Deletion of Rbpj from postnatal endothelium leads to abnormal arteriovenous shunting in mice

Development (Cambridge)

Volumn 141, Issue 19, 2014, Pages 3782-3792

  Nielsen, Corinne M ^a   Cuervo, Henar ^a   Ding, Vivianne W ^a   Kong, Yupeng ^a   Huang, Eric J ^a   Wang, Rong A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Arteriovenous; Cerebrovascular; Endothelial cell; Mouse; Notch; Rbpj

Indexed keywords

TRANSFORMING GROWTH FACTOR BETA; EPHB4 PROTEIN, MOUSE; EPHRIN RECEPTOR B4; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE BINDING PROTEIN; NOTCH RECEPTOR; RBPJ PROTEIN, MOUSE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ARTERIOVENOUS MALFORMATION; BRAIN BLOOD VESSEL; BRAIN PARENCHYMA; BRAIN TISSUE; CEREBELLUM; CLINICAL FEATURE; CONTROLLED STUDY; ENDOTHELIUM; GENE; GENE DELETION; GENE EXPRESSION; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MORPHOGENESIS; MOUSE; MUTANT; NONHUMAN; PARENCHYMA; PERINATAL PERIOD; RBPJ GENE; TISSUE PERFUSION; TRANSGENE; ANIMAL; ARTERIOVENOUS MALFORMATION; DEFICIENCY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION PROFILING; GENETICS; IMAGE PROCESSING; METABOLISM; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM;

ANIMALS; ARTERIOVENOUS MALFORMATIONS; ENDOTHELIUM, VASCULAR; GENE DELETION; GENE EXPRESSION PROFILING; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE-BINDING PROTEIN; MICE; MICROSCOPY, FLUORESCENCE; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, EPHB4; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 84908102195     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.108951     Document Type: Article

References (61)

1. Achrol, A. S., Guzman, R., Varga, M., Adler, J. R., Steinberg, G. K. and Chang, S. D. (2009). Pathogenesis and radiobiology of brain arteriovenous malformations: implications for risk stratification in natural history and posttreatment course. Neurosurg. Focus 26, E9.
2. Acker, T., Beck, H. and Plate, K. H. (2001). Cell type specific expression of vascular endothelial growth factor and angiopoietin-1 and -2 suggests an important role of astrocytes in cerebellar vascularization. Mech. Dev. 108, 45-57.
3. Blokzijl, A., Dahlqvist, C., Reissmann, E., Falk, A., Moliner, A., Lendahl, U. and Ibanez, C. F. (2003). Cross-talk between the Notch and TGF-β signaling pathways mediated by interaction of the Notch intracellular domain with Smad3. J. Cell Biol. 163, 723-728.
4. Carlson, T. R., Yan, Y., Wu, X., Lam, M. T., Tang, G. L., Beverly, L. J., Messina, L. M., Capobianco, A. J., Werb, Z. and Wang, R. (2005). Endothelial expression of constitutively active Notch4 elicits reversible arteriovenous malformations in adult mice. Proc. Natl. Acad. Sci. USA 102, 9884-9889.
5. Copeland, J. N., Feng, Y., Neradugomma, N. K., Fields, P. E. and Vivian, J. L. (2011). Notch signaling regulates remodeling and vessel diameter in the extraembryonic yolk sac. BMC Dev. Biol. 11, 12.
6. Corti, P., Young, S., Chen, C.-Y., Patrick, M. J., Rochon, E. R., Pekkan, K. and Roman, B. L. (2011). Interaction between alk1 and blood flow in the development of arteriovenous malformations. Development 138, 1573-1582.
7. Davy, A. and Soriano, P. (2007). Ephrin-B2 forward signaling regulates somite patterning and neural crest cell development. Dev. Biol. 304, 182-193.
8. Dong, C., Zhu, S., Wang, T., Yoon, W. and Goldschmidt-Clermont, P. J. (2002). Upregulation of PAI-1 is mediated through TGF-β/Smad pathway in transplant arteriopathy. J. Heart Lung Transplant. 21, 999-1008.
9. Dou, G.-R., Wang, Y.-C., Hu, X.-B., Hou, L.-H., Wang, C.-M., Xu, J.-F., Wang, Y.-S., Liang, Y.-M., Yao, L.-B., Yang, A.-G. et al. (2008). RBP-J, the transcription factor downstream of Notch receptors, is essential for the maintenance of vascular homeostasis in adult mice. FASEB J. 22, 1606-1617.
10. Ehling, M., Adams, S., Benedito, R. and Adams, R. H. (2013). Notch controls retinal blood vessel maturation and quiescence. Development 140, 3051-3061.
11. Fleetwood, I. G. and Steinberg, G. K. (2002). Arteriovenous malformations. Lancet 359, 863-873.
12. Friedlander, R. M. (2007). Arteriovenous malformations of the brain. N. Engl. J. Med. 356, 2704-2712.
13. Friedman, W. A. (2013). Stereotactic radiosurgery of intracranial arteriovenous malformations. Neurosurg. Clin. N. Am. 24, 561-574.
14. Gerety, S. S., Wang, H. U., Chen, Z.-F. and Anderson, D. J. (1999). Symmetrical mutant phenotypes of the receptor EphB4 and its specific transmembrane ligand ephrin-B2 in cardiovascular development. Mol. Cell 4, 403-414.
15. Hassed, S. J., Wiley, G. B., Wang, S., Lee, J.-Y., Li, S., Xu, W., Zhao, Z. J., Mulvihill, J. J., Robertson, J., Warner, J. et al. (2012). RBPJ mutations identified in two families affected by Adams-Oliver syndrome. Am. J. Hum. Genet. 91, 391-395.
16. Hofmeister, C., Stapf, C., Hartmann, A., Sciacca, R. R., Mansmann, U., terBrugge, K., Lasjaunias, P., Mohr, J. P., Mast, H. and Meisel, J. (2000). Demographic, morphological, and clinical characteristics of 1289 patients with brain arteriovenous malformation. Stroke 31, 1307-1310.
17. Johnson, D. W., Berg, J. N., Baldwin, M. A., Gallione, C. J., Marondel, I., Yoon, S.-J., Stenzel, T. T., Speer, M., Pericak-Vance, M. A., Diamond, A. et al. (1996). Mutations in the activin receptor-like kinase 1 gene in hereditary haemorrhagic telangiectasia type 2. Nat. Genet. 13, 189-195.
18. Kim, Y. H., Hu, H., Guevara-Gallardo, S., Lam, M. T. Y., Fong, S.-Y. and Wang, R.A. (2008). Artery and vein size is balanced by Notch and ephrin B2/EphB4 during angiogenesis. Development 135, 3755-3764.
19. Kim, J.-H., Peacock, M. R., George, S. C. and Hughes, C. C. W. (2012). BMP9 induces EphrinB2 expression in endothelial cells through an Alk1-BMPRII/ActRIIID1/ ID3-dependent pathway: implications for hereditary hemorrhagic telangiectasia type II. Angiogenesis 15, 497-509.
20. Krebs, L. T., Xue, Y., Norton, C. R., Shutter, J. R., Maguire, M., Sundberg, J. P., Gallahan, D., Closson, V., Kitajewski, J., Callahan, R. et al. (2000). Notch signaling is essential for vascular morphogenesis in mice. Genes Dev. 14, 1343-1352.
21. Krebs, L. T., Shutter, J. R., Tanigaki, K., Honjo, T., Stark, K. L. and Gridley, T. (2004). Haploinsufficient lethality and formation of arteriovenous malformations in Notch pathway mutants. Genes Dev. 18, 2469-2473.
22. Krebs, L. T., Starling, C., Chervonsky, A. V. and Gridley, T. (2010). Notch1 activation in mice causes arteriovenous malformations phenocopied by ephrinB2 and EphB4 mutants. Genesis 48, 146-150.
23. Larrivée, B., Prahst, C., Gordon, E., del Toro, R., Mathivet, T., Duarte, A., Simons, M. and Eichmann, A. (2012). ALK1 signaling inhibits angiogenesis by cooperating with the Notch pathway. Dev. Cell 22, 489-500.
24. Lawson, N. D., Scheer, N., Pham, V. N., Kim, C. H., Chitnis, A. B., Campos- Ortega, J. A. and Weinstein, B. M. (2001). Notch signaling is required for arterialvenous differentiation during embryonic vascular development. Development 128, 3675-3683.
25. Lawson, N. D., Vogel, A. M. and Weinstein, B. M. (2002). Sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Dev. Cell 3, 127-136.
26. Lawton, M. T. (2014). Seven AVMs: Tenets and Techniques for Resection, p. 352. New York: Thieme Medical Publishers.
27. Lee, J. H. (2013). Complete reduction with traction of the infraorbital neurovascular bundle in a delayed case of white-eyed blow-out fracture. J. Craniofac. Surg. 25, e54-55.
28. Li, Z., Feng, L., Wang, C.-M., Zheng, Q.-J., Zhao, B.-J., Yi, W., Zhang, J.-Z., Wang, Y.-M., Guo, H.-T., Yi, D.-H. et al. (2012). Deletion of RBP-J in adult mice leads to the onset of aortic valve degenerative diseases. Mol. Biol. Rep. 39, 3837-3845.
29. Limbourg, F. P., Takeshita, K., Radtke, F., Bronson, R. T., Chin, M. T. and Liao, J. K. (2005). Essential role of endothelial Notch1 in angiogenesis. Circulation 111, 1826-1832.
30. McAllister, K. A., Grogg, K. M., Johnson, D. W., Gallione, C. J., Baldwin, M. A., Jackson, C. E., Helmbold, E. A., Markel, D. S., McKinnon, W. C., Murrell, J. et al. (1994). Endoglin, a TGF-beta binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nat. Genet. 8, 345-351.
31. Meyer-Heim, A. D. and Boltshauser, E. (2003). Spontaneous intracranial haemorrhage in children: aetiology, presentation and outcome. Brain Dev. 25, 416-421.
32. Miniati, D., Jelin, E. B., Ng, J., Wu, J., Carlson, T. R., Wu, X., Looney, M. R. and Wang, R. A. (2010). Constitutively active endothelial Notch4 causes lung arteriovenous shunts in mice. Am. J. Physiol. Lung Cell Mol. Physiol. 298, L169-L177.
33. Murphy, P. A., Lam, M. T. Y., Wu, X., Kim, T. N., Vartanian, S. M., Bollen, A. W., Carlson, T. R. and Wang, R. A. (2008). Endothelial Notch4 signaling induces hallmarks of brain arteriovenous malformations in mice. Proc. Natl. Acad. Sci. USA 105, 10901-10906.
34. Murphy, P. A., Lu, G., Shiah, S., Bollen, A.W. and Wang, R. A. (2009). Endothelial Notch signaling is upregulated in human brain arteriovenous malformations and a mouse model of the disease. Lab. Invest. 89, 971-982.
35. Murphy, P. A., Kim, T. N., Lu, G., Bollen, A. W., Schaffer, C. B. and Wang, R. A. (2012). Notch4 normalization reduces blood vessel size in arteriovenous malformations. Sci. Transl. Med. 4, 117-8.
36. Murray, A. L., Dally, M., Jeffreys, A., Hwang, P. and Anderson, J. F. (2013). Neuropsychological outcomes of stereotactic radiotherapy for cerebral arteriovenous malformations. J. Clin. Neurosci. 21, 601-606.
37. Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L. and Luo, L. (2007). A global double-fluorescent Cre reporter mouse. Genesis 45, 593-605.
38. Nielsen, C. M. and Dymecki, S. M. (2010). Sonic hedgehog is required for vascular outgrowth in the hindbrain choroid plexus. Dev. Biol. 340, 430-437.
39. Park, S. O., Lee, Y. J., Seki, T., Hong, K.-H., Fliess, N., Jiang, Z., Park, A., Wu, X., Kaartinen, V., Roman, B. L. et al. (2008). ALK5- and TGFBR2-independent role of ALK1 in the pathogenesis of hereditary hemorrhagic telangiectasia type 2. Blood 111, 633-642.
40. Park, S. O., Wankhede, M., Lee, Y. J., Choi, E. J., Fliess, N., Choe, S. W., Oh, S. H., Walter, G., Raizada, M. K., Sorg, B. S. et al. (2009). Real-time imaging of de novo arteriovenous malformation in a mouse model of hereditary hemorrhagic telangiectasia. J. Clin. Invest. 119, 3487-3496.
41. Pitulescu, M. E., Schmidt, I., Benedito, R. and Adams, R. H. (2010). Inducible gene targeting in the neonatal vasculature and analysis of retinal angiogenesis in mice. Nat. Protoc. 5, 1518-1534.
42. Quillien, A., Moore, J. C., Shin, M., Siekmann, A. F., Smith, T., Pan, L., Moens, C. B., Parson, M. J. and Lawson, N. D. (2014). Distinct Notch signaling outputs pattern the developing arterial system. Development 141, 1544-1552.
43. Selever, J., Kong, J.-Q. and Arenkiel, B. R. (2011). A rapid approach to highresolution fluorescence imaging in semi-thick brain slices. J. Vis. Exp. pe2807.
44. Sorensen, I., Adams, R. H. and Gossler, A. (2009). DLL1-mediated Notch activation regulates endothelial identity in mouse fetal arteries. Blood 113, 5680-5688.
45. Takamoto, N., You, L.-R., Moses, K., Chiang, C., Zimmer, W. E., Schwartz, R. J., DeMayo, F. J., Tsai, M.-J. and Tsai, S. Y. (2005). COUP-TFII is essential for radial and anteroposterior patterning of the stomach. Development 132, 2179-2189.
46. Tanigaki, K., Han, H., Yamamoto, N., Tashiro, K., Ikegawa, M., Kuroda, K., Suzuki, A., Nakano, T. and Honjo, T. (2002). Notch-RBP-J signaling is involved in cell fate determination of marginal zone B cells. Nat. Immunol. 3, 443-450.
47. The Arteriovenous Malformation Study Group. (1999). Arteriovenous malformations of the brain in adults. N. Engl. J. Med. 340, 1812-1818.
48. Thurston, G. and Yancopoulos, G. D. (2001). Developmental biology: gridlock in the blood. Nature 414, 163-164.
49. Urness, L. D., Sorensen, L. K. and Li, D. Y. (2000). Arteriovenous malformations in mice lacking activin receptor-like kinase-1. Nat. Genet. 26, 328-331.
50. Villa, N., Walker, L., Lindsell, C. E., Gasson, J., Iruela-Arispe, M. L. and Weinmaster, G. (2001). Vascular expression of Notch pathway receptors and ligands is restricted to arterial vessels. Mech. Dev. 108, 161-164.
51. Wang, D.-B., Blocher, N. C., Spence, M. E., Rovainen, C. M. and Woolsey, T. A. (1992). Development and remodeling of cerebral blood vessels and their flow in postnatal mice observed with in vivo videomicroscopy. J. Cereb. Blood Flow Metab. 12, 935-946.
52. Wang, H. U., Chen, Z.-F. and Anderson, D. J. (1998). Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin- B2 and its receptor Eph-B4. Cell 93, 741-753.
53. Wang, L., Wang, C.-M., Hou, L.-H., Dou, G.-R., Wang, Y.-C., Hu, X.-B., He, F., Feng, F., Zhang, H.-W., Liang, Y.-M. et al. (2009). Disruption of the transcription factor recombination signal-binding protein-Jkappa (RBP-J) leads to venoocclusive disease and interfered liver regeneration in mice. Hepatology 49, 268-277.
54. Wang, Y., Nakayama, M., Pitulescu, M. E., Schmidt, T. S., Bochenek, M. L., Sakakibara, A., Adams, S., Davy, A., Deutsch, U., Lüthi, U. et al. (2010). Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature 465, 483-486.
55. Yao, Y., Yao, J., Radparvar, M., Blazquez-Medela, A. M., Guihard, P. J., Jumabay, M. and Bostrom, K. I. (2013). Reducing Jagged 1 and 2 levels prevents cerebral arteriovenous malformations in matrix Gla protein deficiency. Proc. Natl. Acad. Sci. USA 110, 19071-19076.
56. You, L.-R., Lin, F.-J., Lee, C. T., DeMayo, F. J., Tsai, M.-J. and Tsai, S. Y. (2005). Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity. Nature 435, 98-104.
57. Young, W. L. and Yang, G.-Y. (2004). Are there genetic influences on sporadic brain arteriovenous malformations? Stroke 35, 2740-2745.
58. Zacest, A. C., Caon, J., Roos, D. E., Potter, A. E. and Sullivan, T. (2013). LINAC radiosurgery for cerebral arteriovenous malformations: a single centre prospective analysis and review of the literature. J. Clin. Neurosci. 21, 241-245.
59. Zhong, T. P., Childs, S., Leu, J. P. and Fishman, M. C. (2001). Gridlock signalling pathway fashions the first embryonic artery. Nature 414, 216-220.
60. Zhou, L., Sohet, F. and Daneman, R. (2014). Purification of endothelial cells from rodent brain by immunopanning. Cold Spring Harb. Protoc. 2014, 65-77.
61. ZhuGe, Q., Zhong, M., Zheng, W., Yang, G.-Y., Mao, X., Xie, L., Chen, G., Chen, Y., Lawton, M. T., Young, W. L. et al. (2009). Notch-1 signalling is activated in brain arteriovenous malformations in humans. Brain 132, 3231-3241.