New insights into the molecular control of the lymphatic vascular system and its role in disease

Journal of Investigative Dermatology

Volumn 126, Issue 10, 2006, Pages 2167-2177

  Cueni, Leah N ^a   Detmar, Michael ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

MOLECULAR MARKER; VASCULOTROPIN C;

CAPILLARY LEAK SYNDROME; EMBRYO DEVELOPMENT; GENE MUTATION; GENE THERAPY; GENETIC MODEL; HUMAN; IMMUNE RESPONSE; LYMPH VESSEL; LYMPH VESSEL ENDOTHELIUM; LYMPHANGIOGENESIS; LYMPHATIC SYSTEM; LYMPHATIC SYSTEM DISEASE; LYMPHEDEMA; METASTASIS; MOLECULAR MODEL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SKIN CANCER; SKIN INFLAMMATION; TISSUE WATER; ULTRAVIOLET IRRADIATION;

EID: 33748771724     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/sj.jid.5700464     Document Type: Article

References (100)

1. Abtahian F, Guerriero A, Sebzda E, Lu MM, Zhou R, Mocsai A et al. (2003) Regulation of blood and lymphatic vascular separation by signaling proteins slp-76 and syk. Science 299:247-51
2. Achen MG, Jeltsch M, Kukk E, Makinen T, Vitali A, Wilks AF 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 95:548-53
3. Asellius G (1627) De lactibus sive lacteis venis. Milan: Mediolani
4. Auguste P, Javerzat S, Bikfalvi A (2003) Regulation of vascular development by fibroblast growth factors. Cell Tissue Res 314:157-66
5. Avantaggiato V, Orlandini M, Acampora D, Oliviero S, Simeone A (1998) Embryonic expression pattern of the murine figf gene, a growth factor belonging to platelet-derived growth factor/vascular endothelial growth factor family. Mech Dev 73:221-4
6. Ayadi A, Zheng H, Sobieszczuk P, Buchwalter G, Moerman P, Alitalo K et al. (2001) Nettargeted mutant mice develop a vascular phenotype and up-regulate EGR-1. EMBO J 20:5139-52
7. Baldwin ME, Halford MM, Roufail S, Williams RA, Hibbs ML, Grail D et al. (2005) Vascular endothelial growth factor d is dispensable for development of the lymphatic system. Mol Cell Biol 25:2441-9
8. Baluk P, Tammela T, Ator E, Lyubynska N, Achen MG, Hicklin D et al. (2005) Pathogenesis of persistent lymphatic vessel hyperplasia in chronic airway inflammation. J Clin Invest 115:247-57
9. Banerji S, Ni J, Wang SX, Clasper S, Su J, Tammi R 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
10. Barsky SH, Baker A, Siegal GP, Togo S, Liotta LA (1983) Use of anti-basement membrane antibodies to distinguish blood vessel capillaries from lymphatic capillaries. Am J Surg Pathol 7:667-77
11. Bjorndahl M, Cao R, Nissen LJ, Clasper S, Johnson LA, Xue Y et al. (2005) Insulin-like growth factors 1 and 2 induce lymphangiogenesis in vivo. Proc Natl Acad Sci USA 102:15593-8
12. Breiteneder-Geleff S, Soleiman A, Kowalski H, Horvat R, Amann G, Kriehvber E et al. (1999) Angiosarcomas express mixed endothelial phenotypes of blood and lymphatic capillaries: Podoplanin as a specific marker for lymphatic endothelium. Am J Pathol 154: 385-94
13. Brown P (2005) Lymphatic system: unlocking the drains. Nature 436:456-8
14. Cao R, Bjorndahl MA, Religa P, Clasper S, Garvin S, Galter D et al. (2004) Pdgf-bb induces intratumoral lymphangiogenesis and promotes lymphatic metastasis. Cancer Cell 6: 333-45
15. Chang LK, Garcia-Cardena G, Farnebo F, Fannon M, Chen EJ, Butterfield C et al. (2004) Dosedependent response of FGF-2 for lymphangiogenesis. Proc Natl Acad Sci USA 101: 11658-63
16. Cursiefen C, Chen L, Borges LP, Jackson D, Cao J, Radziejewski C et al. (2004) VEGF-a stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J Clin Invest 113: 1040-50
17. Dadras SS, Lange-Asschenfeldt B, Velasco P, Nguyen L, Vora A, Muzikanski A et al. (2005) Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes. Mod Pathol 18:1232-42
18. Dadras SS, Paul T, Bertoncini J, Brown LF, Muzikansky A, Jackson DG et al. (2003) Tumor lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival. Am J Pathol 162: 1951-60
19. Davis S, Aldrich TH, Jones PF, Acheson A, Compton DL, Jain V et al. (1996) Isolation of angiopoietin-1, a ligand for the tie2 receptor, by secretion-trap expression cloning. Cell 87:1161-9
20. Dumont DJ, Gradwohl G, Fong GH, Puri MC, Gertsenstein M, Auerbach A et al. (1994) Dominant-negative and targeted null mutations in the endothelial receptor tyrosine kinase, tek, reveal a critical role in vasculogenesis of the embryo. Genes Dev 8: 1897-909
21. Dumont DJ, Jussila L, Taipale J, Lymboussaki A, Mustonen T, Pajusula K et al. (1998) Cardiovascular failure in mouse embryos deficient in VEGF receptor-3. Science 282: 946-9
22. Ebata N, Nodasaka Y, Sawa Y, Yamaoka Y, Makino S, Totsuka Y et al. (2001) Desmoplakin as a specific marker of lymphatic vessels. Microvasc Res 61:40-8
23. Erhard H, Rietveld FJ, Brocker EB, de Waal RM, Ruiter DJ (1996) Phenotype of normal cutaneous microvasculature. Immunoelectron microscopic observations with emphasis on the differences between blood vessels and lymphatics. J Invest Dermatol 106:135-40
24. Fang J, Dagenais SL, Erickson RP, Arlt MF, Glynn MW, Gorski JL 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 67:1382-8
25. Gale NW, Thurston G, Hackett SF, Renard R, Wang Q, McClain J 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 3:411-23
26. Gerli R, Solito R, Weber E, Agliano M (2000) Specific adhesion molecules bind anchoring filaments and endothelial cells in human skin initial lymphatics. Lymphology 33: 148-57
27. Gluzman-Poltorak Z, Cohen T, Herzog Y, Neufeld G (2000) Neuropilin-2 is a receptor for the vascular endothelial growth factor (VEGF) forms VEGF-145 and VEGF-165. J Biol Chem 275:29922
28. Gunn MD, Tangemann K, Tam C, Cyster JG, Rosen SD, Williams LT et al. (1998) A chemokine expressed in lymphoid high endothelial venules promotes the adhesion and chemotaxis of naive T lymphocytes. Proc Natl Acad Sci USA 95:258-63
29. Harvey NL, Srinivasan RS, Dillard ME, Johnson NC, Witte MH, Boyd K et al. (2005) Lymphatic vascular defects promoted by prox1 haploinsufficiency cause adult-onset obesity. Nat Genet 37:1072-81
30. He Y, Kozaki K, Karpanen T, Koshikawa K, Yla-Herttuala S, Takahashi T et al. (2002) Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling. J Natl Cancer Inst 94:819-25
31. Hirakawa S, Detmar M (2004) New insights into the biology and pathology of the cutaneous lymphatic system. J Dermatol Sci 35:1-8
32. Hirakawa S, Hong YK, Harvey N, Schacht V, Matsuda K, Libermann T et al. (2003) Identification of vascular lineage-specific genes by transcriptional profiling of isolated blood vascular and lymphatic endothelial cells. Am J Pathol 162:575-86
33. Hirakawa S, Kodama S, Kunstfeld R, Kajiya K, Brown LF, Detmar M (2005) VEGF-a induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis. J Exp Med 201:1089-99
34. Hong YK, Foreman K, Shin JW, Hirakawa S, Curry CL, Sage DR et al. (2004a) Lymphatic reprogramming of blood vascular endothelium by Kaposi sarcoma-associated herpesvirus. Nat Genet 36:683-5
35. Hong YK, Harvey N, Noh YH, Schacht V, Hirakawa S, Detmar M et al. (2002) Prox1 is a master control gene in the program specifying lymphatic endothelial cell fate. Dev Dyn 225:351-7
36. Hong YK, Lange-Asschenfeldt B, Velasco P, Hirakawa S, Kunstfeld R, Brown LF et al. (2004b) VEGF-a promotes tissue repairassociated lymphatic vessel formation via VEGFR-2 and the alpha1beta1 and alpha2-beta1 integrins. FASEB J 18:1111-3
37. Huang XZ, Wu JF, Ferrando R, Lee JH, Wang YL, Farese RV et al. (2000) Fatal bilateral chylothorax in mice lacking the integrin alpha9beta1. Mol Cell Biol 20:5208-15
38. Huntington GS, McClure CFW (1910) The anatomy and development of the jugular lymph sac in the domestic cat (Felis domestica). Am J Anat 10:177-311
39. Irjala H, Johansson EL, Grenman R, Alanen K, Salmi M, Jalkanen S et al. (2001) Mannose receptor is a novel ligand for l-selectin and mediates lymphocyte binding to lymphatic endothelium. J Exp Med 194:1033-42
40. Irrthum A, Devriendt K, Chitayat D, Matthijs G, Glade C, Steijlen PM et al. (2003) Mutations in the transcription factor gene sox18 underlie recessive and dominant forms of hypotrichosis-lymphedema-telangiectasia. Am J Hum Genet 72:1470-8
41. Jackson DG (2004) Biology of the lymphatic marker LYVE-1 and applications in research into lymphatic trafficking and lymphangiogenesis. Apmis 112:526-38
42. Jeltsch M, Kaipainen A, Joukov V, Meng X, Lakso M, Rauvala H et al. (1997) Hyperplasia of lymphatic vessels in VEGF-c transgenic mice. Science 276:1423-5
43. Joukov V, Kumar V, Sorsa T, Arighi E, Weich H, Saksela O et al. (1998) A recombinant mutant vascular endothelial growth factor-c that has lost vascular endothelial growth factor receptor-2 binding, activation, and vascular permeability activities. J Biol Chem 273:6599-602
44. Joukov V, Pajusola K, Kaipainen A, Chilov D, Lahtinen I, Kukk E 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
45. Kaipainen A, Korhonen J, Mustonen T, van Hinsbergh VW, Fang GH, Dumont D et al. (1995) Expression of the fms-like tyrosine kinase 4 gene becomes restricted to lymphatic endothelium during development. Proc Natl Acad Sci USA 92:3566-70
46. Kajiya K, Detmar M (2006) An important role of lymphatic vessels in the control of UVBinduced edema formation and inflammation. J Invest Dermatol 126:919-21
47. Kajiya K, Hirakawa S, Ma B, Drinnenberg I, Detmar M (2005) Hepatocyte growth factor promotes lymphatic vessel formation and function. EMBO J 24:2885-95
48. Karkkainen MJ, Haiko P, Sainio K, Partanen J, Taipale J, Petrova TV 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
49. Karkkainen MJ, Saaristo A, Jussila L, Karila KA, Lawrence EC, Pajusola K et al. (2001) A model for gene therapy of human hereditary lymphedema. Proc Natl Acad Sci USA 98: 12677-82
50. Kerjaschki D, Huttary N, Raab I, Regele H, Bojarski-Nagy K, Bartel G et al. (2006) Lymphatic endothelial progenitor cells contribute to de novo lymphangiogenesis in human renal transplants. Nat Med 12:230-4
51. Kriederman BM, Myloyde TL, Witte MH, Dagenais SL, Witte CL, Rennels M et al. (2003) Foxc2 haploinsufficient mice are a model for human autosomal dominant lymphedemadistichiasis syndrome. Hum Mol Genet 12: 1179-85
52. Kriehuber E, Breiteneder-Geleff S, Groeger M, Soleiman A, Schoppmann SF, Stingl G et al. (2001) Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages. J Exp Med 194:797-808
53. Kubo H, Cao R, Brakenhielm E, Makinen T, Cao Y, Alitalo K et al. (2002) Blockade of vascular endothelial growth factor receptor-3 signaling inhibits fibroblast growth factor-2-induced lymphangiogenesis in mouse cornea. Proc Natl Acad Sci USA 99:8868-73
54. Kunstfeld R, Hirakawa S, Hong YK, Schacht V, Lange-Asschenfeldt B, Velasco P et al. (2004) Induction of cutaneous delayed-type hypersensitivity reactions in VEGF-a transgenic mice results in chronic skin inflammation associated with persistent lymphatic hyperplasia. Blood 104:1048-57
55. Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radziejewski C et al. (1997) Angiopoietin-2, a natural antagonist for tie2 that disrupts in vivo angiogenesis. Science 277:55-60
56. Makinen T, Adams RH, Bailey J, Lu Q, Ziemiecki A, Alitalo K et al. (2005) Pdz interaction site in ephrinb2 is required for the remodeling of lymphatic vasculature. Genes Dev 19: 397-410
57. Makinen T, Veikkola T, Mustjoki S, Karpanen T, Catimel B, Nice EC et al. (2001) Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-c/d receptor VEGFR-3. EMBO J 20: 4762-73
58. Mandriota SJ, Jussila L, Jeltsch M, Compagni A, Baetens D, Prevo R et al. (2001) Vascular endothelial growth factor-c-mediated lymphangiogenesis promotes tumour metastasis. EMBO J 20:672-82
59. Martin-Villar E, Scholl FG, Gamallo C, Yurrita MM, Munoz-Guerra M, Cruzes J et al. (2005) Characterization of human pa2.26 antigen (t1alpha-2, podoplanin), a small membrane mucin induced in oral squamous cell carcinomas. Int J Cancer 113:899-910
60. Morisada T, Oike Y, Yamada Y, Urano T, Akao M, Kubota Y et al. (2005) Angiopoietin-1 promotes LYVE-1-positive lymphatic vessel formation. Blood 105:4649-56
61. Nagy JA, Vasile E, Feng D, Sundberg C, Brown LF, Detmar M et al. (2002) Vascular permeability factor/vascular endothelial growth factor induces lymphangiogenesis as well as angiogenesis. J Exp Med 196:1497-506
62. Neufeld G, Cohen T, Shraga N, Lange T, Kessler O, Herzog Y et al. (2002) The neuropilins: multifunctional semaphorin and VEGF receptors that modulate axon guidance and angiogenesis. Trends Cardiovasc Med 12: 13-9
63. Niemela H, Elima K, Henttinen T, Irjala H, Salmi M, Jalkanen S et al. (2005) Molecular identification of pal-e, a widely used endothelial-cell marker. Blood 106:3405-9
64. Oliver G (2004) Lymphatic vasculature development. Nat Rev Immunol 4:35-45
65. Oliver G, Detmar M (2002) The rediscovery of the lymphatic system: old and new insights into the development and biological function of the lymphatic vasculature. Genes Dev 16: 773-83
66. Oliver G, Sosa-Pineda B, Geisendorf S, Spana EP, Doe CQ, Gruss P et al. (1993) Prox 1, a prospero-related homeobox gene expressed during mouse development. Mech Dev 44: 3-16
67. Orlandini M, Marconcini L, Ferruzzi R, Oliviero S (1996) Identification of a c-fos-induced gene that is related to the platelet-derived growth factor/vascular endothelial growth factor family. Proc Natl Acad Sci USA 93: 11675-80
68. Paavonen K, Puolakkainen P, Jussila L, Jahkola T, Alitalo K (2000) Vascular endothelial growth factor receptor-3 in lymphangiogenesis in wound healing. Am J Pathol 156:1499-504
69. Partanen TA, Alitalo K, Miettinen M (1999) Lack of lymphatic vascular specificity of vascular endothelial growth factor receptor 3 in 185 vascular tumors. Cancer 86:2406-12
70. Partanen TA, Arola J, Saaristo A, Jussila L, Ora A, Miettinen L et al. (2000) VEGF-c and VEGF-d expression in neuroendocrine cells and their receptor, VEGFR-3, in fenestrated blood vessels in human tissues. FASEB J 14:2087-96
71. Pennisi D, Gardner J, Chambers D, Hosking B, Peters J, Muscat G et al. (2000) Mutations in sox18 underlie cardiovascular and hair follicle defects in ragged mice. Nat Genet 24:434-7
72. Petrova TV, Karpanen T, Norrmen C, Mellor R, Tamakoshi T, Finegold D et al. (2004) Defective valves and abnormal mural cell recruitment underlie lymphatic vascular failure in lymphedema distichiasis. Nat Med 10: 974-81
73. Petrova TV, Makinen T, Makela TP, Saarela J, Virtanen I, Ferrell RE et al. (2002) Lymphatic endothelial reprogramming of vascular endothelial cells by the prox-1 homeobox transcription factor. EMBO J 21:4593-9
74. Podgrabinska S, Braun P, Velasco P, Kloos B, Pepper MS, Skobe M (2002) Molecular characterization of lymphatic endothelial cells. Proc Natl Acad Sci USA 99:16069-74
75. Ramirez MI, Millien G, Hinds A, Cao Y, Seldin DC, Williams MC (2003) T1alpha, a lung type i cell differentiation gene, is required for normal lung cell proliferation and alveolus formation at birth. Dev Biol 256:61-72
76. Saaristo A, Veikkola T, Tammela T, Enholm B, Karkkainen MJ, Pajusola K et al. (2002) Lymphangiogenic gene therapy with minimal blood vascular side effects. J Exp Med 196: 719-30
77. Sabin FR (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 1:367-91
78. Sauter B, Foedinger D, Sterniczky B, Wolff K, Rappersberger K (1998) Immunoelectron microscopic characterization of human dermal lymphatic microvascular endothelial cells. Differential expression of cd31, cd34, and type iv collagen with lymphatic endothelial cells vs blood capillary endothelial cells in normal human skin, lymphangioma, and hemangioma in situ. J Histochem Cytochem 46:165-76
79. Schacht V, Dadras SS, Johnson LA, Jackson DG, Hong YK, Detmar M (2005) Up-regulation of the lymphatic marker podoplanin, a mucintype transmembrane glycoprotein, in human squamous cell carcinomas and germ cell tumors. Am J Pathol 166:913-21
80. Schacht V, Ramirez MI, Hong YK, Hirakawa S, Feng D, Havrvey N et al. (2003) T1alpha/podoplanin deficiency disrupts normal lymphatic vasculature formation and causes lymphedema. EMBO J 22:3546-56
81. Schlingemann RO, Dingjan GM, Emeis JJ, Blok J, Warnaar SO, Ruiter DJ et al. (1985) Monoclonal antibody pal-e specific for endothelium. Lab Invest 52:71-6
82. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF et al. (1983) Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219:983-5
83. Shin JW, Min M, Larrieu-Lahargue F, Canron X, Kunstfeld R, Nguyen L et al. (2005) Prox1 promotes lineage-specific expression of FGF receptor-3 in lymphatic endothelium: A role for FGF signaling in lymphangiogenesis. Mol Biol Cell 17:576-84
84. Skobe M, Detmar M (2000) Structure, function, and molecular control of the skin lymphatic system. J Investig Dermatol Symp Proc 5:14-9
85. Skobe M, Hawighorst T, Jackson DG, Prevo R, Janes L, Velasco P et al. (2001) Induction of tumor lymphangiogenesis by VEGF-c promotes breast cancer metastasis. Nat Med 7: 192-8
86. Soker S, Takashima S, Miao HQ, Neufeld G, Klagsbrun M. (1998) Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92:735-45
87. Stacker SA, Achen MG, Jussila L, Baldwin ME, Alitalo K (2002) Lymphangiogenesis and cancer metastasis. Nat Rev Cancer 2:573-83
88. Stacker SA, Caesar C, Baldwin ME, Thornton GE, Williams RA, Prevo R et al. (2001) VEGF-d promotes the metastatic spread of tumor cells via the lymphatics. Nat Med 7:186-91
89. Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S et al. (1996) Requisite role of angiopoietin-1, a ligand for the tie2 receptor, during embryonic angiogenesis. Cell 87:1171-80
90. Tammela T, Saaristo A, Lohela M, Morisada T, Tornberg J, Norrmen C et al. (2005) Angio-poietin-1 promotes lymphatic sprouting and hyperplasia. Blood 105:4642-8
91. Valtola R, Salven P, Heikkila P, Taipale J, Joensuu H, Rehn M et al. (1999) VEGFR-3 and its ligand VEGF-c are associated with angiogenesis in breast cancer. Am J Pathol 154: 1381-90
92. Veikkola T, Jussila L, Makinen T, Karpanen T, Jeltsch M, Petrova TV et al. (2001) Signalling via vascular endothelial growth factor receptor-3 is sufficient for lymphangiogenesis in transgenic mice. EMBO J 20: 1223-31
93. Wang HW, Trotter MW, Lagos D, Bourboulia D, Henderson S, Makinen T et al. (2004) Kaposi sarcoma herpesvirus-induced cellular reprogramming contributes to the lymphatic endothelial gene expression in kaposi sarcoma. Nat Genet 36:687-93
94. Wetterwald A, Hoffstetter W, Cecchini MG, Lanske B, Wagner C, Fleisch H et al. (1996) Characterization and cloning of the e11 antigen, a marker expressed by rat osteoblasts and osteocytes. Bone 18:125-32
95. Wigle JT, Harvey N, Detmar M, Lagutina I, Grosveld G, Gunn MD et al. (2002) An essential role for prox1 in the induction of the lymphatic endothelial cell phenotype. EMBO J 21:1505-13
96. Wigle JT, Oliver G (1999) Prox1 function is required for the development of the murine lymphatic system. Cell 98:769-78
97. Wiley HE, Gonzalez EB, Maki W, Wu MT, Hwang ST (2001) Expression of cc chemokine receptor-7 and regional lymph node metastasis of b16 murine melanoma. J Natl Cancer Inst 93:1638-43
98. Witte MH, Bernas MJ, Martin CP, Witte CL (2001) Lymphangiogenesis and lymphangiodysplasia: from molecular to clinical lymphology. Microsc Res Tech 55:122-45
99. Young PE, Baumhueter S, Lasky LA (1995) The sialomucin cd34 is expressed on hematopoietic cells and blood vessels during murine development. Blood 85:96-105
100. Yuan L, Moyon D, Pardanaud L, Breant C, Karkkainen MJ, Alitalo K et al. (2002) Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development 129:4797-806