Immune cell trafficking across the barriers of the central nervous system in multiple sclerosis and stroke

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1862, Issue 3, 2016, Pages 461-471

  Lopes Pinheiro, Melissa A ^a   Kooij, Gijs ^a   Mizee, Mark R ^a   Kamermans, Alwin ^a   Enzmann, Gaby ^b   Lyck, Ruth ^b   Schwaninger, Markus ^c   Engelhardt, Britta ^b   de Vries, Helga E ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF BERN   (Switzerland)

^c UNIVERSITY OF LÜBECK   (Germany)

Author keywords

Astrocyte; Blood brain barrier; Immune cell trafficking; Multiple sclerosis; Stroke

Indexed keywords

CD4 ANTIGEN;

ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN ISCHEMIA; CD4+ T LYMPHOCYTE; CELL INFILTRATION; CELL MIGRATION; CENTRAL NERVOUS SYSTEM; CEREBROVASCULAR ACCIDENT; CHOROID PLEXUS; DIAPEDESIS; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; HUMAN; IMMUNOCOMPETENT CELL; LYMPHOCYTE; MULTIPLE SCLEROSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; TISSUE INJURY;

EID: 84957840947     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2015.10.018     Document Type: Review

References (141)

1. Milo R., Miller A. Revised diagnostic criteria of multiple sclerosis. Autoimmun. Rev. 2014, 13:518.
2. Orrell R.W. Multiple sclerosis: the history of a disease. J. R. Soc. Med. 2005, 98:289.
3. Loma I., Heyman R. Multiple sclerosis: pathogenesis and treatment. Curr. Neuropharmacol. 2011, 9:409.
4. Zlokovic B.V. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 2008, 57:178.
5. Weinshenker B.G., Bass B., Rice G.P.A., Noseworthy J., Carriere W., Baskerville J., Ebers G.C. The natural history of multiple sclerosis: a geographically based study I. Clinical course and disability. Brain 1989, 112:133.
6. Sospedra M., Martin R. Immunology of multiple sclerosis. Annu. Rev. Immunol. 2005, 23:683.
7. Babbe H., Roers A., Waisman A., Lassmann H., Goebels N., Hohlfeld R., Friese M., Schröder R., Deckert M., Schmidt S. Clonal expansions of CD8+ T cells dominate the T cell infiltrate in active multiple sclerosis lesions as shown by micromanipulation and single cell polymerase chain reaction. J. Exp. Med. 2000, 192:393.
8. Alvarez J.I., Cayrol R., Prat A. Disruption of central nervous system barriers in multiple sclerosis. Biochim. Biophys. Acta (BBA) - Mol. Basis Dis. 2011, 1812:252.
9. Ramagopalan S.V., Dobson R., Meier U.C., Giovannoni G. Multiple sclerosis: risk factors, prodromes, and potential causal pathways. Lancet Neurol. 2010, 9:727.
10. Trapp B.D., Peterson J., Ransohoff R.M., Rudick R., Mörk S., Bö L. Axonal transection in the lesions of multiple sclerosis. N. Engl. J. Med. 1998, 338:278.
11. Scheikl T., Pignolet B., Mars L.T., Liblau R.S. Transgenic mouse models of multiple sclerosis. Cell. Mol. Life Sci. 2010, 67:4011.
12. Fletcher J.M., Lalor S.J., Sweeney C.M., Tubridy N., Mills K.H.G. T cells in multiple sclerosis and experimental autoimmune encephalomyelitis. Clin. Exp. Immunol. 2010, 162:1.
13. Langrish C.L., Chen Y., Blumenschein W.M., Mattson J., Basham B., Sedgwick J.D., McClanahan T., Kastelein R.A., Cua D.J. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 2005, 201:233.
14. Pette M., Fujita K., Kitze B., Whitaker J.N., Albert E., Kappos L., Wekerle H. Myelin basic protein-specific T lymphocyte lines from MS patients and healthy individuals. Neurology 1990, 40:1770.
15. Cao Y., Goods B.A., Raddassi K., Nepom G.T., Kwok W.W., Love J.C., Hafler D.A. Functional inflammatory profiles distinguish myelin-reactive T cells from patients with multiple sclerosis. Sci. Transl. Med. 2015, 7. (287ra74).
16. Venken K., Hellings N., Hensen K., Rummens J.-L., Medaer R., D'hooghe M.B., Dubois B., Raus J., Stinissen P. Secondary progressive in contrast to relapsing-remitting multiple sclerosis patients show a normal CD4+ CD25+ regulatory T-cell function and FOXP3 expression. J. Neurosci. Res. 2006, 83:1432.
17. Viglietta V., Baecher-Allan C., Weiner H.L., Hafler D.A. Loss of functional suppression by CD4+ CD25+ regulatory T cells in patients with multiple sclerosis. J. Exp. Med. 2004, 199:971.
18. Schneider A., Long S.A., Cerosaletti K., Ni C.T., Samuels P., Kita M., Buckner J.H. In active relapsing-remitting multiple sclerosis, effector T cell resistance to adaptive Tregs involves IL-6-mediated signaling. Sci. Transl. Med. 2013, 5. (170ra15).
19. Stys P.K., Zamponi G.W., van Minnen J., Geurts J.J. Will the real multiple sclerosis please stand up?. Nat. Rev. Neurosci. 2012, 13:507.
20. Bhat R., Steinman L. Innate and adaptive autoimmunity directed to the central nervous system. Neuron 2009, 64:123.
21. Barnett M.H., Prineas J.W. Relapsing and remitting multiple sclerosis: pathology of the newly forming lesion. Ann. Neurol. 2004, 55:458.
22. Rodriguez M., Scheithauer B. Ultrastructure of multiple sclerosis. Ultrastruct. Pathol. 1994, 18:3.
23. Molyneux P.D., Kappos L., Polman C., Pozzilli C., Barkhof F., Filippi M., Yousry T., Hahn D., Wagner K., Ghazi M. The effect of interferon beta-1b treatment on MRI measures of cerebral atrophy in secondary progressive multiple sclerosis. Brain 2000, 123:2256.
24. Hawker K. Progressive multiple sclerosis: characteristics and management. Neurol. Clin. 2011, 29:423.
25. Harbison S. Cell therapy for multiple sclerosis: a new hope. Biosci. Horiz. 2014, 7. (hzu014).
26. Sheridan C. Third oral MS drug wins FDA nod. Nat. Biotechnol. 2013, 31:373.
27. Johnson K.P., Brooks B.R., Cohen J.A., Ford C.C., Goldstein J., Lisak R.P., Myers L.W., Panitch H.S., Rose J.W., Schiffer R.B. Copolymer 1 reduces relapse rate and improves disability in relapsing-remitting multiple sclerosis results of a phase III multicenter, double-blind, placebo-controlled trial. Neurology 1995, 45:1268.
28. Dhib-Jalbut S., Marks S. Interferon-β mechanisms of action in multiple sclerosis. Neurology 2010, 74:S17-S24.
29. McGraw C.A., Lublin F.D. Interferon beta and glatiramer acetate therapy. Neurotherapeutics 2013, 10:2.
30. Racke M.K., Lovett-Racke A.E., Karandikar N.J. The mechanism of action of glatiramer acetate treatment in multiple sclerosis. Neurology 2010, 74:S25-S30.
31. Kieseier B.C., Wiendl H. New evidence for teriflunomide in multiple sclerosis. Lancet Neurol. 2014, 13:234.
32. Cyster J.G. Chemokines, sphingosine-1-phosphate, and cell migration in secondary lymphoid organs. Annu. Rev. Immunol. 2005, 23:127.
33. Brinkmann V. FTY720 (fingolimod) in multiple sclerosis: therapeutic effects in the immune and the central nervous system. Br. J. Pharmacol. 2009, 158:1173.
34. Albrecht P., Bouchachia I., Goebels N., Henke N., Hofstetter H.H., Issberner A., Kovacs Z., Lewerenz J., Lisak D., Maher P. Effects of dimethyl fumarate on neuroprotection and immunomodulation. J. Neuroinflammation 2012, 9:2094.
35. Bar-Or A., Pachner A., Menguy-Vacheron F., Kaplan J., Wiendl H. Teriflunomide and its mechanism of action in multiple sclerosis. Drugs 2014, 74:659.
36. Dirnagl U., Endres M. Found in translation preclinical stroke research predicts human pathophysiology, clinical phenotypes, and therapeutic outcomes. Stroke 2014, 45:1510.
37. Zhang J., Zhang Y., Xing S., Liang Z., Zeng J. Secondary neurodegeneration in remote regions after focal cerebral infarction a new target for stroke management?. Stroke 2012, 43:1700.
38. Love S., Louis D., Ellison D.W. Greenfield's Neuropathology Eighth Edition 2-Volume Set 2008, CRC Press.
39. Aronowski J., Strong R., Grotta J.C. Reperfusion injury: demonstration of brain damage produced by reperfusion after transient focal ischemia in rats. J. Cereb. Blood Flow Metab. 1997, 17:1048.
40. Emerich D.F., Dean R.L., Bartus R.T. The role of leukocytes following cerebral ischemia: pathogenic variable or bystander reaction to emerging infarct?. Exp. Neurol. 2002, 173:168.
41. Perez-de-Puig I., Miró-Mur F., Ferrer-Ferrer M., Gelpi E., Pedragosa J., Justicia C., Urra X., Chamorro A., Planas A.M. Neutrophil recruitment to the brain in mouse and human ischemic stroke. Acta Neuropathol. 2015, 129:239.
42. Enzmann G., Mysiorek C., Gorina R., Cheng Y.J., Ghavampour S., Hannocks M.J., Prinz V., Dirnagl U., Endres M., Prinz M. The neurovascular unit as a selective barrier to polymorphonuclear granulocyte (PMN) infiltration into the brain after ischemic injury. Acta Neuropathol. 2013, 125:395.
43. Gliem M., Mausberg A.K., Lee J.-I., Simiantonakis I., van Rooijen N., Hartung H.-P., Jander S. Macrophages prevent hemorrhagic infarct transformation in murine stroke models. Ann. Neurol. 2012, 71:743.
44. Dimitrijevic O.B., Stamatovic S.M., Keep R.F., Andjelkovic A.V. Absence of the chemokine receptor CCR2 protects against cerebral ischemia/reperfusion injury in mice. Stroke 2007, 38:1345.
45. Soriano S.G., Amaravadi L.S., Wang Y.F., Zhou H., Gary X.Y., Tonra J.R., Fairchild-Huntress V., Fang Q., Dunmore J.H., Huszar D. Mice deficient in fractalkine are less susceptible to cerebral ischemia-reperfusion injury. J. Neuroimmunol. 2002, 125:59.
46. Lalancette-Hérbert M., Gowing G., Simard A., Weng Y.C., Kriz J. Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J. Neurosci. 2007, 27:2596.
47. Kleinschnitz C., Kraft P., Dreykluft A., Hagedorn I., Göbel K., Schuhmann M.K., Langhauser F., Helluy X., Schwarz T., Bittner S. Regulatory T cells are strong promoters of acute ischemic stroke in mice by inducing dysfunction of the cerebral microvasculature. Blood 2013, 121:679.
48. Liesz A., Suri-Payer E., Veltkamp C., Doerr H., Sommer C., Rivest S., Giese T., Veltkamp R. Regulatory T cells are key cerebroprotective immunomodulators in acute experimental stroke. Nat. Med. 2009, 15:192.
49. Doyle K.P., Quach L.N., Solé M., Axtell R.C., Nguyen T.V., Soler-Llavina G.J., Jurado S., Han J., Steinman L., Longo F.M. B-lymphocyte-mediated delayed cognitive impairment following stroke. J. Neurosci. 2015, 35:2133.
50. Ren X., Akiyoshi K., Dziennis S., Vandenbark A.A., Herson P.S., Hurn P.D., Offner H. Regulatory B cells limit CNS inflammation and neurologic deficits in murine experimental stroke. J. Neurosci. 2011, 31:8556.
51. Connolly E.S., Winfree C.J., Springer T.A., Naka Y., Liao H., Yan S.D., Stern D.M., Solomon R.A., Gutierrez-Ramos J.C., Pinsky D.J. Cerebral protection in homozygous null ICAM-mice after middle cerebral artery occlusion. Role of neutrophil adhesion in the pathogenesis of stroke. J. Clin. Investig. 1996, 97:209.
52. Enlimomab Acute Stroke Trial Investigators Use of anti-ICAM-therapy in ischemic stroke results of the Enlimomab Acute Stroke Trial. Neurology 2001, 57:1428.
53. Becker K.J. Anti-leukocyte antibodies: LeukArrest (Hu23F2G) and Enlimomab (R6. 5) in acute stroke. Curr. Med. Res. Opin. 2002, 18:s18-s22.
54. Furuya K., Takeda H., Azhar S., McCarron R.M., Chen Y., Ruetzler C.A., Wolcott K.M., DeGraba T.J., Rothlein R., Hugli T.E. Examination of several potential mechanisms for the negative outcome in a clinical stroke trial of enlimomab, a murine anti-human intercellular adhesion molecule-antibody a bedside-to-bench study. Stroke 2001, 32:2665.
55. Xu H., Gonzalo J.A., Pierre Y.S., Williams I.R., Kupper T.S., Cotran R.S., Springer T.A., Gutierrez-Ramos J.C. Leukocytosis and resistance to septic shock in intercellular adhesion molecule 1-deficient mice. J. Exp. Med. 1994, 180:95.
56. Sligh J.E., Ballantyne C.M., Rich S.S., Hawkins H.K., Smith C.W., Bradley A., Beaudet A.L. Inflammatory and immune responses are impaired in mice deficient in intercellular adhesion molecule 1. Proc. Natl. Acad. Sci. 1993, 90:8529.
57. van den Engel N.K., Heidenthal E., Vinke A., Kolb H., Martin S. Circulating forms of intercellular adhesion molecule (ICAM)-in mice lacking membranous ICAM-1. Blood 2000, 95:1350.
58. Rieckmann P., Michel U., Albrecht M., Brück W., Wöckel L., Felgenhauer K. Soluble forms of intercellular adhesion molecule-(ICAM-1) block lymphocyte attachment to cerebral endothelial cells. J. Neuroimmunol. 1995, 60:9.
59. Hu X., Barnum S.R., Wohler J.E., Schoeb T.R., Bullard D.C. Differential ICAM-isoform expression regulates the development and progression of experimental autoimmune encephalomyelitis. Mol. Immunol. 2010, 47:1692.
60. Neumann J., Riek-Burchardt M., Herz J., Doeppner T.R., König R., Hütten H., Etemire E., Männ L., Klingberg A., Fischer T., Görtler M.W., Heinze H.-J., Reichardt P., Schraven B., Hermann D.M., Reymann K.G., Gunzer M. Very-late-antigen-(VLA-4)-mediated brain invasion by neutrophils leads to interactions with microglia, increased ischemic injury and impaired behavior in experimental stroke. Acta Neuropathol. 2015, 129:259.
61. Liesz A., Zhou W., Mracskó É., Karcher S., Bauer H., Schwarting S., Sun L., Bruder D., Stegemann S., Cerwenka A. Inhibition of lymphocyte trafficking shields the brain against deleterious neuroinflammation after stroke. Brain 2011, 134:704.
62. Langhauser F., Kraft P., Göb E., Leinweber J., Schuhmann M.K., Lorenz K., Gelderblom M., Bittner S., Meuth S.G., Wiendl H. Blocking of α4 integrin does not protect from acute ischemic stroke in mice. Stroke 2014, 45:1799.
63. Llovera G., Hofmann K., Roth S., Salas-Pérdomo A., Ferrer-Ferrer M., Perego C., Zanier E.R., Mamrak U., Rex A., Party H., Agin V., Fauchon C., Orset C., Haelewyn B., De Simoni M.-G., Dirnagl U., Grittner U., Planas A.M., Plesnila N., Vivien D., Liesz A. Results of a preclinical randomized controlled multicenter trial (pRCT): anti-CD49d treatment for acute brain ischemia. Sci. Transl. Med. 2015, 7. (299ra121).
64. Barker C.F., Billingham R.E. Immunologically privileged sites. Adv. Immunol. 1978, 25:1.
65. Galea I., Bechmann I., Perry V.H. What is immune privilege (not)?. Trends Immunol. 2007, 28:12.
66. Engelhardt B., Coisne C. Fluids and barriers of the CNS establish immune privilege by confining immune surveillance to a two-walled castle moat surrounding the CNS castle. Fluids Barriers CNS 2011, 8:10.
67. Ousman S.S., Kubes P. Immune surveillance in the central nervous system. Nat. Neurosci. 2012, 15:1096.
68. Laman J.D., Weller R.O. Drainage of cells and soluble antigen from the CNS to regional lymph nodes. J. NeuroImmune Pharmacol. 2013, 8:840.
69. Kunis G., Baruch K., Miller O., Schwartz M. Immunization with a myelin-derived antigen activates the brain's choroid plexus for recruitment of immunoregulatory cells to the CNS and attenuates disease progression in a mouse model of ALS. J. Neurosci. 2015, 35:6381.
70. Cepok S., Jacobsen M., Schock S., Omer B., Jaekel S., Böddeker I., Oertel W.H., Sommer N., Hemmer B. Patterns of cerebrospinal fluid pathology correlate with disease progression in multiple sclerosis. Brain 2001, 124:2169.
71. Raposo C., Graubardt N., Cohen M., Eitan C., London A., Berkutzki T., Schwartz M. CNS repair requires both effector and regulatory T cells with distinct temporal and spatial profiles. J. Neurosci. 2014, 34:10141.
72. Meeker R.B., Williams K., Killebrew D.A., Hudson L.C. Cell trafficking through the choroid plexus. Cell Adhes. Migr. 2012, 6:390.
73. Unger W.W., Laban S., Kleijwegt F.S., van der Slik A.R., Roep B.O. Induction of treg by monocyte-derived DC modulated by vitamin D3 or dexamethasone: differential role for PD-L1. Eur. J. Immunol. 2009, 39:3147.
74. Baruch K., Ron-Harel N., Gal H., Deczkowska A., Shifrut E., Ndifon W., Mirlas-Neisberg N., Cardon M., Vaknin I., Cahalon L. CNS-specific immunity at the choroid plexus shifts toward destructive Th2 inflammation in brain aging. Proc. Natl. Acad. Sci. 2013, 110:2264.
75. Engelhardt B., Sorokin L. The Blood-Brain and the Blood-Cerebrospinal Fluid Barriers: Function and Dysfunction 2009, 497-511. Springer.
76. Kooij G., Kopplin K., Blasig R., Stuiver M., Koning N., Goverse G., van der Pol S.M., van het Hof B., Gollasch M., Drexhage J.A. Disturbed function of the blood-cerebrospinal fluid barrier aggravates neuro-inflammation. Acta Neuropathol. 2014, 128:267.
77. Ransohoff R.M. Immunology: in the beginning. Nature 2009, 462:41.
78. Reboldi A., Coisne C., Baumjohann D., Benvenuto F., Bottinelli D., Lira S., Uccelli A., Lanzavecchia A., Engelhardt B., Sallusto F. CC chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat. Immunol. 2009, 10:514.
79. Engelhardt B., Wolburg-Buchholz K., Wolburg H. Involvement of the choroid plexus in central nervous system inflammation. Microsc. Res. Tech. 2001, 52:112.
80. Wolburg K., Gerhardt H., Schulz M., Wolburg H., Engelhardt B. Ultrastructural localization of adhesion molecules in the healthy. Cell Tissue Res. 1999, 296:259.
81. Battistini L., Piccio L., Rossi B., Bach S., Galgani S., Gasperini C., Ottoboni L., Ciabini D., Caramia M.D., Bernardi G. CD8+ T cells from patients with acute multiple sclerosis display selective increase of adhesiveness in brain venules: a critical role for P-selectin glycoprotein ligand-1. Blood 2003, 101:4775.
82. Bahbouhi B., Berthelot L., Pettre S., Michel L., Wiertlewski S., Weksler B., Romero I.A., Miller F., Couraud P.O., Brouard S. Peripheral blood CD4+ T lymphocytes from multiple sclerosis patients are characterized by higher PSGL-expression and transmigration capacity across a human blood-brain barrier-derived endothelial cell line. J. Leukoc. Biol. 2009, 86:1049.
83. Gotsch U., Jäger U., Dominis M., Vestweber D. Expression of P-selectin on endothelial cells is upregulated by LPS and TNF-α in vivo. Cell Commun. Adhes. 1994, 2:7.
84. Piccio L., Rossi B., Scarpini E., Laudanna C., Giagulli C., Issekutz A.C., Vestweber D., Butcher E.C., Constantin G. Molecular mechanisms involved in lymphocyte recruitment in inflamed brain microvessels: critical roles for P-selectin glycoprotein ligand-and heterotrimeric Gi-linked receptors. J. Immunol. 2002, 168:1940.
85. Greenwood J., Heasman S.J., Alvarez J.I., Prat A., Lyck R., Engelhardt B. Review: leucocyte-endothelial cell crosstalk at the blood-brain barrier: a prerequisite for successful immune cell entry to the brain. Neuropathol. Appl. Neurobiol. 2011, 37:24.
86. Krumbholz M., Theil D., Steinmeyer F., Cepok S., Hemmer B., Hofbauer M., Farina C., Derfuss T., Junker A., Arzberger T. CCL19 is constitutively expressed in the CNS, up-regulated in neuroinflammation, active and also inactive multiple sclerosis lesions. J. Neuroimmunol. 2007, 190:72.
87. Subileau E.A., Rezaie P., Davies H.A., Colyer F.M., Greenwood J., Male D.K., Romero I.A. Expression of chemokines and their receptors by human brain endothelium: implications for multiple sclerosis. J. Neuropathol. Exp. Neurol. 2009, 68:227.
88. McManus C., Berman J.W., Brett F.M., Staunton H., Farrell M., Brosnan C.F. MCP-1, MCP-and MCP-expression in multiple sclerosis lesions: an immunohistochemical and in situ hybridization study. J. Neuroimmunol. 1998, 86:20.
89. Prat A., Biernacki K., Lavoie J.F., Poirier J., Duquette P., Antel J.P. Migration of multiple sclerosis lymphocytes through brain endothelium. Arch. Neurol. 2002, 59:391.
90. Steffen B.J., Butcher E.C., Engelhardt B. Evidence for involvement of ICAM-and VCAM-in lymphocyte interaction with endothelium in experimental autoimmune encephalomyelitis in the central nervous system in the SJL/J mouse. Am. J. Pathol. 1994, 145:189.
91. Bö L., Peterson J.W., Mark S., Hoffman P.A., Gallatin M.W., Ransohoff R.M., Trapp B.D. Distribution of immunoglobulin superfamily members ICAM-1,-2,-3, and the β2 integrin LFA-in multiple sclerosis lesions. J. Neuropathol. Exp. Neurol. 1996, 55:1060.
92. Vajkoczy P., Laschinger M., Engelhardt B. α4-integrin-VCAM-binding mediates G protein-independent capture of encephalitogenic T cell blasts to CNS white matter microvessels. J. Clin. Invest. 2001, 108:557.
93. Greenwood J., Wang Y., Calder V.L. Lymphocyte adhesion and transendothelial migration in the central nervous system: the role of LFA-1, ICAM-1, VLA-and VCAM-1. Immunology 1995, 86:408.
94. Bartholomäus I., Kawakami N., Odoardi F., Schläger C., Miljkovic D., Ellwart J.W., Klinkert W.E., Flügel-Koch C., Issekutz T.B., Wekerle H., Flügel A. Effector T cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions. Nature 2009, 462:94.
95. Steiner O., Coisne C., Cecchelli R., Boscacci R., Deutsch U., Engelhardt B., Lyck R. Differential roles for endothelial ICAM-1, ICAM-2, and VCAM-in shear-resistant T cell arrest, polarization, and directed crawling on blood-brain barrier endothelium. J. Immunol. 2010, 185:4846.
96. Svensson L., Stanley P., Willenbrock F., Hogg N. The Gαq/11 Proteins Contribute to T Lymphocyte Migration by Promoting Turnover of Integrin LFA-Through Recycling 2012.
97. Evans R., Lellouch A.C., Svensson L., McDowall A., Hogg N. The integrin LFA-signals through ZAP-70 to regulate expression of high-affinity LFA-on T lymphocytes. Blood 2011, 117:3331.
98. Valignat M.P., Theodoly O., Gucciardi A., Hogg N., Lellouch A.C. T lymphocytes orient against the direction of fluid flow during LFA-1-mediated migration. Biophys. J. 2013, 104:322.
99. Abadier M., Haghayegh Jahromi N., Cardoso Alves L., Boscacci R., Vestweber D., Barnum S., Deutsch U., Engelhardt B., Lyck R. Cell surface levels of endothelial ICAM-influence the transcellular or paracellular T-cell diapedesis across the blood-brain barrier. Eur. J. Immunol. 2015, 45:1043.
100. Engelhardt B., Ransohoff R.M. Capture, crawl, cross: the T cell code to breach the blood-brain barriers. Trends in Immunol. 2012, 33:579.
101. Shulman Z., Shinder V., Klein E., Grabovsky V., Yeger O., Geron E., Montresor A., Bolomini-Vittori M., Feigelson S.W., Kirchhausen T. Lymphocyte crawling and transendothelial migration require chemokine triggering of high-affinity LFA-integrin. Immunity 2009, 30:384.
102. Wittchen E.S. Endothelial signaling in paracellular and transcellular leukocyte transmigration. Front. Biosci.: J. Virtual Libr. 2009, 14:2522.
103. Durieu-Trautmann O., Chaverot N., Cazaubon S., Strosberg A.D., Couraud P.O. Intercellular adhesion molecule 1 activation induces tyrosine phosphorylation of the cytoskeleton-associated protein cortactin in brain microvessel endothelial cells. J. Biol. Chem. 1994, 269:12536.
104. Etienne-Manneville S., Manneville J.B., Adamson P., Wilbourn B., Greenwood J., Couraud P.O. ICAM-1-coupled cytoskeletal rearrangements and transendothelial lymphocyte migration involve intracellular calcium signaling in brain endothelial cell lines. J. Immunol. 2000, 165:3375.
105. Etienne S., Adamson P., Greenwood J., Strosberg A.D., Cazaubon S., Couraud P.O. ICAM-signaling pathways associated with Rho activation in microvascular brain endothelial cells. J. Immunol. 1998, 161:5755.
106. Greenwood J., Amos C.L., Walters C.E., Couraud P.O., Lyck R., Engelhardt B., Adamson P. Intracellular domain of brain endothelial intercellular adhesion molecule-is essential for T lymphocyte-mediated signaling and migration. J. Immunol. 2003, 171:2099.
107. Lyck R., Reiss Y., Gerwin N., Greenwood J., Adamson P., Engelhardt B. T-cell interaction with ICAM-1/ICAM-double-deficient brain endothelium in vitro: the cytoplasmic tail of endothelial ICAM-is necessary for transendothelial migration of T cells. Blood 2003, 102:3675.
108. Turowski P., Martinelli R., Crawford R., Wateridge D., Papageorgiou A.P., Lampugnani M.G., Gamp A.C., Vestweber D., Adamson P., Dejana E. Phosphorylation of vascular endothelial cadherin controls lymphocyte emigration. J. Cell Sci. 2008, 121:29.
109. Martinelli R., Gegg M., Longbottom R., Adamson P., Turowski P., Greenwood J. ICAM-1-mediated endothelial nitric oxide synthase activation via calcium and AMP-activated protein kinase is required for transendothelial lymphocyte migration. Mol. Biol. Cell 2009, 20:995.
110. Anderson M.A., Ao Y., Sofroniew M.V. Heterogeneity of reactive astrocytes. Neurosci. Lett. 2014, 565:23.
111. Sofroniew M.V. Astrocyte barriers to neurotoxic inflammation. Nat. Rev. Neurosci. 2015, 16:249.
112. Van Der Voorn P., Tekstra J., Beelen R.H., Tensen C.P., van der Valk P., De Groot C.J. Expression of MCP-by reactive astrocytes in demyelinating multiple sclerosis lesions. Am. J. Pathol. 1999, 154:45.
113. D'Amelio F.E., Smith M.E., Eng L.F. Sequence of tissue responses in the early stages of experimental allergic encephalomyelitis (EAE): immunohistochemical, light microscopic, and ultrastructural observations in the spinal cord. Glia 1990, 3:229.
114. Wang D., Ayers M.M., Catmull D.V., Hazelwood L.J., Bernard C.C., Orian J.M. Astrocyte-associated axonal damage in pre-onset stages of experimental autoimmune encephalomyelitis. Glia 2005, 51:235.
115. Kooij G., Mizee M.R., van Horssen J., Reijerkerk A., Witte M.E., Drexhage J.A., van der Pol S.M., van het Hof B., Scheffer G., Scheper R. Adenosine triphosphate-binding cassette transporters mediate chemokine (CC motif) ligand 2 secretion from reactive astrocytes: relevance to multiple sclerosis pathogenesis. Brain 2010, (awq330).
116. Kooij G., van Horssen J., de Lange E.C., Reijerkerk A., van der Pol S.M., van het Hof B., Drexhage J., Vennegoor A., Killestein J., Scheffer G. T lymphocytes impair P-glycoprotein function during neuroinflammation. J. Autoimmun. 2010, 34:416.
117. Kooij G., van Horssen J., Bandaru V.V.R., Haughey N.J., de Vries H.E. The role of ATP-binding cassette transporters in neuro-inflammation: relevance for bioactive lipids. Front. Pharmacol. 2012, 3.
118. Ge S., Shrestha B., Paul D., Keating C., Cone R., Guglielmotti A., Pachter J.S. The CCL2 synthesis inhibitor bindarit targets cells of the neurovascular unit, and suppresses experimental autoimmune encephalomyelitis. J. Neuroinflammation 2012, 9:171.
119. Stamatovic S.M., Keep R.F., Wang M.M., Jankovic I., Andjelkovic A.V. Caveolae-mediated internalization of occludin and claudin-during CCL2-induced tight junction remodeling in brain endothelial cells. J. Biol. Chem. 2009, 284:19053.
120. Lee J.Y., Kim H.S., Choi H.Y., Oh T.H., Yune T.Y. Fluoxetine inhibits matrix metalloprotease activation and prevents disruption of blood-spinal cord barrier after spinal cord injury. Brain 2012, (aws171).
121. Ranaivo H.R., Hodge J.N., Choi N., Wainwright M.S. Albumin induces upregulation of matrix metalloproteinase-in astrocytes via MAPK and reactive oxygen species-dependent pathways. J. Neuroinflammation 2012, 9:1.
122. Agrawal S., Anderson P., Durbeej M., van Rooijen N., Ivars F., Opdenakker G., Sorokin L.M. Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis. J. Exp. Med. 2006, 203:1007.
123. Gimenez M.A., Sim J.E., Russell J.H. TNFR1-dependent VCAM-expression by astrocytes exposes the CNS to destructive inflammation. J. Neuroimmunol. 2004, 151:116.
124. van Horssen J., Bo L., Vos C.M., Virtanen I., de Vries H.E. Basement membrane proteins in multiple sclerosis-associated inflammatory cuffs: potential role in influx and transport of leukocytes. J. Neuropathol. Exp. Neurol. 2005, 64:722.
125. Voskuhl R.R., Peterson R.S., Song B., Ao Y., Morales L.B., Tiwari-Woodruff S., Sofroniew M.V. Reactive astrocytes form scar-like perivascular barriers to leukocytes during adaptive immune inflammation of the CNS. J. Neurosci. 2009, 29:11511.
126. Bechmann I., Steiner B., Gimsa U., Mor G., Wolf S., Beyer M., Nitsch R., Zipp F. Astrocyte-induced T cell elimination is CD95 ligand dependent. J. Neuroimmunol. 2002, 132:60.
127. Hara H., Nanri Y., Tabata E., Mitsutake S., Tabira T. Identification of astrocyte-derived immune suppressor factor that induces apoptosis of autoreactive T cells. J. Neuroimmunol. 2011, 233:135.
128. Mohan H., Krumbholz M., Sharma R., Eisele S., Junker A., Sixt M., Newcombe J., Wekerle H., Hohlfeld R., Lassmann H. Extracellular matrix in multiple sclerosis lesions: fibrillar collagens, biglycan and decorin are upregulated and associated with infiltrating immune cells. Brain Pathol. 2010, 20:966.
129. Alvarez J.I., Dodelet-Devillers A., Kebir H., Ifergan I., Fabre P.J., Terouz S., Sabbagh M., Wosik K., Bourbonnière L., Bernard M. The Hedgehog pathway promotes blood-brain barrier integrity and CNS immune quiescence. Science 2011, 334:1727.
130. Mizee M.R., Nijland P.G., van der Pol S.M., Drexhage J.A., van het Hof B., Mebius R., van der Valk P., van Horssen J., Reijerkerk A., de Vries H.E. Astrocyte-derived retinoic acid: a novel regulator of blood-brain barrier function in multiple sclerosis. Acta Neuropathol. 2014, 128:691.
131. Xu J., Drew P.D. 9-Cis-retinoic acid suppresses inflammatory responses of microglia and astrocytes. J. Neuroimmunol. 2006, 171:135.
132. Katsuki H., Kurimoto E., Takemori S., Kurauchi Y., Hisatsune A., Isohama Y., Izumi Y., Kume T., Shudo K., Akaike A. Retinoic acid receptor stimulation protects midbrain dopaminergic neurons from inflammatory degeneration via BDNF-mediated signaling. J. Neurochem. 2009, 110:707.
133. Klemann C., Raveney B.J., Klemann A.K., Ozawa T., von Horsten S., Shudo K., Oki S., Yamamura T. Synthetic retinoid AM80 inhibits Th17 cells and ameliorates experimental autoimmune encephalomyelitis. Am. J. Pathol. 2009, 174:2234.
134. Løken-Amsrud K.I., Myhr K.M., Bakke S.J., Beiske A.G., Bjerve K.S., Bjørnarå B.T., Hovdal H., Lilleås F., Midgard R., Pedersen T. Retinol levels are associated with magnetic resonance imaging outcomes in multiple sclerosis. Mult. Scler. J. 2012, (1352458512457843).
135. Runia T.F., Hop W.C.J., de Rijke Y.B., Hintzen R.Q. Vitamin A is not associated with exacerbations in multiple sclerosis. Mult. Scler. Relat. Disord. 2014, 3:34.
136. Liebner S., Corada M., Bangsow T., Babbage J., Taddei A., Czupalla C.J., Reis M., Felici A., Wolburg H., Fruttiger M. Wnt/β-catenin signaling controls development of the blood-brain barrier. J. Cell Biol. 2008, 183:409.
137. Daneman R., Agalliu D., Zhou L., Kuhnert F., Kuo C.J., Barres B.A. Wnt/β-catenin signaling is required for CNS, but not non-CNS, angiogenesis. Proc. Natl. Acad. Sci. 2009, 106:641.
138. Daneman R., Zhou L., Kebede A.A., Barres B.A. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 2010, 468:562.
139. D'haeseleer M., Hostenbach S., Peeters I., El Sankari S., Nagels G., De Keyser J., D'hooghe M.B. Cerebral hypoperfusion: a new pathophysiologic concept in multiple sclerosis?. J. Cereb. Blood Flow Metab. 2015.
140. van Horssen J., Witte M.E., Schreibelt G., de Vries H.E. Radical changes in multiple sclerosis pathogenesis. Biochim. Biophys. Acta (BBA) - Mol. Basis Dis. 2011, 1812:141.
141. Fazel Nabavi S., Dean M., Turner A., Sureda A., Daglia M., Mohammad Nabavi S. Oxidative stress and post-stroke depression: possible therapeutic role of polyphenols?. Curr. Med. Chem. 2015, 22:343.