Signaling for lymphangiogenesis via VEGFR-3 is required for the early events of metastasis

Clinical and Experimental Metastasis

Volumn 30, Issue 6, 2013, Pages 819-832

  Matsumoto, Masataka ^a,e   Roufail, Sally ^a,d   Inder, Rachael ^a   Caesar, Carol ^a,d   Karnezis, Tara ^a,d   Shayan, Ramin ^a,b,d   Farnsworth, Rae H ^a,b,d   Sato, Teruhiko ^a,f   Achen, Marc G ^a,b,d   Mann, G Bruce ^b,c   Stacker, Steven A ^a,b,d  

^a ROYAL MELBOURNE HOSPITAL   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c ROYAL WOMEN'S HOSPITAL   (Australia)

^d PETER MACCALLUM CANCER CENTRE   (Australia)

^e KAGOSHIMA UNIVERSITY   (Japan)

^f JUNTENDO UNIVERSITY   (Japan)

Author keywords

Angiogenesis; Breast cancer; Lymph nodes; Lymphatic vessels

Indexed keywords

MF 4 31C 1; MF4 31C1; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY DC101; UNCLASSIFIED DRUG; VASCULOTROPIN D; VASCULOTROPIN RECEPTOR 3;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CONTROLLED STUDY; DRUG TARGETING; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; LYMPH NODE METASTASIS; LYMPH VESSEL; LYMPHANGIOGENESIS; MOUSE; NONHUMAN; PRIMARY TUMOR; TUMOR GROWTH; TUMOR MODEL; TUMOR VOLUME; TUMOR XENOGRAFT;

ANIMALS; CELL LINE, TUMOR; FEMALE; HUMANS; LYMPHANGIOGENESIS; LYMPHATIC METASTASIS; LYMPHATIC VESSELS; MICE; MICE, SCID; NEOVASCULARIZATION, PHYSIOLOGIC; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR D; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3;

EID: 84887079128     PISSN: 02620898     EISSN: 15737276     Source Type: Journal    
DOI: 10.1007/s10585-013-9581-x     Document Type: Article

References (53)

1. Fidler IJ (2003) The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat Rev Cancer 3:453-458
2. Campbell PJ, Yachida S, Mudie LJ et al (2010) The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature 467:1109-1113
3. Ferrara N (2002) VEGF and the quest for tumour angiogenesis factors. Nat Rev Cancer 2:795-803
4. Ferrara N, Hillan KJ, Gerber HP et al (2004) Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat Rev Drug Discov 3:391-400
5. Witte L, Hicklin DJ, Zhu Z et al (1998) Monoclonal antibodies targeting the VEGF receptor-2 (Flk1/KDR) as an anti-angiogenic therapeutic strategy. Cancer Metastasis Rev 17:155-161
6. Hurwitz H, Fehrenbacher L, Novotny W et al (2004) Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. New Engl J Med 350:2335-2342
7. Hurwitz HI, Fehrenbacher L, Hainsworth JD et al (2005) Bevacizumab in combination with fluorouracil and leucovorin: an active regimen for first-line metastatic colorectal cancer. J Clin Oncol 23:3502-3508
8. Allegra CJ, Yothers G, O'Connell MJ et al (2011) Phase III trial assessing bevacizumab in stages II and III carcinoma of the colon: results of NSABP protocol C-08. J Clin Oncol 29:11-16
9. Joukov V, Pajusola K, Kaipainen A et al (1996) 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
10. Achen MG, Jeltsch M, Kukk E et al (1998) Vascular endothelial growth factor D (VEGF-D) is a ligand for the tyrosine kinases VEGF receptor 2 (Flk1) and VEGF receptor 3 (Flt4). Proc Natl Acad Sci USA 95:548-553
11. Achen MG, Stacker SA (2012) Vascular endothelial growth factor-D: signalling mechanisms, biology and clinical relevance. Growth Factors 5:283-296
12. Banerji S, Ni J, Wang S-X et al (1999) LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J Cell Biol 144:789-801
13. Breiteneder-Geleff S, Soleiman A, Kowalski H et al (1999) Angiosarcomas express mixed endothelial phenotypes of blood and lymphatic capillaries. Podoplanin as a specific marker for lymphatic endothelium. Am J pathol 154:385-394
14. Mandriota SJ, Jussila L, Jeltsch M et al (2001) Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis. EMBO J 20:672-682
15. Skobe M, Hamberg LM, Hawighorst T et al (2001) Concurrent induction of lymphangiogenesis, angiogenesis, and macrophage recruitment by vascular endothelial growth factor-C in melanoma. Am J Pathol 159:893-903
16. Shayan R, Inder R, Karnezis T et al (2013) Tumor location and nature of lymphatic vessels are key determinants of cancer metastasis. Clin Exp Metastasis 30:345-356
17. Karnezis T, Shayan R, Caesar C et al (2012) VEGF-D promotes tumor metastasis by regulating prostaglandins produced by the collecting lymphatic endothelium. Cancer Cell 21:181-195
18. Stacker SA, Caesar C, Baldwin ME et al (2001) VEGF-D promotes the metastatic spread of tumor cells via the lymphatics. Nat Med 7:186-191
19. Shayan R, Achen MG, Stacker SA (2006) Lymphatic vessels in cancer metastasis: bridging the gaps. Carcinogenesis 27:1729-1738
20. Skobe M, Hawighorst T, Jackson DG et al (2001) Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat Med 7:192-198
21. Kopfstein L, Veikkola T, Djonov VG et al (2007) Distinct roles of vascular endothelial growth factor-D in lymphangiogenesis and metastasis. Am J Pathol 170:1348-1361
22. Farnsworth RH, Karnezis T, Shayan R et al (2011) A role for bone morphogenic protein-4 in vascular endothelial growth factor-D mediated tumor growth, metastasis and vessel remodelling. Cancer Res 71:6547-6557
23. Achen MG, Roufail S, Domagala T et al (2000) Monoclonal antibodies to vascular endothelial growth factor-D block its interactions with both VEGF receptor-2 and VEGF receptor-3. Eur J Biochem 267:2505-2515
24. Stacker SA, Williams RA, Achen MG (2004) Lymphangiogenic growth factors as markers of tumor metastasis. APMIS 112:539-549
25. Kitadai Y, Kodama M, Cho S et al (2005) Quantitative analysis of lymphangiogenic markers for predicting metastasis of human gastric carcinoma to lymph nodes. Int J Cancer 115:388-392
26. White JD, Hewett PW, Kosuge D et al (2002) Vascular endothelial growth factor-D expression is an independent prognostic marker for survival in colorectal carcinoma. Cancer Res 62:1669-1675
27. Renyi-Vamos F, Tovari J, Fillinger J et al (2005) Lymphangiogenesis correlates with lymph node metastasis, prognosis, and angiogenic phenotype in human non-small cell lung cancer. Clin Cancer Res 11:7344-7353
28. Schoppmann SF, Bayer G, Aumayr K et al (2004) Prognostic value of lymphangiogenesis and lymphovascular invasion in invasive breast cancer. Ann Surg 240:306-312
29. Rubbia-Brandt L, Terris B, Giostra E et al (2004) Lymphatic vessel density and vascular endothelial growth factor-C expression correlate with malignant behavior in human pancreatic endocrine tumors. Clin Cancer Res 10:6919-6928
30. Sipos B, Klapper W, Kruse ML et al (2004) Expression of lymphangiogenic factors and evidence of intratumoral lymphangiogenesis in pancreatic endocrine tumors. Am J Pathol 165:1187-1197
31. Yokoyama Y, Charnock-Jones DS, Licence D et al (2003) Expression of vascular endothelial growth factor (VEGF)-D and its receptor, VEGF receptor 3, as a prognostic factor in endometrial carcinoma. Clin Cancer Res 9:1361-1369
32. Yokoyama Y, Charnock-Jones DS, Licence D et al (2003) Vascular endothelial growth factor-D is an independent prognostic factor in epithelial ovarian carcinoma. Br J Cancer 88:237-244
33. Achen MG, McColl BK, Stacker SA (2005) Focus on lymphangiogenesis in tumor metastasis. Cancer Cell 7:121-127
34. Debinski W, Slagle-Webb B, Achen MG et al (2001) VEGF-D is an X-linked/AP-1 regulated putative onco-angiogen in human glioblastoma multiforme. Mol Med 7:598-608
35. Stacker SA, Stenvers K, Caesar C et al (1999) Biosynthesis of vascular endothelial growth factor-D involves proteolytic processing which generates non-covalent homodimers. J Biol Chem 274:32127-32136
36. Pytowski B, Goldman J, Persaud K et al (2005) Complete and specific inhibition of adult lymphatic regeneration by a novel VEGFR-3 neutralizing antibody. J Natl Cancer Inst 97:14-21
37. Shayan R, Karnezis T, Tsantikos E et al (2007) A system for quantifying the patterning of the lymphatic vasculature. Growth Factors 25:417-425
38. Roberts N, Kloos B, Cassella M et al (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 66:2650-2657
39. He Y, Kozaki K, Karpanen T et al (2002) Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling. J Natl Cancer Inst 94:819-825
40. He Y, Rajantie I, Pajusola K et al (2005) 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 65:4739-4746
41. Burton JB, Priceman SJ, Sung JL et al (2008) Suppression of prostate cancer nodal and systemic metastasis by blockade of the lymphangiogenic axis. Cancer Res 68:7828-7837
42. Achen MG, Mann GB, Stacker SA (2006) Targeting lymphangiogenesis to prevent tumour metastasis. Br J Cancer 94:1355-1360
43. Nilsson I, Bahram F, Li X et al (2010) VEGF receptor 2/-3 heterodimers detected in situ by proximity ligation on angiogenic sprouts. EMBO J 29:1377-1388
44. Tammela T, Zarkada G, Wallgard E et al (2008) Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation. Nature 454:656-660
45. Laakkonen P, Waltari M, Holopainen T et al (2007) Vascular endothelial growth factor receptor 3 is involved in tumor angiogenesis and growth. Cancer Res 67:593-599
46. Akahane M, Akahane T, Shah A et al (2005) A potential role for vascular endothelial growth factor-D as an autocrine growth factor for human breast carcinoma cells. Anticancer Res 25:701-707
47. Ebos JM, Lee CR, Cruz-Munoz W et al (2009) Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 15:232-239
48. Paez-Ribes M, Allen E, Hudock J et al (2009) Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 15:220-231
49. Singh M, Couto SS, Forrest WF et al (2012) Anti-VEGF antibody therapy does not promote metastasis in genetically engineered mouse tumour models. J Pathol 227:417-430
50. Chung AS, Kowanetz M, Wu X et al (2012) Differential drug class-specific metastatic effects following treatment with a panel of angiogenesis inhibitors. J Pathol 227:404-416
51. Stacker SA, Achen MG (2013) Where to now with the VEGF signalling pathway in cancer? Chin J Cancer. doi: 10.5732/cjc.012.10319
52. Achen MG, Stacker SA (2008) Molecular control of lymphatic metastasis. Ann NY Acad Sci 1131:225-234
53. Chu KU, Turner RR, Hansen NM et al (1999) Do all patients with sentinel node metastasis from breast carcinoma need complete axillary node dissection? Ann Surg 229:536-541