Sulindac metabolites decrease cerebrovascular malformations in CCM3-knockout mice

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 27, 2015, Pages 8421-8426

  Bravi, Luca ^a   Rudini, Noemi ^a   Cuttano, Roberto ^a   Giampietro, Costanza ^a,b   Maddalunoa, Luigi ^a   Ferrarini, Luca ^a   Adams, Ralf H ^c   Corada, Monica ^a   Boulday, Gwenola ^d   Tournier Lasserve, Elizabeth ^d   Dejana, Elisabetta ^a,e   Lampugnani, Maria Grazia ^a,f   Dietz, Harry C ^g  

^a FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF MÜNSTER   (Germany)

^d INSERM   (France)

^e UPPSALA UNIVERSITY   (Sweden)

^f MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^g JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

? catenin; Cerebral cavernous malformation; Endothelial cells; Sulindac metabolites; Vascular pathology

Indexed keywords

BETA CATENIN; FRIZZLED PROTEIN; SULINDAC SULFIDE; SULINDAC SULFONE; TRANSFORMING GROWTH FACTOR BETA; NONSTEROID ANTIINFLAMMATORY AGENT; PDCD10 PROTEIN, MOUSE; SIGNAL PEPTIDE; SULINDAC;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CEREBROVASCULAR MALFORMATION; CONGENITAL BLOOD VESSEL MALFORMATION; CONTROLLED STUDY; ENDOTHELIUM CELL; EPITHELIAL MESENCHYMAL TRANSITION; IN VITRO STUDY; IN VIVO STUDY; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; VASCULAR LESION; ANALOGS AND DERIVATIVES; ANIMAL; CENTRAL NERVOUS SYSTEM NEOPLASMS; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HEMANGIOMA, CAVERNOUS, CENTRAL NERVOUS SYSTEM; IMMUNOHISTOCHEMISTRY; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

MURINAE; MUS;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BETA CATENIN; CENTRAL NERVOUS SYSTEM NEOPLASMS; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; HEMANGIOMA, CAVERNOUS, CENTRAL NERVOUS SYSTEM; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE, KNOCKOUT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SULINDAC; TRANSFORMING GROWTH FACTOR BETA;

EID: 84936870397     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1501352112     Document Type: Article

References (33)

1. Clatterbuck RE, Eberhart CG, Crain BJ, Rigamonti D (2001) Ultrastructural and immunocytochemical evidence that an incompetent blood-brain barrier is related to the pathophysiology of cavernous malformations. J Neurol Neurosurg Psychiatry 71(2): 188-192.
2. Rigamonti D, et al. (1988) Cerebral cavernous malformations. Incidence and familial occurrence. N Engl J Med 319(6):343-347.
3. Li DY, Whitehead KJ (2010) Evaluating strategies for the treatment of cerebral cavernous malformations. Stroke 41(Suppl 10):S92-S94.
4. Plummer NW, Zawistowski JS, Marchuk DA (2005) Genetics of cerebral cavernous malformations. Curr Neurol Neurosci Rep 5(5):391-396.
5. Boulday G, et al. (2011) Developmental timing of CCM2 loss influences cerebral cavernous malformations in mice. J Exp Med 208(9):1835-1847.
6. He Y, et al. (2010) Stabilization of VEGFR2 signaling by cerebral cavernous malformation 3 is critical for vascular development. Sci Signal 3(116):ra26.
7. Maddaluno L, et al. (2013) EndMT contributes to the onset and progression of cerebral cavernous malformations. Nature 498(7455):492-496.
8. Liebner S, et al. (2004) Beta-catenin is required for endothelial-mesenchymal transformation during heart cushion development in the mouse. J Cell Biol 166(3):359-367.
9. Glading AJ, Ginsberg MH (2010) Rap1 and its effector KRIT1/CCM1 regulate betacatenin signaling. Dis Model Mech 3(1-2):73-83.
10. DiStefano PV, Kuebel JM, Sarelius IH, Glading AJ (2014) KRIT1 protein depletion modifies endothelial cell behavior via increased vascular endothelial growth factor (VEGF) signaling. J Biol Chem 289(47):33054-33065.
11. Stenman JM, et al. (2008) Canonical Wnt signaling regulates organ-specific assembly and differentiation of CNS vasculature. Science 322(5905):1247-1250.
12. Daneman R, et al. (2009) Wnt/beta-catenin signaling is required for CNS, but not non- CNS, angiogenesis. Proc Natl Acad Sci USA 106(2):641-646.
13. Liebner S, et al. (2008) Wnt/beta-catenin signaling controls development of the blood-brain barrier. J Cell Biol 183(3):409-417.
14. Corada M, et al. (2010) The Wnt/beta-catenin pathway modulates vascular remodeling and specification by upregulating Dll4/Notch signaling. Dev Cell 18(6):938-949.
15. Liquori CL, et al. (2006) Low frequency of PDCD10 mutations in a panel of CCM3 probands: Potential for a fourth CCM locus. Hum Mutat 27(1):118.
16. Shenkar R, et al. (2015) Exceptional aggressiveness of cerebral cavernous malformation disease associated with PDCD10 mutations. Genet Med 17(3):188-196.
17. van NoortM, Meeldijk J, van der Zee R, Destree O, Clevers H (2002)Wnt signaling controls the phosphorylation status of beta-catenin. J Biol Chem 277(20):17901-17905.
18. Taddei A, et al. (2008) Endothelial adherens junctions control tight junctions by VEcadherin- mediated upregulation of claudin-5. Nat Cell Biol 10(8):923-934.
19. Fadini GP, Losordo D, Dimmeler S (2012) Critical reevaluation of endothelial progenitor cell phenotypes for therapeutic and diagnostic use. Circ Res 110(4):624-637.
20. Medici D, Kalluri R (2012) Endothelial-mesenchymal transition and its contribution to the emergence of stem cell phenotype. Semin Cancer Biol 22(5-6):379-384.
21. Clevers H, Nusse R (2012) Wnt/β-catenin signaling and disease. Cell 149(6):1192-1205.
22. Anastas JN, Moon RT (2013) WNT signalling pathways as therapeutic targets in cancer. Nat Rev Cancer 13(1):11-26.
23. Vleminckx K, Kemler R, Hecht A (1999) The C-terminal transactivation domain of beta-catenin is necessary and sufficient for signaling by the LEF-1/beta-catenin complex in Xenopus laevis. Mech Dev 81(1-2):65-74.
24. Gurpinar E, Grizzle WE, Piazza GA (2013) COX-independent mechanisms of cancer chemoprevention by anti-inflammatory drugs. Front Oncol 3:181.
25. Li N, et al. (2013) Sulindac selectively inhibits colon tumor cell growth by activating the cGMP/PKG pathway to suppress Wnt/β-catenin signaling. Mol Cancer Ther 12(9): 1848-1859.
26. Teiten MH, Gaascht F, Dicato M, Diederich M (2012) Targeting the wingless signaling pathway with natural compounds as chemopreventive or chemotherapeutic agents. Curr Pharm Biotechnol 13(1):245-254.
27. Glading A, Han J, Stockton RA, Ginsberg MH (2007) KRIT-1/CCM1 is a Rap1 effector that regulates endothelial cell cell junctions. J Cell Biol 179(2):247-254.
28. Lampugnani MG, et al. (2010) CCM1 regulates vascular-lumen organization by inducing endothelial polarity. J Cell Sci 123(Pt 7):1073-1080.
29. He XC, et al. (2004) BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-beta-catenin signaling. Nat Genet 36(10):1117-1121.
30. Polakis P (2012) Wnt signaling in cancer. Cold Spring Harb Perspect Biol 4(5):4.
31. Gurpinar E, Grizzle WE, Piazza GA (2014) NSAIDs inhibit tumorigenesis, but how? Clin Cancer Res 20(5):1104-1113.
32. Piazza GA, et al. (1997) Sulindac sulfone inhibits azoxymethane-induced colon carcinogenesis in rats without reducing prostaglandin levels. Cancer Res 57(14):2909-2915.
33. McDonald DA, et al. (2012) Fasudil decreases lesion burden in a murine model of cerebral cavernous malformation disease. Stroke 43(2):571-574.