Antibody positron emission tomography imaging in anticancer drug development

Journal of Clinical Oncology

Volumn 33, Issue 13, 2015, Pages 1491-1504

  Lamberts, Laetitia E ^a   Williams, Simon P ^b   Terwisscha Van Scheltinga, Anton G T ^a   Hooge, Marjolijn N Lub De ^a   Schröder, Carolien P ^a   Gietema, Jourik A ^a   Brouwers, Adrienne H ^a   De Vries, Elisabeth G E ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BIOLOGICAL MARKER; DRUG ANTIBODY; MONOCLONAL ANTIBODY; RADIOPHARMACEUTICAL AGENT;

ARTICLE; CANCER PATIENT; CLINICAL TRIAL (TOPIC); DRUG EFFICACY; HUMAN; IMMUNO POSITRON EMISSION TOMOGRAPHY; ISOTOPE LABELING; MOLECULARLY TARGETED THERAPY; NONHUMAN; PATIENT SELECTION; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; TISSUE DISTRIBUTION; TREATMENT RESPONSE; ANIMAL; DRUG DEVELOPMENT; IMMUNOLOGY; METABOLISM; NEOPLASMS; PATHOLOGY; PREDICTIVE VALUE; PROCEDURES; SCINTISCANNING; TREATMENT OUTCOME; WHOLE BODY IMAGING;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; DRUG DISCOVERY; HUMANS; MOLECULAR TARGETED THERAPY; NEOPLASMS; PATIENT SELECTION; POSITRON-EMISSION TOMOGRAPHY; PREDICTIVE VALUE OF TESTS; RADIOPHARMACEUTICALS; TISSUE DISTRIBUTION; TREATMENT OUTCOME; WHOLE BODY IMAGING;

EID: 84929417538     PISSN: 0732183X     EISSN: 15277755     Source Type: Journal    
DOI: 10.1200/JCO.2014.57.8278     Document Type: Article

References (102)

1. Mathers CD, Loncar D: Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med 3:e442, 2006
2. Hanahan D, Weinberg RA: Hallmarks of cancer: The next generation. Cell 144:646-674, 2011
3. Reichert JM, Valge-Archer VE: Development trends for monoclonal antibody cancer therapeutics. Nat Rev Drug Discov 6:349-356, 2007
4. Teicher BA, Chari RV: Antibody conjugate therapeutics: Challenges and potential. Clin Cancer Res 17:6389-6397, 2011
5. Reichert JM: Antibodies to watch in 2013: Mid-year update. MAbs 4:513-517, 2013
6. Reichert JM, Wenger JB: Development trends for new cancer therapeutics and vaccines. Drug Discov Today 13:30-37, 2008
7. Wu AM, Olafsen T: Antibodies for molecular imaging of cancer. Cancer J 14:191-197, 2008
8. Willmann JK, van Bruggen N, Dinkelborg LM, et al: Molecular imaging in drug development. Nat Rev Drug Discov 7:591-607, 2008
9. Weissleder R, Pittet MJ: Imaging in the era of molecular oncology. Nature 452:580-589, 2008
10. van Dongen GA, Poot AJ, Vugts DJ: PET imaging with radiolabeled antibodies and tyrosine kinase inhibitors: Immuno-PET and TKI-PET. Tumour Biol 33:607-615, 2012
11. Keizer RJ, Huitema AD, Schellens JH, et al: Clinical pharmacokinetics of therapeutic monoclonal antibodies. Clin Pharmacokinet 49:493-507, 2010
12. Hogarth PM, Pietersz GA: Fc receptor-targeted therapies for the treatment of inflammation, cancer and beyond. Nat Rev Drug Discov 11:311-331, 2012
13. Robert C, Thomas L, Bondarenko I, et al: Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 364:2517-2526, 2011
14. Hamid O, Robert C, Daud A, et al: Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med 369:134-144, 2013
15. Hamid O, Sosman JA, Lawrence DP, et al: Clinical activity, safety, and biomarkers of MPDL3280A, an engineered PD-L1 antibody in patients with locally advanced or metastatic melanoma (mM). J Clin Oncol 31:550s, 2013 (suppl 15s; abstr 9010)
16. Wolchok JD, Kluger H, Callahan MK, et al: Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 369:122-133, 2013
17. Di Fede G, Bronte G, Rizzo S, et al: Monoclonal antibodies and antibody fragments: State of the art and future perspectives in the treatment of non-haematological tumors. Expert Opin Biol Ther 11:1433-1445, 2011
18. Wittrup KD, Thurber GM, Schmidt MM, et al: Practical theoretic guidance for the design of tumor-targeting agents. Methods Enzymol 503:255-268, 2012
19. Ravandi F, Estey EH, Appelbaum FR, et al: Gemtuzumab ozogamicin: Time to resurrect? J Clin Oncol 30:3921-3923, 2012
20. Gualberto A: Brentuximab vedotin (SGN-35), an antibody-drug conjugate for the treatment of CD30-positive malignancies. Expert Opin Investig Drugs 21:205-216, 2012
21. Verma S, Miles D, Gianni L, et al: Trastuzumab emtansine for HER2-positive advanced breast cancer. N Engl J Med 19:1783-1791, 2012
22. Goldsmith SJ: Radioimmunotherapy of lymphoma: Bexxar and zevalin. Semin Nucl Med 40: 122-135, 2010
23. Pospisilova S, Gonzalez D, Malcikova J, et al: ERIC recommendations on TP53 mutation analysis in chronic lymphocytic leukemia. Leukemia 26:1458-1461, 2012
24. Tan DS, Thomas GV, Garrett MD, et al: Biomarker-driven early clinical trials in oncology: A paradigm shift in drug development. Cancer J 15: 406-420, 2009
25. Gerlinger M, Rowan AJ, Horswell S, et al: Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 366:883-892, 2012
26. Sawyers CL: The cancer biomarker problem. Nature 452:548-552, 2008
27. Mach JP, Buchegger F, Forni M, et al: Use of radiolabeled monoclonal anti-CEA antibodies for the detection of human carcinomas by external photo-scanning and tomoscintigraphy. Immunol Today 2:239-249, 1981
28. Douketis JD, Ginsberg JS, Haley S, et al: Accuracy and safety of99m Tc-labeled anti-D-dimer (DI-80B3) fab' fragments (ThromboView(R)) in the diagnosis of deep vein thrombosis: A phase II study. Thromb Res 3:381-389, 2012
29. Prior JO, Farhad H, Muller O: Multimodality imaging in ischemic cardiomyopathy. Curr Cardiovasc Imaging Rep 7:9285, 2014
30. Rischpler C, Nekolla S, Schwaiger M: PET and SPECT in heart failure. Curr Cardiol Rep 15:337, 2013
31. Sharifi S, Nederveen AJ, Booij J, et al: Neuroimaging essentials in essential tremor: A systematic review. Neuroimage Clin 5:217-231, 2014
32. Booth TC, Nathan M, Waldman AD, et al: The role of functional dopamine-transporter SPECT imaging in parkinsonian syndromes, part 2. AJNR Am J Neuroradiol [epub ahead of print on June 12, 2014]
33. Czernin J, Phelps ME: Positron emission tomography scanning: Current and future applications. Annu Rev Med 53:89-112, 2002
34. Nayak TK, Brechbiel MW: Radioimmunoimaging with longer-lived positron-emitting radionuclides: Potentials and challenges. Bioconjug Chem 20:825-841, 2009
35. Histed SN, Lindenberg ML, Mena E, et al: Review of functional/anatomical imaging in oncology. Nucl Med Commun 33:349-361, 2012
36. Verel I, Visser GW, Boellaard R, et al: 89Zr immuno-PET: Comprehensive procedures for the production of 89Zr-labeled monoclonal antibodies. J Nucl Med 44:1271-1281, 2003
37. van Dongen GA, Vosjan MJ: Immunopositron emission tomography: Shedding light on clinical antibody therapy. Cancer Biother Radiopharm 25:375-385, 2010
38. Kaur S, Venktaraman G, Jain M, et al: Recent trends in antibody-based oncologic imaging. Cancer Lett 315:97-111, 2012
39. Dijkers EC, Oude Munnink TH, Kosterink JG, et al: Biodistribution of 89Zr-trastuzumab and PET imaging of HER2-positive lesions in patients with metastatic breast cancer. Clin Pharmacol Ther 87: 586-592, 2010
40. Oosting SF, Brouwers AH, van Es SC, et al: 89Zr-bevacizumab PET visualizes heterogeneous tracer accumulation in tumor lesions of renal cell carcinoma patients and differential effects of anti-angiogenic treatment. J Nucl Med 56:63-69, 2015
41. den Hollander MW, Bensch F, Glaudemans AWJM, et al: 89Zr-GC1008 PET imaging and GC1008 treatment of recurrent glioma patients. J Clin Oncol 31:126s, 2013 (suppl 15s; abstr 2050)
42. Bensch F, Lamberts LE, Lub-de Hooge MN, et al: Phase I imaging study of the HER3 antibody RG7116 using 89Zr-RG7116-PET in patients with metastatic or locally advanced HER3-positive solid tumors. J Clin Oncol 32:718s, 2014 (suppl 15s; abstr 11095)
43. Lamberts LE, Menke-van der Houven van Oordt CW, Bensch F, et al: PET-imaging with 89Zr-labeled anti-mesothelin antibody in patients with pancreatic of ovarian cancer. Ann Oncol 25, 2014 (abstr 1627P)
44. Hnatowich DJ, Layne WW, Childs RL, et al: Radioactive labeling of antibody: A simple and efficient method. Science 220:613-615, 1983
45. Malmberg J, Sandström M, Wester K, et al: Comparative biodistribution of imaging agents for in vivo molecular profiling of disseminated prostate cancer in mice bearing prostate cancer xenografts: Focus on 111In- and 125I-labeled anti-HER2 humanized monoclonal trastuzumab and ABY-025 affibody. Nucl Med Biol 38:1093-1102, 2011
46. Perik PJ, Lub-De Hooge MN, Gietema JA, et al: Indium-111-labeled trastuzumab scintigraphy in patients with human epidermal growth factor receptor 2-positive metastatic breast cancer. J Clin Oncol 24:2276-2282, 2006
47. Oldenhuis C, Dijkers EC, Duiker EW, et al: Development of radiolabeled mapatumumab and imaging in solid tumor patients who are treated with gemcitabine, cisplatin, and mapatumumab. J Clin Oncol 27:67e, 2009 (suppl; abstr e14521)
48. Desar IM, Stillebroer AB, Oosterwijk E, et al: 111In-bevacizumab imaging of renal cell cancer and evaluation of neoadjuvant treatment with the vascular endothelial growth factor receptor inhibitor sorafenib. J Nucl Med 51:1707-1715, 2010
49. Nagengast WB, Hooge MN, van Straten EM, et al: VEGF-SPECT with 111In-bevacizumab in stage III/IV melanoma patients. Eur J Cancer 47:1595-1602, 2011
50. Ellis RJ, Kaminsky DA, Zhou EH, et al: Ten-year outcomes: The clinical utility of single photon emission computed tomography/computed tomography capromab pendetide (prostascint) in a cohort diagnosed with localized prostate cancer. Int J Radiat Oncol Biol Phys 81:29-34, 2011
51. Wong WW, Schild SE, Vora SA, et al: Image-guided radiotherapy for prostate cancer: A prospective trial of concomitant boost using indium-111-capromab pendetide (ProstaScint) imaging. Int J Radiat Oncol Biol Phys 81:e423-e429, 2011
52. Brouwers AH, Buijs WC, Oosterwijk E, et al: Targeting of metastatic renal cell carcinoma with the chimeric monoclonal antibody G250 labeled with 131I or 111In: An intrapatient comparison. Clin Cancer Res 9:3953S-3960S, 2003
53. Goldenberg DM, DeLand F, Kim E, et al: Use of radiolabeled antibodies to carcinoembryonic antigen for the detection and localization of diverse cancers by external photoscanning. N Engl J Med 298:1384-1386, 1978
54. Goldenberg DM, Kim EE, DeLand FH, et al: Clinical radioimmunodetection of cancer with radioactive antibodies to human chorionic gonadotropin. Science 208:1284-1286, 1980
55. Goldenberg DM, Kim EE, Deland F, et al: Clinical studies on the radioimmunodetection of tumors containing alpha-fetoprotein. Cancer 45: 2500-2505, 1980
56. Epenetos AA, Britton KE, Mather S, et al: Targeting of iodine-123-labelled tumour-associated monoclonal antibodies to ovarian, breast, and gastrointestinal tumours. Lancet 2:999-1005, 1982
57. Yao YF, Yang Z, Li ZF, et al: Immunoscintigraphy of local recurrent rectal cancer with 99mTc-labeled anti-CEA monoclonal antibody CL58. World J Gastroenterol 13:1841-1846, 2007
58. Tagawa ST, Milowsky MI, Morris MJ, et al: Phase II study of lutetium-177 labeled anti-prostate-specific membrane antigen (PSMA) monoclonal antibody J591 for metastatic castration-resistant prostate cancer. Clin Cancer Res 7:5182-5191, 2013
59. Stillebroer AB, Franssen GM, Mulders PF, et al: ImmunoPET imaging of renal cell carcinoma with 124I- and 89Zr-labeled anti-CAIX monoclonal antibody cG250 in mice. Cancer Biother Radiopharm 28:510-515, 2013
60. Jayson GC, Zweit J, Jackson A, et al: Molecular imaging and biological evaluation of HuMV833 anti-VEGF antibody: Implications for trial design of antiangiogenic antibodies. J Natl Cancer Inst 94: 1484-1493, 2002
61. Divgi CR, Pandit-Taskar N, Jungbluth AA, et al: Preoperative characterisation of clear-cell renal carcinoma using iodine-124-labelled antibody chimeric G250 (124I-cG250) and PET in patients with renal masses: A phase I trial. Lancet Oncol 8:304-310, 2007
62. Divgi CR, Uzzo RG, Gatsonis C, et al: Positron emission tomography/computed tomography identification of clear cell renal cell carcinoma: Results from the REDECT trial. J Clin Oncol 31:187-194, 2013
63. Carrasquillo JA, Pandit-Taskar N, O'Donoghue JA, et al: 124I-huA33 antibody PET of colorectal cancer. J Nucl Med 52:1173-1180, 2011
64. Philpott GW, Schwarz SW, Anderson CJ, et al: RadioimmunoPET: Detection of colorectal carcinoma with positron-emitting copper-64-labeled monoclonal antibody. J Nucl Med 36:1818-1824, 1995
65. Tamura K, Kurihara H, Yonemori K, et al: 64Cu-DOTA-trastuzumab-PET imaging in patients with HER2-positive breast cancer. J Clin Oncol 30: 660s, 2012 (suppl; abstr 10519)
66. Rizvi SN, Visser OJ, Vosjan MJ, et al: Biodistribution, radiation dosimetry and scouting of 90Y-ibritumomab tiuxetan therapy in patients with relapsed B-cell non-hodgkin's lymphoma using 89Zr-ibritumomab tiuxetan and PET. Eur J Nucl Med Mol Imaging 39:512-520, 2012
67. Aerts HJ, Dubois L, Perk L, et al: Disparity between in vivo EGFR expression and 89Zr-labeled cetuximab uptake assessed with PET. J Nucl Med 50:123-131, 2009
68. Ray GL, Baidoo KE, Wong KJ, et al: Preclinical evaluation of a monoclonal antibody targeting the epidermal growth factor receptor as a radioimmunodiagnostic and radioimmunotherapeutic agent. Br J Pharmacol 157:1541-1548, 2009
69. Niu G, Sun X, Cao Q, et al: Cetuximab-based immunotherapy and radioimmunotherapy of head and neck squamous cell carcinoma. Clin Cancer Res 16:2095-2105, 2010
70. Niu G, Li Z, Xie J, et al: PET of EGFR antibody distribution in head and neck squamous cell carcinoma models. J Nucl Med 50:1116-1123, 2009
71. Nayak TK, Garmestani K, Baidoo KE, et al: Preparation, biological evaluation, and pharmacokinetics of the human anti-HER1 monoclonal antibody panitumumab labeled with 86Y for quantitative PET of carcinoma. J Nucl Med 51:942-950, 2010
72. Menke CW, Gootjes EC, Huisman MC, et al: ImmunoPET imaging with 89Zr-cetuximab in patients with advanced colorectal cancer. J Clin Oncol 32:720s, 2014 (suppl 15s; abstr 11102)
73. Wilson CB, Snook DE, Dhokia B, et al: Quantitative measurement of monoclonal antibody distribution and blood flow using positron emission tomography and 124iodine in patients with breast cancer. Int J Cancer 47:344-347, 1991
74. Pandit-Taskar N, O'Donoghue JA, Beylergil V, et al: 89Zr-huJ591 immuno-PET imaging in patients with advanced metastatic prostate cancer. Eur J Nucl Med Mol Imaging 41:2093-2105, 2014
75. Carrasquillo JA, Danila DC, Beylergil V, et al: Initial PET imaging and pharmacokinetic results from a phase I/II study of Zr-89-labeled anti-STEAP1 antibody in metastatic castrate-resistant prostate cancer (mCRPC) patients. 105th Annual Meeting of the American Association for Cancer Research, San Diego, CA, April 5-9, 2014 (abstr 2069)
76. Gaykema SB, Brouwers AH, Hovenga S, et al: Zirconium-89-trastuzumab positron emission tomography as a tool to solve a clinical dilemma in a patient with breast cancer. J Clin Oncol 30:e74-e75, 2012
77. Gaykema SB, Brouwers AH, Lub-de Hooge MN, et al: 89Zr-bevacizumab PET imaging in primary breast cancer. J Nucl Med 54:1014-1018, 2013
78. Terwisscha van Scheltinga AGT, Lub-de Hooge MN, Abiraj K, et al: ImmunoPET and biodistribution with human epidermal growth factor receptor 3 targeting radiolabeled antibody 89Zr-GE-huMAb-HER3. Eur J Cancer 48:96-97, 2012
79. Gill HS, Tinianow JN, Ogasawara A, et al: A modular platform for the rapid site-specific radiolabeling of proteins with18F exemplified by quantitative positron emission tomography of human epidermal growth factor receptor 2. J Med Chem 52:5816-5825, 2009
80. Nagengast WB, de Korte MA, Oude Munnink TH, et al: 89Zr-bevacizumab PET of early antiangiogenic tumor response to treatment with HSP90 inhibitor NVP-AUY922. J Nucl Med 51:761-767, 2010
81. Gaykema SBM, Schröder CP, Vitfell-Rasmussen J, et al: 89Zr-trastuzumab and 89Zr-bevacizumab PET to evaluate the effect of the heat shock protein 90 inhibitor NVP-AUY922 in metastatic breast cancer patients. Clin Cancer Res 20: 3945-3954, 2014
82. Jain RK: Normalizing tumor vasculature with anti-angiogenic therapy: A new paradigm for combination therapy. Nat Med 7:987-989, 2001
83. Arjaans M, Oude Munnink TH, Oosting SF, et al: Bevacizumab-induced normalization of blood vessels in tumors hampers antibody uptake. Cancer Res 73:3347-3355, 2013
84. Pastuskovas CV, Mundo EE, Williams SP, et al: Effects of anti-VEGF on pharmacokinetics, biodistribution, and tumor penetration of trastuzumab in a preclinical breast cancer model. Mol Cancer Ther 11:752-762, 2012
85. Van der Veldt AA, Lubberink M, Bahce I, et al: Rapid decrease in delivery of chemotherapy to tumors after anti-VEGF therapy: Implications for scheduling of anti-angiogenic drugs. Cancer Cell 21:82-91, 2012
86. van der Bilt AR, Terwisscha van Scheltinga AG, Timmer-Bosscha H, 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 18:6306-6314, 2012
87. van Asselt SJ, Oosting SF, Brouwers AH, et al: Everolimus reduces 89Zr-bevacizumab tumor uptake in patients with neuroendocrine tumors. J Nucl Med 55:1087-1092, 2014
88. Bruno R, Washington CB, Lu JF, et al: Population pharmacokinetics of trastuzumab in patients with HER2+ metastatic breast cancer. Cancer Chemother Pharmacol 56:361-369, 2005
89. Oude Munnink TH, Dijkers EC, Netters SJ, et al: Trastuzumab pharmacokinetics influenced by extent human epidermal growth factor receptor 2-positive tumor load. J Clin Oncol 28:e355-e356, 2010
90. Perk LR, Visser GW, Vosjan MJ, et al: (89)Zr as a PET surrogate radioisotope for scouting biodistribution of the therapeutic radiometals (90)Y and (177)Lu in tumor-bearing nude mice after coupling to the internalizing antibody cetuximab. J Nucl Med 46:1898-1906, 2005
91. Gebhart G, Lamberts LE, Garcia C, et al: PET/CT with 89Zr-trastuzumab and 18F-FDG to individualize treatment with trastuzumab emtansine (T-DM1) in metastatic HER2 positive breast cancer (mBC). J Clin Oncol 32: 695s, 2014 (suppl 15s; abstr 11001)
92. Langer A: A systematic review of PET and PET/CT in oncology: A way to personalize cancer treatment in a cost-effective manner? BMC Health Serv Res 10:283, 2010
93. Borjesson PK, Jauw YW, de Bree R, et al: Radiation dosimetry of 89Zr-labeled chimeric monoclonal antibody U36 as used for immuno-PET in head and neck cancer patients. J Nucl Med 50:1828-1836, 2009
94. van Dam GM, Themelis G, Crane LM, et al: Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-α targeting: First in-human results. Nat Med 17:1315-1319, 2011
95. Frangioni JV: New technologies for human cancer imaging. J Clin Oncol 26:4012-4021, 2008
96. Terwisscha van Scheltinga AG, van Dam GM, Nagengast WB, et al: Intraoperative nearinfrared fluorescence tumor imaging with vascular endothelial growth factor and human epidermal growth factor receptor 2 targeting antibodies. J Nucl Med 52:1778-1785, 2011
97. Azhdarinia A, Ghosh P, Ghosh S, et al: Dual-labeling strategies for nuclear and fluorescence molecular imaging: A review and analysis. Mol Imaging Biol 14:261-276, 2012
98. Cohen R, Vugts DJ, Stigter-van Walsum M, et al: Inert coupling of IRDye800CW and zirconium-89 to monoclonal antibodies for single- or dual-mode fluorescence and PET imaging. Nat Protoc 8:1010-1018, 2013
99. Sliwkowski MX, Mellman I: Antibody therapeutics in cancer. Science 341:1192-1198, 2013
100. D'Huyvetter M, Xavier C, Caveliers V, et al: Radiolabeled nanobodies as theranostic tools in targeted radionuclide therapy of cancer. Expert Opin Drug Deliv 11:1939-1954, 2014
101. Sharkey RM, Karacay H, Litwin S, et al: Improved therapeutic results by pretargeted radioimmunotherapy of non-Hodgkin's lymphoma with a new recombinant, trivalent, anti-CD20, bispecific antibody. Cancer Res 68:5282-5290, 2008
102. Sharkey RM, Karacay H, Johnson CR, et al: Pretargeted versus directly targeted radioimmunotherapy combined with anti-CD20 antibody consolidation therapy of non-Hodgkin lymphoma. J Nucl Med 50:444-453, 2009