In vivo imaging of apoptosis in oncology: An update

Molecular Imaging

Volumn 10, Issue 5, 2011, Pages 340-358

  Vangestel, Christel ^a   Peeters, Marc ^b   Mees, Gilles ^c   Oltenfreiter, Ruth ^d   Boersma, Hendrikus H ^a   Elsinga, Philip H ^a   Reutelingsperger, Chris ^a   Van Damme, Nancy ^a   De Spiegeleer, Bart ^a   Van De Wiele, Christophe ^a  

^a GHENT UNIVERSITY HOSPITAL   (Belgium)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c MAASTRICHT UNIVERSITY   (Netherlands)

^d GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANNEXINS; APOPTOSIS IMAGING; APOPTOTIC PROCESS; APPARENT DIFFUSION COEFFICIENT; BIOLUMINESCENCE IMAGING; CLINICAL STUDY; HUMAN BODIES; IMAGING DATA; IN-VIVO IMAGING; NEAR-INFRARED FLUORESCENCE IMAGING; NON-INVASIVE IMAGING; SMALL ANIMAL IMAGING; TUMOR RESPONSE; UNIQUE IDENTIFIERS;

CELL DEATH; MAGNETIC RESONANCE SPECTROSCOPY; ONCOLOGY; POSITRON EMISSION TOMOGRAPHY; PROBES; SINGLE PHOTON EMISSION COMPUTED TOMOGRAPHY; SURFACE DIFFUSION; TUMORS; ULTRASONOGRAPHY;

MAGNETIC RESONANCE IMAGING;

ANIMAL; APOPTOSIS; CHEMISTRY; COMPUTER ASSISTED EMISSION TOMOGRAPHY; DIAGNOSTIC IMAGING; FEMALE; HUMAN; MALE; NEOPLASM; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PATHOLOGY; PHYSIOLOGY; REVIEW;

ANIMALS; APOPTOSIS; DIAGNOSTIC IMAGING; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; MALE; NEOPLASMS; TOMOGRAPHY, EMISSION-COMPUTED;

EID: 80052976580     PISSN: 15353508     EISSN: None     Source Type: Journal    
DOI: 10.2310/7290.2010.00058     Document Type: Article

References (94)

1. Gerl R, Vaux DL. Apoptosis in the development and treatment of cancer. Carcinogenesis 2005;26:263-70, doi:10.1093/carcin/bgh283. (Pubitemid 40246548)
2. Reed JC. Dysregulation of apoptosis in cancer. J Clin Oncol 1999; 17:2941-53. (Pubitemid 29415256)
3. Hengartner MO. The biochemistry of apoptosis. Nature 2000;407: 770-6, doi:10.1038/35037710.
4. Leist M, Jäättelä M. Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol 2001;2:589-98, doi:10.1038/35085008. (Pubitemid 33674010)
5. Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled annexin V. J Immunol Methods 1995;184:39-51, doi:10.1016/0022-1759(95)00072-I.
6. Zwaal RF, Comfurius P, Bevers EM. Surface exposure of phosphatidylserine in pathological cells. Cell Moll Life Sci 2005; 62:971-88, doi:10.1007/s00018- 005-4527-3. (Pubitemid 40655614)
7. Corsten MF, Hofstra L, Narula J, et al. Counting heads in the war against cancer: defining the role of annexin A5 imaging in cancer treatment and surveillance. Cancer Res 2006;66:1255-60, doi:10. 1158/0008-5472.CAN-05-3000. (Pubitemid 43259900)
8. Munoz LE, Frey B, Pausch F, et al. The role of annexin A5 in the modulation of the immune response against dying and dead cells Curr Med Chem 2007;14:271-7, doi:10.2174/092986707779941131.
9. Haberkorn U, Kinscherf R, Krammer PH, et al. Investigation of a potential scintigraphic marker of apoptosis: radioiodinated Z-Val- Ala-DL-Asp(O-methyl)- fluoromethyl ketone. Nucl Med Biol 2001; 28:793-8, doi:10.1016/S0969-8051(01) 00247-5. (Pubitemid 32900637)
10. Faust A, Wagner S, Law MP, et al. The nonpeptidyl caspase binding radioligand (S)-1-(4-(2-[18]fluoroethoxy)-benzyl)-5-[1- (2- methoxymethylpyrrolidinyl) sulfonyl] isatin ([18F]CbR) as potential positron emission tomography-compatible apoptosis imaging agent. Q J Nucl Med Mol Imaging 2007;51:67-73. (Pubitemid 46824663)
11. Scott DL, Adams JL, Chan G, et al. Potent and selective nonpetide inhibitors of caspase 3 and 7 inhibit apoptosis and maintain cell functionality. J Biol Chem 2000;276:16007-14. (Pubitemid 30366906)
12. 18F-labelled isatin analog for imaging caspase-3 activation of apoptosis. Bioorg Med Chem Lett 2006;16: 5041-6, doi:10.1016/j.bmcl.2006.07.045. (Pubitemid 44247712)
13. Chen DL, Zhou D, Chu W, et al. Comparison of radiolabeled isatin analogs for imaging apoptosis with positron emission tomography. Nucl Med Biol 2009;36:651-8, doi:10.1016/j.nucmedbio.2009. 03.008.
14. 131I-labelled peptides as caspase substrates for apoptosis imaging. J Nucl Med 2005;46: 1066-74. (Pubitemid 43733525)
15. Laxman B, Hall DE, Bhojani MS, et al. Noninvasive real-time imaging of apoptosis. PNAS 2002;99:16551-5, doi:10.1073/ pnas.252644499. (Pubitemid 36034010)
16. Coppola JM, Ross BD, Rehemtulla A. Noninvasive imaging of apoptosis and its application in cancer therapeutics. Clin Cancer Res 2008;14:2492-501, doi:10.1158/1078-0432.CCR-07-0782. (Pubitemid 351551085)
17. Blankenberg FG, Katsikis PD, Tait JF, et al. In vivo detection and imaging of phosphatidylserine expression during programmed cell death. Proc Natl Acad Sci U S A 1998;95:6349-54, doi:10.1073/ pnas.95.11.6349. (Pubitemid 28249015)
18. 99mTc annexin V. J Nucl Med 1999; 40:184-91. (Pubitemid 29044190)
19. Ohtsuki K, Akashi K, Aoka Y, et al. Technetium-99m HYNICannexin A5: a potential radiopharmaceutical for the in-vivo detection of apoptosis. Eur J Nucl Med 1999;26:1251-8, doi:10.1007/s002590050580. (Pubitemid 29467018)
20. Blankenberg F. To scan or not to scan, it is a question of timing: technetium-99m-annexin A5 radionuclide imaging assessement of treatment efficacy after one course of chemotherapy Clin Cancer Res 2002;8:2757-8. (Pubitemid 35025716)
21. 99mTc-HYNIC- annexin A5 uptake and histological findings in an experimental model. J Nucl Med 2004;45:2083-7. (Pubitemid 47611639)
22. 99mTc-HYNIC-annexin A5, a novel human recombinant annexin A5 for human application. J Nucl Med 2003;44: 947-52. (Pubitemid 39663407)
23. 99mTc-HYNIC-annexin A5 imaging of primary head and neck carcinoma. Nucl Med Commun 2004;25:259-63, doi:10.1097/00006231-200403000- 00008. (Pubitemid 38393517)
24. Van de Wiele C, Lahorte C, Vermeersch H, et al. Quantitative tumour apoptosis imaging using technetium-99m-HYNIC annexin A5 single photon emission computed tomography. J Clin Oncol 2003;21:3483-7, doi:10.1200/JCO.2003.12.096. (Pubitemid 46594081)
25. 99mTc-HYNIC-annexin A5 imaging in head and neck carcinoma. Cancer Biother Radiopharm 2004;19:205-10, doi:10.1089/108497804323071986. (Pubitemid 38691096)
26. 99mTc-hydrazinonicotinamide- annexin A5 in patients. Q J Nucl Med Mol Imaging 2009;53: 127-32.
27. 99mTc-HYNICrh- annexin A5 scintigraphy: visual and quantitative evaluation of early treatment-induced apoptosis to predict treatment outcome. Nucl Med Commun 2008;29:39-44, doi:10.1097/MNM.0b013 e3282f1bc22. (Pubitemid 351339339)
28. 99mTc-HYNIC-rh-annexin A5 scintigraphy during platinum-based chemotherapy in advanced lung cancer. J Clin Oncol 2007;25:2534-9, doi:10.1200/JCO.2006.10.1337. (Pubitemid 47041226)
29. 99mTc-annexin A5 scintigraphy: visual analysis in relation to treatment response. Radiol Oncol 2004;72:333-9, doi:10.1016/j. radonc.2004.07.008. (Pubitemid 39265388)
30. 99mTchydrazinonicotinamide- annexin A5 imaging for predicting response to chemotherapy. J Nucl Med 2006;47:1813-8. (Pubitemid 47545004)
31. 99mTc-HYNIC-annexin V imaging of early tumor apoptosis in mice after single dose irradiation. J Exp Clin Can Res 2009;28:136-44, doi:10.1186/1756- 9966-28-136.
32. Haas RLM, de Jong D, Valdés Olmos RA, et al. In vivo imaging of radiation-induced apoptosis in follicular lymphoma patients. Int J Radiat Oncol Biol Phys 2004;59:782-7. (Pubitemid 38748743)
33. 99mTc HYNIC-rhannexin A5 scintigraphy for in vivo imaging of apoptosis in patients with head and neck cancer treated with chemoradiotherapy. Eur J Nucl Med Mol Imaging 2008;35:509-18, doi:10.1007/ s00259-007-0624-x.
34. 99mTc-MAG3- annexin A5: influence of the chelate on in vitro and in vivo properties in mice. Nucl Med Biol 2006;33:135-44, doi:10.1016/ j.nucmedbio.2005.09.002. (Pubitemid 43184088)
35. 99mTc-ECannexin A5. Cancer Biother Radiopharm 2001;16:73-83, doi:10.1089/108497801750096087. (Pubitemid 32231719)
36. 99mTc-EC-annexin A5: preliminary clinical study targeting apoptosis in breast tumours. Appl Radiat Isot 2008;66:1175-82, doi:10.1016/j.apradiso. 2008.01.012. (Pubitemid 352033708)
37. 99mTc-BTAP-annexin A5 in humans. Eur J Nucl Med 2001;28:1373-8, doi:10.1007/s002590100578.
38. 99mTc-annexin A5. Br J Radiol 2003;76:553-60, doi:10.1259/bjr/ 30385847. (Pubitemid 37028410)
39. 99mTc recombinant human annexin A5 in human tumours after one course of chemotherapy as a predictor of tumour response and patient prognosis. Clin Cancer Res 2002;8: 2766-74. (Pubitemid 35025718)
40. Belhocine T, Steinmetz N, Green A, et al. In vivo imaging of chemotherapy-induced apoptosis in human cancers. Ann N Y Acad Sci 2003;1010:525-9, doi:10.1196/annals.1299.097. (Pubitemid 38265038)
41. 99mTc-annexin A5. J Nucl Med 2005;46:807-15.
42. 99mTc-HYNIC-B1 as a novel radioligand for apoptosis imaging. Apoptosis 2008;13:600-8, doi:10.1007/s10495-008-0189-6.
43. 99mTc-labelled HYNIC-Cys-annexin A5 as an apoptosis imaging agent. Bioorg Med Lett 2008;18:3794-8, doi:10.1016/j.bmcl. 2008.05.044. (Pubitemid 351794510)
44. 99mTclabeled annexin A5 variant for non-invasive SPECT imaging of cell death in liver, spleen and prostate. Pharm Res 2009;26:2647-56, doi:10.1007/s11095-009-9981-4.
45. Lahorte CMW, Slegers G, Philippé J, et al. Synthesis and in vitro evaluation of 123I-labelled human annexin A5. Biomed Eng 2001; 17:51-3. (Pubitemid 32037127)
46. Lahorte CMW, Van de Wiele C, Bacher K, et al. Biodistribution and dosimetry study of I-123-rh-annexin A5 in mice and humans. Nucl Med Commun 2003;24:871-80, doi:10.1097/00006231- 200308000-00005.
47. Cornelissen B, Lahorte CMW, Kersemans V, et al. In vivo apoptosis detection with radioiodinated annexin A5 in LoVo tumour-bearing mice following tipifarnib (Zarnestra, R115777) farnesyltransferase inhibitor therapy. Nucl Med Biol 2005;32:233-9, doi:10.1016/j.nucmedbio.2005.01.001. (Pubitemid 40488380)
48. Zavitsanou K, Nguyen V, Greguric I, et al. Detection of apoptotic cell death in the thymus of dexamethasone treated rats using [I123]annexin A5 and in situ oligonucleotide ligation. J Mol Hist 2007;38:313-9, doi:10.1007/s10735-007- 9104-7. (Pubitemid 47106905)
49. 111In-labelled annexin A5. J Nucl Med 2004;45:108-15. (Pubitemid 47611616)
50. 18F-labelled annexin A5: a PET tracer for apoptosis imaging. Eur J Nucl Med Mol Imaging 2004;31:469-74, doi:10.1007/s00259-003-1378-8. (Pubitemid 38461560)
51. Toretsky J, Levenson A, Weinberg IN, et al. Preparation of F-18 labelled annexin A5: a potential PET radiopharmaceutical for imaging cell death. Nucl Med Biol 2004;31:747-52, doi:10.1016/ j.nucmedbio.2004.02.007. (Pubitemid 38887756)
52. 18F-labelled recombinant annexin A5 derivative, for identification and quantification of apoptotic cells with PET. Appl Radiat Isot 2003;58:201-7, doi:10.1016/S0969-8043(02)00302-0. (Pubitemid 36172511)
53. 18F-annexin A5 as a PET imaging agent in an animal model of apoptosis. J Nucl Med 2005;46:658-66. (Pubitemid 41716411)
54. Cauchon N, Langlois R, Rousseau JA, et al. PET imaging of apoptosis with 64Cu-labelled streptavidin following pretargeting of phosphatidylserine with biotinylated annexin A5. Eur J Nucl Med Mol Imaging 2007;34:247-58, doi:10.1007/s00259-006-0199-y. (Pubitemid 46147508)
55. Russell J, O'Donoghue JA, Finn R, et al. Iodination of annexin A5 for imaging apoptosis. J Nucl Med 2002;43:671-7.
56. Glaser M, Collingridge DR, Aboagye EO, et al. Iodine-124 labelled annexin A5 as a potential radiotracer to study apoptosis using positron emission tomography. Appl Radiat Isot 2003;58:55-62, doi:10.1016/S0969-8043(02)00239-7. (Pubitemid 35453947)
57. Keen HG, Dekker BA, Disley L, et al. Imaging apoptosis in vivo using 124I annexin A5 and PET. Nucl Med Biol 2005;32:395-402, doi:10.1016/j.nucmedbio. 2004.12.008. (Pubitemid 40692689)
58. Collingridge DR, Glaser M, Osman S, et al. In vitro selectivity, in vivo distribution and tumour uptake of annexin A5 radiolabelled with positron emitting radioisotopes. Br J Cancer 2003;89:1327-33, doi:10.1038/sj.bjc.6601262. (Pubitemid 37363425)
59. Dekker B, Keen H, Shaw D, et al. Functional comparison of annexin A5 analogues labelled indirectly and directly with iodine-Nucl Med Biol 2005;32:403-13, doi:10.1016/j.nucmedbio. 2005.02.002. (Pubitemid 40692690)
60. Dekker B, Keen H, Lyons S, et al. MBP-annexin A5 radiolabelled directly with iodine-124 can be used to image apoptosis in vivo using PET. Nucl Med Biol 2005;32:241-52, doi:10.1016/j.nucmedbio. 2004.11.006. (Pubitemid 40488381)
61. Zhao M, Beauregard DA, Loizou L, et al. Non-invasive detection of apoptosis using magnetic resonance imaging and a targeted contrast agent. Nat Med 2001;7:1241-4, doi:10.1038/nm1101-1241. (Pubitemid 33063780)
62. Schellenberger EA, Bogdanov A Jr, Högemann D, et al. Annexin A5-CLIO: a nanoparticle for detecting apoptosis by MRI. Mol Imaging 2002;1:102-7, doi:10.1162/153535002320162769.
63. Krishnan AS, Neves AA, de Backer MM, et al. Detection of cell death in tumours by using MR imaging and a gadolinium-based targeted contrast agent. Radiology 2008;246:854-62, doi:10.1148/ radiol.2463070471.
64. Neves AA, Krishnan AS, Kettunen MI, et al. A paramagnetic nanoprobe to detect tumour cell death using magnetic resonance imaging. Nano Lett 2007;7:1419-23, doi:10.1021/nl070126v. (Pubitemid 46834432)
65. Petrovsky A, Schellenberger E, Josephson L, et al. Near-infrared fluorescent imaging of tumour apoptosis. Cancer Res 2003;63: 1936-42. (Pubitemid 36460861)
66. Schellenberger EA, Bogdanov A Jr, Petrovsky A, et al. Optical imaging of apoptosis as a biomarker of tumour response to chemotherapy. Neoplasia 2003;5:187-92. (Pubitemid 36754049)
67. Ntziachristos V, Schellenberger EA, Ripoll J, et al. Visualization of antitumour treatment by means of fluorescence molecular tomography with an annexin A5-Cy5.5 conjugate. PNAS 2004; 101:12294-9, doi:10.1073/pnas.0401137101. (Pubitemid 39145437)
68. Choi HK, Yessayan D, Choi HJ, et al. Quantitative analysis of chemotherapeutic effects in tumours using in vivo staining and correlative histology. Cell Oncol 2005;27:183-90. (Pubitemid 41032903)
69. Edgington LE, Berger AB, Blum G, et al. Noninvasive optical imaging of apoptosis by caspase-targeted activity-based probes. Nat Med 2009;15:967-73, doi:10.1038/nm.1938.
70. Tunis AS, Czarnota GJ, Giles A, et al. Monitoring structural changes in cells with high-frequency ultrasound signal statistics. Ultras Med Biol 2005;8:1041-9, doi:10.1016/j.ultrasmedbio. 2005.04.020. (Pubitemid 41115846)
71. Czarnota GJ, Kolios MC, Abraham J, et al. Ultrasound imaging of apoptosis: high-resolution non-invasive monitoring of programmed cell death in vitro, in situ and in vivo. Br J Cancer 1999;81:520-7, doi:10.1038/sj.bjc. 6690724. (Pubitemid 29458808)
72. Banihashemi B, Vlad R, Debeljevic B, et al. Ultrasound imaging of apoptosis in tumour response: novel preclinical monitoring of photodynamic therapy effects. Cancer Res 2008;68:8590-6, doi:10.1158/0008-5472.CAN-08-0006.
73. Blankenberg FG, Katsikis PD, Storrs RW, et al. Quantitative analysis of apoptotic cell death using proton nuclear magnetic resonance spectroscopy. Blood 1997;89:3778-86. (Pubitemid 27227102)
74. Lehtimäki KK, Valonen PK, Griffin JL, et al. Metabolite changes in BT4C rat gliomas undergoing ganciclovir-thymidine kinase gene therapy-induced programmed cell death as studied by 1H MRS in vivo, ex vivo and in vitro. J Biol Chem 2003;278:45915-23, doi:10.1074/jbc.M306209200. (Pubitemid 37432737)
75. Schmitz JE, Kettunen MI, Hu DE, et al. 1H MRS-visible lipids accumulate during apoptosis of lymphoma cells in vitro and in vivo. Magn Reson Med 2005;54:43-50, doi:10.1002/mrm. 20529. (Pubitemid 40898395)
76. Valonen P, Griffith J, Vaisanen T, et al. Macromolecular and lipid resonances in apoptosis BT4C glioma cells in vitro and tumours in vivo. Proc Int Soc Magn Reson Med 2002;10:26-34.
77. Brindle KM. Detection of apoptosis in tumours using magnetic resonance imaging and spectroscopy. Adv Enzyme Regul 2002;42: 101-12, doi:10.1016/S0065- 2571(01)00025-5. (Pubitemid 35033532)
78. Brindle KM. Molecular imaging using magnetic resonance: new tools for the development of tumour therapy. Br J Radiol 2003;76 Spec No 2:S111-7, doi:10.1259/bjr/50577981. (Pubitemid 39530304)
79. Day SE, Kettunen M, Gallagher FA, et al. Detecting tumour response to treatment using hyperpolarized 13C magnetic resonance imaging and spectroscopy. Nat Med 2007;13:1382-7, doi:10.1038/nm1650. (Pubitemid 350073590)
80. Patterson DM, Padhani AR, Collins DJ. Technology insight: water diffusion MRI-a potential new biomarker of response to cancer therapy. Nat Clin Pract Oncol 2008;5:220-33, doi:10.1038/ ncponc1073. (Pubitemid 351493681)
81. Charles-Edwards EM, deSouza NM. Diffusion-weighted magnetic resonance imaging and its application to cancer. Can Imaging 2006;13:135-43, doi:10.1102/1470-7330.2006.0021.
82. Brauer M. In vivo monitoring of apoptosis. Prog Neuropsychopharmacol Biol Psychiatry 2003;27:323-31, doi:10.1016/S0278- 5846(03)00026-5. (Pubitemid 36355939)
83. Kim H, Morgan D, Zeng H, et al. Diffusion-weightedMR imaging to assess early therapy with novel apoptosis-inducing anti-DR5 antibody. Radiology 2008;248:844-51, doi:10.1148/radiol.2483071740.
84. Morse DL, Galons JP, Payne CM, et al. MRI-measured water mobility increases in response to chemotherapy via multiple celldeath mechanism. NMR Biomed 2007;20:602-14, doi:10.1002/ nbm.1127. (Pubitemid 47499995)
85. Kline RP, Wu EX, Petrylak DP, et al. Rapid in vivo monitoring of chemotherapeutic response using weighted sodium magnetic resonance imaging. Clin Cancer Res 2000;6:2146-56. (Pubitemid 30399179)
86. Sharma R, Katz JK. Taxotere chemosensitivity evaluation in mice prostate tumour: validation and diagnostic accuracy of quantitative measurement of tumour characteristics by MRI, PET, and histology of mice tumour. Technol Cancer Res Treat 2008;7: 175-86.
87. 1p. Magn Reson Med 2008;59:1311-9, doi:10.1002/mrm.21600. (Pubitemid 351813260)
88. Aloya R, Shirvan A, Grimberg H, et al. Molecular imaging of cell death in vivo by a novel small molecule probe. Apoptosis 2006;11: 2089-101, doi:10.1007/s10495-006-0282-7. (Pubitemid 44885386)
89. Grimberg H, Levin G, Shirvan A, et al. Monitoring of tumor response to chemotherapy in vivo by a novel small-molecule detector of apoptosis. Apoptosis 2009;14:257-67, doi:10.1007/ s10495-008-0293-7.
90. Reshef A, Shirvan A, Waterhouse RN, et al. Molecular imaging of neurovascular cell death in experimental cerebral stroke by PET. J Nucl Med 2008;40:1520-8, doi:10.2967/jnumed.107. 043919.
91. 18F-ML-10 for early assessment of response of brain metastase to radiotherapy. J Nucl Med 2009;50 Suppl:453.
92. Zeng W, Yao M-L, Townsend D, et al. Synthesis, biological evaluation and radiochemical labelling of a dansylhydrazone derivates as a potential imaging agent for apoptosis. Biorg Med Chem Lett 2008;18:3573-7, doi:10.1016/j.bmcl. 2008.05.002. (Pubitemid 351787557)
93. Laumonier C, Segers J, Laurent S, et al. A new peptide vector for molecular imaging of apoptosis identified by phage display technology. J Biomol Screen 2006;11:537-45, doi:10.1177/ 1087057106288220. (Pubitemid 44223005)
94. Thapa N, Kim S, So IS, et al. Discovery of a phosphatidylserine recognizing peptide and its utility in molecular imaging of tumour apoptosis. J Cell Mol Med 2008;12:1649-60, doi:10.1111/j.1582- 4934.2008.00305.x.