Abstract
ALS is a fatal paralytic disorder characterized by a progressive loss of spinal cord motor neurons. Herein, we show that NADPH oxidase, the main reactive oxygen species-producing enzyme during inflammation, is activated in spinal cords of ALS patients and in spinal cords in a genetic animal model of this disease. We demonstrate that inactivation of NADPH oxidase in ALS mice delays neurodegeneration and extends survival. We also show that NADPH oxidase-derived oxidant products damage proteins such as insulin-like growth factor 1 (IGF1) receptors, which are located on motor neurons. Our in vivo and in vitro data indicate that such an oxidative modification hinders the IGF1/Akt survival pathway in motor neurons. These findings suggest a non-cell-autonomous mechanism through which inflammation could hasten motor neuron death and contribute to the selective motor neuronal degeneration in ALS.
MeSH Terms
Amyotrophic Lateral Sclerosis/metabolism
Animals
Cell Line, Tumor
Disease Models, Animal
Gene Expression Regulation
Humans
Membrane Glycoproteins/genetics
Mice
Mice, Inbred C57BL
Motor Neurons/metabolism
NADPH Oxidase 2
NADPH Oxidases/chemistry,genetics,metabolism,physiology
Neurons/metabolism
Spinal Cord/pathology
Transgenes
Chemicals
Membrane Glycoproteins
Cybb protein, mouse
NADPH Oxidase 2
NADPH Oxidases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Wu Du-Chu
Department of Neurology, Columbia University, New York, NY 10032, USA.
Ré Diane Bérangère
Nagai Makiko
Ischiropoulos Harry
Przedborski Serge
References (29)
29 references, click to expand
-
Increased expression of the pro-inflammatory enzyme cyclooxygenase-2 in amyotrophic lateral sclerosis.
Ann Neurol. 2001 Feb;49(2):176-85
PMID: 11220737
-
Onset and progression in inherited ALS determined by motor neurons and microglia.
Science. 2006 Jun 2;312(5778):1389-92
PMID: 16741123
-
Amyotrophic lateral sclerosis.
N Engl J Med. 2001 May 31;344(22):1688-700
PMID: 11386269
-
Ten years of protein kinase B signalling: a hard Akt to follow.
Trends Biochem Sci. 2001 Nov;26(11):657-64
PMID: 11701324
-
Target-derived cardiotrophin-1 and insulin-like growth factor-I promote neurite growth and survival of developing oculomotor neurons.
Mol Cell Neurosci. 2002 Jan;19(1):58-71
PMID: 11817898
-
Protein carbonylation in human diseases.
Trends Mol Med. 2003 Apr;9(4):169-76
PMID: 12727143
-
NADPH oxidase mediates oxidative stress in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease.
Proc Natl Acad Sci U S A. 2003 May 13;100(10):6145-50
PMID: 12721370
-
Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model.
Science. 2003 Aug 8;301(5634):839-42
PMID: 12907804
-
Chronic granulomatous disease.
Curr Opin Immunol. 2003 Oct;15(5):578-84
PMID: 14499268
-
Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice.
Science. 2003 Oct 3;302(5642):113-7
PMID: 14526083
-
Exacerbation of motor neuron disease by chronic stimulation of innate immunity in a mouse model of amyotrophic lateral sclerosis.
J Neurosci. 2004 Feb 11;24(6):1340-9
PMID: 14960605
-
Structural requirements for the transmembrane activation of the insulin receptor kinase.
J Biol Chem. 1986 Nov 15;261(32):15281-7
PMID: 3021769
-
Determination of carbonyl content in oxidatively modified proteins.
Methods Enzymol. 1990;186:464-78
PMID: 1978225
-
Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis.
Nature. 1993 Mar 4;362(6415):59-62
PMID: 8446170
-
Amyotrophic lateral sclerosis and structural defects in Cu,Zn superoxide dismutase.
Science. 1993 Aug 20;261(5124):1047-51
PMID: 8351519
-
Insulin-like growth factors: putative muscle-derived trophic agents that promote motoneuron survival.
J Neurobiol. 1993 Dec;24(12):1578-88
PMID: 8301266
-
Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production.
Nat Genet. 1995 Feb;9(2):202-9
PMID: 7719350
-
Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine.
J Neurosci. 1996 Feb 15;16(4):1324-36
PMID: 8778284
-
The cytosolic subunit p67phox contains an NADPH-binding site that participates in catalysis by the leukocyte NADPH oxidase.
J Clin Invest. 1996 Aug 15;98(4):977-83
PMID: 8770870
-
Bcl-2: prolonging life in a transgenic mouse model of familial amyotrophic lateral sclerosis.
Science. 1997 Jul 25;277(5325):559-62
PMID: 9228005
-
Effect of recombinant human insulin-like growth factor-I on progression of ALS. A placebo-controlled study. The North America ALS/IGF-I Study Group.
Neurology. 1997 Dec;49(6):1621-30
PMID: 9409357
-
NADPH oxidase: an update.
Blood. 1999 Mar 1;93(5):1464-76
PMID: 10029572
-
Muscle expression of a local Igf-1 isoform protects motor neurons in an ALS mouse model.
J Cell Biol. 2005 Jan 17;168(2):193-9
PMID: 15657392
-
Lentiviral-mediated silencing of SOD1 through RNA interference retards disease onset and progression in a mouse model of ALS.
Nat Med. 2005 Apr;11(4):423-8
PMID: 15768028
-
Synergy of insulin-like growth factor-1 and exercise in amyotrophic lateral sclerosis.
Ann Neurol. 2005 May;57(5):649-55
PMID: 15852403
-
Peroxynitrite generated by inducible nitric oxide synthase and NADPH oxidase mediates microglial toxicity to oligodendrocytes.
Proc Natl Acad Sci U S A. 2005 Jul 12;102(28):9936-41
PMID: 15998743
-
Chromogranin-mediated secretion of mutant superoxide dismutase proteins linked to amyotrophic lateral sclerosis.
Nat Neurosci. 2006 Jan;9(1):108-18
PMID: 16369483
-
Spinal cord endoplasmic reticulum stress associated with a microsomal accumulation of mutant superoxide dismutase-1 in an ALS model.
Proc Natl Acad Sci U S A. 2006 Apr 11;103(15):6025-30
PMID: 16595634
-
Amyotrophic lateral sclerosis. unfolding the toxicity of the misfolded.
Cell. 2001 Feb 23;104(4):581-91
PMID: 11239414