Body fluid osmolytes and urea and ammonia flux in the colon of two chondrichthyan fishes, the ratfish, Hydrolagus colliei, and spiny dogfish, Squalus acanthias

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 161, Issue 1, 2012, Pages 27-35

  Anderson, W Gary ^a   Nawata, C Michele ^b   Wood, Chris M ^b   Piercey Normore, Michele D ^a   Weihrauch, Dirk ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

Ammonia; Chondrichthyes; Colon; Dogfish; Ratfish; Urea

Indexed keywords

AMMONIA; AMMONIUM CHLORIDE; BICARBONATE; CALCIUM; CARBON 14; CHLORINE; FISH PROTEIN; MAGNESIUM; POTASSIUM; PROTEIN RHBG; SULFATE; SULFUR DIOXIDE; UNCLASSIFIED DRUG; UREA; CARBOHYDRATE; CARRIER PROTEIN; CASEIN; ISOPROTEIN; LIPID; NITROGEN; OSMOLITE; UREA TRANSPORTER; VEGETABLE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BILE; BODY FLUID; COLON; COLON MUCOSA; CONTROLLED STUDY; FISH; GILL; HYDROLAGUS COLLIEI; KIDNEY; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOLALITY; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SEROSA; SQUALUS; ANIMAL; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

CALLORHINCHUS MILII; CHIMAERIDAE; CHONDRICHTHYES; HYDROLAGUS COLLIEI; LEUCORAJA ERINACEA; PISCES; SQUALIDAE; SQUALUS ACANTHIAS;

AMMONIA; ANIMALS; BODY FLUIDS; CARBOHYDRATES; CASEINS; COLON; FISHES; GENE EXPRESSION REGULATION; LIPIDS; MEMBRANE TRANSPORT PROTEINS; NITROGEN; PROTEIN ISOFORMS; SQUALUS ACANTHIAS; UREA; VEGETABLE PROTEINS;

EID: 84858229887     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2011.08.017     Document Type: Article

References (61)

1. Anderson P.M. Urea and glutamine synthesis: environmental influences on nitrogen excretion. Fish Physiol. 2001, 20:239-278.
2. Anderson W.G., Dasiewicz P.J., Liban S., Ryan C., Taylor J.R., Grosell M., Weihrauch D. Gastro-intestinal handling of water and solutes in 3 species of elasmobranch fish, the white-spotted bamboo shark, Chiloscyllium plagiosum, little skate, Leucoraja erinacea, and the clear nose skate, Raja eglanteria. Comp. Biochem. Physiol. A 2010, 155:493-502.
3. Bedford J.J. The composition of the fluid compartments of two chondrichthyans, Callorhyncus millii, and Squalus acanthias. Comp. Biochem. Physiol. A 1983, 76:75-80.
4. Bedford J.J., Harper J.L., Leader J.P., Yancey P.H., Smith R.A.J. Betaine is the principal counteracting osmolyte in tissues of the elephant fish, Callorhincus millii (Elasmobranchii, Holocephali). Comp. Biochem. Physiol. B 1998, 119:521-526.
5. Boyd T.A., Cha C., Forster R.P., Goldstein L. Free amino acids in tissues of the skate, Raja erinacea, and the stingray Dasyatis sabina: effects of environmental dilution. J. Exp. Zool. 1977, 199:435-442.
6. Boylan J.W. Gill permeability in Squalus acanthias. Sharks, Skates and Rays 1967, 197-206. John Hopkins University Press, Baltimore. P.W. Gilbert, R.F. Mathewson, D.P. Rall (Eds.).
7. Cox G., Francis M. Sharks and Rays of New Zealand 1997, Canterbury University Press, Canterbury, New Zealand.
8. Dakin W.J. The osmotic concentration of the blood of Callorhynchus milii and Epiceratodus (Neoceratodus) fosteri, and the significance of the physio-chemical condition of the blood in regard to systematic position on the Holocephali and the Dipnoi. Proc. Zool. Soc. 1931, 101:11-16.
9. De Boeck G., Grosell M., Wood C.M. Sensitivity of the spiny dogfish (Squalus acanthias) to waterborne silver exposure. Aquat. Toxicol. 2001, 54:261-275.
10. Eschmeyer W.N., Herald E.S., Hammann H. A Field Guide to the Pacific Coast Fishes of North America 1983, Houghton Mifflin Company, Boston, U.S.A.
11. Fange R., Fugelli K. Osmoregulation in Chimaeroid fishes. Nature 1962, 196:689.
12. Felsenstein J. Confidence limits on Phylogenies, an approach using Bootstrap. Evolution 1985, 39:783-791.
13. Fines G.A., Ballantyne J.S., Wright P.A. Active urea transport and an unusual basolateral membrane composition in the gills of a marine elasmobranch. Am. J. Physiol. 2001, 280:R16-R24.
14. Gillett M.B., Suko J.R., Santoso F.O., Yancey P.H. Elevated levels of trimethylamine oxide in muscles of deep-sea gadiform teleosts: a high-pressure adaptation?. J. Exp. Zool. 1997, 279:386-391.
15. Grimes D.J., Brayton P., Colwell R.R., Gruber S.H. Vibrios as autochthonous flora of neritic sharks. Syst. Appl. Microbiol. 1985, 6:221-226.
16. Grosell M. Intestinal anion exchange in marine fish osmoregulation. J. Exp. Biol. 2006, 209:2813-2827.
17. Hazon N., Balment R.J., Perrott M., O'Toole L.B. The renin-angiotensin system and vascular and dipsogenic regulation in elasmobranchs. Gen. Comp. Endocrinol. 1989, 74:230-236.
18. Hazon N., Wells A., Pillans R.D., Good J.P., Anderson W.G., Franklin C.E. Urea based osmoregulation and endocrine control in elasmobranch fish with special reference to euryhalinity. Comp. Biochem. Physiol. B 2003, 136:685-700.
19. Hyodo S., Bell J.D., Healy J.M., Kaneko T., Hasegawa S., Takei Y., Donald J.A., Toop T. Osmoregulation in elephant fish Callorhinchus milii (Holocephali), with special reference to the rectal gland. J. Exp. Biol. 2007, 210:1303-1310.
20. Hyodo S., Katoh F., Kaneko T., Takei Y. A facilitative urea transporter is localized in the renal collecting tubule of the dogfish, Triakis scyllia. J. Exp. Biol. 2004, 207:347-356.
21. Inoue J.G., Miya M., Lam K., Tay B.-H., Danks J.A., Bell J.D., Walker T.I., Venkatesh B. Evolutionary origin and phylogeny of the modern holocephalans (Chondrichthyes: Chimaeriformes): a miogenomic perspective. Mol. Biol. Evol. 2010, 27:2576-2586.
22. Janech M.G., Fitzgibbon W.R., Chen R.H., Nowak M.W., Miller D.H., Paul R.V., Ploth D.W. Cloning and functional characterisation of a urea transporter from the kidney of the Atlantic stingray. Dasyatis sabina. Am. J. Physiol. Ren. Physiol. 2006, 284:F996-F1005.
23. Janech M.G., Gefroh H.A., Cwengros E.E., Sulikowski J.A., Ploth D.W., Fitzgibbon W.R. Cloning of urea transporters from the kidneys of two batoid elasmobranchs: evidence for a common elasmobranch urea transporter isoform. Mar. Biol. 2008, 153:1173-1179.
24. Kajimura M., Walsh P.J., Mommsen T.P., Wood C.M. The dogfish shark (Squalus acanthias) increases both hepatic and extrahepatic ornithine urea cycle enzyme activities for nitrogen conservation after feeding. Physiol. Biochem. Zool. 2006, 79:602-613.
25. Kakumura K., Watanabe S., Bell J.D., Donald J.A., Toop T., Kaneko T., Hyodo S. Multiple urea transporter proteins in the kidney of holocephalan elephant fish (Callorhinchus milii). Comp. Biochem. Physiol. B 2009, 154:239-247.
26. King P.A., Cha C.-J., Goldstein L. Amino acid metabolism and cell volume regulation in the little skate, Raja erinacea. I. Oxidation. J. Exp. Zool. 1980, 212:69-77.
27. Knight I.T., Grimes J.D., Colwell R.R. Bacterial hydrolysis of urea in the tissue of charcharinid sharks. Can. J. Fish. Aquat. Sci. 1988, 45:357-360.
28. Krukenberg C.F.W. La retention de l'uree chez les selaciens. Ann. Mus. Hist. Nat. Mars. 1888, 3.
29. + transporters. Trends Biochem. Sci. 1997, 22:460-461.
30. Marshall W.S., Grosell M. Ion transport, osmoregulation and acid base balance. The Physiology of Fishes 2006, 177-230. CRC press, Boca Raton. D.H. Evans, J.B. Claiborne (Eds.).
31. McDonald M.D., Smith C.P., Walsh P.J. The physiology and evolution of urea transport in fishes. J. Membr. Biol. 2006, 212:93-107.
32. Mistry A.C., Honda S., Hirata T., Kato A., Hirose S. Eel urea transporter is localised in to chloride cells and is salinity dependent. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001, 281:R1594-R1604.
33. Morgan R.L., Wright P.A., Ballantyne J.S. Urea transport in kidney brush-border membrane vesicles from an elasmobranch, Raja erinacea. J. Exp. Biol. 2003, 206:3293-3302.
34. Nadella S., Grosell M., Wood C.M. Physical characterization of high-affinity gastrointestinal Cu transport in vitro in freshwater rainbow trout Oncorhynchus mykiss. J. Comp. Physiol. 2007, 176B:793-806.
35. Nakada T., Westhoff C.M., Yamaguchi Y., Hyodo S., Li X., Muro T., Kato A., Nakamura N., Hirose S. Rhesus glycoprotein P2 (Rhp2) is a novel member of the Rh family of ammonia transporters highly expressed in shark kidney. J. Biol. Chem. 2010, 285:2653-2664.
36. Nawata C.M., Wood C.M., O'Donnell M.J. Functional characterization of Rhesus glycoproteins from an ammoniotelic teleost, the rainbow trout, using oocyte expression and SIET analysis. J. Exp. Biol. 2010, 213:1049-1059.
37. Norris E.R., Benoit G.J. Studies on trimethylamine oxide I. Occurrence of trimethylamine oxide in marine organisms. J. Biol. Chem. 1945, 158:433-438.
38. Pärt P., Wright P.A., Wood C.M. Urea and water permeability in dogfish (Squalus acanthias) gills. Comp. Biochem. Physiol. A 1998, 119:117-123.
39. Rahmutallah M., Boyd T.R.C. Improvements in the determination of urea using diacetyl monoxime; methods with and without deproteinisation. Clin. Chim. Acta 1980, 107:3-9.
40. Read L.J. Enzymes of the ornithine-urea cycle in the chimaera, Hydrolagus colliei. Nature 1967, 215:1412. -&.
41. Read L.J. Chemical constituents of body fluids and urine of the Holocephalan Hydrolagus colliei. Comp. Biochem. Physiol. 1971, 39:185-192.
42. Robertson J.D. Chemical composition of the body fluids and muscle of the hagfish Myxine glutinosa and the rabbit-fish Chimaera monstrosa. J. Zool. Lond. 1976, 178:261-277.
43. Smith C.P., Wright P.A. Molecular characterisation of an elasmobranch urea transporter. Am. J. Physiol. 1999, 276:R622-R626.
44. Smith H.W. The absorption and excretion of water and salts by the elasmobranch fishes. II Marine Elasmobranchs. Am. J. Physiol. 1931, 98:296-310.
45. Sulikowski J.A., Maginniss L.A. Effects of environmental dilution on body fluid regulation in the yellow stingray. Urolophus jamaicensis. Comp. Biochem. Physiol. A 2001, 128:223-232.
46. Sulikowski J.A., Treberg J.R., Howell W.H. Fluid regulation and physiological adjustments in the winter skate, Leucoraja ocellata, following exposure to reduced environmental salinities. Environ. Biol. Fish. 2003, 66:339-348.
47. Treberg J.R., Driedzic W.R. Elevated levels of trimethylamine oxide in deep-sea fish: evidence for synthesis and intertissue physiological importance. J. Exp. Zool. 2002, 293:39-45.
48. Treberg J.R., Driedzic W.R. Maintenance and accumulation of trimethylamine oxide by winter skate (Leucoraja ocellata): reliance on low whole animal losses rather than synthesis. Am. J. Physiol. 2006, 291:R1790-R1798.
49. Treberg J.R., Speers-Roesch B., Piermarini P.M., Ip Y.K., Ballantyne J.S., Driedzic W.R. The accumulation of methylamine counteracting solutes in elasmobranchs with differing levels of urea: a comparison of marine and freshwater species. J. Exp. Biol. 2006, 209:860-870.
50. Urist M.R., Van De Putte K.A. Comparative biochemistry of the blood of fishes: identification of fishes by the chemical composition of serum. Sharks, Skates and Rays 1967, 271-285. John Hopkins Uni. Press, Baltimore. P.W. Gilbert, R.F. Mathewson, D.P. Rall (Eds.).
51. Weihrauch D., Wilkie M.P., Walsh P.J. Ammonia and urea transporters in gills of fish and aquatic crustaceans. J. Exp. Biol. 2009, 212:1716-1730.
52. Weiner I.D., Hamm L.L. Molecular mechanisms of renal ammonia transport. Annu. Rev. Physiol. 2007, 69:317-340.
53. Wilgenbusch J.C., Swofford D. Inferring evolutionary trees with PAUP. Curr. Protoc. Bioinform. 2003, chapter 6, unit 6.4.
54. Wilson J.M., Castro L.F.C. Morphological diversity of the gastrointestinal tract in fishes. Fish Physiol. 2010, 30:2-44.
55. Wood C.M., Bucking C., Fitzpatrick J., Nadella S. The alkaline tide goes out and the nitrogen stays in after feeding in the dogfish shark, Squalus acanthias. Respir. Physiol. Neurobiol. 2007, 159:163-170.
56. Wood C.M., Kajimura M., Bucking C., Walsh P.J. Osmoregulation, ionoregulation and acid-base regulation by the gastrointestinal tract after feeding in the elasmobranch (Squalus acanthias). J. Exp. Biol. 2007, 210:1335-1349.
57. Wood C.M., Kajimura M., Mommsen T.P., Walsh P.J. Alkaline tide and nitrogen conservation after feeding in an elasmobranch (Squalus acanthias). J. Exp. Biol. 2005, 208:2693-2705.
58. Wood C.M., Part P., Wright P.A. Ammonia and urea metabolism in relation to gill function and acid-base balance in a marine elasmobranch, the spiny dogfish (Squalus acnathias). J. Exp. Biol. 1995, 198:1545-1558.
59. Wood C.M., Schultz A.G., Munger R.S., Walsh P.J. Using omeprazole to link the components of the post-prandial alkaline tide in the spiny dogfish, Squalus acanthias. J. Exp. Biol. 2009, 212:684-692.
60. Wright P.A., Wood C.M. A new paradigm for ammonia excretion in aquatic animals: role of Rhesus (Rh) glycoproteins. J. Exp. Biol. 2009, 212:2303-2312.
61. Yancey P.H. Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J. Exp. Biol. 2005, 208:2819-2830.