Phospholipase D1 mediates lymphocyte adhesion and migration in experimental autoimmune encephalomyelitis

European Journal of Immunology

Volumn 44, Issue 8, 2014, Pages 2295-2305

  Göbel, Kerstin ^a   Schuhmann, Michael K ^a,b   Pankratz, Susann ^a   Stegner, David ^b,c   Herrmann, Alexander M ^a   Braun, Attila ^c   Breuer, Johanna ^a   Bittner, Stefan ^a   Ruck, Tobias ^a   Wiendl, Heinz ^a   Kleinschnitz, Christoph ^b   Nieswandt, Bernhard ^c   Meuth, Sven G ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Central nervous system inflammation; Experimental autoimmune encephalomyelitis; Lymphocyte migration; Multiple sclerosis; Phospholipase D1 (PLD1)

Indexed keywords

GAMMA INTERFERON; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 4; INTERLEUKIN 6; L SELECTIN; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHOLIPASE D1; STROMAL CELL DERIVED FACTOR 1; TRANSFORMING GROWTH FACTOR BETA; VASCULAR CELL ADHESION MOLECULE 1; VERY LATE ACTIVATION ANTIGEN 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; BRAIN SLICE; CELL ADHESION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE COURSE; DISEASE SEVERITY; ENDOTHELIUM CELL; ENZYME ACTIVITY; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOCOMPETENT CELL; INTRACELLULAR SIGNALING; LYMPHOCYTE ACTIVATION; LYMPHOCYTE ADHESION; LYMPHOCYTE FUNCTION; LYMPHOCYTE MIGRATION; MORBIDITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; SPLEEN CELL; TIGHT JUNCTION;

CENTRAL NERVOUS SYSTEM INFLAMMATION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; LYMPHOCYTE MIGRATION; MULTIPLE SCLEROSIS; PHOSPHOLIPASE D1 (PLD1);

ANIMALS; BLOOD-BRAIN BARRIER; CELL ADHESION; CELL MOVEMENT; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ENDOTHELIAL CELLS; FEMALE; INFLAMMATION; INTERCELLULAR ADHESION MOLECULE-1; LYMPHOCYTES; MICE; MICE, INBRED C57BL; PHOSPHOLIPASE D; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84906091157     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201344107     Document Type: Article

References (42)

1. Engelhardt, B., Molecular mechanisms involved in T cell migration across the blood-brain barrier. J. Neural. Transm. 2006. 113: 477-485.
2. Engelhardt, B. and Ransohoff, R. M., The ins and outs of T-lymphocyte trafficking to the CNS: anatomical sites and molecular mechanisms. Trends Immunol. 2005. 26: 485-495.
3. Engelhardt, B. and Ransohoff, R. M., Capture, crawl, cross: the T cell code to breach the blood-brain barriers. Trends Immunol. 2012. 33: 579-589.
4. Lyck, R. and Engelhardt, B., Going against the tide-how encephalitogenic T cells breach the blood-brain barrier. J. Vasc. Res. 2012. 49: 497-509.
5. Holman, D. W., Klein, R. S. and Ransohoff, R. M., The blood-brain barrier, chemokines and multiple sclerosis. Biochim. Biophys. Acta 2011. 1812: 220-230.
6. Takeshita, Y. and Ransohoff, R. M., Inflammatory cell trafficking across the blood-brain barrier: chemokine regulation and in vitro models. Immunol. Rev. 2012. 248: 228-239.
7. Sospedra, M. and Martin, R., Immunology of multiple sclerosis. Annu. Rev. Immunol. 2005. 23: 683-747.
8. Prendergast, C. T. and Anderton, S. M., Immune cell entry to central nervous system-current understanding and prospective therapeutic targets. Endocr. Metab. Immune. Disord. Drug Targets 2009. 9: 315-327.
9. Steinman, L., Blocking adhesion molecules as therapy for multiple sclerosis: natalizumab. Nat. Rev. Drug Discov. 2005. 4: 510-518.
10. Ley, K., Laudanna, C., Cybulsky, M. I. and Nourshargh, S., Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 2007. 7: 678-689.
11. Wilson, E. H., Weninger, W. and Hunter, C. A., Trafficking of immune cells in the central nervous system. J. Clin. Invest 2010. 120: 1368-1379.
12. Cinamon, G., Shinder, V. and Alon, R., Shear forces promote lymphocyte migration across vascular endothelium bearing apical chemokines. Nat. Immunol. 2001. 2: 515-522.
13. Abram, C. L. and Lowell, C. A., The ins and outs of leukocyte integrin signaling. Annu. Rev. Immunol. 2009. 27: 339-362.
14. Kluger, M. S., Vascular endothelial cell adhesion and signaling during leukocyte recruitment. Adv. Dermatol. 2004. 20: 163-201.
15. Engelhardt, B. and Wolburg, H., Mini-review: transendothelial migration of leukocytes: through the front door or around the side of the house? Eur. J. Immunol. 2004. 34: 2955-2963.
16. Katagiri, K., Shimonaka, M. and Kinashi, T., Rap1-mediated lymphocyte function-associated antigen-1 activation by the T cell antigen receptor is dependent on phospholipase C-gamma1. J. Biol. Chem. 2004. 279: 11875-11881.
17. Shimonaka, M., Katagiri, K., Nakayama, T., Fujita, N., Tsuruo, T., Yoshie, O. and Kinashi, T., Rap1 translates chemokine signals to integrin activation, cell polarization, and motility across vascular endothelium under flow. J. Cell Biol. 2003. 161: 417-427.
18. Giagulli, C., Scarpini, E., Ottoboni, L., Narumiya, S., Butcher, E. C., Constantin, G. and Laudanna, C., RhoA and zeta PKC control distinct modalities of LFA-1 activation by chemokines: critical role of LFA-1 affinity triggering in lymphocyte in vivo homing. Immunity 2004. 20: 25-35.
19. Pasvolsky, R., Grabovsky, V., Giagulli, C., Shulman, Z., Shamri, R., Feigelson, S. W., Laudanna, C. et al., RhoA is involved in LFA-1 extension triggered by CXCL12 but not in a novel outside-in LFA-1 activation facilitated by CXCL9. J. Immunol. 2008. 180: 2815-2823.
20. Bolomini-Vittori, M., Montresor, A., Giagulli, C., Staunton, D., Rossi, B., Martinello, M., Constantin, G. et al., Regulation of conformer-specific activation of the integrin LFA-1 by a chemokine-triggered Rho signaling module. Nat. Immunol. 2009. 10: 185-194.
21. McDermott, M., Wakelam, M. J. and Morris, A. J., Phospholipase D. Biochem. Cell Biol. 2004. 82: 225-253.
22. Elvers, M., Stegner, D., Hagedorn, I., Kleinschnitz, C., Braun, A., Kuijpers, M. E., Boesl, M. et al., Impaired alpha(IIb)beta(3) integrin activation and shear-dependent thrombus formation in mice lacking phospholipase D1. Sci. Signal 2010. 3: ra1.
23. Knoepp, S. M., Chahal, M. S., Xie, Y., Zhang, Z., Brauner, D. J., Hallman, M. A., Robinson, S. A. et al., Effects of active and inactive phospholipase D2 on signal transduction, adhesion, migration, invasion, and metastasis in EL4 lymphoma cells. Mol. Pharmacol. 2008. 74: 574-584.
24. Nishikimi, A., Fukuhara, H., Su, W., Hongu, T., Takasuga, S., Mihara, H., Cao, Q. et al., Sequential regulation of DOCK2 dynamics by two phospholipids during neutrophil chemotaxis. Science 2009. 324: 384-387.
25. Meier, K. E., Gibbs, T. C., Knoepp, S. M. and Ella, K. M., Expression of phospholipase D isoforms in mammalian cells. Biochim. Biophys. Acta 1999. 1439: 199-213.
26. Stromnes, I. M. and Goverman, J. M., Active induction of experimental allergic encephalomyelitis. Nat. Protoc. 2006. 1: 1810-1819.
27. Bittner, S., Meuth, S. G., Gobel, K., Melzer, N., Herrmann, A. M., Simon, O. J., Weishaupt, A. et al., TASK1 modulates inflammation and neurodegeneration in autoimmune inflammation of the central nervous system. Brain 2009. 132: 2501-2516.
28. Gobel, K., Melzer, N., Herrmann, A. M., Schuhmann, M. K., Bittner, S., Ip, C. W., Hunig, T. et al., Collateral neuronal apoptosis in CNS gray matter during an oligodendrocyte-directed CD8(+) T cell attack. Glia 2010. 58: 469-480.
29. Huang, K., Geoffroy, J. S., Singer, M. S. and Rosen, S. D., A lymphocyte homing receptor (L-selectin) mediates the in vitro attachment of lymphocytes to myelinated tracts of the central nervous system. J. Clin. Invest 1991. 88: 1778-1783.
30. Huang, P. and Frohman, M. A., The potential for phospholipase D as a new therapeutic target. Expert Opin. Ther. Targets 2007. 11: 707-716.
31. Chae, Y. C., Kim, K. L., Ha, S. H., Kim, J., Suh, P. G. and Ryu, S. H., Protein kinase Cdelta-mediated phosphorylation of phospholipase D controls integrin-mediated cell spreading. Mol. Cell Biol. 2010. 30: 5086-5098.
32. Rudge, S. A. and Wakelam, M. J., Inter-regulatory dynamics of phospholipase D and the actin cytoskeleton. Biochim. Biophys. Acta 2009. 1791: 856-861.
33. Gomez-Cambronero, J., Di Fulvio, M. and Knapek, K., Understanding phospholipase D (PLD) using leukocytes: PLD involvement in cell adhesion and chemotaxis. J. Leukoc. Biol. 2007. 82: 272-281.
34. Ahn, M., Min, D. S., Kang, J., Jung, K. and Shin, T., Increased expression of phospholipase D1 in the spinal cords of rats with experimental autoimmune encephalomyelitis. Neurosci. Lett. 2001. 316: 95-98.
35. Hogg, N., Smith, A., McDowall, A., Giles, K., Stanley, P., Laschinger, M. and Henderson, R., How T cells use LFA-1 to attach and migrate. Immunol. Lett. 2004. 92: 51-54.
36. Garcia-Bernal, D., Wright, N., Sotillo-Mallo, E., Nombela-Arrieta, C., Stein, J. V., Bustelo, X. R. and Teixido, J., Vav1 and Rac control chemokine-promoted T lymphocyte adhesion mediated by the integrin alpha4beta1. Mol. Biol. Cell 2005. 16: 3223-3235.
37. Schneider-Hohendorf, T., Stenner, M. P., Weidenfeller, C., Zozulya, A. L., Simon, O. J., Schwab, N. and Wiendl, H., Regulatory T cells exhibit enhanced migratory characteristics, a feature impaired in patients with multiple sclerosis. Eur. J. Immunol. 2010. 40: 3581-3590.
38. Weidenfeller, C., Schrot, S., Zozulya, A. and Galla, H. J., Murine brain capillary endothelial cells exhibit improved barrier properties under the influence of hydrocortisone. Brain Res. 2005. 1053: 162-174.
39. Gobel, K., Pankratz, S., Schneider-Hohendorf, T., Bittner, S., Schuhmann, M. K., Langer, H. F., Stoll, G. et al., Blockade of the kinin receptor B1 protects from autoimmune CNS disease by reducing leukocyte trafficking. J. Autoimmun. 2011. 36: 106-114.
40. Racoosin, E. L. and Swanson, J. A., Macrophage colony stimulating factor (rM-CSF) stimulates pinocytosis in bone marrow-derived macrophages. J. Exp. Med. 1989. 170: 1635-1648.
41. Campbell, J. J., Hedrick, J., Zlotnik, A., Siani, M. A., Thompson, D. A. and Butcher, E. C., Chemokines and the arrest of lymphocytes rolling under flow conditions. Science 1998. 279: 381-384.
42. Schuhmann, M. K., Stegner, D., Berna-Erro, A., Bittner, S., Braun, A., Kleinschnitz, C., Stoll, G. et al., Stromal interaction molecules 1 and 2 are key regulators of autoreactive T cell activation in murine autoimmune central nervous system inflammation. J. Immunol. 2010. 184: 1536-1542.