Stromal expression of vascular endothelial growth factor C is relevant to predict sentinel lymph node status in melanomas

Virchows Archiv

Volumn 458, Issue 5, 2011, Pages 621-630

  Gallego, Elena ^a   Vicioso, Luis ^a   Álvarez, Martina ^b   Hierro, Isabel ^a   Pérez Villa, Lidia ^a   Blanes, Alfredo ^a   Matilla, Alfredo ^a  

^a HOSPITAL UNIVERSITARIO VIRGEN DE LA VICTORIA   (Spain)

^b Faculty of Medicine   (Spain)

Author keywords

Immunohistochemistry; Lymphangiogenesis; Melanoma; Sentinel lymph node; Tumour stroma; VEGF C

Indexed keywords

VASCULOTROPIN C;

ADULT; AGED; ARTICLE; BIOPSY; CLINICAL ARTICLE; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPH VESSEL; LYMPHANGIOGENESIS; MACROPHAGE; MALE; MELANOMA; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; SENTINEL LYMPH NODE; STROMA CELL; TUMOR CELL;

ADOLESCENT; ADULT; AGED; ANTIBODIES, MONOCLONAL; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; LYMPHATIC METASTASIS; MALE; MELANOMA; MIDDLE AGED; SENTINEL LYMPH NODE BIOPSY; SKIN NEOPLASMS; STROMAL CELLS; VASCULAR ENDOTHELIAL GROWTH FACTOR C;

EID: 79956199557     PISSN: 09456317     EISSN: 14322307     Source Type: Journal    
DOI: 10.1007/s00428-011-1044-7     Document Type: Article

References (53)

1. Morton DL, Wen DR, Wong JH, Economou JS, Cagle LA, Storm FK, Foshag LJ, Cochran AJ (1992) Technical details of intraoperative lymphatic mapping for early stage melanoma. Arch Surg 127:392-399
2. Folkman J (1971) Tumor angiogenesis: therapeutic implications. N Engl J Med 285:1182-1186
3. Folkman J (1995) Clinical applications of research on angiogenesis. N Engl J Med 333:1757-1762
4. Karpanen T, Egeblad M, Karkkainen MJ, Kubo H, Ylä-Herttuala S, Jäättelä M, Alitalo K (2001) Vascular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth. Cancer Res 61:1786-1790 (Pubitemid 32691984)
5. Schacht V, Dadras SS, Johnson LA, Jackson DG, Hong YK, Detmar M (2005) Up-regulation of the lymphatic marker podoplanin, a mucin-type transmembrane glycoprotein, in human squamous cell carcinomas and germ cell tumors. Am J Pathol 3:913-921 (Pubitemid 40315647)
6. 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 (Pubitemid 40663742)
7. Franchi A, Gallo O, Massi D, Baroni G, Santucci M (2004) Tumor lymphangiogenesis in head and neck squamous cell carcinoma. A morphometric study with clinical correlations. Cancer 5:973-978
8. Nakamura Y, Yasuoka H, Tsujimoto M, Imabun S, Nakahara M, Nakao K, Nakamura M, Mori I, Kakudo K (2005) Lymph vessel density correlates with nodal status, VEGF-C expression, and prognosis in breast cancer. Breast Cancer Res Treat 91:125-132
9. Zeng Y, Opeskin K, Horvath LG, Sutherland RL, Williams ED (2005) Lymphatic vessel density and lymph node metastasis in prostate cancer. Prostate 9999:1-9
10. Yan G, Zhou XY, Cai SJ, Zhang GH, Peng JJ, Du X (2008) Lymphangiogenic and angiogenic microvessel density in human primary sporadic colorectal carcinoma. World J Gastroenterol 14:101-107 (Pubitemid 351314335)
11. Dadras SS, Paul T, Bertoncini J, Brown LF, Muzikansky A, Jackson DG, Ellwanger U, Garbe C, Mihm MC, Detmar M (2003) Tumor lymphangiogenesis. A novel prognostic indicador for cutaneous melanoma metastasis and survival. Am J Pathol 162:1951-1960 (Pubitemid 36613052)
12. Dadras SS, Lange-Asschenfeldt B, Velasco P, Nguyen L, Vora A, Muzikansky A, Jahnke K, Hauschild A, Hirakawa S, Mihm MC, Detmar M (2005) Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph node. Mod Pathol 18:1232-1242 (Pubitemid 43079923)
13. Massi D, Puig S, Franchi A, Malvehy J, Vidal-Sicart S, González-Cao M, Baroni G, Ketabchi S, Palou J, Santucci M (2006) Tumour lymphangiogenesis is a possible predictor of sentinel lymph node status in cutaneous melanoma: a case-control study. J Clin Pathol 59:166-173 (Pubitemid 43235582)
14. Straume O, Jackson DG, Akslen LA (2003) Independent prognostic impact of lymphatic vessel density and presence of low-grade lymphangiogenesis in cutaneous melanoma. Clin Cancer Res 9:250-256 (Pubitemid 36109741)
15. Wobser M, Siedel C, Schrama D, Bröcker EB, Becker JC, Vetter-Kauczok CS (2006) Expression pattern of the lymphatic and vascular markers VEGFR-3 and CD31 does not predict regional lymph node metastasis in cutaneous melanoma. Arch Dermatol Res 297:352-357 (Pubitemid 43144266)
16. Joukov V, Pajusola K, Kaipainen A, Chilov D, Lahtinen I, Kukk E, Saksela O, Kalkkinen N, Alitalo K (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 15:1751 (Pubitemid 26112397)
17. JS Goydos, 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 (Pubitemid 38018082)
18. Schietroma C, Cianfarani F, Lacal PM, Odorisio T, Orecchia A, Kanitakis J, D'Atri S, Failla CM, Zambruno G (2003) Vascular endothelial growth factor-C correlates with lymph node localization of human melanoma metastases. Cancer 98:789-797 (Pubitemid 36959276)
19. Boone B, Blokx W, De Bacquer D, Lambert J, Ruiter D, Brochez L (2008) The role of VEGF-C staining in predicting regional metastasis in melanoma. Virchows Arch 453:257-265
20. Shekhar MP, Pauley R, Heppner G (2003) Host microenvironment in breast cancer development: extracellular matrix-stromal cell contribution to neoplastic phenotype of epithelial cells in the breast. Breast Cancer Res 5:130-135 (Pubitemid 36519405)
21. Meier F, Will S, Ellwanger U, Schlagenhauff B, Schittek B, Rassner G, Garbe C (2002) Metastatic pathways and time courses in the orderly progression of cutaneous melanoma. Br J Dermatol 147:62-70 (Pubitemid 34779439)
22. Reintgen D, Cruse CW, Wells K et al (1994) The orderly progression of melanoma nodal metastases. Ann Surg 220:759-767 (Pubitemid 24376374)
23. Morton DL, Thompson JF, Cochran AJ, Mozzillo N, Elashoff R, Essner R, Nieweg OE, Roses DF, Hoekstra HJ, Karakousis CP, Reintgen DS, Coventry BJ, Glass EC, Wang HJ (2006) Sentinel-node biopsy or nodal observation in melanoma. N Engl J Med 355:1307-1317 (Pubitemid 44465459)
24. Kretschmer L, Thoms KM, Peeters S, Haenssle H, Bertsch HP, Emmert S (2008) Postoperative morbidity of lymph node excision for cutaneous melanoma-sentinel lymphonodectomy versus complete regional lymph node dissection. Melanoma Res 18:16-21 (Pubitemid 351628051)
25. Sleeman JP, Thiele W (2009) Tumor metastasis and the lymphatic vasculature. Int J Cancer 125:2747-2756
26. Tobler NE, Detmar M (2006) Tumor and lymph node lymphangiogenesis - impact on cancer metastasis. J Leukoc Biol 80:691-696 (Pubitemid 44835883)
27. Choi WW, Lewis MM, Lawson D, Yin-Goen Q, Birdsong GG, Cotsonis GA, Cohen C, Young AN (2005) Angiogenic and lymphangiogenic microvessel density in breast carcinoma: correlation with clinicopathologic parameters and VEGF-family gene expression. Mod Pathol 18:143-152 (Pubitemid 40128107)
28. Ueda M, Hung YC, Terai Y, Kanda K, Kanemura M, Futakuchi H, Yamaguchi H, Akise D, Yasuda M, Ueki M (2005) Vascular endothelial growth factor-C expression and invasive phenotype in ovarian carcinomas. Clin Cancer Res 11:3225-3232 (Pubitemid 40627869)
29. Skobe M, Hamberg LM, Hawighorst T, Schirner M, Wolf GL, Alitalo K, Detmar M (2001) Concurrent induction of lymphagiogenesis, angiogénesis and macrophage recruitment by vascular endothelial growth factor-C in melanoma. Am J Pathol 159:893-903 (Pubitemid 32847180)
30. Sahni D, Robson A, Orchard G, Szydlo R, Evans AV, Russell-Jones R (2005) The use of LYVE-1 antibody for detecting lymphatic involvement in patients with malignant melanoma of known sentinel node status. J Clin Pathol 58:715-721 (Pubitemid 40956825)
31. Breiteneder-Geleff S, Soleiman A, Kowalski H, Horvat R, Amann G, Kriehuber E, Diem K, Weninger W, Tschachler E, Alitalo K, Kerjaschki D (1999) Angiosarcomas express mixed endothelial phenotypes of blood and lymphatic capillaries: podoplanin as a specific marker for lymphatic endothelium. AmJ Pathol 154:385-394 (Pubitemid 29094089)
32. Van der Auwera I, Van den Eynden GG, Colpaert CG, Van Laere SJ, van Dam P, Van Marck EA, Dirix LY, Vermeulen PB (2005) Tumor lymphangiogenesis in inflammatory breast carcinoma: a histomorphometric study. Clin Cancer Res 11:7637-7642 (Pubitemid 41611604)
33. Van der Auwera I, Cao Y, Tille JC, Pepper MS, Jackson DG, Fox SB, Harris AL, Dirix LY, Vermeulen PB (2006) First international consensus on the methodology of lymphangiogenesis quantification in solid human tumours. Br J Cancer 95:1611-1625 (Pubitemid 44950785)
34. Cursiefen C, Chen L, Borges LP, Jackson D, Cao J, Radziejewski C, D'Amore PA, Dana MR, Wiegand SJ, Streilein JW (2004) VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J Clin Invest 113:1040-1050 (Pubitemid 38544126)
35. Ristimaki A, Narko K, Enholm B, Joukov V, Alitalo K (1998) Proinflammatory cytokines regulate expression of the lymphatic endothelial mitogen vascular endothelial growth factor-C. J Biol Chem 273:8413-8418 (Pubitemid 28168903)
36. Rinderknecht M, Detmar M (2008) Tumor lymphangiogenesis and melanoma metastasis. J Cell Physiol 216:347-354 (Pubitemid 351898461)
37. Alitalo K, Tammela T, Petrova TV (2005) Lymphangiogenesis in development and human disease. Nature 438:946-953 (Pubitemid 43093960)
38. Vihinen PP, Hilli J, Vuoristo MS, Syrjänen KJ, Kähäri VM, Pyrhönen SO (2007) Serum VEGF-C is associated with metastatic site in patients with malignant melanoma. Acta Oncol 46:678-684 (Pubitemid 46911902)
39. Angeli F, Koumakis G, Chen MC, Kumar S, Delinassios JG (2009) Role of stromal fibroblasts in cancer: promoting or impeding? Tumour Biol 30:109-120
40. Vicioso L, Gonzalez FJ, Alvarez M, Ribelles N, Molina M, Marquez A, Perez L, Matilla A, Alba E (2006) Elevated serum levels of vascular endothelial growth factor are associated with tumor-associated macrophages in primary breast cancer. Am J Clin Pathol 125:111-118 (Pubitemid 43089733)
41. Coffelt SB, Hughes R, Lewis CE (2009) Tumor-associated macrophages: effectors of angiogenesis and tumor progression. Biochim Biophys Acta 1796:11-18
42. Yamashita M, Iwama N, Date F, Shibata N, Miki H, Yamauchi K, Sawai T, Sato S, Takahashi T, Ono M (2009) Macrophages participate in lymphangiogenesis in idiopathic diffuse alveolar damage through CCL19-CCR7 signal. Hum Pathol 40:1553-1563
43. Schoppmann SF, Birner P, Stöckl J, Kalt R, Ullrich R, Caucig C, Kriehuber E, Nagy K, Alitalo K, Kerjaschki D (2002) Tumor-associated macrophages express lymphatic endothelial growth factors and are related to peritumoral lymphangiogenesis. Am J Pathol 161:947-956 (Pubitemid 34988382)
44. Camps JL, Chang SM, Hsu TC, Freeman MR, Hong SJ, Zhau HE, von Eschenbach AC, Chung LW (1990) Fibroblast-mediated acceleration of human epithelial tumor growth in vivo. Proc Natl Acad Sci USA 87:75-79
45. Olumi AF, Grossfeld GD, Hayward SW, Carroll PR, Tlsty TD, Cunha GR (1999) Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Res 59:5002-5011 (Pubitemid 29472907)
46. Kalluri R, Zeisberg M (2006) Fibroblasts in cancer. Nat Rev Cancer 6:392-401
47. Fukumura D, Xavier R, Sugiura T, Chen Y, Park EC, Lu N, Selig M, Nielsen G, Taksir T, Jain RK, Seed B (1998) Tumor induction of VEGF promoter activity in stromal cells. Cell 94:715-725 (Pubitemid 28436004)
48. Koyama H, Kobayashi N, Harada M, Takeoka M, Kawai Y, Sano K, Fujimori M, Amano J, Ohhashi T, Kannagi R, Kimata K, Taniguchi S, Itano N (2008) Significance of tumor-associated stroma in promotion of intratumoral lymphangiogenesis: pivotal role of a hyaluronan-rich tumor microenvironment. Am J Pathol 172:179-193 (Pubitemid 351186379)
49. Tammela T, Alitalo K (2010) Lymphangiogenesis: molecular mechanisms and future promise. Cell 140:460-476
50. Skobe M, Hawighorst T, Jackson DG, Prevo R, Janes L, Velasco P, Riccardi L, Alitalo K, Claffey K, Detmar M (2001) Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat Med 7:192-198 (Pubitemid 32148486)
51. Tammela T, Saaristo A, Holopainen T, Lyytikka J, Kotronen A, Pitkonen M, Abo-Ramadan U, Yla-Herttuala S, Petrova TV, Alitalo K (2007) Therapeutic differentiation and maturation of lymphatic vessels after lymph node dissection and transplantation. Nat Med 13:1458-1466 (Pubitemid 350224251)
52. He Y 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 (Pubitemid 40740810)
53. Hirakawa S (2009) From tumor lymphangiogenesis to lymphvascular niche. Cancer Sci 100:983-989