Epileptiform activity induces vascular remodeling and zonula occludens 1 downregulation in organotypic hippocampal cultures: Role of VEGF signaling pathways

Journal of Neuroscience

Volumn 31, Issue 29, 2011, Pages 10677-10688

  Morin Brureau, Mélanie ^a   Lebrun, Aurore ^a   Rousset, Marie Claude ^a   Fagni, Laurent ^a   Bockaert, Joël ^a   de Bock, Frédéric ^a   Lerner Natoli, Mireille ^a  

^a INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; PROTEIN ZO1; RECOMBINANT VASCULOTROPIN; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL; CELL DEATH; CELL SURVIVAL; DENSITY; DOWN REGULATION; ENZYME ACTIVATION; EPILEPTIC DISCHARGE; HIPPOCAMPUS; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TISSUE CULTURE; VASCULARIZATION;

ANESTHETICS, LOCAL; ANIMALS; ANIMALS, NEWBORN; ANTIBODIES; BRAIN WAVES; DOWN-REGULATION; DRUG INTERACTIONS; ENDOTHELIUM, VASCULAR; HIPPOCAMPUS; KAINIC ACID; L-LACTATE DEHYDROGENASE; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; ORGAN CULTURE TECHNIQUES; PHOSPHOPROTEINS; PROPIDIUM; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TEPROTIDE; TETRODOTOXIN; TIME FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 79960669855     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5692-10.2011     Document Type: Article

References (61)

1. Ahmad S, Hewett PW, Wang P, Al-Ani B, Cudmore M, Fujisawa T, Haigh JJ, le Noble F, Wang L, Mukhopadhyay D, Ahmed A (2006) Direct evidence for endothelial vascular endothelial growth factor receptor-1 function in nitric oxide-mediated angiogenesis. Circ Res 99:715-722.
2. Allan SM, Tyrrell PJ, Rothwell NJ (2005) Interleukin-1 and neuronal injury. Nat Rev Immunol 5:629-640.
3. Argaw AT, Gurfein BT, Zhang Y, Zameer A, John GR (2009) VEGF-mediated disruption of endothelial CLN-5 promotes blood-brain barrier breakdown. Proc Natl Acad Sci U S A 106:1977-1982.
4. Ballabh P, Braun A, Nedergaard M (2004) The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol Dis 16:1-13.
5. Balosso S, Maroso M, Sanchez-Alavez M, Ravizza T, Frasca A, Bartfai T, Vezzani A (2008) A novel non-transcriptional pathway mediates the proconvulsive effects of interleukin-1beta. Brain 131:3256-3265.
6. Bazzoni G, Dejana E (2004) Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol Rev 84:869-901.
7. Bratz E (1899) Ammonshornbefunde bei epileptikern Arch Psychiatr Nervenkr 32:820-835.
8. Bruns AF, Herbert SP, Odell AF, Jopling HM, Hooper NM, Zachary IC, Walker JH, Ponnambalam S (2010) Ligand-stimulated VEGFR-2 signaling is regulated by co-ordinated trafficking and proteolysis. Traffic 11:161-174.
9. Cacheaux LP, Ivens S, David Y, Lakhter AJ, Bar-Klein G, Shapira M, Heinemann U, Friedman A, Kaufer D (2009) Transcriptome profiling reveals TGF-beta signaling involvement in epileptogenesis. J Neurosci 29:8927-8935.
10. Choi JS, Kim SY, Park HJ, Cha JH, Choi YS, Kang JE, Chung JW, Chun MH, Lee MY (2003) Upregulation of gp130 and differential activation of STAT and p42/44 MAPK in the rat hippocampus following kainic acidinduced seizures. Brain Res Mol Brain Res 119:10-18.
11. Croll SD, Goodman JH, Scharfman HE (2004) Vascular endothelial growth factor (VEGF) in seizures: a double-edged sword. Adv Exp Med Biol 548:57-68.
12. Dahmani S, Rouelle D, Gressens P, Mantz J (2007) The effects of lidocaine and bupivacaine on protein expression of cleaved caspase 3 and tyrosine phosphorylation in the rat hippocampal slice. Anesth Analg 104:119-123.
13. David Y, Cacheaux LP, Ivens S, Lapilover E, Heinemann U, Kaufer D, Friedman A (2009) Astrocytic dysfunction in epileptogenesis: consequence of altered potassium and glutamate homeostasis? J Neurosci 29:10588-10599.
14. de Bock F, Derijard B, Dornand J, Bockaert J, Rondouin G (1998) The neuronal death induced by endotoxic shock but not that induced by excitatory amino acids requires TNF-alpha. Eur J Neurosci 10:3107-3114.
15. de Paz P, Barrio JP (1985) Stereological parameters from the analysis of the cell micrographs either by manual point-counting methods or by using a semi-automatic system: a BASIC program for ZX-Spectrum personal computer. Comput Biol Med 15:153-158.
16. Dougher M, Terman BI (1999) Autophosphorylation of KDR in the kinase domain is required for maximal VEGF-stimulated kinase activity and receptor internalization. Oncogene 18:1619-1627.
17. Eid T, Brines ML, Cerami A, Spencer DD, Kim JH, Schweitzer JS, Ottersen OP, de Lanerolle NC (2004) Increased expression of erythropoietin receptor on blood vessels in the human epileptogenic hippocampus with sclerosis. J Neuropathol Exp Neurol 63:73-83.
18. Eid T, Lee TS, Thomas MJ, Amiry-Moghaddam M, Bjørnsen LP, Spencer DD, Agre P, Ottersen OP, de Lanerolle NC (2005) Loss of perivascular aquaporin 4 may underlie deficient water and K+ homeostasis in the human epileptogenic hippocampus. Proc Natl Acad Sci U S A 102:1193-1198.
19. Fabene PF, Navarro Mora G, Martinello M, Rossi B, Merigo F, Ottoboni L, Bach S, Angiari S, Benati D, Chakir A, Zanetti L, Schio F, Osculati A, Marzola P, Nicolato E, Homeister JW, Xia L, Lowe JB, McEver RP, Osculati F, et al. (2008) A role for leukocyte-endothelial adhesion mechanisms in epilepsy. Nat Med 14:1377-1383.
20. Fanning AS, Anderson JM (2009) Zonula occludens-1 and -2 are cytosolic scaffolds that regulate the assembly of cellular junctions. Ann N Y Acad Sci 1165:113-120.
21. Feng Z, Zhang W, Hudson P, Bing G, Feng W, Hong JS (1997) Characterization of the long-lasting activator protein-1 complex induced by kainic acid treatment. Brain Res 770:53-59.
22. Feng Z, Chang RC, Bing G, Hudson P, Tiao N, Jin L, Hong JS (1999) Longterm increase of Sp-1 transcription factors in the hippocampus after kainic acid treatment. Brain Res Mol Brain Res 69:144-148.
23. Gavard J, Gutkind JS (2006) VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat Cell Biol 8:1223-1234.
24. Gerber HP, Condorelli F, Park J, Ferrara N (1997) Differential transcriptional regulation of the two vascular endothelial growth factor receptor genes. Flt-1, but not Flk-1/KDR, is up-regulated by hypoxia. J Biol Chem 272:23659-23667.
25. Ghosh C, Gonzalez-Martinez J, Hossain M, Cucullo L, Fazio V, Janigro D, Marchi N (2010) Pattern of P450 expression at the human blood-brain barrier: roles of epileptic condition and laminar flow. Epilepsia 51:1408-1417.
26. Harhaj NS, Antonetti DA (2004) Regulation of tight junctions and loss of barrier function in pathophysiology. Int J Biochem Cell Biol 36:1206-1237.
27. Holmes K, Roberts OL, Thomas AM, Cross MJ (2007) Vascular endothelial growth factor receptor-2: structure, function, intracellular signalling and therapeutic inhibition. Cell Signal 19:2003-2012.
28. Horowitz A, Simons M (2008) Branching morphogenesis. Circ Res 103:784-795.
29. Ivens S, Kaufer D, Flores LP, Bechmann I, Zumsteg D, Tomkins O, Seiffert E, Heinemann U, Friedman A (2007) TGF-beta receptor-mediated albumin uptake into astrocytes is involved in neocortical epileptogenesis. Brain 130:535-547.
30. Khirug S, Ahmad F, Puskarjov M, Afzalov R, Kaila K, Blaesse P (2010) A single seizure episode leads to rapid functional activation of KCC2 in the neonatal rat hippocampus. J Neurosci 30:12028-12035.
31. Koh JY, Choi DW (1987) Quantitative determination of glutamate mediated cortical neuronal injury in cell culture by lactate dehydrogenase efflux assay. J Neurosci Methods 20:83-90.
32. Kowanetz M, Ferrara N (2006) Vascular endothelial growth factor signaling pathways: therapeutic perspective. Clin Cancer Res 12:5018-5022.
33. Lampugnani MG, Orsenigo F, Gagliani MC, Tacchetti C, Dejana E (2006) Vascular endothelial cadherin controls VEGFR-2 internalization and signaling from intracellular compartments. J Cell Biol 174:593-604.
34. Lee SH, Chun W, Kong PJ, Han JA, Cho BP, Kwon OY, Lee HJ, Kim SS (2006) Sustained activation of Akt by melatonin contributes to the protection against kainic acid-induced neuronal death in hippocampus. J Pineal Res 40:79-85.
35. Marcon J, Gagliardi B, Balosso S, Maroso M, Noé F, Morin M, Lerner-Natoli M, Vezzani A, Ravizza T (2009) Age-dependent vascular changes induced by status epilepticus in rat forebrain: implications for epileptogenesis. Neurobiol Dis 34:121-132.
36. McCloskey DP, Croll SD, Scharfman HE (2005) Depression of synaptic transmission by vascular endothelial growth factor in adult rat hippocampus and evidence for increased efficacy after chronic seizures. J Neurosci 25:8889-8897.
37. Meissner M, Michailidou D, Stein M, Hrgovic I, Kaufmann R, Gille J (2009) Inhibition of Rac1 GTPase down-regulates vascular endothelial growth factor receptor-2 expression by suppressing Sp1-dependentDNAbinding in human endothelial cells. Exp Dermatol 18:863-869.
38. Moser KV, Schmidt-Kastner R, Hinterhuber H, Humpel C (2003) Brain capillaries and cholinergic neurons persist in organotypic brain slices in the absence of blood flow. Eur J Neurosci 18:85-94.
39. Ndode-Ekane XE, Hayward N, Gröhn O, Pitkänen A (2010) Vascular changes in epilepsy: functional consequences and association with network plasticity in pilocarpine-induced experimental epilepsy. Neuroscience 166:312-332.
40. Newton SS, Girgenti MJ, Collier EF, Duman RS (2006) Electroconvulsive seizure increases adult hippocampal angiogenesis in rats. Eur J Neurosci 24:819-828.
41. Nicoletti JN, Shah SK, McCloskey DP, Goodman JH, Elkady A, Atassi H, Hylton D, Rudge JS, Scharfman HE, Croll SD (2008) Vascular endothelial growth factor is up-regulated after status epilepticus and protects against seizure-induced neuronal loss in hippocampus. Neuroscience 151:232-241.
42. Petreaca ML, Yao M, Liu Y, Defea K, Martins-Green M (2007) Transactivation of vascular endothelial growth factor receptor-2 by interleukin-8 (IL-8/CXCL8) is required for IL-8/CXCL8-induced endothelial permeability. Mol Biol Cell 18:5014-5023.
43. Pitkänen A, Sutula TP (2002) Is epilepsy a progressive disorder? Prospects for new therapeutic approaches in temporal-lobe epilepsy. Lancet Neurol 1:173-181.
44. Proia P, Schiera G, Mineo M, Ingrassia AM, Santoro G, Savettieri G, Di Liegro I (2008) Astrocytes shed extracellular vesicles that contain fibroblast growth factor-2 and vascular endothelial growth factor. Int J Mol Med 21:63-67.
45. Ramsey MM, Adams MM, Ariwodola OJ, Sonntag WE, Weiner JL (2005) Functional characterization of des-IGF-1 action at excitatory synapses in the CA1 region of rat hippocampus. J Neurophysiol 94:247-254.
46. Ravizza T, Gagliardi B, Noé F, Boer K, Aronica E, Vezzani A (2008) Innate and adaptive immunity during epileptogenesis and spontaneous seizures: evidence from experimental models and human temporal lobe epilepsy. Neurobiol Dis 29:142-160.
47. 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 (2007) Angiogenesis is associated with blood-brain barrier permeability in temporal lobe epilepsy. Brain 130:1942-1956.
48. Sandoval KE, Witt KA (2008) Blood-brain barrier tight junction permeability and ischemic stroke. Neurobiol Dis 32:200-219.
49. Schiera G, Proia P, Alberti C, Mineo M, Savettieri G, Di Liegro I (2007) Neurons produce FGF2 and VEGF and secrete them at least in part by shedding extracellular vesicles. J Cell Mol Med 11:1384-1394.
50. Scholz W (1959) The contribution of patho-anatomical research to the problem of epilepsy Epilepsia 1:36-55.
51. Seiffert E, Dreier JP, Ivens S, Bechmann I, Tomkins O, Heinemann U, Friedman A (2004) Lasting blood-brain barrier disruption induces epileptic focus in the rat somatosensory cortex. J Neurosci 24:7829-7836.
52. Selvatici R, Marino S, Piubello C, Rodi D, Beani L, Gandini E, Siniscalchi A (2003) Protein kinase C activity, translocation, and selective isoform subcellular redistribution in the rat cerebral cortex after in vitro ischemia. J Neurosci Res 71:64-71.
53. Sheikpranbabu S, Kalishwaralal K, Venkataraman D, Eom SH, Park J, Gurunathan S (2009) Silver nanoparticles inhibit VEGF-and IL-1beta- induced vascular permeability via Src dependent pathway in porcine retinal endothelial cells. J Nanobiotechnology 7:8.
54. Spielmeyer W (1927) Die Pathogenese des epileptisches Krampfes, histopathologischer Teil. Ztschr Neurol Psychiatr 109:501-519.
55. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37:173-182.
56. Takenaga Y, Takagi N, Murotomi K, Tanonaka K, Takeo S (2009) Inhibition of Src activity decreases tyrosine phosphorylation of occludin in brain capillaries and attenuates increase in permeability of the bloodbrain barrier after transient focal cerebral ischemia. J Cereb Blood Flow Metab 29:1099-1108.
57. Tomkins O, Friedman O, Ivens S, Reiffurth C, Major S, Dreier JP, Heinemann U, Friedman A (2007) Blood-brain barrier disruption results in delayed functional and structural alterations in the rat neocortex. Neurobiol Dis 25:367-377.
58. van Vliet EA, da Costa Araú jo S, Redeker S, van Schaik R, Aronica E, Gorter JA (2007) Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy. Brain 130:521-534.
59. Vezzani A, Balosso S, Ravizza T (2008) The role of cytokines in the pathophysiology of epilepsy. Brain Behav Immun 22:797-803.
60. Zhang Z, Chopp M (2002) Vascular endothelial growth factor and angiopoietins in focal cerebral ischemia. Trends Cardiovasc Med 12:62-66.
61. Zlokovic BV (2008) The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 57:178-201.