Collagen signaling enhances tumor progression after anti-VEGF therapy in a murine model of pancreatic ductal adenocarcinoma

Cancer Research

Volumn 74, Issue 4, 2014, Pages 1032-1044

  Aguilera, Kristina Y ^a   Rivera, Lee B ^a,c   Hur, Hoon ^a,d   Carbon, Juliet G ^a   Toombs, Jason E ^a   Goldstein, Courtney D ^a   Dellinger, Michael T ^a   Castrillon, Diego H ^b   Brekken, Rolf A ^a,b  

^a Hamon Center for Therapeutic Oncology Research   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Ajou University School of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; COLLAGEN; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; MICE; MICE, TRANSGENIC; NEOPLASM INVASIVENESS; PANCREATIC NEOPLASMS; SIGNAL TRANSDUCTION; TREATMENT FAILURE; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84894277482     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-2800     Document Type: Article

References (54)

1. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med 1971;285:1182-6.
2. Roskoski R Jr. Vascular endothelial growth factor (VEGF) signaling in tumor progression. Crit Rev Oncol Hematol 2007;62:179-213.
3. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
4. Shojaei F. Anti-angiogenesis therapy in cancer: current challenges and future perspectives. Cancer Lett 2012;320:130-7.
5. Welti J, Loges S, Dimmeler S, Carmeliet P. Recent molecular discoveries in angiogenesis and antiangiogenic therapies in cancer. J Clin Invest 2013;123:3190-200.
6. Norden AD, Young GS, Setayesh K, Muzikansky A, Klufas R, Ross GL, et al. Bevacizumab for recurrent malignant gliomas: efficacy, toxicity, and patterns of recurrence. Neurology 2008;70:779-87.
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. Ghaneh P, Costello E, Neoptolemos JP. Biology and management of pancreatic cancer. Gut 2007;56:1134-52.
9. Korpanty G, Carbon JG, Grayburn PA, Fleming JB, Brekken RA. Monitoring response to anticancer therapy by targeting microbubbles to tumor vasculature. Clin Cancer Res 2007;13:323-30.
10. Dineen SP, Lynn KD, Holloway SE, Miller AF, Sullivan JP, Shames DS, et al. Vascular endothelial growth factor receptor 2 mediates macro-phage infiltration into orthotopic pancreatic tumors in mice. Cancer Res 2008;68:4340-6.
11. Kindler HL, Niedzwiecki D, Hollis D, Sutherland S, Schrag D, Hurwitz H, et al. Gemcitabine plus bevacizumab compared with gemcitabine plus placebo in patients with advanced pancreatic cancer: phase III trial of the Cancer and Leukemia Group B (CALGB 80303). J Clin Oncol 2010;28:3617-22.
12. Van Cutsem E, Vervenne WL, Bennouna J, Humblet Y, Gill S, Van Laethem JL, et al. Phase III trial of bevacizumab in combination with gemcitabine and erlotinib in patients with metastatic pancreatic cancer. J Clin Oncol 2009;27:2231-7.
13. Grzesiak JJ, Ho JC, Moossa AR, Bouvet M. The integrin-extracellular matrix axis in pancreatic cancer. Pancreas 2007;35:293-301.
14. Olive KP, Jacobetz MA, Davidson CJ, 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;324:1457-61.
15. Shields MA, Dangi-Garimella S, Redig AJ, Munshi HG. Biochemical role of the collagen-rich tumour microenvironment in pancreatic cancer progression. Biochem J 2012;441:541-52.
16. Sullivan LA, Carbon JG, Roland CL, Toombs JE, Nyquist-Andersen M, Kavlie A, et al. r84, a novel therapeutic antibody against mouse and human VEGF with potent anti-tumor activity and limited toxicity induction. PLoS ONE 2010;5:e12031.
17. Bradshaw AD, Puolakkainen P, Dasgupta J, Davidson JM, Wight TN, Helene Sage E. SPARC-null mice display abnormalities in the dermis characterized by decreased collagen fibril diameter and reduced tensile strength. J Invest Dermatol 2003;120:949-55.
18. Norose K, Clark JI, Syed NA, Basu A, Heber-Katz E, Sage EH, et al. SPARC deficiency leads to early-onset cataractogenesis. Invest Ophthalmol Vis Sci 1998;39:2674-80.
19. Dineen SP, Roland CL, Greer R, Carbon JG, Toombs JE, Gupta P, et al. Smac mimetic increases chemotherapy response and improves survival in mice with pancreatic cancer. Cancer Res 2010;70:2852-61.
20. Ostapoff KT, Awasthi N, Cenik BK, Hinz S, Dredge K, Schwarz RE, et al. PG545, an angiogenesis and heparanase inhibitor, reduces primary tumor growth and metastasis in experimental pancreatic cancer. Mol Cancer Ther 2013;12:1190-201.
21. Dasch JR, Pace DR, Waegell W, Inenaga D, Ellingsworth L. Monoclonal antibodies recognizing transforming growth factor-beta. Bioactivity neutralization and transforming growth factor beta 2 affinity purification. J Immunol 1989;142:1536-41.
22. Almoguera C, Shibata D, Forrester K, Martin J, Arnheim N, Perucho M. Most human carcinomas of the exocrinepancreas contain mutant c-K-ras genes. Cell 1988;53:549-54.
23. Caldas C, Hahn SA, da Costa LT, Redston MS, Schutte M, Seymour AB, et al. Frequent somatic mutations and homozygous deletions of the p16 (MTS1) gene in pancreatic adenocarcinoma. Nat Genet 1994;8:27-32.
24. Aguirre AJ, Bardeesy N, Sinha M, Lopez L, Tuveson DA, Horner J, et al. Activated Kras and Ink4a/Arf deficiency cooperate to produce metastatic pancreatic ductal adenocarcinoma. Genes Dev 2003;17: 3112-26.
25. 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;2:270-87.
26. Lu KV, Chang JP, Parachoniak CA, Pandika MM, Aghi MK, Meyr-onet D, et al. VEGF inhibits tumor cell invasion and mesenchymal transition through a MET/VEGFR2 complex. Cancer Cell 2012;22: 21-35.
27. Zhang H, Akman HO, Smith EL, Zhao J, Murphy-Ullrich JE, Batuman OA. Cellular response to hypoxia involves signaling via Smad proteins. Blood 2003;101:2253-60.
28. Lee YC, Lane KB, Zoia O, Thompson PJ, Light RW, Blackwell TS. Transforming growth factor-beta induces collagen synthesis without inducing IL-8 production in mesothelial cells. Eur Respir J 2003;22: 197-202.
29. Shintani Y, Fukumoto Y, Chaika N, Svoboda R, Wheelock MJ, Johnson KR. Collagen I-mediated up-regulation of N-cadherin requires cooperative signals from integrins and discoidin domain receptor 1. J Cell Biol 2008;180:1277-89.
30. Kelber JA, Klemke RL. PEAK1, a novel kinase target in the fight against cancer. Oncotarget 2010;1:219-23.
31. Croucher DR, Hochgrafe F, Zhang L, Liu L, Lyons RJ, Rickwood D, et al. Involvement of Lyn and the atypical kinase SgK269/PEAK1 in a basal breast cancer signaling pathway. Cancer Res 2013;73: 1969-80.
32. Hezel AF, Deshpande V, Zimmerman SM, Contino G, Alagesan B, O'Dell MR, et al. TGF-beta and alphavbeta6 integrin act in a common pathway to suppress pancreatic cancer progression. Cancer Res 2012;72:4840-5.
33. Carafoli F, Hohenester E. Collagen recognition and transmembrane signalling by discoidin domain receptors. Biochim Biophys Acta 2013;1934:2187-94.
34. Carafoli F, Bihan D, Stathopoulos S, Konitsiotis AD, Kvansakul M, Farndale RW, et al. Crystallographic insight into collagen recognition by discoidin domain receptor 2. Structure 2009;17:1573-81.
35. Vogel W, Gish GD, Alves F, Pawson T. The discoidin domain receptor tyrosine kinases are activated by collagen. Mol Cell 1997;1:13-23.
36. Castro-Sanchez L, Soto-Guzman A, Navarro-Tito N, Martinez-Orozco R, Salazar EP. Native type IV collagen induces cell migration through a CD9 and DDR1-dependent pathway in MDA-MB-231 breast cancer cells. Eur J Cell Biol 2010;89:843-52.
37. Carbone C, Moccia T, Zhu C, Paradiso G, Budillon A, Chiao PJ, et al. Anti-VEGF treatment-resistant pancreatic cancers secrete proinflam-matory factors that contribute to malignant progression by inducing an EMT cell phenotype. Clin Cancer Res 2011;17:5822-32.
38. 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.
39. Keunen O, Johansson M, Oudin A, Sanzey M, Rahim SA, Fack F, et al. Anti-VEGF treatment reduces blood supply and increases tumor cell invasion in glioblastoma. Proc Natl Acad Sci USA 2011;108:3749-54.
40. Yamagishi N, Teshima-Kondo S, Masuda K, Nishida K, Kuwano Y, Dang DT, et al. Chronic inhibition of tumor cell-derived VEGF enhances the malignant phenotype of colorectal cancer cells. BMC Cancer 2013;13:229.
41. Phan VT, Wu X, Cheng JH, Sheng RX, Chung AS, Zhuang G, et al. Oncogenic RAS pathway activation promotes resistance to anti-VEGF therapy through G-CSF-induced neutrophil recruitment. Proc Natl Acad Sci USA 2013;110:6079-84.
42. Hu YL, Jahangiri A, Delay M, Aghi MK. Tumor cell autophagy as an adaptive response mediating resistance to treatments such as anti-angiogenic therapy. Cancer Res 2012;72:4294-9.
43. Ye X, Li Y, Stawicki S, Couto S, Eastham-Anderson J, Kallop D, et al. An anti-Axl monoclonal antibody attenuates xenograft tumor growth and enhances the effect of multiple anticancer therapies. Oncogene 2010;29:5254-64.
44. Kutluk Cenik B, Ostapoff KT, Gerber DE, Brekken RA. BIBF 1120 (nintedanib), a triple angiokinase inhibitor, induces hypoxia but not EMT and blocks progression of preclinical models of lung and pancreatic cancer. Mol Cancer Ther 2013;12:992-1001.
45. Arnold SA, Brekken RA. SPARC: a matricellular regulator of tumori-genesis. J Cell Commun Signal 2009;3:255-73.
46. Gao J, Song J, Huang H, Li Z, Du Y, Cao J, et al. Methylation of the SPARC gene promoter and its clinical implication in pancreatic cancer. J Exp Clin Cancer Res 2010;29:28.
47. Sato N, Fukushima N, Maehara N, Matsubayashi H, Koopmann J, Su GH, et al. SPARC/osteonectin is a frequent target for aberrant meth-ylation in pancreatic adenocarcinoma and a mediator of tumor-stromal interactions. Oncogene 2003;22:5021-30.
48. Von Hoff DD, Ramanathan RK, Borad MJ, Laheru DA, Smith LS, Wood TE, et al. Gemcitabine plus nab-paclitaxel is an active regimen in patients with advanced pancreatic cancer: a phase I/II trial. J Clin Oncol 2011;29:4548-54.
49. Hohenester E, Sasaki T, Giudici C, Farndale RW, Bachinger HP. Structural basis of sequence-specific collagen recognition by SPARC. Proc Natl Acad Sci USA 2008;105:18273-7.
50. Harris BS, Zhang Y, Card L, Rivera LB, Brekken RA, Bradshaw AD. SPARC regulates collagen interaction with cardiac fibroblast cell surfaces. Am J Physiol Heart Circ Physiol 2011;301:H841-7.
51. Arnold SA, Rivera LB, Carbon JG, Toombs JE, Chang CL, Bradshaw AD, et al. Losartan slows pancreatic tumor progression and extends survival of SPARC-Null mice by abrogating aberrant TGFbeta activation. PLoS ONE 2012;7:e31384.
52. Arnold SA, Rivera LB, Miller AF, Carbon JG, Dineen SP, Xie Y, et al. Lack of host SPARC enhances vascular function and tumor spread in an orthotopic murine model of pancreatic carcinoma. Dis Model Mech 2010;3:57-72.
53. Gao M, Duan L, Luo J, Zhang L, Lu X, Zhang Y, et al. Discovery and optimization of 3-(2-(Pyrazolo[1, 5-a]pyrimidin-6-yl)ethynyl) benzamides as novel selective and orally bioavailable discoidin domain receptor 1 (DDR1) inhibitors. J Med Chem 2013;56: 3281-95.
54. Kim HG, Tan L, Weisberg EL, Liu F, Canning P, Choi HG, et al. Discovery of a potent and selective DDR1 receptor tyrosine Kinase inhibitor. ACS Chem Biol 2013;8:2145-50.