Abstract
Nematocysts are the taxon-defining features of all cnidarians including jellyfish, sea anemones, and corals. They are highly sophisticated organelles used for the capture of prey and defense. The nematocyst capsule is produced within a giant post-Golgi vesicle, which is continuously fed by proteins from the secretory pathway. Mature nematocysts consist of a hollow capsule body in which a long tubule is coiled up that, upon discharge, is expelled in a harpoon-like fashion. This is accompanied by the release of a toxin cocktail stored in the capsule matrix. Nematocyst discharge, which is one of the fastest processes in biology, is driven by an extreme osmotic pressure of about 150 bar. The molecular analysis of the nematocyst has from the beginning indicated a collagenous nature of the capsule structure. In particular, a large family of unusual minicollagens has been demonstrated to form the highly resistant scaffold of the capsule. Recent findings on the molecular composition of Hydra nematocysts have confirmed the notion of a specialized extracellular matrix, which is assembled during an intracellular secretion process to form the most complex predatory apparatus at the cellular level.
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Abbreviations
- ECM:
-
extracellular matrix
- TGN:
-
trans-Golgi network
- PG:
-
proteoglycan
- GAG:
-
glycosaminoglycan
- PNN:
-
perineuronal net
- CRD:
-
cysteine-rich domain
- NOWA:
-
nematocyst outer wall antigen
- SCP:
-
sperm coating protein
- CTLD:
-
C-type lectin domain
References
Adamczyk P, Meier S, Gross T, Hobmayer B, Grzesiek S, Bachinger HP, Holstein TW, Özbek S (2008) Minicollagen-15, a novel minicollagen isolated from Hydra, forms tubule structures in nematocysts. J Mol Biol 376(4):1008–1020
Adamczyk P, Zenkert C, Balasubramanian PG, Yamada S, Murakoshi S, Sugahara K, Hwang JS, Gojobori T, Holstein TW, Özbek S (2010) A non-sulfated chondroitin stabilizes membrane tubulation in cnidarian organelles. J Biol Chem 285(33):25613–25623
Chapman GB, Tilney LG (1959a) Cytological studies of the nematocysts of Hydra. I. Desmonemes, isorhizas, cnidocils, and supporting structures. J Biophys Biochem Cytol 5(1):69–78
Chapman GB, Tilney LG (1959b) Cytological studies of the nematocysts of Hydra. II. The stenoteles. J Biophys Biochem Cytol 5(1):79–84
Dam TK, Brewer CF (2010) Multivalent lectin-carbohydrate interactions energetics and mechanisms of binding. Adv Carbohydr Chem Biochem 63:139–164
David CN, Özbek S, Adamczyk P, Meier S, Pauly B, Chapman J, Hwang JS, Gojobori T, Holstein TW (2008) Evolution of complex structures: minicollagens shape the cnidarian nematocyst. Trends Genet 24(9):431–438
Engel J (1997) Versatile collagens in invertebrates. Science 277(5333):1785–1786
Engel U, Pertz O, Fauser C, Engel J, David CN, Holstein TW (2001) A switch in disulfide linkage during minicollagen assembly in Hydra nematocysts. Embo J 20(12):3063–3073
Engel U, Özbek S, Engel R, Petri B, Lottspeich F, Holstein TW (2002) NOWA, a novel protein with minicollagen Cys-rich domains involved in nematocyst formation in Hydra. J Cell Sci 115(20):3923–3934
Exposito JY, Cluzel C, Garrone R, Lethias C (2002) Evolution of collagens. Anat Rec 268(3):302–316
Fawcett DW, Ito S, Slautterback D (1959) The occurrence of intercellular bridges in groups of cells exhibiting synchronous differentiation. J Biophys Biochem Cytol 5(3):453–460
Holland JW, Okamura B, Hartikainen H, Secombes CJ (2010) A novel minicollagen gene links cnidarians and myxozoans. Proc Biol Sci. doi:rspb.2010.1301
Holstein TW, Benoit GM, Gv H, Wanner G, David CN, Gaub HE (1994) Fibrous mini-collagens in Hydra nematocysts. Science 265:402–404
Hwang HY, Horvitz HR (2002) The Caenorhabditis elegans vulval morphogenesis gene sqv-4 encodes a UDP-glucose dehydrogenase that is temporally and spatially regulated. Proc Natl Acad Sci USA 99(22):14224–14229
Jackson RL, Busch SJ, Cardin AD (1991) Glycosaminoglycans: molecular properties, protein interactions, and role in physiological processes. Physiol Rev 71(2):481–539
Karamanos NK, Aletras AJ, Antonopoulos CA, Tsegenidis T, Tsiganos CP, Vynios DH (1988) Extraction and fractionation of proteoglycans from squid skin. Biochim Biophys Acta 966(1):36–43
King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chapman J, Fairclough S, Hellsten U, Isogai Y, Letunic I, Marr M, Pincus D, Putnam N, Rokas A, Wright KJ, Zuzow R, Dirks W, Good M, Goodstein D, Lemons D, Li W, Lyons JB, Morris A, Nichols S, Richter DJ, Salamov A, Sequencing JG, Bork P, Lim WA, Manning G, Miller WT, McGinnis W, Shapiro H, Tjian R, Grigoriev IV, Rokhsar D (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451(7180):783–788
Kurz EM, Holstein TW, Petri BM, Engel J, David CN (1991) Mini-collagens in Hydra nematocytes. J Cell Biol 115(4):1159–1169
Lenhoff HM, Kline ES, Hurley R (1957) A hydroxyproline-rich, intracellular, collagenlike protein of Hydra nematocysts. Biochim Biophys Acta 26:204–205
Mariscal RN (1974) Experimental marine biology. Academic, New York
Meier S, Jensen PR, Adamczyk P, Bachinger HP, Holstein TW, Engel J, Özbek S, Grzesiek S (2007a) Sequence-structure and structure-function analysis in cysteine-rich domains forming the ultrastable nematocyst wall. J Mol Biol 368(3):718–728
Meier S, Jensen PR, David CN, Chapman J, Holstein TW, Grzesiek S, Özbek S (2007b) Continuous molecular evolution of protein-domain structures by single amino acid changes. Curr Biol 17(2):173–178
Nakagawa H, Hama Y, Sumi T, Li SC, Maskos K, Kalayanamitra K, Mizumoto S, Sugahara K, Li YT (2007) Occurrence of a nonsulfated chondroitin proteoglycan in the dried saliva of Collocalia swiftlets (edible bird's-nest). Glycobiology 17(2):157–164
Nuchter T, Benoit M, Engel U, Ozbek S, Holstein TW (2006) Nanosecond-scale kinetics of nematocyst discharge. Curr Biol 16(9):R316–R318
Özbek S, Engel U, Engel J (2002a) A switch in disulfide linkage during minicollagen assembly in Hydra nematocysts or how to assemble a 150-bar-resistant structure. J Struct Biol 137(1–2):11–14
Özbek S, Pertz O, Schwager M, Lustig A, Holstein T, Engel J (2002b) Structure/function relationships in the minicollagen of Hydra nematocysts. J Biol Chem 277(51):49200–49204
Özbek S, Pokidysheva E, Schwager M, Schulthess T, Tariq N, Barth D, Milbradt AG, Moroder L, Engel J, Holstein TW (2004) The glycoprotein NOWA and minicollagens are part of a disulfide-linked polymer that forms the cnidarian nematocyst wall. J Biol Chem 279(50):52016–52023
Pokidysheva E, Milbradt AG, Meier S, Renner C, Haussinger D, Bachinger HP, Moroder L, Grzesiek S, Holstein TW, Özbek S, Engel J (2004) The structure of the Cys-rich terminal domain of Hydra minicollagen, which is involved in disulfide networks of the nematocyst wall. J Biol Chem 279(29):30395–30401
Rodriguez ML, Jann B, Jann K (1988) Structure and serological characteristics of the capsular K4 antigen of Escherichia coli O5:K4:H4, a fructose-containing polysaccharide with a chondroitin backbone. Eur J Biochem 177(1):117–124
Sato S, St-Pierre C, Bhaumik P, Nieminen J (2009) Galectins in innate immunity: dual functions of host soluble beta-galactoside-binding lectins as damage-associated molecular patterns (DAMPs) and as receptors for pathogen-associated molecular patterns (PAMPs). Immunol Rev 230(1):172–187
Sugahara K, Mikami T, Uyama T, Mizuguchi S, Nomura K, Kitagawa H (2003) Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate. Curr Opin Struct Biol 13(5):612–620
Trembley A (1744) Mémoires pour servir à l’histoire d’un genre de polypes d’eau douce à bras en forme de cornes. Jean and Hermann Verbeek, Leiden
Watson AA, Eble JA, O’Callaghan CA (2008) Crystal structure of rhodocytin, a ligand for the platelet-activating receptor CLEC-2. Protein Sci 17(9):1611–1616
Weber J (1990) Poly(gamma-glutamic acid)s are the major constituents of nematocysts in Hydra (Hydrozoa, Cnidaria). J Biol Chem 265(17):9664–9669
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(8):886–894
Yamada S, Sakamoto K, Tsuda H, Yoshida K, Sugiura M, Sugahara K (1999) Structural studies of octasaccharides derived from the low-sulfated repeating disaccharide region and octasaccharide serines derived from the protein linkage region of porcine intestinal heparin. Biochemistry 38(2):838–847
Zimmermann DR, Dours-Zimmermann MT (2008) Extracellular matrix of the central nervous system: from neglect to challenge. Histochem Cell Biol 130(4):635–653
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Özbek, S. The cnidarian nematocyst: a miniature extracellular matrix within a secretory vesicle. Protoplasma 248, 635–640 (2011). https://doi.org/10.1007/s00709-010-0219-4
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DOI: https://doi.org/10.1007/s00709-010-0219-4