Biomarkers of Migraine: An Integrated Evaluation of Preclinical and Clinical Findings
Abstract
:1. Introduction
Migraine Pathogenesis
2. Methods
3. The Potential Circulating Biomarkers Described in Migraine Patients and Migraine Animal Models
3.1. Neuropeptides
3.1.1. Calcitonin Gene-Related Peptide (CGRP)
3.1.2. Other Peptides of the CGRP Family
3.1.3. Substance P (SP)
3.1.4. Pituitary Adenylate Cyclase-Activating Polypeptide (PACAP)
3.1.5. Vasoactive Intestinal Polypeptide (VIP)
3.1.6. Neuropeptide Y (NPY)
3.2. Classic Neurotransmitters
3.3. Mediators of Inflammation and Immunity
3.3.1. Cytokines
3.3.2. Adipocytokines
3.3.3. Prostaglandins
3.3.4. Pentraxin-3 (PTX-3)
3.3.5. IgG
3.3.6. Matrix Metalloproteinase-9 (MMP-9)
3.4. Endocannabinoids and Related Lipids
3.5. MicroRNAs
3.6. Mediators of Endothelial/Vascular Functions
3.6.1. Endothelial Progenitor Cells (EPCs)
3.6.2. Endothelin-1 (ET-1)
3.6.3. Homocysteine
3.7. Other Biomarkers
3.7.1. Tryptophan and Kynurenine
3.7.2. Melatonin
3.7.3. Growth Factors
3.7.4. Mediators of Oxidative Stress
3.7.5. Apolipoprotein E
4. Fitting Together the Pieces of a Complex Picture
5. Considerations and Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Biomarkers | Clinical Sample | Preclinical Sample | Clinical Findings | Preclinical Findings | Key Conclusions |
---|---|---|---|---|---|
Neuropeptides | |||||
CGRP | Blood (plasma, serum), Saliva, CSF | Blood (plasma, serum) | ↑ Levels in EM and CM patients during interictal and ictal phases [28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,47,48,49,54]; Index of good response to onabotulinumtoxinA treatment and detoxification in CM or MO-CM patients [36,52,65,66,68]; Unchanged levels in EM and CM patients during interictal and ictal phases [42,43,44,45,46,52,63] | ↑ in rodents and cat [55,56,57,58,59,60,61,62] | Potential diagnostic biomarker and potential biomarker for prediction of response to treatments |
Substance P | Blood (plasma, serum) | Blood (plasma, serum) | ↑ Levels in EM patients during interictal and ictal phases and interictal CM [32,33,79] Unchanged levels in EM patients and HC [80,81] | ↑ levels in rat [62] | |
PACAP | Blood (plasma, serum) | Blood (plasma) | ↑ Levels in EM patients during interictal and ictal phases [42,86,87,89] or ↓levels in EM patients during interictal phase [87,88]↑ levels in CM patients during interictal phase [42] Unchanged in EM or CM during interictal or vs. HC [42,85] | ↑ levels in rat and cat [57,61,62,90] | Potential Therapeutic Biomarker |
VIP | Blood (plasma) | Blood (plasma) | ↑Levels EM and CM patients during interictal and ictal phases [31,36,42,65,81,85,86] Correlation with autonomic symptoms [81,94] and cranial parasympathetic symptoms [95] Index of good response to triptan treatment in EM [94] | ↑ levels in rat [61,62] | |
NPY | Blood (plasma) CSF | Blood (plasma) | ↑ Levels in CSF [100] or ↓ levels in plasma in CM and EM patients during ictal phase migraine patients [102] Unchanged levels in EM patients during ictal and interictal phases and vs. HC [81,101] | ↑ levels in rat [61] | |
Classic Neurotransmitters | |||||
Glutamate | Blood (plasma) Saliva CSF | Blood (serum) | ↑ Plasma and salivary levels in EM and CM patients vs. HC during interictal and ictal phase [106,114,115,116,117,118,119] ↑ CSF levels in EM and CM vs. HC during ictal phase [30,120,121] | ↑ levels in rat [122] | |
Inflammatory Mediators | |||||
Cytokines | Blood (plasma, serum), CSF | Blood (serum) | ↑ IL-6, TNF-α, IL-1β, TGF-β1 levels in EM patients during interictal phase [132,138,139,140] ↑ IL-6, TNF-α levels in CM patients during ictal and interictal phase [134,144,145] | ↑ IL-6, TNF-α, IL-1β levels in rat [56] | |
Other Potential Biomarkers | |||||
Endocannabinoids and related lipids | Blood (platelets, plasma), Saliva, CSF | Data available only for brain areas | ↑ PEA levels in EM patients during ictal phase induced by nitroglycerin [188] ↓ Salivary PEA levels in migraine patients [189] ↓ AEA, 2-AG, and PEA levels in CM and MOH patients [185,186] AEA and related lipid levels unchanged during the interictal phase in EM patients vs. HC [187,188] ↑FAAH and AEA transporter activities in woman EM patients [190] ↓FAAH and the AEA transporter activity in CM and MOH patients [191] | Increased levels of the degrading enzymes FAAH and MAGL [193] | |
MicroRNAs | Blood (plasma, serum) | Data available only for brain areas | ↑ miR-34a-5p levels in CM during ictal phase and in CM and MOH patients during interictal phase [66,204] ↑miR-382-5p levels CM during ictal phase and CM and MOH patients during interictal phase [66,204] ↓ miR-30 in EM patients [205] ↑ miR-155 in EM patients in interictal phase [206] | ↑ miR-155-5p, miR-34a-5p, and miR-382-5p in several brain areas. Inhibitory effect of a CGRP antagonist [56] | |
ET-1 | Blood (plasma) | Blood (plasma) | ↑ levels in EM patients in the early stages of the attack [220,221,222,223,224] Conflicting results in interictal phase [221,222,225,226,227] | ↑ or ↓ levels in rodents [108,228] | |
Tryptophan and Kynurenine Metabolism | Blood (plasma, serum) | CSF | ↓ Levels in EM patients during interictal and ictal phases [110,252] ↓ levels only of kynurenine metabolites in CM patients during interictal phase [254] ↑ levels in EM and CM patients vs. HC during interictal phase [254,255] Unchanged levels in EM patients during interictal phase [253] | ↓ levels in rat [251] |
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Demartini, C.; Francavilla, M.; Zanaboni, A.M.; Facchetti, S.; De Icco, R.; Martinelli, D.; Allena, M.; Greco, R.; Tassorelli, C. Biomarkers of Migraine: An Integrated Evaluation of Preclinical and Clinical Findings. Int. J. Mol. Sci. 2023, 24, 5334. https://doi.org/10.3390/ijms24065334
Demartini C, Francavilla M, Zanaboni AM, Facchetti S, De Icco R, Martinelli D, Allena M, Greco R, Tassorelli C. Biomarkers of Migraine: An Integrated Evaluation of Preclinical and Clinical Findings. International Journal of Molecular Sciences. 2023; 24(6):5334. https://doi.org/10.3390/ijms24065334
Chicago/Turabian StyleDemartini, Chiara, Miriam Francavilla, Anna Maria Zanaboni, Sara Facchetti, Roberto De Icco, Daniele Martinelli, Marta Allena, Rosaria Greco, and Cristina Tassorelli. 2023. "Biomarkers of Migraine: An Integrated Evaluation of Preclinical and Clinical Findings" International Journal of Molecular Sciences 24, no. 6: 5334. https://doi.org/10.3390/ijms24065334
APA StyleDemartini, C., Francavilla, M., Zanaboni, A. M., Facchetti, S., De Icco, R., Martinelli, D., Allena, M., Greco, R., & Tassorelli, C. (2023). Biomarkers of Migraine: An Integrated Evaluation of Preclinical and Clinical Findings. International Journal of Molecular Sciences, 24(6), 5334. https://doi.org/10.3390/ijms24065334