In vivo imaging of apoptosis

Cancer Biology and Therapy

Volumn 7, Issue 10, 2008, Pages 1525-1532

  Blankenberg, Francis G ^a,b  

^a LUCILE PACKARD CHILDREN S HOSPITAL   (United States)

^b NONE   (United States)

Author keywords

Apoptosis; Capase; Mitochondria; PET; Phosphatidylserine; Radionuclide; SPECT

Indexed keywords

1,4,7,10 TETRAAZACYCLODODECANE 1,4,7,10 TETRAACETIC ACID; BECLIN 1; CARRIER PROTEIN; CASPASE 10; CASPASE 3; CASPASE 6; CASPASE 7; CASPASE 8; CISPLATIN; COPPER 64; CYSTEINE DERIVATIVE; DEATH RECEPTOR 4; DEATH RECEPTOR 5; EPIRUBICIN; FLUORODEOXYGLUCOSE F 18; FLUOROURACIL; GALLIUM 68; GEFITINIB; IMATINIB; LIPOCORTIN 5; NICOTINAMIDE DERIVATIVE; PACLITAXEL; PENTETATE INDIUM IN 111; PERTECHNETIC ACID TC 99M; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BCL 2; PROTEIN BCL XL; SCRAMBLASE; TECHNETIUM 99M;

APOPTOSIS; AUTOPHAGY; BIOCHEMISTRY; BREAST CANCER; CANCER INHIBITION; CANCER MODEL; CANCER PATIENT; CELL DEATH; CELL STRESS; CLINICAL TRIAL; DRUG EFFICACY; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; GASTROINTESTINAL STROMAL TUMOR; HEAD AND NECK CANCER; HOMEOSTASIS; HUMAN; IN VIVO STUDY; ISOTOPE LABELING; LUNG NON SMALL CELL CANCER; LUNG SMALL CELL CANCER; LYMPHOMA; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; NONHODGKIN LYMPHOMA; NONHUMAN; POSITRON EMISSION TOMOGRAPHY; PROTEIN BINDING; PROTEIN FOLDING; REVIEW; SIGNAL TRANSDUCTION; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; SQUAMOUS CELL CARCINOMA; TREATMENT RESPONSE; TUMOR LOCALIZATION;

EID: 54349096337     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.7.10.6934     Document Type: Review

References (91)

1. Gavrieli Y, Sherman Y, Ben-Sasson S. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 1992; 119:493-501.
2. Koopman G, Reutelingsperger CPM, Kuijten GAM, Keehnen RMJ, Pals ST, van Oers MHJ. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 1994; 84:1415-20.
3. Chan A, Reiter R, Wiese S, Fertig G, Gold R. Plasma membrane phospholipid asymmetry precedes DNA fragmentation in different apoptotic cell models. Histochem Cell Biol 1998; 110:553-8.
4. Boersma AWM, Kees N, Oostrum RG, Stoter G. Quantification of apoptotic cells with fluorescein isothiocynate-labeled annexin V in Chineses hamster overy cell cultures treated with cisplatin. Cytometry 1996; 24:123-30.
5. Steller H. Mechanisms and genes of cellular suicide. Science 1995; 267:1445-9.
6. Orrenius S. Apoptosis: molecular mechanisms and implications for human disease. J Intern Med 1995; 237:529-36.
7. Wu J. Apoptosis and angiogenesis: two promising tumor markers in breast cancer (review). Anticancer Res 1996; 16:2233-9.
8. Olson M, Kornbluth S. Mitochondria in apoptosis and human disease. Curr Mol Med 2001; 1:91-122.
9. Ameisen JC. On the origin, evolution and nature of programmed cell death: a timeline of four billion years. Cell Death Differ 2002; 9:367-93.
10. Martin SJ, Reutelingsperger CPM, McGahon AJ. Early redistribution of plasma membrane phosphatidylserine in a general feature of apoptosis regardless of the initiating stimulus: Inhibition by overexpression of Bcl-2 and Abl. J Exp Med 1995; 182:1545-56.
11. Huerta S, Goulet EJ, Huerta-Yepez S, Livingston EH. Screening and Detection of Apoptosis. Journal of Surgical Research 2007; 139:143-56.
12. Sperandio S, de Belle I, Bredesen DE. An alternative, nonapoptotic form of programmed cell death. Proc Natl Acad Sci USA 2000; 97:14376-81.
13. Green DR, Kroemer G. The pathophysiology of mitochondrial cell death. Science 2004; 305:626-9.
14. th Edition, Eds. Lichtman MA, Beutler E, Kipps TJ, Seligsohn U, Kaushansky K, Prcha JT. McGraw-Hill Companies 2005; 11:125-30.
15. Zwaal RFA, Schroit AJ. Pathophysiologic Implications of Membrane Phospholipid Asymmetry in Blood Cells. Blood 1997; 89:1121-32.
16. Zwaal RFA, Comfurius P, Bevers EM. Surface exposure of phosphatidylserine in pathological cells. CMLS, Cell Mol Life Sci 2005; 62:971-88.
17. Tait JF, Gibson D. Measurements of membrane phospholipid asymmetry in normal and sickle-cell erthyrocytes by means of annexin V binding. J Lab Clin Med 1994; 123:741-8.
18. van Heerde WL, de Groot PG, Reutelingsperger CPM. The complexity of the phospholipid binding protein annexin V. Thrombosis and Haemostasis 1995; 73:172-9.
19. Wood BL, Gibson DF, Tait JF. Increased phosphatidylserine exposure in sickle cell disease: Flow cytometric measurement and clinical associations. Blood 1996; 88:1873-80.
20. Balasubramanian K, Mirnikjoo B, Schroit AJ. Regulated Externalization of Phosphatidylserine at the Cell Surface: Implication for Apoptosis. The Journal of Biological Chemistry 2007; 282:18357-64.
21. Elliott JI, Sardini A, Cooper JC, Alexander DR, Davanture S, Chimini G, Higgins CF. Phosphatidylserine exposure in B lymphocytes: a role for lipid packing. Blood 2006; 108:1611-7.
22. Strauss HW, Narula J, Blankenberg FG. Radioimaging to identify myocardial cell death and probably injury. Lancet 2000; 356:180-1.
23. Lejeune M, Ferster A, Cantinieaux B, Sariban E. Prolonged but reversible neutrophil dyfunctions differentially sensitive to granulocyte colony-stimulating factor in children with acute lymphoblastic leukemia. Br J Haematol 1998; 102:1284-91.
24. Hammill AK, Uhr JW, Scheuermann RH. Annexin V staining due to loss of membrane asymmetry can be reversible and precede commitment to apoptotic death. Exp Cell Res 1999; 251:16-21.
25. Furukawa Y, Bangham CRM, Taylor GP, Weber JN, Osame M. Frequent reversible membrane damage in peripheral blood B cells in human T cell lymphotrophic virus type I (HTLV-I)-associated myelopathy/tropical spastic paraparesis (HAM/TSP). Clinical & Experimental Immunology 2000; 120:307-16.
26. Martin S, Pombo I, Poncet P, David B, Arock M, Blank U. Immunologic stimulation of mast cells leads to the reversible exposure of phosphatidylserine in the absence of apoptosis. Int Arch Allergy Immunol 2000; 123:249-58.
27. Lin SH, Vincent A, Shaw T, Maynard KI, Maiese K. Prevention of nitric oxide-induced neuronal injury through the modulation of independent pathways of programmed cell death. J Cereb Blood Flow Metab 2000; 20:1380-91.
28. Geske FJ, Lieberman R, Strange R, Gerschenson LE. Early stages of p53-induced apoptosis are reversible. Cell Death Differ 2001; 8:182-91.
29. Maiese K, Vincent AM. Membrane asymmetry and DNA degradation: functionally distinct determinants of neuronal programmed cell death. J Neurosci Res 2000; 59:568-80.
30. Yang MY, Chuang H, Chen RF, Yang KD. Reversible phosphatidylserine expression on blood granulocytes related to membrane perturbation but not DNA strand breaks. J Leukoc Biol 2002; 71:231-7.
31. Egger L, Madden DT, Rheme C, Rao RV, Bredesen DE. Endoplasmic reticulum stress-induced cell death mediated by the proteasome. Cell Death and Differentiation 2007; 14:1172-80.
32. Corsten MF, Hofstra L, Narula J, Reutelingsperger CP. 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.
33. Verheij M. Clinical biomarkers and imaging for radiotherapy-induced cell death. Cancer Metastasis Rev 2008; [Epub ahead of print].
34. Fink SL, Cookson BT. Apoptosis, pyroptosis and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun 2005; 73:1907-16.
35. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008; 132:27-42.
36. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 2007; 8:741-52.
37. Aguilar-Quesada R, Muñoz-Gámez JA, Martín-Oliva D, Peralta-Leal A, Quiles-Pérez R, Rodríguez-Vargas JM, Ruiz de Almodóvar M, Conde C, Ruiz-Extremera A, Oliver FJ. Modulation of Transcription by PARP-1: Consequences in Carcinogenesis and Inflammation. Current Medicinal Chemistry 2007; 14:1179-87.
38. Koopman G, Reutelingsperger CP, Kuijten GA, Keehnen RM, Pals ST, van Oers MH. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 1994; 84:1415-20.
39. Boersma HH, Kietselaer BL, Stolk LM, Bennaghmouch A, Hofstra L, Narula J, Heidendal GA, Reutelingsperger CP. Past, present and future of annexin A5: from protein discovery to clinical applications. J Nucl Med 2005; 46:2035-50.
40. Meers P, Mealy T. Calcium-dependent annexin V binding to phospholipids: stoichiometry, specificity, and the role of negative charge. Biochemistry 1993; 32:11711-21.
41. Kenis H, van Genderen H, Bennaghmouch A, Rinia HA, Frederik P, Narula J, Hofstra L, Reutelingsperger CPM. Cell Surface-expressed Phosphatidylserine and Annexin A5. Open a Novel Portal of Cell Entry. The Journal of Biological Chemistry 2004; 279:52623-9.
42. Lahorte CMM, Vanderheyden J-L, Steinmetz N, Van de Wiele C, Dierckx RA, Slegers G. Apoptosis-detecting radioligands: current state of the art and future perspectives. Eur J Nucl Med Mol Imaging 2004; 31:887-919.
43. Munoz LE, Franz S, Pausch F, Funrohr B, Sheriff A, Vogt B, Kern PM, Baum W, Stach C, von Laer D, Brachvogel B, Poschl E, Herrmann M, Gaipl US. The influence on the immunomodulatory effects of dying and dead cells of Annexin V. Journal of Leukocyte Biology 2007; 81:6-14.
44. Munoz LE, Frey B, Pausch F, Baum W, Mueller RB, Brachvogel B, Poschl E, Rödel F, von der Mark K, Herrmann M, Gaipl US. The Role of Annexin A5 in the Modulation of the Immune Response Against Dying and Dead Cells. Current Medicinal Chemistry 2007; 14:271-7.
45. 99mTc-annexin A5. Br J Radiol 2003; 76:553-60.
46. Belhocine T, Steinmetz N, Hustinx R, Bartsch P, Jerusalem G, Seidel L, Rigo P, Green A. Increased uptake of the apoptosis-imaging agent (99m)Tc recombinant human Annexin V in human tumors after one course of chemotherapy as a predictor of tumor response and patient prognosis. Clin Cancer Res 2002; 8:2766-74.
47. Blankenberg F. To scan or not to scan, it is a question of timing: technetium-99m-annexin V radionuclide imaging assessment of treatment efficacy after one course of chemotherapy. Clin Cancer Res 2002; 8:2757-8.
48. 99mTc-HYNIC-Annexin V, a Novel Human Recombinant Annexin V for Human Application. J Nucl Med 2003; 44:947-52.
49. Van den Brande JM, Koehler TC, Zelinkova Z, Bennink RJ, te Velde AA, ten Cate FJ, van Deventer SJ, Peppelenbosch MP, Hommes DW. Prediction of antitumour necrosis factor clinical efficacy by real-time visualisation of apoptosis in patients with Crohn's disease. Gut 2007; 56:509-17.
50. Blankenberg FG. Molecular imaging: The latest generation of contrast agents and tissue characterization techniques. J Cell Biochem 2003; 90:443-53.
51. Haas RL, de Jong D, Valdes Olmos RA, Hoefnagel CA, van den Heuvel I, Zerp SF, Bartelink H, Verheij M. In vivo imaging of radiation-induced apoptosis in follicular lymphoma patients. Int J Radiat Oncol Biol Phys 2004; 59:782-7.
52. 99mTc-HYNIC annexin-V imaging in head and neck carcinoma. Cancer Biother Radiopharm 2004; 19:205-10.
53. 99mTc-Annexin V scintigraphy: visual analysis in relation to treatment response. Radiother Oncol 2004; 72:333-9.
54. 99mTc-hydrazinonicotinamide-annexin V imaging for predicting response to chemotherapy. J Nucl Med 2006; 47:1813-8.
55. 99mTc Hynic-rh-annexin V scintigraphy during platinum-based chemotherapy in advanced lung cancer. J Clin Oncol 2007; 25:2534-9.
56. 99mTc-HYNIC-rh-annexin-V scintigraphy: visual and quantitative evaluation of early treatment-induced apoptosis to predict treatment outcome. Nucl Med Commun 2008; 29:39-44.
57. Tait JF, Brown DS, Gibson DF, Blankenberg FG, Strauss HW. Development and characterization of annexin V mutants with endogenous chelation sites for (99m)Tc. Bioconjug Chem 2000; 11:918-25.
58. Jin M, Smith C, Hsieh HY, Gibson DF, Tait JF. Essential role of B-helix calcium binding sites in annexin V-membrane binding. J Biol Chem 2004; 279:40351-7.
59. 99mTc-annexin V. J Nucl Med 2005; 46:807-15.
60. Tait JF, Smith C, Levashova Z, Patel B, Blankenberg FG, Vanderheyden JL. "Improved detection of cell death in vivo with annexin V radiolabeled by site-specific methods". J Nucl Med 2006; 47:1546-53.
61. 99mTc-labeled annexin V fragments: a potential SPECT radiopharmaceutical for imaging cell death. Nucl Med Biol 2006; 33:635-43.
62. 99mTc-MAG3-annexin V: influence of the chelate on in vitro and in vivo properties in mice. Nucl Med Biol 2006; 33:135-44.
63. 111In-labeled annexin V. J Nucl Med 2004; 45:108-15.
64. Van den Eijnde SM, Boshart L, Reutelingsperger CPM, De Zeeuw CI, Vermeij-Keers C. Phosphatidylserine plasma membrane asymetry in vivo: a pancellular phenomenon which alters during apoptosis. Cell Death Differ 1997; 4:311-6.
65. 99mTc-annexin V and its biologic evaluation for in vivo imaging of apoptosis after photodynamic therapy. J Nucl Med 2003; 44:650-6.
66. Grierson JR, Yagle KJ, Eary JF, Tait JF, Gibson DF, Lewellen B, Link JM, Krohn KA. Production of [F-18]fluoroannexin for imaging apoptosis with PET. Bioconjug Chem 2004; 15:373-9.
67. 18F-labelled annexin V: a PET tracer for apoptosis imaging. Eur J Nucl Med Mol Imaging 2004; 31:469-74.
68. Li X, Link JM, Stekhova S, Yagle KJ, Smith C, Krohn KA, et al. Site-specific labeling of annexin V with F-18 for apoptosis imaging. Bioconjug Chem 2008; In press.
69. Thapa N, Kim S, So IS, Lee BH, Kwon IC, Choi K, Kim IS. Discovery of a Phosphatidylserine Recognizing Peptide and Its Utility in Molecular Imaging of Tumor Apoptosis. J Cell Mol Med 2008; [Epub ahead of print] PMID: 18363834 [PubMed - as supplied by publisher].
70. 99mTc-labeled C2A domain of synaptotagmin I as a target specific molecular probe for noninvasive imaging of acute myocardial infarction. J Nucl Med 2006; 47:1367-74.
71. Zhao M, Beauregard DA, Loizou L, Davletov B, Brindle KM. Non-invasive detection of apoptosis using magnetic resonance imaging and a targeted contrast agent. Nat Med 2001; 7:1241-4.
72. Jung HI, Kettunen MI, Davletov B, Brindle KM. Detection of apoptosis using the C2A domain of synaptotagmin I. Bioconjug Chem 2004; 15:983-7.
73. Krishnan AS, Neves AA, de Backer MM, De-En Hu, Davletov B, Kettunen MI, Brindle KM. Detection of Cell Death in Tumors by Using MR Imaging and a Gadolinium-based Targeted Contrast Agent. Radiology 2008; 246:854-62.
74. Hanshaw RG, Lakshmi C, Lambert TN, Johnson JR, Smith BD. Fluorescent detection of apoptotic cells by using zinc coordination complexes with a selective affinity for membrane surfaces enriched with phosphatidylserine. Chem Bio Chem 2005; 6:2214-20.
75. Bose S, Tuunainen I, Parry M, Medina OP, Mancini G, Kinnunen PK. Binding of cationic liposomes to apoptotic cells. Analy Biochem 2004; 331:385-94.
76. Shao R, Xiong C, Wen X, Gelovani JG, Li C. Targeting phosphatidylserine on apoptotic cells with phages and peptides selected from a bacteriophage display library. Mol Imaging 2007; 6:417-26.
77. 18F-labeled isatin analog for imaging caspase-3 activation in apoptosis. Bioorganic & Medicinal Chemistry Letters 2006; 16:5041-6.
78. Faust A, Wagner S, Law MP, Hermann S, Schnöckel U, Keul P, Schober O, Schäfers M, Levkau B, Kopka K. The nonpeptidyl caspase binding radioligand (S)-1-(4-(2-[18F] 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.
79. Rosado JA, Lopez JJ, Gomez-Arteta E, Redondo PC, Slaido GM, Pariente JA. Early Caspase-3 Activation Independent of Apoptosis Is Required for Cellular Function. Journal of Cellular Physiology 2006; 209:142-52.
80. Spires-Jones TL, de Calignon A, Matsui T, Zehr C, Pitstick R, Wu HY, Osetek JD, Jones PB, Bacskai BJ, Feany MB, Carlson GA, Ashe KH, Lewis J, Hyman BT. In vivo imaging reveals dissociation between caspase activation and acute neuronal death in tangle-bearing neurons. J Neurosci 2008; 28:862-7.
81. Reshef A, Shirvan A, Grimberga H, Levin G, Cohena A, Mayka A, Kidron D, Djaldetti R, Melamed E, Ziv I. Novel molecular imaging of cell death in experimental cerebral stroke. Brain Research 2007; 144:156-64.
82. Damianovich M, Ziv I, Heyman SN, Rosen S, Shina A, Kidron D, Aloya T, Grimberg H, Levin G, Reshef A, Bentolila A, Cohen A, Shirvan A. ApoSense: a novel technology for functional molecular imaging of cell death in models of acute renal tubular necrosis. Eur J Nucl Med Mol Imaging 2006; 33:281-91.
83. Aloya R, Shirvan A, Grimberg H, Reshef A, Levin G, Kidron D, Cohen A, Ziv I. Molecular imaging of cell death in vivo by a novel small molecule probe. Apoptosis 2006; 11:2089-101.
84. Cohen A, Ziv I, Aloya T, Levin G, Kidron D, Grimberg H, Reshef A, Shirvan A. Monitoring of Chemotherapy-Induced Cell Death in Melanoma Tumors by N,N′-Didansyl-L-cystine. Technology in Cancer Research & Treatment 2007; 6:221-33.
85. 18F-FDG, and Histologic Evaluation. J Nucl Med 2005; 46:794-9.
86. 18F-FDG PET/CT and Apoptosis Induced by Neoadjuvant Chemotherapy in Breast Cancer. Cancer Biology & Therapy 2007; 6:1442-8.
87. 18F]2-Fluoro-2-deoxy-D- glucose incorporation by AGS gastric adenocarcinoma cells in vitro during response to epirubicin, cisplatin and 5-fluorouracil. British Journal of Cancer 2007; 97:902-9.
88. Trent JC, Ramdas L, Dupart J, Hunt K, Macapinlac H, Taylor E, Hu L, Salvado A, Abbruzzese JL, Pollock R, Benjamin RS, Zhang W. Early Effects of Imatinib Mesylate on the Expression of Insulin-Like Growth Factor Binding Protein-3 and Positron Emission Tomography in Patients With Gastrointestinal Stromal Tumor. Cancer 2006; 107:1898-908.
89. Su H, Bodenstein C, Dumont RA, Seimbille Y, Dubinett S, Phelps ME, Herschman H, Czernin J, Weber W. Monitoring Tumor Glucose Utilization by Positron Emission Tomography for the Prediction of Treatment Response to Epidermal Growth Factor Receptor Kinase Inhibitors. Clin Cancer Res 2006; 12:5659-67.
90. Haberkorn U, Bellemann ME, Brix G, et al. Apoptosis and changes in glucose transport early after treatment of Morris hepatoma with gemcitabine. Eur J Nucl Med 2001; 28:418-25.
91. Mortimer JE, Dehdashti F, Siegel BA, et al. Metabolic flare: indicator of hormone responsiveness in advanced breast cancer. J Clin Oncol 2001; 19:2797-803.