Role of EGR1 in Hippocampal Synaptic Enhancement Induced by Tetanic Stimulation and Amputation

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 2000 Jun 28

PMID 10871275

Citations 45

Authors

F Wei

Z C Xu

Z Qu

J Milbrandt

M Zhuo

Affiliations

Soon will be listed here.

Abstract

Hippocampal neurons fire spikes when an animal is at a particular location or performs certain behaviors in a particular place, providing a cellular basis for hippocampal involvement in spatial learning and memory. In a natural environment, spatial memory is often associated with potentially dangerous sensory experiences such as noxious or painful stimuli. The central sites for such pain-associated memory or plasticity have not been identified. Here we present evidence that excitatory glutamatergic synapses within the CA1 region of the hippocampus may play a role in storing pain-related information. Peripheral noxious stimulation induced excitatory postsynaptic potentials (EPSPs) in CA1 pyramidal cells in anesthetized animals. Tissue/nerve injury caused a rapid increase in the level of the immediate-early gene product Egr1 (also called NGFI-A, Krox24, or zif/268) in hippocampal CA1 neurons. In parallel, synaptic potentiation induced by a single tetanic stimulation (100 Hz for 1 s) was enhanced after the injury. This enhancement of synaptic potentiation was absent in mice lacking Egr1. Our data suggest that Egr1 may act as an important regulator of pain-related synaptic plasticity within the hippocampus.

Citing Articles

Cortical Tagged Synaptic Long-Term Depression in the Anterior Cingulate Cortex of Adult Mice.

Liu W, Chen Q, Li X, Zhou Z, Zhuo M J Neurosci. 2024; 44(35).

PMID: 39054067 PMC: 11358531. DOI: 10.1523/JNEUROSCI.0028-24.2024.

The neurobiology of irritable bowel syndrome.

Mayer E, Ryu H, Bhatt R Mol Psychiatry. 2023; 28(4):1451-1465.

PMID: 36732586 PMC: 10208985. DOI: 10.1038/s41380-023-01972-w.

Glucose Homeostasis and Pancreatic Islet Size Are Regulated by the Transcription Factors Elk-1 and Egr-1 and the Protein Phosphatase Calcineurin.

Thiel G, Rossler O Int J Mol Sci. 2023; 24(1).

PMID: 36614256 PMC: 9821712. DOI: 10.3390/ijms24010815.

MicroRNA-206 down-regulated human umbilical cord mesenchymal stem cells alleviate cognitive decline in D-galactose-induced aging mice.

Zhang Y, Deng W, Wang W, Song A, Mukama O, Deng S Cell Death Discov. 2022; 8(1):304.

PMID: 35781287 PMC: 9250929. DOI: 10.1038/s41420-022-01097-z.

lncRNA-Associated Competitive Endogenous RNA Regulatory Network in an Aβ-Induced AD Mouse Model Treated with Tripterygium Glycoside.

Tang L, Xiang Q, Xiang J, Li J Neuropsychiatr Dis Treat. 2021; 17:1531-1541.

PMID: 34040378 PMC: 8141406. DOI: 10.2147/NDT.S310271.

References

Wei F, Li P, Zhuo M . Loss of synaptic depression in mammalian anterior cingulate cortex after amputation. J Neurosci. 1999; 19(21):9346-54. PMC: 6782899. View

Malenka R, Nicoll R . Long-term potentiation--a decade of progress?. Science. 1999; 285(5435):1870-4. DOI: 10.1126/science.285.5435.1870. View

Gol A, Faibisch G . Hippocampectomy for relief of intractable pain. Tex Med. 1966; 62(10):76-9. View

Berger T, ALGER B, Thompson R . Neuronal substrate of classical conditioning in the hippocampus. Science. 1976; 192(4238):483-5. DOI: 10.1126/science.1257783. View

Jackson W, Regestein Q . Hippocampal lesions impair prolonged titrated avoidance by rhesus monkeys. Exp Neurol. 1979; 63(1):28-34. DOI: 10.1016/0014-4886(79)90183-3. View

Berger T, Laham R, Thompson R . Hippocampal unit-behavior correlations during classical conditioning. Brain Res. 1980; 193(1):229-48. DOI: 10.1016/0006-8993(80)90960-9. View

Berger T, Rinaldi P, Weisz D, Thompson R . Single-unit analysis of different hippocampal cell types during classical conditioning of rabbit nictitating membrane response. J Neurophysiol. 1983; 50(5):1197-219. DOI: 10.1152/jn.1983.50.5.1197. View

Plaznik A, Danysz W, Kostowski W . Some behavioral effects of microinjections of noradrenaline and serotonin into the hippocampus of the rat. Physiol Behav. 1983; 31(5):625-31. View

SINCLAIR J, Lo G . Morphine, but not atropine, blocks nociceptor-driven activity in rat dorsal hippocampal neurones. Neurosci Lett. 1986; 68(1):47-50. DOI: 10.1016/0304-3940(86)90227-2. View

10.

Brankack J, Buzsaki G . Hippocampal responses evoked by tooth pulp and acoustic stimulation: depth profiles and effect of behavior. Brain Res. 1986; 378(2):303-14. DOI: 10.1016/0006-8993(86)90933-9. View

11.

Muller R, Kubie J, RANCK Jr J . Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J Neurosci. 1987; 7(7):1935-50. PMC: 6568929. View

12.

Milbrandt J . A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor. Science. 1987; 238(4828):797-9. DOI: 10.1126/science.3672127. View

13.

Shors T, Seib T, Levine S, Thompson R . Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science. 1989; 244(4901):224-6. DOI: 10.1126/science.2704997. View

14.

Cole A, Saffen D, Baraban J, Worley P . Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature. 1989; 340(6233):474-6. DOI: 10.1038/340474a0. View

15.

Wisden W, Errington M, Williams S, Dunnett S, Waters C, Hitchcock D . Differential expression of immediate early genes in the hippocampus and spinal cord. Neuron. 1990; 4(4):603-14. DOI: 10.1016/0896-6273(90)90118-y. View

16.

Day M, Fahrner T, Aykent S, Milbrandt J . The zinc finger protein NGFI-A exists in both nuclear and cytoplasmic forms in nerve growth factor-stimulated PC12 cells. J Biol Chem. 1990; 265(25):15253-60. View

17.

Mack K, Day M, Milbrandt J, Gottlieb D . Localization of the NGFI-A protein in the rat brain. Brain Res Mol Brain Res. 1990; 8(2):177-80. DOI: 10.1016/0169-328x(90)90062-i. View

18.

Morgan J, Curran T . Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Annu Rev Neurosci. 1991; 14:421-51. DOI: 10.1146/annurev.ne.14.030191.002225. View

19.

Squire L . The medial temporal lobe memory system. Science. 1991; 253(5026):1380-6. DOI: 10.1126/science.1896849. View

20.

Dudek S, Bear M . Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci U S A. 1992; 89(10):4363-7. PMC: 49082. DOI: 10.1073/pnas.89.10.4363. View