MR Imaging Features of High-Grade Gliomas in Murine Models: How They Compare with Human Disease, Reflect Tumor Biology, and Play a Role in Preclinical Trials

References

1. 1.↵
   1. Barth RF,
   2. Kaur B

   . Rat brain tumor models in experimental neuro-oncology: the C6, 9L, T9, RG2, F98, BT4C, RT-2 and CNS-1 gliomas. J Neurooncol 2009;94:299–312

   CrossRefPubMed
2. 2.↵
   1. Gutmann DH,
   2. Hunter-Schaedle K,
   3. Shannon KM

   . Harnessing preclinical mouse models to inform human clinical cancer trials. J Clin Invest 2006;116:847–52

   CrossRefPubMedWeb of Science
3. 3.↵
   1. Fomchenko EI,
   2. Holland EC

   . Mouse models of brain tumors and their applications in preclinical trials. Clin Cancer Res 2006;12:5288–97

   Abstract/FREE Full Text
4. 4.↵
   1. Miura FK,
   2. Alves MJ,
   3. Rocha MC,
   4. et al

   . Xenograft transplantation of human malignant astrocytoma cells into immunodeficient rats: an experimental model of glioblastoma. Clinics (Sao Paulo) 2010;65:305–09

   PubMed
5. 5.↵
   1. Taillandier L,
   2. Antunes L,
   3. Angioi-Duprez K.S.

   . Models for neuro-oncological preclinical studies: solid orthotopic and heterotopic grafts of human gliomas into nude mice. J Neurosci Methods 2003;125:147–57

   CrossRefPubMedWeb of Science
6. 6.↵
   1. Wang J,
   2. Miletic H,
   3. Sakariassen PØ,
   4. et al

   . A reproducible brain tumour model established from human glioblastoma biopsies. BMC Cancer 2009;9:465

   CrossRefPubMed
7. 7.↵
   1. Holland EC

   . Brain tumor animal models: importance and progress. Curr Opin Oncol 2001;13:143–47

   CrossRefPubMedWeb of Science
8. 8.↵
   1. Weiss WA,
   2. Israel M,
   3. Cobbs C,
   4. et al

   . Neuropathology of genetically engineered mice: consensus report and recommendations from an international forum. Oncogene 2002;21:453–63
9. 9.↵
   1. Xie Q,
   2. Thompson R,
   3. Hardy K,
   4. et al

   . A highly invasive human glioblastoma pre-clinical model for testing therapeutics. J Transl Med 2008;6:77

   CrossRefPubMed
10. 10.↵
    1. Aldape K,
    2. Colman H,
    3. James C

    . Models of malignant glioma. Drug Discovery Today: Disease Models 2996;3:191–96
11. 11.↵
    1. Smilowitz HM,
    2. Weissenberger J,
    3. Weis J,
    4. et al

    . Orthotopic transplantation of v-src-expressing glioma cell lines into immunocompetent mice: establishment of a new transplantable in vivo model for malignant glioma. J Neurosurg 2007;106:652–59

    CrossRefPubMedWeb of Science
12. 12.↵
    1. Huse JT,
    2. Holland EC

    . Genetically engineered mouse models of brain cancer and the promise of preclinical testing. Brain Pathol 2009;19:132–43

    CrossRefPubMedWeb of Science
13. 13.↵
    1. Marumoto T,
    2. Tashiro A,
    3. Friedmann-Morvinski D,
    4. et al

    . Development of a novel mouse glioma model using lentiviral vectors. Nat Med 2009;15:110–06. Epub 2009 Jan 4

    CrossRefPubMedWeb of Science
14. 14.↵
    1. Masdeu JC,
    2. Bakshi R

    . Neuroimaging: anything to do with neurotherapeutics? NeuroRx 2005;2:163–66

    CrossRefPubMed
15. 15.↵
    1. Lyons SK

    . Advances in imaging mouse tumour models in vivo. J Pathol 2005;205:194–205

    CrossRefPubMedWeb of Science
16. 16.↵
    1. Nieman BJ,
    2. Bock NA,
    3. Bishop J,
    4. et al

    . Magnetic resonance imaging for detection and analysis of mouse phenotypes. NMR Biomed 2005;18:447–68

    CrossRefPubMedWeb of Science
17. 17.↵
    1. Lal S,
    2. Lacroix M,
    3. Tofilon P,
    4. et al

    . An implantable guide-screw system for brain tumor studies in small animals. J Neurosurg 2000;92:326–333

    PubMedWeb of Science
18. 18.↵
    1. Collier LS,
    2. Adams DJ,
    3. Hackett CS,
    4. et al

    . Whole-body sleeping beauty mutagenesis can cause penetrant leukemia/lymphoma and rare high-grade glioma without associated embryonic lethality. Cancer Res 2009;69:8429–37. Epub 2009 Oct 20

    Abstract/FREE Full Text
19. 19.↵
    1. de Groot JF,
    2. Fuller G,
    3. Kumar AJ,
    4. et al

    . Tumor invasion after treatment of glioblastoma with bevacizumab: radiographic and pathologic correlation in humans and mice. Neuro Oncol 2010;12:233–42. Epub 2010 Jan 6

    Abstract/FREE Full Text
20. 20.↵
    1. Radaelli E,
    2. Ceruti R,
    3. Patton V,
    4. et al

    . Immunohistopathological and neuroimaging characterization of murine orthotopic xenograft models of glioblastoma multiforme recapitulating the most salient features of human disease. Histol Histopathol 2009;24:879–91

    PubMed
21. 21.↵
    1. Johnson GA,
    2. Cofer GP,
    3. Gewalt SL,
    4. et al

    . Morphologic phenotyping with MR microscopy: the visible mouse. Radiology 2002;222:789–93

    PubMedWeb of Science
22. 22.↵
    1. Dazai J,
    2. Bock NA,
    3. Nieman BJ,
    4. et al

    . Multiple mouse biological loading and monitoring system for MRI. Magn Reson Med 2004;52:709–15

    CrossRefPubMedWeb of Science
23. 23.↵
    1. Righi V,
    2. Roda JM,
    3. Paz J,
    4. et al

    . 1H HR-MAS and genomic analysis of human tumor biopsies discriminate between high and low grade astrocytomas. NMR Biomed 2009;22:629–37

    CrossRefPubMedWeb of Science
24. 24.↵
    1. Jost SC,
    2. Wanebo JE,
    3. Song SK,
    4. et al

    . In vivo imaging in a murine model of glioblastoma. Neurosurgery 2007;60:360–70, discussion 370–71

    PubMed
25. 25.↵
    1. Radaelli E,
    2. Ceruti R,
    3. Patton V,
    4. et al

    . Immunohistopathological and neuroimaging characterization of murine orthotopic xenograft models of glioblastoma multiforme recapitulating the most salient features of human disease. Histol Histopathol 2009;24:879–91

    PubMed
26. 26.↵
    1. Koutcher JA,
    2. Hu X,
    3. Xu S,
    4. et al

    . MRI of mouse models for gliomas shows similarities to humans and can be used to identify mice for preclinical trials. Neoplasia 2002;4:480–85

    CrossRefPubMed
27. 27.↵
    1. Gordon J,
    2. Mohamed F,
    3. Vinitski S,
    4. et al

    . Utilization of experimental animal model for correlative multispectral MRI and pathological analysis of brain tumors. Magn Reson Imaging 1999;17:1495–502

    CrossRefPubMed
28. 28.↵
    1. Kemper EM,
    2. Leenders W,
    3. Küsters B,
    4. et al

    . Development of luciferase tagged brain tumour models in mice for chemotherapy intervention studies. Eur J Cancer 2006;2:3294–303. Epub 2006 Oct 5
29. 29.↵
    1. Davis SC,
    2. Pogue BW,
    3. Springett R,
    4. et al

    . Magnetic resonance-coupled fluorescence tomography scanner for molecular imaging of tissue. Rev Sci Instrum 2008;79:064302

    CrossRefPubMed
30. 30.↵
    1. Rehemtulla A,
    2. Stegman LD,
    3. Cardozo SJ,
    4. et al

    . Rapid and quantitative assessment of cancer treatment response using in vivo bioluminescence imaging. Neoplasia 2000;2:491–95

    CrossRefPubMedWeb of Science
31. 31.↵
    1. Szentirmai O,
    2. Baker CH,
    3. Lin N,
    4. et al

    . Noninvasive bioluminescence imaging of luciferase expressing intracranial U87 xenografts: correlation with magnetic resonance imaging determined tumor volume and longitudinal use in assessing tumor growth and antiangiogenic treatment effect. Neurosurgery 2006;58:365–72, discussion 365–72

    CrossRefPubMedWeb of Science
32. 32.↵
    1. Bryant MJ,
    2. Chuah TL,
    3. Luff J,
    4. et al

    . A novel rat model for glioblastoma multiforme using a bioluminescent F98 cell line. J Clin Neurosci 2008;15:545–51

    CrossRefPubMed
33. 33.↵
    1. Li X,
    2. Rooney WD,
    3. Várallyay CG,
    4. et al

    . Dynamic-contrast-enhanced-MRI with extravasating contrast reagent: rat cerebral glioma blood volume determination. J Magn Reson 2010;206:190–99. Epub 2010 Jul 31

    CrossRefPubMed
34. 34.↵
    1. Adzamli K,
    2. Yablonskiy DA,
    3. Chicoine MR,
    4. et al

    . Albumin-binding MR blood pool agents as MRI contrast agents in an intracranial mouse glioma model. Magn Reson Med 2003;49:586–90

    CrossRefPubMed
35. 35.↵
    1. Goldbrunner RH,
    2. Wagner S,
    3. Roosen K,
    4. et al

    . Models for assessment of angiogenesis in gliomas. J Neurooncol 2000;50:53–62

    CrossRefPubMed
36. 36.↵
    1. Sun Y,
    2. Schmidt NO,
    3. Schmidt K,
    4. et al

    . Perfusion MRI of U87 brain tumors in a mouse model. Magn Reson Med 2004;51:893–99

    CrossRefPubMedWeb of Science
37. 37.↵
    1. Veeravagu A,
    2. Hou LC,
    3. Hsu AR,
    4. et al

    . The temporal correlation of dynamic contrast-enhanced magnetic resonance imaging with tumor angiogenesis in a murine glioblastoma model. Neurol Res 2008;30:952–59. Epub 2008 Jul 25

    CrossRefPubMedWeb of Science
38. 38.↵
    1. Cha S,
    2. Johnson G,
    3. Wadghiri YZ,
    4. et al

    . Dynamic, contrast-enhanced perfusion MRI in mouse gliomas: correlation with histopathology. Magn Reson Med 2003;49:848–55

    CrossRefPubMedWeb of Science
39. 39.↵
    1. Gossmann A,
    2. Helbich TH,
    3. Kuriyama N,
    4. et al

    . Dynamic contrast-enhanced magnetic resonance imaging as a surrogate marker of tumor response to anti-angiogenic therapy in a xenograft model of glioblastoma multiforme. J Magn Reson Imaging 2002;15:233–40

    CrossRefPubMedWeb of Science
40. 40.↵
    1. Muir ER,
    2. Shen Q,
    3. Duong TQ

    . Cerebral blood flow MRI in mice using the cardiac-spin-labeling technique. Magn Reson Med 2008;60:744–48

    CrossRefPubMedWeb of Science
41. 41.↵
    1. Wong ET,
    2. Brem S

    . Antiangiogenesis treatment for glioblastoma multiforme: challenges and opportunities. J Natl Compr Canc Netw 2008;6:515–22

    Abstract/FREE Full Text
42. 42.↵
    1. Nagaraja TN,
    2. Ewing JR,
    3. Karki K,
    4. et al

    . MRI and quantitative autoradiographic studies following bolus injections of unlabeled and (14)C-labeled gadolinium-diethylenetriaminepentaacetic acid in a rat model of stroke yield similar distribution volumes and blood-to-brain influx rate constants. NMR Biomed 2011;24:547–58. Epub 2010 Dec 12

    CrossRefPubMedWeb of Science
43. 43.↵
    1. Sipkins DA,
    2. Cheresh DA,
    3. Kazemi MR

    . Detection of tumor angiogenesis in vivo by alphaVbeta3-targeted magnetic resonance imaging. Nat Med 1998;4:623–26

    CrossRefPubMedWeb of Science
44. 44.↵
    1. Moffat BA,
    2. Hall DE,
    3. Stojanovska J,
    4. et al

    . , Diffusion imaging for evaluation of tumor therapies in preclinical animal models. MAGMA 2004;17:249–59. Epub 2004 Dec 1

    CrossRefPubMed
45. 45.↵
    1. Chenevert TL,
    2. Stegman LD,
    3. Taylor JM,
    4. et al

    . Diffusion magnetic resonance imaging: an early surrogate marker of therapeutic efficacy in brain tumors. J Natl Cancer Inst 2000;92:2029–36

    Abstract/FREE Full Text
46. 46.↵
    1. Sun Y,
    2. Mulkern RV,
    3. Schmidt K,
    4. et al

    . Quantification of water diffusion and relaxation times of human U87 tumors in a mouse model. NMR Biomed 2004;17:399–404

    CrossRefPubMed
47. 47.↵
    1. Fan G,
    2. Zang P,
    3. Jing F,
    4. et al

    . Usefulness of diffusion/perfusion-weighted MRI in rat gliomas: correlation with histopathology. Acad Radiol 2005;12:640–51

    CrossRefPubMedWeb of Science
48. 48.↵
    1. Pacheco-Torres J,
    2. López-Larrubia P,
    3. Ballesteros P,
    4. et al

    . Imaging tumor hypoxia by magnetic resonance methods. NMR Biomed 2011;24:1–16. Epub 2010 Dec 9

    CrossRefPubMed
49. 49.↵
    1. Yetkin FZ,
    2. Mendelsohn D

    . Hypoxia imaging in brain tumors. Neuroimaging Clin N Am 2002;12:537–52

    CrossRefPubMedWeb of Science
50. 50.↵
    1. de Vries NA,
    2. Beijnen JH,
    3. van Tellingen O

    . High-grade glioma mouse models and their applicability for preclinical testing. Cancer Treat Rev 2009;35:714–23

    CrossRefPubMedWeb of Science
51. 51.↵
    1. Amarasingh S,
    2. Macleod MR,
    3. Whittle LR

    . What is the translational efficacy of chemotherapeutic drug research in neuro-oncology? A systematic review and meta-analysis of the efficacy of BCNU and CCNU in animal models of glioma. J Neurooncol 2009;91:117–25. Epub 2008 Sep 24

    CrossRefPubMed
52. 52.↵
    1. Moffat BA,
    2. Chen M,
    3. Kariaapper MS,
    4. et al

    . Inhibition of vascular endothelial growth factor (VEGF)-A causes a paradoxical increase in tumor blood flow and up-regulation of VEGF-D. Clin Cancer Res 2006;12:1525–32

    Abstract/FREE Full Text
53. 53.↵
    1. Mathieu V,
    2. De Nève N,
    3. Le Mercier M,
    4. et al

    . Combining bevacizumab with temozolomide increases the antitumor efficacy of temozolomide in a human glioblastoma orthotopic xenograft model. Neoplasia 2008;10:1383–92

    PubMedWeb of Science
54. 54.↵
    1. McConville P,
    2. Hambardzumyan D,
    3. Moody JB

    . Magnetic resonance imaging determination of tumor grade and early response to temozolomide in a genetically engineered mouse model of glioma. Clin Cancer Res 2007;13:2897–904

    Abstract/FREE Full Text
55. 55.↵
    1. Breton E,
    2. Goetz C,
    3. Kintz J,
    4. et al

    . In vivo preclinical low-field MRI monitoring of tumor growth following a suicide-gene therapy in an orthotopic mice model of human glioblastoma. C R Biol 2010;333:220–25. Epub 2010 Jan 25.

    CrossRefPubMed
56. 56.↵
    1. Huszthy PC,
    2. Immervoll H,
    3. Wang J

    . Cellular effects of oncolytic viral therapy on the glioblastoma microenvironment. Gene Ther 2010;17:202–16. Epub 2009 Oct 15

    CrossRefPubMed
57. 57.↵
    1. Heckl S,
    2. Pipkorn R,
    3. Nägele T,
    4. et al

    . Molecular imaging: bridging the gap between neuroradiology and neurohistology. Histol Histopathol 2004;19:651–68

    PubMedWeb of Science
58. 58.↵
    1. de Backer ME,
    2. Nabuurs RJ,
    3. van Buchem MA,
    4. et al

    . MR-based molecular imaging of the brain: the next frontier. AJNR Am J Neuroradiol 2010;31:1577–83. Epub 2010 Sep 23

    Abstract/FREE Full Text
59. 59.↵
    1. Jacobs AH,
    2. Dittmar C,
    3. Winkeler A,
    4. et al

    . Molecular imaging of gliomas. Mol Imaging 2002;1:309–35

    CrossRefPubMed
60. 60.↵
    1. Chirasani SR,
    2. Markovic DS,
    3. Synowitz M,
    4. et al

    . Transferrin-receptor-mediated iron accumulation controls proliferation and glutamate release in glioma cells. J Mol Med (Berl) 2009;87:153–67. Epub 2008 Dec 9

    CrossRefPubMedWeb of Science
61. 61.↵
    1. Saxena V,
    2. Gonzalez-Gomez I,
    3. Laug WE

    . A non-invasive, in vivo technique for monitoring vascular status of glioblastoma during angiogenesis. Technol Cancer Res Treat 2007;6:641–50

    Abstract/FREE Full Text
62. 62.↵
    1. Griffin JL,
    2. Kauppinen RA

    . Tumour metabolomics in animal models of human cancer. J Proteome Res 2007;6:498–505

    CrossRefPubMed