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MAP kinase cell signaling pathway as biomarker of environmental pollution in the sponge Suberites domuncula

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Abstract

In the present study, we analyzed the effects of two major pollutants of the environment, tributyltin (TBT) and water-accommodated fraction (WAF) of diesel oil, on MAP kinase activation, apoptosis induction and DNA damage, in the marine sponge Suberites domuncula. Our results clearly demonstrated a differential activation of the MAPKs depending on the chemicals tested. TBT induced the activation of p38 and JNK while diesel oil enhanced activation of both ERK and p38. The activation of MAPKs was observed after 1 h exposure and 6 and 24 h of recovery in seawater. In addition, DNA fragmentation, assessed by two techniques, the Fast micromethod® and the TUNEL assay, was detected after sponges were treated with both chemicals. Moreover, the study of caspase 3/7 activity showed that apoptosis was induced and triggered with all concentrations of TBT but only at high diesel oil concentrations. After TBT exposure, a correlation was observed between JNK activation, caspase 3 activity and DNA damage while p38 activation followed the two latter parameters at high concentrations of diesel oil, suggesting that sponges enhanced a specific apoptotic pathway depending on the xenobiotic tested. This study demonstrated a high signal response by the sponge Suberites domuncula to the tested chemicals. Cell signaling pathway studies may thus be of use in water quality biomonitoring programs.

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References

  • Arndt W (1935) Porifera. Tierwelt Nord-Ostsee IIIa:1–140

  • Batel R, Vukmirovic M, Bihari N, Zahn RK, Müller WE (1993) Nonradiometric detection of DNA crosslinks in mussel hemolymph by alkaline elution. Anal Biochem 212:402–406

    Article  CAS  Google Scholar 

  • Batel R, Fafandjel M, Blumbach B, Schröder HC, Hassanein HM, Müller IM, Müller WE (1998) Expression of the human XPB/ERCC-3 excision repair gene-homolog in the sponge Geodia cydonium after exposure to ultraviolet radiation. Mutat Res 409:123–133

    CAS  Google Scholar 

  • Batel R, Jaksic Z, Bihari N, Hamer B, Fafandel M, Chauvin C, Schröder HC, Müller WE, Zahn RK (1999) A microplate assay for DNA damage determination (fast micromethod). Anal Biochem 270:195–200

    Article  CAS  Google Scholar 

  • Bihari N, Fafandel M, Piskur V (2007) Polycyclic aromatic hydrocarbons and ecotoxicological characterization of seawater, sediment, and mussel Mytilus galloprovincialis from the Gulf of Rijeka, the Adriatic Sea, Croatia. Arch Environ Contam Toxicol 52:379–387

    Article  CAS  Google Scholar 

  • Bohm M, Schroder HC, Muller IM, Muller WE, Gamulin V (2000) The mitogen-activated protein kinase p38 pathway is conserved in metazoans: cloning and activation of p38 of the SAPK2 subfamily from the sponge Suberites domuncula. Biol Cell 92(2):95–104

    Article  CAS  Google Scholar 

  • Böhm M, Hentschel U, Friedrich A, Fieseler L, Steffen R, Gamulin V, Müller IM, Müller WEG (2001) Molecular response of the sponge Suberites domuncula to bacterial infection. Mar Biol 139:1037–1045

    Article  Google Scholar 

  • Burlando B, Berti E, Viarengo A (2006) Effects of seawater pollutants on protein tyrosine phosphorylation in mussel tissues. Aquat Toxicol 78(Suppl 1):79–85

    Article  Google Scholar 

  • Carballo JL, Naranjo SA, Garcia-Gomez JC (1996) Use of marine sponges as stress indicators in marine ecosystems at Algeciras Bay (Southern Iberian Peninsula). Mar Ecol Prog Ser 135:109–122

    Article  Google Scholar 

  • Carter LA, Tabor MB, Bonner JC, Bonner LA (2002) Mitogen-activated protein kinase activation by oxidative and bacterial stress in an amphibian cell culture model. Environ Health Perspect 110:641–645

    Article  CAS  Google Scholar 

  • Cebrian E, Uriz MJ, Turon X (2007) Sponges as biomonitors of heavy metals in spatial and temporal surveys in northwestern mediterranean: multispecies comparison. Environ Toxicol Chem 26(11):2430–2439

    Article  CAS  Google Scholar 

  • Châtel A, Hamer B, Talarmin H, Dorange G, Schröder HC, Müller WE (2010) Activation of MAP kinase signaling pathway in the mussel Mytilus galloprovincialis as biomarker of environmental pollution. Aquat Toxicol 96(4):247–255

    Article  Google Scholar 

  • Chen S, Nguyen N, Tamura K, Karin M, Tukey RH (2003) The role of the Ah receptor and p38 in benzo[a]pyrene-7,8-dihydrodiol and benzo[a]pyrene-7,8-dihydrodiol-9,10-epoxide-induced apoptosis. J Biol Chem 278:19526–19533

    Article  CAS  Google Scholar 

  • Cosa G, Foscaneanu KS, McLean JRN, Sciano JC (2001) Photophysical properties of fluorescent DNA-dyes bound to single- and double-stranded DNA in aqueous buffered solution. Photochem Photobiol 73:585–599

    Article  CAS  Google Scholar 

  • Creasy CL, Chernoff J (1995) Cloning and of a member of the MST sunfamily of STE`20-like kinases. Gene 167:303–306

    Article  CAS  Google Scholar 

  • Damiani F, Gianguzza M, Dolcemascolo G (2009) Effects of tributyltin chloride in ascidian embryos: modulation of kinase-mediated signalling pathways. Invert Surviv J 6:87–94

    Google Scholar 

  • Das M, Mukherjee SB, Shaha C (2001) Hydrogen peroxide induces apoptosis-like death in Leishmania donovani promastigotes. J Cell Sci 114:2461–2469

    CAS  Google Scholar 

  • Dayton PK, Robilliard GA, Paine RT (1970) Benthic fauna1 zonation as a result of anchor ice at Mc Murdo Sound, Antarctica. In: Holdgate MW (ed) Antarctic ecology, vol 1. Academic Press, London, pp 244–258

    Google Scholar 

  • Diaz J-P (1977) Transformation histologiques et cytologiques post-traumatiques chez la Demosponge Suberites massa. Nardo Bull Mus Nat Hist Natur (Paris) 3rd Ser No 445. Zoologie 308:375–396

  • Dorneles PR, Lailson-Brito J, Fernandez MA, Vidal LG, Barbosa LA, Azevedo AF, Fragoso AB, Torres JP, Malm O (2008) Evaluation of cetacean exposure to organotin compounds in Brazilian waters through hepatic total tin concentrations. Environ Pollut 156(3):1268–1276

    Article  CAS  Google Scholar 

  • Efremova SM, Margulis BA, Guzhova IV, Itskovich VB, Lauenroth S, Müller WE, Schröder HC (2002) Heat shock protein Hsp70 expression and DNA damage in Baikalian sponges exposed to model pollutants and wastewater from Baikalsk Pulp and Paper Plant. Aquat Toxicol 57:267–280

    Article  CAS  Google Scholar 

  • Fafandel M, Müller WEG, Batel R (2003) Molecular response to TBT stress in marine sponge Suberites domuncula: proteolytical cleavage and phosphorylation of KRS_SD protein kinase. J Exp Mar Biol Ecol 297:239–252

    Article  CAS  Google Scholar 

  • Fauré-Frémiet E (1932) Involution experimentale et tension de structure dans les cultures de Ficulina ficus. Arch Anat Micros 28:121–157

    Google Scholar 

  • Féral JP, Fusey P, Gaill Fr, Lopez E, Martelly E, Oudot J, van Praet M (1979) Evolution des teneurs en hydrocarbures chez quelques organismes marins du Nord Finistère depuis l’échouage de l’Amoco Cadiz et comparaison des méthodes de dosage en infra-rouge et spectrofluorimétrie. CR Acad Sci Paris 288:713–716

    Google Scholar 

  • Gabe M (1968) Techniques histologiques. Masson & Cie, Paris, p 113

  • Gaitanaki C, Kefaloyianni E, Marmari A, Beis I (2004) Various stressors rapidly activate the p38-MAPK signaling pathway in Mytilus galloprovincialis (Lam.). Mol Cell Biochem 260:119–127

    Article  CAS  Google Scholar 

  • Gambaro A, Manodori L, Toscano G, Contini D, Donateo A, Belosi F, Prodi F, Cescon P (2007) Pahs and trace elements in PM(2.5) at the Venice Lagoon. Ann Chim 97(5–6):343–358

    Article  CAS  Google Scholar 

  • Grebenjuk VA, Kuusksalu A, Kelve M, Schütze J, Schröder HC, Müller WE (2002) Induction of (2′–5′)oligoadenylate synthetase in the marine sponges Suberites domuncula and Geodia cydonium by the bacterial endotoxin lipopolysaccharide. Eur J Biochem 269(5):1382–1392

    Article  CAS  Google Scholar 

  • Gundert-Remy U, Dahl SG, Boobis A, Kremers P, Kopp-Schneider A, Oberemm A, Renwick A, Pelkonen O (2005) Molecular approaches to the identification of biomarkers of exposure and effect: report of an expert meeting organized by COST Action B15. November 28, 2003. Toxicol Lett 156:227–240

    Article  CAS  Google Scholar 

  • Haeckel E (1896) Systematische Phylogenie der Wirbellosen Thiere; Teil 2. Georg Reimer, Berlin

    Google Scholar 

  • Halliwell B, Aruoma OI (1991) DNA damage by oxygen-derived species. Its mechanism and measurement in mammalian systems. FEBS Lett 281:9–19

    Article  CAS  Google Scholar 

  • Hamer B, Jakšić Ž, Pavičić-Hamer D, Perić L, Medaković D, Ivanković D, Pavičić J, Zilberberg C, Schröder HC, Müller WEG, Smodlaka N, Batel R (2008) Effect of hypoosmotic stress by low salinity acclimation of Mediterranean mussel Mytilus galloprovincialis on biological parameters used for pollution assessment. Aquat Toxicol 89:137–151

    Article  CAS  Google Scholar 

  • Hansen IV, Weeks JM, Depledge MH (1995) Accumulation of copper, zinc, cadmium and chromium by the marine sponge Halichondria panicea Pallas and the implications for biomonitoring. Mar Poll Bull 31:133–138

    Article  CAS  Google Scholar 

  • Harino H, Yamamoto Y, Eguchi S, Kawai S, Kurokawa Y, Arai T, Ohji M, Okamura H, Miyazaki N (2007) Concentrations of antifouling biocides in sediment and mussel samples collected from Otsuchi bay, Japan. Arch Environ Contam Toxicol 52(2):179–188

    Article  CAS  Google Scholar 

  • Harino H, Ohji M, Wattayakorn G, Adulyanukosol K, Arai T, Miyazaki N (2008) Accumulation of organotin compounds in tissues and organs of dolphins from the coasts of Thailand. Arch Environ Contam Toxicol 54(1):145–153

    Article  CAS  Google Scholar 

  • Jaksic Z, Batel R (2003) DNA integrity determination in marine invertebrates by Fast Micromethod. Aquat Toxicol 65:361–376

    Article  CAS  Google Scholar 

  • Kannan K, Villeneuve DL, Blankenship AL, Giesy JP (1998) Interaction of tributyltin with 3,3′,4,4′, 5-pentachlorobiphenyl-induced ethoxyresorufin O-deethylase activity in rat hepatoma cells. J Toxicol Environ Health A 55:373–384

    Article  CAS  Google Scholar 

  • Karpiak VC, Bridges RJ, Eyer CL (2001) Organotins disrupt components of glutamate homeostasis in rat astrocyte cultures. J Toxicol Environ Health A 63:273–287

    Article  CAS  Google Scholar 

  • Koziol C, Borojevic R, Steffen R, Müller WE (1998) Sponges (Porifera) model systems to study the shift from immortal to senescent somatic cells: the telomerase activity in somatic cells. Mech Ageing Dev 100:107–120

    Article  CAS  Google Scholar 

  • Krasko A, Schroder HC, Perovic S, Steffen R, Kruse M, Reichert W, Muller IM, Muller WE (1999) Ethylene modulates gene expression in cells of the marine sponge Suberites domuncula and reduces the degree of apoptosis. J Biol Chem 274(44):31524–31530

    Article  CAS  Google Scholar 

  • Kruse M, Müller IM, Müller WEG (1997) Early evolution of metazoan serine threonine and tyrosine kinases: identification of selected kinases in marine sponges. Mol Biol Evol 14:1326–1334

    CAS  Google Scholar 

  • Kruszewski M, Green MH, Lowe JE, Szumiel I (1994) DNA strand breakage, cytotoxicity and mutagenicity of hydrogen peroxide treatment at 4 degrees C and 37 degrees C in L5178Y sublines. Mutat Res 308:233–241

    Article  CAS  Google Scholar 

  • Kultz D, Avila K (2001) Mitogen-activated protein kinases are in vivo transducers of osmosensory signals in fish gill cells. Comp Biochem Physiol B Biochem Mol Biol 129:821–829

    Article  CAS  Google Scholar 

  • Kurelec B, Britvic S, Krca S, Muller WE, Zahn RK (1987) Metabolism of some carcinogenic aromatic amines in four species of marine sponges. Comp Biochem Physiol C 86(1):17–22

    Article  CAS  Google Scholar 

  • Kyriakis JM, Avruch J (1996) Protein kinase cascades activated by stress and inflammatory cytokines. Bioessays 18(7):567–577

    Article  CAS  Google Scholar 

  • Kyriakis JM, Avruch J (2001) Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81:807–869

    CAS  Google Scholar 

  • Lavoie JN, L’Allemain G, Brunet A, Muller R, Pouyssegur J (1996) Cyclin D1 expression is regulated positively by the p42/p44MAPK and negatively by the p38/HOGMAPK pathway. J Biol Chem 271(34):20608–20616

    Article  CAS  Google Scholar 

  • Leberer E, Dignard D, Harcus D, Thomas DY, Whiteway M (1992) The protein kinase homologue Ste20p is required to link the yeast pheromone response G-protein subunits to downstream signalling components. EMBO J 11:4815–4824

    CAS  Google Scholar 

  • Lei W, Yu R, Mandlekar S, Kong AN (1998) Induction of apoptosis and activation of interleukin 1beta-converting enzyme/Ced-3 protease (caspase-3) and c-Jun NH2-terminal kinase 1 by benzo(a)pyrene. Cancer Res 58:2102–2106

    CAS  Google Scholar 

  • Lewis C, Pook C, Galloway T (2008) Reproductive toxicity of the water accommodated fraction (WAF) of crude oil in the polychaetes Arenicola marina (L.) and Nereis virens (Sars). Aquat Toxicol 90:73–81

    Article  CAS  Google Scholar 

  • Li J, Huang CY, Zheng RL, Cui KR, Li JF (2000) Hydrogen peroxide induces apoptosis in human hepatoma cells and alters cell redox status. Cell Biol Int 24:9–23

    Article  CAS  Google Scholar 

  • Li BH, Zhou YB, Guo SB, Wang CB (2007) Polypeptide from Chlamys farreri inhibits UVB-induced HaCaT cells apoptosis via inhibition CD95 pathway and reactive oxygen species. Free Radic Res 41(11):1224–1232

    Article  CAS  Google Scholar 

  • Luchetti F, Betti M, Canonico B, Arcangeletti M, Ferri P, Galli F, Papa S (2009) ERK MAPK activation mediates the antiapoptotic signaling of melatonin in UVB-stressed U937 cells. Free Radic Biol Med 46:339–351

    Article  CAS  Google Scholar 

  • Masuda K, Shima H, Katagiri C, Kikuchi K (2003) Activation of ERK induces phosphorylation of MAPK phosphatase-7, a JNK specific phosphatase, at Ser-446. J Biol Chem 278(34):32448–32456

    Article  CAS  Google Scholar 

  • Micic M, Bihari N, Labura Z, Muller WE, Batel R (2001) Induction of apoptosis in the blue mussel Mytilus galloprovincialis by tri-n-butyltin chloride. Aquat Toxicol 55:61–73

    Article  CAS  Google Scholar 

  • Micic M, Bihari N, Jaksic Z, Müller WE, Batel R (2002) DNA damage and apoptosis in the mussel Mytilus galloprovincialis. Mar Environ Res 53:243–262

    Article  CAS  Google Scholar 

  • Muller WE (1998) Origin of Metazoa: sponges as living fossils. Naturwissenschaften 85(1):11–25

    Article  CAS  Google Scholar 

  • Müller WEG, Müller I (1998) Sponge cells and tissue as biological monitors of aquatic pollution. In: Wells PG, Lee K, Blase C (eds) Microscale aquatic toxicology—advances, techniques and practice. CRC Lewis Publishers, Boca Raton

    Google Scholar 

  • Müller WEG, Custódio MR, Wiens M, Zilberberg C, Châtel A, Müller I, Schröder HC (2009) Effect of bacterial infection on stem cell pattern in Porifera. In: Baruch B, Valeria V (Org) Stem cells in marine organisms. Springer, Berlin, pp 1–28

    Google Scholar 

  • Negri A, Burns K, Boyle S, Brinkman D, Webster N (2006) Contamination in sediments, bivalves and sponges of McMurdo Sound, Antarctica. Environ Pollut 143(3):456–467

    Article  CAS  Google Scholar 

  • Orlov YA (1971) Fundamentals of palaeontology, vol II. Israel program for the Scientific Translations, Jerusalem, p 11

    Google Scholar 

  • Owuor ED, Kong AN (2002) Antioxidants and oxidants regulated signal transduction pathways. Biochem Pharmacol 64:765–770

    Article  CAS  Google Scholar 

  • Pages G, Lenormand P, L’Allemain G, Chambard JC, Meloche S, Pouyssegur J (1993) Mitogen-activated protein kinases p42mapk and p44mapk are required for fibroblast proliferation. Proc Natl Acad Sci USA 90:8319–8323

    Article  CAS  Google Scholar 

  • Palomba L, Sestili P, Columbaro M, Falcieri E, Cantoni O (1999) Apoptosis and necrosis following exposure of U937 cells to increasing concentrations of hydrogen peroxide: the effect of the poly(ADP-ribose)polymerase inhibitor 3-aminobenzamide. Biochem Pharmacol 58:1743–1750

    Article  CAS  Google Scholar 

  • Park J, Liu AY (2001) JNK phosphorylates the HSF1 transcriptional activation domain: role of JNK in the regulation of the heat shock response. J Cell Biochem 82:326–338

    Article  CAS  Google Scholar 

  • Patel B, Balani MC, Patel S (1985) Sponge ‘sentinel’ of heavy metals. Sci Total Environ 41(2):143–152

    Article  CAS  Google Scholar 

  • Pelkonen O, Nebert DW (1982) Metabolism of polycyclic aromatic hydrocarbons: etiologic role in carcinogenesis. Pharmacol Rev 34:189–222

    CAS  Google Scholar 

  • Phillips DH, Grover PL (1984) Biologically-active and chemically-reactive polycyclic hydrocarbon metabolites. IARC Sci Publ 47–61

  • Poonam S, Paily KP, Balaraman K (2002) Oviposition attractancy of bacterial culture filtrates: response of Culex quinquefasciatus. Mem Inst Oswaldo Cruz 97:359–362

    Article  CAS  Google Scholar 

  • Ranganna K, Yousefipour Z, Nasif R, Yatsu FM, Milton SG, Hayes BE (2002) Acrolein activates mitogen-activated protein kinase signal transduction pathways in rat vascular smooth muscle cells. Mol Cell Biochem 240:83–98

    Article  CAS  Google Scholar 

  • Rao JV, Kavitha P, Reddy NC, Rao TG (2006) Petrosia testudinaria as a biomarker for metal contamination at Gulf of Mannar, southeast coast of India. Chemosphere 65(4):634–638

    Article  CAS  Google Scholar 

  • Riedl R (1983) Fauna und Flora des Mittelmeeres. Paul Parey édit Hamburg Germ 1–836

  • Roux PP, Blenis J (2004) ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol Mol Biol Rev 68:320–344

    Article  CAS  Google Scholar 

  • Rummel AM, Trosko JE, Wilson MR, Upham BL (1999) Polycyclic aromatic hydrocarbons with bay-like regions inhibited gap junctional intercellular communication and stimulated MAPK activity. Toxicol Sci 49:232–240

    Article  CAS  Google Scholar 

  • Saco-Alvarez L, Bellas J, Nieto O, Bayona JM, Albaigés J, Beiras R (2008) Toxicity and phototoxicity of water-accommodated fraction obtained from Prestige fuel oil and Marine fuel oil evaluated by marine bioassays. Sci Total Environ 394:275–282

    Article  CAS  Google Scholar 

  • Sancar A (1996) DNA excision repair. Annu Rev Biochem 65:43–81

    Article  CAS  Google Scholar 

  • Schröder HC, Hassanein HM, Lauenroth S, Koziol C, Mohamed TA, Lacorn M, Steinhart H, Batel R, Müller WE (1999) Induction of DNA strand breaks and expression of HSP70 and GRP78 homolog by cadmium in the marine sponge Suberites domuncula. Arch Environ Contam Toxicol 36:47–55

    Article  Google Scholar 

  • Shim WJ, Hong SH, Kim NS, Yim UH, Li D, Oh JR (2005) Assessment of butyl- and phenyltin pollution in the coastal environment of Korea using mussels and oysters. Mar Pollut Bull 51(8–12):922–931

    Article  CAS  Google Scholar 

  • Simpson TL (1984) The cell biology of sponges. Springer, New York, pp 414–510

    Google Scholar 

  • Singh NP, McCoy MT, Tice RR, Schneider EL (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175:184–191

    Article  CAS  Google Scholar 

  • Smith RL, Cameron JA (1979) Effect of water soluble fraction of Prudhoe Bay crude oil on embryonic development of Pacific Herring. Trans Am Fish Soc 108:70–75

    Article  Google Scholar 

  • Strasser A, O’Connor L, Dixit VM (2000) Apoptosis signaling. Annu Rev Biochem 69:217–245

    Article  CAS  Google Scholar 

  • Tu VC, Bahl JJ, Chen QM (2003) Distinct roles of p42/p44(ERK) and p38 MAPK in oxidant-induced AP-1 activation and cardiomyocyte hypertrophy. Cardiovasc Toxicol 3:119–133

    Article  CAS  Google Scholar 

  • Valentine JW (1994) The cambrian explosion. In: Bengtson S (ed) Early life on earth. Columbia University Press, New York, pp 401–412

  • Volkman (2006) Biomarkers, isotopes and DNA 1. Marine organic matter. Wat Res 29(8):1877–1884

    Google Scholar 

  • von Sonntag C (1987) New aspects in the free-radical chemistry of pyrimidine nucleobases. Free Radic Res Commun 2:217–224

    Article  Google Scholar 

  • Wada T, Penninger JM (2004) Mitogen-activated protein kinases in apoptosis regulation. Oncogene 23:2838–2849

    Article  CAS  Google Scholar 

  • Wagner C, Steffen R, Koziol C, Batel R, Lacorn M, Steinhart H, Simat T, Müller WEG (1998) Apoptosis in marine sponges: a biomarker for environmental stress (cadmium and bacteria). Mar Biol 131:411–421

    Article  CAS  Google Scholar 

  • Wang Y, Wang C, Zhang J, Chen Y, Zuo Z (2009) DNA hypomethylation induced by tributyltin, triphenyltin, and a mixture of these in Sebastiscus marmoratus liver. Aquat Toxicol 95(2):93–98

    Article  CAS  Google Scholar 

  • Webster NS, Webb RI, Ridd MJ, Hill RT, Negri AP (2001) The effects of copper on the microbial community of a coral reef sponge. Environ Microbiol 3(1):19–31

    Article  CAS  Google Scholar 

  • White KL Jr, Kawabata TT, Ladics GS (1994) Mechanisms of polycyclic aromatic hydrocarbon immunotoxicity. In: Dean JH, Luster MI, Munson AE, Kimber I (eds) Immunotoxicology and immunopharmacology, 2nd edn. Raven Press, New York, pp 123–142

    Google Scholar 

  • Widmann C, Gibson S, Jarpe MB, Johnson GL (1999) Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 79:143–180

    CAS  Google Scholar 

  • Wiens M, Diehl-Seifert B, Müller WE (2001) Sponge Bcl-2 homologous protein (BHP2-GC) confers distinct stress resistance to human HEK-293 cells. Cell Death Differ 8:887–898

    Article  CAS  Google Scholar 

  • Wiens M, Krasko A, Perovic S, Müller WE (2003) Caspase-mediated apoptosis in sponges: cloning and function of the phylogenetic oldest apoptotic proteases from Metazoa. Biochim Biophys Acta 1593:179–189

    Article  CAS  Google Scholar 

  • Wiens M, Korzhev M, Perovic-Ottstadt S, Luthringer B, Brandt D, Klein S, Müller WE (2007) Toll-like receptors are part of the innate immune defense system of sponges (demospongiae: Porifera). Mol Biol Evol 24:792–804

    Article  CAS  Google Scholar 

  • Yu ZP, Matsuoka M, Wispriyono B, Iryo Y, Igisu H (2000) Activation of mitogen-activated protein kinases by tributyltin in CCRF-CEM cells: role of intracellular Ca(2 +). Toxicol Appl Pharmacol 168:200–207

    Article  CAS  Google Scholar 

  • Zahn RK, Zahn G, Muller WE, Müller I, Beyer R, Müller-Berger U, Kupelec B, Rijavec M, Britvic S (1977) Consequences of detergent pollution of the sea: effects on regenerating sponge cubes of Geodia cydonium. Sci Total Environ 8:109–151

    Article  CAS  Google Scholar 

  • Zahn RK, Zahn G, Müller WE, Kurelec B, Rijavec M, Batel R, Given R (1981) Assessing consequences of marine pollution by hydrocarbons using sponges as model organisms. Sci Total Environ 20(2):147–169

    Article  CAS  Google Scholar 

  • Zrouri H, Le Goascogne C, Li WW, Pierre M, Courtin F (2004) The role of MAP kinases in rapid gene induction after lesioning of the rat sciatic nerve. Eur J Neurosci 20:1811–1818

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by grants from the Bundesministerium für Bildung und Forschung (project 03F0451: cooperation project WTZ BRA—Health of marine ecosystems, and Center of Excellence BIOTECmarin), the Bundesministerium für Bildung und Forschung Germany (project “Center of Excellence BIOTECmarin”) and the International Human Frontier Science Program (RG-333/96-M). The authors acknowledge Dr. McKenzie for his help in the english writing.

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  1. EA 4326, Facteurs Nerveux et Structuration Tissulaire, Faculté de Médecine, Université de Bretagne Occidentale, 22 Avenue Camille Desmoulins, 29609, Brest Cedex, France

    A. Châtel, H. Talarmin & G. Dorange

  2. Institut für Physiologische Chemie und Pathobiochemie, Johannes Gutenberg Universität, Duesbergweg 6, 55099, Mainz, Germany

    A. Châtel, H. C. Schröder & W. E. G. Müller

  3. Laboratory for Marine Molecular Biology, Ruder Bošković Institute, Center for Marine Research, Giordano Paliaga 5, 52210, Rovinj, Croatia

    B. Hamer

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  1. A. Châtel
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Correspondence to A. Châtel.

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A. Châtel and H. Talarmin have contributed equally to this work.

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Châtel, A., Talarmin, H., Hamer, B. et al. MAP kinase cell signaling pathway as biomarker of environmental pollution in the sponge Suberites domuncula . Ecotoxicology 20, 1727–1740 (2011). https://doi.org/10.1007/s10646-011-0706-1

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