Endothelial von willebrand factor promotes blood-brain barrier flexibility and provides protection from hypoxia and seizures in mice

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 9, 2013, Pages 2112-2120

  Suidan, Georgette L ^a,b,c   Brill, Alexander ^a,b,c,e   De Meyer, Simon F ^a,b,c,d   Voorhees, Jaymie R ^a,b   Cifuni, Stephen M ^a,b   Cabral, Jessica E ^b   Wagner, Denisa D ^a,b,c  

^a CENTER FOR BLOOD RESEARCH   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF LEUVEN   (Belgium)

^e UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

blood vessels; blood brain barrier; claudin 5; endothelium; hypoxia; seizures; von Willebrand factor

Indexed keywords

CLAUDIN 5; PILOCARPINE; TIGHT JUNCTION PROTEIN; VON WILLEBRAND FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; CONTROLLED STUDY; EPILEPTIC STATE; HYPOXIA; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REOXYGENATION; SEIZURE; VASCULAR ENDOTHELIUM;

BLOOD VESSELS; BLOOD-BRAIN BARRIER; CLAUDIN-5; ENDOTHELIUM; HYPOXIA; SEIZURES; VON WILLEBRAND FACTOR;

ANIMALS; BLOOD-BRAIN BARRIER; CAPILLARY PERMEABILITY; CELLS, CULTURED; CLAUDIN-5; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; FEMALE; GENOTYPE; HYPOXIA-ISCHEMIA, BRAIN; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHENOTYPE; PILOCARPINE; RECOMBINANT PROTEINS; STATUS EPILEPTICUS; THROMBOCYTOPENIA; TIGHT JUNCTIONS; VON WILLEBRAND DISEASES; VON WILLEBRAND FACTOR;

EID: 84883261127     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.113.301362     Document Type: Article

References (65)

1. Fabene PF, Navarro Mora G, Martinello M, et al. A role for leukocyte-endothelial adhesion mechanisms in epilepsy. Nat Med. 2008;14:1377-1383.
2. Kaur C, Ling EA. Blood brain barrier in hypoxic-ischemic conditions. Curr Neurovasc Res. 2008;5:71-81. (Pubitemid 351302657)
3. Marchi N, Fan Q, Ghosh C, Fazio V, Bertolini F, Betto G, Batra A, Carlton E, Najm I, Granata T, Janigro D. Antagonism of peripheral inflammation reduces the severity of status epilepticus. Neurobiol Dis. 2009;33:171-181.
4. Minagar A, Alexander JS. Blood-brain barrier disruption in multiple sclerosis. Mult Scler. 2003;9:540-549. (Pubitemid 37479401)
5. Schoch HJ, Fischer S, Marti HH. Hypoxia-induced vascular endothelial growth factor expression causes vascular leakage in the brain. Brain. 2002;125:2549-2557. (Pubitemid 35303512)
6. Yamamoto K, de Waard V, Fearns C, Loskutoff DJ. Tissue distribution and regulation of murine von Willebrand factor gene expression in vivo. Blood. 1998;92:2791-2801. (Pubitemid 28469093)
7. Wagner DD, Frenette PS. The vessel wall and its interactions. Blood. 2008;111:5271-5281.
8. Sporn LA, Marder VJ, Wagner DD. Differing polarity of the constitutive and regulated secretory pathways for von Willebrand factor in endothelial cells. J Cell Biol. 1989;108:1283-1289. (Pubitemid 19097037)
9. Folsom AR, Rosamond WD, Shahar E, Cooper LS, Aleksic N, Nieto FJ, Rasmussen ML, Wu KK. Prospective study of markers of hemostatic function with risk of ischemic stroke. The Atherosclerosis Risk in Communities (ARIC) Study Investigators. Circulation. 1999;100:736-742. (Pubitemid 29383644)
10. Yokota H. Cerebral endothelial damage after severe head injury. J Nippon Med Sch. 2007;74:332-337. (Pubitemid 47523076)
11. Hollestelle MJ, Donkor C, Mantey EA, Chakravorty SJ, Craig A, Akoto AO, O'Donnell J, van Mourik JA, Bunn J. von Willebrand factor propeptide in malaria: evidence of acute endothelial cell activation. Br J Haematol. 2006;133:562-569.
12. Burns A, Wilson E, Harber M, Brunton C, Sweny P. Cerebral venous sinus thrombosis in minimal change nephrotic syndrome. Nephrol Dial Transplant. 1995;10:30-34.
13. Starke RD, Ferraro F, Paschalaki KE, Dryden NH, McKinnon TA, Sutton RE, Payne EM, Haskard DO, Hughes AD, Cutler DF, Laffan MA, Randi AM. Endothelial von Willebrand factor regulates angiogenesis. Blood. 2011;117:1071-1080.
14. Natah SS, Srinivasan S, Pittman Q, Zhao Z, Dunn JF. Effects of acute hypoxia and hyperthermia on the permeability of the blood-brain barrier in adult rats. J Appl Physiol. 2009;107:1348-1356.
15. Wilson MH, Newman S, Imray CH. The cerebral effects of ascent to high altitudes. Lancet Neurol. 2009;8:175-191.
16. McCaffrey G, Willis CL, Staatz WD, Nametz N, Quigley CA, Hom S, Lochhead JJ, Davis TP. Occludin oligomeric assemblies at tight junctions of the blood-brain barrier are altered by hypoxia and reoxygenation stress. J Neurochem. 2009;110:58-71.
17. Hauser WA, Annegers JF, Rocca WA. Descriptive epidemiology of epilepsy: contributions of population-based studies from Rochester, Minnesota. Mayo Clin Proc. 1996;71:576-586.
18. Brodtkorb E, Sjaastad O. Epilepsy prevalence by individual interview in a Norwegian community. Seizure. 2008;17:646-650.
19. Gaitatzis A, Johnson AL, Chadwick DW, Shorvon SD, Sander JW. Life expectancy in people with newly diagnosed epilepsy. Brain. 2004;127:2427-2432. (Pubitemid 39472970)
20. Vignatelli L, Tonon C, D'Alessandro R; Bologna Group for the Study of Status Epilepticus. Incidence and short-term prognosis of status epilepticus in adults in Bologna, Italy. Epilepsia. 2003;44:964-968. (Pubitemid 36842188)
21. Logroscino G, Hesdorffer DC. Methodologic issues in studies of mortality following epilepsy: measures, types of studies, sources of cases, cohort effects, and competing risks. Epilepsia. 2005;46:3-7. (Pubitemid 44922028)
22. Kleen JK, Holmes GL. Brain inflammation initiates seizures. Nat Med. 2008;14:1309-1310.
23. Turski WA, Czuczwar SJ, Kleinrok Z, Turski L. Cholinomimetics produce seizures and brain damage in rats. Experientia. 1983;39:1408-1411. (Pubitemid 14203754)
24. Turski WA, Cavalheiro EA, Schwarz M, Czuczwar SJ, Kleinrok Z, Turski L. Limbic seizures produced by pilocarpine in rats: behavioural, electroencephalographic and neuropathological study. Behav Brain Res. 1983;9:315-335. (Pubitemid 13002328)
25. Honchar MP, Olney JW, Sherman WR. Systemic cholinergic agents induce seizures and brain damage in lithium-treated rats. Science. 1983;220:323-325. (Pubitemid 13118490)
26. Hamilton SE, Loose MD, Qi M, Levey AI, Hille B, McKnight GS, Idzerda RL, Nathanson NM. Disruption of the m1 receptor gene ablates muscarinic receptor-dependent M current regulation and seizure activity in mice. Proc Natl Acad Sci USA. 1997;94:13311-13316. (Pubitemid 27518518)
27. Clifford DB, Olney JW, Maniotis A, Collins RC, Zorumski CF. The functional anatomy and pathology of lithium-pilocarpine and high-dose pilocarpine seizures. Neuroscience. 1987;23:953-968. (Pubitemid 18014408)
28. Morrisett RA, Jope RS, Snead OC 3rd. Effects of drugs on the initiation and maintenance of status epilepticus induced by administration of pilocarpine to lithium-pretreated rats. Exp Neurol. 1987;97:193-200. (Pubitemid 17106683)
29. Willis CL, Meske DS, Davis TP. Protein kinase C activation modulates reversible increase in cortical blood-brain barrier permeability and tight junction protein expression during hypoxia and posthypoxic reoxygenation. J Cereb Blood Flow Metab. 2010;30:1847-1859.
30. Witt KA, Mark KS, Sandoval KE, Davis TP. Reoxygenation stress on blood-brain barrier paracellular permeability and edema in the rat. Microvasc Res. 2008;75:91-96. (Pubitemid 350266739)
31. Pinsky DJ, Naka Y, Liao H, Oz MC, Wagner DD, Mayadas TN, Johnson RC, Hynes RO, Heath M, Lawson CA, Stern DM. Hypoxia-induced exocytosis of endothelial cell Weibel-Palade bodies. A mechanism for rapid neutrophil recruitment after cardiac preservation. J Clin Invest. 1996;97:493-500.
32. Denis CV, André P, Saffaripour S, Wagner DD. Defect in regulated secretion of P-selectin affects leukocyte recruitment in von Willebrand factordeficient mice. Proc Natl Acad Sci USA. 2001;98:4072-4077. (Pubitemid 32249900)
33. Gutsaeva DR, Parkerson JB, Yerigenahally SD, Kurz JC, Schaub RG, Ikuta T, Head CA. Inhibition of cell adhesion by anti-P-selectin aptamer: a new potential therapeutic agent for sickle cell disease. Blood. 2011;117:727-735.
34. Lopez NE, Krzyzaniak MJ, Blow C, Putnam J, Ortiz-Pomales Y, Hageny AM, Eliceiri B, Coimbra R, Bansal V. Ghrelin prevents disruption of the blood-brain barrier after traumatic brain injury. J Neurotrauma. 2012;29:385-393.
35. Ogata N, Yonekawa Y, Taki W, Kannagi R, Murachi T, Hamakubo T, Kikuchi H. Degradation of neurofilament protein in cerebral ischemia. J Neurosurg. 1989;70:103-107.
36. Balaratnasingam C, Morgan WH, Bass L, Kang M, Cringle SJ, Yu DY. Time-dependent effects of focal retinal ischemia on axonal cytoskeleton proteins. Invest Ophthalmol Vis Sci. 2010;51:3019-3028.
37. Curia G, Longo D, Biagini G, Jones RS, Avoli M. The pilocarpine model of temporal lobe epilepsy. J Neurosci Methods. 2008;172:143-157.
38. André P, Denis CV, Ware J, Saffaripour S, Hynes RO, Ruggeri ZM, Wagner DD. Platelets adhere to and translocate on von Willebrand factor presented by endothelium in stimulated veins. Blood. 2000;96:3322-3328.
39. Hsieh CY, Sung PS, Tsai JJ, Huang CW. Terminating prolonged refractory status epilepticus using ketamine. Clin Neuropharmacol. 2010;33:165-167.
40. Cunha AO, Mortari MR, Liberato JL, dos Santos WF. Neuroprotective effects of diazepam, carbamazepine, phenytoin and ketamine after pilocarpine-induced status epilepticus. Basic Clin Pharmacol Toxicol. 2009;104:470-477.
41. Kramer AH. Early ketamine to treat refractory status epilepticus. Neurocrit Care. 2012;16:299-305.
42. Taddei A, Giampietro C, Conti A, Orsenigo F, Breviario F, Pirazzoli V, Potente M, Daly C, Dimmeler S, Dejana E. Endothelial adherens junctions control tight junctions by VE-cadherin-mediated upregulation of claudin-5. Nat Cell Biol. 2008;10:923-934.
43. Janigro D. Are you in or out? Leukocyte, ion, and neurotransmitter permeability across the epileptic blood-brain barrier. Epilepsia. 2012;53:26-34.
44. Koto T, Takubo K, Ishida S, Shinoda H, Inoue M, Tsubota K, Okada Y, Ikeda E. Hypoxia disrupts the barrier function of neural blood vessels through changes in the expression of claudin-5 in endothelial cells. Am J Pathol. 2007;170:1389-1397. (Pubitemid 47339345)
45. Rigau V, Morin M, Rousset MC, de Bock F, Lebrun A, Coubes P, Picot MC, Baldy-Moulinier M, Bockaert J, Crespel A, Lerner-Natoli M. Angiogenesis is associated with blood-brain barrier permeability in temporal lobe epilepsy. Brain. 2007;130:1942-1956. (Pubitemid 47343810)
46. Chauhan AK, Kisucka J, Brill A, Walsh MT, Scheiflinger F, Wagner DD. ADAMTS13: a new link between thrombosis and inflammation. J Exp Med. 2008;205:2065-2074.
47. Petri B, Broermann A, Li H, Khandoga AG, Zarbock A, Krombach F, Goerge T, Schneider SW, Jones C, Nieswandt B, Wild MK, Vestweber D. von Willebrand factor promotes leukocyte extravasation. Blood. 2010;116:4712-4719.
48. Wang L, Fan W, Cai P, Fan M, Zhu X, Dai Y, Sun C, Cheng Y, Zheng P, Zhao BQ. Recombinant ADAMTS13 reduces tissue plasminogen activator-induced hemorrhage after stroke in mice. Ann Neurol. 2013;73:189-198.
49. Noubade R, del Rio R, McElvany B, Zachary JF, Millward JM, Wagner DD, Offner H, Blankenhorn EP, Teuscher C. von-Willebrand factor influences blood brain barrier permeability and brain inflammation in experimental allergic encephalomyelitis. Am J Pathol. 2008;173:892-900.
50. Goerge T, Niemeyer A, Rogge P, Ossig R, Oberleithner H, Schneider SW. Secretion pores in human endothelial cells during acute hypoxia. J Membr Biol. 2002;187:203-211. (Pubitemid 34587776)
51. Rickles FR, Hoyer LW, Rick ME, Ahr DJ. The effects of epinephrine infusion in patients with von Willebrand's disease. J Clin Invest. 1976;57:1618-1625.
52. Fiedler U, Scharpfenecker M, Koidl S, Hegen A, Grunow V, Schmidt JM, Kriz W, Thurston G, Augustin HG. The Tie-2 ligand angiopoietin-2 is stored in and rapidly released upon stimulation from endothelial cell Weibel-Palade bodies. Blood. 2004;103:4150-4156. (Pubitemid 38685356)
53. Ziegler DR, Innocente CE, Leal RB, Rodnight R, Gonçalves CA. The S100B protein inhibits phosphorylation of GFAP and vimentin in a cytoskeletal fraction from immature rat hippocampus. Neurochem Res. 1998;23:1259-1263. (Pubitemid 28495695)
54. Pelinka LE, Kroepfl A, Leixnering M, Buchinger W, Raabe A, Redl H. GFAP versus S100B in serum after traumatic brain injury: relationship to brain damage and outcome. J Neurotrauma. 2004;21:1553-1561. (Pubitemid 39525165)
55. Pham N, Fazio V, Cucullo L, Teng Q, Biberthaler P, Bazarian JJ, Janigro D. Extracranial sources of S100B do not affect serum levels. PLoS One. 2010;5:e12691.
56. Ding J, Li QY, Wang X, Sun CH, Lu CZ, Xiao BG. Fasudil protects hippocampal neurons against hypoxia-reoxygenation injury by suppressing microglial inflammatory responses in mice. J Neurochem. 2010;114:1619-1629.
57. Gotow T. Neurofilaments in health and disease. Med Electron Microsc. 2000;33:173-199. (Pubitemid 32578395)
58. Smith QR. Transport of glutamate and other amino acids at the bloodbrain barrier. J Nutr. 2000;130:1016S-1022S. (Pubitemid 30173636)
59. Banks P, Franks NP, Dickinson R. Competitive inhibition at the glycine site of the N-methyl-D-aspartate receptor mediates xenon neuroprotection against hypoxia-ischemia. Anesthesiology. 2010;112:614-622.
60. Kume T, Nishikawa H, Taguchi R, Hashino A, Katsuki H, Kaneko S, Minami M, Satoh M, Akaike A. Antagonism of NMDA receptors by sigma receptor ligands attenuates chemical ischemia-induced neuronal death in vitro. Eur J Pharmacol. 2002;455:91-100. (Pubitemid 35351603)
61. Bateman LM, Li CS, Seyal M. Ictal hypoxemia in localizationrelated epilepsy: analysis of incidence, severity and risk factors. Brain. 2008;131:3239-3245.
62. van Eijsden P, Notenboom RG, Wu O, de Graan PN, van Nieuwenhuizen O, Nicolay K, Braun KP. In vivo 1H magnetic resonance spectroscopy, T2-weighted and diffusion-weighted MRI during lithium-pilocarpineinduced status epilepticus in the rat. Brain Res. 2004;1030:11-18. (Pubitemid 39563823)
63. Inamura A, Adachi Y, Inoue T, He Y, Tokuda N, Nawata T, Shirao S, Nomura S, Fujii M, Ikeda E, Owada Y, Suzuki M. Cooling treatment transiently increases the permeability of brain capillary endothelial cells through translocation of claudin-5. Neurochem Res. 2013;38:1641-1647.
64. Osada T, Gu YH, Kanazawa M, Tsubota Y, Hawkins BT, Spatz M, Milner R, del Zoppo GJ. Interendothelial claudin-5 expression depends on cerebral endothelial cell-matrix adhesion by ?(1)-integrins. J Cereb Blood Flow Metab. 2011;31:1972-1985.
65. Wagner DD, Olmsted JB, Marder VJ. Immunolocalization of von Willebrand protein in Weibel-Palade bodies of human endothelial cells. J Cell Biol. 1982;95:355-360. (Pubitemid 13208536)