Neuronal-type acetylcholine receptors and regulation of α7 gene expression in vertebrate skeletal muscle

Journal of Neurobiology

Volumn 32, Issue 1, 1997, Pages 69-80

  Romano, Suzanne J ^a   Pugh, Phyllis C ^a,c   McIntosh, J Michael ^b   Berg, Darwin K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

bungarotoxin; conotoxin; neuronal; nicotinic; transcript

Indexed keywords

8 BROMO CYCLIC AMP; ALPHA BUNGAROTOXIN; CALCITONIN GENE RELATED PEPTIDE RECEPTOR; GENE PRODUCT; MESSENGER RNA; NICOTINIC RECEPTOR; RIBONUCLEASE;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; CHICKEN; EMBRYO; GENE EXPRESSION REGULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; RAT; RECEPTOR BINDING; RECEPTOR UPREGULATION; SKELETAL MUSCLE;

8-BROMO CYCLIC ADENOSINE MONOPHOSPHATE; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODY SPECIFICITY; BINDING, COMPETITIVE; BUNGAROTOXINS; CALCITONIN GENE-RELATED PEPTIDE; CELLS, CULTURED; CHICK EMBRYO; CHICKENS; CHOLINERGIC AGONISTS; COS CELLS; ELECTRIC STIMULATION; GENE EXPRESSION REGULATION; IMMUNOBLOTTING; IODINE RADIOISOTOPES; MOTOR NEURONS; MUSCLE DENERVATION; MUSCLE, SKELETAL; RECEPTORS, CHOLINERGIC; RNA, MESSENGER; TETRODOTOXIN; VERTEBRATES;

EID: 0031024599     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(199701)32:1<69::AID-NEU7>3.0.CO;2-C     Document Type: Article

References (55)

1. BERTRAND, D., GALZI, J. L., DEVILLERS-THIERY, A., BERTRAND, S., and CHANGEUX, J. P. (1993). Mutations at two distinct sites within the channel domain M2 alter calcium permeability of neuronal α7 nicotinic receptor. Proc. Natl. Acad. Sci. USA 90:6971-6975.
2. BETZ, H., and CHANGEUX, J. P. (1979). Regulation of muscle acetylcholine receptor synthesis in vitro by cyclic nucleotide derivatives. Nature 278:749-752.
3. BLOUNT, P., SMITH, M. M., and MERLIE, J. P. (1990). Assembly intermediates of the mouse muscle nicotinic acetylcholine receptor in stably transfected fibroblasts. J. Cell Biol. 111:2601-2611.
4. BRUMWELL, C., LEVEY, M. S., IKONOMOV, O. C., and JACOB, M. H. (1995). Regulation of α-bungarotoxin receptor expression indeveloping neurons. Soc. Neurosci. Abs. 21:1336.
5. CHANGEUX, J. P. (1991). Compartmentalized transcription of acetylcholine receptor genes during motor end-plate epigenesis. New Biol. 3:413-429.
6. CHANGEUX, J. P., DUCLERT, A., and SEKINE, S. (1992). Calcitonin gene-related peptides and neuromuscular interactions. Ann. NY Acad. Sci. 657:361-378.
7. CHENG, Y., and PRUSOFF, W. H. (1973). Relationship between the inhibition constant (Ki) and the concentration of inhibitor which causes 50 per cent inhibition (150) of an enzymatic reaction. Biochem. Pharmacol. 22:3099-3108.
8. CHOMCZYNSKI, P., and SACCHI, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
9. COLQUHOUN, L., LE PICHON, J. B., VOLLRATH, M., and PATRJCK, J. (1994). α7 Receptor function is rescued from cyclosporin block by coexpression with muscle δ subunit. Soc. Neurosci. Abs. 20:840.
10. CONROY, W. G., and BERG, D. K. (1995). Neurons can maintain multiple classes of nicotinic acetylcholine receptors distinguished by different subunit compositions. J. Boil. Chem. 270:4424-4431.
11. CONROY, W. G., VERNALLIS, A. B., and BERG, D. K. (1992). The α5 gene product assembles with multiple acetylcholine receptor subunits to form distinctive receptor subtypes in brain. Neuron 9:679-691.
12. CORRIVEAU, R. A., and BERG, D. K. (1993). Coexpression of multiple acetylcholine receptor genes in neurons: quantification of transcripts during development. J. Neurosci. 13:2662-2671.
13. CORRIVEAU, R. A., ROMANO, S. J., CONROY, W. G., OLIVA, L., and BERG, D. K. (1995). Expression of neuronal acetylcholine receptor genes in vertebrate skeletal muscle during development. J. Neurosci. 15:1372-1383.
14. COUTURIER, S., BERTRAND, D., MATTER, J. M., HERNANDEZ, M. C., BERTRAND, S., MILLAR, N., VALERA. S., BARKAS, T., and BALLIVET, M. (1990a). A neuronal nicotinic acetylcholine receptor subunit (α7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-BTX. Neuron 5:847-856.
15. COUTURIER, S., ERKMAN, L., VALERA, S., RUNGGER, D., BERTRAND, S., BOULTER, J., BALLIVET, M., and BERTRAND, D. (1990b). α5, α3, and non-α3. Three clustered avion genes encoding neuronal nicotinic acetylcholine receptor-related subunits. J. Biol. Chem. 265:17560-17567.
16. DE KONINCK, P., and COOPER, E. (1995). Differential regulation of neuronal nicotinic ACh receptor subunit genes in cultured neonatal rat sympathetic neurons: Specific induction of α7 by membrane depolarization through a Ca2+/calmodulin-dependent kinase pathway. J. Neurosci. 15:7966-7978.
17. FALLS, D. L., HARRIS, D. A., JOHNSON, F. A., MORGAN, M. M., CORFAS, G., and FISCHBACH, G. D. (1990). Mr 42,000 ARIA: a protein that may regulate the accumulation of acetylcholine receptors at developing chick neuromuscular junctions. Cold Spring Harbor Symp. Quant. Biol. 55:397-406.
18. FISCHBACH, G. D. (1972). Synapse formation between dissociated nerve and muscle cells in low density cell cultures. Dev. Biol. 28:407-429.
19. FONTAINE, B., KLARSFELD, A., and CHANGEUX, J. P. (1987). Calcitonin gene-related peptide and muscle activity regulate acetylcholine receptor a-subunit mRNA levels by distinct intracellular pathways. J. Cell. Biol. 105:1337-1342.
20. FROEHNER, S. C., DOUVILLE, K., KLINK, S., and GULP, W. J. (1983). Monoclonal antibodies to cytoplasmic domains of the acetylcholine receptor. J. Biol. Chem. 258:7112-7120.
21. GOTTI, C., HANKE, W., MAURY, K., MORETTI, M., BALLIVET, M., CLEMENTI, F., and BERTRAND, D. (1994). Pharmacology and biophysical properties of α7 and α7-α8 α-bungarotoxin receptor subtypes immunopurified from the chick optic lobe. Eur. J. Neurosci. 6:1281-1291.
22. GROEBE, D. R., DUMM, J. M., LEVITAN, E. S., and ABRAMSON, S. N. (1995). α-Conotoxins selectively inhibit one of the two acetylcholine binding sites of nicotinic receptors. Mol. Pharmacol. 48:105-111.
23. Gu, Y., FRANCO, A., JR., GARDNER, P.D., LANSMAN, J. B., FORSAYETH, J. R., and HALL, Z. W. (1990). Properties of embryonic and adult muscle acetylcholine receptors transiently expressed in COS cells. Neuron 5:147-157.
24. Gu, Y., and HALL, Z. W. (1988). Characterization of acetylcholine receptor subunits in developing and in denervated mammalian muscle. J. Biol. Chem. 263:12878-12885.
25. GULLICK, W. J., and LINDSTROM, J. M. (1983). Mapping the binding of monoclonal antibodies to the acetylcholine receptor from Torpedo californica. Biochemistry 22:3312-3320.
26. HALL, Z. W., and SANES, J. R. (1993). Synaptic structure and development: the neuromuscular junction. Cell 72(Suppl):99-121.
27. HARRIS, D. A., FALLS, D. L., DILL-DEVOR, R. M., and FISCHBACH, G. D. (1988). Acetylcholine receptor-inducing factor from chicken brain increases the level of mRNA encoding the receptor α subunit. Proc. Natl. Acad. Sci. USA 85:1983-1987.
28. HELEKAR, S. A., CHAR, D., NEFF, S., and PATRICK, J. (1994). Prolyl isomerase requirement for the expression of functional homo-oligomeric ligand-gated ion channels. Neuron 12:179-189.
29. JACOB, M. H., and BERG, D. K. (1987). Effects of preganglionic denervation and postganglionic axotomy on acetylcholine receptors in the chick ciliary ganglion. J. Cell. Biol. 105:1847-1854.
30. JOHNSON, D. S., MARTINEZ, J., ELGOYHEN, A. B., HEINEMAN, S. F., and MCINTOSH, J. M. (1995). α-Conotoxin ImI exhibits subtype-specific nicotinic acetylcholine receptor blockade: preferential inhibition of homomeric α7 and α9 receptors. Mol. Pharmacol. 48:194-199.
31. KEYSER, K. T., BRITTO, L. R., SCHOEPFER, R., WHITING. P., COOPER, J., CONROY, W., BROZOZOWSKA-PRECHTL, A., KARTEN, H. J., and LINDSTROM, J. (1993). Three subtypes of α-bungarotoxin-sensitive nicotinic acetyl-choline receptors are expressed in chick retina. J. Neurosci. 13:442-454.
32. KIRILOVSKY, J., DUCLERT, A., FONTAINE, B., DEVILLERS-THIERY, A., OSTERLUND, M., and CHANGEUX, J. P. (1989). Acetylcholine receptor expression in primary cultures of embryonic chick myotubes - II. Comparison between the effects of spinal cord cells and calcitonin gene-related peptide. Neuroscience 32:289-296.
33. KLARSFELD, A., and CHANGEUX, J. P. (1985). Activity regulates the levels of acetylcholine receptor a-subunit mRNA in cultured chicken myotubes. Proc. Natl. Acad. Sci. USA 82:4558-4562.
34. KLARSFELD, A., LAUFER, R., FONTAINE, B., DEVILLERS-THIERY, A., DUBREUIL, C., and CHANGEUX, J. P. (1989). Regulation of muscle AChR a subunit gene expression by electrical activity: involvement of protein kinase C and Ca2+. Neuron 2:1229-1236.
35. LAUFER, R., and CHANGEUX, J. P. (1987). Calcitonin gene-related peptide elevates cyclic AMP levels in chick skeletal muscle: possible neurotrophic role for a coexisting neuronal messenger. Embo. J. 6:901-906.
36. MATTER-SADZINSKI, L., HERNANDEZ, M. C., ROZTOCIL, T., BALLIVET, M., and MATTER, J. M. (1992). Neuronal specificity of the α7 nicotinic acetylcholine receptor promoter develops during morphogenesis of the central nervous system. Embo. J. 11:4529-4538.
37. MCINTOSH, J. M., YOSHIKAMI, D., MAHE, E., NIELSEN, D. B., RIVIER, J. E., GRAY, W. R., and OLIVERA, B. M. (1994). A nicotinic acetylcholine receptor ligand of unique specificity, α-conotoxin ImI. J. Biol. Chem. 269:16733-16739.
38. NEF, P., MAURON, A., STALDER, R., ALLIOD, C., and BALLIVET, M. (1984). Structure linkage, and sequence of the two genes encoding the δ and γ subunits of the nicotinic acetylcholine receptor. Proc. Natl. Acad. Sci. USA 81:7975-7979.
39. NISHI, R., and BERG, O.K. (1981). Two components from eye tissue that differentially stimulate the growth and development of ciliary ganglion neurons in cell culture. J. Neurosci. 1:505-513.
40. OSTERLUND, M., FONTAINE, B., DEVILLERS-THIERY, A., GEOFFROY, B., and CHANGEUX, J. P. (1989). Acetylcholine receptor expression in primary cultures of embryonic chick myotubes - I. Discoordinate regulation of α-, γ-, and δ-subunit gene expression by calcitonin gene-related peptide and by muscle electrical activity. Neuroscience 32:279-287.
41. PATON, W. D. M., and ZAIMIS, E. J. (1949). The pharmacological actions of polymethylene bistrimethylammonium salts. Br. J. Pharmacol. 4:381-400.
42. PUGH, P. C., CORRIVEAU, R. A., CONROY, W. G., and BERG, D. K. (1995). Novel subpopulation of neuronal acetylcholine receptors among those binding α-bungarotoxin. Mol. Pharmacol. 47:717-725.
43. RATNAM, M., SARGENT, P. B., SARIN, V., Fox, J. L., NGUYEN, D. L., RIVIER, J., CRIADO, M., and LINDSTROM, J. (1986). Location of antigenic determinants on primary sequences of subunits of nicotinic acetylcholine receptor by peptide mapping. Biochemistry 25:2621-2632.
44. SASSOON, D. A. (1993). Myogenic regulatory factors: dissecting their role and regulation during vertebrate embryogenesis. Dev. Biol. 156:11-23.
45. SCHOEPFER, R., CONROY, W. G., WHITING, P., GORE, M., and LINDSTROM, J. (1990). Brain α-bungarotoxin binding protein cDNAs and MAbs reveal subtypes of this branch of the ligand-gated ion channel gene superfamily. Neuron 5:35-48.
46. SCHUETZE, S. M., and ROLE, L. W. (1987). Developmental regulation of nicotinic acetylcholine receptors. Annu. Rev. Neurosci. 10:403-457.
47. SEGUELA, P., WADICHE, J., DINELEY-MILLER, K., DANI, J. A., and PATRICK, J. W. (1993). Molecular cloning, functional properties, and distribution of rat brain α7: a nicotinic cation channel highly permeable to calcium. J. Neurosci. 13:596-604.
48. SHIEH, B. H., BALLIVET, M., and SCHMIDT, J. (1987). Quantitation of an alpha subunit splicing intermediate: evidence for transcriptional activation in the control of acetylcholine receptor expression in denervated chick skeletal muscle. J. Cell. Biol. 104:1337-1341.
49. SHIEH, B. H., BALLIVET, M., and SCHMIDT, J. (1988). Acetylcholine receptor synthesis rate and levels of receptor subunit messenger RNAs in chick muscle. Neuroscience 24:175-187.
50. SMITH, M. A., STOLLBERG, J., LINDSTROM, J. M., and BERG, D. K. (1985). Characterization of a component in chick ciliary ganglia that cross-reacts with monoclonal antibodies to muscle and electric organ acetylcholine receptor. J. Neurosci. 5:2726-2731.
51. TOWBIN, H., STAEHELIN, T., and GORDON, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76:4350-4354.
52. TSAY, H. J., and SCHMIDT, J. (1989). Skeletal muscle denervation activates acetylcholine receptor genes. J. Cell. Biol. 108:1523-1526.
53. TZARTOS, S., LANGEBERG, L., HOCHSCHWENDER, S., SWANSON, L. W., and LINDSTROM, J. (1986). Characteristics of monoclonal antibodies to denatured Torpedo and to native calf acetylcholine receptors: species, subunit and region specificity. J. Neuroimmunol. 10:235-253.
54. VERNALLIS, A. B., CONROY, W. G., and BERG, D. K. (1993). Neurons assemble acetylcholine receptors with as many as three kinds of subunits while maintaining subunit segregation among receptor subtypes. Neuron 10:451-464.
55. WARD, J. M., COCKCROFT, V. B., LUNT, G. G., SMILLIE, F.S., and WONNACOTT, S. (1990). Methyllycaconitine: a selective probe for neuronal α-bungarotoxin binding sites. FEBS Lett. 270:45-48.