Functional importance of charged residues within the putative intracellular loops in pH regulation by Na+/H+ exchanger NHE1

FEBS Journal

Volumn 274, Issue 16, 2007, Pages 4326-4335

  Hisamitsu, Takashi ^a   Yamada, Keiji ^a   Nakamura, Tomoe Y ^a   Wakabayashi, Shigeo ^a  

^a NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

Author keywords

Charge reversal mutation; Na+ H+ exchanger; pH regulation; Surface labeling; Transport kinetics

Indexed keywords

5 (N ETHYL N ISOPROPYL)AMILORIDE; ARGININE; ASPARTIC ACID; GLUTAMIC ACID; GROWTH FACTOR; LITHIUM ION; MUTANT PROTEIN; SODIUM 22; SODIUM PROTON EXCHANGE PROTEIN 1;

ACIDITY; ALKALINITY; ANIMAL CELL; ANION EXCHANGE; ARTICLE; BINDING AFFINITY; CELL MEMBRANE; CELL PH; CONTROLLED STUDY; HYPEROSMOLARITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERTANT; SODIUM TRANSPORT;

AMINO ACID SUBSTITUTION; AMINO ACIDS; ANIMALS; CELL LINE; CELL MEMBRANE; FIBROBLASTS; HUMANS; HYDROGEN-ION CONCENTRATION; IMMUNOBLOTTING; ION TRANSPORT; MUTANT PROTEINS; MUTATION; SODIUM; SODIUM RADIOISOTOPES; SODIUM-HYDROGEN ANTIPORTER; TRANSFECTION;

EID: 34547779435     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.05962.x     Document Type: Article

References (43)

1. Wakabayashi S, Shigekawa M Pouysségur J (1997) Molecular physiology of vertebrate Na+/H+ exchangers. Physiol Rev 77, 51 74.
2. Orlowski J Grinstein S (2004) Diversity of the mammalian sodium/proton exchanger SLC9 gene family. Pflugers Arch 447, 549 565.
3. Counillon L Pouysségur J (2000) The expanding family of eucaryotic Na+/H+ exchangers. J Biol Chem 275, 1 4.
4. 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.
5. Slepkov E Fliegel L (2002) Structure and function of the NHE1 isoform of the Na+/H+ exchanger. Biochem Cell Biol 80, 499 508.
6. Zachos NC, Tse M Donowitz M (2005) Molecular physiology of intestinal Na+/H+ exchange. Annu Rev Physiol 67, 411 443.
7. Karmazyn M, Sostaric JV Gan XT (2001) The myocardial Na+/H+ exchanger: a potential therapeutic target for the prevention of myocardial ischaemic and reperfusion injury and attenuation of postinfarction heart failure. Drugs 61, 375 389.
8. Engelhardt S, Hein L, Keller U, Klambt K Lohse MJ (2002) Inhibition of Na+-H+ exchange prevents hypertrophy, fibrosis, and heart failure in β1-adrenergic receptor transgenic mice. Circ Res 90, 814 819.
9. Aronson PS, Nee J Suhm MA (1982) Modifier role of internal H+ in activating the Na+-H+ exchanger in renal microvillus membrane vesicles. Nature 299, 161 163.
10. Aronson PS (1985) Kinetic properties of the plasma membrane Na+-H+ exchanger. Annu Rev Physiol 47, 545 560.
11. Wakabayashi S, Hisamitsu T, Pang T Shigekawa M (2003) Kinetic dissection of two distinct proton binding sites in Na+/H+ exchangers by measurement of reverse mode reaction. J Biol Chem 278, 43580 43585.
12. Hisamitsu T, Pang T, Shigekawa M Wakabayashi S (2004) Dimeric interaction between the cytoplasmic domains of the Na+/H+ exchanger NHE1 revealed by symmetrical intermolecular cross-linking and selective co-immunoprecipitation. Biochemistry 43, 11135 11143.
13. Fafournoux P, Noël J Pouysségur J (1994) Evidence that Na+/H+ exchanger isoforms NHE1 and NHE3 exist as stable dimers in membranes with a high degree of specificity for homodimers. J Biol Chem 269, 2589 2596.
14. Hisamitsu T, Ben Ammar Y, Nakamura TY Wakabayashi S (2006) Dimerization is crucial for the function of the Na+/H+ exchanger NHE1. Biochemistry 45, 13346 13355.
15. Ikeda T, Schmitt B, Pouysségur J, Wakabayashi S Shigekawa M (1997) Identification of cytoplasmic subdomains that control pH-sensing of the Na+/H+ exchanger (NHE1): pH-maintenance, ATP-sensitive, and flexible loop domains. J Biochem (Tokyo) 121, 295 303.
16. Pang T, Hisamitsu T, Mori H, Shigekawa M Wakabayashi S (2004) 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.
17. Pang T, Su X, Wakabayashi S Shigekawa M (2001) Calcineurin homologous protein as an essential cofactor for Na+/H+ exchangers. J Biol Chem 276, 17367 17372.
18. Ben Ammar Y, Takeda S, Hisamitsu T, Mori H Wakabayashi S (2006) Crystal structure of CHP2 complexed with NHE1-cytosolic region and an implication for pH regulation. EMBO J 25, 2315 2325.
19. Wakabayashi S, Hisamitsu T, Pang T Shigekawa M (2003) Mutations of Arg440 and Gly455/Gly456 oppositely change pH sensing of Na+/H+ exchanger J Biol Chem 278, 11828 11835.
20. Lacroix J, Poet M, Maehrel C Counillon L (2004) A mechanism for the activation of the Na/H exchanger NHE-1 by cytoplasmic acidification and mitogens. EMBO Rep 5, 91 96.
21. Pouysségur J, Sardet C, Franchi A, L'Allemain G Paris S (1984) A specific mutation abolishing Na+/H+ antiport activity in hamster fibroblasts precludes growth at neutral and acidic pH. Proc Natl Acad Sci USA 81, 4833 4837.
22. Wakabayashi S, Pang T, Su X Shigekawa M (2000) A novel topology model of the human Na+/H+ exchanger isoform 1. J Biol Chem 275, 7942 7949.
23. Wakabayashi S, Fafournoux P, Sardet C Pouysségur J (1992) The Na+/H+ antiporter cytoplasmic domain mediates growth factor signals and controls 'H+-sensing'. Proc Natl Acad Sci USA 89, 2424 2428.
24. Alexander RT, Malevanets A, Durkan AM, Kocinsky HS, Aronson PS, Orlowski J Grinstein S (2007) Membrane curvature alters the activation kinetics of the epithelial Na+/H+ exchanger, NHE3. J Biol Chem 282, 7376 7384.
25. Hayashi H, Szászi K, Coady-Osberg N, Orlowski J, Kinsella JL Grinstein S (2002) A slow pH-dependent conformational transition underlies a novel mode of activation of the epithelial Na+/H+ exchanger-3 isoform. J Biol Chem 277, 11090 11096.
26. Gerchman Y, Olami Y, Rimon A, Taglicht D, Schuldiner S Padan E (1993) Histidine-226 is part of the pH sensor of NhaA, a Na+/H+ antiporter in Escherichia coli. Proc Natl Acad Sci USA 90, 1212 1216.
27. Rimon A, Gerchman Y, Olami Y, Schuldiner S Padan E (1995) Replacements of histidine 226 of NhaA-Na+/H+ antiporter of Escherichia coli. Cysteine (H226C) or serine (H226S) retain both normal activity and pH sensitivity, aspartate (H226D) shifts the pH profile toward basic pH, and alanine (H226A) inactivates the carrier at all pH values. J Biol Chem 270, 26813 26817.
28. Dibrov P, Young PG Fliegel L (1998) Functional analysis of amino acid residues essential for activity in the Na+/H+ exchanger of fission yeast. Biochemistry 37, 8282 8288.
29. Wiebe CA, Dibattista ER Fliegel L (2001) Functional role of polar amino acid residues in Na+/H+ exchangers. Biochem J 357, 1 10.
30. Cha B, Oh S, Shanmugaratnam J, Donowitz M Yun CC (2003) Two histidine residues in the juxta-membrane cytoplasmic domain of Na+/H+ exchanger isoform 3 (NHE3) determine the set point. J Membr Biol 191, 49 58.
31. Tsuboi Y, Inoue H, Nakamura N Kanazawa H (2003) Identification of membrane domains of the Na+/H+ antiporter (NhaA) protein from Helicobacter pylori required for ion transport and pH sensing. J Biol Chem 278, 21467 21473.
32. Olkhova E, Hunte C, Screpanti E, Padan E Michel H (2006) Multiconformation continuum electrostatics analysis of the NhaA Na+/H+ antiporter of Escherichia coli with functional implications. Proc Natl Acad Sci USA 103, 2629 2634.
33. Counillon L, Franchi A Pouysségur J (1993) A point mutation of the Na+/H+ exchanger gene (NHE1) and amplification of the mutated allele confer amiloride resistance upon chronic acidosis. Proc Natl Acad Sci USA 90, 4508 4512.
34. Counillon L, Noël J, Reithmeier RA Pouysségur J (1997) Random mutagenesis reveals a novel site involved in inhibitor interaction within the fourth transmembrane segment of the Na+/H+ exchanger-1. Biochemistry 36, 2951 2959.
35. Slepkov ER, Chow S, Lemieux MJ Fliegel L (2004) Proline residues in transmembrane segment IV are critical for activity, expression and targeting of the Na+/H+ exchanger isoform 1. Biochem J 379, 31 38.
36. Noël J, Germain D Vadnais J (2003) Glutamate 346 of human Na+-H+ exchanger NHE1 is crucial for modulating both the affinity for Na+ and the interaction with amiloride derivatives. Biochemistry 42, 15361 15368.
37. Orlowski J Kandasamy RA (1996) Delineation of transmembrane domains of the Na+/H+ exchanger that confer sensitivity to pharmacological antagonists. J Biol Chem 271, 19922 19927.
38. Wang D, Balkovetz DF Warnock DG (1995) Mutational analysis of transmembrane histidines in the amiloride-sensitive Na+/H+ exchanger. Am J Physiol 269, C392 C402.
39. Khadilkar A, Iannuzzi P Orlowski J (2001) Identification of sites in the second exomembrane loop and ninth transmembrane helix of the mammalian Na+/H+ exchanger important for drug recognition and cation translocation. J Biol Chem 276, 43792 43800.
40. Slepkov ER, Rainey JK, Li X, Liu Y, Cheng FJ, Lindhout DA, Sykes BD Fliegel L (2005) Structural and functional characterization of transmembrane segment IV of the NHE1 isoform of the Na+/H+ exchanger. J Biol Chem 280, 17863 17872.
41. Vinothkumar KR, Smits SH Kuhlbrandt W (2005) pH-induced structural change in a sodium/proton antiporter from Methanococcus jannaschii. EMBO J 24, 2720 2729.
42. Hunte C, Screpanti E, Venturi M, Rimon A, Padan E Michel H (2005) Structure of a Na+/H+ antiporter and insights into mechanism of action and regulation by pH. Nature 435, 1197 1202.
43. Yamashita A, Singh SK, Kawate T, Jin Y Gouaux E (2005) Crystal structure of a bacterial homologue of Na+/Cl- dependent neurotransmitter transporters. Nature 437, 215 223.