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. 1987 Sep;6(9):2581–2586. doi: 10.1002/j.1460-2075.1987.tb02548.x

Characterization of the cell adhesion molecules L1, N-CAM and J1 in the mouse intestine.

G Thor 1, R Probstmeier 1, M Schachner 1
PMCID: PMC553678  PMID: 3315649

Abstract

To gain insight into the cellular and molecular mechanisms underlying epithelial cell surface interactions in the adult mouse intestine, we have characterized the cell adhesion molecules L1, N-CAM and J1 by immunocytological, biochemical and cell biological methods. Whereas N-CAM and J1 expression was found to be confined to the mesenchymal and neuroectodermally-derived parts of the intestine, L1 was localized in the proliferating epithelial progenitor cells of crypts, but not in the more differentiated epithelial cells of villi. L1 was detected in crypt cells by Western blot analysis in the molecular forms characteristic of peripheral neural cells, with apparent mol. wts of 230, 180 and 150 kd. Aggregation of single, enriched crypt, but not villus cells, was strongly inhibited in the presence of Fab fragments of polyclonal L1 antibodies. These observations show that L1 is not confined to the nervous system and that it may play a functional role in the histogenesis of the intestine in the adult animal.

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Selected References

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  1. Antonicek H., Persohn E., Schachner M. Biochemical and functional characterization of a novel neuron-glia adhesion molecule that is involved in neuronal migration. J Cell Biol. 1987 Jun;104(6):1587–1595. doi: 10.1083/jcb.104.6.1587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bertolotti R., Rutishauser U., Edelman G. M. A cell surface molecule involved in aggregation of embryonic liver cells. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4831–4835. doi: 10.1073/pnas.77.8.4831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bock E., Richter-Landsberg C., Faissner A., Schachner M. Demonstration of immunochemical identity between the nerve growth factor-inducible large external (NILE) glycoprotein and the cell adhesion molecule L1. EMBO J. 1985 Nov;4(11):2765–2768. doi: 10.1002/j.1460-2075.1985.tb04001.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Boller K., Vestweber D., Kemler R. Cell-adhesion molecule uvomorulin is localized in the intermediate junctions of adult intestinal epithelial cells. J Cell Biol. 1985 Jan;100(1):327–332. doi: 10.1083/jcb.100.1.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cheng H., Leblond C. P. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. III. Entero-endocrine cells. Am J Anat. 1974 Dec;141(4):503–519. doi: 10.1002/aja.1001410405. [DOI] [PubMed] [Google Scholar]
  6. Chiquet-Ehrismann R., Mackie E. J., Pearson C. A., Sakakura T. Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell. 1986 Oct 10;47(1):131–139. doi: 10.1016/0092-8674(86)90374-0. [DOI] [PubMed] [Google Scholar]
  7. Damsky C. H., Richa J., Solter D., Knudsen K., Buck C. A. Identification and purification of a cell surface glycoprotein mediating intercellular adhesion in embryonic and adult tissue. Cell. 1983 Sep;34(2):455–466. doi: 10.1016/0092-8674(83)90379-3. [DOI] [PubMed] [Google Scholar]
  8. Daniloff J. K., Levi G., Grumet M., Rieger F., Edelman G. M. Altered expression of neuronal cell adhesion molecules induced by nerve injury and repair. J Cell Biol. 1986 Sep;103(3):929–945. doi: 10.1083/jcb.103.3.929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Edelman G. M. Cell adhesion molecules. Science. 1983 Feb 4;219(4584):450–457. doi: 10.1126/science.6823544. [DOI] [PubMed] [Google Scholar]
  10. Faissner A., Kruse J., Goridis C., Bock E., Schachner M. The neural cell adhesion molecule L1 is distinct from the N-CAM related group of surface antigens BSP-2 and D2. EMBO J. 1984 Apr;3(4):733–737. doi: 10.1002/j.1460-2075.1984.tb01876.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Faissner A., Teplow D. B., Kübler D., Keilhauer G., Kinzel V., Schachner M. Biosynthesis and membrane topography of the neural cell adhesion molecule L1. EMBO J. 1985 Dec 1;4(12):3105–3113. doi: 10.1002/j.1460-2075.1985.tb04052.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fischer G., Schachner M. In vitro reaggregation of dissociated mouse cerebellar cells. I. Demonstration of different aggregation mechanisms. Exp Cell Res. 1982 Jun;139(2):285–296. doi: 10.1016/0014-4827(82)90253-1. [DOI] [PubMed] [Google Scholar]
  13. Friedlander D. R., Grumet M., Edelman G. M. Nerve growth factor enhances expression of neuron-glia cell adhesion molecule in PC12 cells. J Cell Biol. 1986 Feb;102(2):413–419. doi: 10.1083/jcb.102.2.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gennarini G., Hirn M., Deagostini-Bazin H., Goridis C. Studies on the transmembrane disposition of the neural cell adhesion molecule N-CAM. The use of liposome-inserted radioiodinated N-CAM to study its transbilayer orientation. Eur J Biochem. 1984 Jul 2;142(1):65–73. doi: 10.1111/j.1432-1033.1984.tb08251.x. [DOI] [PubMed] [Google Scholar]
  15. Grumet M., Hoffman S., Crossin K. L., Edelman G. M. Cytotactin, an extracellular matrix protein of neural and non-neural tissues that mediates glia-neuron interaction. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8075–8079. doi: 10.1073/pnas.82.23.8075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Grumet M., Hoffman S., Edelman G. M. Two antigenically related neuronal cell adhesion molecules of different specificities mediate neuron-neuron and neuron-glia adhesion. Proc Natl Acad Sci U S A. 1984 Jan;81(1):267–271. doi: 10.1073/pnas.81.1.267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hirn M., Pierres M., Deagostini-Bazin H., Hirsch M., Goridis C. Monoclonal antibody against cell surface glycoprotein of neurons. Brain Res. 1981 Jun 15;214(2):433–439. doi: 10.1016/0006-8993(81)91208-7. [DOI] [PubMed] [Google Scholar]
  18. Imhof B. A., Vollmers H. P., Goodman S. L., Birchmeier W. Cell-cell interaction and polarity of epithelial cells: specific perturbation using a monoclonal antibody. Cell. 1983 Dec;35(3 Pt 2):667–675. doi: 10.1016/0092-8674(83)90099-5. [DOI] [PubMed] [Google Scholar]
  19. Keilhauer G., Faissner A., Schachner M. Differential inhibition of neurone-neurone, neurone-astrocyte and astrocyte-astrocyte adhesion by L1, L2 and N-CAM antibodies. Nature. 1985 Aug 22;316(6030):728–730. doi: 10.1038/316728a0. [DOI] [PubMed] [Google Scholar]
  20. Kemler R., Babinet C., Eisen H., Jacob F. Surface antigen in early differentiation. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4449–4452. doi: 10.1073/pnas.74.10.4449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kruse J., Keilhauer G., Faissner A., Timpl R., Schachner M. The J1 glycoprotein--a novel nervous system cell adhesion molecule of the L2/HNK-1 family. Nature. 1985 Jul 11;316(6024):146–148. doi: 10.1038/316146a0. [DOI] [PubMed] [Google Scholar]
  22. Kruse J., Mailhammer R., Wernecke H., Faissner A., Sommer I., Goridis C., Schachner M. Neural cell adhesion molecules and myelin-associated glycoprotein share a common carbohydrate moiety recognized by monoclonal antibodies L2 and HNK-1. Nature. 1984 Sep 13;311(5982):153–155. doi: 10.1038/311153a0. [DOI] [PubMed] [Google Scholar]
  23. LEBLOND C. P., MESSIER B. Renewal of chief cells and goblet cells in the small intestine as shown by radioautography after injection of thymidine-H3 into mice. Anat Rec. 1958 Nov;132(3):247–259. doi: 10.1002/ar.1091320303. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Lee V., Shelanski M. L., Greene L. A. Specific neural and adrenal medullary antigens detected by antisera to clonal PC12 pheochromocytoma cells. Proc Natl Acad Sci U S A. 1977 Nov;74(11):5021–5025. doi: 10.1073/pnas.74.11.5021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lindner J., Zinser G., Werz W., Goridis C., Bizzini B., Schachner M. Experimental modification of postnatal cerebellar granule cell migration in vitro. Brain Res. 1986 Jul 9;377(2):298–304. doi: 10.1016/0006-8993(86)90872-3. [DOI] [PubMed] [Google Scholar]
  27. Lyles J. M., Linnemann D., Bock E. Biosynthesis of the D2-cell adhesion molecule: post-translational modifications, intracellular transport, and developmental changes. J Cell Biol. 1984 Dec;99(6):2082–2091. doi: 10.1083/jcb.99.6.2082. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Lyles J. M., Norrild B., Bock E. Biosynthesis of the D2 cell adhesion molecule: pulse-chase studies in cultured fetal rat neuronal cells. J Cell Biol. 1984 Jun;98(6):2077–2081. doi: 10.1083/jcb.98.6.2077. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Martini R., Schachner M. Immunoelectron microscopic localization of neural cell adhesion molecules (L1, N-CAM, and MAG) and their shared carbohydrate epitope and myelin basic protein in developing sciatic nerve. J Cell Biol. 1986 Dec;103(6 Pt 1):2439–2448. doi: 10.1083/jcb.103.6.2439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Mirsky R., Jessen K. R., Schachner M., Goridis C. Distribution of the adhesion molecules N-CAM and L1 on peripheral neurons and glia in adult rats. J Neurocytol. 1986 Dec;15(6):799–815. doi: 10.1007/BF01625196. [DOI] [PubMed] [Google Scholar]
  31. Nieke J., Schachner M. Expression of the neural cell adhesion molecules L1 and N-CAM and their common carbohydrate epitope L2/HNK-1 during development and after transection of the mouse sciatic nerve. Differentiation. 1985;30(2):141–151. doi: 10.1111/j.1432-0436.1985.tb00525.x. [DOI] [PubMed] [Google Scholar]
  32. Obrink B. Epithelial cell adhesion molecules. Exp Cell Res. 1986 Mar;163(1):1–21. doi: 10.1016/0014-4827(86)90554-9. [DOI] [PubMed] [Google Scholar]
  33. PORTER R. R. The hydrolysis of rabbit y-globulin and antibodies with crystalline papain. Biochem J. 1959 Sep;73:119–126. doi: 10.1042/bj0730119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Quaroni A. Crypt cell development in newborn rat small intestine. J Cell Biol. 1985 May;100(5):1601–1610. doi: 10.1083/jcb.100.5.1601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Quaroni A. Fetal characteristics of small intestinal crypt cells. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1723–1727. doi: 10.1073/pnas.83.6.1723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Quaroni A., Isselbacher K. J., Ruoslahti E. Fibronectin synthesis by epithelial crypt cells of rat small intestine. Proc Natl Acad Sci U S A. 1978 Nov;75(11):5548–5552. doi: 10.1073/pnas.75.11.5548. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Rathjen F. G., Rutishauser U. Comparison of two cell surface molecules involved in neural cell adhesion. EMBO J. 1984 Feb;3(2):461–465. doi: 10.1002/j.1460-2075.1984.tb01828.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Rathjen F. G., Schachner M. Immunocytological and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion. EMBO J. 1984 Jan;3(1):1–10. doi: 10.1002/j.1460-2075.1984.tb01753.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. 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]
  40. Schachner M., Wortham K. A., Carter L. D., Chaffee J. K. NS-4 (nervous system antigen-4), a cell surface antigen of developing and adult mouse brain and sperm. Dev Biol. 1975 Jun;44(2):313–325. doi: 10.1016/0012-1606(75)90402-9. [DOI] [PubMed] [Google Scholar]
  41. Simon-Assmann P., Kedinger M., Haffen K. Immunocytochemical localization of extracellular-matrix proteins in relation to rat intestinal morphogenesis. Differentiation. 1986;32(1):59–66. doi: 10.1111/j.1432-0436.1986.tb00556.x. [DOI] [PubMed] [Google Scholar]
  42. Simon P. M., Kedinger M., Raul F., Grenier J. F., Haffen K. Developmental pattern of rat intestinal brush-border enzymic proteins along the villus--crypt axis. Biochem J. 1979 Feb 15;178(2):407–413. doi: 10.1042/bj1780407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Sweadner K. J. Post-translational modification and evoked release of two large surface proteins of sympathetic neurons. J Neurosci. 1983 Dec;3(12):2504–2517. doi: 10.1523/JNEUROSCI.03-12-02504.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Sweadner K. J. Size, shape, and solubility of a class of releasable cell surface proteins of sympathetic neurons. J Neurosci. 1983 Dec;3(12):2518–2524. doi: 10.1523/JNEUROSCI.03-12-02518.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Takeichi M. Functional correlation between cell adhesive properties and some cell surface proteins. J Cell Biol. 1977 Nov;75(2 Pt 1):464–474. doi: 10.1083/jcb.75.2.464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Thiery J. P., Delouvée A., Gallin W. J., Cunningham B. A., Edelman G. M. Ontogenetic expression of cell adhesion molecules: L-CAM is found in epithelia derived from the three primary germ layers. Dev Biol. 1984 Mar;102(1):61–78. doi: 10.1016/0012-1606(84)90175-1. [DOI] [PubMed] [Google Scholar]
  47. Thor G., Pollerberg E. G., Schachner M. Molecular association of two neural cell adhesion molecules within the surface membrane of cultured mouse neuroblastoma cells. Neurosci Lett. 1986 May 15;66(2):121–126. doi: 10.1016/0304-3940(86)90176-x. [DOI] [PubMed] [Google Scholar]
  48. Weiser M. M. Intestinal epithelial cell surface membrane glycoprotein synthesis. I. An indicator of cellular differentiation. J Biol Chem. 1973 Apr 10;248(7):2536–2541. [PubMed] [Google Scholar]

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