TWEAK/Fn14 pathway modulates properties of a human microvascular endothelial cell model of blood brain barrier

Journal of Neuroinflammation

Volumn 10, Issue , 2013, Pages

  Stephan, Delphine ^a   Sbai, Oualid ^a   Wen, Jing ^b   Couraud, Pierre Olivier ^c   Putterman, Chaim ^b   Khrestchatisky, Michel ^a   Desplat Jégo, Sophie ^a  

^a Mediterranée University   (France)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c INSTITUT COCHIN   (France)

Author keywords

CCL 2; hCMEC D3; HMEC; IL 8; MMP 9; Neuroinflammation; TNFSF12; ZO 1

Indexed keywords

CELL ADHESION MOLECULE; GELATINASE B; PROTEIN FN14; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR LIKE WEAK INDUCER OF APOPTOSIS PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; BLOOD BRAIN BARRIER; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; ENZYME SYNTHESIS; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; MEMBRANE PERMEABILITY; MICROVASCULAR ENDOTHELIAL CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

EID: 84872122183     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-10-9     Document Type: Article

References (60)

1. Chicheportiche Y, Bourdon PR, Xu H, Hsu YM, Scott H, Hession C, Garcia I, Browning JL. TWEAK, a new secreted ligand in the tumor necrosis factor family that weakly induces apoptosis. J Biol Chem 1997, 272:32401-32410. 10.1074/jbc.272.51.32401, 9405449.
2. Zhao Z, Burkly LC, Campbell S, Schwartz N, Molano A, Choudhury A, Eisenberg RA, Michaelson JS, Putterman C. TWEAK/Fn14 interactions are instrumental in the pathogenesis of nephritis in the chronic graft-versus-host model of systemic lupus erythematosus. J Immunol 2007, 179:7949-7958.
3. van Kuijk AWR, Wijbrandts CA, Vinkenoog M, Zheng TS, Reedquist KA, Tak PP. TWEAK and its receptor Fn14 in the synovium of patients with rheumatoid arthritis compared to psoriatic arthritis and its response to tumour necrosis factor blockade. Ann Rheum Dis 2010, 69:301-304. 10.1136/ard.2008.090548, 2789939, 19147618.
4. Dohi T, Burkly LC. The TWEAK/Fn14 pathway as an aggravating and perpetuating factor in inflammatory diseases: focus on inflammatory bowel diseases. J Leukoc Biol 2012, 92:265-279. 10.1189/jlb.0112042, 22672874.
5. Michaelson JS, Wisniacki N, Burkly LC, Putterman C. Role of TWEAK in lupus nephritis: a bench-to-bedside review. J Autoimmun 2012, 39:130-142. 10.1016/j.jaut.2012.05.003, 22727560.
6. Burkly LC, Michaelson JS, Zheng TS. TWEAK/Fn14 pathway: an immunological switch for shaping tissue responses. Immunol Rev 2011, 244:99-114. 10.1111/j.1600-065X.2011.01054.x, 22017434.
7. Lynch C, Wang Y, Lund J, Chen Y. TWEAK induces angiogenesis and proliferation of endothelial cells. J Biol Chem 1999, 274:8455-8459. 10.1074/jbc.274.13.8455, 10085077.
8. Jakubowski A, Browning B, Lukashev M, Sizing I, Thompson JS, Benjamin CD, Hsu Y-M, Ambrose C, Zheng TS, Burkly LC. Dual role for TWEAK in angiogenic regulation. J Cell Sci 2002, 115:267-274.
9. Desplat-Jégo S, Varriale S, Creidy R, Terra R, Bernard D, Khrestchatisky M, Izui S, Chicheportiche Y, Boucraut J. TWEAK is expressed by glial cells, induces astrocyte proliferation and increases EAE severity. J Neuroimmunol 2002, 133:116-123. 10.1016/S0165-5728(02)00368-5, 12446014.
10. Desplat-Jégo S, Creidy R, Varriale S, Allaire N, Luo Y, Bernard D, Hahm K, Burkly L, Boucraut J. Anti-TWEAK monoclonal antibodies reduce immune cell infiltration in the central nervous system and severity of experimental autoimmune encephalomyelitis. Clin Immunol 2005, 117:15-23. 10.1016/j.clim.2005.06.005, 16027043.
11. Saas P, Boucraut J, Walker P, Quiquerez A. TWEAK stimulation of astrocytes and the proinflammatory consequences. Glia 2000, 32:102-107. 10.1002/1098-1136(200010)32:1<102::AID-GLIA100>3.0.CO;2-U, 10975915.
12. Polavarapu R, Gongora MC, Winkles J, Yepes M. Tumor necrosis factor-like weak inducer of apoptosis increases the permeability of the neurovascular unit through nuclear factor-kappa B pathway activation. J Neurosci 2005, 25:10094-10100. 10.1523/JNEUROSCI.3382-05.2005, 16267216.
13. Romanic AM, Madri JA. The induction of 72-kD gelatinase in T cells upon adhesion to endothelial cells is VCAM-1 dependent. J Cell Biol 1994, 125:1165-1178. 10.1083/jcb.125.5.1165, 2120055, 7515069.
14. Rosenberg GA, Dencoff JE, Correa N, Reiners M, Ford CC. Effect of steroids on CSF matrix metalloproteinases in multiple sclerosis: relation to blood-brain barrier injury. Neurology 1996, 46:1626-1632. 10.1212/WNL.46.6.1626, 8649561.
15. Asahi M, Asahi K, Jung JC, del Zoppo GJ, Fini ME, Lo EH. Role for matrix metalloproteinase 9 after focal cerebral ischemia: effects of gene knockout and enzyme inhibition with BB-94. J Cerebr Blood F Met 2000, 20:1681-1689.
16. Asahi M, Wang X, Mori T, Sumii T, Jung JC, Moskowitz MA, Fini ME, Lo EH. Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J Neurosci 2001, 21:7724-7732.
17. Yepes M, Brown SAN, Moore EG, Smith EP, Lawrence DA, Winkles JA. A soluble Fn14-Fc decoy receptor reduces infarct volume in a murine model of cerebral ischemia. Am J Pathol 2005, 166:511-520. 10.1016/S0002-9440(10)62273-0, 1602337, 15681834.
18. Yepes M. TWEAK and FN14 in central nervous system health and disease. Front Biosci 2007, 12:2772-2781.
19. Yepes M. TWEAK and the central nervous system. Mol Neurobiol 2007, 35:255-265. 10.1007/s12035-007-0024-z, 17917114.
20. Echeverry R, Wu F, Haile WB, Wu J, Yepes M. The cytokine tumor necrosis factor-like weak inducer of apoptosis and its receptor fibroblast growth factor-inducible 14 have a neuroprotective effect in the central nervous system. J Neuroinflammation 2012, 9:45. 10.1186/1742-2094-9-45, 3311607, 22394384.
21. Serafini B, Magliozzi R, Rosicarelli B, Reynolds R, Zheng TS, Aloisi F. Expression of TWEAK and its receptor Fn14 in the multiple sclerosis brain: implications for inflammatory tissue injury. J Neuropathol Exp Neurol 2008, 67:1137-1148. 10.1097/NEN.0b013e31818dab90, 19018248.
22. Desplat-Jégo S, Feuillet L, Creidy R, Malikova I, Rance R, Khrestchatisky M, Hahm K, Burkly LC, Pelletier J, Boucraut J. TWEAK is expressed at the cell surface of monocytes during multiple sclerosis. J Leukoc Biol 2009, 85:132-135.
23. Weksler BB, Subileau E, Perrière N, Charneau P, Holloway K, Leveque M, Tricoire-Leignel H, Nicotra A, Bourdoulous S, Turowski P, Male DK, Roux F, Greenwood J, Romero IA, Couraud PO. Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J 2005, 19:1872-1874.
24. Rivera S, Ogier C, Jourquin J, Timsit S, Szklarczyk AW, Miller K, Gearing AJH, Kaczmarek L, Khrestchatisky M. Gelatinase B and TIMP-1 are regulated in a cell- and time-dependent manner in association with neuronal death and glial reactivity after global forebrain ischemia. Eur J Neurosci 2002, 15:19-32. 10.1046/j.0953-816x.2001.01838.x, 11860503.
25. Sbai O, Ferhat L, Bernard A, Gueye Y, Ould-Yahoui A, Thiolloy S, Charrat E, Charton G, Tremblay E, Risso J-J, Chauvin J-P, Arsanto J-P, Rivera S, Khrestchatisky M. Vesicular trafficking and secretion of matrix metalloproteinases-2, -9 and tissue inhibitor of metalloproteinases-1 in neuronal cells. Mol Cell Neurosci 2008, 39:549-568. 10.1016/j.mcn.2008.08.004, 18817873.
26. Yilmaz MI, Carrero JJ, Ortiz A, Martín-Ventura JL, Sonmez A, Saglam M, Yaman H, Yenicesu M, Egido J, Blanco-Colio LM. Soluble TWEAK plasma levels as a novel biomarker of endothelial function in patients with chronic kidney disease. Clin J Am Soc Nephro: CJASN 2009, 4:1716-1723.
27. Li H, Mittal A, Paul PK, Kumar M, Srivastava DS, Tyagi SC, Kumar A. Tumor necrosis factor-related weak inducer of apoptosis augments matrix metalloproteinase 9 (MMP-9) production in skeletal muscle through the activation of nuclear factor-kappaB-inducing kinase and p38 mitogen-activated protein kinase: a potential role of MMP-9 in myopathy. J Biol Chem 2009, 284:4439-4450. 2640955, 19074147.
28. Kumar M, Makonchuk DY, Li H, Mittal A, Kumar A. TNF-like weak inducer of apoptosis (TWEAK) activates proinflammatory signaling pathways and gene expression through the activation of TGF-beta-activated kinase 1. J Immunol 2009, 182:2439-2448. 10.4049/jimmunol.0803357, 2652039, 19201899.
29. Sbai O, Ould-Yahoui A, Ferhat L, Gueye Y, Bernard A, Charrat E, Mehanna A, Risso J-J, Chauvin J-P, Fenouillet E, Rivera S, Khrestchatisky M. Differential vesicular distribution and trafficking of MMP-2, MMP-9, and their inhibitors in astrocytes. Glia 2010, 58:344-366.
30. Asahi M, Wang X, Mori T, Sumii T, Jung JC, Moskowitz M, Fini ME, Lo EH. Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J Neurosci 2001, 21:7724-7732.
31. Winkles JA. The TWEAK-Fn14 cytokine-receptor axis: discovery, biology and therapeutic targeting. Nat Rev Drug Discov 2008, 7:411. 10.1038/nrd2488, 3018765, 18404150.
32. Potrovita I, Zhang W, Burkly L, Hahm K, Lincecum J, Wang MZ, Maurer MH, Rossner M, Schneider A, Schwaninger M. Tumor necrosis factor-like weak inducer of apoptosis-induced neurodegeneration. J Neurosci 2004, 24:8237-8244. 10.1523/JNEUROSCI.1089-04.2004, 15385607.
33. Garcia JH, Lossinsky AS, Kauffman FC, Conger KA. Neuronal ischemic injury: light microscopy, ultrastructure and biochemistry. Acta Neuropathol 1978, 43:85-95. 10.1007/BF00685002, 97917.
34. Hawkins CP, Mackenzie F, Tofts P, du Boulay EP, McDonald WI. Patterns of blood-brain barrier breakdown in inflammatory demyelination. Brain 1991, 114(Pt 2):801-810.
35. Banks WA, DiPalma CR, Farrell CL. Impaired transport of leptin across the blood-brain barrier in obesity. Peptides 1999, 20:1341-1345. 10.1016/S0196-9781(99)00139-4, 10612449.
36. Yepes M, Sandkvist M, Moore EG, Bugge TH, Strickland DK, Lawrence DA. Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein. J Clin Invest 2003, 112:1533-1540. 259131, 14617754.
37. Ballabh P, Braun A, Nedergaard M. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol Dis 2004, 16:1-13. 10.1016/j.nbd.2003.12.016, 15207256.
38. Engelhardt B. Immune cell entry into the central nervous system: involvement of adhesion molecules and chemokines. J Neurol Sci 2008, 274:23-26. 10.1016/j.jns.2008.05.019, 18573502.
39. Stamatovic SM, Keep RF, Kunkel SL, Andjelkovic AV. Potential role of MCP-1 in endothelial cell tight junction " opening" : signaling via Rho and Rho kinase. J Cell Sci 2003, 116:4615-4628. 10.1242/jcs.00755, 14576355.
40. Stamatovic SM, Shakui P, Keep RF, Moore BB, Kunkel SL, Van Rooijen N, Andjelkovic AV. Monocyte chemoattractant protein-1 regulation of blood-brain barrier permeability. J Cerebr Blood F Met 2005, 25:593-606.
41. Dimitrijevic OB, Stamatovic SM, Keep RF, Andjelkovic AV. Effects of the chemokine CCL2 on blood-brain barrier permeability during ischemia-reperfusion injury. J Cerebr Blood F Met 2006, 26:797-810.
42. Yao Y, Tsirka SE. Truncation of monocyte chemoattractant protein 1 by plasmin promotes blood-brain barrier disruption. J Cell Sci 2011, 124:1486-1495. 10.1242/jcs.082834, 3078815, 21486949.
43. Chicheportiche Y, Chicheportiche R, Sizing I, Thompson J, Benjamin CB, Ambrose C, Dayer J-M. Proinflammatory activity of TWEAK on human dermal fibroblasts and synoviocytes: blocking and enhancing effects of anti-TWEAK monoclonal antibodies. Arthritis Res 2002, 4:126-133. 10.1186/ar388, 83846, 11879548.
44. Wako M, Haro H, Ando T, Hatsushika K, Ohba T, Iwabuchi S, Nakao A, Hamada Y. Novel function of TWEAK in inducing intervertebral disc degeneration. J Orthop Res 2007, 25:1438-1446. 10.1002/jor.20445, 17568422.
45. Kim SH, Kang YJ, Kim WJ, Woo DK, Lee Y, Kim DI, Park YB, Kwon BS, Park J, Lee WH. TWEAK can induce pro-inflammatory cytokines and matrix metalloproteinase-9 in macrophages. Circ J 2004, 68:396-399. 10.1253/circj.68.396, 15056843.
46. Gasche Y, Copin JC, Sugawara T, Fujimura M, Chan PH. Matrix metalloproteinase inhibition prevents oxidative stress-associated blood-brain barrier disruption after transient focal cerebral ischemia. J Cerebr Blood F Met 2001, 21:1393-1400.
47. Ould-yahoui A, Tremblay E, Sbai O, Ferhat L, Bernard A, Charrat E, Gueye Y, Lim NH, Brew K, Risso J-J, Dive V, Khrestchatisky M, Rivera S. A new role for TIMP-1 in modulating neurite outgrowth and morphology of cortical neurons. PLoS One 2009, 4:e8289. 10.1371/journal.pone.0008289, 2788270, 20011518.
48. Yu Q, Stamenkovic I. Localization of matrix metalloproteinase 9 to the cell surface provides a mechanism for CD44-mediated tumor invasion. Genes Dev 1999, 13:35-48. 10.1101/gad.13.1.35, 316376, 9887098.
49. Monferran S, Paupert J, Dauvillier S, Salles B, Muller C. The membrane form of the DNA repair protein Ku interacts at the cell surface with metalloproteinase 9. EMBO J 2004, 23:3758-3768. 10.1038/sj.emboj.7600403, 522801, 15385961.
50. Donohue PJ, Richards CM, Brown SN, Hanscom HN, Buschman J, Thangada S, Hla T, Williams MS, Winkles JA. TWEAK is an endothelial cell growth and chemotactic factor that also potentiates FGF-2 and VEGF-A mitogenic activity. Arterioscler Thromb Vasc Biol 2003, 23:594-600. 10.1161/01.ATV.0000062883.93715.37, 12615668.
51. Han S, Yoon K, Lee K, Kim K, Jang H, Lee NK, Hwang K, Young Lee S. TNF-related weak inducer of apoptosis receptor, a TNF receptor superfamily member, activates NF-κB through TNF receptor-associated factors. Biochem Biophys Res Commun 2003, 305:789-796. 10.1016/S0006-291X(03)00852-0, 12767899.
52. Schneider P, Schwenzer R, Haas E, M\" uhlenbeck F, Schubert G, Scheurich P, Tschopp J, Wajant H. TWEAK can induce cell death via endogenous TNF and TNF receptor 1 - Schneider. Eur J Immunol 1999, 29:1785-1792. 10.1002/(SICI)1521-4141(199906)29:06<1785::AID-IMMU1785>3.0.CO;2-U, 10382740.
53. Zhang D, Wood CE. Neuronal prostaglandin endoperoxide synthase 2 responses to oxygen and glucose deprivation are mediated by mitogen-activated protein kinase ERK1/2. Brain Res 2005, 1060:100-107. 10.1016/j.brainres.2005.08.033, 16185670.
54. Nonaka M, Chen XH, Pierce JE, Leoni MJ, McIntosh TK, Wolf JA, Smith DH. Prolonged activation of NF-kappaB following traumatic brain injury in rats. J Neurotrauma 1999, 16:1023-1034. 10.1089/neu.1999.16.1023, 10595819.
55. Yu Z, Zhou D, Bruce-Keller AJ, Kindy MS, Mattson MP. Lack of the p50 subunit of nuclear factor-kappa B increases the vulnerability of hippocampal neurons to excitotoxic injury. J Neurosci 1999, 19:8856-8865.
56. Chen W, Hartman R, Ayer R, Marcantonio S, Kamper J, Tang J, Zhang JH. Matrix metalloproteinases inhibition provides neuroprotection against hypoxia-ischemia in the developing brain. J Neurochem 2009, 111:726-736. 10.1111/j.1471-4159.2009.06362.x, 19712057.
57. Owen CA, Hu Z, Barrick B, Shapiro SD. Inducible expression of tissue inhibitor of metalloproteinases-resistant matrix metalloproteinase-9 on the cell surface of neutrophils. Am J Respir Cell Mol Biol 2003, 29:283-294. 10.1165/rcmb.2003-0034OC, 12663332.
58. Stamatovic SM, Dimitrijevic OB, Keep RF, Andjelkovic AV. Protein kinase Calpha-RhoA cross-talk in CCL2-induced alterations in brain endothelial permeability. J Biol Chem 2006, 281:8379-8388. 10.1074/jbc.M513122200, 16439355.
59. Harkness KA. Dexamethasone regulation of matrix metalloproteinase expression in CNS vascular endothelium. Brain 2000, 123:698-709. 10.1093/brain/123.4.698, 10734001.
60. Mahajan SD, Aalinkeel R, Reynolds JL, Nair B, Sykes DE, Bonoiu A, Roy I, Yong K-T, Law W-C, Bergey EJ, Prasad PN, Schwartz SA. Suppression of MMP-9 expression in brain microvascular endothelial cells (BMVEC) using a gold nanorod (GNR)-siRNA nanoplex. Immunol Invest 2012, 41:337-355. 10.3109/08820139.2011.604863, 21864113.