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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

Claudia F. Lucchinetti1, Raul N. Mandler4, Dorian McGavern2, Wolfgang Bruck8, Gerald Gleich2, Richard M. Ransohoff5, Corinna Trebst5, Brian Weinshenker1, Dean Wingerchuk6, Joseph E. Parisi1,3 and Hans Lassmann7

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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E. M. Frohman, O. Stuve, E. Havrdova, J. Corboy, A. Achiron, R. Zivadinov, P. S. Sorensen, J. T. Phillips, B. Weinshenker, K. Hawker, et al.
Therapeutic Considerations for Disease Progression in Multiple Sclerosis: Evidence, Experience, and Future Expectations
Arch Neurol, October 1, 2005; 62(10): 1519 - 1530.
[Abstract] [Full Text] [PDF]

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 JEMHome page
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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 Proc. Natl. Acad. Sci. USAHome page
F. Lolli, B. Mulinacci, A. Carotenuto, B. Bonetti, G. Sabatino, B. Mazzanti, A. M. D'Ursi, E. Novellino, M. Pazzagli, L. Lovato, et al.
An N-glucosylated peptide detecting disease-specific autoantibodies, biomarkers of multiple sclerosis
PNAS, July 19, 2005; 102(29): 10273 - 10278.
[Abstract] [Full Text] [PDF]

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 BrainHome page
T. Ishizu, M. Osoegawa, F.-J. Mei, H. Kikuchi, M. Tanaka, Y. Takakura, M. Minohara, H. Murai, F. Mihara, T. Taniwaki, et al.
Intrathecal activation of the IL-17/IL-8 axis in opticospinal multiple sclerosis
Brain, May 1, 2005; 128(5): 988 - 1002.
[Abstract] [Full Text] [PDF]

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 NeurologyHome page
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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 NeurologyHome page
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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 BrainHome page
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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 J. Neurol. Neurosurg. PsychiatryHome page
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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 Mult SclerHome page
S Pradhan and V N Mishra
A central demyelinating disease with atypical features
Multiple Sclerosis, June 1, 2004; 10(3): 308 - 315.
[Abstract] [PDF]

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 Mult SclerHome page
M J Eikelenboom, J Killestein, B M. Uitdehaag, and C H Polman
Letter to the Editor
Multiple Sclerosis, June 1, 2004; 10(3): 334 - 335.
[PDF]

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 Am. J. Pathol.Home page
M. Kerschensteiner, C. Stadelmann, B. S. Buddeberg, D. Merkler, F. M. Bareyre, D. C. Anthony, C. Linington, W. Bruck, and M. E. Schwab
Targeting Experimental Autoimmune Encephalomyelitis Lesions to a Predetermined Axonal Tract System Allows for Refined Behavioral Testing in an Animal Model of Multiple Sclerosis
Am. J. Pathol., April 1, 2004; 164(4): 1455 - 1469.
[Abstract] [Full Text] [PDF]

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 NeurologyHome page
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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 Mult SclerHome page
R Bergamaschi, S Tonietti, D Franciotta, E Candeloro, E Tavazzi, G Piccolo, A Romani, and V Cosi
Oligoclonal bands in Devic's neuromyelitis optica and multiple sclerosis: differences in repeated cerebrospinal fluid examinations
Multiple Sclerosis, February 1, 2004; 10(1): 2 - 4.
[Abstract] [PDF]

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 NeurologyHome page
I. Nakashima, K. Fujihara, J. Fujimori, K. Narikawa, T. Misu, and Y. Itoyama
Absence of IgG1 response in the cerebrospinal fluid of relapsing neuromyelitis optica
Neurology, January 13, 2004; 62(1): 144 - 146.
[Abstract] [Full Text] [PDF]

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 Clin. Microbiol. Rev.Home page
E. L. Oleszak, J. R. Chang, H. Friedman, C. D. Katsetos, and C. D. Platsoucas
Theiler's Virus Infection: a Model for Multiple Sclerosis
Clin. Microbiol. Rev., January 1, 2004; 17(1): 174 - 207.
[Abstract] [Full Text] [PDF]

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 Mult SclerHome page
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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 LupusHome page
J Sastre-Garriga and X Montalban
APS and the brain
Lupus, December 1, 2003; 12(12): 877 - 882.
[Abstract] [PDF]

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 NeurologyHome page
S. Paus, A. Promse, S. Schmidt, T. Klockgether, Y. Mao-Draayer, and H. Panitch
Treatment of steroid-unresponsive tumefactive demyelinating disease with plasma exchange
Neurology, October 14, 2003; 61(7): 1022 - 1023.
[Full Text] [PDF]

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 Mult SclerHome page
J de Seze, C Lebrun, T Stojkovic, D Ferriby, M Chatel, and P Vermersch
Is Devic's neuromyelitis optica a separate disease? A comparative study with multiple sclerosis
Multiple Sclerosis, October 1, 2003; 9(5): 521 - 525.
[Abstract] [PDF]

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 BrainHome page
R. Bergamaschi
Glatiramer acetate treatment in Devic's neuromyelitis optica
Brain, June 1, 2003; 126(6): E1 - E1.
[Full Text] [PDF]

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 NeurologyHome page
D. M. Wingerchuk and B. G. Weinshenker
Neuromyelitis optica: Clinical predictors of a relapsing course and survival
Neurology, March 11, 2003; 60(5): 848 - 853.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
C. Trebst, S. M. Staugaitis, P. Kivisakk, D. Mahad, M. K. Cathcart, B. Tucky, T. Wei, M. R. S. Rani, R. Horuk, K. D. Aldape, et al.
CC Chemokine Receptor 8 in the Central Nervous System Is Associated with Phagocytic Macrophages
Am. J. Pathol., February 1, 2003; 162(2): 427 - 438.
[Abstract] [Full Text] [PDF]

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 BrainHome page
R. Gold and C. Linington
Devic's disease: bridging the gap between laboratory and clinic
Brain, July 1, 2002; 125(7): 1425 - 1427.
[Full Text] [PDF]


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