MRI biomarkers identify the differential response of glioblastoma multiforme to anti-angiogenic therapy

Neuro-Oncology

Volumn 16, Issue 6, 2014, Pages 868-879

  Jalali, Shahrzad ^a   Chung, Caroline ^b   Foltz, Warren ^b,c   Burrell, Kelly ^a   Singh, Sanjay ^a   Hill, Richard ^b,c   Zadeh, Gelareh ^a,d  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b PRINCESS MARGARET HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d TORONTO WESTERN HOSPITAL   (Canada)

Author keywords

anti angiogenic therapies; glioblastoma multiforme (GBM); MRI biomarker

Indexed keywords

AFLIBERCEPT; ANGIOGENESIS INHIBITOR; B 20; BIOLOGICAL MARKER; CONTRAST MEDIUM; SUNITINIB; UNCLASSIFIED DRUG; BEVACIZUMAB; HYBRID PROTEIN; INDOLE DERIVATIVE; MONOCLONAL ANTIBODY; PYRROLE DERIVATIVE; VASCULOTROPIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC THERAPY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BLOOD VESSEL PERMEABILITY; BRAIN BLOOD FLOW; CANCER CHEMOTHERAPY; CANCER RADIOTHERAPY; CELL DENSITY; CELL PROLIFERATION; CHEMORADIOTHERAPY; CONE BEAM COMPUTED TOMOGRAPHY; CONE BEAM COMPUTED TOMOGRAPHY SCANNER; CONTRAST ENHANCEMENT; CONTROLLED STUDY; DIFFUSION COEFFICIENT; DRUG RESPONSE; EXPERIMENTAL NEOPLASM; GLIOBLASTOMA; GROWTH RATE; HUMAN; HUMAN CELL; IMAGE GUIDED RADIOTHERAPY; IMAGING SOFTWARE; IMMUNOHISTOCHEMISTRY; LASER MICROSCOPY; MONOTHERAPY; MOUSE; MOUSE MODEL; MURINAE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; RADIATION DOSE FRACTIONATION; RADIOFREQUENCY; RADIOTHERAPY UNIT; TUMOR GROWTH; TUMOR MODEL; TUMOR VASCULARIZATION; TUMOR VOLUME; TUMOR XENOGRAFT; ANIMAL; BRAIN NEOPLASMS; IMAGE PROCESSING; MULTIMODALITY CANCER THERAPY; PATHOLOGY; TUMOR CELL LINE;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; BIOLOGICAL MARKERS; BRAIN NEOPLASMS; CELL LINE, TUMOR; COMBINED MODALITY THERAPY; GLIOBLASTOMA; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INDOLES; MAGNETIC RESONANCE IMAGING; MICE; PYRROLES; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; RECOMBINANT FUSION PROTEINS;

EID: 84901038490     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/nou040     Document Type: Article

References (45)

1. Wen PY, Kesari S. Malignant gliomas in adults. N Engl J Med. 2008; 359(5):492-507.
2. Huse JT, Holland EC. Targeting brain cancer: advances in the molecular pathology of malignant glioma and medulloblastoma. Nat Rev Cancer. 2010;10(5):319-331.
3. Jain RK, di Tomaso E, Duda DG, et al. Angiogenesis in brain tumours. Nat Rev Neurosci. 2007;8(8):610-622.
4. Butowski N. Anti-angiogenic therapy in glioma. Clin Transl Oncol. 2011;13(5):294-300.
5. Argyriou AA, Giannopoulou E, Kalofonos HP. Angiogenesis and anti-angiogenic molecularly targeted therapies in malignant gliomas. Oncology. 2009;77(1):1-11.
6. Vredenburgh JJ, Desjardins A, Herndon JE 2nd, et al., Phase II trial of bevacizumab and irinotecan in recurrent malignant glioma. Clin Cancer Res. 2007;13(4):1253-1259.
7. Jain RK, Duda DG, Clark JW, et al. Lessons from phase III clinical trials on anti-VEGF therapy for cancer. Nat Clin Pract Oncol. 2006;3(1): 24-40.
8. Wachsberger PR, Burd R, Cardi C, et al. VEGF trap in combination with radiotherapy improves tumor control in u87 glioblastoma. Int J Radiat Oncol Biol Phys. 2007;67(5):1526-1537.
9. Gomez-Manzano C, Holash J, Fueyo J, et al. VEGF Trap induces antiglioma effect at different stages of disease. Neuro Oncol. 2008; 10(6):940-945.
10. Roskoski R Jr. Sunitinib: a VEGF and PDGF receptor protein kinase and angiogenesis inhibitor. Biochem Biophys Res Commun. 2007;356(2): 323-328.
11. de Bouard S, Herlin P, Christensen JG, et al. Antiangiogenic and anti-invasive effects of sunitinib on experimental human glioblastoma. Neuro Oncol. 2007;9(4):412-423.
12. Schueneman AJ, Himmelfarb E, Geng L, et al. SU11248 maintenance therapy prevents tumor regrowth after fractionated irradiation of murine tumor models. Cancer Res. 2003;63(14):4009-4016.
13. de Groot JF, Fuller G, Kumar AJ, et al. Tumor invasion after treatment of glioblastoma with bevacizumab: radiographic and pathologic correlation in humans and mice. Neuro Oncol. 2010;12(3): 233-242.
14. Lu KV, Chang JP, Parachoniak CA, et al. VEGF Inhibits Tumor Cell Invasion and Mesenchymal Transition through a MET/VEGFR2 Complex. Cancer Cell. 2012;22(1):21-35.
15. Reardon DA, Vredenburgh JJ, Coan A, et al. Phase I study of sunitinib and irinotecan for patients with recurrent malignant glioma. J Neurooncol. 2011;105(3):621-627.
16. de Groot JF, Lamborn KR, Chang SM, et al. Phase II study of aflibercept in recurrent malignant glioma: a North American Brain Tumor Consortium study. J Clin Oncol. 2011;29(19):2689-2695.
17. 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(3):491-501.
18. Lee CG, Heijn M, di Tomaso E, et al. Anti-Vascular endothelial growth factor treatment augments tumor radiation response under normoxic or hypoxic conditions. Cancer Res. 2000;60(19): 5565-5570.
19. Narayana A, Gruber D, Kunnakkat S, et al. A clinical trial of bevacizumab, temozolomide, and radiation for newly diagnosed glioblastoma. J Neurosurg. 2012;116(2):341-345.
20. Calli C, Kitis O, Yunten N, et al. Perfusion and diffusion MR imaging in enhancing malignant cerebral tumors. Eur J Radiol. 2006;58(3): 394-403.
21. Hylton N. Dynamic contrast-enhanced magnetic resonance imaging as an imaging biomarker. J Clin Oncol. 2006;24(20):3293-3298.
22. Jenkinson MD, Du Plessis DG, Walker C, et al. Advanced MRI in the management of adult gliomas. Br J Neurosurg. 2007;21(6): 550-561.
23. Essock-Burns E, Lupo JM, Cha S, et al. Assessment of perfusion MRI-derived parameters in evaluating and predicting response to antiangiogenic therapy in patients with newly diagnosed glioblastoma. Neuro Oncol. 2011;13(1):119-131.
24. Pope WB, Qiao XJ, Kim HJ, et al. Apparent diffusion coefficient histogram analysis stratifies progression-free and overall survival in patients with recurrent GBM treated with bevacizumab: a multi-center study. J Neurooncol. 2012;108(3):491-498.
25. Lee J, Kotliarova S, Kotliarov Y, et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell. 2006;9(5):391-403.
26. Woltjen K, Michael IP, Mohseni P, et al. piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature. 2009;458(7239):766-770.
27. Zadeh G, Reti R, Koushan K, et al. Regulation of the pathological vasculature of malignant astrocytomas by angiopoietin-1. Neoplasia. 2005;7(12):1081-1090.
28. Ebos JM, Lee CR, Christensen JG, et al. Multiple circulating proangiogenic factors induced by sunitinib malate are tumor-independent and correlate with antitumor efficacy. Proc Natl Acad Sci USA. 2007;104(43):17069- 17074.
29. Chung C, Jalali S, Foltz W, et al. Imaging Biomarker Dynamics in an Intracranial Murine Glioma Study of Radiation and Antiangiogenic Therapy. Int J Radiat Oncol Biol Phys. 2013;85(3):805-812.
30. Burrell K, Hill RP, Zadeh G. High-resolution in-vivo analysis of normal brain response to cranial irradiation. PLoS One. 2012;7(6):e38366.
31. O'Connor JP, Jackson A, Parker GJ, et al. DCE-MRI biomarkers in the clinical evaluation of antiangiogenic and vascular disrupting agents. Br J Cancer. 2007;96(2):189-195.
32. Zadeh G, Guha A. Neoangiogenesis in human astrocytomas: expression and functional role of angiopoietins and their cognate receptors. Front Biosci. 2003;8:e128-e137.
33. McGee MC, Hamner JB, Williams RF, et al. Improved intratumoral oxygenation through vascular normalization increases glioma sensitivity to ionizing radiation. Int J Radiat Oncol Biol Phys. 2010; 76(5):1537-1545.
34. Rosenzweig SA. Acquired resistance to drugs targeting receptor tyrosine kinases. Biochem Pharmacol. 2012;83(8):1041-1048.
35. Bammer R. Basic principles of diffusion-weighted imaging. Eur J Radiol. 2003;45(3):169-184.
36. Eccles CL, Haider EA, Haider MA, et al. Change in diffusion weighted MRI during liver cancer radiotherapy: preliminary observations. Acta Oncol. 2009;48(7):1034-1043.
37. Larocque MP, Syme A, Yahya A, et al. Temporal and dose dependence of T2 and ADC at 9.4T in a mouse model following single fraction radiation therapy. Med Phys. 2009;36(7):2948-2954.
38. Suh JY, Cho G, Song Y, et al. Is apparent diffusion coefficient reliable and accurate for monitoring effects of antiangiogenic treatment in a longitudinal study?. J Magn Reson Imaging. 2012;35(6):1430-1436.
39. Lemasson B, Christen T, Tizon X, et al. Assessment of multiparametric MRI in a human glioma model to monitor cytotoxic and anti-angiogenic drug effects. NMR Biomed. 2011; 24(5):473-482.
40. Ellingson BM, Cloughesy TF, Lai A, et al. Quantitative volumetric analysis of conventional MRI response in recurrent glioblastoma treated with bevacizumab. Neuro Oncol. 2011;13(4):401-409.
41. Pope WB, Young JR, Ellingson BM. Advances in MRI assessment of gliomas and response to anti-VEGF therapy. Curr Neurol Neurosci Rep. 2011;11(3):336-344.
42. Tofts PS, Brix G, Buckley DL, et al. Estimating kinetic parameters from dynamic contrast-enhanced T(1)-weighted MRI of a diffusable tracer: standardized quantities and symbols. J Magn Reson Imaging. 1999;10(3):223-232.
43. Hoff BA, Bhojani MS, Rudge J, et al. DCE and DW-MRI monitoring of vascular disruption following VEGF-Trap treatment of a rat glioma model. NMR Biomed. 2012;25(7):935-942.
44. Narang J, Jain R, Arbab AS, et al. Differentiating treatment-induced necrosis from recurrent/progressive brain tumor using nonmodel-based semiquantitative indices derived from dynamic contrast-enhanced T1-weighted MR perfusion. Neuro Oncol. 2011; 13(9):1037-1046.
45. Huang H, Bhat A, Woodnutt G, et al. Targeting the ANGPT-TIE2 pathway in malignancy. Nat Rev Cancer. 2010;10(8):575-585.