Brain, Vol. 125, No. 7, 1450-1461,
July 2002
© 2002 Guarantors of Brain
A role for humoral mechanisms in the pathogenesis of Devic’s neuromyelitis optica
Departments of 1 Neurology, 2 Immunology and 3 Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN, 4 Department of Neurology, George Washington University, Washington, DC, 5 Department of Neurosciences of The Lerner Research Institute and Mellen Center for Multiple Sclerosis Treatment and Research, Cleveland Clinic Foundation, Cleveland, OH, 6 Department of Neurology, Mayo Clinic, Scottsdale, AZ, USA, 7 Brain Research Institute, Vienna, Austria and 8 Department of Neuropathology, Charite, Berlin, Germany
Correspondence to: Claudia F. Lucchinetti, Associate Professor of Neurology, Mayo Clinic, Rochester, MN, USA E-mail: lucchinetti.claudia{at}mayo.edu
Devic’s disease [neuromyelitis optica (NMO)] is an idiopathic inflammatory demyelinating disease of the CNS, characterized by attacks of optic neuritis and myelitis. The mechanisms that result in selective localization of inflammatory demyelinating lesions to the optic nerves and spinal cord are unknown. Serological and clinical evidence of B cell autoimmunity has been observed in a high proportion of patients with NMO. The purpose of this study was to investigate the importance of humoral mechanisms, including complement activation, in producing the necrotizing demyelination seen in the spinal cord and optic nerves. Eighty-two lesions were examined from nine autopsy cases of clinically confirmed Devic’s disease. Demyelinating activity in the lesions was immunocytochemically classified as early active (21 lesions), late active (18 lesions), inactive (35 lesions) or remyelinating (eight lesions) by examining the antigenic profile of myelin degradation products within macrophages. The pathology of the lesions was analysed using a broad spectrum of immunological and neurobiological markers, and lesions were defined on the basis of myelin protein loss, the geography and extension of plaques, the patterns of oligodendrocyte destruction and the immunopathological evidence of complement activation. The pathology was identical in all nine patients. Extensive demyelination was present across multiple spinal cord levels, associated with cavitation, necrosis and acute axonal pathology (spheroids), in both grey and white matter. There was a pronounced loss of oligodendrocytes within the lesions. The inflammatory infiltrates in active lesions were characterized by extensive macrophage infiltration associated with large numbers of perivascular granulocytes and eosinophils and rare CD3+ and CD8+ T cells. There was a pronounced perivascular deposition of immunoglobulins (mainly IgM) and complement C9neo antigen in active lesions associated with prominent vascular fibrosis and hyalinization in both active and inactive lesions. The extent of complement activation, eosinophilic infiltration and vascular fibrosis observed in the Devic NMO cases is more prominent compared with that in prototypic multiple sclerosis, and supports a role for humoral immunity in the pathogenesis of NMO. Based on this study, future therapeutic strategies designed to limit the deleterious effects of complement activation, eosinophil degranulation and neutrophil/macrophage/microglial activation are worthy of further investigation.
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V. A. Lennon, T. J. Kryzer, S. J. Pittock, A.S. Verkman, and S. R. Hinson IgG marker of optic-spinal multiple sclerosis binds to the aquaporin-4 water channel J. Exp. Med., August 15, 2005; 202(4): 473 - 477. [Abstract] [Full Text] [PDF]
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B. A.C. Cree, S. Lamb, K. Morgan, A. Chen, E. Waubant, and C. Genain An open label study of the effects of rituximab in neuromyelitis optica Neurology, April 12, 2005; 64(7): 1270 - 1272. [Abstract] [Full Text] [PDF]
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J. Correale and M. Fiol Activation of humoral immunity and eosinophils in neuromyelitis optica Neurology, December 28, 2004; 63(12): 2363 - 2370. [Abstract] [Full Text] [PDF]
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H. Sakuma, K. Kohyama, I.-K. Park, A. Miyakoshi, N. Tanuma, and Y. Matsumoto Clinicopathological study of a myelin oligodendrocyte glycoprotein-induced demyelinating disease in LEW.1AV1 rats Brain, October 1, 2004; 127(10): 2201 - 2213. [Abstract] [Full Text] [PDF]
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S J Pittock, B G Weinshenker, and E F M Wijdicks Mechanical ventilation and tracheostomy in multiple sclerosis J. Neurol. Neurosurg. Psychiatry, September 1, 2004; 75(9): 1331 - 1333. [Abstract] [Full Text] [PDF]
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J. -C. Antoine, J. -P. Camdessanche, L. Absi, F. Lassabliere, and L. Feasson Devic disease and thymoma with anti-central nervous system and antithymus antibodies Neurology, March 23, 2004; 62(6): 978 - 980. [Abstract] [Full Text] [PDF]
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C M Isbister, P J Mackenzie, D Anderson, N K Wade, and J Oger Co-occurrence of multiple sclerosis and myasthenia gravis in British C olumbia Multiple Sclerosis, December 1, 2003; 9(6): 550 - 553. [Abstract] [PDF]
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