We have investigated the expression patterns and subcellular localization in nervous tissue of glypican, a major glycosylphosphatidylinositol-anchored heparan sulfate proteoglycan that is predominantly synthesized by neurons, and of biglycan, a small, leucine-rich chondroitin sulfate proteoglycan. By laser scanning confocal microscopy of rat central nervous tissue and C6 glioma cells, we found that a significant portion of the glypican and biglycan immunoreactivity colocalized with nuclear staining by propidium iodide and was also seen in isolated nuclei. In certain regions, staining was selective, insofar as glypican and biglycan immunoreactivity in the nucleus was seen predominantly in a subpopulation of large spinal cord neurons. The amino acid sequences of both proteoglycans contain potential nuclear localization signals, and these were demonstrated to be functional based on their ability to target β-galactosidase fusion proteins to the nuclei of transfected 293 cells. Nuclear localization of glypican β-galactosidase or Fc fusion proteins in transfected 293 cells and C6 glioma cells was greatly reduced or abolished after mutation of the basic amino acids or deletion of the sequence containing the nuclear localization signal, and no nuclear staining was seen in the case of heparan sulfate and chondroitin sulfate proteoglycans that do not possess a nuclear localization signal, such as syndecan-3 or decorin (which is closely related in structure to biglycan). Transfection of COS-1 cells with an epitope-tagged glypican cDNA demonstrated transport of the full-length proteoglycan to the nucleus, and there are also dynamic changes in the pattern of glypican immunoreactivity in the nucleus of C6 cells both during cell division and correlated with different phases of the cell cycle. Our data therefore suggest that in certain cells and central nervous system regions, glypican and biglycan may be involved in the regulation of cell division and survival by directly participating in nuclear processes.
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17 November 1997
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November 17 1997
Glypican and Biglycan in the Nuclei of Neurons and Glioma Cells: Presence of Functional Nuclear Localization Signals and Dynamic Changes in Glypican During the Cell Cycle
Yu Liang,
Yu Liang
*Department of Pharmacology, New York University Medical Center, New York 10016; ‡Shriners Hospital for Crippled Children, McGill University, Montreal, Canada; and §Department of Pharmacology, State University of New York, Health Science Center, Brooklyn, New York 11203
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Monika Häring,
Monika Häring
*Department of Pharmacology, New York University Medical Center, New York 10016; ‡Shriners Hospital for Crippled Children, McGill University, Montreal, Canada; and §Department of Pharmacology, State University of New York, Health Science Center, Brooklyn, New York 11203
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Peter J. Roughley,
Peter J. Roughley
*Department of Pharmacology, New York University Medical Center, New York 10016; ‡Shriners Hospital for Crippled Children, McGill University, Montreal, Canada; and §Department of Pharmacology, State University of New York, Health Science Center, Brooklyn, New York 11203
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Renée K. Margolis,
Renée K. Margolis
*Department of Pharmacology, New York University Medical Center, New York 10016; ‡Shriners Hospital for Crippled Children, McGill University, Montreal, Canada; and §Department of Pharmacology, State University of New York, Health Science Center, Brooklyn, New York 11203
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Richard U. Margolis
Richard U. Margolis
*Department of Pharmacology, New York University Medical Center, New York 10016; ‡Shriners Hospital for Crippled Children, McGill University, Montreal, Canada; and §Department of Pharmacology, State University of New York, Health Science Center, Brooklyn, New York 11203
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Yu Liang,
Monika Häring,
Peter J. Roughley,
Renée K. Margolis,
Richard U. Margolis
*Department of Pharmacology, New York University Medical Center, New York 10016; ‡Shriners Hospital for Crippled Children, McGill University, Montreal, Canada; and §Department of Pharmacology, State University of New York, Health Science Center, Brooklyn, New York 11203
Address all correspondence to Richard U. Margolis, Department of Pharmacology, New York University Medical Center, 550 First Avenue, New York, NY 10016. Tel.: (212) 263-7113; Fax: (212) 263-8632.
1. Abbreviation used in this paper: bFGF, basic fibroblast growth factor.
Received:
June 03 1997
Revision Received:
September 02 1997
Online ISSN: 1540-8140
Print ISSN: 0021-9525
1997
J Cell Biol (1997) 139 (4): 851–864.
Article history
Received:
June 03 1997
Revision Received:
September 02 1997
Citation
Yu Liang, Monika Häring, Peter J. Roughley, Renée K. Margolis, Richard U. Margolis; Glypican and Biglycan in the Nuclei of Neurons and Glioma Cells: Presence of Functional Nuclear Localization Signals and Dynamic Changes in Glypican During the Cell Cycle . J Cell Biol 17 November 1997; 139 (4): 851–864. doi: https://doi.org/10.1083/jcb.139.4.851
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