Abstract
Axons of dorsal root ganglion neurons express on their surfaces one or more proteins which are mitogenic for Schwann cells (Salzer, J., R. P. Bunge, and L. Glaser, 1980, J. Cell Biol., 84:767-778). Incubation of co-cultures of dorsal root ganglion neurons and Schwann cells with 4- methylumbelliferyl-beta-D-xyloside, an inhibitor of proteoglycan biosynthesis, decreases the mitogenic response of the Schwann cell by over 95%. The effect of the beta-D-xyloside has been localized to the neurons; pretreatment of neurons but not of Schwann cells with the inhibitor causes a marked reduction of the mitogenic response. In addition, Schwann cells treated with beta-D-xyloside are still mitogenically responsive to soluble Schwann cell mitogens (cholera toxin and glial growth factor). Neurons treated with heparitinase and membrane vesicles prepared from heparitinase-treated neurons show diminished mitogenicity for Schwann cells, while other proteoglycan lyases have no effect. We conclude that a cell surface heparan sulfate proteoglycan is a component of the Schwann cell mitogen present on the surface of dorsal root ganglion neurons.
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- Aquino D. A., Margolis R. U., Margolis R. K. Immunocytochemical localization of a chondroitin sulfate proteoglycan in nervous tissue. II. Studies in developing brain. J Cell Biol. 1984 Sep;99(3):1130–1139. doi: 10.1083/jcb.99.3.1130. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Banerjee S. D., Cohn R. H., Bernfield M. R. Basal lamina of embryonic salivary epithelia. Production by the epithelium and role in maintaining lobular morphology. J Cell Biol. 1977 May;73(2):445–463. doi: 10.1083/jcb.73.2.445. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bottenstein J. E., Sato G. H. Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc Natl Acad Sci U S A. 1979 Jan;76(1):514–517. doi: 10.1073/pnas.76.1.514. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brockes J. P., Fields K. L., Raff M. C. Studies on cultured rat Schwann cells. I. Establishment of purified populations from cultures of peripheral nerve. Brain Res. 1979 Apr 6;165(1):105–118. doi: 10.1016/0006-8993(79)90048-9. [DOI] [PubMed] [Google Scholar]
- Brockes J. P., Lemke G. E., Balzer D. R., Jr Purification and preliminary characterization of a glial growth factor from the bovine pituitary. J Biol Chem. 1980 Sep 25;255(18):8374–8377. [PubMed] [Google Scholar]
- Bunge M. B., Williams A. K., Wood P. M. Neuron-Schwann cell interaction in basal lamina formation. Dev Biol. 1982 Aug;92(2):449–460. doi: 10.1016/0012-1606(82)90190-7. [DOI] [PubMed] [Google Scholar]
- Carlstedt I., Cöster L., Malmström A., Fransson L. A. Proteoheparan sulfate from human skin fibroblasts. Isolation and structural characterization. J Biol Chem. 1983 Oct 10;258(19):11629–11635. [PubMed] [Google Scholar]
- Cassel D., Wood P. M., Bunge R. P., Glaser L. Mitogenicity of brain axolemma membranes and soluble factors for dorsal root ganglion Schwann cells. J Cell Biochem. 1982;18(4):433–445. doi: 10.1002/jcb.1982.240180405. [DOI] [PubMed] [Google Scholar]
- Cole G. J., Schubert D., Glaser L. Cell-substratum adhesion in chick neural retina depends upon protein-heparan sulfate interactions. J Cell Biol. 1985 Apr;100(4):1192–1199. doi: 10.1083/jcb.100.4.1192. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cornbrooks C. J., Carey D. J., McDonald J. A., Timpl R., Bunge R. P. In vivo and in vitro observations on laminin production by Schwann cells. Proc Natl Acad Sci U S A. 1983 Jun;80(12):3850–3854. doi: 10.1073/pnas.80.12.3850. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DeVries G. H., Minier L. N., Lewis B. L. Further studies on the mitogenic response of cultured Schwann cells to rat CNS axolemma-enriched fractions. Brain Res. 1983 Jul;285(1):87–93. doi: 10.1016/0165-3806(83)90112-8. [DOI] [PubMed] [Google Scholar]
- Faissner A., Kruse J., Nieke J., Schachner M. Expression of neural cell adhesion molecule L1 during development, in neurological mutants and in the peripheral nervous system. Brain Res. 1984 Jul;317(1):69–82. doi: 10.1016/0165-3806(84)90141-x. [DOI] [PubMed] [Google Scholar]
- Galligani L., Hopwood J., Schwartz N. B., Dorfman A. Stimulation of synthesis of free chondroitin sulfate chains by beta-D-xylosides in cultured cells. J Biol Chem. 1975 Jul 25;250(14):5400–5406. [PubMed] [Google Scholar]
- Gospodarowicz D., Greenburg G., Birdwell C. R. Determination of cellular shape by the extracellular matrix and its correlation with the control of cellular growth. Cancer Res. 1978 Nov;38(11 Pt 2):4155–4171. [PubMed] [Google Scholar]
- Grumet M., Edelman G. M. Heterotypic binding between neuronal membrane vesicles and glial cells is mediated by a specific cell adhesion molecule. J Cell Biol. 1984 May;98(5):1746–1756. doi: 10.1083/jcb.98.5.1746. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grumet M., Hoffman S., Chuong C. M., Edelman G. M. Polypeptide components and binding functions of neuron-glia cell adhesion molecules. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7989–7993. doi: 10.1073/pnas.81.24.7989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hampson I. N., Kumar S., Gallagher J. T. Heterogeneity of cell-associated and secretory heparan sulphate proteoglycans produced by cultured human neuroblastoma cells. Biochim Biophys Acta. 1984 Sep 28;801(2):306–313. doi: 10.1016/0304-4165(84)90081-3. [DOI] [PubMed] [Google Scholar]
- Hanson G. R., Partlow L. M. A comparison of two factors affecting the proliferation of non-neuronal (glial) cells in vitro. Brain Res. 1980 Jun 23;192(2):371–381. doi: 10.1016/0006-8993(80)90890-2. [DOI] [PubMed] [Google Scholar]
- Hedman K., Christner J., Julkunen I., Vaheri A. Chondroitin sulfate at the plasma membranes of cultured fibroblasts. J Cell Biol. 1983 Oct;97(4):1288–1293. doi: 10.1083/jcb.97.4.1288. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kalderon N. Schwann cell proliferation and localized proteolysis: expression of plasminogen-activator activity predominates in the proliferating cell populations. Proc Natl Acad Sci U S A. 1984 Nov;81(22):7216–7220. doi: 10.1073/pnas.81.22.7216. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kanwar Y. S., Hascall V. C., Jakubowski M. L., Gibbons J. T. Effect of beta-D-xyloside on the glomerular proteoglycans. I. Biochemical studies. J Cell Biol. 1984 Aug;99(2):715–722. doi: 10.1083/jcb.99.2.715. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kawakami H., Terayama H. Liver plasma membranes and proteoglycan prepared therefrom inhibit the growth of hepatoma cells in vitro. Biochim Biophys Acta. 1981 Aug 6;646(1):161–168. doi: 10.1016/0005-2736(81)90283-2. [DOI] [PubMed] [Google Scholar]
- 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]
- Lake P., Clark E. A., Khorshidi M., Sunshine G. H. Production and characterization of cytotoxic Thy-1 antibody-secreting hybrid cell lines. Detection of T cell subsets. Eur J Immunol. 1979 Nov;9(11):875–886. doi: 10.1002/eji.1830091109. [DOI] [PubMed] [Google Scholar]
- Lander A. D., Fujii D. K., Gospodarowicz D., Reichardt L. F. Characterization of a factor that promotes neurite outgrowth: evidence linking activity to a heparan sulfate proteoglycan. J Cell Biol. 1982 Sep;94(3):574–585. doi: 10.1083/jcb.94.3.574. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lark M. W., Culp L. A. Modification of proteoglycans during maturation of fibroblast substratum adhesion sites. Biochemistry. 1983 Apr 26;22(9):2289–2296. doi: 10.1021/bi00278a036. [DOI] [PubMed] [Google Scholar]
- Linker A., Hovingh P. The heparitin sulfates (heparan sulfates). Carbohydr Res. 1973 Jul;29(1):41–62. doi: 10.1016/s0008-6215(00)82069-8. [DOI] [PubMed] [Google Scholar]
- Lohmander L. S., Hascall V. C., Caplan A. I. Effects of 4-methyl umbelliferyl-beta-D-xylopyranoside on chondrogenesis and proteoglycan synthesis in chick limb bud mesenchymal cell cultures. J Biol Chem. 1979 Oct 25;254(20):10551–10561. [PubMed] [Google Scholar]
- Maciag T., Mehlman T., Friesel R., Schreiber A. B. Heparin binds endothelial cell growth factor, the principal endothelial cell mitogen in bovine brain. Science. 1984 Aug 31;225(4665):932–935. doi: 10.1126/science.6382607. [DOI] [PubMed] [Google Scholar]
- Maresh G. A., Chernoff E. A., Culp L. A. Heparan sulfate proteoglycans of human neuroblastoma cells: affinity fractionation on columns of platelet factor-4+. Arch Biochem Biophys. 1984 Sep;233(2):428–437. doi: 10.1016/0003-9861(84)90464-8. [DOI] [PubMed] [Google Scholar]
- Markwell M. A., Haas S. M., Bieber L. L., Tolbert N. E. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem. 1978 Jun 15;87(1):206–210. doi: 10.1016/0003-2697(78)90586-9. [DOI] [PubMed] [Google Scholar]
- McGarvey M. L., Baron-Van Evercooren A., Kleinman H. K., Dubois-Dalcq M. Synthesis and effects of basement membrane components in cultured rat Schwann cells. Dev Biol. 1984 Sep;105(1):18–28. doi: 10.1016/0012-1606(84)90257-4. [DOI] [PubMed] [Google Scholar]
- Morris J. E. Isolation of the major chondroitin sulfate/dermatan sulfate and heparan sulfate proteoglycans from embryonic chicken retina. Arch Biochem Biophys. 1984 Nov 15;235(1):127–140. doi: 10.1016/0003-9861(84)90261-3. [DOI] [PubMed] [Google Scholar]
- Moya F., Bunge M. B., Bunge R. P. Schwann cells proliferate but fail to differentiate in defined medium. Proc Natl Acad Sci U S A. 1980 Nov;77(11):6902–6906. doi: 10.1073/pnas.77.11.6902. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pfenninger K. H., Johnson M. P. Membrane biogenesis in the sprouting neuron. I. Selective transfer of newly synthesized phospholipid into the growing neurite. J Cell Biol. 1983 Oct;97(4):1038–1042. doi: 10.1083/jcb.97.4.1038. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pfenninger K. H., Maylié-Pfenninger M. F. Lectin labeling of sprouting neurons. I. Regional distribution of surface glycoconjugates. J Cell Biol. 1981 Jun;89(3):536–546. doi: 10.1083/jcb.89.3.536. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pfenninger K. H., Maylié-Pfenninger M. F. Lectin labeling of sprouting neurons. II. Relative movement and appearance of glycoconjugates during plasmalemmal expansion. J Cell Biol. 1981 Jun;89(3):547–559. doi: 10.1083/jcb.89.3.547. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Raff M. C., Abney E., Brockes J. P., Hornby-Smith A. Schwann cell growth factors. Cell. 1978 Nov;15(3):813–822. doi: 10.1016/0092-8674(78)90266-0. [DOI] [PubMed] [Google Scholar]
- Rapraeger A. C., Bernfield M. Heparan sulfate proteoglycans from mouse mammary epithelial cells. A putative membrane proteoglycan associates quantitatively with lipid vesicles. J Biol Chem. 1983 Mar 25;258(6):3632–3636. [PubMed] [Google Scholar]
- 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]
- Robinson H. C., Brett M. J., Tralaggan P. J., Lowther D. A., Okayama M. The effect of D-xylose, beta-D-xylosides and beta-D-galactosides on chondroitin sulphate biosynthesis in embryonic chicken cartilage. Biochem J. 1975 Apr;148(1):25–34. doi: 10.1042/bj1480025. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sakashita S., Engvall E., Ruoslahti E. Basement membrane glycoprotein laminin binds to heparin. FEBS Lett. 1980 Jul 28;116(2):243–246. doi: 10.1016/0014-5793(80)80654-5. [DOI] [PubMed] [Google Scholar]
- Salzer J. L., Bunge R. P., Glaser L. Studies of Schwann cell proliferation. III. Evidence for the surface localization of the neurite mitogen. J Cell Biol. 1980 Mar;84(3):767–778. doi: 10.1083/jcb.84.3.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Salzer J. L., Bunge R. P. Studies of Schwann cell proliferation. I. An analysis in tissue culture of proliferation during development, Wallerian degeneration, and direct injury. J Cell Biol. 1980 Mar;84(3):739–752. doi: 10.1083/jcb.84.3.739. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Salzer J. L., Williams A. K., Glaser L., Bunge R. P. Studies of Schwann cell proliferation. II. Characterization of the stimulation and specificity of the response to a neurite membrane fraction. J Cell Biol. 1980 Mar;84(3):753–766. doi: 10.1083/jcb.84.3.753. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sobue G., Kreider B., Asbury A., Pleasure D. Specific and potent mitogenic effect of axolemmal fraction on Schwann cells from rat sciatic nerves in serum-containing and defined media. Brain Res. 1983 Dec 5;280(2):263–275. doi: 10.1016/0006-8993(83)90056-2. [DOI] [PubMed] [Google Scholar]
- Sobue G., Pleasure D. Adhesion of axolemmal fragments to Schwann cells: a signal- and target-specific process closely linked to axolemmal induction of Schwann cell mitosis. J Neurosci. 1985 Feb;5(2):379–387. doi: 10.1523/JNEUROSCI.05-02-00379.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thompson H. A., Spooner B. S. Proteoglycan and glycosaminoglycan synthesis in embryonic mouse salivary glands: effects of beta-D-xyloside, an inhibitor of branching morphogenesis. J Cell Biol. 1983 May;96(5):1443–1450. doi: 10.1083/jcb.96.5.1443. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thornton S. C., Mueller S. N., Levine E. M. Human endothelial cells: use of heparin in cloning and long-term serial cultivation. Science. 1983 Nov 11;222(4624):623–625. doi: 10.1126/science.6635659. [DOI] [PubMed] [Google Scholar]
- 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]
- Wood P. M. Separation of functional Schwann cells and neurons from normal peripheral nerve tissue. Brain Res. 1976 Oct 22;115(3):361–375. doi: 10.1016/0006-8993(76)90355-3. [DOI] [PubMed] [Google Scholar]
- Yanagishita M., Hascall V. C. Proteoglycans synthesized by rat ovarian granulosa cells in culture. Isolation, fractionation, and characterization of proteoglycans associated with the cell layer. J Biol Chem. 1984 Aug 25;259(16):10260–10269. [PubMed] [Google Scholar]
