–697. doi: 10.1083/jcb.107.2.687

Isolation and characterization of a laminin-binding protein from rat and chick muscle

PMCID: PMC2115226  PMID: 3417768

Abstract

A major laminin-binding protein (LBP), distinct from previously described LBPs, has been isolated from chick and rat skeletal muscle (Mr 56,000 and 66,000, respectively). The purified LBPs from the two species were shown to be related antigenically and to have similar NH2- terminal amino acid sequences and total amino acid compositions. Protein blots using laminin and laminin fragments provided evidence that this LBP interacts with the major heparin-binding domain, E3, of laminin. Studies on the association of this LBP with muscle membrane fractions and reconstituted lipid vesicles indicate that this protein can interact with lipid bilayers and has properties of a peripheral, not an integral membrane protein. These properties are consistent with its amino acid sequence, determined from cDNAs (Clegg et al., 1988). Examination by light and electron microscopy of the LBP antigen distribution in skeletal muscle indicated that the protein is localized primarily extracellularly, near the extracellular matrix and myotube plasmalemma. While a form of this LBP has been identified in heart muscle, it is present at low or undetectable levels in other tissues examined by immunocytochemistry indicating that it is probably a muscle- specific protein. As this protein is localized extracellularly and can bind to both membranes and laminin, it may mediate myotube interactions with the extracellular matrix.

Full Text

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

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alcaraz G., Kinet J. P., Kumar N., Wank S. A., Metzger H. Phase separation of the receptor for immunoglobulin E and its subunits in Triton X-114. J Biol Chem. 1984 Dec 10;259(23):14922–14927. [PubMed] [Google Scholar]
  2. Anderson M. J. Nerve-induced remodeling of muscle basal lamina during synaptogenesis. J Cell Biol. 1986 Mar;102(3):863–877. doi: 10.1083/jcb.102.3.863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Antin P. B., Tokunaka S., Nachmias V. T., Holtzer H. Role of stress fiber-like structures in assembling nascent myofibrils in myosheets recovering from exposure to ethyl methanesulfonate. J Cell Biol. 1986 Apr;102(4):1464–1479. doi: 10.1083/jcb.102.4.1464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barsky S. H., Rao C. N., Hyams D., Liotta L. A. Characterization of a laminin receptor from human breast carcinoma tissue. Breast Cancer Res Treat. 1984;4(3):181–188. doi: 10.1007/BF01806483. [DOI] [PubMed] [Google Scholar]
  5. Bixby J. L., Reichardt L. F. The expression and localization of synaptic vesicle antigens at neuromuscular junctions in vitro. J Neurosci. 1985 Nov;5(11):3070–3080. doi: 10.1523/JNEUROSCI.05-11-03070.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cates G. A., Holland P. C. Biosynthesis of plasma-membrane proteins during myogenesis of skeletal muscle in vitro. Biochem J. 1978 Sep 15;174(3):873–881. doi: 10.1042/bj1740873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chiu A. Y., Sanes J. R. Development of basal lamina in synaptic and extrasynaptic portions of embryonic rat muscle. Dev Biol. 1984 Jun;103(2):456–467. doi: 10.1016/0012-1606(84)90333-6. [DOI] [PubMed] [Google Scholar]
  8. Clegg D. O., Helder J. C., Hann B. C., Hall D. E., Reichardt L. F. Amino acid sequence and distribution of mRNA encoding a major skeletal muscle laminin binding protein: an extracellular matrix-associated protein with an unusual COOH-terminal polyaspartate domain. J Cell Biol. 1988 Aug;107(2):699–705. doi: 10.1083/jcb.107.2.699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Covault J., Sanes J. R. Distribution of N-CAM in synaptic and extrasynaptic portions of developing and adult skeletal muscle. J Cell Biol. 1986 Mar;102(3):716–730. doi: 10.1083/jcb.102.3.716. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Doms R. W., Helenius A., White J. Membrane fusion activity of the influenza virus hemagglutinin. The low pH-induced conformational change. J Biol Chem. 1985 Mar 10;260(5):2973–2981. [PubMed] [Google Scholar]
  11. Edgar D., Timpl R., Thoenen H. The heparin-binding domain of laminin is responsible for its effects on neurite outgrowth and neuronal survival. EMBO J. 1984 Jul;3(7):1463–1468. doi: 10.1002/j.1460-2075.1984.tb01997.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Elder J. H., Pickett R. A., 2nd, Hampton J., Lerner R. A. Radioiodination of proteins in single polyacrylamide gel slices. Tryptic peptide analysis of all the major members of complex multicomponent systems using microgram quantities of total protein. J Biol Chem. 1977 Sep 25;252(18):6510–6515. [PubMed] [Google Scholar]
  13. Fraker P. J., Speck J. C., Jr Protein and cell membrane iodinations with a sparingly soluble chloroamide, 1,3,4,6-tetrachloro-3a,6a-diphrenylglycoluril. Biochem Biophys Res Commun. 1978 Feb 28;80(4):849–857. doi: 10.1016/0006-291x(78)91322-0. [DOI] [PubMed] [Google Scholar]
  14. Fujita-Yamaguchi Y., LeBon T. R., Tsubokawa M., Henzel W., Kathuria S., Koyal D., Ramachandran J. Comparison of insulin-like growth factor I receptor and insulin receptor purified from human placental membranes. J Biol Chem. 1986 Dec 15;261(35):16727–16731. [PubMed] [Google Scholar]
  15. Graf J., Iwamoto Y., Sasaki M., Martin G. R., Kleinman H. K., Robey F. A., Yamada Y. Identification of an amino acid sequence in laminin mediating cell attachment, chemotaxis, and receptor binding. Cell. 1987 Mar 27;48(6):989–996. doi: 10.1016/0092-8674(87)90707-0. [DOI] [PubMed] [Google Scholar]
  16. Graham R. C., Jr, Karnovsky M. J. The early stages of absorption of injected horseradish peroxidase in the proximal tubules of mouse kidney: ultrastructural cytochemistry by a new technique. J Histochem Cytochem. 1966 Apr;14(4):291–302. doi: 10.1177/14.4.291. [DOI] [PubMed] [Google Scholar]
  17. Greve J. M., Gottlieb D. I. Monoclonal antibodies which alter the morphology of cultured chick myogenic cells. J Cell Biochem. 1982;18(2):221–229. doi: 10.1002/jcb.1982.240180209. [DOI] [PubMed] [Google Scholar]
  18. Hall D. E., Neugebauer K. M., Reichardt L. F. Embryonic neural retinal cell response to extracellular matrix proteins: developmental changes and effects of the cell substratum attachment antibody (CSAT). J Cell Biol. 1987 Mar;104(3):623–634. doi: 10.1083/jcb.104.3.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hawkes R., Niday E., Gordon J. A dot-immunobinding assay for monoclonal and other antibodies. Anal Biochem. 1982 Jan 1;119(1):142–147. doi: 10.1016/0003-2697(82)90677-7. [DOI] [PubMed] [Google Scholar]
  20. Horwitz A., Duggan K., Buck C., Beckerle M. C., Burridge K. Interaction of plasma membrane fibronectin receptor with talin--a transmembrane linkage. Nature. 1986 Apr 10;320(6062):531–533. doi: 10.1038/320531a0. [DOI] [PubMed] [Google Scholar]
  21. Horwitz A., Duggan K., Greggs R., Decker C., Buck C. The cell substrate attachment (CSAT) antigen has properties of a receptor for laminin and fibronectin. J Cell Biol. 1985 Dec;101(6):2134–2144. doi: 10.1083/jcb.101.6.2134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hynes R. O. Integrins: a family of cell surface receptors. Cell. 1987 Feb 27;48(4):549–554. doi: 10.1016/0092-8674(87)90233-9. [DOI] [PubMed] [Google Scholar]
  23. Kessler S. W. Use of protein A-bearing staphylococci for the immunoprecipitation and isolation of antigens from cells. Methods Enzymol. 1981;73(Pt B):442–459. doi: 10.1016/0076-6879(81)73084-2. [DOI] [PubMed] [Google Scholar]
  24. 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. doi: 10.1016/0012-1606(82)90122-1. [DOI] [PubMed] [Google Scholar]
  25. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  26. Lesot H., Kühl U., Mark K. Isolation of a laminin-binding protein from muscle cell membranes. EMBO J. 1983;2(6):861–865. doi: 10.1002/j.1460-2075.1983.tb01514.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Liotta L. A., Horan Hand P., Rao C. N., Bryant G., Barsky S. H., Schlom J. Monoclonal antibodies to the human laminin receptor recognize structurally distinct sites. Exp Cell Res. 1985 Jan;156(1):117–126. doi: 10.1016/0014-4827(85)90266-6. [DOI] [PubMed] [Google Scholar]
  28. Liotta L. A., Rao C. N., Wewer U. M. Biochemical interactions of tumor cells with the basement membrane. Annu Rev Biochem. 1986;55:1037–1057. doi: 10.1146/annurev.bi.55.070186.005133. [DOI] [PubMed] [Google Scholar]
  29. Maher P. A., Singer S. J. Anomalous interaction of the acetylcholine receptor protein with the nonionic detergent Triton X-114. Proc Natl Acad Sci U S A. 1985 Feb;82(4):958–962. doi: 10.1073/pnas.82.4.958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Malinoff H. L., Wicha M. S. Isolation of a cell surface receptor protein for laminin from murine fibrosarcoma cells. J Cell Biol. 1983 May;96(5):1475–1479. doi: 10.1083/jcb.96.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Matthew W. D., Tsavaler L., Reichardt L. F. Identification of a synaptic vesicle-specific membrane protein with a wide distribution in neuronal and neurosecretory tissue. J Cell Biol. 1981 Oct;91(1):257–269. doi: 10.1083/jcb.91.1.257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. McLean J., Fielding C., Drayna D., Dieplinger H., Baer B., Kohr W., Henzel W., Lawn R. Cloning and expression of human lecithin-cholesterol acyltransferase cDNA. Proc Natl Acad Sci U S A. 1986 Apr;83(8):2335–2339. doi: 10.1073/pnas.83.8.2335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. McMahan U. J., Sanes J. R., Marshall L. M. Cholinesterase is associated with the basal lamina at the neuromuscular junction. Nature. 1978 Jan 12;271(5641):172–174. doi: 10.1038/271172a0. [DOI] [PubMed] [Google Scholar]
  34. Mohan P. S., Spiro R. G. Macromolecular organization of basement membranes. Characterization and comparison of glomerular basement membrane and lens capsule components by immunochemical and lectin affinity procedures. J Biol Chem. 1986 Mar 25;261(9):4328–4336. [PubMed] [Google Scholar]
  35. Neff N. T., Lowrey C., Decker C., Tovar A., Damsky C., Buck C., Horwitz A. F. A monoclonal antibody detaches embryonic skeletal muscle from extracellular matrices. J Cell Biol. 1982 Nov;95(2 Pt 1):654–666. doi: 10.1083/jcb.95.2.654. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Nitkin R. M., Wallace B. G., Spira M. E., Godfrey E. W., McMahan U. J. Molecular components of the synaptic basal lamina that direct differentiation of regenerating neuromuscular junctions. Cold Spring Harb Symp Quant Biol. 1983;48(Pt 2):653–665. doi: 10.1101/sqb.1983.048.01.069. [DOI] [PubMed] [Google Scholar]
  37. Olwin B. B., Hall Z. W. Developmental regulation of laminin accumulation in the extracellular matrix of a mouse muscle cell line. Dev Biol. 1985 Dec;112(2):359–367. doi: 10.1016/0012-1606(85)90407-5. [DOI] [PubMed] [Google Scholar]
  38. Ott U., Odermatt E., Engel J., Furthmayr H., Timpl R. Protease resistance and conformation of laminin. Eur J Biochem. 1982 Mar;123(1):63–72. doi: 10.1111/j.1432-1033.1982.tb06499.x. [DOI] [PubMed] [Google Scholar]
  39. Racker E., Violand B., O'Neal S., Alfonzo M., Telford J. Reconstitution, a way of biochemical research; some new approaches to membrane-bound enzymes. Arch Biochem Biophys. 1979 Dec;198(2):470–477. doi: 10.1016/0003-9861(79)90521-6. [DOI] [PubMed] [Google Scholar]
  40. Rao C. N., Margulies I. M., Tralka T. S., Terranova V. P., Madri J. A., Liotta L. A. Isolation of a subunit of laminin and its role in molecular structure and tumor cell attachment. J Biol Chem. 1982 Aug 25;257(16):9740–9744. [PubMed] [Google Scholar]
  41. Rao N. C., Barsky S. H., Terranova V. P., Liotta L. A. Isolation of a tumor cell laminin receptor. Biochem Biophys Res Commun. 1983 Mar 29;111(3):804–808. doi: 10.1016/0006-291x(83)91370-0. [DOI] [PubMed] [Google Scholar]
  42. Ruoslahti E., Pierschbacher M. D. New perspectives in cell adhesion: RGD and integrins. Science. 1987 Oct 23;238(4826):491–497. doi: 10.1126/science.2821619. [DOI] [PubMed] [Google Scholar]
  43. Sanderson R. D., Fitch J. M., Linsenmayer T. R., Mayne R. Fibroblasts promote the formation of a continuous basal lamina during myogenesis in vitro. J Cell Biol. 1986 Mar;102(3):740–747. doi: 10.1083/jcb.102.3.740. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Sanes J. R., Chiu A. Y. The basal lamina of the neuromuscular junction. Cold Spring Harb Symp Quant Biol. 1983;48(Pt 2):667–678. doi: 10.1101/sqb.1983.048.01.070. [DOI] [PubMed] [Google Scholar]
  45. Sanes J. R., Hall Z. W. Antibodies that bind specifically to synaptic sites on muscle fiber basal lamina. J Cell Biol. 1979 Nov;83(2 Pt 1):357–370. doi: 10.1083/jcb.83.2.357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Sanes J. R. Laminin, fibronectin, and collagen in synaptic and extrasynaptic portions of muscle fiber basement membrane. J Cell Biol. 1982 May;93(2):442–451. doi: 10.1083/jcb.93.2.442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Sanes J. R., Lawrence J. C., Jr Activity-dependent accumulation of basal lamina by cultured rat myotubes. Dev Biol. 1983 May;97(1):123–136. doi: 10.1016/0012-1606(83)90070-2. [DOI] [PubMed] [Google Scholar]
  48. Sanes J. R., 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. doi: 10.1083/jcb.102.2.420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Schaffner W., Weissmann C. A rapid, sensitive, and specific method for the determination of protein in dilute solution. Anal Biochem. 1973 Dec;56(2):502–514. doi: 10.1016/0003-2697(73)90217-0. [DOI] [PubMed] [Google Scholar]
  50. Smalheiser N. R., Schwartz N. B. Cranin: a laminin-binding protein of cell membranes. Proc Natl Acad Sci U S A. 1987 Sep;84(18):6457–6461. doi: 10.1073/pnas.84.18.6457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Steck T. L., Yu J. Selective solubilization of proteins from red blood cell membranes by protein perturbants. J Supramol Struct. 1973;1(3):220–232. doi: 10.1002/jss.400010307. [DOI] [PubMed] [Google Scholar]
  52. Terranova V. P., Rao C. N., Kalebic T., Margulies I. M., Liotta L. A. Laminin receptor on human breast carcinoma cells. Proc Natl Acad Sci U S A. 1983 Jan;80(2):444–448. doi: 10.1073/pnas.80.2.444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Timpl R., Johansson S., van Delden V., Oberbäumer I., Hök M. Characterization of protease-resistant fragments of laminin mediating attachment and spreading of rat hepatocytes. J Biol Chem. 1983 Jul 25;258(14):8922–8927. [PubMed] [Google Scholar]
  54. Timpl R., Rohde H., Robey P. G., Rennard S. I., Foidart J. M., Martin G. R. Laminin--a glycoprotein from basement membranes. J Biol Chem. 1979 Oct 10;254(19):9933–9937. [PubMed] [Google Scholar]
  55. 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. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Valentino K. L., Crumrine D. A., Reichardt L. F. Lowicryl K4M embedding of brain tissue for immunogold electron microscopy. J Histochem Cytochem. 1985 Sep;33(9):969–973. doi: 10.1177/33.9.2991364. [DOI] [PubMed] [Google Scholar]
  57. Wewer U. M., Liotta L. A., Jaye M., Ricca G. A., Drohan W. N., Claysmith A. P., Rao C. N., Wirth P., Coligan J. E., Albrechtsen R. Altered levels of laminin receptor mRNA in various human carcinoma cells that have different abilities to bind laminin. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7137–7141. doi: 10.1073/pnas.83.19.7137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Wewer U. M., Taraboletti G., Sobel M. E., Albrechtsen R., Liotta L. A. Role of laminin receptor in tumor cell migration. Cancer Res. 1987 Nov 1;47(21):5691–5698. [PubMed] [Google Scholar]
  59. von der Mark K., Kühl U. Laminin and its receptor. Biochim Biophys Acta. 1985 Dec 17;823(2):147–160. doi: 10.1016/0304-419x(85)90010-1. [DOI] [PubMed] [Google Scholar]

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

RESOURCES