Early MRI changes in a mouse model of multiple sclerosis are predictive of severe inflammatory tissue damage

Brain

Volumn 130, Issue 8, 2007, Pages 2186-2198

  Nessler, Stefan ^a,b   Boretius, Susann ^c   Stadelmann, Christine ^d   Bittner, Alwina ^e   Merkler, Doron ^d   Hartung, Hans Peter ^a   Michaelis, Thomas ^c   Brück, Wolfgang ^d   Frahm, Jens ^c   Sommer, Norbert ^e   Hemmer, Bernhard ^a,b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c Biomedizinische NMR Forschungs GmbH   (Germany)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

^e PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Experimental autoimmune encephalomyelitis (EAE); Histopathology; Magnetic resonance imaging (MRI); Multiple sclerosis; T cell clone

Indexed keywords

IMMUNOGLOBULIN; MYELIN;

ANIMAL MODEL; ARTICLE; BRAIN DAMAGE; CELL INFILTRATION; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; HISTOPATHOLOGY; IMMUNOGLOBULIN DEPOSITION; IN VITRO STUDY; MICROGLIA; MOUSE; MULTIPLE SCLEROSIS; NERVE FIBER; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; TISSUE INJURY;

EID: 34547789342     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awm105     Document Type: Article

References (58)

1. Abromson-Leeman S, Bronson R, Luo Y, Berman M, Leeman R, Leeman J, et al. T-cell properties determine disease site, clinical presentation, and cellular pathology of experimental autoimmune encephalomyelitis. Am J Pathol 2004; 165: 1519-33.
2. Anderson SA, Shukaliak-Quandt J, Jordan EK, Arbab AS, Martin R, McFarland H, et al. Magnetic resonance imaging of labeled T cells in a mouse model of multiple sclerosis. Ann Neurol 2004; 55: 654-9.
3. Bakshi R, Shaikh ZA, Janardhan V. MRI T2 shortening ('black T2') in multiple sclerosis: frequency, location, and clinical correlation. Neuroreport 2000; 11: 15-21.
4. Barkhof F. The clinico-radiological paradox in multiple sclerosis revisited. Curr Opin Neurol 2002; 15: 239-45.
5. Barkhof F, Bruck W, De Groot CJ, Bergers E, Hulshof S, Geurts J, et al. Remyelinated lesions in multiple sclerosis: magnetic resonance image appearance. Arch Neurol 2003; 60: 1073-81.
6. Bell RB, Lindsey JW, Sobel RA, Hodgkinson S, Steinman L. Diverse T cell receptor V beta gene usage in the central nervous system in experimental allergic encephalomyelitis. J Immunol 1993; 150: 4085-92.
7. Bitsch A, Kuhlmann T, Stadelmann C, Lassmann H, Lucchinetti C, Bruck W. A longitudinal MRI study of histopathologically defined hypointense multiple sclerosis lesions. Ann Neurol 2001; 49: 793-6.
8. Blezer EL, Bauer J, Brok HP, Nicolay K, 't Hart BA. Quantitative MRI-pathology correlations of brain white matter lesions developing in a non-human primate model of multiple sclerosis. NMR Biomed 2007; 20: 90-103.
9. Boretius S, Schmelting B, Watanabe T, Merkler D, Tammer R, Czeh B, et al. Monitoring of EAE onset and progression in the common marmoset monkey by sequential high-resolution 3D MRI. NMR Biomed 2006; 19: 41-9.
10. Broom KA, Anthony DC, Blamire AM, Waters S, Styles P, Perry VH, et al. MRI reveals that early changes in cerebral blood volume precede bloodbrain barrier breakdown and overt pathology in MS-like lesions in rat brain. J Cereb Blood Flow Metab 2005; 25: 204-16.
11. Bruck W, Bitsch A, Kolenda H, Bruck Y, Stiefel M, Lassmann H. Inflammatory central nervous system demyelination: correlation of magnetic resonance imaging findings with lesion pathology. Ann Neurol 1997; 42: 783-93.
12. Carrier DA, Mawad ME, Kirkpatrick JB, Schmid MF. Metastatic adenocarcinoma to the brain: MR with pathologic correlation. AJNR Am J Neuroradiol 1994; 15: 155-9.
13. De Groot CJ, Bergers E, Kamphorst W, Ravid R, Polman CH, Barkhof F, et al. Post-mortem MRI-guided sampling of multiple sclerosis brain lesions: increased yield of active demyelinating and (p)reactive lesions. Brain 2001; 124: 1635-45.
14. Drayer BP, Burger P, Hurwitz B, Dawson D, Cain J, Leong J, et al. Magnetic resonance imaging in multiple sclerosis: decreased signal in thalamus and putamen. Ann Neurol 1987; 22: 546-50.
15. Duckers HJ, Muller HJ, Verhaagen J, Nicolay K, Gispen WH. Longitudinal in vivo magnetic resonance imaging studies in experimental allergic encephalomyelitis: effect of a neurotrophic treatment on cortical lesion development. Neuroscience 1997; 77: 1163-73.
16. Fazekas F, Barkhof F, Filippi M, Grossman RI, Li DK, McDonald WI, et al. The contribution of magnetic resonance imaging to the diagnosis of multiple sclerosis. Neurology 1999; 53: 448-56.
17. Filippi M, Paty DW, Kappos L, Barkhof F, Compston DA, Thompson AJ, et al. Correlations between changes in disability and T2-weighted brain MRI activity in multiple sclerosis: a follow-up study. Neurology 1995; 45: 255-60.
18. Filippi M, Tortorella C, Rovaris M. Magnetic resonance imaging of multiple sclerosis. J Neuroimaging 2002; 12: 289-301.
19. Frohman EM, Racke MK, Raine CS. Multiple sclerosis-the plaque and its pathogenesis. N Engl J Med 2006; 354: 942-55.
20. Gold R, Linington C, Lassmann H. Understanding pathogenesis and therapy of multiple sclerosis via animal models: 70 years of merits and culprits in experimental autoimmune encephalomyelitis research. Brain 2006; 129: 1953-71.
21. Grossman RI, Lisak RP, Macchi PJ, Joseph PM. MR of acute experimental allergic encephalomyelitis. AJNR Am J Neuroradiol 1987; 8: 1045-8.
22. Hart BA, Bauer J, Muller HJ, Melchers B, Nicolay K, Brok H, et al. Histopathological characterization of magnetic resonance imagingdetectable brain white matter lesions in a primate model of multiple sclerosis: a correlative study in the experimental autoimmune encephalomyelitis model in common marmosets (Callithrix jacchus). Am J Pathol 1998; 153: 649-63.
23. Hawkins CP, Munro PM, MacKenzie F, Kesselring J, Tofts PS, du Boulay EP, et al. Duration and selectivity of blood-brain barrier breakdown in chronic relapsing experimental allergic encephalomyelitis studied by gadolinium-DTPA and protein markers. Brain 1990; 113 (Pt 2): 365-78.
24. Hemmer B, Nessler S, Zhou D, Kieseier B, Hartung HP. Immunopathogenesis and immunotherapy of multiple sclerosis. Nat Clin Pract Neurol 2006; 2: 201-11.
25. Hiehle JF Jr, Grossman RI, Ramer KN, Gonzalez-Scarano F, Cohen JA. Magnetization transfer effects in MR-detected multiple sclerosis lesions: comparison with gadolinium-enhanced spin-echo images and nonenhanced T1-weighted images. AJNR Am J Neuroradiol 1995; 16: 69-77.
26. Jordan EK, McFarland HI, Lewis BK, Tresser N, Gates MA, Johnson M, et al. Serial MR imaging of experimental autoimmune encephalomyelitis induced by human white matter or by chimeric myelin-basic and proteolipid protein in the common marmoset. AJNR Am J Neuroradiol 1999; 20: 965-76.
27. Kalkers NF, Bergers E, Castelijns JA, van Walderveen MA, Bot JC, Ader HJ, et al. Optimizing the association between disability and biological markers in MS. Neurology 2001; 57: 1253-8.
28. Kim TK, Chang KH, Kim CJ, Goo JM, Kook MC, Han MH. Intracranial tuberculoma: comparison of MR with pathologic findings. AJNR Am J Neuroradiol 1995; 16: 1903-8.
29. Koeller KK, Smirniotopoulos JG, Jones RV. Primary central nervous system lymphoma: radiologic-pathologic correlation. Radiographics 1997; 17: 1497-526.
30. Kornek B, Lassmann H. Neuropathology of multiple sclerosis-new concepts. Brain Res Bull 2003; 61: 321-6.
31. Landtblom AM, Sjoqvist L, Soderfeldt B, Nyland H, Thuomas KA. Proton MR spectroscopy and MR imaging in acute and chronic multiple sclerosis-ringlike appearances in acute plaques. Acta Radiol 1996; 37: 278-87.
32. Lassmann H. Multiple sclerosis pathology: evolution of pathogenetic concepts. Brain Pathol 2005; 15: 217-22.
33. Levesque I, Sled JG, Narayanan S, Santos AC, Brass SD, Francis SJ, et al. The role of edema and demyelination in chronic T1 black holes: a quantitative magnetization transfer study. J Magn Reson Imaging 2005; 21: 103-10.
34. Ludwin SK. The pathogenesis of multiple sclerosis: relating human pathology to experimental studies. J Neuropathol Exp Neurol 2006; 65: 305-18.
35. Maatta JA, Sjoholm UR, Nygardas PT, Salmi AA, Hinkkanen AE. Neutrophils secreting tumor necrosis factor alpha infiltrate the central nervous system of BALB/c mice with experimental autoimmune encephalomyelitis. J Neuroimmunol 1998; 90: 162-75.
36. Miller DH, Rudge P, Johnson G, Kendall BE, Macmanus DG, Moseley IF, et al. Serial gadolinium enhanced magnetic resonance imaging in multiple sclerosis. Brain 1988; 111 (Pt 4): 927-39.
37. Morrissey SP, Stodal H, Zettl U, Simonis C, Jung S, Kiefer R, et al. In vivo MRI and its histological correlates in acute adoptive transfer experimental allergic encephalomyelitis. Quantification of inflammation and oedema. Brain 1996; 119 (Pt 1): 239-48.
38. Mottershead JP, Schmierer K, Clemence M, Thornton JS, Scaravilli F, Barker GJ, et al. High field MRI correlates of myelin content and axonal density in multiple sclerosis-a post-mortem study of the spinal cord. J Neurol 2003; 250: 1293-301.
39. Natt O, Watanabe T, Boretius S, Radulovic J, Frahm J, Michaelis T. High-resolution 3D MRI of mouse brain reveals small cerebral structures in vivo. J Neurosci Methods 2002; 120: 203-9.
40. Nessler S, Stadelmann C, Bittner A, Schlegel K, Gronen F, Bruck W, et al. Suppression of autoimmune encephalomyelitis by a neurokinin-1 receptor antagonist - a putative role for substance P in CNS inflammation. J Neuroimmunol 2006; 179: 1-8.
41. Noseworthy JH, Lucchinetti C, Rodriguez M, Weinshenker BG. Multiple sclerosis. N Engl J Med 2000; 343: 938-52.
42. Pirko I, Johnson A, Ciric B, Games J, Macura SI, Pease LR, et al. In vivo magnetic resonance imaging of immune cells in the central nervous system with superparamagnetic antibodies. FASEB J 2004; 18: 179-82.
43. Prineas JW. The neuropathology of multiple sclerosis. In: Koetsier JC, editor. Demyelinating diseases. Amsterdam: Elsevier Science Publishers; 1985. p. 337-98.
44. Russo C, Smoker WR, Kubal W. Cortical and subcortical T2 shortening in multiple sclerosis. AJNR Am J Neuroradiol 1997; 18: 124-6.
45. Schmierer K, Scaravilli F, Barker GJ, Gordon R, Macmanus DG, Miller DH. Stereotactic co-registration of magnetic resonance imaging and histopathology in post-mortem multiple sclerosis brain. Neuropathol Appl Neurobiol 2003; 29: 596-601.
46. Sommer N, Martin R, McFarland HF, Quigley L, Cannella B, Raine CS, et al. Therapeutic potential of phosphodiesterase type 4 inhibition in chronic autoimmune demyelinating disease. J Neuroimmunol 1997; 79: 54-61.
47. Steinman L, Zamvil SS. How to successfully apply animal studies in experimental allergic encephalomyelitis to research on multiple sclerosis. Ann Neurol 2006; 60: 12-21.
48. Tjoa CW, Benedict RH, Weinstock-Guttman B, Fabiano AJ, Bakshi R. MRI T2 hypointensity of the dentate nucleus is related to ambulatory impairment in multiple sclerosis. J Neurol Sci 2005; 234: 17-24.
49. Trapp BD, Peterson J, Ransohoff RM, Rudick R, Mork S, Bo L. Axonal transection in the lesions of multiple sclerosis. N Engl J Med 1998; 338: 278-85.
50. Truyen L, van Waesberghe JH, van Walderveen MA, van Oosten BW, Polman CH, Hommes OR, et al. Accumulation of hypointense lesions ("black holes") on T1 spin-echo MRI correlates with disease progression in multiple sclerosis. Neurology 1996; 47: 1469-76.
51. van Waesberghe JH, Kamphorst W, De Groot CJ, van Walderveen MA, Castelijns JA, Ravid R, et al. Axonal loss in multiple sclerosis lesions: magnetic resonance imaging insights into substrates of disability. Ann Neurol 1999; 46: 747-54.
52. van Waesberghe JH, van Walderveen MA, Castelijns JA, Scheltens P, Lycklama a Nijeholt GJ, Polman CH, et al. Patterns of lesion development in multiple sclerosis: longitudinal observations with T1-weighted spin-echo and magnetization transfer MR. AJNR Am J Neuroradiol 1998; 19: 675-83.
53. van Walderveen MA, Barkhof F, Pouwels PJ, van Schijndel RA, Polman CH, Castelijns JA. Neuronal damage in T1-hypointense multiple sclerosis lesions demonstrated in vivo using proton magnetic resonance spectroscopy. Ann Neurol 1999; 46: 79-87.
54. van Walderveen MA, Kamphorst W, Scheltens P, van Waesberghe JH, Ravid R, Valk J, et al. Histopathologic correlate of hypointense lesions on T1-weighted spin-echo MRI in multiple sclerosis. Neurology 1998; 50: 1282-8.
55. Wensky AK, Furtado GC, Marcondes MC, Chen S, Manfra D, Lira SA, et al. IFN-gamma determines distinct clinical outcomes in autoimmune encephalomyelitis. J Immunol 2005; 174: 1416-23.
56. Werring DJ, Brassat D, Droogan AG, Clark CA, Symms MR, Barker CJ, et al. The pathogenesis of lesions and normal-appearing white matter changes in multiple sclerosis: a serial diffusion MRI study. Brain 2000; 123 (Pt 8): 1667-76.
57. Xu S, Jordan EK, Brocke S, Bulte JW, Quigley L, Tresser N, et al. Study of relapsing remitting experimental allergic encephalomyelitis SJL mouse model using MION-46L enhanced in vivo MRI: early histopathological correlation. J Neurosci Res 1998; 52: 549-58.
58. Zisman E, Sela M, Ben Nun A, Mozes E. Dichotomy between the T and the B cell epitopes of the synthetic polypeptide (T,G)-A-L. Eur J Immunol 1994; 24: 2497-505.