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Expression, assay, and structure of the extracellular domain of murine carbonic anhydrase XIV: implications for selective inhibition of membrane-associated isozymes.

Whittington DA, Grubb JH, Waheed A, Shah GN, Sly WS, Christianson DW
J Biol Chem 279 7223-8 (2004)
Cited: 63 times
EuropePMC logo PMID: 14660577

Abstract

Carbonic anhydrase (CA) XIV is the most recently identified mammalian carbonic anhydrase isozyme, and its presence has been demonstrated in a number of tissues. Full-length CA XIV is a transmembrane protein composed of an extracellular catalytic domain, a single transmembrane helix, and a short intracellular polypeptide segment. The amino acid sequence identity of human CA XIV relative to the other membrane-associated isozymes (CA IV, CA IX, and CA XII) is 34-46%. We report here the expression and purification of both the full-length enzyme and a truncated, secretory form of murine CA XIV. Both forms of this isozyme are highly active, and both show an abrogation of activity in the presence of 0.2% SDS, in contrast to the behavior of murine CA IV. We also report the crystal structure of the extracellular domain of murine CA XIV at 2.8 A resolution and of an enzyme-acetazolamide complex at 2.9 A resolution. The structure shows a monomeric glycoprotein with a topology similar to that of other mammalian CA isozymes. Based on the x-ray crystallographic results, we compare and contrast known structures of membrane-associated CA isozymes to rationalize the structural elements responsible for the SDS resistance of CA IV and to discuss prospects for the design of selective inhibitors of membrane-associated CA isozymes.

Reviews - 1rj5 mentioned but not cited (1)

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Articles - 1rj5 mentioned but not cited (4)

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Reviews citing this publication (16)

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Articles citing this publication (42)

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  2. The protein tyrosine phosphatases PTPRZ and PTPRG bind to distinct members of the contactin family of neural recognition molecules. Bouyain S, Watkins DJ. Proc Natl Acad Sci U S A 107 2443-2448 (2010)
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  4. Sulfonamides incorporating 1,3,5-triazine moieties selectively and potently inhibit carbonic anhydrase transmembrane isoforms IX, XII and XIV over cytosolic isoforms I and II: Solution and X-ray crystallographic studies. Carta F, Garaj V, Maresca A, Wagner J, Avvaru BS, Robbins AH, Scozzafava A, McKenna R, Supuran CT. Bioorg Med Chem 19 3105-3119 (2011)
  5. X-ray structure of the first `extremo-α-carbonic anhydrase', a dimeric enzyme from the thermophilic bacterium Sulfurihydrogenibium yellowstonense YO3AOP1. Di Fiore A, Capasso C, De Luca V, Monti SM, Carginale V, Supuran CT, Scozzafava A, Pedone C, Rossi M, De Simone G. Acta Crystallogr D Biol Crystallogr 69 1150-1159 (2013)
  6. Crystal structure of human carbonic anhydrase XIII and its complex with the inhibitor acetazolamide. Di Fiore A, Monti SM, Hilvo M, Parkkila S, Romano V, Scaloni A, Pedone C, Scozzafava A, Supuran CT, De Simone G. Proteins 74 164-175 (2009)
  7. Carbonic anhydrase activators: the first X-ray crystallographic study of an adduct of isoform I. Temperini C, Scozzafava A, Supuran CT. Bioorg Med Chem Lett 16 5152-5156 (2006)
  8. Carbonic anhydrase activators: L-Adrenaline plugs the active site entrance of isozyme II, activating better isoforms I, IV, VA, VII, and XIV. Temperini C, Innocenti A, Scozzafava A, Mastrolorenzo A, Supuran CT. Bioorg Med Chem Lett 17 628-635 (2007)
  9. Structural study of interaction between brinzolamide and dorzolamide inhibition of human carbonic anhydrases. Pinard MA, Boone CD, Rife BD, Supuran CT, McKenna R. Bioorg Med Chem 21 7210-7215 (2013)
  10. Carbonic anhydrase XIV is enriched in specific membrane domains of retinal pigment epithelium, Muller cells, and astrocytes. Nagelhus EA, Mathiisen TM, Bateman AC, Haug FM, Ottersen OP, Grubb JH, Waheed A, Sly WS. Proc Natl Acad Sci U S A 102 8030-8035 (2005)
  11. Crystal structure of the most catalytically effective carbonic anhydrase enzyme known, SazCA from the thermophilic bacterium Sulfurihydrogenibium azorense. De Simone G, Monti SM, Alterio V, Buonanno M, De Luca V, Rossi M, Carginale V, Supuran CT, Capasso C, Di Fiore A. Bioorg Med Chem Lett 25 2002-2006 (2015)
  12. Autoimmunity against carbonic anhydrase II affects retinal cell functions in autoimmune retinopathy. Adamus G, Karren L. J Autoimmun 32 133-139 (2009)
  13. Carbonic anhydrase activators: activation of the human isoforms VII (cytosolic) and XIV (transmembrane) with amino acids and amines. Vullo D, Innocenti A, Nishimori I, Scozzafava A, Kaila K, Supuran CT. Bioorg Med Chem Lett 17 4107-4112 (2007)
  14. Carbonic anhydrase activators: the first activation study of the human secretory isoform VI with amino acids and amines. Nishimori I, Onishi S, Vullo D, Innocenti A, Scozzafava A, Supuran CT. Bioorg Med Chem 15 5351-5357 (2007)
  15. Carbonic anhydrase activators: an activation study of the human mitochondrial isoforms VA and VB with amino acids and amines. Vullo D, Nishimori I, Innocenti A, Scozzafava A, Supuran CT. Bioorg Med Chem Lett 17 1336-1340 (2007)
  16. Carbonic anhydrase gene expression in CA II-deficient (Car2-/-) and CA IX-deficient (Car9-/-) mice. Pan P, Leppilampi M, Pastorekova S, Pastorek J, Waheed A, Sly WS, Parkkila S. J Physiol 571 319-327 (2006)
  17. Carbonic anhydrase XIV identified as the membrane CA in mouse retina: strong expression in Müller cells and the RPE. Ochrietor JD, Clamp MF, Moroz TP, Grubb JH, Shah GN, Waheed A, Sly WS, Linser PJ. Exp Eye Res 81 492-500 (2005)
  18. Structural studies of β-carbonic anhydrase from the green alga Coccomyxa: inhibitor complexes with anions and acetazolamide. Huang S, Hainzl T, Grundström C, Forsman C, Samuelsson G, Sauer-Eriksson AE. PLoS One 6 e28458 (2011)
  19. Structural analysis of charge discrimination in the binding of inhibitors to human carbonic anhydrases I and II. Srivastava DK, Jude KM, Banerjee AL, Haldar M, Manokaran S, Kooren J, Mallik S, Christianson DW. J Am Chem Soc 129 5528-5537 (2007)
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  21. Accumulation and distribution of doxorubicin in tumour spheroids: the influence of acidity and expression of P-glycoprotein. Mellor HR, Callaghan R. Cancer Chemother Pharmacol 68 1179-1190 (2011)
  22. Carbonic anhydrase inhibitors. Inhibition of transmembrane isozymes XII (cancer-associated) and XIV with anions. Innocenti A, Vullo D, Pastorek J, Scozzafava A, Pastorekova S, Nishimori I, Supuran CT. Bioorg Med Chem Lett 17 1532-1537 (2007)
  23. Carbonic anhydrase inhibitors. Inhibition studies of the human secretory isoform VI with anions. Nishimori I, Innocenti A, Vullo D, Scozzafava A, Supuran CT. Bioorg Med Chem Lett 17 1037-1042 (2007)
  24. Computational modeling of laminin N-terminal domains using sparse distance constraints from disulfide bonds and chemical cross-linking. Kalkhof S, Haehn S, Paulsson M, Smyth N, Meiler J, Sinz A. Proteins 78 3409-3427 (2010)
  25. Expression of membrane-associated carbonic anhydrase isoforms IV, IX, XII, and XIV in the rabbit: induction of CA IV and IX during maturation. Purkerson JM, Schwartz GJ. Am J Physiol Regul Integr Comp Physiol 288 R1256-63 (2005)
  26. Carbonic anhydrase inhibitors: inhibition of the cytosolic human isozyme VII with anions. Vullo D, Ruusuvuori E, Kaila K, Scozzafava A, Supuran CT. Bioorg Med Chem Lett 16 3139-3143 (2006)
  27. The structural comparison between membrane-associated human carbonic anhydrases provides insights into drug design of selective inhibitors. Alterio V, Pan P, Parkkila S, Buonanno M, Supuran CT, Monti SM, De Simone G. Biopolymers 101 769-778 (2014)
  28. NMDA receptor-dependent afterdepolarizations are curtailed by carbonic anhydrase 14: regulation of a short-term postsynaptic potentiation. Makani S, Chen HY, Esquenazi S, Shah GN, Waheed A, Sly WS, Chesler M. J Neurosci 32 16754-16762 (2012)
  29. The first example of a significant active site conformational rearrangement in a carbonic anhydrase-inhibitor adduct: the carbonic anhydrase I-topiramate complex. Alterio V, Monti SM, Truppo E, Pedone C, Supuran CT, De Simone G. Org Biomol Chem 8 3528-3533 (2010)
  30. Exploration of the binding mode of indanesulfonamides as selective inhibitors of human carbonic anhydrase type VII by targeting Lys 91. Thiry A, Masereel B, Dogné JM, Supuran CT, Wouters J, Michaux C. ChemMedChem 2 1273-1280 (2007)
  31. Expression of cancer-related carbonic anhydrases IX and XII in normal skin and skin neoplasms. Syrjänen L, Luukkaala T, Leppilampi M, Kallioinen M, Pastorekova S, Pastorek J, Waheed A, Sly WS, Parkkila S, Karttunen T. APMIS 122 880-889 (2014)
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  34. pH-controlled histone acetylation amplifies melanocyte differentiation downstream of MITF. Raja DA, Gotherwal V, Burse SA, Subramaniam YJ, Sultan F, Vats A, Gautam H, Sharma B, Sharma S, Singh A, Sivasubbu S, Gokhale RS, Natarajan VT. EMBO Rep 21 e48333 (2020)
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  36. Carbonic anhydrase activators. Activation of the membrane-associated isoform XV with amino acids and amines. Innocenti A, Hilvo M, Parkkila S, Scozzafava A, Supuran CT. Bioorg Med Chem Lett 19 3430-3433 (2009)
  37. Basolateral carbonic anhydrase IV in the proximal tubule is a glycosylphosphatidylinositol-anchored protein. Purkerson JM, Kittelberger AM, Schwartz GJ. Kidney Int 71 407-416 (2007)
  38. Carbonic anhydrase inhibitors. Inhibition of red blood cell ostrich (Struthio camelus) carbonic anhydrase with a series of aromatic and heterocyclic sulfonamides. Ozensoy O, Isik S, Arslan O, Arslan M, Scozzafava A, Supuran CT. J Enzyme Inhib Med Chem 20 383-387 (2005)
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  40. Loss of luminal carbonic anhydrase XIV results in decreased biliary bicarbonate output, liver fibrosis, and cholangiocyte proliferation in mice. Zhou Z, Qian J, Kini A, Riederer B, Römermann D, Gros G, Seidler U. Pflugers Arch 474 529-539 (2022)
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