Glutamatergic reinnervation and assembly of glutamatergic synapses in adult rat skeletal muscle occurs at cholinergic endplates

Journal of Neuropathology and Experimental Neurology

Volumn 68, Issue 10, 2009, Pages 1103-1115

  Francolini, Maura ^a   Brunelli, Giorgio ^b   Cambianica, Ilaria ^a   Barlati, Sergio ^b   Barbon, Alessandro ^b   La Via, Luca ^b   Guarneri, Bruno ^b   Boroni, Flora ^b   Lanzillotta, Annamaria ^b   Baiguera, Cristina ^b   Ettorre, Michele ^c   Buffelli, Mario ^c   Spano, Pierfranco ^b   Clementi, Francesco ^a   Pizzi, Marina ^b  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF BRESCIA   (Italy)

^c UNIVERSITY OF VERONA   (Italy)

Author keywords

Acetylcholine receptors; AMPA receptors; Glutamate; Neuromuscular junction; Reinnervation; Spinal cord injury; Synaptic plasticity.

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMPA RECEPTOR; CHOLINERGIC RECEPTOR; PROTEIN GLUR 2; RAPSYN; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CHOLINERGIC ACTIVITY; CONTROLLED STUDY; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IMMUNOREACTIVITY; MALE; MOTOR PERFORMANCE; MUSCLE CELL; MUSCLE REINNERVATION; NERVE TRANSPLANTATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SKELETAL MUSCLE; SPINAL CORD;

ANIMALS; FLUORESCENT ANTIBODY TECHNIQUE; GLUTAMIC ACID; IMMUNOPRECIPITATION; MALE; MICROSCOPY, IMMUNOELECTRON; MOTOR ENDPLATE; MUSCLE PROTEINS; MUSCLE, SKELETAL; NERVE REGENERATION; NEUROMUSCULAR JUNCTION; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; RECEPTORS, AMPA; RECEPTORS, CHOLINERGIC; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 70349756971     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/NEN.0b013e3181b7bfc8     Document Type: Article

References (48)

1. Brunelli G, Spano P, Barlati S, et al. Glutamatergic re-innervation through peripheral nerve graft dictates assembly of glutamatergic synapses at rat skeletal muscle. Proc Natl Acad Sci U S A 2005;102:8752-57
2. Pizzi M, Brunelli G, Barlati S, et al. Glutamatergic innervation of rat skeletal muscle by supraspinal neurons: A new paradigm in spinal cord injury. Curr Opin Neurobiol 2006;16:323-28
3. Rich MM, Lichtman JW. In vivo visualization of pre- and postsynaptic changes during synapse elimination in re-innervated mouse muscle. J Neurosci 1989;9:1781-805
4. Wang S, Kawabuchi M, Zhou CJ, et al. The spatiotemporal characterization of endplate reoccupation, with special reference to the super-imposition patterns of the presynaptic elements and the postsynaptic receptor regions during muscle re-innervation. J Peripher Nerv Syst 2004;9:144-57
5. Mays TA, Sanford JL, Hanada T, et al. Glutamate receptors localize postsynaptically at neuromuscular junctions in mice. Muscle Nerve 2009;39:343-49
6. Phend KD, Weinberg RJ, Rustioni A. Techniques to optimize post-embedding single and double staining for aminoacid neurotransmitters. J Histochem Cytochem 1992;40:1011-20
7. Storm-Mathisen J, Ottersen OP. Immunocytochemistry of glutamate at the synaptic level. J Histochem Cytochem 1990;38:1733-43
8. Hepler JR, Toomim CS, McCarthy D, et al. Characterization of antisera to glutamate and aspartate. J Histochem Cytochem 1988;36:13-22
9. Olivier E, Corvisier J, Pauluis Q, et al. Evidences for glutamatergic tectotectal neurons in the cat superior colliculus: A comparison with GABAergic tectotectal neurons. Eur J Neurosci 2000;12:2354-66
10. Waerhaug O, Ottersen OP. Demonstration of glutamate-like immuno-reactivity at rat neuromuscular junctions by quantitative electron microscopy immunocytochemistry. Anat Embryol 1993;188:501-13
11. Mayhew TM, Lucocq JM, Griffiths G. Relative Labelling Index: A novel stereological approach to test for non-random immunogold labelling of organelles and membranes on transmission electron microscopy thin sections. J Microsc 2002;205:153-64
12. Gottwald E, Muller O, Polten A. Semiquantitative reverse transcription-polymerase chain reaction with the Agilent 2100 Bioanalyzer. Electro-phoresis 2001;22:4016-22
13. Perego C, Vanoni C, Bossi M, et al. The GLT-1 and GLAST glutamate transporters are expressed on morphologically distinct astrocytes and regulated by neuronal activity in primary hippocampal cocultures. J Neurochem 2000;75:1076-84
14. Huang YZ, Wang Q, Won S, et al. Compartmentalized NRG signaling and PDZ domainYcontaining proteins in synapse structure and function. Int J Dev Neurosci 2002;20(3-5):173-85
15. Rinholm JE, Slettalokken G, Marcaggi P, et al. Subcellular localization of the glutamate transporters at the neuromuscular junction in rodents. Neuroscience 2007;145:571-91
16. Sanes JR, Lichtman JW. Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat Rev Neurosci 2001;2:791-805
17. Chen L, Chetkovich DM, Petralia R-S, et al. Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 2000; 408:936-43
18. Maister B, Arvidsson U, Zhang X, et al. Glutamate transporter mRNA and glutamate-like immunoreactivity in spinal motoneurones. Neuro-Report 1993;5:337-40
19. Urazaev AK, Naumenko NV, Nikolsky EE, et al. The glutamate and carbachol effects on the early post-denervation depolarization in rat diaphragm are directed towards furosemide-sensitive chloride transport. Neurosci Res 1999;33:81-86
20. Malomouzh AI, Mukhtarov MR, Nikolsky EE, et al. Glutamate regulation of non-quantal release of acetylcholine in the rat neuromus-cular junction. J Neurochem 2003;85:206-13
21. Berger UV, Carter RE, Coyle JT. The immunocytochemical localization of N-acetylaspartyl glutamate, its hydrolyzing enzyme NAALADase and the NMDAR-1 receptor at a vertebrate neuromuscular junction. Neuro-science 1995;64:847-50
22. Grozdanovich Z, Gossrau R. Co-localization of nitric oxide synathase I (NOS I) and NMDA receptor subunit 1 (NMDAR1) at the neuro-muscular junction in rat and mouse skeletal muscle. Cell Tissue Res 1998;291:57-63
23. Vyskocil F. Early postdenervation depolarization is controlled by acetylcholine and glutamate via nitric oxide regulation of the chloride transporter. Neurochem Res 2003;28(3,4):575-85
24. Pinard A, Levesque S, Vallee J, et al. Glutamatergic modulation of synaptic plasticity at a PNS vertebrate cholinergic synapse. Eur J Neurosci 2003;18:3241-50
25. Herzog E, Landry M, Buhler E, et al. Expression of vesicular glutamate transporters, VGLUT1 and VGLUT2, in cholinergic spinal neurons. Eur J Neurosci 2004;20:1752-60
26. Kraus T, Neuhuber WL, Raab M. Vesicular glutamate transporter 1 immunoreactivity in motor endplates of striated esophageal but not skeletal muscles in the mouse. Neurosci Lett 2004;360:53-56
27. Boulland JL, Qureshi T, Seal RP, et al. Expression of the vesicular glutamate transporters during development indicates the widespread co-release of multiple neurotransmitters. J Comp Neurol 2004;480:264-80
28. Nishimaru H, Restrepo CE, Ryge J, et al. Mammalian motor neurons co-release glutamate and acetylcholine at central synapses. Proc Natl Acad Sci U S A 2005;102:5245-49
29. Levit TA, Salpeter MM. Denervated endplates have a dual population of junctional acetylcholine receptors. Nature 1981;291:239-41
30. Fumagalli G, Balbi S, Cangiano A, et al. Regulation of turnover and number of acetylcholine receptors at neuromuscular junctions. Neuron 1990;4:563-69
31. 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;18:4953-65
32. Akaaboune M, Culican SM, Turney SG, et al. Rapid and reversible effects of activity on acetylcholine receptor density at the neuromuscular junction in vivo. Science 1999;286:503-7
33. Frank E, Gautvik K, Sommerschild H. Persistence of junctional acetylcholine receptors following denervation. Cold Spring Harb Symp Quant Biol 1976;40:275-81
34. Pun S, Sigrist M, Santos AF, et al. An intrinsic distinction in neuromuscular junction assembly and maintenance in different skeletal muscles. Neuron 2002;34:357-70
35. Goldman D, Brenner HR, Heinemann S. Acetylcholine receptor alpha-, beta-, gamma-, and delta-subunit mRNA levels are regulated by muscle activity. Neuron 1988;1:329-33
36. Ma J, Shen J, Garrett JP, et al. Gene expression of myogenic regulatory factors, nicotinic acetylcholine receptor subunits, and GAP-43 in skeletal muscle following denervation in a rat model. J Orthop Res 2007;25: 1498-505
37. Witzemann V, Brenner HR, Sakmann B. Neural factors regulate AChR subunit mRNAs at rat neuromuscular synapses. J Cell Biol 1991;114: 125-41
38. Adams L, Carlson BM, Henderson L, et al. Adaptation of nicotinic acetylcholine receptor, myogenin, and MRF4 gene expression to long-term muscle denervation. J Cell Biol 1995;131:1341-49
39. Fawcett JW, Keynes RJ. Peripheral nerve regeneration. Annu Rev Neurosci 1990;13:43-60
40. Nishizawa T, Yamashia S, McGrath KF, et al. Plasticity of neuro-muscular junction architectures in rat slow and fast muscle fibers following temporary denervation and re-innervation processes. J Muscle Res Cell Motil 2006;27:607-15
41. Osten P, Stern-Bach Y. Learning from stargazin: The mouse, the phenotype and the unexpected. Curr Op Neurobiol 2006;16:275-80
42. Sanford JL, Mays TA, Rafael-Fortney JA. CASK and Dlg form a PDZ protein complex at the mammalian neuromuscular junction. Muscle Nerve 2004;30:164-71
43. Sans N, Racca C, Petralia RS, et al. Synapse-associated protein 97 selectively associates with a subset of AMPA receptors early in their biosynthetic pathway. J Neurosci 2001;21:7506-16
44. Fukata Y, Tzingounis AV, Trinidad JC, et al. Molecular constituents of neuronal AMPA receptors. J Cell Biol 2005;169:399-404
45. Borodinsky LN, Root CM, Cronin JA, et al. Activity-dependent homeostatic specification of transmitter expression in embryonic neurons. Nature 2004;429:523-30
46. Borodinsky LN, Spitzer NC. Activity-dependent neurotransmitter-receptor matching at the neuromuscular junction. Proc Natl Acad Sci USA 2007;104:335-40
47. Spitzer NC, Borodinsky LN. Implications of activity-dependent neurotransmitter-receptor matching. Phil Trans R Soc 2008;363:1393-99
48. Fox MA, Umemori H. Seeking long-term relationship: Axon and target communicate to organize synaptic differentiation. J Neurochem 2006;97: 1215-31