RBE4 cells are highly resistant to paraquat-induced cytotoxicity: Studies on uptake and efflux mechanisms

Journal of Applied Toxicology

Volumn 34, Issue 9, 2014, Pages 1023-1030

  Vilas Boas, V ^a   Silva, R ^a   Guedes de Pinho, P ^a   Carvalho, F ^a   Bastos, M L ^a   Remiao F ^a  

^a UNIVERSITY OF PORTO   (Portugal)

Author keywords

Blood brain barrier; Choline uptake system; P glycoprotein; Paraquat; RBE4 cells

Indexed keywords

AMINO ACID; ARGININE; ELACRIDAR; HEMICHOLINIUM 3; MULTIDRUG RESISTANCE PROTEIN; PARAQUAT; POLYAMINE; PUTRESCINE; VALINE; CHOLINE; HERBICIDE;

AMINO ACID TRANSPORT; ANIMAL CELL; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CAPILLARY ENDOTHELIAL CELL; CELL MEMBRANE TRANSPORT; CELL VIABILITY; CHOLINE UPTAKE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; FLOW CYTOMETRY; MEMBRANE MODEL; NONHUMAN; PRIORITY JOURNAL; RAT; ANIMAL; CELL LINE; CYTOLOGY; DRUG EFFECTS; ENDOTHELIUM CELL; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

RATTUS;

ANIMALS; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; CELL LINE; CHOLINE; ENDOTHELIAL CELLS; HERBICIDES; P-GLYCOPROTEIN; PARAQUAT; RATS;

EID: 84905042449     PISSN: 0260437X     EISSN: 10991263     Source Type: Journal    
DOI: 10.1002/jat.2926     Document Type: Article

References (41)

1. Almog C, Tal E. 1967. Death from paraquat after subcutaneous injection. Br. Med. J. 3: 721.
2. Bartlett RM, Holden JE, Nickles RJ, Murali D, Barbee DL, Barnhart TE, Christian BT, DeJesus OT. 2009. Paraquat is excluded by the blood brain barrier in rhesus macaque: An in vivo pet study. Brain Res. 1259: 74-79. DOI: 10.1016/j.brainres.2008.12.033
3. Begley DJ, Lechardeur D, Chen ZD, Rollinson C, Bardoul M, Roux F, Scherman D, Abbott NJ. 1996. Functional expression of p-glycoprotein in an immortalised cell line of rat brain endothelial cells, rbe4. J. Neurochem. 67: 988-995.
4. Bernas T, Dobrucki J. 2002. Mitochondrial and nonmitochondrial reduction of mtt: Interaction of mtt with tmre, jc-1, and nao mitochondrial fluorescent probes. Cytometry 47: 236-242.
5. Corasaniti MT, Defilippo R, Rodino P, Nappi G, Nistico G. 1991. Evidence that paraquat is able to cross the blood-brain barrier to a different extent in rats of various age. Funct. Neurol. 6: 385-391.
6. Cordon-Cardo C, O'Brien JP, Casals D, Rittman-Grauer L, Biedler JL, Melamed MR, Bertino JR. 1989. Multidrug-resistance gene (p-glycoprotein) is expressed by endothelial cells at blood-brain barrier sites. Proc. Natl. Acad. Sci. U. S. A. 86: 695-698.
7. Degorter MK, Xia CQ, Yang JJ, Kim RB. 2012. Drug transporters in drug efficacy and toxicity. Annu. Rev. Pharmacol. Toxicol. 52: 249-273. DOI: 10.1146/annurev-pharmtox-010611-134529
8. Dinis-Oliveira RJ, Remiao F, Duarte JA, Ferreira R, Sanchez Navarro A, Bastos ML, Carvalho F. 2006a. P-glycoprotein induction: An antidotal pathway for paraquat-induced lung toxicity. Free Radic. Biol. Med. 41: 1213-1224. DOI: 10.1016/j.freeradbiomed.2006.06.012
9. Dinis-Oliveira RJ, Remiao F, Carmo H, Duarte JA, Navarro AS, Bastos ML, Carvalho F. 2006b. Paraquat exposure as an etiological factor of parkinson's disease. Neurotoxicology 27: 1110-1122. DOI: 10.1016/j.neuro.2006.05.012
10. Fei Q, McCormack AL, Di Monte DA, Ethell DW. 2008. Paraquat neurotoxicity is mediated by a bak-dependent mechanism. J. Biol. Chem. 283: 3357-3364. DOI: 10.1074/jbc.M708451200
11. Friedrich A, George RL, Bridges CC, Prasad PD, Ganapathy V. 2001. Transport of choline and its relationship to the expression of the organic cation transporters in a rat brain microvessel endothelial cell line (rbe4). Biochim. Biophys. Acta 1512: 299-307.
12. Fujimori K, Fukuhara A, Inui T, Allhorn M. 2012. Prevention of paraquat-induced apoptosis in human neuronal sh-sy5y cells by lipocalin-type prostaglandin d synthase. J. Neurochem. 120: 279-291. DOI: 10.1111/j.1471-4159.2011.07570.x
13. Fukushima T, Tanaka K, Lim H, Moriyama M. 2002. Mechanism of cytotoxicity of paraquat. Environ. Health Prev. Med. 7(3): 89-94. DOI: 10.1265/ehpm.2002.89
14. Grabie V, Scemama JL, Robertson JB, Seidel ER. 1993. Paraquat uptake in the cultured gastrointestinal epithelial cell line, iec-6. Toxicol. Appl. Pharmacol. 122: 95-100. DOI: 10.1006/taap.1993.1176
15. Hargreaves KM, Pardridge WM. 1988. Neutral amino acid transport at the human blood-brain barrier. J. Biol. Chem. 263: 19392-19397.
16. Hsu HH, Chang CT, Lin JL. 2003. Intravenous paraquat poisoning-induced multiple organ failure and fatality--a report of two cases. J. Toxicol. Clin. Toxicol. 41: 87-90.
17. Janda E, Parafati M, Aprigliano S, Carresi C, Visalli V, Sacco I, Ventrice D, Mega T, Vadala N, Rinaldi S, Musolino V, Palma E, Gratteri S, Rotiroti D, Mollace V. 2013. The antidote effect of quinone oxidoreductase 2 inhibitor against paraquat-induced toxicity in vitro and in vivo. Br. J. Pharmacol. 168: 46-59. DOI: 10.1111/j.1476-5381.2012.01870.x
18. Lagrange P, Romero IA, Minn A, Revest PA. 1999. Transendothelial permeability changes induced by free radicals in an in vitro model of the blood-brain barrier. Free Radic. Biol. Med. 27: 667-672.
19. Liou HH, Tsai MC, Chen CJ, Jeng JS, Chang YC, Chen SY, Chen RC. 1997. Environmental risk factors and parkinson's disease: A case-control study in taiwan. Neurology 48: 1583-1588.
20. McCormack AL, Atienza JG, Johnston LC, Andersen JK, Vu S, Di Monte DA. 2005. Role of oxidative stress in paraquat-induced dopaminergic cell degeneration. J. Neurochem. 93: 1030-1037. DOI: 10.1111/j.1471-4159.2005.03088.x
21. Moreira PN, de Pinho PG, Baltazar MT, Bastos ML, Carvalho F, Dinis-Oliveira RJ. 2012. Quantification of paraquat in postmortem samples by gas chromatography-ion trap mass spectrometry and review of the literature. Biomed. Chromatogr. 26: 338-349. DOI: 10.1002/bmc.1663
22. Nagao M, Saitoh H, Zhang WD, Iseki K, Yamada Y, Takatori T, Miyazaki K. 1993. Transport characteristics of paraquat across rat intestinal brush-border membrane. Arch. Toxicol. 67: 262-267.
23. Naylor JL, Widdowson PS, Simpson MG, Farnworth M, Ellis MK, Lock EA. 1995. Further evidence that the blood/brain barrier impedes paraquat entry into the brain. Hum. Exp. Toxicol. 14: 587-594.
24. Ortiz-Ortiz MA, Moran JM, Ruiz-Mesa LM, Bonmatty RG, Fuentes JM. 2011. Protective effect of the glial cell line-derived neurotrophic factor (gdnf) on human mesencephalic neuron-derived cells against neurotoxicity induced by paraquat. Environ. Toxicol. Pharmacol. 31: 129-136. DOI: 10.1016/j.etap.2010.09.013
25. Rannels DE, Pegg AE, Clark RS, Addison JL. 1985. Interaction of paraquat and amine uptake by rat lungs perfused in situ. Am. J. Physiol. 249: E506-E513.
26. Rojo AI, Cavada C, de Sagarra MR, Cuadrado A. 2007. Chronic inhalation of rotenone or paraquat does not induce parkinson's disease symptoms in mice or rats. Exp. Neurol. 208: 120-126. DOI: 10.1016/j.expneurol.2007.07.022
27. Roux F, Couraud PO. 2005. Rat brain endothelial cell lines for the study of blood-brain barrier permeability and transport functions. Cell. Mol. Neurobiol. 25: 41-58.
28. Roux F, Durieu-Trautmann O, Chaverot N, Claire M, Mailly P, Bourre JM, Strosberg AD, Couraud PO. 1994. Regulation of gamma-glutamyl transpeptidase and alkaline phosphatase activities in immortalized rat brain microvessel endothelial cells. J. Cell. Physiol. 159: 101-113. DOI: 10.1002/jcp.1041590114
29. Russell LA, Stone BE, Rooney PA. 1981. Paraquat poisoning: Toxicologic and pathologic findings in three fatal cases. Clin. Toxicol. 18: 915-928. DOI: 10.3109/15563658108990319
30. Samai M, Hague T, Naughton DP, Gard PR, Chatterjee PK. 2008. Reduction of paraquat-induced renal cytotoxicity by manganese and copper complexes of egta and ehpg. Free Radic. Biol. Med. 44: 711-721. DOI: 10.1016/j.freeradbiomed.2007.11.001
31. Shimizu K, Ohtaki K, Matsubara K, Aoyama K, Uezono T, Saito O, Suno M, Ogawa K, Hayase N, Kimura K, Shiono H. 2001. Carrier-mediated processes in blood--brain barrier penetration and neural uptake of paraquat. Brain Res. 906: 135-142.
32. Shin WW, Fong WF, Pang SF, Wong PC. 1985. Limited blood-brain barrier transport of polyamines. J. Neurochem. 44: 1056-1059.
33. Silva R, Carmo H, Dinis-Oliveira R, Cordeiro-da-Silva A, Lima SC, Carvalho F, Bastos Mde L, Remiao F. 2011. In vitro study of p-glycoprotein induction as an antidotal pathway to prevent cytotoxicity in caco-2 cells. Arch. Toxicol. 85: 315-326. DOI: 10.1007/s00204-010-0587-8
34. Silva R, Carmo H, Vilas-Boas V, de Pinho PG, Dinis-Oliveira RJ, Carvalho F, Silva I, Correia-de-Sa P, Bastos MdL, Remiao F. 2013. Doxorubicin decreases paraquat accumulation and toxicity in caco-2 cells. Toxicol. Lett. 217: 34-41.
35. Smith LL. 1982. Young scientists award lecture 1981: The identification of an accumulation system for diamines and polyamines into the lung and its relevance to paraquat toxicity. Arch. Toxicol. Suppl. 5: 1-14.
36. Soloukides A, Moutzouris DA, Kassimatis T, Metaxatos G, Hadjiconstantinou V. 2007. A fatal case of paraquat poisoning following minimal dermal exposure. Ren. Fail. 29: 375-377. DOI: 10.1080/08860220601184134
37. de Tezanos Pinto F, Corradi GR, de la Hera DP, Adamo HP. 2012. Cho cells expressing the human p(5)-atpase atp13a2 are more sensitive to the toxic effects of herbicide paraquat. Neurochem. Int. 60: 243-248. DOI:10.1016/j.neuint.2012.01.002
38. Vilas-Boas V, Silva R, Gaio AR, Martins AM, Lima SC, Cordeiro-da-Silva A, de Lourdes Bastos M, Remiao F. 2011. P-glycoprotein activity in human caucasian male lymphocytes does not follow its increased expression during aging. Cytometry A 79: 912-919. DOI: 10.1002/cyto.a.21135
39. Vilas-Boas V, Silva R, Nunes C, Reis S, Ferreira L, Vieira C, Carvalho F, Bastos MD, Remiao F. 2013. Mechanisms of p-gp inhibition and effects on membrane fluidity of a new rifampicin derivative, 1, 8-dibenzoyl-rifampicin. Toxicol. Lett. DOI: 10.1016/j.toxlet.2013.05.005
40. Widdowson PS, Farnworth MJ, Simpson MG, Lock EA. 1996. Influence of age on the passage of paraquat through the blood-brain barrier in rats: A distribution and pathological examination. Hum. Exp. Toxicol. 15: 231-236.
41. Zerin T, Kim YS, Hong SY, Song HY. 2012. Protective effect of methylprednisolone on paraquat-induced a549 cell cytotoxicity via induction of efflux transporter, p-glycoprotein expression. Toxicol. Lett. 208: 101-107. DOI: 10.1016/j.toxlet.2011.10.019