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Polyamines regulate phosphorylation–dephosphorylation kinetics in a crustacean gill (Na+, K+)-ATPase

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Abstract

Aiming to clarify the mechanism of inhibition of (Na+, K+)-ATPase activity by polyamines, we examined the effects of exogenous putrescine, spermidine, and spermine on the kinetic behavior of phosphoenzyme-linked partial reactions using a microsomal gill (Na+, K+)-ATPase from juvenile and adult M. amazonicum, a freshwater palaemonid shrimp. The time course of phosphointermediate formation is greater (0.089 ± 0.006 s−1) in adults than in juveniles (0.053 ± 0.003 s−1) for spermidine, but similar to juveniles (0.059 ± 0.004 s−1) for putrescine. Maximum phosphointermediate formation for the (Na+, K+)-ATPase from juveniles decreased by 46% and 32% with spermidine and putrescine, respectively. In adults, maximum phosphointermediate levels decreased by 50% and 8%, respectively. For both spermidine and putrescine, dephosphorylation rates were higher for adults than for juveniles, and were higher than in controls without polyamines. Spermine had a negligible effect (<10%) on phosphorylation/dephosphorylation rates of both juvenile and adult enzymes. This is the first report on the effects of polyamines on phosphoenzyme-linked partial reactions in juvenile and adult M. amazonicum gill (Na+, K+)-ATPases. Our findings suggest that the phosphorylation/dephosphorylation steps of this gill enzyme may be regulated by polyamines during ontogenetic development.

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References

  1. Albers RW (1967) Biochemical aspects of active transport. Annu Rev Biochem 6:727–756

    Article  Google Scholar 

  2. Post RL, Hegyvary C, Kume S (1972) Activation by adenosine triphosphate in the phosphorylation kinetics of sodium and potassium ion transport adenosine triphosphatase. J Biol Chem 247:6530–6540

    CAS  PubMed  Google Scholar 

  3. Lingrel LB, Williams MT, Vorhees CV, Moseley AE (2007) Na, K-ATPase and the role of α isoforms in behavior. J Bioenerg Biomembr 39:385–389

    Article  CAS  PubMed  Google Scholar 

  4. Morth JP, Pedersen BP, Toustrup-Jensen MS, Sorensen TLM, Petersen J, Eersen JP, Vilsen B, Nissen P (2007) Crystal structure of the sodium–potassium pump. Nature 450:1043–1050

    Article  CAS  PubMed  Google Scholar 

  5. Geering K (2008) Functional roles of Na, K-ATPase subunits. Curr Opinion Nephrol Hypert 17: 526–532

    Article  CAS  Google Scholar 

  6. Poulsen H, Khandelia H, Morth P, Bublitz M, Mouritsen OG, Egebjerg J, Nissen P (2010) Neurological disease mutations compromise a C-terminal ion pathway in the Na1/K1-ATPase. Nature 467:99–102

    Article  CAS  PubMed  Google Scholar 

  7. Kaplan JH (2002) Biochemistry of Na, K-ATPase. Annu Rev Biochem 71:511–535

    Article  CAS  PubMed  Google Scholar 

  8. McDonough AA, Geering K, Farley RA (1990) The sodium pump needs its beta subunit. FASEB J 4:1598–1605

    CAS  PubMed  Google Scholar 

  9. Geering K (2001) The functional role of beta subunits in oligomeric P-type ATPases. J Bioenerg Biomemb 33:425–438

    Article  CAS  Google Scholar 

  10. Therien AG, Blostein R (2000) Mechanisms of sodium pump regulation. Am J Physiol 279:C541–C566

    CAS  Google Scholar 

  11. Cortes VF, Veiga-Lopes FE, Barrabin H, Alves-Ferreira M, Fontes CFL (2006) The gamma subunit of Na+ ,K+-ATPase: role on ATPase activity and regulatory phosphorylation by PKA. Int J Biochem Cell Biol 38:1901–1913

    Article  CAS  PubMed  Google Scholar 

  12. Silva ECC, Masui DC, Furriel RP, McNamara JC, Barrabin H, Scofano HM, Perales J, Teixeira-Ferreira A, Leone FA, Fontes CFL (2012) Identification of a crab gill FXYD2 protein and regulation of crab microsomal Na, K-ATPase activity by mammalian FXYD2 peptide. Biochim Biophys Acta 1818:2588–2597

  13. Horisberger JD (2004) Recent insights into the structure e mechanism of the sodium pump. Physiology 19:377–388

    Article  CAS  PubMed  Google Scholar 

  14. Jorgensen PL, Nielsen JM, Rasmussen JH, Pedersen PA (1998) Structure-function relationships based on E1–E2 transitions and cation binding in NaK-pump protein. Biochim Biophys Acta 1365:65–70

    Article  CAS  PubMed  Google Scholar 

  15. Morth JP, Poulsen P, Toustrup-Jensen MS, Schack VR, Egebjerg J, Andersen JP, Vilsen B, Nissen P (2009) The structure of the Na+,K+-ATPase and mapping of isoform differences and disease-related mutations. Philos Trans R Soc Lond Biol Sci 364:217–227

    Article  CAS  Google Scholar 

  16. Glynn IM (1985) The (Na+K+)-transporting adenosine triphosphatase. In: Martonosi AN (ed) The enzymes of biological membranes, 3. Plenum Press, New York, pp 35–114

    Chapter  Google Scholar 

  17. Fedosova NU, Champeil P, Esmann M (2003) Rapid filtration analysis of nucleotide binding to Na, K-ATPase. BioChemistry 42:3536–3543

    Article  CAS  PubMed  Google Scholar 

  18. Petrushanko IY, Mitkevich VA, Anashkina AA, Klimanova EA, Dergousova EA, Lopina OD, Makarov AA (2014) Critical role of γ-phosphate in structural transition of Na, K-ATPase upon ATP binding. Sci Report 4:5165

    Article  CAS  Google Scholar 

  19. Stekhoven FMAHS, Swarts HGP, Depont JJHHM, Bonting SL (1981) Studies on (Na+,K+)-activated ATPase: mangnesium induces low-affinity non-phosphorylating nucleotide binding-sites per molecule. Biochim Biophys Acta 649:533–540

    Article  Google Scholar 

  20. Beaugé L (2001) Breakdown of Na+/K+-exchanging ATPase phosphoenzymes formed from ATP and from inorganic phosphate during Na+-ATPase activity. Eur J Biochem 268:5627–5632

    Article  PubMed  Google Scholar 

  21. Glynn IM, Karlish SJ (1975) The sodium pump. Annu Rev Physiol 37:13–55

    Article  CAS  PubMed  Google Scholar 

  22. Hobbs AS, Albers RW, Froehlich JP (1983) Effects of oligomycin on the partial reactions of the sodium plus potassium-stimulated adenosine-triphosphate. J Biol Chem 258:8163–8168

    CAS  PubMed  Google Scholar 

  23. Sen AK, Tobin T, Post RL (1969) A cycle for ouabain inhibition of sodium-dependent and potassium-dependent adenosine triphosphatase. J Biol Chem 244:6596–6604

    CAS  PubMed  Google Scholar 

  24. Yoda Y, Yoda S (1983) Characteristics of the electric-eel Na, K-ATPase phosphoprotein. Curr Top Membr Transp 19:343–347

    Article  CAS  Google Scholar 

  25. Yoda S, Yoda A (1986) ADP- and K+-sensitive phosphorylated intermediate of Na, K-ATPase. J Biol Chem 261:1147–1152

    CAS  PubMed  Google Scholar 

  26. Yoda S, Yoda A (1987) Two different phosphorylation-dephosphorylation cycles of Na, K-ATPase proteoliposomes accompanying Na+ transport in the absence of K+. J Biol Chem 262:110–115

    CAS  PubMed  Google Scholar 

  27. Klodos I, Nørby JG (1986) (Na++ K+)-ATPase: confirmation of the three-pool model for the phosphointermediates of Na+-ATPase activity. Estimation of the enzyme-ATP dissociation rate constant. Biochim Biophys Acta 897:302–314

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  29. Péqueux A (1995) Osmotic regulation in crustaceans. J Crust Biol 15:1–60

    Article  Google Scholar 

  30. Freire CA, Onken H, McNamara JC (2008) A structure–function analysis of ion transport in crustacean gills and excretory organs. Comp Biochem Physiol 151A:272–304

    Article  CAS  Google Scholar 

  31. Henry RP, Lucu C, Onken H, Weihrauch D (2012) Multiple functions of the crustacean gill: osmotic/ionic regulation, acid-base balance, ammonia excretion, and bioaccumulation of toxic metals. Front Physiol 3:431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 85:97–177

    Article  CAS  PubMed  Google Scholar 

  33. McNamara JC, Faria SC (2012) Evolution of osmoregulatory patterns and gill ion transport mechanisms in the decapod Crustacea: a review. J Comp Physiol 182B:997–1014

    Article  Google Scholar 

  34. Sáez AG, Lozano E, Zaldívar-Riverón A (2009) Evolutionary history of Na, K-ATPases and their osmoregulatory role. Genetica 136:479–490

    Article  PubMed  Google Scholar 

  35. Lee CE, Kiergaard M, Gelembiuk GW, Eads BD, Posavi M (2011) Pumping ions: rapid parallel evolution of ionic regulation following habitat invasions. Evol Int J Org Evol 65:2229–2244

    Article  CAS  Google Scholar 

  36. Towle DW, Kays WT (1986) Basolateral localization of Na+ ,K+-ATPase in gill epithelium of two osmoregulating crabs, Callinectes sapidus and Carcinus maenas. J Exp Zool 239:311–318

    Article  CAS  Google Scholar 

  37. Taylor HH, Taylor EW (1992) Microscopic anatomy of invertebrates. In: Harrison FW, Humas AG (eds) Decapod crustacea, vol 10. Wiley-Liss, New York, pp 203–293

    Google Scholar 

  38. McNamara JC, Torres AH (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). J Exp Biol 284:617–628

    CAS  Google Scholar 

  39. Holthuis LB (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

  40. Odinetz-Collart O, Rabelo H (1996) Variation in egg size of the fresh-water prawn Macrobrachium amazonicum (Decapoda: Palaemonidae). J Crustacean Biol 16:684–688

    Article  Google Scholar 

  41. Magalhães C, Bueno SLS, Bond-Buckup G, Valenti WC, Silva HLM., Kiyohara F, Mossolin EC, Rocha SS (2005) Exotic species of freshwater decapod crustaceans in the state of São Paulo, Brazil: records and possible causes of their introduction. Biodivers Conserv 14:1929–1945

    Article  Google Scholar 

  42. Charmantier G, Anger K (2001) 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. J Exp Mar Biol Ecol 396:89–98

    Article  Google Scholar 

  43. Anger K (2013) Neotropical Macrobrachium (Caridea: Palaemonidae): on the biology, origin, and radiation of freshwater-invading shrimp. J Crust Biol 33:151–183

    Article  Google Scholar 

  44. Santos A, Hayd L, Anger K (2013) A new species of Macrobrachium Spence Bate, 1868 (Decapoda, Palaemonidae), M. pantanalense, from the Pantanal, Brazil. Zootaxa 3700:534–546

    Article  PubMed  Google Scholar 

  45. Pileggi LA, Mantelatto FL (2012) Taxonomic revision of doubtful Brazilian freshwater shrimp species of the genus Macrobrachium (Decapoda, Palaemonidae). Iheringia, Série Zoologia 102:426–437

    Article  Google Scholar 

  46. Pantaleão JAF, Hirose GL, Costa RC (2014) Occurrence of male morphotypes of Macrobrachium amazonicum (Caridea, Palaemonidea) in a population with an entirely freshwater life cycle. Braz J Biol 74:S223–S232

    Article  PubMed  Google Scholar 

  47. Moreira GS, McNamara JC, Moreira PS (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 

  48. Augusto A, Greene LJ, Laure HJ, McNamara JC (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

    Article  Google Scholar 

  49. Santos LCF, Belli NM, Augusto A, Masui DC, Leone FA, McNamara JC, Furriel RPM (2007) Gill (Na+, K+)-ATPase in diadromous, freshwater palaemonid shrimps: species-specific kinetic characteristics and α-subunit expression. Comp Biochem Physiol 148A:178–188

    Article  CAS  Google Scholar 

  50. Belli NM, Faleiros RO, Firmino KCS, Masui DC, Leone FA, McNamara JC, Furriel RPM (2009) Na, K-ATPase activity and epithelial interfaces in gills of the freshwater shrimp Macrobrachium amazonicum (Decapoda, Palaemonidae). Comp Biochem Physiol 152A:431–439

    Article  CAS  Google Scholar 

  51. Leone FA, Masui DC, Bezerra TMS, Garçon DP, Valenti WC, Augusto AS, McNamara JC (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. J Memb Biol 245:201–215

    Article  CAS  Google Scholar 

  52. Kalac P (2009) Recent advances in the research on biological roles of dietary polyamines in man. J Appl Biomed 7:65–74

    CAS  Google Scholar 

  53. Igarashi K, Kashiwagi K: Modulation of cellular function by polyamines. Int J Biochem Cell Biol 42: 39–51

  54. Pegg AE (2009) Mammalian polyamine metabolism e function. IUBMB Life 61:880–894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Tabor CW, Tabor H (1984) Polyamines. Ann Rev Biochem 53:749–790

    Article  CAS  PubMed  Google Scholar 

  56. Pottosin I, Velarde-Buendia AM, Bose J, Fugisang AT, Shabala S (2014) Polyamines cause plasma membrane depolarization, activate Ca 2+-, and modulate H+-ATPase pump activity in roots. J Exp Botany 65:2463–2472

    Article  CAS  Google Scholar 

  57. Koenig H, Goldstone A, Lu CY (1983) Polyamines regulate calcium fluxes in a rapid plasma membrane response. Nature 305:530–534

  58. Seiler N, Dezeure F (1990) Polyamine transport in mammalian cells. Int J Biochem 22:211–218

  59. Aziz SM, Olson JW, Gillespie MN (1994) Multiple polyamine transport pathways in cultured pulmonary artery smooth muscle cells: regulation by hypoxia. Am J Resp Cell Mol Biol 10:160–166

    Article  CAS  Google Scholar 

  60. Kobayashi M, Fujisaki H, Sugawara M, Iseki K, Miyazaki K (1999) The presence of an Na+/spermine antiporter in the rat renal brush-border membrane. J Pharm Pharmacol 51:279–284

    Article  Google Scholar 

  61. Lin X, Fenn E, Veenstra RD (2006) An amino-terminal lysine residue of rat connexin 40 that is required for spermine block. J Physiol 570:251–269

    Article  CAS  PubMed  Google Scholar 

  62. Tassoni A, Antognoni F, Bagni N (1996) Polyamines binding to plasma membrane vesicles isolated from zucchini hypocotyls. Plant Physiol 110:817–824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Fukushima Y (1990) Membrane destruction by polyamines. Biomed Res 11:345–352

    Article  Google Scholar 

  64. Meksuriyen D, Fukuchi-Shigimori T, Kashiwagi K, Toida T, Imanari T, Kawai G, Igarashi K (1998) Complex formation of ATP, Mg 2+, and spermine: structural evidence and biological significance. J Biol Chem 273:30939–30944

    Article  CAS  PubMed  Google Scholar 

  65. Ha HC, Sirisoma NS, Kuppusamy P, Zweier JL, Woster Pm, Casero RA Jr (1998) The natural spermine functions directly as a free radical scavenger. Proc Natl Acad Sci USA 95:11140–11145.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Toner M, Vaio G, McLaughlin A, McLaughlin S (1988) Adsorption of cations to phosphatidylinositol 4,5-bisphosphate. BioChemistry 27:7435–7443

    Article  CAS  PubMed  Google Scholar 

  67. Heinrich-Hirsch B, Ahlers J, Peter HW (1977) Inhibition of Na+ ,K+-ATPase from chick brain by polyamines. Enzyme 22:235–241

    CAS  PubMed  Google Scholar 

  68. Robinson JD, Leach CA, Robinson LJ (1986) Cation sites, spermine, and the reaction sequence of the (Na+K+)-dependent ATPase. Biochim Biophys Acta 856:536–544

    Article  CAS  PubMed  Google Scholar 

  69. Kuntzweiler TA, Wallick ET, Johnson CL, Lingrel JB (1995) Glutamic-acid-327 in the sheep alpha-1 isoform of Na+ ,K+-ATPase stabilizes a K+-induced conformational change. J Biol Chem 270:2993–3000

    Article  CAS  PubMed  Google Scholar 

  70. Quarfoth G, Ahmed K, Foster D (1978) Effects of polyamines on partial reactions of membrane (Na+K+)-ATPase. Biochim Biophys Acta 526:580–590

    Article  CAS  PubMed  Google Scholar 

  71. Tashima Y, Hasegawa M, Mizunuma H (1978) Activation of (Na+K+)-adenosine triphosphatase by spermine. Biochem Biophys Res Comm 82:13–18

    Article  CAS  PubMed  Google Scholar 

  72. Lovett DL, Watts SA (1995) Changes in polyamine levels in response to acclimation salinity in gills of the blue-crab Callinectes-sapidus rathbun. Comp Biochem Physiol 110B:115–119

    Article  CAS  Google Scholar 

  73. Péqueux A, Labras P, Cann-Moisan C, Coroff J, Sebert P (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 

  74. Silva ECC, Masui DC, Furriel RPM, Mantelatto FLM, McNamara JC, Barrabin H, Leone FA, Scofano HM, Fontes CFL (2008) Regulation by the exogenous polyamine spermidine of Na, K-ATPase activity from the gills of the euryhaline swimming crab Callinectes danae (Brachyura, Portunidae). Comp Biochem Physiol 149B:622–629

    Article  CAS  Google Scholar 

  75. Garçon DP, Lucena MN, França JL, McNamara JC, Fontes CFL, Leone FA (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. J Memb Biol 244:9–20

    Article  Google Scholar 

  76. Lucena MN, McNamara JC, Leone FA (2016) 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. doi:10.1007/s10750-016-2753-3

    Google Scholar 

  77. Jantaro S, Maenpaa P, Mulo P, Incharoensakdi A (2003) Content and biosynthesis of polyamines in salt and osmotically stressed cells of Synechocystis sp PCC 6803. FEMS Microbiol Lett 228:129–135

    Article  CAS  PubMed  Google Scholar 

  78. Araujo MC, Valenti WC (2007) Feeding habit of the Amazon River prawn Macrobrachium amazonicum larvae. Aquaculture 265:187–193

    Article  Google Scholar 

  79. Hayd LA, Anger K, Valenti WC (2008) The moulting cycle of larval amazon river prawn Macrobrachium amazonicum reared in the laboratory. Nauplius 16:55–63

    Google Scholar 

  80. Leone FA, Bezerra TMS, Garçon DP, Lucena MN, Pinto MR, Fontes CFL, McNamara JC (2014) Modulation by K+ and NH4 + of microsomal (Na+, K+)-ATPase activity in selected ontogenetic stages of the diadromous river shrimp Macrobrachium amazonicum (Decapoda, Palaemonidae). PLOS ONE 9(2):e8925. doi:10.1371/journalpone008925

    Article  Google Scholar 

  81. Leone FA, Baranauskas JA, Furriel RPM, Borin IA: SigrafW (2005) An easy-to-use program for fitting enzyme kinetic data. Biochem Mol Biol Ed 33:399–403

    Article  CAS  Google Scholar 

  82. Walseth TF, Johnson RA (1979) The enzymatic preparation of alpha-32P.ATP, alpha-32P.GTP, 32P.cAMP, and 32P.cGMP, and their use in the assay of adenylate and guanylate cyclases and cyclic nucleotide phosphodiesterases. Adv Cyclic Nucleotide Res 10:135–167

    PubMed  Google Scholar 

  83. Maia JCC, Gomes SL, Juliani MA (1983) A laboratory manual proceedings. In: CM Morel (ed) Genes and antigens of parasites-FIOCRUZ, Brasil, RJ, pp 144–157

  84. Barrabin H, Fontes CFL, Scofano HM, Nørby JG (1990) Phosphorylation of (Na+, K+)-ATPase by ATP in the presence of K+ and dimethyl sulfoxide but in the absence of Na+. Biochim Biophys Acta 1023:266–273

    Article  CAS  PubMed  Google Scholar 

  85. Fontes CFL, Barrabin H, Scofano HM, Nørby JG (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+. Biochim Biophys Acta 1104:215–225

    Article  CAS  PubMed  Google Scholar 

  86. Fontes CFL, Scofano HM, Barrabin H, Nørby JG (1995) The effect of dimethyl sulfoxide on the substrate site of Na+/K(+)-ATPase studied through phosphorylation by inorganic phosphate and ouabain binding. Biochim Biophys Acta 1235:43–51

    Article  PubMed  Google Scholar 

  87. Read SM, Northcote DH (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

    Article  CAS  PubMed  Google Scholar 

  88. Cornelius F, Fedosova NU, Klodos I (1991) Interaction between substrate site and cation binding sites in Pi phosphorylation of Na, K-ATPase. Ann NY Acad Sci 834:390–393, 1997

  89. Janne J, Alhone L, Leinonen P (1991) Polyamines: from molecular biology to clinical application. Ann Med 23:241–259

    Article  CAS  PubMed  Google Scholar 

  90. Watts SA, Lee KJ, Cline GB (1994) Elevated ornithine decarboxylase activity e polyamine levels during early development in the brine shrimp Artemia franciscana. J Exp Zool 270:426–431

    Article  CAS  Google Scholar 

  91. Nielsen JM, Pedersen PA, Karlish SJD, Jorgensen PL (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 

  92. Mandal AK, Mikhailova L, Arguelo JM (2003) The Na, K-ATPase S5-H5 helix. Structural link between phosphorylation and cation-binding sites. Ann NY Acad Sci 986:224–225

    Article  CAS  PubMed  Google Scholar 

  93. Féraille E, Carranza ML, Gonin S, Béguin P, Pedemonte C, Rousselot M, Caverzasio J, Geering K, Martin PY, Favre H (1999) Insulin-induced stimulation of Na1,K1-ATPase activity in kidney proximal tubule cells depends on phosphorylation of the a-subunit at Tyr-10. Mol Biol Cell 10:2847–2859

    Article  PubMed  PubMed Central  Google Scholar 

  94. Féraille E, Doucet A (2001) Sodium-potassium-adenosinetriphosphatase-dependent sodium transport in the kidney: hormonal control. Physiol Rev 81:345–418

    PubMed  Google Scholar 

  95. Bibert S, Roy S, Schaer D, Horisberger JD, Geering K (2008) Phosphorylation of phospholemman (FXYD1) by protein kinases A and C modulates distinct Na, K-ATPase isozymes. J Biol Chem 283:476–486

    Article  CAS  PubMed  Google Scholar 

  96. Teriete P, Thai K, Choi J, Marassi FM (2009) Effects of PKA phosphorylation on the conformation of the Na, K-ATPase regulatory protein FXYD1. Biochim Biophys Acta 1788:2462–2470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Arystarkhova E, Wetzel RK, Asinovski NK, Sweadner K (1999) The gamma subunit modulates Na+ and K+ affinity of the renal Na, K-ATPase. J Biol Chem 247:33183–33185

    Article  Google Scholar 

  98. Cortes VF, Ribeiro IM, Barrabin H, Alves-Ferreira M, Fontes CFL (2011) Regulatory phosphorylation of FXYD2 by PKC and cross interactions between FXYD2, plasmalemmal Ca-ATPase and Na, K-ATPase. Arch Biochem Biophys 505:75–82

    Article  CAS  PubMed  Google Scholar 

  99. Elgavish A, Wallace RW, Pillion DJ, Meezan E (1984) Polyamines stimulate D-glucose transport in isolated renal brush-border membrane vesicles. Biochim Biophys Acta 777:1–8

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This investigation was supported by research grants from the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP 2010/17534-0 and 2013/22625-1), Conselho de Desenvolvimento Científico e Tecnológico (CNPq 470177/2008-0), and Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM 573976/2008-2). DPG (2010/06395-9) and MNL (2013/24252-9) received post-doctoral scholarships from FAPESP. FAL (302776/2011-7), JCM (300662/2009-2), and CFLF (308847/2014-8) received research scholarships from CNPq. This laboratory (FAL) is integrated with the Amazon Shrimp Network (Rede de Camarão da Amazônia) and with INCT-ADAPTA (Centro de Estudos de Adaptações da Biota Aquática da Amazônia). FAL is a Senior Professor at the Departamento de Química, FFCLRP/USP.

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  1. Departamento de Química, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Avenida Bandeirantes 3900, Ribeirão Preto, SP, 14040-901, Brazil

    Malson Neilson Lucena, Daniela Pereira Garçon & Francisco Assis Leone

  2. Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, São Paulo, SP, Brazil

    John Campbell McNamara

  3. Instituto de Bioquímica Médica, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

    Carlos Frederico Leite Fontes

  4. Centro de Biologia Marinha, Universidade de São Paulo, São Sebastião, SP, Brazil

    John Campbell McNamara

  5. Universidade Federal do Triângulo Mineiro, Campus Universitário de Iturama, Iturama, Minas Gerais, 38280-000, Brazil

    Daniela Pereira Garçon

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  1. Malson Neilson Lucena
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  2. Daniela Pereira Garçon
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  3. Carlos Frederico Leite Fontes
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  5. Francisco Assis Leone
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Correspondence to Francisco Assis Leone.

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Lucena, M.N., Garçon, D.P., Fontes, C.F.L. et al. Polyamines regulate phosphorylation–dephosphorylation kinetics in a crustacean gill (Na+, K+)-ATPase. Mol Cell Biochem 429, 187–198 (2017). https://doi.org/10.1007/s11010-017-2946-8

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  • DOI: https://doi.org/10.1007/s11010-017-2946-8

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