Functional characterization of Rhesus glycoproteins from an ammoniotelic teleost, the rainbow trout, using oocyte expression and SIET analysis

Journal of Experimental Biology

Volumn 213, Issue 7, 2010, Pages 1049-1059

  Nawata, Michele ^a   Wood, Chris M ^a   O'Donnell, Michael J ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Ammonia transport; Gill; Rh glycoproteins; Trout; Xenopus oocytes

Indexed keywords

ACID; AMMONIA; AMMONIUM CHLORIDE; FISH PROTEIN; GLYCOPROTEIN; METHYLAMINE; PLASMA PROTEIN; PROTON;

ANIMAL; ARTICLE; DRUG EFFECT; ELECTRODE; ELECTROPHYSIOLOGY; INTRACELLULAR SPACE; KINETICS; METABOLISM; METHODOLOGY; OOCYTE; PH; RAINBOW TROUT; TRANSPORT AT THE CELLULAR LEVEL;

ACIDS; AMMONIA; AMMONIUM CHLORIDE; ANIMALS; BIOLOGICAL TRANSPORT; BLOOD PROTEINS; ELECTRODES; ELECTROPHYSIOLOGY; FISH PROTEINS; GLYCOPROTEINS; HYDROGEN-ION CONCENTRATION; INTRACELLULAR SPACE; KINETICS; METHYLAMINES; ONCORHYNCHUS MYKISS; OOCYTES; PROTONS;

ONCORHYNCHUS MYKISS; SALMONIDAE; TELEOSTEI;

EID: 77951437995     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.038752     Document Type: Article

References (75)

1. Ammann, D. (1986). Ion-Selective Microelectrodes. Principles, Design and Application. Berlin, Heidelberg, New York, Tokyo: Springer-Verlag.
2. + transport induced by the functional expression of the human Rh C glycoprotein. J. Biol. Chem. 279, 15975-15983.
3. Biver, S., Beige, H., Bourgeois, S., Van Vooren, P., Nowik, M., Scohy, S., Houillier, P., Szpirer, J., Szpirer, C., Wagner, C. A., Devuyst, O. and Marini, A.M. (2008). A role for Rhesus factor Rhcg in renal ammonium excretion and male fertility. Nature 456, 339-343.
4. 3. Eur. J. Physiol. 446, 652-657.
5. 3, and metabolic inhibitors. J. Gen. Physiol. 87, 91-112.
6. Braun, M. H., Steele, S. L., Ekker, M. and Perry, S. F. (2009). Nitrogen excretion in developing zebrafish (Danio rerio): A role for Rh proteins and urea transporters. Am. J. Physiol. 298, F994-F1005.
7. Bucking, C. and Wood, C. M. (2008). The alkaline tide and ammonia excretion after voluntary feeding in freshwater rainbow trout. J. Exp. Biol. 211, 2533-2541.
8. + conductance in Xenopus laevis oocytes. I. Basic observations. Eur. J. Physiol. 434, 306-312.
9. + permeation across Xenopus laevis oocyte cell membrane. Eur. J. Physiol. 420, 83-86.
10. Cameron, J. N. and Heisler, N. (1983). Studies of ammonia in the rainbow trout: physico-chemical parameters, acid-base behaviour and respiratory clearance. J. Exp. Biol. 105, 107-125.
11. Ceriotti, A. and Colman, A. (1995). mRNA translation in Xenopus oocytes. In Methods in Molecular Biology, Vol.37 (ed. M. J. Tymms), pp. 151-178. Totowa: Humana Press Inc.
12. + pathways in Xenopus laevis oocyte cell membrane. Eur. J. Physiol. 431, 658-667.
13. CRC Handbook of Chemistry and Physics (2005). 86th edition (ed. D. R. Lide), 2616 pp. CRC Press.
14. + concentration gradients adjacent to the surface of anal papillae of the mosquito Aedes aegypti: application of self-referencing ion-selective microelectrodes. J. Exp. Biol. 208, 603-610.
15. 2 channel in the human red cell membrane. FASEB J. 22, 64-73.
16. Handlogten, M. E., Hong, S.-P., Zhang, L., Vander, A. W., Steinbaum, M. L., Campbell-Thompson, M. and Weiner, I. D. (2005). Expression of the ammonia transporter proteins Rh B glycoprotein and Rh C glycoproteins in the intestinal tract. Am. J. Physiol. 288, G1036-G1047.
17. Heisler, N. (1990). Mechanisms of ammonia elimination in fishes. In Animal Nutrition and Transport Processes. 2. Transport, Respiration, and Excretion: Comparative and Environmental Aspects (ed. J.-P. Truchot and B. Lahlou), pp. 137-151. Basel: Karger.
18. + permeability in aquaporin-expressing Xenopus oocytes. Eur. J. Physiol. 450, 415-428.
19. Huang, C-H. (2008). Molecular origin and variability of the Rh gene family: an overview of evolution, genetics and function. In Haematology Education: The Education Programme for the Annual Congress of the European Hematology Association Vol.2, pp. 149-157. Copenhagen: European Hematology Association.
20. Hung, C. Y. C., Tsui, K. N. T., Wilson, J. M., Nawata, M., Wood, C. M. and Wright, P. A. (2007). Molecular cloning, characterization and tissue distribution of the Rhesus glycoproteins Rhbg, Rhcgl and Rhcg2 in the mangrove killifish Rivulus marmoratus exposed to elevated environmental ammonia levels. J. Exp. Biol. 210, 2419-2429.
21. Hung, C. Y. C., Nawata, C. M., Wood, C. M. and Wright, P. A. (2008). Rhesus glycoprotein and urea transporter genes are expressed in early stages of development of rainbow trout (Oncorhynchus myklss). J. Exp. Zool. 309A, 262-268.
22. Javelle, A., Severi, A., Thornton, J. and Merrick, M. (2004). Ammonium sensing in Escherichia coli. J. Biol. Chem. 279, 8530-8538.
23. Javelle, A., Thomas, G., Mamini, A.-M., Kramer, R. and Merrick, M. (2005). In vivo functional characterization of the Escherichia coli ammonium channel AmtB: evidence for metabolic coupling of AmtB to glutamine synthetase. Biochem. J. 390, 215-222.
24. Javelle, A., Lupo, D., Li, X.-D., Merrick, M., Chami, M., Ripoche, P. and Winkler, F. K. (2007). Structural and mechanistic aspects of Amt/Rh proteins. J. Struct. Biol 158,472-481.
25. Kelly, S. P. and Wood, C. M. (2001). The cultured branchial epithelium of the rainbow trout as a model for diffusive fluxes of ammonia across the fish gill. J. Exp. Biol 204, 4115-4124.
26. Khademi, S., O'Connell, J., III, Remis, J., Robles-Colmenares, Y., Mierke, L. J. W. and Stroud, R. M. (2004). Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1.35 Å. Science 305, 1587-1594.
27. 3. Nature 339, 478-480.
28. Kim, H.-Y., Verlander, J. W., Bishop, J. M., Cain, B. D., Han, K.-H., Igarashi, P., Lee, H.-W., Handlogten, M. E. and Weiner, I. D. (2009). Basolateral expression of the ammonia transporter family member Rh C glycoprotein in the mouse kidney. Am. J. Physiol. 296, F543-F555.
29. + across biological membranes. Biochim. Biophys. Acta 639, 41-52.
30. Knepper, M. A., Packer, R. and Good, D. W. (1989). Ammonium transport in the kidney. Physiol. Rev. 69, 179-249.
31. 2 channels. Transfus. Clin. Biol. 13, 103-110.
32. Lee, H.-W., Verlander, J. W., Bishop, J. M., Igarashi, P., Handlogten, M. E. and Weiner, I. D. (2009). Collecting duct-specific Rh C glycoprotein deletion alters basal and acidosis-stimulated renal ammonia excretion. Am. J. Physiol. 296, F1364-F1375.
33. Li, X., Jayachandran, S., Nguyen, H.-H. T. and Chan, M. (2007). Structure of the Nitrosomonas europaea Rh protein. Proc. Natl. Acad. Sci. USA 104, 19279-19284.
34. Liu, Z., Chen, Y., Mo, R., Hui, C., Cheng, J.-F., Mohandas, N. and Huang, C-H. (2000). Characterization of human RhCG and mouse Rhcg as novel nonerythroid Rh glycoprotein homologues predominantly expressed in kidney and testis. J. Biol. Chem. 275, 25641-25651.
35. Liu, Z., Peng, J., Mo, R., Hui, C. and Huang, C-H. (2001). Rh type B glycoprotein is a new member of the Rh superfamily and a putative ammonia transporter in mammals. J. Biol. Chem. 276, 1424-1438.
36. Ludewig, U. (2004). Electroneutral ammonium transport by basolateral rhesus B glycoprotein. J. Physiol. 559, 751-759.
37. Lumsden, J. S., Wright, P., Derksen, J., Byrne, P. J. and Ferguson, H. W. (1993). Paralysis in farmed Arctic char (Saivelinus alpinus) associated with ammonia toxicity. Vet. Rec. 133, 422-423.
38. Lupo, D., Li, X.-D., Curand, A., Tomikazi, T., Cherif-Zahar, B., Matassi, G., Merrick, M. and Winkler, F. K. (2007). The 1.3À resolution structure of Nitrosomonas europaea Rh50 and mechanistic implications for NH3 transport by Rhesus family proteins. Proc. Natl. Acad. Sci. USA 104, 19303-19308.
39. Mak, D. O. D., Dang, B., Weiner, I. D., Foskett, J. K. and Westhoff, C. M. (2006). Characterization of ammonia transport by the kidney Rh glycoproteins RhBG and RhCG. Am. J. Physiol. 290, F297-F305.
40. Marini, A.-M., Vissers, S., Urrestarazu, A. and Andre, B. (1994). Cloning and expression of the MEP1 gene encoding an ammonium transporter of Saccharomyces cerevisiae. EMBO J. 13, 3456-3463.
41. + transporters. Trends Biochem. Sci. 22, 460-461.
42. Marini, A.-M., Matassi, G., Raynal, V., Andre, B., Cartron, J.-P. and Cherif-Zahar, B. (2000). The human Rhesus-associated RhAG protein and a kidney homolgue promote ammonium transport in yeast. Nat. Genet. 26, 341-344.
43. Mayer, M., Schaaf, G., Mouro, I., Lopez., Colin, C., Neumann, P., Cartron, J.-P. and Ludewig, U. (2006). Different transport mechanisms in plant and human AMT/Rh-type ammonium transporters. J. Gen. Physiol. 127, 133-144.
44. Merrick, M., Blakey, D., Courts, G. and Thomas, G. (2001). Bacterial ammonium transport proteins: structure and function. In Nitrogen Fixation: Global Perspectives. Proceedings of the 13th International Congress on Nitrogen Fixation, Hamilton, Ontario, Canada, 2-7 July 2001 (ed. T. M. Finan, M. R. O'Brian, D. B. Layzell, J. K. Vassey, W. Newton), pp. 223-227. UK: CABI Publishing.
45. +. J. Membr. Biol. 228, 15-31.
46. Nakada, T., Westhoff, C. M., Kato, A. and Hirose, S. (2007a). Ammonia secretion from fish gill depends on a set of Rh proteins. FASEB J. 21, 1067-1074.
47. Nakada, T., Hoshijima, K., Esaki, M., Nagayoshi, S., Kawakami, K. and Hirose, S. (2007b). Localization of ammonia transporter Rhcgl in mitochondrion-rich cells of yolk sac, gill, and kidney of zebrafish and its ionic strength-dependent expression. Am. J. Physiol. 293, R1743-R1753.
48. + transporter. Am. J. Physiol. 288, F170-181.
49. 2 and external buffering on ammonia excretion and Rhesus glycoprotein mRNA expression in rainbow trout. J. Exp. Biol. 211, 3226-3236.
50. Nawata, C. M. and Wood, C. M. (2009). mRNA analysis of the physiological responses to ammonia infusion in rainbow trout. J. Comp. Physiol. 179, 799-810.
51. +-ATPase involvement. Physiol. Genomics 31, 463-474.
52. + transporter from plants. EMBO J. 13, 3464-3471.
53. Perry, S. F., Esbough, A., Braun, M. and Glimour, K. M. (2009). Gas transport and gill function in water-breathing fish. In Cardio-Respiratory Control in Vertebrates (ed. M. L. Glass and S. G. Woods), pp. 5-42. Berlin: Springer-Verlag.
54. Rheault, M. R. and O'Donnell, M. J. (2004). Organic cation transport by Malpighian tubules of Drosophila melanogaster. Application of two novel electrophysiological methods. J. Exp. Biol. 207, 2173-2184.
55. 3 into red blood cells. Proc. Natl. Acad. Sci. USA 101, 17222-17227.
56. Shih, T.-H., Horng, J.-L., Hwang, P.-P. and Lin, L.-Y. (2008). Ammonia excretion by the skin of zebrafish (Danio rerio) larvae. Am. J. Physiol. 295, C1625-C1632.
57. 2. Proc. Natl. Acad. Sci. USA 99, 7769-7773.
58. 2. Proc. Natl Acad. Sci. USA 101, 7787-7792.
59. + channel expressed in Xenopus oocytes. Am. J. Physiol. 268, C1173-C1178.
60. + exchange complex. J. Exp. Biol. 212, 878-892.
61. Waisbren, S. J., Geibel, J. P., Modlin, I. M. and Boron, W. F. (1994). Unusual permeability properties of gastric gland cells. Nature 368, 332-335.
62. Weidinger, K., Neuhauser, B., Gilch, S., Ludewig, U., Meyer, O. and Schmidt, I. (2007). Functional and physiological evidence for a Rhesus-type ammonia transporter in Nitrosomonas europaea. FEMS Microbiol. Lett. 273, 260-267.
63. Weihrauch, D., Wilkie, M. P. and Walsh, P. J. (2009). Ammonia and urea transporters in gill of fish and aquatic crustaceans. J. Exp. Biol. 212, 1716-1730.
64. Westhoff, C. M. and Wylie, D. E. (2006). Transport characteristics of mammalian Rh and Rh glycoproteins expressed in heterologous systems. Transfus. Clin. Biol. 13, 132-138.
65. Westhoff, C. M., Ferri-Jacobia, M., Mak, D. O. D. and Foskett, J. K. (2002). Identification of the erythrocyte Rh blood group glycoprotien as a mammalian ammonium transporter. J. Biol. Chem. 277, 12499-12502.
66. Westhoff, C. M., Siegel, D. L., Burd, C. G. and Foskett, J. K. (2004). Mechanism of genetic complementation of ammonium transport in yeast by human erythrocyte Rhassociated glycoprotein. J. Biol. Chem. 279, 17443-17448.
67. Wicks, B. J. and Randall, D. J. (2002). The effect of feeding and fasting on ammonia toxicity in juvenile rainbow trout, Oncorhynchus mykiss. Aquatic Toxicol. 59, 71-82.
68. + exchange. J. Exp. Biol. 191, 37-58.
69. Wood, C. M. (1993). Ammonia and urea metabolism and excretion. In The Physiology of Fishes (ed. D. H. Evans), pp. 379-425. Boca Raton: CRC Press.
70. Wright, P. A. and Wood, C. M. (1985). An analysis of branchial ammonia excretion in the freshwater rainbow trout: effects of environmental pH change and sodium uptake blockade. J. Exp. Biol. 114, 329-353.
71. Wright, P. A. and Wood, C. M. (2009). A new paradigm for ammonia excretion in aquatic animals: role of Rhesus (Rh) glycoproteins. J. Exp. Biol. 212, 2302-2312.
72. Wright, P. A., Heming, T. and Randall, D. J. (1986). Downstream pH changes in water flowing over the gills of rainbow trout. J. Exp. Biol. 126, 499-512.
73. Wright, P. A., Randall, D. J. and Perry, S. F. (1989). Fish gill boundary layer: a site of linkage between carbon dioxide and ammonia excretion. J. Comp. Physiol. 158, 627-635.
74. Zheng, L., Kostrewa, D., Berneche, S., Winkler, F. K. and Li, X.-D. (2004). The mechanism of ammonia transport based on the crystal structure of AmtB of Escherichia coli. Proc. Natl. Acad. Sci. USA 101, 17090-17095.
75. Zidi-Yahiaoui. N., Callebaut, I., Genetet, S., Van Kim, C. L., Cartron, J., -P., Colin, Y., Ripoche, P. and Mouro-Chanteloup, I. (2009). Functional analysis of human RhCG: a comparison with E. coli ammonium transporter reveals similarities in the pore and differences in the vestibule. Am. J. Physiol. 297, C537-C547.