89Zr, a radiometal nuclide with high potential for molecular imaging with pet: Chemistry, applications and remaining challenges

Molecules

Volumn 18, Issue 6, 2013, Pages 6469-6490

  Fischer, Gabriel ^a,b   Seibold, Uwe ^a   Schirrmacher, Ralf ^c   Wängler, Björn ^a   Wängler, Carmen ^a,b  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

89Zr; Biomolecules; Cerenkov luminescence imaging; Desferrioxamine B; Dosimetry; Positron emission tomography (PET)

Indexed keywords

DEFEROXAMINE; RADIOPHARMACEUTICAL AGENT; ZIRCONIUM; DIAGNOSTIC AGENT;

CHEMISTRY; DIAGNOSTIC USE; ISOTOPE LABELING; MOLECULAR IMAGING; POSITRON EMISSION TOMOGRAPHY; REVIEW;

DEFEROXAMINE; ISOTOPE LABELING; MOLECULAR IMAGING; POSITRON-EMISSION TOMOGRAPHY; RADIOPHARMACEUTICALS; ZIRCONIUM;

EID: 84879679457     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules18066469     Document Type: Review

References (101)

1. Zhang, Y.; Hong, H.; Cai, W. PET tracers based on Zirconium-89. Curr. Radiopharm. 2011, 4, 131-139.
2. Severin, G.W.; Engle, J.W.; Barnhart, T.E.; Nickles, R.J. Zr-89 Radiochemistry for positron emission tomography. Med. Chem. 2011, 7, 389-394.
3. Nayak, T.K.; Brechbiel, M.W. Radioimmunoimaging with longer-lived positron-emitting radionuclides: Potentials and challenges. Bioconjug. Chem. 2009, 20, 825-841.
4. Deri, M.A.; Zeglis, B.M.; Francesconi, L.C.; Lewis, J.S. PET imaging with Zr-89: From radiochemistry to the clinic. Nucl. Med. Biol. 2013, 40, 3-14.
5. Holland, J.P.; Sheh, Y.C.; Lewis, J.S. Standardized methods for the production of high specific-activity zirconium-89. Nucl. Med. Biol. 2009, 36, 729-739.
6. Baillie, A.D.; Ledingham, K.W.D.; Lynch, J.G.; Campbell, M. Electron capture to positron emission ratios in the allowed decay of 89Zr. J. Phys. G Nucl. Phys. 1979, 5, 1433-1444.
7. Lubberink, M.; Herzog, H. Quantitative imaging of I-124 and Y-86 with PET. Eur. J. Nucl. Med. Mol. I 2011, 38, 10-18.
8. Verel, I.; Visser, G.W.; Boellaard, R.; Stigter-van Walsum, M.; Snow, G.; van Dongen, G.A. 89Zr immuno-PET: Comprehensive procedures for the production of 89Zr-labeled monoclonal antibodies. J. Nucl. Med. 2003, 44, 1271-1281.
9. Meijs, W.E.; Herscheid, J.D.M.; Haisma, H.J.; Wijbrandts, R.; Vanlangevelde, F.; Vanleuffen, P.J.; Mooy, R.; Pinedo, H.M. Production of highly pure no-carrier added Zr-89 for the labeling of antibodies with a positron emitter. Appl. Radiat. Isotopes 1994, 45, 1143-1147.
10. Taghilo, M.; Kakavand, T.; Rajabifar, S.; Sarabadani, P. Cyclotron production of 89Zr: A potent radionuclide for positron emission tomography. Int. J. Phys. Sci. 2012, 7, 1321-1325.
11. Dejesus, O.T.; Nickles, R.J. Production and Purification of Zr-89, a Potential Pet Antibody Label. Appl. Radiat. Isotopes 1990, 41, 789-790.
12. Kasbollah, A.; Eu, P.; Cowell, S.; Deb, P. Review on Production of 89Zr in a Medical Cyclotron for PET Radiopharmaceuticals. J. Nucl. Med. Technol. 2013, 41, 35-41.
13. Sadeghi, M.; Enferadi, M.; Bakhtiari, M. Accelerator production of the positron emitter zirconium-89. Ann. Nucl. Energy 2012, 41, 97-103.
14. Lobo, E.D.; Hansen, R.J.; Balthasar, J.P. Antibody pharmacokinetics and pharmacodynamics. J. Pharm. Sci. 2004, 93, 2645-2668.
15. Imai, K.; Takaoka, A. Comparing antibody and small-molecule therapies for cancer. Nat. Rev. Cancer 2006, 6, 714-727.
16. Borjesson, P.K.; Jauw, Y.W.; de Bree, R.; Roos, J.C.; Castelijns, J.A.; Leemans, C.R.; van Dongen, G.A.; Boellaard, R. Radiation dosimetry of 89Zr-labeled chimeric monoclonal antibody U36 as used for immuno-PET in head and neck cancer patients. J. Nucl. Med. 2009, 50, 1828-1836.
17. 18F-FDG PET/CT examinations. J. Nucl. Med. 2005, 46, 608-613.
18. van Dongen, G.A.M.S.; Visser, G.W.M.; Hooge, M.N.L.D.; De Vries, E.G.; Perk, L.R. Immuno-PET: A navigator in monoclonal antibody development and applications. Oncologist 2007, 12, 1379-1389.
19. Verel, I.; Visser, G.W.; Boellaard, R.; Boerman, O.C.; van Eerd, J.; Snow, G.B.; Lammertsma, A.A.; van Dongen, G.A. Quantitative 89Zr immuno-PET for in vivo scouting of 90Y-labeled monoclonal antibodies in xenograft-bearing nude mice. J. Nucl. Med. 2003, 44, 1663-1670.
20. Herzog, H.; Tellmann, L.; Qaim, S.M.; Spellerberg, S.; Schmid, A.; Coenen, H.H. PET quantitation and imaging of the non-pure positronemitting iodine isotope I-124. Appl. Radiat. Isotopes 2002, 56, 673-679.
21. Thorek, D.L.J.; Robertson, R.; Bacchus, W.A.; Hahn, J.; Rothberg, J.; Beattie, B.J.; Grimm, J. Cerenkov imaging-a new modality for molecular imaging. Am. J. Nucl. Med. Mol. Imaging 2012, 2, 163-173.
22. Ruggiero, A.; Holland, J.P.; Lewis, J.S.; Grimm, J. Cerenkov Luminescence Imaging of Medical Isotopes. J. Nucl. Med. 2010, 51, 1123-1130.
23. Holland, J.P.; Normand, G.; Ruggiero, A.; Lewis, J.S.; Grimm, J. Intraoperative Imaging of Positron Emission Tomographic Radiotracers Using Cerenkov Luminescence Emissions. Mol. Imaging 2011, 10, 177-186.
24. Nagengast, W.B.; de Vries, E.G.; Hospers, G.A.; Mulder, N.H.; de Jong, J.R.; Hollema, H.; Brouwers, A.H.; van Dongen, G.A.; Perk, L.R.; Lub-de Hooge, M.N. In vivo VEGF imaging with radiolabeled bevacizumab in a human ovarian tumor xenograft. J. Nucl. Med. 2007, 48, 1313-1319.
25. Munnink, T.H.O.; de Korte, M.A.; Nagengast, W.B.; Timmer-Bosscha, H.; Schroder, C.P.; de Jong, J.R.; van Dongen, G.A.M.S.; Jensen, M.R.; Quadt, C.; Lub-de Hooge, M.N.; et al. Zr-89-trastuzumab PET visualises HER2 downregulation by the HSP90 inhibitor NVP-AUY922 in a human tumour xenograft. Eur. J. Cancer 2010, 46, 678-684.
26. Dijkers, E.C.F.; Kosterink, J.G.W.; Rademaker, A.P.; Perk, L.R.; van Dongen, G.A.M.S.; Bart, J.; de Jong, J.R.; de Vries, E.G.E.; Lub-de Hooge, M.N. Development and Characterization of Clinical-Grade Zr-89-Trastuzumab for HER2/neu ImmunoPET Imaging. J. Nucl. Med. 2009, 50, 974-981.
27. Chang, A.J.; DeSilva, R.; Jain, S.; Lears, K.; Rogers, B.; Lapi, S. 89Zr-radiolabeled trastuzumab imaging in orthotopic and metastatic breast tumors. Pharmaceuticals 2012, 5, 79-93.
28. Borjesson, P.K.; Jauw, Y.W.; Boellaard, R.; de Bree, R.; Comans, E.F.; Roos, J.C.; Castelijns, J.A.; Vosjan, M.J.; Kummer, J.A.; Leemans, C.R.; et al. Performance of immuno-positron emission tomography with zirconium-89-labeled chimeric monoclonal antibody U36 in the detection of lymph node metastases in head and neck cancer patients. Clin. Cancer Res. 2006, 12, 2133-2140.
29. Aerts, H.J.W.L.; Dubois, L.; Perk, L.; Vermaelen, P.; van Dongen, G.A.M.S.; Wouters, B.G.; Lambin, P. Disparity Between In Vivo EGFR Expression and (89)Zr-Labeled Cetuximab Uptake Assessed with PET. J. Nucl. Med. 2009, 50, 123-131.
30. Jacobson, O.; Zhu, L.; Niu, G.; Weiss, I.D.; Szajek, L.P.; Ma, Y.; Sun, X.; Yan, Y.; Kiesewetter, D.O.; Liu, S.; et al. MicroPET imaging of integrin alphavbeta3 expressing tumors using 89Zr-RGD peptides. Mol. Imaging Biol. 2011, 13, 1224-1233.
31. Keliher, E.J.; Yoo, J.; Nahrendorf, M.; Lewis, J.S.; Marinelli, B.; Newton, A.; Pittet, M.J.; Weissleder, R. Zr-89-Labeled Dextran Nanoparticles Allow in vivo Macrophage Imaging. Bioconjug. Chem. 2011, 22, 2383-2389.
32. Avila-Rodriguez, M.A.; Selwyn, R.G.; Hampel, J.A.; Thornadsen, B.R.; DeJesus, O.T.; Converse, A.K.; Nickles, R.J. Positron-emitting resin microspheres as surrogates of Y-90 SIR-Spheres: A radiolabeling and stability study. Nucl. Med. Biol. 2007, 34, 585-590.
33. Ruggiero, A.; Villa, C.H.; Holland, J.; Sprinkle, S.R.; May, C.; Lewis, J.S.; Scheinberg, D.A.; McDevitt, M.R. Imaging and treating tumor vasculature with targeted radiolabeled carbon nanotubes. Int. J. Nanomed. 2010, 5, 783-802.
34. Abou, D.S.; Thorek, D.L.; Ramos, N.N.; Pinkse, M.W.; Wolterbeek, H.T.; Carlin, S.D.; Beattie, B.J.; Lewis, J.S. (89)Zr-Labeled Paramagnetic Octreotide-Liposomes for PET-MR Imaging of Cancer. Pharm. Res. 2013, 30, 878-888.
35. Evans, M.J.; Holland, J.P.; Rice, S.L.; Doran, M.G.; Cheal, S.M.; Campos, C.; Carlin, S.D.; Mellinghoff, I.K.; Sawyers, C.L.; Lewis, J.S. Imaging Tumor Burden in the Brain with Zr-89-Transferrin. J. Nucl. Med. 2013, 54, 90-95.
36. Holland, J.P.; Evans, M.J.; Rice, S.L.; Wongvipat, J.; Sawyers, C.L.; Lewis, J.S. Annotating MYC status with Zr-89-transferrin imaging. Nat. Med. 2012, 18, 1586-1597.
37. Meijs, W.E.; Haisma, H.J.; VanderSchors, R.; Wijbrandts, R.; VandenOever, K.; Klok, R.P.; Pinedo, H.M.; Herscheid, J.D.M. A facile method for the labeling of proteins with zirconium isotopes. Nucl. Med. Biol. 1996, 23, 439-448.
38. Sotogaku, N.; Endo, K.; Hirunuma, R.; Enomoto, S.; Ambe, S.; Ambe, F. Biochemical reactions of various trace elements with blood components and transport proteins. J. Radioanal. Nucl. Ch. 1999, 239, 429-432.
39. Abou, D.S.; Ku, T.; Smith-Jones, P.M. In vivo biodistribution and accumulation of Zr-89 in mice. Nucl. Med. Biol. 2011, 38, 675-681.
40. Amano, R.; Enomoto, S.; Nobuta, M.; Sakamoto, M.; Tsujioka, R.; Ambe, F. Bone uptake of vanadium in mice: Simultaneous tracing of V, Se, Sr, Y, Zr, Ru and Rh using a radioactive multitracer. J. Trace Elem. Med. Biol. 1996, 10, 145-148.
41. Meijs, W.E.; Herscheid, J.D.M.; Haisma, H.J.; Pinedo, H.M. Evaluation of Desferal as a Bifunctional Chelating Agent for Labeling Antibodies with Zr-89. Appl. Radiat. Isotopes 1992, 43, 1443-1447.
42. Wadas, T.J.; Wong, E.H.; Weisman, G.R.; Anderson, C.J. Coordinating radiometals of copper, Gallium, Indium, Yttrium, and zirconium for PET and SPECT imaging of disease. Chem. Rev. 2010, 110, 2858-2902.
43. Kiss, T.; Farkas, E. Metal-binding ability of desferrioxamine B. J. Inclus. Phenom. Mol. 1998, 32, 385-403.
44. Hernlem, B.J.; Vane, L.M.; Sayles, G.D. Stability constants for complexes of the siderophore desferrioxamine B with selected heavy metal cations. Inorg. Chim. Acta 1996, 244, 179-184.
45. Baroncelli, F.; Grossi, G. The complexing power of hydroxamic acids and its effect on the behaviour of organic extractants in the reprocessing of irradiated fuels-I the complexes between benzohydroxamic acid and zirconium, iron (III) and uranium (VI). J. Inorg. Nucl. Chem. 1965, 27, 1085-1092.
46. Holland, J.P.; Divilov, V.; Bander, N.H.; Smith-Jones, P.M.; Larson, S.M.; Lewis, J.S. Zr-89-DFO-J591 for ImmunoPET of Prostate-Specific Membrane Antigen Expression In Vivo. J. Nucl. Med. 2010, 51, 1293-1300.
47. Perk, L.R.; Vosjan, M.J.W.D.; Visser, G.W.M.; Budde, M.; Jurek, P.; Kiefer, G.E.; van Dongen, G.A.M.S. p-Isothiocyanatobenzyl-desferrioxamine: A new bifunctional chelate for facile radiolabeling of monoclonal antibodies with zirconium-89 for immuno-PET imaging. Eur. J. Nucl. Med. Mol. I 2010, 37, 250-259.
48. Walther, M.; Gebhardt, P.; Grosse-Gehling, P.; Wurbach, L.; Irmler, I.; Preusche, S.; Khalid, M.; Opfermann, T.; Kamradt, T.; Steinbach, J.; et al. Implementation of Zr-89 production and in vivo imaging of B-cells in mice with Zr-89-labeled anti-B-cell antibodies by small animal PET/CT. Appl. Radiat. Isotopes 2011, 69, 852-857.
49. Vosjan, M.J.; Perk, L.R.; Visser, G.W.; Budde, M.; Jurek, P.; Kiefer, G.E.; van Dongen, G.A. Conjugation and radiolabeling of monoclonal antibodies with zirconium-89 for PET imaging using the bifunctional chelate p-isothiocyanatobenzyl-desferrioxamine. Nat. Protoc. 2010, 5, 739-743.
50. Holland, J.P.; Caldas-Lopes, E.; Divilov, V.; Longo, V.A.; Taldone, T.; Zatorska, D.; Chiosis, G.; Lewis, J.S. Measuring the Pharmacodynamic Effects of a Novel Hsp90 Inhibitor on HER2/neu Expression in Mice Using Zr-89-DFO-Trastuzumab. PLoS One 2010, 5, e8859.
51. Ruggiero, A.; Holland, J.P.; Hudolin, T.; Shenker, L.; Koulova, A.; Bander, N.H.; Lewis, J.S.; Grimm, J. Targeting the Internal Epitope of Prostate-Specific Membrane Antigen with Zr-89-7E11 Immuno-PET. J. Nucl. Med. 2011, 52, 1608-1615.
52. Munnink, T.H.O.; Arjaans, M.E.A.; Timmer-Bosscha, H.; Schroder, C.P.; Hesselink, J.W.; Vedelaar, S.R.; Walenkamp, A.M.E.; Reiss, M.; Gregory, R.C.; Lub-de Hooge, M.N.; et al. PET with the Zr-89-Labeled Transforming Growth Factor-beta Antibody Fresolimumab in Tumor Models. J. Nucl. Med. 2011, 52, 2001-2008.
53. Perk, L.R.; Visser, O.J.; Walsum, M.S.V.; Vosjan, M.J.W.D.; Visser, G.W.M.; Zijlstra, J.M.; Huijgens, P.C.; van Dongen, G.A.M.S. Preparation and evaluation of Zr-89-Zevalin for monitoring of Y-90-Zevalin biodistribution with positron emission tomography. Eur. J. Nucl. Med. Mol. I 2006, 33, 1337-1345.
54. Meijs, W.E.; Haisma, H.J.; Klok, R.P.; vanGog, F.B.; Kievit, E.; Pinedo, H.M.; Herscheid, J.D.M. Zirconium-labeled monoclonal antibodies and their distribution in tumor-bearing nude mice. J. Nucl. Med. 1997, 38, 112-118.
55. Tinianow, J.N.; Gill, H.S.; Ogasawara, A.; Flores, J.E.; Vanderbilt, A.N.; Luis, E.; Vandlen, R.; Darwish, M.; Junutula, J.R.; Williams, S.P.; et al. Site-specifically 89Zr-labeled monoclonal antibodies for ImmunoPET. Nucl. Med. Biol. 2010, 37, 289-297.
56. Zeglis, B.M.; Mohindra, P.; Weissmann, G.I.; Divilov, V.; Hilderbrand, S.A.; Weissleder, R.; Lewis, J.S. Modular strategy for the construction of radiometalated antibodies for positron emission tomography based on inverse electron demand Diels-Alder click chemistry. Bioconjug. Chem. 2011, 22, 2048-2059.
57. Perk, L.R.; Walsum, M.S.V.; Visser, G.W.M.; Kloet, R.W.; Vosjan, M.J.W.D.; Leemans, C.R.; Giaccone, G.; Albano, R.; Comoglio, P.M.; van Dongen, G.A.M.S. Quantitative PET imaging of Met-expressing human cancer xenografts with Zr-89-labelled monoclonal antibody DN30. Eur. J. Nucl. Med. Mol. I 2008, 35, 1857-1867.
58. Verel, I.; Visser, G.W.M.; Boerman, O.C.; van Eerd, J.E.M.; Finn, R.; Boellaard, R.; Vosjan, M.J.W.D.; Walsum, M.S.V.; Snow, G.B.; van Dongen, G.A.M.S. Long-lived positron emitters zirconium-89 and iodine-124 for scouting of therapeutic radioimmunoconjugates with PET. Cancer Biother. Radiol. 2003, 18, 655-661.
59. van Rij, C.M.; Sharkey, R.M.; Goldenberg, D.M.; Frielink, C.; Molkenboer, J.D.M.; Franssen, G.M.; van Weerden, W.M.; Oyen, W.J.G.; Boerman, O.C. Imaging of prostate cancer with Immuno-PET and Immuno-SPECT using a radiolabeled anti-EGP-1 monoclonal antibody. J. Nucl. Med. 2011, 52, 1601-1607.
60. Hong, H.; Severin, G.W.; Yang, Y.A.; Engle, J.W.; Zhang, Y.; Barnhart, T.E.; Liu, G.; Leigh, B.R.; Nickles, R.J.; Cai, W.B. Positron emission tomography imaging of CD105 expression with Zr-89-Df-TRC105. Eur. J. Nucl. Med. Mol. I 2012, 39, 138-148.
61. Nayak, T.K.; Garmestani, K.; Milenic, D.E.; Brechbiel, M.W. PET and MRI of metastatic peritoneal and pulmonary colorectal cancer in mice with human epidermal growth factor receptor 1-targeted Zr-89-labeled panitumumab. J. Nucl. Med. 2012, 53, 113-120.
62. Natarajan, A.; Habte, F.; Gambhir, S.S. Development of a novel long-lived immunopet tracer for monitoring lymphoma therapy in a humanized transgenic mouse model. Bioconjug. Chem. 2012, 23, 1221-1229.
63. Vosjan, M.J.W.D.; Vercammen, J.; Kolkman, J.A.; Stigter-van Walsum, M.; Revets, H.; van Dongen, G.A.M.S. Nanobodies targeting the hepatocyte growth factor: Potential new drugs for molecular cancer therapy. Mol. Cancer Ther. 2012, 11, 1017-1025.
64. O'Mara, R.E.; McAfee, J.G.; Subramanian, G. Rare earth nuclides as potential agents for skeletal imaging. J. Nucl. Med. 1969, 10, 49-51.
65. Wright, E.G. Radiation-induced genomic instability in haemopoietic cells. Int. J. Radiat. Biol. 1998, 74, 681-687.
66. Banfi, A.; Bianchi, G.; Galotto, M.; Cancedda, R.; Quarto, R. Bone marrow stromal damage after chemo/radiotherapy: Occurrence, Consequences and possibilities of treatment. Leuk. Lymph. 2001, 42, 863-870.
67. Otsuka, F.L.; Fleischman, J.B.; Welch, M.J. Comparative studies using 125I- and 111In-labeled monoclonal antibodies. Int. J. Radiat. Appl. Instr.1986, 13, 325-334.
68. Koizumi, M.; Endo, K.; Kunimatsu, M.; Sakahara, H.; Nakashima, T.; Kawamura, Y.; Watanabe, Y.; Saga, T.; Konishi, J.; Yamamuro, T.; et al. Ga-67-labeled antibodies for immunoscintigraphy and evaluation of tumor targeting of drug-antibody conjugates in mice. Cancer Res. 1988, 48, 1189-1194.
69. Smithjones, P.M.; Stolz, B.; Bruns, C.; Albert, R.; Reist, H.W.; Fridrich, R.; Macke, H.R. Gallium-67/Gallium-68-[Dfo]-Octreotide-a Potential Radiopharmaceutical for Pet Imaging of Somatostatin Receptor-Positive Tumors-Synthesis and Radiolabeling in-Vitro and Preliminary in-Vivo Studies. J. Nucl. Med. 1994, 35, 317-325.
70. OgiharaUmeda, I.; Sasaki, T.; Kojima, S.; Nishigori, H. Optimal radiolabeled liposomes for tumor imaging. J. Nucl. Med. 1996, 37, 326-332.
71. Heskamp, S.; van Laarhoven, H.W.M.; Molkenboer-Kuenen, J.D.M.; Franssen, G.M.; Versleijen-Jonkers, Y.M.H.; Oyen, W.J.G.; van der Graaf, W.T.A.; Boerman, O.C. ImmunoSPECT and immunopet of IGF-1R expression with the radiolabeled antibody R1507 in a triple-negative breast cancer model. J. Nucl. Med. 2010, 51, 1565-1572.
72. Perk, L.R.; Visser, G.W.M.; Vosjan, M.J.W.D.; Stigter-van Walsum, M.; Tijink, B.M.; Leemans, C.R.; van Dongen, G.A.M.S. Zr-89 as a PET surrogate radioisotope for scouting biodistribution of the therapeutic radiometals Y-90 and Lu-117 in tumor-bearing nude mice after coupling to the internalizing antibody cetuximab. J. Nucl. Med.2005, 46, 1898-1906.
73. Woodin, K.S.; Heroux, K.J.; Boswell, C.A.; Wong, E.H.; Weisman, G.R.; Niu, W.J.; Tomellini, S.A.; Anderson, C.J.; Zakharov, L.N.; Rheingold, A.L. Kinetic inertness and electrochemical behavior of copper(II) tetraazamacrocyclic complexes: Possible implications for in vivo stability. Eur. J. Inorg. Chem. 2005, 23, 4829-4833.
74. Heroux, K.J.; Woodin, K.S.; Tranchemontagne, D.J.; Widger, P.C.B.; Southwick, E.; Wong, E.H.; Weisman, G.R.; Tomellini, S.A.; Wadas, T.J.; Anderson, C.J.; et al. The long and short of it: The influence of N-carboxyethyl versus N-carboxymethyl pendant arms on in vitro and in vivo behavior of copper complexes of cross-bridged tetraamine macrocycles. Dalton Trans. 2007, 21, 2150-2162.
75. Wangler, B.; Schirrmacher, R.; Bartenstein, P.; Wangler, C. Chelating agents and their use in radiopharmaceutical sciences. Mini Rev. Med.Chem. 2011, 11, 968-983.
76. Guerard, F.; Lee, Y.S.; Tripier, R.; Szajek, L.P.; Deschamps, J.R.; Brechbiel, M.W. Investigation of Zr(IV) and Zr-89(IV) complexation with hydroxamates: Progress towards designing a better chelator than desferrioxamine B for immuno-PET imaging. Chem. Commun. 2013, 49, 1002-1004.
77. Liu, S. Radiolabeled multimeric cyclic RGD peptides as integrin alpha(v)beta(3) targeted radiotracers for tumor imaging. Mol. Pharm. 2006, 3, 472-487.
78. Li, Z.B.; Cai, W.B.; Cao, Q.Z.; Chen, K.; Wu, Z.H.; He, L.N.; Chen, X.Y. 64Cu-Labeled Tetrameric and octameric RGD peptides for small-animal PET of Tumor alpha(v)beta(3) integrin expression. J. Nucl. Med. 2007, 48, 1162-1171.
79. Hoeben, B.A.W.; Kaanders, J.H.A.M.; Franssen, G.M.; Troost, E.G.C.; Rijken, P.F.J.W.; Oosterwijk, E.; van Dongen, G.A.M.S.; Oyen, W.J.G.; Boerman, O.C.; Bussink, J. PET of hypoxia with Zr-89-labeled cG250-F(ab ')(2) in head and neck tumors. J. Nucl. Med. 2010, 51, 1076-1083.
80. Munnink, T.H.O.; de Vries, E.G.E.; Vedelaar, S.R.; Timmer-Bosscha, H.; Schroder, C.P.; Brouwers, A.H.; Lub-de Hooge, M.N. Lapatinib and 17AAG reduce Zr-89-trastuzumab-F(ab')(2) uptake in SKBR3 tumor xenografts. Mol. Pharm. 2012, 9, 2995-3002.
81. Heneweer, C.; Holland, J.P.; Divilov, V.; Carlin, S.; Lewis, J.S. Magnitude of enhanced permeability and retention effect in tumors with different phenotypes: Zr-89-albumin as a model system. J. Nucl. Med. 2011, 52, 625-633.
82. Heuveling, D.A.; Visser, G.W.M.; Baclayon, M.; Roos, W.H.; Wuite, G.J.L.; Hoekstra, O.S.; Leemans, C.R.; de Bree, R.; van Dongen, G.A.M.S. Zr-89-Nanocolloidal albumin-based PET/CT lymphoscintigraphy for sentinel node detection in head and neck cancer: preclinical results. J. Nucl. Med. 2011, 52, 1580-1584.
83. Heuveling, D.A.; van Schie, A.; Vugts, D.J.; Hendrikse, N.H.; Yaqub, M.; Hoekstra, O.S.; Karagozoglu, K.H.; Leemans, C.R.; van Dongen, G.A.; de Bree, R. Pilot study on the feasibility of PET/CT lymphoscintigraphy with 89Zr-nanocolloidal albumin for sentinel node identification in oral cancer patients. J. Nucl. Med. 2013, 54, 585-589.
84. Vugts, D.J.; Visser, G.W.; van Dongen, G.A. (89)Zr-PET radiochemistry in the development and application of therapeutic monoclonal antibodies and other biologicals. Curr. Top. Med. Chem. 2013, 13, 446-457.
85. van Dongen, G.A.M.S.; Vosjan, M.J.W.D. Immuno-positron emission tomography: Shedding light on clinical antibody therapy. Cancer Biother. Radiol. 2010, 25, 375-385.
86. Nagengast, W.B.; de Korte, M.A.; Munnink, T.H.O.; Timmer-Bosscha, H.; den Dunnen, W.F.; Hollema, H.; de Jong, J.R.; Jensen, M.R.; Quadt, C.; Garcia-Echeverria, C.; et al. (89)Zr-bevacizumab PET of early antiangiogenic tumor response to treatment with HSP90 inhibitor NVP-AUY922. J. Nucl. Med. 2010, 51, 761-767.
87. Ulmert, D.; Evans, M.J.; Holland, J.P.; Rice, S.L.; Wongvipat, J.; Pettersson, K.; Abrahamsson, P.A.; Scardino, P.T.; Larson, S.M.; Lilja, H.; et al. Imaging androgen receptor signaling with a radiotracer targeting free prostate-specific antigen. Cancer Discov. 2012, 2, 320-327.
88. Nagengast, W.B.; Lub-de Hooge, M.N.; Oosting, S.F.; den Dunnen, W.F.; Warnders, F.J.; Brouwers, A.H.; de Jong, J.R.; Price, P.M.; Hollema, H.; Hospers, G.A.; et al. VEGF-PET imaging is a noninvasive biomarker showing differential changes in the tumor during sunitinib treatment. Cancer Res. 2011, 71, 143-153.
89. Jagoda, E.M.; Lang, L.X.; Bhadrasetty, V.; Histed, S.; Williams, M.; Kramer-Marek, G.; Mena, E.; Rosenblum, L.; Marik, J.; Tinianow, J.N.; et al. Immuno-PET of the hepatocyte growth factor receptor Met using the 1-Armed antibody onartuzumab. J. Nucl. Med. 2012, 53, 1592-1600.
90. Chang, A.J.; De Silva, R.A.; Lapi, S.E. Development and characterization of 89Zr-labeled panitumumab for immuno-positron emission tomographic imaging of the epidermal growth factor receptor. Mol. Imaging 2013, 12, 17-27.
91. Ogasawara, A.; Tinianow, J.N.; Vanderbilt, A.N.; Gill, H.S.; Yee, S.; Flores, J.E.; Williams, S.P.; Ashkenazi, A.; Marik, J. ImmunoPET imaging of phosphatidylserine in pro-apoptotic therapy treated tumor models. Nucl. Med. Biol. 2013, 40, 15-22.
92. van der Bilt, A.R.; Terwisscha van Scheltinga, A.G.; Timmer-Bosscha, H.; Schroder, C.P.; Pot, L.; Kosterink, J.G.; van der Zee, A.G.; Lub-de Hooge, M.N.; de Jong, S.; de Vries, E.G.; et al. Measurement of tumor VEGF-A levels with 89Zr-bevacizumab PET as an early biomarker for the antiangiogenic effect of everolimus treatment in an ovarian cancer xenograft model. Clin. Cancer Res. 2012, 18, 6306-6314.
93. Dijkers, E.C.; Oude Munnink, T.H.; Kosterink, J.G.; Brouwers, A.H.; Jager, P.L.; de Jong, J.R.; van Dongen, G.A.; Schroder, C.P.; Lub-de Hooge, M.N.; de Vries, E.G. Biodistribution of 89Zr-trastuzumab and PET imaging of HER2-positive lesions in patients with metastatic breast cancer. Clin. Pharm. Ther. 2010, 87, 586-592.
94. Brouwers, A.; Verel, I.; Van Eerd, J.; Visser, G.; Steffens, M.; Oosterwijk, E.; Corstens, F.; Oyen, W.; Van Dongen, G.; Boerman, O. PET radioimmunoscintigraphy of renal cell cancer using 89Zr-labeled cG250 monoclonal antibody in nude rats. Cancer Biother. Radiopharm. 2004, 19, 155-163.
95. Rizvi, S.N.F.; Visser, O.J.; Vosjan, M.J.W.D.; van Lingen, A.; Hoekstra, O.S.; Zijlstra, J.M.; Huijgens, P.C.; van Dongen, G.A.M.S.; Lubberink, M. Biodistribution, radiation dosimetry and scouting of Y-90-ibritumomab tiuxetan therapy in patients with relapsed B-cell non-Hodgkin's lymphoma using Zr-89-ibritumomab tiuxetan and PET. Eur. J. Nucl. Med. Mol. I 2012, 39, 512-520.
96. van Scheltinga, A.G.T.T.; van Dam, G.M.; Nagengast, W.B.; Ntziachristos, V.; Hollema, H.; Herek, J.L.; Schroder, C.P.; Kosterink, J.G.W.; Lub-de Hoog, M.N.; de Vries, E.G.E. Intraoperative near-infrared fluorescence tumor imaging with vascular endothelial growth factor and human epidermal growth factor receptor 2 targeting antibodies. J. Nucl. Med. 2011, 52, 1778-1785.
97. Cohen, R.; Stammes, M.A.; de Roos, I.H.; Stigter-van Walsum, M.; Visser, G.W.; van Dongen, G.A. Inert coupling of IRDye800CW to monoclonal antibodies for clinical optical imaging of tumor targets. EJNMMI Res. 2011, 1, 31.
98. Bhattacharyya, S.; Kurdziel, K.; Wei, L.; Riffle, L.; Kaur, G.; Hill, G.C.; Jacobs, P.M.; Tatum, J.L.; Doroshow, J.H.; Kalen, J.D. Zirconium-89 labeled panitumumab: A potential immuno-PET probe for HER1-expressing carcinomas. Nucl. Med. Biol. 2013, 40, 451-457.
99. Munnink, T.H.O.; Dijkers, E.C.; Netters, S.J.; Lub-de Hooge, M.N.; Brouwers, A.H.; Haasjes, J.G.; Schroder, C.P.; de Vries, E.G. Trastuzumab pharmacokinetics influenced by extent human epidermal growth factor receptor 2-positive tumor load. J. Clin. Oncol. 2010, 28, E355-E356.
100. Gaykema, S.B.M.; Brouwers, A.H.; Hovenga, S.; Lub-de Hooge, M.N.; de Vries, E.G.E.; Schroder, C.P. Zirconium-89-trastuzumab positron emission tomography as a tool to solve a clinical dilemma in a patient with breast cancer. J. Clin. Oncol. 2012, 30, E74-E75.
101. Hong, H.; Zhang, Y.; Severin, G.W.; Yang, Y.N.; Engle, J.W.; Niu, G.; Nickles, R.J.; Chen, X.Y.; Leigh, B.R.; Barnhart, T.E.; et al. Multimodality Imaging of Breast Cancer Experimental Lung Metastasis with Bioluminescence and a Monoclonal Antibody Dual-Labeled with Zr-89 and IRDye 800CW. Mol. Pharm. 2012, 9, 2339-2349.