Rhesus glycoprotein and urea transporter genes in rainbow trout embryos are upregulated in response to alkaline water (pH 9.7) but not elevated water ammonia

Aquatic Toxicology

Volumn 96, Issue 4, 2010, Pages 308-313

  Sashaw, Jessica ^a   Nawata, Michele ^b   Thompson, Sarah ^a   Wood, Chris M ^b   Wright, Patricia A ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

Author keywords

Ammonia excretion; Ammonia toxicity; Development; Rh; Urea excretion; UT

Indexed keywords

AMMONIA; CARRIER PROTEINS AND BINDING PROTEINS; ELONGATION FACTOR 1ALPHA; GLYCOPROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; RHESUS GLYCOPROTEIN; RHESUS GLYCOPROTEIN 1; RHESUS GLYCOPROTEIN 2; SODIUM PROTON EXCHANGE PROTEIN; UNCLASSIFIED DRUG; UREA; UREA TRANSPORTER;

AMMONIA; EMBRYONIC DEVELOPMENT; ENVIRONMENTAL CONDITIONS; GENE EXPRESSION; GENE FLOW; PH; PHYSIOLOGICAL RESPONSE; PROTEIN; SALMONID; UREA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENVIRONMENTAL EXPOSURE; EXCRETION; GENE EXPRESSION REGULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAINBOW TROUT; TISSUE LEVEL; UPREGULATION;

AMMONIA; ANIMALS; CATION TRANSPORT PROTEINS; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOPROTEINS; HYDROGEN-ION CONCENTRATION; MEMBRANE GLYCOPROTEINS; MEMBRANE TRANSPORT PROTEINS; ONCORHYNCHUS MYKISS; RNA, MESSENGER; UP-REGULATION; WATER;

MYKISS; ONCORHYNCHUS MYKISS;

EID: 75849118381     PISSN: 0166445X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquatox.2009.11.012     Document Type: Article

References (53)

1. Barimo J.F., Steele S.L., Wright P.A., and Walsh P.J. Dogmas and controversies in the handling of nitrogenous wastes: ureotely and ammonia tolerance in early life stages of the gulf toadfish, Opsanus beta. J. Exp. Biol. 207 (2004) 2011-2020
2. Barry T.P., Malison J.A., Held J.A., and Parrish J.J. Ontogeny of the cortisol stress response in larval rainbow trout. Gen. Comp. Endocrinol. 97 (1995) 57-65
3. Barry T.P., Ochiai M., and Malison J.A. In vitro effects of ACTH on interrenal corticosteroidogenesis during early larval development in rainbow trout. Gen. Comp. Endocrinol. 99 (1995) 382-387
4. Braun M.H., Steele S.L., Ekker M., and Perry S.F. Nitrogen excretion in developing zebrafish (Danio rerio): a role for Rh proteins and urea transporters. Am. J. Physiol. Renal Physiol. 296 (2009) F994-F1005
5. Brönmark C., and Hansson L.-A. The Biology of Lakes and Ponds (2005), Oxford University Press, Oxford
6. Bucking C., and Wood C.M. The alkaline tide and ammonia excretion after voluntary feeding in freshwater rainbow trout. J. Exp. Biol. 211 (2008) 2533-2541
7. CEPA, 2002. Environmental Registry (www.ec.gc.ca/ceparegistry/subs_list/Ammonia_BG.cfm).
8. Chadwick T.D., and Wright P.A. Nitrogen excretion and expression of urea cycle enzymes in the atlantic cod (Gadus morhua L.): a comparison of early life stages with adults. J. Exp. Biol. 202 (1999) 2653-2662
9. Dépêche J., Gilles R., Daufresne S., and Chiapello H. Urea content and urea production via the ornithine-urea cycle pathway during the ontogenic development of two teleost fishes. Comp. Biochem. Physiol. 63A (1979) 51-56
10. Essex-Fraser P.A., Steele S.L., Bernier N.J., Murray B.W., Stevens E.D., and Wright P.A. Expression of four glutamine synthetase genes in the early stages of development of rainbow trout (Oncorhynchus mykiss) in relationship to nitrogen excretion. J. Biol. Chem. 280 (2005) 20268-20273
11. Griffith R.W. Guppies, toadfish, lungfish, coelacanths and frogs: a scenario for the evolution of urea retention in fishes. Environ. Biol. Fishes 32 (1991) 199-218
12. Hung C.C., Nawata C.M., Wood C.M., and Wright P.A. Rhesus glycoprotein and urea transporter genes are expressed in early stages of development of rainbow trout (Oncorhynchus mykiss). J. Exp. Zool. 309 (2008) 262-268
13. Jeney Z., Nemcsók J., Jeney G., and Oláh J. Acute effect of sublethal ammonia concentrations on common carp (Cyprinus carpio L.). I. Effect of ammonia on adrenaline and noradrenaline levels in different organs. Aquaculture 104 (1992) 139-148
14. Jordan D.H.M., and Lloyd R. The resistance of rainbow trout (Salmo gairdneri Richardson) and roach (Rutilus rutilus L.) to alkaline solutions. Int. J. Air Water Pollut. 8 (1964) 405-409
15. Korsgaard B. Nitrogen distribution and excretion during embryonic post-yolk sac development in Zoarces viviparus. J. Comp. Physiol. B 164 (1994) 42-46
16. Korte J.J., Salo W.L., Cabrera V.M., Wright P.A., Felskie A.K., and Anderson P.M. Expression of carbamoyl-phosphate synthetase III mRNA during the early stages of development and in muscle of adult rainbow trout (Oncorhynchus mykiss). J. Biol. Chem. 272 (1997) 6270-6277
17. Kun E., and Kearney E.B. Enzymatic determination of ammonia. In: Bermeyer H.U. (Ed). Methods of Enzymatic Analysis. 2nd ed. (1974), Academic Press, New York 1802-1806
18. Lin L.Y., Horng J.L., Kunkel J.G., and Hwang P.P. Proton pump-rich cell secretes acid in skin of zebrafish larvae. Am. J. Physiol. Cell Physiol. 290 (2006) C371-C378
19. McDonald M.D., and Wood C.M. Evidence for facilitated diffusion of urea across the gill basolateral membrane of the rainbow trout (Oncorhynchus mykiss). Biochim. Biophys. Acta 1663 (2004) 89-96
20. McGeer J., and Eddy F. Ionic regulation and nitrogenous excretion in rainbow trout exposed to buffered and unbuffered freshwater of pH 10.5. Physiol. Zool. 71 (1998) 179-190
21. Morrison J.K., and Piper R.G. Effect of reused water on Atlantic salmon. Progve. Fish Cult. 50 (1988) 110-112
22. Murray C.A., and Ziebell C.D. Acclimation of rainbow trout to high pH to prevent stocking mortality in summer. Progve. Fish Cult. 46 (1984) 176-179
23. Nakada T., Hoshijima K., Esaki M., Nagayoshi S., Kawakami K., and Hirose S. Localization of ammonia transporter Rhcg1 in mitochondrion-rich cells of yolk sac, gill, and kidney of zebrafish and its ionic strength-dependent expression. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293 (2007) R1743-R1753
24. Nawata C.M., Hung C.C., Tsui T.K., Wilson J.M., Wright P.A., and Wood C.M. Ammonia excretion in rainbow trout (Oncorhynchus mykiss): evidence for Rh glycoprotein and H+-ATPase involvement. Physiol. Genomics 31 (2007) 463-474
25. Nawata C.M., and Wood C.M. mRNA analysis of the physiological responses to ammonia infusion in rainbow trout. J. Comp. Physiol. B 179 (2009) 799-810
26. Ortega V.A., Renner K.J., and Bernier N.J. Appetite-suppressing effects of ammonia exposure in rainbow trout associated with regional and temporal activation of brain monoaminergic and CRF systems. J. Exp. Biol. 208 (2005) 1855-1866
27. Pilley C., and Wright P. The mechanisms of urea transport by early life stages of rainbow trout (Oncorhynchus mykiss). J. Exp. Biol. 203 (2000) 3199-3207
28. Rahaman-Noronha E., Donnell M., Pilley C., and Wright P. Excretion and distribution of ammonia and the influence of boundary layer acidification in embryonic rainbow trout (Oncorhynchus mykiss). J. Exp. Biol. 199 (1996) 2713-2723
29. Rahmatullah M., and Boyde T.R.C. Improvements in the determination of urea using diacetyl monoxime; methods with and without deproteinisation. Clin. Chim. Acta 107 (1980) 3-9
30. Randall D.J., and Tsui T.K.N. Ammonia toxicity in fish. Mar. Poll. Bull. 45 (2002) 17-23
31. Randall D.J., Wood C.M., Perry S.F., Bergman H.L., Maloiy G.M.O., Mommsen T.P., and Wright P.A. Urea excretion as a strategy for survival in a fish living in a very alkaline environment. Nature 337 (1989) 165-166
32. Rombough P.J. Respiratory gas exchange, aerobic metabolism and effects of hypoxia during early life. In: Hoar W.S., and Randall D.J. (Eds). Fish Physiology (1988), Academic Press, London 59-161
33. Shih T.H., Horng J.L., Hwang P.P., and Lin L.Y. Ammonia excretion by the skin of zebrafish (Danio rerio) larvae. Am. J. Physiol. Cell Physiol. 295 (2008) C1625-C1632
34. Steele S.L., Chadwick T.D., and Wright P.A. Ammonia detoxification and localization of urea cycle enzyme activity in embryos of the rainbow trout (Oncorhynchus mykiss) in relation to early tolerance to high environmental ammonia levels. J. Exp. Biol. 204 (2001) 2145-2154
35. Terjesen B.F., Verreth J., and Fyhn H.J. Urea and ammonia excretion by embryos and larvae of the African catfish Clarias gariepinus (Burchell 1822). Fish Physiol. Biochem. 16 (1997) 311-321
36. Thurston R.V., Russo R.C., and Vinogradov G.A. Ammonia toxicity to fishes. Effect of pH on the toxicity of the un-ionized ammonia species. Environ. Sci. Technol. 15 (1981) 837-840
37. + exchange complex. J. Exp. Biol. 212 (2009) 878-892
38. Verdouw H., van Echteld C.J.A., and Dekkers E.M.J. Ammonia determination based on indrophenol formation with sodium salicylate. Water Res. 12 (1978) 399-402
39. Walsh P.J., Grosell M., Goss G.G., Bergman H.L., Bergman A.N., Wilson P., Laurent P., Alper S.L., Smith C.P., Kamunde C., and Wood C.M. Physiological and molecular characterization of urea transport by the gills of the Lake Magadi tilapia (Alcolapia grahami). J. Exp. Biol. 204 (2001) 509-520
40. Weihrauch D., Wilkie M.P., and Walsh P.J. Ammonia and urea transporters in gills of fish and aquatic crustaceans. J. Exp. Biol. 212 (2009) 1716-1730
41. Wilkie M.P., Simmons H.E., and Wood C.M. Physiological adaptations to chronically elevated water pH (pH 9.5) in rainbow trout (Oncorhynchus mykiss). J. Exp. Zool. 274 (1996) 1-14
42. Wilkie M.P., and Wood C.M. Nitrogenous waste excretion, acid-base regulation, and ionoregulation in rainbow trout (Oncorhynchus mykiss) exposed to extremely alkaline water. Physiol. Zool. 64 (1991) 1069-1086
43. Wilkie M.P., and Wood C.M. The effects of extremely alkaline water (pH 9.5) on rainbow trout gill function and morphology. J. Fish Biol. 45 (1994) 87-98
44. Wilkie M.P., and Wood C.M. Recovery from high pH exposure in the rainbow trout: White muscle ammonia storage, ammonia washout, and the restoration of blood chemistry. Physiol. Zool. 68 3 (1995) 379-401
45. Wilkie M.P., and Wood C.M. The adaptations of fish to extremely alkaline environments. Comp. Biochem. Physiol. 113B (1996) 665-673
46. Wood C.M., Kajimura M., Mommsen T.P., and Walsh P.J. Is the alkaline tide a signal to activate metabolic or ionoregulatory enzymes in the dogfish shark (Squalus acanthias)?. Physiol. Biochem. Zool. 81 (2008) 278-287
47. Wood C.M., Perry S.F., Wright P.A., Bergman H.L., and Randall D.J. Ammonia and urea dynamics in the Lake Magadi tilapia, a ureotelic teleost fish adapted to an extremely alkaline environment. Resp. Physiol. 77 (1989) 1-20
48. Wright P., Felskie A., and Anderson P. Induction of ornithine-urea cycle enzymes and nitrogen metabolism and excretion in rainbow trout (Oncorhynchus mykiss) during early life stages. J. Exp. Biol. 198 (1995) 127-135
49. Wright P.A., and Fyhn H.J. Ontogeny of nitrogen metabolism and excretion. In: Wright P., and Anderson P. (Eds). Nitrogen Excretion, Fish Physiology vol. 20 (2001), Academic Press, San Diego 149-200
50. Wright P.A., Iwama G.K., and Wood C.M. Ammonia and urea excretion in Lahontan cutthroat trout (Oncorhynchus clarki henshawi) adapted to highly alkaline Pyramid Lake (pH 9.4). J. Exp. Biol. 175 (1993) 153-172
51. Wright P.A., and Land M.D. Urea production and transport in teleost fishes. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 119 (1998) 47-54
52. Wright P.A., and Wood C.M. An analysis of branchial ammonia excretion in the freshwater rainbow trout: effects of environmental pH change and sodium uptake blockade. J. Exp. Biol. 114 (1985) 329-353
53. Wright P.A., and Wood C.M. A new paradigm for ammonia excretion in aquatic animals: role of Rhesus (Rh) glycoproteins. J. Exp. Biol. 212 (2009) 2303-2312