Radiolabeled nanobodies as theranostic tools in targeted radionuclide therapy of cancer

Expert Opinion on Drug Delivery

Volumn 11, Issue 12, 2014, Pages 1939-1954

  D'Huyvetter, Matthias ^a,b   Xavier, Catarina ^b   Caveliers, Vicky ^b,c   Lahoutte, Tony ^b,c   Muyldermans, Serge ^b,d   Devoogdt, Nick ^b  

^a BELGIAN NUCLEAR RESEARCH CENTRE   (Belgium)

^b VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^c UNIVERSITY HOSPITAL BRUSSELS   (Belgium)

^d DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

Cancer; Nanobody; Nuclear imaging; Radiochemistry; Radionuclide; Targeted radionuclide therapy; Theranostics

Indexed keywords

ANTINEOPLASTIC AGENT; NANOBODY; PEPTIDE; RADIOACTIVE IODINE; RADIOLABELED NANOBODY; RADIOPHARMACEUTICAL AGENT; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

ANTIBODY COMBINING SITE; ANTIGEN BINDING; ANTIGEN SPECIFICITY; CANCER DIAGNOSIS; CANCER IMMUNOTHERAPY; DOSIMETRY; DOUBLE STRANDED DNA BREAK; DRUG CLEARANCE; DRUG HALF LIFE; EXTERNAL BEAM RADIOTHERAPY; HEAVY CHAIN; HUMAN; ISOTOPE LABELING; LINEAR ENERGY TRANSFER; MALIGNANT NEOPLASTIC DISEASE; MOLECULAR WEIGHT; MOLECULARLY TARGETED THERAPY; MULTIPLE MYELOMA; PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); RADIATION EXPOSURE; RADIOIMMUNOTHERAPY; RADIOISOTOPE THERAPY; REVIEW; TARGETED RADIONUCLIDE THERAPY; ANIMAL; NEOPLASMS; SCINTISCANNING;

ANIMALS; HUMANS; NEOPLASMS; RADIOPHARMACEUTICALS; SINGLE-DOMAIN ANTIBODIES;

EID: 84911482207     PISSN: 17425247     EISSN: 17447593     Source Type: Journal    
DOI: 10.1517/17425247.2014.941803     Document Type: Review

References (84)

1. Prise KM, Schettino G, Folkard M, Held KD. New insights on cell death from radiation exposure. Lancet Oncol 2005;6(7):520-8
2. Lee DY, Li KCP. Molecular theranostics: a primer for the imaging professional. AJR Am J Roentgenol 2011;197(2):318-24
3. Ersahin D, Doddamane I, Cheng D. Targeted radionuclide therapy. Cancer 2011;3(4):3838-55
4. Pouget JP, Navarro-Teulon I, Bardiès M, et al. Clinical radioimmunotherapy - the role of radiobiology. Nat Rev Clin Oncol 2011;8(12):720-34
5. Shirley M, McCormack PL. Radium-223 dichloride: a review of its use in patients with castration-resistant prostate cancer with symptomatic bone metastases. Drugs 2014;74(5):579-86
6. Cornelissen B, Darbar S, Kersemans V, et al. Amplification of DNA damage by a gammaH2AX-targeted radiopharmaceutical. Nucl Med Biol 2012;39:1142-51
7. Mishra A, Lai GH, Schmidt NW, et al. Translocation of HIV TAT peptide and analogues induced by multiplexed membrane and cytoskeletal interactions. Proc Natl Acad Sci USA 2011;108:16883-8
8. Van Nostrand D. The benefits and risks of I-131 therapy in patients with well-differentiated thyroid cancer. Thyroid 2009;19(12):1381-91
9. Mazzaferri EL, Jhiang SM. Long-term impact of initial surgical and medical therapy on papillary and follicular thyroid cancer. Am J Med 1994;97(5):418-28
10. Friedman M, Stahl S. Engineered affinity proteins for tumour-targeting applications. Biotechnol Appl Biochem 2009;53:1-29
11. Reichert JM. Antibodies to watch in 2014. MAbs 2014;6(1):5-14
12. Goldsmith SJ. Radioimmunotherapy of lymphoma: bexxar and Zevalin. Semin Nucl Med 2010;40(2):122-35
13. Verheijen RH, Massuger LF, Benigno BB, et al. Phase III trial of intraperitoneal therapy with yttrium-90-labeled HMFG1 murine monoclonal antibody in patients with epithelial ovarian cancer after a surgically defined complete remission. J Clin Oncol 2006;24(4):571-8
14. Goldenberg DM. Targeted therapy of cancer with radiolabeled antibodies. J Nucl Med 2002;43(5):693-713
15. Fang J, Nakamura H, Maeda H. The EPR effect: unique feature of tumor blood vessels for drug delivery, factors involved, and limitations and augmentation of the effect. Adv Drug Deliv Rev 2011;63(3):136-51
16. Frampas E, Rousseau C, Bodet-Milin C, et al. Improvement of radioimmunotherapy using pretargeting. Front Oncol 2013;3:159
17. Sgouros G. Radioimmunotherapy of micrometastatses: sidestepping the solid-tumor hurdle. J Nucl Med 1995;36(10):1910-12
18. Liersch T, Meller J, Kulle B, et al. Phase II trial of carcinoembryonic antigen radioimmunotherapy with (131) I-labetuzumab after salvage resection of colorectal metastases in the liver: five-year safety and efficacy results. J Clin Oncol 2005;23:6763
19. Readon DA, Akabani G, Coleman RE, et al. Salvage radioimmunotherapy with murine iodine-131-labeled antitenascin monoclonal antibody 81C6 for patients with recurrent primary and metastatic malignant brain tumors: phase II study results. J Clin Oncol 2006;24:115-22
20. Hudson PJ, Souriau C. Engineered antibodies. Nat Med 2003;9:129-34
21. De Vos J, Devoogdt N, Lahoutte T, Muyldermans S. Camelid single-domain antibody-fragment engineering for (pre) clinical in vivo molecular imaging applications: adjusting the bullet to its target. Expert Opin Biol Ther 2013;13(8):1149-60
22. Zaknun JJ, Bodei L, Mueller-Brand J, et al. The joint IAEA. EANM, and SNMMI practical guidance on peptide receptor radionuclide therapy (PRRNT) in neuroendocrine tumours. Eur J Nucl Med Mol Imaging 2013;40(5):800-16
23. Kam BLR, Teunissen JJM, Krenning EP, et al. Lutetium-labelled peptides for therapy of neuroendocrine tumours. Eur J Nucl Med Mol Imaging 2012;39(Suppl 1):S103-12
24. Melis M, Bijster M, de Visser M, et al. Dose-response effect of Gelofusine on renal uptake and retention of radiolabelled octreotide in rats with CA20948 tumours. Eur J Nucl Med Mol Imaging 2009;36:1968-76
25. van Eerd JE, Vegt E, Wetzels JF, et al. Gelatin-based plasma expander effectively reduces renal uptake of 111In-octreotide in mice and rats. J Nucl Med 2006;47:528-33
26. Vegt E, Wetzels JF, Russel FG, et al. Renal uptake of radiolabeled octreotide in human subjects is efficiently inhibited by succinylated gelatin. J Nucl Med 2006;47:432-6
27. Rolleman EJ, Bernard BF, Breeman WA, et al. Molecular imaging of reduced renal uptake of radiolabelled [DOTA0,Tyr3] octreotate by the combination of lysine and gelofusine in rats. Nuklearmedizin 2008;47:110-15
28. Gotthardt M, van Eerd-Vismale J, Oyen WJ, et al. Indication for different mechanisms of kidney uptake of radiolabeled peptides. J Nucl Med 2007;48:596-601
29. Sabet A, Ezziddin K, Pape U, et al. Accurate assessment of long-term nephrotoxicity after peptide receptor radionuclide therapy with 177Lu-octreotate. Eur J Nucl Med Mol Imaging 2014;41:505-10
30. Reubi JC, Schaer JC, Waser B. Cholecystokinin(CCK)-A and CCK-B/gastrin receptors in human tumors. Cancer Res 1997;57:1377-86
31. Markwalder R, Reubi JC. Gastrin-releasing peptide receptors in the human prostate: relation to neoplastic transformation. Cancer Res 1999;59:1152-9
32. Reubi JC. In vitro identification of vasoactive intestinal peptide receptors in human tumors: implications for tumor imaging. J Nucl Med 1995;36:1846-53
33. Weidle UH, Auer J, Brinkmann U, et al. The emerging role of new protein scaffold-based agents for treatment of cancer. Cancer Genomics Proteomics 2013;10(4):155-68
34. Kimura RH, Cheng Z, Gambhir SS, Cochran JR. Engineered knottin peptides: a new class of agents for imaging integrin expression in living subjects. Cancer Res 2009;69(6):2435-42
35. Zahnd C, Kawe M, Stumpp MT, et al. Efficient tumor targeting with high-affinity designed ankyrin repeat proteins: effects of affinity and molecular size. Cancer Res 2010;70(4):1595-605
36. Stern LA, Case BA, Hackel BJ. Alternative non-antibody protein scaffolds for molecular imaging of cancer. Curr Opin Chem Eng 2013;published online November 2013; doi: 10.1016/j.coche.2013.08.009
37. Nilsson B, Moks T, Jansson B, et al. A synthetic IgG-binding domain based on staphylococcal protein A. Protein Eng 1987;1(2):107-13
38. Perols A, Honarvar H, Strand J, et al. Influence of DOTA chelator position on biodistribution and targeting properties of (111)In-labeled synthetic anti-HER2 affibody molecules. Bioconjug Chem 2012;23(8):1661-70
39. Malmberg J, Perols A, Varasteh Z, et al. Comparative evaluation of synthetic anti-HER2 Affibody molecules site-specifically labelled with 111In using N-terminal DOTA, NOTA and NODAGA chelators in mice bearing prostate cancer xenografts. Eur J Nucl Med Mol Imaging 2012;39(3):481-92
40. Altai M, Varasteh Z, Andersson K, et al. In vivo and in vitro studies on renal uptake of radiolabeled affibody molecules for imaging of HER2 expression in tumors. Cancer Biother Radiopharm 2013;28(3):187-95
41. Tolmachev V, Orlova A, Pehrson R, et al. Radionuclide therapy of HER2-positive microxenografts using a 177Lu-labeled HER2-specific affibody molecule. Cancer Res 2007;67(6):2773-82
42. Steffen AC, Almqvist Y, Chyan MK, et al. Biodistribution of 211At labeled HER-2 binding affibody molecules in mice. Oncol Rep 2007;17:1141-7
43. Jiang L, Miao Z, Kimura RH, et al. Preliminary evaluation of (177)Lu-labeled knottin peptides for integrin receptor-targeted radionuclide therapy. Eur J Nucl Med Mol Imaging 2011;38(4):613-22
44. Hamers-Casterman C, Atarhouch T, Muyldermans S, et al. Naturally occurring antibodies devoid of light chains. Nature 1993;363(6428):446-8
45. Stijlemans B, Conrath K, Cortez-Retamozo V, et al. Efficient targeting of conserved cryptic epitopes of infectious agents by single domain antibodies, African trypanosomes as paradigm. J Biol Chem 2004;279:1256-61
46. Vu KB, Ghahroudi MA, Wyns L, Muyldermans S. Comparison of llama VH sequences from conventional and heavy chain antibodies. Mol Immunol 1997;34(16-17):1121-31
47. Muyldermans S, Atarhouch T, Saldanha J, et al. Sequence and structure of VH domain from naturally occurring camel heavy chain immunoglobulins lacking light chains. Protein Eng 1994;7(9):1129-35
48. Nguyen VK, Desmyter A, Muyldermans S. Functional heavy-chain antibodies in Camelidae. Adv Immunol 2001;79:261-96
49. Conrath K, Vincke C, Stijlemans B, et al. Antigen binding and solubility effects upon the veneering of a camel VHH in framework-2 to mimic a VH. J Mol Biol 2005;350(1):112-25
50. Dolk E, van Vliet C, Perez JM, et al. Induced refolding of a temperature denatured llama heavy-chain antibody fragment by its antigen. Proteins 2005;59(3):555-64
51. Arbabi Ghahroudi M, Tanha J, MacKenzie R. Prokaryotic expression of antibodies. Cancer Metastasis Rev 2005;24(4):501-19
52. Frenken LG, van der Linden RH, Hermans PW, et al. Isolation of antigen specific llama VHH antibody fragments and their high level secretion by Saccharomyces cerevisiae. J Biotechnol 2000;78(1):11-21
53. Cortez-Retamozo V, Lauwereys M, Hassanzadeh GG, et al. Efficient tumor targeting by single-domain antibody fragments of camels. Int J Cancer 2002;98(3):456-62
54. Vincke C, Loris R, Saerens S, et al. General strategy to humanize a camelid single-domain antibody and identification of a universal humanized nanobody scaffold. J Biol Chem 2009;284(5):3273-84
55. Vaneycken I, Govaert J, Vincke C, et al. In vitro analysis and in vivo tumor targeting of a humanized, grafted nanobody in mice using pinhole SPECT/micro-CT. J Nucl Med 2010;51(7):1099-106
56. Movahedi K, Schoonooghe S, Laoui D, et al. Nanobody-based targeting of the macrophage mannose receptor for effective in vivo imaging of tumor-associated macrophages. Cancer Res 2012;72:4165-77
57. Roovers RC, Vosjan MJ, Laeremans T, et al. A biparatopic anti-EGFR nanobody efficiently inhibits solid tumour growth. Int J Cancer 2011;129(8):2013-24
58. Tijink BM, Laeremans T, Budde M, et al. Improved tumor targeting of antiepidermal growth factor receptor Nanobodies through albumin binding: taking advantage of modular nanobody technology. Mol Cancer Ther 2008;7(8):2288-97
59. Broisat A, Hernot S, Toczek J, et al. Nanobodies targeting mouse/human VCAM1 for the nuclear imaging of atherosclerotic lesions. Circ Res 2012;110(7):927-37
60. De Vos J, Mathijs I, Xavier C, et al. Specific targeting of atherosclerotic plaques in ApoE-/- mice using a new camelid sdAb binding the vulnerable plaque marker LOX-1. Mol Imaging Biol 2014. [Epub ahead of print]
61. Put S, Schoonooghe S, Devoogdt N, et al. SPECT imaging of joint inflammation with Nanobodies targeting the macrophage mannose receptor in a mouse model for rheumatoid arthritis. J Nucl Med 2013;54(5):807-14
62. Zheng F, Put S, Bouwens L, et al. Molecular imaging with macrophage VSIG4-targeting Nbs for diagnosis and prognosis in a mouse model of rheumatoid arthritis. J Nucl Med 2014;55(5):824-9
63. De Groeve K, Deschacht N, De Koninck C, et al. Nanobodies as tools for In Vivo imaging of specific immune cell types. J Nucl Med 2010;51:782-9
64. Gainkam LO, Huang L, Caveliers V, et al. Comparison of the biodistribution and tumor targeting of two 99mTc-labeled anti-EGFR nanobodies in mice, using pinhole SPECT/micro-CT. J Nucl Med 2008;49(5):788-95
65. Vaneycken I, Devoogdt N, Van Gassen N, et al. Preclinical screening of anti-HER2 nanobodies for molecular imaging of breast cancer. FASEB J 2011;25(7):2433-46
66. Evazalipour M, D'Huyvetter M, Soltani Tehrani B, et al. Generation and characterization of nanobodies targeting PSMA for molecular imaging of prostate cancer. Contrast Media Mol Imaging 2014;9(3):211-20
67. Vosjan MJ, Perk LR, Roovers RC, et al. Facile labeling of an anti-epidermal growth factor receptor Nanobody with (68)Ga via a novel bifunctional desferal chelate for immuno-PET. Eur J Nucl Med Mol Imaging 2011;38(4):753-63
68. Xavier C, Vaneycken I, D'huyvetter M, et al. Synthesis, Preclinical Validation, Dosimetry, and Toxicity of 68Ga-NOTA-Anti-HER2 Nanobodies for iPET Imaging of HER2 Receptor Expression in Cancer. J Nucl Med 2013;54(5):776-84
69. Harris N, Super M, Rits M, et al. Characterization of the murine macrophage mannose receptor: demonstration that the downregulation of receptor expression mediated by interferon-gamma occurs at the level of transcription. Blood 1992;80:2363-73
70. Vosjan MJ, Vercammen J, Kolkman JA, et al. Nanobodies targeting the hepatocyte growth factor: potential new drugs for molecular cancer therapy. Mol Cancer Ther 2012;11(4):1017-25
71. Sleep D, Cameron J, Evans LR. Albumin as a versatile platform for drug half-life extension. Biochim Biophys Acta 2013;1830(12):5526-34
72. Gainkam LO, Caveliers V, Devoogdt N, et al. Localization, mechanism and reduction of renal retention of technetium-99m labeled epidermal growth factor receptor-specific nanobody in mice. Contrast Media Mol Imaging 2011;6(2):85-92
73. D'Huyvetter M, Vincke C, Xavier C, et al. Targeted radionuclide therapy with a 177Lu-labeled anti-HER2 nanobody. Theranostics 2014;4(7):708-20
74. Wa˚llberg H, Orlova A, Altai M, et al. Molecular design and optimization of 99mTc-labeled recombinant affibody molecules improves their biodistribution and imaging properties. J Nucl Med 2011;52(3):461-9
75. D'Huyvetter M, Aerts A, Xavier C, et al. Development of 177Lu-nanobodies for radioimmunotherapy of HER2-positive breast cancer: evaluation of different bifunctional chelators. Contrast Media Mol Imaging 2012;7:254-64
76. Pruszynski M, Koumarianou E, Vaidyanathan G, et al. Targeting breast carcinoma with radioiodinated anti-HER2 Nanobody. Nucl Med Biol 2013;40(1):52-9
77. Pruszynski M, Koumarianou E, Vaidyanathan G, et al. Improved tumor targeting of anti-HER2 nanobody through N-succinimidyl 4-guanidinomethyl-3-iodobenzoate radiolabeling. J Nucl Med 2014;55:1-7
78. Kumar SK, Rajkumar SV, Dispenzieri A, et al. Improved survival in multiple myeloma and the impact of novel therapies. Blood 2008;111:2516-20
79. Lemaire M, D'Huyvetter M, Lahoutte T, et al. Imaging and radioimmunotherapy of multiple myeloma with anti-idiotypic Nanobodies. Leukemia 2014;28(2):444-7
80. Sharma P, Wagner K, Wolchok JD, Allison JP. Novel cancer immunotherapy agents with survival benefit: recent successes and next steps. Nat Rev Cancer 2011;11(11):805-12
81. Leader B, Baca QJ, Golan DE. Protein therapeutics: a summary and pharmacological classification. Nat Rev Drug Discov 2008;7(1):21-39
82. Vacchelli E, Vitale I, Tartour E, et al. Trial watch anticancer radioimmunotherapy. Oncoimmunology 2013;2(9):e25595
83. Tomblyn MB, Katin MJ, Wallner PE. The new golden era for radioimmunotherapy: not just for lymphomas anymore. Cancer Contr 2013;20(1):60-71
84. Meredith RF, Torgue J, Azure MT, et al. Pharmacokinetics and imaging of 212Pb-TCMC-trastuzumab after intraperitoneal administration in ovarian cancer patients. Cancer Biother Radiopharm 2014;29(1):12-17