Estrogen receptor-β ligand treatment after disease onset is neuroprotective in the multiple sclerosis model

Journal of Neuroscience Research

Volumn 91, Issue 7, 2013, Pages 901-908

  Wisdom, Amy J ^a   Cao, Yuan ^a   Itoh, Noriko ^a   Spence, Rory D ^a   Voskuhl, Rhonda R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

EAE; Estrogen; Multiple sclerosis; Myelin; Neuroprotection

Indexed keywords

DIARYLPROPIONITRILE; NEUROPROTECTIVE AGENT;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MICROGLIA; MOUSE; MULTIPLE SCLEROSIS; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; TREATMENT OUTCOME;

ANIMALS; AXONS; DEMYELINATING DISEASES; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; FREUND'S ADJUVANT; MICE; MICE, INBRED C57BL; MYELIN-OLIGODENDROCYTE GLYCOPROTEIN; NEUROPROTECTIVE AGENTS; NITRILES; PEPTIDE FRAGMENTS; PROPIONATES; RECEPTORS, ESTROGEN; SEVERITY OF ILLNESS INDEX;

EID: 84877922040     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23219     Document Type: Article

References (31)

1. Bebo BF, Fyfe-Johnson A, Adlard K, Beam AG, Vandenbark AA, Offner H. 2001. Low-dose estrogen therapy ameliorates experimental autoimmune encephalomyelitis in two different inbred mouse strains. J Immunol 166:2080-2089.
2. Brann DW, Dhandapani K, Wakade C, Mahesh VB, Khan MM. 2007. Neurotrophic and neuroprotective actions of estrogen: basic mechanisms and clinical implications. Steroids 72:381-405.
3. Cho JJ, Iannucci FA, Fraile M, Franco J, Alesius TN, Stefano GB. 2003. The role of the estrogen in neuroprotection: implications for neurodegenerative diseases. Neuroendocrinol Lett 24:141-147.
4. Croxford AL, Kurschus FC, Waisman A. 2011. Mouse models for multiple sclerosis: historical facts and future implications. Biochim Biophys Acta 1812:177-183.
5. Du S, Sandoval F, Trinh P, Voskuhl RR. 2010a. Additive effects of combination treatment with anti-inflammatory and neuroprotective agents in experimental autoimmune encephalomyelitis. J Neuroimmunol 219:64-74.
6. Du S, Sandoval F, Trinh P, Voskuhl RR. 2010b. Estrogen receptor-β ligand treatment modulates dendritic cells in the target organ during autoimmune demyelinating disease. Eur J Immunol 41:140-150.
7. Garcia-Segura LM, Azcoitia I, DonCarlos LL. 2001. Neuroprotection by estradiol. Prog Neurobiol 63:29-60.
8. Gold SM, Voskuhl RR. 2009. Estrogen and testosterone therapies in multiple sclerosis. Prog Brain Res 175:239-251.
9. Gold SM, Sasidhar MV, Morales LB, Du S, Sicotte NL, Tiwari-Woodruff SK, Voskuhl RR. 2009. Estrogen treatment decreases matrix metalloproteinase (MMP)-9 in autoimmune demyelinating disease through estrogen receptor alpha (ERalpha). Lab Invest 89:1076-1083.
10. Hartung H-P, Gonsette R, König N, Kwiecinski H, Guseo A, Morrissey SP, Krapf H, Zwingers T. 2002. Mitoxantrone in progressive multiple sclerosis: a placebo-controlled, double-blind, randomised, multicentre trial. Lancet 360:2018-2025.
11. Johnson KP. 2012. Glatiramer acetate for treatment of relapsing-remitting multiple sclerosis. Expert Rev Neurother 12:371-384.
12. Kim S, Liva SM, Dalal MA, Verity MA, Voskuhl RR. 1999. Estriol ameliorates autoimmune demyelinating disease: implications for multiple sclerosis. Neurology 52:1230-1238.
13. Kuiper GG, Carlsson B, Grandien K, Enmark E, Häggblad J, Nilsson S, Gustafsson JA. 1997. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138:863-870.
14. Liu H-B, Loo KK, Palaszynski K, Ashouri J, Lubahn DB, Voskuhl RR. 2003. Estrogen receptor alpha mediates estrogen's immune protection in autoimmune disease. J Immun 171:6936-6940.
15. Milo R, Kahana E. 2010. Multiple sclerosis: geoepidemiology, genetics and the environment. Autoimmun Rev 9:A387-A394.
16. Morales LBJ, Loo KK, Liu H-B, Peterson C, Tiwari-Woodruff S, Voskuhl RR. 2006. Treatment with an estrogen receptor alpha ligand is neuroprotective in experimental autoimmune encephalomyelitis. J Neurosci 26:6823-6833.
17. Offner H. 2004. Neuroimmunoprotective effects of estrogen and derivatives in experimental autoimmune encephalomyelitis: therapeutic implications for multiple sclerosis. J Neurosci Res 78:603-624.
18. Palaszynski KM, Liu H, Loo KK, Voskuhl RR. 2004. Estriol treatment ameliorates disease in males with experimental autoimmune encephalomyelitis: implications for multiple sclerosis. J Neuroimmunol 149:84-89.
19. Sicotte NL, Liva SM, Klutch R, Pfeiffer P, Bouvier S, Odesa S, Wu TCJ, Voskuhl RR. 2002. Treatment of multiple sclerosis with the pregnancy hormone estriol. Ann Neurol 52:421-428.
20. Soldan SS, Alvarez Retuerto AI, Sicotte NL, Voskuhl RR. 2003. Immune modulation in multiple sclerosis patients treated with the pregnancy hormone estriol. J Immunol 171:6267-6274.
21. Spence RD, Voskuhl RR. 2012. Neuroprotective effects of estrogens and androgens in CNS inflammation and neurodegeneration. Front Neuroendocrinol 33:105-115.
22. Spence RD, Hamby ME, Umeda E, Itoh N, Du S, Wisdom AJ, Cao Y, Bondar G, Lam J, Ao Y, Sandoval F, Suriany S, Sofroniew MV, Voskuhl RR. 2011. Neuroprotection mediated through estrogen receptor-alpha in astrocytes. Proc Natl Acad Sci U S A 108:8867-8872.
23. Subramanian S, Matejuk A, Zamora A, Vandenbark AA, Offner H. 2003. Oral feeding with ethinyl estradiol suppresses and treats experimental autoimmune encephalomyelitis in SJL mice and inhibits the recruitment of inflammatory cells into the central nervous system. J Immunol 170:1548-1555.
24. Suzuki S, Brown CM, Wise PM. 2009. Neuroprotective effects of estrogens following ischemic stroke. Front Neuroendocrinol 30:201-211.
25. Tiwari-Woodruff S, Voskuhl RR. 2009. Neuroprotective and anti-inflammatory effects of estrogen receptor ligand treatment in mice. J Neurol Sci 286:81-85.
26. Tiwari-Woodruff S, Morales LBJ, Lee R, Voskuhl RR. 2007. Differential neuroprotective and antiinflammatory effects of estrogen receptor (ER)alpha and ERbeta ligand treatment. Proc Natl Acad Sci U S A 104:14813-14818.
27. Ulzheimer JC, Meuth SG, Bittner S, Kleinschnitz C, Kieseier BC, Wiendl H. 2010. Therapeutic approaches to multiple sclerosis: an update on failed, interrupted, or inconclusive trials of immunomodulatory treatment strategies. BioDrugs Clin Immunother Biopharm Gene Ther 24:249-274.
28. Voskuhl RR, Peterson RS, Song B, Ao Y, Morales LBJ, Tiwari-Woodruff S, Sofroniew MV. 2009. Reactiv0f the CNS. J Neurosci 29:11511-11522.
29. Wolinsky JS, Narayana PA, Johnson KP. 2001. United States open-label glatiramer acetate extension trial for relapsing multiple sclerosis: MRI and clinical correlates. Multiple Sclerosis Study Group and the MRI Analysis Center. Multiple Sclerosis 7:33-41.
30. Wujek JR, Bjartmar C, Richer E, Ransohoff RM, Yu M, Tuohy VK, Trapp BD. 2002. Axon loss in the spinal cord determines permanent neurological disability in an animal model of multiple sclerosis. J Neuropathol Exp Neurol 61:23-32.
31. Ziehn MO, Avedisian AA, Dervin SM, Dell TJOA, Voskuhl RR. 2012. Estriol preserves synaptic transmission in the hippocampus during autoimmune demyelinating disease. Lab Invest 92:1234-1245.