Development of cholinergic terminals around rat spinal motor neurons and their potential relationship to developmental cell death

Journal of Comparative Neurology

Volumn 435, Issue 2, 2001, Pages 171-183

  Wetts, Richard ^a,b   Vaughn, James E ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amyotrophic lateral sclerosis; Apoptosis; Islet; Slice culture; Vesicular acetylcholine transporter

Indexed keywords

ACETYLCHOLINE; ALPHA BUNGAROTOXIN; CHOLINERGIC RECEPTOR; NICOTINIC AGENT; POLYCLONAL ANTIBODY;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CHOLINERGIC SYSTEM; EMBRYO; IMMUNOCYTOCHEMISTRY; MOTONEURON; MOTOR NEURON DISEASE; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD;

ANIMALS; CARRIER PROTEINS; CELL DEATH; CHOLINERGIC ANTAGONISTS; CHOLINERGIC FIBERS; EMBRYO; EMBRYONIC AND FETAL DEVELOPMENT; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE TRANSPORT PROTEINS; MOTOR NEURONS; NERVE ENDINGS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS; VESICULAR TRANSPORT PROTEINS;

EID: 0035948298     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.1200     Document Type: Article

References (78)

1. Annis CM, Edmond J, Robertson RT. 1990. A chemically defined medium for organotypic slice cultures. J Neurnsci Methods 32:63-70.
2. Arvidsson U, Riedl M, Elde R, Meister B. 1997. Vesicular acetylcholine transporter (VAChT) protein; a novel and unique marker for cholinergic neurons in the central and peripheral nervous systems. J Comp Neurol 378:454-467.
3. Barber RP, Phelps PE, Houser CR, Crawford GD, Salvaterra PM, Vaughn JE. 1984. The morphology and distribution of neurons containing choline acetyltransferase in the adult rat spinal cord: an immunocytochemical study. J Comp Neurol 229:329-346.
4. Barber RP, Phelps PE, Vaughn JE. 1991. Generation patterns of immunocytochemically identified cholinergic neurons at autonomic levels of the rat spinal cord. J Comp Neurol 311:509-519.
5. Bejanin S, Cervini R, Mallet J, Berrard S. 1994. A unique gene organization for two cholinergic markers, choline acetyltransferase and a putative vesicular transporter of acetylcholine. J Biol Chem 269:21944-21947.
6. Bergmann M, Lahr G, Mayerhofer A, Gratzl M. 1991. Expression of synaptophysin during the prenatal development of the rat spinal cord: correlation with basic differentiation processes of neurons. Neuroscience 42:569-582.
7. Bernstein JJ, Bernstein ME. 1976. Ventral horn synaptology in the rat. J Neurocytol 5:109-123.
8. Calderó J, Prevette D, Mei X, Oakley RA, Li L, Milligan C, Houenou L, Burek M, Oppenheim RW. 1998. Peripheral target regulation of the development and survival of spinal sensory and motor neurons in the chick embryo. J Neurosci 18:356-370.
9. Clarke PGH, Oppenheim RW. 1995. Neuron death in vertebrate development: in vivo methods. Methods Cell Biol 46:277-321.
10. Connaughton M, Priestley JV, Sofroniew MV, Eckenstein F, Cuello AC. 1986. Inputs to motoneurones in the hypoglossal nucleus of the rat: light and electron microscopic immunocytochemistry for choline acetyltransferase, substance P and enkephalins using monoclonal antibodies. Neuroscience 17:205-224.
11. Cullheim S, Kellerth J-O, Conradi S. 1977. Evidence for direct synaptic interconnections between cat spinal α-motoneurons via the recurrent axon collaterals: a morphological study using intracellular injection of horseradish peroxidase. Brain Res 132:1-10.
12. Cusella-De Angelis MG, Lyons G, Sonnino C, De Angelis L, Vivarelli E, Farmer K, Wright WE, Molinaro M, Bouché M, Buckingham M, Cossu G. 1992. MyoD, myogenin independent differentiation of primordial myoblasts in mouse somites. J Cell Biol 116:1243-1255.
13. D'Costa AP, Prevette DM, Houenou LJ, Wang S, Zackenfels K, Rohrer H, Zapf J, Caroni P, Oppenheim RW. 1998. Mechanisms of insulin-like growth factor regulation of programmed cell death of developing avian motoneurons. J Neurobiol 36:379-394.
14. Drisdel RC, Green WN. 2000. Neuronal α-bungarotoxin receptors are α7 subunit homomers. J Neurosci 20:133-139.
15. Erickson JD, Varoqui H, Schäfer MK-H, Modi W, Diebler M-F, Weihe E, Rand J, Eiden LE, Bonner TI, Usdin TB. 1994. Functional identification of a vesicular acetylcholine transporter and its expression from a "cholinergic" gene locus. J Biol Chem 269:21929-21932.
16. Feany MF, Lee S, Edwards RH, Buckley KM. 1992. The synaptic vesicle protein SV2 is a novel type of transmembrane transporter. Cell 70:861-867.
17. Gillberg P-G, Askmark H, Aquilonius S-M. 1990. Spinal cholinergic mechanisms. Prog Brain Res 84:361-370.
18. Gilmor ML, Nash NR, Roghani A, Edwards RH, Yi H, Hersch SM, Levey AI. 1996. Expression of the putative vesicular acetylcholine transporter in rat brain and localization in cholinergic synaptic vesicles. J Neurosci 16:2179-2190.
19. Gingras J, Cabana T. 1998. The development of synaptophysin-like immunoreactivity in the lumbosacral enlargement of the spinal cord of the opossum Monodelphis domestica. Dev Brain Res 106:211-215.
20. Gingras J, Cabana T. 1999. Synaptogenesis in the brachial and lumbosacral enlargements of the spinal cord in the postnatal opossum, Monodelphis domestica. J Comp Neurol 414:551-560.
21. Hamburger V. 1958. Regression versus peripheral control of differentiation in motor hypoplasia. Am J Anat 102:365-410.
22. Hamburger V, Levi-Montalcini R. 1949. Proliferation, differentiation and degeneration in the spinal ganglia of the chick embryo under normal and experimental conditions. J Exp Zool 111:457-502.
23. Harris AJ, McCaig CD. 1984. Motoneuron death and motor unit size during embryonic development of the rat. J Neurosci 4:13-24.
24. Henrikson CK, Vaughn JE. 1974. Fine structural relationships between neurites and radial glial processes in developing mouse spinal cord. J Neurocytol 3:659-675.
25. Herrup K, Shojaeian-Zanjani H, Panzini L, Sunter K, Mariani J. 1996. The numerical matching of source and target populations in the CNS: the inferior olive to Purkinje cell projection. Dev Brain Res 96:28-35.
26. Hory-Lee F, Frank E. 1995. The nicotinic blocking agents d-tubocurare and α-bungarotoxin save motoneurons from naturally occurring death in the absence of neuromuscular blockade. J Neurosci 15:6453-6460.
27. Houser CR, Crawford GD, Barber RP, Salvaterra PM, Vaughn JE. 1983. Organization and morphological characteristics of cholinergic neurons: an immunocytochemical study with a monoclonal antibody to choline acetyltransferase. Brain Res 266:97-119.
28. Ichikawa T, Shimizu T. 1998. Organization of choline acetyltransferase-containing structures in the cranial nerve motor nuclei and spinal cord of the monkey. Brain Res 779:96-103.
29. Ichikawa T, Ajiki K, Matsuura J, Misawa H. 1997. Localization of two cholinergic markers, choline acetyltransferase and vesicular acetylcholine transporter in the central nervous system of the rat: in situ hybridization histochemistry and immunohistochemistry. J Chem Neuroanat 13:23-39.
30. Ichinose T, Miyata Y. 1998. Recurrent excitation of motoneurons in the isolated spinal cord of newborn rats detected by whole-cell recording. Neurosci Res 31:179-187.
31. Keiger CJ, Prevette D, Oppenheim RW. 1998. Developmental expression of neuronal and muscle nicotinic receptor subunits in chick spinal cord and limb-bud muscle. Soc Neurosci Abstr 24:793.
32. Lagerbäck P-Å, Ronnevi L-O, Cullheim S, Kellerth J-O. 1981. An ultrastructural study of the synaptic contacts of α-motoneurone axon collaterals: I. Contacts in lamina IX and with identified α-motoneurone dendrites in lamina VII. Brain Res 207:247-266.
33. Lance-Jones C. 1982. Motoneuron cell death in the developing lumbar spinal cord of the mouse. Dev Brain Res 4:473-479.
34. Landmesser L. 1992. The relationship of intramuscular nerve branching and synaptogenesis to motoneuron survival. J Neurobiol 23:1131-1139.
35. Landmesser LT, Szente M. 1986. Activation patterns of embryonic chick hind-limb muscles following blockade of activity and motoneurone cell death. J Physiol (Lond) 380:157-174.
36. Lanser ME, Fallon JF. 1987. Development of the brachial lateral motor column in the wingless mutant chick embryo: motoneuron survival under varying degrees of peripheral load. J Comp Neurol 261:423-434.
37. Li C-Y, Ziesmer S, Lazcano-Villareal O. 1987. Use of azide and hydrogen peroxide as an inhibitor for endogenous peroxidase in the immunoperoxidase method. J Histochem Cytochem 35:1457-1460.
38. Li W, Ochalski PAY, Brimijoin S, Jordan LM, Nagy JI. 1995. C-terminals on motoneurons: electron microscope localization of cholinergic markers in adult rats and antibody-induced depletion in neonates. Neuroscience 65:879-891.
39. Mackenzie PJ, Kenner GS, Prange O, Shayan H, Umemiya M, Murphy TH. 1999. Ultrastructural correlates of quantal synaptic function at single CNS synapses. J Neurosci 19:1-7.
40. Matsushita M, Ikeda M. 1973. Propriospinal fiber connections of the cervical motor nuclei in the cat: a light and electron microscope study. J Comp Neurol 150:1-32.
41. McLaughlin BJ. 1972a. The fine structure of neurons and synapses in the motor nuclei of the cat spinal cord. J Comp Neurol 144:429-460.
42. McLaughlin BJ. 1972b. Dorsal root projections to the motor nuclei in the cat spinal cord. J Comp Neurol 144:461-474.
43. McLaughlin BJ. 1972c. Propriospinal and supraspinal projections to the motor nuclei in the cat spinal cord. J Comp Neurol 144:475-500.
44. Melega WP, Howard BD. 1984. Biochemical evidence that vesicles are the source of the acetylcholine released from stimulated PC12 cells. Proc Natl Acad Sci USA 81:6535-6538.
45. Milner LD, Landmesser LT. 1999. Cholinergic and GABAergic inputs drive patterned spontaneous motoneuron activity before target contact. J Neurosci 19:3007-3022.
46. Oppenheim RW. 1986. The absence of significant postnatal motoneuron death in the brachial and lumbar spinal cord of the rat. J Comp Neurol 246:281-286.
47. Oppenheim RW. 1989. The neurotrophic theory and naturally occurring motoneuron death. Trends Neurosci 12:252-255.
48. Oppenheim RW. 1991. Cell death during development of the nervous system. Ann Rev Neurosci 14:453-501.
49. Oppenheim RW, Chu-Wang I-W. 1983. Aspects of naturally-occurring motoneuron death in the chick spinal cord during embryonic development. In: Burnstock G, Vrbova G, editors. Somatic and autonomic nerve-muscle interactions. Amsterdam: Elsevier. p 57-107.
50. Oppenheim RW, Chu-Wang I-W, Foelix RF. 1975. Some aspects of synaptogenesis in the spinal cord of the chick embryo: a quantitative electron microscopic study. J Comp Neurol 161:383-418.
51. Oppenheim RW, Houenou L, Pincon-Raymond M, Powell JA, Rieger F, Standish LJ. 1986. The development of motoneurons in the embryonic spinal cord of the mouse mutant, muscular dysgenesis (mdglmdg): survival, morphology, and biochemical differentiation. Dev Biol 114: 426-436.
52. Oppenheim RW, Prevette D, Houenou LJ, Pincon-Raymond M, Dimitriadou V, Donevan A, O'Donovan M, Wenner P, McKemy DD, Allen PD. 1997. Neuromuscular development in the avian paralytic mutant crooked neck dwarf (cn/cn): further evidence for the role of neuromuscular activity in motoneuron survival. J Comp Neurol 381:353-372.
53. Oppenheim RW, Prevette D, D'Costa A, Wang S, Houenou LJ, McIntosh JM. 2000. Reduction of neuromuscular activity is required for the rescue of motoneurons from naturally occurring cell death by nicotinic-blocking agents. J Neurosci 20:6117-6124.
54. Parsons SM, Prior C, Marshall IG. 1993. Acetylcholine transport, storage, and release. Int Rev Neurobiol 35:279-390.
55. Phelps PE, Barber RP, Houser CR, Crawford GD, Salvaterra PM, Vaughn JE. 1984. Postnatal development of neurons containing choline acetyltransferase in rat spinal cord: an immunocytochemical study. J Comp Neurol 229:347-361.
56. Phelps PE, Barber RP, Brennan LA, Maines VM, Salvaterra PM, Vaughn JE. 1990. Embryonic development of four different subsets of cholinergic neurons in rat cervical spinal cord. J Comp Neurol 291:9-26.
57. Pittman R, Oppenheim RW. 1979. Cell death of motoneurons in the chick embryo spinal cord: IV. Evidence that a functional neuromuscular interaction is involved in the regulation of naturally occurring cell death and the stabilization of synapses. J Comp Neurol 187:425-446.
58. Pullen AH, Martin JE, Swash M. 1992. Ultrastructure of pre-synaptic input to motor neurons in Onufs nucleus: controls and motor neuron disease. Neuropathol Appl Neurobiol 18:213-231.
59. Renshaw G, Rigby P, Self G, Lamb A, Goldie R. 1993. Exogenously administered alpha-bungarotoxin binds to embryonic chick spinal cord: implications for the toxin-induced arrest of naturally occurring motoneuron death. Neuroscience 53:1163-1172.
60. Rieger F, Pincon-Raymond M. 1981. Muscle and nerve in muscular dysgenesis in the mouse at birth: sprouting and multiple innervation. Dev Biol 87:85-101.
61. Roghani A, Feldman J, Kohan SA, Shirzadi A, Gundersen CB, Brecha N, Edwards RH. 1994. Molecular cloning of a putative vesicular transporter for acetylcholine. Proc Natl Acad Sci USA 91:10620-10624.
62. Roghani A, Shirzadi A, Butcher LL, Edwards RH. 1998. Distribution of the vesicular transporter for acetylcholine in the rat central nervous system. Neuroscience 82:1195-1212.
63. Romano SJ, Pugh PC, McIntosh JM, Berg DK. 1997. Neuronal-type acetylcholine receptors and regulation of alpha 7 gene expression in vertebrate skeletal muscle. J Neurobiol 32:69-80.
64. Schäfer MK-H, Eiden LE, Weihe E. 1998. Cholinergic neurons and terminal fields revealed by immunohistochemistry for the vesicular acetylcholine transporter: I. Central nervous system. Neuroscience 84:331-359.
65. Skoff RP, Hamburger V. 1974. Fine structure of dendritic and axonal growth cones in embryonic chick spinal cord. J Comp Neurol 153:107-148.
66. Tanaka H, Landmesser LT. 1986. Cell death of lumbosacral motoneurons in chick, quail, and chick-quail chimera embryos: a test of the quantitative matching hypothesis of neuronal cell death. J Neurosci 6:2889-2899.
67. Tsuchida T, Ensini M, Morton SB, Baldassare M, Edlund T, Jessell TM, Pfaff SL. 1994. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79:957-970.
68. Usiak MF, Landmesser LT. 1999. Neuromuscular activity blockade induced by muscimol and d-tubocurarine differentially affects the survival of embryonic chick motoneurons. J Neurosci 19:7925-7939.
69. Vaughn JE. 1980. Development of synaptic connections in the spinal cord. In: Windle WF, editor: The spinal cord and its reaction to traumatic injury. New York: Marcel Dekker. p 95-123.
70. Vaughn JE, Sims T, Nakashima M. 1977. A comparison of the early development of axodendritic and axosomatic synapses upon embryonic mouse spinal motor neurons. J Comp Neurol 175:79-100.
71. Vogel MW, Sunter K, Herrup K. 1989. Numerical matching between granule and Purkinje cells in Lurcher chimeric mice: a hypothesis for the trophic rescue of granule cells from target-related cell death. J Neurosci 9:3454-3462.
72. Welton J, Stewart W, Kerr R, Maxwell DJ. 1999. Differential expression of the muscarinic m2 acetylcholine receptor by small and large motoneurons of the rat spinal cord. Brain Res 817:215-219.
73. Wetts R, Herrup K. 1983. Direct correlation between Purkinje and granule cell number in the cerebella of Lurcher chimeras and wild-type mice. Dev Brain Res 10:41-47.
74. Wetts R, Vaughn JE. 1998. Differences in developmental cell death between somatic and autonomic motor neurons of rat spinal cord. J Comp Neurol 396:483-492.
75. Wetts R, Phelps PE, Vaughn JE. 1995. Transient and continuous expression of NADPH diaphorase in different neuronal populations of developing rat spinal cord. Dev Dyn 202:215-228.
76. Wu W, Ziskind-Conhaim L, Sweet MA. 1992. Early development of glycine-and GABA-mediated synapses in rat spinal cord. J Neurosci 12:3935-3945.
77. Zieglgänsberger W, Reiter CH. 1974. A cholinergic mechanism in the spinal cord of cats. Neuropharmacology 13:519-527.
78. Ziskind-Conhaim L. 1990. NMDA receptors mediate poly-and monosynaptic potentials in motoneurons of rat embryos. J Neurosci 10:125-135.