The NrF1 and NrF2 balance in oxidative stress regulation and androgen signaling in prostate cancer cells

Cancers

Volumn 2, Issue 2, 2010, Pages 1354-1378

  Schultz, Michelle A ^a   Abdel Mageed, Asim B ^a   Mondal, Debasis ^a  

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Androgen deprivation therapy; Androgen independence; Androgen receptor (AR); Di hydrotestosterone (DHT); Nrf1 (NF E2 related factor 1); Nrf2 (NF E2 related factor 2); Oxidative stress; Prostate cancer; Reactive oxygen species (ROS)

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; ANTIANDROGEN; PEROXIREDOXIN 1; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; THIOREDOXIN 1; TRANSCRIPTION FACTOR MAFG; TRANSCRIPTION FACTOR NRF1; TRANSCRIPTION FACTOR NRF1 P120 ISOFORM; TRANSCRIPTION FACTOR NRF1 P65 ISOFORM; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ANDROGEN DEPRIVATION THERAPY; BINDING SITE; CANCER CELL CULTURE; CANCER GROWTH; CANCER STAGING; CARCINOGENESIS; DNA RESPONSIVE ELEMENT; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; HORMONAL REGULATION; HORMONE DEPENDENCE; HUMAN; METABOLIC REGULATION; MITOGENESIS; NONHUMAN; OXIDATIVE STRESS; PROSTATE CANCER; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; RECEPTOR UPREGULATION; REVIEW; SIGNAL TRANSDUCTION; TRANSACTIVATION; TRANSCRIPTION REGULATION; TUMOR VASCULARIZATION;

EID: 79952272861     PISSN: None     EISSN: 20726694     Source Type: Journal    
DOI: 10.3390/cancers2021354     Document Type: Review

References (110)

1. Cancer Facts and Figures 2009. American Cancer Society: Atlanta, GA, USA, 2009.
2. Niu, Y.; Chang, T.M.; Yeh, S.; Ma, W.L.; Wang, Y.Z.; Chang, C. Differential androgen receptor signals in different cells explain why androgen-deprivation therapy of prostate cancer fails. Oncogene 2010, doi: 10.1038/onc.2010.121.
3. Perlmutter, M.A.; Lepor, H. Androgen deprivation therapy in the treatment of advanced prostate cancer. Rev. Urol. 2007, 9 (Suppl. 1), S3-S8.
4. Thalmann, G.N.; Anezinis, P.E.; Chang, S.M.; Zhau, H.E.; Kim, E.E.; Hopwood, V.L.; Pathak, S.; von Eschenbach, A.C.; Chung, L.W. Androgen-independent cancer progression and bone metastasis in the LNCaP model of human prostate cancer. Cancer Res. 1994, 54, 2577-2581.
5. Isaacs, J.T. The biology of hormone refractory prostate cancer. Why does it develop? Urol. Clin. North Am. 1999, 26, 263-273.
6. Mellado, B.; Codony, J.; Ribal, M.J.; Visa, L.; Gascon, P. Molecular biology of androgenindependent prostate cancer: the role of the androgen receptor pathway. Clin. Transl. Oncol. 2009, 11, 5-10.
7. Khandrika, L.; Kumar, B.; Koul, S.; Maroni, P.; Koul, H.K. Oxidative stress in prostate cancer. Cancer Lett. 2009, 282, 125-136.
8. Zhang, P.; Singh, A.; Yegnasubramanian, S.; Esopi, D.; Kombairaju, P.; Bodas, M.; Wu, H.; Bova, S.G.; Biswal, S. Loss of Kelch-like ECH-associated protein 1 function in prostate cancer cells causes chemoresistance and radioresistance and promotes tumor growth. Mol. Cancer Ther. 2010, 9, 336-346.
9. Cronauer, M.V.; Schulz, W.A.; Burchardt, T.; Anastasiadis, A.G.; de la Taille, A.; Ackermann, R.; Burchardt, M. The androgen receptor in hormone-refractory prostate cancer: relevance of different mechanisms of androgen receptor signaling (Review). Int. J. Oncol. 2003, 23, 1095-1102.
10. Tamura, K.; Furihata, M.; Tsunoda, T.; Ashida, S.; Takata, R.; Obara, W.; Yoshioka, H.; Daigo, Y.; Nasu, Y.; Kumon, H.; et al. Molecular features of hormone-refractory prostate cancer cells by genome-wide gene expression profiles. Cancer Res. 2007, 67, 5117-5125.
11. Li, R.; Wheeler, T.; Dai, H.; Frolov, A.; Thompson, T.; Ayala, G. High level of androgen receptor is associated with aggressive clinicopathologic features and decreased biochemical recurrence-free survival in prostate: cancer patients treated with radical prostatectomy. Am. J. Surg. Pathol. 2004, 28, 928-934.
12. Yin, H.; Radomska, H.S.; Tenen, D.G.; Glass, J. Down regulation of PSA by C/EBPalpha is associated with loss of AR expression and inhibition of PSA promoter activity in the LNCaP cell line. BMC Cancer 2006, 6, 158.
13. Khandrika, L.; Lieberman, R.; Koul, S.; Kumar, B.; Maroni, P.; Chandhoke, R.; Meacham, R.B.; Koul, H.K. Hypoxia-associated p38 mitogen-activated protein kinase-mediated androgen receptor activation and increased HIF-1alpha levels contribute to emergence of an aggressive phenotype in prostate cancer. Oncogene 2009, 28, 1248-1260.
14. Mehraein-Ghomi, F.; Lee, E.; Church, D.R.; Thompson, T.A.; Basu, H.S.; Wilding, G. JunD mediates androgen-induced oxidative stress in androgen dependent LNCaP human prostate cancer cells. Prostate 2008, 68, 924-934.
15. Park, S.Y.; Yu, X.; Ip, C.; Mohler, J.L.; Bogner, P.N.; Park, Y.M. Peroxiredoxin 1 interacts with androgen receptor and enhances its transactivation. Cancer Res. 2007, 67, 9294-9303.
16. Pilat, M.J.; Kamradt, J.M.; Pienta, K.J. Hormone resistance in prostate cancer. Cancer Metastasis Rev. 1998, 17, 373-381.
17. Mostaghel, E.A.; Montgomery, B.; Nelson, P.S. Castration-resistant prostate cancer: targeting androgen metabolic pathways in recurrent disease. Urol. Oncol. 2009, 27, 251-257.
18. Mizokami, A.; Koh, E.; Izumi, K.; Narimoto, K.; Takeda, M.; Honma, S.; Dai, J.; Keller, E.T.; Namiki, M. Prostate cancer stromal cells and LNCaP cells coordinately activate the androgen receptor through synthesis of testosterone and dihydrotestosterone from dehydroepiandrosterone. Endocr. Relat. Cancer 2009, 16, 1139-1155.
19. Yossepowitch, O.; Pinchuk, I.; Gur, U.; Neumann, A.; Lichtenberg, D.; Baniel, J. Advanced but not localized prostate cancer is associated with increased oxidative stress. J. Urol. 2007, 178, 1238-1243; discussion 1243-1234.
20. Tam, N.N.; Gao, Y.; Leung, Y.K.; Ho, S.M. Androgenic regulation of oxidative stress in the rat prostate: involvement of NAD(P)H oxidases and antioxidant defense machinery during prostatic involution and regrowth. Am. J. Pathol. 2003, 163, 2513-2522.
21. Rhee, S.G. Cell signaling. H2O2, a necessary evil for cell signaling. Science 2006, 312, 1882-1883.
22. Marignol, L.; Coffey, M.; Lawler, M.; Hollywood, D. Hypoxia in prostate cancer: a powerful shield against tumour destruction? Cancer Treat. Rev. 2008, 34, 313-327.
23. Brar, S.S.; Corbin, Z.; Kennedy, T.P.; Hemendinger, R.; Thornton, L.; Bommarius, B.; Arnold, R.S.; Whorton, A.R.; Sturrock, A.B.; Huecksteadt, T.P. et al. NOX5 NAD(P)H oxidase regulates growth and apoptosis in DU 145 prostate cancer cells. Am. J. Physiol. Cell Physiol. 2003, 285, C353-369.
24. Kumar, B.; Koul, S.; Khandrika, L.; Meacham, R.B.; Koul, H.K. Oxidative stress is inherent in prostate cancer cells and is required for aggressive phenotype. Cancer Res. 2008, 68, 1777-1785.
25. Hayek, O.R.; Shabsigh, A.; Kaplan, S.A.; Kiss, A.J.; Chen, M.W.; Burchardt, T.; Burchardt, M.; Olsson, C.A.; Buttyan, R. Castration induces acute vasoconstriction of blood vessels in the rat prostate concomitant with a reduction of prostatic nitric oxide synthase activity. J. Urol. 1999, 162, 1527-1531.
26. Park, S.Y.; Kim, Y.J.; Gao, A.C.; Mohler, J.L.; Onate, S.A.; Hidalgo, A.A.; Ip, C.; Park, E.M.; Yoon, S.Y.; Park, Y.M. Hypoxia increases androgen receptor activity in prostate cancer cells. Cancer Res. 2000, 66, 5121-5129.
27. Movsas, B.; Chapman, J.D.; Hanlon, A.L.; Horwitz, E.M.; Greenberg, R.E.; Stobbe, C.; Hanks, G.E.; Pollack, A. Hypoxic prostate/muscle pO2 ratio predicts for biochemical failure in patients with prostate cancer: preliminary findings. Urology 2002, 60, 634-639.
28. Shabsigh, A.; Chang, D.T.; Heitjan, D.F.; Kiss, A.; Olsson, C.A.; Puchner, P.J.; Buttyan, R. Rapid reduction in blood flow to the rat ventral prostate gland after castration: preliminary evidence that androgens influence prostate size by regulating blood flow to the prostate gland and prostatic endothelial cell survival. Prostate 1998, 36, 201-206.
29. Vaquero, E.C.; Edderkaoui, M.; Pandol, S.J.; Gukovsky, I.; Gukovskaya, A.S. Reactive oxygen species produced by NAD(P)H oxidase inhibit apoptosis in pancreatic cancer cells. J. Biol. Chem. 2004, 279, 34643-34654.
30. Sauer, H.; Wartenberg, M.; Hescheler, J. Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell Physiol. Biochem. 2001, 11, 173-186.
31. Mansfield, K.D.; Guzy, R.D.; Pan, Y.; Young, R.M.; Cash, T.P.; Schumacker, P.T.; Simon, M.C. Mitochondrial dysfunction resulting from loss of cytochrome c impairs cellular oxygen sensing and hypoxic HIF-alpha activation. Cell Metab. 2005, 1, 393-399.
32. Bourdeau-Heller, J.; Oberley, T.D. Prostate carcinoma cells selected by long-term exposure to reduced oxygen tension show remarkable biochemical plasticity via modulation of superoxide, HIF-1alpha levels, and energy metabolism. J. Cell Physiol. 2007, 212, 744-752.
33. Chhipa, R.R.; Lee, K.S.; Onate, S.; Wu, Y.; Ip, C. Prx1 enhances androgen receptor function in prostate cancer cells by increasing receptor affinity to dihydrotestosterone. Mol. Cancer Res. 2009, 7, 1543-1552.
34. Rathore, R.; Zheng, Y.M.; Niu, C.F.; Liu, Q.H.; Korde, A.; Ho, Y.S.; Wang, Y.X. Hypoxia activates NADPH oxidase to increase [ROS]i and [Ca2+]i through the mitochondrial ROSPKCepsilon signaling axis in pulmonary artery smooth muscle cells. Free Radic Biol. Med. 2008, 45, 1223-1231.
35. Clark, R.A. Activation of the neutrophil respiratory burst oxidase. J. Infect. Dis. 1999, 179 (Suppl. 2), S309-317.
36. Rhee, S.G. Redox signaling: hydrogen peroxide as intracellular messenger. Exp. Mol. Med 1999, 31, 53-59.
37. Thalmann, G.N.; Anezinis, P.E.; Chang, S.M.; Zhau, H.E.; Kim, E.E.; Hopwood, V.L.; Pathak, S.; von Eschenbach, A.C.; Chung, L.W. Androgen-independent cancer progression and bone metastasis in the LNCaP model of human prostate cancer. Cancer Res. 1994, 54, 2577-2581.
38. Locke, J.A.; Guns, E.S.; Lubik, A.A.; Adomat, H.H.; Hendy, S.C.; Wood, C.A.; Ettinger, S.L.; Gleave, M.E.; Nelson, C.C. Androgen levels increase by intratumoral de novo steroidogenesis during progression of castration-resistant prostate cancer. Cancer Res. 2008, 68, 6407-6415.
39. Xie, B.X.; Zhang, H.; Yu, L.; Wang, J.; Pang, B.; Wu, R.Q.; Qian, X.L.; Li, S.H.; Shi, Q.G.; Wang, L.L.; et al. The radiation response of androgen-refractory prostate cancer cell line C4-2 derived from androgen-sensitive cell line LNCaP. Asian J. Androl. 2010, 12, 405-414.
40. McCord, J.M. Superoxide radical: controversies, contradictions, and paradoxes. Proc. Soc. Exp. Biol. Med. 1995, 209, 112-117.
41. Martin, K.R.; Barrett, J.C. Reactive oxygen species as double-edged swords in cellular processes: low-dose cell signaling versus high-dose toxicity. Hum. Exp. Toxicol. 2002, 21, 71-75.
42. Lau, A.; Villeneuve, N.F.; Sun, Z.; Wong, P.K.; Zhang, D.D. Dual roles of Nrf2 in cancer. Pharmacol Res. 2008, 58, 262-270.
43. Yanagawa, T.; Ishikawa, T.; Ishii, T.; Tabuchi, K.; Iwasa, S.; Bannai, S.; Omura, K.; Suzuki, H.; Yoshida, H. Peroxiredoxin I expression in human thyroid tumors. Cancer Lett. 1999, 145, 127-132.
44. Yanagawa, T.; Iwasa, S.; Ishii, T.; Tabuchi, K.; Yusa, H.; Onizawa, K.; Omura, K.; Harada, H.; Suzuki, H.; Yoshida, H. Peroxiredoxin I expression in oral cancer: a potential new tumor marker. Cancer Lett. 2000, 156, 27-35.
45. Kim, S.K.; Yang, J.W.; Kim, M.R.; Roh, S.H.; Kim, H.G.; Lee, K.Y.; Jeong, H.G.; Kang, K.W. Increased expression of Nrf2/ARE-dependent anti-oxidant proteins in tamoxifen-resistant breast cancer cells. Free Radic Biol. Med. 2008, 45, 537-546.
46. Venugopal, R.; Jaiswal, A.K. Nrf2 and Nrf1 in association with Jun proteins regulate antioxidant response element-mediated expression and coordinated induction of genes encoding detoxifying enzymes. Oncogene 1998, 17, 3145-3156.
47. Osburn, W.O.; Kensler, T.W. Nrf2 signaling: an adaptive response pathway for protection against environmental toxic insults. Mutat. Res. 2008, 659, 31-39.
48. Wang, W.; Kwok, A.M.; Chan, J.Y. The p65 isoform of Nrf1 is a dominant negative inhibitor of ARE-mediated transcription. J. Biol. Chem. 2007, 282, 24670-24678.
49. Kim, Y.J.; Ahn, J.Y.; Liang, P.; Ip, C.; Zhang, Y.; Park, Y.M. Human prx1 gene is a target of Nrf2 and is up-regulated by hypoxia/reoxygenation: implication to tumor biology. Cancer Res. 2007, 67, 546-554.
50. Maher, J.M.; Dieter, M.Z.; Aleksunes, L.M.; Slitt, A.L.; Guo, G.; Tanaka, Y.; Scheffer, G.L.; Chan, J.Y.; Manautou, J.E.; Chen, Y. et al. Oxidative and electrophilic stress induces multidrug resistance-associated protein transporters via the nuclear factor-E2-related factor-2 transcriptional pathway. Hepatology 2007, 46, 1597-1610.
51. Zhu, M.; Fahl, W.E. Functional characterization of transcription regulators that interact with the electrophile response element. Biochem. Biophys. Res. Commun. 2001, 289, 212-219.
52. Toki, T.; Itoh, J.; Kitazawa, J.; Arai, K.; Hatakeyama, K.; Akasaka, J.; Igarashi, K.; Nomura, N.; Yokoyama, M.; Yamamoto, M. et al. Human small Maf proteins form heterodimers with CNC family transcription factors and recognize the NF-E2 motif. Oncogene 1997, 14, 1901-1910.
53. Johnsen, O.; Murphy, P.; Prydz, H.; Kolsto, A.B. Interaction of the CNC-bZIP factor TCF11/LCR-F1/Nrf1 with MafG: binding-site selection and regulation of transcription. Nucleic Acids Res. 1998. 26, 512-520.
54. Chan, J.Y.; Kwong, M. Impaired expression of glutathione synthetic enzyme genes in mice with targeted deletion of the Nrf2 basic-leucine zipper protein. Biochim. Biophys. Acta 2000, 1517, 19-26.
55. Xu, Z.; Chen, L.; Leung, L.; Yen, T.S.; Lee, C.; Chan, J.Y. Liver-specific inactivation of the Nrf1 gene in adult mouse leads to nonalcoholic steatohepatitis and hepatic neoplasia. Proc. Natl. Acad. Sci. USA 2005, 102, 4120-4125.
56. Chen, L.; Kwong, M.; Lu, R.; Ginzinger, D.; Lee, C.; Leung, L.; Chan, J.Y. Nrf1 is critical for redox balance and survival of liver cells during development. Mol. Cell Biol. 2003, 23, 4673-4686.
57. Biswas, M.; Chan, J.Y. Role of Nrf1 in antioxidant response element-mediated gene expression and beyond. Toxicol. Appl. Pharmacol. 2010, 244, 16-20.
58. Ohtsuji, M.; Katsuoka, F.; Kobayashi, A.; Aburatani, H.; Hayes, J.D.; Yamamoto, M. Nrf1 and Nrf2 play distinct roles in activation of antioxidant response element-dependent genes. J. Biol. Chem. 2008, 283, 33554-33562.
59. Ushio-Fukai, M.; Nakamura, Y. Reactive oxygen species and angiogenesis: NADPH oxidase as target for cancer therapy. Cancer Lett. 2008, 266, 37-52.
60. Frohlich, D.A.; McCabe, M.T.; Arnold, R.S.; Day, M.L. The role of Nrf2 in increased reactive oxygen species and DNA damage in prostate tumorigenesis. Oncogene 2008, 27, 4353-4362.
61. Osburn, W.O.; Karim, B.; Dolan, P.M.; Liu, G.; Yamamoto, M.; Huso, D.L.; Kensler, T.W. Increased colonic inflammatory injury and formation of aberrant crypt foci in Nrf2-deficient mice upon dextran sulfate treatment. Int. J. Cancer 2007, 121, 1883-1891.
62. Thimmulappa, R.K.; Lee, H.; Rangasamy, T.; Reddy, S.P.; Yamamoto, M.; Kensler, T.W.; Biswal, S. Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis. J. Clin. Invest. 2006, 116, 984-995.
63. Jin, R.J.; Lho, Y.; Connelly, L.; Wang, Y.; Yu, X.; Saint Jean, L.; Case, T.C.; Ellwood-Yen, K.; Sawyers, C.L.; Bhowmick, N.A. et al. The nuclear factor-kappaB pathway controls the progression of prostate cancer to androgen-independent growth. Cancer Res. 2008, 68, 6762-6769.
64. Tong, K.I.; Katoh, Y.; Kusunoki, H.; Itoh, K.; Tanaka, T.; Yamamoto, M. Keap1 recruits Neh2 through binding to ETGE and DLG motifs: characterization of the two-site molecular recognition model. Mol. Cell Biol. 2006, 26, 2887-2900.
65. Itoh, K.; Tong, K.I.; Yamamoto, M. Molecular mechanism activating Nrf2-Keap1 pathway in regulation of adaptive response to electrophiles. Free Radic. Biol. Med. 2004, 36, 1208-1213.
66. Eggler, A.L.; Liu, G.; Pezzuto, J.M.; van Breemen, R.B.; Mesecar, A.D. Modifying specific cysteines of the electrophile-sensing human Keap1 protein is insufficient to disrupt binding to the Nrf2 domain Neh2. Proc. Natl. Acad. Sci. USA 2005, 102, 10070-10075.
67. Zhang, P.; Singh, A.; Yegnasubramanian, S.; Esopi, D.; Kombairaju, P.; Bodas, M.; Wu, H.; Bova, S.G.; Biswal, S. Loss of Kelch-like ECH-associated protein 1 function in prostate cancer cells causes chemoresistance and radioresistance and promotes tumor growth. Mol. Cancer Ther. 2010, 9, 336-346.
68. Zhang, Y.; Lucocq, J.M.; Yamamoto, M.; Hayes, J.D. The NHB1 (N-terminal homology box 1) sequence in transcription factor Nrf1 is required to anchor it to the endoplasmic reticulum and also to enable its asparagine-glycosylation. Biochem. J. 2007, 408, 161-172.
69. Zhang, Y.; Crouch, D.H.; Yamamoto, M.; Hayes, J.D. Negative regulation of the Nrf1 transcription factor by its N-terminal domain is independent of Keap1: Nrf1, but not Nrf2, is targeted to the endoplasmic reticulum. Biochem. J. 2006, 399, 373-385.
70. Wang, W.; Chan, J.Y. Nrf1 is targeted to the endoplasmic reticulum membrane by an N-terminal transmembrane domain. Inhibition of nuclear translocation and transacting function. J. Biol. Chem. 2006, 281, 19676-19687.
71. Radhakrishnan, S.K.; Lee, C.S.; Young, P.; Beskow, A.; Chan, J.Y.; Deshaies, R.J. Transcription factor Nrf1 mediates the proteasome recovery pathway after proteasome inhibition in mammalian cells. Mol. Cell 2010, 38, 17-28.
72. Magnani, M.; Crinelli, R.; Bianchi, M.; Antonelli, A. The ubiquitin-dependent proteolytic system and other potential targets for the modulation of nuclear factor-kB (NF-κB). Curr. Drug Targets 2000, 1, 387-399.
73. Tanaka, K.; Kawakami, T.; Tateishi, K.; Yashiroda, H.; Chiba, T. Control of IkappaBalpha proteolysis by the ubiquitin-proteasome pathway. Biochimie 2001, 83, 351-356.
74. McMahon, M.; Thomas, N.; Itoh, K.; Yamamoto, M.; Hayes, J.D. Redox-regulated turnover of Nrf2 is determined by at least two separate protein domains, the redox-sensitive Neh2 degron and the redox-insensitive Neh6 degron. J. Biol. Chem. 2004, 279, 31556-31567.
75. Navon, A.; Ciechanover, A. The 26 S proteasome: from basic mechanisms to drug targeting. J. Biol. Chem. 2009, 284, 33713-33718.
76. Yamasaki, M.; Nomura, T.; Sato, F.; Mimata, H. Metallothionein is up-regulated under hypoxia and promotes the survival of human prostate cancer cells. Oncol. Rep. 2007, 18, 1145-1153.
77. Smith, D.J.; Jaggi, M.; Zhang, W.; Galich, A.; Du, C.; Sterrett, S.P.; Smith, L.M.; Balaji, K.C. Metallothioneins and resistance to cisplatin and radiation in prostate cancer. Urology 2006, 67, 1341-1347.
78. Pedersen, M.O.; Larsen, A.; Stoltenberg, M.; Penkowa, M. The role of metallothionein in oncogenesis and cancer prognosis. Prog. Histochem. Cytochem. 2009, 44, 29-64.
79. Surh, Y.J.; Kundu, J.K.; Na, H.K. Nrf2 as a master redox switch in turning on the cellular signaling involved in the induction of cytoprotective genes by some chemopreventive phytochemicals. Planta Med. 2008, 74, 1526-1539.
80. Katsuoka, F.; Motohashi, H.; Engel, J.D.; Yamamoto, M. Nrf2 transcriptionally activates the mafG gene through an antioxidant response element. J. Biol. Chem. 2005, 280, 4483-4490.
81. Arner, E.S.; Holmgren, A. The thioredoxin system in cancer. Semin. Cancer Biol. 2006, 16, 420-426.
82. Pennington, J.D.; Jacobs, K.M.; Sun, L.; Bar-Sela, G.; Mishra, M.; Gius, D. Thioredoxin and thioredoxin reductase as redox-sensitive molecular targets for cancer therapy. Curr. Pharm. Des. 2007, 13, 3368-3377.
83. Berggren, M.I.; Husbeck, B.; Samulitis, B.; Baker, A.F.; Gallegos, A.; Powis, G. Thioredoxin peroxidase-1 (peroxiredoxin-1) is increased in thioredoxin-1 transfected cells and results in enhanced protection against apoptosis caused by hydrogen peroxide but not by other agents including dexamethasone, etoposide, and doxorubicin. Arch. Biochem. Biophys. 2001, 392, 103-109.
84. Powis, G.; Kirkpatrick, D.L. Thioredoxin signaling as a target for cancer therapy. Curr. Opin. Pharmacol. 2007, 7, 392-397.
85. Hansen, J.M.; Moriarty-Craige, S.; Jones, D.P. Nuclear and cytoplasmic peroxiredoxin-1 differentially regulate NF-kappaB activities. Free Radic. Biol. Med. 2007, 43, 282-288.
86. Rhee, S.G.; Chae, H.Z.; Kim, K. Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic. Biol. Med. 2005, 38, 1543-1552.
87. Fourquet, S.; Huang, M.E.; D'Autreaux, B.; Toledano, M.B. The dual functions of thiol-based peroxidases in H2O2 scavenging and signaling. Antioxid. Redox. Signal. 2008, 10, 1565-1576.
88. Lim, J.C.; Choi, H.I.; Park, Y.S.; Nam, H.W.; Woo, H.A.; Kwon, K.S.; Kim, Y.S.; Rhee, S.G.; Kim, K.; Chae, H.Z. Irreversible oxidation of the active-site cysteine of peroxiredoxin to cysteine sulfonic acid for enhanced molecular chaperone activity. J. Biol. Chem. 2008, 283, 28873-28880.
89. Hirota, K.; Murata, M.; Sachi, Y.; Nakamura, H.; Takeuchi, J.; Mori, K.; Yodoi, J. Distinct roles of thioredoxin in the cytoplasm and in the nucleus. A two-step mechanism of redox regulation of transcription factor NF-kappaB. J. Biol. Chem. 1999, 274, 27891-27897.
90. Rao, A.K.; Ziegler, Y.S.; McLeod, I.X.; Yates, J.R.; Nardulli, A.M. Thioredoxin and thioredoxin reductase influence estrogen receptor alpha-mediated gene expression in human breast cancer cells. J. Mol. Endocrinol. 2009, 43, 251-261.
91. Quiros, I.; Sainz, R.M.; Hevia, D.; Garcia-Suarez, O.; Astudillo, A.; Rivas, M. Mayo, J.C. Upregulation of manganese superoxide dismutase (SOD2) is a common pathway for neuroendocrine differentiation in prostate cancer cells. Int. J. Cancer 2009, 125, 1497-1504.
92. Yang, H.; Magilnick, N.; Lee, C.; Kalmaz, D.; Ou, X.; Chan, J.Y.; Lu, S.C. Nrf1 and Nrf2 regulate rat glutamate-cysteine ligase catalytic subunit transcription indirectly via NF-kappaB and AP-1. Mol. Cell Biol. 2005, 25, 5933-5946.
93. Grzywacz, M.J.; Yang, J.M.; Hait, W.N. Effect of the multidrug resistance protein on the transport of the antiandrogen flutamide. Cancer Res. 2003, 63, 2492-2498.
94. Laberge, R.M.; Karwatsky, J.; Lincoln, M.C.; Leimanis, M.L.; Georges, E. Modulation of GSH levels in ABCC1 expressing tumor cells triggers apoptosis through oxidative stress. Biochem. Pharmacol. 2007, 73, 1727-1737.
95. Narayanan, K.; Ramachandran, A.; Peterson, M.C.; Hao, J.; Kolsto, A.B.; Friedman, A.D.; George, A. The CCAAT enhancer-binding protein (C/EBP)beta and Nrf1 interact to regulate dentin sialophosphoprotein (DSPP) gene expression during odontoblast differentiation. J. Biol. Chem. 2004, 279, 45423-45432.
96. Xing, W.; Singgih, A.; Kapoor, A.; Alarcon, C.M.; Baylink, D.J.; Mohan, S. Nuclear factor-E2- related factor-1 mediates ascorbic acid induction of osterix expression via interaction with antioxidant-responsive element in bone cells. J. Biol. Chem. 2007, 282, 22052-22061.
97. Wang, R.S.; Yeh, S.; Tzeng, C.R.; Chang, C. Androgen receptor roles in spermatogenesis and fertility: lessons from testicular cell-specific androgen receptor knockout mice. Endocr. Rev. 2009, 30, 119-132.
98. Vis, A.N.; Schroder, F.H. Key targets of hormonal treatment of prostate cancer. Part 1: the androgen receptor and steroidogenic pathways. BJU Int. 2009, 104, 438-448.
99. Bubendorf, L.; Kononen, J.; Koivisto, P.; Schraml, P.; Moch, H.; Gasser, T.C.; Willi, N.; Mihatsch, M.J.; Sauter, G.; Kallioniemi, O.P. Survey of gene amplifications during prostate cancer progression by high-throughout fluorescence in situ hybridization on tissue microarrays. Cancer Res. 1999, 59, 803-806.
100. Xia, C.; Meng, Q.; Liu, L.Z.; Rojanasakul, Y.; Wang, X.R.; Jiang, B.H. Reactive oxygen species regulate angiogenesis and tumor growth through vascular endothelial growth factor. Cancer Res. 2007, 67, 10823-10830.
101. Chen, C.; Kong, A.N. Dietary chemopreventive compounds and ARE/EpRE signaling. Free Radic. Biol. Med. 2004, 36, 1505-1516.
102. Kang, D.; Lee, K.M.; Park, S.K.; Berndt, S.I.; Peters, U.; Reding, D.; Chatterjee, N.; Welch, R.; Chanock, S.; Huang, W.Y. et al. Functional variant of manganese superoxide dismutase (SOD2 V16A) polymorphism is associated with prostate cancer risk in the prostate, lung, colorectal, and ovarian cancer study. Cancer Epidemiol. Biomarkers Prev. 2007, 16, 1581-1586.
103. Shono, T.; Yokoyama, N.; Uesaka, T.; Kuroda, J.; Takeya, R.; Yamasaki, T.; Amano, T.; Mizoguchi, M.; Suzuki, S.O.; Niiro, H. et al. Enhanced expression of NADPH oxidase Nox4 in human gliomas and its roles in cell proliferation and survival. Int. J. Cancer 2008, 123, 787-792.
104. Yates, M.S.; Tran, Q.T.; Dolan, P.M.; Osburn, W.O.; Shin, S.; McCulloch, C.C.; Silkworth, J.B.; Taguchi, K.; Yamamoto, M.; Williams, C.R. et al. Genetic versus chemoprotective activation of Nrf2 signaling: overlapping yet distinct gene expression profiles between Keap1 knockout and triterpenoid-treated mice. Carcinogenesis 2009, 30, 1024-1031.
105. Raschke, M.; Rowland, I.R.; Magee, P.J.; Pool-Zobel, B.L. Genistein protects prostate cells against hydrogen peroxide-induced DNA damage and induces expression of genes involved in the defence against oxidative stress. Carcinogenesis 2006, 27, 2322-2330.
106. Hernandez-Montes, E.; Pollard, S.E.; Vauzour, D.; Jofre-Montseny, L.; Rota, C.; Rimbach, G.; Weinberg, P.D.; Spencer, J.P. Activation of glutathione peroxidase via Nrf1 mediates genistein's protection against oxidative endothelial cell injury. Biochem. Biophys Res. Commun. 2006, 346, 851-859.
107. Peternac, D.; Klima, I.; Cecchini, M.G.; Schwaninger, R.; Studer, U.E.; Thalmann, G.N. Agents used for chemoprevention of prostate cancer may influence PSA secretion independently of cell growth in the LNCaP model of human prostate cancer progression. Prostate 2008, 68, 1307-1318.
108. Inoue, K.; Kulsum, U.; Chowdhury, S.A.; Fujisawa, S.; Ishihara, M.; Yokoe, I.; Sakagami, H. Tumor-specific cytotoxicity and apoptosis-inducing activity of berberines. Anticancer Res. 2005, 25, 4053-4059.
109. Koka, P.S.; Mondal, D.; Schultz, M.; Abdel-Mageed, A.B.; Agrawal, K.C. Studies on molecular mechanisms of growth inhibitory effects of thymoquinone against prostate cancer cells: role of reactive oxygen species. Exp. Biol. Med. (Maywood) 2010, 235, 751-760.
110. Nioi, P.; McMahon, M.; Itoh, K.; Yamamoto, M.; Hayes, J.D. Identification of a novel Nrf2- regulated antioxidant response element (ARE) in the mouse NAD(P)H:quinone oxidoreductase 1 gene: reassessment of the ARE consensus sequence. Biochem. J. 2003, 374, 337-348.