The slow Wallerian degeneration gene, WldS, inhibits axonal spheroid pathology in gracile axonal dystrophy mice.

Axonal dystrophy is the hallmark of axon pathology in many neurodegenerative disorders of the CNS, including Alzheimer's disease, Parkinson's disease and stroke. Axons can also form larger swellings, or spheroids, as in multiple sclerosis and traumatic brain injury. Some spheroids are terminal endbulbs of axon stumps, but swellings may also occur on unbroken axons and their role in axon loss remains uncertain. Similarly, it is not known whether spheroids and axonal dystrophy in so many different CNS disorders arise by a common mechanism. These surprising gaps in current knowledge result largely from the lack of experimental methods to manipulate axon pathology. The slow Wallerian degeneration gene, Wld(S), delays Wallerian degeneration after injury, and also delays 'dying-back' in peripheral nervous system disorders, revealing a mechanistic link between two forms of axon degeneration traditionally considered distinct. We now report that Wld(S) also inhibits axonal spheroid pathology in gracile axonal dystrophy (gad) mice. Both gracile nucleus (P < 0.001) and cervical gracile fascicle (P = 0.001) contained significantly fewer spheroids in gad/Wld(S) mice, and secondary signs of axon pathology such as myelin loss were also reduced. Motor nerve terminals at neuromuscular junctions continued to degenerate in gad/Wld(S) mice, consistent with previous observations that Wld(S) has a weaker effect on synapses than on axons, and probably contributing to the fact that Wld(S) did not alleviate gad symptoms. Wld(S) acts downstream of the initial pathogenic events to block gad pathology, suggesting that its effect on axonal swelling need not be specific to this disease. We conclude that axon degeneration mechanisms are more closely related than previously thought and that a link exists in gad between spheroid pathology and Wallerian degeneration that could hold for other disorders.

[1]  M. Koenig,et al.  The gene encoding gigaxonin, a new member of the cytoskeletal BTB/kelch repeat family, is mutated in giant axonal neuropathy , 2000, Nature Genetics.

[2]  Jada Lewis Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein , 2000, Nature Genetics.

[3]  P. Aebischer,et al.  Wlds-Mediated Protection of Dopaminergic Fibers in an Animal Model of Parkinson Disease , 2004, Current Biology.

[4]  T. Tomita,et al.  Neuropathology of gracile axonal dystrophy (GAD) mouse , 1989, Acta Neuropathologica.

[5]  E. Rugarli,et al.  Axonal degeneration in paraplegin-deficient mice is associated with abnormal mitochondria and impairment of axonal transport. , 2004, The Journal of clinical investigation.

[6]  M. Coleman,et al.  Genotyping methods to detect a unique neuroprotective factor (Wld s) for axons , 2002, Journal of Neuroscience Methods.

[7]  E. B. George,et al.  Prolonged survival of transected nerve fibres in C57BL/Ola mice is an intrinsic characteristic of the axon , 1993, Journal of neurocytology.

[8]  J. Rothstein,et al.  Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS) , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[9]  V. Perry,et al.  An 85-kb tandem triplication in the slow Wallerian degeneration (Wlds) mouse. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[10]  F. Clarac,et al.  Behavioural profiling of a murine Charcot–Marie–Tooth disease type 1A model , 2001, The European journal of neuroscience.

[11]  Takayuki Harada,et al.  Intragenic deletion in the gene encoding ubiquitin carboxy-terminal hydrolase in gad mice , 1999, Nature Genetics.

[12]  R. Kopito,et al.  Impairment of the ubiquitin-proteasome system by protein aggregation. , 2001, Science.

[13]  M. Esiri,et al.  Axonal damage: a key predictor of outcome in human CNS diseases. , 2003, Brain : a journal of neurology.

[14]  Pawel P. Liberski,et al.  Neuroaxonal pathology in Creutzfeldt-Jakob disease , 1999, Acta Neuropathologica.

[15]  D. Graham,et al.  Beta-amyloid precursor protein (beta APP) as a marker for axonal injury after head injury. , 1993, Neuroscience letters.

[16]  S. Minoshima,et al.  Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism , 1998, Nature.

[17]  S. W. Davies,et al.  Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. , 1997, Science.

[18]  Georg Auburger,et al.  The ubiquitin pathway in Parkinson's disease , 1998, Nature.

[19]  Y. Ihara,et al.  Ubiquitin is a component of paired helical filaments in Alzheimerʼs disease , 1987 .

[20]  K. Wada,et al.  Loss of Uch-L1 and Uch-L3 leads to neurodegeneration, posterior paralysis and dysphagia. , 2001, Human molecular genetics.

[21]  R. Ribchester,et al.  A rat model of slow Wallerian degeneration (WldS) with improved preservation of neuromuscular synapses , 2005, The European journal of neuroscience.

[22]  Richard R. Ribchester,et al.  Quantitative and qualitative analysis of Wallerian degeneration using restricted axonal labelling in YFP-H mice , 2004, Journal of Neuroscience Methods.

[23]  R. Ribchester,et al.  Neuroprotection after Transient Global Cerebral Ischemia in Wlds Mutant Mice , 2004, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[24]  D. Borchelt,et al.  ALS-Linked SOD1 Mutant G85R Mediates Damage to Astrocytes and Promotes Rapidly Progressive Disease with SOD1-Containing Inclusions , 1997, Neuron.

[25]  N. Ichihara,et al.  Axonal degeneration promotes abnormal accumulation of amyloid β-protein in ascending gracile tract of gracile axonal dystrophy (GAD) mouse , 1995, Brain Research.

[26]  D. Graham,et al.  β-Amyloid precursor protein (βAPP) as a marker for axonal injury after head injury , 1993, Neuroscience Letters.

[27]  D. Wagner,et al.  Proteasome inhibition arrests neurite outgrowth and causes “dying‐back” degeneration in primary culture , 2003, Journal of neuroscience research.

[28]  R. A. Crowther,et al.  Axonopathy and amyotrophy in mice transgenic for human four-repeat tau protein , 2000, Acta Neuropathologica.

[29]  V. Perry,et al.  Axonal damage in acute multiple sclerosis lesions. , 1997, Brain : a journal of neurology.

[30]  T. Kamei,et al.  Amyotrophic lateral sclerosis with numerous axonal spheroids in the corticospinal tract and massive degeneration of the cortex , 1997, Acta Neuropathologica.

[31]  T. Miike,et al.  Pathology of skeletal muscle and intramuscular nerves in infantile neuroaxonal dystrophy , 2004, Acta Neuropathologica.

[32]  J. Trojanowski,et al.  Axon pathology in Parkinson ’ s disease and Lewy body dementia hippocampus contains a-, b-, and g-synuclein , 1999 .

[33]  R. Ribchester,et al.  Compartmental neurodegeneration and synaptic plasticity in the Wlds mutant mouse , 2001, The Journal of physiology.

[34]  Till Acker,et al.  Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration , 2001, Nature Genetics.

[35]  J. Mcculloch,et al.  Drug development for stroke: importance of protecting cerebral white matter. , 1999, European journal of pharmacology.

[36]  Zhigang He,et al.  Involvement of the Ubiquitin-Proteasome System in the Early Stages of Wallerian Degeneration , 2003, Neuron.

[37]  Chrétien,et al.  Neuronal apoptosis does not correlate with dementia in HIV infection but is related to microglial activation and axonal damage , 1999, Neuropathology and applied neurobiology.

[38]  T. Kikuchi,et al.  Axonal degeneration of ascending sensory neurons in gracile axonal dystrophy mutant mouse , 2004, Acta Neuropathologica.

[39]  J. Griffin,et al.  The proximo-distal spread of axonal degeneration in the dorsal columns of the rat , 1994, Journal of neurocytology.

[40]  N. Williams,et al.  Chipping away at the old block , 2003, Current Biology.

[41]  K. Nave,et al.  Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. , 1998, Science.

[42]  H. Shibasaki,et al.  Dying back type axonal degeneration of sensory nerve terminals in muscle spindles of the gracile axonal dystrophy (GAD) mutant mouse , 1992, Neuropathology and applied neurobiology.

[43]  J. Povlishock,et al.  The effect of traumatic brain injury on the visual system: a morphologic characterization of reactive axonal change. , 1988, Journal of neurotrauma.

[44]  I. Duncan,et al.  Oligodendroglial modulation of fast axonal transport in a mouse model of hereditary spastic paraplegia , 2004, The Journal of cell biology.

[45]  R. Ribchester,et al.  Age‐Dependent Synapse Withdrawal at Axotomised Neuromuscular Junctions in Wlds Mutant and Ube4b/Nmnat Transgenic Mice , 2002, The Journal of physiology.

[46]  M. Gurney,et al.  Transgenic mice carrying a human mutant superoxide dismutase transgene develop neuronal cytoskeletal pathology resembling human amyotrophic lateral sclerosis lesions. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[47]  John T. Finn,et al.  Axonal Self-Destruction and Neurodegeneration , 2002, Science.

[48]  J. Glass,et al.  Wlds mice are resistant to paclitaxel (taxol) neuropathy , 2002, Annals of neurology.

[49]  C. Goodman,et al.  Ubiquitination-dependent mechanisms regulate synaptic growth and function , 2001, Nature.

[50]  T. Tomita,et al.  Gracile Axonal Dystrophy (GAD), a New Neurological Mutant in the Mouse , 1988, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[51]  V. Perry,et al.  The Rate of Wallerian Degeneration in Cultured Neurons from Wild Type and C57BL/WldS Mice Depends on Time in Culture and may be Extended in the Presence of Elevated K+ Levels , 1995, The European journal of neuroscience.

[52]  R. Lasek,et al.  Correlation of axonal regeneration and slow component B in two branches of a single axon , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[53]  V. Perry,et al.  Absence of Wallerian Degeneration does not Hinder Regeneration in Peripheral Nerve , 1989, The European journal of neuroscience.

[54]  V. Perry,et al.  A Ufd2/D4Cole1e chimeric protein and overexpression of Rbp7 in the slow Wallerian degeneration (WldS) mouse. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[55]  G. Feng,et al.  Imaging Neuronal Subsets in Transgenic Mice Expressing Multiple Spectral Variants of GFP , 2000, Neuron.

[56]  Jeff W Lichtman,et al.  Effects of Neurotoxic and Neuroprotective Agents on Peripheral Nerve Regeneration Assayed by Time-Lapse Imaging In Vivo , 2003, The Journal of Neuroscience.

[57]  J. Sanes,et al.  PDAPP; YFP double transgenic mice: A tool to study amyloid‐β associated changes in axonal, dendritic, and synaptic structures , 2003, The Journal of comparative neurology.

[58]  V. Perry,et al.  Axon pathology in neurological disease: a neglected therapeutic target , 2002, Trends in Neurosciences.

[59]  H. Lassmann,et al.  Distribution of a calcium channel subunit in dystrophic axons in multiple sclerosis and experimental autoimmune encephalomyelitis. , 2001, Brain : a journal of neurology.

[60]  P. Davies,et al.  Deregulation of cdk5, Hyperphosphorylation, and Cytoskeletal Pathology in the Niemann–Pick Type C Murine Model , 2002, The Journal of Neuroscience.

[61]  F. Grosveld,et al.  Frameshift mutants of beta amyloid precursor protein and ubiquitin-B in Alzheimer's and Down patients. , 1998, Science.

[62]  V. Perry,et al.  Focal Lesions in the Rat Central Nervous System Induced by Endothelin‐1 , 2003, Journal of neuropathology and experimental neurology.

[63]  R. Sidman,et al.  Atlas of the Mouse Brain and Spinal Cord , 1971 .

[64]  C. Wessig,et al.  The Wlds Mutation Delays Robust Loss of Motor and Sensory Axons in a Genetic Model for Myelin-Related Axonopathy , 2003, The Journal of Neuroscience.

[65]  David B. Goldstein,et al.  Demography, Recombination Hotspot Intensity, and the Block Structure of Linkage Disequilibrium , 2003, Current Biology.

[66]  C. Fletcher,et al.  Synaptic defects in ataxia mice result from a mutation in Usp14, encoding a ubiquitin-specific protease , 2002, Nature Genetics.

[67]  J Q Trojanowski,et al.  Axon pathology in Parkinson's disease and Lewy body dementia hippocampus contains alpha-, beta-, and gamma-synuclein. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[68]  Harry T Orr,et al.  Mutation of the E6-AP Ubiquitin Ligase Reduces Nuclear Inclusion Frequency While Accelerating Polyglutamine-Induced Pathology in SCA1 Mice , 1999, Neuron.

[69]  J. Milbrandt,et al.  Increased Nuclear NAD Biosynthesis and SIRT1 Activation Prevent Axonal Degeneration , 2004, Science.

[70]  J. Glass,et al.  Stable inheritance of an 85-kb triplication in C57BL/WldS mice. , 2003, Mutation research.

[71]  V. Perry,et al.  Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene , 2001, Nature Neuroscience.

[72]  H Shibasaki,et al.  Progressive degeneration of motor nerve terminals in GAD mutant mouse with hereditary sensory axonopathy , 1993, Neuropathology and applied neurobiology.

[73]  Kaori Nishikawa,et al.  Ubiquitin carboxy-terminal hydrolase L1 binds to and stabilizes monoubiquitin in neuron. , 2003, Human molecular genetics.

[74]  J. Sanes,et al.  Inhibiting Axon Degeneration and Synapse Loss Attenuates Apoptosis and Disease Progression in a Mouse Model of Motoneuron Disease , 2003, Current Biology.

[75]  R. Rudick,et al.  Axonal transection in the lesions of multiple sclerosis. , 1998, The New England journal of medicine.

[76]  H. Lassmann,et al.  Multiple sclerosis and chronic autoimmune encephalomyelitis: a comparative quantitative study of axonal injury in active, inactive, and remyelinated lesions. , 2000, The American journal of pathology.

[77]  M. Esiri,et al.  Cerebral white matter damage in HIV infection demonstrated using β-amyloid precursor protein immunoreactivity , 1997, Acta Neuropathologica.