MiR-98 and let-7g∗ protect the blood-brain barrier under neuroinflammatory conditions

Journal of Cerebral Blood Flow and Metabolism

Volumn 35, Issue 12, 2015, Pages 1957-1965

  Rom, Slava ^a   Dykstra, Holly ^a   Zuluaga Ramirez, Viviana ^a   Reichenbach, Nancy L ^a   Persidsky, Yuri ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

BBB; endothelium; inflammation; let 7g ; miR 98

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; LET 7G; MICRORNA; MICRORNA 192; MICRORNA 523; MICRORNA 98; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; GLYCOGEN SYNTHASE KINASE 3; MIRN98 MICRORNA, MOUSE; MIRNLET7 MICRORNA, MOUSE; TUMOR NECROSIS FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLOOD BRAIN BARRIER; CAPILLARY ENDOTHELIAL CELL; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENZYME INHIBITION; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEUKOCYTE ADHERENCE; MICROARRAY ANALYSIS; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CAPILLARY; CAPILLARY PERMEABILITY; CELL MOTION; DRUG EFFECTS; ENDOTHELIUM CELL; GENETIC TRANSFECTION; INFLAMMATION; MALE; MOUSE; PATHOLOGY;

ANIMALS; BLOOD-BRAIN BARRIER; CAPILLARIES; CAPILLARY PERMEABILITY; CELL ADHESION; CELL MOVEMENT; CHEMOKINE CCL2; CHEMOKINE CCL5; ENDOTHELIAL CELLS; GLYCOGEN SYNTHASE KINASE 3; INFLAMMATION; MALE; MICE; MICE, INBRED C57BL; MICROARRAY ANALYSIS; MICRORNAS; TRANSFECTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84948718015     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2015.154     Document Type: Article

References (38)

1. Zlokovic BV. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron. 2008; 57: 178-201.
2. Neuwelt E, Abbott NJ, Abrey L, Banks WA, Blakley B, Davis T, et al. Strategies to advance translational research into brain barriers. Lancet Neurol. 2008; 7: 84-96.
3. Beurel E. Regulation by glycogen synthase kinase-3 of inflammation and T cells in CNS diseases. Front Mol Neurosci. 2011; 4: 18.
4. Ramirez SH, Fan S, Zhang M, Papugani A, Reichenbach N, Dykstra H, et al. Inhibition of glycogen synthase kinase 3beta (GSK3beta) decreases inflammatory responses in brain endothelial cells. Am J Pathol. 2010; 176: 881-892.
5. Ramirez SH, Fan S, Dykstra H, Rom S, Mercer A, Reichenbach NL, et al. Inhibition of glycogen synthase kinase 3beta promotes tight junction stability in brain endothelial cells by half-life extension of occludin and claudin-5. PLoS One. 2013; 8: e55972.
6. Fish JE A primer on the role of microRNAs in endothelial biology and vascular disease. Semin Nephrol. 2012; 32: 167-175.
7. Hulsmans M, Holvoet P. MicroRNA-containing microvesicles regulating inflammation in association with atherosclerotic disease. Cardiovasc Res. 2013; 100: 7-18.
8. Guo H, Ingolia NT, Weissman JS, Bartel DP. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature. 2010; 466: 835-840.
9. Rom S, Rom I, Passiatore G, Pacifici M, Radhakrishnan S, Del Valle L, et al. CCL8/ MCP-2 is a target for mir-146a in HIV-1-infected human microglial cells. FASEB J. 2010; 24: 2292-2300.
10. Santoro MM, Nicoli S. miRNAs in endothelial cell signaling: the endomiRNAs. Exp Cell Res. 2013; 319: 1324-1330.
11. Sen CK, Gordillo GM, Khanna S, Roy S. Micromanaging vascular biology: tiny microRNAs play big band. J Vasc Res. 2009; 46: 527-540.
12. Mishra R, Singh SK. HIV-1 Tat C modulates expression of miRNA-101 to suppress VE-cadherin in human brain microvascular endothelial cells. J Neurosci. 2013; 33: 5992-6000.
13. McCall MN, Kent OA, Yu J, Fox-Talbot K, Zaiman AL, Halushka MK. MicroRNA profiling of diverse endothelial cell types. BMC Med Genomics. 2011; 4: 78.
14. Liao YC, Wang YS, Guo YC, Lin WL, Chang MH, Juo SH. Let-7g improves multiple endothelial functions through targeting transforming growth factor-beta and SIRT-1 signaling. J Am Coll Cardiol. 2014; 63: 1685-1694.
15. Rom S, Zuluaga-Ramirez V, Dykstra H, Reichenbach N, Pacher P, Persidsky Y. Selective activation of cannabinoid receptor 2 (CB2) in leukocytes suppresses their engagement of the brain endothelium and protects the blood brain barrier (BBB). Am J Pathol. 2013; 183: 1548-1558.
16. Rom S, Zuluaga-Ramirez V, Dykstra H, Reichenbach N, Ramirez SH, Persidsky Y. Poly(ADP-ribose) polymerase-1 inhibition in brain endothelium protects the blood-brain barrier under physiologic and neuroinflammatory conditions. J Cereb Blood Flow Metab. 2015; 35: 28-36.
17. Rom S, Fan S, Reichenbach N, Dykstra H, Ramirez SH, Persidsky Y. Glycogen synthase kinase 3beta inhibition prevents monocyte migration across brain endothelial cells via Rac1-GTPase suppression and down-regulation of active integrin conformation. Am J Pathol. 2012; 181: 1414-1425.
18. Veres B, Gallyas F Jr., Varbiro G, Berente Z, Osz E, Szekeres G, et al. Decrease of the inflammatory response and induction of the Akt/protein kinase B pathway by poly-(ADP-ribose) polymerase 1 inhibitor in endotoxin-induced septic shock. Biochem Pharmacol. 2003; 65: 1373-1382.
19. Larson SD, Jackson LN, Chen LA, Rychahou PG, Evers BM. Effectiveness of siRNA uptake in target tissues by various delivery methods. Surgery. 2007; 142: 262-269.
20. Jiang N, Zhang X, Zheng X, Chen D, Siu K, Wang H, et al A novel in vivo siRNA delivery system specifically targeting liver cells for protection of ConA-induced fulminant hepatitis. PLoS One. 2012; 7: e44138.
21. Chun HB, Scott M, Niessen S, Hoover H, Baird A, Yates J, 3rd, et al. The proteome of mouse brain microvessel membranes and basal lamina. J Cereb Blood Flow Metab. 2011; 31: 2267-2281.
22. Yousif S, Marie-Claire C, Roux F, Scherrmann JM, Decleves X. Expression of drug transporters at the blood-brain barrier using an optimized isolated rat brain microvessel strategy. Brain Res. 2007; 1134: 1-11.
23. Potula R, Ramirez SH, Knipe B, Leibhart J, Schall K, Heilman D, et al. Peroxisome proliferator-Activated receptor-gamma activation suppresses HIV-1 replication in an animal model of encephalitis. AIDS. 2008; 22: 1539-1549.
24. Zhou Z, Wang L, Song Z, Lambert JC, McClain CJ, Kang YJ A critical involvement of oxidative stress in acute alcohol-induced hepatic TNF-Alpha production. Am J Pathol. 2003; 163: 1137-1146.
25. Schober A. Chemokines in vascular dysfunction and remodeling. Arterioscler Thromb Vasc Biol. 2008; 28: 1950-1959.
26. Stamatovic SM, Shakui P, Keep RF, Moore BB, Kunkel SL, Van Rooijen N, et al. Monocyte chemoattractant protein-1 regulation of blood-brain barrier permeability. J Cereb Blood Flow Metab. 2005; 25: 593-606.
27. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ. Structure and function of the blood-brain barrier. Neurobiol Dis. 2010; 37: 13-25.
28. Aghajanian A, Wittchen ES, Allingham MJ, Garrett TA, Burridge K. Endothelial cell junctions and the regulation of vascular permeability and leukocyte transmigration. J Thromb Haemost. 2008; 6: 1453-1460.
29. De Sarno P, Axtell RC, Raman C, Roth KA, Alessi DR, Jope RS. Lithium prevents and ameliorates experimental autoimmune encephalomyelitis. J Immunol. 2008; 181: 338-345.
30. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004; 116: 281-297.
31. Betel D, Wilson M, Gabow A, Marks DS, Sander C. The microRNA.org resource: targets and expression. Nucleic Acids Res. 2008; 36, Database issue D149-D153.
32. Croce CM, Calin GA. miRNAs, cancer, and stem cell division. Cell. 2005; 122: 6-7.
33. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. Human MicroRNA targets. PLoS Biol. 2004; 2: e363.
34. Guo D, Liu J, Wang W, Hao F, Sun X, Wu X, et al. Alteration in abundance and compartmentalization of inflammation-related miRNAs in plasma after intracerebral hemorrhage. Stroke. 2013; 44: 1739-1742.
35. Reijerkerk A, Lopez-Ramirez MA, van Het Hof B, Drexhage JA, Kamphuis WW, Kooij G, et al. MicroRNAs regulate human brain endothelial cell-barrier function in inflammation: implications for multiple sclerosis. J Neurosci. 2013; 33: 6857-6863.
36. Wu D, Cerutti C, Lopez-Ramirez MA, Pryce G, King-Robson J, Simpson JE, et al. Brain endothelial miR-146a negatively modulates T-cell adhesion through repressing multiple targets to inhibit NF-kappaB activation. J Cereb Blood Flow Metab. 2015; 35: 412-423.
37. Artus C, Glacial F, Ganeshamoorthy K, Ziegler N, Godet M, Guilbert T, et al. The Wnt/planar cell polarity signaling pathway contributes to the integrity of tight junctions in brain endothelial cells. J Cereb Blood Flow Metab. 2014; 34: 433-440.
38. Staedel C, Darfeuille F. MicroRNAs and bacterial infection. Cell Microbiol. 2013; 15: 1496-1507.