Lesional-targeting of neuroprotection to the inflammatory penumbra in experimental multiple sclerosis

Brain

Volumn 137, Issue 1, 2014, Pages 92-108

  Al Izki, Sarah ^a   Pryce, Gareth ^a   Hankey, Deborah J R ^b   Lidster, Katie ^a   Von Kutzleben, Stephanie M ^a   Browne, Lorcan ^c   Clutterbuck, Lisa ^c   Posada, Cristina ^c   Edith Chan, A W ^c   Amor, Sandra ^a,d   Perkins, Victoria ^a   Gerritsen, Wouter H ^d   Ummenthum, Kim ^d   Peferoen Baert, Regina ^d   Van Der Valk, Paul ^d   Montoya, Alexander ^a   Joel, Simon P ^a   Garthwaite, John ^c   Giovannoni, Gavin ^a   Selwood, David L ^c   Baker, David ^a   more..

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

animal models; experimental allergic encephalomyelitis; multiple sclerosis; neural repair

Indexed keywords

ATENOLOL; CARBAMAZEPINE; CFM 6104; INDINAVIR; MEMANTINE; MINOCYCLINE; MULTIDRUG RESISTANCE PROTEIN; MYELIN; NEUROPROTECTIVE AGENT; OXCARBAZEPINE; PINDOLOL; PROPRANOLOL; SODIUM CHANNEL BLOCKING AGENT; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; [N ((5 (2 (2 (1H IMIDAZOL 1YL)ETHYL) 2H INDAZOL 3 YL) 1,2,4 OXADIAZOL 3 YL)METHYL) 3 METHYLBENZAMID];

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNE UVEITIS; AUTOIMMUNITY; BLOOD BRAIN BARRIER; BRAIN DAMAGE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; DRUG PENETRATION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; HUMAN; HUMAN TISSUE; LYMPHOCYTE; MAXIMUM PLASMA CONCENTRATION; MOUSE; MULTIPLE SCLEROSIS; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; OPTIC NEURITIS; PRIORITY JOURNAL;

ANIMAL MODELS; EXPERIMENTAL ALLERGIC ENCEPHALOMYELITIS; MULTIPLE SCLEROSIS; NEURAL REPAIR;

ANIMALS; BENZAMIDES; BIOLOGICAL SPECIMEN BANKS; BRAIN; CARBAMAZEPINE; CARRIER PROTEINS; CELL PROLIFERATION; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DRUG DELIVERY SYSTEMS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; IMMUNOHISTOCHEMISTRY; INDAZOLES; MASS SPECTROMETRY; MICE; MICE, INBRED C57BL; MULTIPLE SCLEROSIS; NEUROPROTECTIVE AGENTS; OPTIC NEURITIS; OXADIAZOLES; P-GLYCOPROTEIN; SODIUM CHANNEL BLOCKERS; T-LYMPHOCYTES; UVEITIS; VOLTAGE-GATED SODIUM CHANNELS;

EID: 84892690281     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awt324     Document Type: Article

References (60)

1. Al-Izki S, Pryce G, O'Neill JK, Butter C, Giovannoni G, Amor S, et al. Practical guide to the induction of relapsing progressive experimental autoimmune encephalomyelitis in the Biozzi ABH mouse. Mult Scler Relat Dis 2012; 1: 29-38.
2. Al-Izki S, Pryce G, Jackson SJ, Giovannoni G, Baker D. Immunosuppression with FTY720 is insufficient to prevent secondary progressive neurodegeneration in experimental autoimmune encephalomyelitis. Mult Scler 2011; 17: 939-48.
3. Allen SJ, Baker D, O'Neill JK, Davison AN, Turk JL. Isolation and characterization of cells infiltrating the spinal cord during the course of chronic relapsing experimental allergic encephalomyelitis in the Biozzi AB/H mouse. Cell Immunol 1993; 146: 335-50.
4. Amor S, Groome N, Linington C, Morris MM, Dornmair K, Gardinier MV, et al. Identification of epitopes of myelin oligodendrocyte glycoprotein for the induction of experimental allergic encephalomyelitis in SJL and Biozzi AB/H mice. J Immunol 1994; 153: 4349-56.
5. Baker D, Gerritsen W, Rundle J, Amor S. Critical appraisal of animal models of multiple sclerosis. Mult Scler 2011; 17: 647-57.
6. Baker D, O'Neill JK, Davison AN, Turk JL. Control of immune-mediated disease of the central nervous system requires the use of a neuroactive agent: elucidation by the action of mitoxantrone. Clin Exp Immunol,1992, 90, 124-8.
7. Baker D, O'Neill JK, Gschmeissner SE, Wilcox CE, Butter C, Turk JL. Induction of chronic relapsing experimental allergic encephalomyelitis in Biozzi mice. J Neuroimmunol, 1990. 28, 261-70.
8. Bechtold DA, Miller SJ, Dawson AC, Sun Y, Kapoor R, Berry D, et al. Axonal protection achieved in a model of multiple sclerosis using lamotrigine. J Neurol 2006; 253: 1542-51.
9. Bettelli E, Pagany M, Weiner HL, Linington C, Sobel RA, Kuchroo VK. Myelin oligodendrocyte glycoprotein-specific T cell receptor transgenic mice develop spontaneous autoimmune optic neuritis. J Exp Med 2003; 197: 1073-81.
10. Black JA, Liu S, Carrithers M, Carrithers LM, Waxman SG. Exacerbation of experimental autoimmune encephalomyelitis after withdrawal of phenytoin and carbamazepine. Ann Neurol 2007; 62: 21-33.
11. Black JA, Liu S, Hains BC, Saab CY, Waxman SG. Long-term protection of central axons with phenytoin in monophasic and chronic-relapsing EAE. Brain 2006; 129 (Pt 12): 3196-208.
12. Black JA, Waxman SG. Sodium channels and microglial function. Exp Neurol 2012; 234: 302-15.
13. Butter C, Baker D, O'Neill JK, Turk JL. Mononuclear cell trafficking and plasma protein extravasation into the CNS during chronic relapsing experimental allergic encephalomyelitis in Biozzi AB/H mice. J Neurol Sci 1991; 104: 9-12.
14. Clutterbuck LA, Posada CG, Visintin C, Riddall DR, Lancaster B, Gane PJ, et al. Oxadiazolylindazole sodium channel modulators are neuroprotective toward hippocampal neurones. J Med Chem 2009; 52: 2694-707.
15. Coles AJ, Wing MG, Molyneux P, Paolillo A, Davie CM, Hale G, et al. Monoclonal antibody treatment exposes three mechanisms underlying the clinical course of multiple sclerosis. Ann Neurol 1999; 46: 296-304.
16. Compston A, Coles A. Multiple sclerosis. Lancet 2008; 372: 1502-17.
17. Cotton F, Weiner HL, Jolesz FA, Guttmann CR. MRI contrast uptake in new lesions in relapsing-remitting MS followed at weekly intervals. Neurology 2003; 60: 640-6.
18. Craner MJ, Damarjian TG, Liu S, Hains BC, Lo AC, Black JA, et al. Sodium channels contribute to microglia/macrophage activation and function in EAE and MS. Glia 2005; 49: 220-9.
19. Craner MJ, Newcombe J, Black JA, Hartle C, Cuzner ML, Waxman SG. 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 USA 2004; 101: 8168-73.
20. Crowe A, Teoh YK. Limited P-glycoprotein mediated efflux for anti-epileptic drugs. J Drug Target 2006; 14: 291-300.
21. Dutta R, Trapp BD. Mechanisms of neuronal dysfunction and degeneration in multiple sclerosis. Prog Neurobiol 2011; 93: 1-12.
22. Elger CE, Bauer J. New antiepileptic drugs in epileptology. Neuropsychobiology 1998; 38: 145-8.
23. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 2000; 28: 41-51.
24. Fern R, Ransom BR, Stys PK, Waxman SG. Pharmacological protection of CNS white matter during anoxia: actions of phenytoin, carbamazepine and diazepam. J Pharmacol Exp Ther 1993; 266: 1549-55.
25. Garthwaite G, Brown G, Batchelor AM, Goodwin DA, Garthwaite J. Mechanisms of ischaemic damage to central white matter axons: a quantitative histological analysis using rat optic nerve. Neuroscience 1999; 94: 1219-30.
26. Gnanapavan S, Grant D, Morant S, Furby J, Hayton T, Teunissen CE, et al. Biomarker Report from the Phase II Lamotrigine Trial in Secondary Progressive MS-Neurofilament as a Surrogate of Disease Progression. PLoS One 2013; 8: e70019.
27. Gnanapavan S, Grant D, Pryce G, Jackson S, Baker D, Giovannoni G. Neurofilament a biomarker of neurodegeneration in autoimmune encephalomyelitis. Autoimmunity 2012; 45: 298-303.
28. Greenwood J, Walters CE, Pryce G, Kanuga N, Beraud E, Baker D, et al. Lovastatin inhibits brain endothelial cell Rho-mediated lymphocyte migration and attenuates experimental autoimmune encephalomyelitis. FASEB J 2003; 17: 905-7.
29. Guan Y, Shindler KS, Tabuena P, Rostami AM. Retinal ganglion cell damage induced by spontaneous autoimmune optic neuritis in MOG-specific TCR transgenic mice. J Neuroimmunol 2006; 178: 40-8.
30. Gunnarsson M, Malmestrom C, Axelsson M, Sundstrom P, Dahle C, Vrethem M, et al. Axonal damage in relapsing multiple sclerosis is markedly reduced by natalizumab. Ann Neurol 2011; 69: 83-9.
31. Hampton DW, Anderson J, Pryce G, Irvine KA, Giovannoni G, Fawcett JW, et al. An experimental model of secondary progressive multiple sclerosis that shows regional variation in gliosis, remyelination, axonal and neuronal loss. J Neuroimmunol 2008; 201-02; 200-11.
32. Hankey DJ, Lightman SL, Baker D. Interphotoreceptor retinoid binding protein peptide-induced uveitis in B10.RIII mice: characterization of disease parameters and immunomodulation. Exp Eye Res 2001; 72: 341-50.
33. Jackson SJ, Lee J, Nikodemova M, Fabry Z, Duncan ID. Quantification of myelin and axon pathology during relapsing progressive experimental autoimmune encephalomyelitis in the Biozzi ABH mouse. J Neuropathol Exp Neurol 2009; 68: 616-25.
34. Jackson SJ, Pryce G, Diemel LT, Cuzner ML, Baker D. Cannabinoidreceptor 1 null mice are susceptible to neurofilament damage and caspase 3 activation. Neuroscience 2005; 134: 261-8.
35. Kapoor R, Davies M, Blaker PA, Hall SM, Smith KJ. Blockers of sodium and calcium entry protect axons from nitric oxide-mediated degeneration. Ann Neurol 2003; 53: 174-80.
36. Kapoor R, Furby J, Hayton T, Smith KJ, Altmann DR, Brenner R, et al. Lamotrigine for neuroprotection in secondary progressive multiple sclerosis: a randomised, double-blind, placebo-controlled, parallelgroup trial. Lancet Neurol 2010; 9: 681-8.
37. Kooij G, Mizee MR, van Horssen J, Reijerkerk A, Witte ME, Drexhage JA, et al. Adenosine triphosphate-binding cassette transporters mediate chemokine (C-C motif) ligand 2 secretion from reactive astrocytes: relevance to multiple sclerosis pathogenesis. Brain 2011; 134 (Pt 2): 555-70.
38. Kooij G, van Horssen J, de Lange EC, Reijerkerk A, van der Pol SM, van Het Hof B, et al. T lymphocytes impair P-glycoprotein function during neuroinflammation. J Autoimmun 2010; 34: 416-25.
39. Lassmann H. Pathology and disease mechanisms in different stages of multiple sclerosis. J Neurol Sci 2013; 333: 1-4.
40. Lee Y, Morrison BM, Li Y, Lengacher S, Farah MH, Hoffman PN, et al. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 2012; 487: 443-8.
41. Lidster K, Jackson SJ, Ahmed Z, Munro P, Coffey P, Giovannoni G, et al. Neuroprotection in a novel mouse model of multiple sclerosis. PLoS One 2013; 8: e79188.
42. Lo AC, Saab CY, Black JA, Waxman SG. Phenytoin protects spinal cord axons and preserves axonal conduction and neurological function in a model of neuroinflammation in vivo. J Neurophysiol 2003; 90: 3566-71.
43. Marta M, Giovannoni G. Disease modifying drugs in multiple sclerosis: mechanisms of action and new drugs in the horizon. CNS Neurol Disord Drug Targets 2012; 11: 610-23.
44. Miller DS, Bauer B, Hartz AM. Modulation of P-glycoprotein at the blood-brain barrier: opportunities to improve central nervous system pharmacotherapy. Pharmacol Rev 2008; 60: 196-209.
45. Morsali D, Bechtold D, Lee W, Chauhdry S, Palchaudhuri U, Hassoon P, et al. Safinamide and flecainide protect axons and reduce microglial activation in models of multiple sclerosis. Brain 2013; 136 (Pt 4): 1067-82.
46. Nakanishi H, Yonezawa A, Matsubara K, Yano I. Impact of P-glycoprotein and breast cancer resistance protein on the brain distribution of antiepileptic drugs in knockout mouse models. Eur J Pharmacol 2013; 710: 20-8.
47. Nojiri Y, Ishiwata K, Qinggeletu, Tobiishi S, Sasada T, Yamamoto F, et al. Radiosynthesis and biodistribution in mice of a 18F-labeled analog of O-1302 for use in cerebral CB1 cannabinoid receptor imaging. Biol Pharm Bull 2008; 31: 1274-8.
48. O'Neill JK, Baker D, Davison AN, Allen SJ, Butter C, Waldmann H, et al. Control of immune-mediated disease of the central nervous system with monoclonal (CD4-specific) antibodies. J Neuroimmunol 1993; 45: 1-14.
49. O'Neill JK, Baker D, Davison AN, Maggon KK, Jaffee BD, Turk JL. Therapy of chronic relapsing experimental allergic encephalomyelitis and the role of the blood-brain barrier: elucidation by the action of Brequinar sodium. J Neuroimmunol 1992; 38: 53-62.
50. Parpura V, Verkhratsky A. Homeostatic function of astrocytes: Ca(2 + ) and Na( + ) signalling. Transl Neurosci 2012; 3: 334-44.
51. Piddlesden SJ, Lassmann H, Zimprich F, Morgan BP, Linington C. The demyelinating potential of antibodies to myelin oligodendrocyte glycoprotein is related to their ability to fix complement. Am J Pathol 1993; 143: 555-64.
52. Pryce G, O'Neill JK, Croxford JL, Amor S, Hankey DJ, East E, et al. Autoimmune tolerance eliminates relapses but fails to halt progression in a model of multiple sclerosis. J Neuroimmunol 2005; 165: 41-52.
53. Raftopoulos RE, Kapoor R. Neuroprotection for acute optic neuritis-can it work? Mult Scler Rel Dis 2013; 2: 307-11.
54. Rishton GM, LaBonte K, Williams AJ, Kassam K, Kolovanov E. Computational approaches to the prediction of blood-brain barrier permeability: a comparative analysis of central nervous system drugs versus secretase inhibitors for Alzheimer's disease. Curr Opin Drug Discov Devel 2006; 9: 303-13.
55. Smith PA, Morris-Downes M, Heijmans N, Pryce G, Arter E, O'Neill JK, et al. Epitope spread is not critical for the relapse and progression of MOG 8-21 induced EAE in Biozzi ABH mice. J Neuroimmunol 2005; 164: 76-84.
56. Vesterinen HM, Sena ES, ffrench-Constant C, Williams A, Chandran S, Macleod MR. Improving the translational hit of experimental treatments in multiple sclerosis. Mult Scler 2010; 16: 1044-55.
57. Watson CM, Davison AN, Baker D, O'Neill JK, Turk JL. Suppression of demyelination by mitoxantrone. Int J Immunopharmacol 1991; 13: 923-30.
58. Waxman SG. Mechanisms of disease: sodium channels and neuroprotection in multiple sclerosis-current status. Nat Clin Pract Neurol 2008; 4: 159-69.
59. Waxman SG, Brill MH. Conduction through demyelinated plaques in multiple sclerosis: computer simulations of facilitation by short internodes. J Neurol Neurosurg Psychiatry 1978; 41: 408-16.
60. Wujek JR, Bjartmar C, Richer E, Ransohoff RM, Yu M, Tuohy VK, et al. Axon loss in the spinal cord determines permanent neurological disability in an animal model of multiple sclerosis. J Neuropathol Exp Neurol 2002; 61: 23-32.