The human G93A-SOD1 mutation in a pre-symptomatic rat model of amyotrophic lateral sclerosis increases the vulnerability to a mild spinal cord compression

BMC Genomics

Volumn 11, Issue 1, 2010, Pages

  Jokic, Natasa ^a   Yip, Ping K ^a   Michael Titus, Adina ^a   Priestley, John V ^a   Malaspina, Andrea ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C; SUPEROXIDE DISMUTASE; COPPER ZINC SUPEROXIDE DISMUTASE; NEUROFILAMENT PROTEIN; NEUROFILAMENT PROTEIN H; SYNAPTOPHYSIN;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN ATROPHY; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FUNCTIONAL ASSESSMENT; GENE EXPRESSION PROFILING; GENE MUTATION; INFLAMMATION; ION CURRENT; NERVE CELL EXCITABILITY; NEUROFILAMENT; NONHUMAN; PATHOGENESIS; RAT; SIGNAL TRANSDUCTION; SPINAL CORD COMPRESSION; SPINAL CORD MOTONEURON; SURVIVAL RATE; TRANSGENIC ANIMAL; UPREGULATION; AMINO ACID SUBSTITUTION; ANIMAL; CONVALESCENCE; DISEASE MODEL; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION; GENETICS; HUMAN; LAMINECTOMY; LOCOMOTION; METABOLISM; MOTONEURON; MUTATION; ORGAN SIZE; PATHOLOGY; PATHOPHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPINAL CORD INJURY; TIME;

ANIMALIA; RATTUS;

AMINO ACID SUBSTITUTION; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION TO DISEASE; HUMANS; LAMINECTOMY; LOCOMOTION; MOTOR NEURONS; MUTATION; NEUROFILAMENT PROTEINS; ORGAN SIZE; RATS; RECOVERY OF FUNCTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPINAL CORD COMPRESSION; SPINAL CORD INJURIES; SUPEROXIDE DISMUTASE; SYNAPTOPHYSIN; TIME FACTORS;

EID: 78149445599     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-11-633     Document Type: Article

References (57)

1. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, Donaldson D, Goto J, O'Regan JP, Deng HX. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362:59-62. 10.1038/362059a0, 8446170.
2. Chio A, Benzi G, Dossena M, Mutani R, Mora G. Severely increased risk of amyotrophic lateral sclerosis among Italian professional football players. Brain 2005, 128:472-476. 10.1093/brain/awh373, 15634730.
3. Kihira T, Kanno S, Miwa H, Okamoto K, Kondo T. The role of exogenous risk factors in amyotrophic lateral sclerosis in Wakayama, Japan. Amyotroph Lateral Scler 2007, 8:150-156. 10.1080/17482960601179407, 17538776.
4. Pasinelli P, Brown RH. Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat Rev Neurosci 2006, 7:710-723. 10.1038/nrn1971, 16924260.
5. Valenti M, Pontieri FE, Conti F, Altobelli E, Manzoni T, Frati L. Amyotrophic lateral sclerosis and sports: a case-control study. Eur J Neurol 2005, 12:223-225. 10.1111/j.1468-1331.2004.00978.x, 15693813.
6. Malaspina A, Jokic N, Huang WL, Priestley JV. Comparative analysis of the time-dependent functional and molecular changes in spinal cord degeneration induced by the G93A SOD1 gene mutation and by mechanical compression. BMC Genomics 2008, 9:500. 10.1186/1471-2164-9-500, 2585103, 18947433.
7. Dangond F, Hwang D, Camelo S, Pasinelli P, Frosch MP, Stephanopoulos G, Stephanopoulos G, Brown RH, Gullans SR. Molecular signature of late-stage human ALS revealed by expression profiling of postmortem spinal cord gray matter. Physiol Genomics 2004, 16:229-239.
8. De BA, Knoblach SM, Di GS, Fan C, Molon A, Hoffman EP, Faden AI. Gene expression profiling of experimental traumatic spinal cord injury as a function of distance from impact site and injury severity. Physiol Genomics 2005, 22:368-381. 10.1152/physiolgenomics.00081.2005, 15942019.
9. Grossman SD, Rosenberg LJ, Wrathall JR. Temporal-spatial pattern of acute neuronal and glial loss after spinal cord contusion. Exp Neurol 2001, 168:273-282. 10.1006/exnr.2001.7628, 11259115.
10. Kiernan MC, Bostock H. Effects of membrane polarization and ischaemia on the excitability properties of human motor axons. Brain 2000, (123 Pt 12):2542-2551. 10.1093/brain/123.12.2542, 11099455.
11. Malaspina A, Kaushik N, de BJ. Differential expression of 14 genes in amyotrophic lateral sclerosis spinal cord detected using gridded cDNA arrays. J Neurochem 2001, 77:132-145. 10.1046/j.1471-4159.2001.t01-1-00231.x, 11279269.
12. McEwen ML, Springer JE. A mapping study of caspase-3 activation following acute spinal cord contusion in rats. J Histochem Cytochem 2005, 53:809-819. 10.1369/jhc.4A6467.2005, 15995139.
13. Millecamps S, Robertson J, Lariviere R, Mallet J, Julien JP. Defective axonal transport of neurofilament proteins in neurons overexpressing peripherin. J Neurochem 2006, 98:926-938. 10.1111/j.1471-4159.2006.03932.x, 16787413.
14. Vucic S, Kiernan MC. Novel threshold tracking techniques suggest that cortical hyperexcitability is an early feature of motor neuron disease. Brain 2006, 129:2436-2446. 10.1093/brain/awl172, 16835248.
15. Al-Chalabi A, Andersen PM, Nilsson P, Chioza B, Andersson JL, Russ C, Shaw CE, Powell JF, Leigh PN. Deletions of the heavy neurofilament subunit tail in amyotrophic lateral sclerosis. Hum Mol Genet 1999, 8:157-164. 10.1093/hmg/8.2.157, 9931323.
16. Brettschneider J, Petzold A, Sussmuth SD, Ludolph AC, Tumani H. Axonal damage markers in cerebrospinal fluid are increased in ALS. Neurology 2006, 66:852-856. 10.1212/01.wnl.0000203120.85850.54, 16567701.
17. Sharp PS, Dick JR, Greensmith L. The effect of peripheral nerve injury on disease progression in the SOD1(G93A) mouse model of amyotrophic lateral sclerosis. Neuroscience 2005, 130:897-910. 10.1016/j.neuroscience.2004.09.069, 15652988.
18. Farooque M, Zhang Y, Holtz A, Olsson Y. Exudation of fibronectin and albumin after spinal cord injury in rats. Acta Neuropathol 1992, 84:613-620. 10.1007/BF00227738, 1471470.
19. Nystrom B, Berglund JE, Bergquist E. Methodological analysis of an experimental spinal cord compression model in the rat. Acta Neurol Scand 1988, 78:460-466. 10.1111/j.1600-0404.1988.tb03688.x, 3223232.
20. Basso DM, Beattie MS, Bresnahan JC. Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection. Exp Neurol 1996, 139:244-256. 10.1006/exnr.1996.0098, 8654527.
21. Zeeberg BR, Qin H, Narasimhan S, Sunshine M, Cao H, Kane DW, Reimers M, Stephens RM, Bryant D, Burt SK, Elnekave E, Hari DM, Wynn TA, Cunningham-Rundles C, Stewart DM, Nelson D, Weinstein JN. High-Throughput GoMiner, an 'industrial-strength' integrative gene ontology tool for interpretation of multiple-microarray experiments, with application to studies of Common Variable Immune Deficiency (CVID). BMC Bioinformatics 2005, 6:168. 10.1186/1471-2105-6-168, 1190154, 15998470.
22. Di GS, Knoblach SM, Brandoli C, Aden SA, Hoffman EP, Faden AI. Gene profiling in spinal cord injury shows role of cell cycle in neuronal death. Ann Neurol 2003, 53:454-468. 10.1002/ana.10472, 12666113.
23. Sifringer M, Stefovska V, Zentner I, Hansen B, Stepulak A, Knaute C, Marzahn J, Ikonomidou C. The role of matrix metalloproteinases in infant traumatic brain injury. Neurobiol Dis 2007, 25:526-535. 10.1016/j.nbd.2006.10.019, 17188498.
24. Fitzpatrick MO, Dewar D, Teasdale GM, Graham DI. The neuronal cytoskeleton in acute brain injury. Br J Neurosurg 1998, 12:313-317. 10.1080/02688699844808, 10070422.
25. Gobbel GT, Bonfield C, Carson-Walter EB, Adelson PD. Diffuse alterations in synaptic protein expression following focal traumatic brain injury in the immature rat. Childs Nerv Syst 2007, 23:1171-1179. 10.1007/s00381-007-0345-2, 17457592.
26. Clark AK, Yip PK, Grist J, Gentry C, Staniland AA, Marchand F, Dehvari M, Wotherspoon G, Winter J, Ullah J, Bevan S, Malcangio M. Inhibition of spinal microglial cathepsin S for the reversal of neuropathic pain. Proc Natl Acad Sci USA 2007, 104:10655-10660. 10.1073/pnas.0610811104, 1965568, 17551020.
27. Starkey ML, Davies M, Yip PK, Carter LM, Wong DJ, McMahon SB, Bradbury EJ. Expression of the regeneration-associated protein SPRR1A in primary sensory neurons and spinal cord of the adult mouse following peripheral and central injury. J Comp Neurol 2009, 513:51-68. 10.1002/cne.21944, 19107756.
28. Gonzalez SL, Saravia F, Gonzalez Deniselle MC, Lima AE, De Nicola AF. Glucocorticoid regulation of motoneuronal parameters in rats with spinal cord injury. Cell Mol Neurobiol 1999, 19:597-611. 10.1023/A:1006980301382, 10384258.
29. Holtz A, Nystrom B, Gerdin B, Olsson Y. Neuropathological changes and neurological function after spinal cord compression in the rat. J Neurotrauma 1990, 7:155-167. 10.1089/neu.1990.7.155, 2258946.
30. Zhang Y, Hillered L, Olsson Y, Holtz A. Time course of energy perturbation after compression trauma to the spinal cord: an experimental study in the rat using microdialysis. Surg Neurol 1993, 39:297-304. 10.1016/0090-3019(93)90009-P, 8488449.
31. Goldstein JC, Munoz-Pinedo C, Ricci JE, Adams SR, Kelekar A, Schuler M, Tsien RY, Green DR. Cytochrome c is released in a single step during apoptosis. Cell Death Differ 2005, 12:453-462. 10.1038/sj.cdd.4401596, 15933725.
32. Graf M, Ecker D, Horowski R, Kramer B, Riederer P, Gerlach M, Hager C, Ludolph AC, Becker G, Osterhage J, Jost WH, Schrank B, Stein C, Kostopulos P, Lubik S, Wekwerth K, Dengler R, Troeger M, Wuerz A, Hoge A, Schrader C, Schimke N, Krampfl K, Petri S, Zierz S, Eger K, Neudecker S, Traufeller K, Sievert M, Neundorfer B, Hecht M. High dose vitamin E therapy in amyotrophic lateral sclerosis as add-on therapy to riluzole: results of a placebo-controlled double-blind study. J Neural Transm 2005, 112:649-660. 10.1007/s00702-004-0220-1, 15517433.
33. Halliwell B. Role of free radicals in the neurodegenerative diseases: therapeutic implications for antioxidant treatment. Drugs Aging 2001, 18:685-716. 10.2165/00002512-200118090-00004, 11599635.
34. Dupuis L, Corcia P, Fergani A, Gonzalez De Aguilar JL, Bonnefont-Rousselot D, Bittar R, Seilhean D, Hauw JJ, Lacomblez L, Loeffler JP, Meininger V. Dyslipidemia is a protective factor in amyotrophic lateral sclerosis. Neurology 2008, 70:1004-1009. 10.1212/01.wnl.0000285080.70324.27, 18199832.
35. Corcoran J, So PL, Maden M. Absence of retinoids can induce motoneuron disease in the adult rat and a retinoid defect is present in motoneuron disease patients. J Cell Sci 2002, 115:4735-4741. 10.1242/jcs.00169, 12432062.
36. Jokic N, Ling YY, Ward RE, Michael-Titus AT, Priestley JV, Malaspina A. Retinoid receptors in chronic degeneration of the spinal cord: observations in a rat model of amyotrophic lateral sclerosis. J Neurochem 2007, 103:1821-1833. 10.1111/j.1471-4159.2007.04893.x, 17956549.
37. Malaspina A, Turkheimer F. A review of the functional role and of the expression profile of retinoid signaling and of nuclear receptors in human spinal cord. Brain Res Bull 2007, 71:437-446. 10.1016/j.brainresbull.2006.10.032, 17259011.
38. Malaspina A, Michael-Titus AT. Is the modulation of retinoid and retinoid-associated signaling a future therapeutic strategy in neurological trauma and neurodegeneration?. J Neurochem 2008, 104:584-595.
39. Shojo H, Kibayashi K. Changes in localization of synaptophysin following fluid percussion injury in the rat brain. Brain Res 2006, 1078:198-211. 10.1016/j.brainres.2006.01.063, 16497279.
40. Garcia ML, Cleveland DW. Going new places using an old MAP: tau, microtubules and human neurodegenerative disease. Curr Opin Cell Biol 2001, 13:41-48. 10.1016/S0955-0674(00)00172-1, 11163132.
41. Suzuki M, Klein S, Wetzel EA, Meyer M, McHugh J, Tork C, Hayes A, Svendsen CN. Acute glial activation by stab injuries does not lead to overt damage or motor neuron degeneration in the G93A mutant SOD1 rat model of amyotrophic lateral sclerosis. Exp Neurol 2010, 221:346-352. 10.1016/j.expneurol.2009.12.004, 20005223.
42. Zang DW, Cheema SS. Degeneration of corticospinal and bulbospinal systems in the superoxide dismutase 1(G93A G1H) transgenic mouse model of familial amyotrophic lateral sclerosis. Neurosci Lett 2002, 332:99-102. 10.1016/S0304-3940(02)00944-8, 12384220.
43. Feeney SJ, McKelvie PA, Austin L, Jean-Francois MJ, Kapsa R, Tombs SM, Byrne E. Presymptomatic motor neuron loss and reactive astrocytosis in the SOD1 mouse model of amyotrophic lateral sclerosis. Muscle Nerve 2001, 24:1510-1519. 10.1002/mus.1176, 11745954.
44. Cassina P, Cassina A, Pehar M, Castellanos R, Gandelman M, de LA, Robinson KM, Mason RP, Beckman JS, Barbeito L, Radi R. Mitochondrial dysfunction in SOD1G93A-bearing astrocytes promotes motor neuron degeneration: prevention by mitochondrial-targeted antioxidants. J Neurosci 2008, 28:4115-4122. 10.1523/JNEUROSCI.5308-07.2008, 18417691.
45. Lepore AC, Rauck B, Dejea C, Pardo AC, Rao MS, Rothstein JD, Maragakis NJ. Focal transplantation-based astrocyte replacement is neuroprotective in a model of motor neuron disease. Nat Neurosci 2008, 11:1294-1301. 10.1038/nn.2210, 2656686, 18931666.
46. Lepore AC, Tolmie C, O'Donnell J, Wright MC, Dejea C, Rauck B, Hoke A, Ignagni AR, Onders RP, Maragakis NJ. Peripheral hyperstimulation alters site of disease onset and course in SOD1 rats. Neurobiol Dis 2010, 39:252-264. 10.1016/j.nbd.2010.03.021, 20381620.
47. Malaspina A, Ngoh SF, Ward RE, Hall JC, Tai FW, Yip PK, Jones C, Jokic N, Averill SA, Michael-Titus AT, Priestley JV. Activation transcription factor-3 activation and the development of spinal cord degeneration in a rat model of amyotrophic lateral sclerosis. Neuroscience 2010, 169:812-827. 10.1016/j.neuroscience.2010.04.053, 20470869.
48. Woodruff TM, Costantini KJ, Crane JW, Atkin JD, Monk PN, Taylor SM, Noakes PG. The complement factor C5a contributes to pathology in a rat model of amyotrophic lateral sclerosis. J Immunol 2008, 181:8727-8734.
49. Nagai M, Aoki M, Miyoshi I, Kato M, Pasinelli P, Kasai N, Brown RH, Itoyama Y. Rats expressing human cytosolic copper-zinc superoxide dismutase transgenes with amyotrophic lateral sclerosis: associated mutations develop motor neuron disease. J Neurosci 2001, 21:9246-9254.
50. Sugawara T, Noshita N, Lewen A, Gasche Y, Ferrand-Drake M, Fujimura M, Morita-Fujimura Y, Chan PH. Overexpression of copper/zinc superoxide dismutase in transgenic rats protects vulnerable neurons against ischemic damage by blocking the mitochondrial pathway of caspase activation. J Neurosci 2002, 22:209-217.
51. Hahn CM, Kleinholz H, Koester MP, Grieser S, Thelen K, Pollerberg GE. Role of cyclin-dependent kinase 5 and its activator P35 in local axon and growth cone stabilization. Neuroscience 2005, 134:449-465. 10.1016/j.neuroscience.2005.04.020, 15964697.
52. Huang WL, King VR, Curran OE, Dyall SC, Ward RE, Lal N, Priestley JV, Michael-Titus AT. A combination of intravenous and dietary docosahexaenoic acid significantly improves outcome after spinal cord injury. Brain 2007, 130:3004-3019. 10.1093/brain/awm223, 17901087.
53. Debus E, Weber K, Osborn M. Monoclonal antibodies specific for glial fibrillary acidic (GFA) protein and for each of the neurofilament triplet polypeptides. Differentiation 1983, 25:193-203. 10.1111/j.1432-0436.1984.tb01355.x, 6198232.
54. Ruscheweyh R, Forsthuber L, Schoffnegger D, Sandkuhler J. Modification of classical neurochemical markers in identified primary afferent neurons with Abeta-, Adelta-, and C-fibers after chronic constriction injury in mice. J Comp Neurol 2007, 502:325-336. 10.1002/cne.21311, 17348016.
55. Saganova K, Orendacova J, Cizkova D, Vanicky I. Limited minocycline neuroprotection after balloon-compression spinal cord injury in the rat. Neurosci Lett 2008, 433:246-249. 10.1016/j.neulet.2008.01.041, 18280653.
56. Zelano J, Berg A, Thams S, Hailer NP, Cullheim S. SynCAM1 expression correlates with restoration of central synapses on spinal motoneurons after two different models of peripheral nerve injury. J Comp Neurol 2009, 517:670-682. 10.1002/cne.22186, 19827159.
57. Yip PK, Wong LF, Sears TA, Yanez-Munoz RJ, McMahon SB. Cortical overexpression of neuronal calcium sensor-1 induces functional plasticity in spinal cord following unilateral pyramidal tract injury in rat. PLoS Biol 2010, 8:e1000399. 10.1371/journal.pbio.1000399, 2889931, 20585375.