Proteome of Hydra nematocyst

Journal of Biological Chemistry

Volumn 287, Issue 13, 2012, Pages 9672-9681

  Balasubramanian, Prakash G ^a   Beckmann, Anna ^a   Warnken, Uwe ^b   Schnölzer, Martina ^b   Schüler, Andreas ^c   Bornberg Bauer, Erich ^c   Holstein, Thomas W ^a   Özbek, Suat ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EVOLUTION; BIOMECHANICAL PROPERTIES; CELL TYPES; EXTRACELLULAR MATRICES; GOLGI APPARATUS; MOLECULAR COMPONENTS; NEMATOCYTES; SECRETOME; SECRETORY VESICLES; STINGING CELLS;

BIOCHEMISTRY; BIOLOGY;

BIOMECHANICS;

PROTEOME; STRUCTURAL PROTEIN;

ARTICLE; CONTROLLED STUDY; ELASTICITY; EXOCYTOSIS; EXTRACELLULAR MATRIX; GENETIC CONSERVATION; HYDRA; MOLECULAR WEIGHT; NEMATOCYST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; SEQUENCE HOMOLOGY; STRUCTURAL PROTEOMICS;

ANIMALS; EVOLUTION, MOLECULAR; EXOCYTOSIS; EXTRACELLULAR MATRIX PROTEINS; HYDRA; NEMATOCYST; PROTEOME; SECRETORY VESICLES;

ANIMALIA; CNIDARIA; HYDRA; HYDRA MAGNIPAPILLATA; SCYPHOZOA;

EID: 84857799527     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.328203     Document Type: Article

References (49)

1. Nüchter, T., Benoit, M., Engel, U., Ozbek, S., and Holstein, T. W. (2006) Nanosecond-scale kinetics of nematocyst discharge. Curr. Biol. 16, R316-R318
2. Fry, B. G., Wroe, S., Teeuwisse, W., van Osch, M. J., Moreno, K., Ingle, J., McHenry, C., Ferrara, T., Clausen, P., Scheib, H., Winter, K. L., Greisman, L., Roelants, K., van der Weerd, L., Clemente, C. J., Giannakis, E., Hodgson, W. C., Luz, S., Martelli, P., Krishnasamy, K., Kochva, E., Kwok, H. F., Scanlon, D., Karas, J., Citron, D. M., Goldstein, E. J., McNaughtan, J. E., and Norman, J. A. (2009) A central role for venom in predation by Varanus komodoensis (Komodo dragon) and the extinct giant Varanus (Megalania) priscus. Proc. Natl. Acad. Sci. U.S.A. 106, 8969-8974
3. Fry, B. G., Roelants, K., Champagne, D. E., Scheib, H., Tyndall, J. D., King, G. F., Nevalainen, T. J., Norman, J. A., Lewis, R. J., Norton, R. S., Renjifo, C., and de la Vega, R. C. (2009) The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu. Rev. Genomics Hum. Genet. 10, 483-511
4. Eble, J. A. (2010) Matrix biology meets toxinology. Matrix Biol. 29, 239-247
5. Mariscal, R. N. (1974) Scanning electron microscopy of the sensory surface of the tentacles of sea anemones and corals. Z. Zellforsch. 147, 149-156
6. Ozbek, S., Balasubramanian, P. G., and Holstein, T. W. (2009) Cnidocyst structure and the biomechanics of discharge. Toxicon 54, 1038-1045
7. David, C. N., Ozbek, S., Adamczyk, P., Meier, S., Pauly, B., Chapman, J., Hwang, J. S., Gojobori, T., and Holstein, T. W. (2008) Evolution of complex structures: minicollagens shape the cnidarian nematocyst. Trends Genet. 24, 431-438
8. Chapman, G. B., and Tilney, L. G. (1959) Cytological studies of the nematocysts of Hydra. I. Desmonemes, isorhizas, cnidocils, and supporting structures. J. Biophys. Biochem. Cytol. 5, 69-78
9. Chapman, G. B., and Tilney, L. G. (1959) Cytological studies of the nematocysts of Hydra. II. The stenoteles. J. Biophys. Biochem. Cytol. 5, 79-84
10. Holstein, T. W., Campbell, R. D., and Tardent, P. (1990) Identity crisis. Nature 346, 21-22 (Pubitemid 20213932)
11. Lenhoff, H. M., Kline, E. S., and Hurley, R. (1957) A hydroxyproline-rich intracellular, collagen-like protein of Hydra nematocysts. Biochim. Biophys. Acta 26, 204-205
12. Weber, J. (1990) Poly(γ-glutamic acids) are the major constituents of nematocysts in Hydra (Hydrozoa, Cnidaria). J. Biol. Chem. 265, 9664-9669
13. Kurz, E. M., Holstein, T. W., Petri, B. M., Engel, J., and David, C. N. (1991) Minicollagens in Hydra nematocytes. J. Cell Biol. 115, 1159-1169
14. Holstein, T. W., Benoit, M., Herder, G. V., David, C. N., Wanner, G., and Gaub, H. E. (1994) Fibrous minicollagens in Hydra nematocysts. Science 265, 402-404
15. Holstein, T., and Tardent, P. (1984) An ultrahigh-speed analysis of exocytosis: nematocyst discharge. Science 223, 830-833
16. Engel, U., Ozbek, S., Streitwolf-Engel, R., Petri, B., Lottspeich, F., and Holstein, T. W. (2002) NOWA, a novel protein with minicollagen Cys-rich domains, is involved in nematocyst formation in Hydra. J. Cell Sci. 115, 3923-3934 (Pubitemid 35256493)
17. Koch, A. W., Holstein, T. W., Mala, C., Kurz, E., Engel, J., and David, C. N. (1998) Spinalin, a new glycine- and histidine-rich protein in spines of Hydra nematocysts. J. Cell Sci. 111, 1545-1554 (Pubitemid 28288826)
18. Weber, J. (1989) Nematocysts (stinging capsules of Cnidaria) as Donnan potential-dominated osmotic systems. Eur. J. Biochem. 184, 465-476
19. Schokraie, E., Hotz-Wagenblatt, A., Warnken, U., Mali, B., Frohme, M., Förster, F., Dandekar, T., Hengherr, S., Schill, R. O., and Schnölzer, M. (2010) Proteomic analysis of tardigrades: towards a better understanding of molecular mechanisms by anhydrobiotic organisms. PLoS ONE 5, e9502
20. Chapman, J. A., Kirkness, E. F., Simakov, O., Hampson, S. E., Mitros, T., Weinmaier, T., Rattei, T., Balasubramanian, P. G., Borman, J., Busam, D., Disbennett, K., Pfannkoch, C., Sumin, N., Sutton, G. G., Viswanathan, L. D., Walenz, B., Goodstein, D. M., Hellsten, U., Kawashima, T., Prochnik, S. E., Putnam, N. H., Shu, S., Blumberg, B., Dana, C. E., Gee, L., Kibler, D. F., Law, L., Lindgens, D., Martinez, D. E., Peng, J., Wigge, P. A., Bertulat, B., Guder, C., Nakamura, Y., Ozbek, S., Watanabe, H., Khalturin, K., Hemmrich, G., Franke, A., Augustin, R., Fraune, S., Hayakawa, E., Hayakawa, S., Hirose, M., Hwang, J. S., Ikeo, K., Nishimiya-Fujisawa, C., Ogura, A., Takahashi, T., Steinmetz, P. R., Zhang, X., Aufschnaiter, R., Eder, M. K., Gorny, A. K., Salvenmoser, W., Heimberg, A. M., Wheeler, B. M., Peterson, K. J., Bottger, A., Tischler, P., Wolf, A., Gojobori, T., Remington, K. A., Strausberg, R. L., Venter, J. C., Technau, U., Hobmayer, B., Bosch, T. C., Holstein, T. W., Fujisawa, T., Bode, H. R., David, C. N., Rokhsar, D. S., and Steele, R. E. (2010) The dynamic genome of Hydra. Nature 464, 592-596
21. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402 (Pubitemid 27359211)
22. Hunter, S., Apweiler, R., Attwood, T. K., Bairoch, A., Bateman, A., Binns, D., Bork, P., Das, U., Daugherty, L., Duquenne, L., Finn, R. D., Gough, J., Haft, D., Hulo, N., Kahn, D., Kelly, E., Laugraud, A., Letunic, I., Lonsdale, D., Lopez, R., Madera, M., Maslen, J., McAnulla, C., McDowall, J., Mistry, J., Mitchell, A., Mulder, N., Natale, D., Orengo, C., Quinn, A. F., Selengut, J. D., Sigrist, C. J., Thimma, M., Thomas, P. D., Valentin, F., Wilson, D., Wu, C. H., and Yeats, C. (2009) InterPro: the integrative protein signature database. Nucleic Acids Res. 37, D211-D215
23. Jungo, F., and Bairoch, A. (2005) Tox-Prot, the toxin protein annotation program of the Swiss-Prot protein knowledge base. Toxicon 45, 293-301 (Pubitemid 40431273)
24. Poirot, O., O'Toole, E., and Notredame, C. (2003) Tcoffee@igs: a web server for computing, evaluating, and combining multiple sequence alignments. Nucleic Acids Res. 31, 3503-3506 (Pubitemid 37442186)
25. Roy, A., Kucukural, A., and Zhang, Y. (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5, 725-738
26. Linding, R., Russell, R. B., Neduva, V., and Gibson, T. J. (2003) GlobPlot: Exploring protein sequences for globularity and disorder. Nucleic Acids Res. 31, 3701-3708 (Pubitemid 37442227)
27. Yaross, M. S., and Bode, H. R. (1978) Regulation of interstitial cell differentiation in Hydra attenuata. III. Effects of I-cell and nerve cell densities. J. Cell Sci. 34, 1-26 (Pubitemid 9076417)
28. Hwang, J. S., Ohyanagi, H., Hayakawa, S., Osato, N., Nishimiya-Fujisawa, C., Ikeo, K., David, C. N., Fujisawa, T., and Gojobori, T. (2007) The evolutionary emergence of cell type-specific genes inferred from the gene expression analysis of Hydra. Proc. Natl. Acad. Sci. U.S.A. 104, 14735-14740 (Pubitemid 350003212)
29. Szczepanek, S., Cikala, M., and David, C. N. (2002) Poly-γ- glutamate synthesis during formation of nematocyst capsules in Hydra. J. Cell Sci. 115, 745-751 (Pubitemid 34196334)
30. Denker, E., Bapteste, E., Le Guyader, H., Manuel, M., and Rabet, N. (2008) Horizontal gene transfer and the evolution of cnidarian stinging cells. Curr. Biol. 18, R858-R859
31. Sher, D., and Zlotkin, E. (2009) A Hydra with many heads: protein and polypeptide toxins from Hydra and their biological roles. Toxicon 54, 1148-1161
32. Bosmans, F., and Tytgat, J. (2007) Sea anemone venom as a source of insecticidal peptides acting on voltage-gated Na+ channels. Toxicon 49, 550-560 (Pubitemid 46343847)
33. Gutiérrez, J. M., Rucavado, A., Escalante, T., and Díaz, C. (2005) Hemorrhage induced by snake venom metalloproteinases: biochemical and biophysical mechanisms involved in microvessel damage. Toxicon 45, 997-1011
34. Henriksen, A., King, T. P., Mirza, O., Monsalve, R. I., Meno, K., Ipsen, H., Larsen, J. N., Gajhede, M., and Spangfort, M. D. (2001) Major venom allergen of yellow jackets, Ves v 5: structural characterization of a pathogenesis- related protein superfamily. Proteins 45, 438-448 (Pubitemid 33108078)
35. Ozbek, S., Pokidysheva, E., Schwager, M., Schulthess, T., Tariq, N., Barth, D., Milbradt, A. G., Moroder, L., Engel, J., and Holstein, T. W. (2004) The glycoprotein NOWA and minicollagens are part of a disulfide-linked polymer that forms the cnidarian nematocyst wall. J. Biol. Chem. 279, 52016-52023 (Pubitemid 39656572)
36. Hinman, M. B., and Lewis, R. V. (1992) Isolation of a clone encoding a second dragline silk fibroin. Nephila clavipes dragline silk is a two-protein fiber. J. Biol. Chem. 267, 19320-19324
37. Vollrath, F. (2005) Spiders' webs. Curr. Biol. 15, R364-R365
38. Gosline, J., Lillie, M., Carrington, E., Guerette, P., Ortlepp, C., and Savage, K. (2002) Elastic proteins: biological roles and mechanical properties. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357, 121-132 (Pubitemid 34276203)
39. Holland, J. W., Okamura, B., Hartikainen, H., and Secombes, C. J. (2011) A novel minicollagen gene links cnidarians and myxozoans. Proc. R. Soc. B 278, 546-553
40. Cavalier-Smith, T. (2009) Predation and eukaryote cell origins: a co-evolutionary perspective. Int. J. Biochem. Cell Biol. 41, 307-322
41. Koonin, E. V. (2007) The Biological Big Bang model for the major transitions in evolution. Biol. Direct 2, 21
42. Hausmann, K. (1978) Extrusive organelles in protists. Int. Rev. Cytol. 52, 197-276
43. Westfall, J. A., Bradbury, P. C., and Townsend, J. W. (1983) Ultrastructure of the dinoflagellate Polykrikos. I. Development of the nematocyst-taeniocyst complex and morphology of the site for extrusion. J. Cell Sci. 63, 245-261
44. Meier, S., Jensen, P. R., Adamczyk, P., Bächinger, H. P., Holstein, T. W., Engel, J., Ozbek, S., and Grzesiek, S. (2007) Sequence-structure and structure- function analysis in cysteine-rich domains forming the ultrastable nematocyst wall. J. Mol. Biol. 368, 718-728 (Pubitemid 46527611)
45. Cassab, G. I. (1998) Plant cell wall proteins. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 281-309
46. Oppenheim, F. G., Salih, E., Siqueira, W. L., Zhang, W., and Helmerhorst, E. J. (2007) Salivary proteome and its genetic polymorphisms. Ann. N.Y. Acad. Sci. 1098, 22-50 (Pubitemid 47092551)
47. Wong, R. S., Hofmann, T., and Bennick, A. (1979) The complete primary structure of a proline-rich phosphoprotein from human saliva. J. Biol. Chem. 254, 4800-4808 (Pubitemid 9204189)
48. Clements, S., Mehansho, H., and Carlson, D. M. (1985) Novel multigene families encoding highly repetitive peptide sequences. Sequence analyses of rat and mouse proline-rich protein cDNAs. J. Biol. Chem. 260, 13471-13477 (Pubitemid 16192293)
49. Andersen, J. F., Pham, V. M., Meng, Z., Champagne, D. E., and Ribeiro, J. M. (2009) Insight into the sialome of the black fly, Simulium vittatum. J. Proteome Res. 8, 1474-1488