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Co-vulnerabilities of inhibiting carbonic anhydrase IX in ferroptosis-mediated tumor cell death

FRONTIERS IN MOLECULAR BIOSCIENCES (2023)

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Carbonic Anhydrase IX Controls Vulnerability to Ferroptosis in Gefitinib-Resistant Lung Cancer

Chen Zhang et al.

Oxidative Medicine and Cellular Longevity (2023)

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Article Biochemistry & Molecular Biology

Carbonic Anhydrase IX Suppression Shifts Partial Response to Checkpoint Inhibitors into Complete Tumor Eradication: Model-Based Investigation

Julia Grajek et al.

Summary: Immune checkpoint inhibitors (ICIs) have revolutionized the treatment of solid malignancies, including non-small-cell lung cancer. However, immunotherapy resistance remains a challenge. This study investigates the role of carbonic anhydrase IX (CAIX) in resistance and suggests that combination therapy with a CAIX inhibitor and ICIs can shift the tumor's behavior from stable disease to eradication, especially when there is a sufficient immune infiltrate.

INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES (2023)

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Article Oncology

A Carbonic Anhydrase IX/SLC1A5 Axis Regulates Glutamine Metabolism Dependent Ferroptosis in Hypoxic Tumor Cells

Geetha Venkateswaran et al.

Summary: In this study, researchers discovered that Carbonic anhydrase IX (CAIX) interacts with the glutamine (Gln) transporter, solute carrier family 1 member 5 (SLC1A5), to maintain redox homeostasis in tumor cells. Inhibiting CAIX increases Gln uptake by SLC1A5, leading to an increase in glutathione (GSH) levels. Blocking CAIX activity and Gln metabolism or the GSH/GPX4 pathway results in lipid peroxidation and induces ferroptosis in both in vitro and in vivo models. This study suggests that cotargeting CAIX and Gln metabolism could be a potential strategy to induce ferroptosis in tumor cells.

MOLECULAR CANCER THERAPEUTICS (2023)

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Article Biology

CA9 knockdown enhanced ionizing radiation-induced ferroptosis and radiosensitivity of hypoxic glioma cells

Wenpeng Huang et al.

Summary: The study aimed to investigate whether ionizing radiation could induce ferroptosis in glioma cells and whether CA9 knockdown could enhance the killing effect of ionizing radiation on hypoxic glioma cells through ferroptosis. The results showed that X-ray could induce lipid peroxidation and ferroptosis markers expression in U251 and GL261 glioma cells. Knockdown of CA9 significantly altered the expression of iron regulation-related proteins and enhanced X-ray-induced ferroptosis and radiosensitivity in hypoxic glioma cells. Enhancing ferroptosis in glioma cells could promote the efficacy of radiotherapy for glioma.

INTERNATIONAL JOURNAL OF RADIATION BIOLOGY (2023)

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Article Oncology

The CAIX inhibitor SLC-0111 exerts anti-cancer activity on gastric cancer cell lines and resensitizes resistant cells to 5-Fluorouracil, taxane-derived, and platinum-based drugs

Elena Andreucci et al.

Summary: Gastric cancer is a common malignancy with high mortality rates, mainly due to the development of chemoresistance. Carbonic anhydrase IX (CAIX) has been identified as a potential biomarker associated with poor prognosis in various solid cancers. In this study, it was found that non-responder gastric cancer patients and drug-resistant gastric cancer cell lines showed increased expression of CAIX compared to responder patients and control cells, respectively. Furthermore, a drug called SLC0111 was found to improve the therapy response of both wild-type and resistant gastric cancer cells, suggesting its potential in overcoming chemoresistance.

CANCER LETTERS (2023)

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Article Oncology

Screening of key genes related to ferroptosis and a molecular interaction network analysis in colorectal cancer using machine learning and bioinformatics

Fengfu Xue et al.

Summary: This study identified key genes and molecular interactions related to ferroptosis in colorectal cancer using machine-learning and bioinformatics analyses. The study found that ANGPTL7 gene expression was positively correlated with NGB and CP genes but negatively correlated with TFR2 gene expression. By machine-learning analysis, 4 important genes (NOX4, TFR2, ALOXE3, and CA9) related to ferroptosis were identified. Patients had better prognosis when NOX4 expression levels were relatively low.

JOURNAL OF GASTROINTESTINAL ONCOLOGY (2023)

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Article Oncology

Screening of key genes related to ferroptosis and a molecular interaction network analysis in colorectal cancer using machine learning and bioinformatics

Fengfu Xue et al.

Summary: This study identified key genes and molecular interactions related to ferroptosis in colorectal cancer (CRC) using machine-learning and bioinformatics analyses. Four ferroptosis-related genes (NOX4, TFR2, ALOXE3, and CA9) were identified and their relationship with immune cell infiltration and associated immune checkpoints was validated. Lower expression levels of NOX4 were associated with more favorable patient outcomes.

JOURNAL OF GASTROINTESTINAL ONCOLOGY (2023)

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Article Multidisciplinary Sciences

An in silico model to study the impact of carbonic anhydrase IX expression on tumour growth and anti-PD-1 therapy

Julia Grajek et al.

Summary: Immune checkpoint inhibitors (ICIs) are a revolutionary cancer treatment with mechanisms not fully understood. This study investigates the role of the enzyme carbonic anhydrase IX (CAIX) in ICI success using an in silico model of the tumor microenvironment. The model shows that CAIX-expressing tumors acidify their environment, reducing immune infiltration and increasing tumor burden. Additionally, suppressing CAIX improves the response to anti-PD-1 treatment, independent of PD-L1 expression.

JOURNAL OF THE ROYAL SOCIETY INTERFACE (2023)

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Review Oncology

Understanding Drug Sensitivity and Tackling Resistance in Cancer

Jeffrey W. Tyner et al.

Summary: The diversity of cancer and the problem of drug resistance present major challenges in cancer treatment, but understanding the types and biological causes of resistance can provide opportunities for personalized therapies.

CANCER RESEARCH (2022)

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Review Biochemistry & Molecular Biology

Ferroptosis turns 10: Emerging mechanisms, physiological functions, and therapeutic applications

Brent R. Stockwell

Summary: This review describes the key regulators of ferroptosis and provides an overview of metabolism, ROS biology, and iron biology. Additionally, it highlights the important concepts and unanswered questions in the field of ferroptosis. The future holds promise for further breakthroughs in understanding the mechanisms of ferroptosis and utilizing it for therapeutic purposes.

CELL (2022)

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Article Multidisciplinary Sciences

Genome-wide synthetic lethal screen unveils novel CAIX-NFS1/xCT axis as a targetable vulnerability in hypoxic solid tumors

Shawn C. Chafe et al.

Summary: The study identified a redox homeostasis network involving the iron-sulfur cluster enzyme NFS1 in the survival mechanisms governed by the tumor hypoxia-induced pH regulator CAIX. Targeting CAIX while depleting NFS1 or blocking cyst(e)ine availability enhanced ferroptosis and inhibited tumor growth significantly. Altering intracellular pH and iron homeostasis through inhibiting CAIX activity may lead to the development of innovative therapeutic strategies for solid tumors to overcome hypoxia- and acidosis-mediated tumor progression and therapeutic resistance.

SCIENCE ADVANCES (2021)

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Review Biochemistry & Molecular Biology

Outlining the Complex Pathway of Mammalian Fe-S Cluster Biogenesis

Nunziata Maio et al.

TRENDS IN BIOCHEMICAL SCIENCES (2020)

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Article Oncology

A Phase 1 Study of SLC-0111, a Novel Inhibitor of Carbonic Anhydrase IX, in Patients With Advanced Solid Tumors

Paul C. McDonald et al.

AMERICAN JOURNAL OF CLINICAL ONCOLOGY-CANCER CLINICAL TRIALS (2020)

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Review Biochemistry & Molecular Biology

Persistent Cancer Cells: The Deadly Survivors

Shensi Shen et al.

CELL (2020)

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Review Oncology

The role of carbonic anhydrase IX in cancer development: links to hypoxia, acidosis, and beyond

Silvia Pastorekova et al.

CANCER AND METASTASIS REVIEWS (2019)

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Article Gastroenterology & Hepatology

Regulation of pH by Carbonic Anhydrase 9 Mediates Survival of Pancreatic Cancer Cells With Activated KRAS in Response to Hypoxia

Paul C. McDonald et al.

GASTROENTEROLOGY (2019)

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Article Oncology

Targeting Hypoxia-Induced Carbonic Anhydrase IX Enhances Immune-Checkpoint Blockade Locally and Systemically

Shawn C. Chafe et al.

CANCER IMMUNOLOGY RESEARCH (2019)

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Article Oncology

Harnessing Induced Essentiality: Targeting Carbonic Anhydrase IX and Angiogenesis Reduces Lung Metastasis of Triple Negative Breast Cancer Xenografts

Eva-Maria E. Hedlund et al.

CANCERS (2019)

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Article Biochemistry & Molecular Biology

Carbonic anhydrase 9 confers resistance to ferroptosis/apoptosis in malignant mesothelioma under hypoxia

Zan Li et al.

REDOX BIOLOGY (2019)

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Article Chemistry, Medicinal

Discovery of 4-Hydroxy-3-(3-(phenylureido)benzenesulfonamides as SLC-0111 Analogues for the Treatment of Hypoxic Tumors Overexpressing Carbonic Anhydrase IX

Murat Bozdag et al.

JOURNAL OF MEDICINAL CHEMISTRY (2018)

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Review Chemistry, Medicinal

Inhibition of carbonic anhydrase IX targets primary tumors, metastases, and cancer stem cells: Three for the price of one

Claudiu T. Supuran et al.

MEDICINAL RESEARCH REVIEWS (2018)

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Review Oncology

Eco-evolutionary causes and consequences of temporal changes in intratumoural blood flow

Robert J. Gillies et al.

NATURE REVIEWS CANCER (2018)

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Review Biochemistry & Molecular Biology

Oxygen availability and metabolic reprogramming in cancer

Hong Xie et al.

JOURNAL OF BIOLOGICAL CHEMISTRY (2017)

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Review Biochemistry & Molecular Biology

Biogenesis and functions of mammalian iron-sulfur proteins in the regulation of iron homeostasis and pivotal metabolic pathways

Tracey A. Rouault et al.

JOURNAL OF BIOLOGICAL CHEMISTRY (2017)

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Article Multidisciplinary Sciences

NFS1 undergoes positive selection in lung tumours and protects cells from ferroptosis

Samantha W. Alvarez et al.

NATURE (2017)

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Review Genetics & Heredity

Synthetic lethality and cancer

Nigel J. O'Neil et al.

NATURE REVIEWS GENETICS (2017)

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Article Biochemistry & Molecular Biology

The interactome of metabolic enzyme carbonic anhydrase IX reveals novel roles in tumor cell migration and invadopodia/MMP14-mediated invasion

M. Swayampakula et al.

ONCOGENE (2017)

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Article Medicine, Research & Experimental

Addition of carbonic anhydrase 9 inhibitor SLC-0111 to temozolomide treatment delays glioblastoma growth in vivo

Nathaniel H. Boyd et al.

JCI INSIGHT (2017)

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Review Oncology

Tumour acidosis: from the passenger to the driver's seat

Cyril Corbet et al.

NATURE REVIEWS CANCER (2017)

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Article Biochemical Research Methods

Design and synthesis of a novel class of carbonic anhydrase-IX inhibitor 1-(3-(phenyl/4-fluorophenyl)-7-imino-3H-[1,2,3]triazolo[4,5d]pyrimidin 6(7H)yl)urea

Shikha Kumari et al.

JOURNAL OF MOLECULAR GRAPHICS & MODELLING (2016)

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Review Oncology

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Michael S. Nakazawa et al.

NATURE REVIEWS CANCER (2016)

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Article Oncology

Carbonic Anhydrase IX Promotes Myeloid-Derived Suppressor Cell Mobilization and Establishment of a Metastatic Niche by Stimulating G-CSF Production

Shawn C. Chafe et al.

CANCER RESEARCH (2015)

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Article Oncology

Antiangiogenesis Strategies Revisited: From Starving Tumors to Alleviating Hypoxia

Rakesh K. Jain

CANCER CELL (2014)

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Article Biochemistry & Molecular Biology

Targeting carbonic anhydrase IX depletes breast cancer stem cells within the hypoxic niche

F. E. Lock et al.

ONCOGENE (2013)

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Review Oncology

Disrupting proton dynamics and energy metabolism for cancer therapy

Scott K. Parks et al.

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Carbonic Anhydrase IX Promotes Tumor Growth and Necrosis In Vivo and Inhibition Enhances Anti-VEGF Therapy

Alan McIntyre et al.

CLINICAL CANCER RESEARCH (2012)

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Recent Developments in Targeting Carbonic Anhydrase IX for Cancer Therapeutics

Paul C. McDonald et al.

ONCOTARGET (2012)

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Targeting Tumor Hypoxia: Suppression of Breast Tumor Growth and Metastasis by Novel Carbonic Anhydrase IX Inhibitors

Yuanmei Lou et al.

CANCER RESEARCH (2011)

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Ureido-Substituted Benzenesulfonamides Potently Inhibit Carbonic Anhydrase IX and Show Antimetastatic Activity in a Model of Breast Cancer Metastasis

Fabio Pacchiano et al.

JOURNAL OF MEDICINAL CHEMISTRY (2011)

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NATURE REVIEWS DRUG DISCOVERY (2011)

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High levels of carbonic anhydrase IX in tumour tissue and plasma are biomarkers of poor prognostic in patients with non-small cell lung cancer

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The key hypoxia regulated gene CAIX is upregulated in basal-like breast tumours and is associated with resistance to chemotherapy

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BRITISH JOURNAL OF CANCER (2009)

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Expression of carbonic anhydrase IX suggests poor outcome in rectal cancer

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Carbonic Anhydrase IX in Bladder Cancer A Diagnostic, Prognostic, and Therapeutic Molecular Marker

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Hypoxia-Inducible Carbonic Anhydrase IX and XII Promote Tumor Cell Growth by Counteracting Acidosis through the Regulation of the Intracellular pH

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CANCER RESEARCH (2009)

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Role of carbonic anhydrase IX expression in prediction of the efficacy and outcome of primary epirubicin/tamoxifen therapy for breast cancer

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Prognostic significance of a novel hypoxia-regulated marker, carbonic anhydrase IX, in invasive breast carcinoma

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