Endocan is upregulated on tumor vessels in invasive bladder cancer where it mediates VEGF-A-induced angiogenesis

Cancer Research

Volumn 73, Issue 3, 2013, Pages 1097-1106

  Roudnicky, Filip ^a   Poyet, Cedric ^b   Wild, Peter ^c   Krampitz, Sarah ^a   Negrini, Fabrizia ^a   Huggenberger, Reto ^a   Rogler, Anja ^d   Stöhr, Robert ^d   Hartmann, Arndt ^d   Provenzano, Maurizio ^b   Otto, Vivianne I ^a   Detmar, Michael ^a  

^a ETH ZURICH   (Switzerland)

^b Departments of Urology   (Switzerland)

^c UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^d UNIVERSITY HOSPITAL ERLANGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CELL PROTEIN; ENDOCAN PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLADDER CANCER; CANCER SURVIVAL; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; FILOPODIUM; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RECURRENCE FREE SURVIVAL; SURVIVAL TIME; TUMOR VASCULARIZATION; UPREGULATION;

ADULT; AGED; AGED, 80 AND OVER; CELLS, CULTURED; ENDOTHELIAL CELLS; FEMALE; HUMANS; MALE; MIDDLE AGED; NEOPLASM PROTEINS; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHORYLATION; PROTEOGLYCANS; UP-REGULATION; URINARY BLADDER NEOPLASMS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84873417872     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-1855     Document Type: Article

References (48)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011;61:69-90.
2. Raghavan D, Shipley WU, Garnick MB, Russell PJ, Richie JP. Biology and management of bladder cancer. N Engl J Med 1990;322:1129-38.
3. Eble JN, Sauter G, Epstein JI, Sesterhenn IA, editors. World Health Organization classification of tumours. Pathology and genetics of tumours of the urinary system and male genital organs. Lyon, France: IARC Press; 2004.
4. Wild PJ, Herr A, Wissmann C, Stoehr R, Rosenthal A, Zaak D, et al. Gene expression profiling of progressive papillary noninvasive carcinomas of the urinary bladder. Clin Cancer Res 2005;11:4415-29.
5. Stein JP, Lieskovsky G, Cote R, Groshen S, Feng AC, Boyd S, et al. Radical cystectomy in the treatment of invasive bladder cancer: longterm results in 1,054 patients. J Clin Oncol 2001;19:666-75.
6. Ghoneim MA, el-Mekresh MM, el-Baz MA, el-Attar IA, Ashamallah A. Radical cystectomy for carcinoma of the bladder: critical evaluation of the results in 1,026 cases. J Urol 1997;158:393-9.
7. Bochner BH, Cote RJ, Weidner N, Groshen S, Chen SC, Skinner DG, et al. Angiogenesis in bladder cancer: relationship between microvessel density and tumor prognosis. J Natl Cancer Inst 1995;87: 1603-12.
8. Bernardini S, Fauconnet S, Chabannes E, Henry PC, Adessi G, Bittard H. Serum levels of vascular endothelial growth factor as a prognostic factor in bladder cancer. J Urol 2001;166:1275-9.
9. Goddard JC, Sutton CD, Furness PN, O'Byrne KJ, Kockelbergh RC. Microvessel density at presentation predicts subsequent muscle invasion in superficial bladder cancer. Clin Cancer Res 2003;9:2583-6.
10. Crew JP, O'Brien T, Bradburn M, Fuggle S, Bicknell R, Cranston D, et al. Vascular endothelial growth factor is a predictor of relapse and stage progression in superficial bladder cancer. Cancer Res 1997;57: 5281-5.
11. Dickinson AJ, Fox SB, Persad RA, Hollyer J, Sibley GN, Harris AL. Quantification of angiogenesis as an independent predictor of prognosis in invasive bladder carcinomas. Br J Urol 1994;74:762-6.
12. Lassalle P, Molet S, Janin A, Heyden JV, Tavernier J, Fiers W, et al. ESM-1 is a novel human endothelial cell-specific molecule expressed in lung and regulated by cytokines. J Biol Chem 1996;271:20458-64.
13. Shin JW, Huggenberger R, Detmar M. Transcriptional profiling of VEGF-A and VEGF-C target genes in lymphatic endothelium reveals endothelial-specific molecule-1 as a novel mediator of lymphangiogenesis. Blood 2008;112:2318-26.
14. Rennel E, Mellberg S, Dimberg A, Petersson L, Botling J, Ameur A, et al. Endocan is a VEGF-A and PI3K regulated gene with increased expression in human renal cancer. Exp Cell Res 2007;313:1285-94.
15. Leroy X, Aubert S, Zini L, Franquet H, Kervoaze G, Villers A, et al. Vascular endocan (ESM-1) is markedly overexpressed in clear cell renal cell carcinoma. Histopathology 2010;56:180-7.
16. Grigoriu BD, Depontieu F, Scherpereel A, Gourcerol D, Devos P, Ouatas T, et al. Endocan expression and relationship with survival in human non-small cell lung cancer. Clin Cancer Res 2006;12:4575-82.
17. Maurage C-A, Adam E, Minéo J-F, Sarrazin S, Debunne M, Siminski RM, et al. Endocan expression and localization in human glioblastomas. J Neuropathol Exp Neurol 2009;68:633-41.
18. Sarrazin S, Adam E, Lyon M, Depontieu F, Motte V, Landolfi C, et al. Endocan or endothelial cell specific molecule-1 (ESM-1): a potential novel endothelial cell marker and a new target for cancer therapy. Biochim Biophys Acta 2006;1765:25-37.
19. Baluk P, Morikawa S, Haskell A, Mancuso M, McDonald DM. Abnormalities of basement membrane on blood vessels and endothelial sprouts in tumors. Am J Pathol 2003;163:1801-15.
20. Kunstfeld R, Hirakawa S, Hong Y-K, Schacht V, Lange-Asschenfeldt B, Velasco P, et al. Induction of cutaneous delayed-type hypersensitivity reactions in VEGF-A transgenic mice results in chronic skin inflammation associated with persistent lymphatic hyperplasia. Blood 2004;104:1048-57.
21. Xia YP, Li B, Hylton D, Detmar M, Yancopoulos GD, Rudge JS. Transgenic delivery of VEGF to mouse skin leads to an inflammatory condition resembling human psoriasis. Blood 2003;102:161-8.
22. Huggenberger R, Siddiqui SS, Brander D, Ullmann S, Zimmermann K, Antsiferova M, et al. An important role of lymphatic vessel activation in limiting acute inflammation. Blood 2011;117:4667-78.
23. Hirakawa S, Hong Y-K, Harvey N, Schacht V, Matsuda K, Libermann T, et al. Identification of vascular lineage-specific genes by transcriptional profiling of isolated blood vascular and lymphatic endothelial cells. Am J Pathol 2003;162:575-86.
24. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008;3:1101-8.
25. Schulz MM, Reisen F, Zgraggen S, Fischer S, Yuen D, Kang GJ, et al. Phenotype-based high-content chemical library screening identifies statins as inhibitors of in vivo lymphangiogenesis. Proc Natl Acad Sci USA 2012;109:2665-74.
26. Wessel D, Flügge UI. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 1984;138:141-3.
27. Bignon M, Pichol-Thievend C, Hardouin J, Malbouyres M, Brechot N, Nasciutti L, et al. Lysyl oxidase-like protein-2 regulates sprouting angiogenesis and type IV collagen assembly in the endothelial basement membrane. Blood 2011;118:3979-89.
28. McGonigle S, Shifrin V. In vitro assay of angiogenesis: inhibition of capillary tube formation. Current protocols in pharmacology. Hoboken, NJ, USA: John Wiley & Sons, Inc.; 2008.
29. Geback T, Schulz MM, Koumoutsakos P, Detmar M. TScratch: a novel and simple software tool for automated analysis of monolayer wound healing assays. Biotechniques 2009;46:265-74.
30. Magnusson P, Rolny C, Jakobsson L, Wikner C, WuY, Hicklin DJ, et al. Deregulation of Flk-1/vascular endothelial growth factor receptor-2 in fibroblast growth factor receptor-1-deficient vascular stem cell development. J Cell Sci 2004;117:1513-23.
31. van der Loos CM, Meijer-Jorna LB, Broekmans ME, Ploegmakers HP, Teeling P, de Boer OJ, et al. Anti-human vascular endothelial growth factor (VEGF) antibody selection for immunohistochemical staining of proliferating blood vessels. J Histochem Cytochem 2009;58:109-18.
32. Hardingham TE, Fosang AJ. Proteoglycans: many forms and many functions. FASEB J 1992;6:861-70.
33. Bishop JR, Schuksz M, Esko JD. Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 2007;446:1030-7.
34. van 't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AAM, Mao M, et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 2002;415:530-6.
35. Borczuk AC, Shah L, Pearson GD, Walter KL, Wang L, Austin JH, et al. Molecular signatures in biopsy specimens of lung cancer. Am J Respir Crit Care Med 2004;170:167-74.
36. Wattel S, Mircescu H, Venet D, Burniat A, Franc B, Frank S, et al. Gene expression in thyroid autonomous adenomas provides insight into their physiopathology. Oncogene 2005;24:6902-16.
37. Van Tilborg AA, Bangma CH, Zwarthoff EC. Bladder cancer biomarkers and their role in surveillance and screening. Int J Urol 2009;16:23-30.
38. Brems-Eskildsen AS, Zieger K, Toldbod H, Holcomb C, Higuchi R, Mansilla F, et al. Prediction and diagnosis of bladder cancer recurrence based on urinary content of hTERT, SENP1, PPP1CA, and MCM5 transcripts. BMC Cancer 2010;10:646.
39. De Smet F, Segura I, De Bock K, Hohensinner PJ, Carmeliet P. Mechanisms of vessel branching: filopodia on endothelial tip cells lead the way. Arterioscler Thromb Vasc Biol 2009;29:639-49.
40. Del Toro R, Prahst C, Mathivet T, Siegfried G, Kaminker JS, Larrivee B, et al. Identification and functional analysis of endothelial tip cellenriched genes. Blood 2010;116:4025-33.
41. Strasser GA, Kaminker JS, Tessier-Lavigne M. Microarray analysis of retinal endothelial tip cells identifies CXCR4 as a mediator of tip cell morphology and branching. Blood 2010;115:5102-10.
42. Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 2003;161:1163-77.
43. Aitkenhead M, Wang S-J, Nakatsu MN, Mestas J, Heard C, Hughes CCW. Identification of endothelial cell genes expressed in an in vitro model of angiogenesis: induction of ESM-1, big-h3, and NrCAM. Microvasc Res 2002;63:159-71.
44. Taylor KR, Gallo RL. Glycosaminoglycans and their proteoglycans: host-associated molecular patterns for initiation and modulation of inflammation. FASEB J 2006;20:9-22.
45. Zhang L. Glycosaminoglycan (GAG) biosynthesis and GAG-binding proteins. Prog Mol Biol Transl Sci 2010;93:1-17.
46. Sarrazin S, Lyon M, Deakin JA, Guerrini M, Lassalle P, Delehedde M, et al. Characterization and binding activity of the chondroitin/dermatan sulfate chain from Endocan, a soluble endothelial proteoglycan. Glycobiology 2010;20:1380-8.
47. Bechard D, Gentina T, Delehedde M, Scherpereel A, Lyon M, Aumercier M, et al. Endocan is a novel chondroitin sulfate/dermatan sulfate proteoglycan that promotes hepatocyte growth factor/scatter factor mitogenic activity. J Biol Chem 2001;276:48341-9.
48. Kajiya K, Hirakawa S, Ma B, Drinnenberg I, Detmar M. Hepatocyte growth factor promotes lymphatic vessel formation and function. EMBO J 2005;24:2885-95.