Role of the sodium-dependent phosphate cotransporters and absorptive endocytosis in the uptake of low concentrations of uranium and its toxicity at higher concentrations in LLC-PK1 cells

Toxicological Sciences

Volumn 101, Issue 2, 2008, Pages 254-262

  Muller, Dany S ^a,d   Houpert, Pascale ^a   Cambar, Jean ^b   Hengé Napoli, Marie Hélène ^c  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE IRSN   (France)

^b LSTE EA 3672   (France)

^c CEA DEN Valrhô Dir CVAR   (France)

^d KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Endocytosis; LLC PK1; MDCK; Phosphonoformic acid; Uranium cytotoxicity; Uranium uptake

Indexed keywords

CHLORPROMAZINE; COLCHICINE; CYTOCHALASIN D; FOSCARNET; MEGLUMINE; PHORBOL 13 ACETATE 12 MYRISTATE; RADIOISOTOPE; SODIUM ION; SODIUM PHOSPHATE COTRANSPORTER 2A; UNCLASSIFIED DRUG; URANIUM; URANIUM 233;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL STIMULATION; CELL STRAIN; CELL TRANSPORT; COMPETITIVE INHIBITION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; ENDOCYTOSIS; KIDNEY CELL; NEPHROTOXICITY; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN EXPRESSION; PROTEIN FUNCTION; SODIUM CELL LEVEL; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; BIOLOGICAL TRANSPORT; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCYTOSIS; FOSCARNET; KINETICS; LLC-PK1 CELLS; MICROSCOPY, ELECTRON, TRANSMISSION; SODIUM-PHOSPHATE COTRANSPORTER PROTEINS, TYPE IIA; SWINE; URANYL NITRATE;

EID: 38349116041     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfm266     Document Type: Article

References (40)

1. Becker, D., Lempertz, U., Enk, A., Saloga, J., and Knop, L (1995). Contact sensitizers modulate mechanisms of receptor-mediated endocytosis but not fluid-phase endocytosis in murine epidermal Langerhans cells. Exp. Dermatol. 4, 211-217.
2. Brady, H. R., Kone,.B. C., Brenner, R. K, and Gultans, S. R. (1989). Early effects of uranyl nitrate on respiration and K+ transport in rabbit proximal tubule, Kidney Int. 36, 27-34.
3. Bulger, R. E. (1986). Renal damage caused by heavy metals. Toxicol. Pathol. 14, 58-65.
4. Carrière, M., Avoscan, L., Collins, R., Carrot, F., Khodja, H., Ansoborlo, E., and Gouget, B. (2004). Influence of uranium speciation on normal rat kidey (NRK-52E) proximal cell cytotoxicity. Chem. Res. Toxicol. 17, 446-452.
5. Carrière, M., Thiebault, C., Milgram, S., Avoscan, L., Proux, O., and Gouget, B. (2006). Citrate does not change uranium chemical speciation in cell culture medium but increases its toxicity and accumulation in NRK-52E cells. Chem. Res. Toxicol. 19, 1637-1642.
6. Chow, C. W., Khurana, S., Woodside, M., Grinstein, S., and Orlowski, J. (1999). The epithelial Na(+)/H(+) exchanger, NHE3, is internalized through a clathrin-mediated pathway. J. Biol. Chem. 274, 37551-37558.
7. Collazo, R., Fan, L., Hu, M. C., Zhao, H., Wiederkehr, M. R., and Moe, O. W. (2000). Acute regulation of Na+/H+ exchanger NHE3 by parathyroid hormone via NHE3 phosphorylation and dynamin-dependent endocytosis. J. Biol. Chem. 275, 31601-31608.
8. Galle, P. (1974). Role des lysosomes et des mitochondries dans les phenomenes de concentration et d'elimination d'elements mineraux (uranium et or) par le rein. J. Microscopiel 19, 17-24.
9. Gekle, M., Mildenberger, S., Freudinger, R., Schwerdt G., and Silbemagl, S.(1997). Albumin endocytosis in OK cells: Dependence on actin and microtubules and regulation by protein kinases. Am. J. Physiol. 272, F668-F677.
10. Ghadially, F. N., Lalonde, J. M., and Yang-Steppuhn, S. (1982). Uraniosomes produced in cultured rabbit kidney cells by uranyl acetate. Virchows Arch., B, Cell Pathol. 39, 21-30.
11. Goel, K. A., Garg, V. K., and Garg, V. (1980). Histopathology of kidney of albino rat poisoned with utranyl nitrate. Bull. Environ. Contam. Toxicol. 24, 9-12.
12. Goldman, M., Yaari, A., Doshnitzki Z., Cohen-Luria, R., and Moran, A. (2006). Nephrotoxicity of uranyl acetate: Effect on rat kidney brush border membrane vesicles. Arch. Toxicol. 80, 387-393.
13. Haley, D. P. (1982). Morphologic changes in uranyl nitrate-induced acute renal failure in saline- and water-drinking rats. Lab. Invest. 46, 196-208.
14. Henge-Napoli M. H., Ansoborlo, E., Chazel, V., Houpert, P., Paquet, F., and Gourmelon, P. (1999). Efficacy of ethane-1-hydroxy-1,1-bisphosphonate (EHBP) for the decorporation of uranium after intramuscular contamination in rats. Int. J. Radiat. Biol. 75, 1473-1477.
15. Hernando, N., Karim-Jimenez, Z., Biber J and Murer, H. (2001). Molecular determinants for apical expression and regulatory membrane retrieval of the type IIa Na/Pi cotransporter. Kidney Int. 60, 431-435.
16. Heuser, J. E., and Anderson, R. G. (1989). Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J. Cell Biol. 108, 389-400.
17. Hryciw, D. H., Pollock, C. A., and Poronnik, P. (2005). PKC-alpha-mediated remodeling of the actin cytoskeleton is involved in constitutive albumin uptake by proximal tubule cells. Am. J. Physiol. Renal Physiol. 288, F1227-F1235.
18. Kobayashi, S., Nagase, M., Honda, N., and Hishida, A. (1984). Glomerular alterations in uranyl acetate-induced acute renal failure in rabbits. Kidney Int. 26, 808-815.
19. Kurttio, P., Auvinen, A., Salonen, L., Saha, H., Pekkanen, J., Makelainen, I., Vaisanon, S. B., Penttila, I. M., and Komulainen, H. (2002). Renal effects of uranium in drinking water. Environ. Health Perspect. 110, 337-342.
20. Kurttio, P., Harmoinen, A., Saha, H., Salonen, L., Karpas, Z., Komulainen, H., and Auvinon, A. (2006). Kidney toxicity of ingested uranium from drinking water. Am. J. Kidney Dis. 47, 972-982.
21. L'Azou, B., Henge-Napoli, M. H., Minaro, L., Mirto, H., Barrouillet, M. P., and Camber, J. (2002). Effects of cadmium and uranium on some in vitro renal targets. Cell Biol. Toxicol. 18, 329-340.
22. Legget, R. W. (1989). The behavior and chemical toxicity of U in the kidney: A reassessment. Health Phys. 57, 365-383.
23. Legrand, C., Bour, J. M., Jacob, C., Capiaumont, J., Martial, A., Marc, A., Wudtke, M., Kretzmer, G., Demangel, C., and Duval, D. (1992). Lactate dehydrogenase (LDH) activity of the cultured eukaryotic cells as marker of the number of dead cells in the medium. J. Biotechnol. 25, 231-243.
24. Lopez, R., Diaz Sylvester, P. L., Ubios, A. M., and Cabrini, R. L. (2000). Percutaneous toxicity of uranyl nitrate: Its effect in terms of exposure area and time. Health Phys. 78, 434-437.
25. Mamdouh, Z., Giocondi, M. C., Laprade, R., and Le, G. C. (1996). Temperature dependence of endocytosis in renal epithelial cells in culture. Biochim. Biophys. Acta 1282, 171-173.
26. Mao, Y., Desmeules, M., Schaubel, D., Berube, D., Dyck, R., Brule, D., and Thomas, B. (1995). Inorganic components of drinking water and micro-albuminuria. Environ. Res. 71, 135-140.
27. McDonald-Taylor, C. K., Singh, A., and Gilman, A. (1997). Uranyl nitrate-induced proximal tubule alterations in rabbits: A quantitative analysis. Toxicol. Pathol. 25, 381-389.
28. Miller, A. C., Stewart, M., Brooks, K., Shi, L., and Page, N. (2002). Depleted uranium-catalyzed oxidative DNA damage: Absence of significant alpha particle decay. J. Inorg. Biochem. 91, 246-252.
29. Mirto,, H., Barrouillet, M. P., Henge-Napoli, M. H., Ansoborlo, E., Fournier, M., and Cambar, J. (1999a). Influence of uranium(VI) speciation for the evaluation of in vitro uranium cytotoxicity on LLC-PK1 cells. Hum. Exp. Toxicol. 18, 180-187.
30. Mirto, H., Henge-Napoli, M. H., Gibert, R., Ansoborlo, E., Fournier, M., and Cambar, J. (1999b). Intracellular behaviour of uranium(VI) on renal epithelial cell in culture (LLC-PK1): Influence of uranium speciation. Toxicol. Lett. 104, 249-256.
31. Moss, M. A., McCurdy, R. F., Dooley, K. C., Givner, M. L., Dymond, L. C., Slayter, J. M., and Courneya, M. M. (1983). Uranium in drinking water - report on clinical studies in Nova Scotia. In Chemical Toxicology and Clinical Chemistry of Metals (S. S. Brown and J. Savory, Eds.), pp. 149-152. Academic Press, London.
32. Muller, D., Houpert, P., Cambar, J., and Henge-Napoli, M. H. (2006). Role of the sodium-dependent phosphate co-transporters and of the phosphate complexes of uranyl in the cytotoxicity of uranium in LLC-PK1 cells. Toxicol. Appl. Pharmacol. 214, 166-177.
33. Murer, H., and Biber, J. (1996). Molecular mechanism of renal apical Na/ phosphate cotransport. Annu. Rev. Physiol. 58, 607-618.
34. Quabius, E. S., Murer, H., and Biber, J. (1996). Expression of proximal tubular Na-Pi and Na-SO4 cotransporters in MDCK and LLC-PK1 cells by transfection. Am. J. Physiol. 270, F220-F228.
35. Sano, K., Fujigaki, Y., Ikegaya, N., Ohishi, K., Yonemura, K., and Hishida, A. (1998). The roles of apoptosis in uranyl acetate-induced acute renal failure. Ren. Fail. 20, 697-701.
36. Shimkets, R. A., Lifton, R. P., and Canessa, C. M. (1997). The activity of the epithelial sodium channel is regulated by clathrin-mediated endocytosis. J. Biol. Chem. 272, 25537-25541.
37. Taulan, M., Pauqet, F., Argiles, A., Demaille, J., and Romey, M. C. (2006). Comprehensive analysis of the renal transcriptional response to acute uranyl nitrate exposure. BMC Genomics 7, 2.
38. Taulan, M., Paquet, F., Maubeit, C., Delissen, O., Demaille, J., and Romey, M. C. (2004). Renal toxicogenomic response to chronic uranyl nitrate insult in mice. Environ. Health Perspect. 112, 1628-1635.
39. Tyrakowski, T. (1979). Disturbances in electrolyte transport in UO2++ ion intoxication - Model studies on the preliminary stage of toxic acute renal failure. III. Disturbances in Na+ and K+ ion excretion and decrease in glomerular filtration rate following uranyl acetate intoxication. Acta Med. Pol. 20, 317-329.
40. Zamora, M. L., Tracy, B. L., Zielinski, J. M., Meyerhof, D. P., and Moss, M. A. (1998). Chronic ingestion of uranium in drinking water: A study of kidney bioeffects in humans. Toxicol. Sci. 43, 68-77.