The role of gonadal hormones in regulating opioid antinociception

References

• Mogil JS. Sex differences in pain and pain inhibition: multiple explanations of a controversial phenomenon. Nat Rev Neurosci. 2012;13(12):1–13. doi: 10.1038/nrn3360.
   Web of Science ®Google Scholar
• Fullerton EF, Doyle HH, Murphy AZ. Impact of sex on pain and opioid analgesia: a review. Curr Opin Behav Sci. 2018;23:183–190. doi: 10.1016/j.cobeha.2018.08.001.
   PubMed Web of Science ®Google Scholar
• Lamvu G, Nguyen RH, Burrows LJ, et al. The evidence-based vulvodynia assessment project. A national registry for the study of vulvodynia. J Reprod Med. 2015;60(5-6):223–235.
   PubMed Web of Science ®Google Scholar
• Hassan S, Muere A, Einstein G. Ovarian hormones and chronic pain: a comprehensive review. Pain. 2014;155(12):2448–2460. doi: 10.1016/j.pain.2014.08.027.
   PubMed Web of Science ®Google Scholar
• Nasser SA, Afify EA. Sex differences in pain and opioid mediated antinociception: modulatory role of gonadal hormones. Life Sci. 2019;237:116926. doi: 10.1016/j.lfs.2019.116926.
   PubMed Web of Science ®Google Scholar
• Cepeda MS, Carr DB. Women experience more pain and require more morphine than men to achieve a similar degree of analgesia. Anesth Analg. 2003;97(5):1464–1468. doi: 10.1213/01.ANE.0000080153.36643.83.
   PubMed Web of Science ®Google Scholar
• Doyle HH, Eidson LN, Sinkiewicz DM, et al. Sex differences in microglia activity within the periaqueductal gray of the rat: a potential mechanism driving the dimorphic effects of morphine. J Neurosci. 2017;37(12):3202–3214. doi: 10.1523/JNEUROSCI.2906-16.2017.
   PubMed Web of Science ®Google Scholar
• Posillico CK, Terasaki LS, Bilbo SD, et al. Examination of sex and minocycline treatment on acute morphine-induced analgesia and inflammatory gene expression along the pain pathway in Sprague-Dawley rats. Biol Sex Differ. 2015;6(1):33. doi: 10.1186/s13293-015-0049-3.
   PubMedGoogle Scholar
• Racine M, Tousignant-Laflamme Y, Kloda LA, et al. A systematic literature review of 10 years of research on sex/gender and pain perception - part 2: do biopsychosocial factors alter pain sensitivity differently in women and men? Pain. 2012;153(3):619–635. doi: 10.1016/j.pain.2011.11.026.
   PubMed Web of Science ®Google Scholar
• Guajardo HM, Valentino RJ. Sex differences in mu-opioid regulation of coerulear-cortical transmission. Neurosci Lett. 2021;746:135651. doi: 10.1016/j.neulet.2021.135651.
   PubMed Web of Science ®Google Scholar
• Marrocco J, McEwen BS. Sex in the brain: hormones and sex differences. Dialogues Clin Neurosci. 2016;18(4):373–383. doi: 10.31887/DCNS.2016.18.4/jmarrocco.
   PubMed Web of Science ®Google Scholar
• ThyagaRajan S, Hima L, Pratap UP, et al. Estrogen-induced neuroimmunomodulation as facilitator of and barrier to reproductive aging in brain and lymphoid organs. J Chem Neuroanat. 2019;95:6–12. doi: 10.1016/j.jchemneu.2018.02.008.
   PubMed Web of Science ®Google Scholar
• Toffoletto S, Lanzenberger R, Gingnell M, et al. Emotional and cognitive functional imaging of estrogen and progesterone effects in the female human brain: a systematic review. Psychoneuroendocrinology. 2014;50:28–52. doi: 10.1016/j.psyneuen.2014.07.025.
   PubMed Web of Science ®Google Scholar
• Messinis IE, Messini CI, Dafopoulos K. Novel aspects of the endocrinology of the menstrual cycle. Reprod Biomed Online. 2014;28(6):714–722. doi: 10.1016/j.rbmo.2014.02.003.
   PubMed Web of Science ®Google Scholar
• Knouse MC, Briand LA. Behavioral sex differences in cocaine and opioid use disorders: the role of gonadal hormones. Neurosci Biobehav Rev. 2021;128:358–366. doi: 10.1016/j.neubiorev.2021.06.038.
   PubMed Web of Science ®Google Scholar
• Lacy RT, Austin BP, Strickland JC. The influence of sex and estrous cyclicity on cocaine and remifentanil demand in rats. Addict Biol. 2020;25(1):e12716. doi: 10.1111/adb.12716.
   PubMed Web of Science ®Google Scholar
• Miniksar OH, Onat T, Gocmen AY, et al. Serum levels of mu-opioid receptor according to menstrual cycle phases are associated with postoperative pain and opioid consumption in laparoscopic gynecological surgeries: a prospective observational study. Ir J Med Sci. 2022;192(4):1847–1854. doi: 10.1007/s11845-022-03146-z.
   PubMed Web of Science ®Google Scholar
• Ribeiro-Dasilva MC, Shinal RM, Glover T, 3rd, et al. Evaluation of menstrual cycle effects on morphine and pentazocine analgesia. Pain. 2011;152(3):614–622. doi: 10.1016/j.pain.2010.11.033.
   PubMed Web of Science ®Google Scholar
• Ahmed A, Khan F, Ali M, et al. Effect of the menstrual cycle phase on post-operative pain perception and analgesic requirements. Acta Anaesthesiol Scand. 2012;56(5):629–635. doi: 10.1111/j.1399-6576.2012.02661.x.
   PubMed Web of Science ®Google Scholar
• Raheem OA, Patel SH, Sisul D, et al. The role of testosterone supplemental therapy in opioid-induced hypogonadism: a retrospective pilot analysis. Am J Mens Health. 2017;11(4):1208–1213. doi: 10.1177/1557988316672396.
   PubMed Web of Science ®Google Scholar
• Kumar A, Liu NJ, Madia PA, et al. Contribution of endogenous spinal endomorphin 2 to intrathecal opioid antinociception in rats is agonist dependent and sexually dimorphic. J Pain. 2015;16(11):1200–1210. doi: 10.1016/j.jpain.2015.08.003.
   PubMed Web of Science ®Google Scholar
• Huang G, Travison T, Maggio M, et al. Effects of testosterone replacement on metabolic and inflammatory markers in men with opioid-induced androgen deficiency. Clin Endocrinol (Oxf). 2016;85(2):232–238. doi: 10.1111/cen.13049.
   PubMed Web of Science ®Google Scholar
• Peckham EM, Graves SM, Jutkiewicz E, et al. Role of gonadal hormones on mu-opioid-stimulated [(3)(5)S]GTPgammaS binding and morphine-mediated antinociception in male and female Sprague-Dawley rats. Psychopharmacology (Berl). 2011;218(3):483–492.) doi: 10.1007/s00213-011-2335-z.
   PubMed Web of Science ®Google Scholar
• Sharp JL, Pearson T, Smith MA. Sex differences in opioid receptor mediated effects: role of androgens. Neurosci Biobehav Rev. 2022;134:104522. doi: 10.1016/j.neubiorev.2022.104522.
   PubMed Web of Science ®Google Scholar
• Fullerton EF, Rubaharan M, Karom MC, et al. Advanced age attenuates the antihyperalgesic effect of morphine and decreases mu-opioid receptor expression and binding in the rat midbrain periaqueductal gray in male and female rats. Neurobiol Aging. 2021;98:78–87. doi: 10.1016/j.neurobiolaging.2020.10.020.
   PubMed Web of Science ®Google Scholar
• Lamy J, Liere P, Pianos A, et al. Steroid hormones in bovine oviductal fluid during the estrous cycle. Theriogenology. 2016;86(6):1409–1420. doi: 10.1016/j.theriogenology.2016.04.086.
   PubMed Web of Science ®Google Scholar
• 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(3):285–302. doi: 10.1016/s0304-3959(02)00457-8.
   PubMed Web of Science ®Google Scholar
• Terner JM, Lomas LM, Picker MJ. Influence of estrous cycle and gonadal hormone depletion on nociception and opioid antinociception in female rats of four strains. J Pain. 2005;6(6):372–383. doi: 10.1016/j.jpain.2005.01.354.
   PubMed Web of Science ®Google Scholar
• Arguelles N, Miksys S, Tyndale RF. Sex and estrous cycle differences in analgesia and brain oxycodone levels. Mol Neurobiol. 2021;58(12):6540–6551. doi: 10.1007/s12035-021-02560-1.
   PubMed Web of Science ®Google Scholar
• Kosiorek-Witek A, Makulska-Nowak HE. Morphine analgesia modification in normotensive and hypertensive female rats after repeated fluoxetine administration. Basic Clin Pharmacol Toxicol. 2016;118(1):45–52. doi: 10.1111/bcpt.12438.
   PubMed Web of Science ®Google Scholar
• Loyd DR, Wang X, Murphy AZ. Sex differences in micro-opioid receptor expression in the rat midbrain periaqueductal gray are essential for eliciting sex differences in morphine analgesia. J Neurosci. 2008;28(52):14007–14017. doi: 10.1523/JNEUROSCI.4123-08.2008.
   PubMed Web of Science ®Google Scholar
• Liu NJ, Gintzler AR. Spinal endomorphin 2 antinociception and the mechanisms that produce it are both sex- and stage of estrus cycle-dependent in rats. J Pain. 2013;14(11):1522–1530. doi: 10.1016/j.jpain.2013.09.002.
   PubMed Web of Science ®Google Scholar
• Escudero-Lara A, Cabañero D, Maldonado R. Kappa opioid receptor modulation of endometriosis pain in mice. Neuropharmacology. 2021;195:108677. doi: 10.1016/j.neuropharm.2021.108677.
   PubMed Web of Science ®Google Scholar
• Zhang W, Wu H, Xu Q, et al. Estrogen modulation of pain perception with a novel 17beta-estradiol pretreatment regime in ovariectomized rats. Biol Sex Differ. 2020;11(1):2. doi: 10.1186/s13293-019-0271-5.
   PubMed Web of Science ®Google Scholar
• Bai X, Zhang X, Li Y, et al. Sex differences in peripheral mu-opioid receptor mediated analgesia in rat orofacial persistent pain model. PLoS One. 2015;10(3):e0122924. doi: 10.1371/journal.pone.0122924.
   PubMed Web of Science ®Google Scholar
• Abraham AD, Schattauer SS, Reichard KL, et al. Estrogen regulation of GRK2 inactivates kappa opioid receptor signaling mediating analgesia, but not aversion. J Neurosci. 2018;38(37):8031–8043. doi: 10.1523/JNEUROSCI.0653-18.2018.
   PubMed Web of Science ®Google Scholar
• Cicero TJ, Nock B, O’Connor L, et al. Role of steroids in sex differences in morphine-induced analgesia: activational and organizational effects. J Pharmacol Exp Ther. 2002;300(2):695–701. doi: 10.1124/jpet.300.2.695.
   PubMed Web of Science ®Google Scholar
• Sandner-Kiesling A, Eisenach JC. Estrogen reduces efficacy of mu- but not kappa-opioid agonist inhibition in response to uterine cervical distension. Anesthesiology. 2002;96(2):375–379. doi: 10.1097/00000542-200202000-00024.
   PubMed Web of Science ®Google Scholar
• Mannino CA, South SM, Inturrisi CE, et al. Pharmacokinetics and effects of 17beta-estradiol and progesterone implants in ovariectomized rats. J Pain. 2005;6(12):809–816. doi: 10.1016/j.jpain.2005.07.007.
   PubMed Web of Science ®Google Scholar
• Verdi J, Ahmadiani A. Finasteride, a 5alpha-reductase inhibitor, potentiates antinociceptive effects of morphine, prevents the development of morphine tolerance and attenuates abstinence behavior in the rat. Horm Behav. 2007;51(5):605–610. doi: 10.1016/j.yhbeh.2007.02.008.
   PubMed Web of Science ®Google Scholar
• Stoffel EC, Ulibarri CM, Folk JE, et al. Gonadal hormone modulation of mu, kappa, and Delta opioid antinociception in male and female rats. J Pain. 2005;6(4):261–274. doi: 10.1016/j.jpain.2004.12.006.
   PubMed Web of Science ®Google Scholar
• Kadokawa H. Discovery of new receptors regulating luteinizing hormone and follicle-stimulating hormone secretion by bovine gonadotrophs to explore a new paradigm for mechanisms regulating reproduction. J Reprod Dev. 2020;66(4):291–297. doi: 10.1262/jrd.2020-012.
   PubMed Web of Science ®Google Scholar
• Cheng H, Huang H, Guo Z, et al. Role of prostaglandin E2 in tissue repair and regeneration. Theranostics. 2021;11(18):8836–8854. doi: 10.7150/thno.63396.
   PubMed Web of Science ®Google Scholar
• Smith MA, Armas SP, Schmidt KT. Modulation of morphine physical dependence and discriminative stimulus effects by ovarian hormones: role of estradiol. Pharmacol Biochem Behav. 2022;218:173431. doi: 10.1016/j.pbb.2022.173431.
   PubMed Web of Science ®Google Scholar
• Liu NJ, von Gizycki H, Gintzler AR. Sexually dimorphic recruitment of spinal opioid analgesic pathways by the spinal application of morphine. J Pharmacol Exp Ther. 2007;322(2):654–660. doi: 10.1124/jpet.107.123620.
   PubMed Web of Science ®Google Scholar
• Rasakham K, Liu-Chen LY. Sex differences in kappa opioid pharmacology. Life Sci. 2011;88(1-2):2–16. doi: 10.1016/j.lfs.2010.10.007.
   PubMed Web of Science ®Google Scholar
• Chakrabarti S, Liu NJ, Gintzler AR. Formation of mu-/kappa-opioid receptor heterodimer is sex-dependent and mediates female-specific opioid analgesia. Proc Natl Acad Sci U S A. 2010;107(46):20115–20119. doi: 10.1073/pnas.1009923107.
   PubMed Web of Science ®Google Scholar
• Liu NJ, Chakrabarti S, Schnell S, et al. Spinal synthesis of estrogen and concomitant signaling by membrane estrogen receptors regulate spinal kappa- and mu-opioid receptor heterodimerization and female-specific spinal morphine antinociception. J Neurosci. 2011;31(33):11836–11845. doi: 10.1523/JNEUROSCI.1901-11.2011.
   PubMed Web of Science ®Google Scholar
• Lawson KP, Nag S, Thompson AD, et al. Sex-specificity and estrogen-dependence of kappa opioid receptor-mediated antinociception and antihyperalgesia. Pain. 2010;151(3):806–815. doi: 10.1016/j.pain.2010.09.018.
   PubMed Web of Science ®Google Scholar
• Liu NJ, Murugaiyan V, Storman EM, et al. Estrogens synthesized and acting within a spinal oligomer suppress spinal endomorphin 2 antinociception: ebb and flow over the rat reproductive cycle. Pain. 2017;158(10):1903–1914. doi: 10.1097/j.pain.0000000000000991.
   PubMed Web of Science ®Google Scholar
• Liu NJ, Murugaiyan V, Storman EM, et al. Plasticity of signaling by spinal estrogen receptor alpha, kappa-Opioid receptor, and metabotropic glutamate receptors over the rat reproductive cycle regulates spinal endomorphin 2 antinociception: relevance of endogenous-biased agonism. J Neurosci. 2017;37(46):11181–11191. doi: 10.1523/JNEUROSCI.1927-17.2017.
   PubMed Web of Science ®Google Scholar
• Claiborne J, Nag S, Mokha SS. Activation of opioid receptor like-1 receptor in the spinal cord produces sex-specific antinociception in the rat: estrogen attenuates antinociception in the female, whereas testosterone is required for the expression of antinociception in the male. J Neurosci. 2006;26(50):13048–13053. doi: 10.1523/JNEUROSCI.4783-06.2006.
   PubMed Web of Science ®Google Scholar
• Jeremic D, Sanchez-Rodriguez I, Jimenez-Diaz L, et al. Therapeutic potential of targeting G protein-gated inwardly rectifying potassium (GIRK) channels in the Central nervous system. Pharmacol Ther. 2021;223:107808. doi: 10.1016/j.pharmthera.2021.107808.
   PubMed Web of Science ®Google Scholar
• 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. doi: 10.1016/j.neuroscience.2013.10.034.
   PubMed Web of Science ®Google Scholar
• Wagner EJ, Ronnekleiv OK, Kelly MJ. Protein kinase a maintains cellular tolerance to mu opioid receptor agonists in hypothalamic neurosecretory cells with chronic morphine treatment: convergence on a common pathway with estrogen in modulating mu opioid receptor/effector coupling. The Journal of Pharmacology and Experimental Therapeutics. 1998;285(3):1266–1273.
   PubMed Web of Science ®Google Scholar
• Kelly MJ, Lagrange AH, Wagner EJ, et al. Rapid effects of estrogen to modulate G protein-coupled receptors via activation of protein kinase a and protein kinase C pathways. Steroids. 1999;64(1-2):64–75. doi: 10.1016/s0039-128x(98)00095-6.
   PubMed Web of Science ®Google Scholar
• Stincic TL, Rønnekleiv OK, Kelly MJ. Diverse actions of estradiol on anorexigenic and orexigenic hypothalamic arcuate neurons. Horm Behav. 2018;104:146–155. doi: 10.1016/j.yhbeh.2018.04.001.
   PubMed Web of Science ®Google Scholar
• Malyala A, Kelly MJ, Rønnekleiv OK. Estrogen modulation of hypothalamic neurons: activation of multiple signaling pathways and gene expression changes. Steroids. 2005;70(5-7):397–406. doi: 10.1016/j.steroids.2005.03.004.
   PubMed Web of Science ®Google Scholar
• Ding X, Gao T, Gao P, et al. Activation of the G protein-coupled estrogen receptor elicits store calcium release and phosphorylation of the Mu-opioid receptors in the human neuroblastoma SH-SY5Y cells. Front Neurosci. 2019;13:1351. doi: 10.3389/fnins.2019.01351.
   PubMed Web of Science ®Google Scholar
• Brito RG, Rasmussen LA, Sluka KA. Regular physical activity prevents development of chronic muscle pain through modulation of supraspinal opioid and serotonergic mechanisms. Pain Rep. 2017;2(5):e618. doi: 10.1097/PR9.0000000000000618.
   PubMedGoogle Scholar
• Wang J, Zhang H, Feng YP, et al. Morphological evidence for a neurotensinergic periaqueductal gray-rostral ventromedial medulla-spinal dorsal horn descending pathway in rat. Front Neuroanat. 2014;8:112. doi: 10.3389/fnana.2014.00112.
   PubMed Web of Science ®Google Scholar
• Lau BK, Vaughan CW. Descending modulation of pain: the GABA disinhibition hypothesis of analgesia. Curr Opin Neurobiol. 2014;29:159–164. doi: 10.1016/j.conb.2014.07.010.
   PubMed Web of Science ®Google Scholar
• Averitt DL, Eidson LN, Doyle HH, et al. Neuronal and glial factors contributing to sex differences in opioid modulation of pain. Neuropsychopharmacology. 2019;44(1):155–165. doi: 10.1038/s41386-018-0127-4.
   PubMed Web of Science ®Google Scholar
• Jiao Y, Gao P, Dong L, et al. Molecular identification of bulbospinal on neurons by GPER which drives pain and morphine tolerance. J Clin Invest. 2022;133(1):e154588. doi: 10.1172/JCI154588.
   Web of Science ®Google Scholar
• Flores CA, Shughrue P, Petersen SL, et al. Sex-related differences in the distribution of opioid receptor-like 1 receptor mRNA and colocalization with estrogen receptor mRNA in neurons of the spinal trigeminal nucleus caudalis in the rat. Neuroscience. 2003;118(3):769–778. doi: 10.1016/s0306-4522(02)01000-x.
   PubMed Web of Science ®Google Scholar
• Flores CA, Wang XM, Zhang KM, et al. Orphanin FQ produces gender-specific modulation of trigeminal nociception: behavioral and electrophysiological observations. Neuroscience. 2001;105(2):489–498. doi: 10.1016/s0306-4522(01)00179-8.
   PubMed Web of Science ®Google Scholar
• Sun LH, Xu Q, Jin L, et al. The involvement of CaV1.2 in estrogenic modulation of morphine antinociception in rats under uterine cervix pain. Pain Physician. 2022;25(8):E1239–E1248.
   PubMed Web of Science ®Google Scholar
• Gerald T, Raj G. Testosterone and the androgen receptor. Urol Clin North Am. 2022;49(4):603–614. doi: 10.1016/j.ucl.2022.07.004.
   PubMed Web of Science ®Google Scholar
• Kelava I, Chiaradia I, Pellegrini L, et al. Androgens increase excitatory neurogenic potential in human brain organoids. Nature. 2022;602(7895):112–116. doi: 10.1038/s41586-021-04330-4.
   PubMed Web of Science ®Google Scholar
• Cataldo G, Bernal SY, Rozengurtel S, et al. Neonatal and adult gonadal hormone manipulations enhance morphine analgesia elicited from the ventrolateral periaqueductal gray in female rats. Int J Neurosci. 2010;120(4):265–272. doi: 10.3109/00207451003662120.
   PubMed Web of Science ®Google Scholar
• Borzan J, Fuchs PN. Organizational and activational effects of testosterone on carrageenan-induced inflammatory pain and morphine analgesia. Neuroscience. 2006;143(3):885–893. doi: 10.1016/j.neuroscience.2006.08.034.
   PubMed Web of Science ®Google Scholar
• Zhang X, Zhang Y, Asgar J, et al. Sex differences in mu-opioid receptor expression in trigeminal ganglia under a myositis condition in rats. Eur J Pain. 2014;18(2):151–161. doi: 10.1002/j.1532-2149.2013.00352.x.
   PubMed Web of Science ®Google Scholar
• Lee KS, Zhang Y, Asgar J, et al. Androgen receptor transcriptionally regulates mu-opioid receptor expression in rat trigeminal ganglia. Neuroscience. 2016;331:52–61. doi: 10.1016/j.neuroscience.2016.06.023.
   PubMed Web of Science ®Google Scholar
• Macedo CG, Fanton LE, Fischer L, et al. Coactivation of mu- and kappa-Opioid receptors may mediate the protective effect of testosterone on the development of temporomandibular joint nociception in male rats. J Oral Facial Pain Headache. 2016;30(1):61–67. doi: 10.11607/ofph.1298.
   PubMed Web of Science ®Google Scholar
• Bai X, Wang C, Zhang X, et al. The role of testosterone in mu-opioid receptor expression in the trigeminal ganglia of opioid-tolerant rats. Neurosci Lett. 2020;723:134868. doi: 10.1016/j.neulet.2020.134868.
   PubMed Web of Science ®Google Scholar
• Tripp KM, Dubois M, Delahaut P, et al. Detection and identification of plasma progesterone metabolites in the female Florida manatee (trichechus manatus latirostris) using GC/MS/MS. Theriogenology. 2009;72(3):365–371. doi: 10.1016/j.theriogenology.2009.03.004.
   PubMed Web of Science ®Google Scholar
• Dobrzyn K, Kowalik MK. [Molecular mechanism of progesterone action in the female reproductive system. ]Postepy Biochemii. 2022;68(3):336–343.
   PubMedGoogle Scholar
• Chou CH, Chen MJ. The effect of steroid hormones on ovarian follicle development. Vitamins and Hormones. 2018;107:155–175.
   PubMed Web of Science ®Google Scholar
• Ilicic M, Zakar T, Paul JW. The regulation of uterine function during parturition: an update and recent advances. Reprod Sci. 2020;27(1):3–28. doi: 10.1007/s43032-019-00001-y.
   PubMed Web of Science ®Google Scholar
• Block HS, Biller J. Neurology of pregnancy. Handbook of Clinical Neurology. 2014;121:1595–1622.
   PubMedGoogle Scholar
• Rosen SF, Ham B, Drouin S, et al. T-cell mediation of pregnancy analgesia affecting chronic pain in mice. J Neurosci. 2017;37(41):9819–9827. doi: 10.1523/JNEUROSCI.2053-17.2017.
   PubMed Web of Science ®Google Scholar
• Sternberg WF, Chesler EJ, Wilson SG, et al. Acute progesterone can recruit sex-specific neurochemical mechanisms mediating swim stress-induced and kappa-opioid analgesia in mice. Horm Behav. 2004;46(4):467–473. doi: 10.1016/j.yhbeh.2004.05.007.
   PubMed Web of Science ®Google Scholar
• Liu NJ, Gintzler AR. Prolonged ovarian sex steroid treatment of male rats produces antinociception: identification of sex-based divergent analgesic mechanisms. Pain. 2000;85(1-2):273–281. doi: 10.1016/s0304-3959(99)00278-x.
   PubMed Web of Science ®Google Scholar
• Priyanto B, Rosyidi RM, Islam AA, et al. The effect of progesteron for expression Delta (Delta) opioid receptor spinal cord through peripheral nerve injury. Ann Med Surg (Lond). 2022;75:103376. doi: 10.1016/j.amsu.2022.103376.
   PubMed Web of Science ®Google Scholar
• Coronel MF, Labombarda F, Villar MJ, et al. Progesterone prevents allodynia after experimental spinal cord injury. J Pain. 2011;12(1):71–83. doi: 10.1016/j.jpain.2010.04.013.
   PubMed Web of Science ®Google Scholar
• Labombarda F, González S, Lima A, et al. Progesterone attenuates astro- and microgliosis and enhances oligodendrocyte differentiation following spinal cord injury. Exp Neurol. 2011;231(1):135–146. doi: 10.1016/j.expneurol.2011.06.001.
   PubMed Web of Science ®Google Scholar
• Bartley EJ, Fillingim RB. Sex differences in pain: a brief review of clinical and experimental findings. Br J Anaesth. 2013;111(1):52–58. doi: 10.1093/bja/aet127.
   PubMed Web of Science ®Google Scholar