Comparison of immortalized bEnd5 and primary mouse brain microvascular endothelial cells as in vitro blood-κBrain barrier models for the study of T cell extravasation

Journal of Cerebral Blood Flow and Metabolism

Volumn 31, Issue 1, 2011, Pages 315-327

  Steiner, Oliver ^a   Coisne, Caroline ^a   Engelhardt, Britta ^a   Lyck, Ruth ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

in vitro BBB model; live cell imaging; physiologic shear flow; T cell adhesion; T cell crawling; T cell diapedesis

Indexed keywords

F ACTIN;

ANIMAL CELL; ARTICLE; BLOOD BRAIN BARRIER; CELL ADHESION; CELL DENSITY; CELL IMMORTALIZATION; CELL JUNCTION; CELL LINE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; CYTOSKELETON; IMMUNOFLUORESCENCE; IN VITRO STUDY; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SHEAR FLOW; SURFACE PROPERTY; T LYMPHOCYTE; TIGHT JUNCTION;

ACTINS; ANIMALS; BLOOD-BRAIN BARRIER; CAPILLARIES; CELL ADHESION; CELL CYCLE; CELL LINE; CELL MEMBRANE PERMEABILITY; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; INTERCELLULAR JUNCTIONS; MALE; MICE; MICE, INBRED C57BL; T-LYMPHOCYTES; TIGHT JUNCTIONS; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 78650912377     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1038/jcbfm.2010.96     Document Type: Article

References (42)

1. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ (2010) Structure and function of the blood-brain barrier. Neurobiol Dis 37:13-25
2. Afonso PV, Ozden S, Prevost MC, Schmitt C, Seilhean D, Weksler B, Couraud PO, Gessain A, Romero IA, Ceccaldi PE (2007) Human blood-brain barrier disruption by retroviral-infected lymphocytes: role of myosin light chain kinase in endothelial tight-junction disorganization. J Immunol 179:2576-83
3. Bahbouhi B, Berthelot L, Pettre S, Michel L, Wiertlewski S, Weksler B, Romero IA, Miller F, Couraud PO, Brouard S, Laplaud DA, Soulillou JP (2009) Peripheral blood CD4+ T lymphocytes from multiple sclerosis patients are characterized by higher PSGL-1 expression and transmigration capacity across a human blood-brain barrierderived endothelial cell line. J Leukoc Biol 86:1049-63
4. Bartholomaus I, Kawakami N, Odoardi F, Schlager C, Miljkovic D, Ellwart JW, Klinkert WE, Flugel-Koch C, Issekutz TB, Wekerle H, Flugel A (2009) Effector T cell interactions with meningeal vascular structures in nascent autoimmune CNS lesions. Nature 462:94-8
5. Bogatcheva NV, Verin AD (2008) The role of cytoskeleton in the regulation of vascular endothelial barrier function. Microvasc Res 76:202-7
6. Carman CV (2009) Mechanisms for transcellular diapedesis: probing and pathfinding by 'invadosome-like protrusions'. J Cell Sci 122:3025-35
7. Carman CV, Sage PT, Sciuto TE, de la Fuente MA, Geha RS, Ochs HD, Dvorak HF, Dvorak AM, Springer TA (2007) Transcellular diapedesis is initiated by invasive podosomes. Immunity 26:784-97
8. Cecchelli R, Dehouck B, Descamps L, Fenart L, Buee-Scherrer V, Duhem C, Lundquist S, Rentfel M, Torpier G, Dehouck MP (1999) In vitro model for evaluating drug transport across the blood-brain barrier. Adv Drug Deliv Rev 36:165-78
9. Cinamon G, Shinder V, Alon R (2001) Shear forces promote lymphocyte migration across vascular endothelium bearing apical chemokines. Nat Immunol 2:515-22
10. Coisne C, Dehouck L, Faveeuw C, Delplace Y, Miller F, Landry C, Morissette C, Fenart L, Cecchelli R, Tremblay P, Dehouck B (2005) Mouse syngenic in vitro bloodbrain barrier model: a new tool to examine inflammatory events in cerebral endothelium. Lab Invest 85: 734-46
11. Coisne C, Faveeuw C, Delplace Y, Dehouck L, Miller F, Cecchelli R, Dehouck B (2006) Differential expression of selectins by mouse brain capillary endothelial cells in vitro in response to distinct inflammatory stimuli. Neurosci Lett 392:216-20
12. Dejana E, Orsenigo F, Molendini C, Baluk P, McDonald DM (2009) Organization and signaling of endothelial cell-tocell junctions in various regions of the blood and lymphatic vascular trees. Cell Tissue Res 335:17-25
13. Deli MA, Abraham CS, Kataoka Y, Niwa M (2005) Permeability studies on in vitro blood-brain barrier models: physiology, pathology, and pharmacology. Cell Mol Neurobiol 25:59-127
14. Engelhardt B (2008) Immune cell entry into the central nervous system: involvement of adhesion molecules and chemokines. J Neurol Sci 274:23-6
15. Engelhardt B, Laschinger M, Schulz M, Samulowitz U, Vestweber D, Hoch G (1998) The development of experimental autoimmune encephalomyelitis in the mouse requires alpha4-integrin but not alpha4beta7-integrin. J Clin Invest 102:2096-105
16. Engelhardt B, Wolburg H (2004) Mini-review: transendothelial migration of leukocytes: through the front door or around the side of the house? Eur J Immunol 34:2955-63
17. Jacobelli J, Bennett FC, Pandurangi P, Tooley AJ, Krummel MF (2009) Myosin-IIA and ICAM-1 regulate the interchange between two distinct modes of T cell migration. J Immunol 182:2041-50
18. Laschinger M, Engelhardt B (2000) 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
19. Lawrence MB, Smith CW, Eskin SG, McIntire LV (1990) Effect of venous shear stress on CD18-mediated neutrophil adhesion to cultured endothelium. Blood 75:227-37
20. Ley K, Laudanna C, Cybulsky MI, Nourshargh S (2007) Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 7: 678-89
21. Lyck R, Reiss Y, Gerwin N, Greenwood J, Adamson P, Engelhardt B (2003) T-cell interaction with ICAM-1/ ICAM-2 double-deficient brain endothelium in vitro: the cytoplasmic tail of endothelial ICAM-1 is necessary for transendothelial migration of T cells. Blood 102:3675-83
22. Lyck R, Ruderisch N, Moll AG, Steiner O, Cohen CD, Engelhardt B, Makrides V, Verrey F (2009) Cultureinduced changes in blood-brain barrier transcriptome: implications for amino-acid transporters in vivo. J Cereb Blood Flow Metab 29:1491-502
23. Man S, Ubogu EE, Williams KA, Tucky B, Callahan MK, Ransohoff RM (2008) Human brain microvascular endothelial cells and umbilical vein endothelial cells differentially facilitate leukocyte recruitment and utilize chemokines for T cell migration. Clin Develop Immunol 2008:384982
24. Martinelli R, Gegg M, Longbottom R, Adamson P, Turowski P, Greenwood J (2009) ICAM-1-mediated endothelial nitric oxide synthase activation via calcium and AMP-activated protein kinase is required for transendothelial lymphocyte migration. Mol Biol Cell 20:995-1005
25. Millan J, Hewlett L, Glyn M, Toomre D, Clark P, Ridley AJ (2006) Lymphocyte transcellular migration occurs through recruitment of endothelial ICAM-1 to caveolaand F-actin-rich domains. Nat Cell Biol 8:113-23
26. Oostingh GJ, Schlickum S, Friedl P, Schon MP (2007) Impaired induction of adhesion molecule expression in immortalized endothelial cells leads to functional defects in dynamic interactions with lymphocytes. J Invest Dermatol 127:2253-8
27. Reiss Y, Engelhardt B (1999) T cell interaction with ICAM-1-deficient endothelium in vitro: transendothelial migration of different T cell populations is mediated by endothelial ICAM-1 and ICAM-2. Int Immunol 11:1527-39
28. Reiss Y, Hoch G, Deutsch U, Engelhardt B (1998) T cell interaction with ICAM-1-deficient endothelium in vitro: essential role for ICAM-1 and ICAM-2 in transendothelial migration of T cells. Eur J Immunol 28:3086-99
29. Rohnelt RK, Hoch G, Reiss Y, Engelhardt B (1997) Immunosurveillance modelled in vitro: naive and memory T cells spontaneously migrate across unstimulated microvascular endothelium. Int Immunol 9: 435-50
30. Schreiber TH, Shinder V, Cain DW, Alon R, Sackstein R (2007) Shear flow-dependent integration of apical and subendothelial chemokines in T-cell transmigration: implications for locomotion and the multistep paradigm. Blood 109:1381-6
31. Schulzke JD, Gitter AH, Mankertz J, Spiegel S, Seidler U, Amasheh S, Saitou M, Tsukita S, Fromm M (2005) Epithelial transport and barrier function in occludin-deficient mice. Biochim Biophys Acta 1669:34-42
32. Shulman Z, Shinder V, Klein E, Grabovsky V, Yeger O, Geron E, Montresor A, Bolomini-Vittori M, Feigelson SW, Kirchhausen T, Laudanna C, Shakhar G, Alon R (2009) Lymphocyte crawling and transendothelial migration require chemokine triggering of high-affinity LFA-1 integrin. Immunity 30:384-96
33. Smith A, Carrasco YR, Stanley P, Kieffer N, Batista FD, Hogg N (2005) A talin-dependent LFA-1 focal zone is formed by rapidly migrating T lymphocytes. J Cell Biol 170:141-51
34. Stanley P, Smith A, McDowall A, Nicol A, Zicha D, Hogg N (2008) Intermediate-affinity LFA-1 binds alpha-actinin-1 to control migration at the leading edge of the T cell. EMBO J 27:62-75
35. Stein JV, Soriano SF, M'Rini C, Nombela-Arrieta C, de Buitrago GG, Rodriguez-Frade JM, Mellado M, Girard JP, Martinez AC (2003) CCR7-mediated physiological lymphocyte homing involves activation of a tyrosine kinase pathway. Blood 101:38-44
36. Taddei A, Giampietro C, Conti A, Orsenigo F, Breviario F, Pirazzoli V, Potente M, Daly C, Dimmeler S, Dejana E (2008) Endothelial adherens junctions control tight junctions by VE-cadherin-mediated upregulation of claudin-5. Nat Cell Biol 10:923-34
37. Turowski P, Adamson P, Greenwood J (2005) Pharmacological targeting of ICAM-1 signaling in brain endothelial cells: potential for treating neuroinflammation. Cell Mol Neurobiol 25:153-70
38. Turowski P, Martinelli R, Crawford R, Wateridge D, Papageorgiou AP, Lampugnani MG, Gamp AC, Vestweber D, Adamson P, Dejana E, Greenwood J (2008) Phosphorylation of vascular endothelial cadherin controls lymphocyte emigration. J Cell Sci 121:29-37
39. Vajkoczy P, Laschinger M, Engelhardt B (2001) Alpha4-integrin-VCAM-1 binding mediates G protein-independent capture of encephalitogenic T cell blasts to CNS white matter microvessels. J Clin Invest 108:557-65
40. Vandenbroucke E, Mehta D, Minshall R, Malik AB (2008) Regulation of endothelial junctional permeability. Ann NY Acad Sci 1123:134-45
41. Vestweber D (2008) VE-cadherin: the major endothelial adhesion molecule controlling cellular junctions and blood vessel formation. Arterioscler Thromb Vasc Biol 28:223-32
42. Yang T, Roder KE, Abbruscato TJ (2007) Evaluation of bEnd5 cell line as an in vitro model for the blood-brain barrier under normal and hypoxic/aglycemic conditions. J Pharm Sci 96:3196-213