Notch1 functions as a negative regulator of lymphatic endothelial cell differentiation in the venous endothelium

Development (Cambridge)

Volumn 140, Issue 11, 2012, Pages 2365-2376

  Murtomaki, Aino ^a,b   Uh, Minji K ^a   Choi, Yun K ^a   Kitajewski, Christopher ^a   Borisenko, Valeriya ^a   Kitajewski, Jan ^a   Shawber, Carrie J ^a  

^a NewYork Presbyterian Hospital   (United States)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Lymphatic endothelial cells; Mouse; Notch1; Prox1

Indexed keywords

LYVE1 PROTEIN; MEMBRANE PROTEIN; NOTCH1 RECEPTOR; PODOPLANIN; PROX1 PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 3;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CONTROLLED STUDY; ENDOTHELIUM; ENDOTHELIUM CELL; GENE EXPRESSION; HAPLOINSUFFICIENCY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; LOSS OF FUNCTION MUTATION; LYMPH VESSEL; LYMPHATIC ENDOTHELIAL CELL; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VEIN ENDOTHELIUM; WESTERN BLOTTING;

LYMPHATIC ENDOTHELIAL CELLS; MOUSE; NOTCH1; PROX1;

ALLELES; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; ENDOTHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOPROTEINS; HETEROZYGOTE; HOMEODOMAIN PROTEINS; HUMANS; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, TRANSGENIC; MICROCIRCULATION; RECEPTOR, NOTCH1; SIGNAL TRANSDUCTION; TIME FACTORS; TUMOR SUPPRESSOR PROTEINS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3;

EID: 84877727181     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.083865     Document Type: Article

References (45)

1. Andersson, E. R., Sandberg, R. and Lendahl, U. (2011). Notch signaling: simplicity in design, versatility in function. Development 138, 3593-3612.
2. Bertozzi, C. C., Schmaier, A. A., Mericko, P., Hess, P. R., Zou, Z., Chen, M., Chen, C. Y., Xu, B., Lu, M. M., Zhou, D. et al. (2010). Platelets regulate lymphatic vascular development through CLEC-2-SLP-76 signaling. Blood 116, 661-670.
3. Borggrefe, T. and Liefke, R. (2012). Fine-tuning of the intracellular canonical Notch signaling pathway. Cell Cycle 11, 264-276.
4. Buonamici, S., Trimarchi, T., Ruocco, M. G., Reavie, L., Cathelin, S., Mar, B. G., Klinakis, A., Lukyanov, Y., Tseng, J. C., Sen, F. et al. (2009). CCR7 signalling as an essential regulator of CNS infiltration in T-cell leukaemia. Nature 459, 1000-1004.
5. Coma, S., Shimizu, A. and Klagsbrun, M. (2011). Hypoxia induces tumor and endothelial cell migration in a semaphorin 3F- and VEGF-dependent manner via transcriptional repression of their common receptor neuropilin 2. Cell Adh. Migr. 5, 266-275.
6. Diez, H., Fischer, A., Winkler, A., Hu, C. J., Hatzopoulos, A. K., Breier, G. and Gessler, M. (2007). Hypoxia-mediated activation of Dll4-Notch-Hey2 signaling in endothelial progenitor cells and adoption of arterial cell fate. Exp. Cell Res. 313, 1-9.
7. Duncan, A. W., Rattis, F. M., DiMascio, L. N., Congdon, K. L., Pazianos, G., Zhao, C., Yoon, K., Cook, J. M., Willert, K., Gaiano, N. et al. (2005). Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nat. Immunol. 6, 314-322.
8. Favier, B., Alam, A., Barron, P., Bonnin, J., Laboudie, P., Fons, P., Mandron, M., Herault, J. P., Neufeld, G., Savi, P. et al. (2006). Neuropilin-2 interacts with VEGFR-2 and VEGFR-3 and promotes human endothelial cell survival and migration. Blood 108, 1243-1250.
9. François, M., Caprini, A., Hosking, B., Orsenigo, F., Wilhelm, D., Browne, C., Paavonen, K., Karnezis, T., Shayan, R., Downes, M. et al. (2008). Sox18 induces development of the lymphatic vasculature in mice. Nature 456, 643-647.
10. François, M., Short, K., Secker, G. A., Combes, A., Schwarz, Q., Davidson, T. L., Smyth, I., Hong, Y. K., Harvey, N. L. and Koopman, P. (2012). Segmental territories along the cardinal veins generate lymph sacs via a ballooning mechanism during embryonic lymphangiogenesis in mice. Dev. Biol. 364, 89-98.
11. Funahashi, Y., Shawber, C. J., Vorontchikhina, M., Sharma, A., Outtz, H. H. and Kitajewski, J. (2010). Notch regulates the angiogenic response via induction of VEGFR-1. J. Angiogenes Res. 2, 3.
12. Geudens, I., Herpers, R., Hermans, K., Segura, I., Ruiz de Almodovar, C., Bussmann, J., De Smet, F., Vandevelde, W., Hogan, B. M., Siekmann, A. et al. (2010). Role of delta-like-4/Notch in the formation and wiring of the lymphatic network in zebrafish. Arterioscler. Thromb. Vasc. Biol. 30, 1695-1702.
13. Gridley, T. (2010). Notch signaling in the vasculature. Curr. Top. Dev. Biol. 92, 277-309.
14. Hong, Y. K. and Detmar, M. (2003). Prox1, master regulator of the lymphatic vasculature phenotype. Cell Tissue Res. 314, 85-92.
15. Jakobsson, L., Bentley, K. and Gerhardt, H. (2009). VEGFRs and Notch: a dynamic collaboration in vascular patterning. Biochem. Soc. Trans. 37, 1233-1236.
16. Johnson, N. C., Dillard, M. E., Baluk, P., McDonald, D. M., Harvey, N. L., Frase, S. L. and Oliver, G. (2008). Lymphatic endothelial cell identity is reversible and its maintenance requires Prox1 activity. Genes Dev. 22, 3282-3291.
17. Kang, J., Yoo, J., Lee, S., Tang, W., Aguilar, B., Ramu, S., Choi, I., Otu, H. H., Shin, J. W., Dotto, G. P. et al. (2010). An exquisite cross-control mechanism among endothelial cell fate regulators directs the plasticity and heterogeneity of lymphatic endothelial cells. Blood 116, 140-150.
18. 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.
19. Kärpänen, T. H. C., Heckman, C. A., Keskitalo, S., Jeltsch, M., Ollila, H., Neufeld, G., Tamagnone, L. and Alitalo, K. (2006). Functional interaction of VEGF-C and VEGF-D with neuropilin receptors. FASEB J. 20, 1462-1472.
20. Kim, H., Nguyen, V. P., Petrova, T. V., Cruz, M., Alitalo, K. and Dumont, D. J. (2010). Embryonic vascular endothelial cells are malleable to reprogramming via Prox1 to a lymphatic gene signature. BMC Dev. Biol. 10, 72.
21. 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.
22. 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.
23. Lin, F. J., Chen, X., Qin, J., Hong, Y. K., Tsai, M. J. and Tsai, S. Y. (2010). Direct transcriptional regulation of neuropilin-2 by COUP-TFII modulates multiple steps in murine lymphatic vessel development. J. Clin. Invest. 120, 1694-1707.
24. Liu, H., Chi, A. W., Arnett, K. L., Chiang, M. Y., Xu, L., Shestova, O., Wang, H., Li, Y. M., Bhandoola, A., Aster, J. C. et al. (2010). Notch dimerization is required for leukemogenesis and T-cell development. Genes Dev. 24, 2395-2407.
25. Lohela, M., Heloterä, H., Haiko, P., Dumont, D. J. and Alitalo, K. (2008). Transgenic induction of vascular endothelial growth factor-C is strongly angiogenic in mouse embryos but leads to persistent lymphatic hyperplasia in adult tissues. Am. J. Pathol. 173, 1891-1901.
26. Mäkinen, 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.
27. Niessen, K., Zhang, G., Ridgway, J. B., Chen, H., Kolumam, G., Siebel, C. W. and Yan, M. (2011). The Notch1-Dll4 signaling pathway regulates mouse postnatal lymphatic development. Blood 118, 1989-1997.
28. Oliver, G. and Harvey, N. (2002). A stepwise model of the development of lymphatic vasculature. Ann. N. Y. Acad. Sci. 979, 159-165, discussion 188-196.
29. Oliver, G., Sosa-Pineda, B., Geisendorf, S., Spana, E. P., Doe, C. Q. and Gruss, P. (1993). Prox 1, a prospero-related homeobox gene expressed during mouse development. Mech. Dev. 44, 3-16.
30. Petrova, T. V., Mäkinen, T., Mäkelä, T. P., Saarela, J., Virtanen, I., Ferrell, R. E., Finegold, D. N., Kerjaschki, D., Ylä-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.
31. Shawber, C. J., Funahashi, Y., Francisco, E., Vorontchikhina, M., Kitamura, Y., Stowell, S. A., Borisenko, V., Feirt, N., Podgrabinska, S., Shiraishi, K. et al. (2007). Notch alters VEGF responsiveness in human and murine endothelial cells by direct regulation of VEGFR-3 expression. J. Clin. Invest. 117, 3369-3382.
32. Srinivasan, R. S. and Oliver, G. (2011). Prox1 dosage controls the number of lymphatic endothelial cell progenitors and the formation of the lymphovenous valves. Genes Dev. 25, 2187-2197.
33. Srinivasan, R. S., Dillard, M. E., Lagutin, O. V., Lin, F. J., Tsai, S., Tsai, M. J., Samokhvalov, I. M. and Oliver, G. (2007). Lineage tracing demonstrates the venous origin of the mammalian lymphatic vasculature. Genes Dev. 21, 2422-2432.
34. Srinivasan, R. S., Geng, X., Yang, Y., Wang, Y., Mukatira, S., Studer, M., Porto, M. P., Lagutin, O. V. and Oliver, G. (2010). The nuclear hormone receptor Coup-TFII is required for the initiation and early maintenance of Prox1 expression in lymphatic endothelial cells. Genes Dev. 24, 696-707.
35. Tammela, T., Zarkada, G., Wallgard, E., Murtomäki, A., Suchting, S., Wirzenius, M., Waltari, M., Hellström, M., Schomber, T., Peltonen, R. et al. (2008). Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation. Nature 454, 656-660.
36. Taylor, K. L., Henderson, A. M. and Hughes, C. C. (2002). Notch activation during endothelial cell network formation in vitro targets the basic HLH transcription factor HESR-1 and downregulates VEGFR-2/KDR expression. Microvasc. Res. 64, 372-383.
37. Tu, L., Fang, T. C., Artis, D., Shestova, O., Pross, S. E., Maillard, I. and Pear, W. S. (2005). Notch signaling is an important regulator of type 2 immunity. J. Exp. Med. 202, 1037-1042.
38. Tung, J. J., Hobert, O., Berryman, M. and Kitajewski, J. (2009). Chloride intracellular channel 4 is involved in endothelial proliferation and morphogenesis in vitro. Angiogenesis 12, 209-220.
39. Tung, J. J., Tattersall, I. W. and Kitajewski, J. (2012). Tips, stalks, tubes: notchmediated cell fate determination and mechanisms of tubulogenesis during angiogenesis. Cold Spring Harb. Perspect Med. 2, a006601.
40. Wigle, J. T. and Oliver, G. (1999). Prox1 function is required for the development of the murine lymphatic system. Cell 98, 769-778.
41. 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.
42. Xu, Y., Yuan, L., Mak, J., Pardanaud, L., Caunt, M., Kasman, I., Larrivée, B., Del Toro, R., Suchting, S., Medvinsky, A. et al. (2010). Neuropilin-2 mediates VEGF-C-induced lymphatic sprouting together with VEGFR3. J. Cell Biol. 188, 115-130.
43. Yang, X., Klein, R., Tian, X., Cheng, H.-T., Kopan, R. and Shen, J. (2004). Notch activation induces apoptosis in neural progenitor cells through a p53- dependent pathway. Dev. Biol. 269, 81-94.
44. 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.
45. Zheng, W., Tammela, T., Yamamoto, M., Anisimov, A., Holopainen, T., Kaijalainen, S., Karpanen, T., Lehti, K., Ylä-Herttuala, S. and Alitalo, K. (2011). Notch restricts lymphatic vessel sprouting induced by vascular endothelial growth factor. Blood 118, 1154-1162.