Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1989 Dec 1;109(6):3493–3501. doi: 10.1083/jcb.109.6.3493

The extracellular matrix of Volvox carteri: molecular structure of the cellular compartment

PMCID: PMC2115946  PMID: 2689458

Abstract

The extracellular matrix (ECM) of Volvox contains insoluble fibrous layers that surround individual cells at a distance to form contiguous cellular compartments. Using immunological techniques, we identified a sulfated surface glycoprotein (SSG 185) as the monomeric precursor of this substructure within the ECM. The primary structure of the SSG 185 poly-peptide chain has been derived from cDNA and genomic DNA. A central domain of the protein, 80 amino acid residues long, consists almost exclusively of hydroxyproline residues. The chemical structure of the highly sulfated polysaccharide covalently attached to SSG 185 has been determined by permethylation analysis. As revealed by EM, SSG 185 is a rod-shaped molecule with a 21-nm-long polysaccharide strand protruding from its central region. The chemical nature of the cross- links between SSG 185 monomers is discussed.

Full Text

The Full Text of this article is available as a PDF (2.2 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adair W. S., Steinmetz S. A., Mattson D. M., Goodenough U. W., Heuser J. E. Nucleated assembly of Chlamydomonas and Volvox cell walls. J Cell Biol. 1987 Nov;105(5):2373–2382. doi: 10.1083/jcb.105.5.2373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bozzaro S., Tsugita A., Janku M., Monok G., Opatz K., Gerisch G. Characterization of a purified cell surface glycoprotein as a contact site in Polysphondylium pallidum. Exp Cell Res. 1981 Jul;134(1):181–191. doi: 10.1016/0014-4827(81)90475-4. [DOI] [PubMed] [Google Scholar]
  3. Frischauf A. M., Lehrach H., Poustka A., Murray N. Lambda replacement vectors carrying polylinker sequences. J Mol Biol. 1983 Nov 15;170(4):827–842. doi: 10.1016/s0022-2836(83)80190-9. [DOI] [PubMed] [Google Scholar]
  4. Gerl L., Sumper M. Halobacterial flagellins are encoded by a multigene family. Characterization of five flagellin genes. J Biol Chem. 1988 Sep 15;263(26):13246–13251. [PubMed] [Google Scholar]
  5. Goodenough U. W., Gebhart B., Mecham R. P., Heuser J. E. Crystals of the Chlamydomonas reinhardtii cell wall: polymerization, depolymerization, and purification of glycoprotein monomers. J Cell Biol. 1986 Aug;103(2):405–417. doi: 10.1083/jcb.103.2.405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Goodenough U. W., Heuser J. E. The Chlamydomonas cell wall and its constituent glycoproteins analyzed by the quick-freeze, deep-etch technique. J Cell Biol. 1985 Oct;101(4):1550–1568. doi: 10.1083/jcb.101.4.1550. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gubler U., Hoffman B. J. A simple and very efficient method for generating cDNA libraries. Gene. 1983 Nov;25(2-3):263–269. doi: 10.1016/0378-1119(83)90230-5. [DOI] [PubMed] [Google Scholar]
  8. HAKOMORI S. A RAPID PERMETHYLATION OF GLYCOLIPID, AND POLYSACCHARIDE CATALYZED BY METHYLSULFINYL CARBANION IN DIMETHYL SULFOXIDE. J Biochem. 1964 Feb;55:205–208. [PubMed] [Google Scholar]
  9. Harris P. J., Henry R. J., Blakeney A. B., Stone B. A. An improved procedure for the methylation analysis of oligosaccharides and polysaccharides. Carbohydr Res. 1984 Apr 2;127(1):59–73. doi: 10.1016/0008-6215(84)85106-x. [DOI] [PubMed] [Google Scholar]
  10. Hills G. J., Phillips J. M., Gay M. R., Roberts K. Self-assembly of a plant cell wall in vitro. J Mol Biol. 1975 Aug 15;96(3):431–441. doi: 10.1016/0022-2836(75)90170-9. [DOI] [PubMed] [Google Scholar]
  11. Holst O., Christoffel V., Fründ R., Moll H., Sumper M. A phosphodiester bridge between two arabinose residues as a structural element of an extracellular glycoprotein of Volvox carteri. Eur J Biochem. 1989 May 1;181(2):345–350. doi: 10.1111/j.1432-1033.1989.tb14730.x. [DOI] [PubMed] [Google Scholar]
  12. Kirk D. L., Birchem R., King N. The extracellular matrix of Volvox: a comparative study and proposed system of nomenclature. J Cell Sci. 1986 Feb;80:207–231. doi: 10.1242/jcs.80.1.207. [DOI] [PubMed] [Google Scholar]
  13. Kirk M. M., Kirk D. L. Translational regulation of protein synthesis, in response to light, at a critical stage of Volvox development. Cell. 1985 Jun;41(2):419–428. doi: 10.1016/s0092-8674(85)80015-5. [DOI] [PubMed] [Google Scholar]
  14. Mages H. W., Tschochner H., Sumper M. The sexual inducer of Volvox carteri. Primary structure deduced from cDNA sequence. FEBS Lett. 1988 Jul 18;234(2):407–410. doi: 10.1016/0014-5793(88)80126-1. [DOI] [PubMed] [Google Scholar]
  15. Mages W., Salbaum J. M., Harper J. F., Schmitt R. Organization and structure of Volvox alpha-tubulin genes. Mol Gen Genet. 1988 Aug;213(2-3):449–458. doi: 10.1007/BF00339615. [DOI] [PubMed] [Google Scholar]
  16. Miller D. H., Mellman I. S., Lamport D. T., Miller M. The chemical composition of the cell wall of Chlamydomonas gymnogama and the concept of a plant cell wall protein. J Cell Biol. 1974 Nov;63(2 Pt 1):420–429. doi: 10.1083/jcb.63.2.420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mort A. J., Lamport D. T. Anhydrous hydrogen fluoride deglycosylates glycoproteins. Anal Biochem. 1977 Oct;82(2):289–309. doi: 10.1016/0003-2697(77)90165-8. [DOI] [PubMed] [Google Scholar]
  18. Mörgelin M., Paulsson M., Hardingham T. E., Heinegård D., Engel J. Cartilage proteoglycans. Assembly with hyaluronate and link protein as studied by electron microscopy. Biochem J. 1988 Jul 1;253(1):175–185. doi: 10.1042/bj2530175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nagasawa K., Inoue Y., Kamata T. Solvolytic desulfation of glycosaminoglycuronan sulfates with dimethyl sulfoxide containing water or methanol. Carbohydr Res. 1977 Sep;58(1):47–55. doi: 10.1016/s0008-6215(00)83402-3. [DOI] [PubMed] [Google Scholar]
  20. Ochiai H., Schwarz H., Merkl R., Wagle G., Gerisch G. Stage-specific antigens reacting with monoclonal antibodies against contact site A, a cell-surface glycoprotein of Dictyostelium discoideum. Cell Differ. 1982 Jan;11(1):1–13. doi: 10.1016/0045-6039(82)90011-2. [DOI] [PubMed] [Google Scholar]
  21. Reichlin M. Use of glutaraldehyde as a coupling agent for proteins and peptides. Methods Enzymol. 1980;70(A):159–165. doi: 10.1016/s0076-6879(80)70047-2. [DOI] [PubMed] [Google Scholar]
  22. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Starr R. C., Jaenicke L. Purification and characterization of the hormone initiating sexual morphogenesis in Volvox carteri f. nagariensis Iyengar. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1050–1054. doi: 10.1073/pnas.71.4.1050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Steiner A. L. Assay of cyclic nucleotides by radioimmunoassay methods. Methods Enzymol. 1974;38:96–105. doi: 10.1016/0076-6879(74)38016-0. [DOI] [PubMed] [Google Scholar]
  25. Terho T. T., Hartiala K. Method for determination of the sulfate content of glycosaminoglycans. Anal Biochem. 1971 Jun;41(2):471–476. doi: 10.1016/0003-2697(71)90167-9. [DOI] [PubMed] [Google Scholar]
  26. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Vaskovsky V. E., Kostetsky E. Y., Svetashev V. I., Zhukova I. G., Smirnova G. P. Glycolipids of marine invertebrates. Comp Biochem Physiol. 1970 May 1;34(1):163–177. doi: 10.1016/0010-406x(70)90064-2. [DOI] [PubMed] [Google Scholar]
  28. Vieira J., Messing J. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 1982 Oct;19(3):259–268. doi: 10.1016/0378-1119(82)90015-4. [DOI] [PubMed] [Google Scholar]
  29. Wenzl S., Sumper M. A novel glycosphingolipid that may participate in embryo inversion in Volvox carteri. Cell. 1986 Aug 15;46(4):633–639. doi: 10.1016/0092-8674(86)90889-5. [DOI] [PubMed] [Google Scholar]
  30. Wenzl S., Thym D., Sumper M. Development-dependent modification of the extracellular matrix by a sulphated glycoprotein in Volvox carteri. EMBO J. 1984 Apr;3(4):739–744. doi: 10.1002/j.1460-2075.1984.tb01877.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wieland F., Heitzer R., Schaefer W. Asparaginylglucose: Novel type of carbohydrate linkage. Proc Natl Acad Sci U S A. 1983 Sep;80(18):5470–5474. doi: 10.1073/pnas.80.18.5470. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES