The transcription factor HBP1 promotes ferroptosis in tumor cells by regulating the UHRF1-CDO1 axis

The induction of ferroptosis in tumor cells is one of the most important mechanisms by which tumor progression can be inhibited; however, the specific regulatory mechanism underlying ferroptosis remains unclear. In this study, we found that transcription factor HBP1 has a novel function of reducing the antioxidant capacity of tumor cells. We investigated the important role of HBP1 in ferroptosis. HBP1 down-regulates the protein levels of UHRF1 by inhibiting the expression of the UHRF1 gene at the transcriptional level. Reduced levels of UHRF1 have been shown to regulate the ferroptosis-related gene CDO1 by epigenetic mechanisms, thus up-regulating the level of CDO1 and increasing the sensitivity of hepatocellular carcinoma and cervical cancer cells to ferroptosis. On this basis, we constructed metal-polyphenol-network coated HBP1 nanoparticles by combining biological and nanotechnological. MPN-HBP1 nanoparticles entered tumor cells efficiently and innocuously, induced ferroptosis, and inhibited the malignant proliferation of tumors by regulating the HBP1-UHRF1-CDO1 axis. This study provides a new perspective for further research on the regulatory mechanism underlying ferroptosis and its potential role in tumor therapy.

[1]  Jing Wang,et al.  Discovery of a Potent Glutathione Peroxidase 4 Inhibitor as a Selective Ferroptosis Inducer. , 2021, Journal of medicinal chemistry.

[2]  Yixian Zhou,et al.  Application of glutathione depletion in cancer therapy: Enhanced ROS-based therapy, ferroptosis, and chemotherapy. , 2021, Biomaterials.

[3]  Yanli Yan,et al.  Silencing UHRF1 Enhances Radiosensitivity of Esophageal Squamous Cell Carcinoma by Inhibiting the PI3K/Akt/mTOR Signaling Pathway , 2021, Cancer management and research.

[4]  Cuijun Deng,et al.  The potential application of nanomaterials for ferroptosis-based cancer therapy , 2021, Biomedical materials.

[5]  Yujuan Liu,et al.  HBP1-mediated transcriptional repression of AFP inhibits hepatoma progression , 2021, Journal of experimental & clinical cancer research : CR.

[6]  C. Thompson,et al.  Oncogenic activation of PI3K-AKT-mTOR signaling suppresses ferroptosis via SREBP-mediated lipogenesis , 2020, Proceedings of the National Academy of Sciences.

[7]  D. Klionsky,et al.  Ferroptosis: machinery and regulation , 2020, Autophagy.

[8]  Shouping Xu,et al.  Inhibition of tumor propellant glutathione peroxidase 4 induces ferroptosis in cancer cells and enhances anticancer effect of cisplatin , 2020, Journal of cellular physiology.

[9]  Haitao Zhu,et al.  Branched-chain amino acid aminotransferase 2 regulates ferroptotic cell death in cancer cells , 2020, Cell Death & Differentiation.

[10]  T. Vanden Berghe,et al.  Targeting Ferroptosis to Iron Out Cancer. , 2019, Cancer cell.

[11]  Z. Dai,et al.  Photothermal therapy and photoacoustic imaging via nanotheranostics in fighting cancer. , 2019, Chemical Society reviews.

[12]  J. Asara,et al.  Cysteine dioxygenase 1 is a metabolic liability for non-small cell lung cancer , 2018, bioRxiv.

[13]  Xiaoyuan Chen,et al.  Fenton-Reaction-Acceleratable Magnetic Nanoparticles for Ferroptosis Therapy of Orthotopic Brain Tumors. , 2018, ACS nano.

[14]  Chang-qing Yang,et al.  UHRF1 mediates cell migration and invasion of gastric cancer , 2018, Bioscience reports.

[15]  Wei Li,et al.  BAP1 links metabolic regulation of ferroptosis to tumor suppression , 2018, Nature Cell Biology.

[16]  Juyoung Yoon,et al.  Supramolecular photosensitizers rejuvenate photodynamic therapy. , 2018, Chemical Society reviews.

[17]  Qiaojun He,et al.  The Role of Ferroptosis in Cancer Development and Treatment Response , 2018, Front. Pharmacol..

[18]  J. Yu,et al.  Cysteine Dioxygenase 1 Mediates Erastin-Induced Ferroptosis in Human Gastric Cancer Cells1 , 2017, Neoplasia.

[19]  B. Stockwell,et al.  Ferroptosis: A Regulated Cell Death Nexus Linking Metabolism, Redox Biology, and Disease , 2017, Cell.

[20]  Wei Jiang,et al.  A positive feedback loop between Pim-1 kinase and HBP1 transcription factor contributes to hydrogen peroxide-induced premature senescence and apoptosis , 2017, Journal of Biological Chemistry.

[21]  Xufeng Chen,et al.  Uhrf1 controls the self-renewal versus differentiation of hematopoietic stem cells by epigenetically regulating the cell-division modes , 2016, Proceedings of the National Academy of Sciences.

[22]  K. Yamashita,et al.  Promoter DNA methylation of CDO1 gene and its clinical significance in esophageal squamous cell carcinoma. , 2016, Diseases of the esophagus : official journal of the International Society for Diseases of the Esophagus.

[23]  Yifan Chen,et al.  HBP1-mediated Regulation of p21 Protein through the Mdm2/p53 and TCF4/EZH2 Pathways and Its Impact on Cell Senescence and Tumorigenesis , 2016, The Journal of Biological Chemistry.

[24]  Shu Yang,et al.  UHRF1 overexpression is involved in cell proliferation and biochemical recurrence in prostate cancer after radical prostatectomy , 2016, Journal of experimental & clinical cancer research : CR.

[25]  W. Greenhalf,et al.  UHRF1 regulation of the Keap1–Nrf2 pathway in pancreatic cancer contributes to oncogenesis , 2015, The Journal of pathology.

[26]  Xian‐Zheng Zhang,et al.  A multifunctional metal-organic framework based tumor targeting drug delivery system for cancer therapy. , 2015, Nanoscale.

[27]  Ji-Hee Kim,et al.  Epigenetic regulation of the novel tumor suppressor cysteine dioxygenase 1 in esophageal squamous cell carcinoma , 2015, Tumor Biology.

[28]  M. Conrad,et al.  Glutathione peroxidase 4 (Gpx4) and ferroptosis: what's so special about it? , 2015, Molecular & cellular oncology.

[29]  Yiran Huang,et al.  Epigenetic repression of regulator of G‐protein signaling 2 by ubiquitin‐like with PHD and ring‐finger domain 1 promotes bladder cancer progression , 2015, The FEBS journal.

[30]  B. Chauffert,et al.  Iron‐dependent cell death of hepatocellular carcinoma cells exposed to sorafenib , 2013, International journal of cancer.

[31]  Jiwei Cui,et al.  One-Step Assembly of Coordination Complexes for Versatile Film and Particle Engineering , 2013, Science.

[32]  J. Herman,et al.  Frequent Inactivation of Cysteine Dioxygenase Type 1 Contributes to Survival of Breast Cancer Cells and Resistance to Anthracyclines , 2013, Clinical Cancer Research.

[33]  J. Wong,et al.  UHRF1 targets DNMT1 for DNA methylation through cooperative binding of hemi-methylated DNA and methylated H3K9 , 2013, Nature Communications.

[34]  H. Ju,et al.  Diagnostic and prognostic value of plasma and tissue ubiquitin‐like, containing PHD and RING finger domains 1 in breast cancer patients , 2013, Cancer science.

[35]  A. Yee,et al.  HBP1-Mediated Transcriptional Regulation of DNA Methyltransferase 1 and Its Impact on Cell Senescence , 2012, Molecular and Cellular Biology.

[36]  M. Shirakawa,et al.  Recognition of modification status on a histone H3 tail by linked histone reader modules of the epigenetic regulator UHRF1 , 2012, Proceedings of the National Academy of Sciences.

[37]  Juna Lee,et al.  Cysteine Dioxygenase 1 Is a Tumor Suppressor Gene Silenced by Promoter Methylation in Multiple Human Cancers , 2012, PloS one.

[38]  A. Yee,et al.  Transcriptional factor HBP1 targets P16INK4A, upregulating its expression and consequently is involved in Ras-induced premature senescence , 2010, Oncogene.

[39]  Peter Fratzl,et al.  Iron-Clad Fibers: A Metal-Based Biological Strategy for Hard Flexible Coatings , 2010, Science.

[40]  Colin J. Daniel,et al.  The Tumor Suppressor Protein HBP1 Is a Novel c-Myc-binding Protein That Negatively Regulates c-Myc Transcriptional Activity* , 2009, The Journal of Biological Chemistry.

[41]  J. Dominy,et al.  Cysteine dioxygenase: a robust system for regulation of cellular cysteine levels , 2009, Amino Acids.

[42]  K. Mitsuya,et al.  The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA , 2007, Nature.

[43]  S. Jacobsen,et al.  UHRF1 Plays a Role in Maintaining DNA Methylation in Mammalian Cells , 2007, Science.

[44]  M. Maroney,et al.  Cysteine dioxygenase: structure and mechanism. , 2007, Chemical communications.

[45]  M. McDevitt,et al.  The HBP1 Transcriptional Repressor Participates in RAS-Induced Premature Senescence , 2006, Molecular and Cellular Biology.

[46]  K. Eric Paulson,et al.  HBP1 Repression of the p47phox Gene: Cell Cycle Regulation via the NADPH Oxidase , 2004, Molecular and Cellular Biology.

[47]  G. Austin,et al.  Cloning and expression of human HBP1, a high mobility group protein that enhances myeloperoxidase (MPO) promoter activity , 2001, Leukemia.

[48]  Hui Zhang,et al.  Involvement of Retinoblastoma Protein and HBP1 in Histone H10 Gene Expression , 2000, Molecular and Cellular Biology.

[49]  A. Gartel,et al.  Activation and repression of p21WAF1/CIP1 transcription by RB binding proteins , 1998, Oncogene.