Tumour expression of lymphangiogenic growth factors but not lymphatic vessel density is implicated in human cervical cancer progression

References

• Alitalo K, Tammela T, Petrova TV. Lymphangiogenesis in development and human disease. Nature 2005; 438; 946–53.
   PubMed Web of Science ®Google Scholar
• Sleeman J, Schmid A, Thiele W. Tumour lymphatics. Semin Cancer Biol 2009; 5: 285–97.
   Google Scholar
• Karkkainen MJ, Petrova TV. Vascular endothelial growth factor receptors in the regulation of angiogenesis and lymphangiogenesis. Oncogene 2000; 19: 5598–605.
   PubMed Web of Science ®Google Scholar
• Skobe M, Hawighorst T, Jackson DG, et al Induction of tumour lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat Med 2001; 2: 192–8.
   Google Scholar
• Stacker SA, Caesar C, Baldwin ME, et al VEGF-D promotes the metastatic spread of tumour cells via the lymphatics. Nat Med 2001; 2: 186–91.
   Google Scholar
• Thiele W, Sleeman JP. Tumour-induced lymphangiogenesis: a target for cancer therapy? J Biotechnol 2006; 124: 224–41.
   PubMed Web of Science ®Google Scholar
• Eccles S, Paon L, Sleeman J. Lymphatic metastasis in breast cancer: importance and new insights into cellular and molecular mechanisms. Clin Exp Metastasis 2007; 24: 619–36.
   PubMedGoogle Scholar
• Breiteneder-Geleff S, Soleiman A, Kowalski H, et al Angiosarcomas express mixed endothelial phenotypes of blood and lymphatic capillaries: podoplanin as a specific marker for lymphatic endothelium. Am J Pathol 1999; 2: 385–94.
   Google Scholar
• Banerji S, Ni J, Wang SX, et al LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J Cell Biol 1999; 144: 789–801.
   PubMed Web of Science ®Google Scholar
• Tammela T, Saaristo A, Holopainen T, et al Therapeutic differentiation and maturation of lymphatic vessels after lymph node dissection and transplantation. Nat Med 2007; 12: 1458–66.
   Google Scholar
• Oliver G, Detmar M. The rediscovery of the lymphatic system: old and new insights into the development and biological function of the lymphatic vasculature. Genes Dev 2002; 16: 773–83.
   PubMed Web of Science ®Google Scholar
• Wigle JT, Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell 1999; 98: 769–78.
   PubMed Web of Science ®Google Scholar
• Sleeman JP, Thiele W. Tumour metastasis and the lymphatic vasculature. Int J Cancer 2009; 125: 2747–56.
   PubMedGoogle Scholar
• Baluk P, McDonald DM. Markers for microscopic imaging of lymphangiogenesis and angiogenesis. Ann N Y Acad Sci 2008; 1131: 1–12.
   PubMed Web of Science ®Google Scholar
• Waggoner SE. Cervical cancer. Lancet 2003; 361: 2217–25.
   PubMed Web of Science ®Google Scholar
• Gombos Z, Xu X, Chu CS, Zhang PJ, Acs G. Peritumoural lymphatic vessel density and vascular endothelial growth factor C expression in early-stage squamous cell carcinoma of the uterine cervix. Clin Cancer Res 2005; 11: 8364–71.
   PubMed Web of Science ®Google Scholar
• Zhang SQ, Yu H, Zhang LL. Clinical implications of increased lymph vessel density in the lymphatic metastasis of early-stage cervical cancer: a clinical immunohistochemical method study. BMC Cancer 2009; 9: 64.
   PubMedGoogle Scholar
• Van Trappen PO, Steele D, Lowe DG, et al Expression of vascular endothelial growth factor (VEGF)-C and VEGF-D, and their receptor VEGFR-3, during different stages of cervical carcinogenesis. J Pathol 2003; 201: 544–54.
   PubMed Web of Science ®Google Scholar
• Longatto-Filho A, Pinheiro C, Pereira SM, et al Lymphatic vessel density and epithelial D2-40 immunoreactivity in pre-invasive and invasive lesions of the uterine cervix. Gynecol Oncol 2007; 107: 45–51.
   PubMedGoogle Scholar
• Wulfing P, Kersting C, Buerger H, et al Expression patterns of angiogenic and lymphangiogenic factors in ductal breast carcinoma in situ. Br J Cancer 2005; 92: 1720–8.
   PubMed Web of Science ®Google Scholar
• Nakamura Y, Yasuoka H, Tsujimoto M, et al Clinicopathological significance of vascular endothelial growth factor-C in breast carcinoma with long-term follow-up. Mod Pathol 2003; 16: 309–14.
   PubMed Web of Science ®Google Scholar
• Su JL, Yang PC, Shih JY, et al The VEGF-C/Flt-4 axis promotes invasion and metastasis of cancer cells. Cancer Cell 2006; 9: 209–23.
   PubMed Web of Science ®Google Scholar
• Petrova TV, Bono P, Holnthoner W, et al VEGFR-3 expression is restricted to blood and lymphatic vessels in solid tumours. Cancer Cell 2008; 13: 554–6.
   PubMed Web of Science ®Google Scholar
• Yokoyama Y, Charnock-Jones DS, Licence D, et al Vascular endothelial growth factor-D is an independent prognostic factor in epithelial ovarian carcinoma. Br J Cancer 2003; 88: 237–44.
   PubMed Web of Science ®Google Scholar
• Yokoyama Y, Charnock-Jones DS, Licence D, et al Expression of vascular endothelial growth factor (VEGF)-D and its receptor, VEGF receptor 3, as a prognostic factor in endometrial carcinoma. Clin Cancer Res 2003; 9: 1361–9.
   PubMed Web of Science ®Google Scholar
• Yu H, Zhang S, Zhang R, Zhang L. The role of VEGF-C/D and Flt-4 in the lymphatic metastasis of early-stage invasive cervical carcinoma. J Exp Clin Cancer Res 2009; 28: 98.
   PubMedGoogle Scholar
• Jach R, Dulinska-Litewka J, Laidler P, et al Expression of VEGF, VEGF-C and VEGFR-2 in in situ and invasive SCC of cervix. Front Biosci (Elite Ed) 2010; 2: 411–23.
   PubMedGoogle Scholar
• Niki T, Iba S, Tokunou M, Yamada T, Matsuno Y, Hirohashi S. Expression of vascular endothelial growth factors A, B, C, and D and their relationships to lymph node status in lung adenocarcinoma. Clin Cancer Res 2000; 6: 2431–9.
   PubMed Web of Science ®Google Scholar
• Maekawa S, Iwasaki A, Shirakusa T, Enatsu S, Kawakami T, Kuroki M. Correlation between lymph node metastasis and the expression of VEGF-C, VEGF-D and VEGFR-3 in T1 lung adenocarcinoma. Anticancer Res 2007; 2: 3735–41.
   Google Scholar
• Laakkonen P, Waltari M, Holopainen T, et al Vascular endothelial growth factor receptor 3 is involved in tumour angiogenesis and growth. Cancer Res 2007; 67: 593–9.
   PubMed Web of Science ®Google Scholar
• Ji RC. Lymphatic endothelial cells, tumour lymphangiogenesis and metastasis: New insights into intratumoural and peritumoural lymphatics. Cancer Metastasis Rev 2006; 25: 677–94.
   PubMedGoogle Scholar
• Leu AJ, Berk DA, Lymboussaki A, Alitalo K, Jain RK. Absence of functional lymphatics within a murine sarcoma: a molecular and functional evaluation. Cancer Res 2000; 60: 4324–7.
   PubMed Web of Science ®Google Scholar
• Padera TP, Kadambi A, di Tomaso E, et al Lymphatic metastasis in the absence of functional intratumour lymphatics. Science 2002; 296: 1883–6.
   PubMed Web of Science ®Google Scholar
• Williams CS, Leek RD, Robson AM, et al Absence of lymphangiogenesis and intratumoural lymph vessels in human metastatic breast cancer. J Pathol 2003; 200: 195–206.
   PubMed Web of Science ®Google Scholar
• Weiss L. Metastasis of cancer: a conceptual history from antiquity to the 1990s. Cancer Metastasis Rev 2000; 19: I-XI, 193–383.
   Google Scholar
• Harrell MI, Iritani BM, Ruddell A. Tumour-induced sentinel lymph node lymphangiogenesis and increased lymph flow precede melanoma metastasis. Am J Pathol 2007; 170: 774–86.
   PubMed Web of Science ®Google Scholar
• Hirakawa S, Brown LF, Kodama S, Paavonen K, Alitalo K, Detmar M. VEGF-C-induced lymphangiogenesis in sentinel lymph nodes promotes tumour metastasis to distant sites. Blood 2007; 109: 1010–7.
   PubMed Web of Science ®Google Scholar
• Schacht V, Dadras SS, Johnson LA, Jackson DG, Hong YK, Detmar M. Up-regulation of the lymphatic marker podoplanin, a mucin-type transmembrane glycoprotein, in human squamous cell carcinomas and germ cell tumours. Am J Pathol 2005; 166: 913–21.
   PubMed Web of Science ®Google Scholar
• Botting SK, Fouad H, Elwell K, et al Prognostic significance of peritumoral lymphatic vessel density and vascular endothelial growth factor receptor 3 in invasive squamous cell cervical cancer. Transl Oncol 2010; 3: 170–5.
   PubMedGoogle Scholar
• Oliver G, Srinivasan RS. Endothelial cell plasticity: how to become and remain a lymphatic endothelial cell. Development 2010; 137: 363–72.
   Google Scholar
• Shimoda M, Takahashi M, Yoshimoto T, Kono T, Ikai I, Kubo H. A homeobox protein, prox1, is involved in the differentiation, proliferation, and prognosis in hepatocellular carcinoma. Clin Cancer Res 2006; 12: 6005–11.
   PubMed Web of Science ®Google Scholar
• Laerm A, Helmbold P, Goldberg M, Dammann R, Holzhausen HJ, Ballhausen WG. Prospero-related homeobox 1 (PROX1) is frequently inactivated by genomic deletions and epigenetic silencing in carcinomas of the bilary system. J Hepatol 2007; 46: 89–97.
   Google Scholar
• Yoshimoto T, Takahashi M, Nagayama S, et al RNA mutations of prox1 detected in human esophageal cancer cells by the shifted termination assay. Biochem Biophys Res Commun 2007; 359: 258–62.
   PubMedGoogle Scholar
• Petrova TV, Nykanen A, Norrmen C, et al Transcription factor PROX1 induces colon cancer progression by promoting the transition from benign to highly dysplastic phenotype. Cancer Cell 2008; 13: 407–19.
   PubMedGoogle Scholar
• Schoppmann SF, Schindl M, Breiteneder-Geleff S, et al Inflammatory stromal reaction correlates with lymphatic microvessel density in early-stage cervival cancer. Anticancer Res 2001; 21: 3419–23.
   PubMedGoogle Scholar
• Schoppmann SF, Birner P, Stockl J, et al Tumour-associated macrophages express lymphatic endothelial growth factors and are related to peritumoural lymphangiogenesis. Am J Pathol 2002; 161: 947–56.
   PubMed Web of Science ®Google Scholar
• Groger M, Loewe R, Holnthoner W, et al IL-3 induces expression of lymphatic markers Prox-1 and podoplanin in human endothelial cells. J Immunol 2004; 173: 7161–9.
   PubMedGoogle Scholar
• Maruyama K, Asai J, Ii M, Thorne T, Losordo DW, D'Amore PA. Decreased macrophage number and activation lead to reduced lymphatic vessel formation and contribute to impaired diabetic wound healing. Am J Pathol 2007; 170: 1178–91.
   PubMed Web of Science ®Google Scholar
• Clarijs R, Schalkwijk L, Ruiter DJ, de Waal RM. Lack of lymphangiogenesis despite coexpression of VEGF-C and its receptor Flt-4 in uveal melanoma. Invest Ophthalmol Vis Sci 2001; 42: 1422–8.
   PubMed Web of Science ®Google Scholar
• Issa A, Le TX, Shoushtari AN, Shields JD, Swartz MA. Vascular endothelial growth factor-C and C-C chemokine receptor 7 in tumour cell-lymphatic cross-talk promote invasive phenotype. Cancer Res 2009: 69: 349–57.
   PubMedGoogle Scholar
• Shields JD, Emmett MS, Dunn DB, et al Chemokine-mediated migration of melanoma cells towards lymphatics—a mechanism contributing to metastasis. Oncogene 2007; 26: 2997–3005.
   PubMedGoogle Scholar
• Cao Y, Linden P, Farnebo J, et al Vascular endothelial growth factor C induces angiogenesis in vivo. Proc Natl Acad Sci USA 1998; 95: 14389–94.
   PubMed Web of Science ®Google Scholar