Isolation of a neural chondroitin sulfate proteoglycan with neurite outgrowth promoting properties

doi:10.1083/jcb.126.3.783

This Article

	Full Text (PDF, 4015K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Faissner, A.
	Articles by Schachner, M.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Faissner, A.
	Articles by Schachner, M.


Social Bookmarking

	What's this?

ARTICLES

Isolation of a neural chondroitin sulfate proteoglycan with neurite outgrowth promoting properties

A Faissner, A Clement, A Lochter, A Streit, C Mandl and M Schachner
Department of Neurobiology, University of Heidelberg, Germany.

Proteoglycans are expressed in various tissues on cell surfaces and in the extracellular matrix and display substantial heterogeneity of both protein and carbohydrate constituents. The functions of individual proteoglycans of the nervous system are not well characterized, partly because specific reagents which would permit their isolation are missing. We report here that the monoclonal antibody 473HD, which binds to the surface of early differentiation stages of murine astrocytes and oligodendrocytes, reacts with the chondroitin sulfate/dermatan sulfate hybrid epitope DSD-1 expressed on a central nervous system chondroitin sulfate proteoglycan designated DSD-1-PG. When purified from detergent- free postnatal days 7 to 14 mouse brain extracts, DSD-1-PG displays an apparent molecular mass between 800-1,000 kD with a prominent core glycoprotein of 350-400 kD. Polyclonal anti-DSD-1-PG antibodies and monoclonal antibody 473HD react with the same molecular species as shown by immunocytochemistry and sequential immunoprecipitation performed on postnatal mouse cerebellar cultures, suggesting that the DSD-1 epitope is restricted to one proteoglycan. DSD-1-PG promotes neurite outgrowth of embryonic day 14 mesencephalic and embryonic day 18 hippocampal neurons from rat, a process which can be blocked by monoclonal antibody 473HD and by enzymatic removal of the DSD-1- epitope. These results show that the hybrid glycosaminoglycan structure DSD-1 supports the morphological differentiation of central nervous system neurons.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Yamada, S., Onishi, M., Fujinawa, R., Tadokoro, Y., Okabayashi, K., Asashima, M., Sugahara, K. (2009). Structural and functional changes of sulfated glycosaminoglycans in Xenopus laevis during embryogenesis. Glycobiology 19: 488-498 [Abstract] [Full Text]
Wang, H., Katagiri, Y., McCann, T. E., Unsworth, E., Goldsmith, P., Yu, Z.-X., Tan, F., Santiago, L., Mills, E. M., Wang, Y., Symes, A. J., Geller, H. M. (2008). Chondroitin-4-sulfation negatively regulates axonal guidance and growth. J. Cell Sci. 121: 3083-3091 [Abstract] [Full Text]
Ozog, M. A., Modha, G., Church, J., Reilly, R., Naus, C. C. (2008). Co-administration of Ciliary Neurotrophic Factor with Its Soluble Receptor Protects against Neuronal Death and Enhances Neurite Outgrowth. J. Biol. Chem. 283: 6546-6560 [Abstract] [Full Text]
Fongmoon, D., Shetty, A. K., Basappa, , Yamada, S., Sugiura, M., Kongtawelert, P., Sugahara, K. (2007). Chondroitinase-mediated Degradation of Rare 3-O-Sulfated Glucuronic Acid in Functional Oversulfated Chondroitin Sulfate K and E. J. Biol. Chem. 282: 36895-36904 [Abstract] [Full Text]
Yamada, S., Morimoto, H., Fujisawa, T., Sugahara, K. (2007). Glycosaminoglycans in Hydra magnipapillata (Hydrozoa, Cnidaria): demonstration of chondroitin in the developing nematocyst, the sting organelle, and structural characterization of glycosaminoglycans. Glycobiology 17: 886-894 [Abstract] [Full Text]
Sirko, S., von Holst, A., Wizenmann, A., Gotz, M., Faissner, A. (2007). Chondroitin sulfate glycosaminoglycans control proliferation, radial glia cell differentiation and neurogenesis in neural stem/progenitor cells. Development 134: 2727-2738 [Abstract] [Full Text]
Purushothaman, A., Fukuda, J., Mizumoto, S., ten Dam, G. B., van Kuppevelt, T. H., Kitagawa, H., Mikami, T., Sugahara, K. (2007). Functions of Chondroitin Sulfate/Dermatan Sulfate Chains in Brain Development: CRITICAL ROLES OF E AND iE DISACCHARIDE UNITS RECOGNIZED BY A SINGLE CHAIN ANTIBODY GD3G7. J. Biol. Chem. 282: 19442-19452 [Abstract] [Full Text]
Santos-Silva, A., Fairless, R., Frame, M. C., Montague, P., Smith, G. M., Toft, A., Riddell, J. S., Barnett, S. C. (2007). FGF/Heparin Differentially Regulates Schwann Cell and Olfactory Ensheathing Cell Interactions with Astrocytes: A Role in Astrocytosis. J. Neurosci. 27: 7154-7167 [Abstract] [Full Text]
Yanagisawa, M., Yu, R. K (2007). The expression and functions of glycoconjugates in neural stem cells. Glycobiology 17: 57R-74R [Abstract] [Full Text]
Deepa, S. S, Yamada, S., Fukui, S., Sugahara, K. (2007). Structural determination of novel sulfated octasaccharides isolated from chondroitin sulfate of shark cartilage and their application for characterizing monoclonal antibody epitopes. Glycobiology 17: 631-645 [Abstract] [Full Text]
Li, F., Shetty, A. K., Sugahara, K. (2007). Neuritogenic Activity of Chondroitin/Dermatan Sulfate Hybrid Chains of Embryonic Pig Brain and Their Mimicry from Shark Liver: INVOLVEMENT OF THE PLEIOTROPHIN AND HEPATOCYTE GROWTH FACTOR SIGNALING PATHWAYS. J. Biol. Chem. 282: 2956-2966 [Abstract] [Full Text]
Zimmerman, J. E., Rizzo, W., Shockley, K. R., Raizen, D. M., Naidoo, N., Mackiewicz, M., Churchill, G. A., Pack, A. I. (2006). Multiple mechanisms limit the duration of wakefulness in Drosophila brain. Physiol. Genomics 27: 337-350 [Abstract] [Full Text]
Liu, B. P, Cafferty, W. B.J, Budel, S. O, Strittmatter, S. M (2006). Extracellular regulators of axonal growth in the adult central nervous system. Phil Trans R Soc B 361: 1593-1610 [Abstract] [Full Text]
Mitsunaga, C., Mikami, T., Mizumoto, S., Fukuda, J., Sugahara, K. (2006). Chondroitin Sulfate/Dermatan Sulfate Hybrid Chains in the Development of Cerebellum: SPATIOTEMPORAL REGULATION OF THE EXPRESSION OF CRITICAL DISULFATED DISACCHARIDES BY SPECIFIC SULFOTRANSFERASES. J. Biol. Chem. 281: 18942-18952 [Abstract] [Full Text]
Miller, M. J. C., Costello, C. E., Malmstrom, A., Zaia, J. (2006). A tandem mass spectrometric approach to determination of chondroitin/dermatan sulfate oligosaccharide glycoforms. Glycobiology 16: 502-513 [Abstract] [Full Text]
von Holst, A., Sirko, S., Faissner, A. (2006). The Unique 473HD-Chondroitinsulfate Epitope Is Expressed by Radial Glia and Involved in Neural Precursor Cell Proliferation. J. Neurosci. 26: 4082-4094 [Abstract] [Full Text]
Bao, X., Muramatsu, T., Sugahara, K. (2005). Demonstration of the Pleiotrophin-binding Oligosaccharide Sequences Isolated from Chondroitin Sulfate/Dermatan Sulfate Hybrid Chains of Embryonic Pig Brains. J. Biol. Chem. 280: 35318-35328 [Abstract] [Full Text]
Kuan, W. -L., Barker, R. A. (2005). New Therapeutic Approaches to Parkinson's Disease Including Neural Transplants. Neurorehabil Neural Repair 19: 155-181 [Abstract]
Bao, X., Pavao, M. S. G., dos Santos, J. C., Sugahara, K. (2005). A Functional Dermatan Sulfate Epitope Containing Iduronate(2-O-sulfate){alpha}1-3GalNAc(6-O-sulfate) Disaccharide in the Mouse Brain: DEMONSTRATION USING A NOVEL MONOCLONAL ANTIBODY RAISED AGAINST DERMATAN SULFATE OF ASCIDIAN ASCIDIA NIGRA. J. Biol. Chem. 280: 23184-23193 [Abstract] [Full Text]
Ito, Y., Hikino, M., Yajima, Y., Mikami, T., Sirko, S., von Holst, A., Faissner, A., Fukui, S., Sugahara, K. (2005). Structural characterization of the epitopes of the monoclonal antibodies 473HD, CS-56, and MO-225 specific for chondroitin sulfate D-type using the oligosaccharide library. Glycobiology 15: 593-603 [Abstract] [Full Text]
Lemons, M. L., Barua, S., Abanto, M. L., Halfter, W., Condic, M. L. (2005). Adaptation of Sensory Neurons to Hyalectin and Decorin Proteoglycans. J. Neurosci. 25: 4964-4973 [Abstract] [Full Text]
Bao, X., Mikami, T., Yamada, S., Faissner, A., Muramatsu, T., Sugahara, K. (2005). Heparin-binding Growth Factor, Pleiotrophin, Mediates Neuritogenic Activity of Embryonic Pig Brain-derived Chondroitin Sulfate/Dermatan Sulfate Hybrid Chains. J. Biol. Chem. 280: 9180-9191 [Abstract] [Full Text]
Nandini, C. D., Itoh, N., Sugahara, K. (2005). Novel 70-kDa Chondroitin Sulfate/Dermatan Sulfate Hybrid Chains with a Unique Heterogenous Sulfation Pattern from Shark Skin, Which Exhibit Neuritogenic Activity and Binding Activities for Growth Factors and Neurotrophic Factors. J. Biol. Chem. 280: 4058-4069 [Abstract] [Full Text]
Nandini, C. D., Mikami, T., Ohta, M., Itoh, N., Akiyama-Nambu, F., Sugahara, K. (2004). Structural and Functional Characterization of Oversulfated Chondroitin Sulfate/Dermatan Sulfate Hybrid Chains from the Notochord of Hagfish: NEURITOGENIC AND BINDING ACTIVITIES FOR GROWTH FACTORS AND NEUROTROPHIC FACTORS. J. Biol. Chem. 279: 50799-50809 [Abstract] [Full Text]
Bao, X., Nishimura, S., Mikami, T., Yamada, S., Itoh, N., Sugahara, K. (2004). Chondroitin Sulfate/Dermatan Sulfate Hybrid Chains from Embryonic Pig Brain, Which Contain a Higher Proportion of L-Iduronic Acid than Those from Adult Pig Brain, Exhibit Neuritogenic and Growth Factor Binding Activities. J. Biol. Chem. 279: 9765-9776 [Abstract] [Full Text]
Hikino, M., Mikami, T., Faissner, A., Vilela-Silva, A.-C. E. S., Pavao, M. S. G., Sugahara, K. (2003). Oversulfated Dermatan Sulfate Exhibits Neurite Outgrowth-promoting Activity toward Embryonic Mouse Hippocampal Neurons: IMPLICATIONS OF DERMATAN SULFATE IN NEURITOGENESIS IN THE BRAIN. J. Biol. Chem. 278: 43744-43754 [Abstract] [Full Text]
Mikami, T., Mizumoto, S., Kago, N., Kitagawa, H., Sugahara, K. (2003). Specificities of Three Distinct Human Chondroitin/Dermatan N-Acetylgalactosamine 4-O-Sulfotransferases Demonstrated Using Partially Desulfated Dermatan Sulfate as an Acceptor: IMPLICATION OF DIFFERENTIAL ROLES IN DERMATAN SULFATE BIOSYNTHESIS. J. Biol. Chem. 278: 36115-36127 [Abstract] [Full Text]
Garwood, J., Heck, N., Reichardt, F., Faissner, A. (2003). Phosphacan Short Isoform, a Novel Non-proteoglycan Variant of Phosphacan/Receptor Protein Tyrosine Phosphatase-{beta}, Interacts with Neuronal Receptors and Promotes Neurite Outgrowth. J. Biol. Chem. 278: 24164-24173 [Abstract] [Full Text]
Deepa, S. S., Umehara, Y., Higashiyama, S., Itoh, N., Sugahara, K. (2002). Specific Molecular Interactions of Oversulfated Chondroitin Sulfate E with Various Heparin-binding Growth Factors. IMPLICATIONS AS A PHYSIOLOGICAL BINDING PARTNER IN THE BRAIN AND OTHER TISSUES. J. Biol. Chem. 277: 43707-43716 [Abstract] [Full Text]
Kang, H.-G., Evers, M. R., Xia, G., Baenziger, J. U., Schachner, M. (2002). Molecular Cloning and Characterization of Chondroitin-4-O-sulfotransferase-3. A NOVEL MEMBER OF THE HNK-1 FAMILY OF SULFOTRANSFERASES. J. Biol. Chem. 277: 34766-34772 [Abstract] [Full Text]
Becker, C. G., Becker, T. (2002). Repellent Guidance of Regenerating Optic Axons by Chondroitin Sulfate Glycosaminoglycans in Zebrafish. J. Neurosci. 22: 842-853 [Abstract] [Full Text]
Forster, E., Zhao, S., Frotscher, M. (2001). Hyaluronan-associated adhesive cues control fiber segregation in the hippocampus. Development 128: 3029-3039 [Abstract] [Full Text]
Harroch, S., Palmeri, M., Rosenbluth, J., Custer, A., Okigaki, M., Shrager, P., Blum, M., Buxbaum, J. D., Schlessinger, J. (2000). No Obvious Abnormality in Mice Deficient in Receptor Protein Tyrosine Phosphatase beta. Mol. Cell. Biol. 20: 7706-7715 [Abstract] [Full Text]
Bandtlow, C. E., Zimmermann, D. R. (2000). Proteoglycans in the Developing Brain: New Conceptual Insights for Old Proteins. Physiol. Rev. 80: 1267-1290 [Abstract] [Full Text]
Lauder, R. M., Huckerby, T. N., Nieduszynski, I. A. (2000). A fingerprinting method for chondroitin/dermatan sulfate and hyaluronan oligosaccharides. Glycobiology 10: 393-401 [Abstract] [Full Text]
Yamauchi, S., Mita, S., Matsubara, T., Fukuta, M., Habuchi, H., Kimata, K., Habuchi, O. (2000). Molecular Cloning and Expression of Chondroitin 4-Sulfotransferase. J. Biol. Chem. 275: 8975-8981 [Abstract] [Full Text]
Condic, M. L., Snow, D. M., Letourneau, P. C. (1999). Embryonic Neurons Adapt to the Inhibitory Proteoglycan Aggrecan by Increasing Integrin Expression. J. Neurosci. 19: 10036-10043 [Abstract] [Full Text]
Fidler, P. S., Schuette, K., Asher, R. A., Dobbertin, A., Thornton, S. R., Calle-Patino, Y., Muir, E., Levine, J. M., Geller, H. M., Rogers, J. H., Faissner, A., Fawcett, J. W. (1999). Comparing Astrocytic Cell Lines that Are Inhibitory or Permissive for Axon Growth: the Major Axon-Inhibitory Proteoglycan Is NG2. J. Neurosci. 19: 8778-8788 [Abstract] [Full Text]
Garwood, J., Schnadelbach, O., Clement, A., Schutte, K., Bach, A., Faissner, A. (1999). DSD-1-Proteoglycan Is the Mouse Homolog of Phosphacan and Displays Opposing Effects on Neurite Outgrowth Dependent on Neuronal Lineage. J. Neurosci. 19: 3888-3899 [Abstract] [Full Text]
Maeda, N., Ichihara-Tanaka, K., Kimura, T., Kadomatsu, K., Muramatsu, T., Noda, M. (1999). A Receptor-like Protein-tyrosine Phosphatase PTPzeta /RPTPbeta Binds a Heparin-binding Growth Factor Midkine. INVOLVEMENT OF ARGININE 78�OF MIDKINE IN THE HIGH AFFINITY BINDING TO PTPzeta. J. Biol. Chem. 274: 12474-12479 [Abstract] [Full Text]
Kobayashi, M., Sugumaran, G., Liu, J., Shworak, N. W., Silbert, J. E., Rosenberg, R. D. (1999). Molecular Cloning and Characterization of a Human Uronyl 2-Sulfotransferase That Sulfates Iduronyl and Glucuronyl Residues in Dermatan/Chondroitin Sulfate. J. Biol. Chem. 274: 10474-10480 [Abstract] [Full Text]
Yamauchi, S., Hirahara, Y., Usui, H., Takeda, Y., Hoshino, M., Fukuta, M., Kimura, J. H., Habuchi, O. (1999). Purification and Characterization of Chondroitin 4-Sulfotransferase from the Culture Medium of a Rat Chondrosarcoma Cell Line. J. Biol. Chem. 274: 2456-2463 [Abstract] [Full Text]
Calvet, S., Doherty, P., Prochiantz, A. (1998). Identification of a Signaling Pathway Activated Specifically in the Somatodendritic Compartment by a Heparan Sulfate That Regulates Dendrite Growth. J. Neurosci. 18: 9751-9765 [Abstract] [Full Text]
Clement, A. M., Nadanaka, S., Masayama, K., Mandl, C., Sugahara, K., Faissner, A. (1998). The DSD-1 Carbohydrate Epitope Depends on Sulfation, Correlates with Chondroitin Sulfate D Motifs, and Is Sufficient to Promote Neurite Outgrowth. J. Biol. Chem. 273: 28444-28453 [Abstract] [Full Text]
Hoffman-Kim, D., Lander, A. D., Jhaveri, S. (1998). Patterns of Chondroitin Sulfate Immunoreactivity in the Developing Tectum Reflect Regional Differences in Glycosaminoglycan Biosynthesis. J. Neurosci. 18: 5881-5890 [Abstract] [Full Text]
Schmalfeldt, M., Dours-Zimmermann, M. T., Winterhalter, K. H., Zimmermann, D. R. (1998). Versican V2 Is a Major Extracellular Matrix Component of the Mature Bovine Brain. J. Biol. Chem. 273: 15758-15764 [Abstract] [Full Text]
Nadanaka, S., Clement, A., Masayama, K., Faissner, A., Sugahara, K. (1998). Characteristic Hexasaccharide Sequences in Octasaccharides Derived from Shark Cartilage Chondroitin Sulfate D with a Neurite Outgrowth Promoting Activity. J. Biol. Chem. 273: 3296-3307 [Abstract] [Full Text]
Lander, C., Zhang, H., Hockfield, S. (1998). Neurons Produce a Neuronal Cell Surface-Associated Chondroitin Sulfate Proteoglycan. J. Neurosci. 18: 174-183 [Abstract] [Full Text]
Xiao, Z.-C., Bartsch, U., Margolis, R. K., Rougon, G., Montag, D., Schachner, M. (1997). Isolation of a Tenascin-R Binding Protein from Mouse Brain Membranes. A PHOSPHACAN-RELATED CHONDROITIN SULFATE PROTEOGLYCAN. J. Biol. Chem. 272: 32092-32101 [Abstract] [Full Text]
Kitagawa, H., Tsutsumi, K., Tone, Y., Sugahara, K. (1997). Developmental Regulation of the Sulfation Profile of Chondroitin Sulfate Chains in the Chicken Embryo Brain. J. Biol. Chem. 272: 31377-31381 [Abstract] [Full Text]
Faissner, A. (1997). REVIEW {blacksquare} : Glial Derived Extracellular Matrix Components: Important Roles in Axon Growth and Guidance. Neuroscientist 3: 371-380 [Abstract]
Yamada, H., Fredette, B., Shitara, K., Hagihara, K., Miura, R., Ranscht, B., Stallcup, W. B., Yamaguchi, Y. (1997). The Brain Chondroitin Sulfate Proteoglycan Brevican Associates with Astrocytes Ensheathing Cerebellar Glomeruli and Inhibits Neurite Outgrowth from Granule Neurons. J. Neurosci. 17: 7784-7795 [Abstract] [Full Text]
Stigson, M., Lofberg, J., Kjellen, L. (1997). PG-M/Versican-like Proteoglycans Are Components of Large Disulfide-stabilized Complexes in the Axolotl Embryo. J. Biol. Chem. 272: 3246-3253 [Abstract] [Full Text]
Kitagawa, H., Ujikawa, M., Sugahara, K. (1996). Developmental Changes in Serum UDP-GlcA:Chondroitin Glucuronyltransferase Activity. J. Biol. Chem. 271: 6583-6585 [Abstract] [Full Text]
Bonnet, F.�o., P�rin, J.-P., Charbonnier, F.�d�r., Camuzat, A.�s, Roussel, G., Nussbaum, J.-L., Alliel, P. M. (1996). Structure and Cellular Distribution of Mouse Brain Testican. J. Biol. Chem. 271: 4373-4380 [Abstract] [Full Text]
Maeda, N, Noda, M (1996). 6B4 proteoglycan/phosphacan is a repulsive substratum but promotes morphological differentiation of cortical neurons. Development 122: 647-658 [Abstract]
Thomas, L. B., Steindler, D. A. (1995). Review : Glial Boundaries and Scars: Programs for Normal Development and Wound Healing in the Brain. Neuroscientist 1: 142-154 [Abstract]
Hiraoka, N., Nakagawa, H., Ong, E., Akama, T. O., Fukuda, M. N., Fukuda, M. (2000). Molecular Cloning and Expression of Two Distinct Human Chondroitin 4-O-Sulfotransferases That Belong to the HNK-1 Sulfotransferase Gene Family. J. Biol. Chem. 275: 20188-20196 [Abstract] [Full Text]
Ueoka, C., Kaneda, N., Okazaki, I., Nadanaka, S., Muramatsu, T., Sugahara, K. (2000). Neuronal Cell Adhesion, Mediated by the Heparin-binding Neuroregulatory Factor Midkine, Is Specifically Inhibited by Chondroitin Sulfate E. STRUCTURAL AND FUNCTIONAL IMPLICATIONS OF THE OVER-SULFATED CHONDROITIN SULFATE. J. Biol. Chem. 275: 37407-37413 [Abstract] [Full Text]
Kang, H.-G., Evers, M. R., Xia, G., Baenziger, J. U., Schachner, M. (2001). Molecular Cloning and Expression of an N-Acetylgalactosamine-4-O-sulfotransferase That Transfers Sulfate to Terminal and Non-terminal beta 1,4-Linked N-Acetylgalactosamine. J. Biol. Chem. 276: 10861-10869 [Abstract] [Full Text]
Tsuchida, K., Shioi, J., Yamada, S., Boghosian, G., Wu, A., Cai, H., Sugahara, K., Robakis, N. K. (2001). Appican, the Proteoglycan Form of the Amyloid Precursor Protein, Contains Chondroitin Sulfate E in the Repeating Disaccharide Region and 4-O-Sulfated Galactose in the Linkage Region. J. Biol. Chem. 276: 37155-37160 [Abstract] [Full Text]