Home LiteratureArticle Details
PMID: 11487611 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

On the contribution of the first transmembrane domain to whole-cell current through an ATP-gated ionotropic P2X receptor.

Haines WR, Voigt MM, Migita K, Torres GE, Egan TM

Abstract

Scanning cysteine mutagenesis was used to identify potential pore-forming residues in and around the first transmembrane domains of ionotropic P2X(2) receptor subunits. Twenty-eight unique cysteine-substituted mutants (R28C-Y55C) were individually expressed in HEK293 cells by lipofection. Twenty-three of these were functional as assayed by application of ATP to transfected voltage-clamped cells. Individual mutants varied in their sensitivity to ATP; otherwise, currents through functional mutant receptors resembled those of the homomeric wild-type (WT) receptor. In five (H33C, R34C, I50C, K53C, and S54C) of 23 functional mutants, coapplication of 30 microm ATP and 500 nm Ag(+) irreversibly inhibited inward current evoked by subsequent applications of ATP alone. These inhibitions did not result in a lateral shift in the agonist concentration-response curve and are unlikely to involve a modification of the agonist binding site. Two (K53C and S54C) of the five residues modified by Ag(+) applied in the presence of ATP when the channels were gating were also modified by 1 mm (2-aminoethyl)methanethiosulfonate applied in the absence of ATP when the channels were closed. These data suggest that domains near either end of the first transmembrane domain influence ion conduction through the pore of the P2X(2) receptor.

MeSH Terms
Adenosine Triphosphate/metabolism,pharmacology Amino Acid Substitution Cell Line Cysteine/chemistry,genetics Dose-Response Relationship, Drug Ethyl Methanesulfonate/analogs & derivatives,chemistry Humans Ion Channel Gating/physiology Kidney/cytology,metabolism Mutagenesis, Site-Directed Patch-Clamp Techniques Protein Structure, Tertiary/physiology Receptors, Purinergic P2/genetics,metabolism Receptors, Purinergic P2X2 Silver/pharmacology Structure-Activity Relationship Transfection
Chemicals
P2RX2 protein, human Receptors, Purinergic P2 Receptors, Purinergic P2X2 methanethiosulfonate ethylammonium Silver Adenosine Triphosphate Ethyl Methanesulfonate Cysteine
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Haines W R
Department of Pharmacological and Physiological Science, St. Louis University School of Medicine, St. Louis, Missouri 63104, USA.
Voigt M M
Migita K
Torres G E
Egan T M
References (28)
28 references, click to expand
  1. Identification of amino acid residues contributing to the ATP-binding site of a purinergic P2X receptor.
    J Biol Chem. 2000 Nov 3;275(44):34190-6 PMID: 10940304
  2. International union of pharmacology. XXIV. Current status of the nomenclature and properties of P2X receptors and their subunits.
    Pharmacol Rev. 2001 Mar;53(1):107-18 PMID: 11171941
  3. Mutation in the M1 domain of the acetylcholine receptor alpha subunit decreases the rate of agonist dissociation.
    J Gen Physiol. 1997 Jun;109(6):757-66 PMID: 9222901
  4. On the use of thiol-modifying agents to determine channel topology.
    Neuropharmacology. 1996;35(7):797-804 PMID: 8938712
  5. Different sensitivities to pH of ATP-induced currents at four cloned P2X receptors.
    J Neurophysiol. 1997 Oct;78(4):1837-40 PMID: 9325352
  6. Exposure of residues in the cyclic nucleotide-gated channel pore: P region structure and function in gating.
    Neuron. 1996 Jan;16(1):141-9 PMID: 8562078
  7. Single channel properties of P2X2 purinoceptors.
    J Gen Physiol. 1999 May;113(5):695-720 PMID: 10228183
  8. Silver as a probe of pore-forming residues in a potassium channel.
    Science. 1995 Apr 14;268(5208):304-7 PMID: 7716526
  9. Topological analysis of the ATP-gated ionotropic [correction of ionotrophic] P2X2 receptor subunit.
    FEBS Lett. 1998 Mar 20;425(1):19-23 PMID: 9540999
  10. Hetero-oligomeric assembly of P2X receptor subunits. Specificities exist with regard to possible partners.
    J Biol Chem. 1999 Mar 5;274(10):6653-9 PMID: 10037762
  11. Membrane topology of an ATP-gated ion channel (P2X receptor).
    J Biol Chem. 1998 Jun 12;273(24):15177-82 PMID: 9614131
  12. Domains of P2X receptors involved in desensitization.
    Proc Natl Acad Sci U S A. 1996 Dec 24;93(26):15485-90 PMID: 8986838
  13. Receptors for purines and pyrimidines.
    Pharmacol Rev. 1998 Sep;50(3):413-92 PMID: 9755289
  14. Proton potentiation of ATP-gated ion channel responses to ATP and Zn2+ in rat nodose ganglion neurons.
    J Neurophysiol. 1996 Nov;76(5):3048-58 PMID: 8930254
  15. Identification of amino acid residues contributing to the pore of a P2X receptor.
    EMBO J. 1997 Jun 16;16(12):3446-54 PMID: 9218787
  16. P2X1 and P2X3 receptors form stable trimers: a novel structural motif of ligand-gated ion channels.
    EMBO J. 1998 Jun 1;17(11):3016-28 PMID: 9606184
  17. Cu2+ potently enhances ATP-activated current in rat nodose ganglion neurons.
    Neurosci Lett. 1996 Nov 15;219(1):45-8 PMID: 8961300
  18. A domain contributing to the ion channel of ATP-gated P2X2 receptors identified by the substituted cysteine accessibility method.
    J Neurosci. 1998 Apr 1;18(7):2350-9 PMID: 9502796
  19. Acetylcholine receptor channel structure probed in cysteine-substitution mutants.
    Science. 1992 Oct 9;258(5080):307-10 PMID: 1384130
  20. Full sensitivity of P2X2 purinoceptor to ATP revealed by changing extracellular pH.
    Br J Pharmacol. 1996 Apr;117(7):1371-3 PMID: 8730726
  21. The nicotinic alpha4 receptor subunit contributes to the lining of the ion channel pore when expressed with the 5-HT3 receptor subunit.
    J Biol Chem. 1999 Feb 12;274(7):3934-6 PMID: 9933581
  22. Alteration of the pH-dependent ion selectivity of the colicin E1 channel by site-directed mutagenesis.
    J Biol Chem. 1990 Apr 25;265(12):6984-91 PMID: 1691183
  23. Substituted-cysteine accessibility method.
    Methods Enzymol. 1998;293:123-45 PMID: 9711606
  24. New structural motif for ligand-gated ion channels defined by an ionotropic ATP receptor.
    Nature. 1994 Oct 6;371(6497):519-23 PMID: 7523952
  25. Molecular assembly of the extracellular domain of P2X2, an ATP-gated ion channel.
    Biochem Biophys Res Commun. 1997 Nov 26;240(3):618-22 PMID: 9398614
  26. Zn2+ potentiates excitatory action of ATP on mammalian neurons.
    Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):8264-7 PMID: 7690146
  27. Neurotransmitter action: opening of ligand-gated ion channels.
    Cell. 1993 Jan;72 Suppl:31-41 PMID: 7679054
  28. Signaling by extracellular nucleotides.
    Annu Rev Cell Dev Biol. 1996;12:519-41 PMID: 8970736
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2001-08-15
Pages
5885-92
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6763184
Subset
IM
Grants
NHLBI NIH HHS · HL56236 · United States
NINDS NIH HHS · NS35534 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com