Full Text:   <1321>

Summary:  <1092>

CLC number: R741

On-line Access: 2019-07-05

Received: 2018-11-18

Revision Accepted: 2019-03-21

Crosschecked: 2019-06-13

Cited: 0

Clicked: 2254

Citations:  Bibtex RefMan EndNote GB/T7714

-   Go to

Article info.
Open peer comments

Journal of Zhejiang University SCIENCE B 2019 Vol.20 No.8 P.628-636

http://doi.org/10.1631/jzus.B1800582


Estrogen modulation of visceral pain


Author(s):  Li-Hong Sun, Wen-Xin Zhang, Qi Xu, Hui Wu, Cui-Cui Jiao, Xin-Zhong Chen

Affiliation(s):  Department of Anesthesiology, Women’s Hospital, School of Medicine, Zhejiang University, Hangzhou 310006, China

Corresponding email(s):   chenxinz@zju.edu.cn

Key Words:  Estrogen, Visceral pain, Hyperalgesia, Ovariectomization


Li-Hong Sun, Wen-Xin Zhang, Qi Xu, Hui Wu, Cui-Cui Jiao, Xin-Zhong Chen. Estrogen modulation of visceral pain[J]. Journal of Zhejiang University Science B, 2019, 20(8): 628-636.

@article{title="Estrogen modulation of visceral pain",
author="Li-Hong Sun, Wen-Xin Zhang, Qi Xu, Hui Wu, Cui-Cui Jiao, Xin-Zhong Chen",
journal="Journal of Zhejiang University Science B",
volume="20",
number="8",
pages="628-636",
year="2019",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B1800582"
}

%0 Journal Article
%T Estrogen modulation of visceral pain
%A Li-Hong Sun
%A Wen-Xin Zhang
%A Qi Xu
%A Hui Wu
%A Cui-Cui Jiao
%A Xin-Zhong Chen
%J Journal of Zhejiang University SCIENCE B
%V 20
%N 8
%P 628-636
%@ 1673-1581
%D 2019
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B1800582

TY - JOUR
T1 - Estrogen modulation of visceral pain
A1 - Li-Hong Sun
A1 - Wen-Xin Zhang
A1 - Qi Xu
A1 - Hui Wu
A1 - Cui-Cui Jiao
A1 - Xin-Zhong Chen
J0 - Journal of Zhejiang University Science B
VL - 20
IS - 8
SP - 628
EP - 636
%@ 1673-1581
Y1 - 2019
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B1800582


Abstract: 
It is commonly accepted that females and males differ in their experience of pain. Gender differences have been found in the prevalence and severity of pain in both clinical and animal studies. Sex-related hormones are found to be involved in pain transmission and have critical effects on visceral pain sensitivity. Studies have pointed out the idea that serum estrogen is closely related to visceral nociceptive sensitivity. This review aims to summarize the literature relating to the role of estrogen in modulating visceral pain with emphasis on deciphering the potential central and peripheral mechanisms.

雌激素调节内脏痛的研究进展

概要:女性和男性的疼痛感受不同,疼痛的患病率和严重程度也存在性别差异,这在临床研究和动物实验中均得到证实.性激素参与疼痛传播并调节内脏疼痛敏感性.有研究发现血清雌激素水平与内脏疼痛敏感性密切相关.本综述旨在总结雌激素在调节内脏痛中的作用及其相关的中枢和外周机制.
关键词:雌激素;内脏痛;痛觉过敏;去卵巢

Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article

Reference

[1]Aloisi AM, Bonifazi M, 2006. Sex hormones, central nervous system and pain. Horm Behav, 50(1):1-7.

[2]Aubrun F, Salvi N, Coriat P, et al., 2005. Sex- and age-related differences in morphine requirements for postoperative pain relief. Anesthesiology, 103(1):156-160.

[3]Basbaum AI, 2009. Change is coming! Pain, 141(1-2):1.

[4]Birder LA, Nakamura Y, Kiss S, et al., 2002. Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat Neurosci, 5(9):856-860.

[5]Bokic T, Storr M, Schicho R, 2015. Potential causes and present pharmacotherapy of irritable bowel syndrome (IBS):an overview. Pharmacology, 96(1-2):76-85.

[6]Bradesi S, Golovatscka V, Ennes HS, et al., 2011. Role of astrocytes and altered regulation of spinal glutamatergic neurotransmission in stress-induced visceral hyperalgesia in rats. Am J Physiol Gastrointest Liver Physiol, 301(3):G580-G589.

[7]Campbell-Thompson M, Reyher KK, Wilkinson LB, 2001. Immunolocalization of estrogen receptor α and β in gastric epithelium and enteric neurons. J Endocrinol, 171(1):65-73.

[8]Cao DY, Ji YP, Tang B, et al., 2012. Estrogen receptor β activation is antinociceptive in a model of visceral pain in the rat. J Pain, 13(7):685-694.

[9]Cao DY, Bai G, Ji YP, et al., 2015. Epigenetic upregulation of metabotropic glutamate receptor 2 in the spinal cord attenuates oestrogen-induced visceral hypersensitivity. Gut, 64(12):1913-1920.

[10]Cepeda MS, Carr DB, 2003. Women experience more pain and require more morphine than men to achieve a similar degree of analgesia. Anesth Analg, 97(5):1464-1468.

[11]Cervero PF, Laird JMA, 1999. Visceral pain. Lancet, 353(9170):2145-2148.

[12]Chaban V, 2012. Estrogen and visceral nociception at the level of primary sensory neurons. Pain Res Treat, 2012: 960780.

[13]Chaban V, 2015. Visceral pain modulation in female primary afferent sensory neurons. Curr Trends Neurol, 9:111-114.

[14]Chaban VV, Mayer EA, Ennes HS, et al., 2003. Estradiol inhibits ATP-induced intracellular calcium concentration increase in dorsal root ganglia neurons. Neuroscience, 118(4):941-948.

[15]Chaloner A, Greenwood-van Meerveld B, 2013. Sexually dimorphic effects of unpredictable early life adversity on visceral pain behavior in a rodent model. J Pain, 14(3):270-280.

[16]Chen Y, Chen AQ, Luo XQ, et al., 2014. Hippocampal NR2B-containing NMDA receptors enhance long-term potentiation in rats with chronic visceral pain. Brain Res, 1570: 43-53.

[17]Daniel JM, Dohanich GP, 2001. Acetylcholine mediates the estrogen-induced increase in NMDA receptor binding in CA1 of the hippocampus and the associated improvement in working memory. J Neurosci, 21(17):6949-6956.

[18]Dunn PM, Zhong Y, Burnstock G, 2001. P2X receptors in peripheral neurons. Prog Neurobiol, 65(2):107-134.

[19]Eyster KM, 2016. The estrogen receptors: an overview from different perspectives. Methods Mol Biol, 1366:1-10.

[20]Gao P, Ding XW, Dong L, et al., 2017. Expression of aromatase in the rostral ventromedial medulla and its role in the regulation of visceral pain. CNS Neurosci Ther, 23(12):980-989.

[21]García-Ovejero D, Veiga S, García-Segura LM, et al., 2002. Glial expression of estrogen and androgen receptors after rat brain injury. J Comp Neurol, 450(3):256-271.

[22]Garcia Rodriguez LA, Ruigómez A, Wallander MA, et al., 2000. Detection of colorectal tumor and inflammatory bowel disease during follow-up of patients with initial diagnosis of irritable bowel syndrome. Scand J Gastroenterol, 35(3):306-311.

[23]Gaumond I, Arsenault P, Marchand S, 2002. The role of sex hormones on formalin-induced nociceptive responses. Brain Res, 958(1):139-145.

[24]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.

[25]Hardingham GE, Bading H, 2010. Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat Rev Neurosci, 11(10):682-696.

[26]Heitkemper MM, Jarrett M, 2001. Gender differences and hormonal modulation in visceral pain. Curr Pain Headache Rep, 5(1):35-43.

[27]Hubbard CS, Karpowicz JM, Furman AJ, et al., 2016. Estrogen-dependent visceral hypersensitivity following stress in rats: an fMRI study. Mol Pain, 12:1744806916654145.

[28]Ji YP, Murphy AZ, Traub RJ, 2006. Sex differences in morphine-induced analgesia of visceral pain are supraspinally and peripherally mediated. Am J Physiol Regul Integr Comp Physiol, 291(2):R307-R314.

[29]Ji YP, Murphy AZ, Traub RJ, 2007. Estrogen modulation of morphine analgesia of visceral pain in female rats is supraspinally and peripherally mediated. J Pain, 8(6):494-502.

[30]Ji YP, Tang B, Traub RJ, 2008. The visceromotor response to colorectal distention fluctuates with the estrous cycle in rats. Neuroscience, 154(4):1562-1567.

[31]Ji YP, Tang B, Traub RJ, 2011. Spinal estrogen receptor alpha mediates estradiol-induced pronociception in a visceral pain model in the rat. Pain, 152(5):1182-1191.

[32]Ji YP, Bai G, Cao DY, et al., 2015. Estradiol modulates visceral hyperalgesia by increasing thoracolumbar spinal GluN2B subunit activity in female rats. Neurogastroenterol Motil, 27(6):775-786.

[33]Kalyuzhny AE, Arvidsson U, Wu W, et al., 1996. μ-Opioid and δ-opioid receptors are expressed in brainstem antinociceptive circuits: studies using immunocytochemistry and retrograde tract-tracing. J Neurosci, 16(20):6490-6503.

[34]Labus JS, Gupta A, Coveleskie K, et al., 2013. Sex differences in emotion-related cognitive processes in irritable bowel syndrome and healthy control subjects. Pain, 154(10):2088-2099.

[35]Lefebvre RA, 1995. Nitric oxide in the peripheral nervous system. Ann Med, 27(3):379-388.

[36]Li Y, Xu J, Jiang F, et al., 2016. G protein-coupled estrogen receptor is involved in modulating colonic motor function via nitric oxide release in C57BL/6 female mice. Neurogastroenterol Motil, 28(3):432-442.

[37]Liu LM, Tsuruoka M, Maeda M, et al., 2007. Coeruleospinal inhibition of visceral nociceptive processing in the rat spinal cord. Neurosci Lett, 426(3):139-144.

[38]Magnusson JE, Martin RV, 2002. Additional evidence for the involvement of the basal ganglia in formalin-induced nociception: the role of the nucleus accumbens. Brain Res, 942(1-2):128-132.

[39]Malykhina AP, 2007. Neural mechanisms of pelvic organ cross-sensitization. Neuroscience, 149(3):660-672.

[40]Marino M, Galluzzo P, Ascenzi P, 2006. Estrogen signaling multiple pathways to impact gene transcription. Curr Genomics, 7(8):497-508.

[41]Meleine M, Matricon J, 2014. Gender-related differences in irritable bowel syndrome: potential mechanisms of sex hormones. World J Gastroenterol, 20(22):6725-6743.

[42]Micevych PE, Chaban V, Ogi J, et al., 2007. Estradiol stimulates progesterone synthesis in hypothalamic astrocyte cultures. Endocrinology, 148(2):782-789.

[43]Moriyoshi K, Masu M, Ishii T, et al., 1991. Molecular cloning and characterization of the rat NMDA receptor. Nature, 354(6348):31-37.

[44]Myers B, Schulkin J, Greenwood-van Meerveld B, 2011. Sex steroids localized to the amygdala increase pain responses to visceral stimulation in rats. J Pain, 12(4):486-494.

[45]Nilsen J, Chen SH, Brinton RD, 2002. Dual action of estrogen on glutamate-induced calcium signaling: mechanisms requiring interaction between estrogen receptors and Src/ mitogen activated protein kinase pathway. Brain Res, 930(1-2):216-234.

[46]Pan YW, Chen FG, Huang S, et al., 2016. TRPA1 and TRPM8 receptors may promote local vasodilation that aggravates oxaliplatin-induced peripheral neuropathy amenable to 17β-estradiol treatment. Curr Neurovasc Res, 13(4):309-317.

[47]Papka RE, Storey-Workley M, 2002. Estrogen receptor-α and -β coexist in a subpopulation of sensory neurons of female rat dorsal root ganglia. Neurosci Lett, 319(2):71-74.

[48]Pawlak J, Brito V, Küppers E, et al., 2005. Regulation of glutamate transporter GLAST and GLT-1 expression in astrocytes by estrogen. Mol Brain Res, 138(1):1-7.

[49]Pfaffl MW, Lange IG, Meyer HHD, 2003. The gastrointestinal tract as target of steroid hormone action: quantification of steroid receptor mRNA expression (AR, ERα, ERβ and PR) in 10 bovine gastrointestinal tract compartments by kinetic RT-PCR. J Steroid Biochem Mol Biol, 84(2-3):159-166.

[50]Qiu J, Bosch MA, Tobias SC, et al., 2003. Rapid signaling of estrogen in hypothalamic neurons involves a novel G-protein-coupled estrogen receptor that activates protein kinase C. J Neurosci, 23(29):9529-9540.

[51]Ratka A, Simpkins JW, 1991. Effects of estradiol and progesterone on the sensitivity to pain and on morphine-induced antinociception in female rats. Horm Behav, 25(2):217-228.

[52]Reinders CI, Herulf M, Ljung T, et al., 2005. Rectal mucosal nitric oxide in differentiation of inflammatory bowel disease and irritable bowel syndrome. Clin Gastroenterol Hepatol, 3(8):777-783.

[53]Riley JL III, Robinson ME, Wise EA, et al., 1998. Sex differences in the perception of noxious experimental stimuli: a meta-analysis. Pain, 74(2-3):181-187.

[54]Romeo RD, McCarthy JB, Wang A, et al., 2005. Sex differences in hippocampal estradiol-induced N-methyl-D-aspartic acid binding and ultrastructural localization of estrogen receptor-alpha. Neuroendocrinology, 81(6):391-399.

[55]Rowan MP, Berg KA, Roberts JL, et al., 2014. Activation of estrogen receptor α enhances bradykinin signaling in peripheral sensory neurons of female rats. J Pharmacol Exp Ther, 349(3):526-532.

[56]Rudolph LM, Cornil CA, Mittelman-Smith MA, et al., 2016. Actions of steroids: new neurotransmitters. J Neurosci, 36(45):11449-11458.

[57]Sandner-Kiesling A, Eisenach JC, 2002. Estrogen reduces efficacy of μ- but not κ-opioid agonist inhibition in response to uterine cervical distension. Anesthesiology, 96(2):375-380.

[58]Sherman JJ, LeResche L, 2006. Does experimental pain response vary across the menstrual cycle? A methodological review. Am J Physiol Regul Integr Comp Physiol, 291(2):R245-R256.

[59]Shibuya K, Takata N, Hojo Y, et al., 2003. Hippocampal cytochrome P450s synthesize brain neurosteroids which are paracrine neuromodulators of synaptic signal transduction. Biochim Biophys Acta Gen Subj, 1619(3):301-316.

[60]Sinchak K, Wagner EJ, 2012. Estradiol signaling in the regulation of reproduction and energy balance. Front Neuroendocrinol, 33(4):342-363.

[61]Tang B, Ji YP, Traub RJ, 2008. Estrogen alters spinal NMDA receptor activity via a PKA signaling pathway in a visceral pain model in the rat. Pain, 137(3):540-549.

[62]Ter Horst GJ, Wichmann R, Gerrits M, et al., 2009. Sex differences in stress responses: focus on ovarian hormones. Physiol Behav, 97(2):239-249.

[63]Thomas GM, Huganir RL, 2004. MAPK cascade signalling and synaptic plasticity. Nat Rev Neurosci, 5(3):173-183.

[64]Traub RJ, Cao DY, Karpowicz J, et al., 2014. A clinically relevant animal model of temporomandibular disorder and irritable bowel syndrome comorbidity. J Pain, 15(9):956-966.

[65]Vanderhorst VGJM, Terasawa E, Ralston HJ III, 2002. 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(1):27-42.

[66]Vodo S, Arcelli D, Fiorenzani P, et al., 2013. Gonadal ERα/β, AR and TRPV1 gene expression: modulation by pain and morphine treatment in male and female rats. Physiol Behav, 110-111:80-86.

[67]Zhou HY, Chen SR, Pan HL, 2011. Targeting N-methyl-D-aspartate receptors for treatment of neuropathic pain. Expert Rev Clin Pharmacol, 4(3):379-388.

[68]Zielińska M, Fichna J, Bashashati M, et al., 2017. G protein-coupled estrogen receptor and estrogen receptor ligands regulate colonic motility and visceral pain. Neurogastroenterol Motil, 29(7):e13025.

Open peer comments: Debate/Discuss/Question/Opinion

<1>

Please provide your name, email address and a comment





Journal of Zhejiang University-SCIENCE, 38 Zheda Road, Hangzhou 310027, China
Tel: +86-571-87952783; E-mail: cjzhang@zju.edu.cn
Copyright © 2000 - 2022 Journal of Zhejiang University-SCIENCE