Culture models to study leukocyte trafficking across the choroid plexus

Springer Science and Business Media LLC - Tập 10 - Trang 1-9 - 2013
Tobias Tenenbaum1, Ulrike Steinmann1, Corinna Friedrich2, Jürgen Berger3, Christian Schwerk1, Horst Schroten1
1Paediatric Infectious Diseases, Department of Pediatric and Adolescent Medicine, Universitätsmedizin Mannheim,Medical Faculty Mannheim,Heidelberg University, Mannheim, Germany
2Department für Kardiologie und Angiologie, Institut für Genetik von Herzerkrankungen (IfGH),Universitätsklinikum Münster, Münster, Germany
3Max Planck Institute of Developmental Biology, Tuebingen, Germany

Tóm tắt

A critical point during the course of central nervous system infection is the influx of leukocytes from the blood into the brain across the blood-brain barrier (BBB) and the blood-cerebrospinal fluid barrier (BCSFB). However, experimental in vitro models to investigate leukocyte transmigration across cultured choroid plexus epithelial cells have been lacking so far. We have developed a porcine and human “inverted” culture insert system that enables leukocyte transmigration specifically from the physiologically relevant basolateral side. The models use primary porcine choroid plexus epithelial cells (PCPEC) and human choroid plexus papilloma cells (HIBCPP). As a prerequisite for a functional barrier, we optimized culture conditions in which cells are maintained in serum-containing medium until high barrier function is reached. Leukocyte transmigration through the plexus epithelial cells is analysed by three-dimensional Apotome®-imaging and electron microscopy, and the route of transmigration through the plexus epithelial cells, i.e. transcellular as well as paracellular, can be determined. As a functionally relevant porcine and human BCSFB model, PCPEC and HIBCPP respectively, offer a wide range of options for analysis of disease-related mechanisms at the choroid plexus epithelium, especially involving human pathogens. Moreover, our in vitro models facilitate the investigation of leukocyte entry into the CNS via the blood-CSF barrier.

Tài liệu tham khảo

Balda MS, Matter K: Tight junctions. J Cell Sci. 1998, 111 (Pt 5): 541-547. Strazielle N, Ghersi-Egea JF: Choroid plexus in the central nervous system: biology and physiopathology. J Neuropathol Exp Neurol. 2000, 59 (7): 561-574. Engelhardt B, Wolburg-Buchholz K, Wolburg H: Involvement of the choroid plexus in central nervous system inflammation. Microsc Res Tech. 2001, 52 (1): 112-129. 10.1002/1097-0029(20010101)52:1<112::AID-JEMT13>3.0.CO;2-5. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ: Structure and function of the blood-brain barrier. Neurobiol Dis. 2010, 37 (1): 13-25. 10.1016/j.nbd.2009.07.030. Haselbach M, Wegener J, Decker S, Engelbertz C, Galla HJ: Porcine Choroid plexus epithelial cells in culture: regulation of barrier properties and transport processes. Microsc Res Tech. 2001, 52 (1): 137-152. 10.1002/1097-0029(20010101)52:1<137::AID-JEMT15>3.0.CO;2-J. Tenenbaum T, Matalon D, Adam R, Seibt A, Wewer C, Schwerk C, Galla HJ, Schroten H: Dexamethasone prevents alteration of tight junction-associated proteins and barrier function in porcine choroid plexus epithelial cells after infection with Streptococcus suis in vitro. Brain Res. 2008, 1229: 1-17. Tenenbaum T, Papandreou T, Gellrich D, Friedrichs U, Seibt A, Adam R, Wewer C, Galla HJ, Schwerk C, Schroten H: Polar bacterial invasion and translocation of Streptococcus suis across the blood-cerebrospinal fluid barrier in vitro. Cell Microbiol. 2009, 11 (2): 323-336. 10.1111/j.1462-5822.2008.01255.x. Pron B, Taha MK, Rambaud C, Fournet JC, Pattey N, Monnet JP, Musilek M, Beretti JL, Nassif X: Interaction of Neisseria maningitidis with the components of the blood-brain barrier correlates with an increased expression of PilC. J Infect Dis. 1997, 176 (5): 1285-1292. 10.1086/514124. Smith AL: Pathogenesis of Haemophilus influenzae meningitis. Pediatr Infect Dis J. 1987, 6 (8): 783-786. 10.1097/00006454-198708000-00037. Parkkinen J, Korhonen TK, Pere A, Hacker J, Soinila S: Binding sites in the rat brain for Escherichia coli S fimbriae associated with neonatal meningitis. J Clin Invest. 1988, 81 (3): 860-865. 10.1172/JCI113395. Prats N, Briones V, Blanco MM, Altimira J, Ramos JA, Dominguez L, Marco A: Choroiditis and meningitis in experimental murine infection with Listeria monocytogenes. Eur J Clin Microbiol Infect Dis. 1992, 11 (8): 744-747. 10.1007/BF01989983. Sanford SE: Gross and histopathological findings in unusual lesions caused by Streptococcus suis in pigs. II. Central nervous system lesions. Can J Vet Res. 1987, 51 (4): 486-489. Tabor-Godwin JM, Ruller CM, Bagalso N, An N, Pagarigan RR, Harkins S, Gilbert PE, Kiosses WB, Gude NA, Cornell CT: A novel population of myeloid cells responding to coxsackievirus infection assists in the dissemination of virus within the neonatal CNS. J Neurosci. 2010, 30 (25): 8676-8691. 10.1523/JNEUROSCI.1860-10.2010. Zhang JR, Tuomanen E: Molecular and cellular mechanisms for microbial entry into the CNS. J Neurovirol. 1999, 5 (6): 591-603. 10.3109/13550289909021288. Kim KS: Pathogenesis of bacterial meningitis: from bacteraemia to neuronal injury. Nat Rev Neurosci. 2003, 4 (5): 376-385. 10.1038/nrn1103. Wolburg H, Paulus W: Choroid plexus: biology and pathology. Acta Neuropathol. 2010, 119 (1): 75-88. 10.1007/s00401-009-0627-8. Stins MF, Badger J, Sik Kim K: Bacterial invasion and transcytosis in transfected human brain microvascular endothelial cells. Microb Pathog. 2001, 30 (1): 19-28. 10.1006/mpat.2000.0406. Weksler BB, Subileau EA, Perriere N, Charneau P, Holloway K, Leveque M, Tricoire-Leignel H, Nicotra A, Bourdoulous S, Turowski P: Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J. 2005, 19 (13): 1872-1874. Muruganandam A, Herx LM, Monette R, Durkin JP, Stanimirovic DB: Development of immortalized human cerebromicrovascular endothelial cell line as an in vitro model of the human blood-brain barrier. FASEB J. 1997, 11 (13): 1187-1197. Shi LZ, Zheng W: Establishment of an in vitro brain barrier epithelial transport system for pharmacological and toxicological study. Brain Res. 2005, 1057 (1–2): 37-48. Gath U, Hakvoort A, Wegener J, Decker S, Galla HJ: Porcine choroid plexus cells in culture: expression of polarized phenotype, maintenance of barrier properties and apical secretion of CSF-components. Eur J Cell Biol. 1997, 74 (1): 68-78. Kitazawa T, Hosoya K, Watanabe M, Takashima T, Ohtsuki S, Takanaga H, Ueda M, Yanai N, Obinata M, Terasaki T: Characterization of the amino acid transport of new immortalized choroid plexus epithelial cell lines: a novel in vitro system for investigating transport functions at the blood-cerebrospinal fluid barrier. Pharm Res. 2001, 18 (1): 16-22. 10.1023/A:1011014424212. Zheng W, Zhao Q: Establishment and characterization of an immortalized Z310 choroidal epithelial cell line from murine choroid plexus. Brain Res. 2002, 958 (2): 371-380. 10.1016/S0006-8993(02)03683-1. Strazielle N, Ghersi-Egea JF: In vitro models of the blood-cerebrospinal fluid barrier and their use in neurotoxicological research. NeuroMethods. 2011, 56: 161-184. 10.1007/978-1-61779-077-5_8. Staats JJ, Plattner BL, Stewart GC, Changappa MM: Presence of the Streptococcus suis suilysin gene and expression of MRP and EF correlates with high virulence in Streptococcus suis type 2 isolates. Vet Microbiol. 1999, 70 (3–4): 201-211. Ishiwata I, Ishiwata C, Ishiwata E, Sato Y, Kiguchi K, Tachibana T, Hashimoto H, Ishikawa H: Establishment and characterization of a human malignant choroids plexus papilloma cell line (HIBCPP). Hum Cell. 2005, 18 (1): 67-72. Schwerk C, Papandreou T, Schuhmann D, Nickol L, Borkowski J, Steinmann U, Quednau N, Stump C, Weiss C, Berger J: Polar invasion and translocation of Neisseria meningitidis and Streptococcus suis in a novel human model of the blood-cerebrospinal fluid barrier. PLoS One. 2012, 7 (1): e30069-10.1371/journal.pone.0030069. Chin AC, Parkos CA: Pathobiology of neutrophil transepithelial migration: implications in mediating epithelial injury. Annu Rev Pathol. 2007, 2: 111-143. 10.1146/annurev.pathol.2.010506.091944. Parkos CA, Delp C, Arnaout MA, Madara JL: Neutrophil migration across a cultured intestinal epithelium. Dependence on a CD11b/CD18-mediated event and enhanced efficiency in physiological direction. J Clin Invest. 1991, 88 (5): 1605-1612. 10.1172/JCI115473. Parkos CA, Colgan SP, Delp C, Arnaout MA, Madara JL: Neutrophil migration across a cultured epithelial monolayer elicits a biphasic resistance response representing sequential effects on transcellular and paracellular pathways. J Cell Biol. 1992, 117 (4): 757-764. 10.1083/jcb.117.4.757. Madara JL, Parkos C, Colgan S, Nusrat A, Atisook K, Kaoutzani P: The movement of solutes and cells across tight junctions. Ann N Y Acad Sci. 1992, 664: 47-60. 10.1111/j.1749-6632.1992.tb39748.x. Blake KM, Carrigan SO, Issekutz AC, Stadnyk AW: Neutrophils migrate across intestinal epithelium using beta2 integrin (CD11b/CD18)-independent mechanisms. Clin Exp Immunol. 2004, 136 (2): 262-268. 10.1111/j.1365-2249.2004.02429.x. Schroten M, Hanisch FG, Quednau N, Stump C, Riebe R, Lenk M, Wolburg H, Tenenbaum T, Schwerk C: A novel porcine in vitro model of the blood-cerebrospinal fluid barrier with strong barrier function. PLoS One. 2012, 7 (6): e39835-10.1371/journal.pone.0039835. Zemans RL, Colgan SP, Downey GP: Transepithelial migration of neutrophils: mechanisms and implications for acute lung injury. Am J Respir Cell Mol Biol. 2009, 40 (5): 519-535. 10.1165/rcmb.2008-0348TR. Wong D, Prameya R, Dorovini-Zis K: Adhesion and migration of polymorphonuclear leukocytes across human brain microvessel endothelial cells are differentially regulated by endothelial cell adhesion molecules and modulate monolayer permeability. J Neuroimmunol. 2007, 184 (1–2): 136-148. Wewer C, Seibt A, Wolburg H, Greune L, Schmidt MA, Berger J, Galla HJ, Quitsch U, Schwerk C, Schroten H: Transcellular migration of neutrophil granulocytes through the blood-cerebrospinal fluid barrier after infection with Streptococcus suis. J Neuroinflammation. 2011, 8 (1): 51-10.1186/1742-2094-8-51. Ransohoff RM, Kivisakk P, Kidd G: Three or more routes for leukocyte migration into the central nervous system. Nat Rev Immunol. 2003, 3 (7): 569-581. 10.1038/nri1130. Engelhardt B, Wolburg H: Mini-review: transendothelial migration of leukocytes: through the front door or around the side of the house?. Eur J Immunol. 2004, 34 (11): 2955-2963. 10.1002/eji.200425327. Schneider HWC, Schoeller J, Steinmann U, Borkowski J, Ishikawa H, Findeisen P, Adams O, Doerries R, Schwerk C, Schroten H, Tenenbaum T: Chemotaxis of T-cells after infection of human choroid plexus papilloma cells with echovirus 30 in an in vitro model of the blood-cerebrospinal fluid barrier. Virus Res. 2012, 170 (1-2): 66-74. 10.1016/j.virusres.2012.08.019. Liu L, Mul FP, Kuijpers TW, Lutter R, Roos D, Knol EF: Neutrophil transmigration across monolayers of endothelial cells and airway epithelial cells is regulated by different mechanisms. Ann N Y Acad Sci. 1996, 796: 21-29. 10.1111/j.1749-6632.1996.tb32563.x. Zeillemaker AM, Mul FP, van Papendrecht AA H, Leguit P, Verbrugh HA, Roos D: Neutrophil adherence to and migration across monolayers of human peritoneal mesothelial cells. The role of mesothelium in the influx of neutrophils during peritonitis. J Lab Clin Med. 1996, 127 (3): 279-286. 10.1016/S0022-2143(96)90096-7. Hurley BP, Siccardi D, Mrsny RJ, McCormick BA: Polymorphonuclear cell transmigration induced by Pseudomonas aeruginosa requires the eicosanoid hepoxilin A3. J Immunol. 2004, 173 (9): 5712-5720. McCormick BA, Hofman PM, Kim J, Carnes DK, Miller SI, Madara JL: Surface attachment of Salmonella typhimurium to intestinal epithelia imprints the subepithelial matrix with gradients chemotactic for neutrophils. J Cell Biol. 1995, 131 (6 Pt 1): 1599-1608. Mul FP, Zuurbier AE, Janssen H, Calafat J, van Wetering S, Hiemstra PS, Roos D, Hordijk PL: Sequential migration of neutrophils across monolayers of endothelial and epithelial cells. J Leukoc Biol. 2000, 68 (4): 529-537.