Increased occurrence of pathological mitochondria in astrocytic perivascular endfoot processes and neurons of idiopathic intracranial hypertension.
Adult
Astrocytes
/ ultrastructure
Biopsy
Cerebral Cortex
/ pathology
Endoplasmic Reticulum
/ ultrastructure
Female
Gliosis
/ etiology
Glymphatic System
/ ultrastructure
Humans
Male
Microscopy, Electron
Middle Aged
Mitochondria
/ pathology
Nerve Endings
/ ultrastructure
Neurons
/ ultrastructure
Post-Synaptic Density
/ ultrastructure
Prospective Studies
Pseudotumor Cerebri
/ complications
Single-Blind Method
Young Adult
astrocytes
electron microscopy
idiopathic intracranial hypertension
mitochondria
neurogliovascular unit
neurons
pseudotumor cerebri
reduced postsynaptic density
Journal
Journal of neuroscience research
ISSN: 1097-4547
Titre abrégé: J Neurosci Res
Pays: United States
ID NLM: 7600111
Informations de publication
Date de publication:
02 2021
02 2021
Historique:
received:
16
03
2020
revised:
29
09
2020
accepted:
01
10
2020
pubmed:
27
10
2020
medline:
15
12
2021
entrez:
26
10
2020
Statut:
ppublish
Résumé
Idiopathic intracranial hypertension (IIH) primarily affects fertile, overweight women, and presents with the symptoms of raised intracranial pressure. The etiology is unknown but has been thought to relate to cerebrospinal fluid disturbance or cerebral venous stenosis. We have previously found evidence that IIH is also a disease of the brain parenchyma, evidenced by alterations at the neurogliovascular interface, including astrogliosis, pathological changes in the basement membrane and pericytes, and alterations of perivascular aquaporin-4. The aim of this present electron microscopic study was to examine whether mitochondria phenotype was changed in IIH, particularly focusing on perivascular astrocytic endfeet and neurons (soma and pre- and postsynaptic terminals). Cortical brain biopsies of nine reference individuals and eight IIH patients were analyzed for subcellular distribution and phenotypical features of mitochondria using transmission electron microscopy. We found significantly increased prevalence of pathological mitochondria and reduced number of normal mitochondria in astrocytic endfeet of IIH patients. The degree of astrogliosis correlated negatively with the number of normal mitochondria in astrocytic endfoot processes. Moreover, we found significantly increased number of pathological mitochondria in pre- and postsynaptic neuronal terminals, as well as significantly shortened distance between mitochondria and endoplasmic reticulum contacts. Finally, the length of postsynaptic density, a marker of synaptic strength, was on average reduced in IIH. The present data provide evidence of pathological mitochondria in perivascular astrocytes endfeet and neurons of IIH patients, highlighting that impaired metabolism at the neurogliovascular interface may be a facet of IIH.
Identifiants
pubmed: 33105056
doi: 10.1002/jnr.24743
pmc: PMC7821105
doi:
Types de publication
Journal Article
Observational Study
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
467-480Informations de copyright
© 2020 The Authors. Journal of Neuroscience Research published by Wiley Periodicals LLC.
Références
World Neurosurg. 2011 May-Jun;75(5-6):648-52; discussion 592-5
pubmed: 21704931
Physiol Rev. 2018 Jan 1;98(1):239-389
pubmed: 29351512
Glia. 2017 Feb;65(2):293-308
pubmed: 27785828
Clin Neurol Neurosurg. 2011 Feb;113(2):123-8
pubmed: 21075509
Endocrinology. 2014 Aug;155(8):2858-67
pubmed: 24914942
J Neurol Neurosurg Psychiatry. 2016 Sep;87(9):982-92
pubmed: 26888960
Methods Mol Biol. 2012;814:23-45
pubmed: 22144298
J Clin Endocrinol Metab. 2007 Aug;92(8):3278-84
pubmed: 17536002
Stroke. 2002 Mar;33(3):816-24
pubmed: 11872909
J Neuropathol Exp Neurol. 2019 Sep 1;78(9):808-818
pubmed: 31393574
Eur J Neurol. 2014 Aug;21(8):1055-1059
pubmed: 24698554
J Neurosurg. 2017 Apr;126(4):1312-1322
pubmed: 27341045
Trends Neurosci. 2016 Mar;39(3):146-157
pubmed: 26899735
Eur Arch Otorhinolaryngol. 2009 Jun;266(6):803-6
pubmed: 19352689
J Neurol Neurosurg Psychiatry. 2018 Oct;89(10):1088-1100
pubmed: 29903905
Proc Natl Acad Sci U S A. 2010 Aug 17;107(33):14875-80
pubmed: 20679202
J Neurosci Res. 2017 Nov;95(11):2253-2266
pubmed: 28833444
Mol Cell Neurosci. 2016 Oct;76:68-75
pubmed: 27567688
Neuron. 2008 Jan 24;57(2):178-201
pubmed: 18215617
Brain Res. 2016 Aug 1;1644:161-75
pubmed: 27188961
DNA Cell Biol. 2015 Apr;34(4):261-73
pubmed: 25664381
J Neurosci Res. 2021 Feb;99(2):467-480
pubmed: 33105056
Cell Death Differ. 2016 Sep 1;23(9):1417-27
pubmed: 27341186
J Neuropathol Exp Neurol. 2017 Dec 1;76(12):1034-1045
pubmed: 29040647
Nat Rev Neurosci. 2003 Dec;4(12):991-1001
pubmed: 14682361
Sci Transl Med. 2012 Aug 15;4(147):147ra111
pubmed: 22896675
Neurology. 2002 Nov 26;59(10):1492-5
pubmed: 12455560
J Neurosci. 1985 Dec;5(12):3161-8
pubmed: 4078621
Front Neurosci. 2014 May 09;8:103
pubmed: 24847203
Ann Otol Rhinol Laryngol. 2015 Dec;124(12):996-1001
pubmed: 26082474
Front Neurosci. 2017 Apr 21;11:224
pubmed: 28484368
Physiol Rev. 2014 Oct;94(4):1077-98
pubmed: 25287860
Neurology. 2000 Jan 25;54(2):319-24
pubmed: 10668690
Brain Behav Immun. 2016 Jan;51:230-239
pubmed: 26336035
Neurobiol Aging. 2016 Dec;48:34-47
pubmed: 27639119
Biochim Biophys Acta Mol Basis Dis. 2018 Oct;1864(10):3247-3256
pubmed: 30006151
Behav Neurol. 2011;24(2):143-8
pubmed: 21606575
Nature. 2004 Sep 9;431(7005):195-9
pubmed: 15356633
Neuron. 2017 Sep 27;96(1):17-42
pubmed: 28957666
Lancet Neurol. 2006 May;5(5):433-42
pubmed: 16632314
BMJ. 2010 Jul 07;341:c2701
pubmed: 20610512
Cell Discov. 2017 Mar 28;3:17005
pubmed: 28377822
Acta Neuropathol Commun. 2018 Oct 1;6(1):102
pubmed: 30270816
Brain Behav. 2017 Mar 28;7(5):e00677
pubmed: 28523220
Brain Res. 2018 May 1;1686:72-82
pubmed: 29477544
Neuropathol Appl Neurobiol. 2018 Aug;44(5):474-490
pubmed: 28627088
Brain Plast. 2018 Aug 10;3(2):129-144
pubmed: 30151338
J Cell Biol. 1998 Nov 2;143(3):777-94
pubmed: 9813097
Glia. 2010 Jul;58(9):1094-103
pubmed: 20468051
BMJ Open. 2014 Apr 08;4(4):e004376
pubmed: 24713214
Front Mol Neurosci. 2019 Feb 22;12:40
pubmed: 30853890
Cells. 2018 Dec 21;8(1):
pubmed: 30577576
Neurosurgery. 2005 Jul;57(1):97-108; discussion 97-108
pubmed: 15987545
Hum Mol Genet. 2016 Feb 15;25(4):792-806
pubmed: 26721933
Neuron. 2005 Aug 4;47(3):331-3
pubmed: 16055057
Glia. 2017 Jun;65(6):964-973
pubmed: 28317216
J Cell Sci. 2019 Oct 22;132(20):
pubmed: 31515277
Proc Natl Acad Sci U S A. 2010 Sep 14;107(37):16325-30
pubmed: 20736350
Acta Neuropathol. 2018 Mar;135(3):311-336
pubmed: 29411111
Nat Rev Neurosci. 2012 Jan 05;13(2):77-93
pubmed: 22218207
Obes Rev. 2011 May;12(5):e372-80
pubmed: 20804521
Neurology. 2013 Jul 23;81(4):379-82
pubmed: 23794685
Acta Neuropathol Commun. 2019 May 2;7(1):68
pubmed: 31046837
Neurosurgery. 2010 Jan;66(1):80-91
pubmed: 20023540
Ann Surg. 1937 Oct;106(4):492-513
pubmed: 17857053
J Neurosci Methods. 2017 Jul 15;286:31-37
pubmed: 28527623
J Alzheimers Dis. 2006 Jul;9(2):119-26
pubmed: 16873959
Proc Natl Acad Sci U S A. 2005 Jan 25;102(4):1193-8
pubmed: 15657133
Fluids Barriers CNS. 2019 Dec 18;16(1):39
pubmed: 31849332
J Neuropathol Exp Neurol. 2012 Sep;71(9):814-25
pubmed: 22878665
Scanning Microsc Suppl. 1989;3:57-63; discussion 63-4
pubmed: 2694274
J Neurol Neurosurg Psychiatry. 2014 Sep;85(9):959-64
pubmed: 24474821
Antioxid Redox Signal. 2011 May 15;14(10):1939-51
pubmed: 21128700
J Neurosci. 2010 Aug 11;30(32):10851-9
pubmed: 20702714
World Neurosurg. 2016 Feb;86:186-193.e1
pubmed: 26428326
Eur J Neurol. 2011 Oct;18(10):1266-8
pubmed: 21426442