Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1991 Nov 2;115(4):1159–1169. doi: 10.1083/jcb.115.4.1159

Mini-collagens in hydra nematocytes

PMCID: PMC2289959  PMID: 1955459

Abstract

We have isolated and characterized four collagen-related c-DNA clones (N-COL 1, N-COL 2, N-COL 3, N-COL 4) that are highly expressed in developing nematocytes in hydra. All four c-DNAs as well as their corresponding transcripts are small in size (600-1,000 bp). The deduced amino acid sequences show that they contain a central region consisting of 14 to 16 Gly-X-Y triplets. This region is flanked amino-terminal by a stretch of 14-23 proline residues and carboxy-terminal by a stretch of 6-9 prolines. At the NH2- and COOH-termini are repeated patterns of cysteine residues that are highly conserved between the molecules. A model is proposed which consists of a central stable collagen triple helix of 12-14 nm length from which three 9-22 nm long polyproline II type helices emerge at both ends. Disulfide linkage between cysteine- rich segments in these helices could lead to the formation of oligomeric network structures. Electrophoretic characterization of nematocyst extracts allows resolution of small proline-rich polypeptides that correspond in size to the cloned sequences.

Full Text

The Full Text of this article is available as a PDF (1.3 MB).

Selected References

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

  1. Blanquet R., Lenhoff H. M. A disulfide-linked collagenous protein of nematocyst capsules. Science. 1966 Oct 7;154(3745):152–153. doi: 10.1126/science.154.3745.152. [DOI] [PubMed] [Google Scholar]
  2. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  3. D'Alessio M., Ramirez F., Suzuki H. R., Solursh M., Gambino R. Structure and developmental expression of a sea urchin fibrillar collagen gene. Proc Natl Acad Sci U S A. 1989 Dec;86(23):9303–9307. doi: 10.1073/pnas.86.23.9303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dowling L. M., Crewther W. G., Parry D. A. Secondary structure of component 8c-1 of alpha-keratin. An analysis of the amino acid sequence. Biochem J. 1986 Jun 15;236(3):705–712. doi: 10.1042/bj2360705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Engel J., Chen H. T., Prockop D. J., Klump H. The triple helix in equilibrium with coil conversion of collagen-like polytripeptides in aqueous and nonaqueous solvents. Comparison of the thermodynamic parameters and the binding of water to (L-Pro-L-Pro-Gly)n and (L-Pro-L-Hyp-Gly)n. Biopolymers. 1977 Mar;16(3):601–622. doi: 10.1002/bip.1977.360160310. [DOI] [PubMed] [Google Scholar]
  6. Ertl H., Mengele R., Wenzl S., Engel J., Sumper M. The extracellular matrix of Volvox carteri: molecular structure of the cellular compartment. J Cell Biol. 1989 Dec;109(6 Pt 2):3493–3501. doi: 10.1083/jcb.109.6.3493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Exposito J. Y., Garrone R. Characterization of a fibrillar collagen gene in sponges reveals the early evolutionary appearance of two collagen gene families. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6669–6673. doi: 10.1073/pnas.87.17.6669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Exposito J. Y., Ouazana R., Garrone R. Cloning and sequencing of a Porifera partial cDNA coding for a short-chain collagen. Eur J Biochem. 1990 Jun 20;190(2):401–406. doi: 10.1111/j.1432-1033.1990.tb15589.x. [DOI] [PubMed] [Google Scholar]
  9. Gierer A., Berking S., Bode H., David C. N., Flick K., Hansmann G., Schaller H., Trenkner E. Regeneration of hydra from reaggregated cells. Nat New Biol. 1972 Sep 27;239(91):98–101. doi: 10.1038/newbio239098a0. [DOI] [PubMed] [Google Scholar]
  10. Hausmann K. Extrusive organelles in protists. Int Rev Cytol. 1978;52:197–276. doi: 10.1016/s0074-7696(08)60757-3. [DOI] [PubMed] [Google Scholar]
  11. Holstein T., Tardent P. An ultrahigh-speed analysis of exocytosis: nematocyst discharge. Science. 1984 Feb 24;223(4638):830–833. doi: 10.1126/science.6695186. [DOI] [PubMed] [Google Scholar]
  12. Holstein T. The morphogenesis of nematocytes in Hydra and Forskålia: an ultrastructural study. J Ultrastruct Res. 1981 Jun;75(3):276–290. doi: 10.1016/s0022-5320(81)80085-8. [DOI] [PubMed] [Google Scholar]
  13. Johnson P. M., Michaelsen T. E., Scopes P. M. Conformation of the hinge region and various fragments of human IgG3. Scand J Immunol. 1975;4(2):113–119. doi: 10.1111/j.1365-3083.1975.tb02607.x. [DOI] [PubMed] [Google Scholar]
  14. Kramer J. M., Cox G. N., Hirsh D. Comparisons of the complete sequences of two collagen genes from Caenorhabditis elegans. Cell. 1982 Sep;30(2):599–606. doi: 10.1016/0092-8674(82)90256-2. [DOI] [PubMed] [Google Scholar]
  15. Kramer J. M., Johnson J. J., Edgar R. S., Basch C., Roberts S. The sqt-1 gene of C. elegans encodes a collagen critical for organismal morphogenesis. Cell. 1988 Nov 18;55(4):555–565. doi: 10.1016/0092-8674(88)90214-0. [DOI] [PubMed] [Google Scholar]
  16. LENHOFF H. M., KLINE E. S., HURLEY R. A hydroxyproline-rich intracellular, collagen-like protein of Hydra nematocysts. Biochim Biophys Acta. 1957 Oct;26(1):204–205. doi: 10.1016/0006-3002(57)90074-4. [DOI] [PubMed] [Google Scholar]
  17. Marquart M., Deisenhofer J., Huber R., Palm W. Crystallographic refinement and atomic models of the intact immunoglobulin molecule Kol and its antigen-binding fragment at 3.0 A and 1.0 A resolution. J Mol Biol. 1980 Aug 25;141(4):369–391. doi: 10.1016/0022-2836(80)90252-1. [DOI] [PubMed] [Google Scholar]
  18. Martin G. R., Timpl R., Kühn K. Basement membrane proteins: molecular structure and function. Adv Protein Chem. 1988;39:1–50. doi: 10.1016/s0065-3233(08)60374-5. [DOI] [PubMed] [Google Scholar]
  19. Nordwig A., Nowack H., Hieber-Rogall E. Sea anemone collagen: further evidence for the existence of only one alpha-chain type. J Mol Evol. 1973;2(2-3):175–180. doi: 10.1007/BF01653997. [DOI] [PubMed] [Google Scholar]
  20. SLAUTTERBACK D. B., FAWCETT D. W. The development of the cnidoblasts of Hydra; an electron microscope study of cell differentiation. J Biophys Biochem Cytol. 1959 May 25;5(3):441–452. doi: 10.1083/jcb.5.3.441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Singh L., Jones K. W. The use of heparin as a simple cost-effective means of controlling background in nucleic acid hybridization procedures. Nucleic Acids Res. 1984 Jul 25;12(14):5627–5638. doi: 10.1093/nar/12.14.5627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Skaer R. J. The secretion and development of nematocysts in a siphonophore. J Cell Sci. 1973 Sep;13(2):371–393. doi: 10.1242/jcs.13.2.371. [DOI] [PubMed] [Google Scholar]
  24. St John T. P., Davis R. W. Isolation of galactose-inducible DNA sequences from Saccharomyces cerevisiae by differential plaque filter hybridization. Cell. 1979 Feb;16(2):443–452. doi: 10.1016/0092-8674(79)90020-5. [DOI] [PubMed] [Google Scholar]
  25. Tardent P., Holstein T. Morphology and morphodynamics of the stenotele nematocyst of Hydra attenuata Pall. (Hydrozoa, Cnidaria). Cell Tissue Res. 1982;224(2):269–290. doi: 10.1007/BF00216873. [DOI] [PubMed] [Google Scholar]
  26. Tautz D., Pfeifle C. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma. 1989 Aug;98(2):81–85. doi: 10.1007/BF00291041. [DOI] [PubMed] [Google Scholar]
  27. von Heijne G. Patterns of amino acids near signal-sequence cleavage sites. Eur J Biochem. 1983 Jun 1;133(1):17–21. doi: 10.1111/j.1432-1033.1983.tb07424.x. [DOI] [PubMed] [Google Scholar]

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

RESOURCES