Skip to main content
Log in

Gill (Na+, K+)-ATPase from the Amazon River shrimp, Macrobrachium amazonicum (Decapoda, Palaemonidae): effect of exogenous biogenic amines on enzyme activity in juveniles and adults

  • ADAPTA
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Despite the biological and economic importance of the freshwater shrimp Macrobrachium amazonicum, a role for biogenic amines in the osmoregulatory capability of this diadromous species remains unstudied. This investigation provides an extensive kinetic characterization of the effects of the exogenous polyamines spermine, spermidine, and putrescine on (Na+, K+)-ATPase activity in gill microsomal preparations from juvenile and adult shrimps at varying concentrations of ATP, Mg2+, Na+, and K+, and on inhibition by ouabain. (Na+, K+)-ATPase activity in both juvenile and adult shrimps is inhibited by spermidine (60–95%) and putrescine (40–70%) while spermine has a negligible inhibitory effect (<10%). Putrescine affects the kinetics of ATP hydrolysis and enzyme affinity (K M) for ATP in both enzymes, while spermidine alters specific activity only. Spermidine increases Mg2+ affinity of the adult (Na+, K+)-ATPase while putrescine decreases Mg2+ affinity in both enzymes. Spermidine decreases Na+ affinity by ≈50% in both enzymes, while putrescine increases affinity of the juvenile enzyme twofold. These biogenic amines cause slight changes in K M values in both enzymes. These findings suggest that the effect of biogenic amines on gill (Na+, K+)-ATPase activity and kinetics may be species and stage specific.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Albers, R. W., 1967. Biochemical aspects of active transport. Annual Review of Biochemistry 6: 727–756.

    Article  Google Scholar 

  • Araujo, M. C. & W. C. Valenti, 2007. Feeding habit of the Amazon River prawn Macrobrachium amazonicum larvae. Aquaculture 265: 187–193.

    Article  Google Scholar 

  • Augusto, A. S., L. J. Greene, H. L. Laure & J. C. McNamara, 2009. The ontogeny of isosmotic intracellular regulation in the diadromous, freshwater palaemonid shrimps, Macrobrachium amazonicum and M. olfersii (Decapoda). Journal of Crustacean Biology 27: 626–634.

    Article  Google Scholar 

  • Axelsen, M. G. & K. B. Palmgren, 1998. Evolution of P-type ATPases. Biochimica and Biophysica Acta 1365: 37–45.

    Article  Google Scholar 

  • Belli, N. M., R. O. Faleiros, K. C. S. Firmino, D. C. Masui, F. A. Leone, J. C. McNamara & R. P. M. Furriel, 2009. Na, K-ATPase activity and epithelial interfaces in gills of the freshwater shrimp Macrobrachium amazonicum (Decapoda, Palaemonidae). Comparative Biochemistry and Physiology 152A: 431–439.

    Article  CAS  Google Scholar 

  • Blanco, G. & R. W. Mercer, 1998. Isozymes of the (Na+, K+)-ATPase: heterogeneity in structure, diversity in function. American Journal of Physiology 44: F633–F650.

    Google Scholar 

  • Blanco, G., K. Wagoner, G. Sanchez & G. C. Enders, 2005. Ontogeny of the Na, K-ATPase alpha 4 isoform during rat male germ cell development. FASEB Journal 19: A1153.

    Google Scholar 

  • Brink, B., C. Damink, H. M. L. J. Joosten & J. H. J. Huis In’t Veld, 1990. Occurrence and formation of biologically active amines in foods. International Journal of Food Microbiology 11: 73–84.

    Article  PubMed  Google Scholar 

  • Charmantier, G. & K. Anger, 2011. Ontogeny of osmoregulatory patterns in the South American shrimp Macrobrachium amazonicum: loss of hypo-regulation in a land-locked population indicates phylogenetic separation from estuarine ancestors. Journal of Experimental Marine Biology and Ecology 396: 89–98.

    Article  Google Scholar 

  • Chong-Robles, J., G. Charmantier, V. Boulo, J. Lizarraga-Valdéz, L. M. Enríquez-Paredes & I. Giffard-Mena, 2014. Osmoregulation pattern and salinity tolerance of the white shrimp Litopenaeus vannamei (Boone, 1931) during post-embryonic development. Aquaculture 422–423: 261–267.

    Article  Google Scholar 

  • Corotto, F. S. & C. W. Holliday, 1996. Branchial (Na+, K+)-ATPase and osmoregulation in the purple shore crab Hemigrapsus nudus (Dana). Comparative Biochemistry and Physiology 113A: 361–368.

    Article  CAS  Google Scholar 

  • Crambert, G., U. Hasler, A. T. Beggah, C. L. Yu, N. N. Modyanov, J. D. Horisberger, L. Lelievre & K. Geering, 2000. Transport and pharmacological properties of nine different human isozymes. Journal of Biological Chemistry 275: 1976–1986.

    Article  CAS  PubMed  Google Scholar 

  • D’Orazio, S. E. & C. W. Holliday, 1985. Gill Na, K-ATPase e osmorregulation in the se fiddler crab, Uca pugilator. Physiological Zoology 58: 364–373.

    Article  Google Scholar 

  • Faleiros, R. O., M. H. S. Goldman, R. P. M. Furriel & J. C. McNamara, 2010. Differential adjustment in Gill Na+/K+- and V-ATPase activities and transporter mRNA expression during osmorregulatory acclimation in the cinnamom shrimp Macrobrachium amazonicum (Decapoda, Palaemonidae). Journal of Experimental Biology 213: 3894–3905.

    Article  CAS  PubMed  Google Scholar 

  • FAO, 2011. Fishstat Plus (v. 2.32) Food and Agriculture Organization, Rome

  • Fedosova, N. U., F. Cornelius & I. Klodos, 1998. E2P phosphoforms of (Na+, K+)-ATPase. I: comparison of phosphointermediates formed from ATP e Pi by their reactivity toward hydroxylamine e vanadate. Biochemistry 37: 13634–13642.

    Article  CAS  PubMed  Google Scholar 

  • Fontes, C. F. L., H. Barrabin, H. M. Scofano & J. G. Norby, 1992. The role of Mg2+ and K+ in the phosphorylation of Na+, K+-ATPase by ATP in the presence of dimethyl sulfoxide but in the absence of Na+. Biochimica and Biophysica Acta 1104: 215–225.

    Article  CAS  Google Scholar 

  • França, J. L., M. R. Pinto, M. N. Lucena, D. P. Garçon, W. C. Valenti, J. C. McNamara & F. A. Leone, 2013. Subcellular localization and kinetic characterization of a gill (Na+, K+)-ATPase from the giant freshwater prawn Macrobrachium rosenbergii. Journal of Membrane Biology 246: 529–543.

    Article  PubMed  Google Scholar 

  • Freire, C. A., H. Onken & J. C. McNamara, 2008. A structure-function analysis of ion transport in crustacean gills and excretory organs. Comparative Biochemistry and Physiology 151A: 272–304.

    Article  CAS  Google Scholar 

  • Furriel, R. P. M., J. C. McNamara & F. A. Leone, 2000. Characterization of (Na+, K+)-ATPase in gill microsomes of the freshwater shrimp Macrobrachium olfersii. Comparative Biochemistry and Physiology 126B: 303–315.

    Article  CAS  Google Scholar 

  • Furriel, R. P. M., K. C. S. Firmino, D. C. Masui, R. O. Faleiros, A. H. Torres & J. C. McNamara, 2010. Structural e biochemical correlates of (Na+, K+)-ATPase driven ion uptake across the true freshwater crab, Dilocarcinus pagei Brachyura, Trichodactylidae. Journal of Experimental Zoology 313A: 508–523.

    Article  CAS  Google Scholar 

  • Garçon, D. P., D. C. Masui, F. L. M. Mantelatto, J. C. McNamara, R. P. M. Furriel & F. A. Leone, 2007. K+ and NH4 + modulate gill (Na+, K+)-ATPase activity in the blue crab, Callinectes ornatus: fine tuning of ammonia excretion. Comparative Biochemistry and Physiology 147A: 145–155.

    Article  Google Scholar 

  • Garçon, D. P., M. N. Lucena, J. L. França, J. C. McNamara, C. F. L. Fontes & F. A. Leone, 2011. Na+, K+-ATPase activity in the posterior gills of the blue crab, Callinectes ornatus (Decapoda, Brachyura): modulation of ATP hydrolysis by the biogenic amines spermidine and spermine. Journal of Membrane Biology 244: 9–20.

    Article  PubMed  Google Scholar 

  • Garty, H. & S. J. Karlish, 2006. Role of FXYD proteins in ion transport. Annual Review of Physiology 68: 431–459.

    Article  CAS  PubMed  Google Scholar 

  • Geering, K., 2001. The functional role of beta subunits in oligomeric P-type ATPases. Journal of Bioenergetics and Biomembranes 33: 425–438.

    Article  CAS  PubMed  Google Scholar 

  • Geering, K., 2008. Functional roles of Na, K-ATPase subunits. Current Opinion in Nephrology and Hypertension 17: 526–532.

    Article  CAS  PubMed  Google Scholar 

  • Glynn, I. M., 1985. The (Na+K+)-transporting adenosine triphosphatase. In Martonosi, A. N. (ed.), The enzymes of biological membranes, Vol. 3. Plenum Press, New York: 35–114.

    Chapter  Google Scholar 

  • Gonçalves, R. R., D. C. Masui, J. C. McNamara, F. L. M. Mantelatto, D. P. Garçon, R. P. M. Furriel & F. A. Leone, 2006. A kinetic study of the gill (Na+, K+)-ATPase, and its role in ammonia excretion in the intertidal hermit crab, Clibanarius vittatus. Comparative Biochemistry and Physiology 145A: 346–356.

    Article  Google Scholar 

  • Guest, W. C., 1979. Laboratory life history of the palaemonid shrimp Macrobrachium amazonicum (Heller) (Decapoda, Palaemonidae). Crustaceana 37: 141–152.

    Article  Google Scholar 

  • Hayd, L. & K. Anger, 2013. Reproductive and morphometric traits of Macrobrachium amazonicum (Decapoda, Palaemonidae) from the Pantanal, Brazil, suggests initial speciation. Revista de Biologia Tropical 61: 39–57.

    PubMed  Google Scholar 

  • Hayd, L. A., K. Anger & W. C. Valenti, 2008. The moulting cycle of larval amazon river prawn Macrobrachium amazonicum reared in the laboratory. Nauplius 16: 55–63.

    Google Scholar 

  • Heinrich-Hirsch, B., J. Ahlers & H. W. Peter, 1977. Inhibition of Na+, K+-ATPase from chick brain by polyamines. Enzyme 22: 235–241.

    CAS  PubMed  Google Scholar 

  • Henry, R. P., 2001. Environmentally mediated carbonic anhydrase induction in the gills of euryhaline crustaceans. Journal of Experimental Biology 204: 991–1002.

    CAS  PubMed  Google Scholar 

  • Henry, R. P., C. Lucu, H. Onken & D. Weihrauch, 2012. Multiple functions of the crustacean gill: osmotic/ionic regulation, acid-base balance, ammonia excretion, and bioaccumulation of toxic metals. Frontiers in Physiology 3: 1–33.

    Article  Google Scholar 

  • Holliday, C. W., 1985. Salinity-induced changes in gill (Na+, K+)-ATPase activity in the mud fiddler crab Uca pugnax. Journal of Experimental Zoology 233: 199–208.

    Article  CAS  Google Scholar 

  • Holthuis, L. B., 1952. A general revision of the Palaemonidae (Crustacea Decapoda Natantia) of the Americas. II. The subfamily Palaemonidae. Occasional Paper 12. Allan Hancock Foundations Publications: 396 pp.

  • Horisberger, J. D., 2004. Recent insights into the structure and mechanism of the sodium pump. Physiology 19: 377–388.

    Article  CAS  PubMed  Google Scholar 

  • Iarashi, K. & K. Kashiwagi, 2010. Modulation of cellular function by polyamines. International Journal of Biochemistry and Cell Biology 42: 39–51.

    Article  Google Scholar 

  • Jantaro, S., P. Maenpaa, P. Mulo & A. Incharoensakdi, 2003. Content and biosynthesis of polyamines in salt e osmotically stressed cells of Synechocystis sp PCC 6803. FEMS Microbiology Letters 228: 129–135.

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen, P. L., J. M. Nielsen, J. H. Rasmussen & P. A. Pedersen, 1998. Structure-function relationships based on E1-E2 transitions and cation binding in NaK-pump protein. Biochimica and Biophysica Acta 1365: 65–70.

    Article  CAS  Google Scholar 

  • Kalac, P., 2009. Recent advances in the research on biological roles of dietary polyamines in man. Journal of Applied Biomedicine 7: 65–74.

    CAS  Google Scholar 

  • Kanai, R., H. Ogawa, B. Vilsen, F. Cornelius & C. Toyoshima, 2013. Crystal structure of a Na+-bound (Na+, K+)-ATPase preceding the E1 state. Nature 502: 201–207.

    Article  CAS  PubMed  Google Scholar 

  • Kaplan, J. H., 2002. Biochemistry of Na, K-ATPase. Annual Review of Biochemistry 71: 511–535.

    Article  CAS  PubMed  Google Scholar 

  • Karlish, S. J., 2003. Investigating the energy transduction mechanism of P-type ATPases with Fe2+- catalyzed oxidative cleavage. Annals of New York Academy of Sciences 986: 39–49.

    Article  CAS  Google Scholar 

  • Kobayashi, M., H. Fujisaki, M. Sugawara, K. Iseki & K. Miyazaki, 1999. The presence of an Na+/spermine antiporter in the rat renal brush-border membrane. Journal of Pharmacia and Pharmacology 51: 279–284.

    Article  CAS  Google Scholar 

  • Kuntzweiler, T. A., E. T. Wallick, C. L. Johnson & J. B. Lingrel, 1995. Glutamic-acid-327 in the sheep alpha-1 isoform of (Na+, K+)-ATPase stabilizes a K+-induced conformational change. Journal of Biological Chemistry 270: 2993–3000.

    Article  CAS  PubMed  Google Scholar 

  • Lee, C. E., M. Kiergaard, G. W. Gelembiuk, B. D. Eads & M. Posavi, 2011. Pumping ions: rapid parallel evolution of ionic regulation following habitat invasions. Evolution 65: 2229–2244.

    Article  CAS  PubMed  Google Scholar 

  • Leone, F. A., J. A. Baranauskas, R. P. M. Furriel & I. A. Borin, 2005. SigrafW: an easy-to-use program for fitting enzyme kinetic data. Biochemistry and Molecular Biology Education 33: 399–403.

    Article  CAS  PubMed  Google Scholar 

  • Leone, F. A., D. C. Masui, T. M. S. Bezerra, D. P. Garçon, W. C. Valenti, A. S. Augusto & J. C. McNamara, 2012. Kinetic analysis of gill (Na+, K+)-ATPase activity in selected ontogenetic stages of the Amazon river shrimp, Macrobrachium amazonicum (Decapoda, Palaemonidae): interactions at ATP- and cation-binding sites. Journal of Membrane Biology 245: 201–215.

    Article  CAS  PubMed  Google Scholar 

  • Leone, F. A., M. N. Lucena, L. A. Rezende, D. P. Garçon, M. R. Pinto, F. L. M. Mantelatto & J. C. McNamara, 2015. Kinetic characterization and immunolocalization of (Na+, K+)-ATPase activity from gills of the marine seabob shrimp Xiphopenaeus kroyeri (Decapoda, Penaeidae). Journal of Membrane Biology 248: 257–272.

    Article  CAS  PubMed  Google Scholar 

  • Liu, H. Y., L. Q. Pan & D. Zheng, 2008. Effects of salinity on biogenic amines, hemolymph osmotic pressure, and activity of gill’s Na+/K+-ATPase in Charybdis japonica (Crustacea, Decapoda). Journal of the World Aquaculture Society 39: 812–820.

    Article  Google Scholar 

  • Lopez, L. B., L. E. M. Quintas & F. Noel, 2002. Influence of development on Na+/K+-ATPase expression: isoform- and tissue-dependency. Comparative Biochemistry and Physiology Part A 131: 323–333.

    Article  Google Scholar 

  • Lovett, D. L. & S. A. Watts, 1995. Changes in polyamine levels in response to acclimation salinity in gills of the blue-crab Callinectes-sapidus rathbun. Comparative Biochemistry and Physiology 110B: 115–119.

    Article  CAS  Google Scholar 

  • Lucena, M. N., D. P. Garçon, F. L. M. Mantelatto, M. R. Pinto, J. C. McNamara & F. A. Leone, 2012. Hemolymph ion regulation and kinetic characteristics of the gill (Na+K+)-ATPase in the hermit crab Clibanarius vittatus (Decapoda Anomura) acclimated to high salinity. Comparative Biochemistry and Physiology 161B: 380–391.

    Article  Google Scholar 

  • Lucu, C. & D. W. Towle, 2003. (Na+, K+)-ATPase in gills of aquatic crustacea. Comparative Biochemistry and Physiology 135A: 195–214.

    Article  CAS  Google Scholar 

  • Magalhães, C., S. L. S. Bueno, G. Bond-Buckup, W. C. Valenti, H. L. M. Silva, F. Kiyohara, E. C. Mossolin & S. S. Rocha, 2005. Exotic species of freshwater decapod crustaceans in the state of São Paulo, Brazil: records and possible causes of their introduction. Biodiversity and Conservation 14: 1929–1945.

    Article  Google Scholar 

  • Marks, M. J. & N. W. Seeds, 1978. A heterogeneous ouabain-ATPase interaction in mouse brain. Life Sciences 23: 2735–2744.

    Article  CAS  PubMed  Google Scholar 

  • Masui, D. C., R. P. M. Furriel, J. C. McNamara, F. L. M. Mantelatto & F. A. Leone, 2002. Modulation by ammonium ions of gill microsomal (Na+, K+)-ATPase in the swimming crab Callinectes danae: a possible mechanism for regulation of ammonia excretion. Comparative Biochemistry and Physiology 132C: 471–482.

    CAS  Google Scholar 

  • McNamara, J. C. & S. C. Faria, 2012. Evolution of osmoregulatory patterns and gill ion transport mechanisms in the decapod Crustacea: a review. Comparative Biochemistry and Physiology 182B: 997–1014.

    Google Scholar 

  • McNamara, J. C. & A. G. Lima, 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. Biological Bulletin 192: 321–331.

    Article  Google Scholar 

  • McNamara, J. C. & A. H. Torres, 1999. Ultracytochemical location of Na+/K+-ATPase activity and effects of high salinity acclimation in gill and renal epithelia of the freshwater shrimp Macrobrachium olfersii (Crustacea, Decapoda). Journal of Experimental Zoology 284: 617–628.

    Article  CAS  PubMed  Google Scholar 

  • Meier, S., N. N. Tavraz, K. L. Dürr & T. Friedrich, 2010. Hyperpolarization-activated inward leakage currents caused by deletion or mutation of carboxy-terminal tyrosines of the Na+/K+-ATPase α-subunit. Journal of General Physiology 135: 115–134.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moraes-Valenti, P. M. C. & W. C. Valenti, 2010. Culture of the Amazon River Prawn Macrobrachium amazonicum. In New, M. B., W. C. Valenti, J. H. Tidwell, L. R. D’Abramo & M. N. Dutty (eds.), Freshwater Prawns: Biology and Farming. Wiley-Blackwell, Oxford: 485–501.

    Google Scholar 

  • Moreira, G. S., J. C. McNamara & P. S. Moreira, 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.

    Article  Google Scholar 

  • Morris, S. & T. Edwards, 1995. Control of osmoregulation via regulation of Na+/K+-ATPase activity in the amphibious purple shore crab, Leptograpsus variegatus. Comparative Biochemistry and Physiology Part C 112: 129–136.

    Google Scholar 

  • Morth, J. P., B. P. Pedersen, M. S. Toustrup-Jensen, T. L. M. Sorensen, J. Petersen, J. P. Eersen, B. Vilsen & P. Nissen, 2007. Crystal structure of the sodium–potassium pump. Nature 450: 1043–1050.

    Article  CAS  PubMed  Google Scholar 

  • Morth, J. P., H. Poulsen, M. S. Toustrup-Jensen, V. R. Schack, J. Egebjerg, J. P. Andersen, B. Vilsen & P. Nissen, 2009. The structure of the Na+, K+-ATPase and mapping of isoform differences and disease-related mutations. Philosophical Transactions of the Royal Society B 364: 217–227.

    Article  CAS  Google Scholar 

  • New, M. B., 2010. History and global status of freshwater prawn farming. In New, M. B., W. C. Valenti, J. H. Tidwell, L. R. D’Abramo & M. N. Dutty (eds.), Freshwater Prawns: Biology and Farming. Wiley-Blackwell, Oxford: 1–11.

    Google Scholar 

  • Nielsen, J. M., P. A. Pedersen, S. J. D. Karlish & P. L. Jorgensen, 1998. Importance of intramembrane carboxylic acids for occlusion of K+ ions at equilibrium in renal Na, K-ATPase. Biochemistry 37: 1961–1968.

    Article  CAS  PubMed  Google Scholar 

  • Nyblom, M., H. Poulsen, P. Gourdon, L. Reinhard, M. Andersson, E. Lindahl, N. Fedosova & P. Nissen, 2013. Crystal structure of Na+, K+-ATPase in the Na+-bound state. Science 342: 123–127.

    Article  CAS  PubMed  Google Scholar 

  • Pantaleão, J. A. F., G. L. Hirose & R. C. Costa, 2014. Occurrence of male morphotypes of Macrobrachium amazonicum (Caridea, Palaemonidea) in a population with an entirely freshwater life cycle. Brazilian Journal of Biology 74: S223–S232.

    Article  Google Scholar 

  • Pedemonte, C. H. & L. A. Beaugé, 1983. Inhibition of (Na+, K+)-ATPase by magnesium ions and inorganic phosphate and release of these ligands in the cycles of ATP hydrolysis. Biochimica and Biophysica Acta 748: 245–253.

    Article  CAS  Google Scholar 

  • Pegg, A. E., 2009. Mammalian polyamine metabolism and function. IUBMB Life 61: 880–894.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Péqueux, A., 1995. Osmotic regulation in crustaceans. Journal of Crustacean Biology 15: 1–60.

    Article  Google Scholar 

  • Péqueux, A., P. Labras, C. Cann-Moisan, J. Coroff & P. Sebert, 2002. Polyamines, indolamines, and catecholamines in gills and haemolymph of the euryhaline crab, Eriocheir sinensis. Effects of high pressure and salinity. Crustaceana 75: 567–578.

    Article  Google Scholar 

  • Pileggi, L. A. & F. L. Mantelatto, 2012. Taxonomic revision of doubtful Brazilian freshwater shrimp species of the genus Macrobrachium (Decapoda, Palaemonidae). Iheringia, Série Zoologia 102: 426–437.

    Article  Google Scholar 

  • Post, R. L., C. Hegyvary & S. Kume, 1972. Activation by adenosine triphosphate in the phosphorylation kinetics of sodium and potassium ion transport adenosine triphosphatase. Journal of Biological Chemistry 247: 6530–6540.

    CAS  PubMed  Google Scholar 

  • Poulsen, H., P. Morth, J. Egebjerg & P. Nissen, 2010. Phosphorylation of the (Na+, K+)-ATPase and the H+, K+-ATPase. FEBS Letters 584: 2589–2595.

    Article  CAS  PubMed  Google Scholar 

  • Pressley, T. A., 1992. Ionic regulation of Na+-ATPase, K+-ATPase expression. Seminars in Nephrology 12: 67–71.

    CAS  PubMed  Google Scholar 

  • Quarfoth, G., K. Ahmed & D. Foster, 1978. Effects of polyamines on partial reactions of membrane (Na+K+)-ATPase. Biochimica and Biophysica Acta 526: 580–590.

    Article  CAS  Google Scholar 

  • Read, S. M. & D. H. Northcote, 1981. Minimization of variation in the response to different proteins of the Coomassie blue-G dye-binding assay for protein. Analytical Biochemistry 116: 53–64.

    Article  CAS  PubMed  Google Scholar 

  • Robinson, J. D., 1982. Tryptic digestion of the (Na + K)-ATPase is both sensitive to and modifies K+ interactions with the enzyme. Journal of Bioenergetics and Biomembranes 14: 319–333.

    Article  CAS  PubMed  Google Scholar 

  • Robinson, J. D., C. A. Leach & L. J. Robinson, 1986. Cation sites, spermine, e the reaction sequence of the (Na+K+)-dependent ATPase. Biochimica and Biophysica Acta 856: 536–544.

    Article  CAS  Google Scholar 

  • Santos, L. C. F., N. M. Belli, A. Augusto, D. C. Masui, F. A. Leone, J. C. McNamara & R. P. M. Furriel, 2007. Gill (Na+, K+)-ATPase in diadromous, freshwater palaemonid shrimps: species-specific kinetic characteristics and α-subunit expression. Comparative Biochemistry and Physiology 148A: 178–188.

    Article  CAS  Google Scholar 

  • Seiler, N. & F. Dezeure, 1990. Polyamine transport in mammalian cells. International Journal of Biochemistry 22: 211–218.

    Article  CAS  PubMed  Google Scholar 

  • Shindo, Y., K. Morishita, E. Kotake, H. Miura, P. Carninci, J. Kawai, Y. Hayashizaki, A. Hino, T. Kanda & Y. Kusakabe, 2011. FXYD6, a (Na, K)-ATPase regulator, is expressed in type II taste cells. Bioscience, Biotechnology and Biochemistry 75: 1061–1066.

    Article  CAS  Google Scholar 

  • Shinoda, T., H. Ogawa, F. Cornelius & C. Toyoshima, 2009. Crystal structure of the sodium-potassium pump at 2.4 Å resolution. Nature 459: 446–451.

    Article  CAS  PubMed  Google Scholar 

  • Silva, E. C. C., D. C. Masui, R. P. Furriel, F. L. M. Mantelatto, J. C. McNamara, H. Barrabin, H. M. Scofano, F. A. Leone & C. F. L. Fontes, 2008. Regulation by the exogenous polyamine spermidine of Na, K-ATPase activity from the gills of the euryhaline swimming crab Callinectes danae (Brachyura, Portunidae). Comparative Biochemistry and Physiology 149B: 622–629.

    Article  CAS  Google Scholar 

  • Silva, E. C. C., D. C. Masui, R. P. Furriel, J. C. McNamara, H. Barrabin, H. M. Scofano, J. Perales, A. Teixeira-Ferreira, F. A. Leone & C. F. L. Fontes, 2012. Identification of a crab gill FXYD2 protein and regulation of crab microsomal Na, K-ATPase activity by mammalian FXYD2 peptide. Biochimica and Biophysica Acta 1818: 2588–2597.

    Article  CAS  Google Scholar 

  • Tabor, C. W. & H. Tabor, 1984. Polyamines. Annual Review Biochemistry 53: 749–790.

    Article  CAS  Google Scholar 

  • Tashima, Y., M. Hasegawa & H. Mizunuma, 1978. Activation of (Na+K+)-adenosine triphosphatase by spermine. Biochemical and Biophysical Research Communications 82: 13–18.

    Article  CAS  PubMed  Google Scholar 

  • Tentes, I. & E. Stratakis, 1991. Partial purification and properties of (Na+, K+)-ATPase from Potamon potamios. Comparative Biochemistry and Physiology 100C: 619–624.

    CAS  Google Scholar 

  • Torres, A. H., H. Onken & J. C. McNamara, 2003. Como as brânquias de um camarão de água doce capturam Na+, Ca2+ e Cl do meio ambiente: uma abordagem eletrofisiológica qualitativa. In: XVIII Reunião Anual da Federação das Sociedades de Biologia Experimental. Abstract #11.022.

  • Tribuzy, A. V. B., C. F. L. Fontes, J. G. Norby & H. Barrabin, 2002. Dimethyl sulfoxide-induced conformational state of Na+/K+-ATPase studied by proteolytic cleavage. Archives of Biochemistry and Biophysics 399: 89–95.

    Article  CAS  Google Scholar 

  • Yoda, A. & S. Yoda, 1982. Interaction between ouabain and the phosphorylated intermediate of (Na+, K+)-ATPase. Molecular Pharmacology 22: 700–705.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This investigation was financed by research grants from the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP 2010/17534-0 and 2013/22605-1), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and Instituto Nacional de Ciência e Tecnologia ADAPTA (INCT ADAPTA, CNPq/FAPEAM 573976/2008-2). MNL (2013/24252-9 received a post-doctoral scholarship from FAPESP. FAL (302776/2011-7) and JCM (300662/2009-2) received research scholarships from CNPq. We also thank Nilton Rosa Alves for technical assistance. This laboratory (FAL) is integrated with the Amazon Shrimp Network (Rede de Camarão da Amazônia) and with ADAPTA (Centro de Estudos de Adaptações da Biota Aquática da Amazônia). FAL is a Senior Professor at the Departamento de Química, FFCLRP/USP.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Francisco A. Leone.

Additional information

Guest editors: Adalberto L. Val, Gudrun De Boeck & Sidinei M. Thomaz / Adaptation of Aquatic Biota of the Amazon

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lucena, M.N., McNamara, J.C. & Leone, F.A. Gill (Na+, K+)-ATPase from the Amazon River shrimp, Macrobrachium amazonicum (Decapoda, Palaemonidae): effect of exogenous biogenic amines on enzyme activity in juveniles and adults. Hydrobiologia 789, 59–76 (2017). https://doi.org/10.1007/s10750-016-2753-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-016-2753-3

Keywords

Navigation