Lysosome-related organelles as mediators of metal homeostasis

Journal of Biological Chemistry

Volumn 289, Issue 41, 2014, Pages 28129-28136

  Blaby Haas, Crysten E ^a   Merchant, Sabeeha S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ECONOMICS; METAL IONS; YEAST;

ARABIDOPSIS THALIANA; INTRACELLULAR COMPARTMENTS; METAL HOMEOSTASIS; METAL TRANSPORTERS; SUPPLY AND DEMAND;

METALS;

CARRIER PROTEIN; COPPER; IRON; MANGANESE; ZINC; ARABIDOPSIS PROTEIN; DIVALENT CATION; METALLOPROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ACIDOCALCISOME; ARABIDOPSIS THALIANA; CELL COMPARTMENTALIZATION; CELL ORGANELLE; CELL VACUOLE; EUKARYOTE; GUT GRANULE; HOMEOSTASIS; ION TRANSPORT; LYSOSOME; LYTIC VACUOLE; METAL HOMEOSTASIS; METALLATION; NONHUMAN; NUTRIENT; PROTEIN STORAGE VACUOLE; REVIEW; SACCHAROMYCES CEREVISIAE; SENESCENCE ASSOCIATED VACUOLE; ZINCOSOME; ARABIDOPSIS; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION; GENETICS; METABOLISM; SPECIES DIFFERENCE; STRUCTURE ACTIVITY RELATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARRIER PROTEINS; CATIONS, DIVALENT; GENE EXPRESSION; HOMEOSTASIS; ION TRANSPORT; IRON; LYSOSOMES; MANGANESE; METALLOPROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SPECIES SPECIFICITY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84907835250     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.R114.592618     Document Type: Review

References (100)

1. Williams, R. (2001) Chemical selection of elements by cells. Coordin. Chem. Rev. 216, 583-595
2. Nar, H., Huber, R., Messerschmidt, A., Filippou, A. C., Barth, M., Jaquinod, M., van de Kamp, M., and Canters, G. W. (1992) Characterization and crystal structure of zinc azurin, a by-product of heterologous expression in Escherichia coli of Pseudomonas aeruginosa copper azurin. Eur. J. Biochem. 205, 1123-1129
3. Aguirre, J. D., Clark, H. M., McIlvin, M., Vazquez, C., Palmere, S. L., Grab, D. J., Seshu, J., Hart, P. J., Saito, M., and Culotta, V. C. (2013) A manganese- rich environment supports superoxide dismutase activity in a Lyme disease pathogen, Borrelia burgdorferi. J. Biol. Chem. 288, 8468-8478
4. Tripp, B. C., Bell, C. B., 3rd, Cruz, F., Krebs, C., and Ferry, J. G. (2004) A role for iron in an ancient carbonic anhydrase. J. Biol. Chem. 279, 6683-6687
5. Tottey, S., Waldron, K. J., Firbank, S. J., Reale, B., Bessant, C., Sato, K., Cheek, T. R., Gray, J., Banfield, M. J., Dennison, C., and Robinson, N. J. (2008) Protein-folding location can regulate manganese-binding versus copper- or zinc-binding. Nature 455, 1138-1142
6. Luk, E., Yang, M., Jensen, L. T., Bourbonnais, Y., and Culotta, V. C. (2005) Manganese activation of superoxide dismutase 2 in the mitochondria of Saccharomyces cerevisiae. J. Biol. Chem. 280, 22715-22720
7. Padilla-Benavides, T., George Thompson, A. M., McEvoy, M. M., and Argüello, J. M. (2014) Mechanism of ATPase-mediated Cu+ export and delivery to periplasmic chaperones: the interaction of Escherichia coli CopA and CusF. J. Biol. Chem. 289, 20492-20501
8. González-Guerrero, M., and Argüello, J. M. (2008) Mechanism of Cu+- transporting ATPases: soluble Cu+ chaperones directly transfer Cu+ to transmembrane transport sites. Proc. Natl. Acad. Sci. U.S.A. 105, 5992-5997
9. Eide, D. J., Clark, S., Nair, T. M., Gehl, M., Gribskov, M., Guerinot, M. L., and Harper, J. F. (2005) Characterization of the yeast ionome: a genomewide analysis of nutrient mineral and trace element homeostasis in Saccharomyces cerevisiae. Genome Biol. 6, R77
10. Ramsay, L. M., and Gadd, G. M. (1997) Mutants of Saccharomyces cerevisiae defective in vacuolar function confirm a role for the vacuole in toxic metal ion detoxification. FEMS Microbiol. Lett. 152, 293-298
11. Cowles, C. R., Odorizzi, G., Payne, G. S., and Emr, S. D. (1997) The AP-3 adaptor complex is essential for cargo-selective transport to the yeast vacuole. Cell 91, 109-118
12. Rogers, J. C. (2011) Internal membranes in maize aleurone protein storage vacuoles: beyond autophagy. Plant Cell 23, 4168-4171
13. Wada, T., and Lott, J. (1997) Light and electron microscopic and energy dispersive x-ray microanalysis studies of globoids in protein bodies of embryo tissues and the aleurone layer of rice (Oryza sativa L.) grains. Can. J. Bot. 75, 1137-1147
14. Regvar, M., Eichert, D., Kaulich, B., Gianoncelli, A., Pongrac, P., Vogel-Mikus, K., and Kreft, I. (2011) New insights into globoids of protein storage vacuoles in wheat aleurone using synchrotron soft x-ray microscopy. J. Exp. Bot. 62, 3929-3939
15. Otegui, M. S., Noh, Y. S., Martínez, D. E., Vila Petroff, M. G., Staehelin, L. A., Amasino, R. M., and Guiamet, J. J. (2005) Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean. Plant J. 41, 831-844
16. Kim, E. J., Zhen, R. G., and Rea, P. A. (1994) Heterologous expression of plant vacuolar pyrophosphatase in yeast demonstrates sufficiency of the substrate-binding subunit for proton transport. Proc. Natl. Acad. Sci. U.S.A. 91, 6128-6132
17. Krämer, U. (2005) Phytoremediation: novel approaches to cleaning up polluted soils. Curr. Opin. Biotechnol. 16, 133-141
18. Howe, G., and Merchant, S. (1992) Heavy metal-activated synthesis of peptides in Chlamydomonas reinhardtii. Plant Physiol. 98, 127-136
19. Wolfenstetter, S., Wirsching, P., Dotzauer, D., Schneider, S., and Sauer, N. (2012) Routes to the tonoplast: the sorting of tonoplast transporters in Arabidopsis mesophyll protoplasts. Plant Cell 24, 215-232
20. Viotti, C., Krüger, F., Krebs, M., Neubert, C., Fink, F., Lupanga, U., Scheuring, D., Boutté, Y., Frescatada-Rosa, M., Wolfenstetter, S., Sauer, N., Hillmer, S., Grebe, M., and Schumacher, K. (2013) The endoplasmic reticulum is the main membrane source for biogenesis of the lytic vacuole in Arabidopsis. Plant Cell 25, 3434-3449
21. Docampo, R., de Souza, W., Miranda, K., Rohloff, P., and Moreno, S. N. (2005) Acidocalcisomes: conserved from bacteria to man. Nat. Rev. Microbiol. 3, 251-261
22. Ferella, M., Nilsson, D., Darban, H., Rodrigues, C., Bontempi, E. J., Docampo, R., and Andersson, B. (2008) Proteomics in Trypanosoma cruzi: localization of novel proteins to various organelles. Proteomics 8, 2735-2749
23. Yagisawa, F., Nishida, K., Yoshida, M., Ohnuma, M., Shimada, T., Fujiwara, T., Yoshida, Y., Misumi, O., Kuroiwa, H., and Kuroiwa, T. (2009) Identification of novel proteins in isolated polyphosphate vacuoles in the primitive red alga Cyanidioschyzon merolae. Plant J. 60, 882-893
24. Huang, G., Fang, J., Sant'Anna, C., Li, Z. H., Wellems, D. L., Rohloff, P., and Docampo, R. (2011) Adaptor protein-3 (AP-3) complex mediates the biogenesis of acidocalcisomes and is essential for growth and virulence of Trypanosoma brucei. J. Biol. Chem. 286, 36619-36630
25. Besteiro, S., Tonn, D., Tetley, L., Coombs, G. H., and Mottram, J. C. (2008) The AP3 adaptor is involved in the transport of membrane proteins to acidocalcisomes of Leishmania. J. Cell Sci. 121, 561-570
26. Eide, D. J. (2006) Zinc transporters and the cellular trafficking of zinc. Biochim. Biophys. Acta 1763, 711-722
27. Devirgiliis, C., Murgia, C., Danscher, G., and Perozzi, G. (2004) Exchangeable zinc ions transiently accumulate in a vesicular compartment in the yeast Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 323, 58-64
28. Li, L., and Kaplan, J. (2001) The yeast gene MSC2, a member of the cation diffusion facilitator family, affects the cellular distribution of zinc. J. Biol. Chem. 276, 5036-5043
29. Simm, C., Lahner, B., Salt, D., LeFurgey, A., Ingram, P., Yandell, B., and Eide, D. J. (2007) Saccharomyces cerevisiae vacuole in zinc storage and intracellular zinc distribution. Eukaryot. Cell 6, 1166-1177
30. Haase, H., and Beyersmann, D. (1999) Uptake and intracellular distribution of labile and total Zn(II) in C6 rat glioma cells investigated with fluorescent probes and atomic absorption. Biometals 12, 247-254
31. McCormick, N., Velasquez, V., Finney, L., Vogt, S., and Kelleher, S. L. (2010) X-ray fluorescence microscopy reveals accumulation and secretion of discrete intracellular zinc pools in the lactating mouse mammary gland. PLoS One 5, e11078
32. Khan, M., Goldsmith, C. R., Huang, Z., Georgiou, J., Luyben, T. T., Roder, J. C., Lippard, S. J., and Okamoto, K. (2014) Two-photon imaging of Zn2+ dynamics in mossy fiber boutons of adult hippocampal slices. Proc. Natl. Acad. Sci. U.S.A. 111, 6786-6791
33. Kambe, T., Narita, H., Yamaguchi-Iwai, Y., Hirose, J., Amano, T., Sugiura, N., Sasaki, R., Mori, K., Iwanaga, T., and Nagao, M. (2002) Cloning and characterization of a novel mammalian zinc transporter, zinc transporter 5, abundantly expressed in pancreatic β cells. J. Biol. Chem. 277, 19049-19055
34. Haase, H., and Beyersmann, D. (2002) Intracellular zinc distribution and transport in C6 rat glioma cells. Biochem. Biophys. Res. Commun. 296, 923-928
35. Palmiter, R. D., Cole, T. B., and Findley, S. D. (1996) ZnT-2, a mammalian protein that confers resistance to zinc by facilitating vesicular sequestration. EMBO J. 15, 1784-1791
36. Jeong, J., Walker, J. M., Wang, F., Park, J. G., Palmer, A. E., Giunta, C., Rohrbach, M., Steinmann, B., and Eide, D. J. (2012) Promotion of vesicular zinc efflux by ZIP13 and its implications for spondylocheiro dysplastic Ehlers-Danlos syndrome. Proc. Natl. Acad. Sci. U.S.A. 109, E3530-E3538
37. Roh, H. C., Collier, S., Guthrie, J., Robertson, J. D., and Kornfeld, K. (2012) Lysosome-related organelles in intestinal cells are a zinc storage site in C. elegans. Cell Metab. 15, 88-99
38. Song, W. Y., Park, J., Mendoza-Cózatl, D. G., Suter-Grotemeyer, M., Shim, D., Hörtensteiner, S., Geisler, M., Weder, B., Rea, P. A., Rentsch, D., Schroeder, J. I., Lee, Y., and Martinoia, E. (2010) Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters. Proc. Natl. Acad. Sci. U.S.A. 107, 21187-21192
39. 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
40. Sacher, A., Cohen, A., and Nelson, N. (2001) Properties of the mammalian and yeast metal-ion transporters DCT1 and Smf1p expressed in Xenopus laevis oocytes. J. Exp. Biol. 204, 1053-1061
41. Xia, J., Yamaji, N., Kasai, T., and Ma, J. F. (2010) Plasma membranelocalized transporter for aluminum in rice. Proc. Natl. Acad. Sci. U.S.A. 107, 18381-18385
42. Cellier, M. F. (2012) Nramp: from sequence to structure and mechanism of divalent metal import. Curr. Top. Membr. 69, 249-293
43. Portnoy, M. E., Liu, X. F., and Culotta, V. C. (2000) Saccharomyces cerevisiae expresses three functionally distinct homologues of the NRAMP family of metal transporters. Mol. Cell. Biol. 20, 7893-7902
44. Luk, E. E., and Culotta, V. C. (2001) Manganese superoxide dismutase in Saccharomyces cerevisiae acquires its metal co-factor through a pathway involving the Nramp metal transporter, Smf2p. J. Biol. Chem. 276, 47556-47562
45. Portnoy, M. E., Jensen, L. T., and Culotta, V. C. (2002) The distinct methods by which manganese and iron regulate the Nramp transporters in yeast. Biochem. J. 362, 119-124
46. Singh, A., Kaur, N., and Kosman, D. J. (2007) The metalloreductase Fre6p in Fe-efflux from the yeast vacuole. J. Biol. Chem. 282, 28619-28626
47. Lanquar, V., Lelièvre, F., Bolte, S., Hamès, C., Alcon, C., Neumann, D., Vansuyt, G., Curie, C., Schröder, A., Krämer, U., Barbier-Brygoo, H., and Thomine, S. (2005) Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron. EMBO J. 24, 4041-4051
48. Thomine, S., Lelièvre, F., Debarbieux, E., Schroeder, J. I., and Barbier-Brygoo, H. (2003) AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J. 34, 685-695
49. Lanquar, V., Ramos, M. S., Lelièvre, F., Barbier-Brygoo, H., Krieger-Liszkay, A., Krämer, U., and Thomine, S. (2010) Export of vacuolar manganese by AtNRAMP3 and AtNRAMP4 is required for optimal photosynthesis and growth under manganese deficiency. Plant Physiol. 152, 1986-1999
50. Urzica, E. I., Casero, D., Yamasaki, H., Hsieh, S. I., Adler, L. N., Karpowicz, S. J., Blaby-Haas, C. E., Clarke, S. G., Loo, J. A., Pellegrini, M., and Merchant, S. S. (2012) Systems and trans-system level analysis identifies conserved iron deficiency responses in the plant lineage. Plant Cell 24, 3921-3948
51. Jeong, J., and Eide, D. J. (2013) The SLC39 family of zinc transporters. Mol. Aspects Med. 34, 612-619
52. He, L., Girijashanker, K., Dalton, T. P., Reed, J., Li, H., Soleimani, M., and Nebert, D. W. (2006) ZIP8, member of the solute-carrier-39 (SLC39) metal-transporter family: characterization of transporter properties. Mol. Pharmacol. 70, 171-180
53. Gaither, L. A., and Eide, D. J. (2000) Functional expression of the human hZIP2 zinc transporter. J. Biol. Chem. 275, 5560-5564
54. Lin, W., Chai, J., Love, J., and Fu, D. (2010) Selective electrodiffusion of zinc ions in a Zrt-, Irt-like protein, ZIPB. J. Biol. Chem. 285, 39013-39020
55. Lyons, T. J., Gasch, A. P., Gaither, L. A., Botstein, D., Brown, P. O., and Eide, D. J. (2000) Genome-wide characterization of the Zap1p zinc-responsive regulon in yeast. Proc. Natl. Acad. Sci. U.S.A. 97, 7957-7962
56. MacDiarmid, C. W., Gaither, L. A., and Eide, D. (2000) Zinc transporters that regulate vacuolar zinc storage in Saccharomyces cerevisiae. EMBO J. 19, 2845-2855
57. Blaby-Haas, C. E., and Merchant, S. S. (2012) The ins and outs of algal metal transport. Biochim. Biophys. Acta 1823, 1531-1552
58. Milner, M. J., Seamon, J., Craft, E., and Kochian, L. V. (2013) Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis. J. Exp. Bot. 64, 369-381
59. Grotz, N., Fox, T., Connolly, E., Park, W., Guerinot, M. L., and Eide, D. (1998) Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proc. Natl. Acad. Sci. U.S.A. 95, 7220-7224
60. van de Mortel, J. E., Almar Villanueva, L., Schat, H., Kwekkeboom, J., Coughlan, S., Moerland, P. D., Ver Loren van Themaat, E., Koornneef, M., and Aarts, M. G. (2006) Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiol. 142, 1127-1147
61. De Feo, C. J., Aller, S. G., Siluvai, G. S., Blackburn, N. J., and Unger, V. M. (2009) Three-dimensional structure of the human copper transporter hCTR1. Proc. Natl. Acad. Sci. U.S.A. 106, 4237-4242
62. Tsigelny, I. F., Sharikov, Y., Greenberg, J. P., Miller, M. A., Kouznetsova, V. L., Larson, C. A., and Howell, S. B. (2012) An all-atom model of the structure of human copper transporter 1. Cell Biochem. Biophys 63, 223-234
63. Pope, C. R., Flores, A. G., Kaplan, J. H., and Unger, V. M. (2012) Structure and function of copper uptake transporters. Curr. Top. Membr. 69, 97-112
64. Öhrvik, H., Nose, Y., Wood, L. K., Kim, B. E., Gleber, S. C., Ralle, M., and Thiele, D. J. (2013) Ctr2 regulates biogenesis of a cleaved form of mammalian Ctr1 metal transporter lacking the copper- and cisplatin-binding ecto-domain. Proc. Natl. Acad. Sci. U.S.A. 110, E4279-E4288
65. Rubino, J. T., Chenkin, M. P., Keller, M., Riggs-Gelasco, P., and Franz, K. J. (2011) A comparison of methionine, histidine and cysteine in copper( I)-binding peptides reveals differences relevant to copper uptake by organisms in diverse environments. Metallomics 3, 61-73
66. Rees, E. M., Lee, J., and Thiele, D. J. (2004) Mobilization of intracellular copper stores by the Ctr2 vacuolar copper transporter. J. Biol. Chem. 279, 54221-54229
67. Rees, E. M., and Thiele, D. J. (2007) Identification of a vacuole-associated metalloreductase and its role in Ctr2-mediated intracellular copper mobilization. J. Biol. Chem. 282, 21629-21638
68. Portnoy, M. E., Schmidt, P. J., Rogers, R. S., and Culotta, V. C. (2001) Metal transporters that contribute copper to metallochaperones in Saccharomyces cerevisiae. Mol. Genet. Genomics 265, 873-882
69. Garcia-Molina, A., Andrés-Colás, N., Perea-García, A., Del Valle-Tascón, S., Peñarrubia, L., and Puig, S. (2011) The intracellular Arabidopsis COPT5 transport protein is required for photosynthetic electron transport under severe copper deficiency. Plant J. 65, 848-860
70. Klaumann, S., Nickolaus, S. D., Fürst, S. H., Starck, S., Schneider, S., Ekkehard Neuhaus, H., and Trentmann, O. (2011) The tonoplast copper transporter COPT5 acts as an exporter and is required for interorgan allocation of copper in Arabidopsis thaliana. New Phytol. 192, 393-404
71. Raguzzi, F., Lesuisse, E., and Crichton, R. R. (1988) Iron storage in Saccharomyces cerevisiae. FEBS Lett. 231, 253-258
72. Urbanowski, J. L., and Piper, R. C. (1999) The iron transporter Fth1p forms a complex with the Fet5 iron oxidase and resides on the vacuolar membrane. J. Biol. Chem. 274, 38061-38070
73. Jensen, L. T., and Culotta, V. C. (2002) Regulation of Saccharomyces cerevisiae FET4 by oxygen and iron. J. Mol. Biol. 318, 251-260
74. MacDiarmid, C. W., Milanick, M. A., and Eide, D. J. (2002) Biochemical properties of vacuolar zinc transport systems of Saccharomyces cerevisiae. J. Biol. Chem. 277, 39187-39194
75. Malasarn, D., Kropat, J., Hsieh, S. I., Finazzi, G., Casero, D., Loo, J. A., Pellegrini, M., Wollman, F. A., and Merchant, S. S. (2013) Zinc deficiency impacts CO2 assimilation and disrupts copper homeostasis in Chlamydomonas reinhardtii. J. Biol. Chem. 288, 10672-10683
76. Kawachi, M., Kobae, Y., Mori, H., Tomioka, R., Lee, Y., and Maeshima, M. (2009) A mutant strain Arabidopsis thaliana that lacks vacuolar membrane zinc transporter MTP1 revealed the latent tolerance to excessive zinc. Plant Cell Physiol. 50, 1156-1170
77. Arrivault, S., Senger, T., and Krämer, U. (2006) The Arabidopsis metal tolerance protein AtMTP3 maintains metal homeostasis by mediating Zn exclusion from the shoot under Fe deficiency and Zn oversupply. Plant J. 46, 861-879
78. Peiter, E., Montanini, B., Gobert, A., Pedas, P., Husted, S., Maathuis, F. J., Blaudez, D., Chalot, M., and Sanders, D. (2007) A secretory pathwaylocalized cation diffusion facilitator confers plant manganese tolerance. Proc. Natl. Acad. Sci. U.S.A. 104, 8532-8537
79. Andrews, S. C. (2010) The Ferritin-like superfamily: evolution of the biological iron storeman from a rubrerythrin-like ancestor. Biochim. Biophys. Acta 1800, 691-705
80. Bhubhanil, S., Chamsing, J., Sittipo, P., Chaoprasid, P., Sukchawalit, R., and Mongkolsuk, S. (2014) Roles of Agrobacterium tumefaciens membrane- bound ferritin (MbfA) in iron transport and resistance to iron under acidic conditions. Microbiology 160, 863-871
81. Sankari, S., and O'Brian, M. R. (2014) A bacterial iron exporter for maintenance of iron homeostasis. J. Biol. Chem. 289, 16498-16507
82. Li, L., Chen, O. S., McVey Ward, D., and Kaplan, J. (2001) CCC1 is a transporter that mediates vacuolar iron storage in yeast. J. Biol. Chem. 276, 29515-29519
83. Li, L., Bagley, D., Ward, D. M., and Kaplan, J. (2008) Yap5 is an ironresponsive transcriptional activator that regulates vacuolar iron storage in yeast. Mol. Cell. Biol. 28, 1326-1337
84. Yamada, K., Nagano, A. J., Nishina, M., Hara-Nishimura, I., and Nishimura, M. (2013) Identification of two novel endoplasmic reticulum body-specific integral membrane proteins. Plant Physiol. 161, 108-120
85. Hakoyama, T., Niimi, K., Yamamoto, T., Isobe, S., Sato, S., Nakamura, Y., Tabata, S., Kumagai, H., Umehara, Y., Brossuleit, K., Petersen, T. R., Sandal, N., Stougaard, J., Udvardi, M. K., Tamaoki, M., Kawaguchi, M., Kouchi, H., and Suganuma, N. (2012) The integral membrane protein SEN1 is required for symbiotic nitrogen fixation in Lotus japonicus nodules. Plant Cell Physiol. 53, 225-236
86. Kim, S. A., Punshon, T., Lanzirotti, A., Li, L., Alonso, J. M., Ecker, J. R., Kaplan, J., and Guerinot, M. L. (2006) Localization of iron in Arabidopsis seed requires the vacuolar membrane transporter VIT1. Science 314, 1295-1298
87. Ward, D. M., and Kaplan, J. (2012) Ferroportin-mediated iron transport: expression and regulation. Biochim. Biophys. Acta 1823, 1426-1433
88. Schaaf, G., Honsbein, A., Meda, A. R., Kirchner, S., Wipf, D., and von Wirén, N. (2006) AtIREG2 encodes a tonoplast transport protein involved in iron-dependent nickel detoxification in Arabidopsis thaliana roots. J. Biol. Chem. 281, 25532-25540
89. Morrissey, J., Baxter, I. R., Lee, J., Li, L., Lahner, B., Grotz, N., Kaplan, J., Salt, D. E., and Guerinot, M. L. (2009) The ferroportin metal efflux proteins function in iron and cobalt homeostasis in Arabidopsis. Plant Cell 21, 3326-3338
90. Merchant, S. S., and Helmann, J. D. (2012) Elemental economy: microbial strategies for optimizing growth in the face of nutrient limitation. Adv. Microb. Physiol. 60, 91-210
91. Blaby-Haas, C., and Merchant, S. (2013) Sparing and salvaging metals in chloroplasts. in Encyclopedia of Inorganic and Bioinorganic Chemistry, pp. 51-64, John Wiley & Sons, Chichester, West Sussex, United Kingdom
92. Labbé, R. F., Rettmer, R. L., Shah, A. G., and Turnlund, J. R. (1987) Zinc protoporphyrin: past, present, and future. Ann. N.Y. Acad. Sci. 514, 7-14
93. Yang, M., Cobine, P. A., Molik, S., Naranuntarat, A., Lill, R., Winge, D. R., and Culotta, V. C. (2006) The effects of mitochondrial iron homeostasis on cofactor specificity of superoxide dismutase 2. EMBO J. 25, 1775-1783
94. Macomber, L., and Imlay, J. A. (2009) The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc. Natl. Acad. Sci. U.S.A. 106, 8344-8349
95. Macomber, L., and Hausinger, R. P. (2011) Mechanisms of nickel toxicity in microorganisms. Metallomics 3, 1153-1162
96. Gu, M., and Imlay, J. A. (2013) Superoxide poisons mononuclear iron enzymes by causing mismetallation. Mol. Microbiol. 89, 123-134
97. Korshunova, Y. O., Eide, D., Clark, W. G., Guerinot, M. L., and Pakrasi, H. B. (1999) The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol. Biol. 40, 37-44
98. Vert, G., Grotz, N., Dédaldéchamp, F., Gaymard, F., Guerinot, M. L., Briat, J. F., and Curie, C. (2002) IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14, 1223-1233
99. Merchant, S., Hill, K., and Howe, G. (1991) Dynamic interplay between two copper-titrating components in the transcriptional regulation of cyt c6. EMBO J. 10, 1383-1389
100. Zhao, F. J., Moore, K. L., Lombi, E., and Zhu, Y. G. (2014) Imaging element distribution and speciation in plant cells. Trends Plant Sci. 19, 183-192