Nanostructure-specific X-ray tomography reveals myelin levels, integrity and axon orientations in mouse and human nervous tissue.
Animals
Axons
/ metabolism
Brain
/ metabolism
Central Nervous System
/ diagnostic imaging
Child, Preschool
Female
Humans
Magnetic Resonance Imaging
/ methods
Male
Mice
Mice, Inbred C57BL
Mice, Knockout
Myelin Proteins
/ metabolism
Myelin Sheath
/ metabolism
Nanostructures
/ chemistry
Neuroimaging
/ methods
Proof of Concept Study
Scattering, Small Angle
Spinal Cord
/ metabolism
Tomography, X-Ray Computed
/ methods
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
19 05 2021
19 05 2021
Historique:
received:
13
07
2020
accepted:
24
03
2021
entrez:
20
5
2021
pubmed:
21
5
2021
medline:
1
6
2021
Statut:
epublish
Résumé
Myelin insulates neuronal axons and enables fast signal transmission, constituting a key component of brain development, aging and disease. Yet, myelin-specific imaging of macroscopic samples remains a challenge. Here, we exploit myelin's nanostructural periodicity, and use small-angle X-ray scattering tensor tomography (SAXS-TT) to simultaneously quantify myelin levels, nanostructural integrity and axon orientations in nervous tissue. Proof-of-principle is demonstrated in whole mouse brain, mouse spinal cord and human white and gray matter samples. Outcomes are validated by 2D/3D histology and compared to MRI measurements sensitive to myelin and axon orientations. Specificity to nanostructure is exemplified by concomitantly imaging different myelin types with distinct periodicities. Finally, we illustrate the method's sensitivity towards myelin-related diseases by quantifying myelin alterations in dysmyelinated mouse brain. This non-destructive, stain-free molecular imaging approach enables quantitative studies of myelination within and across samples during development, aging, disease and treatment, and is applicable to other ordered biomolecules or nanostructures.
Identifiants
pubmed: 34011929
doi: 10.1038/s41467-021-22719-7
pii: 10.1038/s41467-021-22719-7
pmc: PMC8134484
doi:
Substances chimiques
Myelin Proteins
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
2941Subventions
Organisme : NIA NIH HHS
ID : R01 AG061120
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA016087
Pays : United States
Organisme : NIH HHS
ID : S10 OD012331
Pays : United States
Organisme : NIGMS NIH HHS
ID : P41 GM111244
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS088040
Pays : United States
Organisme : NIGMS NIH HHS
ID : P41 GM103393
Pays : United States
Organisme : NIBIB NIH HHS
ID : P41 EB017183
Pays : United States
Organisme : NIH HHS
ID : S10 OD021512
Pays : United States
Organisme : NIA NIH HHS
ID : P30 AG066512
Pays : United States
Commentaires et corrections
Type : CommentIn
Références
Proc Natl Acad Sci U S A. 2007 Jul 10;104(28):11796-801
pubmed: 17586684
Brain Plast. 2016 Dec 21;2(1):71-91
pubmed: 29765849
J Appl Crystallogr. 2017 Mar 07;50(Pt 2):462-474
pubmed: 28381972
Nature. 2015 Nov 19;527(7578):353-6
pubmed: 26581292
Neuroimage. 2020 Jan 1;204:116214
pubmed: 31568873
Proc Natl Acad Sci U S A. 2010 Feb 23;107(8):3834-9
pubmed: 20133720
Sci Adv. 2020 Jun 12;6(24):eaba4171
pubmed: 32582855
J Synchrotron Radiat. 2020 Jan 1;27(Pt 1):164-175
pubmed: 31868749
Proc Natl Acad Sci U S A. 2011 May 17;108(20):8293-8
pubmed: 21527720
Sci Rep. 2016 Sep 15;6:33079
pubmed: 27629394
Neuroimage. 2017 Feb 15;147:253-261
pubmed: 27986605
J Comp Neurol. 1978 Jan 1;177(1):1-9
pubmed: 618435
Acta Crystallogr A Found Adv. 2019 Mar 1;75(Pt 2):223-238
pubmed: 30821257
Front Integr Neurosci. 2013 Feb 01;7:3
pubmed: 23378830
Neuroimage. 2015 May 1;111:192-203
pubmed: 25665963
Proc Natl Acad Sci U S A. 1984 Mar;81(6):1871-4
pubmed: 6584921
Neuroimage. 2016 Nov 15;142:394-406
pubmed: 27523449
Neurosci Lett. 1979 Apr;12(1):107-12
pubmed: 460693
Nat Protoc. 2014 Jul;9(7):1682-97
pubmed: 24945384
Nat New Biol. 1971 May 12;231(19):46-52
pubmed: 5283387
Neuroscience. 2019 Apr 1;403:79-92
pubmed: 28579146
Nature. 2015 Nov 19;527(7578):349-52
pubmed: 26581291
Magn Reson Med. 2016 Nov;76(5):1582-1593
pubmed: 26599599
Neuroimage. 2008 Aug 1;42(1):60-9
pubmed: 18502665
Acta Neuropathol. 1983;61(3-4):178-82
pubmed: 6650131
Acta Crystallogr A Found Adv. 2018 Jan 1;74(Pt 1):12-24
pubmed: 29269594
Neuroimage. 2021 Mar;228:117692
pubmed: 33385546
AJNR Am J Neuroradiol. 2016 Aug;37(8):1384-92
pubmed: 26892985
J Biophys Biochem Cytol. 1957 Sep 25;3(5):725-48
pubmed: 13475388
Physiol Rev. 2019 Jul 1;99(3):1381-1431
pubmed: 31066630
Exp Neurol. 2017 May;291:74-86
pubmed: 28163160
Cortex. 2013 Oct;49(9):2569-82
pubmed: 23347559
J Struct Biol. 2009 Dec;168(3):521-6
pubmed: 19576284
Neuroimage. 2018 Dec;183:532-543
pubmed: 30077743
Biochim Biophys Acta. 1969 Apr;173(3):419-26
pubmed: 5769639
Acta Physiol Scand. 1961 Feb-Mar;51:290-5
pubmed: 13715156
J Neurocytol. 2002 Sep-Nov;31(8-9):581-93
pubmed: 14501200
Neuroimage. 2011 Jul 1;57(1):124-129
pubmed: 21514390
J Neuropathol Exp Neurol. 1988 May;47(3):217-34
pubmed: 3367155
Eye Brain. 2014 Sep;2014(6 Suppl 1):5-18
pubmed: 25788835
Proc Natl Acad Sci U S A. 2010 Sep 7;107(36):15676-80
pubmed: 20720164
Neuroimage. 2011 Sep 1;58(1):177-88
pubmed: 21699989
J Cell Biol. 1979 Jul;82(1):140-9
pubmed: 479295
NMR Biomed. 2019 Apr;32(4):e3998
pubmed: 30321478
Prog Neurobiol. 1992;38(3):261-316
pubmed: 1546164
Acta Neuropathol Commun. 2018 Mar 2;6(1):22
pubmed: 29499767
NMR Biomed. 2010 Aug;23(7):698-710
pubmed: 20632416
NMR Biomed. 2016 Dec;29(12):1729-1738
pubmed: 27753154
Dev Neurobiol. 2018 Feb;78(2):136-151
pubmed: 29082667
J Neuropathol Exp Neurol. 1987 May;46(3):283-301
pubmed: 3559630
Magn Reson Med. 2008 Dec;60(6):1396-407
pubmed: 19025906