Long-range regulatory synergy is required to allow control of the TAC1 locus by MEK/ERK signalling in sensory neurones

NeuroSignals

Volumn 18, Issue 3, 2011, Pages 173-185

  Shanley, Lynne ^a   Davidson, Scott ^a   Lear, Marissa ^a   Thotakura, Anil Kumar ^b   McEwan, Iain Joseph ^a   Ross, Ruth A ^a   MacKenzie, Alasdair ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

^b HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

Capsaicin; Comparative genomics; Enhancer promoter selectivity; Gene regulation; Hyperalgesia; MEK ERK signalling; Regulatory synergy; Sensory neurons; Substance P; TAC1 gene

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; NEUROPEPTIDE; SUBSTANCE P; TAC1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENHANCER REGION; GENE EXPRESSION; GENE IDENTIFICATION; GENE LOCUS; GENETIC ANALYSIS; HYPERALGESIA; NEUROMODULATION; NEWBORN; NOCICEPTIVE STIMULATION; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; RAT; SENSORY NERVE CELL; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; CHICK EMBRYO; DOGS; ENHANCER ELEMENTS, GENETIC; GANGLIA, SPINAL; GENETIC LOCI; HUMANS; MACACA MULATTA; MAP KINASE SIGNALING SYSTEM; MICE; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; RATS; SENSORY RECEPTOR CELLS; SEQUENCE HOMOLOGY, AMINO ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID; TACHYKININS;

EID: 79952575131     PISSN: 1424862X     EISSN: None     Source Type: Journal    
DOI: 10.1159/000322010     Document Type: Article

References (69)

1. Visel A, Rubin EM, Pennacchio LA: Genomic views of distant-acting enhancers. Nature 2009; 461: 199-205.
2. Geppetti P, Nassini R, Materazzi S, Benemei S: The concept of neurogenic inflammation. BJU Int 2008; 101(Suppl 3):2-6. (Pubitemid 351328798)
3. Cao YQ, Mantyh PW, Carlson EJ, Gillespie AM, Epstein CJ, Basbaum AI: Primary afferent tachykinins are required to experience moderate to intense pain. Nature 1998; 392: 390-394. (Pubitemid 28168735)
4. Zimmer A, Zimmer AM, Baffi J, Usdin T, Reynolds K, Konig M, Palkovits M, Mezey E: Hypoalgesia in mice with a targeted deletion of the tachykinin 1 gene. Proc Natl Acad Sci USA 1998; 95: 2630-2635. (Pubitemid 28145994)
5. Hokfelt T, Pernow B, Wahren J: Substance p: a pioneer amongst neuropeptides. J Intern Med 2001; 249: 27-40. (Pubitemid 32147090)
6. Neumann S, Doubell TP, Leslie T, Woolf CJ: Inflammatory pain hypersensitivity mediated by phenotypic switch in myelinated primary sensory neurons. Nature 1996; 384: 360-364. (Pubitemid 26408518)
7. Noguchi K, Kawai Y, Fukuoka T, Senba E, Miki K: Substance P induced by peripheral nerve injury in primary afferent sensory neurons and its effect on dorsal column nucleus neurons. J Neurosci 1995; 15: 7633-7643.
8. Cheng JK, Ji RR: Intracellular signaling in primary sensory neurons and persistent pain. Neurochem Res 2008; 33: 1970-1978.
9. Ji RR: Peripheral and central mechanisms of inflammatory pain, with emphasis on MAP kinases. Curr Drug Targets Inflamm Allergy 2004; 3: 299-303.
10. Ji RR: Mitogen-activated protein kinases as potential targets for pain killers. Curr Opin Investig Drugs 2004; 5: 71-75.
11. Ciruela A, Dixon AK, Bramwell S, Gonzalez MI, Pinnock RD, Lee K: Identification of MEK1 as a novel target for the treatment of neuropathic pain. Br J Pharmacol 2003; 138: 751-756. (Pubitemid 36401513)
12. Ma W, Quirion R: The ERK/MAPK pathway, as a target for the treatment of neuropathic pain. Expert Opin Ther Targets 2005; 9: 699-713. (Pubitemid 41131674)
13. Cruz CD, Cruz F: The ERK 1 and 2 pathway in the nervous system: from basic aspects to possible clinical applications in pain and visceral dysfunction. Curr Neuropharmacol 2007; 5: 244-252. (Pubitemid 350268185)
14. Obata K, Noguchi K: MAPK activation in nociceptive neurons and pain hypersensitivity. Life Sci 2004; 74: 2643-2653. (Pubitemid 38369361)
15. Tokuda M, Miyamoto R, Sakuta T, Nagaoka S, Torii M: Substance P activates p38 mitogen- activated protein kinase to promote IL-6 induction in human dental pulp fibroblasts. Connect Tissue Res 2005; 46: 153-158. (Pubitemid 41283148)
16. Mizushima T, Obata K, Yamanaka H, Dai Y, Fukuoka T, Tokunaga A, Mashimo T, Noguchi K: Activation of p38 MAPK in primary afferent neurons by noxious stimulation and its involvement in the development of thermal hyperalgesia. Pain 2005; 113: 51-60. (Pubitemid 40038446)
17. Cuenda A, Rousseau S: P38 MAP-kinases pathway regulation, function and role in human diseases. Biochim Biophys Acta 2007; 1773: 1358-1375. (Pubitemid 47125981)
18. Schett G, Zwerina J, Firestein G: The p38 mitogen- activated protein kinase (MAPK) pathway in rheumatoid arthritis. Ann Rheum Dis 2008; 67: 909-916. (Pubitemid 351956650)
19. Dai Y, Iwata K, Fukuoka T, Kondo E, Tokunaga A, Yamanaka H, Tachibana T, Liu Y, Noguchi K: Phosphorylation of extracellular signal-regulated kinase in primary afferent neurons by noxious stimuli and its involvement in peripheral sensitization. J Neurosci 2002; 22: 7737-7745. (Pubitemid 35386372)
20. Ovcharenko I, Nobrega MA, Loots GG, Stubbs L: ECR browser: a tool for visualizing and accessing data from comparisons of multiple vertebrate genomes. Nucleic Acids Res 2004; 32:W280-W286. (Pubitemid 38997344)
21. Miller KA, Barrow J, Collinson JM, Davidson S, Lear M, Hill RE, Mackenzie A: A highly conserved Wnt-dependent TCF4 binding site within the proximal enhancer of the anti- myogenic Msx1 gene supports expression within Pax3-expressing limb bud muscle precursor cells. Dev Biol 2007; 311: 665-678. (Pubitemid 350046522)
22. Davidson S, Miller KA, Dowell A, Gildea A, Mackenzie A: A remote and highly conserved enhancer supports amygdala specific expression of the gene encoding the anxiogenic neuropeptide substance-P. Mol Psychiatry 2006; 11: 410-421.
23. Shewan D, Berry M, Cohen J: Extensive regeneration in vitro by early embryonic neurons on immature and adult CNS tissue. J Neurosci 1995; 15: 2057-2062.
24. Agarwal N, Pacher P, Tegeder I, Amaya F, Constantin CE, Brenner GJ, Rubino T, Michalski CW, Marsicano G, Monory K, Mackie K, Marian C, Batkai S, Parolaro D, Fischer MJ, Reeh P, Kunos G, Kress M, Lutz B, Woolf CJ, Kuner R: Cannabinoids mediate analgesia largely via peripheral type 1 cannabinoid receptors in nociceptors. Nat Neurosci 2007; 10: 870-879. (Pubitemid 47013432)
25. Quinn JP, Fiskerstrand CE, Gerrard L, MacKenzie A, Payne CM: Molecular models to analyse preprotachykinin-A expression and function. Neuropeptides 2000; 34: 292-302.
26. Fiskerstrand CE, Newey P, Ebrahimi B, Gerrard L, Harrison P, McGregor GP, Quinn JP: Novel cell lines for the analysis of preprotachykinin A gene expression identify a repressor domain 3′ of the major transcriptional start site. Biochem J 1999; 341: 847-852. (Pubitemid 29389219)
27. Gerrard L, Howard M, Paterson T, Thippeswamy T, Quinn JP, Haddley K: A proximal E-box modulates NGF effects on rat PPT-A promoter activity in cultured dorsal root ganglia neurones. Neuropeptides 2005; 39: 475-483. (Pubitemid 41443524)
28. Meireles-Filho AC, Stark A: Comparative genomics of gene regulation-conservation and divergence of cis-regulatory information. Curr Opin Genet Dev 2009; 19: 565-570.
29. Peterson BK, Hare EE, Iyer VN, Storage S, Conner L, Papaj DR, Kurashima R, Jang E, Eisen MB: Big genomes facilitate the comparative identification of regulatory elements. PLoS One 2009; 4:e4688.
30. Davidson S, Miller KA, Dowell A, Gildea A, Mackenzie A: Cellular co-expression of a LacZ marker gene driven by the amygdalaspecific ECR1 enhancer with the substance P neuropeptide. Mol Psychiatry 2006; 11: 323.
31. Miller K, Davidson S, MacKenzie A: Postgenomic bioinformatic analysis of yeast artificial chromosome sequence. Methods Mol Biol 2006; 349: 41-59.
32. Miller KA, Davidson S, Liaros A, Barrow J, Lear M, Heine D, Hoppler S, MacKenzie A: Prediction and characterisation of a highly conserved, remote and camp responsive enhancer that regulates Msx1 gene expression in cardiac neural crest and outflow tract. Dev Biol 2008; 317: 686-694.
33. Harmar AJ, Mulderry PK, al-Shawi R, Lyons V, Sheward WJ, Bishop JO, Chapman K: 3.3 kb of 5′ flanking DNA from the rat preprotachykinin gene directs high level expression of a reporter gene in microinjected dorsal root ganglion neurons but not in transgenic mice. Regul Pept 1993; 46: 67-69.
34. Millward-Sadler SJ, Mackenzie A, Wright MO, Lee HS, Elliot K, Gerrard L, Fiskerstrand CE, Salter DM, Quinn JP: Tachykinin expression in cartilage and function in human articular chondrocyte mechanotransduction. Arthritis Rheum 2003; 48: 146-156. (Pubitemid 36091658)
35. Marchand JE, Wurm WH, Kato T, Kream RM: Altered tachykinin expression by dorsal root ganglion neurons in a rat model of neuropathic pain. Pain 1994; 58: 219-231. (Pubitemid 24263615)
36. Malcangio M, Ramer MS, Jones MG, McMahon SB: Abnormal substance P release from the spinal cord following injury to primary sensory neurons. Eur J Neurosci 2000; 12: 397-399. (Pubitemid 30068447)
37. Pitcher GM, Henry JL: Nociceptive response to innocuous mechanical stimulation is mediated via myelinated afferents and NK-1 receptor activation in a rat model of neuropathic pain. Exp Neurol 2004; 186: 173-197. (Pubitemid 38333192)
38. Garrett NE, Cruwys SC, Kidd BL, Tomlinson DR: Effect of capsaicin on substance P and nerve growth factor in adjuvant arthritic rats. Neurosci Lett 1997; 230: 5-8. (Pubitemid 27308518)
39. Donaldson LF, McQueen DS, Seckl JR: Neuropeptide gene expression and capsaicinsensitive primary afferents: maintenance and spread of adjuvant arthritis in the rat. J Physiol 1995; 486: 473-482.
40. Fiskerstrand CE, Lovejoy E, Gerrard L, Quinn JP: An intronic domain within the rat preprotachykinin-A gene containing a CCCT repetitive motif acts as an enhancer in differentiating embryonic stem cells. Neurosci Lett 1999; 263: 141-144. (Pubitemid 29158948)
41. Fiskerstrand C, Quinn JP: The molecular biology of preprotachykinin-A gene expression. Neuropeptides 1996; 30: 602-610. (Pubitemid 27013987)
42. Morrison CF, McAllister J, Dobson SP, Mulderry PK, Quinn JP: An activator element within the preprotachykinin-A promoter. Mol Cell Neurosci 1994; 5: 165-175. (Pubitemid 24118421)
43. Calin-Jageman IE, Wang J, Bannon MJ: Regulation of the preprotachykinin-I gene promoter through a protein kinase A-dependent, cyclic AMP response element-binding protein-independent mechanism. J Neurochem 2006; 97: 255-264.
44. Hilton KJ, Bateson AN, King AE: A model of organotypic rat spinal slice culture and biolistic transfection to elucidate factors that drive the preprotachykinin-A promoter. Brain Res Brain Res Rev 2004; 46: 191-203. (Pubitemid 39298866)
45. Spencer EM, Chandler KE, Haddley K, Howard MR, Hughes D, Belyaev ND, Coulson JM, Stewart JP, Buckley NJ, Kipar A, Walker MC, Quinn JP: Regulation and role of REST and REST4 variants in modulation of gene expression in in vivo and in vitro in epilepsy models. Neurobiol Dis 2006; 24: 41-52. (Pubitemid 44430146)
46. Adler JE, Walker PD: Cyclic AMP regulates substance P expression in developing and mature spinal sensory neurons. J Neurosci Res 2000; 59: 624-631. (Pubitemid 30133924)
47. Kleinjan DA, Lettice LA: Long-range gene control and genetic disease. Adv Genet 2008; 61: 339-388.
48. Adoue V, Chavanas S, Coudane F, Mechin MC, Caubet C, Ying S, Dong S, Duplan H, Charveron M, Takahara H, Serre G, Simon M: Long-range enhancer differentially regulated by c-Jun and JunD controls peptidylarginine deiminase-3 gene in keratinocytes. J Mol Biol 2008; 384: 1048-1057.
49. Ertzer R, Muller F, Hadzhiev Y, Rathnam S, Fischer N, Rastegar S, Strahle U: Cooperation of sonic hedgehog enhancers in midline expression. Dev Biol 2007; 301: 578-589. (Pubitemid 46073986)
50. Butler JE, Kadonaga JT: Enhancer-promoter specificity mediated by DPE or TATA core promoter motifs. Genes Dev 2001; 15: 2515-2519. (Pubitemid 32937862)
51. Mackenzie A, Miller KA, Collinson JM: Is there a functional link between gene interdigitation and multi-species conservation of synteny blocks? Bioessays 2004; 26: 1217-1224.
52. MacKenzie A, Quinn JP: Post-genomic approaches to exploring neuropeptide gene mis-expression in disease. Neuropeptides 2004; 38: 1-15. (Pubitemid 38372959)
53. MacKenzie A, Payne C, Boyle S, Clarke AR, Quinn JP: The human preprotachykinin-A gene promoter has been highly conserved and can drive human-like marker gene expression in the adult mouse CNS. Mol Cell Neurosci 2000; 16: 620-630. (Pubitemid 32001310)
54. MacKenzie A, Quinn J: A yeast artificial chromosome containing the human preprotachykinin- A gene expresses substance P in mice and drives appropriate marker-gene expression during early brain embryogenesis. Mol Cell Neurosci 2002; 19: 72-87. (Pubitemid 34121050)
55. Ji RR, Baba H, Brenner GJ, Woolf CJ: Nociceptive- specific activation of ERK in spinal neurons contributes to pain hypersensitivity. Nat Neurosci 1999; 2: 1114-1119. (Pubitemid 30126370)
56. Obata K, Yamanaka H, Dai Y, Mizushima T, Fukuoka T, Tokunaga A, Noguchi K: Differential activation of MAPK in injured and uninjured DRG neurons following chronic constriction injury of the sciatic nerve in rats. Eur J Neurosci 2004; 20: 2881-2895. (Pubitemid 40007282)
57. Galan A, Cervero F, Laird JM: Extracellular signaling-regulated kinase-1 and -2 (ERK 1/2) mediate referred hyperalgesia in a murine model of visceral pain. Brain Res Mol Brain Res 2003; 116: 126-134. (Pubitemid 36993703)
58. Firner M, Greffrath W, Treede RD: Phosphorylation of extracellular signal-related protein kinase is required for rapid facilitation of heat-induced currents in rat dorsal root ganglion neurons. Neuroscience 2006; 143: 253-263. (Pubitemid 44667309)
59. Karim F, Hu HJ, Adwanikar H, Kaplan D, Gereau RWt: Impaired inflammatory pain and thermal hyperalgesia in mice expressing neuron-specific dominant negative mitogen activated protein kinase kinase (MEK). Mol Pain 2006; 2:2.
60. Seino D, Tokunaga A, Tachibana T, Yoshiya S, Dai Y, Obata K, Yamanaka H, Kobayashi K, Noguchi K: The role of ERK signaling and the P2X receptor on mechanical pain evoked by movement of inflamed knee joint. Pain 2006; 123: 193-203. (Pubitemid 43816774)
61. Tang HB, Inoue A, Iwasa M, Hide I, Nakata Y: Substance P release evoked by capsaicin or potassium from rat cultured dorsal root ganglion neurons is conversely modulated with bradykinin. J Neurochem 2006; 97: 1412-1418. (Pubitemid 43725580)
62. Im SS, Kwon SK, Kim TH, Kim HI, Ahn YH: Regulation of glucose transporter type 4 isoform gene expression in muscle and adipocytes. IUBMB Life 2007; 59: 134-145.
63. Gibson GG, Phillips A, Aouabdi S, Plant K, Plant N: Transcriptional regulation of the human pregnane-X receptor. Drug Metab Rev 2006; 38: 31-49. (Pubitemid 43738998)
64. Melamed P, Kadir MN, Wijeweera A, Seah S: Transcription of gonadotropin beta subunit genes involves cross-talk between the transcription factors and co-regulators that mediate actions of the regulatory hormones. Mol Cell Endocrinol 2006; 252: 167-183.
65. West AG, Fraser P: Remote control of gene transcription. Hum Mol Genet 2005; 14 Spec No 1:R101-R111. (Pubitemid 40542626)
66. Ma W, Quirion R: Inflammatory mediators modulating the transient receptor potential vanilloid 1 receptor: therapeutic targets to treat inflammatory and neuropathic pain. Expert Opin Ther Targets 2007; 11: 307-320. (Pubitemid 46290955)
67. Ueda H: Molecular mechanisms of neuropathic pain-phenotypic switch and initiation mechanisms. Pharmacol Ther 2006; 109: 57-77.
68. Laird JM, Roza C, De Felipe C, Hunt SP, Cervero F: Role of central and peripheral tachykinin NK1 receptors in capsaicin-induced pain and hyperalgesia in mice. Pain 2001; 90: 97-103. (Pubitemid 32146562)
69. Bulling DG, Kelly D, Bond S, McQueen DS, Seckl JR: Adjuvant-induced joint inflammation causes very rapid transcription of beta-preprotachykinin and alpha-CGRP genes in innervating sensory ganglia. J Neurochem 2001; 77: 372-382. (Pubitemid 32298731)