17β-estradiol activates estrogen receptor β-signalling and inhibits transient receptor potential vanilloid receptor 1 activation by capsaicin in adult rat nociceptor neurons

Endocrinology

Volumn 149, Issue 11, 2008, Pages 5540-5548

  Xu, Shenghong ^a   Cheng, Ying ^a   Keast, Janet R ^a   Osborne, Peregrine B ^a,b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b ROYAL NORTH SHORE HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

1,3,5 TRIS(4 HYDROXYPHENYL) 4 PROPYLPYRAZOLE; 17ALPHA ESTRADIOL; 2 MORPHOLINO 8 PHENYLCHROMONE; ALPHA,BETA METHYLENEADENOSINE TRIPHOSPHATE; CAPSAICIN; COBALT; ESTRADIOL; ESTROGEN RECEPTOR BETA; ICI 182870; PROLACTIN; PROPIONITRILE; TAMOXIFEN; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; WORTMANNIN; TRPV1 RECEPTOR; VANILLOID RECEPTOR;

ANIMAL CELL; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENE EXPRESSION; HORMONAL REGULATION; HYPERALGESIA; NERVE CELL CULTURE; NEUROGENIC INFLAMMATION; NOCICEPTION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROLACTIN RELEASE; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SPINAL GANGLION; WESTERN BLOTTING; ANIMAL; DRUG ANTAGONISM; DRUG EFFECT; FEMALE; METABOLISM; NOCICEPTIVE RECEPTOR; PHYSIOLOGY; SENSORY NERVE CELL; SPRAGUE DAWLEY RAT; SYNAPTIC POTENTIAL;

ANIMALS; CAPSAICIN; COBALT; ESTRADIOL; ESTROGEN RECEPTOR BETA; FEMALE; GANGLIA, SPINAL; NEURONS, AFFERENT; NOCICEPTORS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SYNAPTIC POTENTIALS; TRPV CATION CHANNELS;

EID: 54349122794     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-0278     Document Type: Article

References (52)

1. Holdcroft A, Berkley KJ 2006 Sex and gender differences in pain and its relief. In: Wall PD, McMahon SB, Koltzenburg M, eds. Wall and Melzack's textbook of pain. 5th ed. Amsterdam: Elsevier; 1181-1197
2. Sanoja R, Cervero F 2005 Estrogen-dependent abdominal hyperalgesia induced by ovariectomy in adult mice: a model of functional abdominal pain. Pain 118:243-253
3. Dawson-Basoa M, Gintzler AR 1998 Gestational and ovarian sex steroid antinociception: synergy between spinal κ and δ opioid systems. Brain Res 794:61-67
4. Gintzler AR, Liu NJ 2001 The maternal spinal cord: biochemical and physiological correlates of steroid-activated antinociceptive processes. Prog Brain Res 133:83-97
5. Flake NM, Bonebreak DB, Gold MS 2005 Estrogen and inflammation increase the excitability of rat temporomandibular joint afferent neurons. J Neurophysiol 93:1585-1597
6. Diogenes A, Patwardhan AM, Jeske NA, Ruparel NB, Goffin V, Akopian AN, Hargreaves KM 2006 Prolactin modulates TRPV1 in female rat trigeminal sensory neurons. J Neurosci 26:8126-8136
7. Fillingim RB, Ness TJ 2000 Sex-related hormonal influences on pain and analgesic responses. Neurosci Biobehav Rev 24:485-501
8. Papka RE, Srinivasan B, Miller KE, Hayashi S 1997 Localization of estrogen receptor protein and estrogen receptor messenger RNA in peripheral autonomic and sensory neurons. Neuroscience 79:1153-1163
9. Papka RE, Storey-Workley M, Shughrue PJ, Merchenthaler I, Collins JJ, Usip S, Saunders PT, Shupnik M 2001 Estrogen receptor-α and β- immunoreactivity and mRNA in neurons of sensory and autonomic ganglia and spinal cord. Cell Tissue Res 304:193-214
10. Bennett HL, Gustafsson JA, Keast JR 2003 Estrogen receptor expression in lumbosacral dorsal root ganglion cells innervating the female rat urinary bladder. Auton Neurosci 105:90-100
11. Chaban VV, Mayer EA, Ennes HS, Micevych PE 2003 Estradiol inhibits ATP-induced intracellular calcium concentration increase in dorsal root ganglia neurons. Neuroscience 118:941-948
12. Lee DY, Chai YG, Lee EB, Kim KW, Nah SY, Oh TH, Rhim H 2002 17β-estradiol inhibits high-voltage-activated calcium channel currents in rat sensory neurons via a non-genomic mechanism. Life Sci 70:2047-2059
13. Purves-Tyson TD, Keast JR 2004 Rapid actions of estradiol on cyclic AMP response-element binding protein phosphorylation in dorsal root ganglion neurons. Neuroscience 129:629-637
14. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D 1997 The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816-824
15. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, Raumann BE, Basbaum AI, Julius D 1998 The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21:531-543
16. Brewer GJ, Torricelli JR, Evege EK, Price PJ 1993 Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res 35:567-576
17. Nicholas RS, Winter J, Wren P, Bergmann R, Woolf CJ 1999 Peripheral inflammation increases the capsaicin sensitivity of dorsal root ganglion neurons in a nerve growth factor-dependent manner. Neuroscience 91:1425-1433
18. Prossnitz ER, Arterburn JB, Sklar LA 2007 GPR30: A G protein-coupled receptor for estrogen. Mol Cell Endocrinol 265-266:138-142
19. Leffler A, Mönter B, Koltzenburg M 2006 The role of the capsaicin receptor TRPV1 and acid-sensing ion channels (ASICS) in proton sensitivity of subpopulations of primary nociceptive neurons in rats and mice. Neuroscience 139:699-709
20. Burnstock G, Wood JN 1996 Purinergic receptors: their role in nociception and primary afferent neurotransmission. Curr Opin Neurobiol 6:526-532
21. Chen CC, Akopian AN, Sivilotti L, Colquhoun D, Burnstock G, Wood JN 1995 A P2X purinoceptor expressed by a subset of sensory neurons. Nature 377:428-431
22. Cockayne DA, Dunn PM, Zhong Y, Rong W, Hamilton SG, Knight GE, Ruan HZ, Ma B, Yip P, Nunn P, McMahon SB, Burnstock G, Ford AP 2005 P2X2 knockout mice and P2X2/P2X3 double knockout mice reveal a role for the P2X2 receptor subunit in mediating multiple sensory effects of ATP. J Physiol 567(Pt 2):621-639
23. Lewis C, Neidhart S, Holy C, North RA, Buell G, Surprenant A 1995 Co-expression of P2X2 and P2X3 receptor subunits can account for ATP-gated currents in sensory neurons. Nature 377:432-435
24. Labrakakis C, Tong CK, Weissman T, Torsney C, MacDermott AB 2003 Localization and function of ATP and GABAA receptors expressed by nociceptors and other postnatal sensory neurons in rat. J Physiol 549(Pt 1):131-142
25. Zhong Y, Banning AS, Cockayne DA, Ford AP, Burnstock G, McMahon SB 2003 Bladder and cutaneous sensory neurons of the rat express different functional P2X receptors. Neuroscience 120:667-675
26. Harrington WR, Sheng S, Barnett DH, Petz LN, Katzenellenbogen JA, Katzenellenbogen BS 2003 Activities of estrogen receptor α- and β-selective ligands at diverse estrogen responsive gene sites mediating transactivation or transrepression. Mol Cell Endocrinol 206:13-22
27. Björnström L, Sjöberg M 2005 Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes. Mol Endocrinol 19:833-842
28. Pedram A, Razandi M, Levin ER 2006 Nature of functional estrogen receptors at the plasma membrane. Mol Endocrinol 20:1996-2009
29. Vasudevan N, Pfaff DW 2007 Membrane-initiated actions of estrogens in neuroendocrinology: emerging principles. Endocr Rev 28:1-19
30. Stein AT, Ufret-Vincenty CA, Hua L, Santana LF, Gordon SE 2006 Phosphoinositide 3-kinase binds to TRPV1 and mediates NGF-stimulated TRPV1 trafficking to the plasma membrane. J Gen Physiol 128:509-522
31. Lukacs V, Thyagarajan B, Varnai P, Balla A, Balla T, Rohacs T 2007 Dual regulation of TRPV1 by phosphoinositides. J Neurosci 27:7070-7080
32. Tominaga M, Tominaga T 2005 Structure and function of TRPV1. Pflugers Arch 451:143-150
33. Zhang X, McNaughton PA 2006 Why pain gets worse: the mechanism of heat hyperalgesia. J Gen Physiol 128:491-493
34. Heldring N, Pike A, Andersson S, Matthews J, Cheng G, Hartman J, Tujague M, Strom A, Treuter E, Warner M, Gustafsson JA 2007 Estrogen receptors: how do they signal and what are their targets. Physiol Rev 87:905-931
35. Nilsson S, Makela S, Treuter E, Tujague M, Thomsen J, Andersson G, Enmark E, Pettersson K, Warner M, Gustafsson JA 2001 Mechanisms of estrogen action. Physiol Rev 81:1535-1565
36. Smith CL, O'Malley BW 2004 Coregulator function: a key to understanding tissue specificity of selective receptor modulators. Endocr Rev 25:45-71
37. Leung YK, Gao Y, Lau KM, Zhang X, Ho SM 2006 ICI 182,780-regulated gene expression in DU145 prostate cancer cells is mediated by estrogen receptor-β/NFκB crosstalk. Neoplasia 8:242-249
38. Filardo EJ, Quinn JA, Bland KI, Frackelton Jr AR 2000 Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol Endocrinol 14:1649-1660
39. Filardo EJ, Quinn JA, Frackelton Jr AR, Bland KI 2002 Estrogen action via the G protein-coupled receptor, GPR30: stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptor-to-MAPK signaling axis. Mol Endocrinol 16:70-84
40. Revankar CM, Arterburn JM, Mitchell HD, Field AS, Burai R, Corona C, Ramesh C, Sklar LA, Arterburn JB, Prossnitz ER 2007 Synthetic estrogen derivatives demonstrate the functionality of intracellular GPR30. ACS Chem Biol 2:536-544
41. Filardo EJ, Thomas P 2005 GPR30: a seven-transmembrane-spanning estrogen receptor that triggers EGF release. Trends Endocrinol Metab 16:362-367
42. Thomas P, Pang Y, Filardo EJ, Dong J 2005 Identity of anestrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology 146:624-632
43. Vivacqua A, Bonofiglio D, Albanito L, Madeo A, Rago V, Carpino A, Musti AM, Picard D, Andò S, Maggiolini M 2006 17β-Estradiol, genistein, and 4-hydroxytamoxifen induce the proliferation of thyroid cancer cells through the g protein-coupled receptor GPR30. Mol Pharmacol 70:1414-1423
44. Vivacqua A, Bonofiglio D, Recchia AG, Musti AM, Picard D, Andò S, Maggiolini M 2006 The G protein-coupled receptor GPR30 mediates the proliferative effects induced by 17β-estradiol and hydroxytamoxifen in endometrial cancer cells. Mol Endocrinol 20:631-646
45. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D 2000 Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288:306-313
46. Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K, Hughes SA, Rance K, Grau E, Harper AJ, Pugh PL, Rogers DC, Bingham S, Randall A, Sheardown SA 2000 Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 405:183-187
47. Chuang H, Prescott E, Kong H, Shields S, Jordt S, Basbaum A, Chao M, Julius D 2001 Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2-mediated inhibition. Nature 411:957-962
48. Spooner MF, Robichaud P, Carrier JC, Marchand S 2007 Endogenous pain modulation during the formalin test in estrogen receptor β knockout mice. Neuroscience 150:675-680
49. Leventhal L, Brandt MR, Cummons TA, Piesla MJ, Rogers KE, Harris HA 2006 An estrogen receptor-β agonist is active in models of inflammatory and chemical-induced pain. Eur J Pharmacol 553:146-148
50. Kondo D, Yabe R, Kurihara T, Saegusa H, Zong S, Tanabe T 2006 Progesterone receptor antagonist is effective in relieving neuropathic pain. Eur J Pharmacol 541:44-48
51. Imamov O, Yakimchuk K, Morani A, Schwend T, Wada-Hiraike O, Razumov S, Warner M, Gustafsson JA 2007 Estrogen receptor β-deficient female mice develop a bladder phenotype resembling human interstitial cystitis. Proc Natl Acad Sci USA 104:9806-9809
52. Straub RH 2007 The complex role of estrogens in inflammation. Endocr Rev 28:521-574