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this study, a virtually complete deletion of Mtf1 in the liver of adult, pI–pC-induced Mtf1Mx-cre mice did not detectably affect the phenotype of the respective mice under non-stress conditions, confirming that MTF-1 is dispensable in the adult liver (26), in contrast to its essential role in embryonic liver development (23).\nThe comparison of gene expression in livers of mock- or cadmium-treated Mtf1Mx-cre and Mtf1loxP mice revealed several MTF-1 target gene candidates. Transcripts of the two stress-responsive metallothionein genes Mt1 and Mt2 were severely reduced, in support of a crucial role of MTF-1 for both basal and metal-induced expression of metallothioneins (4,6).\nOne of the newly found target genes is Sepw1. The exact molecular function of SEPW1 protein is unknown to date, but a role as antioxidant has been proposed due to its ability to bind glutathione (35). In accordance with this, ectopic expression of mouse Sepw1 renders cells resistant to hydrogen peroxide, and this resistance is dependent on it binding glutathione (36). Furthermore, Amantana et al. (49) showed that expression of a reporter gene fused to a rat Sepw1 promoter fragment can be induced in rat glial cells by copper and zinc, but not cadmium. This response was dependent on an overlapping-inverted MRE sequence located proximal to the rat Sepw1 transcription start (49), even though initial studies failed to demonstrate MTF-1 binding to that sequence (50). Our expression and DNA-binding studies strongly suggest that MTF-1 is important for the basal expression of mouse Sepw1 by binding to the corresponding overlapping-inverted MRE sequence.\nNdrg1, another interesting MTF-1 target gene was named N-myc downstream regulated gene 1 following the discovery that the transcription factor N-myc represses the expression of mouse Ndrg1 (51). Transcription of Ndrg1 and/or its human ortholog is induced by different physiological and cell stress conditions, such as androgens, nickel compounds, DNA damage and hypoxia (37–40,52,53). In addition, the protein is overexpressed in human cancers of many tissues, such as lung, liver, brain, breast, kidney and skin (40). Although Ndrg1 and especially its human ortholog have been quite intensely studied, its function remains unclear; however, the induction by stimuli like nickel and hypoxia suggests an involvement in the cell stress response. Such a role is strongly endorsed by our finding that Ndrg1 gene expression is also induced by cadmium, and that MTF-1 plays a crucial role in this induction.\nIn the case of Csrp1, expression analyses and DNA-binding studies indicate that MTF-1 is required for cadmium induction by binding to an MRE upstream of the transcription start. Studies with human, avian and chicken CSRP1 have shown that this protein is localized at adhesion plaques and in association with filamentous actin, and interacts with the adhesion plaque protein zyxin, as well as the actin-cross-linking protein alpha-actinin (54–57). The ability to bind these partners suggests a role in cytoskeletal organization (58). Exposure of cultured cells to cadmium causes a decrease in, and destruction of, cellular contact proteins and the actin cytoskeleton (59). In the proximal tubule cells of the rat kidney, a partial loss of actin and the actin-bundling protein villin is observed upon cadmium treatment, as well as the derangement and depolymerization of microtubules (60). Assuming that CSRP1 is important for the organization of cytoskeletal elements in the mouse, its upregulation by cadmium might protect the organism from damage of the cytoskeleton. Such a mechanism would expand the role of MTF-1 in stress response.\nOur expression studies also suggest that MTF-1 represses basal transcription of Slc39a10, in contrast to its role as activator for the expression of other target genes like Mt1, Mt2, and Znt1 (4,19). SLC39A10 is one of 14 mouse SLC39 members, which belong to the ZIP family of metal ion transporters (43,44). All members of the ZIP family characterized so far increase intracellular cytoplasmic metal ion concentrations by promoting extracellular and vesicular ion transport into the cytoplasm. ZIP proteins have been reported to be transporters of zinc, iron, manganese and/or cadmium (44,61–63). Although SLC39A10 is largely uncharacterized (44), it is referred to in several databases as putative zinc transporter. It has been previously shown that MTF-1 is important for both basal expression and metal induction of the mouse Znt1 gene (19). ZnT proteins represent a different family of transporters that reduce intracellular cytoplasmic zinc by promoting zinc efflux from cells or into intracellular vesicles. Thus, members of the ZnT and ZIP family with zinc as predominant substrate have opposite roles in cellular zinc homeostasis (43). Assuming that SLC39A10 is indeed a zinc transporter, MTF-1 would control expression of two zinc transporters with antagonistic functions, namely, Znt1 and Slc39a10. Specific binding of MTF-1 was observed for an MRE located just downstream of the Slc39a10 transcription start. In a simple model, such a binding could interfere with the accessibility of the transcriptional start site for RNA polymerase II and/or general transcription factors, thus preventing transcription initiation of the gene. Indeed, such a mechanism has been described in yeast for the zinc-responsive activator protein 1 (Zap1) and its target gene, zinc-regulated transporter 2 (ZRT2) (64). However, the inhibition of Slc39a10 expression by MTF-1 may well be more complex than a competition for promoter binding. Independent of MTF-1, cadmium treatment also leads to downregulation of Slc39a10 transcripts, suggesting that some other factor is mediating this response.\nA previous target gene search for MTF-1 with mouse embryos of conventional Mtf1 knockout phenotype revealed, besides metallothionein genes, the multifunctional alpha-fetoprotein (Afp) and the liver-enriched transcription factor CCAAT/enhancer binding protein alpha (Cebpa) as prime candidates (65). After an early onset during hepatogenesis, Afp expression is repressed postnatally and replaced by albumin (66). Thus, our adult Mtf1Mx-cre mice lacking MTF-1 were not suitable to analyze Afp expression. Cebpa is expressed in the adult liver as well as in other tissues (67), but the present microarray data revealed no significant expression differences in livers from adult Mtf1loxP and Mtf1Mx-cre mice (data not shown). Therefore, MTF-1 may affect Cebpa expression only during embryonal development, perhaps in combination with as yet unidentified factors.\nThe present study confirms and extends the role of MTF-1 as an important stress response regulator. We have identified and preliminarily characterized four target genes of MTF-1 in the adult mouse liver: in the case of Sepw1, MTF-1 is required to maintain basal expression, supporting a role of mouse MTF-1 in oxidative stress response. In addition, MTF-1 contributes to the cadmium-induced expression of Ndrg1 and Csrp1. Furthermore, MTF-1 helps to repress the basal expression of Slc39a10, in contrast to its role as transcriptional activator for genes like Mt1, Mt2 or Znt1. Thus the same transcription factor apparently serves as an activator or repressor, depending on the target gene.\nThe comparison of liver gene expression of cadmium- and mock-treated mice also revealed a number of genes that were responsive to cadmium exposure, independent of the presence or absence of MTF-1. Evidence suggests that the production of reactive oxygen species is a major effect of acute cadmium toxicity (68,69), and exposure of cultured cells or animals to cadmium is associated with depletion of reduced glutathione, lipid peroxidation and DNA damage (70–73). Oxidative stress and the subsequent restoration of cellular homeostasis have been shown to induce the expression of genes encoding acute-phase proteins and antioxidant enzymes (74). In mammals, cadmium tends to accumulate in the kidney and liver as a cadmium-metallothionein complex that has an extremely slow turnover (75,76). Furthermore, metallothioneins provide protection against oxidative stress (1,17). In addition to metallothioneins, glutathione was postulated as a first line of defense against cadmium toxicity (77). Glutathione efficiently complexes cadmium (78) and scavenges free radicals and other reactive oxygen species directly, and indirectly via enzymatic reactions (45). In such reactions, glutathione is oxidized and has to be regenerated by glutathione reductase. Also, glutathione-S-transferases mediate the conjugation of various electrophiles to glutathione. The observed cadmium-induced upregulation of Gclc, Gsr and Gstm4 supports the importance of glutathione in the cellular cadmium response. The enhanced sensitivity to cadmium toxicity that we found for mouse embryonic fibroblasts upon a combination of Mtf1 deletion and depletion of glutathione further corroborates the importance of MTF-1 and its target genes as well as reduced glutathione for an efficient anti-cadmium defense.\nOur data provide strong evidence for at least two branches of cellular anti-cadmium defense, one via MTF-1 and its target genes, notably metallothioneins, the other via glutathione, with an apparent overlap in Sepw1."}

{"project":"2_test","denotations":[{"id":"16221973-15226267-77403445","span":{"begin":266,"end":268},"obj":"15226267"},{"id":"16221973-9582278-77403446","span":{"begin":337,"end":339},"obj":"9582278"},{"id":"16221973-8026472-77403447","span":{"begin":691,"end":692},"obj":"8026472"},{"id":"16221973-11746217-77403448","span":{"begin":693,"end":694},"obj":"11746217"},{"id":"16221973-8576706-77403449","span":{"begin":893,"end":895},"obj":"8576706"},{"id":"16221973-12062442-77403450","span":{"begin":1063,"end":1065},"obj":"12062442"},{"id":"16221973-12161305-77403451","span":{"begin":1098,"end":1100},"obj":"12161305"},{"id":"16221973-12161305-77403452","span":{"begin":1377,"end":1379},"obj":"12161305"},{"id":"16221973-15337603-77403453","span":{"begin":1464,"end":1466},"obj":"15337603"},{"id":"16221973-10381566-77403454","span":{"begin":1846,"end":1848},"obj":"10381566"},{"id":"16221973-9605764-77403455","span":{"begin":2027,"end":2029},"obj":"9605764"},{"id":"16221973-10910041-77403455","span":{"begin":2027,"end":2029},"obj":"10910041"},{"id":"16221973-11059752-77403455","span":{"begin":2027,"end":2029},"obj":"11059752"},{"id":"16221973-15341671-77403455","span":{"begin":2027,"end":2029},"obj":"15341671"},{"id":"16221973-9766676-77403456","span":{"begin":2033,"end":2035},"obj":"9766676"},{"id":"16221973-10428464-77403457","span":{"begin":2036,"end":2038},"obj":"10428464"},{"id":"16221973-15341671-77403458","span":{"begin":2170,"end":2172},"obj":"15341671"},{"id":"16221973-1469049-77403459","span":{"begin":2997,"end":2999},"obj":"1469049"},{"id":"16221973-8294495-77403459","span":{"begin":2997,"end":2999},"obj":"8294495"},{"id":"16221973-9314536-77403459","span":{"begin":2997,"end":2999},"obj":"9314536"},{"id":"16221973-10926853-77403459","span":{"begin":2997,"end":2999},"obj":"10926853"},{"id":"16221973-10090149-77403460","span":{"begin":3086,"end":3088},"obj":"10090149"},{"id":"16221973-12518998-77403461","span":{"begin":3225,"end":3227},"obj":"12518998"},{"id":"16221973-11522379-77403462","span":{"begin":3441,"end":3443},"obj":"11522379"},{"id":"16221973-8026472-77403463","span":{"begin":3888,"end":3889},"obj":"8026472"},{"id":"16221973-10952993-77403464","span":{"begin":3890,"end":3892},"obj":"10952993"},{"id":"16221973-15189117-77403465","span":{"begin":3996,"end":3998},"obj":"15189117"},{"id":"16221973-10681536-77403466","span":{"begin":4285,"end":4287},"obj":"10681536"},{"id":"16221973-14525987-77403466","span":{"begin":4285,"end":4287},"obj":"14525987"},{"id":"16221973-15722412-77403466","span":{"begin":4285,"end":4287},"obj":"15722412"},{"id":"16221973-10952993-77403467","span":{"begin":4536,"end":4538},"obj":"10952993"},{"id":"16221973-15189117-77403468","span":{"begin":4835,"end":4837},"obj":"15189117"},{"id":"16221973-14976557-77403469","span":{"begin":5499,"end":5501},"obj":"14976557"},{"id":"16221973-11266553-77403470","span":{"begin":6076,"end":6078},"obj":"11266553"},{"id":"16221973-10202132-77403471","span":{"begin":6189,"end":6191},"obj":"10202132"},{"id":"16221973-12006103-77403472","span":{"begin":6352,"end":6354},"obj":"12006103"},{"id":"16221973-11895129-77403473","span":{"begin":7639,"end":7641},"obj":"11895129"},{"id":"16221973-11394715-77403474","span":{"begin":7642,"end":7644},"obj":"11394715"},{"id":"16221973-9149117-77403475","span":{"begin":7788,"end":7790},"obj":"9149117"},{"id":"16221973-8560492-77403475","span":{"begin":7788,"end":7790},"obj":"8560492"},{"id":"16221973-8981039-77403475","span":{"begin":7788,"end":7790},"obj":"8981039"},{"id":"16221973-9931285-77403475","span":{"begin":7788,"end":7790},"obj":"9931285"},{"id":"16221973-10331077-77403476","span":{"begin":7973,"end":7975},"obj":"10331077"},{"id":"16221973-1746026-77403477","span":{"begin":8116,"end":8118},"obj":"1746026"},{"id":"16221973-9187512-77403478","span":{"begin":8119,"end":8121},"obj":"9187512"},{"id":"16221973-9671693-77403479","span":{"begin":8199,"end":8200},"obj":"9671693"},{"id":"16221973-10605938-77403480","span":{"begin":8201,"end":8203},"obj":"10605938"},{"id":"16221973-2887478-77403481","span":{"begin":8319,"end":8321},"obj":"2887478"},{"id":"16221973-8068556-77403482","span":{"begin":8367,"end":8369},"obj":"8068556"},{"id":"16221973-14988435-77403483","span":{"begin":8483,"end":8485},"obj":"14988435"}],"text":"DISCUSSION\nIn this study, a virtually complete deletion of Mtf1 in the liver of adult, pI–pC-induced Mtf1Mx-cre mice did not detectably affect the phenotype of the respective mice under non-stress conditions, confirming that MTF-1 is dispensable in the adult liver (26), in contrast to its essential role in embryonic liver development (23).\nThe comparison of gene expression in livers of mock- or cadmium-treated Mtf1Mx-cre and Mtf1loxP mice revealed several MTF-1 target gene candidates. Transcripts of the two stress-responsive metallothionein genes Mt1 and Mt2 were severely reduced, in support of a crucial role of MTF-1 for both basal and metal-induced expression of metallothioneins (4,6).\nOne of the newly found target genes is Sepw1. The exact molecular function of SEPW1 protein is unknown to date, but a role as antioxidant has been proposed due to its ability to bind glutathione (35). In accordance with this, ectopic expression of mouse Sepw1 renders cells resistant to hydrogen peroxide, and this resistance is dependent on it binding glutathione (36). Furthermore, Amantana et al. (49) showed that expression of a reporter gene fused to a rat Sepw1 promoter fragment can be induced in rat glial cells by copper and zinc, but not cadmium. This response was dependent on an overlapping-inverted MRE sequence located proximal to the rat Sepw1 transcription start (49), even though initial studies failed to demonstrate MTF-1 binding to that sequence (50). Our expression and DNA-binding studies strongly suggest that MTF-1 is important for the basal expression of mouse Sepw1 by binding to the corresponding overlapping-inverted MRE sequence.\nNdrg1, another interesting MTF-1 target gene was named N-myc downstream regulated gene 1 following the discovery that the transcription factor N-myc represses the expression of mouse Ndrg1 (51). Transcription of Ndrg1 and/or its human ortholog is induced by different physiological and cell stress conditions, such as androgens, nickel compounds, DNA damage and hypoxia (37–40,52,53). In addition, the protein is overexpressed in human cancers of many tissues, such as lung, liver, brain, breast, kidney and skin (40). Although Ndrg1 and especially its human ortholog have been quite intensely studied, its function remains unclear; however, the induction by stimuli like nickel and hypoxia suggests an involvement in the cell stress response. Such a role is strongly endorsed by our finding that Ndrg1 gene expression is also induced by cadmium, and that MTF-1 plays a crucial role in this induction.\nIn the case of Csrp1, expression analyses and DNA-binding studies indicate that MTF-1 is required for cadmium induction by binding to an MRE upstream of the transcription start. Studies with human, avian and chicken CSRP1 have shown that this protein is localized at adhesion plaques and in association with filamentous actin, and interacts with the adhesion plaque protein zyxin, as well as the actin-cross-linking protein alpha-actinin (54–57). The ability to bind these partners suggests a role in cytoskeletal organization (58). Exposure of cultured cells to cadmium causes a decrease in, and destruction of, cellular contact proteins and the actin cytoskeleton (59). In the proximal tubule cells of the rat kidney, a partial loss of actin and the actin-bundling protein villin is observed upon cadmium treatment, as well as the derangement and depolymerization of microtubules (60). Assuming that CSRP1 is important for the organization of cytoskeletal elements in the mouse, its upregulation by cadmium might protect the organism from damage of the cytoskeleton. Such a mechanism would expand the role of MTF-1 in stress response.\nOur expression studies also suggest that MTF-1 represses basal transcription of Slc39a10, in contrast to its role as activator for the expression of other target genes like Mt1, Mt2, and Znt1 (4,19). SLC39A10 is one of 14 mouse SLC39 members, which belong to the ZIP family of metal ion transporters (43,44). All members of the ZIP family characterized so far increase intracellular cytoplasmic metal ion concentrations by promoting extracellular and vesicular ion transport into the cytoplasm. ZIP proteins have been reported to be transporters of zinc, iron, manganese and/or cadmium (44,61–63). Although SLC39A10 is largely uncharacterized (44), it is referred to in several databases as putative zinc transporter. It has been previously shown that MTF-1 is important for both basal expression and metal induction of the mouse Znt1 gene (19). ZnT proteins represent a different family of transporters that reduce intracellular cytoplasmic zinc by promoting zinc efflux from cells or into intracellular vesicles. Thus, members of the ZnT and ZIP family with zinc as predominant substrate have opposite roles in cellular zinc homeostasis (43). Assuming that SLC39A10 is indeed a zinc transporter, MTF-1 would control expression of two zinc transporters with antagonistic functions, namely, Znt1 and Slc39a10. Specific binding of MTF-1 was observed for an MRE located just downstream of the Slc39a10 transcription start. In a simple model, such a binding could interfere with the accessibility of the transcriptional start site for RNA polymerase II and/or general transcription factors, thus preventing transcription initiation of the gene. Indeed, such a mechanism has been described in yeast for the zinc-responsive activator protein 1 (Zap1) and its target gene, zinc-regulated transporter 2 (ZRT2) (64). However, the inhibition of Slc39a10 expression by MTF-1 may well be more complex than a competition for promoter binding. Independent of MTF-1, cadmium treatment also leads to downregulation of Slc39a10 transcripts, suggesting that some other factor is mediating this response.\nA previous target gene search for MTF-1 with mouse embryos of conventional Mtf1 knockout phenotype revealed, besides metallothionein genes, the multifunctional alpha-fetoprotein (Afp) and the liver-enriched transcription factor CCAAT/enhancer binding protein alpha (Cebpa) as prime candidates (65). After an early onset during hepatogenesis, Afp expression is repressed postnatally and replaced by albumin (66). Thus, our adult Mtf1Mx-cre mice lacking MTF-1 were not suitable to analyze Afp expression. Cebpa is expressed in the adult liver as well as in other tissues (67), but the present microarray data revealed no significant expression differences in livers from adult Mtf1loxP and Mtf1Mx-cre mice (data not shown). Therefore, MTF-1 may affect Cebpa expression only during embryonal development, perhaps in combination with as yet unidentified factors.\nThe present study confirms and extends the role of MTF-1 as an important stress response regulator. We have identified and preliminarily characterized four target genes of MTF-1 in the adult mouse liver: in the case of Sepw1, MTF-1 is required to maintain basal expression, supporting a role of mouse MTF-1 in oxidative stress response. In addition, MTF-1 contributes to the cadmium-induced expression of Ndrg1 and Csrp1. Furthermore, MTF-1 helps to repress the basal expression of Slc39a10, in contrast to its role as transcriptional activator for genes like Mt1, Mt2 or Znt1. Thus the same transcription factor apparently serves as an activator or repressor, depending on the target gene.\nThe comparison of liver gene expression of cadmium- and mock-treated mice also revealed a number of genes that were responsive to cadmium exposure, independent of the presence or absence of MTF-1. Evidence suggests that the production of reactive oxygen species is a major effect of acute cadmium toxicity (68,69), and exposure of cultured cells or animals to cadmium is associated with depletion of reduced glutathione, lipid peroxidation and DNA damage (70–73). Oxidative stress and the subsequent restoration of cellular homeostasis have been shown to induce the expression of genes encoding acute-phase proteins and antioxidant enzymes (74). In mammals, cadmium tends to accumulate in the kidney and liver as a cadmium-metallothionein complex that has an extremely slow turnover (75,76). Furthermore, metallothioneins provide protection against oxidative stress (1,17). In addition to metallothioneins, glutathione was postulated as a first line of defense against cadmium toxicity (77). Glutathione efficiently complexes cadmium (78) and scavenges free radicals and other reactive oxygen species directly, and indirectly via enzymatic reactions (45). In such reactions, glutathione is oxidized and has to be regenerated by glutathione reductase. Also, glutathione-S-transferases mediate the conjugation of various electrophiles to glutathione. The observed cadmium-induced upregulation of Gclc, Gsr and Gstm4 supports the importance of glutathione in the cellular cadmium response. The enhanced sensitivity to cadmium toxicity that we found for mouse embryonic fibroblasts upon a combination of Mtf1 deletion and depletion of glutathione further corroborates the importance of MTF-1 and its target genes as well as reduced glutathione for an efficient anti-cadmium defense.\nOur data provide strong evidence for at least two branches of cellular anti-cadmium defense, one via MTF-1 and its target genes, notably metallothioneins, the other via glutathione, with an apparent overlap in Sepw1."}

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this study, a virtually complete deletion of Mtf1 in the liver of adult, pI–pC-induced Mtf1Mx-cre mice did not detectably affect the phenotype of the respective mice under non-stress conditions, confirming that MTF-1 is dispensable in the adult liver (26), in contrast to its essential role in embryonic liver development (23).\nThe comparison of gene expression in livers of mock- or cadmium-treated Mtf1Mx-cre and Mtf1loxP mice revealed several MTF-1 target gene candidates. Transcripts of the two stress-responsive metallothionein genes Mt1 and Mt2 were severely reduced, in support of a crucial role of MTF-1 for both basal and metal-induced expression of metallothioneins (4,6).\nOne of the newly found target genes is Sepw1. The exact molecular function of SEPW1 protein is unknown to date, but a role as antioxidant has been proposed due to its ability to bind glutathione (35). In accordance with this, ectopic expression of mouse Sepw1 renders cells resistant to hydrogen peroxide, and this resistance is dependent on it binding glutathione (36). Furthermore, Amantana et al. (49) showed that expression of a reporter gene fused to a rat Sepw1 promoter fragment can be induced in rat glial cells by copper and zinc, but not cadmium. This response was dependent on an overlapping-inverted MRE sequence located proximal to the rat Sepw1 transcription start (49), even though initial studies failed to demonstrate MTF-1 binding to that sequence (50). Our expression and DNA-binding studies strongly suggest that MTF-1 is important for the basal expression of mouse Sepw1 by binding to the corresponding overlapping-inverted MRE sequence.\nNdrg1, another interesting MTF-1 target gene was named N-myc downstream regulated gene 1 following the discovery that the transcription factor N-myc represses the expression of mouse Ndrg1 (51). Transcription of Ndrg1 and/or its human ortholog is induced by different physiological and cell stress conditions, such as androgens, nickel compounds, DNA damage and hypoxia (37–40,52,53). In addition, the protein is overexpressed in human cancers of many tissues, such as lung, liver, brain, breast, kidney and skin (40). Although Ndrg1 and especially its human ortholog have been quite intensely studied, its function remains unclear; however, the induction by stimuli like nickel and hypoxia suggests an involvement in the cell stress response. Such a role is strongly endorsed by our finding that Ndrg1 gene expression is also induced by cadmium, and that MTF-1 plays a crucial role in this induction.\nIn the case of Csrp1, expression analyses and DNA-binding studies indicate that MTF-1 is required for cadmium induction by binding to an MRE upstream of the transcription start. Studies with human, avian and chicken CSRP1 have shown that this protein is localized at adhesion plaques and in association with filamentous actin, and interacts with the adhesion plaque protein zyxin, as well as the actin-cross-linking protein alpha-actinin (54–57). The ability to bind these partners suggests a role in cytoskeletal organization (58). Exposure of cultured cells to cadmium causes a decrease in, and destruction of, cellular contact proteins and the actin cytoskeleton (59). In the proximal tubule cells of the rat kidney, a partial loss of actin and the actin-bundling protein villin is observed upon cadmium treatment, as well as the derangement and depolymerization of microtubules (60). Assuming that CSRP1 is important for the organization of cytoskeletal elements in the mouse, its upregulation by cadmium might protect the organism from damage of the cytoskeleton. Such a mechanism would expand the role of MTF-1 in stress response.\nOur expression studies also suggest that MTF-1 represses basal transcription of Slc39a10, in contrast to its role as activator for the expression of other target genes like Mt1, Mt2, and Znt1 (4,19). SLC39A10 is one of 14 mouse SLC39 members, which belong to the ZIP family of metal ion transporters (43,44). All members of the ZIP family characterized so far increase intracellular cytoplasmic metal ion concentrations by promoting extracellular and vesicular ion transport into the cytoplasm. ZIP proteins have been reported to be transporters of zinc, iron, manganese and/or cadmium (44,61–63). Although SLC39A10 is largely uncharacterized (44), it is referred to in several databases as putative zinc transporter. It has been previously shown that MTF-1 is important for both basal expression and metal induction of the mouse Znt1 gene (19). ZnT proteins represent a different family of transporters that reduce intracellular cytoplasmic zinc by promoting zinc efflux from cells or into intracellular vesicles. Thus, members of the ZnT and ZIP family with zinc as predominant substrate have opposite roles in cellular zinc homeostasis (43). Assuming that SLC39A10 is indeed a zinc transporter, MTF-1 would control expression of two zinc transporters with antagonistic functions, namely, Znt1 and Slc39a10. Specific binding of MTF-1 was observed for an MRE located just downstream of the Slc39a10 transcription start. In a simple model, such a binding could interfere with the accessibility of the transcriptional start site for RNA polymerase II and/or general transcription factors, thus preventing transcription initiation of the gene. Indeed, such a mechanism has been described in yeast for the zinc-responsive activator protein 1 (Zap1) and its target gene, zinc-regulated transporter 2 (ZRT2) (64). However, the inhibition of Slc39a10 expression by MTF-1 may well be more complex than a competition for promoter binding. Independent of MTF-1, cadmium treatment also leads to downregulation of Slc39a10 transcripts, suggesting that some other factor is mediating this response.\nA previous target gene search for MTF-1 with mouse embryos of conventional Mtf1 knockout phenotype revealed, besides metallothionein genes, the multifunctional alpha-fetoprotein (Afp) and the liver-enriched transcription factor CCAAT/enhancer binding protein alpha (Cebpa) as prime candidates (65). After an early onset during hepatogenesis, Afp expression is repressed postnatally and replaced by albumin (66). Thus, our adult Mtf1Mx-cre mice lacking MTF-1 were not suitable to analyze Afp expression. Cebpa is expressed in the adult liver as well as in other tissues (67), but the present microarray data revealed no significant expression differences in livers from adult Mtf1loxP and Mtf1Mx-cre mice (data not shown). Therefore, MTF-1 may affect Cebpa expression only during embryonal development, perhaps in combination with as yet unidentified factors.\nThe present study confirms and extends the role of MTF-1 as an important stress response regulator. We have identified and preliminarily characterized four target genes of MTF-1 in the adult mouse liver: in the case of Sepw1, MTF-1 is required to maintain basal expression, supporting a role of mouse MTF-1 in oxidative stress response. In addition, MTF-1 contributes to the cadmium-induced expression of Ndrg1 and Csrp1. Furthermore, MTF-1 helps to repress the basal expression of Slc39a10, in contrast to its role as transcriptional activator for genes like Mt1, Mt2 or Znt1. Thus the same transcription factor apparently serves as an activator or repressor, depending on the target gene.\nThe comparison of liver gene expression of cadmium- and mock-treated mice also revealed a number of genes that were responsive to cadmium exposure, independent of the presence or absence of MTF-1. Evidence suggests that the production of reactive oxygen species is a major effect of acute cadmium toxicity (68,69), and exposure of cultured cells or animals to cadmium is associated with depletion of reduced glutathione, lipid peroxidation and DNA damage (70–73). Oxidative stress and the subsequent restoration of cellular homeostasis have been shown to induce the expression of genes encoding acute-phase proteins and antioxidant enzymes (74). In mammals, cadmium tends to accumulate in the kidney and liver as a cadmium-metallothionein complex that has an extremely slow turnover (75,76). Furthermore, metallothioneins provide protection against oxidative stress (1,17). In addition to metallothioneins, glutathione was postulated as a first line of defense against cadmium toxicity (77). Glutathione efficiently complexes cadmium (78) and scavenges free radicals and other reactive oxygen species directly, and indirectly via enzymatic reactions (45). In such reactions, glutathione is oxidized and has to be regenerated by glutathione reductase. Also, glutathione-S-transferases mediate the conjugation of various electrophiles to glutathione. The observed cadmium-induced upregulation of Gclc, Gsr and Gstm4 supports the importance of glutathione in the cellular cadmium response. The enhanced sensitivity to cadmium toxicity that we found for mouse embryonic fibroblasts upon a combination of Mtf1 deletion and depletion of glutathione further corroborates the importance of MTF-1 and its target genes as well as reduced glutathione for an efficient anti-cadmium defense.\nOur data provide strong evidence for at least two branches of cellular anti-cadmium defense, one via MTF-1 and its target genes, notably metallothioneins, the other via glutathione, with an apparent overlap in Sepw1."}

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this study, a virtually complete deletion of Mtf1 in the liver of adult, pI–pC-induced Mtf1Mx-cre mice did not detectably affect the phenotype of the respective mice under non-stress conditions, confirming that MTF-1 is dispensable in the adult liver (26), in contrast to its essential role in embryonic liver development (23).\nThe comparison of gene expression in livers of mock- or cadmium-treated Mtf1Mx-cre and Mtf1loxP mice revealed several MTF-1 target gene candidates. Transcripts of the two stress-responsive metallothionein genes Mt1 and Mt2 were severely reduced, in support of a crucial role of MTF-1 for both basal and metal-induced expression of metallothioneins (4,6).\nOne of the newly found target genes is Sepw1. The exact molecular function of SEPW1 protein is unknown to date, but a role as antioxidant has been proposed due to its ability to bind glutathione (35). In accordance with this, ectopic expression of mouse Sepw1 renders cells resistant to hydrogen peroxide, and this resistance is dependent on it binding glutathione (36). Furthermore, Amantana et al. (49) showed that expression of a reporter gene fused to a rat Sepw1 promoter fragment can be induced in rat glial cells by copper and zinc, but not cadmium. This response was dependent on an overlapping-inverted MRE sequence located proximal to the rat Sepw1 transcription start (49), even though initial studies failed to demonstrate MTF-1 binding to that sequence (50). Our expression and DNA-binding studies strongly suggest that MTF-1 is important for the basal expression of mouse Sepw1 by binding to the corresponding overlapping-inverted MRE sequence.\nNdrg1, another interesting MTF-1 target gene was named N-myc downstream regulated gene 1 following the discovery that the transcription factor N-myc represses the expression of mouse Ndrg1 (51). Transcription of Ndrg1 and/or its human ortholog is induced by different physiological and cell stress conditions, such as androgens, nickel compounds, DNA damage and hypoxia (37–40,52,53). In addition, the protein is overexpressed in human cancers of many tissues, such as lung, liver, brain, breast, kidney and skin (40). Although Ndrg1 and especially its human ortholog have been quite intensely studied, its function remains unclear; however, the induction by stimuli like nickel and hypoxia suggests an involvement in the cell stress response. Such a role is strongly endorsed by our finding that Ndrg1 gene expression is also induced by cadmium, and that MTF-1 plays a crucial role in this induction.\nIn the case of Csrp1, expression analyses and DNA-binding studies indicate that MTF-1 is required for cadmium induction by binding to an MRE upstream of the transcription start. Studies with human, avian and chicken CSRP1 have shown that this protein is localized at adhesion plaques and in association with filamentous actin, and interacts with the adhesion plaque protein zyxin, as well as the actin-cross-linking protein alpha-actinin (54–57). The ability to bind these partners suggests a role in cytoskeletal organization (58). Exposure of cultured cells to cadmium causes a decrease in, and destruction of, cellular contact proteins and the actin cytoskeleton (59). In the proximal tubule cells of the rat kidney, a partial loss of actin and the actin-bundling protein villin is observed upon cadmium treatment, as well as the derangement and depolymerization of microtubules (60). Assuming that CSRP1 is important for the organization of cytoskeletal elements in the mouse, its upregulation by cadmium might protect the organism from damage of the cytoskeleton. Such a mechanism would expand the role of MTF-1 in stress response.\nOur expression studies also suggest that MTF-1 represses basal transcription of Slc39a10, in contrast to its role as activator for the expression of other target genes like Mt1, Mt2, and Znt1 (4,19). SLC39A10 is one of 14 mouse SLC39 members, which belong to the ZIP family of metal ion transporters (43,44). All members of the ZIP family characterized so far increase intracellular cytoplasmic metal ion concentrations by promoting extracellular and vesicular ion transport into the cytoplasm. ZIP proteins have been reported to be transporters of zinc, iron, manganese and/or cadmium (44,61–63). Although SLC39A10 is largely uncharacterized (44), it is referred to in several databases as putative zinc transporter. It has been previously shown that MTF-1 is important for both basal expression and metal induction of the mouse Znt1 gene (19). ZnT proteins represent a different family of transporters that reduce intracellular cytoplasmic zinc by promoting zinc efflux from cells or into intracellular vesicles. Thus, members of the ZnT and ZIP family with zinc as predominant substrate have opposite roles in cellular zinc homeostasis (43). Assuming that SLC39A10 is indeed a zinc transporter, MTF-1 would control expression of two zinc transporters with antagonistic functions, namely, Znt1 and Slc39a10. Specific binding of MTF-1 was observed for an MRE located just downstream of the Slc39a10 transcription start. In a simple model, such a binding could interfere with the accessibility of the transcriptional start site for RNA polymerase II and/or general transcription factors, thus preventing transcription initiation of the gene. Indeed, such a mechanism has been described in yeast for the zinc-responsive activator protein 1 (Zap1) and its target gene, zinc-regulated transporter 2 (ZRT2) (64). However, the inhibition of Slc39a10 expression by MTF-1 may well be more complex than a competition for promoter binding. Independent of MTF-1, cadmium treatment also leads to downregulation of Slc39a10 transcripts, suggesting that some other factor is mediating this response.\nA previous target gene search for MTF-1 with mouse embryos of conventional Mtf1 knockout phenotype revealed, besides metallothionein genes, the multifunctional alpha-fetoprotein (Afp) and the liver-enriched transcription factor CCAAT/enhancer binding protein alpha (Cebpa) as prime candidates (65). After an early onset during hepatogenesis, Afp expression is repressed postnatally and replaced by albumin (66). Thus, our adult Mtf1Mx-cre mice lacking MTF-1 were not suitable to analyze Afp expression. Cebpa is expressed in the adult liver as well as in other tissues (67), but the present microarray data revealed no significant expression differences in livers from adult Mtf1loxP and Mtf1Mx-cre mice (data not shown). Therefore, MTF-1 may affect Cebpa expression only during embryonal development, perhaps in combination with as yet unidentified factors.\nThe present study confirms and extends the role of MTF-1 as an important stress response regulator. We have identified and preliminarily characterized four target genes of MTF-1 in the adult mouse liver: in the case of Sepw1, MTF-1 is required to maintain basal expression, supporting a role of mouse MTF-1 in oxidative stress response. In addition, MTF-1 contributes to the cadmium-induced expression of Ndrg1 and Csrp1. Furthermore, MTF-1 helps to repress the basal expression of Slc39a10, in contrast to its role as transcriptional activator for genes like Mt1, Mt2 or Znt1. Thus the same transcription factor apparently serves as an activator or repressor, depending on the target gene.\nThe comparison of liver gene expression of cadmium- and mock-treated mice also revealed a number of genes that were responsive to cadmium exposure, independent of the presence or absence of MTF-1. Evidence suggests that the production of reactive oxygen species is a major effect of acute cadmium toxicity (68,69), and exposure of cultured cells or animals to cadmium is associated with depletion of reduced glutathione, lipid peroxidation and DNA damage (70–73). Oxidative stress and the subsequent restoration of cellular homeostasis have been shown to induce the expression of genes encoding acute-phase proteins and antioxidant enzymes (74). In mammals, cadmium tends to accumulate in the kidney and liver as a cadmium-metallothionein complex that has an extremely slow turnover (75,76). Furthermore, metallothioneins provide protection against oxidative stress (1,17). In addition to metallothioneins, glutathione was postulated as a first line of defense against cadmium toxicity (77). Glutathione efficiently complexes cadmium (78) and scavenges free radicals and other reactive oxygen species directly, and indirectly via enzymatic reactions (45). In such reactions, glutathione is oxidized and has to be regenerated by glutathione reductase. Also, glutathione-S-transferases mediate the conjugation of various electrophiles to glutathione. The observed cadmium-induced upregulation of Gclc, Gsr and Gstm4 supports the importance of glutathione in the cellular cadmium response. The enhanced sensitivity to cadmium toxicity that we found for mouse embryonic fibroblasts upon a combination of Mtf1 deletion and depletion of glutathione further corroborates the importance of MTF-1 and its target genes as well as reduced glutathione for an efficient anti-cadmium defense.\nOur data provide strong evidence for at least two branches of cellular anti-cadmium defense, one via MTF-1 and its target genes, notably metallothioneins, the other via glutathione, with an apparent overlap in Sepw1."}