Estradiol after cardiac arrest and cardiopulmonary resuscitation is neuroprotective and mediated through estrogen receptor-β

Journal of Cerebral Blood Flow and Metabolism

Volumn 29, Issue 2, 2009, Pages 277-286

  Noppens, Ruediger R ^a,b   Kofler, Julia ^a,c   Grafe, Marjorie R ^a   Hurn, Patricia D ^a   Traystman, Richard J ^a,d,e  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF COLORADO   (United States)

Author keywords

Cardiac arrest; Cardiopulmonary resuscitation estradiol; Erebral ischemia; Estrogen receptor subtypes; Neuroprotection

Indexed keywords

1,3,5 TRIS(4 HYDROXYPHENYL) 4 PROPYLPYRAZOLE; DIARYLPROPIONITRILE; E 4389; ESTRADIOL; ESTROGEN RECEPTOR BETA; HORMONE RECEPTOR STIMULATING AGENT; SODIUM CHLORIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN INJURY; BRAIN NERVE CELL; CELL SURVIVAL; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; CORPUS STRIATUM; HEART ARREST; HIPPOCAMPUS; HISTOPATHOLOGY; LOADING DRUG DOSE; MALE; MOUSE; NEUROLOGIC DISEASE; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RESUSCITATION; SINGLE DRUG DOSE; TREATMENT OUTCOME;

ANIMALS; BODY TEMPERATURE; BODY WEIGHT; CARDIOPULMONARY RESUSCITATION; CENTRAL NERVOUS SYSTEM DISEASES; DISEASE MODELS, ANIMAL; ESTRADIOL; ESTROGEN RECEPTOR BETA; HEART ARREST; MALE; MICE; MICE, INBRED C57BL; NEUROPROTECTIVE AGENTS;

EID: 59149084122     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1038/jcbfm.2008.116     Document Type: Article

References (49)

1. Alkayed NJ, Harukuni I, Kimes AS, London ED, Traystman RJ, Hurn PD (1998) Gender-linked brain injury in experimental stroke. Stroke 29:159-65; discussion 166
2. Bernard SA, Gray TW, Buist MD, Jones BM, Silvester W, Gutheridge G, Smith K (2002) Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia. N Engl J Med 346:557-63
3. Bingham D, Macrae IM, Carswell HV (2005) Detrimental effects of 17beta-oestradiol after permanent middle cerebral artery occlusion. J Cereb Blood Flow Metab 25:414-20
4. Bottiger BW, Teschendorf P, Krumnikl JJ, Vogel P, Galmbacher R, Schmitz B, Motsch J, Martin E, Gass P (1999) Global cerebral ischemia due to cardiocirculatory arrest in mice causes neuronal degeneration and early induction of transcription factor genes in the hippocampus. Brain Res Mol Brain Res 65:135-42
5. Carswell HV, Bingham D, Wallace K, Nilsen M, Graham DI, Dominiczak AF, Macrae IM (2004a) Differential effects of 17beta-estradiol upon stroke damage in stroke prone and normotensive rats. J Cereb Blood Flow Metab 24:298-304
6. Carswell HV, Macrae IM, Gallagher L, Harrop E, Horsburgh KJ (2004b) Neuroprotection by a selective estrogen receptor beta agonist in a mouse model of global ischemia. Am J Physiol Heart Circ Physiol 287:H1501-4
7. Cobb LA, Fahrenbruch CE, Walsh TR (1999) Influence of cardiopulmonary resuscitation prior to defibrillation in patients with out-of-hospital ventricular defbrillation. JAMA 281:1182-8
8. Dubal DB, Zhu H, Yu J, Rau SW, Shughrue PJ, Merchenthaler I, Kindy MS, Wise PM (2001) Estrogen receptor alpha, not beta, is a critical link in estradiol-mediated protection against brain injury. Proc Natl Acad Sci USA 98:1952-7
9. Eisenberg MS, Mengert TJ (2001) Cardiac resuscitation. N Engl J Med 344:1304-13
10. Farr TD, Carswell HV, Gsell W, Macrae IM (2007) Estrogen receptor beta agonist diarylpropionitrile (DPN) does not mediate neuroprotection in a rat model of permanent focal ischemia. Brain Res 1185:275-82
11. Fugger HN, Foster TC, Gustafsson J, Rissman EF (2000) Novel effects of estradiol and estrogen receptor alpha and beta on cognitive function. Brain Res 883:258-64
12. Gibson CL, Gray LJ, Murphy SP, Bath PM (2006) Estrogens and experimental ischemic stroke: a systematic review. J Cereb Blood Flow Metab 26:1103-13
13. Gordon KB, Macrae IM, Carswell HV (2005) Effects of 17beta-oestradiol on cerebral ischaemic damage and lipid peroxidation. Brain Res 1036:155-62
14. Gulinello M, Lebesgue D, Jover-Mengual T, Zukin RS, Etgen AM (2006) Acute and chronic estradiol treatments reduce memory deficits induced by transient global ischemia in female rats. Horm Behav 49:246-60
15. Haider AH, Efron DT, Haut ER, Chang DC, Paidas CN, Cornwell EE, III (2007) Mortality in adolescent girls versus boys following traumatic shock: an analysis of the National Pediatric Trauma Registry. Arch Surg 142:875-80; discussion 879-880
16. Harris HA, Katzenellenbogen JA, Katzenellenbogen BS (2002) Characterization of the biological roles of the estrogen receptors, ERalpha and ERbeta, in estrogen target tissues in vivo through the use of an ERalpha-selective ligand. Endocrinology 143:4172-7
17. Harukuni I, Hurn PD, Crain BJ (2001) Deleterious effect of beta-estradiol in a rat model of transient forebrain ischemia. Brain Res 900:137-42
18. He Z, He YJ, Day AL, Simpkins JW (2002) Proestrus levels of estradiol during transient global cerebral ischemia improves the histological outcome of the hippocampal CA1 region: perfusion-dependent and -independent mechanisms. J Neurol Sci 193:79-87
19. Herlitz J, Rundqvist S, Bang A, Aune S, Lundstrom G, Ekstrom L, Lindkvist J (2001) Is there a difference between women and men in characteristics and outcome after in hospital cardiac arrest? Resuscitation 49:15-23
20. Hurn PD, Brass LM (2003) Estrogen and stroke: a balanced analysis. Stroke 34:338-41
21. Hurn PD, Littleton-Kearney MT, Kirsch JR, Dharmarajan AM, Traystman RJ (1995) Postischemic cerebral blood flow recovery in the female: effect of 17 beta-estradiol. J Cereb Blood Flow Metab 15:666-72
22. Jesmin S, Hattori Y, Sakuma I, Liu MY, Mowa CN, Kitabatake A (2003) Estrogen deprivation and replacement modulate cerebral capillary density with vascular expression of angiogenic molecules in middle-aged female rats. J Cereb Blood Flow Metab 23:181-9
23. Kim C, Fahrenbruch CE, Cobb LA, Eisenberg MS (2001) Out-of-hospital cardiac arrest in men and women. Circulation 104:2699-703
24. Kofler J, Hattori K, Sawada M, DeVries AC, Martin LJ, Hurn PD, Traystman RJ (2004) Histopathological and behavioral characterization of a novel model of cardiac arrest and cardiopulmonary resuscitation in mice. J Neurosci Methods 136:33-44
25. Kuppers E, Beyer C (1999) Expression of estrogen receptor-alpha and beta mRNA in the developing and adult mouse striatum. Neurosci Lett 276:95-8
26. Li X, Blizzard KK, Zeng Z, DeVries AC, Hurn PD, McCullough LD (2004) Chronic behavioral testing after focal ischemia in the mouse: functional recovery and the effects of gender. Exp Neurol 187:94-104
27. Lund TD, Rovis T, Chung WC, Handa RJ (2005) Novel actions of estrogen receptor-beta on anxiety-related behaviors. Endocrinology 146:797-807
28. May AK, Dossett LA, Norris PR, Hansen EN, Dorsett RC, Popovsky KA, Sawyer RG (2008) Estradiol is associated with mortality in critically ill trauma and surgical patients*. Crit Care Med 36:62-8
29. McCullough LD, Alkayed NJ, Traystman RJ, Williams MJ, Hurn PD (2001) Postischemic estrogen reduces hypoperfusion and secondary ischemia after experimental stroke. Stroke 32:796-802
30. McCullough LD, Hurn PD (2003) Estrogen and ischemic neuroprotection: an integrated view. Trends Endocrinol Metab 14:228-35
31. Meyers MJ, Sun J, Carlson KE, Marriner GA, Katzenellenbogen BS, Katzenellenbogen JA (2001) Estrogen receptor-beta potency-selective ligands: structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues. J Med Chem 44:4230-51
32. Mitra SW, Hoskin E, Yudkovitz J, Pear L, Wilkinson HA, Hayashi S, Pfaff DW, Ogawa S, Rohrer SP, Schaeffer JM, McEwen BS, Alves SE (2003) Immunolocalization of estrogen receptor beta in the mouse brain: comparison with estrogen receptor alpha. Endocrinology 144:2055-67
33. Noppens RR, Kofler J, Hurn PD, Traystman RJ (2005) Dose-dependent neuroprotection by 17beta-estradiol after cardiac arrest and cardiopulmonary resuscitation. Crit Care Med 33:1595-602
34. Phelan HA, Shafi S, Parks J, Maxson RT, Ahmad N, Murphy JT, Minei JP (2007) Use of a pediatric cohort to examine gender and sex hormone influences on outcome after trauma. J Trauma 63:1127-31
35. Polentini MS, Pirrallo RG, McGill W (2006) The changing incidence of ventricular fibrillation in Milwaukee, Wisconsin (1992-2002). Prehosp Emerg Care 10:52-60
36. Pulsinelli WA, Brierley JB, Plum F (1982) Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol 11:491-8
37. Rusa R, Alkayed NJ, Crain BJ, Traystman RJ, Kimes AS, London ED, Klaus JA, Hurn PD (1999) 17Beta-estradiol reduces stroke injury in estrogen-deficient female animals. Stroke 30:1665-70
38. Sampei K, Goto S, Alkayed NJ, Crain BJ, Korach KS, Traystman RJ, Demas GE, Nelson RJ, Hurn PD (2000) Stroke in estrogen receptor-alpha-deficient mice. Stroke 31:738-43
39. Sawada M, Alkayed NJ, Goto S, Crain BJ, Traystman RJ, Shaivitz A, Nelson RJ, Hurn PD (2000) Estrogen receptor antagonist ICI182,780 exacerbates ischemic injury in female mouse. J Cereb Blood Flow Metab 20:112-8
40. Shughrue P, Scrimo P, Lane M, Askew R, Merchenthaler I (1997) The distribution of estrogen receptor-beta mRNA in forebrain regions of the estrogen receptor-alpha knockout mouse. Endocrinology 138:5649-52
41. Simpkins JW, Rajakumar G, Zhang YQ, Simpkins CE, Greenwald D, Yu CJ, Bodor N, Day AL (1997) Estrogens may reduce mortality and ischemic damage caused by middle cerebral artery occlusion in the female rat. J Neurosurg 87:724-30
42. Stauffer SR, Coletta CJ, Tedesco R, Nishiguchi G, Carlson K, Sun J, Katzenellenbogen BS, Katzenellenbogen JA (2000) Pyrazole ligands: structure-affinity/activity relationships and estrogen receptor-alpha-selective agonists. J Med Chem 43:4934-47
43. Stirone C, Duckles SP, Krause DN (2003) Multiple forms of estrogen receptor-alpha in cerebral blood vessels: regulation by estrogen. Am J Physiol Endocrinol Metab 284:E184-92
44. Theodorsson A, Theodorsson E (2005) Estradiol increases brain lesions in the cortex and lateral striatum after transient occlusion of the middle cerebral artery in rats: no effect of ischemia on galanin in the stroke area but decreased levels in the hippocampus. Peptides 26:2257-64
45. Tunstall-Pedoe H, Morrison C, Woodward M, Fitzpatrick B, Watt G (1996) Sex differences in myocardial infarction and coronary deaths in the Scottish MONICA population of Glasgow 1985 to 1991. Presentation, diagnosis, treatment, and 28-day case fatality of 3991 events in men and 1551 events in women. Circulation 93:1981-92
46. Vergouwen MD, Anderson RE, Meyer FB (2000) Gender differences and the effects of synthetic exogenous and non-synthetic estrogens in focal cerebral ischemia. Brain Res 878:88-97
47. Wide JK, Hanratty K, Ting J, Galea LA (2004) High level estradiol impairs and low level estradiol facilitates non-spatial working memory. Behav Brain Res 155:45-53
48. Wigginton JG, Pepe PE, Bedolla JP, DeTamble LA, Atkins JM (2002) Sex-related differences in the presentation and outcome of out-of-hospital cardiopulmonary arrest: a multiyear, prospective, population-based study. Crit Care Med 30:S131-6
49. Yang SH, Shi J, Day AL, Simpkins JW (2000) Estradiol exerts neuroprotective effects when administered after ischemic insult. Stroke 31:745-9