Targeting receptor tyrosine kinase on lymphatic endothelial cells for the therapy of colon cancer lymph node metastasis

Neoplasia

Volumn 8, Issue 9, 2006, Pages 747-757

  Rebhun, Robert B ^a   Langley, Robert R ^a   Yokoi, Kenji ^a   Fan, Dominic ^a   Gershenwaldy, Jeffrey E ^a   Fidler, Isaiah J ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Colon cancer; Lymph node metastasis; Lymphangiogenesis; Lymphatic endothelial cells; Tyrosine kinase

Indexed keywords

6 [4 (4 ETHYL 1 PIPERAZINYLMETHYL)PHENYL] 4 (ALPHA METHYLBENZYLAMINO) 7H PYRROLO[2,3 D]PYRIMIDINE; CELL MARKER; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL CULTURE; CELL LINE; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; COLON CANCER; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; LYMPH NODE METASTASIS; LYMPH VESSEL ENDOTHELIUM; MALE; MESENTERY; MICROSURGERY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SURGICAL APPROACH; TUMOR CELL;

EID: 33749069984     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.06322     Document Type: Article

References (52)

1. Compton CC and Greene FL (2004). The staging of colorectal cancer: 2004 and beyond. CA Cancer J Clin 54, 295-308.
2. Karpanen T, Egeblad M, Karkkainen MJ, Kubo H, Yla-Herttuala S, Jaattela M, and Alitalo K (2001). Vascular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth. Cancer Res 61, 1786-1790.
3. Stacker SA, Caesar C, Baldwin ME, Thornton GE, Williams RA, Prevo R, Jackson DG, Nishikawa S, Kubo H, and Achen MG (2001). VEGF-D promotes the metastatic spread of tumor cells via the lymphatics. Nat Med 7, 186-191.
4. Skobe M, Hawighorst T, Jackson DG, Prevo R, Janes L, Velasco P, Riccardi L, Alitalo K, Claffey K, and Detmar M (2001). Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat Med 7, 192-198.
5. Mandriota SJ, Jussila L, Jeltsch M, Compagni A, Baetens D, Prevo R, Banerji S, Huarte J, Montesano R, Jackson DG, et al. (2001). Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis. EMBO J 20, 672-682.
6. Bjorndahl MA, Cao R, Burton JB, Brakenhielm E, Religa P, Galter D, Wu L, and Cao Y (2005). Vascular endothelial growth factor-α promotes peritumoral lymphangiogenesis and lymphatic metastasis. Cancer Res 65, 9261-9268.
7. Liu NF and He QL (1997). The regulatory effects of cytokines on lymphatic angiogenesis. Lymphology 30, 3-12.
8. Achen MG and Stacker SA (2006). Tumor lymphangiogenesis and metastatic spread: new players begin to emerge. Int J Cancer [Epub ahead of print].
9. Sleeman JP, Krishnan J, Kirkin V, and Baumann P (2001). Markers for the lymphatic endothelium: in search of the Holy Grail? Microsc Res Tech 55, 61-69.
10. Kaiserling E, Krober S, and Geleff S (2003). Lymphatic vessels in the colonic mucosa in ulcerative colitis. Lymphology 36, 52-61.
11. Fogt F, Pascha TL, Zhang PJ, Gausas RE, Rahemtulla A, and Zimmerman RL (2004). Proliferation of D2-40-expressing intestinal lymphatic vessels in the lamina propria in inflammatory bowel disease. Int J Mol Med 13, 211-214.
12. Fogt F, Zimmerman RL, Ross HM, Daly T, and Gausas RE (2004). Identification of lymphatic vessels in malignant, adenomatous and normal colonic mucosa using the novel immunostain D2-40. Oncol Rep 11, 47-50.
13. Minsky BD, Mies C, Rich TA, and Recht A (1989). Lymphatic vessel invasion is an independent prognostic factor for survival in colorectal cancer. Int J Radiat Oncol Biol Phys 17, 311-318.
14. Kuroyama S, Kobayashi N, Ohbu M, Ohtani Y, Okayasu I, and Kakita A (2005). Enzyme histochemical analysis of lymphatic vessels in colon carcinoma: occurrence of lymphangiogenesis within the tumor. Hepatogastroenterology 52, 1057-1061.
15. Liang P, Hong JW, Ubukata H, Liu G, Katano M, Motohashi G, Kasuga T, Watanabe Y, Nakada I, and Tabuchi T (2006). Increased density and diameter of lymphatic microvessels correlate with lymph node metastasis in early stage invasive colorectal carcinoma. Virchows Arch [Epub ahead of print].
16. Liang P, Hong JW, Ubukata H, Liu G, Katano M, Motohashi G, Kasuga T, Watanabe Y, Nakada I, and Tabuchi T (2005). Myofibroblasts correlate with lymphatic microvessel density and lymph node metastasis in early-stage invasive colorectal carcinoma. Anticancer Res 25, 2705-2712.
17. Akagi K, Ikeda Y, Miyazaki M, Abe T, Kinoshita J, Maehara Y, and Sugimachi K (2000). Vascular endothelial growth factor-C (VEGF-C) expression in human colorectal cancer tissues. Br J Cancer 83, 887-891.
18. Furudoi A, Tanaka S, Haruma K, Kitadai Y, Yoshihara M, Chayama K, and Shimamoto F (2002). Clinical significance of vascular endothelial growth factor C expression and angiogenesis at the deepest invasive site of advanced colorectal carcinoma. Oncology 62, 157-166.
19. George ML, Tutton MG, Janssen F, Arnaout A, Abulafi AM, Eccles SA, and Swift RI (2001). VEGF-A, VEGF-C, and VEGF-Din colorectal cancer progression. Neoplasia 3, 420-427.
20. Soumaoro LT, Uetake H, Takagi Y, Iida S, Higuchi T, Yasuno M, Enomoto M, and Sugihara K (2006). Coexpression ofVEGF-C and Cox-2 in human colorectal cancer and its association with lymph node metastasis. Dis Colon Rectum 49, 392-398.
21. Denekamp J (1984). Vascular endothelium as the vulnerable element in tumours. Acta Radiol Oncol 23, 217-225.
22. Yokoi K, Thaker PH, Yazici S, Rebhun R, Nam D, He J, Kim SJ, Abbruzzese JL, Hamilton SR, and Fidler IJ (2005). Dual inhibition of epidermal growth factor receptor and vascular endothelial growth factor receptor phosphorylation by AEE788 reduces growth and metastasis of human colon carcinoma in an orthotopic nude mouse model. Cancer Res 65, 3716-3725.
23. Yigitbasi OG, Younes MN, Doan D, Jasser SA, Schiff BA, Bucana CD, Bekele BN, Fidler IJ, and Myers JN (2004). Tumor cell and endothelial cell therapy of oral cancer by dual tyrosine kinase receptor blockade. Cancer Res 64, 7977-7984.
24. Younes MN, Yigitbasi OG, Park YW, Kim SJ, Jasser SA, Hawthorne VS, Yazici SD, Mandal M, Bekele BN, Bucana CD, et al. (2005). Antivascular therapy of human follicular thyroid cancer experimental bone metastasis by blockade of epidermal growth factor receptor and vascular growth factor receptor phosphorylation. Cancer Res 65, 4716-4727.
25. Kim SJ, Uehara H, Karashima T, Shepherd DL, Killion JJ, and Fidler IJ (2003). Blockade of epidermal growth factor receptor signaling in tumor cells and tumor-associated endothelial cells for therapy of androgen-independent human prostate cancer growing in the bone of nude mice. Clin Cancer Res 9, 1200-1210.
26. Baker CH, Kedar D, McCarty MF, Tsan R, Weber KL, Bucana CD, and Fidler IJ (2002). Blockade of epidermal growth factor receptor signaling on tumor cells and tumor-associated endothelial cells for therapy of human carcinomas. Am J Pathol 161, 929-938.
27. Langley RR, Fan D, Tsan RZ, Rebhun R, He J, Kim SJ, and Fidler IJ (2004). Activation of the platelet-derived growth factor-receptor enhances survival of murine bone endothelial cells. Cancer Res 64, 3727-3730.
28. Traxler P, Allegrini PR, Brandt R, Brueggen J, Cozens R, Fabbro D, Grosios K, Lane HA, McSheehy P, Mestan J, et al. (2004). AEE788: a dual family epidermal growth factor receptor/ErbB2 and vascular endothelial growth factor receptor tyrosine kinase inhibitor with antitumor and antiangiogenic activity. Cancer Res 64, 4931-4941.
29. Langley RR, Ramirez KM, Tsan RZ, Van Arsdall M, Nilsson MB, and Fidler IJ (2003). Tissue-specific microvascular endothelial cell lines from H-2K(b)-tsA58 mice for studies of angiogenesis and metastasis. Cancer Res 63, 2971-2976.
30. Weidner N, Semple JP, Welch WR, and Folkman J (1991). Tumor angiogenesis and metastasis - correlation in invasive breast carcinoma. N Engl J Med 324, 1-8.
31. Carmichael J, DeGraff WG, Gazdar AF, Minna JD, and Mitchell JB (1987). Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing. Cancer Res 47, 936-942.
32. Makinen T, Veikkola T, Mustjoki S, Karpanen T, Catimel B, Nice EC, Wise L, Mercer A, Kowalski H, Kerjaschki D, et al. (2001). Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3. EMBO J 20, 4762-4773.
33. Cao R, Bjorndahl MA, Religa P, Clasper S, Garvin S, Galter D, Meister B, Ikomi F, Tritsaris K, Dissing S, et al. (2004). PDGF-BB induces intratumoral lymphangiogenesis and promotes lymphatic metastasis. Cancer Cell 6, 333-345.
34. Joukov V, Pajusola K, Kaipainen A, Chilov D, Lahtinen I, Kukk E, Saksela O, Kalkkinen N, and 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, 290-298.
35. Yamada Y, Nezu J, Shimane M, and Hirata Y (1997). Molecular cloning of a novel vascular endothelial growth factor, VEGF-D. Genomics 42, 483-488.
36. Achen MG, Jeltsch M, Kukk E, Makinen T, Vitali A, Wilks AF, Alitalo K, and Stacker SA (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.
37. Aprelikova O, Pajusola K, Partanen J, Armstrong E, Alitalo R, Bailey SK, McMahon J, Wasmuth J, Hueber K, and Alitalo I (1992). FLT4, a novel class III receptor tyrosine kinase in chromosome 5q33-qter. Cancer Res 52, 746-748.
38. Kaipainen A, Korhonen J, Mustonen T, van Hinsbergh VW, Fang GH, Dumont D, Breitman M, and Alitalo K (2005). Expression of the fms-like tyrosine kinase 4 gene becomes restricted to lymphatic endothelium during development. Proc Natl Acad Sci USA 92, 3566-3570.
39. Enholm B, Karpanen T, Jeltsch M, Kubo H, Stenback F, Prevo R, Jackson DG, Yla-Herttuala S, and Alitalo K (2001). Adenoviral expression of vascular endothelial growth factor-C induces lymphangiogenesis in the skin. Circ Res 88, 623-629.
40. Enholm B, Paavonen K, Ristimaki A, Kumar V, Gunji Y, Klefstrom J, Kivinen L, Laiho M, Olofsson B, Joukov V, et al. (1997). Comparison of VEGF, VEGF-B, VEGF-C and Ang-1 mRNA regulation by serum, growth factors, oncoproteins and hypoxia. Oncogene 14, 2475-2483.
41. Ristimaki A, Narko K, Enholm B, Joukov V, and Alitalo K (1998). Proinflammatory cytokines regulate expression of the lymphatic endothelial mitogen vascular endothelial growth factor-C. J Biol Chem 273, 8413-8418.
42. Tang Y, Zhang D, Fallavollita L, and Brodt P (2003). Vascular endothelial growth factor C expression and lymph node metastasis are regulated by the type I insulin-like growth factor receptor. Cancer Res 63, 1166-1171.
43. Cursiefen C, Chen L, Borges LP, Jackson D, Cao J, Radziejewski C, D'Amore PA, Dana MR, Wiegand SJ, and Streilein JW (2004). VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J Clin Invest 113, 1040-1050.
44. Schoppmann SF, Birner P, Stockl J, Kalt R, Ullrich R, Caucig C, Kriehuber E, Nagy K, Alitalo K, and Kerjaschki D (2002). Tumor-associated macrophages express lymphatic endothelial growth factors and are related to peritumoral lymphangiogenesis. Am J Pathol 161, 947-956.
45. Nagy JA, Vasile E, Feng D, Sundberg C, Brown LF, Detmar MJ, Lawitts JA, Benjamin L, Tan X, Manseau EJ, et al. (2002). Vascular permeability factor/vascular endothelial growth factor induces lymphangiogenesis as well as angiogenesis. J Exp Med 196, 1497-1506.
46. Jiang WG, Davies G, Martin TA, Parr C, Watkins G, Mansel RE, and Mason MD (2005). The potential lymphangiogenic effects of hepatocyte growth factor/scatter factor in vitro and in vivo. Int J Mol Med 16, 723-728.
47. Kajiya K, Hirakawa S, Ma B, Drinnenberg I, and Detmar M (2005). Hepatocyte growth factor promotes lymphatic vessel formation and function. EMBO J 24, 2885-2895.
48. Kubo H, Cao R, Brakenhielm E, Makinen T, Cao Y, and Alitalo K (2002). Blockade of vascular endothelial growth factor receptor-3 signaling inhibits fibroblast growth factor-2-induced lymphangiogenesis in mouse cornea. Proc Natl Acad Sci USA 99, 8868-8873.
49. Pietrzkowski Z, Sell C, Lammers R, Ullrich A, and Baserga R (1992). Roles of insulin-like growth factor 1 (IGF-1) and the IGF-1 receptor in epidermal growth factor-stimulated growth of 3T3 cells. Mol Cell Biol 12, 3883-3889.
50. Maity A, Pore N, Lee J, Solomon D, and O'Rourke DM (2000). Epidermal growth factor receptor transcriptionally up-regulates vascular endothelial growth factor expression in human glioblastoma cells via a pathway involving phosphatidylinositol 3′-kinase and distinct from that induced by hypoxia. Cancer Res 60, 5879-5886.
51. Dixelius J, Makinen T, Wirzenius M, Karkkainen MJ, Wernstedt C, Alitalo K, and Claesson-Welsh L (2003). Ligand-induced vascular endothelial growth factor receptor-3 (VEGFR-3) heterodimerization with VEGFR-2 in primary lymphatic endothelial cells regulates tyrosine phosphorylation sites. J Biol Chem 278, 40973-40979.
52. Alan A, Herault JP, Barron P, Favier B, Fons P, Delesque-Touchard N, Senegas I, Laboudie P, Bonnin J, Cassan C, et al. (2004). Heterodimerization with vascular endothelial growth factor receptor-2 (VEGFR-2) is necessary for VEGFR-3 activity. Biochem Biophys Res 324, 909-915.