Advanced search
Publication Cover
Amyotrophic Lateral Sclerosis and Other Motor Neuron Disorders Volume 1, 2000 - Issue 4
Journal homepage
69
Views
13
CrossRef citations to date
0
Altmetric
Research Article

Mechanism and treatment of motoneuron degeneration in ALS: What have SOD1 mutants told us?

Zuoshang Xu Departments of Pharmacology and Molecular Toxicology, Cell Biology and Neuroscience Program, University of Massachusetts Medical School, Worcester, MA, USA
Pages 225-234 | Published online: 10 Jul 2009

  • Mulder DW, Kurland LT, Offord KP, Beard CM. Familial adult motor neuron disease: amyotrophic lateral sclerosis. Neurology 1986; 36: 511-517.
  • Munsat TL Adult motor neuron disease. In: Rowland LP, editor. Merritt's Textbook of Neurology. Philadelphia: Lea & Febiger, 1989: 682-687.
  • Rosen DR. Mutations in Cu,Zn Superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993; 362: 59-62.
  • Brown RH, Jr. Amyotrophic lateral sclerosis: recent insights from genetics and transgenic mice. Cell 1995; 80: 687-692.
  • Orrell RW. Amyotrophic lateral sclerosis: copper/zinc Superoxide dismutase (SODl) gene mutations. Neuromuscular Disorders 2000; 10: 63-68.
  • Fridovich I. Superoxide dismutases. Adv Enzymol 1986; 58: 61-97.
  • Shinobu LA, Beal MF. Mutant Superoxide dismutases and amyotrophic lateral sclerosis. In: Aruorna OI, Halliwell BS, editors. Molecular Biology of Free Radicals in Human Diseases. London: OICA International, 1998.
  • Bowling AC, Schulz JB, Brown RH, Jr., Beal MF. Superoxide dismutase activity, oxidative damage and mitochondria! energy metabolism in familial and sporadic amyotrophic lateral sclerosis. J Neurochem 1993; 61: 2322-2325.
  • Deng H-X, Hentati A, Tainer JA, et al. Amyotrophic lateral sclerosis and structural defects in Cu1Zn Superoxide dismutase. Science 1993; 261: 1047-1051.
  • Robberecht W, Sapp P, Viaene MK, et al. Cu/Zn Superoxide dismutase activity in familial and sporadic amyotrophic lateral sclerosis. J Neurochem 1994; 62: 384-387.
  • Rothstein JD, Bristol LA, Hosier B, Brown RHJ, Kuncl RW. Chronic inhibition of Superoxide dismutase produces apoptotic death of spinal neurons. Proc Nad Acad Sci USA 1994; 91: 4155-4159.
  • Greenland LJ, Deckwerth TL, Johnson EMJ. Superoxide dismutase delays neuronal apoptosis: a role for reactive oxygen species in programmed neuronal death. Neuron 1995; 14: 303-315.
  • Borchelt DR, Lee MK, Slunt MS, et al. Superoxide dismutase 1 with mutations linked to familial amyotrophic lateral sclerosis possesses significant activity. Proc Nad Acad Sci USA 1994; 91: 8292-8296.
  • Borchelt DR, Cuarnieri M, Wong PC, et al. Superoxide dismutase 1 subunits with mutations linked to familial amyotrophic lateral sclerosis do not affect wild-type subunit function. J Biol Chem 1995; 27ft 3234-3238.
  • Curney ME, Pu H, Chiu AY, et al. Motor neuron degeneration in mice that express a human Cu, Zn Superoxide dismutase. Science 1994; 264: 1772-1775 and Science 1995; 269: 149.
  • Ripps ME, Hundey GW, Hof PR, Morrison JH, Gordon JW. Transgenic mice expressing an altered murine Superoxide dismutase gene provide an animal model of amyotrophic lateral sclerosis. Proc Nad Acad Sci USA 1995; 92: 689-693.
  • Wong PC, Paido CA, Borchelt DR, et al. An adverse property of a familial ALS-linked SODl mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 1995; 14: 1105-1116.
  • Bruijn II, Becher MW, Lee MK, et al. ALS-linked SODl mutant C85R mediates damage to astrocytes and promotes rapidly progressive disease with SODl-containing inclusions. Neuron 1997; 18: 327-338.
  • Reaume AC, Hliott JL, Hoffinan EK, et al. Motor neurons in Cu/Zn Superoxide dismutase-deficdent mice develop normally but exhibit enhanced cell death after axonal injury. Nat Gen 1996; 13: 43-47.
  • Bruijn LI, Houseweart MK, Kato S, et al. Aggregation and motor neuron touchy of an ALS-linked SODl mutant independent from wild type SODl. Science 1998; 281: 1851-1854.
  • Beckman JS, Carson M, Smith CD, Koppenol WH. ALS, SOD and peroxinitrate. Nature 1993; 364: 584.
  • Crow JP, Sampson JB, Zhuang Y-X Thompson JA, Beckman JS. Decreased zinc affinity of amyotrophic lateral sclerosisassociated Superoxide dismutase mutants leads to enhanced catalysis of tyrosine nitration by peroxynitrite. J Neurochem 1997; 69: 1936-1944.
  • Crow JP, Ye YZ, Strong M, et al. Superoxide dismutase catalyzes nitration of tyrosines by peroxynitrite in the rod and head domains of neurofilament-L J Neurochem 1997; 69: 1945-1953.
  • Estevez AC, Crow JP, Sampson JB et al. Induction of nitric oxide-dependent apoptosis in motor neurons by zinc-deficient Superoxide dismutase. Science 1999; 286: 2498-2500.
  • Aimer C, Vukosavic S, Romero N, Przedborski S. Inducdble nitric oxide synthase up-regulation in a transgenic mouse model of familial amyotrophic lateral sclerosis. J Neurochem 1999; 72: 2415-2425.
  • Bruijn LL Beal MF, Becher MW, et al. Elevated free nitrotyrosine levels, but not protein-bound nitrotyrosine or hydroxyl radicals, throughout amyotrophic lateral Sclerosis (ALS)-like disease implicate tyrosine nitration as an aberrant in vivo property of one familial ALS-linked Superoxide dismutase 1 mutant Proc Nad Acad Sci USA 1997; 94: 7606-7611.
  • Ferrante RJ, Shinobu IA Schulz JB, et al. Increased 3nitrotyrosine and oxidative damage in mice with a human copper/zinc Superoxide dismutase mutation. Ann Neurol 1997; 42: 326-334.
  • Facchinetti F, Sasaki M, Cutting FB, et al. Lack of involvement of neuronal nitric oxide synthase in the pathogenesis of a transgenic mouse model of familial amyotrophic lateral Sclerosis. Neuroscience 1999; 90: 1483-1492.
  • Upton-Rice MN, Cudkowkz ME, Mathew RK, Reif D, Brown RH, Jr. Administration of nitric oxide synlhase inhibitors does not aher disease course of amyotrophic lateral sclerosis SODl mutant transgenk mice. Ann Neurol 1999; 45: 413-414.
  • Kong J, Xu Z. Overexpression of neurofilament subunit NFL and NF-H extends survival of a mouse model for amyotrophic lateral Sclerosis. Neurosci Let 2000; 281: 72-74.
  • Yim MB, Chock PB, Stadtman ER Copper, zinc Superoxide dismutase catalyzes hydroxyi radical production from hydrogen peroxide. Proc Nad Acad Sci USA 1990; 87: 394-398.
  • Yim MB, Chock PB, Stadtman ER. Enzyme function of copper, zinc Superoxide dismutase as a free radical generator. J Biol Chem 1993; 268: 4099-4105.
  • Wiedau-Pazos M, Goto JJ, Rabizadeh S, et al. Altered reactivity of Superoxide dismutase in familial amyotrophic lateral Sclerosis. Science 1996; 271: 515-518.
  • Yim MB, Kang JH, Yim HS, et al. A gain-of-function of an amyotrophic lateral sclerosis-associated Cu,Zn-superoxide dismutase mutant an enhancement of free radical formation due to a decrease in Km for hydrogen peroxide. Proc Natl Acad Sci USA 1996; 93: 5709-5714.
  • Yim HS, Kang JH, Chock PB, Stadtman ER, Yim MB. A familial amyotrophic lateral sclerosis-associated A4V Cu, Zn-superoxide dismutase mutant has a lower Km for hydrogen peroxide. Correlation between clinical severity and the Km value. J Biol Chem 1997; 272: 8861-8863.
  • Liu R, Althaus JS, Ellerbrock BR, Becker DA, Gurney ME. Enhanced oxygen radical production in a transgenic mouse model of familial amyotrophic lateral sclerosis. Ann Neurol 1998; 44: 763-770.
  • Ferrante RJ, Browne SE, Shinobu LA, et al. Evidence of increased oxidative damage in both sporadic and familial amyotrophic lateral sclerosis. J Neurochem 1997; 69: 2064-2074.
  • Bogdanov MB, Ramos LE, Xu Z, Beal MF. Elevated hydroxyl radical generation in vivo in an animal model of amyotrophic lateral Sclerosis. J Neurochem 1998; 71: 1321-1324.
  • Trotti D, Rolfs A, Danbolt NC, Brown RH, Jr., Hediger MA. SODl mutants linked to amyotrophic lateral sclerosis selectively inactivate a glial glutamate transporter. Nat Neuroscd 1999; 2: 427-433, 848.
  • Pedersen WA, Fu W, Keller JN, et al. Protein modification by the lipid peroxidation product 4-hydroxynonenal in the spinal cords of amyotrophic lateral Sclerosis patients. Ann Neurol 1998; 44: 819-824.
  • Canton T, Pratt J, Stutzmann JM, Imperato A, Boireau A. Glutamate uptake is decreased tardively in the spinal cord of FALS mice. Neuroreport 1998; 9: 775-778.
  • Rothstein JD. Excitotoxicity hypothesis. Neurology 1996; 47: S19-S25.
  • Wong PC, Rothstein JD, Price DL The genetic and molecular mechanisms of motor neuron disease. Curr Opin Neurobiol 1998; 8: 791-799.
  • Liochev SI, Chen LL, Hallewell RA, Fridovich I. Superoxidedependent peroxidase activity of H48Q: a Superoxide dismutase variant associated with familial amyotrophic lateral Sclerosis. Arch Biochem Biophys 1997; 352: 237-239.
  • Singh RJ, Karoui H, Günther MR, et al. Reexamination of the mechanism of hydroxyl radical adducts formed from the reaction between familial amyotrophic lateral sclerosis assodated Cu,Zn Superoxide dismutase mutants and H2O2. Proc Natl Acad Sci USA 1998; 95: 6675-6680.
  • Culotta VC, Klomp LW, Strain J, et al. The copper diaperone for Superoxide dismutase. J Biol Chem 1997; 272: 9221-9226.
  • Casareno RL, Waggoner D, Gitlin JD. The copper chaperone CCS directly interacts with copper/zinc Superoxide dismutase. J Biol Chem 1998; 273: 23625-23628.
  • Corson LB, Strain JJ, Culotta VC, Cleveland DW. Chaper-one-facilitated copper binding is a property common to several classes of familial amyotrophic lateral sclerosis-linked Superoxide dismutase mutants. Proc Natl Acad Sci USA 1998; 95: 6361-6366.
  • Rothstein JD, Dykes-Hoberg M, Corson LB, et al. The copper chaperone CCS is abundant in neurons and astrocytes in human and rodent brain. J Neurochem 1999; 72: 422-429.
  • Tu PH, Raju P, Robinson KA, Gurney ME, Trojanowski JQ, Lee VM. Transgenic mice carrying a human mutant Superoxide dismutase transgene develop neuronal cytoskeletal pathology resembling human amyotrophic lateral sclerosis lesions. Proc Nad Acad Sci USA 1996; 93: 3155-3160.
  • Kostic V, Jackson-Lewis V, de Bilbao F, Dubois-Dauphin M, Przedborsla S. Bd-2: prolonging life in a transgenic mouse model of familial amyotrophic lateral Sclerosis. Science 1997; 277: 559-562.
  • Martin LJ. Neuronal death in amyotrophic lateral Sclerosis is apoptosis: possible contribution of a programmed cell death mechanism. J Neuropathol Exp Neural 1999; 58: 459-471.
  • Li M, Ona VO, Cuegan C, et al. Functional role of caspase-1 and caspase-3 in an ALS transgenic mouse model. Science 2000; 288: 335-339.
  • Migheli A, Atzori C, Piva R, et al. Lack of apoptosis in mice with ALS. Nat Med 1999; 5: 966-967.
  • DaI Canto MC, Curney ML· Neuropathological changes in two lines of mice carrying a transgene for mutant human Cu, Zn SOD, and in mice overexpressing wild type human SOD: a model of familial amyotrophic lateral Sclerosis (FALS). Brain Res 1995; 676: 25-40.
  • Mourelatos Z, Gonatas NK, Stieber A, Curney ME, DaI Canto MC. The Golgi apparatus of spinal cord motor neurons in transgenic mice expressing mutant Cu,Zn Superoxide dismutase becomes fragmented in early, predinical stages of the disease. Proc Nad Acad Sci USA 1996; 93: 5472-5477.
  • Shibata N, Hirano A, Kobayashi M, et al. Presence of Cu/Zn Superoxide dismutase (SOD) immunoreactivity in neuronal hyaline inclusions in spinal cords from mice carrying a transgene for Cly93Ala mutant human Cu/Zn SOD. Acta Neuropathol 1998; 95: 136-142.
  • Kong J, Xu Z. Massive mitochondrial degeneration in motor neurons triggers the onset of amyotrophic lateral Sclerosis in mice expressing a mutant SODl. J Neurosci 1998; 18: 3241-3250.
  • Levine JB, Kong J, Nadler M, Xu Z. Astrocytes interact intimately with degenerating motor neurons in mouse amyotrophic lateral sclerosis (ALS). Glia 1999; 28: 215-224.
  • Cam MT, Ferri A, Battistoni A, et al. Expression of a Cu,Zn Superoxide dismutase typical of familial amyotrophic lateral Sclerosis induces mitochondrial alteration and increase of cytosolic Ca2+ concentration in transfected neuroblastoma SH-SY5Y cells. FEBS Lett 1997; 414: 365-368.
  • Kruman II, Pedersen WA, Springer JL· Mattson MP. ALSlinked Cu/Zn-SOD mutation increases vulnerability of motor neurons to exdtotoxidty by a mechanism involving increased oxidative stress and perturbed calcium homeostasis. Exp Neurol 1999; 160: 28-39.
  • Swerdlow RH, Parks JK, Cassarino DS, et al. Mitochondria in sporadic amyotrophic lateral sclerosis. Exp Neurol 1998; 153: 135-142.
  • Hatazawa J, Brooks RA, Dalakas MC, Mansi L, Di Chiro C. Cortical motor-sensory hypometabolism in amyotrophic lateral sclerosis: a PET study. J Comput Assist Tomogr 1988; 12: 630-636.
  • Bittigau P, Ikonomidou C. Glutamate in neurologic diseases. J Child Neurol 1997; 12: 471-485.
  • Cleveland DW. From Charcot to SODl: mechanisms of selective motor neuron death in ALS. Neuron 1999; 24: 515-520.
  • Robinson D, Ellenberger H. Distribution of N-methyl-Daspartate and non-N-methyl-D-aspartate glutamate receptor subunits on respiratory motor and premotor neurons in the rat J Comp Neurol 1997; 389: 94-116.
  • Williams TL, Ince PG, Oakley AL· Shaw PJ. An immunocytochemical study of the distribution of AMPA selective glutamate receptor subunits in the normal human motor system. Neurosdence 1996; 74: 185-198.
  • Bonnot A, Corio M, Tramu G, Viala D. Immunocytochemical distribution of ionotropic glutamate receptor subunits in the spinal cord of the rabbit J Chem Neuroanat 1996; 11: 267-278.
  • Ikonomidou C, Qin Qin Y, Labruyere J, Olney JW. Motor neuron degeneration induced by excitotoxin agonists has features m common with those seen m the SOD-1 transgenic mouse model of amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 1996; 55: 211-224.
  • Carriedo SG, Yin HZ, Weiss JH. Motor neurons are selectively vulnerable to AMPA/kainate receptor-mediated injury in vitro. J Neurosci 1996; 16: 4069-4079.
  • Rothstein JD, Dykes-Hoberg M, Pardo CA, et al. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 1996; 16: 675-686.
  • Rothstein JD, Jin L, Dykes-Hoberg M, Rund RW. Chronic inhibition of glutamate uptake produces a model of slow neurotoxidty. Proc Natl Acad Sci USA 1993; 90: 6591-6595.
  • Cumey ME, Heck TJ, Himes CS, Hall ED. Riluzole preserves motor function in a transgenic model of familial amyotrophic lateral sclerosis. Neurology 1998; 50: 62-66.
  • Ikonomidou C, Turski L. Neurodegenerative disorders: dues from glutamate and energy metabolism. Grit Rev Neurobiol 1996; 10: 239-263.
  • Rothstein JD, Van Kammen M, Levey AI, Martin LJ, Kuncl RW. Selective loss of glial glutamate transporter CLT-I in amyotrophic lateral sclerosis. Ann Neurol 1995; 38: 73-84.
  • Gong YH, Parsadanian AS, Andreeva A, Snider WD, Elliott JL Restricted expression of G86R Cu/Zn Superoxide dismutase in astrocytes results in astrocytosis but does not cause motoneuron degeneration. J Neurosd 2000; 20: 660-665.
  • Pardo CA, Xu Z, Borchelt DR, et al. Superoxide dismutase is an abundant component in cell bodies, dendrites, and axons of motor neurons and in a subset of other neurons. Proc Natl Acad Sd USA 1995; 92: 954-958.
  • Kong J, Xu Z. Peripheral axotomy slows motoneuron degeneration in a transgenic mouse line expressing mutant SOD1 G93A. J Comp Neurol 1999; 412: 373-380.
  • Standler NA, Bernstein JJ. Degeneration and regeneration of motoneuron dendrites after ventral root crush: computer reconstruction of dendritic fields. Exp Neurol 1982; 75: 600-615.
  • Yawo H. Changes in the dendritic geometry of mouse superior cervical ganglion cells following poslganglionic axotomy. J Neurosd 1987; 7: 3703-3711.
  • Vanden Noven S, Wallace N, Mucdo D, Turtz A, Pinter MJ. Adult spinal motoneurons remain viable despite prolonged absence of functional synaptic contact with muscle. Exp Neurol 1993; 123: 147-156.
  • Zhang B, Tu PH, Abtahian F, Trojanowski JQ, Lee VM-Y. Neurofilaments and orthograde transport are reduced in ventral root axons of transgenic mice that express human SODl with a G93A mutation. J Cell Biol 1997; 139: 1307-1315.
  • Williamson TL, Cleveland DW. Slowing of axonal transport is a very early event in the toxidty of ALS-linked SOD1 mutants to motor neurons. Nat Neurosd 1999; 2: 50-56.
  • Warita H, Itoyama Y, Abe K. Selective impairment of fast anterograde axonal transport in the peripheral nerves of asymptomatic transgenic mice with a G93A mutant SODl gene. Brain Res 1999; 819: 120-131.
  • Choi DW. Calcium and exdtotoxic neuronal injury. Ann NY Acad Sd 1994; 747: 162-171.
  • Heizmann CW, Braun K Changes in Ca(2+)-binding proteins in human neurodegenerative disorders. Trends Neurosd 1992; 15: 259-264.
  • Mattson MP. Calcium as sculptor and destroyer of neural circuitry. Exp Gerontol 1992; 27: 29-49.
  • Morrison BM, Gordan JW, Ripps ME, Morrison JH. Quantitative immunocytochemical analysis of the spinal cord in C86R Superoxide dismutase transgenic mice: Neurochemical correlates of selective vulnerability. J Comp Neurol 1996; 373: 619-631.
  • Siklos L, Engelhardt JI, Alexianu ME, Curney ME, Siddique T, Appel SH. Intracellular calcium parallels motoneuron degeneration in SOD-1 mutant mice. J Neuropathol Exp Neurol 1998; 57: 571-587.
  • Heizmann CW. Calcium-binding proteins: basic concepts and clinical implications. Gen Physiol Biophys 1992; 11: 411-425.
  • Petralia RS, Yokotani N, Wenthold RJ. light and electron microscope distribution of the NMDA receptor subunit NMDARl in the rat nervous system using a selective antipeptide antibody. J Neurosci 1994; 14: 667-696.
  • Petralia RS, Wang YX, Wenthold RJ. Histological and ultra-structural localization of the kainate receptor subunits, KA2 and CluR6/7, in the rat nervous system using selective antipeptide antibodies. J Comp Neurol 1994; 349: 85-110.
  • Petralia RS, Wang YX, Wenthold RJ. The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NRl. J Neurosci 1994; 14: 6102-6120.
  • Tachibana M, Wenthold RJ, Morioka H, Petralia RS. Light and electron microscopic immunocytochemical localization of AMPA-selective glutamate receptors in the rat spinal cord. J Comp Neurol 1994; 344: 431-454.
  • Geiger JR, Meldier T, Koh DS, et al. Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 1995; 15: 193-204.
  • Petralia RS, Wang YX, Mayat E, Wenthold RJ. Glutamate receptor subunit 2-selective antibody shows a differential distribution of calcium-impermeable AMPA receptors among populations of neurons. J Comp Neurol 1997; 385: 456-476.
  • Williams Tl, Day NC, Ince PG, Kamboj RK, Shaw PJ. Calcium-permeable alpha-amino-3-hydroxy-5-methyl-4isoxazole propionic acid receptors: a molecular determinant of selective vulnerability in amyotrophic lateral sclerosis. Ann Neurol 1997; 42: 200-207.
  • Tomiyama M, Rodriguez-Puertas R, Cortes R et al. Differential regional distribution of AMPA receptor subunit messenger RNAs in the human spinal cord as visualized by in situ hybridization. Neuroscience 1996; 75: 901-915.
  • Virgo L, Samarasinghe S, de Belleroche J. Analysis of AMPA receptor subunit mRNA expression in control and ALS spinal cord. Neuroreport 1996; 7: 2507-2511.
  • Morrison BM, Janssen WG, Gordon JW, Morrison JH. Light and electron microscopic distribution of the AMPA receptor subunit, GluR2, in the spinal cord of control and G86R mutant Superoxide dismutase transgenic mice. J Comp Neurol 1998; 395: 523-534.
  • Bensimon G, Lacomblez L, Meininger V. A controlled trial of riluzole in amyotrophic lateral sclerosis. ALS/Riluzole Study Group. N Engl J Med 1994; 330: 585-591.
  • Lacomblez L, Bensimon G, Leigh PN, et al. A confirmatory dose-ranging study of riluzole in ALS. ALS/Riluzole Study Group-II. Neurology 1996; 47: S242-S250.
  • Louvel E, Hugon J, Doble A. Therapeutic advances in amyotrophic lateral sclerosis. Trends Pharmacol Sci 1997; 18: 196-203.
  • Obrenovitch TP. Amyotrophic lateral sclerosis, excitotoxicity and riluzole. Trends Pharmacol Sci 1998; 19: 9-11.
  • Beal MF. Qxidative damage in neurodegenerative diseases. The Neurosdentist 1997; 3: 21-27.
  • Klivenyi P, Ferrante RJ, Matthews RT, et al. Neuroprotective effects of creatine in a transgenic animal model of amyo-trophic lateral sclerosis. Nat Med 1999; 5: 347-350.
  • Gurney ME, Cutting FB, Zhai P, et al. Benefit of vitamin E, riluzole, and gabapentin in a transgenic model of familial amyotrophic lateral Sclerosis. Ann Neural 1996; 39: 147-157.
  • Pedersen WA, Mattson MP. No benefit of dietary restriction on disease onset or progression in amyotrophic lateral sclerosis Cu/Zn-superoxide dismutase mutant mice. Brain Res 1999; 833: 117-120.
  • Mitsumoto H, Ikeda K, Klihkosz B, Cedarbaum JM, Wong V, Iindsay RM. Arrest of motor neuron disease in wobbler mice cotreated with CNIF and BDNF. Science 1994; 265: 1107-1110.
  • Rothstein JD. Therapeutic horizon for amyotrophic lateral sclerosis. Curr Opin Neurobiol 1996; 6: 679-687.
  • Sagot Y, Rosse T, Vejsada R, Perrelet D, Kato AC. Differential effects of neurotrophic factors on motoneuron retrograde labeling in a murine model of motoneuron disease. J Neurosci 1998; 18: 1132-1141.
  • Corse AM, Bilak MM, Bilak SR, Lehar M, Rothstein JD, Kund RW. Predinical testing of neuroprotective neurotrophic factors in a model of chronic motor neuron degeneration. Neurobiol Dis 1999; 6: 335-346.
  • Vergani L, Losa M, Lesma E, et al. Glycosaminoglycans boost insulin-like growth factor-I-promoted neuroprotection: blockade of motor neuron death in the wobbler mouse. Neuroscience 1999; 93: 565-572.
  • Mohajeri MH, Figlewicz DA Bohn MC. Intramuscular grafts of myoblasts genetically modified to secrete glial cell line-derived neurotrophic factor prevent motoneuron loss and disease progression in a mouse model of familial amyotrophic lateral Sclerosis. Hum Gene Ther 1999; 10: 1853-1866.
  • Grothe C, Unsicker K Basic fibroblast growth factor in the hypoglossal system: specific retrograde transport, trophic, and lesion-related responses. J Neurosci Res 1992; 32: 317-328.
  • Ikeda K, Iwasaki Y, Tagaya N, Shiojima T, Kobayashi T, Kinoshita M. Neuroprotective effect of basic fibroblast growth factor on wobbler mouse motor neuron disease. Neural Res 1995; 17: 445-448.
  • Upton-Rice MN, Cudkowicz ME, Warren L, et al. Basic fibroblast growth factor does not prolong survival in a transgenic model of familial amyotrophic lateral Sclerosis. Ann Neural 1999; 46: 934.
  • Friedlander RM, Brown RH, Gagliardini V, Wang J, Yuan J. Inhibition of ICE slows ALS in mice [letter]. Nature 1997; 388: 31; 1998; 392: 560.
  • Bruijn LI, Cleveland DW. Mechanisms of selective motor neuron death in ALS: insights from transgenic mouse models of motor neuron disease. Neuropathol Appl Neurobiol 1996; 22: 373-387.
  • Williamson TL, Bruijn LI, Zhu Q, et al. Absence of neurofilaments reduces the selective vulnerability of motor neurons and slows disease caused by a familial ALS-linked SODl mutant ProcNatl Acad Sci USA 1998; 95: 9631-9636.
  • Couillard-Despres S, Zhu Q, Wong PC, Price DL, Cleveland DW, Julien JP. Protective effect of neurofilament heavy gene overexpression in motor neuron disease induced by mutant Superoxide dismutase. Proc Natl Acad Sd USA 1998; 95: 9626-9630.
  • Monteiro MJ, Hoffman PN, Gearhart JD, Cleveland DW. Expression of NF-L in both neuronal and nonneuronal cells of transgenic mice: increased neurofilament density in axons without affecting caliber. J Cell Biol 1990; 111: 1543-1557.
  • Xu Z, Marszalek JR, Lee MK, et al. Subunit composition of neurofilaments specifies axonal diameter. J Cell Biol 1996; 133: 1061-1070.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.