Transport activity of the sodium bicarbonate cotransporter NBCe1 is enhanced by different isoforms of carbonic anhydrase

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Schueler, Christina ^a   Becker, Holger M ^a   McKenna, Robert ^b   Deitmer, Joachim W ^a  

^a University of Koblenz Landau   (Germany)

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

Author keywords

[No Author keywords available]

Indexed keywords

BICARBONATE SODIUM COTRANSPORTER; BICARBONATE SODIUM COTRANSPORTER 1; CARBONATE DEHYDRATASE; CARBONATE DEHYDRATASE I; CARBONATE DEHYDRATASE II; CARBONATE DEHYDRATASE III; ETHOXZOLAMIDE; ISOENZYME; SODIUM; UNCLASSIFIED DRUG; CARBONATE DEHYDRATASE INHIBITOR; SLC4A4 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; DRUG SENSITIVITY; ENZYME ACTIVITY; FEMALE; IN VITRO STUDY; MOLECULAR INTERACTION; NONHUMAN; PH MEASUREMENT; PHARMACOLOGICAL BLOCKING; PROTEIN EXPRESSION; PROTEIN TRANSPORT; PROTON TRANSPORT; SHUTTLE VECTOR; SODIUM CELL LEVEL; XENOPUS LAEVIS; ANIMAL; CYTOLOGY; DRUG ANTAGONISM; ELECTROPHYSIOLOGY; GENETICS; HUMAN; METABOLISM; OOCYTE; PH; PLASMID; TRANSPORT AT THE CELLULAR LEVEL; WESTERN BLOTTING;

ANIMALS; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; CARBONIC ANHYDRASE I; CARBONIC ANHYDRASE II; CARBONIC ANHYDRASE III; CARBONIC ANHYDRASE INHIBITORS; ELECTROPHYSIOLOGY; ETHOXZOLAMIDE; FEMALE; HUMANS; HYDROGEN-ION CONCENTRATION; OOCYTES; PLASMIDS; SODIUM-BICARBONATE SYMPORTERS; XENOPUS LAEVIS;

EID: 80455150269     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0027167     Document Type: Article

References (60)

1. Luo J, Sun D, (2007) Physiology and pathophysiology of Na+/H+ exchange isoform 1 in the central nervous system. Curr Neurovasc Res 4: 205-215.
2. Romero MF, Fulton CM, Boron WF, (2004) The SLC4 family of HCO3- transporters. Pflugers Arch 447: 495-509.
3. Boron WF, Chen L, Parker MD, (2009) Modular structure of sodium-coupled bicarbonate transporters. J Exp Biol 212: 1697-1706.
4. Vince JW, Reithmeier RA, (1998) Carbonic anhydrase II binds to the carboxyl terminus of human band 3, the erythrocyte C1-/HCO3- exchanger. J Biol Chem 273: 28430-28437.
5. Sterling D, Reithmeier RA, Casey JR, (2001) Carbonic anhydrase: in the driver's seat for bicarbonate transport. J Pancreas 2: 165-170.
6. Li X, Alvarez B, Casey JR, Reithmeier RA, Fliegel L, (2002) Carbonic anhydrase II binds to and enhances activity of the Na+/H+ exchanger. J Biol Chem 277: 36085-36091.
7. Gross E, Pushkin A, Abuladze N, Fedotoff O, Kurtz I, (2002) Regulation of the sodium bicarbonate cotransporter kNBC1 function: role of Asp(986), Asp(988) and kNBC1-carbonic anhydrase II binding. J Physiol 544: 679-685.
8. Loiselle FB, Morgan PE, Alvarez BV, Casey JR, (2004) Regulation of the human NBC3 Na+/HCO3- cotransporter by carbonic anhydrase II and PKA. Am J Physiol Cell Physiol 286: 1423-1433.
9. Becker HM, Hirnet D, Fecher-Trost C, Sültemeyer D, Deitmer JW, (2005) Transport activity of MCT1 expressed in Xenopus oocytes is increased by interaction with carbonic anhydrase. J Biol Chem 280: 39882-39889.
10. Becker HM, Klier M, Deitmer JW, (2010) Nonenzymatic augmentation of lactate transport via monocarboxylate transporter isoform 4 by carbonic anhydrase II. J Membr Biol 234: 125-135.
11. Pushkin A, Abuladze N, Gross E, Newman D, Tatishchev S, et al. (2004) Molecular mechanism of kNBC1-carbonic anhydrase II interaction in proximal tubule cells. J Physiol 559: 55-65.
12. Becker HM, Deitmer JW, (2007) Carbonic anhydrase II increases the activity of the human electrogenic Na+/HCO3- cotransporter. J Biol Chem 282: 13508-13521.
13. Lu J, Daly CM, Parker MD, Gill HS, Piermarini PM, et al. (2006) Effect of human carbonic anhydrase II on the activity of the human electrogenic Na+/HCO3- cotransporter NBCe1-A in Xenopus oocytes. J Biol Chem 281: 19241-19250.
14. Yamada H, Horita S, Suzuki M, Fujita T, Seki G, (2011) Functional role of a putative carbonic anhydrase II-binding domain in the electrogenic Na (+)-HCO3 (-) cotransporter NBCe1 expressed in Xenopus oocytes. Channels (Austin) 5: 106-109.
15. Engberg P, Millqvist E, Pohl G, Lindskog S, (1985) Purification and some properties of carbonic anhydrase from bovine skeletal muscle. Arch Biochem Biophys 241: 628-638.
16. Kararli T, Silverman DN, (1985) Inhibition of the hydration of CO2 catalyzed by carbonic anhydrase III from cat muscle. J Biol Chem 260: 3484-3489.
17. Jewell DA, Tu CK, Paranawithana SR, Tanhauser SM, LoGrasso PV, et al. (1991) Enhancement of the catalytic properties of human carbonic anhydrase III by site-directed mutagenesis. Biochemistry 30: 1484-1490.
18. Behravan G, Jonasson P, Jonsson BH, Lindskog S, (1991) Structural and functional differences between carbonic anhydrase isoenzymes I and II as studied by site-directed mutagenesis. Eur J Biochem 198: 589-592.
19. Sly WS, Hu PY, (1995) Human carbonic anhydrases and carbonic anhydrase deficiencies. Annu Rev Biochem 64: 375-401.
20. Tu CK, Silverman DN, Forsman C, Jonsson BH, Lindskog S, (1989) Role of histidine 64 in the catalytic mechanism of human carbonic anhydrase II studied with a site-specific mutant. Biochemistry 28: 7913-7918.
21. Duda D, Tu C, Qian M, Laipis P, Agbandje-McKenna M, et al. (2001) Structural and kinetic analysis of the chemical rescue of the proton transfer function of carbonic anhydrase II. Biochemistry 40: 1741-1748.
22. Fisher Z, Hernandez Prada JA, Tu C, Duda D, Yoshioka C, et al. (2005) Structural and kinetic characterization of active-site histidine as a proton shuttle in catalysis by human carbonic anhydrase II. Biochemistry 44: 1097-1105.
23. Budayova-Spano M, Fisher SZ, Dauvergne MT, Agbandje-McKenna M, Silverman DN, et al. (2006) Production and X-ray crystallographic analysis of fully deuterated human carbonic anhydrase II. Acta Crystallogr Sect F Struct Biol Cryst Commun 62: 6-9.
24. Fisher SZ, Tu C, Bhatt D, Govindasamy L, Agbandje-McKenna M, et al. (2007) Speeding up proton transfer in a fast enzyme: kinetic and crystallographic studies on the effect of hydrophobic amino acid substitutions in the active site of human carbonic anhydrase II. Biochemistry 46: 3803-3813.
25. Maupin CM, Saunders MG, Thorpe IF, McKenna R, Silverman DN, et al. (2008) Origins of enhanced proton transport in the Y7F mutant of human carbonic anhydrase II. J Am Chem Soc 130: 11399-11408.
26. Becker HM, Klier M, Schüler C, McKenna R, Deitmer JW, (2011) Intramolecular proton shuttle supports not only catalytic but also noncatalytic function of carbonic anhydrase II. Proc Natl Acad Sci U S A 108: 3071-3076.
27. Vince JW, Reithmeier RA, (2000) Identification of the carbonic anhydrase II binding site in the Cl-/HCO3- anion exchanger AE1. Biochemistry 39: 5527-5533.
28. Alexander RS, Nair SK, Christianson DW, (1991) Engineering the hydrophobic pocket of carbonic anhydrase II. Biochemistry 30: 11064-11072.
29. Fierke CA, Calderone TL, Krebs JF, (1991) Functional consequences of engineering the hydrophobic pocket of carbonic anhydrase II. Biochemistry 30: 11054-11063.
30. An H, Tu C, Duda D, Montanez-Clemente I, Math K, et al. (2002) Chemical rescue in catalysis by human carbonic anhydrases II and III. Biochemistry 41: 3235-3242.
31. Deitmer JW, (1991) Electrogenic sodium-dependent bicarbonate secretion by glial cells of the leech central nervous system. J Gen Physiol 98: 637-655.
32. Wendel C, Becker HM, Deitmer JW, (2008) The sodium-bicarbonate cotransporter NBCe1 supports glutamine efflux via SNAT3 (SLC38A3) co-expressed in Xenopus oocytes. Pflugers Arch 455: 885-893.
33. Bröer S, Schneider HP, Bröer A, Rahman B, Hamprecht B, et al. (1998) Characterization of the monocarboxylate transporter 1 expressed in Xenopus laevis oocytes by changes in cytosolic pH. Biochem J 333: 167-174.
34. Becker HM, Bröer S, Deitmer JW, (2004) Facilitated lactate transport by MCT1 when coexpressed with the sodium bicarbonate cotransporter (NBC) in Xenopus oocytes. Biophys J 86: 235-247.
35. Silverman DN, (1982) Carbonic anhydrase: oxygen-18 exchange catalyzed by an enzyme with rate-contributing proton-transfer steps. Methods Enzymol 87: 732-752.
36. Sültemeyer DF, Fock HP, Canvin DT, (1990) Mass spectrometric measurement of intracellular carbonic anhydrase activity in high and low C(i) cells of Chlamydomonas: Studies Using O Exchange with C/O Labeled Bicarbonate. Plant Physiol 94: 1250-1257.
37. Badger MR, Price GD, (1989) Carbonic anhydrase activity associated with the Cyanobacterium Synechococcus PCC7942. Plant Physiol 89: 51-60.
38. Supuran CT, Casini A, Scozzafava A, (2004) Carbonic anhydrase: its inhibitors and activators Boca Raton CRC Press LLC pp. 67-149.
39. Behravan G, Jonsson BH, Lindskog S, (1990) Fine tuning of the catalytic properties of carbonic anhydrase. Studies of a Thr200----His variant of human isoenzyme II. Eur J Biochem 190: 351-357.
40. Briganti F, Mangani S, Orioli P, Scozzafava A, Vernaglione G, et al. (1997) Carbonic anhydrase activators: X-ray crystallographic and spectroscopic investigations for the interaction of isozymes I and II with histamine. Biochemistry 36: 10384-10392.
41. Eriksson AE, Liljas A, (1993) Refined structure of bovine carbonic anhydrase III at 2.0 A resolution. Proteins 16: 29-42.
42. Elder I, Fisher Z, Laipis PJ, Tu C, McKenna R, et al. (2007) Structural and kinetic analysis of proton shuttle residues in the active site of human carbonic anhydrase III. Proteins 68: 337-343.
43. LoGrasso PV, Tu CK, Jewell DA, Wynns GC, Laipis PJ, et al. (1991) Catalytic enhancement of human carbonic anhydrase III by replacement of phenylalanine-198 with leucine. Biochemistry 30: 8463-8470.
44. Tashian RE, (1989) The carbonic anhydrases: Widening perspectives on their evolution, expression and function. Bioessays 10: 186-192.
45. Becker HM, Deitmer JW, (2008) Nonenzymatic proton handling by carbonic anhydrase II during H+-lactate cotransport via monocarboxylate transporter 1. J Biol Chem 283: 21655-21667.
46. Scozzafava A, Supuran CT, (2002) Carbonic anhydrase activators: high affinity isozymes I, II, and IV activators, incorporating a beta-alanyl-histidine scaffold. J Med Chem 45: 284-291.
47. O'Dowd JJ, Robins DJ, Miller DJ, (1988) Detection, characterisation, and quantification of carnosine and other histidyl derivatives in cardiac and skeletal muscle. Biochim Biophys Acta 967: 241-249.
48. Vaughan-Jones RD, Peercy BE, Keener JP, Spitzer KW, (2002) Intrinsic H+ ion mobility in the rabbit ventricular myocyte. J Physiol 541: 139-158.
49. Swietach P, Camelliti P, Hulikova A, Kohl P, Vaughan-Jones RD, (2010) Spatial regulation of intracellular pH in multicellular strands of neonatal rat cardiomyocytes. Cardiovasc Res 85: 729-738.
50. Jonsson BH, Steiner H, Lindskog S, (1976) Participation of buffer in the catalytic mechanism of carbonic anhydrase. FEBS Lett 64: 310-314.
51. Tu CK, Paranawithana SR, Jewell DA, Tanhauser SM, LoGrasso PV, et al. (1990) Buffer enhancement of proton transfer in catalysis by human carbonic anhydrase III. Biochemistry 29: 6400-6405.
52. Weise A, Becker HM, Deitmer JW, (2007) Enzymatic suppression of the membrane conductance associated with the glutamine transporter SNAT3 expressed in Xenopus oocytes by carbonic anhydrase II. J Gen Physiol 130: 203-215.
53. Weise A, Schneider HP, McKenna R, Deitmer JW, (2011) Substrate-dependent interference of carbonic anhydrases with the glutamine transporter SNAT3-induced conductance. Cell Physiol Biochem 27: 79-90.
54. Vince JW, Carlsson U, Reithmeier RA, (2000) Localization of the Cl-/HCO3- anion exchanger binding site to the amino-terminal region of carbonic anhydrase II. Biochemistry 39: 13344-13349.
55. Piermarini PM, Kim EY, Boron WF, (2007) Evidence against a direct interaction between intracellular carbonic anhydrase II and pure C-terminal domains of SLC4 bicarbonate transporters. J Biol Chem 282: 1409-1421.
56. Lönnerholm G, Selking O, Wistrand PJ, (1985) Amount and distribution of carbonic anhydrases CA I and CA II in the gastrointestinal tract. Gastroenterology 88: 1151-1161.
57. Gramlich TL, Hennigar RA, Spicer SS, Schulte BA, (1990) Immunohistochemical localization of sodium-potassium-stimulated adenosine triphosphatase and carbonic anhydrase in human colon and colonic neoplasms. Arch Pathol Lab Med 114: 415-419.
58. Jeffery S, Edwards Y, Carter N, (1980) Distribution of CAIII in fetal and adult human tissue. Biochem Genet 18: 843-849.
59. Yu H, Riederer B, Stieger N, Boron WF, Shull GE, et al. (2009) Secretagogue stimulation enhances NBCe1 (electrogenic Na(+)/HCO(3)(-) cotransporter) surface expression in murine colonic crypts. Am J Physiol Gastrointest Liver Physiol 297: 1223-1231.
60. Kristensen JM, Kristensen M, Juel C, (2004) Expression of Na+/HCO3- co-transporter proteins (NBCs) in rat and human skeletal muscle. Acta Physiol Scand 182: 69-76.