The messenger RNA encoding VGF, a neuronal peptide precursor, is rapidly regulated in the rat central nervous system by neuronal activity, seizure and lesion

Neuroscience

Volumn 82, Issue 1, 1997, Pages 7-19

  Snyder, S E ^a   Cheng, H W ^b   Murray, K D ^c,d   Isackson, P J ^c   McNeill, T H ^b   Salton, S R J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c MAYO CLINIC   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Decortication; Kainate; Monocular deprivation; Seizure; Sprouting; VGF

Indexed keywords

KAINIC ACID; MESSENGER RNA; NEUROTROPHIC FACTOR; NEUROTROPHIN; PROTEIN PRECURSOR; SECRETORY PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; BRAIN REGION; CONTROLLED STUDY; GENE EXPRESSION; MONOCULAR DEPRIVATION; NERVE CELL STIMULATION; NERVE SPROUTING; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RAT; SEIZURE;

ANIMALS; CENTRAL NERVOUS SYSTEM; CEREBRAL CORTEX; EXCITATORY AMINO ACID ANTAGONISTS; EYE; GENICULATE BODIES; IMAGE PROCESSING, COMPUTER-ASSISTED; IN SITU HYBRIDIZATION; INJECTIONS; KAINIC ACID; MALE; NEURONS; NEUROPEPTIDES; PROTEIN BIOSYNTHESIS; PROTEINS; RATS; RATS, INBRED F344; RATS, SPRAGUE-DAWLEY; RNA PROBES; RNA, MESSENGER; SEIZURES; TETRODOTOXIN;

EID: 0030929942     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(97)00280-7     Document Type: Article

References (65)

1. Bartel D. P., Sheng M., Lau M. F., Greenberg M. E. Growth factors and membrane depolarization activate distinct programs of early response gene expression: dissociation of fos and jun induction. Genes Dev. 3:1989;304-313.
2. Baybis M., Salton S. R. J. Nerve growth factor rapidly regulates VGF gene transcription through cycloheximide sensitive and insensitive pathways. Fedn Eur. biochem. Socs Lett. 308:1992;202-206.
3. Benson D., Salton S. R. J. Expression and polarization of VGF in developing hippocampal neurons. Devl Brain Res. 96:1996;219-228.
4. Bonni A., Ginty D. D., Dudek H., Greenberg M. E. Serine 133-phosphorylated CREB induces transcription via a cooperative mechanism that may confer specificity to neurotrophin signals. Molec. Cell. Neurosci. 6:1995;168-183.
5. Cabelli R. J., Hohn A., Shatz C. J. Inhibition of ocular dominance column formation by infusion of NT-4/5 or BDNF. Science. 267:1995;1662-1666.
6. Castrén E., Zafra F., Thoenen H., Lindholm D. Light regulates expression of brain-derived neurotrophic factor mRNA in visual cortex. Proc. natn. Acad. Sci. U.S.A. 89:1992;9444-9448.
7. Cheng H.-W., Anavi Y., Goshgarian H., McNeill T. H., Rafols J. A. Loss and recovery of striatal dendritic spines following lesions in the cerebral cortex of adult and aged mice. Soc. Neurosci. Abstr. 14:1988;1292.
8. Cheng H.-W., Jung T., Brown S. A., Pasinetti G. M., Finch C. E., McNeill T. H. Response of striatal astrocytes to neuronal deafferentation: an immunocytochemical and ultrastructural time course study. Neuroscience. 62:1994;425-439.
9. Cheng H.-W., Mori N. and McNeill T. H. (1997) Differential regulation of growth associated protein mRNAs in the contralateral cortex after a striatal deafferentation lesion in adult rats. J. Neurosci. (in press).
10. Crosby S. D., Veile R. A., Donis-Keller H., Baraban J. M., Simburger K. S., Milbrandt J. Neural-specific gene expression, genomic structure and chromosomal localization of the gene encoding the zinc-finger transcription factor NGFI-A. Proc. natn. Acad. Sci. U.S.A. 89:1992;4739-4743.
11. D'Arcangelo G., Habas R., Wang S., Halegoua S., Salton S. R. J. Activation of co-dependent transcription factors is required for transcriptional induction of the vgf gene by NGF and Ras. Molec. Cell. Biol. 16:1996;4621-4631.
12. Domenici L., Berardi N., Carmignoto G., Vantini G., Maffei L. Nerve growth factor prevents the amblyopic effects of monocular deprivation. Proc. natn. Acad. Sci. U.S.A. 88:1991;8811-8815.
13. Doster S. K., Lozano A. M., Aguayo A. J., Willard M. B. Expression of the growth-associated protein GAP-43 in adult rat retinal ganglion cells following axon injury. Neuron. 6:1991;635-647.
14. Dragunow M., Yamada N., Bilkey D. K., Lawlor P. Induction of immediate-early gene proteins in dentate granule cells and somatostatin interneurons after hippocampal seizures. Molec. Brain Res. 13:1992;119-126.
15. Dugich-Djordjevic M. M., Ohsawa F., Okazaki T., Mori N., Day J. R., Beck K. D., Hefti F. Differential regulation of catalytic and non-catalytic trkB messenger RNAs in the rat hippocampus following systemic administration of kainate. Neuroscience. 66:1995;861-877.
16. Dugich-Djordjevic M. M., Tocco G., Lapchak P. A., Pasinetti G. M., Najm I., Baudry M., Hefti F. Regionally specific and rapid increases in brain-derived neurotrophic factor messenger RNA in the adult rat brain following seizures induced by systemic administration of kainic acid. Neuroscience. 47:1992;303-315.
17. Ferri G.-L., Levi A., Possenti R. A novel neuroendocrine gene product: selective VGF8a gene expression and immunolocalisation of the VGF protein in endocrine and neuronal populations. Molec. Brain Res. 13:1992;139-143.
18. Frostig R. D., Prakash N., Cohen-Cory S. BDNF rapidly modifies activity-dependent responses to tactile stimulation in the adult rat somatosensory cortex. Soc. Neurosci. Abstr. 21:1995;114.
19. Gall C., Murray K., Isackson P. J. Kainic acid-induced seizures stimulate increased expression of nerve growth factor mRNA in rat hippocampus. Molec. Brain Res. 9:1991;113-123.
20. Gass P., Herdegen T., Bravo R., Kiessling M. Spatiotemporal induction of immediate early genes in the rat brain after limbic seizures: effects of NMDA receptor antagonist MK-801. Eur. J. Neurosci. 5:1993;933-943.
21. Goodman C. S., Shatz C. J. Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell. 72:1993;77-98.
22. Greene L. A., Tischler A. S. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc. natn. Acad. Sci. U.S.A. 73:1976;2424-2428.
23. Halegoua S., Armstrong R. C., Kremer N. E. Dissecting the mode of action of a neuronal growth factor. Curr. Top. Microbiol. Immunol. 165:1990;119-170.
24. Hawley R. J., Scheibe R. J., Wagner J. A. NGF induces the expression of the VGF gene through a cAMP response element. J. Neurosci. 12:1992;2573-2581.
25. Kang H., Schuman E. M. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science. 267:1995;1658-1662.
26. Kesslak J. P., Gómez-Pinilla F., So V., Choi J., Cotman C. W. Increased expression of NGF and BDNF mRNA associated with learning. Soc. Neurosci. Abstr. 21:1995;36.
27. Levi A., Eldridge J. D., Paterson B. M. Molecular cloning of a gene sequence regulated by nerve growth factor. Science. 229:1985;393-395.
28. Levine E. S., Dreyfus C. F., Black I. B., Plummer M. R. Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via post-synaptic tyrosine kinase receptors. Proc. natn. Acad. Sci. U.S.A. 92:1995;8074-8077.
29. Liu J.-W., Andrews P. C., Mershon J. L., Yan C., Allen D. L., Ben-Jonathan N. Peptide V: a VGF-derived neuropeptide purified from bovine posterior pituitary. Endocrinology. 135:1994;2742-2748.
30. Loeb D. M., Maragos J., Martin-Zanca D., Chao M. V., Parada L. F., Greene L. A. The trk proto-oncogene rescues NGF responsiveness in mutant NGF-nonresponsive PC12 cell lines. Cell. 66:1991;961-966.
31. Lombardo A., Rabacchi S. A., Cremisi F., Pizzorusso T., Cenni M. C., Possenti R., Barsacchi G., Maffei L. A developmentally regulated nerve growth factor-inducible gene, VGF, is expressed in geniculocortical afferents during synaptogenesis. Neuroscience. 65:1995;997-1008.
32. Lowenstein D. H., Seren M. S., Longo F. M. Prolonged increases in neurotrophic activity associated with kainate-induced hippocampal synaptic reorganization. Neuroscience. 56:1993;597-604.
33. Mack K. J., Yi S. D., Chang S., Millan N., Mack P. NGFI-C expression is affected by physiological stimulation and seizures in the somatosensory cortex. Molec. Brain Res. 29:1995;140-146.
34. Maffei L., Berardi N., Domenici L., Parisi V., Pizzorusso T. Nerve growth factor (NGF) prevents the shift in ocular dominance distribution of visual cortical neurons in monocularly deprived rats. J. Neurosci. 12:1992;4651-4662.
35. Mahata M., Hortnagl H., Mahata S. K., Fischer-Colbrie R., Winkler H. Messenger RNA levels of chromogranin B, secretogranin II, and VGF in rat brain after AF64A-induced septohippocampal cholinergic lesions. J. Neurochem. 61:1993;1648-1656.
36. Mahata S. K., Mahata M., Fischer-Colbrie R., Winkler H. In situ hybridization: mRNA levels of secretogranin II, VGF and peptidylglycine alpha-amidating monooxygenase in brain of salt-loaded rats. Histochemistry. 99:1993;287-293.
37. Mahata S. K., Mahata M., Hortnag H., Fischer-Colbrie R., Steiner H. J., Dietze O., Winkler H. Concomitant changes of messenger ribonucleic acid levels of secretogranin II, VGF, vasopressin and oxytocin in the paraventricular nucleus of rats after adrenalectomy and during lactation. J. Neuroendocr. 5:1993;323-330.
38. Mailleux P., Vanderhaeghen J.-J. Glutamatergic regulation of cannabinoid receptor gene expression in the caudate-putamen. Eur. J. Pharmac. 266:1994;193-196.
39. Marshall C. J. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell. 80:1995;179-185.
40. McNeill T. H., Cheng H.-W., Rafols J. A. and Mori N. (1992) Neuroplasticity and Parkinson's Disease. In Progress in Parkinson Research II (eds Hefti F. and Weiner W. J.), pp. 299-324. Plenum , New York.
41. Merlio J.-P., Ernfors P., Kokaia Z., Middlemas D. S., Bengzon J., Kokaia M., Smith M.-L., Siesjö B. K., Hunter T., Lindvall O., Persson H. Increased production of the TrkB protein tyrosine kinase receptor after brain insults. Neuron. 10:1993;151-164.
42. Neeper S. A., Gómez-Pinilla F., Choi J., Cotman C. W. Exercise and brain neurotrophins [Letter]. Nature. 373:1995;109.
43. Neeper S. A., Gómez-Pinilla F., Choi J., Cotman C. W. Physical activity up-regulates BDNF and NGF mRNA in the rat brain. Soc. Neurosci. Abstr. 21:1995;296.
44. Pasinetti G. M., Cheng H.-W., Morgan D. G., Lampert-Etchells M., McNeill T. H., Finch C. E. Astrocytic messenger RNA responses to striatal deafferentation in male rat. Neuroscience. 53:1993;199-211.
45. Patterson S. L., Abel T., Ernfors P., Jaenisch R., Kandel E. R. Deficits in short-term plasticity and LTP in hippocampal slices from BDNF knockout mice. Soc. Neurosci. Abstr. 21:1995;35.
46. Possenti R., Eldridge J. D., Paterson B. M., Grasso A., Levi A. A protein induced by NGF in PC12 cells is stored in secretory vesicles and released through the regulated pathway. Eur. molec. Biol. Org. J. 8:1989;2217-2223.
47. Possenti R., Rinaldi A. M., Canu N., Levi A., Ferri G.-L., Trani E. Neuronal specific processing of VGF protein leads to the production and regulated secretion of peptides derived from its carboxi-terminal. Soc. Neurosci. Abstr. 20:1994;1151.
48. ras activity and consequent prolonged ERK activity. Neuron. 9:1992;705-717.
49. Reese B. E. "Hidden lamination" in the dorsal lateral geniculate nucleus: the functional organization of this thalamic region in the rat. Brain Res. Rev. 13:1988;119-137.
50. Ringstedt T., Lagercrantz H., Persson H. Expression of members of the trk family in the developing postnatal rat brain. Devl Brain Res. 72:1993;119-131.
51. Salton S. R. J. Nucleotide sequence and regulatory studies of VGF, a nervous system-specific mRNA that is rapidly and relatively selectively induced by nerve growth factor. J. Neurochem. 57:1991;991-996.
52. Salton S. R. J., Fischberg D. J., Dong K.-W. Structure of the gene encoding VGF, a nervous system-specific mRNA that is rapidly and selectively induced by nerve growth factor in PC12 cells. Molec. Cell. Biol. 11:1991;2335-2349.
53. Sambrook J., Fritsch E. F. and Maniatis T. (1989) Molecular Cloning: A Laboratory Manual. 2nd edn, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
54. Schreyer D. J., Skene J. H. P. Fate of GAP-43 in ascending spinal axons of DRG neurons after peripheral nerve injury: delayed accumulation and correlation with regenerative potential. J. Neurosci. 11:1991;3738-3751.
55. Snyder S. E. (1996) Expression of the mRNA encoding VGF, a neural-specific peptide precursor, in the developing and adult rat central nervous systems, and its modulation in response to changes in neuronal electrical activity, seizure, and lesion. Ph.D. dissertation, Mount Sinai School of Medicine of the City University of New York.
56. Snyder S. E., Cheng H.-W., Murray K. D., Isackson P. J., McNeill T. H., Salton S. R. J. Changes in VGF mRNA expression in the rat brain after kainic acid induced seizure and cortical lesion. Soc. Neurosci. Abstr. 21:1995;1550.
57. Snyder S. E., Li J., Schauwecker P. E., McNeill T. H., Salton S. R. J. Comparison of RPTPζ/β, phosphacan, and trkB mRNA expression in the developing and adult rat nervous system, and induction of RPTPζ/β and phosphacan mRNA following brain injury. Molec. Brain Res. 40:1996;79-96.
58. Tauck D. L., Nadler J. V. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J. Neurosci. 5:1985;1016-1022.
59. Tetzlaff W., Alexander S. W., Miller F. D., Bisby M. A. Response of facial and rubrospinal neurons to axotomy: changes in mRNA expression for cytoskeletal proteins and GAP-43. J. Neurosci. 11:1991;2528-2544.
60. Trani E., Ciotti T., Rinaldi A. M., Canu N., Ferri G. L., Levi A., Possenti R. Tissue-specific processing of the neuroendocrine protein VGF. J. Neurochem. 65:1995;2441-2449.
61. van den Pol A. N., Bina K., Decavel C., Ghosh P. VGF expression in the brain. J. comp. Neurol. 347:1994;455-469.
62. van den Pol A. N., Decavel C., Levi A., Paterson B. Hypothalamic expression of a novel gene product, VGF: immunocytochemical analysis. J. Neurosci. 9:1989;4122-4137.
63. Wüllner U., Standaert D. G., Testa C. M., Landwehrmeyer G. B., Catania M. V., Penney J. B. Jr., Young A. B. Glutamate receptor expression in rat striatum: effect of deafferentation. Brain Res. 647:1994;209-219.
64. Zafra F., Hengerer B., Leibrock J., Thoenen H. Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors. Eur. molec. Biol. Org. J. 9:1990;3545-3550.
65. Zheng M., Pintar J. E. Analysis of ontogeny of processing enzyme gene expression and regulation. Meth. Neurosci. 23:1995;45-64.