Gas transfer in dogfish: A unique model of CO2 excretion

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 155, Issue 4, 2010, Pages 476-485

  Gilmour, K M ^a   Perry, S F ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Buffer capacity; Carbonic anhydrase; Dogfish; Elasmobranch; Gill; Red blood cell

Indexed keywords

BICARBONATE; CARBON DIOXIDE; CARBONATE DEHYDRATASE; CARBONATE DEHYDRATASE IV; PROTON;

BIOCHEMISTRY; CARBON DIOXIDE EXCRETION; CONTROLLED STUDY; CYTOPLASM; DEHYDRATION; DOGFISH; ELASMOBRANCHII; ERYTHROCYTE; GAS DIFFUSION; GILL; LUNG; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; REPTILE; REVIEW; TELEOST; VERTEBRA;

ELASMOBRANCHII; MAMMALIA; REPTILIA; SQUALUS ACANTHIAS; TELEOSTEI; VERTEBRATA;

EID: 77249098269     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2009.10.043     Document Type: Review

References (103)

1. +-independent SLC4 anion exchangers. J. Exp. Biol. 212 (2009) 1672-1683
2. Baird T.T., Waheed A., Okuyama T., Sly W.S., and Fierke C.A. Catalysis and inhibition of human carbonic anhydrase IV. Biochem. 36 (1997) 2669-2678
3. Bergenhem N., and Carlsson U. Partial amino acid sequence of erythrocyte carbonic anhydrase from tiger shark. Comp. Biochem. Physiol. 95B (1990) 205-213
4. 2 exchange in vivo. J. Appl. Physiol. 70 (1991) 1686-1699
5. 3-H+ reactions: theory. J. Appl. Physiol. 71 (1991) 1460-1468
6. Butler P.J., and Metcalfe J.D. Cardiovascular and respiratory systems. In: Shuttleworth T.J. (Ed). Physiology of Elasmobranch Fishes (1988), Springer-Verlag, Berlin 1-47
7. 2 excretion and intravascular pH disequilibria during carbonic anhydrase inhibition. J. Appl. Physiol. 84 (1998) 683-694
8. 2 transfer: theory. J. Appl. Physiol. 50 (1981) 265-271
9. 2 reactions. J. Clin. Invest. 62 (1978) 618-622
10. Effros R.M., Chang R.S.Y., and Silverman P. Acceleration of plasma bicarbonate conversion to carbon dioxide by pulmonary carbonic anhydrase. Science 199 (1978) 427-429
11. Egginton S., Skilbeck C., Hoofd L., Calvo J., and Johnston I.A. Peripheral oxygen transport in skeletal muscle of Antarctic and sub-Antarctic notothenioid fish. J. Exp. Biol. 205 (2002) 769-779
12. Esbaugh A., Lund S.G., and Tufts B.L. Comparative physiology and molecular analysis of carbonic anhydrase from the red blood cells of teleost fish. J. Comp. Physiol. B 174 (2004) 429-438
13. Esbaugh A., Perry S.F., Bayaa M., Georgalis T., Nickerson J.G., Tufts B.L., and Gilmour K.M. Cytoplasmic carbonic anhydrase isozymes in rainbow trout Oncorhynchus mykiss: comparative physiology and molecular evolution. J. Exp. Biol. 208 (2005) 1951-1961
14. Esbaugh A., and Tufts B.L. Evidence for a membrane-bound carbonic anhydrase in the heart of an ancient vertebrate, the sea lamprey (Petromyzon marinus). J. Comp. Physiol. B 174 (2004) 399-406
15. Esbaugh A., and Tufts B.L. The structure and function of carbonic anhydrase isozymes in the respiratory system of vertebrates. Respir. Physiol. Neurobiol. 154 (2006) 185-198
16. Esbaugh A., and Tufts B.L. 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 (2006) 1169-1178
17. Esbaugh A.J., Gilmour K.M., and Perry S.F. Membrane-associated carbonic anhydrase in the respiratory system of the Pacific hagfish (Eptatretus stouti). Respir. Physiol. Neurobiol. 166 (2009) 107-116
18. Esbaugh A.J., Perry S.F., and Gilmour K.M. Hypoxia-inducible carbonic anhydrase IX expression is insufficient to alleviate intracellular metabolic acidosis in the muscle of zebrafish, Danio rerio. Am. J. Physiol. 296 (2009) R150-R160
19. Fleming R.E., Crouch E.C., Ruzicka C.A., and Sly W.S. Pulmonary carbonic anhydrase IV: developmental regulation and cell-specific expression in the capillary endothelium. Am. J. Physiol. 265 (1993) L627-L635
20. Georgalis T., Gilmour K.M., Yorston J., and Perry S.F. 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. 291 (2006) F407-F421
21. Gervais M.R., and Tufts B.L. Characterization of carbonic anhydrase and anion exchange in the erythrocytes of bowfin (Amia calva), a primitive air-breathing fish. Comp. Biochem. Physiol. A123 (1999) 343-350
22. Gilmour K.M., Bayaa M., Kenney L., McNeill B., and Perry S.F. Type IV carbonic anhydrase is present in the gills of spiny dogfish (Squalus acanthias). Am. J. Physiol. 292 (2007) R556-R567
23. - dehydration when red blood cell anion exchange is inhibited. Respir. Physiol. Neurobiol. 140 (2004) 173-187
24. Gilmour K.M., Henry R.P., Wood C.M., and Perry S.F. Extracellular carbonic anhydrase and an acid-base disequilibrium in the blood of the dogfish, Squalus acanthias. J. Exp. Biol. 200 (1997) 173-183
25. 2 transfer are revealed by severe experimental anaemia in brown bullhead (Ameiurus nebulosus). Comp. Biochem. Physiol. A 135 (2003) 165-175
26. 2 excretion in vitro in rainbow trout, Oncorhynchus mykiss. Fish Physiol. Biochem. 15 (1996) 83-94
27. 2 excretion in severely anemic dogfish. Am. J. Physiol. 286 (2004) R1138-R1148
28. Gilmour K.M., and Perry S.F. Carbonic anhydrase and acid-base regulation in fish. J. Exp. Biol. 212 (2009) 1647-1661
29. 2 excretion. Physiol. Biochem. Zool. 74 (2001) 477-492
30. Gilmour K.M., Randall D.J., and Perry S.F. Acid-base disequilibrium in the arterial blood of rainbow trout. Respir. Physiol. 96 (1994) 259-272
31. Gilmour K.M., 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 (2002) 77-86
32. Heming T.A., Vanoye C.G., Stabenau E.K., Roush E.D., Fierke C.A., and Bidani A. Inhibitor sensitivity of pulmonary vascular carbonic anhydrase. J. Appl. Physiol. 75 (1993) 1642-1649
33. Henry R.P. Invertebrate red blood cell carbonic anhydrase. J. Exp. Zool. 242 (1987) 113-116
34. Henry R.P. Multiple roles of carbonic anhydrase in cellular transport and metabolism. Annu. Rev. Physiol. 58 (1996) 523-538
35. Henry R.P., Gilmour K.M., Wood C.M., and Perry S.F. Extracellular carbonic anhydrase activity and carbonic anhydrase inhibitors in the circulatory system of fish. Physiol. Zool. 70 (1997) 650-659
36. Henry R.P., Smatresk N.J., and Cameron J.N. 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 (1988) 201-218
37. Henry R.P., and Swenson E.R. The distribution and physiological significance of carbonic anhydrase in vertebrate gas exchange organs. Respir. Physiol. 121 (2000) 1-12
38. Henry R.P., Tufts B.L., and Boutilier R.G. 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 (1993) 380-388
39. Hewett-Emmett D., and Tashian R.E. Functional diversity, conservation, and convergence in the evolution of the α-, ß-, and γ-carbonic anhydrase gene families. Mol. Phyl. Evol. 5 (1996) 50-77
40. Hill E.P. Inhibition of carbonic anhydrase by plasma of dogs and rabbits. J. Appl. Physiol. 60 (1986) 191-197
41. Holeton G.F. Oxygen uptake and circulation by a hemoglobinless Antarctic fish (Chaenocephalus aceratus Lonnberg) compared with three red-blooded Antarctic fish. Comp. Biochem. Physiol. 34 (1970) 457-471
42. Hubner S., Michel F., Rudloff V., and Appelhans H. Amino acid sequence of band-3 protein from rainbow trout erythrocytes derived from cDNA. Biochem. J. 285 (1992) 17-23
43. Jensen F.B. Multiple strategies in oxygen and carbon dioxide transport by haemoglobin. In: Woakes A.J., Grieshaber M.K., and Bridges C.R. (Eds). Physiological Strategies for Gas Exchange and Metabolism (1991), Cambridge University Press, Cambridge 55-78
44. Jewell D.A., Tu C., Paranawithana S.F., Tanhauser S.M., LoGrasso P.V., Laipis P.J., and Silverman D.N. Enhancement of the catalytic properties of human carbonic anhydrase III by site-directed mutagenesis. Biochemistry 30 (1991) 1484-1490
45. 2 reactions by lung carbonic anhydrase. J. Appl. Physiol. 44 (1978) 882-888
46. +-ATPase-rich cells. Am. J. Physiol. 294 (2008) C1250-C1260
47. Lindskog S., and Silverman D.N. The catalytic mechanism of mammalian carbonic anhydrases. In: Chegwidden W.R., Carter N.D., and Edwards Y.H. (Eds). The carbonic anhydrases: new horizons (2000), Birkhäuser Verlag, Basel, Switzerland 175-195
48. Lund S.G., Dyment P., Gervais M.R., Moyes C.D., and Tufts B.L. Characterization of erythrocyte carbonic anhydrase in an ancient fish, the longnose gar (Lepisosteus osseus). J. Comp. Physiol. B 172 (2002) 467-476
49. Maffia M., Rizzello A., Acierno R., Rollo M., Chiloiro R., and Storelli C. Carbonic anhydrase activity in tissues of the icefish Chionodraco hamatus and of the red-blooded teleosts Trematomus bernacchii and Anguilla anguilla. J. Exp. Biol. 204 (2001) 3983-3992
50. Mangum C.P. Oxygen transport in invertebrates. Am. J. Physiol. 248 (1985) R505-R514
51. Maren T.H., Friedland B.R., and Rittmaster R.S. Kinetic properties of primitive vertebrate carbonic anhydrases. Comp. Biochem. Physiol. B 67 (1980) 69-74
52. Maynard J.R., and Coleman J.E. Elasmobranch carbonic anhydrase: purification and properties of the enzyme from two species of shark. J. Biol. Chem. 246 (1971) 4455-4464
53. Meldrum N.U., and Roughton F.J.W. Carbonic anhydrase. Its preparation and properties. J. Physiol. 80 (1933) 113-142
54. Nikinmaa M. Oxygen and carbon dioxide transport in vertebrate erythrocytes: an evolutionary change in the role of membrane transport. J. Exp. Biol. 200 (1997) 369-380
55. Nikinmaa M., Airaksinen S., and Virkki L.V. Haemoglobin function in intact lamprey erythrocytes: interactions with membrane function in the regulation of gas transport and acid-base balance. J. Exp. Biol. 198 (1995) 2423-2430
56. Nikinmaa M., and Railo E. Anion movements across lamprey (Lampetra fluviatilis) red cell membrane. Biochim. Biophys. Acta 899 (1987) 134-136
57. Obaid A.L., Critz A.M., and Crandall E.D. Kinetics of bicarbonate/chloride exchange in dogfish erythrocytes. Am. J. Physiol. 237 (1979) R132-R138
58. Okuyama T., Sato S., Zhu X.L., Waheed A., and Sly W.S. Human carbonic anhydrase IV: cDNA cloning, sequence comparison, and expression in COS cell membranes. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 1315-1319
59. Okuyama T., Waheed A., Kusumoto W., Zhu X.L., and Sly W.S. Carbonic anhydrase IV: role of removal of C-terminal domain in glycosylphosphatidylinositol anchoring and realization of enzyme activity. Arch. Biochem. Biophys. 320 (1995) 315-322
60. Olson K.R. Vascular anatomy of the fish gill. J. Exp. Zool. 293 (2002) 214-231
61. Pastoreková S., Parkkila S., Pastorek J., and Supuran C.T. Carbonic anhydrases: current state of the art, therapeutic applications and future prospects. J. Enzyme Inhib. Med. Chem. 19 (2004) 199-229
62. Perry S.F. Carbon dioxide excretion in fishes. Can. J. Zool. 64 (1986) 565-572
63. 2 excretion in a spontaneously ventilating blood-perfused trout preparation and saline-perfused gill preparations: contribution of the branchial epithelium and red blood cell. J. Exp. Biol. 101 (1982) 47-60
64. Perry S.F., and Gilmour K.M. An evaluation of factors limiting carbon dioxide excretion by trout red blood cells in vitro. J. Exp. Biol. 180 (1993) 39-54
65. Perry S.F., and Gilmour K.M. Sensing and transfer of respiratory gases at the fish gill. J. Exp. Zool. 293 (2002) 249-263
66. 2 excretion in fish: unanswered questions and emerging models. Respir. Physiol. Neurobiol. 154 (2006) 199-215
67. Perry S.F., Wood C.M., Walsh P.J., and Thomas S. Fish red blood cell carbon dioxide transport in vitro: a comparative study. Comp. Biochem. Physiol. A 113 (1996) 121-130
68. 18O exchange. J. Exp. Biol. 203 (2000) 1551-1560
69. Rispens P., Hessels J., Zwart A., and Zijlstra W.G. Inhibition of carbonic anhydrase in dog plasma. Pflügers Arch. 403 (1985) 344-347
70. Romano L., and Passow H. Characterization of anion transport system in trout red blood cell. Am. J. Physiol. 246 (1984) C330-C338
71. Roush E.D., and Fierke C.A. Purification and characterization of a carbonic anhydrase II inhibitor from porcine plasma. Biochemistry 31 (1992) 12536-12542
72. 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 (1999) 43-50
73. 2 transport to tumor markers. EXS 90 (2000) 95-104
74. Stabenau E.K., Bidani A., and Heming T.A. Physiological characterization of pulmonary carbonic anhydrase in the turtle. Respir. Physiol. 104 (1996) 187-196
75. 2 excretion and postcapillary pH equilibration in blood-perfused turtle lungs. J. Exp. Biol. 202 (1999) 965-975
76. Stabenau E.K., and Heming T.A. Pulmonary carbonic anhydrase in vertebrate gas exchange organs. Comp. Biochem. Physiol. A 136 (2003) 271-279
77. Stabenau E.K., and Vietti K.R.N. Pulmonary carbonic anhydrase in the garter snake, Thamnophis sirtalis. Physiol. Biochem. Zool. 75 (2002) 83-89
78. Stams T., and Christianson D.W. X-ray crystallographic studies of mammalian carbonic anhydrase isozymes. In: Chegwidden W.R., Carter N.D., and Edwards Y.H. (Eds). The carbonic anhydrases: new horizons (2000), Birkhäuser Verlag, Basel, Switzerland 160-174
79. Stams T., Nair S.K., Okuyama T., Waheed A., Sly W.S., and Christianson D.W. Crystal structure of the secretory form of membrane-associated human carbonic anhydrase IV at 2.8-Å resolution. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 13589-13594
80. Supuran, C.T., Scozzafava, A., 2004. Benzolamide is not a membrane-impermeant carbonic anhydrase inhibitor. J Enzyme Inhib Med Chem 19, 269-273.
81. Swenson E.R. Teleost erythrocyte carbonic anhydrase: isolation and partial characterization. Bull. MDI Biol. Lab. 19 (1979) 74-77
82. Swenson E.R. Respiratory and renal roles of carbonic anhydrase in gas exchange and acid-base regulation. EXS 90 (2000) 281-341
83. 2 excretion. Am. J. Physiol. 253 (1987) R450-R458
84. Swenson E.R., Gronlund J., Ohlsson J., and Hlastala M.P. In vivo quantitation of carbonic anhydrase and band 3 protein contributions to pulmonary gas exchange. J. Appl. Physiol. 74 (1993) 838-848
85. Swenson E.R., Robertson H.T., and Hlastala M.P. Effects of carbonic anhydrase inhibition on ventilation-perfusion matching in the dog lung. J. Clin. Invest. 92 (1993) 702-709
86. Tashian R.E. Genetics of the mammalian carbonic anhydrases. Adv. Genet. 30 (1992) 321-356
87. Tashian R.E., Hewett-Emmett D., Carter N., and Bergenhem N.C.H. Carbonic anhydrase (CA)-related proteins (CA-RPs), and transmembrane proteins with CA or CA-RP domains. In: Chegwidden W.R., Carter N., and Edwards Y.H. (Eds). The carbonic anhydrases (2000), New Horizons, Birkhäuser Verlag, Basel, Switzerland 105-120
88. Tu C., and Silverman D.N. Role of histidine 64 in the catalytic mechanism of human carbonic anhydrase II studied with a site-specific mutant. Biochem. 28 (1989) 7913-7918
89. Tufts B.L., Bagatto B., and Cameron B. In vivo analysis of gas transport in arterial and venous blood of the sea lamprey Petromyzon marinus. J. Exp. Biol. 169 (1992) 105-119
90. 2 transport and ion distributions between plasma anderythrocytes in the blood of Petromyzon marinus. J. Exp. Biol. 144 (1989) 565-576
91. Tufts B.L., Esbaugh A., and Lund S.G. Comparative physiology and molecular evolution of carbonic anhydrase in the erythrocytes of early vertebrates. Comp. Biochem. Physiol. A 136 (2003) 259-269
92. Tufts B.L., Gervais M.R., Moss A.G., and Henry R.P. Carbonic anhydrase and red blood cell anion exchange in the neotenic aquatic salamander, Necturus maculosus. Physiol. Biochem. Zool. 72 (1999) 317-327
93. Tufts B.L., Gervais M.R., 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 (2002) 287-295
94. Tufts B.L., and Perry S.F. Carbon dioxide transport and excretion. Fish. Physiol. 17 (1998) 229-281
95. Waheed A., Okuyama T., Heyduk T., and Sly W.S. 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 (1996) 432-438
96. Waheed A., Zhu X.L., and Sly W.S. Membrane-associated carbonic anhydrase from rat lung. J. Biol. Chem. 267 (1992) 3308-3311
97. Walsh P.J., and Henry R.P. Carbon dioxide and ammonia metabolism and exchange. In: Hochachka P.W., and Mommsen T.P. (Eds). Biochemistry and molecular biology of fishes. Phylogenetic and biochemical perspectives, Vol. 1 (1991), Elsevier, Amsterdam 181-207
98. Whitney P.L., and Briggle T.V. Membrane-associated carbonic anhydrase purified from bovine lung. J. Biol. Chem. 257 (1982) 12056-12059
99. Wilson J.M., and Laurent P. Fish gill morphology: inside out. J. Exp. Zool. 293 (2002) 192-213
100. Wilson J.M., Randall D.J., Vogl A.W., Harris J., Sly W.S., and Iwama G.K. Branchial carbonic anhydrase is present in the dogfish, Squalus acanthias. Fish Physiol. Biochem. 22 (2000) 329-336
101. Wood C.M., McDonald D.G., and McMahon B.R. The influence of experimental anaemia on blood acid-base regulation in vivo and in vitro in the starry flounder (Platichthys stellatus) and the rainbow trout (Salmo gairdneri). J. Exp. Biol. 96 (1982) 221-237
102. - dehydration by the blood of an elasmobranch in the absence of a Haldane effect. Respir. Physiol. 98 (1994) 319-337
103. Zhu X.L., and Sly W.S. Carbonic anhydrase IV from human lung. Purification, characterization, and comparison with membrane carbonic anhydrase from human kidney. J. Biol. Chem. 265 (1990) 8795-8801