Lymphatic development

Birth Defects Research Part C - Embryo Today: Reviews

Volumn 87, Issue 3, 2009, Pages 222-231

  Butler, Matthew G ^a   Isogai, Sumio ^b   Weinstein, Brant M ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b IWATE MEDICAL UNIVERSITY   (Japan)

Author keywords

Lymphangiogeneis; Lymphatic; Lymphedema; Zebrafish

Indexed keywords

ADRENOMEDULLIN; CELL PROTEIN; CYCLIN E; CYCLIN E 1; EMILIN 1; EPHRIN B2; FIBROBLAST GROWTH FACTOR RECEPTOR 3; GLYCOPROTEIN; HERMES ANTIGEN; INTEGRIN; LYMPHATIC VESSEL ENDOTHELIAL HYALURONAN RECEPTOR 1; NEUROPILIN 2; PODOPLANIN; PROTEIN CCBE 1; PROTEIN COUPTF 2; PROTEIN KINASE SYK; PROTEIN SLP 76; PROTEIN SPRED 1; PROTEIN SPRED 2; RECEPTOR ACTIVITY MODIFYING PROTEIN 2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXC2; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFAT C1; TRANSCRIPTION FACTOR PROX 1; TRANSCRIPTION FACTOR SOX8; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3;

BLOOD VESSEL; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELL SUBPOPULATION; EMBRYO DEVELOPMENT; ENDOTHELIUM CELL; GENE MUTATION; HOMEOSTASIS; HUMAN; HYPOTRICHOSIS LYMPHEDEMA TELANGIECTASIA; LYMPHANGIOGENESIS; LYMPHATIC SYSTEM; LYMPHEDEMA; LYMPHEDEMA DISTICHIASIS; LYMPHOID CELL; MESENCHYME CELL; MILROY DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; LYMPHANGIOGENESIS; LYMPHATIC SYSTEM; LYMPHATIC VESSELS; MODELS, ANIMAL; SIGNAL TRANSDUCTION; URODELA; VERTEBRATES; ZEBRAFISH;

DANIO RERIO;

EID: 70349420002     PISSN: 1542975X     EISSN: None     Source Type: Journal    
DOI: 10.1002/bdrc.20155     Document Type: Review

References (84)

1. Abtahian F, Guerriero A, Sebzda E, et al. 2003. Regulation of blood and lymphatic vascular separation by signaling proteins SLP-76 and Syk. Science 299:247-251. (Pubitemid 36125210)
2. Achen MG, Jeltsch M, Kukk E, et al. 1998. Vascular endothelial growth factor D (VEGF-D) is a ligand for the tyrosine kinases VEGF receptor 2 (Flk1) and VEGF receptor 3 (Flt4). Proc Natl Acad Sci USA 95:548-553.
3. Aselli G. 1627. De Lacteibus sive Lacteis Venis, Quarto Vasorum Mesarai corum Genere novo invento. Milan: Mediolani.
4. Baldwin ME, Halford MM, Roufail S, et al. 2005. Vascular endothelial growth factor D is dispensable for development of the lymphatic system. Mol Cell Biol 25:2441-2449. (Pubitemid 40354637)
5. Baluk P, Fuxe J, Hashizume H, et al. 2007. Functionally specialized junctions between endothelial cells of lymphatic vessels. J Exp Med 204: 2349-2362. (Pubitemid 47529321)
6. Banerji S, Ni J, Wang SX, et al. 1999. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J Cell Biol 144:789-801. (Pubitemid 29234556)
7. Bell R, Brice G, Child AH, et al. 2001. Analysis of lymphoedema- distichiasis families for FOXC2 mutations reveals small insertions and deletions throughout the gene. Hum Genet 108:546-551. (Pubitemid 32700358)
8. Butler MG, Dagenais SL, Rockson SG, Glover TW. 2007. A novel VEGFR3 mutation causes Milroy disease. Am J Med Genet A 143:1212-1217.
9. Buttler K, Kreysing A, von Kaisenberg CS, et al. 2006. Mesenchymal cells with leukocyte and lymphendothelial characteristics in murine embryos. Dev Dyn 235:1554-1562. (Pubitemid 43787957)
10. Buttler K, Ezaki T, Wilting J. 2008. Proliferating mesodermal cells in murine embryos exhibiting macrophage and lymphendothelial characteristics. BMC Dev Biol 8:43. (Pubitemid 351678107)
11. Byzova TV, Goldman CK, Jankau J, et al. 2002. Adenovirus encoding vascular endothelial growth factor-D induces tissue-specific vascular patterns in vivo. Blood 99:4434-4442. (Pubitemid 34627212)
12. Cha YR, Weinstein BM. 2007. Visualization and experimental analysis of blood vessel formation using transgenic zebrafish. Birth Defects Res C Embryo Today 81:286-296.
13. Connell FC, Ostergaard P, Carver C, et al. 2009. Analysis of the coding regions of VEGFR3 and VEGFC in Milroy disease and other primary lymphoedemas. Hum Genet 124:625-631.
14. Dagenais SL, Hartsough RL, Erickson RP, et al. 2004. Foxc2 is expressed in developing lymphatic vessels and other tissues associated with lymphedema-distichiasis syndrome. Gene Expr Patterns 4:611-619.
15. Danussi C, Spessotto P, Petrucco A, et al. 2008. Emilin1 deficiency causes structural and functional defects of lymphatic vasculature. Mol Cell Biol 28:4026-4039. (Pubitemid 351812988)
16. Dixelius J, Makinen T, Wirzenius M, et al. 2003. Ligand-induced vascular endothelial growth factor receptor-3 (VEGFR-3) heterodimerization with VEGFR-2 in primary lymphatic endothelial cells regulates tyrosine phosphorylation sites. J Biol Chem 278: 40973-40979. (Pubitemid 37280919)
17. Enholm B, Karpanen T, Jeltsch M, et al. 2001. Adenoviral expression of vascular endothelial growth factor-C induces lymphangiogenesis in the skin. Circ Res 88:623-629. (Pubitemid 32275799)
18. Erickson RP, Dagenais SL, Caulder MS, et al. 2001. Clinical heterogeneity in lymphoedema-distichiasis with FOXC2 truncating mutations. J Med Genet 38:761-766. (Pubitemid 33032931)
19. Fang J, Dagenais SL, Erickson RP, et al. 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.
20. Finegold DN, Kimak MA, Lawrence EC, et al. 2001. Truncating mutations in FOXC2 cause multiple lymphedema syndromes. Hum Mol Genet 10:1185-1189.
21. Francois M, Caprini A, Hosking B, et al. 2008. Sox18 induces development of the lymphatic vasculature in mice. Nature 456:643-647.
22. Fritz-Six KL, Dunworth WP, Li M, Caron KM. 2008. Adrenomedullin signaling is necessary for murine lymphatic vascular development. J Clin Invest 118:40-50.
23. Gale NW, Prevo R, Espinosa J, et al. 2007. Normal lymphatic development and function in mice deficient for the lymphatic hyaluronan receptor LYVE- 1. Mol Cell Biol 27:595-604. (Pubitemid 46080127)
24. Gerli R, Ibba L, Fruschelli C. 1990. A fibrillar elastic apparatus around human lymph capillaries. Anat Embryol 181:281-286. (Pubitemid 20153529)
25. Hirashima M, Sano K, Morisada T, et al. 2008. Lymphatic vessel assembly is impaired in Aspp1-deficient mouse embryos. Dev Biol 316:149-159.
26. Hogan BM, Bos FL, Bussmann J, et al. 2009. Ccbe1 is required for embryonic lymphangiogenesis and venous sprouting. Nat Genet 41:396-398.
27. Hong YK, Harvey N, Noh YH, et al. 2002. Prox1 is a master control gene in the program specifying lymphatic endothelial cell fate. Dev Dyn 225:351-357. (Pubitemid 35265813)
28. Huntington G, McClure C. 1910. The anatomy and development of the jugular lymph sac in the domestic cat (Felis domestica). Am J Anat 10:177-311.
29. Ichise H, Ichise T, Ohtani O, Yoshida N. 2009. Phospholipase Cgamma2 is necessary for separation of blood and lymphatic vasculature in mice. Development 136:191-195.
30. Irrthum A, Devriendt K, Chitayat D, et al. 2003. Mutations in the transcription factor gene SOX18 underlie recessive and dominant forms of hypotrichosis-lymphedema-telangiectasia. Am J Hum Genet 72:1470-1478. (Pubitemid 36628386)
31. Isogai S, Hitomi J, Yaniv K, Weinstein BM. 2009. Zebrafish as a new animal model to study lymphangiogenesis. Anat Sci Int (in press).
32. Jeltsch M, Kaipainen A, Joukov V, et al. 1997. Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science 276:1423-1425. (Pubitemid 27235412)
33. Johnson NC, Dillard ME, Baluk P, et al. 2008. Lymphatic endothelial cell identity is reversible and its maintenance requires Prox1 activity. Genes Dev 22:3282-3291.
34. Joukov V, Pajusola K, Kaipainen A, et al. 1996. A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J 15:1751.
35. Joukov V, Sorsa T, Kumar V, et al. 1997. Proteolytic processing regulates receptor specificity and activity of VEGF-C. EMBO J 16:3898-3911. (Pubitemid 27281006)
36. Kaipainen A, Korhonen J, Mustonen T, et al. 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.
37. Kamei M, Weinstein BM. 2005. Longterm time-lapse fluorescence imaging of developing zebrafish. Zebrafish 2:113-123. (Pubitemid 41335552)
38. Kamei M, Isogai S, Weinstein BM. 2004. Imaging blood vessels in the zebrafish. Methods Cell Biol 76:51-74.
39. Kampmeier OF. 1969. Evolution and comparative morphology of the lymphatic system. Springfield: Charles C. Thomas Publisher.
40. Karkkainen MJ, Ferrell RE, Lawrence EC, et al. 2000. Missense mutations interfere with VEGFR-3 signalling in primary lymphoedema. Nat Genet 25:153-159.
41. Karkkainen MJ, Saaristo A, Jussila L, et al. 2001. Amodel for gene therapy of human hereditary lymphedema. Proc Natl Acad Sci USA 98:12677-12682. (Pubitemid 33020005)
42. Karkkainen MJ, Haiko P, Sainio K, 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. (Pubitemid 38081471)
43. Kreuger J, Nilsson I, Kerjaschki D, et al. 2006. Early lymph vessel development from embryonic stem cells. Arterioscler Thromb Vasc Biol 26:1073-1078. (Pubitemid 43732114)
44. Kriederman BM, Myloyde TL, Witte MH, et al. 2003. FOXC2 haploinsufficient mice are a model for human autosomal dominant lymphedema-distichiasis syndrome. Hum Mol Genet 12:1179-1185.
45. Kuchler AM, Gjini E, Peterson-Maduro J, et al. 2006. Development of the zebrafish lymphatic system requires VEGFC signaling. Curr Biol 16:1244-1248. (Pubitemid 43867297)
46. Kulkarni RM, Greenberg JM, Akeson AL. NFATc1 regulates lymphatic endothelial development. 2009. Mech Dev 126:350-365.
47. Lawson ND, Weinstein BM. 2002. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 248:307-318.
48. Leak LV, Burke JF. 1966. Fine structure of the lymphatic capillary and the adjoining connective tissue area. Am J Anat 118:785-809.
49. Lohela M, Bry M, Tammela T, Alitalo K. 2009. VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. Curr Opin Cell Biol 21:154-165.
50. Luong MX, Tam J, Lin Q, et al. 2009. Lack of lymphatic vessel phenotype in LYVE-1/CD44 double knockout mice. J Cell Physiol 219:430-437.
51. Makinen T, Veikkola T, Mustjoki S, 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. (Pubitemid 32848629)
52. Makinen T, Adams RH, Bailey J, et al. 2005. PDZ interaction site in ephrinB2 is required for the remodeling of lymphatic vasculature. Genes Dev 19:397-410. (Pubitemid 40189302)
53. Mishima K, Watabe T, Saito A, et al. 2007. Prox1 induces lymphatic endothelial differentiation via integrin alpha9 and other signaling cascades. Mol Biol Cell 18:1421-1429. (Pubitemid 46626636)
54. Norrmen C, Ivanov KI, Cheng J, et al. 2009. FOXC2 controls formation and maturation of lymphatic collecting vessels through cooperation with NFATc1. J Cell Biol 185:439-457.
55. Ny A, Koch M, Schneider M, et al. 2005. A genetic Xenopus laevis tadpole model to study lymphangiogenesis. Nat Med 11:998-1004. (Pubitemid 41294447)
56. Ny A, Koch M, Vandevelde W, et al. 2008. Role of VEGF-D and VEGFR-3 in developmental lymphangiogenesis, a chemicogenetic study in Xenopus tadpoles. Blood 112:1740-1749.
57. Oka M, Iwata C, Suzuki HI, et al. 2008. Inhibition of endogenous TGF-beta signaling enhances lymphangiogenesis. Blood 111:4571-4579.
58. Oliver G, Alitalo K. 2005. The lymphatic vasculature: recent progress and paradigms. Annu Rev Cell Dev Biol 21:457-483. (Pubitemid 41740643)
59. Petrova TV, Makinen T, Makela TP, et al. 2002. Lymphatic endothelial reprogramming of vascular endothelial cells by the Prox-1 homeobox transcription factor. EMBO J 21:4593-4599. (Pubitemid 34984346)
60. Petrova TV, Karpanen T, Norrmen C, et al. 2004. Defective valves and abnormal mural cell recruitment underlie lymphatic vascular failure in lymphedema distichiasis. Nat Med 10:974-981. (Pubitemid 39273739)
61. Rodrigues CO, Nerlick ST, White EL, et al. 2008. A Myc-Slug (Snail2)/Twist regulatory circuit directs vascular development. Development 135:1903-1911.
62. Rossi A, Weber E, Sacchi G, et al. 2007. Mechanotransduction in lymphatic endothelial cells. Lymphology 40:102-113.
63. Rusznyak I, Foldi M, Szabó G. 1960. Lymphatics and the lymph circulation. Oxford: Pergamon Press.
64. Sabin F. 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.
65. Sabin F. 1909. The lymphatic system in human embryos, with a consideration of the morphology of the system as a whole. Am J Anat 9:43-91.
66. Salameh A, Galvagni F, Bardelli M, et al. 2005. Direct recruitment of CRK and GRB2 to VEGFR-3 induces proliferation, migration, and survival of endothelial cells through the activation of ERK, AKT, and JNK pathways. Blood 106:3423-3431. (Pubitemid 41609177)
67. Samokhvalov IM, Samokhvalova NI, Nishikawa S. 2007. Cell tracing shows the contribution of the yolk sac to adult haematopoiesis. Nature 446:1056-1061. (Pubitemid 46676054)
68. Sebzda E, Hibbard C, Sweeney S, et al. 2006. Syk and Slp-76 mutant mice reveal a cell-autonomous hematopoietic cell contribution to vascular development. Dev Cell 11:349-361. (Pubitemid 44283944)
69. Shin JW, Min M, Larrieu-Lahargue F, et al. 2006. Prox1 promotes lineagespecific expression of fibroblast growth factor (FGF) receptor-3 in lymphatic endothelium: a role for FGF signaling in lymphangiogenesis. Mol Biol Cell 17:576-584. (Pubitemid 43191094)
70. Srinivasan RS, Dillard ME, Lagutin OV, et al. 2007. Lineage tracing demonstrates the venous origin of the mammalian lymphatic vasculature. Genes Dev 21:2422-2432.
71. Stadtfeld M, Graf T. 2005. Assessing the role of hematopoietic plasticity for endothelial and hepatocyte development by non-invasive lineage tracing. Development 132:203-213. (Pubitemid 40207979)
72. Taniguchi K, Kohno R, Ayada T, et al. 2007. Spreds are essential for embryonic lymphangiogenesis by regulating vascular endothelial growth factor receptor 3 signaling. Mol Cell Biol 27:4541-4550. (Pubitemid 46906575)
73. Tilney NL. 1971. Patterns of lymphatic drainage in the adult laboratory rat. J Anat 109(Part 3):369-383.
74. Vlahakis NE, Young BA, Atakilit A, et al. 2005. The lymphangiogenic vascular endothelial growth factors VEGF-C and -D are ligands for the integrin alpha9beta1. J Biol Chem 280:4544-4552. (Pubitemid 40288622)
75. Weinstein B. 2002. Vascular cell biology in vivo: a new piscine paradigm? Trends Cell Biol 12:439-445.
76. Wigle JT, Oliver G. 1999. Prox1 function is required for the development of the murine lymphatic system. Cell 98:769-778. (Pubitemid 29446894)
77. Wigle JT, Harvey N, Detmar M, et al. 2002. An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype. EMBO J 21:1505-1513. (Pubitemid 34614607)
78. Wilting J, Papoutsi M, Schneider M, Christ B. 2000. The lymphatic endothelium of the avian wing is of somitic origin. Dev Dyn 217:271-278. (Pubitemid 30131992)
79. Wilting J, Aref Y, Huang R, et al. 2006. Dual origin of avian lymphatics. Dev Biol 292:165-173.
80. Yamazaki T, Yoshimatsu Y, Morishita Y, et al. 2009. COUP-TFII regulates the functions of Prox1 in lymphatic endothelial cells through direct interaction. Genes Cells 14:425-434.
81. Yaniv K, Isogai S, Castranova D, et al. 2006. Live imaging of lymphatic development in the zebrafish. Nat Med 12:711-716. (Pubitemid 43865243)
82. You LR, Lin FJ, Lee CT, et al. 2005. Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity. Nature 435:98-104.
83. Yuan L, Moyon D, Pardanaud L, et al. 2002. Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development 129:4797-4806. (Pubitemid 35282411)
84. Zhang X, Groopman JE, Wang JF. 2005. Extracellular matrix regulates endothelial functions through interaction of VEGFR-3 and integrin alpha5beta1. J Cell Physiol 202:205-214.