Hyperpolarized 13C MR spectroscopic imaging can be used to monitor Everolimus treatment in vivo in an orthotopic rodent model of glioblastoma

NeuroImage

Volumn 59, Issue 1, 2012, Pages 193-201

  Chaumeil, Myriam M ^a   Ozawa, Tomoko ^a   Park, IlWoo ^a   Scott, Kristen ^a   James, C David ^a   Nelson, Sarah J ^a   Ronen, Sabrina M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Carbon 13 13C; Everolimus; Glioblastoma; Hyperpolarization; MRSI; MTOR inhibition

Indexed keywords

CARBONATE DEHYDRATASE IX; EVEROLIMUS; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LACTATE DEHYDROGENASE; LACTIC ACID; PYRUVIC ACID; ANTINEOPLASTIC AGENT; CARBON; DRUG DERIVATIVE; RAPAMYCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN LEVEL; BRAIN METABOLISM; CANCER INHIBITION; CARBON NUCLEAR MAGNETIC RESONANCE; CONTROLLED STUDY; DRUG MECHANISM; DRUG RESPONSE; GLIOBLASTOMA; HYPERPOLARIZATION; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MALE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TUMOR VOLUME; ANIMAL; BRAIN TUMOR; DISEASE MODEL; DRUG SCREENING; HUMAN; METHODOLOGY; NEUROIMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUDE RAT;

ANIMALS; ANTINEOPLASTIC AGENTS; BRAIN NEOPLASMS; CARBON RADIOISOTOPES; DISEASE MODELS, ANIMAL; GLIOBLASTOMA; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MALE; NEUROIMAGING; RATS; RATS, NUDE; SIROLIMUS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 81155160947     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.07.034     Document Type: Article

References (49)

1. Akhavan D., Cloughesy T.F., Mischel P.S. mTOR signaling in glioblastoma: lessons learned from bench to bedside. Neuro Oncol. 2010, 12(8):882-889.
2. 13C lactate, pyruvate, and alanine: noninvasive biomarkers for prostate cancer detection and grading. Cancer Res. 2008, 68(20):8607-8615.
3. Ardenkjaer-Larsen J.H., Fridlund B., Gram A., Hansson G., Hansson L., Lerche M.H., Servin R., Thaning M., Golman K. Increase in signal-to-noise ratio of >10,000 times in liquid-state NMR. Proc. Natl. Acad. Sci. U. S. A. 2003, 100(18):10158-10163.
4. Belda-Iniesta C., de Castro Carpeno J., Sereno M., Gonzalez-Baron M., Perona R. Epidermal growth factor receptor and glioblastoma multiforme: molecular basis for a new approach. Clin. Transl. Oncol. 2008, 10(2):73-77.
5. Bunney T.D., Katan M. Phosphoinositide signalling in cancer: beyond PI3K and PTEN. Nat. Rev. Cancer 2010, 10(5):342-352.
6. Byrnes T.J., Barrick T.R., Bell B.A., Clark C.A. Diffusion tensor imaging discriminates between glioblastoma and cerebral metastases in vivo. NMR Biomed. 2011, 24(1):54-60.
7. CBRTUS Statistical report - Primary brain and central nervous system tumors diagnosed in the United states in 2004-2006 Available from:. http://seer.cancer.gov/.
8. CGARN Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 2008, 455(7216):1061-1068.
9. Chen A.P., Albers M.J., Cunningham C.H., Kohler S.J., Yen Y.F., Hurd R.E., Tropp J., Bok R., Pauly J.M., Nelson S.J., Kurhanewicz J., Vigneron D.B. Hyperpolarized C-13 spectroscopic imaging of the TRAMP mouse at 3T-initial experience. Magn. Reson. Med. 2007, 58(6):1099-1106.
10. 18F] fluorothymidine positron emission tomography: a pilot study. J. Clin. Oncol. 2007, 25(30):4714-4721.
11. Clarke J., Butowski N., Chang S. Recent advances in therapy for glioblastoma. Arch. Neurol. 2010, 67(3):279-283.
12. Cleary J.M., Shapiro G.I. Development of phosphoinositide-3 kinase pathway inhibitors for advanced cancer. Curr. Oncol. Rep. 2010, 12(2):87-94.
13. 13C. J. Magn. Reson. 2007, 187(2):357-362.
14. 13C magnetic resonance imaging and spectroscopy. Nat. Med. 2007, 13(11):1382-1387.
15. di Tomaso E., Snuderl M., Kamoun W.S., Duda D.G., Auluck P.K., Fazlollahi L., Andronesi O.C., Frosch M.P., Wen P.Y., Plotkin S.R., Hedley-Whyte E.T., Sorensen A.G., Batchelor T.T., Jain R.K. Glioblastoma recurrence after cediranib therapy in patients: lack of "rebound" revascularization as mode of escape. Cancer Res. 2011, 71(1):19-28.
16. Ellingson B.M., Cloughesy T.F., Lai A., Nghiemphu P.L., Liau L.M., Pope W.B. High order diffusion tensor imaging in human glioblastoma. Acad. Radiol. 2011, 8(8):947-954.
17. Firth J.D., Ebert B.L., Ratcliffe P.J. Hypoxic regulation of lactate dehydrogenase A. Interaction between hypoxia-inducible factor 1 and cAMP response elements. J. Biol. Chem. 1995, 270(36):21021-21027.
18. 13C magnetic resonance imaging for in vivo tumor diagnosis. Cancer Res. 2006, 66(22):10855-10860.
19. Goudar R.K., Shi Q., Hjelmeland M.D., Keir S.T., McLendon R.E., Wikstrand C.J., Reese E.D., Conrad C.A., Traxler P., Lane H.A., Reardon D.A., Cavenee W.K., Wang X.F., Bigner D.D., Friedman H.S., Rich J.N. Combination therapy of inhibitors of epidermal growth factor receptor/vascular endothelial growth factor receptor 2 (AEE788) and the mammalian target of rapamycin (RAD001) offers improved glioblastoma tumor growth inhibition. Mol. Cancer Ther. 2005, 4(1):101-112.
20. Gunther H.S., Schmidt N.O., Phillips H.S., Kemming D., Kharbanda S., Soriano R., Modrusan Z., Meissner H., Westphal M., Lamszus K. Glioblastoma-derived stem cell-enriched cultures form distinct subgroups according to molecular and phenotypic criteria. Oncogene 2008, 27(20):2897-2909.
21. Hu S., Lustig M., Balakrishnan A., Larson P.E., Bok R., Kurhanewicz J., Nelson S.J., Goga A., Pauly J.M., Vigneron D.B. 3D compressed sensing for highly accelerated hyperpolarized (13)C MRSI with in vivo applications to transgenic mouse models of cancer. Magn. Reson. Med. 2010, 63(2):312-321.
22. 13C]pyruvic acid at 4.6tesla. J. Magn. Reson. 2009, 197(2):167-175.
23. Larson P.E., Hu S., Lustig M., Kerr A.B., Nelson S.J., Kurhanewicz J., Pauly J.M., Vigneron D.B. Fast dynamic 3D MR spectroscopic imaging with compressed sensing and multiband excitation pulses for hyperpolarized (13) C studies. Magn. Reson. Med. 2011, 65(3):610-619.
24. Leenders W.P., Kusters B., de Waal R.M. Vessel co-option: how tumors obtain blood supply in the absence of sprouting angiogenesis. Endothelium 2002, 9(2):83-87.
25. Louis D.N., Ohgaki H., Wiestler O.D., Cavenee W.K., Burger P.C., Jouvet A., Scheithauer B.W., Kleihues P. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007, 114(2):97-109.
26. Minniti G., Muni R., Lanzetta G., Marchetti P., Enrici R.M. Chemotherapy for glioblastoma: current treatment and future perspectives for cytotoxic and targeted agents. Anticancer. Res. 2009, 29(12):5171-5184.
27. Monazzam A., Razifar P., Ide S., Rugaard Jensen M., Josephsson R., Blomqvist C., Langstrom B., Bergstrom M. Evaluation of the Hsp90 inhibitor NVP-AUY922 in multicellular tumour spheroids with respect to effects on growth and PET tracer uptake. Nucl. Med. Biol. 2009, 36(3):335-342.
28. Nelson S.J. Analysis of volume MRI and MR spectroscopic imaging data for the evaluation of patients with brain tumors. Magn. Reson. Med. 2001, 46(2):228-239.
29. Nguyen T.D., Lassman A.B., Lis E., Rosen N., Shaffer D.R., Scher H.I., Deangelis L.M., Abrey L.E. A pilot study to assess the tolerability and efficacy of RAD-001 (everolimus) with gefitinib in patients with recurrent glioblastoma multiforme (GBM). J. Clin. Oncol. 2006, 24(18S).
30. Ozawa T., Wang J., Hu L.J., Bollen A.W., Lamborn K.R., Deen D.F. Growth of human glioblastomas as xenografts in the brains of athymic rats. In Vivo 2002, 16(1):55-60.
31. Ozawa T., Faddegon B.A., Hu L.J., Bollen A.W., Lamborn K.R., Deen D.F. Response of intracerebral human glioblastoma xenografts to multifraction radiation exposures. Int. J. Radiat. Oncol. Biol. Phys. 2006, 66(1):263-270.
32. 13C magnetic resonance metabolic imaging: application to brain tumors. Neuro Oncol. 2010, 12(2):133-144.
33. Phelps M.E., Mazziotta J.C. Positron emission tomography: human brain function and biochemistry. Science 1985, 228(4701):799-809.
34. Pope W.B., Lai A., Mehta R., Kim H.J., Qiao J., Young J.R., Xue X., Goldin J., Brown M.S., Nghiemphu P.L., Tran A., Cloughesy T.F. Apparent diffusion coefficient histogram analysis stratifies progression-free survival in newly diagnosed bevacizumab-treated glioblastoma. AJNR Am. J. Neuroradiol. 2011, 32(5):882-889.
35. Pouyssegur J., Dayan F., Mazure N.M. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 2006, 441(7092):437-443.
36. Saksena S., Jain R., Narang J., Scarpace L., Schultz L.R., Lehman N.L., Hearshen D., Patel S.C., Mikkelsen T. Predicting survival in glioblastomas using diffusion tensor imaging metrics. J. Magn. Reson. Imaging 2010, 32(4):788-795.
37. Sarkaria J.N., Yang L., Grogan P.T., Kitange G.J., Carlson B.L., Schroeder M.A., Galanis E., Giannini C., Wu W., Dinca E.B., James C.D. Identification of molecular characteristics correlated with glioblastoma sensitivity to EGFR kinase inhibition through use of an intracranial xenograft test panel. Mol. Cancer Ther. 2007, 6(3):1167-1174.
38. Sarkaria J.N., Galanis E., Wu W., Peller P.J., Giannini C., Brown P.D., Uhm J.H., McGraw S., Jaeckle K.A., Buckner J.C. North central cancer treatment group phase I trial N057K of Everolimus (RAD001) and temozolomide in combination with radiation therapy in patients with newly diagnosed glioblastoma multiforme. Int. J. Radiat. Oncol. Biol. Phys. 2011, 82(2):468-475.
39. Stupp R., Mason W.P., van den Bent M.J., Weller M., Fisher B., Taphoorn M.J., Belanger K., Brandes A.A., Marosi C., Bogdahn U., Curschmann J., Janzer R.C., Ludwin S.K., Gorlia T., Allgeier A., Lacombe D., Cairncross J.G., Eisenhauer E., Mirimanoff R.O. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 2005, 352(10):987-996.
40. Stupp R., Hegi M.E., Mason W.P., van den Bent M.J., Taphoorn M.J., Janzer R.C., Ludwin S.K., Allgeier A., Fisher B., Belanger K., Hau P., Brandes A.A., Gijtenbeek J., Marosi C., Vecht C.J., Mokhtari K., Wesseling P., Villa S., Eisenhauer E., Gorlia T., Weller M., Lacombe D., Cairncross J.G., Mirimanoff R.O. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009, 10(5):459-466.
41. Stupp R., Tonn J.C., Brada M., Pentheroudakis G. High-grade malignant glioma: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann. Oncol. 2010, 21(Suppl 5):v190-v193.
42. Tropp J., Lupo J.M., Chen A., Calderon P., McCune D., Grafendorfer T., Ozturk-Isik E., Larson P.E., Hu S., Yen Y.F., Robb F., Bok R., Schulte R., Xu D., Hurd R., Vigneron D., Nelson S. Multi-channel metabolic imaging, with SENSE reconstruction, of hyperpolarized [1-(13)C] pyruvate in a live rat at 3.0tesla on a clinical MR scanner. J. Magn. Reson. 2011, 208(1):171-177.
43. Viale A., Aime S. Current concepts on hyperpolarized molecules in MRI. Curr. Opin. Chem. Biol. 2010, 14(1):90-96.
44. Warburg O. On the origin of cancer cells. Science 1956, 123(3191):309-314.
45. 13C magnetic resonance spectroscopy. Cancer Res. 2010, 70(4):1296-1305.
46. Wei L.H., Su H., Hildebrandt I.J., Phelps M.E., Czernin J., Weber W.A. Changes in tumor metabolism as readout for mammalian target of rapamycin kinase inhibition by rapamycin in glioblastoma. Clin. Cancer Res. 2008, 14(11):3416-3426.
47. Witney T.H., Kettunen M.I., Day S.E., Hu D.E., Neves A.A., Gallagher F.A., Fulton S.M., Brindle K.M. A comparison between radiolabeled fluorodeoxyglucose uptake and hyperpolarized (13)C-labeled pyruvate utilization as methods for detecting tumor response to treatment. Neoplasia 2009, 11(6):574-582. 571 p following 582.
48. Workman P., Clarke P.A., Guillard S., Raynaud F.I. Drugging the PI3 kinome. Nat. Biotechnol. 2006, 24(7):794-796.
49. Yang L., Clarke M.J., Carlson B.L., Mladek A.C., Schroeder M.A., Decker P., Wu W., Kitange G.J., Grogan P.T., Goble J.M., Uhm J., Galanis E., Giannini C., Lane H.A., James C.D., Sarkaria J.N. PTEN loss does not predict for response to RAD001 (Everolimus) in a glioblastoma orthotopic xenograft test panel. Clin. Cancer Res. 2008, 14(12):3993-4001.