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PMID: 11967372 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Novel alpha7-like nicotinic acetylcholine receptor subunits in the nematode Caenorhabditis elegans.

Protein science : a publication of the Protein Society ·Vol. 11 ·No. 5 ·2002-05-00 ·Pages 1162-71

Mongan NP, Jones AK, Smith GR, Sansom MS, Sattelle DB

Abstract

We have used reverse-transcription-polymerase chain reaction (RT-PCR) and DNA sequencing techniques to confirm the transcription of seven (six alpha and one non-alpha) novel candidate nicotinic acetylcholine receptor (nAChR) subunit-encoding genes identified in the genome sequence of the nematode Caenorhabditis elegans. Compared to vertebrate nAChR subunits, they most closely resemble the homomer-forming, neuronal alpha7 subunit. Comparison of the predicted amino acid sequences of the new nAChR subunits with those described previously in C. elegans reveals five subunits (four alpha and one non-alpha) which resemble the DEG-3-like group of subunits. To date, this highly divergent nAChR subunit group is unique to C. elegans. ACR-22 is the first non-alpha member of the DEG-3-like group of subunits to be identified. Two new members of the related ACR-16-like nAChR group of subunits have also been shown to be transcribed, making the ACR-16-like subunit group the largest in C. elegans. Residues in the alpha subunit second transmembrane region (M2) which contribute to the channel lining show variations with implications for channel function. For example, in ACR-22, the highly conserved 0' lysine of M2 is replaced by histidine. Restrained molecular dynamics simulations have been used to generate molecular models of homo-pentameric M2 helix bundles for the novel subunits, enabling identification and display of pore-lining and protein interface residues. The number and diversity of genes encoding C. elegans nAChR subunits with similarities to the homomer-forming vertebrate alpha7 subunits and the identification of related non-alpha subunits, only found in C. elegans to date, suggest that at least some of these subunits may contribute to heteromers in vivo.

MeSH Terms
Amino Acid Sequence Animals Caenorhabditis elegans/genetics,metabolism Models, Molecular Molecular Sequence Data Phylogeny Receptors, Nicotinic/genetics,metabolism Reverse Transcriptase Polymerase Chain Reaction Sequence Alignment alpha7 Nicotinic Acetylcholine Receptor
Chemicals
Chrna7 protein, human Receptors, Nicotinic alpha7 Nicotinic Acetylcholine Receptor
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Mongan Nigel P
MRC Functional Genetics Unit, Department of Human Anatomy and Genetics, University of Oxford, South Parks Road, Oxford OX1 3QX, UK.
Jones Andrew K
Smith Graham R
Sansom Mark S P
Sattelle David B
References (54)
54 references, click to expand
  1. Primary structure of alpha-subunit precursor of Torpedo californica acetylcholine receptor deduced from cDNA sequence.
    Nature. 1982 Oct 28;299(5886):793-7 PMID: 6182472
  2. The genetics of levamisole resistance in the nematode Caenorhabditis elegans.
    Genetics. 1980 Aug;95(4):905-28 PMID: 7203008
  3. Brain alpha-bungarotoxin binding protein cDNAs and MAbs reveal subtypes of this branch of the ligand-gated ion channel gene superfamily.
    Neuron. 1990 Jul;5(1):35-48 PMID: 2369519
  4. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  5. Sequence and functional expression of a single alpha subunit of an insect nicotinic acetylcholine receptor.
    EMBO J. 1990 Dec;9(13):4391-8 PMID: 1702381
  6. A neuronal nicotinic acetylcholine receptor subunit (alpha 7) is developmentally regulated and forms a homo-oligomeric channel blocked by alpha-BTX.
    Neuron. 1990 Dec;5(6):847-56 PMID: 1702646
  7. Location of a threonine residue in the alpha-subunit M2 transmembrane segment that determines the ion flow through the acetylcholine receptor channel.
    Proc Biol Sci. 1991 Jan 22;243(1306):69-74 PMID: 1708143
  8. Threonine in the selectivity filter of the acetylcholine receptor channel.
    Biophys J. 1992 Apr;62(1):196-205; discussion 205-8 PMID: 1376167
  9. Three subtypes of alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors are expressed in chick retina.
    J Neurosci. 1993 Feb;13(2):442-54 PMID: 8426223
  10. Molecular cloning, functional properties, and distribution of rat brain alpha 7: a nicotinic cation channel highly permeable to calcium.
    J Neurosci. 1993 Feb;13(2):596-604 PMID: 7678857
  11. Homomeric and native alpha 7 acetylcholine receptors exhibit remarkably similar but non-identical pharmacological properties, suggesting that the native receptor is a heteromeric protein complex.
    FEBS Lett. 1993 Jul 26;327(2):241-6 PMID: 8335115
  12. Homomers of alpha 8 and alpha 7 subunits of nicotinic receptors exhibit similar channel but contrasting binding site properties.
    Mol Pharmacol. 1994 Feb;45(2):212-20 PMID: 7509438
  13. Alpha 9: an acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells.
    Cell. 1994 Nov 18;79(4):705-15 PMID: 7954834
  14. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  15. Acetylcholine receptor channel imaged in the open state.
    Nature. 1995 Jan 5;373(6509):37-43 PMID: 7800037
  16. Molecular evolution of the nicotinic acetylcholine receptor: an example of multigene family in excitable cells.
    J Mol Evol. 1995 Feb;40(2):155-72 PMID: 7699721
  17. A mutated acetylcholine receptor subunit causes neuronal degeneration in C. elegans.
    Neuron. 1995 Apr;14(4):871-7 PMID: 7718248
  18. Evolutionary history of the ligand-gated ion-channel superfamily of receptors.
    Trends Neurosci. 1995 Mar;18(3):121-7 PMID: 7754520
  19. Modelling membrane proteins using structural restraints.
    Nat Struct Biol. 1995 Aug;2(8):624-31 PMID: 7552722
  20. Molecular cloning and functional co-expression of a Caenorhabditis elegans nicotinic acetylcholine receptor subunit (acr-2).
    Receptors Channels. 1995;3(2):107-15 PMID: 8581398
  21. Nicotinic acetylcholine receptors in the nematode Caenorhabditis elegans.
    J Mol Biol. 1996 May 3;258(2):261-9 PMID: 8627624
  22. The emerging three-dimensional structure of a receptor. The nicotinic acetylcholine receptor.
    Eur J Biochem. 1996 Aug 1;239(3):539-57 PMID: 8774696
  23. The pore domain of the nicotinic acetylcholine receptor: molecular modeling, pore dimensions, and electrostatics.
    Biophys J. 1996 Oct;71(4):1659-71 PMID: 8889144
  24. Evolutionary relationship of the ligand-gated ion channels and the avermectin-sensitive, glutamate-gated chloride channels.
    J Mol Evol. 1997 May;44(5):501-8 PMID: 9115174
  25. Expression of the alpha 7 subunit of the nicotinic acetylcholine receptor in normal and myasthenic human thymuses.
    Cell Mol Biol (Noisy-le-grand). 1997 May;43(3):433-42 PMID: 9193799
  26. HOLE: a program for the analysis of the pore dimensions of ion channel structural models.
    J Mol Graph. 1996 Dec;14(6):354-60, 376 PMID: 9195488
  27. Caenorhabditis elegans levamisole resistance genes lev-1, unc-29, and unc-38 encode functional nicotinic acetylcholine receptor subunits.
    J Neurosci. 1997 Aug 1;17(15):5843-57 PMID: 9221782
  28. Molecular biology of insect neuronal GABA receptors.
    Trends Neurosci. 1997 Dec;20(12):578-83 PMID: 9416671
  29. Assigning functions to residues in the acetylcholine receptor channel region (review).
    Mol Membr Biol. 1997 Oct-Dec;14(4):167-77 PMID: 9491368
  30. Evolution of nicotinic acetylcholine receptor subunits.
    Mol Biol Evol. 1998 May;15(5):518-27 PMID: 9580980
  31. Functional contribution of the alpha7 subunit to multiple subtypes of nicotinic receptors in embryonic chick sympathetic neurones.
    J Physiol. 1998 Jun 15;509 ( Pt 3):651-65 PMID: 9596789
  32. ACR-3, a Caenorhabditis elegans nicotinic acetylcholine receptor subunit. Molecular cloning and functional expression.
    Receptors Channels. 1997;5(3-4):149-58 PMID: 9606719
  33. Electrostatics and the ion selectivity of ligand-gated channels.
    Biophys J. 1998 Sep;75(3):1211-22 PMID: 9726923
  34. Identification of major phylogenetic branches of inhibitory ligand-gated channel receptors.
    J Mol Evol. 1998 Sep;47(3):323-33 PMID: 9732459
  35. Genome sequence of the nematode C. elegans: a platform for investigating biology.
    Science. 1998 Dec 11;282(5396):2012-8 PMID: 9851916
  36. Mammalian nicotinic receptors with alpha7 subunits that slowly desensitize and rapidly recover from alpha-bungarotoxin blockade.
    J Neurosci. 1998 Dec 15;18(24):10335-44 PMID: 9852571
  37. Allosteric receptors after 30 years.
    Neuron. 1998 Nov;21(5):959-80 PMID: 9856454
  38. Two functionally dependent acetylcholine subunits are encoded in a single Caenorhabditis elegans operon.
    Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15492-5 PMID: 9860996
  39. The alpha9 nicotinic acetylcholine receptor shares pharmacological properties with type A gamma-aminobutyric acid, glycine, and type 3 serotonin receptors.
    Mol Pharmacol. 1999 Feb;55(2):248-54 PMID: 9927615
  40. How the worm was won. The C. elegans genome sequencing project.
    Trends Genet. 1999 Feb;15(2):51-8 PMID: 10098407
  41. An extensive and diverse gene family of nicotinic acetylcholine receptor alpha subunits in Caenorhabditis elegans.
    Receptors Channels. 1998;6(3):213-28 PMID: 10100329
  42. Nicotinic acetylcholine receptors assembled from the alpha7 and beta3 subunits.
    J Biol Chem. 1999 Jun 25;274(26):18335-40 PMID: 10373437
  43. Neuronal alpha-bungarotoxin receptors are alpha7 subunit homomers.
    J Neurosci. 2000 Jan 1;20(1):133-9 PMID: 10627589
  44. The intrinsic electrostatic potential and the intermediate ring of charge in the acetylcholine receptor channel.
    J Gen Physiol. 2000 Feb;115(2):93-106 PMID: 10653890
  45. Functional effects of periodic tryptophan substitutions in the alpha M4 transmembrane domain of the Torpedo californica nicotinic acetylcholine receptor.
    Biochemistry. 2000 Apr 25;39(16):4666-73 PMID: 10769122
  46. Nicotinic receptor fourth transmembrane domain: hydrogen bonding by conserved threonine contributes to channel gating kinetics.
    J Gen Physiol. 2000 May;115(5):663-72 PMID: 10779322
  47. Ion channels and synaptic organization: analysis of the Drosophila genome.
    Neuron. 2000 Apr;26(1):35-43 PMID: 10798390
  48. Mice homozygous for the L250T mutation in the alpha7 nicotinic acetylcholine receptor show increased neuronal apoptosis and die within 1 day of birth.
    J Neurochem. 2000 May;74(5):2154-66 PMID: 10800961
  49. Nicotinic receptors at the amino acid level.
    Annu Rev Pharmacol Toxicol. 2000;40:431-58 PMID: 10836143
  50. Anthelmintic actions on homomer-forming nicotinic acetylcholine receptor subunits: chicken alpha7 and ACR-16 from the nematode Caenorhabditis elegans.
    Neuroscience. 2000;101(3):785-91 PMID: 11113327
  51. Characterization of the deg-3/des-2 receptor: a nicotinic acetylcholine receptor that mutates to cause neuronal degeneration.
    Mol Cell Neurosci. 2001 Mar;17(3):589-99 PMID: 11273652
  52. Human bronchial epithelial and endothelial cells express alpha7 nicotinic acetylcholine receptors.
    Mol Pharmacol. 2001 Dec;60(6):1201-9 PMID: 11723227
  53. The C. elegans even-skipped homologue, vab-7, specifies DB motoneurone identity and axon trajectory.
    Development. 2002 Feb;129(4):853-62 PMID: 11861469
  54. Genetic manipulation of ion channels: a new approach to structure and mechanism.
    Neuron. 1989 Mar;2(3):1195-205 PMID: 2483110
Article Info
Journal
Protein science : a publication of the Protein Society
Abbr.
Protein Sci
ISSN
0961-8368
Published
2002-05-00
Pages
1162-71
Language
English
Region
United States
NLM ID
9211750
PMCID
PMC2373549
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · BEP17032 · United Kingdom
Medical Research Council · MC_U137761447 · United Kingdom
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