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PMID: 7962068 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Neural regulation of acetylcholinesterase mRNAs at mammalian neuromuscular synapses.

The Journal of cell biology ·Vol. 127 ·No. 4 ·1994-11-00 ·Pages 1061-9

Michel RN, Vu CQ, Tetzlaff W, Jasmin BJ

Abstract

We examined the role of innervation on acetylcholinesterase (AChE) gene expression within mammalian skeletal muscle fibers. First, we showed the selective accumulation of AChE mRNAs within the junctional vs extrajunctional sarcoplasm of adult muscle fibers using a quantitative reverse transcription PCR assay and demonstrated by in situ hybridization experiments that AChE transcripts are concentrated immediately beneath the postsynaptic membrane of the neuromuscular junction. Next, we determined the influence of nerve-evoked activity vs putative trophic factors on the synaptic accumulation of AChE mRNA levels in muscle fibers paralyzed by either surgical denervation or selective blockage of nerve action potentials with chronic superfusion of tetrodotoxin. Our results indicated that muscle paralysis leads to a marked decrease in AChE transcripts from the postsynaptic sarcoplasm, yet the extent of this decrease is less pronounced after tetrodotoxin inactivation than after denervation. These results suggest that although nerve-evoked activity per se appears a key regulator of AChE mRNA levels, the integrity of the synaptic structure or the release of putative trophic factors contribute to maintaining the synaptic accumulation of AChE transcripts at adult neuromuscular synapses. Furthermore, the pronounced downregulation of AChE transcripts in paralyzed muscles stands in sharp contrast to the well-documented increase in nicotinic acetylcholine receptor mRNAs under these conditions, and indicates that expression of the genes encoding these two synaptic proteins are subjected to different regulatory mechanisms in adult muscle fibers in vivo.

MeSH Terms
Acetylcholinesterase/biosynthesis Animals Base Sequence Consensus Sequence DNA Primers Female Gene Expression Regulation, Enzymologic In Situ Hybridization Kinetics Molecular Sequence Data Muscle Fibers, Skeletal/enzymology Neuromuscular Junction/enzymology Organ Specificity Polymerase Chain Reaction RNA, Messenger/biosynthesis,isolation & purification,metabolism Rats Rats, Sprague-Dawley Synapses/enzymology Transcription, Genetic
Chemicals
DNA Primers RNA, Messenger Acetylcholinesterase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Michel R N
Department of Physiology, Faculty of Medicine, University of Ottawa, Ontario, Canada.
Vu C Q
Tetzlaff W
Jasmin B J
References (64)
64 references, click to expand
  1. Tetrodotoxin and neuromuscular transmission.
    Proc R Soc Lond B Biol Sci. 1967 Jan 31;167(1006):8-22 PMID: 4382592
  2. Detection of the nicotinic acetylcholine receptor alpha-subunit mRNA by in situ hybridization at neuromuscular junctions of 15-day-old chick striated muscles.
    EMBO J. 1988 Mar;7(3):603-9 PMID: 3396533
  3. Multiple forms of acetylcholinesterase and their distribution in endplate and non-endplate regions of rat diaphragm muscle.
    J Neurobiol. 1973;4(4):343-61 PMID: 4724813
  4. Comparison of alpha-bungarotoxin binding to skeletal muscles after inactivity or denervation.
    Nature. 1976 Mar 25;260(5549):349-50 PMID: 56717
  5. Effect of muscle disuse on acetylcholine receptors.
    Nature. 1976 Mar 25;260(5549):352-3 PMID: 56718
  6. The motor end-plate specific form of acetylcholinesterase: appearance during embryogenesis and re-innervation of rat muscle.
    J Neurochem. 1976 Dec;27(6):1347-53 PMID: 1003208
  7. The effect of disuse on cholinergic enzymes.
    J Physiol. 1978 Jan;274:593-600 PMID: 625010
  8. Control of acetylcholine receptors in skeletal muscle.
    Physiol Rev. 1979 Jan;59(1):165-227 PMID: 375254
  9. Neural control of skeletal muscle cholinesterase: a study using organ-cultured rat muscle.
    J Physiol. 1979 Apr;289:501-15 PMID: 88516
  10. Allelic variants of acetylcholinesterase: genetic evidence that all acetylcholinesterase forms in avian nerves and muscles are encoded by a single gene.
    Proc Natl Acad Sci U S A. 1988 Oct;85(20):7805-9 PMID: 3174665
  11. Coexistence and gene expression of phenylethanolamine N-methyltransferase, tyrosine hydroxylase, and neuropeptide tyrosine in the rat and bovine adrenal gland: effects of reserpine.
    Proc Natl Acad Sci U S A. 1988 Nov;85(21):8306-10 PMID: 2903502
  12. Exercise selectively increases G4 AChe activity in fast-twitch muscle.
    J Appl Physiol (1985). 1988 Nov;65(5):2245-52 PMID: 3209567
  13. Developmental regulation of five subunit specific mRNAs encoding acetylcholine receptor subtypes in rat muscle.
    FEBS Lett. 1989 Jan 2;242(2):419-24 PMID: 2914620
  14. Localization of nicotinic acetylcholine receptor alpha-subunit transcripts during myogenesis and motor endplate development in the chick.
    J Cell Biol. 1989 Mar;108(3):1025-37 PMID: 2921278
  15. Skeletal muscle denervation activates acetylcholine receptor genes.
    J Cell Biol. 1989 Apr;108(4):1523-6 PMID: 2925794
  16. Silver cholinesterase immunocytochemistry: a new neuromuscular junction stain.
    Muscle Nerve. 1989 Jan;12(1):9-14 PMID: 2473397
  17. Golgi apparatus in chick skeletal muscle: changes in its distribution during end plate development and after denervation.
    Proc Natl Acad Sci U S A. 1989 Sep;86(18):7218-22 PMID: 2674951
  18. Spatial and temporal expression of acetylcholine receptor RNAs in innervated and denervated rat soleus muscle.
    Neuron. 1989 Aug;3(2):219-28 PMID: 2483113
  19. Single gene encodes glycophospholipid-anchored and asymmetric acetylcholinesterase forms: alternative coding exons contain inverted repeat sequences.
    Neuron. 1990 Feb;4(2):289-301 PMID: 2306366
  20. Nucleus-specific translation and assembly of acetylcholinesterase in multinucleated muscle cells.
    J Cell Biol. 1990 Mar;110(3):715-9 PMID: 2307705
  21. Imprinting of acetylcholine receptor messenger RNA accumulation in mammalian neuromuscular synapses.
    Nature. 1990 Apr 5;344(6266):544-7 PMID: 2320126
  22. Compartmentalization of cold-stable and acetylated microtubules in the subsynaptic domain of chick skeletal muscle fibre.
    Nature. 1990 Apr 12;344(6267):673-5 PMID: 2325774
  23. Regulation by exercise of the pool of G4 acetylcholinesterase characterizing fast muscles: opposite effect of running training in antagonist muscles.
    J Neurosci. 1990 May;10(5):1444-54 PMID: 2332790
  24. To what extent is hindlimb suspension a model of disuse?
    Muscle Nerve. 1990 Jul;13(7):646-53 PMID: 2388664
  25. Molecular cloning of mouse acetylcholinesterase: tissue distribution of alternatively spliced mRNA species.
    Neuron. 1990 Sep;5(3):317-27 PMID: 2400605
  26. Expression of dystrophin mRNA and the protein in the developing rat heart.
    Biochem Biophys Res Commun. 1990 Oct 30;172(2):824-9 PMID: 1700710
  27. The cholinesterases.
    J Biol Chem. 1991 Mar 5;266(7):4025-8 PMID: 1999397
  28. An acetylcholine receptor alpha-subunit promoter conferring preferential synaptic expression in muscle of transgenic mice.
    EMBO J. 1991 Mar;10(3):625-32 PMID: 1900467
  29. Neural factors regulate AChR subunit mRNAs at rat neuromuscular synapses.
    J Cell Biol. 1991 Jul;114(1):125-41 PMID: 1646821
  30. Muscle acetylcholinesterase adapts to compensatory overload by a general increase in its molecular forms.
    J Appl Physiol (1985). 1991 Jun;70(6):2485-9 PMID: 1885442
  31. Gene structure of mammalian acetylcholinesterase. Alternative exons dictate tissue-specific expression.
    J Biol Chem. 1991 Dec 5;266(34):23083-90 PMID: 1744105
  32. Selective expression of an acetylcholine receptor-lacZ transgene in synaptic nuclei of adult muscle fibers.
    Development. 1991 Dec;113(4):1181-91 PMID: 1811935
  33. Spatial restriction of AChR gene expression to subsynaptic nuclei.
    Development. 1992 Mar;114(3):545-53 PMID: 1618127
  34. Quantitative analysis of dystrophin in fast- and slow-twitch mammalian skeletal muscle.
    FEBS Lett. 1992 Jun 15;304(2-3):187-91 PMID: 1618321
  35. Cell surface acetylcholinesterase molecules on multinucleated myotubes are clustered over the nucleus of origin.
    J Cell Biol. 1992 Dec;119(6):1657-67 PMID: 1469054
  36. Cloning and expression of a rat acetylcholinesterase subunit: generation of multiple molecular forms and complementarity with a Torpedo collagenic subunit.
    J Neurochem. 1993 Jan;60(1):337-46 PMID: 8417155
  37. Expression of a cDNA encoding the glycolipid-anchored form of rat acetylcholinesterase.
    FEBS Lett. 1993 Jan 4;315(2):163-6 PMID: 8417973
  38. Synaptic structure and development: the neuromuscular junction.
    Cell. 1993 Jan;72 Suppl:99-121 PMID: 8428377
  39. An 83-nucleotide promoter of the acetylcholine receptor epsilon-subunit gene confers preferential synaptic expression in mouse muscle.
    Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):3043-7 PMID: 8464921
  40. Control of acetylcholinesterase gene expression during myogenesis.
    Neuron. 1993 Apr;10(4):679-87 PMID: 8386528
  41. Molecular and cellular biology of cholinesterases.
    Prog Neurobiol. 1993 Jul;41(1):31-91 PMID: 8321908
  42. Comparison between the effects of botulinum toxin-induced paralysis and denervation on molecular forms of acetylcholinesterase in muscles.
    J Neurochem. 1993 Aug;61(2):501-8 PMID: 8336138
  43. Compartmentalization of acetylcholinesterase mRNA and enzyme at the vertebrate neuromuscular junction.
    Neuron. 1993 Sep;11(3):467-77 PMID: 8398140
  44. Dystrophin-glycoprotein complex: its role in the molecular pathogenesis of muscular dystrophies.
    Muscle Nerve. 1994 Jan;17(1):2-15 PMID: 8264699
  45. Effects of tetrodotoxin-induced neural inactivation on single muscle fiber metabolic enzymes.
    Am J Physiol. 1994 Jul;267(1 Pt 1):C55-66 PMID: 8048492
  46. The structural and functional diversity of dystrophin.
    Nat Genet. 1993 Apr;3(4):283-91 PMID: 7981747
  47. A new and rapid colorimetric determination of acetylcholinesterase activity.
    Biochem Pharmacol. 1961 Jul;7:88-95 PMID: 13726518
  48. A "DIRECT-COLORING" THIOCHOLINE METHOD FOR CHOLINESTERASES.
    J Histochem Cytochem. 1964 Mar;12:219-21 PMID: 14187330
  49. Neurotrophic control of 16S acetylcholinesterase at the vertebrate neuromuscular junction.
    J Neurobiol. 1979 Sep;10(5):441-54 PMID: 490155
  50. Neurotrophic control of 16S acetylcholinesterase from mammalian skeletal muscle in organ culture.
    J Neurobiol. 1980 Nov;11(6):557-70 PMID: 7441241
  51. Effects of chronic nerve conduction block on formation of neuromuscular junctions and junctional AChE in the rat.
    Acta Physiol Scand. 1980 Jul;109(3):283-96 PMID: 7446172
  52. Acetylcholinesterase forms in fast and slow rabbit muscle.
    Nature. 1982 Apr 15;296(5858):661-4 PMID: 7070511
  53. The molecular forms of cholinesterase and acetylcholinesterase in vertebrates.
    Annu Rev Neurosci. 1982;5:57-106 PMID: 6176173
  54. Effect of denervation on the molecular forms of acetylcholinesterase in rat diaphragm.
    J Biol Chem. 1982 Nov 25;257(22):13638-44 PMID: 7142170
  55. Molecular forms of acetylcholinesterase in brain, nerve and muscle: nature, localization and dynamics.
    Prog Neurobiol. 1983;21(4):291-322 PMID: 6198691
  56. Denervation supersensitivity in skeletal muscle: analysis with a cloned cDNA probe.
    J Cell Biol. 1984 Jul;99(1 Pt 1):332-5 PMID: 6547444
  57. Stimulation of denervated rat soleus muscle with fast and slow activity patterns induces different expression of acetylcholinesterase molecular forms.
    J Neurosci. 1985 May;5(5):1180-7 PMID: 3998815
  58. Concentration of acetylcholine receptor mRNA in synaptic regions of adult muscle fibres.
    Nature. 1985 Sep 5-11;317(6032):66-8 PMID: 3839905
  59. Primary structure of Torpedo californica acetylcholinesterase deduced from its cDNA sequence.
    Nature. 1986 Jan 30-Feb 5;319(6052):407-9 PMID: 3753747
  60. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
    Anal Biochem. 1987 Apr;162(1):156-9 PMID: 2440339
  61. cDNA sequences of Torpedo marmorata acetylcholinesterase: primary structure of the precursor of a catalytic subunit; existence of multiple 5'-untranslated regions.
    EMBO J. 1987 Jul;6(7):1865-73 PMID: 2820709
  62. Coordinate control of synaptic protein expression at the neuromuscular junction.
    Biochimie. 1987 May;69(5):433-7 PMID: 2823911
  63. Localization of the pool of G4 acetylcholinesterase characterizing fast muscles and its alteration in murine muscular dystrophy.
    J Neurosci Res. 1988;19(1):62-78 PMID: 3343711
  64. Neurotrophic regulation of muscle cholinesterase: effects of botulinum toxin and denervation.
    J Physiol. 1972 Nov;226(3):619-27 PMID: 4344399
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1994-11-00
Pages
1061-9
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2200059
Subset
IM
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