Acknowledgement
This work was supported by the Research Institute for Veterinary Science, and BK21 PLUS Program for Creative Veterinary Science Research Center, Seoul National University, and by the National Research Foundation of Korea (NRF) grant funded by the Korea government (NRF-2018R1A2B2002923). This work was also supported by a clinical research grant (NCC-1810150) provided by the National Cancer Center and by CAPES PhD fellowship and PDSE (process number: 8881.187564/2018-01) granted to Tatiana Takahasi Komoto. Histological analysis was supported by Korea Mouse Phenotyping Center (KMPC).
References
- Huszno J, Kolosza Z (2019) Molecular characteristics of breast cancer according to clinicopathological factors. Mol Clin Oncol 11:192-200. https://doi.org/10.3892/mco.2019.1869
- Harbeck N, Gnant M (2017) Breast cancer. Lancet 389:1134-1150. https://doi.org/10.1016/s0140-6736(16)31891-8
- Wenzel U, Kuntz S, Brendel MD, Daniel H (2000) Dietary flavone is a potent apoptosis inducer in human colon carcinoma cells. Cancer Res 60:3823-3831
- Komoto TT, Bernardes TM, Mesquita TB, Bortolotto LFB, Silva G, Bitencourt TA, Baek SJ, Marins M, Fachin AL (2018) Chalcones repressed the AURKA and MDR proteins involved in metastasis and multiple drug resistance in breast cancer cell lines. Molecules 23:2018. https://doi.org/10.3390/molecules23082018
- Silva G, Marins M, Chaichanasak N, Yoon Y, Fachin AL, Pinhanelli VC, Regasini LO, Dos Santos MB, Ayusso GM, Marques BC, Wu WW, Phue JN, Shen RF, Baek SJ (2018) Trans-chalcone increases p53 activity via DNAJB1/HSP40 induction and CRM1 inhibition. PLoS ONE 13:e0202263. https://doi.org/10.1371/journal.pone.0202263
- Silva G, Marins M, Fachin AL, Lee SH, Baek SJ (2016) Anti-cancer activity of trans-chalcone in osteosarcoma: involvement of Sp1 and p53. Mol Carcinog 55:1438-1448. https://doi.org/10.1002/mc.22386
- Lamoke F, Labazi M, Montemari A, Parisi G, Varano M, Bartoli M (2011) Trans-chalcone prevents VEGF expression and retinal neovascularization in the ischemic retina. Exp Eye Res 93:350-354. https://doi.org/10.1016/j.exer.2011.02.007
- Bortolotto LFB, Barbosa FR, Silva G, Bitencourt TA, Beleboni RO, Baek SJ, Marins M, Fachin AL (2017) Cytotoxicity of trans-chalcone and licochalcone A against breast cancer cells is due to apoptosis induction and cell cycle arrest. Biomed Pharmacother 85:425-433. https://doi.org/10.1016/j.biopha.2016.11.047
- Da Silva JG, Recio Despaigne AA, Louro SR, Bandeira CC, Souza-Fagundes EM, Beraldo H (2013) Cytotoxic activity, albumin and DNA binding of new copper(II) complexes with chalcone-derived thiosemicarbazones. Eur J Med Chem 65:415-426. https://doi.org/10.1016/j.ejmech.2013.04.036
- Nitti M, Piras S, Marinari UM, Moretta L, Pronzato MA, Furfaro AL (2017) HO-1 induction in cancer progression: a matter of cell adaptation. Antioxidants (Basel). https://doi.org/10.3390/antiox6020029
- Gandini NA, Alonso EN, Fermento ME, Mascaro M, Abba MC, Colo GP, Arevalo J, Ferronato MJ, Guevara JA, Nunez M, Pichel P, Curino AC, Facchinetti MM (2019) Heme oxygenase-1 has an antitumor role in breast cancer. Antioxid Redox Signal 30:2030-2049. https://doi.org/10.1089/ars.2018.7554
- Zou C, Zou C, Cheng W, Li Q, Han Z, Wang X, Jin J, Zou J, Liu Z, Zhou Z, Zhao W, Du Z (2016) Heme oxygenase-1 retards hepatocellular carcinoma progression through the microRNA pathway. Oncol Rep 36:2715-2722. https://doi.org/10.3892/or.2016.5056
- Lin CW, Shen SC, Hou WC, Yang LY, Chen YC (2008) Heme oxygenase-1 inhibits breast cancer invasion via suppressing the expression of matrix metalloproteinase-9. Mol Cancer Ther 7:1195-1206. https://doi.org/10.1158/1535-7163.Mct-07-2199
- Andres NC, Fermento ME, Gandini NA, Romero AL, Ferro A, Donna LG, Curino AC, Facchinetti MM (2014) Heme oxygenase-1 has antitumoral effects in colorectal cancer: Involvement of p53. Exp Mol Pathol 97:321-331. https://doi.org/10.1016/j.yexmp.2014.09.012
- Lee HN, Jin HO, Park JA, Kim JH, Kim JY, Kim B, Kim W, Hong SE, Lee YH, Chang YH, Hong SI, Hong YJ, Park IC, Surh YJ, Lee JK (2015) Heme oxygenase-1 determines the differential response of breast cancer and normal cells to piperlongumine. Mol Cells 38:327-335. https://doi.org/10.14348/molcells.2015.2235
- Hill M, Pereira V, Chauveau C, Zagani R, Remy S, Tesson L, Mazal D, Ubillos L, Brion R, Asghar K, Mashreghi MF, Kotsch K, Moffett J, Doebis C, Seifert M, Boczkowski J, Osinaga E, Anegon I (2005) Heme oxygenase-1 inhibits rat and human breast cancer cell proliferation: mutual cross inhibition with indoleamine 2,3-dioxygenase. FASEB J 19:1957-1968. https://doi.org/10.1096/fj.05-3875com
- Caballero F, Meiss R, Gimenez A, Batlle A, Vazquez E (2004) Immunohistochemical analysis of heme oxygenase-1 in preneoplastic and neoplastic lesions during chemical hepatocarcinogenesis. Int J Exp Pathol 85:213-222. https://doi.org/10.1111/j.0959-9673.2004.00391.x
- Paez AV, Pallavicini C, Schuster F, Valacco MP, Giudice J, Ortiz EG, Anselmino N, Labanca E, Binaghi M, Salierno M, Marti MA, Cotignola JH, Woloszynska-Read A, Bruno L, Levi V, Navone N, Vazquez ES, Gueron G (2016) Heme oxygenase-1 in the forefront of a multi-molecular network that governs cell-cell contacts and filopodia-induced zippering in prostate cancer. Cell Death Dis 7:e2570. https://doi.org/10.1038/cddis.2016.420
- Crowe AR, Yue W (2019) Semi-quantitative determination of protein expression using immunohistochemistry staining and analysis: an integrated protocol. Bio-protocol. https://doi.org/10.21769/BioProtoc.3465
- Nishi H, Shaytan A, Panchenko AR (2014) Physicochemical mechanisms of protein regulation by phosphorylation. Front Genet. https://doi.org/10.3389/fgene.2014.00270
- Siegel RL, Miller KD, Jemal A (2019) Cancer statistics. CA Cancer J Clin 69:7-34. https://doi.org/10.3322/caac.21551
- Komoto TT, Bernardes TM, Mesquita TB, Bortolotto LFB, Silva G, Bitencourt TA, Baek SJ, Marins M, Fachin AL (2018) Chalcones repressed the AURKA and MDR proteins involved in metastasis and multiple drug resistance in breast cancer cell lines. Molecules. https://doi.org/10.3390/molecules23082018
- Lima DC, Vale CR, Veras JH, Bernardes A, Perez CN, Chen-Chen L (2017) Absence of genotoxic effects of the chalcone (E)-1-(2-hydroxyphenyl)-3-(4-methylphenyl)-prop-2-en-1-one) and its potential chemoprevention against DNA damage using in vitro and in vivo assays. PLoS ONE 12:e0171224. https://doi.org/10.1371/journal.pone.0171224
- Tsai CF, Chen JH, Chang CN, Lu DY, Chang PC, Wang SL, Yeh WL (2018) Fisetin inhibits cell migration via inducing HO-1 and reducing MMPs expression in breast cancer cell lines. Food Chem Toxicol 120:528-535. https://doi.org/10.1016/j.fct.2018.07.059
- Chiang SK, Chen SE, Chang LC (2018) A dual role of heme oxygenase-1 in cancer cells. Int J Mol Sci. https://doi.org/10.3390/ijms20010039
- Was H, Cichon T, Smolarczyk R, Rudnicka D, Stopa M, Chevalier C, Leger JJ, Lackowska B, Grochot A, Bojkowska K, Ratajska A, Kieda C, Szala S, Dulak J, Jozkowicz A (2006) Overexpression of heme oxygenase-1 in murine melanoma: increased proliferation and viability of tumor cells, decreased survival of mice. Am J Pathol 169:2181-2198. https://doi.org/10.2353/ajpath.2006.051365
- Keum Y-S, Yu S, Chang PP-J, Yuan X, Kim J-H, Xu C, Han J, Agarwal A, Kong A-NT (2006) Mechanism of action of sulforaphane: inhibition of p38 mitogen-activated protein kinase isoforms contributing to the induction of antioxidant response element-mediated heme oxygenase-1 in human hepatoma HepG2 cells. Can Res 66:8804-8813. https://doi.org/10.1158/0008-5472.Can-05-3513
- Loboda A, Damulewicz M, Pyza E, Jozkowicz A, Dulak J (2016) Role of Nrf2/HO-1 system in development, oxidative stress response and diseases: an evolutionarily conserved mechanism. Cell Mol Life Sci 73:3221-3247. https://doi.org/10.1007/s00018-016-2223-0
- Zhang DD, Lo SC, Cross JV, Templeton DJ, Hannink M (2004) Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex. Mol Cell Biol 24:10941-10953. https://doi.org/10.1128/MCB.24.24.10941-10953.2004
- Li Q, Liu Q, Cheng W, Wei H, Jiang Fang WE, Yu Y, Jin J, Zou C (2019) Heme oxygenase-1 inhibits tumor metastasis mediated by notch1 pathway in murine mammary carcinoma. Oncol Res 27:643-651. https://doi.org/10.3727/096504018X15415906335771