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. 1991 Nov 1;115(3):779–794. doi: 10.1083/jcb.115.3.779

Relationship between neuronal migration and cell-substratum adhesion: laminin and merosin promote olfactory neuronal migration but are anti- adhesive

PMCID: PMC2289183  PMID: 1918163

Abstract

Regulation by the extracellular matrix (ECM) of migration, motility, and adhesion of olfactory neurons and their precursors was studied in vitro. Neuronal cells of the embryonic olfactory epithelium (OE), which undergo extensive migration in the central nervous system during normal development, were shown to be highly migratory in culture as well. Migration of OE neuronal cells was strongly dependent on substratum- bound ECM molecules, being specifically stimulated and guided by laminin (or the laminin-related molecule merosin) in preference to fibronectin, type I collagen, or type IV collagen. Motility of OE neuronal cells, examined by time-lapse video microscopy, was high on laminin-containing substrata, but negligible on fibronectin substrata. Quantitative assays of adhesion of OE neuronal cells to substrata treated with different ECM molecules demonstrated no correlation, either positive or negative, between the migratory preferences of cells and the strength of cell-substratum adhesion. Moreover, measurements of cell adhesion to substrata containing combinations of ECM proteins revealed that laminin and merosin are anti-adhesive for OE neuronal cells, i.e., cause these cells to adhere poorly to substrata that would otherwise be strongly adhesive. The evidence suggests that the anti- adhesive effect of laminin is not the result of interactions between laminin and other ECM molecules, but rather an effect of laminin on cells, which alters the way in which cells adhere. Consistent with this view, laminin was found to interfere strongly with the formation of focal contacts by OE neuronal cells.

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Selected References

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  1. Akama T., Yamada K. M., Seno N., Matsumoto I., Kono I., Kashiwagi H., Funaki T., Hayashi M. Immunological characterization of human vitronectin and its binding to glycosaminoglycans. J Biochem. 1986 Nov;100(5):1343–1351. doi: 10.1093/oxfordjournals.jbchem.a121840. [DOI] [PubMed] [Google Scholar]
  2. Beck K., Hunter I., Engel J. Structure and function of laminin: anatomy of a multidomain glycoprotein. FASEB J. 1990 Feb 1;4(2):148–160. doi: 10.1096/fasebj.4.2.2404817. [DOI] [PubMed] [Google Scholar]
  3. Calof A. L., Chikaraishi D. M. Analysis of neurogenesis in a mammalian neuroepithelium: proliferation and differentiation of an olfactory neuron precursor in vitro. Neuron. 1989 Jul;3(1):115–127. doi: 10.1016/0896-6273(89)90120-7. [DOI] [PubMed] [Google Scholar]
  4. Calof A. L., Lander A. D., Chikaraishi D. M. Regulation of neurogenesis and neuronal differentiation in primary and immortalized cells from mouse olfactory epithelium. Ciba Found Symp. 1991;160:249–276. doi: 10.1002/9780470514122.ch13. [DOI] [PubMed] [Google Scholar]
  5. Chiquet-Ehrismann R., Kalla P., Pearson C. A., Beck K., Chiquet M. Tenascin interferes with fibronectin action. Cell. 1988 May 6;53(3):383–390. doi: 10.1016/0092-8674(88)90158-4. [DOI] [PubMed] [Google Scholar]
  6. Chuong C. M., Crossin K. L., Edelman G. M. Sequential expression and differential function of multiple adhesion molecules during the formation of cerebellar cortical layers. J Cell Biol. 1987 Feb;104(2):331–342. doi: 10.1083/jcb.104.2.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cohen J., Burne J. F., McKinlay C., Winter J. The role of laminin and the laminin/fibronectin receptor complex in the outgrowth of retinal ganglion cell axons. Dev Biol. 1987 Aug;122(2):407–418. doi: 10.1016/0012-1606(87)90305-8. [DOI] [PubMed] [Google Scholar]
  8. Daikoku-Ishido H., Okamura Y., Yanaihara N., Daikoku S. Development of the hypothalamic luteinizing hormone-releasing hormone-containing neuron system in the rat: in vivo and in transplantation studies. Dev Biol. 1990 Aug;140(2):374–387. doi: 10.1016/0012-1606(90)90087-y. [DOI] [PubMed] [Google Scholar]
  9. Devreotes P. N., Zigmond S. H. Chemotaxis in eukaryotic cells: a focus on leukocytes and Dictyostelium. Annu Rev Cell Biol. 1988;4:649–686. doi: 10.1146/annurev.cb.04.110188.003245. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Edmondson J. C., Hatten M. E. Glial-guided granule neuron migration in vitro: a high-resolution time-lapse video microscopic study. J Neurosci. 1987 Jun;7(6):1928–1934. doi: 10.1523/JNEUROSCI.07-06-01928.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ehrig K., Leivo I., Argraves W. S., Ruoslahti E., Engvall E. Merosin, a tissue-specific basement membrane protein, is a laminin-like protein. Proc Natl Acad Sci U S A. 1990 May;87(9):3264–3268. doi: 10.1073/pnas.87.9.3264. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Erickson C. A., Turley E. A. Substrata formed by combinations of extracellular matrix components alter neural crest cell motility in vitro. J Cell Sci. 1983 May;61:299–323. doi: 10.1242/jcs.61.1.299. [DOI] [PubMed] [Google Scholar]
  14. Faissner A., Kruse J. J1/tenascin is a repulsive substrate for central nervous system neurons. Neuron. 1990 Nov;5(5):627–637. doi: 10.1016/0896-6273(90)90217-4. [DOI] [PubMed] [Google Scholar]
  15. Goodman S. L., 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. doi: 10.1083/jcb.109.2.799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gundersen R. W. Interference reflection microscopic study of dorsal root growth cones on different substrates: assessment of growth cone-substrate contacts. J Neurosci Res. 1988 Oct-Dec;21(2-4):298–306. doi: 10.1002/jnr.490210222. [DOI] [PubMed] [Google Scholar]
  17. Gundersen R. W. Response of sensory neurites and growth cones to patterned substrata of laminin and fibronectin in vitro. Dev Biol. 1987 Jun;121(2):423–431. doi: 10.1016/0012-1606(87)90179-5. [DOI] [PubMed] [Google Scholar]
  18. Halfter W., Chiquet-Ehrismann R., Tucker R. P. The effect of tenascin and embryonic basal lamina on the behavior and morphology of neural crest cells in vitro. Dev Biol. 1989 Mar;132(1):14–25. doi: 10.1016/0012-1606(89)90200-5. [DOI] [PubMed] [Google Scholar]
  19. Johansson S., Hök M. Substrate adhesion of rat hepatocytes: on the mechanism of attachment to fibronectin. J Cell Biol. 1984 Mar;98(3):810–817. doi: 10.1083/jcb.98.3.810. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kleinman H. K., McGarvey M. L., Liotta L. A., Robey P. G., Tryggvason K., Martin G. R. Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry. 1982 Nov 23;21(24):6188–6193. doi: 10.1021/bi00267a025. [DOI] [PubMed] [Google Scholar]
  21. Lander A. D. Mechanisms by which molecules guide axons. Curr Opin Cell Biol. 1990 Oct;2(5):907–913. doi: 10.1016/0955-0674(90)90091-r. [DOI] [PubMed] [Google Scholar]
  22. Lander A. D. Understanding the molecules of neural cell contacts: emerging patterns of structure and function. Trends Neurosci. 1989 May;12(5):189–195. doi: 10.1016/0166-2236(89)90070-2. [DOI] [PubMed] [Google Scholar]
  23. Letourneau P. C. Cell-to-substratum adhesion and guidance of axonal elongation. Dev Biol. 1975 May;44(1):92–101. doi: 10.1016/0012-1606(75)90379-6. [DOI] [PubMed] [Google Scholar]
  24. Letourneau P. C., Madsen A. M., Palm S. L., Furcht L. T. Immunoreactivity for laminin in the developing ventral longitudinal pathway of the brain. Dev Biol. 1988 Jan;125(1):135–144. doi: 10.1016/0012-1606(88)90066-8. [DOI] [PubMed] [Google Scholar]
  25. Lotz M. M., Burdsal C. A., Erickson H. P., McClay D. R. Cell adhesion to fibronectin and tenascin: quantitative measurements of initial binding and subsequent strengthening response. J Cell Biol. 1989 Oct;109(4 Pt 1):1795–1805. doi: 10.1083/jcb.109.4.1795. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Martin G. R., Timpl R. Laminin and other basement membrane components. Annu Rev Cell Biol. 1987;3:57–85. doi: 10.1146/annurev.cb.03.110187.000421. [DOI] [PubMed] [Google Scholar]
  27. McClay D. R., Ettensohn C. A. Cell adhesion in morphogenesis. Annu Rev Cell Biol. 1987;3:319–345. doi: 10.1146/annurev.cb.03.110187.001535. [DOI] [PubMed] [Google Scholar]
  28. McClay D. R., Wessel G. M., Marchase R. B. Intercellular recognition: quantitation of initial binding events. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4975–4979. doi: 10.1073/pnas.78.8.4975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Morganti M. C., Taylor J., Pesheva P., Schachner M. Oligodendrocyte-derived J1-160/180 extracellular matrix glycoproteins are adhesive or repulsive depending on the partner cell type and time of interaction. Exp Neurol. 1990 Jul;109(1):98–110. doi: 10.1016/s0014-4886(05)80012-3. [DOI] [PubMed] [Google Scholar]
  30. Murphy-Ullrich J. E., Hök M. Thrombospondin modulates focal adhesions in endothelial cells. J Cell Biol. 1989 Sep;109(3):1309–1319. doi: 10.1083/jcb.109.3.1309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Neugebauer K. M., Reichardt L. F. Cell-surface regulation of beta 1-integrin activity on developing retinal neurons. Nature. 1991 Mar 7;350(6313):68–71. doi: 10.1038/350068a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. O'Shea K. S., Rheinheimer J. S., Dixit V. M. Deposition and role of thrombospondin in the histogenesis of the cerebellar cortex. J Cell Biol. 1990 Apr;110(4):1275–1283. doi: 10.1083/jcb.110.4.1275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Perris R., Paulsson M., Bronner-Fraser M. Molecular mechanisms of avian neural crest cell migration on fibronectin and laminin. Dev Biol. 1989 Nov;136(1):222–238. doi: 10.1016/0012-1606(89)90144-9. [DOI] [PubMed] [Google Scholar]
  34. Riggott M. J., Moody S. A. Distribution of laminin and fibronectin along peripheral trigeminal axon pathways in the developing chick. J Comp Neurol. 1987 Apr 22;258(4):580–596. doi: 10.1002/cne.902580408. [DOI] [PubMed] [Google Scholar]
  35. Rogers S. L., Letourneau P. C., Peterson B. A., Furcht L. T., McCarthy J. B. Selective interaction of peripheral and central nervous system cells with two distinct cell-binding domains of fibronectin. J Cell Biol. 1987 Sep;105(3):1435–1442. doi: 10.1083/jcb.105.3.1435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Schwanzel-Fukuda M., Pfaff D. W. Origin of luteinizing hormone-releasing hormone neurons. Nature. 1989 Mar 9;338(6211):161–164. doi: 10.1038/338161a0. [DOI] [PubMed] [Google Scholar]
  37. Sidman R. L., Rakic P. Neuronal migration, with special reference to developing human brain: a review. Brain Res. 1973 Nov 9;62(1):1–35. doi: 10.1016/0006-8993(73)90617-3. [DOI] [PubMed] [Google Scholar]
  38. Spring J., Beck K., Chiquet-Ehrismann R. Two contrary functions of tenascin: dissection of the active sites by recombinant tenascin fragments. Cell. 1989 Oct 20;59(2):325–334. doi: 10.1016/0092-8674(89)90294-8. [DOI] [PubMed] [Google Scholar]
  39. Timpl R., Rohde H., Risteli L., Ott U., Robey P. G., Martin G. R. Laminin. Methods Enzymol. 1982;82(Pt A):831–838. doi: 10.1016/0076-6879(82)82104-6. [DOI] [PubMed] [Google Scholar]
  40. Trinkaus J. P. Further thoughts on directional cell movement during morphogenesis. J Neurosci Res. 1985;13(1-2):1–19. doi: 10.1002/jnr.490130102. [DOI] [PubMed] [Google Scholar]

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