Stage dependent effects of progesterone on motoneurons and glial cells of wobbler mouse spinal cord degeneration

Cellular and Molecular Neurobiology

Volumn 30, Issue 1, 2010, Pages 123-135

  Meyer, Maria ^a   Gonzalez Deniselle, Maria Claudia ^a,b   Garay, Laura I ^a,b   Monachelli, Gisella Gargiulo ^a   Lima, Analia ^a   Roig, Paulina ^a   Guennoun, Rachida ^c   Schumacher, Michael ^c   De Nicola, Alejandro F ^a  

^a Universidad Nacional de Río Cuarto Consejo Nacional de Investigaciones Científicas y Técnicas   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Glial fibrillary acidic protein; Glutamine synthetase; Neurodegeneration; Neuroprotection; Progesterone; Wobbler

Indexed keywords

CHOLINE ACETYLTRANSFERASE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE AMMONIA LIGASE; MESSENGER RNA; NEUROMODULIN; PROGESTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEGENERATION; CHRONOTHERAPY; CONTROLLED STUDY; DISEASE COURSE; DRUG EFFICACY; FEMALE; GENOTYPE; GLIA CELL; MALE; MOUSE; MOUSE MUTANT; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL CORD ATROPHY; SPINAL CORD MOTONEURON; WILD TYPE; WOBBLER MOUSE;

ANIMALS; ANTERIOR HORN CELLS; ASTROCYTES; CELL COUNT; CHOLINE O-ACETYLTRANSFERASE; DISEASE MODELS, ANIMAL; FEMALE; GAP-43 PROTEIN; GENE EXPRESSION REGULATION; GENOTYPE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE-AMMONIA LIGASE; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; MICE; MICE, NEUROLOGIC MUTANTS; MOTOR NEURONS; NEUROGLIA; PROGESTERONE; RNA, MESSENGER; SPINAL CORD; SPINAL CORD DISEASES;

MUS;

EID: 76749135687     PISSN: 02724340     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10571-009-9437-8     Document Type: Article

References (81)

1. I Azcoitia E Leonelli V Magnaghi S Veiga LM Garcia Segura R Melcangi 2003 Progesterone and its derivatives dihydroprogesterone and tetrahydroprogesterone reduce myelin fiber morphological abnormalities and myelin fiber loss in the sciatic nerve of aged rats Neurobiol Aging 24 853 860 10.1016/S0197-4580(02) 00234-8 12927767 (Pubitemid 37288858)
2. LH Barbeito M Pehar P Cassina MR Vargas H Peluffo L Viera AG Estévez JS Beckman 2004 A role for astrocytes in motor neuron loss in amyotrophic lateral sclerosis Brain Res Rev 47 263 274 10.1016/j.brainresrev. 2004.05.003 15572176 (Pubitemid 39574324)
3. EE Benarroch 2005 Neuron-astrocyte interactions: partnership for normal function and disease in the central nervous system Mayo Clin Proc 80 1326 1338 10.4065/80.10.1326 16212146
4. LI Benowitz A Routtenberg 1997 GAP-43: an intrinsic determinant of neuronal development and plasticity Trends Neurosci 20 84 91 10.1016/S0166-2236(96)10072-2 9023877 (Pubitemid 27050703)
5. P Bigini A Bastone T Mennini 2001 Glutamate transporters in the spinal cord of the wobbler mouse NeuroReport 12 1815 1820 10.1097/00001756-200107030- 00011 11435904
6. P Bigini F Gardoni S Barbera A Cagnotto E Fumagalli A Longhi MM Corsi M Di Luca T Mennini 2006 Expression of AMPA and NMDA receptor subunits in the cervical spinal cord of wobbler mice BMC Neurosci 26 7 71
7. P Bigini C Atzori E Fumagalli A Cagnotto S Barbera A Migheli T Mennini 2007 Lack of caspase-dependent apoptosis in spinal motor neurons of the wobbler mouse Neurosci Lett 426 106 110 10.1016/j.neulet.2007.08.057 17890007 (Pubitemid 47464708)
8. B Blondet D Hantaz-Ambroise A Aït-Ikhlef D Cambier M Murawsky F Rieger 1995 Astrocytosis in wobbler mouse spinal cord involves a population of astrocytes which is glutamine synthetase-negative Neurosci Lett 183 179 182 10.1016/0304-3940(94)11145-9 7739788
9. S Boillée L Viala M Peschanski PA Dreyfus 2001 Differential microglial response to progressive neurodegeneration in the murine mutant wobbler Glia 33 277 287 10.1002/1098-1136(20010315)33:4<277::AID- GLIA1026>3.0.CO;2-Y 11246226 (Pubitemid 32285744)
10. S Boillée M Peschanski MP Junier 2003 The wobbler mouse: a neurodegeneration jigsaw puzzle Mol Neurobiol 28 65 106 10.1385/MN:28:1:65 14514986 (Pubitemid 38165332)
11. V Boonyaratanakornkit Y Bi M Rudd DP Edwards 2008 The role and mechanism of progesterone receptor activation of extra-nuclear signaling pathways in regulating gene transcription and cell cycle progression Steroids 73 922 928 10.1016/j.steroids.2008.01.010 18321550
12. RD Brinton 2008 The healthy cell bias of estrogen action: mitochondrial bioenergetics and neurological implications Trends Neurosci 31 529 537 10.1016/j.tins.2008.07.003 18774188
13. V Calabrese C Mancuso M Calvani E Rizzarelli DA Butterfield AM Stella 2007 Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity Nat Rev Neurosci 8 766 775 10.1038/nrn2214 17882254 (Pubitemid 47462116)
14. W Cammer 1990 Glutamine synthetase in the central nervous system is not confined to astrocytes J Neuroimmunol 26 173 178 10.1016/0165-5728(90)90088-5 1688879 (Pubitemid 20023724)
15. I Ciriza I Azcoitia LM Garcia-Segura 2004 Reduced progesterone metabolites protect rat hippocampal neurones from kainic acid excitotoxicity in vivo J Neuroendocrinol 16 58 63 10.1111/j.1365-2826.2004.01121.x 14962077 (Pubitemid 38159394)
16. PG Clarke 1990 Developmental cell death: morphological diversity and multiple mechanisms Anat Embryol (Berl) 181 195 213
17. DW Cleveland JD Rothstein 2001 From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS Nat Rev Neurosci 2 806 819 10.1038/35097565 11715057 (Pubitemid 33674062)
18. GJ Clowry S McHanwell 1996 Expression of nitric oxide synthase by motor neurones in the spinal cord of the mutant mouse wobbler Neurosci Lett 215 177 180 10.1016/0304-3940(96)12971-2 8899742
19. V Corvino R Businaro MC Geloso P Bigini V Cavallo E Pompili T Mennini L Fumagalli F Michetti 2003 S100B protein and 4-hydroxynonenal in the spinal cord of wobbler mice Neurochem Res 28 341 345 10.1023/A:1022345720852 12608707 (Pubitemid 36207358)
20. ME Cudkowicz RH Brown Jr 1996 An update on superoxide dismutase 1 in familial amyotrophic lateral sclerosis J Neurol Sci 139 Suppl 10 15 10.1016/0022-510X(96)00084-6 8899652 (Pubitemid 26323574)
21. KR Dave WG Bradley MA Pérez-Pinzón 2003 Early mitochondrial dysfunction occurs in motor cortex and spinal cord at the onset of disease in the wobbler mouse Exp Neurol 182 412 420 10.1016/S0014-4886(03)00091-8 12895451 (Pubitemid 36937093)
22. AF De Nicola SL Gonzalez F Labombarda MC Gonzalez Deniselle L Garay R Guennoun M Schumacher 2006 Progesterone treatment of spinal cord injury: effects on receptors, neurotrophins, and myelination J Mol Neurosci 28 3 15 10.1385/JMN:28:1:3 16632872 (Pubitemid 43780334)
23. JS Dennis BA Citron 2009 Wobbler mice modeling motor neuron disease display elevated transactive response DNA binding protein Neuroscience 158 745 750 10.1016/j.neuroscience.2008.10.030 19013502
24. M Djebaili Q Guo EH Pettus SW Hoffman DG Stein 2005 The neurosteroids progesterone and allopregnanolone reduce cell death, gliosis, and functional deficits after traumatic brain injury J Neurotrauma 22 106 118 10.1089/neu.2005.22.106 15665606
25. EJ Elliott DA Parks PS Fishman 1997 Effect of proximal axotomy on GAP-43 expression in cortical neurons in the mouse Brain Res 755 221 228 10.1016/S0006-8993(97)00100-5 9175890 (Pubitemid 27196328)
26. M Ferrini A Lima AF De Nicola 1995 Estradiol abolishes autologous down regulation of glucocorticoid receptors in brain Life Sci 57 2403 2412 10.1016/0024-3205(95)02236-3 8847961
27. E Fumagalli P Bigini S Barbera M De Paola T Mennini 2006 Riluzole, unlike the AMPA antagonist RPR119990, reduces motor impairment and partially prevents motoneuron death in the wobbler mouse, a model of neurodegenerative disease Exp Neurol 198 114 128 10.1016/j.expneurol.2005.11.010 16386734 (Pubitemid 43243750)
28. N Gago M El-Etr N Sananès F Cadepond D Samuel V Avellana-Adalid A Baron-VanEvercooren M Schumacher 2004 3alpha, 5alpha tetrahydroprogesterone (allopregnanolone) and gamma-aminobutyric acid: autocrine/paracrine interactions in the control of neonatal PSA-NCAM+ progenitor proliferation J Neurosci Res 78 770 783 10.1002/jnr.20348 15523635 (Pubitemid 39657565)
29. L Garay MC Gonzalez Deniselle A Lima P Roig AF De Nicola 2007 Effects of progesterone in the spinal cord of a mouse model of multiple sclerosis J Steroid Biochem Mol Biol 107 228 237 10.1016/j.jsbmb.2007.03.040 17692515 (Pubitemid 47381578)
30. AM Ghoumari C Ibanez M El-Etr F Leclerc B Eychenne EE Baulieu M Schumacher 2003 Progesterone and its metabolites increase myelination in organotypic slice cultures of rat cerebellum J Neurochem 86 848 859 10.1046/j.1471-4159.2003.01881.x 12887683 (Pubitemid 36988797)
31. C Giulivi JJ Poderoso A Boveris 1998 Production of nitric oxide by mitochondria J Biol Chem 273 11038 11043 10.1074/jbc.273.18.11038 9556586 (Pubitemid 28204947)
32. MC Gonzalez Deniselle S Lavista-Llanos MG Ferrini AE Lima AG Roldán AF De Nicola 1999 In vitro differences between astrocytes of control and wobbler mice spinal cord Neurochem Res 24 1535 1541 10.1023/A:1021199931682
33. MC Gonzalez Deniselle CA Grillo S Gonzalez P Roig AF De Nicola 1999 Evidence for down-regulation of GAP-43 mRNA in wobbler mouse spinal motoneurons by corticosterone and a 21-aminosteroid Brain Res 841 78 84 10.1016/S0006- 8993(99)01783-7 10546990 (Pubitemid 29441002)
34. MC Gonzalez Deniselle JJ López-Costa JP Saavedra L Pietranera SL Gonzalez L Garay R Guennoun M Schumacher AF De Nicola 2002 Progesterone neuroprotection in the wobbler mouse, a genetic model of spinal cord motor neuron disease Neurobiol Dis 11 457 468 10.1006/nbdi.2002.0564 12586554 (Pubitemid 36269130)
35. MC Gonzalez Deniselle L Garay JJ López-Costa S González A Mougel R Guennoun M Schumacher AF De Nicola 2004 Progesterone treatment reduces NADPH-diaphorase/nitric oxide synthase in wobbler mouse motoneuron disease Brain Res 1014 71 79 10.1016/j.brainres.2004.04.004 15212993 (Pubitemid 38798454)
36. MC Gonzalez Deniselle L Garay S Gonzalez R Guennoun M Schumacher AF De Nicola 2005 Progesterone restores retrograde labeling of cervical motoneurons in Wobbler mouse motoneuron disease Exp Neurol 195 518 523 10.1016/j.expneurol. 2005.06.015 16095593 (Pubitemid 41297802)
37. MC Gonzalez Deniselle L Garay S Gonzalez F Saravia F Labombarda R Guennoun M Schumacher AF De Nicola 2007 Progesterone modulates brain-derived neurotrophic factor and choline acetyltransferase in degenerating wobbler motoneurons Exp Neurol 203 406 414 10.1016/j.expneurol.2006.08.019 17052708 (Pubitemid 46164803)
38. R Guennoun D Meffre F Labombarda SL Gonzalez MC Gonzalez Deniselle DG Stein AF De Nicola M Schumacher 2008 The membrane-associated progesterone-binding protein 25-Dx: expression, cellular localization and up-regulation after brain and spinal cord injuries Brain Res Rev 57 493 505 10.1016/j.brainresrev.2007.05.009 17618691
39. D Hantaz-Ambroise C Jacque A Aït Ikhlef C Parmentier P Leclerc D Cambier G Zadigue F Rieger 2001 Specific features of chronic astrocyte gliosis after experimental central nervous system (CNS) xenografting and in wobbler neurological mutant CNS Differentiation 69 100 107 10.1046/j.1432-0436.2001. 690204.x 11798064
40. JT Henderson M Javaheri S Kopko JC Roder 1996 Reduction of lower motor neuron degeneration in wobbler mice by n-acetyl-l-cysteine J Neurosci 16 7574 7582 8922414
41. K Ikeda Y Iwasaki M Kinoshita S Marubuchi S Ono 2000 T-588, a novel neuroprotective agent, delays progression of neuromuscular dysfunction in wobbler mouse motoneuron disease Brain Res 858 84 91 10.1016/S0006-8993(99) 02427-0 10700601 (Pubitemid 30105786)
42. A Ikemoto A Hirano I Akiguchi 1999 Increased expression of growth-associated protein 43 on the surface of the anterior horn cells in amyotrophic lateral sclerosis Acta Neuropathol 98 367 373 10.1007/s004010051096 10502042 (Pubitemid 29440683)
43. T Ishiyama H Ogo V Wong B Klinkosz H Noguchi C Nakayama H Mitsumoto 2002 Methionine-free brain derived neurotrophic factor in wobbler mouse motor neuron disease: dose-related effects and comparison with the methionyl form Brain Res 944 195 199 10.1016/S0006-8993(02)02881-0 12106680 (Pubitemid 34775022)
44. T Ishiyama R Okada H Nishibe H Mitsumoto C Nakayama 2004 Riluzole slows the progression of neuromuscular dysfunction in the wobbler mouse motor neuron disease Brain Res 1019 226 236 10.1016/j.brainres.2004.06.002 15306257 (Pubitemid 39078628)
45. T Ishrat I Sayeed F Atif DG Stein 2009 Effects of progesterone administration on infarct volume and functional deficits following permanent focal cerebral ischemia in rats Brain Res 1257 94 101 10.1016/j.brainres.2008. 12.048 19135987
46. JP Julien 2007 ALS: astrocytes move in as deadly neighbors Nat Neurosci 10 535 537 10.1038/nn0507-535 17453052 (Pubitemid 46652429)
47. JP Kapfhammer ME Schwab 1994 Inverse patterns of myelination and GAP-43 expression in the adult CNS: neurite growth inhibitors as regulators of neuronal plasticity? J Comp Neurol 340 194 206 10.1002/cne.903400206 8201019
48. J Kong Z Xu 1998 Massive mitochondrial degeneration in motor neurons triggers the onset of amyotrophic lateral sclerosis in mice expressing a mutant SOD1 J Neurosci 18 3241 3250 9547233
49. S Laage G Zobel H Jockusch 1988 Astrocyte overgrowth in the brain stem and spinal cord of mice affected by spinal atrophy, wobbler Dev Neurosci 10 190 198 10.1159/000111969 3142758
50. F Labombarda R Guennoun S Gonzalez P Roig A Lima M Schumacher AF De Nicola 2000 Immunocytochemical evidence for a progesterone receptor in neurons and glial cells of the rat spinal cord Neurosci Lett 288 29 32 10.1016/S0304-3940(00)01191-5 10869808 (Pubitemid 30408431)
51. F Labombarda SL Gonzalez MC Gonzalez Deniselle GP Vinson M Schumacher AF De Nicola R Guennoun 2003 Effects of injury and progesterone treatment on progesterone receptor and progesterone binding protein 25-Dx expression in the rat spinal cord J Neurochem 87 902 913 10.1046/j.1471-4159.2003.02055.x 14622121 (Pubitemid 37444566)
52. M Leist M Jäättelä 2001 Four deaths and a funeral: from caspases to alternative mechanisms Nat Rev Mol Cell Biol 2 589 598 10.1038/35085008 11483992 (Pubitemid 33674010)
53. LJ Martin Z Liu K Chen AC Price Y Pan JA Swaby WC Golden 2007 Motor neuron degeneration in amyotrophic lateral sclerosis mutant superoxide dismutase-1 transgenic mice: mechanisms of mitochondriopathy and cell death J Comp Neurol 500 20 46 10.1002/cne.21160 17099894 (Pubitemid 44904300)
54. A Migheli C Atzori R Piva M Tortarolo M Girelli D Schiffer C Bendotti 1999 Lack of apoptosis in mice with ALS Nat Med 5 966 967 10.1038/12381 10470053 (Pubitemid 29439556)
55. A Migliaccio D Piccolo G Castoria M Di Domenico A Bilancio M Lombardi W Gong M Beato F Auricchio 1998 Activation of the Src/p21ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor EMBO J 17 2008 2018 10.1093/emboj/17.7.2008 9524123 (Pubitemid 28154530)
56. H Mitsumoto AL Boggs 1987 Vacuolated anterior horn cells in wobbler mouse motor neuron disease: peripheral axons and regenerative capacity J Neuropathol Exp Neurol 46 214 222 10.1097/00005072-198703000-00008 3819775
57. H Mitsumoto K Ikeda B Klinkosz JM Cedarbaum V Wong RM Lindsay 1994 Arrest of motor neuron disease in wobbler mice cotreated with CNTF and BDNF Science 265 1052 1053 10.1126/science.8066451
58. S Moncada JP Bolaños 2006 Nitric oxide, cell bioenergetics and neurodegeneration J Neurochem 97 1676 1689 10.1111/j.1471-4159.2006.03988.x 16805776 (Pubitemid 43873660)
59. Y Oda S Imai I Nakanishi T Ichikawa T Deguchi 1995 Immunohistochemical study on choline acetyltransferase in the spinal cord of patients with amyotrophic lateral sclerosis Pathol Int 45 933 939 10.1111/j.1440-1827.1995. tb03418.x 8808298
60. SB Pajovićs ZS Saicić 2008 Modulation of antioxidant enzyme activities by sexual steroid hormones Physiol Res 57 801 811
61. IM Parhad R Oishi AW Clark 1992 GAP-43 gene expression is increased in anterior horn cells of amyotrophic lateral sclerosis Ann Neurol 31 593 597 10.1002/ana.410310605 1387517
62. P Popper DB Farber PE Micevych K Minoofar JM Bronstein 1997 TRPM-2 expression and tunel staining in neurodegenerative diseases: studies in wobbler and rd mice Exp Neurol 143 246 254 10.1006/exnr.1996.6364 9056387 (Pubitemid 27148229)
63. S Rathke-Hartlieb VC Schmidt H Jockusch T Schmitt-John JW Bartsch 1999 Spatiotemporal progression of neurodegeneration and glia activation in the wobbler neuropathy of the mouse NeuroReport 10 3411 3416 10.1097/00001756- 199911080-00028 10599854
64. RL Roof ED Hall 2000 Gender differences in acute CNS trauma and stroke: neuroprotective effects of estrogen and progesterone J Neurotrauma 17 367 388 10.1089/neu.2000.17.367 10833057
65. RL Roof SW Hoffman DG Stein 1997 Progesterone protects against lipid peroxidation following traumatic brain injury in rats Mol Chem Neuropathol 31 1 11 10.1007/BF02815156 9271001
66. JD Rothstein M Van Kammen AI Levey LJ Martin RW Kuncl 1995 Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis Ann Neurol 38 73 84 10.1002/ana.410380114 7611729
67. B Santoros P Bigini G Levandis V Nobile M Biggiogera F Botti T Mennini D Curti 2004 Evidence for chronic mitochondrial impairment in the cervical spinal cord of a murine model of motor neuron disease Neurobiol Dis 17 349 357 10.1016/j.nbd.2004.07.003 (Pubitemid 39345790)
68. F Saravia J Beauquis L Pietranera AF De Nicola 2007 Neuroprotective effects of estradiol in hippocampal neurons and glia of middle age mice Psychoneuroendocrinology 32 480 492 10.1016/j.psyneuen.2007.02.012 17459595 (Pubitemid 46756004)
69. T Schmitt-John C Drepper A Mussmann P Hahn M Kuhlmann C Thiel M Hafner A Lengeling P Heimann JM Jones MH Meisler H Jockusch 2005 Mutation of Vps54 causes motor neuron disease and defective spermiogenesis in the wobbler mouse Nat Genet 37 1213 1215 10.1038/ng1661 16244655 (Pubitemid 41568703)
70. M Schumacher R Guennoun DG Stein AF De Nicola 2007 Progesterone: therapeutic opportunities for neuroprotection and myelin repair Pharmacol Ther 116 77 106 10.1016/j.pharmthera.2007.06.001 17659348 (Pubitemid 47398920)
71. S Sperandio I de Belle DE Bredesen 2000 An alternative, nonapoptotic form of programmed cell death Proc Natl Acad Sci U S A 97 14376 14381 10.1073/pnas.97.26.14376 11121041 (Pubitemid 32016583)
72. DG Stein 2008 Progesterone exerts neuroprotective effects after brain injury Brain Res Rev 57 386 397 10.1016/j.brainresrev.2007.06.012 17826842
73. FA Tansey M Farooq W Cammer 1991 Glutamine synthetase in oligodendrocytes and astrocytes: new biochemical and immunocytochemical evidence J Neurochem 56 266 272 10.1111/j.1471-4159.1991.tb02591.x 1670954
74. AJ Thomas RP Nockels HQ Pan CI Shaffrey M Chopp 1999 Progesterone is neuroprotective after acute experimental spinal cord trauma in rats Spine 24 2134 2138 10.1097/00007632-199910150-00013 10543012 (Pubitemid 29489429)
75. K Tsuzaka T Ishiyama EP Pioro H Mitsumoto 2001 Role of brain-derived neurotrophic factor in wobbler mouse motor neuron disease Muscle Nerve 24 474 480 10.1002/mus.1029 11268018 (Pubitemid 32246782)
76. L Vardimon I Ben-Dror N Avisar A Oren L Shiftan 1999 Glucocorticoid control of glial gene expression J Neurobiol 40 513 527 10.1002/(SICI)1097- 4695(19990915)40:4<513::AID-NEU8>3.0.CO;2-D 10453053 (Pubitemid 29400057)
77. GP Xu KR Dave CT Moraes R Busto TJ Sick WG Bradley MA Pérez-Pinzón 2001 Dysfunctional mitochondrial respiration in the wobbler mouse brain Neurosci Lett 300 141 144 10.1016/S0304-3940(01)01575-0 11226631 (Pubitemid 32168207)
78. KK Yung F Tang R Fielding YH Du LL Vacca-Galloway 1992 Alteration in the levels of thyrotropin releasing hormone, substance P and enkephalins in the spinal cord, brainstem, hypothalamus and midbrain of the wobbler mouse at different stages of the motoneuron disease Neuroscience 50 209 222 10.1016/0306-4522(92)90393-G 1383870
79. Y Zhu RN Hanna MJ Schaaf HP Spaink P Thomas 2008 Candidates for membrane progestin receptors-past approaches and future challenges Comp Biochem Physiol C Toxicol Pharmacol 148 381 389 10.1016/j.cbpc.2008.05.019 18602498
80. S Zoccolella E Beghis G Palaganos A Fraddosio V Guerra V Samarelli V Lepore IL Simone P Lamberti L Serlenga G Logroscino SLAP registry 2007 Riluzole and amyotrophic lateral sclerosis survival: a population-based study in southern Italy Eur J Neurol 14 262 268 17355545 (Pubitemid 46384853)
81. MC Zoing D Burke R Pamphlett MC Kiernan 2006 Riluzole therapy for motor neurone disease: an early Australian experience (1996-2002) J Clin Neurosci 13 78 83 10.1016/j.jocn.2004.04.011 16410201 (Pubitemid 43061132)