Vascular endothelial growth factor receptor-3 directly interacts with phosphatidylinositol 3-kinase to regulate lymphangiogenesis

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Coso, Sanja ^a   Zeng, Yiping ^a   Opeskin, Kenneth ^b,c   Williams, Elizabeth D ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c ST VINCENT S HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C GAMMA1; S6 KINASE; VASCULOTROPIN C; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3;

ANTIBODY DETECTION; ARTICLE; CELL GROWTH; CELL SURVIVAL; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME SPECIFICITY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPRECIPITATION; LYMPH NODE METASTASIS; LYMPHANGIOGENESIS; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SMALL CELL CARCINOMA;

BLOTTING, WESTERN; CELLS, CULTURED; ENDOTHELIAL CELLS; HUMANS; IMMUNOPRECIPITATION; LYMPHANGIOGENESIS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHATIDYLINOSITOL 3-KINASE; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3;

EID: 84862637350     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039558     Document Type: Article

References (53)

1. Osaki T, Nagashima A, Yoshimatsu T, Tashima Y, Yasumoto K, (2004) Survival and characteristics of lymph node involvement in patients with N1 non-small cell lung cancer. Lung Cancer 43: 151-157.
2. Morton DL, Thompson JF, Cochran AJ, Mozzillo N, Elashoff R, et al. (2006) Sentinel-node biopsy or nodal observation in melanoma. N Engl J Med 355: 1307-1317.
3. Wilkerson MD, Yin X, Hoadley KA, Liu Y, Hayward MC, et al. (2010) Lung squamous cell carcinoma mRNA expression subtypes are reproducible, clinically-important and correspond to different normal cell types. Clin Cancer Res 16: 4864-4875.
4. Podgrabinska S, Braun P, Velasco P, Kloos B, Pepper MS, et al. (2002) Molecular characterization of lymphatic endothelial cells. PNAS 99: 16069-16074.
5. Leu AJ, Berk DA, Lymboussaki A, Alitalo K, Jain RK, (2000) Absence of functional lymphatics within a murine sarcoma: a molecular and functional evaluation. Cancer Res 60: 4324-4327.
6. Witte MH, Bernas MJ, Martin CP, Witte CL, (2001) Lymphangiogenesis and lymphangiodysplasia: from molecular to clinical lymphology. Microsc Res Tech 55: 122-145.
7. Roma AA, Magi-Galluzzi C, Kral MA, Jin TT, Klein EA, et al. (2006) Peritumoral lymphatic invasion is associated with regional lymph node metastases in prostate adenocarcinoma. Mod Pathol 19: 392-398.
8. Gombos Z, Xu X, Chu CS, Zhang PJ, Acs G, (2005) Peritumoral lymphatic vessel density and vascular endothelial growth factor C expression in early-stage squamous cell carcinoma of the uterine cervix. Clin Cancer Res 11: 8364-8371.
9. Skobe M, Hawighorst T, Jackson DG, Prevo R, Janes L, et al. (2001) Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat Med 7: 192-198.
10. Stacker SA, Caesar C, Baldwin ME, Thornton GE, Williams RA, et al. (2001) VEGF-D promotes the metastatic spread of tumor cells via the lymphatics. Nat Med 7: 186-191.
11. Loges S, Clausen H, Reichelt U, Bubenheim M, Erbersdobler A, et al. (2007) Determination of microvessel density by quantitative real-time PCR in esophageal cancer: correlation with histologic methods, angiogenic growth factor expression, and lymph node metastasis. Clin Cancer Res 13: 76-80.
12. Mandriota SJ, Jussila L, Jeltsch M, Compagni A, Baetens D, et al. (2001) Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis. Embo J 20: 672-682.
13. Zeng Y, Opeskin K, Goad J, Williams ED, (2006) Tumor-induced activation of lymphatic endothelial cells via vascular endothelial growth factor receptor-2 is critical for prostate cancer lymphatic metastasis. Cancer Res 66: 9566-9575.
14. Hirakawa S, Brown LF, Kodama S, Paavonen K, Alitalo K, et al. (2007) VEGF-C-induced lymphangiogenesis in sentinel lymph nodes promotes tumor metastasis to distant sites. Blood 109: 1010-1017.
15. He Y, Rajantie I, Pajusola K, Jeltsch M, Holopainen T, 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.
16. Roberts N, Kloos B, Cassella M, Podgrabinska S, Persaud K, 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.
17. Achen MG, Stacker SA, (2008) Molecular control of lymphatic metastasis. Ann N Y Acad Sci pp. 225-234.
18. Joukov V, Pajusola K, Kaipainen A, Chilov D, Lahtinen I, 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.
19. Kukk E, Lymboussaki A, Taira S, Kaipainen A, Jeltsch M, et al. (1996) VEGF-C receptor binding and pattern of expression with VEGFR-3 suggests a role in lymphatic vascular development. Development 122: 3829-3837.
20. Makinen T, Veikkola T, Mustjoki S, Karpanen T, Catimel B, 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.
21. Zeng Y, Opeskin K, Baldwin ME, Horvath LG, Achen MG, et al. (2004) Expression of vascular endothelial growth factor receptor-3 by lymphatic endothelial cells is associated with lymph node metastasis in prostate cancer. Clin Cancer Res 10: 5137-5144.
22. Zhu C, Qi X, Chen Y, Sun B, Dai Y, et al. (2011) PI3K/Akt and MAPK/ERK1/2 signaling pathways are involved in IGF-1-induced VEGF-C upregulation in breast cancer. J Cancer Res Clin Oncol 137: 1587-1594.
23. Luangdilok S, Box C, Harrington K, Rhŷs-Evans P, Eccles S, (2011) MAPK and PI3K signalling differentially regulate angiogenic and lymphangiogenic cytokine secretion in squamous cell carcinoma of the head and neck. Eur J Cancer 47: 520-529.
24. Wissmann C, Detmar M, (2006) Pathways targeting tumor lymphangiogenesis. Clin Cancer Res 12: 6865-6868.
25. Holmes K, Roberts OL, Thomas AM, Cross MJ, (2007) Vascular endothelial growth factor receptor-2: Structure, function, intracellular signalling and therapeutic inhibition. Cell Signal 19: 2003-2012.
26. Wymann MP, Pirola L, (1998) Structure and function of phosphoinositide 3-kinases. Biochim Biophys Acta 1436: 127-150.
27. Pomel V, Klicic J, Covini D, Church DD, Shaw JP, et al. (2006) Furan-2-ylmethylene thiazolidinediones as novel, potent, and selective inhibitors of phosphoinositide 3-kinase gamma. J Med Chem 49: 3857-3871.
28. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, et al. (1999) Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 399: 597-601.
29. Jia H, Bagherzadeh A, Bicknell R, Duchen MR, Liu D, et al. (2004) Vascular endothelial growth factor (VEGF)-D and VEGF-A differentially regulate KDR-mediated signaling and biological function in vascular endothelial cells. J Biol Chem 279: 36148-36157.
30. Kawakami-Kimura N, Narita T, Ohmori K, Yoneda T, Matsumoto K, et al. (1997) Involvement of hepatocyte growth factor in increased integrin expression on HepG2 cells triggered by adhesion to endothelial cells. Br J Cancer 75: 47-53.
31. Rhee SG, Suh PG, Ryu SH, Lee SY, (1989) Studies of inositol phospholipid-specific phospholipase C. Science 244: 546-550.
32. Takahashi T, Yamaguchi S, Chida K, Shibuya M, (2001) A single autophosphorylation site on KDR/Flk-1 is essential for VEGF-A-dependent activation of PLC-gamma and DNA synthesis in vascular endothelial cells. Embo J 20: 2768-2778.
33. Dellinger MT, Brekken RA, (2011) Phosphorylation of Akt and ERK1/2 is required for VEGF-A/VEGFR2-induced proliferation and migration of lymphatic endothelium. PLoS ONE 6: e28947.
34. Wilde JI, Watson SP, (2001) Regulation of phospholipase C gamma isoforms in haematopoietic cells: why one, not the other? Cell Signal 13: 691-701.
35. Maffucci T, Falasca M, (2007) Phosphoinositide 3-kinase-dependent regulation of phospholipase Cgamma. Biochem Soc Trans 35: 229-230.
36. Soderberg O, Gullberg M, Jarvius M, Ridderstrale K, Leuchowius KJ, et al. (2006) Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods 3: 995-1000.
37. Wong K-K, Engelman JA, Cantley LC, (2010) Targeting the PI3K signaling pathway in cancer. Curr Opin Genetics Dev 20: 87-90.
38. Engelman JA, (2009) Targeting PI3K signalling in cancer: opportunities, challenges and limitations. Nat Rev Cancer 9: 550-562.
39. Shiojima I, Walsh K, (2002) Role of Akt signaling in vascular homeostasis and angiogenesis. Circ Res 90: 1243-1250.
40. Maffucci T, Piccolo E, Cumashi A, Iezzi M, Riley AM, et al. (2005) Inhibition of the phosphatidylinositol 3-kinase/Akt pathway by inositol pentakisphosphate results in antiangiogenic and antitumor effects. Cancer Res 65: 8339-8349.
41. Lahdenranta J, Hagendoorn J, Padera TP, Hoshida T, Nelson G, et al. (2009) Endothelial nitric oxide synthase mediates lymphangiogenesis and lymphatic metastasis. Cancer Res 69: 2801-2808.
42. Kobayashi S, Kishimoto T, Kamata S, Otsuka M, Miyazaki M, et al. (2007) Rapamycin, a specific inhibitor of the mammalian target of rapamycin, suppresses lymphangiogenesis and lymphatic metastasis. Cancer Sci 98: 726-733.
43. Spinella F, Garrafa E, Di Castro V, Rosano L, Nicotra MR, et al. (2009) Endothelin-1 stimulates lymphatic endothelial cells and lymphatic vessels to grow and invade. Cancer Res 69: 2669-2676.
44. Lahdenranta J, Hagendoorn J, Padera TP, Hoshida T, Nelson G, et al. (2009) Endothelial nitric oxide synthase mediates lymphangiogenesis and lymphatic metastasis. Cancer Res 69: 2801-2808.
45. Matsuo M, Yamada S, Koizumi K, Sakurai H, Saiki I, (2007) Tumour-derived fibroblast growth factor-2 exerts lymphangiogenic effects through Akt/mTOR/p70S6kinase pathway in rat lymphatic endothelial cells. Eur J Cancer 43: 1748-1754.
46. Tanno S, Ohsaki Y, Nakanishi K, Toyoshima E, Kikuchi K, (2004) Human small cell lung cancer cells express functional VEGF receptors, VEGFR-2 and VEGFR-3. Lung Cancer 46: 11-19.
47. Kajita T, Ohta Y, Kimura K, Tamura M, Tanaka Y, et al. (2001) The expression of vascular endothelial growth factor C and its receptors in non-small cell lung cancer. Br J Cancer 85: 255-260.
48. Feng Y, Wang W, Hu J, Ma J, Zhang Y, et al. (2010) Expression of VEGF-C and VEGF-D as significant markers for assessment of lymphangiogenesis and lymph node metastasis in non-small cell lung cancer. Anat Rec 293: 802-812.
49. Arinaga M, Noguchi T, Takeno S, Chujo M, Miura T, et al. (2003) Clinical significance of vascular endothelial growth factor C and vascular endothelial growth factor receptor 3 in patients with nonsmall cell lung carcinoma. Cancer 97: 457-464.
50. Renyi-Vamos F, Tovari J, Fillinger J, Timar J, Paku S, 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.
51. Maira S-M, Stauffer F, Brueggen J, Furet P, Schnell C, et al. (2008) Identification and characterization of NVP-BEZ235, a new orally available dual phosphatidylinositol 3-kinase/mammalian target of rapamycin inhibitor with potent in vivo antitumor activity. Mol Cancer Ther 7: 1851-1863.
52. Kang J, Ramu S, Lee S, Aguilar B, Ganesan SK, et al. (2009) Phosphate-buffered saline-based nucleofection of primary endothelial cells. Anal Biochem 386: 251-255.
53. Pegu A, Qin S, Fallert Junecko BA, Nisato RE, Pepper MS, et al. (2008) Human lymphatic endothelial cells express multiple functional TLRs. J Immunol 180: 3399-3405.