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Gender differences in neurological disease

Role of estrogens and cytokines

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Abstract

Increasing evidence suggests that inflammatory response may be a critical component of different brain pathologies. However, the role played by this reaction is not fully understood. The present findings suggest that neuroinflammtory mediators such as cytokines may be involved in a number of key steps in the pathological cascade of events leading to neuronal injury. This hypothesis is strongly supported by experimental and clinical observations indicating that inhibition of the inflammatory reaction correlates with less neuronal damage. Estrogens are thought to play a role in the sex difference observed in many neurological diseases with inflammatory components including stroke, Alzheimer's and Parkinson's diseases, multiple sclerosis, or amyotrophic lateral sclerosis. Clinical and experimental studies have established estrogen as a neuroprotective hormone in these diseases. However, the exact mechanisms involved in the neuroprotective effects of estrogens are still unclear. It is possible that the beneficial effects of these hormones may be dependent on their inhibitory activity on the inflammatory reaction associated with the above-mentioned brain pathologies. Here, we review the current clinical and experimental evidence with respect to the inflammation-modulating effects of estrogens as one potential explanatory factor for sexual dimorzphism in the prevalence of numerous neurological diseases.

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References

  1. Benveniste, E. N., Nguyen, V. T., and O'Keefe, G. M. (2001) Neurochem. Int. 39, 381–391.

    PubMed  CAS  Google Scholar 

  2. Kohutnicka, M. Lewandowska, E., Kurkowska-Jastrzebska, I., Czlonkowski, A., and Członkowska, A. (1999) Immunopharmacol. 39, 167–180.

    Google Scholar 

  3. De Simoni, M. G. Milia P., Barba, M., De Luigi, A., Parnetti, L., and Gallai, V. (2002) Clin. Exp. Hypertens. 24, 535–542.

    PubMed  Google Scholar 

  4. Kurkowska-Jastrzebska, I., Wronska, A., Kohutnicka, M. Czlonkowski, A., and Członkowska, A. (1999) Exp. Neurol. 156, 50–61.

    PubMed  CAS  Google Scholar 

  5. Collawn, J. F. and Benveniste, E. N. (1999). Microbes Infect. 11, 893–902.

    Google Scholar 

  6. Mrak, R. E., and Griffin, W. S. (2005) Neurobiol. Aging 26, 349–354.

    PubMed  CAS  Google Scholar 

  7. Moore, A. H. and O'Banion, M. K. (2002). Adv. Drug Deliv. Rev. 54, 1627–1656.

    PubMed  CAS  Google Scholar 

  8. Bodles, A. M. and Barger, S. W., (2004) Trends Neurosci. 27, 621–626.

    PubMed  CAS  Google Scholar 

  9. Quan N. and Herkenham, M. (2002) Histol. Histopathol. 17, 273–288.

    PubMed  CAS  Google Scholar 

  10. Szelenyi, J. (2001) Brain Res. Bull. 54, 329–338.

    PubMed  CAS  Google Scholar 

  11. Perry, V. H. (2004) Brain Behav. Immun. 18, 407–413.

    PubMed  CAS  Google Scholar 

  12. Marklund, N., Keck, C., Hoover, R., et al. (2005) Restor. Neurol. Neurosci. 23, 31–42.

    PubMed  CAS  Google Scholar 

  13. Hailer, N. P., Vogt, C., Korf, H. W., and Dehghani, F. (2005). Eur. J. Neurosci. 21, 2347–2360.

    PubMed  Google Scholar 

  14. Gomes-Leal W., Corkill, D. J., Freire, M. A., Picanco-Diniz, C. W., and Perry, V. H. (2004) Exp. Neurol. 190, 456–467.

    PubMed  CAS  Google Scholar 

  15. Craft, J. M., Watterson, D. M., Hirsch, E., and Van Eldik, L. J. (2005). J. Neuroinflammation 2, 15.

    PubMed  Google Scholar 

  16. Marquardt, L., Ruf, A., Mansmann, U., et al. (2005) J. Neurol. Sci. 15, 65–71.

    Google Scholar 

  17. Grammas, P., and Ovase, R. (2001) Neurobiol. Aging 22, 837–842.

    PubMed  CAS  Google Scholar 

  18. Hirsch, E. C., Hunot, S., and Hartmann, A. (2005). Parkinsonism Relat. Disord. 11 (Suppl. 1), S9-S15.

    PubMed  Google Scholar 

  19. Silberberg, D. (2001) Mult. Scler. 7, 1.

    PubMed  CAS  Google Scholar 

  20. Al-Shammri, S., Rawoot, P., Azizieh, F., et al. (2004). J. Neurol. Sci. 15, 21–27.

    Google Scholar 

  21. Barbeito, L. H., Pehar, M., Cassina, P., et al. (2004). Brain Res. Brain Res. Rev. 47, 263–274.

    PubMed  CAS  Google Scholar 

  22. Kurkowska-Jastrzebska, I., Litwin, T., Joniec, I., et al. (2004). Int. Immunopharmacol. 4, 1307–1318.

    PubMed  CAS  Google Scholar 

  23. Fahrig, T., Gerlach, I., and Horvath, E. (2005) Mol. Pharmacol. 67, 1544–1555.

    PubMed  CAS  Google Scholar 

  24. Gao, H. M., Liu, B., Zhang, W. and Hong, J. S. (2003) Trends Pharmacol. Sci. 24, 395–401.

    PubMed  CAS  Google Scholar 

  25. Youdim, M. B. and Buccafusco, J. J. (2005) J. Neural. Transm. 112, 519–537.

    PubMed  CAS  Google Scholar 

  26. Lei, D. L., Long, J. M., Hengemihle, J., et al. (2003). Neuroscience 121, 659–666.

    PubMed  CAS  Google Scholar 

  27. Ospina, J. A., Brevig, H. N., Krause, D. N., and Duckles, S. P. (2003) Am. J. Physiol. Heart Circ. Physiol. 286, H2010–2019.

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  29. Mor, G., Nilsen, J., Horvath, T., et al. (1999). J. Neurobiol. 40, 484–496.

    PubMed  CAS  Google Scholar 

  30. Wooten, G. F., Currie, L. J., Bovbjerg, V. E., Lee, J. K., and Patrie, J. (2004) J. Neurol. Neurosurg. Psychiatry 75, 637–639.

    PubMed  CAS  Google Scholar 

  31. Beeson, P. B. (1994). Am. J. Med. 96, 457–462.

    PubMed  CAS  Google Scholar 

  32. Hurn, P. and Brass, L. (2003) Stroke 34, 338–343.

    PubMed  Google Scholar 

  33. Dluzen, D. E. and McDermott, J. L. (2000). J. Gend. Specif. Med. 3, 36–42.

    PubMed  CAS  Google Scholar 

  34. Nordell, V. L., Scarborough, M. M., Buchanan, A. K., and Sohrabji, F. (2003) Neurobiol. Aging 24, 733–743.

    PubMed  CAS  Google Scholar 

  35. Mikkola, T. S. and St Clair, R. W. (2002). Maturitas 41, 313–319.

    PubMed  CAS  Google Scholar 

  36. Suuronen, T., Nuutinen, T., Huuskonen, J., Ojala, J., Thornell, A., and Salminen, A. (2005) Inflamm. Res. 54, 194–203.

    PubMed  CAS  Google Scholar 

  37. Sato, F., Ouchi, Y., Masuyama, A., et al. (1993) Calcif. Tissue Int. 53, 111–116.

    PubMed  CAS  Google Scholar 

  38. Bismar, H., Diel, I., Ziegler, R., and Pfeilschifter, J. (1995) J. Clin. Endocrinol. Metab. 80, 3351–3355.

    PubMed  CAS  Google Scholar 

  39. Cantatore, F. P., Loverro, G., Ingrosso A. M., Lacanna, R., Sassanelli, E., and Selvaggi, L. (1995) Clin. Rheumatol. 14, 157–160.

    PubMed  CAS  Google Scholar 

  40. Liao, S. L., Chen, W. Y., and Chen, C. J. (2002) Neurosci. Lett. 330, 159–162.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  42. Danel, L., Souweine, G., Monier, J. C., and Saez, S. (1983). J. Steroid. Biochem. 18, 559–563.

    PubMed  CAS  Google Scholar 

  43. Vegeto, E., Belcredito, S., Etteri, S., et al. (2003). Proc. Natl. Acad. Sci. USA 100, 9614–9619.

    PubMed  CAS  Google Scholar 

  44. Liu, X., Fan, X. L., Zhao, Y., et al.. (2005) J. Neurosci. Res. 81, 653–665.

    PubMed  CAS  Google Scholar 

  45. Hall, J. M., and McDonnell, D. P. (1999). Endocrinology 140, 5566–5578.

    PubMed  CAS  Google Scholar 

  46. Beato, M., and Klug, J. (2000) Hum. Reprod. Update 6, 225–236.

    PubMed  CAS  Google Scholar 

  47. Pottratz, S. T., Bellido, T., Mocharla, H., Crabb, D., and Manolagas, S. C. (1994). J. Clin. Invest. 93, 944–950.

    PubMed  CAS  Google Scholar 

  48. Fox, H. S., Bond, B. L., and Parslow, T. G. (1991). J. Immunol. 146, 4362–4367.

    PubMed  CAS  Google Scholar 

  49. Srivastava, S., Weitzmann, M. N., Cenci, S., Ross, F. P., Adler, S., and Pacifici, R. (1999). J. Clin. Invest. 104, 503–513.

    PubMed  CAS  Google Scholar 

  50. Mishra, J. P., Mishra, S., Gee, K., and Kumar, A. (2005). J. Biol. Chem. 280, 26825–26837.

    PubMed  CAS  Google Scholar 

  51. Scott, B. B., Zaratin, P. F., Gilmartin, A. G., et al. (2005). Biochem. Biophys. Res. Commun. 328, 409–414.

    PubMed  CAS  Google Scholar 

  52. An, J., Ribeiro, R. C., Webb, P., Gustafsson, J. A., Kushner, P. J., and Baxter, J. D. (1999) Proc. Natl. Acad. Sci. USA 96, 15161–15166.

    PubMed  CAS  Google Scholar 

  53. Galien, R., and Garcia, T. (1997) Nucleic Acids Res. 25, 2424–2429.

    PubMed  CAS  Google Scholar 

  54. Ghosh, S., May, M. J., and Kopp, E. B. (1998) Annu. Rev. Immunol. 16, 225–260.

    PubMed  CAS  Google Scholar 

  55. Boyce, B. F., Xing, L., Franzoso, G., and Siebenlist, U. (1999). Bone 25, 137–139.

    PubMed  CAS  Google Scholar 

  56. Wen, Y., Yang, S., Liu, R., et al. (2004) Brain Res. 1008, 147–154.

    PubMed  CAS  Google Scholar 

  57. Kalaitzidis, D., and Gilmore, T. D. (2005) Trends Endocrinol. Metab. 16, 46–52.

    PubMed  CAS  Google Scholar 

  58. Quaedackers, M. E., Van Den Brink, C. E., Wissink, S., and Schreurs, R. H. (2001) Endocrinology 142, 1156–1166.

    PubMed  CAS  Google Scholar 

  59. Sun, W. H., Keller, E. T., Stebler, B. S., and Ershler, W. B. (1998) Biochem. Biophys. Res. Commun. 244, 691–695.

    PubMed  CAS  Google Scholar 

  60. Waters, K. M., Rickard, D. J., Riggs, B. L., et al. (2001). J. Cell Biochem. 83, 448–462.

    PubMed  CAS  Google Scholar 

  61. Feldmann, M., Brennan, F. M., and Maini, R. (1996), Cell 85, 307–310.

    PubMed  CAS  Google Scholar 

  62. Sunyer, T., Lewis, J., Collin-Osdoby, P., and Osdoby, P. (1999) J. Clin. Invest. 103, 1409–1418.

    PubMed  CAS  Google Scholar 

  63. Ye, K., Dinarello, C. A. and Clark, B. D. (1993) Proc. Natl. Acad. Sci. USA 90, 2295–2299.

    PubMed  CAS  Google Scholar 

  64. Sims, J. E., Painter, S. L., and Gow, I. R. (1995). Cytokine 7, 483–490.

    PubMed  CAS  Google Scholar 

  65. Zhang, Z., Maier, B., Santen, R. J., and Song, R. X. (2002) Biochem. Biophys. Res. Commun. 294, 926–933.

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  67. Marsden, C. D. and Olanow, C. W. (1998) Ann. Neurol. 44, S189–196.

    PubMed  CAS  Google Scholar 

  68. Currie, L. J., Harrison, M. B., Trugman, J. M., Bennett, J. P., and Wooten, G. F. (2004) Arch. Neurol. 61, 886–888.

    PubMed  Google Scholar 

  69. Sandyk, R. (1989). Int. J. Neurosci. 45, 119–122.

    PubMed  CAS  Google Scholar 

  70. Saunders-Pullman, R., Gordon-Elliott, J., Parides, M., Fahn, S., Saunders, H. R., and Bressman, S. (1999) Neurology 52, 1417–1421.

    PubMed  CAS  Google Scholar 

  71. Ragonese, P., D'Amelio, M., Salemi, G., et al. (2004) Neurology, 62, 2010–2014.

    PubMed  CAS  Google Scholar 

  72. Brooks, W. J., Jarvis, M. F., and Wagner, G. C. (1989). Res. Commun. Subst. Abuse 10, 181–184.

    CAS  Google Scholar 

  73. Dluzen, D. E., McDermott, J. L., and Liu, B. (1996). Neurotoxicol. Teratol. 18, 603–606.

    PubMed  CAS  Google Scholar 

  74. Dluzen, D. E., McDermott, J. L., and Liu, B. (1996). J. Neurochem. 66, 658–666.

    PubMed  CAS  Google Scholar 

  75. Nagatsu, T. (2002). J. Neural. Transm. 109, 731–745.

    PubMed  CAS  Google Scholar 

  76. Nagatsu, T., Mogi, M., Ichinose, H., and Togari, A. (2000). J. Neural. Transm. Suppl. 58, 143–151.

    PubMed  Google Scholar 

  77. Muller, T., Blum-Degen, D., Przuntek, H., and Kuhn, W. (1998). Acta Neurol. Scand. 98, 142–144.

    PubMed  CAS  Google Scholar 

  78. Hunot, S., Dugas, N., Faucheux, B., et al., (1999). J. Neurosci. 19, 3440–3447.

    PubMed  CAS  Google Scholar 

  79. Chang, J. Y., Martin, D. P., and Johnson, E. M. (1990), J. Neurochem. 55, 436–445.

    PubMed  CAS  Google Scholar 

  80. Hammerberg, H., Lidman, O., Lundberg, C. et al. (2000). J. Neurosci. 20, 5283–5291.

    Google Scholar 

  81. Wandinger, K. P., Hagenah, J. M., Kluter, H., Rothermundt, M., Peters, M., and Vieregge, P. (1999). J. Neuroimmunol. 98, 214–220.

    PubMed  CAS  Google Scholar 

  82. Mizuta, I., Nishimura, M., Mizuta, E., Yamasaki, S., Ohta, M., and Kuno, S. (2001). J. Neurol. Neurosurg. Psychiatry 71, 818–819.

    PubMed  CAS  Google Scholar 

  83. Ciesielska, A., Joniec, I., Przybyłkowski, A., et al. (2003). Acta Neurobiolog. Exp. 63, 117–126.

    Google Scholar 

  84. Mandel, S., Grunblatt, E., and Youdim, M. (2000). J. Neural. Transm. Suppl. 60, 117–124.

    PubMed  Google Scholar 

  85. Ciesielska, A. and Czlonkowski, A. (2005) Pharmacol. Rep. 57, 4150.

    Google Scholar 

  86. Lawrence, C. B., Allan, S. M., and Rothwell, N. J. (1998) Eur. J. Neurosci. 10, 1188–1195.

    PubMed  CAS  Google Scholar 

  87. Hebert, G., Arsaut, J., Dantzer, R., and Demotes-Mainard, J. (2003), Neurosci. Lett. 349, 191–195.

    PubMed  CAS  Google Scholar 

  88. Bolin, L. M., Strycharska-Orczyk, I., Murray, R., Langston, J. W., and Di Monte, D. (2002). J. Neurochem. 83, 167–175.

    PubMed  CAS  Google Scholar 

  89. Hinkerohe, D., Smikalla, D., Haghikia, A., et al. (2005), Glia 52, 85–97.

    PubMed  Google Scholar 

  90. Tang, M. X., Jacobs, D., Stern Y., et al. (1996). Lancet 348, 429–432.

    PubMed  CAS  Google Scholar 

  91. Barness, L. L., Wilson, R. S., Bienias, J. J., Schneider, J. A., Evans, D. A., and Bennett, D. A. (2005). Arch. Gen. Psychiatry 62, 685–691.

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  93. Doraiswamy, P. M., Bieber, F., Kaiser, L., et al. (1997). Neurology 48, 1511–1517.

    PubMed  CAS  Google Scholar 

  94. Henderson, A. S., Easteal, S., Jorm, A. F., et al. (1995) Lancet 346, 1387–1390.

    PubMed  CAS  Google Scholar 

  95. Yaffe, K., Sawaya, G., Lieberburg, I., and Grady, D. (1998). JAMA 279, 688–695.

    PubMed  CAS  Google Scholar 

  96. Costa, M. M., Reus, V. I., Wolkowitz, O. M., Manfredi, F., and Lieberman, M., (1999). Biol. Psychiatry 46, 182–188.

    PubMed  CAS  Google Scholar 

  97. Henderson, V. W., Paganini-Hill, A., Miller, B. L., et al. (2000). Neurology 54, 295–301.

    PubMed  CAS  Google Scholar 

  98. Mulnard R. A., Cotman, C. W., Kawas, C., et al., (2000). JAMA 283, 1007–1015.

    PubMed  CAS  Google Scholar 

  99. Craig, M. C., Maki, P. M., and Murphy, D. G. M. (2005), Lancet Neurol. 4, 190–194.

    PubMed  Google Scholar 

  100. Webber, K. M., Casadesus, G., Marlatt, M. W. et al. (2005). Ann. NY Acad. Sci., 1052, 201–209.

    PubMed  CAS  Google Scholar 

  101. McGeer, E. G. and McGeer, P. L. (1997) Mov. Disord. 12, 855–860.

    PubMed  CAS  Google Scholar 

  102. Mrak, R.E., and Griffinbe, W. S. (2001) Neurobiol. Aging 22, 915–922.

    PubMed  CAS  Google Scholar 

  103. Rothwell, N. (2003). Brain Behav. Immun. 17, 152–157.

    PubMed  Google Scholar 

  104. Ciallella, J. R., Ikonomovic, M. D., Paljug, W. R., et al. (2002), J. Neurotrauma 19, 1555–1567.

    PubMed  Google Scholar 

  105. Wang, J., Tanila, H., Puolivali, J., Kadish, I., and Groen, T. (2003). Neurobiol. Dis. 14, 318–327.

    PubMed  CAS  Google Scholar 

  106. Morris, F., Shepherd, R., Denys, E. et al. (1993). J. Neurol. Sci. 118, 48–55.

    Google Scholar 

  107. Ono, S., Hu, J., Shimizu, N., Imai, T., and Nakagawa, H. (2001). J. Neurol. Sci. 187, 27–34.

    PubMed  CAS  Google Scholar 

  108. Sekizawa, T., Openshaw, H., Ohbo, K., Sugamura, K., Itoyama, Y., and Nilan, J. C. (1998). J. Neurol. Sci. 154, 194–199.

    PubMed  CAS  Google Scholar 

  109. Hensley, K., Fedynyshyn, J., Ferrell, S., et al. (2003). Neurobiol. Dis. 14, 74–80.

    PubMed  CAS  Google Scholar 

  110. Xie, Y., Weydt, P., Howland, D. S., Kliot, M., and Moller, T.. (2004). Neuroreport 15, 2513–2516.

    PubMed  CAS  Google Scholar 

  111. Weydt, P., Yuen, E.C., Ransom, B. R., and Moller, T., (2004). Glia 48, 179–182.

    PubMed  Google Scholar 

  112. Veldink, J. H., Bar, P. R., Joosten, E. A., Otten, M., Wokke, J. H., and van den Berg, L. H. (2003). Neuromuscul. Disord. 13, 737–743.

    PubMed  CAS  Google Scholar 

  113. Trieu, V. N., and Uskun, F. M. (1999). Biochem. Biophys. Res. Commun. 258, 685–688.

    PubMed  CAS  Google Scholar 

  114. Nakamizo, T., Urushitani, M., Inoue, R. et al. (2000). Neuroreport 11, 3493–3497.

    PubMed  CAS  Google Scholar 

  115. Rudnicki, S. A. (1999). J. Neurol. Sci. 169, 126–127.

    PubMed  CAS  Google Scholar 

  116. Runmarker, B., Martinsson, T., Wahlstrom, J., and Andersen, O. (1994). J. Neurol. 241, 385–390.

    PubMed  CAS  Google Scholar 

  117. Hensiek, A., Sawcer, S., Feakes, R., et al. (2002). J. Neurol. Neurosurg. 72, 184–187.

    CAS  Google Scholar 

  118. Hensiek, A., Roxburgh, R., Smilie, B., et al. (2003). J. Neuroimmunol. 143, 25–30.

    PubMed  CAS  Google Scholar 

  119. Cedlius, E. G., Harbo, H. F., Egeland, T., Vartal, F., Vandvik, B., and Spurkiand A., (2000). J. Neurol. Sci. 178, 132–135.

    Google Scholar 

  120. Confavreux, C., Hutchinson, M., Heurs, M. M., Cortinivis-Tourniare, P., and Moreau, T. (1998). N. Engl. J. Med. 39, 285–291.

    Google Scholar 

  121. Villard-Mackintosh, L. and Vessey, M. P. (1993). Comtraception 47, 161–168.

    CAS  Google Scholar 

  122. Offner, H. (2004). J. Neurosci. Res. 78, 603–624.

    PubMed  CAS  Google Scholar 

  123. Dalal, M., Kim, S., and Voskuhl, R. R. (1997). J. Immunol. 159, 3–6.

    PubMed  CAS  Google Scholar 

  124. Vranckx, R., Muylle, L., Cole, J., Moldenhaser, R., and Peetermans, M. (1986). Vox Sang 50, 220–222.

    PubMed  CAS  Google Scholar 

  125. Amadori, A., Zamarchi, R., De Silvestro, G., et al. (1995). Nat. Med., 1, 1279–1283.

    PubMed  CAS  Google Scholar 

  126. Pelfrey, C. M., Cotleur, A. C., Lee, J. C., and Rudick, R. A. (2002). J. Neuroimmunol. 130, 211–223.

    PubMed  CAS  Google Scholar 

  127. Wilcoxen, S. C., Kirkman, E., Dowdell, K. C., and Stohlman, S. A. (2000). J. Immunol. 164, 6237–6243.

    PubMed  CAS  Google Scholar 

  128. Nguyen, L. T., Ramanathan, M., Weinstock-Guttman, B., Baier, M., Brownscheidle, C., and jacobs, L. D. (2003). J. Neurol. Sci. 209, 93–99.

    PubMed  CAS  Google Scholar 

  129. Mirowska, D., Skierski, J., Paz, A., et al. (2003). J. Neurol. 250, 1229–1236.

    PubMed  CAS  Google Scholar 

  130. Ito, A., Bebo, B. F. Jr., Matejuk, A., et al. (2001), J. Immunol. 1, 542–552.

    Google Scholar 

  131. Matejuk, A., Adlard, K., Zamora, A., Silverman, M., Vandenbark, A. A., and Offner, H. (2001). J. Neurosci. Res. 65, 529–542.

    PubMed  CAS  Google Scholar 

  132. Bonita, R., (1992). Lancet 339, 342–344.

    PubMed  CAS  Google Scholar 

  133. 2002 Heart and Stroke Stautistical Update, American Heart Association; http://www.americanheart.org/statistics.

  134. Niewada, M., Kobayashi, A., Sandercock, P. A., Kaminski, B., and Członkowska, A. (2005). Neuroepidemiology 24, 123–138.

    PubMed  Google Scholar 

  135. Di Carlo, A., Lamassa, M., Baldereschi, M., et al. (2003). Stroke 34, 1114–1119.

    PubMed  Google Scholar 

  136. Murphy, S. J., McCullough, L. D., and Smith, J. M. (2004). ILAR J. 45, 147–159.

    PubMed  CAS  Google Scholar 

  137. Sudlow, C. L. M. and Warlow, C. P. (1997). Stroke 28, 491–499.

    PubMed  CAS  Google Scholar 

  138. Jerntorp, P., and Berglund, G. (1992). Stroke 23, 357–361.

    PubMed  CAS  Google Scholar 

  139. Ricci, S., Celani, M. G., La Rosa, F., et al. (1991). J. Neurol. Neurosurg. Psychiatry 54, 695–698.

    PubMed  CAS  Google Scholar 

  140. Sacco, R. L., Wolf, P. A., Kannel, W. B., and McNamara, P. M. (1982). Stroke 13, 290–295.

    PubMed  CAS  Google Scholar 

  141. Kannel, W. B., Hjortland, M. C., McNamara, P. M., and Gordon, T. (1976). Ann. Intern. Med. 85, 447–452.

    PubMed  CAS  Google Scholar 

  142. Wolf, P. A. (1990)., Stroke, 21(9 Suppl.), II4–6.

    PubMed  CAS  Google Scholar 

  143. Barker, W. H. and Mullooly, J. P. (1997). Stroke 28, 284–290.

    PubMed  CAS  Google Scholar 

  144. Mikkola, T. S. and Clarkson, T. B. (2002). Cardiovasc. Res. 53, 605–619.

    PubMed  CAS  Google Scholar 

  145. Sader, M. A., and Celermajer, D. S. (2002). Cardiovasc. Res. 53, 597–604.

    PubMed  CAS  Google Scholar 

  146. Cusa, C., and Mazzone, A. (2002). Drugs Today, 38, 699–712.

    PubMed  CAS  Google Scholar 

  147. Young, J. L., Libby, P., and Schonbeck, U. (2002), Thromb. Haemost. 88, 554–567.

    PubMed  CAS  Google Scholar 

  148. Chamorro, A., (2004). Cerebrovasc. Dis. 17 (Suppl. 3), 1–5.

    CAS  Google Scholar 

  149. Sukovich, D. A., Kauser, K., Shirley, F. D., DelVecchio, V., Halks-Miller, M., and Rubanyi, G. M. (1998)., Arterioscler. Thromb. Vasc. Biol. 18, 1498–1505.

    PubMed  CAS  Google Scholar 

  150. Elhage, R., Clamens, S., Besnard, S., et al. (2001). Atherosclerosis 156, 315–320.

    PubMed  CAS  Google Scholar 

  151. Whitman, S. C., Ravisankar, P., and Daugherty, A. (2002). J. Interferon Cytokine Res. 22, 661–670.

    PubMed  CAS  Google Scholar 

  152. Ayala, C., Croft, J. B., Greenlund, K. J., et al. (2002). Stroke 33, 1197–1201

    PubMed  Google Scholar 

  153. Glader, E. L., Stegmayr, B., Norrving B., et al. (2003). Stroke 34, 1970–1975.

    PubMed  Google Scholar 

  154. Wyller, T. B., Sodring, K. M., Sveen, U., Ljunggren, A. E., and Bautz-Holter, E. (1997). Clin. Rehabil. 11, 171–179.

    PubMed  CAS  Google Scholar 

  155. Ladecola, C. and Alexander, M. (2001). Curr. Opin. Neurol. 14, 89–94.

    Google Scholar 

  156. del Zoppo, G., Ginis, I., Hallenbeck, J. M., Iadecola, C., Wang, X., and Feuerstein, G. Z. (2000). Brain Pathol. 10, 92–112.

    Google Scholar 

  157. Zheng, Z. and Yenari, M. A. (2004). Neurol. Res. 26, 884–892.

    PubMed  CAS  Google Scholar 

  158. Zhai, Q. H., Futrell, N., and Chen, F. J. (1997). J. Neurol. Sci. 152, 119–124.

    PubMed  CAS  Google Scholar 

  159. Buttini, M., Appel, K., Sauter, A., Gebicke-Haerter, P. J., and Boddeke, H. W. (1996). Neuroscience 71, 1–16.

    PubMed  CAS  Google Scholar 

  160. Li, H. L., Kostulas, N., Huang, Y. M., et al. (2001). J. Neuroimmunol. 116, 5–14.

    PubMed  CAS  Google Scholar 

  161. Wang, X., Yue, T. I., Young, P. R., Barone, F. C., and Feuerstein, G. Z. (1995). J. Cereb. Blood Flow. Metab. 15, 166–171.

    PubMed  CAS  Google Scholar 

  162. Hill, J. K., Gunion-Rinker, L., Kulhanek, D., et al. (1999) Brain Res. 820, 45–54.

    PubMed  CAS  Google Scholar 

  163. Barone, F. C., Arvin, B., White, R. F., et al. (1997). Stroke 28, 1233–1244.

    PubMed  CAS  Google Scholar 

  164. Yamasaki, Y., Matsuura, N., Shozuhara, H., Onodera, H., Itoyama, Y., and Kogure, K. (1995). Stroke, 26, 676–681.

    PubMed  CAS  Google Scholar 

  165. Mulcahy, N. J., Ross, J., and Rothwell, N. J. (2003). Br. J. Pharmacol. 140, 471–476

    PubMed  CAS  Google Scholar 

  166. Relton, J. K., Martin, D., Thompson, R. C., and Russel, D. A. (1996). Exp. Neurol. 138, 206–213.

    PubMed  CAS  Google Scholar 

  167. Nawashiro, H., Martin, D., and Hallenbeck, J. M. (1997). J. Cereb. Blood Flow. Metab. 17, 229–232.

    PubMed  CAS  Google Scholar 

  168. Martin-Villalba, A., Hahne, M., Kleber, S., et al. (2001). Cell. Death Differ. 8, 679–686.

    PubMed  CAS  Google Scholar 

  169. Yang, G. Y., Gong, C., Qin, Z., Ye, W., Mao, Y., and Bertz, A. L. (1998). Neuroreport 9, 2131–2134.

    PubMed  CAS  Google Scholar 

  170. Dawson, D. A., Martin, D., and Hallenbeck, J. M. (1996). Neurosci. Lett. 218, 41–44.

    PubMed  CAS  Google Scholar 

  171. Loddick, S. A. and Rothwell, N. J. (1996). J. Cereb. Blood. Flow Metab. 16, 932–940.

    PubMed  CAS  Google Scholar 

  172. Martin, D., Chinookoswong, N., and Miller, G., (1994). Exp. Neurol. 130, 362–367.

    PubMed  CAS  Google Scholar 

  173. Vila, N., Castillo, J., Davalos, A., and Chamorro, A. (2000). Stroke 31, 2325–2329.

    PubMed  CAS  Google Scholar 

  174. Vila, N., Reverter, J. C., Yague, J., and Chamorro, A. (2000). J. Interferon. Cytokine Res. 20, 325–329.

    PubMed  CAS  Google Scholar 

  175. Zaremba, J., and Losy, J. (2002) Acta Neurol. Scand. 104, 288–295.

    Google Scholar 

  176. Kim, H. M., Shin, H. Y., Jeong, H. J., et al. (2000). J. Mol. Neurosci. 14, 191–196.

    PubMed  Google Scholar 

  177. Grau, A. J., Reis, A., and Buggle, F (2001). J. Neurol. Sci. 15, 41–47.

    Google Scholar 

  178. Smith, C. J., Emsley, H. C., Gavin, C. M., et al. (2004). BMC Neurol., 4, 2–9.

    PubMed  Google Scholar 

  179. Su-Lan, L., Wen-Yin, Ch., and Chun-Jung, Ch. (2002). Neurosci. Lett. 330, 159–162.

    Google Scholar 

  180. Ospina, J. A., Brevig, H. N., Krause, D. N., and Duckles, S. P. (2004). Am. J. Physiol. Heart Circ. Physiol. 286, H2010-H2019.

    PubMed  CAS  Google Scholar 

  181. Nogawa, S., Zhang, F., Ross, M. E., and Iadecola, C. (1997). J. Neurosci. 17, 2746–2755.

    PubMed  CAS  Google Scholar 

  182. Terry, C. F., Loukaci, V., and Green, F. R. (2000). J. Biol. Chem. 275, 18138–18144.

    PubMed  CAS  Google Scholar 

  183. Olivieri, F., Bonafe, M., Cavallone, L., et al. (2002). Exp. Gerontol. 37, 309–314.

    PubMed  CAS  Google Scholar 

  184. Gromadzka, G., Sarzynska-Dlugosz, I., Ciesielska, A., and Członkowska, A. (2002). Eur. J. Neurol. 9(Suppl. 2), 25.

    Google Scholar 

  185. Bonafe, M., Olivieri, F., Cavallone, L., et al. (2001). Eur. J. Immunol., 31, 2357–2361.

    PubMed  CAS  Google Scholar 

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Członkowska, A., Ciesielska, A., Gromadzka, G. et al. Gender differences in neurological disease. Endocr 29, 243–256 (2006). https://doi.org/10.1385/ENDO:29:2:243

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