Skip to main content
SpringerLink
Log in

Stage Dependent Effects of Progesterone on Motoneurons and Glial Cells of Wobbler Mouse Spinal Cord Degeneration

  • Original Paper
  • Published:
Cellular and Molecular Neurobiology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Azcoitia I, Leonelli E, Magnaghi V, Veiga S, Garcia Segura LM, Melcangi R (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

    Article  PubMed  CAS  Google Scholar 

  • Barbeito LH, Pehar M, Cassina P, Vargas MR, Peluffo H, Viera L, Estévez AG, Beckman JS (2004) A role for astrocytes in motor neuron loss in amyotrophic lateral sclerosis. Brain Res Rev 47:263–274

    Article  PubMed  CAS  Google Scholar 

  • Benarroch EE (2005) Neuron-astrocyte interactions: partnership for normal function and disease in the central nervous system. Mayo Clin Proc 80:1326–1338

    Article  PubMed  CAS  Google Scholar 

  • Benowitz LI, Routtenberg A (1997) GAP-43: an intrinsic determinant of neuronal development and plasticity. Trends Neurosci 20:84–91

    Article  PubMed  CAS  Google Scholar 

  • Bigini P, Bastone A, Mennini T (2001) Glutamate transporters in the spinal cord of the wobbler mouse. NeuroReport 12:1815–1820

    Article  PubMed  CAS  Google Scholar 

  • Bigini P, Gardoni F, Barbera S, Cagnotto A, Fumagalli E, Longhi A, Corsi MM, Di Luca M, Mennini T (2006) Expression of AMPA and NMDA receptor subunits in the cervical spinal cord of wobbler mice. BMC Neurosci 26:7–71

    Google Scholar 

  • Bigini P, Atzori C, Fumagalli E, Cagnotto A, Barbera S, Migheli A, Mennini T (2007) Lack of caspase-dependent apoptosis in spinal motor neurons of the wobbler mouse. Neurosci Lett 426:106–110

    Article  PubMed  CAS  Google Scholar 

  • Blondet B, Hantaz-Ambroise D, Aït-Ikhlef A, Cambier D, Murawsky M, Rieger F (1995) Astrocytosis in wobbler mouse spinal cord involves a population of astrocytes which is glutamine synthetase-negative. Neurosci Lett 183:179–182

    Article  PubMed  CAS  Google Scholar 

  • Boillée S, Viala L, Peschanski M, Dreyfus PA (2001) Differential microglial response to progressive neurodegeneration in the murine mutant wobbler. Glia 33:277–287

    Article  PubMed  Google Scholar 

  • Boillée S, Peschanski M, Junier MP (2003) The wobbler mouse: a neurodegeneration jigsaw puzzle. Mol Neurobiol 28:65–106

    Article  PubMed  Google Scholar 

  • Boonyaratanakornkit V, Bi Y, Rudd M, Edwards DP (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

    Article  PubMed  CAS  Google Scholar 

  • Brinton RD (2008) The healthy cell bias of estrogen action: mitochondrial bioenergetics and neurological implications. Trends Neurosci 31:529–537

    Article  PubMed  CAS  Google Scholar 

  • Calabrese V, Mancuso C, Calvani M, Rizzarelli E, Butterfield DA, Stella AM (2007) Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat Rev Neurosci 8:766–775

    Article  PubMed  CAS  Google Scholar 

  • Cammer W (1990) Glutamine synthetase in the central nervous system is not confined to astrocytes. J Neuroimmunol 26:173–178

    Article  PubMed  CAS  Google Scholar 

  • Ciriza I, Azcoitia I, Garcia-Segura LM (2004) Reduced progesterone metabolites protect rat hippocampal neurones from kainic acid excitotoxicity in vivo. J Neuroendocrinol 16:58–63

    Article  PubMed  CAS  Google Scholar 

  • Clarke PG (1990) Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol (Berl) 181:195–213

    CAS  Google Scholar 

  • Cleveland DW, Rothstein JD (2001) From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat Rev Neurosci 2:806–819

    Article  PubMed  CAS  Google Scholar 

  • Clowry GJ, McHanwell S (1996) Expression of nitric oxide synthase by motor neurones in the spinal cord of the mutant mouse wobbler. Neurosci Lett 215:177–180

    Article  PubMed  CAS  Google Scholar 

  • Corvino V, Businaro R, Geloso MC, Bigini P, Cavallo V, Pompili E, Mennini T, Fumagalli L, Michetti F (2003) S100B protein and 4-hydroxynonenal in the spinal cord of wobbler mice. Neurochem Res 28:341–345

    Article  PubMed  CAS  Google Scholar 

  • Cudkowicz ME, Brown RH Jr (1996) An update on superoxide dismutase 1 in familial amyotrophic lateral sclerosis. J Neurol Sci 139(Suppl):10–15

    Article  PubMed  Google Scholar 

  • Dave KR, Bradley WG, Pérez-Pinzón MA (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

    Article  PubMed  CAS  Google Scholar 

  • De Nicola AF, Gonzalez SL, Labombarda F, Gonzalez Deniselle MC, Garay L, Guennoun R, Schumacher M (2006) Progesterone treatment of spinal cord injury: effects on receptors, neurotrophins, and myelination. J Mol Neurosci 28:3–15

    Article  PubMed  Google Scholar 

  • Dennis JS, Citron BA (2009) Wobbler mice modeling motor neuron disease display elevated transactive response DNA binding protein. Neuroscience 158:745–750

    Article  PubMed  CAS  Google Scholar 

  • Djebaili M, Guo Q, Pettus EH, Hoffman SW, Stein DG (2005) The neurosteroids progesterone and allopregnanolone reduce cell death, gliosis, and functional deficits after traumatic brain injury. J Neurotrauma 22:106–118

    Article  PubMed  Google Scholar 

  • Elliott EJ, Parks DA, Fishman PS (1997) Effect of proximal axotomy on GAP-43 expression in cortical neurons in the mouse. Brain Res 755:221–228

    Article  PubMed  CAS  Google Scholar 

  • Ferrini M, Lima A, De Nicola AF (1995) Estradiol abolishes autologous down regulation of glucocorticoid receptors in brain. Life Sci 57:2403–2412

    Article  PubMed  CAS  Google Scholar 

  • Fumagalli E, Bigini P, Barbera S, De Paola M, Mennini T (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

    Article  PubMed  CAS  Google Scholar 

  • Gago N, El-Etr M, Sananès N, Cadepond F, Samuel D, Avellana-Adalid V, Baron-VanEvercooren A, Schumacher M (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

    Article  PubMed  CAS  Google Scholar 

  • Garay L, Gonzalez Deniselle MC, Lima A, Roig P, De Nicola AF (2007) Effects of progesterone in the spinal cord of a mouse model of multiple sclerosis. J Steroid Biochem Mol Biol 107:228–237

    Article  PubMed  CAS  Google Scholar 

  • Ghoumari AM, Ibanez C, El-Etr M, Leclerc F, Eychenne B, Baulieu EE, Schumacher M (2003) Progesterone and its metabolites increase myelination in organotypic slice cultures of rat cerebellum. J Neurochem 86:848–859

    Article  PubMed  CAS  Google Scholar 

  • Giulivi C, Poderoso JJ, Boveris A (1998) Production of nitric oxide by mitochondria. J Biol Chem 273:11038–11043

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez Deniselle MC, Lavista-Llanos S, Ferrini MG, Lima AE, Roldán AG, De Nicola AF (1999a) In vitro differences between astrocytes of control and wobbler mice spinal cord. Neurochem Res 24:1535–1541

    Article  CAS  Google Scholar 

  • Gonzalez Deniselle MC, Grillo CA, Gonzalez S, Roig P, De Nicola AF (1999b) Evidence for down-regulation of GAP-43 mRNA in wobbler mouse spinal motoneurons by corticosterone and a 21-aminosteroid. Brain Res 841:78–84

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez Deniselle MC, López-Costa JJ, Saavedra JP, Pietranera L, Gonzalez SL, Garay L, Guennoun R, Schumacher M, De Nicola AF (2002) Progesterone neuroprotection in the wobbler mouse, a genetic model of spinal cord motor neuron disease. Neurobiol Dis 11:457–468

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez Deniselle MC, Garay L, López-Costa JJ, González S, Mougel A, Guennoun R, Schumacher M, De Nicola AF (2004) Progesterone treatment reduces NADPH-diaphorase/nitric oxide synthase in wobbler mouse motoneuron disease. Brain Res 1014:71–79

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez Deniselle MC, Garay L, Gonzalez S, Guennoun R, Schumacher M, De Nicola AF (2005) Progesterone restores retrograde labeling of cervical motoneurons in Wobbler mouse motoneuron disease. Exp Neurol 195:518–523

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez Deniselle MC, Garay L, Gonzalez S, Saravia F, Labombarda F, Guennoun R, Schumacher M, De Nicola AF (2007) Progesterone modulates brain-derived neurotrophic factor and choline acetyltransferase in degenerating wobbler motoneurons. Exp Neurol 203:406–414

    Article  PubMed  CAS  Google Scholar 

  • Guennoun R, Meffre D, Labombarda F, Gonzalez SL, Gonzalez Deniselle MC, Stein DG, De Nicola AF, Schumacher M (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

    Article  PubMed  CAS  Google Scholar 

  • Hantaz-Ambroise D, Jacque C, Aït Ikhlef A, Parmentier C, Leclerc P, Cambier D, Zadigue G, Rieger F (2001) Specific features of chronic astrocyte gliosis after experimental central nervous system (CNS) xenografting and in wobbler neurological mutant CNS. Differentiation 69:100–107

    Article  PubMed  CAS  Google Scholar 

  • Henderson JT, Javaheri M, Kopko S, Roder JC (1996) Reduction of lower motor neuron degeneration in wobbler mice by n-acetyl-l-cysteine. J Neurosci 16:7574–7582

    PubMed  CAS  Google Scholar 

  • Ikeda K, Iwasaki Y, Kinoshita M, Marubuchi S, Ono S (2000) T-588, a novel neuroprotective agent, delays progression of neuromuscular dysfunction in wobbler mouse motoneuron disease. Brain Res 858:84–91

    Article  PubMed  CAS  Google Scholar 

  • Ikemoto A, Hirano A, Akiguchi I (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

    Article  PubMed  CAS  Google Scholar 

  • Ishiyama T, Ogo H, Wong V, Klinkosz B, Noguchi H, Nakayama C, Mitsumoto H (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

    Article  PubMed  CAS  Google Scholar 

  • Ishiyama T, Okada R, Nishibe H, Mitsumoto H, Nakayama C (2004) Riluzole slows the progression of neuromuscular dysfunction in the wobbler mouse motor neuron disease. Brain Res 1019:226–236

    Article  PubMed  CAS  Google Scholar 

  • Ishrat T, Sayeed I, Atif F, Stein DG (2009) Effects of progesterone administration on infarct volume and functional deficits following permanent focal cerebral ischemia in rats. Brain Res 1257:94–101

    Article  PubMed  CAS  Google Scholar 

  • Julien JP (2007) ALS: astrocytes move in as deadly neighbors. Nat Neurosci 10:535–537

    Article  PubMed  CAS  Google Scholar 

  • Kapfhammer JP, Schwab ME (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

    Article  PubMed  CAS  Google Scholar 

  • Kong J, Xu Z (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

    PubMed  CAS  Google Scholar 

  • Laage S, Zobel G, Jockusch H (1988) Astrocyte overgrowth in the brain stem and spinal cord of mice affected by spinal atrophy, wobbler. Dev Neurosci 10:190–198

    Article  PubMed  CAS  Google Scholar 

  • Labombarda F, Guennoun R, Gonzalez S, Roig P, Lima A, Schumacher M, De Nicola AF (2000) Immunocytochemical evidence for a progesterone receptor in neurons and glial cells of the rat spinal cord. Neurosci Lett 288:29–32

    Article  PubMed  CAS  Google Scholar 

  • Labombarda F, Gonzalez SL, Gonzalez Deniselle MC, Vinson GP, Schumacher M, De Nicola AF, Guennoun R (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

    Article  PubMed  CAS  Google Scholar 

  • Leist M, Jäättelä M (2001) Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol 2:589–598

    Article  PubMed  CAS  Google Scholar 

  • Martin LJ, Liu Z, Chen K, Price AC, Pan Y, Swaby JA, Golden WC (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

    Article  PubMed  CAS  Google Scholar 

  • Migheli A, Atzori C, Piva R, Tortarolo M, Girelli M, Schiffer D, Bendotti C (1999) Lack of apoptosis in mice with ALS. Nat Med 5:966–967

    Article  PubMed  CAS  Google Scholar 

  • Migliaccio A, Piccolo D, Castoria G, Di Domenico M, Bilancio A, Lombardi M, Gong W, Beato M, Auricchio F (1998) Activation of the Src/p21ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor. EMBO J 17:2008–2018

    Article  PubMed  CAS  Google Scholar 

  • Mitsumoto H, Boggs AL (1987) Vacuolated anterior horn cells in wobbler mouse motor neuron disease: peripheral axons and regenerative capacity. J Neuropathol Exp Neurol 46:214–222

    Article  PubMed  CAS  Google Scholar 

  • Mitsumoto H, Ikeda K, Klinkosz B, Cedarbaum JM, Wong V, Lindsay RM (1994) Arrest of motor neuron disease in wobbler mice cotreated with CNTF and BDNF. Science 265:1052–1053

    Article  Google Scholar 

  • Moncada S, Bolaños JP (2006) Nitric oxide, cell bioenergetics and neurodegeneration. J Neurochem 97:1676–1689

    Article  PubMed  CAS  Google Scholar 

  • Oda Y, Imai S, Nakanishi I, Ichikawa T, Deguchi T (1995) Immunohistochemical study on choline acetyltransferase in the spinal cord of patients with amyotrophic lateral sclerosis. Pathol Int 45:933–939

    Article  PubMed  CAS  Google Scholar 

  • Pajovićs SB, Saicić ZS (2008) Modulation of antioxidant enzyme activities by sexual steroid hormones. Physiol Res 57:801–811

    Google Scholar 

  • Parhad IM, Oishi R, Clark AW (1992) GAP-43 gene expression is increased in anterior horn cells of amyotrophic lateral sclerosis. Ann Neurol 31:593–597

    Article  PubMed  CAS  Google Scholar 

  • Popper P, Farber DB, Micevych PE, Minoofar K, Bronstein JM (1997) TRPM-2 expression and tunel staining in neurodegenerative diseases: studies in wobbler and rd mice. Exp Neurol 143:246–254

    Article  PubMed  CAS  Google Scholar 

  • Rathke-Hartlieb S, Schmidt VC, Jockusch H, Schmitt-John T, Bartsch JW (1999) Spatiotemporal progression of neurodegeneration and glia activation in the wobbler neuropathy of the mouse. NeuroReport 10:3411–3416

    Article  PubMed  CAS  Google Scholar 

  • Roof RL, Hall ED (2000) Gender differences in acute CNS trauma and stroke: neuroprotective effects of estrogen and progesterone. J Neurotrauma 17:367–388

    Article  PubMed  CAS  Google Scholar 

  • Roof RL, Hoffman SW, Stein DG (1997) Progesterone protects against lipid peroxidation following traumatic brain injury in rats. Mol Chem Neuropathol 31:1–11

    Article  PubMed  CAS  Google Scholar 

  • Rothstein JD, Van Kammen M, Levey AI, Martin LJ, Kuncl RW (1995) Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis. Ann Neurol 38:73–84

    Article  PubMed  CAS  Google Scholar 

  • Santoros B, Bigini P, Levandis G, Nobile V, Biggiogera M, Botti F, Mennini T, Curti D (2004) Evidence for chronic mitochondrial impairment in the cervical spinal cord of a murine model of motor neuron disease. Neurobiol Dis 17:349–357

    Article  CAS  Google Scholar 

  • Saravia F, Beauquis J, Pietranera L, De Nicola AF (2007) Neuroprotective effects of estradiol in hippocampal neurons and glia of middle age mice. Psychoneuroendocrinology 32:480–492

    Article  PubMed  CAS  Google Scholar 

  • Schmitt-John T, Drepper C, Mussmann A, Hahn P, Kuhlmann M, Thiel C, Hafner M, Lengeling A, Heimann P, Jones JM, Meisler MH, Jockusch H (2005) Mutation of Vps54 causes motor neuron disease and defective spermiogenesis in the wobbler mouse. Nat Genet 37:1213–1215

    Article  PubMed  CAS  Google Scholar 

  • Schumacher M, Guennoun R, Stein DG, De Nicola AF (2007) Progesterone: therapeutic opportunities for neuroprotection and myelin repair. Pharmacol Ther 116:77–106

    Article  PubMed  CAS  Google Scholar 

  • Sperandio S, de Belle I, Bredesen DE (2000) An alternative, nonapoptotic form of programmed cell death. Proc Natl Acad Sci U S A 97:14376–14381

    Article  PubMed  CAS  Google Scholar 

  • Stein DG (2008) Progesterone exerts neuroprotective effects after brain injury. Brain Res Rev 57:386–397

    Article  PubMed  CAS  Google Scholar 

  • Tansey FA, Farooq M, Cammer W (1991) Glutamine synthetase in oligodendrocytes and astrocytes: new biochemical and immunocytochemical evidence. J Neurochem 56:266–272

    Article  PubMed  CAS  Google Scholar 

  • Thomas AJ, Nockels RP, Pan HQ, Shaffrey CI, Chopp M (1999) Progesterone is neuroprotective after acute experimental spinal cord trauma in rats. Spine 24:2134–2138

    Article  PubMed  CAS  Google Scholar 

  • Tsuzaka K, Ishiyama T, Pioro EP, Mitsumoto H (2001) Role of brain-derived neurotrophic factor in wobbler mouse motor neuron disease. Muscle Nerve 24:474–480

    Article  PubMed  CAS  Google Scholar 

  • Vardimon L, Ben-Dror I, Avisar N, Oren A, Shiftan L (1999) Glucocorticoid control of glial gene expression. J Neurobiol 40:513–527

    Article  PubMed  CAS  Google Scholar 

  • Xu GP, Dave KR, Moraes CT, Busto R, Sick TJ, Bradley WG, Pérez-Pinzón MA (2001) Dysfunctional mitochondrial respiration in the wobbler mouse brain. Neurosci Lett 300:141–144

    Article  PubMed  CAS  Google Scholar 

  • Yung KK, Tang F, Fielding R, Du YH, Vacca-Galloway LL (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

    Article  PubMed  CAS  Google Scholar 

  • Zhu Y, Hanna RN, Schaaf MJ, Spaink HP, Thomas P (2008) Candidates for membrane progestin receptors-past approaches and future challenges. Comp Biochem Physiol C Toxicol Pharmacol 148:381–389

    Article  PubMed  CAS  Google Scholar 

  • Zoccolella S, Beghis E, Palaganos G, Fraddosio A, Guerra V, Samarelli V, Lepore V, Simone IL, Lamberti P, Serlenga L, Logroscino G, SLAP registry (2007) Riluzole and amyotrophic lateral sclerosis survival: a population-based study in southern Italy. Eur J Neurol 14:262–268

    PubMed  CAS  Google Scholar 

  • Zoing MC, Burke D, Pamphlett R, Kiernan MC (2006) Riluzole therapy for motor neurone disease: an early Australian experience (1996–2002). J Clin Neurosci 13:78–83

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by FONCYT (BID 1728 OC AR PICT 2004 5-25610 and PICT 2007-01044), CONICET (PIP 112-200801-00542), the University of Buenos Aires (M016 and M611) and a cooperative program INSERM/CONICET.

Author information

Authors and Affiliations

  1. Instituto de Biologia y Medicina Experimental-CONICET, Laboratorio de Bioquimica Neuroendócrina, Obligado 2490, 1428, Buenos Aires, Argentina

    Maria Meyer, Maria Claudia Gonzalez Deniselle, Laura I. Garay, Gisella Gargiulo Monachelli, Analia Lima, Paulina Roig & Alejandro F. De Nicola

  2. Department of Human Biochemistry, Faculty of Medicine, University of Buenos Aires, Buenos Aires, Argentina

    Maria Claudia Gonzalez Deniselle, Laura I. Garay & Alejandro F. De Nicola

  3. UMR788 Inserm and University Paris-Sud 11, Kremlin-Bicêtre, France

    Rachida Guennoun & Michael Schumacher

Authors
  1. Maria Meyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria Claudia Gonzalez Deniselle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Laura I. Garay
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gisella Gargiulo Monachelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Analia Lima
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Paulina Roig
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Rachida Guennoun
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Michael Schumacher
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Alejandro F. De Nicola
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alejandro F. De Nicola.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Meyer, M., Gonzalez Deniselle, M.C., Garay, L.I. et al. Stage Dependent Effects of Progesterone on Motoneurons and Glial Cells of Wobbler Mouse Spinal Cord Degeneration. Cell Mol Neurobiol 30, 123–135 (2010). https://doi.org/10.1007/s10571-009-9437-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10571-009-9437-8

Keywords

Search

Navigation