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Articles

Sulforaphane Suppresses MCF-7 Breast Cancer Cells Growth via miR-19/PTEN Axis to Antagonize the Effect of Butyl Benzyl Phthalate

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Pages 980-991 | Received 07 Jul 2022, Accepted 05 Dec 2022, Published online: 21 Dec 2022

References

  • Kaiser AE, Baniasadi M, Giansiracusa D, Giansiracusa M, Garcia M, Fryda Z, Wong TL, Bishayee A. Sulforaphane: a broccoli bioactive phytocompound with cancer preventive potential. Cancers. 2021;13(19):4796.
  • Herr I, Buchler MW. Dietary constituents of broccoli and other cruciferous vegetables: implications for prevention and therapy of cancer. Cancer Treat Rev. 2010;36(5):377–83.
  • Cohen JH, Kristal AR, Stanford JL. Fruit and vegetable intakes and prostate cancer risk. J Natl Cancer Inst. 2000;92(1):61–8.
  • Traka MH, Melchini A, Coode-Bate J, Al Kadhi O, Saha S, Defernez M, Troncoso-Rey P, Kibblewhite H, O'Neill CM, Bernuzzi F, et al. Transcriptional changes in prostate of men on active surveillance after a 12-mo glucoraphanin-rich broccoli intervention-results from the Effect of Sulforaphane on prostate CAncer PrEvention (ESCAPE) randomized controlled trial. Am J Clin Nutr. 2019;109(4):1133–44.
  • Núñez-Iglesias MJ, Novío S, García C, Pérez-Muñuzuri E, Soengas P, Cartea E, Velasco P, Freire-Garabal M. Glucosinolate-degradation products as co-adjuvant therapy on prostate cancer in vitro. Int J Mol Sci. 2019;20(20):4977.
  • Burnett JP, Lim G, Li Y, Shah RB, Lim R, Paholak HJ, McDermott SP, Sun L, Tsume Y, Bai S, et al. Sulforaphane enhances the anticancer activity of taxanes against triple negative breast cancer by killing cancer stem cells. Cancer Lett. 2017;394:52–64.
  • Centers for Disease Control and Prevention. 2010. Fourth national report on human exposure to environmental chemicals. Washington, DC.
  • Vimalkumar K, Zhu H, Kannan K. Widespread occurrence of phthalate and non-phthalate plasticizers in single-use facemasks collected in the United States. Environ Int. 2022;158:106967.
  • Matsumoto M, Hirata-Koizumi M, Ema M. Potential adverse effects of phthalic acid esters on human health: a review of recent studies on reproduction. Regul Toxicol Pharmacol. 2008;50(1):37–49.
  • Zhou L, Chen H, Xu Q, Han X, Zhao Y, Song X, Zhao T, Ye L. The effect of di-2-ethylhexyl phthalate on inflammation and lipid metabolic disorder in rats. Ecotoxicol Environ Saf. 2019;170:391–8.
  • Hsieh T-H, Tsai C-F, Hsu C-Y, Kuo P-L, Lee J-N, Chai C-Y, Wang S-C, Tsai E-M. Phthalates induce proliferation and invasiveness of estrogen receptor-negative breast cancer through the AhR/HDAC6/c-Myc signaling pathway. Faseb J. 2012;26(2):778–87.
  • Zhang X, Cheng C, Zhang G, Xiao M, Li L, Wu S, Lu X. Co-exposure to BPA and DEHP enhances susceptibility of mammary tumors via up-regulating Esr1/HDAC6 pathway in female rats. Ecotoxicol Environ Saf. 2021;221:112453.
  • Ahern TP, Broe A, Lash TL, Cronin-Fenton DP, Ulrichsen SP, Christiansen PM, Cole BF, Tamimi RM, Sørensen HT, Damkier P, et al. Phthalate exposure and breast cancer incidence: a danish nationwide cohort study. J Clin Oncol. 2019;37(21):1800–9.
  • Pei XQ, Song M, Guo M, Mo FF, Shen XY. Concentration and risk assessment of phthalates present in indoor air from newly decorated apartments. Atmos Environ. 2013;68:17–23.
  • Kay VR, Chambers C, Foster WG. Reproductive and developmental effects of phthalate diesters in females. Crit Rev Toxicol. 2013;43(3):200–19.
  • Al-Saleh I, Elkhatib R. Screening of phthalate esters in 47 branded perfumes. Environ Sci Pollut Res Int. 2016;23(1):455–68.
  • Harris CA, Henttu P, Parker MG, Sumpter JP. The estrogenic activity of phthalate esters in vitro. Environ Health Perspect. 1997;105(8):802–11.
  • Olive V, Bennett MJ, Walker JC, Ma C, Jiang I, Cordon-Cardo C, Li Q-J, Lowe SW, Hannon GJ, He L, et al. miR-19 is a key oncogenic component of mir-17-92. Genes Dev. 2009;23(24):2839–49.
  • Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer. 2006;6(11):857–66.
  • Yin L, Xiao X, Georgikou C, Yin Y, Liu L, Karakhanova S, Luo Y, Gladkich J, Fellenberg J, Sticht C, et al. MicroRNA-365a-3p inhibits c-Rel-mediated NF-kappaB signaling and the progression of pancreatic cancer. Cancer Lett. 2019;452:203–12.
  • Li Q, Yao Y, Eades G, Liu Z, Zhang Y, Zhou Q. Downregulation of miR-140 promotes cancer stem cell formation in basal-like early stage breast cancer. Oncogene. 2014;33(20):2589–600.
  • Banerjee N, Wang H, Wang G, Boor PJ, Khan MF. Differential expression of miRNAs in trichloroethene-mediated inflammatory/autoimmune response and its modulation by sulforaphane: delineating the role of miRNA-21 and miRNA-690. Front Immunol. 2022;13:868539.
  • Wang X, Lv Z, Han B, Li S, Yang Q, Wu P, Li J, Han B, Deng N, Zhang Z, et al. The aggravation of allergic airway inflammation with dibutyl phthalate involved in Nrf2-mediated activation of the mast cells. Sci Total Environ. 2021;789:148029.
  • Jiang X-P, Tang J-Y, Xu Z, Han P, Qin Z-Q, Yang C-d, Wang S-Q, Tang M, Wang W, Qin C, et al. Sulforaphane attenuates di-N-butylphthalate-induced reproductive damage in pubertal mice: Involvement of the Nrf2-antioxidant system. Environ Toxicol. 2017;32(7):1908–17.
  • Wu J, Jiang Y, Cao W, Li X, Xie C, Geng S, Zhu M, Liang Z, Zhu J, Zhu W, et al. miR-19 targeting of PTEN mediates butyl benzyl phthalate-induced proliferation in both ER(+) and ER(-) breast cancer cells. Toxicol Lett. 2018;295:124–33.
  • Zhu J, Wang S, Chen Y, Li X, Jiang Y, Yang X, Li Y, Wang X, Meng Y, Zhu M, et al. miR-19 targeting of GSK3β mediates sulforaphane suppression of lung cancer stem cells. J Nutr Biochem. 2017;44:80–91.
  • Aumeeruddy MZ, Mahomoodally MF. Combating breast cancer using combination therapy with 3 phytochemicals: piperine, sulforaphane, and thymoquinone. Cancer. 2019;125(10):1600–11.
  • Li Y, Zhang T, Korkaya H, Liu S, Lee H-F, Newman B, Yu Y, Clouthier SG, Schwartz SJ, Wicha MS, et al. Sulforaphane, a dietary component of broccoli/broccoli sprouts, inhibits breast cancer stem cells. Clin Cancer Res. 2010;16(9):2580–90.
  • Pledgie-Tracy A, Sobolewski MD, Davidson NE. Sulforaphane induces cell type-specific apoptosis in human breast cancer cell lines. Mol Cancer Ther. 2007;6(3):1013–21.
  • Kanematsu S, Uehara N, Miki H, Yoshizawa K, Kawanaka A, Yuri T, Tsubura A. Autophagy inhibition enhances sulforaphane-induced apoptosis in human breast cancer cells. Anticancer Res. 2010;30(9):3381–90.
  • Hsieh T-H, Tsai C-F, Hsu C-Y, Kuo P-L, Hsi E, Suen J-L, Hung C-H, Lee J-N, Chai C-Y, Wang S-C, et al. n-Butyl benzyl phthalate promotes breast cancer progression by inducing expression of lymphoid enhancer factor 1. PloS One. 2012;7(8):e42750.
  • Wang Y-C, Tsai C-F, Chuang H-L, Chang Y-C, Chen H-S, Lee J-N, Tsai E-M. Benzyl butyl phthalate promotes breast cancer stem cell expansion via SPHK1/S1P/S1PR3 signaling. Oncotarget. 2016;7(20):29563–76.
  • Chen FP, Chien MH, Chern IY. Impact of low concentrations of phthalates on the effects of 17β-estradiol in MCF-7 breast cancer cells. Taiwan J Obstet Gynecol. 2016;55(6):826–34.
  • Wang G, Gormley M, Qiao J, Zhao Q, Wang M, Di Sante G, Deng S, Dong L, Pestell T, Ju X, et al. Cyclin D1-mediated microRNA expression signature predicts breast cancer outcome. Theranostics. 2018;8(8):2251–63.
  • Chen H-S, Hsu C-Y, Chang Y-C, Chuang H-Y, Long C-Y, Hsieh T-H, Tsai E-M. Benzyl butyl phthalate decreases myogenic differentiation of endometrial mesenchymal stem/stromal cells through miR-137-mediated regulation of PITX2. Sci Rep. 2017;7(1):186.
  • Liu A-X, Yang F, Huang L, Zhang L-Y, Zhang J-R, Zheng R-N. Long non-coding RNA Tubulin Alpha 4B (TUBA4B) inhibited breast cancer proliferation and invasion by directly targeting miR-19. Eur Rev Med Pharmacol Sci. 2019;23(2):708–15.
  • Shi X, Tang X, Su L. Overexpression of long noncoding RNA PTENP1 inhibits cell proliferation and migration via suppression of miR-19b in breast cancer cells. Oncol Res. 2018;26(6):869–78.
  • Zhou J, Zhang X, Shi H, Fan C. MiR-19 regulates breast cancer cell aggressiveness by targeting profilin 1. FEBS Lett. 2017;591(11):1623.
  • Hennessy BT, Smith DL, Ram PT, Lu Y, Mills GB. Exploiting the PI3K/AKT pathway for cancer drug discovery. Nat Rev Drug Discov. 2005;4(12):988–1004.
  • Liang J, Zubovitz J, Petrocelli T, Kotchetkov R, Connor MK, Han K, Lee J-H, Ciarallo S, Catzavelos C, Beniston R, et al. PKB/Akt phosphorylates p27, impairs nuclear import of p27 and opposes p27-mediated G1 arrest. Nat Med. 2002;8(10):1153–60.
  • Li X, Xie W, Xie C, Huang C, Zhu J, Liang Z, Deng F, Zhu M, Zhu W, Wu R, et al. Curcumin modulates miR-19/PTEN/AKT/p53 axis to suppress bisphenol A-induced MCF-7 breast cancer cell proliferation. Phytother Res. 2014;28(10):1553–60.
  • Liang Z, Li Y, Huang K, Wagar N, Shim H. Regulation of miR-19 to breast cancer chemoresistance through targeting PTEN. Pharm Res. 2011;28(12):3091–100.
  • Hong L, Lai M, Chen M, Xie C, Liao R, Kang YJ, Xiao C, Hu W-Y, Han J, Sun P, et al. The miR-17-92 cluster of microRNAs confers tumorigenicity by inhibiting oncogene-induced senescence. Cancer Res. 2010;70(21):8547–57.
  • Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136(2):215–33.
  • Knauss JL, Bian S, Sun T. Plasmid-based target protectors allow specific blockade of miRNA silencing activity in mammalian developmental systems. Front Cell Neurosci. 2013;7:163.
  • Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2022. CA Cancer J Clin. 2022;72(1):7–33.
  • Chen S, Wang Z, Liu L, Li Y, Ni X, Yuan H, Wang C. Redox homeostasis modulation using theranostic AIE nanoparticles results in positive-feedback drug accumulation and enhanced drug penetration to combat drug-resistant cancer. Mater Today Bio. 2022;16:100396.
  • Rong Y, Huang L, Yi K, Chen H, Liu S, Zhang W, Yuan C, Song X, Wang F. Co-administration of sulforaphane and doxorubicin attenuates breast cancer growth by preventing the accumulation of myeloid-derived suppressor cells. Cancer Lett. 2020;493:189–96.
  • Simões BM, Santiago-Gómez A, Chiodo C, Moreira T, Conole D, Lovell S, Alferez D, Eyre R, Spence K, Sarmiento-Castro A, et al. Targeting STAT3 signaling using stabilised sulforaphane (SFX-01) inhibits endocrine resistant stem-like cells in ER-positive breast cancer. Oncogene. 2020;39(25):4896–908.
  • Bose C, Awasthi S, Sharma R, Beneš H, Hauer-Jensen M, Boerma M, Singh SP. Sulforaphane potentiates anticancer effects of doxorubicin and attenuates its cardiotoxicity in a breast cancer model. PloS One. 2018;13(3):e0193918.
  • Jabbarzadeh Kaboli P, Afzalipour Khoshkbejari M, Mohammadi M, Abiri A, Mokhtarian R, Vazifemand R, Amanollahi S, Yazdi Sani S, Li M, Zhao Y, et al. Targets and mechanisms of sulforaphane derivatives obtained from cruciferous plants with special focus on breast cancer - contradictory effects and future perspectives. Biomed Pharmacother. 2020;121:109635.
  • Lewinska A, Bednarz D, Adamczyk-Grochala J, Wnuk M. Phytochemical-induced nucleolar stress results in the inhibition of breast cancer cell proliferation. Redox Biol. 2017;12:469–82.

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