Spreds are essential for embryonic lymphangiogenesis by regulating vascular endothelial growth factor receptor 3 signaling

Molecular and Cellular Biology

Volumn 27, Issue 12, 2007, Pages 4541-4550

  Taniguchi, Koji ^a   Kohno, Ri Ichiro ^a   Ayada, Toranoshin ^a   Kato, Reiko ^a   Ichiyama, Kenji ^a   Morisada, Tohru ^b   Oike, Yuichi ^b   Yonemitsu, Yoshikazu ^a,c   Maehara, Yoshihiko ^a   Yoshimura, Akihiko ^a,d  

^a KYUSHU UNIVERSITY   (Japan)

^b KEIO UNIVERSITY   (Japan)

^c CHIBA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN SPRED; PROTEIN SPRED 1; PROTEIN SPRED 2; SPROUTY PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN C; VASCULOTROPIN RECEPTOR 3;

ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; EDEMA; EMBRYO; EMBRYO DEATH; ENDOTHELIUM CELL; ENZYME ACTIVATION; EX VIVO STUDY; GENE DELETION; GENE DISRUPTION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LYMPH VESSEL; LYMPHANGIOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SUBCUTANEOUS HEMORRHAGE;

ANIMALS; CELL LINE; CELLS, CULTURED; COCULTURE TECHNIQUES; EMBRYO; FIBROBLASTS; GENE DELETION; HUMANS; IMMUNOHISTOCHEMISTRY; LYMPHANGIOGENESIS; MICE; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3;

MUS;

EID: 34250165403     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01600-06     Document Type: Article

References (31)

1. Abtahian, F., A. Guerriero, E. Sebzda, M. M. Lu, R. Zhou, A. Mocsai, E. E. Myers, B. Huang, D. G. Jackson, V. A. Ferrari, V. Tybulewicz, C. A. Lowell, J. J. Lepore, G. A. Koretzky, and M. L. Kahn. 2003. Regulation of blood and lymphatic vascular separation by signaling proteins SLP-76 and Syk. Science 299:247-251.
2. Alitalo, K., T. Tammela, and T. V. Petrova. 2005. Lymphangiogenesis in development and human disease. Nature 438:946-953.
3. Bjorndahl, M., R. Cao, L. J. Nissen, S. Clasper, L. A. Johnson, Y. Xue, Z. Zhou, D. Jackson, A. J. Hansen, and Y. Cao. 2005. Insulin-like growth factors 1 and 2 induce lymphangiogenesis in vivo. Proc. Natl. Acad. Sci. USA 102:15593-15598.
4. Cao, R., M. A. Bjorndahl, P. Religa, S. Clasper, S. Garvin, D. Galter, B. Meister, F. Ikomi, K. Tritsaris, S. Dissing, T. Ohhashi, D. G. Jackson, and Y. Cao. 2004. PDGF-BB induces intratumoral lymphangiogenesis and promotes lymphatic metastasis. Cancer Cell 6:333-345.
5. Casci, T., J. Vinos, and M. Freeman. 1999. Sprouty, an intracellular inhibitor of Ras signaling. Cell 96:655-665.
6. de Maximy, A. A., Y. Nakatake, S. Moncada, N. Itoh, J. P. Thiery, and S. Bellusci. 1999. Cloning and expression pattern of a mouse homologue of drosophila sprouty in the mouse embryo. Mech. Dev. 81:213-216.
7. Dumont, D. J., L. Jussila, J. Taipale, A. Lymboussaki, T. Mustonen, K. Pajusola, M. Breitman, and K. Alitalo. 1998. Cardiovascular failure in mouse embryos deficient in VEGF receptor-3. Science 282:946-949.
8. Engelhardt, C. M., K. Bundschu, M. Messerschmitt, T. Renne, U. Walter, M. Reinhard, and K. Schuh. 2004. Expression and subcellular localization of Spred proteins in mouse and human tissues. Histochem. Cell Biol. 122:527-538.
9. Hacohen, N., S. Kramer, D. Sutherland, Y. Hiromi, and M. A. Krasnow. 1998. sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92:253-263.
10. Impagnatiello, M. A., S. Weitzer, G. Gannon, A. Compagni, M. Cotten, and G. Christofori. 2001. Mammalian sprouty-1 and -2 are membrane-anchored phosphoprotein inhibitors of growth factor signaling in endothelial cells. J. Cell Biol. 152:1087-1098.
11. Inoue, H., R. Kato, S. Fukuyama, A. Nonami, K. Taniguchi, K. Matsumoto, T. Nakano, M. Tsuda, M. Matsumura, M. Kubo, F. Ishikawa, B. G. Moon, K. Takatsu, Y. Nakanishi, and A. Yoshimura. 2005. Spred-1 negatively regulates allergen-induced airway eosinophilia and hyperresponsivencss. J. Exp. Med. 201:73-82.
12. Kaipainen, A., J. Korhonen, T. Mustonen, V. W. van Hinsbergh, G. H. Fang, D. Dumont, M. Breitman, and K. Alitalo. 1995. Expression of the fms-like tyrosine kinase 4 gene becomes restricted to lymphatic endothelium during development. Proc. Natl. Acad. Sci. USA 92:3566-3570.
13. Karkkainen, M. J., P. Haiko, K. Sainio, J. Partanen, J. Taipale, T. V. Petrova, M. Jeltsch, D. G. Jackson, M. Talikka, H. Rauvala, C. Betsholtz, and K. Alitalo. 2004. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat. Immunol. 5:74-80.
14. Kato, R., A. Nonami, T. Taketomi, T. Wakioka, A. Kuroiwa, Y. Matsuda, and A. Yoshimura. 2003. Molecular cloning of mammalian Spred-3 which suppresses tyrosine kinase-mediated Erk activation. Biochem. Biophys. Res. Commun. 302:767-772.
15. Lee, S. H., D. J. Schloss, L. Jarvis, M. A. Krasnow, and J. L. Swain. 2001. Inhibition of angiogenesis by a mouse sprouty protein. J. Biol. Chem. 276: 4128-4133.
16. Miyoshi, K., T. Wakioka, H. Nishinakamura, M. Kamio, L. Yang, M. Inoue, M. Hasegawa, Y. Yonemitsu, S. Komiya, and A. Yoshimura. 2004. The Sprouty-related protein, Spred, inhibits cell motility, metastasis, and Rho-mediated actin reorganization. Oncogene 23:5567-5576.
17. Morisada, T., Y. Oike, Y. Yamada, T. Urano, M. Akao, Y. Kubota, H. Maekawa, Y. Kimura, M. Ohmura, T. Miyamoto, S. Nozawa, G. Y. Koh, K. Alitalo, and T. Suda. 2005. Angiopoietin-1 promotes LYVE-1-positive lymphatic vessel formation. Blood 105:4649-4656.
18. Nakano, T., Y. Nakashima, Y. Yonemitsu, S. Sumiyoshi, Y. X. Chen, Y. Akishima, T. Ishii, M. Iida, and K. Sueishi. 2005. Angiogenesis and lymphangiogenesis and expression of lymphangiogenic factors in the atherosclerotic intima of human coronary arteries. Hum. Pathol. 36:330-340.
19. Nobuhisa, I., R. Kato, H. Inoue, M. Takizawa, K. Okita, A. Yoshimura, and T. Taga. 2004. Spred-2 suppresses aorta-gonad-mesonephros hematopoiesis by inhibiting MAP kinase activation. J. Exp. Med. 199:737-742.
20. Nonami, A., R. Kato, K. Taniguchi, D. Yoshiga, T. Taketomi, S. Fukuyama, M. Harada, A. Sasaki, and A. Yoshimura. 2004. Spred-1 negatively regulates interleukin-3-mediated ERK/mitogen-activated protein (MAP) kinase activation in hematopoietic cells. J. Biol. Chem. 279:52543-52551.
21. Oliver, G. 2004. Lymphatic vasculature development. Nat Rev. Immunol. 4:35-45.
22. Sabin, F. R. 1902. On the origin of the lymphatic system from the veins and the development of the lymph hearts and thoratic duct in the pig. Am. J. Anat. 1:367-391.
23. Sasaki, A., T. Taketomi, R. Kato, K. Saeki, A. Nonami, M. Sasaki, M. Kuriyama, N. Saito, M. Shibuya, and A. Yoshimura. 2003. Mammalian Sprouty4 suppresses Ras-independent ERK activation by binding to Raf1. Nat. Cell Biol. 5:427-432.
24. Sivak, J. M., L. F. Petersen, and E. Amaya. 2005. FGF signal interpretation is directed by Sprouty and Spred proteins during mesoderm formation. Dev. Cell 8:689-701.
25. Suzuki, H., T. Watabe, M. Kato, K. Miyazawa, and K. Miyazono. 2005. Roles of vascular endothelial growth factor receptor 3 signaling in differentiation of mouse embryonic stem cell-derived vascular progenitor cells into endothelial cells. Blood 105:2372-2379.
26. Taketomi, T., D. Yoshiga, K. Taniguchi, T. Kobayashi, A. Nonami, R. Kato, M. Sasaki, A. Sasaki, H. Ishibashi, M. Moriyama, K. Nakamura, J. Nishimura, and A. Yoshimura. 2005. Loss of mammalian Sprouty2 leads to enteric neuronal hyperplasia and esophageal achalasia. Nat. Neurosci. 8:855-857.
27. Taniguchi, K., T. Ayada, K. Ichiyama, R. Kohno, Y. Yonemitsu, Y. Minami, A. Kikuchi, Y. Maehara, and A. Yoshimura. 2007. Sprouty2 and Sprouty4 are essential for embryonic morphogenesis and regulation of FGF signaling. Biochem. Biophys. Res. Commun. 352:896-902.
28. Veikkola, T., L. Jussila, T. Makinen, T. Karpanen, M. Jeltsch, T. V. Petrova, H. Kubo, G. Thurston, D. M. McDonald, M. G. Achen, S. A. Stacker, and K. Alitalo. 2001. Signalling via vascular endothelial growth factor receptor-3 is sufficient for lymphangiogenesis in transgenic mice. EMBO J. 20:1223-1231.
29. Wakioka, T., A. Sasaki, R. Kato, T. Shouda, A. Matsumoto, K. Miyoshi, M. Tsuneoka, S. Komiya, R. Baron, and A. Yoshimura. 2001. Spred is a Sprouty-related suppressor of Ras signalling. Nature 412:647-651.
30. Wang, D., J. Feng, R. Wen, J. C. Marine, M. Y. Sangster, E. Parganas, A. Hoffmeyer, C. W. Jackson, J. L. Cleveland, P. J. Murray, and J. N. Ihle. 2000. Phospholipase Cγ2 is essential in the functions of B cell and several Fc receptors. Immunity 13:25-35.
31. Yanagi, S., R. Inatome, J. Ding, H. Kitaguchi, V. L. Tybulewicz, and H. Yamamura. 2001. Syk expression in endothelial cells and their morphologic defects in embryonic Syk-deficient mice. Blood 98:2869-2871.