Suppression of prostate cancer nodal and systemic metastasis by blockade of the lymphangiogenic axis

Cancer Research

Volumn 68, Issue 19, 2008, Pages 7828-7837

  Burton, Jeremy B ^a   Priceman, Saul J ^a   Sung, James L ^a   Brakenhielm, Ebba ^a,b   Dong, Sung An ^a   Pytowski, Bronislaw ^c   Alitalo, Kari ^d   Wu, Lily ^a,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Rouen Medico Pharmacological University   (France)

^c ELI LILLY AND COMPANY   (United States)

^d HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; ANTIMETASTATIC AGENT; MONOCLONAL ANTIBODY DC101; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL GROWTH FACTOR C LIGAND TRAP; VASCULOTROPIN RECEPTOR 3 ANTIBODY;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL; CANCER GROWTH; CANCER INHIBITION; CAPILLARY DENSITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; LUNG METASTASIS; LYMPH NODE METASTASIS; LYMPHANGIOGENESIS; MALE; METASTASIS; METASTASIS INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; TREATMENT OUTCOME; TUMOR VASCULARIZATION; TUMOR XENOGRAFT;

ANIMALS; GENE THERAPY; HUMANS; IMMUNOTHERAPY; LENTIVIRUS; LUNG NEOPLASMS; LYMPH NODES; LYMPHANGIOGENESIS; LYMPHATIC METASTASIS; MALE; MICE; MICE, SCID; NEOVASCULARIZATION, PATHOLOGIC; PROSTATIC NEOPLASMS; SOLUBILITY; TUMOR CELLS, CULTURED; VASCULAR ENDOTHELIAL GROWTH FACTOR C; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 54249140119     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-1488     Document Type: Article

References (44)

1. Jemal A, Siegel R, Ward E, et al. Cancer statistics, 2008. CA Cancer J Clin 2008;58:71-96.
2. Roehl KA, Han M, Ramos CG, Antenor JA, Catalona WJ. Cancer progression and survival rates following anatomical radical retropubic prostatectomy in 3,478 consecutive patients: long-term results. J Urol 2004;172:910-4.
3. Allaf ME, Palapattu GS, Trock BJ, Carter HB, Walsh PC. Anatomical extent of lymph node dissection: impact on men with clinically localized prostate cancer. J Urol 2004;172:1840-4.
4. D'Amico AV, Whittington R, Malkowicz SB, et al. Pretreatment nomogram for prostate-specific antigen recurrence after radical prostatectomy or external-beam radiation therapy for clinically localized prostate cancer. J Clin Oncol 1999;17:168-72.
5. Folkman J, Merler E, Abernathy C, Williams G. Isolation of a tumor factor responsible for angiogenesis. J Exp Med 1971;133:275-88.
6. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003;9:669-76.
7. Carmeliet P. Angiogenesis in health and disease. Nat Med 2003;9:653-60.
8. Klement G, Baruchel S, Rak J, et al. Continuous low-dose therapy with vinblastine and VEGF receptor-2 antibody induces sustained tumor regression without overt toxicity. J Clin Invest 2000;105:R15-24.
9. Lee CG, Heijn M, di Tomaso E, et al. Anti-Vascular endothelial growth factor treatment augments tumor radiation response under normoxic or hypoxic conditions. Cancer Res 2000;60:5565-70.
10. Jeltsch M, Kaipainen A, Joukov V, et al. Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science 1997;276:1423-5.
11. Veikkola T, Jussila L, Makinen T, et al. Signalling via vascular endothelial growth factor receptor-3 is sufficient for lymphangiogenesis in transgenic mice. EMBO J 2001;20:1223-31.
12. He Y, Kozaki K, Karpanen T, et al. Suppression of tumor lymphangiogenesis and lymph node metastasis by blocking vascular endothelial growth factor receptor 3 signaling. J Natl Cancer Inst 2002;94:819-25.
13. Mattila MM, Ruohola JK, Karpanen T, Jackson DG, Alitalo K, Harkonen PL. VEGF-C induced lymphangiogenesis is associated with lymph node metastasis in orthotopic MCF-7 tumors. Int J Cancer 2002;98:946-51.
14. Mandriota SJ, Jussila L, Jeltsch M, et al. Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis. EMBO J 2001;20:672-82.
15. Nagy JA, Vasile E, Feng D, et al. Vascular permeability factor/vascular endothelial growth factor induces lymphangiogenesis as well as angiogenesis. J Exp Med 2002;196:1497-506.
16. Bjorndahl MA, Cao R, Burton JB, et al. Vascular endothelial growth factor-a promotes peritumoral lymphangiogenesis and lymphatic metastasis. Cancer Res 2005;65:9261-8.
17. Hirakawa S, Kodama S, Kunstfeld R, Kajiya K, Brown LF, Detmar M. VEGF-A induces tumor and sentinel lymph node lymphangiogenesis and promotes lymphatic metastasis. J Exp Med 2005;201:1089-99.
18. Zeng Y, Opeskin K, Baldwin ME, et al. Expression of vascular endothelial growth factor receptor-3 by lymphatic endothelial cells is associated with lymph node metastasis in prostate cancer. Clin Cancer Res 2004;10:5137-44.
19. Yang J, Wu HF, Qian LX, et al. Increased expressions of vascular endothelial growth factor (VEGF), VEGF-C and VEGF receptor-3 in prostate cancer tissue are associated with tumor progression. Asian J Androl 2006;8:169-75.
20. Jennbacken K, Vallbo C, Wang W, Damber JE. Expression of vascular endothelial growth factor C (VEGF-C) and VEGF receptor-3 in human prostate cancer is associated with regional lymph node metastasis. Prostate 2005;65:110-6.
21. Roma AA, Magi-Galluzzi C, Kral MA, Jin TT, Klein EA, Zhou M. Peritumoral lymphatic invasion is associated with regional lymph node metastases in prostate adenocarcinoma. Mod Pathol 2006;19:392-8.
22. Brakenhielm E, Burton JB, Johnson M, et al. Modulating metastasis by a lymphangiogenic switch in prostate cancer. Int J Cancer 2007;121:2153-61.
23. Wong SY, Haack H, Crowley D, Barry M, Bronson RT, Hynes RO. Tumor-secreted vascular endothelial growth factor-C is necessary for prostate cancer lymphangiogenesis, but lymphangiogenesis is unnecessary for lymph node metastasis. Cancer Res 2005;65:9789-98.
24. Roberts N, Kloos B, Cassella M, et al. Inhibition of VEGFR-3 activation with the antagonistic antibody more potently suppresses lymph node and distant metastases than inactivation of VEGFR-2. Cancer Res 2006;66:2650-7.
25. An DS, Xie Y, Mao SH, Morizono K, Kung SK, Chen IS. Efficient lentiviral vectors for short hairpin RNA delivery into human cells. Hum Gene Ther 2003;14:1207-12.
26. Sato M, Figueiredo ML, Burton JB, et al. Configurations of a two-tiered amplified gene expression system in adenoviral vectors designed to improve the specificity of in vivo prostate cancer imaging. Gene Ther 2008;8:583-93.
27. Loening AM, Gambhir SS. AMIDE: a free software tool for multimodality medical image analysis. Mol Imaging 2003;2:131-7.
28. Pytowski B, Goldman J, Persaud K, et al. Complete and specific inhibition of adult lymphatic regeneration by a novel VEGFR-3 neutralizing antibody. J Natl Cancer Inst 2005;97:14-21.
29. Witte L, Hicklin DJ, Zhu Z, et al. Monoclonal antibodies targeting the VEGF receptor-2 (Flk1/KDR) as an anti-angiogenic therapeutic strategy. Cancer Metastasis Rev 1998;17:155-61.
30. Cao R, Brakenhielm E, Pawliuk R, et al. Angiogenic synergism, vascular stability and improvement of hindlimb ischemia by a combination of PDGF-BB and FGF-2. Nat Med 2003;9:604-13.
31. Klein KA, Reiter RE, Redula J, et al. Progression of metastatic human prostate cancer to androgen independence in immunodeficient SCID mice. Nat Med 1997;3:402-8.
32. Joukov V, Kumar V, Sorsa T, et al. A recombinant mutant vascular endothelial growth factor-C that has lost vascular endothelial growth factor receptor-2 binding, activation, and vascular permeability activities. J Biol Chem 1998;273:6599-602.
33. Holleran JL, Miller CJ, Culp LA. Tracking micrometastasis to multiple organs with lacZ-tagged CWR22R prostate carcinoma cells. J Histochem Cytochem 2000;48:643-51.
34. De Wever O, Mareel M. Role of tissue stroma in cancer cell invasion. J Pathol 2003;200:429-47.
35. Joukov V, Pajusola K, Kaipainen A, et al. 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 1996;15:290-8.
36. Zhao H, Doyle TC, Coquoz O, Kalish F, Rice BW, Contag CH. Emission spectra of bioluminescent reporters and interaction with mammalian tissue determine the sensitivity of detection in vivo. J Biomed Opt 2005;10:41210.
37. Skobe M, Hawighorst T, Jackson DG, et al. Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat Med 2001;7:192-8.
38. Karpanen T, Egeblad M, Karkkainen MJ, et al. Vascular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth. Cancer Res 2001;61:1786-90.
39. Alitalo K, Carmeliet P. Molecular mechanisms of lymphangiogenesis in health and disease. Cancer Cell 2002;1:219-27.
40. Lin J, Lalani AS, Harding TC, et al. Inhibition of lymphogenous metastasis using adeno-associated virus-mediated gene transfer of a soluble VEGFR-3 decoy receptor. Cancer Res 2005;65:6901-9.
41. Laakkonen P, Waltari M, Holopainen T, et al. Vascular endothelial growth factor receptor 3 is involved in tumor angiogenesis and growth. Cancer Res 2007;67:593-9.
42. Jain RK. Barriers to drug delivery in solid tumors. Sci Am 1994;271:58-65.
43. Padera TP, Kadambi A, di Tomaso E, et al. Lymphatic metastasis in the absence of functional intratumor lymphatics. Science 2002;296:1883-6.
44. Burton JB, Johnson M, Sato M, et al. Adenovirus mediated gene expression imaging to directly detect sentinel lymph node metastasis of prostate cancer. Nat Med 2008;14:882-8.