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Cancer Chemotherapy and Pharmacology

, Volume 84, Issue 5, pp 925–935 | Cite as

The thioredoxin system and cancer therapy: a review

  • Fariba Mohammadi
  • Arash Soltani
  • Atefeh Ghahremanloo
  • Hossein Javid
  • Seyed Isaac HashemyEmail author
Review Article

Abstract

Thioredoxin (Trx), thioredoxin reductase (TrxR), and NADPH are key members of the Trx system that is involved in redox regulation and antioxidant defense. In recent years, several researchers have provided information about the roles of the Trx system in cancer development and progression. These reports indicated that many tumor cells express high levels of Trx and TrxR, which can be responsible for drug resistance in tumorigenesis. Inhibition of the Trx system may thus contribute to cancer therapy and improving chemotherapeutic agents. There are now a number of effective natural and synthetic inhibitors with chemotherapy applications possessing antitumor activity ranging from oxidative stress induction to apoptosis. In this article, we first described the features and functions of the Trx system and then reviewed briefly its correlations with cancer. Finally, we summarized the present knowledge about the Trx/TrxR inhibitors as anticancer drugs.

Keywords

Thioredoxin Thioredoxin reductase Cancer Cancer therapy Oxidative stress 

Notes

Compliance with ethical standards

Conflict of interests

The authors have no competing interests to declare.

References

  1. 1.
    Nordberg J, Arner ES (2001) Reactive oxygen species, antioxidants, and the mammalian thioredoxin system1. Free Radic Biol Med 31(11):1287–1312PubMedCrossRefGoogle Scholar
  2. 2.
    Thannickal VJ, Fanburg BL (2000) Reactive oxygen species in cell signaling. Am J Phys Lung Cell Mol Phys 279(6):L1005–L1028Google Scholar
  3. 3.
    Cortassa S, O’Rourke B, Aon MA (2014) Redox-optimized ROS balance and the relationship between mitochondrial respiration and ROS. Biochim Biophys Acta 183(2):287–295CrossRefGoogle Scholar
  4. 4.
    Gasdaska PY, Oblong JE, Cotgreave IA, Powis G (1994) The predicted amino acid sequence of human thioredoxin is identical to that of the autocrine growth factor human adult T-cell derived factor (ADF): thioredoxin mRNA is elevated in some human tumors. Biochim Biophys Acta 1218(3):292–296PubMedCrossRefGoogle Scholar
  5. 5.
    Karlenius TC, Tonissen KF (2010) Thioredoxin and cancer: a role for thioredoxin in all states of tumor oxygenation. Cancers 2(2):209–232PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Kawahara N, Tanaka T, Yokomizo A, Nanri H, Ono M, Wada M et al (1996) Enhanced coexpression of thioredoxin and high mobility group protein 1 genes in human hepatocellular carcinoma and the possible association with decreased sensitivity to cisplatin. Cancer Res 56(23):5330–5333PubMedGoogle Scholar
  7. 7.
    Lim JY, Yoon SO, Hong SW, Kim JW, Choi SH, Cho JY (2012) Thioredoxin and thioredoxin-interacting protein as prognostic markers for gastric cancer recurrence. World J Gastroenterol 18(39):5581PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Nakamura H, Bai J, Nishinaka Y, Ueda S, Sasada T, Ohshio G et al (2000) Expression of thioredoxin and glutaredoxin, redox-regulating proteins, in pancreatic cancer. Cancer Detect Prev 24(1):53–60PubMedGoogle Scholar
  9. 9.
    Raffel J, Bhattacharyya AK, Gallegos A, Cui H, Einspahr JG, Alberts DS et al (2003) Increased expression of thioredoxin-1 in human colorectal cancer is associated with decreased patient survival. Transl Res 142(1):46–51Google Scholar
  10. 10.
    Arner ES, Holmgren A (eds) (2006) The thioredoxin system in cancer. Seminars in cancer biology. Elsevier, AmsterdamGoogle Scholar
  11. 11.
    Farina AR, Tacconelli A, Cappabianca L, Masciulli MP, Holmgren A, Beckett GJ et al (2001) Thioredoxin alters the matrix metalloproteinase/tissue inhibitors of metalloproteinase balance and stimulates human SK-N-SH neuroblastoma cell invasion. FEBS J 268(2):405–413Google Scholar
  12. 12.
    Oh JH, Chung AS, Steinbrenner H, Sies H, Brenneisen P (2004) Thioredoxin secreted upon ultraviolet A irradiation modulates activities of matrix metalloproteinase-2 and tissue inhibitor of metalloproteinase-2 in human dermal fibroblasts. Arch Biochem Biophys 423(1):218–226PubMedCrossRefGoogle Scholar
  13. 13.
    Welsh SJ, Bellamy WT, Briehl MM, Powis G (2002) The redox protein thioredoxin-1 (Trx-1) increases hypoxia-inducible factor 1alpha protein expression: Trx-1 overexpression results in increased vascular endothelial growth factor production and enhanced tumor angiogenesis. Cancer Res 62(17):5089–5095PubMedGoogle Scholar
  14. 14.
    Tonissen KF, Di Trapani G (2009) Thioredoxin system inhibitors as mediators of apoptosis for cancer therapy. Mol Nutr Food Res 53(1):87–103PubMedCrossRefGoogle Scholar
  15. 15.
    Urig S, Becker K (2006) On the potential of thioredoxin reductase inhibitors for cancer therapy. Semin Cancer Biol 16(6):452–465PubMedCrossRefGoogle Scholar
  16. 16.
    Arner ES (2009) Focus on mammalian thioredoxin reductases—important selenoproteins with versatile functions. Biochem Biophys Acta 1790(6):495–526PubMedCrossRefGoogle Scholar
  17. 17.
    Lee S, Kim SM, Lee RT (2013) Thioredoxin and thioredoxin target proteins: from molecular mechanisms to functional significance. Antioxid Redox Signal 18(10):1165–1207PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Lillig CH, Holmgren A (2007) Thioredoxin and related molecules—from biology to health and disease. Antioxid Redox Signal 9(1):25–47PubMedCrossRefGoogle Scholar
  19. 19.
    Holmgren A (1985) Thioredoxin. Annu Rev Biochem 54(1):237–271PubMedCrossRefGoogle Scholar
  20. 20.
    Arnér ES, Holmgren A (2000) Physiological functions of thioredoxin and thioredoxin reductase. FEBS J 267(20):6102–6109Google Scholar
  21. 21.
    Gromer S, Urig S, Becker K (2004) The thioredoxin system—from science to clinic. Med Res Rev 24(1):40–89PubMedCrossRefGoogle Scholar
  22. 22.
    Mustacich D, Powis G (2000) Thioredoxin reductase. Biochem J 346(Pt 1):1–8PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Zhang J, Li X, Han X, Liu R, Fang J (2017) Targeting the thioredoxin system for cancer therapy. Trends Pharmacol Sci 38(9):794–808PubMedCrossRefGoogle Scholar
  24. 24.
    Miranda-Vizuete A, Ljung J, Damdimopoulos AE, Gustafsson JA, Oko R, Pelto-Huikko M et al (2001) Characterization of Sptrx, a novel member of the thioredoxin family specifically expressed in human spermatozoa. J Biol Chem 276(34):31567–31574PubMedCrossRefGoogle Scholar
  25. 25.
    Go Y-M, Jones DP (2013) Thiol/disulfide redox states in signaling and sensing. Crit Rev Biochem Mol Biol 48(2):173–181PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Rigobello MP, Bindoli A (2010) Mitochondrial thioredoxin reductase: purification, inhibitor studies, and role in cell signaling. Methods in enzymology, vol 474. Elsevier, Amsterdam, pp 109–122Google Scholar
  27. 27.
    Sun Q-A, Su D, Novoselov SV, Carlson BA, Hatfield DL, Gladyshev VN (2005) Reaction mechanism and regulation of mammalian thioredoxin/glutathione reductase. Biochemistry 44(44):14528–14537PubMedCrossRefGoogle Scholar
  28. 28.
    Matsui M, Oshima M, Oshima H, Takaku K, Maruyama T, Yodoi J et al (1996) Early embryonic lethality caused by targeted disruption of the mouse thioredoxin gene. Dev Biol 178(1):179–185PubMedCrossRefGoogle Scholar
  29. 29.
    Kim HY, Gladyshev VN (2005) Different catalytic mechanisms in mammalian selenocysteine- and cysteine-containing methionine-R-sulfoxide reductases. PLoS Biol 3(12):e375PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Moskovitz J, Bar-Noy S, Williams WM, Requena J, Berlett BS, Stadtman ER (2001) Methionine sulfoxide reductase (MsrA) is a regulator of antioxidant defense and lifespan in mammals. Proc Natl Acad Sci 98(23):12920–12925PubMedCrossRefGoogle Scholar
  31. 31.
    Rhee SG, Chae HZ, Kim K (2005) Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radical Biol Med 38(12):1543–1552CrossRefGoogle Scholar
  32. 32.
    Sengupta R, Holmgren A (1820) The role of thioredoxin in the regulation of cellular processes by S-nitrosylation. Biochim Biophysica Acta 6:689–700Google Scholar
  33. 33.
    Sengupta R, Holmgren A (2013) Thioredoxin and thioredoxin reductase in relation to reversible S-nitrosylation. Antioxid Redox Signal 18(3):259–269PubMedCrossRefGoogle Scholar
  34. 34.
    Mitsui A, Hirakawa T, Yodoi J (1992) Reactive oxygen-reducing and protein-refolding activities of adult T cell leukemia-derived factor/human thioredoxin. Biochem Biophys Res Commun 186(3):1220–1226PubMedCrossRefGoogle Scholar
  35. 35.
    Powis G, Montfort WR (2001) Properties and biological activities of thioredoxins. Annu Rev Biophys Biomol Struct 30(1):421–455PubMedCrossRefGoogle Scholar
  36. 36.
    Kang D-H (2002) Oxidative stress, DNA damage, and breast cancer. AACN Adv Crit Care 13(4):540–549Google Scholar
  37. 37.
    Fridovich I (1999) Fundamental aspects of reactive oxygen species, or what’s the matter with oxygen? Ann NY Acad Sci 893(1):13–18PubMedCrossRefGoogle Scholar
  38. 38.
    Valko M, Rhodes C, Moncol J, Izakovic M, Mazur M (2006) Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 160(1):1–40PubMedCrossRefGoogle Scholar
  39. 39.
    Peivandi Yazdi A, Razavi M, Sheikh S, Boroumand N, Salehi M, Hashemy SI (2019) Clinical trial assessment of intermittent and continuous infusion dose of N-acetylcysteine on redox status of the body in patients with sepsis admitted to the ICU. J Intensiv Care Med 885066618823152Google Scholar
  40. 40.
    Peivandi Yazdi A, Bameshki A, Salehi M, Kazemzadeh G, Sharifian Razavi M, Rahmani S et al (2018) The effect of spinal and general anesthesia on serum lipid peroxides and total antioxidant capacity in diabetic patients with lower limb amputation surgery. Arch Bone Jt Surg 6(4):312–317PubMedPubMedCentralGoogle Scholar
  41. 41.
    Ebrahimi S, Soltani A, Hashemy SI (2018) Oxidative stress in cervical cancer pathogenesis and resistance to therapy. J Cell BiochemGoogle Scholar
  42. 42.
    Beiraghi-Toosi A, Askarian R, Sadrabadi Haghighi F, Safarian M, Kalantari F, Hashemy SI (2018) Burn-induced oxidative stress and serum glutathione depletion; a cross sectional study 2018. 6(1)Google Scholar
  43. 43.
    Shoeibi A, Razmi N, Ghabeli Juibary A, Hashemy SI (2017) The evaluation and comparison of oxidative stress in hemorrhagic and ischemic stroke. Casp J Neurol Sci 3(11):206–213CrossRefGoogle Scholar
  44. 44.
    Taheri A, Tanipour MH, Khorasani ZK, Kiafar B, Layegh P, Hashemy SI (2016) Serum protein carbonyl and total antioxidant capacity levels in pemphigus vulgaris and bullous pemphigoid. Iran J Dermatol 18(4):156–162Google Scholar
  45. 45.
    Hashemy SI, Gharaei S, Vasigh S, Kargozar S, Alirezaei B, Keyhani FJ et al (2016) Oxidative stress factors and C-reactive protein in patients with oral lichen planus before and 2 weeks after treatment. J Oral Pathol Med 45(1):35–40PubMedCrossRefGoogle Scholar
  46. 46.
    Amirchaghmaghi M, Hashemy SI, Alirezaei B, Jahed Keyhani F, Kargozar S, Vasigh S et al (2016) Evaluation of plasma isoprostane in patients with oral lichen planus. J Dent 17(1):21–25Google Scholar
  47. 47.
    Ebrahimi S, Hashemy SI (2019) MicroRNA-mediated redox regulation modulates therapy resistance in cancer cells: clinical perspectives. Cell Oncol (Dordr)Google Scholar
  48. 48.
    Saitoh M, Nishitoh H, Fujii M, Takeda K, Tobiume K, Sawada Y et al (1998) Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J 17(9):2596–2606PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Zhang R, Al-Lamki R, Bai L, Streb JW, Miano JM, Bradley J et al (2004) Thioredoxin-2 inhibits mitochondria-located ASK1-mediated apoptosis in a JNK-independent manner. Circ Res 94(11):1483–1491PubMedCrossRefGoogle Scholar
  50. 50.
    Liu Y, Min W (2002) Thioredoxin promotes ASK1 ubiquitination and degradation to inhibit ASK1-mediated apoptosis in a redox activity-independent manner. Circ Res 90(12):1259–1266PubMedCrossRefGoogle Scholar
  51. 51.
    Mitchell DA, Morton SU, Fernhoff NB, Marletta MA (2007) Thioredoxin is required for S-nitrosation of procaspase-3 and the inhibition of apoptosis in Jurkat cells. Proc Natl Acad Sci 104(28):11609–11614PubMedCrossRefGoogle Scholar
  52. 52.
    Meuillet EJ, Mahadevan D, Berggren M, Coon A, Powis G (2004) Thioredoxin-1 binds to the C2 domain of PTEN inhibiting PTEN’s lipid phosphatase activity and membrane binding: a mechanism for the functional loss of PTEN’s tumor suppressor activity. Arch Biochem Biophys 429(2):123–133PubMedCrossRefGoogle Scholar
  53. 53.
    Hirota K, Murata M, Sachi Y, Nakamura H, Takeuchi J, Mori K et al (1999) Distinct roles of thioredoxin in the cytoplasm and in the nucleus a two-step mechanism of redox regulation of transcription factor NF-κB. J Biol Chem 274(39):27891–27897PubMedCrossRefGoogle Scholar
  54. 54.
    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. Proc Natl Acad Sci 94(8):3633–3638PubMedCrossRefGoogle Scholar
  55. 55.
    Powis G, Kirkpatrick DL (2007) Thioredoxin signaling as a target for cancer therapy. Curr Opin Pharmacol 7(4):392–397PubMedCrossRefGoogle Scholar
  56. 56.
    Ueno M, Masutani H, Arai RJ, Yamauchi A, Hirota K, Sakai T et al (1999) Thioredoxin-dependent redox regulation of p53-mediated p21 activation. J Biol Chem 274(50):35809–35815PubMedCrossRefGoogle Scholar
  57. 57.
    Holmgren A, Sengupta R (2010) The use of thiols by ribonucleotide reductase. Free Radic Biol Med 49(11):1617–1628PubMedCrossRefGoogle Scholar
  58. 58.
    Rubartelli A, Bajetto A, Allavena G, Wollman E, Sitia R (1992) Secretion of thioredoxin by normal and neoplastic cells through a leaderless secretory pathway. J Biol Chem 267(34):24161–24164PubMedGoogle Scholar
  59. 59.
    Bertini R, Howard OZ, Dong H-F, Oppenheim JJ, Bizzarri C, Sergi R et al (1999) Thioredoxin, a redox enzyme released in infection and inflammation, is a unique chemoattractant for neutrophils, monocytes, and T cells. J Exp Med 189(11):1783–1789PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Bizzarri C, Holmgren A, Pekkari K, Chang G, Colotta F, Ghezzi P et al (2005) Requirements for the different cysteines in the chemotactic and desensitizing activity of human thioredoxin. Antioxid Redox Signal 7(9–10):1189–1194PubMedCrossRefGoogle Scholar
  61. 61.
    Pekkari K, Goodarzi MT, Scheynius A, Holmgren A, Avila-Carino J (2005) Truncated thioredoxin (Trx80) induces differentiation of human CD14+ monocytes into a novel cell type (TAMs) via activation of the MAP kinases p38, ERK, and JNK. Blood 105(4):1598–1605PubMedCrossRefGoogle Scholar
  62. 62.
    Hwang J, Suh H-W, Jeon YH, Hwang E, Nguyen LT, Yeom J et al (2014) The structural basis for the negative regulation of thioredoxin by thioredoxin-interacting protein. Nat Commun 5:2958PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Chung JW, Jeon JH, Yoon SR, Choi I (2006) Vitamin D3 upregulated protein 1 (VDUP1) is a regulator for redox signaling and stress-mediated diseases. J Dermatol 33(10):662–669PubMedCrossRefGoogle Scholar
  64. 64.
    Nishinaka Y, Masutani H, Nakamura H, Yodoi J (2001) Regulatory roles of thioredoxin in oxidative stress-induced cellular responses. Redox Rep 6(5):289–295PubMedCrossRefGoogle Scholar
  65. 65.
    Nishiyama A, Masutani H, Nakamura H, Nishinaka Y, Yodoi J (2001) Redox regulation by thioredoxin and thioredoxin-binding proteins. IUBMB Life 52(1):29–33PubMedCrossRefGoogle Scholar
  66. 66.
    Rundlöf A-K, Arnér ES (2004) Regulation of the mammalian selenoprotein thioredoxin reductase 1 in relation to cellular phenotype, growth, and signaling events. Antioxid Redox Signal 6(1):41–52PubMedCrossRefGoogle Scholar
  67. 67.
    Lorestani S, Hashemy SI, Mojarad M, Keyvanloo Shahrestanaki M, Bahari A, Asadi M et al (2018) Increased glutathione reductase expression and activity in colorectal cancer tissue samples: an investigational study in Mashhad. Iran Middle East J Cancer 9(2):99–104Google Scholar
  68. 68.
    Pakfetrat A, Dalirsani Z, Hashemy SI, Ghazi A, Mostaan LV, Anvari K et al (2018) Evaluation of serum levels of oxidized and reduced glutathione and total antioxidant capacity in patients with head and neck squamous cell carcinoma. J Cancer Res Ther 14(2):428–431PubMedGoogle Scholar
  69. 69.
    Fujii S, Ozawa M. Expression and growth-promoting effect of adult T-cell leukemia-derived factorGoogle Scholar
  70. 70.
    Wakasugi N, Tagaya Y, Wakasugi H, Mitsui A, Maeda M, Yodoi J et al (1990) Adult T-cell leukemia-derived factor/thioredoxin, produced by both human T-lymphotropic virus type I- and Epstein–Barr virus-transformed lymphocytes, acts as an autocrine growth factor and synergizes with interleukin 1 and interleukin 2. Proc Natl Acad Sci USA 87(21):8282–8286PubMedCrossRefGoogle Scholar
  71. 71.
    Ceccarelli J, Delfino L, Zappia E, Castellani P, Borghi M, Ferrini S et al (2008) The redox state of the lung cancer microenvironment depends on the levels of thioredoxin expressed by tumor cells and affects tumor progression and response to prooxidants. Int J Cancer 123(8):1770–1778PubMedCrossRefGoogle Scholar
  72. 72.
    Gallegos A, Gasdaska JR, Taylor CW, Paine-Murrieta GD, Goodman D, Gasdaska PY et al (1996) Transfection with human thioredoxin increases cell proliferation and a dominant-negative mutant thioredoxin reverses the transformed phenotype of human breast cancer cells. Cancer Res 56(24):5765–5770PubMedGoogle Scholar
  73. 73.
    Matthews JR, Wakasugi N, Virelizier J-L, Yodoi J, Hay RT (1992) Thiordoxin regulates the DNA binding activity of NF-χB by reduction of a disulphid bond involving cysteine 62. Nucl Acids Res 20(15):3821–3830PubMedCrossRefGoogle Scholar
  74. 74.
    Wang C-Y, Mayo MW, Korneluk RG, Goeddel DV, Baldwin AS (1998) NF-κB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 281(5383):1680–1683PubMedCrossRefGoogle Scholar
  75. 75.
    Nakamura H, Nakamura K, Yodoi J (1997) Redox regulation of cellular activation. Annu Rev Immunol 15:351–369PubMedCrossRefGoogle Scholar
  76. 76.
    Zhang P, Liu B, Kang SW, Seo MS, Rhee SG, Obeid LM (1997) Thioredoxin peroxidase is a novel inhibitor of apoptosis with a mechanism distinct from that of Bcl-2. J Biol Chem 272(49):30615–30618PubMedCrossRefGoogle Scholar
  77. 77.
    Gan L, Yang XL, Liu Q, Xu HB (2005) Inhibitory effects of thioredoxin reductase antisense RNA on the growth of human hepatocellular carcinoma cells. J Cell Biochem 96(3):653–664PubMedCrossRefGoogle Scholar
  78. 78.
    Zheng X, Ma W, Sun R, Yin H, Lin F, Liu Y et al (2018) Butaselen prevents hepatocarcinogenesis and progression through inhibiting thioredoxin reductase activity. Redox Biol 14:237–249PubMedCrossRefGoogle Scholar
  79. 79.
    Farina AR, Tacconelli A, Cappabianca L, DeSantis G, Gulino A, Mackay AR (2003) Thioredoxin inhibits microvascular endothelial capillary tubule formation. Exp Cell Res 291(2):474–483PubMedCrossRefGoogle Scholar
  80. 80.
    Lincoln DT, Ali EE, Tonissen KF, Clarke FM (2003) The thioredoxin-thioredoxin reductase system: over-expression in human cancer. Anticancer Res 23(3B):2425–2433PubMedGoogle Scholar
  81. 81.
    Berggren M, Gallegos A, Gasdaska JR, Gasdaska PY, Warneke J, Powis G (1996) Thioredoxin and thioredoxin reductase gene expression in human tumors and cell lines, and the effects of serum stimulation and hypoxia. Anticancer Res 16(6B):3459–3466PubMedGoogle Scholar
  82. 82.
    Kim HJ, Chae HZ, Kim YJ, Kim YH, Hwangs TS, Park EM et al (2003) Preferential elevation of Prx I and Trx expression in lung cancer cells following hypoxia and in human lung cancer tissues. Cell Biol Toxicol 19(5):285–298PubMedCrossRefGoogle Scholar
  83. 83.
    Butler LM, Zhou X, Xu W-S, Scher HI, Rifkind RA, Marks PA et al (2002) The histone deacetylase inhibitor SAHA arrests cancer cell growth, up-regulates thioredoxin-binding protein-2, and down-regulates thioredoxin. Proc Natl Acad Sci 99(18):11700–11705PubMedCrossRefGoogle Scholar
  84. 84.
    Hashemy SI, Ungerstedt JS, Avval FZ, Holmgren A (2006) Motexafin gadolinium, a tumor-selective drug targeting thioredoxin reductase and ribonucleotide reductase. J Biol Chem 281(16):10691–10697PubMedCrossRefGoogle Scholar
  85. 85.
    Kunkel MW, Kirkpatrick DL, Johnson JI, Powis G (1997) Cell line-directed screening assay for inhibitors of thioredoxin reductase signaling as potential anti-cancer drugs. Anticancer Drug Des 12(8):659–670PubMedGoogle Scholar
  86. 86.
    Lu J, Chew E-H, Holmgren A (2007) Targeting thioredoxin reductase is a basis for cancer therapy by arsenic trioxide. Proc Natl Acad Sci 104(30):12288–12293PubMedCrossRefGoogle Scholar
  87. 87.
    Nordberg J, Zhong L, Holmgren A, Arnér ES (1998) Mammalian thioredoxin reductase is irreversibly inhibited by dinitrohalobenzenes by alkylation of both the redox active selenocysteine and its neighboring cysteine residue. J Biol Chem 273(18):10835–10842PubMedCrossRefGoogle Scholar
  88. 88.
    Rigobello MP, Folda A, Baldoin MC, Scutari G, Bindoli A (2005) Effect of auranofin on the mitochondrial generation of hydrogen peroxide. Role of thioredoxin reductase. Free Radic Res 39(7):687–695PubMedCrossRefGoogle Scholar
  89. 89.
    Witte A-B, Anestål K, Jerremalm E, Ehrsson H, Arnér ES (2005) Inhibition of thioredoxin reductase but not of glutathione reductase by the major classes of alkylating and platinum-containing anticancer compounds. Free Radic Biol Med 39(5):696–703PubMedCrossRefGoogle Scholar
  90. 90.
    Kirkpatrick DL, Kuperus M, Dowdeswell M, Potier N, Donald LJ, Kunkel M et al (1998) Mechanisms of inhibition of the thioredoxin growth factor system by antitumor 2-imidazolyl disulfides. Biochem Pharmacol 55(7):987–994PubMedCrossRefGoogle Scholar
  91. 91.
    Tan Y, Bi L, Zhang P, Wang F, Lin F, Ni W et al (2014) Thioredoxin-1 inhibitor PX-12 induces human acute myeloid leukemia cell apoptosis and enhances the sensitivity of cells to arsenic trioxide. Int J Clin Exp Pathol 7(8):4765PubMedPubMedCentralGoogle Scholar
  92. 92.
    Kirkpatrick DL, Ehrmantraut G, Stettner S, Kunkel M, Powis G (1997) Redox active disulfides: the thioredoxin system as a drug target. Oncol Res Featur Preclin Clin Cancer Ther 9(6–7):351–356Google Scholar
  93. 93.
    Baker AF, Dragovich T, Tate WR, Ramanathan RK, Roe D, Hsu C-H et al (2006) The antitumor thioredoxin-1 inhibitor PX-12 (1-methylpropyl 2-imidazolyl disulfide) decreases thioredoxin-1 and VEGF levels in cancer patient plasma. J Lab Clin Med 147(2):83–90PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Welsh SJ, Williams RR, Birmingham A, Newman DJ, Kirkpatrick DL, Powis G (2003) The thioredoxin redox inhibitors 1-methylpropyl 2-imidazolyl disulfide and pleurotin inhibit hypoxia-induced factor 1alpha and vascular endothelial growth factor formation. Mol Cancer Ther 2(3):235–243PubMedGoogle Scholar
  95. 95.
    Welsh SJ, Williams RR, Birmingham A, Newman DJ, Kirkpatrick DL, Powis G (2003) The thioredoxin redox inhibitors 1-methylpropyl 2-imidazolyl disulfide and pleurotin inhibit hypoxia-induced factor 1α and vascular endothelial growth factor formation 1. Mol Cancer Ther 2(3):235–243PubMedGoogle Scholar
  96. 96.
    Kirkpatrick L, Dragovich T, Ramanathan R, Sharlow E, Chow S, Williams D et al (2004) Results from phase I study of PX-12, a thioredoxin inhibitor in patients with advanced solid malignancies. J Clin Oncol 22(14_suppl):3089CrossRefGoogle Scholar
  97. 97.
    Seidel C, Florean C, Schnekenburger M, Dicato M, Diederich M (2012) Chromatin-modifying agents in anti-cancer therapy. Biochimie 94(11):2264–2279PubMedCrossRefGoogle Scholar
  98. 98.
    Marks PA, Richon VM, Rifkind RA (2000) Histone deacetylase inhibitors: inducers of differentiation or apoptosis of transformed cells. J Natl Cancer Inst 92(15):1210–1216PubMedCrossRefGoogle Scholar
  99. 99.
    Dokmanovic M, Clarke C, Marks PA (2007) Histone deacetylase inhibitors: overview and perspectives. Mol Cancer Res 5(10):981–989PubMedCrossRefGoogle Scholar
  100. 100.
    Thiagalingam S, Cheng KH, Lee HJ, Mineva N, Thiagalingam A, Ponte JF (2003) Histone deacetylases: unique players in shaping the epigenetic histone code. Ann NY Acad Sci 983(1):84–100PubMedCrossRefGoogle Scholar
  101. 101.
    Wang Z-Y, Qin W, Yi F (2015) Targeting histone deacetylases: perspectives for epigenetic-based therapy in cardio-cerebrovascular disease. J Geriatr Cardiol 12(2):153PubMedPubMedCentralGoogle Scholar
  102. 102.
    Richon VM, Emiliani S, Verdin E, Webb Y, Breslow R, Rifkind RA et al (1998) A class of hybrid polar inducers of transformed cell differentiation inhibits histone deacetylases. Proc Natl Acad Sci 95(6):3003–3007PubMedCrossRefGoogle Scholar
  103. 103.
    Mann BS, Johnson JR, Cohen MH, Justice R, Pazdur R (2007) FDA approval summary: vorinostat for treatment of advanced primary cutaneous T-cell lymphoma. Oncologist 12(10):1247–1252PubMedCrossRefGoogle Scholar
  104. 104.
    Glaser KB (2007) HDAC inhibitors: clinical update and mechanism-based potential. Biochem Pharmacol 74(5):659–671PubMedCrossRefGoogle Scholar
  105. 105.
    Richon V (2006) Cancer biology: mechanism of antitumour action of vorinostat (suberoylanilide hydroxamic acid), a novel histone deacetylase inhibitor. Br J Cancer 95(S1):S2PubMedCentralCrossRefGoogle Scholar
  106. 106.
    Marks PA, Rifkind RA, Richon VM, Breslow R, Miller T, Kelly WK (2001) Histone deacetylases and cancer: causes and therapies. Nat Rev Cancer 1(3):194PubMedCrossRefGoogle Scholar
  107. 107.
    Rosato RR, Grant S (2004) Histone deacetylase inhibitors in clinical development. Expert Opin Investig Drugs 13(1):21–38PubMedCrossRefGoogle Scholar
  108. 108.
    Zhang C, Richon V, Ni X, Talpur R, Duvic M (2005) Selective induction of apoptosis by histone deacetylase inhibitor SAHA in cutaneous T-cell lymphoma cells: relevance to mechanism of therapeutic action. J Investig Dermatol 125(5):1045–1052PubMedCrossRefGoogle Scholar
  109. 109.
    Ungerstedt JS, Sowa Y, Xu WS, Shao Y, Dokmanovic M, Perez G et al (2005) Role of thioredoxin in the response of normal and transformed cells to histone deacetylase inhibitors. Proc Natl Acad Sci USA 102(3):673–678PubMedCrossRefGoogle Scholar
  110. 110.
    Tan J, Zhuang L, Jiang X, Yang KK, Karuturi KM, Yu Q (2006) Apoptosis signal-regulating kinase 1 is a direct target of E2F1 and contributes to histone deacetylase inhibitor-induced apoptosis through positive feedback regulation of E2F1 apoptotic activity. J Biol ChemGoogle Scholar
  111. 111.
    Kerimova AA, Atalay M, Yusifov EY, Kuprin SP, Kerimov TM (2000) Antioxidant enzymes; possible mechanism of gold compound treatment in rheumatoid arthritis. Pathophysiology 7(3):209–213PubMedCrossRefGoogle Scholar
  112. 112.
    Shaw CF (1999) Gold-based therapeutic agents. Chem Rev 99(9):2589–2600CrossRefGoogle Scholar
  113. 113.
    Milacic V, Fregona D, Dou QP (2008) Gold complexes as prospective metal-based anticancer drugs. Histol Histopathol 23(1):101–108PubMedGoogle Scholar
  114. 114.
    Ronconi L, Giovagnini L, Marzano C, Bettìo F, Graziani R, Pilloni G et al (2005) Gold dithiocarbamate derivatives as potential antineoplastic agents: design, spectroscopic properties, and in vitro antitumor activity. Inorg Chem 44(6):1867–1881PubMedCrossRefGoogle Scholar
  115. 115.
    Gromer S, Arscott LD, Williams CH, Schirmer RH, Becker K (1998) Human placenta thioredoxin reductase isolation of the selenoenzyme, steady state kinetics, and inhibition by therapeutic gold compounds. J Biol Chem 273(32):20096–20101PubMedCrossRefGoogle Scholar
  116. 116.
    Marzano C, Gandin V, Folda A, Scutari G, Bindoli A, Rigobello MP (2007) Inhibition of thioredoxin reductase by auranofin induces apoptosis in cisplatin-resistant human ovarian cancer cells. Free Radic Biol Med 42(6):872–881PubMedCrossRefGoogle Scholar
  117. 117.
    Rigobello MP, Scutari G, Boscolo R, Bindoli A (2002) Induction of mitochondrial permeability transition by auranofin, a Gold (I)-phosphine derivative. Br J Pharmacol 136(8):1162–1168PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Rigobello MP, Scutari G, Folda A, Bindoli A (2004) Mitochondrial thioredoxin reductase inhibition by gold (I) compounds and concurrent stimulation of permeability transition and release of cytochrome c. Biochem Pharmacol 67(4):689–696PubMedCrossRefGoogle Scholar
  119. 119.
    Rackham O, Nichols SJ, Leedman PJ, Berners-Price SJ, Filipovska A (2007) A gold (I) phosphine complex selectively induces apoptosis in breast cancer cells: implications for anticancer therapeutics targeted to mitochondria. Biochem Pharmacol 74(7):992–1002PubMedCrossRefGoogle Scholar
  120. 120.
    Omata Y, Folan M, Shaw M, Messer RL, Lockwood PE, Hobbs D et al (2006) Sublethal concentrations of diverse gold compounds inhibit mammalian cytosolic thioredoxin reductase (TrxR1). Toxicol In Vitro 20(6):882–890PubMedCrossRefGoogle Scholar
  121. 121.
    Chen G-Q, Zhu J, Shi X-G, Ni J, Zhong H, Si G et al (1996) In vitro studies on cellular and molecular mechanisms of arsenic trioxide (As2O3) in the treatment of acute promyelocytic leukemia: as2O3 induces NB4 cell apoptosis with downregulation of Bcl-2 expression and modulation of PML-RAR alpha/PML proteins. Blood 88(3):1052–1061PubMedCrossRefGoogle Scholar
  122. 122.
    Douer D, Tallman MS (2005) Arsenic trioxide: new clinical experience with an old medication in hematologic malignancies. J Clin Oncol 23(10):2396–2410PubMedCrossRefGoogle Scholar
  123. 123.
    Mayorga J, Richardson-Hardin C, Dicke KA (2002) Arsenic trioxide as effective therapy for relapsed acute promyelocytic leukemia. Clin J Oncol Nurs 6(6)PubMedCrossRefGoogle Scholar
  124. 124.
    Ralph SJ (2008). Arsenic-based antineoplastic drugs and their mechanisms of action. Met Based Drugs 2008Google Scholar
  125. 125.
    Miller WH, Schipper HM, Lee JS, Singer J, Waxman S (2002) Mechanisms of action of arsenic trioxide. Cancer Res 62(14):3893–3903PubMedGoogle Scholar
  126. 126.
    Terheyden P, Kortüm A-K, Schulze H-J, Durani B, Remling R, Mauch C et al (2007) Chemoimmunotherapy for cutaneous melanoma with dacarbazine and epifocal contact sensitizers: results of a nationwide survey of the German Dermatologic Co-operative Oncology Group. J Cancer Res Clin Oncol 133(7):437–444PubMedCrossRefGoogle Scholar
  127. 127.
    Ma S, Caprioli RM, Hill KE, Burk RF (2003) Loss of selenium from selenoproteins: conversion of selenocysteine to dehydroalanine in vitro. J Am Soc Mass Spectrom 14(6):593–600PubMedCrossRefGoogle Scholar
  128. 128.
    Arnér ES (1999) Superoxide production by dinitrophenyl-derivatized thioredoxin reductase–a model for the mechanism and correlation to immunostimulation by dinitrohalobenzenes. BioFactors 10(2–3):219–226PubMedCrossRefGoogle Scholar
  129. 129.
    Cenas N, Nivinskas H, Anusevicius Z, Sarlauskas J, Lederer F, Arnér ES (2004) Interactions of quinones with thioredoxin reductase a challenge to the antioxidant role of the mammalian selenoprotein. J Biol Chem 279(4):2583–2592PubMedCrossRefGoogle Scholar
  130. 130.
    Boulikas T, Vougiouka M (2004) Recent clinical trials using cisplatin, carboplatin and their combination chemotherapy drugs. Oncol Rep 11(3):559–595PubMedGoogle Scholar
  131. 131.
    Urig S, Becker K (eds) (2006) On the potential of thioredoxin reductase inhibitors for cancer therapy. Seminars in cancer biology. Elsevier, AmsterdamGoogle Scholar
  132. 132.
    Wang D, Lippard SJ (2005) Cellular processing of platinum anticancer drugs. Nat Rev Drug Discov 4(4):307PubMedCrossRefGoogle Scholar
  133. 133.
    Arnér ES, Nakamura H, Sasada T, Yodoi J, Holmgren A, Spyrou G (2001) Analysis of the inhibition of mammalian thioredoxin, thioredoxin reductase, and glutaredoxin by cis-diamminedichloroplatinum (II) and its major metabolite, the glutathione-platinum complex. Free Radic Biol Med 31(10):1170–1178PubMedCrossRefGoogle Scholar
  134. 134.
    Lu J, Papp LV, Fang J, Rodriguez-Nieto S, Zhivotovsky B, Holmgren A (2006) Inhibition of mammalian thioredoxin reductase by some flavonoids: implications for myricetin and quercetin anticancer activity. Cancer Res 66(8):4410–4418PubMedCrossRefGoogle Scholar
  135. 135.
    Soltani A, Salmaninejad A, Jalili‐Nik M, Soleimani A, Javid H, Hashemy SI, et al (2018) 5′‐Adenosine monophosphate‐activated protein kinase: a potential target for disease prevention by curcumin. J Cell PhysGoogle Scholar
  136. 136.
    Boroumand N, Samarghandian S, Hashemy SI (2018) Immunomodulatory, anti-inflammatory, and antioxidant effects of curcumin. J Herbmed Pharmacol 7(4):211–219CrossRefGoogle Scholar
  137. 137.
    Ghahremanlo A, Boroumand N, Ghazvini K, Hashemy SI (2018) Herbal medicine in oral lichen planus. Phytother ResGoogle Scholar
  138. 138.
    Fang J, Lu J, Holmgren A (2005) Thioredoxin reductase is irreversibly modified by curcumin a novel molecular mechanism for its anticancer activity. J Biol Chem 280(26):25284–25290PubMedCrossRefGoogle Scholar
  139. 139.
    Piaz F, Braca A, Belisario M, De Tommasi N (2010) Thioredoxin system modulation by plant and fungal secondary metabolites. Curr Med Chem 17(5):479–494CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Clinical Biochemistry, Faculty of MedicineMashhad University of Medical SciencesMashhadIran
  2. 2.Student Research Committee, Faculty of MedicineMashhad University of Medical SciencesMashhadIran
  3. 3.Surgical Oncology Research CenterMashhad University of Medical SciencesMashhadIran

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