Induction of Glycerol Phosphate Dehydrogenase Gene Expression During Seizure and Analgesia

Abstract: Using mRNA differential display, we found that the gene for NAD+‐dependent glycerol phosphate dehydrogenase (GPDH; EC 1.1.1.8) is induced in rat brain following seizure activity. Northern blot and in situ hybridization analysis confirmed the differential display results; they also showed, in a separate model of neuronal activation, that after thermal noxious stimulation of the hind‐paws, a similar increase in GPDH mRNA occurs in the areas of somatotopic projection in the lumbar spinal cord. Surprisingly, administration of analgesic doses of morphine or the nonsteroidal antiinflammatory drugs aspirin, metamizol (dipyrone), and indomethacin also increased GPDH mRNA levels in rat spinal cord. The opioid receptor antagonist naloxone completely blocked morphine induction of GPDH but had no effect on GPDH induction by noxious heat stimulation or metamizol treatment, implicating different mechanisms of GPDH induction. Nevertheless, in all cases, induction of the GPDH gene requires adrenal steroids and new protein synthesis, as the induction was blocked in adrenalectomized rats and by cycloheximide treatment, respectively. Our results suggest that the induction of the GPDH gene upon peripheral noxious stimulation is related to the endogenous response to pain as it is mimicked by exogenously applied analgesic drugs.

[1]  U. Staubli,et al.  The polo‐like protein kinases Fnk and Snk associate with a Ca2+‐ and integrin‐binding protein and are regulated dynamically with synaptic plasticity , 1999, The EMBO journal.

[2]  U. Staubli,et al.  Pim kinase expression is induced by LTP stimulation and required for the consolidation of enduring LTP , 1999, The EMBO journal.

[3]  I. Fernaud,et al.  Metamizol potentiates morphine effects on visceral pain and evoked c-Fos immunoreactivity in spinal cord. , 1998, European journal of pharmacology.

[4]  J. Lucas,et al.  Peripheral Noxious Stimulation Induces CREM Expression in Dorsal Horn: Involvement of Glutamate , 1997, The European journal of neuroscience.

[5]  G. Koob,et al.  Activation of corticotropin-releasing factor in the limbic system during cannabinoid withdrawal. , 1997, Science.

[6]  P. Chambon,et al.  TIF2, a 160 kDa transcriptional mediator for the ligand‐dependent activation function AF‐2 of nuclear receptors. , 1996, The EMBO journal.

[7]  S. Ho,et al.  Spinal actions of nonsteroidal anti-inflammatory drugs. , 1996, Acta anaesthesiologica Sinica.

[8]  Thorsten Heinzel,et al.  A CBP Integrator Complex Mediates Transcriptional Activation and AP-1 Inhibition by Nuclear Receptors , 1996, Cell.

[9]  J. Walker.  Australasian Society of Clinical and Experimental Pharmacologists and Toxicologists, 1994: NSAID: AN UPDATE ON THEIR ANALGESIC EFFECTS , 1995 .

[10]  P. Vyas,et al.  The mode of action of aspirin-like drugs: effect on inducible nitric oxide synthase. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[11]  U. Frey,et al.  Somatodendritic expression of an immediate early gene is regulated by synaptic activity. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[12]  U. Danesch,et al.  Arachidonic acid increases c-fos and Egr-1 mRNA in 3T3 fibroblasts by formation of prostaglandin E2 and activation of protein kinase C. , 1994, The Journal of biological chemistry.

[13]  S. Ghosh,et al.  Inhibition of NF-kappa B by sodium salicylate and aspirin. , 1994, Science.

[14]  C. Finch,et al.  Rapid increase in glycerol phosphate dehydrogenase mRNA in adult rat brain: a glucocorticoid-dependent stress response. , 1994, Neuroendocrinology.

[15]  J. Besson,et al.  Chronic treatments with aspirin or acetaminophen reduce both the development of polyarthritis and Fos-like immunoreactivity in rat lumbar spinal cord , 1994, Pain.

[16]  M. Zimmermann,et al.  Application of morphine prior to noxious stimulation differentially modulates expression of Fos, Jun and Krox-24 proteins in rat spinal cord neurons , 1994, Neuroscience.

[17]  J. Reich,et al.  Identification of differentially expressed mRNA species by an improved display technique (DDRT-PCR). , 1993, Nucleic acids research.

[18]  Carol A. Barnes,et al.  Expression of a mitogen-inducible cyclooxygenase in brain neurons: Regulation by synaptic activity and glucocorticoids , 1993, Neuron.

[19]  G. Barbany,et al.  Adrenalectomy attenuates kainic acid-elicited increases of messenger RNAs for neurotrophins and their receptors in the rat brain , 1993, Neuroscience.

[20]  M. Colado,et al.  Molecular mechanisms of pain: Serotonin1A receptor agonists trigger transactivation by c-fos of the prodynorphin gene in spinal cord neurons , 1993, Neuron.

[21]  T. Eling,et al.  Modulation of c-jun and jun-B messenger RNA and inhibition of DNA synthesis by prostaglandin E2 in Syrian hamster embryo cells. , 1992, Cancer research.

[22]  A. Pardee,et al.  Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. , 1992, Science.

[23]  W. Fan,et al.  Cloning of a mu-class glutathione S-transferase gene and identification of the glucocorticoid regulatory domains in its 5' flanking sequence. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[24]  K. Lyford,et al.  Tissue- and cell-specific expression of human sn-glycerol-3-phosphate dehydrogenase in transgenic mice. , 1992, Nucleic acids research.

[25]  Xiaohua Li,et al.  Adrenalectomy Potentiates Immediate Early Gene Expression in Rat Brain , 1992, Journal of neurochemistry.

[26]  J. Licinio,et al.  Induction of constitutive heat shock protein 73 mRNA in the dentate gyrus by seizures. , 1992, Brain research. Molecular brain research.

[27]  C. Kuhn,et al.  Ontogeny of μ- and κ-Opiate Receptor Control of the Hypothalamo-Pituitary-Adrenal Axis in Rats , 1991 .

[28]  Richard E. Miller,et al.  Glycerol 3-phosphate dehydrogenase gene expression in cultured 3T3-L1 adipocytes: regulation by insulin, dexamethasone and dibutyryl cAMP at the level of mRNA abundancem transcription and mRNA stability , 1991, Molecular and Cellular Endocrinology.

[29]  J. Lucas,et al.  Co-induction of jun B and c-fos in a subset of neurons in the spinal cord. , 1991, Oncogene.

[30]  H. Thoenen,et al.  Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non‐NMDA glutamate receptors. , 1990, The EMBO journal.

[31]  K. Lyford,et al.  Sequence conservation and structural organization of the glycerol-3-phosphate dehydrogenase promoter in mice and humans , 1990, Molecular and cellular biology.

[32]  M. Karin,et al.  Transcriptional interference between c-Jun and the glucocorticoid receptor: Mutual inhibition of DNA binding due to direct protein-protein interaction , 1990, Cell.

[33]  J. Lindstrom,et al.  Nucleotide sequence of the human nicotinic acetylcholine receptor β2 subunity gene , 1990 .

[34]  A I Basbaum,et al.  Systemic morphine suppresses noxious stimulus-evoked Fos protein-like immunoreactivity in the rat spinal cord , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  T. Curran,et al.  Regulation of proenkephalin by Fos and Jun. , 1989, Science.

[36]  K. Noguchi,et al.  Prepro-VIP and preprotachykinin mRNAs in the rat dorsal root ganglion cells following peripheral axotomy. , 1989, Brain research. Molecular brain research.

[37]  J. de Vellis,et al.  Differential regulation of oligodendrocyte markers by glucocorticoids: post-transcriptional regulation of both proteolipid protein and myelin basic protein and transcriptional regulation of glycerol phosphate dehydrogenase. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[38]  M. Iadarola,et al.  Differential activation of spinal cord dynorphin and enkephalin neurons during hyperalgesia: evidence using cDNA hybridization , 1988, Brain Research.

[39]  R. J. Mullen,et al.  Neuronal influence on glial enzyme expression: Evidence from chimeric mouse cerebellum , 1988, Neuron.

[40]  H. Weintraub,et al.  Expression of a single transfected cDNA converts fibroblasts to myoblasts , 1987, Cell.

[41]  S. Hunt,et al.  Induction of c-fos-like protein in spinal cord neurons following sensory stimulation , 1987, Nature.

[42]  J. Vane,et al.  Inflammation and the mechanism of action of anti‐inflammatory drugs , 1987, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[43]  T. Curran,et al.  Mapping patterns of c-fos expression in the central nervous system after seizure. , 1987, Science.

[44]  A. F. Nicola,et al.  Glucocorticoid Regulation of Glycerol Phosphate Dehydrogenase and Ornithine Decarboxylase Activities in the Spinal Cord of the Rat , 1987, Journal of neurochemistry.

[45]  L. Kozak,et al.  Primary structure of the mouse glycerol-3-phosphate dehydrogenase gene. , 1986, The Journal of biological chemistry.

[46]  W. Addison,et al.  Nucleotide sequences required for the regulation of a rat alpha 2u-globulin gene by glucocorticoids , 1986, Molecular and cellular biology.

[47]  E. Laska,et al.  The correlation between blood levels of ibuprofen and clinical analgesic response , 1986, Clinical pharmacology and therapeutics.

[48]  I. Pang,et al.  Morphine and norepinephrine but not 5-hydroxytryptamine and γ-aminobutyric acid inhibit the potassium-stimulated release of substance P from rat spinal cord slices , 1986, Brain Research.

[49]  J. P. Schwartz,et al.  Permissive effect of dexamethasone on the increase of proenkephalin mRNA induced by depolarization of chromaffin cells. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[50]  J. de Vellis,et al.  Glucocorticoids regulate the transcription of glycerol phosphate dehydrogenase in cultured glial cells. , 1985, The Journal of biological chemistry.

[51]  C. Dani,et al.  Various rat adult tissues express only one major mRNA species from the glyceraldehyde-3-phosphate-dehydrogenase multigenic family. , 1985, Nucleic acids research.

[52]  N. Weiner,et al.  Regulation of tyrosine hydroxylase mRNA by glucocorticoid and cyclic AMP in a rat pheochromocytoma cell line. Isolation of a cDNA clone for tyrosine hydroxylase mRNA. , 1983, The Journal of biological chemistry.

[53]  G. Ailhaud,et al.  Lipogenic and mitogenic effects of insulin during conversion of Ob17 cells to adipose-like cells , 1983, Molecular and Cellular Endocrinology.

[54]  L. Kozak,et al.  The role of mRNA levels and cellular localization in controlling sn-glycerol-3-phosphate dehydrogenase expression in tissues of the mouse. , 1981, The Journal of biological chemistry.

[55]  David S. Maxwell,et al.  Immunocytochemical localization of glycerol-3-phosphate dehydrogenase in rat oligodendrocytes , 1980, Brain Research.

[56]  H. Green,et al.  Participation of one isozyme of cytosolic glycerophosphate dehydrogenase in the adipose conversion of 3T3 cells. , 1979, The Journal of biological chemistry.

[57]  J. de Vellis,et al.  Glucocorticoid regulation in rat brain cell cultures. Hydrocortisone increases the rate of synthesis of glycerol phosphate dehydrogenase in C6 glioma cells. , 1978, The Journal of biological chemistry.

[58]  J. de Vellis,et al.  Modulation of the hydrocortisone induction of glycerol phosphate dehydrogenase by N6,O2'-dibutyryl cyclic AMP, norepinephrine, and isobutylmethylxanthine in rat brain cell cultures. , 1978, The Journal of biological chemistry.

[59]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[60]  M. Nirenberg,et al.  Dual regulation of adenylate cyclase accounts for narcotic dependence and tolerance. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[61]  J. Vellis,et al.  Cortisol induction of glycerol phosphate dehydrogenase in a rat brain tumour cell line , 1974, Nature.

[62]  S. Shnider,et al.  Relationship of pentazocine plasma levels to pharmacological activity in man , 1969, Clinical pharmacology and therapeutics.

[63]  Berkowitz Ba,et al.  Relationship of pentazocine plasma levels to pharmacological activity in man. , 1969 .

[64]  J. Vellis,et al.  HORMONAL CONTROL OF GLYCEROLPHOSPHATE DEHYDROGENASE IN THE RAT BRAIN 1 , 1968, Journal of neurochemistry.

[65]  R. H. Laatsch,et al.  GLYCEROL PHOSPHATE DEHYDROGENASE ACTIVITY OF DEVELOPING RAT CENTRAL NERVOUS SYSTEM * , 1962, Journal of neurochemistry.

[66]  J. Walker.  NSAID: an update on their analgesic effects. , 1995, Clinical and experimental pharmacology & physiology.

[67]  C. Kuhn,et al.  Ontogeny of mu- and kappa-opiate receptor control of the hypothalamo-pituitary-adrenal axis in rats. , 1991, Endocrinology.

[68]  N. Ruiz-Bravo,et al.  Induction of tyrosine aminotransferase mRNA by glucocorticoids and cAMP in fetal rat liver. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[69]  E. C. Lin,et al.  Glycerol utilization and its regulation in mammals. , 1977, Annual review of biochemistry.

[70]  J. de Vellis,et al.  Age-dependent changes in the regulation of glycerolphosphate dehydrogenase in the rat brain and in a glial cell line. , 1973, Progress in brain research.