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Toxicometallomics of Cadmium, Manganese and Arsenic with Special Reference to the Roles of Metal Transporters

  • Himeno, Seiichiro (Tokushima Bunri University, Faculty of Pharmaceutical Sciences) ;
  • Sumi, Daigo (Tokushima Bunri University, Faculty of Pharmaceutical Sciences) ;
  • Fujishiro, Hitomi (Tokushima Bunri University, Faculty of Pharmaceutical Sciences)
  • Received : 2019.08.29
  • Accepted : 2019.09.05
  • Published : 2019.10.15

Abstract

The transport systems for metals play crucial roles in both the physiological functions of essential metals and the toxic effects of hazardous metals in mammals and plants. In mammalian cells, Zn transporters such as ZIP8 and ZIP14 have been found to function as the transporters for Mn(II) and Cd(II), contributing to the maintenance of Mn homeostasis and metallothionein-independent transports of Cd, respectively. In rice, the Mn transporter OsNramp5 expressed in the root is used for the uptake of Cd from the soil. Japan began to cultivate OsNramp5 mutant rice, which was found to accumulate little Cd, to prevent Cd accumulation. Inorganic trivalent arsenic (As(III)) is absorbed into mammalian cells via aquaglyceroporin, a water and glycerol channel. The ortholog of aquaporin in rice, OsLsi1, was found to be an Si transporter expressed in rice root, and is responsible for the absorption of soil As(III) into the root. Since rice is a hyperaccumulator of Si, higher amounts of As(III) are incorporated into rice compared to other plants. Thus, the transporters of essential metals are also utilized to incorporate toxic metals in both mammals and plants, and understanding the mechanisms of metal transports is important for the development of mitigation strategies against food contamination.

Keywords

References

  1. Haraguchi, H. (2017) Metallomics: the history over the last decade and a future outlook. Metallomics, 9, 1001-1013. https://doi.org/10.1039/C7MT00023E
  2. Hara, T., Takeda, T.A., Takagishi, T., Fukue, K., Kambe, T. and Fukada, T. (2017) Physiological roles of zinc transporters: molecular and genetic importance in zinc homeostasis. J. Physiol. Sci., 67, 283-301. https://doi.org/10.1007/s12576-017-0521-4
  3. Klaassen, C.D., Liu, J., and Diwan, B.A. (2009) Metallothionein protection of cadmium toxicity. Toxicol. Appl. Pharmacol., 238, 215-220. https://doi.org/10.1016/j.taap.2009.03.026
  4. Sabolic, I., Breljak, D., Skarica, M. and Herak-Kramberger, C.M. (2010) Role of metallothionein in cadmium traffic and toxicity in kidneys and other mammalian organs. Biometals, 23, 897-926. https://doi.org/10.1007/s10534-010-9351-z
  5. Wolff, N.A., Abouhamed, M., Verroust, P.J. and Thevenod, F. (2006) Megalin-dependent internalization of cadmium-metallothionein and cytotoxicity in cultured renal proximal tubule cells. J. Pharmacol. Exp. Ther., 318, 782-791. https://doi.org/10.1124/jpet.106.102574
  6. Elinder, C.G., Lind, B., Kjellstrom, T., Linnman, L. and Friberg, L. (1976) Cadmium in kidney cortex, liver, and pancreas from Swedish autopsies. Estimation of biological half time in kidney cortex, considering calorie intake and smoking habits. Arch. Environ. Health, 31, 292-302. https://doi.org/10.1080/00039896.1976.10667239
  7. Yanagiya, T., Imura, N., Kondo, Y. and Himeno, S. (1999) Reduced uptake and enhanced release of cadmium in cadmium resistant metallothionein null fibroblasts. Life Sci., 65, PL177-PL182. https://doi.org/10.1016/S0024-3205(99)00393-8
  8. Yanagiya, T., Imura, N., Enomoto, S., Kondo, Y. and Himeno, S. (2000) Suppression of a high-affinity transport system for manganese in cadmium-resistant metallothionein-null cells. J. Pharmacol. Exp. Ther., 292, 1080-1086.
  9. Himeno, S., Yanagiya, T. and Fujishiro, H. (2009) The role of zinc transporters in cadmium and manganese transport in mammalian cells. Biochimie, 91, 1218-1222. https://doi.org/10.1016/j.biochi.2009.04.002
  10. Fujishiro, H., Okugaki, S., Nagao, S., Satoh, M. and Himeno, S. (2006) Characterization of gene expression profiles of metallothionein-null cadmium-resistant cells. J. Health Sci., 52, 292-299. https://doi.org/10.1248/jhs.52.292
  11. Fujishiro, H., Okugaki, S., Kubota, K., Fujiyama, T., Miyataka, H. and Himeno, S. (2009) The role of ZIP8 down-regulation in cadmium-resistant metallothionein-null cells. J. Appl. Toxicol., 29, 367-373. https://doi.org/10.1002/jat.1419
  12. Fujishiro, H., Okugaki, S., Yasumitsu, S., Enomoto, S. and Himeno, S. (2009) Involvement of DNA hypermethylation in down-regulation of the zinc transporter ZIP8 in cadmium-resistant metallothionein-null cells. Toxicol. Appl. Pharmacol., 241, 195-201. https://doi.org/10.1016/j.taap.2009.08.015
  13. Fujishiro, H., Kubota, K., Inoue, D., Inoue, A., Yanagiya, T., Enomoto, S. and Himeno, S. (2011) Cross-resistance of cadmium-resistant cells to manganese is associated with reduced accumulation of both cadmium and manganese. Toxicology, 280, 118-125. https://doi.org/10.1016/j.tox.2010.12.002
  14. Fujishiro, H., Ohashi, T., Takuma, M. and Himeno, S. (2013) Suppression of ZIP8 expression is a common feature of cadmium-resistant and manganese-resistant RBL-2H3 cells. Metallomics, 5, 437-444. https://doi.org/10.1039/c3mt00003f
  15. Fujishiro, H., Doi, M., Enomoto, S. and Himeno, S. (2011) High sensitivity of RBL-2H3 cells to cadmium and manganese: an implication of the role of ZIP8. Metallomics, 3, 710-718. https://doi.org/10.1039/c1mt00020a
  16. Fujishiro, H., Yoshida, M., Nakano, Y. and Himeno, S. (2014) Interleukin-6 enhances manganese accumulation in SH-SY5Y cells: Implications of the up-regulation of ZIP14 and the down-regulation of ZnT10. Metallomics, 6, 944-949. https://doi.org/10.1039/C3MT00362K
  17. He, L., Wang, B., Hay, E.B. and Nebert, D.W. (2009) Discovery of ZIP transporters that participate in cadmium damage to testis and kidney. Toxicol. Appl. Pharmacol., 238, 250-257. https://doi.org/10.1016/j.taap.2009.02.017
  18. Gunshin, H., Mackenzie, B., Berger, U.V., Gunshin, Y., Romero, M.F., Boron, W.F., Nussberger, S., Gollan, J.L. and Hediger, M.A. (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature, 388, 482-488. https://doi.org/10.1038/41343
  19. Fujishiro, H., Hamao, S., Tanaka, R., Kambe, T. and Himeno, S. (2017) Concentration-dependent roles of DMT1 and ZIP14 in cadmium absorption in Caco-2 cells. J. Toxicol. Sci., 42, 559-567. https://doi.org/10.2131/jts.42.559
  20. Liuzzi, J.P., Lichten, L.A., Rivera, S., Blanchard, R.K., Aydemir, T.B., Knutson, M.D., Ganz, T. and Cousins, R.J. (2005) Interleukin-6 regulates the zinc transporter Zip14 in liver and contributes to the hypozincemia of the acute-phase response. Proc. Natl. Acad. Sci. U.S.A., 102, 6843-6848. https://doi.org/10.1073/pnas.0502257102
  21. Fujishiro, H., Yano, Y., Takada, Y., Tanihara, M. and Himeno, S. (2012) Roles of ZIP8, ZIP14, and DMT1 in transport of cadmium and manganese in mouse kidney proximal tubule cells. Metallomics, 4, 700-708. https://doi.org/10.1039/c2mt20024d
  22. Fujishiro, H. and Himeno, S. (2019) Gene expression profiles of immortalized S1, S2, and S3 cells derived from each segment of mouse kidney proximal tubules. Fundam. Toxicol. Sci., 6, 117-123. https://doi.org/10.2131/fts.6.117
  23. Fujishiro, H., Hamao, S., Isawa, M. and Himeno, S. (2019) Segment-specific and direction-dependent transport of cadmium and manganese in immortalized S1, S2, and S3 cells derived from mouse kidney proximal tubules. J. Toxicol. Sci., 44, 611-619. https://doi.org/10.2131/jts.44.611
  24. Himeno, S. and Fujishiro, H. (2019) Roles of metal transporters in cellular cadmium transport in mammals in Cadmium Toxicity New Aspects in Human Disease, Rice Contamination, and Cytotoxicity (Himeno, S. and Aoshima, K. Eds.). Springer, Singapore, pp. 163-178.
  25. Park, J.H., Hogrebe, M., Fobker, M., Brackmann, R., Fiedler, B., Reunert, J., Rust, S., Tsiakas, K., Santer, R., Gruneberg, M. and Marquardt, T. (2018) SLC39A8 deficiency: Biochemical correction and major clinical improvement by manganese therapy. Genet. Med., 20, 259-268. https://doi.org/10.1038/gim.2017.106
  26. Park, J.H., Hogrebe, M., Gruneberg, M., Duchesne, I., Von Der Heiden, A.L., Reunert, J., Schlingmann, K.P., Boycott, K.M., Beaulieu, C.L., Mhanni, A.A., Innes, A.M., Hortnagel, K., Biskup, S., Gleixner, E.M., Kurlemann, G., Fiedler, B., Omran, H., Rutsch, F., Wada, Y., Tsiakas, K., Santer, R., Nebert, D.W., Rust, S. and Marquardt, T. (2015) SLC39A8 deficiency: a disorder of manganese transport and glycosylation. Am. J. Hum. Genet., 97, 894-903. https://doi.org/10.1016/j.ajhg.2015.11.003
  27. Lin, W., Vann, D.R., Doulias, P.T., Wang, T., Landesberg, G., Li, X., Ricciotti, E., Scalia, R., He, M., Hand, N.J. and Rader, D.J. (2017) Hepatic metal ion transporter ZIP8 regulates manganese homeostasis and manganese-dependent enzyme activity. J. Clin. Invest., 127, 2407-2417. https://doi.org/10.1172/JCI90896
  28. Fujishiro, H. and Himeno, S. (2019) New insights into the roles of ZIP8, a cadmium and manganese transporter, and its relation to human diseases. Biol. Pharm. Bull., 42, 1076-1082. https://doi.org/10.1248/bpb.b18-00637
  29. Sasaki, A., Yamaji, N., Yokosho, K. and Ma, J.F. (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell, 24, 2155-2167. https://doi.org/10.1105/tpc.112.096925
  30. Ishikawa, S., Ishimaru, Y., Igura, M., Kuramata, M., Abe, T., Senoura, T., Hase, Y., Arao, T., Nishizawa, N.K. and Nakanishi, H. (2012) Ion-beam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. Proc. Natl. Acad. Sci. U.S.A., 109, 19166-19171. https://doi.org/10.1073/pnas.1211132109
  31. Yamauchi, H. and Sun, G. (2019) Arsenic Contamination in Asia Biological Effects and Preventive Measures. Springer, Singapore.
  32. Zhang, X.W., Yan, X.J., Zhou, Z.R., Yang, F.F., Wu, Z.Y., Sun, H.B., Liang, W.X., Song, A.X., Lallemand-Breitenbach, V., Jeanne, M., Zhang, Q.Y., Yang, H.Y., Huang, Q.H., Zhou, G.B., Tong, J.H., Zhang, Y., Wu, J.H., Hu, H.Y., de The, H., Chen, S.J. and Chen, Z. (2010) Arsenic trioxide controls the fate of the PML-$RAR{\alpha}$ oncoprotein by directly binding PML. Science, 328, 240-243. https://doi.org/10.1126/science.1183424
  33. Wysocki, R., Chery, C.C., Wawrzycka, D., Van Hulle, M., Cornelis, R., Thevelein, J.M. and Tamas, M.J. (2001) The glycerol channel Fps1p mediates the uptake of arsenite and antimonite in Saccharomyces cerevisiae. Mol. Microbiol., 40, 1391-1401. https://doi.org/10.1046/j.1365-2958.2001.02485.x
  34. Liu, Z., Shen, J., Carbrey, J.M., Mukhopadhyay, R., Agre, P. and Rosen, B.P. (2002) Arsenite transport by mammalian aquaglyceroporins AQP7 and AQP9. Proc. Natl. Acad. Sci. U.S.A., 99, 6053-6058. https://doi.org/10.1073/pnas.092131899
  35. Shinkai, Y., Sumi, D., Toyama, T., Kaji, T. and Kumagai, Y. (2009) Role of aquaporin 9 in cellular accumulation of arsenic and its cytotoxicity in primary mouse hepatocytes. Toxicol. Appl. Pharmacol., 237, 232-236. https://doi.org/10.1016/j.taap.2009.03.014
  36. Lee, T.C., Ho, I.C., Lu, W.J. and Huang, J.D. (2006) Enhanced expression of multidrug resistance-associated protein 2 and reduced expression of aquaglyceroporin 3 in an arsenic-resistant human cell line. J. Biol. Chem., 281, 18401-18407. https://doi.org/10.1074/jbc.M601266200
  37. Calatayud, M., Barrios, J.A., Velez, D. and Devesa, V. (2012) In vitro study of transporters involved in intestinal absorption of inorganic arsenic. Chem. Res. Toxicol., 25, 446-453. https://doi.org/10.1021/tx200491f
  38. Tsukaguchi, H., Shayakul, C., Berger, U.V., Mackenzie, B., Devidas, S., Guggino, W.B., Van Hoek, A.N. and Hediger, M.A. (1998) Molecular characterization of a broad selectivity neutral solute channel. J. Biol. Chem., 273, 24737-24743. https://doi.org/10.1074/jbc.273.38.24737
  39. Sumi, D., Suzukawa, K. and Himeno, S. (2016) Arsenic trioxide augments all-trans retinoic acid-induced differentiation of HL-60 cells. Life Sci., 149, 42-50. https://doi.org/10.1016/j.lfs.2016.02.054
  40. Villa-Bellosta, R. and Sorribas, V. (2010) Arsenate transport by sodium/phosphate cotransporter type IIb. Toxicol. Appl. Pharmacol., 247, 36-40. https://doi.org/10.1016/j.taap.2010.05.012
  41. Meharg, A.A. and Rahman, M. (2003) Arsenic contamination of Bangladesh paddy field soils: implications for rice contribution to arsenic consumption. Environ. Sci. Technol., 37, 229-234. https://doi.org/10.1021/es0259842
  42. Yamamoto, T., Nakamura, A., Iwai, H., Ishii, T., Ma, J.F., Yokoyama, R., Nishitani, K., Satoh, S. and Furukawa, J. (2012) Effect of silicon deficiency on secondary cell wall synthesis in rice leaf. J. Plant Res., 125, 771-779. https://doi.org/10.1007/s10265-012-0489-3
  43. Jian, F.M., Tamai, K., Yamaji, N., Mitani, N., Konishi, S., Katsuhara, M., Ishiguro, M., Murata, Y. and Yano, M. (2006) A silicon transporter in rice. Nature, 440, 688-691. https://doi.org/10.1038/nature04590
  44. Jian, F.M., Yamaji, N., Mitani, N., Xu, X.Y., Su, Y.H., McGrath, S.P. and Zhao, F.J. (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc. Natl. Acad. Sci. U.S.A., 105, 9931-9935. https://doi.org/10.1073/pnas.0802361105
  45. Xu, X.Y., McGrath, S.P., Meharg, A.A. and Zhao, F.J. (2008) Growing rice aerobically markedly decreases arsenic accumulation. Environ. Sci. Technol., 42, 5574-5579. https://doi.org/10.1021/es800324u
  46. Arao, T., Kawasaki, A., Baba, K., Mori, S. and Matsumoto, S. (2009) Effects of water management on cadmium and arsenic accumulation and dimethylarsinic acid concentrations in Japanese rice. Environ. Sci. Technol., 43, 9361-9367. https://doi.org/10.1021/es9022738
  47. Moreno-Jimenez, E., Meharg, A.A., Smolders, E., Manzano, R., Becerra, D., Sanchez-Llerena, J., Albarran, A. and Lopez-Pinero, A. (2014) Sprinkler irrigation of rice fields reduces grain arsenic but enhances cadmium. Sci. Total Environ., 485-486, 468-473. https://doi.org/10.1016/j.scitotenv.2014.03.106
  48. Hu, P., Huang, J., Ouyang, Y., Wu, L., Song, J., Wang, S., Li, Z., Han, C., Zhou, L., Huang, Y., Luo, Y. and Christie, P. (2013) Water management affects arsenic and cadmium accumulation in different rice cultivars. Environ. Geochem. Health, 35, 767-778. https://doi.org/10.1007/s10653-013-9533-z
  49. Arao, T. (2019) Mitigation strategies for cadmium and arsenic in rice in Cadmium Toxicity New Aspects in Human Disease, Rice Contamination, and Cytotoxicity (Himeno, S. and Aoshima, K. Eds.). Springer, Singapore, pp. 125-138.
  50. Horiguchi, H. (2019) Cadmium exposure and its effects on the health status of rice farmers in Akita prefecture in Cadmium Toxicity New Aspects in Human Disease, Rice Contamination, and Cytotoxicity (Himeno, S. and Aoshima, K. Eds.). Springer, Singapore, pp. 75-83.
  51. Codex Alimentarius Commission (2014) Distribution of the report of the eighth session of the Codex Committee on contaminants in foods (REP14/CF). FAO/WHO.
  52. Ishikawa, S., Makino, T., Ito, M., Harada, K., Nakada, H., Nishida, I., Nishimura, M., Tokunaga, T., Shirao, K., Yoshizawa, C., Matsuyama, M., Abe, T. and Arao, T. (2016) Low-cadmium rice (Oryza sativa L.) cultivar can simultaneously reduce arsenic and cadmium concentrations in rice grains. Soil Sci. Plant Nutr., 62, 327-339. https://doi.org/10.1080/00380768.2016.1144452