Dietary zinc absorption is mediated by ZnT1 in Drosophila melanogaster

FASEB Journal

Volumn 23, Issue 8, 2009, Pages 2650-2661

  Wang, Xiaoxi ^a   Wu, Yuantai ^a   Zhou, Bing ^a  

^a TSINGHUA UNIVERSITY   (China)

Author keywords

Basolateral membrane; dZnT1, metallothionein; Midgut constriction

Indexed keywords

RNA; UNCLASSIFIED DRUG; ZINC; ZINC TRANSPORTER; ZINC TRANSPORTER 1; CARRIER PROTEIN; CATION TRANSPORT PROTEIN; DROSOPHILA PROTEIN; SLC30A1 PROTEIN, HUMAN; ZINC BINDING PROTEIN; ZINC-BINDING PROTEIN;

ABSORPTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASOLATERAL MEMBRANE; CELL CULTURE; COMPREHENSION; CONTROLLED STUDY; CYTOPLASM; DROSOPHILA MELANOGASTER; EMBRYO; EUKARYOTE; GENE SILENCING; HUMAN; HUMAN CELL; INTESTINE CELL; LETHALITY; MALE; MIDGUT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; RNA INTERFERENCE; ANIMAL; DIET; DIGESTIVE SYSTEM; DRUG ANTAGONISM; GENE; GENE EXPRESSION; GENETIC COMPLEMENTATION; GENETICS; INTESTINE ABSORPTION; METABOLISM; MOUSE; PHENOTYPE; PHYLOGENY; TRANSGENIC ANIMAL;

DROSOPHILA MELANOGASTER; EUKARYOTA; MUS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CARRIER PROTEINS; CATION TRANSPORT PROTEINS; DIET; DIGESTIVE SYSTEM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENTEROCYTES; GENE EXPRESSION; GENES, INSECT; GENETIC COMPLEMENTATION TEST; HUMANS; INTESTINAL ABSORPTION; MICE; PHENOTYPE; PHYLOGENY; RNA INTERFERENCE; ZINC;

EID: 68849129637     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-126649     Document Type: Article

References (66)

1. Vallee, B. L., and Falchuk, K. H. (1993) The biochemical basis of zinc physiology. Physiol. Rev. 73, 79-118
2. Berg, J. M., and Shi, Y. (1996) The galvanization of biology: a growing appreciation for the roles of zinc. Science 271, 1081-1085
3. MacDonald, R. S. (2000) The role of zinc in growth and cell proliferation. J. Nutr. 130, 1500S-1508S
4. King, J. C., Shames, D. M., and Woodhouse, L. R. (2000) Zinc homeostasis in humans. J. Nutr. 130, 1360S-1366S
5. Sekler, I., Sensi, S. L., Hershfinkel, M., and Silverman, W. F. (2007) Mechanism and regulation of cellular zinc transport. Mol. Med. 13, 337-343 (Pubitemid 47378133)
6. Liuzzi, J. P., and Cousins, R. J. (2004) Mammalian zinc transporters. Annu. Rev. Nutr. 24, 151-172
7. Eide, D. J. (2006) Zinc transporters and the cellular trafficking of zinc. Biochim. Biophys. Acta 1763, 711-722
8. Kumanovics, A., Poruk, K. E., Osborn, K. A., Ward, D. M., and Kaplan, J. (2006) YKE4 (YIL023C) encodes a bidirectional zinc transporter in the endoplasmic reticulum of Saccharomyces cerevisiae. J. Biol. Chem. 281, 22566-22574 (Pubitemid 44242285)
9. Valentine, R. A., Jackson, K. A., Christie, G. R., Mathers, J. C., Taylor, P. M., and Ford, D. (2007) ZnT5 variant B is a bidirectional zinc transporter and mediates zinc uptake in human intestinal Caco-2 cells. J. Biol. Chem. 282, 14389-14393
10. Cousins, R. J., Liuzzi, J. P., and Lichten, L. A. (2006) Mammalian zinc transport, trafficking, and signals. J. Biol. Chem. 281, 24085-24089
11. Wang, K., Zhou, B., Kuo, Y. M., Zemansky, J., and Gitschier, J. (2002) A novel member of a zinc transporter family is defective in acrodermatitis enteropathica. Am. J. Hum. Genet. 71, 66-73 (Pubitemid 34734708)
12. Kury, S., Dreno, B., Bezieau, S., Giraudet, S., Kharfi, M., Kamoun, R., and Moisan, J. P. (2002) Identification of SLC39A4, a gene involved in acrodermatitis enteropathica. Nat. Genet. 31, 239-240 (Pubitemid 34887587)
13. Dufner-Beattie, J., Wang, F., Kuo, Y. M., Gitschier, J., Eide, D., and Andrews, G. K. (2003) The acrodermatitis enteropathica gene ZIP4 encodes a tissue-specific, zinc-regulated zinc transporter in mice. J. Biol. Chem. 278, 33474-33481 (Pubitemid 37055802)
14. Palmiter, R. D., and Findley, S. D. (1995) Cloning and functional characterization of a mammalian zinc transporter that confers resistance to zinc. EMBO J. 14, 639-649
15. Kim, A. H., Sheline, C. T., Tian, M., Higashi, T., McMahon, R. J., Cousins, R. J., and Choi, D. W. (2000) L-type Ca(2+) channel-mediated Zn(2+) toxicity and modulation by ZnT-1 in PC12 cells. Brain Res. 886, 99-107
16. McMahon, R. J., and Cousins, R. J. (1998) Regulation of the zinc transporter ZnT-1 by dietary zinc. Proc. Natl. Acad. Sci. U. S. A. 95, 4841-4846
17. Yu, Y. Y., Kirschke, C. P., and Huang, L. (2007) Immunohistochemical analysis of ZnT1, 4, 5, 6, and 7 in the mouse gastrointestinal tract. J. Histochem. Cytochem. 55, 223-234 (Pubitemid 46311071)
18. Vancampen, D. R., and Mitchell, E. A. (1965) Absorption of Cu-64, Zn-65, Mo-99, and Fe-59 from ligated segments of the rat gastrointestinal tract. J. Nutr. 86, 120-124
19. Huang, L., and Gitschier, J. (1997) A novel gene involved in zinc transport is deficient in the lethal milk mouse. Nat. Genet. 17, 292-297 (Pubitemid 27475991)
20. Cole, T. B., Wenzel, H. J., Kafer, K. E., Schwartzkroin, P. A., and Palmiter, R. D. (1999) Elimination of zinc from synaptic vesicles in the intact mouse brain by disruption of the ZnT3 gene. Proc. Natl. Acad. Sci. U. S. A. 96, 1716-1721
21. Inoue, K., Matsuda, K., Itoh, M., Kawaguchi, H., Tomoike, H., Aoyagi, T., Nagai, R., Hori, M., Nakamura, Y., and Tanaka, T. (2002) Osteopenia and male-specific sudden cardiac death in mice lacking a zinc transporter gene, Znt5. Hum. Mol. Genet. 11, 1775-1784 (Pubitemid 34812098)
22. Huang, L., Yu, Y. Y., Kirschke, C. P., Gertz, E. R., and Lloyd, K. K. (2007) Znt7 (Slc30a7)-deficient mice display reduced body zinc status and body fat accumulation. J. Biol. Chem. 282, 37053-37063
23. Andrews, G. K., Wang, H., Dey, S. K., and Palmiter, R. D. (2004) Mouse zinc transporter 1 gene provides an essential function during early embryonic development. Genesis 40, 74-81 (Pubitemid 39488503)
24. Zhou, H., Cadigan, K. M., and Thiele, D. J. (2003) A copper-regulated transporter required for copper acquisition, pigmentation, and specific stages of development in Drosophila melanogaster. J. Biol. Chem. 278, 48210-48218 (Pubitemid 37523275)
25. Norgate, M., Lee, E., Southon, A., Farlow, A., Batterham, P., Camakaris, J., and Burke, R. (2006) Essential roles in development and pigmentation for the Drosophila copper transporter DmATP7. Mol. Biol. Cell 17, 475-484 (Pubitemid 43049498)
26. Balamurugan, K., Egli, D., Hua, H., Rajaram, R., Seisenbacher, G., Georgiev, O., and Schaffner, W. (2007) Copper homeostasis in Drosophila by complex interplay of import, storage and behavioral avoidance. EMBO J. 26, 1035-1044 (Pubitemid 46303574)
27. Turski, M. L., and Thiele, D. J. (2007) Drosophila Ctr1A functions as a copper transporter essential for development. J. Biol. Chem. 282, 24017-24026
28. Egli, D., Selvaraj, A., Yepiskoposyan, H., Zhang, B., Hafen, E., Georgiev, O., and Schaffner, W. (2003) Knockout of 'metal-responsive transcription factor' MTF-1 in Drosophila by homologous recombination reveals its central role in heavy metal homeostasis. EMBO J. 22, 100-108 (Pubitemid 36091273)
29. Selvaraj, A., Balamurugan, K., Yepiskoposyan, H., Zhou, H., Egli, D., Georgiev, O., Thiele, D. J., and Schaffner, W. (2005) Metal-responsive transcription factor (MTF-1) handles both extremes, copper load and copper starvation, by activating different genes. Genes Dev. 19, 891-896 (Pubitemid 40548057)
30. Egli, D., Yepiskoposyan, H., Selvaraj, A., Balamurugan, K., Rajaram, R., Simons, A., Multhaup, G., Mettler, S., Vardanyan, A., Georgiev, O., and Schaffner, W. (2006) A family knockout of all four Drosophila metallothioneins reveals a central role in copper homeostasis and detoxification. Mol. Cell. Biol. 26, 2286-2296 (Pubitemid 43346928)
31. Egli, D., Domenech, J., Selvaraj, A., Balamurugan, K., Hua, H., Capdevila, M., Georgiev, O., Schaffner, W., and Atrian, S. (2006) The four members of the Drosophila metallothionein family exhibit distinct yet overlapping roles in heavy metal homeostasis and detoxification. Genes Cells 11, 647-658 (Pubitemid 43744815)
32. Van Doren, M., Mathews, W. R., Samuels, M., Moore, L. A., Broihier, H. T., and Lehmann, R. (2003) Fear of intimacy encodes a novel transmembrane protein required for gonad morphogenesis in Drosophila. Development 130, 2355-2364 (Pubitemid 36722387)
33. Pielage, J., Kippert, A., Zhu, M., and Klambt, C. (2004) The Drosophila transmembrane protein Fear-of-intimacy controls glial cell migration. Dev. Biol. 275, 245-257 (Pubitemid 39298189)
34. Mathews, W. R., Wang, F., Eide, D. J., and Van Doren, M. (2005) Drosophila fear of intimacy encodes a Zrt/IRT-like protein (ZIP) family zinc transporter functionally related to mammalian ZIP proteins. J. Biol. Chem. 280, 787-795 (Pubitemid 40165047)
35. Mathews, W. R., Ong, D., Milutinovich, A. B., and Van Doren, M. (2006) Zinc transport activity of fear of intimacy is essential for proper gonad morphogenesis and DE-cadherin expression. Development 133, 1143-1153
36. Yepiskoposyan, H., Egli, D., Fergestad, T., Selvaraj, A., Treiber, C., Multhaup, G., Georgiev, O., and Schaffner, W. (2006) Transcriptome response to heavy metal stress in Drosophila reveals a new zinc transporter that confers resistance to zinc. Nucleic Acids Res. 34, 4866-4877 (Pubitemid 44605630)
37. Kalidas, S., and Smith, D. P. (2002) Novel genomic cDNA hybrids produce effective RNA interference in adult Drosophila. Neuron 33, 177-184 (Pubitemid 34127751)
38. Morin, X., Daneman, R., Zavortink, M., and Chia, W. (2001) A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 98, 15050-15055 (Pubitemid 34013967)
39. Wang, T., Jiao, Y., and Montell, C. (2007) Dissection of the pathway required for generation of vitamin A and for Drosophila phototransduction. J. Cell Biol. 177, 305-316 (Pubitemid 46658641)
40. Carstens, J., Jensen, K. T., Ivarsen, P., Rasmussen, L. M., and Pedersen, E. B. (1997) Development of a urodilatin-specific antibody and radioimmunoassay for urodilatin in human urine. Clin. Chem. 43, 638-643 (Pubitemid 27155048)
41. Aarskog, N. K., and Vedeler, C. A. (2000) Real-time quantitative polymerase chain reaction. A new method that detects both the peripheral myelin protein 22 duplication in Charcot-Marie- Tooth type 1A disease and the peripheral myelin protein 22 deletion in hereditary neuropathy with liability to pressure palsies. Hum. Genet. 107, 494-498
42. 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
43. Naito, Y., Yamada, T., Matsumiya, T., Ui-Tei, K., Saigo, K., and Morishita, S. (2005) dsCheck: highly sensitive off-target search software for double-stranded RNA-mediated RNA interference. Nucleic Acids Res. 33, W589-591 (Pubitemid 44529990)
44. Dietzl, G., Chen, D., Schnorrer, F., Su, K. C., Barinova, Y., Fellner, M., Gasser, B., Kinsey, K., Oppel, S., Scheiblauer, S., Couto, A., Marra, V., Keleman, K., and Dickson, B. J. (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151-156 (Pubitemid 47067374)
45. Durliat, M., Bonneton, F., Boissonneau, E., Andre, M., and Wegnez, M. (1995) Expression of metallothionein genes during the post-embryonic development of Drosophila melanogaster. Biometals 8, 339-351
46. Tomancak, P., Beaton, A., Weiszmann, R., Kwan, E., Shu, S., Lewis, S. E., Richards, S., Ashburner, M., Hartenstein, V., Celniker, S. E., and Rubin, G. M. (2002) Systematic determination of patterns of gene expression during Drosophila embryogenesis. [Online]. Genome Biol 3, RESEARCH0088.1-88.14
47. Brenner, R., and Atkinson, N. S. (1997) Calcium-activated potassium channel gene expression in the midgut of Drosophila. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 118, 411-420 (Pubitemid 28006069)
48. Missirlis, F., Kosmidis, S., Brody, T., Mavrakis, M., Holmberg, S., Odenwald, W. F., Skoulakis, E. M., and Rouault, T. A. (2007) Homeostatic mechanisms for iron storage revealed by genetic manipulations and live imaging of Drosophila ferritin. Genetics 177, 89-100 (Pubitemid 47555833)
49. Kamizono, A., Nishizawa, M., Teranishi, Y., Murata, K., and Kimura, A. (1989) Identification of a gene conferring resistance to zinc and cadmium ions in the yeast Saccharomyces cerevisiae. Mol. Gen. Genet. 219, 161-167
50. Li, L., and Kaplan, J. (1998) Defects in the yeast high affinity iron transport system result in increased metal sensitivity because of the increased expression of transporters with a broad transition metal specificity. J. Biol. Chem. 273, 22181-22187 (Pubitemid 28399771)
51. Bruinsma, J. J., Jirakulaporn, T., Muslin, A. J., and Kornfeld, K. (2002) Zinc ions and cation diffusion facilitator proteins regulate Ras-mediated signaling. Dev. Cell. 2, 567-578 (Pubitemid 34538138)
52. Brewer, G. J., Yuzbasiyan-Gurkan, V., and Lee, D. Y. (1990) Use of zinc-copper metabolic interactions in the treatment of Wilson's disease. J. Am. Coll. Nutr. 9, 487-491
53. Brugger, C. (1974) Research on the ultrastructure and function of the anal organ of the normal and lethal (l(3)tr) larvae of the Drosophila melanogaster. J. Insect. Physiol. 20, 121-141
54. Jarial, M. S. (1987) Ultrastructure of the anal organ of Drosophila larva with reference to ion transport. Tissue Cell. 19, 559-575
55. Mehta, A., Deshpande, A., and Missirlis, F. (2008) Genetic screening for novel Drosophila mutants with discrepancies in iron metabolism. Biochem. Soc. Trans. 36, 1313-1316
56. Kirschke, C. P., and Huang, L. (2003) ZnT7, a novel mammalian zinc transporter, accumulates zinc in the Golgi apparatus. J. Biol. Chem. 278, 4096-4102
57. Murgia, C., Vespignani, I., Cerase, J., Nobili, F., and Perozzi, G. (1999) Cloning, expression, and vesicular localization of zinc transporter Dri 27/ZnT4 in intestinal tissue and cells. Am. J. Physiol. 277, G1231-1239 (Pubitemid 30046026)
58. Huang, L., Kirschke, C. P., and Gitschier, J. (2002) Functional characterization of a novel mammalian zinc transporter, ZnT6. J. Biol. Chem. 277, 26389-26395 (Pubitemid 34967132)
59. Michalczyk, A. A., Allen, J., Blomeley, R. C., and Ackland, M. L. (2002) Constitutive expression of hZnT4 zinc transporter in human breast epithelial cells. Biochem. J. 364, 105-113 (Pubitemid 34538952)
60. Monty, J. F., Llanos, R. M., Mercer, J. F., and Kramer, D. R. (2005) Copper exposure induces trafficking of the menkes protein in intestinal epithelium of ATP7A transgenic mice. J. Nutr. 135, 2762-2766
61. Nyasae, L., Bustos, R., Braiterman, L., Eipper, B., and Hubbard, A. (2007) Dynamics of endogenous ATP7A (Menkes protein) in intestinal epithelial cells: copper-dependent redistribution between two intracellular sites. Am. J. Physiol. Gastrointest. Liver Physiol. 292, G1181-G1194 (Pubitemid 46557793)
62. Lutsenko, S., Barnes, N. L., Bartee, M. Y., and Dmitriev, O. Y. (2007) Function and regulation of human copper-transporting ATPases. Physiol. Rev. 87, 1011-1046 (Pubitemid 47084675)
63. McNulty, M., Puljung, M., Jefford, G., and Dubreuil, R. R. (2001) Evidence that a copper-metallothionein complex is responsible for fluorescence in acid-secreting cells of the Drosophila stomach. Cell Tissue Res. 304, 383-389 (Pubitemid 32480569)
64. Poulson, D. F. B. V. (1952) Organization and function of the inorganic constituents of nuclei. Exp. Cell. Res. Suppl. 2, 161-180
65. Hentze, M. W., Muckenthaler, M. U., and Andrews, N. C. (2004) Balancing acts: molecular control of mammalian iron metabolism. Cell 117, 285-297
66. Baer, M. T., and King, J. C. (1984) Tissue zinc levels and zinc excretion during experimental zinc depletion in young men. Am. J. Clin. Nutr. 39, 556-570