Development of the lymphatic system: New questions and paradigms

Development (Cambridge)

Volumn 143, Issue 6, 2016, Pages 924-935

  Semo, Jonathan ^a   Nicenboim, Julian ^a   Yaniv, Karina ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Embryonic origin; Endothelial; Lymphatic; Venous

Indexed keywords

CELL FATE; CELL MIGRATION; CELL REGENERATION; ENDOTHELIUM CELL; HUMAN; LYMPH VESSEL; LYMPHANGIOGENESIS; LYMPHATIC SYSTEM; PRIORITY JOURNAL; REVIEW; SPROUTING; ANIMAL; BIOLOGICAL MODEL; DISEASES; EMBRYOLOGY; GENETIC TRANSCRIPTION; REGENERATION; SIGNAL TRANSDUCTION;

ANIMALS; DISEASE; HUMANS; LYMPHATIC SYSTEM; MODELS, BIOLOGICAL; REGENERATION; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84960970949     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.132431     Document Type: Review

References (117)

1. Alders, M., Hogan, B. M., Gjini E., Salehi, F., Al-Gazali, L., Hennekam, E. A., Holmberg, E. E., Mannens, M. M. A. M., Mulder, M. F., Offerhaus, G. J. et al. (2009). Mutations in CCBE1 cause generalized lymph vessel dysplasia in humans. Nat. Genet. 41, 1272-1274.
2. Alitalo, K. and Carmeliet, P. (2002). Molecular mechanisms of lymphangiogenesis in health and disease. Cancer Cell 1, 219-227.
3. Aranguren, X. L., Beerens, M., Vandevelde, W., Dewerchin, M., Carmeliet, P. and Luttun, A. (2011). Transcription factor COUP-TFII is indispensable for venous and lymphatic development in zebrafish and Xenopus laevis. Biochem. Biophys. Res. Commun. 410, 121-126.
4. Aspelund, A., Antila, S., Proulx, S. T., Karlsen, T. V., Karaman, S., Detmar, M., Wiig, H. and Alitalo, K. (2015). A dural lymphatic vascular system that drains brain interstitial fluid and macromolecules. J. Exp. Med. 212, 991-999.
5. Banerji, S., Ni, J., Wang, S. X., Clasper, S., Su, J., Tammi, R., Jones, M. and Jackson, D. G. (1999). LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J. Cell Biol. 144, 789-801.
6. Bos, F. L., Caunt, M., Peterson-Maduro J., Planas-Paz, L., Kowalski J., Karpanen T., van Impel, A., Tong, R., Ernst, J. A., Korving, J. et al. (2011). CCBE1 is essential for mammalian lymphatic vascular development and enhances the lymphangiogenic effect of vascular endothelial growth factor-C in vivo. Circ. Res. 109, 486-491.
7. Buttler, K., Becker, J., Pukrop, T. and Wilting, J. (2013). Maldevelopment of dermal lymphatics in Wnt5a-knockout-mice. Dev. Biol. 381, 365-376.
8. Cermenati, S., Moleri, S., Cimbro, S., Corti, P., Del Giacco, L., Amodeo, R., Dejana, E., Koopman, P., Cotelli, F. and Beltrame, M. (2008). Sox18 and Sox7 play redundant roles in vascular development. Blood 111, 2657-2666.
9. Cermenati, S., Moleri, S., Neyt, C., Bresciani, E., Carra, S., Grassini, D. R., Omini, A., Goi, M., Cotelli, F., Francois, M. et al. (2013). Sox18 genetically interacts with VegfC to regulate lymphangiogenesis in zebrafish. Arterioscler. Thromb. Vasc. Biol. 33, 1238-1247.
10. Cha, Y. R., Fujita, M., Butler, M., Isogai, S., Kochhan, E., Siekmann, A. F. and Weinstein, B. M. (2012). Chemokine signaling directs trunk lymphatic network formation along the preexisting blood vasculature. Dev. Cell 22, 824-836.
11. Chen, L., Mupo, A., Huynh, T., Cioffi, S., Woods, M., Jin, C., McKeehan, W., Thompson-Snipes, L., Baldini, A. and Illingworth, E. (2010). Tbx1 regulates Vegfr3 and is required for lymphatic vessel development. J. Cell Biol. 189, 417-424.
12. Clevers, H. (2006). Wnt/beta-catenin signaling in development and disease. Cell 127, 469-480.
13. Covassin, L. D., Villefranc, J. A., Kacergis, M. C., Weinstein, B. M. and Lawson, N. D. (2006). Distinct genetic interactions between multiple Vegf receptors are required for development of different blood vessel types in zebrafish. Proc. Natl. Acad. Sci. USA 103, 6554-6559.
14. Das, A., Sinha, M., Datta, S., Abas, M., Chaffee, S., Sen, C. K. and Roy, S. (2015). Monocyte and macrophage plasticity in tissue repair and regeneration. Am. J. Pathol. 185, 2596-2606.
15. de Vinuesa, A. G., Abdelilah-Seyfried, S., Knaus, P., Zwijsen, A. and Bailly, S. (2016). BMP signaling in vascular biology and dysfunction. Cytokine Growth Factor Rev. 27, 65-79.
16. Deguchi, T., Fujimori, K. E., Kawasaki, T., Ohgushi, H. and Yuba, S. (2009). Molecular cloning and gene expression of the prox1a and prox1b genes in the medaka, Oryzias latipes. Gene Expr. Patterns 9, 341-347.
17. Del Giacco, L., Pistocchi, A. and Ghilardi, A. (2010). prox1b Activity is essential in zebrafish lymphangiogenesis. PLoS ONE 5, e13170.
18. Deng, Y., Atri, D., Eichmann, A. and Simons, M. (2013). Endothelial ERK signaling controls lymphatic fate specification. J. Clin. Invest. 123, 1202-1215.
19. Dieterich, L. C., Klein, S., Mathelier, A., Sliwa-Primorac, A., Ma, Q., Hong, Y.-K., Shin, J. W., Hamada, M., Lizio, M., Itoh, M. et al. (2015). DeepCAGE transcriptomics reveal an important role of the transcription factor MAFB in the lymphatic endothelium. Cell Rep. 13, 1493-1504.
20. Dumont, D. J., Jussila, L., Taipale, J., Lymboussaki, A., Mustonen, T., Pajusola, K., Breitman, M. and Alitalo, K. (1998). Cardiovascular failure in mouse embryos deficient in VEGF receptor-3. Science 282, 946-949.
21. Dunworth, W. P., Cardona-Costa, J., Bozkulak, E. C., Kim, J.-D., Meadows, S., Fischer, J. C., Wang, Y., Cleaver, O., Qyang, Y., Ober, E. A. et al. (2014). Bone morphogenetic protein 2 signaling negatively modulates lymphatic development in vertebrate embryos. Circ. Res. 114, 56-66.
22. Duong, T., Koltowska, K., Pichol-Thievend, C., Le Guen, L., Fontaine, F., Smith, K. A., Truong, V., Skoczylas, R., Stacker, S. A., Achen, M. G. et al. (2014). VEGFD regulates blood vascular development by modulating SOX18 activity. Blood 123, 1102-1112.
23. Fatima, A., Culver, A., Culver, F., Liu, T., Dietz, W. H., Thomson, B. R., Hadjantonakis, A.-K., Quaggin, S. E. and Kume, T. (2014). Murine Notch1 is required for lymphatic vascular morphogenesis during development. Dev. Dyn. 243, 957-964.
24. Flores, M. V., Hall, C. J., Crosier, K. E. and Crosier, P. S. (2010). Visualization of embryonic lymphangiogenesis advances the use of the zebrafish model for research in cancer and lymphatic pathologies. Dev. Dyn. 239, 2128-2135.
25. 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.
26. Gale, N. W., Prevo, R., Espinosa, J., Ferguson, D. J., Dominguez, M. G., Yancopoulos, G. D., Thurston, G. and Jackson, D. G. (2007). Normal lymphatic development and function in mice deficient for the lymphatic hyaluronan receptor LYVE-1. Mol. Cell. Biol. 27, 595-604.
27. 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.
28. Gordon, E. J., Rao, S., Pollard, J. W., Nutt, S. L., Lang, R. A. and Harvey, N. L. (2010). Macrophages define dermal lymphatic vessel calibre during development by regulating lymphatic endothelial cell proliferation. Development 137, 3899-3910.
29. Haiko, P., Makinen, T., Keskitalo, S., Taipale, J., Karkkainen, M. J., Baldwin, M. E., Stacker, S. A., Achen, M. G. and Alitalo, K. (2008). Deletion of vascular endothelial growth factor C (VEGF-C) and VEGF-D is not equivalent to VEGF receptor 3 deletion in mouse embryos. Mol. Cell. Biol. 28, 4843-4850.
30. Harvey, N. L., Srinivasan, R. S., Dillard, M. E., Johnson, N. C., Witte, M. H., Boyd, K., Sleeman, M. W. and Oliver, G. (2005). Lymphatic vascular defects promoted by Prox1 haploinsufficiency cause adult-onset obesity. Nat. Genet. 37, 1072-1081.
31. He, Y., Rajantie, I., Ilmonen, M., Makinen, T., Karkkainen, M. J., Haiko, P., Salven, P. and Alitalo, K. (2004). Preexisting lymphatic endothelium but not endothelial progenitor cells are essential for tumor lymphangiogenesis and lymphatic metastasis. Cancer Res. 64, 3737-3740.
32. Helker, C. S., Schuermann, A., Karpanen T., Zeuschner, D., Belting, H.-G., Affolter, M., Schulte-Merker S. and Herzog, W. (2013). The zebrafish common cardinal veins develop by a novel mechanism: lumen ensheathment. Development 140, 2776-2786.
33. Hen, G., Nicenboim, J., Mayseless, O., Asaf, L., Shin, M., Busolin, G., Hofi, R., Almog, G., Tiso, N., Lawson, N. D. et al. (2015). Venous-derived angioblasts generate organ-specific vessels during zebrafish embryonic development. Development 142, 4266-4278.
34. Herbert, S. P., Huisken, J., Kim, T. N., Feldman, M. E., Houseman, B. T., Wang, R. A., Shokat, K. M. and Stainier, D. Y. (2009). Arterial-venous segregation by selective cell sprouting: an alternative mode of blood vessel formation. Science 326, 294-298.
35. Hirschi, K. K. (2012). Hemogenic endothelium during development and beyond. Blood 119, 4823-4827.
36. 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.
37. Hong, Y.-K., Harvey, N., Noh, Y.-H., Schacht, V., Hirakawa, S., Detmar, M. and Oliver, G. (2002). Prox1 is a master control gene in the program specifying lymphatic endothelial cell fate. Dev. Dyn. 225, 351-357.
38. Huntington, G. S. and McClure, C. F. w. (1912). The anatomy and development of the jugular lymph sacs in the domestic cat (Felis domestica). Am. J. Anat. 10, 177-312.
39. Isogai, S., Lawson, N. D., Torrealday, S., Horiguchi, M. and Weinstein, B. M. (2003). Angiogenic network formation in the developing vertebrate trunk. Development 130, 5281-5290.
40. Jeltsch, M., Kaipainen, A., Joukov, V., Meng, X., Lakso, M., Rauvala, H., Swartz, M., Fukumura, D., Jain, R. K. and Alitalo, K. (1997). Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science 276, 1423-1425.
41. Jeltsch, M., Jha, S. K., Tvorogov, D., Anisimov, A., Leppanen, V.-M., Holopainen, T., Kivela, R., Ortega, S., Karpanen T. and Alitalo, K. (2014). CCBE1 enhances lymphangiogenesis via A disintegrin and metalloprotease with thrombospondin motifs-3-mediated vascular endothelial growth factor-C activation. Circulation 129, 1962-1971.
42. Jiang, S., Bailey, A. S., Goldman, D. C., Swain, J. R., Wong, M. H., Streeter, P. R. and Fleming, W. H. (2008). Hematopoietic stem cells contribute to lymphatic endothelium. PLoS ONE 3, e3812.
43. Jin, S.-W., Beis, D., Mitchell, T., Chen, J.-N. and Stainier, D. Y. R. (2005). Cellular and molecular analyses of vascular tube and lumen formation in zebrafish. Development 132, 5199-5209.
44. Kaipainen, A., Korhonen, J., Mustonen, T., van Hinsbergh, V., Fang, G.-H., Dumont, D., Breitman, M. and Alitalo, K. (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.
45. 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.
46. 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.
47. Kashiwada, T., Fukuhara, S., Terai, K., Tanaka, T., Wakayama, Y., Ando, K., Nakajima, H., Fukui, H., Yuge, S., Saito, Y. et al. (2015). beta-Catenindependent transcription is central to Bmp-mediated formation of venous vessels. Development 142, 497-509.
48. Kim, J.-D. and Kim, J. (2014). Alk3/Alk3b and Smad5 mediate BMP signaling during lymphatic development in zebrafish. Mol. Cells 37, 270-274.
49. 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.
50. Kirschmann, D. A., Seftor, E. A., Hardy, K. M., Seftor, R. E. b. and Hendrix, M. J. c. (2012). Molecular pathways: vasculogenic mimicry in tumor cells: diagnostic and therapeutic implications. Clin. Cancer Res. 18, 2726-2732.
51. Klotz, L., Norman, S., Vieira, J. M., Masters, M., Rohling, M., Dubé, K. N., Bollini S., Matsuzaki F., Carr C. A. and Riley P. R. (2015). Cardiac lymphatics are heterogeneous in origin and respond to injury. Nature 522, 62-67.
52. Kohli, V., Schumacher, J. A., Desai, S. P., Rehn, K. and Sumanas, S. (2013). Arterial and venous progenitors of the major axial vessels originate at distinct locations. Dev. Cell 25, 196-206.
53. Kok, F. O., Shin, M., Ni, C.-W., Gupta, A., Grosse, A. S., van Impel, A., Kirchmaier, B. C., Peterson-Maduro J., Kourkoulis, G., Male, I. et al. (2015). Reverse genetic screening reveals poor correlation between morpholino-induced and mutant phenotypes in zebrafish. Dev. Cell 32, 97-108.
54. Koltowska, K., Lagendijk, A. K., Pichol-Thievend, C., Fischer, J. C., Francois, M., Ober, E. A., Yap, A. S. and Hogan, B. M. (2015a). Vegfc regulates bipotential precursor division and Prox1 expression to promote lymphatic identity in zebrafish. Cell Rep. 13, 1828-1841.
55. Koltowska, K., Paterson, S., Bower, N. I., Baillie, G. J., Lagendijk, A. K., Astin, J.W., Chen, H., Francois, M., Crosier, P. S., Taft, R. J. et al. (2015b). mafba is a downstream transcriptional effector of Vegfc signaling essential for embryonic lymphangiogenesis in zebrafish. Genes Dev. 29, 1618-1630.
56. Küchler, A. M., Gjini E., Peterson-Maduro J., Cancilla B., Wolburg H. and Schulte-Merker S. (2006). Development of the zebrafish lymphatic system requires VEGFC signaling. Curr. Biol. 16, 1244-1248.
57. Kukk, E., Lymboussaki, A., Taira, S., Kaipainen, A., Jeltsch, M., Joukov, V. and Alitalo, K. (1996). VEGF-C receptor binding and pattern of expression with VEGFR-3 suggests a role in lymphatic vascular development. Development 122, 3829-3837.
58. Lawson, N. D. and Weinstein, B. M. (2002). In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248, 307-318.
59. Le Guen, L., Karpanen T., Schulte, D., Harris, N. C., Koltowska, K., Roukens, G., Bower, N. I., van Impel, A., Stacker, S. A., Achen, M. G. et al. (2014). Ccbe1 regulates Vegfc-mediated induction of Vegfr3 signaling during embryonic lymphangiogenesis. Development 141, 1239-1249.
60. Lee, J. Y., Park, C., Cho, Y. P., Lee, E., Kim, H., Kim, P., Yun, S. H. and Yoon, Y.-s. (2010). Podoplanin-expressing cells derived from bone marrow play a crucial role in postnatal lymphatic neovascularization. Circulation 122, 1413-1425.
61. Lee, S.-J., Park, C., Lee, J. Y., Kim, S., Kwon, P. J., Kim, W., Jeon, Y. H., Lee, E. and Yoon, Y. S. (2015). Generation of pure lymphatic endothelial cells from human pluripotent stem cells and their therapeutic effects on wound repair. Sci. Rep. 5, 11019.
62. Levet, S., Ciais, D., Merdzhanova, G., Mallet, C., Zimmers, T. A., Lee, S.-J., Navarro, F. P., Texier, I., Feige, J.-J., Bailly, S. et al. (2013). Bone morphogenetic protein 9 (BMP9) controls lymphatic vessel maturation and valve formation. Blood 122, 598-607.
63. Lewis, F. T. (1905). The development of the lymphatic system in rabbits. Am. J. Anat. 5, 95-111.
64. Lim, A. H., Suli, A., Yaniv, K., Weinstein, B., Li, D. Y. and Chien, C.-B. (2011). Motoneurons are essential for vascular pathfinding. Development 138, 3847-3857.
65. Lindskog, H., Kim, Y. H., Jelin, E. B., Kong, Y., Guevara-Gallardo, S., Kim, T. N. and Wang, R. A. (2014). Molecular identification of venous progenitors in the dorsal aorta reveals an aortic origin for the cardinal vein in mammals. Development 141, 1120-1128.
66. Louveau, A., Smirnov, I., Keyes, T. J., Eccles, J. D., Rouhani, S. J., Peske, J. D., Derecki, N. C., Castle, D., Mandell, J.W., Lee, K. S. et al. (2015). Structural and functional features of central nervous system lymphatic vessels. Nature 523, 337-341.
67. Mahadevan, A., Welsh, I. C., Sivakumar, A., Gludish, D. W., Shilvock, A. R., Noden, D. M., Huss, D., Lansford, R. and Kurpios, N. A. (2014). The left-right Pitx2 pathway drives organ-specific arterial and lymphatic development in the intestine. Dev. Cell 31, 690-706.
68. 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.
69. Martinez-Corral, I., Ulvmar, M. H., Stanczuk, L., Tatin, F., Kizhatil, K., John, S. W. M., Alitalo, K., Ortega, S. and Makinen, T. (2015). Nonvenous origin of dermal lymphatic vasculature. Circ. Res. 116, 1649-1654.
70. Maruyama, K., Ii, M., Cursiefen, C., Jackson, D. G., Keino, H., Tomita, M., Van Rooijen, N., Takenaka, H., D’Amore, P. A., Stein-Streilein, J. et al. (2005). Inflammation-induced lymphangiogenesis in the cornea arises from CD11bpositive macrophages. J. Clin. Invest. 115, 2363-2372.
71. McClure, C. F. W. (1921). The endothelial problem. Anat. Rec. 22, 219-237.
72. Mikels, A. J. and Nusse, R. (2006). PurifiedWnt5a protein activates or inhibits betacatenin– TCF signaling depending on receptor context. PLoS Biol. 4, e115.
73. Murtomaki, A., Uh, M. K., Choi, Y. K., Kitajewski, C., Borisenko, V., Kitajewski, J. and Shawber, C. J. (2013). Notch1 functions as a negative regulator of lymphatic endothelial cell differentiation in the venous endothelium. Development 140, 2365-2376
74. Nguyen, P. D., Hollway, G. E., Sonntag, C., Miles, L. B., Hall, T. E., Berger, S., Fernandez, K. J., Gurevich, D. B., Cole, N. J., Alaei, S. et al. (2014). Haematopoietic stem cell induction by somite-derived endothelial cells controlled by meox1. Nature 512, 314-318.
75. Nicenboim, J., Malkinson, G., Lupo, T., Asaf, L., Sela, Y., Mayseless, O., Gibbs- Bar, L., Senderovich, N., Hashimshony, T., Shin, M. et al. (2015). Lymphatic vessels arise from specialized angioblasts within a venous niche. Nature 522, 56-61.
76. 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.
77. Ny, A., Koch, M., Schneider, M., Neven, E., Tong, R. T., Maity, S., Fischer, C., Plaisance, S., Lambrechts, D., Heligon, C. et al. (2005). A genetic Xenopus laevis tadpole model to study lymphangiogenesis. Nat. Med. 11, 998-1004.
78. Okuda, K. S., Astin, J. W., Misa, J. P., Flores, M. V., Crosier, K. E. and Crosier, P. S. (2012). lyve1 expression reveals novel lymphatic vessels and new mechanisms for lymphatic vessel development in zebrafish. Development 139, 2381-2391.
79. Pennisi, D., Bowles, J., Nagy, A., Muscat, G. and Koopman, P. (2000). Mice null for sox18 are viable and display a mild coat defect. Mol. Cell. Biol. 20, 9331-9336.
80. Potente, M., Gerhardt, H. and Carmeliet, P. (2011). Basic and therapeutic aspects of angiogenesis. Cell 146, 873-887.
81. Religa, P., Cao, R., Bjorndahl, M., Zhou, Z., Zhu, Z. and Cao, Y. (2005). Presence of bone marrow-derived circulating progenitor endothelial cells in the newly formed lymphatic vessels. Blood 106, 4184-4190.
82. Rossi, A., Kontarakis, Z., Gerri, C., Nolte, H., Hölper, S., Krüger, M. and Stainier, D. Y. R. (2015). Genetic compensation induced by deleterious mutations but not gene knockdowns. Nature 524, 230-233.
83. Rufaihah, A. J., Huang, N. F., Kim, J., Herold, J., Volz, K. S., Park, T. S., Lee, J. C., Zambidis, E. T., Reijo-Pera, R. and Cooke, J. P. (2013). Human induced pluripotent stem cell-derived endothelial cells exhibit functional heterogeneity. Am. J. Transl. Res. 5, 21-35.
84. Sabin, F. R. (1902). On the origin of the lymphatic system from the veins and the development of the lymph hearts and thoracic duct in the pig. Am. J. Anat. 1, 367-389.
85. Sabin, F. R. (1904). On the development of the superficial lymphatics in the skin of the pig. Am. J. Anat. 3, 183-195.
86. Sabin, F. R. (1913). The Origin and Development of the Lymphatic System. Baltimore: Johns Hopkins Press.
87. Schledzewski, K., Falkowski, M., Moldenhauer, G., Metharom, P., Kzhyshkowska, J., Ganss, R., Demory, A., Falkowska-Hansen, B., Kurzen, H., Ugurel, S. et al. (2006). Lymphatic endothelium-specific hyaluronan receptor LYVE-1 is expressed by stabilin-1+, F4/80+, CD11b+ macrophages in malignant tumours and wound healing tissuein vivo and in bone marrow culturesin vitro: implications for the assessment of lymphangiogenesis. J. Pathol. 209, 67-77.
88. Siekmann, A. F. and Lawson, N. D. (2007). Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature 445, 781-784.
89. Soda, Y., Marumoto, T., Friedmann-Morvinski, D., Soda, M., Liu, F., Michiue, H., Pastorino, S., Yang, M., Hoffman, R. M., Kesari, S. et al. (2011). Transdifferentiation of glioblastoma cells into vascular endothelial cells. Proc. Natl. Acad. Sci. USA 108, 4274-4280.
90. 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.
91. 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.
92. Srinivasan, R. S., Geng, X., Yang, Y., Wang, Y., Mukatira, S., Studer, M., Porto, M. P. R., Lagutin, O. 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.
93. Srinivasan, R. S., Escobedo, N., Yang, Y., Interiano, A., Dillard, M. E., Finkelstein, D., Mukatira, S., Gil, H. J., Nurmi, H., Alitalo, K. et al. (2014). The Prox1–Vegfr3 feedback loop maintains the identity and the number of lymphatic endothelial cell progenitors. Genes Dev. 28, 2175-2187.
94. Stanczuk, L., Martinez-Corral, I., Ulvmar, M. H., Zhang, Y., Laviña, B., Fruttiger M., Adams R. H., Saur D., Betsholtz C., Ortega, S. et al. (2015). cKit Lineage hemogenic endothelium-derived cells contribute to mesenteric lymphatic vessels. Cell Rep. 10, 1708-1721.
95. 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.
96. Tao, S., Witte, M., Bryson-Richardson, R. J., Currie, P. D., Hogan, B. M. and Schulte-Merker S. (2011). Zebrafish prox1b mutants develop a lymphatic vasculature, and prox1b does not specifically mark lymphatic endothelial cells. PLoS ONE 6, e28934.
97. Tso, P. and Balint, J. A. (1986). Formation and transport of chylomicrons by enterocytes to the lymphatics. Am. J. Physiol. 250, G715-G726.
98. Ullal, S. R., Kluge, T. H. and Gerbode, F. (1972). Functional and pathologic changes in the heart following chronic cardiac lymphatic obstruction. Surgery 71, 328-334.
99. van Amerongen, R., Fuerer, C., Mizutani, M. and Nusse, R. (2012). Wnt5a can both activate and repress Wnt/beta-catenin signaling during mouse embryonic development. Dev. Biol. 369, 101-114.
100. Van der Jagt, E. R. (1932). Memoirs: the origin and development of the anterior lymph-sacs in the sea-turtle (Thalassochelys caretta). Q. J. Microsc. Sci. 2, 151-163.
101. Van Der Putte, S. (1975). The early development of the lymphatic system in mouse embryos. Acta Morphol. Neerl. Scand. 13, 245-286.
102. van Impel, A., Zhao, Z., Hermkens, D. M. A., Roukens, M. G., Fischer, J. C., Peterson-Maduro J., Duckers, H., Ober, E. A., Ingham, P. W. and Schulte- Merker, S. (2014). Divergence of zebrafish and mouse lymphatic cell fate specification pathways. Development 141, 1228-1238.
103. Walls, J. R., Coultas, L., Rossant, J. and Henkelman, R. M. (2008). Threedimensional analysis of vascular development in the mouse embryo. PLoS ONE 3, e2853.
104. Wang, Y., Nakayama, M., Pitulescu, M. E., Schmidt, T. S., Bochenek, M. L., Sakakibara, A., Adams S., Davy, A., Deutsch, U., Luthi, U. et al. (2010). Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature 465, 483-486.
105. Wang, R. N., Green, J., Wang, Z., Deng, Y., Qiao, M., Peabody, M., Zhang, Q., Ye, J., Yan, Z., Denduluri, S. et al. (2014). Bone morphogenetic protein (BMP) signaling in development and human diseases. Genes Dis. 1, 87-105.
106. Wigle, J. T. and Oliver, G. (1999). Prox1 function is required for the development of the murine lymphatic system. Cell 98, 769-778.
107. 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.
108. Wiley, D. M., Kim, J.-D., Hao, J., Hong, C. C., Bautch, V. L. and Jin, S.-W. (2011). Distinct signalling pathways regulate sprouting angiogenesis from the dorsal aorta and the axial vein. Nat. Cell Biol. 13, 687-693.
109. Wilting, J., Aref, Y., Huang, R., Tomarev, S. I., Schweigerer, L., Christ, B., Valasek, P. and Papoutsi, M. (2006). Dual origin of avian lymphatics. Dev. Biol. 292, 165-173.
110. Yang, Y., Garcia-Verdugo, J. M., Soriano-Navarro, M., Srinivasan, R. S., Scallan, J. P., Singh, M. K., Epstein, J. A. and Oliver, G. (2012). Lymphatic endothelial progenitors bud from the cardinal vein and intersomitic vessels in mammalian embryos. Blood 120, 2340-2348.
111. Yaniv, K., Isogai, S., Castranova, D., Dye, L., Hitomi, J. and Weinstein, B. M. (2006). Live imaging of lymphatic development in the zebrafish. Nat. Med. 12, 711-716.
112. Yoshimatsu, Y., Lee, Y. G., Akatsu, Y., Taguchi, L., Suzuki, H. I., Cunha, S. I., Maruyama, K., Suzuki, Y., Yamazaki, T., Katsura, A. et al. (2013). Bone morphogenetic protein-9 inhibits lymphatic vessel formation via activin receptorlike kinase 1 during development and cancer progression. Proc. Natl. Acad. Sci. USA 110, 18940-18945.
113. 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.
114. Yu, M., Zhang, H., Liu, Y., He, Y., Yang, C., Du, Y., Wu, M., Zhang, G. and Gao, F. (2015). The cooperative role of S1P3 with LYVE-1 in LMW-HA-induced lymphangiogenesis. Exp. Cell Res. 336, 150-157.
115. Zheng, W., Tammela, T., Yamamoto, M., Anisimov, A., Holopainen, T., Kaijalainen, S., Karpanen T., Lehti, K., Yla-Herttuala, S. and Alitalo, K. (2011). Notch restricts lymphatic vessel sprouting induced by vascular endothelial growth factor. Blood 118, 1154-1162.
116. Zhong, T. P., Rosenberg, M., Mohideen, M.-A. P. L., Weinstein, B. and Fishman, M. C. (2000). gridlock, an HLH gene required for assembly of the aorta in zebrafish. Science 287, 1820-1824.
117. 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.