Cerebral cavernous malformation is a vascular disease associated with activated RhoA signaling

Biological Chemistry

Volumn 394, Issue 1, 2013, Pages 35-42

  Johnson, Gary L ^a   Richardson, Bryan T ^a   Dibblel, Christopher F ^a   Borikova, Asya L ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Actin dynamics; CCM; Cerebral cavernous malformation; RhoA; ROCK

Indexed keywords

ACTIN; CULLIN; FASUDIL; H 1152; LIM KINASE; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN PHOSPHATASE; OSMOSENSING SCAFFOLD PROTEIN MEKK3; PROTEASOME; PROTEIN; PROTEIN SMURF1; RHO ASSOCIATED COILED COIL FORMING KINASE; RHO KINASE; RHO KINASE INHIBITOR; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SIMVASTATIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; BLOOD VESSEL PERMEABILITY; CAVERNOUS HEMANGIOMA; CELL JUNCTION; CYTOSKELETON; DISEASE COURSE; ENDOTHELIUM CELL; ENZYME INHIBITION; GENE MUTATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; STRESS FIBER;

ANIMALS; HEMANGIOMA, CAVERNOUS, CENTRAL NERVOUS SYSTEM; HUMANS; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; VASCULAR DISEASES;

EID: 84876537947     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2012-0243     Document Type: Review

References (40)

1. Batra, S., Lin, D., Recinos, P.F., Zhang, J., and Rigamonti, D. (2009). Cavernous malformations: natural history, diagnosis and treatment. Nat. Rev. Neurol. 5, 659-670.
2. Borikova, A.L., Dibble, C.F., Sciaky, N., Welch, C.M., Abell, A.N., Bencharit, S., and Johnson, G.L. (2010). Rho kinase inhibition rescues the endothelial cell cerebral cavernous malformation phenotype. J. Biol. Chem. 285, 11760-11764.
3. Boulday, G., Bl é con, A., Petit, N., Chareyre, F., Garcia, L.A., Niwa-Kawakita, M., Giovannini, M., and Tournier-Lasserve, E. (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, 168-177.
4. Ceccarelli, D.F., Laister, R.C., Mulligan, V.K., Kean, M.J., Goudreault, M., Scott, I.C., Derry, W.B., Chakrabartty, A., Gingras, A.-C., and Sicheri, F. (2011). CCM3/PDCD10 heterodimerizes with germinal center kinase III (GCKIII) proteins using a mechanism analogous to CCM3 homodimerization. J. Biol. Chem. 286, 25056-25064.
5. Chan, A.C., Drakos, S.G., Ruiz, O.E., Smith, A.C.H., Gibson, C.C., Ling, J., Passi, S.F., Stratman, A.N., Sacharidou, A., Revelo, et al. (2011). Mutations in 2 distinct genetic pathways result in cerebral cavernous malformations in mice. J. Clin. Invest. 122, 1948.
6. Chen, Y., Yang, Z., Meng, M., Zhao, Y., Dong, N., Yan, H., Liu, L., Ding, M., Peng, H.B., and Shao, F. (2009). Cullin mediates degradation of RhoA through evolutionarily conserved BTB adaptors to control actin cytoskeleton structure and cell movement. Mol. Cell 35, 841-855.
7. Costa, B., Kean, M.J., Ast, V., Knight, J.D., Mett, A., Levy, Z., Ceccarelli, D.F., Badillo, B.G., Eils, R., Koenig, R., et al. (2012). Stk25 mediates TrkA and CCM2 dependent death in pediatric tumor cells of neural origin. J. Biol. Chem. 287, 29285-29289.
8. Crose, L.E.S., Hilder, T.L., Sciaky, N., and Johnson, G.L. (2009). Cerebral cavernous malformation 2 protein promotes smad ubiquitin regulatory factor 1-mediated RhoA degradation in endothelial cells. J. Biol. Chem. 284, 13301-13305.
9. Denier, C., Goutagny, S., Labauge, P., Krivosic, V., Arnoult, M., Cousin, A., Benabid, A.L., Comoy, J., Frerebeau, P., Gilbert, B., et al. (2004). Mutations within the MGC4607 gene cause cerebral cavernous malformations. Am. J. Hum. Genet. 74, 326-337. (Pubitemid 38168620)
10. Ding, F., Yin, Z., and Wang, H.-R. (2011). Ubiquitination in Rho signaling. Curr. Top. Med. Chem. 11, 2879-2887.
11. Faurobert, E. and Albiges-Rizo, C. (2010). Recent insights into cerebral cavernous malformations: a complex jigsaw puzzle under construction. FEBS J. 277, 1084-1096.
12. Fidalgo, M., Guerrero, A., Fraile, M., Iglesias, C., Pombo, C.M., and Zalvide, J. (2012). The adaptor protein cerebral cavernous malformation 3 (CCM3) mediates phosphorylation of the cytoskeletal proteins Ezrin/Radixin/Moesin by Mammalian Ste20-4 to protect cells from oxidative stress. J. Biol. Chem. 287, 11556-11565.
13. Glading, A., Han, J., Stockton, R.A., and Ginsberg, M.H. (2007). KRIT-1/CCM1 is a Rap1 effector that regulates endothelial cell-cell junctions. J. Cell Biol. 179, 247-254. (Pubitemid 350004889)
14. Guclu, B., Ozturk, A.K., Pricola, K.L., Bilguvar, K., Shin, D., O ' Roak, B.J., and Gunel, M. (2005). Mutations in apoptosis-related gene, PDCD10, cause cerebral cavernous malformation 3. Neurosurgery 57, 1008-1013.
15. Gunel, M., Awad, I.A., Finberg, K., Anson, J.A., Steinberg, G.K., Batjer, H.H., Kopitnik, T.A., Morrison, L., Giannotta, S.L., Nelson-Williams, C., et al. (1996). A founder mutation as a cause of cerebral cavernous malformation in Hispanic Americans. N. Engl. J. Med. 334, 946-951. (Pubitemid 26114160)
16. Hilder, T.L., Malone, M.H., Bencharit, S., Colicelli, J., Haystead, T.A., Johnson, G.L., and Wu, C.C. (2007). Proteomic identification of the cerebral cavernous malformation signaling complex. J. Proteome Res. 6, 4343-4355. (Pubitemid 350158510)
17. Jaffe, A.B. and Hall, A. (2005). Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21, 247-269. (Pubitemid 41740635)
18. Kleaveland, B., Zheng, X., Liu, J.J., Blum, Y., Tung, J.J., Zou, Z., Sweeney, S.M., Chen, M., Guo, L., Lu, M.-M., et al. (2009). Regulation of cardiovascular development and integrity by the heart of glass-cerebral cavernous malformation protein pathway. Nat. Med. 15, 169-176.
19. Knudson, A.G., Jr. (1971). Mutation and cancer: statistical study of retinoblastoma. Proc. Natl. Acad. Sci. USA 68, 820-823.
20. Labauge, P., Laberge, S., Brunereau, L., Levy, C., and Tournier-Lasserve, E. (1998). Hereditary cerebral cavernous angiomas: clinical and genetic features in 57 French families. Societe Francaise de Neurochirurgie. Lancet 352, 1892-1897. (Pubitemid 28561250)
21. Laberge-le Couteulx, S., Jung, H.H., Labauge, P., Houtteville, J.P., Lescoat, C., Cecillon, M., Marechal, E., Joutel, A., Bach, J.F., and Tournier-Lasserve, E. (1999). Truncating mutations in CCM1, encoding KRIT1, cause hereditary cavernous angiomas. Nat. Genet. 23, 189-193. (Pubitemid 29455391)
22. Lampugnani, M.G., Orsenigo, F., Rudini, N., Maddaluno, L., Boulday, G., Chapon, F., and Dejana, E. (2010). CCM1 regulates vascular-lumen organization by inducing endothelial polarity. J. Cell Sci. 123, 1073-1080.
23. Li, X., Zhang, R., Zhang, H., He, Y., Ji, W., Min, W., and Boggon, T.J. (2010). Crystal structure of CCM3, a cerebral cavernous malformation protein critical for vascular integrity. J. Biol. Chem. 285, 24099-240107.
24. Liquori, C.L., Berg, M.J., Siegel, A.M., Huang, E., Zawistowski, J.S., Stoffer, T.P., Verlaan, D., Balogun, F., Hughes, L., Leedom, T.P., et al. (2003). Mutations in a gene encoding a novel protein containing a phosphotyrosine-binding domain cause type 2 cerebral cavernous malformations. Am. J. Hum. Genet. 73, 1459-1464. (Pubitemid 38037437)
25. Louvi, A., Chen, L., Two, A.M., Zhang, H., Min, W., and G ü nel, M. (2011). Loss of cerebral cavernous malformation 3 (Ccm3) in neuroglia leads to CCM and vascular pathology. Proc. Natl. Acad. Sci. USA 108, 3737-3742.
26. Pagenstecher, A., Stahl, S., Sure, U., and Felbor, U. (2009). A two-hit mechanism causes cerebral cavernous malformations: complete inactivation of CCM1, CCM2 or CCM3 in affected endothelial cells. Hum. Mol. Genet. 18, 911-918.
27. Ridley, A.J. and Hall, A. (1992). The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399.
28. Riento, K. and Ridley, A.J. (2003). Rocks: multifunctional kinases in cell behaviour. Nat. Rev. Mol. Cell Biol. 4, 446-456. (Pubitemid 36648590)
29. Robinson, J.R., Awad, I.A., and Little, J.R. (1991). Natural history of the cavernous angioma. J. Neurosurg. 75, 709-714.
30. Stahl, S., Gaetzner, S., Voss, K., Brackertz, B., Schleider, E., Surucu, O., Kunze, E., Netzer, C., Korenke, C., Finckh, U., et al. (2008). Novel CCM1, CCM2, and CCM3 mutations in patients with cerebral cavernous malformations: in-frame deletion in CCM2 prevents formation of a CCM1/CCM2/CCM3 protein complex. Hum. Mutat. 29, 709-717. (Pubitemid 351614596)
31. Stockton, R.A., Shenkar, R., Awad, I.A., and Ginsberg, M.H. (2010). Cerebral cavernous malformations proteins inhibit Rho kinase to stabilize vascular integrity. J. Exp. Med. 207, 881-896.
32. Surma, M., Wei, L., and Shi, J. (2011). Rho kinase as a therapeutic target in cardiovascular disease. Future Cardiol. 7, 657-671.
33. Suzuki, Y., Shibuya, M., Satoh, S., Sugimoto, Y., and Takakura, K. (2007). A postmarketing surveillance study of fasudil treatment after aneurysmal subarachnoid hemorrhage. Surg. Neurol. 68, 126-131; discussion 131-122. (Pubitemid 47087900)
34. Takemoto, M. and Liao, J.K. (2001). Pleiotropic effects of 3-hydroxy-3-methylglutaryl coenzyme a reductase inhibitors. Arterioscler. Thromb. Vasc. Biol. 21, 1712-1719. (Pubitemid 34219772)
35. Uhlik, M.T., Abell, A.N., Johnson, N.L., Sun, W., Cuevas, B.D., Lobel-Rice, K.E., Horne, E.A., Dell ' Acqua, M.L., and Johnson, G.L. (2003). Rac-MEKK3-MKK3 scaffolding for p38 MAPK activation during hyperosmotic shock. Nat. Cell Biol. 5, 1104-1110. (Pubitemid 37509118)
36. Wang, H.-R., Zhang, Y., Ozdamar, B., Ogunjimi, A.A., Alexandrova, E., Thomsen, G.H., and Wrana, J.L. (2003). Regulation of cell polarity and protrusion formation by targeting RhoA for degradation. Science 302, 1775-1779. (Pubitemid 37505743)
37. Watanabe, N., Kato, T., Fujita, A., Ishizaki, T., and Narumiya, S. (1999). Cooperation between mDia1 and ROCK in Rho-induced actin reorganization. Nat. Cell Biol. 1, 136-143. (Pubitemid 129656017)
38. Whitehead, K.J., Chan, A.C., Navankasattusas, S., Koh, W., London, N.R., Ling, J., Mayo, A.H., Drakos, S.G., Jones, C.A., Zhu, W., et al. (2009). The cerebral cavernous malformation signaling pathway promotes vascular integrity via Rho GTPases. Nat. Med. 15, 177-184.
39. Zawistowski, J.S., Stalheim, L., Uhlik, M.T., Abell, A.N., Ancrile, B.B., Johnson, G.L., and Marchuk, D.A. (2005). CCM1 and CCM2 protein interactions in cell signaling: implications for cerebral cavernous malformations pathogenesis. Hum. Mol. Genet. 14, 2521-2531. (Pubitemid 41236065)
40. Zheng, X., Xu, C., Di Lorenzo, A., Kleaveland, B., Zou, Z., Seiler, C., Chen, M., Cheng, L., Xiao, J., He, J., 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, 2795-2804.