The role of estrogen and receptor agonists in maintaining organ function after trauma-hemorrhage

Shock

Volumn 31, Issue 3, 2009, Pages 227-237

  Yu, Huang Ping ^a,b   Chaudry, Irshad H ^c,d  

^a CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^b CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^c Kentucky   (United States)

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

Author keywords

Androgen receptors; Estrogen receptors; Sex; Shock

Indexed keywords

1,3,5 TRIS(4 HYDROXYPHENYL) 4 PROPYLPYRAZOLE; CELL ADHESION MOLECULE; CHEMOKINE; CYTOKINE; DIARYLPROPIONITRILE; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; FLUTAMIDE; FULVESTRANT; GENOMIC DNA; HEAT SHOCK PROTEIN; HEAT SHOCK TRANSCRIPTION FACTOR 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; PROPIONITRILE; SEX HORMONE; UNCLASSIFIED DRUG;

BLEEDING; DNA BINDING; DRUG RECEPTOR BINDING; HEART PROTECTION; HORMONE ACTION; HUMAN; INJURY; LIVER PROTECTION; NEUTROPHIL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SEX DIFFERENCE; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE; TISSUE SPECIFICITY; ANTIBODY SPECIFICITY; FEMALE; MALE; METABOLISM; MORTALITY; SEPSIS; SEXUAL DEVELOPMENT;

ESTROGENS; FEMALE; GONADAL STEROID HORMONES; HEMORRHAGE; HUMANS; MALE; ORGAN SPECIFICITY; RECEPTORS, ESTROGEN; SEPSIS; SEX CHARACTERISTICS; WOUNDS AND INJURIES;

EID: 62449166297     PISSN: 10732322     EISSN: None     Source Type: Journal    
DOI: 10.1097/SHK.0b013e31818347e7     Document Type: Review

References (140)

1. Kher A, Wang M, Tsai BM, Pitcher JM, Greenbaum ES, Nagy RD, Patel KM, Wairiuko GM, Markel TA, Meldrum DR: Sex differences in the myocardial inflammatory response to acute injury. Shock 23:1-10, 2005.
2. Hsieh YC, Choudhry MA, Yu HP, Shimizu T, Yang S, Suzuki T, Chen J, Bland KI, Chaudry IH: Inhibition of cardiac PGC-lalpha expression abolishes ERbeta agonist-mediated cardioprotection following trauma-hemorrhage. FASEB J 20:1109-1117, 2006.
3. Finnerty CC, Herndon DN, Chinkes DL, Jeschke MG: Serum cytokine differences in severely burned children with and without sepsis. Shock 27:4-9, 2007.
4. Choudhry MA, Schwacha MG, Hubbard WJ, Kerby JD, Rue LW, Bland KI, Chaudry IH: Gender differences in acute response to trauma-hemorrhage. Shock 24:101-106, 2005.
5. Hsieh YC, Yang S, Choudhry MA, Yu HP, Rue LW, III, Bland KI, Chaudry IH: PGC-1 upregulation via estrogen receptors: a common mechanism of salutary effects of estrogen and flutamide on heart function after trauma-hemorrhage. Am J Physiol Heart Circ Physiol 289:H2665-H2672, 2005.
6. Angele MK, Schwacha MG, Ayala A, Chaudry IH: Effect of gender and sex hormones on immune responses following shock. Shock 14:81-90, 2000.
7. Baue AE: A debate on the subject "Are SIRS and MODS important entities in the clinical evaluation of patients?" The con position. Shock 14:590-593, 2000.
8. Bruhn A, Verdant C, Vercruysse V, Su F, Vray B, Vincent JL: Effects of dexamethasone on macrophage migration inhibitory factor production in sepsis. Shock 26:169-173, 2006.
9. Rossaint R, Cerny V, Coats TJ, Duranteau J, Fernandez-Mondejar E, Gordini G, Stahel PF, Hunt BJ, Neugebauer E, Spahn DR: Key issues in advanced bleeding care in trauma. Shock 26:322-331, 2006.
10. Moore EE, Moore FA, Harken AH, Johnson JL, Ciesla D, Banerjee A: The two-event construct of postinjury multiple organ failure. Shock 24(Suppl 1): 71-74, 2005.
11. Holcomb JB, Jenkins D, Rhee P, Johannigman J, Mahoney P, Mehta S, Cox ED, Gehrke MJ, Beilman GJ, Schreiber M, et al.: Damage control resuscitation: directly addressing the early coagulopathy of trauma. J Trauma 62:307-310, 2007.
12. Kobbe P, Vodovotz Y, Kaczorowski D, Mollen KP, Billiar TR, Pape HC: Patterns of cytokine release and evolution of remote organ dysfunction after bilateral femur fracture. Shock 30:43-47, 2008.
13. Tsujimoto H, Ono S, Efron PA, Scumpia PO, Moldawer LL, Mochizuki H: Role of Toll-like receptors in the development of sepsis. Shock 29:315-321, 2008.
14. Cotton BA, Guy JS, Morris JA Jr, Abumrad NN: The cellular, metabolic, and systemic consequences of aggressive fluid resuscitation strategies. Shock 26:115-121, 2006.
15. Kamoun WS, Shin MC, Keller S, Karaa A, Huynh T, Clemens MG: Induction of biphasic changes in perfusion heterogeneity of rat liver after sequential stress in vivo. Shock 24:324-331, 2005.
16. Gauglitz GG, Song J, Herndon DN, Finnerty CC, Boehning DF, Barral JM, Jeschke MG: Characterization of the inflammatory response during acute and postacute phases after severe burn. Shock 30:503-507, 2008.
17. Murakami K, Enkhbaatar P, Yu YM, Traber LD, Cox RA, Hawkins HK. Tompkins RG, Herndon D, Traber DL: L-Arginine attenuates acute lung injury after smoke inhalation and burn injury in sheep. Shock 28: 477-483, 2007.
18. Acosta JA, Hoyt DB, Schmid-Schonbein GW, Hugli TE, Anjaria DJ, Frankel DA, Coimbra R: Intraluminal pancreatic serine protease activity, mucosal permeability, and shock: a review. Shock 26:3-9, 2006.
19. Yu M, Wang H, Ding A, Golenbock DT, Latz E, Czura CJ, Fenton MJ. Tracey KJ, Yang H: HMGB1 signals through Toll-like receptor (TLR) 4 and TLR2. Shock 26:174-179, 2006.
20. Wheeler DS, Lahni PM, Denenberg AG, Poynter SE, Wong HR, Cook JA, Zingarelli B: Induction of endotoxin tolerance enhances bacterial clearance and survival in murine polymicrobial sepsis. Shock 30:267-273, 2008.
21. + T cells. Shock 25:135-140, 2006.
22. Kawasaki T, Choudhry MA, Schwacha MG, Fujimi S, Lederer JA, Bland KI, Chaudry IH: Trauma-hemorrhage inhibits splenic dendritic cell proinflammatory cytokine production via a mitogen-activated protein kinase process. Am J Physiol Cell Physiol 294:C754-C764, 2008.
23. H1 immunity. Ann Surg 244:514-523, 2006.
24. Remick DG, Ward PA: Evaluation of endotoxin models for the study of sepsis. Shock 24(Suppl 1):7-11, 2005.
25. Hsieh YC, Yang S, Choudhry MA, Yu HP, Bland KI, Schwacha MG, Chaudry IH: Flutamide restores cardiac function after trauma-hemorrhage via an estrogen-dependent pathway through upregulation of PGC-1. Am J Physiol Heart Circ Physiol 290:H416-H423, 2006.
26. George RL, McGwin G Jr, Windham ST, Melton SM, Metzger J, Chaudry IH, Rue LW III: Age-related gender differential in outcome after blunt or penetrating trauma. Shock 19:28-32, 2003.
27. Hsieh YC, Yu HP, Suzuki T, Choudhry MA, Schwacha MG, Bland KI, Chaudry IH: Upregulation of mitochondrial respiratory complex IV by estrogen receptor-beta is critical for inhibiting mitochondrial apoptotic signaling and restoring cardiac functions following trauma-hemorrhage. J Mol Cell Cardiol 41:511-521, 2006.
28. Meldrum DR: Estrogen increases protective proteins following trauma and hemorrhage. Am J Physiol Regul Integr Comp Physiol 290:R809-R811, 2006.
29. Deitch EA, Feketeova E, Lu Q, Zaets S, Berezina TL, Machiedo GW, Hauser CJ, Livingston DH, Xu DZ: Resistance of the female, as opposed to the male, intestine to I/R-mediated injury is associated with increased resistance to gut-induced distant organ injury. Shock 29:78-83, 2008.
30. Sperry JL, Friese RS, Frankel HL, West MA, Cuschieri J, Moore EE, Harbrecht BG, Peitzman AB, Billiar TR, Maier RV, et al.: Male gender is associated with excessive IL-6 expression following severe injury. J Trauma 64:572-578, 2008.
31. Sharma R, Markel TA, Wang Y, Crisostomo PR, Wang M, Sando IC, Weil BR, Meldrum DR: Proestrus female rats are more resistant to right ventricular pressure overload. Shock 30:318-323, 2008.
32. Deitch EA, Senthil M, Brown M, Caputo F, Watkins A, Anjaria D, Badami C, Pisarenko V, Doucet D, Lu Q, et al.: Trauma-shock-induced gut injury and the production of biologically active intestinal lymph is abrogated by castration in a large animal porcine model. Shock 30:135-141, 2008.
33. Schroder J, Kahlke V, Book M, Stuber F: Gender differences in sepsis: genetically determined? Shock 14:307-310, 2000.
34. Frink M, Pape HC, van GM, Krettek C, Chaudry IH, Hildebrand F: Influence of sex and age on MODS and cytokines after multiple injuries. Shock 27: 151-156, 2007.
35. George RL, McGwin G Jr, Metzger J, Chaudry IH, Rue LW III: The association between gender and mortality among trauma patients as modified by age. J Trauma 54:464-471, 2003.
36. Yu HP, Hsieh YC, Suzuki T, Shimizu T, Choudhry MA, Schwacha MG, Chaudry IH: Salutary effects of estrogen receptor-beta agonist on lung injury after trauma-hemorrhage. Am J Physiol Lung Cell Mol Physiol 290: L1004-L1009, 2006.
37. Mostafa G, Huynh T, Sing RE, Miles WS, Norton HJ, Thomason MH: Gender-related outcomes in trauma. J Trauma 53:430-434, 2002.
38. Offner PJ, Moore EE, Biffl WL: Male gender is a risk factor for major infections after surgery. Arch Surg 134:935-938, 1999.
39. Gannon CJ, Pasquale M, Tracy JK, McCarter RJ, Napolitano LM: Male gender is associated with increased risk for postinjury pneumonia. Shock 21: 410-414, 2004.
40. Wichmann MW, Inthorn D, Andress HJ, Schildberg FW: Incidence and mortality of severe sepsis in surgical intensive care patients: the influence of patient gender on disease process and outcome. Intensive Care Med 26: 167-172, 2000.
41. Wohltmann CD, Franklin GA, Boaz PW, Luchette FA, Kearney PA, Richardson JD, Spain DA: A multicenter evaluation of whether gender dimorphism affects survival after trauma. Am J Surg 181:297-300, 2001.
42. Napolitano LM, Greco ME, Rodriguez A, Kufera JA, West RS, Scalea TM: Gender differences in adverse outcomes after blunt trauma. J Trauma 50: 274-280, 2001.
43. Eachempati SR, Hydo L, Barie PS: Gender-based differences in outcome in patients with sepsis. Arch Surg 134:1342-1347, 1999.
44. Gannon CJ, Napolitano LM, Pasquale M, Tracy JK, McCarter RJ: A statewide population-based study of gender differences in trauma: validation of a prior single-institution study. J Am Coll Surg 195:11-18, 2002.
45. Deitch EA, Livingston DH, Lavery RF, Monaghan SF, Bongu A, Machiedo GW: Hormonally active women tolerate shock-trauma better than do men: a prospective study of over 4000 trauma patients. Ann Surg 246:447-453, 2007.
46. Croce MA, Fabian TC, Malhotra AK, Bee TK, Miller PR: Does gender difference influence outcome? J Trauma 53:889-894, 2002.
47. Jarrar D, Wang P, Knoferl MW, Kuebler JF, Cioffi WG, Bland KI, Chaudry IH: Insight into the mechanism by which estradiol improves organ functions after trauma-hemorrhage. Surgery 128:246-252, 2000.
48. Yu HP, Yang S, Hsieh YC, Choudhry MA, Bland KI, Chaudry IH: Maintenance of lung myeloperoxidase activity in proestrus females after trauma-hemorrhage: upregulation of heme oxygenase-1. Am J Physiol Lung Cell Mol Physiol 291:L400-L406, 2006.
49. Schneider CP, Nickel EA, Samy TS, Schwacha MG, Cioffi WG, Bland KI, Chaudry IH: The aromatase inhibitor, 4-hydroxyandrostenedione, restores immune responses following trauma-hemorrhage in males and decreases mortality from subsequent sepsis. Shock 14:347-353, 2000.
50. Jarrar D, Wang P, Cioffi WG, Bland KI, Chaudry IH: The female reproductive cycle is an important variable in the response to trauma-hemorrhage. Am J Physiol Heart Circ Physiol 279:H1015-H1021, 2000.
51. Angele MK, Knoferl MW, Schwacha MG, Ayala A, Cioffi WG, Bland KI, Chaudry IH: Sex steroids regulate pro-and anti-inflammatory cytokine release by macrophages after trauma-hemorrhage. Am J Physiol 277: C35-C42, 1999.
52. Szalay L, Shimizu T, Suzuki T, Yu HP, Choudhry MA, Schwacha MG, Rue LW III, Bland KI, Chaudry IH: Estradiol improves cardiac and hepatic function after trauma-hemorrhage: role of enhanced heat shock protein expression. Am J Physiol Regul Integr Comp Physiol 290:R812-R818, 2006.
53. Kuebler JF, Jarrar D, Bland KI, Rue L, III, Wang P, Chaudry IH: Progesterone administration after trauma and hemorrhagic shock improves cardiovascular responses. Crit Care Med 31:1786-1793, 2003.
54. Wichmann MW, Angele MK, Ayala A, Cioffi WG, Chaudry IH: Flutamide: a novel agent for restoring the depressed cell-mediated immunity following soft-tissue trauma and hemorrhagic shock. Shock 8:242-248, 1997.
55. Lobo R: Menopause. In: Goldman L, Bennett J, eds.: Cecil Textbook of Medicine. Philadelphia, PA: W.B. Sanders Company, 1360-1366, 2000.
56. Katznelson L, Riskind PN, Saxe VC, Klibanski A: Prolactin pulsatile characteristics in postmenopausal women. J Clin Endocrinol Metab 83: 761-764, 1998.
57. Zellweger R, Wichmann MW, Ayala A, DeMaso CM, Chaudry IH: Prolactin: a novel and safe immunomodulating hormone for the treatment of immuno-depression following severe hemorrhage. J Surg Res 63:53-58, 1996.
58. Yang S, Choudhry MA, Hsieh YC, Hu S, Rue LW, III, Bland KI, Chaudry IH: Estrus cycle: influence on cardiac function following trauma-hemorrhage. Am J Physiol Heart Circ Physiol 291:H2807-H2815, 2006.
59. Frink M, Hsieh YC, Hsieh CH, Pape HC, Choudhry MA, Schwacha MG, Chaudry IH: Keratinocyte-derived chemokine plays a critical role in the induction of systemic inflammation and tissue damage after trauma-hemorrhage. Shock 28:576-581, 2007.
60. Yu HP, Shimizu T, Hsieh YC, Suzuki T, Choudhry MA, Schwacha MG, Chaudry IH: Tissue-specific expression of estrogen receptors and their role in the regulation of neutrophil infiltration in various organs following trauma-hemorrhage. / Leukoc Biol 79:963-970, 2006.
61. Gruber CJ, Tschugguel W, Schneeberger C, Huber JC: Production and actions of estrogens. N Engl J Med 346:340-352, 2002.
62. Yu HP, Choudhry MA, Shimizu T, Hsieh YC, Schwacha MG, Yang S, Chaudry IH: Mechanism of the salutary effects of flutamide on intestinal myeloperoxidase activity following trauma-hemorrhage: up-regulation of estrogen receptor-{beta}-dependent HO-1. J Leukoc Biol 79:277-284, 2006.
63. 2++ mobilization. Circ Res 81:885-892, 1997.
64. Lantin-Hermoso RL, Rosenfeld CR, Yuhanna IS, German Z, Chen Z, Shaul PW: Estrogen acutely stimulates nitric oxide synthase activity in fetal pulmonary artery endothelium. Am J Physiol 273:L119-L126, 1997.
65. Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson JA: Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138: 863-870, 1997.
66. Yang S, Choudhry MA, Hsieh YC, Hu S, Rue LW III, Bland KI, Chaudry IH: Estrus cycle: influence on cardiac function following trauma-hemorrhage. Am J Physiol Heart Circ Physiol 291.H2807-H2815, 2006.
67. Adams CA Jr, Hauser CJ, Adams JM, Fekete Z, Xu DZ, Sambol JT, Deitch EA: Trauma-hemorrhage-induced neutrophil priming is prevented by mesenteric lymph duct ligation. Shock 18:513-517, 2002.
68. Wu LL, Tang C, Liu MS: Altered phosphorylation and calcium sensitivity of cardiac myofibrillar proteins during sepsis. Am J Physiol Regul Integr Comp Physiol 281:R408-R416, 2001.
69. Malech HL, Gallin JI: Current concepts: immunology. Neutrophils in human diseases. N Engl J Med 317:687-694, 1987.
70. Angle N, Hoyt DB, Coimbra R, Liu F, Herdon-Remelius C, Loomis W, Junger WG: Hypertonic saline resuscitation diminishes lung injury by suppressing neutrophil activation after hemorrhagic shock. Shock 9:164-170, 1998.
71. Dayal SD, Hasko G, Lu Q, Xu DZ, Caruso JM, Sambol JT, Deitch EA: Trauma/hemorrhagic shock mesenteric lymph upregulates adhesion molecule expression and IL-6 production in human umbilical vein endothelial cells. Shock 17:491-195, 2002.
72. Shanley TP, Schmal H, Warner RL, Schmid E, Friedl HP, Ward PA: Requirement for C-X-C chemokines (macrophage inflammatory protein-2 and cytokine-induced neutrophil chemoattractant) in IgG immune complex-induced lung injury. J Immunol 158:3439-3448, 1997.
73. Iida M, Watanabe K, Tsurufuji M, Takaishi K, Iizuka Y, Tsurufuji S: Level of neutrophil chemotactic factor CINC/gro, a member of the interleukin-8 family, associated with lipopolysaccharide-induced inflammation in rats. Infect Immun 60:1268-1272, 1992.
74. Shimizu T, Yu HP, Suzuki T, Szalay L, Hsieh YC, Choudhry MA, Bland KI, Chaudry IH: The role of estrogen receptor subtypes in ameliorating hepatic injury following trauma-hemorrhage. J Hepatol 46:1047-1054, 2007.
75. Menezes JM, Hierholzer C, Watkins SC, Billiar TR, Peitzman AB, Harbrecht BG: The modulation of hepatic injury and heat shock expression by inhibition of inducible nitric oxide synthase after hemorrhagic shock. Shock 17:13-18, 2002.
76. Meldrum DR, Shenkar R, Sheridan BC, Cain BS, Abraham E, Harken AH: Hemorrhage activates myocardial NFkappaB and increases TNF-alpha in the heart. J Mol Cell Cardiol 29:2849-2854, 1997.
77. Kalaitzidis D, Gilmore TD: Transcription factor cross-talk: the estrogen receptor and NF-kappaB. Trends Endocrinol Metab 16:46-52, 2005.
78. Kushner PJ, Agard DA, Greene GL, Scanlan TS, Shiau AK, Uht RM, Webb P: Estrogen receptor pathways to AP-1. J Steroid Biochem Mol Biol 74:311-317, 2000.
79. Cuzzocrea S, Santagati S, Sautebin L, Mazzon E, Calabro G, Serraino I, Caputi AP, Maggi A: 17beta-Estradiol antiinflammatory activity in carrageenan-induced pleurisy. Endocrinology 141:1455-1463, 2000.
80. Kiang JG, Lu X, Tabaku LS, Bentley TB, Atkins JL, Tsokos GC: Resuscitation with lactated Ringer solution limits the expression of molecular events associated with lung injury after hemorrhage. J Appl Physiol 98: 550-556, 2005.
81. Hierholzer C, Harbrecht B, Menezes JM, Kane J, MacMicking J, Nathan CF, Peitzman AB, Billiar TR, Tweardy DJ: Essential role of induced nitric oxide in the initiation of the inflammatory response after hemorrhagic shock. J Exp Med 187:917-928, 1998.
82. Yu HP, Shimizu T, Choudhry MA, Hsieh YC, Suzuki T, Bland KI, Chaudry IH: Mechanism of cardioprotection following trauma-hemorrhagic shock by a selective estrogen receptor-beta agonist: up-regulation of cardiac heat shock factor-1 and heat shock proteins. J Mol Cell Cardiol 40:185-194, 2006.
83. Iafrati MD, Karas RH, Aronovitz M, Kim S, Sullivan TR Jr, Lubahn DB, O'Donnell TF Jr, Korach KS, Mendelsohn ME: Estrogen inhibits the vascular injury response in estrogen receptor alpha-deficient mice. Nat Med 3:545-548, 1997.
84. Lindner V, Kim SK, Karas RH, Kuiper GG, Gustafsson JA, Mendelsohn ME: Increased expression of estrogen receptor-beta mRNA in male blood vessels after vascular injury. Circ Res 83:224-229, 1998.
85. Gabel SA, Walker VR, London RE, Steenbergen C, Korach KS, Murphy E: Estrogen receptor beta mediates gender differences in ischemia/reperfusion injury. J Mol Cell Cardiol 38:289-297, 2005.
86. Wang JL, Ke DS, Lin MT: Heat shock pretreatment may protect against heatstroke-induced circulatory shock and cerebral ischemia by reducing oxidative stress and energy depletion. Shock 23:161-167, 2005.
87. Nakano M, Mann DL, Knowlton AA: Blocking the endogenous increase in HSP 72 increases susceptibility to hypoxia and reoxygenation in isolated adult feline cardiocytes. Circulation 95:1523-1531, 1997.
88. Szalay L, Shimizu T, Schwacha MG, Choudhry MA, Rue LW III, Bland KI, Chaudry IH: Mechanism of salutary effects of estradiol on organ function after trauma-hemorrhage: upregulation of heme oxygenase. Am J Physiol Heart Circ Physiol 289:H92-H98, 2005.
89. Nishizawa J, Nakai A, Komeda M, Ban T, Nagata K: Increased preload directly induces the activation of heat shock transcription factor 1 in the left ventricular overloaded heart. Cardiovasc Res 55:341-348, 2002.
90. Knowlton AA, Sun L: Heat-shock factor-1, steroid hormones, and regulation of heat-shock protein expression in the heart. Am J Physiol Heart Circ Physiol 280:H455-H464, 2001.
91. Voss MR, Stallone JN, Li M, Comelussen RN, Knuefermann P, Knowlton AA: Gender differences in the expression of heat shock proteins: the effect of estrogen. Am J Physiol Heart Circ Physiol 285:H687-H692, 2003.
92. Kumarapeli AR, Wang X: Genetic modification of the heart: chaperones and the cytoskeleton. J Mol Cell Cardiol 37:1097-1109, 2004.
93. Benjamin IJ, McMillan DR: Stress (heat shock) proteins: molecular chaperones in cardiovascular biology and disease. Circ Res 83:117-132, 1998.
94. Pandey P, Saleh A, Nakazawa A, Kumar S, Srinivasula SM, Kumar V, Weichselbaum R, Nalin C, Alnemri ES, Kufe D, et al.: Negative regulation of cytochrome c-mediated oligomerization of Apaf-1 and activation of procaspase-9 by heat shock protein 90. EMBO J 19:4310-1322, 2000.
95. Beere HM, Wolf BB, Cain K, Mosser DD, Mahboubi A, Kuwana T, Tailor P, Morimoto RI, Cohen GM, Green DR: Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat Cell Biol 2:469-475, 2000.
96. Lin KM, Lin B, Lian IY, Mestril R, Scheffler IE, Dillmann WH: Combined and individual mitochondrial HSP60 and HSP10 expression in cardiac myocytes protects mitochondrial function and prevents apoptotic cell deaths induced by simulated ischemia-reoxygenation. Circulation 103:1787-1792, 2001.
97. Kirchhoff SR, Gupta S, Knowlton AA: Cytosolic heat shock protein 60, apoptosis, and myocardial injury. Circulation 105:2899-2904, 2002.
98. Shi Y, Hutchins W, Ogawa H, Chang CC, Pritchard KA Jr, Zhang C, Khampang P, Lazar J, Jacob HJ, Rafiee P, et al.: Increased resistance to myocardial ischemia in the Brown Norway vs. Dahl S rat: role of nitric oxide synthase and Hsp90. J Mol Cell Cardiol 38:625-635, 2005.
99. Erol E, Kumar LS, Cline GW, Shulman GI, Kelly DP, Binas B: Liver fatty acid binding protein is required for high rates of hepatic fatty acid oxidation but not for the action of PPARalpha in fasting mice. FASEB J 18:347-349, 2004.
100. Herzig S, Long F, Jhala US, Hedrick S, Quinn R, Bauer A, Rudolph D, Schutz G, Yoon C, Puigserver P, et al.: CREB regulates hepatic gluconeo-genesis through the. coactivator PGC-1. Nature 413:179-183, 2001 101. Kanda N, Watanabe S: 17beta-Estradiol stimulates the growth of human keratinocytes by inducing cyclin D2 expression. J Invest Dermatol 123: 319-328, 2004.
101. Wade CB, Dorsa DM: Estrogen activation of cyclic adenosine 5'-monophosphate response element-mediated transcription requires the ex-tracellularly regulated kinase/mitogen-activated protein kinase pathway. Endocrinology 144:832-838, 2003.
102. Chen JQ, Eshete M, Alworth WL, Yager JD: Binding of MCF-7 cell mitochondrial proteins and recombinant human estrogen receptors alpha and beta to human mitochondrial DNA estrogen response elements. J Cell Biochem 93:358-373, 2004.
103. Imahara SD, Jelacic S, Junker CE, O'Keefe GE: The influence of gender on human innate immunity. Surgery 138:275-282, 2005.
104. Schneider CP, Schwacha MG, Chaudry IH: The role of interleukin-10 in the regulation of the systemic inflammatory response following trauma-hemorrhage. Biochim Biophys Acta 1689:22-32, 2004.
105. Diodato MD, Knoferl MW, Schwacha MG, Bland KI, Chaudry IH: Gender differences in the inflammatory response and survival following haemorrhage and subsequent sepsis. Cytokine 14:162-169, 2001.
106. Raju R, Bland KI, Chaudry IH: Estrogen: a novel therapeutic adjunct for the treatment of trauma-hemorrhage-induced immunological alterations. Mol Med 14:213-221, 2008.
107. Knoferl MW, Angele MK, Schwacha MG, Anantha Samy TS, Bland KI, Chaudry IH: Immunoprotection in proestrus females following trauma-hemorrhage: the pivotal role of estrogen receptors. Cell Immunol 222:27-34, 2003.
108. Suzuki T, Shimizu T, Yu HP, Hsieh YC, Choudhry MA, Bland KI, Chaudry IH: 17 beta-Estradiol administration following trauma-hemorrhage prevents the increase in Kupffer cell cytokine production and MAPK activation predominately via estrogen receptor-alpha. Surgery 140:141-148, 2006.
109. Suzuki T, Shimizu T, Yu HP, Hsieh YC, Choudhry MA, Bland KI, Chaudry IH: Estrogen receptor-alpha predominantly mediates the salutary effects of 17beta-estradiol on splenic macrophages following trauma-hemorrhage. Am J Physiol Cell Physiol 293:C978-C984, 2007.
110. Suzuki T, Shimizu T, Yu HP, Hsieh YC, Choudhry MA, Schwacha MG, Chaudry IH: Tissue compartment-specific role of estrogen receptor subtypes in immune cell cytokine production following trauma-hemorrhage. J Appl Physiol 102:163-168, 2007.
111. Suzuki T, Shimizu T, Yu HP, Hsieh YC, Choudhry MA, Chaudry IH: Salutary effects of 17beta-estradiol on T-cell signaling and cytokine production after trauma-hemorrhage are mediated primarily via estrogen receptor-alpha. Am J Physiol Cell Physiol 292:C2103-C2111, 2007.
112. Song RX: Membrane-initiated steroid signaling action of estrogen and breast cancer. Semin Reprod Med 25:187-197, 2007.
113. Govind AP, Thampan RV: Membrane associated estrogen receptors and related proteins: localization at the plasma membrane and the endoplasmic reticulum. Mol Cell Biochem 253:233-240, 2003.
114. Kuiper GG, Enmark E, Pelto-Huikko M, Nilsson S, Gustafsson JA: Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci U S A 93:5925-5930, 1996.
115. Hsieh YC, Frink M, Hsieh CH, Choudhry MA, Schwacha MG, Bland KI, Chaudry IH: Downregulation of migration inhibitory factor is critical for estrogen-mediated attenuation of lung tissue damage following trauma-hemorrhage. Am J Physiol Lung Cell Mol Physiol 292:L1227-L1232, 2007.
116. Yu HP, Hsieh YC, Suzuki T, Choudhry MA, Schwacha MG, Bland KI, Chaudry IH: The PI3K/Akt pathway mediates the nongenomic cardioprotective effects of estrogen following trauma-hemorrhage. Ann Surg 245: 971-977, 2007.
117. Yu HP, Hsieh YC, Suzuki T, Choudhry MA, Schwacha MG, Bland KI, Chaudry IH: Mechanism of the nongenomic effects of estrogen on intestinal myeloperoxidase activity following trauma-hemorrhage: up-regulation of the PI-3K/Akt pathway. J Leukoc Biol 82:774-780, 2007.
118. Ho KJ, Liao JK: Nonnuclear actions of estrogen. Arterioscler Thromh Vase Biol 22:1952-1961, 2002.
119. Yu HP, Shimizu T, Choudhry MA, Hsieh YC, Suzuki T, Bland KI, Chaudry IH: Mechanism of cardioprotection following trauma-hemorrhagic shock by a selective estrogen receptor-beta agonist: up-regulation of cardiac heat shock factor-1 and heat shock proteins. J Mol Cell Cardiol 40:185-194, 2006.
120. Razandi M, Pedram A, Greene GL, Levin ER: Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: studies of ERalpha and ERbeta expressed in Chinese hamster ovary cells. Mol Endocrinol 13: 307-319, 1999.
121. Revankar CM, Cimino DF, Sklar LA, Arterburn JB, Prossnitz ER: A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307:1625-1630, 2005.
122. Hsieh YC, Yu HP, Frink M, Suzuki T, Choudhry MA, Schwacha MG, Chaudry IH: G protein-coupled receptor 30-dependent protein kinase A pathway is critical in nongenomic effects of estrogen in attenuating liver injury after trauma-hemorrhage. Am J Pathol 170:1210-1218, 2007.
123. Guo Z, Krucken J, Benten WP, Wunderlich F: Estradiol-induced nongenomic calcium signaling regulates genotropic signaling in macrophages. J Biol Chem 277:7044-7050, 2002.
124. Kow LM, Pfaff DW: The membrane actions of estrogens can potentiate their lordosis behavior-facilitating genomic actions. Proc Natl Acad Sci U S A 101:12354-12357, 2004.
125. Stevis PE, Deecher DC, Suhandolnik L, Mallis LM, Frail DE: Differential effects of estradiol and estradiol-BSA conjugates. Endocrinology 140: 5455-5458, 1999.
126. Abraham IM, Han SK, Todman MG, Korach KS, Herbison AE: Estrogen receptor beta mediates rapid estrogen actions on gonadotropin-releasing hormone neurons in vivo. J Neurosci 23:5771-5777, 2003.
127. Honda K, Sawada H, Kihara T, Urushitani M, Nakamizo T, Akaike A, Shimohama S: Phosphatidylinositol 3-kinase mediates neuroprotection by estrogen in cultured cortical neurons. J Neurosci Res 60:321-327, 2000.
128. Hisamoto K, Ohmichi M, Kurachi H, Hayakawa J, Kanda Y, Nishio Y, Adachi K, Tasaka K, Miyoshi E, Fujiwara N, et al.: Estrogen induces the Akt-dependent activation of endothelial nitric-oxide synthase in vascular endothelial cells. J Biol Chem 276:3459-3467, 2001.
129. Cai Z, Semenza GL: Phosphatidylinositol-3-kinase signaling is required for erythropoietin-mediated acute protection against myocardial ischemia/ reperfusion injury. Circulation 109:2050-2053, 2004.
130. Fujio Y, Nguyen T, Wencker D, Kitsis RN, Walsh K: Akt promotes survival of cardiomyocytes in vitro and protects against ischemia-reperfusion injury in mouse heart. Circulation 101:660-667, 2000.
131. Haynes MP, Sinha D, Russell KS, Collinge M, Fulton D, Morales-Ruiz M, Sessa WC, Bender JR: Membrane estrogen receptor engagement activates endothelial nitric oxide synthase via the PI3-kinase-Akt pathway in human endothelial cells. Circ Res 87:677-682, 2000.
132. Matsui T, Tao J, del Monte F, Lee KH, Li L, Picard M, Force TL, Franke TF, Hajjar RJ, Rosenzweig A: Akt activation preserves cardiac function and prevents injury after transient cardiac ischemia in vivo. Circulation 104: 330-335, 2001.
133. Rajesh KG, Suzuki R, Maeda H, Yamamoto M, Yutong X, Sasaguri S: Hydrophilic bile salt ursodeoxycholic acid protects myocardium against re-perfusion injury in a PI3K/Akt dependent pathway. J Mol Cell Cardiol 39: 766-776, 2005.
134. Puri KD, Doggett TA, Douangpanya J, Hou Y, Tino WT, Wilson T, Graf T, Clayton E, Turner M, Hayflick JS, et al.: Mechanisms and implications of phosphoinositide 3-kinase delta in promoting neutrophil trafficking into inflamed tissue. Blood 103:3448-3456, 2004.
135. Cadwallader KA, Condliffe AM, McGregor A, Walker TR, White JF, Stephens LR, Chilvers ER: Regulation of phosphatidylinositol 3-kinase activity and phosphatidylinositol 3,4,5-trisphosphate accumulation by neutrophil priming agents. J Immunol 169:3336-3344, 2002.
136. Simoncini T, Hafezi-Moghadam A, Brazil DP, Ley K, Chin WW, Liao JK: Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 407:538-541, 2000.
137. Chen DB, Bird IM, Zheng J, Magness RR: Membrane estrogen receptor-dependent extracellular signal-regulated kinase pathway mediates acute activation of endothelial nitric oxide synthase by estrogen in uterine artery endothelial cells. Endocrinology 145:113-125, 2004.
138. Carrer HF, Cambiasso MJ, Gorosito S: Effects of estrogen on neuronal growth and differentiation. J Steroid Biochem Mol Biol 93:319-323, 2005.
139. Angele MK, Nitsch S, Knoferl MW, Ayala A, Angele P, Schildberg FW, Jauch KW, Chaudry IH: Sex-specific p38 MAP kinase activation following trauma-hemorrhage: involvement of testosterone and estradiol. Am J Physiol Endocrinol Metab 285:E189-E196, 2003.
140. Suzuki T, Yu HP, Hsieh YC, Choudhry MA, Bland KI, Chaudry IH: Estrogen-mediated activation of non-genomic pathway improves macrophages cytokine production following trauma-hemorrhage. J Cell Physiol 214: 662-672, 2008.