Differential regulation of levels of nicotinic receptor subunit transcripts in adult sympathetic neurons after axotomy

Journal of Neurobiology

Volumn 34, Issue 2, 1998, Pages 164-178

  Zhou, Yuefang ^a   Deneris, Evan ^a   Zigmond, Richard E ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Axotomy; Denervation; Leukemia inhibitory factor; Nerve growth factor; Nicotinic receptor

Indexed keywords

LEUKEMIA INHIBITORY FACTOR; NERVE GROWTH FACTOR; NEUROPEPTIDE Y; NICOTINIC RECEPTOR; RECEPTOR SUBUNIT; TYROSINE 3 MONOOXYGENASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTONOMIC GANGLION; CONTROLLED STUDY; DEAFFERENTATION; DENERVATION; EXPLANT; NERVE FIBER TRANSECTION; NERVE INJURY; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION; RETROGRADE NERVE FIBER TRANSPORT; SUPERIOR CERVICAL GANGLION; SYMPATHETIC NERVE CELL; SYNAPTIC TRANSMISSION;

ANIMALS; AXOTOMY; GENE EXPRESSION REGULATION; GROWTH INHIBITORS; INTERLEUKIN-6; LEUKEMIA INHIBITORY FACTOR; LYMPHOKINES; MALE; MICE; MICE, KNOCKOUT; NERVE GROWTH FACTORS; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NICOTINIC; SUPERIOR CERVICAL GANGLION; SYMPATHETIC NERVOUS SYSTEM; TRANSCRIPTION, GENETIC;

EID: 0031911859     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(19980205)34:2<164::AID-NEU6>3.0.CO;2-0     Document Type: Article

References (74)

1. BANNER, L. R., and PATTERSON, P. H. (1994). Major changes in the expression of the mRNAs for cholinergic differentiation factor/leukemia inhibitory factor and its receptor after injury to adult peripheral nerves and ganglia. Proc. Natl. Acad. Sci. USA 91:7109-7113.
2. BLINZINGER, K., and KREUTZBERG, G. (1968). Displacement of synaptic terminals from regenerating motoneurons by microglial cells. Z. Zellforsch Mikrosk Anat. 85:145-157.
3. BOULTER, J., EVANS, K., GOLDMAN, D., MARTIN, G., TRECO, D., HEINEMANN, S., and PATRICK, J. (1986). Isolation of a cDNA clone coding for a possible neural nicotinic acetylcholine receptor α-subunit. Nature 319:368-374.
4. BOULTER, J., O'SHEA-GREENFIELD, A., DUVOISIN, R. M., CONNOLLY, J., WADA, E., JENSEN, A., GARDNER, P., BALLIVET, M., DENERIS, E., MIKINNON, D., HEINEMANN, S., and PATRICK, J. (1990). α3, α5 and β4: three members of the rat neuronal nicotinic acetylcholine receptor-related gene family form a gene cluster. J. Biol. Chem. 265:4472-4482.
5. BURNSTOCK, G., and COSTA, M. (1975). Adrenergic Neurons: Their Organization, Function and Development in the Peripheral Nervous System. Chapman and Hall, London.
6. CANGIANO, A. (1985). Denervation supersensitivity as a model for the neural control of muscle. Neuroscience 14:963-971.
7. CHEAH, H. T., and GEFFEN, L. B. (1973). Effects of axonal injury on norepinephrine, tyrosine hydroxylase and monoamine oxidase levels in sympathetic ganglia. J. Neurobiol. 4:443-452.
8. CHIEN, S. (1960). Supersensitivity of denervated superior cervical ganglion to acetylcholine. Am. J. Physiol. 198:949-954.
9. CHUN, L. L. Y., and PATTERSON, P. H. (1977). Role of nerve growth factor in the development of rat sympathetic neurons in vitro. J. Cell Biol. 75:694-704.
10. CONROY, W., and BERG, D.K. (1995). Neurons can maintain multiple classes of nicotinic acetylcholine receptors distinguished by different subunit compositions. J. Biol. Chem. 270:4424-4431.
11. CURTIS, R., SCHERER, S. S., SOMOGYI, R., ADRYAN, K. M., IP, N. Y., ZHU, Y., LINDSAY, R. M., and DISTREFANO, P. S. (1994). Retrograde axonal transport of LIF is increased by peripheral nerve injury: correlation with increased LIF expression in distal nerve. Neuron 12:191-204.
12. DENERIS, E. S., CONNOLLY, J., BOULTER, J., WADA, E., WADA, K., SWANSON, L., PATRICK, J., and HEINEMANN, S. (1988). Primary structure and expression of β2: a novel subunit of neuronal nicotinic acetylcholine receptors. Neuron 1:45-54.
13. DENERIS, E. S., CONNOLLY, J., ROGERS, S., and DUVOISIN, R. (1991). Pharmacological and functional diversity of neuronal nicotinic acetylcholine receptors. Trends Pharmacol. Sci. 12:34-39.
14. DUVOISIN, R. M., DENERIS, E. S., PATRICK, J., and HEINEMANN, S. (1989). The functional diversity of the neuronal nicotinic acetylcholine receptors is increased by a novel subunit: β4. Neuron 3:487-496.
15. ELLIOTT, K. J., SACAAN, A. I., RAO, T. S., LLOYD, G. K., and COREY-NAEVE, J. (1996). 6-Hydroxydopamine lesion of rat nigrostriatal dopaminergic neurons differentially affects nicotinic acetylcholine receptor subunit mRNA expression. Soc. Neurosci. Abstr. 21:1527.
16. ESCARY, J. L., PERREAU, J., DUMENIL, D., EZINE, S., and BRULET, P. (1993). Leukemia inhibitory factor is necessary for maintenance for hematopoietic stem cells and thymocyte stimulation. Nature 363:361-364.
17. FALLS, D. L., ROSEN, K. M., CORFAS, G., LANE, W. S., and FISCHBACH, G. D. (1993). ARIA, a protein that stimulates acetylcholine receptor synthesis is a member of the Neu ligand family. Cell 72:801-815.
18. FEDEROFF, H. J., GESCHWIND, M. D., GELLER, A. I., and KESSLER, J. A. (1992). Expression of nerve growth factor in vivo from a defective Herpes simplex virus 1 vector prevents effects of axotomy on sympathetic ganglia. Proc. Natl. Acad. USA 89:1636-1640.
19. FUMAGALLI, L., and DE RENZIS, G. (1980). α-Bungaro-toxin binding sites in the rat superior cervical ganglion are influenced by postganglionic axotomy. Neuroscience 5:611-616.
20. FUMAGALLI, L., DE RENZIS, G., and MIANI, N. (1976). Acetylcholine receptors: number and distribution in intact and deafferented superior cervical ganglion of the rat. J. Neurochem. 27:47-52.
21. GLOSTER, A., and DIAMOND, J. (1995). NGF-dependent and NGF-independent recovery of sympathetic function after chemical sympathectomy with 6-hydroxydopamine. J. Comp. Neurol. 359:586-594.
22. GOULD, A., MORRISON, A., SPROAT, G., WHITE, R. A. H., and KRUMLAUF, R. (1997). Positive cross-regulation and enhancer sharing: two mechanisms for specifying overlapping Hox expression patterns. Gene Dev. 11:900-913.
23. GREEN, R. D. III. (1969). The effect of denervation on the sensitivity of the superior cervical ganglion of the pithed cat. J. Pharmacol. Exp. Ther. 167:143-150.
24. HALVORSEN, S. W., and BERG, D. K. (1986). Identification of a nicotinic acetylcholine receptor subunits with and α-neurotoxin that blocks receptor function. J. Neurosci. 6:3405-3412.
25. HALVORSEN, S. W., and BERG, D. K. (1987). Affinity labeling of neuronal acetylcholine receptor subunits with an α-neurotoxin that blocks receptor function. J. Neurosci. 7:2547-2555.
26. HALVORSEN, S. W., and BERG, D. K. (1989). Specific down-regulation of the α-bungarotoxin binding component on chick autonomic neurons by ciliary neurotrophic factor. J. Neurosci. 9:3673-3680.
27. HALVORSEN, S. W., MALEK, R., WANG, X., and JIANG, N. (1996). Ciliary neurotrophic factor regulates nicotinic acetylcholine receptors on human neuroblastoma cells. Neuropharmacology 35:257-265.
28. HEFTI, F., GNAHN, H., SCHWAB, M. E., and THOENEN, H. (1982). Induction of tyrosine hydroxylase by nerve growth factor and by elevated K+ concentrations in cultures of dissociated sympathetic neurons. J. Neurosci. 2:1554-1566.
29. HENDERSON, L. P., GDOVIN, M. J., LIU, C., GARDNER, P. D., and MAUE, R. A. (1994). Nerve growth factor increased nicotinic ACh receptor gene expression and current density in wild type and protein kinase A-deficient PC12 cells. J. Neurosci. 14:1153-1163.
30. HILL, C. E., and HENDRY, I. A. (1976). Differences in sensitivity to nerve growth factor of axon formation and tyrosine hydroxylase induction in cultured sympathetic neurons. Neuroscience 1:489-496.
31. HU, M., WHITING THEOBALD, N. L., and GARDNER, P. D. (1994). Nerve growth factor increases the transcriptional activity of the rat neuronal nicotinic acetylcholine receptor β4 subunit promoter in transfected PC12 cells. J. Neurochem. 62:392-395.
32. HYATT-SACHS, H., SCHREIBER, R. C., BENNETT, T. A., and ZIGMOND, R. E. (1993). Phenotypic plasticity in adult sympathetic ganglia in vivo: effects of deafferentation and axotomy on the expression of vasoactive intestinal peptide. J. Neurosci. 13:1642-1653.
33. JACOB, M. H., and BERG, D. K. (1983). The ultrastructural localization of α-bungarotoxin binding sites in relation to synapses on chick ciliary ganglion neurons. J. Neurosci. 3:260-271.
34. KESSLER, J. A., and BLACK, I. B. (1979). The role of axonal transport in the regulation of enzyme activity in sympathetic ganglia of adult rats. Brain Res. 171:415-424.
35. KOO, E. H., HOFFMAN, P. N., and PRICE, D. L. (1988). Levels of neurotransmitter and cytoskeletal protein mRNAs during nerve regeneration in sympathetic ganglia. Brain Res. 449:361-363.
36. LEVI-MONTALCINI, R. (1987). The nerve growth factor: 35 years later. Science 237:1154-1162.
37. LIEBERMAN, A. R. (1971). The axon reaction: a review for the principal features of perikaryal responses to axon injury. Int. Rev. Neurosci. 14:49-124.
38. LORING, R. H., DAHM, L. M., and ZIGMOND, R. E. (1985). Localization of α-bungarotoxin binding sites in the ciliary ganglion of the embryonic chick: an autoradiographic study at the light and electron microscopic level. Neuroscience 14:645-660.
39. LORING, R. H., SAH, D. W. Y., LANDIS, S. C., and ZIGMOND, R. E. (1988). The ultrastructural distribution of putative nicotinic receptors on cultured neurons from the rat superior cervical ganglion. Neuroscience 24:1071-1080.
40. 125I-toxin F binding sites on chick ciliary neurons: synaptic localization of a toxin that blocks ganglionic nicotinic receptors. J. Neurosci. 7:2153-2162.
41. LUDLAM, W. H., CHANDROSS, K. J., and KESSLER, J. A. (1995). LIF-and IL-1 β-mediated increases in substance P receptor mRNA in axotomized, explanted or dissociated sympathetic ganglia. Brain Res. 685:12-20.
42. MA, Y., CAMPENOT, R. B., and MILLER, F. D. (1992). Concentration-dependent regulation of neuronal gene expression by nerve growth factor. J. Cell Biol. 117:135-141.
43. MANDELZYS, A., PIE, B., DENERIS, E. S., and COOPER, E. (1994). The developmental increase in ACh current densities on rat sympathetic neurons correlates with changes in nicotinic ACh receptor α-subunit gene expression and occurs independent of innervation. J. Neurosci. 14:2357-2364.
44. MARKS, M. J., PAULY, J. R., GROSS, S. D., DENERIS, E. S., HERMANS-BORGMEYER, I., HEINEMANN, S. F., and COLLINS, A. C. (1992). Nicotine binding and nicotinic receptor subunit RNA after chronic nicotine treatment. J. Neurosci. 12:2765-2784.
45. MATTHEWS, M. R., and NELSON, V. H. (1975). Detachment of structurally intact nerve endings from chromatolytic neurons of rat superior cervical ganglion during the depression of synaptic transmission induced by post-ganglionic axotomy. J. Physiol. Lond. 245:91-135.
46. MCGEHEE, D.S., and ROLE, L. (1995). Physiological diversity of nicotinic acetylcholine receptors expressed by vertebrate neurons. Annu. Rev. Physiol. 57:521-546.
47. MCLACHLAN, E. M., DAVIES, P. J., JOACHIM HABLER, H., and JAMIESON, J. (1997). Ongoing and reflex synaptic events in rat superior cervical ganglion cells. J. Physiol. Lond. 501:165-182.
48. PEARSON, R. C. A., TAYLOR, N., and SNYDER, S. H. (1988). Tubulin messenger RNA: in situ hybridization reveals bilateral increased in hypoglossal and facial nuclei following nerve transection. Brain Res. 463:245-249.
49. PURVES, D. (1975). Functional and structural changes in mammalian sympathetic neurons following interruption of their axons. J. Physiol. Lond. 252:429-463.
50. RAO, M. S., SUN, Y., ESCARY, J. L., PERREAU, J., TRESSER, S., PATTERSON, P. H., ZIGMOND, R. E., BRULET, P., and LANDIS, S. C. (1993a). Leukemia inhibitory factor mediates an injury response but not a target-directed developmental transmitter switch in sympathetic neurons. Neuron 11:1175-1185.
51. RAO, M. S., SUN, Y., VAIDYANATHAN, U., ZIGMOND, R. E., LANDIS, S. C., and ZIGMOND, R. E. (1993b). Regulation of substance P is similar to that of vasoactive intestinal peptide after axotomy or explantation of the rat superior cervical ganglion. J. Neurobiol. 24:571-580.
52. RATHOUZ, M. M., and BERG, D. K. (1994). Synaptic-type acetylcholine receptors raise intracellular calcium levels in neurons by two mechanisms. J. Neurosci. 14:6935-6945.
53. ROGERS, S. W., MANDELZYS, A., DENERIS, E. S., COOPER, E., and HEINEMANN, S. (1992). The expression of nicotinic acetylcholine receptors by PC12 cells treated with NGF. J. Neurosci. 12:4611-4623.
54. ROLE, L. W., and BERG, D. K. (1996). Nicotinic receptors in the development and modulation of CNS synapses. Neuron 16:1077-1085.
55. SARGENT, P. B. (1993). The diversity of neuronal nicotinic acetylcholine receptors. Annu. Rev. Neurosci. 16:403-443.
56. SCHREIBER, R. C., HYATT-SACHS, H., BENNETT, T. A., and ZIGMOND, R. E. (1994). Galanin expression increases in adult rat sympathetic neurons after axotomy. Neuroscience 60:17-27.
57. SCHWARTZ LEVEY, M., BRUMWELL, S. E., and JACOB, M. H. (1995). Innervation and target tissue interactions differentially regulates acetylcholine receptor subunit mRNA levels in developing neurons in situ. Neuron 14:153-162.
58. SEGUELA, P., WADICHE, J., DINELEY-MILLER, K., DANI, J. A., and PATRICK, J. W. (1993). Molecular cloning, functional properties, and distribution of rat brain α7: a nicotinic cation channel highly permeable to calcium. J. Neurosci. 13:596-604.
59. SENBA, E., SIMMONS, D. M., WADA, E., WADA, K., and SWANSON, L. W. (1990). RNA levels of neuronal nicotinic acetylcholine receptor subunits are differentially regulated in axotomized facial motoneurons: an in situ hybridization study. Mol. Brain Res. 8:349-353.
60. SINICROPI, D. V., KAUFFMAN, F. C., and BURT, D. R. (1979). Axotomy in rat sympathetic ganglia: reciprocal effects on muscarinic receptor binding and 6-phosphogluconate dehydrogenase activity. Brain Res. 161:560-565.
61. SUN, Y., RAO, M. S., LANDIS, S. C., and ZIGMOND, R. E. (1992). Depolarization increased vasoactive intestinal peptide-and substance P-like immunoreactivities in cultured neonatal and adult sympathetic neurons. J. Neurosci. 12:3717-3728.
62. SUN, Y., RAO, M. S., ZIGMOND, R. E., and LANDIS, S. C. (1994). Regulation of vasoactive intestinal peptide expression in sympathetic neurons in culture and after axotomy: the role of cholinergic differentiation factor/ leukemia inhibitory factor. J. Neurobiol. 25:415-430.
63. SUN, Y., SHADIACK, A., LANDIS, S., and ZIGMOND, R. (1993). Differential effects of cholinergic differentiation factor/leukemia inhibitory factor (CDF/LIF) and NGF on peptide expression in adult rat superior cervical ganglion. Soc. Neurosci. Abstr. 19:664.
64. SUN, Y., and ZIGMOND, R. (1995). Differential effects of long term and short term NGF treatment on neuropeptide expression in axotomized superior cervical ganglia (SCG) in vivo. Soc. Neurosci. Abstr. 21:1052.
65. SUN, Y., and ZIGMOND, R. (1996). Involvement of leukemia inhibitory factor in the increases in galanin and vasoactive intestinal peptide mRNA and the decreases in neuropeptide Y and tyrosine hydroxylase mRNA after axotomy of sympathetic neurons. J. Neurochem. 67:1751-1760.
66. THOENEN, H., and BARDE, Y. A. (1980). Physiology of nerve growth factor. Physiol. Rev. 60:1284-1335.
67. VERNALLIS, A. B., CONROY, W. G., and BERG, D. K. (1993). Neurons assemble acetylcholine receptors with as many as three kinds of subunits while maintaining subunit segregation among receptor subtypes. Neuron 10:451-464.
68. 2+. Neuron 8:353-362.
69. ZHANG, Z., VIJAYARAGHAVAN, S., and BERG, D. (1994). Neuronal acetylcholine receptors that bind α-bungaro-toxin with high affinity function as ligand-gated ion channels. Neuron 12:167-177.
70. ZHANG, Z. W., COGGAN, J. S., and BERG, D. K. (1996). Synaptic currents generated by neuronal acetylcholine receptors sensitive to α-bungarotoxin. Neuron 17:1231-1240.
71. ZIGMOND, R. E. (1997). LIF, NGF and the cell body response to axotomy. Neuroscientist 3:176-185.
72. ZIGMOND, R. E., and CHALAZONITIS, A. (1979). Long-term effects of preganglionic nerve stimulation on tyrosine hydroxylase activity in the rat superior cervical ganglion. Brain Res. 164:137-152.
73. ZIGMOND, R. E., HYATT-SACHS, H., MOHNEY, R. P., SCHREIBER, R. C., SHADIACK, A. M., SUN, Y., and VACCARIELLO, S. A. (1996). Changes in neuropeptide phenotype after axotomy of adult peripheral neurons and the role of leukemia inhibitory factor. Pers. Dev. Neurobiol. 4:75-90.
74. ZIGMOND, R. E., SHADIACK, A., and SUN, Y. (1995). Antiserum to nerve growth factor (NGF) alters neuropeptide expression in the superior cervical ganglion (SCG) and dorsal root ganglion (DRG) in vivo. Soc. Neurosci. Abstr. 21:1052.