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. 1986 Jun 1;102(6):2273–2280. doi: 10.1083/jcb.102.6.2273

Rapid adhesion of nerve cells to muscle fibers from adult rats is mediated by a sialic acid-binding receptor

PMCID: PMC2114257  PMID: 3711146

Abstract

Single viable muscle fibers isolated from adult rats by collagenase digestion rapidly bind dissociated spinal neurons or PC-12 cells but not a variety of other cells tested. The adhesion process is calcium- independent, temperature-sensitive, and is not blocked by pretreating cells with inhibitors of energy metabolism or actin polymerization. Adhesion is mediated by a carbohydrate-binding protein and can be inhibited by N-acetylneuraminic acid or mucin, a glycoprotein with high sialic acids content. The hapten inhibitors do not dissociate cells if added after aggregation has occurred. Experiments to block adhesion by pretreatment of cells with either neuraminidase or mucin show that the sialic acids-rich moiety is on the nerve cells, while its receptor is on the muscle fibers.

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Selected References

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  1. Ahrens P. B., Solursh M., Meier S. The synthesis and localization of glycosaminoglycans in striated muscle differentiating in cell culture. J Exp Zool. 1977 Dec;202(3):375–388. doi: 10.1002/jez.1402020308. [DOI] [PubMed] [Google Scholar]
  2. Anderson M. J., Klier F. G., Tanguay K. E. Acetylcholine receptor aggregation parallels the deposition of a basal lamina proteoglycan during development of the neuromuscular junction. J Cell Biol. 1984 Nov;99(5):1769–1784. doi: 10.1083/jcb.99.5.1769. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BORNSTEIN M. B. Reconstituted rattail collagen used as substrate for tissue cultures on coverslips in Maximow slides and roller tubes. Lab Invest. 1958 Mar-Apr;7(2):134–137. [PubMed] [Google Scholar]
  4. Bekoff A., Betz W. Properties of isolated adult rat muscle fibres maintained in tissue culture. J Physiol. 1977 Oct;271(2):537–547. doi: 10.1113/jphysiol.1977.sp012013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Berg D. K., Kelly R. B., Sargent P. B., Williamson P., Hall Z. W. Binding of -bungarotoxin to acetylcholine receptors in mammalian muscle (snake venom-denervated muscle-neonatal muscle-rat diaphragm-SDS-polyacrylamide gel electrophoresis). Proc Natl Acad Sci U S A. 1972 Jan;69(1):147–151. doi: 10.1073/pnas.69.1.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bird M. M. Ultrastructural observations on rapid formation of neuro-muscular junctions in vitro. Cell Tissue Res. 1981;217(3):647–659. doi: 10.1007/BF00219371. [DOI] [PubMed] [Google Scholar]
  7. Bischoff R. Enzymatic liberation of myogenic cells from adult rat muscle. Anat Rec. 1974 Dec;180(4):645–661. doi: 10.1002/ar.1091800410. [DOI] [PubMed] [Google Scholar]
  8. Bischoff R. Regeneration of single skeletal muscle fibers in vitro. Anat Rec. 1975 Jun;182(2):215–235. doi: 10.1002/ar.1091820207. [DOI] [PubMed] [Google Scholar]
  9. Brodeur G. M., Sekhon G., Goldstein M. N. Chromosomal aberrations in human neuroblastomas. Cancer. 1977 Nov;40(5):2256–2263. doi: 10.1002/1097-0142(197711)40:5<2256::aid-cncr2820400536>3.0.co;2-1. [DOI] [PubMed] [Google Scholar]
  10. Burrage T. G., Lentz T. L. Ultrastructural characterization of surface specializations containing high-density acetylcholine receptors on embryonic chick myotubes in vivo and in vitro. Dev Biol. 1981 Jul 30;85(2):267–286. doi: 10.1016/0012-1606(81)90259-1. [DOI] [PubMed] [Google Scholar]
  11. Carter W. G., Rauvala H., Hakomori S. I. Studies on cell adhesion and recognition. II. The kinetics of cell adhesion and cell spreading on surfaces coated with carbohydrate-reactive proteins (glycosidases and lectins) and fibronectin. J Cell Biol. 1981 Jan;88(1):138–148. doi: 10.1083/jcb.88.1.138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Covault J., Sanes J. R. Neural cell adhesion molecule (N-CAM) accumulates in denervated and paralyzed skeletal muscles. Proc Natl Acad Sci U S A. 1985 Jul;82(13):4544–4548. doi: 10.1073/pnas.82.13.4544. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cunningham B. A., Hoffman S., Rutishauser U., Hemperly J. J., Edelman G. M. Molecular topography of the neural cell adhesion molecule N-CAM: surface orientation and location of sialic acid-rich and binding regions. Proc Natl Acad Sci U S A. 1983 May;80(10):3116–3120. doi: 10.1073/pnas.80.10.3116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Edelman G. M. Modulation of cell adhesion during induction, histogenesis, and perinatal development of the nervous system. Annu Rev Neurosci. 1984;7:339–377. doi: 10.1146/annurev.ne.07.030184.002011. [DOI] [PubMed] [Google Scholar]
  15. Elsdale T., Bard J. Collagen substrata for studies on cell behavior. J Cell Biol. 1972 Sep;54(3):626–637. doi: 10.1083/jcb.54.3.626. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Greene L. A., Tischler A. S. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2424–2428. doi: 10.1073/pnas.73.7.2424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Grumet M., Rutishauser U., Edelman G. M. 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. doi: 10.1038/295693a0. [DOI] [PubMed] [Google Scholar]
  18. Grunwald G. B., Fredman P., Magnani J. L., Trisler D., Ginsburg V., Nirenberg M. Monoclonal antibody 18B8 detects gangliosides associated with neuronal differentiation and synapse formation. Proc Natl Acad Sci U S A. 1985 Jun;82(12):4008–4012. doi: 10.1073/pnas.82.12.4008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hausman R. E., Knapp L. W., Moscona A. A. Preparation of tissue-specific cell-aggregating factors from embryonic neural tissues. J Exp Zool. 1976 Dec;198(3):417–422. doi: 10.1002/jez.1401980316. [DOI] [PubMed] [Google Scholar]
  20. Hausman R. E., Moscona A. A. Immunologic detection of retina cognin on the surface of embryonic cells. Exp Cell Res. 1979 Mar 15;119(2):191–204. doi: 10.1016/0014-4827(79)90348-3. [DOI] [PubMed] [Google Scholar]
  21. Hausman R. E., Moscona A. A. Purification and characterization of the retina-specific cell-aggregating factor. Proc Natl Acad Sci U S A. 1975 Mar;72(3):916–920. doi: 10.1073/pnas.72.3.916. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hefley T. J., Stern P. H., Brand J. S. Enzymatic isolation of cells from neonatal calvaria using two purified enzymes from Clostridium histolyticum. Exp Cell Res. 1983 Nov;149(1):227–236. doi: 10.1016/0014-4827(83)90394-4. [DOI] [PubMed] [Google Scholar]
  23. Jourdian G. W., Dean L., Roseman S. The sialic acids. XI. A periodate-resorcinol method for the quantitative estimation of free sialic acids and their glycosides. J Biol Chem. 1971 Jan 25;246(2):430–435. [PubMed] [Google Scholar]
  24. Kanwar Y. S., Farquhar M. G. Detachment of endothelium and epithelium from the glomerular basement membrane produced by kidney perfusion with neuraminidase. Lab Invest. 1980 Mar;42(3):375–384. [PubMed] [Google Scholar]
  25. Kennedy D. W., Rohrbach D. H., Martin G. R., Momoi T., Yamada K. M. The adhesive glycoprotein laminin is an agglutinin. J Cell Physiol. 1983 Mar;114(3):257–262. doi: 10.1002/jcp.1041140302. [DOI] [PubMed] [Google Scholar]
  26. Kleinman H. K., Martin G. R., Fishman P. H. Ganglioside inhibition of fibronectin-mediated cell adhesion to collagen. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3367–3371. doi: 10.1073/pnas.76.7.3367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  28. Ledeen R. W. Ganglioside structures and distribution: are they localized at the nerve ending? J Supramol Struct. 1978;8(1):1–17. doi: 10.1002/jss.400080102. [DOI] [PubMed] [Google Scholar]
  29. Marshall L. M., Sanes J. R., McMahan U. J. Reinnervation of original synaptic sites on muscle fiber basement membrane after disruption of the muscle cells. Proc Natl Acad Sci U S A. 1977 Jul;74(7):3073–3077. doi: 10.1073/pnas.74.7.3073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. McCarthy J. B., Palm S. L., Furcht L. T. Migration by haptotaxis of a Schwann cell tumor line to the basement membrane glycoprotein laminin. J Cell Biol. 1983 Sep;97(3):772–777. doi: 10.1083/jcb.97.3.772. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nowak T. P., Kobiler D., Roel L. E., Barondes S. H. Developmentally regulated lectin from embryonic chick pectoral muscle. Purification by affinity chromatography. J Biol Chem. 1977 Sep 10;252(17):6026–6030. [PubMed] [Google Scholar]
  32. Obata K., Oide M., Handa S. Effects of glycolipids on in vitro development of neuromuscular junction. Nature. 1977 Mar 24;266(5600):369–371. doi: 10.1038/266369a0. [DOI] [PubMed] [Google Scholar]
  33. Ozawa M., Sato M., Muramatsu T. Basement membrane glycoprotein laminin is an agglutinin. J Biochem. 1983 Aug;94(2):479–485. doi: 10.1093/oxfordjournals.jbchem.a134378. [DOI] [PubMed] [Google Scholar]
  34. Ratner N., Glaser L., Bunge R. P. PC12 cells as a source of neurite-derived cell surface mitogen, which stimulates Schwann cell division. J Cell Biol. 1984 Mar;98(3):1150–1155. doi: 10.1083/jcb.98.3.1150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rutishauser U., Grumet M., Edelman G. M. 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. doi: 10.1083/jcb.97.1.145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Rutishauser U., Hoffman S., Edelman G. M. Binding properties of a cell adhesion molecule from neural tissue. Proc Natl Acad Sci U S A. 1982 Jan;79(2):685–689. doi: 10.1073/pnas.79.2.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. Sanes J. R., Marshall L. M., McMahan U. J. Reinnervation of muscle fiber basal lamina after removal of myofibers. Differentiation of regenerating axons at original synaptic sites. J Cell Biol. 1978 Jul;78(1):176–198. doi: 10.1083/jcb.78.1.176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sasse J., von der Mark H., Kühl U., Dessau W., von der Mark K. Origin of collagen types I, III, and V in cultures of avian skeletal muscle. Dev Biol. 1981 Apr 15;83(1):79–89. doi: 10.1016/s0012-1606(81)80010-3. [DOI] [PubMed] [Google Scholar]
  40. Thiery J. P., Duband J. L., Rutishauser U., Edelman G. M. Cell adhesion molecules in early chicken embryogenesis. Proc Natl Acad Sci U S A. 1982 Nov;79(21):6737–6741. doi: 10.1073/pnas.79.21.6737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wood P. M., Bunge R. P. Evidence that sensory axons are mitogenic for Schwann cells. Nature. 1975 Aug 21;256(5519):662–664. doi: 10.1038/256662a0. [DOI] [PubMed] [Google Scholar]

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