Glioblastoma resistance to anti-VEGF therapy is associated with myeloid cell infiltration, stem cell accumulation, and a mesenchymal phenotype

Neuro-Oncology

Volumn 14, Issue 11, 2012, Pages 1379-1392

  Piao, Yuji ^a   Liang, Ji ^a   Holmes, Lindsay ^a   Zurita, Amado J ^a   Henry, Verlene ^a   Heymach, John V ^a   De Groot, John F ^a  

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

Author keywords

angiogenesis; bevacizumab; glioblastoma; myeloid cell; VEGF

Indexed keywords

BEVACIZUMAB; BIOLOGICAL MARKER; CD11B ANTIGEN; SUNITINIB;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTIANGIOGENIC THERAPY; ARTICLE; BONE MARROW CELL; CANCER COMBINATION CHEMOTHERAPY; CANCER GROWTH; CANCER RESISTANCE; CANCER STEM CELL; CANCER SURVIVAL; CELL INFILTRATION; CELL PROLIFERATION; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENTIATION; FLOW CYTOMETRY; GLIOBLASTOMA; GRANULOCYTE; HUMAN; HUMAN CELL; HYPOXIA; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MESENCHYME; MONOCYTE; MONOTHERAPY; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; TUMOR XENOGRAFT;

ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC AGENTS; CELL HYPOXIA; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; FLOW CYTOMETRY; GLIOBLASTOMA; HUMANS; IMMUNOHISTOCHEMISTRY; INDOLES; MESODERM; MICE; MICE, NUDE; MYELOID CELLS; NEOVASCULARIZATION, PATHOLOGIC; PHENOTYPE; PYRROLES; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; STEM CELLS; TUMOR MICROENVIRONMENT; VASCULAR ENDOTHELIAL GROWTH FACTOR A; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84868035933     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/nos158     Document Type: Article

References (40)

1. Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev. 2004;25:581-611.
2. Takano S, Yoshii Y, Kondo S, et al. Concentration of vascular endothelial growth factor in the serum and tumor tissue of brain tumor patients. Cancer Res. 1996;56:2185-2190.
3. Loges S, Schmidt T, Carmeliet P. "Antimyeloangiogenic" therapy for cancer by inhibiting PlGF. Clin Cancer Res. 2009;15:3648-3653.
4. Kerber M, Reiss Y, Wickersheim A, et al. Flt-1 signaling in macrophages promotes glioma growth in vivo. Cancer Res. 2008;68:7342-7351.
5. Du R, Lu KV, Petritsch C, et al. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell. 2008;13:206-220.
6. Bergers G, Hanahan D. Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer. 2008;8:592-603.
7. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science. 2005;307:58-62.
8. Lucio-Eterovic AK, Piao Y, de Groot JF. Mediators of glioblastoma resistance and invasion during antivascular endothelial growth factor therapy. Clin Cancer Res. 2009;15:4589-4599.
9. Shojaei F, Wu X, Malik AK, et al. Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells. Nature Biotech. 2007;25:911-920.
10. Shojaei F, Wu X, Qu X, et al. G-CSF-initiated myeloid cell mobilization and angiogenesis mediate tumor refractoriness to anti-VEGF therapy in mouse models. Proc Natl Acad Sci USA. 2009;106:6742-6747.
11. Friedman HS, Prados MD, Wen PY, et al. Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J Clin Oncol. 2009;27:4733-4740.
12. de Groot JF, Yung WK. Bevacizumab and irinotecan in the treatment of recurrent malignant gliomas. Cancer J. 2008;14:279-285.
13. Neyns B, Sadones J, Chaskis C, et al. Phase II study of sunitinib malate in patients with recurrent high-grade glioma. J Neurooncol. 2011;103: 491-501.
14. Batchelor TT, Mulholland P, Neyns B, et al. The efficacy of cediranib as monotherapy and in combination with lomustine compared with lomustine alone in patients with recurrent glioblastoma: a phase III randomized study. Neuro-oncol. 2010;12:iv69-iv78.
15. Murray LJ, Abrams TJ, Long KR, et al. SU11248 inhibits tumor growth and CSF-1R-dependent osteolysis in an experimental breast cancer bone metastasis model. Clin Exp Metas. 2003;20:757-766.
16. Lal S, Lacroix M, Tofilon P, et al. An implantable guide-screw system for brain tumor studies in small animals. J Neurosurg. 2000;92:326-333.
17. Chebib I, Shabani-Rad MT, Chow MS, et al. Microvessel density and clinicopathologic characteristics in hepatocellular carcinoma with and without cirrhosis. Biomark Insights. 2007;2:59-68.
18. Bergers G, Song S, Meyer-Morse N, et al. Benefits of targeting both pericytes and endothelial cells in the tumor vasculature with kinase inhibitors. J Clin Invest. 2003;111:1287-1295.
19. Hashizume H, Falcon BL, Kuroda T, et al. Complementary actions of inhibitors of angiopoietin-2 and VEGF on tumor angiogenesis and growth. Cancer Res. 2010;70:2213-2223.
20. Fischer C, Mazzone M, Jonckx B, et al. FLT1 and its ligands VEGFB and PlGF: drug targets for anti-angiogenic therapy? Nat Rev Cancer. 2008;8:942-956.
21. Murdoch C,Muthana M, Coffelt SB, et al. The role of myeloid cells in the promotion of tumour angiogenesis. Nat Rev Cancer. 2008;8:618-631.
22. Dirkx AE, Oude Egbrink MG, Wagstaff J, et al. Monocyte/macrophage infiltration in tumors: modulators of angiogenesis. J Leukoc Biol. 2006;80:1183-1196.
23. Murdoch C, Giannoudis A, Lewis CE. Mechanisms regulating the recruitment of macrophages into hypoxic areas of tumors and other ischemic tissues. Blood. 2004;104:2224-2234.
24. Imai T, Horiuchi A, Wang C, et al. Hypoxia attenuates the expression of E-cadherin via up-regulation of SNAIL in ovarian carcinoma cells. Am J Pathol. 2003;163:1437-1447.
25. Yang MH, Wu KJ. TWIST activation by hypoxia inducible factor-1 (HIF-1): implications in metastasis and development. Cell Cycle. 2008;7:2090-2096.
26. Erber R, Thurnher A, Katsen AD, et al. Combined inhibition of VEGF and PDGF signaling enforces tumor vessel regression by interfering with pericyte-mediated endothelial cell survival mechanisms. Faseb J. 2004;18:338-340.
27. Polverino A, Coxon A, Starnes C, et al. AMG 706, an oral, multikinase inhibitor that selectively targets vascular endothelial growth factor, platelet-derived growth factor, and kit receptors, potently inhibits angiogenesis and induces regression in tumor xenografts. Cancer Res. 2006;66:8715-8721.
28. Zhou Q, Gallo JM. Differential effect of sunitinib on the distribution of temozolomide in an orthotopic glioma model. Neuro-oncology. 2009;11:301-310.
29. Vecchiarelli-Federico LM, Cervi D, Haeri M, et al. Vascular endothelial growth factor-a positive and negative regulator of tumor growth. Cancer Res. 2010;70:863-867.
30. Dawson MR, Duda DG, Fukumura D, et al. VEGFR1-activity-independent metastasis formation. Nature. 2009;461:E4. discussion E5.
31. Dawson MR, Duda DG, Chae SS, et al. VEGFR1 activity modulates myeloid cell infiltration in growing lung metastases but is not required for spontaneous metastasis formation. PLoS One. 2009;4:e6525.
32. Willett CG, Boucher Y, di Tomaso E, et al. Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat Med. 2004;10:145-147.
33. de Groot JF, Piao Y, Tran H, et al. Myeloid biomarkers associated with glioblastoma response to anti-VEGF therapy with aflibercept. Clin Cancer Res. 2011;17:4872-4881.
34. Ebos JM, Lee CR, Cruz-Munoz W, et al. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell. 2009;15:232-239.
35. Paez-Ribes M, Allen E, Hudock J, et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell. 2009;15:220-231.
36. Hammers HJ, Verheul HM, Salumbides B, et al. Reversible epithelial to mesenchymal transition and acquired resistance to sunitinib in patients with renal cell carcinoma: evidence from a xenograft study. Molec Cancer Ther. 2010;9:1525-1535.
37. Thompson EW, Torri J, Sabol M, et al. Oncogene-induced basement membrane invasiveness in human mammary epithelial cells. Clin Exp Metastasis. 1994;12:181-194.
38. Behrens J, Mareel MM, Van Roy FM, et al. Dissecting tumor cell invasion: epithelial cells acquire invasive properties after the loss of uvomorulinmediated cell-cell adhesion. J Cell Biol. 1989;108:2435-2447.
39. KimWY, Perera S,ZhouB, et al. HIF2alpha cooperateswithRAS to promote lung tumorigenesis in mice. J Clin Invest. 2009;119:2160-2170.
40. Lu X, Kang Y. Hypoxia and hypoxia-inducible factors: master regulators of metastasis. Clin Cancer Res. 2010;16:5928-5935.