High-resolution diffusion tensor imaging of fixed brain in a mouse model of Pelizaeus-Merzbacher disease: Comparison with quantitative measures of white matter pathology

NMR in Biomedicine

Volumn 24, Issue 10, 2011, Pages 1369-1379

  Ruest, Torsten ^a   Holmes, William M ^a   Barrie, Jennifer A ^a   Griffiths, Ian R ^a   Anderson, Thomas J ^a   Dewar, Deborah ^a   Edgar, Julia M ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Histology; Myelin; Proteolipid protein

Indexed keywords

CELL DENSITY; CENTRAL NERVOUS SYSTEMS; CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; DIFFUSIVITIES; EX-VIVO; FRACTIONAL ANISOTROPY; GENE DUPLICATIONS; HIGH RESOLUTION; HISTOLOGICAL ANALYSIS; IN-VIVO; MOUSE MODELS; MYELIN; NON-INVASIVE ASSESSMENTS; QUANTITATIVE MEASURES; REGION OF INTEREST; ROI ANALYSIS; SPATIAL STATISTICS; TRANSGENIC MICE; TRANSGENICS; VOXEL-BASED APPROACHES; WATER DIFFUSION; WHITE MATTER; WHITE MATTER TRACTS; WILD TYPES;

ANISOTROPY; DIFFUSION; GENES; HISTOLOGY; IMAGE SEGMENTATION; MAGNETIC RESONANCE IMAGING; MAMMALS; NONINVASIVE MEDICAL PROCEDURES;

TENSORS;

MYELIN; PROTEOLIPID PROTEIN; PROTEOLIPID PROTEIN 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR COMMISSURE; ARTICLE; ASTROCYTOSIS; ATAXIA; BRAIN; CELL DENSITY; CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; FRACTIONAL ANISOTROPY; HIPPOCAMPAL FIMBRIA; HISTOLOGY; IN VIVO STUDY; MOUSE; NERVE FIBER; NEUROIMAGING; NONHUMAN; PELIZAEUS MERZBACHER DISEASE; PRIORITY JOURNAL; SEIZURE; TRANSGENIC MOUSE; WHITE MATTER; WILD TYPE;

AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; AXONS; BRAIN; CELL COUNT; DIFFUSION MAGNETIC RESONANCE IMAGING; DISEASE MODELS, ANIMAL; GLIAL FIBRILLARY ACIDIC PROTEIN; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYELIN BASIC PROTEINS; PELIZAEUS-MERZBACHER DISEASE;

MUS; MUS MUSCULUS;

EID: 84855306010     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.1700     Document Type: Article

References (53)

1. Beaulieu C. The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed. 2002; 15(7-8): 435-455.
2. Beaulieu C, Allen PS. Water diffusion in the giant axon of the squid: implications for diffusion-weighted MRI of the nervous system. Magn. Reson. Med. 1994; 32(5): 579-583.
3. Budde MD, Kim JH, Liang HF, Russell JH, Cross AH, Song SK. Axonal injury detected by in vivo diffusion tensor imaging correlates with neurological disability in a mouse model of multiple sclerosis. NMR Biomed. 2008; 21(6): 589-597.
4. Budde MD, Xie M, Cross AH, Song SK. Axial diffusivity is the primary correlate of axonal injury in the EAE spinal cord: a quantitative pixelwise analysis. J. Neurosci. 2009; 29(9): 2805-2813.
5. DeBoy CA, Zhang J, Dike S, Shats I, Jones M, Reich DS, Mori S, Nguyen T, Rothstein B, Miller RH, Griffin JT, Kerr DA, Calabresi PA. High resolution diffusion tensor imaging of axonal damage in focal inflammatory and demyelinating lesions in rat spinal cord. Brain, 2007; 130 (Pt 8): 2199-2210.
6. Sun SW, Liang HF, Schmidt RE, Cross AH, Song SK. Selective vulnerability of cerebral white matter in a murine model of multiple sclerosis detected using diffusion tensor imaging. Neurobiol. Dis. 2007; 28(1): 30-38.
7. Xie M, Tobin JE, Budde MD, Chen C-I, Trinkaus K, Cross AH, McDaniel DP, Song S-K, Armstrong RC. Rostrocaudal analysis of corpus callosum demyelination and axon damage across disease stages refines diffusion tensor imaging correlations with pathological features. J. Neuropathol. Exp. Neurol. 2010; 69(7): 704-716.
8. Mac Donald CL, Dikranian K, Song SK, Bayly PV, Holtzman DM, Brody DL. Detection of traumatic axonal injury with diffusion tensor imaging in a mouse model of traumatic brain injury. Exp. Neurol. 2007; 205(1): 116-131.
9. Hofling AA, Kim JH, Fantz CR, Sands MS, Song SK. Diffusion tensor imaging detects axonal injury and demyelination in the spinal cord and cranial nerves of a murine model of globoid cell leukodystrophy. NMR Biomed. 2009; 22(10): 1100-1106.
10. Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage, 2002; 17(3): 1429-1436.
11. Tyszka JM, Readhead C, Bearer EL, Pautler RG, Jacobs RE. Statistical diffusion tensor histology reveals regional dysmyelination effects in the shiverer mouse mutant. Neuroimage, 2006; 29(4): 1058-1065.
12. Inoue K. PLP1-related inherited dysmyelinating disorders: Pelizaeus-Merzbacher disease and spastic paraplegia type 2. Neurogenetics, 2005; 6(1): 1-16.
13. Hudson LDGJ, Kamholz JA. Chapter title. In: Lazzarini RA, Griffin JW, Lassmann H, Nave K-A, Miller RH, Trapp BD (eds). Pelizaeus-Merzbacher disease. Myelin Biology and Disorders. Elsevier Academic Press: San Diego, Calif.; 2004, pp. 867-885.
14. Cailloux F, Gauthier-Barichard F, Mimault C, Isabelle V, Courtois V, Giraud G, Dastugue B, Boespflug-Tanguy O. Genotype-phenotype correlation in inherited brain myelination defects due to proteolipid protein gene mutations. Clinical European Network on Brain Dysmyelinating Disease. Eur. J. Hum. Genet. 2000; 8(11): 837-845.
15. Mimault C, Giraud G, Courtois V, Cailloux F, Boire JY, Dastugue B, Boespflug-Tanguy O. Proteolipoprotein gene analysis in 82 patients with sporadic Pelizaeus-Merzbacher disease: duplications, the major cause of the disease, originate more frequently in male germ cells, but point mutations do not. The Clinical European Network on Brain Dysmyelinating Disease. Am. J. Hum. Genet. 1999; 65(2): 360-369.
16. Wolf NI, Sistermans EA, Cundall M, Hobson GM, Davis-Williams AP, Palmer R, Stubbs P, Davies S, Endziniene M, Wu Y, Chong WK, Malcolm S, Surtees R, Garbern JY, Woodward KJ. Three or more copies of the proteolipid protein gene PLP1 cause severe Pelizaeus-Merzbacher disease. Brain, 2005; 128 (Pt 4): 743-751.
17. Woodward K, Kendall E, Vetrie D, Malcolm S. Pelizaeus-Merzbacher disease: identification of Xq22 proteolipid-protein duplications and characterization of breakpoints by interphase FISH. Am. J. Hum. Genet. 1998; 63(1): 207-217.
18. Garbern J, Hobson G. Prenatal diagnosis of Pelizaeus-Merzbacher disease. Prenat. Diagn. 2002; 22(11): 1033-1035.
19. Garbern JY. Pelizaeus-Merzbacher disease: genetic and cellular pathogenesis. Cell Mol. Life Sci. 2007; 64(1): 50-65.
20. Garbern JY, Yool DA, Moore GJ, Wilds IB, Faulk MW, Klugmann M, Nave KA, Sistermans EA, van der Knaap MS, Bird TD, Shy ME, Kamholz JA, Griffiths IR. Patients lacking the major CNS myelin protein, proteolipid protein 1, develop length-dependent axonal degeneration in the absence of demyelination and inflammation. Brain, 2002; 125 (Pt 3): 551-561.
21. Harding B, Ellis D, Malcolm S. A case of Pelizaeus-Merzbacher disease showing increased dosage of the proteolipid protein gene. Neuropathol. Appl. Neurobiol. 1995; 21(2): 111-115.
22. Koeppen AH. A brief history of Pelizaeus-Merzbacher disease and proteolipid protein. J. Neurol. Sci. 2005; 228(2): 198-200.
23. Sima AA, Pierson CR, Woltjer RL, Hobson GM, Golden JA, Kupsky WJ, Schauer GM, Bird TD, Skoff RP, Garbern JY. Neuronal loss in Pelizaeus-Merzbacher disease differs in various mutations of the proteolipid protein 1. Acta Neuropathol. 2009; 118(4): 531-539.
24. Miller E, Widjaja E, Nilsson D, Yoon G, Banwell B, Blaser S. Magnetic resonance imaging of a unique mutation in a family with Pelizaeus-Merzbacher disease. Am. J. Med. Genet. A, 2010; 152A(3): 748-752.
25. Anderson TJ, Klugmann M, Thomson CE, Schneider A, Readhead C, Nave KA, Griffiths IR. Distinct phenotypes associated with increasing dosage of the PLP gene: implications for CMT1A due to PMP22 gene duplication. Ann. NY Acad. Sci. 1999; 883: 234-246.
26. Anderson TJ, Schneider A, Barrie JA, Klugmann M, McCulloch MC, Kirkham D, Kyriakides E, Nave KA, Griffiths IR. Late-onset neurodegeneration in mice with increased dosage of the proteolipid protein gene. J. Comp. Neurol. 1998; 394(4): 506-519.
27. Kagawa T, Ikenaka K, Inoue Y, Kuriyama S, Tsujii T, Nakao J, Nakajima K, Aruga J, Okano H, Mikoshiba K. Glial cell degeneration and hypomyelination caused by overexpression of myelin proteolipid protein gene. Neuron, 1994; 13(2): 427-442.
28. Readhead C, Schneider A, Griffiths I, Nave KA. Premature arrest of myelin formation in transgenic mice with increased proteolipid protein gene dosage. Neuron, 1994; 12(3): 583-595.
29. Ip CW, Kroner A, Bendszus M, Leder C, Kobsar I, Fischer S, Wiendl H, Nave K-A, Martini R. Immune cells contribute to myelin degeneration and axonopathic changes in mice overexpressing proteolipid protein in oligodendrocytes. J. Neurosci. 2006; 26(31): 8206-8216.
30. Gulani V, Webb AG, Duncan ID, Lauterbur PC. Apparent diffusion tensor measurements in myelin-deficient rat spinal cords. Magn. Reson. Med. 2001; 45(2): 191-195.
31. Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, Behrens TE. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage, 2006; 31(4): 1487-1505.
32. Cheng Y, Chou KH, Chen IY, Fan YT, Decety J, Lin CP. Atypical development of white matter microstructure in adolescents with autism spectrum disorders. Neuroimage, 2010; 50(3): 873-882.
33. Giorgio A, Palace J, Johansen-Berg H, Smith SM, Ropele S, Fuchs S, Wallner-Blazek M, Enzinger C, Fazekas F. Relationships of brain white matter microstructure with clinical and MR measures in relapsing-remitting multiple sclerosis. J. Magn. Reson. Imaging, 2010; 31(2): 309-316.
34. Liu Y, Spulber G, Lehtimaki KK, Kononen M, Hallikainen I, Grohn H, Kivipelto M, Hallikainen M, Vanninen R, Soininen H. Diffusion tensor imaging and tract-based spatial statistics in Alzheimer's disease and mild cognitive impairment. Neurobiol. Aging, 2009; [Epub ahead of print].
35. Woods RP, Grafton ST, Holmes CJ, Cherry SR, Mazziotta JC. Automated image registration: I. General methods and intrasubject, intramodality validation. J. Comput. Assist. Tomogr. 1998; 22(1): 139-152.
36. Woods RP, Grafton ST, Watson JD, Sicotte NL, Mazziotta JC. Automated image registration: II. Intersubject validation of linear and nonlinear models. J. Comput. Assist. Tomogr. 1998; 22(1): 153-165.
37. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE. Advances in functional and structural MR image analysis and implementation as FSL. Mathematics Brain Imaging, 2004; 23 (Supplement 1): S208.
38. Woolrich MW, Jbabdi S, Patenaude B, Chappell M, Makni S, Behrens T, Beckmann C, Jenkinson M, Smith SM. Bayesian analysis of neuroimaging data in FSL. Neuroimage, 2009; 45 (1 Suppl): S173-S186.
39. Nichols TE, Holmes AP. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum. Brain Mapp. 2002; 15(1): 1-25.
40. Smith SM, Johansen-Berg H, Jenkinson M, Rueckert D, Nichols TE, Miller KL, Robson MD, Jones DK, Klein JC, Bartsch AJ, Behrens TE. Acquisition and voxelwise analysis of multi-subject diffusion data with tract-based spatial statistics. Nat. Protoc. 2007; 2(3): 499-503.
41. Paxinos G, Franklin KBJ. The Mouse Brain in Stereotaxic Coordinates. Academic Press: San Diego; 2001.
42. Griffiths IR, Duncan ID, McCulloch M. Shaking pups: a disorder of central myelination in the spaniel dog. II. Ultrastructural observations on the white matter of the cervical spinal cord. J. Neurocytol. 1981; 10(5): 847-858.
43. Edgar JM, McCulloch MC, Montague P, Brown AM, Thilemann S, Pratola L, Gruenenfelder FI, Griffiths IR, Nave KA. Demyelination and axonal preservation in a transgenic mouse model of Pelizaeus-Merzbacher disease. EMBO Mol. Med. 2010; 2(2): 42-50.
44. Song SK, Sun SW, Ju WK, Lin SJ, Cross AH, Neufeld AH. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage, 2003; 20(3): 1714-1722.
45. Song S-K, Yoshino J, Le TQ, Lin S-J, Sun S-W, Cross AH, Armstrong RC. Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 2005; 26(1): 132.
46. Harsan LA, Poulet P, Guignard B, Parizel N, Skoff RP, Ghandour MS. Astrocytic hypertrophy in dysmyelination influences the diffusion anisotropy of white matter. J. Neurosci. Res. 2007; 85(5): 935-944.
47. Rosenbluth J. Central myelin in the mouse mutant shiverer. J. Comp. Neurol. 1980; 194(3): 639-648.
48. Sun SW, Liang HF, Cross AH, Song SK. Evolving Wallerian degeneration after transient retinal ischemia in mice characterized by diffusion tensor imaging. Neuroimage, 2008; 40(1): 1-10.
49. Sherriff FE, Bridges LR, Sivaloganathan S. Early detection of axonal injury after human head trauma using immunocytochemistry for beta-amyloid precursor protein. Acta Neuropathol. 1994; 87(1): 55-62.
50. Yam PS, Takasago T, Dewar D, Graham DI, McCulloch J. Amyloid precursor protein accumulates in white matter at the margin of a focal ischaemic lesion. Brain Res. 1997; 760(1-2): 150-157.
51. Coleman M. Axon degeneration mechanisms: commonality amid diversity. Nat. Rev. Neurosci. 2005; 6(11): 889-898.
52. Hassen WB, Begou M, Traore A, Moussa AB, Boehm N, Ghandour MS, Renou JP, Boespflug-Tanguy O, Bonny JM. Characterisation of spinal cord in a mouse model of spastic paraplegia related to abnormal axono-myelin interactions by in vivo quantitative MRI. Neuroimage, 2009; 46(1): 1-9.
53. Schwartz ED, Chin C-L, Shumsky JS, Jawad AF, Brown BK, Wehrli S, Tessler A, Murray M, Hackney DB. Apparent diffusion coefficients in spinal cord transplants and surrounding white matter correlate with degree of axonal dieback after injury in rats. Am. J. Neuroradiol. 2005; 26(1): 7-18.