Selective reduction in the nicotinic acetylcholine receptor and dystroglycan at the postsynaptic apparatus of mdx mouse superior cervical ganglion

Journal of Neuropathology and Experimental Neurology

Volumn 59, Issue 2, 2000, Pages 103-112

  Zaccaria, M Letizia ^a   De Stefano, M Egle ^a   Gotti, Cecilia ^b   Petrucci, Tamara C ^c   Paggi, Paola ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Axotomy; Dystroglycan; Dystrophin and actin cytoskeleton; Immunoelectron microscopy; Mdx mouse superior cervical ganglion; Neuronal nicotinic acetylcholine receptor

Indexed keywords

DYSTROGLYCAN; NICOTINIC RECEPTOR;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; DUCHENNE MUSCULAR DYSTROPHY; MOUSE; NERVE FIBER TRANSECTION; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; SUPERIOR CERVICAL GANGLION;

EID: 0033967033     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1093/jnen/59.2.103     Document Type: Article

References (60)

1. Hoffman EP, Kunkel LM. Dystrophin abnormalities in Duchenne/Becker muscular dystrophy. Neuron 1989;2:1019-29
2. Emery AEH. Duchenne muscular dystrophy. Oxford, UK: Oxford University Press 1988:99-103
3. Yotsukura T, Sasaki K, Kachi L, Sasaki A, Ishihara T, Ishikawa K. Circadian rhythm and variability of heart rate in Duchenne-type progressive muscular dystrophy. Am. J. Cardiol. 1995;76:947-51
4. Byers TJ, Kunkel LM, Watkins SC. The subcellular distribution of dystrophin in mouse skeletal, cardiac, and smooth muscle. J Cell Biol 1991;115:411-21
5. Henry MD, Campbell KP. Dystroglycan: An extracellular matrix receptor linked to the cytoskeleton. Curr Opin Cell Biol 1986;8: 625-31
6. Carpenter S, Karpati G. Duchenne muscular dystrophy: Plasma membrane loss initiates muscle cell necrosis unless it is repaired. Brain 1979;102:147-61
7. Gillis JM. Membrane abnormalities and Ca homeostasis in muscle of the mdx mouse, an animal model of the Duchenne muscular dystrophy: A review. Acta Physiol Scand 1996;156:397-406
8. Spencer MJ, Croall DE, Tidball JG. Calpains are activated in necrotic fibers from mdx dystrophic mice. J Biol Chem 1995;270: 10909-14
9. Ahn AH, Kunkel LM. The structural and functional diversity of dystrophin. Nature Genet 1993;3:283-91
10. Feener CA, Koenig M, Kunkel LM. Alternative splicing of human dystrophin mRNA generates isoforms at the carboxy terminus. Nature 1989;338:509-11
11. Goreki DC, Monaco AP, Derry JMJ, Walker AP, Barnard EA. Barnard PJ. Expression of four alternative dystrophin transcripts in brain regions regulated by different promoters. Hum Molec Genet 1992;1:505-10
12. Gòreki DC, Barnard EA. Specific expression of G-dystrophin (Dp71) in the brain. NeuroReport 1995;6:893-96
13. Ziff EB. Enlightening the postsynaptic density. Neuron 1997;19: 1163-74
14. Sandrock Jr. AW, Dryer SE, Rosen KM, et al. Maintenance of acetylcholine receptor number by neuregulins at the neuromuscular junction in vivo. Science 1997;276:599-603
15. Bray D, Levin MD, Morton-Firth CJ. Receptor clustering as a cellular mechanism to control sensitivity. Nature 1998;393:85-88
16. Apel ED, Roberds SL, Campbell KP, Merlie JP. Rapsyn may function as a link between the acetylcholine receptor and the agrin-binding dystrophin-associated glycoprotein complex. Neuron 1995;15:115-26
17. Cartaud A, Coutant S, Petrucci TC, Cartaud J. Evidence for in situ and in vitro association between DAG and the subsynaptic 43 K-rapsyn protein: Consequence for acetylcholine receptor clustering at the synapse. J Biol Chem 1998;273:11321-26
18. Kirsch J, Wolters I, Triller A, Betz H. Gepheryn antisense oligonucleotides prevent glycin receptor clustering in spinal neurons. Nature 1993;366:745-48
19. Allison DW, Gelfand VI, Spector I, Craig AM. Role of actin in anchoring postsynaptic receptors in cultured hyppocampal neurons: Differential attachment of NMDA versus AMPA receptors. J Neurosci 1998;18:2423-36
20. Gotti C, Briscini L, Verderio C, Oortgiesen M, Balestra B, Clementi E Native nicotinic acetylcholine receptor in human IMR32 neuroblastoma cells: Functional, immunological and pharmacological properties. Eur J Neurosci 1995;7:2083-92
21. Lindstrom J. Nicotinic acetylcholine receptors in health and disease. Molec Neurobiot 1997;15:193-222
22. Purves D, Lichtman JW. Formation and maintenance of synaptic connections in autonomic ganglia. Physiol Rev 1978:58:821-62
23. Matthews MR. The ultrastructure of junctions in sympathetic ganglia of mammals. In: Elfvin LG, ed. Autonomic ganglia. New York: Wiley, 1983:27-66
24. Sargent PB. The diversity of neuronal nicotinic acetylcholine receptors. Ann Rev Neurosci 1993;16:403-43
25. Role LW, Berg KD Nicotinic receptors in the development and modulation of CNS synapses. Neuron 1996;16:1077-85
26. Gotti C, Fornasari D, Clementi C. Human neuronal nicotinic receptors. Progr Neurobiol 1997;53:199-237
27. Mandelzys A, Pie' B, Deneris ES, Cooper E. The developmental increase in ACh current densities on rat symphatetic neurons correlates with changes in nicotinic ACh receptor a subunit gene expression and occurs independent of innervation. J Neurosci 1994;14:2375-64
28. Rust G, Burgunder JM, Lauterburg TE, Caghelin AB. Expression of neuronal acetylcholine receptor genes in the rat autonomic nervous system. Eur J Neurosci 1994;6:403-43
29. 2+ / calmodulin-dependent kinase pathway. J Neurosci 1995;15:7966-78
30. Zaccaria ML, De Stefano ME, Properzi F, Gotti C, Petrucci TC, Paggi P. Disassembly of the cholinergic postsynaptic apparatus induced by axotomy in mouse sympathetic neurons: The loss of dystrophin and β-dystroglycan immunoreactivity precedes that of the acetylcholine receptor. J Neuropathol Exp Neurol 1998;57:768-79
31. Sicinsky O, Geng Y, Ryder-Cook AS, Barnard EA, Darlison MG, Barnard PJ. The molecular basis of the muscular dystrophy in the mdx mouse: A point mutation. Science 1989;244:1578-80
32. De Stefano ME, Zaccaria ML, Cavaldesi M, Petrucci TC, Medori R, Paggi P. Dystrophin and its isoforms in a sympathetic ganglion of normal and dystrophic mdx mice: immunolocalizalion by electron microscopy and biochemical characterization. Neuroscience 1997;80:613-24
33. Sherratt TG, Vulliamy T, Dubowitz V, Sewry CA, Strong PN. Exon skipping and translation in patients with frameshift deletions in the dystrophin gene. Am J Hum Genet 1993;53:1007-15
34. Khurana TS, Hoffman EP, Kunkel LM. Identification of a chromosome 6 encoded dystrophin-related protein. J Biol Chem 1990;265:16717-20
35. Brancaccio A, Schulthess T, Gesemann M, Engel J. The N-terminal region of alpha-dystroglycan is an autonomous globular domain. Eur J Biochem 1997;246:166-72
36. Rosa G, Ceccarini M, Cavaldesi M, Zini M, Petrucci TC. Localization of the dystrophin binding site at the carboxyl terminus of β-dystroglycan. Biochem Biophys Res Comm 1996;223:272-77
37. Love DR, Hill DF, Dickson G, Spurr NK, et al. An autosomal transcript in skeletal muscle with homology to dystrophin. Nature 1989;339:55-58
38. Tinsley JM, Blake DJ, Roche A, et al. Primary structure of dystrophin-related protein. Nature 1992;360:10-12
39. Deconinck AE, Rafael JA, Skinner JA, et al. Utrophin-dystrophin-deficient mice as a model for Duchenne muscular dystrophy. Cell 1997;90:717-27
40. Ervasti JM, Ohlendeieck K. Kahl SD, Gaver MG, Campbell KP. Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature 1990;345:315-19
41. Ibraghimov-Beskrovnaya O, Ervasti JM, Leveille CJ, Slaughter CA, Sernett SW, Campbell KP. Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 1992;335:696-702
42. Purves D. Functional and structural changes in mammalian sympathetic neurones following interruption of their axons. J Physiol 1975;252:429-63
43. Bonilla E, Samitt CE, Miranda AF, et al. Duchenne muscular dystrophy: Deficiency of dystrophin at the muscle cell surface. Cell 1988;54:447-52
44. Lenk U, Oexle K, Voit T, et al. A cysteine 3340 substitution in the dystroglycan-binding domain of dystrophin associated with Duchenne muscular dystrophy, mental retardation and absence of the ERG b-wave. Hum Molec Genet 1996;5:973-75
45. Vernallis AB, Conroy WG, Berg DK. Neurons assemble acetylcholine receptors with as many as three kinds of subunits while maintaining subunit segregation among receptor subtypes. Neuron 1993;10:451-64
46. Ramcharan EJ, Matthews R. Autoradiographic localization of functional muscarinic receptors in the rat superior cervical sympathetic ganglion reveals an extensive distribution over non-synaptic surface ot neuronal somata, dendrites and nerve endings. Neuroscience 1996;71:797-832
47. Deconinck AE, Potter AC, Tinsley JM, et al. Postsynaptic abnormalities at the neuromuscular junctions of utrophin-deficient mice. J Cell Biol 1997:136:883-94
48. Cull-Candy SG, Miledi R, Trautmann A, Uchitel OD. On the release of transmitter at normal, myasthenia gravis and myastenic syndrome affected human end-plates. J Physiol 1980;299:621-28
49. Plomp JJ, van Kempen G ThH, Molenaar PC. Adaptation of quantal content to decreased postsynaptic sensitivity at single endplates in α-bungarotoxin-treated rats. J Physiol 1992;458:487-99
50. Sacchi O, Perri V. Quantal mechanism of transmitter release during progressive depletion of the presynaptic stores at a ganglionic synapse. The action of hemicholinium-3 and thiamine deprivation. J Gen Physiol 1973;61:342-60
51. Sacchi O. Rossi ML, Canella R, Fesce R. Synaptic current at the rat ganglionic synapse and its interactions with the neuronal voltage-dependent currents. J Neurophysiol 1998;79:727-42
52. Feng G, Steinbach JH, Sanes JR. Rapsyn clusters neuronal acetylcholine receptors but is inessential for formation of an interneuronal cholinergic synapse. J Neurosci 1998;18:4166-76
53. Matthews M, Raisman G. A light and electron microscopic study of the cellular response to axonal injury in the superior cervical ganglion in the rat. Proc R Soc London Ser B 1972;181:43-79
54. Bisby MA, Tetzlaff W. Changes in cytoskeletal protein synthesis following axon injury and during axon regeneration. Mol Neurobiol 1992;6:107-23
55. Kuno M, Llinas R. Alterations of synaptic action in chromatolysed motoneurons of the cat. J Physiol 1979;210:823-38
56. De Stefano ME, Ciori-Luzzato A, Paggi P, Mugnaini E, Toschi G. Ultrastructural alterations induced in quail ciliary neurons by postganglionic nerve crush and by ricinus toxin administration, separately and in combination. Neuroscience 1994;60:999-1020
57. Paggi P, Lasek RJ. Degradation of purified neurofilament subunits by calcium-activated neutral protease: Characterization of the cleavage products. Neurochem Int 1984;6:589-97
58. Iwasaki Y, Iizuka H, Yamamoto T, Konno H, Kadoya S. Alleviation of axonal damage in acute spinal cord injury by a protease inhibitor: Automated morphometric analysis of drug-effects. Brain Res 1985;347:124-26
59. Straub V, Rafael JA, Chamberlain JS, Campbell KP. Animal models for muscular dystrophy show different patterns of sarcolemmal disruption. J Cell Biol 1997;139:375-85
60. Culican SM, Nelson CC, Lichtman JW. Axon withdrawal during synapse elimination at the neuromuscular junction is accompanied by disassembly of the postsynaptic specialization and withdrawal of Schwann cell processes. J Neurosci 1998;18:4953-64