EndMT contributes to the onset and progression of cerebral cavernous malformations

Nature

Volumn 498, Issue 7455, 2013, Pages 492-496

  Maddaluno, Luigi ^a   Rudini, Noemi ^a   Cuttano, Roberto ^a   Bravi, Luca ^a   Giampietro, Costanza ^a   Corada, Monica ^a   Ferrarini, Luca ^a   Orsenigo, Fabrizio ^a   Papa, Eleanna ^a   Boulday, Gwenola ^b,c   Tournier Lasserve, Elisabeth ^b,c,d   Chapon, Françoise ^e   Richichi, Cristina ^f   Retta, Saverio Francesco ^g   Lampugnani, Maria Grazia ^a,h   Dejana, Elisabetta ^a,i  

^a FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^b INSERM   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d SAINT LOUIS HOSPITAL   (France)

^e CAEN UNIVERSITY HOSPITAL   (France)

^f EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^g UNIVERSITY OF TURIN   (Italy)

^h MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

ⁱ UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 6; CCM1 PROTEIN; MEMBRANE PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ABNORMALITY; BRAIN; DISEASE TREATMENT; GENE EXPRESSION; LESION; NERVOUS SYSTEM DISORDER; NEUROLOGY; PATHOLOGY; RODENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CAVERNOUS HEMANGIOMA; CELL TRANSFORMATION; CONGENITAL BLOOD VESSEL MALFORMATION; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; ENDOTHELIAL TO MESENCHYMAL TRANSITION; ENDOTHELIUM CELL; HEMANGIOMA; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; BONE MORPHOGENETIC PROTEIN 6; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; EPITHELIAL-MESENCHYMAL TRANSITION; HEMANGIOMA, CAVERNOUS, CENTRAL NERVOUS SYSTEM; HUMANS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; UP-REGULATION;

MUS;

EID: 84879690589     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12207     Document Type: Article

References (37)

1. Bergametti, F. et al. Mutations within the programmed cell death 10 gene cause cerebral cavernous malformations. Am. J. Hum. Genet. 76, 42-51 (2005).
2. Whitehead, K. J. et al. The cerebral cavernous malformation signaling pathway promotes vascular integrity via Rho GTPases. Nature Med. 15, 177-184 (2009).
3. Chan, A. C. et al. Mutations in 2 distinct genetic pathways result in cerebral cavernous malformations in mice. J. Clin. Invest. 121, 1871-1881 (2011).
4. Glading, A., Han, J., Stockton, R. A. & Ginsberg, M. H. KRIT-1/CCM1 is a Rap1 effector that regulates endothelial cell cell junctions. J. Cell Biol. 179, 247-254 (2007).
5. Stockton, R. A., Shenkar, R., Awad, I. A. & Ginsberg, M. H. Cerebral cavernous malformations proteins inhibit Rho kinase to stabilize vascular integrity. J. Exp. Med. 207, 881-896 (2010).
6. Lampugnani, M. G. et al.CCM1regulates vascular-lumen organization by inducing endothelial polarity. J. Cell Sci. 123, 1073-1080 (2010).
7. Wü stehube, J. et al. Cerebral cavernous malformation protein CCM1 inhibits sprouting angiogenesis by activatingDELTA-NOTCHsignaling. Proc.Natl Acad. Sci. USA 107, 12640-12645 (2010).
8. Faurobert, E. & Albiges-Rizo, C. Recent insights into cerebral cavernous malformations: a complex jigsaw puzzle under construction. FEBS J. 277, 1084-1096 (2010).
9. Boulday, G. et al. Developmental timing of CCM2 loss influences cerebral cavernous malformations in mice. J. Exp. Med. 208, 1835-1847 (2011).
10. Zeisberg, E. M. et al. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nature Med. 13, 952-961 (2007).
11. Medici, D. et al. Conversion of vascular endothelial cells into multipotent stem-like cells. Nature Med. 16, 1400-1406 (2010).
12. Kalluri, R.&Weinberg, R. A. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119, 1420-1428 (2009).
13. Labauge, P., Denier, C., Bergametti, F. & Tournier-Lasserve, E. Genetics of cavernous angiomas. Lancet Neurol. 6, 237-244 (2007).
14. Lopez, D., Niu, G., Huber, P. & Carter, W. B. Tumor-induced upregulation of Twist, Snail, and Slug represses the activity of the human VE-cadherin promoter. Arch. Biochem. Biophys. 482, 77-82 (2009).
15. Mariotti, A., Perotti, A., Sessa, C. & Ruegg, C. N-cadherin as a therapeutic target in cancer. Expert Opin. Investig. Drugs 16, 451-465 (2007).
16. Thiery, J. P., Acloque, H., Huang, R. Y. & Nieto, M. A. Epithelial-mesenchymal transitions in development and disease. Cell 139, 871-890 (2009).
17. Li, Y., Yang, J., Luo, J. H., Dedhar, S. & Liu, Y. Tubular epithelial cell dedifferentiation is driven by the helix-loop-helix transcriptional inhibitor Id1. J. Am. Soc. Nephrol. 18, 449-460 (2007).
18. Vivien, C. et al. Non-viral expression of mouse Oct4, Sox2, and Klf4 transcription factors efficiently reprograms tadpole muscle fibers in vivo. J. Biol. Chem. 287, 7427-7435 (2012).
19. Gauger, K. J., Chenausky, K. L., Murray, M. E. & Schneider, S. S. SFRP1 reduction results in an increased sensitivity to TGF-b signaling.BMC Cancer 11, 59 (2011).
20. Melisi, D. et al. LY2109761, a novel transforming growth factor b receptor type I and type II dual inhibitor, as a therapeutic approach to suppressing pancreatic cancer metastasis. Mol. Cancer Ther. 7, 829-840 (2008).
21. Tanaka, H. et al. Transforming growth factor beta signaling inhibitor, SB-431542, inducesmaturation of dendritic cells and enhances anti-tumor activity.Oncol. Rep. 24, 1637-1643 (2010).
22. McLean, K. et al. Human ovarian carcinoma-associated mesenchymal stem cells regulate cancer stem cells and tumorigenesis via altered BMP production. J. Clin. Invest. 121, 3206-3219 (2011).
23. Ao, A., Hao, J., Hopkins, C. R. & Hong, C. C. DMH1, a novel BMP small molecule inhibitor, increases cardiomyocyte progenitors and promotes cardiac differentiation in mouse embryonic stem cells. PLoS ONE 7, e41627 (2012).
24. Murtaugh, L. C., Stanger, B. Z., Kwan, K. M. & Melton, D. A. Notch signaling controls multiple steps of pancreatic differentiation. Proc. Natl Acad. Sci. USA 100, 14920-14925 (2003).
25. Korpal, M. & Kang, Y. Targeting the transforming growth factor-beta signalling pathway in metastatic cancer. Eur. J. Cancer 46, 1232-1240 (2010).
26. Yuan, Q. et al. Fluorofenidone suppresses epithelial-mesenchymal transition and the expression of connective tissue growth factor via inhibiting TGF-b/Smads signaling in humanproximal tubular epithelial cells. Pharmazie 66,961-967 (2011).
27. Glading, A. J. & Ginsberg, M. H. Rap1 and its effector KRIT1/CCM1 regulate b-catenin signaling. Dis. Model Mech. 3, 73-83 (2010).
28. Liebner, S. et al.b-cateninis required for endothelial-mesenchymal transformation duringheart cushiondevelopment in themouse. J.Cell Biol.166,359-367(2004).
29. Liebner, S., Czupalla, C. J. & Wolburg, H. Current concepts of blood-brain barrier development. Int. J. Dev. Biol. 55, 467-476 (2011).
30. Louvi, A. et al. Loss of cerebral cavernousmalformation 3(Ccm3) inneuroglia leads toCCMand vascular pathology. Proc. Natl Acad. Sci. USA108, 3737-3742 (2011).
31. Corada,M. et al. TheWnt/b-catenin pathwaymodulates vascular remodeling and specificationbyupregulatingDll4/Notchsignaling.Dev.Cell 18, 938-949(2010).
32. Soriano, P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nature Genet. 21, 70-71 (1999).
33. Spagnuolo, R. et al. Gas1 is induced by VE-cadherin and vascular endothelial growth factor and inhibits endothelial cell apoptosis. Blood 103, 3005-3012 (2004).
34. Felici, A. et al. TLP, a novel modulator of TGF-b signaling, has opposite effects on Smad2-and Smad3-dependent signaling. EMBO J. 22, 4465-4477 (2003).
35. Bussolino, F. et al. Murine endothelioma cell lines transformed by polyoma middle T oncogene as target for and producers of cytokines. J. Immunol. 147, 2122-2129 (1991).
36. Liebner, S. et al. Wnt/b-catenin signaling controls development of the bloodbrain barrier. J. Cell Biol. 183, 409-417 (2008).
37. Korff, T. & Augustin, H. G. Tensional forces in fibrillar extracellular matrices control directional capillary sprouting. J. Cell Sci. 112, 3249-3258 (1999).