Estrogen modulation of peripheral pain signal transduction: Involvement of P2X3 receptors

Purinergic Signalling

Volumn 7, Issue 1, 2011, Pages 73-83

  Ma, Bei ^a   Yu, Li hua ^a   Fan, Juan ^a   Cong, Binhai ^a   He, Ping ^a   Ni, Xin ^a   Burnstock, Geoffrey ^b  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

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

Author keywords

ATP; Estrogen; Ovariectomy; P2X receptors; Pain

Indexed keywords

EID: 79953079824     PISSN: 15739538     EISSN: 15739546     Source Type: Journal    
DOI: 10.1007/s11302-010-9212-9     Document Type: Article

References (58)

1. Fillingim RB (2000) Sex, gender, and pain: women and men really are different. Curr Rev Pain 4(1): 24-30.
2. Greenspan JD, Craft RM, LeResche L, Arendt-Nielsen L, Berkley KJ, Fillingim RB, Gold MS, Holdcroft A, Lautenbacher S, Mayer EA, Mogil JS, Murphy AZ, Traub RJ (2007) Consensus Working Group of the Sex, Gender, and Pain SIG of the IASP. Pain 132(Suppl 1): S26-S45.
3. Craft RM (2007) Modulation of pain by estrogens. Pain 132: S3-S12.
4. Butcher RL, Collins WE, Fugo NW (1974) Plasma concentration of LH, FSH, prolactin, progesterone, and estradiol-17beta throughout the 4-day estrous cycle of the rat. Endocrinology 94: 1704-1708.
5. Frye CA, Bock BC, Kanarek RB (1992) Hormonal milieu affects tailflick latency in female rats and may be attenuated by access to sucrose. Physiol Behav 52: 699-706.
6. Frye CA, Cuevas CA, Kanarek RB (1993) Diet and estrous cycle influence pain sensitivity in rats. Pharmacol Biochem Behav 45: 255-260.
7. Fischer L, Torres-Chávez KE, Clemente-Napimoga JT, Jorge D, Arsati F, de Arruda Veiga MC, Tambeli CH (2008) The influence of sex and ovarian hormones on temporomandibular joint nociception in rats. J Pain 9(7): 630-638.
8. Sanoja R, Cervero F (2005) Estrogen-dependent abdominal hyperalgesia induced by ovariectomy in adult mice: a model of functional abdominal pain. Pain 118(1-2): 243-253.
9. Sanoja R, Cervero F (2008) Estrogen modulation of ovariectomy-induced hyperalgesia in adult mice. Eur J Pain 12: 573-581.
10. Stoffel EC, Ulibarri CM, Craft RM (2003) Gonadal steroid hormone modulation of nociception, morphine antinociception and reproductive indices in male and female rats. Pain 103: 285-302.
11. Formanl LJ, Tingle V, Estilow S, Cater J (1989) The response to analgesia testing is affected by gonadal steroids in the rat. Life Sci 45(5): 447-454.
12. Bradshaw HB, Berkley KJ (2002) Estrogen replacement reverses ovariectomy-induced vaginal hyperalgesia in the rat. Maturitas 41: 157-165.
13. Gintzler AR, Bohan MC (1990) Pain thresholds are elevated during pseudopregnancy. Brain Res 507(2): 312-316.
14. Dawson-Basoa ME, Gintzler AR (1998) Gestational and ovarian sex steroid antinociception: synergy between spinal and opioid system. Brain Res 757: 37-42.
15. Unruh AM (1996) Gender variations in clinical pain experience. Pain 65: 123-167.
16. Berkley KJ (1997) Sex differences in pain. Behav Brain Sci 20: 371-380.
17. Robbins A, Berkley KJ, Sato Y (1992) Estrous cycle variation of afferent fibers supplying reproductive organs in the female rat. Brain Res 596(1-2): 353-356.
18. Sapsed-Byrne S, Ma D, Ridout D, Holdcroft A (1996) Estrous cycle phase variations in visceromotor and cardiovascular responses to colonic distension in the anesthetized rat. Brain Res 742(1-2): 10-16.
19. Holdcroft A, Sapsed-Byrne S, Ma D, Hammal D, Forsling ML (2000) Sex and oestrous cycle differences in visceromotor responses and vasopressin release in response to colonic distension in male and female rats anaesthetized with halothane. Br J Anaesth 85(6): 907-910.
20. Aloisi AM, Bonifazi M (2006) Sex hormones, central nervous system and pain. Horm Behav 50: 1-7.
21. Bettini E, Pollio G, Santagati S, Maggi A (1992) Estrogen receptor in rat brain: presence in the hippocampal formation. Neuroendocrinology 56(4): 502-508.
22. 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(4): 1153-1163.
23. Taleghany N, Sarajari S, DonCarlos LL, Gollapudi L, Oblinger MM (1999) Differential expression of estrogen receptor alpha and beta in rat dorsal root ganglion neurons. J Neurosci Res 57: 603-615.
24. Xiang Z, Bo X, Burnstock G (1998) Localization of ATP-gated P2X receptor immunoreactivity in rat sensory and sympathetic ganglia. Neurosci Lett 256(2): 105-108.
25. Burnstock G (2007) Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev 87(2): 659-797.
26. 3-deficient mice. Nature 407(6807): 1011-1015.
27. 2 receptor subunit in mediating multiple sensory effects of ATP. J Physiol 567(Pt 2): 621-639.
28. 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.
29. Ma B, Rong W, Dunn PM, Burnstock G (2005) 17β-estradiol attenuates α,β-meATP-induced currents in rat dorsal root ganglion neurons. Life Sci 76(22): 2547-2558.
30. 3 receptor subunit messenger RNA expression in the female mouse bladder after oophorectomy with or without estrogen replacement. Am J Obstet Gynecol 187(1): 103-106.
31. Papka RE, Hafemeister J, Storey-Workley M (2005) P2X receptors in the rat uterine cervix, lumbosacral dorsal root ganglia, and spinal cord during pregnancy. Cell Tissue Res 321(1): 35-44.
32. McGaraughty S, Wismer CT, Zhu CZ, Mikusa J, Honore P, Chu KL, Lee CH, Faltynek CR, Jarvis MF (2003) Effects of A-317491, a novel and selective P2X3/P2X2/3 receptor antagonist, on neuropathic, inflammatory and chemogenic nociception following intrathecal and intraplantar administration. Br J Pharmacol 140(8): 1381-1388.
33. Hamilton SG, Wade A, McMahon SB (1999) The effects of inflammation and inflammatory mediators on nociceptive behaviour induced by ATP analogues in the rat. Br J Pharmacol 126(1): 326-332.
34. Sawynok J, Reid A (1997) Peripheral adenosine 5′-triphosphate enhances nociception in the formalin test via activation of a purinergic p2X receptor. Eur J Pharmacol 330(2-3): 115-121.
35. Gorodeski GI (1998) Estrogen increases the permeability of the cultured human cervical epithelium by modulating cell deformability. Am J Physiol 275: C888-C899.
36. Jarvis MF, Wismer CT, Schweitzer E, Yu H, van Biesen T, Lynch KJ, Burgard EC, Kowaluk EA (2001) Modulation of BzATP and formalin induced nociception: attenuation by the P2X receptor antagonist, TNP-ATP and enhancement by the P2X(3) allosteric modulator, cibacron blue. Br J Pharmacol 132(1): 259-269.
37. Tsuda M, Shigemoto-Mogami Y, Koizumi S, Mizokoshi A, Kohsaka S, Salter MW, Inoue K (2003) P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 424(6950): 778-783.
38. Wakeling AE, Dukes M, Bowler JA (1991) A potent specific pure antiestrogen with clinical potential. Cancer Res 51: 3867-3873.
39. Gaumond I, Arsenault P, Marchand S (2002) The role of sex hormones on formalin-induced nociceptive responses. Brain Res 958(1): 139-145.
40. Gaumond I, Arsenault P, Marchand S (2005) Specificity of female and male sex hormones on excitatory and inhibitory phases of formalin-induced nociceptive responses. Brain Res 1052(1): 105-111.
41. Mannino CA, South SM, Quinones-Jenab V, Inturrisi CE (2007) Estradiol replacement in ovariectomized rats is antihyperalagesic in the formalin test. J Pain 8(4): 334-342.
42. Cutolo M, Villaggio B, Foppiani L, Briata M, Sulli A, Pizzorni C, Faelli F, Prete C, Felli L, Seriolo B, Giusti M (2000) The hypothalamic-pituitary-adrenocortical and gonadal axis function in rheumatoid arthritis. Z Rheumatol 59(Suppl): S65-S69.
43. Navarro MA, Nolla JM, Machuca MI, González A, Mateo L, Bonnin RM, Roig-Escofet D (1998) Salivary testosterone in postmenopausal women with rheumatoid arthritis. J Rheumatol 25: 1059-1062.
44. Green PG, Dahlqvist SR, Isenberg WM, Strausbaugh HJ, Miao FJ, Levine JD (1999) Sex steroid regulation of the inflammatory response: sympathoadrenal dependence in the female rat. J Neurosci 19: 4082-4089.
45. Beyenburg S, Stoffel-Wagner B, Bauer J, Watzka M, Blumcke I, Bidlingmaier F, Elger CE (2001) Neuroactive steroids and seizure susceptibility. Epilepsy Res 44: 141-153.
46. Hammer RP Jr, Bridges RS (1987) Preoptric area opiods and opiate receptors increase during pregnancy and decrease during lactation. Brain Res 420(1): 48-56.
47. Dondi D, Limonta P, Maggi R, Piva F (1992) Effects of ovarian hormones on brain opioid binding sites in castrated female rats. Am J Physiol 263(3 Pt 1): E507-E511.
48. Quinones-Jenab V, Jenab S, Ogawa S, Inturrisi C, Pfaff DW (1997) Estrogen regulation of mu-opioid receptor mRNA in the forebrain of female rats. Brain Res Mol Brain Res 47(1-2): 134-138.
49. Amandusson A, Hallbeck M, Hallbeck AL, Hermanson O, Blomqvist A (1999) Estrogen-induced alterations of spinal cord enkephalin gene expression. Pain 83(2): 243-248.
50. Burnstock G, Wood JN (1996) Purinergic receptors: their role in nociception and primary afferent neurotransmission. Curr Opin Neurobiol 6(4): 526-532.
51. Chen CC, Akopian AN, Sivilotti L, Colquhoun D, Burnstock G, Wood JN (1995) A P2X purinoreceptors expressed by a subset of sensory neurons. Nature 377: 428-431.
52. 3 receptor subunits can account for ATP-gated currents in sensory neurons. Nature 377: 432-435.
53. 3 receptors and peripheral pain mechanisms. J Physiol 554: 301-308.
54. Kobayashi K, Fukuoka T, Yamanaka H, Dai Y, Obata K, Tokunaga A, Noguchi K (2005) Differential expression patterns of mRNAs for P2X receptor subunits in neurochemically characterized dorsal root ganglion neurons in the rat. J Comp Neurol 481: 377-390.
55. Li L, Fan X, Warner M, Lili Li XuX-J, Gustafsson J-A, Wiesenfeld-Hallin Z (2009) Ablation of estrogen receptor α or β eliminates sex differences in mechanical pain threshold in normal and inflamed mice. Pain 143: 37-40.
56. Fan XT, Kim H-J, Warner M, Gustafsson J (2007) Estrogen receptor β is essential for sprouting of nociceptive primary afferents and for morphogenesis and maintenance of the dorsal horn interneurons. Proc Natl Acad Sci USA 104: 13696-13701.
57. Xu GY, Huang LY (2002) Peripheral inflammation sensitizes P2X receptor mediated responses in rat dorsal root ganglion neurons. J Neurosci 22: 93-102.
58. 2+/calmodulin-dependent protein kinase II potentiates ATP responses by promoting trafficking of P2X receptors. Proc Natl Acad Sci USA 101: 11868-11873.