Remyelination of optic nerve lesions: Spatial and temporal factors

Multiple Sclerosis

Volumn 16, Issue 7, 2010, Pages 786-795

  Klistorner, Alexandr ^a   Arvind, Hemamalini ^a   Garrick, Raymond ^b   Yiannikas, Con ^c   Paine, Mark ^d   Graham, Stuart L ^e  

^a UNIVERSITY OF SYDNEY   (Australia)

^b ST VINCENT S HOSPITAL   (Australia)

^c Department of Microbiology and Infectious Diseases   (Australia)

^d ROYAL VICTORIAN EYE AND EAR HOSPITAL   (Australia)

^e MACQUARIE UNIVERSITY   (Australia)

Author keywords

multifocal visual evoked potentials; Optic neuritis; remyelination

Indexed keywords

ADULT; ARTICLE; CLINICAL ARTICLE; DEMYELINATION; EVOKED VISUAL RESPONSE; FEMALE; FOLLOW UP; HUMAN; INFLAMMATION; LATENT PERIOD; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; OPTIC NERVE; OPTIC NEURITIS; REMYELINIZATION; VISUAL ACUITY; AUSTRALIA; CONVALESCENCE; DEMYELINATING DISEASE; PATHOLOGY; PATHOPHYSIOLOGY; PHOTOSTIMULATION; REACTION TIME; TIME;

ADULT; AUSTRALIA; DEMYELINATING DISEASES; EVOKED POTENTIALS, VISUAL; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; OPTIC NERVE; OPTIC NEURITIS; PHOTIC STIMULATION; REACTION TIME; RECOVERY OF FUNCTION; TIME FACTORS; VISUAL ACUITY;

EID: 77955041006     PISSN: 13524585     EISSN: None     Source Type: Journal    
DOI: 10.1177/1352458510371408     Document Type: Article

References (75)

1. Beck RW, Trobe JD, Moke PS, et al. High- and low-risk profiles for the development of multiple sclerosis within 10 years after optic neuritis: experience of the optic neuritis treatment trial. Arch Ophthalmol 2003 ; 121: 944-949.
2. Youl BD, Turano G., Miller DH, et al. The pathophysiology of acute optic neuritis. An association of gadolinium leakage with clinical and electrophysiological deficits. Brain 1991 ; 114: 2437-2450.
3. Halliday AM, McDonald WI, Mushin J. Delayed visual evoked response in optic neuritis. Lancet 1972 ; i: 982-985.
4. Jones SJ, Brusa A. Neurophysiological evidence for long-term repair of MS lesions: implications for axon protection. J Neurol Sci 2003 ; 206: 193-198.
5. Smith KJ, Waxman SG The conduction properties of demyelinated and remyelinated axons. In: Waxman SG (ed.) Multiple sclerosis as a neuronal disease. Amsterdam: Elsevier Academic Press, 2005, p. 85-100.
6. Waxman SG Altered distributions and functions of multiple sodium channel subtypes in multiple sclerosis and its models. In: Waxman SG (ed.) Multiple sclerosis as a neuronal disease. Amsterdam: Elsevier Academic Press, 2005.
7. Felts PA, Baker TA, Smith KJ Conduction in segmentally demyelinated mammalian central axons. J Neurosci 1997 ; 17: 7267-7277.
8. McDonald WI Pathophysiology of conduction in central nerve fibers. In: Desmedt JE (ed.) Visual evoked potentials in man. Oxford: Clarendon Press, 1977, p. 427-437.
9. Davies MB, Willams R., Haq N., Pelosi L., Hawkins CP MRI of optic nerve and postchiasmal visual pathways and visual evoked potentials in secondary progressive multiple sclerosis. Neuroradiology 1998 ; 40: 767-770.
10. Martin M., Hiltner TD, Wood JC, Fraser SE, Jacobs RE, Readhead C. Myelin deficiencies visualized in vivo: visually evoked potentials and T2-weighted magnetic resonance images of Shiverer mutant and wild-type mice. J Neurosci Res 2006 ; 84: 1716-1726.
11. Smith KJ, Blackmore WF, McDonald WI The restoration of conduction by central remyelination. Brain 1981 ; 104: 383-404.
12. Yiannikas C., Walsh JC The variation of the pattern shift visual evoked response with the size of the stimulus field. Electroencephalogr Clin Neurophysiol 1983 ; 55: 427-435.
13. Halliday AM, Darbett G., Blumhardt LD, Kriss A. The macular and submacular subcomponents of the pattern evoked response. In: LDaG B (ed.) Human evoked potentials. New York: Plenum Publishing, 1979, p. 135-151.
14. Hood DC, Odel JG, Zhang X. Tracking the recovery of local optic nerve function after optic neuritis:a multifocal VEP study. Invest Ophthalmol Vis Sci 2000 ; 41: 4032-4038.
15. Graham SL, Klistorner A., Goldberg I. Clinical application of objective perimetry using multifocal VEP in glaucoma practice. Arch Ophthalmol 2005 ; 123: 729-739.
16. Perier O., Gregoire A. Electron microscopic features of multiple sclerosis lesions. Brain 1965 ; 88: 937-952.
17. Patrikios P., Stadelmann C., Kutzelnigg A., et al. Remyelination is extensive in a subset of multiple sclerosis patients. Brain 2006 ; 129: 3165-3172.
18. Prineas JW, Barnard RO, Kwon EE, Sharer LR, Cho ES Multiple sclerosis: remyelination of nascent lesions. Ann Neurol 1993 ; 33: 137-151.
19. Raine CS, Wu E. Multiple sclerosis: remyelination in acute lesions. J Neuropathol Exp Neurol 1993 ; 52: 199-204.
20. Bruck W., Kuhlmann T., Stadelmann C. Remyelination in multiple sclerosis. J Neurol Sci 2003 ; 206: 181-185.
21. Prineas JW, Kwon EE, Goldenberg PZ, et al. Multiple sclerosis. Oligodendrocyte proliferation and differentiation in fresh lesions. Lab Invest 1989 ; 61: 489-503.
22. Barkhof F., Bruck W., De Groot CJA, et al. Remyelinated lesions in multiple sclerosis: magnetic resonance image appearance. Arch Neurology 2003 ; 60: 1073-1081.
23. Patani R., Balaratnam M., Vora A., Reynolds R. Remyelination can be extensive in multiple sclerosis despite a long disease course. Neuropathol Appl Neurobiol 2007 ; 33: 277-287.
24. Ruffini F., Kennedy TE, Antel JP Inflammation and remyelination in the central nervous system. Am J Pathol 2004 ; 164: 1519-1522.
25. John GR, Shankar SL, Shafit-Zagardo B., et al. Multiple sclerosis: re-expression of a developmental pathway that restricts oligodendrocytes maturation. Nat Med 2002 ; 8: 1115-1121.
26. Chari DM, Blakemore WF New insights into remyelination failure in multiple sclerosis: implications for glial cell transplantation. Mult Scler 2002 ; 8: 271-277.
27. Foote AK, Blakemore WF Inflammation stimulates remyelination in areas of chronic demyelination. Brain 2005 ; 128: 528-539.
28. Kornek B., Storch MK, Weissert R., et al. Multiple sclerosis and chronic autoimmune encephalomyelitis: a comparative study of axonal injury in active, inactive and remyelinated lesons. Am J Pathol 2000 ; 157: 267-276.
29. De Groot CJA, Ruuls SR, Theeuwes JMW, et al. Immunocytochemical characterization of the expression of inducible and constitutive isoforms of nitric oxide synthase in demyelinating multiple sclerosis lesions. J Neuropathol Exp Neurol 1997 ; 56: 10-20.
30. McDonald WI, Compston A., Edan G., et al. Recommended diagnostic criteria for multiple sclerosis: guidelines from the international panel on the diagnosis of the multiple sclerosis. Ann Neurol 2001 ; 50: 121-127.
31. Klistorner A., Graham SL Electroencephalogram-based scaling of multifocal visual evoked potentials: effect on intersubject amplitude variability. Invest Ophthalmol Vis Sci 2001 ; 42: 2145-2152.
32. Graham SL, Klistorner A. The diagnostic significance of the multifocal pattern visual evoked potential in glaucoma. Curr Opin Ophthalmol 1999 ; 10: 140-146.
33. Klistorner A., Arvind H., Nguyen T., et al. Inflammation, demyelination and axonal loss in post-acute optic neuritis. Ann Neurol 2008 ; 61: 325-331.
34. Klistorner A., Graham SL, Fraser C., et al. Electrophysiological evidence for heterogeneity of lesions in optic neuritis. Invest Ophthalmol Vis Sci 2007 ; 48: 4549-4556.
35. Zhao C., Fancy S., Kotter MR, Li W-Y., Franklin R. Mechanisms of CNS remyelination - the key to therapeutic advances. J Neurol Sci 2005 ; 233: 87-91.
36. Miller RH Regulation of oligodendrocyte development in the vertebrate CNS. Progr Neurobiol 2002 ; 67: 451-467.
37. Dawson MR, Levine JR, Reynolds R. NG2-expressing cells in the central nervous system: are they oligodendroglial progenitors? J Neurosci Res 2000 ; 61: 179-181.
38. Chandran S., Hunt D., Joannides A., Zhao C., Compston A., Franklin R. Myelin repair: the role of stem and precursor cells in multiple sclerosis. Phil Trans R Soc 2008 ; 363: 171-183.
39. Nishiyama A., Chang A., Trapp BD NG2 glial cells: a novel glial cell population in the adult brain. J Neuropathol Exp Neurol 1999 ; 58: 1113-1124.
40. Jennings AR, Kirilak Y., Carroll WM In situ characterisation of oligodendrocyte progenitor cells in adult mammalian optic nerve. J Neurocytol 2002 ; 31: 27-39.
41. Franklin RJM, Ffrench-Constant C. Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci 2008 ; 9: 839-855.
42. Sim FJ, Zhao C., Penderis J., Franklin RJM The age-related decrease in CNS remyelination efficiency is attributable in an impairment of both oligodenrocyte progenitor recruitment and differentiation. J Neurosci 2002 ; 22: 2451-2459.
43. Li W-W., Penderis J., Zhao C., Schumacher M., Franklin RJM. Females remyelinate more efficiently than males following demyelination in the aged, but not young adult CNS. Exp Neurol 2006 ; 202: 250-254.
44. Niehaus A., Shi J., Grzenkowski M., et al. Patients with active relapsing-remitting multiple sclerosis synthesize antibodies recognizing oligodendrocyte procursor cells surface protein: implications for remyelination. Ann Neurol 2000 ; 48: 362-371.
45. Li G., Crang AJ, Blakemore WF Oligodendrocyte progenitor cells in the adult rat CNS express myelin oligodendrocyte glycoprotein (MOG). Brain Pathol 2002 ; 12: 463-471.
46. Willams A., Piaton G., Aigrot MS, et al. Semaphorin 3A and 3F: key players in myelin repair in multiple sclerosis? Brain 2007 ; 130: 2554-2565.
47. Ono K., Yasui Y., Rutishauser U., Miller RH Focal ventricular origin and migration of oligodendrocytes procursor into the chick optic nerve. Neuron 1997 ; 19: 1-20.
48. Small RK, Riddle P., Noble M. Evidence for migration of oligodendrocyte-type-2 astrocyte progenitor cells into the developing rat optic nerve. Nature 1987 ; 328: 155-157.
49. Sugimoto Y., Taniguchi M., Yagi T., Akagi Y., Nojyo Y. Guidance of glial procursor cell migration by selected cues in the developing optic nerve. Development 2001 ; 128: 3321-3330.
50. Carroll WM, Jennings AR Early recruitment of oligodendrocyte precursors in CNS demyelination. Brain 1994 ; 117: 563-578.
51. Trip A., Schlottmann PG, Jones SJ, et al. Optic nerve atrophy and retinal nerve fibre layer thinning following optic neuritis: evidence that axonal loss is a substrate of MRI-detected atrophy. Neuroimage 2006 ; 31: 286-293.
52. Frohman EM, Dwyer M., Frohman TC, et al. Relationship of optic nerve and brain conventional and non-conventional MRI measures and RNFL, as assessed by OCT and GDx: a pilot study. J Neurol Sci 2009 ; 15: 96-105.
53. Fillipi M. MRI technologies in multiple sclerosis. In: Cook SD (ed.) Handbook on multiple sclerosis. New York: Taylor & Francis, 2005, p. 179-221.
54. Tartaglino LM, Friedman DP, Flanders AE, Lublin FD, Knobler RL, Liem M. Multiple sclerosis in the spinal cord. Radiology 1995 ; 195: 725-732.
55. Franklin RJ, Gilson JM, Blakemore WF Local recruitment of remyelinating cells in the repair of demyelination in the central nervous system. J Neurosci Res 1997 ; 50: 337-344.
56. Mason JL, Tiews A., Hosteller JD, et al. Oligodendrocytes and progenitors become progressively depleted within chronically demyelinated lesions. Am J Pathol 2004 ; 164: 1673-1682.
57. Keirstead HS, Blakemore WF The role of oligodendrocytes and oligodendrocyte progenitors in CNS remyelination. Adv Exp Med Biol 1999 ; 468: 188-197.
58. Blakemore WF, Chari DM, Gilson JM, Crang AJ Modelling large areas of demyelination in the rat reveals the potential and possible limitations of transplanted glial cells for remyelination in the CNS. Glia 2002 ; 38: 155-168.
59. Chari DM, Blakemore WF Efficient recolonization of progenitor-depleted areas of the CNS by adult oligodendrocyte progenitor cells. Glia 2002 ; 37: 307-313.
60. Irvine KA, Blakemore WF Remyelination protects axons from demyelination-associated axon degeneration. Brain 2008 ; 131: 1464-1477.
61. Dubois-Dalcq M., Williams AL, Stadelmann C., Stankooff B., Zalc B., Lubetzki C. From fish to man: understanding endogenous remyelination in central nervous system demyelinating disease. Brain 2008 ; 131: 1686-1700.
62. Franklin R., Zhao C., Sim FJ Astrocyte and macrophage interactions in promoting oligodendrocyte remyelination in the CNS. In: Glial interfaces in the nervous system. Amsterdam: IOS Press, 2002, p. 95-104.
63. Wolswijk G., Noble M. Cooperation between PDGF and FGF converts slowly dividing O-2Aadult progenitor cells to rapidly dividing cells with characteristics of O2Aperinatal progenitor cells. J Cell Biol 1992 ; 118: 889-900.
64. McDonald WI, Sears T. The effect of experimental demyelination on conduction in the central nervous system. Brain 1970 ; 93: 583-598.
65. Carroll WM, Jennings A., Mastaglia FL Experimental demyelinating optic neuropathy: a model for combined morphological and electrophysiological studies. Clin Exper Neurol 1983 ; 19: 17-28.
66. Kuhlmann T., Miron V., Cuo Q., Wegner C., Antel JP, Bruck W. Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. Brain 2008 ; 131: 1749-1758.
67. Wolswijk G. Chronic stage multiple sclerosis lesions contain a relatively quiescent population of oligodendrocytes precursor cells. J Neurosci 1998 ; 18: 601-609.
68. Chang A., Tourtellotte WW, Rudick R., Trapp BD Premyelinating oligodenrocytes in chronic lesions of multiple sclerosis. N Engl J Med 2002 ; 346: 165-173.
69. Klistorner A., Arvind H., Garrick R., Graham S., Paine M., Yannikas C. Correlation of optical coherence tomography and multifocal visual evoked potential after optic neuritis. Invest Ophthalmol Vis Sci 2010 ; 51: 2770-2777. [Epub ahead of print].
70. Smith KJ, Bostock H., Hall SM Saltatory conduction precedes remyelination in axons demyelinated with lysophosphatidyl choline. J Neurol Sci 1982 ; 54: 13-31.
71. Shrager P., Simon W., Kazarinova-Noyes K. Na+ channel reorganisation in demyelinated axons. In: Waxman SG (ed.) Multiple sclerosis as a neuronal disease. Amsterdam: Elsevier Academic Press, 2005.
72. Brusa A., Jones SJ, Plant GT Long-term remyelination after optic neuritis. Brain 2001 ; 124: 468-479.
73. Rodriguez M. A function of myelin is to protect axons from subsequent injury: implication for deficits in multiple sclerosis. Brain Pathol 2003 ; 126: 751-752.
74. Redford EJ, Kapoor R., Smith KJ Nitric oxide donors reversibly block axonal conduction: demyelinated axons are especially susceptible. Brain 1997 ; 120: 2149-2157.
75. Kuhlmann T., Lingfeld G., Bitsch A., Schuchardt J., Bruck W. Acute axonal damage in multiple sclerosis is most extensive in early disease stages and decreases over time. Brain 2002 ; 125: 2202-2212.