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Effects of Agelas Oroides and Petrosia Ficiformis Crude Extracts on Human Neuroblastoma Cell Survival

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Effects of Agelas Oroides and Petrosia Ficiformis Crude Extracts on Human Neuroblastoma Cell Survival 161-169 6/12/06 19:46 Page 161 INTERNATIONAL JOURNAL OF ONCOLOGY 30: 161-169, 2007 161 Effects of Agelas oroides and Petrosia ficiformis crude extracts on human neuroblastoma cell survival CRISTINA FERRETTI1*, BARBARA MARENGO2*, CHIARA DE CIUCIS3, MARIAPAOLA NITTI3, MARIA ADELAIDE PRONZATO3, UMBERTO MARIA MARINARI3, ROBERTO PRONZATO1, RENATA MANCONI4 and CINZIA DOMENICOTTI3 1Department for the Study of Territory and its Resources, University of Genoa, Corso Europa 26, I-16132 Genoa; 2G. Gaslini Institute, Gaslini Hospital, Largo G. Gaslini 5, I-16148 Genoa; 3Department of Experimental Medicine, University of Genoa, Via Leon Battista Alberti 2, I-16132 Genoa; 4Department of Zoology and Evolutionistic Genetics, University of Sassari, Via Muroni 25, I-07100 Sassari, Italy Received July 28, 2006; Accepted September 20, 2006 Abstract. Among marine sessile organisms, sponges (Porifera) Introduction are the major producers of bioactive secondary metabolites that defend them against predators and competitors and are used to Sponges (Porifera) are a type of marine fauna that produce interfere with the pathogenesis of many human diseases. Some bioactive molecules to defend themselves from predators or of these biological active metabolites are able to influence cell spatial competitors (1,2). It has been demonstrated that some survival and death, modifying the activity of several enzymes of these metabolites have a biomedical potential (3) and in involved in these cellular processes. These natural compounds particular, Ara-A and Ara-C are clinically used as antineoplastic show a potential anticancer activity but the mechanism of drugs (4,5) in the routine treatment of patients with leukaemia this action is largely unknown. In this study, we investigated and lymphoma. the effects of two Mediterranean sponges, Agelas oroides and Moreover, in vitro studies have attributed to sponge Petrosia ficiformis on the viability of human neuroblastoma metabolites several biological activities such as antimicrobial, cells. Upon treatment with the methanolic extract of Petrosia antifungal, antiviral, neurotoxic and cytotoxic properties (6-11). ficiformis, a marked cytotoxic effect was observed at any Some of these bioactive compounds are able to influence cell concentration or time of exposure. In contrast, a time- and survival and death, modifying the activity of several enzymes dose-dependent effect was monitored for Agelas oroides that involved in these cellular processes. In fact, it has been found induced the development of apoptotic features and ROS that a polyketide quinone compound, isolated from the marine production in LAN5 cells. These events were suppressed by sponge Xestospongia carbonaria, inhibits protein tyrosine calpeptin or zVAD and by vitamin C suggesting that the cell kinase and is cytotoxic for several malignant cell lines (12). death caused by Agelas oroides was calpain- and caspase- Another enzyme inhibitor, okadaic acid, from the marine dependent and of oxidative nature. Comet assay showed that sponge Halichondria okadai, strongly inhibits a protein this methanolic extract was not able to produce a genotoxic phosphatase, inducing cytoskeletal disruption and is a long- effect. Future studies will be applied to investigate the effect known tumour-promoting compound (13,14). Moreover, of isolated bioactive compounds from crude extract of this many authors have attributed to some of these compounds a sponge which are potentially useful for cancer therapeutics. potential anticancer activity. In particular, Halichondrin B (15-17) has shown a marked in vitro and in vivo anticancer activity against murine melanoma and leukaemia (18) and _________________________________________ Dictyostatin-1, isolated from Spongia sp., is cytotoxic for adenocarcinoma and breast cancer cells (19). Laulimalide and Correspondence to: Dr Cinzia Domenicotti, Department of Discodermolide, isolated from Cacospongia mycofijiensis and Experimental Medicine, University of Genoa, Via Leon Battista Discodermia dissoluta, respectively (20,21) have demonstrated Alberti 2, I-16132 Genoa, Italy tubulin hyperstabilizing properties (22) similar to that of E-mail: [email protected] paclitaxel used to cure breast, lung and ovarian cancers (23,24). The Mediterranean sponge Agelas oroides (Schmidt, *Contributed equally 1864; Agelasida, Agelasidae) contains pyrrole imidazole alkaloids such as oroidin, cyclooroidin and taurodispacamide A Key words: Agelas oroides, Petrosia ficiformis, sponge extracts, (25) with a good antihistaminic activity and the brominated human neuroblastoma, apoptosis, reactive oxygen species, protein compounds agelorin A and B with an antibiotic activity against kinase C Bacillus subtilis and Micrococcus luteus (26). Petrosia ficiformis (Poiret, 1789; Haplosclerida, Petrosiidae), another Mediterranean sponge, is known to 161-169 6/12/06 19:46 Page 162 162 FERRETTI et al: Agelas oroides INDUCES APOPTOSIS OF NEUROBLASTOMA CELLS contain a number of highly toxic and anti-HIV active poly- P. ficiformis methanolic crude extracts. Some samples of acetylenes such as the petrosyformynes and petrosynol (27), LAN5 cells were pre-treated for 30 min with 250 μM and its cytotoxicity has been demonstrated on human red vitamin C, 10 μM calpeptin, 20 μM z-VAD-fmk. blood cells (10). The aim of the present work is to analyse the effect of Annexin V-fluorescein isothiocyanate (FITC)/propidium iodide methanolic crude extracts from the Mediterranean sponge (PI) staining. This assay is based on the ability of Annexin-V species A. oroides and P. ficiformis on two human neuro- to bind to the phosphatidylserine exposed on the surface of blastoma (NB) cell lines: LAN5 and SK-N-BE(2)-C. cells undergoing apoptosis and the capacity of propidium We found that A. oroides extract showed a pro-apoptotic iodide to enter cells that have lost their membrane integrity effect in LAN5 cells and investigations have been performed (28). Cells were grown and treated on chamber slides (Iwaki to elucidate some molecular mechanisms of this apoptotic Seiyaku Co., Tokyo, Japan), the medium was discarded, and the pathway. cells were incubated in the dark for 5 min at room temperature with 200 μl of 1X binding buffer, 0.5 μg/ml FITC-labelled Materials and methods recombinant Annexin-V, and 0.5 μg/ml propidium iodide. The cells were observed and counted (5-fields of ~60 cells) Chemicals. Polyvinylidene difluoride (PVDF) membrane, under a fluorescence Leica DIMRB microscope (Leica enhanced chemiluminescence Western blot analysis system, Microsystems AG, Wetzlar, Germany) using a dual filter set and secondary conjugated horseradish-peroxidase antibodies, for FITC and rhodamine. To evaluate apoptotic process, we which binds first rabbit or mouse antibodies, were supplied considered the percentage of Annexin-V-positive/propidium by Amersham International (Buckinghamshire, UK). iodide-negative cells. Rabbit polyclonal antibodies reacting with PKC‰ and NF-L were from Santa Cruz Biotechnology (Santa Cruz, CA, Measurement of reactive oxygen species (ROS) production. USA). Mouse monoclonal antibodies reacting with PKC· After sponge extract exposure, cells were incubated for 20 min and  were supplied by AbCam (Cambridgeshire, UK) and at 37˚C with 20 μM 2'-7'-dichlorofluorescein-diacetate anti-· fodrin was from Chemicon International (Germany). (DCFH-DA), a cell-permeable, nonfluorescent precursor of Goat anti-rabbit FITC-conjugated antibody was supplied by DCF that can be used as an intracellular probe for oxidative Upstate cell signaling solutions (NY, USA). The Annexin V- stress (29,30). Accumulation of DCF in the cells was measured FITC apoptosis detection kit was from Biovision Research by an increase in fluorescence at 530 nm when the sample Products (Mountain View, CA, USA). Protein G-sepharose was excited at 485 nm. Observations were made with a and dithiothreitol (DTT) were supplied by Pharmacia Biotech Leica DIMRB microscope, and a standard set of filters for (Uppsala, Sweden). [Á-32P]-ATP (specific activity 3,000 Ci/ fluorescein (excitation 460-500 nm, emission 510-560 nm) mmol) was from Perkin-Elmer Life Sciences. All other reagents was used. were from Sigma Chemicals Co. (St. Louis, MO, USA). NF-L detection. After treatments cells were fixed for 15 min Sponge collection and extraction procedure. Some individuals in 4% paraformaldehyde (PFA) in 10 mM PBS. Then, cells of the Mediterranean sponges Agelas oroides and Petrosia were permeabilized with 0.1% Triton X-100 in PBS, and ficiformis were collected during Winter 2003 from Portofino's washed three times in 10 mM PBS. Anti-NF-L primary anti- Promontory (Ligurian Sea, Italy) from depths of 10 to 20 m body (1:200 dilution in PBS) was added and incubated at and then frozen at -20˚C. Samples were then thawed and room temperature. After washing in PBS, FITC-conjugated placed in 0.9% NaCl at room temperature. Sponges were secondary antibody was added (1:300) and the cells were then homogenised and centrifuged at >10,000 rpm for 30 min. incubated for 30 min in a humidified atmosphere. Slides The supernatant was filtered, lyophilised and frozen again at were mounted with Mowiol 4-88 (Calbiochem, Darmstadt, -20˚C. Samples were extracted with methanol (1:1) on a stirrer Germany) and analyzed by Leica DIMRB microscope, using for 3 h or overnight. The supernatant was filtered through a 60x oil-immersion objective. ceramic filter and the solid material was placed again in the solvent for the second and third extraction. The supernatant Single cell
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