Immunocytological and biochemical analysis of the mode of action of bis (tri-n-butyltin) tri-oxide (TBTO) in Jurkat cells

Toxicology Letters

Volumn 212, Issue 2, 2012, Pages 126-136

  Katika, Madhumohan R ^a,b,d   Hendriksen, Peter J M ^a,d   de Ruijter, Norbert C A ^a   van Loveren, Henk ^b,c,d   Peijnenburg, Ad ^a,d  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^d Netherlands Toxicogenomics Centre   (Netherlands)

Author keywords

Bis (tri n butyltin) oxide (TBTO); Calcium mediated signaling; ER stress; Microarray; NF B; Oxidative stress and apoptosis

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; BIS(TRIBUTYLTIN)TRIOXIDE; CALCIUM; CALPAIN 2; GLUTATHIONE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; NUCLEAR RECEPTOR NUR77; ORGANOTIN COMPOUND; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG;

ARTICLE; CALCIUM CELL LEVEL; CELL VIABILITY; CHEMICAL ANALYSIS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; LEUKEMIA CELL LINE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

APOPTOSIS; CALCIUM; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION; HUMANS; IMMUNOSUPPRESSIVE AGENTS; JURKAT CELLS; NF-KAPPA B; NFATC TRANSCRIPTION FACTORS; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; TRIALKYLTIN COMPOUNDS;

MUS;

EID: 84861911900     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2012.05.010     Document Type: Article

References (84)

1. Anderson M.E. Glutathione: an overview of biosynthesis and modulation. Chemico-Biological Interactions 1998, 111-112:1-14.
2. Antizar-Ladislao B. Environmental levels, toxicity and human exposure to tributyltin (TBT)-contaminated marine environment. Environment International 2008, 34:292-308.
3. Aluoch A., Odman-Ghazi S., Whalen M. Pattern of MAP kinases p44/42 and JNK activation by non-lethal doses of tributyltin in human natural killer cells. Archives of Toxicology 2007, 81:271-277.
4. Aluoch A., Whalen M. Tributyltin-induced effects on MAP kinases p38 and p44/42 in human natural killer cells. Toxicology 2005, 209:263-277.
5. Aluoch A.O., Odman-Ghazi S.O., Whalen M.M. Alteration of an essential NK cell signaling pathway by low doses of tributyltin in human natural killer cells. Toxicology 2006, 224:229-237.
6. Aw T.Y., Nicotera P., Manzo L., Orrenius S. Tributyltin stimulates apoptosis in rat thymocytes. Archives of Biochemistry and Biophysics 1990, 283:46-50.
7. Baek S.H., Kim J.Y., Choi J.H., Park E.M., Han M.Y., Kim C.H., Ahn Y.S., Park Y.M. Reduced glutathione oxidation ratio and 8 ohdG accumulation by mild ischemic pretreatment. Brain Research 2000, 856:28-36.
8. Baken K.A., Arkusz J., Pennings J.L., Vandebriel R.J., van Loveren H. In vitro immunotoxicity of bis (tri-n-butyltin)oxide (TBTO) studied by toxicogenomics. Toxicology 2007, 237:35-48.
9. Baken K.A., Pennings J.L., de Vries A., Breit T.M., van Steeg H., van Loveren H. Gene expression profiling of bis(tri-n-butyltin)oxide (TBTO)-induced immunotoxicity in mice and rats. Journal of Immunotoxicology 2006, 3:227-244.
10. Berg C.P., Rothbart A., Lauber K., Stein G.M., Engels I.H., Belka C., Janicke R.U., Schulze-Osthoff K., Wesselborg S. Tributyltin (TBT) induces ultra-rapid caspase activation independent of apoptosome formation in human platelets. Oncogene 2003, 22:775-780.
11. Bissonnette S.L., Haas A., Mann K.K., Schlezinger J.J. The role of CaMKII in calcium-activated death pathways in bone marrow B cells. Toxicological sciences 2010, 118:108-118.
12. Boelsterli U.A. Idiosyncratic drug hepatotoxicity revisited: new insights from mechanistic toxicology. Toxicology Mechanisms and Methods 2003, 13:3-20.
13. Boyer I.J. Toxicity of dibutyltin, tributyltin and other organotin compounds to humans and to experimental animals. Toxicology 1989, 55:253-298.
14. 2+ signaling. American Journal of Physiology - Cell Physiology 2006, 291:C1082-C1088.
15. Cahalan M.D., Zhang S.L., Yeromin A.V., Ohlsen K., Roos J., Stauderman K.A. Molecular basis of the CRAC channel. Cell Calcium 2007, 42:133-144.
16. Chen B.P., Wolfgang C.D., Hai T. Analysis of ATF3, a transcription factor induced by physiological stresses and modulated by gadd153/Chop10. Molecular and Cellular Biology 1996, 16:1157-1168.
17. 2+ efflux. Archives of Biochemistry and Biophysics 1992, 298:143-149.
18. Corsini E., Viviani B., Marinovich M., Galli C.L. Role of mitochondria and calcium ions in tributyltin-induced gene regulatory pathways. Toxicology and Applied Pharmacology 1997, 145:74-81.
19. Elliott M.R., Chekeni F.B., Trampont P.C., Lazarowski E.R., Kadl A., Walk S.F., Park D., Woodson R.I., Ostankovich M., Sharma P., Lysiak J.J., Harden T.K., Leitinger N., Ravichandran K.S. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 2009, 461:282-286.
20. Funahashi N., Iwasaki I., Ide G. Effects of bis (tri-n-butyltin) oxide on endocrine and lymphoid organs of male rats. Acta Pathologica Japonica 1980, 30:955-966.
21. Gallo E.M., Cante-Barrett K., Crabtree G.R. Lymphocyte calcium signaling from membrane to nucleus. Nature Immunology 2006, 7:25-32.
22. Gennari A., Bleumink R., Viviani B., Galli C.L., Marinovich M., Pieters R., Corsini E. Identification by DNA macroarray of nur77 as a gene induced by di-n-butyltin dichloride: its role in organotin-induced apoptosis. Toxicology and Applied Pharmacology 2002, 181:27-31.
23. Granmo A., Ekelund R., Sneli J.A., Berggren M., Svavarsson J. Effects of antifouling paint components (TBTO, copper and triazine) on the early development of embryos in cod (Gadus morhua L.). Marine Pollutution Bulletin 2002, 44:1142-1148.
24. Grinwis G.C., Wester P.W., Vethaak A.D. Histopathological effects of chronic aqueous exposure to bis(tri-n-butyltin)oxide (TBTO) to environmentally relevant concentrations reveal thymus atrophy in European flounder (Platichthys flesus). Environmental Pollution 2009, 157:2587-2593.
25. Grondin M., Marion M., Denizeau F., Averill-Bates D.A. Tributyltin induces apoptotic signaling in hepatocytes through pathways involving the endoplasmic reticulum and mitochondria. Toxicology and Applied Pharmacology 2007, 222:57-68.
26. Grundler W., Dirscherl P., Beisker W., Marx K., Stampfl A., Maier K., Zimmermann I., Nusse M. Early functional apoptotic responses of thymocytes induced by tri-n-butyltin. Cytometry 2001, 44:45-56.
27. Guyton K.Z., Xu Q., Holbrook N.J. Induction of the mammalian stress response gene GADD153 by oxidative stress: role of AP-1 element. Biochemical Journal 1996, 314(Pt 2):547-554.
28. 2+ entry and NFAT activation in lymphocytes. Cell Calcium 2007, 42:145-156.
29. Hagger J.A., Depledge M.H., Galloway T.S. Toxicity of tributyltin in the marine mollusc Mytilus edulis. Marine Pollution Bulletin 2005, 51:811-816.
30. Hewavitharana T., Deng X., Soboloff J., Gill D.L. Role of STIM and Orai proteins in the store-operated calcium signaling pathway. Cell Calcium 2007, 42:173-182.
31. Hoffmann R., Bruno L., Seidl T., Rolink A., Melchers F. Rules for gene usage inferred from a comparison of large-scale gene expression profiles of T and B lymphocyte development. Journal of immunology 2003, 170:1339-1353.
32. Hogan P.G., Chen L., Nardone J., Rao A. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes and Development 2003, 17:2205-2232.
33. Jacobson T., Sundelin B., Yang G., Ford A.T. Low dose TBT exposure decreases amphipod immunocompetence and reproductive fitness. Aquatic Toxicology 2011, 101:72-77.
34. Jeruc J., Vizjak A., Rozman B., Ferluga D. Immunohistochemical expression of activated caspase-3 as a marker of apoptosis in glomeruli of human lupus nephritis. American Journal of Kidney Diseases 2006, 48:410-418.
35. Kannan K., Senthilkumar K., Giesy J.P. Occurrence of butyltin compounds in human blood. Environmental Science & Technology 1999, 33:1776-1779.
36. Kass G.E.N., Orrenius S. Calcium signaling and cytotoxicity. Environmental Health Perspectives 1999, 107:25-35.
37. Kaspar J.W., Niture S.K., Jaiswal A.K. Nrf2:INrf2 (Keap1) signaling in oxidative stress. Free Radical Biology & Medicine 2009, 47:1304-1309.
38. Katika M.R., Hendriksen P.J., van Loveren H., Peijnenburg A. Exposure of Jurkat cells to bis (tri-n-butyltin) oxide (TBTO) induces transcriptomics changes indicative for ER- and oxidative stress, T cell activation and apoptosis. Toxicology and Applied Pharmacology 2011, 254:311-322.
39. Konstantinidou A.E., Givalos N., Gakiopoulou H., Korkolopoulou P., Kotsiakis X., Boviatsis E., Agrogiannis G., Mahera H., Patsouris E. Caspase-3 immunohistochemical expression is a marker of apoptosis, increased grade and early recurrence in intracranial meningiomas. Apoptosis 2007, 12:695-705.
40. Lane R., Ghazi S., Whalen M. Increases in cytosolic calcium ion levels in human natural killer cells in response to butyltin exposure. Archives of Environmental Contamination and Toxicology 2009, 57:816-825.
41. Li G., Mongillo M., Chin K.T., Harding H., Ron D., Marks A.R., Tabas I. Role of ERO1-alpha-mediated stimulation of inositol 1,4,5-triphosphate receptor activity in endoplasmic reticulum stress-induced apoptosis. Journal of Cell Biology 2009, 186:783-792.
42. Luukkonen J., Hakulinen P., Maki-Paakkanen J., Juutilainen J., Naarala J. Enhancement of chemically induced reactive oxygen species production and DNA damage in human SH-SY5Y neuroblastoma cells by 872MHz radiofrequency radiation. Mutation Research 2009, 662:54-58.
43. Marinovich M., Viviani B., Galli C.L. Reversibility of tributyltin-chloride-induced protein synthesis inhibition after ATP recovery in HEL-30 cells. Toxicology Letters 1990, 52:311-317.
44. Martinez J.A., Zhang Z.Q., Svetlov S.I., Hayes R.L., Wang K.K., Larner S.F. Calpain and caspase processing of caspase-12 contribute to the ER stress-induced cell death pathway in differentiated PC12 cells. Apoptosis 2010, 15:1480-1493.
45. Mashima T., Udagawa S., Tsuruo T. Involvement of transcriptional repressor ATF3 in acceleration of caspase protease activation during DNA damaging agent-induced apoptosis. Journal of Cellular Physiology 2001, 188:352-358.
46. 2+ homeostasis under the ER stress. Neurochemistry International 2010, 56:352-356.
47. Nakagawa T., Zhu H., Morishima N., Li E., Xu J., Yankner B.A., Yuan J. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000, 403:98-103.
48. Nakatsu Y., Kotake Y., Ohta S. Tributyltin-induced cell death is mediated by calpain in PC12 cells. Neurotoxicology 2006, 27:587-593.
49. Naugler W.E., Karin M. NF-kappaB and cancer-identifying targets and mechanisms. Current Opinion in Genetics and Development 2008, 18:19-26.
50. Nishikimi A., Kira Y., Kasahara E., Sato E.F., Kanno T., Utsumi K., Inoue M. Tributyltin interacts with mitochondria and induces cytochrome c release. Biochemical Journal 2001, 356:621-626.
51. Niture S.K., Kaspar J.W., Shen J., Jaiswal A.K. Nrf2 signaling and cell survival. Toxicology and Applied Pharmacology 2010, 244:37-42.
52. O'Callaghan J.P., Miller D.B. Acute exposure of the neonatal rat to tributyltin results in decreases in biochemical indicators of synaptogenesis and myelinogenesis. Journal of Pharmacology and Experimental Therapeutics 1988, 246:394-402.
53. Okoro H.K., Fatoki O.S., Adekola F.A., Ximba B.J., Snyman R.G., Opeolu B. Human exposure, biomarkers, and fate of organotins in the environment. Reviews of Environment Contamination and Toxicology 2011, 213:27-54.
54. Osman A.M., van Kol S., Peijnenburg A., Blokland M., Pennings J.L., Kleinjans J.C., van Loveren H. Proteomic analysis of mouse thymoma EL4 cells treated with bis(tri-n-butyltin)oxide (TBTO). Journal of Immunotoxicology 2009, 6:174-183.
55. Oyadomari S., Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death and Differentiation 2004, 11:381-389.
56. Ozcan U., Yilmaz E., Ozcan L., Furuhashi M., Vaillancourt E., Smith R.O., Gorgun C.Z., Hotamisligil G.S. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006, 313:1137-1140.
57. 2+ and reactive oxygen intermediates as messengers. FEBS Letters 1996, 392:129-136.
58. Pan Y.J., Hopkins R.G., Loo G. Increased GADD153 gene expression during iron chelation-induced apoptosis in Jurkat T-lymphocytes. Biochimica et Biophysica Acta 2004, 1691:41-50.
59. Pieters R.H.H., Bol M., Penninks A.H. Immunotoxic organotins as possible model compounds in studying apoptosis and thymocyte differentiation. Toxicology 1994, 91:189-202.
60. Raffray M., Cohen G.M. Bis(tri-n-butyltin)oxide induces programmed cell death (apoptosis) in immature rat thymocytes. Archives of Toxicology 1991, 65:135-139.
61. Raffray M., Mccarthy D., Snowden R.T., Cohen G.M. Apoptosis as a mechanism of tributyltin cytotoxicity to thymocytes - relationship of apoptotic markers to biochemical and cellular effects. Toxicology and Applied Pharmacology 1993, 119:122-130.
62. Rusnak F., Mertz P. Calcineurin: form and function. Physiological Reviews 2000, 80:1483-1521.
63. Santos C.X., Tanaka L.Y., Wosniak J., Laurindo F.R. Mechanisms and implications of reactive oxygen species generation during the unfolded protein response: roles of endoplasmic reticulum oxidoreductases, mitochondrial electron transport, and NADPH oxidase. Antioxidants and Redox Signalling 2009, 11:2409-2427.
64. Shaffer A.L., Rosenwald A., Hurt E.M., Giltnane J.M., Lam L.T., Pickeral O.K., Staudt L.M. Signatures of the immune response. Immunity 2001, 15:375-385.
65. Snoeij N.J., Penninks A.H., Seinen W. Biological activity of organotin compounds - an overview. Environmental Research 1987, 44:335-353.
66. Starr T.K., Jameson S.C., Hogquist K.A. Positive and negative selection of T cells. Annual review of immunology 2003, 21:139-176.
67. Strasser A. Apoptosis - death of a T-cell. Nature 1995, 373:385-386.
68. Stridh H., Gigliotti D., Orrenius S., Cotgreave I. The role of calcium in pre- and postmitochondrial events in tributyltin-induced T-cell apoptosis. Biochemical and Biophysical Research Communications 1999, 266:460-465.
69. Stridh H., Kimland M., Jones D.P., Orrenius S., Hampton M.B. Cytochrome c release and caspase activation in hydrogen peroxide- and tributyltin-induced apoptosis. FEBS Letters 1998, 429:351-355.
70. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., Paulovich A., Pomeroy S.L., Golub T.R., Lander E.S., Mesirov J.P. Gene Set Enrichment Analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:15545-15550.
71. Sun E.W., Shi Y.F. Apoptosis: the quiet death silences the immune system. Pharmacology & Therapeutics 2001, 92:135-145.
72. Sun Z., Zhang S., Chan J.Y., Zhang D.D. Keap1 controls postinduction repression of the Nrf2-mediated antioxidant response by escorting nuclear export of Nrf2. Molecular and Cellular Biology 2007, 27:6334-6349.
73. Suzuki S., Suzuki N., Mirtsos C., Horacek T., Lye E., Noh S.K., Ho A., Bouchard D., Mak T.W., Yeh W.C. Nur77 as a survival factor in tumor necrosis factor signaling. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:8276-8280.
74. Takahashi S., Mukai H., Tanabe S., Sakayama K., Miyazaki T., Masuno H. Butyltin residues in livers of humans and wild terrestrial mammals and in plastic products. Environmental Pollution 1999, 106:213-218.
75. Touyz R.M. Reactive oxygen species, vascular oxidative stress, and redox signaling in hypertension - what is the clinical significance?. Hypertension 2004, 44:248-252.
76. Toyota H., Yanase N., Yoshimoto T., Moriyama M., Sudo T., Mizuguchi J. Calpain-induced Bax-cleavage product is a more potent inducer of apoptotic cell death than wild-type Bax. Cancer Letters 2003, 189:221-230.
77. Tsunoda M., Konno N., Nakano K., Liu Y. Altered metabolism of dopamine in the midbrain of mice treated with tributyltin chloride via subacute oral exposure. Environmental Science & Technology 2004, 11:209-219.
78. Vos J.G., De Klerk A., Krajnc E.I., Van Loveren H., Rozing J. Immunotoxicity of bis(tri-n-butyltin)oxide in the rat: effects on thymus-dependent immunity and on nonspecific resistance following long-term exposure in young versus aged rats. Toxicology and Applied Pharmacology 1990, 105:144-155.
79. Walsh C., Barrow S., Voronina S., Chvanov M., Petersen O.H., Tepikin A. Modulation of calcium signalling by mitochondria. Biochimica et Biophysica Acta 2009, 1787:1374-1382.
80. Whalen M.M., Loganathan B.G., Kannan K. Immunotoxicity of environmentally relevant concentrations of butyltins on human natural killer cells in vitro. Environmental Research 1999, 81:108-116.
81. Wiley J.C., Meabon J.S., Frankowski H., Smith E.A., Schecterson L.C., Bothwell M., Ladiges W.C. Phenylbutyric acid rescues endoplasmic reticulum stress-induced suppression of APP proteolysis and prevents apoptosis in neuronal cells. PLoS One 2010, 5:e9135.
82. Yoshizuka M., Hara K., Haramaki N., Yokoyama M., Mori N., Doi Y., Kawahara A., Fujimoto S. Studies on the hepatotoxicity induced by bis (tributyltin) oxide. Archives of Toxicology 1992, 66:182-187.
83. Yu W.J., Nam S.Y., Kim Y.C., Lee B.J., Yun Y.W. Effects of tributyltin chloride on the reproductive system in pubertal male rats. Journal of Veterinary Science 2003, 4:29-34.
84. 2+. Toxicology and Applied Pharmacology 2000, 168:200-207.