Na+/K+-ATPase expression in gills of the euryhaline sailfin molly, Poecilia latipinna, is altered in response to salinity challenge

Journal of Experimental Marine Biology and Ecology

Volumn 375, Issue 1-2, 2009, Pages 41-50

  Yang, Wen Kai ^a   Hseu, Jinn Rong ^b   Tang, Cheng Hao ^a   Chung, Ming Ju ^c   Wu, Su Mei ^c   Lee, Tsung Han ^a  

^a NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^b FISHERIES RESEARCH INSTITUTE   (Taiwan)

^c NATIONAL CHIAYI UNIVERSITY   (Taiwan)

Author keywords

Gill; Glucose; Heat shock protein; Na+ K+ ATPase; Salinity; Teleost

Indexed keywords

ACCLIMATION; ENZYME ACTIVITY; GLUCOSE; HOMEOSTASIS; HYPOTHESIS TESTING; INTRODUCED SPECIES; OSMOREGULATION; PHYSIOLOGICAL RESPONSE; PROTEIN; SALINITY; SEAWATER; TELEOST;

CYPRINODONTIFORMES; POECILIA LATIPINNA; TELEOSTEI;

EID: 67649103514     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2009.05.004     Document Type: Article

References (118)

1. Arends R.J., Mancera J.M., Muñoz J.L., Wendelaar Bonga S.E., and Flik G. The stress response of the gilthead sea bream (Sparus aurata L.) to air exposure and confinement. J. Endocrinol. 163 (1999) 149-157
2. Arjona F.J., Vargas-Chacoff L., Ruiz-Jarabo I., Martín del Río M.P., and Mancera J.M. Osmoregulatory response of Senegalese sole (Solea senegalensis) to changes in environmental salinity. Comp. Biochem. Physiol. A 148 (2007) 413-421
3. Bagherie-Lachidan M., Wright S.I., and Kelly S.P. Claudin-3 tight junction proteins in Tetraodon nigroviridis: cloning, tissue-specific expression, and a role in hydromineral balance. Am. J. Physiol. 294 (2008) R1638-R1647
4. Bashamohideen M., and Parvatheswararao V. Adaptations to osmotic stress in the fresh-water euryhaline teleost Tilapia mossambica. IV. Changes in blood glucose, liver glycogen and muscle glycogen levels. Mar. Biol. 16 (1972) 68-74
5. Basu N., Todgham A.E., Ackerman P.A., Bibeau M.R., Nakano K., Schulte P.M., and Iwama G.K. Heat shock protein genes and their functional significance in fish. Gene 295 (2002) 173-183
6. Berra T.M. Freshwater Fish Distribution (2001), Academic Press, London 337-341
7. +-ATPase: heterogeneity in structure, diversity in function. Am. J. Physiol. 275 (1998) F633-F650
8. Bond C.E. Biology of Fishes. 2nd ed. (1996), Saunders College Pub, New York 404-412 425
9. Bruslé J., and Anadon G.G. The structure and function of fish liver. In: Munshi J.S.D., and Dutta H.M. (Eds). Fish Morphology: Horizon of new research (1996), Science Publishers, New York 77-93
10. Buckley B.A., Gracey A.Y., and Somero G.N. The cellular response to heat stress in the goby Gillichthys mirabilis: a cDNA microarray and protein-level analysis. J. Exp. Biol. 209 (2006) 2660-2677
11. +-ATPase α-subunit isoforms α1a and α1b during seawater acclimation of three salmonid fishes that vary in their salinity tolerance. J. Exp. Biol. 209 (2006) 1848-1858
12. Cara J.B., Aluru N., Moyano F.J., and Vijayan M.M. Food-deprivation induces HSP70 and HSP90 protein expression in larval gilthead sea bream and rainbow trout. Comp. Biochem. Physiol. B 142 (2005) 426-431
13. Cataldi E., Mandich A., Ozzimo A., and Cataudella S. The interrelationships between stress and osmoregulation in a euryhaline fish, Oreochromis mossambicus. J. Appl. Ichthyol. 21 (2005) 229-231
14. Chang J.C., Wu S.M., Tseng Y.C., Lee Y.C., Baba O., and Hwang P.P. Regulation of glycogen metabolism in gills and liver of the euryhaline tilapia (Oreochromis mossambicus) during acclimation to seawater. J. Exp. Biol. 210 (2007) 3494-3504
15. +-ATPase and osmotic stress transcription factor 1 mRNA in black porgy, Acanthopagrus schlegeli during osmotic stress. Comp. Biochem. Physiol. B 149 (2008) 91-100
16. Choi C.Y., An K.W., Choi Y.K., Jo P.G., and Min B.H. Expression of warm temperature acclimation-related protein 65-kDa (Wap65) mRNA, and physiological changes with increasing water temperature in black porgy, Acanthopagrus schlegeli. J. Exp. Zool. A 309 (2008) 206-214
17. Claireaux G., and Audet C. Seasonal changes in the hypo-osmoregulatory ability of the brook charr: the role of environmental factors. J. Fish Biol. 56 (2000) 347-373
18. +-ATPase immunoreactivity in branchial chloride cells of Oreochromis mossambicus exposed to copper. J. Exp. Biol. 203 (2000) 379-387
19. De Boeck G., Vlaeminck A., Van der Linden A., and Blust R. The energy metabolism of common carp (Cyprinus carpio) when exposed to salt stress: an increase in energy expenditure or effects of starvation?. Physiol. Biochem. Zool. 73 (2000) 102-111
20. De Jong L., Moreau X., Jean S., Scher O., and Thiéry A. Expression of the heat shock protein Hsp70 in chloride target cells of mayfly larvae from motorway retention pond: a biomarker of osmotic shock. Sci. Total Environ. 366 (2006) 164-173
21. Deane E.E., and Woo N.Y.S. Differential gene expression associated with euryhalinity in sea bream (Sparus sarba). Am. J. Physiol. 287 (2004) R1054-R1063
22. Deane E.E., Kelly S.P., Luk J.C.Y., and Woo N.Y.S. Chronic salinity adaptation modulates hepatic heat shock protein and insulin-like growth factor I expression in black sea bream. Mar. Biotechnol. 4 (2002) 193-205
23. Dietz T.J. Acclimation of the threshold induction temperatures for 70-kDa and 90-kDa heat shock proteins in the fish Gillichthys mirabilis. J. Exp. Biol. 188 (1994) 333-338
24. Diouf B., Rioux P., Blier P.U., and Rajotte D. Use of brook char (Salvelinus fontinalis) physiological responses to stress as a teaching exercise. Adv. Physiol. Educ. 23 (2000) 18-23
25. ++-ATPase, and ouabain-insensitive ATPase in Gillichthys mirabilis. J. Comp. Physiol. 145 (1981) 51-61
26. Eddy F.B., and Bath R.N. Ionic regulation in rainbow trout (Salmo gairdneri) adapted to fresh water and dilute sea water. J. Exp. Biol. 83 (1979) 181-192
27. Evans D.H., Piermarini P.M., and Potts W.T.W. Ionic transport in the fish gill epithelium. J. Exp. Zool. 283 (1999) 641-652
28. Evans D.H., Piermarini P.M., and Choe K.P. The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol. Rev. 85 (2005) 97-177
29. Feder M.E., and Hofmann G.E. Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol. 61 (1999) 243-282
30. Fiess J.C., Kunkel-Patterson A., Mathias L., Riley L.G., Yancey P.H., Hirano T., and Grau E.G. Effects of environmental salinity and temperature on osmoregulatory ability, organic osmolytes, and plasma hormone profiles in the Mozambique tilapia (Oreochromis mossambicus). Comp. Biochem. Physiol. A 146 (2007) 252-264
31. Fiol D.F., and Kültz D. Osmotic stress sensing and signaling in fishes. FEBS J. 274 (2007) 5790-5798
32. Freire C.A., Amado E.M., Souza L.R., Veiga M.P., Vitule J.R., Souza M.M., and Prodocimo V. Muscle water control in crustaceans and fishes as a function of habitat, osmoregulatory capacity, and degree of euryhalinity. Comp. Biochem. Physiol. A 149 (2008) 435-446
33. Frisch A., and Anderson T. Physiological stress responses of two species of coral trout (Plectropomus leopardus and Plectropomus maculatus). Comp. Biochem. Physiol. A 140 (2005) 317-327
34. Froese, R., Pauly, D. (Eds.), 2008. FishBase. World Wide Web electronic publication. www.fishbase.org, version (09/2008).
35. Gonzalez R.J., Cooper J., and Head D. Physiological responses to hyper-saline waters in sailfin mollies (Poecilia latipinna). Comp. Biochem. Physiol. A 142 (2005) 397-403
36. - cotransporter and mitochondria-rich cell distribution in three salmonids Salvelinus namaycush, Salvelinus fontinalis and Salmo salar. J. Exp. Biol. 210 (2007) 1015-1024
37. Hirose S., Kaneko T., Naito N., and Takeib Y. Molecular biology of major components of chloride cells. Comp. Biochem. Physiol. B 136 (2003) 593-620
38. Hsieh S.L., Chen Y.N., and Kuo C.M. Physiological responses, desaturase activity, and fatty acid composition in milkfish (Chanos chanos) under cold acclimation. Aquaculture 220 (2003) 903-918
39. Hwang P.P., and Lee T.H. New insights into fish ion regulation and mitochondrion-rich cells. Comp. Biochem. Physiol. A 148 (2007) 479-497
40. +-activated adenosine triphosphatase from tilapia Oreochromis mossambicus. Bull. Inst. Zool. Acad. Sin. 27 (1988) 49-56
41. +-ATPase activity in tilapia Oreochromis mossambicus during seawater acclimation. Mar. Biol. 100 (1989) 295-299
42. Inokuchi M., Hiroi J., Watanabe S., Lee K.M., and Kaneko T. Gene expression and morphological localization of NHE3, NCC and NKCC1a in branchial mitochondria-rich cells of Mozambique tilapia (Oreochromis mossambicus) acclimated to a wide range of salinities. Comp. Biochem. Physiol. A 151 (2008) 151-158
43. Iwama G.K. Stress in fish. Ann. N.Y. Acad. Sci. 851 (1998) 304-310
44. Iwama G.K., Thomas P.T., Forsyth R.B., and Vijayan M.M. Heat shock protein expression in fish. Rev. Fish Biol. Fish. 8 (1998) 35-56
45. Iwama G.K., Vijayan M.M., Forsyth R., and Ackerman P. Heat shock proteins and physiological stress in fish. Am. Zool. 39 (1999) 901-909
46. Iwama G.K., Afonso L.O., Todgham A., Ackerman P., and Nakano K. Are hsps suitable for indicating stressed states in fish?. J. Exp. Biol. 207 (2004) 15-19
47. Jacob W.F., and Taylor M.H. The time course of seawater acclimation in Fundulus heteroclitus L. J. Exp. Zool. 228 (1983) 33-39
48. +-ATPase in the gills of European sea bass, Dicentrarchus labrax (L.). J. Exp. Zool. 282 (1998) 290-300
49. +-ATPase of two medaka species, Oryzias latipes and Oryzias dancena, with different salinity tolerances acclimated to fresh water, brackish water and seawater. Comp. Biochem. Physiol. A 151 (2008) 566-575
50. Kato A., Doi H., Nakada T., Sakai H., and Hirose S. Takifugu obscurus is a euryhaline fugu species very close to Takifugu rubripes and suitable for studying osmoregulation. BMC Physiol. 5 (2005) 18
51. Kelly S.P., and Woo N.Y.S. Cellular and biochemical characterization of hyposmotic adaptation in a marine teleost, Sparus sarba. Zool. Sci. 16 (1999) 505-514
52. Kelly S.P., Chow I.N.K., and Woo N.Y.S. Haloplasticity of black seabream (Mylio macrocephalus): hypersaline to freshwater acclimation. J. Exp. Zool. 283 (1999) 226-241
53. Kubokawa K., Watanabe T., Yoshioka M., and Iwata M. Effects of acute stress on plasma cortisol, sex steroid hormone and glucose levels in male and female sockeye salmon during the breeding season. Aquaculture 172 (1999) 335-349
54. Kültz D. Plasticity and stressor specificity of osmotic and heat shock responses of Gillichthys mirabilis gill cells. Am. J. Physiol. 271 (1996) C1181-C1193
55. Laiz-Carrión R., Guerreiro P.M., Fuentes J., Canario A.V.M., Martín del Río M.P., and Mancera J.M. Branchial osmoregulatory response to salinity in the gilthead sea bream, Sparus auratus. J. Exp. Zool. 303A (2005) 563-576
56. Laiz-Carrión R., Sangiao-Alvarellos S., Guzmán J.M., Martín del Río M.P., Soengas J.L., and Mancera J.M. Growth performance of gilthead sea bream Sparus aurata in different osmotic conditions: implications for osmoregulation and energy metabolism. Aquaculture 250 (2005) 849-861
57. Langdon J.S. Active osmoregulation in the Australian bass, Macquaria novemaculata (Steindachner), and the golden perch, Macquaria ambigua (Richardson) (Percichthyidae). Aust. J. Mar. Freshw. Res. 38 (1987) 771-776
58. Lee T.H., Hwang P.P., Shieh Y.E., and Lin C.H. The relationship between 'deep-hole' mitochondria-rich cells and salinity adaptation in the euryhaline teleost, Oreochromis mossambicus. Fish Physiol. Biochem. 23 (2000) 133-140
59. Lee T.H., Feng S.H., Lin C.H., Hwang Y.H., Huang C.L., and Hwang P.P. Ambient salinity modulates the expression of sodium pumps in branchial mitochondria-rich cells of Mozambique tilapia, Oreochromis mossambicus. Zool. Sci. 20 (2003) 29-36
60. Leray C., Colin D.A., and Florentz A. Time course of osmotic adaptation and gill energetics of rainbow trout (Salmo gairdneri R) following abrupt changes in external salinity. J. Comp. Physiol. 144 (1981) 175-181
61. Lin C.H., and Lee T.H. Sodium or potassium ions activate different kinetics of gill Na, K-ATPase in three seawater- and freshwater-acclimatized euryhaline teleosts. J. Exp. Zool. A 303 (2005) 57-65
62. Lin Y.M., Chen C.N., and Lee T.H. The expression of gill Na, K-ATPase in milkfish, Chanos chanos, acclimatized to seawater, brackish water and fresh water. Comp. Biochem. Physiol. A 135 (2003) 489-497
63. +-ATPase and the morphometry of mitochondrion-rich cells in gills of euryhalie tilapia (Oreochromis mossambicus) during freshwater acclimation. J. Exp. Zool. A 301 (2004) 85-96
64. Lin C.H., Tsai R.S., and Lee T.H. Expression and distribution of Na, K-ATPase in gills and kidneys of the green spotted pufferfish, Tetraodon nigroviridis, in response to salinity challenge. Comp. Biochem. Physiol. A 138 (2004) 287-295
65. +-ATPase expression in gills of the euryhaline milkfish, Chanos chanos (Forsskl, 1775). Comp. Biochem. Physiol. A 143 (2006) 406-415
66. +-ATPase changes during rapid transfer to sea water of yearling trout, Salmo gairdneri: time course and seasonal variation. J. Fish Biol. 34 (1989) 829-840
67. Mancera J.M., Perez-Figares J.M., and Fernandez-Llebrez P. Osmoregulatory responses to abrupt salinity changes in the euryhaline gilthead sea bream (Sparus aurata L.). Comp. Biochem. Physiol. A 106 (1993) 245-250
68. Manchado M., Salas-Leiton E., Infante C., Ponce M., Asensio E., Crespo A., Zuasti E., and Cañavatea J.P. Molecular characterization, gene expression and transcriptional regulation of cytosolic HSP90 genes in the flatfish Senegalese sole (Solea senegalensis Kaup). Gene 416 (2008) 77-84
69. +ATPase in both chloride and pavement cells. Life Sci. 66 (2000) 1663-1673
70. 2+ transport by fish gills: retrospective review prospective synthesis. J. Exp. Zool. 293 (2002) 264-283
71. Marshall W.S., and Bryson S.E. Transport mechanisms of seawater teleost chloride cells: an inclusive model of a multifunctional cell. Comp. Biochem. Physiol. A 119 (1998) 97-106
72. Miller, S.A., Harley, J.P., 2002. Zoology. 5th ed. McGraw-Hill Companies, New York, pp. 275-283, 425-426, 452-453, 461-463.
73. +-ATPase and ion regulation in juvenile coho salmon. J. Fish Biol. 53 (1998) 1110-1119
74. Mwase M., Viktor T., and Norrgren L. Effects on tropical fish of soil sediments from Kafue River, Zambia. Bull. Environ. Contam. Toxicol. 61 (1998) 96-101
75. Nelson J.S. Fishes of the World. 2nd ed. (1984), John Wiley & Sons, New York 214-222 418
76. - cotransporter and CFTR anion channel in juvenile anadromous and landlocked Atlantic salmon Salmo salar. J. Exp. Biol. 210 (2007) 2885-2896
77. Nordlie F.G., Haney D.C., and Walsh S.J. Comparisons of salinity tolerance and osmotic regulatory capabilities in populations of sailfin molly (Poecilia latipinna) from brackish and fresh waters. Copeia 1992 (1992) 741-746
78. Palmisano A.N., Winton J.R., and Dickhoff W.W. Tissue-specific induction of Hsp90 mRNA and plasma cortisol response in chinook salmon following heat shock, seawater challenge, and handling challenge. Mar. Biotechnol. 2 (2000) 329-338
79. Pan F., Zarate J.M., Tremblay G.C., and Bradley T.M. Cloning and characterization of salmon hsp90 cDNA: upregulation by thermal and hyperosmotic stress. J. Exp. Zool. A 287 (2000) 199-212
80. Parsell D.A., and Lindquist S. The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu. Rev. Genet. 27 (1993) 437-496
81. Perry S.F., Shahsavarani A., Georgalis T., Bayaa M., Furimsky M., and Thomas S.L.Y. Channels, pumps, and exchangers in gill and kidney of freshwater fishes: their role in ionic and acid-base regulation. J. Exp. Zool. A 300 (2003) 53-62
82. Peterson G.L. A simplified method for analysis of inorganic phosphate in the presence of interfering substances. Anal. Biochem. 84 (1978) 164-172
83. Pottinger T.G., and Carrick T.R. A comparison of plasma glucose and plasma cortisol as selection markers for high and low stress-responsiveness in female rainbow trout. Aquaculture 175 (1999) 351-363
84. Ptacek M.B., and Breden F. Phylogenetic relationships among the mollies (Poeciliidae: Poecilia: Mollienesia group) based on mitochondrial DNA sequences. J. Fish Biol. 53 (1998) 64-81
85. Rendell J.L., Fowler S., Cockshutt A., and Currie S. Development-dependent differences in intracellular localization of stress proteins (hsps) in rainbow trout, Oncorhynchus mykiss, following heat shock. Comp. Biochem. Physiol., D 1 (2006) 238-252
86. Rotllant J., and Tort L. Cortisol and glucose responses after acute stress by net handling in the sparid red porgy previously subjected to crowding stress. J. Fish Biol. 51 (1997) 21-28
87. Sakamoto T., Kozaka T., Takahashi A., Kawauchi H., and Ando M. Medaka (Oryzias latipes) as a model for hypoosmoregulation of euryhaline fishes. Aquaculture 193 (2001) 347-354
88. Sakamoto T., Uchida K., and Yokota S. Regulation of the ion-transporting mitochondrial-rich cell during adaptation of teleost to different salinities. Zool. Sci. 18 (2001) 1163-1174
89. Sangiao-Alvarellos S., Arjona F.J., Martín del Río M.P., Míguez J.M., Mancera J.M., and Soengas J.L. Time course of osmoregulatory and metabolic changes during osmotic acclimation in Sparus auratus. J. Exp. Biol. 208 (2005) 4291-4304
90. Sangiao-Alvarellos S., Laiz-Carrión R., Guzmán J.M., Martin del Río M.P., Miguez J.M., Mancera J.M., and Soengas J.L. Acclimation of S. aurata to various salinities alters energy metabolism of osmoregulatory and nonosmoregulatory organs. Am. J. Physiol. 285 (2003) R897-R907
91. Sathiyaa R., Campbell T., and Vijayan M.M. Cortisol modulates HSP90 mRNA expression in primary cultures of trout hepatocytes. Comp. Biochem. Physiol. B 129 (2001) 679-685
92. Scheiner-Bobis G. The sodium pump. Its molecular properties and mechanics of ion transport. Eur. J. Biochem. 269 (2002) 2424-2433
93. Shao, K.T. (Eds.), 2008. Taiwan Fish Database. WWW Web electronic publication. http://fishdb.sinica.edu.tw, version (10/2008).
94. Shikano T., and Fujio Y. Effect of the mother's environmental salinity on seawater tolerance of newborn guppy Poecilia reticulata. Fish. Sci. 64 (1998) 10-13
95. +-ATPase and morphological changes in two types of chloride cells in the gill epithelium during seawater and freshwater adaptation in a euryhaline teleost, Poecilia reticulata. J. Exp. Zool. 281 (1998) 80-89
96. +-ATPase in the gill epithelium during seawater and freshwater adaptation of the guppy, Poecilia reticulata. Zool. Sci. 15 (1998) 35-41
97. Shikano T., and Fujio Y. Strain differences in seawater adaptability in newborn guppy Poecilia reticulata. Fish. Sci. 64 (1998) 987-988
98. Silbergeld E.K. Blood glucose: a sensitive indicator of environmental stress in fish. Bull. Environ. Contam. Toxicol. 11 (1974) 20-25
99. Smith T.R., Tremblay G.C., and Bradley T.M. Hsp70 and a 54 kDa protein (Osp54) are induced in salmon (Salmo salar) in response to hyperosmotic stress. J. Exp. Zool. 284 (1999) 286-298
100. Soengas J.L., Aldegunde M., and Andres M.D. Gradual transfer to sea water of rainbow trout: effects on liver carbohydrate metabolism. J. Fish Biol. 47 (1995) 466-478
101. Tanck M.W.T., Booms G.H.R., Eding E.H., Bonga S.E.W., and Komen J. Cold shocks: a stressor for common carp. J. Fish Biol. 57 (2000) 881-894
102. +-ATPase in gills of tilapia exposed to deionized water. Zool. Sci. 25 (2008) 205-211
103. Tintos A., Míguez J.M., Mancera J.M., and Soengas J.L. Development of a microtitre plate indirect ELISA for measuring cortisol in teleosts, and evaluation of stress responses in rainbow trout and gilthead sea bream. J. Fish Biol. 68 (2006) 251-263
104. +-ATPase expression in the branchial epithelium of brown trout (Salmo trutta) and atlantic salmon (Salmo salar). J. Exp. Zool. 293 (2002) 106-118
105. Tipsmark C.K., Madsen S.S., and Borski R.J. Effect of salinity on expression of branchial ion transporters in striped bass (Morone saxatilis). J. Exp. Zool. A 301 (2004) 979-991
106. Tipsmark C.K., Baltzegar D.A., Ozden O., Grubb B.J., and Borski R.J. Salinity regulates claudin mRNA and protein expression in the teleost gill. Am. J. Physiol. 294 (2008) R1004-R1014
107. Tipsmark C.K., Luckenbach J.A., Madsen S.S., Kiilerich P., and Borski R.J. Osmoregulation and expression of ion transport proteins and putative claudins in the gill of southern flounder (Paralichthys lethostigma). Comp. Biochem. Physiol. A 150 (2008) 265-273
108. Todgahm A.E., Schulte P.M., and Iwama G.K. Cross-tolerance in the tidepool sculpin: the role of heat shock proteins. Physiol. Biochem. Zool. 78 (2005) 133-144
109. Uchida K., Kaneko T., Miyazaki H., Hasegawa S., and Hirano T. Excellent salinity tolerance of Mozambique tilapia (Oreochromis mossambicus): elevated chloride cell activity in the branchial and opercular epithelia of the fish adapted to concentrated seawater. Zool. Sci. 17 (2000) 149-160
110. + ATPase activity during early development of European sea bass, Dicentrarchus labrax: ontogeny and short-term regulation following acute salinity changes. J. Exp. Mar. Biol. Ecol. 311 (2004) 189-200
111. Wang J., Wei Y., Li X., Cao H., Xu M., and Dai J. The identification of heat shock protein genes in goldfish (Carassius auratus) and their expression in a complex environment in Gaobeidian Lake, Beijing, China. Comp. Biochem. Physiol. C 145 (2007) 350-362
112. +-ATPase of the euryhaline teleost, Tetraodon nigroviridis. J. Exp. Biol. 211 (2008) 3750-3758
113. Wegele H., Müller L., and Buchner J. Hsp70 and Hsp90-a relay team for protein folding. Rev. Physiol., Biochem. Pharmacol. 151 (2004) 1-44
114. Wilson J.M., and Laurent P. Fish gill morphology: inside out. J. Exp. Zool. 293 (2002) 192-213
115. Wilson J.M., Antunes J.C., Bouça P.D., and Coimbra J. Osmoregulatory plasticity of the glass eel of Anguilla anguilla: freshwater entry and changes in branchial ion-transport protein expression. Can. J. Fish. Aquat. Sci. 61 (2004) 432-442
116. Wilson J.M., Leitão A., Gonçalves A.F., Ferreira C., Reis-Santos P., Fonseca A.V., da Silva J.M., Antunes J.C., Pereira-Wilson C., and Coimbra J. Modulation of branchial ion transport protein expression by salinity in the glass eels (Anguilla anguilla L.). Mar. Biol. 151 (2007) 1633-1645
117. Woo N.Y.S., and Chung K.C. Tolerance of Pomacanthus imperator to hypoosmotic salinities: changes in body composition and hepatic enzyme activities. J. Fish Biol. 47 (1995) 70-81
118. Yavuzcan-Yi{dotless}ldi{dotless}z H., and Ki{dotless}rkǎgaç-Uzbilek M. The evaluation of secondary stress response of grass carp (Ctenopharyngodon idella, Val. 1844) after exposing to the saline water. Fish Physiol. Biochem. 25 (2001) 287-290