Multiple sclerosis is a chronic inflammatory disease of the CNS char-
acterized by sharply demarcated areas of demyelination and axonal
loss or damage, resulting in a multiplicity of neurological deficits
1
.
The etiology of MS remains uncertain, but the disease is generally
thought to result from an autoimmune response against myelin pro-
teins in genetically susceptible individuals
2
. Immunological,
immunohistochemical and molecular analyses of MS tissue suggests
that the development of this disease is driven by a T helper cell type 1
(T
H
1) inflammatory response, in concert with an autoantibody
response directed against defined components of CNS myelin
3–5
.
So far, MS has been regarded as a primary demyelinating disor-
der, and much effort has been devoted to investigating the relation-
ship between the evolution of lesions and clinical progression in
terms of myelin destruction and repair. Current data relating to the
role of axonal damage in the pathogenesis of MS show that there is
a strong correlation among the extent of axon damage in the spinal
cord, paralysis and loss of ambulation
6
. In our EAE model of MS,
we previously found that axonal damage is evident from the earliest
stage of disease and increases in severity with disease progression
7
.
These observations suggest that axonal injury is an important
pathological determinant of permanent disability in MS
6
. Unlike
the PNS, regenerative nerve fiber growth and structural plasticity
are limited in the adult CNS after insult
8
. In many cases, it has been
shown that rather than the absence of growth-promoting mole-
cules in the CNS, it is the presence of axon outgrowth inhibitors,
including components of both CNS myelin and astroglial scars,
that limits regeneration
8
.
Since its identification as a principal inhibitor of neurite out-
growth, Nogo A has received much attention
9
. The nogo gene is differ-
entially spliced to generate three isoforms: A, B and C. Nogo A is the
longest variant, is CNS-specific and contains a unique amino-termi-
nal sequence (amino-Nogo). The carboxy-terminal portion of the
Nogo A protein is common to all isoforms and contains two putative
transmembrane domains that are separated by a short extramembra-
nous region (Nogo-66). Both amino-Nogo and Nogo-66 have been
reported to be inhibitory in vitro: amino-Nogo has a stronger neurite
outgrowth inhibitory activity, whereas Nogo-66 is more potent in
inducing growth cone collapse
10
.
The mode of action of the Nogo-66 domain occurs via the Nogo-
66 receptor, NgR
10,11
. Notably, other inhibitory myelin proteins,
namely myelin-associated glycoprotein (MAG) and oligodendro-
cyte myelin glycoprotein (OMgp), exert their effects by interacting
with the NgR system
12,13
. The emergence of Nogo A as a major
inhibitor of neurite outgrowth and the identification of Nogo-66-
mediated inhibition through the NgR has led to the development of
strategies aimed at overcoming Nogo-mediated inhibition by tar-
geting either NgR or Nogo A, thereby providing some prospect for
spinal cord regeneration and repair
14,15
. Whereas most of the work
on the effects of Nogo has been conducted in models of spinal cord
injury, the role of Nogo in neurodegenerative diseases such as MS
has not been assessed.
Consequently, we have investigated the role of Nogo in the develop-
ment of a chronic form of EAE provoked by the myelin oligodendro-
cyte glycoprotein (MOG)
16
. We postulated that eliciting an immune
1
Neuroimmunology Laboratory, Department of Biochemistry, School of Molecular Sciences, La Trobe University, Bundoora, Victoria 3086, Australia.
2
Department of
Neurology and Neurological Sciences, School of Medicine,
3
Department of Neurobiology, Developmental Biology, School of Medicine, and
4
Department of Biological
Sciences, Howard Hughes Medical Institute, Stanford University, Stanford, California 94305, USA. Correspondence should be addressed to C.C.A.B.
(c.bernard@latrobe.edu.au).
Published online 6 June 2004; doi:10.1038/nn1261
The neurite outgrowth inhibitor Nogo A is involved in
autoimmune-mediated demyelination
Tara Karnezis
1,2
, Wim Mandemakers
3
, Jonathan L McQualter
1
, Binhai Zheng
4
, Peggy P Ho
2
, Kelly A Jordan
1
,
Belinda M Murray
1
, Ben Barres
3
, Marc Tessier-Lavigne
2
& Claude C A Bernard
1
Inhibitors associated with CNS myelin are thought to be important in the failure of axons to regenerate after spinal cord injury
and in other neurodegenerative disorders. Here we show that targeting the CNS-specific inhibitor of neurite outgrowth Nogo A by
active immunization blunts clinical signs, demyelination and axonal damage associated with experimental autoimmune
encephalomyelitis (EAE), a model of multiple sclerosis (MS). Mice vaccinated against Nogo A produce Nogo-specific antibodies
that block the neurite outgrowth inhibitory activity associated with CNS myelin in vitro. Passive immunization with anti-Nogo
IgGs also suppresses EAE. Our results identify Nogo A as an important determinant of the development of EAE and suggest that
its blockade may help to maintain and/or to restore the neuronal integrity of the CNS after autoimmune insult in diseases such as
MS. Our finding that Nogo A is involved in CNS autoimmune demyelination indicates that this molecule may have a far more
complex role than has been previously anticipated.
ARTICLES
736 VOLUME 7 | NUMBER 7 | JULY 2004 NATURE NEUROSCIENCE
© 2004 Nature Publishing Group http://www.nature.com/natureneuroscience