Poly(ADP-ribose) polymerase-1 inhibition in brain endothelium protects the blood-brain barrier under physiologic and neuroinflammatory conditions

Journal of Cerebral Blood Flow and Metabolism

Volumn 35, Issue 1, 2015, Pages 28-36

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

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Department of Pathology ^*  (United States)

Author keywords

BBB; endothelial dysfunction; PARP

Indexed keywords

NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; CYTOKINE; ENZYME INHIBITOR; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PARP1 PROTEIN, HUMAN; PARP1 PROTEIN, MOUSE; TIGHT JUNCTION PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CAPILLARY ENDOTHELIAL CELL; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM; IN VITRO STUDY; IN VIVO STUDY; LEUKOCYTE ADHERENCE; MALE; MEMBRANE PERMEABILITY; MICROVASCULATURE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; VIDEO MICROSCOPY; ANIMAL; ASEPTIC MENINGITIS; C57BL MOUSE; CAPILLARY PERMEABILITY; CELL ADHESION; CELL CULTURE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; ENDOTHELIUM CELL; FLOW CYTOMETRY; HUMAN; IMMUNOLOGY; LEUKOCYTE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; VASCULAR ENDOTHELIUM; WESTERN BLOTTING;

ANIMALS; BLOOD-BRAIN BARRIER; BLOTTING, WESTERN; CAPILLARY PERMEABILITY; CELL ADHESION; CELLS, CULTURED; CYTOKINES; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; ENZYME INHIBITORS; FLOW CYTOMETRY; HUMANS; LEUKOCYTES; MALE; MENINGITIS, ASEPTIC; MICE, INBRED C57BL; MICROSCOPY, VIDEO; POLY(ADP-RIBOSE) POLYMERASE INHIBITORS; TIGHT JUNCTION PROTEINS; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 84920692915     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2014.167     Document Type: Article

References (40)

1. Rouleau M, Patel A, Hendzel MJ, Kaufmann SH, Poirier GG. PARP inhibition: PARP1 and beyond. Nat Rev Cancer 2010; 10: 293-301.
2. Krishnakumar R, Kraus WL. The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol Cell 2010; 39: 8-24.
3. Lescot T, Fulla-Oller L, Palmier B, Po C, Beziaud T, Puybasset L et al. Effect of acute poly(ADP-ribose) polymerase inhibition by 3-AB on blood-brain barrier permeability and edema formation after focal traumatic brain injury in rats. J Neurotrauma 2010; 27: 1069-1079.
4. Lenzser G, Kis B, Snipes JA, Gaspar T, Sandor P, Komjati K et al. Contribution of poly(ADP-ribose) polymerase to postischemic blood-brain barrier damage in rats. J Cereb Blood Flow Metab 2007; 27: 1318-1326.
5. Farez MF, Quintana FJ, Gandhi R, Izquierdo G, Lucas M, Weiner HL. Toll-like receptor 2 and poly(ADP-ribose) polymerase 1 promote central nervous system neuroinflammation in progressive EAE. Nat Immunol 2009; 10: 958-964.
6. Zhang C, Yang J, Jennings LK. Attenuation of neointima formation through the inhibition of DNA repair enzyme PARP-1 in balloon-injured rat carotid artery. Am J Physiol Heart Circ Physiol 2004; 287: H659-H666.
7. Cavone L, Aldinucci A, Ballerini C, Biagioli T, Moroni F, Chiarugi A. PARP-1 inhibition prevents CNS migration of dendritic cells during EAE, suppressing the encephalitogenic response and relapse severity. Mult Scler 2011; 17: 794-807.
8. Ramirez SH, Hasko J, Skuba A, Fan S, Dykstra H, McCormick R et al. Activation of cannabinoid receptor 2 attenuates leukocyte-endothelial cell interactions and blood-brain barrier dysfunction under inflammatory conditions. J Neurosci 2012; 32: 4004-4016.
9. Rom S, Zuluaga-Ramirez V, Dykstra H, Reichenbach NL, Pacher P, Persidsky Y. Selective activation of cannabinoid receptor 2 in leukocytes suppresses their engagement of the brain endothelium and protects the blood-brain barrier. Am J Pathol 2013; 183: 1548-1558.
10. 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.
11. 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.
12. Booth G, Stalker TJ, Lefer AM, Scalia R. Elevated ambient glucose induces acute inflammatory events in the microvasculature: effects of insulin. Am J Physiol Endocrinol Metab 2001; 280: E848-E856.
13. Hay T, Matthews JR, Pietzka L, Lau A, Cranston A, Nygren AO et al. Poly(ADPribose) polymerase-1 inhibitor treatment regresses autochthonous Brca2/p53-mutant mammary tumors in vivo and delays tumor relapse in combination with carboplatin. Cancer Res 2009; 69: 3850-3855.
14. Janzen DM, Paik DY, Rosales MA, Yep B, Cheng D, Witte ON et al. Low levels of circulating estrogen sensitize PTEN-null endometrial tumors to PARP inhibition in vivo. Mol Cancer Ther 2013; 12: 2917-2928.
15. McCullough LD, Zeng Z, Blizzard KK, Debchoudhury I, Hurn PD. Ischemic nitric oxide and poly (ADP-ribose) polymerase-1 in cerebral ischemia: male toxicity, female protection. J Cereb Blood Flow Metab 2005; 25: 502-512.
16. 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.
17. 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.
18. Ramirez SH, Fan S, Dykstra H, Reichenbach N, Del Valle L, Potula R et al. Dyad of CD40/CD40 ligand fosters neuroinflammation at the blood-brain barrier and is regulated via JNK signaling: implications for HIV-1 encephalitis. J Neurosci 2010; 30: 9454-9464.
19. Boudaoud A, Burian A, Borowska-Wykret D, Uyttewaal M, Wrzalik R, Kwiatkowska D et al. FibrilTool, an ImageJ plug-in to quantify fibrillar structures in raw microscopy images. Nat Protoc 2014; 9: 457-463.
20. Aychek T, Vandoorne K, Brenner O, Jung S, Neeman M. Quantitative analysis of intravenously administered contrast media reveals changes in vascular barrier functions in a murine colitis model. Magn Reson Med 2011; 66: 235-243.
21. Haddad M, Rhinn H, Bloquel C, Coqueran B, Szabo C, Plotkine M et al. Antiinflammatory effects of PJ34, a poly(ADP-ribose) polymerase inhibitor, in transient focal cerebral ischemia in mice. Br J Pharmacol 2006; 149: 23-30.
22. Ha HC, Hester LD, Snyder SH. Poly(ADP-ribose) polymerase-1 dependence of stress-induced transcription factors and associated gene expression in glia. Proc Natl Acad Sci USA 2002; 99: 3270-3275.
23. Moroni F. Poly(ADP-ribose)polymerase 1 (PARP-1) and postischemic brain damage. Current Opin Pharmacol 2008; 8: 96-103.
24. Persidsky Y, Ramirez SH, Haorah J, Kanmogne GD. Blood-brain barrier: structural components and function under physiologic and pathologic conditions. J Neuroimmune Pharmacol 2006; 1: 223-236.
25. Birukov KG. Small GTPases in mechanosensitive regulation of endothelial barrier. Microvasc Res 2009; 77: 46-52.
26. Doggett TM, Breslin JW. Study of the actin cytoskeleton in live endothelial cells expressing GFP-actin. J Vis Exp 2011; 57: 3187.
27. Yamamoto M, Ramirez SH, Sato S, Kiyota T, Cerny RL, Kaibuchi K et al. Phosphorylation of claudin-5 and occludin by rho kinase in brain endothelial cells. Am J Pathol 2008; 172: 521-533.
28. Spindler V, Schlegel N, Waschke J. Role of GTPases in control of microvascular permeability. Cardiovasc Res 2010; 87: 243-253.
29. De Craene B, van Roy F, Berx G. Unraveling signalling cascades for the Snail family of transcription factors. Cell Signal 2005; 17: 535-547.
30. Feldman GJ, Mullin JM, Ryan MP. Occludin: structure, function and regulation. Adv Drug Deliv Rev 2005; 57: 883-917.
31. Kajita M, McClinic KN, Wade PA. Aberrant expression of the transcription factors snail and slug alters the response to genotoxic stress. Mol Cell Biol 2004; 24: 7559-7566.
32. Aslam M, Ahmad N, Srivastava R, Hemmer B. TNF-alpha induced NFkappaB signaling and p65 (RelA) overexpression repress Cldn5 promoter in mouse brain endothelial cells. Cytokine 2012; 57: 269-275.
33. Liu L, Ke Y, Jiang X, He F, Pan L, Xu L et al. Lipopolysaccharide activates ERKPARP- 1-RelA pathway and promotes nuclear factor-kappaB transcription in murine macrophages. Human Immunol 2012; 73: 439-447.
34. Kraus WL, Lis JT. PARP goes transcription. Cell 2003; 113: 677-683.
35. Koedel U, Winkler F, Angele B, Fontana A, Pfister HW. Meningitis-associated central nervous system complications are mediated by the activation of poly (ADP-ribose) polymerase. J Cereb Blood Flow Metab 2002; 22: 39-49.
36. Erdelyi K, Kiss A, Bakondi E, Bai P, Szabo C, Gergely P et al. Gallotannin inhibits the expression of chemokines and inflammatory cytokines in A549 cells. Mol Pharmacol 2005; 68: 895-904.
37. Vestweber D. Molecular mechanisms that control leukocyte extravasation through endothelial cell contacts. Ernst Schering Found Symp Proc 2007; 3: 151-167.
38. Bruewer M, Hopkins AM, Hobert ME, Nusrat A, Madara JL. RhoA, Rac1, and Cdc42 exert distinct effects on epithelial barrier via selective structural and biochemical modulation of junctional proteins and F-actin. Am J Physiol Cell Physiol 2004; 287: C327-C335.
39. Rolfe BE, Worth NF, World CJ, Campbell JH, Campbell GR. Rho and vascular disease. Atherosclerosis 2005; 183: 1-16.
40. Wu XL, Wang P, Liu YH, Xue YX. Effects of Poly (ADP-ribose) Polymerase Inhibitor 3-Aminobenzamide on Blood-Brain Barrier and Dopaminergic Neurons of Rats with Lipopolysaccharide-Induced Parkinson's Disease. J Mol Neurosci 2013; 53: 1-9.