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Ex vivo stimulation of the trigeminal nucleus caudalis induces peripheral CGRP release in the trigeminal ganglion and reveals a distinct dopamine–endocannabinoid mechanism relevant to migraine

Christiansen, Isabella Mai ; Reducha, Philip Victor ; Edvinsson, Lars LU ; Holm, Anja and Haanes, Kristian Agmund (2025) In Journal of Headache and Pain 26(1).
Abstract

Background: Calcitonin gene-related peptide (CGRP) release from trigeminal structures is central to migraine pathophysiology. This study employed an ex vivo model preserving anatomical continuity between the trigeminal nucleus caudalis (TNC) and trigeminal ganglion (TG) to investigate (1) whether TNC stimulation induces peripheral CGRP release from the TG and (2) the potential involvement of a distinct dopamine–endocannabinoid mechanism. Methods: Tissues were dissected as a single unit and placed in custom 3D-printed chambers, allowing targeted stimulation of either the TNC or the TG while measuring CGRP in both compartments. Pharmacological tools, including capsaicin (TRPV1 agonist), KCl (depolarizing agent), dopamine, and selective... (More)

Background: Calcitonin gene-related peptide (CGRP) release from trigeminal structures is central to migraine pathophysiology. This study employed an ex vivo model preserving anatomical continuity between the trigeminal nucleus caudalis (TNC) and trigeminal ganglion (TG) to investigate (1) whether TNC stimulation induces peripheral CGRP release from the TG and (2) the potential involvement of a distinct dopamine–endocannabinoid mechanism. Methods: Tissues were dissected as a single unit and placed in custom 3D-printed chambers, allowing targeted stimulation of either the TNC or the TG while measuring CGRP in both compartments. Pharmacological tools, including capsaicin (TRPV1 agonist), KCl (depolarizing agent), dopamine, and selective enzyme inhibitors or receptor antagonists, were used to elucidate underlying signalling pathways. CGRP levels were quantified via enzyme-linked immunosorbent assay. Results: Stimulation of the TNC elicited a significant rise in CGRP release locally and in the TG compartment, whereas directly stimulating the TG did not trigger CGRP release in the TNC. Subsequent experiments showed that applying dopamine to the TNC further enhanced CGRP release. TRPV1 blockade or pharmacological inhibition of N-acyl phosphatidylethanolamine phospholipase D (NAPE-PLD), an enzyme important for anandamide biosynthesis, markedly attenuated dopamine-induced CGRP release, indicating that an endocannabinoid-driven mechanism is involved. Conclusion: Activating the TNC alone was sufficient to evoke CGRP release in the peripheral trigeminal compartment, underscoring a potential central-to-peripheral mechanism that may be relevant to migraine. Moreover, a dopamine–endocannabinoid–TRPV1 axis appears to modulate CGRP signalling in this system, indicating additional complexity and providing potential new strategies for migraine therapy.

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author
; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Calcitonin gene-related peptide, Dopamine, Endocannabinoid system, Ex vivo model, Migraine, Trigeminal ganglion, Trigeminal nucleus caudalis, TRPV1
in
Journal of Headache and Pain
volume
26
issue
1
article number
141
publisher
BioMed Central (BMC)
external identifiers
  • pmid:40524163
  • scopus:105008110962
ISSN
1129-2369
DOI
10.1186/s10194-025-02072-6
language
English
LU publication?
yes
id
55427149-b781-4ab6-b77d-091b1f079f75
date added to LUP
2025-10-23 11:32:15
date last changed
2025-10-24 03:00:02
@article{55427149-b781-4ab6-b77d-091b1f079f75,
  abstract     = {{<p>Background: Calcitonin gene-related peptide (CGRP) release from trigeminal structures is central to migraine pathophysiology. This study employed an ex vivo model preserving anatomical continuity between the trigeminal nucleus caudalis (TNC) and trigeminal ganglion (TG) to investigate (1) whether TNC stimulation induces peripheral CGRP release from the TG and (2) the potential involvement of a distinct dopamine–endocannabinoid mechanism. Methods: Tissues were dissected as a single unit and placed in custom 3D-printed chambers, allowing targeted stimulation of either the TNC or the TG while measuring CGRP in both compartments. Pharmacological tools, including capsaicin (TRPV1 agonist), KCl (depolarizing agent), dopamine, and selective enzyme inhibitors or receptor antagonists, were used to elucidate underlying signalling pathways. CGRP levels were quantified via enzyme-linked immunosorbent assay. Results: Stimulation of the TNC elicited a significant rise in CGRP release locally and in the TG compartment, whereas directly stimulating the TG did not trigger CGRP release in the TNC. Subsequent experiments showed that applying dopamine to the TNC further enhanced CGRP release. TRPV1 blockade or pharmacological inhibition of N-acyl phosphatidylethanolamine phospholipase D (NAPE-PLD), an enzyme important for anandamide biosynthesis, markedly attenuated dopamine-induced CGRP release, indicating that an endocannabinoid-driven mechanism is involved. Conclusion: Activating the TNC alone was sufficient to evoke CGRP release in the peripheral trigeminal compartment, underscoring a potential central-to-peripheral mechanism that may be relevant to migraine. Moreover, a dopamine–endocannabinoid–TRPV1 axis appears to modulate CGRP signalling in this system, indicating additional complexity and providing potential new strategies for migraine therapy.</p>}},
  author       = {{Christiansen, Isabella Mai and Reducha, Philip Victor and Edvinsson, Lars and Holm, Anja and Haanes, Kristian Agmund}},
  issn         = {{1129-2369}},
  keywords     = {{Calcitonin gene-related peptide; Dopamine; Endocannabinoid system; Ex vivo model; Migraine; Trigeminal ganglion; Trigeminal nucleus caudalis; TRPV1}},
  language     = {{eng}},
  number       = {{1}},
  publisher    = {{BioMed Central (BMC)}},
  series       = {{Journal of Headache and Pain}},
  title        = {{Ex vivo stimulation of the trigeminal nucleus caudalis induces peripheral CGRP release in the trigeminal ganglion and reveals a distinct dopamine–endocannabinoid mechanism relevant to migraine}},
  url          = {{http://dx.doi.org/10.1186/s10194-025-02072-6}},
  doi          = {{10.1186/s10194-025-02072-6}},
  volume       = {{26}},
  year         = {{2025}},
}