Sex shapes experimental ischemic brain injury

Steroids

Volumn 75, Issue 11, 2010, Pages 754-759

  Cheng, Jian ^a   Hurn, Patricia D ^a,b  

^a Department of Anesthesiology and Perioperative Medicine ^*  (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Androgens; Cerebral ischemia; Sex; Sexual dimorphism; Stroke

Indexed keywords

ANDROGEN; ANDROSTANOLONE; AROMATASE INHIBITOR; SEX HORMONE; TESTOSTERONE;

BRAIN ISCHEMIA; CELL DEATH; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NEUROPROTECTION; NONHUMAN; REVIEW; RISK FACTOR; SEX; SEX DIFFERENCE; STROKE;

ANDROGENS; ANIMALS; BRAIN INJURIES; BRAIN ISCHEMIA; CELL DEATH; FEMALE; HUMANS; MALE; SEX CHARACTERISTICS; STROKE;

EID: 77955924371     PISSN: 0039128X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.steroids.2009.10.014     Document Type: Review

References (70)

1. C.L. Sudlow, and C.P. Warlow Comparable studies of the incidence of stroke and its pathological types: results from an international collaboration. International Stroke Incidence Collaboration Stroke 28 1997 491 499
2. M.R. Golomb, H.J. Fullerton, U. Nowak-Gottl, G. Deveber International Pediatric Stroke Study Group Male predominance in childhood ischemic stroke: findings from the international pediatric stroke study Stroke 40 2009 52 57
3. M. Giroud, C. Milan, P. Beuriat, P. Gras, E. Essayagh, and P. Arveux Incidence and survival rates during a two-year period of intracerebral and subarachnoid haemorrhages, cortical infarcts, lacunes and transient ischaemic attacks. The Stroke Registry of Dijon: 1985-1989 Int J Epidemiol 20 1991 892 899
4. R.L. Sacco, B. Boden-Albala, R. Gan, X. Chen, D.E. Kargman, and S. Shea Stroke incidence among white, black, and Hispanic residents of an urban community: the Northern Manhattan Stroke Study Am J Epidemiol 147 1998 259 268
5. M.J. Reeves, C.D. Bushnell, G. Howard, J.W. Gargano, P.W. Duncan, and G. Lynch Sex differences in stroke: epidemiology, clinical presentation, medical care, and outcomes Lancet Neurol 7 2008 915 926
6. P. Appelros, B. Stegmayr, and A. Terent Sex differences in stroke epidemiology: a systematic review Stroke 40 2009 1082 1090
7. M. Liu, S. Dziennis, P.D. Hurn, and N.J. Alkayed Mechanisms of gender-linked ischemic brain injury Restor Neurol Neurosci 27 2009 163 179
8. K. Vagnerova, I.P. Koerner, and P.D. Hurn Gender and the injured brain Anesth Analg 107 2008 201 214
9. J.T. Lang, and L.D. McCullough Pathways to ischemic neuronal cell death: are sex differences relevant? J Transl Med 6 2008 33
10. N.J. Alkayed, I. Harukuni, A.S. Kimes, E.D. London, R.J. Traystman, and P.D. Hurn Gender-linked brain injury in experimental stroke Stroke 29 1998 159 165 [discussion 166]
11. H.V. Carswell, N.H. Anderson, J.S. Clark, D. Graham, B. Jeffs, and A.F. Dominiczak Genetic and gender influences on sensitivity to focal cerebral ischemia in the stroke-prone spontaneously hypertensive rat Hypertension 33 1999 681 685
12. H. Cai, H. Yao, S. Ibayashi, H. Uchimura, and M. Fujishima Photothrombotic middle cerebral artery occlusion in spontaneously hypertensive rats: influence of substrain, gender, and distal middle cerebral artery patterns on infarct size Stroke 29 1998 1982 1986 [discussion 1986-7]
13. X. Li, K.K. Blizzard, Z. Zeng, A.C. DeVries, P.D. Hurn, and L.D. McCullough Chronic behavioral testing after focal ischemia in the mouse: functional recovery and the effects of gender Exp Neurol 187 2004 94 104
14. L.D. McCullough, Z. Zeng, K.K. Blizzard, I. Debchoudhury, and P.D. Hurn Ischemic nitric oxide and poly (ADP-ribose) polymerase-1 in cerebral ischemia: male toxicity, female protection J Cereb Blood Flow Metab 25 2005 502 512
15. Y. Yamori, R. Horie, H. Handa, M. Sato, and M. Fukase Pathogenetic similarity of strokes in stroke-prone spontaneously hypertensive rats and humans Stroke 7 1976 46 53
16. N.J. Alkayed, S.J. Murphy, R.J. Traystman, P.D. Hurn, and V.M. Miller Neuroprotective effects of female gonadal steroids in reproductively senescent female rats Stroke 31 2000 161 168
17. H.M. Bramlett, and W.D. Dietrich Neuropathological protection after traumatic brain injury in intact female rats versus males or ovariectomized females J Neurotrauma 18 2001 891 900
18. T.K. Toung, P.D. Hurn, R.J. Traystman, and F.E. Sieber Estrogen decreases infarct size after temporary focal ischemia in a genetic model of type 1 diabetes mellitus Stroke 31 2000 2701 2706
19. S.J. Vannucci, L.B. Willing, S. Goto, N.J. Alkayed, R.M. Brucklacher, and T.L. Wood Experimental stroke in the female diabetic, db/db, mouse J Cereb Blood Flow Metab 21 2001 52 60
20. F. Liu, R. Yuan, S.E. Benashski, and L.D. McCullough Changes in experimental stroke outcome across the life span J Cereb Blood Flow Metab 29 2009 792 802
21. K. Lieb, J. Andrae, I. Reisert, and C. Pilgrim Neurotoxicity of dopamine and protective effects of the NMDA receptor antagonist AP-5 differ between male and female dopaminergic neurons Exp Neurol 134 1995 222 229
22. L. Zhang, P.P. Li, X. Feng, J.L. Barker, S.V. Smith, and D.R. Rubinow Sex-related differences in neuronal cell survival and signaling in rats Neurosci Lett 337 2003 65 68
23. L. Du, H. Bayir, Y. Lai, X. Zhang, P.M. Kochanek, and S.C. Watkins Innate gender-based proclivity in response to cytotoxicity and programmed cell death pathway J Biol Chem 279 2004 38563 38570
24. M. Liu, P.D. Hurn, C.E. Roselli, and N.J. Alkayed Role of P450 aromatase in sex-specific astrocytic cell death J Cereb Blood Flow Metab 27 2007 135 141
25. M. Liu, E.A. Oyarzabal, R. Yang, S.J. Murphy, and P.D. Hurn A novel method for assessing sex-specific and genotype-specific response to injury in astrocyte culture J Neurosci Methods 171 2008 214 217
26. H. Li, S. Pin, Z. Zeng, M.M. Wang, K.A. Andreasson, and L.D. McCullough Sex differences in cell death Ann Neurol 58 2005 317 321
27. Y. Wang, V.L. Dawson, and T.M. Dawson Poly(ADP-ribose) signals to mitochondrial AIF: a key event in parthanatos Exp Neurol 218 2009 193 202
28. M.J. Eliasson, K. Sampei, A.S. Mandir, P.D. Hurn, R.J. Traystman, and J. Bao Poly(ADP-ribose) polymerase gene disruption renders mice resistant to cerebral ischemia Nat Med 3 1997 1089 1095
29. H. Hagberg, M.A. Wilson, H. Matsushita, C. Zhu, M. Lange, and M. Gustavsson PARP-1 gene disruption in mice preferentially protects males from perinatal brain injury J Neurochem 90 2004 1068 1075
30. C. Zhu, F. Xu, X. Wang, M. Shibata, Y. Uchiyama, and K. Blomgren Different apoptotic mechanisms are activated in male and female brains after neonatal hypoxia-ischaemia J Neurochem 96 2006 1016 1027
31. S. Renolleau, S. Fau, C. Goyenvalle, L.M. Joly, D. Chauvier, and E. Jacotot Specific caspase inhibitor Q-VD-OPh prevents neonatal stroke in P7 rat: a role for gender J Neurochem 100 2007 1062 1071
32. F. Liu, Z. Li, J. Li, C. Siegel, R. Yuan, and L.D. McCullough Sex differences in caspase activation after stroke Stroke 40 2009 1842 1848
33. M. Yuan, C. Siegel, Z. Zeng, J. Li, F. Liu, and L.D. McCullough Sex differences in the response to activation of the poly (ADP-ribose) polymerase pathway after experimental stroke Exp Neurol 217 2009 210 218
34. J. Li, and L.D. McCullough Sex differences in minocycline-induced neuroprotection after experimental stroke J Cereb Blood Flow Metab 29 2009 670 674
35. E.M. Park, S. Cho, K.A. Frys, S.B. Glickstein, P. Zhou, and J. Anrather Inducible nitric oxide synthase contributes to gender differences in ischemic brain injury J Cereb Blood Flow Metab 26 2006 392 401
36. H. Kitano, J.M. Young, J. Cheng, L. Wang, P.D. Hurn, and S.J. Murphy Gender-specific response to isoflurane preconditioning in focal cerebral ischemia J Cereb Blood Flow Metab 27 2007 1377 1386
37. P. Cordeau Jr., M. Lalancette-Hebert, Y.C. Weng, and J. Kriz Live imaging of neuroinflammation reveals sex and estrogen effects on astrocyte response to ischemic injury Stroke 39 2008 935 942
38. A. Sakata, M. Mogi, J. Iwanami, K. Tsukuda, L.J. Min, and T. Fujita Sex-different effect of angiotensin II type 2 receptor on ischemic brain injury and cognitive function Brain Res 2009 Epub Aug 31; doi:10.1016
39. W. Zhang, J.J. Iliff, C.J. Campbell, R.K. Wang, P.D. Hurn, and N.J. Alkayed Role of soluble epoxide hydrolase in the sex-specific vascular response to cerebral ischemia J Cereb Blood Flow Metab 29 2009 1475 1481
40. P.S. Herson, I.P. Koerner, and P.D. Hurn Sex, sex steroids, and brain injury Semin Reprod Med 27 2009 229 239
41. B.B. Yeap, Z. Hyde, O.P. Almeida, P.E. Norman, S.A. Chubb, and K. Jamrozik Lower testosterone levels predict incident stroke and transient ischemic attack in older men J Clin Endocrinol Metab 94 2009 2353 2359
42. M. Hollander, P.J. Koudstaal, M.L. Bots, D.E. Grobbee, A. Hofman, and M.M. Breteler Incidence, risk, and case fatality of first ever stroke in the elderly population. The Rotterdam Study J Neurol Neurosurg Psychiatry 74 3 2003 317 321
43. L.L. Jeppesen, H.S. Jorgensen, H. Nakayama, H.O. Raaschou, T.S. Olsen, and K. Winther Decreased serum testosterone in men with acute ischemic stroke Arterioscler Thromb Vasc Biol 16 1996 749 754
44. R.J. Dash, B.K. Sethi, K. Nalini, and S. Singh Circulating testosterone in pure motor stroke Funct Neurol 6 1991 29 34
45. M. Uchida, J.M. Palmateer, P.S. Herson, A.C. Devries, J. Cheng, and P.D. Hurn Dose-dependent effects of androgens on outcome after focal cerebral ischemia in adult male mice J Cereb Blood Flow Metab 29 2009 1454 1462
46. S.H. Yang, E. Perez, J. Cutright, R. Liu, Z. He, and A.L. Day Testosterone increases neurotoxicity of glutamate in vitro and ischemia-reperfusion injury in an animal model J Appl Physiol 92 2002 195 201
47. A. Caruso, V. Di Giorgi Gerevini, M. Castiglione, F. Marinelli, V. Tomassini, and C. Pozzilli Testosterone amplifies excitotoxic damage of cultured oligodendrocytes J Neurochem 88 2004 1179 1185
48. R. Orlando, A. Caruso, G. Molinaro, M. Motolese, F. Matrisciano, and G. Togna Nanomolar concentrations of anabolic-androgenic steroids amplify excitotoxic neuronal death in mixed mouse cortical cultures Brain Res 1165 2007 21 29
49. E. Ahlbom, G.S. Prins, and S. Ceccatelli Testosterone protects cerebellar granule cells from oxidative stress-induced cell death through a receptor mediated mechanism Brain Res 892 2001 255 262
50. C.J. Pike Testosterone attenuates beta-amyloid toxicity in cultured hippocampal neurons Brain Res 919 2001 160 165
51. T.V. Nguyen, M. Yao, and C.J. Pike Androgens activate mitogen-activated protein kinase signaling: role in neuroprotection J Neurochem 94 2005 1639 1651
52. T.V. Nguyen, M. Yao, and C.J. Pike Flutamide and cyproterone acetate exert agonist effects: induction of androgen receptor-dependent neuroprotection Endocrinology 148 2007 2936 2943
53. Y. Zhang, N. Champagne, L.K. Beitel, C.G. Goodyer, M. Trifiro, and A. LeBlanc Estrogen and androgen protection of human neurons against intracellular amyloid beta1-42 toxicity through heat shock protein 70 J Neurosci 24 2004 5315 5321
54. J. Hammond, Q. Le, C. Goodyer, M. Gelfand, M. Trifiro, and A. LeBlanc Testosterone-mediated neuroprotection through the androgen receptor in human primary neurons J Neurochem 77 2001 1319 1326
55. J.W. Gatson, and M. Singh Activation of a membrane-associated androgen receptor promotes cell death in primary cortical astrocytes Endocrinology 148 2007 2458 2464
56. T. Hawk, Y.Q. Zhang, G. Rajakumar, A.L. Day, and J.W. Simpkins Testosterone increases and estradiol decreases middle cerebral artery occlusion lesion size in male rats Brain Res 796 1998 296 298
57. S.H. Yang, R. Liu, Y. Wen, E. Perez, J. Cutright, and A.M. Brun-Zinkernagel Neuroendocrine mechanism for tolerance to cerebral ischemia-reperfusion injury in male rats J Neurobiol 62 2005 341 351
58. Y. Pan, H. Zhang, A.B. Acharya, P.H. Patrick, D. Oliver, and J.E. Morley Effect of testosterone on functional recovery in a castrate male rat stroke model Brain Res 1043 2005 195 204
59. J. Cheng, W. Hu, T.J. Toung, Z. Zhang, S.M. Parker, and C.E. Roselli Age-dependent effects of testosterone in experimental stroke J Cereb Blood Flow Metab. 29 2009 486 494
60. J. Cheng, N.J. Alkayed, and P.D. Hurn Deleterious effects of dihydrotestosterone on cerebral ischemic injury J. Cereb. Blood Flow Metab 27 2007 1553 1562
61. V.K. Patchev, J. Schroeder, F. Goetz, W. Rohde, and A.V. Patchev Neurotropic action of androgens: principles, mechanisms and novel targets Exp Gerontol 39 2004 1651 1660
62. L.L. DonCarlos, S. Sarkey, B. Lorenz, I. Azcoitia, D. Garcia-Ovejero, and C. Huppenbauer Novel cellular phenotypes and subcellular sites for androgen action in the forebrain Neuroscience 138 2006 801 807
63. S.H. Lee, M. Kim, B.W. Yoon, Y.J. Kim, S.J. Ma, and J.K. Roh Targeted hsp70.1 disruption increases infarction volume after focal cerebral ischemia in mice Stroke 32 2001 2905 2912
64. S. Rajdev, K. Hara, Y. Kokubo, R. Mestril, W. Dillmann, and P.R. Weinstein Mice overexpressing rat heat shock protein 70 are protected against cerebral infarction Ann Neurol 47 2000 782 791
65. V. Chisu, P. Manca, M. Zedda, G. Lepore, S. Gadau, and V. Farina Effects of testosterone on differentiation and oxidative stress resistance in C1300 neuroblastoma cells Neuro Endocrinol Lett 27 2006 807 812
66. J.W. Gatson, P. Kaur, and M. Singh Dihydrotestosterone differentially modulates the mitogen-activated protein kinase and the phosphoinositide 3-kinase/Akt pathways through the nuclear and novel membrane androgen receptor in C6 cells Endocrinology 147 2006 2028 2034
67. S. Kousteni, L. Han, J.R. Chen, M. Almeida, L.I. Plotkin, and T. Bellido Kinase-mediated regulation of common transcription factors accounts for the bone-protective effects of sex steroids J Clin Invest 111 2003 1651 1664
68. E. Unni, S. Sun, B. Nan, M.J. McPhaul, B. Cheskis, and M.A. Mancini Changes in androgen receptor nongenotropic signaling correlate with transition of LNCaP cells to androgen independence Cancer Res 64 2004 7156 7168
69. C. Fix, C. Jordan, P. Cano, and W.H. Walker Testosterone activates mitogen-activated protein kinase and the cAMP response element binding protein transcription factor in Sertoli cells Proc Natl Acad Sci USA 101 2004 10919 10924
70. C.J. Pike, T.V. Nguyen, M. Ramsden, M. Yao, M.P. Murphy, and E.R. Rosario Androgen cell signaling pathways involved in neuroprotective actions Horm Behav 53 2008 693 705