A role for transcriptional repressor methyl-CpG-binding protein 2 and plasticity-related gene serum- and glucocorticoid-inducible kinase 1 in the induction of inflammatory pain states

Journal of Neuroscience

Volumn 27, Issue 23, 2007, Pages 6163-6173

  Géranton, Sandrine M ^a   Morenilla Palao, Cruz ^a   Hunt, Stephen P ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Antisense technology; Inflammation; Lamina I; MeCP2; SGK1; Transcriptional repression

Indexed keywords

DNA; FK 506 BINDING PROTEIN; FK 506 BINDING PROTEIN 5; METHYL CPG BINDING PROTEIN 2; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; TRANSCRIPTION FACTOR SIN3A; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANKLE; ARTHRITIS; ARTICLE; DNA FINGERPRINTING; DOWN REGULATION; GENE; GENE EXPRESSION; GENE REPRESSION; GENETIC TRANSCRIPTION; GENOME; HYPERALGESIA; MALE; MICROARRAY ANALYSIS; MODULATION; NERVE CELL; NERVE PROJECTION; NEUROPATHIC PAIN; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASTICITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; SPINAL CORD DORSAL HORN; UPREGULATION;

ANIMALS; GENE EXPRESSION REGULATION; IMMEDIATE-EARLY PROTEINS; INFLAMMATION MEDIATORS; MALE; METHYL-CPG-BINDING PROTEIN 2; NEURONAL PLASTICITY; PAIN; PAIN MEASUREMENT; PHOSPHORYLATION; POSTERIOR HORN CELLS; PROTEIN-SERINE-THREONINE KINASES; RATS; RATS, SPRAGUE-DAWLEY; TRANSCRIPTION, GENETIC;

EID: 34250024827     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1306-07.2007     Document Type: Article

References (59)

1. Bailey CH, Bartsch D, Kandel ER (1996) Toward a molecular definition of long-term memory storage. Proc Natl Acad Sci USA 93:13445-13452.
2. Bennett MI, Attal N, Backonja MM, Baron R, Bouhassira D, Freynhagen R, Scholz J, Tolle TR, Wittchen HU, Jensen TS (2007) Using screening tools to identify neuropathic pain. Pain 127:199-203.
3. Bienvenu T, Chelly J (2006) Molecular genetics of Rett syndrome: when DNA methylation goes unrecognized. Nat Rev Genet 7:415-426.
4. Chen WG, Chang Q, Lin Y, Meissner A, West AE, Griffith EC, Jaenisch R, Greenberg ME (2003) Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science 302:885-889.
5. Costigan M, Befort K, Karchewski L, Griffin RS, D'Urso D, Allchorne A, Sitarski J, Mannion JW, Pratt RE, Woolf CJ (2002) Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci 3:16.
6. Dahlquist KD, Salomonis N, Vranizan K, Lawlor SC, Conklin BR (2002) GenMAPP, a new tool for viewing and analyzing microarray data on biological pathways. Nat Genet 31:19-20.
7. David S, Kalb RG (2005) Serum/glucocorticoid-inducible kinase can phosphorylate the cyclic AMP response element binding protein, CREB. FEBS Lett 579:1534-1538.
8. Doniger SW, Salomonis N, Dahlquist KD, Vranizan K, Lawlor SC, Conklin BR (2003) MAPPFinder: using Gene Ontology and GenMAPP to create a global gene-expression profile from microarray data. Genome Biol 4:R7.
9. Doyle CA, Hunt SP (1999) Substance P receptor (neurokinin-1)-expressing neurons in lamina I of the spinal cord encode for the intensity of noxious stimulation: a c-Fos study in rat. Neuroscience 89:17-28.
10. Fuks F, Hurd PJ, Wolf D, Nan X, Bird AP, Kouzarides T (2003) The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J Biol Chem 278:4035-4040.
11. Garry EM, Fleetwood-Walker SM (2004) Organizing pains. Trends Neurosci 27:292-294.
12. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5:R80.
13. Guy J, Hendrich B, Holmes M, Martin JE, Bird A (2001) A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat Genet 27:322-326.
14. Hunt SP, Mantyh PW (2001) The molecular dynamics of pain control. Nat Rev Neurosci 2:83-91.
15. Ikeda H, Heinke B, Ruscheweyh R, Sandkuhler J (2003) Synaptic plasticity in spinal lamina I projection neurons that mediate hyperalgesia. Science 299:1237-1240.
16. Ikeda H, Stark J, Fischer H, Wagner M, Drdla R, Jager T, Sandkuhler J (2006) Synaptic amplifier of inflammatory pain in the spinal dorsal horn. Science 312:1659-1662.
17. Ji RR, Kohno T, Moore KA, Woolf CJ (2003) Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci 26:696-705.
18. Jones MW, Errington ML, French PJ, Fine A, Bliss TV, Garel S, Charnay P, Bozon B, Laroche S, Davis S (2001) A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat Neurosci 4:289-296.
19. Khasabov SG, Rogers SD, Ghilardi JR, Peters CM, Mantyh PW, Simone DA (2002) Spinal neurons that possess the substance P receptor are required for the development of central sensitization. J Neurosci 22:9086-9098.
20. Klein T, Magerl W, Treede RD (2006) Perceptual correlate of nociceptive long-term potentiation (LTP) in humans shares the time course of early-LTP. J Neurophysiol 96:3551-3555.
21. Klose RJ, Bird AP (2004) MeCP2 behaves as an elongated monomer that does not stably associate with the Sin3a chromatin remodeling complex. J Biol Chem 279:46490-46496.
22. Lee CT, Tyan SW, Ma YL, Tsai MC, Yang YC, Lee EH (2006) Serum- and glucocorticoid-inducible kinase (SGK) is a target of the MAPK/ERK signaling pathway that mediates memory formation in rats. Eur J Neurosci 23:1311-1320.
23. Levenson JM, Choi S, Lee SY, Cao YA, Ahn HJ, Worley KC, Pizzi M, Liou HC, Sweatt JD (2004) A bioinformatics analysis of memory consolidation reveals involvement of the transcription factor c-rel. J Neurosci 24:3933-3943.
24. Ma YL, Tsai MC, Hsu WL, Lee EH (2006) SGK protein kinase facilitates the expression of long-term potentiation in hippocampal neurons. Learn Mem 13:114-118.
25. Martin KC, Barad M, Kandel ER (2000) Local protein synthesis and its role in synapse-specific plasticity. Curr Opin Neurobiol 10:587-592.
26. Martinowich K, Hattori D, Wu H, Fouse S, He F, Hu Y, Fan G, Sun YE (2003) DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 302:890-893.
27. McClung CA, Nestler EJ, Zachariou V (2005) Regulation of gene expression by chronic morphine and morphine withdrawal in the locus ceruleus and ventral tegmental area. J Neurosci 25:6005-6015.
28. Millan MJ (1999) The induction of pain: an integrative review. Prog Neurobiol 57:1-164.
29. Millan MJ, Czlonkowski A, Morris B, Stein C, Arendt R, Huber A, Hollt V, Herz A (1988) Inflammation of the hind limb as a model of unilateral, localized pain: influence on multiple opioid systems in the spinal cord of the rat. Pain 35:299-312.
30. Moretti P, Levenson JM, Battaglia F, Atkinson R, Teague R, Antalffy B, Armstrong D, Arancio O, Sweatt JD, Zoghbi HY (2006) Learning and memory and synaptic plasticity are impaired in a mouse model of Rett syndrome. J Neurosci 26:319-327.
31. Nan X, Cross S, Bird A (1998a) Gene silencing by methyl-CpG-binding proteins. Novartis Found Symp 214:6-16.
32. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird A (1998b) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393:386-389.
33. Neugebauer V, Schaible HG, Weiretter F, Freudenberger U (1994) The involvement of substance P and neurokinin-1 receptors in the responses of rat dorsal horn neurons to noxious but not to innocuous mechanical stimuli applied to the knee joint. Brain Res 666:207-215.
34. Nichols ML, Allen BJ, Rogers SD, Ghilardi JR, Honore P, Luger NM, Finke MP, Li J, Lappi DA, Simone DA, Mantyh PW (1999) Transmission of chronic nociception by spinal neurons expressing the substance P receptor. Science 286:1558-1561.
35. Nuber UA, Kriaucionis S, Roloff TC, Guy J, Selfridge J, Steinhoff C, Schulz R, Lipkowitz B, Ropers HH, Holmes MC, Bird A (2005) Up-regulation of glucocorticoid-regulated genes in a mouse model of Rett syndrome. Hum Mol Genet 14:2247-2256.
36. Okabe S, Kim HD, Miwa A, Kuriu T, Okado H (1999) Continual remodeling of postsynaptic density and its regulation by synaptic activity. Nat Neurosci 2:804-811.
37. Paxinos G, Watson C, Pennisi M, Topple A (1985) Bregma, lambda and the interaural midpoint in stereotaxic surgery with rats of different sex, strain and weight. J Neurosci Methods 13:139-143.
38. Pittenger C, Kandel E (1998) A genetic switch for long-term memory. C R Acad Sci III 321:91-96.
39. Rygh LJ, Suzuki R, Rahman W, Wong Y, Vonsy JL, Sandhu H, Webber M, Hunt S, Dickenson AH (2006) Local and descending circuits regulate long-term potentiation and zif268 expression in spinal neurons. Eur J Neurosci 24:761-772.
40. Samaco RC, Hogart A, LaSalle JM (2005) Epigenetic overlap in autism-spectrum neurodevelopmental disorders: MECP2 deficiency causes reduced expression of UBE3A and GABRB3. Hum Mol Genet 14:483-492.
41. Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3:3.
42. Storkson RV, Kjorsvik A, Tjolsen A, Hole K (1996) Lumbar catheterization of the spinal subarachnoid space in the rat. J Neurosci Methods 65:167-172.
43. Suzuki M, Yamada T, Kihara-Negishi F, Sakurai T, Oikawa T (2003) Direct association between PU. 1 and MeCP2 that recruits mSin3A-HDAC complex for PU. 1-mediated transcriptional repression. Oncogene 22:8688-8698.
44. Suzuki R, Morcuende S, Webber M, Hunt SP, Dickenson AH (2002) Superficial NK1-expressing neurons control spinal excitability through activation of descending pathways. Nat Neurosci 5:1319-1326.
45. Tao F, Tao YX, Gonzalez JA, Fang M, Mao P, Johns RA (2001) Knockdown of PSD-95/SAP90 delays the development of neuropathic pain in rats. NeuroReport 12:3251-3255.
46. Tao YX, Huang YZ, Mei L, Johns RA (2000) Expression of PSD-95/SAP90 is critical for N-methyl-D-aspartate receptor-mediated thermal hyperalgesia in the spinal cord. Neuroscience 98:201-206.
47. Todd AJ (2002) Anatomy of primary afferents and projection neurons in the rat spinal dorsal horn with particular emphasis on substance P and the neurokinin 1 receptor. Exp Physiol 87:245-249.
48. Todd AJ, Puskar Z, Spike RC, Hughes C, Watt C, Forrest L (2002) Projection neurons in lamina I of rat spinal cord with the neurokinin 1 receptor are selectively innervated by substance p-containing afferents and respond to noxious stimulation. J Neurosci 22:4103-4113.
49. Torsney C, MacDermott AB (2006) Disinhibition opens the gate to pathological pain signaling in superficial neurokinin 1 receptor-expressing neurons in rat spinal cord. J Neurosci 26:1833-1843.
50. Tsai KJ, Chen SK, Ma YL, Hsu WL, Lee EH (2002) sgk, a primary glucocorticoid-induced gene, facilitates memory consolidation of spatial learning in rats. Proc Natl Acad Sci USA 99:3990-3995.
51. von Hertzen LS, Giese KP (2005) Memory reconsolidation engages only a subset of immediate-early genes induced during consolidation. J Neurosci 25:1935-1942.
52. Wang Z, Gardell LR, Ossipov MH, Vanderah TW, Brennan MB, Hochgeschwender U, Hruby VJ, Malan Jr TP, Lai J, Porreca F (2001) Pronociceptive actions of dynorphin maintain chronic neuropathic pain. J Neurosci 21:1779-1786.
53. Weihe E, Millan MJ, Hollt V, Nohr D, Herz A (1989) Induction of the gene encoding pro-dynorphin by experimentally induced arthritis enhances staining for dynorphin in the spinal cord of rats. Neuroscience 31:77-95.
54. Westberry JM, Sadosky PW, Hubler TR, Gross KL, Scammell JG (2006) Glucocorticoid resistance in squirrel monkeys results from a combination of a transcriptionally incompetent glucocorticoid receptor and overexpression of the glucocorticoid receptor co-chaperone FKBP51. J Steroid Biochem Mol Biol 100:34-41.
55. Wisden W, Errington ML, Williams S, Dunnett SB, Waters C, Hitchcock D, Evan G, Bliss TV, Hunt SP (1990) Differential expression of immediate early genes in the hippocampus and spinal cord. Neuron 4:603-614.
56. Wochnik GM, Ruegg J, Abel GA, Schmidt U, Holsboer F, Rein T (2005) FK506-binding proteins 51 and 52 differentially regulate dynein interaction and nuclear translocation of the glucocorticoid receptor in mammalian cells. J Biol Chem 280:4609-4616.
57. Woolf CJ (1983) Evidence for a central component of post-injury pain hypersensitivity. Nature 306:686-688.
58. Zhang RX, Lao L, Qiao JT, Malsnee K, Ruda MA (2004a) Endogenous and exogenous glucocorticoid suppresses up-regulation of preprodynorphin mRNA and hyperalgesia in rats with peripheral inflammation. Neurosci Lett 359:85-88.
59. Zhang RX, Lao L, Qiao JT, Ruda MA (2004b) Effects of aging on hyperalgesia and spinal dynorphin expression in rats with peripheral inflammation. Brain Res 999:135-141.