DOI: 10.1242/jcs.00827. A role for the polysialic acid – neural cell adhesion molecule in PDGF-induced chemotaxis of oligodendrocyte precursor cells

A role for the polysialic acid – neural cell adhesion molecule in PDGF-induced chemotaxis of oligodendrocyte precursor cells

10.1242/jcs.00827

Crossref journal-article

The Company of Biologists

Journal of Cell Science (237)

Abstract

Directed migration of oligodendrocyte precursor cells (OPCs) is important for myelin formation and repair but the mechanisms of directional control are poorly understood. Here we have tested the role of polysialic acid-neural cell adhesion molecule (PSA-NCAM) in the directional migration of OPCs towards platelet-derived growth factor (PDGF). Using a Boyden microchemotaxis chamber and the Dunn direct viewing chamber, we show that in concentration gradients of PDGF, PSA-positive OPCs polarize and efficiently migrate towards the source of PDGF (chemotaxis). The loss or inactivation of the polysialic tail of NCAM leads to an altered pattern of OPC migration in response to PDGF gradients. Cells under these conditions, while being polarized and migrating, show no bias of displacement towards the source of PDGF and make random turns. By contrast, directed migration of OPCs towards basic fibroblast growth factor was not affected by the removal of PSA. Moreover, inactivation of PSA does not interfere with the random migration pattern of cells in uniform concentrations of PDGF (chemokinesis). These results suggest that PSA-NCAM is specifically involved in establishing the directionality of OPC migration in response to the concentration gradient of PDGF, but it is not essential for cell motility per se.

Bibliography

Zhang, H., Vutskits, L., Calaora, V., Durbec, P., & Kiss, J. Z. (2004). A role for the polysialic acid â neural cell adhesion molecule in PDGF-induced chemotaxis of oligodendrocyte precursor cells. Journal of Cell Science, 117(1), 93â103.

Authors 5

H. Zhang (first)
L. Vutskits (additional)
V. Calaora (additional)
P. Durbec (additional)
J. Z. Kiss (additional)

References 52 Referenced 105

Dates

Type	When
Created	21 years, 9 months ago (Nov. 24, 2003, 8:14 p.m.)
Deposited	1 year, 7 months ago (Jan. 11, 2024, 9:24 a.m.)
Indexed	1 month ago (Aug. 3, 2025, 7:03 p.m.)
Issued	21 years, 8 months ago (Jan. 1, 2004)
Published	21 years, 8 months ago (Jan. 1, 2004)
Published Print	21 years, 8 months ago (Jan. 1, 2004)

Funders 0

None

BibTeX

@article{Zhang_2004, title={A role for the polysialic acid – neural cell adhesion molecule in PDGF-induced chemotaxis of oligodendrocyte precursor cells}, volume={117}, ISSN={0021-9533}, url={http://dx.doi.org/10.1242/jcs.00827}, DOI={10.1242/jcs.00827}, number={1}, journal={Journal of Cell Science}, publisher={The Company of Biologists}, author={Zhang, H. and Vutskits, L. and Calaora, V. and Durbec, P. and Kiss, J. Z.}, year={2004}, month=jan, pages={93–103} }

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  "abstract": "<jats:p>Directed migration of oligodendrocyte precursor cells (OPCs) is important for myelin formation and repair but the mechanisms of directional control are poorly understood. Here we have tested the role of polysialic acid-neural cell adhesion molecule (PSA-NCAM) in the directional migration of OPCs towards platelet-derived growth factor (PDGF). Using a Boyden microchemotaxis chamber and the Dunn direct viewing chamber, we show that in concentration gradients of PDGF, PSA-positive OPCs polarize and efficiently migrate towards the source of PDGF (chemotaxis). The loss or inactivation of the polysialic tail of NCAM leads to an altered pattern of OPC migration in response to PDGF gradients. Cells under these conditions, while being polarized and migrating, show no bias of displacement towards the source of PDGF and make random turns. By contrast, directed migration of OPCs towards basic fibroblast growth factor was not affected by the removal of PSA. Moreover, inactivation of PSA does not interfere with the random migration pattern of cells in uniform concentrations of PDGF (chemokinesis). These results suggest that PSA-NCAM is specifically involved in establishing the directionality of OPC migration in response to the concentration gradient of PDGF, but it is not essential for cell motility per se.</jats:p>",
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      "unstructured": "Acheson, A., Sunshine, J. L. and Rutishauser, U. (1991). NCAM polysialic acid can regulate both cell-cell and cell-substrate interactions. J. Cell Biol.114, 143-153.",
      "DOI": "10.1083/jcb.114.1.143"
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      "doi-asserted-by": "crossref",
      "unstructured": "Allen, W. E., Zicha, D., Ridley, A. J. and Jones, G. E. (1998). A role for Cdc42 in macrophage chemotaxis. J. Cell Biol.141, 1147-1157.",
      "DOI": "10.1083/jcb.141.5.1147"
    },
    {
      "key": "2021042517553023300_REF3",
      "doi-asserted-by": "crossref",
      "unstructured": "Armstrong, R. C., Harvath, L. and Dubois-Dalcq, M. E. (1990). Type 1 astrocytes and oligodendrocyte-type 2 astrocyte glial progenitors migrate toward distinct molecules. J. Neurosci. Res.27, 400-407.",
      "DOI": "10.1002/jnr.490270319"
    },
    {
      "key": "2021042517553023300_REF4",
      "doi-asserted-by": "crossref",
      "unstructured": "Avellana-Adalid, V., Nait-Oumesmar, B., Lachapelle, F. and Baron-Van Evercooren, A. (1996). Expansion of rat oligodendrocyte progenitors into proliferative \u201coligospheres\u201d that retain differentiation potential. J. Neurosci. Res.45, 558-570.",
      "DOI": "10.1002/(SICI)1097-4547(19960901)45:5<558::AID-JNR6>3.0.CO;2-B"
    },
    {
      "key": "2021042517553023300_REF5",
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      "unstructured": "Barral-Moran, M. J., Calaora, V., Vutskits, L., Wang, C., Zhang, H., Rougon, G. and Kiss, J. Z. (2003). Contribution of PSA-NCAM to wound healing of glial monolayer. J. Neurosci. Res.72, 679-690.",
      "DOI": "10.1002/jnr.10627"
    },
    {
      "key": "2021042517553023300_REF6",
      "doi-asserted-by": "crossref",
      "unstructured": "Behar, T. N., Scott, C. A., Greene, C. L., Wen, X., Smith, S. V., Maric, D., Liu, Q. Y., Colton, C. A. and Barker, J. L. (1999). Glutamate acting at NMDA receptors stimulates embryonic cortical neuronal migration. J. Neurosci.19, 4449-4461.",
      "DOI": "10.1523/JNEUROSCI.19-11-04449.1999"
    },
    {
      "key": "2021042517553023300_REF7",
      "doi-asserted-by": "crossref",
      "unstructured": "Blakemore, W. F. and Keirstead, H. S. (1999). The origin of remyelinating cells in the central nervous system. J. Neuroimmunol.98, 69-76.",
      "DOI": "10.1016/S0165-5728(99)00083-1"
    },
    {
      "key": "2021042517553023300_REF8",
      "unstructured": "Blaschuk, K. L., Frost, E. E. and ffrench-Constant, C. (2000). The regulation of proliferation and differentiation in oligodendrocyte progenitor cells by alphaV integrins. Development127, 1961-1969."
    },
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      "key": "2021042517553023300_REF9",
      "doi-asserted-by": "crossref",
      "unstructured": "Chazal, G., Durbec, P., Jankovski, A., Rougon, G. and Cremer, H. (2000). Consequences of neural cell adhesion molecule deficiency on cell migration in the rostral migratory stream of the mouse. J. Neurosci.20, 1446-1457.",
      "DOI": "10.1523/JNEUROSCI.20-04-01446.2000"
    },
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      "key": "2021042517553023300_REF10",
      "doi-asserted-by": "crossref",
      "unstructured": "Chung, C. Y., Potikyan, G. and Firtel, R. A. (2001). Control of cell polarity and chemotaxis by Akt/PKB and PI3 kinase through the regulation of PAKa. Mol. Cell7, 937-947.",
      "DOI": "10.1016/S1097-2765(01)00247-7"
    },
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      "key": "2021042517553023300_REF11",
      "doi-asserted-by": "crossref",
      "unstructured": "Decker, L., Avellana-Adalid, V., Nait-Oumesmar, B., Durbec, P. and Baron-Van Evercooren, A. (2000). Oligodendrocyte precursor migration and differentiation: combined effects of PSA residues, growth factors, and substrates. Mol. Cell Neurosci.16, 422-439.",
      "DOI": "10.1006/mcne.2000.0885"
    },
    {
      "key": "2021042517553023300_REF12",
      "doi-asserted-by": "crossref",
      "unstructured": "Eisenbarth, G. S., Walsh, F. S. and Nirenberg, M. (1979). Monoclonal antibody to a plasma membrane antigen of neurons. Proc. Natl. Acad. Sci. USA76, 4913-4917.",
      "DOI": "10.1073/pnas.76.10.4913"
    },
    {
      "key": "2021042517553023300_REF13",
      "doi-asserted-by": "crossref",
      "unstructured": "Fok-Seang, J., DiProspero, N. A., Meiners, S., Muir, E. and Fawcett, J. W. (1998). Cytokine-induced changes in the ability of astrocytes to support migration of oligodendrocyte precursors and axon growth. Eur. J. Neurosci.10, 2400-2415.",
      "DOI": "10.1046/j.1460-9568.1998.00251.x"
    },
    {
      "key": "2021042517553023300_REF14",
      "doi-asserted-by": "crossref",
      "unstructured": "Foxman, E. F., Kunkel, E. J. and Butcher, E. C. (1999). Integrating conflicting chemotactic signals. The role of memory in leukocyte navigation. J. Cell Biol.147, 577-588.",
      "DOI": "10.1083/jcb.147.3.577"
    },
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      "key": "2021042517553023300_REF15",
      "doi-asserted-by": "crossref",
      "unstructured": "Frosch, M., Gorgen, I., Boulnois, G. J., Timmis, K. N. and Bitter-Suermann, D. (1985). NZB mouse system for production of monoclonal antibodies to weak bacterial antigens: isolation of an IgG antibody to the polysaccharide capsules of Escherichia coli K1 and group B meningococci. Proc. Natl. Acad. Sci. USA82, 1194-1198.",
      "DOI": "10.1073/pnas.82.4.1194"
    },
    {
      "key": "2021042517553023300_REF16",
      "doi-asserted-by": "crossref",
      "unstructured": "Funamoto, S., Meili, R., Lee, S., Parry, L. and Firtel, R. A. (2002). Spatial and temporal regulation of 3-phosphoinositides by PI 3-kinase and PTEN mediates chemotaxis. Cell109, 611-623.",
      "DOI": "10.1016/S0092-8674(02)00755-9"
    },
    {
      "key": "2021042517553023300_REF17",
      "doi-asserted-by": "crossref",
      "unstructured": "Grabham, P. W. and Goldberg, D. J. (1997). Nerve growth factor stimulates the accumulation of beta1 integrin at the tips of filopodia in the growth cones of sympathetic neurons. J. Neurosci.17, 5455-5465.",
      "DOI": "10.1523/JNEUROSCI.17-14-05455.1997"
    },
    {
      "key": "2021042517553023300_REF18",
      "doi-asserted-by": "crossref",
      "unstructured": "Hall, A. (1998). G proteins and small GTPases: distant relatives keep in touch. Science280, 2074-2075.",
      "DOI": "10.1126/science.280.5372.2074"
    },
    {
      "key": "2021042517553023300_REF19",
      "doi-asserted-by": "crossref",
      "unstructured": "Hu, H., Tomasiewicz, H., Magnuson, T. and Rutishauser, U. (1996). The role of polysialic acid in migration of olfactory bulb interneuron precursors in the subventricular zone. Neuron16, 735-743.",
      "DOI": "10.1016/S0896-6273(00)80094-X"
    },
    {
      "key": "2021042517553023300_REF20",
      "doi-asserted-by": "crossref",
      "unstructured": "Kiss, J. Z., Wang, C., Olive, S., Rougon, G., Lang, J., Baetens, D., Harry, D. and Pralong, W. F. (1994). Activity-dependent mobilization of the adhesion molecule polysialic NCAM to the cell surface of neurons and endocrine cells. EMBO J.13, 5284-5292.",
      "DOI": "10.1002/j.1460-2075.1994.tb06862.x"
    },
    {
      "key": "2021042517553023300_REF21",
      "doi-asserted-by": "crossref",
      "unstructured": "Lauffenburger, D. A. and Horwitz, A. F. (1996). Cell migration: a physically integrated molecular process. Cell84, 359-369.",
      "DOI": "10.1016/S0092-8674(00)81280-5"
    },
    {
      "key": "2021042517553023300_REF22",
      "doi-asserted-by": "crossref",
      "unstructured": "Lee, J. C., Mayer-Proschel, M. and Rao, M. S. (2000). Gliogenesis in the central nervous system. Glia30, 105-121.",
      "DOI": "10.1002/(SICI)1098-1136(200004)30:2<105::AID-GLIA1>3.0.CO;2-H"
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      "doi-asserted-by": "crossref",
      "unstructured": "Lillien, L. E., Sendtner, M., Rohrer, H., Hughes, S. M. and Raff, M. C. (1988). Type-2 astrocyte development in rat brain cultures is initiated by a CNTF-like protein produced by type-1 astrocytes. Neuron1, 485-494.",
      "DOI": "10.1016/0896-6273(88)90179-1"
    },
    {
      "key": "2021042517553023300_REF24",
      "doi-asserted-by": "crossref",
      "unstructured": "Lubetzki, C., Goujet-Zalc, C., Gansmuller, A., Monge, M., Brillat, A. and Zalc, B. (1991). Morphological, biochemical, and functional characterization of bulk isolated glial progenitor cells. J. Neurochem.56, 671-680.",
      "DOI": "10.1111/j.1471-4159.1991.tb08202.x"
    },
    {
      "key": "2021042517553023300_REF25",
      "doi-asserted-by": "crossref",
      "unstructured": "Miller, M., Bower, E., Levitt, P., Li, D. and Chantler, P. D. (1992). Myosin II distribution in neurons is consistent with a role in growth cone motility but not synaptic vesicle mobilization. Neuron8, 25-44.",
      "DOI": "10.1016/0896-6273(92)90106-N"
    },
    {
      "key": "2021042517553023300_REF26",
      "doi-asserted-by": "crossref",
      "unstructured": "Milner, R., Edwards, G., Streuli, C. and Ffrench-Constant, C. (1996). A role in migration for the alpha V beta 1 integrin expressed on oligodendrocyte precursors. J. Neurosci.16, 7240-7252.",
      "DOI": "10.1523/JNEUROSCI.16-22-07240.1996"
    },
    {
      "key": "2021042517553023300_REF27",
      "doi-asserted-by": "crossref",
      "unstructured": "Milner, R., Anderson, H. J., Rippon, R. F., McKay, J. S., Franklin, R. J., Marchionni, M. A., Reynolds, R. and Ffrench-Constant, C. (1997). Contrasting effects of mitogenic growth factors on oligodendrocyte precursor cell migration. Glia19, 85-90.",
      "DOI": "10.1002/(SICI)1098-1136(199701)19:1<85::AID-GLIA9>3.0.CO;2-9"
    },
    {
      "key": "2021042517553023300_REF28",
      "doi-asserted-by": "crossref",
      "unstructured": "Muller, D., Djebbara-Hannas, Z., Jourdain, P., Vutskits, L., Durbec, P., Rougon, G. and Kiss, J. Z. (2000). Brain-derived neurotrophic factor restores long-term potentiation in polysialic acid-neural cell adhesion molecule-deficient hippocampus. Proc. Natl. Acad. Sci. USA97, 4315-4320.",
      "DOI": "10.1073/pnas.070022697"
    },
    {
      "key": "2021042517553023300_REF29",
      "doi-asserted-by": "crossref",
      "unstructured": "Noble, M., Murray, K., Stroobant, P., Waterfield, M. D. and Riddle, P. (1988). Platelet-derived growth factor promotes division and motility and inhibits premature differentiation of the oligodendrocyte/type-2 astrocyte progenitor cell. Nature333, 560-562.",
      "DOI": "10.1038/333560a0"
    },
    {
      "key": "2021042517553023300_REF30",
      "doi-asserted-by": "crossref",
      "unstructured": "Ono, K., Tomasiewicz, H., Magnuson, T. and Rutishauser, U. (1994). N-CAM mutation inhibits tangential neuronal migration and is phenocopied by enzymatic removal of polysialic acid. Neuron13, 595-609.",
      "DOI": "10.1016/0896-6273(94)90028-0"
    },
    {
      "key": "2021042517553023300_REF31",
      "doi-asserted-by": "crossref",
      "unstructured": "Ono, K., Yasui, Y., Rutishauser, U. and Miller, R. H. (1997). Focal ventricular origin and migration of oligodendrocyte precursors into the chick optic nerve. Neuron19, 283-292.",
      "DOI": "10.1016/S0896-6273(00)80939-3"
    },
    {
      "key": "2021042517553023300_REF32",
      "doi-asserted-by": "crossref",
      "unstructured": "Parent, C. A. and Devreotes, P. N. (1999). A cell's sense of direction. Science284, 765-770.",
      "DOI": "10.1126/science.284.5415.765"
    },
    {
      "key": "2021042517553023300_REF33",
      "doi-asserted-by": "crossref",
      "unstructured": "Ranscht, B., Clapshaw, P. A., Price, J., Noble, M. and Seifert, W. (1982). Development of oligodendrocytes and Schwann cells studied with a monoclonal antibody against galactocerebroside. Proc. Natl. Acad. Sci. USA79, 2709-2713.",
      "DOI": "10.1073/pnas.79.8.2709"
    },
    {
      "key": "2021042517553023300_REF34",
      "doi-asserted-by": "crossref",
      "unstructured": "Rougon, G., Dubois, C., Buckley, N., Magnani, J. L. and Zollinger, W. (1986). A monoclonal antibody against meningococcus group B polysaccharides distinguishes embryonic from adult N-CAM. J. Cell Biol.103, 2429-2437.",
      "DOI": "10.1083/jcb.103.6.2429"
    },
    {
      "key": "2021042517553023300_REF35",
      "doi-asserted-by": "crossref",
      "unstructured": "Rutishauser, U., Acheson, A., Hall, A. K., Mann, D. M. and Sunshine, J. (1988). The neural cell adhesion molecule (NCAM) as a regulator of cell-cell interactions. Science240, 53-57.",
      "DOI": "10.1126/science.3281256"
    },
    {
      "key": "2021042517553023300_REF36",
      "doi-asserted-by": "crossref",
      "unstructured": "Schmidt, C., Ohlemeyer, C., Labrakakis, C., Walter, T., Kettenmann, H. and Schnitzer, J. (1997). Analysis of motile oligodendrocyte precursor cells in vitro and in brain slices. Glia20, 284-298.",
      "DOI": "10.1002/(SICI)1098-1136(199708)20:4<284::AID-GLIA2>3.0.CO;2-6"
    },
    {
      "key": "2021042517553023300_REF37",
      "doi-asserted-by": "crossref",
      "unstructured": "Simpson, P. B. and Armstrong, R. C. (1999). Intracellular signals and cytoskeletal elements involved in oligodendrocyte progenitor migration. Glia26, 22-35.",
      "DOI": "10.1002/(SICI)1098-1136(199903)26:1<22::AID-GLIA3>3.0.CO;2-M"
    },
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      "key": "2021042517553023300_REF38",
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      "unstructured": "Spassky, N., Heydon, K., Mangatal, A., Jankovski, A., Olivier, C., Queraud-Lesaux, F., Goujet-Zalc, C., Thomas, J. L. and Zalc, B. (2001). Sonic hedgehog-dependent emergence of oligodendrocytes in the telencephalon: evidence for a source of oligodendrocytes in the olfactory bulb that is independent of PDGFRalpha signaling. Development128, 4993-5004.",
      "DOI": "10.1242/dev.128.24.4993"
    },
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      "key": "2021042517553023300_REF39",
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      "DOI": "10.1523/JNEUROSCI.22-14-05992.2002"
    },
    {
      "key": "2021042517553023300_REF40",
      "doi-asserted-by": "crossref",
      "unstructured": "Sugimoto, Y., Taniguchi, M., Yagi, T., Akagi, Y., Nojyo, Y. and Tamamaki, N. (2001). Guidance of glial precursor cell migration by secreted cues in the developing optic nerve. Development128, 3321-3330.",
      "DOI": "10.1242/dev.128.17.3321"
    },
    {
      "key": "2021042517553023300_REF41",
      "doi-asserted-by": "crossref",
      "unstructured": "Trotter, J., Bitter-Suermann, D. and Schachner, M. (1989). Differentiation-regulated loss of the polysialylated embryonic form and expression of the different polypeptides of the neural cell adhesion molecule by cultured oligodendrocytes and myelin. J. Neurosci. Res.22, 369-383.",
      "DOI": "10.1002/jnr.490220402"
    },
    {
      "key": "2021042517553023300_REF42",
      "doi-asserted-by": "crossref",
      "unstructured": "Tsai, H. H., Frost, E., To, V., Robinson, S., Ffrench-Constant, C., Geertman, R., Ransohoff, R. M. and Miller, R. H. (2002). The chemokine receptor CXCR2 controls positioning of oligodendrocyte precursors in developing spinal cord by arresting their migration. Cell110, 373-383.",
      "DOI": "10.1016/S0092-8674(02)00838-3"
    },
    {
      "key": "2021042517553023300_REF43",
      "doi-asserted-by": "crossref",
      "unstructured": "Tsai, H. H., Tessier-Lavigne, M. and Miller, R. H. (2003). Netrin 1 mediates spinal cord oligodendrocyte precursor dispersal. Development130, 2095-2105.",
      "DOI": "10.1242/dev.00424"
    },
    {
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      "DOI": "10.1046/j.1460-9568.2003.02660.x"
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      "DOI": "10.1523/JNEUROSCI.14-07-04446.1994"
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      "DOI": "10.1083/jcb.135.6.1565"
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      "DOI": "10.1073/pnas.96.7.4089"
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