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. 2002 Sep 1;366(Pt 2):481–490. doi: 10.1042/BJ20020711

Molecular characterization of chicken syndecan-2 proteoglycan.

Ligong Chen 1, John R Couchman 1, Jacqueline Smith 1, Anne Woods 1
PMCID: PMC1222803  PMID: 12038962

Abstract

A partial syndecan-2 sequence (147 bp) was obtained from chicken embryonic fibroblast poly(A)+ RNA by reverse transcription-PCR. This partial sequence was used to produce a 5'-end-labelled probe. A chicken liver cDNA library was screened with this probe, and overlapping clones were obtained encompassing the entire cDNA of 3 kb. The open reading frame encodes a protein of 201 amino acids. The cytoplasmic domain is identical with that of mammalian syndecan-2, and highly similar to those of Xenopus laevis and zebrafish syndecan-2. The transmembrane domain is identical with that of mammalian and zebrafish syndecan-2, and highly similar to that of Xenopus laevis syndecan-2. The ectodomain is 45-62% identical with that of zebrafish, Xenopus laevis and mammalian syndecan-2. Two coding single nucleotide polymorphisms were observed. In vitro transcription and translation yielded a product of 30 kDa. Western blotting of chicken embryonic fibroblast cell lysates with species-specific monoclonal antibody mAb 8.1 showed that chicken syndecan-2 is substituted with heparan sulphate, and that the major form of chicken syndecan-2 isolated from chicken fibroblasts is consistent with the formation of SDS-resistant dimers, which is common for syndecans. A 5'-end-labelled probe hybridized to two mRNA species in chicken embryonic fibroblasts, while Northern analysis with poly(A)+ RNAs from different tissues of chicken embryos showed wide and distinct distributions of chicken syndecan-2 during embryonic development. This pattern was different from that reported for syndecan-4, but consistent with the roles of syndecan-2 in neural maturation and in mesenchymal-matrix interactions.

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Selected References

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  1. Alexander C. M., Reichsman F., Hinkes M. T., Lincecum J., Becker K. A., Cumberledge S., Bernfield M. Syndecan-1 is required for Wnt-1-induced mammary tumorigenesis in mice. Nat Genet. 2000 Jul;25(3):329–332. doi: 10.1038/77108. [DOI] [PubMed] [Google Scholar]
  2. Baciu P. C., Acaster C., Goetinck P. F. Molecular cloning and genomic organization of chicken syndecan-4. J Biol Chem. 1994 Jan 7;269(1):696–703. [PubMed] [Google Scholar]
  3. Bernfield M., Götte M., Park P. W., Reizes O., Fitzgerald M. L., Lincecum J., Zako M. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem. 1999;68:729–777. doi: 10.1146/annurev.biochem.68.1.729. [DOI] [PubMed] [Google Scholar]
  4. Cargill M., Altshuler D., Ireland J., Sklar P., Ardlie K., Patil N., Shaw N., Lane C. R., Lim E. P., Kalyanaraman N. Characterization of single-nucleotide polymorphisms in coding regions of human genes. Nat Genet. 1999 Jul;22(3):231–238. doi: 10.1038/10290. [DOI] [PubMed] [Google Scholar]
  5. Cohen A. R., Woods D. F., Marfatia S. M., Walther Z., Chishti A. H., Anderson J. M., Wood D. F. Human CASK/LIN-2 binds syndecan-2 and protein 4.1 and localizes to the basolateral membrane of epithelial cells. J Cell Biol. 1998 Jul 13;142(1):129–138. doi: 10.1083/jcb.142.1.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Collins F. S., Brooks L. D., Chakravarti A. A DNA polymorphism discovery resource for research on human genetic variation. Genome Res. 1998 Dec;8(12):1229–1231. doi: 10.1101/gr.8.12.1229. [DOI] [PubMed] [Google Scholar]
  7. Couchman J. R., Chen L., Woods A. Syndecans and cell adhesion. Int Rev Cytol. 2001;207:113–150. doi: 10.1016/s0074-7696(01)07004-8. [DOI] [PubMed] [Google Scholar]
  8. David G., Bai X. M., Van der Schueren B., Marynen P., Cassiman J. J., Van den Berghe H. Spatial and temporal changes in the expression of fibroglycan (syndecan-2) during mouse embryonic development. Development. 1993 Nov;119(3):841–854. doi: 10.1242/dev.119.3.841. [DOI] [PubMed] [Google Scholar]
  9. Echtermeyer F., Streit M., Wilcox-Adelman S., Saoncella S., Denhez F., Detmar M., Goetinck P. Delayed wound repair and impaired angiogenesis in mice lacking syndecan-4. J Clin Invest. 2001 Jan;107(2):R9–R14. doi: 10.1172/JCI10559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ethell I. M., Hagihara K., Miura Y., Irie F., Yamaguchi Y. Synbindin, A novel syndecan-2-binding protein in neuronal dendritic spines. J Cell Biol. 2000 Oct 2;151(1):53–68. doi: 10.1083/jcb.151.1.53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ethell I. M., Irie F., Kalo M. S., Couchman J. R., Pasquale E. B., Yamaguchi Y. EphB/syndecan-2 signaling in dendritic spine morphogenesis. Neuron. 2001 Sep 27;31(6):1001–1013. doi: 10.1016/s0896-6273(01)00440-8. [DOI] [PubMed] [Google Scholar]
  12. Ethell I. M., Yamaguchi Y. Cell surface heparan sulfate proteoglycan syndecan-2 induces the maturation of dendritic spines in rat hippocampal neurons. J Cell Biol. 1999 Feb 8;144(3):575–586. doi: 10.1083/jcb.144.3.575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gould S. E., Upholt W. B., Kosher R. A. Characterization of chicken syndecan-3 as a heparan sulfate proteoglycan and its expression during embryogenesis. Dev Biol. 1995 Apr;168(2):438–451. doi: 10.1006/dbio.1995.1093. [DOI] [PubMed] [Google Scholar]
  14. Granés F., García R., Casaroli-Marano R. P., Castel S., Rocamora N., Reina M., Ureña J. M., Vilaró S. Syndecan-2 induces filopodia by active cdc42Hs. Exp Cell Res. 1999 May 1;248(2):439–456. doi: 10.1006/excr.1999.4437. [DOI] [PubMed] [Google Scholar]
  15. Granés F., Urena J. M., Rocamora N., Vilaró S. Ezrin links syndecan-2 to the cytoskeleton. J Cell Sci. 2000 Apr;113(Pt 7):1267–1276. doi: 10.1242/jcs.113.7.1267. [DOI] [PubMed] [Google Scholar]
  16. Grootjans J. J., Zimmermann P., Reekmans G., Smets A., Degeest G., Dürr J., David G. Syntenin, a PDZ protein that binds syndecan cytoplasmic domains. Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):13683–13688. doi: 10.1073/pnas.94.25.13683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Horowitz A., Simons M. Phosphorylation of the cytoplasmic tail of syndecan-4 regulates activation of protein kinase Calpha. J Biol Chem. 1998 Oct 2;273(40):25548–25551. doi: 10.1074/jbc.273.40.25548. [DOI] [PubMed] [Google Scholar]
  18. Hsueh Y. P., Sheng M. Regulated expression and subcellular localization of syndecan heparan sulfate proteoglycans and the syndecan-binding protein CASK/LIN-2 during rat brain development. J Neurosci. 1999 Sep 1;19(17):7415–7425. doi: 10.1523/JNEUROSCI.19-17-07415.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ishiguro K., Kadomatsu K., Kojima T., Muramatsu H., Iwase M., Yoshikai Y., Yanada M., Yamamoto K., Matsushita T., Nishimura M. Syndecan-4 deficiency leads to high mortality of lipopolysaccharide-injected mice. J Biol Chem. 2001 Oct 3;276(50):47483–47488. doi: 10.1074/jbc.M106268200. [DOI] [PubMed] [Google Scholar]
  20. Ishiguro K., Kadomatsu K., Kojima T., Muramatsu H., Matsuo S., Kusugami K., Saito H., Muramatsu T. Syndecan-4 deficiency increases susceptibility to kappa-carrageenan-induced renal damage. Lab Invest. 2001 Apr;81(4):509–516. doi: 10.1038/labinvest.3780259. [DOI] [PubMed] [Google Scholar]
  21. Ishiguro K., Kadomatsu K., Kojima T., Muramatsu H., Nakamura E., Ito M., Nagasaka T., Kobayashi H., Kusugami K., Saito H. Syndecan-4 deficiency impairs the fetal vessels in the placental labyrinth. Dev Dyn. 2000 Dec;219(4):539–544. doi: 10.1002/1097-0177(2000)9999:9999<::AID-DVDY1081>3.0.CO;2-K. [DOI] [PubMed] [Google Scholar]
  22. Kim C. W., Goldberger O. A., Gallo R. L., Bernfield M. Members of the syndecan family of heparan sulfate proteoglycans are expressed in distinct cell-, tissue-, and development-specific patterns. Mol Biol Cell. 1994 Jul;5(7):797–805. doi: 10.1091/mbc.5.7.797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Klass C. M., Couchman J. R., Woods A. Control of extracellular matrix assembly by syndecan-2 proteoglycan. J Cell Sci. 2000 Feb;113(Pt 3):493–506. doi: 10.1242/jcs.113.3.493. [DOI] [PubMed] [Google Scholar]
  24. Kozak M. An analysis of vertebrate mRNA sequences: intimations of translational control. J Cell Biol. 1991 Nov;115(4):887–903. doi: 10.1083/jcb.115.4.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kramer Kenneth L., Yost H. Joseph. Ectodermal syndecan-2 mediates left-right axis formation in migrating mesoderm as a cell-nonautonomous Vg1 cofactor. Dev Cell. 2002 Jan;2(1):115–124. doi: 10.1016/s1534-5807(01)00107-1. [DOI] [PubMed] [Google Scholar]
  26. Kusano Y., Oguri K., Nagayasu Y., Munesue S., Ishihara M., Saiki I., Yonekura H., Yamamoto H., Okayama M. Participation of syndecan 2 in the induction of stress fiber formation in cooperation with integrin alpha5beta1: structural characteristics of heparan sulfate chains with avidity to COOH-terminal heparin-binding domain of fibronectin. Exp Cell Res. 2000 May 1;256(2):434–444. doi: 10.1006/excr.2000.4802. [DOI] [PubMed] [Google Scholar]
  27. Langford J. K., Stanley M. J., Cao D., Sanderson R. D. Multiple heparan sulfate chains are required for optimal syndecan-1 function. J Biol Chem. 1998 Nov 6;273(45):29965–29971. doi: 10.1074/jbc.273.45.29965. [DOI] [PubMed] [Google Scholar]
  28. Lee D., Oh E. S., Woods A., Couchman J. R., Lee W. Solution structure of a syndecan-4 cytoplasmic domain and its interaction with phosphatidylinositol 4,5-bisphosphate. J Biol Chem. 1998 May 22;273(21):13022–13029. doi: 10.1074/jbc.273.21.13022. [DOI] [PubMed] [Google Scholar]
  29. Longley R. L., Woods A., Fleetwood A., Cowling G. J., Gallagher J. T., Couchman J. R. Control of morphology, cytoskeleton and migration by syndecan-4. J Cell Sci. 1999 Oct;112(Pt 20):3421–3431. doi: 10.1242/jcs.112.20.3421. [DOI] [PubMed] [Google Scholar]
  30. McFall A. J., Rapraeger A. C. Identification of an adhesion site within the syndecan-4 extracellular protein domain. J Biol Chem. 1997 May 16;272(20):12901–12904. doi: 10.1074/jbc.272.20.12901. [DOI] [PubMed] [Google Scholar]
  31. Oh E. S., Couchman J. R., Woods A. Serine phosphorylation of syndecan-2 proteoglycan cytoplasmic domain. Arch Biochem Biophys. 1997 Aug 1;344(1):67–74. doi: 10.1006/abbi.1997.0180. [DOI] [PubMed] [Google Scholar]
  32. Oh E. S., Woods A., Couchman J. R. Multimerization of the cytoplasmic domain of syndecan-4 is required for its ability to activate protein kinase C. J Biol Chem. 1997 May 2;272(18):11805–11811. doi: 10.1074/jbc.272.18.11805. [DOI] [PubMed] [Google Scholar]
  33. Oh E. S., Woods A., Lim S. T., Theibert A. W., Couchman J. R. Syndecan-4 proteoglycan cytoplasmic domain and phosphatidylinositol 4,5-bisphosphate coordinately regulate protein kinase C activity. J Biol Chem. 1998 Apr 24;273(17):10624–10629. doi: 10.1074/jbc.273.17.10624. [DOI] [PubMed] [Google Scholar]
  34. Pierce A., Lyon M., Hampson I. N., Cowling G. J., Gallagher J. T. Molecular cloning of the major cell surface heparan sulfate proteoglycan from rat liver. J Biol Chem. 1992 Feb 25;267(6):3894–3900. [PubMed] [Google Scholar]
  35. Reizes O., Lincecum J., Wang Z., Goldberger O., Huang L., Kaksonen M., Ahima R., Hinkes M. T., Barsh G. S., Rauvala H. Transgenic expression of syndecan-1 uncovers a physiological control of feeding behavior by syndecan-3. Cell. 2001 Jul 13;106(1):105–116. doi: 10.1016/s0092-8674(01)00415-9. [DOI] [PubMed] [Google Scholar]
  36. Romarís M., Coomans C., Ceulemans H., Bruystens A. M., Vekemans S., David G. Molecular polymorphism of the syndecans. Identification of a hypo-glycanated murine syndecan-1 splice variant. J Biol Chem. 1999 Jun 25;274(26):18667–18674. doi: 10.1074/jbc.274.26.18667. [DOI] [PubMed] [Google Scholar]
  37. Selleck S. B. Proteoglycans and pattern formation: sugar biochemistry meets developmental genetics. Trends Genet. 2000 May;16(5):206–212. doi: 10.1016/s0168-9525(00)01997-1. [DOI] [PubMed] [Google Scholar]
  38. Tomita K., Yamasu K., Suyemitsu T. Cloning and characterization of cDNA for syndecan core protein in sea urchin embryos. Dev Growth Differ. 2000 Oct;42(5):449–458. doi: 10.1046/j.1440-169x.2000.00529.x. [DOI] [PubMed] [Google Scholar]
  39. Utani A., Nomizu M., Matsuura H., Kato K., Kobayashi T., Takeda U., Aota S., Nielsen P. K., Shinkai H. A unique sequence of the laminin alpha 3 G domain binds to heparin and promotes cell adhesion through syndecan-2 and -4. J Biol Chem. 2001 May 23;276(31):28779–28788. doi: 10.1074/jbc.M101420200. [DOI] [PubMed] [Google Scholar]
  40. Woods A., Couchman J. R. Protein kinase C involvement in focal adhesion formation. J Cell Sci. 1992 Feb;101(Pt 2):277–290. doi: 10.1242/jcs.101.2.277. [DOI] [PubMed] [Google Scholar]
  41. Woods A., Couchman J. R. Syndecans: synergistic activators of cell adhesion. Trends Cell Biol. 1998 May;8(5):189–192. doi: 10.1016/s0962-8924(98)01244-6. [DOI] [PubMed] [Google Scholar]
  42. Woods A., Longley R. L., Tumova S., Couchman J. R. Syndecan-4 binding to the high affinity heparin-binding domain of fibronectin drives focal adhesion formation in fibroblasts. Arch Biochem Biophys. 2000 Feb 1;374(1):66–72. doi: 10.1006/abbi.1999.1607. [DOI] [PubMed] [Google Scholar]
  43. Xu N., Chen C. Y., Shyu A. B. Modulation of the fate of cytoplasmic mRNA by AU-rich elements: key sequence features controlling mRNA deadenylation and decay. Mol Cell Biol. 1997 Aug;17(8):4611–4621. doi: 10.1128/mcb.17.8.4611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Yung S., Woods A., Chan T. M., Davies M., Williams J. D., Couchman J. R. Syndecan-4 up-regulation in proliferative renal disease is related to microfilament organization. FASEB J. 2001 Jul;15(9):1631–1633. doi: 10.1096/fj.00-0794fje. [DOI] [PubMed] [Google Scholar]

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