Sex differences in autoimmune diseases

Hormones, Brain and Behavior Online

Volumn , Issue , 2009, Pages 2259-2291

  Voskuhl, R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Autoimmunity; Central nervous system; Cytokine; Estrogen; Experimental autoimmune encephalomyelitis; Immune system; Lupus; Multiple sclerosis; Pregnancy; Progesterone; Rheumatoid arthritis; Testosterone; X chromosome; Y chromosome

Indexed keywords

EID: 84884779470     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-008088783-8.00070-X     Document Type: Chapter

References (252)

1. Abramsky O. Pregnancy and multiple sclerosis. Annals of Neurology 1994, 36:S38-S41.
2. Aharoni R., Teitelbaum D., Sela M., Arnon R. Bystander suppression of experimental autoimmune encephalomyelitis by T cell lines and clones of the Th2 type induced by copolymer 1. Journal of Neuroimmunology 1998, 91:135-146.
3. Ahmed S.A., Penhale W.J. The influence of testosterone on the development of autoimmune thyroiditis in thymectomized and irradiated rats. Clinical and Experimental Immunology 1982, 48:367-374.
4. Al-Shammri S., Rawoot P., Azizieh F., AbuQoora A., Hanna M., Saminathan T.R., Raghupathy R. Th1/Th2 cytokine patterns and clinical profiles during and after pregnancy in women with multiple sclerosis. Journal of Neurological Science 2004, 222:21-27.
5. Alonso A., Jick S.S., Olek M.J., Ascherio A., Jick H., Hernan M.A. Recent use of oral contraceptives and the risk of multiple sclerosis. Archives of Neurology 2005, 62:1362-1365.
6. Ansar Ahmed S., Young P.R., Penhale W.J. Beneficial effect of testosterone in the treatment of chronic autoimmune thyroiditis in rats. Journal of Immunology 1986, 136:143-147.
7. Arnold A.P. Sex chromosomes and brain gender. Nature Reviews Neuroscience 2004, 5:701-708.
8. Arnold A.P., Burgoyne P.S. Are XX and XY brain cells intrinsically different?. Trends in Endocrinology and Metabolism 2004, 15:6-11.
9. Azcoitia I., Sierra A., Garcia-Segura L.M. Localization of estrogen receptor beta-immunoreactivity in astrocytes of the adult rat brain. Glia 1999, 26:260-267.
10. Bake S., Sohrabji F. 17beta-estradiol differentially regulates blood-brain barrier permeability in young and aging female rats. Endocrinology 2004, 145:5471-5475.
11. Bakshi R., Benedict R.H., Bermel R.A., Jacobs L. Regional brain atrophy is associated with physical disability in multiple sclerosis: Semiquantitative magnetic resonance imaging and relationship to clinical findings. Journal of Neuroimaging 2001, 11:129-136.
12. Bannerman P.G., Hahn A., Ramirez S., et al. Motor neuron pathology in experimental autoimmune encephalomyelitis: Studies in THY1-YFP transgenic mice. Brain 2005, 128:1877-1886.
13. Baulieu E., Schumacher M. Progesterone as a neuroactive neurosteroid, with special reference to the effect of progesterone on myelination. Steroids 2000, 65:605-612.
14. Bebo B.F., Adlard K., Schuster J.C., Unsicker L., Vandenbark A.A., Offner H. Gender differences in protection from EAE induced by oral tolerance with a peptide analogue of MBP-Ac1-11. Journal of Neuroscience Research 1999, 55:432-440.
15. Bebo B.F., Fyfe-Johnson A., Adlard K., Beam A.G., Vandenbark A.A., Offner H. Low-dose estrogen therapy ameliorates experimental autoimmune encephalomyelitis in two different inbred mouse strains. Journal of Immunology 2001, 166:2080-2089.
16. Bebo B.F., Schuster J.C., Vandenbark A.A., Offner H. Gender differences in experimental autoimmune encephalomyelitis develop during the induction of the immune response to encephalitogenic peptides. Journal of Neuroscience Research 1998, 52:420-426.
17. Bebo B.F., Schuster J.C., Vandenbark A.A., Offner H. Androgens alter the cytokine profile and reduce encephalitogenicity of myelin-reactive T cells. Journal of Immunology 1999, 162:35-40.
18. Bebo B.F., Vandenbark A.A., Offner H. Male SJL mice do not relapse after induction of EAE with PLP 139-151. Journal of Neuroscience Research 1996, 45:680-689.
19. Bebo B.F., Zelinka-Vincent E., Adamus G., Amundson D., Vandenbark A.A., Offner H. Gonadal hormones influence the immune response to PLP 139-151 and the clinical course of relapsing experimental autoimmune encephalomyelitis. Journal of Neuroimmunology 1998, 84:122-130.
20. Behl C., Skutella T., Lezoualc'h F., Post A., Widmann M., Newton C.J., Holsboer F. Neuroprotection against oxidative stress by estrogens: Structure-activity relationship. Molecular Pharmacology 1997, 51:535-541.
21. Behl C., Widmann M., Trapp T., Holsboer F. 17-beta estradiol protects neurons from oxidative stress-induced cell death in vitro. Biochemical and Biophysical Research Communications 1995, 216:473-482.
22. Bialek M., Zaremba P., Borowicz K.K., Czuczwar S.J. Neuroprotective role of testosterone in the nervous system. Polish Journal of Pharmacology 2004, 56:509-518.
23. Binder E.F., Schechtman K.B., Birge S.J., Williams D.B., Kohrt W.M. Effects of hormone replacement therapy on cognitive performance in elderly women. Maturitas 2001, 38:137-146.
24. Birk K., Ford C., Smeltzer S., Ryan D., Miller R., Rudick R.A. The clinical course of multiple sclerosis during pregnancy and the puerperium. Archives of Neurology 1990, 47:738-742.
25. Birk K., Smeltzer S.C., Rudick R. Pregnancy and multiple sclerosis. Seminars in Neurology 1988, 8:205-213.
26. Bo L., Vedeler C.A., Nyland H.I., Trapp B.D., Mork S.J. Subpial demyelination in the cerebral cortex of multiple sclerosis patients. Journal of Neuropathology and Experimental Neurology 2003, 62:723-732.
27. Brex P.A., Jenkins R., Fox N.C., Crum W.R., O'Riordan J.I., Plant G.T., Miller D.H. Detection of ventricular enlargement in patients at the earliest clinical stage of MS. Neurology 2000, 54:1689-1691.
28. Brinton R.D. Cellular and molecular mechanisms of estrogen regulation of memory function and neuroprotection against Alzheimer's disease: Recent insights and remaining challenges. Learning and Memory 2001, 8:121-133.
29. Brinton R.D. Investigative models for determining hormone therapy-induced outcomes in brain: Evidence in support of a healthy cell bias of estrogen action. Annals of the New York Academy of Sciences 2005, 1052:57-74.
30. Brown A., McFarlin D.E., Raine C.S. Chronologic neuropathology of relapsing experimental allergic encephalomyelitis in the mouse. Laboratory Investigation 1982, 46:171-185.
31. Bruce-Keller A.J., Keeling J.L., Keller J.N., Huang F.F., Camondola S., Mattson M.P. Antiinflammatory effects of estrogen on microglial activation. Endocrinology 2000, 141:3646-3656.
32. Burgoyne P.S., Lovell-Badge R., Rattigan A. Evidence that the testis determination pathway interacts with a non-dosage compensated, X-linked gene. International Journal of Developmental Biology 2001, 45:509-512.
33. Butterfield R.J., Blankenhorn E.P., Roper R.J., et al. Genetic analysis of disease subtypes and sexual dimorphisms in mouse experimental allergic encephalomyelitis (EAE): Relapsing/remitting and monophasic remitting/nonrelapsing EAE are immunogenetically distinct. Journal of Immunology 1999, 162:3096-3102.
34. Buyon J.P., Petri M.A., Kim M.Y., et al. The effect of combined estrogen and progesterone hormone replacement therapy on disease activity in systemic lupus erythematosus: A randomized trial. Annals of Internal Medicine 2005, 142:953-962.
35. Bynoe M.S., Grimaldi C.M., Diamond B. Estrogen up-regulates Bcl-2 and blocks tolerance induction of naive B cells. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:2703-2738.
36. Calabresi P.A., Stone L.A., Bash C.N., Frank J.A., McFarland H.F. Interferon beta results in immediate reduction of contrast-enhanced MRI lesions in multiple sclerosis patients followed by weekly MRI. Neurology 1997, 48:1446-1448.
37. Cantarella G., Risuglia N., Lombardo G., Lempereur L., Nicoletti F., Memo M., Bernardini R. Protective effects of estradiol on TRIAL-induced apoptosis in a human oligodendrocytic cell line: Evidence for multiple sites of interactions. Cell Death and Differentiation 2004, 11:503-511.
38. Capel B., Albrecht K.H., Washburn L.L., Eicher E.M. Migration of mesonephric cells into the mammalian gonad depends on Sry. Mechanisms of Development 1999, 84:127-131.
39. Carruth L.L., Reisert I., Arnold A.P. Sex chromosome genes directly affect brain sexual differentiation. Nature Neuroscience 2002, 5:933-934.
40. Caruso A., Di Giorgi Gerevini V., Castiglione M., et al. Testosterone amplifies excitotoxic damage of cultured oligodendrocytes. Journal of Neurochemistry 2004, 88:1179-1185.
41. Catalaa I., Fulton J.C., Zhang X., et al. MR imaging quantitation of gray matter involvement in multiple sclerosis and its correlation with disability measures and neurocognitive testing. American Journal of Neuroradiology 1999, 20:1613-1618.
42. Catalaa I., Grossman R.I., Kolson D.L., et al. Multiple sclerosis: Magnetization transfer histogram analysis of segmented normal-appearing white matter. Radiology 2000, 216:351-355.
43. Cerghet M., SkoffR.P., Bessert D., Zhang Z., Mullins C., Ghandour M.S. Proliferation and death of oligodendrocytes and myelin proteins are differentially regulated in male and female rodents. Journal of Neuroscience 2006, 26:1439-1447.
44. Cherrier M.M., Asthana S., Plymate S., et al. Testosterone supplementation improves spatial and verbal memory in healthy older men. Neurology 2001, 57:80-88.
45. Cherrier M.M., Craft S., Matsumoto A.H. Cognitive changes associated with supplementation of testosterone or dihydrotestosterone in mildly hypogonadal men: A preliminary report. Journal of Andrology 2003, 24:568-576.
46. Cherrier M.M., Matsumoto A.M., Amory J.K., et al. The role of aromatization in testosterone supplementation: Effects on cognition in older men. Neurology 2005, 64:290-296.
47. Coles A.J., Cox A., Le Page E., et al. The window of therapeutic opportunity in multiple sclerosis: Evidence from monoclonal antibody therapy. Journal of Neurology 2006, 253:98-108.
48. Confavreux C., Hutchinson M., Hours M.M., Cortinovis-Tourniaire P., Moreau T. Rate of pregnancy-related relapse in multiple sclerosis. Pregnancy in multiple sclerosis group. New England Journal of Medicine 1998, 339:285-291.
49. Confavreux C., Vukusic S., Adeleine P. Early clinical predictors and progression of irreversible disability in multiple sclerosis: An amnesic process. Brain 2003, 126:770-782.
50. Costenbader K.H., Feskanich D., Stampfer M.J., Karlson E.W. Reproductive and menopausal factors and risk of systemic lupus erythematosus in women. Arthritis and Rheumatism 2007, 56:1251-1262.
51. Craig A., Ling Luo N., Beardsley D.J., Wingate-Pearse N., Walker D.W., Hohimer A.R., Back S.A. Quantitative analysis of perinatal rodent oligodendrocyte lineage progression and its correlation with human. Experimental Neurology 2003, 181:231-240.
52. Cua D.J., Coffman R.L., Stohlman S.A. Exposure to T helper 2 cytokines in vivo before encounter with antigen selects for T helper subsets via alterations in antigen-presenting cell function. Journal of Immunology 1996, 157:2830-2836.
53. Cua D.J., Hinton D.R., Stohlman S.A. Self-antigen-induced Th2 responses in experimental allergic encephalomyelitis (EAE)-resistant mice. Th2-mediated suppression of autoimmune disease. Journal of Immunology 1995, 155:4052-4059.
54. Da Silva J.A., Hall G.M. The effects of gender and sex hormones on outcome in rheumatoid arthritis. Baillieres Clinical Rheumatology 1992, 6:196-219.
55. Da Silva J.A., Spector T.D. The role of pregnancy in the course and aetiology of rheumatoid arthritis. Clinical Rheumatology 1992, 11:189-194.
56. Dalal M., Kim S., Voskuhl R.R. Testosterone therapy ameliorates experimental autoimmune encephalomyelitis and induces a T helper 2 bias in the autoantigen-specific T lymphocyte response. Journal of Immunology 1997, 159:3-6.
57. Damek D.M., Shuster E.A. Pregnancy and multiple sclerosis. Mayo Clinic Proceedings 1997, 72:977-989.
58. De Stefano N., Narayanan S., Matthews P.M., Francis G.S., Antel J.P., Arnold D.L. In vivo evidence for axonal dysfunction remote from focal cerebral demyelination of the type seen in multiple sclerosis. Brain 1999, 122:1933-1939.
59. De Vries G.J. Minireview: Sex differences in adult and developing brains: Compensation, compensation, compensation. Endocrinology 2004, 145:1063-1068.
60. De Vries G.J., Rissman E.F., Simerly R.B., et al. A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits. Journal of Neuroscience 2002, 22:9005-9014.
61. Deboy C.A., Zhang J., Dike S., et al. High resolution diffusion tensor imaging of axonal damage in focal inflammatory and demyelinating lesions in rat spinal cord. Brain 2007, 130:2199-2210.
62. Doran M.F., Pond G.R., Crowson C.S., O'Fallon M., Gabriel S.E. Trends in incidence and mortality in rheumatoid arthritis in Rochester, Minnesota, over a forty-year period. Arthritis and Rheumatism 2002, 46:625-631.
63. Drew P.D., Chavis J.A. Female sex steroids: Effects upon microglial cell activation. Journal of Neuroimmunology 2000, 111:77-85.
64. Dubal D.B., Zhu H., Yu J., et al. Estrogen receptor alpha, not beta, is a critical link in estradiol-mediated protection against brain injury. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:1952-1957.
65. Duda P.W., Schmied M.C., Cook S.L., Krieger J.I., Hafler D.A. Glatiramer acetate (copaxone) induces degenerate, Th2-polarized immune responses in patients with multiple sclerosis. Journal of Clinical Investigation 2000, 105:967-976.
66. Dudley D.J., Chen C.L., Mitchell M.D., Daynes R.A., Araneo B.A. Adaptive immune responses during murine pregnancy: Pregnancy-induced regulation of lymphokine production by activated T lymphocytes. American Journal of Obstetrics and Gynecology 1993, 168:1155-1163.
67. Duquette P., Pleines J., Girard M., Charest L., Senecal-Quevillon M., Masse C. The increased susceptibility of women to multiple sclerosis. Canadian Journal of Neurological Sciences 1992, 19:466-471.
68. Elenkov I.J., Wilder R.L., Bakalov V.K., et al. IL-12, TNF-alpha, and hormonal changes during late pregnancy and early postpartum: Implications for autoimmune disease activity during these times. Journal of Clinical Endocrinology and Metabolism 2001, 86:4933-4938.
69. Elloso M.M., Phiel K., Henderson R.A., Harris H.A., Adelman S.J. Suppression of experimental autoimmune encephalomyelitis using estrogen receptor-selective ligands. Journal of Endocrinology 2005, 185:243-252.
70. Enmark E., Gustafsson J.A. Oestrogen receptors - an overview. Jounal of Internal Medicine 1999, 246:133-138.
71. Erlandsson M.C., Ohlsson C., Gustafsson J.A., Carlsten H. Role of oestrogen receptors alpha and beta in immune organ development and in oestrogen-mediated effects on thymus. Immunology 2001, 103:17-25.
72. Fabris N., Piantanelli L., Muzzioli M. Differential effect of pregnancy or gestagens on humoral and cell-mediated immunity. Clinical and Experimental Immunology 1977, 28:306-314.
73. Filippi M., Bozzali M., Rovaris M., et al. Evidence for widespread axonal damage at the earliest clinical stage of multiple sclerosis. Brain 2003, 126:433-437.
74. Filippi M., Iannucci G., Cercignani M., Assunta R.M., Pratesi A., Comi G. A quantitative study of water diffusion in multiple sclerosis lesions and normal-appearing white matter using echo-planar imaging. Archives of Neurology 2000, 57:1017-1021.
75. Filippi M., Inglese M., Rovaris M., et al. Magnetization transfer imaging to monitor the evolution of MS: A 1-year follow-up study [in process citation. Neurology 2000, 55:940-946.
76. Fitzpatrick F., Lepault F., Homo-Delarche F., Bach J.F., Dardenne M. Influence of castration, alone or combined with thymectomy, on the development of diabetes in the nonobese diabetic mouse. Endocrinology 1991, 129:1382-1390.
77. Formby B. Immunologic response in pregnancy. Its role in endocrine disorders of pregnancy and influence on the course of maternal autoimmune diseases. Endocrinology and Metabolism Clinics of North America 1995, 24:187-205.
78. Foster S.C., Daniels C., Bourdette D.N., Bebo B.F. Dysregulation of the hypothalamic-pituitary-gonadal axis in experimental autoimmune encephalomyelitis and multiple sclerosis. Journal of Neuroimmunology 2003, 140:78-87.
79. Fox H.S. Androgen treatment prevents diabetes in nonobese diabetic mice. Journal of Experimental Medicine 1992, 175:1409-1412.
80. Gago N., Akwa Y., Sananes N., Guennoun R., Baulieu E.E., El-Etr M., Schumacher M. Progesterone and the oligodendroglial lineage: Stage-dependent biosynthesis and metabolism. Glia 2001, 36:295-308.
81. Garcia-Segura L.M., Azcoitia I., DonCarlos L.L. Neuroprotection by estradiol. Progress in Neurobiology 2001, 63:29-60.
82. Garcia-Segura L.M., Naftolin F., Hutchison J.B., Azcoitia I., Chowen J.A. Role of astroglia in estrogen regulation of synaptic plasticity and brain repair. Journal of Neurobiology 1999, 40:574-584.
83. Garidou L., Laffont S., Douin-Echinard V., Coureau C., Krust A., Chambon P., Guery J.C. Estrogen receptor alpha signaling in inflammatory leukocytes is dispensable for 17beta-estradiol-mediated inhibition of experimental autoimmune encephalomyelitis. Journal of Immunology 2004, 173:2435-2442.
84. Gasperini C., Horsfield M.A., Thorpe J.W., et al. Macroscopic and microscopic assessments of disease burden by MRI in multiple sclerosis: Relationship to clinical parameters. Journal of Magnetic Resonance Imaging 1996, 6:580-584.
85. Gatewood J.D., Wills A., Shetty S., Xu J., Arnold A.P., Burgoyne P.S., Rissman E.F. Sex chromosome complement and gonadal sex influence aggressive and parental behaviors in mice. Journal of Neuroscience 2006, 26:2335-2342.
86. Ge Y., Grossman R.I., Udupa J.K., et al. Glatiramer acetate (Copaxone) treatment in relapsing-remitting MS: Quantitative MR assessment. Neurology 2000, 54:813-817.
87. Ge Y., Grossman R.I., Udupa J.K., Wei L., Mannon L.J., Polansky M., Kolson D.L. Brain atrophy in relapsing-remitting multiple sclerosis and secondary progressive multiple sclerosis: Longitudinal quantitative analysis. Radiology 2000, 214:665-670.
88. Ghoumari A.M., Ibanez C., El-Etr M., et al. Progesterone and its metabolites increase myelin basic protein expression in organotypic slice cultures of rat cerebellum. Journal of Neurochemistry 2003, 86:848-859.
89. Gilmore W., Arias M., Stroud N., Stek A., McCarthy K.A., Correale J. Preliminary studies of cytokine secretion patterns associated with pregnancy in MS patients. Journal of Neurological Science 2004, 224:69-76.
90. Gioiosa L., Chen X., Watkins R., Klanfer N., Bryant C.D., Evans C.J., Arnold A.P. Sex chromosome complement affects nociception in tests of acute and chronic exposure to morphine in mice. Hormones and Behavior 2008, 53:124-130.
91. Goodman Y., Bruce A.J., Cheng B., Mattson M.P. Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury, and amyloid beta-peptide toxicity in hippocampal neurons. Journal of Neurochemistry 1996, 66:1836-1844.
92. Gray A., Berlin J.A., McKinlay J.B., Longcope C. An examination of research design effects on the association of testosterone and male aging: Results of a meta-analysis. Journal of Clinical Epidemiology 1991, 44:671-684.
93. Gregg C., Shikar V., Larsen P., Mak G., Chojnacki A., Yong V.W., Weiss S. White matter plasticity and enhanced remyelination in the maternal CNS. Journal of Neuroscience 2007, 27:1812-1823.
94. Grimaldi C.M., Cleary J., Dagtas A.S., Moussai D., Diamond B. Estrogen alters thresholds for B cell apoptosis and activation. Journal of Clinical Investigation 2002, 109:1625-1633.
95. Grimaldi C.M., Michael D.J., Diamond B. Cutting edge: Expansion and activation of a population of autoreactive marginal zone B cells in a model of estrogen-induced lupus. Journal of Immunology 2001, 167:1886-1890.
96. Hall G.M., Daniels M., Huskisson E.C., Spector T.D. A randomised controlled trial of the effect of hormone replacement therapy on disease activity in postmenopausal rheumatoid arthritis. Annals of the Rheumatic Diseases 1994, 53:112-116.
97. Harbuz M.S., Perveen-Gill Z., Lightman S.L., Jessop D.S. A protective role for testosterone in adjuvant-induced arthritis. British Journal of Rheumatology 1995, 34:1117-1122.
98. Harms C., Lautenschlager M., Bergk A., et al. Differential mechanisms of neuroprotection by 17 beta-estradiol in apoptotic versus necrotic neurodegeneration. Journal of Neuroscience 2001, 21:2600-2609.
99. Harrington W.R., Sheng S., Barnett D.H., Petz L.N., Katzenellenbogen J.A., Katzenellenbogen B.S. Activities of estrogen receptor alpha- and beta-selective ligands at diverse estrogen responsive gene sites mediating transactivation or transrepression. Molecular and Cellular Endocrinology 2003, 206:13-22.
100. Hawkins S.A., McDonnell G.V. Benign multiple sclerosis? Clinical course, long term follow up, and assessment of prognostic factors. Journal of Neurology, Neurosurgery and Psychiatry 1999, 67:148-152.
101. Hernan M.A., Hohol M.J., Olek M.J., Spiegelman D., Ascherio A. Oral contraceptives and the incidence of multiple sclerosis. Neurology 2000, 55:848-854.
102. Hill J.A., Polgar K., Anderson D.J. T-helper 1-type immunity to trophoblast in women with recurrent spontaneous abortion [see comments]. Journal of the American Medical Association 1995, 273:1933-1936.
103. Hoffman G.E., Le W.W., Murphy A.Z., Koski C.L. Divergent effects of ovarian steroids on neuronal survival during experimental allergic encephalitis in Lewis rats. Experimental Neurology 2001, 171:272-284.
104. Igarashi H., Kouro T., Yokota T., Comp P.C., Kincade P.W. Age and stage dependency of estrogen receptor expression by lymphocyte precursors. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:15131-15136.
105. Ito A., Bebo B.F., Matejuk A., Zamora A., Silverman M., Fyfe-Johnson A., Offner H. Estrogen treatment down-regulates TNF-alpha production and reduces the severity of experimental autoimmune encephalomyelitis in cytokine knockout mice. Journal of Immunology 2001, 167:542-552.
106. Janowsky J.S., Chavez B., Orwoll E. Sex steroids modify working memory. Journal of Cognitive Neuroscience 2000, 12:407-414.
107. Jansson L., Holmdahl R. Oestrogen induced suppression of collagen arthritis. IV: Progesterone alone does not affect the course of arthritis but enhances the oestrogen-mediated therapeutic effect. Journal of Reproductive Immunology 1989, 15:141-150.
108. Jansson L., Holmdahl R. Oestrogen-induced suppression of collagen arthritis; 17 beta-oestradiol is therapeutically active in normal and castrated F1 hybrid mice of both sexes. Clinical and Experimental Immunology 1992, 89:446-451.
109. Jansson L., Holmdahl R. Estrogen-mediated immunosuppression in autoimmune diseases. Inflammation Research 1998, 47:290-301.
110. Jansson L., Holmdahl R. Enhancement of collagen-induced arthritis in female mice by estrogen receptor blockage. Arthritis and Rheumatism 2001, 44:2168-2175.
111. Jansson L., Mattsson A., Mattsson R., Holmdahl R. Estrogen induced suppression of collagen arthritis. V: Physiological level of estrogen in DBA/1 mice is therapeutic on established arthritis, suppresses anti-type II collagen T-cell dependent immunity and stimulates polyclonal B-cell activity. Journal of Autoimmunity 1990, 3:257-270.
112. Jansson L., Olsson T., Holmdahl R. Estrogen induces a potent suppression of experimental autoimmune encephalomyelitis and collagen-induced arthritis in mice. Journal of Neuroimmunology 1994, 53:203-207.
113. Jiang P.P., Frederick K., Hansen T.H., Miller R.D. Localization of the mouse gene releasing sex-limited expression of Slp. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:913-917.
114. Jover T., Tanaka H., Calderone A., Oguro K., Bennett M.V., Etgen A.M., Zukin R.S. Estrogen protects against global ischemia-induced neuronal death and prevents activation of apoptotic signaling cascades in the hippocampal CA1. Journal of Neuroscience 2002, 22:2115-2124.
115. Jungers P., Dougados M., Pélissier C., Kuttenn F., Tron F., Lesavre P., Bach J.F. Lupus nephropathy and pregnancy. Report of 104 cases in 36 patients. Archives of Internal Medicine 1982, 142:771-776.
116. Kanik K.S., Chrousos G.P., Schumacher H.R., Crane M.L., Yarboro C.H., Wilder R.L. Adrenocorticotropin, glucocorticoid, and androgen secretion in patients with new onset synovitis/rheumatoid arthritis: Relations with indices of inflammation. Journal of Clinical Endocrinology and Metabolism 2000, 85:1461-1466.
117. Kantarci O.H., Goris A., Hebrink D.D., et al. IFNG polymorphisms are associated with gender differences in susceptibility to multiple sclerosis. Genes and Immunity 2005, 6:153-161.
118. Kim J.H., Budde M.D., Liang H.F., Klein R.S., Russell J.H., Cross A.H., Song S.K. Detecting axon damage in spinal cord from a mouse model of multiple sclerosis. Neurobiology of Disease 2006, 21:626-632.
119. Kim S., Liva S.M., Dalal M.A., Verity M.A., Voskuhl R.R. Estriol ameliorates autoimmune demyelinating disease: Implications for multiple sclerosis. Neurology 1999, 52:1230-1238.
120. Kim S., Voskuhl R.R. Decreased IL-12 production underlies the decreased ability of male lymph node cells to induce experimental autoimmune encephalomyelitis. Journal of Immunology 1999, 162:5561-5568.
121. Kozovska M.E., Hong J., Zang Y.C., Li S., Rivera V.M., Killian J.M., Zhang J.Z. Interferon beta induces T-helper 2 immune deviation in MS. Neurology 1999, 53:1692-1697.
122. Krishnan L., Guilbert L.J., Wegmann T.G., Belosevic M., Mosmann T.R. T helper 1 response against Leishmania major in pregnant C57BL/6 mice increases implantation failure and fetal resorptions. Correlation with increased IFN-gamma and TNF and reduced IL-10 production by placental cells. Journal of Immunology 1996, 156:653-662.
123. Kuiper G.G., Carlsson B., Grandien K., Enmark E., Haggblad J., Nilsson S., Gustafsson J.A. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 1997, 138:863-870.
124. Kuiper G.G., Shughrue P.J., Merchenthaler I., Gustafsson J.A. The estrogen receptor beta subtype: A novel mediator of estrogen action in neuroendocrine systems. Frontiers in Neuroendocrinology 1998, 19:253-286.
125. Langer-Gould A., Garren H., Slansky A., Ruiz P.J., Steinman L. Late pregnancy suppresses relapses in experimental autoimmune encephalomyelitis: Evidence for a suppressive pregnancy-related serum factor. Journal of Immunology 2002, 169:1084-1091.
126. Leranth C., Roth R.H., Elswoth J.D., Naftolin F., Horvath T.L., Redmond D.E. Estrogen is essential for maintaining nigrostriatal dopamine neurons in primates: Implications for Parkinson's disease and memory. Journal of Neuroscience 2000, 20:8604-8609.
127. Li D.K., Paty D.W. Magnetic resonance imaging results of the PRISMS trial: A randomized, double-blind, placebo-controlled study of interferon-beta1a in relapsing-remitting multiple sclerosis. Prevention of relapses and disability by interferon-beta1a subcutaneously in multiple sclerosis. Annals of Neurology 1999, 46:197-206.
128. Lin H., Mosmann T.R., Guilbert L., Tuntipopipat S., Wegmann T.G. Synthesis of T helper 2-type cytokines at the maternal-fetal interface. Journal of Immunology 1993, 151:4562-4573.
129. Liu H.B., Loo K.K., Palaszynski K., Ashouri J., Lubahn D.B., Voskuhl R.R. Estrogen receptor alpha mediates estrogen's immune protection in autoimmune disease. Journal of Immunology 2003, 171:6936-6940.
130. Liu H.Y., Buenafe A.C., Matejuk A., et al. Estrogen inhibition of EAE involves effects on dendritic cell function. Journal of Neuroscience Research 2002, 70:238-248.
131. Liva S.M., Voskuhl R.R. Testosterone acts directly on CD4+ T-lymphocytes to increase IL10 production. Journal of Immunology 2001, 167:2060-2067.
132. LosseffN.A., Wang L., Lai H.M., et al. Progressive cerebral atrophy in multiple sclerosis. A serial MRI study. Brain 1996, 119:2009-2019.
133. Mackenzie-Graham A., Tinsley M.R., Shah K.P., et al. Cerebellar cortical atrophy in experimental autoimmune encephalomyelitis. NeuroImage 2006, 32:1016-1023.
134. Mahadevaiah S.K., Odorisio T., Elliott D.J., et al. Mouse homologues of the human AZF candidate gene RBM are expressed in spermatogonia and spermatids, and map to a Y chromosome deletion interval associated with a high incidence of sperm abnormalities. Human Molecular Genetics 1998, 7:715-727.
135. Manson J.E., Allison M.A., Rossouw J.E., et al. Estrogen therapy and coronary-artery calcification. New England Journal of Medicine 2007, 356:2591-2602.
136. Markham J.A., Jurgens H.A., Auger C.J., De Vries G.J., Arnold A.P., Juraska J.M. Sex differences in mouse cortical thickness are independent of the complement of sex chromosomes. Neuroscience 2003, 116:71-75.
137. Martin R., McFarland H.F., McFarlin D.E. Immunological aspects of demyelinating diseases. Annual Review of Immunology 1992, 10:153-187.
138. Marzi M., Vigano A., Trabattoni D., Villa M.L., Salvaggio A., Clerici E., Clerici M. Characterization of type 1 and type 2 cytokine production profile in physiologic and pathologic human pregnancy. Clinical and Experimental Immunology 1996, 106:127-133.
139. Matejuk A., Adlard K., Zamora A., Silverman M., Vandenbark A.A., Offner H. 17Beta-estradiol inhibits cytokine, chemokine, and chemokine receptor mRNA expression in the central nervous system of female mice with experimental autoimmune encephalomyelitis. Journal of Neuroscience Research 2001, 65:529-542.
140. Matejuk A., Bakke A.C., Hopke C., Dwyer J., Vandenbark A.A., Offner H. Estrogen treatment induces a novel population of regulatory cells, which suppresses experimental autoimmune encephalomyelitis. Journal of Neuroscience Research 2004, 77:119-126.
141. Matsuda J., Vanier M.T., Saito Y., Suzuki K. Dramatic phenotypic improvement during pregnancy in a genetic leukodystrophy: Estrogen appears to be a critical factor. Human Molecular Genetics 2001, 10:2709-2715.
142. Melez K.A., Boegel W.A., Steinberg A.D. Therapeutic studies in New Zealand mice. VII. Successful androgen treatment of NZB/NZW F1 females of different ages. Arthritis and Rheumatism 1980, 23:41-47.
143. Mellor A.L., Munn D.H. IDO expression by dendritic cells: Tolerance and tryptophan catabolism. Nature Reviews Immunology 2004, 4:762-774.
144. Miller D.H., Barkhof F., Frank J.A., Parker G.J., Thompson A.J. Measurement of atrophy in multiple sclerosis: Pathological basis, methodological aspects and clinical relevance. Brain 2002, 125:1676-1695.
145. Mokhtarian F., McFarlin D.E., Raine C.S. Adoptive transfer of myelin basic protein-sensitized T cells produces chronic relapsing demyelinating disease in mice. Nature 1984, 309:356-358.
146. Morales L.B., Loo K.K., Liu H.B., Peterson C., Tiwari-WoodruffS., Voskuhl R.R. Treatment with an estrogen receptor alpha ligand is neuroprotective in experimental autoimmune encephalomyelitis. Journal of Neuroscience 2006, 26:6823-6833.
147. Morley J.E., Kaiser F.E., Perry H.M., et al. Longitudinal changes in testosterone, luteinizing hormone, and follicle-stimulating hormone in healthy older men. Metabolism: Clinical and Experimental 1997, 46:410-413.
148. Mulnard R.A., Corrada M.M., Kawas C.H. Estrogen replacement therapy, Alzheimer's disease, and mild cognitive impairment. Current Neurology and Neuroscience Reports 2004, 4:368-373.
149. Mulnard R.A., Cotman C.W., Kawas C., et al. Estrogen replacement therapy for treatment of mild to moderate Alzheimer disease: A randomized controlled trial. Alzheimer's Disease Cooperative Study [see comments]. Journal of the American Medical Association 2000, 283:1007-1015.
150. Munn D.H., Zhou M., Attwood J.T., et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 1998, 281:1191-1193.
151. Murphy D.D., Cole N.B., Greenberger V., Segal M. Estradiol increases dendritic spine density by reducing GABA neurotransmission in hippocampal neurons. Journal of Neuroscience 1998, 18:2550-2559.
152. Nankin H.R., Calkins J.H. Decreased bioavailable testosterone in aging normal and impotent men. Journal of Clinical Endocrinology and Metabolism 1986, 63:1418-1420.
153. Narayanan S., Fu L., Pioro E., et al. Imaging of axonal damage in multiple sclerosis: Spatial distribution of magnetic resonance imaging lesions. Annals of Neurology 1997, 41:385-391.
154. Nelson J.L., Hughes K.A., Smith A.G., Nisperos B.B., Branchaud A.M., Hansen J.A. Remission of rheumatoid arthritis during pregnancy and maternal-fetal class II alloantigen disparity. American Journal of Reproductive Immunology 1992, 28:226-227.
155. Nilsson S., Makela S., Treuter E., et al. Mechanisms of estrogen action. Physiological Reviews 2001, 81:1535-1565.
156. Okuda Y., Okuda M., Bernard C.C. Gender does not influence the susceptibility of C57BL/6 mice to develop chronic experimental autoimmune encephalomyelitis induced by myelin oligodendrocyte glycoprotein. Immunology Letters 2002, 81:25-29.
157. Orton S.M., Herrera B.M., Yee I.M., Valdar W., Ramagopalan S.V., Sadovnick A.D., Ebers G.C. Sex ratio of multiple sclerosis in Canada: A longitudinal study. Lancet Neurology 2006, 5:932-936.
158. Paech K., Webb P., Kuiper G.G., Nilsson S., Gustafsson J., Kushner P.J., Scanlan T.S. Differential ligand activation of estrogen receptors ERalpha and ERbeta at AP1 sites. Science 1997, 277:1508-1510.
159. Palaszynski K.M., Liu H., Loo K.K., Voskuhl R.R. Estriol treatment ameliorates disease in males with experimental autoimmune encephalomyelitis: Implications for multiple sclerosis. Journal of Neuroimmunology 2004, 149:84-89.
160. Palaszynski K.M., Loo K.K., Ashouri J.F., Liu H., Voskuhl R.R. Androgens are protective in experimental autoimmune encephalomyelitis: Implications for multiple sclerosis. Journal of Neuroimmunology 2004, 146:144-152.
161. Palaszynski K.M., Smith D.L., Kamrava S., Burgoyne P.S., Arnold A.P., Voskuhl R.R. A Yin-Yang effect between sex chromosome complement and sex hormones on the immune response. Endocrinology 2005, 146:3280-3285.
162. Papenfuss T.L., Rogers C.J., Gienapp I., et al. Sex differences in experimental autoimmune encephalomyelitis in multiple murine strains. Journal of Neuroimmunology 2004, 150:59-69.
163. Peterson J.W., Bo L., Mork S., Chang A., Trapp B.D. Transected neurites, apoptotic neurons, and reduced inflammation in cortical multiple sclerosis lesions. Annals of Neurology 2001, 50:389-400.
164. Petri M., Kim M.Y., Kalunian K.C., et al. Combined oral contraceptives in women with systemic lupus erythematosus. New England Journal of Medicine 2005, 353:2550-2558.
165. Pisitkun P., Deane J.A., Difilippantonio M.J., Tarasenko T., Satterthwaite A.B., Bolland S. Autoreactive B cell responses to RNA-related antigens due to TLR7 gene duplication. Science 2006, 312:1669-1672.
166. Platania P., Laureanti F., Bellomo M., Giuffrida R., Giuffrida-Stella A.M., Catania M.V., Sortino M.A. Differential expression of estrogen receptors alpha and beta in the spinal cord during postnatal development: Localization in glial cells. Neuroendocrinology 2003, 77:334-340.
167. Polanczyk M., Zamora A., Subramanian S., et al. The protective effect of 17beta-estradiol on experimental autoimmune encephalomyelitis is mediated through estrogen receptor-alpha. American Journal of Pathology 2003, 163:1599-1605.
168. Polanczyk M.J., Carson B.D., Subramanian S., Afentoulis M., Vandenbark A.A., Ziegler S.F., Offner H. Cutting edge: Estrogen drives expansion of the CD4+CD25+ regulatory T cell compartment. Journal of Immunology 2004, 173:2227-2230.
169. Polman C.H., O'Connor P.W., Havrdova E., et al. A randomized, placebo-controlled trial of natalizumab for relapsing multiple sclerosis. New England Journal of Medicine 2006, 354:899-910.
170. Pozzilli C., Tomassini V., Marinelli F., Paolillo A., Gasperini C., Bastianello S. 'Gender gap' in multiple sclerosis: Magnetic resonance imaging evidence. European Journal of Neurology 2003, 10:95-97.
171. Quinn J.J., Hitchcott P.K., Umeda E.A., Arnold A.P., Taylor J.R. Sex chromosome complement regulates habit formation. Nature Neuroscience 2007, 10:1398-1400.
172. Raghupathy R. Th1-type immunity is incompatible with successful pregnancy [see comments]. Immunology Today 1997, 18:478-482.
173. Raine C.S., Barnett L.B., Brown A., Behar T., McFarlin D.E. Neuropathology of experimental allergic encephalomyelitis in inbred strains of mice. Laboratory Investigation 1980, 43:150-157.
174. Raine C.S., Cannella B., Hauser S.L., Genain C.P. Demyelination in primate autoimmune encephalomyelitis and acute multiple sclerosis lesions: A case for antigen-specific antibody mediation. Annals of Neurology 1999, 46:144-160.
175. Rau S.W., Dubal D.B., Bottner M., Gerhold L.M., Wise P.M. Estradiol attenuates programmed cell death after stroke-like injury. Journal of Neuroscience 2003, 23:11420-11426.
176. Rice G.P., Filippi M., Comi G. Cladribine and progressive MS: Clinical and MRI outcomes of a multicenter controlled trial. Cladribine MRI Study Group. Neurology 2000, 54:1145-1155.
177. Riskind P.N., Massacesi L., Doolittle T.H., Hauser S.L. The role of prolactin in autoimmune demyelination: Suppression of experimental allergic encephalomyelitis by bromocriptine. Annals of Neurology 1991, 29:542-547.
178. Roubinian J.R., Talal N., Greenspan J.S., Goodman J.R., Siiteri P.K. Effect of castration and sex hormone treatment on survival, anti-nucleic acid antibodies, and glomerulonephritis in NZB/NZW F1 mice. Journal of Experimental Medicine 1978, 147:1568-1583.
179. Rudick C.N., Woolley C.S. Estrogen regulates functional inhibition of hippocampal CA1 pyramidal cells in the adult female rat. Journal of Neuroscience 2001, 21:6532-6543.
180. Rudick R.A., Fisher E., Lee J.C., Simon J., Jacobs L. Use of the brain parenchymal fraction to measure whole brain atrophy in relapsing-remitting MS. Multiple Sclerosis Collaborative Research Group. Neurology 1999, 53:1698-1704.
181. Rudick R.A., RansohoffR.M., Lee J.C., Peppler R., Yu M., Mathisen P.M., Tuohy V.K. In vivo effects of interferon beta-1a on immunosuppressive cytokines in multiple sclerosis. Neurology 1998, 50:1294-1300. [published erratum appears in Neurology 1998 Jul;51(1):332].
182. Runmarker B., Andersen O. Pregnancy is associated with a lower risk of onset and a better prognosis in multiple sclerosis [see comments]. Brain 1995, 118:253-261.
183. Runmarker B., Andersson C., Odén A., Andersen O. Prediction of outcome in multiple sclerosis based on multivariate models. Journal of Neurology 1994, 241:597-604.
184. Sacks G.P., Clover L.M., Bainbridge D.R., Redman C.W., Sargent I.L. Flow cytometric measurement of intracellular Th1 and Th2 cytokine production by human villous and extravillous cytotrophoblast. Placenta 2001, 22:550-559.
185. Sanchez-Guerrero J., Uribe A.G., Jimenez-Santana L., Mestanza-Peralta M., Lara-Reyes P., Seuc A.H., Cravioto M.D. A trial of contraceptive methods in women with systemic lupus erythematosus. New England Journal of Medicine 2005, 353:2539-2549.
186. Sandstrom N.J., Williams C.L. Memory retention is modulated by acute estradiol and progesterone replacement. Behavioral Neuroscience 2001, 115:384-393.
187. Santos A.C., Narayanan S., De Stefano N., et al. Magnetization transfer can predict clinical evolution in patients with multiple sclerosis. Journal of Neurology 2002, 249:662-668.
188. Sato E.H., Ariga H., Sullivan D.A. Impact of androgen therapy in Sjögren's syndrome: Hormonal influence on lymphocyte populations and Ia expression in lacrimal glands of MRL/Mp-lpr/lpr mice. Investigative Ophthalmology and Visual Science 1992, 33:2537-2545.
189. Schumacher M., Guennoun R., Robert F., et al. Local synthesis and dual actions of progesterone in the nervous system: Neuroprotection and myelination. Growth Hormone IGF Research 2004, 14(supplement A):S18-S33.
190. Scofield R., Bruner G., Kelly J.B.N., Harley J. Evidence from XXY, XX and XY for a gene dose effect from the X chromosome in human systematic lupus erythematosus. Lupus 2007, 13:757.
191. Shang Y., Brown M. Molecular determinants for the tissue specificity of SERMs. Science 2002, 295:2465-2468.
192. Sherwin B.B. Estrogen and/or androgen replacement therapy and cognitive functioning in surgically menopausal women. Psychoneuroendocrinology 1988, 13:345-357.
193. Shim G.J., Kis L.L., Warner M., Gustafsson J.A. Autoimmune glomerulonephritis with spontaneous formation of splenic germinal centers in mice lacking the estrogen receptor alpha gene. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:1720-1724.
194. Sicotte N.L., Giesser B.S., Tandon V., et al. Testosterone treatment in multiple sclerosis: A pilot study. Archives of Neurology 2007, 64:683-688.
195. Sicotte N.L., Liva S.M., Klutch R., et al. Treatment of multiple sclerosis with the pregnancy hormone estriol. Annals of Neurology 2002, 52:421-428.
196. Sierra A., Azcoitia I., Garcia-Segura L. Endogenous estrogen formation is neuroprotective in model of cerebellar ataxia. Endocrine 2003, 21:43-51.
197. Simon J.H., Jacobs L.D., Campion M., et al. Magnetic resonance studies of intramuscular interferon beta-1a for relapsing multiple sclerosis. The Multiple Sclerosis Collaborative Research Group [see comments]. Annals of Neurology 1998, 43:79-87.
198. Smith-Bouvier D.L., Divekar A.A., Sasidhar M., et al. A role for sex chromosome complement in the female bias in autoimmune disease. Journal of Experimental Medicine 2008, 205:1099.
199. Smith D.L., Dong X., Du S., Oh M., Singh R.R., Voskuhl R.R. A female preponderance for chemically induced lupus in SJL/J mice. Clinical Immunolology 2007, 122:101-107.
200. Smith M.E., Eller N.L., McFarland H.F., Racke M.K., Raine C.S. Age dependence of clinical and pathological manifestations of autoimmune demyelination. Implications for multiple sclerosis. American Journal of Pathology 1999, 155:1147-1161.
201. Soldan S.S., Retuerto A.I., Sicotte N.L., Voskuhl R.R. Immune modulation in multiple sclerosis patients treated with the pregnancy hormone estriol. Journal of Immunology 2003, 171:6267-6274.
202. Spring S., Lerch J.P., Henkelman R.M. Sexual dimorphism revealed in the structure of the mouse brain using three-dimensional magnetic resonance imaging. NeuroImage 2007, 35:1424-1433.
203. Sribnick E.A., Ray S.K., Nowak M.W., Li L., Banik N.L. 17Beta-estradiol attenuates glutamate-induced apoptosis and preserves electrophysiologic function in primary cortical neurons. Journal of Neuroscience Research 2004, 76:688-696.
204. Sribnick E.A., Wingrave J.M., Matzelle D.D., Ray S.K., Banik N.L. Estrogen as a neuroprotective agent in the treatment of spinal cord injury. Annals of the New York Academy of Sciences 2003, 993:125-133. discussion 159-160.
205. Steinberg A.D., Melez K.A., Raveche E.S., et al. Approach to the study of the role of sex hormones in autoimmunity. Arthritis and Rheumatism 1979, 22:1170-1176.
206. Stevenson V.L., Leary S.M., LosseffN.A., et al. Spinal cord atrophy and disability in MS: A longitudinal study. Neurology 1998, 51:234-238.
207. Stevenson V.L., Miller D.H., Leary S.M., et al. One year follow up study of primary and transitional progressive multiple sclerosis. Journal of Neurology, Neurosurgery and Psychiatry 2000, 68:713-718.
208. Stone L.A., Frank J.A., Albert P.S., Bash C.N., Calabresi P.A., Maloni H., McFarland H.F. Characterization of MRI response to treatment with interferon beta-1b: Contrast-enhancing MRI lesion frequency as a primary outcome measure. Neurology 1997, 49:862-869.
209. Subramanian S., Matejuk A., Zamora A., Vandenbark A.A., Offner H. 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. Journal of Immunology 2003, 170:1548-1555.
210. Sur P., Sribnick E.A., Wingrave J.M., Nowak M.W., Ray S.K., Banik N.L. Estrogen attenuates oxidative stress-induced apoptosis in C6 glial cells. Brain Research 2003, 971:178-188.
211. Suzuki S., Brown C.M., Dela Cruz C.D., Yang E., Bridwell D.A., Wise P.M. Timing of estrogen therapy after ovariectomy dictates the efficacy of its neuroprotective and antiinflammatory actions. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:6013-6018.
212. SwerdloffR.S., Wang C. Androgens and the ageing male. Best Practice and Research Clinical Endocrinology and Metabolism 2004, 18:349-362.
213. Takao T., Flint N., Lee L., Ying X., Merrill J., Chandross K.J. 17Beta-estradiol protects oligodendrocytes from cytotoxicity induced cell death. Journal of Neurochemistry 2004, 89:660-673.
214. Tan R.S., Pu S.J. A pilot study on the effects of testosterone in hypogonadal aging male patients with Alzheimer's disease. Aging Male 2003, 6:13-17.
215. Tenover J.S., Matsumoto A.M., Plymate S.R., Bremner W.J. The effects of aging in normal men on bioavailable testosterone and luteinizing hormone secretion: Response to clomiphene citrate. Journal of Clinical Endocrinology and Metabolism 1987, 65:1118-1126.
216. Teuscher C., Noubade R., Spach K., et al. Evidence that the Y chromosome influences autoimmune disease in male and female mice. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:8024-8029.
217. Thorogood M., Hannaford P.C. The influence of oral contraceptives on the risk of multiple sclerosis. British Journal of Obstetric Gynaecology 1998, 105:1296-1299.
218. Tiwari-WoodruffS., Morales L.B., Lee R., Voskuhl R.R. Differential neuroprotective and antiinflammatory effects of estrogen receptor (ER){alpha} and ERbeta ligand treatment. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:14813-14818.
219. Tomassini V., Onesti E., Mainero C., et al. Sex hormones modulate brain damage in multiple sclerosis: MRI evidence. Journal of Neurology, Neurosurgery and Psychiatry 2005, 76:272-275.
220. Tortorella C., Viti B., Bozzali M., et al. A magnetization transfer histogram study of normal-appearing brain tissue in MS. Neurology 2000, 54:186-193.
221. Urowitz M.B., Ibanez D., Jerome D., Gladman D.D. The effect of menopause on disease activity in systemic lupus erythematosus. Journal of Rheumatology 2006, 33:2192-2198.
222. van Walderveen M.A., Tas M.W., Barkhof F., Polman C.H., Frequin S.T., Hommes O.R., Valk J. Magnetic resonance evaluation of disease activity during pregnancy in multiple sclerosis. Neurology 1994, 44:327-329.
223. Vegeto E., Bonincontro C., Pollio G., et al. Estrogen prevents the lipopolysaccharide-induced inflammatory response in microglia. Journal of Neuroscience 2001, 21:1809-1818.
224. Verdru P., Theys P., D'Hooghe M.B., Carton H. Pregnancy and multiple sclerosis: The influence on long term disability. Clinical Neurology and Neurosurgery 1994, 96:38-41.
225. Verghese J., Kuslansky G., Katz M.J., et al. Cognitive performance in surgically menopausal women on estrogen. Neurology 2000, 55:872-874.
226. Vermeulen A. Clinical review 24: Androgens in the aging male. Journal of Clinical Endocrinology and Metabolism 1991, 73:221-224.
227. Vidaver R. Molecular and clinical evidence of the role of estrogen in lupus. Trends in Immunology 2002, 23:229-230.
228. Villard-Mackintosh L., Vessey M.P. Oral contraceptives and reproductive factors in multiple sclerosis incidence. Contraception 1993, 47:161-168.
229. Viscoli C.M., Brass L.M., Kernan W.N., Sarrel P.M., Suissa S., Horwitz R.I. Estrogen therapy and risk of cognitive decline: Results from the Women's Estrogen for Stroke Trial (WEST). American Journal of Obstetric Gynecology 2005, 192:387-393.
230. Voskuhl R. Sex hormomes and other pregnancy-related factors with therapeutic potential in multiple sclerosis. Multiple Sclerosis Therapeutics 2003, vol. 32:535-549. Martin Dunitz, London. D. Cohen, R. Rudick (Eds.).
231. Voskuhl R.R. Chronic relapsing experimental allergic encephalomyelitis in the SJL mouse: Relevant techniques. Methods 1996, 10:435-439.
232. Voskuhl R.R., Palaszynski K. Sex hormones and experimental autoimmune encephalomyelitis: Implications for multiple sclerosis. Neuroscientist 2001, 7:258-270.
233. Voskuhl R.R., Pitchekian-Halabi H., MacKenzie-Graham A., McFarland H.F., Raine C.S. Gender differences in autoimmune demyelination in the mouse: Implications for multiple sclerosis. Annals of Neurology 1996, 39:724-733.
234. Vukusic S., Hutchinson M., Hours M., et al. Pregnancy and multiple sclerosis (the PRIMS study): Clinical predictors of post-partum relapse. Brain 2004, 127:1353-1360.
235. Wagner C.K., Xu J., Pfau J.L., Quadros P.S., De Vries G.J., Arnold A.P. Neonatal mice possessing an Sry transgene show a masculinized pattern of progesterone receptor expression in the brain independent of sex chromosome status. Endocrinology 2004, 145:1046-1049.
236. Waxman S.G. Demyelinating diseases - new pathological insights, new therapeutic targets [editorial; comment]. New England Journal of Medicine 1998, 338:323-325.
237. Wegmann T.G., Lin H., Guilbert L., Mosmann T.R. Bidirectional cytokine interactions in the maternal-fetal relationship: Is successful pregnancy a TH2 phenomenon? [see comments]. Immunology Today 1993, 14:353-356.
238. Wei T., Lightman S.L. The neuroendocrine axis in patients with multiple sclerosis. Brain 1997, 120:1067-1076.
239. Weinshenker B.G. Natural history of multiple sclerosis. Annals of Neurology 1994, 36:S6-S11.
240. Weiss D.J., Gurpide E. Non-genomic effects of estrogens and antiestrogens. Journal of Steroid Biochemistry 1988, 31:671-676.
241. Whitacre C.C., Reingold S.C., O'Looney P.A. A gender gap in autoimmunity. Science 1999, 283:1277-1278.
242. Wilcoxen S.C., Kirkman E., Dowdell K.C., Stohlman S.A. Gender-dependent IL-12 secretion by APC is regulated by IL-10. Journal of Immunology 2000, 164:6237-6243.
243. Wise P.M., Dubal D.B., Wilson M.E., Rau S.W., Bottner M. Minireview: Neuroprotective effects of estrogen - new insights into mechanisms of action. Endocrinology 2001, 142:969-973.
244. Woolley C.S. Effects of estrogen in the CNS. Current Opinion in Neurobiology 1999, 9:349-354.
245. Wujek J.R., Bjartmar C., Richer E., RansohoffR.M., Yu M., Tuohy V.K., Trapp B.D. Axon loss in the spinal cord determines permanent neurological disability in an animal model of multiple sclerosis. Journal of Neuropathology and Experimental Neurology 2002, 61:23-32.
246. Xiao B.G., Liu X., Link H. Antigen-specific T cell functions are suppressed over the estrogen-dendritic cell-indoleamine 2,3-dioxygenase axis. Steroids 2004, 69:653-659.
247. Yankova M., Hart S.A., Woolley C.S. Estrogen increases synaptic connectivity between single presynaptic inputs and multiple postsynaptic CA1 pyramidal cells: A serial electron-microscopic study. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:3525-3530.
248. Yune T.Y., Kim S.J., Lee S.M., et al. Systemic administration of 17beta-estradiol reduces apoptotic cell death and improves functional recovery following traumatic spinal cord injury in rats. Journal of Neurotrauma 2004, 21:293-306.
249. Zhang Q.H., Hu Y.Z., Cao J., Zhong Y.Q., Zhao Y.F., Mei Q.B. Estrogen influences the differentiation, maturation and function of dendritic cells in rats with experimental autoimmune encephalomyelitis. Acta Psychiatrica Scandinavica 2004, 25:508-513.
250. Zhang Z., Cerghet M., Mullins C., Williamson M., Bessert D., SkoffR. Comparison of in vivo and in vitro subcellular localization of estrogen receptors alpha and beta in oligodendrocytes. Journal of Neurochemistry 2004, 89:674-684.
251. Zhao G.J., Koopmans R.A., Li D.K., Bedell L., Paty D.W. Effect of interferon beta-1b in MS: Assessment of annual accumulation of PD/T2 activity on MRI. UBC MS/MRI Analysis Group and the MS Study Group. Neurology 2000, 54:200-206.
252. Zhao L., Wu T.W., Brinton R.D. Estrogen receptor subtypes alpha and beta contribute to neuroprotection and increased Bcl-2 expression in primary hippocampal neurons. Brain Research 2004, 1010:22-34.