Spinal estrogen receptor alpha mediates estradiol-induced pronociception in a visceral pain model in the rat

Pain

Volumn 152, Issue 5, 2011, Pages 1182-1191

  Ji, Yaping ^a   Tang, Bin ^a   Traub, Richard J ^a  

^a UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

Author keywords

Colonic afferent; Colorectal distention; Dorsal horn neurons; Estradiol; Estrogen receptor alpha; Gonadal hormones; pERK; PPT; Spinal cord; Visceral pain; Visceromotor response

Indexed keywords

4,4',4'' [4 PROPYL (1H) PYRAZOLE 1,3,5 TRIYL]TRIS PHENOL; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CATHETER; COLON DILATATION; CONTROLLED STUDY; ELECTRODE; ELECTROMYOGRAPHY; ELECTROPHYSIOLOGY; ENZYME ACTIVATION; FEMALE; IMMUNOCYTOCHEMISTRY; INTRACELLULAR SIGNALING; NONHUMAN; OVARIECTOMY; PAIN THRESHOLD; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SPINAL CORD DORSAL HORN; VASOMOTOR REFLEX; VISCERAL PAIN; VISCEROMOTOR RESPONSE; WESTERN BLOTTING;

AFFERENT PATHWAYS; ANALYSIS OF VARIANCE; ANIMALS; COLON; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; ESTRADIOL; ESTROGEN ANTAGONISTS; ESTROGEN RECEPTOR ALPHA; ESTROGENS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GINSENOSIDES; OVARIECTOMY; PAIN; RATS; RATS, SPRAGUE-DAWLEY; SAPOGENINS; SPINAL CORD; VISCERA;

EID: 79954584498     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pain.2011.01.046     Document Type: Article

References (90)

1. F. Acconcia, P. Totta, S. Ogawa, I. Cardillo, S. Inoue, S. Leone, A. Trentalance, M. Muramatsu, and M. Marino Survival versus apoptotic 17beta-estradiol effect: role of ER alpha and ER beta activated non-genomic signaling J Cell Physiol 203 2005 193 201 (Pubitemid 40330938)
2. G. Affaitati, I. Ceccarelli, P. Fiorenzani, C. Rossi, M.C. Pace, M.B. Passavanti, C. Aurilio, G. Sorda, B. Danielli, M.A. Giamberardino, and A.M. Aloisi Sex differences in the analgesic effects of ICI 182,780 and Flutamide on ureteral calculosis in rats Horm Behav 59 2011 9 13
3. A.L. Allen, and K.E. McCarson Estrogen increases nociception-evoked brain-derived neurotrophic factor gene expression in the female rat Neuroendocrinology 81 2005 193 199 (Pubitemid 41158959)
4. A. Amandusson, and A. Blomqvist Estrogen receptor-[alpha] expression in nociceptive-responsive neurons in the medullary dorsal horn of the female rat Eur J Pain 14 2010 245 248
5. J.L. Banko, L. Hou, and E. Klann NMDA receptor activation results in PKA- and ERK-dependent Mnk1 activation and increased eIF4E phosphorylation in hippocampal area CA1 J Neurochem 91 2004 462 470 (Pubitemid 39363445)
6. H.L. Bennett, J.A. Gustafsson, and J.R. Keast Estrogen receptor expression in lumbosacral dorsal root ganglion cells innervating the female rat urinary bladder Auton Neurosci 105 2003 90 100 (Pubitemid 36686720)
7. D.A. Bereiter Sex differences in brainstem neural activation after injury to the TMJ region Cells Tissues Organs 169 2001 226 237 (Pubitemid 32656649)
8. D.A. Bereiter, K. Okamoto, and D.F. Bereiter Effect of persistent monoarthritis of the temporomandibular joint region on acute mustard oil-induced excitation of trigeminal subnucleus caudalis neurons in male and female rats Pain 117 2005 58 67 (Pubitemid 41781614)
9. R. Bi, M.R. Foy, R.F. Thompson, and M. Baudry Effects of estrogen, age, and calpain on MAP kinase and NMDA receptors in female rat brain Neurobiol Aging 24 2003 977 983 (Pubitemid 36962984)
10. R. Bi, M.R. Foy, R.M. Vouimba, R.F. Thompson, and M. Baudry Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway Proc Natl Acad Sci USA 98 2001 13391 13395 (Pubitemid 33051373)
11. L. Bjornstrom, and M. Sjoberg Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes Mol.Endocrinol 19 2005 833 842 (Pubitemid 40397050)
12. M.I. Boulware, J.P. Weick, B.R. Becklund, S.P. Kuo, R.D. Groth, and P.G. Mermelstein Estradiol activates group I and II metabotropic glutamate receptor signaling, leading to opposing influences on cAMP response element-binding protein J Neurosci 25 2005 5066 5078 (Pubitemid 40712851)
13. H.B. Bradshaw, and K.J. Berkley Estrous changes in responses of rat gracile nucleus neurons to stimulation of skin and pelvic viscera J Neurosci 20 2000 7722 7727
14. H.B. Bradshaw, J.L. Temple, E. Wood, and K.J. Berkley Estrous variations in behavioral responses to vaginal and uterine distention in the rat Pain 82 1999 187 197 (Pubitemid 29317530)
15. A.M. Cason, C.L. Samuelsen, and K.J. Berkley Estrous changes in vaginal nociception in a rat model of endometriosis Horm Behav 44 2003 123 131 (Pubitemid 37108634)
16. V.V. Chaban, and P.E. Micevych Estrogen receptor-alpha mediates estradiol attenuation of ATP-induced Ca(2+) signaling in mouse dorsal root ganglion neurons J Neurosci Res 81 2005 31 37 (Pubitemid 41139107)
17. C.A. Cornil, G.F. Ball, and J. Balthazart Functional significance of the rapid regulation of brain estrogen action: where do the estrogens come from? Brain Res 1126 2006 2 26 (Pubitemid 44889243)
18. K. Dechering, C. Boersma, and S. Mosselman Estrogen receptors alpha and beta: two receptors of a kind? Curr Med Chem 7 2000 561 576 (Pubitemid 30396429)
19. R. Dubner, and M.A. Ruda Activity-dependent neuronal plasticity following tissue injury and inflammation Trends Neurosci 15 1992 96 103
20. S.L. Dun, G.C. Brailoiu, X. Gao, E. Brailoiu, J.B. Arterburn, E.R. Prossnitz, T.I. Oprea, and N.J. Dun Expression of estrogen receptor GPR30 in the rat spinal cord and in autonomic and sensory ganglia J Neurosci Res 87 2009 1610 1619
21. H.C. Evrard Estrogen synthesis in the spinal dorsal horn: a new central mechanism for the hormonal regulation of pain Am J Physiol Regul Integr Comp Physiol 291 2006 R291 R299
22. H.C. Evrard, and J. Balthazart Rapid regulation of pain by estrogens synthesized in spinal dorsal horn neurons J Neurosci 24 2004 7225 7229 (Pubitemid 39100692)
23. Y. Fu, J. Han, T. Ishola, M. Scerbo, H. Adwanikar, C. Ramsey, and V. Neugebauer PKA and ERK, but not PKC, in the amygdala contribute to pain-related synaptic plasticity and behavior Mol Pain 4 2008 26
24. A. Galan, F. Cervero, and J.M. Laird 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 116 2003 126 134 (Pubitemid 36993703)
25. Y.J. Gao, and R.R. Ji Chemokines, neuronal-glial interactions, and central processing of neuropathic pain Pharmacol Ther 126 2010 56 68
26. L.R. Gardell, L. Hyldtoft, A.L. Del Tredici, C.B. Andersen, L.C. Fairbairn, B.W. Lund, M. Gustafsson, M.R. Brann, R. Olsson, and F. Piu Differential modulation of inflammatory pain by a selective estrogen receptor beta agonist Eur J Pharmacol 592 2008 158 159
27. P. Geraldes, M.G. Sirois, P.N. Bernatchez, and J.F. Tanguay Estrogen regulation of endothelial and smooth muscle cell migration and proliferation: role of p38 and p42/44 mitogen-activated protein kinase Arterioscler Thromb Vasc Biol 22 2002 1585 1590
28. I. Guillemin, M. Becker, K. Ociepka, E. Friauf, and H.G. Nothwang A subcellular prefractionation protocol for minute amounts of mammalian cell cultures and tissue Proteomics 5 2005 35 45 (Pubitemid 40189635)
29. A. Holdcroft, S. Sapsed-Byrne, D. Ma, D. Hammal, and M.L. Forsling Sex and oestrous cycle differences in visceromotor responses and vasopressin release in response to colonic distention in male and female rats anesthetized with halothane Br J Anaesth 85 2000 907 910
30. A. Howell, C.K. Osborne, C. Morris, and A.E. Wakeling ICI 182, 780 (Faslodex): development of a novel, "pure" antiestrogen Cancer 89 2000 817 825
31. R.R. Ji, H. Baba, G.J. Brenner, and C.J. Woolf Nociceptive-specific activation of ERK in spinal neurons contributes to pain hypersensitivity Nat Neurosci 2 1999 1114 1119 (Pubitemid 30126370)
32. R.R. Ji, K. Befort, G.J. Brenner, and C.J. Woolf ERK MAP kinase activation in superficial spinal cord neurons induces prodynorphin and NK-1 upregulation and contributes to persistent inflammatory pain hypersensitivity J Neurosci 22 2002 478 485 (Pubitemid 34049086)
33. R.R. Ji, R.W. Gereau, M. Malcangio, and G.R. Strichartz MAP kinase and pain Brain Res Rev 60 2009 135 148
34. Y. Ji, A.Z. Murphy, and R.J. Traub Estrogen modulates the visceromotor reflex and responses of spinal dorsal horn neurons to colorectal stimulation in the rat J Neurosci 23 2003 3908 3915 (Pubitemid 36958496)
35. Y. Ji, B. Tang, and R.J. Traub Estrogen increases and progesterone decreases behavioral and neuronal responses to colorectal distention following colonic inflammation in the rat Pain 117 2005 433 442
36. Y. Ji, B. Tang, and R.J. Traub The visceromotor response to colorectal distention fluctuates with the estrous cycle in rats Neuroscience 154 2008 1562 1567
37. Y. Ji, and R.J. Traub Spinal NMDA receptors contribute to neuronal processing of acute noxious and nonnoxious colorectal stimulation in the rat J Neurophysiol 86 2001 1783 1791 (Pubitemid 32953227)
38. F. Karim, H.J. Hu, H. Adwanikar, D. Kaplan, and R.W. Gereau Impaired inflammatory pain and thermal hyperalgesia in mice expressing neuron-specific dominant negative mitogen activated protein kinase kinase (MEK) Mol Pain 2 2006 2
39. F. Karim, C.C. Wang, and R.W. Gereau Metabotropic glutamate receptor subtypes 1 and 5 are activators of extracellular signal-regulated kinase signaling required for inflammatory pain in mice J Neurosci 21 2001 3771 3779 (Pubitemid 32466469)
40. Y. Kawasaki, T. Kohno, Z.Y. Zhuang, G.J. Brenner, H. Wang, M.C. Van Der, K. Befort, C.J. Woolf, and R.R. Ji Ionotropic and metabotropic receptors, protein kinase A, protein kinase C, and Src contribute to C-fiber-induced ERK activation and cAMP response element-binding protein phosphorylation in dorsal horn neurons, leading to central sensitization J Neurosci 24 2004 8310 8321 (Pubitemid 39280810)
41. V. Kayser, K.J. Berkley, H. Keita, M. Gautron, and G. Guilbaud Estrous and sex variations in vocalization thresholds to hindpaw and tail pressure stimulation in the rat Brain Res 742 1996 352 354 (Pubitemid 27016044)
42. M.B. Klinger, S. Sacks, and F. Cervero A role for extracellular signal-regulated kinases 1 and 2 (ERK 1/2) in the maintenance of persistent mechanical hyperalgesia in ovariectomized mice Neurosci 172 2010 483 493
43. G. Krapivinsky, L. Krapivinsky, Y. Manasian, A. Ivanov, R. Tyzio, C. Pellegrino, Y. Ben Ari, D.E. Clapham, and I. Medina The NMDA receptor is coupled to the ERK pathway by a direct interaction between NR2B and RasGRF1 Neuron 40 2003 775 784 (Pubitemid 37431037)
44. L. Leventhal, M.R. Brandt, T.A. Cummons, M.J. Piesla, K.E. Rogers, and H.A. Harris An estrogen receptor-beta agonist is active in models of inflammatory and chemical-induced pain Eur J Pharmacol 553 2006 146 148 (Pubitemid 44779596)
45. E.R. Levin Integration of the extranuclear and nuclear actions of estrogen Mol Endocrinol 19 2005 1951 1959 (Pubitemid 41124194)
46. E.R. Levin Plasma membrane estrogen receptors Trends Endocrinol Metab 20 2009 477 482
47. B. Liu, J.C. Eisenach, and C. Tong Chronic estrogen sensitizes a subset of mechanosensitive afferents innervating the uterine cervix J Neurophysiol 93 2005 2167 2173 (Pubitemid 40404414)
48. F. Liu, M. Day, L.C. Muniz, D. Bitran, R. Arias, R. Revilla-Sanchez, S. Grauer, G. Zhang, C. Kelley, V. Pulito, A. Sung, R.F. Mervis, R. Navarra, W.D. Hirst, P.H. Reinhart, K.L. Marquis, S.J. Moss, M.N. Pangalos, and N.J. Brandon Activation of estrogen receptor-beta regulates hippocampal synaptic plasticity and improves memory Nat Neurosci 11 2008 334 343 (Pubitemid 351311804)
49. C.S. Liverman, J.W. Brown, R. Sandhir, R.M. Klein, K. McCarson, and N.E. Berman Oestrogen increases nociception through ERK activation in the trigeminal ganglion: evidence for a peripheral mechanism of allodynia Cephalalgia 29 2009 520 531
50. M. Maggiolini, and D. Picard The unfolding stories of GPR30, a new membrane-bound estrogen receptor J Endocrinol 204 2010 105 114
51. C.A. Mannino, S.M. South, V. Quinones-Jenab, and C.E. Inturrisi Estradiol replacement in ovariectomized rats is antihyperalgesic in the formalin test J Pain 8 2007 334 342 (Pubitemid 46551875)
52. J. Matthews, and J.A. Gustafsson Estrogen signaling: a subtle balance between ER alpha and ER beta Mol Interv 3 2003 281 292
53. J.A. McRoberts, J. Li, H.S. Ennes, and E.A. Mayer Sex-dependent differences in the activity and modulation of N-methyl-d-aspartic acid receptors in rat dorsal root ganglia neurons Neuroscience 148 2007 1015 1020 (Pubitemid 47422390)
54. I. Merchenthaler, M.V. Lane, S. Numan, and T.L. Dellovade Distribution of estrogen receptor alpha and beta in the mouse central nervous system: in vivo autoradiographic and immunocytochemical analyses J Comp Neurol 473 2004 270 291 (Pubitemid 38569232)
55. P.G. Mermelstein Membrane-localised oestrogen receptor alpha and beta influence neuronal activity through activation of metabotropic glutamate receptors J Neuroendocrinol 21 2009 257 262
56. P. Micevych, and R. Dominguez Membrane estradiol signaling in the brain Front Neuroendocrinol 30 2009 315 327
57. J. Nilsen, and R.D. Brinton Divergent impact of progesterone and medroxyprogesterone acetate (Provera) on nuclear mitogen-activated protein kinase signaling Proc Natl Acad Sci USA 100 2003 10506 10511 (Pubitemid 37071908)
58. R.E. Papka, M. Storey-Workley, P.J. Shughrue, I. Merchenthaler, J.J. Collins, S. Usip, P.T. Saunders, and M. Shupnik Estrogen receptor-alpha and beta-immunoreactivity and mRNA in neurons of sensory and autonomic ganglia and spinal cord Cell Tissue Res 304 2001 193 214 (Pubitemid 32454506)
59. F. Piu, C. Cheevers, L. Hyldtoft, L.R. Gardell, A.L. Del Tredici, C.B. Andersen, L.C. Fairbairn, B.W. Lund, M. Gustafsson, H.H. Schiffer, J.E. Donello, R. Olsson, D.W. Gil, and M.R. Brann Broad modulation of neuropathic pain states by a selective estrogen receptor beta agonist Eur J Pharmacol 590 2008 423 429
60. E.R. Prossnitz, J.B. Arterburn, and L.A. Sklar GPR30: a G protein-coupled receptor for estrogen Mol Cell Endocrinol 265-266 2007 138 142 (Pubitemid 46273957)
61. A.P. Raval, I. Saul, K.R. Dave, R.A. DeFazio, M.A. Perez-Pinzon, and H. Bramlett Pretreatment with a single estradiol-17beta bolus activates cyclic-AMP response element binding protein and protects CA1 neurons against global cerebral ischemia Neuroscience 160 2009 307 318
62. M. Razandi, A. Pedram, G.L. Greene, and E.R. Levin Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: studies of ERalpha and ERbeta expressed in Chinese hamster ovary cells Mol Endocrinol 13 1999 307 319 (Pubitemid 29068005)
63. A. Robbins, K.J. Berkley, and Y. Sato Estrous cycle variation of afferent fibers supplying reproductive organs in the female rat Brain Res 596 1992 353 356
64. M.T. Robbins, H. Mebane, C.L. Ball, A.D. Shaffer, and T.J. Ness Effect of estrogen on bladder nociception in rats J Urol 183 2010 1201 1205
65. M.W. Salter, and L.V. Kalia SRC kinases: a hub for NMDA receptor regulation Nat Rev Neurosci 5 2004 317 328 (Pubitemid 38478658)
66. R. Sanoja, and F. Cervero Estrogen-dependent abdominal hyperalgesia induced by ovariectomy in adult mice: a model of functional abdominal pain Pain 118 2005 243 253 (Pubitemid 41566605)
67. R. Sanoja, and F. Cervero Estrogen modulation of ovariectomy-induced hyperalgesia in adult mice Eur J Pain 12 2008 573 581 (Pubitemid 351615306)
68. S. Sapsed-Byrne, D. Ma, D. Ridout, and A. Holdcroft Estrous cycle phase variations in visceromotor and cardiovascular responses to colonic distension in the anesthetized rat Brain Res 742 1996 10 16 (Pubitemid 27016002)
69. P.J. Shughrue, M.V. Lane, and I. Merchenthaler Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system J Comp Neurol 388 1997 507 525 (Pubitemid 27481288)
70. S.E. Slack, S. Pezet, S.B. McMahon, S.W. Thompson, and M. Malcangio Brain-derived neurotrophic factor induces NMDA receptor subunit one phosphorylation via ERK and PKC in the rat spinal cord Eur J Neurosci 20 2004 1769 1778 (Pubitemid 39471570)
71. T. Smejkalova, and C.S. Woolley Estradiol acutely potentiates hippocampal excitatory synaptic transmission through a presynaptic mechanism J Neurosci 30 2010 16137 16148
72. M.F. Spooner, P. Robichaud, J.C. Carrier, and S. Marchand Endogenous pain modulation during the formalin test in estrogen receptor beta knockout mice Neuroscience 150 2007 675 680 (Pubitemid 350198731)
73. E.C. Stoffel, C.M. Ulibarri, and R.M. Craft Gonadal steroid hormone modulation of nociception, morphine antinociception and reproductive indices in male and female rats Pain 103 2003 285 302 (Pubitemid 36644167)
74. B. Tang, Y. Ji, and R.J. Traub Estrogen alters spinal NMDA receptor activity via a PKA signaling pathway in a visceral pain model in the rat Pain 137 2008 540 549
75. A. Tashiro, K. Okamoto, and D.A. Bereiter Chronic inflammation and estradiol interact through MAPK activation to affect TMJ nociceptive processing by trigeminal caudalis neurons Neuroscience 164 2009 1813 1820
76. J.M. Terner, L.M. Lomas, and M.J. Picker Influence of estrous cycle and gonadal hormone depletion on nociception and opioid antinociception in female rats of four strains J Pain 6 2005 372 383 (Pubitemid 40804342)
77. G.M. Thomas, and R.L. Huganir MAPK cascade signalling and synaptic plasticity Nat Rev Neurosci 5 2004 173 183 (Pubitemid 38252474)
78. R.J. Traub Evidence for thoracolumbar spinal cord processing of inflammatory, but not acute colonic pain NeuroReport 11 2000 2113 2116 (Pubitemid 30485545)
79. R.J. Traub, T. Herdegen, and G.F. Gebhart Differential expression of c-Fos and c-Jun in two regions of the rat spinal cord following noxious colorectal distention Neurosci Lett 160 1993 121 125 (Pubitemid 23294721)
80. R.J. Traub, Q.Z. Zhai, Y. Ji, and M. Kovalenko NMDA receptor antagonists attenuate noxious and nonnoxious colorectal distention-induced Fos expression and the visceromotor reflex Neurosci 113 2002 205 211 (Pubitemid 34786025)
81. V.G. VanderHorst, J.A. Gustafsson, and B. Ulfhake Estrogen receptor-alpha and -beta immunoreactive neurons in the brainstem and spinal cord of male and female mice. relationships to monoaminergic, cholinergic, and spinal projection systems J Comp Neurol 488 2005 152 179 (Pubitemid 40846457)
82. V.G. VanderHorst, E. Terasawa, and H.J. Ralston III Estrogen receptor-alpha immunoreactive neurons in the ventrolateral periaqueductal gray receive monosynaptic input from the lumbosacral cord in the rhesus monkey J Comp Neurol 443 2002 27 42 (Pubitemid 34027567)
83. V.G.J.M. VanderHorst, E. Terasawa, and H.J. Ralston III Estrogen receptor-[alpha] immunoreactive neurons in the brainstem and spinal cord of the female rhesus monkey: species-specific characteristics Neuroscience 158 2009 798 810
84. N. Vasudevan, and D.W. Pfaff Non-genomic actions of estrogens and their interaction with genomic actions in the brain Front Neuroendocrinol 29 2008 238 257
85. R. Waltereit, and M. Weller Signaling from cAMP/PKA to MAPK and synaptic plasticity Mol Neurobiol 27 2003 99 106 (Pubitemid 36515162)
86. G. Wang, B. Tang, and R.J. Traub Differential processing of noxious colonic input by thoracolumbar and lumbosacral dorsal horn neurons in the rat J Neurophysiol 94 2005 3788 3794 (Pubitemid 41691745)
87. E.M. Waters, K. Mitterling, J.L. Spencer, S. Mazid, B.S. McEwen, and T.A. Milner Estrogen receptor alpha and beta specific agonists regulate expression of synaptic proteins in rat hippocampus Brain Res 1290 2009 1 11
88. C.S. Woolley, N.G. Weiland, B.S. McEwen, and P.A. Schwartzkroin Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density J Neurosci 17 1997 1848 1859 (Pubitemid 27089829)
89. X.J. Zhang, Z. Li, E.K. Chung, H.Q. Zhang, H.X. Xu, J.J. Sung, and Z.X. Bian Activation of extracellular signal-regulated protein kinase is associated with colorectal distension-induced spinal and supraspinal neuronal response and neonatal maternal separation-induced visceral hyperalgesia in rats J Mol Neurosci 37 2009 274 287
90. L. Zhao, and R.D. Brinton Estrogen receptor alpha and beta differentially regulate intracellular Ca(2+) dynamics leading to ERK phosphorylation and estrogen neuroprotection in hippocampal neurons Brain Res 1172 2007 48 59 (Pubitemid 47417943)