Tumor location and nature of lymphatic vessels are key determinants of cancer metastasis

Clinical and Experimental Metastasis

Volumn 30, Issue 3, 2013, Pages 345-356

  Shayan, Ramin ^a,b,c   Inder, Rachael ^a   Karnezis, Tara ^a,b,c   Caesar, Carol ^a,b,c   Paavonen, Karri ^a   Ashton, Mark W ^b   Mann, G Bruce ^b   Taylor, G Ian ^b   Achen, Marc G ^a,b,c   Stacker, Steven A ^a,b,c  

^a ROYAL MELBOURNE HOSPITAL   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c PETER MACCALLUM CANCER CENTRE   (Australia)

Author keywords

Lymph node; Lymphatics; Metastasis; Prognosis; VEGF D

Indexed keywords

VASCULOTROPIN D;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER LOCALIZATION; FEMALE; HUMAN; HUMAN TISSUE; LYMPH NODE METASTASIS; LYMPH VESSEL; LYMPHANGIOGENESIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SKIN METASTASIS; ENZYME LINKED IMMUNOSORBENT ASSAY; METASTASIS; PATHOLOGY; WESTERN BLOTTING;

BLOTTING, WESTERN; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; LYMPHATIC VESSELS; NEOPLASM METASTASIS;

MLCS; MLOWN;

EID: 84875784137     PISSN: 02620898     EISSN: 15737276     Source Type: Journal    
DOI: 10.1007/s10585-012-9541-x     Document Type: Article

References (50)

1. Markovic SN, Erickson LA, Rao RD et al (2007) Malignant melanoma in the 21st century, part 2: staging, prognosis, and treatment. Mayo Clin Proc 82:490-513
2. DeVita VT, Hellman S, Rosenberg A (2001) Cancer, principles and practice of oncology, 6th edn. Lippincott, Williams and Wilkins, Philadelphia, PA
3. Mandriota SJ, Jussila L, Jeltsch M et al (2001) Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis. EMBO J 20:672-682
4. 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
5. 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
6. Nagy JA, Vasile E, Feng D et al (2002) Vascular permeability factor/vascular endothelial growth factor induces lymphangiogenesis as well as angiogenesis. J Exp Med 196:1497-1506
7. Schietroma C, Cianfarani F, Lacal PM et al (2003) Vascular endothelial growth factor-C expression correlates with lymph node localization of human melanoma metastases. Cancer 98:789-797
8. 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
9. Stacker SA, Williams RA, Achen MG (2004) Lymphangiogenic growth factors as markers of tumor metastasis. APMIS 112:539-549
10. Caunt M, Mak J, Liang WC et al (2008) Blocking neuropilin-2 function inhibits tumor cell metastasis. Cancer Cell 13:331-342
11. Achen MG, Mann GB, Stacker SA (2006) Targeting lymphangiogenesis to prevent tumour metastasis. Br J Cancer 94:1355-1360
12. Achen MG, McColl BK, Stacker SA (2005) Focus on lymphangiogenesis in tumor metastasis. Cancer Cell 7:121-127
13. Shayan R, Achen MG, Stacker SA (2006) Lymphatic vessels in cancer metastasis: bridging the gaps. Carcinogenesis 27:1729-1738
14. Goydos JS, Gorski DH (2003) Vascular endothelial growth factor C mRNA expression correlates with stage of progression in patients with melanoma. Clin Cancer Res 9:5962-5967
15. Nakamura Y, Yasuoka H, Tsujimoto M et al (2005) Lymph vessel density correlates with nodal status, VEGF-C expression, and prognosis in breast cancer. Breast Cancer Res Treat 91:125-132
16. Shayan R, Karnezis T, Murali R et al (2012) Variations in tumor lymphatic density in primary cutaneous melanomas predicts risk of lymph node metastasis. Histopathology. doi: 10.1111/j.1365-2559.2012.04310.x.
17. Stacker SA, Achen MG, Jussila L et al (2002) Lymphangiogenesis and cancer metastasis. Nat Rev Cancer 2:573-583
18. Alitalo K, Tammela T, Petrova TV (2005) Lymphangiogenesis in development and human disease. Nature (Lond) 438:946-953
19. Achen MG, Stacker SA (2008) Molecular control of lymphatic metastasis. Ann NY Acad Sci 1131:225-234
20. 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
21. Cunningham JE, Juri AL, Oman L et al (2006) Is risk of axillary lymph node metastasis associated with proximity of breast cancer to the skin? Breast Cancer Res Treat 100:319-328
22. Onogawa S, Kitadai Y, Tanaka S et al (2004) Expression of VEGF-C and VEGF-D at the invasive edge correlates with lymph node metastasis and prognosis of patients with colorectal carcinoma. Cancer Sci 95:32-39
23. Bevacqua SJ, Welch DR, Diez de Pinos SM et al (1990) Quantitation of human melanoma, carcinoma and sarcoma tumor cell adhesion to lymphatic endothelium. Lymphology 23:4-14
24. Padera TP, Kadambi A, di Tomaso E et al (2002) Lymphatic metastasis in the absence of functional intratumor lymphatics. Science 296:1883-1886
25. Smith KJ, Jones PF, Burke DA et al (2011) Lymphatic vessel distribution in the mucosa and submucosa and potential implications for T1 colorectal tumors. Dis Colon Rectum 54:35-40
26. Scavelli C, Weber E, Agliano M et al (2004) Lymphatics at the crossroads of angiogenesis and lymphangiogenesis. J Anat 204:433-449
27. Van der Auwera I, Cao Y, Tille JC et al (2006) First international consensus on the methodology of lymphangiogenesis quantification in solid human tumours. Br J Cancer 95:1611-1625
28. Pepper MS, Skobe M (2003) Lymphatic endothelium: morphological, molecular and functional properties. J Cell Biol 163:209-213
29. Makinen T, Adams RH, Bailey J et al (2005) PDZ interaction site in ephrinB2 is required for the remodeling of lymphatic vasculature. Genes Dev 19:397-410
30. Baldwin ME, Stacker SA, Achen MG (2002) Molecular control of lymphangiogenesis. BioEssays 24:1030-1040
31. Adams RH, Alitalo K (2007) Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 8:464-478
32. Tammela T, Saaristo A, Holopainen T et al (2007) Therapeutic differentiation and maturation of lymphatic vessels after lymph node dissection and transplantation. Nat Med 13:1458-1466
33. 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
34. Azzali G (2007) Tumor cell transendothelial passage in the absorbing lymphatic vessel of transgenic adenocarcinoma mouse prostate. Am J Pathol 170:334-346
35. 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
36. Hoshida T, Isaka N, Hagendoorn J et al (2006) Imaging steps of lymphatic metastasis reveals that vascular endothelial growth factor-C increases metastasis by increasing delivery of cancer cells to lymph nodes: therapeutic implications. Cancer Res 66:8065-8075
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. 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
39. 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
40. Saaristo A, Tammela T, Farkkila A et al (2006) Vascular endothelial growth factor-C accelerates diabetic wound healing. Am J Pathol 169:1080-1087
41. Muthuchamy M, Gashev A, Boswell N et al (2003) Molecular and functional analyses of the contractile apparatus in lymphatic muscle. FASEB J 17:920-922
42. Karpanen T, Egeblad M, Karkkainen MJ et al (2001) Vascular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth. Cancer Res 61:1786-1790
43. Wirzenius M, Tammela T, Uutela M et al (2007) Distinct vascular endothelial growth factor signals for lymphatic vessel enlargement and sprouting. J Exp Med 204:1431-1440
44. 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
45. Achen MG, Stacker SA (2012) Vascular endothelial growth factor-D: signalling mechanisms, biology and clinical relevance. Growth Factors 30:283-296
46. Shayan R, Rozen W, Bernard S et al (2008) Perforator dilatation induced by body weight gain is not reversed by subsequent weight loss: implications for perforator flaps. Plast Reconstr Surg 122:1765-1772
47. Stadelmann WK, Reintgen DS (1998) Prognosis in malignant melanoma. Hematol Oncol Clin North Am 12:767-796, vi
48. Deutsch A, Lubach D, Nissen S et al (1992) Ultrastructural studies on the invasion of melanomas in initial lymphatics of human skin. J Invest Dermatol 98:64-67
49. Gordon EJ, Rao S, Pollard JW et al (2010) Macrophages define dermal lymphatic vessel calibre during development by regulating lymphatic endothelial cell proliferation. Development 137:3899-3910
50. Harvey NL, Gordon EJ (2012) Deciphering the roles of macrophages in developmental and inflammation stimulated lymphangiogenesis. Vasc Cell 4:15