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Original Article

Phenethyl isothiocyanate, by virtue of its antioxidant activity, inhibits invasiveness and metastatic potential of breast cancer cells: HIF-1α as a putative target

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Pages 84-100 | Received 02 Jul 2015, Accepted 11 Oct 2015, Published online: 07 Dec 2015

References

  • Fang Y, Chen Y, Yu L, Zheng C, Qi Y, Li Z, et al. Inhibition of breast cancer metastases by a novel inhibitor of TGFβ receptor 1. J Natl Cancer Inst 2013;105:47–58.
  • Wang Y. Breast cancer metastasis driven by ErbB2 and 14-3-3zeta: a division of labor. Cell Adh Migr 2010;4:7–9.
  • Hwang ES, Lee HJ. Phenylethyl isothiocyanate and its N-acetylcysteine conjugate suppress the metastasis of SK-Hep1 human hepatoma cells. J Nutr Biochem 2006;17:837–846.
  • Calvani M, Comito G, Giannoni E, Chiarugi P. Time-dependent stabilization of hypoxia inducible factor-1α by different intracellular sources of reactive oxygen species. PLoS One 2012;7:e38388.
  • Vaupel P, Harrison L. Tumor hypoxia: causative factors, compensatory mechanisms, and cellular response. Oncologist 2004;9:4–9.
  • Manda G, Nechifor MT, Neagu TM. Reactive oxygen species, cancer and anti-cancer therapies. Curr Chem Biol 2009;3:342–366.
  • Waris G, Ahsan H. Reactive oxygen species: role in the development of cancer and various chronic conditions. J Carcinog 2006;5:14.
  • Bell EL, Klimova TA, Eisenbart J, Schumacker PT, Chandel NS. Mitochondrial reactive oxygen species trigger hypoxia-inducible factor-dependent extension of the replicative life span during hypoxia. Mol Cell Biol 2007;27:5737–5745.
  • Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA, Rodriguez AM, Schumacker PT. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem 2000;275:25130–25138.
  • Acharya A, Das I, Chandhok D, Saha T. Redox regulation in cancer: a double-edged sword with therapeutic potential. Oxid Med Cell Longev 2010;3:23–34.
  • Liou GY, Storz P. Reactive oxygen species in cancer. Free Radic Res 2010;44:479–496.
  • Liao D, Corle C, Seagroves TN, Johnson RS. Hypoxia-inducible factor-1alpha is a key regulator of metastasis in a transgenic model of cancer initiation and progression. Cancer Res 2007;67:563–572.
  • Galanis A, Pappa A, Giannakakis A, Lanitis E, Dangaj D, Sandaltzopoulos R. Reactive oxygen species and HIF-1 signalling in cancer. Cancer Lett 2008;266:12–20.
  • López-Lázaro M. HIF-1: hypoxia-inducible factor or dysoxia-inducible factor? FASEB J 2006;20:828–832.
  • Wu S, Kasim V, Kano MR, Tanaka S, Ohba S, Miura Y, et al. Transcription factor YY1 contributes to tumor growth by stabilizing hypoxia factor HIF-1α in a p53-independent manner. Cancer Res 2013;73:1787–1799.
  • Du J, Xu R, Hu Z, Tian Y, Zhu Y, Gu L, Zhou L. PI3K and ERK-induced Rac1 activation mediates hypoxia-induced HIF-1α expression in MCF-7 breast cancer cells. PLoS One 2011;6:e25213.
  • Park JH, Kim TY, Jong HS, Kim TY, Chun YS, Park JW, et al. Gastric epithelial reactive oxygen species prevent normoxic degradation of hypoxia-inducible factor-1alpha in gastric cancer cells. Clin Cancer Res 2003;9:433–440.
  • Ke Q, Costa M. Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol 2006;70:1469–1480.
  • Shi YH, Wang YX, Bingle L, Gong LH, Heng WJ, Li Y, Fang WG. In vitro study of HIF-1 activation and VEGF release by bFGF in the T47D breast cancer cell line under normoxic conditions: involvement of PI-3K/Akt and MEK1/ERK pathways. J Pathol 2005;205:530–536.
  • Liu Y, Cui Y, Shi M, Zhang Q, Wang Q, Chen X. Deferoxamine promotes MDA-MB-231 cell migration and invasion through increased ROS-dependent HIF-1α accumulation. Cell Physiol Biochem 2014;33:1036–1046.
  • Katschinski DM, Le L, Schindler SG, Thomas T, Voss AK, Wenger RH. Interaction of the PAS B domain with HSP90 accelerates hypoxia-inducible factor-1alpha stabilization. Cell Physiol Biochem 2004;14:351–360.
  • Li Y, Zhang T, Schwartz SJ, Sun D. New developments in Hsp90 inhibitors as anti-cancer therapeutics: mechanisms, clinical perspective and more potential. Drug Resist Updat 2009;12:17–27.
  • Barliya T, Mandel M, Livnat T, Weinberger D, Lavie G. Degradation of HIF-1alpha under hypoxia combined with induction of Hsp90 polyubiquitination in cancer cells by hypericin: a unique cancer therapy. PLoS One 2011;6:e22849.
  • Lee JM, Lee WH, Kay HY, Kim ES, Moon A, Kim SG. Hemin, an iron-binding porphyrin, inhibits HIF-1α induction through its binding with heat shock protein 90. Int J Cancer 2012;130:716–727.
  • Sarkar R, Mukherjee A, Mukherjee S, Biswas R, Biswas J, Roy M. Curcumin augments the efficacy of antitumor drugs used in leukemia by modulation of heat shock proteins via HDAC6. J Environ Pathol Toxicol Oncol 2014;33:247–263.
  • Singh B, Chatterjee A, Ronghe AM, Bhat NK, Bhat HK. Antioxidant-mediated up-regulation of OGG1 via NRF2 induction is associated with inhibition of oxidative DNA damage in estrogen-induced breast cancer. BMC Cancer 2013;13:253.
  • Cardozo LF, Pedruzzi LM, Stenvinkel P, Stockler-Pinto MB, Daleprane JB, Leite Jr M, Mafra D. Nutritional strategies to modulate inflammation and oxidative stress pathways via activation of the master antioxidant switch Nrf2. Biochimie 2013;95:1525–1533.
  • Yang Y, Cai X, Yang J, Sun X, Hu C, Yan Z, et al. Chemoprevention of dietary digitoflavone on colitis-associated colon tumorigenesis through inducing Nrf2 signaling pathway and inhibition of inflammation. Mol Cancer 2014;13:48.
  • Funes JM, Henderson S, Kaufman R, Flanagan JM, Robson M, Pedley B, et al. Oncogenic transformation of mesenchymal stem cells decreases Nrf2 expression favoring in vivo tumor growth and poorer survival. Mol Cancer 2014;13:20.
  • Loignon M, Miao W, Hu L, Bier A, Bismar TA, Scrivens PJ, et al. Cul3 overexpression depletes Nrf2 in breast cancer and is associated with sensitivity to carcinogens, to oxidative stress, and to chemotherapy. Mol Cancer Ther 2009;8:2432–2440.
  • Thangasamy A, Rogge J, Krishnegowda NK, Freeman JW, Ammanamanchi S. Novel function of transcription factor Nrf2 as an inhibitor of RON tyrosine kinase receptor-mediated cancer cell invasion. J Biol Chem 2011;286:32115–32122.
  • Satoh H, Moriguchi T, Taguchi K, Takai J, Maher JM, Suzuki T, et al. Nrf2-deficiency creates a responsive microenvironment for metastasis to the lung. Carcinogenesis 2010;31:1833–1843.
  • Shelton P, Jaiswal AK. The transcription factor NF-E2-related factor 2 (Nrf2): a protooncogene? FASEB J 2013;27:414–423.
  • Kim WD, Kim YW, Cho IJ, Lee CH, Kim SG. E-cadherin inhibits nuclear accumulation of Nrf2: implications for chemoresistance of cancer cells. J Cell Sci 2012;125:1284–1295.
  • Rahman K. Studies on free radicals, antioxidants, and co-factors. Clin Interv Aging 2007;2:219–236.
  • Mohd Ghazali MA, Al-Naqeb G, Krishnan Selvarajan K, Hazizul Hasan M, Adam A. Apoptosis induction by Polygonum minus is related to antioxidant capacity, alterations in expression of apoptotic-related genes, and S-phase cell cycle arrest in HepG2 cell line. Biomed Res Int 2014;2014:539607.
  • Prasad KN. Multiple dietary antioxidants enhance the efficacy of standard and experimental cancer therapies and decrease their toxicity. Integr Cancer Ther 2004;3:310–322.
  • Dey M, Kuhn P, Ribnicky D, Premkumar V, Reuhl K, Raskin I. Dietary phenethylisothiocyanate attenuates bowel inflammation in mice. BMC Chem Biol 2010;10:4 (also in discussion).
  • Liu Y, Chakravarty S, Dey M. Phenethylisothiocyanate alters site- and promoter-specific histone tail modifications in cancer cells. PLoS One 2013;8:e64535 (also in discussion).
  • Valgimigli L, Iori R. Antioxidant and pro-oxidant capacities of ITCs. Environ Mol Mutagen 2009;50:222–237.
  • Gerhäuser C, Klimo K, Heiss E, Neumann I, Gamal-Eldeen A, Knauft J, et al. Mechanism-based in vitro screening of potential cancer chemopreventive agents. Mutat Res 2003;523-524:163–172.
  • Lee KY, Shibutani M, Kuroiwa K, Takagi H, Inoue K, Nishikawa H, et al. Chemoprevention of acrylamide toxicity by antioxidative agents in rats–effective suppression of testicular toxicity by phenylethyl isothiocyanate. Arch Toxicol 2005;79:531–541.
  • Dey M, Ribnicky D, Kurmukov AG, Raskin I. In vitro and in vivo anti-inflammatory activity of a seed preparation containing phenethylisothiocyanate. J Pharmacol Exp Ther 2006;317:326–333.
  • Tosetti F, Noonan DM, Albini A. Metabolic regulation and redox activity as mechanisms for angioprevention by dietary phytochemicals. Int J Cancer 2009;125:1997–2003.
  • Okulicz M, Bialik I, Chichłowska J. The time-dependent effect of gluconasturtiin and phenethyl isothiocyanate on metabolic and antioxidative parameters in rats. J Anim Physiol Anim Nutr (Berl) 2005;89:367–372.
  • Lai C-S, Pan M-H. Mechanism for possible chemopreventive effects of natural dietary compounds on smoking-induced tumorigenesis. J Exp Clin Med 2011;3:262–271.
  • Syed Alwi SS, Cavell BE, Donlevy A, Packham G. Differential induction of apoptosis in human breast cancer cell lines by phenethyl isothiocyanate, a glutathione depleting agent. Cell Stress Chaperones 2012;17:529–538.
  • Sarkars R, Mukherjee S, Roy M. Targeting heat shock proteins by phenethyl isothiocyanate results in cell-cycle arrest and apoptosis of human breast cancer cells. Nutr Cancer 2013;65:480–493.
  • Blois MS. 1958. Antioxidant determinations by the use of a stable free radical. Nature 181:1199–1200.
  • Hayes SA, Huang X, Kambhampati S, Platanias LC, Bergan RC. p38 MAP kinase modulates Smad-dependent changes in human prostate cell adhesion. Oncogene 2003;22:4841–4850.
  • Thoreson MA, Anastasiadis PZ, Daniel JM, Ireton RC, Wheelock MJ, Johnson KR, et al. Selective uncoupling of p120(ctn) from E-cadherin disrupts strong adhesion. J Cell Biol 2000;148:189–202.
  • Martínez-Sánchez G, Giuliani A. Cellular redox status regulates hypoxia inducible factor-1 activity. Role in tumour development. J Exp Clin Cancer Res 2007;26:39–50.
  • Veeravalli KK, Chetty C, Ponnala S, Gondi CS, Lakka SS, Fassett D, et al. MMP-9, uPAR and cathepsin B silencing downregulate integrins in human glioma xenograft cells in vitro and in vivo in nude mice. PLoS One 2010;5:e11583.
  • Mercurio AM, Lipscomb EA, Bachelder RE. Non-angiogenic functions of VEGF in breast cancer. J Mammary Gland Biol Neoplasia 2005;10:283–290 (also in discussion).
  • Sethi N, Kang Y. Unravelling the complexity of metastasis - molecular understanding and targeted therapies. Nat Rev Cancer 2011;11:735–748.
  • Khan N, Mukhtar H. Cancer and metastasis: prevention and treatment by green tea. Cancer Metastasis Rev 2010;29:435–445.
  • Liu ZJ, Semenza GL, Zhang HF. Hypoxia-inducible factor 1 and breast cancer metastasis. J Zhejiang Univ Sci B 2015;16:32–43.
  • Jezierska-Drutel A, Rosenzweig SA, Neumann CA. Role of oxidative stress and the microenvironment in breast cancer development and progression. Adv Cancer Res 2013;119:107–125.
  • Brown NS, Bicknell R. Hypoxia and oxidative stress in breast cancer. Oxidative stress: its effects on the growth, metastatic potential and response to therapy of breast cancer. Breast Cancer Res 2001;3:323–327.
  • Wang J, Yi J. Cancer cell killing via ROS: to increase or decrease, that is the question. Cancer Biol Ther 2008;7:1875–1884.
  • Han ZB, Ren H, Zhao H, Chi Y, Chen K, Zhou B, et al. Hypoxia-inducible factor (HIF)-1 alpha directly enhances the transcriptional activity of stem cell factor (SCF) in response to hypoxia and epidermal growth factor (EGF). Carcinogenesis 2008;29:1853–1861.
  • Sahu D, Zhao Z, Tsen F, Cheng CF, Park R, Situ AJ, et al. A potentially common peptide target in secreted heat shock protein-90α for hypoxia-inducible factor-1α-positive tumors. Mol Biol Cell 2012;23:602–613.
  • Jung SN, Yang WK, Kim J, Kim HS, Kim EJ, Yun H, et al. Reactive oxygen species stabilize hypoxia-inducible factor-1 alpha protein and stimulate transcriptional activity via AMP-activated protein kinase in DU145 human prostate cancer cells. Carcinogenesis 2008;29:713–721.
  • Manesh C, Kuttan G. Anti-tumour and anti-oxidant activity of naturally occurring isothiocyanates. J Exp Clin Cancer Res 2003;22:193–199.
  • Isaacs JS, Jung YJ, Mimnaugh EG, Martinez A, Cuttitta F, Neckers LM. Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1 alpha-degradative pathway. J Biol Chem 2002;277:29936–29944.
  • Minet E, Mottet D, Michel G, Roland I, Raes M, Remacle J, Michiels C. Hypoxia-induced activation of HIF-1: role of HIF-1alpha-Hsp90 interaction. FEBS Lett 1999;460:251–256.
  • Wang XH, Cavell BE, Syed Alwi SS, Packham G. Inhibition of hypoxia inducible factor by phenethyl isothiocyanate. Biochem Pharmacol 2009; 78:261–272.
  • Cronin PA, Wang JH, Redmond HP. Hypoxia increases the metastatic ability of breast cancer cells via upregulation of CXCR4. BMC Cancer 2010;10:225.
  • Benson CS, Babu SD, Radhakrishna S, Selvamurugan N, Ravi Sankar B. Expression of matrix metalloproteinases in human breast cancer tissues. Dis Markers 2013;34:395–405.
  • Shi J, Wan Y, Di W. Effect of hypoxia and re-oxygenation on cell invasion and adhesion in human ovarian carcinoma cells. Oncol Rep 2008;20:803–807.
  • Muñoz-Nájar UM, Neurath KM, Vumbaca F, Claffey KP. Hypoxia stimulates breast carcinoma cell invasion through MT1-MMP and MMP-2 activation. Oncogene 2006;25:2379–2392.
  • Krishnamachary B, Zagzag D, Nagasawa H, Rainey K, Okuyama H, Baek JH, Semenza GL. Hypoxia-inducible factor-1-dependent repression of E-cadherin in von Hippel-Lindau tumor suppressor-null renal cell carcinoma mediated by TCF3, ZFHX1A, and ZFHX1B. Cancer Res 2006;66:2725–2731.
  • Choi JY, Jang YS, Min SY, Song JY. Overexpression of MMP-9 and HIF-1α in breast cancer cells under hypoxic conditions. J Breast Cancer 2011;14:88–495.
  • Shemirani B, Crowe DL. Hypoxic induction of HIF-1alpha and VEGF expression in head and neck squamous cell carcinoma lines is mediated by stress activated protein kinases. Oral Oncol 2002;38:251–257.

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