Skip to main content
SpringerLink
Log in

Dietary Supplementation with S-Adenosyl Methionine Delays the Onset of Motor Neuron Pathology in a Murine Model of Amyotrophic Lateral Sclerosis

  • Original Paper
  • Published:
NeuroMolecular Medicine Aims and scope Submit manuscript

Abstract

The full range of causative factors in Amyotrophic lateral sclerosis (ALS) remains elusive, but oxidative stress is recognized as a contributing factor. Mutations in Cu/Zn superoxide dismutase 1 (SOD-1), associated with familial ALS, promote widespread oxidative damage. Mice-expressing G93A mutant human SOD-1 mice display multiple pathological changes characteristic of ALS and are therefore useful for therapeutic development. Dietary supplementation with S-adenosyl methionine (SAM) has provided multiple neuroprotective effects in mouse models of age-related cognitive pathology. We examined herein whether SAM supplementation could affect the course of motor neuron pathology in mice-expressing mutant human SOD-1. SAM delayed disease onset by 2–3 weeks. SAM also delayed hallmarks of neurodegeneration in these mice and in ALS, including preventing loss of motor neurons, and reducing gliosis, SOD-1 aggregation, protein carbonylation, and induction of antioxidant activity. SAM did not increase survival time. These preliminary findings, using a single concentration of SAM, suggest that SAM supplementation maybe useful as part of a comprehensive therapeutic approach for ALS.

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

Similar content being viewed by others

References

  • Agar, J., & Durham, H. (2003). Relevance of oxidative injury in the pathogenesis of motor neuron diseases. Amyotroph Lateral Scler Other Motor Neuron Disord, 4, 232–242.

    Article  PubMed  CAS  Google Scholar 

  • Barbeito, L. H., Pehar, M., Cassina, P., Vargas, M. R., Peluffo, H., Viera, L., et al. (2004). A role for astrocytes in motor neuron loss in amyotrophic lateral sclerosis. Brain Research Brain Research Reviews, 47, 263–274.

    Article  PubMed  CAS  Google Scholar 

  • Barber, S. C., Mead, R. J., & Shaw, P. J. (2006). Oxidative stress in ALS: A mechanism of neurodegeneration and a therapeutic target. Biochimica et Biophysica Acta, 1762, 1051–1067.

    PubMed  CAS  Google Scholar 

  • Barneoud, P., & Curet, O. (1999). Beneficial effects of lysine acetylsalicylate, a soluble salt of aspirin, on motor performance in a transgenic model of amyotrophic lateral sclerosis. Experimental Neurology, 155, 243–251.

    Article  PubMed  CAS  Google Scholar 

  • Barneoud, P., Lolivier, J., Sanger, D. J., Scatton, B., & Moser, P. (1997). Quantitative motor assessment in FALS mice: A longitudinal study. NeuroReport, 8, 2861–2865.

    Article  PubMed  CAS  Google Scholar 

  • Bottiglieri, T. (2002). S-Adenosyl-L-methionine (SAMe): From the bench to the bedside–molecular basis of a pleiotropic molecule. American Journal of Clinical Nutrition, 76, 1151S–1157S.

    PubMed  CAS  Google Scholar 

  • Bottiglieri, T., Godfrey, P., Flynn, T., Carney, M. W., Toone, B. K., & Reynolds, E. H. (1990). Cerebrospinal fluid S-adenosylmethionine in depression and dementia: Effects of treatment with parenteral and oral S-adenosylmethionine. Journal of Neurology, Neurosurgery and Psychiatry, 53, 1096–1098.

    Article  CAS  Google Scholar 

  • Bruijn, L. I., Miller, T. M., & Cleveland, D. W. (2004). Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annual Review of Neuroscience, 27, 723–749.

    Article  PubMed  CAS  Google Scholar 

  • Chan, A., Paskavitz, J., Remington, R., Rasmussen, S., & Shea, T. B. (2008a). Efficacy of a vitamin/nutriceutical formulation for early-stage Alzheimer’s disease: A 1-year, open-label pilot study with an 16-month caregiver extension. American Journal of Alzheimer’s Disease and Other Dementias, 23, 571–585.

    Article  PubMed  Google Scholar 

  • Chan, A., & Shea, T. B. (2007). Effects of dietary supplementation with N-acetyl cysteine, acetyl-L-carnitine and S-adenosyl methionine on cognitive performance and aggression in normal mice and mice expressing human ApoE4. Neuromolecular Medicine, 9, 264–269.

    Article  PubMed  CAS  Google Scholar 

  • Chan, A., Tchantchou, F., Graves, V., Rozen, R., & Shea, T. B. (2008b). Dietary and genetic compromise in folate availability reduces acetylcholine, cognitive performance and increases aggression: Critical role of S-adenosyl methionine. The Journal of Nutrition, Health and Aging, 12, 252–261.

    Article  CAS  Google Scholar 

  • Chi, L., Ke, Y., Luo, C., Gozal, D., & Liu, R. (2007). Depletion of reduced glutathione enhances motor neuron degeneration in vitro and in vivo. Neuroscience, 144, 991–1003.

    Article  PubMed  CAS  Google Scholar 

  • Chiang, P. K., Gordon, R. K., Tal, J., Zeng, G. C., Doctor, B. P., Pardhasaradhi, K., et al. (1996). S-Adenosylmethionine and methylation. FASEB Journal, 10, 471–480.

    PubMed  CAS  Google Scholar 

  • Cozzolino, M., Ferri, A., & Carri, M. T. (2008). Amyotrophic lateral sclerosis: From current developments in the laboratory to clinical implications. Antioxidants and Redox Signaling, 10, 405–443.

    Article  PubMed  CAS  Google Scholar 

  • Dupuis, L., Gonzalez de Aguilar, J. L., Oudart, H., de Tapia, M., Barbeito, L., & Loeffler, J. P. (2004). Mitochondria in amyotrophic lateral sclerosis: A trigger and a target. Neuro-Degenerative Diseases, 1, 245–254.

    PubMed  Google Scholar 

  • Dwyer, B. E., Lu, S. Y., & Nishimura, R. N. (1998). Heme oxygenase in the experimental ALS mouse. Experimental Neurology, 150, 206–212.

    Article  PubMed  CAS  Google Scholar 

  • Erdmann, K., Cheung, B. W., Immenschuh, S., & Schroder, H. (2008). Heme oxygenase-1 is a novel target and antioxidant mediator of S-adenosylmethionine. Biochemical and Biophysical Research Communications, 368, 937–941.

    Article  PubMed  CAS  Google Scholar 

  • Esposito, E., Rossi, C., Amodio, R., Di Castelnuovo, A., Bendotti, C., Rotondo, T., et al. (2000). Lyophilized red wine administration prolongs survival in an animal model of amyotrophic lateral sclerosis. Annals of Neurology, 48, 686–687.

    Article  PubMed  CAS  Google Scholar 

  • Exner, M., Minar, E., Wagner, O., & Schillinger, M. (2004). The role of heme oxygenase-1 promoter polymorphisms in human disease. Free Radical Biology and Medicine, 37, 1097–1104.

    Article  PubMed  CAS  Google Scholar 

  • Fornai, F., Longone, P., Cafaro, L., Kastsiuchenka, O., Ferrucci, M., Manca, M. L., et al. (2008). Lithium delays progression of amyotrophic lateral sclerosis. Proceedings of the National Academy of Sciences of the United States of America, 105, 2052–2057.

    Article  PubMed  Google Scholar 

  • Fujita, K., Kato, T., Yamauchi, M., Ando, M., Honda, M., & Nagata, Y. (1998). Increases in fragmented glial fibrillary acidic protein levels in the spinal cords of patients with amyotrophic lateral sclerosis. Neurochemical Research, 23, 169–174.

    Article  PubMed  CAS  Google Scholar 

  • Gharib, A., Sarda, N., Chabannes, B., Cronenberger, L., & Pacheco, H. (1982). The regional concentrations of S-adenosyl-L-methionine, S-adenosyl-L-homocysteine, and adenosine in rat brain. Journal of Neurochemistry, 38, 810–815.

    Article  PubMed  CAS  Google Scholar 

  • Grunfeld, J. F., Barhum, Y., Blondheim, N., Rabey, J. M., Melamed, E., & Offen, D. (2007). Erythropoietin delays disease onset in an amyotrophic lateral sclerosis model. Experimental Neurology, 204, 260–263.

    Article  PubMed  CAS  Google Scholar 

  • Guo, H., Lai, L., Butchbach, M. E., Stockinger, M. P., Shan, X., Bishop, G. A., et al. (2003). Increased expression of the glial glutamate transporter EAAT2 modulates excitotoxicity and delays the onset but not the outcome of ALS in mice. Human Molecular Genetics, 12, 2519–2532.

    Article  PubMed  CAS  Google Scholar 

  • Gurney, M. E., Cutting, F. B., Zhai, P., Doble, A., Taylor, C. P., Andrus, P. K., et al. (1996). Benefit of vitamin E, riluzole, and gabapentin in a transgenic model of familial amyotrophic lateral sclerosis. Annals of Neurology, 39, 147–157.

    Article  PubMed  CAS  Google Scholar 

  • Gurney, M. E., Pu, H., Chiu, A. Y., Dal Canto, M. C., Polchow, C. Y., Alexander, D. D., et al. (1994). Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science, 264, 1772–1775.

    Article  PubMed  CAS  Google Scholar 

  • Hensley, K., Mhatre, M., Mou, S., Pye, Q. N., Stewart, C., West, M., et al. (2006). On the relation of oxidative stress to neuroinflammation: Lessons learned from the G93A-SOD1 mouse model of amyotrophic lateral sclerosis. Antioxidants and Redox Signaling, 8, 2075–2087.

    Article  PubMed  CAS  Google Scholar 

  • Ho, P. I., Ashline, D., Dhitavat, S., Ortiz, D., Collins, S. C., Shea, T. B., et al. (2003). Folate deprivation induces neurodegeneration: Roles of oxidative stress and increased homocysteine. Neurobiology of Diseases, 14, 32–42.

    Article  CAS  Google Scholar 

  • Ho, P. I., Ortiz, D., Rogers, E., & Shea, T. B. (2002). Multiple aspects of homocysteine neurotoxicity: Glutamate excitotoxicity, kinase hyperactivation and DNA damage. Journal of Neuroscience Research, 70, 694–702.

    Article  PubMed  CAS  Google Scholar 

  • Holzbaur, E. L., Howland, D. S., Weber, N., Wallace, K., She, Y., Kwak, S., et al. (2006). Myostatin inhibition slows muscle atrophy in rodent models of amyotrophic lateral sclerosis. Neurobiology of Diseases, 23, 697–707.

    Article  CAS  Google Scholar 

  • Hyland, K., Smith, I., Bottiglieri, T., Perry, J., Wendel, U., Clayton, P. T., et al. (1988). Demyelination and decreased S-adenosylmethionine in 5, 10-methylenetetrahydrofolate reductase deficiency. Neurology, 38, 459–462.

    PubMed  CAS  Google Scholar 

  • Ito, H., Wate, R., Zhang, J., Ohnishi, S., Kaneko, S., Ito, H., et al. (2008). Treatment with edaravone, initiated at symptom onset, slows motor decline and decreases SOD1 deposition in ALS mice. Experimental Neurology, 213, 448–455.

    Article  PubMed  CAS  Google Scholar 

  • Izumi, Y., & Kaji, R. (2007). Clinical trials of ultra-high-dose methylcobalamin in ALS. Brain Nerve, 59, 1141–1147.

    PubMed  CAS  Google Scholar 

  • Johnston, J. A., Dalton, M. J., Gurney, M. E., & Kopito, R. R. (2000). Formation of high molecular weight complexes of mutant Cu, Zn-superoxide dismutase in a mouse model for familial amyotrophic lateral sclerosis. Proceedings of the National Academy of Sciences of the United States of America, 97, 12571–12576.

    Article  PubMed  CAS  Google Scholar 

  • Julien, J. P., & Mushynski, W. E. (1998). Neurofilaments in health and disease. Progress in Nucleic Acid Research and Molecular Biology, 61, 1–23.

    Article  PubMed  CAS  Google Scholar 

  • Jung, C., Rong, Y., Doctrow, S., Baudry, M., Malfroy, B., & Xu, Z. (2001). Synthetic superoxide dismutase/catalase mimetics reduce oxidative stress and prolong survival in a mouse amyotrophic lateral sclerosis model. Neuroscience Letters, 304, 157–160.

    Article  PubMed  CAS  Google Scholar 

  • Kennedy, B. P., Bottiglieri, T., Arning, E., Ziegler, M. G., Hansen, L. A., & Masliah, E. (2004). Elevated S-adenosylhomocysteine in Alzheimer brain: Influence on methyltransferases and cognitive function. Journal of neural transmission, 111, 547–567.

    Article  PubMed  CAS  Google Scholar 

  • Levine, J. B., Kong, J., Nadler, M., & Xu, Z. (1999). Astrocytes interact intimately with degenerating motor neurons in mouse amyotrophic lateral sclerosis (ALS). Glia, 28, 215–224.

    Article  PubMed  CAS  Google Scholar 

  • Lieber, C. S., & Packer, L. (2002). S-Adenosylmethionine: molecular, biological, and clinical aspects–an introduction. American Journal of Clinical Nutrition, 76, 1148S–1150S.

    PubMed  CAS  Google Scholar 

  • Liu, R., Li, B., Flanagan, S. W., Oberley, L. W., Gozal, D., & Qiu, M. (2002). Increased mitochondrial antioxidative activity or decreased oxygen free radical propagation prevent mutant SOD1-mediated motor neuron cell death and increase amyotrophic lateral sclerosis-like transgenic mouse survival. Journal of Neurochemistry, 80, 488–500.

    Article  PubMed  CAS  Google Scholar 

  • Lu, S. C. (2000). S-Adenosylmethionine. International Journal of Biochemistry and Cell Biology, 32, 391–395.

    Article  PubMed  CAS  Google Scholar 

  • Mahoney, D. J., Kaczor, J. J., Bourgeois, J., Yasuda, N., & Tarnopolsky, M. A. (2006). Oxidative stress and antioxidant enzyme upregulation in SOD1–G93A mouse skeletal muscle. Muscle and Nerve, 33, 809–816.

    Article  PubMed  CAS  Google Scholar 

  • Mattson, M. P., & Shea, T. B. (2003). Folate and homocysteine metabolism in neural plasticity and neurodegenerative disorders. Trends in Neurosciences, 26, 137–146.

    Article  PubMed  CAS  Google Scholar 

  • Muller, T., Woitalla, D., Hauptmann, B., Fowler, B., & Kuhn, W. (2001). Decrease of methionine and S-adenosylmethionine and increase of homocysteine in treated patients with Parkinson’s disease. Neuroscience Letters, 308, 54–56.

    Article  PubMed  CAS  Google Scholar 

  • Oommen, A. M., Griffin, J. B., Sarath, G., & Zempleni, J. (2005). Roles for nutrients in epigenetic events. The Journal of Nutritional Biochemistry, 16, 74–77.

    Article  PubMed  CAS  Google Scholar 

  • Park, J. H., Hong, Y. H., Kim, H. J., Kim, S. M., Kim, M. J., Park, K. S., et al. (2007). Pyruvate slows disease progression in a G93A SOD1 mutant transgenic mouse model. Neuroscience Letters, 413, 265–269.

    Article  PubMed  CAS  Google Scholar 

  • Perluigi, M., Poon, H. F., Maragos, W., Pierce, W. M., Klein, J. B., Calabrese, V., et al. (2005). Proteomic analysis of protein expression and oxidative modification in r6/2 transgenic mice: A model of Huntington disease. Mol Cell Proteomics, 4, 1849–1861.

    Article  PubMed  CAS  Google Scholar 

  • Poon, H. F., Hensley, K., Thongboonkerd, V., Merchant, M. L., Lynn, B. C., Pierce, W. M., et al. (2005). Redox proteomics analysis of oxidatively modified proteins in G93A-SOD1 transgenic mice–a model of familial amyotrophic lateral sclerosis. Free Radical Biology and Medicine, 39, 453–462.

    Article  PubMed  CAS  Google Scholar 

  • Rakhit, R., Crow, J. P., Lepock, J. R., Kondejewski, L. H., Cashman, N. R., & Chakrabartty, A. (2004). Monomeric Cu, Zn-superoxide dismutase is a common misfolding intermediate in the oxidation models of sporadic and familial amyotrophic lateral sclerosis. Journal of Biological Chemistry, 279, 15499–15504.

    Article  PubMed  CAS  Google Scholar 

  • Rao, S. D., & Weiss, J. H. (2004). Excitotoxic and oxidative cross-talk between motor neurons and glia in ALS pathogenesis. Trends in Neurosciences, 27, 17–23.

    Article  PubMed  CAS  Google Scholar 

  • Ratter, F., Germer, M., Fischbach, T., Schulze-Osthoff, K., Peter, M. E., Droge, W., et al. (1996). S-adenosylhomocysteine as a physiological modulator of Apo-1-mediated apoptosis. International Immunology, 8, 1139–1147.

    Article  PubMed  CAS  Google Scholar 

  • Remington, R., Chan, A., Paskavitz, J., & Shea, T. B. (2009). Efficacy of a vitamin/nutriceutical formulation for moderate-stage to later-stage Alzheimer’s disease: A placebo-controlled pilot study. American Journal of Alzheimer’s Disease and Other Dementias, 24, 27–33.

    Article  PubMed  Google Scholar 

  • Robberecht, W. (2000). Oxidative stress in amyotrophic lateral sclerosis. Journal of Neurology, 247(Suppl 1), I1–I6.

    Article  PubMed  Google Scholar 

  • Rosen, D. R., Siddique, T., Patterson, D., Figlewicz, D. A., Sapp, P., Hentati, A., et al. (1993). Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature, 362, 59–62.

    Article  PubMed  CAS  Google Scholar 

  • Rothstein, J. D. (1996). Therapeutic horizons for amyotrophic lateral sclerosis. Current Opinion in Neurobiology, 6, 679–687.

    Article  PubMed  CAS  Google Scholar 

  • Schatz, R. A., Wilens, T. E., & Sellinger, O. Z. (1981). Decreased in vivo protein and phospholipid methylation after in vivo elevation of brain S-adenosyl-homocysteine. Biochemical and Biophysical Research Communications, 98, 1097–1107.

    Article  PubMed  CAS  Google Scholar 

  • Scott, S., Kranz, J. E., Cole, J., Lincecum, J. M., Thompson, K., Kelly, N., et al. (2008). Design, power, and interpretation of studies in the standard murine model of ALS. Amyotrophic Lateral Sclerosis, 9, 4–15.

    Article  PubMed  CAS  Google Scholar 

  • Sekiya, M., Ichiyanagi, T., Ikeshiro, Y., & Yokozawa, T. (2009). The Chinese prescription Wen-Pi-Tang extract delays disease onset in amyotrophic lateral sclerosis model mice while attenuating the activation of glial cells in the spinal cord. Biological and Pharmaceutical Bulletin, 32, 382–388.

    Article  PubMed  CAS  Google Scholar 

  • Selhub, J., & Miller, J. W. (1992). The pathogenesis of homocysteinemia: interruption of the coordinate regulation by S-adenosylmethionine of the remethylation and transsulfuration of homocysteine. American Journal of Clinical Nutrition, 55, 131–138.

    PubMed  CAS  Google Scholar 

  • Shea, T. B., & Chan, A. (2008). S-adenosyl methionine: a natural therapeutic agent effective against multiple hallmarks and risk factors associated with Alzheimer’s disease. Journal of Alzheimer’s Disease, 13, 67–70.

    PubMed  CAS  Google Scholar 

  • Shea, T. B., & Rogers, E. (2002). Folate quenches oxidative damage in brains of apolipoprotein E-deficient mice: Augmentation by vitamin E. Molecular Brain Research, 108, 1–6.

    Article  PubMed  CAS  Google Scholar 

  • Shibata, N. (2001). Transgenic mouse model for familial amyotrophic lateral sclerosis with superoxide dismutase-1 mutation. Neuropathology, 21, 82–92.

    Article  PubMed  CAS  Google Scholar 

  • Strong, M. J. (2003). The basic aspects of therapeutics in amyotrophic lateral sclerosis. Pharmacology and Therapeutics, 98, 379–414.

    Article  PubMed  CAS  Google Scholar 

  • Tchantchou, F., Graves, M., Falcone, D., & Shea, T. B. (2008). S-adenosylmethionine mediates glutathione efficacy by increasing glutathione S-transferase activity: Implications for S-adenosyl methionine as a neuroprotective dietary supplement. Journal of Alzheimer’s Disease, 14, 323–328.

    PubMed  CAS  Google Scholar 

  • Tchantchou, F., Graves, M., & Shea, T. B. (2006). Expression and activity of methionine cycle genes are altered following folate and vitamin E deficiency under oxidative challenge: Modulation by apolipoprotein E-deficiency. Nutritional Neuroscience, 9, 17–24.

    Article  PubMed  CAS  Google Scholar 

  • Turner, B. J., & Talbot, K. (2008). Transgenics, toxicity and therapeutics in rodent models of mutant SOD1-mediated familial ALS. Progress in Neurobiology, 85, 94–134.

    Article  PubMed  CAS  Google Scholar 

  • Veldink, J. H., Kalmijn, S., Groeneveld, G. J., Wunderink, W., Koster, A., de Vries, J. H., et al. (2007). Intake of polyunsaturated fatty acids and vitamin E reduces the risk of developing amyotrophic lateral sclerosis. Journal of Neurology, Neurosurgery and Psychiatry, 78, 367–371.

    Article  CAS  Google Scholar 

  • Wang, R., & Zhang, D. (2005). Memantine prolongs survival in an amyotrophic lateral sclerosis mouse model. European Journal of Neuroscience, 22, 2376–2380.

    Article  PubMed  Google Scholar 

  • Watanabe, M., Dykes-Hoberg, M., Culotta, V. C., Price, D. L., Wong, P. C., & Rothstein, J. D. (2001). Histological evidence of protein aggregation in mutant SOD1 transgenic mice and in amyotrophic lateral sclerosis neural tissues. Neurobiology of Diseases, 8, 933–941.

    Article  CAS  Google Scholar 

  • Weydt, P., Hong, S. Y., Kliot, M., & Moller, T. (2003). Assessing disease onset and progression in the SOD1 mouse model of ALS. NeuroReport, 14, 1051–1054.

    Article  PubMed  Google Scholar 

  • Weydt, P., Hong, S., Witting, A., Moller, T., Stella, N., & Kliot, M. (2005). Cannabinol delays symptom onset in SOD1 (G93A) transgenic mice without affecting survival. Amyotrophic Lateral Sclerosis and Other Motor Neuron Disorders, 6, 182–184.

    Article  PubMed  CAS  Google Scholar 

  • Xu, Z., Chen, S., Li, X., Luo, G., Li, L., & Le, W. (2006). Neuroprotective effects of (-)-epigallocatechin-3-gallate in a transgenic mouse model of amyotrophic lateral sclerosis. Neurochemical Research, 31, 1263–1269.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, X., Chen, S., Li, L., Wang, Q., & Le, W. (2008). Folic acid protects motor neurons against the increased homocysteine, inflammation and apoptosis in SOD1 G93A transgenic mice. Neuropharmacology, 54, 1112–1119.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was inspired by and is dedicated to the memory of Suzanne Seidel, mother, teacher, and philosopher, who passed away from ALS. This research was supported by internal funds from UMass Lowell. The continued advice of UMass Lowell Veterinarian Dr. Sonja (“Scout”) Chou is greatly appreciated.

Author information

Authors and Affiliations

  1. Center for Cellular Neurobiology and Neurodegeneration Research, Department of Biological Sciences, University of Massachusetts Lowell, Lowell, MA, 01854, USA

    James Suchy, Sangmook Lee, Ambar Ahmed & Thomas B. Shea

Authors
  1. James Suchy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sangmook Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ambar Ahmed
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thomas B. Shea
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thomas B. Shea.

Additional information

James Suchy and Sangmook Lee contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Suchy, J., Lee, S., Ahmed, A. et al. Dietary Supplementation with S-Adenosyl Methionine Delays the Onset of Motor Neuron Pathology in a Murine Model of Amyotrophic Lateral Sclerosis. Neuromol Med 12, 86–97 (2010). https://doi.org/10.1007/s12017-009-8089-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12017-009-8089-7

Keywords

Search

Navigation