The cerebral cavernous malformation proteins CCM2L and CCM2 prevent the activation of the MAP kinase MEKK3

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

Volumn 112, Issue 46, 2015, Pages 14284-14289

  Cullerea, Xavier ^a   Plovieb, Eva ^a   Bennetta, Paul M ^a   MacRaeb, Calum A ^a   Mayadasa, Tanya N ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Cerebral cavernous malformation; Endothelium; Expression; Map kinase; Signaling

Indexed keywords

CCM2 PROTEIN; CCM2L PROTEIN; CLAUDIN 5; KRUPPEL LIKE FACTOR 4; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE KINASE 5; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; REGULATOR PROTEIN; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; UNCLASSIFIED DRUG; CARRIER PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 7; MULTIPROTEIN COMPLEX; ZEBRAFISH PROTEIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; CAVERNOUS HEMANGIOMA; CELL DENSITY; EMBRYO; ENDOTHELIAL PROGENITOR CELL; ENZYME ACTIVATION; GENE DELETION; GENE INTERACTION; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION; ZEBRA FISH; ANIMAL; CARDIOMEGALY; CYTOLOGY; EMBRYOLOGY; ENDOTHELIUM CELL; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CARDIOMEGALY; CARRIER PROTEINS; ENDOTHELIAL CELLS; ENZYME ACTIVATION; GENE KNOCKDOWN TECHNIQUES; MAP KINASE KINASE KINASE 3; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 7; MULTIPROTEIN COMPLEXES; TRANSCRIPTION, GENETIC; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84963577686     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1510495112     Document Type: Article

References (36)

1. Fischer A, Zalvide J, Faurobert E, Albiges-Rizo C, Tournier-Lasserve E (2013) Cerebral cavernous malformations: From CCM genes to endothelial cell homeostasis. Trends Mol Med 19(5):302-308.
2. Fisher OS, Boggon TJ (2014) Signaling pathways and the cerebral cavernous malformation proteins: Lessons from structural biology. Cell Mol Life Sci 71(10):1881-1892.
3. Zheng X, et al. (2010) CCM3 signaling through sterile 20-like kinases plays an essential role during zebrafish cardiovascular development and cerebral cavernous malformations. J Clin Invest 120(8):2795-2804.
4. Yoruk B, Gillers BS, Chi NC, Scott IC (2012) Ccm3 functions in a manner distinct from Ccm1 and Ccm2 in a zebrafish model of CCM vascular disease. Dev Biol 362(2): 121-131.
5. Richardson BT, Dibble CF, Borikova AL, Johnson GL (2013) Cerebral cavernous malformation is a vascular disease associated with activated RhoA signaling. Biol Chem 394(1):35-42.
6. Zhu Y, et al. (2010) Differential angiogenesis function of CCM2 and CCM3 in cerebral cavernous malformations. Neurosurg Focus 29(3):E1.
7. Wüstehube J, et al. (2010) Cerebral cavernous malformation protein CCM1 inhibits sprouting angiogenesis by activating DELTA-NOTCH signaling. Proc Natl Acad Sci USA 107(28):12640-12645.
8. Maddaluno L, et al. (2013) EndMT contributes to the onset and progression of cerebral cavernous malformations. Nature 498(7455):492-496.
9. Renz M, et al. (2015) Regulation of β1 integrin-Klf2-mediated angiogenesis by CCM proteins. Dev Cell 32(2):181-190.
10. Zheng X, et al. (2012) Dynamic regulation of the cerebral cavernous malformation pathway controls vascular stability and growth. Dev Cell 23(2):342-355.
11. Rosen JN, Sogah VM, Ye LY, Mably JD (2013) ccm2-like is required for cardiovascular development as a novel component of the Heg-CCM pathway. Dev Biol 376(1):74-85.
12. Uhlik MT, et al. (2003) Rac-MEKK3-MKK3 scaffolding for p38 MAPK activation during hyperosmotic shock. Nat Cell Biol 5(12):1104-1110.
13. Drew BA, Burow ME, Beckman BS (2012) MEK5/ERK5 pathway: The first fifteen years. Biochim Biophys Acta 1825(1):37-48.
14. Yang J, et al. (2000) Mekk3 is essential for early embryonic cardiovascular development. Nat Genet 24(3):309-313.
15. Rose BA, Force T, Wang Y (2010) Mitogen-activated protein kinase signaling in the heart: Angels versus demons in a heart-breaking tale. Physiol Rev 90(4):1507-1546.
16. Boulday G, et al. (2009) Tissue-specific conditional CCM2 knockout mice establish the essential role of endothelial CCM2 in angiogenesis: Implications for human cerebral cavernous malformations. Dis Model Mech 2(3-4):168-177.
17. Boulday G, et al. (2011) Developmental timing of CCM2 loss influences cerebral cavernous malformations in mice. J Exp Med 208(9):1835-1847.
18. Taddei A, et al. (2008) Endothelial adherens junctions control tight junctions by VEcadherin-mediated up-regulation of claudin-5. Nat Cell Biol 10(8):923-934.
19. Gimbrone MA, Jr, Garcia-Cardena G (2013) Vascular endothelium, hemodynamics, and the pathobiology of atherosclerosis. Cardiovasc Pathol 22(1):9-15.
20. Wang X, et al. (2015) Structural insights into the molecular recognition between cerebral cavernous malformation 2 and mitogen-activated protein kinase kinase kinase 3. Structure 23(6):1087-1096.
21. Fritz A, et al. (2006) Phosphorylation of serine 526 is required for MEKK3 activity, and association with 14-3-3 blocks dephosphorylation. J Biol Chem 281(10):6236-6245.
22. Di Y, Li S, Wang L, Zhang Y, Dorf ME (2008) Homeostatic interactions between MEKK3 and TAK1 involved in NF-kappaB signaling. Cell Signal 20(4):705-713.
23. Cheng J, et al. (2005) Dimerization through the catalytic domain is essential for MEKK2 activation. J Biol Chem 280(14):13477-13482.
24. Matitau AE, Gabor TV, Gill RM, Scheid MP (2013) MEKK2 kinase association with 14-3-3 protein regulates activation of c-Jun N-terminal kinase. J Biol Chem 288(39): 28293-28302.
25. Matitau AE, Scheid MP (2008) Phosphorylation of MEKK3 at threonine 294 promotes 14-3-3 association to inhibit nuclear factor kappaB activation. J Biol Chem 283(19): 13261-13268.
26. Mably JD, et al. (2006) santa and valentine pattern concentric growth of cardiac myocardium in the zebrafish. Development 133(16):3139-3146.
27. Hammerschmidt M, Mullins MC (2002) Dorsoventral patterning in the zebrafish: Bone morphogenetic proteins and beyond. Pattern Formation in Zebrafish (Results and Problems in Cell Differentiation), ed Solnica-Krezel L (Springer, Berlin, Germany).
28. Mably JD, Mohideen MA, Burns CG, Chen JN, Fishman MC (2003) heart of glass regulates the concentric growth of the heart in zebrafish. Curr Biol 13(24):2138-2147.
29. Zhou Z, et al. (2015) The cerebral cavernous malformation pathway controls cardiac development via regulation of endocardial MEKK3 signaling and KLF expression. Dev Cell 32(2):168-180.
30. Hawkins TA, Cavodeassi F, Erdélyi F, Szabó G, Lele Z (2008) The small molecule Mek1/2 inhibitor U0126 disrupts the chordamesoderm-to-notochord transition in zebrafish. BMC Dev Biol 8:42.
31. Wu X, et al. (2004) Tissue-engineered microvessels on three-dimensional biodegradable scaffolds using human endothelial progenitor cells. Am J Physiol Heart Circ Physiol 287(2):H480-H487.
32. Bevilacqua MP, Pober JS, Wheeler ME, Cotran RS, Gimbrone MA, Jr (1985) Interleukin1 acts on cultured human vascular endothelium to increase the adhesion of polymorphonuclear leukocytes, monocytes, and related leukocyte cell lines. J Clin Invest 76(5): 2003-2011.
33. Dardik A, et al. (2005) Differential effects of orbital and laminar shear stress on endothelial cells. J Vasc Surg 41(5):869-880.
34. dela Paz NG, Walshe TE, Leach LL, Saint-Geniez M, D'Amore PA (2012) Role of shearstress-induced VEGF expression in endothelial cell survival. J Cell Sci 125(Pt 4): 831-843.
35. Ellinger-Ziegelbauer H, Brown K, Kelly K, Siebenlist U (1997) Direct activation of the stress-activated protein kinase (SAPK) and extracellular signal-regulated protein kinase (ERK) pathways by an inducible mitogen-activated protein kinase/ERK kinase kinase 3 (MEKK) derivative. J Biol Chem 272(5):2668-2674.
36. Asimaki A, et al. (2014) Identification of a new modulator of the intercalated disc in a zebrafish model of arrhythmogenic cardiomyopathy. Sci Transl Med 6(240):240ra74.