Lymphangiogenesis and cancer metastasis

Frontiers in Bioscience

Volumn 16, Issue 2, 2011, Pages 723-739

  Al Rawi, Mahir Aa ^a   Jiang, Wen G ^b  

^a GLAN CLWYD HOSPITAL   (United Kingdom)

^b CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

Author keywords

Cancer; Lymphangiogenesis; Lymphatic; Metastasis; Review

Indexed keywords

5' NUCLEOTIDASE; BIOLOGICAL MARKER; HOMEODOMAIN PROTEIN; LYMPHATIC VESSEL ENDOTHELIAL HA RECEPTOR 1 PROTEIN, HUMAN; LYMPHATIC VESSEL ENDOTHELIAL HA RECEPTOR-1 PROTEIN, HUMAN; MEMBRANE PROTEIN; PDPN PROTEIN, HUMAN; PROSPERO RELATED HOMEOBOX 1 PROTEIN; PROSPERO-RELATED HOMEOBOX 1 PROTEIN; TUMOR SUPPRESSOR PROTEIN; VASCULOTROPIN; VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 3; VESICULAR TRANSPORT PROTEIN;

ANIMAL; HUMAN; LYMPH NODE METASTASIS; LYMPHANGIOGENESIS; LYMPHATIC SYSTEM; METABOLISM; NEOPLASM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; WEIBEL PALADE BODY;

5'-NUCLEOTIDASE; ANIMALS; BIOLOGICAL MARKERS; HOMEODOMAIN PROTEINS; HUMANS; LYMPHANGIOGENESIS; LYMPHATIC METASTASIS; LYMPHATIC SYSTEM; MEMBRANE GLYCOPROTEINS; NEOPLASMS; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3; VASCULAR ENDOTHELIAL GROWTH FACTORS; VESICULAR TRANSPORT PROTEINS; WEIBEL-PALADE BODIES;

EID: 79955029845     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/3715     Document Type: Article

References (185)

1. J. P. Sleeman: The lymph node as a bridgehead in the metastatic dissemination of tumours. Recent Results Cancer Res, 157, 55-81 (2000)
2. M. Francois, A. Caprini, B. Hosking, F. Orsenigo, D. Wilhelm, C. Browne, K. Paavonen, T. Karnezis, R. Shayan, M. Downes, T. Davidson, D. Tutt, K. S. Cheah, S. A. Stacker, G. E. Muscat, M. G. Achen, E. Dejana and P. Koopman: Sox18 induces development of the lymphatic vasculature in mice. Nature, 456(7222), 643-7 (2008)
3. J. T. Wigle and G. Oliver: Prox1 function is required for the development of the murine lymphatic system. Cell, 98(6), 769-78 (1999) d (Pubitemid 29446894)
4. W. P. Dunworth and K. M. Caron: G protein-coupled receptors as potential drug targets for lymphangiogenesis and lymphatic vascular diseases. Arterioscler Thromb Vasc Biol, 29(5), 650-6 (2009)
5. J. Folkman: Angiogenesis and tumour growth. New Eng J Med, 334, 921 (1996)
6. F. E. Fisher B: Role of the lymphatic system in dissemination of tumour. Lymph and lymphatic system(Sprigfield IL), 324 (1968)
7. D. A. B. A J Leu, A Lymboussaki, K Alitalo, R K jain: Absence of functional lymphatics within a murine sarcoma: a molecular and functional evaluation. Cancer Res, 60, 4324-4327 (2000) (Pubitemid 32103603)
8. P. Carmeliet and R. Jain: Angiogenisis in cancer and other diseases. Nature Med, 407, 249-257 (2000)
9. R. Jain: Transport of molecules in the tumour interstitium: a review. Cancer Res, 47, 3039-3051 (1987) (Pubitemid 17082621)
10. N. Tanigawa, T. Kanazawa, K. Satomura, Y. Hikasa, M. Hashida, S. Muranishi and H. Sezaki: Experimental-Study on Lymphatic Vascular Changes in the Development of Cancer. Lymphology, 14(4), 149-154 (1981) (Pubitemid 12250913)
11. A. J. Leu, D. A. Berk, A. Lymboussaki, K. Alitalo and R. K. Jain: Absence of functional lymphatics within a murine sarcoma: A molecular and functional evaluation. Cancer Res, 60(16), 4324-4327 (2000) (Pubitemid 32103603)
12. F. Hartveit: Attenuated Cells in Breast Stroma-the Missing Lymphatic-System of the Breast. Histopathology, 16(6), 533-543 (1990) (Pubitemid 20183002)
13. S. Breiteneder-Geleff, A. Soleiman, H. Kowalski, R. Horvat, G. Amman, E. Kriehuber, K. Diem, W. Weninger, E. Tschachler, K. Alitalo and D. Kerjaschki: Angiosarcomas express mixed endothelial phenotypes of blood and lymphatic capillaries: Podoplanin as a specific marker for lymphatic endothelium. Am J Patholy, 154, 385-394 (1999) (Pubitemid 29094089)
14. W. Weninger, T. A. Partanen, S. Breiteneder-Geleff, C. Mayer, H. Kowalski, M. Mildner, J. Pammer, M. Sturzl, D. Kerjaschki, K. Alitalo and E. Tschachler: Expression of vascular endothelial growth factor receptor-3 and podoplanin suggests a lymphatic endothelial cell origin of Kaposi's sarcoma tumour cells. Lab Invest, 79(2), 243-251 (1999) (Pubitemid 29110654)
15. J. Wigle and G. Oliver: Prox-1 function is required for the development of the murine lymphatic system. Cell, 98, 769-778 (1999) (Pubitemid 29446894)
16. G. Oliver, B. Sosapineda, S. Geisendorf, E. P. Spana, C. Q. Doe and P. Gruss: Prox-1, a Prospero-Related Homeobox Gene Expressed During Mouse Development. Mech Develop, 44(1), 3-16 (1993) (Pubitemid 24037694)
17. S. Banerji, J. Ni, S. X. Wang, S. Clasper, J. Su, R. Tammi, M. Jones and D. G. Jackson: LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J Cell Biol, 144(4), 789-801 (1999) (Pubitemid 29234556)
18. S. J. Mandriota, L. Jussila, M. Jeltsch, A. Compagni, D. Baetens, R. Prevo, S. Banerji, J. Huarte, R. Montesano, D. G. Jackson, L. Orci, K. Alitalo, G. Christofori and M. S. Pepper: Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis. Embo J, 20(4), 672-682 (2001) (Pubitemid 32167632)
19. M. Skobe, T. Hawighorst, D. G. Jackson, R. Prevo, L. Janes, P. Velasco, L. Riccardi, K. Alitalo, K. Claffey and M. Detmar: Induction of tumour lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nature Med, 7(2), 192-198 (2001) (Pubitemid 32148486)
20. C. C. Stacker SA, Baldwin ME, Thornton GE, Williams RA, Prevo R, Jackson DG, Nishikawa S, Kubo H, Achen MG: VEGF-D promots the metastatic spreadof tumour cells via the lymphatics. Nat Med, 7, 186-191 (2001) (Pubitemid 32148485)
21. A. Kaipainen, J. Korhonen, T. Mustonen, V. W. van Hinsbergh, G. H. Fang, D. Dumont, M. Breitman and K. Alitalo: Expression of the fms-like tyrosine kinase 4 gene becomes restricted to lymphatic endothelium during development. Proc Natl Acad Sci U S A, 92(8), 3566-70 (1995)
22. M. J. Karkkainen, R. E. Ferrell, E. C. Lawrence, M. A. Kimak, K. L. Levinson, M. A. McTigue, K. Alitalo and D. N. Finegold: Missense mutations interfere with VEGFR-3 signalling in primary lymphoedema. Nat Genet, 25(2), 153-9 (2000) (Pubitemid 30394984)
23. M. J. Karkkainen and T. V. Petrova: Vascular endothelial growth factor receptors in the regulation of angiogenesis and lymphangiogenesis. Oncogene, 19(49), 5598-605 (2000)
24. L. Jussila and K. Alitalo: Vascular growth factors and lymphangiogenesis. Physiol Rev, 82(3), 673-700 (2002) (Pubitemid 34743335)
25. M. J. Karkkainen, K. Alitalo and T. Makinen: Lymphatic endothelial regulation, lymphoedema, and lymph node metastasisLymphatic endothelium: a new frontier of metastasis research. Semin Cell Dev Biol, 13(1), 9-18 (2002)
26. M. J. Karkkainen, T. Makinen and K. Alitalo: Lymphatic endothelium: a new frontier of metastasis research. Nat Cell Biol, 4(1), E2-5 (2002) (Pubitemid 34071967)
27. M. J. Karkkainen, L. Jussila, R. E. Ferrell, D. N. Finegold and K. Alitalo: Molecular regulation of lymphangiogenesis and targets for tissue oedema. Trends Mol Med, 7(1), 18-22 (2001) (Pubitemid 33718078)
28. K. Alitalo: Vascular endothelial growth factors and receptors involved in angiogenesis and lymphangiogenesis. Eur J Cancer, 33, 1017-1017 (1997)
29. M. J. Karkkainen and K. Alitalo: Lymphatic endothelial regulation, lymphoedema, and lymph node metastasis. Semin Cell Dev Biol, 13(1), 9-18 (2002) (Pubitemid 35418310)
30. K. Alitalo and P. Carmeliet: Molecular mechanisms of lymphangiogenesis in health and disease. Cancer Cell, 1(3), 219-27 (2002) (Pubitemid 41039145)
31. G. Oliver and M. Detmar: The rediscovery of the lymphatic system: old and new insights into the development and biological function of the lymphatic vasculature. Genes Dev, 16(7), 773-83 (2002) (Pubitemid 34280101)
32. P. O. Van Trappen and M. S. Pepper: Lymphangiogenesis and lymph node microdissemination. Gynecologic Oncology, 82(1), 1-3 (2001) (Pubitemid 32634944)
33. D. Hanahan and R. A. Weinberg: The hallmarks of cancer. Cell, 100(1), 57-70 (2000) (Pubitemid 30046295)
34. N. Weidner: Intratumour microvessel density as a prognostic factor in cancer. Am J Pathol, 147(1), 9-19 (1995)
35. P. Birner, M. Schindl, A. Obermair, G. Breitenecker, H. Kowalski and G. Oberhuber: Lymphatic microvessel density as a novel prognostic factor in early-stage invasive cervical cancer. Int J Cancer, 95(1), 29-33 (2001)
36. P. Birner, M. Schindl, A. Obermair, C. Plank, G. Breitenecker, H. Kowalski and G. Oberhuber: Lymphatic microvessel density in epithelial ovarian cancer: its impact on prognosis. Anticancer Res, 20(5A), 2981-5 (2000)
37. G. A. Lee J, Yuan J, Luoh SM, Avraham H, Wood WI: Vascular endothelial growth factor-related protein: a ligand and specific activator of the tyrosine kinase receptor Flt4. Proc Natl Acad Sci USA(93), 1988-1992 (1996) (Pubitemid 26079868)
38. B. Olofsson, M. Jeltsch, U. Eriksson and K. Alitalo: Current biology of VEGF-B and VEGF-C. Cur Opinion Biotechnology, 10(6), 528-535 (1999)
39. P. K. Joukov V, Kaipainen A, Chilov D, Lahtinen I, Kukk E, Saksela O, Kalkkinen N, Alitalo K: 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 [erratum EMBO J 1996;15:1751] (1996) (Pubitemid 26029207)
40. M. Orlandini, L. Marconcini, R. Ferruzzi and S. Oliviero: 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 U S A, 93(21), 11675-80 (1996)
41. D. Shweiki, M. Neeman, A. Itin and E. Keshet: Induction of vascular endothelial growth factor expression by hypoxia and by glucose deficiency in multicell spheroids: implications for tumour angiogenesis. Proc Natl Acad Sci U S A, 92(3), 768-72 (1995)
42. M. G. Achen, R. A. Williams, M. P. Minekus, G. E. Thornton, K. Stenvers, P. A. Rogers, F. Lederman, S. Roufail and S. A. Stacker: Localization of vascular endothelial growth factor-D in malignant melanoma suggests a role in tumour angiogenesis. J Pathol, 193(2), 147-54 (2001) (Pubitemid 32118124)
43. N. Ferrara and T. Davis-Smyth: The biology of vascular endothelial growth factor. Endocr Rev, 18(1), 4-25 (1997) (Pubitemid 27076453)
44. P. Salven, A. Lymboussaki, P. Heikkila, H. Jaaskela-Saari, B. Enholm, K. Aase, G. von Euler, U. Eriksson, K. Alitalo and H. Joensuu: Vascular endothelial growth factors VEGF-B and VEGF-C are expressed in human tumours. Am J Pathol, 153(1), 103-8 (1998) (Pubitemid 28317512)
45. T. Karpanen, M. Egeblad, M. J. Karkkainen, H. Kubo, S. Yla-Herttuala, M. Jaattela and K. Alitalo: Vascular endothelial growth factor C promotes tumour lymphangiogenesis and intralymphatic tumour growth. Cancer Res, 61(5), 1786-1790 (2001) (Pubitemid 32691984)
46. S. Stacker, C. Caeser, M. Baldwin, G. Thornton, R. Williams, R. Prevo, D. Jackson, S. Nishikawa, H. Kubo and M. Achen: VEGF-D promots the metastatic spread of tumour cells via the lymphatics. Nat Med, 7, 186-191 (2001) (Pubitemid 32148485)
47. M. S. Pepper: Lymphangiogenesis and tumour metastasis: Myth or reality? Clin Cancer Res, 7(3), 462-468 (2001) (Pubitemid 32707965)
48. V. Joukov, K. Pajusola, A. Kaipainen, D. Chilov, I. Lahtinen, E. Kukk, O. Saksela, N. Kalkkinen and K. Alitalo: A novel vascular endothelial growth factor, VEGFC, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J(15), 290-298 [erratum EMBO J 1996;15:1751] (1996) (Pubitemid 26029207)
49. J. Lee, A. Gray, J. Yuan, S. Luoh, H. Avraham and W. Wood: Vascular endothelial growth factor-related protein: a ligand and specific activator of the tyrosine kinase receptor Flt4. Proc Natl Acad Sci USA(93), 1988-1992 (1996) (Pubitemid 26079868)
50. M. Achen, M. Jeltsch, E. Kukk, T. Makinen, A. Vitali, A. Wilks, K. Alitalo and S. Stacker: Vascular endothelial growth factor-D (VEGF-D) is a ligand for tyrosine kinases VEGF receptor 2 (Flk1) and VEGF receptor 3 (Flk4). Proc Natl Acad Sci USA, 95, 548-553 (1998) (Pubitemid 28083780)
51. J. M. Achen MG, Kukk E, Makinen T, Vitali A, Wilks AF, Alitalo K, Stacker SA: Vascular endothelial growth factor-D (VEGF-D) is a ligand for tyrosine kinases VEGF receptor 2 (Flk1) and VEGF receptor 3 (Flk4). Proc Natl Acad Sci USA, 95, 548-553 (1998) (Pubitemid 28083780)
52. V. Joukov, T. Sorsa, V. Kumar, M. Jeltsch, L. ClaessonWelsh, Y. H. Cao, O. Saksela, N. Kalkkinen and K. Alitalo: Proteolytic processing regulates receptor specificity and activity of VEGF-C. Embo J, 16(13), 3898-3911 (1997) (Pubitemid 27281006)
53. E. Kukk, A. Lymboussaki, S. Taira, A. Kaipainen, M. Jeltsch, V. Joukov and K. Alitalo: VEGF-C receptor binding and pattern of expression with VEGFR-3 suggests a role in lymphatic vascular development. Development, 122(12), 3829-37 (1996) (Pubitemid 27033879)
54. M. Jeltsch, A. Kaipainen, V. Joukov, X. Meng, M. Lakso, H. Rauvala, M. Swartz, D. Fukumura, R. Jain and K. Alitalo: Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science, 276, 1423-1425 [erratum Science 1997;277:463] (1997) (Pubitemid 27235412)
55. S. Oh, M. Jeltsch, R. Birkenhager, J. McCarthy, H. Weich, B. Christ, K. Alitalo and J. Wilting: VEGF and VEGF-C: specific induction of angiogenesis and lymphangiogenesis in the differentiated avian chorioallantoic membrane. Dev Biol, 188, 96-109 (1997) (Pubitemid 27360090)
56. Y. Cao, P. Linden, J. Farnebo, R. Cao, A. Eriksson, V. Kumar, J. H. Qi, L. Claesson-Welsh and K. Alitalo: Vascular endothelial growth factor C induces angiogenesis in vivo. Proc Natl Acad Sci U S A, 95(24), 14389-94 (1998) (Pubitemid 28549377)
57. B. Witzenbichler, T. Asahara, T. Murohara, M. Silver, I. Spyridopoulos, M. Magner, N. Principe, M. Kearney, J. S. Hu and J. M. Isner: Vascular endothelial growth factor-C (VEGF-C/VEGF-2) promotes angiogenesis in the setting of tissue ischemia. Am J Pathol, 153(2), 381-94 (1998) (Pubitemid 28373650)
58. G. Bunone, P. Vigneri, L. Mariani, S. Buto, P. Collini, S. Pilotti, M. A. Pierotti and I. Bongarzone: Expression of angiogenesis stimulators and inhibitors in human thyroid tumours and correlation with clinical pathological features. American J Pathol, 155(6), 1967-1976 (1999)
59. Y. Yonemura, Y. Endo, H. Fujita, S. Fushida, I. Ninomiya, E. Bandou, K. Taniguchi, K. Miwa, S. Ohoyama, K. Sugiyama and T. Sasaki: Role of vascular endothelial growth factor C expression in the development of lymph node metastasis in gastric cancer. Clin Cancer Res, 5(7), 1823-1829 (1999) (Pubitemid 29334464)
60. K. Akagi, Y. Ikeda, M. Miyazaki, T. Abe, J. Kinoshita, Y. Maehara and K. Sugimachi: Vascular endothelial growth factor-C (VEGF-C) expression in human colorectal cancer tissues. Br J Cancer, 83(7), 887-891 (2000)
61. T. Niki, S. Iba, M. Tokunou, T. Yamada, Y. Matsuno and S. Hirohashi: Expression of vascular endothelial growth factors A, B, C, and D and their relationships to lymph node status in lung adenocarcinoma. Clin Cancer Res, 6(6), 2431-2439 (2000) (Pubitemid 30399212)
62. Y. Ohta, H. Nozawa, Y. Tanaka, M. Oda and Y. Watanabe: Increased vascular endothelial growth factor and vascular endothelial growth factor-C and decreased NM23 expression associated with microdissemination in the lymph nodes in stage I non-small cell lung cancer. J Thoracic Cardiovascular Surg, 119(4), 804-813 (2000) (Pubitemid 30395479)
63. Y. Ohta, V. Shridhar, R. K. Bright, G. P. Kalemkerian, W. Du, M. Carbone, Y. Watanabe and H. I. Pass: VEGF and VEGF type C play an important role in angiogenesis and lymphangiogenesis in human malignant mesothelioma tumours. Br J Cancer, 81(1), 54-61 (1999) (Pubitemid 29415491)
64. Y. Yamada, J. Nezu, M. Shimane and Y. Hirata: Molecular cloning of a novel vascular endothelial growth factor, VEGF-D. Genomics, 42(3), 483-8 (1997) (Pubitemid 27287391)
65. M. G. Achen, M. Jeltsch, E. Kukk, T. Makinen, A. Vitali, A. Wilks, K. Alitalo and S. Stacker: Vascular endothelial growth factor-D (VEGF-D) is a ligand for tyrosine kinases VEGF receptor 2 (Flk1) and VEGF receptor 3 (Flk4). Proc Natl Acad Sci USA, 95, 548-553 (1998) (Pubitemid 28083780)
66. L. Marconcini, S. Marchio, L. Morbidelli, E. Cartocci, A. Albini, M. Ziche, F. Bussolino and S. Oliviero: c-fosinduced growth factor/vascular endothelial growth factor D induces angiogenesis in vivo and in vitro. Proc Natl Acad Sci U S A, 96(17), 9671-6 (1999) (Pubitemid 29398790)
67. D. Bellomo, J. P. Headrick, G. U. Silins, C. A. Paterson, P. S. Thomas, M. Gartside, A. Mould, M. M. Cahill, I. D. Tonks, S. M. Grimmond, S. Townson, C. Wells, M. Little, M. C. Cummings, N. K. Hayward and G. F. Kay: Mice lacking the vascular endothelial growth factor-B gene (Vegfb) have smaller hearts, dysfunctional coronary vasculature, and impaired recovery from cardiac ischemia. Circ Res, 86(2), E29-35 (2000)
68. Y. Akagi, W. Liu, K. Xie, B. Zebrowski, R. M. Shaheen and L. M. Ellis: Regulation of vascular endothelial growth factor expression in human colon cancer by interleukin-1beta. Br J Cancer, 80(10), 1506-11 (1999) (Pubitemid 29308627)
69. M. A. Al-Rawi, R. E. Mansel and W. G. Jiang: Interleukin-7 induced lymphangiogenesis is mediated by autocrine secretion of vascular endothelial growth factor-D (VEGF-D) in breast cancer. Breast Cancer Res Treat, 82 (Supp 1), S134 (2003)
70. P. Xia, L. P. Aiello, H. Ishii, Z. Y. Jiang, D. J. Park, G. S. Robinson, H. Takagi, W. P. Newsome, M. R. Jirousek and G. L. King: Characterization of vascular endothelial growth factor's effect on the activation of protein kinase C, its isoforms, and endothelial cell growth. J Clin Invest, 98(9), 2018-26 (1996) (Pubitemid 26376289)
71. H. P. Gerber, A. McMurtrey, J. Kowalski, M. Yan, B. A. Keyt, V. Dixit and N. Ferrara: Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem, 273(46), 30336-43 (1998) (Pubitemid 28545503)
72. B. J. Leak L: Ultrastructural studies on the lymphatic ancchoring filaments. Journal of Biological Biology, 36, 129-149 (1968)
73. R. R. Aukland K: Interstitial-lymphatic mechanisms in the control of extracellular fluid volume. physiol Rev, 73, 1-78 (1993)
74. J. P. Sleeman, J. Krishnan, V. Kirkin and P. Baumann: Markers for the lymphatic endothelium: In search of the holy grail? Microscopy Res Technique, 55(2), 61-69 (2001) (Pubitemid 32988907)
75. S. Breiteneder-Geleff, K. Matsui, A. Soleiman, P. Meraner, H. Poczewski, R. Kalt, G. Schaffner and D. Kerjaschki: Podoplanin, novel 43-kd membrane protein of glomerular epithelial cells, is down-regulated in puromycin nephrosis. Am J Pathol, 151(4), 1141-52 (1997) (Pubitemid 27424324)
76. K. Nose, H. Saito and T. Kuroki: Isolation of a gene sequence induced later by tumour-promoting 12-Otetradecanoylphorbol-13-acetate in mouse osteoblastic cells (MC3T3-E1) and expressed constitutively in rastransformed cells. Cell Growth Differ, 1, 511-518 (1990)
77. A. Wetterwald, W. Hoffstetter, M. Cecchini, B. Lanske, C. Wagner, H. Fleisch and M. Atkinson: Characterization and cloning of the E11 antigen, a marker expressed by rat osteoblasts and osteocytes. Bone, 18, 125-132 (1996) (Pubitemid 26092592)
78. A. Rishi, M. Joyce-Brady, J. Fisher, L. Dobbs, J. Floros, J. Vander Spek, J. Brody and M. Williams: Cloning, characterization, and development expression of a rat lung alveolar type I cell gene inembryonic endodermal and neural derivatives. Dev Biol, 167, 294-306 (1995)
79. K. Matsui, S. Breiteneder-Geleff, A. Soleiman, H. Kowalski and D. Kerjaschki: Podoplanin, a novel 43-kDa membrane protein, controls the shape of podocytes. Nephrology Dialysis Transplantation, 14, 9-11 (1999) (Pubitemid 29041825)
80. K. Matsui, S. Breiteneder-Geleff and D. Kerjaschki: Epitope-specific antibodies to the 43-kD glomerular membrane protein podoplanin cause proteinuria and rapid flattening of podocytes. J Am Soc Nephrol, 9, 2013-2026 (1998) (Pubitemid 28482149)
81. A. S. S Breiteneder-Geleff, H Kowalski, R Horvat, G Amman, E Kriehuber, K Diem, W weninger, E Tschachler E, Alitalo K, Kerjaschki D: Angiosarcomas express mixed endothelial phenotypes of blood and lymphatic capillaries: Podoplanin as a specific marker for lymphatic endothelium. American Journal of Pathology, 154, 385-394 (1999) (Pubitemid 29094089)
82. O. G. Wigle JT: Prox-1 function is required for the development of the murine lymphatic system. Cell, 98, 769-778 (1999)
83. S. I. Tomarev, O. Sundin, S. BanerjeeBasu, M. K. Duncan, J. M. Yang and J. Piatigorsky: Chicken homeobox gene Prox 1 related to Drosophila prospero is expressed in the developing lens and retina. Developmental Dynamics, 206(4), 354-367 (1996) (Pubitemid 26260170)
84. J. R. Fraser and T. C. Laurent: Turnover and metabolism of hyaluronan. Ciba Found Symp, 143, 41-53; discussion 53-9, 281-5 (1989)
85. J. R. Fraser, W. G. Kimpton, T. C. Laurent, R. N. Cahill and N. Vakakis: Uptake and degradation of hyaluronan in lymphatic tissue. Biochem J, 256(1), 153-8 (1988)
86. L. J. Picker, M. Nakache and E. C. Butcher: Monoclonal antibodies to human lymphocyte homing receptors define a novel class of adhesion molecules on diverse cell types. J Cell Biol, 109(2), 927-37 (1989) (Pubitemid 19197049)
87. N. J. Beasley, R. Prevo, S. Banerji, R. D. Leek, J. Moore, P. van Trappen, G. Cox, A. L. Harris and D. G. Jackson: Intratumoural lymphangiogenesis and lymph node metastasis in head and neck cancer. Cancer Res, 62(5), 1315-20 (2002) (Pubitemid 34407785)
88. M. M. Mattila, J. K. Ruohola, T. Karpanen, D. G. Jackson, K. Alitalo and P. L. Harkonen: VEGF-C induced lymphangiogenesis is associated with lymph node metastasis in orthotopic MCF-7 tumours. Int J Cancer, 98(6), 946-51 (2002) (Pubitemid 34286696)
89. B. Olofsson, M. Jeltsch, U. Eriksson and K. Alitalo: Current biology of VEGF-B and VEGF-C. Curr Opin Biotechnol, 10(6), 528-35 (1999)
90. T. Veikkola, M. Karkkainen, L. Claesson-Welsh and K. Alitalo: Regulation of angiogenesis via vascular endothelial growth factor receptors. Cancer Res, 60(2), 203-212 (2000) (Pubitemid 30070735)
91. U. Eriksson and K. Alitalo: Structure, expression and receptor-binding properties of novel vascular endothelial growth factors. Curr Top Microbiol Immunol, 237, 41-57 (1999) (Pubitemid 28554858)
92. R. Valtola, P. Salven, P. Heikkila, J. Taipale, H. Joensuu, M. Rehn, T. Pihlajaniemi, H. Weich, R. deWaal and K. Alitalo: VEGFR-3 and its ligand VEGF-C are associated with angiogenesis in breast cancer. Am J Pathology, 154(5), 1381-1390 (1999) (Pubitemid 29226433)
93. T. A. Partanen, J. Arola, A. Saaristo, L. Jussila, A. Ora, M. Miettinen, S. A. Stacker, M. G. Achen and K. Alitalo: VEGF-C and VEGF-D expression in neuroendocrine cells and their receptor, VEGFR-3, in fenestrated blood vessels in human tissues. Faseb J, 14(13), 2087-96 (2000)
94. R. E. Ferrell, K. L. Levinson, J. H. Esman, M. A. Kimak, E. C. Lawrence, M. M. Barmada and D. N. Finegold: Hereditary lymphedema: evidence for linkage and genetic heterogeneity. Hum Mol Genet, 7(13), 2073-8 (1998) (Pubitemid 28546416)
95. M. H. Witte, R. Erickson, M. Bernas, M. Andrade, F. Reiser, W. Conlon, H. E. Hoyme and C. L. Witte: Phenotypic and genotypic heterogeneity in familial Milroy lymphedema. Lymphology, 31(4), 145-55 (1998) (Pubitemid 29056708)
96. A. L. Evans, G. Brice, V. Sotirova, P. Mortimer, J. Beninson, K. Burnand, J. Rosbotham, A. Child and M. Sarfarazi: Mapping of primary congenital lymphedema to the 5q35.3 region. Am J Hum Genet, 64(2), 547-55 (1999) (Pubitemid 129500537)
97. D. Dumont, L. Jussila, J. Taipale, A. Lymboussaki, T. Mustonen, K. Pajusola, M. Breitman and K. Alitalo: Cardiovascular failure in mouse embryos deficient in VEGF receptor-3. Science, 282, 946-949 (1998) (Pubitemid 28507528)
98. K. Pajusola, O. Aprelikova, E. Armstrong, S. Morris and K. Alitalo: Two human FLT4 receptor tyrosine kinase isoforms with distinct carboxy terminal tails are produced by alternative processing of primary transcripts. Oncogene, 8(11), 2931-7 (1993) (Pubitemid 23312896)
99. F. Galland, A. Karamysheva, M. J. Pebusque, J. P. Borg, R. Rottapel, P. Dubreuil, O. Rosnet and D. Birnbaum: The FLT4 gene encodes a transmembrane tyrosine kinase related to the vascular endothelial growth factor receptor. Oncogene, 8(5), 1233-40 (1993) (Pubitemid 23129845)
100. E. Fournier, P. Dubreuil, D. Birnbaum and J. P. Borg: Mutation at tyrosine residue 1337 abrogates liganddependent transforming capacity of the FLT4 receptor. Oncogene, 11(5), 921-31 (1995)
101. K. Pajusola, O. Aprelikova, G. Pelicci, H. Weich, L. Claesson-Welsh and K. Alitalo: Signalling properties of FLT4, a proteolytically processed receptor tyrosine kinase related to two VEGF receptors. Oncogene, 9(12), 3545-55 (1994) (Pubitemid 24359392)
102. J. P. Borg, O. deLapeyriere, T. Noguchi, R. Rottapel, P. Dubreuil and D. Birnbaum: Biochemical characterization of two isoforms of FLT4, a VEGF receptor-related tyrosine kinase. Oncogene, 10(5), 973-84 (1995)
103. V. Joukov, V. Kumar, T. Sorsa, E. Arighi, H. Weich, O. Saksela and K. Alitalo: 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(12), 6599-602 (1998) (Pubitemid 28160314)
104. J. F. Wang, R. K. Ganju, Z. Y. Liu, H. Avraham, S. Avraham and J. E. Groopman: Signal transduction in human hematopoietic cells by vascular endothelial growth factor related protein, a novel ligand for the FLT4 receptor. Blood, 90(9), 3507-15 (1997) (Pubitemid 27473420)
105. E. Fournier, P. Blaikie, O. Rosnet, B. Margolis, D. Birnbaum and J. P. Borg: Role of tyrosine residues and protein interaction domains of SHC adaptor in VEGF receptor 3 signaling. Oncogene, 18(2), 507-14 (1999) (Pubitemid 29060626)
106. A. Lymboussaki, B. Olofsson, U. Eriksson and K. Alitalo: Vascular endothelial growth factor (VEGF) and VEGF-C show overlapping binding sites in embryonic endothelia and distinct sites in differentiated adult endothelia. Circulation Res, 85(11), 992-999 (1998)
107. V. R. Jussila L, Partanen TA, Salven P, Heikkila P, Matikainen, R. R. MT, Kaipainen A, Detmar M, Tschachler E, Alitalo R, and A. K: Lymphatic endothelium and Kaposi's sarcoma spindle cells detected by antibodies against the vascular endothelial growth factor receptor-3. Cancer Res, 58, 1599-1604 (1998) (Pubitemid 28215077)
108. K. Paavonen, P. Puolakkainen, L. Jussila, T. Jahkola and K. Alitalo: Vascular endothelial growth factor receptor-3 in lymphangiogenesis in wound healing. Am J Pathology, 156(5), 1499-1504 (2000) (Pubitemid 30646689)
109. A. J. Partanen TA, Saaristo A, Jussila L, Ora A, Miettinen M, Stacker SA, Achen MG, Alitalo K: VEGF-C and VEGF-D expression in neuroendocrine cells and their receptor, VEGFR-3, in fenestrated blood vessels in human tissues. FASEB J, 14, 2087-2096 (2000)
110. F. T. Kubo H, Jussila L, Hashi H, Ogawa M, Shimizu K, Awane M, Sakai Y, Takabayashi A, Alitalo K, Yamaoka Y, Nishikawa SI: Involvement of vascular endothelial growth factor receptor-3 in maintenance of integrity of endothelial cell lining during tumour angiogenesis.. Blood, 96, 546-553 (2000) (Pubitemid 30463374)
111. T. Partanen, K. Alitalo and M. Miettinen: Lack of lymphatic vascular specificity of vascular endothelial growth factor receptor 3 in 185 vascular tumours. Cancer Res, 86, 2406-2412 (1999) (Pubitemid 30010384)
112. H. Kubo, T. Fujiwara, L. Jussila, H. Hashi, M. Ogawa, K. Shimizu, M. Awane, Y. Sakai, A. Takabayashi, K. Alitalo, Y. Yamaoka and S. Nishikawa: Involvement of vascular endothelial growth factor receptor-3 in maintenance of integrity of endothelial cell lining during tumour angiogenesis.. Blood, 96, 546-553 (2000) (Pubitemid 30463374)
113. Y. Wang, M. Nakayama, M. E. Pitulescu, T. S. Schmidt, M. L. Bochenek, A. Sakakibara, S. Adams, A. Davy, U. Deutsch, U. Luthi, A. Barberis, L. E. Benjamin, T. Makinen, C. D. Nobes and R. H. Adams: Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature, 465(7297), 483-6
114. E. Weber, P. Lorenzoni, G. Lozzi and G. Sacchi: Cytochemical differentiation between blood and lymphatic endothelium: bovine blood and lymphatic large vessels and endothelial cells in culture. J Histochem Cytochem, 42, 1109-1115 (1994) (Pubitemid 24226338)
115. J. Werner, M. Schunke and B. Tillmann: Histochemical visualization of lymphatic capillaries in the rat: a comparison of methods demonstrated at the posterior pharyngeal surface. Arch Histol Jpn, 50, 505-514 (1987)
116. S. Kato, A. Yasunaga and U. Uchida: Enzymehistochemical method for identification of lymphatic capillaries . Lymphology, 24, 125-129 (1991)
117. H. Zoellner and N. Hunter: Histochemical identification of the vascular endothelial isoenzyme of alkaline phosphatase. J Histochem Cytochem, 37, 1893-1898 (1989) (Pubitemid 20002754)
118. J. Werner, M. Schunke and B. Tillmann: Histochemical visualization of lymphatic capillaries in the rat: a comparison of methodsdemonstrated at the posterior pharyngeal surface. Arch Histol Jpn, 50, 505-514 (1987)
119. S. Kato, A. Yasunaga and U. Uchida: Enzymehistochemical methodfor identification of lymphatic capillaries. Lymphology, 24, 125-129 (1991)
120. H. Erhard, F. Rietveldt, E. Brocker, R. de Waal and D. Ruiter: Phenotype of normal cutaneous microvasculature immunoelectron microscopic observations with emphasis on the differences between blood vessels and lymphatics. Journal of Investigative Dermatology, 106, 135-140 (1996) (Pubitemid 126444646)
121. B. Sauter, D. Foedinger, B. Sterniczky, K. Wolff and K. Rappersberger: Immuneelectron microscopic characterization of human lymphatic microvascular endothelial cells. Differential expression of CD31, CD34 and type VI collagene with lymphatic endothelial cells vs blood capillary endothelial cells in normal human skin, lymphangioma and haemangioma in-situ. J Histochem Cytochem, 46, 165-176 (1998) (Pubitemid 28087847)
122. R. Harrison, A. Ewert and D. Folse: Presence of Weible-Palade bodies in lymphatic endothelium of the cat. Lymphology, 19, 170-171 (1986)
123. S. Magari and Y. Ito: Weible-Palade bodies in endothelial cells of normal thoracic ducts and deep cervical lymphatics in rabbits. Lympholog, (21, 93-98 (1988)
124. C. Marchetti, P. Poggi, A. Calligaro and A. Casasco: Lymphatic vessels of the human dental pulp in different conditions. Anat Rec, 234, 27-33 (1992)
125. R. Nagle, M. Witte, A. Martinez, C. Witte, M. Hendrix, D. Way and K. Reed: Factor VIII-associated antigen in human lymphatic endothelium. Lymphology, 20, 20-24 (1987) (Pubitemid 17073798)
126. Y. Otsuki, H. Kubo and S. Magari: Immunohistochemical differentiation between lymphatic vessels and blood vessels-use of antibasement membrane antibodies and anti-factor VIII-related antigen. Arch Histol Cytol, 53, 95-105 (1990)
127. T. Ryan: Structure and function of lymphatics. J Invest Dermatol, 93, 18S-24S (1989)
128. M. Yoshizawa, S. Shingaki, T. Nakajima and T. Saku: Histopathological study of lymphatic invasion in squamous cell carcinoma (O-1N) with high potential of lymph node metastasis. Clin Exp Metastasis, 12, 347-356 (1994) (Pubitemid 24339064)
129. J. Madri, S. Sankar and A. Romanic: Angiogenesis. In: Clark RAF, editor. The molecular and cellular biology of wound repair, 2nd ed. New York: Plenum Press, 355-371 (1996)
130. S. Paku and N. Paweletz: First steps of tumour-related angiogenesis. Lab Invest, 65, 334-346 (1991)
131. K. Aukland and R. Reed: Interstitial-lymphatic mechanisms in the control of extracellular fluid volume. Physiol Rev, 73, 1-78 (1993) (Pubitemid 23065433)
132. L. Benjamin, I. Hemo and K. E.: A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF. Development, 125, 591-1598 (1998)
133. Y. Sawa, K. Shibata, M. Braithwaite, M. Suzuki and S. Yoshida: Expression of immunoglobulin superfamily members on the lymphatic endothelium of inflamed human small intestine. Microvasc Res, 57, 100-106 (1999b) (Pubitemid 29393287)
134. M. Schmelz, R. Moll, C. Kuhn and W. Franke: Complexus adhaerentes, a new group of desmoplakincontaining junctions in endothelialcells: II Different types of lymphatic vessels. Differentiation, 57, 97-117 (1994) (Pubitemid 24211106)
135. A. Kowalczyk, P. Navarro, E. Dejana, E. Bornslaeger, K. Green, D. Kopp and B. JE.: VE-cadherin and desmoplakin are assembled into dermal microvascular endothelial intercellularjunctions: a pivotal role for plakoglobin in the recruitment of desmoplakin to intercellular junctions. J Cell Sci, 111, 3045-3057 (1998) (Pubitemid 28517393)
136. O. Valiron, V. Chevrier, Y. Usson, F. Breviario, D. Job and E. Dejana: Desmoplakin expression and organization at human umbilical vein endothelial cell-tocell junctions. J Cell Sci, 109, 2141-2149 (1996) (Pubitemid 26265694)
137. A. Lymboussaki, B. Olofsson, U. Eriksson and K. Alitalo: Vascular endothelial growth factor (VEGF) and VEGF-C show overlapping binding sites in embryonic endothelia and distinct sites in differentiated adult endothelia. Circ Res, 85(11), 992-9 (1999)
138. D. Ruiter, R. Schlingemann, J. Westphal, M. Denijn, F. Rietveld and R. De Waal: Angiogenesis in wound healing and tumour metastasis. Behring Inst Mitt, 258-272 (1993)
139. R. Schlingemann, P. Hofman, L. Anderson, D. Troost and R. van der Gaag: Vascular expression of endothelial antigen PAL-E indicates absence of blood-ocular barriers in the normal eye. Ophthalmic Res, 29, 130-138 (1997) (Pubitemid 27270312)
140. T. Ezaki, K. Matsuno, H. Fuji, N. Hayashi, K. Miyakawa, J. Ohmori and M. Kotani: A new approach for identification of rat lymphatic capillaries using a monoclonal antibody. Arch Histol Cytol, 53, 77-86 (1990)
141. Y. Sawa, K. Shibata, M. Braithwaite, M. Suzuki and S. Yoshida: Expression of immunoglobulin superfamily members on the lymphatic endothelium of inflamed human small intestine. Microvasc Res, 57, 100-106 (1999) (Pubitemid 29393287)
142. G. Jurisic and M. Detmar: Lymphatic endothelium in health and disease. Cell Tissue Res, 335(1), 97-108 (2009)
143. H. Maby-El Hajjami and T. V. Petrova: Developmental and pathological lymphangiogenesis: from models to human disease. Histochem Cell Biol, 130(6), 1063-78 (2008)
144. G. Oliver and R. S. Srinivasan: Lymphatic vasculature development: current concepts. Ann N Y Acad Sci, 1131, 75-81 (2008) doi:1131/1/75 (Pubitemid 351758504)
145. J. Dixelius, T. Makinen, M. Wirzenius, M. J. Karkkainen, C. Wernstedt, K. Alitalo and L. Claesson-Welsh: 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(42), 40973-9 (2003) (Pubitemid 37280919)
146. A. Salameh, F. Galvagni, M. Bardelli, F. Bussolino and S. Oliviero: 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(10), 3423-31 (2005) (Pubitemid 41609177)
147. J. F. Wang, X. Zhang and J. E. Groopman: Activation of vascular endothelial growth factor receptor-3 and its downstream signaling promote cell survival under oxidative stres. J Biol Chem, 279(26), 27088-97 (2004) (Pubitemid 38812545)
148. N. E. Tobler and M. Detmar: Tumour and lymph node lymphangiogenesis- impact on cancer metastasis. J Leukoc Biol, 80(4), 691-6 (2006)
149. M. G. Achen, B. K. McColl and S. A. Stacker: Focus on lymphangiogenesis in tumour metastasis. Cancer Cell, 7(2), 121-7 (2005)
150. W. Thiele and J. P. Sleeman: Tumour-induced lymphangiogenesis: a target for cancer therapy? J Biotechnol, 124(1), 224-41 (2006) (Pubitemid 43816134)
151. C. S. Williams, R. D. Leek, A. M. Robson, S. Banerji, R. Prevo, A. L. Harris and D. G. Jackson: Absence of lymphangiogenesis and intratumoural lymph vessels in human metastatic breast cancer. J Pathol, 200(2), 195-206 (2003) (Pubitemid 36748028)
152. W. D. Witte MH, Witte CL, Bernas M: Lymphangiogenesis: mechanisms, significance and clinical implications. EXS, 79, 65-112 (1997)
153. T. Makinen, L. Jussila, T. Veikkola, T. Karpanen, M. I. Kettunen, K. J. Pulkkanen, R. Kauppinen, D. G. Jackson, H. Kubo, S. Nishikawa, S. Yla-Herttuala and K. Alitalo: Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3. Nat Med, 7(2), 199-205 (2001) (Pubitemid 32148487)
154. J. Kurebayashi, T. Otsuki, H. Kunisue, Y. Mikami, K. Tanaka, S. Yamamoto and H. Sonoo: Expression of vascular endothelial growth factor (VEGF) family members in breast cancer. Japanese Journal of Cancer Research, 90(9), 977-981 (1999) (Pubitemid 29500437)
155. J. Krishnan, V. Kirkin, A. Steffen, M. Hegen, D. Weih, S. Tomarev, J. Wilting and J. P. Sleeman: Differential in vivo and in vitro expression of vascular endothelial growth factor (VEGF)-C and VEGF-D in tumours and its relationship to lymphatic metastasis in immunocompetent rats. Cancer Res, 63(3), 713-22 (2003) (Pubitemid 36158152)
156. Z. Von Marschall, A. Scholz, S. A. Stacker, M. G. Achen, D. G. Jackson, F. Alves, M. Schirner, M. Haberey, K. H. Thierauch, B. Wiedenmann and S. Rosewicz: Vascular endothelial growth factor-D induces lymphangiogenesis and lymphatic metastasis in models of ductal pancreatic cancer. Int J Oncol, 27(3), 669-79 (2005)
157. K. Cui, W. Zhao, C. Wang, A. Wang, B. Zhang, W. Zhou, J. Yu, Z. Sun and S. Li: The CXCR4-CXCL12 Pathway Facilitates the Progression of Pancreatic Cancer Via Induction of Angiogenesis and Lymphangiogenesis. J Surg Res 2010 in press
158. M. I. Auvinen, E. I. Sihvo, T. Ruohtula, J. T. Salminen, A. Koivistoinen, P. Siivola, R. Ronnholm, J. O. Ramo, M. Bergman and J. A. Salo: Incipient angiogenesis in Barrett's epithelium and lymphangiogenesis in Barrett's adenocarcinoma. J Clin Oncol, 20(13), 2971-9 (2002) (Pubitemid 34728892)
159. Y. Kitadai, T. Amioka, K. Haruma, S. Tanaka, M. Yoshihara, K. Sumii, N. Matsutani, W. Yasui and K. Chayama: Clinicopathological significance of vascular endothelial growth factor (VEGF)-C in human esophageal squamous cell carcinomas. Int J Cancer, 93(5), 662-6 (2001) (Pubitemid 32695113)
160. T. Noguchi, S. Takeno, T. Shibata, Y. Uchida, S. Yokoyama and W. Muller: VEGF-C expression correlates with histological differentiation and metastasis in squamous cell carcinoma of the esophagus. Oncol Rep, 9(5), 995-9 (2002)
161. T. Amioka, Y. Kitadai, S. Tanaka, K. Haruma, M. Yoshihara, W. Yasui and K. Chayama: Vascular endothelial growth factor-C expression predicts lymph node metastasis of human gastric carcinomas invading the submucosa. Eur J Cancer, 38(10), 1413-9 (2002) (Pubitemid 34686854)
162. T. Ichikura, S. Tomimatsu, E. Ohkura and H. Mochizuki: Prognostic significance of the expression of vascular endothelial growth factor (VEGF) and VEGF-C in gastric carcinoma. J Surg Oncol, 78(2), 132-7 (2001)
163. A. Kabashima, Y. Maehara, Y. Kakeji and K. Sugimachi: Overexpression of vascular endothelial growth factor C is related to lymphogenous metastasis in early gastric carcinoma. Oncology, 60(2), 146-50 (2001) (Pubitemid 32245333)
164. A. Takahashi, K. Kono, J. Itakura, H. Amemiya, R. Feng Tang, H. Iizuka, H. Fujii and Y. Matsumoto: Correlation of vascular endothelial growth factor-C expression with tumourinfiltrating dendritic cells in gastric cancer. Oncology, 62(2), 121-7 (2002) (Pubitemid 34253081)
165. Y. Yonemura, S. Fushida, E. Bando, K. Kinoshita, K. Miwa, Y. Endo, K. Sugiyama, T. Partanen, H. Yamamoto and T. Sasaki: Lymphangiogenesis and the vascular endothelial growth factor receptor (VEGFR)-3 in gastric cancer. Eur J Cancer, 37(7), 918-923 (2001) (Pubitemid 32323971)
166. S. Juttner, C. Wissmann, T. Jons, M. Vieth, J. Hertel, S. Gretschel, P. M. Schlag, W. Kemmner and M. Hocker: Vascular endothelial growth factor-D and its receptor VEGFR-3: two novel independent prognostic markers in gastric adenocarcinoma. J Clin Oncol, 24(2), 228-40 (2006) (Pubitemid 46622052)
167. A. Furudoi, S. Tanaka, K. Haruma, Y. Kitadai, M. Yoshihara, K. Chayama and F. Shimamoto: Clinical significance of vascular endothelial growth factor C expression and angiogenesis at the deepest invasive site of advanced colorectal carcinoma. Oncology, 62(2), 157-66 (2002) (Pubitemid 34253086)
168. C. Parr and W. G. Jiang: Quantitative analysis of lymphangiogenic markers in human colorectal cancer. Int J Oncol, 23(2), 533-9 (2003)
169. M. L. George, M. G. Tutton, F. Janssen, A. Arnaout, A. M. Abulafi, S. A. Eccles and R. I. Swift: VEGF-A, VEGF-C, and VEGF-D in colorectal cancer progression. Neoplasia, 3(5), 420-7 (2001) (Pubitemid 32988812)
170. J. D. White, P. W. Hewett, D. Kosuge, T. McCulloch, B. C. Enholm, J. Carmichael and J. C. Murray: Vascular endothelial growth factor-D expression is an independent prognostic marker for survival in colorectal carcinoma. Cancer Res, 62(6), 1669-75 (2002) (Pubitemid 34408487)
171. T. Tsurusaki, S. Kanda, H. Sakai, H. Kanetake, Y. Saito, K. Alitalo and T. Koji: Vascular endothelial growth factor-C expression in human prostatic carcinoma and its relationship to lymph node metastasis. Br J Cancer, 80(1-2), 309-13 (1999) (Pubitemid 29210123)
172. S. S. Dadras, T. Paul, J. Bertoncini, L. F. Brown, A. Muzikansky, D. G. Jackson, U. Ellwanger, C. Garbe, M. C. Mihm and M. Detmar: Tumour lymphangiogenesis: a novel prognostic indicator for cutaneous melanoma metastasis and survival. Am J Pathol, 162(6), 1951-60 (2003) (Pubitemid 36613052)
173. J. Lin, A. S. Lalani, T. C. Harding, M. Gonzalez, W. W. Wu, B. Luan, G. H. Tu, K. Koprivnikar, M. J. VanRoey, Y. He, K. Alitalo and K. Jooss: Inhibition of lymphogenous metastasis using adeno-associated virusmediated gene transfer of a soluble VEGFR-3 decoy receptor. Cancer Res, 65(15), 6901-9 (2005) (Pubitemid 41060729)
174. T. Niki, S. Iba, M. Tokunou, T. Yamada, Y. Matsuno and S. Hirohashi: Expression of vascular endothelial growth factors A, B, C, and D and their relationships to lymph node status in lung adenocarcinoma. Clin Cancer Res, 6(6), 2431-9 (2000) (Pubitemid 30399212)
175. Z. Chen, M. L. Varney, M. W. Backora, K. Cowan, J. C. Solheim, J. E. Talmadge and R. K. Singh: Downregulation of vascular endothelial cell growth factor-C expression using small interfering RNA vectors in mammary tumours inhibits tumour lymphangiogenesis and spontaneous metastasis and enhances survival. Cancer Res, 65(19), 9004-11 (2005) (Pubitemid 41377392)
176. S. M. Maula, M. Luukkaa, R. Grenman, D. Jackson, S. Jalkanen and R. Ristamaki: Intratumoural lymphatics are essential for the metastatic spread and prognosis in squamous cell carcinomas of the head and neck region. Cancer Res, 63(8), 1920-6 (2003) (Pubitemid 36460859)
177. Y. He, K. Kozaki, T. Karpanen, K. Koshikawa, S. Yla-Herttuala, T. Takahashi and K. Alitalo: Suppression of tumour lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling. J Natl Cancer Inst, 94(11), 819-25 (2002) (Pubitemid 34705053)
178. B. Pytowski, J. Goldman, K. Persaud, Y. Wu, L. Witte, D. J. Hicklin, M. Skobe, K. C. Boardman and M. A. Swartz: Complete and specific inhibition of adult lymphatic regeneration by a novel VEGFR-3 neutralizing antibody. J Natl Cancer Inst, 97(1), 14-21 (2005)
179. T. Makinen, L. Jussila, T. Veikkola, T. Karpanen, M. I. Kettunen, K. J. Pulkkanen, R. Kauppinen, D. G. Jackson, H. Kubo, S. I. Nishikawa, S. Yla-Herttuala and K. Alitalo: Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3. Nature Med, 7(2), 199-205 (2001) (Pubitemid 32148487)
180. T. Karpanen and K. Alitalo: Lymphatic vessels as targets of tumour therapy? J Exp Med, 194(6), F37-F42 (2001) (Pubitemid 32983007)
181. N. Honda, M. Jinnin, I. Kajihara, T. Makino, S. Fukushima and H. Ihn: Impaired lymphangiogenesis due to excess VEGF-D/Flt-4 signaling in the skin of patients with systemic sclerosis. Br J Dermatol 2010 in press
182. B. Regenfuss, J. Onderka, F. Bock, D. Hos, K. Maruyama and C. Cursiefen: Genetic Heterogeneity of Lymphangiogenesis in Different Mouse Strains. Am J Pathol 2010 in press
183. B. Garmy-Susini, C. J. Avraamides, M. C. Schmid, P. Foubert, L. G. Ellies, L. Barnes, C. Feral, T. Papayannopoulou, A. Lowy, S. L. Blair, D. Cheresh, M. Ginsberg and J. A. Varner: Integrin alpha4beta1 signaling is required for lymphangiogenesis and tumour metastasis. Cancer Res, 70(8), 3042-51 (2000)
184. X. M. Yang, H. X. Han, F. Sui, Y. M. Dai, M. Chen and J. G. Geng: Slit-Robo signaling mediates lymphangiogenesis and promotes tumour lymphatic metastasis. Biochem Biophys Res Commun, 396(2), 571-7, (2010) d
185. F. Larrieu-Lahargue, A. L. Welm, K. R. Thomas and D. Y. Li: Netrin-4 induces lymphangiogenesis in vivo. Blood 2010, in press