Short- and long-term, salinity-induced modulation of V-ATPase activity in the posterior gills of the true freshwater crab, Dilocarcinus pagei (Brachyura, Trichodactylidae)

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 160, Issue 1, 2011, Pages 24-31

  Firmino, Kelly Cristina Silva ^a   Faleiros, Rogério Oliveira ^a   Masui, Douglas Chodi ^a   McNamara, John Campbell ^a   Furriel, Rosa Prazeres Melo ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Crustacean gill microsomes; Kinetic characterization; Osmoregulation; True freshwater crab; V ATPase

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; BAFILOMYCIN A1; FRESH WATER; MAGNESIUM ION;

ACCLIMATIZATION; ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CRAB; DILOCARCINUS PAGEI; DRUG PROTEIN BINDING; ENZYME ACTIVITY; ENZYME KINETICS; GILL; ION TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; SALINITY;

BRACHYURA; CRUSTACEA; DECAPODA (CRUSTACEA); DILOCARCINUS PAGEI; TRICHODACTYLIDAE;

EID: 79960083186     PISSN: 10964959     EISSN: 18791107     Source Type: Journal    
DOI: 10.1016/j.cbpb.2011.05.002     Document Type: Article

References (61)

1. Alzamora R., Thali R.F., Gong F., Smolak C., Li H., Baty C.J., Bertrand C.A., Auchli Y., Brunisholz R.A., Neumann D., Hallows K.R., Pastor-Soler N.M. PKA regulates vacuolar H+-ATPase localization and activity via direct phosphorylation of the A subunit in kidney cells. J. Biol. Chem. 2010, 285:24676-24685.
2. Amado E.M., Freire C.A., Souza M.M. Osmoregulation and tissue water regulation in the freshwater red crab Dilocarcinus pagei (Crustacea, Decapoda), and the effect of waterborne inorganic lead. Aquat. Toxicol. 2006, 79:1-8.
3. Augusto A., Greene L.J., Laure H.J., McNamara J.C. Adaptive shifts in osmoregulatory strategy and the invasion of freshwater by brachyuran crabs: evidence from Dilocarcinus pagei (Trichodactylidae). J. Exp. Zool. A 2007, 307:688-698.
4. Belli N.M., Faleiros R.O., Firmino K.C.S., Masui D.C., Leone F.A., McNamara J.C., Furriel R.P.M. Na, K-ATPase activity and epithelial interfaces in gills of the freshwater shrimp Macrobrachium amazonicum (Decapoda, Palaemonidae). Comp. Biochem. Physiol. A 2009, 152:431-439.
5. Beyenbach K.W., Wieczorek H. The V-type H ATPase: molecular structure and function, physiological roles and regulation. J. Exp. Biol. 2006, 209:577-589.
6. Bianchini A., Lauer M.M., Nery L.E.M., Colares P.E., Monserrat J.M., dos Santos E.A. Biochemical and physiological adaptations in the estuarine crab Neohelice granulata during salinity acclimation. Comp. Biochem. Physiol. A 2008, 151:423-436.
7. Dames P., Zimmermann B., Schmidt R., Rein J., Voss M., Schewe B., Walz B., Baumann O. cAMP regulates plasma membrane vacuolar-type H+-ATPase assembly and activity in blowfly salivary glands. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:3926-3931.
8. Demenis M.A., Furriel R.P.M., Leone F.A. Characterization of an ectonucleoside triphosphate diphosphohydrolase 1 activity in alkaline phosphatase-depleted rat osseous plate membranes: possible functional involvement in the calcification process. Biochim. Biophys. Acta. 2003, 1646:216-225.
9. Dröse S., Altendorf K. Bafilomycins and concanamycins as inhibitors of V-ATPases and P-ATPases. J. Exp. Biol. 1997, 200:1-8.
10. Faleiros R.O., Goldman M.H.S., Furriel R.P.M., McNamara J.C. 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). J. Exp. Biol. 2010, 213:3894-3905.
11. Forgac M. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell Biol. 2007, 8:917-929.
12. Freire C.A., Onken H., McNamara J.C. A structure-function analysis of ion transport in crustacean gills and excretory organs. Comp. Biochem. Physiol. A 2008, 151:272-304.
13. Furriel R.P.M., McNamara J.C., Leone F.A. Characterization of (Na+, K+)-ATPase in gill microsomes of the freshwater shrimp Macrobrachium olfersii. Comp. Biochem. Physiol. B 2000, 126:303-315.
14. Furriel R.P.M., Firmino K.C.S., Masui D.C., Faleiros R.O., Torres A.H., McNamara J.C. Structural and biochemical correlates of Na, K-ATPase driven ion uptake across the posterior gill epithelium of the true freshwater crab, Dilocarcinus pagei (Brachyura, Trichodactylidae). J. Exp. Zool. A 2010, 313:508-523.
15. Garçon D.P., Masui D.C., Mantelatto F.L.M., McNamara J.C., Furriel R.P.M., Leone F.A. K+ and NH4+ modulate gill (Na+,K+)-ATPase activity in the blue crab, Callinectes ornatus: fine tuning of ammonia excretion. Comp. Biochem. Physiol. A 2007, 147:145-155.
16. Garçon D.P., Masui D.C., Mantelatto F.L.M., Furriel R.P.M., McNamara J.C., Leone F.A. Hemolymph ionic regulation and adjustments in gill (Na+, K+)-ATPase activity during salinity acclimation in the swimming crab Callinectes ornatus (Decapoda, Brachyura). Comp. Biochem. Physiol. A 2009, 154:44-55.
17. Genovese G., Luchetti C.G., Luquet C.M. Na+/K+-ATPase activity and gill ultrastructure in the hyper-hypo-regulating crab Chasmagnathus granulatus acclimated to dilute, normal, and concentrated seawater. Mar. Biol. 2004, 144:111-118.
18. Genovese G., Ortiz N., Urcola M.R., Luquet C.M. Possible role of carbonic anhydrase, V-H(+)-ATPase, and Cl(-)/HCO3- exchanger in electrogenic ion transport across the gills of the euryhaline crab Chasmagnathus granulatus. Comp. Biochem. Physiol. A 2005, 42:62-69.
19. Greenaway P. Sodium regulation in the freshwater/land crab Holthuisana transversa. J. Comp. Physiol. B 1981, 142:451-456.
20. Heinonen J.K., Lahti R.J. A new and convenient colorimetric determination of inorganic orthophosphate and its application to the assay of inorganic pyrophosphatase. Anal. Biochem. 1981, 113:313-317.
21. Jefferies K., Cipriano D.J., Forgac M. Function, structure and regulation of the vacuolar (H+)-ATPases Arch. Biochem. Biophys. 2008, 476:33-42.
22. Kawasaki-Nishi S., Bowers K., Nishi T., Forgac M., Stevens T.H. The amino-terminal domain of the vacuolar proton translocating ATPase a subunit controls targeting and in vivo dissociation, and the carboxyl-terminal domain affects coupling of proton transport and ATP hydrolysis. J. Biol. Chem. 2001, 276:47411-47420.
23. Kawasaki-Nishi S., Nishi T., Forgac M. Proton translocation driven by ATP hydrolysis in V-ATPases. FEBS Lett. 2003, 545:76-85.
24. Kirschner L.B. The mechanism of sodium chloride uptake in hyperregulating aquatic animals. J. Exp. Biol. 2004, 207:1439-1452.
25. Leone F.A., Baranauskas J.A., Furriel R.P.M., Borin I.A. An easy-to-use program for fitting enzyme kinetic data. Biochem. Mol. Biol. Educ. 2005, 33:399-403.
26. Leone F.A., Furriel R.P.M., McNamara J.C., Mantelatto F.L.M., Masui D.C., Rezende L.A., Gonçalves R.R., Garçon D.P. (Na+, K+)-ATPase from crustacean gill microsomes: a molecular marker to evaluate adaptation to biotopes of different salinity. Trends Comp. Biochem. Physiol. 2005, 11:1-15.
27. Li T.D., Roer R., Vana M., Pate S., Check J. Gill area, permeability and Na+, K+-ATPase activity as a function of size and salinity in the blue crab, Callinectes sapidus. J. Exp. Zool. A 2006, 305:233-245.
28. Lucu C., Towle D.W. Na++K+-ATPase in gills of aquatic crustacea. Comp. Biochem. Physiol. A 2003, 135:195-214.
29. Luquet C.M., Weihrauch D., Senek M., Towle D.W. Induction of branchial ion transporter mRNA expression during acclimation to salinity change in the euryhaline crab Chasmagnathus granulatus. J. Exp. Biol. 2005, 208:3627-3636.
30. MacLeod K.J., Vasilyeva E., Baleja J.D., Forgac M. Mutational analysis of the nucleotide binding sites of the yeast vacuolar proton-translocating ATPase. J. Biol. Chem. 1998, 273:150-156.
31. Magalhães C., Bueno S.L.S., Bond-Buckup G., Valenti W.C., Da Silva H.L.M., Kiyohara F., Mossolin E.C., Rocha S.S. Exotic species of freshwater decapod crustaceans in the state of São Paulo, Brazil: records and possible causes of their introduction. Biodivers. Conserv. 2005, 14:1929-1945.
32. Masui D.C., Silva E.C.C., Mantelatto F.L.M., McNamara J.C., Barrabin H., Scofano H.M., Fontes C.F.L., Furriel R.P.M., Leone F.A. The crustacean gill (Na+, K+)-ATPase: allosteric modulation of high- and low-affinity ATP binding sites by sodium and potassium. Arch. Biochem. Biophys. 2008, 479:139-144.
33. Masui D.C., Mantelatto F.L.M., McNamara J.C., Furriel R.P.M., Leone F.A. Na+, K+-ATPase activity in gill microsomes from the blue crab, Callinectes danae, acclimated to low salinity: novel perspectives on ammonia excretion. Comp. Biochem. Physiol. A 2009, 153:141-148.
34. McNamara J.C., Torres A.H. Ultracytochemical location of Na+/K+-ATPase activity and effect of high salinity acclimation in gill and renal epithelia of the freshwater shrimp Macrobrachium olfersii (Crustacea, Decapoda). J. Exp. Zool. 1999, 284:617-628.
35. McNamara J.C., Zanotto F.P., Onken H. Adaptation to hypoosmotic challenge in brachyuran crabs: a microanatomical and electrophysiological characterization of the intestinal epithelia. J. Exp. Zool. A 2005, 303:880-893.
36. Morris S., Van Aardt W.J. Salt and water relations, and nitrogen excretion, in the amphibious freshwater crab Potamonautes warreni in water and in air. J. Exp. Biol. 1998, 201:883-893.
37. Nakanishi-Matsui M., Sekiya M., Nakamoto R.K., Futai M. The mechanism of rotating proton pumping ATPases. Biochim. Biophys. Acta. 2010, 1797:1343-1352.
38. Nakano M., Imamura H., Toei M., Tamakoshi M., Yoshida M., Yokoyama K. ATP hydrolysis and synthesis of a rotary motor V-ATPase from Thermus thermophilus. J. Biol. Chem. 2008, 283:20789-20796.
39. ODonnell M.J., Dow J.A.T., Huesmann G.R., Tublitz N.J., Maddrell S.H.P. Separate control of anion and cation transport in Malpighian tubules of Drosophila melanogaster. J. Exp. Biol. 1996, 199:1163-1175.
40. Onken H., McNamara J.C. Hyperosmoregulation in the red freshwater crab Dilocarcinus pagei (Brachyura, Trichodactylidae): structural and functional asymmetries of the posterior gills. J. Exp. Biol. 2002, 205:167-175.
41. Onken H., Putzenlechner M. A V-ATPase drives active, electrogenic and Na+-independent Cl- absorption across the gills of Eriocheir sinensis. J. Exp. Biol. 1995, 198:767-774.
42. Onken H., Riestenpatt S. NaCl absorption across split gill lamellae of hyperregulating crabs: transport mechanisms and their regulation. Comp. Biochem. Physiol. A 1998, 119:883-893.
43. Onken H., Schobel A., Kraft J., Putzenlechner M. Active NaCl absorption across split lamellae of posterior gills of the Chinese crab Eriocheir sinensis: stimulation by eyestalk extract. J. Exp. Biol. 2000, 203:1373-1381.
44. Pan L.Q., Zhang L.J., Liu H.Y. Effects of salinity and pH on ion-transport enzyme activities, survival and growth of Litopenaeus vannamei postlarvae. Aquaculture 2007, 273:711-720.
45. Read S.M., Northcote D.H. Minimization of variation in the response to different proteins of the Coomassie Blue-G dye-binding assay for protein. Anal. Biochem. 1981, 116:53-64.
46. Santos L.C.F., Belli N.M., Augusto A., Masui D.C., Leone F.A., McNamara J.C., Furriel R.P.M. Gill (Na+, K+)-ATPase in diadromous, freshwater palaemonid shrimps: species-specific kinetic characteristics and α-subunit expression. Comp. Biochem. Physiol. A 2007, 148:178-188.
47. Saroussi S., Nelson N. The little we know on the structure and machinery of V-ATPase. J. Exp. Biol. 2009, 212:1604-1610.
48. Schubart C.D., Diesel R., Hedges S.B. Rapid evolution to terrestrial life in Jamaican crabs. Nature 1998, 393:363-365.
49. Shaw J. Salt and water balance in the East African freshwater crab, Potamon niloticus (M. Edw.). J. Exp. Biol. 1959, 36:157-179.
50. Stevens T.H., Forgac M. Structure, function and regulation of the vacuolar H+-ATPase. Annu. Rev. Cell Dev. Biol. 1997, 13:779-808.
51. Sun-Wada G.H., Wada Y. Vacuolar-type proton pump ATPases: roles of subunit isoforms in physiology and pathology. Histol. Histopathol. 2010, 25:1611-1620.
52. Sun-Wada G.H., Tabata H., Kawamura N. Selective assembly of V-ATPase subunit isoforms in mouse kidney. J. Bioenerg. Biomembr. 2005, 37:415-418.
53. Toei M., Saum R., Forgac M. Regulation and isoform function of the V-ATPases. Biochemistry 2010, 49:4715-4723.
54. Tresguerres M., Parks S.K., Sabatini S.E., Goss G.G., Luquet C.M. Regulation of ion transport by pH and [HCO3-] in isolated gills of the crab Neohelice (Chasmagnathus) granulata. Am. J. Physiol. 2008, 294:R1033-R1043.
55. Tsai J.R., Lin H.C. V-type H+-ATPase and Na+, K+-ATPase in the gills of 13 euryhaline crabs during salinity acclimation. J. Exp. Biol. 2007, 210:620-627.
56. Voss M., Vitavska O., Walz B., Wieczorek H., Baumann O. Stimulus-induced phosphorylation of vacuolar H+-ATPase by protein kinase A. J. Biol. Chem. 2007, 282:33735-33742.
57. Voss M., Blenau W., Walz B., Baumann O. V-ATPase deactivation in blowfly salivary glands is mediated by protein phosphatase 2c. Arch. Insect Biochem. Physiol. 2009, 71:130-138.
58. Wang Y., Inoue T., Forgac M. Subunit a of the yeast V-ATPase participates in binding of bafilomycin. J. Biol. Chem. 2005, 280:40481-40488.
59. Weihrauch D., Ziegler A., Siebers D., Towle D.W. Molecular characterization of V-type H+-ATPase (B-subunit) in gills of euryhaline crabs and its physiological role in osmoregulatory ion uptake. J. Exp. Biol. 2001, 204:25-37.
60. Weihrauch D., Ziegler A., Siebers D., Towle D.W. Active ammonia excretion across the gills of the green shore crab Carcinus maenas: participation of Na+/K+-ATPase, V-type H+-ATPase and functional microtubules. J. Exp. Biol. 2002, 205:2765-2775.
61. Weihrauch D., McNamara J.C., Towle D.W., Onken H. Ion-motive ATPases and active, transbranchial NaCl uptake in the red freshwater crab, Dilocarcinus pagei (Decapoda, Trichodactylidae). J. Exp. Biol. 2004, 207:4623-4631.