The MAP kinase pathway mediates transcytosis induced by TNF-α in an in vitro blood-brain barrier model

European Journal of Neuroscience

Volumn 22, Issue 4, 2005, Pages 835-844

  Miller, Florence ^a   Fenart, Laurence ^a   Landry, Valérie ^a   Coisne, Caroline ^a   Cecchelli, Roméo ^a   Dehouck, Marie Pierre ^a   Buée Scherrer, Valérie ^a  

^a UNIVERSITÉ D'ARTOIS   (France)

Author keywords

Bovine; Caveolae; Co culture; Endothelial cells; Inflammation; Rat

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; MANNITOL; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN P42; PROTEIN P44; TRANSFERRIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; BLOOD BRAIN BARRIER; CAPILLARY FLOW; CELL TRANSPORT; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ANALYSIS; GLIA CELL; IN VITRO STUDY; INFLAMMATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; TRANSCYTOSIS;

ACTINS; ANIMALS; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; BLOTTING, WESTERN; BUTADIENES; CATTLE; CELLS, CULTURED; COCULTURE TECHNIQUES; DRUG INTERACTIONS; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; ENZYME INHIBITORS; IMMUNOHISTOCHEMISTRY; MANNITOL; MEMBRANE PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 11; MITOGEN-ACTIVATED PROTEIN KINASE 8; MITOGEN-ACTIVATED PROTEIN KINASES; NEUROGLIA; NITRILES; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 24144476258     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.04273.x     Document Type: Article

References (69)

1. Alessi, D.R., Cuenda, A., Cohen, P., Dudley, D.T. & Saltiel, A.R. (1995) PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J. Biol. Chem., 270, 27489-27494.
2. Amrani, Y., Ammit, A.J. & Panettieri Ra, J.R. (2001) Tumor necrosis factor receptor (TNFR) 1, but not TNFR2, mediates tumor necrosis factor-alpha-induced interleukin-6 and RANTES in human airway smooth muscle cells: role of p38 and p42/44 mitogen-activated protein kinases. Mol. Pharmacol., 60, 646-655.
3. Annunziata, P., Cioni, C., Santonini, R. & Paccagnini, E. (2002) Substance P antagonist blocks leakage and reduces activation of cytokine-stimulated rat brain endothelium. J. Neuroimmunol., 131, 41-49.
4. Betz, A.L., Firth, J.A. & Goldstein, G.W. (1980) Polarity of the blood-brain barrier: distribution of enzymes between the luminal and antiluminal membranes of brain capillary endothelial cells. Brain Res., 192, 17-28.
5. Bornstein, M.B. (1958) Reconstituted rattail collagen used as substrate for tissue cultures on coverslips in Maximow slides and roller tubes. Lab. Invest., 7, 134-137.
6. Boulton, T.G., Gregory, J.S. & Cobb, M.H. (1991a) Purification and properties of extracellular signal-regulated kinase 1, an insulin-stimulated microtubule-associated protein 2 kinase. Biochemistry, 30, 278-286.
7. Boulton, T.G., Nye, S.H., Robbins, D.J., Ip, N.Y., Radziejewska, E., Morgenbesser, S.D., Depinho, R.A., Panayotatos, N., Cobb, M.H. & Yancopoulos, G.D. (1991b) ERKs: a family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF. Cell, 65, 663-675.
8. Brillault, J., Berezowski, V., Cecchelli, R. & Dehouck, M.P. (2002) Intercommunications between brain capillary endothelial cells and glial cells increase the transcellular permeability of the blood-brain barrier during ischaemia. J. Neurochem., 83, 807-817.
9. Carpentier, M., Descamps, L., Allain, F., Denys, A., Durieux, S., Fenart, L., Kieda, C., Cecchelli, R. & Spik, G. (1999) Receptor-mediated transcytosis of cyclophilin B through the blood-brain barrier. J. Neurochem., 73, 260-270.
10. Cecchelli, R., Dehouck, B., Descamps, L., Fenart, L., Buee Scherrer, V., Duhem, C., Lundquist, S., Rentfel, M., Torpier, G. & Dehouck, M.P. (1999) In vitro model for evaluating drug transport across the blood-brain barrier. Adv. Drug Deliv. Rev., 36, 165-178.
11. Cohen, P. (1997) The search for physiological substrates of MAP and SAP kinases in mammalian cells. Trends Cell Biol., 7, 295-305.
12. Cuenda, A., Cohen, P., Buee Scherrer, V. & Goedert, M. (1997) Activation of stress-activated protein kinase-3 (SAPK3) by cytokines and cellular stresses is mediated via SAPKK3 (MKK6); comparison of the specificities of SAPK3 and SAPK2 (RK/p38). EMBO J., 16, 295-305.
13. D'Alessio, A., Al Lamki, R.S., Bradley, J.R. & Pober, J.S. (2005) Caveolae participate in tumor necrosis factor receptor 1 signaling and internalization in a human endothelial cell line. Am. J. Pathol., 166, 1273-1282.
14. De Vries, H.E., Blom Roosemalen, M.C., Van Oosten, M., de Boer, A.G., Van Berkel, T.J., Breimer, D.D. & Kuiper, J. (1996) The influence of cytokines on the integrity of the blood-brain barrier in vitro. J. Neuroimmunol., 64, 37-43.
15. Dehouck, B., Dehouck, M.P., Fruchart, J.C. & Cecchelli, R. (1994) Upregulation of the low density lipoprotein receptor at the blood-brain barrier: intercommunications between brain capillary endothelial cells and astrocytes. J. Cell. Biol., 126, 465-473.
16. Dehouck, B., Fenart, L., Dehouck, M.P., Pierce, A., Torpier, G. & Cecchelli, R. (1997) A new function for the LDL receptor: transcytosis of LDL across the blood-brain barrier. J. Cell. Biol., 138, 877-889.
17. Dehouck, M.P., Jolliet Riant, P., Bree, F., Fruchart, J.C., Cecchelli, R. & Tillement, J.P. (1992) Drug transfer across the blood-brain barrier: correlation between in vitro and in vivo models. J. Neurochem., 58, 1790-1797.
18. Dehouck, M.P., Méresse, S., Delorme, P., Fruchart, J.C. & Cecchelli, R. (1990) An easier, reproducible, and mass-production method to study the blood-brain barrier in vitro. J. Neurochem., 54, 1798-1801.
19. Deli, M.A., Abraham, C.S., Kataoka, Y. & Niwa, N. (2005) Permeability studies on in vitro blood-brain barrier models: physiology, pathology, and pharmacology. Cell. Mol. Neurobiol., 25, 59-127.
20. Deli, M.A., Descamps, L., Dehouck, M.P., Cecchelli, R., Joo, F., Abraham, C.S. & Torpier, G. (1995) Exposure of tumor necrosis factor-alpha to luminal membrane of bovine brain capillary endothelial cells cocultured with astrocytes induces a delayed increase of permeability and cytoplasmic stress fiber formation of actin. J. Neurosci. Res., 41, 717-726.
21. Demeule, M., Poirier, J., Jodoin, J., Bertrand, Y., Desrosiers, R.R., Dagenais, C., Nguyen, T., Lanthier, J., Gabathuler, R., Kennard, M., Jefferies, W.A., Karkan, D., Tsai, S., Fenart, L., Cecchelli, R. & Beliveau, R. (2002) High transcytosis of melanotransferrin (P97) across the blood-brain barrier. J. Neurochem., 83, 924-933.
22. Derijard, B., Hibi, M., Wu, I.H., Barrett, T., Su, B., Deng, T, Karin, M. & Davis, R.J. (1994) JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell, 76, 1025-1037.
23. Descamps, L., Cecchelli, R. & Torpier, G. (1997) Effects of tumor necrosis factor on receptor-mediated endocytosis and barrier functions of bovine brain capillary endothelial cell monolayers. J. Neuroimmunol., 74, 173-184.
24. Descamps, L., Dehouck, M.P., Torpier, G. & Cecchelli, R. (1996) Receptor-mediated transcytosis of transferrin through blood-brain barrier endothelial cells. Am. J. Physiol., 270, H1149-H1158.
25. Dobbie, M.S., Hurst, R.D., Klein, N.J. & Surtees, R.A. (1999) Upregulation of intercellular adhesion molecule-1 expression on human endothelial cells by tumor necrosis factor-alpha in an in vitro model of the blood-brain barrier. Brain Res., 830, 330-336.
26. Engelman, J.A., Berg, A.H., Lewis, R.Y., Lisanti, M.P. & Scherer, P.E. (2000) Tumor necrosis factor alpha-mediated insulin resistance, but not dedifferentiation, is abrogated by MEK1/2 inhibitors in 3T3-L1 adipocytes. Mol. Endocrinol., 14, 1557-1569.
27. Favata, M.F., Horiuchi, K.Y., Manos, E.J., Daulerio, A.J., Stradley, D.A., Feeser, W.S., Van Dyk, D.E., Pitts, W.J., Earl, R.A., Hobbs, F., Copeland, R.A., Magolda, R.L., Scherle, P.A. & Trzaskos, J.M. (1998) Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chem., 273, 18623-18632.
28. Fenart, L., Buee Scherrer, V., Descamps, L., Duhem, C., Poullain, M.G., Cecchelli, R. & Dehouck, M.P. (1998) Inhibition of P-glycoprotein: rapid assessment of its implication in blood-brain barrier integrity and drug transport to the brain by an in vitro model of the blood-brain barrier. Pharm. Res., 15, 993-1000.
29. Fillebeen, C., Dehouck, B., Benaissa, M., Dhennin Duthille, I., Cecchelli, R. & Pierce, A. (1999a) Tumor necrosis factor-alpha increases lactoferrin transcytosis through the blood-brain barrier. J. Neurochem., 73, 2491-2500.
30. Fillebeen, C., Descamps, L., Dehouck, M.P., Fenart, L., Benaissa, M., Spik, G., Cecchelli, R. & Pierce, A. (1999b) Receptor-mediated transcytosis of lactoferrin through the blood-brain barrier. J. Biol. Chem., 274, 7011-7017.
31. Fillit, H., Ding, W.H., Buee, L., Kalman, J., Altstiel, L., Lawlor, B. & Wolf Klein, G. (1991) Elevated circulating tumor necrosis factor levels in Alzheimer's disease. Neurosci. Lett., 129, 318-320.
32. Goueli, S.A. & Jarvis, B.W. (2001) Phospho-specific mitogen-activated protein kinase antibodies for ERK, JNK, and p38 activation. Meth. Enzymol., 332, 337-343.
33. Grau, G.E., Fajardo, L.F., Piguet, P.F., Allet, B., Lambert, P.H. & Vassalli, P. (1987) Tumor necrosis factor (cachectin) as an essential mediator in murine cerebral malaria. Science, 237, 1210-1212.
34. Gupta, S., Barrett, T., Whitmarsh, A.J., Cavanagh, J., Sluss, H.K., Derijard, B. & Davis, R.J. (1996) Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J., 15, 2760-2770.
35. Hiesiger, E.M., Voorhies, R.M., Basler, G.A., Lipschutz, L.E., Posner, J.B. & Shapiro, W.R. (1986) Opening the blood-brain and blood-tumor barriers in experimental rat brain tumors: the effect of intracarotid hyperosmolar mannitol on capillary permeability and blood flow. Ann. Neurol., 19, 50-59.
36. Huber, J.D., Egleton, R.D. & Davis, T.P. (2001) Molecular physiology and pathophysiology of tight junctions in the blood-brain barrier. Trends Neurosci., 24, 719-725.
37. Hurst, R.D. & Clark, J.B. (1997) Nitric oxide-induced blood-brain barrier dysfunction is not mediated by inhibition of mitochondrial respiratory chain activity and/or energy depletion. Nitric Oxide, 1, 121-129.
38. Kermode, A.G., Thompson, A.J., Tofts, P., MacManus, D.G., Kendall, B.E., Kingsley, O.P., Moseley, I.F., Rudge, P. & McDonald, W.I. (1990) Breakdown of the blood-brain barrier precedes symptoms and other MRI signs of new lesions in multiple sclerosis. Pathogenetic and clinical implications. Brain, 113, 1477-1489.
39. Kyriakis, J.M., Banerjee, P., Nikolakaki, E., Dai, T., Rubie, E.A., Ahmad, M.F., Avruch, J. & Woodgett, J.R. (1994) The stress-activated protein kinase subfamily of c-Jun kinases. Nature, 369, 156-160.
40. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
41. Leist, T.P., Frei, K., Kam Hansen, S., Zinkernagel, R.M. & Fontana, A. (1988) Tumor necrosis factor alpha in cerebrospinal fluid during bacterial, but not viral, meningitis. Evaluation in murine model infections and in patients. J. Exp. Med., 167, 1743-1748.
42. Lou, J., Gasche, Y., Zheng, L., Critico, B., Monso Hinard, C., Juillard, P., Morel, P., Buurman, W.A. & Grau, G.E. (1998) Differential reactivity of brain microvascular endothelial cells to TNF reflects the genetic susceptibility to cerebral malaria. Eur. J. Immunol., 28, 3989-4000.
43. Lucas, R., Garcia, I., Donati, Y.R., Hribar, M., Mandriota, S.J., Giroud, C., Buurman, W.A., Fransen, L., Suter, P.M., Nunez, G., Pepper, M.S. & Grau, G.E. (1998) Both TNF receptors are required for direct TNF-mediated cytotoxicity in microvascular endothelial cells. Eur. J. Immunol., 28, 3577-3586.
44. Lucas, R., Lou, J.N., Juillard, P., Moore, M., Bluethmann, H. & Grau, G.E. (1997) Respective role of TNF receptors in the development of experimental cerebral malaria. J. Neuroimmunol., 72, 143-148.
45. Lundquist, S., Renftel, M., Brillault, J., Fenart, L., Cecchelli, R. & Dehouck, M.P. (2002) Prediction of drug transport through the blood-brain barrier in vivo: a comparison between two in vitro cell models. Pharm. Res., 19, 976-981.
46. MacEwan, D.J. (2002) TNF receptor subtype signalling: differences and cellular consequences. Cell Signal., 14, 477-492.
47. Mark, K.S. & Miller, D.W. (1999) Increased permeability of primary cultured brain microvessel endothelial cell monolayers following TNF-alpha exposure. Life Sci., 64, 1941-1953.
48. Mark, K.S., Trickler, W.J. & Miller, D.W. (2001) Tumor necrosis factor-alpha induces cyclooxygenase-2 expression and prostaglandin release in brain microvessel endothelial cells. J. Pharmacol. Exp. Ther., 297, 1051-1058.
49. Mecocci, P., Parnetti, L., Reboldi, G.P., Santucci, C., Gaiti, A., Ferri, C., Gemini, I., Romagnoli, M., Cadini, D. & Senin, U. (1991) Blood-brain barrier in a geriatric population: barrier function in degenerative and vascular dementias. Acta Neurol. Scand., 84, 210-213.
50. Méresse, S., Dehouck, M.P., Delorme, P., Bensaid, M., Tauber, J.P., Delbart, C., Fruchart, J.C. & Cecchelli, R. (1989) Bovine brain endothelial cells express tight junctions and monoamine oxidase activity in long-term culture. J. Neurochem., 53, 1363-1371.
51. Mogi, M., Harada, M., Riederer, P., Narabayashi, H., Fujita, K. & Nagatsu, T. (1994) Tumor necrosis factor-alpha (TNF-alpha) increases both in the brain and in the cerebrospinal fluid from parkinsonian patients. Neurosci. Lett., 165, 208-210.
52. Pan, W. & Kastin, A.J. (2002) TNFalpha transport across the blood-brain barrier is abolished in receptor knockout mice. Exp. Neurol., 174, 193-200.
53. Pardridge, W.M., Buciak, J.L. & Friden, P.M. (1991) Selective transport of an anti-transferrin receptor antibody through the blood-brain barrier in vivo. J. Pharmacol. Exp. Ther., 259, 66-70.
54. Parton, R.G., Joggerst, B. & Simons, K. (1994) Regulated internalization of caveolae. J. Cell. Biol., 127, 1199-1215.
55. Payne, D.M., Rossomando, A.J., Martino, P., Erickson, A.K., Her, J.H., Shabanowitz, J., Hunt, D.F., Weber, M.J. & Sturgill, T.W. (1991) Identification of the regulatory phosphorylation sites in pp42/mitogen-activated protein kinase (MAP kinase). EMBO J., 10, 885-892.
56. Pearson, G., Robinson, F., Beers Gibson, T., Xu, B.E., Karandikar, M., Berman, K. & Cobb, M.H. (2001) Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev., 22, 153-183.
57. Peterson, G.L. (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem., 83, 346-356.
58. Petito, C.K. & Cash, K.S. (1992) Blood-brain barrier abnormalities in the acquired immunodeficiency syndrome: immunohistochemical localization of serum proteins in postmortem brain. Ann. Neurol., 32, 658-666.
59. Plateel, M., Dehouck, M.P., Torpier, G., Cecchelli, R. & Teissier, E. (1995) Hypoxia increases the susceptibility to oxidant stress and the permeability of the blood-brain barrier endothelial cell monolayer. J. Neurochem., 65, 2138-2145.
60. Prieto, P., Blaauboer, B.J., de Boer, A.G., Boveri, M., Cecchelli, R., Clemedson, C., Coecke, S., Forsby, A., Galla, H.J., Garberg, P., Greenwood, J., Price, A. & Tahti, H. (2004) Blood-brain barrier in vitro models and their application in toxicology. The report and recommendations of ECVAM Workshop 49. ATLA, 32, 37-50.
61. Rapoport, S.I. & Robinson, P.J. (1986) Tight-junctional modification as the basis of osmotic opening of the blood-brain barrier. Ann. N. Y. Acad. Sci., 481, 250-267.
62. Reese, T.S. & Karnovsky, M.J. (1967) Fine structural localization of a blood-brain barrier to exogenous peroxidase. J. Cell. Biol., 34, 207-217.
63. Sibson, N.R., Blamire, A.M., Perry, V.H., Gauldie, J., Styles, P. & Anthony, B.C. (2002) TNF-alpha reduces cerebral blood volume and disrupts tissue homeostasis via an endothelin- and TNFR2-dependent pathway. Brain, 125, 2446-2459.
64. Siflinger Birnboim, A., Del Vecchio, P.J., Cooper, J.A., Blumenstock, F.A., Shepard, J.M. & Malik, A.B. (1987) Molecular sieving characteristics of the cultured endothelial monolayer. J. Cell. Physiol., 132, 111-117.
65. Tuomanen, E., Tomasz, A., Hengstler, B. & Zak, O. (1985) The relative role of bacterial cell wall and capsule in the induction of inflammation in pneumococcal meningitis. J. Infect. Dis., 151, 535-540.
66. Volmat, V., Camps, M., Arkinstall, S., Pouyssegur, J. & Lenormand, P. (2001) The nucleus, a site for signal termination by sequestration and inactivation of p42/p44 MAP kinases. J. Cell. Sci., 114, 3433-3443.
67. Waage, A., Halstensen, A., Shalaby, R., Brandtzaeg, P., Kierulf, P. & Espevik, T. (1989) Local production of tumor necrosis factor alpha, interleukin 1, and interleukin 6 in meningococcal meningitis. Relation to the inflammatory response. J. Exp. Med., 170, 1859-1867.
68. Wallach, D., Varfolomeev, E.E., Malini, M.L., Goltsey, Y.V., Kovalenko, A.V. & Boldin, M.P. (1999) Tumor necrosis factor receptor and Fas signaling mechanisms. Annu. Rev. Immunol., 17, 331-367.
69. Wang, Y., Zhang, J., Yi, X.J. & Yu, F.S. (2004) Activation of ERK1/2 MAP kinase pathway induces tight junction disruption in human corneal epithelial cells. Exp. Eye Res., 78, 125-136.