Protein phosphatase 2a interacts with the na +,k +-atpase and modulates its trafficking by inhibition of its association with arrestin

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Kimura, Toru ^a,b   Han, WonSun ^b   Pagel, Philipp ^b   Nairn, Angus C ^b   Caplan, Michael J ^b  

^a KYORIN UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); G PROTEIN COUPLED RECEPTOR KINASE; PHOSPHOPROTEIN PHOSPHATASE 2A; PHOSPHOPROTEIN PHOSPHATASE 2A A SUBUNIT; PHOSPHOPROTEIN PHOSPHATASE 2A C SUBUNIT; RETINA S ANTIGEN; UNCLASSIFIED DRUG; PHOSPHOPROTEIN PHOSPHATASE 2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING COMPETITION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; IMMUNOPRECIPITATION; INTRACELLULAR TRANSPORT; KIDNEY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; ANIMAL; CELL STRAIN COS1; CERCOPITHECUS; CHEMISTRY; ENZYMOLOGY; GENE DELETION; HUMAN; METABOLISM; MOUSE; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; PROTEIN SUBUNIT; PROTEIN SYNTHESIS; PROTEIN TRANSPORT;

RATTUS;

ANIMALS; ARRESTIN; BINDING, COMPETITIVE; CERCOPITHECUS AETHIOPS; COS CELLS; G-PROTEIN-COUPLED RECEPTOR KINASES; GENE DELETION; HUMANS; IMMUNOPRECIPITATION; KIDNEY; MICE; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN PHOSPHATASE 2; PROTEIN STRUCTURE, SECONDARY; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RATS; SODIUM-POTASSIUM-EXCHANGING ATPASE;

EID: 84855271009     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029269     Document Type: Article

References (69)

1. Maeda M, Hamano K, Hirano Y, Suzuki M, Takahashi E, et al. (1998) Structures of P-type transporting ATPases and chromosomal locations of their genes. Cell Structure & Function 23: 315-323.
2. Scarborough GA, (2002) Molecular mechanism of the P-type ATPases. Journal of Bioenergetics & Biomembranes 34: 235-250.
3. Skou JC, Esmann M, (1992) The Na,K-ATPase. Journal of Bioenergetics & Biomembranes 24: 249-261.
4. Morth JP, Pedersen BP, Toustrup-Jensen MS, Sorensen TL, Petersen J, et al. (2007) Crystal structure of the sodium-potassium pump. Nature 450: 1043-1049.
5. Shinoda T, Ogawa H, Cornelius F, Toyoshima C, (2009) Crystal structure of the sodium-potassium pump at 2.4 A resolution. Nature 459: 446-450.
6. Therien AG, Blostein R, (2000) Mechanisms of sodium pump regulation. Am J Physiol Cell Physiol 279: C541-566.
7. Scheiner-Bobis G, Farley RA, (1994) Subunit requirements for expression of functional sodium pumps in yeast cells. Biochimica et Biophysica Acta 1193: 226-234.
8. Blostein R, Pu HX, Scanzano R, Zouzoulas A, (2003) Structure/function studies of the gamma subunit of the Na,K-ATPase. Ann N Y Acad Sci 986: 420-427.
9. Therien AG, Pu HX, Karlish SJ, Blostein R, (2001) Molecular and functional studies of the gamma subunit of the sodium pump. J Bioenerg Biomembr 33: 407-414.
10. Zouzoulas A, Therien AG, Scanzano R, Deber CM, Blostein R, (2003) Modulation of Na,K-ATPase by the gamma subunit: studies with transfected cells and transmembrane mimetic peptides. J Biol Chem 278: 40437-40441.
11. Sweadner KJ, Arystarkhova E, Donnet C, Wetzel RK, (2003) FXYD proteins as regulators of the Na,K-ATPase in the kidney. Ann N Y Acad Sci 986: 382-387.
12. Crambert G, Geering K, (2003) FXYD proteins: new tissue-specific regulators of the ubiquitous Na,K-ATPase. Sci STKE 2003: RE1.
13. Geering K, Beguin P, Garty H, Karlish S, Fuzesi M, et al. (2003) FXYD proteins: new tissue- and isoform-specific regulators of Na,K-ATPase. Ann N Y Acad Sci 986: 388-394.
14. Arystarkhova E, Wetzel RK, Asinovski NK, Sweadner KJ, (1999) The gamma subunit modulates Na(+) and K(+) affinity of the renal Na,K-ATPase. J Biol Chem 274: 33183-33185.
15. Beguin P, Wang X, Firsov D, Puoti A, Claeys D, et al. (1997) The gamma subunit is a specific component of the Na,K-ATPase and modulates its transport function. EMBO Journal 16: 4250-4260.
16. Ohtsubo M, Noguchi S, Takeda K, Morohashi M, Kawamura M, (1990) Site-directed mutagenesis of Asp-376, the catalytic phosphorylation site, and Lys-507, the putative ATP-binding site, of the alpha-subunit of Torpedo californica Na+/K(+)-ATPase. Biochimica et Biophysica Acta 1021: 157-160.
17. Pagel P, Zatti A, Kimura T, Duffield A, Chauvet V, et al. (2003) Ion pump-interacting proteins: promising new partners. Annals of the New York Academy of Sciences 986: 360-368.
18. Lecuona E, Dada LA, Sun H, Butti ML, Zhou G, et al. (2006) Na,K-ATPase alpha1-subunit dephosphorylation by protein phosphatase 2A is necessary for its recruitment to the plasma membrane. Faseb J 20: 2618-2620.
19. Turowski P, Favre B, Campbell KS, Lamb NJ, Hemmings BA, (1997) Modulation of the enzymatic properties of protein phosphatase 2A catalytic subunit by the recombinant 65-kDa regulatory subunit PR65alpha. European Journal of Biochemistry 248: 200-208.
20. Sontag E, (2001) Protein phosphatase 2A: the Trojan Horse of cellular signaling. Cellular Signalling 13: 7-16.
21. Kremmer E, Ohst K, Kiefer J, Brewis N, Walter G, (1997) Separation of PP2A core enzyme and holoenzyme with monoclonal antibodies against the regulatory A subunit: abundant expression of both forms in cells. Molecular & Cellular Biology 17: 1692-1701.
22. Shenoy SK, Lefkowitz RJ, (2003) Multifaceted roles of beta-arrestins in the regulation of seven-membrane-spanning receptor trafficking and signalling. Biochem J 375: 503-515.
23. Tan CM, Brady AE, Nickols HH, Wang Q, Limbird LE, (2004) Membrane trafficking of G protein-coupled receptors. Annu Rev Pharmacol Toxicol 44: 559-609.
24. Wang Q, Limbird LE, (2002) Regulated interactions of the alpha 2A adrenergic receptor with spinophilin, 14-3-3zeta, and arrestin 3. J Biol Chem 277: 50589-50596.
25. Wang Q, Zhao J, Brady AE, Feng J, Allen PB, et al. (2004) Spinophilin blocks arrestin actions in vitro and in vivo at G protein-coupled receptors. Science 304: 1940-1944.
26. Smith FD, Oxford GS, Milgram SL, (1999) Association of the D2 dopamine receptor third cytoplasmic loop with spinophilin, a protein phosphatase-1-interacting protein. J Biol Chem 274: 19894-19900.
27. Brady AE, Wang Q, Colbran RJ, Allen PB, Greengard P, et al. (2003) Spinophilin stabilizes cell surface expression of alpha 2B-adrenergic receptors. J Biol Chem 278: 32405-32412.
28. Kimura T, Allen PB, Nairn AC, Caplan MJ, (2007) Arrestins and spinophilin competitively regulate Na+,K+-ATPase trafficking through association with a large cytoplasmic loop of the Na+,K+-ATPase. Mol Biol Cell 18: 4508-4518.
29. Bertorello AM, Aperia A, Walaas SI, Nairn AC, Greengard P, (1991) Phosphorylation of the catalytic subunit of Na+,K(+)-ATPase inhibits the activity of the enzyme. Proc Natl Acad Sci U S A 88: 11359-11362.
30. Feraille E, Doucet A, (2001) Sodium-potassium-adenosinetriphosphatase-dependent sodium transport in the kidney: hormonal control. Physiol Rev 81: 345-418.
31. Pedemont CH, Bertorello AM, (2001) Short-term regulation of the proximal tubule Na+,K+-ATPase: increased/decreased Na+,K+-ATPase activity mediated by protein kinase C isoforms. J Bioenerg Biomembr 33: 439-447.
32. Nestor NB, Lane LK, Blostein R, (1997) Effects of protein kinase modulators on the sodium pump activities of HeLa cells transfected with distinct alpha isoforms of Na,K-ATPase. Ann N Y Acad Sci 834: 579-581.
33. Meister B, Aperia A, (1993) Molecular mechanisms involved in catecholamine regulation of sodium transport. Semin Nephrol 13: 41-49.
34. Bertorello A, Aperia A, (1990) Short-term regulation of Na+,K(+)-ATPase activity by dopamine. Am J Hypertens 3: 51S-54S.
35. Soares-da-Silva P, Vieira-Coelho MA, Pinto-do OP, Pestana M, Bertorello AM, (1995) Studies on the nature of the antagonistic actions of dopamine and 5-hydroxytryptamine in renal tissues. Hypertens Res 18 (Suppl 1): S47-51.
36. Baskin DG, Stahl WL, (1982) Immunocytochemical localization of Na+, K+-ATPase in the rat kidney. Histochemistry 73: 535-548.
37. Takada T, Yamamoto A, Omori K, Tashiro Y, (1992) Quantitative immunogold localization of Na, K-ATPase along rat nephron. Histochemistry 98: 183-197.
38. Dunbar LA, Aronson P, Caplan MJ, (2000) A transmembrane segment determines the steady-state localization of an ion-transporting adenosine triphosphatase. Journal of Cell Biology 148: 769-778.
39. Yang CS, Vitto MJ, Busby SA, Garcia BA, Kesler CT, et al. (2005) Simian virus 40 small t antigen mediates conformation-dependent transfer of protein phosphatase 2A onto the androgen receptor. Mol Cell Biol 25: 1298-1308.
40. Goodarzi AA, Jonnalagadda JC, Douglas P, Young D, Ye R, et al. (2004) Autophosphorylation of ataxia-telangiectasia mutated is regulated by protein phosphatase 2A. Embo J 23: 4451-4461.
41. Lubert EJ, Sarge KD, (2003) Interaction between protein phosphatase 2A and members of the importin beta superfamily. Biochem Biophys Res Commun 303: 908-913.
42. Toyoshima C, Mizutani T, (2004) Crystal structure of the calcium pump with a bound ATP analogue. Nature 430: 529-535.
43. Marks AR, Marx SO, Reiken S, (2002) Regulation of ryanodine receptors via macromolecular complexes: a novel role for leucine/isoleucine zippers. Trends Cardiovasc Med 12: 166-170.
44. Marx SO, Reiken S, Hisamatsu Y, Gaburjakova M, Gaburjakova J, et al. (2001) Phosphorylation-dependent regulation of ryanodine receptors: a novel role for leucine/isoleucine zippers. J Cell Biol 153: 699-708.
45. Yokoyama N, Reich NC, Miller WT, (2003) Determinants for the interaction between Janus kinase 2 and protein phosphatase 2A. Archives of Biochemistry & Biophysics 417: 87-95.
46. Fisone G, Cheng SX, Nairn AC, Czernik AJ, Hemmings HC Jr, et al. (1994) Identification of the phosphorylation site for cAMP-dependent protein kinase on Na+,K(+)-ATPase and effects of site-directed mutagenesis. Journal of Biological Chemistry 269: 9368-9373.
47. Beguin P, Beggah AT, Chibalin AV, Burgener-Kairuz P, Jaisser F, et al. (1994) Phosphorylation of the Na,K-ATPase alpha-subunit by protein kinase A and C in vitro and in intact cells. Identification of a novel motif for PKC-mediated phosphorylation. Journal of Biological Chemistry 269: 24437-24445.
48. Feschenko MS, Stevenson E, Sweadner KJ, (2000) Interaction of protein kinase C and cAMP-dependent pathways in the phosphorylation of the Na,K-ATPase. J Biol Chem 275: 34693-34700.
49. Fisone G, Snyder GL, Fryckstedt J, Caplan MJ, Aperia A, et al. (1995) Na+,K(+)-ATPase in the choroid plexus. Regulation by serotonin/protein kinase C pathway. J Biol Chem 270: 2427-2430.
50. Feschenko MS, Sweadner KJ, (1995) Structural basis for species-specific differences in the phosphorylation of Na,K-ATPase by protein kinase C. J Biol Chem 270: 14072-14077.
51. Davare MA, Horne MC, Hell JW, (2000) Protein phosphatase 2A is associated with class C L-type calcium channels (Cav1.2) and antagonizes channel phosphorylation by cAMP-dependent protein kinase. Journal of Biological Chemistry 275: 39710-39717.
52. Bauman AL, Apparsundaram S, Ramamoorthy S, Wadzinski BE, Vaughan RA, et al. (2000) Cocaine and antidepressant-sensitive biogenic amine transporters exist in regulated complexes with protein phosphatase 2A. J Neurosci 20: 7571-7578.
53. Bean BP, Nowycky MC, Tsien RW, (1984) Beta-adrenergic modulation of calcium channels in frog ventricular heart cells. Nature 307: 371-375.
54. Sculptoreanu A, Scheuer T, Catterall WA, (1993) Voltage-dependent potentiation of L-type Ca2+ channels due to phosphorylation by cAMP-dependent protein kinase. Nature 364: 240-243.
55. Cheng XJ, Fisone G, Aizman O, Aizman R, Levenson R, et al. (1997) PKA-mediated phosphorylation and inhibition of Na(+)-K(+)-ATPase in response to beta-adrenergic hormone. Am J Physiol 273: C893-901.
56. Lecuona E, Garcia A, Sznajder JI, (2000) A novel role for protein phosphatase 2A in the dopaminergic regulation of Na,K-ATPase. FEBS Letters 481: 217-220.
57. Horiuchi A, Takeyasu K, Mouradian MM, Jose PA, Felder RA, (1993) D1A dopamine receptor stimulation inhibits Na+/K(+)-ATPase activity through protein kinase A. Mol Pharmacol 43: 281-285.
58. Coutry N, Farman N, Bonvalet JP, Blot-Chabaud M, (1995) Synergistic action of vasopressin and aldosterone on basolateral Na(+)-K(+)-ATPase in the cortical collecting duct. J Membr Biol 145: 99-106.
59. Benovic JL, Strasser RH, Caron MG, Lefkowitz RJ, (1986) Beta-adrenergic receptor kinase: identification of a novel protein kinase that phosphorylates the agonist-occupied form of the receptor. Proc Natl Acad Sci U S A 83: 2797-2801.
60. Benovic JL, DeBlasi A, Stone WC, Caron MG, Lefkowitz RJ, (1989) Beta-adrenergic receptor kinase: primary structure delineates a multigene family. Science 246: 235-240.
61. Blakely RD, Berson HE, Fremeau RT Jr, Caron MG, Peek MM, et al. (1991) Cloning and expression of a functional serotonin transporter from rat brain. Nature 354: 66-70.
62. Dinudom A, Fotia AB, Lefkowitz RJ, Young JA, Kumar S, et al. (2004) The kinase Grk2 regulates Nedd4/Nedd4-2-dependent control of epithelial Na+ channels. Proc Natl Acad Sci U S A 101: 11886-11890.
63. Garty H, Palmer LG, (1997) Epithelial sodium channels: function, structure, and regulation. Physiol Rev 77: 359-396.
64. Ferguson SS, (2001) Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharmacol Rev 53: 1-24.
65. Lefkowitz RJ, Whalen EJ, (2004) beta-arrestins: traffic cops of cell signaling. Curr Opin Cell Biol 16: 162-168.
66. Szabo EZ, Numata M, Lukashova V, Iannuzzi P, Orlowski J, (2005) beta-Arrestins bind and decrease cell-surface abundance of the Na+/H+ exchanger NHE5 isoform. Proc Natl Acad Sci U S A 102: 2790-2795.
67. Pietrini G, Matteoli M, Banker G, Caplan MJ, (1992) Isoforms of the Na,K-ATPase are present in both axons and dendrites of hippocampal neurons in culture. Proc Natl Acad Sci U S A 89: 8414-8418.
68. Gottardi CJ, Caplan MJ, (1993) Molecular requirements for the cell-surface expression of multisubunit ion-transporting ATPases. Identification of protein domains that participate in Na,K-ATPase and H,K-ATPase subunit assembly. J Biol Chem 268: 14342-14347.
69. Biemesderfer D, Dekan G, Aronson PS, Farquhar MG, (1992) Assembly of distinctive coated pit and microvillar microdomains in the renal brush border. Am J Physiol 262: F55-67.