Inhibition of VEGF-C Modulates Distal Lymphatic Remodeling and Secondary Metastasis

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Gogineni, Alvin ^a   Caunt, Maresa ^a   Crow, Ailey ^a   Lee, Chingwei V ^a   Fuh, Germaine ^a   van Bruggen, Nicholas ^a   Ye, Weilan ^a   Weimer, Robby M ^a  

^a GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMETASTATIC AGENT; NRP2 ANTIBODY; RAGWEED ANTIBODY; UNCLASSIFIED DRUG; VASCULOTROPIN A ANTIBODY; VASCULOTROPIN ANTIBODY; VASCULOTROPIN C; VASCULOTROPIN C ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER ADJUVANT THERAPY; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; DISTANT METASTASIS; FEMALE; IN VIVO STUDY; LONGITUDINAL STUDY; LYMPHATIC DRAINAGE; METASTASIS; MOUSE; NONHUMAN; PROTEIN FAMILY; PROTEIN FUNCTION; RAT; SECONDARY METASTASIS; SENTINEL LYMPH NODE METASTASIS; UPREGULATION;

ANIMALS; ANTIBODIES; FEMALE; LYMPH; LYMPH NODES; LYMPHATIC METASTASIS; MALE; MICE; MICE, INBRED BALB C; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR C;

EID: 84880456245     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068755     Document Type: Article

References (57)

1. Liotta LA, (1992) Cancer cell invasion and metastasis. Sci Am 266: 54-9-62-3.
2. Nguyen DX, Bos PD, Massagué J, (2009) Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer 9: 274-284 doi:10.1038/nrc2622.
3. Pipas JM, Barth RJ, Zaki B, Tsapakos MJ, Suriawinata AA, et al. (2005) Docetaxel/Gemcitabine followed by gemcitabine and external beam radiotherapy in patients with pancreatic adenocarcinoma. Ann Surg Oncol 12: 995-1004 doi:10.1245/ASO.2005.04.503.
4. Ramnath N, Sommers E, Robinson L, Nwogu C, Sharma A, et al. (2005) Phase II study of neoadjuvant chemotherapy with gemcitabine and vinorelbine in resectable non-small cell lung cancer. Chest 128: 3467-3474 doi:10.1378/chest.128.5.3467.
5. Peintinger F, Symmans WF, Gonzalez-Angulo AM, Boughey JC, Buzdar AU, et al. (2006) The safety of breast-conserving surgery in patients who achieve a complete pathologic response after neoadjuvant chemotherapy. Cancer 107: 1248-1254 doi:10.1002/cncr.22111.
6. Zbytek B, Carlson JA, Granese J, Ross J, Mihm MC, et al. (2008) Current concepts of metastasis in melanoma. Expert Rev Dermatol 3: 569-585 doi:10.1586/17469872.3.5.569.
7. Gallagher DJ, Milowsky MI, (2009) Bladder cancer. Curr Treat Options Oncol 10: 205-215 doi:10.1007/s11864-009-0112-6.
8. Campbell NP, Villaflor VM, (2010) Neoadjuvant treatment of esophageal cancer. World J Gastroenterol 16: 3793-3803.
9. Taylor MD, Nagji AS, Bhamidipati CM, Theodosakis N, Kozower BD, et al. (2012) Tumor recurrence after complete resection for non-small cell lung cancer. Ann Thorac Surg 93: 1813-1821 doi:10.1016/j.athoracsur.2012.03.031.
10. Alitalo K, (2011) The lymphatic vasculature in disease. Nat Med 17: 1371-1380 doi:10.1038/nm.2545.
11. Pepper MS, Tille J-C, Nisato R, Skobe M, (2003) Lymphangiogenesis and tumor metastasis. Cell Tissue Res 314: 167-177 doi:10.1007/s00441-003-0748-7.
12. Kyzas PA, Geleff S, Batistatou A, Agnantis NJ, Stefanou D, (2005) Evidence for lymphangiogenesis and its prognostic implications in head and neck squamous cell carcinoma. J Pathol 206: 170-177 doi:10.1002/path.1776.
13. Krag D, Weaver D, Ashikaga T, Moffat F, Klimberg VS, et al. (1998) The sentinel node in breast cancer-a multicenter validation study. N Engl J Med 339: 941-946 doi:10.1056/NEJM199810013391401.
14. Lin KM, Rodriguez F, Ota DM, (2002) The sentinel node in colorectal carcinoma. Mapping technique, pathologic assessment, and clinical relevance. Oncology (Williston Park, NY) 16: 567-75.
15. Veronesi U, Paganelli G, Viale G, Luini A, Zurrida S, et al. (2003) A randomized comparison of sentinel-node biopsy with routine axillary dissection in breast cancer. N Engl J Med 349: 546-553 doi:10.1056/NEJMoa012782.
16. 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 doi:10.1056/NEJMoa060992.
17. Saad RS, Kordunsky L, Liu YL, Denning KL, Kandil HA, et al. (2006) Lymphatic microvessel density as prognostic marker in colorectal cancer. Mod Pathol 19: 1317-1323 doi:10.1038/modpathol.3800651.
18. Zivanovic O, Khoury-Collado F, Abu-Rustum NR, Gemignani ML, (2009) Sentinel lymph node biopsy in the management of vulvar carcinoma, cervical cancer, and endometrial cancer. Oncologist 14: 695-705 doi:10.1634/theoncologist.2009-0075.
19. Stacker SA, Achen MG, Jussila L, Baldwin ME, Alitalo K, (2002) Lymphangiogenesis and cancer metastasis. Nat Rev Cancer 2: 573-583 doi:10.1038/nrc863.
20. Tammela T, Alitalo K, (2010) Lymphangiogenesis: Molecular mechanisms and future promise. Cell 140: 460-476 doi:10.1016/j.cell.2010.01.045.
21. Karkkainen MJ, Saaristo A, Jussila L, Karila KA, Lawrence EC, et al. (2001) A model for gene therapy of human hereditary lymphedema. Proc Natl Acad Sci USA 98: 12677-12682 doi:10.1073/pnas.221449198.
22. Duong T, Koopman P, Francois M, (2012) Tumor lymphangiogenesis as a potential therapeutic target. Journal of Oncology 2012: 204946 doi:10.1155/2012/204946.
23. Skobe M, Hawighorst T, Jackson D, Prevo R, Janes L, et al. (2001) Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat Med 7: 192-198 doi:10.1038/84643.
24. 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 doi:10.1038/84635.
25. 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 doi:10.1093/emboj/20.4.672.
26. Hagendoorn J, Tong R, Fukumura D, Lin Q, Lobo J, et al. (2006) Onset of abnormal blood and lymphatic vessel function and interstitial hypertension in early stages of carcinogenesis. Cancer Res 66: 3360-3364 doi:10.1158/0008-5472.CAN-05-2655.
27. Hoshida T, Isaka N, Hagendoorn J, di Tomaso E, Chen Y-L, 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 doi:10.1158/0008-5472.CAN-06-1392.
28. Karnezis T, Shayan R, Caesar C, Roufail S, Harris NC, et al. (2012) VEGF-D Promotes Tumor Metastasis by Regulating Prostaglandins Produced by the Collecting Lymphatic Endothelium. Cancer Cell 21: 181-195 doi:10.1016/j.ccr.2011.12.026.
29. Harrell MI, Iritani BM, Ruddell A, (2007) Tumor-induced sentinel lymph node lymphangiogenesis and increased lymph flow precede melanoma metastasis. Am J Pathol 170: 774-786 doi:10.2353/ajpath.2007.060761.
30. Ruddell A, Harrell MI, Minoshima S, Maravilla KR, Iritani BM, et al. (2008) Dynamic contrast-enhanced magnetic resonance imaging of tumor-induced lymph flow. Neoplasia 10: 706-713.
31. Proulx ST, Luciani P, Derzsi S, Rinderknecht M, Mumprecht V, et al. (2010) Quantitative imaging of lymphatic function with liposomal indocyanine green. Cancer Res 70: 7053-7062 doi:10.1158/0008-5472.CAN-10-0271.
32. He Y, Kozaki K-I, Karpanen T, Koshikawa K, Ylä-Herttuala S, et al. (2002) Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling. J Natl Cancer Inst 94: 819-825.
33. Chen Z, Varney ML, Backora MW, Cowan K, Solheim JC, et al. (2005) Down-regulation of vascular endothelial cell growth factor-C expression using small interfering RNA vectors in mammary tumors inhibits tumor lymphangiogenesis and spontaneous metastasis and enhances survival. Cancer Res 65: 9004-9011 doi:10.1158/0008-5472.CAN-05-0885.
34. Lin J, Lalani AS, Harding TC, Gonzalez M, Wu W-W, et al. (2005) Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor. Cancer Res 65: 6901-6909 doi:10.1158/0008-5472.CAN-05-0408.
35. Caunt M, Mak J, Liang W-C, Stawicki S, Pan Q, et al. (2008) Blocking neuropilin-2 function inhibits tumor cell metastasis. Cancer Cell 13: 331-342 doi:10.1016/j.ccr.2008.01.029.
36. 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 doi:10.1158/0008-5472.CAN-04-4576.
37. Kwon S, Sevick-Muraca EM, (2010) Functional lymphatic imaging in tumor-bearing mice. J Immunol Methods 360: 167-172 doi:10.1016/j.jim.2010.06.016.
38. Papoutsi M, Sleeman JP, Wilting J, (2001) Interaction of rat tumor cells with blood vessels and lymphatics of the avian chorioallantoic membrane. Microsc Res Tech 55: 100-107 doi:10.1002/jemt.1161.
39. Cohen B, Addadi Y, Sapoznik S, Meir G, Kalchenko V, et al. (2009) Transcriptional regulation of vascular endothelial growth factor C by oxidative and thermal stress is mediated by lens epithelium-derived growth factor/p75. Neoplasia 11: 921-933.
40. Sharma R, Wang W, Rasmussen JC, Joshi A, Houston JP, et al. (2007) Quantitative imaging of lymph function. Am J Physiol Heart Circ Physiol 292: H3109-H3118 doi:10.1152/ajpheart.01223.2006.
41. Rasmussen JC, Tan I-C, Marshall MV, Fife CE, Sevick-Muraca EM, (2009) Lymphatic imaging in humans with near-infrared fluorescence. Curr Opin Biotechnol 20: 74-82 doi:10.1016/j.copbio.2009.01.009.
42. Harrell MI, Iritani BM, Ruddell A, (2008) Lymph node mapping in the mouse. J Immunol Methods 332: 170-174 doi:10.1016/j.jim.2007.11.012.
43. Haiko P, Karkkainem M, Achen M. Growth factors and lymphangiogenesis. In: Ferrara, ed. Angiogenesis: From Basic Science to Clinical Applications. Boca Raton, FL, USA: Taylor & Francis Group 2007: 53-74.
44. Shibuya M. Signal transduction of VEGF receptors toward angiogenesis. In: Ferrara, ed. Angiogenesis: From Basic Science to Clinical Applications. Boca Raton, FL, USA: Taylor & Francis Group 2007: 34-52.
45. Liang W, Wu X, Peale F, Lee C, Meng G, et al. (2006) Cross-species vascular endothelial growth factor (VEGF)-blocking antibodies completely inhibit the growth of human tumor xenografts and measure the contribution of stromal VEGF. J Biol Chem 281: 951-961 doi:10.1074/jbc.M508199200.
46. Wilson N, Yang A, Yang B, Couto S, Stern H, et al. (2012) Proapoptotic Activation of Death Receptor 5 on Tumor Endothelial Cells Disrupts the Vasculature and Reduces Tumor Growth. Cancer Cell 22: 80-90 doi:10.1016/j.ccr.2012.05.014.
47. Senger DR, Connolly DT, Van de Water L, Feder J, Dvorak HF, (1990) Purification and NH2-terminal amino acid sequence of guinea pig tumor-secreted vascular permeability factor. Cancer Res 50: 1774-1778.
48. Pham CD, Roberts TP, van Bruggen N, Melnyk O, Mann J, et al. (1998) Magnetic resonance imaging detects suppression of tumor vascular permeability after administration of antibody to vascular endothelial growth factor. Cancer Invest 16: 225-230.
49. Allen JM, McHale NG, (1986) Neuromuscular transmission in bovine mesenteric lymphatics. Microvascular Research 31: 77-83.
50. Van Helden DF, (1993) Pacemaker potentials in lymphatic smooth muscle of the guinea-pig mesentery. J Physiol (Lond) 471: 465-479.
51. 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 doi:10.1182/blood-2006-05-021758.
52. Planas-Paz L, Cacute BS, Goedecke A, Breier G, Ssler RFA, et al. (2011) Mechanoinduction of lymph vessel expansion. EMBO J 31: 788-804 doi:10.1038/emboj.2011.456.
53. Swartz MA, Lund AW (2012) Lymphatic and interstitial flow in the tumour microenvironment: linking mechanobiology with immunity: 1-10. doi:10.1038/nrc3186.
54. Allegra CJ, Yothers G, O'Connell MJ, Sharif S, Petrelli NJ, et al. (2010) Phase III Trial Assessing Bevacizumab in Stages II and III Carcinoma of the Colon: Results of NSABP Protocol C-08. Journal of Clinical Oncology 29: 11-16 doi:10.1200/JCO.2010.30.0855.
55. Sevick-Muraca EM, Sharma R, Rasmussen JC, Marshall MV, Wendt JA, et al. (2008) Imaging of lymph flow in breast cancer patients after microdose administration of a near-infrared fluorophore: feasibility study. Radiology 246: 734-741 doi:10.1148/radiol.2463070962.
56. Unno N, Nishiyama M, Suzuki M, Yamamoto N, Inuzuka K, et al. (2008) Quantitative lymph imaging for assessment of lymph function using indocyanine green fluorescence lymphography. Eur J Vasc Endovasc Surg 36: 230-236 doi:10.1016/j.ejvs.2008.04.013.
57. Notohamiprodjo M, Baumeister RGH, Jakobs TF, Bauner KU, Boehm HF, et al. (2009) MR-lymphangiography at 3.0 T-a feasibility study. Eur Radiol 19: 2771-2778 doi:10.1007/s00330-009-1461-z.