Indole-3-carbinol as a radiosensitizer and modulator of IR-dependent stemness in triple-negative breast cancer

References

• Jayachandran P, Battaglin F, Strelez C, et al. Breast cancer and neurotransmitters: emerging insights on mechanisms and therapeutic directions. Oncogene. 2023;42(9):627–637. doi: 10.1038/s41388-022-02584-4
   PubMed Web of Science ®Google Scholar
• Pruneri G, Lorenzini D, Mastropasqua MG, et al. The central role of pathology labs in breast cancer precision oncology: a call for action. NPJ Breast Cancer. 2023;9(1):3. doi: 10.1038/s41523-023-00506-5
   PubMed Web of Science ®Google Scholar
• To NH, Nguyen HQ, Thiolat A, et al. On behalf of the TransAtlantic Radiation Oncology Network (TRONE) & Association of Radiotherapy, and Oncology of the Mediterranean Area (AROME), radiation therapy for triple-negative breast cancer: emerging role of microRnas as biomarkers and radiosensitivity modifiers. A systematic review. Breast Cancer Res Treat. 2022;193(2):265–279. doi: 10.1007/s10549-022-06533-3
   PubMedGoogle Scholar
• Wang Y, Liu F, Sun L, et al. Association between human blood metabolome and the risk of breast cancer. Breast Cancer Res. 2023;25(1):9. doi: 10.1186/s13058-023-01609-4
   PubMed Web of Science ®Google Scholar
• He Y, Chen S, Gao X, et al. Robustness of VMAT to setup errors in postmastectomy radiotherapy of left-sided breast cancer: Impact of bolus thickness. PLOS ONE. 2023;18(1):e0280456. doi: 10.1371/journal.pone.0280456
   PubMed Web of Science ®Google Scholar
• Sjostrom M, Fyles A, Liu F-F, et al. Development and validation of a genomic profile for the omission of local adjuvant radiation in breast cancer. J Clin Oncol. 2023;41(8):1533–1540. doi: 10.1200/JCO.22.00655
   PubMed Web of Science ®Google Scholar
• Bronzatti E, Siqueira LO. Radiotherapy for breast cancer. Springer Nature Switzerland AG 2019 467, G. Novita et al. (eds.). Breast Dis. 2019. doi: 10.1007/978-3-030-13636-9_57
   Google Scholar
• Bensadoun R-J, Nair R. Principles and practice of radiation oncology and modern radiation therapy techniques. In: Nair R, editor. Orofacial supportive care in cancer. Springer Nature Switzerland AG; 2022. doi: 10.1007/978-3-030-86510-8_4
   Google Scholar
• Lee V-F, Lee A-M. Principle of cancer radiotherapy. In: Seong J, editor. Radiotherapy of liver cancer. Springer Nature Singapore Pte Ltd; 2021. doi: 10.1007/978-981-16-1815-4_1
   Google Scholar
• Nosrati H, Salehiabar M, Charmi J, et al. Enhanced in vivo radiotherapy of breast cancer using gadolinium oxide and gold hybrid nanoparticles. Appl Biomater. 2023;6(2):784–792. doi: 10.1021/acsabm.2c00965
   Google Scholar
• Loenhout VJ, Peeters M, Bogaerts A, et al. Oxidative stress-inducing anticancer therapies: taking a closer look at their immunomodulating effects. Antioxidants. 2020;9(12):1188. doi: 10.3390/antiox9121188
   Web of Science ®Google Scholar
• Mileo AM, Miccadei S. Polyphenols as modulator of oxidative stress in cancer disease: new therapeutic strategies, oxid. Med Cell Longev. 2016;2016:1–17. doi: 10.1155/2016/6475624
   Web of Science ®Google Scholar
• Li F, Zhou K, Gao L, et al. Radiation induces the generation of cancer stem cells: a novel mechanism for cancer radioresistance. Oncol Lett. 2016;12(5):3059–3065. doi: 10.3892/ol.2016.5124. PMCID: PMC5103903.
   PubMed Web of Science ®Google Scholar
• Zhou S, Zhang M, Zhou C, et al. The role of epithelial-mesenchymal transition in regulating radioresistance. Crit Rev Oncol Hematol. 2020;150:102961. doi: 10.1016/j.critrevonc.2020.102961
   PubMed Web of Science ®Google Scholar
• Yang HJ, Youn H, Seong KM, et al. Phosphorylation of ribosomal protein S3 and antiapoptotic TRAF2 protein mediates radioresistance in non-small cell lung cancer cells. J Biol Chem. 2013;288(5):2965–2975. doi: 10.1074/jbc.M112.385989
   PubMed Web of Science ®Google Scholar
• Wu Y, Song Y, Wang R, et al. Molecular mechanisms of tumor resistance to radiotherapy. Mol Cancer. 2023 15;22(1):96. doi: 10.1186/s12943-023-01801-2. PMID: 37322433; PMCID: PMC10268375.
   PubMed Web of Science ®Google Scholar
• Choudhari AS, Mandave PC, Deshpande M, et al. Phytochemicals in cancer treatment: from preclinical studies to clinical practice. Front Pharmacol. 2019;10:1614. doi: 10.3389/fphar.2019.01614
   PubMed Web of Science ®Google Scholar
• Prakash D, Gupta C. Therapeutic implications of phytochemicals in ROS induced cancer. In: Chakraborti S, editor. Handbook of oxidative stress in cancer: therapeutic aspects. Springer Nature Singapore Pte Ltd; 2022. doi: 10.1007/978-981-16-1247-3_14-1
   Google Scholar
• Abdraboh ME, Essa ZS, Abdelrazzak AB, et al. Radio-sensitizing effect of a cocktail of phytochemicals on HepG2 cell proliferation, motility and survival. Biomed Pharmacother. 2020;131:110620. doi: 10.1016/j.biopha.2020.110620
   PubMed Web of Science ®Google Scholar
• Wang T, Zhang D, Yang B, et al. Salicylic acid regulates indole-3-carbinol biosynthesis under blue light in broccoli sprouts (Brassica oleracea L.). Front Plant Sci. 2022;13:848454. doi: 10.3389/fpls.2022.848454
   PubMed Web of Science ®Google Scholar
• Wang X, Zhang L, Dai Q, et al. Combined luteolin and indole-3-carbinol synergistically constrains ERα-positive breast cancer by dual inhibiting estrogen receptor alpha and cyclin-dependent kinase 4/6 pathway in cultured cells and xenograft mice. Cancers (Basel). 2021;13(9):2116. doi: 10.3390/cancers13092116
   PubMed Web of Science ®Google Scholar
• Qi Y, Zhang C, Wu D, et al. Indole-3-carbinol stabilizes p53 to induce miR-34a, which targets LDHA to block aerobic glycolysis in liver cancer cells. Pharmaceuticals. 2022;15(10):1257. doi: 10.3390/ph15101257
   Web of Science ®Google Scholar
• Martín-Ruiz A, Peña L, González-Gil A, et al. Effects of indole-3-carbinol on steroid hormone profile and tumor progression in a mice model of canine inflammatory mammary cancer. BMC Cancer. 2018;18(1). doi: 10.1186/s12885-018-4518-z
   PubMedGoogle Scholar
• Odongo R, Demiroglu-Zergeroglu A, Çakır T. A systems pharmacology approach based on oncogenic signalling pathways to determine the mechanisms of action of natural products in breast cancer from transcriptome data. BMC Complement Med Ther. 2021;21(1):181. doi: 10.1186/s12906-021-03340-z
   PubMedGoogle Scholar
• Poloznikova AA, Muyzhnekb EL, Nikulinc SV, et al. Antitumor activity of indole-3-carbinol in breast cancer cells: phenotype, genetic pattern, and DNA methylation inversion. Appl Biochem Microbiol. 2020;56(9):909–919. ISSN 0003-6838. doi: 10.1134/S0003683820090070
   Web of Science ®Google Scholar
• Wilsher NE, Arroo RR, Matsoukas MT, et al. Cytochrome p450 cyp1 metabolism of hydroxylated flavones and flavonols: selective bioactivation of luteolin in breast cancer cells. Food And Chemical Toxicology. 2017;110:383–394. doi: 10.1016/j.fct.2017.10.051
   PubMed Web of Science ®Google Scholar
• Abdraboh ME, Essa ZS, Abdelrazzak AB. Radio-sensitizing effect of a cocktail of phytochemicals on HepG2 cell proliferation, motility and survival. Biomed Pharmacother. 2020;131:110620. doi: 10.1016/j.biopha.2020.110620
   PubMed Web of Science ®Google Scholar
• Pandya V, Githaka JM, Patel N, et al. BIK drives an aggressive breast cancer phenotype through sublethal apoptosis and predicts poor prognosis of ER-positive breast cancer. Cell Death Dis. 2020;11(6):448. doi: 10.1038/s41419-020-2654-2
   PubMed Web of Science ®Google Scholar
• Golestani BE, Sanati MH, Houshmand M, et al. Expression and prognostic significance of bcl-2 and bax in the progression and clinical outcome of transitional bladder cell carcinoma. Cell J. 2014;15(4):356–363.
   PubMed Web of Science ®Google Scholar
• Kotecha R, Takami A, Espinoza JL. Dietary phytochemicals and cancer chemoprevention: a review of the clinical evidence. Oncotarget. 2016;7(32):52517. doi: 10.18632/oncotarget.9593
   PubMedGoogle Scholar
• Nisar S, Masoodi T, Prabhu KS, et al. Natural products as chemo-radiation therapy sensitizers in cancers. Biomedicine & Pharmacotherapy. 2022;154:113610. doi: 10.1016/j.biopha.2022.113610
   PubMed Web of Science ®Google Scholar
• Davey GM, Hynes SO, Kerin MJ, et al. Ki-67 as a prognostic biomarker in invasive breast cancer. Cancers (Basel). 2021 3;13(17):4455. doi: 10.3390/cancers13174455
   PubMed Web of Science ®Google Scholar
• Ma B, Huang X-T, Zou G-J, et al. Relationship between Ki-67 and CD44 expression and microvascular formation in gastric stromal tumor tissues. World J Clin Cases. 2022 14;10(2):469–476. doi: 10.12998/wjcc.v10.i2.469
   PubMed Web of Science ®Google Scholar
• Huang P, He Y, Cao J, et al. Up-regulated Nrf2 in colorectal carcinoma and predicts poor prognosis. Int J Clin Exp Med. 2017;10(1):1034–1042. Available from: www.ijcem.com/ISSN:1940-5901/IJCEM0039190
   Web of Science ®Google Scholar
• Hajra S, Patra AR, Basu A, et al. Indole-3-carbinol (I3C) enhances the sensitivity of murine breast adenocarcinoma cells to doxorubicin (DOX) through inhibition of NF-κβ, blocking angiogenesis and regulation of mitochondrial apoptotic pathway. Chem Biol Inter. 2018;290:19–36. doi: 10.1016/j.cbi.2018.05.005
   PubMed Web of Science ®Google Scholar
• Singh-Gupta V, Banerjee S, Yunker CK, et al. B-DIM impairs radiation-induced survival pathways independently of androgen receptor expression and augments radiation efficacy in prostate cancer. Cancer Lett. 2012;318(1):86–92. Elsevier Ireland Ltd. doi: 10.1016/j.canlet.2011.12.006
   PubMed Web of Science ®Google Scholar
• Zamanian A, Changizi V, Nedaie H, et al. Combination treatment of glioblastoma by low-dose radiation and genistein. Curr Radiopharm. 2016;9(3):258–263. doi: 10.2174/1874471009666160813232031
   PubMedGoogle Scholar
• Singh AA, Jo S-H, Kiddane AT, et al. Indole-3-carbinol induces apoptosis in AGS cancer cells via mitochondrial pathway. Chem Biol Drug Des. 2023;101(6):1367–1381. doi: 10.1111/cbdd.14219
   PubMed Web of Science ®Google Scholar
• Xu X-L, Deng S-L, Lian Z-X, et al. Resveratrol targets a variety of oncogenic and oncosuppressive signaling for ovarian cancer prevention and treatment. Antioxidants. 2021;10(11):1718. doi: 10.3390/antiox10111718
   Web of Science ®Google Scholar
• Abdraboh ME, Gaur RL, Hollenbach AD, et al. Survivin is a novel target of CD44-promoted breast tumor invasion. Am J Pathol. 2011 Aug;179(2):555–563. doi: 10.1016/j.ajpath.2011.04.042
   PubMed Web of Science ®Google Scholar
• Zhao Y, Kang J-H, Yoo K-C, et al. K-RAS acts as a critical regulator of CD44 to promote the invasiveness and stemness of GBM in response to ionizing radiation. Int J Mol Sci. 2021;22(20):10923. doi: 10.3390/ijms222010923
   PubMed Web of Science ®Google Scholar
• Lin S, Shen Z, Yang Y, et al. Expression profiles of radio-resistant genes in colorectal cancer cells. Radiat Med Prot. 2021;2(2):48–54. doi: 10.1016/j.radmp.2021.04.006
   Google Scholar
• Ouhtit A, Abdraboh ME, Hollenbach AD, et al. CD146, a novel target of CD44-signaling, suppresses breast tumor cell invasion. Cell Commun Signaling. 2017;15(1):45. doi: 10.1186/s12964-017-0200-3
   PubMedGoogle Scholar
• Abd Elhakeem AA, Essa AA, Soliman RK, et al. Novel evaluation of the expression patterns CD44 and MMP9 proteins in intracranial meningiomas and their relationship to the overall survival. Egypt J Neurosurg. 2022;37(1):33. doi: 10.1186/s41984-022-00173-x
   Google Scholar
• Desai B, Ma T, Zhu J, et al. Characterization of the expression of variant and standard CD44 in prostate cancer cells: identification of the possible molecular mechanism of CD44/MMP9 complex formation on the cell surface. J Cell Biochem. 2009;108(1):272–284. doi: 10.1002/jcb.22248
   PubMed Web of Science ®Google Scholar
• Gupta A, Cao W, Sadashivaiah K, et al. Promising noninvasive cellular phenotype in prostate cancer cells knockdown of matrix metalloproteinase 9. Sci World J. 2013;2013:1–13. doi: 10.1155/2013/493689
   Google Scholar
• Ludwig N, Szczepanski MJ, Gluszko A, et al. CD44(+) tumor cells promote early angiogenesis in head and neck squamous cell carcinoma. Cancer Lett. 2019;28(467):85–95. doi: 10.1016/j.canlet.2019.10.010
   Google Scholar
• Kumar H, Kumar RM, Bhattacharjee D, et al. Role of Nrf2 signaling cascade in breast cancer: strategies and treatment. Front Pharmacol. 2022;29(13):720076. doi: 10.3389/fphar.2022.720076
   Google Scholar
• McDonald JT, Kim K, Norris AJ, et al. Ionizing radiation activates the Nrf2 antioxidant response. Cancer Res. 2010 1;70(2):8886–8895. doi: 10.1158/0008-5472.CAN-10-0171
   PubMedGoogle Scholar
• Faraonio R, Vergar P, Di Marzo D, et al. p53 suppresses the Nrf2-dependent transcription of antioxidant response genes. J Biol Chem. 2006;281(52):39776–39784. doi: 10.1074/jbc.M605707200
   PubMed Web of Science ®Google Scholar
• Gao Y, Wan L, Li M, et al. NRF2/HO-1 axis, BIRC5, and TP53 expression in ESCC and its correlation with clinical pathological characteristics and prognosis. Int J Biol Markers. 2023;38(3–4):174–184. doi: 10.1177/03936155231176571
   PubMed Web of Science ®Google Scholar
• Choi B-H, Ryoo I, Sim KH, Ahn H-J, Lee YJ, and Kwak M-K. High levels of hyaluronic acid synthase-2 mediate NRF2-driven chemoresistance in breast cancer cells. Biomol Ther. 2022;30(4):368–379. doi: 10.4062/biomolther.2022.074
   PubMed Web of Science ®Google Scholar
• Praharaj PP, Singh A, Patra S, et al. Co-targeting autophagy and NRF2 signaling triggers mitochondrial superoxide to sensitize oral cancer stem cells for cisplatin-induced apoptosis. Free Radic Biol Med. 2023;207:72–88. doi: 10.1016/j.freeradbiomed.2023.07.008
   PubMed Web of Science ®Google Scholar
• Qiao L, Chen Y, Liang N, et al. Targeting epithelial-to-mesenchymal transition in radioresistance: crosslinked mechanisms and strategies. Front Oncol. 2022;16(12):775238. doi: 10.3389/fonc.2022.775238
   Google Scholar
• Xu H, Tian Y, Yuan X, et al. The role of CD44 in epithelial–mesenchymal transition and cancer development. Onco Targets Ther. 2015;16(8):3783–3792. doi: 10.2147/OTT.S95470
   Google Scholar
• Saito S, Okabe H, Watanabe M, et al. CD44v6 expression is related to mesenchymal phenotype and poor prognosis in patients with colorectal cancer. Oncol Rep. 2013;29(4):1570–1578. doi: 10.3892/or.2013.2273
   PubMed Web of Science ®Google Scholar
• Frascogna C, Mottareale R, La Verde G, et al. Role of the mechanical microenvironment on CD-44 expression of breast adenocarcinoma in response to radiotherapy. Sci Rep. 2024 3;14(1):391. doi: 10.1038/s41598-023-50473-x
   PubMed Web of Science ®Google Scholar
• Mesrati MH, Syafruddin SE, Mohtar MA, et al. CD44: a multifunctional mediator of cancer progression. Biomolecules. 2021 9;11(12):1850. doi: 10.3390/biom11121850
   PubMed Web of Science ®Google Scholar
• Hu C, Li M, Guo T, et al. Anti-metastasis activity of curcumin against breast cancer via the inhibition of stem cell-like properties and EMT. Phytomedicine. 2019;58:152740. doi: 10.1016/j.phymed.2018.11.001
   PubMed Web of Science ®Google Scholar
• Loh C-Y, Chai JY, Tang TF, et al. The E-Cadherin and N-Cadherin switch in epithelial-to-mesenchymal transition: signaling, therapeutic implications, and challenges. Cells. 2019;8(10):1118. doi: 10.3390/cells8101118
   PubMed Web of Science ®Google Scholar
• Das U, Kundu J, Shaw P, et al. Self-transfecting GMO-PMO chimera targeting Nanog enable gene silencing in vitro and suppresses tumor growth in 4T1 allografts in mouse. Mol Ther Nucl Acids. 2023;32. doi: 10.1016/j.omtn.2023.03.011
   Google Scholar
• Peng G, Tang Z, Xiang Y, et al. Glutathione peroxidase 4 maintains a stemness phenotype, oxidative homeostasis and regulates biological processes in Panc‑1 cancer stem‑like cells. Oncol Rep. 2019;41:1264–1274. doi: 10.3892/or.2018.6905
   PubMed Web of Science ®Google Scholar