17β-estradiol enhances ASIC activity in primary sensory neurons to produce sex difference in acidosis-induced nociception

Endocrinology (United States)

Volumn 156, Issue 12, 2015, Pages 4660-4671

  Qu, Zu Wei ^a   Liu, Ting Ting ^a   Ren, Cuixia ^a   Gan, Xiong ^a   Qiu, Chun Yu ^a   Ren, Ping ^a   Rao, Zhiguo ^b   Hu, Wang Ping ^a  

^a HUBEI UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b General Hospital of Wuhan Military   (China)

Author keywords

[No Author keywords available]

Indexed keywords

1,3,5 TRIS(4 HYDROXYPHENYL) 4 PROPYLPYRAZOLE; ACETIC ACID; ACID SENSING ION CHANNEL; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTON; 1,3,5-TRIS(4-HYDROXYPHENYL)-4-PROPYL-1H-PYRAZOLE; 2,3-BIS(4-HYDROXYPHENYL)-PROPIONITRILE; ESTROGEN RECEPTOR BETA; NITRILE; PHENOL DERIVATIVE; PYRAZOLE DERIVATIVE;

ACIDOSIS; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; ION CURRENT; MALE; MEMBRANE DEPOLARIZATION; NERVE CELL EXCITABILITY; NOCICEPTION; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; SEX DIFFERENCE; SPIKE; SPINAL GANGLION; AGONISTS; ANIMAL; ANIMAL BEHAVIOR; CELL MEMBRANE; CYTOLOGY; DRUG EFFECTS; METABOLISM; NERVE CELL; PAIN RECEPTOR; PATCH CLAMP TECHNIQUE; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ACETIC ACID; ACID SENSING ION CHANNELS; ACIDOSIS; ANIMALS; BEHAVIOR, ANIMAL; CELL MEMBRANE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTROGENS; FEMALE; GANGLIA, SPINAL; MALE; MAP KINASE SIGNALING SYSTEM; NEURONS; NITRILES; NOCICEPTION; NOCICEPTORS; PAIN PERCEPTION; PATCH-CLAMP TECHNIQUES; PHENOLS; PYRAZOLES; RATS; RATS, SPRAGUE-DAWLEY; SENSORY RECEPTOR CELLS; SEX FACTORS;

EID: 84948176001     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2015-1557     Document Type: Article

References (58)

1. Mogil JS. Sex differences in pain and pain inhibition: multiple explanations of a controversial phenomenon. Nat Rev Neurosci. 2012; 13(12):859-866.
2. Racine M, Tousignant-Laflamme Y, Kloda LA, Dion D, Dupuis G, Choiniere M. A systematic literature review of 10 years of research on sex/gender and experimental pain perception, part 1: are there really differences between women and men? Pain. 2012;153(3): 602-618.
3. Boerner KE, Birnie KA, Caes L, Schinkel M, Chambers CT. Sex differences in experimental pain among healthy children: a systematic review and meta-analysis. Pain. 2014;155(5):983-993.
4. Hashmi JA, Davis KD. Deconstructing sex differences in pain sensitivity. Pain. 2014;155(1):10-13.
5. Kim SJ, Calejesan AA, Li P, Wei F, Zhuo M. Sex differences in late behavioral response to subcutaneous formalin injection in mice. Brain Res. 1999;829(1-2):185-189.
6. Berkley KJ. Sex differences in pain. Behav Brain Sci. 1997;20(3): 371-380; discussion 435-513.
7. Gupta S, McCarson KE, Welch KM, Berman NE. Mechanisms of pain modulation by sex hormones in migraine. Headache. 2011; 51(6):905-922.
8. Craft RM. Modulation of pain by estrogens. Pain. 2007;132(suppl 1):S3-S12.
9. Fillingim RB, Ness TJ. Sex-related hormonal influences on pain and analgesic responses. Neurosci Biobehav Rev. 2000;24(4):485-501.
10. Amandusson A, Blomqvist A. Estrogenic influences in pain processing. Front Neuroendocrinol. 2013;34(4):329-349.
11. Allen AL, McCarson KE. Estrogen increases nociception-evoked brain-derived neurotrophic factor gene expression in the female rat. Neuroendocrinology. 2005;81(3):193-199.
12. 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(1-2):58-67.
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. Flake NM, Bonebreak DB, Gold MS. Estrogen and inflammation increase the excitability of rat temporomandibular joint afferent neurons. J Neurophysiol. 2005;93(3):1585-1597.
15. Kellenberger S, Schild L. International union of basic and clinical pharmacology. XCI. structure, function, and pharmacology of acidsensing ion channels and the epithelial Na+ channel. Pharmacol Rev. 2015;67(1):1-35.
16. Fillingim RB, King CD, Ribeiro-Dasilva MC, Rahim-Williams B, Riley JL 3rd. Sex, gender, and pain: a review of recent clinical and experimental findings. J Pain. 2009;10(5):447-485.
17. Papka RE, Storey-Workley M. Estrogen receptor-α and -β coexist in a subpopulation of sensory neurons of female rat dorsal root ganglia. Neurosci Lett. 2002;319(2):71-74.
18. Cui S, Goldstein RS. Expression of estrogen receptors in the dorsal root ganglia of the chick embryo. Brain Res. 2000;882(1-2):236-240.
19. Li L, Fan X, Warner M, Xu XJ, Gustafsson JA, Wiesenfeld-Hallin Z. Ablation of estrogen receptor α or β eliminates sex differences in mechanical pain threshold in normal and inflamed mice. Pain. 2009; 143(1-2):37-40.
20. Chaban VV, Micevych PE. Estrogen receptor-α mediates estradiol attenuation of ATP-induced Ca2+ signaling in mouse dorsal root ganglion neurons. J Neurosci Res. 2005;81(1):31-37.
21. Lu Y, Jiang Q, Yu L, et al. 17β-Estradiol rapidly attenuates P2X3 receptor-mediated peripheral pain signal transduction via ERα and GPR30. Endocrinology. 2013;154(7):2421-2433.
22. Xu S, Cheng Y, Keast JR, Osborne PB. 17β-Estradiol activates estrogen receptorβ-signalling and inhibits transient receptor potential vanilloid receptor 1 activation by capsaicin in adult rat nociceptor neurons. Endocrinology. 2008;149(11):5540-5548.
23. Deval E, Noel J, Lay N, et al. ASIC3, a sensor of acidic and primary inflammatory pain. EMBO J. 2008;27(22):3047-3055.
24. Deval E, Lingueglia E. Acid-sensing ion channels and nociception in the peripheral and central nervous systems. Neuropharmacology. 2015;94:49-57.
25. Price MP, McIlwrath SL, Xie J, et al. The DRASIC cation channel contributes to the detection of cutaneous touch and acid stimuli in mice. Neuron. 2001;32(6):1071-1083.
26. Yan J, Wei X, Bischoff C, Edelmayer RM, Dussor G. pH-evoked dural afferent signaling is mediated by ASIC3 and is sensitized by mast cell mediators. Headache. 2013;53(8):1250-1261.
27. Deval E, Noel J, Gasull X, et al. Acid-sensing ion channels in postoperative pain. J Neurosci. 2011;31(16):6059-6066.
28. Dussor G. ASICs as therapeutic targets for migraine. Neuropharmacology. 2015;94:64-71.
29. Steen KH, Issberner U, Reeh PW. Pain due to experimental acidosis in human skin: evidence for non-adapting nociceptor excitation. Neurosci Lett. 1995;199(1):29-32.
30. Steen KH, Reeh PW. Sustained graded pain and hyperalgesia from harmless experimental tissue acidosis in human skin. Neurosci Lett. 1993;154(1-2):113-116.
31. Basbaum AI, Bautista DM, Scherrer G, Julius D. Cellular and molecular mechanisms of pain. Cell. 2009;139(2):267-284.
32. Staruschenko A, Dorofeeva NA, Bolshakov KV, Stockand JD. Subunit- dependent cadmium and nickel inhibition of acid-sensing ion channels. Dev Neurobiol. 2007;67(1):97-107.
33. Steen KH, Reeh PW, Anton F, Handwerker HO. Protons selectively induce lasting excitation and sensitization to mechanical stimulation of nociceptors in rat skin, in vitro. J Neurosci. 1992;12(1):86-95.
34. Smith ML, von Hanwehr R, Siesjo BK. Changes in extra- and intracellular pH in the brain during and following ischemia in hyperglycemic and in moderately hypoglycemic rats. J Cereb Blood Flow Metab. 1986;6(5):574-583.
35. Wemmie JA, Price MP, Welsh MJ. Acid-sensing ion channels: advances, questions and therapeutic opportunities. Trends Neurosci. 2006;29(10):578-586.
36. Ikeuchi M, Kolker SJ, Burnes LA, Walder RY, Sluka KA. Role of ASIC3 in the primary and secondary hyperalgesia produced by joint inflammation in mice. Pain. 2008;137(3):662-669.
37. Noel J, Salinas M, Baron A, Diochot S, Deval E, Lingueglia E. Current perspectives on acid-sensing ion channels: new advances and therapeutic implications. Expert Rev Clin Pharmacol. 2010;3(3): 331-346.
38. Hubscher CH, Brooks DL, Johnson JR. A quantitative method for assessing stages of the rat estrous cycle. Biotech Histochem. 2005; 80(2):79-87.
39. Wood GE, Shors TJ. Stress facilitates classical conditioning in males, but impairs classical conditioning in females through activational effects of ovarian hormones. Proc Natl Acad Sci USA. 1998;95(7): 4066-4071.
40. Omori M, Yokoyama M, Matsuoka Y, et al. Effects of selective spinal nerve ligation on acetic acid-induced nociceptive responses and ASIC3 immunoreactivity in the rat dorsal root ganglion. Brain Res. 2008;1219:26-31.
41. Qiu F, Qiu CY, Cai H, et al. Oxytocin inhibits the activity of acidsensing ion channels through the vasopressin, V1A receptor in primary sensory neurons. Br J Pharmacol. 2014;171(12):3065-3076.
42. Poirot O, Berta T, Decosterd I, Kellenberger S. Distinct ASIC currents are expressed in rat putative nociceptors and are modulated by nerve injury. J Physiol. 2006;576(Pt 1):215-234.
43. Gaumond I, Arsenault P, Marchand S. The role of sex hormones on formalin-induced nociceptive responses. Brain Res. 2002;958(1): 139-145.
44. Lu YC, Chen CW, Wang SY, Wu FS. 17β-Estradiol mediates the sex difference in capsaicin-induced nociception in rats. J Pharmacol Exp Ther. 2009;331(3):1104-1110.
45. Ugawa S, Ueda T, Ishida Y, Nishigaki M, Shibata Y, Shimada S. Amiloride-blockable acid-sensing ion channels are leading acid sensors expressed in human nociceptors. J Clin Invest. 2002;110(8): 1185-1190.
46. Habelt C, Kessler F, Distler C, Kress M, Reeh PW. Interactions of inflammatory mediators and low pH not influenced by capsazepine in rat cutaneous nociceptors. Neuroreport. 2000;11(5):973-976.
47. Alvarez de la Rosa D, Zhang P, Shao D, White F, Canessa CM. Functional implications of the localization and activity of acid-sensitive channels in rat peripheral nervous system. Proc Natl Acad Sci USA. 2002;99(4):2326-2331.
48. Benson CJ, Xie J, Wemmie JA, et al. Heteromultimers of DEG/ ENaC subunits formH+-gated channels in mouse sensory neurons. Proc Natl Acad Sci USA. 2002;99(4):2338-2343.
49. Vyklicky L, Knotkova-Urbancova H. Can sensory neurones in culture serve as a model of nociception? Physiol R. 1996;45(1):1-9.
50. McRoberts JA, Li J, Ennes HS, Mayer EA. Sex-dependent differences in the activity and modulation of N-methyl-D-aspartic acid receptors in rat dorsal root ganglia neurons. Neuroscience. 2007; 148(4):1015-1020.
51. Rowan MP, Berg KA, Milam SB, et al. 17β-Estradiol rapidly enhances bradykinin signaling in primary sensory neurons in vitro and in vivo. J Pharmacol Exp Ther. 2010;335(1):190-196.
52. Xu Y, Traystman RJ, Hurn PD, Wang MM. Neurite-localized estrogen receptor-α mediates rapid signaling by estrogen. J Neurosci Res. 2003;74(1):1-11.
53. Purves-Tyson TD, Keast JR. Rapid actions of estradiol on cyclic amp response-element binding protein phosphorylation in dorsal root ganglion neurons. Neuroscience. 2004;129(3):629-637.
54. Liverman CS, Brown JW, Sandhir R, Klein RM, McCarson K, Berman NE. Oestrogen increases nociception through ERK activation in the trigeminal ganglion: evidence for a peripheral mechanism of allodynia. Cephalalgia. 2009;29(5):520-531.
55. Nag S, Mokha SS. Activation of a Gq-coupled membrane estrogen receptor rapidly attenuates α2-adrenoceptor-induced antinociception via an ERK I/II-dependent, non-genomic mechanism in the female rat. Neuroscience. 2014;267:122-134.
56. Small KM, Nag S, Mokha SS. Activation of membrane estrogen receptors attenuates opioid receptor-like1 receptor-mediated antinociception via an ERK-dependent non-genomic mechanism. Neuroscience. 2013;255:177-190.
57. Liu TT, Qu ZW, Ren C, Gan X, Qiu CY, Hu WP. Prolactin potentiates the activity of acid-sensing ion channels in female rat primary sensory neurons. Neuropharmacology. In press.
58. Wemmie JA, Taugher RJ, Kreple CJ. Acid-sensing ion channels in pain and disease. Nat Rev Neurosci. 2013;14(7):461-471.