Type IV carbonic anhydrase is present in the gills of spiny dogfish (Squalus acanthias)

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 292, Issue 1, 2007, Pages

  Gilmour, K M ^a,b   Bayaa, M ^a   Kenney, L ^a   McNeill, B ^a   Perry, S F ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Carbon dioxide excretion; Gill

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); AMINO ACID DERIVATIVE; BICARBONATE; CARBON DIOXIDE; CARBONATE DEHYDRATASE IV; COMPLEMENTARY DNA; MESSENGER RNA; POLYCLONAL ANTIBODY;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CATALYSIS; CELL MEMBRANE; DEHYDRATION; DOGFISH; GILL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REAL TIME POLYMERASE CHAIN REACTION;

AMINO ACID SEQUENCE; ANIMALS; BLOTTING, WESTERN; CARBONIC ANHYDRASE IV; CLONING, MOLECULAR; DNA, COMPLEMENTARY; GILLS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MOLECULAR SEQUENCE DATA; PHYLOGENY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SQUALUS; TISSUE DISTRIBUTION;

EID: 33846170889     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00477.2006     Document Type: Article

References (74)

1. Baird TT, Waheed A, Okuyama T, Sly WS, and Fierke CA. Catalysis and inhibition of human carbonic anhydrase IV. Biochemistry 36: 2669-2678, 1997.
2. 2 exchange in vivo. J Appl Physiol 70: 1686-1699, 1991.
3. + reactions: theory. J Appl Physiol 71: 1460-1468, 1991.
4. Brown D, Zhu XL, and Sly WS. Localization of membrane-associated carbonic anhydrase type IV in kidney epithelial cells. Proc Natl Acad Sci USA 87: 7457-7461, 1990.
5. 2 excretion and intravascular pH disequilibria during carbonic anhydrase inhibition. J Appl Physiol 84: 683-694, 1998.
6. 2 transfer: theory. J Appl Physiol 50: 265-271, 1981.
7. Esbaugh A, Lund SG, and Tufts BL. Comparative physiology and molecular analysis of carbonic anhydrase from the red blood cells of teleost fish. J Comp Physiol [B] 174: 429-438, 2004.
8. Esbaugh A, Perry SF, Bayaa M, Georgalis T, Nickerson JG, Tufts BL, and Gilmour KM. Cytoplasmic carbonic anhydrase isozymes in rainbow trout Oncorhynchus mykiss: comparative physiology and molecular evolution. J Exp Biol 208: 1951-1961, 2005.
9. Esbaugh A and Tufts BL.The structure and function of carbonic anhydrase isozymes in the respiratory system of vertebrates. Respir Physiol Neurobiol. In press.
10. Esbaugh A and Tufts BL. Tribute to R. G. Boutilier: evidence of a high activity carbonic anhydrase isozyme in the red blood cells of an ancient vertebrate, the sea lamprey Petromyzon marinus. J Exp Biol 209: 1169-1178, 2006.
11. Fleming RE, Crouch EC, Ruzicka CA, and Sly WS. Pulmonary carbonic anhydrase IV: developmental regulation and cell-specific expression in the capillary endothelium. Am J Physiol Lung Cell Mol Physiol 265: L627-L635, 1993.
12. Georgalis T, Gilmour KM, Yorston J, and Perry SF. The roles of cytosolic and membrane bound carbonic anhydrase in the renal control of acid-base balance in rainbow trout Oncorhynchus mykiss. Am J Physiol Renal Physiol 291: F407-F421, 2006.
13. Gervais MR and Tufts BL. Evidence for membrane-bound carbonic anhydrase in the air bladder of bowfin (Amia calva), a primitive air-breathing fish. J Exp Biol 201: 2205-2212, 1998.
14. Gilmour KM, Henry RP, Wood CM, and Perry SF. Extracellular carbonic anhydrase and an acid-base disequilibrium in the blood of the dogfish, Squalus acanthias. J Exp Biol 200: 173-183, 1997.
15. 2 excretion in severely anemic dogfish. Am J Physiol Regul Integr Comp Physiol 286: R1138-R1148, 2004.
16. 2 excretion. Physiol Biochem Zool 74: 477-492, 2001.
17. Gilmour KM, Shah B, and Szebedinszky C. An investigation of carbonic anhydrase activity in the gills and blood plasma of brown bullhead (Ameiurus nebulosus), longnose skate (Raja rhina), and spotted ratfish (Hydrolagus colliei). J Comp Physiol [B] 172: 77-86, 2002.
18. Heming TA, Vanoye CG, Stabenau EK, Roush ED, Fierke CA, and Bidani A. Inhibitor sensitivity of pulmonary vascular carbonic anhydrase. J Appl Physiol 75: 1642-1649, 1993.
19. Henry RP, Gilmour KM, Wood CM, and Perry SF. Extracellular carbonic anhydrase activity and carbonic anhydrase inhibitors in the circulatory system of fish. Physiol Zool 70: 650-659, 1997.
20. Henry RP, Smatresk NJ, and Cameron JN. The distribution of branchial carbonic anhydrase and the effects of gill and erythrocyte carbonic anhydrase inhibition in the channel catfish Ictalurus punctatus. J Exp Biol 134: 201-218, 1988.
21. Henry RP and Swenson ER. The distribution and physiological significance of carbonic anhydrase in vertebrate gas exchange organs. Respir Physiol 121: 1-12, 2000.
22. Henry RP, Tufts BL, and Boutilier RG. The distribution of carbonic anhydrase type I and II isozymes in lamprey and trout: possible co-evolution with erythrocyte chloride/bicarbonate exchange. J Comp Physiol [B] 163: 380-388, 1993.
23. Hewett-Emmett D and Tashian RE. Functional diversity, conservation, and convergence in the evolution of the α-, β-, and γ-carbonic anhydrase gene families. Mol Phylogenet Evol 5: 50-77, 1996.
24. Hill EP. Inhibition of carbonic anhydrase by plasma of dogs and rabbits. J Appl Physiol 60: 191-197, 1986.
25. Lacy ER. Carbonic anhydrase localization in the elasmobranch rectal gland. J Exp Zool 226: 163-169, 1983.
26. Laurent P. Gill internal morphology. In: Fish Physiology, edited by Hoar WS and Randall DJ. London: Academic, 1984, p. 73-183.
27. Laurent P and Dunel S. Morphology of gill epithelia in fish. Am J Physiol Regul Integr Comp Physiol 238: R147-R159, 1980.
28. Lenfant C and Johansen K. Respiratory function in the elasmobranch Squalus suckleyi G. Respir Physiol 1: 13-29, 1966.
29. Lindskog S. Structure and mechanism of carbonic anhydrase. Pharmacol Ther 74: 1-20, 1997.
30. Lindskog S and Silverman DN. The catalytic mechanism of mammalian carbonic anhydrases. In: The Carbonic Anhydrases: New Horizons, edited by Chegwidden WR, Carter ND, and Edwards YH. Basel, Switzerland: Birkhäuser Verlag, 2000, p. 175-195.
31. Maren TH, Friedland BR, and Rittmaster RS. Kinetic properties of primitive vertebrate carbonic anhydrases. Comp Biochem Physiol 67B: 69-74, 1980.
32. Okuyama T, Sato S, Zhu XL, Waheed A, and Sly WS. Human carbonic anhydrase IV: cDNA cloning, sequence comparison, and expression in COS cell membranes. Proc Natl Acad Sci USA 89: 1315-1319, 1992.
33. Okuyama T, Waheed A, Kusumoto W, Zhu XL, and Sly WS. Carbonic anhydrase IV: role of removal of C-terminal domain in glycosylphosphatidylinositol anchoring and realization of enzyme activity. Arch Biochem Biophys 320: 315-322, 1995.
34. Olson KR. Vascular anatomy of the fish gill. J Exp Zool 293: 214-231, 2002.
35. Parkkila S. An overview of the distirbution and function of carbonic anhydrase in mammals. EXS 90: 79-93, 2000.
36. Pastoreková S, Parkkila S, Pastorek J, and Supuran CT. Carbonic anhydrases: current state of the art, therapeutic applications and future prospects. J Enzyme Inhib Med Chem 19: 199-229, 2004.
37. Perry SF, Gilmour KM, Bernier NJ, and Wood CM. Does gill boundary layer carbonic anhydrase contribute to carbon dioxide excretion: a comparison between dogfish (Squalus acanthias) and rainbow trout (Oncorhynchus mykiss). J Exp Biol 202: 749-756, 1999.
38. Piermarini PM, Verlander JW, Royauz IE, and Evans DH. Pendrin immunoreactivity in the gill epithelium of a euryhaline elasmobranch. Am J Physiol Regul Integr Comp Physiol 283: R983-R992, 2002.
39. Rispens P, Hessels J, Zwart A, and Zijlstra WG. Inhibition of carbonic anhydrase in dog plasma. Pflügers Arch 403: 344-347, 1985.
40. Roush ED and Fierke CA. Purification and characterization of a carbonic anhydrase II inhibitor from porcine plasma. Biochemistry 31: 12536-12542, 1992.
41. Saitou N and Nei M. The neighbour-joining method: a new method for constructing phylogenetic trees. Mol Biol Evol 4: 405-425, 1987.
42. Schwartz GJ. Physiology and molecular biology of renal carbonic anhydrase. J Nephrol 15: S61-S74, 2002.
43. Sender S, Böttcher K, Cetin Y, and Gros G. Carbonic anhydrase in the gills of seawater- and freshwater-acclimated flounders Platichthys flesus: purification, characterization, and immunohistochemical localization. J Histochem Cytochem 47: 43-50, 1999.
44. Shah GN, Ulmasov B, Waheed A, Becker T, Makani S, Svichar N, Chesler M, and Sly WS. Carbonic anhydrase IV and XIV knockout mice: roles of the respective carbonic anhydrases in buffering the extracellular space in brain. Proc Natl Acad Sci USA 102: 16771-16776, 2005.
45. Shuttleworth TJ. Salt and water balance: extrarenal mechanisms. In: Physiology of Elasmobranch Fishes, edited by Shuttleworth TJ. Berlin: Springer-Verlag, 1988, p. 171-199.
46. Silva P, Solomon RJ, and Epstein FH. Transport mechanisms that mediate the secretion of chloride by the rectal gland of Squalus acanthias. J Exp Zool 279: 504-508, 1997.
47. 2 transport to tumor markers. EXS 90: 95-104, 2000.
48. Stams T and Christianson DW. X-ray crystallographic studies of mammalian carbonic anhydrase isozymes. In: The Carbonic Anhydrases: New Horizons, edited by Chegwidden WR, Carter ND, and Edwards YH. Basel, Switzerland: Birkhäuser Verlag, 2000, p. 160-174.
49. Stams T, Nair SK, Okuyama T, Waheed A, Sly WS, and Christianson DW. Crystal structure of the secretory form of membrane-associated human carbonic anhydrase IV at 2.8-Å resolution. Proc Natl Acad Sci USA 93: 13589-13594, 1996.
50. Supuran CT. Carbonic anhydrases: catalytic and inhibition mechanisms, distribuion and physiological roles. In: Carbonic Anhydrase: Its Inhibitors and Activators, edited by Supuran CT, Scozzafava A, and Conway J. Boca Raton, FL: CRC, 2004, p. 1-23.
51. Swenson ER. Respiratory and renal roles of carbonic anhydrase in gas exchange and acid-base regulation. EXS 90: 281-341, 2000.
52. Swenson ER, Gronlund J, Ohlsson J, and Hlastala MP. In vivo quantitation of carbonic anhydrase and band 3 protein contributions to pulmonary gas exchange. J Appl Physiol 74: 838-848, 1993.
53. Swenson ER, Lippincott L, and Maren TH. Effect of gill membrane-bound carbonic anhydrase inhibition on branchial bicarbonate excretion in the dogfish shark, Squalus acanthias. Bull MDI Biol Lab 34: 94-95, 1995.
54. Swenson ER and Maren TH. Effects of acidosis and carbonic anhydrase inhibition in the elasmobranch rectal gland. Am J Physiol Renal Fluid Electrolyte Physiol 247: F86-F92, 1984.
55. 2 excretion. Am J Physiol Regul Integr Comp Physiol 253: R450-R458, 1987.
56. Swenson ER, Robertson HT, and Hlastala MP. Effects of carbonic anhydrase inhibition on ventilation-perfusion matching in the dog lung. J Clin Invest 92: 702-709, 1993.
57. Swenson ER, Taschner BC, and Maren TH. Effect of membrane-bound carbonic anhydrase (CA) inhibition on bicarbonate excretion in the shark, Squalus acanthias. Bull MDI Biol Lab 35: 35, 1996.
58. Tashian RE. Genetics of the mammalian carbonic anhydrases. Adv Genet 30: 321-356, 1992.
59. Tashian RE, Hewett-Emmett D, Carter N, and Bergenhem NCH. Carbonic anhydrase (CA)-related proteins (CA-RPs), and transmembrane proteins with CA or CA-RP domains. In: The Carbonic Anhydrases. New Horizons, edited by Chegwidden WR, Carter N, and Edwards YH. Basel, Switzerland: Birkhäuser Verlag, 2000, p. 105-120.
60. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, and Higgins DG. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24: 4876-4882, 1997.
61. +-ATPase and NHE2 in response to acid and base infusions in the Pacific spiny dogfish (Squalus acanthias). J Exp Biol 208: 345-354, 2005.
62. +-ATPase to the basolateral membrane in the Pacific spiny dogfish (Squalus acanthias): a role in base secretion. J Exp Biol 209: 599-609, 2006.
63. Tu C and Silverman DN. Role of histidine 64 in the catalytic mechanism of human carbonic anhydrase II studied with a site-specific mutant. Biochemistry 28: 7913-7918, 1989.
64. Tufts BL, Esbaugh A, and Lund SG. Comparative physiology and molecular evolution of carbonic anhydrase in the erythrocytes of early vertebrates. Comp Biochem Physiol A 136: 259-269, 2003.
65. Tufts BL, Gervais MR, Staebler M, and Weaver J. Subcellular distribution and characterization of gill carbonic anhydrase and evidence for a plasma carbonic anhydrase inhibitor in Antarctic fish. J Comp Physiol [B] 172: 287-295, 2002.
66. Waheed A, Okuyama T, Heyduk T, and 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 333: 432-438, 1996.
67. Waheed A, Zhu XL, and Sly WS. Membrane-associated carbonic anhydrase from rat lung. J Biol Chem 267: 3308-3311, 1992.
68. Wetzel P and Gros G. Carbonic anhydrases in striated muscle. In: The Carbonic Anhydrases. New Horizons, edited by Chegwidden WR, Carter N, and Edwards YH. Basel, Switzerland: Birkhäuser Verlag, 2000, p. 375-399.
69. Whitney PL and Briggle TV. Membrane-associated carbonic anhydrase purified from bovine lung. J Biol Chem 257: 12056-12059, 1982.
70. Wilson JM and Laurent P. Fish gill morphology: inside out. J Exp Zool 293: 192-213, 2002.
71. Wilson JM, Randall DJ, Vogl AW, Harris J, Sly WS, and Iwama GK. Branchial carbonic anhydrase is present in the dogfish, Squalus acanthias. Fish Physiol Biochem 22: 329-336, 2000.
72. Wistrand PJ and Knuuttila KG. Renal membrane-bound carbonic anhydrase. Purification and properties. Kidney Int 35: 851-859, 1989.
73. - dehydration by the blood of an elasmobranch in the absence of a Haldane effect. Respir Physiol 98: 319-337, 1994.
74. Zhu XL and Sly WS. Carbonic anhydrase IV from human lung. Purification, characterization, and comparison with membrane carbonic anhydrase from human kidney. J Biol Chem 265: 8795-8801, 1990.