Functional characterization of Klippel-Trenaunay syndrome gene AGGF1 identifies a novel angiogenic signaling pathway for specification of vein differentiation and angiogenesis during embryogenesis

Human Molecular Genetics

Volumn 22, Issue 5, 2013, Pages 963-976

  Chen, Di ^a,b   Li, Lei ^a   Tu, Xin ^a,b   Yin, Zhan ^a,c   Wang, Qing ^a,b,d  

^a BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c INSTITUTE OF HYDROBIOLOGY   (China)

^d LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENIC FACTOR; ANGIOGENIC FACTOR WITH G PATCH AND FORKHEAD ASSOCIATED DOMAIN 1 PROTEIN; CD11B ANTIGEN; EPHRIN RECEPTOR B4; FORKHEAD TRANSCRIPTION FACTOR; MESSENGER RNA; NOTCH5 RECEPTOR; PROTEIN KINASE B; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 3;

ANGIOGENESIS; ANGIOOSTEOHYPERTROPHY SYNDROME; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL FATE; DOWN REGULATION; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVATION; GENE OVEREXPRESSION; GENE SILENCING; IN VIVO STUDY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; UPREGULATION; VEIN DIAMETER; ZEBRA FISH;

ANGIOGENIC PROTEINS; ANIMALS; CELL DIFFERENTIATION; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; KLIPPEL-TRENAUNAY-WEBER SYNDROME; NEOVASCULARIZATION, PHYSIOLOGIC; ONCOGENE PROTEIN V-AKT; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3; VEINS; ZEBRAFISH;

EID: 84873457790     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds501     Document Type: Article

References (53)

1. Wang, Q.K. (2005) Update on the molecular genetics of vascular anomalies. Lymphat. Res. Biol., 3, 226-233.
2. Jacob, A.G., Driscoll, D.J., Shaughnessy, W.J., Stanson, A.W., Clay, R.P. and Gloviczki, P. (1998) Klippel-Trenaunay syndrome: spectrum and management. Mayo Clin. Proc., 73, 28-36.
3. Timur, A.A., Sadgephour, A., Graf, M., Schwartz, S., Libby, E.D., Driscoll, D.J. and Wang, Q. (2004) Identification and molecular characterization of a de novo supernumerary ring chromosome 18 in a patient with Klippel-Trenaunay syndrome. Ann. Hum. Genet., 68, 353-361.
4. Timur, A.A., Driscoll, D.J. and Wang, Q. (2005) Biomedicine and diseases: the Klippel-Trenaunay syndrome, vascular anomalies and vascular morphogenesis. Cell Mol. Life Sci., 62, 1434-1447.
5. Wang, Q., Timur, A.A., Szafranski, P., Sadgephour, A., Jurecic, V., Cowell, J., Baldini, A. and Driscoll, D.J. (2001) Identification and molecular characterization of de novo translocation t(8;14)(q22.3;q13) associated with a vascular and tissue overgrowth syndrome. Cytogenet. Cell Genet., 95, 183-188.
6. Whelan, A.J., Watson, M.S., Porter, F.D. and Steiner, R.D. (1995) Klippel-Trenaunay-Weber syndrome associated with a 5:11 balanced translocation. Am. J. Med Genet., 59, 492-494.
7. Tian, X.L., Kadaba, R., You, S.A., Liu, M., Timur, A.A., Yang, L., Chen, Q., Szafranski, P., Rao, S. and Wu, L. et al. (2004) Identification of an angiogenic factor that when mutated causes susceptibility to Klippel- Trenaunay syndrome. Nature, 427, 640-645.
8. Hu, Y., Li, L., Seidelmann, S.B., Timur, A.A., Shen, P.H., Driscoll, D.J. and Wang, Q.K. (2008) Identification of association of common AGGF1 variants with susceptibility for Klippel-Trenaunay syndrome using the structure association program. Ann. Hum. Genet., 72, 636-643.
9. Fan, C., Ouyang, P., Timur, A.A., He, P., You, S.A., Hu, Y., Ke, T., Driscoll, D.J., Chen, Q. and Wang, Q.K. (2009) Novel roles of GATA1 in regulation of angiogenic factor AGGF1 and endothelial cell function. J. Biol. Chem., 284, 23331-23343.
10. Carmeliet, P. (2003) Angiogenesis in health and disease. Nat. Med., 9, 653-660.
11. Aitsebaomo, J., Portbury, A.L., Schisler, J.C. and Patterson, C. (2008) Brothers and sisters: molecular insights into arterial-venous heterogeneity. Circ. Res., 103, 929-939.
12. Kume, T. (2010) Specification of arterial, venous, and lymphatic endothelial cells during embryonic development Histol. Histopathol., 25, 637-646.
13. Lawson, N.D. and Weinstein, B.M. (2002) Arteries and veins: making a difference with zebrafish. Nat. Rev. Genet., 3, 674-682.
14. Rocha, S.F. and Adams, R.H. (2009) Molecular differentiation and specialization of vascular beds. Angiogenesis, 12, 139-147.
15. Swift, M.R. and Weinstein, B.M. (2009) Arterial-venous specification during development. Circ. Res., 104, 576-588.
16. Yamashita, J.K. (2007) Differentiation of arterial, venous, and lymphatic endothelial cells from vascular progenitors. Trends Cardiovasc. Med., 17, 59-63.
17. Lamont, R.E. and Childs, S. (2006) MAPping out arteries and veins. Sci. STKE., 2006, e39.
18. Hong, C.C., Peterson, Q.P., Hong, J.Y. and Peterson, R.T. (2006) Artery/ vein specification is governed by opposing phosphatidylinositol-3 kinase and MAP kinase/ERK signaling. Curr. Biol., 16, 1366-1372.
19. Hong, C.C., Kume, T. and Peterson, R.T. (2008) Role of crosstalk between phosphatidylinositol 3-kinase and extracellular signal-regulated kinase/mitogen-activated protein kinase pathways in artery-vein specification. Circ. Res., 103, 573-579.
20. Ren, B., Deng, Y., Mukhopadhyay, A., Lanahan, A.A., Zhuang, Z.W., Moodie, K.L., Mulligan-Kehoe, M.J., Byzova, T.V., Peterson, R.T. and Simons, M. (2010) ERK1/2-Akt1 crosstalk regulates arteriogenesis in mice and zebrafish. J. Clin. Invest., 120, 1217-1228.
21. 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.
22. Baskerville, P.A., Ackroyd, J.S. and Browse, N.L. (1985) The etiology of the Klippel-Trenaunay syndrome. Ann. Surg., 202, 624-627.
23. Cohen, M.M. Jr. (2000) Klippel-Trenaunay syndrome. Am. J. Med. Genet., 93, 171-175.
24. Klippel, M. and Trenaunay, P. (1900) Du naevus variqueux osteohypertrophique. Arch. Gen. Med., 185, 641-672.
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. Williams, C., Kim, S.H., Ni, T.T., Mitchell, L., Ro, H., Penn, J.S., Baldwin, S.H., Solnica-Krezel, L. and Zhong, T.P. (2010) Hedgehog signaling induces arterial endothelial cell formation by repressing venous cell fate. Dev. Biol., 341, 196-204.
27. Lu, Q., Yao, Y., Yao, Y., Liu, S., Huang, Y., Lu, S., Bai, Y., Zhou, B., Xu, Y., Li, L. et al. (2012) Angiogenic factor AGGF1 promotes therapeutic angiogenesis in a mouse limb ischemia model. PLoS One, 7, e46998.
28. Komsuoglu, B., Goldeli, O., Kulan, K., Cetinarslan, B. and Komsuoglu, S.S. (1994) Prevalence and risk factors of varicose veins in an elderly population. Gerontology, 40, 25-31.
29. John, A.R., Bramhall, S.R. and Eggo, M.C. (2008) Antiangiogenic therapy and surgical practice. Br. J. Surg., 95, 281-293.
30. Nagy, J.A., Chang, S.H., Shih, S.C., Dvorak, A.M. and Dvorak, H.F. (2010) Heterogeneity of the tumor vasculature. Semin. Thromb. Hemost., 36, 321-331.
31. Gale, N.W., Baluk, P., Pan, L., Kwan, M., Holash, J., DeChiara, T.M., McDonald, D.M. and Yancopoulos, G.D. (2001) Ephrin-B2 selectively marks arterial vessels and neovascularization sites in the adult, with expression in both endothelial and smooth-muscle cells. Dev. Biol., 230, 151-160.
32. Shin, D., Garcia-Cardena, G., Hayashi, S., Gerety, S., Asahara, T., Stavrakis, G., Isner, J., Folkman, J., Gimbrone, M.A. Jr. and Anderson, D.J. (2001) Expression of ephrinB2 identifies a stable genetic difference between arterial and venous vascular smooth muscle as well as endothelial cells, and marks subsets of microvessels at sites of adult neovascularization. Dev. Biol., 230, 139-150.
33. Rodriguez, F., Vacaru, A., Overvoorde, J. and den, H.J. (2008) The receptor protein-tyrosine phosphatase, Dep1, acts in arterial/venous cell fate decisions in zebrafish development. Dev. Biol., 324, 122-130.
34. Hogan, B.M., Bos, F.L., Bussmann, J., Witte, M., Chi, N.C., Duckers, H.J. and Schulte-Merker, S. (2009) Ccbe1 is required for embryonic lymphangiogenesis and venous sprouting. Nat. Genet., 41, 396-398.
35. Choi, J., Dong, L., Ahn, J., Dao, D., Hammerschmidt, M. and Chen, J.N. (2007) FoxH1 negatively modulates flk1 gene expression and vascular formation in zebrafish. Dev. Biol., 304, 735-744.
36. Westerfield, M. (2000) The zebrafish book. The University of Oregon Press, Eugene, Oregon.
37. Hyatt, T.M. and Ekker, S.C. (1999) Vectors and techniques for ectopic gene expression in zebrafish. Methods Cell Biol., 59, 117-126.
38. Chan, J., Bayliss, P.E., Wood, J.M. and Roberts, T.M. (2002) Dissection of angiogenic signaling in zebrafish using a chemical genetic approach. Cancer Cell, 1, 257-267.
39. Klippel, A., Reinhard, C., Kavanaugh, W.M., Apell, G., Escobedo, M.A. and Williams, L.T. (1996) Membrane localization of phosphatidylinositol 3-kinase is sufficient to activate multiple signal-transducing kinase pathways. Mol. Cell Biol., 16, 4117-4127.
40. Ramaswamy, S., Nakamura, N., Vazquez, F., Batt, D.B., Perera, S., Roberts, T.M. and Sellers, W.R. (1999) Regulation of G1 progression by the PTEN tumor suppressor protein is linked to inhibition of the phosphatidylinositol 3-kinase/Akt pathway 1. Proc. Natl Acad. Sci. USA, 96, 2110-2115.
41. Wu, L., Archacki, S.R., Zhang, T. and Wang, Q.K. (2007) Induction of high STAT1 expression in transgenic mice with LQTS and heart failure. Biochem. Biophys. Res. Commun., 358, 449-454.
42. Wu, L., Yong, S.L., Fan, C., Ni, Y., Yoo, S., Zhang, T., Zhang, X., Obejero-Paz, C.A., Rho, H.J. and Ke, T., et al. (2008) Identification of a new co-factor, MOG1, required for the full function of cardiac sodium channel Nav 1.5. J. Biol. Chem., 283, 6968-6978.
43. You, S.A., Archacki, S.R., Angheloiu, G., Moravec, C.S., Rao, S., Kinter, M., Topol, E.J. and Wang, Q. (2003) Proteomic approach to coronary atherosclerosis shows ferritin light chain as a significant marker: evidence consistent with iron hypothesis in atherosclerosis. Physiol. Genomics, 13, 25-30.
44. Archacki, S.R., Angheloiu, G., Tian, X.L., Tan, F.L., DiPaola, N., Shen, G.Q., Moravec, C., Ellis, S., Topol, E.J. and Wang, Q. (2003) Identification of new genes differentially expressed in coronary artery disease by expression profiling. Physiol. Genomics, 15, 65-74.
45. Archacki, S.R., Angheloiu, G., Moravec, C.S., Liu, H., Topol, E.J. and Wang, Q.K. (2012) Comparative gene expression analysis between coronary arteries and internal mammary arteries identifies a role for the TES gene in endothelial cell functions relevant to coronary artery disease. Hum. Mol. Genet., 21, 1364-1373.
46. Fan, C., Chen, Q. and Wang, Q.K. (2009) Functional role of transcriptional factor TBX5 in pre-mRNA splicing and Holt-Oram syndrome via association with SC35. J. Biol. Chem., 284, 25653-25663.
47. Wang, F., Xu, C.Q., He, Q., Cai, J.P., Li, X.C., Wang, D., Xiong, X., Liao, Y.H., Zeng, Q.T. and Yang, Y.Z. et al. (2011) Genome-wide association identifies a susceptibility locus for coronary artery disease in the Chinese Han population. Nat. Genet., 43, 345-349.
48. Serbedzija, G.N., Flynn, E. and Willett, C.E. (1999) Zebrafish angiogenesis: a new model for drug screening. Angiogenesis, 3, 353-359.
49. Habeck, H., Odenthal, J., Walderich, B., Maischein, H. and Schulte-Merker, S. (2002) Analysis of a zebrafish VEGF receptor mutant reveals specific disruption of angiogenesis. Curr. Biol., 12, 1405-1412.
50. Thisse, C. and Thisse, B. (2008) High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat. Protoc., 3, 59-69.
51. Zhang, T., Yong, S.L., Tian, X.L. and Wang, Q.K. (2007) Cardiac-specific overexpression of SCN5A gene leads to shorter P wave duration and PR interval in transgenic mice. Biochem. Biophys. Res. Commun., 355, 444-450.
52. Zhang, T., Yong, S.L., Drinko, J.K., Popovic, Z.B., Shryock, J.C., Belardinelli, L. and Wang, Q.K. (2011) LQTS mutation N1325S in cardiac sodium channel gene SCN5A causes cardiomyocyte apoptosis, cardiac fibrosis and contractile dysfunction in mice. Int. J. Cardiol., 147, 239-245.
53. Leung, T., Chen, H., Stauffer, A.M., Giger, K.E., Sinha, S., Horstick, E.J., Humbert, J.E., Hansen, C.A. and Robishaw, J.D. (2006) Zebrafish G protein gamma2 is required for VEGF signaling during angiogenesis. Blood, 108, 160-166.