Lymphangiogenesis in post-natal tissue remodeling: Lymphatic endothelial cell connection with its environment

Molecular Aspects of Medicine

Volumn 32, Issue 2, 2011, Pages 146-158

  Paupert, Jenny ^a   Sounni, Nor Eddine ^a   Noël, Agnès ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Cell cell junctions; Extracellular matrix; Integrins; Interstitial tissue; Lymphangiogenesis; Metalloproteases

Indexed keywords

FIBRONECTIN; INTEGRIN;

BLOOD VESSEL; CANCER CELL; CELL ADHESION; CELL COMMUNICATION; CELL FUNCTION; CELL INTERACTION; CELL JUNCTION; CELL MIGRATION; CELL PROLIFERATION; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; LYMPH VESSEL ENDOTHELIUM; LYMPHANGIOGENESIS; METASTASIS; NONHUMAN; PATHOPHYSIOLOGY; POSTNATAL DEVELOPMENT; PROTEIN FUNCTION; REVIEW; TISSUE REGENERATION; VASCULARIZATION;

ANIMALS; CELL COMMUNICATION; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; HUMANS; LEUKOCYTES; LYMPHANGIOGENESIS; NEOPLASMS;

EID: 79957879861     PISSN: 00982997     EISSN: 18729452     Source Type: Journal    
DOI: 10.1016/j.mam.2011.04.002     Document Type: Review

References (146)

1. Achen, M.G., McColl, B.K., Stacker, S.A., 2005. Focus on lymphangiogenesis in tumor metastasis. Cancer Cell 7 (2), 121-127. (Pubitemid 40248338)
2. Adams, R.H., Alitalo, K., 2007. Molecular regulation of angiogenesis and lymphangiogenesis. Nat. Rev. Mol. Cell Biol. 8 (6), 464-478.
3. Albuquerque, R.J., Hayashi, T., Cho, W.G., Kleinman, M.E., Dridi, S., Takeda, A., Baffi, J.Z., Yamada, K., Kaneko, H., Green, M.G., Chappell, J., Wilting, J., Weich, H.A., Yamagami, S., Amano, S., Mizuki, N., Alexander, J.S., Peterson, M.L., Brekken, R.A., Hirashima, M., Capoor, S., Usui, T., Ambati, B.K., Ambati, J., 2009. Alternatively spliced vascular endothelial growth factor receptor-2 is an essential endogenous inhibitor of lymphatic vessel growth. Nat. Med. 15 (9), 1023-1030.
4. Alitalo, K., Tammela, T., Petrova, T.V., 2005. Lymphangiogenesis in development and human disease. Nature 438 (7070), 946-953. (Pubitemid 43093960)
5. Aurrand-Lions, M., Duncan, L., Ballestrem, C., Imhof, B.A., 2001. JAM-2, a novel immunoglobulin superfamily molecule, expressed by endothelial and lymphatic cells. J. Biol. Chem. 276 (4), 2733-2741.
6. Avraamides, C.J., Garmy-Susini, B., Varner, J.A., 2008. Integrins in angiogenesis and lymphangiogenesis. Nat. Rev. Cancer 8 (8), 604-617.
7. Avraham, T., Clavin, N.W., Daluvoy, S.V., Fernandez, J., Soares, M.A., Cordeiro, A.P., Mehrara, B.J., 2009. Fibrosis is a key inhibitor of lymphatic regeneration. Plast. Reconstr. Surg. 124 (2), 438-450.
8. Bajou, K., Noel, A., Gerard, R.D., Masson, V., Brunner, N., Holst-Hansen, C., Skobe, M., Fusenig, N.E., Carmeliet, P., Collen, D., Foidart, J.M., 1998. Absence of host plasminogen activator inhibitor 1 prevents cancer invasion and vascularization. Nat. Med. 4 (8), 923-928.
9. Baluk, P., Fuxe, J., Hashizume, H., Romano, T., Lashnits, E., Butz, S., Vestweber, D., Corada, M., Molendini, C., Dejana, E., McDonald, D.M., 2007. Functionally specialized junctions between endothelial cells of lymphatic vessels. J. Exp. Med. 204 (10), 2349-2362.
10. Bauerschlag, D.O., Schem, C., Tiwari, S., Egberts, J.H., Weigel, M.T., Kalthoff, H., Jonat, W., Maass, N., Meinhold-Heerlein, I., 2010. Sunitinib (SU11248) inhibits growth of human ovarian cancer in xenografted mice. Anticancer Res. 30 (9), 3355-3360.
11. Bazigou, E., Xie, S., Chen, C., Weston, A., Miura, N., Sorokin, L., Adams, R., Muro, A.F., Sheppard, D., Makinen, T., 2009. Integrin-alpha9 is required for fibronectin matrix assembly during lymphatic valve morphogenesis. Dev. Cell 17 (2), 175-186.
12. Berx, G., van Roy, F., 2009. Involvement of members of the cadherin superfamily in cancer. Cold Spring Harbor Perspect. Biol. 1 (6), a003129.
13. Boardman, K.C., Swartz, M.A., 2003. Interstitial flow as a guide for lymphangiogenesis. Circ. Res. 92 (7), 801-808.
14. Bock, F., Onderka, J., Dietrich, T., Bachmann, B., Pytowski, B., Cursiefen, C., 2008. Blockade of VEGFR3-signalling specifically inhibits lymphangiogenesis in inflammatory corneal neovascularisation. Graefes Arch. Clin. Exp. Ophthalmol. 246 (1), 115-119.
15. Bono, A.V., Pannellini, T., Liberatore, M., Montironi, R., Cunico, S.C., Cheng, L., Sasso, F., Musiani, P., Iezzi, M., 2010. Sorafenib's inhibition of prostate cancer growth in transgenic adenocarcinoma mouse prostate mice and its differential effects on endothelial and pericyte growth during tumor angiogenesis. Anal. Quant. Cytol. Histol. 32 (3), 136-145.
16. Bressan, G.M., Daga-Gordini, D., Colombatti, A., Castellani, I., Marigo, V., Volpin, D., 1993. Emilin, a component of elastic fibers preferentially located at the elastin-microfibrils interface. J. Cell Biol. 121 (1), 201-212. (Pubitemid 23097376)
17. Brideau, G., Makinen, M.J., Elamaa, H., Tu, H., Nilsson, G., Alitalo, K., Pihlajaniemi, T., Heljasvaara, R., 2007. Endostatin overexpression inhibits lymphangiogenesis and lymph node metastasis in mice. Cancer Res. 67 (24), 11528-11535.
18. Bruyere, F., Melen-Lamalle, L., Blacher, S., Detry, B., Masset, A., Lecomte, J., Lambert, V., Maillard, C., Hoyer-Hansen, G., Lund, L.R., Foidart, J.M., Noel, A., 2010. Does plasminogen activator inhibitor-1 drive lymphangiogenesis? PLoS ONE 5 (3), e9653.
19. Bruyere, F., Melen-Lamalle, L., Blacher, S., Roland, G., Thiry, M., Moons, L., Frankenne, F., Carmeliet, P., Alitalo, K., Libert, C., Sleeman, J.P., Foidart, J.M., Noel, A., 2008. Modeling lymphangiogenesis in a three-dimensional culture system. Nat. Methods 5 (5), 431-437. (Pubitemid 351619102)
20. Cera, M.R., Del Prete, A., Vecchi, A., Corada, M., Martin-Padura, I., Motoike, T., Tonetti, P., Bazzoni, G., Vermi, W., Gentili, F., Bernasconi, S., Sato, T.N., Mantovani, A., Dejana, E., 2004. Increased DC trafficking to lymph nodes and contact hypersensitivity in junctional adhesion molecule-A-deficient mice. J. Clin. Invest. 114 (5), 729-738.
21. Chen, Z., Varney, M.L., Backora, M.W., Cowan, K., Solheim, J.C., Talmadge, J.E., Singh, R.K., 2005. Down-regulation of vascular endothelial cell growth factor-C expression using small interfering RNA vectors in mammary tumors inhibits tumor lymphangiogenesis and spontaneous metastasis and enhances survival. Cancer Res. 65 (19), 9004-9011. (Pubitemid 41377392)
22. Chen, L., Huq, S., Gardner, H., de Fougerolles, A.R., Barabino, S., Dana, M.R., 2007. Very late antigen 1 blockade markedly promotes survival of corneal allografts. Arch. Ophthalmol. 125 (6), 783-788.
23. Clasper, S., Royston, D., Baban, D., Cao, Y., Ewers, S., Butz, S., Vestweber, D., Jackson, D.G., 2008. A novel gene expression profile in lymphatics associated with tumor growth and nodal metastasis. Cancer Res. 68 (18), 7293-7303.
24. Clavin, N.W., Avraham, T., Fernandez, J., Daluvoy, S.V., Soares, M.A., Chaudhry, A., Mehrara, B.J., 2008. TGF-beta1 is a negative regulator of lymphatic regeneration during wound repair. Am. J. Physiol. Heart Circ. Physiol. 295 (5), H2113-H2127.
25. Colombatti, A., Doliana, R., Bot, S., Canton, A., Mongiat, M., Mungiguerra, G., Paron-Cilli, S., Spessotto, P., 2000. The EMILIN protein family. Matrix Biol. 19 (4), 289-301. (Pubitemid 30665652)
26. Da, M.X., Wu, Z., Tian, H.W., 2008. Tumor lymphangiogenesis and lymphangiogenic growth factors. Arch. Med. Res. 39 (4), 365-372.
27. Danussi, C., Spessotto, P., Petrucco, A., Wassermann, B., Sabatelli, P., Montesi, M., Doliana, R., Bressan, G.M., Colombatti, A., 2008. Emilin1 deficiency causes structural and functional defects of lymphatic vasculature. Mol. Cell. Biol. 28 (12), 4026-4039.
28. Dejana, E., Orsenigo, F., Molendini, C., Baluk, P., McDonald, D.M., 2009. Organization and signaling of endothelial cell-to-cell junctions in various regions of the blood and lymphatic vascular trees. Cell Tissue Res. 335 (1), 17-25.
29. Delva, E., Tucker, D.K., Kowalczyk, A.P., 2009. The desmosome. Cold Spring Harbor Perspect. Biol. 1 (2), a002543.
30. Dietrich, T., Bock, F., Yuen, D., Hos, D., Bachmann, B.O., Zahn, G., Wiegand, S., Chen, L., Cursiefen, C., 2010. Cutting edge: lymphatic vessels, not blood vessels, primarily mediate immune rejections after transplantation. J. Immunol. 184 (2), 535-539.
31. Dietrich, T., Onderka, J., Bock, F., Kruse, F.E., Vossmeyer, D., Stragies, R., Zahn, G., Cursiefen, C., 2007. Inhibition of inflammatory lymphangiogenesis by integrin alpha5 blockade. Am. J. Pathol. 171 (1), 361-372.
32. Durbeej, M., 2010. Laminins. Cell Tissue Res. 339 (1), 259-268.
33. Ebata, N., Nodasaka, Y., Sawa, Y., Yamaoka, Y., Makino, S., Totsuka, Y., Yoshida, S., 2001. Desmoplakin as a specific marker of lymphatic vessels. Microvasc. Res. 61 (1), 40-48.
34. El-Chemaly, S., Malide, D., Zudaire, E., Ikeda, Y., Weinberg, B.A., Pacheco-Rodriguez, G., Rosas, I.O., Aparicio, M., Ren, P., MacDonald, S.D., Wu, H.P., Nathan, S.D., Cuttitta, F., McCoy, J.P., Gochuico, B.R., Moss, J., 2009. Abnormal lymphangiogenesis in idiopathic pulmonary fibrosis with insights into cellular and molecular mechanisms. Proc. Natl. Acad. Sci. U. S. A 106 (10), 3958-3963.
35. Ellenberg, D., Azar, D.T., Hallak, J.A., Tobaigy, F., Han, K.Y., Jain, S., Zhou, Z., Chang, J.H., 2010. Novel aspects of corneal angiogenic and lymphangiogenic privilege. Prog. Retin. Eye Res. 29 (3), 208-248.
36. Fanjul-Fernandez, M., Folgueras, A.R., Cabrera, S., Lopez-Otin, C., 2010. Matrix metalloproteinases: evolution, gene regulation and functional analysis in mouse models. Biochim. Biophys. Acta 1803 (1), 3-19.
37. Ferrell, R.E., Baty, C.J., Kimak, M.A., Karlsson, J.M., Lawrence, E.C., Franke-Snyder, M., Meriney, S.D., Feingold, E., Finegold, D.N., 2010. GJC2 missense mutations cause human lymphedema. Am. J. Hum. Genet. 86 (6), 943-948.
38. Furuse, M., 2010. Molecular basis of the core structure of tight junctions. Cold Spring Harbor Perspect. Biol. 2 (1), a002907.
39. Gale, N.W., Prevo, R., Espinosa, J., Ferguson, D.J., Dominguez, M.G., Yancopoulos, G.D., Thurston, G., Jackson, D.G., 2007. Normal lymphatic development and function in mice deficient for the lymphatic hyaluronan receptor LYVE-1. Mol. Cell. Biol. 27 (2), 595-604.
40. Garmy-Susini, B., Avraamides, C.J., Schmid, M.C., Foubert, P., Ellies, L.G., Barnes, L., Feral, C., Papayannopoulou, T., Lowy, A., Blair, S.L., Cheresh, D., Ginsberg, M., Varner, J.A., 2010. Integrin alpha4beta1 signaling is required for lymphangiogenesis and tumor metastasis. Cancer Res. 70 (8), 3042-3051.
41. Gerli, R., Ibba, L., Fruschelli, C., 1990. A fibrillar elastic apparatus around human lymph capillaries. Anat. Embryol. (Berlin) 181 (3), 281-286.
42. Goffman, T.E., Laronga, C., Wilson, L., Elkins, D., 2004. Lymphedema of the arm and breast in irradiated breast cancer patients: risks in an era of dramatically changing axillary surgery. Breast J. 10 (5), 405-411. (Pubitemid 39281312)
43. Goldman, J., Conley, K.A., Raehl, A., Bondy, D.M., Pytowski, B., Swartz, M.A., Rutkowski, J.M., Jaroch, D.B., Ongstad, E.L., 2007. Regulation of lymphatic capillary regeneration by interstitial flow in skin. Am. J. Physiol. Heart Circ. Physiol. 292 (5), H2176-H2183.
44. Goodenough, D.A., Paul, D.L., 2009. Gap junctions. Cold Spring Harbor Perspect. Biol. 1 (1), a002576.
45. Gordon, M.K., Hahn, R.A., 2010. Collagens. Cell Tissue Res. 339 (1), 247-257.
46. Gridelli, C., Maione, P., Del Gaizo, F., Colantuoni, G., Guerriero, C., Ferrara, C., Nicolella, D., Comunale, D., De Vita, A., Rossi, A., 2007. Sorafenib and sunitinib in the treatment of advanced non-small cell lung cancer. Oncologist 12 (2), 191-200.
47. Guo, Y.L., Bai, R., Chen, C.X., Liu, D.Q., Liu, Y., Zhang, C.Y., Zen, K., 2009. Role of junctional adhesion molecule-like protein in mediating monocyte transendothelial migration. Arterioscler. Thromb. Vasc. Biol. 29 (1), 75-83.
48. Hamano, Y., Zeisberg, M., Sugimoto, H., Lively, J.C., Maeshima, Y., Yang, C., Hynes, R.O., Werb, Z., Sudhakar, A., Kalluri, R., 2003. Physiological levels of tumstatin, a fragment of collagen IV alpha3 chain, are generated by MMP-9 proteolysis and suppress angiogenesis via alphaV beta3 integrin. Cancer Cell 3 (6), 589-601. (Pubitemid 36808653)
49. Hammerling, B., Grund, C., Boda-Heggemann, J., Moll, R., Franke, W.W., 2006. The complexus adhaerens of mammalian lymphatic endothelia revisited: a junction even more complex than hitherto thought. Cell Tissue Res. 324 (1), 55-67. (Pubitemid 43320242)
50. He, X.W., Liu, T., Chen, Y.X., Cheng, D.J., Li, X.R., Xiao, Y., Feng, Y.L., 2008. Calcium carbonate nanoparticle delivering vascular endothelial growth factor-C siRNA effectively inhibits lymphangiogenesis and growth of gastric cancer in vivo. Cancer Gene Ther. 15 (3), 193-202. (Pubitemid 351240670)
51. He, Y., Kozaki, K., Karpanen, T., Koshikawa, K., Yla-Herttuala, S., Takahashi, T., Alitalo, K., 2002. Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling. J. Natl Cancer Inst. 94 (11), 819-825. (Pubitemid 34705053)
52. Heldin, C.H., Rubin, K., Pietras, K., Ostman, A., 2004. High interstitial fluid pressure - an obstacle in cancer therapy. Nat. Rev. Cancer 4 (10), 806-813.
53. Helm, C.L., Zisch, A., Swartz, M.A., 2007. Engineered blood and lymphatic capillaries in 3-D VEGF-fibrin-collagen matrices with interstitial flow. Biotechnol. Bioeng. 96 (1), 167-176.
54. Hirakawa, S., Brown, L.F., Kodama, S., Paavonen, K., Alitalo, K., Detmar, M., 2007. VEGF-C-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites. Blood 109 (3), 1010-1017. (Pubitemid 46220646)
55. Hirakawa, S., Hong, Y.K., Harvey, N., Schacht, V., Matsuda, K., Libermann, T., Detmar, M., 2003. Identification of vascular lineage-specific genes by transcriptional profiling of isolated blood vascular and lymphatic endothelial cells. Am. J. Pathol. 162 (2), 575-586.
56. Hong, Y.K., Lange-Asschenfeldt, B., Velasco, P., Hirakawa, S., Kunstfeld, R., Brown, L.F., Bohlen, P., Senger, D.R., Detmar, M., 2004. VEGF-A promotes tissue repair-associated lymphatic vessel formation via VEGFR-2 and the alpha1beta1 and alpha2beta1 integrins. FASEB J. 18 (10), 1111-1113. (Pubitemid 39561540)
57. Hos, D., Bock, F., Dietrich, T., Onderka, J., Kruse, F.E., Thierauch, K.H., Cursiefen, C., 2008. Inflammatory corneal (lymph)angiogenesis is blocked by VEGFR-tyrosine kinase inhibitor ZK 261991, resulting in improved graft survival after corneal transplantation. Invest. Ophthalmol. Vis. Sci. 49 (5), 1836-1842.
58. Huang, S.S., Liu, I.H., Smith, T., Shah, M.R., Johnson, F.E., Huang, J.S., 2006. CRSBP-1/LYVE-l-null mice exhibit identifiable morphological and functional alterations of lymphatic capillary vessels. FEBS Lett. 580 (26), 6259-6268. (Pubitemid 44666810)
59. Huang, X.Z., Wu, J.F., Ferrando, R., Lee, J.H., Wang, Y.L., Farese Jr., R.V., Sheppard, D., 2000. Fatal bilateral chylothorax in mice lacking the integrin alpha9beta1. Mol. Cell. Biol. 20 (14), 5208-5215.
60. Huggenberger, R., Ullmann, S., Proulx, S.T., Pytowski, B., Alitalo, K., Detmar, M., 2010. Stimulation of lymphangiogenesis via VEGFR-3 inhibits chronic skin inflammation. J. Exp. Med. 207 (10), 2255-2269.
61. Irjala, H., Alanen, K., Grenman, R., Heikkila, P., Joensuu, H., Jalkanen, S., 2003. Mannose receptor (MR) and common lymphatic endothelial and vascular endothelial receptor (CLEVER)-1 direct the binding of cancer cells to the lymph vessel endothelium. Cancer Res. 63 (15), 4671-4676. (Pubitemid 36951046)
62. Irjala, H., Johansson, E.L., Grenman, R., Alanen, K., Salmi, M., Jalkanen, S., 2001. Mannose receptor is a novel ligand for L-selectin and mediates lymphocyte binding to lymphatic endothelium. J. Exp. Med. 194 (8), 1033-1042.
63. Issa, A., Le, T.X., Shoushtari, A.N., Shields, J.D., Swartz, M.A., 2009. Vascular endothelial growth factor-C and C-C chemokine receptor 7 in tumor cell-lymphatic cross-talk promote invasive phenotype. Cancer Res. 69 (1), 349-357.
64. Jackson, D.G., 2009. Immunological functions of hyaluronan and its receptors in the lymphatics. Immunol. Rev. 230 (1), 216-231.
65. Ji, R.C., 2006. Lymphatic endothelial cells, lymphangiogenesis, and extracellular matrix. Lymphat. Res. Biol. 4 (2), 83-100.
66. Johnson, L.A., Clasper, S., Holt, A.P., Lalor, P.F., Baban, D., Jackson, D.G., 2006. An inflammation-induced mechanism for leukocyte transmigration across lymphatic vessel endothelium. J. Exp. Med. 203 (12), 2763-2777.
67. Jurisic, G., Iolyeva, M., Proulx, S.T., Halin, C., Detmar, M., 2010. Thymus cell antigen 1 (Thy1, CD90) is expressed by lymphatic vessels and mediates cell adhesion to lymphatic endothelium. Exp. Cell Res. 316 (17), 2982-2992.
68. Karikoski, M., Irjala, H., Maksimow, M., Miiluniemi, M., Granfors, K., Hernesniemi, S., Elima, K., Moldenhauer, G., Schledzewski, K., Kzhyshkowska, J., Goerdt, S., Salmi, M., Jalkanen, S., 2009. Clever-1/Stabilin-1 regulates lymphocyte migration within lymphatics and leukocyte entrance to sites of inflammation. Eur. J. Immunol. 39 (12), 3477-3487.
69. Karpanen, T., Alitalo, K., 2008. Molecular biology and pathology of lymphangiogenesis. Annu. Rev. Pathol. 3, 367-397.
70. Kawai, Y., Kaidoh, M., Ohhashi, T., 2008. MDA-MB-231 produces ATP-mediated ICAM-1-dependent facilitation of the attachment of carcinoma cells to human lymphatic endothelial cells. Am. J. Physiol. Cell Physiol. 295 (5), C1123-C1132.
71. Kielty, C.M., 2006. Elastic fibres in health and disease. Expert Rev. Mol. Med. 8 (19), 1-23.
72. Kim, M., Koh, Y.J., Kim, K.E., Koh, B.I., Nam, D.H., Alitalo, K., Kim, I., Koh, G.Y., 2010. CXCR4 signaling regulates metastasis of chemoresistant melanoma cells by a lymphatic metastatic niche. Cancer Res. 70 (24), 10411-10421.
73. Kojima, T., Azar, D.T., Chang, J.H., 2008. Neostatin-7 regulates bFGF-induced corneal lymphangiogenesis. FEBS Lett. 582 (17), 2515-2520.
74. Koyama, H., Kobayashi, N., Harada, M., Takeoka, M., Kawai, Y., Sano, K., Fujimori, M., Amano, J., Ohhashi, T., Kannagi, R., Kimata, K., Taniguchi, S., Itano, N., 2008. Significance of tumor-associated stroma in promotion of intratumoral lymphangiogenesis: pivotal role of a hyaluronan-rich tumor microenvironment. Am. J. Pathol. 172 (1), 179-193.
75. Kriehuber, E., Breiteneder-Geleff, S., Groeger, M., Soleiman, A., Schoppmann, S.F., Stingl, G., Kerjaschki, D., Maurer, D., 2001. Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages. J. Exp. Med. 194 (6), 797-808.
76. Kwaan, H.C., McMahon, B., 2009. The role of plasminogen-plasmin system in cancer. Cancer Treat. Res. 148, 43-66.
77. Lanati, S., Dunn, D.B., Roussigne, M., Emmett, M.S., Carriere, V., Jullien, D., Budge, J., Fryer, J., Erard, M., Cailler, F., Girard, J.P., Bates, D.O., 2010. Chemotrap-1: an engineered soluble receptor that blocks chemokine-induced migration of metastatic cancer cells in vivo. Cancer Res. 70 (20), 8138-8148.
78. Larrieu-Lahargue, F., Welm, A.L., Thomas, K.R., Li, D.Y., 2010. Netrin-4 induces lymphangiogenesis in vivo. Blood 115 (26), 5418-5426.
79. Leak, L.V., Burke, J.F., 1968. Ultrastructural studies on the lymphatic anchoring filaments. J. Cell Biol. 36 (1), 129-149.
80. Leak, L.V., Jones, M., 1994. Lymphangiogenesis in vitro: formation of lymphatic capillary-like channels from confluent monolayers of lymphatic endothelial cells. In Vitro Cell. Dev. Biol. Anim. 30A (8), 512-518. (Pubitemid 24243543)
81. Li, X., Shimada, T., Zhang, Y., Zhou, X., Zhao, L., 2009. Ultrastructure changes of cardiac lymphatics during cardiac fibrosis in hypertensive rats. Anat. Rec. (Hoboken) 292 (10), 1612-1618.
82. Lin, J., Lalani, A.S., Harding, T.C., Gonzalez, M., Wu, W.W., Luan, B., Tu, G.H., Koprivnikar, K., VanRoey, M.J., He, Y., Alitalo, K., Jooss, K., 2005. Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor. Cancer Res. 65 (15), 6901-6909. (Pubitemid 41060729)
83. Lund, A.W., Swartz, M.A., 2010. Role of lymphatic vessels in tumor immunity: passive conduits or active participants? J. Mammary Gland Biol. Neoplasia 15 (3), 341-352.
84. 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., 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 (11), 1057-1063.
85. Makinen, T., Norrmen, C., Petrova, T.V., 2007. Molecular mechanisms of lymphatic vascular development. Cell. Mol. Life Sci. 64 (15), 1915-1929.
86. Marttila-Ichihara, F., Turja, R., Miiluniemi, M., Karikoski, M., Maksimow, M., Niemela, J., Martinez-Pomares, L., Salmi, M., Jalkanen, S., 2008. Macrophage mannose receptor on lymphatics controls cell trafficking. Blood 112 (1), 64-72.
87. Masset, A., Maillard, C., Sounni, N.E., Jacobs, N., Bruyere, F., Delvenne, P., Tacke, M., Reinheckel, T., Foidart, J.M., Coussens, L.M., Noel, A., 2011. Unimpeded skin carcinogenesis in K14-HPV16 transgenic mice deficient for plasminogen activator inhibitor. Int. J. Cancer 128 (2), 283-293.
88. Matsuo, M., Sakurai, H., Koizumi, K., Saiki, I., 2007. Curcumin inhibits the formation of capillary-like tubes by rat lymphatic endothelial cells. Cancer Lett. 251 (2), 288-295. (Pubitemid 46669800)
89. McColl, B.K., Baldwin, M.E., Roufail, S., Freeman, C., Moritz, R.L., Simpson, R.J., Alitalo, K., Stacker, S.A., Achen, M.G., 2003. Plasmin activates the lymphangiogenic growth factors VEGF-C and VEGF-D. J. Exp. Med. 198 (6), 863-868.
90. Meng, W., Takeichi, M., 2009. Adherens junction: molecular architecture and regulation. Cold Spring Harbor Perspect. Biol. 1 (6), a002899.
91. Miner, J.H., Yurchenco, P.D., 2004. Laminin functions in tissue morphogenesis. Annu. Rev. Cell Dev. Biol. 20, 255-284.
92. Mishima, K., Watabe, T., Saito, A., Yoshimatsu, Y., Imaizumi, N., Masui, S., Hirashima, M., Morisada, T., Oike, Y., Araie, M., Niwa, H., Kubo, H., Suda, T., Miyazono, K., 2007. Prox1 induces lymphatic endothelial differentiation via integrin alpha9 and other signaling cascades. Mol. Biol. Cell 18 (4), 1421-1429.
93. Miteva, D.O., Rutkowski, J.M., Dixon, J.B., Kilarski, W., Shields, J.D., Swartz, M.A., 2010. Transmural flow modulates cell and fluid transport functions of lymphatic endothelium. Circ. Res. 106 (5), 920-931.
94. Mouta, C., Heroult, M., 2003. Inflammatory triggers of lymphangiogenesis. Lymphat. Res. Biol. 1 (3), 201-218.
95. Nakamura, E.S., Koizumi, K., Kobayashi, M., Saiki, I., 2004. Inhibition of lymphangiogenesis-related properties of murine lymphatic endothelial cells and lymph node metastasis of lung cancer by the matrix metalloproteinase inhibitor MMI270. Cancer Sci. 95 (1), 25-31. (Pubitemid 38208403)
96. Negrini, D., Passi, A., Moriondo, A., 2008. The role of proteoglycans in pulmonary edema development. Intensive Care Med. 34 (4), 610-618.
97. Ng, C.P., Helm, C.L., Swartz, M.A., 2004. Interstitial flow differentially stimulates blood and lymphatic endothelial cell morphogenesis in vitro. Microvasc. Res. 68 (3), 258-264.
98. Noel, A., Jost, M., Maquoi, E., 2008. Matrix metalloproteinases at cancer tumor-host interface. Semin. Cell Dev. Biol. 19 (1), 52-60.
99. Norrmen, C., Tammela, T., Petrova, T.V., Alitalo, K., 2011. Biological basis of therapeutic lymphangiogenesis. Circulation 123 (12), 1335-1351.
100. Nusgens, B.V., 2010. Hyaluronic acid and extracellular matrix: a primitive molecule? Ann. Dermatol. Venereol. 137 (Suppl. 1), 3-8.
101. Oh, S.J., Jeltsch, M.M., Birkenhager, R., McCarthy, J.E., Weich, H.A., Christ, B., Alitalo, K., Wilting, J., 1997. VEGF and VEGF-C: specific induction of angiogenesis and lymphangiogenesis in the differentiated avian chorioallantoic membrane. Dev. Biol. 188 (1), 96-109.
102. Okazaki, T., Ni, A., Ayeni, O.A., Baluk, P., Yao, L.C., Vossmeyer, D., Zischinsky, G., Zahn, G., Knolle, J., Christner, C., McDonald, D.M., 2009. Alpha5beta1 Integrin blockade inhibits lymphangiogenesis in airway inflammation. Am. J. Pathol. 174 (6), 2378-2387.
103. Orlova, V.V., Chavakis, T., 2007. Regulation of vascular endothelial permeability by junctional adhesion molecules (JAM). Thromb. Haemost. 98 (2), 327-332. (Pubitemid 47250235)
104. Ou, J.J., Wu, F., Liang, H.J., 2010. Colorectal tumor derived fibronectin alternatively spliced EDA domain exerts lymphangiogenic effect on human lymphatic endothelial cells. Cancer Biol. Ther. 9 (3), 186-191.
105. Page-McCaw, A., Ewald, A.J., Werb, Z., 2007. Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 8 (3), 221-233.
106. Pelosi, P., Rocco, P.R., Negrini, D., Passi, A., 2007. The extracellular matrix of the lung and its role in edema formation. An. Acad. Bras. Cienc. 79 (2), 285-297.
107. Pepper, M.S., Skobe, M., 2003. Lymphatic endothelium: morphological, molecular and functional properties. J. Cell Biol. 163 (2), 209-213. (Pubitemid 37363121)
108. Perez-Santonja, J.J., Campos-Mollo, E., Lledo-Riquelme, M., Javaloy, J., Alio, J.L. 2010. Inhibition of corneal neovascularization by topical bevacizumab (Anti-VEGF) and Sunitinib (Anti-VEGF and Anti-PDGF) in an animal model. Am. J. Ophthalmol. 150 (4), 519-528 e511.
109. Petrova, T.V., Karpanen, T., Norrmen, C., Mellor, R., Tamakoshi, T., Finegold, D., Ferrell, R., Kerjaschki, D., Mortimer, P., Yla-Herttuala, S., Miura, N., Alitalo, K., 2004. Defective valves and abnormal mural cell recruitment underlie lymphatic vascular failure in lymphedema distichiasis. Nat. Med. 10 (9), 974-981.
110. Podgrabinska, S., Braun, P., Velasco, P., Kloos, B., Pepper, M.S., Skobe, M., 2002. Molecular characterization of lymphatic endothelial cells. Proc. Natl. Acad. Sci. U. S. A 99 (25), 16069-16074.
111. Podgrabinska, S., Kamalu, O., Mayer, L., Shimaoka, M., Snoeck, H., Randolph, G.J., Skobe, M., 2009. Inflamed lymphatic endothelium suppresses dendritic cell maturation and function via Mac-1/ICAM-1-dependent mechanism. J. Immunol. 183 (3), 1767-1779.
112. Raschperger, E., Thyberg, J., Pettersson, S., Philipson, L., Fuxe, J., Pettersson, R.F., 2006. The coxsackie- and adenovirus receptor (CAR) is an in vivo marker for epithelial tight junctions, with a potential role in regulating permeability and tissue homeostasis. Exp. Cell Res. 312 (9), 1566-1580.
113. Regenfuss, B., Bock, F., Parthasarathy, A., Cursiefen, C., 2008. Corneal (lymph)angiogenesis-from bedside to bench and back: a tribute to Judah Folkman. Lymphat. Res. Biol. 6 (3-4), 191-201.
114. Regenfuss, B., Onderka, J., Bock, F., Hos, D., Maruyama, K., Cursiefen, C., 2010. Genetic heterogeneity of lymphangiogenesis in different mouse strains. Am. J. Pathol. 177 (1), 501-510.
115. Rinderknecht, M., Villa, A., Ballmer-Hofer, K., Neri, D., Detmar, M., 2010. Phage-derived fully human monoclonal antibody fragments to human vascular endothelial growth factor-C block its interaction with VEGF receptor-2 and 3. PLoS ONE 5 (8), e11941.
116. Roberts, N., Kloos, B., Cassella, M., Podgrabinska, S., Persaud, K., Wu, Y., Pytowski, B., Skobe, M., 2006. Inhibition of VEGFR-3 activation with the antagonistic antibody more potently suppresses lymph node and distant metastases than inactivation of VEGFR-2. Cancer Res. 66 (5), 2650-2657.
117. Roskoski Jr., R., 2007. Sunitinib: a VEGF and PDGF receptor protein kinase and angiogenesis inhibitor. Biochem. Biophys. Res. Commun. 356 (2), 323-328.
118. Saalbach, A., Wetzel, A., Haustein, U.F., Sticherling, M., Simon, J.C., Anderegg, U., 2005. Interaction of human Thy-1 (CD 90) with the integrin alphavbeta3 (CD51/CD61): an important mechanism mediating melanoma cell adhesion to activated endothelium. Oncogene 24 (29), 4710-4720. (Pubitemid 41032607)
119. Salmi, M., Koskinen, K., Henttinen, T., Elima, K., Jalkanen, S., 2004. CLEVER-1 mediates lymphocyte transmigration through vascular and lymphatic endothelium. Blood 104 (13), 3849-3857. (Pubitemid 39620128)
120. Sawa, Y., Shibata, K., Braithwaite, M.W., Suzuki, M., Yoshida, S., 1999. Expression of immunoglobulin superfamily members on the lymphatic endothelium of inflamed human small intestine. Microvasc. Res. 57 (2), 100-106.
121. Sawa, Y., Ueki, T., Hata, M., Iwasawa, K., Tsuruga, E., Kojima, H., Ishikawa, H., Yoshida, S., 2008. LPS-induced IL-6, IL-8, VCAM-1, and ICAM-1 expression in human lymphatic endothelium. J. Histochem. Cytochem. 56 (2), 97-109.
122. Schaefer, L., Schaefer, R.M., 2010. Proteoglycans: from structural compounds to signaling molecules. Cell Tissue Res. 339 (1), 237-246.
123. Schenkel, A.R., Chew, T.W., Chlipala, E., Harbord, M.W., Muller, W.A., 2006. Different susceptibilities of PECAM-deficient mouse strains to spontaneous idiopathic pneumonitis. Exp. Mol. Pathol. 81 (1), 23-30.
124. Schenkel, A.R., Chew, T.W., Muller, W.A., 2004. Platelet endothelial cell adhesion molecule deficiency or blockade significantly reduces leukocyte emigration in a majority of mouse strains. J. Immunol. 173 (10), 6403-6408. (Pubitemid 39487800)
125. Schmelz, M., Moll, R., Kuhn, C., Franke, W.W., 1994. Complexus adhaerentes, a new group of desmoplakin-containing junctions in endothelial cells: II. Different types of lymphatic vessels. Differentiation 57 (2), 97-117. (Pubitemid 24211106)
126. Seidman, M.A., Chew, T.W., Schenkel, A.R., Muller, W.A., 2009. PECAM-independent thioglycollate peritonitis is associated with a locus on murine chromosome 2. PLoS ONE 4 (1), e4316.
127. Shields, J.D., Fleury, M.E., Yong, C., Tomei, A.A., Randolph, G.J., Swartz, M.A., 2007. Autologous chemotaxis as a mechanism of tumor cell homing to lymphatics via interstitial flow and autocrine CCR7 signaling. Cancer Cell 11 (6), 526-538. (Pubitemid 46856909)
128. Singh, P., Carraher, C., Schwarzbauer, J.E., 2010. Assembly of fibronectin extracellular matrix. Annu. Rev. Cell Dev. Biol. 26, 397-419.
129. Sleeman, J.P., Thiele, W., 2009. Tumor metastasis and the lymphatic vasculature. Int. J. Cancer 125 (12), 2747-2756.
130. Stramer, B.M., Mori, R., Martin, P., 2007. The inflammation-fibrosis link? A Jekyll and Hyde role for blood cells during wound repair. J. Invest. Dermatol. 127 (5), 1009-1017.
131. Stratman, A.N., Malotte, K.M., Mahan, R.D., Davis, M.J., Davis, G.E., 2009. Pericyte recruitment during vasculogenic tube assembly stimulates endothelial basement membrane matrix formation. Blood 114 (24), 5091-5101.
132. Tammela, T., Alitalo, K., 2010. Lymphangiogenesis: molecular mechanisms and future promise. Cell 140 (4), 460-476.
133. Tammela, T., Petrova, T.V., Alitalo, K., 2005. Molecular lymphangiogenesis: new players. Trends Cell Biol. 15 (8), 434-441. (Pubitemid 41125775)
134. Tvorogov, D., Anisimov, A., Zheng, W., Leppanen, V.M., Tammela, T., Laurinavicius, S., Holnthoner, W., Helotera, H., Holopainen, T., Jeltsch, M., Kalkkinen, N., Lankinen, H., Ojala, P.M., Alitalo, K., 2010. Effective suppression of vascular network formation by combination of antibodies blocking VEGFR ligand binding and receptor dimerization. Cancer Cell 18 (6), 630-640.
135. Ueki, T., Iwasawa, K., Ishikawa, H., Sawa, Y., 2008. Expression of junctional adhesion molecules on the human lymphatic endothelium. Microvasc. Res. 75 (2), 269-278.
136. Vigl, B., Zgraggen, C., Rehman, N., Banziger-Tobler, N.E., Detmar, M., Halin, C., 2009. Coxsackie and adenovirus receptor (CAR) is expressed in lymphatic vessels in human skin and affects lymphatic endothelial cell function in vitro. Exp. Cell Res. 315 (2), 336-347.
137. Vlahakis, N.E., Young, B.A., Atakilit, A., Sheppard, D., 2005. The lymphangiogenic vascular endothelial growth factors VEGF-C and -D are ligands for the integrin alpha9beta1. J. Biol. Chem. 280 (6), 4544-4552.
138. von der Weid, P.Y., Rainey, K.J., 2010. Review article: lymphatic system and associated adipose tissue in the development of inflammatory bowel disease. Aliment. Pharmacol. Ther. 32 (6), 697-711.
139. Wang, Y., Oliver, G., 2010. Current views on the function of the lymphatic vasculature in health and disease. Genes Dev. 24 (19), 2115-2126.
140. Wegmann, F., Petri, B., Khandoga, A.G., Moser, C., Khandoga, A., Volkery, S., Li, H., Nasdala, I., Brandau, O., Fassler, R., Butz, S., Krombach, F., Vestweber, D., 2006. ESAM supports neutrophil extravasation, activation of Rho, and VEGF-induced vascular permeability. J. Exp. Med. 203 (7), 1671-1677.
141. Wetzel, A., Chavakis, T., Preissner, K.T., Sticherling, M., Haustein, U.F., Anderegg, U., Saalbach, A., 2004. Human Thy-1 (CD90) on activated endothelial cells is a counterreceptor for the leukocyte integrin Mac-1 (CD11b/CD18). J. Immunol. 172 (6), 3850-3859. (Pubitemid 38337972)
142. Wiig, H., Keskin, D., Kalluri, R., 2010. Interaction between the extracellular matrix and lymphatics: consequences for lymphangiogenesis and lymphatic function. Matrix Biol. 29 (8), 645-656.
143. Witte, M.H., Dellinger, M.T., McDonald, D.M., Nathanson, S.D., Boccardo, F.M., Campisi, C.C., Sleeman, J.P., Gershenwald, J.E., 2011. Lymphangiogenesis and hemangiogenesis: potential targets for therapy. J. Surg. Oncol. 103 (6), 489-500.
144. Young, E., Miele, L., Tucker, K.B., Huang, M., Wells, J., Gu, J.W., 2010. SU11248, a selective tyrosine kinases inhibitor suppresses breast tumor angiogenesis and growth via targeting both tumor vasculature and breast cancer cells. Cancer Biol. Ther. 10 (7), 703-711.
145. Zawieja, D.C., Davis, K.L., Schuster, R., Hinds, W.M., Granger, H.J. 1993. Distribution, propagation, and coordination of contractile activity in lymphatics. Am. J. Physiol. 264 (4 Pt 2), H1283-1291.
146. Zhang, X., Groopman, J.E., Wang, J.F., 2005. Extracellular matrix regulates endothelial functions through interaction of VEGFR-3 and integrin alpha5beta1. J. Cell. Physiol. 202 (1), 205-214.