Initial contact of glioblastoma cells with existing normal brain endothelial cells strengthen the barrier function via fibroblast growth factor 2 secretion: A new in vitro blood-brain barrier model

Cellular and Molecular Neurobiology

Volumn 33, Issue 4, 2013, Pages 489-501

  Toyoda, Keisuke ^a   Tanaka, Kunihiko ^a   Nakagawa, Shinsuke ^a,b   Thuy, Dinh Ha Duy ^a,b   Ujifuku, Kenta ^a   Kamada, Kensaku ^a   Hayashi, Kentaro ^a   Matsuo, Takayuki ^a   Nagata, Izumi ^a   Niwa, Masami ^a,b  

^a NAGASAKI UNIVERSITY GRADUATE SCHOOL OF BIOMEDICAL SCIENCES   (Japan)

^b PharmaCo Cell Company Ltd   (Japan)

Author keywords

Blood brain barrier; Fibroblast growth factor 2; Glioblastoma; Rat brain endothelial cells

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; OCCLUDIN; PROTEIN ZO1;

ANIMAL CELL; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; CELL INTERACTION; CELL INVASION; CELLULAR PARAMETERS; COCULTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; GLIOBLASTOMA; HUMAN; HUMAN CELL; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROTEIN SECRETION; RAT; TRANSENDOTHELIAL ELECTRICAL RESISTANCE; TUMOR CELL;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN NEOPLASMS; CELL COMMUNICATION; CELL LINE, TUMOR; CELL MEMBRANE; CELL MOVEMENT; CULTURE MEDIA, CONDITIONED; ELECTRIC IMPEDANCE; ENDOTHELIAL CELLS; FIBROBLAST GROWTH FACTOR 2; GLIOBLASTOMA; GREEN FLUORESCENT PROTEINS; HUMANS; LUNG NEOPLASMS; MODELS, BIOLOGICAL; RATS; RATS, WISTAR; TIGHT JUNCTIONS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

RATTUS;

EID: 84876686880     PISSN: 02724340     EISSN: 15736830     Source Type: Journal    
DOI: 10.1007/s10571-013-9913-z     Document Type: Article

References (47)

1. Abbott NJ (2005) Dynamics of CNS barriers: evolution, differentiation, and modulation. Cell Mol Neurobiol 25:5-23
2. Argaw AT, Gurfein BT, Zhang Y, Zameer A, John GR (2009) VEGF-mediated disruption of endothelial CLN-5 promotes blood-brain barrier breakdown. Proc Natl Acad Sci USA 106:1977-1982
3. Behzadian MA, Wang XL, Windsor LJ, Ghaly N, Caldwell RB (2001) TGF-beta increases retinal endothelial cell permeability by increasing MMP-9: possible role of glial cells in endothelial barrier function. Invest Ophthalmol Vis Sci 42:853-859
4. Bendfeldt K, Radojevic V, Kapfhammer J, Nitsch C (2007) Basic fibroblast growth factor modulates density of blood vessels and preserves tight junctions in organotypic cortical cultures of mice: a new in vitro model of the blood-brain barrier. J Neurosci 27:3260-3267
5. Bernstein JJ, Woodard CA (1995) Glioblastoma cells do not intravasate into blood vessels. Neurosurgery 36:124-132
6. de Lange EC, Danhof M (2002) Considerations in the use of cerebrospinal fluid pharmacokinetics to predict brain target concentrations in the clinical setting: implications of the barriers between blood and brain. Clin Pharmacokinet 41:691-703
7. Dejana E (2004) Endothelial cell-cell junctions: happy together. Nat Rev Mol Cell Biol 5:261-270
8. Deli MA (2007) Blood-brain barrier models. In: Lajtha A (ed) Handbook of neurochemistry and molecular neurobiology, neural membranes and transport vol 11. Springer, New York, pp 29-56
9. Deli MA, Szabo C, Dung N, Joo F (1997) Immunohistochemical and electron microscopy detections on primary cultures of rat cerebral endothelial cells. In: Boer AG, Sutant W (eds) Drug transport across the blood-brain barrier: in vivo and in vitro techniques. Harwood Academic Publishers, Amsterdam, pp 23-28
10. Deli MA, Ábrahám 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
11. Dobbie MS, Hurst RD, Klein NJ, Surtees RA (1999) Upregulation of intracellular adhesion molecule-1 expression on human endothelial cells by tumour necrosis factor-α in an in vitro model of the blood-brain barrier. Brain Res 830:330-336
12. Dunn IF, Hesse O, Black P (2000) Growth factors in glioma angiogenesis: FGFs, PDGF, EGF, and TGFs. J Neurooncol 50:121-137
13. Gilbertson RJ, Rich JN (2007) Making a tumour's bed: glioblastoma stem cells and the vascular niche. Nat Rev Cancer 7:733-736
14. Grabb PA, Gilbert MR (1995) Neoplastic and pharmacological influence on the permeability of an in vitro blood-brain barrier. J Neurosurg 82:1053-1058
15. Greenwood J, Pryce G, Devine L, Male DK, dos Santos WL, Calder VL, Adamson P (1996) SV40 large T immortalized cell lines of the rat blood-brain and blood-retinal barriers retain their phenotypic and immunological characteristics. J Neuroimmunol 71:51-63
16. Hoheisel D, Nitz T, Franke H, Wegener J, Hakvoort A, Tilling T, Galla H-J (1998) Hydrocortisone reinforces the blood-brain barrier properties in a serum free cell culture system. Biochem Biophys Res Commun 247:312-315
17. Huang MS, Wang TJ, Liang CL, Huang HM, Yang IC, Yi-Jan H, Hisao M (2002) Establishment of fluorescent lung carcinoma metastasis model and its real-time microscopic detection in SCID mice. Clin Exp Metastasis 19:359-368
18. 2 involves matrix metalloproteinase and tight junction proteins. J Neuropathol Exp Neurol 67:435-448
19. Kato Y, Holm DA, Okollie B, Artemov D (2010) Noninvasive detection of temozolomide in brain tumor xenografts by magnetic resonance spectroscopy. Neuro-Oncology 12:71-79
20. Klint P, Kanda S, Kloog Y, Claesson-Welsh L (1999) Contribution of Src and Ras pathways in FGF-2 induced endothelial cell differentiation. Oncogene 18:3354-3364
21. Lund-Johansen M, Forsberg K, Bjerkvig R, Laerum OD (1992) Effects of growth factors on a human glioma cell line during invasion into rat brain aggregates in culture. Acta Neuropathol 84:190-197
22. Nakagawa S, Deli MA, Nakao S, Honda M, Hayashi K, Nakaoke R, Kataoka Y, Niwa M (2007) Pericytes from brain microvessels strengthen the barrier integrity in primary cultures of rat brain endothelial cells. Cell Mol Neurobiol 27:687-694
23. Nakagawa S, Deli MA, Kawaguchi H, Shimizudani T, Shimono T, Kittel A, Tanaka K, Niwa M (2009) A new blood-brain barrier model using primary rat brain endothelial cells, pericytes and astrocytes. Neurochem Int 54:253-263
24. Nir I, Levanon D, Iosilevsky G (1989) Permeability of blood vessels in experimental gliomas: uptake of 99mTc-glucoheptonate and alteration in blood-brain barrier as determined by cytochemistry and electron microscopy. Neurosurgery 25:523-531
25. Okumura N, Takimoto K, Okada M, Nakagawa H (1989) C6 glioma cells produce basic fibroblast growth factor that can stimulate their own proliferation. Biochemistry 106:904-909
26. Ostermann S, Csajka C, Buclin T, Leyvraz S, Lejeune F, Decosterd LA, Stupp R (2004) Plasma and cerebrospinal fluid population pharmacokinetics of temozolomide in malignant glioma patients. Clin Cancer Res 10:3728-3736
27. Paradridge WM (2002) Drug and gene targeting to brain with molecular Trojan horses. Nat Rev Drug Discov 1:131-139
28. Perrière N, Demeuse P, Garcia E, Regina A, Debray M, Andreux JP, Couvreur P, Scherrmann JM, Temsamani J, Couraud PO, Deli MA, Roux F (2005) Puromycin-based purification of rat brain capillary endothelial cell cultures. Effect on the expression of blood-brain barrier-specific properties. J Neurochem 93:279-289
29. Pitz MW, Desai A, Grossman SA, Blakeley JO (2011) Tissue concentration of systemically administered antineoplastic agents in human brain tumors. J Neurooncol 104:629-638
30. Plate KH, Breier G, Weich HA, Risau W (1992) Vascular endothelial growth factor is a potential tumor angiogenesis factor in human gliomas in vivo. Nature 359:845-848
31. Plowman J, Waud WR, Koutsoukos AD, Rubinstein LV, Moore TD, Grever MR (1994) Preclinical antitumor activity of temozolomide in mice: efficacy against human brain tumor xenografts and synergism with 1,3-bis(2-chloroethyl)-1- nitrosourea. Cancer Res 54:3793-3799
32. Reese TS, Karnovsky MJ (1967) Fine structural location of a blood-brain barrier to exogenous peroxidase. J Cell Biol 34:207-217
33. Reuss B, Dono R, Unsicker K (2003) Functions of fibroblast growth factor (FGF)-2 and FGF-5 in astroglial differentiation and blood-brain barrier permeability: evidence from mouse mutants. J Neurosci 23:6404-6412
34. Scherer HD (1940) Cerebral astrocytomas and their derivatives. Am J Cancer 1:159-198
35. Sobue K, Yamamoto N, Yoneda K, Hodgson ME, Yamashiro K, Tsuruoka N, Katsuya H, Miura Y, Asai K, Kato T (1999) Induction of blood brain barrier properties in immortalized bovine brain endothelial cells by astrocytic factors. Neurosci Res 35:155-164
36. Stefaik DF, Rizlkalla LR, Soi A, Goldblatt SA, Rizkalla WM (1991) Acidic and basic fibroblast growth factors are present in glioblastoma multiforme. Cancer Res 51:5705-5760
37. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987-996
38. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, Hau P, Brandes AA, Gijtenbeek J, Marosi C, Vecht CJ, Mokhtari K, Wesseling P, Villa S, Eisenhauer E, Gorlia T, Weller M, Lacombe D, Cairncross JG, Mirimanoff RO (2009) Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 10:459-466
39. Tanghetti E, Ria R, Dell'Era P, Urbinati C, Rusnati M, Ennas MG, Presta M (2002) Biological activity of substrate-bound basic fibroblast growth factor (FGF2): recruitment of FGF receptor-1 in endothelial cell adhesion contacts. Oncogene 21:3889-3897
40. Tovi M, Hartman M, Lilja A, Ericsson A (1994) MR imaging in cerebral gliomas. Tissue component analysis in correlation with histopathology of whole-brain specimens. Acta Radiol 35:495-505
41. Watanabe M, Tanaka R, Taeda N (1992) Magnetic resonance imaging and histopathology of cerebral gliomas. Neuroradiology 34:463-469
42. Wen PY, Kesari S (2008) Malignant gliomas in adults. N Engl J Med 359:492-507
43. Winkler F, Kienast Y, Fuhrmann M, Von Baumgarten L, Burgold S, Mitteregger G, Kretzschimar H, Herms J (2009) Imaging glioma cell invasion in vivo reveals mechanisms of dissemination and peritumoral angiogenesis. Glia 57:1306-1315
44. Yamamoto M, Mohanam S, Sawaya R (1998) Differential expression of membrane-type matrix metalloproteinase and its correlation with gelatinase A activation in human malignant brain tumors in vivo and in vitro. Cancer Res 56:384-392
45. Yang Y, Rosenberg GA (2011) MMP-mediated disruption of claudin-5 in the blood-brain barrier of rat brain after cerebral ischemia. Methods Mol Biol 762:333-345
46. ZagZag D, Goldenberg M, Brem S (1989) Angiogenesis and blood-brain barrier breakdown modulate CT contrast enhancement: an experimental study in a rabbit brain-tumor model. Am J Roentgenol 153:141-146
47. Zlokovic BV (2008) The blood-brain barrier in health and neurodegenerative disorders. Neuron 57:178-201