Ultrastructural imaging reveals vascular remodeling in migraine patients.
Microscopy
Migraine disorders
Pain
Phenotypic switching
Vascular remodeling
Vascular smooth muscle cell
Journal
Histochemistry and cell biology
ISSN: 1432-119X
Titre abrégé: Histochem Cell Biol
Pays: Germany
ID NLM: 9506663
Informations de publication
Date de publication:
Apr 2022
Apr 2022
Historique:
accepted:
09
12
2021
pubmed:
30
1
2022
medline:
14
4
2022
entrez:
29
1
2022
Statut:
ppublish
Résumé
Migraine is a neurological disorder and one of the most common pain conditions worldwide. Despite its prevalence, the basic biology and underlying mechanisms contributing to the development of migraine are still poorly understood. It is still unclear, for instance, whether the vasculature, both extra and intracranial, plays a significant role in the generation of migraine pain. Neuroimaging data, indeed, have reported conflicting results on blood vessels abnormalities like vasodilation, while functional studies suggest that vessels dysfunction may extend beyond vasodilation. Here we combined light and electron microscopy imaging to investigate the fine structure of superficial temporal (STA) and occipital arteries (OA) from patients that underwent minimally invasive surgery for migraine. Using optical microscopy, we observed that both STA and OA vessels showed marked endothelial thickening and internal elastic lamina fragmentation. In the muscular layer, we found profound shape changes of vascular smooth muscle cells (VSMCs), abundant extracellular matrix, and the presence of clear extracellular vacuoles. The electron microscopy analysis confirmed putative VSMCs infiltrated within the intima layer and revealed a consistent shifting of VSMCs from contractile to a synthetically active phenotype. We also report the presence of (i) abundant extracellular vacuoles filled with fine granular material and membranes, (ii) multilamellar structures, (iii) endosome-like organelles, and (iv) bona fide extracellular vesicles in the matrix space surrounding synthetically active cells. As both the endothelial layer and VSMCs coordinate a variety of vascular functions, these results suggest that a significant vascular remodeling is occurring in STA and OA of migraine patients. Thus, this phenomenon may represent an important target for future investigation designed toward the development of new therapeutic approaches.
Identifiants
pubmed: 35091837
doi: 10.1007/s00418-021-02066-w
pii: 10.1007/s00418-021-02066-w
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
459-465Subventions
Organisme : Università degli Studi di Genova
ID : 100008-2020-EC-FRA_001_FRA2020
Organisme : Università degli Studi di Genova
ID : D.R. 3404
Organisme : Università degli Studi di Genova
ID : Grant Heavy Equipment
Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Amin FM, Asghar MS, Hougaard A et al (2013) Magnetic resonance angiography of intracranial and extracranial arteries in patients with spontaneous migraine without aura: a cross-sectional study. Lancet Neurol 12:454–461. https://doi.org/10.1016/S1474-4422(13)70067-X
doi: 10.1016/S1474-4422(13)70067-X
pubmed: 23578775
Ashina M, Terwindt GM, Al-Karagholi MAM et al (2021) Migraine: disease characterisation, biomarkers, and precision medicine. Lancet 397:1496–1504. https://doi.org/10.1016/S0140-6736(20)32162-0
doi: 10.1016/S0140-6736(20)32162-0
pubmed: 33773610
Bertozzi N, Simonacci F, Lago GL et al (2018) Surgical therapy of temporal triggered migraine headache. Plast Reconstr Surg Glob Open 6:1–8. https://doi.org/10.1097/GOX.0000000000001980
doi: 10.1097/GOX.0000000000001980
Cavestro C, Degan D, Micca G et al (2021) Thrombophilic alterations, migraine, and vascular disease: results from a case-control study. Neurol Sci 42:3821–3828. https://doi.org/10.1007/s10072-020-05006-z
doi: 10.1007/s10072-020-05006-z
pubmed: 33471261
Eid RA, Radad K, Al-Shraim M (2012) Ultrastructural changes of smooth muscles in varicocele veins. Ultrastruct Path 36:201–206. https://doi.org/10.3109/01913123.2011.637663
doi: 10.3109/01913123.2011.637663
Eigenbrodt AK, Ashina H, Khan S et al (2021) Diagnosis and management of migraine in ten steps. Nat Rev Neurol 17:501–514
doi: 10.1038/s41582-021-00509-5
Gfrerer L, Raposio E, Ortiz R, Gerald Austen W (2018) Surgical treatment of migraine headache: back to the future. Plast Reconstr Surg 142:1036–1045. https://doi.org/10.1097/PRS.0000000000004795
doi: 10.1097/PRS.0000000000004795
pubmed: 30252818
Jacobs B, Dussor G (2016) Neurovascular contributions to migraine: moving beyond vasodilation. Neuroscience 338:130–144. https://doi.org/10.1016/j.neuroscience.2016.06.012
doi: 10.1016/j.neuroscience.2016.06.012
pubmed: 27312704
Kapustin AN, Shanahan CM (2016) Emerging roles for vascular smooth muscle cell exosomes in calcification and coagulation. J Physiol 594:2905–2914. https://doi.org/10.1113/JP271340
doi: 10.1113/JP271340
pubmed: 26864864
pmcid: 4887700
Lacolley P, Regnault V, Nicoletti A et al (2012) The vascular smooth muscle cell in arterial pathology: a cell that can take on multiple roles. Cardiovasc Res 95:194–204. https://doi.org/10.1093/cvr/cvs135
doi: 10.1093/cvr/cvs135
pubmed: 22467316
Mason BN, Russo AF (2018) Vascular contributions to migraine: Time to revisit? Front Cell Neurosci. https://doi.org/10.3389/FNCEL.2018.00233
doi: 10.3389/FNCEL.2018.00233
pubmed: 30498434
pmcid: 6249377
Øie LR, Øie LR, Kurth T et al (2020) Migraine and risk of stroke. J Neurol Neurosurg Psychiatry 91:593–604. https://doi.org/10.1136/jnnp-2018-318254
doi: 10.1136/jnnp-2018-318254
pubmed: 32217787
Omranifard M, Abdali H, Ardakani M, Talebianfar M (2016) A comparison of outcome of medical and surgical treatment of migraine headache: In 1 year follow-up. Adv Biomed Res. https://doi.org/10.4103/2277-9175.186994
doi: 10.4103/2277-9175.186994
pubmed: 27563631
pmcid: 4976529
Pahk K, Joung C, Jung SM et al (2017) Visualization of synthetic vascular smooth muscle cells in atherosclerotic carotid rat arteries by F-18 FDG PET. Sci Rep 7:1–8. https://doi.org/10.1038/s41598-017-07073-3
doi: 10.1038/s41598-017-07073-3
Petsophonsakul P, Furmanik M, Forsythe R et al (2019) Role of vascular smooth muscle cell phenotypic switching and calcification in aortic aneurysm formation involvement of Vitamin K-dependent processes. Arterioscler Thromb Vasc Biol 39:1351–1368. https://doi.org/10.1161/ATVBAHA.119.312787
doi: 10.1161/ATVBAHA.119.312787
pubmed: 31144989
Renna NF, de Las Heras N, Miatello RM (2013) Pathophysiology of vascular remodeling in hypertension. Int J Hypertens. https://doi.org/10.1155/2013/808353
doi: 10.1155/2013/808353
pubmed: 24228174
pmcid: 3818852
Rensen SSM, Doevendans PAFM, van Eys GJJM (2007) Regulation and characteristics of vascular smooth muscle cell phenotypic diversity. Neth Heart J 15:100–108. https://doi.org/10.1007/BF03085963
doi: 10.1007/BF03085963
pubmed: 17612668
pmcid: 1847757
Ripa P, Ornello R, Pistoia F et al (2015) Spreading depolarization may link migraine, stroke, and other cardiovascular disease. Headache 55:180–182. https://doi.org/10.1111/head.12436
doi: 10.1111/head.12436
pubmed: 25163584
Sacco S, Ripa P, Grassi D et al (2013) Peripheral vascular dysfunction in migraine: a review. J Headache Pain 14:80. https://doi.org/10.1186/1129-2377-14-80
doi: 10.1186/1129-2377-14-80
pubmed: 24083826
pmcid: 3849862
Salabei JK, Hill BG (2015) Autophagic regulation of smooth muscle cell biology. Redox Biol 4:97–103. https://doi.org/10.1016/j.redox.2014.12.007
doi: 10.1016/j.redox.2014.12.007
pubmed: 25544597
Sridharan G, Shankar AA (2012) Toluidine blue: a review of its chemistry and clinical utility. J Oral Maxillofac Pathol 16:251–255. https://doi.org/10.4103/0973-029X.99081
doi: 10.4103/0973-029X.99081
pubmed: 22923899
pmcid: 3424943
Sutherland HG, Albury CL, Griffiths LR (2019) Advances in genetics of migraine. J Headache Pain. https://doi.org/10.1186/s10194-019-1017-9
doi: 10.1186/s10194-019-1017-9
pubmed: 31226929
pmcid: 6734342
Trillo AA (1981) Formation of “ghost” bodies and calcification in experimental atherosclerosis in nonhuman primates—An Ultrastructural Study. Virchows Arch 38:127–139. https://doi.org/10.1007/BF02892808
doi: 10.1007/BF02892808