Camelid single-domain antibody-fragment engineering for (pre)clinical in vivo molecular imaging applications: adjusting the bullet to its target

Bibliography

• Mankoff DA. A definition of molecular imaging. J Nucl Med 2007;48(6):18N; 21N
   PubMed Web of Science ®Google Scholar
• Willmann JK, van Bruggen N, Dinkelborg LM, Gambhir SS. Molecular imaging in drug development. Nat Rev Drug Discov 2008;7(7):591-607
   PubMed Web of Science ®Google Scholar
• Lee S, Xie J, Chen X. Peptide-based probes for targeted molecular imaging. Biochemistry 2010;49(7):1364-76
   PubMed Web of Science ®Google Scholar
• Lin X, Xie J, Chen X. Protein-based tumor molecular imaging probes. Amino Acids 2011;41(5):1013-36
   PubMed Web of Science ®Google Scholar
• Sinusas AJ, Thomas JD, Mills G. The future of molecular imaging. JACC Cardiovasc Imaging 2011;4(7):799-806
   PubMed Web of Science ®Google Scholar
• Peterson TE, Manning HC. Molecular imaging: 18F-FDG PET and a whole lot more. J Nucl Med Technol 2009;37(3):151-61
   PubMedGoogle Scholar
• Matter CM, Stuber M, Nahrendorf M. Imaging of the unstable plaque: how far have we got? Eur Heart J 2009;30(21):2566-74
   PubMed Web of Science ®Google Scholar
• Wong FC, Kim EE. A review of molecular imaging studies reaching the clinical stage. Eur J Radiol 2009;70(2):205-11
   PubMed Web of Science ®Google Scholar
• Wilbanks T, Peterson JA, Miller S, et al. Localization of mammary tumors in vivo with 131I-labeled Fab fragments of antibodies against mouse mammary epithelial (MME) antigens. Cancer 1981;48(8):1768-75
   PubMed Web of Science ®Google Scholar
• Adams GP, McCartney JE, Tai MS, et al. Highly specific in vivo tumor targeting by monovalent and divalent forms of 741F8 anti-c-erbB-2 single-chain Fv. Cancer Res 1993;53(17):4026-34
   PubMed Web of Science ®Google Scholar
• Hu S, Shively L, Raubitschek A, et al. Minibody: a novel engineered anti-carcinoembryonic antigen antibody fragment (single-chain Fv-CH3) which exhibits rapid, high-level targeting of xenografts. Cancer Res 1996;56(13):3055-61
   PubMed Web of Science ®Google Scholar
• Sundaresan G, Yazaki PJ, Shively JE, et al. 124I-labeled engineered anti-CEA minibodies and diabodies allow high-contrast, antigen-specific small-animal PET imaging of xenografts in athymic mice. J Nucl Med 2003;44(12):1962-9
   PubMed Web of Science ®Google Scholar
• Orlova A, Nilsson FY, Wikman M, et al. Comparative in vivo evaluation of technetium and iodine labels on an anti-HER2 affibody for single-photon imaging of HER2 expression in tumors. J Nucl Med 2006;47(3):512-19
   PubMed Web of Science ®Google Scholar
• Cortez-Retamozo V, Lahoutte T, Caveliers V, et al. 99mTc-labeled nanobodies: a new type of targeted probes for imaging antigen expression. Curr Radiopharm 2008;1(1):37-41
   Google Scholar
• Tijink BM, Perk LR, Budde M, et al. (124)I-L19-SIP for immuno-PET imaging of tumour vasculature and guidance of (131)I-L19-SIP radioimmunotherapy. Eur J Nucl Med Mol Imaging 2009;36(8):1235-44
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Hackel BJ, Kimura RH, Gambhir SS. Use of (64)Cu-labeled fibronectin domain with EGFR-overexpressing tumor xenograft: molecular imaging. Radiology 2012;263(1):179-88
   PubMed Web of Science ®Google Scholar
• Olafsen T, Sirk SJ, Olma S, et al. ImmunoPET using engineered antibody fragments: fluorine-18 labeled diabodies for same-day imaging. Tumour Biol 2012;33(3):669-77
   PubMed Web of Science ®Google Scholar
• Heskamp S, Laverman P, Rosik D, et al. Imaging of human epidermal growth factor receptor type 2 expression with 18F-labeled affibody molecule ZHER2:2395 in a mouse model for ovarian cancer. J Nucl Med 2012;53(1):146-53
   PubMed Web of Science ®Google Scholar
• 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(16):4165-77
   PubMed Web of Science ®Google Scholar
• Delaloye B, Bischof-Delaloye A, Buchegger F, et al. Detection of colorectal carcinoma by emission-computerized tomography after injection of 123I-labeled Fab or F(ab')2 fragments from monoclonal anti-carcinoembryonic antigen antibodies. J Clin Invest 1986;77(1):301-11
   PubMed Web of Science ®Google Scholar
• Goldenberg DM, Goldenberg H, Sharkey RM, et al. Clinical studies of cancer radioimmunodetection with carcinoembryonic antigen monoclonal antibody fragments labeled with 123I or 99mTc. Cancer Res 1990;50(3 Suppl):909s-21s
   PubMed Web of Science ®Google Scholar
• Wong JY, Chu DZ, Williams LE, et al. Pilot trial evaluating an 123I-labeled 80-kilodalton engineered anticarcinoembryonic antigen antibody fragment (cT84.66 minibody) in patients with colorectal cancer. Clin Cancer Res 2004;10(15):5014-21
   PubMed Web of Science ®Google Scholar
• Baum RP, Prasad V, Müller D, et al. Molecular imaging of HER2-expressing malignant tumors in breast cancer patients using synthetic 111In- or 68Ga-Labeled affibody molecules. J Nucl Med 2010;51(6):892-7
   PubMed Web of Science ®Google Scholar
• 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; Epub ahead of print
   PubMed Web of Science ®Google Scholar
• Knowles SM, Wu AM. Advances in immuno-positron emission tomography: antibodies for molecular imaging in oncology. J Clin Oncol 2012;30(31):3884-92
   PubMed Web of Science ®Google Scholar
• Ghetie V, Hubbard JG, Kim JK, et al. Abnormally short serum half-lives of IgG in beta 2-microglobulin-deficient mice. Eur J Immunol 1996;26(3):690-6
   PubMed Web of Science ®Google Scholar
• Ward ES, Zhou J, Ghetie V, Ober RJ. Evidence to support the cellular mechanism involved in serum IgG homeostasis in humans. Int Immunol 2003;15(2):187-95
   PubMed Web of Science ®Google Scholar
• Ober RJ, Martinez C, Vaccaro C, et al. Visualizing the site and dynamics of IgG salvage by the MHC class I-related receptor. FcRn. J Immunol 2004;172(4):2021-9
   PubMed Web of Science ®Google Scholar
• Fang J, Nakamura H, Maeda H. The EPR effect: unique features 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
   PubMed Web of Science ®Google Scholar
• Hamers-Casterman C, Atarhouch T, Muyldermans S, et al. Naturally occurring antibodies devoid of light chains. Nature 1993;363(6428):446-8
   PubMed Web of Science ®Google Scholar
• Arbabi Ghahroudi M, Desmyter A, Wyns L, et al. Selection and identification of single domain antibody fragments from camel heavy-chain antibodies. FEBS Lett 1997;414(3):521-6
   PubMed Web of Science ®Google Scholar
• Muyldermans S, Baral TN, Retamozzo VC, et al. Camelid immunoglobulins and nanobody technology. Vet Immunol Immunopathol 2009;128(1-3):178-83
   PubMed Web of Science ®Google Scholar
• Nuttall SD. Overview and discovery of IgNARs and generation of VNARs. Methods Mol Biol 2012;911:27-36
   PubMedGoogle Scholar
• Vaneycken I, D'Huyvetter M, Hernot S, et al. Immuno-imaging using nanobodies. Curr Opin Biotechnol 2011;22(6):877-81
   PubMed Web of Science ®Google Scholar
• Devoogdt N, Xavier C, Hernot S, et al. Molecular imaging using Nanobodies: a case study. Methods Mol Biol 2012;911:559-67
   PubMedGoogle Scholar
• Holliger P, Hudson PJ. Engineered antibody fragments and the rise of single domains. Nat Biotechnol 2005;23(9):1126-36
   PubMed Web of Science ®Google Scholar
• Cortez-Retamozo V, Lauwereys M, Hassanzadeh Gh G, et al. Efficient tumor targeting by single-domain antibody fragments of camels. Int J Cancer 2002;98(3):456-62
   PubMed Web of Science ®Google Scholar
• Van Bockstaele F, Holz JB, Revets H. The development of nanobodies for therapeutic applications. Curr Opin Investig Drugs 2009;10(11):1212-24
   PubMed Web of Science ®Google Scholar
• Vincke C, Loris R, Saerens D, 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Binz HK, Stumpp MT, Forrer P, et al. Designing repeat proteins: well-expressed, soluble and stable proteins from combinatorial libraries of consensus ankyrin repeat proteins. J Mol Biol 2003;332(2):489-503
   PubMed Web of Science ®Google Scholar
• Wikman M, Steffen AC, Gunneriusson E, et al. Selection and characterization of HER2/neu-binding affibody ligands. Protein Eng Des Sel 2004;17(5):455-62
   PubMed Web of Science ®Google Scholar
• Hansson M, Ringdahl J, Robert A, et al. An in vitro selected binding protein (affibody) shows conformation-dependent recognition of the respiratory syncytial virus (RSV) G protein. Immunotechnology 1999;4(3-4):237-52
   PubMedGoogle Scholar
• Els Conrath K, Lauwereys M, Wyns L, Muyldermans S. Camel single-domain antibodies as modular building units in bispecific and bivalent antibody constructs. J Biol Chem 2001;276(10):7346-50
   PubMed Web of Science ®Google Scholar
• Steffen AC, Wikman M, Tolmachev V, et al. In vitro characterization of a bivalent anti-HER-2 affibody with potential for radionuclide-based diagnostics. Cancer Biother Radiopharm 2005;20(3):239-48
   PubMed Web of Science ®Google Scholar
• Friedrich K, Hanauer JR, Prufer S, et al. DARPin-targeting of measles virus: unique bispecificity, effective oncolysis, and enhanced safety. Mol Ther 2013;21(4):849-59
   PubMed Web of Science ®Google Scholar
• Emanuel SL, Engle LJ, Chao G, et al. A fibronectin scaffold approach to bispecific inhibitors of epidermal growth factor receptor and insulin-like growth factor-I receptor. MAbs 2011;3(1):38-48
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Huang L, Gainkam LO, Caveliers V, et al. SPECT imaging with 99mTc-labeled EGFR-specific nanobody for in vivo monitoring of EGFR expression. Mol Imaging Biol 2008;10(3):167-75
   PubMed Web of Science ®Google Scholar
• Gainkam LO, Keyaerts M, Caveliers V, et al. Correlation between epidermal growth factor receptor-specific nanobody uptake and tumor burden: a tool for noninvasive monitoring of tumor response to therapy. Mol Imaging Biol 2011;13(5):940-8
   PubMed Web of Science ®Google Scholar
• Tchouate 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
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• 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(2):254-64
   PubMed Web of Science ®Google Scholar
• Oliveira S, van Dongen GA, Stigter-van Walsum M, et al. Rapid visualization of human tumor xenografts through optical imaging with a near-infrared fluorescent anti-epidermal growth factor receptor nanobody. Mol Imaging 2012;11(1):33-46
   PubMed Web of Science ®Google Scholar
• Desmyter A, Decanniere K, Muyldermans S, Wyns L. Antigen specificity and high affinity binding provided by one single loop of a camel single-domain antibody. J Biol Chem 2001;276(28):26285-90
   PubMed Web of Science ®Google Scholar
• Rasmussen SG, Choi HJ, Fung JJ, et al. Structure of a nanobody-stabilized active state of the beta(2) adrenoceptor. Nature 2011;469(7329):175-80
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Dumoulin M, Conrath K, Van Meirhaeghe A, et al. Single-domain antibody fragments with high conformational stability. Protein Sci 2002;11(3):500-15
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• van der Linden RH, Frenken LG, de Geus B, et al. Comparison of physical chemical properties of llama VHH antibody fragments and mouse monoclonal antibodies. Biochim Biophys Acta 1999;1431(1):37-46
   PubMed Web of Science ®Google Scholar
• Van de Broek B, Devoogdt N, D'Hollander A, et al. Specific cell targeting with nanobody conjugated branched gold nanoparticles for photothermal therapy. ACS Nano 2011;5(6):4319-28
   PubMed Web of Science ®Google Scholar
• Xavier C, Devoogdt N, Hernot S, et al. Site-specific labeling of his-tagged Nanobodies with (9)(9)mTc: a practical guide. Methods Mol Biol 2012;911:485-90
   PubMedGoogle Scholar
• Weissleder R, Ntziachristos V. Shedding light onto live molecular targets. Nat Med 2003;9(1):123-8
   PubMed Web of Science ®Google Scholar
• Behr TM, Goldenberg DM, Becker W. Reducing the renal uptake of radiolabeled antibody fragments and peptides for diagnosis and therapy: present status, future prospects and limitations. Eur J Nucl Med 1998;25(2):201-12
   PubMedGoogle Scholar
• Pruszynski M, Koumarianou E, Vaidyanathan G, et al. Targeting breast carcinoma with radioiodinated anti-HER2 Nanobody. Nucl Med Biol 2013;40(1):52-9
   PubMed Web of Science ®Google Scholar
• Fani M, Andre JP, Maecke HR. 68Ga-PET: a powerful generator-based alternative to cyclotron-based PET radiopharmaceuticals. Contrast Media Mol Imaging 2008;3(2):67-77
   PubMed Web of Science ®Google Scholar
• Abulrob A, Sprong H, Van Bergen en Henegouwen P, Stanimirovic D. The blood-brain barrier transmigrating single domain antibody: mechanisms of transport and antigenic epitopes in human brain endothelial cells. J Neurochem 2005;95(4):1201-14
   PubMed Web of Science ®Google Scholar
• Pardridge WM. Drug transport across the blood-brain barrier. J Cereb Blood Flow Metab 2012;32(11):1959-72
   PubMed Web of Science ®Google Scholar
• Muruganandam A, Tanha J, Narang S, Stanimirovic D. Selection of phage-displayed llama single-domain antibodies that transmigrate across human blood-brain barrier endothelium. Faseb J 2002;16(2):240-2
   PubMed Web of Science ®Google Scholar
• Caljon G, Caveliers V, Lahoutte T, et al. Using microdialysis to analyse the passage of monovalent nanobodies through the blood-brain barrier. Br J Pharmacol 2012;165(7):2341-53
   PubMed Web of Science ®Google Scholar
• Nabuurs RJ, Rutgers KS, Welling MM, et al. In vivo detection of amyloid-beta deposits using heavy chain antibody fragments in a transgenic mouse model for Alzheimer's disease. PLoS One 2012;7(6):e38284
   PubMed Web of Science ®Google Scholar
• Li T, Bourgeois JP, Celli S, et al. Cell-penetrating anti-GFAP VHH and corresponding fluorescent fusion protein VHH-GFP spontaneously cross the blood-brain barrier and specifically recognize astrocytes: application to brain imaging. FASEB J 2012;26(10):3969-79
   PubMed Web of Science ®Google Scholar
• Rutgers KS, Nabuurs RJ, van den Berg SA, et al. Transmigration of beta amyloid specific heavy chain antibody fragments across the in vitro blood-brain barrier. Neuroscience 2011;190:37-42
   PubMed Web of Science ®Google Scholar
• Jones DR, Taylor WA, Bate C, et al. A camelid anti-PrP antibody abrogates PrP replication in prion-permissive neuroblastoma cell lines. PLoS One 2010;5(3):e9804
   PubMed Web of Science ®Google Scholar
• Iqbal U, Albaghdadi H, Luo Y, et al. Molecular imaging of glioblastoma multiforme using anti-insulin-like growth factor-binding protein-7 single-domain antibodies. Br J Cancer 2010;103(10):1606-16
   PubMed Web of Science ®Google Scholar
• Iqbal U, Trojahn U, Albaghdadi H, et al. Kinetic analysis of novel mono- and multivalent VHH-fragments and their application for molecular imaging of brain tumours. Br J Pharmacol 2010;160(4):1016-28
   PubMed Web of Science ®Google Scholar
• Harmsen MM, Van Solt CB, Fijten HP, Van Setten MC. Prolonged in vivo residence times of llama single-domain antibody fragments in pigs by binding to porcine immunoglobulins. Vaccine 2005;23(41):4926-34
   PubMed Web of Science ®Google Scholar
• Coppieters K, Dreier T, Silence K, et al. Formatted anti-tumor necrosis factor alpha VHH proteins derived from camelids show superior potency and targeting to inflamed joints in a murine model of collagen-induced arthritis. Arthritis Rheum 2006;54(6):1856-66
   PubMed Web of Science ®Google Scholar
• Vugmeyster Y, Entrican CA, Joyce AP, et al. Pharmacokinetic, biodistribution, and biophysical profiles of TNF nanobodies conjugated to linear or branched poly(ethylene glycol). Bioconjug Chem 2012;23(7):1452-62
   PubMed Web of Science ®Google Scholar
• 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(5):782-9
   PubMed Web of Science ®Google Scholar
• 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;
   PubMed Web of Science ®Google Scholar
• Vosjan MJ, Perk LR, Roovers RC, et al. Facile labelling 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
   PubMed Web of Science ®Google Scholar
• Bell A, Wang ZJ, Arbabi-Ghahroudi M, et al. Differential tumor-targeting abilities of three single-domain antibody formats. Cancer Lett 2010;289(1):81-90
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Tijink BM, Laeremans T, Budde M, et al. Improved tumor targeting of anti-epidermal growth factor receptor Nanobodies through albumin binding: taking advantage of modular Nanobody technology. Mol Cancer Ther 2008;7(8):2288-97
   PubMed Web of Science ®Google Scholar
• Hernot S, Unnikrishnan S, Du Z, et al. Nanobody-coupled microbubbles as novel molecular tracer. J Control Release 2012;158(2):346-53
   PubMed Web of Science ®Google Scholar
• Ahlgren S, Wallberg H, Tran TA, et al. Targeting of HER2-expressing tumors with a site-specifically 99mTc-labeled recombinant affibody molecule, ZHER2:2395, with C-terminally engineered cysteine. J Nucl Med 2009;50(5):781-9
   PubMed Web of Science ®Google Scholar
• Willuda J, Kubetzko S, Waibel R, et al. Tumor targeting of mono-, di-, and tetravalent anti-p185(HER-2) miniantibodies multimerized by self-associating peptides. J Biol Chem 2001;276(17):14385-92
   PubMed Web of Science ®Google Scholar
• Tang Y, Scollard D, Chen P, et al. Imaging of HER2/neu expression in BT-474 human breast cancer xenografts in athymic mice using [(99m)Tc]-HYNIC-trastuzumab (Herceptin) Fab fragments. Nucl Med Commun 2005;26(5):427-32
   PubMed Web of Science ®Google Scholar
• Olafsen T, Tan GJ, Cheung CW, et al. Characterization of engineered anti-p185HER-2 (scFv-CH3)2 antibody fragments (minibodies) for tumor targeting. Protein Eng Des Sel 2004;17(4):315-23
   PubMed Web of Science ®Google Scholar
• Smith-Jones PM, Solit DB, Akhurst T, et al. Imaging the pharmacodynamics of HER2 degradation in response to Hsp90 inhibitors. Nat Biotechnol 2004;22(6):701-6
   PubMed Web of Science ®Google Scholar
• Dijkers EC, Kosterink JG, Rademaker AP, et al. Development and characterization of clinical-grade 89Zr-trastuzumab for HER2/neu immunoPET imaging. J Nucl Med 2009;50(6):974-81
   PubMed Web of Science ®Google Scholar