Putative roles for the inducible transcription factor c-fos in the central nervous system: Studies with antisense oligonucleotides

Neurochemistry International

Volumn 31, Issue 3, 1997, Pages 459-475

  Chiasson, Bernard J ^a   Hong, Murray G L ^b   Robertson, Harold A ^b  

^a UNIVERSITY OF TORONTO   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHETAMINE; ANTISENSE OLIGONUCLEOTIDE; PROTEIN C FOS; PSYCHOSTIMULANT AGENT; TRANSCRIPTION FACTOR;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; BRAIN; BRAIN FUNCTION; CENTRAL NERVOUS SYSTEM; CIRCLING BEHAVIOR; CONTROLLED STUDY; ELECTROSTIMULATION; IMMEDIATE EARLY GENE; KINDLING; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROVOCATION TEST;

ANIMALS; BRAIN; CORPUS STRIATUM; DEXTROAMPHETAMINE; NEURONAL PLASTICITY; NEURONS; OLIGONUCLEOTIDES, ANTISENSE; PROTO-ONCOGENE PROTEINS C-FOS; TRANSCRIPTION, GENETIC;

ANIMALIA;

EID: 0030857278     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0197-0186(96)00115-5     Document Type: Article

References (119)

1. Abraham, W. C., Christie, B. R., Logan, B., Lawlor, P. and Dragunow, M. (1994) Immediate early gene expression associated with the persistence of heterosynaptic long-term depression in the hippocampus. Proc. Natt. Acad. Sci. USA 91, 10049-10053.
2. Beretta, S., Robertson, H. A. and Graybiel, A. M. (1993) Neurochemically specialized projection neurons of the striatum respond differently to psychomotor stimulants. Prog. Brain Res. 99, 201-205.
3. Berridge, M. (1986) Second messenger dualism in neuromodulation and memory. Nature 323, 294-295.
4. Bishop, J. M., (1985) Viral Oncogenes. Cell 42, 23-38.
5. Bishop, J. M. (1983) Cellular oncogenes and retroviruses. Annu. Rev. Biochem. 52, 301-354.
6. Brysch, W. and Schlingensiepen, K.-H. (1994) Design and application of antisense oligonucleotides in cell culture, in vivo, and as therapeutic agents. Cell. Mol. Neurobiol. 14, 557-568.
7. Cain, D. P. (1992). Kindling and the amygdala. In The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction, ed. J. P. Aggleton, pp. 539-560. Wiley-Liss, New York.
8. Cain, D. P. (1989) Long-term potentiation and kindling: how similar are the mechanisms? Trends Neurosci. 12, 6-10.
9. Campbell, J. M., Bacon, T. A. and Wickstrom, E. (1990) Oligodeoxynucleoside phosphorothioate stability in subcellular extracts, culture media, sera and cerebrospinal fluid. J. Biochem. Biophys. Meth. 20, 259-267.
10. Chiang, M.-Y., Chan, H., Zounes, M. A., Freier, S. M., Lima, W. F. and Bennett, C. F. (1991) Antisense oligonucleotides inhibit intercellular adhesion molecule 1 expression by two distinct mechanisms. J. Biol. Chem. 266, 18162-18171.
11. Chiasson, B. J., Armstrong, J. N., Hooper, M. L., Murphy, P. R. and Robertson, H. A. (1994) The application of antisense oligonucleotides to the brain: some pitfalls. Cell. Mol. Neurobiol. 14, 507-521.
12. Chiasson, B. J., Dennison, Z. and Robertson, H. A. (1995) Amygdala kindling and immediate-early genes. Mol. Brain Res. 29, 191-199.
13. Chiasson, B. J., Hooper, M. L. and Robertson, H. A. (1992a) Amphetamine induced rotational behavior in nonlesioned rats: A role for c-fos expression in the striatum. Soc. Neurosci. Abstr..
14. Chiasson, B. J., Hooper, M., Murphy, P. R. and Robertson, H. A. (1992) Antisense oligonucleotide eliminates in vivo expression of c-fos in mammalian brain. Eur. J. Pharmacol. Mol. Pharmacol. 227, 451-453.
15. Christy, B., Lau, L. F. and Nathans, D. (1988) A gene activated in mouse 3T3 cells by serum growth factors encodes a protein with "zinc finger" sequences. Proc. Natl. Acad. Sci. USA 85, 7857-7861.
16. Cochran, B. H., Zullo, J., Verma, I. M. and Stiles, C. D. (1984) Expression of the c-fos gene and of a Fos-related gene is stimulated by platelet-derived growth factor. Science (Wash. DC) 226, 1080-1082.
17. Cohen, D. R. and Curran, T. (1988) fra-1 serum inducible, cellular immediate-early gene that encodes a Fos-related antigen. Mol. Cell. Biol. 8, 2063-2069.
18. Cole, A. J., Saffen, D. W., Baraban, J. M. and Worley, P. F. (1989) Rapid increase of an immediate early gone messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340, 474-476.
19. Curran, T. (1988) The fos oncogene. In The Oncogens Handbook, eds E. P. Reddy, A. M. Skalka and T. Curran, vol. 16, pp. 307-325. Elsevier Science B.V., Biomedical Division.
20. Curran, T. and Franza, B. R. (1988) Fos and Jun: The AP-1 connection. Cell 55, 395-397.
21. Curran, T., Gordon, M. B., Rubino, K. L. and Sambucetti, L. C. (1987) Isolation and characterization of the c-fos (rat) cDNA and analysis of post-translational modification in vitro. Oncogene 2, 79-84.
22. Curran, T. and Morgan, J. I. (1995) Fos: An immediate-early transcription factor in neurons. J. Neurobiol. 26, 403-412.
23. Curran, T. and Teich, N. M. (1982) Candidate product of the FBJ murine osteosarcoma virus oncogene: characterization of a 55,000-Dalton phosphoprotein. J. Virol. 42, 114-122.
24. Downs, A. W. and Eddy, N. B. (1932) The effect of repeated doses of cocaine on the rat. J. Pharmacol. Exp. Therap. 46, 199-200.
25. Dragunow, M., Currie, R. W., Faull, R. L. M., Robertson, H. A. and Jansen, K. (1989) Immediate-early genes, kindling and long-term potentiation. Neurosci. Biobehav. Rev. 13, 301-313.
26. Dragunow, M., Lawlor, P. A., Chiasson, B. J. and Robertson, H. A. (1993) Antisense to c-fos suppresses both Fos and Jun B expression in rat striatum and generates apomorphine and amphetamine-induced rotation. Neuroreport 5, 305-306.
27. Dragunow, M., Robertson, H. A. and Robertson, G. S. (1988) Effects of kindled seizures on the induction of c-fos protein(s) in mammalian neurons. Exp. Neurol. 102, 261-263.
28. Dragunow, M. and Robertson, H. A. (1987) Kindling stimulation induces c-fos protein(s) in granule cells of the rat dentate gyrus. Nature 329, 441-442.
29. Dragunow, M., Tse, C., Glass, M. and Lawlor, P. (1994) c-fos antisense reduces expression of Krox 24 in rat caudate and neocortex. Cell. Mol. Neurobiol. 14, 395-405.
30. Eckstein, F. and Gish, G. (1989) Phosphorothioates in molecular biology. Trends Biochem. Sci. 14, 97-100.
31. Gao, W.-Y., Han, F.-S., Storm, C., Egan, W. and Cheng, Y.-C. (1991) Phosphorothioate oligonucleotides are inhibitors of human DNA polymerases and RNase H: Implications for antisense technology. Mol. Pharmacol. 41, 223-229.
32. Gillardon, F., Beck, H., Uhlmann, E., Herdegen, T., Sandkuler, J., Peyman, A. and Zimmermann, M. (1994) Inhibition of c-fos protein expression in rat spinal cord by antisense oligodeoxynucleotide superfusion. Eur. J. Neurosci. 6, 880-884.
33. Goddard, G. V., Mcintyre, D. and Leech, C. (1969) A permanent change in brain function resulting from daily electrical stimulation. Exp. Neurol. 25, 295-330.
34. Goelet, P., Castellucci, V. F., Schacher, S. and Kandel, E. R. (1986) The long and short of longterm memory - a molecular framework. Nature (Lond.) 322, 419-422.
35. Goelet, P. and Kandel, E. R. (1986) Tracking the flow of learned information from membrane receptors to genome. Trends Neurosci. 9, 492-499.
36. Graybiel, A. M., Moratalla, R. and Robertson, H. A. (1990) Amphetamine and cocaine induce drug-specific activation of the c-fos gene in striosome-matrix compartments and limbic subdivisions of the striatum. Proc. Natl Acad. Sci. USA 87, 6912-6916.
37. Guvakova, M. A., Yakubov, L. A., Vlodavsky, I., Tonkinson, J. L. and Stein, C. A. (1995) Phosphorothioate oligodcoxynucleotides bind to basic fibroblast growth factor, inhibit its binding to cell surface receptors, and remove it from low affinity binding sites on extracellular matrix. J. Biol. Chem. 270, 2620-2627.
38. Heilig, M., Pich, E. M., Koob, G. F., Yee, F. and Wahlestedt, C. (1992) In vivo down regulation of neuropeptide Y (NPY) Y1 receptors by icv antisense oligodeoxynucleotide administration is associated with signs of anxiety in rats. Soc. Neurosci. Abstr. 642, 18.
39. Heilig, M., Engel, J. A. and Söderpalm, B. (1993) C-fos antisense in the nucleus accumbens blocks the locomotor stimulant action of cocaine. Eur. J. Pharmacol. 236, 339-340.
40. Hengerer, B., Lindholm, D., Hcumann, R., Ruther, U., Wagner, E. F. and Thoenen, H. (1990) Lesion-induced increase in nerve growth factor mRNA is mediated by c-fos. Proc. Natl. Acad. Sci. 87, 3899-3903.
41. Hirai, S.-I., Ryseck, R.-P. and Mechta, F. (1989) Characterization of jun-D: a new member of the jun proto-oncogene family. EMBO J. 8, 1433-1439.
42. Höllt, V. (1993). Regulation of opioid peptide gene expression. In Handbook of experimental pharmacology. Opioids I, ed. A. Herz, pp. 307-346. Springer-Verlag, Germany.
43. Hooper, M. L., Chiasson, B. I. and Robertson, H. A. (1994) Infusion into the brain of an antisense oligonucleotide to the immediate-early gene c-fos suppresses production of Fos and produces a behavioral effect. Neuroscience 63, 917-924.
44. Hosford, D. A., Simonato, M., Cao, Z., Garcia-Cairasco, N., Silver, J. M., Butler, L., Shin, C. and McNamara, J. O. (1995) Differences in the anatomic distribution of immediate-early gene expression in amygdala and angular bundle kindling development. J. Neurosci. 15, 2513-2523.
45. Hughes, P. and Dragunow, M. (1995) Induction of immediate-early genes and the control of neurotransmitter-regulated gene expression within the nervous system. Pharmacol. Rev. 47, 133-178.
46. Hughes, P., Singleton, K. and Dragunow, M. (1994) MK-801 does not attenuate immediate-early gene expression following an amygdala after discharge. Exp. Neurol. 128, 276283.
47. Hunt, S. P., Pini, A. and Evan, G. (1987) Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature (Lond.) 328, 632-634.
48. Hunter, J. C., Woodbum, V. L., Duricux, C., Pettersson, E. K. E., Poat, J. A. and Hughes, J. (1995) C-fos antisense oligodeoxynucleotide increases formalin-induced nociception and regulates preprodynorphin expression. Neuroscience 65, 485-492.
49. Konradi, C., Kobicrski, L. A., Nguyen, T. V., Hcckers, S. and Hyman, S. E. (1993) The c-AMP-response-clement-binding-protein interacts but Fos protein does not interact, with the proenkephalin enhancer in rat striatum. Proc. Natl. Acad. Sci., USA 90, 7005-7009.
50. Krieg, A. M. (1993) Uptake and efficacy of phosphodiester and modified antisense oligonucleotides in primary cell cultures. Clin. Chem. 39, 710-712.
51. Krieg, A. M., Yi, A.-K., Maison, S., Waldschmidt, T. J., Bishop, G. A., Teasdale, R., Koretzky, G. A. and Klinman, D. M (1995) CpG motifs in bacterial DNA trigger direct B-cell activation. Nature (Lond.) 374, 546-548.
52. Labiner, D. M., Butler, L. S., Cao, Z., Hosford, D. A., Shin, C. and McNamara, J. O. (1993) Induction of c-fos mRNA by kindled seizures: Complex relationship with neuronal burst firing. J. Neurosci. 13, 744-751.
53. Lau, L. F. and Nathans, D. (1987) Expression of a set of growth-regulated immediate-early genes in BALB/c3T3 cells: coordinate regulation with c-fos or c-myc. Proc. Natl. Acad. Sci. USA 4, 1182-1186.
54. Lemaire, P., Revelant, O., Bravo, R. and Charnay, P. (1988) Two mouse genes encoding potential transcription factors with identical DNA-binding domains are activated by growth factors in cultured cells. Proc. Natl. Acad. Sci. USA 85, 4691-4695.
55. Liu, P. K., Salminen, A., He, Y. Y., Jiang, M. H., Xue, J. J., Liu, J. S. and Hsu, C. Y. (1994) Suppression of ischemiainduced fos expression and AP-1 activity by an antisense oligodeoxynucleotide to c-fos mRNA. Ann. Neurol. 36, 566-576.
56. Maki, Y., Bos, T. J., Davis, C., Starbuck, M. and Vogt, P. K. (1987) Avian sarcoma virus 17 carries a new oncogene jun. Proc. Natl. Acad. Sci. USA 84, 2848-2852.
57. Merchant, K. M. (1994) c-fos antisense oligonucleotide specifically attenuates haloperidolinduced increases in neurotensin/neuromedin N mRNA expression in rat dorsal striatum. Mol. Cell. Neurosci. 5, 336-344.
58. Merchant, K. M. and Miller, M. A. (1994) Coexpression of neurotensin and c-fos mRNAs in rat neostriatal neurons following acute haloperidol. Brain Res. Mol. Brain. Res. 23, 271-277.
59. Milbrandt, J. (1987) A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor. Science (Wash. DC) 238, 797-799.
60. Möller, C., Bing, O. and Heilig, M. (1994) c-fos expression in the amygdala: in vivo antisense modulation and role in anxiety. Cell. Mol. Neurobiol. 14, 415-423.
61. Moore, S. D., Madamba, S. G., Schweitzer, P. and Siggins, G. R. (1994) Voltage-dependent effects of opioid peptides on hippocampal CA3 pyramidal neurons in vitro. J. Neurosci. 14, 809-820.
62. Moratalla, R., Robertson, H. A. and Graybiel, A. M. (1992) Dynamic regulation of NGFI-A (zif268, egr1) gene expression in the striatum. J. Neurosci. 12, 2609-2622.
63. Moratalla, R., Vickers, E. A., Robertson, H. A., Cochran, B. H. and Graybiel, A. M. (1993) Coordinate expression of c-fos and junB is induced in the striatum by cocaine. J. Neurosci. 13, 423-433.
64. Morgan, J. I., Cohen, D. R., Hempstead, J. L. and Curran, T. (1987) Mapping patterns of c-fos expression in the central nervous system after seizure. Science (Wash. DC) 237, 192-197.
65. Morgan, J. I. and Curran, T. (1991) Stimulus-transcription coupling in the nervous system: Involvement of the inducible proto-oncogenes fos and jun. Annu. Rev. Neurosci. 14, 421-451.
66. Morris, B. J. and Johnston, H. M. (1995) A role for hippocampal opioids in long-term functional plasticity. Trends Neurosci. 18, 350-355.
67. Naranjo, J. R., Mellström, B., Achaval, M. and Sassone-Corsi, P. (1991) Molecular pathways of pain: fos/jun-mediated activation of noncanonical AP-1 site in the prodynorphin gene. Neuron 6, 606-617.
68. Nellen, W. and Lichtenstein, C. (1993) What makes an mRNA anti-sensitive? Trends Biochem. Sci., vol. 18, pp. 419-423. Elsevier, U.K.
69. Nestler, E. J., Hope, B. T. and Widnell, K. L. (1993) Drug addiction: A model for the molecular basis of neural plasticity. Neuron 11, 995-1006.
70. Nishina, H., Sato, H., Suzuki, T., Sato, N. and Iba, H. (1990) Isolation and characterisation of Fra-2, an additional member of the fos gene family. Proc. Natl. Acad. Sci. USA 87, 3619-3623.
71. 2-like dopamine receptors synergistically activate rotation and c-fos expression in the dopamine-depleted striatum in a rat model of Parkinson's disease. J. Neurosci. 12, 3729-3742.
72. Paul, M. L., Currie, R. W. and Robertson, H. A. (1995) Priming of a D1 dopamine receptor behavioural response is dissociated from striatal immediate-early gene activity. Neurosci. 66, 347-359.
73. Perez, J. R., Li, Y., Stein, A., Majumder, S., van Oorschot, A. and Narayanan, R. (1994) Sequence-independent induction of Spl transcription factor activity by phosphorothioate oligodeoxynucleotides. Proc. Natl. Acad. Sci. Usa 91, 5957-5961.
74. Racine, R. J. (1972) Modification of seizure activity by electrical stimulation: Motor seizure. Electroencephalogr. Clin. Neurophysiol. 38, 281-294.
75. Robertson, G. S., Herrera, D. G., Dragunow, M. and Robertson, H. A. (1989) L-Dopa activates c-fos expression in the striatum of 6-hydroxydopamine-lesioned rats. Europ. J. Pharmacol. 159, 99-100.
76. 1-dopamine receptor agonists selectively activate striatal c-fos independent of rotational behaviour. Brain Res. 503, 346-349.
77. Robertson, G. S. and Robertson, H. A. (1989) Evidence that L-dopa-induced rotational behavior is dependent on both striatal and nigral mechanisms. J. Neurosci. 9, 3326-3331.
78. Robertson, G. S. and Robertson, H. A. (1987) D1 and D2 dopamine agonist synergism: Separate sites of action. Trends Pharmacol. Sci. 8, 295-299.
79. Robertson, G. S., Tetzlaff, W., Bedard, A., St-Jean, M. and Wigle, N. (1995) c-fos mediates antipsychotic-induced neurotensin gene expression in the rodent striatum. Neurosci. 67, 325-344.
80. Robertson, G. S., Vincent, S. R. and Fibiger, H. C. (1992) D1 and D2 dopamine receptors differentially regulate c-fos expression in striatonigral and striatopallidal neurons. Neurosci. 49, 285-296.
81. Robertson, H. A. (1992) Immediate-early genes, neuronal plasticity, and memory. Biochem. Cell Biol. 70, 729-737.
82. Robertson, H. A. (1992) Dopamine receptor interactions: some implications for the treatment of Parkinson's disease. Trends Neurosci. 15, 201-206.
83. Robertson, H. A. and Dragunow, M. (1990) From synapse to genome: the role of immediate-early genes in permanent alterations in the central nervous system. In Current aspects of the neurosciences, ed. N. N. Osborne, pp. 143-157. Macmillan Press.
84. Rossier, J. (1993). Biosynthesis of enkephalin-derived peptides. In Handbook of experimental pharmacology: Opioids I, ed. A. Herz, vol. 104, pp. 423-447. Springer-Verlag, Germany.
85. Rusak, B., Robertson, H. A., Wisden, W. and Hunt, S. P. (1990) Light pulses that shift rhythms induce gene expression in the suprachiasmatic nucleus. Science 248, 1237-1240.
86. Ryder, K., Lanahan, A., Perez-Albuerne, E. and Nathans, D. (1989) Jun-D: a third member of the Jun gene family. Proc. Natl. Acad. Sci. USA 86, 1500-1503.
87. Ryder, K., Lau, L. F. and Nathans, D. (1988) A gene activated by growth factors is related to the oncogene v-jun. Proc. Natl. Acad. Sci. USA 85, 1487-1491.
88. Schlingensiepen, K.-H., Wollnik, F., Kunst, M., Schlingensiepen, R., Herdegen, T. and Brysch, W. (1994) The role of jun transcription factor expression and phosphorylation in neuronal differentiation, neuronal cell death, and plastic adaptations in vivo. Cell. Mol. Neurobiol. 14, 487-505.
89. Sheng, M. and Greenberg, M. E. (1990) The regulation and function of c-fos and other immediate-early genes in the nervous system. Neuron 4, 477-485.
90. Shin, C., McNamara, J. O., Morgan, J. I., Curran, T. and Cohen, D. R. (1990) Induction of c-fos mRNA expression by afterdischarge in the hippocampus of naive and kindled rats. J. Neurochem. 55, 1050-1055.
91. Silvia, C. P., King, G. R., Lee, T. H., Xue, Z.-Y., Caron, M. G. and Ellinwood, E. H. (1994) Intranigral administration of D2 dopamine receptor antisense oligodeoxynucleotides establishes a role for nigrostriatal D2 autoreceptors in the motor actions of cocaine. Mol. Pharmacol. 46, 51-57.
92. Sinomato, M., Hosford, D. A., Labiner, D. M., Shin, C., Mansbach, H. H. and McNamara, J. O. (1991) Differential expression of immediate early genes in the hippocampus in the kindling model of epilepsy. Mol. Brain Res. 11, 115-124.
93. Sommer, W., Bjelke, B., Ganten, D. and Fuxe, K. (1993) Antisense oligonucleotide to c-fos induces ipsilateral rotational behavior to d-amphetamine. Neuroreport 5, 277-280.
94. Sonnenberg, J. L., Rauscher, J. R. III, Morgan, J. I. and Curran, T. (1989) Regulation of proenkephalin by Fos and Jun, Science 246, 1622-1625.
95. Standifer, K. M., Chien, C.-C., Wahlestedt, C., Brown, G. P. and Pasternak, G. W. (1994) Selective loss of d opioid analgesia and binding by antisense oligodeoxynucleotides to a d opioid receptor. Neuron 12, 805-810.
96. Stehelin, D., Varmus, H. E., Bishop, J. M. and Vogt, P. K. (1976) DNA related to the transforming gent(s) of avian sarcoma viruses is present in normal avian DNA. Nature (Lond.) 260, 170-173.
97. Stein, C. A. and Cheng, Y.-C. (1993) Antisense oligonucleotides as therapeutic agents - Is the bullet really magical? Science 261, 1004-1012.
98. Stein, C. A., Subasinghe, C., Shinozuka, K. and Cohen, J. S. (1988) Physicochemical properties of phosphorothioate oligodeoxynucleotides. Nucl. Acids Res. 16, 3209-3221.
99. Sukhatme, V. P., Cao, X., Chang, L. C., Tsai-Morris, C.-H., Stamenkovich, D., Ferreira, P. C.P., Cohen, D. R., Edwards, S. A., Shows, T. B., Curran, T., LeBeau, M. M. and Adamson, E. D. A. (1988) A zinc finger-encoding gene coregulated with c-fos during growth and differentiation and after cellular depolarization. Cell 53, 37-43.
100. Terman, G. W., Wagner, J. J. and Charkin, C. (1994) Kappa opioids inhibit induction of long-term potentiation in the dentate gyrus of the guinea pig hippocampus. J. Neurosci. 14, 4740-4747.
101. Teskey, C. G., Atkinson, B. G. and Cain, D. P. (1991) Expression of the proto-oncogene c-fos following electrical kindling in the rat. Mol. Brain. Res. 11, 1-10.
102. Tseng, L. F. and Collins, K. A. (1994) Antisense oligodeoxynucleotide to a d-opioid receptor given intrathecally blocks I.C.V. administered b-endorphin-induced antinociception in the mouse. Life Sciences 55, 127-131.
103. Ungerstedt, U. (1971) Striatal dopamine release after amphetamine or nerve degeneration revealed by rotational behaviour. Acta Physiol. Scand. (Suppl) 367, 49-68.
104. Ungerstedt, U. (1971) Postsynaptic supersensitivity after 6-hydroxydopamine induced degeneration of the nigro-striatal dopamine system. Acta. Physiol. Scand. (Suppl) 367, 69-93.
105. Wagner, J. J., Terman, G. W. and Chavkin, C. (1993) Endogenous dynorphins inhibit excitatory neurotransmission and block LTP induction in the hippocampus. Nature (Lond.) 363, 451-454.
106. Wagner, R. W. (1994) Gene inhibition using antisense oligodeoxynucleotides. Nature 372, 333-335.
107. Wahlestedt, C. (1994) Antisense oligonucleotide strategies in neuropharmacology. Trends Pharmacol. Sci. 15, 42-46.
108. Wahlestedt, C., Golanov, E., Yamamoto, S., Yee, F., Ericson, H., Yee, H., Inturrisi, C. E. and Reis, D. J. (1993) Antisense oligonucleotides to NMDA-R1 receptor channel protect conical neurons from excitotoxicity and reduce focal ischaemic infarctions. Nature 363, 260-263.
109. Wahlestedt, C., Pich, E. M., Koob, G. F., Yee, F. and Heilig, M. (1993) Modulation of anxiety and neuropeptide Y-Y1 receptors by antisense oligodeoxynucleotides. Science 259, 528-531.
110. Weiss, B., Zhou, L.-W., Zhang, S.-P. and Oin, Z.-H. (1993) Antisense oligodeoxynucleotide inhibits D2 dopaminc receptor-mediated behavior and D2 messenger RNA. Neuroscience 55, 607-612.
111. Whitesell, L., Geselowitz, D., Chavany, C., Fahmy, B., Walbridge, S., Alger, J. R. and Neckers, L. M. (1993) Stability, clearance, and disposition of intraventricularly administered oligodeoxynucleotides: implications for therapeutic application within the central networks system. Proc. Natl. Acad. Sci. USA 90, 4665-4669.
112. Wisden, W., Errington, M. L., Williams, S., Dunnett, S. B., Waters, C., Hitchcock, D., Evan, G., Bliss, T. V. P. and Hunt, S. P. (1990) Differential expression of immediate-early genes in the hippocampus and spinal cord. Neuron 4, 603-614.
113. Wollnik, F., Brysch, W., Uhlmann, E., Gillardon, F., Bravo, R., Zimmermann, M., Schlingensiepen, K. H. and Herdegen, T. (1995) Block of c-fos and jun-B expression by antisense-oligonucleotides inhibits light-induced phase shifts of the mammalian circadian clock. (In press).
114. Woolf, T. M., Jennings, G. B., Rebagliati, M. and Melton, D. A. (1990) The stability, toxicity and effectiveness of unmodified and phosphorothioate antisense oligodeoxynucleotides in Xenopus oocytes and embryos. Nucl. Acids Res. 18, 1763-1769.
115. Woolf, T. M., Melton, D. A. and Jennings, C. G. B. (1992) Specificity of antisense oligonucleotides in vivo (Xenopus oocytes). Proc. Natl. Acad. Sci. USA 89, 7305-7309.
116. Yee, F., Ericson, H., Reis, D. J. and Wahlestedt, C. (1994) Cellular uptake of intracerebroventricularly administered biotin-or digoxigenin-labeled antisense oligodeoxynucleotides in the rat. Cell. Mol. Neurobiol. 14, 475-486.
117. Zerial, M., Toschi, L., Ryseck, R.-P., Schuermann, M., Muller, R. and Bravo, R. (1989) The product of a novel growth factor activated gene, fos-B, interacts with JUN proteins enhancing their DNA binding activity. EMBO J. 8, 805-813.
118. Zhang, M. and Creese, I. (1993) Antisense oligonucleotide reduces brain dopamine D2 receptor: behavioral correlates. Neurosci. Lett. 161, 223-226.
119. Zhou, L. M., Zhang, S. P., Qin, Z. H. and Weiss, B. (1994) In vivo administration of an oligonucleotide antisense to the D2 dopamine receptor messenger RNA inhibits D2 dopamine receptor mediated behavior and the expression of D2 dopamine receptors in mouse striatum. J. Pharmacol. Exp. Ther. 268, 1015-1023.