Purkinje cell loss in experimental autoimmune encephalomyelitis

NeuroImage

Volumn 48, Issue 4, 2009, Pages 637-651

  MacKenzie Graham, Allan ^a   Tiwari Woodruff, Seema K ^b   Sharma, Gaurav ^b   Aguilar, Cynthia ^a   Vo, Kieumai T ^a   Strickland, Lauren V ^a   Morales, Laurie ^b   Fubara, Boma ^c   Martin, Melanie ^d   Jacobs, Russell E ^e   Johnson, G Allan ^c   Toga, Arthur W ^a   Voskuhl, Rhonda R ^b  

^a Laboratory of Neuro Imaging   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c DUKE UNIVERSITY   (United States)

^d UNIVERSITY OF WINNIPEG   (Canada)

^e CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Cerebellum; Gray matter atrophy; Mouse; MRI; Multiple sclerosis

Indexed keywords

CASPASE 3;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ATROPHY; BRAIN CORTEX; BRAIN SIZE; CELL COUNT; CELL LOSS; CEREBELLUM; FEMALE; GRAY MATTER; HISTOPATHOLOGY; IMAGE QUALITY; MICROSCOPY; MOUSE; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PURKINJE CELL;

ANIMALS; ANTIGENS, CD45; APOPTOSIS; ATROPHY; BRAIN; CASPASE 3; CELL COUNT; CEREBELLUM; DEMYELINATING DISEASES; DISEASE MODELS, ANIMAL; ENCEPHALITIS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; MICE; MICE, INBRED C57BL; MULTIPLE SCLEROSIS; ORGAN SIZE; PURKINJE CELLS; TIME FACTORS;

EID: 69049097944     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2009.06.073     Document Type: Article

References (59)

1. Aktas O., Smorodchenko A., Brocke S., Infante-Duarte C., Schulze Topphoff U., Vogt J., Prozorovski T., Meier S., Osmanova V., Pohl E., Bechmann I., Nitsch R., and Zipp F. Neuronal damage in autoimmune neuroinflammation mediated by the death ligand TRAIL. Neuron 46 (2005) 421-432
2. Alusi S.H., Worthington J., Glickman S., and Bain P.G. A study of tremor in multiple sclerosis. Brain 124 (2001) 720-730
3. Bannerman P.G., Hahn A., Ramirez S., Morley M., Bonnemann C., Yu S., Zhang G.X., Rostami A., and Pleasure D. Motor neuron pathology in experimental autoimmune encephalomyelitis: studies in THY1-YFP transgenic mice. Brain 128 (2005) 1877-1886
4. Black J.A., Dib-Hajj S., Baker D., Newcombe J., Cuzner M.L., and Waxman S.G. Sensory neuron-specific sodium channel SNS is abnormally expressed in the brains of mice with experimental allergic encephalomyelitis and humans with multiple sclerosis. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 11598-11602
5. Black J.A., Liu S., Hains B.C., Saab C.Y., and Waxman S.G. Long-term protection of central axons with phenytoin in monophasic and chronic-relapsing EAE. Brain 129 (2006) 3196-3208
6. Camicioli R., Moore M.M., Kinney A., Corbridge E., Glassberg K., and Kaye J.A. Parkinson's disease is associated with hippocampal atrophy. Mov. Disord. 18 (2003) 784-790
7. Carter S.L., Muller M., Manders P.M., and Campbell I.L. Induction of the genes for Cxcl9 and Cxcl10 is dependent on IFN-gamma but shows differential cellular expression in experimental autoimmune encephalomyelitis and by astrocytes and microglia in vitro. Glia 55 (2007) 1728-1739
8. Chard D.T., Griffin C.M., Parker G.J., Kapoor R., Thompson A.J., and Miller D.H. Brain atrophy in clinically early relapsing-remitting multiple sclerosis. Brain 125 (2002) 327-337
9. Craner M.J., Kataoka Y., Lo A.C., Black J.A., Baker D., and Waxman S.G. Temporal course of upregulation of Na(v)1.8 in Purkinje neurons parallels the progression of clinical deficit in experimental allergic encephalomyelitis. J. Neuropathol. Exp. Neurol. 62 (2003) 968-975
10. Craner M.J., Newcombe J., Black J.A., Hartle C., Cuzner M.L., and Waxman S.G. Molecular changes in neurons in multiple sclerosis: altered axonal expression of Nav1.2 and Nav1.6 sodium channels and Na+/Ca2+ exchanger. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 8168-8173
11. Damarjian T.G., Craner M.J., Black J.A., and Waxman S.G. Upregulation and colocalization of p75 and Nav1.8 in Purkinje neurons in experimental autoimmune encephalomyelitis. Neurosci. Lett. 369 (2004) 186-190
12. Dutta R., McDonough J., Yin X., Peterson J., Chang A., Torres T., Gudz T., Macklin W.B., Lewis D.A., Fox R.J., Rudick R., Mirnics K., and Trapp B.D. Mitochondrial dysfunction as a cause of axonal degeneration in multiple sclerosis patients. Ann. Neurol. 59 (2006) 478-489
13. Edwards S.G., Gong Q.Y., Liu C., Zvartau M.E., Jaspan T., Roberts N., and Blumhardt L.D. Infratentorial atrophy on magnetic resonance imaging and disability in multiple sclerosis. Brain 122 Pt. 2 (1999) 291-301
14. Evangelou N., Esiri M.M., Smith S., Palace J., and Matthews P.M. Quantitative pathological evidence for axonal loss in normal appearing white matter in multiple sclerosis. Ann. Neurol. 47 (2000) 391-395
15. Farrar T.C., and Becker E.D. Pulse and Fourier Transform NMR (1971), Academic Press, New York
16. Firbank M.J., Blamire A.M., Krishnan M.S., Teodorczuk A., English P., Gholkar A., Harrison R., and O'Brien J.T. Atrophy is associated with posterior cingulate white matter disruption in dementia with Lewy bodies and Alzheimer's disease. NeuroImage 36 (2007) 1-7
17. Fisher E., Rudick R.A., Simon J.H., Cutter G., Baier M., Lee J.C., Miller D., Weinstock-Guttman B., Mass M.K., Dougherty D.S., and Simonian N.A. Eight-year follow-up study of brain atrophy in patients with MS. Neurology 59 (2002) 1412-1420
18. Floris S., Blezer E.L., Schreibelt G., Dopp E., van der Pol S.M., Schadee-Eestermans I.L., Nicolay K., Dijkstra C.D., and de Vries H.E. Blood-brain barrier permeability and monocyte infiltration in experimental allergic encephalomyelitis: a quantitative MRI study. Brain 127 (2004) 616-627
19. Fukushima E., and Roeder S.B.W. Experimental Pulse NMR (1981), Addison-Wesley, Reading, MA
20. Geurts J.J., and Barkhof F. Grey matter pathology in multiple sclerosis. Lancet Neurol. 7 (2008) 841-851
21. Ge Y., Grossman R.I., Udupa J.K., Wei L., Mannon L.J., Polansky M., and Kolson D.L. Brain atrophy in relapsing-remitting multiple sclerosis and secondary progressive multiple sclerosis: longitudinal quantitative analysis. Radiology 214 (2000) 665-670
22. Iannucci G., Minicucci L., Rodegher M., Sormani M.P., Comi G., and Filippi M. Correlations between clinical and MRI involvement in multiple sclerosis: assessment using T(1), T(2) and MT histograms. J. Neurol. Sci. 171 (1999) 121-129
23. Johnson G.A., Benveniste H., Black R.D., Hedlund L.W., Maronpot R.R., and Smith B.R. Histology by magnetic resonance microscopy. Magn. Reson. Q. 9 (1993) 1-30
24. Johnson G.A., Cofer G.P., Fubara B., Gewalt S.L., Hedlund L.W., and Maronpot R.R. Magnetic resonance histology for morphologic phenotyping. J. Magn. Reson. Imaging 16 (2002) 423-429
25. Johnson G.A., Cofer G.P., Gewalt S.L., and Hedlund L.W. Morphologic phenotyping with MR microscopy: the visible mouse. Radiology 222 (2002) 789-793
26. Kalkers N.F., Bergers E., Castelijns J.A., van Walderveen M.A., Bot J.C., Ader H.J., Polman C.H., and Barkhof F. Optimizing the association between disability and biological markers in MS. Neurology 57 (2001) 1253-1258
27. Kochunov P., Lancaster J.L., Thompson P., Woods R., Mazziotta J., Hardies J., and Fox P. Regional spatial normalization: toward an optimal target. J. Comput. Assist. Tomogr. 25 (2001) 805-816
28. Kuerten S., Kostova-Bales D.A., Frenzel L.P., Tigno J.T., Tary-Lehmann M., Angelov D.N., and Lehmann P.V. MP4- and MOG:35-55-induced EAE in C57BL/6 mice differentially targets brain, spinal cord and cerebellum. J. Neuroimmunol. 189 (2007) 31-40
29. Kutzelnigg A., Faber-Rod J.C., Bauer J., Lucchinetti C.F., Sorensen P.S., Laursen H., Stadelmann C., Bruck W., Rauschka H., Schmidbauer M., and Lassmann H. Widespread demyelination in the cerebellar cortex in multiple sclerosis. Brain Pathol. 17 (2007) 38-44
30. Lees J.R., Golumbek P.T., Sim J., Dorsey D., and Russell J.H. Regional CNS responses to IFN-gamma determine lesion localization patterns during EAE pathogenesis. J. Exp. Med. 205 (2008) 2633-2642
31. Liu C., Edwards S., Gong Q., Roberts N., and Blumhardt L.D. Three dimensional MRI estimates of brain and spinal cord atrophy in multiple sclerosis. J. Neurol. Neurosurg. Psychiatry 66 (1999) 323-330
32. Liu H.B., Loo K.K., Palaszynski K., Ashouri J., Lubahn D.B., and Voskuhl R.R. Estrogen receptor alpha mediates estrogen's immune protection in autoimmune disease. J. Immunol. 171 (2003) 6936-6940
33. MacKenzie-Graham A., Lee E.F., Dinov I.D., Bota M., Shattuck D.W., Ruffins S., Yuan H., Konstantinidis F., Pitiot A., Ding Y., Hu G., Jacobs R.E., and Toga A.W. A multimodal, multidimensional atlas of the C57BL/6J mouse brain. J. Anat. 204 (2004) 93-102
34. MacKenzie-Graham A., Tinsley M.R., Shah K.P., Aguilar C., Strickland L.V., Boline J., Martin M., Morales L., Shattuck D.W., Jacobs R.E., Voskuhl R.R., and Toga A.W. Cerebellar cortical atrophy in experimental autoimmune encephalomyelitis. NeuroImage 32 (2006) 1016-1023
35. Mauk M.D., Medina J.F., Nores W.L., and Ohyama T. Cerebellar function: coordination, learning or timing?. Curr. Biol. 10 (2000) R522-525
36. Melzer N., Meuth S.G., Torres-Salazar D., Bittner S., Zozulya A.L., Weidenfeller C., Kotsiari A., Stangel M., Fahlke C., and Wiendl H. A beta-lactam antibiotic dampens excitotoxic inflammatory CNS damage in a mouse model of multiple sclerosis. PLoS ONE 3 (2008) e3149
37. Muller D.M., Pender M.P., and Greer J.M. Blood-brain barrier disruption and lesion localisation in experimental autoimmune encephalomyelitis with predominant cerebellar and brainstem involvement. J. Neuroimmunol. 160 (2005) 162-169
38. Nicot A., Kurnellas M., and Elkabes S. Temporal pattern of plasma membrane calcium ATPase 2 expression in the spinal cord correlates with the course of clinical symptoms in two rodent models of autoimmune encephalomyelitis. Eur. J. Neurosci. 21 (2005) 2660-2670
39. Peterson J.W., Bo L., Mork S., Chang A., and Trapp B.D. Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Ann. Neurol. 50 (2001) 389-400
40. Pettinelli C.B., and McFarlin D.E. Adoptive transfer of experimental allergic encephalomyelitis in SJL/J mice after in vitro activation of lymph node cells by myelin basic protein: requirement for Lyt 1+ 2-T lymphocytes. J. Immunol. 127 (1981) 1420-1423
41. Rausch M., Hiestand P., Baumann D., Cannet C., and Rudin M. MRI-based monitoring of inflammation and tissue damage in acute and chronic relapsing EAE. Magn. Reson. Med. 50 (2003) 309-314
42. Renganathan M., Gelderblom M., Black J.A., and Waxman S.G. Expression of Nav1.8 sodium channels perturbs the firing patterns of cerebellar Purkinje cells. Brain Res. 959 (2003) 235-242
43. Rex D.E., Ma J.Q., and Toga A.W. The LONI Pipeline Processing Environment. NeuroImage 19 (2003) 1033-1048
44. Rudick R.A., Fisher E., Lee J.C., Simon J., and Jacobs L. Use of the brain parenchymal fraction to measure whole brain atrophy in relapsing-remitting MS. Multiple Sclerosis Collaborative Research Group. Neurology 53 (1999) 1698-1704
45. Selvaraj R.K., and Geiger T.L. Mitigation of experimental allergic encephalomyelitis by TGF-beta induced Foxp3+ regulatory T lymphocytes through the induction of anergy and infectious tolerance. J. Immunol. 180 (2008) 2830-2838
46. Shattuck D.W., and Leahy R.M. Automated graph-based analysis and correction of cortical volume topology. IEEE Trans. Med. Imag. 20 (2001) 1167-1177
47. Sled J.G., Zijdenbos A.P., and Evans A.C. A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans. Med. Imag. 17 (1998) 87-97
48. Stevenson V.L., Miller D.H., Leary S.M., Rovaris M., Barkhof F., Brochet B., Dousset V., Filippi M., Hintzen R., Montalban X., Polman C.H., Rovira A., de Sa J., and Thompson A.J. One year follow up study of primary and transitional progressive multiple sclerosis. J. Neurol. Neurosurg. Psychiatry 68 (2000) 713-718
49. Suen W.E., Bergman C.M., Hjelmstrom P., and Ruddle N.H. A critical role for lymphotoxin in experimental allergic encephalomyelitis. J. Exp. Med. 186 (1997) 1233-1240
50. Tonra J.R. Cerebellar susceptibility to experimental autoimmune encephalomyelitis in SJL/J mice: potential interaction of immunology with vascular anatomy. Cerebellum 1 (2002) 57-68
51. Tonra J.R., Reiseter B.S., Kolbeck R., Nagashima K., Robertson R., Keyt B., and Lindsay R.M. Comparison of the timing of acute blood-brain barrier breakdown to rabbit immunoglobulin G in the cerebellum and spinal cord of mice with experimental autoimmune encephalomyelitis. J. Comp. Neurol. 430 (2001) 131-144
52. Trapp B.D., Peterson J., Ransohoff R.M., Rudick R., Mork S., and Bo L. Axonal transection in the lesions of multiple sclerosis. N. Engl. J. Med. 338 (1998) 278-285
53. Trapp B.D., Ransohoff R., and Rudick R. Axonal pathology in multiple sclerosis: relationship to neurologic disability. Curr. Opin. Neurol. 12 (1999) 295-302
54. Uemura Y., Ohno H., Ohzeki Y., Takanashi H., Murooka H., Kubo K., and Serizawa I. The selective M-CSF receptor tyrosine kinase inhibitor Ki20227 suppresses experimental autoimmune encephalomyelitis. J. Neuroimmunol. 195 (2008) 73-80
55. Wang L., Wang R., and Herrup K. E2F1 works as a cell cycle suppressor in mature neurons. J. Neurosci. 27 (2007) 12555-12564
56. Waxman S.G. Cerebellar dysfunction in multiple sclerosis: evidence for an acquired channelopathy. Prog. Brain Res. 148 (2005) 353-365
57. Weinshenker B.G., Issa M., and Baskerville J. Long-term and short-term outcome of multiple sclerosis: a 3-year follow-up study. Arch. Neurol. 53 (1996) 353-358
58. Woods R.P., Grafton S.T., Holmes C.J., Cherry S.R., and Mazziotta J.C. Automated image registration: I. General methods and intrasubject, intramodality validation. J. Comput. Assist. Tomogr. V22 (1998) 139-152
59. Woods R.P., Grafton S.T., Watson J.D., Sicotte N.L., and Mazziotta J.C. Automated image registration: II. Intersubject validation of linear and nonlinear models. J. Comput. Assist. Tomogr. 22 (1998) 153-165