Tumor necrosis factor disrupts claudin-5 endothelial tight junction barriers in two distinct NF-κB-dependent phases

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Clark, Paul R ^a   Kim, Richard K ^a   Pober, Jordan S ^a   Kluger, Martin S ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CLAUDIN 5; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MYOSIN LIGHT CHAIN; RHO ASSOCIATED KINASE 1; RHO ASSOCIATED KINASE 2; RHO KINASE; RHO KINASE INHIBITOR; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; MYOSIN LIGHT CHAIN KINASE;

ARTICLE; CELL DEATH; CONTROLLED STUDY; DERMAL MICROVASCULAR ENDOTHELIAL CELL; EC50; ELECTRIC RESISTANCE; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; PERMEABILITY BARRIER; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TIGHT JUNCTION; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL MEMBRANE PERMEABILITY; CYTOLOGY; DERMIS; DRUG EFFECTS; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; PHOSPHORYLATION; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR ENDOTHELIUM;

CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; CLAUDIN-5; DERMIS; ENDOTHELIUM, VASCULAR; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MICROSCOPY, FLUORESCENCE; MYOSIN LIGHT CHAINS; MYOSIN-LIGHT-CHAIN KINASE; NF-KAPPA B; PHOSPHORYLATION; RHO-ASSOCIATED KINASES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TIGHT JUNCTIONS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84929472536     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120075     Document Type: Article

References (53)

1. Cotran RS, Majno G (1964) The delayed and prolonged vascular leakage in inflammation. I. Topography of the leaking vessels after thermal injury. Am J Pathol 45:261-281. PMID: 14202525
2. Aird WC (2007) Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ Res 100:158-173. PMID: 17272818
3. Angus DC, Van Der Poll T (2013) Severe sepsis and septic shock. N Engl J Med 369:840-851. doi: 10. 1056/NEJMra1208623 PMID: 23984731
4. Piantadosi CA, Schwartz DA (2004) The acute respiratory distress syndrome. Ann Intern Med 141:460-470. PMID: 15381520
5. Simionescu M, Simionescu N, Palade GE (1975) Segmental differentiations of cell junctions in the vascular endothelium. The microvasculature. J Cell Biol 67:863-885. PMID: 1202025
6. Dejana E, Tournier-Lasserve E, Weinstein BM (2009) The control of vascular integrity by endothelial cell junctions: molecular basis and pathological implications. Dev Cell 16:209-221. doi: 10.1016/j. devcel.2009.01.004 PMID: 19217423
7. Lentsch AB, Ward PA (2000) Regulation of inflammatory vascular damage. J Pathol 190:343-348. PMID: 10685068
8. Waage A, Brandtzaeg P, Halstensen A, Kierulf P, Espevik T (1989) The complex pattern of cytokines in serum from patients with meningococcal septic shock. Association between interleukin 6, interleukin 1, and fatal outcome. J Exp Med 169:333-338. PMID: 2783334
9. Waage A (1998) Tumour necrosis factor and septic shock. Lancet 351:603. PMID: 9492816
10. Al-Lamki RS, Brookes AP, Wang J, Reid MJ, Parameshwar J, et al. (2009) TNF receptors differentially signal and are differentially expressed and regulated in the human heart. Am J Transplant 9:2679-2696. doi: 10.1111/j.1600-6143.2009.02831.x PMID: 19788501
11. Pober JS, Sessa WC (2007) Evolving functions of endothelial cells in inflammation. Nat Rev Immunol 7:803-815. PMID: 17893694
12. Newton K, Dixit VM (2012) Signaling in innate immunity and inflammation. Cold Spring Harb Perspect Biol 4:a006049 doi: 10.1101/cshperspect.a006049 PMID: 22296764
13. Li JH, Pober JS (2005) The cathepsin B death pathway contributes to TNF plus IFN-gamma-mediated human endothelial injury. J Immunol 175:1858-1866. PMID: 16034129
14. Bach FH, Hancock WW, Ferran C (1997) Protective genes expressed in endothelial cells: a regulatory response to injury. Immunol Today 18:483-486. PMID: 9357140
15. Ye X, Ding J, Zhou X, Chen G, Liu SF (2008) Divergent roles of endothelial NF-kappaB in multiple organ injury and bacterial clearance in mouse models of sepsis. J Exp Med 205:1303-1315. doi: 10. 1084/jem.20071393 PMID: 18474628
16. Kluger MS, Clark PR, Tellides G, Gerke V, Pober JS (2013) Claudin-5 controls intercellular barriers of human dermal microvascular but not human umbilical vein endothelial cells. Arterioscler Thromb Vasc Biol 33:489-500. doi: 10.1161/ATVBAHA.112.300893 PMID: 23288152
17. Clark PR, Manes TD, Pober JS, Kluger MS (2007) Increased ICAM-1 expression causes endothelial cell leakiness, cytoskeletal reorganization and junctional alterations. J Invest Dermatol 127:762-774. PMID: 17195014
18. Lo CM, Keese CR, Giaever I (1995) Impedance analysis of MDCK cells measured by electric cell-substrate impedance sensing. Biophys J 69:2800-2807. PMID: 8599686
19. Costes SV, Daelemans D, Cho EH, Dobbin Z, Pavlakis G, et al. (2004) Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys J 86:3993-4003. PMID: 15189895
20. Pober JS, Slowik MR, De Luca LG, Ritchie AJ (1993) Elevated cyclic AMP inhibits endothelial cell synthesis and expression of TNF-induced endothelial leukocyte adhesion molecule-1, and vascular cell adhesion molecule-1, but not intercellular adhesion molecule-1. J Immunol 150:5114-5123. PMID: 7684420
21. Xia P, Gamble JR, Rye KA, Wang L, Hii CS, et al. (1998) Tumor necrosis factor-alpha induces adhesion molecule expression through the sphingosine kinase pathway. Proc Natl Acad Sci U S A 95:14196-14201. PMID: 9826677
22. Slowik MR, De Luca LG, Fiers W, Pober JS (1993) Tumor necrosis factor activates human endothelial cells through the p55 tumor necrosis factor receptor but the p75 receptor contributes to activation at low tumor necrosis factor concentration. Am J Pathol 143:1724-1730. PMID: 7504889
23. Garcia JG, Davis HW, Patterson CE (1995) Regulation of endothelial cell gap formation and barrier dysfunction: role of myosin light chain phosphorylation. J Cell Physiol 163:510-522. PMID: 7775594
24. Kawkitinarong K, Linz-McGillem L, Birukov KG, Garcia JG (2004) Differential regulation of human lung epithelial and endothelial barrier function by thrombin. Am J Respir Cell Mol Biol 31:517-527. PMID: 15284075
25. Goeckeler ZM, Wysolmerski RB (1995) Myosin light chain kinase-regulated endothelial cell contraction: the relationship between isometric tension, actin polymerization, and myosin phosphorylation. J Cell Biol 130:613-627. PMID: 7622562
26. Mong PY, Wang Q (2009) Activation of Rho kinase isoforms in lung endothelial cells during inflammation. J Immunol 182:2385-2394. doi: 10.4049/jimmunol.0802811 PMID: 19201893
27. Riento K, Ridley AJ (2003) ROCKs: multifunctional kinases in cell behaviour. Nat Rev Mol Cell Biol 4:446-456. PMID: 12778124
28. Collins T, Palmer HJ, Whitley MZ, Neish AS, Williams AJ (1993) A common theme in endothelial activation insights from the structural analysis of the genes for E-selectin and VCAM-1. Trends Cardiovasc Med 3:92-97. doi: 10.1016/1050-1738 (93) 90030-A PMID: 21244946
29. Wang C, Qin L, Manes TD, Kirkiles-Smith NC, Tellides G, et al. (2014) Rapamycin antagonizes TNF induction of VCAM-1 on endothelial cells by inhibiting mTORC2. J Exp Med 211:395-404. doi: 10.1084/jem.20131125 PMID: 24516119
30. Smale ST (2011) Hierarchies of NF-kappaB target-gene regulation. Nat Immunol 12:689-694. doi: 10. 1038/ni.2070 PMID: 21772277
31. Zhu W, London NR, Gibson CC, Davis CT, Tong Z, et al. (2012) Interleukin receptor activates a MYD88-ARNO-ARF6 cascade to disrupt vascular stability. Nature 492:252-255. doi: 10.1038/nature11603 PMID: 23143332
32. Davis CT, Zhu W, Gibson CC, Bowman-Kirigin JA, Sorensen L, et al. (2014) ARF6 inhibition stabilizes the vasculature and enhances survival during endotoxic shock. J Immunol 192:6045-6052. doi: 10. 4049/jimmunol.1400309 PMID: 24835390
33. Goldenberg NM, Steinberg BE, Slutsky AS, Lee WL (2011) Broken barriers: a new take on sepsis pathogenesis. Sci Transl Med 3:88ps25. doi: 10.1126/scitranslmed.3002011 PMID: 21697528
34. Aveleira CA, Lin CM, Abcouwer SF, Ambrosio AF, Antonetti DA (2010) TNF-alpha signals through PKCzeta/NF-kappaB to alter the tight junction complex and increase retinal endothelial cell permeability. Diabetes 59:2872-2882. doi: 10.2337/db09-1606 PMID: 20693346
35. Petrache I, Verin AD, Crow MT, Birukova A, Liu F, et al. (2001) Differential effect of MLC kinase in TNFalphainduced endothelial cell apoptosis and barrier dysfunction. Am J Physiol Lung Cell Mol Physiol 280:L1168-1178. PMID: 11350795
36. McKenzie JA, Ridley AJ (2007) Roles of Rho/ROCK and MLCK in TNF-alpha-induced changes in endothelial morphology and permeability. J Cell Physiol 213:221-228. PMID: 17476691
37. Shen L, Black ED, Witkowski ED, Lencer WI, Guerriero V, et al. (2006) Myosin light chain phosphorylation regulates barrier function by remodeling tight junction structure. J Cell Sci 119:2095-2106. PMID: 16638813
38. Amano M, Ito M, Kimura K, Fukata Y, Chihara K, et al. (1996) Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J Biol Chem 271:20246-20249. PMID: 8702756
39. Marcus BC, Gewertz BL (1998) Measurement of endothelial permeability. Ann Vasc Surg 12:384-390. PMID: 9676938
40. Garcia JG, Liu F, Verin AD, Birukova A, Dechert MA, et al. (2001) Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J Clin Invest 108:689-701. PMID: 11544274
41. David S, Ghosh CC, Mukherjee A, Parikh SM (2011) Angiopoietin-1 requires IQ domain GTPase-activating protein 1 to activate Rac1 and promote endothelial barrier defense. Arterioscler Thromb Vasc Biol 31:2643-2652. doi: 10.1161/ATVBAHA.111.233189 PMID: 21885850
42. Bryan BA, Dennstedt E, Mitchell DC, Walshe TE, Noma K, et al. (2010) RhoA/ROCK signaling is essential for multiple aspects of VEGF-mediated angiogenesis. FASEB J 24:3186-3195. doi: 10.1096/fj.09-145102 PMID: 20400538
43. Nwariaku FE, Rothenbach P, Liu Z, Zhu X, Turnage RH, et al. (2003) Rho Inhibition decreases TNF-induced endothelial MAPK activation and monolayer permeability. J Appl Physiol 95:1889-1895. PMID: 12844496
44. Millan J, Cain RJ, Reglero-Real N, Bigarella C, Marcos-Ramiro B, et al. (2010) Adherens junctions connect stress fibres between adjacent endothelial cells. BMC Biol 8:11. doi: 10.1186/1741-7007-8-11 PMID: 20122254
45. Breslin JW, Sun H, Xu W, Rodarte C, Moy AB, et al. (2006) Involvement of ROCK-mediated endothelial tension development in neutrophil-stimulated microvascular leakage. Am J Physiol Heart Circ Physiol 290:H741-750. PMID: 16172166
46. Stockton RA, Shenkar R, Awad IA, Ginsberg MH (2010) Cerebral cavernous malformations proteins inhibit Rho kinase to stabilize vascular integrity. J Exp Med 207:881-896. doi: 10.1084/jem.20091258 PMID: 20308363
47. Wang J, Liu H, Chen B, Li Q, Huang X, et al. (2012) RhoA/ROCK-dependent moesin phosphorylation regulates AGE-induced endothelial cellular response. Cardiovasc Diabetol 11:7. doi: 10.1186/1475-2840-11-7 PMID: 22251897
48. Uehata M, Ishizaki T, Satoh H, Ono T, Kawahara T, et al. (1997) Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389:990-994. PMID: 9353125
49. Ishizaki T, Uehata M, Tamechika I, Keel J, Nonomura K, et al. (2000) Pharmacological properties of Y-27632, a specific inhibitor of rho-associated kinases. Mol Pharmacol 57:976-983. PMID: 10779382
50. Ikenoya M, Hidaka H, Hosoya T, Suzuki M, Yamamoto N, et al. (2002) Inhibition of rho-kinase-induced myristoylated alanine-rich C kinase substrate (MARCKS) phosphorylation in human neuronal cells by H-1152, a novel and specific Rho-kinase inhibitor. J Neurochem 81:9-16. PMID: 12067241
51. Davies SP, Reddy H, Caivano M, Cohen P (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351:95-105. PMID: 10998351
52. Nichols RJ, Dzamko N, Hutti JE, Cantley LC, Deak M, et al. (2009) Substrate specificity and inhibitors of LRRK2, a protein kinase mutated in Parkinson's disease. Biochem J 424:47-60. doi: 10.1042/BJ20091035 PMID: 19740074
53. Weber G, Fabbrini P, Resi L, Jones R, Vesselinovitch D, et al. (1977) Regression of arteriosclerotic lesions in rhesus monkey aortas after regression diet. Scanning and transmission electron microscope observations of the endothelium. Atherosclerosis 26:535-547. PMID: 405022