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Imaging Angiogenesis, Inflammation, and Metastasis in the Tumor Microenvironment with Magnetic Resonance Imaging

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Tumor Microenvironment and Cellular Stress

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 772))

Abstract

With the development of new imaging techniques, the potential for probing the molecular, cellular, and structural components of the tumor microenvironment in situ has increased dramatically. A multitude of imaging modalities have been successfully employed to probe different aspects of the tumor microenvironment, including expression of molecules, cell motion, cellularity, vessel permeability, vascular perfusion, metabolic and physiological changes, apoptosis, and inflammation. This chapter focuses on the most recent advances in magnetic resonance imaging methods, which offer a number of advantages over other methodologies, including high spatial resolution and the use of nonionizing radiation, as well as the use of such methods in the context of primary and secondary brain tumors. It also highlights how they can be used to assess the molecular and cellular changes in the tumor microenvironment in response to therapy.

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References

  • Ahrens ET, Flores R, Xu H, Morel PA (2005) In vivo imaging platform for tracking immunotherapeutic cells. Nat Biotechnol 23:983–987

    Google Scholar 

  • Alsop DC, Detre JA (1996) Reduced transit-time sensitivity in noninvasive magnetic resonance imaging of human cerebral blood flow. J Cereb Blood Flow Metab 16:1236–1249

    PubMed  CAS  Google Scholar 

  • Arbab AS, Bashaw LA, Miller BR, Jordan EK, Lewis BK, Kalish H, Frank JA (2003) Characterization of biophysical and metabolic properties of cells labeled with superparamagnetic iron oxide nanoparticles and transfection agent for cellular MR imaging. Radiology 229:838–846

    PubMed  Google Scholar 

  • Aronen HJ, Gazit IE, Louis DN, Buchbinder BR, Pardo FS, Weisskoff RM, Harsh GR, Cosgrove GR, Halpern EF, Hochberg FH et al (1994) Cerebral blood volume maps of gliomas: comparison with tumor grade and histologic findings. Radiology 191:41–51

    PubMed  CAS  Google Scholar 

  • Aronen HJ, Pardo FS, Kennedy DN, Belliveau JW, Packard SD, Hsu DW, Hochberg FH, Fischman AJ, Rosen BR (2000) High microvascular blood volume is associated with high glucose uptake and tumor angiogenesis in human gliomas. Clin Cancer Res 6:2189–2200

    PubMed  CAS  Google Scholar 

  • Bataveljic D, Stamenkovic S, Bacic G, Andjus PR (2011) Imaging cellular markers of neuroinflammation in the brain of the rat model of amyotrophic lateral sclerosis. Acta Physiol Hung 98:27–31

    PubMed  CAS  Google Scholar 

  • Bauerle T, Komljenovic D, Merz M, Berger MR, Goodman SL, Semmler W (2011) Cilengitide inhibits progression of experimental breast cancer bone metastases as imaged noninvasively using VCT, MRI and DCE-MRI in a longitudinal in vivo study. Int J Cancer 128:2453–2462

    Google Scholar 

  • Bauerle T, Komljenovic D, Semmler W (2012) Monitoring molecular, functional and morphologic aspects of bone metastases using non-invasive imaging. Curr Pharm Biotechnol 13:584–594

    PubMed  Google Scholar 

  • Bell LK, Ainsworth NL, Lee SH, Griffiths JR (2011) MRI & MRS assessment of the role of the tumour microenvironment in response to therapy. NMR Biomed 24:612–635

    PubMed  Google Scholar 

  • Bhorade R, Weissleder R, Nakakoshi T, Moore A, Tung CH (2000) Macrocyclic chelators with paramagnetic cations are internalized into mammalian cells via a HIV-tat derived membrane translocation peptide. Bioconjug Chem 11:301–305

    PubMed  CAS  Google Scholar 

  • Boulland JL, Leung DS, Thuen M, Vik-Mo E, Joel M, Perreault MC, Langmoen IA, Haraldseth O, Glover JC (2012) Evaluation of intracellular labeling with micron-sized particles of iron oxide (MPIOs) as a general tool for in vitro and in vivo tracking of human stem and progenitor cells. Cell Transplant 21:1743–1759

    PubMed  Google Scholar 

  • Brindle K (2008) New approaches for imaging tumour responses to treatment. Nat Rev Cancer 8:94–107

    PubMed  CAS  Google Scholar 

  • Brown JM, WILSON WR (2004) Exploiting tumour hypoxia in cancer treatment. Nat Rev Cancer 4:437–447

    PubMed  CAS  Google Scholar 

  • Budde MD, Gold E, Jordan EK, Frank JA (2012) Differential microstructure and physiology of brain and bone metastases in a rat breast cancer model by diffusion and dynamic contrast enhanced MRI. Clin Exp Metastasis 29:51–62

    PubMed  Google Scholar 

  • Buxton RB, Frank LR, Wong EC, Siewert B, Warach S, Edelman RR (1998) A general kinetic model for quantitative perfusion imaging with arterial spin labeling. Magn Reson Med 40:383–396

    PubMed  CAS  Google Scholar 

  • Carbonell WS, Ansorge O, Sibson N, Muschel R (2009) The vascular basement membrane as “soil” in brain metastasis. PLoS One 4:e5857

    PubMed  Google Scholar 

  • Carmeliet P (2005) Angiogenesis in life, disease and medicine. Nature 438:932–936

    PubMed  CAS  Google Scholar 

  • Carmeliet P, Jain RK (2000) Angiogenesis in cancer and other diseases. Nature 407:249–257

    PubMed  CAS  Google Scholar 

  • Cerdan S, Lotscher HR, Kunnecke B, Seelig J (1989) Monoclonal antibody-coated magnetite particles as contrast agents in magnetic resonance imaging of tumors. Magn Reson Med 12:151–163

    PubMed  CAS  Google Scholar 

  • Chaumeil MM, Gini B, Yang H, Iwanami A, Sukumar S, Ozawa T, Pieper RO, Mischel PS, James CD, Berger MS, Ronen SM (2012) Longitudinal evaluation of MPIO-labeled stem cell biodistribution in glioblastoma using high resolution and contrast-enhanced MR imaging at 14.1 tesla. Neuro Oncol 14:1050–1061

    PubMed  CAS  Google Scholar 

  • Colotta F, Allavena P, Sica A, Garlanda C, Mantovani A (2009) Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 30:1073–1081

    PubMed  CAS  Google Scholar 

  • Combes S, Jacob S, Combes N, Karam N, Chaumeil A, Guy-Moyat B, Treguer F, Deplagne A, Boveda S, Marijon E, Albenque JP (2013) Predicting favourable outcomes in the setting of radiofrequency catheter ablation of long-standing persistent atrial fibrillation: a pilot study assessing the value of left atrial appendage peak flow velocity. Arch Cardiovasc Dis 106:36–43

    PubMed  Google Scholar 

  • de Vries IJ, Lesterhuis WJ, Barentsz JO, Verdijk P, van Krieken JH, Boerman OC, Oyen WJ, Bonenkamp JJ, Boezeman JB, Adema GJ, Bulte JW, Scheenen TW, Punt CJ, Heerschap A, Figdor CG (2005) Magnetic resonance tracking of dendritic cells in melanoma patients for monitoring of cellular therapy. Nat Biotechnol 23:1407–1413

    PubMed  Google Scholar 

  • Deddens LH, van Tilborg GA, van Der Toorn A, van Der Marel K, Paulis LE, van Bloois L, Storm G, Strijkers GJ, Mulder WJ, de Vries HE, Dijkhuizen RM (2013) MRI of ICAM-1 upregulation after stroke: the importance of choosing the appropriate target-specific particulate contrast agent. Mol Imaging Biol 15(4):411–422

    PubMed  Google Scholar 

  • Denardo DG, Andreu P, Coussens LM (2010) Interactions between lymphocytes and myeloid cells regulate pro- versus anti-tumor immunity. Cancer Metastasis Rev 29:309–316

    PubMed  Google Scholar 

  • Detre JA, Leigh JS, Williams DS, Koretsky AP (1992) Perfusion imaging. Magn Reson Med 23:37–45

    PubMed  CAS  Google Scholar 

  • Domingo G, Perez CA, Velez M, Cudris J, Raez LE, Santos ES (2010) EGF receptor in lung cancer: a successful story of targeted therapy. Expert Rev Anticancer Ther 10:1577–1587

    PubMed  CAS  Google Scholar 

  • Dvorak HF, Galli SJ, Dvorak AM (1986) Cellular and vascular manifestations of cell-mediated immunity. Hum Pathol 17:122–137

    PubMed  CAS  Google Scholar 

  • Ferjancic S, Gil-Bernabe AM, Hill SA, Allen PD, Richardson P, Sparey T, Savory E, Mcguffog J, Muschel RJ (2013) VCAM-1 and VAP-1 recruit myeloid cells that promote pulmonary metastasis in mice. Blood 121(16):3289–3297

    PubMed  CAS  Google Scholar 

  • Ferrara N, Kerbel RS (2005) Angiogenesis as a therapeutic target. Nature 438:967–974

    PubMed  CAS  Google Scholar 

  • Fleige G, Nolte C, Synowitz M, Seeberger F, Kettenmann H, Zimmer C (2001) Magnetic labeling of activated microglia in experimental gliomas. Neoplasia 3:489–499

    PubMed  CAS  Google Scholar 

  • Fokas E, Mckenna WG, Muschel RJ (2012) The impact of tumor microenvironment on cancer treatment and its modulation by direct and indirect antivascular strategies. Cancer Metastasis Rev 31:823–842

    PubMed  CAS  Google Scholar 

  • Folkman J (1971) Tumor angiogenesis: therapeutic implications. N Engl J Med 285:1182–1186

    PubMed  CAS  Google Scholar 

  • Gao Z, Zhang L, Hu J, Sun Y (2013) Mesenchymal stem cells: a potential targeted-delivery vehicle for anti-cancer drug, loaded nanoparticles. Nanomedicine 9:174–184

    PubMed  CAS  Google Scholar 

  • Geelen T, Yeo SY, Paulis LE, Starmans LW, Nicolay K, Strijkers GJ (2012) Internalization of paramagnetic phosphatidylserine-containing liposomes by macrophages. J Nanobiotechnology 10:37

    PubMed  CAS  Google Scholar 

  • Goldschmidt P, Degorge S, Benallaoua D, Batellier L, Di Cave D, Chaumeil C (2012) Rapid detection and simultaneous molecular profile characterization of Acanthamoeba infections. Diagn Microbiol Infect Dis 74:137–141

    PubMed  CAS  Google Scholar 

  • Hahn PF, Weissleder R, Stark DD, Saini S, Elizondo G, Ferrucci JT (1988) MR imaging of focal splenic tumors. AJR Am J Roentgenol 150:823–827

    PubMed  CAS  Google Scholar 

  • Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674

    PubMed  CAS  Google Scholar 

  • Harisinghani MG, Weissleder R (2004) Sensitive, noninvasive detection of lymph node metastases. PLoS Med 1:e66

    PubMed  Google Scholar 

  • Harisinghani MG, Barentsz J, Hahn PF, Deserno WM, Tabatabaei S, van de Kaa CH, de la Rosette J, Weissleder R (2003) Noninvasive detection of clinically occult lymph-node metastases in prostate cancer. N Engl J Med 348:2491–2499

    PubMed  Google Scholar 

  • Heijmen L, Verstappen MC, Ter Voert EE, Punt CJ, Oyen WJ, de Geus-Oei LF, Hermans JJ, Heerschap A, van Laarhoven HW (2012) Tumour response prediction by diffusion-weighted MR imaging: ready for clinical use? Crit Rev Oncol Hematol 83:194–207

    PubMed  Google Scholar 

  • Heyn C, Ronald JA, Mackenzie LT, Macdonald IC, Chambers AF, Rutt BK, Foster PJ (2006a) In vivo magnetic resonance imaging of single cells in mouse brain with optical validation. Magn Reson Med 55:23–29

    PubMed  Google Scholar 

  • Heyn C, Ronald JA, Ramadan SS, Snir JA, Barry AM, Kmackenzie LT, Mikulis DJ, Palmieri D, Bronder JL, Steeg PS, Yoneda T, Macdonald IC, Chambers AF, Rutt BK, Foster PJ (2006b) In vivo MRI of cancer cell fate at the single-cell level in a mouse model of breast cancer metastasis to the brain. Magn Reson Med 56:1001–1010

    PubMed  Google Scholar 

  • Hoefnagels FW, Lagerwaard FJ, Sanchez E, Haasbeek CJ, Knol DL, Slotman BJ, Vandertop WP (2009) Radiological progression of cerebral metastases after radiosurgery: assessment of perfusion MRI for differentiating between necrosis and recurrence. J Neurol 256:878–887

    PubMed  Google Scholar 

  • Hoyte LC, Brooks KJ, Nagel S, Akhtar A, Chen R, Mardiguian S, Mcateer MA, Anthony DC, Choudhury RP, Buchan AM, Sibson NR (2010) Molecular magnetic resonance imaging of acute vascular cell adhesion molecule-1 expression in a mouse model of cerebral ischemia. J Cereb Blood Flow Metab 30:1178–1187

    PubMed  CAS  Google Scholar 

  • Ihnen M, Kilic E, Kohler N, Loning T, Witzel I, Hagel C, Holler S, Kersten JF, Muller V, Janicke F, Milde-Langosch K (2011) Protein expression analysis of ALCAM and CEACAM6 in breast cancer metastases reveals significantly increased ALCAM expression in metastases of the skin. J Clin Pathol 64:146–152

    PubMed  Google Scholar 

  • Jackson A, O’Connor J, Thompson G, Mills S (2008) Magnetic resonance perfusion imaging in neuro-oncology. Cancer Imaging 8:186–199

    PubMed  Google Scholar 

  • Joyal CC, Pennanen C, Tiihonen E, Laakso MP, Tiihonen J, Aronen HJ (2004) MRI volumetry of the vermis and the cerebellar hemispheres in men with schizophrenia. Psychiatry Res 131:115–124

    PubMed  Google Scholar 

  • Jung CW, Jacobs P (1995) Physical and chemical properties of superparamagnetic iron oxide MR contrast agents: ferumoxides, ferumoxtran, ferumoxsil. Magn Reson Imaging 13:661–674

    PubMed  CAS  Google Scholar 

  • Keunen O, Johansson M, Oudin A, Sanzey M, Rahim SA, Fack F, Thorsen F, Taxt T, Bartos M, JIRIK R, Miletic H, Wang J, Stieber D, Stuhr L, Moen I, Rygh CB, Bjerkvig R, Niclou SP (2011) Anti-VEGF treatment reduces blood supply and increases tumor cell invasion in glioblastoma. Proc Natl Acad Sci U S A 108:3749–3754

    PubMed  CAS  Google Scholar 

  • Kircher MF, Gambhir SS, Grimm J (2011) Noninvasive cell-tracking methods. Nat Rev Clin Oncol 8:677–688

    PubMed  CAS  Google Scholar 

  • Kleijn A, Chen JW, Buhrman JS, Wojtkiewicz GR, Iwamoto Y, Lamfers ML, Stemmer-Rachamimov AO, Rabkin SD, Weissleder R, Martuza RL, Fulci G (2011) Distinguishing inflammation from tumor and peritumoral edema by myeloperoxidase magnetic resonance imaging. Clin Cancer Res 17:4484–4493

    PubMed  CAS  Google Scholar 

  • Klemke M, Weschenfelder T, Konstandin MH, Samstag Y (2007) High affinity interaction of integrin alpha4beta1 (VLA-4) and vascular cell adhesion molecule 1 (VCAM-1) enhances migration of human melanoma cells across activated endothelial cell layers. J Cell Physiol 212:368–374

    PubMed  CAS  Google Scholar 

  • Laubli H, Borsig L (2010) Selectins promote tumor metastasis. Semin Cancer Biol 20:169–177

    PubMed  Google Scholar 

  • Law M, Cha S, Knopp EA, Johnson G, Arnett J, Litt AW (2002) High-grade gliomas and solitary metastases: differentiation by using perfusion and proton spectroscopic MR imaging. Radiology 222:715–721

    PubMed  Google Scholar 

  • Law M, Teicher N, Zagzag D, Knopp EA (2003a) Dynamic contrast enhanced perfusion MRI in mycosis fungoides. J Magn Reson Imaging 18:364–367

    PubMed  Google Scholar 

  • Law M, Yang S, Wang H, Babb JS, Johnson G, Cha S, Knopp EA, Zagzag D (2003b) Glioma grading: sensitivity, specificity, and predictive values of perfusion MR imaging and proton MR spectroscopic imaging compared with conventional MR imaging. AJNR Am J Neuroradiol 24:1989–1998

    PubMed  Google Scholar 

  • Leenders W, Kusters B, Pikkemaat J, Wesseling P, Ruiter D, Heerschap A, Barentsz J, de Waal RM (2003) Vascular endothelial growth factor-A determines detectability of experimental melanoma brain metastasis in GD-DTPA-enhanced MRI. Int J Cancer 105:437–443

    PubMed  CAS  Google Scholar 

  • Liu Y, Karonen JO, Vanninen RL, Nuutinen J, Koskela A, Soimakallio S, Aronen HJ (2004) Acute ischemic stroke: predictive value of 2D phase-contrast MR angiography–serial study with combined diffusion and perfusion MR imaging. Radiology 231:517–527

    PubMed  Google Scholar 

  • Mcateer MA, Sibson NR, von Zur Muhlen C, Schneider JE, Lowe AS, Warrick N, Channon KM, Anthony DC, Choudhury RP (2007) In vivo magnetic resonance imaging of acute brain inflammation using microparticles of iron oxide. Nat Med 13:1253–1258

    PubMed  CAS  Google Scholar 

  • Milanezi F, Carvalho S, Schmitt FC (2008) EGFR/HER2 in breast cancer: a biological approach for molecular diagnosis and therapy. Expert Rev Mol Diagn 8:417–434

    PubMed  CAS  Google Scholar 

  • Miller JC, Pien HH, Sahani D, Sorensen AG, Thrall JH (2005) Imaging angiogenesis: applications and potential for drug development. J Natl Cancer Inst 97:172–187

    PubMed  CAS  Google Scholar 

  • Moffat BA, Chenevert TL, Lawrence TS, Meyer CR, Johnson TD, Dong Q, Tsien C, Mukherji S, Quint DJ, Gebarski SS, Robertson PL, Junck LR, Rehemtulla A, Ross BD (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

    PubMed  CAS  Google Scholar 

  • Moore A, Weissleder R, Bogdanov A Jr (1997) Uptake of dextran-coated monocrystalline iron oxides in tumor cells and macrophages. J Magn Reson Imaging 7:1140–1145

    PubMed  CAS  Google Scholar 

  • Neuwelt EA, Varallyay P, Bago AG, Muldoon LL, Nesbit G, Nixon R (2004) Imaging of iron oxide nanoparticles by MR and light microscopy in patients with malignant brain tumours. Neuropathol Appl Neurobiol 30:456–471

    PubMed  CAS  Google Scholar 

  • Nguyen DX, Bos PD, Massague J (2009) Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer 9:274–284

    PubMed  CAS  Google Scholar 

  • O'connor JP, Jackson A, Parker GJ, Jayson GC (2007) DCE-MRI biomarkers in the clinical evaluation of antiangiogenic and vascular disrupting agents. Br J Cancer 96:189–195

    PubMed  Google Scholar 

  • Oude Engberink RD, Blezer EL, Dijkstra CD, van Der Pol SM, van Der Toorn A, de Vries HE (2010) Dynamics and fate of USPIO in the central nervous system in experimental autoimmune encephalomyelitis. NMR Biomed 23:1087–1096

    PubMed  Google Scholar 

  • Partlow KC, Chen J, Brant JA, Neubauer AM, Meyerrose TE, Creer MH, Nolta JA, Caruthers SD, Lanza GM, Wickline SA (2007) 19F magnetic resonance imaging for stem/progenitor cell tracking with multiple unique perfluorocarbon nanobeacons. FASEB J 21:1647–1654

    PubMed  CAS  Google Scholar 

  • Paulis LE, Jacobs I, van Den Akker NM, Geelen T, Molin DG, Starmans LW, Nicolay K, Strijkers GJ (2012) Targeting of ICAM-1 on vascular endothelium under static and shear stress conditions using a liposomal Gd-based MRI contrast agent. J Nanobiotechnology 10:25

    PubMed  CAS  Google Scholar 

  • Perini R, Choe R, Yodh AG, Sehgal C, Divgi CR, Rosen MA (2008) Non-invasive assessment of tumor neovasculature: techniques and clinical applications. Cancer Metastasis Rev 27:615–630

    PubMed  Google Scholar 

  • Perkio J, Soinne L, Ostergaard L, Helenius J, Kangasmaki A, Martinkauppi S, Salonen O, Savolainen S, Kaste M, Tatlisumak T, Aronen HJ (2005) Abnormal intravoxel cerebral blood flow heterogeneity in human ischemic stroke determined by dynamic susceptibility contrast magnetic resonance imaging. Stroke 36:44–49

    PubMed  Google Scholar 

  • Pirko I, Ciric B, Johnson AJ, Gamez J, Rodriguez M, Macura S (2003) Magnetic resonance imaging of immune cells in inflammation of central nervous system. Croat Med J 44:463–468

    PubMed  Google Scholar 

  • Plate KH, Breier G, Weich HA, Risau W (1992) Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature 359:845–848

    PubMed  CAS  Google Scholar 

  • Qian BZ, Pollard JW (2010) Macrophage diversity enhances tumor progression and metastasis. Cell 141:39–51

    PubMed  CAS  Google Scholar 

  • Rausch M, Baumann D, Neubacher U, Rudin M (2002) In-vivo visualization of phagocytotic cells in rat brains after transient ischemia by USPIO. NMR Biomed 15:278–283

    PubMed  CAS  Google Scholar 

  • Roberts HC, Roberts TP, Ley S, Dillon WP, Brasch RC (2002) Quantitative estimation of microvascular permeability in human brain tumors: correlation of dynamic Gd-DTPA-enhanced MR imaging with histopathologic grading. Acad Radiol 9(Suppl 1):S151–S155

    PubMed  Google Scholar 

  • Roland CL, Harken AH, Sarr MG, Barnett CC Jr (2007) ICAM-1 expression determines malignant potential of cancer. Surgery 141:705–707

    PubMed  Google Scholar 

  • Saif MW (2010) Colorectal cancer in review: the role of the EGFR pathway. Expert Opin Investig Drugs 19:357–369

    PubMed  CAS  Google Scholar 

  • Saudek F, Jirak D, Girman P, Herynek V, Dezortova M, Kriz J, Peregrin J, Berkova Z, Zacharovova K, Hajek M (2010) Magnetic resonance imaging of pancreatic islets transplanted into the liver in humans. Transplantation 90:1602–1606

    PubMed  Google Scholar 

  • Sauter G, Maeda T, Waldman FM, Davis RL, Feuerstein BG (1996) Patterns of epidermal growth factor receptor amplification in malignant gliomas. Am J Pathol 148:1047–1053

    PubMed  CAS  Google Scholar 

  • Schafer R, Bantleon R, Kehlbach R, Siegel G, Wiskirchen J, Wolburg H, Kluba T, Eibofner F, Northoff H, Claussen CD, Schlemmer HP (2010) Functional investigations on human mesenchymal stem cells exposed to magnetic fields and labeled with clinically approved iron nanoparticles. BMC Cell Biol 11:22

    PubMed  Google Scholar 

  • Schmieder AH, Winter PM, Caruthers SD, Harris TD, Williams TA, Allen JS, Lacy EK, Zhang H, Scott MJ, Hu G, Robertson JD, Wickline SA, Lanza GM (2005) Molecular MR imaging of melanoma angiogenesis with alphanubeta3-targeted paramagnetic nanoparticles. Magn Reson Med 53:621–627

    PubMed  CAS  Google Scholar 

  • Schwechheimer K, Huang S, Cavenee WK (1995) EGFR gene amplification–rearrangement in human glioblastomas. Int J Cancer 62:145–148

    PubMed  CAS  Google Scholar 

  • Serres S, Anthony DC, Jiang Y, Broom KA, Campbell SJ, Tyler DJ, van Kasteren SI, Davis BG, Sibson NR (2009) Systemic inflammatory response reactivates immune-mediated lesions in rat brain. J Neurosci 29:4820–4828

    PubMed  CAS  Google Scholar 

  • Serres S, Mardiguian S, Campbell SJ, Mcateer MA, Akhtar A, Krapitchev A, Choudhury RP, Anthony DC, Sibson NR (2011) VCAM-1-targeted magnetic resonance imaging reveals subclinical disease in a mouse model of multiple sclerosis. FASEB J 25:4415–4422

    PubMed  CAS  Google Scholar 

  • Serres S, Soto MS, Hamilton A, Mcateer MA, Carbonell WS, Robson MD, Ansorge O, Khrapitchev A, Bristow C, Balathasan L, Weissensteiner T, Anthony DC, Choudhury RP, Muschel RJ, Sibson NR (2012) Molecular MRI enables early and sensitive detection of brain metastases. Proc Natl Acad Sci U S A 109:6674–6679

    PubMed  CAS  Google Scholar 

  • Shapiro EM, Skrtic S, Sharer K, Hill JM, Dunbar CE, Koretsky AP (2004) MRI detection of single particles for cellular imaging. Proc Natl Acad Sci U S A 101:10901–10906

    PubMed  CAS  Google Scholar 

  • Shapiro EM, Skrtic S, Koretsky AP (2005) Sizing it up: cellular MRI using micron-sized iron oxide particles. Magn Reson Med 53:329–338

    PubMed  Google Scholar 

  • Shazeeb MS, Sotak CH, Deleo M 3rd, Bogdanov A Jr (2011) Targeted signal-amplifying enzymes enhance MRI of EGFR expression in an orthotopic model of human glioma. Cancer Res 71:2230–2239

    PubMed  CAS  Google Scholar 

  • Shen JF, Saunders JK (1993) Double inversion recovery improves water suppression in vivo. Magn Reson Med 29:540–542

    PubMed  CAS  Google Scholar 

  • Shen T, Weissleder R, Papisov M, Bogdanov A Jr, Brady TJ (1993) Monocrystalline iron oxide nanocompounds (MION): physicochemical properties. Magn Reson Med 29:599–604

    PubMed  CAS  Google Scholar 

  • Sipe JC, Filippi M, Martino G, Furlan R, Rocca MA, Rovaris M, Bergami A, Zyroff J, Scotti G, Comi G (1999) Method for intracellular magnetic labeling of human mononuclear cells using approved iron contrast agents. Magn Reson Imaging 17:1521–1523

    PubMed  CAS  Google Scholar 

  • Sitohy B, Nagy JA, Dvorak HF (2012) Anti-VEGF/VEGFR therapy for cancer: reassessing the target. Cancer Res 72:1909–1914

    PubMed  CAS  Google Scholar 

  • Song HT, Jordan EK, Lewis BK, Gold E, Liu W, Frank JA (2011) Quantitative T2* imaging of metastatic human breast cancer to brain in the nude rat at 3 T. NMR Biomed 24:325–334

    PubMed  Google Scholar 

  • Sundstrom T, Daphu I, Wendelbo I, Hodneland E, Lundervold A, Immervoll H, Skaftnesmo KO, Babic M, Jendelova P, Sykova E, Lund-Johansen M, Bjerkvig R, Thorsen F (2013) Automated tracking of nanoparticle-labeled melanoma cells improves the predictive power of a brain metastasis model. Cancer Res 73(8):2445–2456

    PubMed  CAS  Google Scholar 

  • Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L, Verweij J, van Glabbeke M, van Oosterom AT, Christian MC, Gwyther SG (2000) New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst 92:205–216

    PubMed  CAS  Google Scholar 

  • Unger EC (2003) How can superparamagnetic iron oxides be used to monitor disease and treatment? Radiology 229:615–616

    PubMed  Google Scholar 

  • Valable S, Barbier EL, Bernaudin M, Roussel S, Segebarth C, Petit E, Remy C (2007) In vivo MRI tracking of exogenous monocytes/macrophages targeting brain tumors in a rat model of glioma. Neuroimage 37(Suppl 1):S47–S58

    PubMed  Google Scholar 

  • van Kasteren SI, Campbell SJ, Serres S, Anthony DC, Sibson NR, Davis BG (2009) Glyconanoparticles allow pre-symptomatic in vivo imaging of brain disease. Proc Natl Acad Sci U S A 106:18–23

    PubMed  Google Scholar 

  • von Zur Muhlen C, Sibson NR, Peter K, Campbell SJ, Wilainam P, Grau GE, Bode C, Choudhury RP, Anthony DC (2008) A contrast agent recognizing activated platelets reveals murine cerebral malaria pathology undetectable by conventional MRI. J Clin Invest 118:1198–1207

    Google Scholar 

  • Wang J, Alsop DC, Li L, Listerud J, Gonzalez-AT JB, Schnall MD, Detre JA (2002) Comparison of quantitative perfusion imaging using arterial spin labeling at 1.5 and 4.0 Tesla. Magn Reson Med 48:242–254

    PubMed  Google Scholar 

  • Wang J, Rao H, Wetmore GS, Furlan PM, Korczykowski M, Dinges DF, Detre JA (2005) Perfusion functional MRI reveals cerebral blood flow pattern under psychological stress. Proc Natl Acad Sci U S A 102:17804–17809

    PubMed  CAS  Google Scholar 

  • Warmuth C, Gunther M, Zimmer C (2003) Quantification of blood flow in brain tumors: comparison of arterial spin labeling and dynamic susceptibility-weighted contrast-enhanced MR imaging. Radiology 228:523–532

    PubMed  Google Scholar 

  • Weissleder R, Pittet MJ (2008) Imaging in the era of molecular oncology. Nature 452:580–589

    PubMed  CAS  Google Scholar 

  • Weissleder R, Hahn PF, Stark DD, Rummeny E, Saini S, Wittenberg J, Ferrucci JT (1987a) MR imaging of splenic metastases: ferrite-enhanced detection in rats. AJR Am J Roentgenol 149:723–726

    PubMed  CAS  Google Scholar 

  • Weissleder R, Stark DD, Compton CC, Wittenberg J, Ferrucci JT (1987b) Ferrite-enhanced MR imaging of hepatic lymphoma: an experimental study in rats. AJR Am J Roentgenol 149:1161–1165

    PubMed  CAS  Google Scholar 

  • Weissleder R, Hahn PF, Stark DD, Elizondo G, Saini S, Todd LE, Wittenberg J, Ferrucci JT (1988a) Superparamagnetic iron oxide: enhanced detection of focal splenic tumors with MR imaging. Radiology 169:399–403

    PubMed  CAS  Google Scholar 

  • Weissleder R, Stark DD, Elizondo G, Hahn PF, Compton C, Saini S, Wittenberg J, Ferrucci JT (1988b) MRI of hepatic lymphoma. Magn Reson Imaging 6:675–681

    PubMed  CAS  Google Scholar 

  • Weissleder R, Elizondo G, Wittenberg J, Lee AS, Josephson L, Brady TJ (1990) Ultrasmall superparamagnetic iron oxide: an intravenous contrast agent for assessing lymph nodes with MR imaging. Radiology 175:494–498

    PubMed  CAS  Google Scholar 

  • Weissleder R, Bogdanov A, Papisov M (1992) Drug targeting in magnetic resonance imaging. Magn Reson Q 8:55–63

    PubMed  CAS  Google Scholar 

  • Weissleder R, Cheng HC, Bogdanova A, Bogdanov A Jr (1997) Magnetically labeled cells can be detected by MR imaging. J Magn Reson Imaging 7:258–263

    PubMed  CAS  Google Scholar 

  • Wiiger MT, Gehrken HB, Fodstad O, Maelandsmo GM, Andersson Y (2010) A novel human recombinant single-chain antibody targeting CD166/ALCAM inhibits cancer cell invasion in vitro and in vivo tumour growth. Cancer Immunol Immunother 59:1665–1674

    PubMed  CAS  Google Scholar 

  • Williams DS, Detre JA, Leigh JS, Koretsky AP (1992) Magnetic resonance imaging of perfusion using spin inversion of arterial water. Proc Natl Acad Sci U S A 89:212–216

    PubMed  CAS  Google Scholar 

  • Wolf RL, Wang J, Wang S, Melhem ER, O’Rourke DM, Judy KD, Detre JA (2005) Grading of CNS neoplasms using continuous arterial spin labeled perfusion MR imaging at 3 Tesla. J Magn Reson Imaging 22:475–482

    PubMed  Google Scholar 

  • Wong EC, Buxton RB, Frank LR (1998) A theoretical and experimental comparison of continuous and pulsed arterial spin labeling techniques for quantitative perfusion imaging. Magn Reson Med 40:348–355

    PubMed  CAS  Google Scholar 

  • Wong EC, Cronin M, Wu WC, Inglis B, Frank LR, Liu TT (2006) Velocity-selective arterial spin labeling. Magn Reson Med 55:1334–1341

    PubMed  Google Scholar 

  • Yankeelov TE, Lepage M, Chakravarthy A, Broome EE, Niermann KJ, Kelley MC, Meszoely I, Mayer IA, Herman CR, Mcmanus K, Price RR, Gore JC (2007) Integration of quantitative DCE-MRI and ADC mapping to monitor treatment response in human breast cancer: initial results. Magn Reson Imaging 25:1–13

    PubMed  Google Scholar 

  • Zhang C, Jugold M, Woenne EC, Lammers T, Morgenstern B, Mueller MM, Zentgraf H, Bock M, Eisenhut M, Semmler W, Kiessling F (2007) Specific targeting of tumor angiogenesis by RGD-conjugated ultrasmall superparamagnetic iron oxide particles using a clinical 1.5-T magnetic resonance scanner. Cancer Res 67:1555–1562

    PubMed  CAS  Google Scholar 

  • Zhang F, Huang X, Zhu L, Guo N, Niu G, Swierczewska M, Lee S, Xu H, Wang AY, Mohamedali KA, Rosenblum MG, Lu G, Chen X (2012) Noninvasive monitoring of orthotopic glioblastoma therapy response using RGD-conjugated iron oxide nanoparticles. Biomaterials 33:5414–5422

    Google Scholar 

  • Zimmer C, Weissleder R, O’Connor D, Lapointe L, Brady TJ, Enochs WS (1995a) Cerebral iron oxide distribution: in vivo mapping with MR imaging. Radiology 196:521–527

    PubMed  CAS  Google Scholar 

  • Zimmer C, Weissleder R, Poss K, Bogdanova A, Wright SC Jr, Enochs WS (1995b) MR imaging of phagocytosis in experimental gliomas. Radiology 197:533–538

    PubMed  CAS  Google Scholar 

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Acknowledgements

The authors thank Dr Clare Howarth for her careful read of the manuscript.

Funding statement This work was funded by Cancer Research UK (Research Grant C5255/A12678).

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Authors and Affiliations

  1. CR-UK/MRC Gray Institute for Radiation Oncology and Biology, Department of Oncology, University of Oxford, Churchill Hospital, Oxford, OX3 7LJ, UK

    Sébastien Serres, Emma R. O’Brien & Nicola R. Sibson

  2. Experimental Neuroimaging Group, Radiobiology Research Institute, Churchill Hospital, Oxford, OX3 7LJ, UK

    Sébastien Serres

Authors
  1. Sébastien Serres
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  2. Emma R. O’Brien
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  3. Nicola R. Sibson
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Corresponding author

Correspondence to Sébastien Serres .

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Editors and Affiliations

  1. Department of Radiation Oncology, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, USA

    Constantinos Koumenis

  2. Cancer Research, Gray Institute for Radiation Oncology, Oxford, United Kingdom

    Ester Hammond

  3. Department of Radiation Oncology, Stanford University School of Medicine, Stanford, California, USA

    Amato Giaccia

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Serres, S., O’Brien, E.R., Sibson, N.R. (2014). Imaging Angiogenesis, Inflammation, and Metastasis in the Tumor Microenvironment with Magnetic Resonance Imaging. In: Koumenis, C., Hammond, E., Giaccia, A. (eds) Tumor Microenvironment and Cellular Stress. Advances in Experimental Medicine and Biology, vol 772. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-5915-6_12

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