Homologues of the human multidrug resistance genes MRP and MDR contribute to heavy metal resistance in the soil nematode Caenorhabditis elegans

EMBO Journal

Volumn 15, Issue 22, 1996, Pages 6132-6143

  Broeks, Annegien ^a   Gerrard, Bernard ^b   Allikmets, Rando ^b   Dean, Michael ^b   Plasterk, Ronald H A ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Arsenite; C. elegans; Cadmium; Multidrug resistance associated protein; P glycoprotein

Indexed keywords

ABC TRANSPORTER; ARSENIC TRIOXIDE; CADMIUM; GLYCOPROTEIN P; HEAVY METAL; TOXIN;

ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DETOXIFICATION; EMBRYO; GENE DELETION; GENE FUSION; INTESTINE CELL; MULTIDRUG RESISTANCE; MULTIGENE FAMILY; NONHUMAN; PHARYNX; PRIORITY JOURNAL; PROTEIN EXPRESSION; VULVA;

ANIMALIA; CAENORHABDITIS ELEGANS; MAMMALIA; NEMATODA;

EID: 0029910521     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb01001.x     Document Type: Article

References (79)

1. Al-Awqati, Q. (1995) Regulation of ion channels by ABC transporters that secrete ATP. Science, 269, 805-806.
2. Ammala, C., Moorhouse, A., Gribble, F., Ashfield, R., Proks, P., Smith, P.A., Sakura, H., Coles, B., Ahscroft, S.J.H. and Ashcroft, F. (1996) Promiscuous coupling between the sulfonylurea receptor and inwardly rectifying potassium channels. Nature, 379, 545-548.
3. Aposhian, H.V. and Aposhian, M.M. (1989) New developments in arsenic toxicity. J. Am. Coll. Toxicol., 8, 1273-1281.
4. Bakos, E., Hegedus, T., Hollo, Z., Welker, E., Tusnady, G.E., Varadi, A., Zaman, G.J.R., Scheper, R.J. and Sarkadi, B. (1996) Membrane topology and glycosylation of the human multidrug resistance associated protein (MRP). J. Biol. Chem., in press.
5. Blumemhal, T. (1995) Trans-splicing and polycistronic transcription in Caenorhabditis elegans. Trends Genet., 11, 132-136.
6. Borst, P. and Ouellette, M. (1995) New mechanisms of drug resistance in parasitic protozoa. Annu. Rev. Microbiol., 49, 427-460.
7. Broeks, A., Janssen, H.W.R.M., Calafat, J. and Plasterk, R.H.A. (1995) A P-glycoprotein protects Caenorhabditis elegans against natural toxins. EMBO J., 14, 1858-1866.
8. Burger, H., Nooter, K., Sonneveld, P., Van Wingerden, K.E., Zaman, G.J.R. and Stoter, G. (1994) High expression of the multidrug resistance-associated protein (MRP) in chronic- and prolymphocytic leukaemia. Br. J. Haematol., 88, 348-356.
9. Callahan, H.L., Roberts, W.L., Rainey, P.M. and Beverley, S.M. (1994) The pgpA gene of Leishmania major mediates antimony (SbIII) resistance by decreasing influx and not by increasing efflux. Mol. Biochem. Parasitol., 68, 145-149.
10. Cole, S.P.C. et al. (1992) Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science, 258, 1650-1654.
11. Cole, S.P.C., Sparks, K.E., Fraser, K., Loe, D.W., Grant, C.E., Wilson, G.M. and Deeley, R.G. (1994) Pharmacological characterization of multidrug resistant MRP-transfected human tumor cells. Cancer Res., 54, 5902-5910.
12. Dey, S., Papadopoulou, B., Roy, G., Grondin, K., Dou, D., Rosen, B.P. and Ouellette, M. (1994) High level arsenite resistance in Leishmania tarentolae is mediated by an active extrusion system. Mol. Biochem. Parasitol., 67, 49-57.
13. Dey, S., Ouellette, M., Lightbody, J., Papadopoulou, B. and Rosen, B.P. (1996) An ATP dependent As(III)-glutathione transport system in membrane vesicles of Leishmania tarentolae. Proc. Natl Acad. Sci. USA, 93, 2192-2197.
14. Engleman, D.M., Steitz, T.A. and Goldman, A. (1986) Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins. Annu. Rev. Biophys. Biophys. Chem., 15, 321-353.
15. Evers, R., Zaman, G.J.R., van Deemter, L., Jansen, H., Calafat, J., Oomen, L.J.C.M., Oude Elferink, R.P.J., Borst, P. and Schinkel, A.H. (1996) Basolateral localization and export activity of the human multidrug resistance-associated protein (MRP) in polarized pig kidney cells. J. Clin. Invest., 97, 1211-1218.
16. Fire, A. (1992) Histochemical techniques for locating Escherichia coli beta-galactosidase activity in transgenic organisms. Genet. Anal. Tech. Appl., 9, 151-158.
17. Fire, A., Harrison, S.W. and Dixon, D. (1990) A modular set of LacZ fusion vectors for studying gene expression in Caenorhabditis elegans. Gene, 93, 189-198.
18. Flens, M.J. et al. (1996) Tissue distribution of the multidrug resistance-associated protein (MRP). Am. J. Pathol., 148, 1237-1247.
19. Foote, S.J., Thompson, J.K., Cowman, A.F. and Kemp, D.J. (1989) Amplification of the multidrug resistance gene in some chloroquine-resistant isolates of Plasmodium falciparum. Cell. 57, 921-930.
20. Freedman, J.H., Slice, L.W., Dixon, D., Fire, A. and Rubin, C.S. (1993) The novel methallothionein genes of Caenorhabditis elegans, structural organization and inducible, cell-specific expression. J. Biol. Chem., 268, 2554-2564.
21. Gerrard, B., Stewart, C. and Dean, M. (1993) Analysis of Mdr50: a Drosophila P-glycoprotein multidrug resistance gene homolog. Genomics, 17, 83-88.
22. Gottesman, M.M. and Pastan, I. (1993) Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu. Rev. Biochem., 62, 385-427.
23. Grant, C.E., Valdimarsson, G., Hipfner, D.R., Almquist, K.C. Cole, S.P. and Deeley, R.G. (1994) Overexpression of multidrug resistance-associated protein (MRP) increases resistance to natural product drugs. Cancer Res., 54, 357-361.
24. Gros, P., Ben-Neriah, Y. Croop, J. and Housman, D.E. (1986) Isolation and expression of a complementary DNA that confers multidrug resistance. Nature, 323, 728-731.
25. Hardy, S.P., Goodfellow, H.R., Valverde, M.A., Gill, D.R., Sepulveda, V. and Higgins, C.F. (1995) Protein kinase C-mediated phosphorylation of the human multidrug resistance P-glycoprotein regulates cell volume-activated chloride channels. EMBO J., 14, 68-75. [Published corrigendum appears in EMBO J., 14. 1844 (1995).]
26. Higgins, C.F. (1992) ABC transporters, from microorganisms to man. Annu. Rev. Cell. Biol., 8, 67-113.
27. Hortensteiner, S., Vogt, E., Hagenbuch, B., Meier, P.J., Amrhein, N. and Martinoia, E. (1993) Direct energization of bile acid transport into plant vacuoles. J. Biol. Chem., 268, 18446-18449.
28. Jedlitschky, G., Leier, I., Bucholz, U., Center, M. and Keppler, D. (1994) ATP-dependent transport of glutathione S-conjugates by the multidrug resistance-associated protein. Cancer Res., 54, 4833-4836.
29. + channels and volume regulated anion channels in multidrug-resistant small cell lung cancer cells. Cancer Res., 53, 4156-4160.
30. Juliano, R.L. and Ling, V. (1976) A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim. Biophys. Acta, 455, 152-162.
31. Kartenbeck, J., Leuschner, U., Mayer, R. and Keppler, D. (1996) Absence of the canalicular isoform of the MRP gene encoded conjugate export pump from the hepatocytes in the Dubin Johnson syndrome. Hepathology, 23, 1061-1066.
32. Kramer, J.M., French, R.P., Park, E. and Johnson, J.J. (1990) The C.elegans rol-6 gene, which interacts with the sqt-1 g collagen gene to determine organismal morphology encodes a collagen. Mol. Cell. Biol., 10, 2018-2089.
33. Krause, M. (1995) Techniques for analyzing transcription and translation. In Epstein, H.F. and Shakes, D.C. (eds), Caenorhabditis elegans: Modern Biological Analysis of an Organism. Methods in Cell Biology, Volume 48. Academic Press, San Diego, CA, pp. 513-534.
34. Krause, M., Wild, M. Rosenzweig, B. and Hirsh, D. (1989) Wild-type and mutant actin genes in Caenorhabditis elegans. J. Mol. Biol., 208, 381-392.
35. Kyte, J. and Doolittle, R.F. (1982) A simple method for displaying the hydropathic character of a protein. J. Mol. Biol., 157, 105-132.
36. Leier, I., Jedlitschky, G., Buchholz, U., Cole, S.P.C., Deeley, R.G. and Keppler, D. (1994) The MRP gene encodes an ATP-dependent export pump for leukotriene C4 and structurally related conjugates. J. Biol. Chem., 269, 27807-27810.
37. Leonard, A. and Belgium, B. (1991) Arsenic. In Merian, E. (ed.), Metals and Their Compounds in the Environment. VCH, New York, pp. 751-773.
38. Lewis, J.A. and Fleming, J.T. (1995) Basic culture methods. In Epstein, H.F. and Shakes, D.C. (eds), Caenorhabditis elegans: Modern Biological Analysis of an Organism. Methods in Cell Biology, Volume 48. Academic Press, San Diego, CA, pp. 4-31.
39. Li, W. and Chou, I-N. (1992) Effects of sodium arsenite on the cytoskeleton and cellular glutathione levels in cultured cells. Toxicol. Appl. Pharmacol., 114, 132-139.
40. Lincke, C.R., The, I., van Groenigen, M. and Borst, P. (1992) The P-glycoprotein gene family of Caenorhabditis elegans cloning and characterization of genomic and complementary DNA sequences. J. Mol. Biol., 228, 701-711.
41. Lincke, C.R., Broeks, A., The, I., Plasterk, R.H.A. and Borst, P. (1993) The expression of two P-glycoprotein (pgp) genes in transgenic Caenorhabditis elegans is confined to intestinal cells. EMBO J., 12, 1615-1620.
42. - currents in NIH/3T3 cells. Am J. Physiol. 267, C650-C658.
43. Mayer, R., Kartenbeck, J., Büchler, M., Jedlitschky, G., Leier, I. and Keppler, D. (1995) Expression of the MRP gene-encoded conjugate export pump in liver and its selective absence from the canalicular membrane in transport-deficient mutant hepatocytes, J. Cell Biol., 131, 137-150.
44. Mello, C.C. Kramer, J.M., Stinchcomb, C. and Ambros, V. (1991) Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J., 10, 3959-3970.
45. Müller, M., Meijer, C., Zaman, G.J.R., Borst, P., Scheper, R.J., Mulder, N.H., De Vries, E.G.E. and Jansen, P.L.M. (1994) Overexpression of the multidrug resistance associated protein (MRP) gene results in increased ATP-dependent glutathione S-conjugale transport. Proc. Natl Acad. Sci. USA, 91, 13033-13037.
46. Ouellette, M. and Borst, P. (1991) Drug resistance and P-glycoprotein gene amplification in the protozoan parasite Leishmania. Res. Microbiol., 142, 737-746.
47. Ouellelte, M. and Papadopoulou, B. (1993) Mechanisms of drug resistance in Leishmania. Parasitol. Today, 9, 150-153.
48. Ouellette, M., Fase-Fowler, F. and Borst, P. (1990) The amplified H circle of methotrexate resistant Leishmania tarentolae contains a novel P-glycoprotein gene. EMBO J., 9, 1027-1033.
49. Papadopoulou, B., Roy, G., Dey, S., Rosen, B.P. and Ouellette, M. (1994) Contribution of the Leishmania P-glycoprotein related gene ltpgpA to oxyanion resistance. J. Biol. Chem., 269, 11980-11986.
50. Paulusma, C.C., Bosma, P.J., Zaman, G.J.R., Bakker, C.T.M., Otter, M., Scheffer, G.L., Scheper, R.J., Borst, P. and Oude Elferink, R.P.J. (1996) Congenital jaundice in rats with a mutation in a multidrug resistance-associated protein gene. Science, 271, 1126-1128.
51. Pettit, J. and Kingston, I.B. (1994) Developmentally regulated alternative splicing of a nematode type IV collagen gene. Dev. Biol., 161, 22-29.
52. Plasterk, R.H.A. (1995) Reverse genetics: from gene sequence to mutant worm. In Epstein, H.F. and Shakes, D.C. (eds), Caenorhabditis elegans; Modern Biological Analysis of an Organism. Methods in Cell Biology, Volume 48. Academic Press, San Diego, CA, pp. 59-80.
53. Popham, J.D. and Webster, J.M. (1979) Cadmium toxicity in the free living nematode C. elegans. Environ. Res., 20, 183-191.
54. Rosenquist, T.A. and Kimble, J. (1988) Molecular cloning and transcript analysis of fem-3, a sex determination gene in C.elegans. Genes Dev., 2, 606-616.
55. Samuelson, J., Ayala, P., Orozco, E. and Wirth, D. (1990) Emetine-resistant mutants of Entamoeba histolytica overexpress mRNAs for multidrug resistance. Mol. Biochem. Parasitol., 38, 281-290.
56. Schinkel, A.H. and Borst, P. (1991) Multidrug resistance mediated by P-glycoproteins. Semin. Cancer Biol., 2, 213-226.
57. Schinkel, A.H. et al. (1994) Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-rain barrier and to increased sensitivity to drugs. Cell, 77, 491-502.
58. Schwiebert, E.M., Egan, M.E., Hwang, T.H., Fulmer, S.B., Allen, S.S., Cutting, G.R. and Guggino, W.B. (1995) CFTR regulates outwardly rectifying chloride channels through an autocrine mechanism involving ATP. Cell, 81, 1063-1073.
59. Stringham, E. and Candido, P. (1994) Transgenic hsp16-lacZ strains of the soil nematode Caenorhabditis elegans as biological monitors of environmental stress. Environ. Toxicol. Chem., 13, 1211-1220.
60. Stutts, M.J., Canessa, C.M., Olsen, J.C., Hamrick, M., Cohn, J.A., Rossier, B.C. and Boucher, R.C. (1995) CFTR as a cAMP-dependent regulator of sodium channels. Science, 269, 847-850.
61. Sulston, J. and Hodgkin, J. (1988) Methods. In Wood, W.B. (ed.), The Nematode Caenorhabditis elegans. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 587-606.
62. Szczypka, M.S., Wemmie, J.A., Moye-Rowley, W.S. and Thiele, D.J. (1994) A yeast metal resistance protein similar to human cystic fibrosis transmembrane conductance regulator (CFTR) and multidrug resistance-associated protein. J. Biol. Chem., 269, 22853-22857.
63. Thiebaut, F., Tsuruo, T., Hamada, H., Gottesman, M.M., Pastan, I. and Willingham, M.C. (1987) Cellular localization of the multidrug resistance gene product in normal human tissues. Proc. Natl Acad. Sci. USA, 84, 7735-7738.
64. Thomas, G.A., Barrand, M.A., Stewart, S., Rabbitts, P.H., Williams, E.D. and Twentyman, P.R. (1994) Expression of the multidrug resistance-associated protein (MRP) gene in human lung tumours and normal tissue as determined by in situ hybridisation. Eur. J. Cancer, 30A, 1705-1709.
65. Tommasini, R., Evers, R., Vogt, E., Mornet, C., Zaman, G.J.R., Schinkel, A.H., Borst, P. and Martinoia, E. (1996) The human multidrug resistance-associated protein (MRP) functionally complements the yeast cadmium resistance factor (YCF1). Proc. Natl Acad. Sci. USA, in press.
66. Ueda, K., Cardarelli, C., Gottesman, M.M. and Pastan, I. (1987) Expression of a full-length cDNA for the human 'mdrI' gene confers resistance to colchicine, doxorubicin, and vinblastine. Proc. Natl Acad. Sci. USA, 84, 3004-3008.
67. Valverde, M.A., Diaz, M., Sepulveda, F.V., Gill, D.R., Hyde, S.C. and Higgens, C.F. (1992) Volume regulated channels associated with the human multidrug-resistance P-glycoprotein. Nature, 355, 830-833.
68. van der Valk, P. et al. (1990) Distribution of multidrug resistance-associated P-glycoprotein in normal and neoplastic human tissues. Ann. Oncol., 1, 56-64.
69. van Kuijck, M.A., van Aubel, R.A.M.H., Busch, A.E., Lang, F., Russel, F.G.M., Bindels, R.J.M., van Os, C.H. and Deen, P.M.T. (1996) Molecular cloning and expression of a cyclic AMP-activated chloride conductance regulator: a novel ATP-binding cassette transporter. Proc. Natl Acad. Sci. USA, in press.
70. Versantvoort, C.H.M., Broxterman, H.J., Bagrij, T., Scheper, R.J. and Twentyman, P.R. (1995) Regulation by glutathione of drug transport in multidrug-resistant human lung tumor cell lines overexpressing multidrug resistance-associated protein. Br. J. Cancer, 72, 82-89.
71. Wang, H-F. and Lee, T-C. (1993) Glutathione S-transferase π facilitates the excretion of arsenic from arsenic-resistant Chinese hamster ovary cells. Biochem. Biophys. Res. Commun., 192, 1093-1099.
72. Waterston, R.H. et al. (1993) The genome of the nematode Caenorhabditis elegans. Cold Spring Harbor Symp. Quant. Biol., 58, 367-376.
73. Wilson, C.W., Serrano, A.E., Wasley, A., Bogenschutz, M.P., Shankar, A.H. and Wirth, D.F. (1989) Amplification of a gene related to mammalian mdr genes in drug-resistant Plasmodium falciparum. Science, 244, 1184-1186.
74. Wilson, R. et al. (1994) 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature, 368, 32-38.
75. Wu, C.T., Budding, M., Griffin, M.S. and Croop, J.M. (1991) Isolation and characterization of Drosophila multidrug resistance gene homologs. Mol. Cell. Biol., 11, 3940-3948.
76. Zaman, G.J.R. et al. (1993) Analysis of the expression of MRP, the gene for a new putative transmembrane drug transporter, in human multidrug resistant lung cancer cell lines. Cancer Res., 53, 1747-1750.
77. Zaman, G.J.R. et al. (1994) The human multidrug resistance-associated protein MRP is a plasma membrane drug-efflux pump. Proc. Natl Acad. Sci. USA, 91, 8822-8826.
78. Zaman, G.J.R., Lankelma, J., van Tellingen, O., Beijnen, J., Dekker, H., Paulusma, C., Baas, F. and Borst, P. (1995) Role of glutathione in the export of compounds from cells by the multidrug-resistance-associated protein. Proc. Natl Acad. Sci. USA, 92, 7690-7694.
79. Zwaal, R.R., Broeks, A., van Meurs, J., Groenen, J.T. and Plasterk, R.H.A. (1993) Target-selected gene inactivation in Caenorhabditis elegans by using a frozen transposon insertion mutant bank. Proc. Natl Acad. Sci. USA. 90, 7431-7435.