Arsenic and antimony are toxic metalloids, naturally present in the environment and all organisms have developed pathways for their detoxification. The most effective metalloid tolerance systems in eukaryotes include downregulation of metalloid uptake, efflux out of the cell, and complexation with phytochelatin or glutathione followed by sequestration into the vacuole. Understanding of arsenic and antimony transport system is of high importance due to the increasing usage of arsenic-based drugs in the treatment of certain types of cancer and diseases caused by protozoan parasites as well as for the development of bio- and phytoremediation strategies for metalloid polluted areas. However, in contrast to prokaryotes, the knowledge about specific transporters of arsenic and antimony and the mechanisms of metalloid transport in eukaryotes has been very limited for a long time. Here, we review the recent advances in understanding of arsenic and antimony transport pathways in eukaryotes, including a dual role of aquaglyceroporins in uptake and efflux of metalloids, elucidation of arsenic transport mechanism by the yeast Acr3 transporter and its role in arsenic hyperaccumulation in ferns, identification of vacuolar transporters of arsenic-phytochelatin complexes in plants and forms of arsenic substrates recognized by mammalian ABC transporters.
References
[1]
Martinez, V.D.; Vucic, E.A.; Becker-Santos, D.D.; Gil, L.; Lam, W.L. Arsenic exposure and the induction of human cancers. J. Toxicol 2011, 2011, 431287.
Dilda, P.J.; Hogg, P.J. Arsenical-based cancer drugs. Cancer Treat. Rev 2007, 33, 542–564.
[4]
Frézard, F.; Demicheli, C. New delivery strategies for the old pentavalent antimonial drugs. Expert. Opin. Drug Deliv 2010, 7, 1343–1358.
[5]
Chappuis, F. Melarsoprol-free drug combinations for second-stage Gambian sleeping sickness: the way to go. Clin. Infect. Dis 2007, 45, 1443–1445.
[6]
Ali, W.; Isayenkov, S.V.; Zhao, F.J.; Maathuis, F.J. Arsenite transport in plants. Cell. Mol. Life Sci 2009, 66, 2329–2339.
[7]
Wysocki, R.; Tamás, M.J. How Saccharomyces cerevisiae copes with toxic metals and metalloids. FEMS Microbiol. Rev 2010, 34, 925–951.
[8]
Wysocki, R.; Tamás, M.J. Saccharomyces cerevisiae as a model organism for elucidating arsenic tolerance mechanisms. In Cellular Effects of Heavy Metals, 1st ed; Banfalvi, G., Ed.; Springer: Heidelberg, Germany, 2011; pp. 87–112.
[9]
Ramirez-Solis, A.; Mukopadhyay, R.; Rosen, B.P.; Stemmler, T.L. Experimental and theoretical characterization of arsenite in water: insights into the coordination environment of As-O. Inorg. Chem 2004, 43, 2954–2959.
[10]
Porquet, A.; Filella, M. Structural evidence of the similarity of Sb(OH)3 and As(OH)3 with glycerol: implications for their uptake. Chem. Res. Toxicol 2007, 20, 1269–1276.
[11]
Bienert, G.P.; Schüssler, M.D.; Jahn, T.P. Metalloids: essential, beneficial or toxic? Major intrinsic proteins sort it out. Trends Biochem. Sci 2007, 33, 20–26.
[12]
Bhattacharjee, H.; Mukhopadhyay, R.; Thiyagarajan, S.; Rosen, B.P. Aquaglyceroporins: ancient channels for metalloids. J. Biol 2008, 7, doi:10.1186/jbiol91.
[13]
Brochu, C.; Wang, J.; Roy, G.; Messier, N.; Wang, X.Y.; Saravia, N.G.; Ouellette, M. Antimony uptake systems in the protozoan parasite Leishmania and accumulation differences in antimony-resistant parasites. Antimicrob. Agents Chemother 2003, 47, 3073–3079.
[14]
Tschan, M.; Robinson, B.; Schulin, R. Antimony uptake by Zea mays (L.) and Helianthus annuus (L.) from nutrient solution. Environ. Geochem. Health 2008, 30, 187–191.
[15]
Persson, B.L.; Lagerstedt, J.O.; Pratt, J.R.; Pattison-Granberg, J.; Lundh, K.; Shokrollahzadeh, S.; Lundh, F. Regulation of phosphate acquisition in Saccharomyces cerevisiae. Curr. Genet 2003, 43, 225–244.
[16]
Bun-Ya, M.; Harashima, S.; Oshima, Y. Putative GTP-binding protein, Gtr1, associated with the function of the Pho84 inorganic phosphate transporter in Saccharomyces cerevisiae. Mol. Cell. Biol 1992, 12, 2958–2966.
[17]
Bun-ya, M.; Shikata, K.; Nakade, S.; Yompakdee, C.; Harashima, S.; Oshima, Y. Two new genes, PHO86 and PHO87, involved in inorganic phosphate uptake in Saccharomyces cerevisiae. Curr. Genet 1996, 29, 344–351.
[18]
Yompakdee, C.; Ogawa, N.; Harashima, S.; Oshima, Y.A. putative membrane protein, Pho88p, involved in inorganic phosphate transport in Saccharomyces cerevisiae. Mol. Gen. Genet 1996, 251, 580–590.
[19]
Meharg, A.A.; Macnair, M.R. An altered phosphate uptake system in arsenate tolerant Holcus lanatus. New Phytol 1990, 16, 29–35.
[20]
Meharg, A.A.; Macnair, M.R. Mechanisms of arsenate tolerance in Deschampsia cespitosa L. (Beauv.) and Agrostis capillaris L., adaptation of the arsenate uptake system. New Phytol 1991, 119, 291–297.
[21]
Abedin, M.J.; Cresser, M.S.; Meharg, A.A.; Feldmann, J.; Cotter-Howells, J. Arsenic accumulation and metabolism in rice (Oryza sativa L.). Environ. Sci. Technol 2002, 36, 962–968.
[22]
Shin, H.; Shin, H.S.; Dewbre, G.R.; Harrison, M.J. Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J 2004, 39, 629–642.
[23]
Gonzáles, E.; Solano, R.; Rubio, V.; Leyva, A.; Paz-Ares, J. PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1 is a plant-specific SEC12-related protein that enables the endoplasmic reticulum exit of a high-affinity phosphate transporter in Arabidopsis. Plant Cell 2005, 17, 3500–3512.
[24]
Wu, Z.; Ren, H.; McGrath, S.P.; Wu, P.; Zhao, F.J. Investigating the contribution of the phosphate transport pathway to arsenic accumulation in rice. Plant Physiol 2011, 157, 498–508.
[25]
Villa-Bellosta, R.; Sorribas, V. Arsenate transport by sodium phosphate cotransporter type IIb. Toxicol. Appl. Pharmacol 2010, 247, 36–40.
[26]
Beene, L.C.; Halluer, J.; Yoshinaga, M.; Hamdi, M.; Liu, Z. Pentavalent arsenate transport by zebrafish phosphate transporter NaPi-IIb1. Zebrafish 2011, 8, 125–131.
[27]
Sanders, O.I.; Rensing, C.; Kuroda, M.; Mitra, B.; Rosen, B.P. Antimonite is accumulated by the glycerol facilitator GlpF in Escherichia coli. J. Bacteriol 1997, 179, 3365–3367.
[28]
Wysocki, R.; Chéry, C.C.; Wawrzycka, D.; Van Hulle, M.; Cornelis, R.; Thevelein, J.M.; Tamás, M.J. The glycerol channel Fps1p mediates the uptake of arsenite and antimonite in Saccharomyces cerevisiae. Mol. Microbiol 2001, 40, 1391–1401.
[29]
Tamás, M.J.; Luyten, K.; Sutherland, F.C.; Hernandez, A.; Albertyn, J.; Valadi, H.; Li, H.; Prior, B.A.; Kilian, S.G.; Ramos, J.; et al. Fps1p controls the accumulation and release of the compatible solute glycerol in yeast osmoregulation. Mol. Microbiol 1999, 31, 1087–1104.
[30]
Thorsen, M.; Di, Y.; T?ngemo, C.; Morillas, M.; Ahmadpour, D.; van der Does, C.; Wagner, A.; Johansson, E.; Boman, J.; Posas, F.; et al. The MAPK Hog1p modulates Fps1p-dependent arsenite uptake and tolerance in yeast. Mol. Biol. Cell 2006, 17, 4400–4410.
[31]
Beese, S.E.; Negishi, T.; Levin, D.E. Identification of positive regulators of the yeast Fps1 glycerol channel. PLoS Genet 2009, 5, e1000738.
[32]
Bienert, G.P.; Thorsen, M.; Schüssler, M.D.; Nilsson, H.R.; Wagner, A.; Tamás, M.J.; Jahn, T.P. A subgroup of plant aquaporins facilitate the bidirectional diffusion of As(OH)3 and Sb(OH)3 across membranes. BMC Biol 2008, 6, 26.
[33]
Isayenkov, S.V.; Maathuis, F.J.M. The Arabidopsis thaliana aquaglyceroporin AtNIP7;1 is a pathway for arsenite uptake. FEBS Lett 2008, 582, 1625–1628.
[34]
Ma, J.F.; Yamaji, N.; Mitani, N.; Xu, X.Y.; Su, Y.H.; McGrath, S.P.; Zhao, F.J. Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc. Natl. Acad. Sci. USA 2008, 105, 9931–9935.
[35]
Maurel, C. Plant aquaporins: novel functions and regulation properties. FEBS Lett 2007, 581, 2227–2236.
[36]
Takano, J.; Wada, M.; Ludewig, U.; Schaaf, G.; von Wirén, N.; Fujiwara, T. The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell 2006, 18, 1498–1509.
[37]
Ma, J.F.; Tamai, K.; Yamaji, N.; Mitani, N.; Konishi, S.; Katsuhara, M.; Ishiguro, M.; Murata, Y.; Yano, M. A silicon transporter in rice. Nature 2006, 440, 688–691.
[38]
Kamiya, T.; Tanaka, M.; Mitani, N.; Ma, J.F.; Maeshima, M.; Fujiwara, T. NIP1;1, an aquaporin homolog, determines the arsenite sensitivity of Arabidopsis thaliana. J. Biol. Chem 2009, 284, 2114–2120.
Kamiya, T.; Fujiwara, T. Arabidopsis NIP1;1 transports antimonite and determines antimonite sensitivity. Plant Cell Physiol 2009, 50, 1977–1981.
[41]
Mosa, K.A.; Kumar, K.; Chhikara, S.; McDermott, J.; Liu, Z.; Musante, C.; White, J.C.; Dhankher, O.P. Members of rice plasma membrane intrinsic proteins subfamily are involved in arsenite permeability and tolerance in plants. Transgenic Res 2012, doi:10.1007/s11248-012-9600-8.
[42]
Gourbal, B.; Sonuc, N.; Bhattacharjee, H.; Legare, D.; Sundar, S.; Ouellette, M.; Rosen, B.P.; Mukhopadhyay, R. Drug uptake and modulation of drug resistance in Leishmania by an aquaglyceroporin. J. Biol. Chem 2004, 279, 31010–31017.
[43]
Marquis, N.; Gourbal, B.; Rosen, B.P.; Mukhopadhyay, R.; Ouellette, M. Modulation in aquaglyceroporin AQP1 gene transcript levels in drug-resistant Leishmania. Mol. Microbiol 2005, 57, 1690–1699.
[44]
Mandal, S.; Maharjan, M.; Singh, S.; Chatterjee, M.; Madhubala, R. Assessing aquaglyceroporin gene status and expression profile in antimony-susceptible and -resistant clinical isolates of Leishmania donovani from India. J. Antimicrob. Chemother 2010, 65, 496–507.
[45]
Ishibashi, K.; Hara, S.; Kondo, S. Aquaporin water channels in mammals. Clin. Exp. Nephrol 2009, 13, 107–117.
[46]
Liu, Z.; Shen, J.; Carbrey, J.M.; Mukhopadhyay, R.; Agre, P.; Rosen, B.P. Arsenite transport by mammalian aquaglyceroporins AQP7 and AQP9. Proc. Natl. Acad. Sci. USA 2002, 99, 6053–6058.
[47]
Liu, Z.; Carbrey, J.M.; Agre, P.; Rosen, B.P. Arsenic trioxide uptake by human and rat aquaglyceroporins. Biochem. Biophys. Res. Commun 2004, 316, 1178–1185.
[48]
Bhattacharjee, H.; Carbrey, J.; Rosen, B.P.; Mukhopadhyay, R. Drug uptake and pharmacological modulation of drug sensitivity in leukemia by AQP9. Biochem. Biophys. Res. Commun 2004, 322, 836–841.
[49]
Leung, J.; Pang, A.; Yuen, W.H.; Kwong, Y.L.; Tse, E.W. Relationship of expression of aquaglyceroporin 9 with arsenic uptake and sensitivity in leukemia cells. Blood 2007, 109, 740–746.
[50]
Lee, T.C.; Ho, I.C.; Lu, W.J.; Huang, J.D. Enhanced expression of multidrug resistance-associated protein 2 and reduced expression of aquaglyceroporin 3 in an arsenic-resistant human cell line. J. Biol. Chem 2006, 281, 18401–18407.
[51]
Calatayud, M.; Barrios, J.A.; Vélez, D.; Devesa, V. In vitro study of transporters involved in intestinal absorption of inorganic arsenic. Chem. Res. Toxicol 2012, 25, 446–453.
[52]
Hamdi, M.; Sanchez, M.A.; Beene, L.C.; Liu, Q.; Landfear, S.M.; Rosen, B.P.; Liu, Z. Arsenic transport by zebrafish aquaglyceroporins. BMC Mol. Biol 2009, 10, 104.
[53]
Liu, Z.; Styblo, M.; Rosen, B.P. Methylarsonous acid transport by aquaglyceroporins. Environ. Health Perspect 2006, 114, 527–531.
[54]
McDermott, J.R.; Jiang, X.; Beene, L.C.; Rosen, B.P.; Liu, Z. Pentavalent methylated arsenicals are substrates of human AQP9. Biometals 2010, 23, 119–127.
[55]
Liu, Z.; Boles, E.; Rosen, B.P. Arsenic trioxide uptake by hexose permeases in Saccharomyces cerevisiae. J. Biol. Chem 2004, 279, 17312–17318.
Jiang, X.; McDermott, J.R.; Ajees, A.A.; Rosen, B.P.; Liu, Z. Trivalent arsenicals and glucose use different translocation pathways in mammalian GLUT1. Metallomics 2010, 2, 211–219.
[58]
Drobná, Z.; Walton, F.S.; Paul, D.S.; Xing, W.; Thomas, D.J.; Styblo, M. Metabolism of arsenic in human liver: the role of membrane transporters. Arch. Toxicol 2010, 84, 3–16.
[59]
Lu, W.; Tamai, I.; Nezu, J.; Lai, M.; Huang, J. Organic anion transportin polypeptide-C mediates arsenic uptake in HEK-293 cells. J. Biomed. Sci 2006, 13, 525–353.
[60]
Hagenbuch, B.; Meier, P.J. Organic anion transporting polypeptides of the OATP/SLC21 family: phylogenetic classification as OATP/SLCO superfamily, new nomenclature and molecular/functional properties. Pflugers Arch 2004, 447, 653–665.
[61]
Mukhopadhyay, R.; Shi, J.; Rosen, B.P. Purification and characterization of Acr2p, the Saccharomyces cerevisiae arsenate reductase. J. Biol. Chem 2000, 275, 21149–21157.
[62]
Zhou, Y.; Messier, N.; Ouellette, M.; Rosen, B.P.; Mukhopadhyay, R. Leishmania major LmACR2 is a pentavalent antimony reductase that confers sensitivity to the drug pentostam. J. Biol. Chem 2004, 279, 37445–37451.
[63]
Ellis, D.R.; Gumaelius, L.; Indriolo, E.; Pickering, I.J.; Banks, J.A.; Salt, D.E. A novel arsenate reductase from the arsenic hyperaccumulating fern Pteris vittata. Plant Physiol 2006, 141, 1544–1554.
[64]
Duan, G.; Zhou, Y.; Tong, Y.P.; Mukhopadhyay, R.; Rosen, B.P.; Zhu, Y.G. A CDC25 homologue from rice functions as an arsenate reductase. New Phytol 2007, 174, 311–321.
[65]
Bhattacharjee, H.; Sheng, J.; Ajees, A.A.; Mukhopadhyay, R.; Rosen, B.P. Adventitious arsenate reductase activity of the catalytic domain of the human Cdc25B and Cdc25C phosphatases. Biochemistry 2010, 49, 802–809.
[66]
Yang, H.C.; Cheng, J.; Finan, T.M.; Rosen, B.P.; Bhattacharjee, H. Novel pathway for arsenic detoxification in the legume symbiont Sinorhizobium meliloti. J. Bacteriol 2005, 187, 6991–6997.
[67]
Zhao, F.J.; Ago, Y.; Mitani, N.; Li, R.Y.; Su, Y.H.; Yamaji, N.; McGrath, S.P.; Ma, J.F. The role of the rice aquaporin Lsi1 in arsenite efflux from roots. New Phytol 2010, 186, 392–399.
[68]
Maciaszczyk-Dziubinska, E.; Migdal, I.; Migocka, M.; Bocer, T.; Wysocki, R. The yeast aquaglyceroporin Fps1p is a bidirectional arsenite channel. FEBS Lett 2010, 584, 726–732.
[69]
Jacobson, T.; Thorsen, M.; Vooijs, R.; Schat, H.; Tamás, M.J. Yeast cells export glutathione as an extracellular defence mechanism. In FEBS J, Presented at 35th Congress of the Federation of European Biochemical Societies, Gothenburg, Sweden, 26 June–1 July, 2010; 2010; 277, p. 206.
[70]
Dhaoui, M.; Auchère, F.; Blaiseau, P.L.; Lesuisse, E.; Landoulsi, A.; Camadro, J.M.; Haguenauer-Tsapis, R.; Belgareh-Touzé, N. Gex1 is a yeast glutathione exchanger that interferes with pH and redox homeostasis. Mol. Biol. Cell 2011, 22, 2054–2067.
[71]
Thomas, D.J.; Li, J.; Waters, S.B.; Xing, W.; Adair, B.M.; Drobna, Z.; Devesa, V.; Styblo, M. Arsenic (+3 oxidation state) methyltransferase and methylation of arsenicals. Exp. Biol. Med 2007, 232, 3–11.
[72]
Carbrey, JM.; Song, L.; Zhou, Y.; Yoshinaga, M.; Rojek, A.; Wang, Y.; Liu, Y.; Lujan, H.L.; DiCarlo, S.E.; Nielsen, S.; et al. Reduced arsenic clearance and increased toxicity in aquaglyceroporin-9-null mice. Proc. Natl. Acad. Sci. USA 2009, 106, 15956–15960.
[73]
Rosen, B.P.; Tamás, M.J. Arsenic transport in prokaryotes and eukaryotic microbes. Adv. Exp. Med. Biol 2010, 679, 47–55.
[74]
Fu, H.L.; Meng, Y.; Ordó?ez, E.; Villadangos, A.F.; Bhattacharjee, H.; Gil, J.A.; Mateos, L.M.; Rosen, B.P. Properties of arsenite efflux permeases (Acr3) from Alkaliphilus metalliredigens and Corynebacterium glutamicum. J. Biol. Chem 2009, 284, 19887–19895.
[75]
Indriolo, E.; Na, G.; Ellis, D.; Salt, D.E.; Banks, J.A. A vacuolar arsenite transporter necessary for arsenic tolerance in the arsenic hyperaccumulating fern Pteris vittata is missing in flowering plants. Plant Cell 2010, 22, 2045–2057.
[76]
Wu, J.; Tisa, L.S.; Rosen, B.P. Membrane topology of the ArsB protein, the membrane subunit of an anion-translocating ATPase. J. Biol. Chem 1992, 267, 12570–12576.
[77]
Meng, Y.L.; Liu, Z.; Rosen, B.P. As(III) and Sb(III) uptake by GlpF and efflux by ArsB in Escherichia coli. J. Biol. Chem 2004, 279, 18334–18341.
[78]
Mansour, N.M.; Sawhney, M.; Tamang, D.G.; Vogl, C.; Saier, M.H., Jr. The bile/arsenite/riboflavin transporter (BART) superfamily. FEBS J 2007, 274, 612–629.
[79]
Bobrowicz, P.; Wysocki, R.; Owsianik, G.; Goffeau, A.; Ulaszewski, S. Isolation of three contiguous genes, ACR1, ACR2 and ACR3, involved in resistance to arsenic compounds in the yeast Saccharomyces cerevisiae. Yeast 1997, 13, 819–828.
[80]
Wysocki, R.; Bobrowicz, P.; Ulaszewski, S. The Saccharomyces cerevisiae ACR3 gene encodes a putative membrane protein involved in arsenite transport. J. Biol. Chem 1997, 272, 30061–30066.
[81]
Ghosh, M.; Shen, J.; Rosen, B.P. Pathways of As(III) detoxification in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 1999, 96, 5001–5006.
[82]
Maciaszczyk-Dziubinska, E.; Wawrzycka, D.; Sloma, E.; Migocka, M.; Wysocki, R. The yeast permease Acr3p is a dual arsenite and antimonite plasma membrane transporter. Biochim. Biophys. Acta 2010, 1798, 2170–2175.
[83]
Maciaszczyk-Dziubinska, E.; Migocka, M.; Wysocki, R. Acr3p is a plasma membrane antiporter that catalyzes As(III)/H+ and Sb(III)/H+ exchange in Saccharomyces cerevisiae. Biochim. Biophys. Acta 2011, 1808, 1855–1859.
[84]
Sato, T.; Kobayashi, Y. The ars operon in the skin element of Bacillus subtilis confers resistance to arsenate and arsenite. J. Bacteriol 1998, 180, 1655–1661.
[85]
Villadangos, A.F.; Fu, H.L.; Gil, J.A.; Messens, J.; Rosen, B.P.; Mateos, L.M. Efflux permease CgAcr3-1 of Corynebacterium glutamicum is an arsenite-specific antiporter. J. Biol. Chem 2012, 287, 723–735.
[86]
Maciaszczyk, E.; Wysocki, R.; Golik, P.; Lazowska, J.; Ulaszewski, S. Arsenical resistance genes in Saccharomyces douglasii and other yeast species undergo rapid evolution involving genomic rearrangements and duplications. FEMS Yeast Res 2004, 4, 821–832.
[87]
López-Maury, L.; Florencio, F.J.; Reyes, J.C. Arsenic sensing and resistance system in the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol 2003, 185, 5363–5371.
[88]
Xia, X.; Postis, V.L.; Rahman, M.; Wright, G.S.; Roach, P.C.; Deacon, S.E.; Ingram, J.C.; Henderson, P.J.; Findlay, J.B.; Phillips, S.E.; et al. Investigation of the structure and function of a Shewanella oneidensis arsenical-resistance family transporter. Mol. Membr. Biol 2008, 25, 691–705.
[89]
Aaltonen, E.K.; Silow, M. Transmembrane topology of the Acr3 family arsenite transporter from Bacillus subtilis. Biochim. Biophys. Acta 2008, 1778, 963–973.
[90]
Maciaszczyk-Dziubinska, E.; Wawrzycka, D.; Migocka, M.; Wysocki, R. Mutational analysis of the yeast As(III)/Sb(III) transporter Acr3; University of Wroc?aw: Wroc?aw, Poland. Unpublished work, 2012.
[91]
Wysocki, R.; Fortier, P.K.; Maciaszczyk, E.; Thorsen, M.; Leduc, A.; Odhagen, A.; Owsianik, G.; Ulaszewski, S.; Ramotar, D.; Tamás, M.J. Transcriptional activation of metalloid tolerance genes in Saccharomyces cerevisiae requires the AP-1-like proteins Yap1p and Yap8p. Mol. Biol. Cell 2004, 15, 2049–2060.
[92]
Di, Y.; Tamás, M.J. Regulation of the arsenic-responsive transcription factor Yap8p involves the ubiquitin-proteasome pathway. J. Cell Sci 2007, 120, 256–264.
[93]
Ilina, Y.; Sloma, E.; Maciaszczyk-Dziubinska, E.; Novotny, M.; Thorsen, M.; Wysocki, R.; Tamás, M.J. Characterization of the DNA binding motif of the arsenic-responsive transcription factor Yap8p. Biochem. J 2008, 415, 467–475.
[94]
Leslie, E.M. Arsenic-glutathione conjugate transport by the human multidrug resistance proteins (MRPs/ABCCs). J. Inorg. Biochem 2011, doi:10.1016/j.jinorgbio.2011.11.009.
Wawrzycka, D.; Sobczak, I.; Bartosz, G.; Bocer, T.; U?aszewski, S.; Goffeau, A. Vmr1p is a novel vacuolar multidrug resistance ABC transporter in Saccharomyces cerevisiae. FEMS Yeast Res 2010, 10, 828–838.
[98]
Paumi, C.M.; Chuk, M.; Snider, J.; Stagljar, I.; Michaelis, S. ABC transporters in Saccharomyces cerevisiae and their interactors: new technology advances the biology of the ABCC (MRP) subfamily. Microbiol. Mol. Biol. Rev 2009, 73, 577–593.
[99]
Vatamaniuk, O.K.; Bucher, E.A.; Ward, J.T.; Rea, P.A. Wormstake the phyto out of phytochelatins. Trends Biotechnol 2002, 20, 61–64.
[100]
Vatamaniuk, O.K.; Mari, S.; Lu, Y.P.; Rea, P.A. Mechanism of heavy metal ion activation of phytochelatin (PC) synthase: blocked thiols are sufficient for PC synthase-catalyzed transpeptidation of glutathione and related thiol peptides. J. Biol. Chem 2000, 275, 31451–31459.
[101]
Ortiz, D.F.; Ruscitti, T.; McCue, K.F.; Ow, D.W. Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. J. Biol. Chem 1995, 270, 4721–4728.
[102]
Prévéral, S.; Gayet, L.; Moldes, C.; Hoffmann, J.; Mounicou, S.; Gruet, A.; Reynaud, F.; Lobinski, R.; Verbavatz, J.M.; Vavasseur, A.; et al. A common highly conserved cadmium detoxification mechanism from bacteria to humans: heavy metal tolerance conferred by the ATP-binding cassette (ABC) transporter SpHMT1 requires glutathione but not metal-chelating phytochelatin peptides. J. Biol. Chem 2009, 284, 4936–4943.
[103]
Sooksa-Nguan, T.; Yakubov, B.; Kozlovskyy, V.I.; Barkume, C.M.; Howe, K.J.; Thannhauser, T.W.; Rutzke, M.A.; Hart, J.J.; Kochian, L.V.; Rea, P.A.; et al. Drosophila ABC transporter, DmHMT-1, confers tolerance to cadmium. DmHMT-1 and its yeast homolog, SpHMT-1, are not essential for vacuolar phytochelatin sequestration. J. Biol. Chem 2009, 284, 354–362.
[104]
Schwartz, M.S.; Benci, J.L.; Selote, D.S.; Sharma, A.K.; Chen, A.G.; Dang, H.; Fares, H.; Vatamaniuk, O.K. Detoxification of multiple heavy metals by a half-molecule ABC transporter, HMT-1, and coelomocytes of Caenorhabditis elegans. PLoS One 2010, 5, e9564.
[105]
Song, W.Y.; Park, J.; Mendoza-Cózatl, D.G.; Suter-Grotemeyer, M.; Shim, D.; H?rtensteiner, S.; Geisler, M.; Weder, B.; Rea, P.A.; Rentsch, D.; et al. Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters. Proc. Natl. Acad. Sci. USA 2010, 107, 21187–21192.
[106]
Mendoza-Cózatl, D.G.; Zhai, Z.; Jobe, T.O.; Akmakjian, G.Z.; Song, W.Y.; Limbo, O.; Russell, M.R.; Kozlovskyy, V.I.; Martinoia, E.; Vatamaniuk, O.K.; et al. Tonoplast-localized Abc2 transporter mediates phytochelatin accumulation in vacuoles and confers cadmium tolerance. J. Biol. Chem 2010, 285, 40416–40426.
[107]
Callahan, H.L.; Beverley, S.M. Heavy metal resistance: a new role for P-glycoproteins in Leishmania. Biol. Chem 1991, 266, 18427–18430.
[108]
Ouellette, M.; Legare, D.; Haimeur, A.; Grondin, K.; Roy, G.; Brochu, C.; Papadopoulou, B. ABC transporters in Leishmania and their role in drug resistance. Drug Resist Updat 1998, 1, 43–48.
[109]
Légaré, D.; Richard, D.; Mukhopadhyay, R.; Stierhof, Y.D.; Rosen, B.P.; Haimeur, A.; Papadopoulou, B.; Ouellette, M. The Leishmania ABC protein PGPA is an intracellular metal-thiol transporter ATPase. J. Biol. Chem 2001, 276, 26301–26307.
[110]
Coelho, A.C.; Beverley, S.M.; Cotrim, P.C. Functional genetic identification of PRP1, an ABC transporter superfamily member conferring pentamidine resistance in Leishmania major. Mol. Biochem. Parasitol 2003, 130, 83–90.
[111]
Coelho, A.C.; Yamashiro-Kanashiro, E.H.; Bastos, S.F.; Mortara, R.A.; Cotrim, P.C. Intracellular location of the ABC transporter PRP1 related to pentamidine resistance in Leishmania major. Mol. Biochem. Parasitol 2006, 150, 378–383.
[112]
Broeks, A.; Gerrard, B.; Allikmets, R.; Dean, M.; Plasterk, R.H. Homologues of the human multidrug resistance genes MRP and MDR contribute to heavy metal resistance in the soil nematode Caenorhabditis elegans. EMBO J 1996, 15, 6132–6143.
[113]
Long, Y.; Li, Q.; Wang, Y.; Cui, Z. MRP proteins as potential mediators of heavy metal resistance in zebrafish cells. Comp. Biochem. Physiol. C Toxicol. Pharmacol 2011, 153, 310–317.
[114]
Long, Y.; Li, Q.; Cui, Z. Molecular analysis and heavy metal detoxification of ABCC1/MRP1 in zebrafish. Mol. Biol. Rep 2011, 38, 1703–1711.
[115]
Chin, K.V.; Tanaka, S.; Darlington, G.; Pastan, I.; Gottesman, M.M. Heat shock and arsenite increase expression of the multidrug resistance (MDR1) gene in human renal carcinoma cells. J. Biol. Chem 1990, 265, 221–226.
[116]
Liu, J.; Chen, H.; Miller, D.S.; Saavedra, J.E.; Keefer, L.K.; Johnson, D.R.; Klaassen, C.D.; Waalkes, M.P. Overexpression of glutathione S-transferase II and multidrug resistance transport proteins is associated with acquired tolerance to inorganic arsenic. Mol. Pharmacol 2001, 60, 302–309.
[117]
Liu, J.; Liu, Y.; Powell, D.A.; Waalkes, M.P.; Klaassen, C.D. Multidrug-resistance mdr1a/1b double knockout mice are more sensitive than wild type mice to acute arsenic toxicity, with higher arsenic accumulation in tissues. Toxicology 2002, 170, 55–62.
[118]
Xie, Y.; Liu, J.; Liu, Y.; Klaassen, C.D.; Waalkes, M.P. Toxicokinetic and genomic analysis of chronic arsenic exposure in multidrug-resistance mdr1a/1b(-/-) double knockout mice. Mol. Cell. Biochem 2004, 255, 11–18.
[119]
Cole, S.P.; Sparks, K.E.; Fraser, K.; Loe, D.W.; Grant, C.E.; Wilson, G.M.; Deeley, R.G. Pharmacological characterization of multidrug resistant MRP-transfected human tumor cells. Cancer Res 1994, 54, 5902–5910.
[120]
Vernhet, L.; Courtois, A.; Allain, N.; Payen, L.; Anger, J.P.; Guillouzo, A.; Fardel, O. Overexpression of the multidrug resistance-associated protein (MRP1) in human heavy metal-selected tumor cells. FEBS Lett 1999, 443, 321–325.
[121]
Vernhet, L.; Allain, N.; Bardiau, C.; Anger, J.P.; Fardel, O. Differential sensitivities of MRP1-overexpressing lung tumor cells to cytotoxic metals. Toxicology 2000, 142, 127–134.
[122]
Vernhet, L.; Allain, N.; Payen, L.; Anger, J.P.; Guillouzo, A.; Fardel, O. Resistance of human multidrug resistance-associated protein 1-overexpressing lung tumor cells to the anticancer drug arsenic trioxide. Biochem. Pharmacol 2001, 6, 1387–1391.
[123]
Rappa, G.; Lorico, A.; Flavell, R.A.; Sartorelli, A.C. Evidence that the multidrug resistance protein (MRP) functions as a co-transporter of glutathione and natural product toxins. Cancer Res 1997, 57, 5232–5237.
[124]
Allen, J.D.; Brinkhuis, R.F.; van Deemter, L.; Wijnholds, J.; Schinkel, A.H. Extensive contribution of the multidrug transporters P-glycoprotein and Mrp1 to basal drug resistance. Cancer Res 2000, 60, 5761–5766.
[125]
Leslie, E.M.; Haimeur, A.; Waalkes, M.P. Arsenic transport by the human multidrug resistance protein 1 (MRP1/ABCC1). Evidence that a tri-glutathione conjugate is required. J. Biol. Chem 2004, 279, 32700–32708.
[126]
Carew, M.W.; Naranmandura, H.; Shukalek, C.B.; Le, X.C.; Leslie, E.M. Monomethylarsenic diglutathione transport by the human multidrug resistance protein 1 (MRP1/ABCC1). Drug Metab. Dispos 2011, 39, 2298–22304.
[127]
Kala, S.V.; Neely, M.W.; Kala, G.; Prater, C.I.; Atwood, D.W.; Rice, J.S.; Lieberman, M.W. The MRP2/cMOAT transporter and arsenic-glutathione complex formation are required for biliary excretion of arsenic. J. Biol. Chem 2000, 275, 33404–33408.
[128]
Carew, M.W.; Leslie, E.M. Selenium-dependent and -independent transport of arsenic by the human multidrug resistance protein 2 (MRP2/ABCC2): implications for the mutual detoxification of arsenic and selenium. Carcinogenesis 2010, 31, 1450–1455.
[129]
Duan, G.; Kamiya, T.; Ishikawa, S.; Arao, T.; Fujiwara, T. Expressing ScACR3 in rice enhanced arsenite efflux and reduced arsenic accumulation in rice grains. Plant Cell. Physiol 2012, 53, 154–163.
[130]
Guo, J.; Xu, W.; Ma, M. The assembly of metals chelation by thiols and vacuolar compartmentalization conferred increased tolerance to and accumulation of cadmium and arsenic in transgenic Arabidopsis thaliana. J. Hazard. Mater 2012, 199–200, 309–313.