439
Views
41
CrossRef citations to date
0
Altmetric
Review

Carbonic anhydrases as disease markers

, , &
Pages 509-533 | Received 10 Feb 2019, Accepted 05 Jun 2019, Published online: 17 Jun 2019

References

  • Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discovery. 2008;7:168–181.
  • Supuran CT. Structure and function of carbonic anhydrases. Biochem J. 2016 Jul 15;473(14):2023–2032.
  • Supuran CT, Capasso C. An overview of the bacterial carbonic anhydrases. Metabolites. 2017 Nov 11;7:4.
  • Zolfaghari Emameh R, Barker HR, Syrjanen L, et al. Identification and inhibition of carbonic anhydrases from nematodes. J Enzyme Inhib Med Chem. 2016;31(sup4):176–184.
  • Capasso C, Supuran CT. Bacterial, fungal and protozoan carbonic anhydrases as drug targets. Expert Opin Ther Targets. 2015;19(12):1689–1704.
  • Alterio V, Di Fiore A, D’Ambrosio K, et al. Multiple binding modes of inhibitors to carbonic anhydrases: how to design specific drugs targeting 15 different isoforms? Chem Rev. 2012 Aug 8;112(8):4421–4468.
  • Ilies MA, Banciu MD. Non-sulfonamide carbonic anhydrase inhibitors. In: Supuran CT, Scozzafava A, Conway J, editors. Carbonic anhydrase: its inhibitors and activators. Boca Raton: CRC Press; 2004. p. 207–239.
  • Krishnamurthy VM, Kaufman GK, Urbach AR, et al. Carbonic anhydrase as a model for biophysical and physical-organic studies of proteins and protein-ligand binding. Chem Rev. 2008 Mar;108(3):946–1051.
  • Akocak S, Ilies MA. Next-generation primary sulfonamide carbonic anhydrase inhibitors. In: Supuran CT, Capasso C, editors. Targeting carbonic anhydrases. London: Future Science; 2014. p. 35–51.
  • Supuran CT. Advances in structure-based drug discovery of carbonic anhydrase inhibitors. Expert Opin Drug Discov. 2017 Jan;12(1):61–88.
  • Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discovery. 2011 Sep 16; 10(10):767–777.
  • Supuran CT, Scozzafava A, Jurca BC, et al. Carbonic anhydrase inhibitors. part 49. Synthesis of substituted-ureido and thioureido derivatives of aromatic/heterocyclic sulfonamides with increased affinities for isozyme I. Eur J Med Chem. 1998;33:83–93.
  • Pacchiano F, Carta F, McDonald PC, et al. Ureido-substituted benzenesulfonamides potently inhibit carbonic anhydrase IX and show antimetastatic activity in a model of breast cancer metastasis. J Med Chem. 2011 Mar 24;54(6):1896–1902.
  • Krall N, Pretto F, Decurtins W, et al. A small-molecule drug conjugate for the treatment of carbonic anhydrase IX expressing tumors. Angew Chem Int Ed Engl. 2014 Apr 14;53(16):4231–4235.
  • Shabana AM, Mondal UK, Alam MR, et al. pH-sensitive multiligand gold nanoplatform targeting carbonic anhydrase IX enhances the delivery of doxorubicin to hypoxic tumor spheroids and overcomes the hypoxia-induced chemoresistance. ACS Appl Mater Interfaces. 2018 May 30;10(21):17792–17808.
  • Supuran CT. Carbonic anhydrase activators. Future Med Chem. 2018 Mar 1; 10(5):561–573.
  • Sun MK, Alkon DL. Carbonic anhydrase gating of attention: memory therapy and enhancement. Trends Pharmacol Sci. 2002 Feb;23(2):83–89.
  • Dave K, Scozzafava A, Vullo D, et al. Pyridinium derivatives of histamine are potent activators of cytosolic carbonic anhydrase isoforms I, II and VII. Org Biomol Chem. 2011 Apr 21;9(8):2790–2800.
  • Draghici B, Vullo D, Akocak S, et al. Ethylene bis-imidazoles are highly potent and selective activators for isozymes VA and VII of carbonic anhydrase, with a potential nootropic effect. Chem Commun (Camb). 2014 Jun 7;50(45):5980–5983.
  • Canto de Souza L, Provensi G, Vullo D, et al. Carbonic anhydrase activation enhances object recognition memory in mice through phosphorylation of the extracellular signal-regulated kinase in the cortex and the hippocampus. Neuropharmacology. 2017 May 15;118:148–156.
  • Sanku RKK, John JS, Salkovitz M, et al. Potential learning and memory disruptors and enhancers in a simple, 1-day operant task in mice. Behav Pharmacol. 2018 29(6):482-492.
  • Bhatt A, Mondal UK, Supuran CT, et al. Crystal structure of carbonic anhydrase II in complex with an activating ligand: implications in neuronal function. Mol Neurobiol. 2018 Sep;55(9):7431–7437.
  • Ilies M, Banciu MD, Ilies MA, et al. Carbonic anhydrase activators: design of high affinity isozymes I, II, and IV activators, incorporating tri-/tetrasubstituted-pyridinium-azole moieties. J Med Chem. 2002 Jan 17;45(2):504–510.
  • Dave K, Ilies MA, Scozzafava A, et al. An inhibitor-like binding mode of a carbonic anhydrase activator within the active site of isoform II. Bioorg Med Chem Lett. 2011 May 1;21(9):2764–2768.
  • Sly WS, Hu PY. Human carbonic anhydrases and carbonic anhydrase deficiencies. Annu Rev Biochem. 1995;64:375–401.
  • Lee HS, Shin HS, Kang UB, et al., Multiple biomarker set for breast cancer diagnosis, method of detecting the same, and diagnosis kit for breast cancer using antibody against the same. US20150024960. 2015.
  • Wang DB, Lu XK, Zhang X, et al. Carbonic anhydrase 1 is a promising biomarker for early detection of non-small cell lung cancer. Tumour Biol. 2016 Jan;37(1):553–559.
  • Takakura M, Yokomizo A, Tanaka Y, et al. Carbonic anhydrase I as a new plasma biomarker for prostate cancer. ISRN Oncol. 2012;2012:768190.
  • Taka-Aki N, Tomoaki H, Diagnostic agent for sepsis WO2018088455. 2018.
  • Kardoush MI, Ward BJ, Ndao M. Serum carbonic anhydrase 1 is a biomarker for diagnosis of human schistosoma mansoni infection. Am J Trop Med Hyg. 2017 Apr;96(4):842–849.
  • Granier C, Molina F, Salvetat N, et al. Early prediction markers of diabetic nephropathy. EP2963422. 2016.
  • Geyer RR, Zhao P, Parker MD, et al. Assay and method for quantitating carbonic anhydrase activity and assessing red blood hemolysis. US20160355867. 2016.
  • Clofent-Sanchez G, Deramchia K, Jacobin AJ, et al. Antibodies for molecular imaging of vulnerable plaques in atherosclerosis. WO2011IB03011. 2013.
  • Parkkila S, Lasota J, Fletcher JA, et al. Carbonic anhydrase II. A novel biomarker for gastrointestinal stromal tumors. Mod Pathol. 2010 May;23(5):743–750.
  • Carter N, Jeffery S, Shiels A, et al. Characterization of human carbonic anhydrase III from skeletal muscle. Biochem Genet. 1979 Oct;17(9–10):837–854.
  • Barak AJ, Beckenhauer HC, Tuma DJ, et al. Effects of prolonged ethanol feeding on methionine metabolism in rat liver. Biochem Cell Biol. 1987 Mar;65(3):230–233.
  • Kharbanda KK, Vigneswara V, McVicker BL, et al. Proteomics reveal a concerted upregulation of methionine metabolic pathway enzymes, and downregulation of carbonic anhydrase-III, in betaine supplemented ethanol-fed rats. Biochem Biophys Res Commun. 2009 Apr 17;381(4):523–527.
  • Carter WG, Vigneswara V, Newlaczyl A, et al. Isoaspartate, carbamoyl phosphate synthase-1, and carbonic anhydrase-III as biomarkers of liver injury. Biochem Biophys Res Commun. 2015 Mar 13;458(3):626–631.
  • Vaananen HK, Syrjala H, Rahkila P, et al. Serum carbonic anhydrase III and myoglobin concentrations in acute myocardial infarction. Clin Chem. 1990 Apr;36(4):635–638.
  • Vuori J, Syrjala H, Vaananen HK. Myoglobin/carbonic anhydrase III ratio: highly specific and sensitive early indicator for myocardial damage in acute myocardial infarction. Clin Chem. 1996 Jan;42(1):107–109.
  • Kemp M, Donovan J, Higham H, et al. Biochemical markers of myocardial injury. Br J Anaesth. 2004 Jul;93(1):63–73.
  • Vuotikka P, Uusimaa P, Niemela M, et al. Serum myoglobin/carbonic anhydrase III ratio as a marker of reperfusion after myocardial infarction. Int J Cardiol. 2003 Oct;91(2–3):137–144.
  • Sawicki M, Sypniewska G, Krintus M, et al. Multi-Marker approach with the use of biochip cardiac array technology for early diagnosis in patients with acute coronary syndromes. Ejifcc. 2008 Dec;19(3):160–171.
  • Robert-Pachot M, Desbos A, Moreira A, et al. Carbonic anhydrase III: a new target for autoantibodies in autoimmune diseases. Autoimmunity. 2007 Jul;40(5):380–389.
  • Saito R, Watanabe H, Asano T, et al. Anti-carbonic anhydrase III autoantibodies in vasculitis syndrome. Int J Rheum Dis. 2013 Jun;16(3):339–346.
  • Stams T, Nair SK, Okuyama T, et al. Crystal structure of the secretory form of membrane-associated human carbonic anhydrase IV at 2.8-A resolution. Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13589–13594.
  • Zhu XL, Sly WS. Carbonic anhydrase IV from human lung. Purification, characterization, and comparison with membrane carbonic anhydrase from human kidney. J Biol Chem. 1990 May 25;265(15):8795–8801.
  • Wistrand PJ, Knuuttila KG. Renal membrane-bound carbonic anhydrase. Purification and properties. Kidney Int. 1989 Mar;35(3):851–859.
  • Supuran CT, Ilies MA, Scozzafava A. Carbonic anhydrase inhibitors – part 29: interaction of isozymes I, II and IV with benzolamide-like derivatives. Eur J Med Chem. 1998;33:739–751.
  • Supuran CT, Scozzafava A, Ilies MA, et al. Carbonic anhydrase inhibitors – part 53 – synthesis of substituted-pyridinium derivatives of aromatic sulfonamides: the first non-polymeric membrane-impermeable inhibitors with selectivity for isozyme IV. Eur J Med Chem. 1998 Jul-Aug;33(7–8):577–594.
  • Supuran CT, Scozzafava A, Ilies MA, et al. Carbonic anhydrase inhibitors: synthesis of sulfonamides incorporating 2,4,6-trisubstituted-pyridinium-ethylcarboxamido moieties possessing membrane-impermeability and in vivo selectivity for the membrane-bound (CA IV) versus the cytosolic (CA I and CA II) isozymes. J Enzyme Inhib. 2000;15(4):381–401.
  • Scozzafava A, Briganti F, Ilies MA, et al. Carbonic anhydrase inhibitors: synthesis of membrane-impermeant low molecular weight sulfonamides possessing in vivo selectivity for the membrane-bound versus cytosolic isozymes. J Med Chem. 2000 Jan 27;43(2):292–300.
  • Akocak S, Alam MR, Shabana AM, et al. PEGylated bis-sulfonamide carbonic anhydrase inhibitors can efficiently control the growth of several carbonic anhydrase IX-expressing carcinomas. J Med Chem. 2016 May 26;59(10):5077–5088.
  • Maren TH, Conroy CW, Wynns GC, et al. Renal and cerebrospinal fluid formation pharmacology of a high molecular weight carbonic anhydrase inhibitor. J Pharmacol Exp Ther. 1997 Jan;280(1):98–104.
  • Supuran CT, Scozzafava A. Carbonic anhydrase inhibitors and their therapeutic potential. Expert Opin Ther Pat. 2000;10(5):575–600.
  • Nam SU, Noh JH, Kim BJ, et al. A marker for early diagnosis of acute myocardial infarction. KR2013141044. 2013.
  • Nishimori I, Miyaji E, Morimoto K, et al. Serum antibodies to carbonic anhydrase IV in patients with autoimmune pancreatitis. Gut. 2005 Feb;54(2):274–281.
  • Chawla LS, Mccaffrey TA, Mcpherson P, et al. Blood biomarkers for appendicitis and diagnostics methods using biomarkers. WO2016065202A1. 2016.
  • Nagao Y, Platero JS, Waheed A, et al. Human mitochondrial carbonic anhydrase: cDNA cloning, expression, subcellular localization, and mapping to chromosome 16. Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7623–7627.
  • Nagao Y, Batanian JR, Clemente MF, et al. Genomic organization of the human gene (CA5) and pseudogene for mitochondrial carbonic anhydrase V and their localization to chromosomes 16q and 16p. Genomics. 1995 Aug 10;28(3):477–484.
  • Dodgson SJ, Forster RE 2nd, Storey BT, et al. Mitochondrial carbonic anhydrase. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5562–5566.
  • Fujikawa-Adachi K, Nishimori I, Taguchi T, et al. Human mitochondrial carbonic anhydrase VB. cDNA cloning, mRNA expression, subcellular localization, and mapping to chromosome x. J Biol Chem. 1999 Jul 23;274(30):21228–21233.
  • Shah GN, Hewett-Emmett D, Grubb JH, et al. Mitochondrial carbonic anhydrase CA VB: differences in tissue distribution and pattern of evolution from those of CA VA suggest distinct physiological roles. Proc Natl Acad Sci U S A. 2000 Feb 15;97(4):1677–1682.
  • Shah GN, Rubbelke TS, Hendin J, et al. Targeted mutagenesis of mitochondrial carbonic anhydrases VA and VB implicates both enzymes in ammonia detoxification and glucose metabolism. Proc Natl Acad Sci U S A. 2013 Apr 30;110(18):7423–7428.
  • Ghandour MS, Parkkila AK, Parkkila S, et al. Mitochondrial carbonic anhydrase in the nervous system: expression in neuronal and glial cells. J Neurochem. 2000 Nov;75(5):2212–2220.
  • van Karnebeek CD, Sly WS, Ross CJ, et al. Mitochondrial carbonic anhydrase VA deficiency resulting from CA5A alterations presents with hyperammonemia in early childhood. Am J Hum Genet. 2014 Mar 6;94(3):453–461.
  • Scozzafava A, Supuran CT, Carta F. Antiobesity carbonic anhydrase inhibitors: a literature and patent review. Expert Opin Ther Pat. 2013;23(6):725–735.
  • Baine MJ, Chakraborty S, Smith LM, et al. Transcriptional profiling of peripheral blood mononuclear cells in pancreatic cancer patients identifies novel genes with potential diagnostic utility. PLoS One. 2011 Feb 10;6(2):e17014.
  • Baine MJ, Menning M, Smith LM, et al. Differential gene expression analysis of peripheral blood mononuclear cells reveals novel test for early detection of pancreatic cancer. Cancer Biomark. 2011;11(1):1–14.
  • Parkkila S, Parkkila AK, Vierjoki T, et al. Competitive time-resolved immunofluorometric assay for quantifying carbonic anhydrase VI in saliva. Clin Chem. 1993 Oct;39(10):2154–2157.
  • Borghi GN, Rodrigues LP, Lopes LM, et al. Relationship among alpha amylase and carbonic anhydrase VI in saliva, visible biofilm, and early childhood caries: a longitudinal study. Int J Paediatr Dent. 2017 May;27(3):174–182.
  • Zaidel L, Miller S, Carpentier G, et al. Diagnostic methods. WO2013095367. 2013.
  • Beckman KA, Luchs J, Milner MS. Making the diagnosis of Sjogren’s syndrome in patients with dry eye. Clin Ophthalmol. 2016;10:43–53.
  • Ambrus JL, Shen JL Method of diagnosing Sjogren’s disease. EP20110735215. 2011.
  • Ruusuvuori E, Kaila K. Carbonic anhydrases and brain pH in the control of neuronal excitability. Subcell Biochem. 2014;75:271–290.
  • Ruusuvuori E, Huebner AK, Kirilkin I, et al. Neuronal carbonic anhydrase VII provides GABAergic excitatory drive to exacerbate febrile seizures. Embo J. 2013 Aug 14;32(16):2275–2286.
  • Ruusuvuori E, Li H, Huttu K, et al. Carbonic anhydrase isoform VII acts as a molecular switch in the development of synchronous gamma-frequency firing of hippocampal CA1 pyramidal cells. J Neurosci. 2004 Mar 17;24(11):2699–2707.
  • Chu C-M, Chang Y Genetic marker for detecting colorectal cancer and method using the same. TW20130113645. 2013.
  • 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(29):3264–3276.
  • Aspatwar A, Tolvanen ME, Parkkila S. An update on carbonic anhydrase-related proteins VIII, X and XI. J Enzyme Inhib Med Chem. 2013 Dec;28(6):1129–1142.
  • Taniuchi K, Nishimori I, Takeuchi T, et al. Developmental expression of carbonic anhydrase-related proteins VIII, X, and XI in the human brain. Neuroscience. 2002;112(1):93–99.
  • Picaud SS, Muniz JR, Kramm A, et al. Crystal structure of human carbonic anhydrase-related protein VIII reveals the basis for catalytic silencing. Proteins. 2009 Aug 1;76(2):507–511.
  • Hirota J, Ando H, Hamada K, et al. Carbonic anhydrase-related protein is a novel binding protein for inositol 1,4,5-trisphosphate receptor type 1. Biochem J. 2003 Jun 1;372(Pt 2):435–441.
  • Akisawa Y, Nishimori I, Taniuchi K, et al. Expression of carbonic anhydrase-related protein CA-RP VIII in non-small cell lung cancer. Virchows Arch. 2003 Jan;442(1):66–70.
  • Turkmen S, Guo G, Garshasbi M, et al. CA8 mutations cause a novel syndrome characterized by ataxia and mild mental retardation with predisposition to quadrupedal gait. PLoS Genet. 2009 5;May(5):e1000487.
  • Kaya N, Aldhalaan H, Al-Younes B, et al. Phenotypical spectrum of cerebellar ataxia associated with a novel mutation in the CA8 gene, encoding carbonic anhydrase (CA) VIII. Am J Med Genet B Neuropsychiatr Genet. 2011 Dec;156B(7):826–834.
  • Bataller L, Sabater L, Saiz A, et al. Carbonic anhydrase-related protein VIII: autoantigen in paraneoplastic cerebellar degeneration. Ann Neurol. 2004 Oct;56(4):575–579.
  • Nishikata M, Nishimori I, Taniuchi K, et al. Carbonic anhydrase-related protein VIII promotes colon cancer cell growth. Mol Carcinog. 2007 Mar;46(3):208–214.
  • Hewett-Emmett D, Tashian RE. Functional diversity, conservation, and convergence in the evolution of the alpha-, beta-, and gamma-carbonic anhydrase gene families. Mol Phylogenet Evol. 1996 Feb;5(1):50–77.
  • Mikoshiba K, Okano H, Miyawaki A, et al. Molecular genetic analyses of myelin deficiency and cerebellar ataxia. Prog Brain Res. 1995;105:23–41.
  • Kilpinen S, Autio R, Ojala K, et al. Systematic bioinformatic analysis of expression levels of 17,330 human genes across 9,783 samples from 175 types of healthy and pathological tissues. Genome Biol. 2008;9(9):R139.
  • Morimoto K, Nishimori I, Takeuchi T, et al. Overexpression of carbonic anhydrase-related protein XI promotes proliferation and invasion of gastrointestinal stromal tumors. Virchows Arch. 2005 Jul;447(1):66–73.
  • Karjalainen SL, Haapasalo HK, Aspatwar A, et al. Carbonic anhydrase related protein expression in astrocytomas and oligodendroglial tumors. BMC Cancer. 2018 May 23;18(1):584.
  • Pastorek J, Pastorekova S. Hypoxia-induced carbonic anhydrase IX as a target for cancer therapy: from biology to clinical use. Semin Cancer Biol. 2015 Apr;31:52–64.
  • Alterio V, Hilvo M, Di Fiore A, et al. Crystal structure of the catalytic domain of the tumor-associated human carbonic anhydrase IX. Proc Natl Acad Sci U S A. 2009 Sep 22;106(38):16233–16238.
  • 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 Oct 10;283(41):27799–27809.
  • Ivanov S, Liao SY, Ivanova A, et al. Expression of hypoxia-inducible cell-surface transmembrane carbonic anhydrases in human cancer. Am J Pathol. 2001 Mar;158(3):905–919.
  • Zavada J, Zavadova Z, Pastorek J, et al. Human tumour-associated cell adhesion protein MN/CA IX: identification of M75 epitope and of the region mediating cell adhesion. Br J Cancer. 2000 Jun;82(11):1808–1813.
  • Gillies RJ, Gatenby RA. Metabolism and its sequelae in cancer evolution and therapy. Cancer J. 2015 Mar-Apr;21(2):88–96.
  • Sneddon D, Niemans R, Bauwens M, et al. Synthesis and in vivo biological evaluation of (68)ga-labeled carbonic anhydrase IX targeting small molecules for positron emission tomography. J Med Chem. 2016 Jul 14;59(13):6431–6443.
  • Mboge MY, Mahon BP, McKenna R, et al. Carbonic anhydrases: role in pH control and cancer. Metabolites. 2018 Feb 28;8(1):E19.
  • Damaghi M, Wojtkowiak JW, Gillies RJ. pH sensing and regulation in cancer. Front Physiol. 2013 Dec;17(4):370.
  • Svastova E, Hulikova A, Rafajova M, et al. Hypoxia activates the capacity of tumor-associated carbonic anhydrase IX to acidify extracellular pH. FEBS Lett. 2004 Nov 19;577(3):439–445.
  • Ilies MA, Vullo D, Pastorek J, et al. Carbonic anhydrase inhibitors. Inhibition of tumor-associated isozyme IX by halogenosulfanilamide and halogenophenylaminobenzolamide derivatives. J Med Chem. 2003 May 22;46(11):2187–2196.
  • Kanfar N, Tanc M, Dumy P, et al. Effective access to multivalent inhibitors of carbonic anhydrases promoted by peptide bioconjugation. Chemistry. 2017 May 17;23(28):6788–6794.
  • Lomelino C, McKenna R. Carbonic anhydrase inhibitors: a review on the progress of patent literature (2011–2016). Expert Opin Ther Pat. 2016 Aug;26(8):947–956.
  • Supuran CT, Winum JY. Carbonic anhydrase IX inhibitors in cancer therapy: an update. Future Med Chem. 2015;7(11):1407–1414.
  • Nocentini A, Supuran CT. Carbonic anhydrase inhibitors as antitumor/antimetastatic agents: a patent review (2008–2018). Expert Opin Ther Pat. 2018 Aug;9:1–12.
  • Benej M, Pastorekova S, Pastorek J. Carbonic anhydrase IX: regulation and role in cancer. Subcell Biochem. 2014;75:199–219.
  • Yang X, Minn I, Rowe SP, et al. Imaging of carbonic anhydrase IX with an 111In-labeled dual-motif inhibitor. Oncotarget. 2015 Oct 20;6(32):33733–33742.
  • Groves K, Bao B, Zhang J, et al. Synthesis and evaluation of near-infrared fluorescent sulfonamide derivatives for imaging of hypoxia-induced carbonic anhydrase IX expression in tumors. Bioorg Med Chem Lett. 2012 Jan 1;22(1):653–657.
  • Krall N, Pretto F, Mattarella M, et al. A 99mTc-labeled ligand of carbonic anhydrase IX selectively targets renal cell carcinoma in vivo. J Nucl Med. 2016 Jun;57(6):943–949.
  • Minn I, Koo SM, Lee HS, et al. [64Cu]XYIMSR-06: a dual-motif CAIX ligand for PET imaging of clear cell renal cell carcinoma. Oncotarget. 2016 Aug 30;7(35):56471–56479.
  • Hulick P, Zimmer M, Margulis V, et al. Blood levels of carbonic anhydrase 9 correlate with clear cell renal cell carcinoma activity. Clin Proteomics. 2009 March 01;5(1):37–45.
  • Pastorekova S, Zavadova Z, Kostal M, et al. A novel quasi-viral agent, MaTu, is a two-component system. Virology. 1992 Apr;187(2):620–626.
  • Genega EM, Ghebremichael M, Najarian R, et al. Carbonic anhydrase IX expression in renal neoplasms: correlation with tumor type and grade. Am J Clin Pathol. 2010 Dec;134(6):873–879.
  • Luong-Player A, Liu H, Wang HL, et al. Immunohistochemical reevaluation of carbonic anhydrase IX (CA IX) expression in tumors and normal tissues. Am J Clin Pathol. 2014 Feb;141(2):219–225.
  • Korkeila E, Talvinen K, Jaakkola PM, et al. Expression of carbonic anhydrase IX suggests poor outcome in rectal cancer. Br J Cancer. 2009 Mar 24;100(6):874–880.
  • Nakao M, Ishii G, Nagai K, et al. Prognostic significance of carbonic anhydrase IX expression by cancer-associated fibroblasts in lung adenocarcinoma. Cancer. 2009 Jun 15;115(12):2732–2743.
  • 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 May 25;102(11):1627–1635.
  • Kim JY, Lee SH, An S, et al. Carbonic anhydrase 9 expression in well-differentiated pancreatic neuroendocrine neoplasms might be associated with aggressive behavior and poor survival. Virchows Arch. 2018 May;472(5):739–748.
  • Hyrsl L, Zavada J, Zavadova Z, et al. Soluble form of carbonic anhydrase IX (CAIX) in transitional cell carcinoma of urinary tract. Neoplasma. 2009;56(4):298–302.
  • Chu X, Zhao P, Lv Y, et al. Expression of carbonic anhydrase-9 correlates with metastasis and prognosis of Chinese patients with invasive breast ductal carcinoma. Int J Clin Exp Pathol. 2016;9(2):1446–1452.
  • Tureci O, Sahin U, Vollmar E, et al. Human carbonic anhydrase XII: cDNA cloning, expression, and chromosomal localization of a carbonic anhydrase gene that is overexpressed in some renal cell cancers. Proc Natl Acad Sci U S A. 1998 Jun 23;95(13):7608–7613.
  • Whittington DA, Waheed A, Ulmasov B, et al. Crystal structure of the dimeric extracellular domain of human carbonic anhydrase XII, a bitopic membrane protein overexpressed in certain cancer tumor cells. Proc Natl Acad Sci U S A. 2001 Aug 14;98(17):9545–9550.
  • Waheed A, Sly WS. Carbonic anhydrase XII functions in health and disease. Gene. 2017 Aug 5;623:33–40.
  • Ivanov SV, Kuzmin I, Wei M-H, et al. Down-regulation of transmembrane carbonic anhydrases in renal cell carcinoma cell lines by wild-type von hippel-lindau transgenes. Proc Nat Acad Sci. 1998;95(21):12596–12601.
  • Ulmasov B, Waheed A, Shah GN, et al. Purification and kinetic analysis of recombinant CA XII, a membrane carbonic anhydrase overexpressed in certain cancers. Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14212–14217.
  • Parkkila S, Parkkila AK, Saarnio J, et al. Expression of the membrane-associated carbonic anhydrase isozyme XII in the human kidney and renal tumors. J Histochem Cytochem. 2000 Dec;48(12):1601–1608.
  • Parkkila S, Rajaniemi H, Parkkila A-K, et al. Carbonic anhydrase inhibitor suppresses invasion of renal cancer cells in vitro. Proc Nat Acad Sci. 2000;97(5):2220–2224.
  • Wykoff CC, Beasley NJP, Watson PH, et al. Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res. 2000;60(24):7075–7083.
  • Ondriskova E, Debreova M, Pastorekova S. Tumor-associated carbonic anhydrases IX and XII. In: Supuran CT, De Simone G, editors. Carbonic anhydrases as biocatalysts – from theory to medical and industrial applications. Amsterdam: Elsevier; 2015. p. 169–205.
  • Moon YR, Ji GY. Antibody binding to carbonic anhydrase and use thereof. US201615344764. 2016.
  • Watson PH, Chia SK, Wykoff CC, et al. Carbonic anhydrase XII is a marker of good prognosis in invasive breast carcinoma. Br J Cancer. 2003;88:1065.
  • Gruvberger S, Ringnér M, Chen Y, et al. Estrogen receptor status in breast cancer is associated with remarkably distinct gene expression patterns. Cancer Res. 2001;61(16):5979–5984.
  • Ilie MI, Hofman V, Ortholan C, et al. Overexpression of carbonic anhydrase XII in tissues from resectable non-small cell lung cancers is a biomarker of good prognosis. Int J Cancer. 2011 Apr 1;128(7):1614–1623.
  • Yoo CW, Nam BH, Kim JY, et al. Carbonic anhydrase XII expression is associated with histologic grade of cervical cancer and superior radiotherapy outcome. Radiat Oncol. 2010 Nov 1;5:101.
  • Lee S, Shin HJ, Han IO, et al. Tumor carbonic anhydrase 9 expression is associated with the presence of lymph node metastases in uterine cervical cancer. Cancer Sci. 2007 Mar;98(3):329–333.
  • Hynninen P, Vaskivuo L, Saarnio J, et al. Expression of transmembrane carbonic anhydrases IX and XII in ovarian tumours. Histopathology. 2006 Dec;49(6):594–602.
  • Kivela A, Parkkila S, Saarnio J, et al. Expression of a novel transmembrane carbonic anhydrase isozyme XII in normal human gut and colorectal tumors. Am J Pathol. 2000 Feb;156(2):577–584.
  • Saarnio J, Parkkila S, Parkkila AK, et al. Immunohistochemical study of colorectal tumors for expression of a novel transmembrane carbonic anhydrase, MN/CA IX, with potential value as a marker of cell proliferation. Am J Pathol. 1998 Jul;153(1):279–285.
  • Proescholdt MA, Mayer C, Kubitza M, et al. Expression of hypoxia-inducible carbonic anhydrases in brain tumors. Neuro Oncol. 2005 Oct;7(4):465–475.
  • 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 Apr;10(2):131–138.
  • Ochi F, Shiozaki A, Ichikawa D, et al. Carbonic anhydrase xii as an independent prognostic factor in advanced esophageal squamous cell carcinoma. J Cancer. 2015;6(10):922–929.
  • Lee M, Vecchio-Pagan B, Sharma N, et al. Loss of carbonic anhydrase XII function in individuals with elevated sweat chloride concentration and pulmonary airway disease. Hum Mol Genet. 2016 May 15;25(10):1923–1933.
  • Hong JH, Muhammad E, Zheng C, et al. Essential role of carbonic anhydrase XII in secretory gland fluid and HCO3(-) secretion revealed by disease causing human mutation. J Physiol. 2015 Dec 15;593(24):5299–5312.
  • Purkerson JM, Schwartz GJ. The role of carbonic anhydrases in renal physiology. Kidney Int. 2007 Jan;71(2):103–115.
  • Quinton PM. Role of epithelial HCO3(-) transport in mucin secretion: lessons from cystic fibrosis. Am J Physiol Cell Physiol. 2010 Dec;299(6):C1222–33.
  • Feldshtein M, Elkrinawi S, Yerushalmi B, et al. Hyperchlorhidrosis caused by homozygous mutation in CA12, encoding carbonic anhydrase XII. Am J Hum Genet. 2010 Nov 12;87(5):713–720.
  • Muhammad E, Leventhal N, Parvari G, et al. Autosomal recessive hyponatremia due to isolated salt wasting in sweat associated with a mutation in the active site of carbonic anhydrase 12. Hum Genet. 2011 Apr;129(4):397–405.
  • Lee MG, Ohana E, Park HW, et al. Molecular mechanism of pancreatic and salivary gland fluid and HCO3 secretion. Physiol Rev. 2012 Jan;92(1):39–74.
  • Maleth J, Hegyi P. Calcium signaling in pancreatic ductal epithelial cells: an old friend and a nasty enemy. Cell Calcium. 2014 Jun;55(6):337–345.
  • Almstahl A, Wikstrom M. Electrolytes in stimulated whole saliva in individuals with hyposalivation of different origins. Arch Oral Biol. 2003 May;48(5):337–344.
  • Power KA, Grad S, Rutges JP, et al. Identification of cell surface-specific markers to target human nucleus pulposus cells: expression of carbonic anhydrase XII varies with age and degeneration. Arthritis Rheum. 2011 Dec;63(12):3876–3886.
  • Richardson SM, Ludwinski FE, Gnanalingham KK, et al. Notochordal and nucleus pulposus marker expression is maintained by sub-populations of adult human nucleus pulposus cells through aging and degeneration. Sci Rep. 2017 May 4;7(1):1501.
  • Liao SY, Ivanov S, Ivanova A, et al. Expression of cell surface transmembrane carbonic anhydrase genes CA9 and CA12 in the human eye: overexpression of CA12 (CAXII) in glaucoma. J Med Genet. 2003 Apr;40(4):257–261.
  • Scozzafava A, Supuran CT. Glaucoma and the applications of carbonic anhydrase inhibitors. Subcell Biochem. 2014;75:349–359.
  • Mincione F, Scozzafava A, Supuran CT. The development of topically acting carbonic anhydrase inhibitors as anti-glaucoma agents. Curr Top Med Chem. 2007;7(9):849–854.
  • Baldwin JJ, Ponticello GS, Anderson PS, et al. Thienothiopyran-2-sulfonamides: novel topically active carbonic anhydrase inhibitors for the treatment of glaucoma. J Med Chem. 1989 Dec 01;32(12):2510–2513.
  • Lehtonen J, Shen B, Vihinen M, et al. Characterization of CA XIII, a novel member of the carbonic anhydrase isozyme family. J Biol Chem. 2004 Jan 23;279(4):2719–2727.
  • Di Fiore A, Monti SM, Hilvo M, et al. Crystal structure of human carbonic anhydrase XIII and its complex with the inhibitor acetazolamide. Proteins. 2009 Jan;74(1):164–175.
  • Hilvo M, Innocenti A, Monti SM, et al. Recent advances in research on the most novel carbonic anhydrases, CA XIII and XV. Curr Pharm Des. 2008;14(7):672–678.
  • Kummola L, Hamalainen JM, Kivela J, et al. Expression of a novel carbonic anhydrase, CA XIII, in normal and neoplastic colorectal mucosa. BMC Cancer. 2005 Apr 18;5:41.
  • Pertovaara M, Bootorabi F, Kuuslahti M, et al. Novel carbonic anhydrase autoantibodies and renal manifestations in patients with primary Sjogren’s syndrome. Rheumatology (Oxford). 2011 Aug;50(8):1453–1457.
  • Supuran CT, Scozzafava A. Carbonic anhydrases as targets for medicinal chemistry. Bioorg Med Chem. 2007 Jul 1;15(13):4336–4350.
  • Mori K, Ogawa Y, Ebihara K, et al. Isolation and characterization of CA XIV, a novel membrane-bound carbonic anhydrase from mouse kidney. J Biol Chem. 1999 May 28;274(22):15701–15705.
  • Kaunisto K, Parkkila S, Rajaniemi H, et al. Carbonic anhydrase XIV: luminal expression suggests key role in renal acidification. Kidney Int. 2002 Jun;61(6):2111–2118.
  • Nagelhus EA, Mathiisen TM, Bateman AC, et al. Carbonic anhydrase XIV is enriched in specific membrane domains of retinal pigment epithelium, Muller cells, and astrocytes. Proc Natl Acad Sci U S A. 2005 May 31;102(22):8030–8035.
  • Ogilvie JM, Ohlemiller KK, Shah GN, et al. Carbonic anhydrase XIV deficiency produces a functional defect in the retinal light response. Proc Natl Acad Sci U S A. 2007 May 15;104(20):8514–8519.
  • Parkkila S, Parkkila AK, Rajaniemi H, et al. Expression of membrane-associated carbonic anhydrase XIV on neurons and axons in mouse and human brain. Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):1918–1923.
  • Gao J, Aksoy BA, Dogrusoz U, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal. 2013 Apr 2;6(269):pl1.
  • Cerami E, Gao J, Dogrusoz U, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012 May;2(5):401–404.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.