Carbonic Anhydrase XII is a Clinically Significant, Molecular Tumor-Subtype Specific Therapeutic Target in Glioma with the Potential to Combat Invasion of Brain Tumor Cells

References

• Lathia JD, Mack SC, Mulkearns-Hubert EE, Valentim CLL, Rich JN. Cancer stem cells in glioblastoma. Genes Dev. 2015;29:1203–1217. doi:10.1101/gad.261982.115
   PubMed Web of Science ®Google Scholar
• Kahlert UD, Joseph JV, Kruyt FAE. EMT- and MET-related processes in nonepithelial tumors: importance for disease progression, prognosis, and therapeutic opportunities. Mol Oncol. 2017;11:860–877. doi:10.1002/1878-0261.12085
   PubMed Web of Science ®Google Scholar
• Kahlert UD, Suwala AK, Raabe EH, et al. ZEB1 promotes invasion in human fetal neural stem cells and hypoxic glioma neurospheres. Brain Pathol. 2015;25:724–732. doi:10.1111/bpa.12240
   PubMed Web of Science ®Google Scholar
• Siebzehnrubl FA, Silver DJ, Tugertimur B, et al. The ZEB1 pathway links glioblastoma initiation, invasion and chemoresistance. EMBO Mol Med. 2013;5:1196–1212. doi:10.1002/emmm.201302827
   PubMed Web of Science ®Google Scholar
• Rosmaninho P, Mükusch S, Piscopo V, et al. Zeb1 potentiates genome-wide gene transcription with lef1 to promote glioblastoma cell invasion. EMBO J. 2018;37:e97115. doi:10.15252/embj.201797115
   PubMed Web of Science ®Google Scholar
• Suzuki K, Kawataki T, Endo K, Miyazawa K, Kinouchi H, Saitoh M. Expression of ZEBs in gliomas is associated with invasive properties and histopathological grade. Oncol Lett. 2018;16:1758–1764. doi:10.3892/ol.2018.8852
   PubMed Web of Science ®Google Scholar
• Kahlert UD, Maciaczyk D, Doostkam S, et al. Activation of Canonical WNT/β-Catenin signaling enhances in vitro motility of glioblastoma cells by activation of ZEB1 and Other Activators of Epithelial-to-Mesenchymal Transition. Cancer Lett. 2012;325:42–53. doi:10.1016/j.canlet.2012.05.024
   PubMed Web of Science ®Google Scholar
• Mboge MY, Mahon BP, McKenna R, Frost SC. Carbonic Anhydrases: role in PH Control and Cancer. Metabolites. 2018;8. doi:10.3390/metabo8010019
   PubMed Web of Science ®Google Scholar
• Chiche J, Ilc K, Laferrière J, et al. Hypoxia-Inducible Carbonic Anhydrase IX and XII promote tumor cell growth by counteracting acidosis through the regulation of the intracellular PH. Cancer Res. 2009;69:358–368. doi:10.1158/0008-5472.CAN-08-2470
   PubMed Web of Science ®Google Scholar
• Doyen J, Parks SK, Marcié S, Pouysségur J, Chiche J. Knock-down of hypoxia-induced carbonic anhydrases ix and xii radiosensitizes tumor cells by increasing intracellular acidosis. Front Oncol. 2012;2:199. doi:10.3389/fonc.2012.00199
   PubMedGoogle Scholar
• Beckner ME, Pollack IF, Nordberg ML, Hamilton RL. Glioblastomas with Copy Number Gains in EGFR and RNF139 show increased expressions of carbonic anhydrase genes transformed by ENO1. BBA Clin. 2015;5:1–15. doi:10.1016/j.bbacli.2015.11.001
   PubMedGoogle Scholar
• Haapasalo J, Hilvo M, Nordfors K, et al. Identification of an alternatively spliced isoform of carbonic anhydrase XII in Diffusely Infiltrating Astrocytic Gliomas. Neuro Oncol. 2008;10:131–138. doi:10.1215/15228517-2007-065
   PubMed Web of Science ®Google Scholar
• Proescholdt MA, Merrill MJ, Stoerr E-M, Lohmeier A, Pohl F, Brawanski A. Function of Carbonic Anhydrase IX in Glioblastoma Multiforme. Neuro Oncol. 2012;14:1357–1366. doi:10.1093/neuonc/nos216
   PubMed Web of Science ®Google Scholar
• Capper D, Jones DTW, Sill M, et al. DNA methylation-based classification of central nervous system tumours. Nature. 2018;555:469–474. doi:10.1038/nature26000
   PubMed Web of Science ®Google Scholar
• Verhaak RGW, Hoadley KA, Purdom E, et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 2010;17:98–110. doi:10.1016/j.ccr.2009.12.020
   PubMed Web of Science ®Google Scholar
• Louis DN, Perry A, Reifenberger G, et al. The 2016 world health organization classification of tumors of the central nervous system: a summary. Acta Neuropathol. 2016;131:803–820. doi:10.1007/s00401-016-1545-1
   PubMed Web of Science ®Google Scholar
• Louis DN, Wesseling P, Aldape K, et al. cIMPACT-NOW update 6: new entity and diagnostic principle recommendations of the cIMPACT-utrecht meeting on future CNS tumor classification and grading. Brain Pathol. 2020;30:844–856. doi:10.1111/bpa.12832
   PubMed Web of Science ®Google Scholar
• Reifenberger J, Reifenberger G, Liu L, James CD, Wechsler W, Collins VP. Molecular genetic analysis of oligodendroglial tumors shows preferential allelic deletions on 19q and 1p. Am J Pathol. 1994;145:1175–1190.
   PubMed Web of Science ®Google Scholar
• Singh S, Lomelino CL, Mboge MY, Frost SC, McKenna R. Cancer drug development of carbonic anhydrase inhibitors beyond the active site. Molecules. 2018;23:1045. doi:10.3390/molecules23051045
   PubMed Web of Science ®Google Scholar
• Herrera-Rios D, Li G, Khan D, et al. A computational guided, functional validation of a novel therapeutic antibody proposes notch signaling as a clinical relevant and druggable target in glioma. Sci Rep. 2020;10:16218. doi:10.1038/s41598-020-72480-y
   PubMed Web of Science ®Google Scholar
• Battke C, Kremmer E, Mysliwietz J, et al. Generation and characterization of the first inhibitory antibody targeting tumour-associated carbonic anhydrase XII. Cancer Immunol Immunother. 2011;60:649–658. doi:10.1007/s00262-011-0980-z
   PubMed Web of Science ®Google Scholar
• von Neubeck B, Gondi G, Riganti C, et al. An inhibitory antibody targeting carbonic anhydrase XII abrogates chemoresistance and significantly reduces lung metastases in an orthotopic breast cancer model in vivo. Int J Cancer. 2018;143:2065–2075. doi:10.1002/ijc.31607
   PubMed Web of Science ®Google Scholar
• Koch K, Hartmann R, Tsiampali J, et al. A comparative pharmaco-metabolomic study of glutaminase inhibitors in glioma stem-like cells confirms biological effectiveness but reveals differences in target-specificity. Cell Death Discov. 2020;6:20. doi:10.1038/s41420-020-0258-3
   PubMed Web of Science ®Google Scholar
• Vargas-Toscano A, Nickel A-C, Li G, et al. Rapalink-1 targets glioblastoma stem cells and acts synergistically with tumor treating fields to reduce resistance against temozolomide. Cancers. 2020;12:3859. doi:10.3390/cancers12123859
   PubMed Web of Science ®Google Scholar
• Gravendeel LAM, Kouwenhoven MCM, Gevaert O, et al. Intrinsic gene expression profiles of gliomas are a better predictor of survival than histology. Cancer Res. 2009;69:9065–9072. doi:10.1158/0008-5472.CAN-09-2307
   PubMed Web of Science ®Google Scholar
• Kawaguchi A, Yajima N, Tsuchiya N, et al. Gene expression signature-based prognostic risk score in patients with Glioblastoma. Cancer Sci. 2013;104:1205–1210. doi:10.1111/cas.12214
   PubMed Web of Science ®Google Scholar
• Mehrjardi NZ, Hänggi D, Kahlert UD. Current biomarker-associated procedures of cancer modeling-a reference in the context of IDH1 Mutant Glioma. Cell Death Dis. 2020;11:998. doi:10.1038/s41419-020-03196-0
   PubMed Web of Science ®Google Scholar
• Wiestler B, Capper D, Sill M, et al. Integrated DNA methylation and copy-number profiling identify three clinically and biologically relevant groups of anaplastic glioma. Acta Neuropathol. 2014;128:561–571. doi:10.1007/s00401-014-1315-x
   PubMed Web of Science ®Google Scholar
• Riemenschneider MJ, Hegi ME, Reifenberger G. MGMT Promoter Methylation in Malignant Gliomas. Target Oncol. 2010;5:161–165. doi:10.1007/s11523-010-0153-6
   PubMed Web of Science ®Google Scholar
• Ghosh D, Ulasov IV, Chen L, et al. TGFβ-Responsive HMOX1 expression is associated with stemness and invasion in glioblastoma multiforme. Stem Cells. 2016;34:2276–2289. doi:10.1002/stem.2411
   PubMed Web of Science ®Google Scholar
• Kim E-J, Jin X, Kim OR, Ham SW, Park S-H, Kim H. Glioma stem cells and their non-stem differentiated glioma cells exhibit differences in mitochondrial structure and function. Oncol Rep. 2018;39:411–416. doi:10.3892/or.2017.6075
   PubMed Web of Science ®Google Scholar
• Neradil J, Veselska R. Nestin as a Marker of Cancer Stem Cells. Cancer Sci. 2015;106:803–811. doi:10.1111/cas.12691
   PubMed Web of Science ®Google Scholar
• Berezovsky AD, Poisson LM, Cherba D, et al. Sox2 promotes malignancy in glioblastoma by regulating plasticity and astrocytic differentiation. Neoplasia. 2014;16:193–206.e25. doi:10.1016/j.neo.2014.03.006
   PubMed Web of Science ®Google Scholar
• Singh SK, Hawkins C, Clarke ID, et al. Identification of human brain tumour initiating cells. Nature. 2004;432:396–401. doi:10.1038/nature03128
   PubMed Web of Science ®Google Scholar
• Calvo KA, Scrideli CA, Moraes T, Da S, Teixeira SA. Silencing of CA12 by Interfering RNA sensitizes GBM cells to chemotherapy and reduces cell proliferation. Rev Med. 2020;99:14–15. doi:10.11606/issn.1679-9836.v99iSupplp14-15
   Google Scholar
• Fiedler L, Kellner M, Gosewisch A, et al. Evaluation of 177Lu[Lu]-CHX-A″-DTPA-6A10 fab as a radioimmunotherapy agent targeting carbonic anhydrase XII. Nucl Med Biol. 2018;60:55–62. doi:10.1016/j.nucmedbio.2018.02.004
   PubMed Web of Science ®Google Scholar
• Gondi G, Mysliwietz J, Hulikova A, et al. Antitumor efficacy of a monoclonal antibody that inhibits the activity of cancer-associated carbonic anhydrase XII. Cancer Res. 2013;73:6494–6503. doi:10.1158/0008-5472.CAN-13-1110
   PubMed Web of Science ®Google Scholar
• Schreck KC, Taylor P, Marchionni L, et al. The Notch Target Hes1 Directly Modulates Gli1 Expression and Hedgehog Signaling: a Potential Mechanism of Therapeutic Resistance. Clin Cancer Res. 2010;16:6060–6070. doi:10.1158/1078-0432.CCR-10-1624
   PubMed Web of Science ®Google Scholar
• Stravinskiene D, Sliziene A, Baranauskiene L, Petrikaite V, Zvirbliene A. Inhibitory monoclonal antibodies and their recombinant derivatives targeting surface-exposed carbonic anhydrase xii on cancer cells. Int J Mol Sci. 2020;21. doi:10.3390/ijms21249411
   PubMed Web of Science ®Google Scholar
• Uda NR, Stenner F, Seibert V, et al. Humanized monoclonal antibody blocking carbonic anhydrase 12 enzymatic activity leads to reduced tumor growth in vitro. Anticancer Res. 2019;39:4117–4128. doi:10.21873/anticanres.13570
   PubMed Web of Science ®Google Scholar
• Aslam S, Gupta V. Carbonic Anhydrase Inhibitors. In StatPearls; StatPearls Publishing: treasure Island (FL). 2020.
   Google Scholar
• Supuran CT. Carbonic Anhydrases: novel Therapeutic Applications for Inhibitors and Activators. Nat Rev Drug Discov. 2008;7:168–181. doi:10.1038/nrd2467
   PubMed Web of Science ®Google Scholar
• Williams KJ, Gieling RG. Preclinical evaluation of ureidosulfamate carbonic anhydrase ix/xii inhibitors in the treatment of cancers. Int J Mol Sci. 2019;20. doi:10.3390/ijms20236080
   PubMed Web of Science ®Google Scholar
• Salaroglio IC, Mujumdar P, Annovazzi L, et al. Carbonic anhydrase xii inhibitors overcome p-glycoprotein-mediated resistance to temozolomide in glioblastoma. Mol Cancer Ther. 2018;17:2598–2609. doi:10.1158/1535-7163.MCT-18-0533
   PubMed Web of Science ®Google Scholar
• Mujumdar P, Kopecka J, Bua S, Supuran CT, Riganti C, Poulsen S-A. Carbonic anhydrase xii inhibitors overcome temozolomide resistance in glioblastoma. J Med Chem. 2019;62:4174–4192. doi:10.1021/acs.jmedchem.9b00282
   PubMed Web of Science ®Google Scholar
• Koch K, Hartmann R, Schröter F, et al. Reciprocal regulation of the cholinic phenotype and epithelial-mesenchymal transition in glioblastoma cells. Oncotarget. 2016;7:73414–73431. doi:10.18632/oncotarget.12337
   PubMedGoogle Scholar
• Vergara D, Ravaioli S, Fonzi E, et al. Carbonic anhydrase xii expression is modulated during epithelial mesenchymal transition and regulated through protein kinase c signaling. Int J Mol Sci. 2020:21. doi:10.3390/ijms21030715
   PubMedGoogle Scholar
• Shaul YD, Freinkman E, Comb WC, et al. Dihydropyrimidine accumulation is required for the epithelial-mesenchymal transition. Cell. 2014;158:1094–1109. doi:10.1016/j.cell.2014.07.032
   PubMed Web of Science ®Google Scholar
• Ghosh D, Funk CC, Caballero J, et al. A cell-surface membrane protein signature for glioblastoma. Cell Syst. 2017;4:516–529.e7. doi:10.1016/j.cels.2017.03.004
   PubMed Web of Science ®Google Scholar