Sensitivity of MRI tumor biomarkers to VEGFR inhibitor therapy in an orthotopic mouse glioma model

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Farrar, Christian T ^a   Kamoun, Walid S ^a   Ley, Carsten D ^a   Kim, Young R ^a   Catana, Ciprian ^a   Kwon, Seon J ^a   Rosen, Bruce R ^a   Jain, Rakesh K ^a   Sorensen, A Gregory ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; BOVINE SERUM ALBUMIN; CEDIRANIB; TETRAMETHYLRHODAMINE; TUMOR MARKER; VASCULOTROPIN; 4 ((4 FLUORO 2 METHYL 1H INDOL 5 YL)OXY) 6 METHOXY 7 (3 (PYRROLIDIN 1 YL)PROPOXY)QUINAZOLINE; 4-((4-FLUORO-2-METHYL-1H-INDOL-5-YL)OXY)-6-METHOXY-7-(3-(PYRROLIDIN-1-YL)PROPOXY)QUINAZOLINE; PROTEIN KINASE INHIBITOR; QUINAZOLINE DERIVATIVE; VASCULOTROPIN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; BLOOD VESSEL DIAMETER; BLOOD VESSEL PERMEABILITY; BRAIN BLOOD VOLUME; CONTRAST ENHANCEMENT; CONTROLLED STUDY; DIFFUSION COEFFICIENT; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; EX VIVO STUDY; EXTRACELLULAR SPACE; EXTRAVASCULAR SPACE; GLIOMA; HISTOPATHOLOGY; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OUTCOME ASSESSMENT; PROTEIN SYNTHESIS INHIBITION; RELAXATION TIME; SENSITIVITY AND SPECIFICITY; SURVIVAL RATE; TREATMENT RESPONSE; TUMOR DIAGNOSIS; TUMOR REGRESSION; TUMOR VOLUME; ANIMAL; CAPILLARY PERMEABILITY; CELL PROLIFERATION; DIFFUSION; DISEASE MODEL; DRUG ANTAGONISM; HUMAN; METABOLISM; METHODOLOGY; PATHOLOGY; PATHOPHYSIOLOGY; TUMOR CELL LINE; VASCULARIZATION;

ANIMALIA; MUS;

ANIMALS; CAPILLARY PERMEABILITY; CELL LINE, TUMOR; CELL PROLIFERATION; DIFFUSION; DISEASE MODELS, ANIMAL; EXTRACELLULAR SPACE; GLIOMA; HUMANS; MAGNETIC RESONANCE IMAGING; MICE; PROTEIN KINASE INHIBITORS; QUINAZOLINES; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; TUMOR MARKERS, BIOLOGICAL;

EID: 79952307327     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017228     Document Type: Article

References (50)

1. Aronen HJ, Gazit IE, Louis DN, Buchbinder BR, Pardo FS, et al. (1994) Cerebral blood volume maps of gliomas: comparison with tumor grade and histologic findings. Radiology 191: 41-51.
2. Donahue KM, Krouwer HGJ, Rand SD, Pathak AP, Marszalkowski CS, et al. (2000) Utility of simultaneously acquired gradient-echo and spin-echo cerebral blood volume and morphology maps in brain tumor patients. Magn Reson Med 43: 845-853.
3. Schmainda KM, Rand SD, Joseph AM, Lund R, Ward BD, et al. (2004) Characterization of a first-pass gradient-echo spin-echo method to predict brain tumor grade and angiogenesis. Am J Neuroradiol 25: 1524-1532.
4. Dennie J, Mandeville JB, Boxerman JL, Packard SD, Rosen BR, et al. (1998) NMR imaging of changes in vascular morphology due to tumor angiogenesis. Magn Reson Med 40: 793-799.
5. Tropres I, Grimault S, Vaeth A, Grillon E, Julien C, et al. (2001) Vessel Size Imaging. Magn Reson Med 45: 397-408.
6. Badruddoja MA, Krouwer HGJ, Rand SD, Rebro KJ, Pathak AP, et al. (2003) Antiangiogenic effects of dexamethasone in 9L gliosarcoma assesed by MRI cerebral blood volume maps. Neuro-Oncology 5: 235-243.
7. Batchelor TT, Sorensen AG, Tomaso Ed, Zhang W, Duda DG, et al. (2007) AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 11: 83-95.
8. Valable S, Lemasson B, Farion R, Beaumont M, Segebarth C, et al. (2008) Assessment of blood volume, vessel size, and the expression of angiogenic factors in two rat glioma models: a longitudinal in vivo and ex vivo study. NMR Biomed 21: 1043-1056.
9. Ostergaard L, Hochberg FH, Rabinov JD, Sorensen AG, Lev M, et al. (1999) Early chnages measured by magnetic resonance imaging in cerebral blood flow, blood volume, and blood-brain barrier permeability following dexamethasone treatment in patients with brain tumors. J Neurosurg 90: 300-305.
10. Ferretti S, Allegrini PR, O'Reilly T, Schnell C, Stumm M, et al. (2005) Patupilone induced vascular disruption in orthotopic rodent tumor models detected by magnetic resonance imaging and interstitial fluid pressure. Clin Cancer Res 11: 7773-7784.
11. Oh J, Cha S, Aiken AH, Han ET, Crane JC, et al. (2005) Quantitative apparent diffusion coefficients and T2 relaxation times in characterizing contrast enhancing brain tumors and regions of peritumoral edema. J Magn Reson Imaging 21: 701-708.
12. Eis M, Els T, Hoehn-Berlage M, (1995) High resolution quantitative relaxation and diffusion MRI of three different experimental brain tumors in rat. Magn Reson Med 34: 835-844.
13. Tofts PS, Kermode AG, (1991) Measurement of the blood-brain barrier permeability and leakage space using dynamic MR imaging. 1. Fundamental concepts. Magn Reson Med 17: 357-367.
14. Tofts PS, (1997) Modeling tracer kinetics in dynamic Gd-DTPA MR imaging. J Magn Reson Imaging 7: 91-101.
15. Tofts P, Brix G, Buckley D, Evelhoch J, Henderson E, et al. (1999) Estimating kinetic parameters from dynamic contrast-enhanced T1-weighted MRI of diffusable tracer: standardized quantities and symbols. J Magn Reson Imag 10: 223-232.
16. Padhani AR, (2002) Dynamic contrast-enhanced MRI in clinical oncology: current status and future directions. J Magn Reson Imaging 16: 407-422.
17. Hylton N, (2006) Dynamic contrast-enhanced magnetic resonance imaging as an imaging biomarker. J Clin Oncol 24: 3293-3298.
18. Yankeelov TE, Gore JC, (2009) Dynamic Contrast Enhanced Magnetic Resonance Imaging in Oncology: Theory, Data Acquisition, Analysis, and Examples. Curr Med Imaging Rev 3: 91-107.
19. Wedge SR, Kendrew J, Hennequin LF, Valentine PJ, Barry ST, et al. (2005) AZD2171: a highly potent, orally bioavailable, vascular endothelial growth factor receptor-2 tyrosine kinase inhibitor for the treatment of cancer. Cancer Res 65: 4389-4400.
20. Kamoun WS, Ley CD, Farrar CT, Duyverman AM, Lahdenranta J, et al. (2009) Edema control by cediranib, a vascular endothelial growth factor receptor-targeted kinase inhibitor, prolongs survival despite persistent brain tumor growth in mice. J Clin Oncol 27: 2542-2552.
21. Packard SD, Mandeville JB, Ichikawa T, Ikeda K, Terada K, et al. (2003) Functional response of tumor vasculature to PaCO2: determination of total and microvascular blood volume by MRI. Neoplasia 5: 330-338.
22. Tropres I, Lamalle L, Peoc'h M, Farion R, Usson Y, et al. (2004) In vivo assesment of tumoral angiogenesis. Magn Reson Med 51: 533-541.
23. Kiselev VG, Strecker R, Ziyeh S, Speck O, Hennig J, (2005) Vessel size imaging in humans. Magn Reson Med 53: 553-563.
24. Carmeliet P, Jain RK, (2000) Angiogenesis in cancer and other diseases. Nature 407: 249-257.
25. Brown EB, Campbell RB, Tsuzuki Y, Xu L, Carmeliet P, et al. (2001) In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy. Nat Med 7: 864-868.
26. Jain RK, di Tomaso E, Duda DG, Loeffler JS, Sorensen AG, et al. (2007) Angiogenesis in brain tumours. Nat Rev Neurosci 8: 610-622.
27. Lyng H, Haraldseth O, Rofstad EK, (2000) Measurement of cell density and necrotic fraction in human melanoma xenografts by diffusion weighted magnetic resonance imaging. Magn Reson Med 43: 828-836.
28. Kono K, Inoue Y, Nakayama K, Shakudo M, Morino M, et al. (2001) The role of diffusion-weighted imaging in patients with brain tumors. AJNR Am J Neuroradiol 22: 1081-1088.
29. Sugahara T, Korogi Y, Kochi M, Ikushima I, Shigematu Y, et al. (1999) Usefulness of diffusion-weighted MRI with echo-planar technique in the evaluation of cellularity in gliomas. J Magn Reson Imaging 9: 53-60.
30. Chenevert TL, McKeever PE, Ross BD, (1997) Monitoring early response of experimental brain tumors to therapy using diffusion magnetic resonance imaging. Clin Cancer Res 3: 1457-1466.
31. Chenevert TL, Stegman LD, Taylor JM, Robertson PL, Greenberg HS, et al. (2000) Diffusion magnetic resonance imaging: an early surrogate marker of therapeutic efficacy in brain tumors. J Natl Cancer Inst 92: 2029-2036.
32. Hall DE, Moffat BA, Stojanovska J, Johnson TD, Li Z, et al. (2004) Therapeutic efficacy of DTI-015 using diffusion magnetic resonance imaging as an early surrogate marker. Clin Cancer Res 10: 7852-7859.
33. Moffat BA, Chenevert TL, Lawrence TS, Meyer CR, Johnson TD, et al. (2005) Functional diffusion map: a noninvasive MRI biomarker for early stratification of clinical brain tumor response. Proc Natl Acad Sci U S A 102: 5524-5529.
34. Ross BD, Moffat BA, Lawrence TS, Mukherji SK, Gebarski SS, et al. (2003) Evaluation of cancer therapy using diffusion magnetic resonance imaging. Mol Cancer Ther 2: 581-587.
35. Szafer A, Zhong J, Gore J, (1995) Theoretical model for water diffusion in tissues. Magn Reson Med 33: 697-712.
36. Gerstner ER, Frosch MP, Batchelor TT, (2010) Diffusion magnetic resonance imaging detects pathologically confirmed, nonenhancing tumor progression in a patient with recurrent glioblastoma receiving bevacizumab. J Clin Oncol 28: e91-93.
37. Yuan F, Salehi HA, Boucher Y, Vasthare US, Tuma RF, et al. (1994) Vascular permeability and microcirculation of gliomas and mammary carcinomas transplanted in rat and mouse cranial windows. Cancer Res 54: 4564-4568.
38. Jain RK, Munn LL, Fukumura D, (2002) Dissecting tumour pathophysiology using intravital microscopy. Nat Rev Cancer 2: 266-276.
39. Tyrrell JA, di Tomaso E, Fuja D, Tong R, Kozak K, et al. (2007) Robust 3-D modeling of vasculature imagery using superellipsoids. IEEE Trans Med Imaging 26: 223-237.
40. McGrath DM, Bradley DP, Tessier JL, Lacey T, Taylor CJ, et al. (2009) Comparison of model-based arterial input functions for dynamic contrast-enhanced MRI in tumor bearing rats. Magn Reson Med 61: 1173-1184.
41. Jain RK, Duda DG, Willett CG, Sahani DV, Zhu AX, et al. (2009) Biomarkers of response and resistance to antiangiogenic therapy. Nat Rev Clin Oncol 6: 327-338.
42. Sorensen AG, Batchelor TT, Zhang WT, Chen PJ, Yeo P, et al. (2009) A "vascular normalization index" as potential mechanistic biomarker to predict survival after a single dose of cediranib in recurrent glioblastoma patients. Cancer Res 69: 5296-5300.
43. Pathak AP, Rand SD, Schmainda KM, (2003) The effect of brain tumor angiogenesis on the in vivo relationship between the gradient-echo relaxation rate change (ΔR2*) and contrast agent (MION) dose. J Magn Reson Imaging 18: 397-403.
44. Pathak AP, Ward BD, Schmainda KM, (2008) A novel technique for modeling susceptibility-based contrast mechanisms for arbitrary microvascular geometries: the finite perturber method. Neuroimage 40: 1130-1143.
45. Weisskoff RM, Zuo CS, Boxerman JL, Rosen BR, (1994) Microscopic susceptibility variation and transverse relaxation: Theory and experiment. Magn Reson Med 31: 601-610.
46. Boxerman JL, Hamberg LM, Rosen BR, Weisskoff RM, (1995) MR contrast due to intravascular magnetic susceptibility perturbations. Magn Reson Med 34: 555-566.
47. Holash J, Maisonpierre PC, Compton D, Boland P, Alexander CR, et al. (1999) Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF. Science 284: 1994-1998.
48. Yankeelov TE, Luci JJ, Lepage M, Li R, Debusk L, et al. (2005) Quantitative pharmacokinetic analysis of DCE-MRI data without an arterial input function: a reference region model. Magn Reson Imaging 23: 519-529.
49. Parker GJ, Roberts C, Macdonald A, Buonaccorsi GA, Cheung S, et al. (2006) Experimentally-derived functional form for a population-averaged high-temporal-resolution arterial input function for dynamic contrast-enhanced MRI. Magn Reson Med 56: 993-1000.
50. Buckley DL, Roberts C, Parker GJ, Logue JP, Hutchinson CE, (2004) Prostate cancer: evaluation of vascular characteristics with dynamic contrast-enhanced T1-weighted MR imaging-initial experience. Radiology 233: 709-715.