Acetylcholinesterase and nicotinic acetylcholine receptor expression diverge in muscular dysgenic mice lacking the L-type calcium channel

Journal of Neurochemistry

Volumn 67, Issue 1, 1996, Pages 111-118

  Luo, Z David ^a   Pincon Raymond, Martine ^b   Taylor, Palmer ^a  

^a San Diego   (United States)

^b CENTRE DE RECHERCHE DES CORDELIERS   (France)

Author keywords

Acetylcholinesterase expression; L type Ca2+ channels; mRNA stabilization; Muscle development; Muscular dysgenesis; Nicotinic acetylcholine receptors

Indexed keywords

ACETYLCHOLINESTERASE; CALCIUM CHANNEL; CHOLINERGIC RECEPTOR; MESSENGER RNA; NICOTINIC RECEPTOR;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; ENZYME ACTIVITY; MOUSE; MUSCLE DEVELOPMENT; MUSCLE DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; RNA ANALYSIS;

ANIMALIA;

EID: 0029931262     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1996.67010111.x     Document Type: Article

References (47)

1. Adams B. A., Tanabe T., Mikami A., Numa S., and Beam K. (1990) Intramembrane charge movement restored in dysgenic skeletal muscle by injection of the dihydropyridine receptor cDNAs. Nature 346, 569-572.
2. Baldwin T. and Burden S. J. (1988) Isolation and characterization of the mouse acetylcholine receptor δ-subunit gene: identification of a 148-bp cis-acting region that confers myotube specific expression. J. Cell Biol. 107, 2271-2279.
3. Beam K. G., Knudson C. M., and Powell J. A. (1986) A lethal mutation in mice eliminates the slow calcium current in skeletal muscle cells. Nature 320, 168-170.
4. Buonanno A. and Merlie J. P. (1986) Transcriptional regulation of nicotinic acetylcholine receptor genes during muscle development. J. Biol. Chem. 261, 11452-11455.
5. Chaudhari N. (1992) A single nucleotide deletion in the skeletal muscle-specific calcium channel transcript of muscular dysgenesis (mdg) mice. J. Biol. Chem. 267, 25636-25639.
6. Chaudhari N. and Beam K. G. (1989) The muscular dysgenesis mutation in mice leads to arrest of the genetic program for muscle differentiation. Dev. Biol. 133, 456-467.
7. Chomczynski P. and Sacchi N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
8. Decker M. M. and Berman H. A. (1990) Denervation-induced alteration of acetylcholinesterase biosynthesis. Exp. Neurol. 109, 247-255.
9. Ellman G. L., Courtney K. D., Andres V. Jr., and Featherstone R. M. (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmacol. 7, 88-95.
10. Evans S., Goldman D., Heinemann S., and Patrick J. (1987) Muscle acetylcholine receptor biosynthesis: regulation by transcript availability. J. Biol. Chem. 262, 4911-4916.
11. Fambrough D. M. (1979) Control of acetylcholine receptor in skeletal muscle. Physiol. Rev. 59, 165-227.
12. Flucher B. E., Andrews S. B., Fleischer S., Marks A. R., Caswell A., and Powell J. A. (1993) Triad formation: organization and function of the sarcoplasmic reticulum calcium release channel and triadin in normal and dysgenic muscle in vitro. J. Cell Biol. 123, 1161-1174.
13. Frail D. E., Musil L. S., Buonanno A., and Merlie J. P. (1989) Expression of RAPsyn (43K protein) and nicotinic acetylcholine receptor genes is not coordinately regulated in mouse muscle. Neuron 2, 1077-1086.
14. Franzini-Armstrong C., Pincon-Raymond M., and Rieger F. (1991) Muscle fibers from dysgenic mouse in vivo lack a surface component of peripheral couplings. Dev. Biol. 146, 364-376.
15. Fuentes M. E. and Taylor P. (1993) Control of acetylcholinesterase gene expression during myogenesis. Neuron 10, 679-687.
16. Gilman M. (1989) Ribonuclease protection assay, in Current Protocol in Molecular Biology, Suppl. 7 (Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A., and Struhl K., eds), pp. 4.7.1-4.7.8. John Wiley and Sons, New York.
17. Gluecksohn-Waelsch S. (1963) Lethal genes and analysis of the differentiation. Science 142, 1269-1276.
18. Goldman D., Boulter J., Heinemann S., and Patrick J. (1985) Muscle denervation increases the levels of two mRNAs encoding for the acetylcholine receptor α-subunit. J. Neurosci. 5, 2553-2558.
19. Goldman D., Brenner H. R., and Heinemann S. (1988) Acetylcholine receptor α-, β-, γ-, and δ-subunit mRNA levels are regulated by muscle activity. Neuron 1, 329-333.
20. Howe J. G. and Steitz J. A. (1986) Localization of Epstein-Barr virus-encoded small RNAs by in situ hybridization. Proc. Natl. Acad. Sci. USA 83, 9006-9010.
21. Huang C.-F., Flucher B. E., Schmidt M. M., Stroud S. K., and Schmidt J. (1994) Depolarization-transcription signals in skeletal muscle use calcium flux through L channels, but bypass the sarcoplasmic reticulum. Neuron 13, 167-177.
22. Inestrosa N. C., Miller J. B., Silberstein L., Ziskind-Conhaim L., and Hall Z. W. (1983) Development and regulation of 16S acetylcholinesterase and acetylcholine receptors in a mouse muscle cell line. Exp. Cell Res. 147, 393-405.
23. Isenberg K. E., Mudd J., Shah V., and Merlie J. P. (1986) Nucleotide sequence of the mouse muscle nicotinic acetylcholine receptor a subunit. Nucleic Acids Res. 14, 5111.
24. Janis R. A., Silver P. J., and Triggle D. J. (1987) Drug action and cellular calcium regulation. Adv. Drug Res. 16, 309-591.
25. 2+ in excitation-contraction uncoupled dysgenic muscle. Dev. Biol. 99, 152-165.
26. 1 subunit of the dihydropyridine receptor in mice with muscular dysgenesis. J. Biol. Chem. 264, 1345-1348.
27. Li Y., Camp S., Rachinsky T. L., Getman D., and Taylor P. (1991) Gene structure of mammalian acetylcholinesterase: alternative exons dictate tissue-specific expression. J. Biol. Chem. 266, 23083-23090.
28. Lu X., Xu L., and Meissner G. (1994) Activation of the skeletal muscle calcium release channel by a cytoplasmic loop of the dihydropyridine receptor. J. Biol. Chem. 269, 6511-6516.
29. Luo Z., Fuentes M.-E., and Taylor P. (1994) Regulation of acetylcholinesterase mRNA stability by calcium during differentiation from myoblasts to myotubes. J. Biol. Chem. 269, 27216-27223.
30. Massoulie J., Pezzementi L., Bon S., Krejci E., and Valletta F.-M. (1993) Molecular and cellular biology of cholinesterases. Prog. Neurobiol. 41, 31-91.
31. Merlie J. P., Isenberg K. E., Russell S. D., and Sanes J. R. (1984) Denervation supersensitivity in skeletal muscle: analysis with a cloned cDNA probe. J. Cell Biol. 99, 332-335.
32. Michel R. N., Vu C. Q., Tetzlaff W., and Jasmin B. J. (1994) Neural regulation of acetylcholinesterase mRNAs at mammalian neuromuscular synapses. J. Cell Biol. 127, 1061-1069.
33. Pai A. C. (1965) Developmental genetics of a lethal mutation, muscular dysgenesis (mdg), in the mouse. Dev. Biol. 11, 82-92.
34. 2+ channel inhibitors of the dihydropyridine family in skeletal muscle from mice with embryonic muscular dysgenesis. Dev. Biol. 112, 458-466.
35. Pincon-Raymond M., Garcia L., Romey G., Lazdunski M., and Rieger F. (1990) A genetic model for the study of abnormal nerve-muscle interaction at the level of excitation-contraction coupling: the mutation muscular dysgenesis. J. Physiol. (Paris) 84, 82-87.
36. Pincon-Raymond M., Vicart P., Bois P., Chassande O., Romey G., Varadi G., Li Z. L., Lazdunski M., Rieger F., and Paulin D. (1991) Conditional immortalization of normal and dysgenic mouse muscle cells by the SV40 large T antigen under the vimentin promoter control. Dev. Biol. 148, 517-528.
37. Powell J. A. and Fambrough D. M. (1973) Electrical properties of normal and dysgenic mouse skeletal muscle in culture. J. Cell. Physiol. 82, 21-38.
38. Rieger F., Bournaud R., Shimagara T., Garcia L., Pincon-Raymond M., Romey G., and Lazdunski M. (1987) Restoration of dysgenic muscle contraction and calcium channel function by co-culture with normal spinal cord neurons. Nature 330, 563-566.
39. 2+ mediate changes in acetylcholinesterase and acetylcholine receptors caused by muscle contraction. Proc. Natl. Acad. Sci. USA 92, 7121-7125.
40. Schneider M. F. and Chandler W. K. (1973) Voltage-dependent charge movement in skeletal muscle: a possible step in excitation-contraction coupling. Nature 242, 244-246.
41. Silman I., Lyles J. M., and Barnard E. A. (1978) Intrinsic forms of acetylcholinesterase in skeletal muscle. FEBS Lett. 94, 166-170.
42. Sketelj J., Črne-Finderle N., and Brzin M. (1992) Influence of denervation on the molecular forms of junctional and extrajunctional acetylcholinesterase in fast and slow muscles of the rat. Neurochem. Int. 21, 415-421.
43. Sketelj J., Črne-Finderle N., Sket D., Dettbarn W.-D., and Brzin M. (1993) Comparison between the effects of botulinum toxin-induced paralysis and denervation on molecular forms of acetylcholinesterase in muscles. J. Neurochem. 61, 501-508.
44. Tanabe T., Beam K. G., Powell J. A., and Numa S. (1588) Restoration of excitation-contraction coupling and slow calcium current in dysgenic muscle by dihydropyridine receptor complementary DNA. Nature 336, 134-139.
45. 2+ channels do not overcome the E-C coupling defect in immortalized dysgenic muscle cells: evidence for a missing link. FEBS Lett. 368, 405-410.
46. Wang Y., Xu H.-P., Wang X.-M., Ballivet M., and Schmidt J. (1988) A cell type-specific enhancer drives expression of the chick muscle acetylcholine receptor α-subunit gene. Neuron 1, 527-534.
47. Weintraub H., Davis R., Tapscott S., Thayer M., Krause M., Benezra R., Blackwell K., Turner D., Rupp R., Hollenberg S., Zhuang Y., and Lassar A. (1991) The myoD gene family: nodal point during specification of the muscle cell lineage. Science 251, 761-766.