Oncostatin M triggers brain inflammation by compromising blood-brain barrier integrity.
Blood–brain barrier
Endothelial cells
Multiple sclerosis
Neuroinflammation
Oncostatin M
T helper 17 cells
Journal
Acta neuropathologica
ISSN: 1432-0533
Titre abrégé: Acta Neuropathol
Pays: Germany
ID NLM: 0412041
Informations de publication
Date de publication:
08 2022
08 2022
Historique:
received:
01
03
2022
accepted:
23
05
2022
revised:
06
05
2022
pubmed:
7
6
2022
medline:
20
7
2022
entrez:
6
6
2022
Statut:
ppublish
Résumé
Oncostatin M (OSM) is an IL-6 family member which exerts neuroprotective and remyelination-promoting effects after damage to the central nervous system (CNS). However, the role of OSM in neuro-inflammation is poorly understood. Here, we investigated OSM's role in pathological events important for the neuro-inflammatory disorder multiple sclerosis (MS). We show that OSM receptor (OSMRβ) expression is increased on circulating lymphocytes of MS patients, indicating their elevated responsiveness to OSM signalling. In addition, OSM production by activated myeloid cells and astrocytes is increased in MS brain lesions. In experimental autoimmune encephalomyelitis (EAE), a preclinical model of MS, OSMRβ-deficient mice exhibit milder clinical symptoms, accompanied by diminished T helper 17 (Th17) cell infiltration into the CNS and reduced BBB leakage. In vitro, OSM reduces BBB integrity by downregulating the junctional molecules claudin-5 and VE-cadherin, while promoting secretion of the Th17-attracting chemokine CCL20 by inflamed BBB-endothelial cells and reactive astrocytes. Using flow cytometric fluorescence resonance energy transfer (FRET) quantification, we found that OSM-induced endothelial CCL20 promotes activation of lymphocyte function-associated antigen 1 (LFA-1) on Th17 cells. Moreover, CCL20 enhances Th17 cell adhesion to OSM-treated inflamed endothelial cells, which is at least in part ICAM-1 mediated. Together, these data identify an OSM-CCL20 axis, in which OSM contributes significantly to BBB impairment during neuro-inflammation by inducing permeability while recruiting Th17 cells via enhanced endothelial CCL20 secretion and integrin activation. Therefore, care should be taken when considering OSM as a therapeutic agent for treatment of neuro-inflammatory diseases such as MS.
Identifiants
pubmed: 35666306
doi: 10.1007/s00401-022-02445-0
pii: 10.1007/s00401-022-02445-0
doi:
Substances chimiques
Oncostatin M Receptor beta Subunit
0
Oncostatin M
106956-32-5
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
259-281Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Abraham M, Karni A, Mausner-Fainberg K, Weiss ID, Peled A (2017) Natural and induced immunization against CCL20 ameliorate experimental autoimmune encephalitis and may confer protection against multiple sclerosis. Clin Immunol 183:316–324. https://doi.org/10.1016/j.clim.2017.09.018
doi: 10.1016/j.clim.2017.09.018
pubmed: 28939272
Akgün K, Blankenburg J, Marggraf M, Haase R, Ziemssen T (2020) Event-driven immunoprofiling predicts return of disease activity in alemtuzumab-treated multiple sclerosis. Front Immunol 11:56. https://doi.org/10.3389/fimmu.2020.00056
doi: 10.3389/fimmu.2020.00056
pubmed: 32082320
pmcid: 7005935
Alcaide P, Maganto-Garcia E, Newton G, Travers R, Croce KJ, Bu DX et al (2012) Difference in Th1 and Th17 lymphocyte adhesion to endothelium. J Immunol 188(3):1421–1430. https://doi.org/10.4049/jimmunol.1101647
doi: 10.4049/jimmunol.1101647
pubmed: 22219321
Alon R, Shulman Z (2011) Chemokine triggered integrin activation and actin remodeling events guiding lymphocyte migration across vascular barriers. Exp Cell Res 317(5):632–641. https://doi.org/10.1016/j.yexcr.2010.12.007
doi: 10.1016/j.yexcr.2010.12.007
pubmed: 21376176
Ambrosini E, Remoli ME, Giacomini E, Rosicarelli B, Serafini B et al (2005) Astrocytes produce dendritic cell-attracting chemokines in vitro and in multiple sclerosis lesions. J Neuropathol Exp Neurol 64(8):706–715. https://doi.org/10.1097/01.jnen.0000173893.01929.fc
doi: 10.1097/01.jnen.0000173893.01929.fc
pubmed: 16106219
Benson K, Cramer S, Galla HJ (2013) Impedance-based cell monitoring: barrier properties and beyond. Fluids Barriers CNS 10(1):5. https://doi.org/10.1186/2045-8118-10-5
doi: 10.1186/2045-8118-10-5
pubmed: 23305242
pmcid: 3560213
Broux B, Gowing E, Prat A (2015) Glial regulation of the blood-brain barrier in health and disease. Semin Immunopathol 37(6):577–590. https://doi.org/10.1007/s00281-015-0516-2
doi: 10.1007/s00281-015-0516-2
pubmed: 26245144
Broux B, Zandee S, Gowing E, Charabati M, Lécuyer MA, Tastet O et al (2020) Interleukin-26, preferentially produced by T(H)17 lymphocytes, regulates CNS barrier function. Neurol Neuroimmunol Neuroinflamm. https://doi.org/10.1212/nxi.0000000000000870
doi: 10.1212/nxi.0000000000000870
pubmed: 32788322
pmcid: 7428369
Chen SH, Benveniste EN (2004) Oncostatin M: a pleiotropic cytokine in the central nervous system. Cytokine Growth Factor Rev 15(5):379–391. https://doi.org/10.1016/j.cytogfr.2004.06.002
doi: 10.1016/j.cytogfr.2004.06.002
pubmed: 15450253
Chigaev A, Smagley Y, Haynes MK, Ursu O, Bologa CG, Halip L et al (2015) FRET detection of lymphocyte function-associated antigen-1 conformational extension. Mol Biol Cell 26(1):43–54. https://doi.org/10.1091/mbc.E14-06-1050
doi: 10.1091/mbc.E14-06-1050
pubmed: 25378583
pmcid: 4279228
Deerhake ME, Danzaki K, Inoue M, Cardakli ED, Nonaka T, Aggarwal N et al (2021) Dectin-1 limits autoimmune neuroinflammation and promotes myeloid cell-astrocyte crosstalk via Card9-independent expression of Oncostatin M. Immunity 54(3):484–98.e8. https://doi.org/10.1016/j.immuni.2021.01.004
doi: 10.1016/j.immuni.2021.01.004
pubmed: 33581044
pmcid: 7956124
Dendrou CA, Fugger L, Friese MA (2015) Immunopathology of multiple sclerosis. Nat Rev Immunol 15(9):545–558. https://doi.org/10.1038/nri3871
doi: 10.1038/nri3871
pubmed: 26250739
Dhaeze T, Tremblay L, Lachance C, Peelen E, Zandee S, Grasmuck C et al (2019) CD70 defines a subset of proinflammatory and CNS-pathogenic T(H)1/T(H)17 lymphocytes and is overexpressed in multiple sclerosis. Cell Mol Immunol 16(7):652–665. https://doi.org/10.1038/s41423-018-0198-5
doi: 10.1038/s41423-018-0198-5
pubmed: 30635649
pmcid: 6804668
Drechsler J, Grötzinger J, Hermanns HM (2012) Characterization of the rat oncostatin M receptor complex which resembles the human, but differs from the murine cytokine receptor. PLoS ONE 7(8):e43155. https://doi.org/10.1371/journal.pone.0043155
doi: 10.1371/journal.pone.0043155
pubmed: 22937020
pmcid: 3425591
El Sharkawi FZ, Ali SA, Hegazy MI, Atya HB (2019) The combined effect of IL-17F and CCL20 gene polymorphism in susceptibility to multiple sclerosis in Egypt. Gene 685:164–169. https://doi.org/10.1016/j.gene.2018.11.006
doi: 10.1016/j.gene.2018.11.006
pubmed: 30399422
Ensoli F, Fiorelli V, Lugaresi A, Farina D, De Cristofaro M, Collacchi B et al (2002) Lymphomononuclear cells from multiple sclerosis patients spontaneously produce high levels of oncostatin M, tumor necrosis factors alpha and beta, and interferon gamma. Mult Scler 8(4):284–288. https://doi.org/10.1191/1352458502ms817oa
doi: 10.1191/1352458502ms817oa
pubmed: 12166497
Fearon U, Mullan R, Markham T, Connolly M, Sullivan S, Poole AR et al (2006) Oncostatin M induces angiogenesis and cartilage degradation in rheumatoid arthritis synovial tissue and human cartilage cocultures. Arthritis Rheum 54(10):3152–3162. https://doi.org/10.1002/art.22161
doi: 10.1002/art.22161
pubmed: 17009243
Fitzhugh DJ, Naik S, Caughman SW, Hwang ST (2000) Cutting edge: C-C chemokine receptor 6 is essential for arrest of a subset of memory T cells on activated dermal microvascular endothelial cells under physiologic flow conditions in vitro. J Immunol 165(12):6677–6681. https://doi.org/10.4049/jimmunol.165.12.6677
doi: 10.4049/jimmunol.165.12.6677
pubmed: 11120783
Ghannam S, Dejou C, Pedretti N, Giot JP, Dorgham K, Boukhaddaoui H et al (2011) CCL20 and β-defensin-2 induce arrest of human Th17 cells on inflamed endothelium in vitro under flow conditions. J Immunol 186(3):1411–1420. https://doi.org/10.4049/jimmunol.1000597
doi: 10.4049/jimmunol.1000597
pubmed: 21178014
Haghayegh Jahromi N, Marchetti L, Moalli F, Duc D, Basso C, Tardent H et al (2019) Intercellular adhesion molecule-1 (ICAM-1) and ICAM-2 differentially contribute to peripheral activation and CNS entry of autoaggressive Th1 and Th17 cells in experimental autoimmune encephalomyelitis. Front Immunol 10:3056. https://doi.org/10.3389/fimmu.2019.03056
doi: 10.3389/fimmu.2019.03056
pubmed: 31993059
Hanlon MM, Rakovich T, Cunningham CC, Ansboro S, Veale DJ, Fearon U et al (2019) STAT3 mediates the differential effects of Oncostatin M and TNFα on RA synovial fibroblast and endothelial cell function. Front Immunol 10:2056. https://doi.org/10.3389/fimmu.2019.02056
doi: 10.3389/fimmu.2019.02056
pubmed: 31555281
pmcid: 6724663
Haroon F, Drögemüller K, Händel U, Brunn A, Reinhold D, Nishanth G et al (2011) Gp130-dependent astrocytic survival is critical for the control of autoimmune central nervous system inflammation. J Immunol 186(11):6521–6531. https://doi.org/10.4049/jimmunol.1001135
doi: 10.4049/jimmunol.1001135
pubmed: 21515788
Houben E, Hellings N, Broux B (2019) Oncostatin M, an underestimated player in the central nervous system. Front Immunol 10:1165. https://doi.org/10.3389/fimmu.2019.01165
doi: 10.3389/fimmu.2019.01165
pubmed: 31191538
pmcid: 6549448
Houben E, Janssens K, Hermans D, Vandooren J, Van den Haute C, Schepers M et al (2020) Oncostatin M-induced astrocytic tissue inhibitor of metalloproteinases-1 drives remyelination. Proc Natl Acad Sci U S A 117(9):5028–5038. https://doi.org/10.1073/pnas.1912910117
doi: 10.1073/pnas.1912910117
pubmed: 32071226
pmcid: 7060743
Huang J, Khademi M, Fugger L, Lindhe Ö, Novakova L, Axelsson M et al (2020) Inflammation-related plasma and CSF biomarkers for multiple sclerosis. Proc Natl Acad Sci U S A 117(23):12952–12960. https://doi.org/10.1073/pnas.1912839117
doi: 10.1073/pnas.1912839117
pubmed: 32457139
pmcid: 7293699
Ichihara M, Hara T, Kim H, Murate T, Miyajima A (1997) Oncostatin M and leukemia inhibitory factor do not use the same functional receptor in mice. Blood 90(1):165–173
doi: 10.1182/blood.V90.1.165.165_165_173
Ishiwata I, Ishiwata C, Ishiwata E, Sato Y, Kiguchi K, Tachibana T et al (2005) Establishment and characterization of a human malignant choroids plexus papilloma cell line (HIBCPP). Hum Cell 18(1):67–72. https://doi.org/10.1111/j.1749-0774.2005.tb00059.x
doi: 10.1111/j.1749-0774.2005.tb00059.x
pubmed: 16130902
Janssens K, Maheshwari A, Van den Haute C, Baekelandt V, Stinissen P, Hendriks JJ et al (2015) Oncostatin M protects against demyelination by inducing a protective microglial phenotype. Glia 63(10):1729–1737. https://doi.org/10.1002/glia.22840
doi: 10.1002/glia.22840
pubmed: 25921393
Janssens K, Van den Haute C, Baekelandt V, Lucas S, van Horssen J, Somers V et al (2015) Leukemia inhibitory factor tips the immune balance towards regulatory T cells in multiple sclerosis. Brain Behav Immun 45:180–188. https://doi.org/10.1016/j.bbi.2014.11.010
doi: 10.1016/j.bbi.2014.11.010
pubmed: 25514345
Jones SA, Jenkins BJ (2018) Recent insights into targeting the IL-6 cytokine family in inflammatory diseases and cancer. Nat Rev Immunol 18(12):773–789. https://doi.org/10.1038/s41577-018-0066-7
doi: 10.1038/s41577-018-0066-7
pubmed: 30254251
Kerfoot SM, Raharjo E, Ho M, Kaur J, Serirom S, McCafferty DM et al (2001) Exclusive neutrophil recruitment with oncostatin M in a human system. Am J Pathol 159(4):1531–1539. https://doi.org/10.1016/s0002-9440(10)62538-2
doi: 10.1016/s0002-9440(10)62538-2
pubmed: 11583979
pmcid: 1850489
Larochelle C, Cayrol R, Kebir H, Alvarez JI, Lécuyer MA, Ifergan I et al (2012) Melanoma cell adhesion molecule identifies encephalitogenic T lymphocytes and promotes their recruitment to the central nervous system. Brain 135(Pt 10):2906–2924. https://doi.org/10.1093/brain/aws212
doi: 10.1093/brain/aws212
pubmed: 22975388
Lassmann H, Bradl M (2017) Multiple sclerosis: experimental models and reality. Acta Neuropathol 133(2):223–244. https://doi.org/10.1007/s00401-016-1631-4
doi: 10.1007/s00401-016-1631-4
pubmed: 27766432
Lee DSW, Yam JY, Grasmuck C, Dasoveanu D, Michel L, Ward LA et al (2021) CCR6 expression on B cells is not required for clinical or pathological presentation of MOG protein-induced experimental autoimmune encephalomyelitis despite an altered germinal center response. J Immunol 207(6):1513–1521. https://doi.org/10.4049/jimmunol.2001413
doi: 10.4049/jimmunol.2001413
pubmed: 34400521
Li R, Sun X, Shu Y, Wang Y, Xiao L, Wang Z et al (2017) Serum CCL20 and its association with SIRT1 activity in multiple sclerosis patients. J Neuroimmunol 313:56–60. https://doi.org/10.1016/j.jneuroim.2017.10.013
doi: 10.1016/j.jneuroim.2017.10.013
pubmed: 29153609
Lindberg RA, Juan TS, Welcher AA, Sun Y, Cupples R, Guthrie B et al (1998) Cloning and characterization of a specific receptor for mouse oncostatin M. Mol Cell Biol 18(6):3357–3367. https://doi.org/10.1128/mcb.18.6.3357
doi: 10.1128/mcb.18.6.3357
pubmed: 9584176
pmcid: 108917
Liston A, Kohler RE, Townley S, Haylock-Jacobs S, Comerford I, Caon AC et al (2009) Inhibition of CCR6 function reduces the severity of experimental autoimmune encephalomyelitis via effects on the priming phase of the immune response. J Immunol 182(5):3121–3130. https://doi.org/10.4049/jimmunol.0713169
doi: 10.4049/jimmunol.0713169
pubmed: 19234209
Lopes Pinheiro MA, Kooij G, Mizee MR, Kamermans A, Enzmann G, Lyck R et al (1862) (2016) Immune cell trafficking across the barriers of the central nervous system in multiple sclerosis and stroke. Biochim Biophys Acta 3:461–471. https://doi.org/10.1016/j.bbadis.2015.10.018
doi: 10.1016/j.bbadis.2015.10.018
Ma Q, Shimaoka M, Lu C, Jing H, Carman CV, Springer TA (2002) Activation-induced conformational changes in the I domain region of lymphocyte function-associated antigen 1. J Biol Chem 277(12):10638–10641. https://doi.org/10.1074/jbc.M112417200
doi: 10.1074/jbc.M112417200
pubmed: 11792712
Maki W, Morales RE, Carroll VA, Telford WG, Knibbs RN, Stoolman LM et al (2002) CCR6 colocalizes with CD18 and enhances adhesion to activated endothelial cells in CCR6-transduced jurkat T cells. J Immunol 169(5):2346–2353. https://doi.org/10.4049/jimmunol.169.5.2346
doi: 10.4049/jimmunol.169.5.2346
pubmed: 12193700
Marchetti L, Engelhardt B (2020) Immune cell trafficking across the blood-brain barrier in the absence and presence of neuroinflammation. Vasc Biol 2(1):H1-h18. https://doi.org/10.1530/vb-19-0033
doi: 10.1530/vb-19-0033
pubmed: 32923970
pmcid: 7439848
Meares GP, Ma X, Qin H, Benveniste EN (2012) Regulation of CCL20 expression in astrocytes by IL-6 and IL-17. Glia 60(5):771–781. https://doi.org/10.1002/glia.22307
doi: 10.1002/glia.22307
pubmed: 22319003
Michel L, Grasmuck C, Charabati M, Lécuyer MA, Zandee S, Dhaeze T et al (2019) Activated leukocyte cell adhesion molecule regulates B lymphocyte migration across central nervous system barriers. Sci Transl Med. https://doi.org/10.1126/scitranslmed.aaw0475
doi: 10.1126/scitranslmed.aaw0475
pubmed: 31723036
Moidunny S, Dias RB, Wesseling E, Sekino Y, Boddeke HW, Sebastião AM et al (2010) Interleukin-6-type cytokines in neuroprotection and neuromodulation: oncostatin M, but not leukemia inhibitory factor, requires neuronal adenosine A1 receptor function. J Neurochem 114(6):1667–1677. https://doi.org/10.1111/j.1471-4159.2010.06881.x
doi: 10.1111/j.1471-4159.2010.06881.x
pubmed: 20598020
Mony JT, Khorooshi R, Owens T (2014) Chemokine receptor expression by inflammatory T cells in EAE. Front Cell Neurosci 8:187. https://doi.org/10.3389/fncel.2014.00187
doi: 10.3389/fncel.2014.00187
pubmed: 25071447
pmcid: 4081975
Moser T, Akgün K, Proschmann U, Sellner J, Ziemssen T (2020) The role of TH17 cells in multiple sclerosis: therapeutic implications. Autoimmun Rev 19(10):102647. https://doi.org/10.1016/j.autrev.2020.102647
doi: 10.1016/j.autrev.2020.102647
pubmed: 32801039
Murakami M, Kamimura D, Hirano T (2019) Pleiotropy and specificity: insights from the interleukin 6 family of cytokines. Immunity 50(4):812–831. https://doi.org/10.1016/j.immuni.2019.03.027
doi: 10.1016/j.immuni.2019.03.027
pubmed: 30995501
Nakamura K, Nonaka H, Saito H, Tanaka M, Miyajima A (2004) Hepatocyte proliferation and tissue remodeling is impaired after liver injury in oncostatin M receptor knockout mice. Hepatology 39(3):635–644. https://doi.org/10.1002/hep.20086
doi: 10.1002/hep.20086
pubmed: 14999682
Profaci CP, Munji RN, Pulido RS, Daneman R (2020) The blood-brain barrier in health and disease: important unanswered questions. J Exp Med. https://doi.org/10.1084/jem.20190062
doi: 10.1084/jem.20190062
pubmed: 32211826
pmcid: 7144528
Reboldi A, Coisne C, Baumjohann D, Benvenuto F, Bottinelli D, Lira S et al (2009) C-C 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 10(5):514–523. https://doi.org/10.1038/ni.1716
doi: 10.1038/ni.1716
pubmed: 19305396
Repovic P, Benveniste EN (2002) Prostaglandin E2 is a novel inducer of oncostatin-M expression in macrophages and microglia. J Neurosci 22(13):5334–5343. https://doi.org/10.1523/jneurosci.22-13-05334.2002
doi: 10.1523/jneurosci.22-13-05334.2002
pubmed: 12097485
pmcid: 6758185
Rodríguez-Lorenzo S, Ferreira Francisco DM, Vos R, van Het Hof B, Rijnsburger M, Schroten H et al (2020) Altered secretory and neuroprotective function of the choroid plexus in progressive multiple sclerosis. Acta Neuropathol Commun 8(1):35. https://doi.org/10.1186/s40478-020-00903-y
doi: 10.1186/s40478-020-00903-y
pubmed: 32192527
pmcid: 7083003
Ruprecht K, Kuhlmann T, Seif F, Hummel V, Kruse N, Brück W et al (2001) Effects of oncostatin M on human cerebral endothelial cells and expression in inflammatory brain lesions. J Neuropathol Exp Neurol 60(11):1087–1098. https://doi.org/10.1093/jnen/60.11.1087
doi: 10.1093/jnen/60.11.1087
pubmed: 11706938
Sambrano J, Chigaev A, Nichani KS, Smagley Y, Sklar LA, Houston JP (2018) Evaluating integrin activation with time-resolved flow cytometry. J Biomed Opt 23(7):1–10. https://doi.org/10.1117/1.Jbo.23.7.075004
doi: 10.1117/1.Jbo.23.7.075004
pubmed: 29992797
Slaets H, Nelissen S, Janssens K, Vidal PM, Lemmens E, Stinissen P et al (2014) Oncostatin M reduces lesion size and promotes functional recovery and neurite outgrowth after spinal cord injury. Mol Neurobiol 50(3):1142–1151. https://doi.org/10.1007/s12035-014-8795-5
doi: 10.1007/s12035-014-8795-5
pubmed: 24996996
Srinivasan B, Kolli AR, Esch MB, Abaci HE, Shuler ML, Hickman JJ (2015) TEER measurement techniques for in vitro barrier model systems. J Lab Autom 20(2):107–126. https://doi.org/10.1177/2211068214561025
doi: 10.1177/2211068214561025
pubmed: 25586998
pmcid: 4652793
Sugaya M, Fang L, Cardones AR, Kakinuma T, Jaber SH, Blauvelt A et al (2006) Oncostatin M enhances CCL21 expression by microvascular endothelial cells and increases the efficiency of dendritic cell trafficking to lymph nodes. J Immunol 177(11):7665–7672. https://doi.org/10.4049/jimmunol.177.11.7665
doi: 10.4049/jimmunol.177.11.7665
pubmed: 17114436
Takata F, Dohgu S, Matsumoto J, Machida T, Sakaguchi S, Kimura I et al (2018) Oncostatin M-induced blood-brain barrier impairment is due to prolonged activation of STAT3 signaling in vitro. J Cell Biochem 119(11):9055–9063. https://doi.org/10.1002/jcb.27162
doi: 10.1002/jcb.27162
pubmed: 30076740
Takata F, Dohgu S, Sakaguchi S, Sakai K, Yamanaka G, Iwao T et al (2019) Oncostatin-M-reactive pericytes aggravate blood-brain barrier dysfunction by activating JAK/STAT3 signaling in vitro. Neuroscience 422:12–20. https://doi.org/10.1016/j.neuroscience.2019.10.014
doi: 10.1016/j.neuroscience.2019.10.014
pubmed: 31705893
Takata F, Sumi N, Nishioku T, Harada E, Wakigawa T, Shuto H et al (2008) Oncostatin M induces functional and structural impairment of blood-brain barriers comprised of rat brain capillary endothelial cells. Neurosci Lett 441(2):163–166. https://doi.org/10.1016/j.neulet.2008.06.030
doi: 10.1016/j.neulet.2008.06.030
pubmed: 18603369
Tanaka M, Hirabayashi Y, Sekiguchi T, Inoue T, Katsuki M, Miyajima A (2003) Targeted disruption of oncostatin M receptor results in altered hematopoiesis. Blood 102(9):3154–3162. https://doi.org/10.1182/blood-2003-02-0367
doi: 10.1182/blood-2003-02-0367
pubmed: 12855584
Tenenbaum T, Steinmann U, Friedrich C, Berger J, Schwerk C, Schroten H (2013) Culture models to study leukocyte trafficking across the choroid plexus. Fluids Barriers CNS 10(1):1. https://doi.org/10.1186/2045-8118-10-1
doi: 10.1186/2045-8118-10-1
pubmed: 23305147
pmcid: 3560101
Tinevez JY, Perry N, Schindelin J, Hoopes GM, Reynolds GD, Laplantine E et al (2017) TrackMate: an open and extensible platform for single-particle tracking. Methods 115:80–90. https://doi.org/10.1016/j.ymeth.2016.09.016
doi: 10.1016/j.ymeth.2016.09.016
pubmed: 27713081
Ujlaky-Nagy L, Nagy P, Szöllősi J, Vereb G (2018) Flow cytometric FRET analysis of protein interactions. Methods Mol Biol 1678:393–419. https://doi.org/10.1007/978-1-4939-7346-0_17
doi: 10.1007/978-1-4939-7346-0_17
pubmed: 29071688
van Keulen D, Pouwer MG, Pasterkamp G, van Gool AJ, Sollewijn Gelpke MD, Princen HMG et al (2018) Inflammatory cytokine oncostatin M induces endothelial activation in macro- and microvascular endothelial cells and in APOE*3Leiden.CETP mice. PLoS One 13(10):e0204911. https://doi.org/10.1371/journal.pone.0204911
doi: 10.1371/journal.pone.0204911
pubmed: 30273401
pmcid: 6166945
Villares R, Cadenas V, Lozano M, Almonacid L, Zaballos A, Martínez AC et al (2009) CCR6 regulates EAE pathogenesis by controlling regulatory CD4+ T-cell recruitment to target tissues. Eur J Immunol 39(6):1671–1681. https://doi.org/10.1002/eji.200839123
doi: 10.1002/eji.200839123
pubmed: 19499521
Walling BL, Kim M (2018) LFA-1 in T cell migration and differentiation. Front Immunol 9:952. https://doi.org/10.3389/fimmu.2018.00952
doi: 10.3389/fimmu.2018.00952
pubmed: 29774029
pmcid: 5943560
Weiss TW, Samson AL, Niego B, Daniel PB, Medcalf RL (2006) Oncostatin M is a neuroprotective cytokine that inhibits excitotoxic injury in vitro and in vivo. Faseb j 20(13):2369–2371. https://doi.org/10.1096/fj.06-5850fje
doi: 10.1096/fj.06-5850fje
pubmed: 17023520
Weksler B, Romero IA, Couraud PO (2013) The hCMEC/D3 cell line as a model of the human blood brain barrier. Fluids Barriers CNS 10(1):16. https://doi.org/10.1186/2045-8118-10-16
doi: 10.1186/2045-8118-10-16
pubmed: 23531482
pmcid: 3623852
Wojkowska DW, Szpakowski P, Glabinski A (2017) Interleukin 17A promotes lymphocytes adhesion and induces CCL2 and CXCL1 release from brain endothelial cells. Int J Mol Sci. https://doi.org/10.3390/ijms18051000
doi: 10.3390/ijms18051000
pubmed: 28481289
pmcid: 5454913
Zhang X, Li J, Qin JJ, Cheng WL, Zhu X, Gong FH et al (2017) Oncostatin M receptor β deficiency attenuates atherogenesis by inhibiting JAK2/STAT3 signaling in macrophages. J Lipid Res 58(5):895–906. https://doi.org/10.1194/jlr.M074112
doi: 10.1194/jlr.M074112
pubmed: 28258089
pmcid: 5408608