Phosphorylation and activation of the plasma membrane Na +/H + exchanger (NHE1) during osmotic cell shrinkage

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Rigor, Robert R ^a   Damoc, Catalina ^b   Phinney, Brett S ^b   Cala, Peter M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALYCULIN A; SERINE; SODIUM PROTON EXCHANGE PROTEIN 1; THREONINE; CATION TRANSPORT PROTEIN; SLC9A1 PROTEIN, HUMAN; SODIUM; SODIUM PROTON EXCHANGE PROTEIN;

AMPHIUMA TRIDACTYLUM; ANIMAL CELL; ARTICLE; CELL VOLUME; CONTROLLED STUDY; ERYTHROCYTE MEMBRANE; IMMUNOPRECIPITATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MICHAELIS MENTEN KINETICS; NONHUMAN; OSMOSIS; OSMOTIC CELL SHRINKAGE; PROTEIN PHOSPHORYLATION; SALAMANDER; SIGNAL TRANSDUCTION; SODIUM TRANSPORT; AMINO ACID SEQUENCE; CELL SIZE; CHEMISTRY; CYTOLOGY; ERYTHROCYTE; HUMAN; ION TRANSPORT; KINETICS; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; SEQUENCE HOMOLOGY; TANDEM MASS SPECTROMETRY;

AMPHIUMA TRIDACTYLUM; VERTEBRATA;

AMINO ACID SEQUENCE; CATION TRANSPORT PROTEINS; CELL SIZE; CHROMATOGRAPHY, LIQUID; ERYTHROCYTES; HUMANS; IMMUNOPRECIPITATION; ION TRANSPORT; KINETICS; MOLECULAR SEQUENCE DATA; OSMOSIS; PHOSPHORYLATION; SEQUENCE HOMOLOGY, AMINO ACID; SODIUM; SODIUM-HYDROGEN ANTIPORTER; TANDEM MASS SPECTROMETRY;

EID: 84555205226     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029210     Document Type: Article

References (51)

1. Hoffmann EK, Pedersen SF, (2010) Cell volume homeostatic mechanisms: effectors and signalling pathways. Acta Physiol (Oxf).
2. Hoffmann EK, Lambert IH, Pedersen SF, (2009) Physiology of cell volume regulation in vertebrates. Physiological Reviews 89: 193-277.
3. Pedersen SF, O'Donnell ME, Anderson SE, Cala PM, (2006) Physiology and pathophysiology of Na+/H+ exchange and Na+-K+-2Cl- cotransport in the heart, brain, and blood. Am J Physiol Regul Integr Comp Physiol 291: R1-25.
4. Pedersen SF, (2006) The Na(+)/H (+) exchanger NHE1 in stress-induced signal transduction: implications for cell proliferation and cell death. Pflugers Arch 452: 249-259.
5. Malo ME, Fliegel L, (2006) Physiological role and regulation of the Na+/H+ exchanger. Can J Physiol Pharmacol 84: 1081-1095.
6. Karmazyn M, Sawyer M, Fliegel L, (2005) The Na(+)/H(+) exchanger: a target for cardiac therapeutic intervention. Curr Drug Targets Cardiovasc Haematol Disord 5: 323-335.
7. Putney LK, Denker SP, Barber DL, (2002) The changing face of the Na+/H+ exchanger, NHE1: structure, regulation, and cellular actions. Annu Rev Pharmacol Toxicol 42: 527-552.
8. Pedersen SF, Cala PM, (2004) Comparative biology of the ubiquitous Na+/H+ exchanger, NHE1: lessons from erythrocytes. J Exp Zoolog A Comp Exp Biol 301: 569-578.
9. Lang F, (2007) Mechanisms and significance of cell volume regulation. J Am Coll Nutr 26: 613S-623S.
10. Pedersen SF, Hoffmann EK, Mills JW, (2001) The cytoskeleton and cell volume regulation. Comp Biochem Physiol A Mol Integr Physiol 130: 385-399.
11. Hoffmann EK, Pedersen SF, (2006) Sensors and signal transduction pathways in vertebrate cell volume regulation. Contrib Nephrol 152: 54-104.
12. Grinstein S, Furuya W, Bianchini L, (1992) Protein Kinases, Phosphatases and the Control of Cell Volume. NIPS 7: 232-237.
13. Cala PM, (1983) Volume regulation by red blood cells: Mechanisms of ion transport. Journal of Molecular Physiology 4: 33-52.
14. Meima ME, Webb BA, Witkowska HE, Barber DL, (2009) The sodium-hydrogen exchanger NHE1 is an Akt substrate necessary for actin filament reorganization by growth factors. J Biol Chem 284: 26666-26675.
15. Coccaro E, Karki P, Cojocaru C, Fliegel L, (2009) Phenylephrine and sustained acidosis activate the neonatal rat cardiomyocyte Na+/H+ exchanger through phosphorylation of amino acids Ser770 and Ser771. Am J Physiol Heart Circ Physiol 297: H846-858.
16. Grenier AL, Abu-ihweij K, Zhang G, Ruppert SM, Boohaker R, et al. (2008) Apoptosis-induced alkalinization by the Na+/H+ exchanger isoform 1 is mediated through phosphorylation of amino acids Ser726 and Ser729. Am J Physiol Cell Physiol 295: C883-896.
17. Snabaitis AK, Cuello F, Avkiran M, (2008) Protein kinase B/Akt phosphorylates and inhibits the cardiac Na+/H+ exchanger NHE1. Circ Res 103: 881-890.
18. Malo ME, Li L, Fliegel L, (2007) Mitogen-activated protein kinase-dependent activation of the Na+/H+ exchanger is mediated through phosphorylation of amino acids Ser770 and Ser771. J Biol Chem 282: 6292-6299.
19. Li X, Liu Y, Alvarez BV, Casey JR, Fliegel L, (2006) A Novel Carbonic Anhydrase II Binding Site Regulates NHE1 Activity. Biochemistry 45: 2414-2424.
20. Liu H, Stupak J, Zheng J, Keller BO, Brix BJ, et al. (2004) Open tubular immobilized metal ion affinity chromatography combined with MALDI MS and MS/MS for identification of protein phosphorylation sites. Anal Chem 76: 4223-4232.
21. Lehoux S, Abe J, Florian JA, Berk BC, (2001) 14-3-3 Binding to Na+/H+ exchanger isoform-1 is associated with serum- dependent activation of Na+/H+ exchange. J Biol Chem 276: 15794-15800.
22. Takahashi E, Abe J, Gallis B, Aebersold R, Spring DJ, et al. (1999) p90(RSK) is a serum-stimulated Na+/H+ exchanger isoform-1 kinase. Regulatory phosphorylation of serine 703 of Na+/H+ exchanger isoform-1. J Biol Chem 274: 20206-20214.
23. Grinstein S, Woodside M, Sardet C, Pouyssegur J, Rotin D, (1992) Activation of the Na+/H+ antiporter during cell volume regulation. Evidence for a phosphorylation-independent mechanism. J Biol Chem 267: 23823-23828.
24. Bianchini L, Woodside M, Sardet C, Pouyssegur J, Takai A, et al. (1991) Okadaic acid, a phosphatase inhibitor, induces activation and phosphorylation of the Na+/H+ antiport. J Biol Chem 266: 15406-15413.
25. Livne AA, Sardet C, Pouyssegur J, (1991) The Na+/H+ exchanger is phosphorylated in human platelets in response to activating agents. FEBS Lett 284: 219-222.
26. Sardet C, Fafournoux P, Pouyssegur J, (1991) Alpha-thrombin, epidermal growth factor, and okadaic acid activate the Na+/H+ exchanger, NHE-1, by phosphorylating a set of common sites. J Biol Chem 266: 19166-19171.
27. Holt ME, King SA, Cala PM, Pedersen SF, (2006) Regulation of the Pleuronectes americanus Na+/H+ exchanger by osmotic shrinkage, beta-adrenergic stimuli, and inhibition of Ser/Thr protein phosphatases. Cell Biochem Biophys 45: 1-18.
28. McSwine RL, Li J, Villereal ML, (1996) Examination of the role for Ca2+ in regulation and phosphorylation of the Na+/H+ antiporter NHE1 via mitogen and hypertonic stimulation. J Cell Physiol 168: 8-17.
29. Bianchini L, Kapus A, Lukacs G, Wasan S, Wakabayashi S, et al. (1995) Responsiveness of mutants of NHE1 isoform of Na+/H+ antiport to osmotic stress. American Journal of Physiology 269: C998-1007.
30. Cala PM, (1980) Volume regulation by Amphiuma red blood cells. The membrane potential and its implications regarding the nature of the ion-flux pathways. Journal of General Physiology 76: 683-708.
31. Ortiz-Acevedo A, Rigor RR, Maldonado HM, Cala PM, (2008) Activation of Na+/H+ and K+/H+ exchange by calyculin A in Amphiuma tridactylum red blood cells: implications for the control of volume-induced ion flux activity. Am J Physiol Cell Physiol 295: C1316-1325.
32. Ortiz-Acevedo A, Rigor RR, Maldonado HM, Cala PM, (2010) Coordinated control of volume regulatory Na+/H+ and K+/H+ exchange pathways in Amphiuma red blood cells. Am J Physiol Cell Physiol.
33. Cala PM, Maldonado HM, (1994) pH regulatory Na/H exchange by Amphiuma red blood cells. J Gen Physiol 103: 1035-1053.
34. McLean LA, Zia S, Gorin FA, Cala PM, (1999) Cloning and expression of the Na+/H+ exchanger from Amphiuma RBCs: resemblance to mammalian NHE1. Am J Physiol 276: C1025-1037.
35. Herschlag D, Johnson FB, (1993) Synergism in transcriptional activation: a kinetic view. Genes Dev 7: 173-179.
36. Cleland WW, (1975) Partition analysis and the concept of net rate constants as tools in enzyme kinetics. Biochemistry 14: 3220-3224.
37. Yan W, Nehrke K, Choi J, Barber DL, (2001) The Nck-interacting kinase (NIK) phosphorylates the Na+-H+ exchanger NHE1 and regulates NHE1 activation by platelet-derived growth factor. Journal of Biological Chemistry 276: 31349-31356.
38. Baumgartner M, Sillman AL, Blackwood EM, Srivastava J, Madson N, et al. (2006) The Nck-interacting kinase phosphorylates ERM proteins for formation of lamellipodium by growth factors. Proc Natl Acad Sci U S A 103: 13391-13396.
39. Rasmussen M, Alexander RT, Darborg BV, Mobjerg N, Hoffmann EK, et al. (2008) Osmotic cell shrinkage activates ezrin/radixin/moesin (ERM) proteins: activation mechanisms and physiological implications. Am J Physiol Cell Physiol 294: C197-212.
40. Bianchini L, L'Allemain G, Pouyssegur J, (1997) The p42/p44 mitogen-activated protein kinase cascade is determinant in mediating activation of the Na+/H+ exchanger (NHE1 isoform) in response to growth factors. J Biol Chem 272: 271-279.
41. Bertrand B, Wakabayashi S, Ikeda T, Pouyssegur J, Shigekawa M, (1994) The Na+/H+ exchanger isoform 1 (NHE1) is a novel member of the calmodulin-binding proteins. Identification and characterization of calmodulin-binding sites. J Biol Chem 269: 13703-13709.
42. Köster S, Pavkov-Keller T, Kühlbrandt W, Yildiz Ö, (2011) Structure of human Na+/H+ exchanger NHE1 regulatory region in complex with CaM and Ca2+. J Biol Chem In press.
43. Wakabayashi S, Ikeda T, Iwamoto T, Pouysségur J, Shigekawa M, (1997) Calmodulin-binding autoinhibitory domain controls "pH-sensing" in the Na+/H+ exchanger NHE1 through sequence-specific interaction. Biochemistry 36: 12854-12861.
44. Cala PM, (1985) Volume regulation by Amphiuma red blood cells: strategies for identifying alkali metal/H+ transport. Federation Proceedings 44: 2500-2507.
45. Lytle C, (1997) Activation of the avian erythrocyte Na-K-Cl cotransport protein by cell shrinkage, cAMP, fluoride, and calyculin-A involves phosphorylation at common sites. J Biol Chem 272: 15069-15077.
46. Musch MW, Hubert EM, Goldstein L, (1999) Volume expansion stimulates p72(syk) and p56(lyn) in skate erythrocytes. J Biol Chem 274: 7923-7928.
47. Schneider C, Newman RA, Sutherland DR, Asser U, Greaves MF, (1982) A one-step purification of membrane proteins using a high efficiency immunomatrix. J Biol Chem 257: 10766-10769.
48. Rowley A, Choudhary JS, Marzioch M, Ward MA, Weir M, et al. (2000) Applications of protein mass spectrometry in cell biology. Methods 20: 383-397.
49. Shevchenko A, Wilm M, Vorm O, Mann M, (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68: 850-858.
50. Keller A, Nesvizhskii AI, Kolker E, Aebersold R, (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74: 5383-5392.
51. Nesvizhskii AI, Keller A, Kolker E, Aebersold R, (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75: 4646-4658.