Correlations between immediate early gene induction and the persistence of long-term potentiation

The duration of long-term potentiation in the dentate gyrus of awake rats was examined following systematic manipulation of the number of stimulus trains delivered. This was correlated with the induction of immediate early genes in separate groups of animals given identical stimulus regimes. Following 10 trains of stimulation, long-term potentiation decayed with a time constant of up to several days (long-term potentiation 2), and this correlated with the appearance of an increase in the messenger RNA and protein levels of zif/268. Increasing the number of stimulus trains resulted in a greater probability of eliciting long-term potentiation with a time constant of several weeks (long-term potentiation 3), as well as increasing the induction of zif/268, c-Jun, Jun-B, Jun-D and Fos-related proteins. When 10 trains were delivered repeatedly on up to five consecutive days, only the zif/268 protein levels showed associated changes. These data provide support for the hypothesis that long-term potentiation 3 involves mechanisms additional to those for long-term potentiation 2. One possible mechanism is altered gene expression, initiated by immediate early gene transcription factors such as zif/268 and possibly homo- or heterodimers of Fos and Jun family members, that then contributes to the stabilization or maintenance of long-term potentiation 3.

[1]  W. Abraham,et al.  Inhibition of protein synthesis in the dentate gyrus, but not the entorhinal cortex, blocks maintenance of long-term potentiation in rats , 1989, Neuroscience Letters.

[2]  M. Dragunow,et al.  Kindling stimulation induces c-fos protein(s) in granule cells of the rat dentate gyrus , 1987, Nature.

[3]  R. Racine,et al.  The effects of repeated induction of long-term potentiation in the dentate gyrus , 1985, Brain Research.

[4]  I. Verma,et al.  Induction of proto-oncogene JUN/AP-1 by serum and TPA , 1988, Nature.

[5]  Eileen D. Adamson,et al.  A zinc finger-encoding gene coregulated with c-fos during growth and differentiation, and after cellular depolarization , 1988, Cell.

[6]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[7]  M. Krug,et al.  Transient increase of raf protein kinase-like immunoreactivity in the rat dentate gyrus during long-term potentiation , 1990, Neuroscience Letters.

[8]  G. Lynch,et al.  Stable hippocampal long-term potentiation elicited by ‘theta’ pattern stimulation , 1987, Brain Research.

[9]  J. Milbrandt,et al.  Structure of the NGFI-A gene and detection of upstream sequences responsible for its transcriptional induction by nerve growth factor. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[10]  L. Lau,et al.  A gene activated in mouse 3T3 cells by serum growth factors encodes a protein with "zinc finger" sequences. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[11]  R. Racine,et al.  Long-term potentiation phenomena in the rat limbic forebrain , 1983, Brain Research.

[12]  R. Bravo,et al.  Expression of different Jun and Fos proteins during the G0-to-G1 transition in mouse fibroblasts: in vitro and in vivo associations , 1991, Molecular and cellular biology.

[13]  D. Nathans,et al.  jun-D: a third member of the jun gene family. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[14]  B. Varnum,et al.  Tumor promoter-inducible genes are differentially expressed in the developing mouse , 1988, Molecular and cellular biology.

[15]  C. Barnes Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. , 1979, Journal of comparative and physiological psychology.

[16]  K. Jeffery,et al.  Induction of Fos-like immunoreactivity and the maintenance of long-term potentiation in the dentate gyrus of unanesthetized rats. , 1990, Brain research. Molecular brain research.

[17]  R. Douglas,et al.  High-frequency discharge of dentate granule cells, but not long-term potentiation, induces c-fos protein. , 1988, Brain research.

[18]  T. Bliss,et al.  Heterosynaptic changes accompany long‐term but not short‐term potentiation of the perforant path in the anaesthetized rat. , 1985, The Journal of physiology.

[19]  M. Krug,et al.  Anisomycin blocks the late phase of long-term potentiation in the dentate gyrus of freely moving rats , 1984, Brain Research Bulletin.

[20]  P. Chomczyński,et al.  Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. , 1987, Analytical biochemistry.

[21]  Philip Goelet,et al.  The long and the short of long–term memory—a molecular framework , 1986, Nature.

[22]  T. Bliss,et al.  Differential expression of immediate early genes in the hippocampus and spinal cord , 1990, Neuron.

[23]  W. Abraham,et al.  Correlation between the induction of an immediate early gene,zif/268, and long-term potentiation in the dentate gyrus , 1992, Brain Research.

[24]  L. Lau,et al.  A gene activated by growth factors is related to the oncogene v-jun. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[25]  T. Shors,et al.  A negative correlation between the induction of long-term potentiation and activation of immediate early genes. , 1991, Brain research. Molecular brain research.

[26]  W. Abraham,et al.  Differential expression of immediate early genes after hippocampal long-term potentiation in awake rats. , 1993, Brain research. Molecular brain research.

[27]  James I. Morgan,et al.  Role of ion flux in the control of c-fos expression , 1986, Nature.

[28]  Andrew J. Cole,et al.  Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation , 1989, Nature.

[29]  R. Bravo,et al.  Selective expression of Jun proteins following axotomy and axonal transport block in peripheral nerves in the rat: evidence for a role in the regeneration process , 1991, Brain Research.

[30]  F. Dautry,et al.  Northern blot normalization with a 28S rRNA oligonucleotide probe. , 1989, Nucleic acids research.

[31]  Y. Nakabeppu,et al.  DNA binding activities of three murine Jun proteins: Stimulation by Fos , 1988, Cell.

[32]  W. Abraham,et al.  Long-term potentiation and the induction of c-fos mRNA and proteins in the dentate gyrus of unanesthetized rats , 1989, Neuroscience Letters.

[33]  G. V. Goddard,et al.  Maintenance of long-term potentiation in rat dentate gyrus requires protein synthesis but not messenger RNA synthesis immediately post-tetanization , 1989, Neuroscience.

[34]  P. Lemaire,et al.  Two mouse genes encoding potential transcription factors with identical DNA-binding domains are activated by growth factors in cultured cells. , 1988, Proceedings of the National Academy of Sciences of the United States of America.