Ets family members induce lymphangiogenesis through physical and functional interaction with Prox1

Journal of Cell Science

Volumn 124, Issue 16, 2011, Pages 2753-2762

  Yoshimatsu, Yasuhiro ^a   Yamazaki, Tomoko ^a   Mihira, Hajime ^a   Itoh, Taichi ^a   Suehiro, Junichi ^b   Yuki, Keiko ^a   Harada, Kaori ^a   Morikawa, Masato ^a   Iwata, Caname ^a   Minami, Takashi ^b   Morishita, Yasuyuki ^a   Kodama, Tatsuhiko ^b   Miyazono, Kohei ^a   Watabe, Tetsuro ^a,c  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Ets protein family; Lymphangiogenesis; Prox1; Transcription; Vascular endothelial growth factor receptor 3

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ETS; TRANSCRIPTION FACTOR PROX1; UNCLASSIFIED DRUG; VASCULOTROPIN C; VASCULOTROPIN RECEPTOR 3;

ARTICLE; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; LYMPHANGIOGENESIS; LYMPHATIC ENDOTHELIAL CELL; PERITONITIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

ANIMALS; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; HUMANS; INFLAMMATION; LYMPHANGIOGENESIS; MICE; MICE, INBRED BALB C; MUTATION; PERITONITIS; PROTO-ONCOGENE PROTEIN C-ETS-1; PROTO-ONCOGENE PROTEIN C-ETS-2; RNA, SMALL INTERFERING; THIOGLYCOLATES; TUMOR SUPPRESSOR PROTEINS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3;

EID: 79961149491     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.083998     Document Type: Article

References (48)

1. Ayadi, A., Zheng, H., Sobieszczuk, P., Buchwalter, G., Moerman, P., Alitalo, K. and Wasylyk, B. (2001). Net-targeted mutant mice develop a vascular phenotype and up-regulate egr-1. EMBO J. 20, 5139-5152.
2. Barton, K., Muthusamy, N., Fischer, C., Ting, C. N., Walunas, T. L., Lanier, L. L. and Leiden, J. M. (1998). The Ets-1 transcription factor is required for the development of natural killer cells in mice. Immunity 9, 555-563.
3. Bazigou, E., Xie, S., Chen, C., Weston, A., Miura, N., Sorokin, L., Adams, R., Muro, A. F., Sheppard, D. and Makinen, T. (2009). Integrin-α9 is required for fibronectin matrix assembly during lymphatic valve morphogenesis. Dev. Cell 17, 175-186.
4. Bories, J. C., Willerford, D. M., Grevin, D., Davidson, L., Camus, A., Martin, P., Stehelin, D. and Alt, F. W. (1995). Increased T-cell apoptosis and terminal B-cell differentiation-induced by inactivation of the Ets-1 protooncogene. Nature 377, 635-638.
5. Carlsson, P. and Mahlapuu, M. (2002). Forkhead transcription factors: key players in development and metabolism. Dev. Biol. 250, 1-23.
6. Cursiefen, C., Chen, L., Borges, L. P., Jackson, D., Cao, J., Radziejewski, C., D'Amore, P. A., Dana, M. R., Wiegand, S. J. and Streilein, J. W. (2004). VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J. Clin. Invest. 113, 1040-1050.
7. De Val, S. and Black, B. L. (2009). Transcriptional control of endothelial cell development. Dev. Cell 16, 180-195.
8. Flister, M., Wilber, A., Hall, K., Iwata, C., Miyazono, K., Nisato, R., Pepper, M., Zawieja, D. and Ran, S. (2010). Inflammation induces lymphangiogenesis through upregulation of VEGFR-3 mediated by NF-κB and Prox1. Blood 115, 418-429.
9. Harada, K., Yamazaki, T., Iwata, C., Yoshimatsu, Y., Sase, H., Mishima, K., Morishita, Y., Hirashima, M., Oike, Y., Suda, T. et al. (2009). Identification of targets of Prox1 during in vitro vascular differentiation from embryonic stem cells: functional roles of HoxD8 in lymphangiogenesis. J. Cell Sci. 122, 3923-3930.
10. Hasegawa, Y., Abe, M., Yamazaki, T., Niizeki, O., Shiiba, K., Sasaki, I. and Sato, Y. (2004). Transcriptional regulation of human angiopoietin-2 by transcription factor Ets-1. Biochem. Biophys. Res. Commun. 316, 52-58.
11. Hashiya, N., Jo, N., Aoki, M., Matsumoto, K., Nakamura, T., Sato, Y., Ogata, N., Ogihara, T., Kaneda, Y. and Morishita, R. (2004). In vivo evidence of angiogenesis induced by transcription factor ets-1-Ets-1 is located upstream of angiogenesis cascade. Circulation 109, 3035-3041.
12. Hirakawa, S. (2009). From tumor lymphangiogenesis to lymphvascular niche. Cancer Sci. 100, 983-989.
13. Hirashima, M., Sano, K., Morisada, T., Murakami, K., Rossant, J. and Suda, T. (2008). Lymphatic vessel assembly is impaired in Aspp1-deficient mouse embryos. Dev. Biol. 316, 149-159.
14. Hollenhorst, P. C., Shah, A. A., Hopkins, C. and Graves, B. J. (2007). Genome-wide analyses reveal properties of redundant and specific promoter occupancy within the ETS gene family. Genes Dev. 21, 1882-1894.
15. Iwasaka, C., Tanaka, K., Abe, M. and Sato, Y. (1996). Ets-1 regulates angiogenesis by inducing the expression of urokinase-type plasminogen activator and matrix metalloproteinase-1 and the migration of vascular endothelial cells. J. Cell. Physiol. 169, 522-531.
16. Iwata, C., Kano, M. R., Komuro, A., Oka, M., Kiyono, K., Johansson, E., Morishita, Y., Yashiro, M., Hirakawa, K., Kaminishi, M. et al. (2007). Inhibition of cyclooxygenase-2 suppresses lymph node metastasis via reduction of lymphangiogenesis. Cancer Res. 67, 10181-10189.
17. Karkkainen, M. J., Haiko, P., Sainio, K., Partanen, J., Taipale, J., Petrova, T. V., Jeltsch, M., Jackson, D. G., Talikka, M., Rauvala, H. et al. (2004). Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat. Immunol. 5, 74-80.
18. Koinuma, D., Tsutsumi, S., Kamimura, N., Imamura, T., Aburatani, H. and Miyazono, K. (2009). Promoter-wide analysis of Smad4 binding sites in human epithelial cells. Cancer Sci. 100, 2133-2142.
19. Laitem, C., Leprivier, G., Choul-Li, S., Begue, A., Monte, D., Larsimont, D., Dumont, P., Duterque-Coquillaud, M. and Aumercier, M. (2009). Ets-1 p27: a novel Ets-1 isoform with dominant-negative effects on the transcriptional properties and the subcellular localization of Ets-1 p51. Oncogene 28, 2087-2099.
20. Lee, S., Kang, J., Yoo, J., Ganesan, S. K., Cook, S. C., Aguilar, B., Ramu, S., Lee, J. and Hong, Y. K. (2009). Prox1 physically and functionally interacts with COUP-TFII to specify lymphatic endothelial cell fate. Blood 113, 1856-1859.
21. Makinen, T., Veikkola, T., Mustjoki, S., Karpanen, T., Catimel, B., Nice, E. C., Wise, L., Mercer, A., Kowalski, H., Kerjaschki, D. et al. (2001). Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3. EMBO J. 20, 4762-4773.
22. Mavrothalassitis, G. and Ghysdael, J. (2000). Proteins of the ETS family with transcriptional repressor activity. Oncogene 19, 6524-6532.
23. Mishima, K., Watabe, T., Saito, A., Yoshimatsu, Y., Imaizumi, N., Masui, S., Hirashima, M., Morisada, T., Oike, Y., Araie, M. et al. (2007). Prox1 induces lymphatic endothelial differentiation via integrin α9 and other signaling cascades. Mol. Biol. Cell 18, 1421-1429.
24. Mochizuki, T., Miyazaki, H., Hara, T., Furuya, T., Imamura, T., Watabe, T. and Miyazono, K. (2004). Roles for the MH2 domain of Smad7 in the specific inhibition of transforming growth factor-β superfamily signaling. J. Biol. Chem. 279, 31568-31574.
25. Muthusamy, N., Barton, K. and Leiden, J. M. (1995). Defective activation and survival of T-cells lacking the Ets-1 transcription factor. Nature 377, 639-642.
26. Nakano, T., Abe, M., Tanaka, K., Shineha, R., Satomi, S. and Sato, Y. (2000). Angiogenesis inhibition by transdominant mutant Ets-1. J. Cell. Physiol. 184, 255-262.
27. Oliver, G. (2004). Lymphatic vasculature development. Nat. Rev. Immunol. 4, 35-45.
28. Papadaki, C., Alexiou, M., Cecena, G., Verykokakis, M., Bilitou, A., Cross, J. C., Oshima, R. G. and Mavrothalassitis, G. (2007). Transcriptional repressor Erf determines extraembryonic ectoderm differentiation. Mol. Cell. Biol. 27, 5201-5213.
29. Petrova, T. V., Makinen, T., Makela, T. P., Saarela, J., Virtanen, I., Ferrell, R. E., Finegold, D. N., Kerjaschki, D., Yla-Herttuala, S. and Alitalo, K. (2002). Lymphatic endothelial reprogramming of vascular endothelial cells by the Prox-1 homeobox transcription factor. EMBO J. 21, 4593-4599.
30. Petrovic, N., Bhagwat, S. V., Ratzan, W. J., Ostrowski, M. C. and Shapiro, L. H. (2003). CD13/APN transcription is induced by RAS/MAPK-mediated phosphorylation of Ets-2 in activated endothelial cells. J. Biol. Chem. 278, 49358-49368.
31. Pourtier-Manzanedo, A., Vercamer, C., Van Belle, E., Mattot, V., Mouquet, F. and Vandenbunder, B. (2003). Expression of an Ets-1 dominant-negative mutant perturbs normal and tumor angiogenesis in a mouse ear model. Oncogene 22, 1795-1806.
32. Qin, J., Gao, D. M., Jiang, Q. F., Zhou, Q., Kong, Y. Y., Wang, Y. and Xie, Y. H. (2004). Prospero-related homeobox (Prox1) is a corepressor of human liver receptor homolog-1 and suppresses the transcription of the cholesterol 7-α-hydroxylase gene. Mol. Endocrinol. 18, 2424-2439.
33. Saharinen, P. and Petrova, T. V. (2004). Molecular regulation of lymphangiogenesis. Ann. N. Y. Acad. Sci. 1014, 76-87.
34. Schoppmann, S. F., Birner, P., Stockl, J., Kalt, R., Ullrich, R., Caucig, C., Kriehuber, E., Nagy, K., Alitalo, K. and Kerjaschki, D. (2002).Tumor-associated macrophages express lymphatic endothelial growth factors and are related to peritumoral lymphangiogenesis. Am. J. Pathol. 161, 947-956.
35. Shirakihara, T., Saitoh, M. and Miyazono, K. (2007). Differential regulation of epithelial and mesenchymal markers by δEF1 proteins in epithelial-mesenchymal transition induced by TGF-β. Mol. Biol. Cell 18, 3533-3544.
36. Söderberg, O., Gullberg, M., Jarvius, M., Ridderstråle, K., Leuchowius, K., Jarvius, J., Wester, K., Hydbring, P., Bahram, F., Larsson, L. et al. (2006). Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3, 995-1000.
37. Söderberg, O., Leuchowius, K., Gullberg, M., Jarvius, M., Weibrecht, I., Larsson, L. and Landegren, U. (2008). Characterizing proteins and their interactions in cells and tissues using the in situ proximity ligation assay. Methods 45, 227-232.
38. Sosa-Pineda, B., Wigle, J. T. and Oliver, G. (2000). Hepatocyte migration during liver development requires Prox1. Nat. Genet. 25, 254-255.
39. Sugimoto, H., Okamura, K., Sugimoto, S., Satou, M., Hattori, T., Vance, D. E. and Izumi, T. (2005). Sp1 is a co-activator with Ets-1, and net is an important repressor of the transcription of CTP: Phosphocholine cytidylyltransferase α. J. Biol. Chem. 280, 40857-40866.
40. Tammela, T., Zarkada, G., Wallgard, E., Murtomaki, A., Suchting, S., Wirzenius, M., Waltari, M., Hellstrom, M., Schomber, T., Peltonen, R. et al. (2008). Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation. Nature 454, 656-660.
41. Watabe, T., Nishihara, A., Mishima, K., Yamashita, J., Shimizu, K., Miyazawa, K., Nishikawa, S. and Miyazono, K. (2003). TGF-β receptor kinase inhibitor enhances growth and integrity of embryonic stem cell-derived endothelial cells. J. Cell Biol. 163, 1303-1311.
42. Watson, D. K., McWilliams, M. J., Lapis, P., Lautenberger, J. A., Schweinfest, C. W. and Papas, T. S. (1988). Mammalian ets-1 and ets-2 genes encode highly conserved proteins. Proc. Natl. Acad. Sci. USA 85, 7862-7866.
43. Wei, G., Srinivasan, R., Cantemir-Stone, C. Z., Sharma, S. M., Santhanam, R., Weinstein, M., Muthusamy, N., Man, A. K., Oshima, R. G., Leone, G. et al. (2009). Ets1 and Ets2 are required for endothelial cell survival during embryonic angiogenesis. Blood 114, 1123-1130.
44. Wigle, J. T. and Oliver, G. (1999). Prox1 function is required for the development of the murine lymphatic system. Cell 98, 769-778.
45. Wigle, J. T., Chowdhury, K., Gruss, P. and Oliver, G. (1999). Prox1 function is crucial for mouse lens-fibre elongation. Nat. Genet. 21, 318-322.
46. Wigle, J. T., Harvey, N., Detmar, M., Lagutina, I., Grosveld, G., Gunn, M. D., Jackson, D. G. and Oliver, G. (2002). An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype. EMBO J. 21, 1505-1513.
47. Yamamoto, H., Flannery, M. L., Kupriyanov, S., Pearce, J., McKercher, S. R., Henkel, G. W., Maki, R. A., Werb, Z. and Oshima, R. G. (1998). Defective trophoblast function in mice with a targeted mutation of Ets2. Genes Dev. 12, 1315-1326.
48. Yamazaki, T., Yoshimatsu, Y., Morishita, Y., Miyazono, K. and Watabe, T. (2009). COUP-TFII regulates the functions of Prox1 in lymphatic endothelial cells through direct interaction. Genes Cells 14, 425-434.