NKIM-6, a new immortalized human brain capillary endothelial cell line with conserved endothelial characteristics

Cell and Tissue Research

Volumn 328, Issue 1, 2007, Pages 19-29

  Ketabi Kiyanvash, Nahal ^a   Herold Mende, Christel ^a   Kashfi, Farzaneh ^a   Caldeira, Sandra ^b,c   Tommasino, Massimo ^b,d   Haefeli, Walter E ^a   Weiss, Johanna ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c European Molecular Biology Institute   (Germany)

^d INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

Author keywords

ABC transporters; Blood brain barrier; Brain capillary endothelial cell; Endothelial markers; Human; Tight junctions

Indexed keywords

BIOLOGICAL MARKER;

ARTICLE; BLOOD BRAIN BARRIER; BRAIN CAPILLARY; CELL IMMORTALIZATION; CELL LINE; CELL STRUCTURE; CELL SURVIVAL; ENDOTHELIUM CELL; EPITHELIUM CELL; GENETIC TRANSFECTION; GLIA; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; NERVE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS TYPING;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL MARKERS; BLOOD-BRAIN BARRIER; BRAIN; CELL LINE, TRANSFORMED; CELL PROLIFERATION; DOGS; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; MALE; MIDDLE AGED; PROPIONATES; QUINOLINES; RNA, MESSENGER;

HUMAN PAPILLOMAVIRUS TYPE 16;

EID: 33947180056     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00441-006-0348-4     Document Type: Article

References (56)

1. Albermann N, Schmitz-Winnenthal FH, Z'graggen K, Volk C, Hoffmann MM, Haefeli WE, Weiss J (2005) Expression of the drug transporters MDR1/ABCB1, MRP1/ABCC1, MRP2/ ABCC2, BCRP/ABCG2, and PXR in peripheral blood mononuclear cells and their relationship with the expression in intestine and liver. Biochem Pharmacol 70:949-958
2. Aronica E, Gorter JA, Jansen GH, van Veelen CW, van Rijen PC, Leenstra S, Ramkema M, Scheffer GL, Scheper RJ, Troost D (2003) Expression and cellular distribution of multidrug transporter proteins in two major causes of medically intractable epilepsy: focal cortical dysplasia and glioneuronal tumors. Neuroscience 118:417-429
3. Bauer B, Miller DS, Fricker G (2003) Compound profiling for P-glycoprotein at the blood-brain barrier using a microplate screening system. Pharm Res 20:1170-1176
4. Bauer B, Hartz AM, Fricker G, Miller DS (2004) Pregnane X receptor up-regulation of P-glycoprotein expression and transport function at the blood-brain barrier. Mol Pharmacol 66:413-419
5. Begley DJ, Lechardeur D, Chen ZD, Rollinson C, Bardoul M, Roux F, Scherman D, Abbott NJ (1996) Functional expression of P-glycoprotein in an immortalised cell line of rat brain endothelial cells, RBE4. J Neurochem 67:988-995
6. Caldeira S, Zehbe I, Accardi R, Malanchi I, Dong W, Giarre M, de Villiers EM, Filotico R, Boukamp P, Tommasino M (2003) The E6 and E7 proteins of the cutaneous human papillomavirus type 38 display transforming properties. J Virol 77:2195-2206
7. Cantz T, Nies AT, Brom M, Hofmann AF, Keppler D (2000) MRP2, a human conjugate export pump, is present and transports fluo 3 into apical vacuoles of Hep G2 cells. Am J Physiol Gastrointest Liver Physiol 278:G522-G531
8. Cervos-Navarro J (1963) Elektronenmikroskopischer Befund an den Kapillaren der Hirnrinde. Arch Psychiatr Nervenkr 204:484-504
9. Claude P, Goodenough DA (1973) Fracture faces of zonulae occludentes from "tight" and "leaky" epithelia. J Cell Biol 58:390-400
10. Cordon-Cardo C, O'Brien JP, Casals D, Rittman-Grauer L, Biedler JL, Melamed MR, Bertino JR (1989) Multidrug-resistance gene (P-glycoprotein) is expressed by endothelial cells at blood-brain barrier sites. Proc Natl Acad Sci USA 86:695-698
11. 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
12. Dombrowski SM, Desai SY, Marroni M, Cucullo L, Goodrich K, Bingaman W, Mayberg MR, Bengez L, Janigro D (2001) Overexpression of multiple drug resistance genes in endothelial cells from patients with refractory epilepsy. Epilepsia 42:1501-1506
13. Evers R, Cnubben NHP, Wijnholds J, van Deemter L, van Bladeren PJ, Borst P (1997) Transport of glutathione prostaglandin A conjugates by the multidrug resistance protein 1. FEBS Lett 419:112-116
14. Evers R, Kool M, van Deemter L, Janssen H, Calafat J, Oomen LC, Paulusma CC, Oude Elferink RP, Baas F, Schinkel AH, Borst P (1998) Drug export activity of the human canalicular multispecific organic anion transporter in polarized kidney MDCK cells expressing cMOAT (MRP2) cDNA. J Clin Invest 101:1310-1319
15. Golden PL, Pollack GM (2003) Blood-brain barrier efflux transport. J Pharm Sci 92:1739-1753
16. Goldstein GW, Betz AL, Bowman PD, Dorovini-Zis K (1986) In vitro studies of the blood-brain barrier using isolated brain capillaries and cultured endothelial cells. Ann N Y Acad Sc 481:202-213
17. Greenwood J, Pryce G, Devine L, Male DK, dos Santos WL, Calder VL, Adamson P (1996) SV40 large T immortalised cell lines of the rat blood-brain and blood-retinal barriers retain their phenotypic and immunological characteristics. J Neuroimmunol 71:51-63
18. Gutmann H, Fricker G, Torok M, Michael S, Beglinger C, Drewe J (1999) Evidence for different ABC-transporters in Caco-2 cells modulating drug uptake. Pharm Res 16:402-407
19. Herold-Mende C, Seiter S, Born AI, Patzelt E, Schupp M, Zoller J (1996) Expression of CD44 splice variants in squamous epithelia and squamous cell carcinomas of the head and neck. J Pathol 179:66-73
20. Kim RB, Fromm MF, Wandel C, Leake B, Wood AJ, Roden DM, Wilkinson GR (1998) The drug transporter P-glycoprotein limits oral absorption and brain entry of HIV-1 protease inhibitors. J Clin Invest 101:289-294
21. Kusch-Poddar M, Drewe J, Fux I, Gutmann H (2005) Evaluation of the immortalized human brain capillary endothelial cell line BB19 as a human cell culture model for the blood-brain barrier. Brain Res 1064:21-31
22. Lage H (2003) ABC-transporters: implications on drug resistance from microorganisms to human cancers. Int J Antimicrob Agents 22:188-199
23. Lindenmaier H, Becker M, Haefeli WE, Weiss J (2005) Interaction of progestins with the human multidrug resistance-associated protein 2 (MRP2). Drug Metab Dispos 33:1576-1579
24. Ling V (1997) Multidrug resistance: molecular mechanisms and clinical relevance. Cancer Chemother Pharmacol 40 Suppl:S3-S8
25. Löscher W, Potschka H (2005a) Role of drug efflux transporters in the brain for drug disposition and treatment of brain diseases. Prog Neurobiol 76:22-76
26. Löscher W, Potschka H (2005b) Drug resistance in brain diseases and the role of drug efflux transporters. Nat Rev Neurosci 6:591-602
27. Madara JL (1988) Tight junction dynamics: is paracellular transport regulated? Cell 53:497-498
28. Martin TA, Mansel RE, Jiang WG (2002) Antagonistic effect of NK4 on HGF/SF induced changes in the transendothelial resistance (TER) and paracellular permeability of human vascular endothelial cells. J Cell Physiol 192:268-275
29. McFarland DC (2000) Preparation of pure cell cultures by cloning. Methods Cell Sci 22:63-66
30. Merino G, Jonker JW, Wagenaar E, van Herwaarden AE, Schinkel AH (2005) The breast cancer resistance protein (BCRP/ABCG2) affects pharmacokinetics, hepatobiliary excretion, and milk secretion of the antibiotic nitrofurantoin. Mol Pharmacol 67:1758-1764
31. Minn A, Ghersi-Egea JF, Perrin R, Leininger B, Siest G (1991) Drug metabolizing enzymes in the brain and cerebral microvessels. Brain Res Brain Res Rev 16:65-82
32. Muruganandam A, Herx LM, Monette R, Durkin JP, Stanimirovic DB (1997) Development of immortalized human cerebromicrovascular endothelial cell line as an in vitro model of the human blood-brain barrier. FASEB J 11:1187-1197
33. Nies AT, Jedlitschky G, König J, Herold-Mende C, Steiner HH, Schmitt HP, Keppler D (2004) Expression and immunolocalization of the multidrug reistance proteins, MRP1-MRP6 (ABCC1-ABCC6), in human brain. Neuroscience 129:349-360
34. Pascolo L, Fernetti C, Pirulli D, Crovella S, Amoroso A, Tiribelli C (2003) Effects of maturation on RNA transcription and protein expression of four MRP genes in human placenta and in BeWo cells. Biochem Biophys Res Commun 303:259-265
35. Pear WS, Nolan GP, Scott ML, Baltimore D (1993) Production of high-titer helper-free retroviruses by transient transfection. Proc Natl Acad Sci USA 90:8392-8396
36. Potschka H, Fedrowitz M, Löscher W (2003) Multidrug resistance protein MRP2 contributes to blood-brain barrier function and restricts antiepileptic drug activity. J Pharmacol Exp Ther 306:124-131
37. Prudhomme JG, Sherman IW, Land KM, Moses AV, Stenglein S, Nelson JA (1996) Studies of Plasmodium falciparum cytoadherence using immortalized human brain capillary endothelial cells. Int J Parasitol 26:647-655
38. Regina A, Romero IA, Greenwood J, Adamson P, Bourre JM, Couraud PO, Roux F (1999) Dexamethasone regulation of P-glycoprotein activity in an immortalized rat brain endothelial cell line, GPNT. J Neurochem 73:1954-1963
39. Roux F, Couraud PO (2005) Rat brain endothelial cell lines for the study of blood-brain barrier permeability and transport functions. Cell Mol Neurobiol 25:41-58
40. Roux F, Durieu-Trautmann O, Chaverot N, Claire M, Mailly P, Bourre JM, Strosberg AD, Couraud PO (1994) Regulation of gamma-glutamyl transpeptidase and alkaline phosphatase activities in immortalized rat brain microvessel endothelial cells. J Cell Physiol 159:101-113
41. Rubin LL, Staddon JM (1999) The cell biology of the blood-brain barrier. Annu Rev Neurosci 22:11-28
42. Sauerbrey A, Sell W, Steinbach D, Voigt A, Zintl F (2002) Expression of the BCRP gene (ABCG2/MXR/ABCP) in childhood acute lymphoblastic leukaemia. Br J Haematol 118:147-150
43. Schaub TP, Kartenbeck J, Konig J, Spring H, Dorsam J, Staehler G, Storkel S, Thon WF, Keppler D (1999) Expression of the MRP2 gene-encoded conjugate export pump in human kidney proximal tubules and in renal cell carcinoma. J Am Soc Nephrol 10:1159-1169
44. Schinkel AH, Jonker JW (2003) Mammalian drug efflux transporters of the ATP binding cassette (ABC) family: an overview. Adv Drug Deliv Rev 55:3-29
45. Schinkel AH, Smit JJ, van Tellingen O, Beijnen JH, Wagenaar E, van Deemter L, Mol CA, van der Valk MA, Robanus-Maandag EC, te Riele HP (1994) Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 77:491-502
46. Seki M, Toi M, Kobayashi K, Shitara K, Umezawa K, Seon BK, Kan M (2000) Differential behavior of VEGF receptor expression and response to TNP-470 in two immortalized human endothelial cell lines. Int J Oncol 17:525-533
47. Shin JS, Jang IK, Kim CW, Kim JC (2004) Development and characterization of a rabbit corneal endothelial cell line. Jpn J Ophthalmol 48:454-459
48. Steiner HH, Karcher S, Mueller MM, Nalbantis E, Kunze S, Herold-Mende C (2004) Autocrine pathways of the vascular endothelial growth factor (VEGF) in glioblastoma multiforme: clinical relevance of radiation-induced increase of VEGF levels. J Neurooncol 66:129-138
49. Stins MF, Gilles F, Kim KS (1997) Selective expression of adhesion molecules on human brain microvascular endothelial cells. J Neuroimmunol 76:81-90
50. Stins MF, Badger J, Sik KK (2001) Bacterial invasion and transcytosis in transfected human brain microvascular endothelial cells. Microb Pathog 30:19-28
51. Sugiyama Y, Kusuhara H, Suzuki H (1999) Kinetic and biochemical analysis of carrier-mediated efflux of drugs through the blood-brain and blood-cerebrospinal fluid barriers: importance in the drug delivery to the brain. J Control Release 62:179-186
52. Takakura Y, Audus KL, Borchardt RT (1991) Blood-brain barrier: transport studies in isolated brain capillaries and in cultured brain endothelial cells. Adv Pharmacol 22:137-165
53. Thiebaut F, Tsuruo T, Hamada H, Gottesman MM, Pastan I, Willingham MC (1989) Immunohistochemical localization in normal tissues of different epitopes in the multidrug transport protein P170: evidence for localization in brain capillaries and crossreactivity of one antibody with a muscle protein. J Histochem Cytochem 37:159-164
54. Weiss J, Dormann SMG, Martin-Facklam M, Kerpen CJ, Ketabi-Kiyanvash N, Haefeli WE (2003) Inhibition of P-glycoprotein by newer antidepressants. J Pharmacol Exp Ther 305:197-204
55. Weksler BB, Subileau EA, Perriere N, Charneau P, Holloway K, Leveque M, Tricoire-Leignel H, Nicotra A, Bourdoulous S, Turowski P, Male DK, Roux F, Greenwood J, Romero IA, Couraud PO (2005) Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J 19:1872-1874
56. Zenker D, Begley D, Bratzke H, Rubsamen-Waigmann H, von Briesen H (2003) Human blood-derived macrophages enhance barrier function of cultured primary bovine and human brain capillary endothelial cells. J Physiol (Lond) 551:1023-1032