Skip to main content
SpringerLink
Log in

Oxidative stress and 17-α- and 17-β-estradiol modulate neurofilaments differently

  • Original Article
  • Published:
Journal of Molecular Neuroscience Aims and scope Submit manuscript

Abstract

Oxidative stress plays an important role in the pathogenesis of neurodegenerative diseases such as Parkinson's disease (PD). Neuronal death in the substantia nigra of PD patients is partly caused by exacerbated oxidative damage. Our previous studies demonstrated that oxidative stress can alter the structure and stability of neuro-filament (NF) proteins and that 17-α- and 17-β-estradiol are potent neuroprotective agents. The aim of this study was to investigate the cytoskeletal target of neuroprotection by estrogens in neuronal PC12 cells. We induced oxidative stress by MPP+ administration for 24 h, and 17-α- and 17-β-estradiol were used as neuroprotective drugs. We measured gene expression and protein expression of each NF subunit, NFL, NFM, and NFH, by semiquantitative RT-PCR, Western blot, and immunofluorescence. Our results demonstrate that NFL mRNA and protein levels are not modulated by MPP+ or estradiol isomers, whereas NFM gene expression, as well as protein expression, are strongly influenced by MPP+, 17-α-, and 17-β-estradiol after a 24-h treatment. Finally, mRNA levels of the most phosphorylated subunits, NFH, are not changed by MPP+ or treatment with both estradiol isomers, whereas NFH protein expression is decreased by the same treatments. These results suggest that oxidative stress affects neuronal cytoskeleton, maybe though proteolysis and/or abnormal structural changes in NFs. Then, 17-α- and 17-β-estradiol might help the neuronal cell in recovering after oxidative stress by inducing protein expression of NFM and NFH subunits.

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

Similar content being viewed by others

References

  • Al-Chalabi A. and Miller C. C. (2003) Neurofilaments and neurological disease. Bioessays 25(4), 346–355.

    Article  PubMed  CAS  Google Scholar 

  • Amantea D., Russo R., Bagetta G., and Corasaniti M. T. (2005) From clinicalevidence to molecular mechanisms underlying neuroprotection afforded by estrogens. Pharmacol. Res. 52(2), 119–132.

    Article  PubMed  CAS  Google Scholar 

  • Anneser J. (2002) Molecular basis of treatment in motor neurone disease. Neurol. Sci. 21(Suppl. 5), S913-S918.

    Google Scholar 

  • Bains J. S. and Shaw C. A. (1997) Neurodegenerative disorders in humans: the role of glutathione in oxidative stress-mediated neuronal death. Brain Res. Brain Res. Rev. 25(3), 335–358.

    Article  PubMed  CAS  Google Scholar 

  • Barp J., Araujo A. S., Fernandes T. R., Rigatto K. V., Llesuy S., Bello-Klein A. and Singal P. (2002) Myocardial antioxidant and oxidative stress changes due to sex hormones. Braz. J. Med. Biol. Res 35(9), 1075–1081.

    Article  PubMed  CAS  Google Scholar 

  • Berlett B. S. and Stadtman E. R. (1997) Protein oxidation in aging, disease, and oxidative stress. J. Biol. Chem. 272(33) 20,313–20,316.

    Article  CAS  Google Scholar 

  • Bjorkdahl C., Sjogren M. J., Winblad B. and Pei J. J. (2005) Zinc induces neurofilament phosphorylation independent of p70S6 kinase in N2a cells. Neuroreport 16(6), 591–595.

    Article  PubMed  Google Scholar 

  • Bomont P., Cavalier L., Blondeau F., Ben Hamida C., Belal S., Tazir M., et al. (2000), The gene encoding gigaxonin, a new member of the cytoskeletal BTB/kelch repeat family, is mutated in giant axonal neuropathy. Nat. Genet 26(3), 370–374.

    Article  PubMed  CAS  Google Scholar 

  • Booth, E. A., Marchesi M., Kilbourne E. J. and Lucchesi B. R. (2003) 17β-estradiol as a receptor-mediated cardioprotective agent. J. Pharmacol. Exp. Ther. 307(1), 395–401.

    Article  PubMed  CAS  Google Scholar 

  • Callier S., Morissette M., Grandbois M. and Di Paolo T. (2000) Stereospecific prevention by 17β-estradiol of MPTP-induced dopamine depletion in mice. Synapse 37(4), 245–251.

    Article  PubMed  CAS  Google Scholar 

  • Carter J., Gragerov A., Konvicka K., Elder G., Weinstein H., and Lazzarini R. A. (1998) Neurofilament (NF) assembly: divergent characteristics of human and rodent NF-L subunits. J. Biol. Chem. 273(9), 5101–5108.

    Article  PubMed  CAS  Google Scholar 

  • Dave K. R., Bradley W. G. and Perez-Pinzon M. A. (2003) Early mitochondrial dysfunction occurs in motor cortex and spinal cord at the onset of disease in the Wobbler mouse. Exp. Neurol. 182(2), 412–420.

    Article  PubMed  CAS  Google Scholar 

  • De Girolamo L. A., Hargreaves A. J. and Billett E. E. (2001) Protection from MPTP-induced neurotoxicity in differentiating mouse N2a neuroblastoma cells. J. Neurochem. 76(3), 650–660.

    Article  PubMed  Google Scholar 

  • Dluzen D. E. (2000) Neuroprotective effects of estrogen upon the nigrostriatal dopaminergic system. J. Neurocytol. 29(5–6), 387–399.

    Article  PubMed  CAS  Google Scholar 

  • Egana J. T., Zambrano C., Nunez M. T., Gonzalez-Billault C., and Maccioni R. B. (2003). Iron-induced oxidative stress modify tau phosphorylation patterns in hippocampal cell cultures. Biometals 16(1), 215–223.

    Article  PubMed  CAS  Google Scholar 

  • Fall C. P. and Bennett J. P. Jr. (1999) Characterization and time course of MPP+-induced apoptosis in human SH-SY5Y neuroblastoma cells. J. Neurosci. Res. 55(5), 620–628.

    Article  PubMed  CAS  Google Scholar 

  • Farah C. A., Nguyen M. D., Julien J. P. and Leclerc N. (2003) Altered levels and distribution of microtubule-associated proteins before disease onset in a mouse model of amyotrophic lateral sclerosis. J. Neurochem. 84(1), 77–86.

    Article  PubMed  CAS  Google Scholar 

  • Gagne B., Gelinas S., Bureau G., Lagace B., Ramassamy C., Chiasson K., et al. (2003). Effects of estradiol, phyto-estrogens, and Ginkgo biloba extracts against 1-methyl-4-phenyl-pyridine-induced oxidative stress. Endocrine 21(1), 89–95.

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Segura L. M., Azcoitia I., and DonCarlos L. L. (2001) Neuroprotection by estradiol. Prog. Neurobiol. 63(1), 29–60.

    Article  PubMed  CAS  Google Scholar 

  • Gelinas S. and Martinoli M. G. (2002) Neuroprotective effect of estradiol and phytoestrogens on MPP+-induced cytotoxicity in neuronal PC12 cells. J. Neurosci. Res. 70(1), 90–96.

    Article  PubMed  CAS  Google Scholar 

  • Gelinas S., Bureau G., Valastro B., Massicotte G., Cicchetti F., Chiasson K., et al. (2004) Alpha and beta estradiol protect neuronal but not native PC12 cells from paraquat-induced oxidative stress. Neurotox. Res. 6(2), 141–148.

    Article  PubMed  Google Scholar 

  • Gelinas S., Chapados C., Beauregard M., Gosselin I., and Martinoli M. G. (2000) Effect of oxidative stress on stability and structure of neurofilament proteins. Biochem. Cell Biol. 78(6), 667–674.

    Article  PubMed  CAS  Google Scholar 

  • Gomez-Mancilla B. and Bedard P. J. (1992) Effect of estrogen and progesterone on L-dopa induced dyskinesia in MPTP-treated monkeys. Neurosci. Lett. 135(1), 129–132.

    Article  PubMed  CAS  Google Scholar 

  • Gong C. X., Wang J. Z., Iqbal K. and Grundke-Iqbal I. (2003) Inhibition of protein phosphatase 2A induces phosphorylation and accumulation of neurofilaments in metabolically active rat brain slices. Neurosci. Lett. 340(2), 107–110.

    Article  PubMed  CAS  Google Scholar 

  • Green P. S. and Simpkins J. W. (2000) Neuroprotective effects of estrogens: potential mechanisms of action. Int. J. Dev. Neurosci. 18(4–5), 347–358.

    Article  PubMed  CAS  Google Scholar 

  • Hale S. L., Birnbaum Y. and Kloner R. A. (1997) Estradiol, administered acutely, protects ischemic myocardium in both female and male rabbits. J. Cardiovasc. Pharmacol. Ther. 2(1), 47–52.

    Article  PubMed  CAS  Google Scholar 

  • Han H. J., Park S. H., Park H. J., Park K. M., Kang J. W., Lee J. H., et al. (2002) Effect of various oestrogens on cell injury and alteration of apical transporters induced by tert-butyl hydroperoxide in renal proximal tubule cells. Clin. Exp. Pharmacol. Physiol. 29(1–2), 60–67.

    Article  PubMed  CAS  Google Scholar 

  • Hand C. K. and Rouleau G. A. (2002) Familiar amyotrophic lateral sclerosis. Muscle Nerve 25(2) 135–139.

    Article  PubMed  CAS  Google Scholar 

  • Hirano A. (1994) Hirano bodies and related neuronal inclusions. Neuropathol. Appl. Neurobiol. 20(1), 3–11.

    Article  PubMed  CAS  Google Scholar 

  • Itano Y., Kitamura Y. and Nomura Y. (1994) 1-Methyl-4-phenylpyridinium (MPP+)-induced cell death in PC12 cells: inhibitory effects of several drugs. Neurochem. Int. 25(5) 419–424.

    Article  PubMed  CAS  Google Scholar 

  • Jayaraman D., Giasson B. I. and Mushynski W. E. (1995) Increased phosphorylation of neurofila ment subunits in PC12 cells and rat dorsal root ganglion neurons treated with N-Acetyl-Leu-Leu-norleucinal. Int J. Dev. Neurosci. 13(7), 753–758.

    Article  PubMed  CAS  Google Scholar 

  • Jenner P. (2003), Oxidative stress in Parkinson's disease. Ann. Neurol. 53(Suppl. 3), S26-S36.

    Article  PubMed  CAS  Google Scholar 

  • Kajta M. and Beyer C. (2003) Cellular strategies of estrogen-mediated neuroprotection during brain development. Endocrine 21(1), 3–9.

    Article  PubMed  CAS  Google Scholar 

  • Kam K. W., Qi J. S., Chen M. and Wong, T. M. (2004) Estrogen reduces cardiac injury and expression of beta 1-adrenoceptor upon ischemic insult in the rat heart. J. Pharmacol. Exp. Ther. 309(1), 8–15.

    Article  PubMed  CAS  Google Scholar 

  • Kocaturk P. A., Akbostanci M. C., Tan F. and Kavas G. O. (2000) Superoxide dismutase activity and zinc and copper concentrations in Parkinson's disease. Pathophysiology 7(1), 63–67.

    Article  PubMed  CAS  Google Scholar 

  • Kosta, P., Argyropoulou M. I., Markoula S. and Konitsiotis S. (2005) MRI evaluation of the basal ganglia size and iron content in patients with Parkinson's disease. J. Neurol 253, 26–32.

    Article  PubMed  Google Scholar 

  • Lee V., Trojanowski J. Q., and Schlaepfer W. W. (1982) Induction of neurofilament trip let proteins in PC12 cells by nerve growth factor. Brain Res. 238(1), 169–180.

    Article  PubMed  CAS  Google Scholar 

  • Leranth C., Roth R. H., Elsworth J. D., Naftolin F., Horvath T. L., and Redmond D. E. Jr. (2000) Estrogen is essential for maintaining nigrostriatal dopamine neurons in primates: implications for Parkinson's disease and memory. J. Neurosci. 20(23), 8604–8609.

    PubMed  CAS  Google Scholar 

  • Leranth C., Shanabrough M., and Redmond D. E. Jr. (2002) Gonadal hormones are responsible for maintaining the integrity of spine synapses in the CA1 hippocampal subfield of female nonhuman primates. J. Comp. Neurol. 447(1), 34–42.

    Article  PubMed  CAS  Google Scholar 

  • Leterrier J. F. and Eyer J. (1992) Age-dependent changes in the ultrastructure and in the molecular composition of rat brain microtubules. J. Neurochem. 59(3), 1126–1137.

    Article  PubMed  CAS  Google Scholar 

  • Lindenbaum M. H., Carbonetto S., and Mushynski W. E. (1987) Nerve growth factor enhances the synthesis, phosphorylation, and metabolic stability of neurofilament proteins in PC12 cells. J. Biol. Chem. 262(2), 605–610.

    PubMed  CAS  Google Scholar 

  • Liu Q., Raina A. K., Smith M. A., Sayre L. M., and Perry G. (2003) hydroxynonenal, tocxic carbonyl, and Alzheimer disease. Mol. Aspects Med. 24, 305–313.

    Article  PubMed  CAS  Google Scholar 

  • Liu S. J., Fang Z. Y., Yang Y., Deng H. M., and Wang J. Z. (2003) Alzheimer-like phosphorylation of tau and neurofilament induced by cocaine in vivo. Acta Pharmacol. Sin. 24(6), 512–518.

    PubMed  CAS  Google Scholar 

  • Ma Z. Q., Spreafico E., Pollio G., Santagati S., Conti, E., Cattaneo E., and Maggi A. (1993) Activated estrogen receptor mediates growth arrest and differentiation of a neuroblastoma cell line. Proc. Natl. Acad. Sci. U. S. A. 90(8), 3740–3744.

    Article  PubMed  CAS  Google Scholar 

  • MacLusky N. J., Chalmers-Redman R., Kay G., Ju W., Nethrapalli I. S., and Tatton W. G. (2003) Ovarian steroids reduce apoptosis induced by trophic insufficiency in nerve growth factor-differentiated PC12 cells and axotomized rat facial motoneurons. Neuroscience 118(3), 741–754.

    Article  PubMed  CAS  Google Scholar 

  • Miller D. B., Ali S. F., O'Callaghan J. P., and Laws S. C. (1998) The impact of gender and estrogen on striatal dopaminergic neurotoxicity. Ann. N. Y. Acad. Sci. 844, 153–165.

    Article  PubMed  CAS  Google Scholar 

  • Mitsumoto H., and Gambetti P. (1986) Impaired slow axonal transport in wobbler mouse motor neuron disease. Ann. Neurol. 19(1), 36–43.

    Article  PubMed  CAS  Google Scholar 

  • Mori H., Oda M., and Mizuno Y. (1996) Cortical ballooned neurons in progressive supranuclear palsy. Neurosci. Lett. 209(2), 109–112.

    Article  PubMed  CAS  Google Scholar 

  • Nilsen J., Mor G., and Naftolin F. (1998) Raloxifene induces neurite outgrowth in estrogen receptor positive PC12 cells. Menopause 5(4), 211–216.

    Article  PubMed  CAS  Google Scholar 

  • Perez-Olle R., Lopez-Toledano M. A., Goryunov D., Cabrera-Poch N., Stefanis L., Brown K., and Liem R. K. (2005) Mutations in the neurofilament light gene linked to Charcot-Marie-Tooth disease cause defects in transport. J. Neurochem. 93(4), 861–874.

    Article  PubMed  CAS  Google Scholar 

  • Pernas-Alonso R., Perrone-Capano C., Volpicelli F., and di Porzio U. (2001) Regionalized neurofilament accumulation and motoneuron degeneration are linked phenotypes in Wobbler neurom uscular disease. Neuro biol. Dis. 8(4), 581–589.

    Article  CAS  Google Scholar 

  • Pernas-Alonso R., Schaffner A. E., Perrone-Capano C., Orlando A., Morelli F., Hansen C. T., et al. (1996), Early upregulation of medium neurofilament gene expression in developing spinal cord of the Wobbler mouse mutant. Brain Res. Mol. Brain Res. 38(2), 267–275.

    Article  PubMed  CAS  Google Scholar 

  • Pong K. (2003) Oxidative stress in neurodegenerative diseases: therapeutic implications for superoxide dismutase mimetics. Expert Opin. Biol. Ther. 3(1), 127–139.

    Article  PubMed  CAS  Google Scholar 

  • Radunovic A., Porto W. G., Zeman S., and Leigh P. N. (1997) Increased mitochondrial superoxide dismutase activity in Parkinson's disease but not amyotrophic lateral sclerosis motor cortex. Neurosci. Lett. 239(2–3), 105–108.

    Article  PubMed  CAS  Google Scholar 

  • Rahaman S. O., Ghosh S., Mohanakumar K. P., Das S., and Sakar P. K. (2001) Hypothyroidism in the developing rat brain is associated with marked oxidative stress and aberrant intraneuronal accumulation of neurofilaments. Neurosci. Res. 40, 273–279.

    Article  PubMed  CAS  Google Scholar 

  • Ramirez A. D., Liu X., and Menniti F. S. (2003) Repeated estradiol treatment prevents MPTP-induced dopamine depletion in male mice. Neuroendocrinology 77(4), 223–231.

    Article  PubMed  CAS  Google Scholar 

  • Rau S. W., Dubal D. B., Bottner M., Gerhold L. M., and Wise P. M. (2003) Estradiolattenuates programmed cell death after stroke-like injury. J. Neurosci. 23(36), 11420–11426.

    PubMed  CAS  Google Scholar 

  • Rousseau J., Cossette L., Grenier S., and Martinoli M.-G. (2002) Modulation of prolactin expression by xeno-estrogens. Gen. Comp. Endocrinol. 126, 175–182.

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Larrea M. B., Garrido M. J., and Lacort M. (1993). Estradiol-induced effects on glutathione metabolism in rat hepatocytes. J. Biochem. (Tokyo) 113(5), 563–567.

    CAS  Google Scholar 

  • Schapira A. H., Cooper J. M., Dexter D., Clark J. B., Jenner P., and Marsden C. D. (1990a) Mitochondrial complex I deficiency in Parkinson's disease. J. Neurochem. 54(3), 823–827.

    Article  PubMed  CAS  Google Scholar 

  • Schapira A. H., Holt I. J., Sweeney M., Harding A. E., Jenner P., and Marsden C. D. (1990b) Mitochondrial DNA analysis in Parkinson's disease. Mov. Disord. 5(4), 294–297.

    Article  PubMed  CAS  Google Scholar 

  • Schimmelpfeng J., Weibezahn K. F., and Dertinger H. (2004) Quantification of NGF-dependent neuronal differentiation of PC-12 cells by means of neurofilament-LmRNA expression and neuronal outgrowth. J. Neurosci. Methods 139(2), 299–306.

    Article  PubMed  CAS  Google Scholar 

  • Schmidt R. E., Beaudet L. N., Plurad S. B., and Dorsey D. A. (1997) A xonal cytoskeletal pathology in aged and diabetic human sympathetic autonomic ganglia. Brain Res. 769(2), 375–383.

    Article  PubMed  CAS  Google Scholar 

  • Schmittgen T. D., and Zakrajsek B. A. (2000) Effect of experimental treatment on housekeeping gene expression: validation by real-time, quantitative RT-PCR. J. Biochem. Biophys. Methods 46(1–2), 69–81.

    Article  PubMed  CAS  Google Scholar 

  • Schober A. (2004) Classic toxin-induced animal models of Parkinson's disease: 6-OHDA and MPTP. Cell Tissue Res. 318(1), 215–224.

    Article  PubMed  Google Scholar 

  • Schon E. A. and Manfredi G. (2003) Neuronal degeneration and mitochondrial dysfunction. J. Clin. Invest. 111(3), 303–312.

    PubMed  CAS  Google Scholar 

  • Scoville S. A., Bufton S. M., and Liuzzi F. J. (1997) Estrogen regulates neurofilament gene expression in adult female rat dorsal root ganglion neurons. Exp. Neurol. 146(2), 596–599.

    Article  PubMed  CAS  Google Scholar 

  • Shepherd C. E., McCann H., Thiel E., and Halliday G. M. (2002) Neurofilament-immunoreactive neurons in Alzheimer's disease and dementia with Lewy bodies. Neurobiol Dis. 9(2), 249–257.

    Article  PubMed  Google Scholar 

  • Smeyne R. J., and Jackson-Lewis V. (2005) The MPTP model of Parkinson's disease. Brain Res. Mol. Brain Res. 134(1), 57–66.

    Article  PubMed  CAS  Google Scholar 

  • Smith D. S., and Tsai L. H. (2002) Cdk5 behind the wheel: a role in trafficking and transport? Trends Cell Biol. 12(1), 28–36.

    Article  PubMed  Google Scholar 

  • Stadtman E. R., and Berlett B. S. (1997) Reactive oxygen-mediated protein oxidation in aging and disease. Chem. Res. Toxicol. 10(5), 485–494.

    Article  PubMed  CAS  Google Scholar 

  • Topalli I., and Etgen A. M. (2004) Insulin-like growth factor-I receptor and estrogen receptor crosstalk mediates horm one-induced neurite outgrowth in PC12 cells. Brain Res. 1030(1), 116–124.

    Article  PubMed  CAS  Google Scholar 

  • Toran-A'llerand C. D. (2004) Estrogen and the brain: beyond ER-alpha and ER-beta. Exp. Gerontol. 39(11–12), 1579–1586.

    Article  CAS  Google Scholar 

  • Toung T. J., Traystman R. J., and Hurn P. D. (1998) Estrogen-mediated neuroprotection after experimental stroke in male rats. Stroke 29(8), 1666–1670.

    PubMed  CAS  Google Scholar 

  • Trimpin S., Mixon A. E., Stapels M. D., Kim M. Y., Spencer P. S., and Deinzer M. L. (2004) Identification of endogenous phosphorylation sites of bovine medium and low molecular weight neurofilament proteins by tandem mass spectrometry. Biochemistry 43(7), 2091–2105.

    Article  PubMed  CAS  Google Scholar 

  • Wise, P. M., Dubal D. B., Wilson M. E., Rau S. W., and Liu Y. (2001) Estrogens: trophic and protective factors in the adult brain. Front. Neuroendocrinol. 22(1), 33–66.

    Article  PubMed  CAS  Google Scholar 

  • Wise P. M. (2002) Estrogens and neuroprotection. Trends Endocrinol. Metab. 13, 229–230.

    Article  PubMed  CAS  Google Scholar 

  • Yang S. H., Liu R., Wu S. S., and Simpkins J. W. (2003) The use of estrogens and related compounds in the treatment of damage from cerebral ischemia. Ann. N. Y. Acad. Sci. 1007, 101–107.

    Article  PubMed  CAS  Google Scholar 

  • Zecca L., Berg D., Arzberger T., Ruprecht P., Rausch W. D., Musicco M., et al. (2005) In vivo detection of iron and neuromelanin by transcranial sonography: A new approach for early detection of substantia nigra damage. Mov. Disord. 20, 1278–1285.

    Article  PubMed  Google Scholar 

  • Zhang H., Joseph J., Feix J., Hogg N., and Kalyanaraman B. (2001) Nitration and oxidation of a hydrophobic tyrosine probe by peroxynitrite in membranes: comparison with nitration and oxidation of tyrosine by peroxynitrite in aqueous solution. Biochemistry 40(25), 7675–7686.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry and Research Group in Neuroscience, Université du Québec à Trois-Rivières, Trois-Rivières, Québec, Canada

    Keith Chiasson, Vicky Lahaie-Collins, Julie Bournival, Benoit Delapierre, Sylvie Gélinas & Maria-Grazia Martinoli

  2. Neuroscience Research Center, Centre de Recherche de l'Université Laval, G1V 4G2, Ste-Foy, Québec, Canada

    Keith Chiasson & Maria-Grazia Martinoli

Authors
  1. Keith Chiasson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vicky Lahaie-Collins
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Julie Bournival
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Benoit Delapierre
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sylvie Gélinas
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maria-Grazia Martinoli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria-Grazia Martinoli.

Additional information

These authors contributed equally to this paper.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chiasson, K., Lahaie-Collins, V., Bournival, J. et al. Oxidative stress and 17-α- and 17-β-estradiol modulate neurofilaments differently. J Mol Neurosci 30, 297–310 (2006). https://doi.org/10.1385/JMN:30:3:297

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1385/JMN:30:3:297

Index Entries

Search

Navigation