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Current Applications of Nanotechnology for Magnetic Resonance Imaging of Apoptosis

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Cancer Nanotechnology

Part of the book series: Methods in Molecular Biology ((MIMB,volume 624))

Abstract

Apoptosis, or programmed cell death, is a morphologically and biochemically distinct form of cell death, which together with proliferation plays an important role in tissue development and homeostasis. Insufficient apoptosis is important in the pathology of various disorders such as cancer and autoimmune diseases, whereas a high apoptotic activity is associated with myocardial infarction, neurodegenerative diseases, and advanced atherosclerotic lesions. Consequently, apoptosis is recognized as an important therapeutic target, which should be either suppressed, e.g., during an ischemic cardiac infarction, or promoted, e.g., in the treatment of cancerous lesions. Imaging tools to address location, amount, and time course of apoptotic activity non-invasively in vivo are therefore of great clinical use in the evaluation of such therapies. This chapter reviews current literature and new developments in the application of nanoparticles for non-invasive apoptosis imaging. Focus is on functionalized nanoparticle contrast agents for MR imaging and bimodal nanoparticle agents that combine magnetic and fluorescent properties.

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References

  1. Kerr, J. F., Wyllie, A. H., and Currie, A. R. (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26, 239–257.

    Article  PubMed  CAS  Google Scholar 

  2. Samali, A., Gorman, A. M., and Cotter, T. G. (1996) Apoptosis the story so far. Experientia 52, 933–941.

    Article  PubMed  CAS  Google Scholar 

  3. Kerr, J. F. (2002) History of the events leading to the formulation of the apoptosis concept. Toxicology 181–182, 471–474.

    Article  PubMed  Google Scholar 

  4. Leist, M. and Jaattela, M. (2001) Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol 2, 589–598.

    Article  PubMed  CAS  Google Scholar 

  5. Van Cruchten, S. and Van Den Broeck, W. (2002) Morphological and biochemical aspects of apoptosis, oncosis and necrosis. Anat Histol Embryol 31, 214–223.

    Article  PubMed  Google Scholar 

  6. van Heerde, W. L., Robert-Offerman, S., Dumont, E., Hofstra, L., Doevendans, P. A., Smits, J. F., Daemen, M. J., and Reutelingsperger, C. P. (2000) Markers of apoptosis in cardiovascular tissues: focus on Annexin V. Cardiovasc Res 45, 549–559.

    Article  PubMed  Google Scholar 

  7. Fadok, V. A., de Cathelineau, A., Daleke, D. L., Henson, P. M., and Bratton, D. L. (2001) Loss of phospholipid asymmetry and surface exposure of phosphatidylserine is required for phagocytosis of apoptotic cells by macrophages and fibroblasts. J Biol Chem 276, 1071–1077.

    Article  PubMed  CAS  Google Scholar 

  8. Devaux, P. F. (1991) Static and dynamic lipid asymmetry in cell membranes. Biochemistry 30, 1163–1173.

    Article  PubMed  CAS  Google Scholar 

  9. Schroit, A. J. and Zwaal, R. F. (1991) Transbilayer movement of phospholipids in red cell and platelet membranes. Biochim Biophys Acta 1071, 313–329.

    PubMed  CAS  Google Scholar 

  10. Balasubramanian, K. and Schroit, A. J. (2003) Aminophospholipid asymmetry: a matter of life and death. Annu Rev Physiol 65, 701–734.

    Article  PubMed  CAS  Google Scholar 

  11. Kolodgie, F. D., Narula, J., Guillo, P., and Virmani, R. (1999) Apoptosis in human atherosclerotic plaques. Apoptosis 4, 5–10.

    Article  PubMed  CAS  Google Scholar 

  12. Haunstetter, A. and Izumo, S. (1998) Apoptosis: basic mechanisms and implications for cardiovascular disease. Circ Res 82, 1111–1129.

    PubMed  CAS  Google Scholar 

  13. Korngold, E. C., Jaffer, F. A., Weissleder, R., and Sosnovik, D. E. (2008) Noninvasive imaging of apoptosis in cardiovascular disease. Heart Fail Rev 13, 163–173.

    Article  PubMed  Google Scholar 

  14. Anversa, P., Cheng, W., Liu, Y., Leri, A., Redaelli, G., and Kajstura, J. (1998) Apoptosis and myocardial infarction. Basic Res Cardiol 93(Suppl 3), 8–12.

    Article  PubMed  Google Scholar 

  15. Kang, P. M. and Izumo, S. (2003) Apoptosis in heart: basic mechanisms and implications in cardiovascular diseases. Trends Mol Med 9, 177–182.

    Article  PubMed  CAS  Google Scholar 

  16. Olivetti, G., Quaini, F., Sala, R., Lagrasta, C., Corradi, D., Bonacina, E., Gambert, S. R., Cigola, E., and Anversa, P. (1996) Acute myocardial infarction in humans is associated with activation of programmed myocyte cell death in the surviving portion of the heart. J Mol Cell Cardiol 28, 2005–2016.

    Article  PubMed  CAS  Google Scholar 

  17. Bardales, R. H., Hailey, L. S., Xie, S. S., Schaefer, R. F., and Hsu, S. M. (1996) In situ apoptosis assay for the detection of early acute myocardial infarction. Am J Pathol 149, 821–829.

    PubMed  CAS  Google Scholar 

  18. Saraste, A., Pulkki, K., Kallajoki, M., Henriksen, K., Parvinen, M., and Voipio-Pulkki, L. M. (1997) Apoptosis in human acute myocardial infarction. Circulation 95, 320–323.

    PubMed  CAS  Google Scholar 

  19. Gottlieb, R. A., Burleson, K. O., Kloner, R. A., Babior, B. M., and Engler, R. L. (1994) Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J Clin Invest 94, 1621–1628.

    Article  PubMed  CAS  Google Scholar 

  20. Garg, S., Narula, J., and Chandrashekhar, Y. (2005) Apoptosis and heart failure: clinical relevance and therapeutic target. J Mol Cell Cardiol 38, 73–79.

    Article  PubMed  CAS  Google Scholar 

  21. Davies, M. J., Richardson, P. D., Woolf, N., Katz, D. R., and Mann, J. (1993) Risk of thrombosis in human atherosclerotic plaques: role of extracellular lipid, macrophage, and smooth muscle cell content. Br Heart J 69, 377–381.

    Article  PubMed  CAS  Google Scholar 

  22. Libby, P., Geng, Y. J., Aikawa, M., Schoenbeck, U., Mach, F., Clinton, S. K., Sukhova, G. K., and Lee, R. T. (1996) Macrophages and atherosclerotic plaque stability. Curr Opin Lipidol 7, 330–335.

    Article  PubMed  CAS  Google Scholar 

  23. Kolodgie, F. D., Narula, J., Burke, A. P., Haider, N., Farb, A., Hui-Liang, Y., Smialek, J., and Virmani, R. (2000) Localization of apoptotic macrophages at the site of plaque rupture in sudden coronary death. Am J Pathol 157, 1259–1268.

    PubMed  CAS  Google Scholar 

  24. Kolodgie, F. D., Petrov, A., Virmani, R., Narula, N., Verjans, J. W., Weber, D. K., Hartung, D., Steinmetz, N., Vanderheyden, J. L., Vannan, M. A., Gold, H. K., Reutelingsperger, C. P., Hofstra, L., and Narula, J. (2003) Targeting of apoptotic macrophages and experimental atheroma with radiolabeled annexin V: a technique with potential for noninvasive imaging of vulnerable plaque. Circulation 108, 3134–3139.

    Article  PubMed  CAS  Google Scholar 

  25. Li, W., Hellsten, A., Jacobsson, L. S., Blomqvist, H. M., Olsson, A. G., and Yuan, X. M. (2004) Alpha-tocopherol and astaxanthin decrease macrophage infiltration, apoptosis and vulnerability in atheroma of hyperlipidaemic rabbits. J Mol Cell Cardiol 37, 969–978.

    Article  PubMed  CAS  Google Scholar 

  26. Carson, D. A. and Ribeiro, J. M. (1993) Apoptosis and disease. Lancet 341, 1251–1254.

    Article  PubMed  CAS  Google Scholar 

  27. Brown, J. M. and Attardi, L. D. (2005) The role of apoptosis in cancer development and treatment response. Nat Rev Cancer 5, 231–237.

    Article  PubMed  Google Scholar 

  28. Meyn, R. E., Stephens, L. C., Hunter, N. R., and Milas, L. (1995) Apoptosis in murine tumors treated with chemotherapy agents. Anticancer Drugs 6, 443–450.

    Article  PubMed  CAS  Google Scholar 

  29. Dubray, B., Breton, C., Delic, J., Klijanienko, J., Maciorowski, Z., Vielh, P., Fourquet, A., Dumont, J., Magdelenat, H., and Cosset, J. M. (1997) In vitro radiation-induced apoptosis and tumour response to radiotherapy: a prospective study in patients with non-Hodgkin lymphomas treated by low-dose irradiation. Int J Radiat Biol 72, 759–60.

    Google Scholar 

  30. Dubray, B., Breton, C., Delic, J., Klijanienko, J., Maciorowski, Z., Vielh, P., Fourquet, A., Dumont, J., Magdelenat, H., and Cosset, J. M. (1998) In vitro radiation-induced apoptosis and early response to low-dose radiotherapy in non-Hodgkin’s lymphomas. Radiother Oncol 46, 185–191.

    Article  PubMed  CAS  Google Scholar 

  31. Strijkers, G. J., Mulder, W. J., van Tilborg, G. A., and Nicolay, K. (2007) MRI contrast agents: current status and future perspectives. Anticancer Agents Med Chem 7, 291–305.

    Article  PubMed  CAS  Google Scholar 

  32. Armitage, F. E., Richardson, D. E., and Li, K. C. (1990) Polymeric contrast agents for magnetic resonance imaging: synthesis and characterization of gadolinium diethylenetriaminepentaacetic acid conjugated to polysaccharides. Bioconjug Chem 1, 365–374.

    Article  PubMed  CAS  Google Scholar 

  33. Aime, S., Botta, M., Geninatti Crich, S., Giovenzana, G., Palmisano, G., and Sisti, M. (1999) Novel paramagnetic macromolecular complexes derived from the linkage of a macrocyclic Gd(III) complex to polyamino acids through a squaric acid moiety. Bioconjug Chem 10, 192–199.

    Article  PubMed  CAS  Google Scholar 

  34. Wang, S. J., Brechbiel, M., and Wiener, E. C. (2003) Characteristics of a new MRI contrast agent prepared from polypropyleneimine dendrimers, generation 2. Invest Radiol 38, 662–668.

    Article  PubMed  CAS  Google Scholar 

  35. Kobayashi, H. and Brechbiel, M. W. (2004) Dendrimer-based nanosized MRI contrast agents. Curr Pharm Biotechnol 5, 539–549.

    Article  PubMed  CAS  Google Scholar 

  36. de Lussanet, Q. G., Langereis, S., Beets-Tan, R. G., van Genderen, M. H., Griffioen, A. W., van Engelshoven, J. M., and Backes, W. H. (2005) Dynamic contrast-enhanced MR imaging kinetic parameters and molecular weight of dendritic contrast agents in tumor angiogenesis in mice. Radiology 235, 65–72.

    Article  PubMed  Google Scholar 

  37. Storrs, R. W., Tropper, F. D., Li, H. Y., Song, C. K., Sipkins, D. A., Kuniyoshi, J. K., Bednarski, M. D., Strauss, H. W., and Li, K. C. (1995) Paramagnetic polymerized liposomes as new recirculating MR contrast agents. J Magn Reson Imaging 5, 719–724.

    Article  PubMed  CAS  Google Scholar 

  38. Torchilin, V. P. (2002) PEG-based micelles as carriers of contrast agents for different imaging modalities. Adv Drug Deliv Rev 54, 235–252.

    Article  PubMed  CAS  Google Scholar 

  39. Glogard, C., Stensrud, G., Hovland, R., Fossheim, S. L., and Klaveness, J. (2002) Liposomes as carriers of amphiphilic gadolinium chelates: the effect of membrane composition on incorporation efficacy and in vitro relaxivity. Int J Pharm 233, 131–140.

    Article  PubMed  CAS  Google Scholar 

  40. Glogard, C., Stensrud, G., and Klaveness, J. (2003) Novel high relaxivity colloidal particles based on the specific phase organisation of amphiphilic gadolinium chelates with cholesterol. Int J Pharm 253, 39–48.

    Article  PubMed  CAS  Google Scholar 

  41. Hovland, R., Glogard, C., Aasen, A. J., and Klaveness, J. (2003) Preparation and in vitro evaluation of a novel amphiphilic GdPCTA-[12] derivative; a micellar MRI contrast agent. Org Biomol Chem 1, 644–647.

    Article  PubMed  CAS  Google Scholar 

  42. Mulder, W. J., Strijkers, G. J., Griffioen, A. W., van Bloois, L., Molema, G., Storm, G., Koning, G. A., and Nicolay, K. (2004) A liposomal system for contrast-enhanced magnetic resonance imaging of molecular targets. Bioconjug Chem 15, 799–806.

    Article  PubMed  CAS  Google Scholar 

  43. Nitin, N., LaConte, L. E., Zurkiya, O., Hu, X., and Bao, G. (2004) Functionalization and peptide-based delivery of magnetic nanoparticles as an intracellular MRI contrast agent. J Biol Inorg Chem 9, 706–712.

    Article  PubMed  CAS  Google Scholar 

  44. Nitin, N., Santangelo, P. J., Kim, G., Nie, S., and Bao, G. (2004) Peptide-linked molecular beacons for efficient delivery and rapid mRNA detection in living cells. Nucleic Acids Res 32, e58.

    Article  PubMed  CAS  Google Scholar 

  45. Morawski, A. M., Winter, P. M., Crowder, K. C., Caruthers, S. D., Fuhrhop, R. W., Scott, M. J., Robertson, J. D., Abendschein, D. R., Lanza, G. M., and Wickline, S. A. (2004) Targeted nanoparticles for quantitative imaging of sparse molecular epitopes with MRI. Magn Reson Med 51, 480–486.

    Article  PubMed  CAS  Google Scholar 

  46. Strijkers, G. J., Mulder, W. J., van Heeswijk, R. B., Frederik, P. M., Bomans, P., Magusin, P. C., and Nicolay, K. (2005) Relaxivity of liposomal paramagnetic MRI contrast agents. MAGMA 18, 186–192.

    Article  PubMed  CAS  Google Scholar 

  47. van Tilborg, G. A., Mulder, W. J., Chin, P. T., Storm, G., Reutelingsperger, C. P., Nicolay, K., and Strijkers, G. J. (2006) Annexin A5-conjugated quantum dots with a paramagnetic lipidic coating for the multimodal detection of apoptotic cells. Bioconjug Chem 17, 865–868.

    Article  PubMed  CAS  Google Scholar 

  48. van Tilborg, G. A., Mulder, W. J., Deckers, N., Storm, G., Reutelingsperger, C. P., Strijkers, G. J., and Nicolay, K. (2006) Annexin A5-functionalized bimodal lipid-based contrast agents for the detection of apoptosis. Bioconjug Chem 17(3), 741–749.

    Article  PubMed  CAS  Google Scholar 

  49. Laurent, S., Forge, D., Port, M., Roch, A., Robic, C., Vander Elst, L., and Muller, R. N. (2008) Magnetic iron oxide nanoparticles: synthesis, stabilization, vectorization, physicochemical characterizations, and biological applications. Chem Rev 108, 2064–2110.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  51. Wunderbaldinger, P., Josephson, L., and Weissleder, R. (2002) Crosslinked iron oxides (CLIO): a new platform for the development of targeted MR contrast agents. Acad Radiol 9(Suppl 2), S304–S306.

    Article  PubMed  Google Scholar 

  52. Mulder, W. J., Koole, R., Brandwijk, R. J., Storm, G., Chin, P. T., Strijkers, G. J., de Mello Donega, C., Nicolay, K., and Griffioen, A. W. (2006) Quantum dots with a paramagnetic coating as a bimodal molecular imaging probe. Nano Lett 6, 1–6.

    Article  PubMed  CAS  Google Scholar 

  53. Schellenberger, E. A., Bogdanov, A., Högemann, D., Tait, J., Weissleder, R., and Josephson, L. (2002) Annexin V-CLIO: a nanoparticle for detecting apoptosis by MRI. Mol Imaging 1, 102–107.

    Article  PubMed  CAS  Google Scholar 

  54. Tait, J. F., Gibson, D., and Fujikawa, K. (1989) Phospholipid binding properties of human placental anticoagulant protein-I, a member of the lipocortin family. J Biol Chem 264, 7944–7949.

    PubMed  CAS  Google Scholar 

  55. Andree, H. A., Reutelingsperger, C. P., Hauptmann, R., Hemker, H. C., Hermens, W. T., and Willems, G. M. (1990) Binding of vascular anticoagulant alpha (VAC alpha) to planar phospholipid bilayers. J Biol Chem 265, 4923–4928.

    PubMed  CAS  Google Scholar 

  56. van Engeland, M., Nieland, L. J., Ramaekers, F. C., Schutte, B., and Reutelingsperger, C. P. (1998) Annexin V-affinity assay: a review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry 31, 1–9.

    Article  PubMed  Google Scholar 

  57. Schellenberger, E. A., Högemann, D., Josephson, L., and Weissleder, R. (2002) Annexin V-CLIO: a nanoparticle for detecting apoptosis by MRI. Acad Radiol 9(Suppl 2), S.

    Google Scholar 

  58. Schellenberger, E., Schnorr, J., Reutelingsperger, C., Ungethüm, L., Meyer, W., Taupitz, M., and Hamm, B. (2008) Linking proteins with anionic nanoparticles via protamine: ultrasmall protein-coupled probes for magnetic resonance imaging of apoptosis. Small 4, 225–230.

    Article  PubMed  CAS  Google Scholar 

  59. Jung, H. I., Kettunen, M. I., Davletov, B., and Brindle, K. M. (2004) Detection of apoptosis using the C2A domain of synaptotagmin I. Bioconjug Chem 15, 983–987.

    Article  PubMed  CAS  Google Scholar 

  60. Neves, A. A., Krishnan, A. S., Kettunen, M. I., Hu, D. E., Backer, M. M., Davletov, B., and Brindle, K. M. (2007) A paramagnetic nanoprobe to detect tumor cell death using magnetic resonance imaging. Nano Lett 7, 1419–1423.

    Article  PubMed  CAS  Google Scholar 

  61. Prinzen, L., Miserus, R. J., Dirksen, A., Hackeng, T. M., Deckers, N., Bitsch, N. J., Megens, R. T., Douma, K., Heemskerk, J. W., Kooi, M. E., Frederik, P. M., Slaaf, D. W., van Zandvoort, M. A., and Reutelingsperger, C. P. (2007) Optical and magnetic resonance imaging of cell death and platelet activation using annexin a5-functionalized quantum dots. Nano Lett 7, 93–100.

    Article  PubMed  CAS  Google Scholar 

  62. Hernandez-Sanchez, B. A., Boyle, T. J., Lambert, T. N., Daniel-Taylor, S. D., Oliver, J. M., Wilson, B. S., Lidke, D. S., and Andrews, N. L. (2006) Synthesizing biofunctionalized nanoparticles to image cell signaling pathways. IEEE Trans Nanobiosci 5, 222–230.

    Article  Google Scholar 

  63. Kim, K., Lee, M., Park, H., Kim, J. H., Kim, S., Chung, H., Choi, K., Kim, I. S., Seong, B. L., and Kwon, I. C. (2006) Cell-permeable and biocompatible polymeric nanoparticles for apoptosis imaging. J Am Chem Soc 128, 3490–1.

    Google Scholar 

  64. Le Gac, S., Vermes, I., and van den Berg, A. (2006) Quantum dots based probes conjugated to annexin V for photostable apoptosis detection and imaging. Nano Lett 6, 1863–1869.

    Article  PubMed  CAS  Google Scholar 

  65. Koeppel, F., Jaiswal, J. K., and Simon, S. M. (2007) Quantum dot-based sensor for improved detection of apoptotic cells. Nanomedicine (London, England) 2, 71–78.

    Article  CAS  Google Scholar 

  66. Shi, H., He, X., Wang, K., Yuan, Y., Deng, K., Chen, J., and Tan, W. (2007) Rhodamine B isothiocyanate doped silica-coated fluorescent nanoparticles (RBITC-DSFNPs)-based bioprobes conjugated to Annexin V for apoptosis detection and imaging. Nanomedicine 3, 266–272.

    PubMed  CAS  Google Scholar 

  67. Yu, K. N., Lee, S. M., Han, J. Y., Park, H., Woo, M. A., Noh, M. S., Hwang, S. K., Kwon, J. T., Jin, H., Kim, Y. K., Hergenrother, P. J., Jeong, D. H., Lee, Y. S., and Cho, M. H. (2007) Multiplex targeting, tracking, and imaging of apoptosis by fluorescent surface enhanced Raman spectroscopic dots. Bioconjug Chem 18, 1155–1162.

    Article  PubMed  CAS  Google Scholar 

  68. Sosnovik, D. E., Schellenberger, E. A., Nahrendorf, M., Novikov, M. S., Matsui, T., Dai, G., Reynolds, F., Grazette, L., Rosenzweig, A., Weissleder, R., and Josephson, L. (2005) Magnetic resonance imaging of cardiomyocyte apoptosis with a novel magneto-optical nanoparticle. Magn Reson Med 54, 718–724.

    Article  PubMed  Google Scholar 

  69. Hiller, K. H., Waller, C., Nahrendorf, M., Bauer, W. R., and Jakob, P. M. (2006) Assessment of cardiovascular apoptosis in the isolated rat heart by magnetic resonance molecular imaging. Mol Imaging 5, 115–121.

    PubMed  Google Scholar 

  70. Brindle, K. M. (2003) Molecular imaging using magnetic resonance: new tools for the development of tumour therapy. Br J Radiol 76 Spec No 2 , S111–S117.

    Article  PubMed  CAS  Google Scholar 

  71. Neves, A. A. and Brindle, K. M. (2006) Assessing responses to cancer therapy using molecular imaging. Biochim Biophys Acta 1766, 242–261.

    PubMed  CAS  Google Scholar 

  72. Raman, V., Pathak, A. P., Glunde, K., Artemov, D., and Bhujwalla, Z. M. (2007) Magnetic resonance imaging and spectroscopy of transgenic models of cancer. NMR Biomed 20, 186–199.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  74. Mulder, W. J., van der Schaft, D. W., Hautvast, P. A., Strijkers, G. J., Koning, G. A., Storm, G., Mayo, K. H., Griffioen, A. W., and Nicolay, K. (2007) Early in vivo assessment of angiostatic therapy efficacy by molecular MRI. FASEB J 21, 378–383.

    Article  PubMed  CAS  Google Scholar 

  75. Chenevert, T. L., Meyer, C. R., Moffat, B. A., Rehemtulla, A., Mukherji, S. K., Gebarski, S. S., Quint, D. J., Robertson, P. L., Lawrence, T. S., Junck, L., Taylor, J. M., Johnson, T. D., Dong, Q., Muraszko, K. M., Brunberg, J. A., and Ross, B. D. (2002) Diffusion MRI: a new strategy for assessment of cancer therapeutic efficacy. Mol Imaging 1, 336–343.

    Article  PubMed  Google Scholar 

  76. Ross, B. D., Moffat, B. A., Lawrence, T. S., Mukherji, S. K., Gebarski, S. S., Quint, D. J., Johnson, T. D., Junck, L., Robertson, P. L., Muraszko, K. M., Dong, Q., Meyer, C. R., Bland, P. H., McConville, P., Geng, H., Rehemtulla, A., and Chenevert, T. L. (2003) Evaluation of cancer therapy using diffusion magnetic resonance imaging. Mol Cancer Ther 2, 581–587.

    PubMed  CAS  Google Scholar 

  77. Moffat, B. A., Chenevert, T. L., Lawrence, T. S., Meyer, C. R., Johnson, T. D., Dong, Q., Tsien, C., Mukherji, S., Quint, D. J., Gebarski, S. S., Robertson, P. L., Junck, L. R., Rehemtulla, A., and Ross, B. D. (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.

    Article  PubMed  CAS  Google Scholar 

  78. Brindle, K. M. (2002) Detection of apoptosis in tumors using magnetic resonance imaging and spectroscopy. Adv Enzyme Regul 42, 101–112.

    Article  PubMed  CAS  Google Scholar 

  79. Zhao, M., Beauregard, D. A., Loizou, L., Davletov, B., and Brindle, K. M. (2001) Non-invasive detection of apoptosis using magnetic resonance imaging and a targeted contrast agent. Nat Med 7, 1241–1244.

    Article  PubMed  CAS  Google Scholar 

  80. Krishnan, A. S., Neves, A. A., de Backer, M. M., Hu, D. E., Davletov, B., Kettunen, M. I., and Brindle, K. M. (2008) Detection of cell death in tumors by using MR imaging and a gadolinium-based targeted contrast agent. Radiology 246, 854–862.

    Article  PubMed  Google Scholar 

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Acknowledgments

This research was supported by the Dutch Technology Foundation STW, applied science division of NWO and the Technology Program of the Ministry of Economic Affairs (grant number 07952). This study was funded in part by the BSIK program entitled Molecular Imaging of Ischemic Heart Disease (project number BSIK03033) and by the EC – FP6-project DiMI, LSHB-CT-2005-512146. This study was performed in the framework of the European Cooperation in the field of Scientific and Technical Research (COST) D38 Action Metal-Based Systems for Molecular Imaging Applications.

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Authors and Affiliations

  1. Biomedical NMR, Department of Biomedical Engineering, Eindhoven University of Technology, Eindhoven, The Netherlands

    Gustav J. Strijkers, Geralda A.F. van Tilborg, Tessa Geelen & Klaas Nicolay

  2. Department of Biochemistry, Cardiovascular Research Institute Maastricht, University of Maastricht, Maastricht, The Netherlands

    Chris P.M. Reutelingsperger

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  1. Gustav J. Strijkers
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  2. Geralda A.F. van Tilborg
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  3. Tessa Geelen
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  4. Chris P.M. Reutelingsperger
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  1. Dept. Surgery, University of Florida, Gainesville, USA

    Stephen R. Grobmyer

  2. ERC - Engineering Research Center, University of Florida, Gainesville, USA

    Brij M. Moudgil

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Strijkers, G.J., van Tilborg, G.A., Geelen, T., Reutelingsperger, C.P., Nicolay, K. (2010). Current Applications of Nanotechnology for Magnetic Resonance Imaging of Apoptosis. In: Grobmyer, S., Moudgil, B. (eds) Cancer Nanotechnology. Methods in Molecular Biology, vol 624. Humana Press. https://doi.org/10.1007/978-1-60761-609-2_22

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