Molecular response to TBT stress in marine sponge Suberites domuncula: Proteolytical cleavage and phosphorylation of KRS_SD protein kinase

Journal of Experimental Marine Biology and Ecology

Volumn 297, Issue 2, 2003, Pages 239-252

  Fafandel, Maja ^a   Müller, Werner E G ^b   Batel, Renato ^a  

^a RUDER BO KOVI INSTITUTE   (Croatia)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

KRS_SD; Marine sponge; Protein kinase; Stress; Tributyl tin

Indexed keywords

PHYSIOLOGICAL RESPONSE; POLLUTION EFFECT; SPONGE; STRESS; TRIBUTYLTIN;

PORIFERA; SUBERITES; SUBERITES DOMUNCULA;

EID: 0242573481     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2003.07.008     Document Type: Article

References (47)

1. Alzieu, C., 1998. Tributyltin: case study of a chronic contaminant in the coastal environment. Ocean Coast. Manag. 40, 23-36.
2. Batel, R., Bihari, N., Rinkevich, B., Dapper, J., Schäcke, H., Schröder, H.C., Müller, W.E.G., 1993. Modulation of organotin-induced apoptosis by the water pollutant methyl mercury in a human lymphoblastoid tumor cell line and marine sponge. Mar. Ecol. Prog. Ser. 93, 245-251.
3. Böhm, M., Schröder, H.C., Müller, I.M., Müller, W.E.G., 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, 95-104.
4. Böhm, M., Hentschel, U., Friedrich, A.B., Fieseler, L., Steffen, R., Müller, I.M., Müller, W.E.G., 2001. Molecular response of the sponge Suberites domuncula to bacterial infection. Mar. Biol. 139, 1037-1045.
5. Chomczynsky, P., Sacchi, N., 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chlorophorm extraction. Anal. Biochem. 162, 156-159.
6. Cikala, M., Wilm, B., Hobmayer, Bottger, A., David, C.N., 1999. Identification of caspases and apoptosis in the simple metazoan Hydra. Curr. Biol. 9, 959-962.
7. Cima, F., Ballarin, L., 1999. TBT-induced apoptosis in Tunicate haemocytes. Appl. Organomet. Chem. 13, 697-703.
8. Creasy, C.L., Chernoff, J., 1995. Cloning and characterization of a human protein kinase with homology to Ste20. J. Biol. Chem. 270, 21695-21700.
9. Creasy, C.L., Ambrose, D.M., Chernoff, J., 1996. The ste20-like protein kinase MST1 dimerizes and contains an inhibitory domain. J. Biol. Chem. 271, 21049-21053.
10. Dyrynda, E.A., 1992. Incidence of abnormal shell thickening in the Pacific oyster Crassostrea gigas in Poole harbour (UK), subsequent to the 1987 TBT restrictions. Mar. Pollut. Bull. 24, 156-163.
11. Earnshaw, W.C., Martins, L.M., Kaufmann, S.H., 1999. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Ann. Rev. Biochem. 68, 383-424.
12. Efremova, S.M., Margulis, B.A., Guzhova, I.V., Itskovich, V.B., Laurenroth, S., Müller, W.E.G., Schröder, H.C., 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.
13. Ellis, R.E., Yuan, J., Horvitz, H.R., 1991. Mechanisms and functions of cell death. Annu. Rev. Cell Biol. 7, 663-698.
14. Franklin, R.A., McCubrey, J.A., 2000. Kinases: positive and negative regulators of apoptosis. Leukemia 14, 2019-2034.
15. Graves, J.D., Krebs, E.G., 1999. Protein phosphorylation and signal transduction. Pharmacol. Ther. 82, 111-121.
16. Graves, J.D., Gotoh, Y., Draves, K.E., Ambrose, D., Han, D.K., Wright, M., Chernoff, J., Clark, E.A., Krebs, E.G., 1998. Caspase-mediated activation and induction of apoptosis by the mammalian ste-20-like kinase MST1. EMBO J. 17, 2224-2234.
17. Graves, J.D., Draves, K.E., Gotoh, Y., Krebs, E.G., Clark, E.A., 2001. Both phosphorylation and caspase-mediated cleavage contribute to regulation of the Ste20-like protein kinase MST1 during CD95/Fas-induced apoptosis. J. Biol. Chem. 276, 14909-14915.
18. Jha, A.N., Hagger, J.A., Hill, S.J., Depledge, M.H., 2000. Genotoxic, cytotoxic and developmental effects of tributyltin oxide (ZBTO): an integrated approach to the evaluation of the relative sensitivities of two marine species. Mar. Environ. Res. 50, 565-573.
19. Kakeya, H., Onose, R., Osada, H., 1998. Caspase-mediated activation of 36 kDa myelin basic protein kinase during anticancer drug-induced apoptosis. Cancer Res. 58, 4888-4894.
20. Koziol, C., Batel, R., Arinc, E., Schröder, H.C., Müller, W.E.G., 1997. Expression of the potential bimarker heat shock protein 70 and its regulator, the metazoan DnaJ homolog, by temperature stress in the sponge Geodia cydonium. Mar. Ecol. Prog. Ser. 154, 261-268.
21. Kruse, M., Müller, I.M., Müller, W.E.G., 1997. Early evolution of metazoan serine/threonine and tyrosine kinases: identification of selected kinases in marine sponges. Mol. Biol. Evol. 14, 1326-1334.
22. Lee, K.K., Yonehara, S., 2002. Phosphorylation and dimerization regulate nucleoplasmic shuttling of mammalian STE20-like kinase (MST). J. Biol. Chem. 277, 12351-12358.
23. Lee, K.K., Murakawa, M., Nishida, E., Tsubuki, S., Kawashima, S., Sakamaki, K., Yonehara, S., 1998. Proteolytic activation of MST/KRS, STE20-related protein kinase by caspase during apoptosis. Oncogene 16, 3029-3037.
24. Lee, K.K., Ohyama, T., Yajima, N., Tsabuki, S., Yonehara, S., 2001. MST, a physiological caspase substrate, highly sensitizes apoptosis both upstream and downstream of caspase activation. J. Biol. Chem. 276, 19276-19285.
25. Lowry, D.H., Rosenbrough, N.J., Farr, A.L., Randall, R.J., 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
26. Mičić, M., Bihari, N., Labura, Ž., Müller, W.E.G., Batel, R., 2001. Induction of apoptosis in the blue mussel Mytilus galloprovincialis by tri-n-butyltin chloride. Aquat. Toxicol. 55, 61-73.
27. Mosser, D.D., Caron, A.W., Bourget, L., Denislarose, C., Massie, B., 1997. Role of the human heat shock protein hsp70 in protection against stress-induced apoptosis. Mol. Cell. Biol. 17, 5317-5327.
28. Müller, W.E.G. (Ed.), 1994. Use of Aquatic Invertebrates as Tools for Monitoring of Environmental Hazards. Gustav Fischer Verlag, Stuttgart.
29. Müller, W.E.G., Koziol, C., Kurelec, C., Dapper, J., Batel, R., Rinkevich, B., 1995. Combinatory effects of temperature stress and nonionic organic pollutants on stress protein (hsp70) gene expression in the fresh water sponge Ephydatia fluviatilis. Its potential assessment of environmental pollution. Mar. Biol. 125, 165-170.
30. Nicholson, D.W., Thornberry, N.A., 1997. Caspases: killer proteases. Trends Biochem. Sci. 22, 299-306.
31. Oehlmann, J., Stoben, E., Fioroni, P., 1991. The morphological expression of imposex in Nucella lapillus (L.). J. Molluscan Stud. 57, 375-390.
32. Samali, A., Cotter, T.G., 1996. Heat shock proteins increase resistance to apoptosis. Exp. Cell Res. 223, 163-170.
33. Sarà, M., Vacelet, J., 1973. Ecologie des Démosponges. In: Grassé, P.P. (Ed.), Traité de Zoologie: Spongiaires. Tome III (1). Masson, Paris, pp. 462-576.
34. Schröder, H.C., Shostak, K., Gamulin, V., Lacorn, M., Skorokhod, A., Kavsan, V., Müller, W.E.G., 2000. Purification, cDNA cloning and expression of a cadmium-inducible cystein-rich methallothionein-like protein from marine sponge Suberites domuncula. Mar. Ecol. Prog. Ser. 200, 149-157.
35. Stenalt, E., Johansen, B., Lillienskjold, S.V., Hansen, B.W., 1998. Mesocosm study of Mytilus edulis larvae and postlarvae, including the settlement phase, exposed to a gradient of tributyltin. Ecotoxicol. Environ. Saf. 40, 212-225.
36. Stridh, H., Kimland, M., Jones, D.P., Orrenius, S., Hampton, M.B., 1998. Cytochrome c release and caspase activation in hydrogen peroxide-and tributyltin-induced apoptosis. FEBS Lett. 429, 351-355.
37. Stridh, H., Orrenius, S., Hampton, M.B., 1999. Caspase involvement in the induction of apoptosis by the environmental toxicants tributyltin and triphenyltin. Toxicol. Appl. Pharmacol. 156, 141-146.
38. Taylor, L.K., Wang, H.R., Erikson, R.L., 1996. Newly identified stress-responsive protein kinases, Krs-1 and Krs-2. Proc. Natl. Acad. Sci. U. S. A. 93, 10099-10104.
39. Ura, S., Masuyama, N., Graves, J.D., Gotoh, Y., 2001. Caspase cleavage of MST1 promotes nuclear translocation and chromatin condensation. Proc. Natl. Acad. Sci. U. S. A. 98, 10148-10153.
40. Verdenal, B., Diana, C., Arnaux, A., Vacelet, J., 1990. Pollutant levels in Mediterranean commercial sponges. In: Rützler, K. (Ed.), New Perspectives in Sponge Biology. Smithsonian Institution Press, Washington, DC. 544 pp.
41. Vogel, S., 1977. Current-induced flow through living sponges in nature. Proc. Natl. Acad. Sci. U. S. A. 74, 2069-2071.
42. Wagner, C., Steffen, R., Koziol, C., Batel, R., Lacorn, M., Steinhart, H., Simat, T., Müller, W.E.G., 1998. Apoptosis in marine sponges - a biomarker for environmental stress (cadmium and bacteria). Mar. Biol. 131, 411-421.
43. Watabe, M., Kakeya, H., Osada, H., 1999. Requirement of protein kinase (KRS/MST) activation for MT-21 induced apoptosis. Oncogene 18, 5211-5220.
44. Williams, G.T., 1991. Programmed cell death: apoptosis and oncogenesis. Cell 65, 1097-1098.
45. Yue, T., Wang, C., Romanic, A.M., Kikly, K., Keller, P., DeWolf Jr., W.E., Hart, T.K., Thomas, H.C., Storer, B., Gu, J., Wang, X., Feuerstein, G.Z., 1998. Staurosporine-induced apoptosis in cardiomycetes. A potential role of caspase-3. J. Mol. Cell Cardiol. 30, 495-507.
46. Zahn, R.K., Zahn, G., Müller, W.E.G., Müller, I., Beyer, R., Müller-Berger, U., Kurelec, 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.
47. Zakeri, Z.F., Quaglino, D., Latham, T., Lockshin, R.A., 1993. Delayed internucleosomal DNA fragmentation in programmed cell death. FASEB J. 7, 470-478.