γ-AChR/ε-AChR switch at agrin-induced postsynaptic-like apparatus in skeletal muscle

Molecular and Cellular Neurosciences

Volumn 9, Issue 4, 1997, Pages 254-263

  Rimer, Mendell ^a   Mathiesen, Iacob ^b   Lømo, Terje ^b   McMahan, U J ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; AGRIN; ALPHA BUNGAROTOXIN; CHOLINERGIC RECEPTOR; COMPLEMENTARY DNA; RECEPTOR SUBUNIT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; MALE; MUSCLE DENERVATION; MUSCLE REINNERVATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; RAT; SKELETAL MUSCLE; SOLEUS MUSCLE; ANIMAL; DRUG EFFECT; INNERVATION; ISOMERISM; METABOLISM; PHYSIOLOGY; SYNAPSE; WISTAR RAT;

ANIMALIA;

AGRIN; ANIMALS; ISOMERISM; MALE; MUSCLE DENERVATION; MUSCLE, SKELETAL; NEUROMUSCULAR JUNCTION; RATS; RATS, WISTAR; RECEPTORS, CHOLINERGIC; SYNAPSES;

EID: 0030609997     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1006/mcne.1997.0622     Document Type: Article

References (47)

1. Adams L., Carlson B. M., Henderson L., Goldman D. Adaptation of nicotinic acetylcholine receptor, myogenin, and mrf4 gene expression to long-term muscle denervation. J. Cell Biol. 131:1995;1341-1349.
2. Altiok N., Bessereau J.-L., Changeux J.-P. ErbB3 and erbB2/neu mediate the effect of heregulin on acetylcholine receptor gene expression in muscle: Differential expression at the endplate. EMBO J. 14:1995;4258-4266.
3. Andreose J. S., Xu R., Lømo T., Salpeter M. M., Fumagalli G. Degradation of two AChR populations at rat neuromuscular junctions: Regulation in vivo by electrical stimulation. J. Neurosci. 13:1993;3433-3438.
4. Brenner H. R., Lømo T., Williamson R. Control of end-plate channel properties by neurotrophic effects and by muscle activity in rats. J. Physiol. 388:1987;367-381.
5. Brenner H. R., Herczeg A., Slater C. R. Synapse-specific expression of acetylcholine receptor genes and their products at original synaptic sites in rat soleus muscle fibers regenerating in the absence of innervation. Development. 116:1992;41-53.
6. Brenner H. R., Rotzler S., Kues W. A., Witzemann V., Sakmann B. Nerve-dependent induction of AChR ε-subunit gene expression in muscle is independent of the state of differentiation. Dev. Biol. 165:1994;527-536.
7. Buckley K., Kelly R. B. Identification of a transmembrane glycoprotein specific for secretory vesicles of neural and endocrine origin. J. Cell Biol. 100:1985;1284-1294.
8. Chu G. C., Moscoso L. M., Sliwkowski M. X., Merlie J. P. Regulation of the acetylcholine receptor ε-subunit gene by recombinant ARIA: An in vitro model for transynaptic gene regulation. Neuron. 14:1995;329-339.
9. Cohen I., Rimer M., Lømo T., McMahan U. J. Agrin-induced postsynaptic-like apparatus in skeletal muscle fibers in vivo. Mol. Cell. Neurosci. 9:1997;327-253.
10. +. J. Neurosci. 13:1993;2118-2125.
11. DeChiara T. M., Bowen D. C., Valenzuela D. M., Simmons M. V., Poueymirou W. T., Thomas S., Kinetz E., Compton D. L., Rojas E., Park J. S., Smith C., DiStefano P. S., Glass D. J., Burden S. J., Yancopoulos G. D. The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell. 85:1996;501-512.
12. Duclert A., Changeux J. P. Acetylcholine receptor gene expression at the developing neuromuscular junction. Physiol. Rev. 75:1995;339-368.
13. Falls D. L., Rosen K. M., Corfas G., Lane W. S., Fischbach G. D. ARIA, a protein that stimulates acetylcholine receptor synthesis, is a member of the neu ligand family. Cell. 72:1993;801-815.
14. Fambrough D. M. Control of acetylcholine receptors in skeletal muscle. Physiol. Rev. 59:1979;165-227.
15. Fischbach G. D., Schuetze S. M. A post-natal decrease in acetylcholine receptor open time in rat end-plates. J. Physiol. 303:1980;125-137.
16. Gautam M., Noakes P. G., Moscoso L., Rupp F., Scheller R. H., Merlie J. P., Sanes J. R. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell. 85:1996;525-535.
17. Godfrey E. W., Nitkin R. M., Wallace B. G., Rubin L. L., McMahan U. J. Components of the Torpedo electric organ and muscle that cause aggregation of acetylcholine receptors on cultured muscle cells. J. Cell Biol. 99:1984;615-627.
18. Goldman D., Brenner H. R., Heinemann S. Acetylcholine receptor α-, β-, γ-, and δ-subunit mRNA levels are regulated by muscle activity. Neuron. 1:1988;329-333.
19. Goldman D., Carlson B. M., Staple J. Induction of adult-type acetylcholine receptor gene expression in non-innervated regenerating muscle. Neuron. 7:1991;649-658.
20. Goodearl A. D., Yee A. G., Sandrock A. A. Jr., Corfas G., Fischbach G. D. ARIA is concentrated in the synaptic basal lamina of the developing chick neuromuscular junction. J. Cell Biol. 130:1995;1423-1424.
21. Gordon T., Jones R., Vrbova G. Changes in chemosensitivity of skeletal muscles as related to endplate formation. Prog. Neurobiol. 6:1976;103-136.
22. Greengard P., Valtorta F., Czernik A. J., Benfenati F. Synaptic vesicle phosphoproteins and regulation of synaptic function. Science. 259:1993;780-785.
23. Gu Y., Hall Z. W. Immunological evidence for a change in subunits of the acetylcholine receptor in developing and denervated rat muscle. Neuron. 1:1988;117-125.
24. Jo S. A., Zhu X., Marchionni M. A., Burden S. J. Neuregulins are concentrated at nerve-muscle synapses and activate ACh-receptor gene expression. Nature. 373:1995;158-161.
25. Jones G., Herczeg A., Ruegg M. A., Lichtsteiner M., Kroger S., Brenner H. R. Substrate-bound agrin induces expression of acetylcholine receptor ε-subunit gene in cultured mammalian muscle cells. Proc. Natl. Acad. Sci. USA. 93:1996;5985-5990.
26. Jones G., Meier T., Lichtsteiner M., Witzemann V., Sakmann B., Brenner H. R. Induction by agrin of ectopic and functional postsynaptic-like membrane in innervated muscle. Proc. Natl. Acad. Sci. USA. 94:1997;2654-2659.
27. Korneliussen H., Sommerschild H. Ultrastructure of the new neuromuscular junctions formed during reinnervation of rat soleus muscle by a "foreign" nerve. Cell Tissue Res. 167:1976;439-452.
28. Kues W. A., Brenner H. R., Sakmann B., Witzemann V. Local neurotrophic repression of gene transcripts encoding fetal AChRs at rat neuromuscular synapses. J. Cell Biol. 130:1995;949-957.
29. Letinsky M. S., Fischbeck K. H., McMahan U. J. Precision of reinnervation of original postsynaptic sites in frog muscle after a nerve crush. J. Neurocytol. 5:1976;691-718.
30. Lømo T., Westgaard R. H. Further studies on the control of ACh sensitivity by muscle activity in the rat. J. Physiol. 252:1975;603-626.
31. Lømo T., Slater C. R. Control of acetylcholine sensitivity and synapse formation by muscle activity. J. Physiol. 275:1978;391-402.
32. Lømo T., Slater C. R. Acetylcholine sensitivity of developing ectopic nerve-muscle junctions in adult rat soleus muscle. J. Physiol. 303:1980;73-189.
33. Lømo T., Pockett S., Sommerschild H. Control of number and distribution of synapses during ectopic synapse formation in adult rat soleus muscles. Neuroscience. 24:1988;673-686.
34. Martinou J.-C., Falls D. L., Fischbach G. D., Merlie J. P. Acetylcholine receptor-inducing activity stimulates expression of ε-subunit gene of the muscle acetylcholine receptor. Proc. Natl. Acad. Sci. USA. 88:1991;7669-7673.
35. McMahan U. J. The agrin hypothesis. Cold Spring Harbor Symp. Quant. Biol. 50:1990;407-418.
36. 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. 321:1986;406-411.
37. Missias A. C., Chu G. C., Klocke B. J., Sanes J. R., Merlie J. P. Maturation of the acetylcholine receptor in skeletal muscle: Regulation of the AChR γ-to-ε switch. Dev. Biol. 179:1996;223-238.
38. Moscoso L. M., Chu G. C., Gautam M., Noakes P. G., Merlie J. P., Sanes J. R. Synapse-associated expression of an acetylcholine receptor-inducing protein, ARIA/heregulin, and its putative receptors, erbB2 and erbB3, in developing mammalian muscle. Dev. Biol. 172:1995;158-169.
39. Nitkin R. M., Smith M. A., Magill C., Fallon J. R., Yao Y.-M. M., Wallace B. G., McMahan U. J. Identification of agrin, a synaptic organizing protein from Torpedo electric organ. J. Cell Biol. 105:1987;2471-2478.
40. Reist N. E., Werle M. J., McMahan U. J. Agrin released by motor neurons induces the aggregation of AChRs at neuromuscular junctions. Neuron. 8:1992;865-868.
41. Rotzler S., Brenner H. R. Metabolic stabilization of acetylcholine receptors in vertebrate neuromuscular junction by muscle activity. J. Cell Biol. 111:1990;655-661.
42. Sola L. M., Martin A. W. Denervation hypertrophy and atrophy of the hemidiaphragm of the rat. Am. J. Physiol. 172:1953;324-332.
43. Tello J. F. Genesis de las terminaciones nerviosas motrices y sensitivas. I. En el sistema locomotor de los vertrebrados superiores. Histogenesis muscular. Trab. Inst. Cajal Invest. Biol. 15:1917;101-199.
44. Valenzuela D. M., Stitt T. N., DiStefano P. S., Rojas E., Mattson K., Compton D. L., Nunez L., Thomas S., Le Beau M. M., Fernald A. A., Copeland N. G., Jenkins N. A., Burden S. J., Glass D. J., Yancopoulos G. D. Receptor tyrosine kinase specific for the skeletal muscle lineage: Expression in embryonic muscle, at the neuromuscular junction and after injury. Neuron. 15:1995;573-584.
45. Witzemann V., Barg B., Nishikawa Y., Sakmann B., Numa S. Differential regulation of muscle acetylcholine receptor γ- and ε-subunit mRNAs. FEBS Lett. 223:1987;104-112.
46. Witzemann V., Brenner H. R., Sakmann B. Neural factors regulate AChR subunit mRNAs at rat neuromuscular synapses. J. Cell Biol. 114:1991;125-141.
47. Zhu X., Lai C., Thomas S., Burden S. J. Neuregulin receptors, erbB3 and erbB4, are localized at neuromuscular synapses. EMBO J. 14:1995;5842-5848.