Ultrastructural localization of the binding fragment of tetanus toxin in putative γ-aminobutyric acidergic terminals in the intermediolateral cell column: A potential basis for sympathetic dysfunction in generalized tetanus

Journal of Comparative Neurology

Volumn 419, Issue 4, 2000, Pages 471-484

  Ligorio, Michael A ^a   Akmentin, Wendy ^a   Gallery, Frances ^a   Cabot, John B ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

Axon terminal; Inhibition; Spinal cord inhibitory neurotransmitter; Sympathetic preganglionic neuron; Transsynaptic transport

Indexed keywords

4 AMINOBUTYRIC ACID; TETANUS TOXIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY SPECIFICITY; ARTICLE; CELL ULTRASTRUCTURE; CONTROLLED STUDY; GABAERGIC TRANSMISSION; IMMUNOHISTOCHEMISTRY; MEAN ARTERIAL PRESSURE; NERVE FIBER TRANSPORT; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; RECEPTOR BINDING; RELIABILITY; STIMULUS RESPONSE; SYMPATHETIC FUNCTION; SYNAPTIC TRANSMISSION; TETANUS;

ANIMALS; CHOLERA TOXIN; GAMMA-AMINOBUTYRIC ACID; MALE; MICROSCOPY, IMMUNOELECTRON; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; SYMPATHETIC NERVOUS SYSTEM; TETANUS TOXIN;

EID: 0034678784     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(20000417)419:4<471::AID-CNE5>3.0.CO;2-H     Document Type: Article

References (88)

1. Backman SB, Henry JL. 1983. Effects of GABA and glycine on sympathetic preganglionic neurons in the upper thoracic intermedioiateral nucleus of the cat. Brain Res 277:365-369.
2. Bacon SJ, Smith AD. 1988. Preganglionic sympathetic neurones innervating the rat adrenal medulla: immunocytochemical evidence of synaptic input from nerve terminals containing substance P, GABA or 5-hydroxytryptamine. J Auton Nerv Syst 24:97-122.
3. Bergey GK, Bigalke H, Nelson PG. 1987. Differential effects of tetanus toxin on inhibitory and excitatory synaptic transmission in mammalian spinal cord neurons in culture: a presynaptic locus of action for tetanus toxin. J Neurophysiol 57:121-131.
4. Betz H. 1998. Gephyrin, a major player in GABAergic postsynaptic membrane assembly? Nat Neurosci 1:541-543.
5. Bigalke H, Heller I, Bizzini B, Habermann E. 1981. Tetanus toxin and botulinum A toxin inhibit release and uptake of various transmitters, as studied with particulate preparations from rat brain and spinal cord. Naunyn Schmiedebergs Arch Pharmacol 316:244-251.
6. Bizzini B. 1989. Axoplasmic transport and transynaptic movement of tetanus toxin. In: Simpson LL, editor. Botulinum neurotoxin and tetanus toxin. New York: Academic Press. p 203-229.
7. Bleck TP. 1989. Clinical aspects of tetanus. In: Simpson LL, editor. Botulinum neurotoxin and tetanus toxin. New York: Academic Press. p 379-398.
8. Began N, Mennone A, Cabot JB. 1989. Light microscopic and ultrastructural localization of GABA-like immunoreactive input to retrogradely labeled sympathetic preganglionic neurons. Brain Res 505:257-270.
9. Britton P, Whitton PS, Bowery NG. 1995. Effect of tetanus toxin on basal and evoked release of 5-hydroxytryptamine and dopamine in rat hippocampus in vivo. Brain Res 673:331-334.
10. Brooks VB, Curtis DR, Eccles JC. 1957. The action of tetanus toxin on the inhibition of motoneurones. J Physiol (London) 135:655-672.
11. Cabot JB. 1990. Sympathetic preganglionic neurons: cytoarchitecture, ultrastructure and biophysical properties. In: Loewy AD, Spyer KM, editors. Central regulation of autonomic functions. New York: Oxford University Press. p 44-67.
12. Cabot JB, Mennone A, Bogan N, Carroll J, Evinger C, Erichsen JT. 1991. Retrograde, trans-synaptic and transneuronal transport of fragment C of tetanus toxin by sympathetic preganglionic neurons. Neuroscience 40:805-823.
13. Cabot JB, Alessi V, Bushnell A. 1992. Glycine-like immunoreactive input to sympathetic preganglionic neurons. Brain Res 571:1-18.
14. Cabot JB, Alessi V, Carroll J, Ligorio M. 1994. Spinal cord lamina V and lamina VII interneuronal projections to sympathetic preganglionic neurons. J Comp Neurol 347:515-530.
15. Cabot JB, Bushnell A, Alessi V, Mendell NR. 1995. Postsynaptic gephyrin immunoreactivity exhibits a nearly one-to-one correspondence with gamma-aminobutyric acid-like immunogold-labeled synaptic inputs to sympathetic preganglionic neurons. J Comp Neurol 356:418-432.
16. Carrea R, Lanari A. 1962. Chronic effect of tetanus toxin applied locally to the cerebral cortex of the dog. Science 137:342-343.
17. Chiba T, Semba R. 1991. Immuno-electronmicroscopic studies on the gamma-aminobutyric acid and glycine receptor in the intermediolateral nucleus of the thoracic spinal cord of rats and guinea pigs. J Auton Nerv Syst 36:173-181.
18. Clendening B, Hume RI. 1990. Expression of multiple neurotransmitter receptors by sympathetic preganglionic neurons in vitro. J Neurosci 10:3977-3991.
19. Collingridge GL, Davies J. 1982. The in vitro inhibition of GABA release by tetanus toxin. Neuropharmacology 21:851-855.
20. Collingridge GL, Thompson PA, Davies J, Mellanby J. 1981. In vitro effect of tetanus toxin on GABA release from rat hippocampal slices. J Neurochem 37:1039-1041.
21. Coote JH. 1988. The organisation of cardiovascular neurons in the spinal cord. Rev Physiol Biochem Pharmacol 110:147-285.
22. Curtis DR, De Groat WC. 1968. Tetanus toxin and spinal inhibition. Brain Res 10:208-212.
23. Curtis DR, Felix D, Game CJA, McCulloch RM. 1973. Tetanus toxin and the synaptic release of GABA. Brain Res 51:358-362.
24. Davies J, Tongroach P. 1979. Tetanus toxin and synaptic inhibition in the substantia nigra and striatum of the rat. J Physiol (London) 290:23-36.
25. Dreyer F. 1989. Peripheral actions of tetanus toxin. In: Simpson LL, editor. Botulinum neurotoxin and tetanus toxin. New York: Academic Press. p 179-202.
26. Dun NJ, Karczmar AG, Wu SY, Shen E. 1993. Putative transmitter systems of mammalian sympathetic preganglionic neurons. Acta Neurobiol Exp 53:53-63.
27. Empson RM, Jefferys JGR. 1993. Synaptic inhibition in primary and secondary chronic epileptic foci induced by intrahippocampal tetanus toxin in the rat. J Physiol (London) 465:595-614.
28. Empson RM, Amitai Y, Jefferys JGR, Gutnick MJ. 1993. Injection of tetanus toxin into the neocortex elicits persistent epileptiform activity but only transient impairment of GABA release. Neuroscience 57:235-239.
29. Essrich C, Lorez M, Benson JA, Fritschy JM, Lüscher B. 1998. Postsynaptic clustering of major GABAA receptor subtypes requires the γ2 subunit and gephyrin. Nat Neurosci 1:563-571.
30. Fishman PS, Carrigan DR. 1987. Retrograde transneuronal transfer of the C-fragment of tetanus toxin. Brain Res 406:275-279.
31. Fishman PS, Carrigan DR. 1988. Motoneuron uptake from the circulation of the binding fragment of tetanus toxin. Arch Neurol 45:558-561.
32. Fishman PS, Savitt JM. 1989. Transsynaptic transfer of retrogradely transported tetanus protein-peroxidase conjugates. Exp Neurol 106: 197-203.
33. Fleiss JL. 1981. Statistical methods for rates and proportions. New York: John Wiley & Sons, Inc.
34. Goldberg RL, Costa T, Habig WH, Kohn LD, Hardegree MC. 1981. Characterization of fragment C and tetanus toxin binding to rat brain membranes. Mol Pharmacol 20:565-570.
35. Halpern JL, Neale EA. 1995. Neurospecific binding, internalization and retrograde axonal transport. Curr Top Microbiol Immunol 195:221-241.
36. Hasséssian H, Prat A, De Champlain J, Couture R. 1991. Regulation of cardiovascular sympathetic neurons by substance P and gamma-aminobutyric acid in the rat spinal cord. Eur J Pharmacol 202:51-60.
37. Hodgson AJ, Penke B, Erdei A, Chubb IW, Somogyi P. 1985. Antisera to gamma-aminobutyric acid. I. Production and characterization using a new model system. J Histochem Cytochem 33:229-239.
38. Hörtnagl H, Brücke T, Hackl JM. 1979. The involvement of the sympathetic nervous system in tetanus. Klin Wochenschr 57:383-389.
39. Hosoya Y, Sugiura Y, Okado N, Loewy AD, Kohno K. 1991. Descending input from the hypothalamic paraventricular nucleus to sympathetic preganglionic neurons in the rat. Exp Brain Res 85:10-20.
40. Inokuchi H, Yoshimura M, Trzebski A, Polosa C, Nishi S. 1992. Fast inhibitory postsynaptic potentials and responses to inhibitory amino acids of sympathetic preganglionic neurons in the adult cat. J Auton Nerv Syst 41:53-60.
41. Janicki PK, Habermann E. 1983. Tetanus and botulinum toxins inhibit and black widow spider venom stimulates the release of methionine-enkephalin-like material in vitro. J Neurochem 41:395-402.
42. Jonas P, Bischofberger J, Sandkühler J. 1998. Corelease of two fast neurotransmitters at a central synapse. Science 281:419-424.
43. Kanda K, Takano K. 1983. Effect of tetanus toxin on the excitatory and the inhibitory post-synaptic potentials in the cat motoneurone. J Physiol (London) 335:319-333.
44. Kirsch J, Wolters I, Triller A, Betz H. 1993. Gephyrin antisense oligonucleotides prevent glycine receptor clustering in spinal neurons. Nature 366:745-748.
45. Lewis DI, Coote JH. 1995. Chemical mediators of spinal inhibition of rat sympathetic neurones on stimulation in the nucleus tractus solitarii. J Physiol (London) 486:483-494.
46. Ligorio MA. 1996. A study of the pathogenesis of tetanus in the sympathetic nervous system. Ph.D. Thesis, State University of New York at Stony Brook.
47. Llewellyn-Smith IJ, Phend KD, Minson JB, Pilowsky PM, Chalmers JP. 1992. Glutamate-immunoreactive synapses on retrogradely-labelled sympathetic preganglionic neurons in rat thoracic spinal cord. Brain Res 581:67-80.
48. Madorin WS, Calaresu FR. 1994. Cardiovascular changes elicited by microinjection of glycine or GABA into the spinal intermediolateral nucleus in urethane-anesthetized rats. Brain Res 634:13-19.
49. Marxen P, Bigalke H. 1989. Tetanus toxin: inhibitory action in chromaffin cells is initiated by specified types of gangliosides and promoted in low ionic strength solution. Neurosci Lett 107:261-266.
50. McMahon HT, Foran P, Dolly JO, Verhage M, Wiegant VM, Nicholls DG. 1992. Tetanus toxin and botulinum toxins type A and B inhibit glutamate, gamma-aminobutyric acid, aspartate and met-enkephalin release from synaptosomes. Clues to the locus of action. J Biol Chem 267:21338-21343.
51. Meckler RL, Baron R, McLachlan EM. 1990. Selective uptake of C-fragment of tetanus toxin by sympathetic preganglionic nerve terminals. Neuroscience 36:823-829.
52. Montecucco C. 1986. How do tetanus and botulinum toxins bind to neuronal membranes? Trends Biochem Sci 11:314-317.
53. Montecucco C, Schiavo G. 1994. Mechanism of action of tetanus and botulinum neurotoxins. Mol Microbiol 13:1-8.
54. Morris NP, Consiglio E, Kohn LD, Habig WH, Hardegree MC, Helting TB. 1980. Interactions of fragments B and C of tetanus toxin with neural and thyroid membranes and with gangliosides. J Biol Chem 255:6071-6076.
55. Nicoll RA, Malenka RC. 1998. A tale of two transmitters. Science 281:360-361.
56. Örnung G, Shupliakov O, Lindà H, Ottersen OP, Storm-Mathisen J, Ulfhake B, Cullheim S. 1996. Qualitative and quantitative analysis of glycine- and GABA-immunoreactive nerve terminals on motoneuron cell bodies in the cat spinal cord: a postembedding electron microscopic study. J Comp Neurol 365:413-426.
57. Örnung G, Ottersen OP, Cullheim S, Ulfhake B. 1998. Distribution of glutamate-, glycine- and GABA-immunoreactive nerve terminals on dendrites in the cat spinal motor nucleus. Exp Brain Res 118:517-532.
58. Osborne RH, Bradford HF. 1973. Patterns of amino acid release from nerve-endings isolated from spinal cord and medulla. J Neurochem 21:407-419.
59. Paar GH, Wellhöner HH. 1973. The action of tetanus toxin on preganglionic sympathetic reflex discharges. Naunyn Schmiedebergs Arch Pharmacol 276:437-445.
60. Parton RG, Ockleford CD, Critchley DR. 1987. A study of the mechanism of internalisation of tetanus toxin by primary mouse spinal cord cultures. J Neurochem 49:1057-1068.
61. Phend KD, Weinberg RJ, Rustioni A. 1992. Techniques to optimize post-embedding single and double staining for amino acid neurotransmitters. J Histochem Cytochem 40:1011-1020.
62. Poulain B. 1994. Molecular mechanism of action of tetanus toxin and botulinum neurotoxins. Pathol Biol 42:173-182.
63. Poulain B, Mochida S, Wadsworth JDF, Weller U, Habermann E. 1990. Inhibition of neurotransmitter release by botulinum neurotoxins and tetanus toxin at Aplysia synapses: role of the constituent chains. J Physiol (Paris) 84:247-261.
64. Price DL, Griffin J, Young A, Peck K, Stocks A. 1975. Tetanus toxin: direct evidence for retrograde intraaxonal transport. Science 188:945-947.
65. Ramírez-León V, Ulfhake B. 1993. GABA-like immunoreactive innervation and dendro-dendritic contacts in the ventrolateral dendritic bundle in the cat S1 spinal cord segment: an electron microscopic study. Exp Brain Res 97:1-12.
66. Rie MA, Wilson RS. 1978. Morphine therapy controls autonomic hyperactivity in tetanus. Ann Intern Med 88:653-654.
67. Schengrund CL, Ringler NJ, DasGupta BR. 1992. Adherence of botulinum and tetanus neurotoxins to synaptosomal proteins. Brain Res Bull 29:917-924.
68. Schengrund CL, DasGupta BR, Hughes CA, Ringler NJ. 1996. Ganglioside-induced adherence of botulinum and tetanus neurotoxins to adducin. J Neurochem 66:2556-2561.
69. Schwab ME, Thoenen H. 1976. Electron microscopic evidence for a transsynaptic migration of tetanus toxin in spinal cord motoneurons: an autnradiographic and morphometric study. Brain Res 105:213-227.
70. Schwab M, Thoenen H. 1977. Selective trans-synaptic migration of tetanus toxin after retrograde axonal transport in peripheral sympathetic nerves: a comparison with nerve growth factor. Brain Res 122:459-474.
71. Seguela P, Geffard M, Buijs RM, Le Moal M. 1984. Antibodies against γ-aminobutyric acid: specificity studies and immunocytochemical results. Proc Natl Acad Sci USA 81:3888-3892.
72. Sherrington CS. 1905. On reciprocal innervation of antagonistic muscles. VIIIth note. Proc R Soc London [Biol] 76:269-297.
73. Simpson LL. 1984. Fragment C of tetanus toxin antagonizes the neuromuscular blocking properties of native tetanus toxin. J Pharmacol Exp Ther 228:600-604.
74. Smiley JF, Goldman-Rakic PS. 1993. Silver-enhanced diaminobenzidine-sulfide (SEDS): a technique for high-resolution immunoelectron microscopy demonstrated with monoamine immunoreactivity in monkey cerebral cortex and caudate. J Histochem Cytochem 41:1393-1404.
75. Somogyi P, Hodgson AJ. 1985. Antisera to gamma-aminobutyric acid. III. Demonstration of GABA in Golgi-impregnated neurons and in conventional electron microscopic sections of cat striate cortex. J Histochem Cytochem 33:249-257.
76. Somogyi P, Hodgson AJ, Chubb IW, Penke B, Erdei A. 1985. Antisera to gamma-aminobutyric acid. II. Immunocytochemical application to the central nervous system. J Histochem Cytochem 33:240-248.
77. Spreafico R, Frassoni C, Arcelli P, De Biasi S. 1994. GABAergic interneurons in the somatosensory thalamus of the guinea-pig: a light and ultrastructural immunocytochemical investigation. Neuroscience 59: 961-973.
78. Storm-Mathisen J, Leknes AK, Bore AT, Vaaland JL, Edminson P, Haug FMS, Ottersen OP. 1983. First visualization of glutamate and GABA in neurones by imniunocytochemistry. Nature 301:517-520.
79. Strack AM, Sawyer WB, Marubio LM, Loewy AD. 1988. Spinal origin of sympathetic preganglionic neurons in the rat. Brain Res 455:187-191.
80. Takano K. 1993. Clinical tetanus: (spinal) disinhibition or not? In: DasGupta BR, editor. Botulinum and tetanus neurotoxins. New York: Plenum Press. p 299-310.
81. Takano K, Kirchner F, Gremmelt A, Matsuda M, Ozutsumi N, Sugimoto N. 1989. Blocking effects of tetanus toxin and its fragment [A-B] on the excitatory and inhibitory synapses of the spinal motoneurone of the cat. Toxicon 27:385-392.
82. Todd AJ, Spike RC, Chong D, Neilson M. 1995. The relationship between glycine and gephyrin in synapses of the rat spinal cord. Eur J Neurosci 7:1-11.
83. Todd AJ, Watt C, Spike RC, Sieghart W. 1996. Colocalization of GABA, glycine, and their receptors at synapses in the rat spinal cord. J Neurosci 16:974-982.
84. Weller U, Taylor CF, Habermann E. 1986. Quantitative comparison between tetanus toxin, some fragments and toxoid for binding and axonal transport in the rat. Toxicon 24:1055-1063.
85. Williamson LC, Fitzgerald SC, Neale EA. 1992. Differential effects of tetanus toxin on inhibitory and excitatory neurotransmitter release from mammalian spinal cord cells in culture. J Neurochem 59:2148-2157.
86. Wright DK, Lalloo UG, Nayiager S, Govender P. 1989. Autonomic nervous system dysfunction in severe tetanus: current perspectives. Crit Care Med 17:371-375.
87. Wu SY, Dun NJ. 1992. Presynaptic GABAB receptor activation attenuates synaptic transmission to rat sympathetic preganglionic neurons in vitro. Brain Res 572:94-102.
88. Yoshimura M, Nishi S. 1982. Intracellular recordings from lateral horn cells of the spinal cord in vitro. J Auton Nerv Syst 6:5-11.