FoxM1 regulates re-annealing of endothelial adherens junctions through transcriptional control of β-catenin expression

Journal of Experimental Medicine

Volumn 207, Issue 8, 2010, Pages 1675-1685

  Mirza, Muhammad K ^a   Sun, Ying ^a   Zhao, Yidan D ^a   Potula, Hari Hara S K ^a   Frey, Randall S ^a   Vogel, Steven M ^a   Malik, Asrar B ^a   Zhao, You Yang ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; PROTEINASE ACTIVATED RECEPTOR 1; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FORKHEAD BOX M1; UNCLASSIFIED DRUG; CATENIN; CTNNB1 PROTEIN, HUMAN; DELTA CATENIN; FORKHEAD TRANSCRIPTION FACTOR; FOXM1 PROTEIN, HUMAN; FOXM1 PROTEIN, MOUSE; JUP PROTEIN, MOUSE; OLIGOPEPTIDE; PAR-1-ACTIVATING PEPTIDE; PLAKOGLOBIN; PROTEIN BINDING; THROMBIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; CELL JUNCTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOTHELIUM CELL; ENDOTHELIUM INJURY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; LUNG BLOOD VESSEL; MICROVASCULATURE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANIMAL; CAPILLARY PERMEABILITY; CELL CULTURE; CELL MEMBRANE; CHROMATIN IMMUNOPRECIPITATION; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; IMPEDANCE; INBRED MOUSE STRAIN; LUNG; METABOLISM; PHYSIOLOGY; PROMOTER REGION; TRANSGENIC MOUSE;

ADHERENS JUNCTIONS; ANIMALS; BETA CATENIN; CAPILLARY PERMEABILITY; CATENINS; CELL MEMBRANE; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; ELECTRIC IMPEDANCE; ENDOTHELIAL CELLS; FORKHEAD TRANSCRIPTION FACTORS; GAMMA CATENIN; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMANS; INTERCELLULAR JUNCTIONS; LUNG; MICE; MICE, INBRED STRAINS; MICE, TRANSGENIC; OLIGOPEPTIDES; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RNA, SMALL INTERFERING; THROMBIN; TRANSFECTION;

EID: 77955395384     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20091857     Document Type: Article

References (35)

1. Aberle, H., H. Schwartz, and R. Kemler. 1996. Cadherin-catenin complex: protein interactions and their implications for cadherin function. J. Cell. Biochem. 61:514-523. doi:10.1002/(SICI)1097-4644(19960616)61:4〈514::AID- JCB4〉3.0.CO;2-R
2. Aird, W.C. 2007. Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ. Res. 100:158-173. doi:10.1161/01.RES.0000255691.76142.4a
3. Bachmaier, K., S. Toya, X. Gao, T. Triantafillou, S. Garrean, G.Y. Park, R.S. Frey, S. Vogel, R. Minshall, J.W. Christman, et al. 2007. E3 ubiquitin ligase Cblb regulates the acute inflammatory response underlying lung injury. Nat. Med. 13:920-926. doi:10.1038/nm1607 (Pubitemid 47222038)
4. Bazzoni, G., and E. Dejana. 2004. Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis. Physiol. Rev. 84:869-901. doi:10.1152/physrev.00035.2003
5. Birukova, A.A., K. Smurova, K.G. Birukov, K. Kaibuchi, J.G. Garcia, and A.D. Verin. 2004. Role of Rho GTPases in thrombin-induced lung vascular endothelial cells barrier dysfunction. Microvasc. Res. 67:64-77. doi:10.1016/j.mvr.2003.09.007
6. Broman, M.T., P. Kouklis, X. Gao, R. Ramchandran, R.F. Neamu, R.D. Minshall, and A.B. Malik. 2006. Cdc42 regulates adherens junction stability and endothelial permeability by inducing alpha-catenin interaction with the vascular endothelial cadherin complex. Circ. Res. 98:73-80. doi:10.1161/01.RES. 0000198387.44395.e9
7. Camerer, E., I. Cornelissen, H. Kataoka, D.N. Duong, Y.W. Zheng, and S.R. Coughlin. 2006. Roles of protease-activated receptors in a mouse model of endotoxemia. Blood. 107:3912-3921. doi:10.1182/blood-2005-08-3130
8. Carmeliet, P., M.G. Lampugnani, L. Moons, F. Breviario, V. Compernolle, F. Bono, G. Balconi, R. Spagnuolo, B. Oosthuyse, M. Dewerchin, et al. 1999. Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell. 98:147-157. doi:10.1016/S0092-8674(00)81010-7
9. Cattelino, A., S. Liebner, R. Gallini, A. Zanetti, G. Balconi, A. Corsi, P. Bianco, H. Wolburg, R. Moore, B. Oreda, et al. 2003. The conditional inactivation of the β-catenin gene in endothelial cells causes a defective vascular pattern and increased vascular fragility. J. Cell Biol. 162:1111-1122. doi:10.1083/jcb.200212157 (Pubitemid 37174193)
10. Clark, K.L., E.D. Halay, E. Lai, and S.K. Burley. 1993. Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5. Nature. 364:412-420. doi:10.1038/364412a0
11. Costa, R.H. 2005. FoxM1 dances with mitosis. Nat. Cell Biol. 7:108-110. doi:10.1038/ncb0205-108
12. Coughlin, S.R. 2000. Thrombin signalling and protease-activated receptors. Nature. 407:258-264. doi:10.1038/35025229
13. Dejana, E. 2004. Endothelial cell-cell junctions: happy together. Nat. Rev. Mol. Cell Biol. 5:261-270. doi:10.1038/nrm1357 (Pubitemid 38480607)
14. Dejana, E., F. Orsenigo, and M.G. Lampugnani. 2008. The role of adherens junctions and VE-cadherin in the control of vascular permeability. J. Cell Sci. 121:2115-2122. doi:10.1242/jcs.017897
15. Huber, A.H., D.B. Stewart, D.V. Laurents, W.J. Nelson, and W.I. Weis. 2001. The cadherin cytoplasmic domain is unstructured in the absence of beta-catenin. A possible mechanism for regulating cadherin turnover. J. Biol. Chem. 276:12301-12309. doi:10.1074/jbc.M010377200
16. Huelsken, J., R. Vogel, V. Brinkmann, B. Erdmann, C. Birchmeier, and W. Birchmeier. 2000. Requirement for β-catenin in anterior-posterior axis formation in mice. J. Cell Biol. 148:567-578. doi:10.1083/jcb.148.3.567
17. Kaestner, K.H., W. Knochel, and D.E. Martinez. 2000. Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev. 14:142-146.
18. Kalinichenko, V.V., M.L. Major, X. Wang, V. Petrovic, J. Kuechle, H.M. Yoder, M.B. Dennewitz, B. Shin, A. Datta, P. Raychaudhuri, and R.H. Costa. 2004. Foxm1b transcription factor is essential for development of hepatocellular carcinomas and is negatively regulated by the p19ARF tumor suppressor. Genes Dev. 18:830-850. doi:10.1101/gad.1200704
19. Korver, W., M.W. Schilham, P. Moerer, M.J. van den Hoff, K. Dam, W.H. Lamers, R.H. Medema, and H. Clevers. 1998. Uncoupling of S phase and mitosis in cardiomyocytes and hepatocytes lacking the winged-helix transcription factor Trident. Curr. Biol. 8:1327-1330. doi:10.1016/S0960-9822(07)00563-5
20. Krupczak-Hollis, K., X. Wang, V.V. Kalinichenko, G.A. Gusarova, I.C. Wang, M.B. Dennewitz, H.M. Yoder, H. Kiyokawa, K.H. Kaestner, and R.H. Costa. 2004. The mouse Forkhead Box m1 transcription factor is essential for hepatoblast mitosis and development of intrahepatic bile ducts and vessels during liver morphogenesis. Dev. Biol. 276:74-88. doi:10.1016/j.ydbio.2004.08. 022
21. Lampugnani, M.G., and E. Dejana. 2007. Adherens junctions in endothelial cells regulate vessel maintenance and angiogenesis. Thromb. Res. 120:S1-S6. doi:10.1016/S0049-3848(07)70124-X
22. Lampugnani, M.G., M. Corada, L. Caveda, F. Breviario, O. Ayalon, B. Geiger, and E. Dejana. 1995. The molecular organization of endothelial cell to cell junctions: differential association of plakoglobin, β-catenin, and α-catenin with vascular endothelial cadherin (VE-cadherin). J. Cell Biol. 129:203-217. doi:10.1083/jcb.129.1.203
23. Laoukili, J., M.R. Kooistra, A. Brás, J. Kauw, R.M. Kerkhoven, A. Morrison, H. Clevers, and R.H. Medema. 2005. FoxM1 is required for execution of the mitotic programme and chromosome stability. Nat. Cell Biol. 7:126-136. doi:10.1038/ncb1217 (Pubitemid 40268127)
24. Mehta, D., and A.B. Malik. 2006. Signaling mechanisms regulating endothelial permeability. Physiol. Rev. 86:279-367. doi:10.1152/physrev.00012. 2005
25. Navarro, P., L. Caveda, F. Breviario, I. Mândoteanu, M.G. Lampugnani, and E. Dejana. 1995. Catenin-dependent and -independent functions of vascular endothelial cadherin. J. Biol. Chem. 270:30965-30972. doi:10.1074/jbc.270.52.30965
26. Tauseef, M., V. Kini, N. Knezevic, M. Brannan, R. Ramchandaran, H. Fyrst, J. Saba, S.M. Vogel, A.B. Malik, and D. Mehta. 2008. Activation of sphingosine kinase-1 reverses the increase in lung vascular permeability through sphingosine-1-phosphate receptor signaling in endothelial cells. Circ. Res. 103:1164-1172. doi:10.1161/01.RES.0000338501.84810.51
27. Tiruppathi, C., A.B. Malik, P.J. Del Vecchio, C.R. Keese, and I. Giaever. 1992. Electrical method for detection of endothelial cell shape change in real time: assessment of endothelial barrier function. Proc. Natl. Acad. Sci. USA. 89:7919-7923. doi:10.1073/pnas.89.17.7919
28. Tiruppathi, C., M. Freichel, S.M. Vogel, B.C. Paria, D. Mehta, V. Flockerzi, and A.B. Malik. 2002. Impairment of store-operated Ca2+ entry in TRPC4(-/-) mice interferes with increase in lung microvascular permeability. Circ. Res. 91:70-76. doi:10.1161/01.RES.0000023391.40106.A8
29. Vogel, S.M., X. Gao, D. Mehta, R.D. Ye, T.A. John, P. Andrade-Gordon, C. Tiruppathi, and A.B. Malik. 2000. Abrogation of thrombin-induced increase in pulmonary microvascular permeability in PAR-1 knockout mice. Physiol. Genomics. 4:137-145.
30. Wang, I.C., Y.J. Chen, D. Hughes, V. Petrovic, M.L. Major, H.J. Park, Y. Tan, T. Ackerson, and R.H. Costa. 2005. Forkhead box M1 regulates the transcriptional network of genes essential for mitotic progression and genes encoding the SCF (Skp2-Cks1) ubiquitin ligase. Mol. Cell. Biol. 25:10875-10894. doi:10.1128/MCB.25.24.10875-10894.2005
31. Ware, L.B., and M.A. Matthay. 2000. The acute respiratory distress syndrome. N. Engl. J. Med. 342:1334-1349. doi:10.1056/NEJM200005043421806
32. Weis, S.M., and D.A. Cheresh. 2005. Pathophysiological consequences of VEGF-induced vascular permeability. Nature. 437:497-504. doi:10.1038/nature03987
33. Wierstra, I., and J. Alves. 2007. FOXM1, a typical proliferation- associated transcription factor. Biol. Chem. 388:1257-1274. doi:10.1515/BC.2007. 159 (Pubitemid 350135573)
34. Zhao, Y.Y., X.P. Gao, Y.D. Zhao, M.K. Mirza, R.S. Frey, V.V. Kalinichenko, I.C. Wang, R.H. Costa, and A.B. Malik. 2006. Endothelial cell-restricted disruption of FoxM1 impairs endothelial repair following LPS-induced vascular injury. J. Clin. Invest. 116:2333-2343. doi:10.1172/JCI27154
35. Zhao, Y.D., H. Ohkawara, S.M. Vogel, A.B. Malik, and Y.Y. Zhao. 2010. Bone marrow-derived progenitor cells prevent thrombin-induced increase in lung vascular permeability. Am. J. Physiol. Lung Cell. Mol. Physiol. 298:L36-L44. doi:10.1152/ajplung.00064.2009