64
Views
7
CrossRef citations to date
0
Altmetric
Review

Transcriptional mechanisms underlying neuropathic pain: DREAM, transcription factors and future pain management?

&
Pages 677-689 | Published online: 10 Jan 2014

References

  • Dib-Hajj SD, Fjell J, Cummins TR etal. Plasticity of sodium channel expression in DRG neurons in the chronic constriction injury model of neuropathic pain. Pain 83(3), 591–600 (1999).
  • Boucher TJ, Okuse K, Bennett DL, Munson JB, Wood JN, McMahon SB. Potent analgesic effects of GDNF in neuropathic pain states. Science 290(5489), 124–127 (2000).
  • •• The analgesic effects of GDNF in neuropathic pain models and the ability of GDNF to reverse an established neuropathy are described. Normal expression of several sodium channel subunits is restored following administration of GDNF.
  • Decosterd I, Ji RR, Abdi S, Tate S, Woolf CJ. The pattern of expression of the voltage-gated sodium channels Na(v)1.8 and Na(v)1.9 does not change in uninjured primary sensory neurons in experimental neuropathic pain models. Pain 96(3), 269–277 (2002).
  • Novakovic SD, Tzoumaka E, McGivern JG et al Distribution of the tetrodotoxin-resistant sodium channel PN3 in rat sensory neurons in normal and neuropathic conditions. j Neurosci. 18(6), 2174–2187 (1998).
  • Shah BS, Stevens EB, Gonzalez MI et al. beta3, a novel auxiliary subunit for the voltage-gated sodium channel, is expressed preferentially in sensory neurons and is upregulated in the chronic constriction injury model of neuropathic pain. Eur. Neurosci 12(11), 3985–3990 (2000).
  • Saegusa H, Kurihara T, Zong S et al Suppression of inflammatory and neuropathic pain symptoms in mice lacking the N-type Ca2+ channel. EMI30 20(10), 2349–2356 (2001).
  • Cizkova D, Marsala M, Stauderman K, Yaksh TL. Calcium channel alB subunit in spinal cord/DRG of normal and nerve-injured rats. floceeclings of the 9th World COIVESS on Pain. Vienna, Austria, 134 (1999).
  • Luo ZD, Chaplan SR, Higuera ES et al Upregulation of dorsal root ganglion (alpha)2(delta) calcium channel subunit and its correlation with allodynia in spinal nerve-injured rats. J. Neurosci 21(6), 1868–1875 (2001).
  • Gee NS, Brown JP, Dissanayake VU, Offord J, Thurlow R, Woodruff GN. The novel anticonvulsant drug, gabapentin (Neurontin), binds to the alpha2delta subunit of a calcium channel. j Biol. Chem. 271(10), 5768–5776 (1996).
  • Ishikawa K, Tanaka M, Black JA, Waxman SG. Changes in expression of voltage-gated potassium channels in dorsal root ganglion neurons following axotomy. Muscle Nerve 22(4), 502–507 (1999).
  • Kim DS, Lee SJ, Park SY et al. Differentially expressed genes in rat dorsal root ganglia following peripheral nerve injury. Neummport 12(15), 3401–3405 (2001).
  • Bradbury EJ, Bumstock G, McMahon SB. The expression of P2X3 purinoreceptors in sensory neurons: effects of axotomy and glial-derived neurotrophic factor. Mal Cell Neurosci 12(4/5), 256–268 (1998).
  • Novakovic SD, Kassotakis LC, Oglesby TB et al. Immunocytochemical localization of P2X3 purinoceptors in sensory neurons in naive rats and following neuropathic injury. Pain 80(1–2), 273–282 (1999).
  • Romero MI, Rangappa N, Garry MG, Smith GM. Functional regeneration of chronically injured sensory afferents into adult spinal cord after neurotrophin gene therapy. Neurosci. 21(21), 8408–8416 (2001).
  • Heppenstall PA, Lewin GR. BDNF but not NT-4 is required for normal flexion reflex plasticity and function. Proc. Natl Acad. Li. USA 98(14), 8107–8112 (2001).
  • Koltzenburg M, Bennett DL, Shelton DL, McMahon SB. Neutralization of endogenous NGF prevents the sensitization of nociceptors supplying inflamed skin. Eur. j Neurosci. 11(5), 1698–1704 (1999).
  • Romero MI, Rangappa N, Li L, Lightfoot E, Garry MG, Smith GM. Extensive sprouting of sensory afferents and hyperalgesia induced by conditional expression of nerve growth factor in the adult spinal cord. J. Neurosci 20(12), 4435–4445 (2000).
  • Fukuoka T, Kondo E, Dai Y, Hashimoto N, Noguchi K Brain-derived neurotrophic factor increases in the uninjured dorsal root ganglion neurons in selective spinal nerve ligation model. Neumsci. 21(13), 4891–4900 (2001).
  • Zhou XF, Chie ET, Deng YS et al Injured primary sensory neurons switch phenotype for brain-derived neurotrophic factor in the rat. Neuroscience 92 (3), 841–853 (1999) .
  • Shen H, Chung JM, Chung K. Expression of neurotrophin mRNAs in the dorsal root ganglion after spinal nerve injury. Brain Res. Mal Brain Res 64(2), 186–192 (1999).
  • Shen H, Chung JM, Coggeshall RE, Chung K. Changes in trkA expression in the dorsal root ganglion after peripheral nerve injury. Exp. Brain Res. 127(2), 141–146 (1999).
  • Bennett DL, Boucher TJ, Armanini MP et al The glial cell line-derived neurotrophic factor family receptor components are differentially regulated within sensory neurons after nerve injury. Neurosci 20(1), 427–437 (2000).
  • Nahin RL, Ren K, De Leon M, Ruda M. Primary sensory neurons exhibit altered gene expression in a rat model of neuropathic pain. Pain 58(1), 95–108 (1994).
  • Martinez-Caro L, Laird JM. Allodynia and hyperalgesia evoked by sciatic mononeuropathy in NKI receptor knockout mice. Neuroreportll (6), 1213–1217 (2000).
  • Na HS, Kim HJ, Sung B et al. Decrease in spinal CGRP and substance P is not related to neuropathic pain in a rat model. Neuromport12(1), 175–178 (2001).
  • Zhang YZ, Hannibal J, Zhao Q et al Pituitary adenyl cyclase activating peptide expression in the rat dorsal root ganglia: upregulation after peripheral nerve injury. Neuroscience 74 (4), 1099–1110 (1996) .
  • Marchand JE, Cepeda MS, Carr DB, Wurm WH, Kream RM. Alterations in neuropeptide Y, tyrosine hydroxylase and Y-receptor subtype distribution following spinal nerve injury to rats. Pain 79(2-3), 187–200 (1999).
  • Kerr BJ, Cafferty WB, Gupta YK etal. Galanin knockout mice reveal nociceptive deficits following peripheral nerve injury. Eur. j Neurosci 12(3), 793–802 (2000).
  • Shi TJ, Zhang X, Berge OG, Erickson JC, Palmiter RD, Hokfelt T Effect of peripheral axotomy on dorsal root ganglion neurone phenotype and autonomy behaviour in neuropeptideY-deficient mice. Rebut. Pept. 75–76,161-173 (1998).
  • Naveilhan P, Hassani H, Lucas G et al Reduced antinociception and plasma extravasation in mice lacking a neuropeptide Y receptor. Nature 409(6819), 513–517 (2001).
  • Dickinson T, Fleetwood-Walker SM. VIP and PACAP: very important in pain? Bends Pharmacol Sci. 20(8), 324–329 (1999).
  • Draisci G, Kajander KC, Dubner R, Bennett GJ, Iadarola MJ. Upregulation of opioid gene expression in spinal cord evoked by experimental nerve injuries and inflammation. Brain Res. 560 (1-2), 186–192 (1991).
  • Wang Z, Gardell LR, Ossipov MET et al Pronociceptive actions of dynorphin maintain chronic neuropathic pain. Neurosci. 21(5), 1779–1786 (2001).
  • Zhang X, Bao L, Shi TJ, Ju G, Elde R, Hokfelt T Downregulation of mu-opioid receptors in rat and monkey dorsal root ganglion neurons and spinal cord after peripheral axotomy. Neuroscience 82(1), 223–240 (1998).
  • Xu XJ, Puke MJ, Verge VM, Wiesenfeld- Hallin Z, Hughes J, Hokfelt T. Upregulation of cholecystokinin in primary sensory neurons is associated with morphine insensitivity in experimental neuropathic pain in the rat. Neurosci. Lett. 152(1–2), 129–132 (1993).
  • Antunes Bras JM, Laporte AM, Benoliel JJ cholecystokinin neurotransmission in the rat spinal cord. I Neurochem. 72(2), 858–867 (1999).
  • Fukuoka T, Tokunaga A, Kondo E, Miki K, Tachibana T, Noguchi K. Change in mRNAs for neuropeptides and the GABA(A) receptor in dorsal root ganglion neurons in a rat experimental neuropathic pain model. Pain 78(1), 13–26 (1998).
  • Wu GY, Deisseroth K, Tsien RVV. Activity- dependent CREB phosphorylation: convergence of a fast, sensitive calmodulin kinase pathway and a slow, less sensitive mitogen-activated protein kinase pathway. Proc. Nati Acad. Sci. USA 98(5), 2808–2813 (2001).
  • Ma W Quirion R. Increased phosphorylation of cyclic AMP response element-binding protein (CREB) in the superficial dorsal horn neurons following partial sciatic nerve ligation. Pain 93 (3), 295–301 (2001).
  • Ma W, Eisenach JC. Morphological and pharmacological evidence for the role of peripheral prostaglandins in the pathogenesis of neuropathic pain. Eur: Neumsci. 15(6), 1037–1047 (2002).
  • Messersmith DJ, Kim DJ, Iadarola MJ. Transcription factor regulation of prodynorphin gene expression following rat hindpaw inflammation. Brain Res. Mol Brain Res. 53(1–2), 260–269 (1998).
  • Hansen TV, Rehfeld JF, Nielsen PC. Mitogen-activated protein kinase and protein kinase A signaling pathways stimulate cholecystokinin transcription via activation of cyclic adenosine 3%5 monophosphate response element-binding protein. Mol Endocrinol 13(3), 466–475 (1999).
  • Freeland K, Liu YZ, Latchman DS. Distinct signalling pathways mediate the cAMP response element (CRE)-dependent activation of the calcitonin gene-related peptide gene promoter by cAMP and nerve growth factor. Biochem. I 345 (2), 233–238 (2000).
  • Zachariou V, Georgescu D, Kansal L, Merriam P, Picciotto MR. Galanin receptor 1 gene expression is regulated by cyclic AMP through a CREB-dependent mechanism. Neurochem. 76(1), 191–200 (2001).
  • Shieh PB, Hu SC, Bobb K, Timmusk T, Ghosh A. Identification of a signaling pathway involved in calcium regulation of BDNF expression. Neuron 20(4), 727–740 (1998).
  • Ahn S, Olive M, Aggarwal S, Krylov D, Ginty DD, Vinson C. A dominant-negative inhibitor of CREB reveals that it is a general mediator of stimulus-dependent transcription of c-fos. Mal Cell Biol. 18(2), 967–977 (1998).
  • Lonze BE, Riccio A, Cohen S, Ginty DD. Apoptosis, axonal growth defects and degeneration of peripheral neurons in mice lacking CREB. Neuron 34(3), 371–385 (2002).
  • White DM, Walker S, Brenneman DE, Gozes I. CREB contributes to the increased neurite outgrowth of sensory neurons induced by vasoactive intestinal polypeptide and activity-dependent neurotrophic factor. Bmin Res 868(1), 31–38 (2000).
  • Neumann S, Bradke F, Tessier-Lavigne M, Basbaum Pd. Regeneration of sensory axons within the injured spinal cord induced by intraganglionic cAMP elevation. Neuron 34(6), 885–893 (2002).
  • Qiu J, Cai D, Dai H et al. Spinal axon regeneration induced by elevation of cyclic AMP Neuron 34(6), 895–903 (2002).
  • Mayr B, Montminy M. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev Mal Cell Biol. 2(8), 599–609 (2001).
  • Naranjo JR, Mellstrom B, Carrion AM, Lucas JJ, Foulkes NS, Sassone-Corsi Peripheral noxious stimulation induces CREM expression in dorsal horn: involvement of glutamate. Eur j Neurosci. 9(12), 2778–2783 (1997).
  • Hunt SP, Pini A, Evan G. Induction of c- fos-like protein in spinal cord neurons following sensory stimulation. Nature 328(6131), 632–634 (1987).
  • Ma QP, Woolf CJ. Basal and touch-evoked fos-like immunoreactivity during experimental inflammation in the rat. Pain 67(2-3), 307–316 (1996).
  • Catheline G, Le Guen S, Besson JM. Effects of opioid receptor antagonists on the effects of iv. morphine on carrageenin evoked c-Fos expression in the superficial dorsal horn of the rat spinal cord. Brain Res. 824(1), 105–111 (1999).
  • Kajander KC, Madsen AM, Iadarola MJ, Draisci G, Wakisaka S. Fos-like immunoreactivity increases in the lumbar spinal cord following a chronic constriction injury to the sciatic nerve of rat. Neurosci. Lett. 206(1), 9–12 (1996).
  • Catheline G, Le Guen S, Honore P, Besson JM. Are there long-term changes in the basal or evoked Fos expression in the dorsal horn of the spinal cord of the mononeuropathic rat? Pain 80 (1–2), 347–357 (1999).
  • Todd AJ, Spike RC, Brodbelt AR, Price RF, Shehab SA. Some inhibitory neurons in the spinal cord develop c-fos-immunoreactivity after noxious stimulation. Neuroscience 63(3), 805–816 (1994).
  • Hunter JC, Woodburn VL, Durieux C, Pettersson EK, Poat JA, Hughes J. c-fos antisense oligodeoxynucleotide increases formalin-induced nociception and regulates preprodynorphin expression. Neumscience 65(2), 485–492 (1995).
  • •One of the few studies which directly addresses the effect of c-fos expression on nociception. Using antisense knock-down technique, this study shows that reducing c-fos expression enhances forrnalin-induced pain behavior. The downregulation of spinal prod3morphin expression in antisense-treated animals is suggested to be responsible for the increased pain behavior.
  • Herdegen T, Rudiger S, Mayer B, Bravo R, Zimmermann M. Expression of nitric oxide synthase and colocalisation with Jun, Fos and Krox transcription factors in spinal cord neurons following noxious stimulation of the rat hindpaw. Brain Res. Mal Brain Res. 22(1–4), 245–258 (1994).
  • Kenney AM, Kocsis JD. Peripheral axotomy induces long-term c-Jun amino-terminal kinase-1 activation and activator protein-1 binding activity by c-Jun and junD in adult rat dorsal root ganglia in vivo. Neurosci 18(4), 1318–1328 (1998).
  • Broude E, McAtee M, Kelley MS, Bregman BS. c-Jun expression in adult rat dorsal root ganglion neurons: differential response after central or peripheral axotomy. Exp. Neural 148(1), 367–377 (1997).
  • Herdegen T, Fiallos-Estrada CE, Schmid W Bravo R, Zimmermann M. The transcription factors c-JUN, JUN D and CREB but not FOS and KROX-24, are differentially regulated in axotomized neurons following transection of rat sciatic nerve. Brain Res. Mal Brain Res 14(3), 155–165 (1992).
  • De Leon M, Nahin RL, Molina CA, De Leon DD, Ruda MA. Comparison of c-jun, junB and junD mRNA expression and protein in the rat dorsal root ganglia following sciatic nerve transection. Neurosci Res. 42(3), 391–401 (1995).
  • Crocker SJ, Lamba WR, Smith PD et al c-Jun mediates axotomy-induced dopamine neurone death in vivo. Proc. Nall Acad. Sci. USA 98(23), 13385–13390 (2001).
  • Sommer C, Schafers M. Painful mononeuropathy in C57BUW1d mice with delayed Wallerian degeneration: differential effects of cytokine production and nerve regeneration on thermal and mechanical hypersensitivity. Brain Res. 784(1–2), 154–162 (1998).
  • Shamash S, Reichert F, Rotshenker S. The cytokine network of Wallerian degeneration: tumor necrosis factor-alpha, interleukin-lalpha and interleukin-lbeta. Neurosci 22(8), 3052–3060 (2002).
  • Sommer C, Schafers M, Marziniak M, Toyka Ky. Etanercept reduces hyperalgesia in experimental painful neuropathy. Peripher. Nerv. Syst. 6(2), 67–72 (2001).
  • Schafers M, Brinkhoff J, Neukirchen S, Marziniak M, Sommer C. Combined epineurial therapy with neutralizing antibodies to tumor necrosis factor-alpha and interleukin-1 receptor has an additive effect in reducing neuropathic pain in mice. Neurosci Lett. 310(2–3), 113–116 (2001).
  • Murphy PG, Ramer MS, Borthwick L, Gauldie J, Richardson PM, Bisby MA. Endogenous interleukin-6 contributes to hypersensitivity to cutaneous stimuli and changes in neuropeptides associated with chronic nerve constriction in mice. Eur. Neurosci 11(7), 2243–2253 (1999).
  • Ma W, Bisby MA. Increased activation of nuclear factor kappa B in rat lumbar dorsal root ganglion neurons following partial sciatic nerve injuries. Brain Res. 797(2), 243–254 (1998).
  • Kim GM, Xu J, Xu J et al Tumor necrosis factor receptor deletion reduces nuclear factor-kappaB activation, cellular inhibitor of apoptosis protein 2 expression and functional recovery after traumatic spinal cord injury. Neumsci. 21(17), 6617–6625 (2001).
  • Sakaue G, Shimaoka M, Fukuoka T et al NF-kappa B decoy suppresses cytokine expression and thermal hyperalgesia in a rat neuropathic pain model. Neumreport 12(10), 2079–2084 (2001).
  • Carrion AM, Mellstrom B, Naranjo JR. Protein kinase A-dependent derepression of the human prodynorphin gene via differential binding to an intragenic silencer element. Mol Cell Biol. 18(12), 6921–6929 (1998).
  • •The first indication that both basal and inducible expression of the prodynorphin gene is under the regulation of a repressor element in its promoter and that a protein (complex) exists within the nucleus to mediate this repression.
  • Carrion AM, Link WA, Ledo F, Mellstrom B, Naranjo JR. DREAM is a Ca2+-regulated transcriptional repressor. Nature 398(6722), 80–84 (1999).
  • ••Cloning and characterization ofDREAM, the first calcium-binding protein shown to function as a transcription factor. DREAM can bind directly to DNA and repress transcription, both of which are abrogated when Ca2+ associates with DREAM's EF-hand domains. This study reveals a new paradigm in calcium-dependent regulation of gene expression.
  • Ledo F, Carrion AM, Link WA, Mellstrom B, Naranjo JR. DREAM-alphaCREM interaction via leucine-charged domains derepresses downstream regulatory element-dependent transcription. Mol Cell. Biol. 20 (24), 9120–9126 (2000).
  • Spreafico F, Barski JJ, Farina C, Meyer M. Mouse DREAM/calsenilin/KChIP3: gene structure, coding potential and expression. Mol. Cell. Neurosci. 17(1), 1–16 (2001).
  • Buxbaum JD, Choi EK, Luo Y et al. Calsenilin: a calcium-binding protein that interacts with the presenilins and regulates the levels of a presenilin fragment. Nat. Med. 4(10), 1177–1181 (1998).
  • •First published report of calsenilin/ DREAM as a protein identified in a yeast two-hybrid screen for presenilin binding partners. Overexpressed calsenilin binds physically with presenilins and leads to enhanced proteolysis of presenilins at the caspase-3 cleavage site. Given the association between Alzheimer's disease (AD), neurodegeneration (apoptosis) and increased calcium levels, the presenilin—calsenilin association was suggested to contribute to perturbed calcium homeostasis and apoptosis in AD.
  • An WF, Bowlby MR, Betty M et al Modulation of A-type potassium channels by a family of calcium sensors. Nature 403(6769), 553–556 (2000).
  • •Homologues of DREAM are discovered in a yeast two-hybrid screen for potassium channel interacting proteins (KChIPs). KChIP1 and 2 are identified in the screen, and database mining reveals that DREAM, renamed KCh1P3, bears significant homology
  • Cheng HY, Pitcher GM, Laviolette SR et al DREAM is a critical transcriptional repressor for pain modulation. Ce11108(1), 31–43 (2002).
  • ••The first study of DREAM function usinga genetic model. DREAM knock-out mice are generated and exhibit attenuated pain behavior in acute and chronic pain models. The hypoalgesic phenotype observed in these animals is mediated via K-opiate receptor activation, and prodynorphin mRNA and dynorphin peptides are shown to be elevated in dream/ spinal cords. This study highlights the essential contribution of DREAM to pain modulation, owing to its role as a transcriptional repressor for prodynorphin.
  • Weber P, Metzger D, Chambon Temporally controlled targeted somatic mutagenesis in the mouse brain. Eur. Neumsci. 14(11), 1777–1783 (2001).
  • Lariviere WR, Wilson SG, Laughlin TM et al Heritability of nociception. III. Genetic relationships among commonly used assays of nociception and hypersensitivity. Pain 97 (1–2), 75–86 (2002).
  • Xiao HS, Huang QH, Zhang FX et al Identification of gene expression profile of dorsal root ganglion in the rat peripheral axotomy model of neuropathic pain. Floc. Natl Acad. Sci. USA 99(12), 8360–8365 (2002).
  • Ren B, Robert F, Wyrick JJ et al Genome- wide location and function of DNA binding proteins. Science 290 (5500), 2306–2309 (2000).
  • •The first report of combining chromatin imrnunoprecipitation with DNA microarray analysis to study DNA-transcription factor interaction across the entire yeast genome.
  • Levy D, Kubes P, Zochodne DW. Delayed peripheral nerve degeneration, regeneration and pain in mice lacking inducible nitric oxide synthase. I Neuropathol Exp. Neural 60(5), 411–421 (2001).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.