Sex differences in mechanisms and outcome of neonatal hypoxia-ischemia in rodent models: Implications for sex-specific neuroprotection in clinical neonatal practice

Neurology Research International

Volumn 2012, Issue , 2012, Pages

  Hill, Courtney A ^a   Fitch, R Holly ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84866170598     PISSN: 20901852     EISSN: 20901860     Source Type: Journal    
DOI: 10.1155/2012/867531     Document Type: Review

References (97)

1. Fatemi A., Wilson M. A., Johnston M. V., Hypoxic-ischemic encephalopathy in the term infant. Clinics in Perinatology 2009 36 4 835 858 2-s2.0-70450213256 10.1016/j.clp.2009.07.011
2. Boylan G. B., Young K., Panerai R. B., Rennie J. M., Evans D. H., Dynamic cerebral autoregulation in sick newborn infants. Pediatric Research 2000 48 1 12 17 2-s2.0-0033917037 (Pubitemid 30419165)
3. Volpe J. J., Hypoxic-ischemic encephalopathy and intracranial hemorrhage. Neurology of the Newborn 2001 Philadelphia, Pa, USA WB Saunders
4. Takashima S., Itoh M., Oka A., A history of our understanding of cerebral vascular development and pathogenesis of perinatal brain damage over the past 30 years. Seminars in Pediatric Neurology 2009 16 4 226 236 2-s2.0-70450285344 10.1016/j.spen.2009.09.004
5. Rice J. E. III, Vannucci R. C., Brierley J. B., The influence of immaturity on hypoxic-ischemic brain damage in the rat. Annals of Neurology 1981 9 2 131 141 2-s2.0-0019366919 (Pubitemid 11191192)
6. Vannucci R. C., Vannucci S. J., Perinatal hypoxic-ischemic brain damage: evolution of an animal model. Developmental Neuroscience 2005 27 24 81 86 2-s2.0-23244434256 10.1159/000085978 (Pubitemid 41096212)
7. Vannucci S. J., Hagberg H., Hypoxia-ischemia in the immature brain. Journal of Experimental Biology 2004 207, part 18 3149 3154 2-s2.0-4644236077 10.1242/jeb.01064 (Pubitemid 39275289)
8. Lotgering F. K., Bishai J. M., Struijk P. C., Blood A. B., Hunter C. J., Oberg K. C., Power G. G., Longo L. D., Absence of robust ischemic preconditioning by five 1-minute total umbilical cord occlusions in fetal sheep. Journal of the Society for Gynecologic Investigation 2004 11 7 449 456 2-s2.0-5344257560 10.1016/j.jsgi.2004.03.007 (Pubitemid 39349196)
9. Gonzalez H., Hunter C. J., Bennet L., Power G. G., Gunn A. J., Cerebral oxygenation during postasphyxial seizures in near-term fetal sheep. Journal of Cerebral Blood Flow and Metabolism 2005 25 7 911 918 2-s2.0-21344452096 10.1038/sj.jcbfm.9600087 (Pubitemid 40905618)
10. Mayoral S. R., Omar G., Penn A. A., Sex differences in a hypoxia model of preterm brain damage. Pediatric Research 2009 66 3 248 253 2-s2.0-70350446726 10.1203/PDR.0b013e3181b1bc34
11. Schwartz M. L., Vaccarino F., Chacon M., Li Yan W., Ment L. R., Stewart W. B., Chronic neonatal hypoxia leads to long term decreases in the volume and cell number of the rat cerebral cortex. Seminars in Perinatology 2004 28 6 379 388 2-s2.0-11144349071 10.1053/j.semperi.2004.10.009 (Pubitemid 40037564)
12. Barrett R. D., Bennet L., Davidson J., Dean J. M., George S., Emerald B. S., Gunn A. J., Destruction and reconstruction: hypoxia and the developing brain. Birth Defects Research Part CEmbryo Today 2007 81 3 163 176 2-s2.0-36048972633 10.1002/bdrc.20095 (Pubitemid 350086245)
13. Gunn A. J., Bennet L., Fetal hypoxia insults and patterns of brain injury: insights from animal models. Clinics in Perinatology 2009 36 3 579 593 2-s2.0-69249249242 10.1016/j.clp.2009.06.007
14. van Handel M., Swaab H., De Vries L. S., Jongmans M. J., Long-term cognitive and behavioral consequences of neonatal encephalopathy following perinatal asphyxia: a review. European Journal of Pediatrics 2007 166 7 645 654 2-s2.0-34249100023 10.1007/s00431-007-0437-8 (Pubitemid 46800741)
15. Silbereis J. C., Huang E. J., Back S. A., Rowitch D. H., Towards improved animal models of neonatal white matter injury associated with cerebral palsy. Disease Models and Mechanisms 2010 3 11-12 678 688 2-s2.0-78649289322 10.1242/dmm.002915
16. Sie L. T. L., van der Knaap M. S., Oosting J., De Vries L. S., Lafeber H. N., Valk J., MR patterns of hypoxic-ischemic brain damage after prenatal, perinatal or postnatal asphyxia. Neuropediatrics 2000 31 3 128 136 2-s2.0-0033915058 10.1055/s-2000-7496 (Pubitemid 30495436)
17. McLean C., Ferriero D., Mechanisms of hypoxic-ischemic injury in the term infant. Seminars in Perinatology 2004 28 6 425 432 2-s2.0-11144264169 10.1053/j.semperi.2004.10.005 (Pubitemid 40037569)
18. Northington F. J., Brief update on animal models of hypoxic-ischemic encephalopathy and neonatal stroke. ILAR Journal 2006 47 1 32 38 2-s2.0-29544443469 (Pubitemid 43013510)
19. Fotopoulos S., Pavlou K., Skouteli H., Papassotiriou I., Lipsou N., Xanthou M., Early markers of brain damage in premature low-birth-weight neonates who suffered from perinatal asphyxia and/or infection. Biology of the Neonate 2001 79 3-4 213 218 2-s2.0-0035079138 10.1159/000047094 (Pubitemid 32247089)
20. Allin M., Matsumoto H., Santhouse A. M., Nosarti C., Alasady M. H. S., Stewart A. L., Rifkin L., Murray R. M., Cognitive and motor function and the size of the cerebellum in adolescents born very pre-term. Brain 2001 124, part 1 60 66 2-s2.0-0035191265 (Pubitemid 32055989)
21. Isaacs E. B., Edmonds C. J., Chong W. K., Lucas A., Morley R., Gadian D. G., Brain morphometry and IQ measurements in preterm children. Brain 2004 127, part 12 2595 2607 2-s2.0-10344252360 10.1093/brain/awh300 (Pubitemid 39627369)
22. Casiro O. G., Moddemann D. M., Stanwick R. S., Panikkar-Thiessen V. K., Cowan H., Cheang M. S., Language development of very low birth weight infants and fullterm controls at 12 months of age. Early Human Development 1990 24 1 65 77 2-s2.0-0025123486 (Pubitemid 20344895)
23. Marlow N., Rose A. S., Rands C. E., Draper E. S., Neuropsychological and educational problems at school age associated with neonatal encephalopathy. Archives of Disease in Childhood: Fetal and Neonatal Edition 2005 90 5 F380 F387 2-s2.0-24044548649 10.1136/adc.2004.067520 (Pubitemid 41224071)
24. Steinman K. J., Gorno-Tempini M. L., Glidden D. V., Kramer J. H., Miller S. P., Barkovich A. J., Ferriero D. M., Neonatal watershed brain injury on magnetic resonance imaging correlates with verbal IQ at 4 years. Pediatrics 2009 123 3 1025 1030 2-s2.0-63149150133 10.1542/peds.2008-1203
25. Tioseco J. A., Aly H., Essers J., Patel K., El-Mohandes A. A. E., Male sex and intraventricular hemorrhage. Pediatric Critical Care Medicine 2006 7 1 40 44 2-s2.0-33646098428 10.1097/01.PCC.0000192341.67078.61
26. Donders J., Hoffman N. M., Gender differences in learning and memory after pediatric traumatic brain injury. Neuropsychology 2002 16 4 491 499 2-s2.0-0036791913 10.1037//0894-4105.16.4.491
27. Lauterbach M. D., Raz S., Sander C. J., Neonatal hypoxic risk in preterm birth infants: the influence of sex and severity of respiratory distress on cognitive recovery. Neuropsychology 2001 15 3 411 420 2-s2.0-0034822090 10.1037 (Pubitemid 32879004)
28. Raz S., Debastos A. K., Newman J. B., Batton D., Extreme prematurity and neuropsychological outcome in the preschool years. Journal of the International Neuropsychological Society 2010 16 1 169 179 2-s2.0-77149131829 10.1017/S1355617709991147
29. Costeloe K., Hennessy E., Gibson A. T., Marlow N., Wilkinson A. R., The EPICure study: outcomes to discharge from hospital for infants born at the threshold of viability. Pediatrics 2000 106 4 I 659 671 2-s2.0-0033781313
30. Gualtieri T., Hicks R. E., An immunoreactive theory of selective male affliction. Behavioral and Brain Sciences 1985 8 427 441
31. Kesler S. R., Ment L. R., Vohr B., Pajot S. K., Schneider K. C., Katz K. H., Ebbitt T. B., Duncan C. C., Makuch R. W., Reiss A. L., Volumetric analysis of regional cerebral development in preterm children. Pediatric Neurology 2004 31 5 318 325 2-s2.0-7044262244 10.1016/j.pediatrneurol.2004.06.008 (Pubitemid 39424196)
32. Rutter M., Caspi A., Moffitt T. E., Using sex differences in psychopathology to study causal mechanisms: unifying issues and research strategies. Journal of Child Psychology and Psychiatry and Allied Disciplines 2003 44 8 1092 1115 2-s2.0-0344513309 10.1111/1469-7610.00194 (Pubitemid 37461053)
33. Raz S., Lauterbach M. D., Hopkins T. L., Glogowski B. K., Porter C. L., Riggs W. W., Sander C. J., A female advantage in cognitive recovery from early cerebral insult. Developmental Psychology 1995 31 6 958 966 2-s2.0-21844504884
34. Hines M., Early androgen influences on human neural and behavioural development. Early Human Development 2008 84 12 805 807 2-s2.0-54949148269 10.1016/j.earlhumdev.2008.09.006
35. Christine Knickmeyer R., Baron-Cohen S., Fetal testosterone and sex differences. Early Human Development 2006 82 12 755 760 2-s2.0-33750605073 10.1016/j.earlhumdev.2006.09.014 (Pubitemid 44692408)
36. McCarthy M. M., Estradiol and the developing brain. Physiological Reviews 2008 88 1 91 124 2-s2.0-38349049457 10.1152/physrev.00010.2007
37. Yang S. H., Perez E., Cutright J., Liu R., He Z., Dayand A. L., Simpkins J. W., Testosterone increases neurotoxicity of glutamate in vitro and ischemia-reperfusion injury in an animal model. Journal of Applied Physiology 2002 92 1 195 201 2-s2.0-0036089716 (Pubitemid 34670006)
38. Du L., Bayir H., Lai Y., Zhang X., Kochanek P. M., Watkins S. C., Graham S. H., Clark R. S. B., Innate gender-based proclivity in response to cytotoxicity and programmed cell death pathway. Journal of Biological Chemistry 2004 279 37 38563 38570 2-s2.0-4644305774 10.1074/jbc.M405461200 (Pubitemid 39296010)
39. Rosen G. D., Herman A. E., Galaburda A. M., Sex differences in the effects of early neocortical injury on neuronal size distribution of the medial geniculate nucleus in the rat are mediated by perinatal gonadal steroids. Cerebral Cortex 1999 9 1 27 34 2-s2.0-0032916572 10.1093/cercor/9.1.27 (Pubitemid 29062017)
40. Hill C. A., Threlkeld S. W., Fitch R. H., roslyn.h.fitch@uconn.edu Early testosterone modulated sex differences in behavioral outcome following neonatal hypoxia ischemia in rats. International Journal of Developmental Neuroscience 2011 29 4 381 388 10.1016/j.ijdevneu.2011.03.005
41. Lang J. T., McCullough L. D., Pathways to ischemic neuronal cell death: are sex differences relevant? Journal of Translational Medicine 2008 6, article 33 2-s2.0-47749128919 10.1186/1479-5876-6-33 (Pubitemid 352025077)
42. Renolleau S., Fau S., Charriaut-Marlangue C., Gender-related differences in apoptotic pathways after neonatal cerebral ischemia. Neuroscientist 2008 14 1 46 52 2-s2.0-37749032239 10.1177/1073858407308889
43. Zhu C., Xu F., Wang X., Shibata M., Uchiyama Y., Blomgren K., Hagberg H., Different apoptotic mechanisms are activated in male and female brains after neonatal hypoxia-ischaemia. Journal of Neurochemistry 2006 96 4 1016 1027 2-s2.0-33645100937 10.1111/j.1471-4159.2005.03639.x
44. Hagberg H., Wilson M. A., Matsushita H., Zhu C., Lange M., Gustavsson M., Poitras M. F., Dawson T. M., Dawson V. L., Northington F., Johnston M. V., PARP-1 gene disruption in mice preferentially protects males from perinatal brain injury. Journal of Neurochemistry 2004 90 5 1068 1075 2-s2.0-4444383142 10.1111/j.1471-4159.2004.02547.x (Pubitemid 39167340)
45. Nijboer C. H. A., Groenendaal F., Kavelaars A., Hagberg H. H., Van Bel F., Heijnen C. J., Gender-specific neuroprotection by 2-iminobiotin after hypoxia-ischemia in the neonatal rat via a nitric oxide independent pathway. Journal of Cerebral Blood Flow and Metabolism 2007 27 2 282 292 2-s2.0-33846441658 10.1038/sj.jcbfm.9600342 (Pubitemid 46148455)
46. Renolleau S., Fau S., Goyenvalle C., Joly L. M., Chauvier D., Jacotot E., Mariani J., Charriaut-Marlangue C., Specific caspase inhibitor Q-VD-OPh prevents neonatal stroke in P7 rat: a role for gender. Journal of Neurochemistry 2007 100 4 1062 1071 2-s2.0-33846785574 10.1111/j.1471-4159.2006.04269.x (Pubitemid 46213929)
47. Deveraux Q. L., Reed J. C., IAP family proteinssuppressors of apoptosis. Genes and Development 1999 13 3 239 252 2-s2.0-0033082995
48. Deveraux Q. L., Takahashi R., Salvesen G. S., Reed J. C., X-linked IAP is a direct inhibitor of cell-death proteases. Nature 1997 388 6639 300 304 2-s2.0-0030810926 10.1038/40901 (Pubitemid 27317977)
49. Deveraux Q. L., Roy N., Stennicke H. R., Van Arsdale T., Zhou Q., Srinivasula S. M., Alnemri E. S., Salvesen G. S., Reed J. C., IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO Journal 1998 17 8 2215 2223 2-s2.0-0032522738 10.1093/emboj/17.8.2215 (Pubitemid 28171907)
50. Ferrer I., Planas A. M., Signaling of cell death and cell survival following focal cerebral ischemia: life and death struggle in the penumbra. Journal of Neuropathology and Experimental Neurology 2003 62 4 329 339 2-s2.0-0037384802 (Pubitemid 36403033)
51. Srinivasula S. M., Ashwell J. D., IAPs: what's in a name? Molecular Cell 2008 30 2 123 135 2-s2.0-43049091895 10.1016/j.molcel.2008.03.008 (Pubitemid 351626688)
52. Carrel L., Willard H. F., X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 2005 434 7031 400 404 2-s2.0-15244353967 10.1038/nature03479 (Pubitemid 40469185)
53. McCarthy M. M., Molecular aspects of sexual differentiation of the rodent brain. Psychoneuroendocrinology 1994 19 57 415 427 2-s2.0-0028285978 10.1016/0306-4530(94)90029-9 (Pubitemid 24214314)
54. Fitch R. H., Denenberg V. H., A role for ovarian hormones in sexual differentiation of the brain. Behavioral and Brain Sciences 1998 21 3 311 352 2-s2.0-0031671145 10.1017/S0140525X98001216 (Pubitemid 28435132)
55. Arnold A. P., Rissman E. F., De Vries G. J., Two perspectives on the origin of sex differences in the brain. Annals of the New York Academy of Sciences 2003 1007 176 188 2-s2.0-1342288018 10.1196/annals.1286.018 (Pubitemid 38253665)
56. Sakuma Y., Gonadal steroid action and brain sex differentiation in the rat. Journal of Neuroendocrinology 2009 21 4 410 414 2-s2.0-63549117299 10.1111/j.1365-2826.2009.01856.x
57. Arnold A. P., Sex chromosomes and brain gender. Nature Reviews Neuroscience 2004 5 9 701 708 2-s2.0-4344685681 10.1038/nrn1494 (Pubitemid 39150141)
58. Arnold A. P., Burgoyne P. S., Are XX and XY brain cells intrinsically different? Trends in Endocrinology and Metabolism 2004 15 1 6 11 2-s2.0-1042290510 10.1016/j.tem.2003.11.001 (Pubitemid 38198093)
59. Arnold A. P., Xu J., Grisham W., Chen X., Kim Y. H., Itoh Y., Minireview: sex chromosomes and brain sexual differentiation. Endocrinology 2004 145 3 1057 1062 2-s2.0-1442299160 10.1210/en.2003-1491 (Pubitemid 38280982)
60. MacLusky N. J., Philips A., Hurlburt C., Naftolin F., Estrogen formation in the developing rat brain: sex differences in aromatase activity during early post-natal life. Psychoneuroendocrinology 1985 10 3 355 361 2-s2.0-0022376599 (Pubitemid 16237745)
61. Weisz J., Ward I. L., Plasma testosterone and progesterone titers of pregnant rats, their male and female fetuses, and neonatal offspring. Endocrinology 1980 106 1 306 316 2-s2.0-0018921896 (Pubitemid 10212501)
62. Michael R. P., Bonsall R. W., Rees H. D., Sites at which testosterone may act as an estrogen in the brain of the male primate. Neuroendocrinology 1987 46 6 511 521 2-s2.0-0023572169 (Pubitemid 18015760)
63. Goto M., Hanley K. P., Marcos J., Wood P. J., Wright S., Postle A. D., Cameron I. T., Mason J. I., Wilson D. I., Hanley N. A., In humans, early cortisol biosynthesis provides a mechanism to safeguard female sexual development. Journal of Clinical Investigation 2006 116 4 953 960 2-s2.0-33645511061 10.1172/JCI25091
64. Konkle A. T. M., McCarthy M. M., Developmental time course of estradiol, testosterone, and dihydrotestosterone levels in discrete regions of male and female rat brain. Endocrinology 2011 152 1 223 235 2-s2.0-78650824047 10.1210/en.2010-0607
65. Nuñez J. L., nunezj@msu.edu McCarthy M. M., Androgens predispose males to GABAA-mediated excitotoxicity in the developing hippocampus. Experimental Neurology 2008 210 2 699 708 10.1016/j.expneurol.2008.01.001
66. Hawk T., Zhang Y. Q., Rajakumar G., Day A. L., Simpkins J. W., Testosterone increases and estradiol decreases middle cerebral artery occlusion lesion size in male rats. Brain Research 1998 796 1-2 296 298 2-s2.0-0032527057 10.1016/S0006-8993(98)00327-8 (Pubitemid 28343260)
67. Cheng J., Alkayed N. J., Hurn P. D., Deleterious effects of dihydrotestosterone on cerebral ischemic injury. Journal of Cerebral Blood Flow and Metabolism 2007 27 9 1553 1562 2-s2.0-34548142225 10.1038/sj.jcbfm.9600457 (Pubitemid 47301443)
68. Elwan O., Abdallah M., Issa I., Taher Y., El-Tamawy M., Hormonal changes in cerebral infarction in the young and elderly. Journal of the Neurological Sciences 1990 98 2-3 235 243 2-s2.0-0025112768 10.1016/0022-510X(90)90264-N (Pubitemid 20288818)
69. Jeppesen L. L., Jorgensen H. S., Nakayama H., Raaschou H. O., Olsen T. S., Winther K., Decreased serum testosterone in men with acute ischemic stroke. Arteriosclerosis, Thrombosis, and Vascular Biology 1996 16 6 749 754 (Pubitemid 26179363)
70. Cheng J., Hu W., Toung T. J., Zhang Z., Parker S. M., Roselli C. E., Hurn P. D., Age-dependent effects of testosterone in experimental stroke. Journal of Cerebral Blood Flow and Metabolism 2009 29 3 486 494 2-s2.0-61349084196 10.1038/jcbfm.2008.138
71. Lan W. C. J., Priestley M., Mayoral S. R., Tian L., Shamloo M., Penn A. A., apenn@stanford.edu Sex-specific cognitive deficits and regional brain volume loss in mice exposed to chronic, sublethal hypoxia. Pediatric Research 2011 70 1 15 20 10.1203/PDR.0b013e31821b98a3
72. Hill C. A., Threlkeld S. W., Rosen G. D., Fitch R. H., Sex differences in rapid auditory processing deficits associated with neonatal hypoxia-ischemia in rats. 2007. Society for Neuroscience
73. Hill C. A., Alexander M. L., McCullough L. D., Fitch R. H., Inhibition of X-linked inhibitor of apoptosis with embelin differentially affects male versus female behavioral outcome following neonatal hypoxia-ischemia in rats. Developmental Neuroscience. In press
74. Mayoral S. R., Omar G., Penn A. A., Sex differences in a hypoxia model of preterm brain damage. Pediatric Research 2009 66 3 248 253 2-s2.0-70350446726 10.1203/PDR.0b013e3181b1bc34
75. McCullough L. D., Hurn P. D., Estrogen and ischemic neuroprotection: an integrated view. Trends in Endocrinology and Metabolism 2003 14 5 228 235 2-s2.0-0038268485 10.1016/S1043-2760(03)00076-6 (Pubitemid 36841481)
76. Turtzo L. C., McCullough L. D., Sex differences in stroke. Cerebrovascular Diseases 2008 26 5 462 474 2-s2.0-52049127043 10.1159/000155983
77. Carswell H. V. O., Anderson N. H., Morton J. J., McCulloch J., Dominiczak A. F., Macrae I. M., Investigation of estrogen status and increased stroke sensitivity on cerebral blood flow after a focal ischemic insult. Journal of Cerebral Blood Flow and Metabolism 2000 20 6 931 936 2-s2.0-0034046443 (Pubitemid 30413676)
78. Yamori Y., Horie R., Sato M., Ohta K., Prophylactic trials for stroke in stroke prone SHR. Effect of sex hormones. Japanese Heart Journal 1976 17 3 404 406 2-s2.0-0017083393
79. Herson P. S., Koerner I. P., Hurn P. D., Sex, sex steroids, and brain injury. Seminars in Reproductive Medicine 2009 27 3 229 239 2-s2.0-67649643462 10.1055/s-0029-1216276
80. Liu F., Li Z., Li J., Siegel C., Yuan R., Mccullough L. D., Sex differences in caspase activation after stroke. Stroke 2009 40 5 1842 1848 2-s2.0-65549170958 10.1161/STROKEAHA.108.538686
81. Fitch R. H., Brown C. P., Tallal P., Rosen G. D., Effects of sex and MK-801 on auditory-processing deficits associated with developmental microgyric lesions in rats. Behavioral Neuroscience 1997 111 2 404 412 2-s2.0-0030890591 10.1037/0735-7044.111.2.404 (Pubitemid 27169330)
82. Peiffer A. M., Rosen G. D., Fitch R. H., Sex differences in rapid auditory processing deficits in microgyric rats. Developmental Brain Research 2004 148 1 53 57 2-s2.0-0742324446 10.1016/j.devbrainres.2003.09.020 (Pubitemid 38147804)
83. Introduction to apoptosis. 2003
84. Billiards S. S., Pierson C. R., Haynes R. L., Folkerth R. D., Kinney H. C., Is the late preterm infant more vulnerable to gray matter injury than the term infant? Clinics in Perinatology 2006 33 4 915 933 2-s2.0-33751534891 10.1016/j.clp.2006.10.003 (Pubitemid 44834646)
85. Johnston M. V., Ishida A., Ishida W. N., Matsushita H. B., Nishimura A., Tsuji M., Plasticity and injury in the developing brain. Brain and Development 2009 31 1 1 10 2-s2.0-57349115397 10.1016/j.braindev.2008.03.014
86. Yuan M., Siegel C., Zeng Z., Li J., Liu F., McCullough L. D., Sex differences in the response to activation of the poly (ADP-ribose) polymerase pathway after experimental stroke. Experimental Neurology 2009 217 1 210 218 2-s2.0-64249104435 10.1016/j.expneurol.2009.02.012
87. Cho B. B., Toledo-Pereyra L. H., Caspase-independent programmed cell death following ischemic stroke. Journal of Investigative Surgery 2008 21 3 141 147 2-s2.0-46649100324 10.1080/08941930802029945 (Pubitemid 351935711)
88. Mabley J. G., Horváth E. M., Murthy K. G. K., Zsengellér Z., Vaslin A., Benko R., Kollai M., Szabó C., szabocsaba@aol.com Gender differences in the endotoxin-induced inflammatory and vascular responses: potential role of poly(ADP-ribose) polymerase activation. Journal of Pharmacology and Experimental Therapeutics 2005 315 2 812 820 10.1124/jpet.105.090480 (Pubitemid 41500748)
89. McCullough L. D., Zeng Z., Blizzard K. K., Debchoudhury I., Hurn P. D., Ischemic nitric oxide and poly (ADP-ribose) polymerase-1 in cerebral ischemia: male toxicity, female protection. Journal of Cerebral Blood Flow and Metabolism 2005 25 4 502 512 2-s2.0-17044430692 10.1038/sj.jcbfm.9600059
90. Chiarugi A., Poly(ADP-ribosyl)ation and stroke. Pharmacological Research 2005 52 1 15 24 2-s2.0-19444364781 10.1016/j.phrs.2005.02.018 (Pubitemid 40725596)
91. Nikolovska-Coleska Z., Xu L., Hu Z., Tomita Y., Li P., Roller P. P., Wang R., Fang X., Guo R., Zhang M., Lippman M. E., Yang D., Wang S., Discovery of embelin as a cell-permeable, small-molecular weight inhibitor of XIAP through structure-based computational screening of a traditional herbal medicine three-dimensional structure database. Journal of Medicinal Chemistry 2004 47 10 2430 2440 2-s2.0-2342448582 10.1021/jm030420+ (Pubitemid 38580082)
92. Askalan R., Salweski R., Tuor U. I., Hutchison J., Hawkins C., X-linked inhibitor of apoptosis protein expression after ischemic injury in the human and rat developing brain. Pediatric Research 2009 65 1 21 26 2-s2.0-58149376280 10.1203/PDR.0b013e3181894a25
93. Russell J. C., Whiting H., Szuflita N., Hossain M. A., Nuclear translocation of X-linked inhibitor of apoptosis (XIAP) determines cell fate after hypoxia ischemia in neonatal brain. Journal of Neurochemistry 2008 106 3 1357 1370 2-s2.0-48249110961 10.1111/j.1471-4159.2008.05482.x
94. Wang X., Zhu C., Wang X., Hagberg H., Korhonen L., Sandberg M., Lindholm D., Blomgren K., X-linked inhibitor of apoptosis (XIAP) protein protects against caspase activation and tissue loss after neonatal hypoxia-ischemia. Neurobiology of Disease 2004 16 1 179 189 2-s2.0-2342536508 10.1016/j.nbd.2004. 01.014 (Pubitemid 38569809)
95. Vischioni B., van der Valk P., Span S. W., Kruyt F. A. E., Rodriguez J. A., Giaccone G., Expression and localization of inhibitor of apoptosis proteins in normal human tissues. Human Pathology 2006 37 1 78 86 2-s2.0-29044444557 10.1016/j.humpath.2005.09.022 (Pubitemid 41790506)
96. Harlin H., Birkey Reffey S., Duckett C. S., Lindsten T., Thompson C. B., Characterization of XIAP-deficient mice. Molecular and Cellular Biology 2001 21 10 3604 3608 2-s2.0-0035037802 10.1128/MCB.21.10.3604-3608.2001 (Pubitemid 32381796)
97. Arnold A. P., Chen X., What does the four core genotypes mouse model tell us about sex differences in the brain and other tissues? Frontiers in Neuroendocrinology 2009 30 1 1 9 2-s2.0-58049173922 10.1016/j.yfrne.2008.11.001