Thioredoxin and thioredoxin reductase influence estrogen receptor α-mediated gene expression in human breast cancer cells

Journal of Molecular Endocrinology

Volumn 43, Issue 6, 2009, Pages 251-261

  Rao, Abhi K ^a   Ziegler, Yvonne S ^a   McLeod, Ian X ^b   Yates, John R ^b   Nardulli, Ann M ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; HYDROGEN PEROXIDE; PROTEIN PS2; REACTIVE OXYGEN METABOLITE; THIOREDOXIN; THIOREDOXIN REDUCTASE;

ARTICLE; BREAST CELL; CELL NUCLEUS; CELL STRAIN MCF 7; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; TARGET CELL; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; ESTROGEN RECEPTOR ALPHA; ETHANOL; GENE EXPRESSION; HUMANS; HYDROGEN PEROXIDE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; OXIDATIVE STRESS; PROTEIN BINDING; RNA INTERFERENCE; THIOREDOXIN-DISULFIDE REDUCTASE; THIOREDOXINS;

EID: 69449093242     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1677/JME-09-0053     Document Type: Article

References (84)

1. Altucci L, Addeo R, Cicatiello L, Dauvois S, Parker MG, Truss M, Beato M, Sica V, Bresciani F & Weisz A 1996 17beta-Estradiol induces cyclin D1 gene transcription, p36D1-p34cdk4 complex activation and p105Rb phosphorylation during mitogenic stimulation of G(1)-arrested human breast cancer cells. Oncogene 12 2315-2324. (Pubitemid 26192711)
2. Ando K, Hirao S, Kabe Y, Ogura Y, Sato I, Yamaguchi Y, Wada T & Handa H 2008 A new APE1/Ref-1-dependent pathway leading to reduction of NF-kappaB and AP-1, and activation of their DNA-binding activity. Nucleic Acids Research 36 4327-4336.
3. Arai RJ, Masutani H, Yodoi J, Debbas V, Laurindo FR, Stern A & Monteiro HP 2006 Nitric oxide induces thioredoxin-1 nuclear translocation: possible association with the p21Ras survival pathway. Biochemical and Biophysical Research Communications 348 1254-1260. (Pubitemid 44291340)
4. Arner ES & Holmgren A 2000 Physiological functions of thioredoxin and thioredoxin reductase. European Journal of Biochemistry 267 6102-6109.
5. Arner ES & Holmgren A 2006 The thioredoxin system in cancer. Seminars in Cancer Biology 16 420-426.
6. Atkin JD, Farg MA, Turner BJ, Tomas D, Lysaght JA, Nunan J, Rembach A, Nagley P, Beart PM, Cheema SS et al. 2006 Induction of the unfolded protein response in familial amyotrophic lateral sclerosis and association of protein-disulfide isomerase with superoxide dismutase 1. Journal of Biological Chemistry 281 30152-30165. (Pubitemid 44537023)
7. Beckman JS, Beckman TW, Chen J, Marshall PA & Freeman BA 1990 Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. PNAS 87 1620-1624. (Pubitemid 20080360)
8. Biaglow JE & Miller RA 2005 The thioredoxin reductase/thioredoxin system: novel redox targets for cancer therapy. Cancer Biology and Therapy 4 6-13. (Pubitemid 41350919)
9. Burdon RH 1995 Superoxide and hydrogen peroxide in relation to mammalian cell proliferation. Free Radical Biology and Medicine 18 775-794.
10. Carroll JS, Liu XS, Brodsky AS, Li W, Meyer CA, Szary AJ, Eeckhoute J, Shao W, Hestermann EV, Geistlinger TR et al. 2005 Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 122 33-43. (Pubitemid 40977938)
11. Cheung PY, Churchich JE & Lee KS 1999 Refolding of thioredoxin reductase assisted by groEL and PDI. Biochemical and Biophysical Research Communications 255 17-22.
12. Creekmore AL, Walt KA, Schultz-Norton JR, Ziegler YS, McLeod IX, Yates JR & Nardulli AM 2008 The role of retinoblastoma associated proteins 46 and 48 in estrogen receptor alpha mediated gene expression. Molecular and Cellular Endocrinology 291 79-86.
13. Curtis CD, Likhite VS, McLeod IX, Yates JR & Nardulli AM 2007 Interaction of thetumormetastasis suppressornonmetastatic protein 23 homologue H1 and estrogen receptor alpha alters estrogen-responsive gene expression. Cancer Research 67 10600-10607.
14. Curtis CD, Thorngren DL, Ziegler YS, Sarkeshik A, Yates JR & Nardulli AM 2009 Apurinic/apyrimidinic endonuclease 1 alters estrogen receptor activity and estrogen responsive gene expression. Molecular Endocrinology 23 1346-1359.
15. Das KC, Lewis-Molock Y & White CW 1997 Elevation of manganese superoxide dismutase gene expression by thioredoxin. American Journal of Respiratory Cell and Molecular Biology 17 713-726. (Pubitemid 127348662)
16. Deroo BJ, Hewitt SC, Peddada SD & Korach KS 2004 Estradiol regulates the thioredoxin antioxidant system in the mouse uterus. Endocrinology 145 5485-5492.
17. Druege PM, Klein-Hitpass L, Green S, Stack G, Chambon P & Ryffel GU 1986 Introduction of estrogen-responsiveness into mammalian cell lines. Nucleic Acids Research 14 9329-9337. (Pubitemid 17220803)
18. Eckert RL & Katzenellenbogen BS 1982 Effects of estrogens and antiestrogens on estrogen receptor dynamics and the induction of progesterone receptor in MCF-7 breast cancer cells. Cancer Research 42 139-144.
19. Feinendegen LE 2005 Evidence for beneficial low level radiation effects and radiation hormesis. British Journal of Radiology 78 3-7.
20. Felty Q, Xiong WC, Sun D, Sarkar S, Singh KP, Parkash J & Roy D 2005 Estrogen-induced mitochondrial reactive oxygen species as signal-transducing messengers. Biochemistry 44 6900-6909. (Pubitemid 40632408)
21. Finkel T & Holbrook NJ 2000 Oxidants, oxidative stress and the biology of ageing. Nature 408 239-247. (Pubitemid 30839429)
22. Fujino G, Noguchi T, Takeda K & Ichijo H 2006 Thioredoxin and protein kinases in redox signaling. Seminars in Cancer Biology 16 427-435. (Pubitemid 44794596)
23. Goldstein BJ, Mahadev K, Wu X, Zhu L & Motoshima H 2005 Role of insulin-induced reactive oxygen species in the insulin signaling pathway. Antioxidants & Redox Signaling 7 1021-1031. (Pubitemid 40973798)
24. Green S, Walter P, Kumar V, Krust A, Bornert J-M, Argos P & Chambon P 1986 Human oestrogen receptor cDNA: sequence, expression and homology to v-erb-A. Nature 320 134-139. (Pubitemid 16105150)
25. Greene GL, Gilna P, Waterfield M, Baker A, Hort Y & Shine J 1986 Sequence and expression of human estrogen receptor complementary DNA. Science 231 1150-1154. (Pubitemid 16016313)
26. Halliwell B & Gutteridge JM 1985 The importance of free radicals and catalytic metal ions in human diseases. Molecular Aspects of Medicine 8 89-193. (Pubitemid 16224567)
27. Harman D 1956 Aging: a theory based on free radical and radiation chemistry. Journal of Gerontology 11 298-300.
28. Harman D 2001 Aging: overview. Annals of the New York Academy of Sciences 928 1-21.
29. Hashemy SI, Ungerstedt JS, Zahedi Avval F & Holmgren A 2006 Motexafin gadolinium, a tumor-selective drug targeting thioredoxin reductase and ribonucleotide reductase. Journal of Biological Chemistry 281 10691-10697. (Pubitemid 43855490)
30. Hayashi S, Hajiro-Nakanishi K, Makino Y, Eguchi H, Yodoi J & Tanaka H 1997 Functional modulation of estrogen receptor by redox state with reference to thioredoxin as a mediator. Nucleic Acids Research 25 4035-4040. (Pubitemid 27443331)
31. Hirota K, Matsui M, Iwata S, Nishiyama A, Mori K & Yodoi J 1997 AP-1 transcriptional activity is regulated by a direct association between thioredoxin and Ref-1. PNAS 94 3633-3638. (Pubitemid 27180424)
32. Hirota K, Murata M, Sachi Y, Nakamura H, Takeuchi J, Mori K & Yodoi J 1999 Distinct roles of thioredoxin in the cytoplasm and in the nucleus. A two-step mechanism of redox regulation of transcription factor NF-kappaB. Journal of Biological Chemistry 274 27891-27897. (Pubitemid 129527845)
33. Holmgren A 1979 Reduction of disulfides by thioredoxin. Exceptional reactivity of insulin and suggested functions of thioredoxin in mechanism of hormone action. Journal of Biological Chemistry 254 9113-9119. (Pubitemid 10239373)
34. Holmgren A 1985 Thioredoxin. Annual Review of Biochemistry 54 237-271.
35. Holmgren A & Bjornstedt M 1995 Thioredoxin and thioredoxin reductase. Methods in Enzymology 252 199-208.
36. Jakupoglu C, Przemeck G, Schneider M, Moreno S, Mayr N, Hatzopoulos A, de Angelis M, Wurst W, Bornkamm G, Brielmeier M et al. 2005 Cytoplasmic thioredoxin reductase is essential for embryogenesis but dispensable for cardiac development. Molecular and Cellular Biology 25 1980-1988. (Pubitemid 40280160)
37. Jayaraman L, Murthy KG, Zhu C, Curran T, Xanthoudakis S & Prives C 1997 Identification of redox/repair protein Ref-1 as a potent activator of p53. Genes and Development 11 558-570. (Pubitemid 27133376)
38. Katzenellenbogen BS, Kendra KL, Norman MJ & Berthois Y 1987 Proliferation, hormonal responsiveness, and estrogen receptor content of MCF-7 human breast cancer cells grown in the short-term and long-term absence of estrogens. Cancer Research 47 4355-4360. (Pubitemid 17128144)
39. Kim J, Petz LN, Ziegler YS, Wood JR, Potthoff SJ & Nardulli AM 2000 Regulation of the estrogen-responsive pS2 gene in MCF-7 human breast cancer cells. Journal of Steroid Biochemistry and Molecular Biology 74 157-168. (Pubitemid 32121651)
40. Kirkwood T & Austad S 2000 Why do we age? Nature 408 233-238.
41. Lehnert BE & Iyer R 2002 Exposure to low-level chemicals and ionizing radiation: reactive oxygen species and cellular pathways. Human & Experimental Toxicology 21 65-69. (Pubitemid 34591266)
42. Liang X, Lu B, Scott GK, Chang CH, Baldwin MA & Benz CC 1998 Oxidant stress impaired DNA-binding of estrogen receptor from human breast cancer. Molecular and Cellular Endocrinology 146 151-161. (Pubitemid 29003290)
43. Lincoln DT, Ali Emadi EM, Tonissen KF & Clarke FM 2003 The thioredoxin-thioredoxin reductase system: over-expression in human cancer. Anticancer Research 23 2425-2433. (Pubitemid 36897112)
44. Lundstrom J & Holmgren A 1990 Protein disulfide-isomerase is a substrate for thioredoxin reductase and has thioredoxin-like activity. Journal of Biological Chemistry 265 9114-9120. (Pubitemid 20190355)
45. Lyles MM & Gilbert HF 1991 Catalysis of the oxidative folding of ribonuclease A by protein disulfide isomerase: pre-steady-state kinetics and the utilization of the oxidizing equivalents of the isomerase. Biochemistry 30 619-625.
46. Makino Y, Okamoto K, Yoshikawa N, Aoshima M, Hirota K, Yodoi J, Umesono K, Makino I & Tanaka H 1996 Thioredoxin: a redox-regulating cellular cofactor for glucocorticoid hormone action. Cross talk between endocrine control of stress response and cellular antioxidant defense system. Journal of Clinical Investigation 98 2469-2477. (Pubitemid 26415067)
47. Maruyama T, Kitaoka Y, Sachi Y, Nakanoin K, Hirota K, Shiozawa T, Yoshimura Y, Fujii S & Yodoi J 1997 Thioredoxin expression in the human endometrium during the menstrual cycle. Molecular Human Reproduction 3 989-993. (Pubitemid 127509965)
48. Maruyama T, Sachi Y, Furuke K, Kitaoka Y, Kanzaki H, Yoshimura Y & Yodoi J 1999 Induction of thioredoxin, a redox-active protein, by ovarian steroid hormones during growth and differentiation of endometrial stromal cells in vitro. Endocrinology 140 365-372. (Pubitemid 29011181)
49. Matsui M, Oshima M, Oshima H, Takaku K, Maruyama T, Yodoi J & Taketo MM 1996 Early embryonic lethality caused by targeted disruption of the mouse thioredoxin gene. Developmental Biology 178 179-185. (Pubitemid 26297250)
50. Matthews JR, Wakasugi N, Virelizier JL, Yodoi J & Hay RT 1992 Thioredoxin regulates the DNA binding activity of NF-kappa B by reduction of a disulphide bond involving cysteine 62. Nucleic Acids Research 20 3821-3830.
51. Mobley JA & Brueggemeier RW 2004 Estrogen receptor-mediated regulation of oxidative stress and DNA damage in breast cancer. Carcinogenesis 25 3-9. (Pubitemid 38128614)
52. Mustacich D & Powis G 2000 Thioredoxin reductase. Biochemical Journal 346 1-8.
53. Nardulli AM, Greene GL, O'Malley BW & Katzenellenbogen BS 1988 Regulation of progesterone receptor messenger ribonucleic acid and protein levels in MCF-7 cells by estradiol: analysis of estrogen's effect on progesterone receptor synthesis and degradation. Endocrinology 122 935-944.
54. Nishi T, Shimizu N, Hiramoto M, Sato I, Yamaguchi Y, Hasegawa M, Aizawa S, Tanaka H, Kataoka K, Watanabe H et al. 2002 Spatial redox regulation of a critical cysteine residue of NF-kappa B in vivo. Journal of Biological Chemistry 277 44548-44556.
55. Noiva R, Freedman RB & Lennarz WJ 1993 Peptide binding to protein disulfide isomerase occurs at a site distinct from the active sites. Journal of Biological Chemistry 268 19210-19217. (Pubitemid 23270690)
56. Nordberg J & Arner ES 2001 Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radical Biology and Medicine 31 1287-1312. (Pubitemid 33145299)
57. Osborne LJ, Tonissen KF, Tang VH & Clarke FM 2001 Expression and localisation of thioredoxin in mouse reproductive tissues during the oestrous cycle. Molecular Reproduction and Development 58 359-367.
58. Powell C, Swenberg J & Rusyn I 2005 Expression of base excision DNA repair genes as a biomarker of oxidative DNA damage. Cancer Letters 229 1-11. (Pubitemid 41262535)
59. Puig A, Lyles MM, Noiva R & Gilbert HF 1994 The role of the thiol/disulfide centers and peptide binding site in the chaperone and anti-chaperone activities of protein disulfide isomerase. Journal of Biological Chemistry 269 19128-19135. (Pubitemid 24226236)
60. Quan H, Fan G & Wang CC 1995 Independence of the chaperone activity of protein disulfide isomerase from its thioredoxin-like active site. Journal of Biological Chemistry 270 17078-17080.
61. Rao AK, Ziegler YS, McLeod IX, Yates JR & Nardulli AM 2008 Effects of Cu/Zn superoxide dismutase on estrogen responsiveness and oxidative stress in human breast cancer cells. Molecular Endocrinolgy 22 1113-1124.
62. Salganik RI 2001 The benefits and hazards of antioxidants: controlling apoptosis and other protective mechanisms in cancer patients and the human population. Journal of the American College of Nutrition 20 464S-472S (discussion 473S-475S).
63. Schultz-Norton JR, McDonald WH, Yates JR & Nardulli AM 2006 Protein disulfide isomerase serves as a molecular chaperone to maintain estrogen receptor {alpha} structure and function. Molecular Endocrinology 20 1982-1995.
64. Schultz-Norton JR, Walt KA, Ziegler YS, McLeod IX, Yates JR, Raetzman LT & Nardulli AM 2007 The deoxyribonucleic acid repair protein flap endonuclease-1 modulates estrogen-responsive gene expression. Molecular Endocrinology 21 1569-1580.
65. Schultz-Norton JR, Ziegler YS, Likhite VS, Yates JR & Nardulli AM 2008 Isolation of novel coregulatory protein networks associated with DNA-bound estrogen receptor alpha. BMC Molecular Biology 9 97.
66. Schultz-Norton JR, Ziegler YS, Likhite VS & Nardulli AM 2009 Isolation of proteins associated with the DNA-bound estrogen receptor a. In Molecular Endocrinology: A Comprehensive Guide to Current Methodologies, Eds O-K Park Sarge & T Curry. Totowa, NJ, USA: Humana Press.
67. Smart DK, Ortiz KL, Mattson D, Bradbury CM, Bisht KS, Sieck LK, Brechbiel MW & Gius D 2004 Thioredoxin reductase as a potential molecular target for anticancer agents that induce oxidative stress. Cancer Research 64 6716-6724. (Pubitemid 39297934)
68. Storz G, Tartaglia LA, Farr SB & Ames BN 1990 Bacterial defenses against oxidative stress. Trends in Genetics 6 363-368. (Pubitemid 20354471)
69. Stossi F, Likhite VS, Katzenellenbogen JA & Katzenellenbogen BS 2006 Estrogen-occupied estrogen receptor represses cyclin G2 gene expression and recruits a repressor complex at the cyclin G2 promoter. Journal of Biological Chemistry 281 16272-16278. (Pubitemid 43909575)
70. Sun QA, Wu Y, Zappacosta F, Jeang KT, Lee BJ, Hatfield DL & Gladyshev VN 1999 Redox regulation of cell signaling by selenocysteine in mammalian thioredoxin reductases. Journal of Biological Chemistry 274 24522-24530. (Pubitemid 129529330)
71. Tam NN, Gao Y, Leung YK & Ho SM 2003 Androgenic regulation of oxidative stress in the rat prostate: involvement of NAD(P)H oxidases and antioxidant defense machinery during prostatic involution and regrowth. American Journal of Pathology 163 2513-2522. (Pubitemid 37466492)
72. Toussaint O, Royer V, Salmon M & Remacle J 2002 Stress-induced premature senescence and tissue ageing. Biochemical Pharmacology 64 1007-1009. (Pubitemid 35232276)
73. Turano C, Coppari S, Altieri F & Ferraro A 2002 Proteins of the PDI family: unpredicted non-ER locations and functions. Journal of Cellular Physiology 193 154-163.
74. Turunen N, Karihtala P, Mantyniemi A, Sormunen R, Holmgren A, Kinnula VL & Soini Y 2004 Thioredoxin is associated with proliferation, p53 expression and negative estrogen and progesterone receptor status in breast carcinoma. Acta Pathologica et Microbiologica Scandinavica 112 123-132. (Pubitemid 38406686)
75. Ueno M, Masutani H, Arai RJ, Yamauchi A, Hirota K, Sakai T, Inamoto T, Yamaoka Y, Yodoi J & Nikaido T 1999 Thioredoxin-dependent redox regulation of p53-mediated p21 activation. Journal of Biological Chemistry 274 35809-35815. (Pubitemid 129512885)
76. Urig S & Becker K 2006 On the potential of thioredoxin reductase inhibitors for cancer therapy. Seminars in Cancer Biology 16 452-465. (Pubitemid 44780136)
77. Wang CC & Tsou CL 1993 Protein disulfide isomerase is both an enzyme and a chaperone. FASEB Journal 7 1515-1517. (Pubitemid 24003272)
78. Webster KA, Prentice H & Bishopric NH 2001 Oxidation of zinc finger transcription factors: physiological consequences. Antioxidants and Redox Signaling 3 535-548. (Pubitemid 32785979)
79. Wei SJ, Botero A, Hirota K, Bradbury CM, Markovina S, Laszlo A, Spitz DR, Goswami PC, Yodoi J & Gius D 2000 Thioredoxin nuclear translocation and interaction with redox factor-1 activates the activator protein-1 transcription factor in response to ionizing radiation. Cancer Research 60 6688-6695.
80. Westley BR & May FE 1987 Oestrogen regulates cathepsin D mRNA levels in oestrogen responsive human breast cancer cells. Nucleic Acids Research 15 3773-3786.
81. Wood JR, Likhite VS, Loven MA & Nardulli AM 2001 Allosteric modulation of estrogen receptor conformation by different estrogen response elements. Molecular Endocrinology 15 1114-1126. (Pubitemid 32614066)
82. Wu X, Bishopric NH, Discher DJ, Murphy BJ & Webster KA 1996 Physical and functional sensitivity of zinc finger transcription factors to redox change. Molecular and Cellular Biology 16 1035-1046. (Pubitemid 26061675)
83. Xanthoudakis S & Curran T 1992 Identification and characterization of Ref-1, a nuclear protein that facilitates AP-1 DNA-binding activity. EMBO Journal 11 653-665.
84. Yoshida T, Oka S, Masutani H, Nakamura H & Yodoi J 2003 The role of thioredoxin in the aging process: involvement of oxidative stress. Antioxidants and Redox Signaling 5 563-570. (Pubitemid 37315143)