Stage dependent effects of progesterone on motoneurons and glial cells of wobbler mouse spinal cord degeneration
In the Wobbler mouse, a mutation in the Vps54 gene is accompanied by motoneuron degeneration and astrogliosis in the cervical spinal cord. Previous work has shown that these abnormalities are greatly attenuated by progesterone treatment of clinically afflicted Wobblers. However, whether progesterone...
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2010
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| Sumario: | In the Wobbler mouse, a mutation in the Vps54 gene is accompanied by motoneuron degeneration and astrogliosis in the cervical spinal cord. Previous work has shown that these abnormalities are greatly attenuated by progesterone treatment of clinically afflicted Wobblers. However, whether progesterone is effective at all disease stages has not yet been tested. The present work used genotyped (wr/wr) Wobbler mice at three periods of the disease: early progressive (1-2 months), established (5-8 months) or late stages (12 months) and age-matched wildtype controls (NFR/NFR), half of which were implanted with a progesterone pellet (20 mg) for 18 days. In untreated Wobblers, degenerating vacuolated motoneurons were initially abundant, experienced a slight reduction at the established stage and dramatically diminished during the late period. In motoneurons, the cholinergic marker choline acetyltransferase (ChAT) was reduced at all stages of the Wobbler disease, whereas hyperexpression of the growth-associated protein (GAP43) mRNA preferentially occurred at the early progressive and established stages. Progesterone therapy significantly reduced motoneuron vacuolation, enhanced ChAT immunoreactive perikarya and reduced the hyperexpression of GAP43 during the early progressive and established stages. At all stage periods, untreated Wobblers showed high density of glial fibrillary acidic protein (GFAP)+ astrocytes and decreased number of glutamine synthase (GS) immunostained cells. Progesterone treatment down-regulated GFAP+ astrocytes and up-regulated GS+ cell number. These data reinforced the usefulness of progesterone to improve motoneuron and glial cell abnormalities of Wobbler mice and further showed that therapeutic benefit seems more effective at the early progressive and established periods, rather than on advance stages of spinal cord neurodegeneration. © 2009 Springer Science+Business Media, LLC. |
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| Bibliografía: | Azcoitia, I., Leonelli, E., Magnaghi, V., Veiga, S., Garcia-Segura, L.M., Melcangi, R.C., Progesterone and its derivatives dihydroprogesterone and tetrahydroprogesterone reduce myelin fiber morphological abnormalities and myelin fiber loss in the sciatic nerve of aged rats (2003) Neurobiology of Aging, 24 (6), pp. 853-860. , DOI 10.1016/S0197-4580(02)00234-8 Barbeito, L.H., Pehar, M., Cassina, P., Vargas, M.R., Peluffo, H., Viera, L., Estevez, A.G., Beckman, J.S., A role for astrocytes in motor neuron loss in amyotrophic lateral sclerosis (2004) Brain Research Reviews, 47 (1-3), pp. 263-274. , DOI 10.1016/j.brainresrev.2004.05.003, PII S0165017304000700, Chemical and Electrical Synapses Benarroch, E.E., Neuron-astrocyte interactions: Partnership for normal function and disease in the central nervous system (2005) Mayo Clin Proc, 80, pp. 1326-1338. , 10.4065/80.10.1326 16212146 Benowitz, L.I., Routtenberg, A., GAP-43: An intrinsic determinant of neuronal development and plasticity (1997) Trends in Neurosciences, 20 (2), pp. 84-91. , DOI 10.1016/S0166-2236(96)10072-2, PII S0166223696100722 Bigini, P., Bastone, A., Mennini, T., Glutamate transporters in the spinal cord of the wobbler mouse (2001) NeuroReport, 12, pp. 1815-1820. , 10.1097/00001756-200107030-00011 11435904 Bigini, P., Gardoni, F., Barbera, S., Cagnotto, A., Fumagalli, E., Longhi, A., Corsi, M.M., Mennini, T., Expression of AMPA and NMDA receptor subunits in the cervical spinal cord of wobbler mice (2006) BMC Neurosci, 26, pp. 7-71 Bigini, P., Atzori, C., Fumagalli, E., Cagnotto, A., Barbera, S., Migheli, A., Mennini, T., Lack of caspase-dependent apoptosis in spinal motor neurons of the wobbler mouse (2007) Neuroscience Letters, 426 (2), pp. 106-110. , DOI 10.1016/j.neulet.2007.08.057, PII S030439400700910X Blondet, B., Hantaz-Ambroise, D., Aït-Ikhlef, A., Cambier, D., Murawsky, M., Rieger, F., Astrocytosis in wobbler mouse spinal cord involves a population of astrocytes which is glutamine synthetase-negative (1995) Neurosci Lett, 183, pp. 179-182. , 10.1016/0304-3940(94)11145-9 7739788 Boillee, S., Viala, L., Peschanski, M., Dreyfus, P.A., Differential microglial response to progressive neurodegeneration in the murine mutant wobbler (2001) GLIA, 33 (4), pp. 277-287. , DOI 10.1002/1098-1136(20010315)33:4<277::AID-GLIA1026>3.0.CO;2-Y Boillee, S., Peschanski, M., Junier, M.-P., The wobbler mouse: A neurodegeneration Jigsaw puzzle (2003) Molecular Neurobiology, 28 (1), pp. 65-106. , DOI 10.1385/MN:28:1:65 Boonyaratanakornkit, V., Bi, Y., Rudd, M., Edwards, D.P., The role and mechanism of progesterone receptor activation of extra-nuclear signaling pathways in regulating gene transcription and cell cycle progression (2008) Steroids, 73, pp. 922-928. , 10.1016/j.steroids.2008.01.010 18321550 Brinton, R.D., The healthy cell bias of estrogen action: Mitochondrial bioenergetics and neurological implications (2008) Trends Neurosci, 31, pp. 529-537. , 10.1016/j.tins.2008.07.003 18774188 Calabrese, V., Mancuso, C., Calvani, M., Rizzarelli, E., Butterfield, D.A., Giuffrida Stella, A.M., Nitric oxide in the central nervous system: Neuroprotection versus neurotoxicity (2007) Nature Reviews Neuroscience, 8 (10), pp. 766-775. , DOI 10.1038/nrn2214, PII NRN2214 Cammer, W., Glutamine synthetase in the central nervous system is not confined to astrocytes (1990) Journal of Neuroimmunology, 26 (2), pp. 173-178. , DOI 10.1016/0165-5728(90)90088-5 Ciriza, I., Azcoitia, I., Garcia-Segura, L.M., Reduced progesterone metabolites protect rat hippocampal neurones from kainic acid excitotoxicity in vivo (2004) Journal of Neuroendocrinology, 16 (1), pp. 58-63. , DOI 10.1111/j.1365-2826.2004.01121.x Clarke, P.G., Developmental cell death: Morphological diversity and multiple mechanisms (1990) Anat Embryol (Berl), 181, pp. 195-213 Cleveland, D.W., Rothstein, J.D., From Charcot to Lou Gehrig: Deciphering selective motor neuron death in ALS (2001) Nature Reviews Neuroscience, 2 (11), pp. 806-819. , DOI 10.1038/35097565 Clowry, G.J., McHanwell, S., Expression of nitric oxide synthase by motor neurones in the spinal cord of the mutant mouse wobbler (1996) Neurosci Lett, 215, pp. 177-180. , 10.1016/0304-3940(96)12971-2 8899742 Corvino, V., Businaro, R., Geloso, M.C., Bigini, P., Cavallo, V., Pompili, E., Mennini, T., Michetti, F., S100B protein and 4-hydroxynonenal in the spinal cord of wobbler mice (2003) Neurochemical Research, 28 (2), pp. 341-345. , DOI 10.1023/A:1022345720852 Cudkowicz, M.E., Brown Jr., R.H., An update on superoxide dismutase 1 in familial amyotrophic lateral sclerosis (1996) Journal of the Neurological Sciences, 139 (SUPPL.), pp. 10-15. , DOI 10.1016/0022-510X(96)00084-6 Dave, K.R., Bradley, W.G., Perez-Pinzon, M.A., Early mitochondrial dysfunction occurs in motor cortex and spinal cord at the onset of disease in the Wobbler mouse (2003) Experimental Neurology, 182 (2), pp. 412-420. , DOI 10.1016/S0014-4886(03)00091-8 De Nicola, A.F., Gonzalez, S.L., Labombarda, F., Deniselle, M.C.G., Garay, L., Guennoun, R., Schumacher, M., Progesterone treatment of spinal cord injury: Effects on receptors, neurotrophins, and myelination (2006) Journal of Molecular Neuroscience, 28 (1), pp. 3-16. , DOI 10.1385/JMN:28:1:3 Dennis, J.S., Citron, B.A., Wobbler mice modeling motor neuron disease display elevated transactive response DNA binding protein (2009) Neuroscience, 158, pp. 745-750. , 10.1016/j.neuroscience.2008.10.030 19013502 Djebaili, M., Guo, Q., Pettus, E.H., Hoffman, S.W., Stein, D.G., The neurosteroids progesterone and allopregnanolone reduce cell death, gliosis, and functional deficits after traumatic brain injury (2005) J Neurotrauma, 22, pp. 106-118. , 10.1089/neu.2005.22.106 15665606 Elliott, E.J., Parks, D.A., Fishman, P.S., Effect of proximal axotomy on GAP-43 expression in cortical neurons in the mouse (1997) Brain Research, 755 (2), pp. 221-228. , DOI 10.1016/S0006-8993(97)00100-5, PII S0006899397001005 Ferrini, M., Lima, A., De Nicola, A.F., Estradiol abolishes autologous down regulation of glucocorticoid receptors in brain (1995) Life Sci, 57, pp. 2403-2412. , 10.1016/0024-3205(95)02236-3 8847961 Fumagalli, E., Bigini, P., Barbera, S., De Paola, M., Mennini, T., Riluzole, unlike the AMPA antagonist RPR119990, reduces motor impairment and partially prevents motoneuron death in the wobbler mouse, a model of neurodegenerative disease (2006) Experimental Neurology, 198 (1), pp. 114-128. , DOI 10.1016/j.expneurol.2005.11.010, PII S0014488605004206 Gago, N., El-Etr, M., Sananes, N., Cadepond, F., Samuel, D., Avellana-Adalid, V., Baron-Van Evercooren, A., Schumacher, M., 3α,5α-Tetrahydroprogesterone (allopregnanolone) and γ-aminobutyric acid: Autocrine/paracrine interactions in the control of neonatal PSA-NCAM+ progenitor proliferation (2004) Journal of Neuroscience Research, 78 (6), pp. 770-783. , DOI 10.1002/jnr.20348 Garay, L., Deniselle, M.C.G., Lima, A., Roig, P., De Nicola, A.F., Effects of progesterone in the spinal cord of a mouse model of multiple sclerosis (2007) Journal of Steroid Biochemistry and Molecular Biology, 107 (3-5), pp. 228-237. , DOI 10.1016/j.jsbmb.2007.03.040, PII S0960076007001665 Ghoumari, A.M., Ibanez, C., El-Etr, M., Leclerc, P., Eychenne, B., O'Malley, B.W., Baulieu, E.E., Schumacher, M., Progesterone and its metabolites increase myelin basic protein expression in organotypic slice cultures of rat cerebellum (2003) Journal of Neurochemistry, 86 (4), pp. 848-859. , DOI 10.1046/j.1471-4159.2003.01881.x Giulivi, C., Poderoso, J.J., Boveris, A., Production of nitric oxide by mitochondria (1998) Journal of Biological Chemistry, 273 (18), pp. 11038-11043. , DOI 10.1074/jbc.273.18.11038 Gonzalez Deniselle, M.C., Lavista-Llanos, S., Ferrini, M.G., Lima, A.E., Roldán, A.G., De Nicola, A.F., In vitro differences between astrocytes of control and wobbler mice spinal cord (1999) Neurochem Res, 24, pp. 1535-1541. , 10.1023/A:1021199931682 Gonzalez Deniselle, M.C., Grillo, C.A., Gonzalez, S., Roig, P., De Nicola, A.F., Evidence for down-regulation of GAP-43 mRNA in Wobbler mouse spinal motoneurons by corticosterone and a 21-aminosteroid (1999) Brain Research, 841 (1-2), pp. 78-84. , DOI 10.1016/S0006-8993(99)01783-7, PII S0006899399017837 Gonzalez Deniselle, M.C., Lopez-Costa, J.J., Saavedra, J.P., Pietranera, L., Gonzalez, S.L., Garay, L., Guennoun, R., De Nicola, A.F., Progesterone neuroprotection in the Wobbler mouse, a genetic model of spinal cord motor neuron disease (2002) Neurobiology of Disease, 11 (3), pp. 457-468. , DOI 10.1006/nbdi.2002.0564 Gonzalez Deniselle, M.C., Garay, L., Lopez-Costa, J.J., Gonzalez, S., Mougel, A., Guennoun, R., Schumacher, M., De Nicola, A.F., Progesterone treatment reduces NADPH-diaphorase/nitric oxide synthase in Wobbler mouse motoneuron disease (2004) Brain Research, 1014 (1-2), pp. 71-79. , DOI 10.1016/j.brainres.2004.04.004, PII S0006899304005566 Gonzalez Deniselle, M.C., Garay, L., Gonzalez, S., Guennoun, R., Schumacher, M., De Nicola, A.F., Progesterone restores retrograde labeling of cervical motoneurons in Wobbler mouse motoneuron disease (2005) Experimental Neurology, 195 (2), pp. 518-523. , DOI 10.1016/j.expneurol.2005.06.015, PII S0014488605002232 Gonzalez Deniselle, M.C., Garay, L., Gonzalez, S., Saravia, F., Labombarda, F., Guennoun, R., Schumacher, M., De Nicola, A.F., Progesterone modulates brain-derived neurotrophic factor and choline acetyltransferase in degenerating Wobbler motoneurons (2007) Experimental Neurology, 203 (2), pp. 406-414. , DOI 10.1016/j.expneurol.2006.08.019, PII S0014488606005267 Guennoun, R., Meffre, D., Labombarda, F., Gonzalez, S.L., Gonzalez Deniselle, M.C., Stein, D.G., De Nicola, A.F., Schumacher, M., The membrane-associated progesterone-binding protein 25-Dx: Expression, cellular localization and up-regulation after brain and spinal cord injuries (2008) Brain Res Rev, 57, pp. 493-505. , 10.1016/j.brainresrev.2007.05.009 17618691 Hantaz-Ambroise, D., Jacque, C., Aït Ikhlef, A., Parmentier, C., Leclerc, P., Cambier, D., Zadigue, G., Rieger, F., Specific features of chronic astrocyte gliosis after experimental central nervous system (CNS) xenografting and in wobbler neurological mutant CNS (2001) Differentiation, 69, pp. 100-107. , 10.1046/j.1432-0436.2001.690204.x 11798064 Henderson, J.T., Javaheri, M., Kopko, S., Roder, J.C., Reduction of lower motor neuron degeneration in wobbler mice by n-acetyl-l-cysteine (1996) J Neurosci, 16, pp. 7574-7582. , 8922414 Ikeda, K., Iwasaki, Y., Kinoshita, M., Marubuchi, S., Ono, S., T-588, a novel neuroprotective agent, delays progression of neuromuscular dysfunction in wobbler mouse motoneuron disease (2000) Brain Research, 858 (1), pp. 84-91. , DOI 10.1016/S0006-8993(99)02427-0, PII S0006899399024270 Ikemoto, A., Hirano, A., Akiguchi, I., Increased expression of growth-associated protein 43 on the surface of the anterior horn cells in amyotrophic lateral sclerosis (1999) Acta Neuropathologica, 98 (4), pp. 367-373. , DOI 10.1007/s004010051096 Ishiyama, T., Ogo, H., Wong, V., Klinkosz, B., Noguchi, H., Nakayama, C., Mitsumoto, H., Methionine-free brain-derived neurotrophic factor in wobbler mouse motor neuron disease: Dose-related effects and comparison with the methionyl form (2002) Brain Research, 944 (1-2), pp. 195-199. , DOI 10.1016/S0006-8993(02)02881-0, PII S0006899302028810 Ishiyama, T., Okada, R., Nishibe, H., Mitsumoto, H., Nakayama, C., Riluzole slows the progression of neuromuscular dysfunction in the wobbler mouse motor neuron disease (2004) Brain Research, 1019 (1-2), pp. 226-236. , DOI 10.1016/j.brainres.2004.06.002, PII S0006899304009382 Ishrat, T., Sayeed, I., Atif, F., Stein, D.G., Effects of progesterone administration on infarct volume and functional deficits following permanent focal cerebral ischemia in rats (2009) Brain Res, 1257, pp. 94-101. , 10.1016/j.brainres.2008.12.048 19135987 Julien, J.-P., ALS: Astrocytes move in as deadly neighbors (2007) Nature Neuroscience, 10 (5), pp. 535-537. , DOI 10.1038/nn0507-535, PII NN0507535 Kapfhammer, J.P., Schwab, M.E., Inverse patterns of myelination and GAP-43 expression in the adult CNS: Neurite growth inhibitors as regulators of neuronal plasticity? (1994) J Comp Neurol, 340, pp. 194-206. , 10.1002/cne.903400206 8201019 Kong, J., Xu, Z., Massive mitochondrial degeneration in motor neurons triggers the onset of amyotrophic lateral sclerosis in mice expressing a mutant SOD1 (1998) J Neurosci, 18, pp. 3241-3250. , 9547233 Laage, S., Zobel, G., Jockusch, H., Astrocyte overgrowth in the brain stem and spinal cord of mice affected by spinal atrophy, wobbler (1988) Dev Neurosci, 10, pp. 190-198. , 10.1159/000111969 3142758 Labombarda, F., Guennoun, R., Gonzalez, S., Roig, P., Lima, A., Schumacher, M., De Nicola, A.F., Immunocytochemical evidence for a progesterone receptor in neurons and glial cells of the rat spinal cord (2000) Neuroscience Letters, 288 (1), pp. 29-32. , DOI 10.1016/S0304-3940(00)01191-5, PII S0304394000011915 Labombarda, F., Gonzalez, S.L., Deniselle, M.C.G., Vinson, G.P., Schumacher, M., De Nicola, A.F., Guennoun, R., Effects of injury and progesterone treatment on progesterone receptor and progesterone binding protein 25-Dx expression in the rat spinal cord (2003) Journal of Neurochemistry, 87 (4), pp. 902-913. , DOI 10.1046/j.1471-4159.2003.02055.x Leist, M., Jaattela, M., Four deaths and a funeral: From caspases to alternative mechanisms (2001) Nature Reviews Molecular Cell Biology, 2 (8), pp. 589-598. , DOI 10.1038/35085008 Martin, L.J., Liu, Z., Chen, K., Price, A.C., Yan, P., Swaby, J.A., Golden, W.C., Motor neuron degeneration in amyotrophic lateral sclerosis mutant superoxide dismutase-1 transgenic mice: Mechanisms of mitochondriopathy and cell death (2007) Journal of Comparative Neurology, 500 (1), pp. 20-46. , DOI 10.1002/cne.21160 Migheli, A., Atzori, C., Piva, R., Tortarolo, M., Girelli, M., Schiffer, D., Bendotti, C., Lack of apoptosis in mice with ALS [3] (1999) Nature Medicine, 5 (9), pp. 966-967. , DOI 10.1038/12381 Migliaccio, A., Piccolo, D., Castoria, G., Domenico, M.D., Bilancio, A., Lombardi, M., Gong, W., Auricchio, F., Activation of the Src/p21(ras)/Erk pathway by progesterone receptor via cross-talk with estrogen receptor (1998) EMBO Journal, 17 (7), pp. 2008-2018. , DOI 10.1093/emboj/17.7.2008 Mitsumoto, H., Boggs, A.L., Vacuolated anterior horn cells in wobbler mouse motor neuron disease: Peripheral axons and regenerative capacity (1987) J Neuropathol Exp Neurol, 46, pp. 214-222. , 10.1097/00005072-198703000-00008 3819775 Mitsumoto, H., Ikeda, K., Klinkosz, B., Cedarbaum, J.M., Wong, V., Lindsay, R.M., Arrest of motor neuron disease in wobbler mice cotreated with CNTF and BDNF (1994) Science, 265, pp. 1052-1053. , 10.1126/science.8066451 Moncada, S., Bolanos, J.P., Nitric oxide, cell bioenergetics and neurodegeneration (2006) Journal of Neurochemistry, 97 (6), pp. 1676-1689. , DOI 10.1111/j.1471-4159.2006.03988.x Oda, Y., Imai, S., Nakanishi, I., Ichikawa, T., Deguchi, T., Immunohistochemical study on choline acetyltransferase in the spinal cord of patients with amyotrophic lateral sclerosis (1995) Pathol Int, 45, pp. 933-939. , 10.1111/j.1440-1827.1995.tb03418.x 8808298 Pajovićs, S.B., Saicić, Z.S., Modulation of antioxidant enzyme activities by sexual steroid hormones (2008) Physiol Res, 57, pp. 801-811 Parhad, I.M., Oishi, R., Clark, A.W., GAP-43 gene expression is increased in anterior horn cells of amyotrophic lateral sclerosis (1992) Ann Neurol, 31, pp. 593-597. , 10.1002/ana.410310605 1387517 Popper, P., Farber, D.B., Micevych, P.E., Minoofar, K., Bronstein, J.M., TRPM-2 expression and TUNEL staining in neurodegenerative diseases: Studies in wobbler and rd mice (1997) Experimental Neurology, 143 (2), pp. 246-254. , DOI 10.1006/exnr.1996.6364 Rathke-Hartlieb, S., Schmidt, V.C., Jockusch, H., Schmitt-John, T., Bartsch, J.W., Spatiotemporal progression of neurodegeneration and glia activation in the wobbler neuropathy of the mouse (1999) NeuroReport, 10, pp. 3411-3416. , 10.1097/00001756-199911080-00028 10599854 Roof, R.L., Hall, E.D., Gender differences in acute CNS trauma and stroke: Neuroprotective effects of estrogen and progesterone (2000) J Neurotrauma, 17, pp. 367-388. , 10.1089/neu.2000.17.367 10833057 Roof, R.L., Hoffman, S.W., Stein, D.G., Progesterone protects against lipid peroxidation following traumatic brain injury in rats (1997) Mol Chem Neuropathol, 31, pp. 1-11. , 10.1007/BF02815156 9271001 Rothstein, J.D., Van Kammen, M., Levey, A.I., Martin, L.J., Kuncl, R.W., Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis (1995) Ann Neurol, 38, pp. 73-84. , 10.1002/ana.410380114 7611729 Santoro, B., Bigini, P., Levandis, G., Nobile, V., Biggiogera, M., Botti, F., Mennini, T., Curti, D., Evidence for chronic mitochondrial impairment in the cervical spinal cord of a murine model of motor neuron disease (2004) Neurobiology of Disease, 17 (2), pp. 349-357. , DOI 10.1016/j.nbd.2004.07.003, PII S0969996104001548 Saravia, F., Beauquis, J., Pietranera, L., De Nicola, A.F., Neuroprotective effects of estradiol in hippocampal neurons and glia of middle age mice (2007) Psychoneuroendocrinology, 32 (5), pp. 480-492. , DOI 10.1016/j.psyneuen.2007.02.012, PII S030645300700056X Schmitt-John, T., Drepper, C., Mussmann, A., Hahn, P., Kuhlmann, M., Thiel, C., Hafner, M., Jockusch, H., Mutation of Vps54 causes motor neuron disease and defective spermiogenesis in the wobbler mouse (2005) Nature Genetics, 37 (11), pp. 1213-1215. , DOI 10.1038/ng1661, PII N1661 Schumacher, M., Guennoun, R., Stein, D.G., De Nicola, A.F., Progesterone: Therapeutic opportunities for neuroprotection and myelin repair (2007) Pharmacology and Therapeutics, 116 (1), pp. 77-106. , DOI 10.1016/j.pharmthera.2007.06.001, PII S0163725807001106, Neurosteroids Special Issue Sperandio, S., De Belle, I., Bredesen, D.E., An alternative, nonapoptotic form of programmed cell death (2000) Proceedings of the National Academy of Sciences of the United States of America, 97 (26), pp. 14376-14381. , DOI 10.1073/pnas.97.26.14376 Stein, D.G., Progesterone exerts neuroprotective effects after brain injury (2008) Brain Res Rev, 57, pp. 386-397. , 10.1016/j.brainresrev.2007.06.012 17826842 Tansey, F.A., Farooq, M., Cammer, W., Glutamine synthetase in oligodendrocytes and astrocytes: New biochemical and immunocytochemical evidence (1991) J Neurochem, 56, pp. 266-272. , 10.1111/j.1471-4159.1991.tb02591.x 1670954 Thomas, A.J., Nockels, R.P., Pan, H.Q., Shaffrey, C.I., Chopp, M., Progesterone is neuroprotective after acute experimental spinal cord trauma in rats (1999) Spine, 24 (20), pp. 2134-2138. , DOI 10.1097/00007632-199910150-00013 Tsuzaka, K., Ishiyama, T., Pioro, E.P., Mitsumoto, H., Role of brain-derived neurotrophic factor in wobbler mouse motor neuron disease (2001) Muscle and Nerve, 24 (4), pp. 474-480. , DOI 10.1002/mus.1029 Vardimon, L., Ben-Dror, I., Avisar, N., Oren, A., Shiftan, L., Glucocorticoid control of glial gene expression (1999) Journal of Neurobiology, 40 (4), pp. 513-527. , DOI 10.1002/(SICI)1097-4695(19990915)40:4<513::AID-NEU8>3.0.CO;2-D Xu, G.-P., Dave, K.R., Moraes, C.T., Busto, R., Sick, T.J., Bradley, W.G., Perez-Pinzon, M.A., Dysfunctional mitochondrial respiration in the wobbler mouse brain (2001) Neuroscience Letters, 300 (3), pp. 141-144. , DOI 10.1016/S0304-3940(01)01575-0, PII S0304394001015750 Yung, K.K., Tang, F., Fielding, R., Du, Y.H., Vacca-Galloway, L.L., 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 (1992) Neuroscience, 50, pp. 209-222. , 10.1016/0306-4522(92)90393-G 1383870 Zhu, Y., Hanna, R.N., Schaaf, M.J., Spaink, H.P., Thomas, P., Candidates for membrane progestin receptors-past approaches and future challenges (2008) Comp Biochem Physiol C Toxicol Pharmacol, 148, pp. 381-389. , 10.1016/j.cbpc.2008.05.019 18602498 Zoccolella, S., Beghi, E., Palagano, G., Fraddosio, A., Guerra, V., Samarelli, V., Lepore, V., Logroscino, G., Riluzole and amyotrophic lateral sclerosis survival: A population-based study in southern Italy (2007) European Journal of Neurology, 14 (3), pp. 262-268. , DOI 10.1111/j.1468-1331.2006.01575.x Zoing, M.C., Burke, D., Pamphlett, R., Kiernan, M.C., Riluzole therapy for motor neurone disease: An early Australian experience (1996-2002) (2006) Journal of Clinical Neuroscience, 13 (1), pp. 78-83. , DOI 10.1016/j.jocn.2004.04.011, PII S0967586805003693 |
| ISSN: | 02724340 |
| DOI: | 10.1007/s10571-009-9437-8 |