Structural annotation of human carbonic anhydrases

Journal of Enzyme Inhibition and Medicinal Chemistry

Volumn 28, Issue 2, 2013, Pages 267-277

  Aggarwal, Mayank ^a   Boone, Christopher D ^a   Kondeti, Bhargav ^a   McKenna, Robert ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Annotation; Classification; Comparison; Human carbonic anhydrase; Industrial applications; Thermostability

Indexed keywords

CARBONATE DEHYDRATASE; CARBONATE DEHYDRATASE III; CARBONATE DEHYDRATASE IV; CARBONATE DEHYDRATASE IX; CARBONATE DEHYDRATASE VI; CARBONATE DEHYDRATASE VII; CARBONATE DEHYDRATASE X; CARBONATE DEHYDRATASE XI; CARBONATE DEHYDRATASE XII; CARBONATE DEHYDRATASE XIII; CARBONATE DEHYDRATASE XIV; PROTEIN; UNCLASSIFIED DRUG; ISOENZYME;

CATALYSIS; CRYSTAL STRUCTURE; CYTOSOL; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME STABILITY; ENZYME STRUCTURE; HUMAN; PHYSIOLOGICAL PROCESS; REVIEW; CHEMISTRY; ISOLATION AND PURIFICATION; METABOLISM; PROTEIN CONFORMATION;

CARBONIC ANHYDRASES; HUMANS; ISOENZYMES; PROTEIN CONFORMATION;

EID: 84875720899     PISSN: 14756366     EISSN: 14756374     Source Type: Journal    
DOI: 10.3109/14756366.2012.737323     Document Type: Review

References (110)

1. Messerchmidt A, Bode W, Cygler M. (2004). Handbook of Metalloproteins. West Sussex, England: John Wiley and Sons Ltd.
2. Domsic JF, Avvaru BS, Kim CU, Gruner SM, Agbandje-McKenna M, Silverman DN et al. Entrapment of carbon dioxide in the active site of carbonic anhydrase II. J Biol Chem 2008; 283: 30766-30771.
3. Supuran CT. Carbonic anhydrases-an overview. Curr Pharm Des 2008; 14: 603-614.
4. Scozzafava A, Mastrolorenzo A, Supuran CT. Carbonic anhydrase inhibitors and activators and their use in therapy. Expert Opinion on Therapeutic Patents 2006; 16: 1627-1664.
5. Supuran CT, Scozzafava A, Conway J. (2004). Carbonic anhydrase: its inhibitors and activators. Boca Raton, Florida (USA): CRC Press.
6. Pastorekova S, Parkkila S, Pastorek J, Supuran CT. Carbonic anhydrases: current state of the art, therapeutic applications and future prospects. J Enzyme Inhib Med Chem 2004; 19: 199-229.
7. Chegwidden WR, Carter ND. (2000). The carbonic anhydrases: new horizons. Birkhauser Verlag. Basel, Switzerland: Birkhauser.
8. Krishnamurthy VM, Kaufman GK, Urbach AR, Gitlin I, Gudiksen KL, Weibel DB et al. Carbonic anhydrase as a model for biophysical and physical-organic studies of proteins and protein-ligand binding. Chem Rev 2008; 108: 946-1051.
9. Supuran CT, Scozzafava A, Casini A. Carbonic anhydrase inhibitors. Med Res Rev 2003; 23: 146-189.
10. Nishimori I, Minakuchi T, Onishi S, Vullo D, Cecchi A, Scozzafava A et al. Carbonic anhydrase inhibitors: cloning, characterization, and inhibition studies of the cytosolic isozyme III with sulfonamides. Bioorg Med Chem 2007; 15: 7229-7236.
11. Vullo D, Franchi M, Gallori E, Antel J, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors. Inhibition of mitochondrial isozyme V with aromatic and heterocyclic sulfonamides. J Med Chem 2004; 47: 1272-1279.
12. Nishimori I, Vullo D, Innocenti A, Scozzafava A, Mastrolorenzo A, Supuran CT. Carbonic anhydrase inhibitors. The mitochondrial isozyme VB as a new target for sulfonamide and sulfamate inhibitors. J Med Chem 2005; 48: 7860-7866.
13. Nishimori I, Minakuchi T, Onishi S, Vullo D, Scozzafava A, Supuran CT. Carbonic anhydrase inhibitors. DNA cloning, characterization, and inhibition studies of the human secretory isoform VI, a new target for sulfonamide and sulfamate inhibitors. J Med Chem 2007; 50: 381-388.
14. Vullo D, Voipio J, Innocenti A, Rivera C, Ranki H, Scozzafava A et al. Carbonic anhydrase inhibitors. Inhibition of the human cytosolic isozyme VII with aromatic and heterocyclic sulfonamides. Bioorg Med Chem Lett 2005; 15: 971-976.
15. Vullo D, Franchi M, Gallori E, Pastorek J, Scozzafava A, Pastorekova S et al. Carbonic anhydrase inhibitors: inhibition of the tumor-associated isozyme IX with aromatic and heterocyclic sulfonamides. Bioorg Med Chem Lett 2003; 13: 1005-1009.
16. Vullo D, Innocenti A, Nishimori I, Pastorek J, Scozzafava A, Pastorekova S et al. Carbonic anhydrase inhibitors. Inhibition of the transmembrane isozyme XII with sulfonamides-a new target for the design of antitumor and antiglaucoma drugs? Bioorg Med Chem Lett 2005; 15: 963-969.
17. Nishimori I, Vullo D, Innocenti A, Scozzafava A, Mastrolorenzo A, Supuran CT. Carbonic anhydrase inhibitors: inhibition of the transmembrane isozyme XIV with sulfonamides. Bioorg Med Chem Lett 2005; 15: 3828-3833.
18. Lehtonen J, Shen B, Vihinen M, Casini A, Scozzafava A, Supuran CT et al. Characterization of CA XIII, a novel member of the carbonic anhydrase isozyme family. J Biol Chem 2004; 279: 2719-2727.
19. Supuran CT, Ilies MA, Scozzafava A. Carbonic anhydrase inhibitors - Part 29 1: Interaction of isozymes I, II and IV with benzolamidelike derivatives. Eur J Med Chem 1998; 33: 739-751.
20. Supuran CT, Scozzafava A, Ilies MA, Briganti F. 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 Enzym Inhib 2000; 15: 381-401.
21. Scozzafava A, Briganti F, Ilies MA, Supuran CT. 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; 43: 292-300.
22. Winum JY, Temperini C, El Cheikh K, Innocenti A, Vullo D, Ciattini S et al. Carbonic anhydrase inhibitors: clash with Ala65 as a means for designing inhibitors with low affinity for the ubiquitous isozyme II, exemplified by the crystal structure of the topiramate sulfamide analogue. J Med Chem 2006; 49: 7024-7031.
23. Saczewski F, Slawinski J, Kornicka A, Brzozowski Z, Pomarnacka E, Innocenti A et al. Carbonic anhydrase inhibitors. Inhibition of the cytosolic human isozymes I and II, and the transmembrane, tumor-associated isozymes IX and XII with substituted aromatic sulfonamides activatable in hypoxic tumors. Bioorg Med Chem Lett 2006; 16: 4846-4851.
24. De Simone G, Vitale RM, Di Fiore A, Pedone C, Scozzafava A, Montero JL et al. Carbonic anhydrase inhibitors: Hypoxiaactivatable sulfonamides incorporating disulfide bonds that target the tumor-associated isoform IX. J Med Chem 2006; 49: 5544-5551.
25. Kohler K, Hillebrecht A, Schulze Wischeler J, Innocenti A, Heine A, Supuran CT et al. Saccharin inhibits carbonic anhydrases: possible explanation for its unpleasant metallic aftertaste. Angew Chem Int Ed Engl 2007; 46: 7697-7699.
26. Liang JY, Lipscomb WN. Binding of substrate CO2 to the active site of human carbonic anhydrase II: a molecular dynamics study. Proc Natl Acad Sci USA 1990; 87: 3675-3679.
27. Lindskog S. Structure and mechanism of carbonic anhydrase. Pharmacol Ther 1997; 74: 1-20.
28. Avvaru BS, Kim CU, Sippel KH, Gruner SM, Agbandje-McKenna M, Silverman DN et al. A short, strong hydrogen bond in the active site of human carbonic anhydrase II. Biochemistry 2010; 49: 249-251.
29. Maupin CM, Castillo N, Taraphder S, Tu C, McKenna R, Silverman DN et al. Chemical rescue of enzymes: proton transfer in mutants of human carbonic anhydrase II. J Am Chem Soc 2011; 133: 6223-6234.
30. Shimahara H, Yoshida T, Shibata Y, Shimizu M, Kyogoku Y, Sakiyama F et al. Tautomerism of histidine 64 associated with proton transfer in catalysis of carbonic anhydrase. J Biol Chem 2007; 282: 9646-9656.
31. Fisher Z, Hernandez Prada JA, Tu C, Duda D, Yoshioka C, An H et al. Structural and kinetic characterization of active-site histidine as a proton shuttle in catalysis by human carbonic anhydrase II. Biochemistry 2005; 44: 1097-1105.
32. Elder I, Fisher Z, Laipis PJ, Tu C, McKenna R, Silverman DN. Structural and kinetic analysis of proton shuttle residues in the active site of human carbonic anhydrase III. Proteins 2007; 68: 337-343.
33. Duda DM, Tu C, Fisher SZ, An H, Yoshioka C, Govindasamy L et al. Human carbonic anhydrase III: structural and kinetic study of catalysis and proton transfer. Biochemistry 2005; 44: 10046-10053.
34. Boriack-Sjodin PA, Heck RW, Laipis PJ, Silverman DN, Christianson DW. Structure determination of murine mitochondrial carbonic anhydrase V at 2.45-A resolution: implications for catalytic proton transfer and inhibitor design. Proc Natl Acad Sci USA 1995; 92: 10949-10953.
35. Mitterberger MC, Kim G, Rostek U, Levine RL, Zwerschke W. Carbonic anhydrase III regulates peroxisome proliferatoractivated receptor-?2. Exp Cell Res 2012; 318: 877-886.
36. Imtaiyaz Hassan M, Shajee B, Waheed A, Ahmad F, Sly WS. Structure, function and applications of carbonic anhydrase isozymes. Bioorg Med Chem 2012 (In Press).
37. Pilka ES, Kochan G, Oppermann U, Yue WW. Crystal structure of the secretory isozyme of mammalian carbonic anhydrases CA VI: implications for biological assembly and inhibitor development. Biochem Biophys Res Commun 2012; 419: 485-489.
38. Di Fiore A, Monti SM, Hilvo M, Parkkila S, Romano V, Scaloni A et al. Crystal structure of human carbonic anhydrase XIII and its complex with the inhibitor acetazolamide. Proteins 2009; 74: 164-175.
39. Cianchi F, Vinci MC, Supuran CT, Peruzzi B, De Giuli P, Fasolis G et al. Selective inhibition of carbonic anhydrase IX decreases cell proliferation and induces ceramide-mediated apoptosis in human cancer cells. J Pharmacol Exp Ther 2010; 334: 710-719.
40. Nagelhus EA, Mathiisen TM, Bateman AC, Haug FM, Ottersen OP, Grubb JH et al. Carbonic anhydrase XIV is enriched in specific membrane domains of retinal pigment epithelium, Muller cells, and astrocytes. Proc Natl Acad Sci USA 2005; 102: 8030-8035.
41. Bergenhem NC, Hallberg M, Wisen S. Molecular characterization of the human carbonic anhydrase-related protein (HCA-RP VIII). Biochim Biophys Acta 1998; 1384: 294-298.
42. Tashian RE, Hewett-Emmett D, Carter N, Bergenhem NC. Carbonic anhydrase (CA)-related proteins (CA-RPs), and transmembrane proteins with CA or CA-RP domains. EXS 2000: 105-120.
43. Picaud SS, Muniz JR, Kramm A, Pilka ES, Kochan G, Oppermann U et al. Crystal structure of human carbonic anhydrase-related protein VIII reveals the basis for catalytic silencing. Proteins 2009; 76: 507-511.
44. Lakkis MM, Bergenhem NC, O'Shea KS, Tashian RE. Expression of the acatalytic carbonic anhydrase VIII gene, Car8, during mouse embryonic development. Histochem J 1997; 29: 135-141.
45. Hirota J, Ando H, Hamada K, Mikoshiba K. Carbonic anhydrase-related protein is a novel binding protein for inositol 1, 4, 5-trisphosphate receptor type 1. Biochem J 2003; 372: 435-441.
46. Bosanac I, Alattia JR, Mal TK, Chan J, Talarico S, Tong FK et al. Structure of the inositol 1, 4, 5-trisphosphate receptor binding core in complex with its ligand. Nature 2002; 420: 696-700.
47. Jiao Y, Yan J, Zhao Y, Donahue LR, Beamer WG, Li X et al. Carbonic anhydrase-related protein VIII deficiency is associated with a distinctive lifelong gait disorder in waddles mice. Genetics 2005; 171: 1239-1246.
48. Peles E, Schlessinger J, Grumet M. Multi-ligand interactions with receptor-like protein tyrosine phosphatase beta: implications for intercellular signaling. Trends Biochem Sci 1998; 23: 121-124.
49. Willuda J, Honegger A, Waibel R, Schubiger PA, Stahel R, Zangemeister-Wittke U et al. High thermal stability is essential for tumor targeting of antibody fragments: engineering of a humanized anti-epithelial glycoprotein-2 (epithelial cell adhesion molecule) single-chain Fv fragment. Cancer Res 1999; 59: 5758-5767.
50. Yao M, Bolen DW. How valid are denaturant-induced unfolding free energy measurements? Level of conformance to common assumptions over an extended range of ribonuclease A stability. Biochemistry 1995; 34: 3771-3781.
51. Samiotakis A, Homouz D, Cheung MS. Multiscale investigation of chemical interference in proteins. J Chem Phys 2010; 132: 175101.
52. Wang Q, Christiansen A, Samiotakis A, Wittung-Stafshede P, Cheung MS. Comparison of chemical and thermal protein denaturation by combination of computational and experimental approaches. II. J Chem Phys 2011; 135: 175102.
53. Stadie WC, O'Brien H. The catalysis of the hydration of carbon dioxide and dehydration of carbonic acid by an enzyme isolated from red blood cells. J Biol Chem 1933; 103: 521-529.
54. Jagannadham MV, Balasubramanian D. The molten globular intermediate form in the folding pathway of human carbonic anhydrase B. FEBS Lett 1985; 188: 326-330.
55. Carlsson U, Henderson LE, Lindskog S. Denaturation and reactivation of human carbonic anhydrases in guanidine hydrochloride and urea. Biochim Biophys Acta 1973; 310: 376-387.
56. Yazgan A, Henkens RW. Role of zinc (II) in the refolding of guanidine hydrochloride denatured bovine carbonic anhydrase. Biochemistry 1972; 11: 1314-1318.
57. Laurent G, Charrel M, Garcon D, Castay M, Marriq C, Derrien Y. [On the proteins accompanying human hemoglobin in its preparations. 3. Identification of proteins Y, X1 and X2 with erythrocyte carbonic anhydrases and unequal stability of these in an alkaline medium]. Bull Soc Chim Biol 1964; 46: 603-620.
58. Riddiford LM, Stellwagen RH, Mehta S, Edsall JT. Hydrogen ion equilibria of human carbonic anhydrases B and C. J Biol Chem 1965; 240: 3305-3316.
59. Svensson M, Jonasson P, Freskgard PO, Jonsson BH, Lindgren M, Martensson LG et al. Mapping the folding intermediate of human carbonic anhydrase II. Probing substructure by chemical reactivity and spin and fluorescence labeling of engineered cysteine residues. Biochemistry 1995; 34: 8606-8620.
60. Martensson LG, Jonsson BH, Andersson M, Kihlgren A, Bergenhem N, Carlsson U. Role of an evolutionarily invariant serine for the stability of human carbonic anhydrase II. Biochim Biophys Acta 1992; 1118: 179-186.
61. Martensson LG, Jonasson P, Freskgard PO, Svensson M, Carlsson U, Jonsson BH. Contribution of individual tryptophan residues to the fluorescence spectrum of native and denatured forms of human carbonic anhydrase II. Biochemistry 1995; 34: 1011-1021.
62. Fransson C, Freskgard PO, Herbertsson H, Johansson A, Jonasson P, Martensson LG et al. Cis-trans isomerization is rate-determining in the reactivation of denatured human carbonic anhydrase II as evidenced by proline isomerase. FEBS Lett 1992; 296: 90-94.
63. Tweedy NB, Nair SK, Paterno SA, Fierke CA, Christianson DW. Structure and energetics of a non-proline cis-peptidyl linkage in a proline-202->alanine carbonic anhydrase II variant. Biochemistry 1993; 32: 10944-10949.
64. Aronsson G, Martensson LG, Carlsson U, Jonsson BH. Folding and stability of the N-terminus of human carbonic anhydrase II. Biochemistry 1995; 34: 2153-2162.
65. Henkens RW, Kitchell BB, Lottich SC, Stein PJ, Williams TJ. Detection and characterization using circular dichroism and fluorescence spectroscopy of a stable intermediate conformation formed in the denaturation of bovine carbonic anhydrase with guanidinium chloride. Biochemistry 1982; 21: 5918-5923.
66. Carlsson U, Aasa R, Henderson LE, Jonsson BH, Lindskog S. Paramagnetic and fluorescent probes attached to "buried" sulfhydryl groups in human carbonic anhydrases. Application to inhibitor binding, denaturation and refolding. Eur J Biochem 1975; 52: 25-36.
67. Martensson LG, Jonsson BH, Freskgard PO, Kihlgren A, Svensson M, Carlsson U. Characterization of folding intermediates of human carbonic anhydrase II: probing substructure by chemical labeling of SH groups introduced by site-directed mutagenesis. Biochemistry 1993; 32: 224-231.
68. Carlsson U, Henderson LE, Nyman PO, Samuelsson T. Studies on the influence of carboxyl-terminal amino acid residues on the activity and stability of human erythrocyte carbonic anhydrase B. FEBS Lett 1974; 48: 167-171.
69. Avvaru BS, Busby SA, Chalmers MJ, Griffin PR, Venkatakrishnan B, Agbandje-McKenna M et al. Apo-human carbonic anhydrase II revisited: implications of the loss of a metal in protein structure, stability, and solvent network. Biochemistry 2009; 48: 7365-7372.
70. Hakansson K, Wehnert A, Liljas A. X-ray analysis of metalsubstituted human carbonic anhydrase II derivatives. Acta Crystallogr D Biol Crystallogr 1994; 50: 93-100.
71. Hunt JA, Ahmed M, Fierke CA. Metal binding specificity in carbonic anhydrase is influenced by conserved hydrophobic core residues. Biochemistry 1999; 38: 9054-9062.
72. Bergenhem N, Carlsson U, Lind G, Astrand IM. Denaturation and reactivation of bovine and human cobalt-carbonic anhydrases in guanidine hydrochloride. Acta Chem Scand, B, Org Chem Biochem 1983; 37: 244-246.
73. Boren K, Grankvist H, Hammarstrom P, Carlsson U. Reshaping the folding energy landscape by chloride salt: impact on molten-globule formation and aggregation behavior of carbonic anhydrase. FEBS Lett 2004; 566: 95-99.
74. Beychok S, Armstrong JM, Lindblow C, Edsall JT. Optil rotatory dispersion and circular dichroism of human carbonic anhydrases B and C. J Biol Chem 1966; 241: 5150-5160.
75. Wong KP, Hamlin LM. Acid denaturation of bovine carbonic anhydrase B. Biochemistry 1974; 13: 2678-2683.
76. Wong KP, Tanford C. Denaturation of bovine carbonic anhydrase B by guanidine hydrochloride. A process involving separable sequential conformational transitions. J Biol Chem 1973; 248: 8518-8523.
77. Riddiford LM. Acid difference spectra of human carbonic anhydrases. J Biol Chem 1965; 240: 168-172.
78. Boren K, Andersson P, Larsson M, Carlsson U. Characterization of a molten globule state of bovine carbonic anhydrase III: loss of asymmetrical environment of the aromatic residues has a profound effect on both the near- and far-UV CD spectrum. Biochim Biophys Acta 1999; 1430: 111-118.
79. Cabiscol E, Levine RL. Carbonic anhydrase III. Oxidative modification in vivo and loss of phosphatase activity during aging. J Biol Chem 1995; 270: 14742-14747.
80. Di Fiore A, Truppo E, Supuran CT, Alterio V, Dathan N, Bootorabi F et al. Crystal structure of the C183S/C217S mutant of human CA VII in complex with acetazolamide. Bioorg Med Chem Lett 2010; 20: 5023-5026.
81. Baranauskiene L, Matulis D. Intrinsic thermodynamics of ethoxzolamide inhibitor binding to human carbonic anhydrase XIII. BMC Biophys 2012; 5: 12.
82. Matulis D, Kranz JK, Salemme FR, Todd MJ. Thermodynamic stability of carbonic anhydrase: measurements of binding affinity and stoichiometry using ThermoFluor. Biochemistry 2005; 44: 5258-5266.
83. Fisher Z, Boone CD, Biswas SM, Venkatakrishnan B, Aggarwal M, Tu C et al. Kinetic and structural characterization of thermostabilized mutants of human carbonic anhydrase II. Protein Eng Des Sel 2012; 25: 347-355.
84. Stams T, Nair SK, Okuyama T, Waheed A, Sly WS, Christianson DW. Crystal structure of the secretory form of membrane-associated human carbonic anhydrase IV at 2.8-A resolution. Proc Natl Acad Sci USA 1996; 93: 13589-13594.
85. Whitney PL, Briggle TV. Membrane-associated carbonic anhydrase purified from bovine lung. J Biol Chem 1982; 257: 12056-12059.
86. Waheed A, Okuyama T, Heyduk T, Sly WS. Carbonic anhydrase IV: purification of a secretory form of the recombinant human enzyme and identification of the positions and importance of its disulfide bonds. Arch Biochem Biophys 1996; 333: 432-438.
87. Martensson LG, Karlsson M, Carlsson U. Dramatic stabilization of the native state of human carbonic anhydrase II by an engineered disulfide bond. Biochemistry 2002; 41: 15867-15875.
88. Alterio V, Hilvo M, Di Fiore A, Supuran CT, Pan P, Parkkila S et al. Crystal structure of the catalytic domain of the tumorassociated human carbonic anhydrase IX. Proc Natl Acad Sci USA 2009; 106: 16233-16238.
89. Whittington DA, Waheed A, Ulmasov B, Shah GN, Grubb JH, Sly WS 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 USA 2001; 98: 9545-9550.
90. Whittington DA, Grubb JH, Waheed A, Shah GN, Sly WS, Christianson DW. Expression, assay, and structure of the extracellular domain of murine carbonic anhydrase XIV: implications for selective inhibition of membrane-associated isozymes. J Biol Chem 2004; 279: 7223-7228.
91. Wykoff CC, Beasley NJ, Watson PH, Turner KJ, Pastorek J, Sibtain A et al. Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res 2000; 60: 7075-7083.
92. Andersson D, Hammarstrom P, Carlsson U. Cofactor-induced refolding: refolding of molten globule carbonic anhydrase induced by Zn(II) and Co(II). Biochemistry 2001; 40: 2653-2661.
93. Kannan KK, Ramanadham M, Jones TA. Structure, refinement, and function of carbonic anhydrase isozymes: refinement of human carbonic anhydrase I. Ann N Y Acad Sci 1984; 429: 49-60.
94. Aggarwal M, McKenna R. Update on carbonic anhydrase inhibitors: a patent review (2008 - 2011). Expert Opin Ther Pat 2012; 22: 903-915.
95. Supuran CT. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat Rev Drug Discov 2008; 7: 168-181.
96. Thiry A, Dogne JM, Masereel B, Supuran CT. Targeting tumorassociated carbonic anhydrase IX in cancer therapy. Trends Pharmacol Sci 2006; 27: 566-573.
97. Brahimi-Horn MC, Pouyssegur J. Oxygen, a source of life and stress. FEBS Lett 2007; 581: 3582-3591.
98. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME et al. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999; 399: 271-275.
99. Semenza GL. Hypoxia and cancer. Cancer Metastasis Rev 2007; 26: 223-224.
100. Hon WC, Wilson MI, Harlos K, Claridge TD, Schofield CJ, Pugh CW et al. Structural basis for the recognition of hydroxyproline in HIF-1 alpha by pVHL. Nature 2002; 417: 975-978.
101. Neri D, Supuran CT. Interfering with pH regulation in tumours as a therapeutic strategy. Nat Rev Drug Discov 2011; 10: 767-777.
102. Aggarwal M, Kondeti B, McKenna R. Insights towards sulfonamide drug specificity in a-carbonic anhydrases. Bioorg Med Chem 2012 (In Press).
103. Vullo D, De Luca V, Scozzafava A, Carginale V, Rossi M, Supuran CT et al. The first activation study of a bacterial carbonic anhydrase (CA). The thermostable a-CA from Sulfurihydrogenibium yellowstonense YO3AOP1 is highly activated by amino acids and amines. Bioorg Med Chem Lett 2012; 22: 6324-6327.
104. De Luca V, Vullo D, Scozzafava A, Carginale V, Rossi M, Supuran CT et al. Anion inhibition studies of an a-carbonic anhydrase from the thermophilic bacterium Sulfurihydrogenibium yellowstonense YO3AOP1. Bioorg Med Chem Lett 2012; 22: 5630-5634.
105. Fulke AB, Mudliar SN, Yadav R, Shekh A, Srinivasan N, Ramanan R et al. Bio-mitigation of CO(2), calcite formation and simultaneous biodiesel precursors production using Chlorella sp. Bioresour Technol 2010; 101: 8473-8476.
106. Ramanan R, Kannan K, Deshkar A, Yadav R, Chakrabarti T. Enhanced algal CO(2) sequestration through calcite deposition by Chlorella sp. and Spirulina platensis in a mini-raceway pond. Bioresour Technol 2010; 101: 2616-2622.
107. Hunt JA, Lesburg CA, Christianson DW, Thompson RB, Fierke CA. Active-site engineering of carbonic anhydrase and its application to biosensors. EXS 2000: 221-240.
108. Kanbar B, Ozdemir E. Thermal stability of carbonic anhydrase immobilized within polyurethane foam. Biotechnol Prog 2010; 26: 1474-1480.
109. Vinoba M, Lim KS, Lee SH, Jeong SK, Alagar M. Immobilization of human carbonic anhydrase on gold nanoparticles assembled onto amine/thiol-functionalized mesoporous SBA-15 for biomimetic sequestration of CO2. Langmuir 2011; 27: 6227-6234.
110. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC et al. UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 2004; 25: 1605-1612.