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Molecular/Cancer Biology Laboratory, Haartman Institute and Ludwig Institute for Cancer Research, FIN-00014 University of Helsinki, Finland [T. K., M. J. K., H. K., K. A.]; Apoptosis Laboratory, Danish Cancer Society, DK-2100 Copenhagen, Denmark [M. E., M. J.]; and A. I. Virtanen Institute, University of Kuopio, FIN-70211 Kuopio, Finland [S. Y-H.]
Many solid tumors produce vascular endothelial growth factor C (VEGF-C), and its receptor, VEGFR-3, is expressed in tumor blood vessels. To study the role of VEGF-C in tumorigenesis, we implanted MCF-7 human breast carcinoma cells overexpressing recombinant VEGF-C orthotopically into severe combined immunodeficient mice. VEGF-C increased tumor growth, but unlike VEGF, it had little effect on tumor angiogenesis. Instead, VEGF-C strongly promoted the growth of tumor-associated lymphatic vessels, which in the tumor periphery were commonly infiltrated with the tumor cells. These effects of VEGF-C were inhibited by a soluble VEGFR-3 fusion protein. Our data suggest that VEGF-C facilitates tumor metastasis via the lymphatic vessels and that tumor spread can be inhibited by blocking the interaction between VEGF-C and its receptor.
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D Massi, S Puig, A Franchi, J Malvehy, S Vidal-Sicart, M Gonzalez-Cao, G Baroni, S Ketabchi, J Palou, and M Santucci Tumour lymphangiogenesis is a possible predictor of sentinel lymph node status in cutaneous melanoma: a case-control study J. Clin. Pathol., February 1, 2006; 59(2): 166 - 173. [Abstract] [Full Text] [PDF] |
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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., January 10, 2006; 24(2): 228 - 240. [Abstract] [Full Text] [PDF] |
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Y Nakamura, H Yasuoka, M Tsujimoto, K Kurozumi, M Nakahara, K Nakao, and K Kakudo Importance of lymph vessels in gastric cancer: a prognostic indicator in general and a predictor for lymph node metastasis in early stage cancer J. Clin. Pathol., January 1, 2006; 59(1): 77 - 82. [Abstract] [Full Text] [PDF] |
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Z. Gombos, X. Xu, C. S. Chu, P. J. Zhang, and G. Acs Peritumoral Lymphatic Vessel Density and Vascular Endothelial Growth Factor C Expression in Early-Stage Squamous Cell Carcinoma of the Uterine Cervix Clin. Cancer Res., December 1, 2005; 11(23): 8364 - 8371. [Abstract] [Full Text] [PDF] |
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X.-M. Yu, C.-Y. Lo, W.-F. Chan, K.-Y. Lam, P. Leung, and J. M. Luk Increased Expression of Vascular Endothelial Growth Factor C in Papillary Thyroid Carcinoma Correlates with Cervical Lymph Node Metastases Clin. Cancer Res., November 15, 2005; 11(22): 8063 - 8069. [Abstract] [Full Text] [PDF] |
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S. Y. Wong, H. Haack, D. Crowley, M. Barry, R. T. Bronson, and R. O. Hynes Tumor-Secreted Vascular Endothelial Growth Factor-C Is Necessary for Prostate Cancer Lymphangiogenesis, but Lymphangiogenesis Is Unnecessary for Lymph Node Metastasis Cancer Res., November 1, 2005; 65(21): 9789 - 9798. [Abstract] [Full Text] [PDF] |
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F. Renyi-Vamos, J. Tovari, J. Fillinger, J. Timar, S. Paku, I. Kenessey, G. Ostoros, L. Agocs, I. Soltesz, and B. Dome Lymphangiogenesis Correlates with Lymph Node Metastasis, Prognosis, and Angiogenic Phenotype in Human Non-Small Cell Lung Cancer Clin. Cancer Res., October 15, 2005; 11(20): 7344 - 7353. [Abstract] [Full Text] [PDF] |
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M. S. Ostenfeld, N. Fehrenbacher, M. Hoyer-Hansen, C. Thomsen, T. Farkas, and M. Jaattela Effective Tumor Cell Death by {sigma}-2 Receptor Ligand Siramesine Involves Lysosomal Leakage and Oxidative Stress Cancer Res., October 1, 2005; 65(19): 8975 - 8983. [Abstract] [Full Text] [PDF] |
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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, et al. Inhibition of Lymphogenous Metastasis Using Adeno-Associated Virus-Mediated Gene Transfer of a Soluble VEGFR-3 Decoy Receptor Cancer Res., August 1, 2005; 65(15): 6901 - 6909. [Abstract] [Full Text] [PDF] |
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G. Breier Lymphangiogenesis in Regenerating Tissue: Is VEGF-C Sufficient? Circ. Res., June 10, 2005; 96(11): 1132 - 1134. [Full Text] [PDF] |
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Y. He, I. Rajantie, K. Pajusola, M. Jeltsch, T. Holopainen, S. Yla-Herttuala, T. Harding, K. Jooss, T. Takahashi, and K. Alitalo Vascular Endothelial Cell Growth Factor Receptor 3-Mediated Activation of Lymphatic Endothelium Is Crucial for Tumor Cell Entry and Spread via Lymphatic Vessels Cancer Res., June 1, 2005; 65(11): 4739 - 4746. [Abstract] [Full Text] [PDF] |
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S. Hirakawa, S. Kodama, R. Kunstfeld, K. Kajiya, L. F. Brown, and M. Detmar VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis J. Exp. Med., April 4, 2005; 201(7): 1089 - 1099. [Abstract] [Full Text] [PDF] |
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T. Tammela, C. Heckman, and K. Alitalo Lymphangiogenesis and Metastasis Am. Assoc. Cancer Res. Educ. Book, April 1, 2005; 2005(1): 67 - 73. [Full Text] [PDF] |
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M. E. Baldwin, M. M. Halford, S. Roufail, R. A. Williams, M. L. Hibbs, D. Grail, H. Kubo, S. A. Stacker, and M. G. Achen Vascular Endothelial Growth Factor D Is Dispensable for Development of the Lymphatic System Mol. Cell. Biol., March 15, 2005; 25(6): 2441 - 2449. [Abstract] [Full Text] [PDF] |
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X. Jimenez, D. Lu, L. Brennan, K. Persaud, M. Liu, H. Miao, L. Witte, and Z. Zhu A recombinant, fully human, bispecific antibody neutralizes the biological activities mediated by both vascular endothelial growth factor receptors 2 and 3 Mol. Cancer Ther., March 1, 2005; 4(3): 427 - 434. [Abstract] [Full Text] [PDF] |
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V. Schacht, S. S. Dadras, L. A. Johnson, D. G. Jackson, Y.-K. Hong, and M. Detmar Up-Regulation of the Lymphatic Marker Podoplanin, a Mucin-Type Transmembrane Glycoprotein, in Human Squamous Cell Carcinomas and Germ Cell Tumors Am. J. Pathol., March 1, 2005; 166(3): 913 - 921. [Abstract] [Full Text] [PDF] |
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T. Tammela, B. Enholm, K. Alitalo, and K. Paavonen The biology of vascular endothelial growth factors Cardiovasc Res, February 15, 2005; 65(3): 550 - 563. [Abstract] [Full Text] [PDF] |
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M I Koukourakis, A Giatromanolaki, E Sivridis, C Simopoulos, K C Gatter, A L Harris, and D G Jackson LYVE-1 immunohistochemical assessment of lymphangiogenesis in endometrial and lung cancer J. Clin. Pathol., February 1, 2005; 58(2): 202 - 206. [Abstract] [Full Text] [PDF] |
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V. Kaushal, P. Mukunyadzi, R. A. Dennis, E. R. Siegel, D. E. Johnson, and M. Kohli Stage-Specific Characterization of the Vascular Endothelial Growth Factor Axis in Prostate Cancer: Expression of Lymphangiogenic Markers Is Associated with Advanced-Stage Disease Clin. Cancer Res., January 15, 2005; 11(2): 584 - 593. [Abstract] [Full Text] [PDF] |
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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, January 5, 2005; 97(1): 14 - 21. [Abstract] [Full Text] [PDF] |
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K. Alitalo, S. Mohla, and E. Ruoslahti Lymphangiogenesis and Cancer: Meeting Report Cancer Res., December 15, 2004; 64(24): 9225 - 9229. [Full Text] [PDF] |
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H. Kurahara, S. Takao, K. Maemura, H. Shinchi, S. Natsugoe, and T. Aikou Impact of Vascular Endothelial Growth Factor-C and -D Expression in Human Pancreatic Cancer: Its Relationship to Lymph Node Metastasis Clin. Cancer Res., December 15, 2004; 10(24): 8413 - 8420. [Abstract] [Full Text] [PDF] |
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I. Crnic, K. Strittmatter, U. Cavallaro, L. Kopfstein, L. Jussila, K. Alitalo, and G. Christofori Loss of Neural Cell Adhesion Molecule Induces Tumor Metastasis by Up-regulating Lymphangiogenesis Cancer Res., December 1, 2004; 64(23): 8630 - 8638. [Abstract] [Full Text] [PDF] |
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A. Hoeben, B. Landuyt, M. S. Highley, H. Wildiers, A. T. Van Oosterom, and E. A. De Bruijn Vascular Endothelial Growth Factor and Angiogenesis Pharmacol. Rev., December 1, 2004; 56(4): 549 - 580. [Abstract] [Full Text] [PDF] |
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P. Bono, V.-M. Wasenius, P. Heikkila, J. Lundin, D. G. Jackson, and H. Joensuu High LYVE-1-Positive Lymphatic Vessel Numbers Are Associated with Poor Outcome in Breast Cancer Clin. Cancer Res., November 1, 2004; 10(21): 7144 - 7149. [Abstract] [Full Text] [PDF] |
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Y. Nakamura, H. Yasuoka, M. Tsujimoto, Q. Yang, S. Imabun, M. Nakahara, K. Nakao, M. Nakamura, I. Mori, and K. Kakudo Flt-4-Positive Vessel Density Correlates with Vascular Endothelial Growth Factor-D Expression, Nodal Status, and Prognosis in Breast Cancer Clin. Cancer Res., November 1, 2003; 9(14): 5313 - 5317. [Abstract] [Full Text] [PDF] |
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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., October 17, 2003; 278(42): 40973 - 40979. [Abstract] [Full Text] [PDF] |
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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 Tumor Lymphangiogenesis: A Novel Prognostic Indicator for Cutaneous Melanoma Metastasis and Survival Am. J. Pathol., June 1, 2003; 162(6): 1951 - 1960. [Abstract] [Full Text] [PDF] |
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E. D. Emberley, Y. Niu, E. Leygue, L. Tomes, R. D. Gietz, L. C. Murphy, and P. H. Watson Psoriasin Interacts with Jab1 and Influences Breast Cancer Progression Cancer Res., April 15, 2003; 63(8): 1954 - 1961. [Abstract] [Full Text] [PDF] |
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Y. Tang, D. Zhang, L. Fallavollita, and P. Brodt Vascular Endothelial Growth Factor C Expression and Lymph Node Metastasis Are Regulated by the Type I Insulin-like Growth Factor Receptor Cancer Res., March 15, 2003; 63(6): 1166 - 1171. [Abstract] [Full Text] [PDF] |
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L. Yuan, D. Moyon, L. Pardanaud, C. Breant, M. J. Karkkainen, K. Alitalo, and A. Eichmann Abnormal lymphatic vessel development in neuropilin 2 mutant mice Development, March 12, 2003; 129(20): 4797 - 4806. [Abstract] [Full Text] [PDF] |
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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 Tumors and Its Relationship to Lymphatic Metastasis in Immunocompetent Rats Cancer Res., February 1, 2003; 63(3): 713 - 722. [Abstract] [Full Text] [PDF] |
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S. Hirakawa, Y.-K. Hong, N. Harvey, V. Schacht, K. Matsuda, T. Libermann, and M. Detmar Identification of Vascular Lineage-Specific Genes by Transcriptional Profiling of Isolated Blood Vascular and Lymphatic Endothelial Cells Am. J. Pathol., February 1, 2003; 162(2): 575 - 586. [Abstract] [Full Text] [PDF] |
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O. Straume, D. G. Jackson, and L. A. Akslen Independent Prognostic Impact of Lymphatic Vessel Density and Presence of Low-Grade Lymphangiogenesis in Cutaneous Melanoma Clin. Cancer Res., January 1, 2003; 9(1): 250 - 256. [Abstract] [Full Text] [PDF] |
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P. Salven, S. Mustjoki, R. Alitalo, K. Alitalo, and S. Rafii VEGFR-3 and CD133 identify a population of CD34+ lymphatic/vascular endothelial precursor cells Blood, January 1, 2003; 101(1): 168 - 172. [Abstract] [Full Text] [PDF] |
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A. Saaristo, T. Veikkola, T. Tammela, B. Enholm, M. J. Karkkainen, K. Pajusola, H. Bueler, S. Yla-Herttuala, and K. Alitalo Lymphangiogenic Gene Therapy With Minimal Blood Vascular Side Effects J. Exp. Med., September 16, 2002; 196(6): 719 - 730. [Abstract] [Full Text] [PDF] |
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S. F. Schoppmann, P. Birner, J. Stockl, R. Kalt, R. Ullrich, C. Caucig, E. Kriehuber, K. Nagy, K. Alitalo, and D. Kerjaschki Tumor-Associated Macrophages Express Lymphatic Endothelial Growth Factors and Are Related to Peritumoral Lymphangiogenesis Am. J. Pathol., September 1, 2002; 161(3): 947 - 956. [Abstract] [Full Text] [PDF] |
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S. A. STACKER, M. E. BALDWIN, and M. G. ACHEN The role of tumor lymphangiogenesis in metastatic spread FASEB J, July 1, 2002; 16(9): 922 - 934. [Abstract] [Full Text] [PDF] |
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L. Jussila and K. Alitalo Vascular Growth Factors and Lymphangiogenesis Physiol Rev, July 1, 2002; 82(3): 673 - 700. [Abstract] [Full Text] [PDF] |
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H. Kubo, R. Cao, E. Brakenhielm, T. Makinen, Y. Cao, and K. Alitalo Blockade of vascular endothelial growth factor receptor-3 signaling inhibits fibroblast growth factor-2-induced lymphangiogenesis in mouse cornea PNAS, June 25, 2002; 99(13): 8868 - 8873. [Abstract] [Full Text] [PDF] |
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T. P. Padera, A. Kadambi, E. di Tomaso, C. M. Carreira, E. B. Brown, Y. Boucher, N. C. Choi, D. Mathisen, J. Wain, E. J. Mark, et al. Lymphatic Metastasis in the Absence of Functional Intratumor Lymphatics Science, June 7, 2002; 296(5574): 1883 - 1886. [Abstract] [Full Text] [PDF] |
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Y. He, K.-i. Kozaki, T. Karpanen, K. Koshikawa, S. Yla-Herttuala, T. Takahashi, and K. Alitalo Suppression of Tumor Lymphangiogenesis and Lymph Node Metastasis by Blocking Vascular Endothelial Growth Factor Receptor 3 Signaling J Natl Cancer Inst, June 5, 2002; 94(11): 819 - 825. [Abstract] [Full Text] [PDF] |
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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., April 1, 2002; 16(7): 773 - 783. [Full Text] [PDF] |
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R. K. Jain and B. T. Fenton Intratumoral Lymphatic Vessels: A Case of Mistaken Identity or Malfunction? J Natl Cancer Inst, March 20, 2002; 94(6): 417 - 421. [Full Text] [PDF] |
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O. Straume and L. A. Akslen Importance of Vascular Phenotype by Basic Fibroblast Growth Factor, and Influence of the Angiogenic Factors Basic Fibroblast Growth Factor/Fibroblast Growth Factor Receptor-1 and Ephrin-A1/EphA2 on Melanoma Progression Am. J. Pathol., March 1, 2002; 160(3): 1009 - 1019. [Abstract] [Full Text] [PDF] |
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T. MAKINEN and K. ALITALO Molecular Mechanisms of Lymphangiogenesis Cold Spring Harb Symp Quant Biol, January 1, 2002; 67(0): 189 - 196. [Abstract] [PDF] |
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J. F. Wang, X.-F. Zhang, and J. E. Groopman Stimulation of beta 1 Integrin Induces Tyrosine Phosphorylation of Vascular Endothelial Growth Factor Receptor-3 and Modulates Cell Migration J. Biol. Chem., November 2, 2001; 276(45): 41950 - 41957. [Abstract] [Full Text] [PDF] |
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T. Karpanen and K. Alitalo Lymphatic Vessels as Targets of Tumor Therapy? J. Exp. Med., September 17, 2001; 194(6): f37 - f42. [Full Text] [PDF] |
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M. Skobe, L. M. Hamberg, T. Hawighorst, M. Schirner, G. L. Wolf, K. Alitalo, and M. Detmar Concurrent Induction of Lymphangiogenesis, Angiogenesis, and Macrophage Recruitment by Vascular Endothelial Growth Factor-C in Melanoma Am. J. Pathol., September 1, 2001; 159(3): 893 - 903. [Abstract] [Full Text] [PDF] |
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