COX-2 inhibition potentiates antiangiogenic cancer therapy and prevents metastasis in preclinical models

Science Translational Medicine

Volumn 6, Issue 242, 2014, Pages

  Xu, Lihong ^a   Stevens, Janine ^a   Hilton, Mary Beth ^a,b   Seaman, Steven ^a   Conrads, Thomas P ^b,d   Veenstra, Timothy D ^b   Logsdon, Daniel ^b   Morris, Holly ^c   Swing, Deborah A ^c   Patel, Nimit L ^b   Kalen, Joseph ^b   Haines, Diana C ^b   Zudaire, Enrique ^a   St Croix, Brad ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d BETTY AND GUY BEATTY CENTER FOR INTEGRATED RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AXITINIB; BEVACIZUMAB; CD11B ANTIGEN; CD45 ANTIGEN; CELECOXIB; CYCLOOXYGENASE 2; MONOCLONAL ANTIBODY DC101; PROSTAGLANDIN A2; PROSTAGLANDIN E2; PROSTAGLANDIN SYNTHASE; PROSTAGLANDIN SYNTHASE 2; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; ANGIOGENESIS INHIBITOR; CYCLOOXYGENASE 2 INHIBITOR; IMIDAZOLE DERIVATIVE; INDAZOLE DERIVATIVE; PTGS2 PROTEIN, MOUSE; VASCULOTROPIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTIANGIOGENIC THERAPY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BONE MARROW CELL; BREAST CANCER; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CANCER PREVENTION; CANCER SURVIVAL; CARCINOGENICITY; CELL INFILTRATION; COLON CANCER; CONTROLLED STUDY; DISEASE ASSOCIATION; DRUG MECHANISM; DRUG POTENTIATION; ENZYME INHIBITION; HCT116 CELL LINE; HISTOPATHOLOGY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LONG TERM SURVIVAL; METASTASIS; MOLECULAR CLONING; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MONOTHERAPY; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; OVERALL SURVIVAL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SURVIVAL RATE; SURVIVAL TIME; TUMOR VOLUME; TUMOR XENOGRAFT; ADJUVANT THERAPY; ANIMAL; CARCINOGENESIS; CELL CLONE; DRUG EFFECTS; DRUG SCREENING; FEMALE; LIVER NEOPLASMS; MAMMARY NEOPLASMS, EXPERIMENTAL; METABOLISM; PATHOLOGY; SECONDARY; SIGNAL TRANSDUCTION; SURVIVAL; TUMOR CELL LINE; VASCULARIZATION;

ANGIOGENESIS INHIBITORS; ANIMALS; CARCINOGENESIS; CELL LINE, TUMOR; CLONE CELLS; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITORS; DINOPROSTONE; FEMALE; HUMANS; IMIDAZOLES; INDAZOLES; LIVER NEOPLASMS; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; NEOADJUVANT THERAPY; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84903782541     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3008455     Document Type: Article

References (40)

1. R. S. Kerbel, Tumor angiogenesis. N. Engl. J. Med. 358, 2039-2049 (2008).
2. B. Patson, R. B. Cohen, A. J. Olszanski, Pharmacokinetic evaluation of axitinib. Expert Opin. Drug Metab. Toxicol. 8, 259-270 (2012).
3. G. Bergers, D. Hanahan, Modes of resistance to anti-angiogenic therapy. Nat. Rev. Cancer 8, 592-603 (2008).
4. A. Chaudhary, M. B. Hilton, S. Seaman, D. C. Haines, S. Stevenson, P. K. Lemotte, W. R. Tschantz, X. M. Zhang, S. Saha, T. Fleming, B. St Croix, TEM8/ANTXR1 blockade inhibits pathological angiogenesis and potentiates tumoricidal responses against multiple cancer types. Cancer Cell 21, 212-226 (2012).
5. A. Bagri, H. Kouros-Mehr, K. G. Leong, G. D. Plowman, Use of anti-VEGF adjuvant therapy in cancer: Challenges and rationale. Trends Mol. Med. 16, 122-132 (2010).
6. J. M. Ebos, R. S. Kerbel, Antiangiogenic therapy: Impact on invasion, disease progression, and metastasis. Nat. Rev. Clin. Oncol. 8, 210-221 (2011).
7. J. M. Ebos, C. R. Lee, W. Cruz-Munoz, G. A. Bjarnason, J. G. Christensen, R. S. Kerbel, Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 15, 232-239 (2009).
8. M. Pàez-Ribes, E. Allen, J. Hudock, T. Takeda, H. Okuyama, F. Viñals, M. Inoue, G. Bergers, D. Hanahan, O. Casanovas, Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 15, 220-231 (2009).
9. P. S. Steeg, Angiogenesis inhibitors: Motivators of metastasis? Nat. Med. 9, 822-823 (2003).
10. L. M. Ellis, D. A. Reardon, Cancer: The nuances of therapy. Nature 458, 290-292 (2009).
11. J. F. de Groot, G. Fuller, A. J. Kumar, Y. Piao, K. Eterovic, Y. Ji, C. A. Conrad, Tumor invasion after treatment of glioblastoma with bevacizumab: Radiographic and pathologic correlation in humans and mice. Neurol. Oncol. 12, 233-242 (2010).
12. C. Fischer, B. Jonckx, M. Mazzone, S. Zacchigna, S. Loges, L. Pattarini, E. Chorianopoulos, L. Liesenborghs, M. Koch, M. De Mol, M. Autiero, S. Wyns, S. Plaisance, L. Moons, N. van Rooijen, M. Giacca, J. M. Stassen, M. Dewerchin, D. Collen, P. Carmeliet, Anti-PlGF inhibits growth of VEGF(R)-inhibitor-resistant tumors without affecting healthy vessels. Cell 131, 463-475 (2007).
13. L. Yang, L. M. DeBusk, K. Fukuda, B. Fingleton, B. Green-Jarvis, Y. Shyr, L. M. Matrisian, D. P. Carbone, P. C. Lin, Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 6, 409-421 (2004).
14. G. Milligan, F. Marshall, S. Rees, G 16 as a universal G protein adapter: Implications for agonist screening strategies. Trends Pharmacol. Sci. 17, 235-237 (1996).
15. M. Sahin, E. Sahin, S. Gümüslü, Cyclooxygenase-2 in cancer and angiogenesis. Angiology 60, 242-253 (2009).
16. P. Sinha, V. K. Clements, A. M. Fulton, S. Ostrand-Rosenberg, Prostaglandin E2 promotes tumor progression by inducing myeloid-derived suppressor cells. Cancer Res. 67, 4507-4513 (2007).
17. D. T. Dang, F. Chen, L. B. Gardner, J. M. Cummins, C. Rago, F. Bunz, S. V. Kantsevoy, L. H. Dang, Hypoxia-inducible factor-1α promotes nonhypoxia-mediated proliferation in colon cancer cells and xenografts. Cancer Res. 66, 1684-1936 (2006).
18. D. T. Dang, S. Y. Chun, K. Burkitt, M. Abe, S. Chen, P. Havre, N. J. Mabjeesh, E. I. Heath, N. J. Vogelzang, M. Cruz-Correa, D. W. Blayney, W. D. Ensminger, B. St Croix, N. H. Dang, L. H. Dang, Hypoxia-inducible factor-1 target genes as indicators of tumor vessel response to vascular endothelial growth factor inhibition. Cancer Res. 68, 1872-1880 (2008).
19. G. Wu, J. Luo, J. S. Rana, R. Laham, F. W. Sellke, J. Li, Involvement of COX-2 in VEGF-induced angiogenesis via P38 and JNK pathways in vascular endothelial cells. Cardiovasc. Res. 69, 512-519 (2006).
20. 2 is mediated by hypoxia-inducible factor 1. Cancer Res. 63, 2330-2334 (2003).
21. R. Wu, A. L. Abramson, M. J. Shikowitz, A. J. Dannenberg, B. M. Steinberg, Epidermal growth factor-induced cyclooxygenase-2 expression is mediated through phosphatidylinositol-3 kinase, not mitogen-activated protein/extracellular signal-regulated kinase kinase, in recurrent respiratory papillomas. Clin. Cancer Res. 11, 6155-6161 (2005).
22. J. R. Vane, R. M. Botting, The mechanism of action of aspirin. Thromb. Res. 110, 255-258 (2003).
23. A. Ristimäki, A. Sivula, J. Lundin, M. Lundin, T. Salminen, C. Haglund, H. Joensuu, J. Isola, Prognostic significance of elevated cyclooxygenase-2 expression in breast cancer. Cancer Res. 62, 632-635 (2002).
24. C. E. Eberhart, R. J. Coffey, A. Radhika, F. M. Giardiello, S. Ferrenbach, R. N. DuBois, Upregulation of cyclooxygenase 2 gene expression in human colorectal adenomas and adenocarcinomas. Gastroenterology 107, 1183-1188 (1994).
25. K. Krysan, K. L. Reckamp, S. Sharma, S. M. Dubinett, The potential and rationale for COX-2 inhibitors in lung cancer. Anticancer Agents Med. Chem. 6, 209-220 (2006).
26. R. E. Harris, Cyclooxygenase-2 (cox-2) blockade in the chemoprevention of cancers of the colon, breast, prostate, and lung. Inflammopharmacology 17, 55-67 (2009).
27. E. Van Cutsem, D. Lambrechts, H. Prenen, R. K. Jain, P. Carmeliet, Lessons from the adjuvant bevacizumab trial on colon cancer: What next? J. Clin. Oncol. 29, 1-4 (2011).
28. B. Oyan, Why do targeted agents not work in the adjuvant setting in colon cancer? Expert Rev. Anticancer Ther. 12, 1337-1345 (2012).
29. C. J. Allegra, G. Yothers, M. J. O'Connell, S. Sharif, N. J. Petrelli, S. H. Lopa, N. Wolmark, Bevacizumab in stage II-III colon cancer: 5-year update of the National Surgical Adjuvant Breast and Bowel Project C-08 trial. J. Clin. Oncol. 31, 359-364 (2013).
30. G. Francia, W. Cruz-Munoz, S. Man, P. Xu, R. S. Kerbel, Mouse models of advanced spontaneous metastasis for experimental therapeutics. Nat. Rev. Cancer 11, 135-141 (2011).
31. C. P. Day, J. Carter, C. Bonomi, M. Hollingshead, G. Merlino, Preclinical therapeutic response of residual metastatic disease is distinct from its primary tumor of origin. Int. J. Cancer 130, 190-199 (2012).
32. T. P. Padera, A. H. Kuo, T. Hoshida, S. Liao, J. Lobo, K. R. Kozak, D. Fukumura, R. K. Jain, Differential response of primary tumor versus lymphatic metastasis to VEGFR-2 and VEGFR-3 kinase inhibitors cediranib and vandetanib. Mol. Cancer Ther. 7, 2272-2279 (2008).
33. G. C. Jayson, D. J. Hicklin, L. M. Ellis, Antiangiogenic therapy - Evolving view based on clinical trial results. Nat. Rev. Clin. Oncol. 9, 297-303 (2012).
34. X. Liao, P. Lochhead, R. Nishihara, T. Morikawa, A. Kuchiba, M. Yamauchi, Y. Imamura, Z. R. Qian, Y. Baba, K. Shima, R. Sun, K. Nosho, J. A. Meyerhardt, E. Giovannucci, C. S. Fuchs, A. T. Chan, S. Ogino, Aspirin use, tumor PIK3CA mutation, and colorectal-cancer survival. N. Engl. J. Med. 367, 1596-1606 (2012).
35. T. Grosser, Y. Yu, G. A. Fitzgerald, Emotion recollected in tranquility: Lessons learned from the COX-2 saga. Annu. Rev. Med. 61, 17-33 (2010).
36. M. M. Bertagnolli, C. J. Eagle, A. G. Zauber, M. Redston, A. Breazna, K. Kim, J. Tang, R. B. Rosenstein, A. Umar, D. Bagheri, N. T. Collins, J. Burn, D. C. Chung, T. Dewar, T. R. Foley, N. Hoffman, F. Macrae, R. E. Pruitt, J. R. Saltzman, B. Salzberg, T. Sylwestrowicz, E. T. Hawk; Adenoma Prevention with Celecoxib Study Investigators, Five-year efficacy and safety analysis of the Adenoma Prevention with Celecoxib Trial. Cancer Prev. Res. 2, 310-321 (2009).
37. S. D. Solomon, J. Wittes, P. V. Finn, R. Fowler, J. Viner, M. M. Bertagnolli, N. Arber, B. Levin, C. L. Meinert, B. Martin, J. L. Pater, P. E. Goss, P. Lance, S. Obara, E. Y. Chew, J. Kim, G. Arndt, E. Hawk; Cross Trial Safety Assessment Group, Cardiovascular risk of celecoxib in 6 randomized placebo-controlled trials: The cross trial safety analysis. Circulation 117, 2104-2113 (2008).
38. D. J. Graham, D. Campen, R. Hui, M. Spence, C. Cheetham, G. Levy, S. Shoor, W. A. Ray, Risk of acute myocardial infarction and sudden cardiac death in patients treated with cyclo-oxygenase 2 selective and non-selective non-steroidal anti-inflammatory drugs: Nested case-control study. Lancet 365, 475-481 (2005).
39. D. Wang, R. N. DuBois, The role of anti-inflammatory drugs in colorectal cancer. Annu. Rev. Med. 64, 131-144 (2013).
40. J. M. Reichert, Antibodies to watch in 2013: Mid-year update. MAbs 5, 513-517 (2013).