MR Molecular Imaging of Tumor Vasculature and Vascular Targets

Advances in Genetics

Volumn 69, Issue C, 2010, Pages 1-30

  Pathak, Arvind P ^a,b   Penet, Marie France ^a   Bhujwalla, Zaver M ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONTRAST MEDIUM;

BLOOD VESSEL; CHEMISTRY; HUMAN; METHODOLOGY; MOLECULAR IMAGING; MOLECULAR WEIGHT; NEOVASCULARIZATION (PATHOLOGY); NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; REVIEW;

BLOOD VESSELS; CONTRAST MEDIA; HUMANS; MAGNETIC RESONANCE IMAGING; MOLECULAR IMAGING; MOLECULAR WEIGHT; NEOVASCULARIZATION, PATHOLOGIC;

EID: 77956149129     PISSN: 00652660     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0065-2660(10)69010-4     Document Type: Book

References (132)

1. Abramovitch R., Dafni H., Smouha E., Benjamin L., Neeman M. In vivo prediction of vascular susceptibility to vascular endothelial growth factor withdrawal: Magnetic resonance imaging of C6 rat glioma in nude mice. Cancer Res. 1999, 59:5012-5016.
2. 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. USA 2003, 100(18):10158-10163.
3. Aronen H.J., Cohen M.S., Belliveau J.W., Fordham J.A., Rosen B.R. Ultrafast imaging of brain tumors. Top. Magn. Reson. Imaging 1993, 5(1):14-24.
4. Aronen H.J., Gazit I.E., Louis D.N., Buchbinder B.R., Pardo F.S., Weisskoff R.M., Harsh G.R., Cosgrove G.R., Halpern E.F., Hochberg F.H., Rosen B.R. Cerebral blood volume maps of gliomas: Comparison with tumor grade and histological findings. Radiology 1994, 191:41-51.
5. Artemov D., Bhujwalla Z.M., Bulte J.W. Magnetic resonance imaging of cell surface receptors using targeted contrast agents. Curr. Pharm. Biotechnol. 2004, 5(6):485-494.
6. Axel L. Cerebral blood flow determination by rapid-sequence computed tomography: Theoretical analysis. Radiology 1980, 137(3):679-686.
7. Baar J., Silverman P., Lyons J., Fu P., Abdul-Karim F., Ziats N., Wasman J., Hartman P., Jesberger J., Dumadag L., Hohler E., Leeming R., et al. A vasculature-targeting regimen of preoperative docetaxel with or without bevacizumab for locally advanced breast cancer: impact on angiogenic biomarkers. Clin. Cancer Res. 2009, 15(10):3583-3590.
8. Baluk P., Hashizume H., McDonald D.M. Cellular abnormalities of blood vessels as targets in cancer. Curr. Opin. Genet. Dev. 2005, 15(1):102-111.
9. Batchelor T.T., Sorensen A.G., di Tomaso E., Zhang W.T., Duda D.G., Cohen K.S., Kozak K.R., Cahill D.P., Chen P.J., Zhu M., Ancukiewicz M., Mrugala M.M., et al. AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 2007, 11(1):83-95.
10. 18F]galacto-RGD positron emission tomography for imaging of alphavbeta3 expression on the neovasculature in patients with squamous cell carcinoma of the head and neck. Clin. Cancer Res. 2007, 13(22 Pt 1):6610-6616.
11. Bertout J.A., Patel S.A., Simon M.C. The impact of O2 availability on human cancer. Nat. Rev. Cancer 2008, 8(12):967-975.
12. Bhujwalla Z.M., Artemov D., Ballesteros P., Cerdan S., Gillies R.J., Solaiyappan M. Combined vascular and extracellular pH imaging of solid tumors. NMR Biomed 2002, 15(2):114-119.
13. Bhujwalla Z.M., Artemov D., Natarajan K., Ackerstaff E., Solaiyappan M. Vascular differences detected by MRI for metastatic versus nonmetastatic breast and prostate cancer xenografts. Neoplasia 2001, 3(2):143-153.
14. Boxerman J.L., Hamberg L.M., Rosen B.R., Weisskoff R.M. MR contrast due to intravascular magnetic susceptibility perturbations. Magn. Reson. Med. 1995, 34:555-566.
15. Brasch R., Pham C., Shames D., et al. Assessing tumor angiogenesis using macromolecular MR imaging contrast media. J. Magn. Reson. Imaging 1997, 7:68-74.
16. Brooks P.C., Montgomery A.M., Rosenfeld M., Reisfeld R.A., Hu T., Klier G., Cheresh D.A. Integrin alpha v beta 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell 1994, 79(7):1157-1164.
17. Brown L.F., Berse B., Jackman R.W., Tognazzi K., Manseau E.J., Dvorak H.F., Senger D.R. Increased expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in kidney and bladder carcinomas. Am. J. Pathol. 1993, 143(5):1255-1262.
18. Burrows F.J., Derbyshire E.J., Tazzari P.L., Amlot P., Gazdar A.F., King S.W., Letarte M., Vitetta E.S., Thorpe P.E. Up-regulation of endoglin on vascular endothelial cells in human solid tumors: Implications for diagnosis and therapy. Clin. Cancer Res. 1995, 1(12):1623-1634.
19. Carmeliet P. Angiogenesis in life, disease and medicine. Nature 2005, 438(7070):932-936.
20. Carmeliet P., Dor Y., Herbert J.-M., Fukumura D., Brusselmans K., Dewerchin M., Neeman M., Bono F., Abramovitch R., Maxwell P., Koch C.J., Ratcliffe P., et al. Role of HIF-1 in hypoxia-mediated apoptosis, cell proliferation and tumor angiogenesis. Nature 1998, 394:485-490.
21. Chang Y.S., di Tomaso E., McDonald D.M., Jones R., Jain R.K., Munn L.L. Mosaic blood vessels in tumors: Frequency of cancer cells in contact with flowing blood. Proc. Natl. Acad. Sci. USA 2000, 97(26):14608-14613.
22. Clark E.R., Hitschler W.J., KirbySmith H.T., Rex R.O., Smith J.H. General observations on the ingrowth of new blood vessels into standardized chambers in the rabbit's ear, and the subsequent changes in the newly grown vessels over a period of months. Anat. Rec. 1931, 50:129-167.
23. Corada M., Zanetta L., Orsenigo F., Breviario F., Lampugnani M.G., Bernasconi S., Liao F., Hicklin D.J., Bohlen P., Dejana E. A monoclonal antibody to vascular endothelial-cadherin inhibits tumor angiogenesis without side effects on endothelial permeability. Blood 2002, 100(3):905-911.
24. Day S.E., Kettunen M.I., Gallagher F.A., Hu D.E., Lerche M., Wolber J., Golman K., Ardenkjaer-Larsen J.H., Brindle K.M. Detecting tumor response to treatment using hyperpolarized 13C magnetic resonance imaging and spectroscopy. Nat. Med. 2007, 13(11):1382-1387.
25. Deane B.R., Lantos P.L. The vasculature of experimental brain tumors-Part 1: A sequential light and electron microscope study of angiogenesis. J. Neurol. Sci. 1981, 49:55-66.
26. Dennie J., Mandeville J.B., Boxerman J.L., Packard S.D., Rosen B.R., Weisskoff R.M. NMR imaging of changes in vascular morphology due to tumor angiogenesis. Magn. Reson. Med. 1998, 40:793-799.
27. Donahue K.M., Burstein D., MAnning W.J., Gray M.L. Studies of Gd-DTPA relaxivity and proton exchange rates in tissue. Magn. Reson. Med. 1994, 32:66-75.
28. Donahue K.M., Krouwer H.G., Rand S.D., Pathak A.P., Marszalkowski C.S., Censky S.C., Prost R.W. Utility of simultaneously acquired gradient-echo and spin-echo cerebral blood volume and morphology maps in brain tumor patients. Magn. Reson. Med. 2000, 43(6):845-853.
29. Donahue K.M., Weisskoff R.M., Burstein D. Water diffusion and exchange as they influence contrast enhancement. J. Magn. Reson. Imaging 1997, 7(1):102-110.
30. 1 contrast agents: Accuracy, precision, and water exchange. Magn. Reson. Med. 1996, 36:858-867.
31. Driessen W.H., Ozawa M.G., Arap W., Pasqualini R. Ligand-directed cancer gene therapy to angiogenic vasculature. Adv. Genet. 2009, 67:103-121.
32. Epstein A.L., Khawli L.A., Hornick J.L., Taylor C.R. Identification of a monoclonal antibody, TV-1, directed against the basement membrane of tumor vessels, and its use to enhance the delivery of macromolecules to tumors after conjugation with interleukin 2. Cancer Res. 1995, 55(12):2673-2680.
33. Fisel C.R., Ackerman J.L., Buxton R.B., Garrido L., Belliveau J.W., Rosen R.B., Brady T.J. MR contrast due to microscopically heterogeneous magnetic susceptibility: Numerical simulations and applications to cerebral physiology. Magn. Reson. Med. 1991, 17:336-347.
34. Folkman J. Tumor angiogenesis: therapeutic implications. N. Engl. J. Med. 1971, 285(21):1182-1186.
35. Folkman J. Angiogenesis: An organizing principle for drug discovery?. Nat. Rev. Drug Discov. 2007, 6(4):273-286.
36. Forster-Horvath C., Meszaros L., Raso E., Dome B., Ladanyi A., Morini M., Albini A., Timar J. Expression of CD44v3 protein in human endothelial cells in vitro and in tumoral microvessels in vivo. Microvasc. Res. 2004, 68(2):110-118.
37. Glunde K., Pathak A.P., Bhujwalla Z.M. Molecular-functional imaging of cancer: to image and imagine. Trends Mol. Med. 2007, 13(7):287-297.
38. Goldman E. The growth of malignant disease in man and the lower animals, with special reference to the vascular system. Proc. R. Soc. Med. 1907, 1:1-13.
39. Hagemeier H.H., Vollmer E., Goerdt S., Schulze-Osthoff K., Sorg C. A monoclonal antibody reacting with endothelial cells of budding vessels in tumors and inflammatory tissues, and non-reactive with normal adult tissues. Int. J. Cancer 1986, 38(4):481-488.
40. Hallahan D.E., Staba-Hogan M.J., Virudachalam S., Kolchinsky A. X-ray-induced P-selectin localization to the lumen of tumor blood vessels. Cancer Res. 1998, 58(22):5216-5220.
41. Holash J., Maisonpierre P.C., Compton D., Boland P., Alexander C.R., Zagzag D., Yancopoulos G.D., Wiegand S.J. Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF. Science 1999, 284(5422):1994-1998.
42. Hunter J. Treatise on the blood, inflammation and gunshot wounds. 1794, Thomas Bradford, Phildelphia.
43. Jain R.K. Determinants of tumor blood flow: A review. Cancer Res. 1988, 48(10):2641-2658.
44. Jain R.K., Carmeliet P.F. Vessels of death or life. Sci. Am. 2001, 285(6):38-45.
45. Jain R.K., Duda D.G., Willett C.G., Sahani D.V., Zhu A.X., Loeffler J.S., Batchelor T.T., Sorensen A.G. Biomarkers of response and resistance to antiangiogenic therapy. Nat. Rev. Clin. Oncol. 2009, 6(6):327-338.
46. Jarnum H., Steffensen E.G., Knutsson L., Frund E.T., Simonsen C.W., Lundbye-Christensen S., Shankaranarayanan A., Alsop D.C., Jensen F.T., Larsson E.M. Perfusion MRI of brain tumours: a comparative study of pseudo-continuous arterial spin labelling and dynamic susceptibility contrast imaging. Neuroradiology 2010, 52(4):307-317.
47. JuanYin J., Tracy K., Zhang L., Munasinghe J., Shapiro E., Koretsky A., Kelly K. Noninvasive imaging of the functional effects of anti-VEGF therapy on tumor cell extravasation and regional blood volume in an experimental brain metastasis model. Clin. Exp. Metastasis 2009, 26(5):403-414.
48. Kalluri R. Basement membranes: Structure, assembly and role in tumour angiogenesis. Nat. Rev. Cancer 2003, 3(6):422-433.
49. Karumanchi S.A., Jha V., Ramchandran R., Karihaloo A., Tsiokas L., Chan B., Dhanabal M., Hanai J.I., Venkataraman G., Shriver Z., Keiser N., Kalluri R., et al. Cell surface glypicans are low-affinity endostatin receptors. Mol. Cell 2001, 7(4):811-822.
50. Kennan R.P. Intravascular susceptibility contrast mechanisms in tissues. Magn. Reson. Med. 1994, 31:9-21.
51. Khemtong C., Kessinger C.W., Ren J., Bey E.A., Yang S.G., Guthi J.S., Boothman D.A., Sherry A.D., Gao J. In vivo off-resonance saturation magnetic resonance imaging of alphavbeta3-targeted superparamagnetic nanoparticles. Cancer Res. 2009, 69(4):1651-1658.
52. 1-GRE blood volume measurements: Implications for the evaluation of tumor angiogenesis. Magn. Reson. Med. 2002, 47(6):1110-1120.
53. Knutsson L., van Westen D., Petersen E.T., Bloch K.M., Holtas S., Stahlberg F., Wirestam R. Absolute quantification of cerebral blood flow: correlation between dynamic susceptibility contrast MRI and model-free arterial spin labeling. Magn. Reson. Imaging 2010, 28(1):1-7.
54. Koivunen E., Arap W., Valtanen H., Rainisalo A., Medina O.P., Heikkila P., Kantor C., Gahmberg C.G., Salo T., Konttinen Y.T., Sorsa T., Ruoslahti E., et al. Tumor targeting with a selective gelatinase inhibitor. Nat. Biotechnol. 1999, 17(8):768-774.
55. Kolonin M., Pasqualini R., Arap W. Molecular addresses in blood vessels as targets for therapy. Curr. Opin. Chem. Biol. 2001, 5(3):308-313.
56. Konerding M.A., van Ackern C., Fait E., Steinberg F., Streffer C. Morphological aspects of tumor angiogenesis and microcirculation. Blood Perfusion and Microenvironment of Human Tumors: Implications for Clinical Radiooncology 2000, Springer Verlag, New York, pp. 5-17.
57. Landis C.S., Li X., Telang F.W., Coderre J.A., Micca P.L., Rooney W.D., Latour L.L., Vetek G., Palyka I., Springer C.S. Determination of the MRI contrast agent concentration time course in vivo following bolus injection: Effect of equilibrium transcytolemmal water exchange. Magn. Reson. Med. 2000, 44(4):563-574.
58. Langenkamp E., Molema G. Microvascular endothelial cell heterogeneity: General concepts and pharmacological consequences for anti-angiogenic therapy of cancer. Cell Tissue Res. 2009, 335(1):205-222.
59. Lauffer R.B. Paramagnetic metal complexes as water proton relaxation agents for NMR imaging: Theory and design. Chem. Rev. 1987, 87:901-927.
60. Lewis V.O., Ozawa M.G., Deavers M.T., Wang G., Shintani T., Arap W., Pasqualini R. The interleukin-11 receptor alpha as a candidate ligand-directed target in osteosarcoma: Consistent data from cell lines, orthotopic models, and human tumor samples. Cancer Res. 2009, 69(5):1995-1999.
61. Lewis W. The vascular patterns of tumors. Bull. Johns Hopkins Hosp. 1927, 41:156-162.
62. Li K.L., Wilmes L.J., Henry R.G., Pallavicini M.G., Park J.W., Hu-Lowe D.D., McShane T.M., Shalinsky D.R., Fu Y.J., Brasch R.C., Hylton N.M. Heterogeneity in the angiogenic response of a BT474 human breast cancer to a novel vascular endothelial growth factor-receptor tyrosine kinase inhibitor: Assessment by voxel analysis of dynamic contrast-enhanced MRI. J. Magn. Reson. Imaging 2005, 22(4):511-519.
63. Lijowski M., Caruthers S., Hu G., Zhang H., Scott M.J., Williams T., Erpelding T., Schmieder A.H., Kiefer G., Gulyas G., Athey P.S., Gaffney P.J., et al. High sensitivity: High-resolution SPECT-CT/MR molecular imaging of angiogenesis in the Vx2 model. Invest. Radiol. 2009, 44(1):15-22.
64. Loveless M.E., Whisenant J.G., Wilson K., Lyshchik A., Sinha T.K., Gore J.C., Yankeelov T.E. Coregistration of ultrasonography and magnetic resonance imaging with a preliminary investigation of the spatial colocalization of vascular endothelial growth factor receptor 2 expression and tumor perfusion in a murine tumor model. Mol. Imaging 2009, 8(4):187-198.
65. Maeda M., Itoh S., Kimura H., Iwasaki T., Hayashi N., Yamamoto K., Ishii Y., Kubota T. Tumor vascularity in the brain: Evaluation with dynamic susceptibility-contrast MR imaging. Radiology 1993, 189:233-238.
66. Maniotis A.J., Folberg R., Hess A., Seftor E.A., Gardner L.M., Pe'er J., Trent J.M., Meltzer P.S., Hendrix M.J. Vascular channel formation by human melanoma cells in vivo and in vitro: Vasculogenic mimicry. Am. J. Pathol. 1999, 155(3):739-752.
67. Mayr N.A., Yuh W.T., Jajoura D., Wang J.Z., Lo S.S., Montebello J.F., Porter K., Zhang D., McMeekin D.S., Buatti J.M. Ultra-early predictive assay for treatment failure using functional magnetic resonance imaging and clinical prognostic parameters in cervical cancer. Cancer 2010, 116(4):903-912.
68. McDonald D.M., Choyke P.L. Imaging of angiogenesis: From microscope to clinic. Nat. Med. 2003, 9(6):713-725.
69. Mikhaylova M., Stasinopoulos I., Kato Y., Artemov D., Bhujwalla Z.M. Imaging of cationic multifunctional liposome-mediated delivery of COX-2 siRNA. Cancer Gene Ther. 2009, 16(3):217-226.
70. Minowa T., Kawano K., Kuribayashi H., Shiraishi K., Sugino T., Hattori Y., Yokoyama M., Maitani Y. Increase in tumour permeability following TGF-β type I receptor-inhibitor treatment observed by dynamic contrast-enhanced MRI. Br. J. Cancer 2009, 101(11):1884-1890.
71. Molema G. Design of vascular endothelium-specific drug-targeting strategies for the treatment of cancer. Acta Biochim. Pol. 2005, 52(2):301-310.
72. Molls M., Vaupel P. The impact of the tumor microenvironment on experimental and clinical radiation oncology and other therapeutic modalities. Blood Perfusion and Microenvironment of Human Tumors: Implications for Clinical Radiooncology 2000, 1-4. Springer Verlag, New York. L.W. Brady, H.-P. Heilman, M. Molls (Eds.).
73. Monzani E., La Porta C.A. Targeting cancer stem cells to modulate alternative vascularization mechanisms. Stem Cell Rev. 2008, 4(1):51-56.
74. Moser T.L., Stack M.S., Asplin I., Enghild J.J., Hojrup P., Everitt L., Hubchak S., Schnaper H.W., Pizzo S.V. Angiostatin binds ATP synthase on the surface of human endothelial cells. Proc. Natl. Acad. Sci. USA 1999, 96(6):2811-2816.
75. Munn L.L. Aberrant vascular architecture in tumors and its importance in drug-based therapies. Drug Discov. Today 2003, 8(9):396-403.
76. Neri D., Bicknell R. Tumour vascular targeting. Nat. Rev. Cancer 2005, 5(6):436-446.
77. Neuwelt E.A., Hamilton B.E., Varallyay C.G., Rooney W.R., Edelman R.D., Jacobs P.M., Watnick S.G. Ultrasmall superparamagnetic iron oxides (USPIOs): A future alternative magnetic resonance (MR) contrast agent for patients at risk for nephrogenic systemic fibrosis (NSF)?. Kidney Int. 2009, 75(5):465-474.
78. Nguyen M., Strubel N.A., Bischoff J. A role for sialyl Lewis-X/A glycoconjugates in capillary morphogenesis. Nature 1993, 365(6443):267-269.
79. Ogan M.D., Schmiedl U., Mosley M.E., Grodd W., Paajanen H., Brasch R.C. Albumin labeled with Gd-DTPA; an intravascular contrast enhancing agent for magnetic resonance blood pool imaging: Preparation and characterization. Invest. Radiol. 1987, 22:665-671.
80. Ogawa S. Oxygenation-sensitive contrast in MR image of rodent brain at high magnetic fields. Magn. Reson. Med. 1990, 14:68-78.
81. Oh P., Li Y., Yu J., Durr E., Krasinska K.M., Carver L.A., Testa J.E., Schnitzer J.E. Subtractive proteomic mapping of the endothelial surface in lung and solid tumours for tissue-specific therapy. Nature 2004, 429(6992):629-635.
82. Ohno K.P., Pettigrew K.D., Rapoport S.I. Local cerebral blood flow in the conscious rat as measured with 14C-antipyrine, 14C-iodoantipyrine and 3H-nicotine. Stroke 1979, 10(1):62-67.
83. Ostergaard L., Weisskoff R.M., Chesler D.A., Gyldensted C., Rosen B.R. High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part I: Mathematical approach and statistical analysis. Magn. Reson. Med. 1996, 36(5):715-725.
84. Pasqualini R., Koivunen E., Kain R., Lahdenranta J., Sakamoto M., Stryhn A., Ashmun R.A., Shapiro L.H., Arap W., Ruoslahti E. Aminopeptidase N is a receptor for tumor-homing peptides and a target for inhibiting angiogenesis. Cancer Res. 2000, 60(3):722-727.
85. Pathak A.P. Magnetic resonance susceptibility based perfusion imaging of tumors using iron oxide nanoparticles. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2009, 1(1):84-97.
86. Pathak A.P., Artemov D., Bhujwalla Z.B. A novel system for determining contrast agent concentration in mouse blood in vivo. Magn. Reson. Med. 2004, 51(3):612-615.
87. Pathak A.P., Hochfeld W.E., Goodman S.L., Pepper M.S. Circulating and imaging markers for angiogenesis. Angiogenesis 2008, 11(4):321-335.
88. Pathak A.P., Rand S.D., Schmainda K.M. The effect of brain tumor angiogenesis on the in vivo relationship between the gradient echo relaxation rate change (DR2*) and contrast agent (MION) dose. J. Magn. Reson. Imaging 2003, 18(4):397-403.
89. Pathak A.P., Schmainda K.M., Ward B.D., Linderman J.R., Rebro K.J., Greene A.S. MR-derived cerebral blood volume maps: Issues regarding histological validation and assessment of tumor angiogenesis. Magn. Reson. Med. 2001, 46(4):735-747.
90. Pathak A.P., Ward B.D., Schmainda K.M. A novel technique for modeling susceptibility-based contrast mechanisms for arbitrary microvascular geometries: The finite perturber method. Neuroimage 2008, 40(3):1130-1143.
91. Patlak C.S., Blasberg R.G., Fenstermacher J.D. Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. J. Cereb. Blood Flow Metab. 1983, 3:1-7.
92. Penet M.F., Pathak A.P., Raman V., Ballesteros P., Artemov D., Bhujwalla Z.M. Noninvasive multiparametric imaging of metastasis-permissive microenvironments in a human prostate cancer xenograft. Cancer Res. 2009, 69(22):8822-8829.
93. Persigehl T., Bieker R., Matuszewski L., Wall A., Kessler T., Kooijman H., Meier N., Ebert W., Berdel W.E., Heindel W., Mesters R.M., Bremer C. Antiangiogenic tumor treatment: Early noninvasive monitoring with USPIO-enhanced MR imaging in mice. Radiology 2007, 244(2):449-456.
94. Provent P., Benito M., Hiba B., Farion R., Lopez-Larrubia P., Ballesteros P., Remy C., Segebarth C., Cerdan S., Coles J.A., Garcia-Martin M.L. Serial in vivo spectroscopic nuclear magnetic resonance imaging of lactate and extracellular pH in rat gliomas shows redistribution of protons away from sites of glycolysis. Cancer Res. 2007, 67(16):7638-7645.
95. Raman V., Artemov D., Pathak A.P., Winnard P.T., McNutt S., Yudina A., Bogdanov A., Bhujwalla Z.M. Characterizing vascular parameters in hypoxic regions: A combined magnetic resonance and optical imaging study of a human prostate cancer model. Cancer Res. 2006, 66(20):9929-9936.
96. Rettig W.J., Garin-Chesa P., Healey J.H., Su S.L., Jaffe E.A., Old L.J. Identification of endosialin, a cell surface glycoprotein of vascular endothelial cells in human cancer. Proc. Natl. Acad. Sci. USA 1992, 89(22):10832-10836.
97. Ribatti D. Early evidence of the vascular phase and its importance in tumor growth. History of Research on Tumor Angiogenesis 2009, 1-17. Springer, Netherlands. D. Ribatti (Ed.).
98. Roberts H.C., Roberts R.C., Brasch R.T., Dillon W.P. Quantitative measurement of microvascular permeability in human brain tumors achieved using dynamic contrast-enhanced MR imaging: Correlation with histologic grade. AJNR Am J Neuroradiol 2000, 21(5):891-899.
99. Rosen B.R., Belliveau J.W., Buchbinder B.R., McKinstry R.C., Porkka L.M., Kennedy D.N., Neuder M.S., Fisel C.R., Aronen H.J., Kwong K.K., Weisskoff R.M., Cohen M.S., et al. Contrast agents and cerebral hemodynamics. Magn. Reson. Med. 1991, 19:285-292.
100. Sato T.N., Tozawa Y., Deutsch U., Wolburg-Buchholz K., Fujiwara Y., Gendron-Maguire M., Gridley T., Wolburg H., Risau W., Qin Y. Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature 1995, 376(6535):70-74.
101. Schlingemann R.O., Rietveld F.J., de Waal R.M., Bradley N.J., Skene A.I., Davies A.J., Greaves M.F., Denekamp J., Ruiter D.J. Leukocyte antigen CD34 is expressed by a subset of cultured endothelial cells and on endothelial abluminal microprocesses in the tumor stroma. Lab. Invest. 1990, 62(6):690-696.
102. Schmainda K.M., Rand S.D., Joseph A.M., Lund R., Ward B.D., Pathak A.P., Ulmer J.L., Badruddoja M.A., Krouwer H.G. Characterization of a first-pass gradient-echo spin-echo method to predict brain tumor grade and angiogenesis. AJNR Am. J. Neuroradiol. 2004, 25(9):1524-1532.
103. Schmieder A.H., Caruthers S.D., Zhang H., Williams T.A., Robertson J.D., Wickline S.A., Lanza G.M. Three-dimensional MR mapping of angiogenesis with alpha5beta1(alpha nu beta3)-targeted theranostic nanoparticles in the MDA-MB-435 xenograft mouse model. FASEB J. 2008, 22(12):4179-4189.
104. 1 mapping. Magn. Reson. Med. 1993, 29:709-712.
105. Semenza G.L. Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene 2010, 29(5):625-634.
106. Senpan A., Caruthers S.D., Rhee I., Mauro N.A., Pan D., Hu G., Scott M.J., Fuhrhop R.W., Gaffney P.J., Wickline S.A., Lanza G.M. Conquering the dark side: Colloidal iron oxide nanoparticles. ACS Nano 2009, 3(12):3917-3926.
107. Silva A.C., Kim S.-G., Garwood M. Imaging blood flow in brain tumors using arterial spin labeling. Magn. Reson. Med. 2000, 44:169-173.
108. Sipkins D.A., Cheresh D.A., Kazemi M.R., Nevin L.M., Bednarski M.D., Li K.C. Detection of tumor angiogenesis in vivo by alphaVbeta3-targeted magnetic resonance imaging. Nat. Med. 1998, 4(5):623-626.
109. Sorensen A.G., Batchelor T.T., Zhang W.T., Chen P.J., Yeo P., Wang M., Jennings D., Wen P.Y., Lahdenranta J., Ancukiewicz M., di Tomaso E., Duda D.G., et al. A "vascular normalization index" as potential mechanistic biomarker to predict survival after a single dose of cediranib in recurrent glioblastoma patients. Cancer Res. 2009, 69(13):5296-5300.
110. Croix B., Rago C., Velculescu V., Traverso G., Romans K.E., Montgomery E., Lal A., Riggins G.J., Lengauer C., Vogelstein B., Kinzler K.W. Genes expressed in human tumor endothelium. Science 2000, 289(5482):1197-1202.
111. Tarli L., Balza E., Viti F., Borsi L., Castellani P., Berndorff D., Dinkelborg L., Neri D., Zardi L. A high-affinity human antibody that targets tumoral blood vessels. Blood 1999, 94(1):192-198.
112. Thomlinson R.H., Gray L.H. The histological structure of some human lung cancers and the possible implications for radiotherapy. Br. J. Cancer 1955, 9(4):539-549.
113. Thompson H.K.J., Starmer C.F., Whalen R.E., McIntosh H.D. Indicator transit time considered as a gamma-variate. Circulation Res. 1964, XIV. June.
114. Tofts P.S. Modeling tracer kinetics in dynamic Gd-DTPA MR imaging. J. Magn. Reson. Imaging 1997, 7(1):91-101.
115. Tofts P.S., Brix G., Evelhoch J.L., Buckley D.L., Henderson E., Larsson H.B., Knopp M.V., Lee T.Y., Parker G.J., Mayr N.A., Taylor J., Port R.E., 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.
116. Torchilin V.P. Recent advances with liposomes as pharmaceutical carriers. Nat. Rev. Drug Discov. 2005, 4(2):145-160.
117. van der Schaft D.W., Seftor R.E., Seftor E.A., Hess A.R., Gruman L.M., Kirschmann D.A., Yokoyama Y., Griffioen A.W., Hendrix M.J. Effects of angiogenesis inhibitors on vascular network formation by human endothelial and melanoma cells. J. Natl. Cancer Inst. 2004, 96(19):1473-1477.
118. Varallyay C.G., Muldoon L.L., Gahramanov S., Wu Y.J., Goodman J.A., Li X., Pike M.M., Neuwelt E.A. Dynamic MRI using iron oxide nanoparticles to assess early vascular effects of antiangiogenic versus corticosteroid treatment in a glioma model. J. Cereb. Blood Flow Metab. 2009, 29(4):853-860.
119. Vaupel P., Kallinowski F., Okunieff P. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: A review. Cancer Res. 1989, 49(23):6449-6465.
120. Villringer A., Rosen B.R., Belliveau J.W., Ackerman J.L., Lauffer R.B., Buxton R.B., Chao Y.S., Wedeen V.J., Brady T.J. Dynamic imaging with lanthanide chelates in normal brain: Contrast due to magnetic susceptibility effects. Magn. Reson. Med. 1988, 6:164-174.
121. Virchow R. Die krankhaften Geschwultste 1863, Hirschwald, Berlin.
122. Weisskoff R.M. Pitfalls in MR measurement of tissue blood flow with intravascular tracers: Which mean transit time. Magn. Reson. Med. 1993, 29:553-559.
123. Weisskoff R.M., Zuo C.S., Boxerman J.L., Rosen B.R. Microscopic susceptibility variation and transverse relaxation: Theory and experiment. Magn. Reson. Med. 1994, 31:601-610.
124. Weissleder R., Cheng H.C., Marecos E., Kwong K., Bogdanov A. Non-invasive in vivo mapping of tumour vascular and interstitial volume fractions. Eur. J. Cancer 1998, 34(9):1448-1454.
125. Willett C.G., Duda D.G., di Tomaso E., Boucher Y., Ancukiewicz M., Sahani D.V., Lahdenranta J., Chung D.C., Fischman A.J., Lauwers G.Y., Shellito P., Czito B.G., et al. Efficacy, safety, and biomarkers of neoadjuvant bevacizumab, radiation therapy, and fluorouracil in rectal cancer: A multidisciplinary phase II study. J. Clin. Oncol. 2009, 27(18):3020-3026.
126. Yablonskiy D.A. Theory of NMR signal behavior in magnetically inhomogeneous tissues: The static dephasing regime. Magn. Reson. Med. 1994, 32:749-763.
127. Yu H., Su M.Y., Wang Z., Nalcioglu O. A longitudinal study of radiation-induced changes in tumor vasculature by contrast-enhanced magnetic resonance imaging. Radiat. Res. 2002, 158(2):152-158.
128. Zaharchuk G. Theoretical basis of hemodynamic MR imaging techniques to measure cerebral blood volume, cerebral blood flow, and permeability. AJNR Am. J. Neuroradiol. 2007, 28(10):1850-1858.
129. Zhang C., Jugold M., Woenne E.C., Lammers T., Morgenstern B., Mueller M.M., Zentgraf H., Bock M., Eisenhut M., Semmler W., Kiessling F. Specific targeting of tumor angiogenesis by RGD-conjugated ultrasmall superparamagnetic iron oxide particles using a clinical 1.5-T magnetic resonance scanner. Cancer Res. 2007, 67(4):1555-1562.
130. Zhao D., Jiang L., Hahn E.W., Mason R.P. Comparison of 1H blood oxygen level-dependent (BOLD) and 19F MRI to investigate tumor oxygenation. Magn. Reson. Med. 2009, 62(2):357-364.
131. Zhu A.X., Holalkere N.S., Muzikansky A., Horgan K., Sahani D.V. Early antiangiogenic activity of bevacizumab evaluated by computed tomography perfusion scan in patients with advanced hepatocellular carcinoma. Oncologist 2008, 13(2):120-125.
132. Zierler K.L. Theoretical basis of indicator-dilution methods for measuring flow and volume. Circulation Res. 1962, X:393-407. March.