RAFF-4, Magnetization Transfer and Diffusion Tensor MRI of Lysophosphatidylcholine Induced Demyelination and Remyelination in Rats

. 2021 ; 15 () : 625167. [epub] 20210304

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33746698

Grantová podpora
P41 EB027061 NIBIB NIH HHS - United States

Remyelination is a naturally occurring response to demyelination and has a central role in the pathophysiology of multiple sclerosis and traumatic brain injury. Recently we demonstrated that a novel MRI technique entitled Relaxation Along a Fictitious Field (RAFF) in the rotating frame of rank n (RAFFn) achieved exceptional sensitivity in detecting the demyelination processes induced by lysophosphatidylcholine (LPC) in rat brain. In the present work, our aim was to test whether RAFF4, along with magnetization transfer (MT) and diffusion tensor imaging (DTI), would be capable of detecting the changes in the myelin content and microstructure caused by modifications of myelin sheets around axons or by gliosis during the remyelination phase after LPC-induced demyelination in the corpus callosum of rats. We collected MRI data with RAFF4, MT and DTI at 3 days after injection (demyelination stage) and at 38 days after injection (remyelination stage) of LPC (n = 12) or vehicle (n = 9). Cell density and myelin content were assessed by histology. All MRI metrics detected differences between LPC-injected and control groups of animals in the demyelination stage, on day 3. In the remyelination phase (day 38), RAFF4, MT parameters, fractional anisotropy, and axial diffusivity detected signs of a partial recovery consistent with the remyelination evident in histology. Radial diffusivity had undergone a further increase from day 3 to 38 and mean diffusivity revealed a complete recovery correlating with the histological assessment of cell density attributed to gliosis. The combination of RAFF4, MT and DTI has the potential to differentiate between normal, demyelinated and remyelinated axons and gliosis and thus it may be able to provide a more detailed assessment of white matter pathologies in several neurological diseases.

Erratum v

PubMed

Zobrazit více v PubMed

Armstrong R. C., Mierzwa A. J., Marion C. M., Sullivan G. M. (2016a). White matter involvement after TBI: clues to axon and myelin repair capacity. Exp. Neurol. 275 328–333. 10.1016/j.expneurol.2015.02.011 PubMed DOI

Armstrong R. C., Mierzwa A. J., Sullivan G. M., Sanchez M. A. (2016b). Myelin and oligodendrocyte lineage cells in white matter pathology and plasticity after traumatic brain injury. Neuropharmacology 110 654–659. 10.1016/j.neuropharm.2015.04.029 PubMed DOI

Benjamini Y., Hochberg Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57 289–300. 10.1111/j.2517-6161.1995.tb02031.x DOI

Budde M. D., Janes L., Gold E., Turtzo L. C., Frank J. A. (2011). The contribution of gliosis to diffusion tensor anisotropy and tractography following traumatic brain injury: validation in the rat using Fourier analysis of stained tissue sections. Brain 134:2248. 10.1093/brain/awr161 PubMed DOI PMC

Chenevert T., Stegman L., Taylor J., Robertson P., Greenberg H., Rehemtulla A. (2000). Diffusion magnetic resonance imaging: an early surrogate marker of therapeutic efficacy in brain tumors. ı J. Natl. Cancer Inst. 92 2029–2036. 10.1093/jnci/92.24.2029 PubMed DOI

Dula A. N., Gochberg D. F., Valentine H. L., Valentine W. M., Does M. D. (2010). Multiexponential T2, magnetization transfer, and quantitative histology in white matter tracts of rat spinal cord. Magn. Reson. Med. 63 902–909. 10.1002/mrm.22267 PubMed DOI PMC

Franklin R. J. M., Ffrench-Constant C. (2008). Remyelination in the CNS: from biology to therapy. Nat. Rev. Neurosci. 9 839–855. 10.1038/nrn2480 PubMed DOI

Hakkarainen H., Sierra A., Mangia S., Garwood M., Michaeli S., Gröhn O., et al. (2016). MRI relaxation in the presence of fictitious fields correlates with myelin content in normal rat brain. Magn. Reson. Med. 75 161–168. 10.1002/mrm.25590 PubMed DOI PMC

Heath F., Hurley S. A., Johansen-Berg H., Sampaio-Baptista C. (2018). Advances in noninvasive myelin imaging. Dev. Neurobiol. 78 136–151. 10.1002/dneu.22552 PubMed DOI PMC

Hirano A. (1989). Review of the morphological aspects of remyelination. Dev. Neurosci. 11 112–117. 10.1159/000111892 PubMed DOI

Laitinen T., Sierra A., Pitkänen A., Gröhn O. (2010). Diffusion tensor MRI of axonal plasticity in the rat hippocampus. Neuroimage 51 521–530. 10.1016/j.neuroimage.2010.02.077 PubMed DOI

Leemans A., Jeurissen B., Sijbers J., Jones D. K. (2009). ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data. Proc. Intl. Soc. Mag. Reson. Med. 17.

Lehto L. J., Albors A. A., Sierra A., Tolppanen L., Eberly L. E., Mangia S., et al. (2017). Lysophosphatidyl choline induced demyelination in rat probed by relaxation along a fictitious field in high rank rotating frame. Front. Neurosci. 11:433. 10.3389/fnins.2017.00433 PubMed DOI PMC

Liimatainen T., Hakkarainen H., Mangia S., Huttunen J. M. J., Storino C., Idiyatullin D., et al. (2015). MRI contrasts in high rank rotating frames. Magn. Reson. Med. 73 254–262. 10.1002/mrm.25129 PubMed DOI PMC

Liimatainen T., Mangia S., Ling W., Ellermann J., Sorce D. J., Garwood M., et al. (2011). Relaxation dispersion in MRI induced by fictitious magnetic fields. J. Magn. Reson. 209 269–276. 10.1016/j.jmr.2011.01.022 PubMed DOI PMC

Liimatainen T., Sorce D. J., O’Connell R., Garwood M., Michaeli S. (2010). MRI contrast from relaxation along a fictitious field (RAFF). Magn. Reson. Med. 64 983–994. 10.1002/mrm.22372 PubMed DOI PMC

Luo T., Oladosu O., Rawji K. S., Zhai P., Pridham G., Hossain S., et al. (2019). Characterizing structural changes with evolving remyelination following experimental demyelination using high angular resolution diffusion MRI and texture analysis. J. Magn. Reson. Imaging 49 1750–1759. 10.1002/jmri.26328 PubMed DOI

Mangia S., Federico De F., Liimatainen T., Garwood M., Michaeli S. (2011). Magnetization transfer using inversion recovery during off-resonance irradiation. Magn. Reson. Imaging. 29 1346–1350. 10.1016/j.mri.2011.04.002 PubMed DOI PMC

Nasrabady S. E., Rizvi B., Goldman J. E., Brickman A. M. (2018). White matter changes in Alzheimer’s disease: a focus on myelin and oligodendrocytes. Acta Neuropathol. Commun. 6:22. PubMed PMC

Noseworthy J. H., Lucchinetti C., Rodriguez M., Weinshenker B. G. (2000). Multiple sclerosis. N. Engl. J. Med. 343 938–952. PubMed

Oluich L.-J., Stratton J. A. S., Xing Y. L., Ng S. W., Cate H. S., Sah P., et al. (2012). Targeted ablation of oligodendrocytes induces axonal pathology independent of overt demyelination. J. Neurosci. 32:8317. 10.1523/jneurosci.1053-12.2012 PubMed DOI PMC

Pfeiffer F., Frommer-Kaestle G., Fallier-Becker P. (2019). Structural adaption of axons during de- and remyelination in the Cuprizone mouse model. Brain Pathol. 29 675–692. 10.1111/bpa.12748 PubMed DOI PMC

Podbielska M., Banik N. L., Kurowska E., Hogan E. L. (2013). Myelin recovery in multiple sclerosis: the challenge of remyelination. Brain Sci. 3:1282. 10.3390/brainsci3031282 PubMed DOI PMC

Prineas J. W., Connell F. (1979). Remyelination in multiple sclerosis. Ann. Neurol. 5 22–31. PubMed

Raine C. (1984). “Morphology of myelin and myelination,” in Myelin, ed. Morell P. (Boston, MA: Springer; ), 1–50. 10.1007/978-1-4757-1830-0_1 DOI

Saab A., Nave K. (2017). Myelin dynamics: protecting and shaping neuronal functions. Curr. Opin. Neurobiol. 47 104–112. 10.1016/j.conb.2017.09.013 PubMed DOI

Satzer D., DiBartolomeo C., Ritchie M. M., Storino C., Liimatainen T., Hakkarainen H., et al. (2015). Assessment of dysmyelination with RAFFn MRI: application to murine MPS I. PLoS One 10:e0116788. 10.1371/journal.pone.0116788 PubMed DOI PMC

Seifert A. C., Li C., Wilhelm M. J., Wehrli S. L., Wehrli F. W. (2017). Towards quantification of myelin by solid-state MRI of the lipid matrix protons. Neuroimage 163 358–367. 10.1016/j.neuroimage.2017.09.054 PubMed DOI PMC

Song S.-K., Yoshino J., Le T., Lin S.-J., Sun S.-W., Cross A., et al. (2005). Demyelination increases radial diffusivity in corpus callosum of mouse brain. NeuroImage 26 132–140. 10.1016/j.neuroimage.2005.01.028 PubMed DOI

Tozer D. J., Davies G. R., Altmann D. R., Miller D. H., Tofts P. S. (2005). Correlation of apparent myelin measures obtained in multiple sclerosis patients and controls from magnetization transfer and multicompartmental T2 analysis. Magn. Reson. Med. 53 1415–1422. 10.1002/mrm.20479 PubMed DOI

van Zijl P., Lam W. W., Xu J., Knutsson L., Stanisz G. J. (2018). Magnetization transfer contrast and chemical exchange saturation transfer MRI. Features and analysis of the field-dependent saturation spectrum. Neuroimage 168 222–241. 10.1016/j.neuroimage.2017.04.045 PubMed DOI PMC

Waxman S. G., Kocsis J. D., Nitta K. C. (1979). Lysophosphatidyl choline-induced focal demyelination in the rabbit corpus callosum. Light-microscopic observations. J. Neurol. Sci. 44 45–53. 10.1016/0022-510x(79)90221-1 PubMed DOI

Wilhelm M. J., Ong H. H., Wehrli S. L., Li C., Tsai P.-H., Hackney D. B., et al. (2012). Direct magnetic resonance detection of myelin and prospects for quantitative imaging of myelin density. Proc. Natl. Acad. Sci. U.S.A. 109 9605–9610. 10.1073/pnas.1115107109 PubMed DOI PMC

Wolff S. D., Balaban R. S. (1989). Magnetization transfer contrast (MTC) and tissue water proton relaxation in vivo. Magn. Reson. Med. 10 135–144. 10.1002/mrm.1910100113 PubMed DOI

Woodruff R. H., Franklin R. J. M. (1999). Demyelination and remyelination of the caudal cerebellar peduncle of adult rats following stereotaxic injections of lysolecithin, ethidium bromide, and complement/anti-galactocerebroside: a comparative study. Glia 25 216–228. 10.1002/(sici)1098-1136(19990201)25:3<216::aid-glia2>3.0.co;2-l PubMed DOI

Zhao C., Fancy S. P. J., Kotter M. R., Li W.-W., Franklin R. J. M. (2005). Mechanisms of CNS Remyelination-the Key to therapeutic advances. J. Neurol. Sci 233 87–91. 10.1016/j.jns.2005.03.008 PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...