Phenylpyrazole insecticides induce cytotoxicity by altering mechanisms involved in cellular energy supply in the human epithelial cell model Caco-2

Toxicology in Vitro

Volumn 23, Issue 4, 2009, Pages 589-597

  Vidau, Cyril ^a   Brunet, Jean Luc ^a   Badiou, Alexandra ^a   Belzunces, Luc P ^a  

^a Laboratoire de Toxicologie Environnementale   (France)

Author keywords

ATP; Caco 2 cell; Cytotoxicity; Energetic metabolism; Fipronil; Human; LDH; TEER

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; ADENOSINE TRIPHOSPHATE; ETHIPROL; FIPRONIL; INSECTICIDE; LACTATE DEHYDROGENASE; LACTIC ACID; SULFIDE; SULFONE; UNCLASSIFIED DRUG; XENOBIOTIC AGENT;

ARTICLE; BIOSYNTHESIS; CELL ENERGY; CELL METABOLISM; CELL STRAIN CACO 2; CELL VIABILITY; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; ELECTRIC RESISTANCE; ENERGY CONSUMPTION; EPITHELIUM CELL; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM; MEMBRANE PERMEABILITY; METABOLITE; MITOCHONDRION; NITROBLUE TETRAZOLIUM TEST; PROTEIN EXPRESSION; TOXICITY TESTING;

ADENOSINE TRIPHOSPHATE; CACO-2 CELLS; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRIC IMPEDANCE; ENERGY METABOLISM; EPITHELIAL CELLS; HUMANS; INSECTICIDES; L-LACTATE DEHYDROGENASE; LACTIC ACID; MITOCHONDRIA; PYRAZOLES;

HEXAPODA;

EID: 67349087405     PISSN: 08872333     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tiv.2009.01.017     Document Type: Article

References (60)

1. Aspenstrom-Fagerlund B., Ring L., Aspenstrom P., Tallkvist J., Ilback N.G., and Glynn A.W. Oleic acid and docosahexaenoic acid cause an increase in the paracellular absorption of hydrophilic compounds in an experimental model of human absorptive enterocytes. Toxicology 237 (2007) 12-23
2. Berridge M.V., and Tan A.S. Characterization of the cellular reduction of 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT): subcellular localization, substrate dependence, and involvement of mitochondrial electron transport in MTT reduction. Archives of Biochemistry and Biophysics 303 (1993) 474-482
3. Berridge M.V., Tan A.S., McCoy K.D., and Wang R. The biochemical and cellular basis of cell proliferation assays that use tetrazolium salts. Biochemica 4 (1996) 14-19
4. Berridge M.V., Herst P.M., and Tan A.S. Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction. Biotechnology Annual Review 11 (2005) 127-152
5. Brunet J.L., Maresca M., Fantini J., and Belzunces L.P. Human intestinal absorption of imidacloprid with Caco-2 cells as enterocyte model. Toxicology and Applied Pharmacology 194 (2004) 1-9
6. Buckingham S.D., Hosie A.M., Roush R.L., and Sattelle D.B. Actions of agonists and convulsant antagonists on a Drosophila melanogaster GABA receptor (Rdl) homo-oligomer expressed in Xenopus oocytes. Neuroscience Letters 181 (1994) 137-140
7. Cittadini A., Bossi D., Longhi G., and Terranova T. Energy metabolism of isolated rat thymus cells. Molecular and Cellular Biochemistry 8 (1975) 49-57
8. Cole L.M., Nicholson R.A., and Casida J.E. Action of phenylpyrazole insecticides at the GABA-gated chloride channel. Pesticide Biochemistry and Physiology 46 (1993) 47-54
9. Collier A.C., and Pritsos C.A. The mitochondrial uncoupler dicumarol disrupts the MTT assay. Biochemical Pharmacology 66 (2003) 281-287
10. Cooper J., and Dobson H. The benefits of pesticides to mankind and the environment. Crop Protection 26 (2007) 1337-1348
11. Curtis C.F., Jana-Kara B., and Maxwell C.A. Insecticide treated nets: impact on vector populations and relevance of initial intensity of transmission and pyrethroid resistance. Journal of Vector Borne Diseases 40 (2003) 1-8
12. Das P.C., Cao Y., Cherrington N., Hodgson E., and Rose R.L. Fipronil induces CYP isoforms and cytotoxicity in human hepatocytes. Chemico-Biological Interactions 164 (2006) 200-214
13. Delie F., and Rubas W. A human colonic cell line sharing similarities with enterocytes as a model to examine oral absorption: advantages and limitations of the Caco-2 model. Critical Reviews in Therapeutic Drug Carrier Systems 14 (1997) 221-286
14. Den Hond E., and Schoeters G. Endocrine disrupters and human puberty. International Journal of Andrology 29 (2006) 264-271 (discussion 286-290)
15. Dickman K.G., and Mandel L.J. Differential effects of respiratory inhibitors on glycolysis in proximal tubules. American Journal of Physiology 258 (1990) F1608-F1615
16. Eisenbrand G., Pool-Zobel B., Baker V., Balls M., Blaauboer B.J., Boobis A., Carere A., Kevekordes S., Lhuguenot J.C., Pieters R., and Kleiner J. Methods of in vitro toxicology. Food and Chemical Toxicology 40 (2002) 193-236
17. Forawi H.A., Tchounwou P.B., and McMurray R.W. Xenoestrogen modulation of the immune system: effects of dichlorodiphenyltrichloroethane (DDT) and 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Reviews on Environmental Health 19 (2004) 1-13
18. Galloway T., and Handy R. Immunotoxicity of organophosphorous pesticides. Ecotoxicology 12 (2003) 345-363
19. Gramatté T., and Terhaag B. The variability of orocecal transit time evaluated by the salicylazosulphapyridine/sulphapyridine method. International Journal of Clinical Pharmacology, Therapy and Toxicology 29 (1991) 147-150
20. Hurley P.M. Mode of carcinogenic action of pesticides inducing thyroid follicular cell tumors in rodents. Environmental Health Perspectives 106 (1998) 437-445
21. Joo H., Choi K., Rose R.L., and Hodgson E. Inhibition of fipronil and nonane metabolism in human liver microsomes and human cytochrome P450 isoforms by chlorpyrifos. Journal of Biochemical and Molecular Toxicology 21 (2007) 76-80
22. Keller G., Ben-Shaul Y., and Bacher A. Influence of metabolic inhibitors on the degradation of tight junctions in HT29 cells. Experimental Cell Research 200 (1992) 16-25
23. Khanjani N., Hoving J.L., Forbes A.B., and Sim M.R. Systematic review and meta-analysis of cyclodiene insecticides and breast cancer. Journal of environmental Science and Health. Part C, Environmental Carcinogenesis & Ecotoxicology Reviews 25 (2007) 23-52
24. Konsoula R., and Barile F.A. Correlation of in vitro cytotoxicity with paracellular permeability in mortal rat intestinal cells. Journal of Pharmacological and Toxicological Methods 55 (2007) 176-183
25. Lapierre L.A. The molecular structure of the tight junction. Advanced Drug Delivery Reviews 41 (2000) 255-264
26. Le faouder J., Bichon E., Brunschwig P., Landelle R., Andre F., and Le Bizec B. Transfer assessment of fipronil residues from feed to cow milk. Talanta 73 (2007) 710-717
27. Ledirac N., Antherieu S., d'Uby A.D., Caron J.C., and Rahmani R. Effects of organochlorine insecticides on MAP kinase pathways in human HaCaT keratinocytes: key role of reactive oxygen species. Toxicological Sciences 86 (2005) 444-452
28. Lee R.B., and Urban J.P. Evidence for a negative Pasteur effect in articular cartilage. Biochemical Journal 321 Pt 1 (1997) 95-102
29. Li Q. New mechanism of organophosphorus pesticide-induced immunotoxicity. Journal of Nippon Medical School 74 (2007) 92-105
30. Liua D., Wang P., Zhu W., Gu X., Zhou W., and Zhou Z. Enantioselective degradation of fipronil in Chinese cabbage (Brassica pekinensis). Food Chemistry 110 (2008) 399-405
31. Maciel A.A., Oria R.B., Braga-Neto M.B., Braga A.B., Carvalho E.B., Lucena H.B., Brito G.A., Guerrant R.L., and Lima A.A. Role of retinol in protecting epithelial cell damage induced by Clostridium difficile toxin A. Toxicon 50 (2007) 1027-1040
32. McClain R.M. Mechanistic considerations for the relevance of animal data on thyroid neoplasia to human risk assessment. Mutation Research 333 (1995) 131-142
33. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. Journal of Immunological Methods 65 (1983) 55-63
34. Musser D.A., and Oseroff A.R. The use of tetrazolium salts to determine sites of damage to the mitochondrial electron transport chain in intact cells following in vitro photodynamic therapy with Photofrin II. Photochemistry and Photobiology 59 (1994) 621-626
35. Nigam S.K., Rodriguez-Boulan E., and Silver R.B. Changes in intracellular calcium during the development of epithelial polarity and junctions. Proceedings of the National Academy of Sciences of the United States of America 89 (1992) 6162-6166
36. Ohi M., Dalsenter P.R., Andrade A.J., and Nascimento A.J. Reproductive adverse effects of fipronil in Wistar rats. Toxicology Letters 146 (2004) 121-127
37. Ramond M.J., Martinot-Peignoux M., and Erlinger S. Dome formation in the human colon carcinoma cell line Caco-2 in culture. Influence of ouabain and permeable supports. Biology of the Cell 54 (1985) 89-92
38. Rees L.E., Cogan T.A., Dodson A.L., Birchall M.A., Bailey M., and Humphrey T.J. Campylobacter and IFNgamma interact to cause a rapid loss of epithelial barrier integrity. Inflammatory Bowel Diseases 14 (2008) 303-309
39. Rousset M. The human colon carcinoma cell lines HT-29 and Caco-2: two in vitro models for the study of intestinal differentiation. Biochimie 68 (1986) 1035-1040
40. Rusak T., Tomasiak M., and Ciborowski M. Peroxynitrite can affect platelet responses by inhibiting energy production. Acta Biochimica Polonica 53 (2006) 769-776
41. Sambuy Y., De Angelis I., Ranaldi G., Scarino M.L., Stammati A., and Zucco F. The Caco-2 cell line as a model of the intestinal barrier: influence of cell and culture-related factors on Caco-2 cell functional characteristics. Cell Biology and Toxicology 21 (2005) 1-26
42. Scudiero D.A., Shoemaker R.H., Paull K.D., Monks A., Tierney S., Nofziger T.H., Currens M.J., Seniff D., and Boyd M.R. Evaluation of a soluble tetrazolium/formazan assay for cell growth and drug sensitivity in culture using human and other tumor cell lines. Cancer Research 48 (1988) 4827-4833
43. Sharma R., Awasthi Y.C., Yang Y., Sharma A., Singhal S.S., and Awasthi S. Energy dependent transport of xenobiotics and its relevance to multidrug resistance. Current Cancer Drug Targets 3 (2003) 89-107
44. Skandrani D., Gaubin Y., Beau B., Murat J.C., Vincent C., and Croute F. Effect of selected insecticides on growth rate and stress protein expression in cultured human A549 and SH-SY5Y cells. Toxicology In Vitro 20 (2006) 1378-1386
45. Sprague L.A., and Nowell L.H. Comparison of pesticide concentrations in streams at low flow in six metropolitan areas of the United States. Environmental Toxicology and Chemistry 27 (2008) 288-298
46. Takahashi S., Abe T., Gotoh J., and Fukuuchi Y. Substrate-dependence of reduction of MTT: a tetrazolium dye differs in cultured astroglia and neurons. Neurochemistry International 40 (2002) 441-448
47. Tang J., Amin Usmani K., Hodgson E., and Rose R.L. In vitro metabolism of fipronil by human and rat cytochrome P450 and its interactions with testosterone and diazepam. Chemico-Biological Interactions 147 (2004) 319-329
48. Terada H. Uncouplers of oxidative phosphorylation. Environmental Health Perspectives 87 (1990) 213-218
49. Tingle C.C., Rother J.A., Dewhurst C.F., Lauer S., and King W.J. Fipronil: environmental fate, ecotoxicology, and human health concerns. Reviews of Environmental Contamination & Toxicology 176 (2003) 1-66
50. Tirelli V., Catone T., Turco L., Di Consiglio E., Testai L., and De Angelis I. Effects of the pesticide clorpyrifos on an in vitro model of intestinal barrier. Toxicology In Vitro 21 (2007) 308-313
51. Tomizawa M., Cowan A., and Casida J.E. Analgesic and toxic effects of neonicotinoid insecticides in mice. Toxicology and Applied Pharmacology 177 (2001) 77-83
52. Ulukaya E., Ozdikicioglu F., Oral A.Y., and Demirci M. The MTT assay yields a relatively lower result of growth inhibition than the ATP assay depending on the chemotherapeutic drugs tested. Toxicology In Vitro 22 (2008) 232-239
53. Unno N., Menconi M.J., Smith M., Hagen S.J., Brown D.A., Aguirre D.E., and Fink M.P. Acidic conditions ameliorate both adenosine triphosphate depletion and the development of hyperpermeability in cultured Caco-2BBe enterocytic monolayers subjected to metabolic inhibition. Surgery 121 (1997) 668-680
54. Vellonen K.S., Honkakoski P., and Urtti A. Substrates and inhibitors of efflux proteins interfere with the MTT assay in cells and may lead to underestimation of drug toxicity. European Journal of Pharmaceutical Sciences 23 (2004) 181-188
55. Williams Z.R., Goodman C.B., and Soliman K.F. Anaerobic glycolysis protection against 1-methyl-4-phenylpyridinium (MPP+) toxicity in C6 glioma cells. Neurochemical Research 32 (2007) 1071-1080
56. Winkler B.S., Sauer M.W., and Starnes C.A. Modulation of the Pasteur effect in retinal cells: implications for understanding compensatory metabolic mechanisms. Experimental Eye Research 76 (2003) 715-723
57. Xu L.C., Liu L., Ren X.M., Zhang M.R., Cong N., Xu A.Q., and Shao J.H. Evaluation of androgen receptor transcriptional activities of some pesticides in vitro. Toxicology 243 (2008) 59-65
58. Ye D., Ma I., and Ma T.Y. Molecular mechanism of tumor necrosis factor-alpha modulation of intestinal epithelial tight junction barrier. American Journal of Physiology - Gastrointestinal and Liver Physiology 290 (2006) G496-G504
59. Ying G.G., and Kookana R.S. Persistence and movement of fipronil termiticide with under-slab and trenching treatments. Environmental Toxicology and Chemistry 25 (2006) 2045-2050
60. Zhao X., Yeh J.Z., Salgado V.L., and Narahashi T. Fipronil is a potent open channel blocker of glutamate-activated chloride channels in cockroach neurons. The Journal of Pharmacology and Experimental Therapeutics 310 (2004) 192-201