Literature DB >> 28028214

Arginine substitution of a cysteine in transmembrane helix M8 converts Na+,K+-ATPase to an electroneutral pump similar to H+,K+-ATPase.

Rikke Holm1, Jaanki Khandelwal2, Anja P Einholm1, Jens P Andersen1, Pablo Artigas3, Bente Vilsen4.   

Abstract

Na+,K+-ATPase and H+,K+-ATPase are electrogenic and nonelectrogenic ion pumps, respectively. The underlying structural basis for this difference has not been established, and it has not been revealed how the H+,K+-ATPase avoids binding of Na+ at the site corresponding to the Na+-specific site of the Na+,K+-ATPase (site III). In this study, we addressed these questions by using site-directed mutagenesis in combination with enzymatic, transport, and electrophysiological functional measurements. Replacement of the cysteine C932 in transmembrane helix M8 of Na+,K+-ATPase with arginine, present in the H+,K+-ATPase at the corresponding position, converted the normal 3Na+:2K+:1ATP stoichiometry of the Na+,K+-ATPase to electroneutral 2Na+:2K+:1ATP stoichiometry similar to the electroneutral transport mode of the H+,K+-ATPase. The electroneutral C932R mutant of the Na+,K+-ATPase retained a wild-type-like enzyme turnover rate for ATP hydrolysis and rate of cellular K+ uptake. Only a relatively minor reduction of apparent Na+ affinity for activation of phosphorylation from ATP was observed for C932R, whereas replacement of C932 with leucine or phenylalanine, the latter of a size comparable to arginine, led to spectacular reductions of apparent Na+ affinity without changing the electrogenicity. From these results, in combination with structural considerations, it appears that the guanidine+ group of the M8 arginine replaces Na+ at the third site, thus preventing Na+ binding there, although allowing Na+ to bind at the two other sites and become transported. Hence, in the H+,K+-ATPase, the ability of the M8 arginine to donate an internal cation binding at the third site is decisive for the electroneutral transport mode of this pump.

Entities:  

Keywords:  H+,K+-pump; Na+,K+-pump; alternating hemiplegia of childhood; electrogenicity; internal cation

Mesh:

Substances:

Year:  2016        PMID: 28028214      PMCID: PMC5240710          DOI: 10.1073/pnas.1617951114

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  31 in total

1.  A third Na+-binding site in the sodium pump.

Authors:  Ciming Li; Oihana Capendeguy; Käthi Geering; Jean-Daniel Horisberger
Journal:  Proc Natl Acad Sci U S A       Date:  2005-08-25       Impact factor: 11.205

2.  Rescue of Na+ affinity in aspartate 928 mutants of Na+,K+-ATPase by secondary mutation of glutamate 314.

Authors:  Rikke Holm; Anja P Einholm; Jens P Andersen; Bente Vilsen
Journal:  J Biol Chem       Date:  2015-02-24       Impact factor: 5.157

3.  Sodium and proton effects on inward proton transport through Na/K pumps.

Authors:  Travis J Mitchell; Camila Zugarramurdi; J Fernando Olivera; Craig Gatto; Pablo Artigas
Journal:  Biophys J       Date:  2014-06-17       Impact factor: 4.033

4.  Kinetics of transient pump currents generated by the (H,K)-ATPase after an ATP concentration jump.

Authors:  M Stengelin; K Fendler; E Bamberg
Journal:  J Membr Biol       Date:  1993-03       Impact factor: 1.843

5.  Selectivity of externally facing ion-binding sites in the Na/K pump to alkali metals and organic cations.

Authors:  Ian M Ratheal; Gail K Virgin; Haibo Yu; Benoît Roux; Craig Gatto; Pablo Artigas
Journal:  Proc Natl Acad Sci U S A       Date:  2010-10-11       Impact factor: 11.205

6.  A conformation-specific interhelical salt bridge in the K+ binding site of gastric H,K-ATPase.

Authors:  Jan B Koenderink; Herman G P Swarts; Peter H G M Willems; Elmar Krieger; Jan Joep H H M De Pont
Journal:  J Biol Chem       Date:  2004-02-03       Impact factor: 5.157

7.  Arginine oscillation explains Na+ independence in the substrate/product antiporter CaiT.

Authors:  Sissy Kalayil; Sabrina Schulze; Werner Kühlbrandt
Journal:  Proc Natl Acad Sci U S A       Date:  2013-10-07       Impact factor: 11.205

8.  Mechanism of chloride interaction with neurotransmitter:sodium symporters.

Authors:  Elia Zomot; Annie Bendahan; Matthias Quick; Yongfang Zhao; Jonathan A Javitch; Baruch I Kanner
Journal:  Nature       Date:  2007-08-19       Impact factor: 49.962

9.  The permeability of the sodium channel to organic cations in myelinated nerve.

Authors:  B Hille
Journal:  J Gen Physiol       Date:  1971-12       Impact factor: 4.086

10.  Inhibition of K+ transport through Na+, K+-ATPase by capsazepine: role of membrane span 10 of the α-subunit in the modulation of ion gating.

Authors:  Yasser A Mahmmoud; Michael Shattock; Flemming Cornelius; Davor Pavlovic
Journal:  PLoS One       Date:  2014-05-09       Impact factor: 3.240

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  9 in total

1.  External Ion Access in the Na/K Pump: Kinetics of Na+, K+, and Quaternary Amine Interaction.

Authors:  Kevin S Stanley; Victoria C Young; Craig Gatto; Pablo Artigas
Journal:  Biophys J       Date:  2018-07-17       Impact factor: 4.033

2.  Displacement of the Na+/K+ pump's transmembrane domains demonstrates conserved conformational changes in P-type 2 ATPases.

Authors:  Victoria C Young; Pablo Artigas
Journal:  Proc Natl Acad Sci U S A       Date:  2021-02-23       Impact factor: 11.205

3.  Role of a conserved ion-binding site tyrosine in ion selectivity of the Na+/K+ pump.

Authors:  Kerri Spontarelli; Daniel T Infield; Hang N Nielsen; Rikke Holm; Victoria C Young; Jason D Galpin; Christopher A Ahern; Bente Vilsen; Pablo Artigas
Journal:  J Gen Physiol       Date:  2022-06-03       Impact factor: 4.000

4.  On the effect of hyperaldosteronism-inducing mutations in Na/K pumps.

Authors:  Dylan J Meyer; Craig Gatto; Pablo Artigas
Journal:  J Gen Physiol       Date:  2017-10-13       Impact factor: 4.086

5.  A single K+-binding site in the crystal structure of the gastric proton pump.

Authors:  Kenta Yamamoto; Vikas Dubey; Katsumasa Irie; Hanayo Nakanishi; Himanshu Khandelia; Yoshinori Fujiyoshi; Kazuhiro Abe
Journal:  Elife       Date:  2019-08-22       Impact factor: 8.140

Review 6.  Transient Electrical Currents Mediated by the Na+/K+-ATPase: A Tour from Basic Biophysics to Human Diseases.

Authors:  Cristina Moreno; Sho Yano; Francisco Bezanilla; Ramon Latorre; Miguel Holmgren
Journal:  Biophys J       Date:  2020-06-12       Impact factor: 4.033

7.  Structure and function of H+/K+ pump mutants reveal Na+/K+ pump mechanisms.

Authors:  Victoria C Young; Hanayo Nakanishi; Dylan J Meyer; Tomohiro Nishizawa; Atsunori Oshima; Pablo Artigas; Kazuhiro Abe
Journal:  Nat Commun       Date:  2022-09-09       Impact factor: 17.694

8.  K+ binding and proton redistribution in the E2P state of the H+, K+-ATPase.

Authors:  Vikas Dubey; Minwoo Han; Wojciech Kopec; Ilia A Solov'yov; Kazuhiro Abe; Himanshu Khandelia
Journal:  Sci Rep       Date:  2018-08-24       Impact factor: 4.379

9.  Distinct effects of Q925 mutation on intracellular and extracellular Na+ and K+ binding to the Na+, K+-ATPase.

Authors:  Hang N Nielsen; Kerri Spontarelli; Rikke Holm; Jens Peter Andersen; Anja P Einholm; Pablo Artigas; Bente Vilsen
Journal:  Sci Rep       Date:  2019-09-16       Impact factor: 4.379

  9 in total

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