Interferon-γ safeguards blood-brain barrier during experimental autoimmune encephalomyelitis

American Journal of Pathology

Volumn 184, Issue 12, 2014, Pages 3308-3320

  Ni, Chen ^a,b   Wang, Chunhui ^a,b   Zhang, Jingjing ^c,d   Qu, Liwei ^a,b   Liu, Xiaoman ^a   Lu, Yu ^a,b   Yang, Wei ^a,b   Deng, Jingjing ^a,b   Lorenz, Dorothea ^d   Gao, Pan ^e   Meng, Qinghong ^a,b   Yan, Xiyun ^a   Blasig, Ingolf E ^d   Qin, Zhihai ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c GUANGDONG MEDICAL UNIVERSITY   (China)

^d LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^e XINXIANG MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN RECEPTOR; CLAUDIN 5; GAMMA INTERFERON RECEPTOR; INTERLEUKIN 17; OCCLUDIN; PROTEIN ZO1; TIGHT JUNCTION PROTEIN; TUMOR NECROSIS FACTOR ALPHA; CLDN5 PROTEIN, MOUSE; GAMMA INTERFERON; GREEN FLUORESCENT PROTEIN; TEK PROTEIN, MOUSE; TJP1 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BONE MARROW TRANSPLANTATION; CELL INFILTRATION; CELL MIGRATION; CEREBELLUM; CHIMERA; CONTROLLED STUDY; ENDOTHELIUM CELL; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; GENE SILENCING; LEUKOCYTE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; UPREGULATION; WHITE MATTER; ANIMAL; BRAIN; C57BL MOUSE; CELL CULTURE; CELL MOTION; CELL SEPARATION; FLOW CYTOMETRY; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; INFLAMMATION; METABOLISM; TRANSGENIC MOUSE;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; CELL MOVEMENT; CELL SEPARATION; CELLS, CULTURED; CLAUDIN-5; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ENDOTHELIAL CELLS; FEMALE; FLOW CYTOMETRY; GREEN FLUORESCENT PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INTERFERON-GAMMA; LEUKOCYTES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RECEPTOR, TIE-2; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84913573590     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2014.08.019     Document Type: Article

References (61)

1. M. Sospedra, and R. Martin Immunology of multiple sclerosis Annu Rev Immunol 23 2005 683 747
2. H.F. McFarland, and R. Martin Multiple sclerosis: a complicated picture of autoimmunity Nat Immunol 8 2007 913 919
3. L. Steinman Multiple sclerosis: a two-stage disease Nat Immunol 2 2001 762 764
4. J. Goverman Autoimmune T cell responses in the central nervous system Nat Rev Immunol 9 2009 393 407
5. I.M. Stromnes, L.M. Cerretti, D. Liggitt, R.A. Harris, and J.M. Goverman Differential regulation of central nervous system autoimmunity by T(H)1 and T(H)17 cells Nat Med 14 2008 337 342
6. G. Krause, L. Winkler, S.L. Mueller, R.F. Haseloff, J. Piontek, and I.E. Blasig Structure and function of claudins Biochim Biophys Acta 1778 2008 631 645
7. I.E. Blasig, C. Bellmann, J. Cording, G. del Vecchio, D. Zwanziger, O. Huber, and R.F. Haseloff Occludin protein family: oxidative stress and reducing conditions Antioxid Redox Signal 15 2011 1195 1219
8. A. Minagar, and J.S. Alexander Blood-brain barrier disruption in multiple sclerosis Mult Scler 9 2003 540 549
9. C. Forster, M. Burek, I.A. Romero, B. Weksler, P.O. Couraud, and D. Drenckhahn Differential effects of hydrocortisone and TNFalpha on tight junction proteins in an in vitro model of the human blood-brain barrier J Physiol 586 2008 1937 1949
10. A.T. Argaw, B.T. Gurfein, Y. Zhang, A. Zameer, and G.R. John VEGF-mediated disruption of endothelial CLN-5 promotes blood-brain barrier breakdown Proc Natl Acad Sci U S A 106 2009 1977 1982
11. H. Kebir, K. Kreymborg, I. Ifergan, A. Dodelet-Devillers, R. Cayrol, M. Bernard, F. Giuliani, N. Arbour, B. Becher, and A. Prat Human T(H)17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation Nat Med 13 2007 1173 1175
12. J.I. Alvarez, A. Dodelet-Devillers, H. Kebir, I. Ifergan, P.J. Fabre, S. Terouz, M. Sabbagh, K. Wosik, L. Bourbonniere, M. Bernard, J. van Horssen, H.E. de Vries, F. Charron, and A. Prat The Hedgehog pathway promotes blood-brain barrier integrity and CNS immune quiescence Science 334 2011 1727 1731
13. E. Cristante, S. McArthur, C. Mauro, E. Maggioli, I.A. Romero, M. Wylezinska-Arridge, P.O. Couraud, J. Lopez-Tremoleda, H.C. Christian, B.B. Weksler, A. Malaspina, and E. Solito Identification of an essential endogenous regulator of blood-brain barrier integrity, and its pathological and therapeutic implications Proc Natl Acad Sci U S A 110 2013 832 841
14. T.V. Lanz, S. Becker, M. Osswald, S. Bittner, M.K. Schuhmann, C.A. Opitz, S. Gaikwad, B. Wiestler, U.M. Litzenburger, F. Sahm, M. Ott, S. Iwantscheff, C. Grabitz, M. Mittelbronn, A. von Deimling, F. Winkler, S.G. Meuth, W. Wick, and M. Platten Protein kinase C beta as a therapeutic target stabilizing blood-brain barrier disruption in experimental autoimmune encephalomyelitis Proc Natl Acad Sci U S A 110 2013 14735 14740
15. K. Hirota, J.H. Duarte, M. Veldhoen, E. Hornsby, Y. Li, D.J. Cua, H. Ahlfors, C. Wilhelm, M. Tolaini, U. Menzel, A. Garefalaki, A.J. Potocnik, and B. Stockinger Fate mapping of IL-17-producing T cells in inflammatory responses Nat Immunol 12 2011 255 263
16. D.O. Willenborg, S. Fordham, C.C. Bernard, W.B. Cowden, and I.A. Ramshaw IFN-gamma plays a critical down-regulatory role in the induction and effector phase of myelin oligodendrocyte glycoprotein-induced autoimmune encephalomyelitis J Immunol 157 1996 3223 3227
17. M. Krakowski, and T. Owens Interferon-gamma confers resistance to experimental allergic encephalomyelitis Eur J Immunol 26 1996 1641 1646
18. I.A. Ferber, S. Brocke, C. Taylor-Edwards, W. Ridgway, C. Dinisco, L. Steinman, D. Dalton, and C.G. Fathman Mice with a disrupted IFN-gamma gene are susceptible to the induction of experimental autoimmune encephalomyelitis (EAE) J Immunol 156 1996 5 7
19. A.K. Wensky, G.C. Furtado, M.C. Marcondes, S. Chen, D. Manfra, S.A. Lira, D. Zagzag, and J.J. Lafaille IFN-gamma determines distinct clinical outcomes in autoimmune encephalomyelitis J Immunol 174 2005 1416 1423
20. S. Abromson-Leeman, R. Bronson, Y. Luo, M. Berman, R. Leeman, J. Leeman, and M. Dorf T-cell properties determine disease site, clinical presentation, and cellular pathology of experimental autoimmune encephalomyelitis Am J Pathol 165 2004 1519 1533
21. J.R. Lees, P.T. Golumbek, J. Sim, D. Dorsey, and J.H. Russell Regional CNS responses to IFN-gamma determine lesion localization patterns during EAE pathogenesis J Exp Med 205 2008 2633 2642
22. J. Deng, X. Liu, L. Rong, C. Ni, X. Li, W. Yang, Y. Lu, X. Yan, C. Qin, L. Zhang, and Z. Qin IFNgamma-responsiveness of endothelial cells leads to efficient angiostasis in tumours involving down-regulation of Dll4 J Pathol 233 2014 170 182
23. T. Korn, J. Reddy, W. Gao, E. Bettelli, A. Awasthi, T.R. Petersen, B.T. Backstrom, R.A. Sobel, K.W. Wucherpfennig, T.B. Strom, M. Oukka, and V.K. Kuchroo Myelin-specific regulatory T cells accumulate in the CNS but fail to control autoimmune inflammation Nat Med 13 2007 423 431
24. Z.H. Qin, and T. Blankenstein CD4(+) T cell-mediated tumor rejection involves inhibition of angiogenesis that is dependent on IFN gamma receptor expression by nonhematopoietic cells Immunity 12 2000 677 686
25. C.H. Wang, M.J. Xiao, X.M. Liu, C. Ni, J.H. Liu, U. Erben, and Z.H. Qin IFN-gamma-mediated downregulation of LXA4 is necessary for the maintenance of nonresolving inflammation and papilloma persistence Cancer Res 73 2013 1742 1751
26. R.C. Brown, A.P. Morris, and R.G. O'Neil Tight junction protein expression and barrier properties of immortalized mouse brain microvessel endothelial cells Brain Res 1130 2007 17 30
27. Y. Omidi, L. Campbell, J. Barar, D. Connell, S. Akhtar, and M. Gumbleton Evaluation of the immortalised mouse brain capillary endothelial cell line, b.End3, as an in vitro blood-brain barrier model for drug uptake and transport studies Brain Res 990 2003 95 112
28. V. Sanna, A. Di Giacomo, A. La Cava, R.I. Lechler, S. Fontana, S. Zappacosta, and G. Matarese Leptin surge precedes onset of autoimmune encephalomyelitis and correlates with development of pathogenic T cell responses J Clin Invest 111 2003 241 250
29. R. Aharoni, R. Eilam, H. Domev, G. Labunskay, M. Sela, and R. Arnon The immunomodulator glatiramer acetate augments the expression of neurotrophic factors in brains of experimental autoimmune encephalomyelitis mice Proc Natl Acad Sci U S A 102 2005 19045 19050
30. H.B. Li, Y.K. Ge, L. Zhang, and X.X. Zheng Astragaloside IV improved barrier dysfunction induced by acute high glucose in human umbilical vein endothelial cells Life Sci 79 2006 1186 1193
31. E.A. Bach, M. Aguet, and R.D. Schreiber The IFN gamma receptor: a paradigm for cytokine receptor signaling Annu Rev Immunol 15 1997 563 591
32. M.A. Farrar, and R.D. Schreiber The molecular cell biology of interferon-gamma and its receptor Annu Rev Immunol 11 1993 571 611
33. T. Nitta, M. Hata, S. Gotoh, Y. Seo, H. Sasaki, N. Hashimoto, M. Furuse, and S. Tsukita Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice J Cell Biol 161 2003 653 660
34. R. Daneman, L. Zhou, D. Agalliu, J.D. Cahoy, A. Kaushal, and B.A. Barres The mouse blood-brain barrier transcriptome: a new resource for understanding the development and function of brain endothelial cells PLoS One 5 2010 e13741
35. T.N. Sato, Y. Qin, C.A. Kozak, and K.L. Audus Tie-1 and Tie-2 define another class of putative receptor tyrosine kinase genes expressed in early embryonic vascular system Proc Natl Acad Sci U S A 90 1993 9355 9358
36. F. Arai, A. Hirao, M. Ohmura, H. Sato, S. Matsuoka, K. Takubo, K. Ito, G.Y. Koh, and T. Suda Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche Cell 118 2004 149 161
37. P.A. Astolfi, F. Salamini, and V. Sgaramella Are we genomic mosaics? variations of the genome of somatic cells can contribute to diversify our phenotypes Curr Genomics 11 2010 379 386
38. G. Andonegui, H. Zhou, D. Bullard, M.M. Kelly, S.C. Mullaly, B. McDonald, E.M. Long, S.M. Robbins, and P. Kubes Mice that exclusively express TLR4 on endothelial cells can efficiently clear a lethal systemic Gram-negative bacterial infection J Clin Invest 119 2009 1921 1930
39. R. Shechter, A. London, and M. Schwartz Orchestrated leukocyte recruitment to immune-privileged sites: absolute barriers versus educational gates Nat Rev Immunol 13 2013 206 218
40. R.M. Ransohoff, P. Kivisakk, and G. Kidd Three or more routes for leukocyte migration into the central nervous system Nat Rev Immunol 3 2003 569 581
41. G. Kooij, K. Kopplin, R. Blasig, M. Stuiver, N. Koning, G. Goverse, S.M. van der Pol, B. van Het Hof, M. Gollasch, J.A. Drexhage, A. Reijerkerk, I.C. Meij, R. Mebius, T.E. Willnow, D. Muller, I.E. Blasig, and H.E. de Vries Disturbed function of the blood-cerebrospinal fluid barrier aggravates neuro-inflammation Acta Neuropathol 128 2014 267 277
42. F. Pfeiffer, J. Schafer, R. Lyck, V. Makrides, S. Brunner, N. Schaeren-Wiemers, U. Deutsch, and B. Engelhardt Claudin-1 induced sealing of blood-brain barrier tight junctions ameliorates chronic experimental autoimmune encephalomyelitis Acta Neuropathol 122 2011 601 614
43. C. Piehl, J. Piontek, J. Cording, H. Wolburg, and I.E. Blasig Participation of the second extracellular loop of claudin-5 in paracellular tightening against ions, small and large molecules Cell Mol Life Sci 67 2010 2131 2140
44. M. Saitou, M. Furuse, H. Sasaki, J.D. Schulzke, M. Fromm, H. Takano, T. Noda, and S. Tsukita Complex phenotype of mice lacking occludin, a component of tight junction strands Mol Biol Cell 11 2000 4131 4142
45. T. Oshima, F.S. Laroux, L.L. Coe, Z. Morise, S. Kawachi, P. Bauer, M.B. Grisham, R.D. Specian, P. Carter, S. Jennings, D.N. Granger, T. Joh, and J.S. Alexander Interferon-gamma and interleukin-10 reciprocally regulate endothelial junction integrity and barrier function Microvasc Res 61 2001 130 143
46. A. Minagar, A. Long, T. Ma, T.H. Jackson, R.E. Kelley, D.V. Ostanin, M. Sasaki, A.C. Warren, A. Jawahar, B. Cappell, and J.S. Alexander Interferon (IFN)-beta 1a and IFN-beta 1b block IFN-gamma-induced disintegration of endothelial junction integrity and barrier Endothelium 10 2003 299 307
47. A. Taddei, C. Giampietro, A. Conti, F. Orsenigo, F. Breviario, V. Pirazzoli, M. Potente, C. Daly, S. Dimmeler, and E. Dejana Endothelial adherens junctions control tight junctions by VE-cadherin-mediated upregulation of claudin-5 Nat Cell Biol 10 2008 923 934
48. R. Daneman, D. Agalliu, L. Zhou, F. Kuhnert, C.J. Kuo, and B.A. Barres Wnt/beta-catenin signaling is required for CNS, but not non-CNS, angiogenesis Proc Natl Acad Sci U S A 106 2009 641 646
49. J.M. Stenman, J. Rajagopal, T.J. Carroll, M. Ishibashi, J. McMahon, and A.P. McMahon Canonical Wnt signaling regulates organ-specific assembly and differentiation of CNS vasculature Science 322 2008 1247 1250
50. S. Liebner, M. Corada, T. Bangsow, J. Babbage, A. Taddei, C.J. Czupalla, M. Reis, A. Felici, H. Wolburg, M. Fruttiger, M.M. Taketo, H. von Melchner, K.H. Plate, H. Gerhardt, and E. Dejana Wnt/beta-catenin signaling controls development of the blood-brain barrier J Cell Biol 183 2008 409 417
51. R. Paolinelli, M. Corada, L. Ferrarini, K. Devraj, C. Artus, C.J. Czupalla, N. Rudini, L. Maddaluno, E. Papa, B. Engelhardt, P.O. Couraud, S. Liebner, and E. Dejana Wnt activation of immortalized brain endothelial cells as a tool for generating a standardized model of the blood brain barrier in vitro PLoS One 8 2013 e70233
52. S.H. Ramirez, S. Fan, H. Dykstra, S. Rom, A. Mercer, N.L. Reichenbach, L. Gofman, and Y. Persidsky Inhibition of glycogen synthase kinase 3beta promotes tight junction stability in brain endothelial cells by half-life extension of occludin and claudin-5 PLoS One 8 2013 e55972
53. J. Gavard, and J.S. Gutkind VE-cadherin and claudin-5: it takes two to tango Nat Cell Biol 10 2008 883 885
54. V. Bartanusz, D. Jezova, B. Alajajian, and M. Digicaylioglu The blood-spinal cord barrier: morphology and clinical implications Ann Neurol 70 2011 194 206
55. E.A. Winkler, J.D. Sengillo, R.D. Bell, J. Wang, and B.V. Zlokovic Blood-spinal cord barrier pericyte reductions contribute to increased capillary permeability J Cereb Blood Flow Metab 32 2012 1841 1852
56. S. Ge, and J.S. Pachter Isolation and culture of microvascular endothelial cells from murine spinal cord J Neuroimmunol 177 2006 209 214
57. L. Sanvito, C.S. Constantinescu, B. Gran, and B.A. 't Hart The multifaceted role of interferon-gamma in central nervous system autoimmune demyelination Open Autoimmun J 2 2010 151 159
58. H.S. Panitch, R.L. Hirsch, J. Schindler, and K.P. Johnson Treatment of multiple sclerosis with gamma interferon: exacerbations associated with activation of the immune system Neurology 37 1987 1097 1102
59. S. Skurkovich, A. Boiko, I. Beliaeva, A. Buglak, T. Alekseeva, N. Smirnova, O. Kulakova, V. Tchechonin, O. Gurova, T. Deomina, O.O. Favorova, B. Skurkovic, and E. Gusev Randomized study of antibodies to IFN-gamma and TNF-alpha in secondary progressive multiple sclerosis Mult Scler 7 2001 277 284
60. Z. Li, L. Chen, and Z. Qin Paradoxical roles of IL-4 in tumor immunity Cell Mol Immunol 6 2009 415 422
61. M.J. Xiao, C.H. Wang, J.H. Zhang, Z.G. Li, X.Q. Zhao, and Z.H. Qin IFN gamma promotes papilloma development by up-regulating Th17-associated inflammation Cancer Res 69 2009 2010 2017