Home LiteratureArticle Details
PMID: 23748444 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

EndMT contributes to the onset and progression of cerebral cavernous malformations.

Nature ·Vol. 498 ·No. 7455 ·2013-06-27 ·Pages 492-6

Maddaluno L, Rudini N, Cuttano R, Bravi L, Giampietro C, Corada M, Ferrarini L, Orsenigo F, Papa E, Boulday G, Tournier-Lasserve E, Chapon F, Richichi C, Retta SF, Lampugnani MG, Dejana E

Abstract

Cerebral cavernous malformation (CCM) is a vascular dysplasia, mainly localized within the brain and affecting up to 0.5% of the human population. CCM lesions are formed by enlarged and irregular blood vessels that often result in cerebral haemorrhages. CCM is caused by loss-of-function mutations in one of three genes, namely CCM1 (also known as KRIT1), CCM2 (OSM) and CCM3 (PDCD10), and occurs in both sporadic and familial forms. Recent studies have investigated the cause of vascular dysplasia and fragility in CCM, but the in vivo functions of this ternary complex remain unclear. Postnatal deletion of any of the three Ccm genes in mouse endothelium results in a severe phenotype, characterized by multiple brain vascular malformations that are markedly similar to human CCM lesions. Endothelial-to-mesenchymal transition (EndMT) has been described in different pathologies, and it is defined as the acquisition of mesenchymal- and stem-cell-like characteristics by the endothelium. Here we show that endothelial-specific disruption of the Ccm1 gene in mice induces EndMT, which contributes to the development of vascular malformations. EndMT in CCM1-ablated endothelial cells is mediated by the upregulation of endogenous BMP6 that, in turn, activates the transforming growth factor-β (TGF-β) and bone morphogenetic protein (BMP) signalling pathway. Inhibitors of the TGF-β and BMP pathway prevent EndMT both in vitro and in vivo and reduce the number and size of vascular lesions in CCM1-deficient mice. Thus, increased TGF-β and BMP signalling, and the consequent EndMT of CCM1-null endothelial cells, are crucial events in the onset and progression of CCM disease. These studies offer novel therapeutic opportunities for this severe, and so far incurable, pathology.

MeSH Terms
Animals Bone Morphogenetic Protein 6/antagonists & inhibitors,metabolism,pharmacology Disease Models, Animal Disease Progression Epithelial-Mesenchymal Transition/drug effects,genetics Hemangioma, Cavernous, Central Nervous System/genetics,pathology Humans KRIT1 Protein Mice Microtubule-Associated Proteins/deficiency,genetics,metabolism Proto-Oncogene Proteins/deficiency,genetics,metabolism Signal Transduction/drug effects,genetics Transforming Growth Factor beta/antagonists & inhibitors,metabolism Up-Regulation
Chemicals
Bone Morphogenetic Protein 6 KRIT1 Protein Krit1 protein, mouse Microtubule-Associated Proteins Proto-Oncogene Proteins Transforming Growth Factor beta
Authors & Affiliations
16 authors, click to expand affiliations / ORCID
Maddaluno Luigi
IFOM Fondazione, FIRC Institute of Molecular Oncology, 20139 Milan, Italy. uigi.maddaluno@ifom.eu
Rudini Noemi
Cuttano Roberto
Bravi Luca
Giampietro Costanza
Corada Monica
Ferrarini Luca
Orsenigo Fabrizio
Papa Eleanna
Boulday Gwenola
Tournier-Lasserve Elisabeth
Chapon Françoise
Richichi Cristina
Retta Saverio Francesco
Lampugnani Maria Grazia
Dejana Elisabetta
References (37)
37 references, click to expand
  1. Human ovarian carcinoma–associated mesenchymal stem cells regulate cancer stem cells and tumorigenesis via altered BMP production.
    J Clin Invest. 2011 Aug;121(8):3206-19 PMID: 21737876
  2. CCM1 regulates vascular-lumen organization by inducing endothelial polarity.
    J Cell Sci. 2010 Apr 1;123(Pt 7):1073-80 PMID: 20332120
  3. Current concepts of blood-brain barrier development.
    Int J Dev Biol. 2011;55(4-5):467-76 PMID: 21769778
  4. Tubular epithelial cell dedifferentiation is driven by the helix-loop-helix transcriptional inhibitor Id1.
    J Am Soc Nephrol. 2007 Feb;18(2):449-60 PMID: 17202424
  5. Mutations in 2 distinct genetic pathways result in cerebral cavernous malformations in mice.
    J Clin Invest. 2011 May;121(5):1871-81 PMID: 21490399
  6. Targeting the transforming growth factor-beta signalling pathway in metastatic cancer.
    Eur J Cancer. 2010 May;46(7):1232-40 PMID: 20307969
  7. The Wnt/beta-catenin pathway modulates vascular remodeling and specification by upregulating Dll4/Notch signaling.
    Dev Cell. 2010 Jun 15;18(6):938-49 PMID: 20627076
  8. Mutations within the programmed cell death 10 gene cause cerebral cavernous malformations.
    Am J Hum Genet. 2005 Jan;76(1):42-51 PMID: 15543491
  9. Epithelial-mesenchymal transitions in development and disease.
    Cell. 2009 Nov 25;139(5):871-90 PMID: 19945376
  10. SFRP1 reduction results in an increased sensitivity to TGF-β signaling.
    BMC Cancer. 2011 Feb 08;11:59 PMID: 21303533
  11. Fluorofenidone suppresses epithelial-mesenchymal transition and the expression of connective tissue growth factor via inhibiting TGF-beta/Smads signaling in human proximal tubular epithelial cells.
    Pharmazie. 2011 Dec;66(12):961-7 PMID: 22312703
  12. Murine endothelioma cell lines transformed by polyoma middle T oncogene as target for and producers of cytokines.
    J Immunol. 1991 Oct 1;147(7):2122-9 PMID: 1918946
  13. Cerebral cavernous malformation protein CCM1 inhibits sprouting angiogenesis by activating DELTA-NOTCH signaling.
    Proc Natl Acad Sci U S A. 2010 Jul 13;107(28):12640-5 PMID: 20616044
  14. Wnt/beta-catenin signaling controls development of the blood-brain barrier.
    J Cell Biol. 2008 Nov 3;183(3):409-17 PMID: 18955553
  15. Conversion of vascular endothelial cells into multipotent stem-like cells.
    Nat Med. 2010 Dec;16(12):1400-6 PMID: 21102460
  16. Rap1 and its effector KRIT1/CCM1 regulate beta-catenin signaling.
    Dis Model Mech. 2010 Jan-Feb;3(1-2):73-83 PMID: 20007487
  17. Developmental timing of CCM2 loss influences cerebral cavernous malformations in mice.
    J Exp Med. 2011 Aug 29;208(9):1835-47 PMID: 21859843
  18. Notch signaling controls multiple steps of pancreatic differentiation.
    Proc Natl Acad Sci U S A. 2003 Dec 9;100(25):14920-5 PMID: 14657333
  19. Beta-catenin is required for endothelial-mesenchymal transformation during heart cushion development in the mouse.
    J Cell Biol. 2004 Aug 2;166(3):359-67 PMID: 15289495
  20. The basics of epithelial-mesenchymal transition.
    J Clin Invest. 2009 Jun;119(6):1420-8 PMID: 19487818
  21. Cerebral cavernous malformations proteins inhibit Rho kinase to stabilize vascular integrity.
    J Exp Med. 2010 Apr 12;207(4):881-96 PMID: 20308363
  22. Non-viral expression of mouse Oct4, Sox2, and Klf4 transcription factors efficiently reprograms tadpole muscle fibers in vivo.
    J Biol Chem. 2012 Mar 2;287(10):7427-35 PMID: 22232554
  23. N-cadherin as a therapeutic target in cancer.
    Expert Opin Investig Drugs. 2007 Apr;16(4):451-65 PMID: 17371194
  24. DMH1, a novel BMP small molecule inhibitor, increases cardiomyocyte progenitors and promotes cardiac differentiation in mouse embryonic stem cells.
    PLoS One. 2012;7(7):e41627 PMID: 22848549
  25. KRIT-1/CCM1 is a Rap1 effector that regulates endothelial cell cell junctions.
    J Cell Biol. 2007 Oct 22;179(2):247-54 PMID: 17954608
  26. Gas1 is induced by VE-cadherin and vascular endothelial growth factor and inhibits endothelial cell apoptosis.
    Blood. 2004 Apr 15;103(8):3005-12 PMID: 15070677
  27. TLP, a novel modulator of TGF-beta signaling, has opposite effects on Smad2- and Smad3-dependent signaling.
    EMBO J. 2003 Sep 1;22(17):4465-77 PMID: 12941698
  28. LY2109761, a novel transforming growth factor beta receptor type I and type II dual inhibitor, as a therapeutic approach to suppressing pancreatic cancer metastasis.
    Mol Cancer Ther. 2008 Apr;7(4):829-40 PMID: 18413796
  29. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis.
    Nat Med. 2007 Aug;13(8):952-61 PMID: 17660828
  30. Tumor-induced upregulation of Twist, Snail, and Slug represses the activity of the human VE-cadherin promoter.
    Arch Biochem Biophys. 2009 Feb;482(1-2):77-82 PMID: 19046938
  31. Generalized lacZ expression with the ROSA26 Cre reporter strain.
    Nat Genet. 1999 Jan;21(1):70-1 PMID: 9916792
  32. Loss of cerebral cavernous malformation 3 (Ccm3) in neuroglia leads to CCM and vascular pathology.
    Proc Natl Acad Sci U S A. 2011 Mar 1;108(9):3737-42 PMID: 21321212
  33. Tensional forces in fibrillar extracellular matrices control directional capillary sprouting.
    J Cell Sci. 1999 Oct;112 ( Pt 19):3249-58 PMID: 10504330
  34. Recent insights into cerebral cavernous malformations: a complex jigsaw puzzle under construction.
    FEBS J. 2010 Mar;277(5):1084-96 PMID: 20096036
  35. The cerebral cavernous malformation signaling pathway promotes vascular integrity via Rho GTPases.
    Nat Med. 2009 Feb;15(2):177-84 PMID: 19151728
  36. Transforming growth factor β signaling inhibitor, SB-431542, induces maturation of dendritic cells and enhances anti-tumor activity.
    Oncol Rep. 2010 Dec;24(6):1637-43 PMID: 21042762
  37. Genetics of cavernous angiomas.
    Lancet Neurol. 2007 Mar;6(3):237-44 PMID: 17303530
Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
Published
2013-06-27
Epub
2013-00-09
Pages
492-6
Language
English
Region
England
NLM ID
0410462
Subset
IM
Corrections
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com