Abstract
- The working hypothesis that neuropeptide gene expression in a neuron is an indicator of that neuron's physiological activity is discussed. 
- Representative examples from the literature are presented to support the hypothesis. 
- Further, we discuss the regulation of expression of two opioid peptides, preproenkephalin and preprodynorphin, in laminae I and II of the spinal cord and in nucleus caudalis of the trigeminal nuclear complex, where they may play a role in pain modulation. 
- The expression of the opioid peptide genes can be induced by both painful and nonnoxious stimuli in neurons in time-dependent and sensory-specific fashions. 
Key words: molecular biology of peptidergic neurons, in situ hybridization, gene expression, preproenkephalin, preprodynorphin
References
- Akil, H., Watson, S. J., Young, E., Lewis, M. E., Khachaturian, H., and Walker, J. M. (1984). Endogenous opioids: Biology and function.Annu. Rev. Neurosci.7223–255. [DOI] [PubMed] [Google Scholar]
- Andrisani, O. M., Zhu, Z., Pot, D. A., and Dixon, J. E. (1989). In vitro transcription directed from the somatostatin promoter is dependent upon a purified 43-kDa-binding protein.Proc. Natl. Acad. Sci. USA862181–2185. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Angulo, J. A., Davis, L. G., Burkhart, B. A., and Christoph, G. R. (1986). Reduction of striatal dopaminergic neurotransmission elevates striatal proenkephalin mRNA.Eur. J. Pharm.130341–343. [DOI] [PubMed] [Google Scholar]
- Aronin, U., DiFiglia, M., Liotta, A. S., and Martin, J. B. (1981). Ultrastructural localization and biochemical features of immunoreactive leu-enkephalin in monkey dorsal horn.J. Neurosci.1561–567. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Arvidsson, J., and Ygge, J. (1986). A quantitative study of the effects of neonatal capsaicin treatment and of subsequent peripheral nerve transection in the adult rat.Brain Res.397130–136. [DOI] [PubMed] [Google Scholar]
- Atchison, M. L. (1988). Enhancers: Mechanisms of action and cell specificity.Annu. Rev. Cell Biol.4127–153. [DOI] [PubMed] [Google Scholar]
- Baldino, F., Jr., and Davis, L. G. (1986). Glucocorticoid regulation of vasopressin messenger RNA. In Uhl, G. R. (ed.), In SituHybridization in Brain, Plenum Press, New York, pp. 97–116. [Google Scholar]
- Baldino, F., Jr., Fitzpatrick-McElligott, S., O'Kane, T. M., and Gozes, I. (1988a). Hormonal regulation of somatostatin messenger RNA.Synapse2317–325. [DOI] [PubMed] [Google Scholar]
- Baldino, F., Jr., O'Kane, T. M., Fitzpatrick-McElligott, S., and Wolfson, B. (1988b). Coordinate hormonal and synaptic regulation of vasopressin messenger RNA.Science241978–981. [DOI] [PubMed] [Google Scholar]
- Barber, R. P., Vaughn, J. E., Slemmon, J. R., Salvaterra, P. M., Roberts, E., and Leeman, S. E. (1979). The origin, distribution and synaptic relationships of substance P axons in rat spinal cord.J. Comp. Neurol.184331–352. [DOI] [PubMed] [Google Scholar]
- Barinaga, M., Bilezikjian, L. M., Vale, W. W., Rosenfeld, M. G., and Evans, R. M. (1989). Independent effects of growth hormone releasing factor on growth hormone release and gene transcription.Nature314279–281. [DOI] [PubMed] [Google Scholar]
- Basbaum, A. I., and Fields, H. L. (1984). Endogenous pain control system: Brainstem spinal pathways and endorphin circuitry.Annu. Rev. Neurosci.7309–338. [DOI] [PubMed] [Google Scholar]
- Beal, J. A., and Knight, D. S. (1987). Classification of aberrant primary afferents in the substantia gelatinosa of the rat following neonatal capsaicin treatment.Neurosci. Lett.74139–144. [DOI] [PubMed] [Google Scholar]
- Belasco, J. G., and Higgins, C. F. (1988). Mechanisms of mRNA decay in bacteria: A perspective.Gene7215–23. [DOI] [PubMed] [Google Scholar]
- Belasco, J. G., Nilsson, G., von Gabain, A., and Cohen, S. N. (1986). The stability of E. coli gene transcripts is dependent on determinants localized to specific mRNA segments.Cell46245–251. [DOI] [PubMed] [Google Scholar]
- Bennett, G. J., Hayashi, H., Abdelmoumene, M., and Dubner, R. (1979). Physiological properties of stalked cells of the substantia gelatinosa intracellularly stained with horseradish peroxidase.Brain Res.164285–289. [DOI] [PubMed] [Google Scholar]
- Bennefitt, G. J., Abdelmoumene, H., Hayashi, H., and Dubner, R. (1980). Physiology and morphology of substantia gelatinosa neurons intracellularly stained with horseradish peroxidase.J. Comp. Neurol.194809–827. [DOI] [PubMed] [Google Scholar]
- Bennett, G. J., Ruda, M. A., Gobel, S., and Dubner, R. (1982). Enkephalin immunoreactive stalked cells and lamina IIb islet cells in cat substantia gelatinosa.Brain Res.240162–166. [DOI] [PubMed] [Google Scholar]
- Bernstein, P., Peltz, S. W., and Ross, J. (1989). The poly(A)-poly(A)-binding protein complex is a major determinant of mRNA stability in vitro.Mol. Cell. Biol.9(2):659–670. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Botticelli, L. J., Cox, B. M., and Goldstein, A. (1981). Immunoreactive dynorphin in mammalian spinal cord and dorsal root ganglia.Proc. Natl. Acad. Sci. USA787783–7786. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brent, G. A., Larsen, P. R., Harney, J. W., Koenig, R. J., and Moore, D. D. (1989). Functional characterization of the rat growth hormone promoter elements required for induction by thyroid hormone with and without a co-transfected B type thyroid hormone receptor.J. Biol. Chem.264(1):178–182. [PubMed] [Google Scholar]
- Bruhn, T. O., Sutton, R. E., Rivier, C. L., and Vale, W. W. (1984). Corticotropin-releasing factor regulates proopiomelanocortin messenger ribonucleic acid levels in vivo.Neuroendocrinology39170–175. [DOI] [PubMed] [Google Scholar]
- Burbach, J. P., DeHoop, M. J., Schmale, H., Richter, D., De Kloet, R., Ten Haaf, J. A., and De Wied, D. (1984). Differential responses to osmotic stress of vasopressin-neurophysin mRNA in hypothalamic nuclei.Neuroendocrinology39582–584. [DOI] [PubMed] [Google Scholar]
- Burbach, J. P. H., Liu, B., Voorhuis, T. A. M., and Van Tol, H. H. M. (1988). Diurnal variation in vasopressin and oxytocin messenger RNAs in hypothalamic nuclei of the rat.Mol. Br. Res.4157–160. [DOI] [PubMed] [Google Scholar]
- Campbell, D. J., and Habener, J. F. (1986). Angiotensinogen gene is expressed and differentially regulated in multiple tissues of the rat.J. Clin. Invest.7831–39. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carlton, S. M., McNeill, D. L., Chung, K., and Coggeshall, R. E. (1987). A light and electron microscopic level analysis of calcitonin gene-related peptide (CGRP) in the spinal cord of the primate: An immunohistochemical study.Neurosci. Lett.82145–150. [DOI] [PubMed] [Google Scholar]
- Cervero, F., and Iggo, A. (1980). The substantia gelatinosa of the spinal cord. A critical review.Brain103717–772. [DOI] [PubMed] [Google Scholar]
- Cervero, F., and McRitchie, H. A. (1981). Neonatal capsaicin and thermal nociception: A paradox.Brain Res.215414–418. [DOI] [PubMed] [Google Scholar]
- Chan-Palay, V., and Palay, S. L. (1977). Ultrastructural identification of substance P cells and their processes in rat sensory ganglia and their terminals in the spinal cord by immunocytochemistry.Proc. Natl. Acad. Sci. USA744050–4054. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Charnay, Y., Christian, P., Dray, F., and Dubois, P.-M. (1984). Distribution of enkephalin in human fetus and infant spinal cord: An immunofluorescence study.J. Comp. Neurol.223415–423. [DOI] [PubMed] [Google Scholar]
- Cho, H. J., and Basbaum, A. I. (1988). Increased staining of immunoreactive dynorphin cell bodies in the deafferented spinal cord of the rat.Neurosci. Lett.84125–130. [DOI] [PubMed] [Google Scholar]
- Cleveland, D. W. (1988). Autoregulated instability of tubulin mRNAs: A novel eukaryotic regulatory mechanism.TIBS13339–343. [DOI] [PubMed] [Google Scholar]
- Comb, M., Birnberg, N. C., Seasholtz, A., Herbert, E., and Goodman, H. M. (1986). A cyclic AMP-and phorbol ester-inducible DNA element.Nature323353–356. [DOI] [PubMed] [Google Scholar]
- Comb, M., Mermod, N., Hyman, S. E., Pearlberg, J., Ross, M. E., and Goodman, H. M. (1988). Proteins bound at adjacent DNA elements act synergistically to regulate human proenkephalin cAMP inducible transcription.EMBO7(12):3793–3805. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cote, G. J., and Gagel, R. F. (1986). Dexamethasone differentially affects the levels of calcitonin and calcitonin gene-related peptide mRNAs expressed in a human medullary thyroid carcinoma cell line.J. Biol. Chem.26115524–15528. [PubMed] [Google Scholar]
- Cruz, L., and Basbaum, A. I. (1985). Multiple opioid peptides and the modulation of pain: Immunohistochemical analysis of dynorphin and enkephalin in the trigeminal nucleus caudalis and spinal cord of the cat.J. Comp. Neurol.240331–348. [DOI] [PubMed] [Google Scholar]
- Cuello, A. C., and Kanazawa, I. (1978). The distribution of substance P immunoreactive fibers in the rat central nervous system.J. Comp. Neurol.178129–156. [DOI] [PubMed] [Google Scholar]
- Cuello, A. C., DelFiacco, M., and Paxinos, G. (1978). The central and peripheral ends of the substance P-containing sensory neurons in the rat trigeminal system.Brain Res.152499–509. [DOI] [PubMed] [Google Scholar]
- Cuello, A. C., Gamse, R., Holzer, P., and Lembeck, F. (1981). Substance P immuno-reactive neurons following neonatal administration of capsaicin.Naunyn-Schmiedeberg Arch. Pharmacol.345185–194. [DOI] [PubMed] [Google Scholar]
- Danoff, A., and Shields, D. (1988). Differential translation of two distinct preprosomatostatin messenger RNAs.J. Biol. Chem.263(31):16461–16466. [PubMed] [Google Scholar]
- Davis, L. G., Arentzen, R., Reid, J. M., Manning, R. W., Wolfson, B., Lawrence, K. L., and Baldino, F., Jr. (1986). Glucocorticoid sensitivity of vasopressin mRNA levels in the paraventricular nucleus of the rat.Proc. Natl. Acad. Sci.831145–1149. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DeLanerolle, N. C., and LaMotte, C. C. (1982). The human spinal cord: Substance P and methionine-enkephalin immunoreactivity.J. Neurosci.21369–1386. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DeLanerolle, N. C., and LaMotte, C. C. (1983). Ultrastructure of chemically defined neuron systems in the dorsal horn of the monkey. I. Substance P immunoreactivity.Brain Res.27431–49. [DOI] [PubMed] [Google Scholar]
- DelFiacco, M., and Cuello, A. C. (1980). Substance P- and enkephalin-containing neurons in the rat trigeminal system.Neuroscience5803–815. [DOI] [PubMed] [Google Scholar]
- Diamond, D. J., and Goodman, H. M. (1985). Regulation of growth hormone messenger RNA synthesis by dexamethasone and triiodothyronine: Transcriptional rate and mRNA stability changes in pituitary tumor cells.J. Mol. Biol.18141–62. [DOI] [PubMed] [Google Scholar]
- DiGiulio, A. M., Borella, F., Mantegazza, P., Hong, J.-S., Panozzo, C., Zanoni, R., and Gorio, A. (1985a). Structural and biochemical alterations in the dorsal horn of the spinal cord caused by peripheral nerve lesions.Peptides6249–256. [DOI] [PubMed] [Google Scholar]
- DiGiulio, A. M., Mantegazza, P., Dona, M., and Gorio, A. (1985b). Peripheral nerve lesions cause simultaneous alterations of substance P and enkephalin levels in the spinal cord.Brain Res.342405–408. [DOI] [PubMed] [Google Scholar]
- Dobner, P. R., Tischler, A. S., Lee, Y. C., Bloom, S. R., and Donahue, S. R. (1988). Lithium dramatically potentiates neurotensin/neuromedin N gene expression.J. Biol. Chem.26313983–13986. [PubMed] [Google Scholar]
- Douglass, J., Civelli, O., and Herbert, E. (1984). Polyprotein gene expression: Generation of diversity of neuroendocrine peptides.Annu. Rev. Biochem.53665–715. [DOI] [PubMed] [Google Scholar]
- Dubner, R., and Bennett, G. J. (1983). Spinal and trigeminal mechanisms of nociception.Annu. Rev. Neurosci.6381–418. [DOI] [PubMed] [Google Scholar]
- Eberwine, J. H., and Roberts, J. L. (1984). Glucocorticoid regulation of pro-opiomelanocortin gene transcription in the rat pituitary.J. Biol. Chem.2592166–2170. [PubMed] [Google Scholar]
- Elde, R., Hokfelt, T., Johansson, O., and Terenius, L. (1976). Immunohistochemical studies using antibodies to leucine-enkephalin: Initial observations on the nervous system of the rat.Neuroscience1349–351. [DOI] [PubMed] [Google Scholar]
- Emson, P. C. (ed.) (1983).Chemical Neuroanatomy, Raven Press, New York. [Google Scholar]
- Faccini, E., Uzumaki, H., Govoni, S., Missale, C., Spano, P. F., Covelli, V., and Trabucchi, M. (1984). Afferent fibers mediate the increase of metenkephalin elicited in rat spinal cord by localized pain.Pain1825–31. [DOI] [PubMed] [Google Scholar]
- Fallon, J. H., and Leslie, F. M. (1986). Distribution of dynorphin and enkephalin peptides in the rat brain.J. Comp. Neurol.249293–336. [DOI] [PubMed] [Google Scholar]
- Fink, J. S., Verhave, M., Kasper, S., Tsukada, T., Mandel, G., and Goodman, R. H. (1988). The CGTA sequence motif is essential for biological activity of the vasoactive intestinal peptide gene cAMP-regulated enhancer.Proc. Natl. Acad. Sci. USA856662–6666. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Finley, J. C. W., Maderdrut, J. L., and Petrusz, P. (1981). The immunocytochemical localization of enkephalin in the central nervous system of the rat.J. Comp. Neurol.198541–565. [DOI] [PubMed] [Google Scholar]
- Fisher, J. M., and Scheller, R. H. (1988). Prohormone processing and the secretory pathway.J. Biol. Chem.263(32):16515–16518. [PubMed] [Google Scholar]
- Fisher, J. M., Sossin, W., Newcomb, R., and Scheller, R. H. (1988). Multiple neuropeptides derived from a common precursor are differentially packaged and transported.Cell54813–822. [DOI] [PubMed] [Google Scholar]
- Fischer-Colbrie, R., Iacangelo, A., and Eiden, L. E. (1988). Neural and humoral factors separately regulate neuropeptide Y, enkephalin, and chromogranin A and B mRNA levels in rat adrenal medulla.Proc. Natl. Acad. Sci.853240–3244. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fitzgerald, M. (1983). Capsaicin and sensory neurones. A review.Pain15109–130. [DOI] [PubMed] [Google Scholar]
- Fuller, R. S., Brake, A., and Thorner, J. (1989). Yeast prohormone processing enzyme (KEX2 gene product) is a Ca2+-dependent serine protease.Biochemistry861434–1438. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gainer, H. (1981). The biology of neurosecretory neurons. InNeurosecretion and Brain Peptides (J. B. Martin, S. Reichlin, and K. L. Bick, Eds.), Raven Press, New York, pp. 5–20. [Google Scholar]
- Gamse, R. (1982). Capsaicin and nociception in the rat and mouse.Naunyn-Schmiedeberg Arch. Pharmacol.320205–216. [DOI] [PubMed] [Google Scholar]
- Gibson, S. J., Polak, J. M., Bloom, S. R., Sabate, I. M., Mulderry, P. M., Ghatei, M. A., McGregor, G. P., Morrison, J. F. B., Kelly, J. S., Evans, R. M., and Rosenfeld, M. G. (1984). Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and eight other species.J. Neurosci.43101–3111. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Glazer, E. J., and Basbaum, A. I. (1981). Immunohistochemical localization of leucine-enkephalin in the spinal cord of the cat: Enkephalin-containing marginal neurons and pain modulation.J. Comp. Neurol.196377–389. [DOI] [PubMed] [Google Scholar]
- Gluschankof, P., Gomez, S., Morel, A., and Cohen, P. (1987). Enzymes that process somatostatin precursors.J. Biol. Chem.262(20):9615–9620. [PubMed] [Google Scholar]
- Gobel, S. (1975). Golgi studies of the substantia gelatinosa neurons in the trigeminal nucleus.J. Comp. Neurol.162397–415. [DOI] [PubMed] [Google Scholar]
- Gobel, S. (1978). Golgi studies of the neurons in layer II of the dorsal horn of the medulla (trigeminal nucleus caudalis).J. Comp. Neurol.180395–414. [DOI] [PubMed] [Google Scholar]
- Gobel, S., and Falls, W. M. (1979). Anatomical observations of horseradish peroxidase-filled terminal primary axonal arborizations in layer II of the substantia gelatinosa of Rolando.Brain Res.175335–340. [DOI] [PubMed] [Google Scholar]
- Gobel, S., Falls, W. M., Bennett, G. J., Abdelmoumene, M., Hayashi, H., and Humphrey, E. (1980). An EM analysis of the synaptic connections of horseradish peroxidase-filled stalked cells and islet cells in the substantia gelatinosa of the adult cat spinal cord.J. Comp. Neurol.194781–807. [DOI] [PubMed] [Google Scholar]
- Hammer, R. E., Brinster, R. L., Rosenfeld, M. G., Evans, R. M., and Mayo, K. E. (1985). Expression of human growth hormone-releasing factor in transgenic mice results in increased somatic growth.Nature315413–416. [DOI] [PubMed] [Google Scholar]
- Harlan, R. E., Shivers, B. D., Romano, G. J., Howells, R. D., and Pfaff, D. W. (1987). Localization of preproenkephalin mRNA in the rat brain and spinal cord byin situ hybridization.J. Comp. Neurol.258159–184. [DOI] [PubMed] [Google Scholar]
- Hayes, A. G., Scadding, J. W., Skingle, M., and Tyers, M. B. (1981). Effects of neonatal administration of capsaicin on nociceptive thresholds in the mouse and rat.J. Pharm. Pharmacol.33183–185. [DOI] [PubMed] [Google Scholar]
- Heinrich, G., Kronenberg, H. M., Potts, J. T., Jr., and Habener, J. F. (1983). Parathyroid hormone messenger ribonucleic acid: Effects of calcium on cellular regulation in vitro.Endocrinology112449–458. [DOI] [PubMed] [Google Scholar]
- Helke, C. J., DiMicco, J. A., Jacobowitz, D. M., and Kopin, I. J. (1981). Effect of capsaicin administration to neonatal rats on the substance P content of discrete CNS regions.Brain Res.222428–431. [DOI] [PubMed] [Google Scholar]
- Hökfelt, T., Kellerth, J. O., Nilsson, G., and Pernow, B. (1975a). Substance P: Localization in the central nervous system and in some primary sensory neurons.Science190889–890. [DOI] [PubMed] [Google Scholar]
- Hökfelt, T., Kellerth, J. O., Nilsson, G., and Pernow, B. (1975b). Experimental immunohistochemical studies on the localization and distribution of substance P in cat primary sensory neurones.Brain Res.100235–252. [DOI] [PubMed] [Google Scholar]
- Hökfelt, T., Ljungdahl, A., Terenius, L., Elde, R., and Nilsson, G. (1977a). Immunohistochemical analysis of peptide pathways possibly related to pain and analgesia: Enkephalin and substance P.Proc. Natl. Acad. Sci. USA743081–3085. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hökfelt, T., Elde, R., Johansson, O., Terenius, L., and Stein, L. (1977b). The distribution of enkephalin-immunoreactive cell bodies in the rat central nervous system.Neurosci. Lett.525–31. [DOI] [PubMed] [Google Scholar]
- Hollt, V., Haarmann, I., Millan, M. J., and Hertz, A. (1987). Prodynorphin gene expression is enhanced in the spinal cord of chronic arthritic rats.Neurosci. Lett.7390–94. [DOI] [PubMed] [Google Scholar]
- Holzer, P., Jurna, I., Gamse, R., and Lembeck, F. (1979). Nociceptive threshold after neonatal capsaicin treatment.Eur. J. Pharmacol.58511–514. [DOI] [PubMed] [Google Scholar]
- Hyman, S. E., Comb, M., Lin, Y. S., Pearlberg, J., Green, M. R., and Goodman, H. M. (1988). A common trans-acting factor is involved in transcriptional regulation of neurotransmitter genes by cyclic AMP.Mol. Cell. Biol.8(10):4225–4233. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hyman, S. E., Comb, M., Pearlberg, J., and Goodman, H. M. (1989). An AP-2 element acts synergistically with the cyclic AMP- and phorbol ester-inducible enhancer of the human proenkephalin gene.Mol. Cell. Biol.9(1):321–324. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Iadarola, M. J., Douglass, J., Civelli, O., and Naranjo, J. R. (1986). Increased spinal cord dynorphin mRNA during peripheral inflammation.NIDA Res. Monogr.75406–409. [PubMed] [Google Scholar]
- Iadarola, M. J., Brady, L. S., Draisci, G., and Dubner, R. (1988a). Enhancement of dynorphin gene expression in spinal cord following experimental inflammation: Stimulus specificity, behavioral parameters and opioid receptor binding.Pain35313–326. [DOI] [PubMed] [Google Scholar]
- Iadarola, M. J., Douglass, J., Civelli, O., and Naranjo, R. (1988b). Differential activation of spinal cord dynorphin and enkephalin neurons during hyperalgesia: Evidence using cDNA hybridization.Brain Res.455205–212. [DOI] [PubMed] [Google Scholar]
- Ilan, J. (Ed.) (1987).Translational Regulation of Gene Expression. Cell, Plenum Press, New York. [Google Scholar]
- Iversen, L. L. (1976). Uptake processes for biogenic amines. In (L. Iverson, S. L. Iverson and S. Snyder, Eds.),Handbook of Psychopharmacology, Raven Press, New York, pp. 381–442. [Google Scholar]
- Iversen, L. L. (1985). Function and distribution of peptides in the nervous system.Biochem. Soc. Trans.13(1):35–37. [DOI] [PubMed] [Google Scholar]
- Jacquin, M. F., Renehan, W. E., Mooney, R. D., and Rhoades, R. W. (1986). Structure-function relationships in rat medullary and cervical dorsal horns. I. Trigeminal primary afferents.J. Neurophysiol.551153–1186. [DOI] [PubMed] [Google Scholar]
- Jancso, G., Kiraly, E., and Jancso-Gabor, A. (1977). Pharmacologically induced selective degeneration of chemosensitive primary sensory neurons.Nature270741–743. [DOI] [PubMed] [Google Scholar]
- Jansco, H., Hokfelt, T., Lundberg, J. M., Kiraly, E., Halesz, N., Nilsson, G., Terenius, L., Rehfeld, J., Steinbusch, H., Verhofstad, A., Elde, R., Said, S., and Brown, M. (1981). Immunohistochemical studies on the effect of capsaicin on spinal and medullary peptide and monoamine neurons using antisera to substance P, gastrin/CCK, somatostain, VIP, enkephalin, neurotensin and 5-Hydroxytryptamine.J. Neurocytol.10963–980. [DOI] [PubMed] [Google Scholar]
- Kabnick, K. S., and Housman, D. E. (1988). Determinants that contribute to cytoplasmic stability of human c-fos and B-globin mRNAs are located at several sites in each mRNA.Mol. Cell. Biol.8(8):3244–3250. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kaplan, L. M., Gabriel, S. M., Koenig, J. I., Sunday, M. E., Spindel, E. R., Martin, J. B., and Chin, W. W. (1988). Galanin is an extrogen-inducible, secretory product of the rat anterior pituitary.Proc. Natl. Acad. Sci.857408–7412. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kelly, R. B. (1988). Pathways of protein secretion in eukaryotes.Science23025–32. [DOI] [PubMed] [Google Scholar]
- Kelsey, J. E., Watson, S. J., Burke, S., Akil, H., and Roberts, J. L. (1986). Characterization of proopiomelanocortin mRNA detected by in situ hybridization.J. Neurosci.638–42. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Khachaturian, H., Watson, S. J., Lewis, M. E., Coy, D., Goldstein, A., and Akil, H. (1982). Dynorphin immunocytochemistry in the rat central nervous system.Peptides3941–954. [DOI] [PubMed] [Google Scholar]
- Kley, N., Loeffler, J. P., and Hollt, V. (1987). Ca2+-dependent histaminergic regulation of proenkephalin mRNA levels in cultured adrenal chromaffin cells.Neuroendocrinology4689–92. [DOI] [PubMed] [Google Scholar]
- Koller, K. J., Wolff, R. S., Warden, M. K., and Zoeller, R. T. (1987). Thyroid hormones regulate levels of thyrotropin-releasing-hormone mRNA in the paraventricular nucleus.Proc. Natl. Acad. Sci.847329–7333. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LaMotte, C. C., and deLanerolle, N. C. (1983). Ultrastructure of chemically defined nervous systems in the dorsal horn of the monkey. II. Methionine-enkephalin immunoreactivity.Brain Res.27451–63. [DOI] [PubMed] [Google Scholar]
- Light, A. R., and Perl, E. R. (1979). Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers.J. Comp. Neurol.186133–150. [DOI] [PubMed] [Google Scholar]
- Lightman, S. L., and Young, W. S., III (1987a). Changes in hypothalamic preproenkephalin A mRNA following stress and opiate withdrawal.Nature328643–645. [DOI] [PubMed] [Google Scholar]
- Lightman, S. L., and Young, W. S., III (1987b). Vasopressin, oxytocin, dynorphin, enkephalin, and corticotrophin releasing factor mRNA stimulation in the rat.J. Physiol. (Lond.)39423–39. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ljungdahl, A., Hokfelt, T., and Nilsson, C. (1978). Distribution of substance P-like immunoreactivity in the central nervous system of the rat. I. Cell bodies and nerve terminals.Neuroscience3861–943. [DOI] [PubMed] [Google Scholar]
- Loeffler, J., Kley, N., Pittius, C. W., and Hollt, V. (1985). Corticotropin-releasing factor and forskolin increase proopiomelanocortin messenger RNA levels in rat anterior and intermediate cells in vitro.Neurosci. Lett.62383–387. [DOI] [PubMed] [Google Scholar]
- Markowitz, S., Saito, K., and Moskowitz, M. A. (1988). Neurogenically mediated plasma extravasation in dura mater: Effect of ergot alkaloids.Cephalalgia883–91. [DOI] [PubMed] [Google Scholar]
- Martin, J. B., Reichlin, S., and Bick, K. L. (Eds.) (1981).Neurosecretion and Brain Peptides, Raven Press, New York. [Google Scholar]
- May, V., and Eipper, B. A. (1985). Regulation of peptide amidation in cultured pituitary cells.J. Biol. Chem.260(30):16224–16231. [PubMed] [Google Scholar]
- McNeill, D. L., Coggeshall, R. E., and Carlton, S. M. (1988). A light and electron microscopic study of calcitonin gene-related peptide in the spinal cord of the rat.Exp. Neurol.99699–708. [DOI] [PubMed] [Google Scholar]
- Merchenthaler, I., Maderdrut, J. L., Altschuler, R. A., and Petrusz, P. (1986). Immunocytochemical localization of proenkephalin-derived peptides in the central nervous system of the rat.Neuroscience17325–348. [DOI] [PubMed] [Google Scholar]
- Millan, M. J. (1986). Multiple opioid systems and pain.Pain27303–347. [DOI] [PubMed] [Google Scholar]
- Millan, M. J., Millan, M. H., Pilcher, C. W. T., Cztonkowski, A., Herz, A., and Colpaert, F. C. (1985). Spinal cord dynorphin may modulate nociception via a K-opioid receptor in chronic arthritic rats.Brain Res.340156–159. [DOI] [PubMed] [Google Scholar]
- Millan, M. J., Millan, M. H., Cztonkowski, A., Hollt, V., Pilcher, C. W. T., Herz, A., and Colpaert, F. C. (1986). A model of chronic pain in the rat: Response of multiple opioid systems to adjuvant-induced arthritis.J. Neurosci.6899–906. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Miller, K. E., and Seybold, V. S. (1987). Comparison of met-enkephalin-, dynorphin A-, neurotensin-immunoreactive neurons in the cat and rat spinal cords. I. Lumbar cord.J. comp. neurol.255293–304. [DOI] [PubMed] [Google Scholar]
- Morris, B. J., Moneta, M. E., Bruggencate, G. T., and Hollt, V. (1987). Levels of prodynorphin mRNA in rat dentate gyrus are decreased during hippocampal kindling.Neurosci. Lett.80298–302. [DOI] [PubMed] [Google Scholar]
- Morris, B. J., Feasey, K. J., Bruggencate, G. T., Herz, A., and Hollt, V. (1988a). Electrical stimulation in vivo increases the expression of proenkephaline mRNA and decreases the expression of prodynorphin mRNA in rat hippocampal granule cells.85:3226–3230. [DOI] [PMC free article] [PubMed]
- Morris, B. J., Hollt, V., and Herz, A. (1988b). Dopaminergic regulation of striatal proenkephalin mRNA and prodynorphin mRNA: Contrasting effects of D1 and D2 antagonists.25:525–532. [DOI] [PubMed]
- Morris, B. J., Hollt, V., and Herz, A. (1988c). Opioid gene expression in rat striatum is modulated via opioid receptors: Evidence from localized receptor inactivation.89:80–84. [DOI] [PubMed]
- Morris, B. J., Reimer, S., Hollt, V., and Herz, A. (1988d). Regulation of striatal prodynorphin mRNA by the raphe-striatal pathway.Mol. Brain Res.415–22. [DOI] [PubMed] [Google Scholar]
- Nagy, J. I. (1982). Capsaicin's action on the nervous system.Trends Neurosci.5362–365. [Google Scholar]
- Nagy, J. I., and Hunt, S. P. (1983). The termination of primary afferents within the rat dorsal horn: Evidence for rearrangement following capsaicin treatment.J. Comp. Neurol.218145–158. [DOI] [PubMed] [Google Scholar]
- Nagy, J. I., Vincent, S. R., Staines, W. A., Fibiger, H. C., Reisine, T. D., and Yamumura, H. I. (1980). Neurotoxic action of capsaicin on spinal substance P neurons.Brain Res.186435–444. [DOI] [PubMed] [Google Scholar]
- Nagy, J. I., Hunt, S. P., Iversen, L. L., and Emson, P. C. (1981). Biochemical and anatomical observation on the degeneration of peptide-containing primary afferent neurons after neonatal capsaicin.Neuroscience61923–1934. [DOI] [PubMed] [Google Scholar]
- Ninkovic, M., Hunt, S. P., and Kelly, J. S. (1981). Effect of dorsal rhizotomy on the autoradiographic distribution of opiate and neurotensin receptors and neurotensin-like immunoreactivity within the rat spinal cord.Brain Res.230111–119. [DOI] [PubMed] [Google Scholar]
- Nishimori, T., Moskowitz, M. A., and Uhl, G. R. (1988). Opioid peptide gene expression in rat trigeminal nucleus caudalis neurons: Normal distribution and effects of trigeminal deafferentiation.J. Comp. Neurol.274142–150. [DOI] [PubMed] [Google Scholar]
- Nishimori, T., Buzzi, M. G., Moskowitz, M. A., and Uhl, G. R. (1989a). Preproenkephalin mRNA expression in nucleus caudalis neurons is enhanced by trigeminal stimulation.Mol. Brain. Res. (in press). [DOI] [PubMed]
- Nishimori, T., Buzzi, M. G., Moskowitz, M. A., and Uhl, G. R. (1989b). Differential effects of small-and large-caliber primary afferents on nucleus caudalis preproenkephalin expression. (Submitted for publication).
- Noguchi, K., Morita, Y., Kiyama,H., Sato, M., Ono, K., and Tohyama, M. (1989). Preproenkephalin gene expression in the rat spinal cord after noxious stimuli.Mol. Brain Res.5227–234. [DOI] [PubMed] [Google Scholar]
- Normand, E., Popovici, T., Onteniente, B., Fellmann, D., Piatier-Tonneau, D., Auffray, C., and Bloch, B. (1988). Dopaminergic neurons of the substancia nigra modulate preproenkephalin A gene expression in rat striatal neurons.Brain Res.43939–46. [DOI] [PubMed] [Google Scholar]
- Ouafik, L., May, V., Keutmann, H. T., and Eipper, B. A. (1989). Developmental regulation of peptidylglycine a-amidating monooxygenase (PAM) in rat heart atrium and ventricle.J. Biol. Chem.264(10):5839–5845. [PubMed] [Google Scholar]
- Panerai, A. E., Sacerdote, P., Brini, A., Bianchi, M., and Mantegazza, P. (1988). Central nervous system neuropeptides after peripheral nerve deafferentation.Peptides9319–324. [DOI] [PubMed] [Google Scholar]
- Price, D. D., Hayashi, H., Dubner, R., and Ruda, M. A. (1979). Functional relationships between neurons of marginal and substantia gelatinosa layers of primate dorsal horn.J. Neurophysiol.421590–1608. [DOI] [PubMed] [Google Scholar]
- Priestley, J. V., Somogyi, P., and Cuello, A. C. (1982). Immunocytochemical localization of substance P in the spinal trigeminal nucleus of the rat: A light and electron microscopic study.J. Comp. Neurol.21131–49. [DOI] [PubMed] [Google Scholar]
- Przewlocki, R., Haarmann, I., Nikolarakis, K., Herz, A., and Hollt, V. (1988). Prodynorphin gene expression in spinal cord is enhanced after traumatic injury in the rat.Mol. Brain Res.437–41. [DOI] [PubMed] [Google Scholar]
- Ptashne, M. (1988). How eukaryotic transcriptional activators work.Nature335683–689. [DOI] [PubMed] [Google Scholar]
- Reppert, S. M., and Uhl, G. R. (1987). Vasopressin messenger ribonucleic acid in supraoptic and suprachiasmatic nuclei: Appearance and circadian regulation during development.Endocrinology1202483–2487. [DOI] [PubMed] [Google Scholar]
- Robinson, B. G., Frim, D. M., Schwartz, W. J., and Majzoub, J. A. (1988). Vasopressin mRNA in the suprachiasmatic nuclei: Daily regulation.Science241(4863):342–344. [DOI] [PubMed] [Google Scholar]
- Rodriguez, C., Brayton, K. A., Brownstein, M., and Dixon, J. E. (1989). Rat preprocarboxypeptidase H.J. Biol. Chem.264(10):5988–5995. [PubMed] [Google Scholar]
- Rosenfeld, M. G., Mermod, J.-J., Amara, S. G., Swanson, L. W., Sawchenko, P. E., Rivier, J., Vale, W. W., and Evans, R. M. (1983). Production of a novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing.Nature304129–135. [DOI] [PubMed] [Google Scholar]
- Rothfeld, J. M., Hejtmancik, J. F., Conn, P. M., and Pfaff, D. W. (1987). LHRH messenger RNA in neurons in the intact and castrate male rat forebrain, studied by in situ hybridization.Exp. Brain Res.67113–118. [DOI] [PubMed] [Google Scholar]
- Ruda, M. A., Bennett, G. J., and Dubner, R. (1986). Neurochemistry and neural circuitry in the dorsal horn.Prog. Brain Res.66219–268. [DOI] [PubMed] [Google Scholar]
- Ruda, M. A., Iadarola, M. J., Choen, L. V., and Young, W. S., III (1988).In situ hybridization histochemistry and immunocytochemistry reveal an increase in spinal dynorphin biosynthesis in a rat model of peripheral inflammation and hyperalgesia.Proc. Natl. Acad. Sci. USA85622–626. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saffen, D. W., Cole, A. J., Worley, P. F., Christy, B. A., Ryder, K., and Baraban, J. M. (1988). Convulsant-induced increase in transcription factor messenger RNAs in rat brain.Proc. Natl. Acad. Sci. USA851–5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saito, K., Markowitz, S., and Moskowitz, M. A. (1989). Ergot alkaloids block neurogenic extravasation in dura mater: Proposed action in vascular headaches.Ann. Neurol. (in press). [DOI] [PubMed]
- Schalling, M., Dagerlind, A., Brene, S., Hallman, H., Djurfeldt, M., Persson, H., Terenius, L., Goldstein, M., Schlesinger, D., and Hökfelt, T. (1988a). Coexistence and gene expression of phenylethanolamine N-methyltransferase, tyrosine hydroxylase, and neuropeptide tyrosine in the rat and bovine adrenal gland: Effects of reserpine.Proc. Natl. Acad. Sci.858306–8310. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schalling, M., Franco-Cereceda, A., Hökfelt, T., Persson, H., and Lundberg, J. M. (1988b). Increased neuropeptide Y messenger RNA and peptide in sympathetic ganglia after reserpine pretreatment.Eur. J. Pharmacol.156419–420. [DOI] [PubMed] [Google Scholar]
- Segerson, T. P., Kauer, J., Wolfe, H. C., Mobtaker, H., Wu, P., Jackson, I., and Lechan, R. M. (1987). Thyroid hormone regulates TRH biosynthesis in the paraventricular nucleus of the rat hypothalamus.Science23878–80. [DOI] [PubMed] [Google Scholar]
- Seidman, C. E., Wong, D. W., Jarcho, J. A., Bloch, K. D., and Seidman, J. G. (1988). Cis-acting sequences that modulate atrial natriuretic factor gene expression.Proc. Natl. Acad. Sci. USA854104–4108. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Selden, R. F., Skoskiewicz, M. J., Howie, K. B., Russell, P. S., and Goodman, H. M. (1986). Regulation of human insulin gene expression in transgenic mice.Nature321525–528. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sherman, T. G., Day, R., Civelli, O., Douglass, J., Herbert, E., Akil, H., and Watson, S. J. (1988). Regulation of hypothalamic magnocellular neuropeptides and their mRNAs in the Brattleboro rat: Coordiante responses to further osmotic challenge.J. Neurosci.83785–3796. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shivers, B. D., Harlan, R. E., Romano, G. J., Howells, R. D., and Pfaff, D. W. (1986). Cellular location and regulation of proenkephalin mRNA in rat brain. In In SituHybridization in Brain (G. R. Uhl, Ed.), Plenum Press, New York, pp. 3–20. [Google Scholar]
- Sivam, S. P., Takeuchi, K., Li, S., Douglass, J., Civelli, O., Calvetta, L., Herbert, E., McGinty, J. F., and Hong, J. S. (1988). Lithium increases dynorphin A(1-8) and prodynorphin mRNA levels in the basal ganglia of rats.Mol. Brain Res.3155–164. [DOI] [PubMed] [Google Scholar]
- Skofitsch, G., and Jacobowitz, D. M. (1985a). Calcitonin gene-related peptide: Detailed immunohistochemical distribution in the central nervous system.Peptides6721–745. [DOI] [PubMed] [Google Scholar]
- Skofitsch, G., and Jacobowitz, D. M. (1985b). Calcitonin gene-related peptide coexists with substance P in capsaicin sensitive neurons and sensory ganglia of the rat.Peptides6747–754. [DOI] [PubMed] [Google Scholar]
- Sossin, W. S., Fisher, J. M., and Scheller, R. H. (1989). Cellular and molecular biology of neuropeptide processing and packaging.Neuron21407–1417. [DOI] [PubMed] [Google Scholar]
- Stine, S. M., Yang, H.-Y., and Costa, E. (1982). Evidence for ascending and descending intraspinal as well as primary sensory somatostatin projections in the rat spinal cord.J. Neurochem.381144–1150. [DOI] [PubMed] [Google Scholar]
- Sugiura, Y., Lee, C. L., and Perl, E. R. (1986). Central projections of identified, unmyelinated (C) afferent fibers innervating mammalian skin.Science234358–361. [DOI] [PubMed] [Google Scholar]
- Sumal, K. K., Pickel, V. M., Miller, R. J., and Reis, D. J. (1982). Enkephalin containing neurons in substantia gelatinosa of spinal trigeminal complex: Ultrastructure and synaptic interaction with primary sensory afferents.Brain Res.248223–236. [DOI] [PubMed] [Google Scholar]
- Sweetman, P. M., Wrathall, J. R., and Neale, J. H. (1986). Localization of dynorphin gene product-immunoreactivity in neurons from spinal cord and dorsal root ganglia.Neuroscience18947–955. [DOI] [PubMed] [Google Scholar]
- Tang, F., Costa, E., and Schwartz, J. P. (1983). Increase of proenkephalin mRNA and enkephalin content of rat striatum after daily injection of haloperidol for 2 to 3 weeks.Proc. Natl. Acad. Sci.803841–3844. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tsukada, T., Fink, J. S., Mandel, G., and Goodman, R. H. (1987). Identification of a region in the human vasoactive intestinal polypeptide gene responsible for regulation of cyclic AMP.J. Biol. Chem.262(18):8743–8747. [PubMed] [Google Scholar]
- Uhl, G. R. (ed.) (1986).In situ Hybridization in Brain, Plenum Press, New York. [Google Scholar]
- Uhl, G. R., and Reppert, S. M. (1986). Suprachiasmatic nucleus vasopressin messenger RNA: Circadian variaction in normal and Brattleboro rats.Science232390–393. [DOI] [PubMed] [Google Scholar]
- Uhl, G. R., Zing, H. H., and Habener, J. F. (1985). Vasopressin mRNA in situ hybridization: Localization and regulation studied with oligonucleotide cDNA probes in normal and Brattleboro rat hypothalamus.Proc. Natl. Acad. USA825555–5559. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Uhl, G. R., Goodman, R. R., Kuhar, M. J., Childers, S. R., and Snyder, S. H. (1979). Immunohistochemical mapping of enkephalin containing cell bodies, fibers and nerve terminals in the brain stem of the rat.Brain Res.16675–94. [DOI] [PubMed] [Google Scholar]
- Uhl, G. R., Evans, J., Parta, M., Walworth, C., Hill, K., Sasek, C., Voigt, M., and Reppert, S. (1986). Vasopressin and somatostatin mRNAin situ hybridization. In In SituHybridization in Brain (G. R. Uhl, Ed.), Plenum Press, New York, pp. 21–47. [Google Scholar]
- Uhl, G. R., Navia, B., and Douglas, J. (1988a). Differential expression of preproenkephalin and preprodynorphin mRNAs in striatal neurons: High levels of preproenkephalin expression depend on cerebral cortical afferents.J. Neurosci.8(12):4755–4764. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Uhl, G. R., Ryan, J. P., and Schwartz, J. F. (1988b). Morphine alters preproenkephalin gene expression.Brain Res.459391–397. [DOI] [PubMed] [Google Scholar]
- Vincent, S. R., Hokfelt, T., Christensson, I., and Terenius, L. (1982). Dynorphin-immunoreactive neurons in the central nervous system of the rat.Neurosci. Lett.33185–190. [DOI] [PubMed] [Google Scholar]
- Wall, P. D. (1978). The gate control theory of pain mechanisms. A re-examination and re-statement.Brain1011–18. [DOI] [PubMed] [Google Scholar]
- Wasylyk, B. (1988). Enhancers and transcription factors in the control of gene expression.Biochim. Biophys. Acta95117–35. [DOI] [PubMed] [Google Scholar]
- Watson, S. J., Khachaturian, H., Akil, H., Coy, D. H., and Goldstein, A. (1982). Comparison of the distribution of dynorphin systems and enkephalin systems in brain.Science2181134–1136. [DOI] [PubMed] [Google Scholar]
- Watson, S. J., Khachaturian, H., Taylor, L., Fischli, W., Goldstein, A., and Akil, H. (1983). Pro-dynorphin peptides are found in the same neurons throughout rat brain: Immunocytochemical study.Proc. Natl. Acad. Sci. USA80891–894. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weber, E., and Barchas, J. D. (1983). Immunohistochemical distribution of dynorphin B in rat brain: Relation to dynorphin A and a-neo-endorphin-system.Proc. Natl. Acad. Sci. USA801125–1129. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Werner, H., Koch, Y., Baldino, F., Jr., and Gozes, I. (1988). Steroid regulation of somatostatin mRNA in the rat hypothalamus.J. Biol. Chem.2637666–7671. [PubMed] [Google Scholar]
- Wiesenfeld-Hallin, Z., Hokfelt, T., Lundberg, J. M., Forssmann, W. G., Renecke, M., Tschopp, F. A., and Fischer, J. A. (1984). Immunoreactive calcitonin gene-related peptide and substance P coexist in sensory neurons to the spinal cord and interact in spinal behavioral responses of the rat.Neurosci. Lett.52199–204. [DOI] [PubMed] [Google Scholar]
- Williams, R. G., and Dockray, G. J. (1983). Distribution of enkephalin-related peptides in rat brain: Immunohistochemical studies using antisera to met-enkephalin and met-enkephalin Arg6 Phe7.Neuroscience9563–586. [DOI] [PubMed] [Google Scholar]
- Wolfson, B., Manning, R. W., Davis, L. G., Arentzen, R., and Baldino, F., Jr. (1984). Co-localization of corticotropin-releasing factor and vasopressin mRNA in neurones after adrenalectomy.Nature31559–61. [DOI] [PubMed] [Google Scholar]
- Woolf, C. J., and Wall, P. D. (1982). Chronic peripheral nerve section diminishes the primary afferent A-fibre mediated inhibition of rat dorsal horn neurones.Brain Res.24277–85. [DOI] [PubMed] [Google Scholar]
- Woolf, C. J., and Wall, P. D. (1986). Relative effectiveness of C-primary afferent fibers of different origins in evoking a prolonged facilitation of the flexor reflex in the rat.J. Neurosci.61433–1442. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yen, T. J., Machlin, P. S., and Cleveland, D. W. (1988). Autoregulated instability of B-tubulin mRNAs by recognition of the nascent amino terminus of B-tubulin.Nature334580–585. [DOI] [PubMed] [Google Scholar]
- Yoshikawa, K., Hong, J.-S., and Sabol, S. L. (1985). Electroconvulsive shock increases preproenkephalin messenger RNAabundance in rat hypothalamus.Proc. Natl. Acad. Sci.82589–593. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Young, W. S., III, Bonner, T. I., and Brann, M. R. (1986a). Mesencephalic dopamine neurons regulate the expression of neuropeptide mRNAs in the rat forebrain.Proc. Natl. Acad. Sci. USA839827–9831. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Young, W. S. III, Mezey, E., and Siegel, R. E. (1986b). Quantitative in situ hybridization histochemistry reveals increased levels of corticotropin-releasing factor mRNA after adrenalectomy in rats.Neurosci. Lett.70198–203. [DOI] [PubMed] [Google Scholar]
- Zingg, H. H., and Lefebvre, D. L. (1988). Oxytocin and vasopressin gene expression during gestation and lactation.Mol. Brain Res.41–6. [DOI] [PubMed] [Google Scholar]
- Zingg, H. H., Lefebvre, D. L., and Almazan, G. (1988). Regulation of poly(A) tail size of vasopressin mRNA.J. Biol. Chem.263(23):11041–11043. [PubMed] [Google Scholar]
