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Estrogen-dependent effects of 5-hydroxytryptophan on cortical spreading depression in rat: Modelling the serotonin-ovarian hormone interaction in migraine aura.
Cephalalgia 2018; 38(3):427-436C

Abstract

Background Cortical spreading depression (CSD) is the likely culprit of the migraine aura. Migraine is sexually dimorphic and thought to be a "low 5-HT" condition. We sought to decipher the interrelation between serotonin, ovarian hormones and cortical excitability in a model of migraine aura. Methods Occipital KCl-induced CSDs were recorded for one hour at parieto-occipital and frontal levels in adult male (n = 16) and female rats (n = 64) one hour after intraperitoneal (i.p.) injection of 5-hydroxytryptophan (5-HTP) or NaCl. Sixty-five oophorectomized females were treated with estradiol- (E2) or cholesterol- (Chol) filled capsules. Two weeks later we recorded CSDs after 5-HTP/NaCl injections before or 20 hours after capsule removal. Results 5-HTP had no effect in males, but decreased CSD frequency in cycling females, significantly so during estrus, at parieto-occipital (-3.5CSD/h, p < 0.001) and frontal levels (-2.5CSD/h, p = 0.014). In oophorectomized rats, CSD susceptibility increased during E2 treatment at both recording sites (+5CSD/h, p = 0.001 and +3CSD/h, p < 0.01), but decreased promptly after E2 withdrawal (-4.7CSD/h, p < 0.001 and -1.7CSD/h, p = 0.094). The CSD inhibitory effect of 5-HTP was significant only in E2-treated rats (-3.4CSD/h, p = 0.006 and -1.8CSD/h, p = 0.029). Neither the estrous cycle phase, nor E2 or 5-HTP treatments significantly modified CSD propagation velocity. Conclusion 5-HTP decreases CSD occurrence in the presence of ovarian hormones, suggesting its potential efficacy in migraine with aura prophylaxis in females. Elevated E2 levels increase CSD susceptibility, while estrogen withdrawal decreases CSD. In a translational perspective, these findings may explain why migraine auras can appear during pregnancy and why menstrual-related migraine attacks are rarely associated with an aura.

Authors+Show Affiliations

1 Cephalic Pain Unit of GIGA-Neurosciences, Liège University, Liège, Belgium.1 Cephalic Pain Unit of GIGA-Neurosciences, Liège University, Liège, Belgium.1 Cephalic Pain Unit of GIGA-Neurosciences, Liège University, Liège, Belgium. 2 Headache Research Unit, Department of Neurology, Liège University, Citadelle Hospital, Liège, Belgium.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

28145727

Citation

Chauvel, Virginie, et al. "Estrogen-dependent Effects of 5-hydroxytryptophan On Cortical Spreading Depression in Rat: Modelling the Serotonin-ovarian Hormone Interaction in Migraine Aura." Cephalalgia : an International Journal of Headache, vol. 38, no. 3, 2018, pp. 427-436.
Chauvel V, Multon S, Schoenen J. Estrogen-dependent effects of 5-hydroxytryptophan on cortical spreading depression in rat: Modelling the serotonin-ovarian hormone interaction in migraine aura. Cephalalgia. 2018;38(3):427-436.
Chauvel, V., Multon, S., & Schoenen, J. (2018). Estrogen-dependent effects of 5-hydroxytryptophan on cortical spreading depression in rat: Modelling the serotonin-ovarian hormone interaction in migraine aura. Cephalalgia : an International Journal of Headache, 38(3), pp. 427-436. doi:10.1177/0333102417690891.
Chauvel V, Multon S, Schoenen J. Estrogen-dependent Effects of 5-hydroxytryptophan On Cortical Spreading Depression in Rat: Modelling the Serotonin-ovarian Hormone Interaction in Migraine Aura. Cephalalgia. 2018;38(3):427-436. PubMed PMID: 28145727.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Estrogen-dependent effects of 5-hydroxytryptophan on cortical spreading depression in rat: Modelling the serotonin-ovarian hormone interaction in migraine aura. AU - Chauvel,Virginie, AU - Multon,Sylvie, AU - Schoenen,Jean, Y1 - 2017/02/01/ PY - 2017/2/2/pubmed PY - 2019/1/27/medline PY - 2017/2/2/entrez KW - 5-hydroxytryptophan KW - Cortical spreading depression KW - estrogen KW - migraine with aura KW - serotonin SP - 427 EP - 436 JF - Cephalalgia : an international journal of headache JO - Cephalalgia VL - 38 IS - 3 N2 - Background Cortical spreading depression (CSD) is the likely culprit of the migraine aura. Migraine is sexually dimorphic and thought to be a "low 5-HT" condition. We sought to decipher the interrelation between serotonin, ovarian hormones and cortical excitability in a model of migraine aura. Methods Occipital KCl-induced CSDs were recorded for one hour at parieto-occipital and frontal levels in adult male (n = 16) and female rats (n = 64) one hour after intraperitoneal (i.p.) injection of 5-hydroxytryptophan (5-HTP) or NaCl. Sixty-five oophorectomized females were treated with estradiol- (E2) or cholesterol- (Chol) filled capsules. Two weeks later we recorded CSDs after 5-HTP/NaCl injections before or 20 hours after capsule removal. Results 5-HTP had no effect in males, but decreased CSD frequency in cycling females, significantly so during estrus, at parieto-occipital (-3.5CSD/h, p < 0.001) and frontal levels (-2.5CSD/h, p = 0.014). In oophorectomized rats, CSD susceptibility increased during E2 treatment at both recording sites (+5CSD/h, p = 0.001 and +3CSD/h, p < 0.01), but decreased promptly after E2 withdrawal (-4.7CSD/h, p < 0.001 and -1.7CSD/h, p = 0.094). The CSD inhibitory effect of 5-HTP was significant only in E2-treated rats (-3.4CSD/h, p = 0.006 and -1.8CSD/h, p = 0.029). Neither the estrous cycle phase, nor E2 or 5-HTP treatments significantly modified CSD propagation velocity. Conclusion 5-HTP decreases CSD occurrence in the presence of ovarian hormones, suggesting its potential efficacy in migraine with aura prophylaxis in females. Elevated E2 levels increase CSD susceptibility, while estrogen withdrawal decreases CSD. In a translational perspective, these findings may explain why migraine auras can appear during pregnancy and why menstrual-related migraine attacks are rarely associated with an aura. SN - 1468-2982 UR - https://www.unboundmedicine.com/medline/citation/28145727/Estrogen_dependent_effects_of_5_hydroxytryptophan_on_cortical_spreading_depression_in_rat:_Modelling_the_serotonin_ovarian_hormone_interaction_in_migraine_aura_ L2 - http://journals.sagepub.com/doi/full/10.1177/0333102417690891?url_ver=Z39.88-2003&amp;rfr_id=ori:rid:crossref.org&amp;rfr_dat=cr_pub=pubmed DB - PRIME DP - Unbound Medicine ER -