Journal of Neuroimmunology
Volume 211, Issue 1 , Pages 49-55 , 25 June 2009

Distinct spatiotemporal pattern of CNS lesions revealed by USPIO-enhanced MRI in MOG-induced EAE rats implicates the involvement of spino-olivocerebellar pathways

  • Chih-Liang Chin

      Affiliations

    • Advanced Technology, Global Pharmaceutical Research and Development, Abbott Laboratories, Abbott Park, IL 60064, USA
    • Corresponding Author InformationCorresponding author. GPRD/Experimental Imaging, Dept. R4DF Bldg. AP9-1, 100 Abbott Park Road, Abbott Park, IL 60064-6119, USA. Tel.: +1 847 937 8093; fax: +1 847 935 9293.
  • ,
  • Madhavi Pai

      Affiliations

    • Neuroscience Research, Global Pharmaceutical Research and Development, Abbott Laboratories, Abbott Park, IL 60064, USA
  • ,
  • Peter F. Bousquet

      Affiliations

    • Department of Pharmacology, Abbott Bioresearch Center, 100 Research Drive, Worcester, MA 01605, USA
  • ,
  • Annette J. Schwartz

      Affiliations

    • Department of Pathology, Abbott Bioresearch Center, 100 Research Drive, Worcester, MA 01605, USA
  • ,
  • Elizabeth M. O'Connor

      Affiliations

    • Department of Pathology, Abbott Bioresearch Center, 100 Research Drive, Worcester, MA 01605, USA
  • ,
  • Christine M. Nelson

      Affiliations

    • Department of Pharmacology, Abbott Bioresearch Center, 100 Research Drive, Worcester, MA 01605, USA
  • ,
  • Vincent P. Hradil

      Affiliations

    • Neuroscience Research, Global Pharmaceutical Research and Development, Abbott Laboratories, Abbott Park, IL 60064, USA
  • ,
  • Bryan F. Cox

      Affiliations

    • Advanced Technology, Global Pharmaceutical Research and Development, Abbott Laboratories, Abbott Park, IL 60064, USA
  • ,
  • Bradford L. McRae

      Affiliations

    • Department of Pharmacology, Abbott Bioresearch Center, 100 Research Drive, Worcester, MA 01605, USA
  • ,
  • Gerard B. Fox

      Affiliations

    • Advanced Technology, Global Pharmaceutical Research and Development, Abbott Laboratories, Abbott Park, IL 60064, USA

Received 14 November 2008 ,Revised 16 February 2009 ,Accepted 5 March 2009.

References 

  1. Apps R. Movement-related gating of climbing fibre input to cerebellar cortical zones. Prog. Neurobiol. 1999;57:537–562
  2. Baeten K, Hendriks JJ, Hellings N, Theunissen E, Vanderlocht J, Ryck LD, et al. Visualisation of the kinetics of macrophage infiltration during experimental autoimmune encephalomyelitis by magnetic resonance imaging. J. Neuroimmunol. 2008;195:1–6
  3. Beckmann N, Falk R, Zurbrugg S, Dawson J, Engelhardt P. Macrophage infiltration into the rat knee detected by MRI in a model of antigen-induced arthritis. Magn. Reson. Med. 2003;49:1047–1055
  4. Bengtsson F, Hesslow G. Cerebellar control of the inferior olive. Cerebellum. 2006;5:7–14
  5. Berger C, Hiestand P, Kindler-Baumann D, Rudin M, Rausch M. Analysis of lesion development during acute inflammation and remission in a rat model of experimental autoimmune encephalomyelitis by visualization of macrophage infiltration, demyelination and blood–brain barrier damage. NMR Biomed. 2006;19:101–107
  6. 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
  7. Brochet B, Deloire MS, Touil T, Anne O, Caille JM, Dousset V, et al. Early macrophage MRI of inflammatory lesions predicts lesion severity and disease development in relapsing EAE. Neuroimage. 2006;32:266–274
  8. Compston A, Coles A. Multiple sclerosis. Lancet. 2002;359:1221–1231
  9. Dousset V, Ballarino L, Delalande C, Coussemacq M, Canioni P, Petry KG, et al. Comparison of ultrasmall particles of iron oxide (USPIO)-enhanced T2-weighted, conventional T2-weighted, and gadolinium-enhanced T1-weighted MR images in rats with experimental autoimmune encephalomyelitis. AJNR Am. J. Neuroradiol. 1999;20:223–227
  10. Dousset V, Brochet B, Deloire MS, Lagoarde L, Barroso B, Caille JM, et al. MR imaging of relapsing multiple sclerosis patients using ultra-small-particle iron oxide and compared with gadolinium. AJNR Am. J. Neuroradiol. 2006;27:1000–1005
  11. Filippi M, Grossman RI. MRI techniques to monitor MS evolution: the present and the future. Neurology. 2002;58:1147–1153
  12. Floris S, Blezer EL, Schreibelt G, Dopp E, van der Pol SM, Schadee-Eestermans IL, et al. Blood–brain barrier permeability and monocyte infiltration in experimental allergic encephalomyelitis: a quantitative MRI study. Brain. 2004;127:616–627
  13. Frohman EM, Racke MK, Raine CS. Multiple sclerosis—the plaque and its pathogenesis. N. Engl. J. Med. 2006;354:942–955
  14. 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;129:1953–1971
  15. Hemmer B, Nessler S, Zhou D, Kieseier B, Hartung HP. Immunopathogenesis and immunotherapy of multiple sclerosis. Nat. Clin. Pract. Neurol. 2006;2:201–211
  16. Kennedy PR, Ross HG, Brooks VB. Participation of the principal olivary nucleus in neocerebellar motor control. Exp. Brain Res. 1982;47:95–104
  17. Kim JH, Budde MD, Liang HF, Klein RS, Russell JH, Cross AH, et al. Detecting axon damage in spinal cord from a mouse model of multiple sclerosis. Neurobiol. Dis. 2006;21:626–632
  18. Kumar D, Timperley WR. The clinical, pathological and genetic aspects of sporadic late onset cerebellar ataxia: observations on a series of ten patients. Acta. Neurol. Scand. 1988;77:181–186
  19. Lalonde R, Joyal CC, Botez MI. Exploration and motor coordination in dystonia musculorum mutant mice. Physiol. Behav. 1994;56:277–280
  20. McFarland HF, Barkhof F, Antel J, Miller DH. The role of MRI as a surrogate outcome measure in multiple sclerosis. Mult. Scler. 2002;8:40–51
  21. Metz S, Bonaterra G, Rudelius M, Settles M, Rummeny EJ, Daldrup-Link HE. Capacity of human monocytes to phagocytose approved iron oxide MR contrast agents in vitro. Eur. Radiol. 2004;14:1851–1858
  22. Miller DH, Grossman RI, Reingold SC, McFarland HF. The role of magnetic resonance techniques in understanding and managing multiple sclerosis. Brain. 1998;121(Pt 1):3–24
  23. Namer IJ, Steibel J, Klinguer C, Trifilieff E, Mohr M, Poulet P. Magnetic resonance imaging of PLP-induced experimental allergic encephalomyelitis in Lewis rats. J. Neuroimmunol. 1998;92:22–28
  24. Nguyen KB, McCombe PA, Pender MP. Macrophage apoptosis in the central nervous system in experimental autoimmune encephalomyelitis. J. Autoimmun. 1994;7:145–152
  25. Noseworthy JH, Lucchinetti C, Rodriguez M, Weinshenker BG. Multiple sclerosis. N. Engl. J. Med. 2000;343:938–952
  26. Oweida AJ, Dunn EA, Karlik SJ, Dekaban GA, Foster PJ. Iron-oxide labeling of hematogenous macrophages in a model of experimental autoimmune encephalomyelitis and the contribution to signal loss in fast imaging employing steady state acquisition (FIESTA) images. J. Magn. Reson. Imaging. 2007;26:144–151
  27. Rausch M, Hiestand P, Foster CA, Baumann DR, Cannet C, Rudin M. Predictability of FTY720 efficacy in experimental autoimmune encephalomyelitis by in vivo macrophage tracking: clinical implications for ultrasmall superparamagnetic iron oxide-enhanced magnetic resonance imaging. J. Magn. Reson. Imaging. 2004;20:16–24
  28. Saab CY, Craner MJ, Kataoka Y, Waxman SG. Abnormal Purkinje cell activity in vivo in experimental allergic encephalomyelitis. Exp. Brain Res. 2004;158:1–8
  29. Sattler MB, Togni M, Gadjanski I, Suhs KW, Meyer N, Bahr M, et al. Strain-specific susceptibility for neurodegeneration in a rat model of autoimmune optic neuritis. J. Neuroimmunol. 2008;193:77–86
  30. Simon GH, von Vopelius-Feldt J, Fu Y, Schlegel J, Pinotek G, Wendland MF, et al. Ultrasmall supraparamagnetic iron oxide-enhanced magnetic resonance imaging of antigen-induced arthritis: a comparative study between SHU 555 C, ferumoxtran-10, and ferumoxytol. Invest. Radiol. 2006;41:45–51
  31. Skundric DS. Experimental models of relapsing–remitting multiple sclerosis: current concepts and perspective. Curr. Neurovasc. Res. 2005;2:349–362
  32. Steinbrecher A, Weber T, Neuberger T, Mueller AM, Pedre X, Giegerich G, et al. Experimental autoimmune encephalomyelitis in the rat spinal cord: lesion detection with high-resolution MR microscopy at 17.6 T. AJNR Am. J. Neuroradiol. 2005;26:19–25
  33. Steinman L, Zamvil SS. Virtues and pitfalls of EAE for the development of therapies for multiple sclerosis. Trends Immunol. 2005;26:565–571
  34. Stoll G, Wesemeier C, Gold R, Solymosi L, Toyka KV, Bendszus M. In vivo monitoring of macrophage infiltration in experimental autoimmune neuritis by magnetic resonance imaging. J. Neuroimmunol. 2004;149:142–146
  35. Stromnes IM, Cerretti LM, Liggitt D, Harris RA, Goverman JM. Differential regulation of central nervous system autoimmunity by T(H)1 and T(H)17 cells. Nat. Med. 2008;14:337–342
  36. Swanborg RH. Experimental autoimmune encephalomyelitis in the rat: lessons in T-cell immunology and autoreactivity. Immunol. Rev. 2001;184:129–135
  37. t Hart BA, Amor S, Jonker M. Evaluating the validity of animal models for research into therapies for immune-based disorders. Drug Discov. Today. 2004;9:517–524
  38. t Hart BA, Blezer EL, Brok HP, Boon L, de Boer M, Bauer J, et al. Treatment with chimeric anti-human CD40 antibody suppresses MRI-detectable inflammation and enlargement of pre-existing brain lesions in common marmosets affected by MOG-induced EAE. J. Neuroimmunol. 2005;163:31–39
  39. Weissleder R, Stark DD, Engelstad BL, Bacon BR, Compton CC, White DL, et al. Superparamagnetic iron oxide: pharmacokinetics and toxicity. AJR Am. J. Roentgenol. 1989;152:167–173
  40. Welsh JP, Llinas R. Some organizing principles for the control of movement based on olivocerebellar physiology. Prog. Brain Res. 1997;114:449–461
  41. Welsh JP, Lang EJ, Suglhara I, Llinas R. Dynamic organization of motor control within the olivocerebellar system. Nature. 1995;374:453–457

PII: S0165-5728(09)00106-4

doi: 10.1016/j.jneuroim.2009.03.012

Journal of Neuroimmunology
Volume 211, Issue 1 , Pages 49-55 , 25 June 2009