Carbonic anhydrase IX as a novel candidate in liquid biopsy

References

• Johnson X, Alric J. Interaction between starch breakdown, acetate assimilation, and photosynthetic cyclic electron flow in Chlamydomonas reinhardtii. J Biol Chem 2012;287:26445–52.
   PubMed Web of Science ®Google Scholar
• Tcherkez G, Boex-Fontvieille E, Mahe A. Respiratory carbon fluxes in leaves. Curr Opin Plant Biol 2012;15:308–14.
   PubMed Web of Science ®Google Scholar
• Smith KS, Ferry JG. Prokaryotic carbonic anhydrases. FEMS Microbiol Rev 2000;24:335–66.
   PubMed Web of Science ®Google Scholar
• Maeda S, Price GD, Badger MR, et al. Bicarbonate binding activity of the CmpA protein of the cyanobacterium Synechococcus sp. strain PCC 7942 involved in active transport of bicarbonate. J Biol Chem 2000;275:20551–5.
   PubMed Web of Science ®Google Scholar
• Joseph P, Ouahrani-Bettache S, Montero JL, et al. A new beta-carbonic anhydrase from Brucella suis, its cloning, characterization, and inhibition with sulfonamides and sulfamates, leading to impaired pathogen growth. Bioorg Med Chem 2011;19:1172–8.
   PubMed Web of Science ®Google Scholar
• Joseph P, Turtaut F, Ouahrani-Bettache S, et al. Cloning, characterization, and inhibition studies of a beta-carbonic anhydrase from Brucella suis. J Med Chem 2010;53:2277–85.
   PubMed Web of Science ®Google Scholar
• Annunziato G, Angeli A, D’Alba F, et al. Discovery of new potential anti-infective compounds based on carbonic anhydrase inhibitors by rational target-focused repurposing approaches. ChemMedChem 2016;11:1904–14.
   PubMed Web of Science ®Google Scholar
• Ozensoy Guler O, Capasso C, Supuran CT. A magnificent enzyme superfamily: carbonic anhydrases, their purification and characterization. J Enzyme Inhib Med Chem 2016;31:689–94.
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, De Luca V, et al. Sulfonamide inhibition studies of the beta-carbonic anhydrase from the pathogenic bacterium Vibrio cholerae. Bioorg Med Chem 2016;24:1115–20.
   PubMed Web of Science ®Google Scholar
• Del Prete S, De Luca V, De Simone G, et al. Cloning, expression and purification of the complete domain of the eta-carbonic anhydrase from Plasmodium falciparum. J Enzyme Inhib Med Chem 2016;31:54–9.
   PubMed Web of Science ®Google Scholar
• Capasso C, Supuran CT. An overview of the carbonic anhydrases from two pathogens of the oral cavity: Streptococcus mutans and Porphyromonas gingivalis. Curr Top Med Chem 2016;16:2359–68.
   PubMed Web of Science ®Google Scholar
• Jensen EL, Clement R, Kosta A, et al. A new widespread subclass of carbonic anhydrase in marine phytoplankton. Isme J 2019;13:2094–106.
   PubMed Web of Science ®Google Scholar
• Kikutani S, Nakajima K, Nagasato C, et al. Thylakoid luminal theta-carbonic anhydrase critical for growth and photosynthesis in the marine diatom Phaeodactylum tricornutum. Proc Natl Acad Sci USA 2016;113:9828–33.
   PubMed Web of Science ®Google Scholar
• Del Prete S, Vullo D, Fisher GM, et al. Discovery of a new family of carbonic anhydrases in the malaria pathogen Plasmodium falciparum–the eta-carbonic anhydrases. Bioorg Med Chem Lett 2014;24:4389–96.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Capasso C. Biomedical applications of prokaryotic carbonic anhydrases. Expert Opin Ther Pat 2018;28:745–54.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrase activators. Future Med Chem 2018;10:561–73.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Capasso C. An overview of the bacterial carbonic anhydrases. Metabolites 2017;7:56–74.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Capasso C. Carbonic anhydrase from Porphyromonas gingivalis as a drug target. Pathogens 2017;6:30–42.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Advances in structure-based drug discovery of carbonic anhydrase inhibitors. Expert Opin Drug Discov 2017;12:61–88.
   PubMed Web of Science ®Google Scholar
• Capasso C, Supuran CT. Bacterial, fungal and protozoan carbonic anhydrases as drug targets. Expert Opin Ther Targets 2015;19:1689–704.
   PubMed Web of Science ®Google Scholar
• Aspatwar A, Tolvanen ME, Ortutay C, et al. Carbonic anhydrase related proteins: molecular biology and evolution. Subcell Biochem 2014;75:135–56.
   PubMedGoogle Scholar
• Supuran CT. Carbonic anhydrases as drug targets–an overview. Curr Top Med Chem 2007;7:825–33.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Capasso C. The eta-class carbonic anhydrases as drug targets for antimalarial agents. Expert Opin Ther Targets 2015;19:551–63.
   PubMed Web of Science ®Google Scholar
• Capasso C, Supuran CT. An overview of the selectivity and efficiency of the bacterial carbonic anhydrase inhibitors. Curr Med Chem 2015;22:2130–9.
   PubMed Web of Science ®Google Scholar
• Capasso C, Supuran CT. An overview of the alpha-, beta- and gamma-carbonic anhydrases from bacteria: can bacterial carbonic anhydrases shed new light on evolution of bacteria? J Enzyme Inhib Med Chem 2015;30:325–32.
   PubMed Web of Science ®Google Scholar
• Capasso C, Supuran CT. Sulfa and trimethoprim-like drugs – antimetabolites acting as carbonic anhydrase, dihydropteroate synthase and dihydrofolate reductase inhibitors. J Enzyme Inhib Med Chem 2014;29:379–87.
   PubMed Web of Science ®Google Scholar
• Capasso C, Supuran CT. Anti-infective carbonic anhydrase inhibitors: a patent and literature review. Expert Opin Ther Pat 2013;23:693–704.
   PubMed Web of Science ®Google Scholar
• Miyamoto H, Miyashita T, Okushima M, et al. A carbonic anhydrase from the nacreous layer in oyster pearls. Proc Natl Acad Sci USA 1996;93:9657–60.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrases–an overview. Curr Pharm Des 2008;14:603–14.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrase inhibition and the management of hypoxic tumors. Metabolites 2017;7:48–60.
   PubMed Web of Science ®Google Scholar
• Lane TW, Saito MA, George GN, et al. Biochemistry: a cadmium enzyme from a marine diatom. Nature 2005;435:42.
   PubMed Web of Science ®Google Scholar
• Ferry JG. The gamma class of carbonic anhydrases. Biochim Biophys Acta 2010;1804:374–81.
   PubMed Web of Science ®Google Scholar
• Jang M, Kim SS, Lee J. Cancer cell metabolism: implications for therapeutic targets. Exp Mol Med 2013;45:e45.
   PubMed Web of Science ®Google Scholar
• Petrou A, Geronikaki A, Terzi E, et al. Inhibition of carbonic anhydrase isoforms I, II, IX and XII with secondary sulfonamides incorporating benzothiazole scaffolds. J Enzyme Inhib Med Chem 2016;31:1306–11.
   PubMed Web of Science ®Google Scholar
• Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov 2011;10:767–77.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Di Fiore A, Alterio V, et al. Recent advances in structural studies of the carbonic anhydrase family: the crystal structure of human CA IX and CA XIII. Curr Pharm Des 2010;16:3246–54.
   PubMed Web of Science ®Google Scholar
• Hilvo M, Baranauskiene L, Salzano AM, et al. Biochemical characterization of CA IX, one of the most active carbonic anhydrase isozymes. J Biol Chem 2008;283:27799–809.
   PubMed Web of Science ®Google Scholar
• Di Fiore A, De Simone G, Menchise V, et al. Carbonic anhydrase inhibitors: X-ray crystal structure of a benzenesulfonamide strong CA II and CA IX inhibitor bearing a pentafluorophenylaminothioureido tail in complex with isozyme II. Bioorg Med Chem Lett 2005;15:1937–42.
   PubMed Web of Science ®Google Scholar
• Winum JY, Rami M, Scozzafava A, et al. Carbonic anhydrase IX: a new druggable target for the design of antitumor agents. Med Res Rev 2008;28:445–63.
   PubMed Web of Science ®Google Scholar
• Winum JY, Pastorekova S, Jakubickova L, et al. Carbonic anhydrase inhibitors: synthesis and inhibition of cytosolic/tumor-associated carbonic anhydrase isozymes I, II, and IX with bis-sulfamates. Bioorg Med Chem Lett 2005;15:579–84.
   PubMed Web of Science ®Google Scholar
• Eldehna WM, Abo-Ashour MF, Berrino E, et al. SLC-0111 enaminone analogs, 3/4-(3-aryl-3-oxopropenyl) aminobenzenesulfonamides, as novel selective subnanomolar inhibitors of the tumor-associated carbonic anhydrase isoform IX. Bioorg Chem 2019;83:549–58.
   PubMed Web of Science ®Google Scholar
• Mboge MY, Chen Z, Wolff A, et al. Selective inhibition of carbonic anhydrase IX over carbonic anhydrase XII in breast cancer cells using benzene sulfonamides: Disconnect between activity and growth inhibition. PLoS One 2018;13:e0207417.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrase inhibitors as emerging agents for the treatment and imaging of hypoxic tumors. Expert Opin Investig Drugs 2018;27:963–70.
   PubMed Web of Science ®Google Scholar
• Eldehna WM, Nocentini A, Al-Rashood ST, et al. Tumor-associated carbonic anhydrase isoform IX and XII inhibitory properties of certain isatin-bearing sulfonamides endowed with in vitro antitumor activity towards colon cancer. Bioorg Chem 2018;81:425–32.
   PubMed Web of Science ®Google Scholar
• Liao SY, Lerman MI, Stanbridge EJ. Expression of transmembrane carbonic anhydrases, CAIX and CAXII, in human development. BMC Dev Biol 2009;9:22.
   PubMed Web of Science ®Google Scholar
• Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008;7:168–81.
   PubMed Web of Science ®Google Scholar
• Muller V, Riethdorf S, Rack B, et al. Prospective evaluation of serum tissue inhibitor of metalloproteinase 1 and carbonic anhydrase IX in correlation to circulating tumor cells in patients with metastatic breast cancer. Breast Cancer Res 2011;13:R71.
   PubMed Web of Science ®Google Scholar
• Aspatwar A, Tolvanen ME, Ortutay C, et al. Carbonic anhydrase related protein VIII and its role in neurodegeneration and cancer. Curr Pharm Des 2010;16:3264–76.
   PubMed Web of Science ®Google Scholar
• Horie K, Kawakami K, Fujita Y, et al. Exosomes expressing carbonic anhydrase 9 promote angiogenesis. Biochem Biophys Res Commun 2017;492:356–61.
   PubMed Web of Science ®Google Scholar
• Zavada J, Zavadova Z, Zat’ovicova M, et al. Soluble form of carbonic anhydrase IX (CA IX) in the serum and urine of renal carcinoma patients. Br J Cancer 2003;89:1067–71.
   PubMed Web of Science ®Google Scholar
• Pan PW, Waheed A, Sly WS, et al. Carbonic anhydrases in the mouse harderian gland. J Mol Histol 2010;41:411–7.
   PubMed Web of Science ®Google Scholar
• Supuran CT. How many carbonic anhydrase inhibition mechanisms exist? J Enzyme Inhib Med Chem 2016;31:345–60.
   PubMed Web of Science ®Google Scholar
• Parkkila S, Rajaniemi H, Parkkila AK, et al. Carbonic anhydrase inhibitor suppresses invasion of renal cancer cells in vitro. Proc Natl Acad Sci USA 2000;97:2220–4.
   PubMed Web of Science ®Google Scholar
• Guler O, Simone G, Supuran C. Drug design studies of the novel antitumor targets carbonic anhydrase IX and XII. Curr Med Chem 2010;17:1516–26.
   PubMed Web of Science ®Google Scholar
• Monti SM, Supuran CT, De Simone G. Anticancer carbonic anhydrase inhibitors: a patent review (2008–2013). Expert Opin Ther Pat 2013;23:737–49.
   PubMed Web of Science ®Google Scholar
• Nishiumi S, Yoshida M. [Possibility of metabolite biomarkers for early detection of cancer]. Gan to Kagaku Ryoho 2018;45:894–8.
   PubMedGoogle Scholar
• Han X, Wang J, Sun Y. Circulating tumor DNA as biomarkers for cancer detection. Genomics Proteomics Bioinformatics 2017;15:59–72.
   PubMed Web of Science ®Google Scholar
• Zhang W, Xia W, Lv Z, et al. Liquid biopsy for cancer: circulating tumor cells, circulating free DNA or exosomes? Cell Physiol Biochem 2017;41:755–68.
   PubMedGoogle Scholar
• Offin M, Chabon JJ, Razavi P, et al. Capturing genomic evolution of lung cancers through liquid biopsy for circulating tumor DNA. J Oncol 2017;2017:1.
   Web of Science ®Google Scholar
• Ashworth TR. A case of cancer in which cells similar to those in the tumours were seen in the blood after death. Austr Med J 1869;14:146–7.
   Google Scholar
• Sheng W, Ogunwobi OO, Chen T, et al. Capture, release and culture of circulating tumor cells from pancreatic cancer patients using an enhanced mixing chip. Lab Chip 2014;14:89–98.
   PubMed Web of Science ®Google Scholar
• Suo Y, Gu Z, Wei X. Advances of in vivo flow cytometry on cancer studies. Cytometry A 2019. [Epub ahead of print]. doi:10.1002/cyto.a.23851
   PubMed Web of Science ®Google Scholar
• Khetani S, Mohammadi M, Nezhad AS. Filter-based isolation, enrichment, and characterization of circulating tumor cells. Biotechnol Bioeng 2018;115:2504–29.
   PubMed Web of Science ®Google Scholar
• Werbin JL, Nordberg JJ, Tzucker J, et al. RareCyte® CTC analysis step 2: detection of circulating tumor cells by CyteFinder® automated scanning and semiautomated image analysis. Methods Mol Biol 2017;1634:173–80.
   PubMedGoogle Scholar
• Hassan EM, Willmore WG, DeRosa MC. Aptamers: promising tools for the detection of circulating tumor cells. Nucleic Acid Ther 2016;26:335–47.
   PubMed Web of Science ®Google Scholar
• Ghossein RA, Bhattacharya S. Molecular detection and characterization of circulating tumor cells and micrometastases in prostatic, urothelial, and renal cell carcinomas. Semin Surg Oncol 2001;20:304–11.
   PubMed Web of Science ®Google Scholar
• Mandel P, Metais P. Les acides nucléiques du plasma sanguin chez l'homme. C R Seances Soc Biol Fil 1948;142:241–3.
   PubMedGoogle Scholar
• Kanwar N, Hu P, Bedard P, et al. Identification of genomic signatures in circulating tumor cells from breast cancer. Int J Cancer 2015;137:332–44.
   PubMed Web of Science ®Google Scholar
• Li H, Jing C, Wu J, et al. Circulating tumor DNA detection: a potential tool for colorectal cancer management. Oncol Lett 2019;17:1409–16.
   PubMed Web of Science ®Google Scholar
• Heitzer E, Auer M, Ulz P, et al. Circulating tumor cells and DNA as liquid biopsies. Genome Med 2013;5:73.
   PubMed Web of Science ®Google Scholar
• Lim M, Kim CJ, Sunkara V, et al. Liquid biopsy in lung cancer: clinical applications of circulating biomarkers (CTCs and ctDNA). Micromachines (Basel) 2018;9. doi:10.3390/mi9030100
   Web of Science ®Google Scholar
• Neumann MHD, Bender S, Krahn T, et al. ctDNA and CTCs in liquid biopsy - current status and where we need to progress. Comput Struct Biotechnol J 2018;16:190–5.
   PubMed Web of Science ®Google Scholar
• Shang M, Ji JS, Song C, et al. Extracellular vesicles: a brief overview and its role in precision medicine. Methods Mol Biol 2017;1660:1–14.
   PubMedGoogle Scholar
• Campanella C, Caruso Bavisotto C, Logozzi M, et al. On the choice of the extracellular vesicles for therapeutic purposes. Int J Mol Sci 2019;20. doi:10.3390/ijms20020236
   Web of Science ®Google Scholar
• Colombo M, Giannandrea D, Lesma E, et al. Extracellular vesicles enhance multiple myeloma metastatic dissemination. Int J Mol Sci 2019;20. doi: 10.3390/ijms20133236
   Web of Science ®Google Scholar
• Fais S, O’Driscoll L, Borras FE, et al. Evidence-based clinical use of nanoscale extracellular vesicles in nanomedicine. ACS Nano 2016;10:3886–99.
   PubMed Web of Science ®Google Scholar
• Logozzi M, Angelini DF, Giuliani A, et al. Increased plasmatic levels of PSA-expressing exosomes distinguish prostate cancer patients from benign prostatic hyperplasia: a prospective study. Cancers (Basel) 2019;11. doi:10.3390/cancers11101449
   Web of Science ®Google Scholar
• De Simone G, Supuran CT. Carbonic anhydrase IX: Biochemical and crystallographic characterization of a novel antitumor target. Biochim Biophys Acta 2010;1804:404–9.
   PubMed Web of Science ®Google Scholar
• Svastova E, Witarski W, Csaderova L, et al. Carbonic anhydrase IX interacts with bicarbonate transporters in lamellipodia and increases cell migration via its catalytic domain. J Biol Chem 2012;287:3392–402.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Alterio V, Di Fiore A, et al. Inhibition of carbonic anhydrase IX targets primary tumors, metastases, and cancer stem cells: Three for the price of one. Med Res Rev 2018;38:1799–836.
   PubMed Web of Science ®Google Scholar
• Ilie M, Mazure NM, Hofman V, et al. High levels of carbonic anhydrase IX in tumour tissue and plasma are biomarkers of poor prognostic in patients with non-small cell lung cancer. Br J Cancer 2010;102:1627–35.
   PubMed Web of Science ®Google Scholar
• Logozzi M, Capasso C, Di Raimo R, et al. Prostate cancer cells and exosomes in acidic condition show increased carbonic anhydrase IX expression and activity. J Enzyme Inhib Med Chem 2019;34:272–8.
   PubMed Web of Science ®Google Scholar
• Dorai T, Sawczuk IS, Pastorek J, et al. The role of carbonic anhydrase IX overexpression in kidney cancer. Eur J Cancer 2005;41:2935–47.
   PubMed Web of Science ®Google Scholar
• Murai T. The role of lipid rafts in cancer cell adhesion and migration. Int J Cell Biol 2012;2012:1.
   Google Scholar
• Kaluz S, Kaluzova M, Liao SY, et al. Transcriptional control of the tumor- and hypoxia-marker carbonic anhydrase 9: a one transcription factor (HIF-1) show? Biochim Biophys Acta 2009;1795:162–72.
   PubMed Web of Science ®Google Scholar
• Brown-Glaberman U, Marron M, Chalasani P, et al. Circulating carbonic anhydrase IX and antiangiogenic therapy in breast cancer. Dis Markers 2016;2016:1.
   Web of Science ®Google Scholar
• Finkelmeier F, Canli O, Peiffer KH, et al. Circulating hypoxia marker carbonic anhydrase IX (CA9) in patients with hepatocellular carcinoma and patients with cirrhosis. PLoS One 2018;13:e0200855.
   PubMed Web of Science ®Google Scholar
• Malentacchi F, Vinci S, Melina AD, et al. Urinary carbonic anhydrase IX splicing messenger RNA variants in urogenital cancers. Urol Oncol 2016;34:292 e9–292 e16.
   PubMed Web of Science ®Google Scholar
• Liu S, Tian Z, Zhang L, et al. Combined cell surface carbonic anhydrase 9 and CD147 antigens enable high-efficiency capture of circulating tumor cells in clear cell renal cell carcinoma patients. Oncotarget 2016;7:59877–91.
   PubMedGoogle Scholar