How Sex Hormones Affect Migraine: An Interdisciplinary Preclinical Research Panel Review
Abstract
:1. Introduction
2. Sex Hormone Fluctuation as a Trigger of Migraine
3. Which Sex Hormones Should Be the Target?
3.1. Estrogen
3.2. Progesterone
3.3. Testosterone
3.4. Oxytocin
3.5. Vasopressin
3.6. Prolactin
4. Limitations of Current Methods
5. Conclusions and Future Directions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Burch, R.C.; Buse, D.C.; Lipton, R.B. Migraine: Epidemiology, Burden, and Comorbidity. Neurol. Clin. 2019, 37, 631–649. [Google Scholar] [CrossRef] [PubMed]
- Tsai, C.K.; Tsai, C.L.; Lin, G.Y.; Yang, F.C.; Wang, S.J. Sex Differences in Chronic Migraine: Focusing on Clinical Features, Pathophysiology, and Treatments. Curr. Pain Headache Rep. 2022, 26, 347–355. [Google Scholar] [CrossRef] [PubMed]
- Vos, T.; Abajobir, A.A.; Abate, K.H.; Abbafati, C.; Abbas, K.M.; Abd-Allah, F.; Abdulkader, R.S.; Abdulle, A.M.; Abebo, T.A.; Abera, S.F.; et al. Global, regional, and national incidence, prevalence, and years lived with disability for 328 diseases and injuries for 195 countries, 1990–2016: A systematic analysis for the Global Burden of Disease Study 2016. Lancet 2017, 390, 1211–1259. [Google Scholar] [CrossRef] [PubMed]
- Szperka, C. Headache in Children and Adolescents. Continuum 2021, 27, 703–731. [Google Scholar] [CrossRef] [PubMed]
- Tonini, M.C. Gender differences in migraine. Neurol. Sci. 2018, 39, 77–78. [Google Scholar] [CrossRef] [PubMed]
- Vetvik, K.G.; MacGregor, E.A. Sex differences in the epidemiology, clinical features, and pathophysiology of migraine. Lancet Neurol. 2017, 16, 76–87. [Google Scholar] [CrossRef]
- MacGregor, E.A.; Frith, A.; Ellis, J.; Aspinall, L.; Hackshaw, A. Incidence of migraine relative to menstrual cycle phases of rising and falling estrogen. Neurology 2006, 67, 2154–2158. [Google Scholar] [CrossRef] [PubMed]
- Chalmer, M.A.; Kogelman, L.J.A.; Ullum, H.; Sørensen, E.; Didriksen, M.; Mikkelsen, S.; Dinh, K.M.; Brodersen, T.; Nielsen, K.R.; Bruun, M.T.; et al. Population-Based Characterization of Menstrual Migraine and Proposed Diagnostic Criteria. JAMA Netw. Open 2023, 6, e2313235. [Google Scholar] [CrossRef]
- Pavlović, J.M.; Allshouse, A.A.; Santoro, N.F.; Crawford, S.L.; Thurston, R.C.; Neal-Perry, G.S.; Lipton, R.B.; Derby, C.A. Sex hormones in women with and without migraine: Evidence of migraine-specific hormone profiles. Neurology 2016, 87, 49–56. [Google Scholar] [CrossRef]
- Calhoun, A.H.; Batur, P. Combined hormonal contraceptives and migraine: An update on the evidence. Clevel. Clin. J. Med. 2017, 84, 631–638. [Google Scholar] [CrossRef]
- Warhurst, S.; Rofe, C.J.; Brew, B.J.; Bateson, D.; McGeechan, K.; Merki-Feld, G.S.; Garrick, R.; Tomlinson, S.E. Effectiveness of the progestin-only pill for migraine treatment in women: A systematic review and meta-analysis. Cephalalgia 2018, 38, 754–764. [Google Scholar] [CrossRef] [PubMed]
- Lyall, M.; de Oliveira, B.R.; Mody, S.K. Considerations for Contraceptive Use Among Patients with Migraines. Curr. Obstet. Gynecol. Rep. 2023, 12, 57–63. [Google Scholar] [CrossRef]
- MacGregor, E.A. Migraine, menopause and hormone replacement therapy. Post Reprod. Health 2018, 24, 11–18. [Google Scholar] [CrossRef]
- Aubé, M. Migraine in pregnancy. Neurology 1999, 53 (Suppl. S1), S26–S28. [Google Scholar]
- Ertresvåg, J.M.; Zwart, J.A.; Helde, G.; Johnsen, H.J.; Bovim, G. Headache and transient focal neurological symptoms during pregnancy, a prospective cohort. Acta Neurol. Scand. 2005, 111, 233–237. [Google Scholar] [CrossRef]
- Kvisvik, E.V.; Stovner, L.J.; Helde, G.; Bovim, G.; Linde, M. Headache and migraine during pregnancy and puerperium: The MIGRA-study. J. Headache Pain 2011, 12, 443–451. [Google Scholar] [CrossRef]
- Goadsby, P.J.; Goldberg, J.; Silberstein, S.D. Migraine in pregnancy. BMJ 2008, 336, 1502–1504. [Google Scholar] [CrossRef] [PubMed]
- Robbins, M.S.; Farmakidis, C.; Dayal, A.K.; Lipton, R.B. Acute headache diagnosis in pregnant women: A hospital-based study. Neurology 2015, 85, 1024–1030. [Google Scholar] [CrossRef]
- Sances, G.; Granella, F.; Nappi, R.E.; Fignon, A.; Ghiotto, N.; Polatti, F.; Nappi, G. Course of migraine during pregnancy and postpartum: A prospective study. Cephalalgia 2003, 23, 197–205. [Google Scholar] [CrossRef]
- Wells, R.E.; Turner, D.P.; Lee, M.; Bishop, L.; Strauss, L. Managing Migraine during Pregnancy and Lactation. Curr. Neurol. Neurosci. Rep. 2016, 16, 40. [Google Scholar] [CrossRef]
- Mueller, L. Predictability of exogenous hormone effect on subgroups of migraineurs. Headache 2000, 40, 189–193. [Google Scholar] [CrossRef] [PubMed]
- Hodson, J.; Thompson, J.; Al-Azzawi, F. Headache at menopause and in hormone replacement therapy users. Climacteric J. Int. Menopause Soc. 2000, 3, 119–124. [Google Scholar] [CrossRef] [PubMed]
- Ibrahimi, K.; Couturier, E.G.M.; MaassenVanDenBrink, A. Migraine and perimenopause. Maturitas 2014, 78, 277–280. [Google Scholar] [CrossRef] [PubMed]
- Granella, F.; Sances, G.; Zanferrari, C.; Costa, A.; Martignoni, E.; Manzoni, G.C. Migraine without aura and reproductive life events: A clinical epidemiological study in 1300 women. Headache 1993, 33, 385–389. [Google Scholar] [CrossRef] [PubMed]
- Cupini, L.M.; Matteis, M.; Troisi, E.; Calabresi, P.; Bernardi, G.; Silvestrini, M. Sex-hormone-related events in migrainous females. A clinical comparative study between migraine with aura and migraine without aura. Cephalalgia 1995, 15, 140–144. [Google Scholar] [CrossRef] [PubMed]
- Wang, S.J.; Fuh, J.L.; Lu, S.R.; Juang, K.D.; Wang, P.H. Migraine prevalence during menopausal transition. Headache 2003, 43, 470–478. [Google Scholar] [CrossRef] [PubMed]
- Freeman, E.W.; Sammel, M.D.; Lin, H.; Gracia, C.R.; Kapoor, S. Symptoms in the menopausal transition: Hormone and behavioral correlates. Obstet. Gynecol. 2008, 111, 127–136. [Google Scholar] [CrossRef]
- Mattsson, P. Hormonal factors in migraine: A population-based study of women aged 40 to 74 years. Headache 2003, 43, 27–35. [Google Scholar] [CrossRef]
- Park, J.H.; Viirre, E. Vestibular migraine may be an important cause of dizziness/vertigo in perimenopausal period. Med. Hypotheses 2010, 75, 409–414. [Google Scholar] [CrossRef]
- Pavlović, J.M. Evaluation and management of migraine in midlife women. Menopause 2018, 25, 927–929. [Google Scholar] [CrossRef]
- Kaiser, H.J.; Meienberg, O. Deterioration or onset of migraine under oestrogen replacement therapy in the menopause. J. Neurol. 1993, 240, 195–196. [Google Scholar] [CrossRef]
- Sacco, S.; Ricci, S.; Degan, D.; Carolei, A. Migraine in women: The role of hormones and their impact on vascular diseases. J. Headache Pain 2012, 13, 177–189. [Google Scholar] [CrossRef]
- Burke, B.E.; Olson, R.D.; Cusack, B.J. Randomized, controlled trial of phytoestrogen in the prophylactic treatment of menstrual migraine. Biomed. Pharmacother. 2002, 56, 283–288. [Google Scholar] [CrossRef] [PubMed]
- Patisaul, H.B.; Jefferson, W. The pros and cons of phytoestrogens. Front. Neuroendocrinol. 2010, 31, 400–419. [Google Scholar] [CrossRef]
- Chen, M.N.; Lin, C.C.; Liu, C.F. Efficacy of phytoestrogens for menopausal symptoms: A meta-analysis and systematic review. Climacteric 2015, 18, 260–269. [Google Scholar] [CrossRef]
- Rietjens, I.M.C.M.; Louisse, J.; Beekmann, K. The potential health effects of dietary phytoestrogens. Br. J. Pharmacol. 2017, 174, 1263–1280. [Google Scholar] [CrossRef]
- Sarajari, S.; Oblinger, M.M. Estrogen Effects on Pain Sensitivity and Neuropeptide Expression in Rat Sensory Neurons. Exp. Neurol. 2010, 224, 163–169. [Google Scholar] [CrossRef] [PubMed]
- Welch, K.M.A.; Brandes, J.L.; Berman, N.E.J. Mismatch in how oestrogen modulates molecular and neuronal function may explain menstrual migraine. Neurol. Sci. 2006, 27 (Suppl. S2), S190–S192. [Google Scholar] [CrossRef] [PubMed]
- Wattiez, A.S.; Sowers, L.P.; Russo, A.F. Calcitonin gene-related peptide (CGRP): Role in migraine pathophysiology and therapeutic targeting. Expert Opin. Ther. Targets 2020, 24, 91–100. [Google Scholar] [CrossRef] [PubMed]
- Puri, V.; Cui, L.; Liverman, C.S.; Roby, K.F.; Klein, R.M.; Welch, K.M.A.; Berman, N.E.J. Ovarian steroids regulate neuropeptides in the trigeminal ganglion. Neuropeptides 2005, 39, 409–417. [Google Scholar] [CrossRef]
- Rettberg, J.R.; Yao, J.; Brinton, R.D. Estrogen: A master regulator of bioenergetic systems in the brain and body. Front. Neuroendocrinol. 2014, 35, 8–30. [Google Scholar] [CrossRef] [PubMed]
- Kudo, C.; Harriott, A.M.; Moskowitz, M.A.; Waeber, C.; Ayata, C. Estrogen modulation of cortical spreading depression. J. Headache Pain 2023, 24, 62. [Google Scholar] [CrossRef] [PubMed]
- Chen, Q.; Zhang, W.; Sadana, N.; Chen, X. Estrogen receptors in pain modulation: Cellular signaling. Biol. Sex Differ. 2021, 12, 22. [Google Scholar] [CrossRef] [PubMed]
- Kelly, M.J.; Rønnekleiv, O.K. Minireview: Neural Signaling of Estradiol in the Hypothalamus. Mol. Endocrinol. 2015, 29, 645–657. [Google Scholar] [CrossRef]
- Stincic, T.L.; Grachev, P.; Bosch, M.A.; Rønnekleiv, O.K.; Kelly, M.J. Estradiol Drives the Anorexigenic Activity of Proopiomelanocortin Neurons in Female Mice. eNeuro 2018, 5, ENEURO.0103-18.2018. [Google Scholar] [CrossRef]
- Cahill, C.M.; Cook, C.; Pickens, S. Migraine and Reward System—Or Is It Aversive? Curr. Pain Headache Rep. 2014, 18, 410. [Google Scholar] [CrossRef]
- Krentzel, A.A.; Proaño, S.B.; Dorris, D.M.; Setzer, B.; Meitzen, J. The estrous cycle and 17β-estradiol modulate the electrophysiological properties of rat nucleus accumbens core medium spiny neurons. J. Neuroendocrinol. 2022, 34, e13122. [Google Scholar] [CrossRef]
- Yoest, K.E.; Quigley, J.A.; Becker, J.B. Rapid effects of ovarian hormones in dorsal striatum and nucleus accumbens. Horm. Behav. 2018, 104, 119–129. [Google Scholar] [CrossRef]
- Aggarwal, M.; Puri, V.; Puri, S. Effects of estrogen on the serotonergic system and calcitonin gene-related peptide in trigeminal ganglia of rats. Ann. Neurosci. 2012, 19, 151–157. [Google Scholar] [CrossRef] [PubMed]
- Bereiter, D.A.; Stanford, L.R.; Barker, D.J. Hormone-induced enlargement of receptive fields in trigeminal mechanoreceptive neurons. II. possible mechanisms. Brain Res. 1980, 184, 411–423. [Google Scholar] [CrossRef] [PubMed]
- Schertzinger, M.; Wesson-Sides, K.; Parkitny, L.; Younger, J. Daily Fluctuations of Progesterone and Testosterone Are Associated with Fibromyalgia Pain Severity. J. Pain 2018, 19, 410–417. [Google Scholar] [CrossRef]
- Chuang, S.H.; Reddy, D.S. 3β-Methyl-Neurosteroid Analogs Are Preferential Positive Allosteric Modulators and Direct Activators of Extrasynaptic δ-Subunit γ-Aminobutyric Acid Type A Receptors in the Hippocampus Dentate Gyrus Subfield. J. Pharmacol. Exp. Ther. 2018, 365, 583–601. [Google Scholar] [CrossRef]
- Reddy, D.S. Neurosteroids: Endogenous role in the human brain and therapeutic potentials. Prog. Brain Res. 2010, 186, 113–137. [Google Scholar] [CrossRef] [PubMed]
- Singh, M. Ovarian Hormones Elicit Phosphorylation of Akt and Extracellular-Signal Regulated Kinase in Explants of the Cerebral Cortex. ENDO 2001, 14, 407–416. [Google Scholar] [CrossRef] [PubMed]
- Jang, Y.; Kim, M.; Hwang, S.W. Molecular mechanisms underlying the actions of arachidonic acid-derived prostaglandins on peripheral nociception. J. Neuroinflamm. 2020, 17, 30. [Google Scholar] [CrossRef] [PubMed]
- Andersen, M.L.; Bittencourt, L.R.A.; Antunes, B.I.; Tufik, S. Effects of Progesterone on Sleep: A Possible Pharmacological Treatment for Sleep-Breathing Disorders? CMC 2006, 13, 3575–3582. [Google Scholar] [CrossRef]
- Standeven, L.R.; McEvoy, K.O.; Osborne, L.M. Progesterone, reproduction, and psychiatric illness. Best Pract. Res. Clin. Obstet. Gynaecol. 2020, 69, 108–126. [Google Scholar] [CrossRef]
- Simpson, E.R. Sources of estrogen and their importance. J. Steroid Biochem. Mol. Biol. 2003, 86, 225–230. [Google Scholar] [CrossRef]
- Bartley, E.J.; Palit, S.; Kuhn, B.L.; Kerr, K.L.; Terry, E.L.; DelVentura, J.L.; Rhudy, J.L. Nociceptive processing in women with premenstrual dysphoric disorder (PMDD): The role of menstrual phase and sex hormones. Clin. J. Pain 2015, 31, 304–314. [Google Scholar] [CrossRef]
- Bartley, E.J.; Palit, S.; Kuhn, B.L.; Kerr, K.L.; Terry, E.L.; DelVentura, J.L.; Rhudy, J.L. Natural variation in testosterone is associated with hypoalgesia in healthy women. Clin. J. Pain 2015, 31, 730–739. [Google Scholar] [CrossRef]
- Choi, J.C.; Park, Y.H.; Park, S.K.; Lee, J.S.; Kim, J.; Choi, J.I.; Yoon, K.B.; Lee, S.; Lim, D.E.; Choi, J.Y.; et al. Testosterone effects on pain and brain activation patterns. Acta Anaesthesiol. Scand. 2017, 61, 668–675. [Google Scholar] [CrossRef]
- Choi, J.C.; Chung, M.I.; Lee, Y.D. Modulation of pain sensation by stress-related testosterone and cortisol. Anaesthesia 2012, 67, 1146–1151. [Google Scholar] [CrossRef] [PubMed]
- Teepker, M.; Peters, M.; Vedder, H.; Schepelmann, K.; Lautenbacher, S. Menstrual variation in experimental pain: Correlation with gonadal hormones. Neuropsychobiology 2010, 61, 131–140. [Google Scholar] [CrossRef]
- Aloisi, A.M.; Ceccarelli, I.; Fiorenzani, P. Gonadectomy affects hormonal and behavioral responses to repetitive nociceptive stimulation in male rats. Ann. N. Y. Acad. Sci. 2003, 1007, 232–237. [Google Scholar] [CrossRef] [PubMed]
- Ceccarelli, I.; Scaramuzzino, A.; Massafra, C.; Aloisi, A.M. The behavioral and neuronal effects induced by repetitive nociceptive stimulation are affected by gonadal hormones in male rats. Pain 2003, 104, 35–47. [Google Scholar] [CrossRef] [PubMed]
- Gaumond, I.; Arsenault, P.; Marchand, S. Specificity of female and male sex hormones on excitatory and inhibitory phases of formalin-induced nociceptive responses. Brain Res. 2005, 1052, 105–111. [Google Scholar] [CrossRef] [PubMed]
- Aloisi, A.M.; Ceccarelli, I.; Fiorenzani, P.; De Padova, A.M.; Massafra, C. Testosterone affects formalin-induced responses differently in male and female rats. Neurosci. Lett. 2004, 361, 262–264. [Google Scholar] [CrossRef] [PubMed]
- Stoffel, E.C.; Ulibarri, C.M.; Craft, R.M. Gonadal steroid hormone modulation of nociception, morphine antinociception and reproductive indices in male and female rats. Pain 2003, 103, 285–302. [Google Scholar] [CrossRef]
- Basaria, S.; Travison, T.G.; Alford, D.; Knapp, P.E.; Teeter, K.; Cahalan, C.; Eder, R.; Lakshman, K.; Bachman, E.; Mensing, G.; et al. Effects of testosterone replacement in men with opioid-induced androgen deficiency: A randomized controlled trial. Pain 2015, 156, 280–288. [Google Scholar] [CrossRef]
- Verhagen, I.E.; Brandt, R.B.; Kruitbosch, C.M.A.; MaassenVanDenBrink, A.; Fronczek, R.; Terwindt, G.M. Clinical symptoms of androgen deficiency in men with migraine or cluster headache: A cross-sectional cohort study. J. Headache Pain 2021, 22, 125. [Google Scholar] [CrossRef]
- Martinez, C.I.; Liktor-Busa, E.; Largent-Milnes, T.M. Molecular mechanisms of hormones implicated in migraine and the translational implication for transgender patients. Front. Pain Res. 2023, 4, 1117842. [Google Scholar] [CrossRef]
- Ahmad, A.H.; Ismail, Z. c-fos and its Consequences in Pain. Malays. J. Med. Sci. 2002, 9, 3–8. [Google Scholar] [PubMed]
- White, H.D.; Brown, L.A.J.; Gyurik, R.J.; Manganiello, P.D.; Robinson, T.D.; Hallock, L.S.; Lewis, L.D.; Yeo, Y.-T.J. Treatment of pain in fibromyalgia patients with testosterone gel: Pharmacokinetics and clinical response. Int. Immunopharmacol. 2015, 27, 249–256. [Google Scholar] [CrossRef] [PubMed]
- Fischer, L.; Clemente, J.T.; Tambeli, C.H. The protective role of testosterone in the development of temporomandibular joint pain. J. Pain 2007, 8, 437–442. [Google Scholar] [CrossRef] [PubMed]
- Glaser, R.; Dimitrakakis, C.; Trimble, N.; Martin, V. Testosterone pellet implants and migraine headaches: A pilot study. Maturitas 2012, 71, 385–388. [Google Scholar] [CrossRef] [PubMed]
- English, K.M.; Steeds, R.P.; Jones, T.H.; Diver, M.J.; Channer, K.S. Low-dose transdermal testosterone therapy improves angina threshold in men with chronic stable angina: A randomized, double-blind, placebo-controlled study. Circulation 2000, 102, 1906–1911. [Google Scholar] [CrossRef] [PubMed]
- Tzabazis, A.; Kori, S.; Mechanic, J.; Miller, J.; Pascual, C.; Manering, N.; Carson, D.; Klukinov, M.; Spierings, E.; Jacobs, D.; et al. Oxytocin and Migraine Headache. Headache 2017, 57 (Suppl. S2), 64–75. [Google Scholar] [CrossRef] [PubMed]
- Rash, J.A.; Aguirre-Camacho, A.; Campbell, T.S. Oxytocin and pain: A systematic review and synthesis of findings. Clin. J. Pain 2014, 30, 453–462. [Google Scholar] [CrossRef] [PubMed]
- Shamay-Tsoory, S.G.; Abu-Akel, A. The Social Salience Hypothesis of Oxytocin. Biol. Psychiatry 2016, 79, 194–202. [Google Scholar] [CrossRef]
- Phillips, W.J.; Ostrovsky, O.; Galli, R.L.; Dickey, S. Relief of acute migraine headache with intravenous oxytocin: Report of two cases. J. Pain Palliat. Care Pharmacother. 2006, 20, 25–28. [Google Scholar] [CrossRef]
- Wang, Y.L.; Yuan, Y.; Yang, J.; Wang, C.H.; Pan, Y.J.; Lu, L.; Wu, Y.Q.; Wang, D.X.; Lv, L.X.; Li, R.R.; et al. The interaction between the oxytocin and pain modulation in headache patients. Neuropeptides 2013, 47, 93–97. [Google Scholar] [CrossRef]
- Paloyelis, Y.; Krahé, C.; Maltezos, S.; Williams, S.C.; Howard, M.A.; Fotopoulou, A. The Analgesic Effect of Oxytocin in Humans: A Double-Blind, Placebo-Controlled Cross-Over Study Using Laser-Evoked Potentials. J. Neuroendocrinol. 2016, 28. [Google Scholar] [CrossRef] [PubMed]
- MacDonald, E.; Dadds, M.R.; Brennan, J.L.; Williams, K.; Levy, F.; Cauchi, A.J. A review of safety, side-effects and subjective reactions to intranasal oxytocin in human research. Psychoneuroendocrinology 2011, 36, 1114–1126. [Google Scholar] [CrossRef] [PubMed]
- Iwasaki, M.; Lefevre, A.; Althammer, F.; Creusot, E.C.; Łąpieś, O.; Petitjean, H.; Hilfiger, L.; Kerspern, D.; Melchior, M.; Küppers, S.; et al. An analgesic pathway from parvocellular oxytocin neurons to the periaqueductal gray in rats. Nat. Commun. 2023, 14, 1066. [Google Scholar] [CrossRef] [PubMed]
- Swanson, L.W.; McKellar, S. The distribution of oxytocin- and neurophysin-stained fibers in the spinal cord of the rat and monkey. J. Comp. Neurol. 1979, 188, 87–106. [Google Scholar] [CrossRef] [PubMed]
- Breton, J.D.; Veinante, P.; Uhl-Bronner, S.; Vergnano, A.M.; Freund-Mercier, M.J.; Schlichter, R.; Poisbeau, P. Oxytocin-induced antinociception in the spinal cord is mediated by a subpopulation of glutamatergic neurons in lamina I-II which amplify GABAergic inhibition. Mol. Pain 2008, 4, 19. [Google Scholar] [CrossRef] [PubMed]
- Rojas-Piloni, G.; López-Hidalgo, M.; Martínez-Lorenzana, G.; Rodríguez-Jiménez, J.; Condés-Lara, M. GABA-mediated oxytocinergic inhibition in dorsal horn neurons by hypothalamic paraventricular nucleus stimulation. Brain Res. 2007, 1137, 69–77. [Google Scholar] [CrossRef] [PubMed]
- Condés-Lara, M.; González, N.M.; Martínez-Lorenzana, G.; Delgado, O.L.; Freund-Mercier, M.J. Actions of oxytocin and interactions with glutamate on spontaneous and evoked dorsal spinal cord neuronal activities. Brain Res. 2003, 976, 75–81. [Google Scholar] [CrossRef]
- Miranda-Cardenas, Y.; Rojas-Piloni, G.; Martínez-Lorenzana, G.; Rodríguez-Jiménez, J.; López-Hidalgo, M.; Freund-Mercier, M.J.; Condés-Lara, M. Oxytocin and electrical stimulation of the paraventricular hypothalamic nucleus produce antinociceptive effects that are reversed by an oxytocin antagonist. Pain 2006, 122, 182–189. [Google Scholar] [CrossRef]
- Yang, J.; Liang, J.Y.; Li, P.; Pan, Y.J.; Qiu, P.Y.; Zhang, J.; Hao, F.; Wang, D.X. Oxytocin in the periaqueductal gray participates in pain modulation in the rat by influencing endogenous opiate peptides. Peptides 2011, 32, 1255–1261. [Google Scholar] [CrossRef]
- Yang, J.; Li, P.; Liang, J.Y.; Pan, Y.J.; Yan, X.Q.; Yan, F.L.; Hao, F.; Zhang, X.Y.; Zhang, J.; Qiu, P.Y.; et al. Oxytocin in the periaqueductal grey regulates nociception in the rat. Regul. Pept. 2011, 169, 39–42. [Google Scholar] [CrossRef]
- Yang, J.; Yang, Y.; Chen, J.M.; Liu, W.Y.; Wang, C.H.; Lin, B.C. Central oxytocin enhances antinociception in the rat. Peptides 2007, 28, 1113–1119. [Google Scholar] [CrossRef] [PubMed]
- Yang, J.; Yang, Y.; Chen, J.M.; Liu, W.Y.; Lin, B.C. Investigating the role of the hypothalamic supraoptic nucleus in nociception in the rat. Life Sci. 2008, 82, 166–173. [Google Scholar] [CrossRef] [PubMed]
- Warfvinge, K.; Krause, D.N.; Maddahi, A.; Grell, A.-S.; Edvinsson, J.C.A.; Haanes, K.A.; Edvinsson, L. Oxytocin as a regulatory neuropeptide in the trigeminovascular system: Localization, expression and function of oxytocin and oxytocin receptors. Cephalalgia 2020, 40, 1283–1295. [Google Scholar] [CrossRef] [PubMed]
- Warfvinge, K.; Krause, D.; Edvinsson, L. The distribution of oxytocin and the oxytocin receptor in rat brain: Relation to regions active in migraine. J. Headache Pain 2020, 21, 10. [Google Scholar] [CrossRef] [PubMed]
- Huang, C.L.; Liu, F.; Zhang, Y.Y.; Lin, J.; Fu, M.; Li, Y.L.; Zhou, C.; Li, C.J.; Shen, J.F. Activation of oxytocin receptor in the trigeminal ganglion attenuates orofacial ectopic pain attributed to inferior alveolar nerve injury. J. Neurophysiol. 2021, 125, 223–231. [Google Scholar] [CrossRef] [PubMed]
- Bharadwaj, V.N.; Porreca, F.; Cowan, R.P.; Kori, S.; Silberstein, S.D.; Yeomans, D.C. A new hypothesis linking oxytocin to menstrual migraine. Headache J. Head Face Pain 2021, 61, 1051–1059. [Google Scholar] [CrossRef] [PubMed]
- Dalkara, T.; Nozari, A.; Moskowitz, M.A. Migraine aura pathophysiology: The role of blood vessels and microembolisation. Lancet Neurol. 2010, 9, 309–317. [Google Scholar] [CrossRef] [PubMed]
- Gupta, V. Does Vasopressin Serve a Vasomotor Adaptive Function in Migraine? Cephalalgia 1993, 13, 221. [Google Scholar] [CrossRef]
- Buschmann, J.; Leppla-Wollsiffer, G.; Nemeth, N.; Nelson, K.; Kirsten, R. Migraine patients show increased platelet vasopressin receptors. Headache 1996, 36, 586–588. [Google Scholar] [CrossRef]
- Hampton, K.K.; Esack, A.; Peatfield, R.C.; Grant, P.J. Elevation of plasma vasopressin in spontaneous migraine. Cephalalgia 1991, 11, 249–250. [Google Scholar] [CrossRef]
- Peatfield, R.C.; Hampton, K.K.; Grant, P.J. Plasma vasopressin levels in induced migraine attacks. Cephalalgia 1988, 8, 55–57. [Google Scholar] [CrossRef]
- Bahadoram, M.; Mahmoudian-Sani, M.R.; Keikhaei, B.; Alikhani, K.; Bahadoram, S. The antimigraine action of arginine-vasopressin: A theoretical basis. Future Neurol. 2020, 15, FNL51. [Google Scholar] [CrossRef]
- Yang, J.; Lu, L.; Wang, H.C.; Zhan, H.Q.; Hai, G.F.; Pan, Y.J.; Lv, Q.Q.; Wang, D.X.; Wu, Y.Q.; Li, R.R.; et al. Effect of intranasal arginine vasopressin on human headache. Peptides 2012, 38, 100–104. [Google Scholar] [CrossRef] [PubMed]
- Warfvinge, K.; Krause, D.N.; Maddahi, A.; Edvinsson, J.C.A.; Edvinsson, L.; Haanes, K.A. Estrogen receptors α, β and GPER in the CNS and trigeminal system—Molecular and functional aspects. J. Headache Pain 2020, 21, 131. [Google Scholar] [CrossRef]
- Maddahi, A.; Edvinsson, L.; Warfvinge, K. Expression of vasopressin and its receptors in migraine-related regions in CNS and the trigeminal system: Influence of sex. J. Headache Pain 2022, 23, 152. [Google Scholar] [CrossRef]
- Avona, A.; Mason, B.N.; Burgos-Vega, C.; Hovhannisyan, A.H.; Belugin, S.N.; Mecklenburg, J.; Goffin, V.; Wajahat, N.; Price, T.J.; Akopian, A.N.; et al. Meningeal CGRP-Prolactin Interaction Evokes Female-Specific Migraine Behavior. Ann. Neurol. 2021, 89, 1129–1144. [Google Scholar] [CrossRef] [PubMed]
- Al-Karagholi, M.A.M.; Kalatharan, V.; Ghanizada, H.; Gram, C.; Dussor, G.; Ashina, M. Prolactin in headache and migraine: A systematic review of clinical studies. Cephalalgia 2023, 43, 3331024221136286. [Google Scholar] [CrossRef]
- Maciuba, S.; Bowden, G.D.; Stratton, H.J.; Wisniewski, K.; Schteingart, C.D.; Almagro, J.C.; Valadon, P.; Lowitz, J.; Glaser, S.M.; Lee, G.; et al. Discovery and characterization of prolactin neutralizing monoclonal antibodies for the treatment of female-prevalent pain disorders. mAbs 2023, 15, 2254676. [Google Scholar] [CrossRef] [PubMed]
- Mamlouk, G.M.; Dorris, D.M.; Barrett, L.R.; Meitzen, J. Sex bias and omission in neuroscience research is influenced by research model and journal, but not reported NIH funding. Front. Neuroendocrinol. 2020, 57, 100835. [Google Scholar] [CrossRef]
- Will, T.R.; Proaño, S.B.; Thomas, A.M.; Kunz, L.M.; Thompson, K.C.; Ginnari, L.A.; Jones, C.H.; Lucas, S.-C.; Reavis, E.M.; Dorris, D.M.; et al. Problems and Progress regarding Sex Bias and Omission in Neuroscience Research. eNeuro 2017, 4, ENEURO.0278-17.2017. [Google Scholar] [CrossRef] [PubMed]
- Labastida-Ramírez, A.; Rubio-Beltrán, E.; Villalón, C.M.; MaassenVanDenBrink, A. Gender aspects of CGRP in migraine. Cephalalgia 2019, 39, 435–444. [Google Scholar] [CrossRef] [PubMed]
- Lenert, M.E.; Avona, A.; Garner, K.M.; Barron, L.R.; Burton, M.D. Sensory Neurons, Neuroimmunity, and Pain Modulation by Sex Hormones. Endocrinology 2021, 162, bqab109. [Google Scholar] [CrossRef]
- Harvey, M.P.; Dubois, M.C.; Chalaye, P.; Sansoucy, Y.; Marchand, S. Sex-Related Effects of Adrenergic Drugs on Conditioned Pain Modulation: A Randomized Controlled Cross-Over Double-Blind Trial. Pain Res. Manag. 2022, 2022, 2757101. [Google Scholar] [CrossRef] [PubMed]
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Godley, F., III; Meitzen, J.; Nahman-Averbuch, H.; O’Neal, M.A.; Yeomans, D.; Santoro, N.; Riggins, N.; Edvinsson, L. How Sex Hormones Affect Migraine: An Interdisciplinary Preclinical Research Panel Review. J. Pers. Med. 2024, 14, 184. https://doi.org/10.3390/jpm14020184
Godley F III, Meitzen J, Nahman-Averbuch H, O’Neal MA, Yeomans D, Santoro N, Riggins N, Edvinsson L. How Sex Hormones Affect Migraine: An Interdisciplinary Preclinical Research Panel Review. Journal of Personalized Medicine. 2024; 14(2):184. https://doi.org/10.3390/jpm14020184
Chicago/Turabian StyleGodley, Frederick, III, John Meitzen, Hadas Nahman-Averbuch, Mary Angela O’Neal, David Yeomans, Nanette Santoro, Nina Riggins, and Lars Edvinsson. 2024. "How Sex Hormones Affect Migraine: An Interdisciplinary Preclinical Research Panel Review" Journal of Personalized Medicine 14, no. 2: 184. https://doi.org/10.3390/jpm14020184