Lymphangiogenesis in development and human disease (original) (raw)

• Hirakawa, S. & Detmar, M. New insights into the biology and pathology of the cutaneous lymphatic system. J. Dermatol. Sci. 35, 1–8 (2004).
  Article CAS PubMed Google Scholar
• Oliver, G. Lymphatic vasculature development. Nature Rev. Immunol. 4, 35–45 (2004).
  Article CAS Google Scholar
• Tammela, T., Petrova, T. V. & Alitalo, K. Molecular lymphangiogenesis: new players. Trends Cell Biol. 15, 434–441 (2005).
  Article CAS PubMed Google Scholar
• Kaipainen, A. et al. Expression of the fms-like tyrosine kinase FLT4 gene becomes restricted to lymphatic endothelium during development. Proc. Natl Acad. Sci. USA 92, 3566–3570 (1995).
  Article ADS CAS PubMed PubMed Central Google Scholar
• Achen, M. G. et al. 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 (1998).
  Article ADS CAS PubMed PubMed Central Google Scholar
• Joukov, V. et al. 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, 290–298 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Jeltsch, M. et al. Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science 276, 1423–1425 (1997).
  Article CAS PubMed Google Scholar
• Mäkinen, T. et al. Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3. EMBO J. 20, 4762–4773 (2001).
  Article PubMed PubMed Central Google Scholar
• Karkkainen, M. J. et al. A model for gene therapy of human hereditary lymphedema. Proc. Natl Acad. Sci. USA 98, 12677–12682 (2001).
  Article ADS CAS PubMed PubMed Central Google Scholar
• Yuan, L. et al. Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development 129, 4797–4806 (2002).
  Article CAS PubMed Google Scholar
• Joukov, V. et al. Proteolytic processing regulates receptor specificity and activity of VEGF-C. EMBO J. 16, 3898–3911 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Cao, Y. et al. Vascular endothelial growth factor C induces angiogenesis in vivo. Proc. Natl Acad. Sci. USA 95, 14389–14392 (1998).
  Article ADS CAS PubMed PubMed Central Google Scholar
• Stacker, S. A. et al. Biosynthesis of vascular endothelial growth factor-D involves proteolytic processing which generates non-covalent homodimers. J. Biol. Chem. 274, 32127–32136 (1999).
  Article CAS PubMed Google Scholar
• Rissanen, T. T. et al. VEGF-D is the strongest angiogenic and lymphangiogenic effector among VEGFs delivered into skeletal muscle via adenoviruses. Circ. Res. 92, 1098–1106 (2003).
  Article CAS PubMed Google Scholar
• Nagy, J. A. et al. Vascular permeability factor/vascular endothelial growth factor induces lymphangiogenesis as well as angiogenesis. J. Exp. Med. 196, 1497–1506 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Karkkainen, M. J. et al. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nature Immunol. 5, 74–80 (2004).
  Article CAS Google Scholar
• Gannon, G. et al. Overexpression of vascular endothelial growth factor-A165 enhances tumor angiogenesis but not metastasis during beta-cell carcinogenesis. Cancer Res. 62, 603–608 (2002).
  CAS PubMed Google Scholar
• Oh, S. J. et al. VEGF and VEGF-C: specific induction of angiogenesis and lymphangiogenesis in the differentiated avian chorioallantoic membrane. Dev. Biol. 188, 96–109 (1997).
  Article CAS PubMed Google Scholar
• Cursiefen, C. et al. VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J. Clin. Invest. 113, 1040–1050 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Baluk, P. et al. Pathogenesis of persistent lymphatic vessel hyperplasia in chronic airway inflammation. J. Clin. Invest. 115, 247–257 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Wang, J. F., Zhang, X. F. & Groopman, J. E. Stimulation of beta 1 integrin induces tyrosine phosphorylation of vascular endothelial growth factor receptor-3 and modulates cell migration. J. Biol. Chem. 276, 41950–41957 (2001).
  Article CAS PubMed Google Scholar
• Vlahakis, N. E., Young, B. A., Atakilit, A. & Sheppard, D. The lymphangiogenic vascular endothelial growth factors VEGF-C and -D are ligands for the integrin alpha9beta1. J. Biol. Chem. 280, 4544–4552 (2005).
  Article CAS PubMed Google Scholar
• Huang, X. Z. et al. Fatal bilateral chylothorax in mice lacking the integrin alpha9beta1. Mol. Cell Biol. 20, 5208–5215 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Zhang, X. et al. KSHV activation of VEGFR-3 alters endothelial function and enhances infection. J. Biol. Chem. 280, 26216–26224 (2005).
  Article CAS PubMed Google Scholar
• Kubo, H. et al. Blockade of vascular endothelial growth factor receptor-3 signaling inhibits fibroblast growth factor-2-induced lymphangiogenesis in mouse cornea. Proc. Natl Acad. Sci. USA 99, 8868–8873 (2002).
  Article ADS CAS PubMed PubMed Central Google Scholar
• Cao, R. et al. PDGF-BB induces intratumoral lymphangiogenesis and promotes tumour metastasis. Cancer Cell 6, 333–345 (2004).
  Article CAS PubMed Google Scholar
• Kajiya, K., Hirakawa, S., Ma, B., Drinnenberg, I. & Detmar, M. Hepatocyte growth factor promotes lymphatic vessel formation and function. EMBO J. 24, 2885–2895 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Sabin, F. R. The lymphatic system in human embryos, with a consideration of the morphology of the system as a whole. Am. J. Anat. 9, 43–91 (1909).
  Article Google Scholar
• Wigle, J. T. & Oliver, G. Prox1 function is required for the development of the murine lymphatic system. Cell 98, 769–778 (1999).
  Article CAS PubMed Google Scholar
• Wigle, J. T. et al. An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype. EMBO J. 21, 1505–1513 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Hong, Y. K. et al. Prox1 is a master control gene in the program specifying lymphatic endothelial cell fate. Dev. Dyn. 225, 351–357 (2002).
  Article CAS PubMed Google Scholar
• Petrova, T. V. et al. Lymphatic endothelial reprogramming of vascular endothelial cells by the Prox-1 homeobox transcription factor. EMBO J. 21, 4593–4599. (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Harvey, N. L. et al. Lymphatic vascular defects promoted by Prox1 haploinsufficiency cause adult-onset obesity. Nature Genet. 37, 1072–1081 (2005).
  Article CAS PubMed Google Scholar
• Baldwin, M. E. et al. Vascular endothelial growth factor D is dispensable for development of the lymphatic system. Mol. Cell Biol. 25, 2441–2449 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Dumont, D. J. et al. Cardiovascular failure in mouse embryos deficient in VEGF receptor-3. Science 282, 946–949 (1998).
  Article ADS CAS PubMed Google Scholar
• Karkkainen, M. J. et al. Missense mutations interfere with VEGFR-3 signaling in primary lymphoedema. Nature Genet. 25, 153–159 (2000).
  Article CAS PubMed Google Scholar
• Jackson, D. G. Biology of the lymphatic marker LYVE-1 and applications in research into lymphatic trafficking and lymphangiogenesis. APMIS 112, 526–538 (2004).
  Article CAS PubMed Google Scholar
• Makinen, T. et al. PDZ interaction site in ephrinB2 is required for the remodeling of lymphatic vasculature. Genes Dev. 19, 397–410 (2005).
  Article PubMed PubMed Central CAS Google Scholar
• Jeltsch, M., Tammela, T., Alitalo, K. & Wilting, J. Genesis and pathogenesis of lymphatic vessels. Cell Tissue Res. 314, 69–84 (2003).
  Article CAS PubMed Google Scholar
• Aalami, O. O., Allen, D. B. & Organ, C. H. Jr. Chylous ascites: a collective review. Surgery 128, 761–778 (2000).
  Article CAS PubMed Google Scholar
• Abtahian, F. et al. Regulation of blood and lymphatic vascular separation by signaling proteins SLP-76 and Syk. Science 299, 247–251 (2003).
  Article ADS CAS PubMed PubMed Central Google Scholar
• Saharinen, P. et al. Multiple angiopoietin recombinant proteins activate the Tie1 receptor tyrosine kinase and promote its interaction with Tie2. J. Cell Biol. 169, 239–243 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Gale, N. W. et al. 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 (2002).
  Article CAS PubMed Google Scholar
• Morisada, T. et al. Angiopoietin-1 promotes LYVE-1-positive lymphatic vessel formation. Blood 105, 4649–4656 (2005).
  Article CAS PubMed Google Scholar
• Tammela, T. et al. Angiopoietin-1 promotes lymphatic sprouting and hyperplasia. Blood 105, 4642–4648 (2005).
  Article CAS PubMed Google Scholar
• Adams, R. H. & Klein, R. Eph receptors and ephrin ligands. essential mediators of vascular development. Trends Cardiovasc. Med. 10, 183–188 (2000).
  Article CAS PubMed Google Scholar
• Petrova, T. V. et al. Defective valves and abnormal mural cell recruitment underlie lymphatic vascular failure in lymphedema distichiasis. Nature Med. 10, 974–981 (2004).
  Article CAS PubMed Google Scholar
• Dagenais, S. L. et al. Foxc2 is expressed in developing lymphatic vessels and other tissues associated with lymphedema-distichiasis syndrome. Gene Expr. Patterns 4, 611–619 (2004).
  Article CAS PubMed Google Scholar
• Ferrell, R. E. Research perspectives in inherited lymphatic disease. Ann. N Y Acad. Sci. 979, 39–51 (2002).
  Article ADS CAS PubMed Google Scholar
• Brice, G. et al. 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 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Schacht, V. et al. T1alpha/podoplanin deficiency disrupts normal lymphatic vasculature formation and causes lymphedema. EMBO J. 22, 3546–3556 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Kriehuber, E. et al. Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages. J. Exp. Med. 194, 797–808 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Makinen, T. et al. Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3. EMBO J. 20, 4762–4773. (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Podgrabinska, S. et al. Molecular characterization of lymphatic endothelial cells. Proc. Natl Acad. Sci. USA 99, 16069–16074 (2002).
  Article ADS CAS PubMed PubMed Central Google Scholar
• Hirakawa, S. et al. Identification of vascular lineage-specific genes by transcriptional profiling of isolated blood vascular and lymphatic endothelial cells. Am. J. Pathol. 162, 575–586 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Rockson, S. G. Lymphedema. Am. J. Med. 110, 288–295 (2001).
  Article CAS PubMed Google Scholar
• Yla-Herttuala, S. & Alitalo, K. Gene transfer as a tool to induce therapeutic vascular growth. Nature Med. 9, 694–701 (2003).
  Article PubMed CAS Google Scholar
• Saaristo, A. et al. Lymphangiogenic gene therapy with minimal blood vascular side effects. J. Exp. Med. 196, 719–730 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Thurston, G. et al. Angiopoietin-1 protects the adult vasculature against plasma leakage. Nature Med. 6, 460–463 (2000).
  Article CAS PubMed Google Scholar
• Weis, S. & Cheresh, D. A. Pathophysiological consequences of VEGF-induced vascular permeability. Nature 65, 9789–9798 (2005).
  Google Scholar
• Pepper, M. S. Lymphangiogenesis and tumor metastasis: myth or reality? Clin. Cancer Res. 7, 462–468 (2001).
  CAS PubMed Google Scholar
• Stacker, S. A., Achen, M. G., Jussila, L., Baldwin, M. E. & Alitalo, K. Lymphangiogenesis and cancer metastasis. Nature Rev. Cancer 2, 573–583 (2002).
  Article CAS Google Scholar
• He, Y. et al. Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling. J. Natl Cancer Inst. 94, 819–825 (2002).
  Article CAS PubMed Google Scholar
• Skobe, M. et al. Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nature Med. 7, 192–198 (2001).
  Article CAS PubMed Google Scholar
• Mandriota, S. J. et al. Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis. EMBO J. 20, 672–682 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Stacker, S. A. et al. Vascular endothelial growth factor-D promotes the metastatic spread of cancer via the lymphatics. Nature Med. 7, 186–191 (2001).
  Article CAS PubMed Google Scholar
• Karpanen, T. et al. Vacular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth. Cancer Res. 61, 1786–1790 (2001).
  CAS PubMed Google Scholar
• Valtola, R. et al. VEGFR-3 and its ligand VEGF-C are associated with angiogenesis in breast cancer. Am. J. Pathol. 154, 1381–1390 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Krishnan, J. et al. Differential in vivo and in vitro expression of vascular endothelial growth factor (VEGF)-C and VEGF-D in tumors and its relationship to lymphatic metastasis in immunocompetent rats. Cancer Res. 63, 713–722 (2003).
  CAS PubMed Google Scholar
• Dadras, S. S. et al. Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival. Am. J. Pathol. 162, 1951–1960 (2003).
  Article PubMed PubMed Central Google Scholar
• Maula, S. M. et al. Intratumoral lymphatics are essential for the metastatic spread and prognosis in squamous cell carcinomas of the head and neck region. Cancer Res. 63, 1920–1926 (2003).
  CAS PubMed Google Scholar
• Padera, T. P. et al. Pathology: cancer cells compress intratumour vessels. Nature 427, 695 (2004).
  Article ADS CAS PubMed Google Scholar
• Wong, S. Y. et al. Tumor-secreted VEGF-C is necessary for prostate cancer lymphangiogenesis, but lymphangiogenesis is unnecessary for lymph node metastasis. Cancer Res. 65, 9789–9798.
• Padera, T. P. et al. Lymphatic metastasis in the absence of functional intratumor lymphatics. Science 296, 1883–1886 (2002).
  Article ADS CAS PubMed Google Scholar
• He, Y. et al. Vascular endothelial cell growth factor receptor 3-mediated activation of lymphatic endothelium is crucial for tumor cell entry and spread via lymphatic vessels. Cancer Res. 65, 4739–4746 (2005).
  Article CAS PubMed Google Scholar
• Laakkonen, P., Porkka, K., Hoffman, J. A. & Ruoslahti, E. A tumor-homing peptide with a targeting specificity related to lymphatic vessels. Nature Med. 8, 751–755 (2002).
  Article CAS PubMed Google Scholar
• Zlotnik, A. Chemokines in neoplastic progression. Semin. Cancer Biol. 14, 181–185 (2004).
  Article CAS PubMed Google Scholar
• Hirakawa, S. et al. VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis. J. Exp. Med. 201, 1089–1099 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Pullinger, B. D. & Florey, H. W. Proliferation of lymphatics in inflammation. J. Pathol. Bact. 45, 157–170 (1937).
  Article Google Scholar
• Ristimaki, A., Narko, K., Enholm, B., Joukov, V. & Alitalo, K. Proinflammatory cytokines regulate expression of the lymphatic endothelial mitogen vascular endothelial growth factor-C. J. Biol. Chem. 273, 8413–8418 (1998).
  Article CAS PubMed Google Scholar
• Saban, M. R. et al. Visualization of lymphatic vessels through NF-kappaB activity. Blood 104, 3228–3230 (2004).
  Article CAS PubMed Google Scholar
• Kerjaschki, D. et al. Lymphatic neoangiogenesis in human kidney transplants is associated with immunologically active lymphocytic infiltrates. J. Am. Soc. Nephrol. 15, 603–612 (2004).
  Article CAS PubMed Google Scholar
• Hamrah, P., Chen, L., Zhang, Q. & Dana, M. R. Novel expression of vascular endothelial growth factor receptor (VEGFR)-3 and VEGF-C on corneal dendritic cells. Am. J. Pathol. 163, 57–68 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Chen, L. et al. Vascular endothelial growth factor receptor-3 mediates induction of corneal alloimmunity. Nature Med. 10, 813–815 (2004).
  Article CAS PubMed Google Scholar
• Ohl, L. et al. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity 21, 279–288 (2004).
  Article CAS PubMed Google Scholar
• Irjala, H. et al. Mannose receptor is a novel ligand for L-selectin and mediates lymphocyte binding to lymphatic endothelium. J. Exp. Med. 194, 1033–1041 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Salmi, M., Koskinen, K., Henttinen, T., Elima, K. & Jalkanen, S. CLEVER-1 mediates lymphocyte transmigration through vascular and lymphatic endothelium. Blood 104, 3849–3857 (2004).
  Article CAS PubMed Google Scholar
• Nibbs, R. J. et al. The beta-chemokine receptor D6 is expressed by lymphatic endothelium and a subset of vascular tumors. Am. J. Pathol. 158, 867–877 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Kriederman, B. M. et al. FOXC2 haploinsufficient mice are a model for human autosomal dominant lymphedema-distichiasis syndrome. Hum. Mol. Genet. 12, 1179–1185 (2003).
  Article CAS PubMed Google Scholar
• Ayadi, A. et al. Net-targeted mutant mice develop a vascular phenotype and up-regulate egr-1. EMBO J. 20, 5139–5152 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Fruman, D. A. et al. Hypoglycaemia, liver necrosis and perinatal death in mice lacking all isoforms of phosphoinositide 3-kinase p85 alpha. Nature Genet. 26, 379–382 (2000).
  Article CAS PubMed Google Scholar
• Pennisi, D. et al. Mutations in Sox18 underlie cardiovascular and hair follicle defects in ragged mice. Nature Genet. 24, 434–437 (2000).
  Article CAS PubMed Google Scholar
• Gittenberger-De Groot, A. C. et al. Abnormal lymphatic development in trisomy 16 mouse embryos precedes nuchal edema. Dev. Dyn. 230, 378–384 (2004).
  Article PubMed Google Scholar
• Dixelius, J. et al. 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 (2003).
  Article CAS PubMed Google Scholar
• Salameh, A., Galvagni, F., Bardelli, M., Bussolino, F. & Oliviero, S. Direct recruitment of CRK and GRB2 to VEGFR-3 induce proliferation, migration and survival of endothelial cells through the activation of ERK, AKT and JNK pathways. Blood 15, 3423–3431 (2005).
  Article CAS Google Scholar
• Ny, A. et al. A genetic Xenopus laevis tadpole model to study lymphangiogenesis. Nature Med. 11, 998–1004 (2005).
  Article CAS PubMed Google Scholar
• Schneider, M., Othman-Hassan, K., Christ, B. & Wilting, J. Lymphangioblasts in the avian wing bud. Dev. Dyn. 216, 311–319 (1999).
  Article CAS PubMed Google Scholar
• Rajantie, I. et al. Adult bone marrow-derived cells recruited during angiogenesis comprise precursors for periendothelial vascular mural cells. Blood 104, 2084–2086 (2004).
  Article CAS PubMed Google Scholar
• Wang, H. W. et al. Kaposi sarcoma herpesvirus-induced cellular reprogramming contributes to the lymphatic endothelial gene expression in Kaposi sarcoma. Nature Genet. 36, 687–693 (2004).
  Article CAS PubMed Google Scholar
• Hong, Y. K. et al. Lymphatic reprogramming of blood vascular endothelium by Kaposi sarcoma-associated herpesvirus. Nature Genet. 36, 683–685 (2004).
  Article CAS PubMed Google Scholar