Protein kinase A (PKA) phosphorylation of Na+/K +-ATPase opens intracellular C-terminal water pathway leading to third Na+-binding site in molecular dynamics simulations

Journal of Biological Chemistry

Volumn 287, Issue 19, 2012, Pages 15959-15965

  Poulsen, Hanne ^a   Nissen, Poul ^a   Mouritsen, Ole G ^b   Khandelia, Himanshu ^b  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

C TERMINUS; CHARGED MOIETIES; IN-VIVO; INTERACTION NETWORKS; ION-BINDING; MOLECULAR DYNAMICS SIMULATIONS; PHOSPHORYLATION SITES; POST-TRANSCRIPTIONAL MODIFICATION; PROTEIN KINASE A; TRANSMEMBRANES; WATER-PATHWAY; XENOPUS OOCYTE;

ELECTROPHYSIOLOGY; ENZYMES; METAL IONS; MOLECULAR DYNAMICS; PROTEINS;

PHOSPHORYLATION;

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ASPARTIC ACID; CARBOXY TERMINAL TELOPEPTIDE; CYCLIC AMP DEPENDENT PROTEIN KINASE; SERINE; SODIUM ION;

ANIMAL CELL; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ENZYME ACTIVITY; IN VIVO STUDY; MOLECULAR DYNAMICS; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; SIMULATION; XENOPUS;

ANIMALS; BINDING SITES; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FEMALE; HUMANS; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MUTATION; PHOSPHORYLATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; SODIUM; SODIUM-POTASSIUM-EXCHANGING ATPASE; SWINE; WATER; XENOPUS LAEVIS;

EID: 84860850396     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.340406     Document Type: Article

References (51)

1. Therien, A. G., and Blostein, R. (2000) Mechanisms of sodium pump regulation. Am. J. Physiol. Cell Physiol. 279, C541-566
2. +-ATPase inhibits the activity of the enzyme. Proc. Natl. Acad. Sci. U.S.A. 88, 11359-11362
3. +-ATPase in response to β-adrenergic hormone. Am. J. Physiol. Cell Physiol. 273, C893-901
4. +-ATPase. Nature 467, 99-102
5. Morth, J. P., Pedersen, B. P., Toustrup-Jensen, M. S., Sørensen, T. L., Petersen, J., Andersen, J. P., Vilsen, B., and Nissen, P. (2007) Crystal structure of the sodium-potassium pump. Nature 450, 1043-1049 (Pubitemid 350273618)
6. Shinoda, T., Ogawa, H., Cornelius, F., and Toyoshima, C. (2009) Crystal structure of the sodium-potassium pump at 2.4 angstrom resolution. Nature 459, 446-450
7. +-ATPase ion pumps. Nat. Rev. Mol. Cell Biol. 12, 60-70
8. +-ATPase. FEBS Lett. 584, 2589-2595
9. +-ATPase activity is not associated with internalization of the enzyme. Acta Physiol. Scand. 164, 39-46
10. + pumps. Acta Physiol. Scand. 185, 329-334
11. +-ATPase and mapping of isoform differences and disease-related mutations. Philos. Trans. R. Soc. B Biol. Sci. 364, 217-227
12. +-ATPase. J. Physiol. 518, 37-46
13. +-ATPase in the striatum upon activation of opioid receptors by morphine. Mol. Pharmacol. 71, 519-530
14. +-ATPase activity in rat hippocampus: implications for neurological diseases. J. Neurochem. 109, 416-426
15. Kristensen, B., Birkelund, S., and Jorgensen, P. L. (2003) Trafficking of Na,K-ATPase fused to enhanced green fluorescent protein is mediated by protein kinase A or C. J. Membr. Biol. 191, 25-36 (Pubitemid 37011463)
16. + controls cell surface expression of Na,K-ATPase via a cAMP-independent PKA pathway in mammalian kidney collecting duct cells. Mol. Biol. Cell 14, 2677-2688
17. +-ATPase α-subunit. J. Gen. Physiol. 135, 115-134
18. + from the Na/K pump. Proc. Natl. Acad. Sci. U.S.A. 106, 15507-15512
19. Wang, H. L., Cheng, X., Taylor, P., McCammon, J. A., and Sine, S. M. (2008) Control of cation permeation through the nicotinic receptor channel. PLoS Comp. Biol. 4, e41
20. Law, R. J., Munson, K., Sachs, G., and Lightstone, F. C. (2008) An ion gating mechanism of gastric H,K-ATPase based on molecular dynamics simulations. Biophys. J. 95, 2739-2749
21. Espinoza-Fonseca, L. M., and Thomas, D. D. (2011) Atomic-level characterization of the activation mechanism of SERCA by calcium. PLoS One 6, e26936
22. 2+-ATPase: a molecular modeling study. Biochemistry 50, 11109-11120
23. Witzke, S., Duelund, L., Petersen, M., Kongsted, J., Mouritsen, O. G., and Khandelia, H. (2010) The inclusion of terpenoid plant extracts in lipid bilayers investigated by molecular dynamics simulations. J. Phys. Chem. B 114, 15825-15831
24. Berendsen, H. J. C., van der Spoel, D., and van Drunen, R. (1995) GROMACS: a message-passing parallel molecular dynamics implementation. Comput. Phys. Commun. 91, 43-56
25. Hess, B., Kutzner, C., van der Spoel, D., and Lindahl, E. (2008) GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theoret. Comput. 4, 435-447
26. Spoel, D. V. D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., and Berendsen, H. J. C. (2005) GROMACS: fast, flexible, and free. J. Comput. Chem. 26, 1701-1718 (Pubitemid 43076182)
27. Berger, O., Edholm, O., and Jähnig, F. (1997) Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophys. J. 72, 2002-2013 (Pubitemid 27184429)
28. Jorgensen, W. L., Maxwell, D. S., and TiradoRives, J. (1996) Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J. Am. Chem. Soc. 118, 11225-11236 (Pubitemid 26399746)
29. Tieleman, D. P., Maccallum, J. L., Ash, W. L., Kandt, C., Xu, Z., and Monticelli, L. (2006) Membrane protein simulations with a united-atom lipid and all-atom protein model: lipid-protein interactions, side chain transfer free energies, and model proteins. J. Phys. Condens. Matter 18, S1221-1234 (Pubitemid 43982969)
30. Chakrabarti, N., Neale, C., Payandeh, J., Pai, E. F., and Pomès, R. (2010) An iris-like mechanism of pore dilation in the CorA magnesium transport system. Biophys. J. 98, 784-792
31. Provasi, D., Bortolato, A., and Filizola, M. (2009) Exploring molecular mechanisms of ligand recognition by opioid receptors with metadynamics. Biochemistry 48, 10020-10029
32. Ramachandran, S., Serohijos, A. W., Xu, L., Meissner, G., and Dokholyan, N. V. (2009) A structural model of the pore-forming region of the skeletal muscle ryanodine receptor (RyR1) PLoS Comp. Biol. 5, e1000367
33. Stansfeld, P. J., and Sansom, M. S. (2011) Molecular simulation approaches to membrane proteins. Structure 19, 1562-1572
34. Piana, S., Lindorff-Larsen, K., and Shaw, D. E. (2011) How robust are protein folding simulations with respect to force field parameterization? Biophys. J. 100, L47-49
35. Berendsen, H. J. C., Postma, J. P. M., Vangunsteren, W. F., Dinola, A., and Haak, J. R. (1984) Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684-3690
36. Leach, A. R. (2001) Molecular Modelling: Principles and Applications, 2nd Ed., pp. 356-357, Pearson Prentice Hall, Harlow, UK
37. Hess, B. (2008) P-LINCS: a parallel linear constraint solver for molecular simulation. J. Chem. Theoret. Comput. 4, 116-122
38. Hess, B., Bekker, H., Berendsen, H. J. C., and Fraaije, J. G. E. M. (1997) LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 18, 1463-1472 (Pubitemid 127637344)
39. Miyamoto, S., and Kollman, P. A. (1992) Settle: an analytical version of the SHAKE and RATTLE algorithm for rigid water models. J. Comput. Chem. 13, 952-962
40. Darden, T., York, D., and Pedersen, L. (1993) Particle mesh Ewald: An Nlog(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089-10092
41. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: visual molecular dynamics. J. Mol. Graphics 14, 33-38 (Pubitemid 26152973)
42. 935 J. Biol. Chem. 284, 18715-18725
43. Awayda, M. S., Ismailov, I. I., Berdiev, B. K., Fuller, C. M., and Benos, D. J. (1996) Protein kinase regulation of a cloned epithelial Na+ channel. J. Gen. Physiol. 108, 49-65 (Pubitemid 26238812)
44. Lee, Y. S., Lee, J. A., Jung, J., Oh, U., and Kaang, B. K. (2000) The cAMP-dependent kinase pathway does not sensitize the cloned vanilloid receptor type 1 expressed in Xenopus oocytes or Aplysia neurons. Neurosci. Lett. 288, 57-60 (Pubitemid 30408438)
45. Groban, E. S., Narayanan, A., and Jacobson, M. P. (2006) Conformational changes in protein loops and helices induced by post-translational phosphorylation. PLoS Comp. Biol. 2, e32
46. Chibalin, A. V., Vasilets, L. A., Hennekes, H., Pralong, D., and Geering, K. (1992) Phosphorylation of Na,K-ATPase α-subunits in microsomes and in homogenates of Xenopus oocytes resulting from the stimulation of protein kinase A and protein kinase C. J. Biol. Chem. 267, 22378-22384
47. +-ATPase a2-subunit causing familial hemiplegic migraine type 2. J. Biol. Chem. 283, 31097-31106
48. Feschenko, M. S., and Sweadner, K. J. (1994) Conformation-dependent phosphorylation of Na,K-ATPase by protein kinase A and protein kinase C. J. Biol. Chem. 269, 30436-30444 (Pubitemid 24376522)
49. +-ATPase endocytosis and recruitment to the plasma membrane Ann. N.Y. Acad. Sci. 986, 587-594
50. Codina, J., Liu, J., Bleyer, A. J., Penn, R. B., and DuBose, T. D. (2006) Phosphorylation of S-955 at the protein kinase A consensus promotes maturation of the α- subunit of the colonic H+,K+-ATPase. J. Am. Soc. Nephrol. 17, 1833-1840 (Pubitemid 44036167)
51. Blanco, G., and Mercer, R. W. (1998) Isozymes of the Na-K-ATPase: heterogeneity in structure, diversity in function. Am. J. Physiol. 275, F633-650