Ciliary neurotrophic factor may act in target musculature to regulate developmental synapse elimination?

Developmental Neuroscience

Volumn 18, Issue 3, 1996, Pages 185-198

  Jordan, Cynthia L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Neuromuscular development; Neurotrophic factors; Sexually dimorphic development; Spinal nucleus of the bulbocavernosus; Synapse elimination; Synaptic competition

Indexed keywords

CILIARY NEUROTROPHIC FACTOR; TETRAZOLIUM BLUE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; INNERVATION; LEVATOR ANI MUSCLE; MALE; MOTONEURON; MUSCLE CELL; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NEUROMUSCULAR SYNAPSE; NEWBORN; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; RAT; SKELETAL MUSCLE;

EID: 0029815048     PISSN: 03785866     EISSN: 14219859     Source Type: Journal    
DOI: 10.1159/000111407     Document Type: Article

References (87)

1. Arakawa Y. Sendtncr M. Tliocncn H (1990) Survival effect of ciliary neurotrophic factor (CNTF) on chick embryonic motoneurons in culture: Comparison with other neurotrophic factors and cytokines. J Neurosci 10:3507-3515.
2. Balicc-Gordon RJ. Thompson WJ (1988a) Synaptic rearrangements and alterations in motor unit properties in neonatal rat extensor digitorum iongus muscle. J Physiol (Lond) 398:191-210.
3. Barde Y-A (1989) Trophic factors and neuronal survival. Neuron 2: 1525-1534.
4. Betz WJ. Caldwell JH. Rihchcster RR (1980) The effects of partial denervation at birth on the development of muscle fibres and motor units in the rat lumbrical muscle. J Physiol (Lond) 303:265-279.
5. Betz WJ, Ribchcster RR, Ridge RMAP (1990) Competitive mechanisms underlying synapse elimination in the lumbrical muscle of the rat. J Neurobiol 21:1-17.
6. Bixby, JL (1981) Ultrastructural observations on synapse elimination in neonatal rabbit skeletal muscle. J Ncurocytol 10:81-100.
7. Breedlove SM. Arnold AP (1980) Hormone accumulation in a sexually dimorphic motor nucleus of the rat spinal cord. Science 210: 564-566.
8. Brown MC. Holland RL. Hopkins WG (1981) Restoration of focal multiple innervation in rat muscles by transmission block during a critical stage of development. J Physiol (Lond) 318: 355-364.
9. Brown MC, Jansen JKS. Van Essen D (1976) Polyneuronal innervation of skeletal muscle in new-born rats and its elimination during maturation. J Physiol (Lond) 261:387-422.
10. Cabelli R. Hohn JA. Shatz CJ (1995) Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF. Science 267: 1662-1666.
11. Caldwell JH. Ridge MAP (1983): The effects of deaffcrcntation and spinal cord transection on synapse elimination in developing rat muscles. J Physiol (Lond) 339:145-159.
12. Colman H, Lichtman JW (1993) Interactions between nerve and muscle: Synapse elimination at the developing neuromuscular junction. Dev Biol 156:1-10.
13. Curtis R, Adryan KM, Zhu Y, Harkncss PJ. Lindsay RM, DiStcphano PS (1993) Retrograde axonal transport of ciliary neurotrophic factor is increased by peripheral nerve injury. Nature 365: 253-255.
14. Davis S, Aldrich TH, Valenzuela DM. Wong V, Furth ME. Squinto SP, Yancopoulos GD (1991) The receptor for ciliary neurotrophic factor. Science 253:59-63.
15. Davis S. Aldrich TH, Stahl N. Pan L, Taga T, Kishimoto T. Ip NY, Yancopoulos GD (1993a) HFRp and gpl30 as helerodimerizing signal transducers of the tripartite CNTF receptor. Science 260:1805-1808.
16. English AW, Schwartz G (1993) Is there a sensitive period for the effect of ciliary neurotrophic factor on neuromuscular synapse elimination? Soc Neurosci Abstr 19:1099.
17. English AW. Schwartz G (1995) Both basic fibroblast growth factor and ciliary neurotrophic factor promote the retention of polyneuronal innervation of developing skeletal muscle fibers. Dev Biol 169:57-64.
18. Fladby T, Jansen JKS (1987) Postnatal loss of synaptic terminals in the partially denervated mouse soleus muscle. Acta Physiol Scand 129: 73-98.
19. Forger NG, Roberts SL. Wong V, Breedlove SM (1993) Ciliary neurotrophic factor maintains motoneurons and their target muscles in developing rats. J Neurosci 13:4720-4726.
20. Friedman B, Scherer SS, Rudge JS, Helgren M, Morrisey D. McClain J, Wang D. Wiegand SJ. Fruth ME, Lindsay RM, Ip NY (1992) Regulation of ciliary neurotrophic factor expression in myelin-related Schwann cells in vivo. Neuron 9:295-305.
21. Gibbs R. Pfaff DW (1992) Effects estrogen and fimbria/fomix transection on P75NGFR and CliAT expression in the medial septum and diagonal band of Broca. Exp Neurol 116: 23-39.
22. Gurney ME. Kwon YVV (1993) Neurotrophic factors reset the timing of programmed synapse elimination in neonatal muscles. Soc Neurosci Abstr 19:1099.
23. Gurney ME. Yamamoto H. Kwon Y (1992) Induction of motor neuron sprouting in vivo by ciliary' neurotrophic factor and basic fibroblast growth factor. J Neurosci 12: 3241-3247.
24. Hamburger V (1934) The effects of wing bud extirpation on the development of the central nervous system in chick embryos. J Exp Zool 68:449-494.
25. Hamburger V (1939) Motor and sensory hyperplasia following limb-bud transplantation in chick embryos. Physiol Zool 12: 268-284.
26. Helgrcn ME. Squinto SP. Davis HL. Parry DJ. Boulton TG. Heck CS. Zhu Y, Yancopoulos CD. Lindsay RM. DiStefano PS (1994) Trophic effect of ciliary neurotrophic factor on denervated skeletal muscle. Cell 76:493-504.
27. Henderson CE, Huchct M. Changeux JP (1981) Neurite outgrowth from embryonic chicken spinal neurons is promoted by media conditioned by muscle cells. Proc Natl Acad Sci USA 78:2625-2629.
28. Henderson JT. Seniuk NA. Roder JC (1994a) Localization of CNTF immunoreactivity to neurons and astroglia in the CNS. Mol Brain Res 22: 151-165.
29. Henderson JT. Seniuk NA, Richardson PM, Gauldie J. Roder JC (1994b) Systemic administration of ciliary neurotrophic factor induces cachexia in rodents. J Clin Invest 93: 2632-2638.
30. Herrera AA. Werle MJ (1990) Mechanisms of elimination, remodeling, and competition at frog neuromuscular junctions. J Ncurobio! 21: 73-98.
31. Hughes RA. Sendtner M. Thoencn H (1993) Members of several gene families influence survival of rat motoneurons in vitro and in vivo. J Neurosci Res 36:663-671.
32. Ignar-Trowbridge D. Nelson KG. Bidwell MC, Curtis SW, Washburn TF. McLachlan JA, Korach KS (1992) Coupling of dual signaling pathways: Epidermal growth factor action involves the estrogen receptor. Proc Natl Acad Sci USA 89:4658-4662.
33. Ip NY. Nye SI I. Boulton TG. Davis S. Taga T. Li Y. Birren SJ, Yasukawa K. Kishimoto T, Anderson DJ. Stahl N. Yancopoulos GD (1992) CNTF and L1F act on neuronal cells via shared signaling pathways that involve the IL-6 signal transducing receptor component gp130. Cell 69:1121-1132.
34. Ip NY. McClain J. Barrczucta NX, Aldrich TH. Pan L, Li Y, Wiegand SJ, Friedman B, Davis S, Yancopoulos GD (1993) The a component of the CNTF receptor is required for signaling and defines potential CNTF targets in the adult and during development. Neuron 10:89-102.
35. Ip NY. Yancopoulos GD (1994) Neurotrophic factors and their receptors. Ann Neurol 35:13-16.
36. Jansen JKS. Fladby T (1990) The perinatal reorganization of the innervation of skeletal muscle in mammals. Prog Ncurobiol 34:39-90.
37. Jordan CL (1993) Ciliary neurotrophic factor delays synapse elimination in the rat levator ani muscle. Soc Neurosci Abstr 19:1009.
38. Jordan CL (1995) Ciliary neurotrophic factor regulates multiple innervation only during neuromuscular synapse elimination. Soc Neurosci Abstr 20:1538.
39. Jordan CL, Lctinsky MS. Arnold AP (1988) Synapse elimination occurs late in the hormone-sensitive levator ani muscle of the rat. J Neurobiol 19:335-356.
40. Jordan CL. Lctinsky MS. Arnold AP (1989a) The role of gonadal hormones in neuromuscular synapse elimination in rats. I. Androgen delays the loss of multiple innervation in the levator ani muscle. J Neurosci 9:229-247.
41. Jordan CL. Lctinsky MS. Arnold AP (1989b) The role of gonadal hormones in neuromuscular synapse elimination in rats. II. Multiple innervation persists in the adult levator ani after juvenile androgen treatment. J Neurosci 9: 239-247.
42. Jordan CL, Letinsky MS. Arnold AP (1990) Critical period for the androgenic block neuromuscular synapse elimination. J Neurobiol 21: 760-767.
43. Jordan CL. Pawson P. Arnold AP. Grinnell AD (1992) Hormonal regulation of motor unit size and synaptic strength during synapse elimination in the rat levator ani muscle. J Neurosci 12:4447-4459.
44. Jordan CL, Watamura S, Arnold AP(1995) Androgenic. not estrogenic, steroids alter neuromuscular synapse elimination in the rat levator ani. Dev Brain Res 84: 225-232.
45. Koliatsos VE. Clatterbuck RE, Ip NY, Yancopoulos GD. Price DL (1991) Sexually dimorphic vs nondimorphic spinal motor neurons: two peripheral systems with distinct trophic profiles that may respond to different trophic factors. Soc Neurosci Abstr 17:752.
46. Koliatsos VE. Clatterbuck RE. Winslow JW. Cay-oulte Mil. Price DL (1993) Evidence that brain-derived neurotrophic factor as a trophic factor for motoneurons in vivo. Neuron 10: 359-367.
47. Kwon YW, Abbondanzo SJ, Stewart CL, Gurney ME (1994) Synapse withdrawal from developing neuromuscular junctions occurs earlier in LIF deficient transgenic mice. Soc Neurosci Abstr 20:1091.
48. Li L, Oppenheim RW. Lei M, Houenou LJ (1994) Neurotrophic agents prevent motoneuron death following sciatic nerve section in the neonatal mouse. J Neurobiol 25:759-766.
49. Lichtman JW. Balicc-Gordon RJ (1990) Understanding synaptic competition in theory and in practice. J Neurobiol 21:99-106.
50. Lin LFH, Mismer D, Lile JD. Armes LG, Butler ET HI, Vannice JL. Collins F (1989) Purification, cloning and expression of ciliary neurotrophic factor (CNTF). Science 246:1023-1025.
51. Lohof AM. Ip NY. Poo M-M (1993) Potentiation of developing neuromuscular synapses by the neurotrophins NT-3 and BDNF. Nature 363: 350-353.
52. Lubischer JL, Jordan CL. Arnold AP (1992) Transient and permanent effects of androgen treatment during synapse elimination in the levator ani muscle of the rat. J Neurobiol 23:1-9.
53. Masu Y, Wolf E. Holtmann B. Sendtner M. Brem G. Thoenen H (1993) Disruption of the CNTF gene results in the motor neuron degeneration. Nature 365:27-32.
54. Mignatti P. Morimoto T, Rilkin DB (1992) Basic fibroblast growth factor, a protein devoid of secretory signal sequence, is released by cells via a pathway independent of the endoplasmic rcliculum-golgi complex. J Cell Physiol 151: 81-93.
55. Mucsch A. Hartmann E. Rohde K. Rubartclli A. Sitia R. Rapoporl TA (1990) A novel pathway for secretory proteins. Trends Biochcm 15: 86-88.
56. Nordeen EJ. Nordeen KW. Sengclaub DR. Arnold AP (1985) Androgens prevent normally occurring cell death in a sexually dimorphic spinal nucleus. Science 229:671-673.
57. Nurcombe V. Hill MA. Eagleson KL. Bennett MR (1984) Motor neuron survival and neurite extension from spinal cord explants induced by factors released from denervated muscle. Brain Res 291:19-28.
58. Oppenheim RW (1991) Cell death during development of the nervous system. Annu Rev Neurosci 14:453-501.
59. Oppenheim RW. Haverkamp LJ. Prcvette D. McManaman JL. Appel SH (1988) Reduction of naturally occurring motoneuron death in vivo by target-derived neurotrophic factor. Science 240:919-922.
60. Oppenheim RW. Prcvette D. Qin-Wei Y. Collins F. MacDonald J (1991) Control of embryonic motoneuron survival in vivo by ciliary neurotrophic factor. Science 251:1616-1618.
61. Oppenheim RW. Qin-Wei Y. Prcvette D. Yan Q (1992) Brain-derived neurotrophic factor rescues developing avian motoneurons from cell death. Nature 360:755-757.
62. Persson H. Aycr-Lc Lievre C. Sodor O. Villar MJ. Mctsis M. Olson L. Rizcn M. Hokfelt M (1990) Expression of Tnerve growth factor mRNA in sertoli cells down-regulated by testosterone. Science 247:704-707.
63. Purves D (1988) Body and brain: A trophic theory of neural connections. Cambridge. Harvard University Press.
64. Purves D. Snider WD. Voyvodic JT (1988)Trophic regulation of nerve cell morphology and innervation in the autonomic nervous system. Nature 336:123-128.
65. Rende M. Muir D. Ruoslahli E. Hagg T. Varon S. Manthorpc M (1992) lmmunolocalization of ciliary neuronotrophic factor in adult rat sciatic-nerve. Cilia 5:25-32.
66. Riley DA (1981) Ultrastructural evidence for axon retraction during the spontaneous elimination of polyneuronal innervation of the rat solcus muscle. J Neuroeytoi 10:425-440.
67. Rubartelli A, Cozzolino F. Talio M. Sitia R (1990) A novel secretory pathway for interleukin-11. A protein lacking a signal sequence. EMBO J 9:1503-1510.
68. Sendtner M. Kreutzberg GW. Thocnen H (1990) Ciliary neurotrophic factor prevents the degeneration of motor neurons after axotomy. Nature 345:440-441.
69. Sendtner M, Holtman B. Kolbeck R, Thocnen H. Barde YA (1992a) Brain-derived neurotrophic factor prevents the death of motoneurons in newborn rats after nerve section. Nature 360: 757-758.
70. Sendtner M. Schmalbruch H. Stockli KA. Carroll P, Kreutberg GW, Thocnen H (1992b) Ciliary neurotrophic factor prevents degeneration of motor neurons in mouse mutant progressive motor neuronopathy. Nature 358:502-504.
71. Sendtner M, Stockli KA, Thoenen H (1992c) Synthesis and localization of ciliary' neurotrophic factor in the sciatic nerve of the adult rat after lesion and during regeneration. J Cell Biol 118:139-148.
72. Seniuk-Tatton NA, Henderson JT. Roder JC (1994) Neurons express CNTF mRNA in the early postnatal and adult rat brain. J Neurosci Res 41:663-676.
73. Shatz CJ (1990) Impulse activity and the patterning of connections during the CNS development. Neuron 5:745-756.
74. Smith RG. Appel SH (1983) Extracts of skeletal muscle increase neuriie outgrowth and cholinergic activity of fetal rat spinal motor neurons. Science 219:1079-1081.
75. Smith RG, Vaca K, McManaman J, Appel SH (1986) Selective effects of skeletal muscle extracts fractions on motoneuron development in vitro. J Neurosci 6:439-447.
76. Sohrabji F. Miranda RC, Toran-Allerand CD (1994) Estrogen differentially regulates estrogen and nerve growth factor receptor mRNAs in adult sensory neurons. J Neurosci 14: 459-471.
77. Stockli KA, Lillicn LE. Nahcr-Noc M, Breitfeld G, Hughes RA, Raff MC, Thoenen H, Sendtner M (1991) Regional distribution, developmental changes, and cellular localization of CNTF-mRNA and protein in the rat brain. J Cell Biol 115:447-459.
78. Stockli KA, Lottspeich F, Sendtner M, Masia-kowski P. Carroll P, Gotz R, Lindholm D, Thoenen H (1989) Molecular cloning, expression and regional distribution of rat ciliary neurotrophic factor. Nature 342:920-923.
79. Stoop R. Poo M-m (1995) Potentiation of transmitter release by ciliary neurotrophic factor requires somatic signaling. Science 267:695-699.
80. Thoenen H, Hughes RA, Sendtner M (1993) Trophic support of motoneurons: Physiological. pathophysiological, and therapeutic implications. Exp Neurol 124:47-55.
81. Thompson W, Jansen JKS (1977) The extent of sprouting of remaining motor units in partly denervated immature and adult rat soleus muscle. Neuroscience 2:523-535.
82. Thompson W (1985) Activity and synapse elimination at the neuromuscular junction. Cell Mol Neurobiol 5:167-182.
83. Van Essen DC. Gordon H, Soha JM, Fraser SE (1990) Synaptic dynamics at the neuromuscular junction: mechanisms and models. J Neurobiol 21:223-249.
84. Woodward JA, Bonett DG, Brecht M (1990) Introduction to linear models and experimental design. New York, Harcourt Brace & Jovanovich Academic Press.
85. Wright LL. Marchctti D, Pcrcz-Polo JR (1988) Effects of gonadal steroids on nerve growth factor receptors in sympathetic and sensory ganglia of neonatal rats. Int J Dev Neurosci 6:217-222.
86. Yan Q, Elliot J. Snider WD (1992) Brain-derived neurotrophic factor rescues spinal motor neurons from axotomy-induccd cell death. Nature 360:753-755.
87. Zum AD, Werren F (1994) Development of CNS cholinergic neurons in vitro: Selective effects of CNTF and LIF on neurons from mesencephalic cranial motor nuclei. Dev Biol 163: 309-315.