Getting out and about: The emergence and morphogenesis of the vertebrate lymphatic vasculature

Development (Cambridge)

Volumn 140, Issue 9, 2013, Pages 1857-1870

  Koltowska, Katarzyna ^a   Betterman, Kelly L ^b   Harvey, Natasha L ^b,c   Hogan, Benjamin M ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b CENTRE FOR CANCER BIOLOGY   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Lymphatic vasculature; Morphogenesis; Vertebrate embryo

Indexed keywords

ADRENOMEDULLIN; CALCINEURIN; COLLAGEN TYPE 4; CONNEXIN 37; EPHRIN; EPHRIN B2; FIBRONECTIN; PODOPLANIN; RECEPTOR ACTIVITY MODIFYING PROTEIN 2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXC2; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR PROX1; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN;

ANGIOGENESIS; ANTERIOR POSTERIOR AXIS; BASEMENT MEMBRANE; EMBRYO DEVELOPMENT; EMBRYO INDUCTION; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENE INACTIVATION; HEMATOPOIETIC CELL; INTERNALIZATION; LYMPH VESSEL; LYMPHANGIOGENESIS; LYMPHATIC DRAINAGE; LYMPHATIC SYSTEM; LYMPHEDEMA; MEGAKARYOCYTE; MORPHOGENESIS; MOTONEURON; MOUSE; MOUSE EMBRYO; NONHUMAN; PDZ DOMAIN; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; SPROUTING; THROMBOCYTE AGGREGATION; VERTEBRATE; ZEBRA FISH;

ANIMALS; BIOLOGICAL EVOLUTION; CELL MOVEMENT; ENDOTHELIUM, VASCULAR; EPHRIN-B2; FORKHEAD TRANSCRIPTION FACTORS; HOMEODOMAIN PROTEINS; LYMPHANGIOGENESIS; LYMPHATIC VESSELS; MICE; MORPHOGENESIS; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS; ZEBRAFISH;

DANIO RERIO; VERTEBRATA;

EID: 84875981816     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.089565     Document Type: Review

References (134)

1. Abtahian, F., Guerriero, A., Sebzda, E., Lu, M. M., Zhou, R., Mocsai, A., Myers, E. E., Huang, B., Jackson, D. G., Ferrari, V. A. et al. (2003). Regulation of blood and lymphatic vascular separation by signaling proteins SLP-76 and Syk. Science 299, 247-251.
2. Alders, M., Hogan, B. M., Gjini, E., Salehi, F., Al-Gazali, L., Hennekam, E. A., Holmberg, E. E., Mannens, M. 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.
3. Alitalo, K. (2011). The lymphatic vasculature in disease. Nat. Med. 17, 1371-1380.
4. 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.
5. Au, A. C., Hernandez, P. A., Lieber, E., Nadroo, A. M., Shen, Y. M., Kelley, K. A., Gelb, B. D. and Diaz, G. A. (2010). Protein tyrosine phosphatase PTPN14 is a regulator of lymphatic function and choanal development in humans. Am. J. Hum. Genet. 87, 436-444.
6. Augustin, H. G., Koh, G. Y., Thurston, G. and Alitalo, K. (2009). Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat. Rev. Mol. Cell Biol. 10, 165-177.
7. Baluk, P., Fuxe, J., Hashizume, H., Romano, T., Lashnits, E., Butz, S., Vestweber, D., Corada, M., Molendini, C., Dejana, E. et al. (2007). Functionally specialized junctions between endothelial cells of lymphatic vessels. J. Exp. Med. 204, 2349-2362.
8. Bazigou, E. and Makinen, T. (2013). Flow control in our vessels: vascular valves make sure there is no way back. Cell. Mol. Life Sci. 70, 1055-1066.
9. Bazigou, E., Xie, S., Chen, C., Weston, A., Miura, N., Sorokin, L., Adams, R., Muro, A. F., Sheppard, D. and Makinen, T. (2009). Integrin-alpha9 is required for fibronectin matrix assembly during lymphatic valve morphogenesis. Dev. Cell 17, 175-186.
10. Bazigou, E., Lyons, O. T., Smith, A., Venn, G. E., Cope, C., Brown, N. A. and Makinen, T. (2011). Genes regulating lymphangiogenesis control venous valve formation and maintenance in mice. J. Clin. Invest. 121, 2984-2992.
11. 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.
12. Böhmer, R., Neuhaus, B., Bühren, S., Zhang, D., Stehling, M., Böck, B. and Kiefer, F. (2010). Regulation of developmental lymphangiogenesis by Syk(+) leukocytes. Dev. Cell 18, 437-449.
13. 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.
14. Bouvrée, K., Brunet, I., Del Toro, R., Gordon, E., Prahst, C., Cristofaro, B., Mathivet, T., Xu, Y., Soueid, J., Fortuna, V. et al. (2012). Semaphorin3A, Neuropilin-1, and PlexinA1 are required for lymphatic valve formation. Circ. Res. 111, 437-445.
15. Brice, G., Mansour, S., Bell, R., Collin, J. R., Child, A. H., Brady, A. F., Sarfarazi, M., Burnand, K. G., Jeffery, S., Mortimer, P. et al. (2002). Analysis of the phenotypic abnormalities in lymphoedema-distichiasis syndrome in 74 patients with FOXC2 mutations or linkage to 16q24. J. Med. Genet. 39, 478-483.
16. Bussmann, J., Bos, F. L., Urasaki, A., Kawakami, K., Duckers, H. J. and Schulte-Merker, S. (2010). Arteries provide essential guidance cues for lymphatic endothelial cells in the zebrafish trunk. Development 137, 2653-2657.
17. Carramolino, L., Fuentes, J., García-Andrés, C., Azcoitia, V., Riethmacher, D. and Torres, M. (2010). Platelets play an essential role in separating the blood and lymphatic vasculatures during embryonic angiogenesis. Circ. Res. 106, 1197-1201.
18. 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.
19. 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.
20. Clark, E. R. (1915). An anomaly of the thoracic duct with a bearing on the embryology of the lymphatic system. Contributions to Embryology 2, 45-54.
21. Connell, F., Kalidas, K., Ostergaard, P., Brice, G., Homfray, T., Roberts, L., Bunyan, D. J., Mitton, S., Mansour, S., Mortimer, P. et al.; Lymphoedema Consortium (2010). Linkage and sequence analysis indicate that CCBE1 is mutated in recessively inherited generalised lymphatic dysplasia. Hum. Genet. 127, 231-241.
22. D'Amico, G., Jones, D. T., Nye, E., Sapienza, K., Ramjuan, A. R., Reynolds, L. E., Robinson, S. D., Kostourou, V., Martinez, D., Aubyn, D. et al. (2009). Regulation of lymphatic-blood vessel separation by endothelial Rac1. Development 136, 4043-4053.
23. D'Amico, G., Korhonen, E. A., Waltari, M., Saharinen, P., Laakkonen, P. and Alitalo, K. (2010). Loss of endothelial Tie1 receptor impairs lymphatic vessel development-brief report. Arterioscler. Thromb. Vasc. Biol. 30, 207-209.
24. Dahl Ejby Jensen, L., Cao, R., Hedlund, E.-M., Söll, I., Lundberg, J. O., Hauptmann, G., Steffensen, J. F. and Cao, Y. (2009). Nitric oxide permits hypoxia-induced lymphatic perfusion by controlling arterial-lymphatic conduits in zebrafish and glass catfish. Proc. Natl. Acad. Sci. USA 106, 18408-18413.
25. Debrincat, M. A., Josefsson, E. C., James, C., Henley, K. J., Ellis, S., Lebois, M., Betterman, K. L., Lane, R. M., Rogers, K. L., White, M. J. et al. (2012). Mcl-1 and Bcl-x(L) coordinately regulate megakaryocyte survival. Blood 119, 5850-5858.
26. Del Giacco, L., Pistocchi, A. and Ghilardi, A. (2010). prox1b Activity is essential in zebrafish lymphangiogenesis. PLoS ONE 5, e13170.
27. Delamere, G. P. and Cuneo, P. B. (1903). The Lymphatics: General Anatomy of the Lymphatics by G. Delamere, Special Study of the Lymphatics in Different Parts of the Body by P. Poirier and B Cuneo. Westminster: Archibald Constable.
28. Dellinger, M., Hunter, R., Bernas, M., Gale, N., Yancopoulos, G., Erickson, R. and Witte, M. (2008). Defective remodeling and maturation of the lymphatic vasculature in Angiopoietin-2 deficient mice. Dev. Biol. 319, 309-320.
29. 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.
30. Eilken, H. M. and Adams, R. H. (2010). Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr. Opin. Cell Biol. 22, 617-625.
31. Fang, J., Dagenais, S. L., Erickson, R. P., Arlt, M. F., Glynn, M. W., Gorski, J. L., Seaver, L. H. and Glover, T. W. (2000). Mutations in FOXC2 (MFH-1), a forkhead family transcription factor, are responsible for the hereditary lymphedema-distichiasis syndrome. Am. J. Hum. Genet. 67, 1382-1388.
32. Ferrell, R. E., Levinson, K. L., Esman, J. H., Kimak, M. A., Lawrence, E. C., Barmada, M. M. and Finegold, D. N. (1998). Hereditary lymphedema: evidence for linkage and genetic heterogeneity. Hum. Mol. Genet. 7, 2073-2078.
33. Ferrell, R. E., Baty, C. J., Kimak, M. A., Karlsson, J. M., Lawrence, E. C., Franke-Snyder, M., Meriney, S. D., Feingold, E. and Finegold, D. N. (2010). GJC2 missense mutations cause human lymphedema. Am. J. Hum. Genet. 86, 943-948.
34. Finegold, D. N., Kimak, M. A., Lawrence, E. C., Levinson, K. L., Cherniske, E. M., Pober, B. R., Dunlap, J. W. and Ferrell, R. E. (2001). Truncating mutations in FOXC2 cause multiple lymphedema syndromes. Hum. Mol. Genet. 10, 1185-1189.
35. Flanagan, J. G. and Vanderhaeghen, P. (1998). The ephrins and Eph receptors in neural development. Annu. Rev. Neurosci. 21, 309-345.
36. 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.
37. 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.
38. 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.
39. Fritz-Six, K. L., Dunworth, W. P., Li, M. and Caron, K. M. (2008). Adrenomedullin signaling is necessary for murine lymphatic vascular development. J. Clin. Invest. 118, 40-50.
40. Fu, J., Gerhardt, H., McDaniel, J. M., Xia, B., Liu, X., Ivanciu, L., Ny, A., Hermans, K., Silasi-Mansat, R., McGee, S. et al. (2008). Endothelial cell Oglycan deficiency causes blood/lymphatic misconnections and consequent fatty liver disease in mice. J. Clin. Invest. 118, 3725-3737.
41. Gale, N. W., Thurston, G., Hackett, S. F., Renard, R., Wang, Q., McClain, J., Martin, C., Witte, C., Witte, M. H., Jackson, D. et al. (2002). Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by Angiopoietin-1. Dev. Cell 3, 411-423.
42. Galvagni, F., Pennacchini, S., Salameh, A., Rocchigiani, M., Neri, F., Orlandini, M., Petraglia, F., Gotta, S., Sardone, G. L., Matteucci, G. et al. (2010). Endothelial cell adhesion to the extracellular matrix induces c-Srcdependent VEGFR-3 phosphorylation without the activation of the receptor intrinsic kinase activity. Circ. Res. 106, 1839-1848.
43. Geudens, I. and Gerhardt, H. (2011). Coordinating cell behaviour during blood vessel formation. Development 138, 4569-4583.
44. 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.
45. 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.
46. Hägerling, R., Pollmann, C., Andreas, M., Schmidt, C., Nurmi, H., Adams, R. H., Alitalo, K., Andresen, V., Schulte-Merker, S. and Kiefer, F. (2013). A novel multistep mechanism for initial lymphangiogenesis in mouse embryos based on ultramicroscopy. EMBO J. 32, 629-644.
47. Hazan, F., Ostergaard, P., Ozturk, T., Kantekin, E., Atlihan, F., Jeffery, S. and Ozkinay, F. (2012). A novel KIF11 mutation in a Turkish patient with microcephaly, lymphedema, and chorioretinal dysplasia from a consanguineous family. Am. J. Med. Genet. 158A, 1686-1689.
48. Hermans, K., Claes, F., Vandevelde, W., Zheng, W., Geudens, I., Orsenigo, F., De Smet, F., Gjini, E., Anthonis, K., Ren, B. et al. (2010). Role of synectin in lymphatic development in zebrafish and frogs. Blood 116, 3356-3366.
49. Hewson, W. and Hunter, W. (1769). An account of the lymphatic system in fish. By the same. Philosophical Transactions (1683-1775) 59, 204-215.
50. Hogan, B. M., Bos, F. L., Bussmann, J., Witte, M., Chi, N. C., Duckers, H. J. and Schulte-Merker, S. (2009a). Ccbe1 is required for embryonic lymphangiogenesis and venous sprouting. Nat. Genet. 41, 396-398.
51. Hogan, B. M., Herpers, R., Witte, M., Heloterä, H., Alitalo, K., Duckers, H. J. and Schulte-Merker, S. (2009b). Vegfc/Flt4 signalling is suppressed by Dll4 in developing zebrafish intersegmental arteries. Development 136, 4001-4009.
52. 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.
53. Hosking, B., François, M., Wilhelm, D., Orsenigo, F., Caprini, A., Svingen, T., Tutt, D., Davidson, T., Browne, C., Dejana, E. et al. (2009). Sox7 and Sox17 are strain-specific modifiers of the lymphangiogenic defects caused by Sox18 dysfunction in mice. Development 136, 2385-2391.
54. Hoyer, H. (1934). Das Lymphgefäßsystem der Wirbeltiere vom Standpunkte der vergleichenden Anatomie. Mem. Acad. Polon. Sci. Lett. Med. 1, 1-205.
55. Huang, X. Z., Wu, J. F., Ferrando, R., Lee, J. H., Wang, Y. L., Farese, R. V., Jr and Sheppard, D. (2000). Fatal bilateral chylothorax in mice lacking the integrin alpha9beta1. Mol. Cell. Biol. 20, 5208-5215.
56. Ichise, H., Ichise, T., Ohtani, O. and Yoshida, N. (2009). Phospholipase Cgamma2 is necessary for separation of blood and lymphatic vasculature in mice. Development 136, 191-195.
57. Irrthum, A., Karkkainen, M. J., Devriendt, K., Alitalo, K. and Vikkula, M. (2000). Congenital hereditary lymphedema caused by a mutation that inactivates VEGFR3 tyrosine kinase. Am. J. Hum. Genet. 67, 295-301.
58. Irrthum, A., Devriendt, K., Chitayat, D., Matthijs, G., Glade, C., Steijlen, P. M., Fryns, J. P., Van Steensel, M. A. and Vikkula, M. (2003). Mutations in the transcription factor gene SOX18 underlie recessive and dominant forms of hypotrichosis-lymphedema-telangiectasia. Am. J. Hum. Genet. 72, 1470-1478.
59. 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.
60. Isogai, S., Hitomi, J., Yaniv, K. and Weinstein, B. M. (2009). Zebrafish as a new animal model to study lymphangiogenesis. Anat. Sci. Int. 84, 102-111.
61. 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.
62. 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.
63. Jurisic, G., Maby-El Hajjami, H., Karaman, S., Ochsenbein, A. M., Alitalo, A., Siddiqui, S. S., Ochoa Pereira, C., Petrova, T. V. and Detmar, M. (2012). An unexpected role of semaphorin3a-neuropilin-1 signaling in lymphatic vessel maturation and valve formation. Circ. Res. 111, 426-436.
64. Kampmeier, O. F. (1928). The genetic history of the valves in the lymphatic system of man. Am. J. Anat. 40, 413-457.
65. Kampmeier, O. F. (1969). Evolution and Comparative Morphology of The Lymphatic System. Springfield, IL: Charles C. Thomas.
66. Kanady, J. D., Dellinger, M. T., Munger, S. J., Witte, M. H. and Simon, A. M. (2011). Connexin37 and Connexin43 deficiencies in mice disrupt lymphatic valve development and result in lymphatic disorders including lymphedema and chylothorax. Dev. Biol. 354, 253-266.
67. 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.
68. Karkkainen, M. J., Ferrell, R. E., Lawrence, E. C., Kimak, M. A., Levinson, K. L., McTigue, M. A., Alitalo, K. and Finegold, D. N. (2000). Missense mutations interfere with VEGFR-3 signalling in primary lymphoedema. Nat. Genet. 25, 153-159.
69. Karkkainen, M. J., Saaristo, A., Jussila, L., Karila, K. A., Lawrence, E. C., Pajusola, K., Bueler, H., Eichmann, A., Kauppinen, R., Kettunen, M. I. et al. (2001). A model for gene therapy of human hereditary lymphedema. Proc. Natl. Acad. Sci. USA 98, 12677-12682.
70. 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.
71. Kazenwadel, J., Secker, G. A., Liu, Y. J., Rosenfeld, J. A., Wildin, R. S., Cuellar-Rodriguez, J., Hsu, A. P., Dyack, S., Fernandez, C. V., Chong, C.-E. et al. (2012). Loss-of-function germline GATA2 mutations in patients with MDS/AML or MonoMAC syndrome and primary lymphedema reveal a key role for GATA2 in the lymphatic vasculature. Blood 119, 1283-1291.
72. Kim, H., Nguyen, V. P. K. H., 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.
73. Knower, H. M. (1908). Symposium on the development and structure of the lymphatic system. VI. The origin and development of the anterior lymph hearts and the subcutaneous lymph sacs in the frog. Anat. Rec. 2, 59-62.
74. 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.
75. Kuijper, S., Turner, C. J. and Adams, R. H. (2007). Regulation of angiogenesis by Eph-ephrin interactions. Trends Cardiovasc. Med. 17, 145-151.
76. 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.
77. Lauweryns, J. M. and Boussauw, L. (1973). The ultrastructure of lymphatic valves in the adult rabbit lung. Z. Zellforsch. Mikrosk. Anat. 143, 149-168.
78. Lawson, N. D., Mugford, J. W., Diamond, B. A. and Weinstein, B. M. (2003). Phospholipase C gamma-1 is required downstream of vascular endothelial growth factor during arterial development. Genes Dev. 17, 1346-1351.
79. Leak, L. V. and Burke, J. F. (1968). Ultrastructural studies on the lymphatic anchoring filaments. J. Cell Biol. 36, 129-149.
80. 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.
81. 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.
82. Lim, K. C., Hosoya, T., Brandt, W., Ku, C. J., Hosoya-Ohmura, S., Camper, S. A., Yamamoto, M. and Engel, J. D. (2012). Conditional Gata2 inactivation results in HSC loss and lymphatic mispatterning. J. Clin. Invest. 122, 3705-3717.
83. 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.
84. Lord, R. S. (1968). The white veins: conceptual difficulties in the history of the lymphatics. Med. Hist. 12, 174-184.
85. Ma, G. C., Liu, C. S., Chang, S. P., Yeh, K. T., Ke, Y. Y., Chen, T. H., Wang, B. B., Kuo, S. J., Shih, J. C. and Chen, M. (2008). A recurrent ITGA9 missense mutation in human fetuses with severe chylothorax: possible correlation with poor response to fetal therapy. Prenat. Diagn. 28, 1057-1063.
86. Makinen, T., Olofsson, B., Karpanen, T., Hellman, U., Soker, S., Klagsbrun, M., Eriksson, U. and Alitalo, K. (1999). Differential binding of vascular endothelial growth factor B splice and proteolytic isoforms to neuropilin-1. J. Biol. Chem. 274, 21217-21222.
87. Mäkinen, T., Jussila, L., Veikkola, T., Karpanen, T., Kettunen, M. I., Pulkkanen, K. J., Kauppinen, R., Jackson, D. G., Kubo, H., Nishikawa, S. et al. (2001). Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3. Nat. Med. 7, 199-205.
88. Mäkinen, T., Adams, R. H., Bailey, J., Lu, Q., Ziemiecki, A., Alitalo, K., Klein, R. and Wilkinson, G. A. (2005). PDZ interaction site in ephrinB2 is required for the remodeling of lymphatic vasculature. Genes Dev. 19, 397-410.
89. Mellor, R. H., Hubert, C. E., Stanton, A. W., Tate, N., Akhras, V., Smith, A., Burnand, K. G., Jeffery, S., Mäkinen, T., Levick, J. R. et al. (2010). Lymphatic dysfunction, not aplasia, underlies Milroy disease. Microcirculation 17, 281-296.
90. Munger, S. J., Kanady, J. D. and Simon, A. M. (2013). Absence of venous valves in mice lacking Connexin37. Dev. Biol. 373, 338-348.
91. Navankasattusas, S., Whitehead, K. J., Suli, A., Sorensen, L. K., Lim, A. H., Zhao, J., Park, K. W., Wythe, J. D., Thomas, K. R., Chien, C. B. et al. (2008). The netrin receptor UNC5B promotes angiogenesis in specific vascular beds. Development 135, 659-667.
92. Navas, V., O'Morchoe, P. J. and O'Morchoe, C. C. (1991). Lymphatic valves of the rat pancreas. Lymphology 24, 146-154.
93. 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.
94. Norrmén, C., Ivanov, K. I., Cheng, J., Zangger, N., Delorenzi, M., Jaquet, M., Miura, N., Puolakkainen, P., Horsley, V., Hu, J. et al. (2009). FOXC2 controls formation and maturation of lymphatic collecting vessels through cooperation with NFATc1. J. Cell Biol. 185, 439-457.
95. Ny, A., Koch, M., Schneider, M., Neven, E., Tong, R. T., Maity, S., Fischer, C., Plaisance, S., Lambrechts, D., Héligon, C. et al. (2005). A genetic Xenopus laevis tadpole model to study lymphangiogenesis. Nat. Med. 11, 998-1004.
96. 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.
97. Oliver, G. (2004). Lymphatic vasculature development. Nat. Rev. Immunol. 4, 35-45.
98. Oliver, G. and Srinivasan, R. S. (2010). Endothelial cell plasticity: how to become and remain a lymphatic endothelial cell. Development 137, 363-372.
99. Osada, M., Inoue, O., Ding, G., Shirai, T., Ichise, H., Hirayama, K., Takano, K., Yatomi, Y., Hirashima, M., Fujii, H. et al. (2012). Platelet activation receptor CLEC-2 regulates blood/lymphatic vessel separation by inhibiting proliferation, migration, and tube formation of lymphatic endothelial cells. J. Biol. Chem. 287, 22241-22252.
100. Ostergaard, P., Simpson, M. A., Brice, G., Mansour, S., Connell, F. C., Onoufriadis, A., Child, A. H., Hwang, J., Kalidas, K., Mortimer, P. S. et al. (2011a). Rapid identification of mutations in GJC2 in primary lymphoedema using whole exome sequencing combined with linkage analysis with delineation of the phenotype. J. Med. Genet. 48, 251-255.
101. Ostergaard, P., Simpson, M. A., Connell, F. C., Steward, C. G., Brice, G., Woollard, W. J., Dafou, D., Kilo, T., Smithson, S., Lunt, P. et al. (2011b). Mutations in GATA2 cause primary lymphedema associated with a predisposition to acute myeloid leukemia (Emberger syndrome). Nat. Genet. 43, 929-931.
102. Ostergaard, P., Simpson, M. A., Mendola, A., Vasudevan, P., Connell, F. C., van Impel, A., Moore, A. T., Loeys, B. L., Ghalamkarpour, A., Onoufriadis, A. et al. (2012). Mutations in KIF11 cause autosomal-dominant microcephaly variably associated with congenital lymphedema and chorioretinopathy. Am. J. Hum. Genet. 90, 356-362.
103. Petrova, T. V., Karpanen, T., Norrmén, C., Mellor, R., Tamakoshi, T., Finegold, D., Ferrell, R., Kerjaschki, D., Mortimer, P., Ylä-Herttuala, S. et al. (2004). Defective valves and abnormal mural cell recruitment underlie lymphatic vascular failure in lymphedema distichiasis. Nat. Med. 10, 974-981.
104. Peyrot, S. M., Martin, B. L. and Harland, R. M. (2010). Lymph heart musculature is under distinct developmental control from lymphatic endothelium. Dev. Biol. 339, 429-438.
105. Planas-Paz, L., Strilić, B., Goedecke, A., Breier, G., Fässler, R. and Lammert, E. (2012). Mechanoinduction of lymph vessel expansion. EMBO J. 31, 788-804.
106. Qu, X., Tompkins, K., Batts, L. E., Puri, M. and Baldwin, S. (2010). Abnormal embryonic lymphatic vessel development in Tie1 hypomorphic mice. Development 137, 1285-1295.
107. Rodriguez-Niedenführ, M., Papoutsi, M., Christ, B., Nicolaides, K. H., von Kaisenberg, C. S., Tomarev, S. I. and Wilting, J. (2001). Prox1 is a marker of ectodermal placodes, endodermal compartments, lymphatic endothelium and lymphangioblasts. Anat. Embryol. (Berl.) 204, 399-406.
108. 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.
109. Sabine, A., Agalarov, Y., Maby-El Hajjami, H., Jaquet, M., Hägerling, R., Pollmann, C., Bebber, D., Pfenniger, A., Miura, N., Dormond, O. et al. (2012). Mechanotransduction, PROX1, and FOXC2 cooperate to control connexin37 and calcineurin during lymphatic-valve formation. Dev. Cell 22, 430-445.
110. Sebzda, E., Hibbard, C., Sweeney, S., Abtahian, F., Bezman, N., Clemens, G., Maltzman, J. S., Cheng, L., Liu, F., Turner, M. et al. (2006). Syk and Slp-76 mutant mice reveal a cell-autonomous hematopoietic cell contribution to vascular development. Dev. Cell 11, 349-361.
111. Smith, R. O. (1949). Lymphatic contractility; a possible intrinsic mechanism of lymphatic vessels for the transport of lymph. J. Exp. Med. 90, 497-509.
112. Soker, S., Takashima, S., Miao, H. Q., Neufeld, G. and Klagsbrun, M. (1998). Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92, 735-745.
113. 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.
114. 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.
115. 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.
116. Steffensen, J. F. and Lomholt, J. P. (1992). The secondary vascular system. In Fish Physiology, Vol. 12, Part A (ed. D. J. R. W. S. Hoar and A. P. Farrell). California: Academic Press.
117. Suzuki-Inoue, K., Inoue, O., Ding, G., Nishimura, S., Hokamura, K., Eto, K., Kashiwagi, H., Tomiyama, Y., Yatomi, Y., Umemura, K. et al. (2010). Essential in vivo roles of the C-type lectin receptor CLEC-2: embryonic/neonatal lethality of CLEC-2-deficient mice by blood/lymphatic misconnections and impaired thrombus formation of CLEC-2-deficient platelets. J. Biol. Chem. 285, 24494-24507.
118. Tammela, T., Zarkada, G., Nurmi, H., Jakobsson, L., Heinolainen, K., Tvorogov, D., Zheng, W., Franco, C. A., Murtomäki, A., Aranda, E. et al. (2011). VEGFR-3 controls tip to stalk conversion at vessel fusion sites by reinforcing Notch signalling. Nat. Cell Biol. 13, 1202-1213.
119. 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.
120. Uhrin, P., Zaujec, J., Breuss, J. M., Olcaydu, D., Chrenek, P., Stockinger, H., Fuertbauer, E., Moser, M., Haiko, P., Fässler, R. et al. (2010). Novel function for blood platelets and podoplanin in developmental separation of blood and lymphatic circulation. Blood 115, 3997-4005.
121. van der Putte, S. C. (1975). The early development of the lymphatic system in mouse embryos. Acta Morphol. Neerl. Scand. 13, 245-286.
122. Veikkola, T., Jussila, L., Makinen, T., Karpanen, T., Jeltsch, M., Petrova, T. V., Kubo, H., Thurston, G., McDonald, D. M., Achen, M. G. et al. (2001). Signalling via vascular endothelial growth factor receptor-3 is sufficient for lymphangiogenesis in transgenic mice. EMBO J. 20, 1223-1231.
123. Wang, Y., Nakayama, M., Pitulescu, M. E., Schmidt, T. S., Bochenek, M. L., Sakakibara, A., Adams, S., Davy, A., Deutsch, U., Lüthi, U. et al. (2010). Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature 465, 483-486.
124. Wigle, J. T. and Oliver, G. (1999). Prox1 function is required for the development of the murine lymphatic system. Cell 98, 769-778.
125. 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.
126. Wilson, B. D., Ii, M., Park, K. W., Suli, A., Sorensen, L. K., Larrieu-Lahargue, F., Urness, L. D., Suh, W., Asai, J., Kock, G. A. H. et al. (2006). Netrins promote developmental and therapeutic angiogenesis. Science 313, 640-644.
127. 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.
128. Wise, L. M., Veikkola, T., Mercer, A. A., Savory, L. J., Fleming, S. B., Caesar, C., Vitali, A., Makinen, T., Alitalo, K. and Stacker, S. A. (1999). Vascular endothelial growth factor (VEGF)-like protein from orf virus NZ2 binds to VEGFR2 and neuropilin-1. Proc. Natl. Acad. Sci. USA 96, 3071-3076.
129. 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 to Cells 14, 425-434.
130. Yang, Y., García-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.
131. 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.
132. Yuan, L., Moyon, D., Pardanaud, L., Bréant, C., Karkkainen, M. J., Alitalo, K. and Eichmann, A. (2002). Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development 129, 4797-4806.
133. 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.
134. Zhuo, W., Jia, L., Song, N., Lu, X. A., Ding, Y., Wang, X., Song, X., Fu, Y. and Luo, Y. (2012). The CXCL12-CXCR4 chemokine pathway: a novel axis regulates lymphangiogenesis. Clin. Cancer Res. 18, 5387-5398.