Modeling immune functions of the mouse blood–cerebrospinal fluid barrier in vitro: primary rather than immortalized mouse choroid plexus epithelial cells are suited to study immune cell migration across this brain barrier
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  • 作者:Ivana Lazarevic ; Britta Engelhardt
  • 关键词:Blood cerebrospinal fluid barrier ; Choroid plexus ; Immortomouse® ; ECPC4
  • 刊名:Fluids and Barriers of the CNS
  • 出版年:2015
  • 出版时间:December 2015
  • 年:2015
  • 卷:13
  • 期:1
  • 全文大小:3,059 KB
  • 参考文献:1.Strazielle N, Ghersi-Egea JF. Choroid plexus in the central nervous system: biology and physiopathology. J Neuropathol Exp Neurol. 2000;59:561–74.CrossRef PubMed
    2.Wolburg H, Paulus W. Choroid plexus: biology and pathology. Acta Neuropathol. 2010;119:75–88.CrossRef PubMed
    3.Engelhardt B, Wolburg-Buchholz K, Wolburg H. Involvement of the choroid plexus in central nervous system inflammation. Microsc Res Tech. 2001;52:112–29.CrossRef PubMed
    4.Tietz S, Engelhardt B. Brain barriers: crosstalk between complex tight junctions and adherens junctions. J Cell Biol. 2015;209:493–506.CrossRef PubMedCentral PubMed
    5.Vorbrodt AW, Dobrogowska DH. Molecular anatomy of intercellular junctions in brain endothelial and epithelial barriers: electron microscopist’s view. Brain Res Brain Res Rev. 2003;42:221–42.CrossRef PubMed
    6.Lippoldt A, Jansson A, Kniesel U, Andbjer B, Andersson A, Wolburg H, et al. Phorbol ester induced changes in tight and adherens junctions in the choroid plexus epithelium and in the ependyma. Brain Res. 2000;854:197–206.CrossRef PubMed
    7.Steffen BJ, Breier G, Butcher EC, Schulz M, Engelhardt B. ICAM-1, VCAM-1, and MAdCAM-1 are expressed on choroid plexus epithelium but not endothelium and mediate binding of lymphocytes in vitro. Am J Pathol. 1996;148:1819–38.PubMedCentral PubMed
    8.Kunis G, Baruch K, Rosenzweig N, Kertser A, Miller O, Berkutzki T, et al. IFN-gamma-dependent activation of the brain’s choroid plexus for CNS immune surveillance and repair. Brain. 2013;136:3427–40.CrossRef PubMed
    9.Engelhardt B, Ransohoff RM. Capture, crawl, cross: the T cell code to breach the blood–brain barriers. Trends Immunol. 2012;33:579–89.CrossRef PubMed
    10.Shechter R, Miller O, Yovel G, Rosenzweig N, London A, Ruckh J, et al. Recruitment of beneficial M2 macrophages to injured spinal cord is orchestrated by remote brain choroid plexus. Immunity. 2013;38:555–69.CrossRef PubMedCentral PubMed
    11.Reboldi A, Coisne C, Baumjohann D, Benvenuto F, Bottinelli D, Lira S, et al. 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. 2009;10:514–23.CrossRef PubMed
    12.Szmydynger-Chodobska J, Strazielle N, Zink BJ, Ghersi-Egea JF, Chodobski A. The role of the choroid plexus in neutrophil invasion after traumatic brain injury. J Cereb Blood Flow Metab. 2009;29:1503–16.CrossRef PubMedCentral PubMed
    13.Steinmann U, Borkowski J, Wolburg H, Schroppel B, Findeisen P, Weiss C, et al. Transmigration of polymorphnuclear neutrophils and monocytes through the human blood–cerebrospinal fluid barrier after bacterial infection in vitro. J Neuroinflammation. 2013;10:31.CrossRef PubMedCentral PubMed
    14.Crook RB, Kasagami H, Prusiner SB. Culture and characterization of epithelial cells from bovine choroid plexus. J Neurochem. 1981;37:845–54.CrossRef PubMed
    15.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;52:137–52.CrossRef PubMed
    16.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;74:68–78.PubMed
    17.Holm NR, Hansen LB, Nilsson C, Gammeltoft S. Gene expression and secretion of insulin-like growth factor-II and insulin-like growth factor binding protein-2 from cultured sheep choroid plexus epithelial cells. Brain Res Mol Brain Res. 1994;21:67–74.CrossRef PubMed
    18.Ramanathan VK, Hui AC, Brett CM, Giacomini KM. Primary cell culture of the rabbit choroid plexus: an experimental system to investigate membrane transport. Pharm Res. 1996;13:952–6.CrossRef PubMed
    19.Zheng W, Zhao Q, Graziano JH. Primary culture of choroidal epithelial cells: characterization of an in vitro model of blood–CSF barrier. In Vitro Cell Dev Biol Anim. 1998;34:40–5.CrossRef PubMed
    20.Strazielle N, Ghersi-Egea JF. Demonstration of a coupled metabolism-efflux process at the choroid plexus as a mechanism of brain protection toward xenobiotics. J Neurosci. 1999;19:6275–89.PubMed
    21.Kitazawa T, Hosoya K, Watanabe M, Takashima T, Ohtsuki S, Takanaga H, et al. 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;18:16–22.CrossRef PubMed
    22.Zheng W, Zhao Q. Establishment and characterization of an immortalized Z310 choroidal epithelial cell line from murine choroid plexus. Brain Res. 2002;958:371–80.CrossRef PubMedCentral PubMed
    23.Shi LZ, Li GJ, Wang S, Zheng W. Use of Z310 cells as an in vitro blood–cerebrospinal fluid barrier model: tight junction proteins and transport properties. Toxicol In Vitro. 2008;22:190–9.CrossRef PubMedCentral PubMed
    24.Monnot AD, Zheng W. Culture of choroid plexus epithelial cells and in vitro model of blood–CSF barrier. Methods Mol Biol. 2013;945:13–29.CrossRef PubMedCentral PubMed
    25.Ishiwata I, Ishiwata C, Ishiwata E, Sato Y, Kiguchi K, Tachibana T, et al. Establishment and characterization of a human malignant choroids plexus papilloma cell line (HIBCPP). Hum Cell. 2005;18:67–72.CrossRef PubMed
    26.Nakashima N, Goto K, Tsukidate K, Sobue M, Toida M, Takeuchi J. Choroid plexus papilloma. Light and electron microscopic study. Virchows Arch A Pathol Anat Histopathol. 1983;400:201–11.CrossRef PubMed
    27.Takahashi K, Satoh F, Hara E, Murakami O, Kumabe T, Tominaga T, et al. Production and secretion of adrenomedullin by cultured choroid plexus carcinoma cells. J Neurochem. 1997;68:726–31.CrossRef PubMed
    28.Peraldi-Roux S, Dao BN-T, Hirn M, Gabrion J. Choroidal ependymocytes in culture: expression of markers of polarity and function. Int J Dev Neurosci. 1990;8:575–88.CrossRef PubMed
    29.Gabrion JB, Herbute S, Bouille C, Maurel D, Kuchler-Bopp S, Laabich A, et al. Ependymal and choroidal cells in culture: characterization and functional differentiation. Microsc Res Tech. 1998;41:124–57.CrossRef PubMed
    30.Menheniott TR, Charalambous M, Ward A. Derivation of primary choroid plexus epithelial cells from the mouse. Methods Mol Biol. 2010;633:207–20.CrossRef PubMed
    31.Barkho BZ, Monuki ES. Proliferation of cultured mouse choroid plexus epithelial cells. PLoS ONE. 2015;10:e0121738.CrossRef PubMedCentral PubMed
    32.Whitehead RH, Robinson PS. Establishment of conditionally immortalized epithelial cell lines from the intestinal tissue of adult normal and transgenic mice. Am J Physiol Gastrointest Liver Physiol. 2009;296:G455–60.CrossRef PubMedCentral PubMed
    33.Kohn EA, Du Z, Sato M, Van Schyndle CM, Welsh MA, Yang YA, et al. A novel approach for the generation of genetically modified mammary epithelial cell cultures yields new insights into TGFbeta signaling in the mammary gland. BCR. 2010;12:R83.CrossRef PubMedCentral PubMed
    34.Enjoji M, Iwaki T, Hara H, Sakai H, Nawata H, Watanabe T. Establishment and characterization of choroid plexus carcinoma cell lines: connection between choroid plexus and immune systems. Jpn J Cancer Res. 1996;87:893–9.CrossRef PubMed
    35.Spector R. Pharmacokinetics and metabolism of cytosine arabinoside in the central nervous system. J Pharmacol Exp Ther. 1982;222:1–6.PubMed
    36.Jat PS, Noble MD, Ataliotis P, Tanaka Y, Yannoutsos N, Larsen L, et al. Direct derivation of conditionally immortal cell lines from an H-2 Kb-tsA58 transgenic mouse. Proc Natl Acad Sci USA. 1991;88:5096–100.CrossRef PubMedCentral PubMed
    37.Tenenbaum T, Papandreou T, Gellrich D, Friedrichs U, Seibt A, Adam R, et al. Polar bacterial invasion and translocation of Streptococcus suis across the blood–cerebrospinal fluid barrier in vitro. Cell Microbiol. 2009;11:323–36.CrossRef PubMed
    38.Steiner O, Coisne C, Cecchelli R, Boscacci R, Deutsch U, Engelhardt B, et al. Differential roles for endothelial ICAM-1, ICAM-2, and VCAM-1 in shear-resistant T cell arrest, polarization, and directed crawling on blood–brain barrier endothelium. J Immunol. 2010;185:4846–55.CrossRef PubMed
    39.Coisne C, Dehouck L, Faveeuw C, Delplace Y, Miller F, Landry C, et al. Mouse syngenic in vitro blood–brain barrier model: a new tool to examine inflammatory events in cerebral endothelium. Lab Invest. 2005;85:734–46.CrossRef PubMed
    40.Cecchelli R, Aday S, Sevin E, Almeida C, Culot M, Dehouck L, et al. A stable and reproducible human blood–brain barrier model derived from hematopoietic stem cells. PLoS ONE. 2014;9:e99733.CrossRef PubMedCentral PubMed
    41.Abadier M, Haghayegh Jahromi N, Cardoso Alves L, Boscacci R, Vestweber D, Barnum S, et al. Cell surface levels of endothelial ICAM-1 influence the transcellular or paracellular T-cell diapedesis across the blood–brain barrier. Eur J Immunol. 2015;45:1043–58.CrossRef PubMed
    42.Lo CM, Keese CR, Giaever I. Cell-substrate contact: another factor may influence transepithelial electrical resistance of cell layers cultured on permeable filters. Exp Cell Res. 1999;250:576–80.CrossRef PubMed
    43.Murugesan N, Paul D, Lemire Y, Shrestha B, Ge S, Pachter JS. Active induction of experimental autoimmune encephalomyelitis by MOG35-55 peptide immunization is associated with differential responses in separate compartments of the choroid plexus. Fluids Barriers CNS. 2012;9:15.CrossRef PubMedCentral PubMed
    44.Marques F, Mesquita SD, Sousa JC, Coppola G, Gao F, Geschwind DH, et al. Lipocalin 2 is present in the EAE brain and is modulated by natalizumab. Front Cell Neurosci. 2012;6:33.CrossRef PubMedCentral PubMed
    45.Schwerk C, Tenenbaum T, Kim KS, Schroten H. The choroid plexus-a multi-role player during infectious diseases of the CNS. Front Cell Neurosci. 2015;9:80.CrossRef PubMedCentral PubMed
    46.Wagner EF, Risau W. Oncogenes in the study of endothelial cell growth and differentiation. Semin Cancer Biol. 1994;5:137–45.PubMed
    47.Weksler B, Romero IA, Couraud PO. The hCMEC/D3 cell line as a model of the human blood brain barrier. Fluids Barriers CNS. 2013;10:16.CrossRef PubMedCentral PubMed
    48.Klas J, Wolburg H, Terasaki T, Fricker G, Reichel V. Characterization of immortalized choroid plexus epithelial cell lines for studies of transport processes across the blood–cerebrospinal fluid barrier. Cerebrospinal Fluid Res. 2010;7:11.CrossRef PubMedCentral PubMed
    49.Szmydynger-Chodobska J, Pascale CL, Pfeffer AN, Coulter C, Chodobski A. Expression of junctional proteins in choroid plexus epithelial cell lines: a comparative study. Cerebrospinal Fluid Res. 2007;4:11.CrossRef PubMedCentral PubMed
    50.Schwerk C, Papandreou T, Schuhmann D, Nickol L, Borkowski J, Steinmann U, et al. 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:e30069.CrossRef PubMedCentral PubMed
    51.Resnick A. Chronic fluid flow is an environmental modifier of renal epithelial function. PLoS ONE. 2011;6:e27058.CrossRef PubMedCentral PubMed
    52.May T, Wirth D, Hauser H, Mueller PP. Transcriptionally regulated immortalization overcomes side effects of temperature-sensitive SV40 large T antigen. Biochem Biophys Res Commun. 2005;327:734–41.CrossRef PubMed
    53.Takano M, Satoh C, Kunimatsu N, Otani M, Hamada-Kanazawa M, Miyake M, et al. Lipopolysaccharide activates the kallikrein-kinin system in mouse choroid plexus cell line ECPC4. Neurosci Lett. 2008;434:310–4.CrossRef PubMed
    54.Takano M, Ohkusa M, Otani M, Min KS, Kadoyama K, Minami K, et al. Lipid A-activated inducible nitric oxide synthase expression via nuclear factor-kappaB in mouse choroid plexus cells. Immunol Lett. 2015;167:57–62.CrossRef PubMed
    55.Southwell BR, Duan W, Alcorn D, Brack C, Richardson SJ, Kohrle J, et al. Thyroxine transport to the brain: role of protein synthesis by the choroid plexus. Endocrinology. 1993;133:2116–26.PubMed
    56.Shu C, Shen H, Teuscher NS, Lorenzi PJ, Keep RF, Smith DE. Role of PEPT2 in peptide/mimetic trafficking at the blood–cerebrospinal fluid barrier: studies in rat choroid plexus epithelial cells in primary culture. J Pharmacol Exp Ther. 2002;301:820–9.CrossRef PubMed
    57.Welch K, Araki H. Features of the choroid plexus of the cat, studied in vitro. In: Cserr HR, Fenstermacher JD, editors. Fluid Environment of the Brain. New York: Academic Press Inc; 1975. p. 157–65.
    58.Strazielle N, Belin MF, Ghersi-Egea JF. Choroid plexus controls brain availability of anti-HIV nucleoside analogs via pharmacologically inhibitable organic anion transporters. AIDS. 2003;17:1473–85.CrossRef PubMed
    59.Staat C, Coisne C, Dabrowski S, Stamatovic SM, Andjelkovic AV, Wolburg H, et al. Mode of action of claudin peptidomimetics in the transient opening of cellular tight junction barriers. Biomaterials. 2015;54:9–20.CrossRef PubMed
    60.Steiner O, Coisne C, Engelhardt B, Lyck R. Comparison of immortalized bEnd5 and primary mouse brain microvascular endothelial cells as in vitro blood–brain barrier models for the study of T cell extravasation. J Cereb Blood Flow Metab. 2011;31:315–27.CrossRef PubMedCentral PubMed
  • 作者单位:Ivana Lazarevic (1)
    Britta Engelhardt (1)

    1. Theodor Kocher Institute, University of Bern, Freiestrasse 1, 3012, Bern, Switzerland
  • 刊物主题:Neurosciences; Neurology;
  • 出版者:BioMed Central
  • ISSN:2045-8118
文摘
Background The blood–cerebrospinal fluid barrier (BCSFB) established by the choroid plexus (CP) epithelium has been recognized as a potential entry site of immune cells into the central nervous system during immunosurveillance and neuroinflammation. The location of the choroid plexus impedes in vivo analysis of immune cell trafficking across the BCSFB. Thus, research on cellular and molecular mechanisms of immune cell migration across the BCSFB is largely limited to in vitro models. In addition to forming contact-inhibited epithelial monolayers that express adhesion molecules, the optimal in vitro model must establish a tight permeability barrier as this influences immune cell diapedesis.

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