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Regulation of Neuronal Acetylcholine Receptors by Cell-Cell Interactions

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Part of the book series: NATO ASI Series ((ASIH,volume 25))

Abstract

Much of what is known about the role of cell-cell interactions in regulating synaptic components comes from studies of the vertebrate neuromuscular junction, and by far the best understood component there is the nicotinic acetylcholine receptor (AChR). Monoclonal antibodies (mAbs) and neurotoxins are now available that recognize neuronal AChRs (for reviews see Lindstrom et al., 1987; Loring and Zigmond, 1988), and cDNA and genomic probes have been isolated for neuronal AChR mRNAs (Boulter et al., 1986, 1987; Deneris et al., 1988; Nef et al., 1988). Such probes permit comparative studies assessing whether principles governing the regulation of AChRs at the neuromuscular junction can be extended to neurotransmitter receptors at synapses on neurons. We have found that while neuronal AChRs are similar to AChRs of muscle and electric organ in a number of respects, they differ in regulation of receptor levels by presynaptic input and in regulation of receptor function by second messengers. The differences may render neuronal AChRs particularly responsive to modulation by cell-cell interactions, and the modulation could regulate neuronal detection of synaptic signalling.

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References

  • Adler R, Landa KB, Manthorpe M and Varon S (1979) Cholinergic neuronotrophic factors: intraocular distribution of trophic activity for ciliary neurons. Science 204: 1434–1436

    Article  PubMed  CAS  Google Scholar 

  • Albuquerque EX, Desparde SS, Arcava Y, Alkondon M and Daly JW (1986) A possible involvement of cyclic AMP in the expression of desensitization of the nicotinic acetylcholine receptor. A study with forskolin and its analogs. Febs Lett 199: 113–120

    Article  PubMed  CAS  Google Scholar 

  • Baldwin TJ, Yoshihara CM, Blackmer K, Kintner CR and Burden SJ (1988) Regulation of acetylcholine receptor transcript expression during development in Xenopus laevis. J Cell Biol 106: 469–478

    Article  PubMed  CAS  Google Scholar 

  • Barbin G, Manthorpe M and Varon S (1984) Purification of the chick eye ciliary neuronotrophic factor. J Neurochem 43: 1468–1478

    Article  PubMed  CAS  Google Scholar 

  • Boulter J, Evans K, Goldman D, Martin G, Treco D, Heinemann S and Patrick J (1986) Isolation of a cDNA clone coding for a possible neural nicotinic acetylcholine α-subunit. Nature 319: 368–374

    Article  PubMed  CAS  Google Scholar 

  • Boulter J, Connolly J, Deneris E, Goldman D, Heinemann S and Patrick J (1987) Functional expression of two neuronal nicotinic acetylcholine receptors from cDNA clones identifies a gene family. Proc Natl Acad Sci USA 84:7763–7767

    Article  PubMed  CAS  Google Scholar 

  • Boyd RT, Jacob MH, Couturier S, Ballivet M and Berg DK. Expression and regulation of neuronal acetylcholine receptor mRNA in chick ciliary ganglia. Submitted

    Google Scholar 

  • Brenner HR and Martin AR (1976) Reduction in acetylcholine sensitivity of axotomized ciliary ganglion cells. J Physiol (Lond) 260: 159–175

    CAS  Google Scholar 

  • Deneris ES, Connolly J, Boulter J, Wada E, Wada K, Swanson LW, Patrick J and Heinemann S (1988) Primary structure and expression of β2: a novel subunit of neuronal nicotinic acetylcholine receptors. Neuron 1: 45–54

    Article  PubMed  CAS  Google Scholar 

  • Dennis MJ and Sargent PB (1979) Loss of extrasynaptic acetylcholine sensitivity upon reinnervation of parasympathetic ganglion cells. J Physiol (Lond) 289: 263–275

    CAS  Google Scholar 

  • Dunn PM and Marshall LM (1985) Lack of nicotinic supersensitivity in frog sympathetic neurones following denervation. J Physiol (Lond) 363: 211–225

    CAS  Google Scholar 

  • Fenwick EM, Marty A and Neher E (1982) A patch-clamp study of bovine chromaffin cells and of their sensitivity to acetylcholine. J Physiol (Lond) 331: 577–597

    CAS  Google Scholar 

  • Halvorsen SW and Berg DK (1987) Affinity labeling of neuronal acetylcholine receptor subunits with an α-neurotoxin that blocks receptor function. J Neurosci 7: 2547–2555

    PubMed  CAS  Google Scholar 

  • Higgins LS and Berg DK (1987) Immunological identification of a nicotinic acetylcholine receptor on bovine chromaffin cells. J Neurosci 7: 1792–1798

    PubMed  CAS  Google Scholar 

  • Higgins LS and Berg DK (1988) A desensitized form of neuronal acetylcholine receptor detected by 3H-nicotine binding on bovine adrenal chromaffin cells. J Neurosci, in press

    Google Scholar 

  • Higgins LS and Berg DK. Metabolic stability and antigenic modulation of nicotinic acetylcholine receptors on bovine adrenal chromaffin cells. Submitted a

    Google Scholar 

  • Higgins LS and Berg DK. A cyclic AMP-dependent mechanism regulates acetylcholine receptor function on bovine adrenal chromaffin cells and discriminates between new and old receptors. Submitted b

    Google Scholar 

  • Huganir RL, Delcour AH, Greengard P and Hess GP (1986) Phosphorylation of the nicotinic acetylcholine receptor regulates its rate of desensitization. Nature 321: 774–776

    Article  PubMed  CAS  Google Scholar 

  • Jacob MH and Berg DK (1987) Effects of preganglionic denervation and post-ganglionic axotomy on ACh receptors in the chick ciliary ganglion. J Cell Biol 105: 1847–1854

    Article  PubMed  CAS  Google Scholar 

  • Jacob MH and Berg DK (1988) The acetylcholine receptor distribution of chick ciliary ganglion neurons following disruption of ganglionic connections. J Neurosci, in press

    Google Scholar 

  • Jacob MH, Lindstrom JM and Berg DK (1986) Surface and intracellular distribution of a putative neuronal acetylcholine receptor. J Cell Biol 103: 205–214

    Article  PubMed  CAS  Google Scholar 

  • Kuffler SW, Dennis MJ and Harris AJ (1971) The development of chemosensitivity in extrasynaptic areas of the neuronal surface after denervation of parasympathetic ganglion cells in the heart of the frog. Proc Roy Soc Lond B 177: 555–563

    Article  CAS  Google Scholar 

  • Lindstrom J, Schoepfer R and Whiting P (1987) Molecular studies of the neuronal nicotinic acetylcholine receptor family. Mol Neurobiol 1: 281–337

    Article  PubMed  CAS  Google Scholar 

  • Livett BG (1984) Adrenal medullary chromaffin cells in vitro. Physiol Rev 64: 1103–1161

    PubMed  CAS  Google Scholar 

  • Loring RH and Zigmond RE (1988) Characterization of neuronal nicotinic receptors by snake venom neurotoxins. Trends in Neurosci 11: 73–78

    Article  CAS  Google Scholar 

  • Margiotta JF, Berg DK and Dionne VE (1987a) The properties and regulation of functional acetylcholine receptors on chick ciliary ganglion neurons. J Neurosci 7: 3612–3622

    PubMed  CAS  Google Scholar 

  • Margiotta JF, Berg DK and Dionne VE (1987b) Cyclic AMP regulates the proportion of functional acetylcholine receptors on chicken ciliary ganglion neurons. Proc Natl Acad Sci USA 84: 8155–8159

    Article  PubMed  CAS  Google Scholar 

  • McEachern AE, Margiotta JF and Berg DK (1985) GABA receptors on chick ciliary ganglion neurons in vivo and in cell culture. J Neurosci 5: 2690–2695

    PubMed  CAS  Google Scholar 

  • McHugh EM and McGee Jr. R (1986) Direct anesthetic-like effects of forskolin on the nicotinic acetylcholine receptors of PC12 cells. J Biol Chem 261: 3103–3106

    PubMed  CAS  Google Scholar 

  • Merlie JP, Isenberg KE, Russell SD and Sanes JR (1984) Denervation supersensitivity in skeletal muscle: analysis with a cloned cDNA probe. J Cell Biol 99: 332–335

    Article  PubMed  CAS  Google Scholar 

  • Middleton P, Jaramillo F and Schuetze SM (1986) Forskolin increases the rate of acetylcholine receptor desensitization at rat soleus endplates. Proc Natl Acad Sci USA 83: 4967–4971

    Article  PubMed  CAS  Google Scholar 

  • Miles K, Anthony DT, Rubin LL, Greengard P and Huganir RL (1987) Regulation of nicotinic acetylcholine receptor phosphorylation in rat myotubes by forskolin and cAMP. Proc Natl Acad Sci USA 84: 6591–6595

    Article  PubMed  CAS  Google Scholar 

  • Nef P, Oneyser C, Alliod C, Couturier S and Ballivet M (1988) Genes expressed in the brain define three distinct neuronal nicotinic acetylcholine receptors. EMBO J 7: 595–601

    PubMed  CAS  Google Scholar 

  • Nja A and Purves D (1978) The effects of nerve growth factor and its antiserum on synapses in the superior cervical ganglion of the guinea-pig. J Physiol (Lond) 277: 53–75

    CAS  Google Scholar 

  • Nishi R and Berg DK (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 Purves D (1975) Functional and structural changes in mammalian sympathetic neurones following interruption of their axons. J Physiol (Lond) 252: 429–463

    Google Scholar 

  • Roper S (1976) The acetylcholine sensitivity of the surface membrane of multiply-innervated parasympathetic ganglion cells in the mudpuppy before and after partial denervation. J Physiol (Lond) 254: 455–473

    CAS  Google Scholar 

  • Schuetze SM and Role LW (1987) Developmental regulation of the nicotinic acetylcholine receptor. Ann Rev Neurosci 10: 403–457

    Article  PubMed  CAS  Google Scholar 

  • Smith MA, Margiotta JF and Berg DK (1983) Differential regulation of acetylcholine sensitivity and α-bungarotoxin-binding sites on ciliary ganglion neurons in cell culture. J Neurosci 3: 2395–2402

    PubMed  CAS  Google Scholar 

  • Smith MM, Merlie JP and Lawrence JC, Jr (1987) Regulation of phosphorylation of nicotinic acetylcholine receptors in mouse BC3H1 myocytes. Proc Natl Acad Sci USA 84: 6601–6605

    Article  PubMed  CAS  Google Scholar 

  • Stollberg J and Berg DK (1987) Neuronal acetylcholine receptors: fate of surface and internal pools in cell culture. J Neurosci 7: 1809–1815

    PubMed  CAS  Google Scholar 

  • Tuttle JB (1983) Interaction with membrane remnants of target myotubes maintains transmitter sensitivity of cultured neurons. Science 220: 977–979

    Article  PubMed  CAS  Google Scholar 

  • Tzartos SJ, Rand DE, Einarson BL and Lindstrom JM (1981) Mapping of surface structure of Electrophorus acetylcholine receptor using monoclonal antibodies. J Biol Chem 256: 8635–8645

    PubMed  CAS  Google Scholar 

  • Whiting PJ and Lindstrom J (1986) Purification and characterization of an acetylcholine receptor from chick brain. Biochemistry 25: 2082–2093

    Article  PubMed  CAS  Google Scholar 

  • Whiting PJ and Lindstrom J (1987) Purification and characterization of a nicotinic acetylcholine receptor from rat brain. Proc Natl Acad Sci USA 84: 595–599

    Article  PubMed  CAS  Google Scholar 

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© 1988 Springer-Verlag Berlin Heidelberg

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Berg, D.K. et al. (1988). Regulation of Neuronal Acetylcholine Receptors by Cell-Cell Interactions. In: Clementi, F., Gotti, C., Sher, E. (eds) Nicotinic Acetylcholine Receptors in the Nervous System. NATO ASI Series, vol 25. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-74167-8_21

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  • DOI: https://doi.org/10.1007/978-3-642-74167-8_21

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-74169-2

  • Online ISBN: 978-3-642-74167-8

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