Increased vascular endothelial growth factor-C expression is insufficient to induce lymphatic metastasis in human soft-tissue sarcomas

Clinical Cancer Research

Volumn 15, Issue 8, 2009, Pages 2637-2646

  Lahat, Guy ^a   Lazar, Alexander ^a   Wang, Xuemei ^a   Wang, Wei Lien ^a   Zhu, Quan Sheng ^a   Hunt, Kelly K ^a   Pollock, Raphael E ^a   Lev, Dina ^a  

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; VASCULOTROPIN A; VASCULOTROPIN C;

ARTICLE; BREAST CANCER; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPH NODE METASTASIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOFT TISSUE SARCOMA;

ANTIGENS, CD31; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; ENDOTHELIAL CELLS; GENE KNOCKDOWN TECHNIQUES; HUMANS; LYMPHATIC METASTASIS; LYMPHATIC VESSEL TUMORS; RNA, SMALL INTERFERING; SARCOMA; VASCULAR ENDOTHELIAL GROWTH FACTOR C;

EID: 65249117712     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-08-2442     Document Type: Article

References (50)

1. Achen MG, Stacker SA. Molecular control of lymphatic metastasis. Ann N YAcad Sci 2008;1131: 225-34.
2. Gershenwald JE, Fidler I J. Cancer. Targeting lymphatic metastasis. Science 2002;296:1811 -2.
3. Padera TP, Kadambi A, di Tomaso E, et al. Lymphatic metastasis in the absence of functional intratumor lymphatics. Science 2002;296:1883-6.
4. Nakamura Y, Yasuoka H,Tsujimoto M, et al. Lymph vessel density correlates with nodal status, VEGF-C expression, and prognosis in breast cancer. Breast Cancer Res Treat 2005;91:125-32.
5. Roma AA, Magi-Galluzzi C, Kral MA, Jin TT, Klein EA, Zhou M. Peritumoral lymphatic invasion is associated with regional lymph node metastases in prostate adenocarcinoma. Mod Pathol 2006;19:392 -8.
6. Beasley NJ, Prevo R, Banerji S, et al. Intratumoral lymphangiogenesis and lymph node metastasis in head and neck cancer. Cancer Res 2002;62: 1315-20.
7. Achen MG, McColl BK, Stacker SA. Focus on lymphangiogenesis in tumor metastasis. Cancer Cell 2005;7:121 -7.
8. Stacker SA, Achen MG, Jussila L, Baldwin ME, Alitalo K. Lymphangiogenesis and cancer metastasis. Nature Rev 2002;2:573-83.
9. Dadras SS, Paul T, Bertoncini J, et al. Tumor lymphan- giogenesis: a novel prognosticindicator forcutaneous melanoma metastasis and survival. Am JPathol 2003; 162:1951 -60.
10. CaoY. Opinion: emerging mechanisms of tumour lymphangiogenesis and lymphatic metastasis. Nature Rev 2005;5:735-43.
11. Joukov V, Pajusola K, Kaipainen A, et al. 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 1996;15:1751.
12. Karpanen T, Heckman CA, Keskitalo S, et al. Functional interaction ofVEGF-C and VEGF-D with neuro- pilin receptors. FASEB J 2006;20:1462 -72.
13. Karkkainen MJ, Haiko P, Sainio K, et al. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat Immunol 2004;5:74-80.
14. Akagi K, Ikeda Y, Miyazaki M, et al. Vascular endothelial growth factor-C (VEGF-C) expression in human colorectal cancer tissues. Br J Cancer 2000; 83:887-91.
15. Su JL, Yang PC, Shih JY, et al.TheVEGF-C/Flt-4 axis promotes invasion and metastasis of cancer cells. Cancer Cell 2006;9:209-23.
16. Cunnick GH, Jiang WG, Douglas-Jones T, et al. Lym- phangiogenesis and lymph node metastasis in breast cancer. Mol Cancer 2008;7:23.
17. Kuroda K, Horiguchi A, AsanoT, AsanoT, Hayakawa M. Prediction of lymphatic invasion by peritumoral lymphatic vessel density in prostate biopsy cores. Prostate 2008;68:1057 -63.
18. Niakosari F, Kahn HJ, McCready D, et al. Lymphatic invasion identified by monoclonal antibody D2-40, younger age, and ulceration: predictors of sentinel lymph node involvement in primary cutaneous mela- noma.ArchDermatol2008;144:462- 7.
19. Lahat G, LazarA, Lev D. Sarcoma epidemiologyand etiology: potential environmental and genetic factors. Surg Clin North Am 2008;88:451 -81, v.
20. Fong Y, Coit DG, Woodruff JM, Brennan MF. Lymph node metastasis from soft tissue sarcoma in adults. Analysis of data from a prospective database of1772 sarcoma patients. Ann Surg1993;217:72 -7.
21. Behranwala KA, A'Hern R, Omar AM,Thomas JM. Prognosis of lymph node metastasis in soft tissue sarcoma. Ann Surg Oncol 2004;11:714-9.
22. Jin Z, Lahat G, Korchin B, et al. Midkine enhances soft-tissue sarcoma growth: a possible novel therapeutic target. Clin Cancer Res 2008;14:5033 -42.
23. 2 receptors in migration of murine and human breast cancer cells. Exp Cell Res 2003;289:265 -74.
24. 1 integrins. FASEB J 2004;18:1111 -3.
25. Bjorndahl MA, Cao R, Burton JB, et al. Vascular endothelial growth factor-a promotes peritumoral lymphangiogenesis and lymphatic metastasis. Cancer Res 2005;65:9261 -8.
26. Pakos EE, Goussia AC, Tsekeris PG, Papachristou DJ, Stefanou D, Agnantis NJ. Expression of vascular endothelial growth factor and its receptor, KDR/Flk-1, in soft tissue sarcomas. Anticancer Res 2005;25: 3591 -6.
27. Du Bois S, Demetri G. Markers of angiogenesis and clinical features in patients with sarcoma. Cancer 2007;109:813 -9.
28. Dias S, Choy M, Alitalo K, Rafii S.Vascularendothelial growth factor (VEGF)-C signaling through FLT-4 (VEGFR-3) mediates leukemic cell proliferation, survival, and resistance to chemotherapy. Blood 2002; 99:2179 -84.
29. Paget S. The distribution of secondary growths in cancer of the breast. Cancer Metastasis Rev 1989;8: 98-101.
30. Veronesi G, Landoni C, Pelosi G, et al. Fluoro- deoxy-glucose uptake and angiogenesis are independent biological features in lung metastases. Br J Cancer 2002;86:1391 -5.
31. Friedrichs N, Hahne JC, Pepper MS, et al. Immuno- histochemical quantification oflymph vessels,VEGF-C andVEGF receptor 3 in human sarcomas. Histopathol- ogy 2006;49:87 -8.
32. Maula SM, Luukkaa M, Grenman R, Jackson D, Jalkanen S, Ristamaki R. Intratumoral lymphatics are essential for the metastatic spread and prognosis in squamous cell carcinomas of the head and neck region. Cancer Res 2003;63:1920-6.
33. Gombos Z, Xu X, Chu CS, Zhang PJ, Acs G. Peritumoral 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.
34. Kadota K, Huang CL, Liu D, et al. The clinical significance of lymphangiogenesis and angiogenesis in non-small cell lung cancer patients. Eur J Cancer 2008;44:1057-67.
35. Von Marschall Z, Scholz A, Stacker SA, et al. Vascular endothelial growth factor-D induces lympha- ngiogenesis and lymphatic metastasis in models of ductal pancreatic cancer. Int J Oncol 2005;27: 669-79.
36. Franchi A, Gallo O, Massi D, Baroni G, Santucci M. Tumor lymphangiogenesis in head and neck squa- mous cell carcinoma: a morphometric study with clinical correlations. Cancer 2004;101:973 -8.
37. Massi D, Puig S, Franchi A, et al. Tumour lymphan- giogenesis is a possible predictor of sentinel lymph node status in cutaneous melanoma: a case-control study. J Clin Pathol 2006;59:166-73.
38. Renyi-Vamos F, Tovari J, Fillinger J, et al. Lymphan- giogenesis correlates with lymph node metastasis, prognosis, and angiogenic phenotype in human non- small cell lung cancer. Clin Cancer Res 2005;11: 7344-53.
39. Cheng L, Jones TD, Lin H, et al. Lymphovascularin- vasion is an independent prognosticfactor in prostatic adenocarcinoma. J Urol 2005;174:2181 -5.
40. Katz A, Smith BL, Golshan M, et al. Nomogramfor the prediction of having four or more involved nodes for sentinel lymph node-positive breast cancer. J Clin Oncol 2008;26:2093-8.
41. CaoY, Linden P, FarneboJ, et al.Vascular endothelial growth factor C induces angiogenesis in vivo. Proc Natl Acad Sci U S A1998;95:14389 -94.
42. Shibuya M, Claesson-Welsh L. Signal transduction by VEGF receptors in regulation of angiogenesis and lymphangiogenesis. Exp Cell Res 2006;312:549 -60.
43. Mandriota SJ, Jussila L, Jeltsch M, et al. Vascular endothelial growth factor-C-mediated lymphangio- genesis promotes tumour metastasis. EMBO J 2001; 20:672 -82.
44. Karpanen T, Egeblad M, Karkkainen MJ, et al. Vascular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth. Cancer Res 2001;61:1786 -90.
45. Wong SY, Haack H, Crowley D, Barry M, Bronson RT, Hynes RO. Tumor-secreted vascular endothelial growth factor-C is necessary for prostate cancer lym- phangiogenesis, but lymphangiogenesis is unnecessary for lymph node metastasis. Cancer Res 2005; 65:9789 -98.
46. Hoshida T, Isaka N, Hagendoorn J, et al. Imaging steps oflymphatic metastasisreveals that vascularen- dothelial growth factor-C increases metastasis by increasing delivery of cancer cells to lymph nodes: therapeutic implications. Cancer Res 2006;66: 8065-75.
47. Baird K, Davis S, Antonescu CR, et al. Gene expression profiling of human sarcomas: insights into sarcoma biology. Cancer Res 2005;65:9226 -35.
48. Hirakawa S, Kodama S, Kunstfeld R, Kajiya K, Brown LF, Detmar M.VEGF-Ainduces tumorand sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis. J Exp Med 2005;201: 1089-99.
49. Mburu YK,Wang J, Wood MA, Walker WH, Ferris RL. CCR7 mediates inflammation-associated tumor progression. Immunol Res 2006;36:61 -72.
50. Shields JD, Emmett MS, Dunn DB, et al. Chemo- kine-mediated migration of melanoma cells towards lymphatics-a mechanism contributing to metastasis. Oncogene2007;26:2997-3005.