Estrogen protects the blood–brain barrier from inflammation-induced disruption and increased lymphocyte trafficking

Brain, Behavior, and Immunity

Volumn 51, Issue , 2016, Pages 212-222

  Maggioli, E ^a   McArthur, S ^a,b   Mauro, C ^a   Kieswich, J ^a   Kusters, D H M ^c,d   Reutelingsperger, C P M ^c   Yaqoob, M ^a   Solito, E ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY OF WESTMINSTER   (United Kingdom)

^c MAASTRICHT UNIVERSITY   (Netherlands)

^d UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

Annexin A1; Blood brain barrier; Estrogen; Lymphocytes; Tight junction

Indexed keywords

ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; G PROTEIN COUPLED RECEPTOR 30; GAMMA INTERFERON; INTERCELLULAR ADHESION MOLECULE 1; LIPOCORTIN 1; LIPOPOLYSACCHARIDE; TUMOR NECROSIS FACTOR; CYTOKINE; ESTROGEN RECEPTOR; G PROTEIN COUPLED RECEPTOR; GPR30 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CAPILLARY ENDOTHELIAL CELL; BRAIN PROTECTION; C57BL 6 MOUSE; CELL MEMBRANE PERMEABILITY; CELL MIGRATION; CEREBROVASCULAR DISEASE; CONTROLLED STUDY; ELECTRIC RESISTANCE; FEMALE; HOMEOSTASIS; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE; LYMPHOCYTE MIGRATION; MALE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OVARIECTOMY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SENESCENCE; SEX DIFFERENCE; TIGHT JUNCTION; UPREGULATION; YOUNG ADULT; ANIMAL; C57BL MOUSE; CELL MOTION; CHEMICALLY INDUCED; DRUG EFFECTS; IMMUNOLOGY; INFLAMMATION; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; ANNEXIN A1; BLOOD-BRAIN BARRIER; CELL MOVEMENT; CYTOKINES; ESTRADIOL; FEMALE; HUMANS; INFLAMMATION; LIPOPOLYSACCHARIDES; LYMPHOCYTES; MALE; MICE, INBRED C57BL; RECEPTORS, ESTROGEN; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84940704808     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2015.08.020     Document Type: Article

References (48)

1. Abbott, N.J., Hughes, C.C., Revest, P.A., Greenwood, J., Development and characterisation of a rat brain capillary endothelial culture: towards an in vitro blood–brain barrier. J. Cell Sci. 103:Pt 1 (1992), 23–37.
2. Abbott, N.J., Patabendige, A.A., Dolman, D.E., Yusof, S.R., Begley, D.J., Structure and function of the blood–brain barrier. Neurobiol. Dis. 37:1 (2010), 13–25.
3. Broughton, B.R., et al. Stroke increases g protein-coupled estrogen receptor expression in the brain of male but not female mice. Neurosignals 21:3–4 (2013), 229–239.
4. Burek, M., Arias-Loza, P.A., Roewer, N., Forster, C.Y., Claudin-5 as a novel estrogen target in vascular endothelium. Arterioscler. Thromb. Vasc. Biol. 30:2 (2010), 298–304.
5. Burek, M., Steinberg, K., Forster, C.Y., Mechanisms of transcriptional activation of the mouse claudin-5 promoter by estrogen receptor alpha and beta. Mol. Cell. Endocrinol. 392:1–2 (2014), 144–151.
6. Carvey, P.M., Hendey, B., Monahan, A.J., The blood–brain barrier in neurodegenerative disease: a rhetorical perspective. J. Neurochem. 111:2 (2009), 291–314.
7. Cignarella, A., et al. Distinct roles of estrogen receptor-alpha and beta in the modulation of vascular inducible nitric-oxide synthase in diabetes. J. Pharmacol. Exp. Ther. 328:1 (2009), 174–182.
8. Coisne, C., et al. Mouse syngenic in vitro blood–brain barrier model: a new tool to examine inflammatory events in cerebral endothelium. Lab. Invest. 85:6 (2005), 734–746.
9. Cristante, E., et al. Feature Article: Identification of an essential endogenous regulator of blood–brain barrier integrity, and its pathological and therapeutic implications. Proc. Natl. Acad. Sci. U.S.A. 110:3 (2013), 832–841.
10. Czlonkowska, A., Ciesielska, A., Gromadzka, G., Kurkowska-Jastrzebska, I., Estrogen and cytokines production – the possible cause of gender differences in neurological diseases. Curr. Pharm. Des. 11:8 (2005), 1017–1030.
11. Davies, E., Omer, S., Morris, J.F., Christian, H.C., The influence of 17beta-estradiol on annexin 1 expression in the anterior pituitary of the female rat and in a folliculo-stellate cell line. J. Endocrinol. 192:2 (2007), 429–442.
12. Dietrich, J.B., Endothelial cells of the blood–brain barrier: a target for glucocorticoids and estrogens?. Front. Biosci. 9 (2004), 684–693.
13. Flower, R.J., Blackwell, G.J., Anti-inflammatory steroids induce biosynthesis of a phospholipase A2 inhibitor which prevents prostaglandin generation. Nature 278:5703 (1979), 456–459.
14. Gameiro, C.M., Romao, F., Castelo-Branco, C., Menopause and aging: changes in the immune system—a review. Maturitas 67:4 (2010), 316–320.
15. Gee, J.M., Kalil, A., Shea, C., Becker, K.J., Lymphocytes: potential mediators of postischemic injury and neuroprotection. Stroke 38:2 (Suppl.) (2007), 783–788.
16. Gillies, G.E., McArthur, S., Estrogen actions in the brain and the basis for differential action in men and women: a case for sex-specific medicines. Pharmacol. Rev. 62:2 (2010), 155–198.
17. Haas, R., et al. Lactate regulates metabolic and pro-inflammatory circuits in control of t cell migration and effector functions. PLoS Biol., 13(7), 2015, e1002202.
18. Haast, R.A., Gustafson, D.R., Kiliaan, A.J., Sex differences in stroke. J. Cereb. Blood Flow Metab. 32:12 (2012), 2100–2107.
19. Hannon, R., et al. Aberrant inflammation and resistance to glucocorticoids in annexin 1−/− mouse. FASEB J. 17:2 (2003), 253–255.
20. Herter, J., Zarbock, A., Integrin regulation during leukocyte recruitment. J. Immunol. 190:9 (2013), 4451–4457.
21. Hou, X., Pei, F., Estradiol inhibits cytokine-induced expression of VCAM-1 and ICAM-1 in cultured human endothelial cells via AMPK/PPARalpha activation. Cell Biochem. Biophys., 2015.
22. Koellhoffer, E.C., McCullough, L.D., The effects of estrogen in ischemic stroke. Transl. Stroke Res. 4:4 (2013), 390–401.
23. Li, T., et al. Age and sex differences in vascular responsiveness in healthy and trauma patients: contribution of estrogen receptor-mediated Rho kinase and PKC pathways. Am. J. Physiol. Heart Circ. Physiol. 306:8 (2014), H1105–H1115.
24. Lopez-Ramirez, M.A., et al. Role of caspases in cytokine-induced barrier breakdown in human brain endothelial cells. J. Immunol., 2012.
25. McArthur, S., et al. Annexin A1: a central player in the anti-inflammatory and neuroprotective role of microglia. J. Immunol. 185:10 (2010), 6317–6328.
26. McArthur, S., et al. Annexin A1 regulates hormone exocytosis through a mechanism involving actin reorganization. FASEB J. 23:11 (2009), 4000–4010.
27. Murray, K.N., Buggey, H.F., Denes, A., Allan, S.M., Systemic immune activation shapes stroke outcome. Mol. Cell. Neurosci. 53 (2013), 14–25.
28. Nadkarni, S., McArthur, S., Oestrogen and immunomodulation: new mechanisms that impact on peripheral and central immunity. Curr. Opin. Pharmacol. 13:4 (2013), 576–581.
29. Nadkarni, S., Cooper, D., Brancaleone, V., Bena, S., Perretti, M., Activation of the annexin A1 pathway underlies the protective effects exerted by estrogen in polymorphonuclear leukocytes. Arterioscler. Thromb. Vasc. Biol. 31:11 (2011), 2749–2759.
30. Oztas, B., Kucuk, M., Kaya, M., Sex-dependent changes in blood–brain barrier permeability in epileptic rats following acute hyperosmotic exposure. Pharmacol. Res. 43:5 (2001), 469–472.
31. Parkening, T.A., Lau, I.F., Saksena, S.K., Chang, M.C., Circulating plasma levels of pregnenolone, progesterone, estrogen, luteinizing hormone, and follicle stimulating hormone in young and aged C57BL/6 mice during various stages of pregnancy. J. Gerontol. 33:2 (1978), 191–196.
32. Perretti, M., D'Acquisto, F., Annexin A1 and glucocorticoids as effectors of the resolution of inflammation. Nat. Rev. Immunol. 9:1 (2009), 62–70.
33. Ransohoff, R.M., Engelhardt, B., The anatomical and cellular basis of immune surveillance in the central nervous system. Nat. Rev. Immunol. 12:9 (2012), 623–635.
34. Rohnelt, R.K., Hoch, G., Reiss, Y., Engelhardt, B., Immunosurveillance modelled in vitro: naive and memory T cells spontaneously migrate across unstimulated microvascular endothelium. Int. Immunol. 9:3 (1997), 435–450.
35. Rubinson, D.A., et al. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat. Genet. 33:3 (2003), 401–406.
36. Solito, E., et al. Dexamethasone induces rapid serine-phosphorylation and membrane translocation of annexin 1 in a human folliculostellate cell line via a novel nongenomic mechanism involving the glucocorticoid receptor, protein kinase C, phosphatidylinositol 3-kinase, and mitogen-activated protein kinase. Endocrinology 144:4 (2003), 1164–1174.
37. Solito, E., Raguenes-Nicol, C., de Coupade, C., Bisagni-Faure, A., Russo-Marie, F., U937 cells deprived of endogenous annexin 1 demonstrate an increased PLA2 activity. Br. J. Pharmacol. 124:8 (1998), 1675–1683.
38. Solito, E., Froud, K., Christian, H., Morris, J., Buckingham, J., Opposite effects of dexamethasone and oestardiol on annexin 1 expression. Endocr. Abstr., 10, 2003, 65.
39. Solito, E., et al. Post-translational modification plays an essential role in the translocation of annexin A1 from the cytoplasm to the cell surface. FASEB J. 20:9 (2006), 1498–1500.
40. Suzuki, S., Brown, C.M., Wise, P.M., Mechanisms of neuroprotection by estrogen. Endocrine 29:2 (2006), 209–215.
41. Suzuki, S., Brown, C.M., Wise, P.M., Neuroprotective effects of estrogens following ischemic stroke. Front. Neuroendocrinol. 30:2 (2009), 201–211.
42. Tsinti, M., et al. Functional estrogen receptors alpha and beta are expressed in normal human salivary gland epithelium and apparently mediate immunomodulatory effects. Eur. J. Oral Sci. 117:5 (2009), 498–505.
43. Tu, J., Jufri, N.F., Estrogen signaling through estrogen receptor beta and G-protein-coupled estrogen receptor 1 in human cerebral vascular endothelial cells: implications for cerebral aneurysms. Biomed. Res. Int., 2013, 2013, 524324.
44. Villar, I.C., et al. Suppression of endothelial P-selectin expression contributes to reduced cell trafficking in females: an effect independent of NO and prostacyclin. Arterioscler. Thromb. Vasc. Biol. 31:5 (2011), 1075–1083.
45. Weksler, B., Linking thrombophilia and idiopathic intracranial hypertension. J. Lab. Clin. Med. 145:2 (2005), 63–64.
46. Weksler, B.B., et al. blood–brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J. 19:13 (2005), 1872–1874.
47. Xing, D., et al. Estrogen modulates TNF-alpha-induced inflammatory responses in rat aortic smooth muscle cells through estrogen receptor-beta activation. Am. J. Physiol. Heart Circ. Physiol. 292:6 (2007), H2607–H2612.
48. Yazid, S., et al. Anti-allergic drugs and the Annexin-A1 system. Pharmacol. Rep. 62:3 (2010), 511–517.