Mechanism of the anti-inflammatory effect of 17β-estradiol on brain following trauma-hemorrhage

Shock

Volumn 33, Issue 1, 2010, Pages 43-48

  Akabori, Hiroya ^a   Moeinpour, Fariba ^a   Bland, Kirby I ^a   Chaudry, Irshad H ^a  

^a Kentucky   (United States)

Author keywords

CNS; Female sex hormone; Microglia; Minocycline; TNF

Indexed keywords

CYCLODEXTRIN; CYTOKINE; ESTRADIOL; MINOCYCLINE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLOOD LEVEL; BRAIN HEMORRHAGE; BRAIN INJURY; BRAIN TISSUE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CYTOKINE PRODUCTION; FLOW CYTOMETRY; HORMONE ACTION; HYPOTHALAMUS; IMMUNE RESPONSE; INFLAMMATION; LAPAROTOMY; MACROPHAGE; MALE; MICROGLIA; NONHUMAN; PLASMA; RAT; RESUSCITATION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BRAIN; CELLS, CULTURED; ENZYME-LINKED IMMUNOSORBENT ASSAY; ESTRADIOL; FLOW CYTOMETRY; HEMORRHAGE; MALE; MICROGLIA; RATS; RATS, SPRAGUE-DAWLEY; TUMOR NECROSIS FACTOR-ALPHA;

EID: 73849116159     PISSN: 10732322     EISSN: None     Source Type: Journal    
DOI: 10.1097/SHK.0b013e3181b0ebcb     Document Type: Article

References (42)

1. Deitch EA, Shi HP, Lu Q, Feketeova E, Xu DZ: Serine proteases are involved in the pathogenesis of trauma-hemorrhagic shock-induced gut and lung injury. Shock 19:452-456, 2003.
2. 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.
3. Hopkins SJ: Central nervous system recognition of peripheral inflammation: a neural, hormonal collaboration. Acta Biomed 78(Suppl 1):231-247, 2007.
4. Turnbull AV, Rivier CL: Regulation of the hypothalamic-pituitary-adrenal axis by cytokines: actions and mechanisms of action. Physiol Rev 79:1-71, 1999.
5. Remick DG, Bolgos GR, Siddiqui J, Shin J, Nemzek JA: Six at six: interleukin-6 measured 6 h after the initiation of sepsis predicts mortality over 3 days. Shock 17:463-467, 2002.
6. Nguyen KT, Deak T, Owens SM, Kohno T, Fleshner M, Watkins LR, Maier SF: Exposure to acute stress induces brain interleukin-1beta protein in the rat. J Neurosci 18:2239-2246, 1998.
7. Francis J, Zhang ZH, Weiss RM, Felder RB: Neural regulation of the proinflammatory cytokine response to acute myocardial infarction. Am J Physiol Heart Circ Physiol 287:H791-H797, 2004. (Pubitemid 38955314)
8. Aloisi F: Immune function of microglia. Glia 36:165-179, 2001.
9. Blandino P Jr, Barnum CJ, Deak T: The involvement of norepinephrine and microglia in hypothalamic and splenic IL-1beta responses to stress. J Neuroimmunol 173:87-95, 2006.
10. 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.
11. Vegeto E, Belcredito S, Etteri S, Ghisletti S, Brusadelli A, Meda C, Krust A, Dupont S, Ciana P, Chambon P, et al.: Estrogen receptor-alpha mediates the brain antiinflammatory activity of estradiol. Proc Natl Acad Sci U S A 100: 9614-9619, 2003.
12. Dunn AJ: Cytokine activation of the HPA axis. Ann N Y Acad Sci 917: 608-617, 2000.
13. Yrjanheikki J, Keinanen R, Pellikka M, Hokfelt T, Koistinaho J: Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc Natl Acad Sci U S A 95:15769-15774, 1998.
14. Wang W, Wang P, Chaudry IH: Impaired enterocyte triglyceride synthesis after trauma-hemorrhage and resuscitation. Shock 8:33-39, 1997.
15. Zhanel GG, Homenuik K, Nichol K, Noreddin A, Vercaigne L, Embil J, Gin A, Karlowsky JA, Hoban DJ: The glycylcyclines: a comparative review with the tetracyclines. Drugs 64:63-88, 2004.
16. Francis J, MohanKumar PS, MohanKumar SM: Lipopolysaccharide stimulates norepinephrine efflux from the rat hypothalamus in vitro: blockade by soluble IL-1 receptor. Neurosci Lett 308:71-74, 2001.
17. Cardona AE, Huang D, Sasse ME, Ransohoff RM: Isolation of murine microglial cells for RNA analysis or flow cytometry. Nat Protoc 1:1947-1951, 2006.
18. Yokoyama Y, Kuebler JF, Matsutani T, Schwacha MG, Bland KI, Chaudry IH: Mechanism of the salutary effects of 17beta-estradiol following traumahemorrhage: direct downregulation of Kupffer cell proinflammatory cytokine production. Cytokine 21:91-97, 2003.
19. Hopkins SJ, Rothwell NJ: Cytokines and the nervous system. I: expression and recognition. Trends Neurosci 18:83-88, 1995.
20. Stein VM, Czub M, Schreiner N, Moore PF, Vandevelde M, Zurbriggen A, Tipold A: Microglial cell activation in demyelinating canine distemper lesions. J Neuroimmunol 153:122-131, 2004.
21. Cooney RN: Suppressors of cytokine signaling (SOCS): inhibitors of the JAK/STAT pathway. Shock 17:83-90, 2002.
22. Feuerstein GZ, Liu T, Barone FC: Cytokines, inflammation, and brain injury: role of tumor necrosis factor-alpha. Cerebrovasc Brain Metab Rev 6:341-360, 1994.
23. Douglas SD, Lai JP, Tuluc F, Schwartz L, Kilpatrick LE: Neurokinin-1 receptor expression and function in human macrophages and brain: perspective on the role in HIV neuropathogenesis. Ann N Y Acad Sci 1144:90Y96, 2008.
24. Ahn MJ, Sherwood ER, Prough DS, Lin CY, DeWitt DS: The effects of traumatic brain injury on cerebral blood flow and brain tissue nitric oxide levels and cytokine expression. J Neurotrauma 21:1431-1442, 2004.
25. Smith SM, Vale WW: The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress. Dialogues Clin Neurosci 8:383-395, 2006.
26. Kreutzberg GW: Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19:312-318, 1996.
27. Akiyama H, Kawamata T, Yamada T, Tooyama I, Ishii T, McGeer PL: Expression of intercellular adhesion molecule (ICAM)-1 by a subset of astrocytes in Alzheimer disease and some other degenerative neurological disorders. Acta Neuropathol 85:628-634, 1993.
28. 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 traumahemorrhage. J Leukoc Biol 79:963-970, 2006.
29. Bell MD, Perry VH: Adhesion molecule expression on murine cerebral endothelium following the injection of a proinflammagen or during acute neuronal degeneration. J Neurocytol 24:695-710, 1995.
30. Kreutzberg GW, Barron KD: 5¶-Nucleotidase of microglial cells in the facial nucleus during axonal reaction. J Neurocytol 7:601-610, 1978.
31. Raivich G, Bohatschek M, Kloss CU, Werner A, Jones LL, Kreutzberg GW: Neuroglial activation repertoire in the injured brain: graded response, molecular mechanisms and cues to physiological function. Brain Res Brain Res Rev 30:77-105, 1999.
32. Sanchez Mejia RO, Ona VO, Li M, Friedlander RM: Minocycline reduces traumatic brain injury-mediated caspase-1 activation, tissue damage, and neurological dysfunction. Neurosurgery 48:1393-1399, 2001.
33. Lewis DK, Johnson AB, Stohlgren S, Harms A, Sohrabji F: Effects of estrogen receptor agonists on regulation of the inflammatory response in astrocytes from young adult and middle-aged female rats. J Neuroimmunol 195:47-59, 2008.
34. 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.
35. Vegeto E, Ghisletti S, Meda C, Etteri S, Belcredito S, Maggi A: Regulation of the lipopolysaccharide signal transduction pathway by 17beta-estradiol in macrophage cells. J Steroid Biochem Mol Biol 91:59-66, 2004.
36. Bruce-Keller AJ, Keeling JL, Keller JN, Huang FF, Camondola S, Mattson MP: Antiinflammatory effects of estrogen on microglial activation. Endocrinology 141:3646-3656, 2000.
37. Hsieh YC, Yu HP, Frink M, Suzuki T, Choudhry MA, Schwacha MG, Chaudry IH: G proteinYcoupled receptor 30-dependent protein kinase A pathway is critical in nongenomic effects of estrogen in attenuating liver injury after trauma-hemorrhage. Am J Pathol 170:1210Y1218, 2007.
38. Brailoiu E, Dun SL, Brailoiu GC, Mizuo K, Sklar LA, Oprea TI, Prossnitz ER, Dun NJ: Distribution and characterization of estrogen receptor G proteincoupled receptor 30 in the rat central nervous system. J Endocrinology 193: 311-321, 2007.
39. Angele MK, Schwacha MG, Ayala A, Chaudry IH: Effect of gender and sex hormones on immune responses following shock. Shock 14:81-90, 2000.
40. 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.
41. Yu H-P, Chaudry IH: The role of estrogen and receptor agonists in maintaining organ function following trauma-hemorrhage. Shock 31:227-237, 2009.
42. Carson MJ, Reilly CR, Sutcliffe JG, Lo D: Mature microglia resemble immature antigen-presenting cells. Glia 22:72-85, 1998.