Skip to main content
Log in

Neuroprotection by ovarian hormones in animal models of neurological disease

  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

Overian hormones can protect against brain injury, neurodegeneration, and cognitive decline. Most attention has focused on estrogens and accumulating data demonstrate that estrogen seems to specifically protect cortical and hippocampal neurons from ischemic injury and from damage due to severe seizures. Although multiple studies demonstrate protection by estrogen, in only a few instances is the issue of how the steroid confers protection known. Here, we first review data evaluating the neuroprotective effects of estrogens, a selective estrogen receptor modulator (SERM), and estrogen receptor α-and β-selective ligands in animal models of focal and global ischemia. Using focal ischemia in ovariectomized ERαKO, ERβKO, and wild-type mice, we clearly established that the ERα subtype is the critical ER mediating neuroprotection in mouse focal ischemia. In rats and mice, the middle cerebral artery occlusion (MCAO) model was used to represent cerebrovascular stroke, while in gerbils the two-vessel occlusion model, representing global ischemia, was used. The gerbil global ischemia model was used to evaluate the neuroprotective effects of estrogen, SERMs, and ERα-and ERβ-selective compounds in the hippocampus. Analysis of neurogranin mRNA, a marker of viability of hippocampal neurons, with in situ hybridization, revealed that estrogen treatment protected the dorsal CA1 regions not only when administered before, but also when given 1 h after occlusion. Estrogen rarely is secreted alone and studies of neuroprotection have been less extensive for a second key ovarian hormone progesterone. In the second half of this review, we present data on neuroprotection by estrogen and progesterone in animal model of epilepsy followed by exploration into ovarian steroid effects on neuronal damage in models of multiple sclerosis and traumatic brain injury.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Behl, C. (2002). Nat. Rev. Neurosci. 3, 433–442.

    PubMed  CAS  Google Scholar 

  2. Garcia-Segura, L. M., Azcoitia, I., and DonCarlos, L. L. (2001). Prog. Neurobiol. 63, 29–60.

    Article  PubMed  CAS  Google Scholar 

  3. 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 

  4. Hoffman, G. E., Moore, N., Fiskum, G., and Murphy, A. Z. (2003). Exp. Neurol. 182, 124–134.

    Article  PubMed  CAS  Google Scholar 

  5. Veliskova, J., Velisek, L., Galanopoulou, A. S., and Sperber E. F. (2000). Epilepsia 41 (Suppl. 6), S30-S35.

    Article  PubMed  Google Scholar 

  6. Backstrom, T. (1976). Acta Neurolog. Scand. 54, 321–347.

    CAS  Google Scholar 

  7. Ramsay, R. E. (1987). J. Clin. Neurophysiol. 4, 23–25.

    Article  PubMed  CAS  Google Scholar 

  8. Schachter, S. C. (1988). Arch. Neurol. 45, 1267–1270.

    PubMed  CAS  Google Scholar 

  9. Morrell, M. J. (1992). Epilepsia 33, S49–61.

    PubMed  Google Scholar 

  10. Morrell, M. J. (1999). Neurology 53(4 Suppl. 1), S42–48.

    PubMed  CAS  Google Scholar 

  11. Morrell, M. J., Sarto, G. E., Shafer, P. O., Borda, E. A., Herzog, A., and Callanan, M. (2000). J. Womens Health Gend. Based Med. 9, 959–965.

    Article  PubMed  CAS  Google Scholar 

  12. Huang, Z., Huang, P. L., Panahian, N., Dalkara, T., Fishman, M. C., and Moskowitz, M. A. (1994). Science 265, 1883–1885.

    Article  PubMed  CAS  Google Scholar 

  13. Alkayed, N. J., Harukuni, I., Kimes, A. S., London, E. D., Traystman, R. J., and Hurn, P. D. (1998). Stroke 29, 159–165; discussion 166.

    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. Dubal, D. B., Shughrue, P. J., Wilson, M. E., Merchenthaler, I., and Wise, P. M. (1999). J. Neurosci 19, 6385–6393.

    PubMed  CAS  Google Scholar 

  16. Dubal, D. B., and Wise, P. M. (2001). Endocrinology, 142, 43–48.

    Article  PubMed  CAS  Google Scholar 

  17. Simpkins, J. W., Green, P. S., Gridley, K. E., Singh, M., de Fiebre, N. C., and Rajakumar, G. (1997). Am. J. Med. 103, 19S-25S.

    Article  PubMed  CAS  Google Scholar 

  18. Dubal, D. B., Zhu, H., Yu. J., et al. (2001). Proc. Natl. Acad. Sci. USA 98, 1952–1957.

    Article  PubMed  CAS  Google Scholar 

  19. Yang, S. H., Shi, J., Day, A. L., and Simpkins, J. W. (2000). Stroke 31, 745–749; discussion 749-750.

    PubMed  CAS  Google Scholar 

  20. Merchenthaler, I., Dellovade, T. L., and Shughrue, P. J. (2003). Ann. NY Acad. Sci. 1007, 89–100.

    Article  PubMed  CAS  Google Scholar 

  21. Shughrue, P. J., Stumpf, W. E., MacLusky, N. J., Zielinski, J. E., and Hochberg, R. B. (1990). Endocrinology 126, 1112–1124.

    Article  PubMed  CAS  Google Scholar 

  22. Choi, D. W. (1996). Curr. Opin. Neurobiol. 6, 667–672.

    Article  PubMed  CAS  Google Scholar 

  23. Leker R. R. and Shohami, E. (2002). Brain Res. Brain Res. Rev. 39, 55–73.

    Article  PubMed  Google Scholar 

  24. Teixeira, C., Reed, J. C. and Pratt, M. A. (1995). Cancer Res., 55, 3902–3907.

    PubMed  CAS  Google Scholar 

  25. Bredesen D. E. (1995). Ann. Neurol. 38, 839–851.

    Article  PubMed  CAS  Google Scholar 

  26. MacManus, J. P. and Buchan, A. M. (2000). J. Neurotrauma 17, 899–914.

    PubMed  CAS  Google Scholar 

  27. Merry, D. E. and Korsmeyer, S. J. (1997). Ann. Rev. Neurosci. 20, 245–267.

    Article  PubMed  CAS  Google Scholar 

  28. Tanaka, H., Grooms, S. Y., Bennett, M. V., and Zukin, R. S. (2000). Brain Res. 886, 190–207.

    Article  PubMed  CAS  Google Scholar 

  29. Graham, S. H. and Chen, J. (2001). J. Cereb. Blood Flow Metabol. 21, 99–109.

    Article  CAS  Google Scholar 

  30. Shughrue, P. J. and Merchenthaler, I. (2003). Neuroscience 116, 851–861.

    Article  PubMed  CAS  Google Scholar 

  31. Green, P. S., Gordon, K., and Simpkins, J. W. (1997). J. Steroid Biochem. Mol. Biol. 63, 229–235.

    Article  PubMed  CAS  Google Scholar 

  32. Toran-Allerand, C. D. (2000). Novartis Found. Symp. 230, 56–69 discussion 69-73.

    Article  PubMed  CAS  Google Scholar 

  33. Asimiadou, S., Bittigau, P., Felderhoff-Mueser, U., et al. (2005). Ann. Neurol. 58, 266–276.

    Article  PubMed  CAS  Google Scholar 

  34. Balthazart, J., Baillien, M., and Ball, G. F. (2005). J. Neuroendocrinol. 17, 553–559.

    Article  PubMed  CAS  Google Scholar 

  35. Bryant, D. N., Bosch, M. A., Ronnekleiv, O. K., and Dorsa, D. M. (2005). Neuroscience 133, 343–352.

    Article  PubMed  CAS  Google Scholar 

  36. Foster, T. C. (2005). Front. Neuroendocrinol. 26, 51–64.

    Article  PubMed  CAS  Google Scholar 

  37. Guerra, B., Diaz, M., Alonso, R., and Marin, R. (2004). J. Neurochem. 91, 99–109.

    Article  PubMed  CAS  Google Scholar 

  38. Hilke, S., Theodorsson, A., Fetissov, S., et al. (2005) Eur. J. Neurosci. 21, 2089–2099.

    Article  PubMed  Google Scholar 

  39. Malyala, A., Kelly, M. J., and Ronnekleiv, O. K. (2005). Steroids 70, 397–406.

    Article  PubMed  CAS  Google Scholar 

  40. Marin, R., Guerra, B., Alonso, R., Ramirez, C. M., and Diaz, M. (2005). Curr. Neurovasc. Res. 2, 287–301.

    Article  PubMed  CAS  Google Scholar 

  41. Qiu, J., Bosch, M. A., Tobias, S. C., et al. (2003). J. Neurosci. 23, 9529–9540.

    PubMed  CAS  Google Scholar 

  42. Moosmann, B. and Behl, C. (1999). Proc. Natl. Acad. Sci. USA 96, 8867–8872.

    Article  PubMed  CAS  Google Scholar 

  43. Wu, T. W., Wang, J. M., Chen, S., and Brinton, R. D. (2005). Neuroscience 135, 59–72.

    Article  PubMed  CAS  Google Scholar 

  44. Roof, R. L., Duvdevani, R., Heyburn, J. W., and Stein, D. G. (1996). Exp. Neurol. 138, 246–251.

    Article  PubMed  CAS  Google Scholar 

  45. Grossman, K. J., Goss, C. W. and Stein, D. G. (2004). Brain Res. 1008, 29–39.

    Article  PubMed  CAS  Google Scholar 

  46. He, J., Evans, C. O., Hoffman, S. W., Oyesiku, N. M., and Stein, D. G. (2004). Exp. Neurol. 189, 404–412.

    Article  PubMed  CAS  Google Scholar 

  47. Roof, R. L., Duvdevani, R., and Stein, D. L. (1993). Brain Res. 607, 333–336.

    Article  PubMed  CAS  Google Scholar 

  48. Gonzalez Deniselle, M. C., Lopez-Costa, J. J., Saavedra, J. P. et al. (2002). Neurobiol. Dis. 11, 457–468.

    Article  PubMed  CAS  Google Scholar 

  49. Chen, J., Chopp, M., and Li, Y. (1999). J. Neurol. Sci. 171, 24–30.

    Article  PubMed  CAS  Google Scholar 

  50. Jiang, N., Chopp, M., Stein, D., and Feit, H. (1996) Brain Res. 735, 101–107.

    Article  PubMed  CAS  Google Scholar 

  51. Murphy, S. J., Littleton-Kearney, M. T., and Hurn, P. D. (2002) J. Cereb. Blood Flow Metab. 22, 1181–1188.

    Article  PubMed  CAS  Google Scholar 

  52. Gibson, C. L., Constantin, D., Prior, M. J., Bath, P. M., and Murphy, S. P. (2005). Exp. Neurol. 193, 522–530.

    Article  PubMed  CAS  Google Scholar 

  53. Murphy, S. J., Traystman, R. J., Hurn, P. D., and Duckles, S. P. (2000). Stroke 31, 1173–1178.

    PubMed  CAS  Google Scholar 

  54. Miller, L., Alley, E. W., Murphy, W. J., Russell, S. W., and Hunt, J. S. (1996). J. Leuk. Biol. 59, 442–450.

    CAS  Google Scholar 

  55. Murphy, S., Simmons, M. L., Agullo, L. et al. (1993) Trends Neurosci. 16, 323–328.

    Article  PubMed  CAS  Google Scholar 

  56. Polan, M. L., Loukides, J., Nelson, P., et al. (1989). J. Clin. Endocrinol. Metab. 69, 1200–1206.

    PubMed  CAS  Google Scholar 

  57. Betz, A. L. (1986). Fed. Proc. 45, 2050–2054.

    PubMed  CAS  Google Scholar 

  58. Chaplin, E. R., Free, R. G., and Goldstein, G. W. (1981). Biochem. Pharmacol. 30, 241–245.

    Article  PubMed  CAS  Google Scholar 

  59. Herkes, G. K., Eadie, M. J., Sharbrough, F., and Moyer, T. (1993). Epilepsy Res. 15, 47–52.

    Article  PubMed  CAS  Google Scholar 

  60. Herzog, A. G., Klein, P., and Ransil, B. J. (1997). Epilepsia 38, 1082–1088.

    Article  PubMed  CAS  Google Scholar 

  61. Murri, L. and Galli, R. (1997). Cephalalgia 17 (Suppl. 20), 46–47.

    PubMed  Google Scholar 

  62. Beyenburg, S., Stoffel-Wagner, B., Bauer, J., et al. (2001). Epilepsy Res. 44, 141–153.

    Article  PubMed  CAS  Google Scholar 

  63. Bonuccelli, U., Melis, G. B., Paoletti, A. M., Fioretti, P., Murri, L., and Muratorio, A. (1989). Epilepsy Res. 3, 100–106.

    Article  PubMed  CAS  Google Scholar 

  64. Buterbaugh G. G. (1987). Pharmacol. Biochem. Behav. 28, 291–297.

    Article  PubMed  CAS  Google Scholar 

  65. Buterbaugh, G. G. (1989). Epilepsy Res. 4, 207–215.

    Article  PubMed  CAS  Google Scholar 

  66. Edwards, H. E., Burnham, W. M., Mendonca A., Bowlby, D. A., and MacLusky, N. J. (1999). Brain Res. 838, 136–150.

    Article  PubMed  CAS  Google Scholar 

  67. Hom, A. C., Leppik, I. E., and Rask, C. A. (1993). Neurology 43, 198–204.

    PubMed  CAS  Google Scholar 

  68. Hom, A. C. and Buterbaugh, G. G. (1986). Epilepsia 27, 103–108.

    PubMed  CAS  Google Scholar 

  69. Buterbaugh, G. G. and Hudson, G. M. (1991). Exp. Neurol. 111, 55–64.

    Article  PubMed  CAS  Google Scholar 

  70. Bauer, J. (2001). Epilepsia 42, 20–22.

    Article  PubMed  Google Scholar 

  71. Herzog, A. G. (1995). Neurology 45, 1660–1662.

    PubMed  CAS  Google Scholar 

  72. Holmes, G. L. and Weber, D. A. (1984). Dev. Brain Res. 16, 45–53.

    Article  CAS  Google Scholar 

  73. Kalviainen, R., Salmenpera, T., Partanen, K., Vainio, P., Riekkinen, P. and Pitkanen A. (1998). Neurology 50, 1377–1382.

    PubMed  CAS  Google Scholar 

  74. Mathern, G. W., Price, G., Rosales, C., Pretorius, J. K., Lozada, A., and Mendoza, D. (1998). Epilepsy Res. 30, 133–151.

    Article  PubMed  CAS  Google Scholar 

  75. Moshe, S. L. (1988). J. Child Neurol. 13 (Suppl. 1), S3–6; discussion S30-32.

    Google Scholar 

  76. Salmenpera, T., Kalviainen, R., Partanen, K., and Pitkanen, A. (2001). Epilepsy Res. 46, 69–82.

    Article  PubMed  CAS  Google Scholar 

  77. Tasch, E., Cendes, F., Li, L. M., Dubeau, F., Andermann, F., and Arnold, D. L. (1999). Ann. Neurol. 45, 568–576.

    Article  PubMed  CAS  Google Scholar 

  78. Gayoso, M. J., Primo, C., al-Majdalawj, A., Fernandez, J. M., Garrosa, M., and Iniguez, C. (1994). Brain Res. 653, 92–100.

    Article  PubMed  CAS  Google Scholar 

  79. Jarrard, L. E. and Meldrum, B. S. (1993). Neuropathol. Appl. Neurobiol. 19, 381–389.

    PubMed  CAS  Google Scholar 

  80. Lothman, E. W. and Collins, R. C. (1981). Brain Res. 218, 299–318.

    Article  PubMed  CAS  Google Scholar 

  81. Olney, J. W., Collins, R. C., and Sloviter, R. S. (1986). Adv. Neurol. 44, 857–877.

    PubMed  CAS  Google Scholar 

  82. Olney, J. W., Fuller, T., and de Gubareff, T. (1979). Brain Res. 176, 91–100.

    Article  PubMed  CAS  Google Scholar 

  83. Sperk, G., Lassmann, H., Baran, H., Kish, S. J., Seitelberger, F., and Hornykiewicz O. (1983). Neuroscience 10, 1301–1315.

    Article  PubMed  CAS  Google Scholar 

  84. Frye, C. A., Manjarrez, J., and Camacho-Arroyo, I. (2000). Brain Res. 881, 98–102.

    Article  PubMed  CAS  Google Scholar 

  85. Tauboll, E. and Lindstrom, S. (1993). Epilepsy Res. 14, 17–30.

    Article  PubMed  CAS  Google Scholar 

  86. Baulieu, E. E., Schumacher, M., Koenig, H., Jung-Testas, I., and Akwa, Y. (1996). Cell Mol. Neurobiol. 16, 143–154.

    Article  PubMed  CAS  Google Scholar 

  87. Frye, C. A. (1995). Brain Res. 696, 113–120.

    Article  PubMed  CAS  Google Scholar 

  88. Frye, C. A., Murphy R. E., and Platek, S. M. (2000). Behav. Brain Res. 115, 55–64.

    Article  PubMed  CAS  Google Scholar 

  89. Frye, C. A., Scalise, T. J., and Bayon, L. E. (1998). J. Neuroendocrinol. 10, 291–296.

    Article  PubMed  CAS  Google Scholar 

  90. Galli, R., Luisi, M., Pizzanelli, C. et al. (2001). Epilepsia 42, 216–219.

    Article  PubMed  CAS  Google Scholar 

  91. Barbaccia, M. L., Roscetti, G., Trabucchi, M., et al. (1996). Neuroendocrinology 63, 166–172.

    PubMed  CAS  Google Scholar 

  92. Friedman, L., Gibbs, T. T. and Farb, D. H. (1993). Mol. Pharmacol. 44, 191–197.

    PubMed  CAS  Google Scholar 

  93. Gulinello, M., Gong, Q. H., Li, X., and Smith, S. S. (2001). Brain Res. 910, 55–66.

    Article  PubMed  CAS  Google Scholar 

  94. Wohlfarth, K. M., Bianchi, M. T., and Macdonald, R. L. (2002). J. Neurosci. 22, 1541–1549.

    PubMed  CAS  Google Scholar 

  95. Azcoitia, I., Sierra, A., and Garcia-Segura, L. M. (1998). Neuroreport 9, 3075–3079.

    Article  PubMed  CAS  Google Scholar 

  96. Fujikawa, D. G., Shinmei, S. S., and Cai, B. (2000). Epilepsia 41, S9–13.

    Article  PubMed  Google Scholar 

  97. Kondo, T., Sharp, F. R., Honkaniemi, J., Mikawa, S., Epstein, C. J., and Chan, P. H. (1997). J. Cereb. Blood Flow Metab. 17, 241–256.

    Article  PubMed  CAS  Google Scholar 

  98. Kondratyev, A. and Gale, K. (2001). Neurosci. Lett. 310, 13–16.

    Article  PubMed  CAS  Google Scholar 

  99. Liu, W., Liu, R., Chun, J. T., et al. (2001). Brain Res. 916, 239–248.

    Article  PubMed  CAS  Google Scholar 

  100. Pollard, H., Cantagrel, S., Charriaut-Marlangue, C., Moreau, J., and Ben Ari, Y. (1994). Neuroreport 5, 1053–1055.

    Article  PubMed  CAS  Google Scholar 

  101. Pollard, H., Charriaut-Marlangue, C., Cantagrel, S., et al. (1994). Neuroscience 63, 7–18.

    Article  PubMed  CAS  Google Scholar 

  102. Venero, J. L., Revuelta, M., Machado, A., and Cano, J. (1999). Neuroscience 94, 1071–1081.

    Article  PubMed  CAS  Google Scholar 

  103. Gillardon, F., Wickert, H., and Zimmermann, M. (1995). Neurosci. Lett. 192, 85–88.

    Article  PubMed  CAS  Google Scholar 

  104. Choi, K. C., Kang, S. K., Tai, C. J., Auersperg, N., and Leung, P. C. (2001). Endocrinology 142, 2351–2360.

    Article  PubMed  CAS  Google Scholar 

  105. Harms, C., Lautenschlager, M., Bergk, A., et al. (2001). J. Neurosci. 21, 2600–2609.

    PubMed  CAS  Google Scholar 

  106. Pike, C. J. (1999). J. Neurochem. 72, 1552–1563.

    Article  PubMed  CAS  Google Scholar 

  107. Sawada, H., Ibi, M., Kihara, T., et al. (2000) FASEB J. 14, 1202–1214.

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  109. Bramlett, H. M. and Dietrich W. D. (2001). J. Neurotrauma 18, 891–900.

    Article  PubMed  CAS  Google Scholar 

  110. Roof, R. L., Duvdevani, R., Braswell, L., and Stein, D. G. (1994). Exp. Neurol. 129, 64–69.

    Article  PubMed  CAS  Google Scholar 

  111. Robertson, C. L., Puskar, A., Hoffman, G. E., Murphy, A. Z., Saraswati, M., and Fiskum, G. (2006). Exp. Neurol. 197, 235–243.

    Article  PubMed  CAS  Google Scholar 

  112. Cutler, S. M., Pettus, E. H., Hoffman, S. W., and Stein, D. G. (2005). Exp. Neurol. 195, 423–429.

    Article  PubMed  CAS  Google Scholar 

  113. Meffre, D., Delespierre, B., Gouezou, M. et al. (2005). J. Neurochem. 93, 1314–1326.

    Article  PubMed  CAS  Google Scholar 

  114. Suzuki, T., Bramlett, H. M., Ruenes, G., and Dietrich, W. D. (2004). J. Neurotrauma 21, 842–853.

    Article  PubMed  Google Scholar 

  115. Stein, D. G. and Hoffman S. W. (2003). Pediatr. Rehabil. 6, 13–22.

    Article  PubMed  Google Scholar 

  116. Perry, V. H., and Anthony, D. C. (1999). Philos. Trans. R. Soc. Lond. B Biol. Sci. 354, 1641–1647.

    Article  PubMed  CAS  Google Scholar 

  117. Peterson, J. W., Bo, L., Mork, S., Chang, A., and Trapp, B. D. (2001). Ann. Neurol. 50, 389–400.

    Article  PubMed  CAS  Google Scholar 

  118. Alcazar, A., Regidor, I., Masjuan, J., Salinas, M., and Alvarez-Cermeno, J. C. (1998). Neurosci. Lett. 255, 75–78.

    Article  PubMed  CAS  Google Scholar 

  119. Alcazar, A., Regidor, I., Masjuan, J., Salinas, M., and Alvarez-Cermeno, J. C. (2000). J. Neuroimmunol. 104, 58–67.

    Article  PubMed  CAS  Google Scholar 

  120. Oren, A., White, L. R., and Aasly, J. (2001) J. Neurol. Sci. 186, 31–36.

    Article  PubMed  CAS  Google Scholar 

  121. Whitacre, C. C. (2001). Nat. Immunol. 2, 777–780.

    Article  PubMed  CAS  Google Scholar 

  122. Duquette, P. and Girard, M. (1993). Curr. Opin. Neurol. Neurosurg. 6, 195–201.

    PubMed  CAS  Google Scholar 

  123. Runmarker, B. and Andersen, O. (1995). Brain 118, 253–261.

    Article  PubMed  Google Scholar 

  124. Siiteri, P. K. and Stites, D. P. (1982). Biol. Reprod. 26, 1–14.

    Article  PubMed  CAS  Google Scholar 

  125. Arnason, B. G. and Richman, D. P. (1969). Trans. Am. Neurol. Assoc. 94, 54–58.

    PubMed  CAS  Google Scholar 

  126. Bebo, B. F. Jr., Fyfe-Johnson, A., Adlard K., Beam, A. G., Vandenbark, A. A., and Offner, H. (2001). J. Immunol. 166, 2080–2089.

    PubMed  CAS  Google Scholar 

  127. Gilmore, W., Weiner, L. P., and Correale, J. (1997) J. Immunol. 158, 446–451.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  129. Kim, S., Liva, S. M., Dalal, M. A., Verity, M. A., and Voskuhl, R. R. (1999). Neurology 52, 1230–1238.

    Article  PubMed  CAS  Google Scholar 

  130. Marzi, M., Vigano, A., Trabattoni, D., et al., (1996). Clin. Exp. Immunol. 106, 127–133.

    Article  PubMed  CAS  Google Scholar 

  131. Trooster, W. J., Teelken, A. W., Gerrits, P. O., et al. (1996) Clin. Neurol. Neurosurg. 98, 222–226.

    Article  PubMed  CAS  Google Scholar 

  132. Piccinni, M. P., Giudizi, M. G., Biagiotti, R., et al. (1995) J. Immunol. 155, 128–133.

    PubMed  CAS  Google Scholar 

  133. Hoffman, G. E., Le, W. W., Murphy, A. Z., and Koski, C. L. (2001). Exp. Neurol. 171, 272–284.

    Article  PubMed  CAS  Google Scholar 

  134. Venters, H. D., Dantzer, R., and Kelley, K. W. (2000). Trends Neurosci. 23, 175–180.

    Article  PubMed  CAS  Google Scholar 

  135. Koski, C. L., Hila, S., and Hoffman, G. E. (2004) Endocrinology 145, 95–103.

    Article  PubMed  CAS  Google Scholar 

  136. Green, P. S. and Simpkins, J. W. (2000). Int. J. Dev. Neurosci. 18, 347–358.

    Article  PubMed  CAS  Google Scholar 

  137. Jellinger, K. A., and Bancher, C. (1998). J. Neural. Transm. Suppl. 54, 77–95.

    PubMed  CAS  Google Scholar 

  138. MacLusky, N. J., Chalmers-Redman, R., Kay, G., Ju, W., Nethrapalli, I. S., and Tatton, W. G. (2003). Neuroscience 118, 741–754.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  140. Formby, B. and Wiley, T. S. (1998). Ann. Clin. Lab. Sci. 28, 360–369.

    PubMed  CAS  Google Scholar 

  141. Gompel, A., Somai, S., Chaouat, M., et al. (2000). Steroids 65, 593–598.

    Article  PubMed  CAS  Google Scholar 

  142. Bernauer, S., Wehling, M., Gerdes, D., and Falkenstein, E. (2001). DNA Seq. 12, 13–25.

    PubMed  CAS  Google Scholar 

  143. Krippner-Heidenreich, A., Tubing, F., Bryde, S., Willi, S. Zimmermann, G., and Scheurich, P. (2002). J. Biol. Chem. 277, 44155–44163.

    Article  PubMed  CAS  Google Scholar 

  144. Littlejohn, A. F., Tucker, S. J., Mohamed, A. A. et al. (2003). Biochem. Pharmacol. 65, 91–99.

    Article  PubMed  CAS  Google Scholar 

  145. Mielke, K. and Herdegen, T. (2000). Prog. Neurobiol. 61, 45–60

    Article  PubMed  CAS  Google Scholar 

  146. reen, D. R. (1998). Cell 94, 695–698.

    Article  Google Scholar 

  147. Mielke, K. and Herdegen, T. (2002). Mol. Cell. Neurosci. 20, 211–224.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gloria E. Hoffman Ph.D..

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hoffman, G.E., Merchenthaler, I. & Zup, S.L. Neuroprotection by ovarian hormones in animal models of neurological disease. Endocr 29, 217–231 (2006). https://doi.org/10.1385/ENDO:29:2:217

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1385/ENDO:29:2:217

Key Words

Navigation