Anti-VEGF treatment-resistant pancreatic cancers secrete proinflammatory factors that contribute to malignant progression by inducing an EMT cell phenotype

Clinical Cancer Research

Volumn 17, Issue 17, 2011, Pages 5822-5832

  Carbone, Carmine ^a   Moccia, Tania ^a   Zhu, Cihui ^b   Paradiso, Genni ^a   Budillon, Alfredo ^a   Chiao, Paul J ^b   Abbruzzese, James L ^b   Melisi, Davide ^a,b  

^a NATIONAL CANCER INSTITUTE   (Italy)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BEVACIZUMAB; CD11B ANTIGEN; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CXCL3 CHEMOKINE; CYTOKINE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1BETA; INTERLEUKIN 8; JAGGED1; PROTEIN ADM; PROTEIN ANGPTL2; PROTEIN MDK; PROTEIN TYMP; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOCRINE EFFECT; BONE MARROW CELL; CANCER GROWTH; CARCINOGENESIS; CELL STIMULATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENOME ANALYSIS; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; PANCREAS CANCER; PARACRINE SIGNALING; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIGENS, CD11B; CELL LINE, TUMOR; CHEMOKINES; CYTOKINES; DISEASE PROGRESSION; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MICE; MICE, NUDE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PANCREATIC NEOPLASMS; TRANSPLANTATION, HETEROLOGOUS; TUMOR ESCAPE; TUMOR MARKERS, BIOLOGICAL; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 80052453669     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-11-1185     Document Type: Article

References (44)

1. Hanahan D., Weinberg R.A. Hallmarks of cancer: The next generation. Cell 2011;144:646-674
2. Ellis L.M., Hicklin D.J. VEGF-targeted therapy: Mechanisms of antitumour activity. Nat Rev Cancer 2008;8:579-591
3. Ocana A., Amir E., Vera F., Eisenhauer E.A., Tannock I.F. Addition of bevacizumab to chemotherapy for treatment of solid tumors: Similar results but different conclusions. J Clin Oncol 2011;29:254-256
4. Van Cutsem E., Vervenne W.L., Bennouna J., Humblet Y., Gill S., Van Laethem J.L., et al. Phase III trial of bevacizumab in combination with gemcitabine and erlotinib in patients with metastatic pancreatic cancer. J Clin Oncol 2009;27:2231-2237
5. Duda D.G., Ancukiewicz M., Jain R.K. Biomarkers of antiangiogenic therapy: How do we move from candidate biomarkers to valid biomarkers? J Clin Oncol 2010;28:183-185
6. Jain R.K., Duda D.G., Willett C.G., Sahani D.V., Zhu A.X., Loeffler J.S., et al. Biomarkers of response and resistance to antiangiogenic therapy. Nat Rev Clin Oncol 2009;6:327-338
7. Jubb A.M., Harris A.L. Biomarkers to predict the clinical efficacy of bevacizumab in cancer. Lancet Oncol 2010;11:1172-1183
8. Van Cutsem E., Lambrechts D., Prenen H., Jain R.K., Carmeliet P. Lessons from the adjuvant bevacizumab trial on colon cancer: What next? J Clin Oncol 2011;29:1-4.
9. Brower V. How well do angiogenesis inhibitors work? Biomarkers of response prove elusive. J Natl Cancer Inst 2009;101:846-847
10. Bergers G., Hanahan D. Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer 2008;8:592-603.
11. Crawford Y., Ferrara N. Tumor and stromal pathways mediating refractoriness/resistance to anti-angiogenic therapies. Trends Pharmacol Sci 2009;30:624-630
12. Casanovas O., Hicklin D.J., 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)
13. Crawford Y., Kasman I., Yu L., Zhong C., Wu X., Modrusan Z., et al. PDGFC mediates the angiogenic and tumorigenic properties of fibroblasts associated with tumors refractory to anti-VEGF treatment. Cancer Cell 2009;15:21-34.
14. Shojaei F., Ferrara N. Refractoriness to antivascular endothelial growth factor treatment: Role of myeloid cells. Cancer Res 2008;68:5501-5504
15. Butler J.M., Kobayashi H., Rafii S. Instructive role of the vascular niche in promoting tumour growth and tissue repair by angiocrine factors. Nat Rev Cancer 2010;10:138-146
16. Melisi D., Ossovskaya V., Zhu C., Rosa R., Ling J., Dougherty P.M., et al. Oral poly(ADP-ribose) polymerase-1 inhibitor BSI-401 has antitumor activity and synergizes with oxaliplatin against pancreatic cancer, preventing acute neurotoxicity. Clin Cancer Res 2009;15:6367-6377
17. Melisi D., Ishiyama S., Sclabas G.M., Fleming J.B., Xia Q., Tortora G., et al. LY2109761, a novel transforming growth factor {beta} receptor type I and type II dual inhibitor, as a therapeutic approach to suppressing pancreatic cancer metastasis. Mol Cancer Ther 2008;7:829-840 (Pubitemid 351551036)
18. Bockhorn M., Tsuzuki Y., Xu L., Frilling A., Broelsch C.E., Fukumura D. Differential vascular and transcriptional responses to anti-vascular endothelial growth factor antibody in orthotopic human pancreatic cancer xenografts. Clin Cancer Res 2003;9:4221-4226 (Pubitemid 37204043)
19. Pei H., Li L., Fridley B.L., Jenkins G.D., Kalari K.R., Lingle W., et al. FKBP51 affects cancer cell response to chemotherapy by negatively regulating Akt. Cancer Cell 2009;16:259-266
20. Badea L., Herlea V., Dima S.O., Dumitrascu T., Popescu I. Combined gene expression analysis of whole-tissue and microdissected pancreatic ductal adenocarcinoma identifies genes specifically over-expressed in tumor epithelia. Hepatogastroenterology 2008;55:2016-2027
21. Peinado H., Olmeda D., Cano A. Snail, Zeb and bHLH factors in tumour progression: An alliance against the epithelial phenotype? Nat Rev Cancer 2007;7:415-428 (Pubitemid 46809165)
22. Vincent T., Neve E.P., Johnson J.R., Kukalev A., Rojo F., Albanell J., et al. A SNAIL1-SMAD3/4 transcriptional repressor complex promotes TGF-beta mediated epithelial-mesenchymal transition. Nat Cell Biol 2009;11:943-950
23. Vandercappellen J., Van Damme J., Struyf S. The role of CXC chemokines and their receptors in cancer. Cancer Lett 2008;267:226-244
24. Apte R.N., Dotan S., Elkabets M., White M.R., Reich E., Carmi Y., et al. The involvement of IL-1 in tumorigenesis, tumor invasiveness, metastasis and tumor-host interactions. Cancer Metastasis Rev 2006;25:387-408. (Pubitemid 44922357)
25. Carmi Y., Voronov E., Dotan S., Lahat N., Rahat M.A., Fogel M., et al. The role of macrophage-derived IL-1 in induction and maintenance of angiogenesis. J Immunol 2009;183:4705-4714
26. Melisi D., Niu J., Chang Z., Xia Q., Peng B., Ishiyama S., et al. Secreted interleukin-1alpha induces a metastatic phenotype in pancreatic cancer by sustaining a constitutive activation of nuclear factor-kappaB. Mol Cancer Res 2009;7:624-633
27. Kim I., Moon S.O., Koh K.N., Kim H., Uhm C.S., Kwak H.J., et al. Molecular cloning, expression, and characterization of angiopoietin-related protein. angiopoietin-related protein induces endothelial cell sprouting. J Biol Chem 1999;274:26523-26528
28. Oike Y., Yasunaga K., Suda T. Angiopoietin-related/angiopoietin-like proteins regulate angiogenesis. Int J Hematol 2004;80:21-28 (Pubitemid 38937871)
29. Coffelt S.B., Lewis C.E., Naldini L., Brown J.M., Ferrara N., De Palma M. Elusive identities and overlapping phenotypes of proangiogenic myeloid cells in tumors. Am J Pathol 2010;176:1564-1576
30. Ebos J.M., Lee C.R., Cruz-Munoz W., Bjarnason G.A., Christensen J.G., Kerbel R.S. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 2009;15:232-239
31. 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;15:220-231
32. Ferrara N. Pathways mediating VEGF-independent tumor angiogenesis. Cytokine Growth Factor Rev 2010;21:21-26
33. Loges S., Mazzone M., Hohensinner P., Carmeliet P. Silencing or fueling metastasis with VEGF inhibitors: Antiangiogenesis revisited. Cancer Cell 2009;15:167-170
34. Thiery J.P., Acloque H., Huang R.Y., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009;139:871-890
35. Philip P.A., Mooney M., Jaffe D., Eckhardt G., Moore M., Meropol N., et al. Consensus report of the national cancer institute clinical trials planning meeting on pancreas cancer treatment. J Clin Oncol 2009;27:5660-5669
36. Hruban R.H., Adsay N.V., Albores-Saavedra J., Anver M.R., Biankin A.V., Boivin G.P., et al. Pathology of genetically engineered mouse models of pancreatic exocrine cancer: Consensus report and recommendations. Cancer Res 2006;66:95-106. (Pubitemid 43166014)
37. Olive K.P., Jacobetz M.A., Davidson C.J., Gopinathan A., McIntyre D., Honess D., et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 2009;324:1457-1461
38. Ali M.M., Janic B., Babajani-Feremi A., Varma N.R., Iskander A.S., Anagli J., et al. Changes in vascular permeability and expression of different angiogenic factors following anti-angiogenic treatment in rat glioma. PLoS One 2010;5:e8727.
39. Lucio-Eterovic A.K., Piao Y., De Groot J.F. Mediators of glioblastoma resistance and invasion during antivascular endothelial growth factor therapy. Clin Cancer Res 2009;15:4589-4599
40. Huang D., Ding Y., Zhou M., Rini B.I., Petillo D., Qian C.N., et al. Interleukin- 8 mediates resistance to antiangiogenic agent sunitinib in renal cell carcinoma. Cancer Res 2010;70:1063-1071
41. Altorki N., Lane M.E., Bauer T., Lee P.C., Guarino M.J., Pass H., et al. Phase II proof-of-concept study of pazopanib monotherapy in treatmentnaive patients with stage I/II resectable non-small-cell lung cancer. J Clin Oncol 2010;28:3131-3137
42. Hanrahan E.O., Lin H.Y., Kim E.S., Yan S., Du D.Z., McKee K.S., et al. Distinct patterns of cytokine and angiogenic factor modulation and markers of benefit for vandetanib and/or chemotherapy in patients with non-small-cell lung cancer. J Clin Oncol 2010;28:193-201.
43. Kopetz S., Hoff P.M., Morris J.S., Wolff R.A., Eng C., Glover K.Y., et al. Phase II trial of infusional fluorouracil, irinotecan, and bevacizumab for metastatic colorectal cancer: Efficacy and circulating angiogenic biomarkers associated with therapeutic resistance. J Clin Oncol 2010;28:453-459
44. Nikolinakos P.G., Altorki N., Yankelevitz D., Tran H.T., Yan S., Rajagopalan D., et al. Plasma cytokine and angiogenic factor profiling identifies markers associated with tumor shrinkage in early-stage non-small cell lung cancer patients treated with pazopanib. Cancer Res 2010;70:2171-2179