Differential adjustment in gill Na+/K+- and V-ATPase activities and transporter mRNA expression during osmoregulatory acclimation in the cinnamon shrimp Macrobrachium amazonicum (Decapoda, Palaemonidae)

Journal of Experimental Biology

Volumn 213, Issue 22, 2010, Pages 3894-3905

  Faleiros, Rogério Oliveira ^a   Goldman, Maria Helena S ^a   Furriel, Rosa P M ^a   McNamara, John Campbell ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Enzyme activity; Gill epithelial ultrastructure; Ion transporters; Macrobrachium; mRNA expression; Na+ K+ ATPase; Osmoregulation; Palaemonid shrimp; Salinity acclimation; V ATPase

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CHLORIDE; MESSENGER RNA; PRIMER DNA; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ACCLIMATIZATION; AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; ELECTROLYTE BALANCE; GENE EXPRESSION; GENETICS; GILL; HEMOLYMPH; HISTOLOGY; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PALAEMONIDAE; PHYSIOLOGY; SALINITY; SEQUENCE HOMOLOGY; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ACCLIMATIZATION; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CHLORIDES; DNA PRIMERS; GENE EXPRESSION; GILLS; HEMOLYMPH; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; PALAEMONIDAE; RNA, MESSENGER; SALINITY; SEQUENCE HOMOLOGY, AMINO ACID; SODIUM-POTASSIUM-EXCHANGING ATPASE; VACUOLAR PROTON-TRANSLOCATING ATPASES; WATER-ELECTROLYTE BALANCE;

CINNAMOMUM VERUM; DECAPODA (CRUSTACEA); MACROBRACHIUM; MACROBRACHIUM AMAZONICUM; PALAEMONIDAE;

EID: 78649236919     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.046870     Document Type: Article

References (74)

1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
2. Anger, K. (1995). The conquest of freshwater and land by marine crabs: adaptations in life-history patterns and larval bioenergetics. J. Exp. Mar. Biol. Ecol. 193, 119-145.
3. Augusto, A., Greene, L. J., Laure, H. J. and McNamara, J. C. (2007). The ontogeny of isosmotic intracellular regulation in the diadromous, freshwater palaemonid shrimps, Macrobrachium amazonicum and M. olfersi (Crustacea, Decapoda). J. Crust. Biol. 27, 626-634.
4. Augusto, A., Pinheiro, A. S., Greene, L. J., Laure, H. J. and McNamara, J. C. (2009). Evolutionary transition of freshwater by ancestral marine palaemonids: evidence from osmoregulation of in a tide pool shrimp. Aquat. Biol. 7, 113-122.
5. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A. and Struhl, K. (1992). Current protocols in molecular biology, pp. 2.1.1-2.4.5. New York: Greene Publishing Associates & Wiley-Interscience.
6. Belli, N. M., Faleiros, R. O., Firmino, K. C. S., Masui, D. C., Leone, F. A., McNamara, J. C. and Furriel, R. P. M. (2009). Na,K-ATPase activity and epithelial interfaces in gills of the freshwater shrimp Macrobrachium amazonicum (Decapoda, Palaemonidae). Comp. Biochem. Physiol. A Physiol. 152, 431-439.
7. Berger, V. J. and Kharazova, A. D. (1997). Mechanism of salinity adaptation in marine mollusks. Hydrobiologia 355, 115-126.
8. Bond-Buckup, G. and Buckup, L. (1989). Os Palaemonidae de águas continentais do Brasil meridional (Crustacea, Decapoda). Rev. Bras. Biol. 49, 883-896.
9. Chung, K. F. and Lin, H. C. (2006). Osmoregulation and Na,K-ATPase expression in osmoregulatory organs of Scylla paramamosain. Comp. Biochem. Physiol. A Physiol. 144, 48-57.
10. Collart, O. and Rabelo, H. (1996). Variation in egg size of the fresh-water prawn Macrobrachium amazonicum (Decapoda: Palaemonidae). J. Crust. Biol. 16, 684-688.
11. Copeland, D. E. (1968). Fine structure of salt and water uptake in the land crab Gecarcinus lateralis. Am. Zool. 8, 417-432.
12. Copeland, D. E. and Fitzjarrell, A. T. (1968). The salt absorbing cells in the gills of the blue crab (Callinectes sapidus, Rathbun) with notes on modified mitochondria. Z. Zellforsch. 92, 1-22.
13. Dröse, S. and Altendorf, K. (1997). Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases. J. Exp. Biol. 200, 1-8.
14. Evans, D. H., Piermarini, P. M. and Potts, W. T. W. (1999). Ionic transport in the fish gill epithelium. J. Exp. Zool. 283, 641-652.
15. Freire, C. A. and McNamara, J. C. (1995). Fine structure of the gills of the fresh-water shrimp Macrobrachium olfersii (Decapoda): effect of acclimation to high salinity medium and evidence for involvement of the lamellar septum in ion uptake. J. Crust. Biol. 15, 103-116.
16. Freire, C. A., Cavassin, F., Rodrigues, E. M., Torres, A. H. and McNamara, J. C. (2003). Adaptive patterns of osmotic and ionic regulation, and the invasion of fresh water by the palaemonid shrimps. Comp. Biochem. Physiol. A Physiol. 136, 771-778.
17. Freire, C. A., Onken, H. and McNamara, J. C. (2008a). A structure function analysis of ion transport in crustacean gills and excretory organs. Comp. Biochem. Physiol. A Physiol. 51, 272-304.
18. Freire, C. A., Amado, E. M., Souza, L. R., Veiga, M. P., Vitule, J. R., Souza, M. M. and Prodocimo, V. (2008b). Muscle water control in crustaceans and fishes as a function of habitat, osmoregulatory capacity, and degree of euryhalinity. Comp. Biochem. Physiol. A Physiol. 149, 435-446.
19. +)-ATPase in gill microsomes from the freshwater shrimp Macrobrachium olfersii. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 126, 303-315.
20. +-ATPase activity and gill ultrastructure in the hyper-hypo-regulating crab Chasmagnathus granulatus acclimated to dilute, normal, and concentrated seawater. Mar. Biol. 144, 111-118.
21. Gilles, R. and Péqueux, A. (1986). Physiological and ultrastructural studies of NaCl transport in crustacean gills. Boll. Zool. 53, 173-182.
22. Holthuis, L. B. (1952). A general revision of the Palaemonidae (Crustacea, Decapoda, Natantia) of the Americas. II. The subfamily Palaemoninae. Occ. Pap. Allan Hancock Found. 12, 1-136.
23. Jalihal, D. R., Sankolli, K. N. and Shenoy, S. (1993). Evolution of larval development patterns and process of freshwaterization in the prawn genus Macrobrachium Bate, 1868 (Decapoda, Palaemonidae). Crustaceana 65, 365-376.
24. Kamemoto, F. I. (1991). Neuroendocrinology of osmoregulation in crabs. Zool. Sci. 8, 827-833.
25. Kirschner, L. B. (2004). The mechanism of sodium chloride uptake in hyperregulating aquatic animals. J. Exp. Biol. 207, 1439-1452.
26. +-ATPase activities during acclimation to saline media in the freshwater shrimp Macrobrachium olfersii (Wiegmann, 1836) (Decapoda, Palaemonidae). J. Exp. Mar. Biol. Ecol. 215, 81-91.
27. +-ATPase activity in crude homogenates of fish gill tissue: inhibitor sensitivity and environmental and hormonal regulation. J. Exp. Biol. 180, 163-174.
28. Lohrman, D. M. and Kamemoto, F. I. (1987). The effect of dibutyryl cAMP on sodium uptake by isolated perfused gills of Callinectes sapidus. Gen. Comp. Endocrinol. 65, 300-305.
29. Lovett, D. L., Verzi, M. P., Burgents, J. E., Tanner, C. A., Glosmski, K., Lee, J. J. and Towle, D. W. (2006). Expression profiles of Na,K-ATPase during acute and chronic hypo-osmotic stress in the blue crab Callinectes sapidus. Biol. Bull. 211, 58-65.
30. Lowy, R. J., Dawson, D. C. and Ernst, S. A. (1989). Mechanism of ion transport by avian salt gland primary cell cultures. Am. J. Physiol. 256, 1184-1191.
31. 2+ exchange activities in gills of hyperregulating Carcinus maenas. Am. J. Physiol. 276, 490-499.
32. +-ATPase in gills of aquatic crustacea. Comp. Biochem. Physiol. A Physiol. 135, 195-214.
33. Luquet, C. M., Pellerano, G. and Rosa, G. (1997). Salinity-induced changes in the fine structure of the gills of the semiterrestrial estuarine crab Uca uruguayensis. Tissue Cell 29, 495-501.
34. Luquet, C. M., Genovese, G., Rosa, G. A. and Pellerano, G. N. (2002). Ultrastructural changes in the gill epithelium of the crab Chasmagnathus granulatus (Decapoda: Grapsidae) in diluted and concentrated seawater. Mar. Biol. 141, 753-760.
35. Luquet, C. M., Weihrauch, D., Senek, M. and Towle, D. W. (2005). Induction of branchial ion transporter mRNA expression during acclimation to salinity change in the euryhaline crab Chasmagnathus granulatus. J. Exp. Biol. 208, 3627-3636.
36. Martinez, C. B., Harris, R. R. and Santos, M. C. (1998). Transepithelial potential differences and sodium fluxes in isolated perfused gills of the mangrove crab (Ucides cordatus). Comp. Biochem. Physiol. A Physiol. 120, 227-236.
37. +)-ATPase in the swimming crab Callinectes danae: a possible mechanism for regulation of ammonia excretion. Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 132, 471-482.
38. McNamara, J. C. and Lima, A. G. (1997). The route of ion water movements across the gill epithelium of the freshwater shrimp Macrobrachium olfersii (Decapoda, Palaemonidae): evidence from ultrastructural changes induced by acclimation to saline media. Biol. Bull. 192, 321-331.
39. +-ATPase activity and effects of high salinity acclimation in gill and renal epithelia of the freshwater shrimp Macrobrachium olfersii (Crustacea, Decapoda). J. Exp. Zool. 284, 617-628.
40. McNamara, J. C., Moreira, G. S. and Moreira, P. S. (1983). The effects of salinity on respiratory metabolism, survival and moulting in the first zoea of Macrobrachium amazonicum (Heller) (Crustacea, Palaemonidae). Hydrobiologia 101, 239-242.
41. +-phosphatase activity. Comp. Biochem. Physiol. A Physiol. 146, 534-543.
42. Moreira, G. S. and McNamara, J. C. (1986). The effect of salinity on the upper thermal limits of survival and metamorphosis during larval development in Macrobrachium amazonicum (Heller) (Decapoda, Palaemonidae). Crustaceana 50, 231-238.
43. Moreira, G. S., McNamara, J. C., Shumway, S. E. and Moreira, P. S. (1983). Osmoregulation and respiratory metabolism in Brazilian Macrobrachium (Decapoda, Palaemonidae). Comp. Biochem. Physiol. A Physiol. 74, 57-62.
44. Mount, D. B., Delpire, E., Gamba, G., Hall, A. E., Poch, E., Hoover, R. S. and Hebert, S. C. (1998). The electroneutral cation-chloride cotransporters. J. Exp. Biol. 201, 2091-2102.
45. Murphy, N. P. and Austin, C. M. (2005). Phylogenetic relationships of the globally distributed freshwater prawn genus Macrobrachium (Crustacea: Decapoda: Palaemonidae): biogeography, taxonomy and the convergent evolution of abbreviated larval development. Zool. Scripta 34, 187-197.
46. - across posterior gills of Eriocheir sinensis: influence of short-term osmotic variations. J. Exp. Biol. 199, 901-910.
47. - absorption across the gills of Eriocheir sinensis. J. Exp. Biol. 198, 767-774.
48. Onken, H., Tresguerres, M. and Luquet, C. M. (2003). Active NaCl absorption across posterior gills of hyperosmoregulating Chasmagnathus granulatus. J. Exp. Biol. 206, 1017-1023.
49. Paller, M. S. (1994). Lateral mobility of Na,K-ATPase and membrane lipids in renal cells. Importance of cytoskeletal integrity. J. Membr. Biol. 142, 127-135.
50. Péqueux, A. (1995). Osmotic regulation in crustaceans. J. Crust. Biol. 15, 1-60.
51. Pereira, G. and Garcia, A. (1995). Larval development of Macrobrachium reyesi Pereira (Decapoda: Palaemonidae), with a discussion on the origin of abbreviated development in palaemonids. J. Crust. Biol. 15, 117-133.
52. 2+-dependent ATPase activities in shrimp (Macrobrachium amazonicum) gill homogenates. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 97, 383-390.
53. Read, S. M. and Northcote, D. H. (1981). Minimization of variation in the response to different proteins of the Coomassie blue G dye-binding assay for protein. Anal. Biochem. 116, 53-64.
54. Reynolds, E. S. (1963). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208-212.
55. - across the gill epithelium of the Chinese crab Eriocheir sinensis. J. Exp. Biol. 188, 159-174.
56. - across the gill epithelium of the shore crab Carcinus maenas: voltage-clamp and ionflux studies. J. Exp. Biol. 199, 1545-1554.
57. Riordan, J. R., Forbush, B. and Hanrahan, J. W. (1994). The molecular basis of chloride transport in shark rectal gland. J. Exp. Biol. 196, 405-418.
58. Sanger, F., Nicklen, S. and Coulson, A. R. (1977). DNA sequencing with chainterminating inhibitors. Proc. Natl. Acad. Sci. USA 74, 5463-5467.
59. Santos, F. H. and McNamara, J. C. (1996). Neuroendocrine modulation of osmoregulatory parameters in the freshwater shrimp Macrobrachium olfersii (Wiegmann) (Crustacea, Decapoda). J. Exp. Mar. Biol. Ecol. 206, 109-120.
60. +)-ATPase in diadromous, freshwater palaemonid shrimps: species-specific kinetic characteristics and α-subunit expression. Comp. Biochem. Physiol. A Physiol. 148, 178-188.
61. Schales, O. and Schales, S. S. (1941). A simple and accurate method for the determination of chloride in biological fluids. J. Biol. Chem. 140, 879-883.
62. Sollaud, M. E. (1923). Le développment larvaire des 'Palaemoninae'. I. Partie descriptive. La condensation progressive de l'ontogénèse. Bull. Biol. Fr. Belg. 57, 509-603.
63. Sommer, M. J. and Mantel, L. H. (1988). Effect of dopamine, cyclic AMP, and pericardial organs on sodium uptake and Na, K-ATPase activity in gills of the green crab, Carcinus maenas (L). J. Exp. Biol. 248, 272-277.
64. Sommer, M. J. and Mantel, L. H. (1991). Effects of dopamine and acclimation to reduced salinity on the concentration of cyclic AMP in the gills of the green crab, Carcinus maenas (L). Gen. Comp. Endocrinol. 82, 364-368.
65. Sun-Wada, G. H., Tabata, H. and Kawamura, N. (2005). Selective assembly of VATPase subunit isoforms in mouse kidney. J. Bioenerg. Biomembr. 37, 415-418.
66. Taylor, H. H. and Taylor, E. W. (1992). Gills and lungs: the exchange of gases and ions. In Microscopic Anatomy of Invertebrates, Vol. 10. Decapod Crustacea (ed. W. F. Harrison and A. G. Humes), pp. 203-293. New York: Wiley-Liss, Inc.
67. +-ATPase in gill epithelium of two osmoregulating crabs, Callinectes sapidus and Carcinus maenas. J. Exp. Zool. 239, 311-318.
68. Towle, D. W., Rushton, M. E., Heidysch, D., Magnani, J. J., Rose, M. J., Amstutz, A., Jordan, M. K., Shearer, D. W. and Wu, W. S. (1997). Sodium/proton antiporter in the euryhaline crab Carcinus maenas: molecular cloning, expression and tissue distribution. J. Exp. Biol. 200, 1003-1014.
69. +-ATPase in gills of the blue crab Callinectes sapidus: cDNA sequencing and salinity-related expression of α-subunit mRNA and protein. J. Exp. Biol. 204, 4005-4012.
70. +-ATPase (b-subunit) in gills of euryhaline crabs and its physiological role in osmoregulatory ion uptake. J. Exp. Biol. 204, 25-37.
71. Weihrauch, D., McNamara, J. C., Towle, D. W. and Onken, H. (2004). Ion-motive ATPases and active, transbranchial NaCl uptake in the red freshwater crab, Dilocarcinus pagei (Decapoda, Trichodactylidae). J. Exp. Biol. 207, 4623-4631.
72. Zanders, P. and Rodríguez, J. M. (1992). Effects of temperature and salinity stress on osmoionic regulation in adults and on oxygen consumption in larvae and adults of Macrobrachium amazonicum (Decapoda, Palaemonidae). Comp. Biochem. Physiol. A Physiol. 101, 505-509.
73. +-ATPase, and V-ATPase in the freshwater crayfish Cherax destructor (Crustacea: Parastacidae). Comp. Biochem. Physiol. A Physiol. 119, 739-745.
74. Zatta, P. (1987). Dopamine, noradrenaline and serotonin during hypoosmotic stress of Carcinus maenas. Comp. Biochem. Physiol. A Physiol. 96, 479-481.