Metallothionein induction by hypoxia involves cooperative interactions between metal-responsive transcription factor-1 and hypoxia-inducible transcription factor-1α

Molecular Cancer Research

Volumn 6, Issue 3, 2008, Pages 483-490

  Murphy, Brian J ^a   Kimura, Tomoki ^b   Sato, Barbara G ^a   Shi, Yihui ^a   Andrews, Glen K ^c  

^a SRI INTERNATIONAL   (United States)

^b SETSUNAN UNIVERSITY   (Japan)

^c UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; METAL RESPONSIVE TRANSCRIPTION FACTOR 1; METALLOTHIONEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ZINC;

ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HYPOXIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

3T3 CELLS; ANIMALS; CELL HYPOXIA; CELL LINE, TRANSFORMED; DNA-BINDING PROTEINS; GENE DELETION; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; METALLOTHIONEIN; MICE; RNA INTERFERENCE; TRANSCRIPTION FACTORS; ZINC;

MAMMALIA;

EID: 40949105551     PISSN: 15417786     EISSN: None     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-07-0341     Document Type: Article

References (77)

1. Andrews GK. Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochem Pharmacol 2000;59:95-104.
2. Palmiter RD. The elusive function of metallothioneins. Proc Natl Acad Sci U S A 1998;95:8428-30.
3. Penkowa M. Metallothioneins are multipurpose neuroprotectants during brain pathology. FEBS J 2006;273:1857-70.
4. Jin R, Chow VT, Tan PH, Dheen ST, Duan W, Bay BH. Metallothionein 2A expression is associated with cell proliferation in breast cancer. Carcinogenesis 2002;23:81-6.
5. Lazo JS, Pitt BR. Metallothioneins and cell death by anticancer drugs. Annu Rev Pharmacol Toxicol 1995;35:635-53.
6. Shimoda R, Achanzar WE, Qu W, et al. Metallothionein is a potential negative regulator of apoptosis. Toxicol Sci 2003;73:294-300.
7. Cai L. Suppression of nitrative damage by metallothionein in diabetic heart contributes to the prevention of cardiomyopathy. Free Radic Biol Med 2006;41:851-61.
8. Cai L, Wang J, Li Y, et al. Inhibition of superoxide generation and associated nitrosative damage is involved in metallothionein prevention of diabetic cardiomyopathy. Diabetes 2005;54:1829-37.
9. Cai L, Cherian MG. Zinc-metallothionein protects from DNA damage induced by radiation better than glutathione and copper- or cadmium-metallothioneins. Toxicol Lett 2003;136:193-8.
10. Ye B, Maret W, Vallee BL. Zinc metallothionein imported into liver mitochondria modulates respiration. Proc Natl Acad Sci U S A 2001;10.
11. Beattie JH, Wood AM, Newman AM, et al. Obesity and hyperleptinemia in metallothionein (-I and -II) null mice. Proc Natl Acad Sci U S A 1998;95:358-63.
12. Beattie JH, Wood AM, Trayhurn P, et al. Metallothionein is expressed in adipocytes of brown fat and is induced by catecholamines and zinc. Am J Physiol Regul Integr Comp Physiol 2000;278:R1082-9.
13. Inoue K, Takano H, Shimada A, et al. Role of metallothionein in coagulatory disturbance and systemic inflammation induced by lipopolysaccharide in mice. FASEB J 2006;20:533-5.
14. Inoue K, Takano H, Yanagisawa R, et al. Role of metallothionein in antigen-related airway inflammation. Exp Biol Med (Maywood) 2005;230:75-81.
15. Jiang Y, Kang YJ. Metallothionein gene therapy for chemical-induced liver fibrosis in mice. Mol Ther 2004;10:1130-9.
16. Seth D, Leo MA, McGuinness PH, et al. Gene expression profiling of alcoholic liver disease in the baboon (Papio hamadryas) and human liver. Am J Pathol 2003;163:2303-17.
17. Wang L, Zhou Z, Saari JT, Kang YJ. Alcohol-induced myocardial fibrosis in metallothionein-null mice: prevention by zinc supplementation. Am J Pathol 2005;167:337-44.
18. Cherian MG, Kang YJ. Metallothionein and liver cell regeneration. Exp Biol Med (Maywood) 2006;231:138-44.
19. Bay BH, Jin R, Huang J, Tan PH. Metallothionein as a prognostic biomarker in breast cancer. Exp Biol Med (Maywood) 2006;231:1516-21.
20. Murphy BJ. Regulation of malignant progression by the hypoxia-sensitive transcription factors HIF-1α and MTF-1. Comp Biochem Physiol B Biochem Mol Biol 2004;139:495-507.
21. Jin R, Bay B, Tan P, Tan BK. Metallothionein expression and zinc levels in invasive ductal breast carcinoma [In Process Citation]. Oncol Rep 1999;6:871-5.
22. Jasani B, Schmid KW. Significance of metallothionein overexpression in human tumors. Histopathology 1997;31:211-4.
23. Datta J, Majumder S, Kutay H, et al. Metallothionein expression is suppressed in primary human hepatocellular carcinomas and is mediated through inactivation of CCAAT/enhancer binding protein {α} by phosphatidylinositol 3-kinase signaling cascade. Cancer Res 2007;67:2736-46.
24. Cherian MG, Jayasurya A, Bay BH. Metallothioneins in human tumors and potential roles in carcinogenesis. Mutat Res 2003;533:201-9.
25. Lee SS, Yang SF, Ho YC, Tsai CH, Chang YC. The upregulation of metallothionein-1 expression in areca quid chewing-associated oral squamous cell carcinomas. Oral Oncol 2008;44:180-6.
26. Lazo JS, Kuo SM, Woo ES, Pitt BR. The protein thiol metallothionein as an antioxidant and protectant against antineoplastic drugs. Chem Biol Interact 1998;111-2:255-62.
27. Yang M, Kroft SH, Chitambar CR. Gene expression analysis of gallium-resistant and gallium-sensitive lymphoma cells reveals a role for metal-responsive transcription factor-1, metallothionein-2A, and zinc transporter-1 in modulating the antineoplastic activity of gallium nitrate. Mol Cancer Ther 2007;6:633-43.
28. Cai L, Satoh M, Tohyama C, Cherian MG. Metallothionein in radiation exposure: its induction and protective role. Toxicology 1999;132:85-98.
29. Laity JH, Andrews GK. Understanding the mechanisms of zinc-sensing by metal-response element binding transcription factor-1 (MTF-1). Arch Biochem Biophys 2007;463:201-10.
30. Westin G, Schaffner W. A zinc-responsive factor interacts with a metal-regulated enhancer element (MRE) of the mouse metallothionein-I gene. EMBO J 1988;7:3763-70.
31. Jiang H, Daniels PJ, Andrews GK. Putative zinc-sensing zinc fingers of metal-response element-binding transcription factor-1 stabilize a metal-dependent chromatin complex on the endogenous metallothionein-I promoter. J Biol Chem 2003;278:30394-402.
32. Daniels PJ, Andrews GK. Dynamics of the metal-dependent transcription factor complex in vivo at the mouse metallothionein-I promoter. Nucleic Acids Res 2003;31:6710-21.
33. Potter BM, Feng LS, Parasuram P, et al. The six zinc fingers of metal-responsive element-binding transcription factor-1 form stable and quasi-ordered structures with relatively small differences in zinc affinities. J Biol Chem 2005;280:28529-40.
34. Li Y, Kimura T, Laity JH, Andrews GK. The zinc-sensing mechanism of mouse MTF-1 involves linker peptides between the zinc fingers. Mol Cell Biol 2006;26:5580-7.
35. Radtke F, Heuchel R, Georgiev O, et al. Cloned transcription factor MTF-1 activates the mouse metallothionein I promoter. EMBO J 1993;12:1355-62.
36. Wang Y, Lorenzi I, Georgiev O, Schaffner W. Metal-responsive transcription factor-1 (MTF-1) selects different types of metal response elements at low vs. high zinc concentration. Biol Chem 2004;385:623-32.
37. Selvaraj A, Balamurugan K, Yepiskoposyan H, et al. Metal-responsive transcription factor (MTF-1) handles both extremes, copper load and copper starvation, by activating different genes. Genes Dev 2005;19:891-6.
38. Dalton T, Palmiter RD, Andrews GK. Transcriptional induction of the mouse metallothionein-I gene in hydrogen peroxide-treated Hepa cells involves a composite major late transcription factor/antioxidant response element and metal response promoter elements. Nucleic Acids Res 1994;22:5016-23.
39. Dalton T, Fu K, Enders GC, Palmiter RD, Andrews GK. Analysis of the effects of overexpression of metallothionein-I in transgenic mice on the reproductive toxicology of cadmium. Environ Health Perspect 1996;104:68-76.
40. Stitt MS, Wasserloos KJ, Tang X, Liu X, Pitt BR, St Croix CM. Nitric oxide-induced nuclear translocation of the metal responsive transcription factor, MTF-1 is mediated by zinc release from metallothionein. Vascul Pharmacol 2006;44:149-55.
41. Saydam N, Steiner F, Georgiev O, Schaffner W. Heat and heavy metal stress synergize to mediate transcriptional hyperactivation by metal-responsive transcription factor MTF-1. J Biol Chem 2003;278:31879-83.
42. Cousins RJ, Liuzzi JP, Lichten LA. Mammalian zinc transport, trafficking, and signals. J Biol Chem 2006;281:24085-9.
43. Murphy BJ, Andrews GK, Bittel D, et al. Activation of metallothionein gene expression by hypoxia involves metal response elements and metal transcription factor-1. Cancer Res 1999;59:1315-22.
44. 2 in vitro is modulated by metallothionein. Mol Cell Biol 2003;23:8471-85.
45. Castello PR, David PS, McClure T, Crook Z, Poyton RO. Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: implications for oxygen sensing and hypoxic signaling in eukaryotes. Cell Metab 2006;3:277-87.
46. Lichtlen P, Wang Y, Belser T, et al. Target gene search for the metal-responsive transcription factor MTF-1. Nucleic Acids Res 2001;29:1514-23.
47. Green CJ, Lichtlen P, Huynh NT, et al. Placenta growth factor gene expression is induced by hypoxia in fibroblasts: a central role for metal transcription factor-1. Cancer Res 2001;61:2696-703.
48. Haroon ZA, Amin K, Lichtlen P, et al. Loss of metal transcription factor-1 suppresses tumor growth through enhanced matrix deposition. FASEB J 2004;18:1176-84.
49. Wimmer U, Wang Y, Georgiev O, Schaffner W. Two major branches of anticadmium defense in the mouse: MTF-1/metallothioneins and glutathione. Nucleic Acids Res 2005;33:5715-27.
50. Andrews GK, Lee DK, Ravindra R, et al. The transcription factors MTF-1 and USF1 cooperate to regulate mouse metallothionein-I expression in response to the essential metal zinc in visceral endoderm cells during early development. EMBO J 2001;20:1114-22.
51. Wan M, Heuchel R, Radtke F, Hunziker PE, Kagi JH. Regulation of metallothionein gene expression in Cd- or Zn-adapted RK-13 cells. Experientia 1995;51:606-11.
52. Mueller PR, Salser SJ, Wold B. Constitutive and metal-inducible protein: DNA interactions at the mouse metallothionein I promoter examined by in vivo and in vitro footprinting. Genes Dev1988;2:412-27.
53. Dalton T, Qingwen L, Bittel D, Liang L, Andrews GK. Oxidative stress activates metal-responsive transcription factor-1 binding activity. J Biol Chem 1996;271:26233-41.
54. Ghoshal K, Datta J, Majumder S, et al. Inhibitors of histone deacetylase and DNA methyltransferase synergistically activate the methylated metallothionein I promoter by activating the transcription factor MTF-1 and forming an open chromatin structure. Mol Cell Biol 2002;22:8302-19.
55. 2 tension. Proc Natl Acad Sci U S A 1995;92:5510-4.
56. Semenza GL. Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology (Bethesda) 2004;19:176-82.
57. Murphy BJ, Sato BG, Dalton TP, Laderoute KR. The metal-responsive transcription factor-1 contributes to HIF-1 activation during hypoxic stress. Biochem Biophys Res Commun 2005;337:860-7.
58. Greijer A, van der Groep P, Kemming D, et al. Up-regulation of gene expression by hypoxia is mediated predominantly by hypoxia-inducible factor 1 (HIF-1). J Pathol 2005;206:291-304.
59. Semenza GL, Shimoda LA, Prabhakar NR. Regulation of gene expression by HIF-1. Novartis Found Symp 2006;272:2-8; discussion -14, 33-6.
60. Jung JE, Lee HG, Cho IH, et al. STAT3 is a potential modulator of HIF-1-mediated VEGF expression in human renal carcinoma cells. FASEB J 2005;19:1296-8.
61. Liao H, Hyman MC, Lawrence DA, Pinsky DJ. Molecular regulation of the PAI-1 gene by hypoxia: contributions of Egr-1, HIF-1{α}, and C/EBP{α}. FASEB J 2007;21:935-49.
62. Ema M, Hirota K, Mimura J, et al. Molecular mechanisms of transcription activation by HLF and HIF1α in response to hypoxia: their stabilization and redox signal-induced interaction with CBP/p300. EMBO J 1999;18:1905-14.
63. Cramer M, Nagy I, Murphy BJ, et al. NF-κB contributes to transcription of placenta growth factor and interacts with metal responsive transcription factor-1 in hypoxic human cells. Biol Chem 2005;386:865-72.
64. Murphy BJ, Laderoute KR, Chin RJ, Sutherland RM. Methallothionein IIA is up-regulated by hypoxia in human A431 squamous carcinoma cells. Cancer Res 1994;54:5808-10.
65. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003;3:721-32.
66. Semenza GL. Regulation of physiological responses to continuous and intermittent hypoxia by hypoxia-inducible factor 1. Exp Physiol 2006;91:803-6.
67. Semenza GL. Development of novel therapeutic strategies that target HIF-1. Expert Opin Ther Targets 2006;10:267-80.
68. Semenza GL. Hypoxia-inducible factor 1: control of oxygen homeostasis in health and disease. Pediatr Res 2001;49:614-7.
69. Semenza GL. Expression of hypoxia-inducible factor 1: mechanisms and consequences. Biochem Pharmacol 2000;59:47-53.
70. LaRochelle O, Gagne V, Charron J, Soh JW, Seguin C. Phosphorylation is involved in the activation of metal-regulatory transcription factor 1 in response to metal ions. J Biol Chem 2001;276:41879-88.
71. Saydam N, Adams TK, Steiner F, Schaffner W, Freedman JH. Regulation of metallothionein transcription by the metal-responsive transcription factor MTF-1: identification of signal transduction cascades that control metal-inducible transcription. J Biol Chem 2002;277:20438-45.
72. Lee JY, Lee YS, Kim JM, et al. A novel chimeric promoter that is highly responsive to hypoxia and metals. Gene Ther 2006;13:857-68.
73. Smirnova IV, Bittel DC, Ravindra R, Jiang H, Andrews GK. Zinc and cadmium can promote rapid nuclear translocation of metal response element-binding transcription factor-1. J Biol Chem 2000;275:9377-84.
74. Laderoute KR, Calaoagan JM, Knapp M, Johnson RS. Glucose utilization is essential for hypoxia-inducible factor 1 α-dependent phosphorylation of c-Jun. Mol Cell Biol 2004;24:4128-37.
75. Gunes C, Heuchel R, Georgiev O, et al. Embryonic lethality and liver degeneration in mice lacking the metal- responsive transcriptional activator MTF-1. EMBO J 1998;17:2846-54.
76. Jiang H, Fu K, Andrews GK. Gene- and cell-type-specific effects of signal transduction cascades on metal-regulated gene transcription appear to be independent of changes in the phosphorylation of metal-response-element-binding transcription factor-1. Biochem J 2004;382:33-41.
77. Ryan HE, Poloni M, McNulty W, et al. Hypoxia-inducible factor-1α is a positive factor in solid tumor growth. Cancer Res 2000;60:4010-5.