Inhibition of c-met reduces lymphatic metastasis in RIP-Tag2 transgenic mice

Cancer Research

Volumn 73, Issue 12, 2013, Pages 3692-3703

  Sennino, Barbara ^a   Ishiguro Oonuma, Toshina ^a,c   Schriver, Brian J ^a   Christensen, James G ^b   McDonald, Donald M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b PFIZER GLOBAL RESEARCH AND DEVELOPMENT   (United States)

^c EHIME UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE RECEPTOR ANTAGONIST; PF 04217903; SCATTER FACTOR RECEPTOR; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; LYMPH NODE METASTASIS; MOUSE; NONHUMAN; PANCREATIC NEUROENDOCRINE TUMOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; TUMOR CELL;

ANIMALS; ANTIBODIES; ANTINEOPLASTIC AGENTS; GENE EXPRESSION REGULATION, NEOPLASTIC; IMMUNOHISTOCHEMISTRY; INDOLES; LYMPHATIC METASTASIS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; PANCREATIC NEOPLASMS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-MET; PYRAZINES; PYRROLES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRIAZOLES; VASCULAR ENDOTHELIAL GROWTH FACTOR C;

EID: 84879114193     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-2160     Document Type: Article

References (60)

1. Cao Y. Opinion: emerging mechanisms of tumour lymphangiogenesis and lymphatic metastasis. Nat Rev Cancer 2005;5:735-43. (Pubitemid 41486366)
2. Mandriota SJ, Jussila L, Jeltsch M, Compagni A, Baetens D, Prevo R, et al. Vascular endothelial growth factor-C-mediated lymphangiogenesis promotes tumour metastasis. EMBO J 2001;20:672-82. (Pubitemid 32167632)
3. Skobe M, Hawighorst T, Jackson DG, Prevo R, Janes L, Velasco P, et al. Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat Med 2001;7:192-8. (Pubitemid 32148486)
4. Stacker SA, Caesar C, Baldwin ME, Thornton GE, Williams RA, Prevo R, et al. VEGF-D promotes the metastatic spread of tumor cells via the lymphatics. Nat Med 2001;7:186-91. (Pubitemid 32148485)
5. Casanovas O, Hicklin DJ, Bergers G, Hanahan D. Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell 2005;8:299-309. (Pubitemid 41443415)
6. Ebos JM, Lee CR, Cruz-Munoz W, Bjarnason GA, Christensen JG, Kerbel RS. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 2009;15:232-9.
7. Paez-Ribes M, Allen E, Hudock J, Takeda T, Okuyama H, Vinals F, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009;15: 220-31.
8. Sennino B, Ishiguro-Oonuma T, Wei Y, Naylor RM, Williamson CW, Bhagwandin V, et al. Suppression of tumor invasion and metastasis by concurrent inhibition of c-Met and VEGF signaling in pancreatic neuroendocrine tumors. Cancer Discov 2012;2:1-18.
9. Pennacchietti S, Michieli P, Galluzzo M, Mazzone M, Giordano S, Comoglio PM. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell 2003;3:347-61. (Pubitemid 38340304)
10. Benvenuti S, Comoglio PM. The MET receptor tyrosine kinase in invasion and metastasis. J Cell Physiol 2007;213:316-25. (Pubitemid 47509708)
11. Christensen J, Anderes K. Beyond VEGF: targeting tumor growth and angiogenesis via alternative mechanisms. Adv ExpMed Biol 2008;610: 43-53.
12. Gherardi E, Birchmeier W, Birchmeier C, Vande Woude G. Targeting MET in cancer: rationale and progress. Nat Rev Cancer 2012;12: 89-103.
13. Graveel CR, DeGroot JD, Su Y, Koeman J, Dykema K, Leung S, et al. Met induces diverse mammary carcinomas in mice and is associated with human basal breast cancer. Proc Natl Acad Sci U S A 2009;106: 12909-14.
14. Ghoussoub RA, Dillon DA, D'Aquila T, Rimm EB, Fearon ER, Rimm DL. Expression of c-met is a strong independent prognostic factor in breast carcinoma. Cancer 1998;82:1513-20. (Pubitemid 28164998)
15. Kong DS, Song SY, Kim DH, Joo KM, Yoo JS, Koh JS, et al. Prognostic significance of c-Met expression in glioblastomas. Cancer 2009;115: 140-8.
16. Sawada K, Radjabi AR, Shinomiya N, Kistner E, Kenny H, Becker AR, et al. c-Met overexpression is a prognostic factor in ovarian cancer and an effective target for inhibition of peritoneal dissemination and invasion. Cancer Res 2007;67:1670-9. (Pubitemid 46383393)
17. Lai AZ, Abella JV, Park M. Crosstalk in Met receptor oncogenesis. Trends Cell Biol 2009;19:542-51.
18. Cao R, Bjorndahl MA, Gallego MI, Chen S, Religa P, Hansen AJ, et al. Hepatocyte growth factor is a lymphangiogenic factor with an indirect mechanism of action. Blood 2006;107:3531-6.
19. 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. (Pubitemid 43079892)
20. Christensen JG. A preclinical review of sunitinib, a multitargeted receptor tyrosine kinase inhibitor with anti-angiogenic and antitumour activities. Ann Oncol 2007;18 Suppl 10:x3-10.
21. Timofeevski SL, McTigue MA, Ryan K, Cui J, Zou HY, Zhu JX, et al. Enzymatic characterization of c-Met receptor tyrosine kinase oncogenic mutants and kinetic studies with aminopyridine and triazolopyrazine inhibitors. Biochemistry 2009;48:5339-49.
22. Hanahan D. Heritable formation of pancreatic beta-cell tumours in transgenicmice expressing recombinant insulin/simian virus 40 oncogenes. Nature 1985;315:115-22. (Pubitemid 15064530)
23. Inai T, Mancuso M, Hashizume H, Baffert F, Haskell A, Baluk P, et al. Inhibition of vascular endothelial growth factor (VEGF) signaling in cancer causes loss of endothelial fenestrations, regression of tumor vessels, and appearance of basement membrane ghosts. Am J Pathol 2004;165:35-52. (Pubitemid 38821812)
24. Van den Broeck W, Derore A, Simoens P. Anatomy and nomenclature of murine lymph nodes: descriptive study and nomenclatory standardization in BALB/cAnNCrl mice. J Immunol Methods 2006;312: 12-9. (Pubitemid 43795993)
25. Dadras SS, Lange-Asschenfeldt B, Velasco P, Nguyen L, Vora A, Muzikansky A, et al. Tumor lymphangiogenesis predicts melanoma metastasis to sentinel lymph nodes. Mod Pathol 2005;18:1232-42. (Pubitemid 43079923)
26. Hall FT, Freeman JL, Asa SL, Jackson DG, Beasley NJ. Intratumoral lymphatics and lymph node metastases in papillary thyroid carcinoma. Arch Otolaryngol Head Neck Surg 2003;129:716-9. (Pubitemid 36858956)
27. Baluk P, McDonald DM. Markers for microscopic imaging of lymphangiogenesis and angiogenesis. Ann N Y Acad Sci 2008;1131:1-12. (Pubitemid 351758499)
28. Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, Tamaki K, et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2000;2:737-44.
29. Ferrara N, Mass RD, Campa C, Kim R. Targeting VEGF-A to treat cancer and age-related macular degeneration. Annu Rev Med 2007;58:491-504. (Pubitemid 46706529)
30. Bruns CJ, Liu W, Davis DW, Shaheen RM, McConkey DJ, Wilson MR, et al. Vascular endothelial growth factor is an in vivo survival factor for tumor endothelium in a murine model of colorectal carcinoma liver metastases. Cancer 2000;89:488-99. (Pubitemid 30640095)
31. Mendel DB, Laird AD, Xin X, Louie SG, Christensen JG, Li G, et al. In vivo antitumor activity of SU11248, a novel tyrosine kinase inhibitor targeting vascular endothelial growth factor and platelet-derived growth factor receptors: determination of a pharmacokinetic/pharmacodynamic relationship. Clin Cancer Res 2003;9:327-37. (Pubitemid 36109749)
32. Eckerich C, Zapf S, Fillbrandt R, Loges S, Westphal M, Lamszus K. Hypoxia can induce c-Met expression in glioma cells and enhance SF/HGF-induced cell migration. Int J Cancer 2007;121:276-83. (Pubitemid 46917695)
33. Hayashi M, Sakata M, Takeda T, Tahara M, Yamamoto T, Okamoto Y, et al. Up-regulation of c-met protooncogene product expression through hypoxia-inducible factor-1alpha is involved in trophoblast invasion under low-oxygen tension. Endocrinology 2005;146: 4682-9. (Pubitemid 41446605)
34. Maula SM, Luukkaa M, Grenman R, Jackson D, Jalkanen S, Ristamaki R. Intratumoral lymphatics are essential for the metastatic spread and prognosis in squamous cell carcinomas of the head and neck region. Cancer Res 2003;63:1920-6. (Pubitemid 36460859)
35. Lee K, Park do J, Choe G, Kim HH, Kim WH, Lee HS. Increased intratumoral lymphatic vessel density correlates with lymph node metastasis in early gastric carcinoma. Ann Surg Oncol 2010;17:73-80.
36. Petrova TV, Nykanen A, Norrmen C, Ivanov KI, Andersson LC, Haglund C, et al. Transcription factor PROX1 induces colon cancer progression by promoting the transition from benign to highly dysplastic phenotype. Cancer Cell 2008;13:407-19. (Pubitemid 351609440)
37. 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. (Pubitemid 40524677)
38. Lohela M, Bry M, Tammela T, Alitalo K. VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. Curr Opin Cell Biol 2009;21:154-65.
39. Tammela T, Alitalo K. Lymphangiogenesis: molecular mechanisms and future promise. Cell 2010;140:460-76.
40. Partanen TA, Arola J, Saaristo A, Jussila L, Ora A, Miettinen M, et al. VEGF-C and VEGF-D expression in neuroendocrine cells and their receptor, VEGFR-3, in fenestrated blood vessels in human tissues. FASEB J 2000;14:2087-96.
41. Roberts N, Kloos B, Cassella M, Podgrabinska S, Persaud K, Wu Y, 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.
42. Kodera Y, Katanasaka Y, Kitamura Y, Tsuda H, Nishio K, Tamura T, et al. Sunitinib inhibits lymphatic endothelial cell functions and lymph node metastasis in a breast cancer model through inhibition of vascular endothelial growth factor receptor 3. Breast Cancer Res 2011; 13:R66.
43. Hong YK, Lange-Asschenfeldt B, Velasco P, Hirakawa S, Kunstfeld R, Brown LF, et al. VEGF-A promotes tissue repair-associated lymphatic vessel formation via VEGFR-2 and the alpha1beta1 and alpha2beta1 integrins. FASEB J 2004;18:1111-3. (Pubitemid 39561540)
44. Maione F, Capano S, Regano D, Zentilin L, Giacca M, Casanovas O, et al. Semaphorin 3A overcomes cancer hypoxia and metastatic dissemination induced by antiangiogenic treatment in mice. J Clin Invest 2012;122:1832-48.
45. Singh M, Couto SS, Forrest WF, Lima A, Cheng JH, Molina R, et al. Anti-VEGF antibody therapy does not promote metastasis in genetically engineered mouse tumor models. J Pathol 2012;227:417-30.
46. Chung AS, Kowanetz M, Wu X, Zhuang G, Ngu H, Finkle D, et al. Differential drug-class specific metastatic effects following treatment with a panel of angiogenesis inhibitors. J Pathol 2012;227:404-16.
47. Skobe M, Rockwell P, Goldstein N, Vosseler S, Fusenig NE. Halting angiogenesis suppresses carcinoma cell invasion. Nat Med 1997;3: 1222-7. (Pubitemid 27508822)
48. Mazzone M, Basilico C, Cavassa S, Pennacchietti S, Risio M, Naldini L, et al. An uncleavable form of pro-scatter factor suppresses tumor growth and dissemination in mice. J Clin Invest 2004;114:1418-32. (Pubitemid 40385573)
49. Christensen JG, Zou HY, Arango ME, Li Q, Lee JH, McDonnell SR, et al. Cytoreductive antitumor activity of PF-2341066, a novel inhibitor of anaplastic lymphoma kinase and c-Met, in experimental models of anaplastic large-cell lymphoma. Mol Cancer Ther 2007;6:3314-22.
50. Jin H, Yang R, Zheng Z, Romero M, Ross J, Bou-Reslan H, et al. MetMAb, the one-armed 5D5 anti-c-Met antibody, inhibits orthotopic pancreatic tumor growth and improves survival. Cancer Res 2008; 68:4360-8.
51. Puri N, Ahmed S, Janamanchi V, Tretiakova M, Zumba O, Krausz T, et al. c-Met is a potentially new therapeutic target for treatment of human melanoma. Clin Cancer Res 2007;13:2246-53. (Pubitemid 46649894)
52. Yakes FM, Chen J, Tan J, Yamaguchi K, Shi Y, Yu P, et al. Cabozantinib (XL184), a novel MET and VEGFR2 inhibitor, simultaneously suppresses metastasis, angiogenesis, and tumor growth. Mol Cancer Ther 2011;10:2298-308.
53. Hussain M, Smith MR, Sweeney C, Corn PG, Elfiky A, Gordon MS, et al. Cabozantinib (XL184) in metastatic castration-resistant prostate cancer (mCRPC): results from a phase II randomized discontinuation trial. J Clin Oncol. 29, 2011 (suppl; abstr 4516.
54. Lennerz JK, Kwak EL, Ackerman A, Michael M, Fox SB, Bergethon K, et al. MET amplification identifies a small and aggressive subgroup of esophagogastric adenocarcinoma with evidence of responsiveness to crizotinib. J Clin Oncol 2011;29:4803-10.
55. Catenacci DV, Henderson L, Xiao SY, Patel P, Yauch RL, Hegde P, et al. Durable complete response of metastatic gastric cancer with anti-Met therapy followed by resistance at recurrence. Cancer Discov 2011;1:573-9.
56. Surati M, Patel P, Peterson A, Salgia R. Role of MetMAb (OA-5D5) in c-MET active lung malignancies. Expert Opin Biol Ther 2011;11: 1655-62.
57. Lee RJ, Smith MR. Targeting MET and vascular endothelial growth factor receptor signaling in castration-resistant prostate cancer. Cancer J 2013;19:90-8.
58. Traynor K. Cabozantinib approved for advanced medullary thyroid cancer. Am J Health Syst Pharm 2013;70:88.
59. Santoro A, Rimassa L, Borbath I, Daniele B, Salvagni S, Van Laethem JL, et al. Tivantinib for second-line treatment of advanced hepatocellular carcinoma: a randomised, placebo-controlled phase 2 study. Lancet Oncol 2013;14:55-63.
60. You WK, Sennino B, Williamson CW, Falcon B, Hashizume H, Yao LC, et al. VEGF and c-Met blockade amplify angiogenesis inhibition in pancreatic islet cancer. Cancer Res 2011;71:4758-68.