Induction of (2′−5′)oligoadenylate synthetase in the marine sponges <i>Suberites domuncula</i> and <i>Geodia cydonium</i> by the bacterial endotoxin lipopolysaccharide

Grebenjuk, Vladislav A.; Kuusksalu, Anne; Kelve, Merike; Schütze, Joachim; Schröder, Heinz C.; Müller, Wernér E.G.

doi:10.1046/j.1432-1033.2002.02781.x

Cited by 55 publications

(35 citation statements)

References 51 publications

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“…dsRNA for the duck (7 g) was included in the experiment on panel b for comparison. The chi-square statistic was used to assess the significance of the observed antiviral protection relative to positive controls: (a) poly CG ( (17,28), and the possibility that these genes exist in crustaceans and play a role in antiviral immunity cannot be excluded. On the other hand, signal transduction pathways homologous to those known to regulate the vertebrate IFN response do exist in arthropods.…”

Section: Discussionmentioning

confidence: 99%

Induction of Antiviral Immunity by Double-Stranded RNA in a Marine Invertebrate

Robalino¹,

Browdy

Prior

et al. 2004

J Virol

263

168

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Vertebrates mount a strong innate immune response against viruses, largely by activating the interferon system. Double-stranded RNA (dsRNA), a common intermediate formed during the life cycle of many viruses, is a potent trigger of this response. In contrast, no general inducible antiviral defense mechanism has been reported in any invertebrate. Here we show that dsRNA induces antiviral protection in the marine crustacean Litopenaeus vannamei. When treated with dsRNA, shrimp showed increased resistance to infection by two unrelated viruses, white spot syndrome virus and Taura syndrome virus. Induction of this antiviral state is independent of the sequence of the dsRNA used and therefore distinct from the sequence-specific dsRNAmediated genetic interference phenomenon. This demonstrates for the first time that an invertebrate immune system, like its vertebrate counterparts, can recognize dsRNA as a virus-associated molecular pattern, resulting in the activation of an innate antiviral response.

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Section: Discussionmentioning

confidence: 99%

Induction of Antiviral Immunity by Double-Stranded RNA in a Marine Invertebrate

Robalino¹,

Browdy

Prior

et al. 2004

J Virol

263

168

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“…and from tissue around parts in which these organisms had been identified. RNA was extracted from liquid-nitrogen-pulverized tissue with TRIzol reagent as previously described (19). Then 5 g of total RNA was electrophoresed and blotted onto Hybond-N ϩ nylon membrane.…”

Section: Methodsmentioning

confidence: 99%

Okadaic Acid, an Apoptogenic Toxin for Symbiotic/Parasitic Annelids in the Demosponge Suberites domuncula

Schröder

Breter

Fattorusso

et al. 2006

Appl Environ Microbiol

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The role of okadaic acid (OA) in the defense system of the marine demosponge Suberites domuncula against symbiotic/parasitic annelids was examined. Bacteria within the mesohyl produced okadaic acid at concentrations between 32 ng/g and 58 ng/g of tissue (wet weight). By immunocytochemical methods and by use of antibodies against OA, we showed that the toxin was intracellularly stored in vesicles. Western blotting experiments demonstrated that OA also existed bound to a protein with a molecular weight of 35,000 which was tentatively identified as a galectin (by application of antigalectin antibodies). Annelids that are found in S. domuncula undergo apoptotic cell death. OA is one candidate inducer molecule of this process, since this toxin accumulated in these symbionts/parasites. Furthermore, we identified the cDNA encoding the multifunctional prosurvival molecule BAG-1 in S. domuncula; it undergoes strong expression in the presence of the annelid. Our data suggest that sponges use toxins (here, OA) produced from bacteria to eliminate metazoan symbionts/ parasites by apoptosis.Sponges, the evolutionarily oldest metazoan phylum (Porifera), share one common ancestor with the other metazoan phylum, the Urmetazoa (31, 35). Most sponges are marine sessile filter feeders; some species daily filter tons of water containing millions of bacteria or viruses through their bodies (48; reviewed in references 18 and 26). Due to their efficient chemical and biological defense systems, sponges have survived not only adverse climatic periods (24) but also biotic and anthropogenic threats (34).Two strategies are used by sponges to eliminate attacking (infectious) bacteria: first, chemical strategies via the production of secondary metabolites (see references 45 and 51) and, second, humoral and cellular defense mechanisms (33). The hitherto studied molecular biological or cell biological defense systems used by sponges against microorganisms have been elucidated primarily in the demosponge Suberites domuncula. This species is able to recognize and defeat gram-positive as well as gram-negative bacteria by the antimicrobial lectin tachylectin (52). In addition, S. domuncula has developed a specific system to recognize gram-positive bacteria via the peptidoglycan coat; subsequently bacteria are endocytosed and/or extracellularly digested by lysozyme (59). The lipopolysaccharide (LPS) outer membrane of gram-negative bacteria induces in S. domuncula an adaptive antibacterial response by increasing the release of bioactive and antimicrobial lyso-plateletactivating factors (36). We have shown that in the aqueous environment also, fungi are recognized by sponges via a receptor, the (133)-␤-D-glucan binding protein; after interaction of fungal (133)-␤-D-glucans with the corresponding receptor, S. domuncula causes the expression of a series of defense molecules, e.g., a fibrinogen-like protein and an epidermal growth factor precursor (43).Finally, the more general defense system against microorganisms should be highlighted; LPS activates th...

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“…The cells that were used for the preparation of the primmorphs came from animals that had been kept in an aquarium for 5 months. From such animals, it is known that they are exposed to only a minute level of bacteria in the surrounding seawater (40). The assays, which were performed as described under ''Materials and Methods,'' remained either non-treated or were supplemented with 10 g/ml LPS.…”

Section: Gene Expression Of the Lectin In Different Specimens-tomentioning

confidence: 99%

Emergence and Disappearance of an Immune Molecule, an Antimicrobial Lectin, in Basal Metazoa

Schröder

Ushijima

Krasko

et al. 2003

Journal of Biological Chemistry

Self Cite

100

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Sponges (phylum Porifera) represent the evolutionarily oldest metazoans that comprise already a complex immune system and are related to the crown taxa of the protostomians and the deuterostomians. Here, we demonstrate the existence of a tachylectin-related protein in the demosponge Suberites domuncula, termed Suberites lectin. The MAPK pathway was activated in response to lipopolysaccharide treatment of the three-dimensional cell aggregates, the primmorphs; this process was abolished by the monosaccharide D-GlcNAc. The cDNA encoding the S. domuncula lectin was identified and cloned; it comprises 238 amino acids (26 kDa) in the open reading frame. The deduced protein has one potential transmembrane region, three characteristic Cys residues, and six internal tandem repeats; it shares the highest sequence similarity with lectins from the horseshoe crab Tachypleus trunculus. The steady-state level of expression of the Suberites lectin rises in primmorphs in response to lipopolysaccharide, an effect that was prevented by co-incubation with D-GlcNAc. The natural sponge lectin was purified by affinity chromatography; it has a size of 27 kDa and displays antibacterial activity against the Gram-negative bacteria Escherichia coli and the Gram-positive bacteria Staphylococcus aureus. The putative protein, deduced from the cloned gene, is identical/similar to the purified natural protein, as demonstrated by immunological cross-reactivity with specific antibodies. We conclude that the S. domuncula lectin acts as an antibacterial molecule involved in immune defense against bacterial invaders.

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Induction of (2′−5′)oligoadenylate synthetase in the marine sponges Suberites domuncula and Geodia cydonium by the bacterial endotoxin lipopolysaccharide

Cited by 55 publications

References 51 publications

Induction of Antiviral Immunity by Double-Stranded RNA in a Marine Invertebrate

Induction of Antiviral Immunity by Double-Stranded RNA in a Marine Invertebrate

Okadaic Acid, an Apoptogenic Toxin for Symbiotic/Parasitic Annelids in the Demosponge Suberites domuncula

Emergence and Disappearance of an Immune Molecule, an Antimicrobial Lectin, in Basal Metazoa

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