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. 1987 Dec 20;6(13):3917–3921. doi: 10.1002/j.1460-2075.1987.tb02732.x

Differential expression of nicotinic acetylcholine receptor genes in innervated and denervated chicken muscle.

S J Moss 1, D M Beeson 1, J F Jackson 1, M G Darlison 1, E A Barnard 1
PMCID: PMC553869  PMID: 3443094

Abstract

We have studied the mRNAs encoding all four subunits of the acetylcholine receptor in 13-day embryonic, innervated and denervated chicken pectoral muscle. In all three states the transcript sizes of the alpha, beta-, gamma- and delta-subunit mRNAs were approximately 3.2, 2.8, 1.8 and 1.9 kb respectively. Denervation was found to result in a large increase in the steady-state levels of each mRNA compared with those in innervated muscle. This increase was 8- to 9-fold for the beta and delta subunits and approximately 12-fold for the alpha subunit. The evidence obtained shows a coordinate regulation of the acetylcholine receptor genes in response to denervation. Interestingly, no gamma-subunit transcript was detected in innervated muscle, while significant levels were detected in embryonic and denervated tissue. This evidence suggests that there exists in a non-mammalian muscle acetylcholine receptor an additional subunit, analogous to the bovine epsilon subunit, and shows that the extra-junctional receptor of adult denervated muscle is produced by the same set of mRNAs which produce the major form of the receptor in embryonic muscle.

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Selected References

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  1. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Buonanno A., Merlie J. P. Transcriptional regulation of nicotinic acetylcholine receptor genes during muscle development. J Biol Chem. 1986 Sep 5;261(25):11452–11455. [PubMed] [Google Scholar]
  3. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  4. Devillers-Thiery A., Giraudat J., Bentaboulet M., Changeux J. P. Complete mRNA coding sequence of the acetylcholine binding alpha-subunit of Torpedo marmorata acetylcholine receptor: a model for the transmembrane organization of the polypeptide chain. Proc Natl Acad Sci U S A. 1983 Apr;80(7):2067–2071. doi: 10.1073/pnas.80.7.2067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dolly J. O., Barnard E. A. Nicotinic acetylcholine receptors: an overview. Biochem Pharmacol. 1984 Mar 15;33(6):841–858. doi: 10.1016/0006-2952(84)90437-4. [DOI] [PubMed] [Google Scholar]
  6. Evans S., Goldman D., Heinemann S., Patrick J. Muscle acetylcholine receptor biosynthesis. Regulation by transcript availability. J Biol Chem. 1987 Apr 5;262(10):4911–4916. [PMC free article] [PubMed] [Google Scholar]
  7. Fambrough D. M. Control of acetylcholine receptors in skeletal muscle. Physiol Rev. 1979 Jan;59(1):165–227. doi: 10.1152/physrev.1979.59.1.165. [DOI] [PubMed] [Google Scholar]
  8. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  9. Fischbach G. D., Schuetze S. M. A post-natal decrease in acetylcholine channel open time at rat end-plates. J Physiol. 1980 Jun;303:125–137. doi: 10.1113/jphysiol.1980.sp013275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Goldman D., Boulter J., Heinemann S., Patrick J. Muscle denervation increases the levels of two mRNAs coding for the acetylcholine receptor alpha-subunit. J Neurosci. 1985 Sep;5(9):2553–2558. doi: 10.1523/JNEUROSCI.05-09-02553.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Holly R. G., Barnett J. G., Ashmore C. R., Taylor R. G., Molé P. A. Stretch-induced growth in chicken wing muscles: a new model of stretch hypertrophy. Am J Physiol. 1980 Jan;238(1):C62–C71. doi: 10.1152/ajpcell.1980.238.1.C62. [DOI] [PubMed] [Google Scholar]
  12. Klarsfeld A., Changeux J. P. Activity regulates the levels of acetylcholine receptor alpha-subunit mRNA in cultured chicken myotubes. Proc Natl Acad Sci U S A. 1985 Jul;82(13):4558–4562. doi: 10.1073/pnas.82.13.4558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kubo T., Noda M., Takai T., Tanabe T., Kayano T., Shimizu S., Tanaka K., Takahashi H., Hirose T., Inayama S. Primary structure of delta subunit precursor of calf muscle acetylcholine receptor deduced from cDNA sequence. Eur J Biochem. 1985 May 15;149(1):5–13. doi: 10.1111/j.1432-1033.1985.tb08885.x. [DOI] [PubMed] [Google Scholar]
  14. McMaster G. K., Carmichael G. G. Analysis of single- and double-stranded nucleic acids on polyacrylamide and agarose gels by using glyoxal and acridine orange. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4835–4838. doi: 10.1073/pnas.74.11.4835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Merlie J. P., Isenberg K. E., Russell S. D., Sanes J. R. Denervation supersensitivity in skeletal muscle: analysis with a cloned cDNA probe. J Cell Biol. 1984 Jul;99(1 Pt 1):332–335. doi: 10.1083/jcb.99.1.332. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Mishina M., Takai T., Imoto K., Noda M., Takahashi T., Numa S., Methfessel C., Sakmann B. Molecular distinction between fetal and adult forms of muscle acetylcholine receptor. Nature. 1986 May 22;321(6068):406–411. doi: 10.1038/321406a0. [DOI] [PubMed] [Google Scholar]
  17. Nef P., Mauron A., Stalder R., Alliod C., Ballivet M. Structure linkage, and sequence of the two genes encoding the delta and gamma subunits of the nicotinic acetylcholine receptor. Proc Natl Acad Sci U S A. 1984 Dec;81(24):7975–7979. doi: 10.1073/pnas.81.24.7975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Noda M., Furutani Y., Takahashi H., Toyosato M., Tanabe T., Shimizu S., Kikyotani S., Kayano T., Hirose T., Inayama S. Cloning and sequence analysis of calf cDNA and human genomic DNA encoding alpha-subunit precursor of muscle acetylcholine receptor. 1983 Oct 27-Nov 2Nature. 305(5937):818–823. doi: 10.1038/305818a0. [DOI] [PubMed] [Google Scholar]
  19. Noda M., Takahashi H., Tanabe T., Toyosato M., Furutani Y., Hirose T., Asai M., Inayama S., Miyata T., Numa S. Primary structure of alpha-subunit precursor of Torpedo californica acetylcholine receptor deduced from cDNA sequence. Nature. 1982 Oct 28;299(5886):793–797. doi: 10.1038/299793a0. [DOI] [PubMed] [Google Scholar]
  20. Noda M., Takahashi H., Tanabe T., Toyosato M., Kikyotani S., Furutani Y., Hirose T., Takashima H., Inayama S., Miyata T. Structural homology of Torpedo californica acetylcholine receptor subunits. Nature. 1983 Apr 7;302(5908):528–532. doi: 10.1038/302528a0. [DOI] [PubMed] [Google Scholar]
  21. Noda M., Takahashi H., Tanabe T., Toyosato M., Kikyotani S., Hirose T., Asai M., Takashima H., Inayama S., Miyata T. Primary structures of beta- and delta-subunit precursors of Torpedo californica acetylcholine receptor deduced from cDNA sequences. Nature. 1983 Jan 20;301(5897):251–255. doi: 10.1038/301251a0. [DOI] [PubMed] [Google Scholar]
  22. Popot J. L., Changeux J. P. Nicotinic receptor of acetylcholine: structure of an oligomeric integral membrane protein. Physiol Rev. 1984 Oct;64(4):1162–1239. doi: 10.1152/physrev.1984.64.4.1162. [DOI] [PubMed] [Google Scholar]
  23. Sakmann B., Brenner H. R. Change in synaptic channel gating during neuromuscular development. Nature. 1978 Nov 23;276(5686):401–402. doi: 10.1038/276401a0. [DOI] [PubMed] [Google Scholar]
  24. Schuetze S. M. The acetylcholine channel open time in chick muscle is not decreased following innervation. J Physiol. 1980 Jun;303:111–124. doi: 10.1113/jphysiol.1980.sp013274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Stroud R. M., Finer-Moore J. Acetylcholine receptor structure, function, and evolution. Annu Rev Cell Biol. 1985;1:317–351. doi: 10.1146/annurev.cb.01.110185.001533. [DOI] [PubMed] [Google Scholar]
  26. Sumikawa K., Houghton M., Smith J. C., Bell L., Richards B. M., Barnard E. A. The molecular cloning and characterisation of cDNA coding for the alpha subunit of the acetylcholine receptor. Nucleic Acids Res. 1982 Oct 11;10(19):5809–5822. doi: 10.1093/nar/10.19.5809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sumikawa K., Mehraban F., Dolly J. O., Barnard E. A. Similarity of acetylcholine receptors of denervated, innervated and embryonic chicken muscles. 1. Molecular species and their purification. Eur J Biochem. 1982 Sep 1;126(3):465–472. doi: 10.1111/j.1432-1033.1982.tb06803.x. [DOI] [PubMed] [Google Scholar]
  28. Takai T., Noda M., Furutani Y., Takahashi H., Notake M., Shimizu S., Kayano T., Tanabe T., Tanaka K., Hirose T. Primary structure of gamma subunit precursor of calf-muscle acetylcholine receptor deduced from the cDNA sequence. Eur J Biochem. 1984 Aug 15;143(1):109–115. doi: 10.1111/j.1432-1033.1984.tb08348.x. [DOI] [PubMed] [Google Scholar]
  29. Takai T., Noda M., Mishina M., Shimizu S., Furutani Y., Kayano T., Ikeda T., Kubo T., Takahashi H., Takahashi T. Cloning, sequencing and expression of cDNA for a novel subunit of acetylcholine receptor from calf muscle. 1985 Jun 27-Jul 3Nature. 315(6022):761–764. doi: 10.1038/315761a0. [DOI] [PubMed] [Google Scholar]
  30. Tanabe T., Noda M., Furutani Y., Takai T., Takahashi H., Tanaka K., Hirose T., Inayama S., Numa S. Primary structure of beta subunit precursor of calf muscle acetylcholine receptor deduced from cDNA sequence. Eur J Biochem. 1984 Oct 1;144(1):11–17. doi: 10.1111/j.1432-1033.1984.tb08424.x. [DOI] [PubMed] [Google Scholar]

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