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Immune modulation by estrogens

Role in CNS HIV-1 infection

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Abstract

Experimental and epidemiological data suggest that estrogen can be protective in both brain injury and infection. While estrogens can act directly on neurons to promote neuronal survival, estrogen also has anti-inflammatory properties that may contribute to overall neuroprotection. Accordingly, estrogens may have particular relevance in chronic neuroimmune disorders such as HIV dementia. As AIDS is now a leading cause of death among women in their reproductive years, understanding the role that female sex hormones might play in the physiology of HIV-1 infection is especially critical. Indeed, there is accumulating evidence that many manifestations of HIV differ in women. For instance, it is now well established that women present with a lower viral titer at the time of seroconversion, have lower HIV viral loads compared to men at similar stages of disease, and may have altered disease progression during pregnancy. Conversely, while epidemiological studies suggest that women may be more volunerable to certain late-stage AIDS-related illnesses including HIV dementia, there is accumulating data that strongly suggest an estrogen-deficient state is associated with long-term HIV infection in some women. Evaluated as a whole, existing evidence indicates that estrogen can directly protect neurons from damage, can modulate brain inflammation, and could act to maintain low titers of the HIV-1 virus. Accordingly, it can be hypothesized that maintenance of serum estradiol levels could decrease the incidence of HIV dementia and other AIDS-related neurological syndromes in HIV-1 positive women. In this article, we both summarize current understanding and present new data related to the potential mechanisms whereby estrogen could modulate the mechanics and the consequences of HIV-1 infection in the brain and thereby thwart the development of HIV dementia.

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References

  1. McEwen B. S. and Alves, S. E. (1999) Endocr. Rev. 20, 279–307.

    Article  PubMed  CAS  Google Scholar 

  2. Lang, T. J. (2004) Clin. Immunol. 113, 224–230.

    Article  PubMed  CAS  Google Scholar 

  3. Mendelsohn, M. E. and Karas, R. H. (2005) Science 308, 1583–1587.

    Article  PubMed  CAS  Google Scholar 

  4. Mirza, F. S. and Prestwood, K. M. (2004) Endocrinol. Metab. Clin. North. Am. 33, 741–759.

    Article  PubMed  CAS  Google Scholar 

  5. Kleerekoper, M. (2005) Semin. Reprod. Med. 23, 141–148.

    Article  PubMed  Google Scholar 

  6. Paganini-Hill, A. and Henderson, V. W. (1994) Am. J. Epidem. 140, 256–261.

    CAS  Google Scholar 

  7. Henderson, V. M., Paganini-Hill, A., Emanuel, C. K., Dunn, M. E., and Buckwalter, G. (1994). Arch. Neurol. 51, 896–900

    PubMed  CAS  Google Scholar 

  8. Paganini-Hill, A. (1995). Prog. Cardiovasc. Dis. 38, 223–242

    Article  PubMed  CAS  Google Scholar 

  9. Kawas, C., Resnick, S., Morrison, A., et al. (1997) Neurology 48, 1517–1521.

    PubMed  CAS  Google Scholar 

  10. Sherwin, B. B. (2005). Horm. Behav. 47, 371–375.

    Article  PubMed  CAS  Google Scholar 

  11. MacLusky, N. J. and Naftolin, F. (1981). Science 211, 1294–1230.

    Article  PubMed  CAS  Google Scholar 

  12. Woolley, C. S. and McEwen, B. S. (1992). J. Neurosci. 12, 2549–2554.

    PubMed  CAS  Google Scholar 

  13. Gould, E., Woolley, C. S., Frankfort, M., and McEwen, B. S. (1990). J. Neurosci. 10, 1286–1291.

    PubMed  CAS  Google Scholar 

  14. Dubal, D. B., Kashon, M. L., Pettigrew, L. C., et al. (1998). J. Cereb. Blood Flow Metab. 18, 1253–1258.

    Article  PubMed  CAS  Google Scholar 

  15. Mendelowitsch, A., Ritz, M. F., Ros, J., Langemann, H., and Gratzl, O. (2001). Brain Res. 901, 230–236.

    Article  PubMed  CAS  Google Scholar 

  16. Toran-Allerand, C. D., Ellis, L. and Pfenninger, K. H. (1988). Brain Res. 469, 87–100.

    PubMed  CAS  Google Scholar 

  17. Goodman, Y., Bruce, A. J., Cheng, B., and Mattson, M. P. (1996). J. Neurochem. 66, 1836–1844.

    Article  PubMed  CAS  Google Scholar 

  18. Singer, C. A., Figueroa-Masot, X. A., Batchelor, R. H., and Dorsa, D. M. (1999). J. Neurosci. 19, 2455–2463.

    PubMed  CAS  Google Scholar 

  19. Koike, S., Sakai, M., and Muramatsu, M. (1997). Nucleic Acids Res. 15, 2499–2513.

    Article  Google Scholar 

  20. Kuper, G. G., Carlsson, B., Grandien, K., et al. (1997). Endocrinology 138, 863–870.

    Article  Google Scholar 

  21. Shughrue, P. J., Lane, M. V., and Merchenthaler, I. (1997) J. Comp. Neurol. 388, 507–525.

    Article  PubMed  CAS  Google Scholar 

  22. McEwen, B. S., Kloet, E. R. D. and Rostene, W. (1986). Physiol. Rev. 66, 1121–1188.

    PubMed  CAS  Google Scholar 

  23. Langub, M. and Matson, R. (1992). Endocrinology 130, 364–372.

    Article  PubMed  CAS  Google Scholar 

  24. Santagati, S., Melcangi, R., Celotti, F., Martini, L., and Maggi, A. (1994). J. Neurochem. 63, 2058–2064.

    Article  PubMed  CAS  Google Scholar 

  25. Cowley, S. M., Hoare, S., Mosselman, S., and Parker, M. G. (1997). J. Biol. Chem. 272, 19858–19862.

    Article  PubMed  CAS  Google Scholar 

  26. Nilsson, S. and Gustafsson, J. A. (2002). Crit. Rev. Eukaryot. Gene Expr. 12, 237–257.

    Article  PubMed  CAS  Google Scholar 

  27. Paech, K., Webb, P., Kuiper, G. G., et al. (1997). Science 277, 1508–1510.

    Article  PubMed  CAS  Google Scholar 

  28. Revelli, A., Massobrio, M., and Tesarik, J. (1998). Endorc. Rev. 19, 3–17.

    Article  CAS  Google Scholar 

  29. Aronica, S., Kraus, W., and Katzenellenbogen, B. (1994). Proc. Natl. Acad. Sci. USA 91, 8517–8521.

    Article  PubMed  CAS  Google Scholar 

  30. Wong, M. and Moss. R. (1992). J. Neurosci. 12, 3217–3225.

    PubMed  CAS  Google Scholar 

  31. Zhou Y., Watters, J. J., and Dorsa, D. M. (1996). Endocrinology 137, 2163–2166

    Article  PubMed  CAS  Google Scholar 

  32. Wilson, M. E., Dubal, D. B., and Wise, P. M. (2000). Brain Res. Brain Res. Protoc. 873, 235–242.

    CAS  Google Scholar 

  33. Wilson, M. E., Liu, Y., and Wise, P. M. (2002). Brain Res. Mol. Brain Res. 102, 48–54.

    Article  PubMed  CAS  Google Scholar 

  34. Watters, J. J., Campbel, I. J. S., Cunningham, M. J. Krebs, E. G., and Dorsa, D. M. (1997). Endocrinology 138, 4030–4033.

    Article  PubMed  CAS  Google Scholar 

  35. Singh, M., Setalo, G., Gauan, X., Warren, M., and Toran-Allarand C. D. (1999). J. Neurosci. 19, 1179–1188.

    PubMed  CAS  Google Scholar 

  36. Fitzpatrick, J. L., Mize, A. L., Wade, C. B., Harris, J. A., Shapiro, R. A., and Dorsa, D. M. (2002). J. Neurochem. 82, 674–682.

    Article  PubMed  CAS  Google Scholar 

  37. Mize, A. L., Shapiro, R. A., and Dorsa, D. M. (2003). Endocrinology 144, 306–312.

    Article  PubMed  CAS  Google Scholar 

  38. Toran-Allerand, C. D., Guan, X., MacLusky, N. J. et al. (2002). J. Neurosci. 22, 8391–8340.

    PubMed  CAS  Google Scholar 

  39. Simoncini, T., Hafezi-Moghadam, A., Brazil, D. P., Ley, K., Chin, W. W., and Liao, J. K. (2000). Nature 407, 538–541.

    Article  PubMed  CAS  Google Scholar 

  40. DeVita, V. T., Hellman, S. and Rosenberg, S. A. (eds.) (1997). AIDS: Etiology, Diagnosis, Treatment, and Prevention. Lippincott-Raven. Philadelphia, PA.

    Google Scholar 

  41. Freed, E. O. (2001). Somat. Cell. Mol. Genet. 26, 13–33.

    Article  PubMed  CAS  Google Scholar 

  42. Brigati, C., Giacca, M., Noonan, D., and Albini, A. (2003). FEMS Microbiol. Lett. 220, 57–65.

    Article  PubMed  CAS  Google Scholar 

  43. Marcello, A., Lusic, M., Pegoraro, G., Pellegrini, V., Beltram, F., and Giacca, M. (2004). Gene 326, 1–11.

    Article  PubMed  CAS  Google Scholar 

  44. Pereira, L. A., Bentley, K., Peeters, A., Churchill, M. J., and Deacon, N. J. (2000). Nucleic Acids Res. 28, 663–668.

    Article  PubMed  CAS  Google Scholar 

  45. Surabhi, R. M. and Gaynor, R. B. (2002). J. Virol. 76, 12963–12973.

    Article  PubMed  CAS  Google Scholar 

  46. Janssen, R. S., Cornblath, D. R., Epstein, L. G., McArthur, J., and Price, R. W. (1989). Neurology 39, 119–122.

    PubMed  CAS  Google Scholar 

  47. Atwood, W. J., Berger, J., Kaderman, R., Tornatore, C. S., and Major, E. O. (1993). Clin. Microbiol. Rev. 6, 339–366.

    PubMed  CAS  Google Scholar 

  48. Heaton, R. K., Velim, R. A., McCutchan, J. A., et al. (1994). Psychosomatic Med. 56, 8–17.

    CAS  Google Scholar 

  49. Belman, A. L., Ultman, M., Kurtzberg, D., and Conewesson, B. (1985). Ann. Neurol. 18, 560–566.

    Article  PubMed  CAS  Google Scholar 

  50. Epstein, L. G., Sharer, L. R., Joshi, V. V., Fojas, M. M., Koenigsberger, M. R., and Oleske, J. M. (1985). Ann. Neurol. 17, 488–496.

    Article  PubMed  CAS  Google Scholar 

  51. Ensoli, F., Fiorelli, V., Muratori, S., et al. (1999). Crit. Rev. Immunol. 19, 97–116.

    PubMed  CAS  Google Scholar 

  52. Navia, B. A., Cho, E. S., Petiio, C. K., and Price, R. W. (1986) Ann. Neurol. 19, 525–535.

    Article  PubMed  CAS  Google Scholar 

  53. Everall, I., Luthert, P., and Lantos, P. (1993). J. Neuropath. Exp. Neurol. 52, 561–566.

    Article  PubMed  CAS  Google Scholar 

  54. Spargo, E., Everall, I. P., and Lantos, P. L. (1993). J. Neurol. Neurosurg. Psychiatry 56, 487–491.

    PubMed  CAS  Google Scholar 

  55. Fox, L., Alford, M., Achim, C., Mallory, M., and Masliaah, E. (1997). J. Neuropathol. Exp. Neurol. 56, 360–368.

    PubMed  CAS  Google Scholar 

  56. Masliah, E., Ge, N., Morey, M., DeTeresa, R., Terry, R. D., and Wiley, C. A. (1992). Lab. Invest. 66, 285–291.

    PubMed  CAS  Google Scholar 

  57. Masliah, E., Heaton, R. K., Marcotte, T. D., Ellis, R. J., and Wiley, C. A. (1997). Ann. Neurol. 42, 963–972.

    Article  PubMed  CAS  Google Scholar 

  58. Wiley, C. A., Soontornniyomkij, V., Radhakrishnan, L., et al. (1998). Brain Pathol. 8, 277–284.

    Article  PubMed  CAS  Google Scholar 

  59. Del-Rio Hortega, P. (1932) In: Cytology and cellular pathology of the nervous system. Penfield, W. (ed.) P.B. Hoeber New York, pp. 481–534.

    Google Scholar 

  60. Glass, L., Fedor, H., Wesselingh, S. L., and McArthur, J. C. (1995). Ann. Neurol. 38, 755–762.

    Article  PubMed  CAS  Google Scholar 

  61. Tyor, W. R., Wesselingh, W., Griffith, S. W., McArther, J. C., and Griffen, D. E. (1995). J. AIDS Human Ret. 9, 379–388.

    CAS  Google Scholar 

  62. Colton, A. C. and Gilbert, D. L. (1987). FEBS Lett. 223, 284–288.

    Article  PubMed  CAS  Google Scholar 

  63. Hewitt, R. G., Parsa, N., and Gugino, L. (2001). AIDS Read. 11, 29–33.

    PubMed  CAS  Google Scholar 

  64. Farzadegan, H., Hoover, D. R., Astemborski, J., et al. (1998). Lancet 352, 1510–1514.

    Article  PubMed  CAS  Google Scholar 

  65. Biber, C. L., Jaker, M. A., Kloser, P., Auerbach, S. B., and Rhoads, G. G. (1999) AIDS Patient Care STDS 13, 103–110.

    Article  PubMed  CAS  Google Scholar 

  66. Denison, R. (1999). World 96, 4–5.

    Google Scholar 

  67. Quinn, T. C. and Overbaugh, J. (2005). Science 308, 1582–1583.

    Article  PubMed  CAS  Google Scholar 

  68. Chiesi, A., Vella, S., Dally, L. G., et al. (1996). J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 11, 39–44.

    PubMed  CAS  Google Scholar 

  69. Morlat, P., Parneix, P., Douard, D., et al. (1992). AIDS 6, 1187–1193.

    Article  PubMed  CAS  Google Scholar 

  70. Chiesi, A., Seeber, A. C., Dally, L. G., Floridia, M., Rezza, G., and Vella, S. (1996). J. Neurol. Sci. 144, 107–113.

    Article  PubMed  CAS  Google Scholar 

  71. Semple, S. J., Patterson, T. L., Stratis-Troster, K., Atkinson, J. H., McCutchan, J. A., and Grant, I. (1996). Women and Health 24, 17–41.

    Article  CAS  Google Scholar 

  72. Robertson, K., Wilkins, J., Messenheimer, J., et al. (1996). J. Neuro-AIDS 1, 166.

    Google Scholar 

  73. Bouwman, F. H., Skolasky, R. L., Hes, D., et al. (1998). Neurology 50, 1814–1820.

    PubMed  CAS  Google Scholar 

  74. Lopez, O. L., Wess, J., Sanchez, J., Dew, M. A., and Becker, J. T. (1999). Eur. J. Neurol. 6, 205–209.

    PubMed  CAS  Google Scholar 

  75. Clark, R. A. and Bessinger, R. (1997). J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 15, 341–354.

    PubMed  CAS  Google Scholar 

  76. Chirgwin, K. D., Feldman, J., Muneyyirci-Delale, O., Landesman, S., and Minkoff, H. (1996). J. Acquir. Immune. Defic. Syndr. Hum. Retrovirol. 12, 489–494.

    PubMed  CAS  Google Scholar 

  77. Kirkham, C. M., and Lobb, D. J. (1998). CMAJ 158, 317–323.

    PubMed  CAS  Google Scholar 

  78. Minkoff, H. L., Eisenberger Matityahu, D., Feldman, J., Burk, R., and Clarke, L. (1999). Am. J. Obstet. Gynecol. 180, 824–836.

    Article  PubMed  CAS  Google Scholar 

  79. Cu-Uvin, S., Wright, D. J., Anderson, D., et al. (2000). J. Womens Health Gend. Based Med. 9, 857–863.

    Article  PubMed  CAS  Google Scholar 

  80. Grinspoon, S., Corcoran, C., Miller, K., et al. (1997). J. Clin. Endocrinol. Metab. 82, 1332–1337.

    Article  PubMed  CAS  Google Scholar 

  81. Sterling, T. R., Lyles, C. M., Vlahov, D., Astemborski, J., Margolick, J. B., and Quinn, T. C. (1999). J. Infect. Dis. 180, 666–672.

    Article  PubMed  CAS  Google Scholar 

  82. Lyles, C. M., Dorrucci, M., Vlahov, D., et al. (1999). J. Infect. Dis. 180, 1018–1024.

    Article  PubMed  CAS  Google Scholar 

  83. Rezza, G., Lepri, A. C., d'Arminio Monforte, A., et al. (2000). J. Acquir. Immune. Defic. Syndr. 25, 56–62.

    Article  PubMed  CAS  Google Scholar 

  84. Anastos, K., Gange, S. J., Lau, B., et al. (2000). J. Acquir. Immune. Defic. Syndr. 24, 218–226.

    PubMed  CAS  Google Scholar 

  85. Sterling, T. R., Vlahov, D., Astemborski, J., Hoover, D. R., Margolick, J. B., and Quinn, T. C. (2001). N. Engl. J. Med. 344, 720–725.

    Article  PubMed  CAS  Google Scholar 

  86. Napravnik, S., Poole, C., Thomas, J. C., and Eron, J. J. J. (2002). J. Acquir. Immune. Defic. Syndr. 31, 11–19.

    PubMed  CAS  Google Scholar 

  87. Cooney, A. J., Tsai, S. Y., O'Malley, B. W., and Tsai, M. J. (1991). J. Virol. 65, 2853–2860.

    PubMed  CAS  Google Scholar 

  88. Mitra, D., Sikder, S. K., and Laurence, J. (1995). Virology 214, 512–521.

    Article  PubMed  CAS  Google Scholar 

  89. Bourinbaiar, A. S., Nagorny, R., and Tan, X. (1992). FEBS Lett. 302, 206–208.

    Article  PubMed  CAS  Google Scholar 

  90. Lee, A. W., Mitra, D., and Laurence, J. (1997). AIDS Res. Hum. Retroviruses 13, 1235–1242.

    Article  PubMed  CAS  Google Scholar 

  91. Smith, S. M., Baskin, G. B., and Marx, P. A. (2000). J. Infect. Dis. 182, 708–715.

    Article  PubMed  CAS  Google Scholar 

  92. Wilson, M. E., Allred, K. F., Bisotti, A. J., et al. (2006). AIDS Res. Human Retroviruses 22, 350–356.

    Article  CAS  Google Scholar 

  93. Savio, T., and Levi, G. (1993). J. Neurosci. Res. 34, 265–272.

    Article  PubMed  CAS  Google Scholar 

  94. New, D., Ma, M., Epstein, L. G., Nath, A., and Gelbard, H. A. (1997). J. Neuroviol. 3, 168–173.

    Article  CAS  Google Scholar 

  95. Nath, A., Haughey, N. J., Jones, M., Anderson, C., Bell, J. E., and Geiger, J. D. (2000). Ann. Neurol. 47, 186–194.

    Article  PubMed  CAS  Google Scholar 

  96. Singh, I. N., Good, R. J., Dean, C., et al. (2004). J. Neurovirol. 10, 141–151.

    Article  PubMed  CAS  Google Scholar 

  97. Turchan, J., Anderson, C., Hauser, K. F., et al. (2001). BMC Neurosci. 2, 3–11.

    Article  PubMed  CAS  Google Scholar 

  98. Kendall, S. L., Anderson, C. F., Nath, A., et al. (2005) BMC Neurosci. 6, 40.

    Article  PubMed  CAS  Google Scholar 

  99. Howard, S. A., Brooke, S. M., and Sapolsky, R. M. (2001). Exp. Neurol. 168, 385–391.

    Article  PubMed  CAS  Google Scholar 

  100. Zemlyak, I., Brooke, S. M., and Sapolsky, R. M. (2002). Brain Res. 958, 272–276.

    Article  PubMed  CAS  Google Scholar 

  101. Zemlyak, I., Brooke, S., and Sapolsky, R. (2005). Brain Res. 1046, 130–136.

    Article  PubMed  CAS  Google Scholar 

  102. Corasaniti, M. T., Amantea, D., Russo, R., et al. (2005). Neurotoxicology 26, 893–903.

    Article  PubMed  CAS  Google Scholar 

  103. Bahr, B. A. (1995). J. Neurosci. Res. 42, 294–305.

    Article  PubMed  CAS  Google Scholar 

  104. Gahwiler, B. H., Capogna, M., Debanne, J. S., McKinney, J. S., and Thompson, S. M. (1997). Trends. Neurosci. 20, 471–477.

    Article  PubMed  CAS  Google Scholar 

  105. Xiang, Z., Hrabetova, S., Moskowitz, S. I., et al. (2000). J. Neurosci. Methods 98, 145–154.

    Article  PubMed  CAS  Google Scholar 

  106. Turchan, J., Pocernich, C. B., Gairola, C. et al. (2003). Neurology 60, 307–314.

    PubMed  CAS  Google Scholar 

  107. Cutolo, M., Sulli, A., Seriolo, B., Accardo, S., and Masi, A. T. (1995). Clin. Exp. Rheum. 13, 217–226.

    CAS  Google Scholar 

  108. Elenkov, I. J., Hoffman, J., and Wilder, R. L. (1997). Mol. Med. Today 3, 379–383.

    Article  PubMed  CAS  Google Scholar 

  109. Cutolo, M., and Wilder, R. L. (2000). Rheum. Dis. Clin. North Am. 26, 825–839.

    Article  PubMed  CAS  Google Scholar 

  110. Vegeto, E., Pollio, G., Ciana, P., and Maggi, A. (2000). Exp. Gerontol. 35, 1309–1316.

    Article  PubMed  CAS  Google Scholar 

  111. Bruce-Keller, A. J., Keeling, J. L., Keller, J. N., Huang, F. F., Camondola, S., and Mattson, M. P. (2000). Endocrinology 141, 3646–3656.

    Article  PubMed  CAS  Google Scholar 

  112. Baker, A. E., Brautigam, V. M., and Watters, J. J. (2004). Endocrinology 145, 5021–5032.

    Article  PubMed  CAS  Google Scholar 

  113. Bruce-Keller, A. J., Barger, S. W., Moss, N. I., Pham, J. T., Keller, J. N., and Nath, A. (2001). J. Neurochem. 78, 1315–1324.

    Article  PubMed  CAS  Google Scholar 

  114. Grimaldi, L. M., Martino, G. V., Franciotta, D. M., et al. (1991). Ann. Neurol. 29, 21–25.

    Article  PubMed  CAS  Google Scholar 

  115. Perrella, O., Carrieri, P. B., Guarnaccia, D., and Soscia, M. (1992). J. Neurol. 239, 387–389.

    PubMed  CAS  Google Scholar 

  116. Wesselingh, S. L., Takahashi, K., Glass, J. D., McArthur, J. C., Griffin, J. W., and Griffin, D. E. (1997). J. Neuroimmunol. 74, 1–8.

    Article  PubMed  CAS  Google Scholar 

  117. Adamski, J., Ma, Z., Nozell, S., and Benveniste, E. N. (2004). Mol. Endocrinol. 18, 1963–1974.

    Article  PubMed  CAS  Google Scholar 

  118. Dimayuga, F. O., Reed, J. L., Carnero, G. A., et al. (2005). J. Neuroimmunol. 161, 123–136.

    Article  PubMed  CAS  Google Scholar 

  119. Adamski, J. and Benveniste, E. N. (2005). Mol. Endocrinol. 19, 113–124.

    Article  PubMed  CAS  Google Scholar 

  120. Lee, Y. W., Eum, S. Y., Nath, A., and Toborek, M. (2004). Cardiovasc. Res. 63, 139–148.

    Article  PubMed  CAS  Google Scholar 

  121. Paul, C. and Bolton, C. (1995). Int. J. Immunopharmacol. 17, 497–503.

    Article  PubMed  CAS  Google Scholar 

  122. Eralinna, J. P., Soilu-Hanninen, M., Roytta, M., Hukkanen, V., Salmi, A. A., and Salonen, R. (1996). J. Neuroimmunol. 66, 103–114.

    Article  PubMed  CAS  Google Scholar 

  123. Petito, C. K. and Cash, K. S. (1992). Ann. Neurol. 32, 658–666.

    Article  PubMed  CAS  Google Scholar 

  124. Power, C., Kong, P. A., Crawford, T. O., et al. (1993). Ann. Neurol. 34, 339–350.

    Article  PubMed  CAS  Google Scholar 

  125. Buttner, A., Mehraein, P., and Weis, S. (1996). Acta Neuropathol. (Berl.) 92, 35–41.

    Article  CAS  Google Scholar 

  126. Weis, S., Hang, H., and Budka, H. (1996). Clin. Neuropathol. 15, 361–366.

    PubMed  CAS  Google Scholar 

  127. Marshall, D. W., Brey, R. L., Butzin, C. A., Lucey, D. R., Abbadessa, S. M., and Boswell, R. N. (1991). J. Acquir. Immune. Defic. Syndr. 4, 777–778.

    PubMed  CAS  Google Scholar 

  128. Conant, K., McArthur, J. C., Griffin, D. E., Sjulson, L., Wahl, L. M., and Irani, D. N. (1999). Ann. Neurol. 46, 391–398.

    Article  PubMed  CAS  Google Scholar 

  129. Liuzzi, G. M., Mastroianni, C. M., Santacroce, M. P., et al. (2000). J. Neurovirol. 6, 156–163.

    PubMed  CAS  Google Scholar 

  130. Johnston, J. B., Zhang, K., Silva, C., et al. (2001). Ann. Neurol. 49, 230–241.

    Article  PubMed  CAS  Google Scholar 

  131. Mastroianni, C. M., Liuzzi, G., D'Ettorte, G., et al. (2002) HIV Clin. Triads 3, 310–315.

    Article  Google Scholar 

  132. Zhao, H., Xia, Z., Cai, G., Du, J., Zhu, T., and Shen, L. (1998). Chin. Med. J. (Engl.) 111, 551–555.

    CAS  Google Scholar 

  133. Pirila, E., Ramamurthy, N., Maisi, P., et al. (2001). Curr. Med. Chem. 8, 281–294.

    PubMed  CAS  Google Scholar 

  134. Liao, E. Y. and Luo, X. H. (2001). Endocrine 15, 291–295.

    Article  PubMed  CAS  Google Scholar 

  135. Curry, T. E. J., Mann, J. S., Huang, M. H., and Keeble, S. C. (1992). Biol. Reprod. 42, 256–264.

    Article  Google Scholar 

  136. Wise, P. M., Dubal, D. B., Wilson, M. E., Rau, S. W., and Bottner, M. (2001). Endocrinology 142, 969–973.

    Article  PubMed  CAS  Google Scholar 

  137. Mor, G., Nilson, J., Horvath, T., et al. (1999). J. neurobiol. 40, 484–496.

    Article  PubMed  CAS  Google Scholar 

  138. Ito, A., Bebo, B. F. J., Matejuk, A., et al. (2001). J. Immunol. 167, 542–552.

    PubMed  CAS  Google Scholar 

  139. Voskuhl, R. R. (2003). Int. MS J. 10, 60–66.

    PubMed  CAS  Google Scholar 

  140. Soldan, S. S., Retuerto, A. I. A., Sicotte, N. L., and Voskuhl, R. R. (2003). J. Immunol. 171, 6267–6274.

    PubMed  CAS  Google Scholar 

  141. Soucy, G., Boivin, G., Labrie, F., and Rivest, S. (2005). J. Immunol. 174, 6391–6398.

    PubMed  CAS  Google Scholar 

  142. Horvath, S., Kis, Z., Boldogkoi, Z., Nogradi, A., and Toldi, J. (2002). Eur. J. Neurosci. 15, 937–943.

    Article  PubMed  Google Scholar 

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Correspondence to Annadora J. Bruce-Keller.

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Wilson, M.E., Dimayuga, F.O., Reed, J.L. et al. Immune modulation by estrogens. Endocr 29, 289–297 (2006). https://doi.org/10.1385/ENDO:29:2:289

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  • DOI: https://doi.org/10.1385/ENDO:29:2:289

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