Activated leukocyte cell adhesion molecule promotes leukocyte trafficking into the central nervous system

Nature Immunology

Volumn 9, Issue 2, 2008, Pages 137-145

  Cayrol, Romain ^a   Wosik, Karolina ^a   Berard, Jennifer L ^b   Dodelet Devillers, Aurore ^a   Ifergan, Igal ^a   Kebir, Hania ^a   Haqqani, Arsalan S ^c   Kreymborg, Katharina ^d   Krug, Sebastian ^a   Moumdjian, Robert ^a   Bouthillier, Alain ^a   Becher, Burkhard ^d   Arbour, Nathalie ^a   David, Samuel ^b   Stanimirovic, Danica ^c   Prat, Alexandre ^a  

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^b MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^d UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; IMMUNOGLOBULIN;

ADULT; AGED; ALLERGIC ENCEPHALOMYELITIS; ARTICLE; BLOOD BRAIN BARRIER; CD4+ T LYMPHOCYTE; CENTRAL NERVOUS SYSTEM; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; DRUG TARGETING; ENDOTHELIUM; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LEUKOCYTE ACTIVATION; LEUKOCYTE MIGRATION; LIPID RAFT; MALE; MONOCYTE; MULTIPLE SCLEROSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS; UPREGULATION;

ACTIVATED-LEUKOCYTE CELL ADHESION MOLECULE; BLOOD-BRAIN BARRIER; BRAIN; CD4-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; CELLS, CULTURED; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HUMANS; MEMBRANE MICRODOMAINS; PROTEOMICS;

EID: 38349176343     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni1551     Document Type: Article

References (47)

1. Bailey, S.L., Carpentier, P.A., McMahon, E.J., Begolka, W.S. & Miller, S.D. Innate and adaptive immune responses of the central nervous system. Crit. Rev. Immunol. 26, 149-188 (2006).
2. Hickey, W.F. Leukocyte traffic in the central nervous system: The participants and their roles, Semin. Immunol. 11, 125-137 (1999).
3. Lucchinetti, C. et al. Heterogeneity of multiple sclerosis lesions: Implications for the pathogenesis of demyelination. Ann. Neurol. 47, 707-717 (2000).
4. Noseworthy, J.H., Lucchinetti, C., Rodriguez, M. & Weinshenker, B.G. Multiple sclerosis. N. Engl. J. Med. 343, 938-952 (2000).
5. Butcher, E.C. Leukocyte-endothelial cell recognition: Three (or more) steps to specificity and diversity. Cell 67, 1033-1036 (1991).
6. Springer, T.A. Traffic signals for lymphocyte recirculation and leukocyte emigration: The multistep paradigm. Cell 76, 301-314 (1994).
7. Engelhardt, B. Regulation of immune cell entry into the central nervous system. Results Probl. Cell Differ. 43, 259-280 (2006).
8. von Andrian, U.H. & Mackay, C.R. T-cell function and migration. Two sides of the same coin. N. Engl. J. Med. 343, 1020-1034 (2000).
9. H-17 lymphocytes promote blood-brain barrier disruption and CNS inflammation. Nat. Med. 13, 1173-1175 (2007).
10. Ifergan, I. et al. Statins reduce human blood-brain barrier permeability and restrict leukocyte migration: Relevance to multiple sclerosis. Ann. Neurol. 60, 45-55 (2006).
11. Reijerkerk, A. et al. Diapedesis.of monocytes is associated with MMP-mediated occludin disappearance in brain endothelial cells. FASEB J. 20, 2550-2552 (2006).
12. Carman, C.V. & Springer, T.A. A transmigratory cup in leukocyte diapedesis both through individual vascular endothelial cells and between them. J. Cell Biol. 167, 377-388 (2004).
13. Bullard, D.C. et al. Intercellular adhesion molecule-1 expression is required on multiple cell types for the development of experimental autoimmune encephalomyelitis. J. Immunol. 178, 851-857 (2007).
14. Turowski, P., Adamson, P. & Greenwood, J. Pharmacological targeting of ICAM-1 signaling in brain endothelial cells: Potential for treating neuroinflammation. Cell. Mol. Neurobiol. 25, 153-170 (2005).
15. Walters, C.E. et al. Inhibition of Rho GTPases with protein prenyltransferase inhibitors prevents leukocyte recruitment to the central nervous system and attenuates clinical signs of disease in an animal model of multiple sclerosis. J. Immunol. 168, 4087-4094 (2002).
16. Greenwood, J., Steinman, L. & Zamvil, S.S. Statin therapy and autoimmune disease: From protein prenylation to immunomodulation. Nat. Rev. Immunol. 6, 358-370 (2006).
17. Hordijk, P.L. Endothelial signalling events during leukocyte transmigration. FEBS J. 273, 4408-4415 (2006).
18. Weiner, J.A. et al. Axon fasciculation defects and retinal dysiplasias in mice lacking the immunoglobulin superfamily adhesion molecule BEN/ALCAM/SCI. Mol. Cell. Neurosci. 27, 59-69 (2004).
19. Swart, G.W. Activated leukocyte cell adhesion molecule (CD166/ALCAM): developmental and mechanistic aspects of cell clustering and cell migration. Eur. J. Cell Biol. 81, 313-321 (2002).
20. Bowen, M.A. et al. Cloning, mapping, and characterization of activated leukocyte-cell adhesion molecule (ALCAM), a CD6 ligand. J. Exp. Med. 181, 2213-2220 (1995).
21. Gimferrer, I. et al. Relevance of CD6-mediated interactions in T cell activation and proliferation. J. Immunol. 173, 2262-2270 (2004).
22. Zimmerman, A.W. et al. Long-term engagement of CD6 and ALCAM is essential for T-cell proliferation induced by dendritic cells. Blood 107, 3212-3220 (2006).
23. van Kempen, L.C. et al. Molecular basis for the homophilic activated leukocyte cell adhesion molecule (ALCAM)-ALCAM interaction. J. Biol. Chem. 276, 25783-25790 (2001).
24. Masedunskas, A. et al. Activated leukocyte cell adhesion molecule is a component of the endothelial junction involved in transendothelial monocyte migration. FEBS Lett. 580, 2637-2645 (2006).
25. + regulatory T cell infiltration of human pancreatic carcinoma. J. Natl. Cancer Inst. 99, 1188-1199 (2007).
26. Manes, S. & Viola, A. Lipid rafts in lymphocyte activation and migration. Mol. Membr. Biol. 23, 59-69 (2006).
27. Amos, C. et al. Cross-linking of brain endothelial intercellular adhesion molecule (ICAM)-1 induces association of ICAM-1 with detergent-insoluble cytoskeletal fraction. Arterioscler. Thromb. Vasc. Biol. 21, 810-816 (2001).
28. Wosik, K. et al. Angiotensin II controls occludin function and is required for blood brain barrier maintenance: Relevance to multiple sclerosis. J. Neurosci. 27, 9032-9042 (2007).
29. Milian, J. et al. Lymphocyte transcellular migration occurs through recruitment of endotheliai ICAM-1 to caveola- and F-actin-rich domains. Nat. Cell Biol. 8, 113-123 (2006).
30. Luster, A.D., Alon, R. & von Andrian, U.H. Immune cell migration in inflammation: Present and future therapeutic targets. Nat. Immunol. 6, 1182-1190 (2005).
31. Lucchinetti, C.F, Brueck, W., Rodriguez, M. & Lassmann, H. Multiple sclerosis: Lessons from neuropathology. Semin. Neurol. 18, 337-349 (1998).
32. Virgintino, D. et al. Expression of caveolin-1 in human brain microvessels. Neuroscience 115, 145-152 (2002).
33. Biernacki, K., Prat, A., Blain, M. & Antel, J.P. Regulation of Th1 and Th2 lymphocyte migration by human adult brain endothellal cells. J. Neuropathol. Exp. Neurol. 60, 1127-1136 (2001).
34. Greenwood, J. et al. Intracellular domain of brain enfothelial intercellular adhesion molecule-1 is essential for T lymphocyte-mediated signaling and migration. J. Immunol. 171, 2099-2108 (2003).
35. Laschinger, M. & Engelhardt, B. Interaction of alpha4-integrin with VCAM-1 is involved in adhesion of encephalitogenic T cell blasts to brain endothelium but not in their transendothelial migration in vitro. J. Neuroimmunol. 102, 32-43 (2000).
36. Shang, X.Z., Lang, B.J. & Issekutz, A.C. Adhesion molecule mechanisms mediating monocyte migration through synovial fibroblast and endothelium barriers: Role for CD11/CD18, very late antigen-4 (CD49(VCD29), very late antigen-5 (CD49e/CD29), and vascular cell adhesion molecule-1 (CD106). J. Immunol. 160, 467-474 (1998).
37. Seguin, R., Biernacki, K., Rotondo, R.L., Prat, A. & Antel, J.P. Regulation and functional effects of monocyte migration across human brain-derived endothelial cells. J. Neuropathol. Exp. Neurol. 62, 412-419 (2003).
38. Zimmerman, A.W. et al. Cytoskeletal restraints regulate homotypic ALCAM-mediated adhesion through PKCalpha independently of Rho-like GTPases. J. Cell Sci. 117, 2841-2852 (2004).
39. Tomita, K., van Bolkhoven, A., Jansen, C.F., Bussemakers, M.J. & Schalken, J A. Coordinate recruitment of E-cadherin and ALCAM to cell-cell contacts by α-catenin. Biochem. Biophys. Res. Commun. 267, 870-874 (2000).
40. Uhlenbrock, K. et al. The RacGEF Tiam1 inhibits migration and invasion of metastatic melanoma via a novel adhesive mechanism. J. Cell Sci. 117, 4863-4871 (2004).
41. Kiely, J.M., Hu, Y., Garcia-Cardena, G. & Gimbrone, M.A., Jr. Lipid raft localization of cell surface E-selectin is required for ligation-induced activation of phospholipase Cγ. J. Immunol. 171, 3216-3224 (2003).
42. Steinman, L. Blocking adhesion molecules as therapy for multiple sclerosis: Natalizumab. Nat. Rev. Drug Discov. 4, 510-518 (2005).
43. Langer-Gould, A., Atlas, S.W., Green, A.J., Batten, A.W. & Pelletier, D. Progressive multifocal leukoenocephalopathy in a patient treated with natalizumab. N. Engl. J. Med. 353, 375-381 (2005).
44. Prat, A., Biernacki, K., Becher, B. & Antel, J.P. B7 expression and antigen presentation by human -brain endothelial cells: Requirement for proinflammatory cytokines. J. Neuropathol. Exp. Neurol. 59, 129-136 (2000).
45. Prat, A. et al. Kinin B1 receptor expression and function on human brain endothelial cells. J. Neuropathol. Exp. Neurol. 59, 896-906 (2000).
46. Nusrat, A. et al. Tight junctions are membrane microdomains. J. Cell Sci. 113, 1771-1781 (2000).
47. Kalyvas, A. & David, S. Cytosolic phospholipase A2 plays a key role in the pathogenesis of multiple sclerosis-like disease. Neuron 41 323-335 (2004).