2,144
Views
20
CrossRef citations to date
0
Altmetric
Report

Chemically-defined camelid antibody bioconjugate for the magnetic resonance imaging of Alzheimer's disease

, , , , , , , , , , ORCID Icon, & ORCID Icon show all
Pages 1016-1027 | Received 14 Feb 2017, Accepted 12 Jun 2017, Published online: 31 Jul 2017

References

  • Hermanson GT. In: Bioconjugate techniques. Antibody modification and conjugation. Academic Press; 2013. p. 783-823.
  • Beck A, Goetsch L, Dumontet C, Corvaia N. Strategies and challenges for the next generation of antibody drug conjugates. Nat Rev Drug Discov 2017; 16:315-37; PMID:28303026; https://doi.org/10.1038/nrd.2016.268
  • Behrens CR, Liu B. Methods for site-specific drug conjugation to antibodies. mAbs 2014; 6:46-53; PMID:24135651; https://doi.org/10.4161/mabs.26632
  • Krall N, da Cruz FP, Boutureira O, Bernardes GJL. Site-selective protein-modification chemistry for basic biology and drug development. Nat Chem 2016; 8:103-13; PMID:26791892; https://doi.org/10.1038/nchem.2393
  • Massa S, Xavier C, Muyldermans S, Devoogdt N. Emerging site-specific bioconjugation strategies for radioimmunotracer development. Expert Opin Drug Deliv 2016; 13:1149-63; PMID:27116898; https://doi.org/10.1080/17425247.2016.1178235
  • Panowski S, Bhakta S, Raab H, Polakis P, Junutula JR. Site-specific antibody drug conjugates for cancer therapy. mAbs 2014; 6:34-45; PMID:24423619; https://doi.org/10.4161/mabs.27022
  • Spicer CD, Davis BG. Selective chemical protein modification. Nat Commun 2014; 5:4740; PMID:25190082; https://doi.org/10.1038/ncomms5740
  • Kim CH, Axup JY, Schultz PG. Protein conjugation with genetically encoded unnatural amino acids. Curr Opin Chem Biol 2013; 17:412-9; PMID:23664497; https://doi.org/10.1016/j.cbpa.2013.04.017
  • Tian F, Lu Y, Manibusan A, Sellers A, Tran H, Sun Y, Phuong T, Barnett R, Hehli B, Song F, et al. A general approach to site-specific antibody drug conjugates. Proc Natl Acad Sci U S A 2014; 111:1766-71; PMID:24443552; https://doi.org/10.1073/pnas.1321237111
  • Junutula JR, Raab H, Clark S, Bhakta S, Leipold DD, Weir S, Chen Y, Simpson M, Tsai SP, Dennis MS, et al. Site-specific conjugation of a cytotoxic drug to an antibody improves the therapeutic index. Nat Biotechnol 2008; 26:925-32; PMID:18641636; https://doi.org/10.1038/nbt.1480
  • Albrecht H, Burke PA, Natarajan A, Xiong CY, Kalicinsky M, DeNardo GL, DeNardo SJ. Production of soluble ScFvs with C-terminal-free thiol for site-specific conjugation or stable dimeric ScFvs on demand. Bioconjug Chem 2004; 15:16-26; PMID:14733579; https://doi.org/10.1021/bc030018+
  • Olafsen T, Cheung CW, Yazaki PJ, Li L, Sundaresan G, Gambhir SS, Sherman MA, Williams LE, Shively JE, Raubitschek AA, et al. Covalent disulfide-linked anti-CEA diabody allows site-specific conjugation and radiolabeling for tumor targeting applications. Protein Eng Des Sel 2004; 17:21-7; PMID:14985534; https://doi.org/10.1093/protein/gzh009
  • Mume E, Orlova A, Larsson B, Nilsson AS, Nilsson FY, Sjoberg S, Tolmachev V. Evaluation of ((4-hydroxyphenyl)ethyl)maleimide for site-specific radiobromination of anti-HER2 affibody. Bioconjug Chem 2005; 16:1547-55; PMID:16287254; https://doi.org/10.1021/bc050056o
  • Ahlgren S, Orlova A, Rosik D, Sandstrom M, Sjoberg A, Baastrup B, Widmark O, Fant G, Feldwisch J, Tolmachev V. Evaluation of maleimide derivative of DOTA for site-specific labeling of recombinant affibody molecules. Bioconjug Chem 2008; 19:235-43; PMID:18163536; https://doi.org/10.1021/bc700307y
  • Lundberg E, Hoiden-Guthenberg I, Larsson B, Uhlen M, Graslund T. Site-specifically conjugated anti-HER2 Affibody molecules as one-step reagents for target expression analyses on cells and xenograft samples. J Immunol Methods 2007; 319:53-63; PMID:17196217; https://doi.org/10.1016/j.jim.2006.10.013
  • Sirk SJ, Olafsen T, Barat B, Bauer KB, Wu AM. Site-specific, thiol-mediated conjugation of fluorescent probes to cysteine-modified diabodies targeting CD20 or HER2. Bioconjug Chem 2008; 19:2527-34; PMID:19053310; https://doi.org/10.1021/bc800113v
  • Massa S, Xavier C, De Vos J, Caveliers V, Lahoutte T, Muyldermans S, Devoogdt N. Site-specific labeling of cysteine-tagged camelid single-domain antibody-fragments for use in molecular imaging. Bioconjug Chem 2014; 25:979-88; PMID:24815083; https://doi.org/10.1021/bc500111t
  • Hamers-Casterman C, Atarhouch T, Muyldermans S, Robinson G, Hamers C, Songa EB, Bendahman N, Hamers R. Naturally occurring antibodies devoid of light chains. Nature 1993; 363:446-8; PMID:8502296; https://doi.org/10.1038/363446a0
  • 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; 13:1149-60; PMID:23675652; https://doi.org/10.1517/14712598.2013.800478
  • Harmsen MM, De Haard HJ. Properties, production, and applications of camelid single-domain antibody fragments. Appl Microbiol Biotechnol 2007; 77:13-22; PMID:17704915; https://doi.org/10.1007/s00253-007-1142-2
  • De Genst E, Silence K, Decanniere K, Conrath K, Loris R, Kinne R, Muyldermans S, Wyns L. Molecular basis for the preferential cleft recognition by dromedary heavy-chain antibodies. Proc Natl Acad Sci U S A 2006; 103:4586-91; PMID:16537393; https://doi.org/10.1073/pnas.0505379103
  • Lafaye P, Achour I, England P, Duyckaerts C, Rougeon F. Single-domain antibodies recognize selectively small oligomeric forms of amyloid beta, prevent Abeta-induced neurotoxicity and inhibit fibril formation. Mol Immunol 2009; 46:695-704; PMID:18930548; https://doi.org/10.1016/j.molimm.2008.09.008
  • Perruchini C, Pecorari F, Bourgeois JP, Duyckaerts C, Rougeon F, Lafaye P. Llama VHH antibody fragments against GFAP: Better diffusion in fixed tissues than classical monoclonal antibodies. Acta Neuropathol 2009; 118:685-95; PMID:19597828; https://doi.org/10.1007/s00401-009-0572-6
  • Li Z, Krippendorff BF, Sharma S, Walz AC, Lave T, Shah DK. Influence of molecular size on tissue distribution of antibody fragments. mAbs, 2016; 8:113-9; PMID:25484055; https://doi.org/10.1080/19420862.2015.1111497
  • Baral TN, Magez S, Stijlemans B, Conrath K, Vanhollebeke B, Pays E, Muyldermans S, De Baetselier P. Experimental therapy of African trypanosomiasis with a nanobody-conjugated human trypanolytic factor. Nat Med 2006; 12:580-4; PMID:16604085; https://doi.org/10.1038/nm1395
  • Achour I, Cavelier P, Tichit M, Bouchier C, Lafaye P, Rougeon F. Tetrameric and homodimeric camelid IgGs originate from the same IgH locus. J Immunol 2008; 181:2001-9; PMID:18641337; https://doi.org/10.4049/jimmunol.181.3.2001
  • Vincke C, Loris R, Saerens D, Martinez-Rodriguez S, Muyldermans S, Conrath K. General strategy to humanize a camelid single-domain antibody and identification of a universal humanized nanobody scaffold. J Biol Chem 2009; 284:3273-84; PMID:19010777; https://doi.org/10.1074/jbc.M806889200
  • David MA, Jones DR, Tayebi M. Potential candidate camelid antibodies for the treatment of protein-misfolding diseases. J Neuroimmunol 2014; 272:76-85; PMID:24864011; https://doi.org/10.1016/j.jneuroim.2014.05.001
  • Li T, Bourgeois JP, Celli S, Glacial F, Le Sourd AM, Mecheri S, Weksler B, Romero I, Couraud PO, Rougeon F, 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; 26:3969-79; PMID:22730440; https://doi.org/10.1096/fj.11-201384
  • Nabuurs RJ, Rutgers KS, Welling MM, Metaxas A, de Backer ME, Rotman M, Bacskai BJ, van Buchem MA, van der Maarel SM, van der Weerd L. 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:e38284; PMID:22675537; https://doi.org/10.1371/journal.pone.0038284
  • Rutgers KS, Nabuurs RJ, van den Berg SA, Schenk GJ, Rotman M, Verrips CT, van Duinen SG, Maat-Schieman ML, van Buchem MA, de Boer AG, et al. Transmigration of beta amyloid specific heavy chain antibody fragments across the in vitro blood-brain barrier. Neuroscience 2011; 190:37-42; PMID:21683126; https://doi.org/10.1016/j.neuroscience.2011.05.076
  • Rissiek B, Koch-Nolte F, Magnus T. Nanobodies as modulators of inflammation: Potential applications for acute brain injury. Front Cell Neurosci 2014; 8:344; PMID:25374510; https://doi.org/10.3389/fncel.2014.00344
  • Klunk WE, Engler H, Nordberg A, Wang Y, Blomqvist G, Holt DP, Bergstrom M, Savitcheva I, Huang GF, Estrada S, et al. Imaging brain amyloid in Alzheimer's disease with Pittsburgh compound-B. Ann Neurol 2004; 55:306-19; PMID:14991808; https://doi.org/10.1002/ana.20009
  • Clark CM, Schneider JA, Bedell BJ, Beach TG, Bilker WB, Mintun MA, Pontecorvo MJ, Hefti F, Carpenter AP, Flitter ML, et al. Use of florbetapir-PET for imaging beta-amyloid pathology. JAMA 2011; 305:275-83; PMID:21245183; https://doi.org/10.1001/jama.2010.2008
  • Villemagne VL, Furumoto S, Fodero-Tavoletti MT, Mulligan RS, Hodges J, Harada R, Yates P, Piguet O, Pejoska S, Dore V, et al. In vivo evaluation of a novel tau imaging tracer for Alzheimer's disease. Eur J Nucl Med Mol Imag 2014; 41:816-26; PMID:24514874; https://doi.org/10.1007/s00259-013-2681-7
  • Maruyama M, Shimada H, Suhara T, Shinotoh H, Ji B, Maeda J, Zhang MR, Trojanowski JQ, Lee VM, Ono M, et al. Imaging of tau pathology in a tauopathy mouse model and in Alzheimer patients compared to normal controls. Neuron 2013; 79:1094-108; PMID:24050400; https://doi.org/10.1016/j.neuron.2013.07.037
  • Hickey JL, Lim S, Hayne DJ, Paterson BM, White JM, Villemagne VL, Roselt P, Binns D, Cullinane C, Jeffery CM, et al. Diagnostic imaging agents for Alzheimer's disease: Copper radiopharmaceuticals that target Abeta plaques. J Am Chem Soc 2013; 135:16120-32; PMID:24070589; https://doi.org/10.1021/ja4057807
  • Ono M, Saji H. Recent advances in molecular imaging probes for beta-amyloid plaques. Med Chem Comm 2015; 6:391-402; https://doi.org/10.1039/C4MD00365A
  • Teipel S, Drzezga A, Grothe MJ, Barthel H, Chetelat G, Schuff N, Skudlarski P, Cavedo E, Frisoni GB, Hoffmann W, et al. Multimodal imaging in Alzheimer's disease: Validity and usefulness for early detection. Lancet Neurol 2015; 14:1037-53; PMID:26318837; https://doi.org/10.1016/S1474-4422(15)00093-9
  • Santin MD, Debeir T, Bridal SL, Rooney T, Dhenain M. Fast in vivo imaging of amyloid plaques using mu-MRI Gd-staining combined with ultrasound-induced blood-brain barrier opening. NeuroImage 2013; 79:288-94; PMID:23660031; https://doi.org/10.1016/j.neuroimage.2013.04.106
  • Ramakrishnan M, Wengenack TM, Kandimalla KK, Curran GL, Gilles EJ, Ramirez-Alvarado M, Lin J, Garwood M, Jack CR, Jr., Poduslo JF. Selective contrast enhancement of individual Alzheimer's disease amyloid plaques using a polyamine and Gd-DOTA conjugated antibody fragment against fibrillar Abeta42 for magnetic resonance molecular imaging. Pharm Res 2008; 25:1861-72; PMID:18443900; https://doi.org/10.1007/s11095-008-9600-9
  • Sigurdsson EM, Wadghiri YZ, Mosconi L, Blind JA, Knudsen E, Asuni A, Scholtzova H, Tsui WH, Li Y, Sadowski M, et al. A non-toxic ligand for voxel-based MRI analysis of plaques in AD transgenic mice. Neurobiol Aging 2008; 29:836-47; PMID:17291630; https://doi.org/10.1016/j.neurobiolaging.2006.12.018
  • Wadghiri YZ, Sigurdsson EM, Sadowski M, Elliott JI, Li Y, Scholtzova H, Tang CY, Aguinaldo G, Pappolla M, Duff K, et al. Detection of Alzheimer's amyloid in transgenic mice using magnetic resonance microimaging. Magn Reson Med 2003; 50:293-302; PMID:12876705; https://doi.org/10.1002/mrm.10529
  • Yang J, Wadghiri YZ, Hoang DM, Tsui W, Sun Y, Chung E, Li Y, Wang A, de Leon M, Wisniewski T. Detection of amyloid plaques targeted by USPIO-Abeta1-42 in Alzheimer's disease transgenic mice using magnetic resonance microimaging. NeuroImage 2011; 55:1600-9; PMID:21255656; https://doi.org/10.1016/j.neuroimage.2011.01.023
  • Li T, Vandesquille M, Koukouli F, Dudeffant C, Youssef I, Lenormand P, Ganneau C, Maskos U, Czech C, Grueninger F, et al. Camelid single-domain antibodies: A versatile tool for in vivo imaging of extracellular and intracellular brain targets. J Control Release 2016; 243:1-10; PMID:27671875; https://doi.org/10.1016/j.jconrel.2016.09.019
  • Richards JG, Higgins GA, Ouagazzal AM, Ozmen L, Kew JN, Bohrmann B, Malherbe P, Brockhaus M, Loetscher H, Czech C, et al. PS2APP transgenic mice, coexpressing hPS2mut and hAPPswe, show age-related cognitive deficits associated with discrete brain amyloid deposition and inflammation. J Neurosci 2003; 23:8989-9003; PMID:14523101.
  • Cuatrecasas P, Parikh I. Adsorbents for affinity chromatography. Use of N-hydroxysuccinimide esters of agarose. Biochemistry 1972; 11:2291-9; PMID:5028497; https://doi.org/10.1021/bi00762a013
  • Dumoulin M, Conrath K, Van Meirhaeghe A, Meersman F, Heremans K, Frenken LGJ, Muyldermans S, Wyns L, Matagne A. Single-domain antibody fragments with high conformational stability. Protein Sci 2002; 11:500-15; PMID:11847273; https://doi.org/10.1110/ps.34602
  • Olichon A, Schweizer D, Muyldermans S, de Marco A. Heating as a rapid purification method for recovering correctly-folded thermotolerant VH and VHH domains. BMC Biotechnol 2007; 7:7; PMID:17257422; https://doi.org/10.1186/1472-6750-7-7
  • Papini A, Rudolph S, Siglmuller G, Musiol HJ, Gohring W, Moroder L. Alkylation of histidine with maleimido-compounds. Int J Pept Protein Res 1992; 39:348-55; PMID:1428524; https://doi.org/10.1111/j.1399-3011.1992.tb01594.x
  • Paulech J, Solis N, Cordwell SJ. Characterization of reaction conditions providing rapid and specific cysteine alkylation for peptide-based mass spectrometry. Biochim Biophys Acta 2013; 1834:372-9; PMID:22910378; https://doi.org/10.1016/j.bbapap.2012.08.002
  • Selkoe DJ. Toward a comprehensive theory for Alzheimer's disease. Hypothesis: Alzheimer's disease is caused by the cerebral accumulation and cytotoxicity of amyloid beta-protein. Ann N Y Acad Sci 2000; 924:17-25; PMID:11193794; https://doi.org/10.1111/j.1749-6632.2000.tb05554.x
  • Caravan P, Ellison JJ, McMurry TJ, Lauffer RB. Gadolinium(III) chelates as MRI contrast agents: Structure, dynamics, and applications. Chem Rev 1999; 99:2293-352; PMID:11749483; https://doi.org/10.1021/cr980440x
  • Debie P, Van Quathem J, Hansen I, Bala G, Massa S, Devoogdt N, Xavier C, Hernot S. Effect of dye and conjugation chemistry on the biodistribution profile of near-infrared-labeled nanobodies as tracers for image-guided surgery. Mol Pharm 2017; 14:1145-53; PMID:28245129; https://doi.org/10.1021/acs.molpharmaceut.6b01053
  • Berzofsky JA, Berkover IJ. In: Fundamental immunology. Antigen-antibody interaction. Raven Press; 1984. p. 595-644.
  • Beck A, Wagner-Rousset E, Ayoub D, Van Dorsselaer A, Sanglier-Cianferani S. Characterization of therapeutic antibodies and related products. Anal Chem 2013; 85:715-36; PMID:23134362; https://doi.org/10.1021/ac3032355
  • Wakankar A, Chen Y, Gokarn Y, Jacobson FS. Analytical methods for physicochemical characterization of antibody drug conjugates. mAbs 2011; 3:161-72; PMID:21441786; https://doi.org/10.4161/mabs.3.2.14960
  • Gronwall C, Sjoberg A, Ramstrom M, Hoiden-Guthenberg I, Hober S, Jonasson P, Stahl S. Affibody-mediated transferrin depletion for proteomics applications. Biotechnol J 2007; 2:1389-98; PMID:17639529; https://doi.org/10.1002/biot.200700053
  • Habicht G, Haupt C, Friedrich RP, Hortschansky P, Sachse C, Meinhardt J, Wieligmann K, Gellermann GP, Brodhun M, Gotz J, et al. Directed selection of a conformational antibody domain that prevents mature amyloid fibril formation by stabilizing Abeta protofibrils. Proc Natl Acad Sci U S A 2007; 104:19232-7; PMID:18042730; https://doi.org/10.1073/pnas.0703793104
  • Luheshi LM, Hoyer W, de Barros TP, van Dijk Hard I, Brorsson AC, Macao B, Persson C, Crowther DC, Lomas DA, Stahl S, et al. Sequestration of the Abeta peptide prevents toxicity and promotes degradation in vivo. PLoS Biol 2010; 8:e1000334; PMID:20305716; https://doi.org/10.1371/journal.pbio.1000334
  • Morgado I, Wieligmann K, Bereza M, Ronicke R, Meinhardt K, Annamalai K, Baumann M, Wacker J, Hortschansky P, Malesevic M, et al. Molecular basis of beta-amyloid oligomer recognition with a conformational antibody fragment. Proc Natl Acad Sci U S A 2012; 109:12503-8; PMID:22814377; https://doi.org/10.1073/pnas.1206433109
  • Pain C, Dumont J, Dumoulin M. Camelid single-domain antibody fragments: Uses and prospects to investigate protein misfolding and aggregation, and to treat diseases associated with these phenomena. Biochimie 2015; 111:82-106; PMID:25656912; https://doi.org/10.1016/j.biochi.2015.01.012
  • Rotman M, Welling MM, van den Boogaard ML, Moursel LG, van der Graaf LM, van Buchem MA, van der Maarel SM, van der Weerd L. Fusion of hIgG1-Fc to 111In-anti-amyloid single domain antibody fragment VHH-pa2H prolongs blood residential time in APP/PS1 mice but does not increase brain uptake. Nucl Med Biol 2015; 42:695-702; PMID:25960433; https://doi.org/10.1016/j.nucmedbio.2015.03.003
  • Petiet A, Delatour B, Dhenain M. Models of neurodegenerative disease - Alzheimer's anatomical and amyloid plaque imaging. Methods Mol Biol 2011; 771:293-308; PMID:21874485; https://doi.org/10.1007/978-1-61779-219-9_16
  • Jack CR Jr, Wengenack TM, Reyes DA, Garwood M, Curran GL, Borowski BJ, Lin J, Preboske GM, Holasek SS, Adriany G, et al. In vivo magnetic resonance microimaging of individual amyloid plaques in Alzheimer's transgenic mice. J Neurosci 2005; 25:10041-8; PMID:16251453; https://doi.org/10.1523/JNEUROSCI.2588-05.2005
  • Nabuurs RJ, Natte R, de Ronde FM, Hegeman-Kleinn I, Dijkstra J, van Duinen SG, Webb AG, Rozemuller AJ, van Buchem MA, van der Weerd L. MR microscopy of human amyloid-beta deposits: Characterization of parenchymal amyloid, diffuse plaques, and vascular amyloid. J Alzheimers Dis 2013; 34:1037-49; PMID:23340037; https://doi.org/10.3233/JAD-122215
  • Amet S, Launay-Vacher V, Clement O, Frances C, Tricotel A, Stengel B, Gauvrit JY, Grenier N, Reinhardt G, Janus N, et al. Incidence of nephrogenic systemic fibrosis in patients undergoing dialysis after contrast-enhanced magnetic resonance imaging with gadolinium-based contrast agents the prospective fibrose nephrogenique systemique study. Invest Radiol 2014; 49:109-15; PMID:24169070; https://doi.org/10.1097/RLI.0000000000000000
  • European Medicines Agency. Assessment report for Gadolinium-containing contrast agents. 2010; EMA/740640/2010.
  • Guerbet LLC. Dotarem® (gadoterate meglumine) injection. Medical Imaging Drugs Advisory Committee (MIDAC) - Advisory Committee Briefing Document NDA 204-781. U.S. Food Drug Admin 2013.
  • Saake M, Langner S, Schwenke C, Weibart M, Jansen O, Hosten N, Doerfler A. MRI in multiple sclerosis: An intra-individual, randomized and multicentric comparison of gadobutrol with gadoterate meglumine at 3 T. Eur Radiol 2016; 26:820-8; PMID:26123410; https://doi.org/10.1007/s00330-015-3889-7
  • Petiet A, Santin M, Bertrand A, Wiggins CJ, Petit F, Houitte D, Hantraye P, Benavides J, Debeir T, Rooney T, et al. Gadolinium-staining reveals amyloid plaques in the brain of Alzheimer's transgenic mice. Neurobiol Aging 2012; 33:1533-44; PMID:21531045; https://doi.org/10.1016/j.neurobiolaging.2011.03.009

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.