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

American Journal of Physiology - Cell Physiology

Volumn 295, Issue 5, 2008, Pages

  Ortiz Acevedo, Alejandro ^a,b   Rigor, Robert R ^a,c   Maldonado, Hector M ^a,d   Cala, Peter M ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF PUERTO RICO   (Puerto Rico)

^c NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^d SCHOOL OF MEDICINE   (Puerto Rico)

Author keywords

Cell volume regulation; Phosphatase inhibitors; Phosphoprotein; Phosphorylation; Volume dependent coordination of K loss and na uptake

Indexed keywords

CALYCULIN A; POTASSIUM ION; RUBIDIUM 86; SODIUM 22; SODIUM ION;

ARTICLE; CELL SWELLING; CELL VOLUME; CONTROLLED STUDY; DRUG EFFECT; ENZYME INHIBITION; ERYTHROCYTE; ION CURRENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SALAMANDER; SODIUM TRANSPORT;

AMILORIDE; ANIMALS; CELL SIZE; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; ERYTHROCYTES; OSMOTIC PRESSURE; OXAZOLES; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; POTASSIUM; POTASSIUM-HYDROGEN ANTIPORTERS; PROTEIN KINASES; RUTHENIUM; SODIUM; SODIUM-HYDROGEN ANTIPORTER; TIME FACTORS; URODELA;

AMPHIUMA; AMPHIUMA TRIDACTYLUM; VERTEBRATA;

EID: 57349185697     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00160.2008     Document Type: Article

References (51)

1. Adorante JS, Cala PM. Activation of electroneutral K flux in Amphiuma red blood cells by N-ethylmaleimide. Distinction between K/H exchange and KCl cotransport. J Gen Physiol 90: 209-227, 1987.
2. Aharonovitz O, Demaurex N, Woodside M, Grinstein S. ATP dependence is not an intrinsic property of Na+/H+ exchanger NHE1: requirement for an ancillary factor. Am J Physiol Cell Physiol 276: C1303-C1311, 1999.
3. Aharonovitz O, Zaun HC, Balla T, York JD, Orlowski J, Grinstein S. Intracellular pH regulation by Na(+)/H(+) exchange requires phosphatidylinositol 4,5-bisphosphate. J Cell Biol 150: 213-224, 2000.
4. Bertrand B, Wakabayashi S, Ikeda T, Pouysségur J, Shigekawa M. 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, 1994.
5. Bianchini L, Woodside M, Sardet C, Pouyssegur J, Takai A, Grinstein S. Okadaic acid, a phosphatase inhibitor, induces activation and phosphorylation of the Na+/H+ antiport. J Biol Chem 266: 15406-15413, 1991.
6. Bize I. Theoretical validation for a model of KCC regulation in human erythrocytes. Blood Cells Mol Dis 27: 121-126, 2001.
7. Bize I, Guvenc B, Buchbinder G, Brugnara C. Stimulation of human erythrocyte K-Cl cotransport and protein phosphatase type 2A by n-ethylmaleimide: role of intracellular Mg++. J Membr Biol 177: 159-168, 2000.
8. Cala PM. Volume regulation by Amphiuma red blood cells: The membrane potential and its implications regarding the nature of the ion-flux pathways. J Gen Physiol 76: 683-708, 1980.
9. Cala PM. Volume regulation by Amphiuma red blood cells: strategies for identifying alkali metal/H+ transport. Fed Proc 44: 2500-2507, 1985.
10. Cala PM. Volume-sensitive alkali metal-H transport in Amphiuma red blood cells. In: Current Topics in Membranes and Transport. New York: Academic, 1986, p. 79-99.
11. Cala PM, Hoffmann KS. Alkali metal/proton exchange. Methods Enzymol 173: 330-346, 1989.
12. Cala PM, Maldonado HM. pH regulatory Na/H exchange by Amphiuma red blood cells. J Gen Physiol 103: 1035-1053, 1994.
13. Cossins AR, Gibson JS. Volume-sensitive transport systems and volume homeostasis in vertebrate red blood cells. J Exp Biol 200: 343-352, 1997.
14. Dunham PB, Klimczak J, Logue PJ. Swelling activation of K-Cl cotransport in LK sheep erythrocytes: a three-state process. J Gen Physiol 101: 733-765, 1993.
15. Goss G, Orlowski J, Grinstein S. Coimmunoprecipitation of a 24-kDa protein with NHE1, the ubiquitous isoform of the Na+/H+ exchanger. Am J Physiol Cell Physiol 270: C1493-C1502, 1996.
16. Goss GG, Woodside M, Wakabayashi S, Pouyssegur J, Waddell T, Downey GP, Grinstein S. ATP dependence of NHE-1, the ubiquitous isoform of the Na+/H+ antiporter. Analysis of phosphorylation and subcellular localization. J Biol Chem 269: 8741-8748, 1994.
17. Grinstein S, Furuya W, Bianchini L. Protein kinases, phosphatases and the control of cell volume. News Physiol 7: 232-237, 1992.
18. Grinstein S, Woodside M, Sardet C, Pouyssegur J, Rotin D. Activation of the Na+/H+ antiporter during cell volume regulation. Evidence for a phosphorylation-independent mechanism. J Biol Chem 267: 23823-23828, 1992.
19. Haas M, McManus TJ. Effect of norepinephrine on swelling-induced potassium transport in duck red cells. Evidence against a volume-regulatory decrease under physiological conditions. J Gen Physiol 85: 649-667, 1985.
20. Hardy SP, Goodfellow HR, Valverde MA, Gill DR, Sepulveda V, Higgins CF. Protein kinase C-mediated phosphorylation of the human multidrug resistance P-glycoprotein regulates cell volume-activated chloride channels [published erratum appears in EMBO J 1995 Apr 18;14(8): 1844]. EMBO J 14: 68-75, 1995.
21. Hill JK, Brett CL, Chyou A, Kallay LM, Sakaguchi M, Rao R, Gillespie PG. Vestibular hair bundles control pH with (Na+, K+)/H+ exchangers NHE6 and NHE9. J Neurosci 26: 9944-9955, 2006.
22. Hoffmann EK, Pedersen SF. Sensors and signal transduction in the activation of cell volume regulatory ion transport systems. Contrib Nephrol 123: 50-78, 1998.
23. Hoffmann EK, Pedersen SF. Sensors and signal transduction pathways in vertebrate cell volume regulation. Contrib Nephrol 152: 54-104, 2006.
24. Holt ME, King SA, Cala PM, Pedersen SF. 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, 2006.
25. Jennings ML. Volume-sensitive K(+)/Cl(-) cotransport in rabbit erythrocytes. Analysis of the rate-limiting activation and inactivation events. J Gen Physiol 114: 743-758, 1999.
26. Jennings ML, Al-Rohil N. Kinetics of activation and inactivation of swelling-stimulated K+/Cl- transport The volume-sensitive parameter is the rate constant for inactivation. J Gen Physiol 95: 1021-1040, 1990.
27. Jennings ML, Schulz RK. Okadaic acid inhibition of KCl cotransport. Evidence that protein dephosphorylation is necessary for activation of transport by either cell swelling or N-ethylmaleimide. J Gen Physiol 97: 799-817, 1991.
28. Lauf PK, Bauer J, Adragna NC, Fujise H, Zade-Oppen AM, Ryu KH, Delpire E. Erythrocyte K-Cl cotransport: properties and regulation. Am J Physiol Cell Physiol 263: C917-C932, 1992.
29. Li X, Liu Y, Alvarez BV, Casey JR, Fliegel L. A Novel Carbonic Anhydrase II Binding Site Regulates NHE1 Activity. Biochemistry 45: 2414-2424, 2006.
30. Li X, Liu Y, Kay CM, Muller-Esterl W, Fliegel L. The Na+/H+ exchanger cytoplasmic tail: structure, function, and interactions with tescalcin. Biochemistry 42: 7448-7456, 2003.
31. Lin X, Barber DL. A calcineurin homologous protein inhibits GTPase-stimulated Na-H exchange. Proc Nat Acad Sci USA 93: 12631-12636, 1996.
32. + exchange, and cell volume in ferret erythrocytes. Am J Physiol Cell Physiol 271: C1603-C1611, 1996.
33. Malo ME, Li L, Fliegel L. 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, 2007.
34. + exchanger from Ampiuma RBCs: resemblance to mammalian NHE1. Am J Physiol Cell Physiol 276: C1025-C1037, 1999.
35. McSwine RL, Li J, Villereal ML. 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, 1996.
36. Orlowski J, Grinstein S. Diversity of the mammalian sodium/proton exchanger SLC9 gene family. Pflügers Arch 447: 549-565, 2004.
37. Pang T, Hisamitsu T, Mori H, Shigekawa M, Wakabayashi S. Role of calcineurin B homologous protein in pH regulation by the Na+/H+ exchanger 1: tightly bound Ca2+ ions as important structural elements. Biochemistry 43: 3628-3636, 2004.
38. Pang T, Su X, Wakabayashi S, Shigekawa M. Calcineurin homologous protein as an essential cofactor for Na+/H+ exchangers. J Biol Chem 276: 17367-17372, 2001.
39. Parker JC, Colclasure GC, McManus TJ. Coordinated regulation of shrinkage-induced Na/H exchange and swelling-induced [K-Cl] cotransport in dog red cells. Further evidence from activation kinetics and phosphatase inhibition. J Gen Physiol 98: 869-880, 1991.
40. Parker JC, McManus TJ, Starke LC, Gitelman HJ. Coordinated regulation of Na/H exchange and [K-Cl] cotransport in dog red cells. J Gen Physiol 96: 1141-1152, 1990.
41. Pedersen SF, Kramhoft B, Jorgensen NK, Hoffmann EK. Shrinkage-induced activation of the Na+/H+ exchanger in Ehrlich ascites tumor cells: mechanisms involved in the activation and a role for the exchanger in cell volume regulation. J Membr Biol 149: 141-159, 1996.
42. Robson L, Hunter M. Role of cell volume and protein kinase C in regulation of a Cl- conductance in single proximal tubule cells of Rana temporaria. J Physiol 480: 1-7, 1994.
43. Sardet C, Counillon L, Franchi A, Pouyssegur J. Growth factors induce phosphorylation of the Na+/H+ antiporter, glycoprotein of 110 kD. Science 247: 723-726, 1990.
44. Sardet C, Fafournoux P, Pouysségur J. 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, 1991.
45. Sarkadi B, Mack E, Rothstein A. Ionic events during the volume response of human peripheral blood lymphocytes to hypotonic media. I. Distinctions between volume-activated Cl- and K+ conductance pathways. J Gen Physiol 83: 497-512, 1984.
46. Silva NL, Haworth RS, Singh D, Fliegel L. The carboxyl-terminal region of the Na+/H+ exchanger interacts with mammalian heat shock protein. Biochemistry 34: 10412-10420, 1995.
47. Starke LC, Jennings ML. K-Cl cotransport in rabbit red cells: further evidence for regulation by protein phosphatase type 1. Am J Physiol Cell Physiol 264: C118-C124, 1993.
48. Takahashi E, Abe J, Gallis B, Aebersold R, Spring DJ, Krebs EG, Berk BC. 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, 1999.
49. Tilly BC, van, den Berghe N, Tertoolen LG, Edixhoven MJ, de JH. Protein tyrosine phosphorylation is involved in osmoregulation of ionic conductances. J Biol Chem 268: 19919-19922, 1993.
50. Wakabayashi S, Bertrand B, Shigekawa M, Fafournoux P, Pouysségur J. Growth factor activation and "H(+)-sensing" of the Na+/H+ exchanger isoform 1 (NHE1). Evidence for an additional mechanism not requiring direct phosphorylation. J Biol Chem 269: 5583-5588, 1994.
51. Wakabayashi S, Ikeda T, Iwamoto T, Pouysségur J, Shigekawa M. Calmodulin-binding autoinhibitory domain controls "pH-sensing" in the Na+/H+ exchanger NHE1 through sequence-specific interaction. Biochemistry 36: 12854-12861, 1997.