17β-estradiol rapidly attenuates P2X3 receptor-mediated peripheral pain signal transduction via ERα and GPR30

Endocrinology

Volumn 154, Issue 7, 2013, Pages 2421-2433

  Lu, Yi ^a   Jiang, Qian ^a   Yu, Lihua ^a   Lu, Zhan Ying ^a   Meng, Shuang Ping ^a   Su, Dingfeng ^b   Burnstock, Geoffrey ^c,d   Ma, Bei ^a  

^a BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 4,49,499 (4 PROPYL [1H] PYRAZOLE 1,3,5 TRIYL) TRISPHENOL; ALPHA,BETA METHYLENEADENOSINE DIPHOSPHATE; ALPHA,BETA METHYLENEADENOSINE TRIPHOSPHATE; ANTIESTROGEN; CYCLIC AMP DEPENDENT PROTEIN KINASE; DIARYLPROPIONITRILE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FORSKOLIN; G PROTEIN COUPLED RECEPTOR 30; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE C; PURINERGIC P2X3 RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; DOSE RESPONSE; ENZYME INHIBITION; ESTRADIOL BLOOD LEVEL; FEMALE; IMMUNOHISTOCHEMISTRY; NONHUMAN; OVARIECTOMY; PAIN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SPINAL GANGLION;

EID: 84879313738     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-2119     Document Type: Article

References (62)

1. Berkley KJ. Sex differences in pain. Behav Brain Sci. 1997;20:371-380; discussion 435-513.
2. Unruh AM. Gender variations in clinical pain experience. Pain. 1996;65:123-167. (Pubitemid 26228032)
3. Fillingim RB, King CD, Ribeiro-Dasilva MC, Rahim-Williams B, Riley JL. Sex, gender, and pain: a review of recent clinical and experimental findings. J Pain. 2009;10:447-485.
4. Gintzler AR, Liu NJ. Importance of sex to pain and its amelioration; relevance of spinal estrogens and its membrane receptors. Front Neuroendocrinol. 2012;33(4):412-424.
5. Bradshaw HB, Berkley KJ. Estrous changes in responses of rat gracile nucleus neurons to stimulation of skin and pelvic viscera. J Neurosci. 2000;20:7722-7727.
6. Kramer PR, Bellinger LL. The effects of cycling levels of 17beta-estradiol and progesterone on the magnitude of temporomandibular joint-induced nociception. Endocrinology. 2009;150:3680-3689.
7. Sanoja R, Cervero F. Estrogen-dependent abdominal hyperalgesia induced by ovariectomy in adult mice: a model of functional abdominal pain. Pain. 2005;118(1-2):243-253. (Pubitemid 41566605)
8. Stoffel EC, Ulibarri CM, Craft RM. Gonadal steroid hormone modulation of nociception, morphine antinociception and reproductive indices in male and female rats. Pain. 2003;103:285-302. (Pubitemid 36644167)
9. Bradshaw HB, Berkley KJ. Estrogen replacement reverses ovariectomy-induced vaginal hyperalgesia in the rat. Maturitas. 2002;41:157-165. (Pubitemid 34142505)
10. Allen AL, McCarson KE. Estrogen increases nociception-evoked brain-derived neurotrophic factor gene expression in the female rat. Neuroendocrinology. 2005;81:193-199. (Pubitemid 41158959)
11. Bereiter DA, Okamoto K, Bereiter DF. 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. 2005;117:58-67. (Pubitemid 41781614)
12. Hunter DA, Barr GA, Amador N, et al. Estradiol-induced antinociceptive responses on formalin-induced nociception are independent of COX and HPA activation. Synapse. 2011;65:643-651.
13. Coulombe MA, Spooner MF, Gaumond I, Carrier JC, Marchand S. Estrogen receptors β and α have specific pro- and anti-nociceptive actions. Neuroscience. 2011;184:172-182.
14. Kato S, Sato T, Watanabe T, et al. Function of nuclear sex hormone receptors in gene regulation. Cancer Chemother Pharmacol 2005;56(Suppl 1):4-9.
15. Deroo BJ, Korach KS. Estrogen receptors and human disease. J Clin Invest. 2006;116(3):561-570. (Pubitemid 43326860)
16. Razandi M, Pedram A, Greene GL, Levin ER. Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: studies of ERα and ERβ expressed in Chinese hamster ovary cells. Mol Endocrinol. 1999;13:307-319. (Pubitemid 29068005)
17. Clarke CH, Norfleet AM, Clarke MS, Watson CS, Cunningham KA, Thomas ML. Perimembrane localization of the estrogen receptor α protein in neuronal processes of cultured hippocampal neurons. Neuroendocrinology. 2000;71:34-42. (Pubitemid 30045333)
18. Watson CS, Campbell CH, Gametchu B. The dynamic and elusive membrane estrogen receptor-α. Steroids. 2002;67:429-437. (Pubitemid 34311757)
19. Fehrenbacher JC, Loverme J, Clarke W, Hargreaves KM, Piomelli D, Taylor BK. Rapid pain modulation with nuclear receptor ligands. Brain Res Rev. 2009;60(1):114-124.
20. Chambliss KL, Yuhanna IS, Mineo C, Liu P, German Z, Sherman TS, Mendelsohn ME, Anderson RG, Shaul PW. Estrogen receptor α and endothelial nitric oxide synthase are organized into a functional signaling module in caveolae. Circ Res. 2000;87:E44-E52.
21. Acconcia F, Bocedi A, Ascenzi P, Marino M. Does palmitoylation target estrogen receptors to plasma membrane caveolae? IUBMB Life. 2003;55:33-35. (Pubitemid 36427597)
22. Notas G, Kampa M, Pelekanou V, Castanas E. Interplay of estrogen receptors and GPR30 for the regulation of early membrane initiated transcriptional effects: a pharmacological approach. Steroids. 2012;77(10):943-950.
23. 2+signaling in mouse dorsal root ganglion neurons. J Neurosci Res. 2005;81(1):31-37.
24. Xu S, Cheng Y, Keast JR, Osborne PB. 17β-Estradiol activates estrogen receptor-signalling and inhibits transient receptor potential vanilloid receptor 1 activation by capsaicin in adult rat nociceptor neurons. Endocrinology. 2008;149:5540-5548.
25. Cao DY, Ji Y, Tang B, Traub RJ. Estrogen receptor β activation is antinociceptive in a model of visceral pain in the rat. J Pain. 2012;13(7):685-694.
26. Olde B, Leeb-Lundberg LM. GPR30/GPER1: searching for a role in estrogen physiology. Trends in Endocrinology and Metabolism. 2009;20(8):409-416.
27. Prossnitz ER, Arterburn JB, Sklar LA. GPR30: a G protein-coupled receptor for estrogen. Mol Cell Endocrinol. 2007;265-266:138-142. (Pubitemid 46273957)
28. Prossnitz ER, Barton M. The G-protein-coupled estrogen receptor GPER in health and disease. Nat Rev Endocrinol. 2011;7:715-726.
29. Liverman CS, Brown JW, Sandhir R, McCarson KE, Berman NE. Role of the oestrogen receptors GPR30 and ERα in peripheral sensitization: relevance to trigeminal pain disorders in women. Cephalalgia. 2009;29(7):729-741.
30. Dun SL, Brailoiu GC, Gao X, et al. Expression of estrogen receptor GPR30 in the rat spinal cord and in autonomic and sensory ganglia. J Neurosci Res. 2009;87(7):1610-1619.
31. Burnstock G, Kennedy C. P2X receptors in health and disease. Adv Pharmacol. 2011;61:333-372.
32. Hamilton SG, McMahon SB. ATP as a peripheral mediator of pain. J Auton Nerv Syst. 2000;81:187-194. (Pubitemid 30408497)
33. North RA. P2X3 receptors and peripheral pain mechanisms. J Physiol. 2004;554(Pt 2):301-308. (Pubitemid 38181345)
34. Stanfa LC, Kontinen VK, Dickenson AH. Effects of spinally administered P2X receptor agonists and antagonists on the responses of dorsal horn neurones recorded in normal, carrageenan-inflamed and neuropathic rats. Br J Pharmacol. 2000;29:351-359. (Pubitemid 30072656)
35. Cockayne DA, Hamilton SG, Zhu et al. Urinary bladder hyporeflexia and reduced pain-related behaviour in P2X3-deficient mice. Nature. 2000;407(6807):1011-1015.
36. Carley ME, Cliby WA, Spelsberg TC. P2X(3) receptor subunit messenger RNA expression in the female mouse bladder after oophorectomy with or without estrogen replacement. Am J Obstet Gynecol. 2002;187(1):103-106. (Pubitemid 34800308)
37. Papka RE, Hafemeister J, Storey-Workley M. P2X receptors in the rat uterine cervix, lumbosacral dorsal root ganglia, and spinal cord during pregnancy. Cell Tissue Res. 2005;321(1):35-44. (Pubitemid 40984837)
38. Ma B, Rong W, Dunn PM, Burnstock G. 17β-Estradiol attenuates α,β-meATP-induced currents in rat dorsal root ganglion neurons. Life Sciences. 2005;76(22):2547-2558. (Pubitemid 40354257)
39. Ma B, Yu LH, Fan J, Cong B, He P, Ni X. Estrogen modulation of peripheral pain signal transduction: involvement of P2X(3) receptors. Purinergic Signal. 2011;7:73-83.
40. Ji Y, Tang B, Traub RJ. Spinal estrogen receptor α mediates estradiol-induced pronociception in a visceral pain model in the rat. Pain. 2011;152(5):1182-1191.
41. Liu NJ, Chakrabarti S, Schnell S, Wessendorf M, Gintzler AR. Spinal synthesis of estrogen and concomitant signaling by membrane estrogen receptors regulate spinal κ- and μ-opioid receptor heterodimerization and female-specific spinal morphine antinociception. J Neurosci. 2011;131(33):1836-11845.
42. Taleghany N, Sarajari S, DonCarlos LL, Gollapudi L, Oblinger MM. Differential expression of estrogen receptor alpha and beta in rat dorsal root ganglion neurons. J Neurosci Res. 1999;57(5):603-615. (Pubitemid 29411475)
43. Lu CL, Hsieh JC, Dun NJ, et al. Estrogen rapidly modulates 5-hy-droxytrytophan-induced visceral hypersensitivity via GPR30 in rats. Gastroenterology. 2009;137(3):1040-1050.
44. Revankar CM, Mitchell HD, Field AS, et al. Synthetic estrogen derivatives demonstrate the functionality of intracellular GPR30. ACS Chem Biol. 2007;2:536-544. (Pubitemid 350011324)
45. Kuhn J, Dina OA, Goswami C, Suckow V, Levine JD, Hucho T. GPR30 estrogen receptor agonists induce mechanical hyperalgesia in the rat. Eur J Neurosci. 2008;27(7):1700-1709. (Pubitemid 351473574)
46. Zhu W, Xu P, Cuascut FX, Hall AK, Oxford GS. Activin acutely sensitizes dorsal root ganglion neurons and induces hyperalgesia via PKC-mediated potentiation of transient receptor potential vanilloid I. J Neurosci. 2007;27(50):13770-13780. (Pubitemid 350278254)
47. Goswami C, Kuhn J, Dina OA, et al. Estrogen destabilizes microtubules through an ion-conductivity-independent TRPV1 pathway. J Neurochem. 2011;117(6):995-1008.
48. Thomas P, Pang Y, Filardo EJ, Dong J. Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology. 2005;146(2):624-632. (Pubitemid 40129818)
49. Prossnitz ER, Maggiolini M. Mechanisms of estrogen signaling and gene expression via GPR30. Mol Cell Endocrinol. 2009;308(1-2):32-38.
50. Vivacqua A, Bonofiglio D, Albanito L, et al. 17β-Estradiol genistein, and 4-hydroxytamxifen induce the proliferation of thyroid cancer cells through the g protein-coupled receptor GPR30. Mol Pharmacol. 2006;70:1414-1423. (Pubitemid 44435994)
51. Revankar CM, Cimino DF, Sklar LA, Arterburn JB, Prossnitz ER. Atransmembrane intracellular estrogen receptor mediates rapid cell signaling. Science. 2005;307:1625-1630. (Pubitemid 40354745)
52. Dennis MK, Burai R, Ramesh C, et al. In vivo effects of a GPR30 antagonist. Nat Chem Biol. 2009;5:421-427.
53. Impey S, Obrietan K, Storm DR. Making new connections: role of ERK/MAP kinase signaling in neuronal plasticity. Neuron. 1999;23:11-14. (Pubitemid 29262459)
54. Cheng Y, Keast JR. Effects of estrogens and bladder inflammation on mitogen-activated protein kinases in lumbosacral dorsal root ganglia from adult female rats. BMC Neurosci. 2009;10:156.
55. Klinger MB, Sacks S, Cervero F. A role for extracellular signal-regulated kinases1 and 2 in the maintenance of persistent mechanical hyperalgesia in ovariectomized mice. Neuroscience. 2011;172:483-493.
56. Hu HJ, Glauner KS, Gereau RW 4th. ERK integrates PKA and PKC signaling in superficial dorsal horn neurons. I. Modulation of A-type K+currents. J Neurophysiol. 2003;90:1671-1679. (Pubitemid 37129376)
57. Hu HJ, Gereau RW 4th. ERK integrates PKA and PKC signaling in superficial dorsal horn neurons. II. Modulation of neuronal excitability. J Neurophysiol. 2003;90:1680-1688.
58. +current requires the βγ subunits of Go protein, protein kinase A, and extracellular signal-regulated kinase 1/2 (ERK1/2) in sensory neurons. J Biol Chem. 2012;287(22):18562-18572.
59. Wirkner K, Stanchev D, Köles L, et al. Regulation of human recombinant P2X3 receptors by ecto-protein kinase C. J Neurosci. 2005;25(34):7734-7742. (Pubitemid 41208644)
60. Kawabata A. Prostaglandin E2 and pain - an update. Biol Pharm Bull. 2011;34(8):1170-1173.
61. Brown DA, Yule DI. Protein kinase C regulation of P2X3 receptors is unlikely to involve direct receptor phosphorylation. Biochim Biophys Acta. 2007;1773(2):166-175. (Pubitemid 46123612)
62. Wang S, Dai Y, Kobayashi K, et al. Potentiation of the P2X3 ATP receptor by PAR-2 in rat dorsal root ganglia neurons, through protein kinase-dependent mechanisms, contributes to inflammatory pain. Eur J Neurosci. 2012;36(3):2293-2301.