Krüppel-like factor 4 regulates blood-tumor barrier permeability via ZO-1, occludin and claudin-5

Journal of Cellular Physiology

Volumn 229, Issue 7, 2014, Pages 916-926

  Ma, Jun ^a   Wang, Ping ^a   Liu, Yunhui ^a   Zhao, Lini ^a   Li, Zhen ^a   Xue, Yixue ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 5; DNA; KRUPPEL LIKE FACTOR 4; LUCIFERASE; MESSENGER RNA; OCCLUDIN; PROTEIN ZO1; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR GATA 6; TRANSCRIPTION FACTOR SP1; TRANSCRIPTION FACTOR SP3;

ARTICLE; BLOOD BRAIN BARRIER; BLOOD TUMOR BARRIER; CELL CULTURE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA SEQUENCE; DOWN REGULATION; ENDOTHELIUM CELL; GENE SILENCING; GENETIC TRANSFECTION; GLIOBLASTOMA; GLIOMA CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; LUCIFERASE ASSAY; MOLECULAR INTERACTION; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIGHT JUNCTION; TRANSCRIPTION INITIATION SITE; UPREGULATION; WESTERN BLOTTING;

BLOOD-BRAIN BARRIER; BRAIN NEOPLASMS; CAPILLARY PERMEABILITY; CLAUDIN-5; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOMA; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; NEOPLASMS; NUCLEOTIDE MOTIFS; OCCLUDIN; PROMOTER REGIONS, GENETIC; TIGHT JUNCTIONS; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84896509261     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.24523     Document Type: Article

References (47)

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. Abbruscato TJ, Lopez SP, Mark KS, Hawkins BT, Davis TP. 2002. Nicotine and cotinine modulate cerebral microvascular permeability and protein expression of ZO-1 through nicotinic acetylcholine receptors expressed on brain endothelial cells. J Pharm Sci 91:2525-2538.
3. Ando-Akatsuka Y, Saitou M, Hirase T, Kishi M, Sakakibara A, Itoh M, Yonemura S, Furuse M, Tsukita S. 1996. Interspecies diversity of the occludin sequence: cDNA cloning of human, mouse, dog, and rat-kangaroo homologues. J Cell Biol 133:43-47.
4. Begley DJ, Brightman MW. 2003. Structural and functional aspects of the blood-brain barrier. Prog Drug Res 61:39-78.
5. Black KL, Ningaraj NS. 2004. Modulation of brain tumor capillaries for enhanced drug delivery selectively to brain tumor. Cancer Control 11:165-173.
6. Cowan CE, Kohler EE, Dugan TA, Mirza MK, Malik AB, Wary KK. 2010. Kruppel-like factor-4 transcriptionally regulates VE-cadherin expression and endothelial barrier function. Circ Res 107:959-966.
7. Dai X, Segre JA. 2004. Transcriptional control of epidermal specification and differentiation. Curr Opin Genet Dev 14:485-491.
8. Dang DT, Pevsner J, Yang VW. 2000. The biology of the mammalian Kruppel-like family of transcription factors. Int J Biochem Cell Biol 32:1103-1121.
9. Fanning AS, Jameson BJ, Jesaitis LA, Anderson JM. 1998. The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J Biol Chem 273:29745-29753.
10. Fischer S, Wobben M, Marti HH, Renz D, Schaper W. 2002. Hypoxia-induced hyperpermeability in brain microvessel endothelial cells involves VEGF-mediated changes in the expression of zonula occludens-1. Microvasc Res 63:70-80.
11. Hamik A, Lin Z, Kumar A, Balcells M, Sinha S, Katz J, Feinberg MW, Gerzsten RE, Edelman ER, Jain MK. 2007. Kruppel-like factor 4 regulates endothelial inflammation. J Biol Chem 282:13769-13779.
12. Higaki Y, Schullery D, Kawata Y, Shnyreva M, Abrass C, Bomsztyk K. 2002. Synergistic activation of the rat laminin gamma1 chain promoter by the gut-enriched Kruppel-like factor (GKLF/KLF4) and Sp1. Nucleic Acids Res 30:2270-2279.
13. Holmberg J, He X, Peredo I, Orrego A, Hesselager G, Ericsson C, Hovatta O, Oba-Shinjo SM, Marie SK, Nister M, Muhr J. 2011. Activation of neural and pluripotent stem cell signatures correlates with increased malignancy in human glioma. PLoS ONE 6:e18454.
14. Huber JD, Egleton RD, Davis TP. 2001. Molecular physiology and pathophysiology of tight junctions in the blood-brain barrier. Trends Neurosci 24:719-725.
15. Iaconetti C, Polimeni A, Sorrentino S, Sabatino J, Pironti G, Esposito G, Curcio A, Indolfi C. 2012. Inhibition of miR-92a increases endothelial proliferation and migration in vitro as well as reduces neointimal proliferation in vivo after vascular injury. Basic Res Cardiol 107:296.
16. Itoh M, Nagafuchi A, Yonemura S, Kitani-Yasuda T, Tsukita S. 1993. The 220-kD protein colocalizing with cadherins in non-epithelial cells is identical to ZO-1, a tight junction-associated protein in epithelial cells: cDNA cloning and immunoelectron microscopy. J Cell Biol 121:491-502.
17. Jaubert J, Cheng J, Segre JA. 2003. Ectopic expression of kruppel like factor 4 (Klf4) accelerates formation of the epidermal permeability barrier. Development 130:2767-2777.
18. Lee VH, Chow BK, Lo KW, Chow LS, Man C, Tsao SW, Lee LT. 2009. Regulation of RASSF1A in nasopharyngeal cells and its response to UV irradiation. Gene 443:55-63.
19. Lefranc F, Sadeghi N, Camby I, Metens T, Dewitte O, Kiss R. 2006. Present and potential future issues in glioblastoma treatment. Expert Rev Anticancer Ther 6:719-732.
20. Li L, Davie JR. 2010. The role of Sp1 and Sp3 in normal and cancer cell biology. Ann Anat 192:275-283.
21. Lowry JA, Mackay JP. 2006. GATA-1: One protein, many partners. Int J Biochem Cell Biol 38:6-11.
22. Luissint AC, Federici C, Guillonneau F, Chretien F, Camoin L, Glacial F, Ganeshamoorthy K, Couraud PO. 2012. Guanine nucleotide-binding protein Galphai2: A new partner of claudin-5 that regulates tight junction integrity in human brain endothelial cells. J Cereb Blood Flow Metab 32:860-873.
23. McConnell BB, Yang VW. 2010. Mammalian Kruppel-like factors in health and diseases. Physiol Rev 90:1337-1381.
24. McCormick SM, Eskin SG, McIntire LV, Teng CL, Lu CM, Russell CG, Chittur KK. 2001. DNA microarray reveals changes in gene expression of shear stressed human umbilical vein endothelial cells. Proc Natl Acad Sci U S A 98:8955-8960.
25. Merika M, Orkin SH. 1995. Functional synergy and physical interactions of the erythroid transcription factor GATA-1 with the Kruppel family proteins Sp1 and EKLF. Mol Cell Biol 15:2437-2447.
26. Nakahara Y, Northcott PA, Li M, Kongkham PN, Smith C, Yan H, Croul S, Ra YS, Eberhart C, Huang A, Bigner D, Grajkowska W, Van Meter T, Rutka JT, Taylor MD. 2010. Genetic and epigenetic inactivation of Kruppel-like factor 4 in medulloblastoma. Neoplasia 12:20-27.
27. Panigrahi SK, Vasileva A, Wolgemuth DJ. 2012. Sp1 transcription factor and GATA1 cis-acting elements modulate testis-specific expression of mouse cyclin A1. PLoS ONE 7:e47862.
28. Paolinelli R, Corada M, Orsenigo F, Dejana E. 2011. The molecular basis of the blood brain barrier differentiation and maintenance. Is it still a mystery? Pharmacol Res 63:165-171.
29. Papetti M, Wontakal SN, Stopka T, Skoultchi AI. 2010. GATA-1 directly regulates p21 gene expression during erythroid differentiation. Cell Cycle 9:1972-1980.
30. Rowland BD, Peeper DS. 2006. KLF4, p21 and context-dependent opposing forces in cancer. Nat Rev Cancer 6:11-23.
31. Schwartzbaum JA, Fisher JL, Aldape KD, Wrensch M. 2006. Epidemiology and molecular pathology of glioma. Nat Clin Pract Neurol 2:494-503; quiz 491 p. following 516.
32. Segre JA, Bauer C, Fuchs E. 1999. Klf4 is a transcription factor required for establishing the barrier function of the skin. Nat Genet 22:356-360.
33. Shie JL, Chen ZY, Fu M, Pestell RG, Tseng CC. 2000. Gut-enriched Kruppel-like factor represses cyclin D1 promoter activity through Sp1 motif. Nucleic Acids Res 28:2969-2976.
34. Stevenson BR, Siliciano JD, Mooseker MS, Goodenough DA. 1986. Identification of ZO-1: A high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J Cell Biol 103:755-766.
35. Stewart LA. 2002. Chemotherapy in adult high-grade glioma: A systematic review and meta-analysis of individual patient data from 12 randomised trials. Lancet 359:1011-1018.
36. Swamynathan SK, Katz JP, Kaestner KH, Ashery-Padan R, Crawford MA, Piatigorsky J. 2007. Conditional deletion of the mouse Klf4 gene results in corneal epithelial fragility, stromal edema, and loss of conjunctival goblet cells. Mol Cell Biol 27:182-194.
37. Swamynathan S, Kenchegowda D, Piatigorsky J. 2011. Regulation of corneal epithelial barrier function by Kruppel-like transcription factor 4. Invest Ophthalmol Vis Sci 52:1762-1769.
38. Sze KL, Lee WM, Lui WY. 2008. Expression of CLMP, a novel tight junction protein, is mediated via the interaction of GATA with the Kruppel family proteins, KLF4 and Sp1, in mouse TM4 Sertoli cells. J Cell Physiol 214:334-344.
39. Wei D, Gong W, Kanai M, Schlunk C, Wang L, Yao JC, Wu TT, Huang S, Xie K. 2005. Drastic down-regulation of Kruppel-like factor 4 expression is critical in human gastric cancer development and progression. Cancer Res 65:2746-2754.
40. 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.
41. Wigner NA, Soung DY, Einhorn TA, Drissi H, Gerstenfeld LC. 2013. Functional role of Runx3 in the regulation of aggrecan expression during cartilage development. J Cell Physiol 228:2232-2242.
42. Wolburg H, Noell S, Mack A, Wolburg-Buchholz K, Fallier-Becker P. 2009. Brain endothelial cells and the glio-vascular complex. Cell Tissue Res 335:75-96.
43. Yet SF, McA'Nulty MM, Folta SC, Yen HW, Yoshizumi M, Hsieh CM, Layne MD, Chin MT, Wang H, Perrella MA, Jain MK, Lee ME. 1998. Human EZF, a Kruppel-like zinc finger protein, is expressed in vascular endothelial cells and contains transcriptional activation and repression domains. J Biol Chem 273:1026-1031.
44. Zhang P, Basu P, Redmond LC, Morris PE, Rupon JW, Ginder GD, Lloyd JA. 2005. A functional screen for Kruppel-like factors that regulate the human gamma-globin gene through the CACCC promoter element. Blood Cells Mol Dis 35:227-235.
45. Zhao W, Hisamuddin IM, Nandan MO, Babbin BA, Lamb NE, Yang VW. 2004. Identification of Kruppel-like factor 4 as a potential tumor suppressor gene in colorectal cancer. Oncogene 23:395-402.
46. Zheng X, Li A, Zhao L, Zhou T, Shen Q, Cui Q, Qin X. 2013. Key role of microRNA-15a in the KLF4 suppressions of proliferation and angiogenesis in endothelial and vascular smooth muscle cells. Biochem Biophys Res Commun 437:625-631.
47. Zhou B, Francis TA, Yang H, Tseng W, Zhong Q, Frenkel B, Morrisey EE, Ann DK, Minoo P, Crandall ED, Borok Z. 2008. GATA-6 mediates transcriptional activation of aquaporin-5 through interactions with Sp1. Am J Physiol Cell Physiol 295:C1141-C1150.