Resveratrol neuroprotection in a chronic mouse model of multiple sclerosis

Frontiers in Neurology

Volumn MAY, Issue , 2012, Pages

  Fonseca Kelly, Zoe ^a   Nassrallah, Mayssa ^a   Uribe, Jorge ^a   Khan, Reas S ^a   Dine, Kimberly ^a   Dutt, Mahasweta ^a   Shindler, Kenneth S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

EAE; Multiple sclerosis; Neuroprotection; Optic neuritis; Resveratrol; SIRT1

Indexed keywords

EID: 84865851734     PISSN: None     EISSN: 16642295     Source Type: Journal    
DOI: 10.3389/fneur.2012.00084     Document Type: Article

References (34)

1. Arnold, A. C. (2005). Evolving management of optic neuritis and multiple sclerosis. Am. J. Ophthalmol. 139, 1101-1108.
2. Costello, F., Coupland, S., Hodge, W., Lorello, G. R., Koroluk, J., Pan, Y. I., Freedman, M. S., Zackon, D. H., and Kardon, R. H. (2006). Quantifying axonal loss after optic neuritis with optical coherence tomography. Ann. Neurol. 59, 963-969.
3. De La Lastra, C. A., and Villegas, I. (2007). Resveratrol as an antioxidant and pro-oxidant agent: mechanisms and clinical implications. Biochem. Soc. Trans. 35, 1156-1160.
4. Fisher, J. B., Jacobs, D. A., Markowitz, C. E., Galetta, S. L., Volpe, N. J., Nano-Schiavi, M. L., Baier, M. L., Frohman, E. M., Winslow, H., Frohman, T. C., Calabresi, P. A., Maguire, M. G., Cutter, G. R., and Balcer, L. J. (2006). Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis. Ophthalmology 113, 324-332.
5. Fitzgerald, D. C., Ciric, B., Touil, T., Harle, H., Grammatikopolou, J., Das Sarma, J., Gran, B., Zhang, G. X., and Rostami, A. (2007). Suppressive effect of IL-27 on encephalitogenic Th17 cells and the effector phase of experimental autoimmune encephalomyelitis. J. Immunol. 179, 3268-3275.
6. Gran, B., Zhang, G. X., and Rostami, A. (2004). Role of the IL-12/IL-23 system in the regulation of Tcell responses in central nervous system inflammatory demyelination. Crit. Rev. Immunol. 24, 111-128.
7. Hickman, S. J., Kapoor, R., Jones, S. J., Altmann, D. R., Plant, G. T., and Miller, D. H. (2003). Corticos-teroids do not prevent optic nerve atrophy following optic neuritis. J. Neurol. Neurosurg. Psychiatr. 74, 1139-1141.
8. Hussain, R. Z., Hopkins, S. C., Frohman, E. M., Eagar, T. N., Cravens, P. C., Greenberg, B. M., Vernino, S., and Stüve, O. (2009). Direct and consensual murine pupillary reflex metrics: establishing normative values. Auton. Neurosci. 151, 164-167.
9. Imler, T. J. Jr., and Petro, T. M. (2009). Decreased severity of experimental autoimmune encephalomyelitis during resveratrol administration is associated with increased IL-17+IL-10+ T cells, CD4(-) IFN-gamma+ cells, and decreased macrophage IL-6 expression. Int. Immunopharma-col. 9, 134-143.
10. Jacobs, L. D., Cookfair, D. L., Rudick, R. A., Herndon, R. M., Richert, J. R., Salazar, A. M., Fischer, J. S., Goodkin, D. E., Granger, C. V., Simon, J. H., Alam, J. J., Bartoszak, D. M., Bour- dette, D. M., Braiman, J., Brown- scheidle, C. M., Coats, M. E., Cohan, S. L., Dougherty, D. S., Kinkel, R. P., Mass, M. K., Munschauer, F. E. III, Priore, R. L., Pullicino, P. M., Scherokman, B. J., Weinstock- Guttman, B., Whitham, R. H., and The Multiple Sclerosis Collaborative Research Group. (1996). Intramus cular interferon beta-1a for disease progression in relapsing multiple sclerosis. Ann. Neurol. 39,285-294.
11. Johnson K P., Brooks, B. R., Cohen, J. A., Ford, C. C., Goldstein, J., Lisak, R. P., Myers, L. W., Panitch, H. S., Rose, J. W., Schiffer, R. B., Vollmer, T., Weiner, L. P., Wolinsky, J. S., and the Copolymer 1 Multiple Sclerosis Study Group. (1995). Copolymer 1 reduces relapse rate and improves disability in relapsing-remitting multiple sclerosis: results of a phase III multicenter, double-blind, placebo-controlled trial. Neurology 45, 1268-1276.
12. Langrish, C. L., Chen, Y., Blumen-schein, W. M., Mattson, J., Basham, B., Sedgwick, J. D., McClanahan, T., Kastelein, R. A., and Cua, D. J. (2005). IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201,233-240.
13. Lock C, Hermans, G., Pedotti, R., Bren-dolan, A., Schadt, E., Garren, H., Langer-Gould, A., Strober, S., Can-nella, B., Allard, J., Klonowski, P., Austin, A., Lad, N., Kaminski, N., Galli, S. J., Oksenberg, J. R., Raine, C. S., Heller, R., and Steinman, L. (2002). Gene microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat. Med. 8, 500-508.
14. Losseff, N. A., Webb, S. L., O'Riordan, J. I., Page, R., Wang, L., Barker, G. J., Tofts, P. S., McDonald, W. I., Miller, D. H., and Thompson, A. J. (1996a). Spinal cord atrophy and disability in multiple sclerosis: a new reproducible and sensitive MRI method with potential to monitor disease progression. Brain 119, 701-708.
15. Losseff, N. A., Wang, L., Lai, H. M., Yoo, D. S., Gawne-Cain, M. L., McDonald, W I., Miller, D. H., and Thompson, A. J. (1996b). Progressive cerebral atrophy in multiple sclerosis: a serial MRI study. Brain 119, 2009-2019.
16. Milne, J. C., Lambert, P. D., Schenk, S., Carney, D. P., Smith, J. J., Gagne, D. J., Jin, L., Boss, O., Perni, R. B., Vu, C. B., Bemis, J. E., Xie, R., Disch, J. S., Ng, P. Y., Nunes, J. J., Lynch, A. V., Yang, H., Galonek, H., Israelian, K., Choy, W., Iffland, A., Lavu, S., Medvedik, O., Sinclair, D. A., Olef-sky, J. M., Jirousek, M. R., Elliott, P. J., and Westphal, C. H. (2007). Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes. Nature 450, 712-716.
17. Noseworthy, J. H., Lucchinetti, C., Rodriguez, M., and Weinshenker, B. G. (2000). Multiple sclerosis. N. Engl. J. Med. 343, 938-952.
18. Parisi, V., Manni, G., Spadaro, M., Cola-cino, G., Restuccia, R., Marchi, S., Bucci, M. G., and Pierelli, F. (1999). Correlation between morphological and functional retinal impairment in multiple sclerosis patients. Invest. Ophthalmol. Vis. Sci. 40, 2520-2527.
19. Parry, A., Corkill, R., Blamire, A. M., Palace, J., Narayanan, S., Arnold, D., Styles, P., and Matthews, P. M. (2003). Beta-Interferon treatment does not always slow the progression of axonal injuryin multiple sclerosis. J. Neurol. 250,171-178.
20. Prusky G T., Alam, N. M., Beekman, S., and Douglas, R.M. (2004). Rapid quantification of adult and developing mouse spatial vision using a virtual optomotor system. Invest. Ophthalmol. Vis. Sci. 45, 4611-4616.
21. Quinn, T., Dutt, M., and Shindler, K. S. (2011). Optic neuritis and retinal ganglion cell loss in a chronic murine model of multiple sclerosis. Front. Neurol. 2:50. doi:10.3389/fneur.2011.00050
22. Shao H, Huang, Z., Sun, S. L., Kaplan, H. J., and Sun, D. (2004). Myelin/oligodendrocyte glycoprotein-specific T-cells induce severe optic neuritis in the C57BL/6 mouse. Invest. Ophthalmol. Vis. Sci. 45, 4060-4065.
23. Shindler, K. S., Chatterjee, D., Biswas, K., Goyal, A., Dutt, M., Nassrallah, M., Khan, R.S., and Das Sarma, J. (2011). Macrophage-mediated optic neuritis induced by retrograde axonal transport of spike gene recombi-nant mouse hepatitis virus. J. Neu-ropathol. Exp. Neurol. 70,470-480.
24. Shindler K S., Guan, Y., Ventura, E., Bennett, J., and Rostami, A. (2006). Retinal ganglion cell loss induced by acute optic neuritis in a relapsing model of multiple sclerosis. Mult. Scler. 12, 526-532.
25. Shindler, K. S., Revere, K., Dutt, M., Ying, G.-S., and Chung, D. C. (2012). In vivo detection of experimental optic neuritis by pupillometry. Exp. Eye Res. doi: 10.1016/j.exer.2012.04.005
26. Shindler, K. S., Ventura, E., Dutt, M., Elliott, P., Fitzgerald, D. C., and Rostami, A. (2010). Oral resveratrol reduces neuronal damage in a model of multiple sclerosis. J. Neuroophthalmol. 30, 328-339.
27. Shindler, K. S., Ventura, E., Rex, T. S., Elliott, P., and Rostami, A. (2007). SIRT1 activation confers neuroprotection in experimental optic neuritis. Invest. Ophthalmol. Vis. Sci. 48, 3602-3609.
28. Singh, N. P., Hegde, V L, Hof-seth, L. J., Nagarkatti, M., and Nagarkatti, P. (2007). Resveratrol (trans-3,5,4'-trihydroxystilbene) ameliorates experimental allergic encephalomyelitis, primarily via induction of apoptosis in T cells involving activation of aryl hydrocarbon receptor and estrogen receptor. Mol. Pharmacol. 72, 1508-1521.
29. Steel, D. H. W., and Waldock, A. (1998). Measurement of the retinal nerve fiber layer with scanning laser polarimetry in patients with previous demyelinating optic neuritis. J. Neurol. Neurosurg. Psychiatr. 64, 505-509.
30. Steinman, L. (2008). A rush to judgment on Th17. J. Exp. Med. 205, 1517-1522.
31. Stromnes, I. M., Cerretti, L. M., Liggitt, D., Harris, R. A., and Goverman, J. M. (2008). Differential regulation of central nervous system autoimmu-nity by T(H) 1 and T(H) 17 cells. Nat. Med. 14, 337-342.
32. Trapp, B. D., Peterson, J., Ransohoff, R. M., Rudick, R., Mork, S., and Bo, L. (1998). Axonal transection in the lesions of multiple sclerosis. N Engl. J. Med. 338, 278-285.
33. Trip, S. A., Schlottmann, P. G., Jones, S. J., Altmann, D. R., Garway-Heath, D. F., Thompson, A. J., Plant, G. T., and Miller, D. H. (2005). Retinal nerve fiber layer axonal loss and visual dysfunction in optic neuritis. Ann. Neurol. 58, 383-391.
34. Weiner, H. L., Hafler, D. A., Fallis, R. J., Johnson, D., Ault, K. A., and Hauser, S. L. (1984). T cell subsets in patients with multiple sclerosis. An overview. Ann. N Y. Acad. Sci. 436, 281-293.