VEGFR inhibitors upregulate CXCR4 in VEGF receptor-expressing glioblastoma in a TGFβR signaling-dependent manner

Cancer Letters

Volumn 360, Issue 1, 2015, Pages 60-67

  Pham, Kien ^a   Luo, Defang ^a   Siemann, Dietmar W ^a   Law, Brian K ^a   Reynolds, Brent A ^a   Hothi, Parvinder ^b   Foltz, Gregory ^b   Harrison, Jeffrey K ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b SWEDISH MEDICAL CENTER   (United States)

Author keywords

Anti angiogenic therapy; CXCR4; GBM; MET; TGF R; VEGFR

Indexed keywords

CEDIRANIB; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR4 ANTAGONIST; PLERIXAFOR; STROMAL CELL DERIVED FACTOR 1; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; VANDETANIB; VASCULOTROPIN RECEPTOR; ANGIOGENESIS INHIBITOR; CXCR4 PROTEIN, HUMAN; HETEROCYCLIC COMPOUND; IL2RA PROTEIN, MOUSE; INTERLEUKIN 2 RECEPTOR ALPHA; N-(4-BROMO-2-FLUOROPHENYL)-6-METHOXY-7-((1-METHYLPIPERIDIN-4-YL)METHOXY)QUINAZOLIN-4-AMINE; PIPERIDINE DERIVATIVE; PROTEIN KINASE INHIBITOR; QUINAZOLINE DERIVATIVE;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER SURVIVAL; CELL MIGRATION; DRUG MECHANISM; FEMALE; FLOW CYTOMETRY; GLIOBLASTOMA; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MALE; MONOTHERAPY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN NEOPLASMS; CELL MOTION; DEFICIENCY; DRUG EFFECTS; DRUG SCREENING; ENZYMOLOGY; GENETICS; KNOCKOUT MOUSE; METABOLISM; MIDDLE AGED; NONOBESE DIABETIC MOUSE; PATHOLOGY; SCID MOUSE; SIGNAL TRANSDUCTION; TIME; TUMOR CELL LINE; TUMOR INVASION;

ANIMALIA;

ADULT; AGED; ANGIOGENESIS INHIBITORS; ANIMALS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; FEMALE; GLIOBLASTOMA; HETEROCYCLIC COMPOUNDS; HUMANS; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; MALE; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; MIDDLE AGED; NEOPLASM INVASIVENESS; PIPERIDINES; PROTEIN KINASE INHIBITORS; QUINAZOLINES; RECEPTOR CROSS-TALK; RECEPTORS, CXCR4; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TIME FACTORS; UP-REGULATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84924460395     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2015.02.005     Document Type: Article

References (59)

1. Schneider T., et al. Gliomas in adults. Dtsch. Arztebl. Int 2010, 107:799-807.
2. McComb R.D., et al. The biology of malignant gliomas - a comprehensive survey. Clin. Neuropathol 1984, 3:93-106.
3. Clarke J., et al. Recent advances in therapy for glioblastoma. Arch. Neurol 2010, 67:279-283.
4. Plate K.H., et al. Up-regulation of vascular endothelial growth factor and its cognate receptors in a rat glioma model of tumor angiogenesis. Cancer Res 1993, 53:5822-5827.
5. Plate K.H., et al. Vascular endothelial growth factor and glioma angiogenesis: coordinate induction of VEGF receptors, distribution of VEGF protein and possible in vivo regulatory mechanisms. Int. J. Cancer 1994, 59:520-529.
6. Samoto K., et al. Expression of vascular endothelial growth factor and its possible relation with neovascularization in human brain tumors. Cancer Res 1995, 55:1189-1193.
7. Hofer S., et al. Clinical outcome with bevacizumab in patients with recurrent high-grade glioma treated outside clinical trials. Acta Oncol 2011, 50:630-635.
8. Reardon D.A., et al. Glioblastoma multiforme: an emerging paradigm of anti-VEGF therapy. Expert Opin. Biol. Ther 2008, 8:541-553.
9. Iwamoto F.M., et al. Bevacizumab for malignant gliomas. Arch. Neurol 2010, 67:285-288.
10. Batchelor T.T., et al. AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 2007, 11:83-95.
11. Drappatz J., et al. Phase I study of vandetanib with radiotherapy and temozolomide for newly diagnosed glioblastoma. Int. J. Radiat. Oncol. Biol. Phys 2010, 78:85-90.
12. Gilbert M.R., et al. A randomized trial of bevacizumab for newly diagnosed glioblastoma. N. Engl. J. Med 2014, 370:699-708.
13. Chinot O.L., et al. Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N. Engl. J. Med 2014, 370:709-722.
14. Bergers G., et al. Modes of resistance to anti-angiogenic therapy. Nat. Rev. Cancer 2008, 8:592-603.
15. Iwamoto F.M., et al. Patterns of relapse and prognosis after bevacizumab failure in recurrent glioblastoma. Neurology 2009, 73:1200-1206.
16. de Groot J.F., et al. Tumor invasion after treatment of glioblastoma with bevacizumab: radiographic and pathologic correlation in humans and mice. Neuro-Oncol 2010, 12:233-242.
17. Narayana A., et al. A clinical trial of bevacizumab, temozolomide, and radiation for newly diagnosed glioblastoma. J. Neurosurg 2012, 116:341-345.
18. Lu K.V., et al. VEGF inhibits tumor cell invasion and mesenchymal transition through a MET/VEGFR2 complex. Cancer Cell 2012, 22:21-35.
19. Koshiba T., et al. Expression of stromal cell-derived factor 1 and CXCR4 ligand receptor system in pancreatic cancer: a possible role for tumor progression. Clin. Cancer Res 2000, 6:3530-3535.
20. Hall J.M., et al. Stromal cell-derived factor 1, a novel target of estrogen receptor action, mediates the mitogenic effects of estradiol in ovarian and breast cancer cells. Mol. Endocrinol 2003, 17:792-803.
21. Rubin J.B., et al. A small-molecule antagonist of CXCR4 inhibits intracranial growth of primary brain tumors. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:13513-13518.
22. Burns J.M., et al. A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J. Exp. Med 2006, 203:2201-2213.
23. Ehtesham M., et al. CXCR4 expression mediates glioma cell invasiveness. Oncogene 2006, 25:2801-2806.
24. Zagzag D., et al. Hypoxia-inducible factor 1 and VEGF upregulate CXCR4 in glioblastoma: implications for angiogenesis and glioma cell invasion. Lab. Invest 2006, 86:1221-1232.
25. Zagzag D., et al. Hypoxia- and vascular endothelial growth factor-induced stromal cell-derived factor-1alpha/CXCR4 expression in glioblastomas: one plausible explanation of Scherer's structures. Am. J. Pathol 2008, 173:545-560.
26. Mantovani A., et al. The chemokine system in cancer biology and therapy. Cytokine Growth Factor Rev 2010, 21:27-39.
27. Sun X., et al. CXCL12/CXCR4/CXCR7 chemokine axis and cancer progression. Cancer Metastasis Rev 2010, 29:709-722.
28. Duda D.G., et al. CXCL12 (SDF1alpha)-CXCR4/CXCR7 pathway inhibition: an emerging sensitizer for anticancer therapies. Clin. Cancer Res 2011, 17:2074-2080.
29. Ping Y.F., et al. The chemokine CXCL12 and its receptor CXCR4 promote glioma stem cell-mediated VEGF production and tumour angiogenesis via PI3K/AKT signalling. J. Pathol 2011, 224:344-354.
30. Tseng D., et al. Targeting SDF-1/CXCR4 to inhibit tumour vasculature for treatment of glioblastomas. Br. J. Cancer 2011, 104:1805-1809.
31. Hattermann K., et al. The chemokine receptor CXCR7 is highly expressed in human glioma cells and mediates antiapoptotic effects. Cancer Res 2010, 70:3299-3308.
32. Komatani H., et al. Expression of CXCL12 on pseudopalisading cells and proliferating microvessels in glioblastomas: an accelerated growth factor in glioblastomas. Int. J. Oncol 2009, 34:665-672.
33. Liu C., et al. Expression and functional heterogeneity of chemokine receptors CXCR4 and CXCR7 in primary patient-derived glioblastoma cells. PLoS ONE 2013, 8:e59750.
34. Galli R., et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004, 64:7011-7021.
35. Sarkisian M.R., et al. Detection of primary cilia in human glioblastoma. J. Neurooncol 2014, 117:15-24.
36. Silver D.J., et al. Chondroitin sulfate proteoglycans potently inhibit invasion and serve as a central organizer of the brain tumor microenvironment. J. Neurosci 2013, 33:15603-15617.
37. Siebzehnrubl F.A., et al. The ZEB1 pathway links glioblastoma initiation, invasion and chemoresistance. EMBO Mol. Med 2013, 5:1196-1212.
38. Deleyrolle L.P., et al. Evidence for label-retaining tumour-initiating cells in human glioblastoma. Brain 2011, 134:1331-1343.
39. Deleyrolle L.P., et al. Determination of somatic and cancer stem cell self-renewing symmetric division rate using sphere assays. PLoS ONE 2011, 6:e15844.
40. Liu C., et al. Chemokine receptor CXCR3 promotes growth of glioma. Carcinogenesis 2011, 32:129-137.
41. Hothi P., et al. High-throughput chemical screens identify disulfiram as an inhibitor of human glioblastoma stem cells. Oncotarget 2012, 3:1124-1136.
42. Esencay M., et al. HGF upregulates CXCR4 expression in gliomas via NF-kappaB: implications for glioma cell migration. J. Neurooncol 2010, 99:33-40.
43. Roth P., et al. Integrin control of the transforming growth factor-β pathway in glioblastoma. Brain 2013, 136:564-576.
44. Gold L.I. The role for transforming growth factor-beta (TGF-beta) in human cancer. Crit. Rev. Oncog 1999, 10:303-360.
45. Fontana A., et al. Expression of TGF-beta 2 in human glioblastoma: a role in resistance to immune rejection. Ciba Found. Symp 1991, 157:232-238.
46. Kuczynski E.A., et al. VEGFR2 expression and TGF-β signaling in initial and recurrent high-grade human glioma. Oncology 2011, 81:126-134.
47. Zhang M., et al. Blockade of TGF-β signaling by the TGFβR-I kinase inhibitor LY2109761 enhances radiation response and prolongs survival in glioblastoma. Cancer Res 2011, 71:7155-7167.
48. Piao Y., et al. Glioblastoma resistance to anti-VEGF therapy is associated with myeloid cell infiltration, stem cell accumulation, and a mesenchymal phenotype. Neuro-Oncol 2012, 14:1379-1392.
49. Hardee M.E., et al. Resistance of glioblastoma-initiating cells to radiation mediated by the tumor microenvironment can be abolished by inhibiting transforming growth factor-β. Cancer Res 2012, 72:4119-4129.
50. Maddirela D.R., et al. MMP-2 suppression abrogates irradiation-induced microtubule formation in endothelial cells by inhibiting αvβ3-mediated SDF-1/CXCR4 signaling. Int. J. Oncol 2013, 42:1279-1288.
51. Mischel P.S., et al. Identification of molecular subtypes of glioblastoma by gene expression profiling. Oncogene 2003, 22:2361-2373.
52. Brennan C., et al. Glioblastoma subclasses can be defined by activity among signal transduction pathways and associated genomic alterations. PLoS ONE 2009, 4:e7752.
53. Verhaak R.G., et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010, 17:98-110.
54. Eichhorn P.J., et al. USP15 stabilizes TGF-β receptor I and promotes oncogenesis through the activation of TGF-β signaling in glioblastoma. Nat. Med 2012, 18:429-435.
55. Beier C.P., et al. The cancer stem cell subtype determines immune infiltration of glioblastoma. Stem Cells Dev 2012, 21:2753-2761.
56. Kreisl T.N., et al. Phase II trial of single-agent bevacizumab followed by bevacizumab plus irinotecan at tumor progression in recurrent glioblastoma. J. Clin. Oncol 2009, 27:740-745.
57. Møller S., et al. A phase II trial with bevacizumab and irinotecan for patients with primary brain tumors and progression after standard therapy. Acta Oncol 2012, 51:797-804.
58. Reardon D.A., et al. Phase II study of carboplatin, irinotecan, and bevacizumab for bevacizumab naïve, recurrent glioblastoma. J. Neurooncol 2012, 107:155-164.
59. Barone A., et al. Combined VEGF and CXCR4 antagonism targets the GBM stem cell population and synergistically improves survival in an intracranial mouse model of glioblastoma. Oncotarget 2014, 5:9811-9822.